Advertisement

STIM-TRP Pathways and Microdomain Organization: Contribution of TRPC1 in Store-Operated Ca2+ Entry: Impact on Ca2+ Signaling and Cell Function

  • Hwei Ling OngEmail author
  • Indu S. AmbudkarEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 993)

Abstract

Store-operated calcium entry (SOCE) is a ubiquitous Ca2+ entry pathway that is activated in response to depletion of ER-Ca2+ stores and critically controls the regulation of physiological functions in a wide variety of cell types. The transient receptor potential canonical (TRPC) channels (TRPCs 1–7), which are activated by stimuli leading to PIP2 hydrolysis, were first identified as molecular components of SOCE channels. While TRPC1 was associated with SOCE and regulation of function in several cell types, none of the TRPC members displayed ICRAC, the store-operated current identified in lymphocytes and mast cells. Intensive search finally led to the identification of Orai1 and STIM1 as the primary components of the CRAC channel. Orai1 was established as the pore-forming channel protein and STIM1 as the ER-Ca2+ sensor protein involved in activation of Orai1. STIM1 also activates TRPC1 via a distinct domain in its C-terminus. However, TRPC1 function depends on Orai1-mediated Ca2+ entry, which triggers recruitment of TRPC1 into the plasma membrane where it is activated by STIM1. TRPC1 and Orai1 form distinct store-operated Ca2+ channels that regulate specific cellular functions. It is now clearly established that regulation of TRPC1 trafficking can change plasma membrane levels of the channel, the phenotype of the store-operated Ca2+ current, as well as pattern of SOCE-mediated [Ca2+]i signals. Thus, TRPC1 is activated downstream of Orai1 and modifies the initial [Ca2+]i signal generated by Orai1. This review will highlight current concepts of the activation and regulation of TRPC1 channels and its impact on cell function.

Keywords

TRPC STIM1 Orai1 SOCE ER-PM junctions Lipid rafts Caveolin 

Notes

Acknowledgments

Work in ISA’s laboratory is supported by the Intramural Research Program of the NIH, NIDCR.

References

  1. Ahmmed GU, Mehta D, Vogel S, Holinstat M, Paria BC, Tiruppathi C, Malik AB (2004) Protein kinase Ca phosphorylates the TRPC1 channel and regulates store-operated Ca2+ entry in endothelial cells. J Biol Chem 279:20941–20949PubMedCrossRefGoogle Scholar
  2. Alabi AA, Tsien RW (2013) Perspectives on kiss-and-run: role in exocytosis, endocytosis, and neurotransmission. Annu Rev Physiol 75:393–422PubMedCrossRefGoogle Scholar
  3. 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 44:479–491PubMedCrossRefGoogle Scholar
  4. Almirza WH, Peters PH, van Zoelen EJ, Theuvenet AP (2012) Role of Trpc channels, Stim1 and Orai1 in PGF2a-induced calcium signaling in NRK fibroblasts. Cell Calcium 51:12–21PubMedCrossRefGoogle Scholar
  5. Ambudkar IS, Ong HL, Singh BB (2010) Molecular and functional determinants of Ca2+ signaling microdomains. In: Sitaramayya A (ed) Signal transduction: pathways, mechanisms and diseases. Springer, Heidelberg, pp 237–253CrossRefGoogle Scholar
  6. 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 57:1–13PubMedCrossRefGoogle Scholar
  7. Avila-Medina J, Calderon-Sanchez E, Gonzalez-Rodriguez P, Monje-Quiroga F, Rosado JA, Castellano A, Ordonez A, Smani T (2016) Orai1 and TRPC1 proteins co-localize with CaV1.2 channels to form a signal complex in vascular smooth muscle cells. J Biol Chem 291:21148–21159PubMedCrossRefGoogle Scholar
  8. Bergdahl A, Gomez MF, Dreja K, SZ X, Adner M, Beech DJ, Broman J, Hellstrand P, Sward K (2003) Cholesterol depletion impairs vascular reactivity to endothelin-1 by reducing store-operated Ca2+ entry dependent on TRPC1. Circ Res 93:839–847PubMedCrossRefGoogle Scholar
  9. Berthier A, Lemaire-Ewing S, Prunet C, Monier S, Athias A, Bessede G, Pais de Barros JP, Laubriet A, Gambert P, Lizard G, Neel D (2004) Involvement of a calcium-dependent dephosphorylation of BAD associated with the localization of Trpc-1 within lipid rafts in 7-ketocholesterol-induced THP-1 cell apoptosis. Cell Death Differ 11:897–905PubMedCrossRefGoogle Scholar
  10. Bollimuntha S, Cornatzer E, Singh BB (2005a) Plasma membrane localization and function of TRPC1 is dependent on its interaction with b-tubulin in retinal epithelium cells. Vis Neurosci 22:163–170PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bollimuntha S, Singh BB, Shavali S, Sharma SK, Ebadi M (2005b) TRPC1-mediated inhibition of 1-methyl-4-phenylpyridinium ion neurotoxicity in human SH-SY5Y neuroblastoma cells. J Biol Chem 280:2132–2140PubMedCrossRefGoogle Scholar
  12. Bomben VC, Turner KL, Barclay TT, Sontheimer H (2011) Transient receptor potential canonical channels are essential for chemotactic migration of human malignant gliomas. J Cell Physiol 226:1879–1888PubMedCrossRefGoogle Scholar
