G-protein-mediated signaling in vascular smooth muscle cells — implications for vascular disease

Journal of Molecular Medicine

Volumn 93, Issue 9, 2015, Pages 973-981

  Althoff, Till F ^a   Offermanns, Stefan ^b,c  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

G protein signaling; G protein coupled receptors; Vascular smooth muscle cells

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CALPONIN; CYCLIC AMP; CYCLIC GMP; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MYOCARDIN; MYOSIN HEAVY CHAIN; MYOSIN LIGHT CHAIN; SMOOTHELIN; TERNARY COMPLEX FACTOR;

BLOOD VESSEL TONE; CARDIOVASCULAR DISEASE; CELL DIFFERENTIATION; CELL PROLIFERATION; DISEASE ASSOCIATION; ENZYME PHOSPHORYLATION; HUMAN; MOLECULAR PATHOLOGY; NONHUMAN; PLASTICITY; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CONTRACTION; SMOOTH MUSCLE RELAXATION; TRANSCRIPTION REGULATION; VASCULAR REMODELING; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; CYTOLOGY; METABOLISM; PHYSIOLOGY; VASCULAR SMOOTH MUSCLE;

ANIMALS; GTP-BINDING PROTEINS; HUMANS; MUSCLE, SMOOTH, VASCULAR; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 84942294172     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-015-1305-z     Document Type: Review

References (74)

