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Intracellular organelles in the saga of Ca2+ homeostasis: different molecules for different purposes?

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Abstract

An increase in the concentration of cytosolic free Ca2+ is a key component regulating different cellular processes ranging from egg fertilization, active secretion and movement, to cell differentiation and death. The multitude of phenomena modulated by Ca2+, however, do not simply rely on increases/decreases in its concentration, but also on specific timing, shape and sub-cellular localization of its signals that, combined together, provide a huge versatility in Ca2+ signaling. Intracellular organelles and their Ca2+ handling machineries exert key roles in this complex and precise mechanism, and this review will try to depict a map of Ca2+ routes inside cells, highlighting the uniqueness of the different Ca2+ toolkit components and the complexity of the interactions between them.

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Abbreviations

AD:

Alzheimer’s disease

Aeq:

Aequorin

[Ca2+]:

Ca2+ concentration

cADPR:

Cyclic ADP-ribose

CaM:

Calmodulin

CCE:

Capacitative Ca2+ entry

CGN:

cis-Golgi network

CICR:

Ca2+-induced Ca2+ release

CPA:

Cyclopiazonic acid

CRT:

Calreticulin

CSQ:

Calsequestrin

DHPR:

Dihydropyridine receptor

Δψm:

IMM potential

ER:

Endoplasmic reticulum

FAD:

Familial Alzheimer’s disease

FKBP:

FK506-binding protein

GA:

Golgi apparatus

Htt:

Huntingtin

IMM:

Inner mitochondrial membrane

IMS:

Inter-membrane space

INM:

Inner nuclear membrane

IP3 :

Inositol 1,4,5 trisphosphate

IP3R:

IP3 receptor

MAM:

Mitochondria-associated membrane

MCU:

Mitochondrial Ca2+ Uniporter

Mfn2:

Mitofusin2

mPTP:

Mitochondrial permeability transition pore

NAADP:

Nicotinic acid adenine dinucleotide phosphate

NCX:

Na+/Ca2+ exchanger

NE:

Nuclear envelope

NPC:

Nuclear pore complex

OMM:

Outer mitochondrial membrane

ONM:

Outer nuclear membrane

PDI:

Protein-disulfide isomerase

PKA:

Protein kinase A

PLC:

Phospholipase C

PM:

Plasma membrane

PMCA:

Plasma membrane Ca2+ ATPase

PNS:

Perinuclear space

PPAR:

Peroxisome proliferator-activated receptor

PTS1:

Peroxisome-targeting sequence 1

PS:

Presenilin

RyR:

Ryanodine receptor

SERCA:

Sarco-endoplasmic reticulum Ca2+ ATPase

SOCE:

Store-operated Ca2+ entry

SPCA:

Secretory pathway Ca2+ ATPase

SR:

Sarcoplasmic reticulum

STIM:

Stromal interaction molecule

tBHQ:

2,5-di(t-butyl)hydroquinone

TG:

Thapsigargin

TGN:

trans-Golgi network

TPC:

Two pore channels

TpMs:

Trichoplein/mitostatin

UCP:

Uncoupling protein

VDAC:

Voltage-dependent anion channel

References

  1. Catterall WA, Hulme JT, Jiang X, Few WP (2006) Regulation of sodium and calcium channels by signaling complexes. J Recept Signal Transduct Res 26(5–6):577–598

    PubMed  CAS  Google Scholar 

  2. Lewis RS (2007) The molecular choreography of a store-operated calcium channel. Nature 446(7133):284–287

    Article  PubMed  CAS  Google Scholar 

  3. Wang Y, Deng X, Gill DL (2010) Calcium signaling by STIM and Orai: intimate coupling details revealed. Sci Signal 3(148):pe42

    Article  PubMed  CAS  Google Scholar 

  4. Brini M, Carafoli E (2009) Calcium pumps in health and disease. Physiol Rev 89(4):1341–1378

    Article  PubMed  CAS  Google Scholar 

  5. Zhu MX, Ma J, Parrington J, Calcraft PJ, Galione A, Evans AM (2010) Calcium signaling via two-pore channels: local or global, that is the question. Am J Physiol Cell Physiol 298(3):C430–C441

    Article  PubMed  CAS  Google Scholar 

  6. Koch-Nolte F, Haag F, Guse AH, Lund F, Ziegler M (2009) Emerging roles of NAD+ and its metabolites in cell signaling. Sci Signal 2(57):mr1

    Article  PubMed  Google Scholar 

  7. Gorlach A, Klappa P, Kietzmann T (2006) The endoplasmic reticulum: folding, calcium homeostasis, signaling, and redox control. Antioxid Redox Signal 8(9–10):1391–1418

    Article  PubMed  Google Scholar 

  8. Zhang K, Kaufman RJ (2006) The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology 66(2 Suppl 1):S102–S109

    PubMed  CAS  Google Scholar 

  9. Carafoli E (1987) Intracellular calcium homeostasis. Annu Rev Biochem 56:395–433

    Article  PubMed  CAS  Google Scholar 

  10. Lynes EM, Simmen T (2011) Urban planning of the endoplasmic reticulum (ER): how diverse mechanisms segregate the many functions of the ER. Biochim Biophys Acta

  11. Franzini-Armstrong C (2009) Architecture and regulation of the Ca2+ delivery system in muscle cells. Appl Physiol Nutr Metab Physiologie appliquee nutrition et metabolisme 34(3):323–327

    Article  CAS  Google Scholar 

  12. Wray S, Burdyga T (2010) Sarcoplasmic reticulum function in smooth muscle. Physiol Rev 90(1):113–178

    Article  PubMed  CAS  Google Scholar 

  13. Borgese N, Francolini M, Snapp E (2006) Endoplasmic reticulum architecture: structures in flux. Curr Opin Cell Biol 18(4):358–364

    Article  PubMed  CAS  Google Scholar 

  14. Pendin D, McNew JA, Daga A (2011) Balancing ER dynamics: shaping, bending, severing, and mending membranes. Curr Opin Cell Biol 23(4):435–442

    Article  PubMed  CAS  Google Scholar 

  15. Palade GE (1956) The endoplasmic reticulum. J Biophys Biochem Cytol 2(4 Suppl):85–98

    Article  PubMed  CAS  Google Scholar 

  16. Meldolesi J, Pozzan T (1998) The heterogeneity of ER Ca2+ stores has a key role in nonmuscle cell signaling and function. J Cell Biol 142(6):1395–1398

    Article  PubMed  CAS  Google Scholar 

  17. Aulestia FJ, Redondo PC, Rodriguez-Garcia A, Rosado JA, Salido GM, Alonso MT, Garcia-Sancho J (2011) Two distinct calcium pools in the endoplasmic reticulum of HEK-293T cells. Biochem J 435(1):227–235

    Article  PubMed  CAS  Google Scholar 

  18. Blaustein MP, Golovina VA, Song H, Choate J, Lencesova L, Robinson SW, Wier WG (2002) Organization of Ca2+ stores in vascular smooth muscle: functional implications. Novartis Found Symp 246:125–137 (discussion 137–141, 221–227)

    Article  PubMed  CAS  Google Scholar 

  19. Golovina VA, Blaustein MP (1997) Spatially and functionally distinct Ca2+ stores in sarcoplasmic and endoplasmic reticulum. Science 275(5306):1643–1648

    Article  PubMed  CAS  Google Scholar 

  20. Cheek TR, Berridge MJ, Moreton RB, Stauderman KA, Murawsky MM, Bootman MD (1994) Quantal Ca2+ mobilization by ryanodine receptors is due to all-or-none release from functionally discrete intracellular stores. Biochem J 301(Pt 3):879–883

    PubMed  CAS  Google Scholar 

  21. Ohta T, Wakade AR, Yonekubo K, Ito S (2002) Functional relation between caffeine- and muscarine-sensitive Ca2+ stores and no Ca2+ releasing action of cyclic adenosine diphosphate-ribose in guinea-pig adrenal chromaffin cells. Neurosci Lett 326(3):167–170

    Article  PubMed  CAS  Google Scholar 

  22. Pezzati R, Bossi M, Podini P, Meldolesi J, Grohovaz F (1997) High-resolution calcium mapping of the endoplasmic reticulum-Golgi-exocytic membrane system. Electron energy loss imaging analysis of quick frozen-freeze dried PC12 cells. Mol Biol Cell 8:1501–1512

    PubMed  CAS  Google Scholar 

  23. Montero M, Alvarez J, Scheenen WJJ, Rizzuto R, Meldolesi J, Pozzan T (1997) Ca2+ homeostasis in the endoplasmic reticulum: coexistence of high and low [Ca2+] subcompartments in intact HeLa cells. J Cell Biol 139:601–611

    Article  PubMed  CAS  Google Scholar 

  24. Lippincott-Schwartz J, Patterson GH (2003) Development and use of fluorescent protein markers in living cells. Science 300(5616):87–91

    Article  PubMed  CAS  Google Scholar 

  25. Jones VC, McKeown L, Verkhratsky A, Jones OT (2008) LV-pIN-KDEL: a novel lentiviral vector demonstrates the morphology, dynamics and continuity of the endoplasmic reticulum in live neurones. BMC Neurosci 9:10

    Article  PubMed  CAS  Google Scholar 

  26. Jones VC, Rodríguez JJ, Verkhratsky A, Jones OT (2009) A lentivirally delivered photoactivatable GFP to assess continuity in the endoplasmic reticulum of neurones and glia. Pflugers Arch 458(4):809–818

    Article  PubMed  CAS  Google Scholar 

  27. Mogami H, Nakano K, Tepikin AV, Petersen OH (1997) Ca2+ flow via tunnels in polarized cells: recharging of apical Ca2+ stores by focal Ca2+ entry through basal membrane patch. Cell 88(1):49–55

    Article  PubMed  CAS  Google Scholar 

  28. Verkhratsky A (2005) Physiology and pathophysiology of the calcium store in the endoplasmic reticulum of neurons. Physiol Rev 85(1):201–279

    Article  PubMed  CAS  Google Scholar 

  29. Park MK, Petersen OH, Tepikin AV (2000) The endoplasmic reticulum as one continuous Ca2+ pool: visualization of rapid Ca2+ movements and equilibration. EMBO J 19(21):5729–5739

    Article  PubMed  CAS  Google Scholar 

  30. Solovyova N, Verkhratsky A (2003) Neuronal endoplasmic reticulum acts as a single functional Ca2+ store shared by ryanodine and inositol-1, 4, 5-trisphosphate receptors as revealed by intra-ER [Ca2+] recordings in single rat sensory neurones. Pflugers Arch 446(4):447–454

    Article  PubMed  CAS  Google Scholar 

  31. Petersen OH, Verkhratsky A (2007) Endoplasmic reticulum calcium tunnels integrate signalling in polarised cells. Cell Calcium 42(4–5):373–378

    Article  PubMed  CAS  Google Scholar 

  32. Meldolesi J, Pozzan T (1998) The endoplasmic reticulum Ca2+ store: a view from the lumen. Trends Biochem Sci 23:10–14

    Article  PubMed  CAS  Google Scholar 

  33. Palmer AE, Jin C, Reed JC, Tsien RY (2004) Bcl-2-mediated alterations in endoplasmic reticulum Ca2+ analyzed with an improved genetically encoded fluorescent sensor. Proc Natl Acad Sci USA 101(50):17404–17409

    Article  PubMed  CAS  Google Scholar 

  34. Hofer AM, Machen TE (1993) Technique for in situ measurement of calcium in intracellular inositol 1, 4, 5-trisphosphate-sensitive stores using the fluorescent indicator mag-fura-2. Proc Natl Acad Sci USA 90:2598–2602

    Article  PubMed  CAS  Google Scholar 

  35. Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, Ikura M, Tsien RY (1997) Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388:882–887

    Article  PubMed  CAS  Google Scholar 

  36. Rudolf R, Magalhaes PJ, Pozzan T (2006) Direct in vivo monitoring of sarcoplasmic reticulum Ca2+ and cytosolic cAMP dynamics in mouse skeletal muscle. J Cell Biol 173(2):187–193

    Article  PubMed  CAS  Google Scholar 

  37. Pinton P, Ferrari D, Magalhães P, Schulze-Osthoff K, Di Virgilio F, Pozzan T, Rizzuto R (2000) Reduced loading of intracellular Ca2+ stores and downregulation of capacitative Ca2+ influx in Bcl-2-overexpressing cells. J Cell Biol 148:857–862

    Article  PubMed  CAS  Google Scholar 

  38. Alonso MT, Barrero MJ, Michelena P, Carnicero E, Cuchillo I, Garcia AG, Garcia-Sancho J, Montero M, Alvarez J (1999) Ca2+-induced Ca2+ release in chromaffin cells seen from inside the ER with targeted aequorin. J Cell Biol 144(2):241–254

    Article  PubMed  CAS  Google Scholar 

  39. Burdakov D, Petersen OH, Verkhratsky A (2005) Intraluminal calcium as a primary regulator of endoplasmic reticulum function. Cell Calcium 38(3–4):303–310

    Article  PubMed  CAS  Google Scholar 

  40. Putney JW Jr, Broad LM, Braun FJ, Lievremont JP, Bird GS (2001) Mechanisms of capacitative calcium entry. J Cell Sci 114(Pt 12):2223–2229

