Skip to main content
NCBI home page
Protein & Cell logoLink to Protein & Cell
. 2010 Oct 7;1(9):802–810. doi: 10.1007/s13238-010-0108-9

Heteromerization of TRP channel subunits: extending functional diversity

Wei Cheng 1,2, Changsen Sun 1, Jie Zheng 2,✉
PMCID: PMC4875230  PMID: 21203922

Abstract

Transient receptor potential (TRP) channels are widely found throughout the animal kingdom. By serving as cellular sensors for a wide spectrum of physical and chemical stimuli, they play crucial physiological roles ranging from sensory transduction to cell cycle modulation. TRP channels are tetrameric protein complexes. While most TRP subunits can form functional homomeric channels, heteromerization of TRP channel subunits of either the same subfamily or different subfamilies has been widely observed. Heteromeric TRP channels exhibit many novel properties compared to their homomeric counterparts, indicating that co-assembly of TRP channel subunits has an important contribution to the diversity of TRP channel functions.

Keywords: co-assembly, molecular mechanism, diversification, nonselective cation channel, polymodal receptor, multi-subunit protein complex

References

  1. Alessandri-Haber N., Dina O.A., Chen X., Levine J.D. TRPC1 and TRPC6 channels cooperate with TRPV4 to mediate mechanical hyperalgesia and nociceptor sensitization. J Neurosci. 2009;29:6217–6228. doi: 10.1523/JNEUROSCI.0893-09.2009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arniges M., Fernández-Fernández J.M., Albrecht N., Schaefer M., Valverde M.A. Human TRPV4 channel splice variants revealed a key role of ankyrin domains in multimerization and trafficking. J Biol Chem. 2006;281:1580–1586. doi: 10.1074/jbc.M511456200. [DOI] [PubMed] [Google Scholar]
  3. Bai C.X., Giamarchi A., Rodat-Despoix L., Padilla F., Downs T., Tsiokas L., Delmas P. Formation of a new receptoroperated channel by heteromeric assembly of TRPP2 and TRPC1 subunits. EMBO Rep. 2008;9:472–479. doi: 10.1038/embor.2008.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bargal R., Avidan N., Ben-Asher E., Olender Z., Zeigler M., Frumkin A., Raas-Rothschild A., Glusman G., Lancet D., Bach G. Identification of the gene causing mucolipidosis type IV. Nat Genet. 2000;26:118–123. doi: 10.1038/79095. [DOI] [PubMed] [Google Scholar]
  5. Bautista D.M., Jordt S.E., Nikai T., Tsuruda P.R., Read A.J., Poblete J., Yamoah E.N., Basbaum A.I., Julius D. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell. 2006;124:1269–1282. doi: 10.1016/j.cell.2006.02.023. [DOI] [PubMed] [Google Scholar]
  6. Becker D., Müller M., Leuner K., Jendrach M. The Cterminal domain of TRPV4 is essential for plasma membrane localization. Mol Membr Biol. 2008;25:139–151. doi: 10.1080/09687680701635237. [DOI] [PubMed] [Google Scholar]
  7. Chang Q., Gyftogianni E., van de Graaf S.F., Hoefs S., Weidema F. A., Bindels R.J., Hoenderop J.G. Molecular determinants in TRPV5 channel assembly. J Biol Chem. 2004;279:54304–54311. doi: 10.1074/jbc.M406222200. [DOI] [PubMed] [Google Scholar]
  8. Cheng W., Yang F., Takanishi C.L., Zheng J. Thermosensitive TRPV channel subunits coassemble into heteromeric channels with intermediate conductance and gating properties. J Gen Physiol. 2007;129:191–207. doi: 10.1085/jgp.200709731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chuang H.H., Neuhausser W.M., Julius D. The supercooling agent icilin reveals a mechanism of coincidence detection by a temperature-sensitive TRP channel. Neuron. 2004;43:859–869. doi: 10.1016/j.neuron.2004.08.038. [DOI] [PubMed] [Google Scholar]
