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Calcium Around the Golgi Apparatus: Implications for Intracellular Membrane Trafficking

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Calcium Signaling

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 740))

Abstract

As with other complex cellular functions, intracellular membrane transport involves the coordinated engagement of a series of organelles and machineries; in the last couple of decades more importance has been given to the role of calcium (Ca2+) in the regulation of membrane trafficking, which is directly involved in coordinating the endoplasmic reticulum-to-Golgi-to-plasma membrane delivery of cargo. Consequently, the Golgi apparatus (GA) is now considered not just the place proteins mature in as they move to their final destination(s), but it is increasingly viewed as an intracellular Ca2+ store. In the last few years the mechanisms regulating the homeostasis of Ca2+ in the GA and its role in membrane trafficking have begun to be elucidated. Here, these recent discoveries that shed light on the role Ca2+ plays as of trigger of different steps during membrane trafficking has been reviewed. This includes recruitment of proteins and SNARE cofactors to the Golgi membranes, which are both fundamental for the membrane remodeling and the regulation of fusion/fission events occurring during the passage of cargo across the GA. I conclude by focusing attention on Ca2+ homeostasis dysfunctions in the GA and their related pathological implications.

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Abbreviations

Ca2+ :

Calcium ions

[Ca2+]cyt :

Free calcium ion concentration in the cell cytosol

[Ca2+]ext :

Free extracellular calcium ion concentration

[Ca2+]GA :

Free calcium ion concentration in the Golgi apparatus

CaR:

Ca2+ receptor

CGN:

Cis-Golgi network

COPI:

Coat protein I

ER:

Endoplasmic reticulum

GA:

Golgi apparatus

HDD:

Hailey-Hailey disease

IGF1R:

Insulin-like growth factor receptor

IP3R:

Inositol 1,4,5-trisphospahate receptor

NCS-1:

Neuronal calcium sensor 1

PLA2:

Phospholipase A2

PM:

Plasma membrane

SERCA:

Sarco/endoplasmic reticulum Ca2+-transport ATPase pump

SNARE:

Soluble N-ethylmaleimide-sensitive fusion factor attachment protein receptor

SPCA1:

Secretory pathway Ca2+-ATPase isoform 1

TGN:

Trans-Golgi network

VSMCs:

Vascular smooth muscle cells

VSVG:

Temperature sensitive variant of the G protein of vesicular stomatitis virus

References

  1. Golgi C (1898) Intorno alla struttura delle cellule nervose. Boll Soc Med Chir Pavia 13:3–16

    Google Scholar 

  2. Pelham HR, Rothman JE (2000) The debate about transport in the Golgi – two sides of the same coin? Cell 102:713–719

    Article  PubMed  CAS  Google Scholar 

  3. Emr S, Glick BS, Linstedt AD, Lippincott-Schwartz J, Luini A, Malhotra V, Marsh BJ, Nakano A, Pfeffer SR, Rabouille C, Rothman JE, Warren G, Wieland FT (2009) Journeys through the Golgi – taking stock in a new era. J Cell Biol 187:449–453

    Article  PubMed  CAS  Google Scholar 

  4. Glick BS, Nakano A (2009) Membrane traffic within the Golgi apparatus. Annu Rev Cell Dev Biol 25:113–132

    Article  PubMed  CAS  Google Scholar 

  5. Bonfanti L, Mironov AA Jr, Martinez-Menarguez JA, Martella O, Fusella A, Baldassarre M, Buccione R, Geuze HJ, Mironov AA, Luini A (1998) Procollagen traverses the Golgi stack without leaving the lumen of cisternae: evidence for cisternal maturation. Cell 95:993–1003

    Article  PubMed  CAS  Google Scholar 

  6. Marsh BJ, Volkmann N, McIntosh JR, Howell KE (2004) Direct continuities between cisternae at different levels of the Golgi complex in glucose-stimulated mouse islet beta cells. Proc Natl Acad Sci USA 101:5565–5570

    Article  PubMed  CAS  Google Scholar 

  7. Losev E, Reinke CA, Jellen J, Strongin DE, Bevis BJ, Glick BS (2006) Golgi maturation visualized in living yeast. Nature 441:1002–1006

    Article  PubMed  CAS  Google Scholar 

  8. Matsuura-Tokita K, Takeuchi M, Ichihara A, Mikuriya K, Nakano A (2006) Live imaging of yeast Golgi cisternal maturation. Nature 441:1007–1010

    Article  PubMed  CAS  Google Scholar 

  9. Rivera-Molina FE, Novick PJ (2009) A Rab GAP cascade defines the boundary between two Rab GTPases on the secretory pathway. Proc Natl Acad Sci USA 106:14408–14413