    PubMed  CAS  Google Scholar 

  41. Camello C, Lomax R, Petersen OH, Tepikin AV (2002) Calcium leak from intracellular stores—the enigma of calcium signalling. Cell Calcium 32(5–6):355–361

    Article  PubMed  CAS  Google Scholar 

  42. Putney JW (2011) The physiological function of store-operated calcium entry. Neurochem Res 36(7):1157–1165

    Article  PubMed  CAS  Google Scholar 

  43. Zhang SL, Yu Y, Roos J, Kozak JA, Deerinck TJ, Ellisman MH, Stauderman KA, Cahalan MD (2005) STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437(7060):902–905

    Article  PubMed  CAS  Google Scholar 

  44. Liou J, Kim ML, Heo WD, Jones JT, Myers JW, Ferrell JE Jr, Meyer T (2005) STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr Biol 15(13):1235–1241

    Article  PubMed  CAS  Google Scholar 

  45. Liou J, Fivaz M, Inoue T, Meyer T (2007) Live-cell imaging reveals sequential oligomerization and local plasma membrane targeting of stromal interaction molecule 1 after Ca2+ store depletion. Proc Natl Acad Sci USA 104(22):9301–9306

    Article  PubMed  CAS  Google Scholar 

  46. Prakriya M, Lewis RS (2006) Regulation of CRAC channel activity by recruitment of silent channels to a high open-probability gating mode. J Gen Physiol 128(3):373–386

    Article  PubMed  CAS  Google Scholar 

  47. Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH, Tanasa B, Hogan PG, Lewis RS, Daly M, Rao A (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441(7090):179–185

    Article  PubMed  CAS  Google Scholar 

  48. Zhang SL, Yeromin AV, Zhang XH, Yu Y, Safrina O, Penna A, Roos J, Stauderman KA, Cahalan MD (2006) Genome-wide RNAi screen of Ca(2+) influx identifies genes that regulate Ca(2+) release-activated Ca(2+) channel activity. Proc Natl Acad Sci USA 103(24):9357–9362

    Article  PubMed  CAS  Google Scholar 

  49. Yeromin AV, Zhang SL, Jiang W, Yu Y, Safrina O, Cahalan MD (2006) Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 443(7108):226–229

    Article  PubMed  CAS  Google Scholar 

  50. Vig M, Beck A, Billingsley JM, Lis A, Parvez S, Peinelt C, Koomoa DL, Soboloff J, Gill DL, Fleig A, Kinet JP, Penner R (2006) CRACM1 multimers form the ion-selective pore of the CRAC channel. Current biology CB 16(20):2073–2079

    Article  PubMed  CAS  Google Scholar 

  51. Cahalan MD (2009) STIMulating store-operated Ca2+ entry. Nat Cell Biol 11(6):669–677

    Article  PubMed  CAS  Google Scholar 

  52. Brandman O, Liou J, Park WS, Meyer T (2007) STIM2 is a feedback regulator that stabilizes basal cytosolic and endoplasmic reticulum Ca2+ levels. Cell 131(7):1327–1339

    Article  PubMed  CAS  Google Scholar 

  53. Sammels E, Parys JB, Missiaen L, De Smedt H, Bultynck G (2010) Intracellular Ca2+ storage in health and disease: a dynamic equilibrium. Cell Calcium 47(4):297–314

    Article  PubMed  CAS  Google Scholar 

  54. Roy A, Wonderlin WF (2003) The permeability of the endoplasmic reticulum is dynamically coupled to protein synthesis. J Biol Chem 278(7):4397–4403

    Article  PubMed  CAS  Google Scholar 

  55. Flourakis M, Van Coppenolle F, Lehen’kyi V, Beck B, Skryma R, Prevarskaya N (2006) Passive calcium leak via translocon is a first step for iPLA2-pathway regulated store operated channels activation. FASEB J 20(8):1215–1217

    Article  PubMed  CAS  Google Scholar 

  56. Ong HL, Liu X, Sharma A, Hegde RS, Ambudkar IS (2007) Intracellular Ca(2+) release via the ER translocon activates store-operated calcium entry. Pflugers Arch 453(6):797–808

    Article  PubMed  CAS  Google Scholar 

  57. Anyatonwu GI, Ehrlich BE (2005) Organic cation permeation through the channel formed by polycystin-2. J Biol Chem 280(33):29488–29493

    Article  PubMed  CAS  Google Scholar 

  58. Tu H, Nelson O, Bezprozvanny A, Wang Z, Lee SF, Hao YH, Serneels L, De Strooper B, Yu G, Bezprozvanny I (2006) Presenilins form ER Ca2+ leak channels, a function disrupted by familial Alzheimer’s disease-linked mutations. Cell 126(5):981–993

    Article  PubMed  CAS  Google Scholar 

  59. Kim HR, Lee GH, Ha KC, Ahn T, Moon JY, Lee BJ, Cho SG, Kim S, Seo YR, Shin YJ, Chae SW, Reed JC, Chae HJ (2008) Bax Inhibitor-1 Is a pH-dependent regulator of Ca2+ channel activity in the endoplasmic reticulum. J Biol Chem 283(23):15946–15955

    Article  PubMed  CAS  Google Scholar 

  60. D’Hondt C, Ponsaerts R, De Smedt H, Vinken M, De Vuyst E, De Bock M, Wang N, Rogiers V, Leybaert L, Himpens B, Bultynck G (2011) Pannexin channels in ATP release and beyond: an unexpected rendezvous at the endoplasmic reticulum. Cell Signal 23(2):305–316

    Article  PubMed  CAS  Google Scholar 

  61. Oakes SA, Scorrano L, Opferman JT, Bassik MC, Nishino M, Pozzan T, Korsmeyer SJ (2005) Proapoptotic BAX and BAK regulate the type 1 inositol trisphosphate receptor and calcium leak from the endoplasmic reticulum. Proc Natl Acad Sci USA 102(1):105–110

    Article  PubMed  CAS  Google Scholar 

  62. Cai C, Lin P, Cheung KH, Li N, Levchook C, Pan Z, Ferrante C, Boulianne GL, Foskett JK, Danielpour D, Ma J (2006) The presenilin-2 loop peptide perturbs intracellular Ca2+ homeostasis and accelerates apoptosis. J Biol Chem 281(24):16649–16655

    Article  PubMed  CAS  Google Scholar 

  63. Cheung KH, Shineman D, Muller M, Cardenas C, Mei L, Yang J, Tomita T, Iwatsubo T, Lee VM, Foskett JK (2008) Mechanism of Ca2+ disruption in Alzheimer’s disease by presenilin regulation of InsP3 receptor channel gating. Neuron 58(6):871–883

    Article  PubMed  CAS  Google Scholar 

  64. Cheung KH, Mei L, Mak DO, Hayashi I, Iwatsubo T, Kang DE, Foskett JK (2010) Gain-of-function enhancement of IP3 receptor modal gating by familial Alzheimer’s disease-linked presenilin mutants in human cells and mouse neurons. Sci Signal 3(114):ra22

    Article  PubMed  CAS  Google Scholar 

  65. Rybalchenko V, Hwang SY, Rybalchenko N, Koulen P (2008) The cytosolic N terminus of presenilin-1 potentiates mouse ryanodine receptor single channel activity. Int J Biochem Cell Biol 40(1):84–97

    Article  PubMed  CAS  Google Scholar 

  66. Hayrapetyan V, Rybalchenko V, Rybalchenko N, Koulen P (2008) The N-terminus of presenilin-2 increases single channel activity of brain ryanodine receptors through direct protein-protein interaction. Cell Calcium 44(5):507–518

    Article  PubMed  CAS  Google Scholar 

  67. Pinton P, Pozzan T, Rizzuto R (1998) The Golgi apparatus is an inositol 1, 4, 5-trisphosphate-sensitive Ca2+ store, with functional properties distinct from those of the endoplasmic reticulum. EMBO J 17(18):5298–5308

    Article  PubMed  CAS  Google Scholar 

  68. MacLennan DH, Kranias EG (2003) Phospholamban: a crucial regulator of cardiac contractility. Nat Rev Mol Cell Biol 4(7):566–577

    Article  PubMed  CAS  Google Scholar 

  69. Brunello L, Zampese E, Florean C, Pozzan T, Pizzo P, Fasolato C (2009) Presenilin-2 dampens intracellular Ca2+ stores by increasing Ca2+ leakage and reducing Ca2+ uptake. J Cell Mol Med 13:3358–3369

    Article  PubMed  Google Scholar 

  70. John LM, Lechleiter JD, Camacho P (1998) Differential modulation of SERCA2 isoforms by calreticulin. J Cell Biol 142(4):963–973

    Article  PubMed  CAS  Google Scholar 

  71. Foskett JK, White C, Cheung KH, Mak DO (2007) Inositol trisphosphate receptor Ca2+ release channels. Physiol Rev 87(2):593–658

    Article  PubMed  CAS  Google Scholar 

  72. Mendes CC, Gomes DA, Thompson M, Souto NC, Goes TS, Goes AM, Rodrigues MA, Gomez MV, Nathanson MH, Leite MF (2005) The type III inositol 1, 4, 5-trisphosphate receptor preferentially transmits apoptotic Ca2+ signals into mitochondria. J Biol Chem 280(49):40892–40900

    Article  PubMed  CAS  Google Scholar 

  73. Hattori M, Suzuki AZ, Higo T, Miyauchi H, Michikawa T, Nakamura T, Inoue T, Mikoshiba K (2004) Distinct roles of inositol 1, 4, 5-trisphosphate receptor types 1 and 3 in Ca2+ signaling. J Biol Chem 279(12):11967–11975

    Article  PubMed  CAS  Google Scholar 

  74. Schmidt M, Evellin S, Weernink PA, von Dorp F, Rehmann H, Lomasney JW, Jakobs KH (2001) A new phospholipase-C-calcium signalling pathway mediated by cyclic AMP and a Rap GTPase. Nat Cell Biol 3(11):1020–1024

    Article  PubMed  CAS  Google Scholar 

  75. Mikoshiba K (2007) The IP3 receptor/Ca2+ channel and its cellular function. Biochem Soc Symp 74:9–22

    Article  PubMed  CAS  Google Scholar 

  76. Yule DI, Betzenhauser MJ, Joseph SK (2010) Linking structure to function: recent lessons from inositol 1, 4, 5-trisphosphate receptor mutagenesis. Cell Calcium 47(6):469–479

    Article  PubMed  CAS  Google Scholar 

  77. Higo T, Hattori M, Nakamura T, Natsume T, Michikawa T, Mikoshiba K (2005) Subtype-specific and ER lumenal environment-dependent regulation of inositol 1, 4, 5-trisphosphate receptor type 1 by ERp44. Cell 120(1):85–98

    Article  PubMed  CAS  Google Scholar 

  78. Berridge MJ (2009) Inositol trisphosphate and calcium signalling mechanisms. Biochim Biophys Acta 1793(6):933–940

    Article  PubMed  CAS  Google Scholar 

  79. Taylor CW, Taufiq Ur R, Pantazaka E (2009) Targeting and clustering of IP3 receptors: key determinants of spatially organized Ca2+ signals. Chaos (Woodbury NY) 19(3):037102

    Article  CAS  Google Scholar 

  80. Wilson BS, Pfeiffer JR, Smith AJ, Oliver JM, Oberdorf JA, Wojcikiewicz RJ (1998) Calcium-dependent clustering of inositol 1, 4, 5-trisphosphate receptors. Mol Biol Cell 9(6):1465–1478

    PubMed  CAS  Google Scholar 

  81. Tateishi Y, Hattori M, Nakayama T, Iwai M, Bannai H, Nakamura T, Michikawa T, Inoue T, Mikoshiba K (2005) Cluster formation of inositol 1, 4, 5-trisphosphate receptor requires its transition to open state. J Biol Chem 280(8):6816–6822

    Article  PubMed  CAS  Google Scholar 

  82. Taufiq Ur R, Skupin A, Falcke M, Taylor CW (2009) Clustering of InsP3 receptors by InsP3 retunes their regulation by InsP3 and Ca2+. Nature 458(7238):655–659

    Article  Google Scholar 

  83. Chalmers M, Schell MJ, Thorn P (2006) Agonist-evoked inositol trisphosphate receptor (IP3R) clustering is not dependent on changes in the structure of the endoplasmic reticulum. Biochem J 394(Pt 1):57–66

    PubMed  CAS  Google Scholar 

  84. Rios E, Brum G (1987) Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature 325:717–720

    Article  PubMed  CAS  Google Scholar 

  85. Fabiato A (1983) Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. J Physiol 245:C1–C4

    CAS  Google Scholar 

  86. Chavis P, Fagni L, Lansman JB, Bockaert J (1996) Functional coupling between ryanodine receptors and L-type calcium channels in neurons. Nature 382(6593):719–722

    Article  PubMed  CAS  Google Scholar 

  87. Schwab Y, Mouton J, Chasserot-Golaz S, Marty I, Maulet Y, Jover E (2001) Calcium-dependent translocation of synaptotagmin to the plasma membrane in the dendrites of developing neurones. Brain Res Mol Brain Res 96(1–2):1–13

