Skip to main content

TRP channels as sensors of oxygen availability

Abstract

An ability to adapt to changes in oxygen availability is essential for survival in both prokaryotic and eukaryotic organisms. Recently, cation channels encoded by the transient receptor potential (trp) gene superfamily have been recognized as multimodal sensors of a wide variety of factors inside the cells and in the extracellular environment and also as transducers of electrical and chemical signals mediated by ions such as Ca2+. The functional features of TRP channels enable the body to react and adapt to different forms of environmental changes, including oxygen levels. A subclass of TRP channels regulates various cellular processes in response to fluctuations in oxygen. In this article, we describe the physiological and pathological significance of the oxygen-sensitive TRP channels, which are heterogeneous in the cellular responses to acute changes in oxygen, by contrasting their oxygen monitoring function with that of other ion channels, transporters, and enzymes. We also discuss the physiological relevance of oxygen-sensitive TRP channels as a novel class of target proteins for pharmaceutical therapeutics.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Aarts M, Iihara K, Wei WL, Xiong ZG, Arundine M, Cerwinski W, MacDonald JF, Tymianski M (2003) A key role for TRPM7 channels in anoxic neuronal death. Cell 115:863–877

    PubMed  CAS  Article  Google Scholar 

  2. Acker T, Acker H (2004) Cellular oxygen sensing need in CNS function: physiological and pathological implications. J Exp Biol 207:3171–3188

    PubMed  CAS  Article  Google Scholar 

  3. Amador FJ, Liu S, Ishiyama N, Plevin MJ, Wilson A, MacLennan DH, Ikura M (2009) Crystal structure of type I ryanodine receptor amino-terminal beta-trefoil domain reveals a disease-associated mutation “hot spot” loop. Proc Natl Acad Sci U S A 106:11040–11044

    PubMed  CAS  Article  Google Scholar 

  4. Aracena-Parks P, Goonasekera SA, Gilman CP, Dirksen RT, Hidalgo C, Hamilton SL (2006) Identification of cysteines involved in S-nitrosylation, S-glutathionylation, and oxidation to disulfides in ryanodine receptor type 1. J Biol Chem 281:40354–40368

    PubMed  CAS  Article  Google Scholar 

  5. Arpan G (2004) Head injury research: what have we learnt. Indian J Crit Care Med 8:111–115

    Google Scholar 

  6. Babior BM (2004) NADPH oxidase. Curr Opin Immunol 16:42–47

    PubMed  CAS  Article  Google Scholar 

  7. Bautista DM, Movahed P, Hinman A, Axelsson HE, Sterner O, Högestätt ED, Julius D, Jordt SE, Zygmunt PM (2005) Pungent products from garlic activate the sensory ion channel TRPA1. Proc Natl Acad Sci U S A 102:12248–12252

    PubMed  CAS  Article  Google Scholar 

  8. Behrooz A, Ismail-Beigi F (1999) Stimulation of glucose transport by hypoxia: signals and mechanisms. Physiology 14:105–110

    CAS  Google Scholar 

  9. Berenbrink M, Völkel S, Heisler N, Nikinmaa M (2000) O2-dependent K+ fluxes in trout red blood cells: the nature of O2 sensing revealed by the O2 affinity, cooperativity and pH dependence of transport. J Physiol 526:69–80

    PubMed  CAS  Article  Google Scholar 

  10. Bessac BF, Jordt SE (2008) Breathtaking TRP channels: TRPA1 and TRPV1 in airway chemosensation and reflex control. Physiology (Bethesda) 23:360–370

    CAS  Article  Google Scholar 

  11. Bessac BF, Sivula M, von Hehn CA, Escalera J, Cohn L, Jordt SE (2008) TRPA1 is a major oxidant sensor in murine airway sensory neurons. J Clin Invest 118:1899–1910