    Article  PubMed  CAS  Google Scholar 

  10. Pfeffer SR (2010) How the Golgi works: a cisternal progenitor model. Proc Natl Acad Sci USA 107:19614–19618

    Article  PubMed  CAS  Google Scholar 

  11. Hong W (2005) SNAREs and traffic. Biochim Biophys Acta 1744:493–517

    Article  PubMed  CAS  Google Scholar 

  12. Jena BP (2009) Membrane fusion: role of SNAREs and calcium. Protein Pept Lett 16:712–717

    Article  PubMed  CAS  Google Scholar 

  13. Jeremic A, Kelly M, Cho JA, Cho SJ, Horber JK, Jena BP (2004) Calcium drives fusion of SNARE-apposed bilayers. Cell Biol Int 28:19–31

    Article  PubMed  CAS  Google Scholar 

  14. Micaroni M, Perinetti G, Di Giandomenico D, Bianchi K, Spaar A, Mironov AA (2010) Synchronous intra-Golgi transport induces the release of Ca2+ from the Golgi apparatus. Exp Cell Res 316:2071–2086

    Article  PubMed  CAS  Google Scholar 

  15. Montero M, Brini M, Marsault R, Alvarez J, Sitia R, Pozzan T, Rizzuto R (1995) Monitoring dynamic changes in free Ca2+ concentration in the endoplasmic reticulum of intact cells. EMBO J 14:5467–5475

    PubMed  CAS  Google Scholar 

  16. 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 17:5298–5308

    Article  PubMed  CAS  Google Scholar 

  17. Berridge MJ (2002) The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32:235–249

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  19. Roseman S (2001) Reflections on glycobiology. J Biol Chem 276:41527–41542

    Article  PubMed  CAS  Google Scholar 

  20. Hu Z, Bonifas JM, Beech J, Bench G, Shigihara T, Ogawa H, Ikeda S, Mauro T, Epstein EH Jr (2000) Mutations in ATP2C1, encoding a calcium pump, cause Hailey-Hailey disease. Nat Genet 24:61–65

    Article  PubMed  CAS  Google Scholar 

  21. 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 34:157–162

    Article  PubMed  CAS  Google Scholar 

  22. Ward DT (2004) Calcium receptor-mediated intracellular signalling. Cell Calcium 35:217–228

    Article  PubMed  CAS  Google Scholar 

  23. Tu CL, Chang W, Bikle DD (2007) The role of the calcium sensing receptor in regulating intracellular calcium handling in human epidermal keratinocytes. J Invest Dermatol 127: 1074–1083

    Article  PubMed  CAS  Google Scholar 

  24. Chen JL, Ahluwalia JP, Stamnes M (2002) Selective effects of calcium chelators on anterograde retrograde protein transport in the cell. J Biol Chem 277:35682–35687

    Article  PubMed  CAS  Google Scholar 

  25. Mayorga LS, Colombo MI, Lennartz M, Brown EJ, Rahman KH, Weiss R, Lennon PJ, Stahl PD (1993) Inhibition of endosome fusion by phospholipase A2 (PLA2) inhibitors points to a role for PLA2 in endocytosis. Proc Natl Acad Sci USA 90:10255–10259

    Article  PubMed  CAS  Google Scholar 

  26. Peters C, Mayer A (1998) Ca2+/calmodulin signals the completion of docking and triggers a late step of vacuole fusion. Nature 396:575–580

    Article  PubMed  CAS  Google Scholar 

  27. Pryor PR, Mullock BM, Bright NA, Gray SR, Luzio JP (2000) The role of intraorganellar Ca(2+) in late endosome–lysosome heterotypic fusion in the reformation of lysosomes from hybrid organelles. J Cell Biol 149:1053–1062

    Article  PubMed  CAS  Google Scholar 

  28. Beckers CJ, Balch WE (1989) Calcium and GTP: essential components in vesicular trafficking between the endoplasmic reticulum and Golgi apparatus. J Cell Biol 108:1245–1256

    Article  PubMed  CAS  Google Scholar 

  29. Porat A, Elazar Z (2000) Regulation of intra-Golgi membrane transport by calcium. J Biol Chem 275:29233–29237

    Article  PubMed  CAS  Google Scholar 

  30. Scherer PE, Lederkremer GZ, Williams S, Fogliano M, Baldini G, Lodish HF (1996) Cab45, a novel (Ca2+)-binding protein localized to the Golgi lumen. J Cell Biol 133:257–268