    Article  PubMed  CAS  Google Scholar 

  88. Zalk R, Lehnart SE, Marks AR (2007) Modulation of the ryanodine receptor and intracellular calcium. Annu Rev Biochem 76:367–385

    Article  PubMed  CAS  Google Scholar 

  89. Lanner JT, Georgiou DK, Joshi AD, Hamilton SL (2010) Ryanodine receptors: structure, expression, molecular details, and function in calcium release. Cold Spring Harbor Perspect Biol 2(11):a003996

    Article  CAS  Google Scholar 

  90. Fill M, Copello JA (2002) Ryanodine receptor calcium release channels. Physiol Rev 82(4):893–922

    PubMed  CAS  Google Scholar 

  91. Guse AH, Lee HC (2008) NAADP: a universal Ca2+ trigger. Sci Signal 1(44):re10

    Article  PubMed  CAS  Google Scholar 

  92. Meszaros LG, Bak J, Chu A (1993) Cyclic ADP-ribose as an endogenous regulator of the non-skeletal type ryanodine receptor Ca2+ channel. Nature 364(6432):76–79

    Article  PubMed  CAS  Google Scholar 

  93. Clapper DL, Walseth TF, Dargie PJ, Lee HC (1987) Pyridine nucleotide metabolites stimulate calcium release from sea urchin egg microsomes desensitized to inositol trisphosphate. J Biol Chem 262(20):9561–9568

    PubMed  CAS  Google Scholar 

  94. Galione A, Lee HC, Busa WB (1991) Ca(2+)-induced Ca2+ release in sea urchin egg homogenates: modulation by cyclic ADP-ribose. Science (New York NY) 253(5024):1143–1146

    Article  CAS  Google Scholar 

  95. Guse AH (2005) Second messenger function and the structure-activity relationship of cyclic adenosine diphosphoribose (cADPR). FEBS J 272(18):4590–4597

    Article  PubMed  CAS  Google Scholar 

  96. Ogunbayo OA, Zhu Y, Rossi D, Sorrentino V, Ma J, Zhu MX, Evans AM (2011) Cyclic adenosine diphosphate ribose activates ryanodine receptors, whereas NAADP activates two-pore domain channels. J Biol Chem 286(11):9136–9140

    Article  PubMed  CAS  Google Scholar 

  97. Lee HC (2004) Multiplicity of Ca2+ messengers and Ca2+ stores: a perspective from cyclic ADP-ribose and NAADP. Curr Mol Med 4(3):227–237

    Article  PubMed  CAS  Google Scholar 

  98. Galione A, Churchill GC (2000) Cyclic ADP ribose as a calcium-mobilizing messenger. Sci STKE 2000(41):pe1

    Article  PubMed  CAS  Google Scholar 

  99. Walseth TF, Aarhus R, Kerr JA, Lee HC (1993) Identification of cyclic ADP-ribose-binding proteins by photoaffinity labeling. J Biol Chem 268(35):26686–26691

    PubMed  CAS  Google Scholar 

  100. Noguchi N, Takasawa S, Nata K, Tohgo A, Kato I, Ikehata F, Yonekura H, Okamoto H (1997) Cyclic ADP-ribose binds to FK506-binding protein 12.6 to release Ca2+ from islet microsomes. J Biol Chem 272(6):3133–3136

    Article  PubMed  CAS  Google Scholar 

  101. Zheng J, Wenzhi B, Miao L, Hao Y, Zhang X, Yin W, Pan J, Yuan Z, Song B, Ji G (2010) Ca(2+) release induced by cADP-ribose is mediated by FKBP12.6 proteins in mouse bladder smooth muscle. Cell Calcium 47(5):449–457

    Article  PubMed  CAS  Google Scholar 

  102. Bai N, Lee HC, Laher I (2005) Emerging role of cyclic ADP-ribose (cADPR) in smooth muscle. Pharmacol Ther 105(2):189–207

    Article  PubMed  CAS  Google Scholar 

  103. Thorn P, Gerasimenko O, Petersen OH (1994) Cyclic ADP-ribose regulation of ryanodine receptors involved in agonist evoked cytosolic Ca2+ oscillations in pancreatic acinar cells. EMBO J 13(9):2038–2043

    PubMed  CAS  Google Scholar 

  104. Higashida H, Salmina AB, Olovyannikova RY, Hashii M, Yokoyama S, Koizumi K, Jin D, Liu HX, Lopatina O, Amina S, Islam MS, Huang JJ, Noda M (2007) Cyclic ADP-ribose as a universal calcium signal molecule in the nervous system. Neurochem Int 51(2–4):192–199

    Article  PubMed  CAS  Google Scholar 

  105. Lee D, Michalak M (2010) Membrane associated Ca2+ buffers in the heart. BMB Rep 43(3):151–157

    Article  PubMed  CAS  Google Scholar 

  106. Coe H, Michalak M (2009) Calcium binding chaperones of the endoplasmic reticulum. Gen Physiol Biophys 28 Spec No Focus: F96–F103

  107. Michalak M, Groenendyk J, Szabo E, Gold LI, Opas M (2009) Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochem J 417(3):651–666

    Article  PubMed  CAS  Google Scholar 

  108. Fliegel L, Burns K, MacLennan DH, Reithmeier RA, Michalak M (1989) Molecular cloning of the high affinity calcium-binding protein (calreticulin) of skeletal muscle sarcoplasmic reticulum. J Biol Chem 264(36):21522–21528

    PubMed  CAS  Google Scholar 

  109. Bastianutto C, Clementi E, Codazzi F, Podini P, De Giorgi F, Rizzuto R, Meldolesi J, Pozzan T (1995) Overexpression of calreticulin increases the Ca2+ capacity of rapidly exchanging Ca2+ stores and reveals aspects of their lumenal microenvironment and function. J Cell Biol 130:847–855

    Article  PubMed  CAS  Google Scholar 

  110. Mery L, Mesaeli N, Michalak M, Opas M, Lew DP, Krause KH (1996) Overexpression of calreticulin increases intracellular Ca2+ storage and decreases store-operated Ca2+ influx. J Biol Chem 271:9332–9339

    Article  PubMed  CAS  Google Scholar 

  111. Mesaeli N, Nakamura K, Zvaritch E, Dickie P, Dziak E, Krause KH, Opas M, MacLennan DH, Michalak M (1999) Calreticulin is essential for cardiac development. J Cell Biol 144(5):857–868

    Article  PubMed  CAS  Google Scholar 

  112. Guo L, Lynch J, Nakamura K, Fliegel L, Kasahara H, Izumo S, Komuro I, Agellon LB, Michalak M (2001) COUP-TF1 antagonizes Nkx2.5-mediated activation of the calreticulin gene during cardiac development. J Biol Chem 276(4):2797–2801

    Article  PubMed  CAS  Google Scholar 

  113. Wada I, Rindress D, Cameron PH, Ou WJ, Doherty JJ 2nd, Louvard D, Bell AW, Dignard D, Thomas DY, Bergeron JJ (1991) SSR alpha and associated calnexin are major calcium binding proteins of the endoplasmic reticulum membrane. J Biol Chem 266(29):19599–19610

    PubMed  CAS  Google Scholar 

  114. Lievremont JP, Rizzuto R, Hendershot L, Meldolesi J (1997) BiP, a major chaperone protein of the endoplasmic reticulum lumen, plays a direct and important role in the storage of the rapidly exchanging pool of Ca2+. J Biol Chem 272(49):30873–30879

    Article  PubMed  CAS  Google Scholar 

  115. Koch G, Smith M, Macer D, Webster P, Mortara R (1986) Endoplasmic reticulum contains a common, abundant calcium-binding glycoprotein, endoplasmin. J Cell Sci 86:217–232

    PubMed  CAS  Google Scholar 

  116. Nigam SK, Goldberg AL, Ho S, Rohde MF, Bush KT, Sherman M (1994) A set of endoplasmic reticulum proteins possessing properties of molecular chaperones includes Ca(2+)-binding proteins and members of the thioredoxin superfamily. J Biol Chem 269(3):1744–1749

    PubMed  CAS  Google Scholar 

  117. Lebeche D, Lucero HA, Kaminer B (1994) Calcium binding properties of rabbit liver protein disulfide isomerase. Biochem Biophys Res Commun 202(1):556–561

    Article  PubMed  CAS  Google Scholar 

  118. Lucero HA, Lebeche D, Kaminer B (1994) ERcalcistorin/protein disulfide isomerase (PDI). Sequence determination and expression of a cDNA clone encoding a calcium storage protein with PDI activity from endoplasmic reticulum of the sea urchin egg. J Biol Chem 269(37):23112–23119

    PubMed  CAS  Google Scholar 

  119. MacLennan DH, Wong TS (1971) Isolation of a calcium sequestering protein from sarcoplasmic reticulum. Proc Natl Acad Sci USA 68:1231–1235

    Article  PubMed  CAS  Google Scholar 

  120. Royer L, Rios E (2009) Deconstructing calsequestrin. Complex buffering in the calcium store of skeletal muscle. J Physiol 587(Pt 13):3101–3111

    Article  PubMed  CAS  Google Scholar 

  121. Volpe P, Martini A, Furlan S, Meldolesi J (1994) Calsequestrin is a component of smooth muscles: the skeletal- and cardiac-muscle isoforms are both present, although in highly variable amounts and ratios. Biochem J 301(Pt 2):465–469

    PubMed  CAS  Google Scholar 

  122. Volpe P, Nori A, Martini A, Sacchetto R, Villa A (1993) Multiple/heterogeneous Ca2+ stores in cerebellum Purkinje neurons. Comp Biochem Physiol Comp Physiol 105(2):205–211

    Article  PubMed  CAS  Google Scholar 

  123. Leberer E, Timms BG, Campbell KP, MacLennan DH (1990) Purification, calcium binding properties, and ultrastructural localization of the 53,000- and 160,000 (sarcalumenin)-dalton glycoproteins of the sarcoplasmic reticulum. J Biol Chem 265(17):10118–10124

    PubMed  CAS  Google Scholar 

  124. Hofmann SL, Goldstein JL, Orth K, Moomaw CR, Slaughter CA, Brown MS (1989) Molecular cloning of a histidine-rich Ca2+-binding protein of sarcoplasmic reticulum that contains highly conserved repeated elements. J Biol Chem 264(30):18083–18090

    PubMed  CAS  Google Scholar 

  125. Solovyova N, Veselovsky N, Toescu EC, Verkhratsky A (2002) Ca2+ dynamics in the lumen of the endoplasmic reticulum in sensory neurones: direct visualisation of Ca2+-induced Ca2+ release triggered by physiological Ca2+ entry. EMBO J 21:622–630

    Article  PubMed  CAS  Google Scholar 

  126. Foggia L, Aronchik I, Aberg K, Brown B, Hovnanian A, Mauro TM (2006) Activity of the hSPCA1 Golgi Ca2+ pump is essential for Ca2+-mediated Ca2+ response and cell viability in Darier disease. J Cell Sci 119(Pt 4):671–679

    Article  PubMed  CAS  Google Scholar 

  127. Odermatt A, Taschner PE, Khanna VK, Busch HF, Karpati G, Jablecki CK, Breuning MH, MacLennan DH (1996) Mutations in the gene-encoding SERCA1, the fast-twitch skeletal muscle sarcoplasmic reticulum Ca2+ ATPase, are associated with Brody disease. Nat Genet 14(2):191–194

    Article  PubMed  CAS  Google Scholar 

  128. Kranias EG, Bers DM (2007) Calcium and cardiomyopathies. Subcell Biochem 45:523–537

    Article  PubMed  CAS  Google Scholar 

  129. Monteith GR, McAndrew D, Faddy HM, Roberts-Thomson SJ (2007) Calcium and cancer: targeting Ca2+ transport. Nat Rev Cancer 7(7):519–530

    Article  PubMed  CAS  Google Scholar 

  130. Varadi A, Lebel L, Hashim Y, Mehta Z, Ashcroft SJ, Turner R (1999) Sequence variants of the sarco(endo)plasmic reticulum Ca(2+)-transport ATPase 3 gene (SERCA3) in Caucasian type II diabetic patients (UK Prospective Diabetes Study 48). Diabetologia 42(10):1240–1243

    Article  PubMed  CAS  Google Scholar 

  131. Green KN, Demuro A, Akbari Y, Hitt BD, Smith IF, Parker I, LaFerla FM (2008) SERCA pump activity is physiologically regulated by presenilin and regulates amyloid beta production. J Cell Biol 181(7):1107–1116

    Article  PubMed  CAS  Google Scholar 

  132. van de Leemput J, Chandran J, Knight MA, Holtzclaw LA, Scholz S, Cookson MR, Houlden H, Gwinn-Hardy K, Fung HC, Lin X, Hernandez D, Simon-Sanchez J, Wood NW, Giunti P, Rafferty I, Hardy J, Storey E, Gardner RJ, Forrest SM, Fisher EM, Russell JT, Cai H, Singleton AB (2007) Deletion at ITPR1 underlies ataxia in mice and spinocerebellar ataxia 15 in humans. PLoS Genet 3(6):e108