  13. Brandman O, Liou J, Park WS, Meyer T (2007) STIM2 is a feedback regulator that stabilizes basal cytosolic and endoplasmic reticulum Ca2+ levels. Cell 131:1327–1339PubMedPubMedCentralCrossRefGoogle Scholar
  14. 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 278:27208–27215PubMedPubMedCentralCrossRefGoogle Scholar
  15. Brownlow SL, Sage SO (2005) Transient receptor potential protein subunit assembly and membrane distribution in human platelets. Thromb Haemost 94:839–845PubMedGoogle Scholar
  16. Brownlow SL, Harper AG, Harper MT, Sage SO (2004) A role for hTRPC1 and lipid raft domains in store-mediated calcium entry in human platelets. Cell Calcium 35:107–113PubMedCrossRefGoogle Scholar
  17. Byron KL (1996) Vasopressin stimulates Ca2+ spiking activity in A7r5 vascular smooth muscle cells via activation of phospholipase A2. Circ Res 78:813–820PubMedCrossRefGoogle Scholar
  18. Cahalan MD, Lewis RS (1990) Functional roles of ion channels in lymphocytes. Semin Immunol 2:107–117PubMedGoogle Scholar
  19. Chang CL, Liou J (2016) Homeostatic regulation of the PI(4,5)P2-Ca2+ signaling system at ER–PM junctions. Biochim Biophys Acta 1861:862–873PubMedPubMedCentralCrossRefGoogle Scholar
  20. 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 5:813–825PubMedCrossRefGoogle Scholar
  21. Chantome A, Potier-Cartereau M, Clarysse L, Fromont G, Marionneau-Lambot S, Gueguinou M, Pages JC, Collin C, Oullier T, Girault A, Arbion F, Haelters JP, Jaffres PA, Pinault M, Besson P, Joulin V, Bougnoux P, Vandier C (2013) Pivotal role of the lipid Raft SK3-Orai1 complex in human cancer cell migration and bone metastases. Cancer Res 73:4852–4861PubMedCrossRefGoogle Scholar
  22. Chao JT, Wong AK, Tavassoli S, Young BP, Chruscicki A, Fang NN, Howe LJ, Mayor T, Foster LJ, Loewen CJ (2014) Polarization of the endoplasmic reticulum by ER-septin tethering. Cell 158:620–632PubMedCrossRefGoogle Scholar
  23. Cheng KT, Liu X, Ong HL, Ambudkar IS (2008) Functional requirement for Orai1 in store-operated TRPC1-STIM1 channels. J Biol Chem 283:12935–12940PubMedPubMedCentralCrossRefGoogle Scholar
  24. Cheng KT, Liu X, Ong HL, Swaim W, Ambudkar IS (2011) Local Ca2+ entry via Orai1 regulates plasma membrane recruitment of TRPC1 and controls cytosolic Ca2+ signals required for specific cell functions. PLoS Biol 9:e1001025PubMedPubMedCentralCrossRefGoogle Scholar
  25. Cheng KT, Ong HL, Liu X, Ambudkar IS (2013) Contribution and regulation of TRPC channels in store-operated Ca2+ entry. In: Prakriya M (ed) Store-operated calcium channels. Elsevier, Amsterdam, pp 149–179CrossRefGoogle Scholar
  26. Chichili GR, Rodgers W (2009) Cytoskeleton-membrane interactions in membrane raft structure. Cell Mol Life Sci 66:2319–2328PubMedPubMedCentralCrossRefGoogle Scholar
  27. Collins SR, Meyer T (2011) Evolutionary origins of STIM1 and STIM2 within ancient Ca2+ signaling systems. Trends Cell Biol 21:202–211PubMedPubMedCentralCrossRefGoogle Scholar
  28. Cuddapah VA, Turner KL, Sontheimer H (2013) Calcium entry via TRPC1 channels activates chloride currents in human glioma cells. Cell Calcium 53:187–194PubMedCrossRefGoogle Scholar
  29. Dart C (2010) Lipid microdomains and the regulation of ion channel function. J Physiol 588:3169–3178PubMedPubMedCentralCrossRefGoogle Scholar
  30. Derler I, Jardin I, Stathopulos PB, Muik M, Fahrner M, Zayats V, Pandey SK, Poteser M, Lackner B, Absolonova M, Schindl R, Groschner K, Ettrich R, Ikura M, Romanin C (2016) Cholesterol modulates Orai1 channel function. Sci Signal 9:ra10PubMedPubMedCentralCrossRefGoogle Scholar
  31. Desai PN, Zhang X, Wu S, Janoshazi A, Bolimuntha S, Putney JW Jr, Trebak M (2015) Multiple types of calcium channels arising from alternative translation initiation of the Orai1 message. Sci Signal 8:ra74PubMedPubMedCentralCrossRefGoogle Scholar
  32. de Souza LB, Ambudkar IS (2014) Trafficking mechanisms and regulation of TRPC channels. Cell Calcium 56:43–50PubMedCrossRefGoogle Scholar
  33. de Souza LB, Ong HL, Liu X, Ambudkar IS (2015) Fast endocytic recycling determines TRPC1-STIM1 clustering in ER-PM junctions and plasma membrane function of the channel. Biochim Biophys Acta 1853:2709–2721PubMedCrossRefGoogle Scholar
  34. Dietrich A, Gudermann T (2014) TRPC6: physiological function and pathophysiological relevance. Handb Exp Pharmacol 222:157–188PubMedCrossRefGoogle Scholar
  35. Dietrich A, Chubanov V, Kalwa H, Rost BR, Gudermann T (2006) Cation channels of the transient receptor potential superfamily: their role in physiological and pathophysiological processes of smooth muscle cells. Pharmacol Ther 112:744–760PubMedCrossRefGoogle Scholar
  36. Dietrich A, Fahlbusch M, Gudermann T (2014) Classical transient receptor potential 1 (TRPC1): channel or channel regulator? Cell 3:939–962CrossRefGoogle Scholar
