Skip to main content
SpringerLink
Log in

Microdomains Associated to Lipid Rafts

  • Chapter
  • First Online:
Calcium Entry Pathways in Non-excitable Cells

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 898))

Abstract

Store Operated Ca2+ Entry (SOCE), the main Ca2+ influx mechanism in non-excitable cells, is implicated in the immune response and has been reported to be affected in several pathologies including cancer. The basic molecular constituents of SOCE are Orai, the pore forming unit, and STIM, a multidomain protein with at least two principal functions: one is to sense the Ca2+ content inside the lumen of the endoplasmic reticulum(ER) and the second is to activate Orai channels upon depletion of the ER. The link between Ca2+ depletion inside the ER and Ca2+ influx from extracellular media is through a direct association of STIM and Orai, but for this to occur, both molecules have to interact and form clusters where ER and plasma membrane (PM) are intimately apposed. In recent years a great number of components have been identified as participants in SOCE regulation, including regions of plasma membrane enriched in cholesterol and sphingolipids, the so called lipid rafts, which recruit a complex platform of specialized microdomains, which cells use to regulate spatiotemporal Ca2+ signals.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

AC8:

Adenylyl cyclase 8

APC:

Adenomatous polyposis coli

ARC channels:

Arachidonic acid gated channels

ASM:

Airway smooth muscle

CaM:

Calmodulin

cAMP:

Cyclic adenosine monophosphate

Cav1.2:

Voltage gated Ca2+ channel 1.2

Cav-1:

Caveolin 1

CNS:

Central nervous system

CRAC:

Cholesterol recognition/amino acid consensus

CRACR2A:

Ca2+ release-activated Ca2+ channel regulator 2A

DRMs:

Detergent-resistance membranes

EAE:

Experimental autoimmune encephalomyelitis

ER:

Endoplasmic reticulum

ERM:

Ezrin/radixin/moesin domain

ER-PM junctions:

Endoplasmic reticulum-plasma membrane junctions

FCS:

Fluorescence correlation spectroscopy

FRET:

Fluorescence resonance energy transfer

GPI:

Glycosylphosphatidyl inositol

HEK293:

Human embryonic kidney 293

IBD:

Inflammatory bowel disease

Icrac:

Ca2+ release-activated Ca2+ current

IP3R:

Inositol trisphosphate receptor

IS:

Immunological synapse

MS:

Multiple sclerosis

MβCD:

Methyl-β-cyclodextrin

NFAT:

Nuclear factor of activated T-cells

PDGF:

Platelet-derived growth factor

PI4P:

Phosphatidylinositol 4-phosphate

PIP2 :

Phosphatidylinositol 4,5-biphosphate

PIP3 :

Phosphatidylinositol (3,4,5)-trisphosphate

PIP5KIβ:

Phosphatidylinositol 4-phosphate-5-kinase I isoform β

PIP5KIγ:

Phosphatidylinositol 4-phosphate-5-kinase I isoform γ

PKB:

Protein kinase B

PM:

Plasma membrane

PMCA:

Plasma membrane Ca2+-ATPase

POST:

Partner of STIM1

RYR:

Ryanodine receptor

SCID:

Severe combined immunodeficiency

SERCA:

Sarco/endoplasmic reticulum Ca2+-ATPase

SG:

Salivary gland

SOCE:

Store operated Ca2+ entry

SOCIC:

Store operated Ca2+ influx complex

SPCA2:

Secretory pathway Ca2+-ATPase

TCR:

T-cells receptors

TIRFM:

Total internal reflexion fluorescence microscopy

TRPC:

Transient receptor potential canonical

VGCC:

Voltage gated Ca2+ channels

References

  1. Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175(4023):720–731

    Article  CAS  PubMed  Google Scholar 

  2. Goni FM (2014) The basic structure and dynamics of cell membranes: an update of the Singer-Nicolson model. Biochim Biophys Acta 1838(6):1467–1476

    Article  CAS  PubMed  Google Scholar 

  3. Vereb G, Szollosi J, Matko J, Nagy P, Farkas T, Vigh L, Matyus L, Waldmann TA, Damjanovich S (2003) Dynamic, yet structured: the cell membrane three decades after the Singer-Nicolson model. Proc Natl Acad Sci U S A 100(14):8053–8058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Blom T, Somerharju P, Ikonen E (2011) Synthesis and biosynthetic trafficking of membrane lipids. Cold Spring Harb Perspect Biol 3(8):a004713

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Pike LJ (2006) Rafts defined: a report on the keystone symposium on lipid rafts and cell function. J Lipid Res 47(7):1597–1598

    Article  CAS  PubMed  Google Scholar 

  6. Epand RM (2006) Cholesterol and the interaction of proteins with membrane domains. Prog Lipid Res 45(4):279–294

    Article  CAS  PubMed  Google Scholar 

  7. Quinn PJ (2010) A lipid matrix model of membrane raft structure. Prog Lipid Res 49(4):390–406

    Article  CAS  PubMed  Google Scholar 

  8. Laude AJ, Prior IA (2004) Plasma membrane microdomains: organization, function and trafficking. Mol Membr Biol 21(3):193–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Vaca L (2010) SOCIC: the store-operated calcium influx complex. Cell Calcium 47(3):199–209