    Article  PubMed  CAS  Google Scholar 

  133. Hara K, Shiga A, Nozaki H, Mitsui J, Takahashi Y, Ishiguro H, Yomono H, Kurisaki H, Goto J, Ikeuchi T, Tsuji S, Nishizawa M, Onodera O (2008) Total deletion and a missense mutation of ITPR1 in Japanese SCA15 families. Neurology 71(8):547–551

    Article  PubMed  CAS  Google Scholar 

  134. Iwaki A, Kawano Y, Miura S, Shibata H, Matsuse D, Li W, Furuya H, Ohyagi Y, Taniwaki T, Kira J, Fukumaki Y (2008) Heterozygous deletion of ITPR1, but not SUMF1, in spinocerebellar ataxia type 16. J Med Genet 45(1):32–35

    Article  PubMed  CAS  Google Scholar 

  135. Tang TS, Tu H, Chan EY, Maximov A, Wang Z, Wellington CL, Hayden MR, Bezprozvanny I (2003) Huntingtin and huntingtin-associated protein 1 influence neuronal calcium signaling mediated by inositol-(1, 4, 5) triphosphate receptor type 1. Neuron 39(2):227–239

    Article  PubMed  CAS  Google Scholar 

  136. Boehning D, Patterson RL, Sedaghat L, Glebova NO, Kurosaki T, Snyder SH (2003) Cytochrome c binds to inositol (1, 4, 5) trisphosphate receptors, amplifying calcium-dependent apoptosis. Nat Cell Biol 5(12):1051–1061

    Article  PubMed  CAS  Google Scholar 

  137. Lao Y, Chang DC (2007) Study of the functional role of Bcl-2 family proteins in regulating Ca(2+) signals in apoptotic cells. Biochem Soc Trans 35(Pt 5):1038–1039

    PubMed  CAS  Google Scholar 

  138. Rong YP, Barr P, Yee VC, Distelhorst CW (2009) Targeting Bcl-2 based on the interaction of its BH4 domain with the inositol 1, 4, 5-trisphosphate receptor. Biochim Biophys Acta 1793(6):971–978

    Article  PubMed  CAS  Google Scholar 

  139. Vance JE (1990) Phospholipid synthesis in a membrane fraction associated with mitochondria. J Biol Chem 265(13):7248–7256

    PubMed  CAS  Google Scholar 

  140. Rusinol AE, Cui Z, Chen MH, Vance JE (1994) A unique mitochondria-associated membrane fraction from rat liver has a high capacity for lipid synthesis and contains pre-Golgi secretory proteins including nascent lipoproteins. J Biol Chem 269(44):27494–27502

    PubMed  CAS  Google Scholar 

  141. Pizzo P, Pozzan T (2007) Mitochondria-endoplasmic reticulum choreography: structure and signaling dynamics. Trends Cell Biol 17(10):511–517

    Article  PubMed  CAS  Google Scholar 

  142. Betzenhauser MJ, Marks AR (2010) Ryanodine receptor channelopathies. Pflugers Archiv Eur J Physiol 460(2):467–480

    Article  CAS  Google Scholar 

  143. Bellinger AM, Reiken S, Dura M, Murphy PW, Deng SX, Landry DW, Nieman D, Lehnart SE, Samaru M, LaCampagne A, Marks AR (2008) Remodeling of ryanodine receptor complex causes “leaky” channels: a molecular mechanism for decreased exercise capacity. Proc Natl Acad Sci USA 105(6):2198–2202

    Article  PubMed  CAS  Google Scholar 

  144. Wehrens XH, Lehnart SE, Huang F, Vest JA, Reiken SR, Mohler PJ, Sun J, Guatimosim S, Song LS, Rosemblit N, D’Armiento JM, Napolitano C, Memmi M, Priori SG, Lederer WJ, Marks AR (2003) FKBP12.6 deficiency and defective calcium release channel (ryanodine receptor) function linked to exercise-induced sudden cardiac death. Cell 113(7):829–840

    Article  PubMed  CAS  Google Scholar 

  145. Chakroborty S, Goussakov I, Miller MB, Stutzmann GE (2009) Deviant ryanodine receptor-mediated calcium release resets synaptic homeostasis in presymptomatic 3xTg-AD mice. J Neurosci 29(30):9458–9470

    Article  PubMed  CAS  Google Scholar 

  146. Stutzmann GE, Smith I, Caccamo A, Oddo S, Laferla FM, Parker I (2006) Enhanced ryanodine receptor recruitment contributes to Ca2+ disruptions in young, adult, and aged Alzheimer’s disease mice. J Neurosci 26(19):5180–5189

    Article  PubMed  CAS  Google Scholar 

  147. Stutzmann GE, Smith I, Caccamo A, Oddo S, Parker I, Laferla F (2007) Enhanced ryanodine-mediated calcium release in mutant PS1-expressing Alzheimer’s mouse models. Ann NY Acad Sci 1097:265–277

    Article  PubMed  CAS  Google Scholar 

  148. Supnet C, Noonan C, Richard K, Bradley J, Mayne M (2010) Up-regulation of the type 3 ryanodine receptor is neuroprotective in the TgCRND8 mouse model of Alzheimer’s disease. J Neurochem 112(2):356–365

    Article  PubMed  CAS  Google Scholar 

  149. De Matteis MA, Luini A (2008) Exiting the Golgi complex. Nat Rev Mol Cell Biol 9(4):273–284

    Article  PubMed  CAS  Google Scholar 

  150. Breton C, Mucha J, Jeanneau C (2001) Structural and functional features of glycosyltransferases. Biochimie 83(8):713–718

    Article  PubMed  CAS  Google Scholar 

  151. Chandra S, Kable EP, Morrison GH, Webb WW (1991) Calcium sequestration in the Golgi apparatus of cultured mammalian cells revealed by laser scanning confocal microscopy and ion microscopy. J Cell Sci 100(Pt 4):747–752

    PubMed  Google Scholar 

  152. Carnell L, Moore HP (1994) Transport via the regulated secretory pathway in semi-intact PC12 cells: role of intra-cisternal calcium and pH in the transport and sorting of secretogranin II. J Cell Biol 127:693–705

    Article  PubMed  CAS  Google Scholar 

  153. Oda K (1992) Calcium depletion blocks proteolytic cleavages of plasma protein precursors which occur at the Golgi and/or trans -Golgi network. Possible involvement of Ca(2+)-dependent Golgi endoproteases. J Biol Chem 267(24):17465–17471

    PubMed  CAS  Google Scholar 

  154. Chanat E, Huttner WB (1991) Milieu-induced, selective aggregation of regulated secretory proteins in the trans-Golgi network. J Cell Biol 115(6):1505–1519

    Article  PubMed  CAS  Google Scholar 

  155. Ivessa NE, De Lemos-Chiarandini C, Gravotta D, Sabatini DD, Kreibich G (1995) The Brefeldin A-induced retrograde transport from the Golgi apparatus to the endoplasmic reticulum depends on calcium sequestered to intracellular stores. J Biol Chem 270(43):25960–25967

    Article  PubMed  CAS  Google Scholar 

  156. Missiaen L, Dode L, Vanoevelen J, Raeymaekers L, Wuytack F (2007) Calcium in the Golgi apparatus. Cell Calcium 41(5):405–416

    Article  PubMed  CAS  Google Scholar 

  157. Lin P, Yao Y, Hofmeister R, Tsien RY, Farquhar MG (1999) Overexpression of CALNUC (nucleobindin) increases agonist and thapsigargin releasable Ca2+ storage in the Golgi. J Cell Biol 145(2):279–289

    Article  PubMed  CAS  Google Scholar 

  158. Surroca A, Wolff D (2000) Inositol 1, 4, 5-trisphosphate but not ryanodine-receptor agonists induces calcium release from rat liver Golgi apparatus membrane vesicles. J Membr Biol 177(3):243–249

    Article  PubMed  CAS  Google Scholar 

  159. Callewaert G, Parys JB, De Smedt H, Raeymaekers L, Wuytack F, Vanoevelen J, Van Baelen K, Simoni A, Rizzuto R, Missiaen L (2003) Similar Ca(2+)-signaling properties in keratinocytes and in COS-1 cells overexpressing the secretory-pathway Ca(2+)-ATPase SPCA1. Cell Calcium 34(2):157–162

    Article  PubMed  CAS  Google Scholar 

  160. Missiaen L, Van Acker K, Van Baelen K, Raeymaekers L, Wuytack F, Parys JB, De Smedt H, Vanoevelen J, Dode L, Rizzuto R, Callewaert G (2004) Calcium release from the Golgi apparatus and the endoplasmic reticulum in HeLa cells stably expressing targeted aequorin to these compartments. Cell Calcium 36(6):479–487

    Article  PubMed  CAS  Google Scholar 

  161. Vanoevelen J, Raeymaekers L, Parys JB, De Smedt H, Van Baelen K, Callewaert G, Wuytack F, Missiaen L (2004) Inositol trisphosphate producing agonists do not mobilize the thapsigargin-insensitive part of the endoplasmic-reticulum and Golgi Ca2+ store. Cell Calcium 35(2):115–121

    Article  PubMed  CAS  Google Scholar 

  162. Missiaen L, Van Acker K, Parys JB, De Smedt H, Van Baelen K, Weidema AF, Vanoevelen J, Raeymaekers L, Renders J, Callewaert G, Rizzuto R, Wuytack F (2001) Baseline cytosolic Ca2+ oscillations derived from a non-endoplasmic reticulum Ca2+ store. J Biol Chem 276(42):39161–39170

    Article  PubMed  CAS  Google Scholar 

  163. Vanoevelen J, Raeymaekers L, Dode L, Parys JB, De Smedt H, Callewaert G, Wuytack F, Missiaen L (2005) Cytosolic Ca2+ signals depending on the functional state of the Golgi in HeLa cells. Cell Calcium 38(5):489–495

    Article  PubMed  CAS  Google Scholar 

  164. Missiaen L, Vanoevelen J, Parys JB, Raeymaekers L, De Smedt H, Callewaert G, Erneux C, Wuytack F (2002) Ca2+ uptake and release properties of a thapsigargin-insensitive nonmitochondrial Ca2+ store in A7r5 and 16HBE14o- cells. J Biol Chem 277(9):6898–6902

    Article  PubMed  CAS  Google Scholar 

  165. Taylor RS, Jones SM, Dahl RH, Nordeen MH, Howell KE (1997) Characterization of the Golgi complex cleared of proteins in transit and examination of calcium uptake activities. Mol Biol Cell 8(10):1911–1931

    PubMed  CAS  Google Scholar 

  166. Van Baelen K, Vanoevelen J, Callewaert G, Parys JB, De Smedt H, Raeymaekers L, Rizzuto R, Missiaen L, Wuytack F (2003) The contribution of the SPCA1 Ca2+ pump to the Ca2+ accumulation in the Golgi apparatus of HeLa cells assessed via RNA-mediated interference. Biochem Biophys Res Commun 306(2):430–436

    Article  PubMed  CAS  Google Scholar 

  167. Vangheluwe P, Sepulveda MR, Missiaen L, Raeymaekers L, Wuytack F, Vanoevelen J (2009) Intracellular Ca2+- and Mn2+-transport ATPases. Chem Rev 109(10):4733–4759

    Article  PubMed  CAS  Google Scholar 

  168. Xiang M, Mohamalawari D, Rao R (2005) A novel isoform of the secretory pathway Ca2+ , Mn2+ -ATPase, hSPCA2, has unusual properties and is expressed in the brain. J Biol Chem 280(12):11608–11614

    Article  PubMed  CAS  Google Scholar 

  169. Vanoevelen J, Dode L, Van Baelen K, Fairclough RJ, Missiaen L, Raeymaekers L, Wuytack F (2005) The secretory pathway Ca2+/Mn2+-ATPase 2 is a Golgi-localized pump with high affinity for Ca2+ ions. J Biol Chem 280(24):22800–22808

    Article  PubMed  CAS  Google Scholar 

  170. Behne MJ, Tu CL, Aronchik I, Epstein E, Bench G, Bikle DD, Pozzan T, Mauro TM (2003) Human keratinocyte ATP2C1 localizes to the Golgi and controls Golgi Ca2+ stores. J Invest Dermatol 121(4):688–694

    Article  PubMed  CAS  Google Scholar 

  171. Mitchell KJ, Tsuboi T, Rutter GA (2004) Role for plasma membrane-related Ca2+-ATPase-1 (ATP2C1) in pancreatic beta-cell Ca2+ homeostasis revealed by RNA silencing. Diabetes 53(2):393–400

    Article  PubMed  CAS  Google Scholar 

  172. Yoshimoto A, Nakanishi K, Anzai T, Komine S (1990) Effects of inositol 1, 4, 5-trisphosphate on calcium release from the endoplasmic reticulum and Golgi apparatus in mouse mammary epithelial cells: a comparison during pregnancy and lactation. Cell Biochem Funct 8(4):191–198

    Article  PubMed  CAS  Google Scholar 

  173. Cifuentes F, Gonzalez CE, Fiordelisio T, Guerrero G, Lai FA, Hernandez-Cruz A (2001) A ryanodine fluorescent derivative reveals the presence of high-affinity ryanodine binding sites in the Golgi complex of rat sympathetic neurons, with possible functional roles in intracellular Ca2+ signaling. Cell Signal 13(5):353–362