  10. Chubanov V., Mederos y Schnitzler M., Wäring J., Plank A., Gudermann T. Emerging roles of TRPM6/TRPM7 channel kinase signal transduction complexes. Naunyn Schmiedebergs Arch Pharmacol. 2005;371:334–341. doi: 10.1007/s00210-005-1056-4. [DOI] [PubMed] [Google Scholar]
  11. Chubanov V., Waldegger S., Mederos y Schnitzler M., Vitzthum H., Sassen M.C., Seyberth H.W., Konrad M., Gudermann T. Disruption of TRPM6/TRPM7 complex formation by a mutation in the TRPM6 gene causes hypomagnesemia with secondary hypocalcemia. Proc Natl Acad Sci U S A. 2004;101:2894–2899. doi: 10.1073/pnas.0305252101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Clapham D.E. TRP channels as cellular sensors. Nature. 2003;426:517–524. doi: 10.1038/nature02196. [DOI] [PubMed] [Google Scholar]
  13. Clapham D.E., Runnels L.W., Strübing C. The TRP ion channel family. Nat Rev Neurosci. 2001;2:387–396. doi: 10.1038/35077544. [DOI] [PubMed] [Google Scholar]
  14. Cosens D.J., Manning A. Abnormal electroretinogram from a Drosophila mutant. Nature. 1969;224:285–287. doi: 10.1038/224285a0. [DOI] [PubMed] [Google Scholar]
  15. Curcio-Morelli C., Zhang P., Venugopal B., Charles F.A., Browning M.F., Cantiello H.F., Slaugenhaupt S.A. Functional multimerization of mucolipin channel proteins. J Cell Physiol. 2010;222:328–335. doi: 10.1002/jcp.21956. [DOI] [PubMed] [Google Scholar]
  16. Delmas P. Polycystins: polymodal receptor/ion-channel cellular sensors. Pflugers Arch. 2005;451:264–276. doi: 10.1007/s00424-005-1431-5. [DOI] [PubMed] [Google Scholar]
  17. Delmas P., Nauli S.M., Li X., Coste B., Osorio N., Crest M., Brown D.A., Zhou J. Gating of the polycystin ion channel signaling complex in neurons and kidney cells. FASEB J. 2004;18:740–742. doi: 10.1096/fj.03-0319fje. [DOI] [PubMed] [Google Scholar]
  18. Di Palma F., Belyantseva I.A., Kim H.J., Vogt T.F., Kachar B., Noben-Trauth K. Mutations in Mcoln3 associated with deafness and pigmentation defects in varitint-waddler (Va) mice. Proc Natl Acad Sci U S A. 2002;99:14994–14999. doi: 10.1073/pnas.222425399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Engelke M., Friedrich O., Budde P., Schäfer C., Niemann U., Zitt C., Jüngling E., Rocks O., Lückhoff A., Frey J. Structural domains required for channel function of the mouse transient receptor potential protein homologue TRP1beta. FEBS Lett. 2002;523:193–199. doi: 10.1016/S0014-5793(02)02971-X. [DOI] [PubMed] [Google Scholar]
  20. Erler I., Hirnet D., Wissenbach U., Flockerzi V., Niemeyer B.A. Ca2+-selective transient receptor potential V channel architecture and function require a specific ankyrin repeat. J Biol Chem. 2004;279:34456–34463. doi: 10.1074/jbc.M404778200. [DOI] [PubMed] [Google Scholar]
  21. Feng S., Okenka G.M., Bai C.X., Streets A.J., Newby L.J., DeChant B.T., Tsiokas L., Obara T., Ong A.C. Identification and functional characterization of an N-terminal oligomerization domain for polycystin-2. J Biol Chem. 2008;283:28471–28479. doi: 10.1074/jbc.M803834200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. GarcÍa-Sanz N., Fernández-Carvajal A., Morenilla-Palao C., Planells-Cases R., Fajardo-Sánchez E., Fernández-Ballester G., Ferrer-Montiel A. Identification of a tetramerization domain in the C terminus of the vanilloid receptor. J Neurosci. 