    Article  CAS  PubMed  Google Scholar 

  10. Hogan PG, Lewis RS, Rao A (2010) Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu Rev Immunol 28:491–533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Alicia S, Angelica Z, Carlos S, Alfonso S, Vaca L (2008) STIM1 converts TRPC1 from a receptor-operated to a store-operated channel: moving TRPC1 in and out of lipid rafts. Cell Calcium 44(5):479–491

    Article  CAS  PubMed  Google Scholar 

  12. Galan C, Woodard GE, Dionisio N, Salido GM, Rosado JA (2010) Lipid rafts modulate the activation but not the maintenance of store-operated Ca(2+) entry. Biochim Biophys Acta 1803(9):1083–1093

    Article  CAS  PubMed  Google Scholar 

  13. Pani B, Ong HL, Liu X, Rauser K, Ambudkar IS, Singh BB (2008) Lipid rafts determine clustering of STIM1 in endoplasmic reticulum-plasma membrane junctions and regulation of store-operated Ca2+ entry (SOCE). J Biol Chem 283(25):17333–17340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Shim AH, Tirado-Lee L, Prakriya M (2015) Structural and functional mechanisms of CRAC channel regulation. J Mol Biol 427(1):77–93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Baba Y, Hayashi K, Fujii Y, Mizushima A, Watarai H, Wakamori M, Numaga T, Mori Y, Iino M, Hikida M, Kurosaki T (2006) Coupling of STIM1 to store-operated Ca2+ entry through its constitutive and inducible movement in the endoplasmic reticulum. Proc Natl Acad Sci U S A 103(45):16704–16709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Wu MM, Buchanan J, Luik RM, Lewis RS (2006) Ca2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J Cell Biol 174(6):803–813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Luik RM, Wang B, Prakriya M, Wu MM, Lewis RS (2008) Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation. Nature 454(7203):538–542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Forstner GG, Tanaka K, Isselbacher KJ (1968) Lipid composition of the isolated rat intestinal microvillus membrane. Biochem J 109(1):51–59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Kawai K, Fujita M, Nakao M (1974) Lipid components of two different regions of an intestinal epithelial cell membrane of mouse. Biochim Biophys Acta 369(2):222–233

    Article  CAS  PubMed  Google Scholar 

  20. Simons K, van Meer G (1988) Lipid sorting in epithelial cells. Biochemistry 27(17):6197–6202

    Article  CAS  PubMed  Google Scholar 

  21. Sankaram MB, Thompson TE (1991) Cholesterol-induced fluid-phase immiscibility in membranes. Proc Natl Acad Sci U S A 88(19):8686–8690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Brown DA, London E (1998) Structure and origin of ordered lipid domains in biological membranes. J Membr Biol 164(2):103–114

    Article  CAS  PubMed  Google Scholar 

  23. Brown DA, Rose JK (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68(3):533–544

    Article  CAS  PubMed  Google Scholar 

  24. Sonnino S, Prinetti A (2013) Membrane domains and the “lipid raft” concept. Curr Med Chem 20(1):4–21

    CAS  PubMed  Google Scholar 

  25. Brown DA, London E (1997) Structure of detergent-resistant membrane domains: does phase separation occur in biological membranes? Biochem Biophys Res Commun 240(1):1–7

    Article  CAS  PubMed  Google Scholar 

  26. Schroeder R, London E, Brown D (1994) Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior. Proc Natl Acad Sci U S A 91(25):12130–12134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Ahmed SN, Brown DA, London E (1997) On the origin of sphingolipid/cholesterol-rich detergent-insoluble cell membranes: physiological concentrations of cholesterol and sphingolipid induce formation of a detergent-insoluble, liquid-ordered lipid phase in model membranes. Biochemistry 36(36):10944–10953

    Article  CAS  PubMed  Google Scholar 

  28. Cerneus DP, Ueffing E, Posthuma G, Strous GJ, van der Ende A (1993) Detergent insolubility of alkaline phosphatase during biosynthetic transport and endocytosis. Role of cholesterol. J Biol Chem 268(5):3150–3155

    CAS  PubMed  Google Scholar 

  29. Melkonian KA, Chu T, Tortorella LB, Brown DA (1995) Characterization of proteins in detergent-resistant membrane complexes from Madin-Darby canine kidney epithelial cells. Biochemistry 34(49):16161–16170

    Article  CAS  PubMed  Google Scholar 

  30. Munro S (2003) Lipid rafts: elusive or illusive? Cell 115(4):377–388

    Article  CAS  PubMed  Google Scholar 

  31. Harder T, Scheiffele P, Verkade P, Simons K (1998) Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol 141(4):929–942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Pralle A, Keller P, Florin EL, Simons K, Horber JK (2000) Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J Cell Biol 148(5):997–1008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Sohn HW, Tolar P, Jin T, Pierce SK (2006) Fluorescence resonance energy transfer in living cells reveals dynamic membrane changes in the initiation of B cell signaling. Proc Natl Acad Sci U S A 103(21):8143–8148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Varma R, Mayor S (1998) GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394(6695):798–801

    Article  CAS  PubMed  Google Scholar 

  35. Lasserre R, Guo XJ, Conchonaud F, Hamon Y, Hawchar O, Bernard AM, Soudja SM, Lenne PF, Rigneault H, Olive D, Bismuth G, Nunes JA, Payrastre B, Marguet D, He HT (2008) Raft nanodomains contribute to Akt/PKB plasma membrane recruitment and activation. Nat Chem Biol 4(9):538–547