    Article  PubMed  CAS  Google Scholar 

  174. Lissandron V, Podini P, Pizzo P, Pozzan T (2010) Unique characteristics of Ca2+ homeostasis of the trans-Golgi compartment. Proc Natl Acad Sci USA 107(20):9198–9203

    Article  PubMed  CAS  Google Scholar 

  175. Pizzo P, Lissandron V, Capitanio P, Pozzan T (2011) Ca(2+) signalling in the Golgi apparatus. Cell Calcium

  176. Lin P, Le-Niculescu H, Hofmeister R, McCaffery JM, Jin M, Hennemann H, McQuistan T, De Vries L, Farquhar MG (1998) The mammalian calcium-binding protein, nucleobindin (CALNUC), is a Golgi resident protein. J Cell Biol 141(7):1515–1527

    Article  PubMed  CAS  Google Scholar 

  177. Mitchell KJ, Pinton P, Varadi A, Tacchetti C, Ainscow EK, Pozzan T, Rizzuto R, Rutter GA (2001) Dense core secretory vesicles revealed as a dynamic Ca2+ store in neuroendocrine cells with a vesicle-associated membrane protein aequorin chimaera. J Cell Biol 155(1):41–51

    Article  PubMed  CAS  Google Scholar 

  178. Palmer AE, Giacomello M, Kortemme T, Hires SA, Lev-Ram V, Baker D, Tsien RY (2006) Ca2+ indicators based on computationally redesigned calmodulin-peptide pairs. Chem Biol 13(5):521–530

    Article  PubMed  CAS  Google Scholar 

  179. Zerfaoui M, Fukuda M, Langlet C, Mathieu S, Suzuki M, Lombardo D, El-Battari A (2002) The cytosolic and transmembrane domains of the beta 1, 6 N-acetylglucosaminyltransferase (C2GnT) function as a cis to medial/Golgi-targeting determinant. Glycobiology 12(1):15–24

    Article  PubMed  CAS  Google Scholar 

  180. Austin CD, Shields D (1996) Prosomatostatin processing in permeabilized cells. Calcium is required for prohormone cleavage but not formation of nascent secretory vesicles. J Biol Chem 271:1194–1199

    Article  PubMed  CAS  Google Scholar 

  181. Duncan JS, Burgoyne RD (1996) Characterization of the effects of Ca2+ depletion on the synthesis, phosphorylation and secretion of caseins in lactating mammary epithelial cells. Biochem J 317:487–493

    PubMed  CAS  Google Scholar 

  182. Ramos-Castaneda J, Park YN, Liu M, Hauser K, Rudolph H, Shull GE, Jonkman MF, Mori K, Ikeda S, Ogawa H, Arvan P (2005) Deficiency of ATP2C1, a Golgi ion pump, induces secretory pathway defects in endoplasmic reticulum (ER)-associated degradation and sensitivity to ER stress. J Biol Chem 280(10):9467–9473

    Article  PubMed  CAS  Google Scholar 

  183. Foggia L, Hovnanian A (2004) Calcium pump disorders of the skin. Am J Med Genet C Semin Med Genet 131C(1):20–31. doi:10.1002/ajmg.c.30031

    Article  PubMed  Google Scholar 

  184. Missiaen L, Raeymaekers L, Dode L, Vanoevelen J, Van Baelen K, Parys JB, Callewaert G, De Smedt H, Segaert S, Wuytack F (2004) SPCA1 pumps and Hailey–Hailey disease. Biochem Biophys Res Commun 322(4):1204–1213

    Article  PubMed  CAS  Google Scholar 

  185. Holst VA, Fair KP, Wilson BB, Patterson JW (2000) Squamous cell carcinoma arising in Hailey–Hailey disease. J Am Acad Dermatol 43(2 Pt 2):368–371

    Article  PubMed  CAS  Google Scholar 

  186. Grice DM, Vetter I, Faddy HM, Kenny PA, Roberts-Thomson SJ, Monteith GR (2010) Golgi calcium pump secretory pathway calcium ATPase 1 (SPCA1) is a key regulator of insulin-like growth factor receptor (IGF1R) processing in the basal-like breast cancer cell line MDA-MB-231. J Biol Chem 285(48):37458–37466

    Article  PubMed  CAS  Google Scholar 

  187. Rippe K (2007) Dynamic organization of the cell nucleus. Curr Opin Genet Dev 17(5):373–380

    Article  PubMed  CAS  Google Scholar 

  188. Hardingham GE, Arnold FJL, Bading H (2001) A calcium microdomain near NMDA receptors: on switch for ERK-dependent synapse-to-nucleus communication. Nat Neurosci 4:565–566

    Article  PubMed  CAS  Google Scholar 

  189. Hardingham GE, Chawla S, Johnson CM, Bading H (1997) Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature 385:260–265

    Article  PubMed  CAS  Google Scholar 

  190. Dolmetsch RE, Xu K, Lewis RS (1998) Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392:933–936

    Article  PubMed  CAS  Google Scholar 

  191. Bootman MD, Fearnley C, Smyrnias I, MacDonald F, Roderick HL (2009) An update on nuclear calcium signalling. J Cell Sci 122(Pt 14):2337–2350

    Article  PubMed  CAS  Google Scholar 

  192. Hetzer MW (2010) The nuclear envelope. Cold Spring Harbor Perspect Biol 2(3):a000539

    Article  CAS  Google Scholar 

  193. Ross CA, Meldolesi J, Milner TA, Satoh T, Supattapone S, Snyder SH (1989) Inositol 1, 4, 5-trisphosphate receptor localized to endoplasmic reticulum in cerebellar Purkinje neurons. Nature 339(6224):468–470

    Article  PubMed  CAS  Google Scholar 

  194. Gerasimenko J, Maruyama Y, Tepikin A, Petersen OH, Gerasimenko O (2003) Calcium signalling in and around the nuclear envelope. Biochem Soc Trans 31(Pt 1):76–78

    PubMed  CAS  Google Scholar 

  195. Nicotera P, McConkey DJ, Jones DP, Orrenius S (1989) ATP stimulates Ca2+ uptake and increases the free Ca2+ concentration in isolated rat liver nuclei. Proc Natl Acad Sci USA 86(2):453–457

    Article  PubMed  CAS  Google Scholar 

  196. Malviya AN, Rogue P, Vincendon G (1990) Stereospecific inositol 1, 4, 5-[32P]trisphosphate binding to isolated rat liver nuclei: evidence for inositol trisphosphate receptor-mediated calcium release from the nucleus. Proc Natl Acad Sci USA 87(23):9270–9274

    Article  PubMed  CAS  Google Scholar 

  197. Walton PD, Airey JA, Sutko JL, Beck CF, Mignery GA, Sudhof TC, Deerinck TJ, Ellisman MH (1991) Ryanodine and inositol trisphosphate receptors coexist in avian cerebellar Purkinje neurons. J Cell Biol 113(5):1145–1157

    Article  PubMed  CAS  Google Scholar 

  198. Lanini L, Bachs O, Carafoli E (1992) The calcium pump of the liver nuclear membrane is identical to that of endoplasmic reticulum. J Biol Chem 267(16):11548–11552

    PubMed  CAS  Google Scholar 

  199. Stehno-Bittel L, Luckhoff A, Clapham DE (1995) Calcium release from the nucleus by InsP3 receptor channels. Neuron 14(1):163–167

    Article  PubMed  CAS  Google Scholar 

  200. Gerasimenko OV, Gerasimenko JV, Tepikin AV, Petersen OH (1995) ATP-dependent accumulation and inositol trisphosphate- or cyclic ADP-ribose-mediated release of Ca2+ from the nuclear envelope. Cell 80(3):439–444

    Article  PubMed  CAS  Google Scholar 

  201. Humbert JP, Matter N, Artault JC, Koppler P, Malviya AN (1996) Inositol 1, 4, 5-trisphosphate receptor is located to the inner nuclear membrane vindicating regulation of nuclear calcium signaling by inositol 1, 4, 5-trisphosphate. Discrete distribution of inositol phosphate receptors to inner and outer nuclear membranes. J Biol Chem 271(1):478–485

    Article  PubMed  CAS  Google Scholar 

  202. Abrenica B, Gilchrist JS (2000) Nucleoplasmic Ca(2+)loading is regulated by mobilization of perinuclear Ca(2+). Cell Calcium 28(2):127–136

    Article  PubMed  CAS  Google Scholar 

  203. Marius P, Guerra MT, Nathanson MH, Ehrlich BE, Leite MF (2006) Calcium release from ryanodine receptors in the nucleoplasmic reticulum. Cell Calcium 39(1):65–73

    Article  PubMed  CAS  Google Scholar 

  204. Bezin S, Charpentier G, Lee HC, Baux G, Fossier P, Cancela JM (2008) Regulation of nuclear Ca2+ signaling by translocation of the Ca2+ messenger synthesizing enzyme ADP-ribosyl cyclase during neuronal depolarization. J Biol Chem 283(41):27859–27870

    Article  PubMed  CAS  Google Scholar 

  205. Bezin S, Fossier P, Cancela JM (2008) Nucleoplasmic reticulum is not essential in nuclear calcium signalling mediated by cyclic ADPribose in primary neurons. Pflugers Archiv Eur J Physiol 456(3):581–586

    Article  CAS  Google Scholar 

  206. Hoelz A, Debler EW, Blobel G (2011) The structure of the nuclear pore complex. Annu Rev Biochem 80:613–643

    Article  PubMed  CAS  Google Scholar 

  207. Peters R (1984) Nucleo-cytoplasmic flux and intracellular mobility in single hepatocytes measured by fluorescence microphotolysis. EMBO J 3(8):1831–1836

    PubMed  CAS  Google Scholar 

  208. O’Malley DM (1994) Calcium permeability of the neuronal nuclear envelope: evaluation using confocal volumes and intracellular perfusion. J Neurosci 14(10):5741–5758

    PubMed  Google Scholar 

  209. Kapon R, Naim B, Zbaida D, Nevo R, Tsabari O, Reich Z (2010) Permeating the nuclear pore complex. Nucleus (Austin Tex) 1(6):475–480

    Google Scholar 

  210. Leite MF, Thrower EC, Echevarria W, Koulen P, Hirata K, Bennett AM, Ehrlich BE, Nathanson MH (2003) Nuclear and cytosolic calcium are regulated independently. Proc Natl Acad Sci USA 100(5):2975–2980

    Article  PubMed  CAS  Google Scholar 

  211. Lui PP, Kong SK, Fung KP, Lee CY (1998) The rise of nuclear and cytosolic Ca2+ can be uncoupled in HeLa cells. Pflugers Archiv Eur J Physiol 436(3):371–376

    Article  CAS  Google Scholar 

  212. Alonso MT, Villalobos C, Chamero P, Alvarez J, Garcia-Sancho J (2006) Calcium microdomains in mitochondria and nucleus. Cell Calcium 40(5–6):513–525

    Article  PubMed  CAS  Google Scholar 

  213. Brini M, Murgia M, Pasti L, Picard D, Pozzan T, Rizzuto R (1993) Nuclear Ca2+ concentration measured with specifically targeted recombinant aequorin. EMBO J 12(12):4813–4819

    PubMed  CAS  Google Scholar 

  214. Nagai T, Sawano A, Park ES, Miyawaki A (2001) Circularly permuted green fluorescent proteins engineered to sense Ca2+. Proc Natl Acad Sci USA 98(6):3197–3202

    Article  PubMed  CAS  Google Scholar 

  215. Giacomello M, Drago I, Bortolozzi M, Scorzeto M, Gianelle A, Pizzo P, Pozzan T (2010) Ca2+ hot spots on the mitochondrial surface are generated by Ca2+ mobilization from stores, but not by activation of store-operated Ca2+ channels. Mol Cell 38(2):280–290

    Article  PubMed  CAS  Google Scholar 

  216. Manjarres IM, Chamero P, Domingo B, Molina F, Llopis J, Alonso MT, Garcia-Sancho J (2008) Red and green aequorins for simultaneous monitoring of Ca2+ signals from two different organelles. Pflugers Archiv Eur J Physiol 455(5):961–970

    Article  CAS  Google Scholar 

  217. Allbritton NL, Oancea E, Kuhn MA, Meyer T (1994) Source of nuclear calcium signals. Proc Natl Acad Sci USA 91(26):12458–12462

    Article  PubMed  CAS  Google Scholar 

  218. Hernandez-Cruz A, Sala F, Adams PR (1990) Subcellular calcium transients visualized by confocal microscopy in a voltage-clamped vertebrate neuron. Science 247:858–862

    Article  PubMed  CAS  Google Scholar 

  219. Lin C, Hajnoczky G, Thomas AP (1994) Propagation of cytosolic calcium waves into the nuclei of hepatocytes. Cell Calcium 16(4):247–258

    Article  PubMed  CAS  Google Scholar 

  220. Shirakawa H, Miyazaki S (1996) Spatiotemporal analysis of calcium dynamics in the nucleus of hamster oocytes. J Physiol 494(Pt 1):29–40

