Distinctive G Protein-Dependent Signaling by Protease-Activated Receptor 2 (PAR2) in Smooth Muscle: Feedback Inhibition of RhoA by cAMP-Independent PKA

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Sriwai, Wimolpak ^a   Mahavadi, Sunila ^a   Al Shboul, Othman ^a   Grider, John R ^a   Murthy, Karnam S ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (5 CHLORO 1 NAPHTHALENESULFONYL)HEXAHYDRO 1H 1,4 DIAZEPINE; 1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; EXOENZYME C3; GUANINE NUCLEOTIDE BINDING PROTEIN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEINASE ACTIVATED RECEPTOR 2; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; ADENYLATE CYCLASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE PHOSPHODIESTERASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; NEGATIVE FEEDBACK; NONHUMAN; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; PROTEIN LOCALIZATION; RABBIT; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CONTRACTION; SMOOTH MUSCLE FIBER; STOMACH MUSCLE; ANIMAL; CYTOLOGY; ENZYME ACTIVATION; ENZYMOLOGY; LEPORIDAE; METABOLISM; MUSCLE CONTRACTION; SMOOTH MUSCLE;

CLOSTRIDIUM BOTULINUM; ORYCTOLAGUS CUNICULUS;

ADENYLYL CYCLASES; ANIMALS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; GTP-BINDING PROTEINS; MUSCLE CONTRACTION; MUSCLE, SMOOTH; NF-KAPPA B; PHOSPHOINOSITIDE PHOSPHOLIPASE C; RABBITS; RECEPTOR, PAR-2; SIGNAL TRANSDUCTION;

EID: 84879168646     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066743     Document Type: Article

References (43)

