Skip to main content
SpringerLink
Log in

The Contribution of TRPC1 and STIM1 to Capacitative Ca2+ Entry in Pulmonary Artery

  • Conference paper
  • First Online:
Membrane Receptors, Channels and Transporters in Pulmonary Circulation

Part of the book series: Advances in Experimental Medicine and Biology ((volume 661))

Abstract

Capacitative calcium entry (CCE) through store-operated channels (SOCs) has been shown to contribute to the rise in intracellular calcium concentration ([Ca2+]i) and mediate pulmonary artery smooth muscle contraction. CCE is activated as a result of depletion of intracellular Ca2+ stores but there is a great deal of controversy surrounding the underlying signal that active CCE and the molecular makeup of SOCs. The discovery of canonical subgroup of transient receptor potential channels (TRPC) and recent identification of stromal-interacting molecule 1 (STIM1) protein have opened a door to the study of the identity of SOCs and the signal that activates these channels. Among all the TRPC channels, TRPC1 is widely studied in many cell types and shown to be part of SOCs components, whereas STIM1 protein is found to act as a Ca2+ sensor in the intracellular Ca2+ stores and activates SOCs. However, there is very little evidence for the roles of TRPC1 and STIM1 in the contribution of CCE in pulmonary artery. This chapter outlines the roles of TRPC1 and STIM1 in pulmonary artery smooth muscle cells and discusses our recent findings that TRPC1 and STIM1 are functionally interact with each other to mediate CCE in these cells. We also propose a model for the molecular makeup of SOCs formed by TRPC1 and STIM1 in pulmonary artery.

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 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
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

References

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

    Article  CAS  PubMed  Google Scholar 

  2. Parekh AB, Putney JW Jr (2005) Store-operated calcium channels. Physiol Rev 85:757-810

    Article  CAS  PubMed  Google Scholar 

  3. Hoth M, Penner R (1992) Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 355:353-356

    Article  CAS  PubMed  Google Scholar 

  4. Leung FP, Yung LM, Yao X, Laher I, Huang Y (2007) Store-operated calcium entry in vascular smooth muscle. Br J Pharmacol 153:846-857

    Article  PubMed  Google Scholar 

  5. Trepakova ES, Gericke M, Hirakawa Y, Weisbrod RM, CohenRA, Bolotina VM (2001) The properties of a native cation channel activated by Ca2+ store depletion in vascular smooth muscle cells. J Biol Chem 276:7782-7790

    Article  CAS  PubMed  Google Scholar 

  6. Golovina VA, Platoshyn O, Bailey CL et al (2001) Upregulated TRP and enhanced capacitative Ca2+ entry in human pulmonary artery myocytes during proliferation. Am J Physiol Heart Circ Physiol 280:H746-H755

    CAS  PubMed  Google Scholar 

  7. Albert AP, Large WA (2002) A Ca2+-permeable non-selective cation channel activated by depletion of internal Ca2+ stores in single rabbit portal vein myocytes. J Physiol 538:717-728

    Article  CAS  PubMed  Google Scholar 

  8. Saleh SN, Albert AP, Peppiatt CM, Large WA (2006) Angiotensin II activates two cation conductances with distinct TRPC1 and TRPC6 channel properties in rabbit mesenteric artery myocytes. J Physiol 577:479-495

    Article  CAS  PubMed  Google Scholar 

  9. Saleh SN, Albert AP, Peppiatt-Wildman CM, Large WA (2008) Diverse properties of store-operated TRPC channels activated by protein kinase C in vascular myocytes. J Physiol 586:2463-2476

    Article  CAS  PubMed  Google Scholar 

  10. Ng LC, Gurney AM (2001) Store-operated channels mediate Ca2+ influx and contraction in rat pulmonary artery. Circ Res 89:923-929

    Article  CAS  PubMed  Google Scholar 

  11. Li J, Sukumar P, Milligan CJ et al (2008) Interactions, functions, and independence of plasma membrane STIM1 and TRPC1 in vascular smooth muscle cells. Circ Res 103:e97-e104

    Article  CAS  PubMed  Google Scholar 

  12. Wilson SM, Mason HS, Smith GD et al (2002) Comparative capacitative calcium entry mechanisms in canine pulmonary and renal arterial smooth muscle cells. J Physiol 543:917-931

    Article  CAS  PubMed  Google Scholar 

  13. Weirich J, Dumont L, Fleckenstein-Grun G (2005) Contribution of capacitative and non-capacitative Ca2+-entry to M3-receptor-mediated contraction of porcine coronary smooth muscle. Cell Calcium 38:457-467

    Article  CAS  PubMed  Google Scholar 

  14. McElroy SP, Gurney AM, Drummond RM (2008) Pharmacological profile of store-operated Ca2+ entry in intrapulmonary artery smooth muscle cells. Eur J Pharmacol 584:10-20

    Article  CAS  PubMed  Google Scholar 

  15. Ng LC, Kyle BD, Lennox AR, Shen XM, Hatton WJ, Hume JR (2008) Cell culture alters Ca2+ entry pathways activated by store-depletion or hypoxia in canine pulmonary arterial smooth muscle cells. Am J Physiol Cell Physiol 294:C313-C323