1. Walsh MP (2011) Vascular smooth muscle myosin light chain diphosphorylation: mechanism, function, and pathological implications. IUBMB Life 63:987–1000
2. Owens GK (1995) Regulation of differentiation of vascular smooth muscle cells. Physiol Rev 75:487–517
3. Somlyo AP, Somlyo AV (1994) Signal transduction and regulation in smooth muscle. Nature 372:231–236
4. Somlyo AP, Somlyo AV (2003) Ca2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 83:1325–1358
5. Burdyga T, Paul RJ (2012) Calcium homeostatis and signaling in smooth muscle. In: Hill JA, Olson EN (eds) Muscle: fundamental biology and mechanisms of disease. Elsevier Academic Press, London/Waltham/SanDiego, pp 1155–1171
6. Puetz S, Lubomirov LT, Pfitzer G (2009) Regulation of smooth muscle contraction by small GTPases. Physiology (Bethesda) 24:342–356
7. Gohla A, Schultz G, Offermanns S (2000) Role for G(12)/G(13) in agonist-induced vascular smooth muscle cell contraction. Circ Res 87:221–227
8. Wirth A, Benyo Z, Lukasova M, Leutgeb B, Wettschureck N, Gorbey S, Orsy P, Horvath B, Maser-Gluth C, Greiner E et al (2008) G12-G13-LARG-mediated signaling in vascular smooth muscle is required for salt-induced hypertension. Nat Med 14:64–68
9. Fukuhara S, Chikumi H, Gutkind JS (2001) RGS-containing RhoGEFs: the missing link between transforming G proteins and Rho? Oncogene 20:1661–1668
10. Wuertz CM, Lorincz A, Vettel C, Thomas MA, Wieland T, Lutz S (2010) p63RhoGEF—a key mediator of angiotensin II-dependent signaling and processes in vascular smooth muscle cells. FASEB J 24:4865–4876
11. Booden MA, Siderovski DP, Der CJ (2002) Leukemia-associated Rho guanine nucleotide exchange factor promotes G alpha q-coupled activation of RhoA. Mol Cell Biol 22:4053–4061
12. Guilluy C, Bregeon J, Toumaniantz G, Rolli-Derkinderen M, Retailleau K, Loufrani L, Henrion D, Scalbert E, Bril A, Torres RM et al (2010) The Rho exchange factor Arhgef1 mediates the effects of angiotensin II on vascular tone and blood pressure. Nat Med 16:183–190
13. Rhee SG (2001) Regulation of phosphoinositide-specific phospholipase C. Annu Rev Biochem 70:281–312
14. Hanoune J, Defer N (2001) Regulation and role of adenylyl cyclase isoforms. Annu Rev Pharmacol Toxicol 41:145–174
15. Hofmann F (2004) Smooth muscle tone regulation. In: Rosenthal W (ed) Offermanns S. Encyclopedic reference of molecular pharmacology Springer-Verlag, Heidelberg, pp 870–875
16. Murthy KS (2006) Signaling for contraction and relaxation in smooth muscle of the gut. Annu Rev Physiol 68:345–374
17. Alexander MR, Owens GK (2012) Epigenetic control of smooth muscle cell differentiation and phenotypic switching in vascular development and disease. Annual Rev Physiol 74(74):13–40
18. Pipes GC, Creemers EE, Olson EN (2006) The myocardin family of transcriptional coactivators: versatile regulators of cell growth, migration, and myogenesis. Genes Dev 20:1545–1556
19. Kim C, Jun K, Lee T, Kim SS, McEnery MW, Chin H, Kim HL, Park JM, Kim DK, Jung SJ et al (2001) Altered nociceptive response in mice deficient in the alpha(1B) subunit of the voltage-dependent calcium channel. Mol Cell Neurosci 18:235–245
20. Wamhoff BR, Lynch KR, Macdonald TL, Owens GK (2008) Sphingosine-1-phosphate receptor subtypes differentially regulate smooth muscle cell phenotype. Arterioscler Thromb Vasc Biol 28:1454–1461
21. Hahn AW, Resink TJ, Kern F, Buhler FR (1992) Effects of endothelin-1 on vascular smooth muscle cell phenotypic differentiation. J Cardiovasc Pharmacol 20(Suppl 12):S33–S36
22. Morishita R, Nagata K, Ito H, Ueda H, Asano M, Shinohara H, Kato K, Asano T (2007) Expression of smooth muscle cell-specific proteins in neural progenitor cells induced by agonists of G protein-coupled receptors and transforming growth factor-beta. J Neurochem 101:1031–1040