    Article  CAS  PubMed  Google Scholar 

  36. Lenne PF, Wawrezinieck L, Conchonaud F, Wurtz O, Boned A, Guo XJ, Rigneault H, He HT, Marguet D (2006) Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. EMBO J 25(14):3245–3256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Wenger J, Conchonaud F, Dintinger J, Wawrezinieck L, Ebbesen TW, Rigneault H, Marguet D, Lenne PF (2007) Diffusion analysis within single nanometric apertures reveals the ultrafine cell membrane organization. Biophys J 92(3):913–919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Asanov A, Zepeda A, Vaca L (2010) A novel form of Total Internal Reflection Fluorescence Microscopy (LG-TIRFM) reveals different and independent lipid raft domains in living cells. Biochim Biophys Acta 1801(2):147–155

    Article  CAS  PubMed  Google Scholar 

  39. Lingwood D, Kaiser HJ, Levental I, Simons K (2009) Lipid rafts as functional heterogeneity in cell membranes. Biochem Soc Trans 37(Pt 5):955–960

    Article  CAS  PubMed  Google Scholar 

  40. Owen DM, Magenau A, Williamson D, Gaus K (2012) The lipid raft hypothesis revisited--new insights on raft composition and function from super-resolution fluorescence microscopy. Bioessays 34(9):739–747

    Article  CAS  PubMed  Google Scholar 

  41. Grigoriev I, Gouveia SM, van der Vaart B, Demmers J, Smyth JT, Honnappa S, Splinter D, Steinmetz MO, Putney JW Jr, Hoogenraad CC, Akhmanova A (2008) STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Curr Biol 18(3):177–182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Asanov A, Sherry R, Sampieri A, Vaca L (2013) A relay mechanism between EB1 and APC facilitate STIM1 puncta assembly at endoplasmic reticulum-plasma membrane junctions. Cell Calcium 54(3):246–256

    Article  CAS  PubMed  Google Scholar 

  43. Roos J, DiGregorio PJ, Yeromin AV, Ohlsen K, Lioudyno M, Zhang S, Safrina O, Kozak JA, Wagner SL, Cahalan MD, Velicelebi G, Stauderman KA (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 169(3):435–445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Palty R, Raveh A, Kaminsky I, Meller R, Reuveny E (2012) SARAF inactivates the store operated calcium entry machinery to prevent excess calcium refilling. Cell 149(2):425–438

    Article  CAS  PubMed  Google Scholar 

  45. 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  CAS  PubMed  Google Scholar 

  46. Srikanth S, Jung HJ, Kim KD, Souda P, Whitelegge J, Gwack Y (2010) A novel EF-hand protein, CRACR2A, is a cytosolic Ca2+ sensor that stabilizes CRAC channels in T cells. Nat Cell Biol 12(5):436–446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Zhou Y, Meraner P, Kwon HT, Machnes D, Oh-hora M, Zimmer J, Huang Y, Stura A, Rao A, Hogan PG (2010) STIM1 gates the store-operated calcium channel ORAI1 in vitro. Nat Struct Mol Biol 17(1):112–116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Hoth M, Penner R (1993) Calcium release-activated calcium current in rat mast cells. J Physiol 465:359–386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Liu X, Groschner K, Ambudkar IS (2004) Distinct Ca(2+)-permeable cation currents are activated by internal Ca(2+)-store depletion in RBL-2H3 cells and human salivary gland cells, HSG and HSY. J Membr Biol 200(2):93–104

    Article  CAS  PubMed  Google Scholar 

  50. Birnbaumer L (2009) The TRPC class of ion channels: a critical review of their roles in slow, sustained increases in intracellular Ca(2+) concentrations. Annu Rev Pharmacol Toxicol 49:395–426

    Article  CAS  PubMed  Google Scholar 

  51. Huang GN, Zeng W, Kim JY, Yuan JP, Han L, Muallem S, Worley PF (2006) STIM1 carboxyl-terminus activates native SOC, I(crac) and TRPC1 channels. Nat Cell Biol 8(9):1003–1010

    Article  CAS  PubMed  Google Scholar 

  52. Yuan JP, Zeng W, Huang GN, Worley PF, Muallem S (2007) STIM1 heteromultimerizes TRPC channels to determine their function as store-operated channels. Nat Cell Biol 9(6):636–645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Cheng KT, Liu X, Ong HL, Ambudkar IS (2008) Functional requirement for Orai1 in store-operated TRPC1-STIM1 channels. J Biol Chem 283(19):12935–12940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Asanov A, Sampieri A, Moreno C, Pacheco J, Salgado A, Sherry R, Vaca L (2015) Combined single channel and single molecule detection identifies subunit composition of STIM1-activated transient receptor potential canonical (TRPC) channels. Cell Calcium 57(1):1–13

    Article  CAS  PubMed  Google Scholar 

  55. Soboloff J, Rothberg BS, Madesh M, Gill DL (2012) STIM proteins: dynamic calcium signal transducers. Nat Rev Mol Cell Biol 13(9):549–565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Sampieri A, Zepeda A, Asanov A, Vaca L (2009) Visualizing the store-operated channel complex assembly in real time: identification of SERCA2 as a new member. Cell Calcium 45(5):439–446

    Article  CAS  PubMed  Google Scholar 

  57. Smyth JT, DeHaven WI, Bird GS, Putney JW Jr (2007) Role of the microtubule cytoskeleton in the function of the store-operated Ca2+ channel activator STIM1. J Cell Sci 120(Pt 21):3762–3771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Galan C, Dionisio N, Smani T, Salido GM, Rosado JA (2011) The cytoskeleton plays a modulatory role in the association between STIM1 and the Ca2+ channel subunits Orai1 and TRPC1. Biochem Pharmacol 82(4):400–410