2004;24:5307–5314. doi: 10.1523/JNEUROSCI.0202-04.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Gaudet R. Divide and conquer: high resolution structural information on TRP channel fragments. J Gen Physiol. 2009;133:231–237. doi: 10.1085/jgp.200810137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Gillo B., Chorna I., Cohen H., Cook B., Manistersky I., Chorev M., Arnon A., Pollock J.A., Selinger Z., Minke B. Coexpression of Drosophila TRP and TRP-like proteins in Xenopus oocytes reconstitutes capacitative Ca2+ entry. Proc Natl Acad Sci U S A. 1996;93:14146–14151. doi: 10.1073/pnas.93.24.14146. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Goel M., Sinkins W.G., Schilling W.P. Selective association of TRPC channel subunits in rat brain synaptosomes. J Biol Chem. 2002;277:48303–48310. doi: 10.1074/jbc.M207882200. [DOI] [PubMed] [Google Scholar]
  26. Grimm D.H., Cai Y., Chauvet V., Rajendran V., Zeltner R., Geng L., Avner E.D., Sweeney W., Somlo S., Caplan M.J. Polycystin-1 distribution is modulated by polycystin-2 expression in mammalian cells. J Biol Chem. 2003;278:36786–36793. doi: 10.1074/jbc.M306536200. [DOI] [PubMed] [Google Scholar]
  27. Groves M.R., Barford D. Topological characteristics of helical repeat proteins. Curr Opin Struct Biol. 1999;9:383–389. doi: 10.1016/S0959-440X(99)80052-9. [DOI] [PubMed] [Google Scholar]
  28. Gudermann T., Hofmann T., Mederos Y.S.M., Dietrich A. Activation, subunit composition and physiological relevance of DAG-sensitive TRPC proteins. Novartis Found Symp. 2004;258:103–118. doi: 10.1002/0470862580.ch8. [DOI] [PubMed] [Google Scholar]
  29. Hanaoka K., Qian F., Boletta A., Bhunia A.K., Piontek K., Tsiokas L., Sukhatme V.P., Guggino W.B., Germino G.G. Coassembly of polycystin-1 and -2 produces unique cation-permeable currents. Nature. 2000;408:990–994. doi: 10.1038/35050128. [DOI] [PubMed] [Google Scholar]
  30. Hellwig N., Albrecht N., Harteneck C., Schultz G., Schaefer M. Homo- and heteromeric assembly of TRPV channel subunits. J Cell Sci. 2005;118:917–928. doi: 10.1242/jcs.01675. [DOI] [PubMed] [Google Scholar]
  31. Hoenderop J.G., Voets T., Hoefs S., Weidema F., Prenen J., Nilius B., Bindels R.J. Homo- and heterotetrameric architecture of the epithelial Ca2+ channels TRPV5 and TRPV6. EMBO J. 2003;22:776–785. doi: 10.1093/emboj/cdg080. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hofmann T., Schaefer M., Schultz G., Gudermann T. Subunit composition of mammalian transient receptor potential channels in living cells. Proc Natl Acad Sci U S A. 2002;99:7461–7466. doi: 10.1073/pnas.102596199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ishimaru Y., Inada H., Kubota M., Zhuang H., Tominaga M., Matsunami H. Transient receptor potential family members PKD1L3 and PKD2L1 form a candidate sour taste receptor. Proc Natl Acad Sci U S A. 2006;103:12569–12574. doi: 10.1073/pnas.0602702103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Jiang L.H. Subunit interaction in channel assembly and functional regulation of transient receptor potential melastatin (TRPM) channels. Biochem Soc Trans. 2007;35:86–88. doi: 10.1042/BST0350086. [DOI] [PubMed] [Google Scholar]
  35. Jin X., Touhey J., Gaudet R. Structure of the N-terminal ankyrin repeat domain of the TRPV2 ion channel. J Biol Chem. 2006;281:25006–25010. doi: 10.1074/jbc.C600153200. [DOI] [PubMed] [Google Scholar]