23. Dulin NO, Orlov SN, Kitchen CM, Voyno-Yasenetskaya TA, Miano JM (2001) G-protein-coupled-receptor activation of the smooth muscle calponin gene. Biochem J 357:587–592
24. Smyth SS, Cheng HY, Miriyala S, Panchatcharam M, Morris AJ (2008) Roles of lysophosphatidic acid in cardiovascular physiology and disease. Biochim Biophys Acta 1781:563–570
25. Martin K, Weiss S, Metharom P, Schmeckpeper J, Hynes B, O’Sullivan J, Caplice N (2009) Thrombin stimulates smooth muscle cell differentiation from peripheral blood mononuclear cells via protease-activated receptor-1, RhoA, and myocardin. Circ Res 105:214–218
26. Althoff TF, Juarez JA, Troidl K, Tang C, Wang S, Wirth A, Takefuji M, Wettschureck N, Offermanns S (2012) Procontractile G protein-mediated signaling pathways antagonistically regulate smooth muscle differentiation in vascular remodeling. J Exp Med 209:2277–2290
27. Medlin MD, Staus DP, Dubash AD, Taylor JM, Mack CP (2010) Sphingosine 1-phosphate receptor 2 signals through leukemia-associated RhoGEF (LARG), to promote smooth muscle cell differentiation. Arterioscler Thromb Vasc Biol 30:1779–1786
28. Wamhoff BR, Bowles DK, McDonald OG, Sinha S, Somlyo AP, Somlyo AV, Owens GK (2004) L-type voltage-gated Ca2+ channels modulate expression of smooth muscle differentiation marker genes via a rho kinase/myocardin/SRF-dependent mechanism. Circ Res 95:406–414
29. Olson EN, Nordheim A (2010) Linking actin dynamics and gene transcription to drive cellular motile functions. Nat Rev Mol Cell Biol 11:353–365
30. Staus DP, Blaker AL, Medlin MD, Taylor JM, Mack CP (2011) Formin homology domain-containing protein 1 regulates smooth muscle cell phenotype. Arterioscler Thromb Vasc Biol 31:360–367
31. Staus DP, Blaker AL, Taylor JM, Mack CP (2007) Diaphanous 1 and 2 regulate smooth muscle cell differentiation by activating the myocardin-related transcription factors. Arterioscler Thromb Vasc Biol 27:478–486
32. Shibata R, Kai H, Seki Y, Kato S, Morimatsu M, Kaibuchi K, Imaizumi T (2001) Role of Rho-associated kinase in neointima formation after vascular injury. Circulation 103:284–289
33. Noma K, Rikitake Y, Oyama N, Yan G, Alcaide P, Liu PY, Wang H, Ahl D, Sawada N, Okamoto R et al (2008) ROCK1 mediates leukocyte recruitment and neointima formation following vascular injury. J Clin Invest 118:1632–1644
34. Ohtsu H, Suzuki H, Nakashima H, Dhobale S, Frank GD, Motley ED, Eguchi S (2006) Angiotensin II signal transduction through small GTP-binding proteins: mechanism and significance in vascular smooth muscle cells. Hypertension 48:534–540
35. Lorenz K, Schmitt JP, Schmitteckert EM, Lohse MJ (2009) A new type of ERK1/2 autophosphorylation causes cardiac hypertrophy. Nat Med 15:75–83
36. Gunaje JJ, Bahrami AJ, Schwartz SM, Daum G, Mahoney WM Jr (2011) PDGF-dependent regulation of regulator of G protein signaling-5 expression and vascular smooth muscle cell functionality. Am J Physiol Cell Physiol 301:C478–C489
37. Hendriks-Balk MC, van Loenen PB, Hajji N, Michel MC, Peters SL, Alewijnse AE (2008) S1P receptor signalling and RGS proteins; expression and function in vascular smooth muscle cells and transfected CHO cells. Eur J Pharmacol 600:1–9
38. Adams LD, Geary RL, Li J, Rossini A, Schwartz SM (2006) Expression profiling identifies smooth muscle cell diversity within human intima and plaque fibrous cap: loss of RGS5 distinguishes the cap. Arterioscler Thromb Vasc Biol 26:319–325
39. Kim MR, Jeon ES, Kim YM, Lee JS, Kim JH (2009) Thromboxane a(2) induces differentiation of human mesenchymal stem cells to smooth muscle-like cells. Stem Cells 27:191–199
40. Sachinidis A, Flesch M, Ko Y, Schror K, Bohm M, Dusing R, Vetter H (1995) Thromboxane A2 and vascular smooth muscle cell proliferation. Hypertension 26:771–780
