The TRPC Family of TRP Channels: Roles Inferred (Mostly) from Knockout Mice and Relationship to ORAI Proteins (original) (raw)
References
Bair AM, Thippegowda PB, Freichel M, Cheng N, Ye RD, Vogel SM, Yu Y, Flockerzi V, Malik AB, Tiruppathi C (2009) Ca2+ entry via TRPC channels is necessary for thrombin-induced NF-kappaB activation in endothelial cells through AMP-activated protein kinase and protein kinase Cdelta. J Biol Chem 284:563–574. doi: 10.1074/jbc.M803984200. Epub 2008 Nov 6
Beck A, Speicher T, Stoerger C, Sell T, Dettmer V, Jusoh SA, Abdulmughni A, Cavalié A, Philipp SE, Zhu MX, Helms V, Wissenbach U, Flockerzi V (2013) Conserved gating elements in TRPC4 and TRPC5 channels. J Biol Chem 288:19471–19483 ArticleCASPubMedPubMed Central Google Scholar
Becker EB, Oliver PL, Glitsch MD, Banks GT, Achilli F, Hardy A, Nolan PM, Fisher EM, Davies KE (2009) A point mutation in TRPC3 causes abnormal Purkinje cell development and cerebellar ataxia in moonwalker mice. Proc Natl Acad Sci U S A 106:6706–6711 ArticleCASPubMedPubMed Central Google Scholar
Chaudhuri P, Colles SM, Bhat M, Van Wagoner DR, Birnbaumer L, Graham LM (2008) Elucidation of a TRPC6-TRPC5 channel cascade that restricts endothelial cell movement. Mol Biol Cell 19:3203–3211 ArticleCASPubMedPubMed Central Google Scholar
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 ArticleCASPubMedPubMed Central Google Scholar
Davis J, Burr AR, Davis G, Birnbaumer L, Molkentin JD (2012) A novel TRPC6-dependent pathway for myofibroblast transdifferentiation and wound healing in vivo. Dev Cell 23:705–715 ArticleCASPubMedPubMed Central Google Scholar
Dietrich A, Mederos Y, Schnitzler M, Gollasch M, Gross V, Storch U, Dubrovska G, Obst M, Yildirim E, Salanova B, Kalwa H, Essin K, Pinkenburg O, Luft FC, Gudermann T, Birnbaumer L (2005) Increased vascular smooth muscle contractility in TRPC6-/- mice. Mol Cell Biol 25:6980–6989 ArticleCASPubMedPubMed Central Google Scholar
Dietrich A, Kalwa H, Storch U, Mederos y Schnitzler M, Salanova B, Pinkenburg O, Dubrovska G, Essin K, Gollasch M, Birnbaumer L, Gudermann T (2007) Pressure-induced and store-operated cation influx in vascular smooth muscle cells is independent of TRPC1. Pflugers Arch 455:465–477 ArticleCASPubMed Google Scholar
Eckel J, Lavin PJ, Finch EA, Mukerji N, Burch J, Gbadegesin R, Wu G, Bowling B, Byrd A, Hall G, Sparks M, Zhang ZS, Homstad A, Barisoni L, Birnbaumer L, Rosenberg P, Winn MP (2011) TRPC6 enhances angiotensin II-induced albuminuria. J Am Soc Nephrol 22:526–535 ArticleCASPubMedPubMed Central Google Scholar
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 441:179–185 ArticleCASPubMed Google Scholar
Freichel M, Suh SH, Pfeifer A, Schweig U, Trost C, Weissgerber P, Biel M, Philipp S, Freise D, Droogmans G, Hofmann F, Flockerzi V, Nilius B (2001) Lack of an endothelial store-operated Ca2+ current impairs agonist-dependent vasorelaxation in TRP4-/- mice. Nat Cell Biol 3:121–127 ArticleCASPubMed Google Scholar
Gerasimenko JV, Gryshchenko O, Ferdek PE, Stapleton E, Hébert TO, Bychkova S, Peng S, Begg M, Gerasimenko OV, Petersen OH (2013) Ca2+ release-activated Ca2+ channel blockade as a potential tool in antipancreatitis therapy. Proc Natl Acad Sci U S A 110:13186–13191 ArticleCASPubMedPubMed Central Google Scholar