    Article  CAS  PubMed  Google Scholar 

  16. Pedersen SF, Owsianik G, Nilius B (2005) TRP channels: an overview. Cell Calcium 38:233-252

    Article  CAS  PubMed  Google Scholar 

  17. Albert AP, Saleh SN, Peppiatt-Wildman CM, Large WA (2007) Multiple activation mechanisms of store-operated TRPC channels in smooth muscle cells. J Physiol 583:25-36

    Article  CAS  PubMed  Google Scholar 

  18. Xu SZ, Beech DJ (2001) TrpC1 is a membrane-spanning subunit of store-operated Ca2+ channels in native vascular smooth muscle cells. Circ Res 88:84-87

    Article  CAS  PubMed  Google Scholar 

  19. Brueggemann LI, Markun DR, Henderson KK, Cribbs LL, Byron KL (2006) Pharmacological and electrophysiological characterization of store-operated currents and capacitative Ca2+ entry in vascular smooth muscle cells. J Pharmacol Exp Ther 317:488-499

    Article  CAS  PubMed  Google Scholar 

  20. Bergdahl A, Gomez MF, Wihlborg AK et al (2005) Plasticity of TRPC expression in arterial smooth muscle: correlation with store-operated Ca2+ entry. Am J Physiol Cell Physiol 288:C872-C880

    Article  CAS  PubMed  Google Scholar 

  21. Takahashi Y, Watanabe H, Murakami M et al (2007) Involvement of transient receptor potential canonical 1 (TRPC1) in angiotensin II-induced vascular smooth muscle cell hypertrophy. Atherosclerosis 195:287-926

    Article  CAS  PubMed  Google Scholar 

  22. Xu SZ, Boulay G, Flemming R, Beech DJ (2006) E3-targeted anti-TRPC5 antibody inhibits store-operated calcium entry in freshly isolated pial arterioles. Am J Physiol Heart Circ Physiol 291:H2653-H2669

    Article  CAS  PubMed  Google Scholar 

  23. Goel M, Sinkins WG, Schilling WP (2002) Selective association of TRPC channel subunits in rat brain synaptosomes. J Biol Chem 277:48303-48310

    Article  CAS  PubMed  Google Scholar 

  24. Hofmann T, Schaefer M, Schultz G, Gudermann T (2002) Subunit composition of mammalian transient receptor potential channels in living cells. Proc Natl Acad Sci U S A 99:7461-7466

    Article  CAS  PubMed  Google Scholar 

  25. Strübing C, Krapivinsky G, Krapivinsky L, Clapham DE (2003) Formation of novel TRPC channels by complex subunit interactions in embryonic brain. J Biol Chem 278:39014-39019

    Article  PubMed  Google Scholar 

  26. 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 280:21600-21606

    Article  CAS  PubMed  Google Scholar 

  27. Poteser M, Graziani A, Rosker C et al (2006) TRPC3 and TRPC4 associate to form redox-sensitive cation channel. Evidence for expression of native TRPC3-TRPC4 heterotetrameric channels in endothelial cells. J Biol Chem 281:13588-13595

    Article  CAS  PubMed  Google Scholar 

  28. Roos J, DiGregorio PJ, Yeromin AV et al (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 169:435-445

    Article  CAS  PubMed  Google Scholar 

  29. Zhang SL, Yu Y, Roos J et al (2005) STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437:902-905

    Article  CAS  PubMed  Google Scholar 

  30. Spassova MA, Soboloff J, He LP, Xu W, Dziadek MA, Gill DL (2006) STIM1 has a plasma membrane role in the activation of store-operated Ca2+ channels. Proc Natl Acad Sci U S A 103:4040-4045

    Article  CAS  PubMed  Google Scholar 

  31. Takahashi Y, Watanabe H, Murakami M et al (2007) Functional role of stromal interaction molecule 1 (STIM1) in vascular smooth muscle cells. Biochem Biophys Res Commun 361:934-940

    Article  CAS  PubMed  Google Scholar 

  32. Dietrich A, Kalwa H, Storch U et al (2007) Pressure-induced and store-operated cation influx in vascular smooth muscle cells is independent of TRPC1. Pflügers Arch 455:465-477

    Article  CAS  PubMed  Google Scholar 

  33. Peel SE, Liu B, Hall IP (2006) A key role for STIM1 in store operated calcium channel activation in airway smooth muscle. Respir Res 7:119-126

    Article  PubMed  Google Scholar 

  34. 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 9:636-645

    Article  CAS  PubMed  Google Scholar 

  35. Walker RL, Hume JR, Horowitz B (2001) Differential expression and alternative splicing of TRP channel genes in smooth muscles. Am J Physiol Cell Physiol 280:C1184-C1192

    CAS  PubMed  Google Scholar 

  36. Wang J, Shimoda LA, Sylvester JT (2003) Capacitative calcium entry and TRPC channel proteins are expressed in rat distal pulmonary arterial smooth muscle. Am J Physiol Lung Cell Mol Physiol 286:L848-L858