    Article  CAS  PubMed  Google Scholar 

  59. Prins D, Groenendyk J, Touret N, Michalak M (2011) Modulation of STIM1 and capacitative Ca2+ entry by the endoplasmic reticulum luminal oxidoreductase ERp57. EMBO Rep 12(11):1182–1188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Thompson JL, Mignen O, Shuttleworth TJ (2013) The ARC channel – an endogenous store-independent Orai channel. Curr Top Membr 71:125–148

    Article  CAS  PubMed  Google Scholar 

  62. Thompson JL, Shuttleworth TJ (2012) A plasma membrane-targeted cytosolic domain of STIM1 selectively activates ARC channels, an arachidonate-regulated store-independent Orai channel. Channels 6(5):370–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Zhang X, Gonzalez-Cobos JC, Schindl R, Muik M, Ruhle B, Motiani RK, Bisaillon JM, Zhang W, Fahrner M, Barroso M, Matrougui K, Romanin C, Trebak M (2013) Mechanisms of STIM1 activation of store-independent leukotriene C4-regulated Ca2+ channels. Mol Cell Biol 33(18):3715–3723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Wang Y, Deng X, Mancarella S, Hendron E, Eguchi S, Soboloff J, Tang XD, Gill DL (2010) The calcium store sensor, STIM1, reciprocally controls Orai and CaV1.2 channels. Science 330(6000):105–109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Yu F, Sun L, Hubrack S, Selvaraj S, Machaca K (2013) Intramolecular shielding maintains the ER Ca(2)(+) sensor STIM1 in an inactive conformation. J Cell Sci 126(Pt 11):2401–2410

    Article  CAS  PubMed  Google Scholar 

  66. Stathopulos PB, Schindl R, Fahrner M, Zheng L, Gasmi-Seabrook GM, Muik M, Romanin C, Ikura M (2013) STIM1/Orai1 coiled-coil interplay in the regulation of store-operated calcium entry. Nat Commun 4:2963

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Walsh CM, Doherty MK, Tepikin AV, Burgoyne RD (2010) Evidence for an interaction between Golli and STIM1 in store-operated calcium entry. Biochem J 430(3):453–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Maleth J, Choi S, Muallem S, Ahuja M (2014) Translocation between PI(4,5)P2-poor and PI(4,5)P2-rich microdomains during store depletion determines STIM1 conformation and Orai1 gating. Nat Commun 5:5843

    Article  PubMed  PubMed Central  Google Scholar 

  69. Mullins FM, Park CY, Dolmetsch RE, Lewis RS (2009) STIM1 and calmodulin interact with Orai1 to induce Ca2+ -dependent inactivation of CRAC channels. Proc Natl Acad Sci U S A 106(36):15495–15500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Srikanth S, Jew M, Kim KD, Yee MK, Abramson J, Gwack Y (2012) Junctate is a Ca2+-sensing structural component of Orai1 and stromal interaction molecule 1 (STIM1). Proc Natl Acad Sci U S A 109(22):8682–8687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Krapivinsky G, Krapivinsky L, Stotz SC, Manasian Y, Clapham DE (2011) POST, partner of stromal interaction molecule 1 (STIM1), targets STIM1 to multiple transporters. Proc Natl Acad Sci U S A 108(48):19234–19239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Cully TR, Edwards JN, Friedrich O, Stephenson DG, Murphy RM, Launikonis BS (2012) Changes in plasma membrane Ca-ATPase and stromal interacting molecule 1 expression levels for Ca(2+) signaling in dystrophic mdx mouse muscle. Am J Physiol Cell Physiol 303(5):C567–C576

    Article  CAS  PubMed  Google Scholar 

  73. Quintana A, Pasche M, Junker C, Al-Ansary D, Rieger H, Kummerow C, Nunez L, Villalobos C, Meraner P, Becherer U, Rettig J, Niemeyer BA, Hoth M (2011) Calcium microdomains at the immunological synapse: how ORAI channels, mitochondria and calcium pumps generate local calcium signals for efficient T-cell activation. EMBO J 30(19):3895–3912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Sathish V, Abcejo AJ, Thompson MA, Sieck GC, Prakash YS, Pabelick CM (2012) Caveolin-1 regulation of store-operated Ca(2+) influx in human airway smooth muscle. Eur Respir J 40(2):470–478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Brazer SC, Singh BB, Liu X, Swaim W, Ambudkar IS (2003) Caveolin-1 contributes to assembly of store-operated Ca2+ influx channels by regulating plasma membrane localization of TRPC1. J Biol Chem 278(29):27208–27215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Pani B, Ong HL, Brazer SC, Liu X, Rauser K, Singh BB, Ambudkar IS (2009) Activation of TRPC1 by STIM1 in ER-PM microdomains involves release of the channel from its scaffold caveolin-1. Proc Natl Acad Sci U S A 106(47):20087–20092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Yu F, Sun L, Machaca K (2010) Constitutive recycling of the store-operated Ca2+ channel Orai1 and its internalization during meiosis. J Cell Biol 191(3):523–535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Dustin ML (2014) The immunological synapse. Cancer Immunol Res 2(11):1023–1033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Martin AC, Willoughby D, Ciruela A, Ayling LJ, Pagano M, Wachten S, Tengholm A, Cooper DM (2009) Capacitative Ca2+ entry via Orai1 and stromal interacting molecule 1 (STIM1) regulates adenylyl cyclase type 8. Mol Pharmacol 75(4):830–842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Willoughby D, Everett KL, Halls ML, Pacheco J, Skroblin P, Vaca L, Klussmann E, Cooper DM (2012) Direct binding between Orai1 and AC8 mediates dynamic interplay between Ca2+ and cAMP signaling. Sci Signal 5(219), ra29