  36. Kobori T., Smith G.D., Sandford R., Edwardson J.M. The transient receptor potential channels TRPP2 and TRPC1 form a heterotetramer with a 22 stoichiometry and an alternating subunit arrangement. J Biol Chem. 2009;284:35507–35513. doi: 10.1074/jbc.M109.060228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Köttgen M., Buchholz B., Garcia-Gonzalez M.A., Kotsis F., Fu X., Doerken M., Boehlke C., Steffl D., Tauber R., Wegierski T., et al. TRPP2 and TRPV4 form a polymodal sensory channel complex. J Cell Biol. 2008;182:437–447. doi: 10.1083/jcb.200805124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Lepage P.K., Boulay G. Molecular determinants of TRP channel assembly. Biochem Soc Trans. 2007;35:81–83. doi: 10.1042/BST0350081. [DOI] [PubMed] [Google Scholar]
  39. Lepage P.K., Lussier M.P., Barajas-Martinez H., Bousquet S.M., Blanchard A.P., Francoeur N., Dumaine R., Boulay G. Identification of two domains involved in the assembly of transient receptor potential canonical channels. J Biol Chem. 2006;281:30356–30364. doi: 10.1074/jbc.M603930200. [DOI] [PubMed] [Google Scholar]
  40. Li M., Jiang J., Yue L. Functional characterization of homo- and heteromeric channel kinases TRPM6 and TRPM7. J Gen Physiol. 2006;127:525–537. doi: 10.1085/jgp.200609502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Liapi A., Wood J.N. Extensive co-localization and heteromultimer formation of the vanilloid receptor-like protein TRPV2 and the capsaicin receptor TRPV1 in the adult rat cerebral cortex. Eur J Neurosci. 2005;22:825–834. doi: 10.1111/j.1460-9568.2005.04270.x. [DOI] [PubMed] [Google Scholar]
  42. Lintschinger B., Balzer-Geldsetzer M., Baskaran T., Graier W.F., Romanin C., Zhu M.X., Groschner K. Coassembly of Trp1 and Trp3 proteins generates diacylglycerol- and Ca2+-sensitive cation channels. J Biol Chem. 2000;275:27799–27805. doi: 10.1074/jbc.M002705200. [DOI] [PubMed] [Google Scholar]
  43. Liu B., Zhang C., Qin F. Functional recovery from desensitization of vanilloid receptor TRPV1 requires resynthesis of phosphatidylinositol 4,5-bisphosphate. J Neurosci. 2005;25:4835–4843. doi: 10.1523/JNEUROSCI.1296-05.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Liu D., Liman E.R. Intracellular Ca2+ and the phospholipid PIP2 regulate the taste transduction ion channel TRPM5. Proc Natl Acad Sci U S A. 2003;100:15160–15165. doi: 10.1073/pnas.2334159100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Liu X., Bandyopadhyay B.C., Singh B.B., Groschner K., Ambudkar I.S. Molecular analysis of a store-operated and 2-acetyl-sn-glycerol-sensitive non-selective cation channel. Heteromeric assembly of TRPC1-TRPC3. J Biol Chem. 2005;280:21600–21606. doi: 10.1074/jbc.C400492200. [DOI] [PubMed] [Google Scholar]
  46. LopezJimenez N.D., Cavenagh M.M., Sainz E., Cruz-Ithier M.A., Battey J.F., Sullivan S.L. Two members of the TRPP family of ion channels, Pkd1l3 and Pkd2l1, are co-expressed in a subset of taste receptor cells. J Neurochem. 2006;98:68–77. doi: 10.1111/j.1471-4159.2006.03842.x. [DOI] [PubMed] [Google Scholar]
