Critical roles of Gi/o proteins and phospholipase C-δ1 in the activation of receptor-operated TRPC4 channels

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 4, 2016, Pages 109-1097

  Thakur, Dhananjay P ^a,b   Tian, Jin Bin ^a   Jeon, Jaepyo ^a   Xiong, Jian ^a,b   Huang, Yu ^a,b   Flockerzi, Veit ^c   Zhu, Michael X ^a,b  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c SAARLAND UNIVERSITY   (Germany)

Author keywords

Calcium; G proteins; Pertussis toxin; Phospholipase C; TRP channels

Indexed keywords

CALCIUM ION; GUANOSINE TRIPHOSPHATASE; OPIATE RECEPTOR; PHOSPHATASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOLIPASE C DELTA1; PROTEIN G; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL 4; CALCIUM; CARBACHOL; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; PHOSPHOLIPASE C DELTA; RHOA PROTEIN, HUMAN; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TRPC4 ION CHANNEL;

ALPHA CHAIN; ARTICLE; CALCIUM CELL LEVEL; HEK293 CELL LINE; HUMAN; HUMAN CELL; KIDNEY CARCINOMA; MUTANT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SUBUNIT; SIGNAL TRANSDUCTION; METABOLISM; PHYSIOLOGY;

CALCIUM; CARBACHOL; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; HEK293 CELLS; HUMANS; PHOSPHOLIPASE C DELTA; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; TRPC CATION CHANNELS;

EID: 84955450086     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1522294113     Document Type: Article

References (50)