    Article  PubMed  CAS  Google Scholar 

  31. 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 145:279–289

    Article  PubMed  CAS  Google Scholar 

  32. Kawano J, Kotani T, Ogata Y, Ohtaki S, Takechi S, Nakayama T, Sawaguchi A, Nagaike R, Oinuma T, Suganuma T (2000) CALNUC (nucleobindin) is localized in the Golgi apparatus in insect cells. Eur J Cell Biol 79:208–217

    Article  PubMed  CAS  Google Scholar 

  33. Morel-Huaux VM, Pypaert M, Wouters S, Tartakoff AM, Jurgan U, Gevaert K, Courtoy PJ (2002) The calcium-binding protein p54/NEFA is a novel luminal resident of medial Golgi cisternae that traffics independently of mannosidase II. Eur J Cell Biol 81:87–100

    Article  PubMed  CAS  Google Scholar 

  34. Haynes LP, Tepikin AV, Burgoyne RD (2004) Calcium-binding protein 1 is an inhibitor of agonist-evoked, inositol 1,4,5-trisphosphate-mediated calcium signaling. J Biol Chem 279: 547–555

    Article  PubMed  CAS  Google Scholar 

  35. Haynes LP, Fitzgerald DJ, Wareing B, O’Callaghan DW, Morgan A, Burgoyne RD (2006) Analysis of the interacting partners of the neuronal calcium-binding proteins L-CaBP1, hippocalcin, NCS-1 and neurocalcin delta. Proteomics 6:1822–1832

    Article  PubMed  CAS  Google Scholar 

  36. Haynes LP, Thomas GM, Burgoyne RD (2005) Interaction of neuronal calcium sensor-1 and ADP-ribosylation factor 1 allows bidirectional control of phosphatidylinositol 4-kinase beta trans-Golgi network-plasma membrane traffic. J Biol Chem 280:6047–6054

    Article  PubMed  CAS  Google Scholar 

  37. Hata S, Koyama S, Kawahara H, Doi N, Maeda T, Toyama-Sorimachi N, Abe K, Suzuki K, Sorimachi H (2006) Stomach-specific calpain, nCL-2, localizes in mucus cells and proteolyzes the beta-subunit of coatomer complex, beta-COP. J Biol Chem 281:11214–11224

    Article  PubMed  CAS  Google Scholar 

  38. O’Callaghan DW, Ivings L, Weiss JL, Ashby MC, Tepikin AV, Burgoyne RD (2002) Differential use of myristoyl groups on neuronal calcium sensor proteins as a determinant of spatio-temporal aspects of Ca2+ signal transduction. J Biol Chem 277:14227–14237

    Article  PubMed  CAS  Google Scholar 

  39. Bivona TG, Perez-De Castro I, Ahearn IM, Grana TM, Chiu VK, Lockyer PJ, Cullen PJ, Pellicer A, Cox AD, Philips MR (2003) Phospholipase Cgamma activates Ras on the Golgi apparatus by means of RasGRP1. Nature 424:694–698

    Article  PubMed  CAS  Google Scholar 

  40. Evans JH, Leslie CC (2004) The cytosolic phospholipase A2 catalytic domain modulates association and residence time at Golgi membranes. J Biol Chem 279:6005–6016

    Article  PubMed  CAS  Google Scholar 

  41. Lopez-Alcala C, Alvarez-Moya B, Villalonga P, Calvo M, Bachs O, Agell N (2008) Identification of essential interacting elements in K-Ras/Calmodulin binding and its role in K-Ras localization. J Biol Chem 283:10621–10631

    Article  PubMed  CAS  Google Scholar 

  42. Noguchi H, Kobayashi M, Miwa N, Takamatsu K (2007) Lack of hippocalcin causes impairment in Ras/extracellular signal-regulated kinase cascade via a Raf-mediated activation process. J Neurosci Res 85:837–884

    Article  PubMed  CAS  Google Scholar 

  43. Rodriguez-Viciana P, Sabatier C, McCormick F (2004) Signaling specificity by Ras family GTPases is determined by the full spectrum of effectors they regulate. Mol Cell Biol 24:4943–4954

    Article  PubMed  CAS  Google Scholar 

  44. Rodriguez-Viciana P, McCormick F (2005) RalGDS comes of age. Cancer Cell 7:205–206

    Article  PubMed  CAS  Google Scholar 

  45. Quatela SE, Philips MR (2006) Ras signaling on the Golgi. Curr Opin Cell Biol 18:162–167

    Article  PubMed  CAS  Google Scholar 

  46. Chiu VK, Bivona T, Hach A, Sajous JB, Silletti J, Wiener H, Johnson RL 2nd, Cox AD, Philips MR (2002) Ras signalling on the endoplasmic reticulum and the Golgi. Nat Cell Biol 4:343–350