    Article  PubMed  Google Scholar 

  81. Ayling LJ, Briddon SJ, Halls ML, Hammond GR, Vaca L, Pacheco J, Hill SJ, Cooper DM (2012) Adenylyl cyclase AC8 directly controls its micro-environment by recruiting the actin cytoskeleton in a cholesterol-rich milieu. J Cell Sci 125(Pt 4):869–886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Murata T, Lin MI, Stan RV, Bauer PM, Yu J, Sessa WC (2007) Genetic evidence supporting caveolae microdomain regulation of calcium entry in endothelial cells. J Biol Chem 282(22):16631–16643

    Article  CAS  PubMed  Google Scholar 

  83. Prakash YS, Thompson MA, Vaa B, Matabdin I, Peterson TE, He T, Pabelick CM (2007) Caveolins and intracellular calcium regulation in human airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 293(5):L1118–L1126

    Article  CAS  PubMed  Google Scholar 

  84. Jardin I, Salido GM, Rosado JA (2008) Role of lipid rafts in the interaction between hTRPC1, Orai1 and STIM1. Channels 2(6):401–403

    Article  PubMed  Google Scholar 

  85. Dionisio N, Galan C, Jardin I, Salido GM, Rosado JA (2011) Lipid rafts are essential for the regulation of SOCE by plasma membrane resident STIM1 in human platelets. Biochim Biophys Acta 1813(3):431–437

    Article  CAS  PubMed  Google Scholar 

  86. Pike LJ (2004) Lipid rafts: heterogeneity on the high seas. Biochem J 378(Pt 2):281–292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Parton RG, Richards AA (2003) Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 4(11):724–738

    Article  CAS  PubMed  Google Scholar 

  88. Lockwich TP, Liu X, Singh BB, Jadlowiec J, Weiland S, Ambudkar IS (2000) Assembly of Trp1 in a signaling complex associated with caveolin-scaffolding lipid raft domains. J Biol Chem 275(16):11934–11942

    Article  CAS  PubMed  Google Scholar 

  89. Rathor N, Chung HK, Wang SR, Wang JY, Turner DJ, Rao JN (2014) Caveolin-1 enhances rapid mucosal restitution by activating TRPC1-mediated Ca2+ signaling. Physiol Rep 2(11):1–11

    Google Scholar 

  90. Pani B, Liu X, Bollimuntha S, Cheng KT, Niesman IR, Zheng C, Achen VR, Patel HH, Ambudkar IS, Singh BB (2013) Impairment of TRPC1-STIM1 channel assembly and AQP5 translocation compromise agonist-stimulated fluid secretion in mice lacking caveolin1. J Cell Sci 126(Pt 2):667–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Gwozdz T, Dutko-Gwozdz J, Schafer C, Bolotina VM (2012) Overexpression of Orai1 and STIM1 proteins alters regulation of store-operated Ca2+ entry by endogenous mediators. J Biol Chem 287(27):22865–22872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Wu MM, Covington ED, Lewis RS (2014) Single-molecule analysis of diffusion and trapping of STIM1 and Orai1 at ER-plasma membrane junctions. Mol Biol Cell 25:3672–3685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Liu Y, Casey L, Pike LJ (1998) Compartmentalization of phosphatidylinositol 4,5-bisphosphate in low-density membrane domains in the absence of caveolin. Biochem Biophys Res Commun 245(3):684–690

    Article  CAS  PubMed  Google Scholar 

  94. Brown DA (2006) Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology 21:430–439

    Article  CAS  PubMed  Google Scholar 

  95. Brown DA, London E (1998) Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 14:111–136

    Article  CAS  PubMed  Google Scholar 

  96. Zacharias DA, Violin JD, Newton AC, Tsien RY (2002) Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296(5569):913–916

    Article  CAS  PubMed  Google Scholar 

  97. Epand RM (2008) Proteins and cholesterol-rich domains. Biochim Biophys Acta 1778(7–8):1576–1582

    Article  CAS  PubMed  Google Scholar 

  98. Levental I, Grzybek M, Simons K (2010) Greasing their way: lipid modifications determine protein association with membrane rafts. Biochemistry 49(30):6305–6316

    Article  CAS  PubMed  Google Scholar 

  99. Gagnoux-Palacios L, Dans M, van’t Hof W, Mariotti A, Pepe A, Meneguzzi G, Resh MD, Giancotti FG (2003) Compartmentalization of integrin alpha6beta4 signaling in lipid rafts. J Cell Biol 162(7):1189–1196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Feng JM, Hu YK, Xie LH, Colwell CS, Shao XM, Sun XP, Chen B, Tang H, Campagnoni AT (2006) Golli protein negatively regulates store depletion-induced calcium influx in T cells. Immunity 24(6):717–727

    Article  CAS  PubMed  Google Scholar 

  101. Fantini J, Barrantes FJ (2013) How cholesterol interacts with membrane proteins: an exploration of cholesterol-binding sites including CRAC, CARC, and tilted domains. Front Physiol 4:31