  47. McCleverty C.J., Koesema E., Patapoutian A., Lesley S.A., Kreusch A. Crystal structure of the human TRPV2 channel ankyrin repeat domain. Protein Sci. 2006;15:2201–2206. doi: 10.1110/ps.062357206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Mei Z.Z., Jiang L.H. Requirement for the N-terminal coiled-coil domain for expression and function, but not subunit interaction of, the ADPR-activated TRPM2 channel. J Membr Biol. 2009;230:93–99. doi: 10.1007/s00232-009-9190-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Mei Z.Z., Xia R., Beech D.J., Jiang L.H. Intracellular coiled-coil domain engaged in subunit interaction and assembly of melastatin-related transient receptor potential channel 2. J Biol Chem. 2006;281:38748–38756. doi: 10.1074/jbc.M607591200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Mery L., Strauss B., Dufour J.F., Krause K.H., Hoth M. The PDZ-interacting domain of TRPC4 controls its localization and surface expression in HEK293 cells. J Cell Sci. 2002;115:3497–3508. doi: 10.1242/jcs.115.17.3497. [DOI] [PubMed] [Google Scholar]
  51. Moiseenkova-Bell V.Y., Wensel T.G. Hot on the trail of TRP channel structure. J Gen Physiol. 2009;133:239–244. doi: 10.1085/jgp.200810123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Montell, C. (2005). The TRP superfamily of cation channels. Sci STKE 2005, re3. [DOI] [PubMed]
  53. Murakami M., Ohba T., Xu F., Shida S., Satoh E., Ono K., Miyoshi I., Watanabe H., Ito H., Iijima T. Genomic organization and functional analysis of murine PKD2L1. J Biol Chem. 2005;280:5626–5635. doi: 10.1074/jbc.M411496200. [DOI] [PubMed] [Google Scholar]
  54. Nilius B. Transient receptor potential (TRP) cation channels: rewarding unique proteins. Bull Mem Acad R Med Belg. 2007;162:244–253. [PubMed] [Google Scholar]
  55. Nilius B. TRP channels in disease. Biochim Biophys Acta. 2007;1772:805–812. doi: 10.1016/j.bbadis.2007.02.002. [DOI] [PubMed] [Google Scholar]
  56. Owsianik G., D’hoedt D., Voets T., Nilius B. Structurefunction relationship of the TRP channel superfamily. Rev Physiol Biochem Pharmacol. 2006;156:61–90. [PubMed] [Google Scholar]
  57. Phelps C.B., Huang R.J., Lishko P.V., Wang R.R., Gaudet R. Structural analyses of the ankyrin repeat domain of TRPV6 and related TRPV ion channels. Biochemistry. 2008;47:2476–2484. doi: 10.1021/bi702109w. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Plant T.D., Schaefer M. TRPC4 and TRPC5: receptoroperated Ca2+-permeable nonselective cation channels. Cell Calcium. 2003;33:441–450. doi: 10.1016/S0143-4160(03)00055-1. [DOI] [PubMed] [Google Scholar]
  59. Plant T.D., Schaefer M. Receptor-operated cation channels formed by TRPC4 and TRPC5. Naunyn Schmiedebergs Arch Pharmacol. 2005;371:266–276. doi: 10.1007/s00210-005-1055-5. [DOI] [PubMed] [Google Scholar]
  60. Poteser M., Graziani A., Rosker C., Eder P., Derler I., Kahr H., Zhu M.X., Romanin C., Groschner K. TRPC3 and TRPC4 associate to form a redox-sensitive cation channel. Evidence for expression of native TRPC3-TRPC4 heteromeric channels in endothelial cells. J Biol Chem. 2006;281:13588–13595. doi: 10.1074/jbc.M512205200. [DOI] [PubMed] [Google Scholar]
  61. Qian F., Germino F.J., Cai Y., Zhang X., Somlo S., Germino G. G. PKD1 interacts with PKD2 through a probable coiledcoil domain. Nat Genet. 1997;16:179–183. doi: 10.1038/ng0697-179. [DOI] [PubMed] [Google Scholar]
  62. Reaves B.J., Wolstenholme A.J. The TRP channel superfamily: insights into how structure, protein-lipid interactions and localization influence function. Biochem Soc Trans. 2007;35:77–80. doi: 10.1042/BST0350077. [DOI] [PubMed] [Google Scholar]
  63. Riccio A., Medhurst A.D., Mattei C., Kelsell R.E., Calver A.R., Randall A.D., Benham C.D., Pangalos M.N. mRNA distribution analysis of human TRPC family in CNS and peripheral tissues. Brain Res Mol Brain Res. 2002;109:95–104. doi: 10.1016/S0169-328X(02)00527-2. [DOI] [PubMed] [Google Scholar]