    PubMed  CAS  Google Scholar 

  47. Michaelson D, Ahearn I, Bergo M, Young S, Philips M (2002) Membrane trafficking of heterotrimeric G proteins via the endoplasmic reticulum and Golgi. Mol Biol Cell 13:3294–3302

    Article  PubMed  CAS  Google Scholar 

  48. Bivona TG, Philips MR (2003) Ras pathway signaling on endomembranes. Curr Opin Cell Biol 15:136–142

    Article  PubMed  CAS  Google Scholar 

  49. Bonifacino JS, Glick BS (2004) The mechanisms of vesicle budding and fusion. Cell 116:153–166

    Article  PubMed  CAS  Google Scholar 

  50. Sollner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318–324

    Article  PubMed  CAS  Google Scholar 

  51. Fukuda R, McNew JA, Weber T, Parlati F, Engel T, Nickel W, Rothman JE, Sollner TH (2000) Functional architecture of an intracellular membrane t-SNARE. Nature 407:198–202

    Article  PubMed  CAS  Google Scholar 

  52. Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M, Parlati F, Sollner TH, Rothman JE (1998) SNAREpins: minimal machinery for membrane fusion. Cell 92:759–772

    Article  PubMed  CAS  Google Scholar 

  53. Antonin W, Fasshauer D, Becker S, Jahn R, Schneider TR (2002) Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs. Nat Struct Biol 9:107–111

    Article  PubMed  CAS  Google Scholar 

  54. Sutton RB, Fasshauer D, Jahn R, Brunger AT (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395:347–353

    Article  PubMed  CAS  Google Scholar 

  55. Fasshauer D (2003) Structural insights into the SNARE mechanism. Biochim Biophys Acta 1641:87–97

    Article  PubMed  CAS  Google Scholar 

  56. Brose N, Hofmann K, Hata Y, Sudhof TC (1995) Mammalian homologues of Caenorhabditis elegans Munc-13 gene define novel family of C2-domain proteins. J Biol Chem 270: 25273–25280

    Article  PubMed  CAS  Google Scholar 

  57. Sudhof TC (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27:509–547

    Article  PubMed  CAS  Google Scholar 

  58. Sudhof TC (2002) Synaptotagmins: why so many? J Biol Chem 277:7629–7632

    Article  PubMed  CAS  Google Scholar 

  59. Geppert M, Goda Y, Hammer RE, Li C, Rosahl TW, Stevens CF, Sudhof TC (1994) Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell 79:717–727

    Article  PubMed  CAS  Google Scholar 

  60. Fernandez-Chacon R, Konigstorfer A, Gerber SH, Garcia J, Matos MF, Stevens CF, Brose N, Rizo J, Rosenmund C, Sudhof TC (2001) Synaptotagmin I functions as a calcium regulator of release probability. Nature 410:41–49

    Article  PubMed  CAS  Google Scholar 

  61. Bai J, Chapman ER (2004) The C2 domains of synaptotagmin – partners in exocytosis. Trends Biochem Sci 29:143–151

    Article  PubMed  CAS  Google Scholar 

  62. Bai J, Tucker WC, Chapman ER (2004) PIP2 increases the speed of response of synaptotagmin and steers its membrane-penetration activity toward the plasma membrane. Nat Struct Mol Biol 11:36–44

    Article  PubMed  CAS  Google Scholar 

  63. Zhang X, Kim-Miller MJ, Fukuda M, Kowalchyk JA, Martin TF (2002) Ca2  +  -dependent synaptotagmin binding to SNAP-25 is essential for Ca2  +  -triggered exocytosis. Neuron 34:599–611

    Article  PubMed  CAS  Google Scholar 

  64. Tucker WC, Weber T, Chapman ER (2004) Reconstitution of Ca2  +  -regulated membrane fusion by synaptotagmin and SNAREs. Science 304:435–438

    Article  PubMed  CAS  Google Scholar 

  65. Brown WJ, Chambers K, Doody A (2003) Phospholipase A2 (PLA2) enzymes in membrane trafficking: mediators of membrane shape and function. Traffic 4:214–221

    Article  PubMed  CAS  Google Scholar 

  66. Six DA, Dennis EA (2000) The expanding superfamily of phospholipase A(2) enzymes: classification and characterization. Biochim Biophys Acta 1488:1–19