    PubMed  PubMed Central  Google Scholar 

  102. Li H, Papadopoulos V (1998) Peripheral-type benzodiazepine receptor function in cholesterol transport. Identification of a putative cholesterol recognition/interaction amino acid sequence and consensus pattern. Endocrinology 139(12):4991–4997

    CAS  PubMed  Google Scholar 

  103. Dietzen DJ, Hastings WR, Lublin DM (1995) Caveolin is palmitoylated on multiple cysteine residues. Palmitoylation is not necessary for localization of caveolin to caveolae. J Biol Chem 270(12):6838–6842

    Article  CAS  PubMed  Google Scholar 

  104. Yang G, Xu H, Li Z, Li F (2014) Interactions of caveolin-1 scaffolding and intramembrane regions containing a CRAC motif with cholesterol in lipid bilayers. Biochim Biophys Acta 1838(10):2588–2599

    Article  CAS  PubMed  Google Scholar 

  105. Epand RM, Sayer BG, Epand RF (2005) Caveolin scaffolding region and cholesterol-rich domains in membranes. J Mol Biol 345(2):339–350

    Article  CAS  PubMed  Google Scholar 

  106. Fridolfsson HN, Roth DM, Insel PA, Patel HH (2014) Regulation of intracellular signaling and function by caveolin. FASEB J 28:3823–3831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Dziadek MA, Johnstone LS (2007) Biochemical properties and cellular localisation of STIM proteins. Cell Calcium 42(2):123–132

    Article  CAS  PubMed  Google Scholar 

  108. Parameswaran N, Gupta N (2013) Re-defining ERM function in lymphocyte activation and migration. Immunol Rev 256(1):63–79

    Article  CAS  PubMed  Google Scholar 

  109. Heo WD, Inoue T, Park WS, Kim ML, Park BO, Wandless TJ, Meyer T (2006) PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314(5804):1458–1461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Collins SR, Meyer T (2011) Evolutionary origins of STIM1 and STIM2 within ancient Ca2+ signaling systems. Trends Cell Biol 21(4):202–211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Zhou Y, Srinivasan P, Razavi S, Seymour S, Meraner P, Gudlur A, Stathopulos PB, Ikura M, Rao A, Hogan PG (2013) Initial activation of STIM1, the regulator of store-operated calcium entry. Nat Struct Mol Biol 20(8):973–981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. 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 U S A 104(22):9301–9306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Korzeniowski MK, Popovic MA, Szentpetery Z, Varnai P, Stojilkovic SS, Balla T (2009) Dependence of STIM1/Orai1-mediated calcium entry on plasma membrane phosphoinositides. J Biol Chem 284(31):21027–21035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Walsh CM, Chvanov M, Haynes LP, Petersen OH, Tepikin AV, Burgoyne RD (2010) Role of phosphoinositides in STIM1 dynamics and store-operated calcium entry. Biochem J 425(1):159–168

    Article  CAS  PubMed Central  Google Scholar 

  115. Calloway N, Owens T, Corwith K, Rodgers W, Holowka D, Baird B (2011) Stimulated association of STIM1 and Orai1 is regulated by the balance of PtdIns(4,5)P(2) between distinct membrane pools. J Cell Sci 124(Pt 15):2602–2610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Crossthwaite AJ, Seebacher T, Masada N, Ciruela A, Dufraux K, Schultz JE, Cooper DM (2005) The cytosolic domains of Ca2+-sensitive adenylyl cyclases dictate their targeting to plasma membrane lipid rafts. J Biol Chem 280(8):6380–6391

    Article  CAS  PubMed  Google Scholar 

  117. Head BP, Patel HH, Insel PA (2014) Interaction of membrane/lipid rafts with the cytoskeleton: impact on signaling and function: membrane/lipid rafts, mediators of cytoskeletal arrangement and cell signaling. Biochim Biophys Acta 1838(2):532–545

    Article  CAS  PubMed  Google Scholar 

  118. Vasudevan L, Jeromin A, Volpicelli-Daley L, De Camilli P, Holowka D, Baird B (2009) The beta- and gamma-isoforms of type I PIP5K regulate distinct stages of Ca2+ signaling in mast cells. J Cell Sci 122(Pt 14):2567–2574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Schon A, Freire E (1989) Thermodynamics of intersubunit interactions in cholera toxin upon binding to the oligosaccharide portion of its cell surface receptor, ganglioside GM1. Biochemistry 28(12):5019–5024

    Article  CAS  PubMed  Google Scholar 

  120. Somlyo AP, Bond M, Somlyo AV (1985) Calcium content of mitochondria and endoplasmic reticulum in liver frozen rapidly in vivo. Nature 314(6012):622–625

    Article  CAS  PubMed  Google Scholar 

  121. Carrasco S, Meyer T (2011) STIM proteins and the endoplasmic reticulum-plasma membrane junctions. Annu Rev Biochem 80:973–1000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Lam AK, Galione A (2013) The endoplasmic reticulum and junctional membrane communication during calcium signaling. Biochim Biophys Acta 1833(11):2542–2559

    Article  CAS  PubMed  Google Scholar 

  123. Lee KW, Maeng JS, Choi JY, Lee YR, Hwang CY, Park SS, Park HK, Chung BH, Lee SG, Kim YS, Jeon H, Eom SH, Kang C, Kim do H, Kwon KS (2012) Role of Junctin protein interactions in cellular dynamics of calsequestrin polymer upon calcium perturbation. J Biol Chem 287(3):1679–1687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Pan Z, Yang D, Nagaraj RY, Nosek TA, Nishi M, Takeshima H, Cheng H, Ma J (2002) Dysfunction of store-operated calcium channel in muscle cells lacking mg29. Nat Cell Biol 4(5):379–383