    Article  PubMed  Google Scholar 

  37. Lu W, Wang J, Shimoda LA, Sylvester JT (2008) Differences in STIM1 and TRPC expression in proximal and distal pulmonary arterial smooth muscle are associated with differences in Ca2+ responses to hypoxia. Am J Physiol Lung Cell Mol Physiol 295:L104-L113

    Article  CAS  PubMed  Google Scholar 

  38. Golovina VA (1999) Cell proliferation is associated with enhanced capacitative Ca2+ entry in human arterial myocytes. Am J Physiol Cell Physiol 277:C343-C349

    CAS  Google Scholar 

  39. Sweeney M, Yu Y, Platoshyn O, Zhang S, McDaniel SS, Yuan JX-J (2002) Inhibition of endogenous TRP1 decreases capacitative Ca2+ entry and attenuates pulmonary artery smooth muscle cell proliferation. Am J Physiol Lung Cell Mol Physiol 283:L144-L155

    CAS  PubMed  Google Scholar 

  40. Kunichika N, Yu Y, Remillard CV, Platoshyn O, Zhang S, Yuan JX-J (2004) Overexpression of TRPCs enhances pulmonary vasoconstriction induced by capacitative Ca2+ entry. Am J Physiol Lung Cell Mol Physiol 287:L962-L969

    Article  CAS  PubMed  Google Scholar 

  41. Lin MJ, Leung GP, Zhang WM et al (2004) Chronic hypoxia-induced upregulation of store-operated and receptor-operated Ca2+ channels in pulmonary arterial smooth muscle cells: a novel mechanism of hypoxic pulmonary hypertension. Circ Res 95:496-505

    Article  CAS  PubMed  Google Scholar 

  42. Ng LC, McCormack MD, Airey JA et al (2009) TRPC1 and STIM1 mediate capacitative calcium entry in mouse pulmonary artery smooth muscle cells. J Physiol 587:2429-2442

    Article  CAS  PubMed  Google Scholar 

  43. Feske S, Gwack Y, Prakriya M et al (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441:179-185

    Article  CAS  PubMed  Google Scholar 

  44. Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A, Hogan PG (2006) Orai1 is an essential pore subunit of the CRAC channel. Nature 443:230-233

    Article  CAS  PubMed  Google Scholar 

  45. Soboloff J, Spassova MA, Tang XD, Hewavitharana T, Xu W, Gill DL (2006) Orai1 and STIM reconstitute store-operated calcium channel function. J Biol Chem 281:20661-20665

    Article  CAS  PubMed  Google Scholar 

  46. Mercer JC, Dehaven WI, Smyth JT et al (2006) Large store-operated calcium selective currents due to co-expression of Orai1 or Orai2 with the intracellular calcium sensor. Stim1. J Biol Chem 281:24979-24990

    Article  CAS  Google Scholar 

  47. Liao Y, Erxleben C, Yildirim E, Abramowitz J, Armstrong DL, Birnbaumer L (2007) Orai proteins interact with TRPC channels and confer responsiveness to store depletion. Proc Natl Acad Sci U S A 104:4682-4687

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  49. Robertson TP, Hague D, Aaronson PI, Ward JP (2000) Voltage-independent calcium entry in hypoxic pulmonary vasoconstriction of intrapulmonary arteries of the rat. J Physiol 525:669-680

    Article  CAS  PubMed  Google Scholar 

  50. Weigand L, Foxson J, Wang J, Shimoda LA, Sylvester JT (2005) Inhibition of hypoxic pulmonary vasoconstriction by antagonists of store-operated Ca2+ and nonselective cation channels. Am J Physiol Lung Cell Mol Physiol 289:L5-L13

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Our work was supported by National Institutes of Health grants HL 49254 (Joseph R. Hume), P20RR15581 from the National Center for Research Resources (Joseph R. Hume), and an American Heart Association Scientist Development Grant (Lih Chyuan Ng).

Author information

Authors and Affiliations

  1. Department of Pharmacology/318, University of Nevada School of Medicine, 1664 North Virginia Street, Reno, NV, 89557, USA

    Lih Chyuan Ng, Judith A. Airey & Joseph R. Hume

Authors
  1. Lih Chyuan Ng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Judith A. Airey
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joseph R. Hume
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lih Chyuan Ng .

Editor information

Editors and Affiliations

  1. Departments of Medicine and Pharmacology, University of Illinois at Chicago, Chicago, 60612, USA

    Jason X. -J. Yuan

  2. Guy’s Hospital Campus, Dept. Physiology, King’s College London, London, SE1 1UL, United Kingdom

    Jeremy P. T. Ward

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Humana Press, a part of Springer Science+Business Media, LLC

About this paper

Cite this paper

Ng, L.C., Airey, J.A., Hume, J.R. (2010). The Contribution of TRPC1 and STIM1 to Capacitative Ca2+ Entry in Pulmonary Artery. In: Yuan, JJ., Ward, J. (eds) Membrane Receptors, Channels and Transporters in Pulmonary Circulation. Advances in Experimental Medicine and Biology, vol 661. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-60761-500-2_8

Download citation

Publish with us

Policies and ethics

Search

Navigation