1. Venkatachalam K, Montell C (2007) TRP channels. Annu Rev Biochem 76:387-417.
2. Otsuguro K, et al. (2008) Isoform-specific inhibition of TRPC4 channel by phosphatidylinositol 4, 5-bisphosphate. J Biol Chem 283(15):10026-10036.
3. Jeon JP, et al. (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.
4. Kim J, et al. (2014) Isoform- and receptor-specific channel property of canonical transient receptor potential (TRPC)1/4 channels. Pflugers Arch 466(3):491-504.
5. Tiruppathi C, et al. (2002) Impairment of store-operated Ca2+ entry in TRPC4(-/-) mice interferes with increase in lung microvascular permeability. Circ Res 91(1):70-76.
6. Akbulut Y, et al. (2015) (-)-Englerin A is a potent and selective activator of TRPC4 and TRPC5 calcium channels. Angew Chem Int Ed Engl 54(12):3787-3791.
7. Carson C, et al. (2015) Englerin A agonizes the TRPC4/C5 cation channels to inhibit tumor cell line proliferation. PLoS One 10(6):e0127498.
8. 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 USA 100(26):16065-16070.
9. Tsvilovskyy VV, et al. (2009) Deletion of TRPC4 and TRPC6 in mice impairs smooth muscle contraction and intestinal motility in vivo. Gastroenterology 137(4):1415-1424.
10. Weick JP, Austin Johnson M, Zhang SC (2009) Developmental regulation of human embryonic stem cell-derived neurons by calcium entry via transient receptor potential channels. Stem Cells 27(12):2906-2916.
11. Phelan KD, et al. (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(3):384-392.
12. Tian J, et al. (2014) Dual depolarization responses generated within the same lateral septal neurons by TRPC4-containing channels. Pflugers Arch 466(7):1301-1316.
13. Miller M, et al. (2011) Identification of ML204, a novel potent antagonist that selectively modulates native TRPC4/C5 ion channels. J Biol Chem 286(38):33436-33446.
14. Plant TD, Schaefer M (2005) Receptor-operated cation channels formed by TRPC4 and TRPC5. Naunyn Schmiedebergs Arch Pharmacol 371(4):266-276.
15. Obukhov AG, Nowycky MC (2004) TRPC5 activation kinetics are modulated by the scaffolding protein ezrin/radixin/moesin-binding phosphoprotein-50 (EBP50). J Cell Physiol 201(2):227-235.
16. Kim H, et al. (2012) The roles of G proteins in the activation of TRPC4 and TRPC5 transient receptor potential channels. Channels (Austin) 6(5):333-343.
17. Berridge MJ, Lipp P, Bootman MD (2000) Signal transduction. The calcium entry pas de deux. Science 287(5458):1604-1605.
18. Hofmann T, et al. (1999) Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397(6716):259-263.
19. Okada T, et al. (1999) Molecular and functional characterization of a novel mouse transient receptor potential protein homologue TRP7. Ca(2+)-permeable cation channel that is constitutively activated and enhanced by stimulation of G proteincoupled receptor. J Biol Chem 274(39):27359-27370.
20. Zhang Z, et al. (2001) Activation of Trp3 by inositol 1, 4, 5-trisphosphate receptors through displacement of inhibitory calmodulin from a common binding domain. Proc Natl Acad Sci USA 98(6):3168-3173.
21. Tang J, et al. (2001) Identification of common binding sites for calmodulin and inositol 1, 4, 5-trisphosphate receptors on the carboxyl termini of trp channels. J Biol Chem 276(24):21303-21310.
22. Vaca L, Sampieri A (2002) Calmodulin modulates the delay period between release of calcium from internal stores and activation of calcium influx via endogenous TRP1 channels. J Biol Chem 277(44):42178-42187.
23. Zhu MX (2005) Multiple roles of calmodulin and other Ca(2+)-binding proteins in the functional regulation of TRP channels. Pflugers Arch 451(1):105-115.
24. Kinoshita-Kawada M, et al. (2005) Inhibition of TRPC5 channels by Ca2+-binding protein 1 in Xenopus oocytes. Pflugers Arch 450(5):345-354.
25. Ordaz B, et al. (2005) Calmodulin and calcium interplay in the modulation of TRPC5 channel activity. Identification of a novel C-terminal domain for calcium/calmodulinmediated facilitation. J Biol Chem 280(35):30788-30796.
26. Gross SA, et al. (2009) TRPC5 is a Ca2+-activated channel functionally coupled to Ca2+-selective ion channels. J Biol Chem 284(49):34423-34432.
27. Blair NT, Kaczmarek JS, Clapham DE (2009) Intracellular calcium strongly potentiates agonist-activated TRPC5 channels. J Gen Physiol 133(5):525-546.
28. Shi J, et al. (2004)Multiple regulation by calcium of murine homologues of transient receptor potential proteins TRPC6 and TRPC7 expressed in HEK293 cells. J Physiol 561(Pt 2):415-432.
29. Kim H, et al. (2013) An essential role of PI(4, 5)P2 for maintaining the activity of the transient receptor potential canonical (TRPC)4β. Pflugers Arch 465(7):1011-1021.
30. Hossain MI, et al. (2008) Enzyme domain affects the movement of the voltage sensor in ascidian and zebrafish voltage-sensing phosphatases. J Biol Chem283(26):18248-18259.
31. Suh BC, Inoue T, Meyer T, Hille B (2006) Rapid chemically induced changes of PtdIns(4, 5)P2 gate KCNQ ion channels. Science 314(5804):1454-1457.
32. Kanki H, et al. (2001) Activation of inositol 1, 4, 5-trisphosphate receptor is essential for the opening of mouse TRP5 channels. Mol Pharmacol 60(5):989-998.
33. Foskett JK, White C, Cheung KH, Mak DO (2007) Inositol trisphosphate receptor Ca2+ release channels. Physiol Rev 87(2):593-658.
34. Suh PG, et al. (2008) Multiple roles of phosphoinositide-specific phospholipase C isozymes. BMB Rep 41(6):415-434.
35. Atwood BK, Lopez J, Wager-Miller J, Mackie K, Straiker A (2011) Expression of G protein-coupled receptors and related proteins in HEK293, AtT20, BV2, and N18 cell lines as revealed by microarray analysis. BMC Genomics 12:14.
36. Murthy KS, Zhou H, Huang J, Pentyala SN (2004) Activation of PLC-δ1 by Gi/o-coupled receptor agonists. Am J Physiol Cell Physiol 287(6):C1679-C1687.
37. Ellis MV, U S, Katan M (1995) Mutations within a highly conserved sequence present in the X region of phosphoinositide-specific phospholipase C-delta 1. Biochem J 307(Pt 1):69-75.
38. Hodson EA, Ashley CC, Hughes AD, Lymn JS (1998) Regulation of phospholipase C-δ by GTPbinding proteins-rhoA as an inhibitory modulator. Biochim Biophys Acta 1403(1):97-101.
39. Hicks SN, et al. (2008) General and versatile autoinhibition of PLC isozymes. Mol Cell 31(3):383-394.
40. Zhu Y, et al. (2015) Identification and optimization of 2-aminobenzimidazole derivatives as novel inhibitors of TRPC4 and TRPC5 channels. Br J Pharmacol 172(14):3495-3509.
41. Allen V, Swigart P, Cheung R, Cockcroft S, KatanM(1997) Regulation of inositol lipid-specific phospholipase cdelta by changes in Ca2+ ion concentrations. Biochem J 327(Pt 2):545-552.
42. Kouchi Z, et al. (2011) Phospholipase Cdelta3 regulates RhoA/Rho kinase signaling and neurite outgrowth. J Biol Chem 286(10):8459-8471.
43. Strübing C, Krapivinsky G, Krapivinsky L, Clapham DE (2001) TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron 29(3):645-655.
44. Lemonnier L, Trebak M, Putney JW, Jr (2008) Complex regulation of the TRPC3, 6 and 7 channel subfamily by diacylglycerol and phosphatidylinositol-4, 5-bisphosphate. Cell Calcium 43(5):506-514.
45. Trebak M, et al. (2009) Complex functions of phosphatidylinositol 4, 5-bisphosphate in regulation of TRPC5 cation channels. Pflugers Arch 457(4):757-769.
46. Imai Y, Itsuki K, Okamura Y, Inoue R, Mori MX (2012) A self-limiting regulation of vasoconstrictor-activated TRPC3/C6/C7 channels coupled to PI(4, 5)P2-diacylglycerol signalling. J Physiol 590(Pt 5):1101-1119.
47. Itsuki K, et al. (2014) PLC-mediated PI(4, 5)P2 hydrolysis regulates activation and inactivation of TRPC6/7 channels. J Gen Physiol 143(2):183-201.
48. Kim BJ, Kim MT, Jeon JH, Kim SJ, So I (2008) Involvement of phosphatidylinositol 4, 5-bisphosphate in the desensitization of canonical transient receptor potential 5. Biol Pharm Bull 31(9):1733-1738.
49. Miehe S, et al. (2010) The phospholipid-binding protein SESTD1 is a novel regulator of the transient receptor potential channels TRPC4 and TRPC5. J Biol Chem285(16):12426-12434.
50. Lee KP, et al. (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.