    PubMed  CAS  Article  Google Scholar 

  12. Birmingham K (2002) Future of neuroprotective drugs in doubt. Nat Med 8:5

    PubMed  CAS  Article  Google Scholar 

  13. Buckler KJ (1997) A novel oxygen-sensitive potassium current in rat carotid body type I cells. J Physiol 498:649–662

    PubMed  CAS  Google Scholar 

  14. Butenko O, Dzamba D, Benesova J, Honsa P, Benfenati V, Rusnakova V, Ferroni S, Anderova M (2012) The increased activity of TRPV4 channel in the astrocytes of the adult rat hippocampus after cerebral hypoxia/ischemia. PLoS One 7:e39959

    PubMed  CAS  Article  Google Scholar 

  15. Carter AJ (1998) The importance of voltage-dependent sodium channels in cerebral ischaemia. Amino Acids 14:159–169

    PubMed  CAS  Article  Google Scholar 

  16. Conforti L, Millhorn DE (1997) Selective inhibition of a slow-inactivating voltage-dependent K+ channel in rat PC12 cells by hypoxia. J Physiol 502:293–305

    PubMed  CAS  Article  Google Scholar 

  17. Cummins TR, Jiang C, Haddad GG (1993) Human neocortical excitability is decreased during anoxia via sodium channel modulation. J Clin Invest 91:608–615

    PubMed  CAS  Article  Google Scholar 

  18. Cvetkov TL, Huynh KW, Cohen MR, Moiseenkova-Bell VY (2011) Molecular architecture and subunit organization of TRPA1 ion channel revealed by electron microscopy. J Biol Chem 286:38168–38176

    PubMed  CAS  Article  Google Scholar 

  19. De Sanctis GT, Green FH, Remmers JE (1991) Ventilatory responses to hypoxia and hypercapnia in awake rats pretreated with capsaicin. J Appl Physiol 70:1168–1174

    PubMed  Article  Google Scholar 

  20. Delpiano MA, Hescheler J (1989) Evidence for a pO2-sensitive K+ channel in the type-I cell of the rabbit carotid body. FEBS Lett 249:195–198

    PubMed  CAS  Article  Google Scholar 

  21. Duncan LM, Deeds J, Hunter J, Shao J, Holmgren LM, Woolf EA, Tepper RI, Shyjan AW (1998) Down-regulation of the novel gene melastatin correlates with potential for melanoma metastasis. Cancer Res 58:1515–1520

    PubMed  CAS  Google Scholar 

  22. Enyedi P, Czirják G (2010) Molecular background of leak K+ currents: two-pore domain potassium channels. Physiol Rev 90:559–605

    PubMed  CAS  Article  Google Scholar 

  23. Eu JP, Sun J, Xu L, Stamler JS, Meissner G (2000) The skeletal muscle calcium release channel: coupled O2 sensor and NO signaling functions. Cell 102:499–509

    PubMed  CAS  Article  Google Scholar 

  24. Fearon IM, Palmer AC, Balmforth AJ, Ball SG, Mikala G, Schwartz A, Peers C (1997) Hypoxia inhibits the recombinant alpha 1C subunit of the human cardiac L-type Ca2+ channel. J Physiol 500:551–556

    PubMed  CAS  Google Scholar 

  25. Franco-Obregón A, López-Barneo J (1996) Differential oxygen sensitivity of calcium channels in rabbit smooth muscle cells of conduit and resistance pulmonary arteries. J Physiol 491:511–518

    PubMed  Google Scholar 

  26. Franco-Obregon A, Lopez-Barneo J (1996) Low pO2 inhibits calcium channel activity in arterial smooth muscle cells. Am J Physiol Heart Circ Physiol 271:H2290–H2299

    CAS  Google Scholar 

  27. Ganfornina MD, López-Barneo J (1991) Single K+ channels in membrane patches of arterial chemoreceptor cells are modulated by O2 tension. Proc Natl Acad Sci U S A 88:2927–2930