    PubMed  CAS  Google Scholar 

  221. Nakazawa H, Murphy TH (1999) Activation of nuclear calcium dynamics by synaptic stimulation in cultured cortical neurons. J Neurochem 73(3):1075–1083

    Article  PubMed  CAS  Google Scholar 

  222. Zhao L, Brinton RD (2002) Vasopressin-induced cytoplasmic and nuclear calcium signaling in cultured cortical astrocytes. Brain Res 943(1):117–131

    Article  PubMed  CAS  Google Scholar 

  223. Power JM, Sah P (2002) Nuclear calcium signaling evoked by cholinergic stimulation in hippocampal CA1 pyramidal neurons. J Neurosci 22(9):3454–3462

    PubMed  CAS  Google Scholar 

  224. Power JM, Sah P (2007) Distribution of IP3-mediated calcium responses and their role in nuclear signalling in rat basolateral amygdala neurons. J Physiol 580(Pt.3):835–857

    Article  PubMed  CAS  Google Scholar 

  225. Williams DA, Fogarty KE, Tsien RY, Fay FS (1985) Calcium gradients in single smooth muscle cells revealed by the digital imaging microscope using Fura-2. Nature 318(6046):558–561

    Article  PubMed  CAS  Google Scholar 

  226. al-Mohanna FA, Caddy KW, Bolsover SR (1994) The nucleus is insulated from large cytosolic calcium ion changes. Nature 367(6465):745–750

    Article  PubMed  CAS  Google Scholar 

  227. Badminton MN, Kendall JM, Sala-Newby G, Campbell AK (1995) Nucleoplasmin-targeted aequorin provides evidence for a nuclear calcium barrier. Exp Cell Res 216(1):236–243

    Article  PubMed  CAS  Google Scholar 

  228. Genka C, Ishida H, Ichimori K, Hirota Y, Tanaami T, Nakazawa H (1999) Visualization of biphasic Ca2+ diffusion from cytosol to nucleus in contracting adult rat cardiac myocytes with an ultra-fast confocal imaging system. Cell Calcium 25(3):199–208

    Article  PubMed  CAS  Google Scholar 

  229. Chamero P, Villalobos C, Alonso MT, Garcia-Sancho J (2002) Dampening of cytosolic Ca2+ oscillations on propagation to nucleus. J Biol Chem 277(52):50226–50229

    Article  PubMed  CAS  Google Scholar 

  230. Assandri R, Mazzanti M (1997) Ionic permeability on isolated mouse liver nuclei: influence of ATP and Ca2+. J Membr Biol 157(3):301–309

    Article  PubMed  CAS  Google Scholar 

  231. Greber UF, Gerace L (1995) Depletion of calcium from the lumen of endoplasmic reticulum reversibly inhibits passive diffusion and signal-mediated transport into the nucleus. J Cell Biol 128(1–2):5–14

    Article  PubMed  CAS  Google Scholar 

  232. Perez-Terzic C, Pyle J, Jaconi M, Stehno-Bittel L, Clapham DE (1996) Conformational states of the nuclear pore complex induced by depletion of nuclear Ca2+ stores. Science (New York NY) 273(5283):1875–1877

    Article  CAS  Google Scholar 

  233. Bustamante JO, Michelette ER, Geibel JP, Dean DA, Hanover JA, McDonnell TJ (2000) Calcium, ATP and nuclear pore channel gating. Pflugers Archiv Eur J Physiol 439(4):433–444

    Article  CAS  Google Scholar 

  234. Strubing C, Clapham DE (1999) Active nuclear import and export is independent of lumenal Ca2+ stores in intact mammalian cells. J Gen Physiol 113(2):239–248

    Article  PubMed  CAS  Google Scholar 

  235. Fricker M, Hollinshead M, White N, Vaux D (1997) The convoluted nucleus. Trends Cell Biol 7(5):181

    Article  PubMed  CAS  Google Scholar 

  236. Lui PP, Kong SK, Kwok TT, Lee CY (1998) The nucleus of HeLa cell contains tubular structures for Ca2+ signalling. Biochem Biophys Res Commun 247(1):88–93

    Article  PubMed  CAS  Google Scholar 

  237. Lui PP, Lee CY, Tsang D, Kong SK (1998) Ca2+ is released from the nuclear tubular structure into nucleoplasm in C6 glioma cells after stimulation with phorbol ester. FEBS Lett 432(1–2):82–87

    Article  PubMed  CAS  Google Scholar 

  238. Echevarria W, Leite MF, Guerra MT, Zipfel WR, Nathanson MH (2003) Regulation of calcium signals in the nucleus by a nucleoplasmic reticulum. Nat Cell Biol 5(5):440–446

    Article  PubMed  CAS  Google Scholar 

  239. Guatimosim S, Amaya MJ, Guerra MT, Aguiar CJ, Goes AM, Gomez-Viquez NL, Rodrigues MA, Gomes DA, Martins-Cruz J, Lederer WJ, Leite MF (2008) Nuclear Ca2+ regulates cardiomyocyte function. Cell Calcium 44(2):230–242

    Article  PubMed  CAS  Google Scholar 

  240. Cardenas C, Liberona JL, Molgo J, Colasante C, Mignery GA, Jaimovich E (2005) Nuclear inositol 1, 4, 5-trisphosphate receptors regulate local Ca2 + transients and modulate cAMP response element binding protein phosphorylation. J Cell Sci 118(Pt 14):3131–3140

    Article  PubMed  CAS  Google Scholar 

  241. Huh YH, Huh SK, Chu SY, Kweon HS, Yoo SH (2006) Presence of a putative vesicular inositol 1, 4, 5-trisphosphate-sensitive nucleoplasmic Ca2+ store. Biochemistry 45(5):1362–1373

    Article  PubMed  CAS  Google Scholar 

  242. Huh YH, Yoo SH (2003) Presence of the inositol 1, 4, 5-triphosphate receptor isoforms in the nucleoplasm. FEBS Lett 555(2):411–418

    Article  PubMed  CAS  Google Scholar 

  243. Katagiri S, Takamatsu T, Minamikawa T, Fujita S (1993) Secretagogue-induced calcium wave shows higher and prolonged transients of nuclear calcium concentration in mast cells. FEBS Lett 334(3):343–346

    Article  PubMed  CAS  Google Scholar 

  244. Fox JL, Burgstahler AD, Nathanson MH (1997) Mechanism of long-range Ca2+ signalling in the nucleus of isolated rat hepatocytes. Biochem J 326(Pt 2):491–495

    PubMed  CAS  Google Scholar 

  245. Lipp P, Thomas D, Berridge MJ, Bootman MD (1997) Nuclear calcium signalling by individual cytoplasmic calcium puffs. EMBO J 16(23):7166–7173

    Article  PubMed  CAS  Google Scholar 

  246. Giorgi C, De Stefani D, Bononi A, Rizzuto R, Pinton P (2009) Structural and functional link between the mitochondrial network and the endoplasmic reticulum. Int J Biochem Cell Biol 41(10):1817–1827

    Article  PubMed  CAS  Google Scholar 

  247. Heath-Engel HM, Shore GC (2006) Mitochondrial membrane dynamics, cristae remodelling and apoptosis. Biochim Biophys Acta 1763(5–6):549–560

    Article  PubMed  CAS  Google Scholar 

  248. Contreras L, Drago I, Zampese E, Pozzan T (2010) Mitochondria: the calcium connection. Biochim Biophys Acta 1797(6–7):607–618

    PubMed  CAS  Google Scholar 

  249. Giacomello M, Drago I, Pizzo P, Pozzan T (2007) Mitochondrial Ca2+ as a key regulator of cell life and death. Cell Death Differ 14(7):1267–1274

    Article  PubMed  CAS  Google Scholar 

  250. Campello S, Scorrano L (2010) Mitochondrial shape changes: orchestrating cell pathophysiology. EMBO Rep 11(9):678–684

    Article  PubMed  CAS  Google Scholar 

  251. Sheridan C, Martin SJ (2010) Mitochondrial fission/fusion dynamics and apoptosis. Mitochondrion 10(6):640–648

    Article  PubMed  CAS  Google Scholar 

  252. Szabadkai G, Simoni AM, Chami M, Wieckowski MR, Youle RJ, Rizzuto R (2004) Drp-1-dependent division of the mitochondrial network blocks intraorganellar Ca2+ waves and protects against Ca2+-mediated apoptosis. Mol Cell 16(1):59–68

    Article  PubMed  CAS  Google Scholar 

  253. Jeyaraju DV, Cisbani G, Pellegrini L (2009) Calcium regulation of mitochondria motility and morphology. Biochim Biophys Acta 1787(11):1363–1373

    Article  PubMed  CAS  Google Scholar 

  254. Frederick RL, Shaw JM (2007) Moving mitochondria: establishing distribution of an essential organelle. Traffic (Copenhagen Denmark) 8(12):1668–1675

    Article  CAS  Google Scholar 

  255. Nangaku M, Sato-Yoshitake R, Okada Y, Noda Y, Takemura R, Yamazaki H, Hirokawa N (1994) KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell 79(7):1209–1220

    Article  PubMed  CAS  Google Scholar 

  256. Glater EE, Megeath LJ, Stowers RS, Schwarz TL (2006) Axonal transport of mitochondria requires milton to recruit kinesin heavy chain and is light chain independent. J Cell Biol 173(4):545–557

    Article  PubMed  CAS  Google Scholar 

  257. Wang X, Schwarz TL (2009) The mechanism of Ca2+ -dependent regulation of kinesin-mediated mitochondrial motility. Cell 136(1):163–174

    Article  PubMed  CAS  Google Scholar 

  258. Saotome M, Safiulina D, Szabadkai G, Das S, Fransson A, Aspenstrom P, Rizzuto R, Hajnoczky G (2008) Bidirectional Ca2+-dependent control of mitochondrial dynamics by the Miro GTPase. Proc Natl Acad Sci USA 105(52):20728–20733

    Article  PubMed  CAS  Google Scholar 

  259. Macaskill AF, Rinholm JE, Twelvetrees AE, Arancibia-Carcamo IL, Muir J, Fransson A, Aspenstrom P, Attwell D, Kittler JT (2009) Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 61(4):541–555

    Article  PubMed  CAS  Google Scholar 

  260. MacAskill AF, Kittler JT (2010) Control of mitochondrial transport and localization in neurons. Trends Cell Biol 20(2):102–112

    Article  PubMed  CAS  Google Scholar 

  261. Denton RM (2009) Regulation of mitochondrial dehydrogenases by calcium ions. Biochim Biophys Acta 1787(11):1309–1316

    Article  PubMed  CAS  Google Scholar 

  262. Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, Lifshitz LM, Tuft RA, Pozzan T (1998) Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 280(5370):1763–1766

    Article  PubMed  CAS  Google Scholar 

  263. Palmieri L, Pardo B, Lasorsa FM, del Arco A, Kobayashi K, Iijima M, Runswick MJ, Walker JE, Saheki T, Satrustegui J, Palmieri F (2001) Citrin and aralar1 are Ca2+-stimulated aspartate/glutamate transporters in mitochondria. EMBO J 20(18):5060–5069

    Article  PubMed  CAS  Google Scholar 

  264. Lasorsa FM, Pinton P, Palmieri L, Fiermonte G, Rizzuto R, Palmieri F (2003) Recombinant expression of the Ca2+-sensitive aspartate/glutamate carrier increases mitochondrial ATP production in agonist-stimulated Chinese hamster ovary cells. J Biol Chem 278(40):38686–38692

    Article  PubMed  CAS  Google Scholar 

  265. Pinton P, Giorgi C, Siviero R, Zecchini E, Rizzuto R (2008) Calcium and apoptosis: ER–mitochondria Ca2+ transfer in the control of apoptosis. Oncogene 27(50):6407–6418

    Article  PubMed  CAS  Google Scholar 

  266. Rasola A, Bernardi P (2011) Mitochondrial permeability transition in Ca(2+)-dependent apoptosis and necrosis. Cell Calcium

  267. Szalai G, Krishnamurthy R, Hajnoczky G (1999) Apoptosis driven by IP(3)-linked mitochondrial calcium signals. EMBO J 18(22):6349–6361

    Article  PubMed  CAS  Google Scholar 

  268. Pinton P, Ferrari D, Rapizzi E, Di Virgilio F, Pozzan T, Rizzuto R (2001) The Ca2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: significance for the molecular mechanism of Bcl-2 action. EMBO J 20(11):2690–2701

    Article  PubMed  CAS  Google Scholar 

  269. Deluca HF, Engstrom GW (1961) Calcium uptake by rat kidney mitochondria. Proc Natl Acad Sci USA 47:1744–1750

    Article  PubMed  CAS  Google Scholar 

  270. Vasington F, Murphy JV (1962) Ca2+ uptake by rat kidney mitochondria and its dependence on respiration and phosphorylation. J Biol Chem 237:2670–2677

    PubMed  CAS  Google Scholar 

  271. Colombini M (1980) Structure and mode of action of a voltage dependent anion-selective channel (VDAC) located in the outer mitochondrial membrane. Ann NY Acad Sci 341:552–563