  64. Rohács T., Lopes C.M., Michailidis I., Logothetis D.E. PI(4,5)P2 regulates the activation and desensitization of TRPM8 channels through the TRP domain. Nat Neurosci. 2005;8:626–634. doi: 10.1038/nn1451. [DOI] [PubMed] [Google Scholar]
  65. Rutter A.R., Ma Q.P., Leveridge M., Bonnert T.P. Heteromerization and colocalization of TrpV1 and TrpV2 in mammalian cell lines and rat dorsal root ganglia. Neuroreport. 2005;16:1735–1739. doi: 10.1097/01.wnr.0000185958.03841.0f. [DOI] [PubMed] [Google Scholar]
  66. Salas M.M., Hargreaves K.M., Akopian A.N. TRPA1-mediated responses in trigeminal sensory neurons: interaction between TRPA1 and TRPV1. Eur J Neurosci. 2009;29:1568–1578. doi: 10.1111/j.1460-9568.2009.06702.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Schaefer M. Homo- and heteromeric assembly of TRP channel subunits. Pflugers Arch. 2005;451:35–42. doi: 10.1007/s00424-005-1467-6. [DOI] [PubMed] [Google Scholar]
  68. Schindl R., Romanin C. Assembly domains in TRP channels. Biochem Soc Trans. 2007;35:84–85. doi: 10.1042/BST0350084. [DOI] [PubMed] [Google Scholar]
  69. Schmidt M., Dubin A.E., Petrus M.J., Earley T.J., Patapoutian A. Nociceptive signals induce trafficking of TRPA1 to the plasma membrane. Neuron. 2009;64:498–509. doi: 10.1016/j.neuron.2009.09.030. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Sedgwick S.G., Smerdon S.J. The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem Sci. 1999;24:311–316. doi: 10.1016/S0968-0004(99)01426-7. [DOI] [PubMed] [Google Scholar]
  71. Sharif-Naeini R., Folgering J.H., Bichet D., Duprat F., Lauritzen I., Arhatte M., Jodar M., Dedman A., Chatelain F.C., Schulte U., et al. Polycystin-1 and -2 dosage regulates pressure sensing. Cell. 2009;139:587–596. doi: 10.1016/j.cell.2009.08.045. [DOI] [PubMed] [Google Scholar]
  72. Smith G.D., Gunthorpe M.J., Kelsell R.E., Hayes P.D., Reilly P., Facer P., Wright J.E., Jerman J.C., Walhin J.P., Ooi L., et al. TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature. 2002;418:186–190. doi: 10.1038/nature00894. [DOI] [PubMed] [Google Scholar]
  73. Stewart A.P., Smith G.D., Sandford R.N., Edwardson J.M. Atomic force microscopy reveals the alternating subunit arrangement of the TRPP2-TRPV4 heterotetramer. Biophys J. 2010;99:790–797. doi: 10.1016/j.bpj.2010.05.012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Stowers L., Holy T.E., Meister M., Dulac C., Koentges G. Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science. 2002;295:1493–1500. doi: 10.1126/science.1069259. [DOI] [PubMed] [Google Scholar]
  75. Strübing C., Krapivinsky G., Krapivinsky L., Clapham D.E. TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron. 2001;29:645–655. doi: 10.1016/S0896-6273(01)00240-9. [DOI] [PubMed] [Google Scholar]
  76. Strübing C., Krapivinsky G., Krapivinsky L., Clapham D.E. Formation of novel TRPC channels by complex subunit interactions in embryonic brain. J Biol Chem. 2003;278:39014–39019. doi: 10.1074/jbc.M306705200. [DOI] [PubMed] [Google Scholar]
  77. Tominaga M., Caterina M.J., Malmberg A.B., Rosen T.A., Gilbert H., Skinner K., Raumann B.E., Basbaum A.I., Julius D. The cloned capsaicin receptor integrates multiple painproducing stimuli. Neuron. 1998;21:531–543. doi: 10.1016/S0896-6273(00)80564-4. [DOI] [PubMed] [Google Scholar]