  37. Doherty GJ, McMahon HT (2009) Mechanisms of endocytosis. Annu Rev Biochem 78:857–902PubMedCrossRefGoogle Scholar
  38. Du J, Sours-Brothers S, Coleman R, Ding M, Graham S, Kong DH, Ma R (2007) Canonical transient receptor potential 1 channel is involved in contractile function of glomerular mesangial cells. J Am Soc Nephrol 18:1437–1445PubMedCrossRefGoogle Scholar
  39. 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 441:179–185PubMedCrossRefGoogle Scholar
  40. Fiorio Pla A, Maric D, Brazer SC, Giacobini P, Liu X, Chang YH, Ambudkar IS, Barker JL (2005) Canonical transient receptor potential 1 plays a role in basic fibroblast growth factor (bFGF)/FGF receptor-1-induced Ca2+ entry and embryonic rat neural stem cell proliferation. J Neurosci 25:2687–2701PubMedCrossRefGoogle Scholar
  41. Formigli L, Sassoli C, Squecco R, Bini F, Martinesi M, Chellini F, Luciani G, Sbrana F, Zecchi-Orlandini S, Francini F, Meacci E (2009) Regulation of transient receptor potential canonical channel 1 (TRPC1) by sphingosine 1-phosphate in C2C12 myoblasts and its relevance for a role of mechanotransduction in skeletal muscle differentiation. J Cell Sci 122:1322–1333PubMedCrossRefGoogle Scholar
  42. Freichel M, Tsvilovskyy V, Camacho-Londono JE (2014) TRPC4- and TRPC4-containing channels. Handb Exp Pharmacol 222:85–128PubMedCrossRefGoogle Scholar
  43. Galan C, Woodard GE, Dionisio N, Salido GM, Rosado JA (2010) Lipid rafts modulate the activation but not the maintenance of store-operated Ca2+ entry. Biochim Biophys Acta 1803:1083–1093PubMedCrossRefGoogle Scholar
  44. Grant BD, Donaldson JG (2009) Pathways and mechanisms of endocytic recycling. Nat Rev Mol Cell Biol 10:597–608PubMedPubMedCentralCrossRefGoogle Scholar
  45. Gwack Y, Srikanth S, Feske S, Cruz-Guilloty F, Oh-hora M, Neems DS, Hogan PG, Rao A (2007) Biochemical and functional characterization of Orai proteins. J Biol Chem 282:16232–16243PubMedCrossRefGoogle Scholar
  46. Hartzell CA, Jankowska KI, Burkhardt JK, Lewis RS (2016) Calcium influx through CRAC channels controls actin organization and dynamics at the immune synapse. eLife 5. doi: 10.7554/eLife.14850
  47. He K, Qi F, Guo C, Zhan S, Xu H, Liu J, Yang X (2016) Movement deficits and neuronal loss in basal ganglia in TRPC1 deficient mice. Oncotarget 7:69337–69346PubMedPubMedCentralGoogle Scholar
  48. Hogan PG, Lewis RS, Rao A (2010) Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu Rev Immunol 28:491–533PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hong JH, Li Q, Kim MS, Shin DM, Feske S, Birnbaumer L, Cheng KT, Ambudkar IS, Muallem S (2011) Polarized but differential localization and recruitment of STIM1, Orai1 and TRPC channels in secretory cells. Traffic 12:232–245PubMedCrossRefGoogle Scholar
  50. Hoth M, Penner R (1992) Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 355:353–356PubMedCrossRefGoogle Scholar
  51. Hoth M, Penner R (1993) Calcium release-activated calcium current in rat mast cells. J Physiol 465:359–386PubMedPubMedCentralCrossRefGoogle Scholar
  52. Huang GN, Zeng W, Kim JY, Yuan JP, Han L, Muallem S, Worley PF (2006) STIM1 carboxyl-terminus activates native SOC, Icrac and TRPC1 channels. Nat Cell Biol 8:1003–1010PubMedCrossRefGoogle Scholar
  53. Idevall-Hagren O, Lu A, Xie B, De Camilli P (2015) Triggered Ca2+ influx is required for extended synaptotagmin 1-induced ER-plasma membrane tethering. EMBO J 34:2291–2305PubMedPubMedCentralCrossRefGoogle Scholar
  54. Jardin I, Lopez JJ, Salido GM, Rosado JA (2008a) Orai1 mediates the interaction between STIM1 and hTRPC1 and regulates the mode of activation of hTRPC1-forming Ca2+ channels. J Biol Chem 283:25296–25304PubMedCrossRefGoogle Scholar
  55. Jardin I, Salido GM, Rosado JA (2008b) Role of lipid rafts in the interaction between hTRPC1, Orai1 and STIM1. Channels 2:401–403PubMedCrossRefGoogle Scholar
  56. Jha A, Ahuja M, Maleth J, Moreno CM, Yuan JP, Kim MS, Muallem S (2013) The STIM1 CTID domain determines access of SARAF to SOAR to regulate Orai1 channel function. J Cell Biol 202:71–79PubMedPubMedCentralCrossRefGoogle Scholar
  57. Jing J, He L, Sun A, Quintana A, Ding Y, Ma G, Tan P, Liang X, Zheng X, Chen L, Shi X, Zhang SL, Zhong L, Huang Y, Dong MQ, Walker CL, Hogan PG, Wang Y, Zhou Y (2015) Proteomic mapping of ER-PM junctions identifies STIMATE as a regulator of Ca influx. Nat Cell Biol 17:1339–1347PubMedPubMedCentralCrossRefGoogle Scholar
  58. Kannan KB, Barlos D, Hauser CJ (2007) Free cholesterol alters lipid raft structure and function regulating neutrophil Ca2+ entry and respiratory burst: correlations with calcium channel raft trafficking. J Immunol 178:5253–5261PubMedCrossRefGoogle Scholar
