PDGF-dependent regulation of regulator of G protein signaling-5 expression and vascular smooth muscle cell functionality

American Journal of Physiology - Cell Physiology

Volumn 301, Issue 2, 2011, Pages

  Gunaje, Jagadambika J ^a   Bahrami, Arya J ^a   Schwartz, Stephen M ^a   Daum, Guenter ^a   Mahoney Jr , William M ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Cardiovascular signaling; G protein coupled receptor; Platelet derived growth factor; Regulator of G protein signaling; Vasoactive agonists

Indexed keywords

ANGIOTENSIN II; EPIDERMAL GROWTH FACTOR; G PROTEIN COUPLED RECEPTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR AA; PLATELET DERIVED GROWTH FACTOR BB; PLATELET DERIVED GROWTH FACTOR C; REGULATOR OF G PROTEIN SIGNALING 5; RGS PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL CELL; AORTA; ARTICLE; CANCER CELL CULTURE; CELL FUNCTION; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; IN VITRO STUDY; INHIBITION KINETICS; MUSCLE HYPERTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CONTRACTION; SMOOTH MUSCLE FIBER; UPREGULATION; VASCULAR SMOOTH MUSCLE;

ANGIOTENSIN II; ANIMALS; CELL LINE; CELL MOVEMENT; GENE EXPRESSION REGULATION; HYPERTROPHY; LIGANDS; MITOGEN-ACTIVATED PROTEIN KINASES; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PLATELET-DERIVED GROWTH FACTOR; RATS; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, PLATELET-DERIVED GROWTH FACTOR; RGS PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; VASOCONSTRICTION;

EID: 79961004841     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00348.2010     Document Type: Article

References (87)