    PubMed  CAS  Article  Google Scholar 

  28. Gaudet R (2008) A primer on ankyrin repeat function in TRP channels and beyond. Mol Biosyst 4:372–379

    PubMed  CAS  Article  Google Scholar 

  29. Gees M, Colsoul B, Nilius B (2010) The role of transient receptor potential cation channels in Ca2+ signaling. Cold Spring Harb Perspect Biol 2:a003962

    PubMed  CAS  Article  Google Scholar 

  30. Giaccia AJ, Simon MC, Johnson R (2004) The biology of hypoxia: the role of oxygen sensing in development, normal function, and disease. Genes Dev 18:2183–2194

    PubMed  CAS  Article  Google Scholar 

  31. Gibson JS, Cossins AR, Ellory JC (2000) Oxygen-sensitive membrane transporters in vertebrate red cells. J Exp Biol 203:1395–1407

    PubMed  CAS  Google Scholar 

  32. Gonzalez C, Almaraz L, Obeso A, Rigual R (1994) Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiol Rev 74:829–898

    PubMed  CAS  Google Scholar 

  33. Gray JM, Karow DS, Lu H, Chang AJ, Chang JS, Ellis RE, Marletta MA, Bargmann CI (2004) Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 430:317–322

    PubMed  CAS  Article  Google Scholar 

  34. Gruss M, Ettorre G, Stehr AJ, Henrich M, Hempelmann G, Scholz A (2006) Moderate hypoxia influences excitability and blocks dendrotoxin sensitive K+ currents in rat primary sensory neurones. Mol Pain 2:12

    PubMed  Article  CAS  Google Scholar 

  35. Haase VH (2012) Renal cancer: oxygen meets metabolism. Exp Cell Res 318:1057–1067

    PubMed  CAS  Article  Google Scholar 

  36. Hamilton SL, Serysheva II (2009) Ryanodine receptor structure: progress and challenges. J Biol Chem 284:4047–4051

    PubMed  CAS  Article  Google Scholar 

  37. Hammarström AKM, Gage PW (1998) Inhibition of oxidative metabolism increases persistent sodium current in rat CA1 hippocampal neurons. J Physiol 510:735–741

    PubMed  Article  Google Scholar 

  38. Hampl V, Bibova J, Straňák Z, Wu X, Michelakis ED, Hashimoto K, Archer SL (2002) Hypoxic fetoplacental vasoconstriction in humans is mediated by potassium channel inhibition. Am J Physiol Heart Circ Physiol 283:H2440–H2449

    PubMed  CAS  Google Scholar 

  39. Hara Y, Wakamori M, Ishii M, Maeno E, Nishida M, Yoshida T, Yamada H, Shimizu S, Mori E, Kudoh J, Shimizu N, Kurose H, Okada Y, Imoto K, Mori Y (2002) LTRPC2 Ca2+-permeable channel activated by changes in redox status confers susceptibility to cell death. Molecular Cell 9:163–173

    PubMed  CAS  Article  Google Scholar 

  40. Hawkins BJ, Irrinki KM, Mallilankaraman K, Lien YC, Wang Y, Bhanumathy CD, Subbiah R, Ritchie MF, Soboloff J, Baba Y, Kurosaki T, Joseph SK, Gill DL, Madesh M (2010) S-glutathionylation activates STIM1 and alters mitochondrial homeostasis. J Cell Biol 190:391–405

    PubMed  CAS  Article  Google Scholar 

  41. Hetz SK, Bradley TJ (2005) Insects breathe discontinuously to avoid oxygen toxicity. Nature 433:516–519

    PubMed  CAS  Article  Google Scholar 

  42. Howe A, Pack RJ, Wise JC (1981) Arterial chemoreceptor-like activity in the abdominal vagus of the rat. J Physiol 320:309–318

    PubMed  CAS  Google Scholar 

  43. Ikonomidou C, Turski L (2002) Why did NMDA receptor antagonists fail clinical trials for stroke and traumatic brain injury. Lancet Neurol 1:383–386