    Article  CAS  PubMed  Google Scholar 

  125. Giordano F, Saheki Y, Idevall-Hagren O, Colombo SF, Pirruccello M, Milosevic I, Gracheva EO, Bagriantsev SN, Borgese N, De Camilli P (2013) PI(4,5)P(2)-dependent and Ca(2+)-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153(7):1494–1509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Chang CL, Hsieh TS, Yang TT, Rothberg KG, Azizoglu DB, Volk E, Liao JC, Liou J (2013) Feedback regulation of receptor-induced Ca2+ signaling mediated by E-Syt1 and Nir2 at endoplasmic reticulum-plasma membrane junctions. Cell Rep 5(3):813–825

    Article  PubMed  CAS  Google Scholar 

  127. Takeshima H, Komazaki S, Nishi M, Iino M, Kangawa K (2000) Junctophilins: a novel family of junctional membrane complex proteins. Mol Cell 6(1):11–22

    CAS  PubMed  Google Scholar 

  128. Stefan CJ, Manford AG, Emr SD (2013) ER-PM connections: sites of information transfer and inter-organelle communication. Curr Opin Cell Biol 25(4):434–442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Stiber J, Hawkins A, Zhang ZS, Wang S, Burch J, Graham V, Ward CC, Seth M, Finch E, Malouf N, Williams RS, Eu JP, Rosenberg P (2008) STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat Cell Biol 10(6):688–697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Xu P, Lu J, Li Z, Yu X, Chen L, Xu T (2006) Aggregation of STIM1 underneath the plasma membrane induces clustering of Orai1. Biochem Biophys Res Commun 350(4):969–976

    Article  CAS  PubMed  Google Scholar 

  131. Luik RM, Wu MM, Buchanan J, Lewis RS (2006) The elementary unit of store-operated Ca2+ entry: local activation of CRAC channels by STIM1 at ER-plasma membrane junctions. J Cell Biol 174(6):815–825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Orci L, Ravazzola M, Le Coadic M, Shen WW, Demaurex N, Cosson P (2009) From the cover: STIM1-induced precortical and cortical subdomains of the endoplasmic reticulum. Proc Natl Acad Sci U S A 106(46):19358–19362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Sharma S, Quintana A, Findlay GM, Mettlen M, Baust B, Jain M, Nilsson R, Rao A, Hogan PG (2013) An siRNA screen for NFAT activation identifies septins as coordinators of store-operated Ca2+ entry. Nature 499(7457):238–242

    Article  CAS  PubMed  Google Scholar 

  134. Srikanth S, Gwack Y (2012) Orai1, STIM1, and their associating partners. J Physiol 590(Pt 17):4169–4177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Treves S, Vukcevic M, Griesser J, Armstrong CF, Zhu MX, Zorzato F (2010) Agonist-activated Ca2+ influx occurs at stable plasma membrane and endoplasmic reticulum junctions. J Cell Sci 123(Pt 23):4170–4181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Nathke IS (2004) The adenomatous polyposis coli protein: the Achilles heel of the gut epithelium. Annu Rev Cell Dev Biol 20:337–366

    Article  PubMed  CAS  Google Scholar 

  137. Lur G, Haynes LP, Prior IA, Gerasimenko OV, Feske S, Petersen OH, Burgoyne RD, Tepikin AV (2009) Ribosome-free terminals of rough ER allow formation of STIM1 puncta and segregation of STIM1 from IP(3) receptors. Curr Biol 19(19):1648–1653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Lioudyno MI, Kozak JA, Penna A, Safrina O, Zhang SL, Sen D, Roos J, Stauderman KA, Cahalan MD (2008) Orai1 and STIM1 move to the immunological synapse and are up-regulated during T cell activation. Proc Natl Acad Sci U S A 105(6):2011–2016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Jozsef L, Tashiro K, Kuo A, Park EJ, Skoura A, Albinsson S, Rivera-Molina F, Harrison KD, Iwakiri Y, Toomre D, Sessa WC (2014) Reticulon 4 is necessary for endoplasmic reticulum tubulation, STIM1-Orai1 coupling, and store-operated calcium entry. J Biol Chem 289(13):9380–9395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Holowka D, Korzeniowski MK, Bryant KL, Baird B (2014) Polyunsaturated fatty acids inhibit stimulated coupling between the ER Ca(2+) sensor STIM1 and the Ca(2+) channel protein Orai1 in a process that correlates with inhibition of stimulated STIM1 oligomerization. Biochim Biophys Acta 1841(8):1210–1216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Montixi C, Langlet C, Bernard AM, Thimonier J, Dubois C, Wurbel MA, Chauvin JP, Pierres M, He HT (1998) Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J 17(18):5334–5348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Xavier R, Brennan T, Li Q, McCormack C, Seed B (1998) Membrane compartmentation is required for efficient T cell activation. Immunity 8(6):723–732