Gwack Y, Srikanth S, Oh-Hora M, Hogan PG, Lamperti ED, Yamashita M, Gelinas C, Neems DS, Sasaki Y, Feske S, Prakriya M, Rajewsky K, Rao A (2008) Hair loss and defective T- and B-cell function in mice lacking ORAI1. Mol Cell Biol 28:5209–5222 ArticleCASPubMedPubMed Central Google Scholar
Harper MT, Camacho Londoño JE, Quick K, Camacho Londoño J, Flockerz V, Philipp S, Birnbaumer L, Freichel M, Poole AW (2013) Transient receptor potential channels function as a coincidence signal detector mediating phosphatidylserine exposure. Sci Signal 6:ra80 Google Scholar
Hartmann J, Dragicevic E, Adelsberger H, Henning HA, Sumser M, Abramowitz J, Blum R, Dietrich A, Freichel M, Flockerzi V, Birnbaumer L, Konnerth A (2008) TRPC3 channels are required for synaptic transmission and motor coordination. Neuron 59:392–398 ArticleCASPubMedPubMed Central Google Scholar
Hou X, Pedi L, Diver MM, Long SB (2012) Crystal structure of the calcium release-activated calcium channel Orai. Science 338:1308–1313 ArticleCASPubMedPubMed Central Google Scholar
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 284:9733–9741 ArticleCASPubMedPubMed Central Google Scholar
Kim KD, Srikanth S, Yee MK, Mock DC, Lawson GW, Gwack Y (2011) ORAI1 deficiency impairs activated T cell death and enhances T cell survival. J Immunol 187:3620–3630 ArticleCASPubMedPubMed Central Google Scholar
Klaiber M, Dankworth B, Kruse M, Hartmann M, Nikolaev VO, Yang RB, Völker K, Gassner B, Oberwinkler H, Feil R, Freichel M, Groschner K, Skryabin BV, Frantz S, Birnbaumer L, Pongs O, Kuhn M (2011) A cardiac pathway of cyclic GMP-independent signaling of guanylyl cyclase A, the receptor for atrial natriuretic peptide. Proc Natl Acad Sci U S A 108:18500–18505 ArticleCASPubMedPubMed Central Google Scholar
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 ArticleCASPubMedPubMed Central Google Scholar
Liao Y, Erxleben C, Abramowitz J, Flockerzi V, Zhu MX, Armstrong DL, Birnbaumer L (2008) Functional interactions among Orai1, TRPCs, and STIM1 suggest a STIM-regulated heteromeric Orai/TRPC model for SOCE/Icrac channels. Proc Natl Acad Sci U S A 105:2895–2900 ArticleCASPubMedPubMed Central Google Scholar
Liao Y, Plummer NW, George MD, Abramowitz J, Zhu MX, Birnbaumer L (2009) A role for Orai in TRPC-mediated Ca2+ entry suggests that a TRPC:Orai complex may mediate store and receptor operated Ca2+ entry. Proc Natl Acad Sci U S A 106:3202–3206 ArticleCASPubMedPubMed Central Google Scholar
Liman ER, Innan H (2003) Relaxed selective pressure on an essential component of pheromone transduction in primate evolution. Proc Natl Acad Sci U S A 100:3328–3332 ArticleCASPubMedPubMed Central Google Scholar
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 104:17542–17547 ArticleCASPubMedPubMed Central Google Scholar
Long SB, Tao X, Campbell EB, MacKinnon R (2007) Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature 450:376–382 ArticleCASPubMed Google Scholar
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 174:815–825 ArticleCASPubMedPubMed Central Google Scholar
Mercer JC, Dehaven WI, Smyth JT, Wedel B, Boyles RR, Bird GS, Putney JW Jr (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 ArticleCASPubMedPubMed Central Google Scholar
Mio K, Ogura T, Kiyonaka S, Hiroaki Y, Tanimura Y, Fujiyoshi Y, Mori Y, Sato C (2007) The TRPC3 channel has a large internal chamber surrounded by signal sensing antennas. J Mol Biol 367(2):373–383, Epub 2006 ArticleCASPubMed Google Scholar