  78. Tsiokas L., Arnould T., Zhu C., Kim E., Walz G., Sukhatme V. P. Specific association of the gene product of PKD2 with the TRPC1 channel. Proc Natl Acad Sci U S A. 1999;96:3934–3939. doi: 10.1073/pnas.96.7.3934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Tsiokas L., Kim E., Arnould T., Sukhatme V.P., Walz G. Homo- and heterodimeric interactions between the gene products of PKD1 and PKD2. Proc Natl Acad Sci U S A. 1997;94:6965–6970. doi: 10.1073/pnas.94.13.6965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Tsuruda P.R., Julius D., Minor D.L., Jr. Coiled coils direct assembly of a cold-activated TRP channel. Neuron. 2006;51:201–212. doi: 10.1016/j.neuron.2006.06.023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Venkatachalam K., Hofmann T., Montell C. Lysosomal localization of TRPML3 depends on TRPML2 and the mucolipidosis-associated protein TRPML1. J Biol Chem. 2006;281:17517–17527. doi: 10.1074/jbc.M600807200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Vetter I., Cheng W., Peiris M., Wyse B.D., Roberts-Thomson S.J., Zheng J., Monteith G.R., Cabot P.J. Rapid, opioidsensitive mechanisms involved in transient receptor potential vanilloid 1 sensitization. J Biol Chem. 2008;283:19540–19550. doi: 10.1074/jbc.M707865200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Xu X.Z., Chien F., Butler A., Salkoff L., Montell C. TRPgamma, a drosophila TRP-related subunit, forms a regulated cation channel with TRPL. Neuron. 2000;26:647–657. doi: 10.1016/S0896-6273(00)81201-5. [DOI] [PubMed] [Google Scholar]
  84. Xu X.Z., Li H.S., Guggino W.B., Montell C. Coassembly of TRP and TRPL produces a distinct store-operated conductance. Cell. 1997;89:1155–1164. doi: 10.1016/S0092-8674(00)80302-5. [DOI] [PubMed] [Google Scholar]
  85. Yu Y., Ulbrich M.H., Li M.H., Buraei Z., Chen X.Z., Ong A.C., Tong L., Isacoff E.Y., Yang J. Structural and molecular basis of the assembly of the TRPP2/PKD1 complex. Proc Natl Acad Sci U S A. 2009;106:11558–11563. doi: 10.1073/pnas.0903684106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Zagranichnaya T.K., Wu X., Villereal M.L. Endogenous TRPC1, TRPC3, and TRPC7 proteins combine to form native store-operated channels in HEK-293 cells. J Biol Chem. 2005;280:29559–29569. doi: 10.1074/jbc.M505842200. [DOI] [PubMed] [Google Scholar]
  87. Zhang P., Luo Y., Chasan B., González-Perrett S., Montalbetti N., Timpanaro G.A., Cantero M.R., Ramos A.J., Goldmann W.H., Zhou J., et al. The multimeric structure of polycystin-2 (TRPP2): structural-functional correlates of homo- and heteromultimers with TRPC1. Hum Mol Genet. 2009;18:1238–1251. doi: 10.1093/hmg/ddp024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Zhang Y., Hoon M.A., Chandrashekar J., Mueller K.L., Cook B., Wu D., Zuker C.S., Ryba N.J. Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell. 2003;112:293–301. doi: 10.1016/S0092-8674(03)00071-0. [DOI] [PubMed] [Google Scholar]
  89. Zhong H., Molday L.L., Molday R.S., Yau K.W. The heteromeric cyclic nucleotide-gated channel adopts a 3A:1B stoichiometry. Nature. 2002;420:193–198. doi: 10.1038/nature01201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Zhou X.L., Batiza A.F., Loukin S.H., Palmer C.P., Kung C., Saimi Y. The transient receptor potential channel on the yeast vacuole is mechanosensitive. Proc Natl Acad Sci U S A. 2003;100:7105–7110. doi: 10.1073/pnas.1230540100. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Protein & Cell are provided here courtesy of Oxford University Press

RESOURCES