  59. Kim MS, Zeng W, Yuan JP, Shin DM, Worley PF, Muallem S (2009) Native store-operated Ca2+ influx requires the channel function of Orai1 and TRPC1. J Biol Chem 284:9733–9741PubMedPubMedCentralCrossRefGoogle Scholar
  60. Kochukov MY, Balasubramanian A, Noel RC, Marrelli SP (2013) Role of TRPC1 and TRPC3 channels in contraction and relaxation of mouse thoracic aorta. J Vasc Res 50:11–20PubMedCrossRefGoogle Scholar
  61. Kwan HY, Shen B, Ma X, Kwok YC, Huang Y, Man YB, Yu S, Yao X (2009) TRPC1 associates with BKCa channel to form a signal complex in vascular smooth muscle cells. Circ Res 104:670–678PubMedCrossRefGoogle Scholar
  62. Kwiatek AM, Minshall RD, Cool DR, Skidgel RA, Malik AB, Tiruppathi C (2006) Caveolin-1 regulates store-operated Ca2+ influx by binding of its scaffolding domain to transient receptor potential channel-1 in endothelial cells. Mol Pharmacol 70:1174–1183PubMedCrossRefGoogle Scholar
  63. Lee KP, Choi S, Hong JH, Ahuja M, Graham S, Ma R, So I, Shin DM, Muallem S, Yuan JP (2014) Molecular determinants mediating gating of transient receptor potential canonical (TRPC) channels by stromal interaction molecule 1 (STIM1). J Biol Chem 289:6372–6382PubMedPubMedCentralCrossRefGoogle Scholar
  64. Leitz J, Kavalali ET (2011) Ca2+ influx slows single synaptic vesicle endocytosis. J Neurosci 31:16318–16326PubMedPubMedCentralCrossRefGoogle Scholar
  65. Lewis RS, Cahalan MD (1989) Mitogen-induced oscillations of cytosolic Ca2+ and transmembrane Ca2+ current in human leukemic T cells. Cell Regul 1:99–112PubMedPubMedCentralGoogle Scholar
  66. Li M, Chen C, Zhou Z, Xu S, Yu Z (2012) A TRPC1-mediated increase in store-operated Ca2+ entry is required for the proliferation of adult hippocampal neural progenitor cells. Cell Calcium 51:486–496PubMedCrossRefGoogle Scholar
  67. Lichtenegger M, Groschner K (2014) TRPC3: a multifunctional signaling molecule. Handb Exp Pharmacol 222:67–84PubMedCrossRefGoogle Scholar
  68. Lin MI, Yu J, Murata T, Sessa WC (2007) Caveolin-1-deficient mice have increased tumor microvascular permeability, angiogenesis, and growth. Cancer Res 67:2849–2856PubMedCrossRefGoogle Scholar
  69. Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327:46–50PubMedCrossRefGoogle Scholar
  70. Liou J, Chang CL (2015) Unveiling physiological functions of extended synaptotagmins. Cell Cycle 14:799–800PubMedPubMedCentralCrossRefGoogle Scholar
  71. 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 15:1235–1241PubMedPubMedCentralCrossRefGoogle Scholar
  72. Liu AP, Fletcher DA (2006) Actin polymerization serves as a membrane domain switch in model lipid bilayers. Biophys J 91:4064–4070PubMedPubMedCentralCrossRefGoogle Scholar
  73. Liu X, Wang W, Singh BB, Lockwich T, Jadlowiec J, O’Connell B, Wellner R, Zhu MX, Ambudkar IS (2000) Trp1, a candidate protein for the store-operated Ca2+ influx mechanism in salivary gland cells. J Biol Chem 275:3403–3411PubMedCrossRefGoogle Scholar
  74. Liu X, Singh BB, Ambudkar IS (2003) TRPC1 is required for functional store-operated Ca2+ channels. Role of acidic amino acid residues in the S5–S6 region. J Biol Chem 278:11337–11343PubMedCrossRefGoogle Scholar
  75. Liu X, Groschner K, Ambudkar IS (2004) Distinct Ca2+-permeable cation currents are activated by internal Ca2+-store depletion in RBL-2H3 cells and human salivary gland cells, HSG and HSY. J Membr Biol 200:93–104PubMedCrossRefGoogle Scholar
  76. Liu X, Bandyopadhyay BC, Singh BB, Groschner K, Ambudkar IS (2005) Molecular analysis of a store-operated and 2-acetyl-sn-glycerol-sensitive non-selective cation channel. Heteromeric assembly of TRPC1-TRPC3. J Biol Chem 280:21600–21606PubMedCrossRefGoogle Scholar
  77. Liu X, Cheng KT, Bandyopadhyay BC, Pani B, Dietrich A, Paria BC, Swaim WD, Beech D, Yildrim E, Singh BB, Birnbaumer L, Ambudkar IS (2007) Attenuation of store-operated Ca2+ current impairs salivary gland fluid secretion in TRPC1−/− mice. Proc Natl Acad Sci U S A 104:17542–17547PubMedPubMedCentralCrossRefGoogle Scholar
  78. 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 275:11934–11942PubMedCrossRefGoogle Scholar
  79. Lopez JJ, Salido GM, Pariente JA, Rosado JA (2006) Interaction of STIM1 with endogenously expressed human canonical TRP1 upon depletion of intracellular Ca2+ stores. J Biol Chem 281:28254–28264PubMedCrossRefGoogle Scholar
  80. Lu M, Branstrom R, Berglund E, Hoog A, Bjorklund P, Westin G, Larsson C, Farnebo LO, Forsberg L (2010) Expression and association of TRPC subtypes with Orai1 and STIM1 in human parathyroid. J Mol Endocrinol 44:285–294PubMedCrossRefGoogle Scholar
  81. Luik RM, MM W, 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 174:815–825PubMedPubMedCentralCrossRefGoogle Scholar
  82. Ma X, Cheng KT, Wong CO, O’Neil RG, Birnbaumer L, Ambudkar IS, Yao X (2011a) Heteromeric TRPV4-C1 channels contribute to store-operated Ca2+ entry in vascular endothelial cells. Cell Calcium 50:502–509PubMedCrossRefGoogle Scholar