Munsch T, Freichel M, Flockerzi V, Pape HC (2003) Contribution of transient receptor potential channels to the control of GABA release from dendrites. Proc Natl Acad Sci U S A 100:16065–16070 ArticleCASPubMedPubMed Central Google Scholar
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 282:9105–9116 ArticleCASPubMedPubMed Central Google Scholar
Onohara N, Nishida M, Inoue R, Kobayashi H, Sumimoto H, Sato Y, Mori Y, Nagao T, Kurose H (2006) TRPC3 and TRPC6 are essential for angiotensin II-induced cardiac hypertrophy. EMBO J 25:5305–5316 ArticleCASPubMedPubMed Central Google Scholar
Park CY, Hoover PJ, Mullins FM, Bachhawat P, Covington ED, Raunser S, Walz T, Garcia KC, Dolmetsch RE, Lewis RS (2009) STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 136:876–890 ArticleCASPubMedPubMed Central Google Scholar
Peinelt C, Vig M, Koomoa DL, Beck A, Nadler MJ, Koblan-Huberson M, Lis A, Fleig A, Penner R, Kinet JP (2006) Amplification of CRAC current by STIM1 and CRACM1 (Orai1). Nat Cell Biol 8:771–773 ArticleCASPubMed Google Scholar
Penna A, Demuro A, Yeromin AV, Zhang SL, Safrina O, Parker I, Cahalan MD (2008) The CRAC channel consists of a tetramer formed by Stim-induced dimerization of Orai dimers. Nature 456:116–120 ArticleCASPubMedPubMed Central Google Scholar
Perez-Leighton CE, Schmidt TM, Abramowitz J, Birnbaumer L, Kofuji P (2011) Intrinsic phototransduction persists in melanopsin-expressing ganglion cells lacking diacylglycerol-sensitive TRPC subunits. Eur J Neurosci 33:856–867 ArticlePubMedPubMed Central Google Scholar
Phelan KD, Mock MM, Kretz O, Shwe UT, Kozhemyakin M, Greenfield LJ, Dietrich A, Birnbaumer L, Freichel M, Flockerzi V, Zheng F (2012) Heteromeric canonical transient receptor potential 1 and 4 channels play a critical role in epileptiform burst firing and seizure-induced neurodegeneration. Mol Pharmacol 81:384–392 ArticleCASPubMedPubMed Central Google Scholar
Phelan KD, Shwe UT, Abramowitz J, Wu H, Rhee SW, Howell MD, Gottschall PE, Freichel M, Flockerzi V, Birnbaumer L, Zheng F (2013) Canonical transient receptor channel 5 (TRPC5) and TRPC1/4 contribute to seizure and excitotoxicity by distinct cellular mechanisms. Mol Pharmacol 83:429–438 ArticleCASPubMedPubMed Central Google Scholar
Poteser M, Schleifer H, Lichtenegger M, Schernthaner M, Stockner T, Kappe CO, Glasnov TN, Romanin C, Groschner K (2011) PKC-dependent coupling of calcium permeation through transient receptor potential canonical 3 (TRPC3) to calcineurin signaling in HL-1 myocytes. Proc Natl Acad Sci U S A 108:10556–10561 ArticleCASPubMedPubMed Central Google Scholar
Quick K, Zhao J, Eijkelkamp N, Linley JE, Rugiero F, Cox JJ, Raouf R, Gringhuis M, Sexton JE, Abramowitz J, Taylor R, Forge A, Ashmore J, Kirkwood N, Kros CJ, Richardson GP, Freichel M, Flockerzi V, Birnbaumer L, Wood JN (2012) TRPC3 and TRPC6 are essential for normal mechanotransduction in subsets of sensory neurons and cochlear hair cells. Open Biol 2:120068 ArticlePubMedPubMed Central Google Scholar
Reiser J, Polu KR, Möller CC, Kenlan P, Altintas MM, Wei C, Faul C, Herbert S, Villegas I, Avila-Casado C, McGee M, Sugimoto H, Brown D, Kalluri R, Mundel P, Smith PL, Clapham DE, Pollak MR (2005) TRPC6 is a glomerular slit diaphragm-associated channel required for normal renal function. Nat Genet 37:739–744 ArticleCASPubMedPubMed Central Google Scholar