    PubMed  CAS  Article  Google Scholar 

  44. Ismail S, Sturrock A, Wu P, Cahill B, Norman K, Huecksteadt T, Sanders K, Kennedy T, Hoidal J (2009) NOX4 mediates hypoxia-induced proliferation of human pulmonary artery smooth muscle cells: the role of autocrine production of transforming growth factor-β1 and insulin-like growth factor binding protein-3. Am J Physiol Lung Cell Mol Physiol 296:L489–L499

    PubMed  CAS  Article  Google Scholar 

  45. Ito S, Ohta T, Nakazato Y (1999) Characteristics of 5-HT-containing chemoreceptor cells of the chicken aortic body. J Physiol 515:49–59

    PubMed  CAS  Article  Google Scholar 

  46. Jia J, Verma S, Nakayama S, Quillinan N, Grafe MR, Hurn PD, Herson PS (2011) Sex differences in neuroprotection provided by inhibition of TRPM2 channels following experimental stroke. J Cereb Blood Flow Metab 31:2160–2168

    PubMed  CAS  Article  Google Scholar 

  47. Jordt SE, Bautista DM, Chuang H, McKemy DD, Zygmunt PM, Höqestätt ED, Meng ID, Julius D (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427:260–265

    PubMed  CAS  Article  Google Scholar 

  48. Kaloyianni M, Rasidaki A (1996) Adrenergic responses of R. ridibunda red cells. J Exp Zool 276:175–185

    PubMed  CAS  Article  Google Scholar 

  49. Kaneko S, Kawakami S, Hara Y, Wakamori M, Itoh E, Minami T, Takada Y, Kume T, Katsuki H, Mori Y, Akaike A (2006) A critical role of TRPM2 in neuronal cell death by hydrogen peroxide. J Pharmacol Sci 101:66–76

    PubMed  CAS  Article  Google Scholar 

  50. Kubin L, Alheid GF, Zuperku EJ, McCrimmon DR (2006) Central pathways of pulmonary and lower airway vagal afferents. J Appl Physiol 101:618–627

    PubMed  Article  Google Scholar 

  51. Lahiri S (2000) Historical perspectives of cellular oxygen sensing and responses to hypoxia. J Appl Physiol 88:1467–1473

    PubMed  CAS  Google Scholar 

  52. Lahiri S, Roy A, Baby SM, Hoshi T, Semenza GL, Prabhakar NR (2006) Oxygen sensing in the body. Prog Biophys Mol Biol 91:249–286

    PubMed  CAS  Article  Google Scholar 

  53. Lange CAK, Bainbridge JWB (2012) Oxygen sensing in retinal health and disease. Ophthalmologica 227:115–131

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  55. Latorre R, Brauchi S, Orta G, Zaelzer C, Vargas G (2007) Thermo TRP channels as modular proteins with allosteric gating. Cell Calcium 42:427–438

    PubMed  CAS  Article  Google Scholar 

  56. Lee YM, Kim BJ, Chun YS, So I, Choi H, Kim MS, Park JW (2006) NOX4 as an oxygen sensor to regulate TASK-1 activity. Cell Signal 18:499–507

    PubMed  CAS  Article  Google Scholar 

  57. Liu Z, Wang R, Zhang J, Chen SRW, Wagenknecht T (2005) Localization of a disease-associated mutation site in the three-dimensional structure of the cardiac muscle ryanodine receptor. J Biol Chem 280:37941–37947

    PubMed  CAS  Article  Google Scholar 

  58. Lobo PA, Van Petegem F (2009) Crystal structures of the N-terminal domains of cardiac and skeletal muscle ryanodine receptors: insights into disease mutations. Structure 17:1505–1514