    PubMed  CAS  Google Scholar 

  67. San Pietro E, Capestrano M, Polishchuk EV, Di Pentima A, Trucco A, Zizza P, Mariggio’ S, Pulvirenti T, Sallese M, Tete’ S, Mironov AA, Leslie CC, Corda D, Luini A, Polishchuk RS (2009) Group IV phospholipase A(2)alpha controls the formation of inter-cisternal continuities involved in intra-Golgi transport. PLoS Biol 7:e1000194

    Article  PubMed  CAS  Google Scholar 

  68. Bezprozvanny I, Scheller RH, Tsien RW (1995) Functional impact of syntaxin on gating of N-type and Q-type calcium channels. Nature 378:623–626

    Article  PubMed  CAS  Google Scholar 

  69. Schekman R (1998) Membrane fusion. Ready…aim…fire! Nature 396:514–515

    Article  PubMed  CAS  Google Scholar 

  70. Ghosh M, Tucker DE, Burchett SA, Leslie CC (2006) Properties of the Group IV phospholipase A2 family. Prog Lipid Res 45:487–510

    Article  PubMed  CAS  Google Scholar 

  71. Lippincott-Schwartz J, Snapp E, Kenworthy A (2001) Studying protein dynamics in living cells. Nat Rev Mol Cell Biol 2:444–456

    Article  PubMed  CAS  Google Scholar 

  72. de Figueiredo P, Drecktrah D, Polizotto RS, Cole NB, Lippincott-Schwartz J, Brown WJ (2000) Phospholipase A2 antagonists inhibit constitutive retrograde membrane traffic to the endoplasmic reticulum. Traffic 1:504–511

    Article  PubMed  Google Scholar 

  73. Polizotto RS, de Figueiredo P, Brown WJ (1999) Stimulation of Golgi membrane tubulation and retrograde trafficking to the ER by phospholipase A(2) activating protein (PLAP) peptide. J Cell Biochem 74:670–683

    Article  PubMed  CAS  Google Scholar 

  74. de Figueiredo P, Drecktrah D, Katzenellenbogen JA, Strang M, Brown WJ (1998) Evidence that phospholipase A2 activity is required for Golgi complex and trans Golgi network membrane tubulation. Proc Natl Acad Sci USA 95:8642–8647

    Article  PubMed  Google Scholar 

  75. de Figueiredo P, Doody A, Polizotto RS, Drecktrah D, Wood S, Banta M, Strang MS, Brown WJ (2001) Inhibition of transferrin recycling and endosome tubulation by phospholipase A2 antagonists. J Biol Chem 276:47361–47370

    Article  PubMed  Google Scholar 

  76. de Figueiredo P, Polizotto RS, Drecktrah D, Brown WJ (1999) Membrane tubule-mediated reassembly and maintenance of the Golgi complex is disrupted by phospholipase A2 antagonists. Mol Biol Cell 10:1763–1782

    PubMed  Google Scholar 

  77. Micaroni M (2010) The role of calcium in intracellular trafficking. Curr Mol Med 10:763–773

    Article  PubMed  CAS  Google Scholar 

  78. Gunteski-Hamblin AG, Clarke DM, Shull GE (1992) Molecular cloning and tissue distribution of alternatively spliced mRNAs encoding possible mammalian homologs of the yeast secretory pathway calcium pump. Biochemistry 31:7600–7608

    Article  PubMed  CAS  Google Scholar 

  79. Park CS, Kim JY, Crispino C, Chang CC, Ryu DD (1998) Molecular cloning of YIPMR1, a S. cerevisiae PMR1 homologue encoding a novel P-type secretory pathway Ca2  +  -ATPase, in the yeast Yarrowia lipolytica. Gene 206:107–116

    Article  PubMed  CAS  Google Scholar 

  80. 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 121:688–694

    Article  PubMed  CAS  Google Scholar 

  81. Micaroni M, Perinetti G, Berrie CP, Mironov AA (2010) The SPCA1 Ca2+ pump and intracellular membrane trafficking. Traffic 11:1315–1333

    Article  PubMed  CAS  Google Scholar 

  82. Fairclough RJ, Dode L, Vanoevelen J, Andersen JP, Missiaen L, Raeymaekers L, Wuytack F, Hovnanian A (2003) Effect of Hailey-Hailey disease mutations on the function of a new variant of human secretory pathway Ca2+/Mn2  +  -ATPase (hSPCA1). J Biol Chem 278: 24721–24730

    Article  PubMed  CAS  Google Scholar 

  83. 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 306:430–436

    Article  PubMed  CAS  Google Scholar 

  84. Sepulveda RM, Vanoevelen J, Raeymakers L, Mata AM, Wuytack F (2009) Silencing the SPCA1 (Secretory Pathway Ca2+-ATPase isoform 1) impairs Ca2+ homeostasis in the Golgi and disturbs neural polarity. J Neurosci 29:12174–12182