  83. Ma X, Nilius B, Wong JW, Huang Y, Yao X (2011b) Electrophysiological properties of heteromeric TRPV4-C1 channels. Biochim Biophys Acta 1808:2789–2797PubMedCrossRefGoogle Scholar
  84. 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 5:5843PubMedPubMedCentralCrossRefGoogle Scholar
  85. Matthews G, Neher E, Penner R (1989) Second messenger-activated calcium influx in rat peritoneal mast cells. J Physiol 418:105–130PubMedPubMedCentralCrossRefGoogle Scholar
  86. Maxfield FR, McGraw TE (2004) Endocytic recycling. Nat Rev Mol Cell Biol 5:121–132PubMedCrossRefGoogle Scholar
  87. McGurk JS, Shim S, Kim JY, Wen Z, Song H, Ming GL (2011) Postsynaptic TRPC1 function contributes to BDNF-induced synaptic potentiation at the developing neuromuscular junction. J Neurosci 31:14754–14762PubMedPubMedCentralCrossRefGoogle Scholar
  88. Mehta D, Ahmmed GU, Paria BC, Holinstat M, Voyno-Yasenetskaya T, Tiruppathi C, Minshall RD, Malik AB (2003) RhoA interaction with inositol 1,4,5-triphosphate receptor and transient receptor potential channel-1 regulates Ca2+ entry. J Biol Chem 278:33492–33500PubMedCrossRefGoogle Scholar
  89. Miller BA (2014) Trpc2. Handb Exp Pharmacol 222:53–65PubMedCrossRefGoogle Scholar
  90. Min SW, Chang WP, Sudhof TC (2007) E-Syts, a family of membranous Ca2+-sensor proteins with multiple C2 domains. Proc Natl Acad Sci U S A 104:3823–3828PubMedPubMedCentralCrossRefGoogle Scholar
  91. Murata T, Lin MI, Huang Y, Yu J, Bauer PM, Giordano FJ, Sessa WC (2007a) Reexpression of caveolin-1 in endothelium rescues the vascular, cardiac, and pulmonary defects in global caveolin-1 knockout mice. J Exp Med 204:2373–2382PubMedPubMedCentralCrossRefGoogle Scholar
  92. Murata T, Lin MI, Stan RV, Bauer PM, Yu J, Sessa WC (2007b) Genetic evidence supporting caveolae microdomain regulation of calcium entry in endothelial cells. J Biol Chem 282:16631–16643PubMedCrossRefGoogle Scholar
  93. Nesin V, Tsiokas L (2014) Trpc1. Handb Exp Pharmacol 222:15–51PubMedCrossRefGoogle Scholar
  94. Ng LC, McCormack MD, Airey JA, Singer CA, Keller PS, Shen XM, Hume JR (2009) TRPC1 and STIM1 mediate capacitative Ca2+ entry in mouse pulmonary arterial smooth muscle cells. J Physiol 587:2429–2442PubMedPubMedCentralCrossRefGoogle Scholar
  95. Niemeyer BA (2016) Changing calcium: CRAC channel (STIM and Orai) expression, splicing, and posttranslational modifiers. Am J Physiol Cell Physiol 310:C701–C709PubMedCrossRefGoogle Scholar
  96. Niggli V (2001) Structural properties of lipid-binding sites in cytoskeletal proteins. Trends Biochem Sci 26:604–611PubMedCrossRefGoogle Scholar
  97. Ong HL, Ambudkar IS (2012) Role of lipid rafts in the regulation of store-operated Ca2+ channels. In: Levitan I, Barrantes F (eds) Cholesterol regulation of ion channels and receptors. Wiley, Hoboken, NJ, pp 69–90CrossRefGoogle Scholar
  98. Ong HL, Ambudkar IS (2015) Molecular determinants of TRPC1 regulation within ER-PM junctions. Cell Calcium 58:376–386PubMedCrossRefGoogle Scholar
  99. Ong HL, Cheng KT, Liu X, Bandyopadhyay BC, Paria BC, Soboloff J, Pani B, Gwack Y, Srikanth S, Singh BB, Gill DL, Ambudkar IS (2007) Dynamic assembly of TRPC1-STIM1-Orai1 ternary complex is involved in store-operated calcium influx. Evidence for similarities in store-operated and calcium release-activated calcium channel components. J Biol Chem 282:9105–9116PubMedPubMedCentralCrossRefGoogle Scholar
  100. Ong HL, Jang SI, Ambudkar IS (2012) Distinct contributions of Orai1 and TRPC1 to agonist-induced [Ca2+]i signals determine specificity of Ca2+-dependent gene expression. PLoS One 7:e47146PubMedPubMedCentralCrossRefGoogle Scholar
  101. Ong EC, Nesin V, Long CL, Bai CX, Guz JL, Ivanov IP, Abramowitz J, Birnbaumer L, Humphrey MB, Tsiokas L (2013) A TRPC1-dependent pathway regulates osteoclast formation and function. J Biol Chem 288:22219–22231PubMedPubMedCentralCrossRefGoogle Scholar
  102. Ong HL, de Souza LB, Cheng KT, Ambudkar IS (2014) Physiological functions and regulation of TRPC channels. Handb Exp Pharmacol 223:1005–1034PubMedCrossRefGoogle Scholar
  103. Ong HL, de Souza LB, Zheng C, Cheng KT, Liu X, Goldsmith CM, Feske S, Ambudkar IS (2015) STIM2 enhances receptor-stimulated Ca2+ signaling by promoting recruitment of STIM1 to the endoplasmic reticulum-plasma membrane junctions. Sci Signal 8:ra3PubMedCrossRefGoogle Scholar
  104. Ong HL, de Souza LB, Ambudkar IS (2016) Role of TRPC channels in store-operated calcium entry. Adv Exp Med Biol 898:87–109PubMedCrossRefGoogle Scholar
  105. Pani B, Singh BB (2009) Lipid rafts/caveolae as microdomains of calcium signaling. Cell Calcium 45:625–633PubMedPubMedCentralCrossRefGoogle Scholar
  106. 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 283:17333–17340PubMedPubMedCentralCrossRefGoogle Scholar