    PubMed  CAS  Article  Google Scholar 

  59. Longhurst JC, Tjen-A-Looi SC, Fu LW (2001) Cardiac sympathetic afferent activation provoked by myocardial ischemia and reperfusion. Mechanisms and reflexes. Ann N Y Acad Sci 940:74–95

    PubMed  CAS  Article  Google Scholar 

  60. López-Barneo J, Pardal R, Ortega-Sáenz P (2001) Cellular mechanism of oxygen sensing. Annu Rev Physiol 63:259–287

    PubMed  Article  Google Scholar 

  61. 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

    PubMed  CAS  Article  Google Scholar 

  62. Macpherson LJ, Geierstanger BH, Viswanath V, Bandell M, Eid SR, Hwang S, Patapoutian A (2005) The pungency of garlic: activation of TRPA1 and TRPV1 in response to allicin. Curr Biol 15:929–934

    PubMed  CAS  Article  Google Scholar 

  63. McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52–58

    PubMed  CAS  Article  Google Scholar 

  64. McNulty S, Fonfria E (2005) The role of TRPM channels in cell death. Pflugers Arch 451:235–242

    PubMed  CAS  Article  Google Scholar 

  65. Meller ST, Gebhart GF (1992) A critical review of the afferent pathways and the potential chemical mediators involved in cardiac pain. Neuroscience 48:501–524

    PubMed  CAS  Article  Google Scholar 

  66. Motais R, Garcia-Romeu F, Borgese F (1987) The control of Na+/H+ exchange by molecular oxygen in trout erythrocytes. A possible role of hemoglobin as a transducer. J Gen Physiol 90:197–207

    PubMed  CAS  Article  Google Scholar 

  67. Morris GF, Bullock R, Marshall SB, Marmarou A, Maas A, Marshall LF (1999) Failure of the competitive N-methyl-d-aspartate antagonist Selfotel (CGS 19755) in the treatment of severe head injury: results of two phase III clinical trials. The Selfotel Investigators. J Neurosurg 91:737–743

    PubMed  CAS  Article  Google Scholar 

  68. Murphy PJ (2005) The fetal circulation. Contin Educ Anaesth Crit Care Pain 5:107–112

    Article  Google Scholar 

  69. Muzyamba MC, Cossins AR, Gibson JS (1999) Regulation of Na+–K+–2Cl cotransport in turkey red cells: the role of oxygen tension and protein phosphorylation. J Physiol 517:421–429

    PubMed  CAS  Article  Google Scholar 

  70. Nadler MJS, Hermosura MC, Inabe K, Perraud AL, Zhu Q, Stokes AJ, Kurosaki T, Kinet JP, Penner R, Scharenberg AM, Fleig A (2001) LTRPC7 is a Mg2+ ATP-regulated divalent cation channel required for cell viability. Nature 411:590–595

    PubMed  CAS  Article  Google Scholar 

  71. Naeije R, Brimioulle S (2001) Physiology in medicine: importance of hypoxic pulmonary vasoconstriction in maintaining arterial oxygenation during acute respiratory failure. Crit Care 5:67–71

    PubMed  CAS  Article  Google Scholar 

  72. Nassenstein C, Kwong K, Taylor-Clark T, Kollarik M, Macglashan DM, Braun A, Undem BJ (2008) Expression and function of the ion channel TRPA1 in vagal afferent nerves innervating mouse lungs. J Physiol 586:1595–1604

    PubMed  CAS  Article  Google Scholar 

  73. Neubauer JA, Sunderram J (2004) Oxygen-sensing neurons in the central nervous system. J Appl Physiol 96:367–374

    PubMed  CAS  Article  Google Scholar 

  74. Ng LC, O’Neill KG, French D, Airey JA, Singer CA, Tian H, Shen XM, Hume JR (2012) TRPC1 and Orai1 interact with STIM1 and mediate capacitative Ca2+ entry caused by acute hypoxia in mouse pulmonary arterial smooth muscle cells. Am J Physiol Cell Physiol 303:C1156–C1172