1. Nystedt S, Emilsson K, Wahlestedt C, Sundelin J, (1994) Molecular cloning of a potential proteinase activated receptor. Proc Natl Acad Sci USA 91: 9208-9212.
2. Xu WF, Andersen H, Whitmore TE, Presnell SR, Yee DP, et al. (1998) Cloning and characterization of human protease-activated receptor 4. Proc Natl Acad Sci USA 95: 6642-6646.
3. Bohm SK, Kong W, Bromme D, Smeekens SP, Anderson DC, et al. (1996) Molecular cloning, expression and potential functions of the human proteinase-activated receptor-2. Biochem J 314 (Pt 3): 1009-1016.
4. Bunnett NW, (2006) Protease-activated receptors: how proteases signal to cells to cause inflammation and pain. Semin Thromb Hemost 32(1): 39-48.
5. Corvera CU, Dery O, McConalogue K, Gamp P, Thoma M, et al. (1999) Thrombin and mast cell typtase regulate guinea-pig myenteric neurons through proteinase-activated receptors-1 and-2. J Physiol 517(Pt3): 741-756.
6. Nishikawa H, Kawai K, Nishimura S, Tanaka S, Araki H, et al. (2002) Suppression by protease-activated receptor-2 activation of gastric acid secretion in rats. Eur J Pharmacol 447: 87-90.
7. Kawabata A, Matsunami M, Sekiguchi F, (2008) Gastrointestinal roles for proteinase-activated receptors in health and disease. Br J Pharmacol 153(1): S230-40.
8. Gao C, Liu S, Hu HZ, Gao N, Kim GY, et al. (2002) Serine proteases excite myenteric neurons through protease-activated receptors in guinea pig small intestine. Gastroenterology 123: 1554-1564.
9. Shea-Donohue T, Notari L, Stiltz J, Sun R, Madden KB, et al. (2010) Role of enteric nerves in immune-mediated changes in protease-activated receptor 2 effects on gut function. Neurogastroenterol Motil 22(10): 1138-e291.
10. Dulon S, Cande C, Bunnett NW, Hollenberg MD, Chignard M, et al. (2003) Proteinase-activated receptor 2 and human lung epithelial cells disarming by neutrophil serine proteinases. Am J Respir Cell Mol Biol 28(3): 339-346.
11. Schmidlin F, Amadesi S, Vidil R, Trevisani M, Martinet N, et al. (2001) Expression and function of proteinase-activated receptor 2 in human bronchial smooth muscle. Am J Respir Crit Care Med 164: 1276-1281.
12. Steinhoff M, Vergnolle N, Young SH, Tognetto M, Amadesi S, et al. (2000) Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nature Medicine 6: 151-158.
13. Kawabata A, Kuroda R, Nagata N, Kawao N, Masuko T, et al. (2001) In vivo evidence that protease-activated receptors 1 and 2 modulate gastrointestinal transit in the mouse. Br J Pharmacol 133(8): 1213-8.
14. Cocks TM, Sozzi V, Moffatt JD, Selemidis S, (1999) Protease-activated receptors mediate apamin-sensitive relaxation of mouse and guinea pig gastrointestinal smooth muscle. Gastroenterology 116: 586-592.
15. Kawabata A, Kuroda R, Nishikawa H, Kawai K, (1999) Modulation by protease-activated receptors of the rat duodenal motility in vitro:possible mechanisms underlying the evoked contraction and relaxation. Br J Pharmacol 128: 865-872.
16. Mule F, Baffi MC, Cerra MC, (2002) Dual effect mediated by protease-activated receptors on the mechanical activity of rat colon. Br J Pharmacol 136: 367-374.
17. Murthy KS, Makhlouf GM, (1991) Phosphoinositide metabolism in intestinal smooth muscel: preferential production of Ins(1,4,5)P3 in circular muscle cells. Am J Physiol 261: G945-951.
18. Murthy KS, Makhlouf GM, (1996) Opioid mu, delta and kappa receptor induced activation of phospholipase C beta 3 and inhibition of adenylyl cyclase is mediated by Gi2 and G(o) in smooth muscle. Mol Pharmacol 50: 870-877.
19. Murthy KS, Zhou H, Grider JR, Brautigan DL, Eto M, et al. (2003) Differential signalling by muscarinic receptors in smooth muscle: m2-mediated inactivation of myosin light chain kinase via Gi3, Cdc42/Rac1 and p21-activated kinase 1 pathway, and m3-mediated MLC20 (20 kDa regulatory light chain of myosin II) phosphorylation via Rho-associated kinase/myosin phosphatase targeting subunit 1 and protein kinase C/CPI-17 pathway. Biochem J 374: 145-55.
20. Huang J, Zhou H, Mahavadi S, Sriwai W, Murthy KS, (2007) Inhibition of Galpha q dependent PLC-beta1 activity by PKG and PKA is mediated by phosphorylation of RGS4 and GRK2. Am J Physiol Cell Physiol 292: C200-208.
21. Zhou H, Murthy KS, (2004) Distinctive G protein-dependent signaling in smooth muscle by sphingosine 1-phosphate receptors S1P1 and S1P2. Am J Physiol Cell Physiol 286: C1130-1138.
22. Gilchrist A, Bunemann M, Li A, Hosey MM, Hamm HE, (1999) A dominat -negative strategy for studying roles of G proens in vivo. J. Biol. Chem. 274: 6610-6616.
23. Gilchrist A, Vanhauwe J, Li A, Thoma TT, Voyno-Yasenetskaya T, et al. (2001) Gα minigenes expressing C-terminal peptides serve a specific inhibitors of thrombin-mediated endothelail activation. J. Biol. Chem. 276: 25672-25679.
24. Okamoto T, Ikezu T, Murayama Y, Ogata E, Nishimoto I, (1992) Measurement of GTP gamma S binding to specific G proteins in membranes using G protein antibodies. FEBS Lett 305: 125-128.
25. Berridge MJ, Downes CP, Hanley MR, (1982) Lithium amplifies agonist dependent phosphatidylinositol responses in brain and salivary glands. Biochem J 206: 587-595.
26. Murthy KS, Zhou H, Grider JR, Makhlouf GM, (2003) Inhibition of sustained smooth muscle contraction by PKA and PKG preferentially mediated by phosphorylation of RhoA. Am J Physiol Gastrointest Liver Physiol 284(6): G1006-16.
27. Huang J, Mahavadi S, Sriwai W, Hu W, Murthy KS, (2006) Gi coupled receptors mediate phosphorylation of CPI-17 and MLC20 via preferential activation of the PI3K/ILK pathway. Biochem J 396: 193-200.
28. De Godoy MA, Rattan S, (2011) Role of Rho kinase in the functional and dysfunctional tonic smooth muscles. Trends Pharmacol Sci 32(7): 384-93.
29. Somlyo AP, Somlyo AV, (2003) Ca2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 83(4): 1325-58.
30. Garrido R, Segura B, Zhang W, Mulholland M, (2002) Presence of functionally active protease-activated receptors 1 and 2 in myenteric glia. J Neurochem 83: 556-564.
31. Cottrell GS, Amadesi S, Grady EF, Bunnett NW, (2004) Trypsin IV, a novel agonist of protease-activated receptors 2 and 4. J Biol Chem 279: 13532-13539.
32. Kunzelmann K, Schreiber R, Konig J, Mall M, (2002) Ion transport induced by proteinase-activated receptors (PAR2) in colon and airways. Cell Biochem Biophys 36: 209-214.
33. D'Andrea MR, Derian CK, Leturcq D, Baker SM, Brunmark A, et al. (1998) Characterization of protease-activated receptor 2 immunoreactivity in normal human tissues. J Histochem Cytochem 46: 157-164.
34. Kawabata A, (2003) Physiological functions of protease activated receptor 2. Nippon Yakurigaku Zasshi 121: 411-420.
35. Ubl JJ, Grishina ZV, Sukhomlin TK, Welte T, Sedehizade F, et al. (2002) Human bronchial epithelial cells express PAR-2 with different sensitivity to thermolysin. Am J Physiol Lung Cell Mol Physiol 282(6): L1339-134.
36. Murthy KS, (2006) Signaling for contraction and relaxation in smooth muscle of the gut Annu Rev Physiol. (68): 345-74.
37. Siehler S, (2009) Regulation of RhoGEF proteins by G12/13 coupled receptors. Br J Pharmacol 158(1): 41-49.
38. Wang Q, Liu M, Kozasa T, Rothstein JD, Sternweis PC, et al. (2004) Thrombin and lysophosphatidic acid receptors utilize distinct RhoGEFs in prostate cancer cells. J Biol Chem 279(28): 28831-28834.
39. Profirovic J, Gorovoy M, Niu J, Pavlovic S, Voyno-Yasenetskaya T, (2005) A novel mechanism of G protein-dependent phosphorylation of vasodilator-stimulated phosphoprotein. J Biol Chem 280(38): 32866-76.
40. Salinthone S, Singer CA, Gerthoffer WT, (2004) Inflammatory gene expression by human colonic smooth muscle cells. Am J Physiol Gastrointest Liver Physiol. 287: G627-637.
41. Singer CA, Salinthone S, Baker KJ, Gerthoffer WT, (2004) Synthesis of immune modulators by smooth muscles. Bioessays 26: 646-655.
42. Shi X-Z, Sarna SK, (2005) Transcriptional regulation of inflammatory mediators secreted by human colonic circular smooth muscle cells. Am J Physiol Gastrointest Liver Physiol 289: G274-284.
43. Hu W, Li F, Mahavadi M, Murthy KS, (2008) Interleukin-1β up-regulates RGS4 through the canonical IKK2/IkBα/NF-kB pathway in rabbit colonic smooth muscle. Biochem. J. 412: 35-48.