    Article  PubMed  CAS  Google Scholar 

  85. 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 53:393–400

    Article  PubMed  CAS  Google Scholar 

  86. Okunade GW, Miller ML, Azhar M, Andringa A, Sanford LP, Doetschman T et al (2007) Loss of the ATP2C1 secretory pathway Ca(2+)-ATPase (SPCA1) in mice causes Golgi stress, apoptosis, and mid-gestational death in homozygous embryos and squamous cell tumours in adult heterozygotes. J Biol Chem 282:26517–26527

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  88. Pizzo P, Lissandron V, Pozzan T (2010) The trans-Golgi compartment: a new distinct intracellular Ca2+ store. Commun Integr Biol 3:462–464

    Article  PubMed  CAS  Google Scholar 

  89. Mishiro E, Liu MY, Sakakibara Y, Suiko M, Liu MC (2004) Zebrafish tyrosylprotein sulfotransferase: molecular cloning, expression, and functional characterization. Biochem Cell Biol 82:295–303

    Article  PubMed  CAS  Google Scholar 

  90. Seko A, Sumiya J, Yamashita K (2005) Porcine, mouse and human galactose 3-O-sulphotransferase-2 enzymes have different substrate specificities; the porcine enzyme requires basic compounds for its catalytic activity. Biochem J 391:77–85

    Article  PubMed  CAS  Google Scholar 

  91. Anderson ED, VanSlyke JK, Thulin CD, Jean F, Thomas G (1997) Activation of the furin endoprotease is a multiple-step process: requirements for acidification and internal propeptide cleavage. EMBO J 16:1508–1518

    Article  PubMed  CAS  Google Scholar 

  92. LaFerla FM (2002) Calcium dyshomeostasis and intracellular signalling in Alzheimer’s disease. Nat Rev Neurosci 3:862–872

    Article  PubMed  CAS  Google Scholar 

  93. 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 280:9467–9473

    Article  PubMed  CAS  Google Scholar 

  94. Leitch S, Feng M, Muend S, Braiterman LT, Hubbard AL, Rao R (2011) Vesicular distribution of secretory pathway Ca2+-ATPase isoform 1 and a role in manganese detoxification in liver-derived polarized cells. Biometals 24:159–170

    Article  PubMed  CAS  Google Scholar 

  95. Harris A, Burge SM, Dykes PJ, Finlay AY (1996) Handicap in Darier’s disease and Hailey-Hailey disease. Br J Dermatol 135:959–963

    Article  PubMed  CAS  Google Scholar 

  96. Chun SI, Wang KC, Su WP (1988) Squamous cell carcinoma arising in Hailey-Hailey disease. J Cutan Pathol 15:234–237

    Article  PubMed  CAS  Google Scholar 

  97. Sudbrak R, Brown J, Dobson-Stone C, Carter S, Ramser J, White J, Healy E, Dissanayake M, Larregue M, Perrussel M, Lehrach H, Munro CS, Strachan T, Burge S, Hovnanian A, Monaco AP (2000) Hailey-Hailey disease is caused by mutation in ATP2C1 encoding a novel Ca(2+) pump. Hum Mol Genet 9:1131–1140

    Article  PubMed  CAS  Google Scholar 

  98. Micaroni M, Mironov AA (2010) Roles of Ca2+ and secretory pathway Ca2+-ATPase pump type 1 (SPCA1) in intra-Golgi transport. Commun Integr Biol 3:504–507

    Article  PubMed  Google Scholar 

  99. Tian H, Yan X, Liu H, Yu Y, Zhang F (2010) Six novel mutations identified in Chinese patients with Hailey-Hailey disease. J Dermatol Sci 58:80–82

    Article  PubMed  CAS  Google Scholar 

  100. Lipoff JB, Mudgil AV, Young S, Chu P, Cohen SR (2009) Acantholytic dermatosis of the crural folds with APT2C1mutation is a possible variant of Hailey-Hailey disease. J Cutan Med Surg 13:151–154

    PubMed  CAS  Google Scholar 

  101. Vasioukhin V, Bauer C, Yin M, Fuchs E (2000) Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 100:209–219

    Article  PubMed  CAS  Google Scholar 

  102. Missiaen L, Raeymakers 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 322:1204–1213

    Article  PubMed  CAS  Google Scholar 

  103. Wootton LL, Argent CCH, Wheatley M, Michelangeli F (2004) The expression, activity and localization of the secretory pathway Ca2+-ATPase (SPCA1) in different mammalian tissues. Biochim Biophys Acta 1664:189–197