  107. 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 106:20087–20092PubMedPubMedCentralCrossRefGoogle Scholar
  108. 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 126:667–675PubMedPubMedCentralCrossRefGoogle Scholar
  109. Parekh AB (2011) Decoding cytosolic Ca2+ oscillations. Trends Biochem Sci 36:78–87PubMedCrossRefGoogle Scholar
  110. Parekh AB, Putney JW Jr (2005) Store-operated calcium channels. Physiol Rev 85:757–810PubMedCrossRefGoogle Scholar
  111. Parekh AB, Fleig A, Penner R (1997) The store-operated calcium current ICRAC: nonlinear activation by InsP3 and dissociation from calcium release. Cell 89:973–980PubMedCrossRefGoogle Scholar
  112. Paria BC, Vogel SM, Ahmmed GU, Alamgir S, Shroff J, Malik AB, Tiruppathi C (2004) Tumor necrosis factor-a-induced TRPC1 expression amplifies store-operated Ca2+ influx and endothelial permeability. Am J Physiol Lung Cell Mol Physiol 287:L1303–L1313PubMedCrossRefGoogle Scholar
  113. Penner R, Matthews G, Neher E (1988) Regulation of calcium influx by second messengers in rat mast cells. Nature 334:499–504PubMedCrossRefGoogle Scholar
  114. Poteser M, Leitinger G, Pritz E, Platzer D, Frischauf I, Romanin C, Groschner K (2016) Live-cell imaging of ER-PM contact architecture by a novel TIRFM approach reveals extension of junctions in response to store-operated Ca2+-entry. Sci Rep 6:35656PubMedPubMedCentralCrossRefGoogle Scholar
  115. Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A, Hogan PG (2006) Orai1 is an essential pore subunit of the CRAC channel. Nature 443:230–233PubMedCrossRefGoogle Scholar
  116. Prinz WA (2014) Bridging the gap: membrane contact sites in signaling, metabolism, and organelle dynamics. J Cell Biol 205:759–769PubMedPubMedCentralCrossRefGoogle Scholar
  117. Quintana A, Rajanikanth V, Farber-Katz S, Gudlur A, Zhang C, Jing J, Zhou Y, Rao A, Hogan PG (2015) TMEM110 regulates the maintenance and remodeling of mammalian ER-plasma membrane junctions competent for STIM-ORAI signaling. Proc Natl Acad Sci U S A 112:E7083–E7092PubMedPubMedCentralGoogle Scholar
  118. Rao JN, Platoshyn O, Golovina VA, Liu L, Zou T, Marasa BS, Turner DJ, Yuan JX, Wang JY (2006) TRPC1 functions as a store-operated Ca2+ channel in intestinal epithelial cells and regulates early mucosal restitution after wounding. Am J Physiol Gastrointest Liver Physiol 290:G782–G792PubMedCrossRefGoogle Scholar
  119. Rao JN, Rathor N, Zhuang R, Zou T, Liu L, Xiao L, Turner DJ, Wang JY (2012) Polyamines regulate intestinal epithelial restitution through TRPC1-mediated Ca2+ signaling by differentially modulating STIM1 and STIM2. Am J Physiol Cell Physiol 303:C308–C317PubMedPubMedCentralCrossRefGoogle Scholar
  120. 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:e1219CrossRefGoogle Scholar
  121. Redondo PC, Harper AG, Salido GM, Pariente JA, Sage SO, Rosado JA (2004) A role for SNAP-25 but not VAMPs in store-mediated Ca2+ entry in human platelets. J Physiol 558:99–109PubMedPubMedCentralCrossRefGoogle Scholar
  122. Richards DA (2010) Regulation of exocytic mode in hippocampal neurons by intra-bouton calcium concentration. J Physiol 588:4927–4936PubMedPubMedCentralCrossRefGoogle Scholar
  123. 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 169:435–445PubMedPubMedCentralCrossRefGoogle Scholar
  124. Rosado JA, Brownlow SL, Sage SO (2002) Endogenously expressed Trp1 is involved in store-mediated Ca2+ entry by conformational coupling in human platelets. J Biol Chem 277:42157–42163PubMedCrossRefGoogle Scholar
  125. Sabourin J, Cognard C, Constantin B (2009a) Regulation by scaffolding proteins of canonical transient receptor potential channels in striated muscle. J Muscle Res Cell Motil 30:289–297PubMedCrossRefGoogle Scholar
  126. Sabourin J, Lamiche C, Vandebrouck A, Magaud C, Rivet J, Cognard C, Bourmeyster N, Constantin B (2009b) Regulation of TRPC1 and TRPC4 cation channels requires an a1-syntrophin-dependent complex in skeletal mouse myotubes. J Biol Chem 284:36248–36261PubMedPubMedCentralCrossRefGoogle Scholar
  127. Selvaraj S, Watt JA, Singh BB (2009) TRPC1 inhibits apoptotic cell degeneration induced by dopaminergic neurotoxin MPTP/MPP+. Cell Calcium 46:209–218PubMedPubMedCentralCrossRefGoogle Scholar
  128. Selvaraj S, Sun Y, Watt JA, Wang S, Lei S, Birnbaumer L, Singh BB (2012) Neurotoxin-induced ER stress in mouse dopaminergic neurons involves downregulation of TRPC1 and inhibition of AKT/mTOR signaling. J Clin Invest 122:1354–1367PubMedPubMedCentralCrossRefGoogle Scholar
  129. Seth M, Zhang ZS, Mao L, Graham V, Burch J, Stiber J, Tsiokas L, Winn M, Abramowitz J, Rockman HA, Birnbaumer L, Rosenberg P (2009) TRPC1 channels are critical for hypertrophic signaling in the heart. Circ Res 105:1023–1030PubMedPubMedCentralCrossRefGoogle Scholar