    Article  CAS  PubMed  Google Scholar 

  143. Hashimoto-Tane A, Yokosuka T, Ishihara C, Sakuma M, Kobayashi W, Saito T (2010) T-cell receptor microclusters critical for T-cell activation are formed independently of lipid raft clustering. Mol Cell Biol 30(14):3421–3429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Owen DM, Oddos S, Kumar S, Davis DM, Neil MA, French PM, Dustin ML, Magee AI, Cebecauer M (2010) High plasma membrane lipid order imaged at the immunological synapse periphery in live T cells. Mol Membr Biol 27(4–6):178–189

    Article  CAS  PubMed  Google Scholar 

  145. Wheeler G, Tyler KM (2011) Widefield microscopy for live imaging of lipid domains and membrane dynamics. Biochim Biophys Acta 1808(3):634–641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Feske S, Giltnane J, Dolmetsch R, Staudt LM, Rao A (2001) Gene regulation mediated by calcium signals in T lymphocytes. Nat Immunol 2(4):316–324

    Article  CAS  PubMed  Google Scholar 

  147. Rao A, Luo C, Hogan PG (1997) Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol 15:707–747

    Article  CAS  PubMed  Google Scholar 

  148. Srikanth S, Gwack Y (2013) Orai1-NFAT signalling pathway triggered by T cell receptor stimulation. Mol Cells 35(3):182–194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Dolmetsch RE, Lewis RS, Goodnow CC, Healy JI (1997) Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature 386(6627):855–858

    Article  CAS  PubMed  Google Scholar 

  150. Ong HL, Jang SI, Ambudkar IS (2012) Distinct contributions of Orai1 and TRPC1 to agonist-induced [Ca(2+)](i) signals determine specificity of Ca(2+)-dependent gene expression. PLoS One 7(10), e47146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Kar P, Nelson C, Parekh AB (2011) Selective activation of the transcription factor NFAT1 by calcium microdomains near Ca2+ release-activated Ca2+ (CRAC) channels. J Biol Chem 286(17):14795–14803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Picard C, McCarl CA, Papolos A, Khalil S, Luthy K, Hivroz C, LeDeist F, Rieux-Laucat F, Rechavi G, Rao A, Fischer A, Feske S (2009) STIM1 mutation associated with a syndrome of immunodeficiency and autoimmunity. N Engl J Med 360(19):1971–1980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. McCarl CA, Khalil S, Ma J, Oh-hora M, Yamashita M, Roether J, Kawasaki T, Jairaman A, Sasaki Y, Prakriya M, Feske S (2010) Store-operated Ca2+ entry through ORAI1 is critical for T cell-mediated autoimmunity and allograft rejection. J Immunol 185(10):5845–5858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Schuhmann MK, Stegner D, Berna-Erro A, Bittner S, Braun A, Kleinschnitz C, Stoll G, Wiendl H, Meuth SG, Nieswandt B (2010) Stromal interaction molecules 1 and 2 are key regulators of autoreactive T cell activation in murine autoimmune central nervous system inflammation. J Immunol 184(3):1536–1542

    Article  CAS  PubMed  Google Scholar 

  155. Ma J, McCarl CA, Khalil S, Luthy K, Feske S (2010) T-cell-specific deletion of STIM1 and STIM2 protects mice from EAE by impairing the effector functions of Th1 and Th17 cells. Eur J Immunol 40(11):3028–3042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Bergmeier W, Weidinger C, Zee I, Feske S (2013) Emerging roles of store-operated Ca(2)(+) entry through STIM and ORAI proteins in immunity, hemostasis and cancer. Channels 7(5):379–391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Fedida-Metula S, Feldman B, Koshelev V, Levin-Gromiko U, Voronov E, Fishman D (2012) Lipid rafts couple store-operated Ca2+ entry to constitutive activation of PKB/Akt in a Ca2+/calmodulin-, Src- and PP2A-mediated pathway and promote melanoma tumor growth. Carcinogenesis 33(4):740–750

    Article  CAS  PubMed  Google Scholar 

  158. 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(1):84–98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Grim KJ, Abcejo AJ, Barnes A, Sathish V, Smelter DF, Ford GC, Thompson MA, Prakash YS, Pabelick CM (2012) Caveolae and propofol effects on airway smooth muscle. Br J Anaesth 109(3):444–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Peel SE, Liu B, Hall IP (2006) A key role for STIM1 in store operated calcium channel activation in airway smooth muscle. Respir Res 7:119

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  161. Suganuma N, Ito S, Aso H, Kondo M, Sato M, Sokabe M, Hasegawa Y (2012) STIM1 regulates platelet-derived growth factor-induced migration and Ca2+ influx in human airway smooth muscle cells. PLoS One 7(9), e45056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Putney JW Jr (1986) A model for receptor-regulated calcium entry. Cell Calcium 7(1):1–12

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, Ciudad Universitaria, México, DF, 04510, Mexico

    Jonathan Pacheco, Josué O. Ramírez-Jarquín & Luis Vaca

Authors
  1. Jonathan Pacheco
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Josué O. Ramírez-Jarquín
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luis Vaca
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luis Vaca .

Editor information

Editors and Affiliations

  1. Depto. Fisiología, University of Extremadura, Cáceres, Spain

    Juan A. Rosado

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Pacheco, J., Ramírez-Jarquín, J.O., Vaca, L. (2016). Microdomains Associated to Lipid Rafts. In: Rosado, J. (eds) Calcium Entry Pathways in Non-excitable Cells. Advances in Experimental Medicine and Biology, vol 898. Springer, Cham. https://doi.org/10.1007/978-3-319-26974-0_15

Download citation

Publish with us

Policies and ethics

Search

Navigation