41. Rateri DL, Moorleghen JJ, Knight V, Balakrishnan A, Howatt DA, Cassis LA, Daugherty A (2012) Depletion of endothelial or smooth muscle cell-specific angiotensin II type 1a receptors does not influence aortic aneurysms or atherosclerosis in LDL receptor deficient mice. PLoS One 7:e51483
42. Hsieh HL, Tung WH, Wu CY, Wang HH, Lin CC, Wang TS, Yang CM (2009) Thrombin induces EGF receptor expression and cell proliferation via a PKC(delta)/c-Src-dependent pathway in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 29:1594–1601
43. Lockman K, Hinson JS, Medlin MD, Morris D, Taylor JM, Mack CP (2004) Sphingosine 1-phosphate stimulates smooth muscle cell differentiation and proliferation by activating separate serum response factor co-factors. J Biol Chem 279:42422–42430
44. Alewijnse AE, Peters SL, Michel MC (2004) Cardiovascular effects of sphingosine-1-phosphate and other sphingomyelin metabolites. Br J Pharmacol 143:666–684
45. Windh RT, Lee MJ, Hla T, An S, Barr AJ, Manning DR (1999) Differential coupling of the sphingosine 1-phosphate receptors Edg-1, Edg-3, and H218/Edg-5 to the G(i), G(q), and G(12) families of heterotrimeric G proteins. J Biol Chem 274:27351–27358
46. Daum G, Grabski A, Reidy MA (2009) Sphingosine 1-phosphate: a regulator of arterial lesions. Arterioscler Thromb Vasc Biol 29:1439–1443
47. Martorell L, Martinez-Gonzalez J, Rodriguez C, Gentile M, Calvayrac O, Badimon L (2008) Thrombin and protease-activated receptors (PARs) in atherothrombosis. Thromb Haemost 99:305–315
48. Wilcox JN, Rodriguez J, Subramanian R, Ollerenshaw J, Zhong C, Hayzer DJ, Horaist C, Hanson SR, Lumsden A, Salam TA et al (1994) Characterization of thrombin receptor expression during vascular lesion formation. Circ Res 75:1029–1038
49. Nelken NA, Soifer SJ, O’Keefe J, Vu TK, Charo IF, Coughlin SR (1992) Thrombin receptor expression in normal and atherosclerotic human arteries. J Clin Invest 90:1614–1621
50. Cheng Y, Makarova N, Tsukahara R, Guo H, Shuyu E, Farrar P, Balazs L, Zhang C, Tigyi G (2009) Lysophosphatidic acid-induced arterial wall remodeling: requirement of PPARgamma but not LPA1 or LPA2 GPCR. Cell Signal 21:1874–1884
51. Osei-Owusu P, Sun X, Drenan RM, Steinberg TH, Blumer KJ (2007) Regulation of RGS2 and second messenger signaling in vascular smooth muscle cells by cGMP-dependent protein kinase. J Biol Chem 282:31656–31665
52. Tang KM, Wang GR, Lu P, Karas RH, Aronovitz M, Heximer SP, Kaltenbronn KM, Blumer KJ, Siderovski DP, Zhu Y et al (2003) Regulator of G-protein signaling-2 mediates vascular smooth muscle relaxation and blood pressure. Nat Med 9:1506–1512
53. Surks HK, Mochizuki N, Kasai Y, Georgescu SP, Tang KM, Ito M, Lincoln TM, Mendelsohn ME (1999) Regulation of myosin phosphatase by a specific interaction with cGMP- dependent protein kinase Ialpha. Science 286:1583–1587
54. Schlossmann J, Desch M (2011) IRAG and novel PKG targeting in the cardiovascular system. Am J Physiol Heart Circ Physiol 301:H672–H682
55. Zieba BJ, Artamonov MV, Jin L, Momotani K, Ho R, Franke AS, Neppl RL, Stevenson AS, Khromov AS, Chrzanowska-Wodnicka M et al (2011) The cAMP-responsive Rap1 guanine nucleotide exchange factor, epac, induces smooth muscle relaxation by down-regulation of RhoA activity. J Biol Chem 286:16681–16692
56. Rolli-Derkinderen M, Sauzeau V, Boyer L, Lemichez E, Baron C, Henrion D, Loirand G, Pacaud P (2005) Phosphorylation of serine 188 protects RhoA from ubiquitin/proteasome-mediated degradation in vascular smooth muscle cells. Circ Res 96:1152–1160
57. 2+ regulation of phosphoinositide 3-kinase C2alpha, Rho, and myosin phosphatase in vascular smooth muscle. J Pharmacol Exp Ther 320:907–916
58. Klemm DJ, Watson PA, Frid MG, Dempsey EC, Schaack J, Colton LA, Nesterova A, Stenmark KR, Reusch JE (2001) cAMP response element-binding protein content is a molecular determinant of smooth muscle cell proliferation and migration. J Biol Chem 276:46132–46141