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  105. Thyberg J (1998) Tyrphostin A9 and wortmannin perturb the Golgi complex and block proliferation of vascular smooth muscle cells. Eur J Cell Biol 76:33–42

    Article  PubMed  CAS  Google Scholar 

  106. Shahbazi S, Lenting PJ, Fribourg C, Terraube V, Denis CV, Christophe OD (2007) Characterization of the interaction between von Willebrand factor and osteoprotegerin. J Thromb Haemost 5:1956–1962

    Article  PubMed  CAS  Google Scholar 

  107. Lai P, Michelangeli F (2009) Changes in expression and activity of the secretory pathway Ca2+ APTase 1 (SPCA1) in A7r5 vascular smooth muscle cells cultured at different glucose concentrations. Biosci Rep 29:397–404

    Article  PubMed  CAS  Google Scholar 

  108. Stalker TJ, Gong Y, Scalia R (2005) The calcium-dependent protease calpain causes endothelial dysfunction in type 2 diabetes. Diabetes 54:1132–1140

    Article  PubMed  CAS  Google Scholar 

  109. Yousif MH, Akhtar S, Walther T, Benter IF (2008) Role of Ca2+/calmodulin-dependent protein kinase II in development of vascular dysfunction in diabetic rats with hypertension. Cell Biochem Funct 26:256–263

    Article  PubMed  CAS  Google Scholar 

  110. Curtis TM, Major EH, Trimble ER, Scholfield CN (2003) Diabetes-induced activation of protein kinase C inhibits store-operated Ca2+ uptake in rat retinal microvascular smooth muscle. Diabetologia 46:1252–1259

    Article  PubMed  CAS  Google Scholar 

  111. Li M, Zhang M, Huang LP, Zhou J, Zhuang H, Taylor JT, Keyser BM, Whitehurst RM Jr (2005) T-type Ca2+ channels are involved in high glucose-induced rat neonatal cardiomyocyte proliferation. Pediatr Res 57:550–556

    Article  PubMed  CAS  Google Scholar 

  112. Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4:517–529

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  114. Roderick HL, Cook SJ (2008) Ca2+ signalling checkpoints in cancer: remodelling Ca2+ for cancer cell proliferation and survival. Nat Rev Cancer 8:361–375

    Article  PubMed  CAS  Google Scholar 

  115. Feng M, Grice DM, Faddy HM, Nguyen N, Leitch S, Wang Y, Muend S, Kenny PA, Sukumar S, Roberts-Thomson SJ, Monteith GR, Rao R (2010) Store-independent activation of Orai1 by SPCA2 in mammary tumors. Cell 143:84–98

    Article  PubMed  CAS  Google Scholar 

  116. Cahalan MD, Zhang SL, Yeromin AV, Ohlsen K, Roos J (2007) Stauderman KA Molecular basis of the CRAC channel. Cell Calcium 42:133–144

    Article  PubMed  CAS  Google Scholar 

  117. Anantamongkol U, Takemura H, Suthiphongchai T, Krishnamra N, Horio Y (2007) Regulation of Ca2+ mobilization by prolactin in mammary gland cells: possible role of secretory pathway Ca2  +  -ATPase type 2. Biochem Biophys Res Commun 352:537–542

    Article  PubMed  CAS  Google Scholar 

  118. Reinhardt TA, Lippolis JD (2009) Mammary gland involution is associated with rapid down regulation of major mammary Ca2  +  -ATPases. Biochem Biophys Res Commun 378: 99–102

    Article  PubMed  CAS  Google Scholar 

  119. Faddy HM, Smart CE, Xu R, Lee GY, Kenny PA, Feng M, Rao R, Brown MA, Bissell MJ, Roberts-Thomson SJ, Monteith GR (2008) Localization of plasma membrane and secretory calcium pumps in the mammary gland. Biochem Biophys Res Commun 369:977–981

    Article  PubMed  CAS  Google Scholar 

  120. Newbury DF, Winchester L, Addis L, Paracchini S, Buckingham LL, Clark A, Cohen W, Cowie H, Dworzynski K, Everitt A, Goodyer IM, Hennessy E, Kindley AD, Miller LL, Nasir J, O’Hare A, Shaw D, Simkin Z, Simonoff E, Slonims V, Watson J, Ragoussis J, Fisher SE, Seckl JR, Helms PJ, Bolton PF, Pickles A, Conti-Ramsden G, Baird G, Bishop DV, Monaco AP (2009) CMIP and ATP2C2 modulate phonological short-term memory in language impairment. Am J Hum Genet 85:264–272

