Extracellular disulfide bridges stabilize TRPC5 dimerization, trafficking, and activity

Pflugers Archiv European Journal of Physiology

Volumn 467, Issue 4, 2015, Pages 703-712

  Hong, Chansik ^a   Kwak, Misun ^a   Myeong, Jongyun ^a   Ha, Kotdaji ^a   Wie, Jinhong ^a   Jeon, Ju Hong ^a   So, Insuk ^a  

^a Seoul National University College of Medicine   (South Korea)

Author keywords

Cysteine; Disulfide; DTT; Tetramer; Trafficking; TRPC5

Indexed keywords

CYSTINE; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TRPC5 PROTEIN, HUMAN;

ANIMAL; CHEMISTRY; HEK293 CELL LINE; HUMAN; METABOLISM; MOUSE; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT;

ANIMALS; CYSTINE; HEK293 CELLS; HUMANS; MICE; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; TRPC CATION CHANNELS;

EID: 84939880965     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1540-0     Document Type: Article

References (34)

1. Ahmmed GU, Malik AB (2005) Functional role of TRPC channels in the regulation of endothelial permeability. Pflugers Arch 451(1):131–142. doi:10.1007/s00424-005-1461-z
2. Bienert GP, Cavez D, Besserer A, Berny MC, Gilis D, Rooman M, Chaumont F (2012) A conserved cysteine residue is involved in disulfide bond formation between plant plasma membrane aquaporin monomer. Biochem J 445(1):101–111. doi:10.1042/BJ20111704
3. Blair NT, Kaczmarek JS, Clapham DE (2009) Intracellular calcium strongly potentiates agonist-activated TRPC5 channels. J Gen Physiol 133(5):525–546. doi:10.1085/jgp.200810153
4. Bollimuntha S, Selvaraj S, Singh BB (2011) Emerging roles of canonical TRP channels in neuronal function. Adv Exp Med Biol 704:573–593. doi:10.1007/978-94-007-0265-3_31
5. Braakman I, Helenius J, Helenius A (1992) Manipulating disulfide bond formation and protein folding in the endoplasmic reticulum. EMBO J 11(5):1717–1722
6. Brohawn SG, del Mármol J, MacKinnon R (2012) Crystal structure of the human K2P TRAAK, a lipid- and mechano-sensitive K + ion channel. Science 335(6067):436–441. doi:10.1126/science.1213808
7. Chen C, Calhoun JD, Zhang Y, Lopez-Santiago L, Zhou N, Davis TH, Salzer JL, Isom LL (2012) Identification of the cysteine residue responsible for disulfide linkage of Na + channel α and β2 subunits. J Biol Chem 287(46):39061–39069. doi:10.1074/jbc.M112.397646
8. Cho HC, Tsushima RG, Nguyen TT, Guy HR, Backx PH (2000) Two critical cysteine residues implicated in disulfide bond formation and proper folding of Kir2.1. Biochemistry 39(16):4649–4657. doi:10.1021/bi992469g
9. Dietrich A, Kalwa H, Fuchs B, Grimminger F, Weissmann N, Gudermann T (2007) In vivo TRPC functions in the cardiopulmonary vasculature. Cell Calcium 42(2):233–244. doi:10.1016/j.ceca.2007.02.009
10. Ennion SJ, Evans RJ (2002) Conserved cysteine residues in the extracellular loop of the human P2X(1) receptor form disulfide bonds and are involved in receptor trafficking to the cell surface. Mol Pharmacol 61(2):303–311. doi:10.1124/mol.61.2.303
11. Freichel M, Vennekens R, Olausson J, Hoffmann M, Müller C, Stolz S, Scheunemann J, Weissgerber P, Flockerzi V (2004) Functional role of TRPC proteins in vivo: lessons from TRPC-deficient mouse models. Biochem Biophys Res Commun 322(4):1352–1358. doi:10.1016/j.bbrc.2004.08.041
12. 2+-selective ion channels. J Biol Chem 284(49):34423–34432. doi:10.1074/jbc.M109.018192
13. Hong C, Kim J, Jeon JP, Wie J, Kwak M, Ha K, Kim H, Myeong J, Kim SY, Jeon JH, So I (2012) Gs cascade regulates canonical transient receptor potential 5 (TRPC5) through cAMP mediated intracellular Ca2+ release and ion channel trafficking. Biochem Biophys Res Commun 421(1):105–111. doi:10.1016/j.bbrc.2012.03.123
14. Jeon JP, Hong C, Park EJ, Jeon JH, Cho NH, Kim IG, Choe H, Muallem S, Kim HJ, So I (2012) Selective Gαi subunits as novel direct activators of transient receptor potential canonical (TRPC)4 and TRPC5 channels. J Biol Chem 287(21):17029–17039. doi:10.1074/jbc.M111.326553