    PubMed  CAS  Article  Google Scholar 

  75. Nilius B, Appendino G, Owsianik G (2012) The transient receptor potential channel TRPA1: from gene to pathophysiology. Pflugers Arch Eur J Physiol 464:425–458

    CAS  Article  Google Scholar 

  76. Nilius B, Owsianik G, Voets T, Peters JA (2007) Transient receptor potential cation channels in disease. Physiol Rev 87:165–217

    PubMed  CAS  Article  Google Scholar 

  77. Nishida M, Hara Y, Yoshida T, Inoue R, Mori Y (2006) TRP channels: molecular diversity and physiological function. Microcirculation 13:535–550

    PubMed  CAS  Article  Google Scholar 

  78. Numata T, Kiyonaka S, Kato K, Takahashi N, Mori Y (2011) Activation of TRP channels in mammalian systems. In: Zhu MX (ed) TRP channels. CRC, Boca Raton

    Google Scholar 

  79. Olah ME, Jackson MF, Li H, Perez Y, Sun HS, Kiyonaka S, Mori Y, Tymianski M, MacDonald JF (2009) Ca2+-dependent induction of TRPM2 currents in hippocampal neurons. J Physiol 587:965–979

    PubMed  CAS  Article  Google Scholar 

  80. O’Kelly I, Stephens RH, Peers C, Kemp PJ (1999) Potential identification of the O2-sensitive K+ current in a human neuroepithelial body-derived cell line. Am J Physiol Lung Cell Mol Physiol 276:L96–L104

    Google Scholar 

  81. Pan HL, Chen SR (2004) Sensing tissue ischemia: another new function for capsaicin receptors. Circulation 110:1826–1831

    PubMed  Article  Google Scholar 

  82. Pani B, Bollimuntha S, Singh BB (2012) The TR (i)P to Ca2+ signaling just got STIMy: an update on STIM1 activated TRPC channels. Front Biosci 17:805–823

    CAS  Article  Google Scholar 

  83. Peers C (1990) Hypoxic suppression of K+ currents in type I carotid body cells: selective effect on the Ca2(+)-activated K+ current. Neurosci Lett 119:253–256

    PubMed  CAS  Article  Google Scholar 

  84. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, Bevan S, Patapoutian A (2002) A TRP channel that senses cold stimuli and menthol. Cell 108:705–715

    PubMed  CAS  Article  Google Scholar 

  85. Pendyala S, Gorshkova IA, Usatyuk PV, He D, Pennathur A, Lambeth JD, Thannickal VJ, Natarajan V (2009) Role of Nox4 and Nox2 in hyperoxia-induced reactive oxygen species generation and migration of human lung endothelial cells. Antioxid Redox Signal 11:747–764

    PubMed  CAS  Article  Google Scholar 

  86. Perraud AL, Fleig A, Dunn CA, Bagley LA, Launay P, Schmitz C, Stokes AJ, Zhu Q, Bessman MJ, Penner R, Kinet JP, Scharenberg AM (2001) ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature 411:595–599

    PubMed  CAS  Article  Google Scholar 

  87. Petrotchenko EV, Yamaguchi N, Pasek DA, Borchers CH, Meissner G (2011) Mass spectrometric analysis and mutagenesis predict involvement of multiple cysteines in redox regulation of the skeletal muscle ryanodine receptor ion channel complex. Res Rep Biol 2011:13–21

    PubMed  Google Scholar 

  88. Post JM, Hume JR, Archer SL, Weir EK (1992) Direct role for potassium channel inhibition in hypoxic pulmonary vasoconstriction. Am J Physiol Cell Physiol 262:C882–C890

    CAS  Google Scholar 

  89. Quaegebeur A, Carmeliet P (2010) Oxygen sensing: a common crossroad in cancer and neurodegeneration. Curr. Top. Microbiol Immunol 345:71–103