    Article  PubMed  CAS  Google Scholar 

  121. Zheng JQ, Poo MM (2007) Calcium signaling in neuronal motility. Annu Rev Cell Dev Biol 23:375–404

    Article  PubMed  CAS  Google Scholar 

  122. Normandin L, Hazell AS (2002) Manganese neurotoxicity: an update of pathophysiologic mechanisms. Metab Brain Dis 17:375–387

    Article  PubMed  CAS  Google Scholar 

  123. Pizzo P, Lissandron V, Capitanio P, Pozzan T (2011) Ca(2+) signalling in the Golgi apparatus. Cell Calcium 50:184–192

    Google Scholar 

  124. Isshiki M, Anderson RG (1999) Calcium signal transduction from caveolae. Cell Calcium 26:201–208

    Article  PubMed  CAS  Google Scholar 

  125. Brown DA, London E (2000) Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J Biol Chem 275:17221–17224

    Article  PubMed  CAS  Google Scholar 

  126. Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1:31–39

    Article  PubMed  CAS  Google Scholar 

  127. Pani B, Singh BB (2009) Lipid rafts/caveolae as microdomains of calcium signaling. Cell Calcium 45:625–633

    Article  PubMed  CAS  Google Scholar 

  128. Bagnat M, Kernen S, Shevchenko A, Shevchenko A, Simons K (2000) Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc Natl Acad Sci USA 97:3254–3259

    Article  PubMed  CAS  Google Scholar 

  129. Heino S, Lusa S, Somerharju P, Ehnholm C, Olkkonen VM, Ikonen E (2000) Dissecting the role of the Golgi complex and lipid rafts in biosynthetic transport of cholesterol to the cell surface. Proc Natl Acad Sci USA 97:8375–8380

    Article  PubMed  CAS  Google Scholar 

  130. Simons K, Ehehalt R (2002) Cholesterol, lipid rafts, and disease. J Clin Invest 110:597–603

    PubMed  CAS  Google Scholar 

  131. Hirschberg K, Miller CM, Ellenberg J, Presley JF, Siggia ED, Phair RD, Lippincott-Schwartz J (1998) Kinetic analysis of secretory protein traffic and characterization of Golgi to plasma membrane transport intermediates in living cells. J Cell Biol 143:1485–1503

    Article  PubMed  CAS  Google Scholar 

  132. Patterson GH, Hirschberg K, Polishchuk RS, Gerlich D, Phair RD, Lippincott-Schwartz J (2008) Transport through the Golgi apparatus by rapid partitioning within a two-phase membrane system. Cell 133:1055–1067

    Article  PubMed  CAS  Google Scholar 

  133. Baron S, Vangheluwe P, Sepulveda MR, Wuytack F, Raeymakers L, Vanoevelen J (2010) The secretory pathway Ca2+-ATPase 1 is associated with cholesterol-rich microdomains of human colon adenocarcinoma cells. Biochim Biophys Acta 1798:1512–1521

    Article  PubMed  CAS  Google Scholar 

  134. 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 280:11608–11614

    Article  PubMed  CAS  Google Scholar 

  135. Dolman NJ, Tepikin AV (2006) Calcium gradients and the Golgi. Cell Calcium 40:505–512

    Article  PubMed  CAS  Google Scholar 

  136. Baron S, Struyf S, Wuytack F, Van Damme J, Missiaen L, Raeymaekers L, Vanoevelen J (2009) Contribution of intracellular Ca2+ stores to Ca2+ signaling during chemokinesis of human neutrophil granulocytes. Biochim Biophys Acta 1793:1041–1049

    Article  PubMed  CAS  Google Scholar 

  137. 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 285:37458–37466

    Article  PubMed  CAS  Google Scholar 

  138. 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 Ca(2+) store in neuroendocrine cells with a vesicle-associated membrane protein aequorin chimaera. J Cell Biol 155:41–51

    Article  PubMed  CAS  Google Scholar 

  139. 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 

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Acknowledgments

The author thanks Dr. Joshua S. Mylne for proofreading of the manuscript, Dr. Parashuraman Seetharaman for discussion and critical reading, and Dr. Giada Giacchetti for assistance with manuscript preparation and artworks.

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Correspondence to Massimo Micaroni .

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Micaroni, M. (2012). Calcium Around the Golgi Apparatus: Implications for Intracellular Membrane Trafficking. In: Islam, M. (eds) Calcium Signaling. Advances in Experimental Medicine and Biology, vol 740. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2888-2_18

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