    Article  PubMed  CAS  Google Scholar 

  272. Rizzuto R, Simpson AW, Brini M, Pozzan T (1992) Rapid changes of mitochondrial Ca2+ revealed by specifically targeted recombinant aequorin. Nature 358(6384):325–327

    Article  PubMed  CAS  Google Scholar 

  273. Miyata H, Silverman HS, Sollott SJ, Lakatta EG, Stern MD, Hansford RG (1991) Measurement of mitochondrial free Ca2+ concentration in living single rat cardiac myocytes. Am J Physiol Heart Circ Physiol 261:H1123–H1134

    CAS  Google Scholar 

  274. Filippin L, Magalhães PJ, Di Benedetto G, Colella M, Pozzan T (2003) Stable interactions between mitochondria and endoplasmic reticulum allow rapid accumulation of calcium in a subpopulation of mitochondria. J Biol Chem 278:39224–39234

    Article  PubMed  CAS  Google Scholar 

  275. Pozzan T, Rizzuto R (2000) The renaissance of mitochondrial calcium transport. Eur J Biochem 267:5269–5273

    Article  PubMed  CAS  Google Scholar 

  276. Rizzuto R, Brini M, Murgia M, Pozzan T (1993) Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria. Science 262(5134):744–747

    Article  PubMed  CAS  Google Scholar 

  277. Rizzuto R, Pozzan T (2006) Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol Rev 86(1):369–408

    Article  PubMed  CAS  Google Scholar 

  278. Rizzuto R, Pinton P, Brini M, Chiesa A, Filippin L, Pozzan T (1999) Mitochondria as biosensors of calcium microdomains. Cell Calcium 26(5):193–199

    Article  PubMed  CAS  Google Scholar 

  279. Csordas G, Varnai P, Golenar T, Roy S, Purkins G, Schneider TG, Balla T, Hajnoczky G (2010) Imaging interorganelle contacts and local calcium dynamics at the ER-mitochondrial interface. Mol Cell 39(1):121–132

    Article  PubMed  CAS  Google Scholar 

  280. Hoppe UC (2010) Mitochondrial calcium channels. FEBS Lett 584(10):1975–1981

    Article  PubMed  CAS  Google Scholar 

  281. Kirichok Y, Krapivinsky G, Clapham DE (2004) The mitochondrial calcium uniporter is a highly selective ion channel. Nature 427(6972):360–364

    Article  PubMed  CAS  Google Scholar 

  282. Bragadin M, Pozzan T, Azzone GF (1979) Kinetics of Ca2+ carrier in rat liver mitochondria. Biochemistry 18(26):5972–5978

    Article  PubMed  CAS  Google Scholar 

  283. Perocchi F, Gohil VM, Girgis HS, Bao XR, McCombs JE, Palmer AE, Mootha VK (2010) MICU1 encodes a mitochondrial EF hand protein required for Ca(2+) uptake. Nature 467(7313):291–296

    Article  PubMed  CAS  Google Scholar 

  284. Baughman JM, Perocchi F, Girgis HS, Plovanich M, Belcher-Timme CA, Sancak Y, Bao XR, Strittmatter L, Goldberger O, Bogorad RL, Koteliansky V, Mootha VK (2011) Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature PMID:21685886

  285. De Stefani D, Raffaello A, Teardo E, Szabo I, Rizzuto R (2011) A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature PMID:21685888

  286. Cardenas C, Miller RA, Smith I, Bui T, Molgo J, Muller M, Vais H, Cheung KH, Yang J, Parker I, Thompson CB, Birnbaum MJ, Hallows KR, Foskett JK (2010) Essential regulation of cell bioenergetics by constitutive InsP3 receptor Ca2+ transfer to mitochondria. Cell 142(2):270–283

    Article  PubMed  CAS  Google Scholar 

  287. Csordas G, Renken C, Varnai P, Walter L, Weaver D, Buttle KF, Balla T, Mannella CA, Hajnoczky G (2006) Structural and functional features and significance of the physical linkage between ER and mitochondria. J Cell Biol 174(7):915–921

    Article  PubMed  CAS  Google Scholar 

  288. Bravo R, Vicencio JM, Parra V, Troncoso R, Munoz JP, Bui M, Quiroga C, Rodriguez AE, Verdejo HE, Ferreira J, Iglewski M, Chiong M, Simmen T, Zorzano A, Hill JA, Rothermel BA, Szabadkai G, Lavandero S (2011) Increased ER-mitochondrial coupling promotes mitochondrial respiration and bioenergetics during early phases of ER stress. J Cell Sci 124(Pt 13):2143–2152

    Article  PubMed  CAS  Google Scholar 

  289. Szabadkai G, Bianchi K, Varnai P, De Stefani D, Wieckowski MR, Cavagna D, Nagy AI, Balla T, Rizzuto R (2006) Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels. J Cell Biol 175(6):901–911

    Article  PubMed  CAS  Google Scholar 

  290. de Brito OM, Scorrano L (2008) Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature 456(7222):605–610

    Article  PubMed  CAS  Google Scholar 

  291. Iwasawa R, Mahul-Mellier AL, Datler C, Pazarentzos E, Grimm S (2011) Fis1 and Bap31 bridge the mitochondria–ER interface to establish a platform for apoptosis induction. EMBO J 30(3):556–568

    Article  PubMed  CAS  Google Scholar 

  292. Cerqua C, Anesti V, Pyakurel A, Liu D, Naon D, Wiche G, Baffa R, Dimmer KS, Scorrano L (2010) Trichoplein/mitostatin regulates endoplasmic reticulum-mitochondria juxtaposition. EMBO Rep 11(11):854–860

    Article  PubMed  CAS  Google Scholar 

  293. Simmen T, Aslan JE, Blagoveshchenskaya AD, Thomas L, Wan L, Xiang Y, Feliciangeli SF, Hung CH, Crump CM, Thomas G (2005) PACS-2 controls endoplasmic reticulum-mitochondria communication and Bid-mediated apoptosis. EMBO J 24(4):717–729

    Article  PubMed  CAS  Google Scholar 

  294. Kornmann B, Currie E, Collins SR, Schuldiner M, Nunnari J, Weissman JS, Walter P (2009) An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325(5939):477–481

    Article  PubMed  CAS  Google Scholar 

  295. Zampese E, Fasolato C, Kipanyula MJ, Bortolozzi M, Pozzan T, Pizzo P (2011) Presenilin 2 modulates endoplasmic reticulum (ER)–mitochondria interactions and Ca2+ cross-talk. Proc Natl Acad Sci USA 108(7):2777–2782

    Article  PubMed  CAS  Google Scholar 

  296. Zampese E, Fasolato C, Pozzan T, Pizzo P (2011) Presenilin-2 modulation of ER–mitochondria interactions. Commun Integr Biol 4(3):357–360

    Article  PubMed  CAS  Google Scholar 

  297. Hayashi T, Rizzuto R, Hajnoczky G, Su TP (2009) MAM: more than just a housekeeper. Trends Cell Biol 19(2):81–88

    Article  PubMed  CAS  Google Scholar 

  298. Hayashi T, Su TP (2010) Cholesterol at the endoplasmic reticulum: roles of the sigma-1 receptor chaperone and implications thereof in human diseases. Subcell Biochem 51:381–398

    Article  PubMed  CAS  Google Scholar 

  299. Palty R, Silverman WF, Hershfinkel M, Caporale T, Sensi SL, Parnis J, Nolte C, Fishman D, Shoshan-Barmatz V, Herrmann S, Khananshvili D, Sekler I (2010) NCLX is an essential component of mitochondrial Na+/Ca2+ exchange. Proc Natl Acad Sci USA 107(1):436–441

    Article  PubMed  CAS  Google Scholar 

  300. Puskin JS, Gunter TE, Gunter KK, Russell PR (1976) Evidence for more than one Ca2+ transport mechanism in mitochondria. Biochemistry 15(17):3834–3842

    Article  PubMed  CAS  Google Scholar 

  301. Walsh C, Barrow S, Voronina S, Chvanov M, Petersen OH, Tepikin A (2009) Modulation of calcium signalling by mitochondria. Biochim Biophys Acta 1787(11):1374–1382

    Article  PubMed  CAS  Google Scholar 

  302. Villalobos C, Nunez L, Montero M, Garcia AG, Alonso MT, Chamero P, Alvarez J, Garcia-Sancho J (2002) Redistribution of Ca2+ among cytosol and organella during stimulation of bovine chromaffin cells. FASEB J 16(3):343–353

    Article  PubMed  CAS  Google Scholar 

  303. Ishii K, Hirose K, Iino M (2006) Ca2+ shuttling between endoplasmic reticulum and mitochondria underlying Ca2+ oscillations. EMBO Rep 7(4):390–396

    Article  PubMed  CAS  Google Scholar 

  304. Arnaudeau S, Kelley WL, Walsh JV Jr, Demaurex N (2001) Mitochondria recycle Ca2+ to the endoplasmic reticulum and prevent the depletion of neighboring endoplasmic reticulum regions. J Biol Chem 276(31):29430–29439

    Article  PubMed  CAS  Google Scholar 

  305. Tinel H, Cancela JM, Mogami H, Gerasimenko JV, Gerasimenko OV, Tepikin AV, Petersen OH (1999) Active mitochondria surrounding the pancreatic acinar granule region prevent spreading of inositol trisphosphate-evoked local cytosolic Ca2+ signals. EMBO J 18(18):4999–5008

    Article  PubMed  CAS  Google Scholar 

  306. Seksek O, Biwersi J, Verkman AS (1995) Direct measurement of trans-Golgi pH in living cells and regulation by second messengers. J Biol Chem 270(10):4967–4970

    Article  PubMed  CAS  Google Scholar 

  307. Llopis J, McCaffery JM, Miyawaki A, Farquhar MG, Tsien RY (1998) Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins. Proc Natl Acad Sci USA 95(12):6803–6808

    Article  PubMed  CAS  Google Scholar 

  308. Lopez JJ, Redondo PC, Salido GM, Pariente JA, Rosado JA (2006) Two distinct Ca2+ compartments show differential sensitivity to thrombin, ADP and vasopressin in human platelets. Cell Signal 18(3):373–381

    Article  PubMed  CAS  Google Scholar 

  309. Mahapatra NR, Mahata M, Hazra PP, McDonough PM, O’Connor DT, Mahata SK (2004) A dynamic pool of calcium in catecholamine storage vesicles. Exploration in living cells by a novel vesicle-targeted chromogranin A-aequorin chimeric photoprotein. J Biol Chem 279(49):51107–51121

    Article  PubMed  CAS  Google Scholar 

  310. Duman JG, Chen L, Palmer AE, Hille B (2006) Contributions of intracellular compartments to calcium dynamics: implicating an acidic store. Traffic 7(7):859–872

    Article  PubMed  CAS  Google Scholar 

  311. Santodomingo J, Vay L, Camacho M, Hernandez-Sanmiguel E, Fonteriz RI, Lobaton CD, Montero M, Moreno A, Alvarez J (2008) Calcium dynamics in bovine adrenal medulla chromaffin cell secretory granules. Eur J Neurosci 28(7):1265–1274

    Article  PubMed  Google Scholar 

  312. Klemper MS (1985) An adenosine triphosphate-dependent calcium uptake pump in human neutrophil lysosomes. J Clin Invest 76(1):303–310

    Article  PubMed  CAS  Google Scholar 

  313. Ezaki J, Himeno M, Kato K (1992) Purification and characterization of (Ca2+-Mg2+)-ATPase in rat liver lysosomal membranes. J Biochem 112(1):33–39

    PubMed  CAS  Google Scholar 

  314. Salceda R, Sanchez-Chavez G (2000) Calcium uptake, release and ryanodine binding in melanosomes from retinal pigment epithelium. Cell Calcium 27(4):223–229

    Article  PubMed  CAS  Google Scholar 

  315. Fasolato C, Zottini M, Clementi E, Zacchetti D, Meldolesi J, Pozzan T (1991) Intracellular Ca2+ pools in PC12 cells. Three intracellular pools are distinguished by their turn-over and mechanisms of Ca2+ accumulation, storage and release. J Biol Chem 267:20159–20167

    Google Scholar 

  316. Patel S, Docampo R (2010) Acidic calcium stores open for business: expanding the potential for intracellular Ca2+ signaling. Trends Cell Biol 20(5):277–286

    Article  PubMed  CAS  Google Scholar 

  317. Krieger-Brauer HI, Gratzl M (1983) Effects of monovalent and divalent cations on Ca2+ fluxes across chromaffin secretory membrane vesicles. J Neurochem 41(5):1269–1276

    Article  PubMed  CAS  Google Scholar 

  318. Gerasimenko JV, Tepikin AV, Petersen OH, Gerasimenko OV (1998) Calcium uptake via endocytosis with rapid release from acidifying endosomes. Curr Biol 8(24):1335–1338

    Article  PubMed  CAS  Google Scholar 

  319. Pryor PR, Mullock BM, Bright NA, Gray SR, Luzio JP (2000) The role of intraorganellar Ca2+ in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J Cell Biol 149(5):1053–1062

    Article  PubMed  CAS  Google Scholar 

  320. Sherwood MW, Prior IA, Voronina SG, Barrow SL, Woodsmith JD, Gerasimenko OV, Petersen OH, Tepikin AV (2007) Activation of trypsinogen in large endocytic vacuoles of pancreatic acinar cells. Proc Natl Acad Sci USA 104(13):5674–5679