    CAS  Article  Google Scholar 

  90. Rezvani HR, Ali N, Nissen LJ, Harfouche G, Verneuil H, de Taïeb A, Mazurier F (2011) HIF-1α in epidermis: oxygen sensing, cutaneous angiogenesis, cancer, and non-cancer disorders. J Invest Dermatol 131:1793–1805

    PubMed  CAS  Article  Google Scholar 

  91. Runnels LW, Yue L, Clapham DE (2001) TRP-PLIK, a bifunctional protein with kinase and ion channel activities. Science 291:1043–1047

    PubMed  CAS  Article  Google Scholar 

  92. Schofield CJ, Ratcliffe PJ (2004) Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 5:343–354

    PubMed  CAS  Article  Google Scholar 

  93. Semenza GL, Wang GL (1992) A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol 12:5447–5454

    PubMed  CAS  Google Scholar 

  94. Semenza GL (1999) Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol 15:551–578

    PubMed  CAS  Article  Google Scholar 

  95. Shan D, Marchase RB, Chatham JC (2008) Overexpression of TRPC3 increases apoptosis but not necrosis in response to ischemia-reperfusion in adult mouse cardiomyocytes. Am J Physiol Cell Physiol 294:C833–C841

    PubMed  CAS  Article  Google Scholar 

  96. Stea A, Nurse CA (1991) Whole-cell and perforated-patch recordings from O2-sensitive rat carotid body cells grown in short- and long-term culture. Pflugers Arch 418:93–101

    PubMed  CAS  Article  Google Scholar 

  97. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819–829

    PubMed  CAS  Article  Google Scholar 

  98. Sun HS, Jackson MF, Martin LJ, Jansen K, Teves L, Cui H, Kiyonaka S, Mori Y, Jones M, Forder JP, Golde TE, Orser BA, Macdonald JF, Tymianski M (2009) Suppression of hippocampal TRPM7 protein prevents delayed neuronal death in brain ischemia. Nat Neurosci 12:1300–1307

    PubMed  CAS  Article  Google Scholar 

  99. Sun J, Xin C, Eu JP, Stamler JS, Meissner G (2001) Cysteine-3635 is responsible for skeletal muscle ryanodine receptor modulation by NO. Proc Natl Acad Sci U S A 98:11158–11162

    PubMed  CAS  Article  Google Scholar 

  100. Sun MK, Reis DJ (1994) Hypoxia-activated Ca2+ currents in pacemaker neurones of rat rostral ventrolateral medulla in vitro. J Physiol 476:101–116

    PubMed  CAS  Google Scholar 

  101. Sun QA, Hess DT, Nogueira L, Yong S, Bowles DE, Eu J, Laurita KR, Meissner G, Stamler JS (2011) Oxygen-coupled redox regulation of the skeletal muscle ryanodine receptor-Ca2+ release channel by NADPH oxidase 4. Proc Natl Acad Sci U S A 108:16098–16103

    PubMed  CAS  Article  Google Scholar 

  102. Takahashi N, Kuwaki T, Kiyonaka S, Numata T, Kozai D, Mizuno Y, Yamamoto S, Naito S, Knevels E, Carmeliet P, Oga T, Kaneko S, Suga S, Nokami T, Yoshida J, Mori Y (2011) TRPA1 underlies a sensing mechanism for O2. Nat Chem Biol 7:701–711

    PubMed  CAS  Article  Google Scholar 

  103. Thompson RJ, Jackson A, Nurse CA (1997) Developmental loss of hypoxic chemosensitivity in rat adrenomedullary chromaffin cells. J Physiol 498:503–510

    PubMed  CAS  Google Scholar 

  104. Tymianski M (2011) Emerging mechanisms of disrupted cellular signaling in brain ischemia. Nat Neurosci 14:1369–1373

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  106. Venkatachalam K, Montell C (2007) TRP channels. Annu Rev Biochem 76:387–417