15. Jung S, Mühle A, Schaefer M, Strotmann R, Schultz G, Plant TD (2003) Lanthanides potentiate TRPC5 currents by an action at extracellular sites close to the pore mouth. J Biol Chem 278(6):3562–3571. doi:10.1074/jbc.M211484200
16. Kang TM, Kim YC, Sim JH, Rhee JC, Kim SJ, Uhm DY, So I, Kim KW (2001) The properties of carbachol-activated nonselective cation channels at the single channel level in guinea pig gastric myocytes. Jpn J Pharmocol 85(3):291–298. doi:10.1254/jjp.85.291
17. Kanki H, Kinoshita M, Akaike A, Satoh M, Mori Y, Kaneko S (2001) Activation of inositol 1,4,5-triphosphate receptor is essential for the opening of mouse TRP5 channels. Mol Pharmacol 60(5):989–998. doi:10.1124/mol.60.5.989
18. Kim MJ, Jeon JP, Kim HJ, Kim BJ, Lee YM, Choe H, Jeon JH, Kim SJ, So I (2008) Molecular determinant of sensing extracellular pH in classical transient receptor potential channel 5. Biochem Biophys Res Commun 365(2):239–245. doi:10.1016/j.bbrc.2007.10.154
19. Lee KP, Jun JY, Chang IY, Suh SH, So I, Kim KW (2005) TRPC4 is an essential component of the nonselective cation channel activated by muscarinic stimulation in mouse visceral smooth muscle cells. Mol Cells 20(3):435–441
20. Lee YM, Kim BJ, Kim HJ, Yang DK, Zhu MH, Lee KP, So I, Kim KW (2003) TRPC5 as a candidate for the nonselective cation channel activated by muscarinic stimulation in murine stomach. Am J Physiol Gastrointest Liver Physiol 284(4):G604–G616. doi:10.1152/ajpgi.00069.2002
21. Lesage F, Reyes R, Fink M, Duprat F, Guillemare E, Lazdunski M (1996) Dimerization of TWIK-1 K + channel subunits via a disulfide bridge. EMBO J 15(23):6400–6407
22. Leyland ML, Dart C, Spencer PJ, Sutcliffe MJ, Stanfield PR (1999) The possible role of a disulfide bond in forming functional Kir2.1 potassium channels. Pflugers Arch 438(6):778–781. doi:10.1007/s004249900153
23. 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(5):3403–3411. doi:10.1074/jbc.275.5.3403
24. Nilius B, Owsianik G, Voets T, Peters JA (2007) Transient receptor potential cation channels in disease. Physiol Rev 87(1):165–217. doi:10.1152/physrev.00021.2006
25. Schaefer M, Plant TD, Obukhov AG, Hofmann T, Gudermann T, Schultz G (2000) Receptor-mediated regulation of the nonselective cation channels TRPC4 and TRPC5. J Biol Chem 275(23):17517–17526. doi:10.1074/jbc.275.23.17517
26. So I, Kim KW (2003) Nonselective cation channels activated by the stimulation of muscarinic receptors in mammalian gastric smooth muscle. J Smooth Muscle Res 39(6):231–247. doi:10.1540/jsmr.39.231
27. Strubing C, Krapivinsky G, Krapivinsky L, Clapham DE (2003) Formation of novel TRPC channels by complex subunit interactions in embryonic brain. J Biol Chem 278(40):39014–39019. doi:10.1074/jbc.M306705200
28. Tao X, Avalos JL, Chen J, MacKinnon R (2009) Crystal Structure of the eukaryotic strong inward-rectifier K + channel Kir2.2 at 3.1 Å resolution. Science 326(5960):1668–1674. doi:10.1126/science.1180310
29. 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(4):1415–1424. doi:10.1053/j.gastro.2009.06.046
30. Venkatachalam K, van Rossum DB, Patterson RL, Ma HT, Gill DL (2002) The cellular and molecular basis of store-operated calcium entry. Nat Cell Biol 4(11):E263–E272. doi:10.1038/ncb1102-e263
31. Xu SZ, Sukumar P, Zeng F, Li J, Jairaman A, English A, Naylor J, Ciurtin C, Majeed Y, Milligan CJ, Bahnasi YM, Al-Shawaf E, Porter KE, Jiang LH, Emery P, Sivaprasadarao A, Beech DJ (2008) TRPC channel activation by extracellular thioredoxin. Nature 451(7174):69–72. doi:10.1038/nature06414
32. Yip H, Chan WY, Leung PC, Kwan HY, Liu C, Huang Y, Michel V, Yew DT, Yao X (2004) Expression of TRPC homologs in endothelial cells and smooth muscle layers of human arteries. Histochem Cell Biol 122(6):553–561. doi:10.1007/s00418-004-0720-y
33. 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(11):596–607. doi:10.1038/nchembio821
34. Yu MS, Ho YS, So KF, Yuen WH, Chang RC (2006) Cytoprotective effects of Lycium barbarum against reducing stress on endoplasmic reticulum. Int J Mol Med 17(6):1157–1161. doi:10.3892/ijmm.17.6.1157