59. Blindt R, Bosserhoff AK, vom Dahl J, Hanrath P, Schror K, Hohlfeld T, Meyer-Kirchrath J (2002) Activation of IP and EP(3) receptors alters cAMP-dependent cell migration. Eur J Pharmacol 444:31–37
60. Fetalvero KM, Martin KA, Hwa J (2007) Cardioprotective prostacyclin signaling in vascular smooth muscle. Prostagland Other Lipid Mediat 82:109–118
61. Li F, Yu X, Szynkarski CK, Meng C, Zhou B, Barhoumi R, White RE, Heaps CL, Stallone JN, Han G (2013) Activation of GPER induces differentiation and inhibition of coronary artery smooth muscle cell proliferation. PLoS One 8:e64771
62. Haas E, Bhattacharya I, Brailoiu E, Damjanovic M, Brailoiu GC, Gao X, Mueller-Guerre L, Marjon NA, Gut A, Minotti R et al (2009) Regulatory role of G protein-coupled estrogen receptor for vascular function and obesity. Circ Res 104:288–291
63. Wang WC, Pauer SH, Smith DC, Dixon MA, Disimile DJ, Panebra A, An SS, Camoretti-Mercado B, Liggett SB (2014) Targeted transgenesis identifies galphas as the bottleneck in beta2-adrenergic receptor cell signaling and physiological function in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 307:L775–L780
64. Hayashi S, Morishita R, Matsushita H, Nakagami H, Taniyama Y, Nakamura T, Aoki M, Yamamoto K, Higaki J, Ogihara T (2000) Cyclic AMP inhibited proliferation of human aortic vascular smooth muscle cells, accompanied by induction of p53 and p21. Hypertension 35:237–243
65. Palmer D, Tsoi K, Maurice DH (1998) Synergistic inhibition of vascular smooth muscle cell migration by phosphodiesterase 3 and phosphodiesterase 4 inhibitors. Circ Res 82:852–861
66. Souness JE, Hassall GA, Parrott DP (1992) Inhibition of pig aortic smooth muscle cell DNA synthesis by selective type III and type IV cyclic AMP phosphodiesterase inhibitors. Biochem Pharmacol 44:857–866
67. Graves LM, Bornfeldt KE, Raines EW, Potts BC, Macdonald SG, Ross R, Krebs EG (1993) Protein kinase a antagonizes platelet-derived growth factor-induced signaling by mitogen-activated protein kinase in human arterial smooth muscle cells. Proc Natl Acad Sci U S A 90:10300–10304
68. Indolfi C, Avvedimento EV, Di Lorenzo E, Esposito G, Rapacciuolo A, Giuliano P, Grieco D, Cavuto L, Stingone AM, Ciullo I et al (1997) Activation of cAMP-PKA signaling in vivo inhibits smooth muscle cell proliferation induced by vascular injury. Nat Med 3:775–779
69. Tsuchikane E, Fukuhara A, Kobayashi T, Kirino M, Yamasaki K, Kobayashi T, Izumi M, Otsuji S, Tateyama H, Sakurai M et al (1999) Impact of cilostazol on restenosis after percutaneous coronary balloon angioplasty. Circulation 100:21–26
70. Take S, Matsutani M, Ueda H, Hamaguchi H, Konishi H, Baba Y, Kawaratani H, Sugiura T, Iwasaka T, Inada M (1997) Effect of cilostazol in preventing restenosis after percutaneous transluminal coronary angioplasty. Am J Cardiol 79:1097–1099
71. Bernelot Moens SJ, Schnitzler GR, Nickerson M, Guo H, Ueda K, Lu Q, Aronovitz MJ, Nickerson H, Baur WE, Hansen U et al (2012) Rapid estrogen receptor signaling is essential for the protective effects of estrogen against vascular injury. Circulation 126:1993–2004
72. Li F, Li L, Qin X, Pan W, Feng F, Chen F, Zhu B, Liao D, Tanowitz H, Albanese C et al (2008) Apelin-induced vascular smooth muscle cell proliferation: the regulation of cyclin D1. Front Biosci 13:3786–3792
73. Kojima Y, Kundu RK, Cox CM, Leeper NJ, Anderson JA, Chun HJ, Ali ZA, Ashley EA, Krieg PA, Quertermous T (2010) Upregulation of the apelin-APJ pathway promotes neointima formation in the carotid ligation model in mouse. Cardiovasc Res 87:156–165
74. Iaccarino G, Smithwick LA, Lefkowitz RJ, Koch WJ (1999) Targeting Gbeta gamma signaling in arterial vascular smooth muscle proliferation: a novel strategy to limit restenosis. Proc Natl Acad Sci U S A 96:3945–3950