  130. Shalygin A, Skopin A, Kalinina V, Zimina O, Glushankova L, Mozhayeva GN, Kaznacheyeva E (2015) STIM1 and STIM2 proteins differently regulate endogenous store-operated channels in HEK293 cells. J Biol Chem 290:4717–4727PubMedCrossRefGoogle Scholar
  131. 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 499:238–242PubMedCrossRefGoogle Scholar
  132. Shi J, Birnbaumer L, Large WA, Albert AP (2014) Myristoylated alanine-rich C kinase substrate coordinates native TRPC1 channel activation by phosphatidylinositol 4,5-bisphosphate and protein kinase C in vascular smooth muscle. FASEB J 28:244–255PubMedPubMedCentralCrossRefGoogle Scholar
  133. Shi J, Miralles F, Birnbaumer L, Large WA, Albert AP (2016) Store depletion induces Galphaq-mediated PLCb1 activity to stimulate TRPC1 channels in vascular smooth muscle cells. FASEB J 30:702–715PubMedCrossRefGoogle Scholar
  134. Shi J, Miralles F, Birnbaumer L, Large WA, Albert AP (2017) Store-operated STIM1 translocation and interaction with TRPC1 at the plasma membrane stimulates PLC activity to induce channel gating in vascular smooth muscle cells. J Physiol 595(4):1039–1058PubMedCrossRefGoogle Scholar
  135. Shim AH, Tirado-Lee L, Prakriya M (2015) Structural and functional mechanisms of CRAC channel regulation. J Mol Biol 427:77–93PubMedCrossRefGoogle Scholar
  136. Sours S, Du J, Chu S, Ding M, Zhou XJ, Ma R (2006) Expression of canonical transient receptor potential (TRPC) proteins in human glomerular mesangial cells. Am J Physiol Renal Physiol 290:F1507–F1515PubMedCrossRefGoogle Scholar
  137. 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 109:8682–8687PubMedPubMedCentralCrossRefGoogle Scholar
  138. Stathopulos PB, Zheng L, Ikura M (2009) Stromal interaction molecule (STIM) 1 and STIM2 calcium sensing regions exhibit distinct unfolding and oligomerization kinetics. J Biol Chem 284:728–732PubMedCrossRefGoogle Scholar
  139. Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10:513–525PubMedCrossRefGoogle Scholar
  140. Stiber JA, Zhang ZS, Burch J, JP E, Zhang S, Truskey GA, Seth M, Yamaguchi N, Meissner G, Shah R, Worley PF, Williams RS, Rosenberg PB (2008) Mice lacking Homer 1 exhibit a skeletal myopathy characterized by abnormal transient receptor potential channel activity. Mol Cell Biol 28:2637–2647PubMedPubMedCentralCrossRefGoogle Scholar
  141. Sun Y, Birnbaumer L, Singh BB (2015) TRPC1 regulates calcium-activated chloride channels in salivary gland cells. J Cell Physiol 230:2848–2856PubMedPubMedCentralCrossRefGoogle Scholar
  142. Sundivakkam PC, Kwiatek AM, Sharma TT, Minshall RD, Malik AB, Tiruppathi C (2009) Caveolin-1 scaffold domain interacts with TRPC1 and IP3R3 to regulate Ca2+ store release-induced Ca2+ entry in endothelial cells. Am J Physiol Cell Physiol 296:C403–C413PubMedCrossRefGoogle Scholar
  143. Taguchi T (2013) Emerging roles of recycling endosomes. J Biochem 153:505–510PubMedCrossRefGoogle Scholar
  144. Takeshima H, Hoshijima M, Song LS (2015) Ca2+ microdomains organized by junctophilins. Cell Calcium 58:349–356PubMedPubMedCentralCrossRefGoogle Scholar
  145. Tiruppathi C, Ahmmed GU, Vogel SM, Malik AB (2006) Ca2+ signaling, TRP channels, and endothelial permeability. Microcirculation 13:693–708PubMedCrossRefGoogle Scholar
  146. Treves S, Franzini-Armstrong C, Moccagatta L, Arnoult C, Grasso C, Schrum A, Ducreux S, Zhu MX, Mikoshiba K, Girard T, Smida-Rezgui S, Ronjat M, Zorzato F (2004) Junctate is a key element in calcium entry induced by activation of InsP3 receptors and/or calcium store depletion. J Cell Biol 166:537–548PubMedPubMedCentralCrossRefGoogle Scholar
  147. Vandebrouck A, Sabourin J, Rivet J, Balghi H, Sebille S, Kitzis A, Raymond G, Cognard C, Bourmeyster N, Constantin B (2007) Regulation of capacitative calcium entries by a1-syntrophin: association of TRPC1 with dystrophin complex and the PDZ domain of a1-syntrophin. FASEB J 20:136–138Google Scholar
  148. 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. Curr Biol 16:2073–2079PubMedCrossRefGoogle Scholar
  149. 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 330:105–109PubMedPubMedCentralCrossRefGoogle Scholar
  150. Weihuang Y, Chang SJ, Harn HI, Huang HT, Lin HH, Shen MR, Tang MJ, Chiu WT (2015) Mechanosensitive store-operated calcium entry regulates the formation of cell polarity. J Cell Physiol 230:2086–2097CrossRefGoogle Scholar
  151. Wes PD, Chevesich J, Jeromin A, Rosenberg C, Stetten S, Montell C (1995) TRPC1, a human homolog of a Drosophila store-operated channel. Proc Natl Acad Sci USA 92:9652–9656PubMedPubMedCentralCrossRefGoogle Scholar
  152. Williams IA, Allen DG (2007) Intracellular calcium handling in ventricular myocytes from mdx mice. Am J Physiol Heart Circ Physiol 292:H846–H855PubMedCrossRefGoogle Scholar