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 ArticleCASPubMedPubMed Central Google Scholar
Sandow SL, Tare M, Coleman HA, Hill CE, Parkington HC (2002) Involvement of myoendothelial gap junctions in the actions of endothelium-derived hyperpolarizing factor. Circ Res 90:1108–1113 ArticleCASPubMed Google Scholar
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 122:1354–1367 ArticleCASPubMedPubMed Central Google Scholar
Senadheera S, Kim Y, Grayson TH, Toemoe S, Kochukov MY, Abramowitz J, Housley GD, Bertrand RL, Chadha PS, Bertrand PP, Murphy TV, Tare M, Birnbaumer L, Marrelli SP, Sandow SL (2012) Transient receptor potential canonical type 3 channels facilitate endothelium-derived hyperpolarization-mediated resistance artery vasodilator activity. Cardiovasc Res 95:439–447 ArticleCASPubMedPubMed Central Google Scholar
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 105:1023–1030 ArticleCASPubMedPubMed Central Google Scholar
Shi J, Ju M, Saleh SN, Albert AP, Large WA (2010) TRPC6 channels stimulated by angiotensin II are inhibited by TRPC1/C5 channel activity through a Ca2+− and PKC-dependent mechanism in native vascular myocytes. J Physiol 588:3671–3682 ArticleCASPubMedPubMed Central Google Scholar
Shi J, Ju M, Abramowitz J, Large WA, Birnbaumer L, Albert AP (2012) TRPC1 proteins confer PKC and phosphoinositol activation on native heteromeric TRPC1/C5 channels in vascular smooth muscle: comparative study of wild-type and TRPC1-/- mice. FASEB J 26:409–419 ArticleCASPubMedPubMed Central Google Scholar
Smedlund K, Tano JY, Vazquez G (2010) The constitutive function of native TRPC3 channels modulates vascular cell adhesion molecule-1 expression in coronary endothelial cells through nuclear factor kappaB signaling. Circ Res 106:1479–1488 ArticleCASPubMed Google Scholar
Stowers L, Holy TE, Meister M, Dulac C, Koentges G (2002) Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 295:1493–1500 ArticleCASPubMed Google Scholar
Stroh O, Freichel M, Kretz O, Birnbaumer L, Hartmann J, Egger V (2012) NMDA receptor-dependent synaptic activation of TRPC channels in olfactory bulb granule cells. J Neurosci 32:5737–5746 ArticleCASPubMedPubMed Central Google Scholar
Suresh Babu S, Wojtowicz A, Freichel M, Birnbaumer L, Hecker M, Cattaruzza M (2012) Mechanism of stretch-induced activation of the mechanotransducer zyxin in vascular endothelial cells. Sci Signal 5:ra91 PubMed Google Scholar
Tai C, Hines DJ, Choi HB, MacVicar BA (2011) Plasma membrane insertion of TRPC5 channels contributes to the cholinergic plateau potential in hippocampal CA1 pyramidal neurons. Hippocampus 21:958–967 CASPubMed Google Scholar
Tano JY, Vazquez G (2011) Requirement for non-regulated, constitutive calcium influx in macrophage survival signaling. Biochem Biophys Res Commun 407:432–437 ArticleCASPubMed Google Scholar
Tano JY, Smedlund K, Lee R, Abramowitz J, Birnbaumer L, Vazquez G (2011) Impairment of survival signaling and efferocytosis in TRPC3-deficient macrophages. Biochem Biophys Res Commun 410(3):643–647. doi:10.1016/j.bbrc.2011.06.045 ArticleCASPubMed Google Scholar
Tauseef M, Knezevic N, Chava KR, Smith M, Sukriti S, Gianaris S, Obukhov AG, Vogel SM, Schraufnagel SE, Dietrich A, Birnbaumer L, Malik AB, Mehta D (2012) Cation channel TRPC6 activation of TLR4 in endothelial cells mediates sepsis-induced acute lung injury. J Exp Med 209:1953–1968 ArticleCASPubMedPubMed Central Google Scholar