    Article  PubMed  CAS  Google Scholar 

  321. Yoo SH (2010) Secretory granules in inositol 1, 4, 5-trisphosphate-dependent Ca2 + signaling in the cytoplasm of neuroendocrine cells. FASEB J 24(3):653–664

    Article  PubMed  CAS  Google Scholar 

  322. Bulenda D, Gratzl M (1985) Matrix free Ca2+ in isolated chromaffin vesicles. Biochemistry 24(26):7760–7765

    Article  PubMed  CAS  Google Scholar 

  323. Nguyen T, Chin WC, Verdugo P (1998) Role of Ca2+/K+ ion exchange in intracellular storage and release of Ca2+. Nature 395(6705):908–912

    Article  PubMed  CAS  Google Scholar 

  324. Yoo SH, Chu SY, Kim KD, Huh YH (2007) Presence of secretogranin II and high-capacity, low-affinity Ca2+ storage role in nucleoplasmic Ca2+ store vesicles. Biochemistry 46(50):14663–14671

    Article  PubMed  CAS  Google Scholar 

  325. Mitchell KJ, Lai FA, Rutter GA (2003) Ryanodine receptor type I and nicotinic acid adenine dinucleotide phosphate receptors mediate Ca2+ release from insulin-containing vesicles in living pancreatic beta-cells (MIN6). J Biol Chem 278(13):11057–11064

    Article  PubMed  CAS  Google Scholar 

  326. Gerasimenko OV, Gerasimenko JV, Belan PV, Petersen OH (1996) Inositol trisphosphate and cyclic ADP-ribose-mediated release of Ca2+ from single isolated pancreatic zymogen granules. Cell 84:473–480

    Article  PubMed  CAS  Google Scholar 

  327. Gerasimenko JV, Sherwood M, Tepikin AV, Petersen OH, Gerasimenko OV (2006) NAADP, cADPR and IP3 all release Ca2+ from the endoplasmic reticulum and an acidic store in the secretory granule area. J Cell Sci 119(Pt 2):226–238

    Article  PubMed  CAS  Google Scholar 

  328. Thorn P, Lawrie AM, Smith PM, Gallacher DV, Petersen OH (1993) Local and global cytosolic Ca2+ oscillations in exocrine cells evoked by agonists and inositol trisphosphate. Cell 74(4):661–668

    Article  PubMed  CAS  Google Scholar 

  329. Dell’Angelica EC, Mullins C, Caplan S, Bonifacino JS (2000) Lysosome-related organelles. FASEB J 14(10):1265–1278

    Article  PubMed  Google Scholar 

  330. Lloyd-Evans E, Morgan AJ, He X, Smith DA, Elliot-Smith E, Sillence DJ, Churchill GC, Schuchman EH, Galione A, Platt FM (2008) Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat Med 14(11):1247–1255

    Article  PubMed  CAS  Google Scholar 

  331. Holmsen H, Weiss HJ (1979) Secretable storage pools in platelets. Annu Rev Med 30:119–134

    Article  PubMed  CAS  Google Scholar 

  332. Docampo R, de Souza W, Miranda K, Rohloff P, Moreno SN (2005) Acidocalcisomes—conserved from bacteria to man. Nat Rev Microbiol 3(3):251–261

    Article  PubMed  CAS  Google Scholar 

  333. Lee HC, Aarhus R (1995) A derivative of NADP mobilizes calcium stores insensitive to inositol trisphosphate and cyclic ADP-ribose. J Biol Chem 270(5):2152–2157

    Article  PubMed  CAS  Google Scholar 

  334. Lee HC (1998) Calcium signaling by cyclic ADP-ribose and NAADP. A decade of exploration. Cell Biochem Biophys 28(1):1–17

    Article  PubMed  Google Scholar 

  335. Churchill GC, Okada Y, Thomas JM, Genazzani AA, Patel S, Galione A (2002) NAADP mobilizes Ca(2+) from reserve granules, lysosome-related organelles, in sea urchin eggs. Cell 111(5):703–708

    Article  PubMed  CAS  Google Scholar 

  336. Menteyne A, Burdakov A, Charpentier G, Petersen OH, Cancela JM (2006) Generation of specific Ca(2+) signals from Ca(2+) stores and endocytosis by differential coupling to messengers. Curr Biol 16(19):1931–1937

    Article  PubMed  CAS  Google Scholar 

  337. Yamasaki M, Masgrau R, Morgan AJ, Churchill GC, Patel S, Ashcroft SJ, Galione A (2004) Organelle selection determines agonist-specific Ca2+ signals in pancreatic acinar and beta cells. J Biol Chem 279(8):7234–7240

    Article  PubMed  CAS  Google Scholar 

  338. Palade P (2007) The hunt for an alternate way to generate NAADP. Focus on “NAADP as a second messenger: neither CD38 nor base-exchange reaction are necessary for in vivo generation of NAADP in myometrial cells”. Am J Physiol Cell Physiol 292(1):C4–C7

    Article  PubMed  CAS  Google Scholar 

  339. Soares S, Thompson M, White T, Isbell A, Yamasaki M, Prakash Y, Lund FE, Galione A, Chini EN (2007) NAADP as a second messenger: neither CD38 nor base-exchange reaction are necessary for in vivo generation of NAADP in myometrial cells. Am J Physiol Cell Physiol 292(1):C227–C239

    Article  PubMed  CAS  Google Scholar 

  340. De Flora A, Zocchi E, Guida L, Franco L, Bruzzone S (2004) Autocrine and paracrine calcium signaling by the CD38/NAD+/cyclic ADP-ribose system. Ann NY Acad Sci 1028:176–191

    PubMed  Google Scholar 

  341. Guse AH (2009) Second messenger signaling: multiple receptors for NAADP. Current Biol CB 19(13):R521–R523

    Article  CAS  Google Scholar 

  342. Zhang F, Li PL (2007) Reconstitution and characterization of a nicotinic acid adenine dinucleotide phosphate (NAADP)-sensitive Ca2+ release channel from liver lysosomes of rats. J Biol Chem 282(35):25259–25269

    Article  PubMed  CAS  Google Scholar 

  343. Gerasimenko JV, Maruyama Y, Yano K, Dolman NJ, Tepikin AV, Petersen OH, Gerasimenko OV (2003) NAADP mobilizes Ca2+ from a thapsigargin-sensitive store in the nuclear envelope by activating ryanodine receptors. J Cell Biol 163(2):271–282

    Article  PubMed  CAS  Google Scholar 

  344. Dammermann W, Guse AH (2005) Functional ryanodine receptor expression is required for NAADP-mediated local Ca2+ signaling in T-lymphocytes. J Biol Chem 280(22):21394–21399

    Article  PubMed  CAS  Google Scholar 

  345. Zhu MX, Ma J, Parrington J, Galione A, Evans AM (2010) TPCs: Endolysosomal channels for Ca2+ mobilization from acidic organelles triggered by NAADP. FEBS Lett 584(10):1966–1974

    Article  PubMed  CAS  Google Scholar 

  346. Brailoiu E, Churamani D, Cai X, Schrlau MG, Brailoiu GC, Gao X, Hooper R, Boulware MJ, Dun NJ, Marchant JS, Patel S (2009) Essential requirement for two-pore channel 1 in NAADP-mediated calcium signaling. J Cell Biol 186(2):201–209

    Article  PubMed  CAS  Google Scholar 

  347. Calcraft PJ, Ruas M, Pan Z, Cheng X, Arredouani A, Hao X, Tang J, Rietdorf K, Teboul L, Chuang KT, Lin P, Xiao R, Wang C, Zhu Y, Lin Y, Wyatt CN, Parrington J, Ma J, Evans AM, Galione A, Zhu MX (2009) NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459(7246):596–600

    Article  PubMed  CAS  Google Scholar 

  348. Zong X, Schieder M, Cuny H, Fenske S, Gruner C, Rotzer K, Griesbeck O, Harz H, Biel M, Wahl-Schott C (2009) The two-pore channel TPCN2 mediates NAADP-dependent Ca(2+)-release from lysosomal stores. Pflugers Archiv Eur J Physiol 458(5):891–899

    Article  CAS  Google Scholar 

  349. Platta HW, Erdmann R (2007) Peroxisomal dynamics. Trends Cell Biol 17(10):474–484

    Article  PubMed  CAS  Google Scholar 

  350. Wanders RJ (2004) Peroxisomes, lipid metabolism, and peroxisomal disorders. Mol Genet Metab 83(1–2):16–27

    Article  PubMed  CAS  Google Scholar 

  351. Wanders RJ, Waterham HR (2006) Biochemistry of mammalian peroxisomes revisited. Annu Rev Biochem 75:295–332

    Article  PubMed  CAS  Google Scholar 

  352. Hoepfner D, Schildknegt D, Braakman I, Philippsen P, Tabak HF (2005) Contribution of the endoplasmic reticulum to peroxisome formation. Cell 122(1):85–95

    Article  PubMed  CAS  Google Scholar 

  353. Motley AM, Hettema EH (2007) Yeast peroxisomes multiply by growth and division. J Cell Biol 178(3):399–410

    Article  PubMed  CAS  Google Scholar 

  354. Nagotu S, Veenhuis M, van der Klei IJ (2010) Divide et impera: the dictum of peroxisomes. Traffic (Copenhagen Denmark) 11(2):175–184

    Article  CAS  Google Scholar 

  355. Neuspiel M, Schauss AC, Braschi E, Zunino R, Rippstein P, Rachubinski RA, Andrade-Navarro MA, McBride HM (2008) Cargo-selected transport from the mitochondria to peroxisomes is mediated by vesicular carriers. Curr Biol CB 18(2):102–108

    Article  CAS  Google Scholar 

  356. Koch A, Yoon Y, Bonekamp NA, McNiven MA, Schrader M (2005) A role for Fis1 in both mitochondrial and peroxisomal fission in mammalian cells. Mol Biol Cell 16(11):5077–5086

    Article  PubMed  CAS  Google Scholar 

  357. Schrader M, Yoon Y (2007) Mitochondria and peroxisomes: are the ‘big brother’ and the ‘little sister’ closer than assumed? BioEssays : news and reviews in molecular. Cell Dev Biol 29(11):1105–1114

    CAS  Google Scholar 

  358. Titorenko VI, Rachubinski RA (2004) The peroxisome: orchestrating important developmental decisions from inside the cell. J Cell Biol 164(5):641–645

    Article  PubMed  CAS  Google Scholar 

  359. Tan NS, Shaw NS, Vinckenbosch N, Liu P, Yasmin R, Desvergne B, Wahli W, Noy N (2002) Selective cooperation between fatty acid binding proteins and peroxisome proliferator-activated receptors in regulating transcription. Mol Cell Biol 22(14):5114–5127

    Article  PubMed  CAS  Google Scholar 

  360. Fidaleo M (2010) Peroxisomes and peroxisomal disorders: the main facts. Exp Toxicol Pathol 62(6):615–625

    Article  PubMed  CAS  Google Scholar 

  361. Raychaudhury B, Gupta S, Banerjee S, Datta SC (2006) Peroxisome is a reservoir of intracellular calcium. Biochim Biophys Acta 1760(7):989–992

    Article  PubMed  CAS  Google Scholar 

  362. Drago I, Giacomello M, Pizzo P, Pozzan T (2008) Calcium dynamics in the peroxisomal lumen of living cells. J Biol Chem 283(21):14384–14390

    Article  PubMed  CAS  Google Scholar 

  363. Lasorsa FM, Pinton P, Palmieri L, Scarcia P, Rottensteiner H, Rizzuto R, Palmieri F (2008) Peroxisomes as novel players in cell calcium homeostasis. J Biol Chem 283(22):15300–15308

    Article  PubMed  CAS  Google Scholar 

  364. Yang T, Poovaiah BW (2002) Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin. Proc Natl Acad Sci USA 99(6):4097–4102

    Article  PubMed  CAS  Google Scholar 

  365. Costa A, Drago I, Behera S, Zottini M, Pizzo P, Schroeder JI, Pozzan T, Lo Schiavo F (2010) H2O2 in plant peroxisomes: an in vivo analysis uncovers a Ca(2+)-dependent scavenging system. Plant J 62(5):760–772

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We acknowledge the Italian Ministry of University and Research (MIUR) and the University of Padua (Progetto di Ateneo 2011) for supporting our work. We thank P. Capitanio and I. Drago for providing us with some Cameleon images. We are grateful to P. Magalhães for English editing and to T. Pozzan for critical reading of the manuscript, valuable discussions and scientific support.

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  1. Department of Biomedical Sciences, University of Padova, Viale G. Colombo 3, 35121, Padova, Italy

    Enrico Zampese & Paola Pizzo

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  1. Enrico Zampese
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  2. Paola Pizzo
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Correspondence to Paola Pizzo.

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Zampese, E., Pizzo, P. Intracellular organelles in the saga of Ca2+ homeostasis: different molecules for different purposes?. Cell. Mol. Life Sci. 69, 1077–1104 (2012). https://doi.org/10.1007/s00018-011-0845-9

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