  153. Worley PF, Zeng W, Huang G, Kim JY, Shin DM, Kim MS, Yuan JP, Kiselyov K, Muallem S (2007) Homer proteins in Ca2+ signaling by excitable and non-excitable cells. Cell Calcium 42:363–371PubMedPubMedCentralCrossRefGoogle Scholar
  154. 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 174:803–813PubMedPubMedCentralCrossRefGoogle Scholar
  155. Wu MM, Covington ED, Lewis RS (2014) Single-molecule analysis of diffusion and trapping of STIM1 and Orai1 at endoplasmic reticulum-plasma membrane junctions. Mol Biol Cell 25:3672–3685PubMedPubMedCentralCrossRefGoogle Scholar
  156. Yeh YC, Parekh AB (2015) Distinct structural domains of caveolin-1 independently regulate CRAC channels and Ca2+ microdomain-dependent gene expression. Mol Cell Biol 35:1341–1349PubMedPubMedCentralCrossRefGoogle Scholar
  157. Yin HL, Janmey PA (2003) Phosphoinositide regulation of the actin cytoskeleton. Annu Rev Physiol 65:761–789PubMedCrossRefGoogle Scholar
  158. Yu F, Sun L, Machaca K (2010) Constitutive recycling of the store-operated Ca2+channel Orai1 and its internalization during meiosis. J Cell Biol 191:523–535PubMedPubMedCentralCrossRefGoogle Scholar
  159. Yuan JP, Kiselyov K, Shin DM, Chen J, Shcheynikov N, Kang SH, Dehoff MH, Schwarz MK, Seeburg PH, Muallem S, Worley PF (2003) Homer binds TRPC family channels and is required for gating of TRPC1 by IP3 receptors. Cell 114:777–789PubMedCrossRefGoogle Scholar
  160. 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 9:636–645PubMedPubMedCentralCrossRefGoogle Scholar
  161. Yuan JP, Zeng W, Dorwart MR, Choi YJ, Worley PF, Muallem S (2009) SOAR and the polybasic STIM1 domains gate and regulate Orai channels. Nat Cell Biol 11:337–343PubMedPubMedCentralCrossRefGoogle Scholar
  162. Yuan JP, Lee KP, Hong JH, Muallem S (2012) The closing and opening of TRPC channels by Homer1 and STIM1. Acta Physiol 204:238–247CrossRefGoogle Scholar
  163. Zanou N, Shapovalov G, Louis M, Tajeddine N, Gallo C, Van Schoor M, Anguish I, Cao ML, Schakman O, Dietrich A, Lebacq J, Ruegg U, Roulet E, Birnbaumer L, Gailly P (2010) Role of TRPC1 channel in skeletal muscle function. Am J Physiol Cell Physiol 298:C149–C162PubMedCrossRefGoogle Scholar
  164. Zanou N, Schakman O, Louis P, Ruegg UT, Dietrich A, Birnbaumer L, Gailly P (2012) Trpc1 ion channel modulates phosphatidylinositol 3-kinase/Akt pathway during myoblast differentiation and muscle regeneration. J Biol Chem 287:14524–14534PubMedPubMedCentralCrossRefGoogle Scholar
  165. Zeng W, Yuan JP, Kim MS, Choi YJ, Huang GN, Worley PF, Muallem S (2008) STIM1 gates TRPC channels, but not Orai1, by electrostatic interaction. Mol Cell 32:439–448PubMedPubMedCentralCrossRefGoogle Scholar
  166. Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2:107–117PubMedCrossRefGoogle Scholar
  167. Zhang X, Trebak M (2014) Transient receptor potential canonical 7: a diacylglycerol-activated non-selective cation channel. Handb Exp Pharmacol 222:189–204PubMedPubMedCentralCrossRefGoogle Scholar
  168. 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 437:902–905PubMedPubMedCentralCrossRefGoogle Scholar
  169. Zhang SL, Yeromin AV, Zhang XH, Yu Y, Safrina O, Penna A, Roos J, Stauderman KA, Cahalan MD (2006) Genome-wide RNAi screen of Ca2+ influx identifies genes that regulate Ca2+ release-activated Ca2+ channel activity. Proc Natl Acad Sci U S A 103:9357–9362PubMedPubMedCentralCrossRefGoogle Scholar
  170. Zhang ZY, Pan LJ, Zhang ZM (2010) Functional interactions among STIM1, Orai1 and TRPC1 on the activation of SOCs in HL-7702 cells. Amino Acids 39:195–204PubMedCrossRefGoogle Scholar
  171. Zhang P, Mao AQ, Sun CY, Zhang XD, Pan QX, Yang DT, Jin J, Tang CL, Yang ZY, Yao XQ, Lu XJ, Ma X (2016) Translocation of PKG1a acts on TRPV4-C1 heteromeric channels to inhibit endothelial Ca2+ entry. Acta Pharmacol Sin 37:1199–1207PubMedPubMedCentralCrossRefGoogle Scholar
  172. Zheng L, Stathopulos PB, Li GY, Ikura M (2008) Biophysical characterization of the EF-hand and SAM domain containing Ca2+ sensory region of STIM1 and STIM2. Biochem Biophys Res Commun 369:240–246PubMedCrossRefGoogle Scholar
  173. Zheng L, Stathopulos PB, Schindl R, Li GY, Romanin C, Ikura M (2011) Auto-inhibitory role of the EF-SAM domain of STIM proteins in store-operated calcium entry. Proc Natl Acad Sci U S A 108:1337–1342PubMedPubMedCentralCrossRefGoogle Scholar
  174. Zholos AV (2014) Trpc5. Handb Exp Pharmacol 222:129–156PubMedCrossRefGoogle Scholar
  175. Zhu X, Chu PB, Peyton M, Birnbaumer L (1995) Molecular cloning of a widely expressed human homologue for the Drosophila trp gene. FEBS Lett 373:193–198PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Secretory Physiology Section, Molecular Physiology and Therapeutics Branch, National Institute of Dental and Craniofacial Research – NIDCRNational Institutes of Health – NIHBethesdaUSA

Personalised recommendations