Tsvilovskyy VV, Zholos AV, Aberle T, Philipp SE, Dietrich A, Zhu MX, Birnbaumer L, Freichel M, Flockerzi V (2009) Deletion of TRPC4 and TRPC6 in mice impairs smooth muscle contraction and intestinal motility in vivo. Gastroenterology 137:1415–1424 ArticlePubMedPubMed Central Google Scholar
Vannier B, Zhu X, Brown D, Birnbaumer L (1998) The membrane topology of human transient receptor potential 3 as inferred from glycosylation-scanning mutagenesis and epitope immunocytochemistry. J Biol Chem 273:8675–8679 ArticleCASPubMed Google Scholar
Vig M, Peinelt C, Beck A, Koomoa DL, Rabah D, Koblan-Huberson M, Kraft S, Turner H, Fleig A, Penner R, Kinet JP (2006) CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 312:1220–1223 ArticleCASPubMed Google Scholar
Vig M, DeHaven WI, Bird GS, Billingsley JM, Wang H, Rao PE, Hutchings AB, Jouvin MH, Putney JW, Kinet JP (2008) Defective mast cell effector functions in mice lacking the CRACM1 pore subunit of store-operated calcium release-activated calcium channels. Nat Immunol 9:89–96 ArticleCASPubMedPubMed Central Google Scholar
Welsh DG, Morielli AD, Nelson MT, Brayden JE (2003) Transient receptor potential channels regulate myogenic tone of resistance arteries. Circ Res 90:248–250 Article Google Scholar
Winn MP, Conlon PJ, Lynn KL, Farrington MK, Creazzo T, Hawkins AF, Daskalakis N, Kwan SY, Ebersviller S, Burchette JL, Pericak-Vance MA, Howell DN, Vance JM, Rosenberg PB (2005) A mutation in the TRPC6 cation channel causes familial focal segmental glomerulosclerosis. Science 308:1801–1804 ArticleCASPubMed Google Scholar
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 174:803–813 ArticleCASPubMedPubMed Central Google Scholar
Xue T, Do MT, Riccio A, Jiang Z, Hsieh J, Wang HC, Merbs SL, Welsbie DS, Yoshioka T, Weissgerber P, Stolz S, Flockerzi V, Freichel M, Simon MI, Clapham DE, Yau KW (2011) Melanopsin signalling in mammalian iris and retina. Nature 479:67–73 ArticleCASPubMedPubMed Central Google Scholar
Yildirim E, Carey MA, Card JW, Dietrich A, Flake GP, Zhang Y, Bradbury JA, Rebolloso Y, Germolec DR, Morgan DL, Zeldin DC, Birnbaumer L (2012) Severely blunted allergen-induced pulmonary Th2-cell response and lung hyperresponsiveness in type 1 transient receptor potential channel (TRPC1)-deficient mice. Am J Physiol Lung Cell Mol Physiol 303:L539–L549 ArticleCASPubMedPubMed Central Google Scholar
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 11:337–343 ArticleCASPubMedPubMed Central Google Scholar
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–C162 ArticleCASPubMedPubMed Central Google Scholar
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 287:14524–14534 ArticleCASPubMedPubMed Central Google Scholar
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 32:439–448 ArticleCASPubMedPubMed Central Google Scholar
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 103:9357–9362 ArticleCASPubMedPubMed Central Google Scholar
Zimmermann K, Lennerz JK, Hein A, Link AS, Kaczmarek JS, Delling M, Uysal S, Pfeifer JD, Riccio A, Clapham DE (2011) Transient receptor potential cation channel, subfamily C, member 5 (TRPC5) is a cold-transducer in the peripheral nervous system. Proc Natl Acad Sci U S A 108:18114–18119 ArticleCASPubMedPubMed Central Google Scholar