    PubMed  CAS  Article  Google Scholar 

  107. Voets T (2012) Quantifying and modeling the temperature-dependent gating of TRP channels. In: Nilius B, Amara SG, Gudermann T, Jahn R, Lill R, Offermanns S, Petersen OH (eds) Reviews of physiology, biochemistry and pharmacology. Springer, Berlin, pp 91–119

    Google Scholar 

  108. Voets T, Droogmans G, Wissenbach U, Janssens A, Flockerzi V, Nilius B (2004) The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430:748–754

    PubMed  CAS  Article  Google Scholar 

  109. Voets T, Talavera K, Owsianik G, Nilius B (2005) Sensing with TRP channels. Nat Chem Biol 1:85–92

    PubMed  CAS  Article  Google Scholar 

  110. Voss AA, Lango J, Ernst-Russell M, Morin D, Pessah IN (2004) Identification of hyperreactive cysteines within ryanodine receptor type 1 by mass spectrometry. J Biol Chem 279:34514–34520

    PubMed  CAS  Article  Google Scholar 

  111. Webb JD, Coleman ML, Pugh CW (2009) Hypoxia, hypoxia-inducible factors (HIF), HIF hydroxylases and oxygen sensing. Cell Mol Life Sci 66:3539–3554

    PubMed  CAS  Article  Google Scholar 

  112. Weir EK, López-Barneo J, Buckler KJ, Archer SL (2005) Acute oxygen-sensing mechanisms. N Engl J Med 353:2042–2055

    PubMed  CAS  Article  Google Scholar 

  113. Weir EK, Olschewski A (2006) Role of ion channels in acute and chronic responses of the pulmonary vasculature to hypoxia. Cardiovasc Res 71:630–641

    PubMed  CAS  Article  Google Scholar 

  114. Weissmann N, Dietrich A, Fuchs B, Kalwa H, Ay M, Dumitrascu R, Olschewski A, Storch U, Mederos Y, Schnitzler M, Ghofrani HA, Schermuly RT, Pinkenburg O, Seeger W, Grimminger F, Gudermann T (2006) Classical transient receptor potential channel 6 (TRPC6) is essential for hypoxic pulmonary vasoconstriction and alveolar gas exchange. Proc Natl Acad Sci U S A 103:19093–19098

    PubMed  CAS  Article  Google Scholar 

  115. Wenger RH (2000) Mammalian oxygen sensing, signalling and gene regulation. J Exp Biol 203:1253–1263

    PubMed  CAS  Google Scholar 

  116. Xie YF, MacDonald JF, Jackson MF (2010) TRPM2, calcium and neurodegenerative diseases. Int J Physiol Pathophysiol Pharmacol 2:95–103

    PubMed  CAS  Google Scholar 

  117. Yoshida T, Inoue R, Morii T, Takahashi N, Yamamoto S, Hara Y, Tominaga M, Shimizu S, Sato Y, Mori Y (2006) Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat Chem Biol 2:596–607

    PubMed  CAS  Article  Google Scholar 

  118. Youngson C, Nurse C, Yeger H, Cutz E (1993) Oxygen sensing in airway chemoreceptors. Nature 365:153–155

    PubMed  CAS  Article  Google Scholar 

  119. Zhu WH, Conforti L, Czyzyk-Krzeska MF, Millhorn DE (1996) Membrane depolarization in PC-12 cells during hypoxia is regulated by an O2-sensitive K+ current. Am J Physiol Cell Physiol 271:C658–C665

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yasuo Mori.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Numata, T., Ogawa, N., Takahashi, N. et al. TRP channels as sensors of oxygen availability. Pflugers Arch - Eur J Physiol 465, 1075–1085 (2013). https://doi.org/10.1007/s00424-013-1237-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-013-1237-9

Keywords

  • TRP channels
  • Oxygen
  • Cysteine
  • TRPA1
  • Ca2+