1. Adams LD, Geary RL, Li J, Rossini A, Schwartz SM. 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, 2006.
2. Adams LD, Geary RL, McManus B, Schwartz SM. A comparison of aorta and vena cava medial message expression by cDNA array analysis identifies a set of 68 consistently differentially expressed genes, all in aortic media. Circ Res 87: 623-631, 2000.
3. Andrae J, Gallini R, Betsholtz C. Role of platelet-derived growth factors in physiology and medicine. Genes Dev 22: 1276-1312, 2008.
4. az-Flores L, Gutierrez R, Madrid JF, Varela H, Valladares F, Acosta E, Martin-Vasallo P, az-Flores L,Jr. Pericytes Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche. Histol Histopathol 24: 909-969, 2009.
5. Bansal G, Druey KM, Xie Z. R4 RGS proteins: regulation of G-protein signaling and beyond. Pharmacol Ther 116: 473-495, 2007.
6. Benjamin LE, Hemo I, Keshet E. A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development 125: 1591-1598, 1998.
7. Berger M, Bergers G, Arnold B, Hammerling GJ, Ganss R. Regulator of G-protein signaling-5 induction in pericytes coincides with active vessel remodeling during neovascularization. Blood 105: 1094-1101, 2005.
8. Berk BC, Alexander RW, Brock TA, Gimbrone MA,Jr, Webb RC. Vasoconstriction: a new activity for platelet-derived growth factor. Science 232: 87-90, 1986.
9. Berman DM, Wilkie TM, Gilman AG. GAIP and RGS4 are GTPaseactivating proteins for the Gi subfamily of G protein alpha subunits. Cell 86: 445-452, 1996.
10. Betsholtz C, Lindblom P, Gerhardt H. Role of pericytes in vascular morphogenesis. EXS: 115-125, 2005.
11. Bockaert J, Pin JP. Molecular tinkering of G protein-coupled receptors: an evolutionary success. EMBO J 18: 1723-1729, 1999.
12. Bondjers C, He L, Takemoto M, Norlin J, Asker N, Hellstrom M, Lindahl P, Betsholtz C. Microarray analysis of blood microvessels from PDGF-B and PDGF-Rbeta mutant mice identifies novel markers for brain pericytes. FASEB J 20: 1703-1705, 2006.
13. Bondjers C, Kalen M, Hellstrom M, Scheidl SJ, Abramsson A, Renner O, Lindahl P, Cho H, Kehrl J, Betsholtz C. Transcription profiling of platelet-derived growth factor-B-deficient mouse embryos identifies RGS5 as a novel marker for pericytes and vascular smooth muscle cells. Am J Pathol 162: 721-729, 2003.
14. Booz GW, Baker KM. Molecular signalling mechanisms controlling growth and function of cardiac fibroblasts. Cardiovasc Res 30: 537-543, 1995.
15. Bornfeldt KE, Graves LM, Raines EW, Igarashi Y, Wayman G, Yamamura S, Yatomi Y, Sidhu JS, Krebs EG, Hakomori S. Sphingosine-1-phosphate inhibits PDGF-induced chemotaxis of human arterial smooth muscle cells: spatial and temporal modulation of PDGF chemotactic signal transduction. J Cell Biol 130: 193-206, 1995.
16. Bornfeldt KE, Krebs EG. Crosstalk between protein kinase A and growth factor receptor signaling pathways in arterial smooth muscle. Cell Signal 11: 465-477, 1999.
17. Boss CN, Grunebach F, Brauer K, Hantschel M, Mirakaj V, Weinschenk T, Stevanovic S, Rammensee HG, Brossart P. Identification and characterization of T-cell epitopes deduced from RGS5, a novel broadly expressed tumor antigen. Clin Cancer Res 13: 3347-3355, 2007.
18. Chang YP, Liu X, Kim JD, Ikeda MA, Layton MR, Weder AB, Cooper RS, Kardia SL, Rao DC, Hunt SC, Luke A, Boerwinkle E, Chakravarti A. Multiple genes for essential-hypertension susceptibility on chromosome 1q. Am J Hum Genet 80: 253-264, 2007.
19. Chen X, Higgins J, Cheung ST, Li R, Mason V, Montgomery K, Fan ST, van de RM, So S. Novel endothelial cell markers in hepatocellular carcinoma. Mod Pathol 17: 1198-1210, 2004.
20. Cho H, Harrison K, Kehrl JH. Regulators of G protein signaling: potential drug targets for controlling cardiovascular and immune function. Curr Drug Targets Immune Endocr Metabol Disord 4: 107-118, 2004.
21. Cho H, Kozasa T, Bondjers C, Betsholtz C, Kehrl JH. Pericyte-specific expression of Rgs5: implications for PDGF and EDG receptor signaling during vascular maturation. FASEB J 17: 440-442, 2003.
22. Cho H, Park C, Hwang IY, Han SB, Schimel D, Despres D, Kehrl JH. Rgs5 targeting leads to chronic low blood pressure and a lean body habitus. Mol Cell Biol 28: 2590-2597, 2008.
23. Daub H, Weiss FU, Wallasch C, Ullrich A. Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature 379: 557-560, 1996.
24. De Vries L, Gist FM. RGS proteins: more than just GAPs for heterotrimeric G proteins. Trends Cell Biol 9: 138-144, 1999.
25. De Vries L, Zheng B, Fischer T, Elenko E, Farquhar MG. The regulator of G protein signaling family. Annu Rev Pharmacol Toxicol 40: 235-271, 2000.
26. Deaton RA, Gan Q, Owens GK. Sp1-dependent activation of KLF4 is required for PDGF-BB-induced phenotypic modulation of smooth muscle. Am J Physiol Heart Circ Physiol 296: H1027-H1037, 2009.
27. Druey KM. Bridging with GAPs: receptor communication through RGS proteins. Sci STKE 2001: RE14, 2001.
28. Ferns GA, Sprugel KH, Seifert RA, Bowen-Pope DF, Kelly JD, Murray M, Raines EW, Ross R. Relative platelet-derived growth factor receptor subunit expression determines cell migration to different dimeric forms of PDGF. Growth Factors 3: 315-324, 1990.
29. Georgoussi Z, Leontiadis L, Mazarakou G, Merkouris M, Hyde K, Hamm H. Selective interactions between G protein subunits and RGS4 with the C-terminal domains of the mu- and delta-opioid receptors regulate opioid receptor signaling. Cell Signal 18: 771-782, 2006.
30. Grayson TH, Ohms SJ, Brackenbury TD, Meaney KR, Peng K, Pittelkow YE, Wilson SR, Sandow SL, Hill CE. Vascular microarray profiling in two models of hypertension identifies Cav-1, Rgs2 and Rgs5 as antihypertensive targets. BMC Genomics 8: 404, 2007.
31. Gross V, Tank J, Obst M, Plehm R, Blumer KJ, Diedrich A, Jordan J, Luft FC. Autonomic nervous system and blood pressure regulation in RGS2-deficient mice. Am J Physiol Regul Integr Comp Physiol 288: R1134-R1142, 2005.
32. Gu S, Cifelli C, Wang S, Heximer SP. RGS proteins: identifying new GAPs in the understanding of blood pressure regulation and cardiovascular function. Clin Sci (Lond) 116: 391-399, 2009.
33. Hague C, Bernstein LS, Ramineni S, Chen Z, Minneman KP, Hepler JR. Selective inhibition of alpha1A-adrenergic receptor signaling by RGS2 association with the receptor third intracellular loop. J Biol Chem 280: 27289-27295, 2005.
34. Hamzah J, Jugold M, Kiessling F, Rigby P, Manzur M, Marti HH, Rabie T, Kaden S, Grone HJ, Hammerling GJ, Arnold B, Ganss R. Vascular normalization in Rgs5-deficient tumours promotes immune destruction. Nature 453: 410-414, 2008.
35. Hellstrom M, Kalen M, Lindahl P, Abramsson A, Betsholtz C. Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126: 3047-3055, 1999.
36. Hendriks-Balk M, van Loenen P, Hajji N, Michel M, Peters S, Alewijnse A. S1P receptor signalling and RGS proteins: expression and function in vascular smooth muscle cells and transfected CHO cells. Eur J Pharmacol 600: 1-9, 2008.
37. Hendriks-Balk MC, Peters SL, Michel MC, Alewijnse AE. Regulation of G protein-coupled receptor signalling: focus on the cardiovascular system and regulator of G protein signalling proteins. Eur J Pharmacol 585: 278-291, 2008.
38. Heximer SP, Knutsen RH, Sun X, Kaltenbronn KM, Rhee MH, Peng N, Oliveira-Dos-Santos A, Penninger JM, Muslin AJ, Steinberg TH, Wyss JM, Mecham RP, Blumer KJ. Hypertension and prolonged vasoconstrictor signaling in RGS2-deficient mice. J Clin Invest 111: 445-452, 2003.
39. Holycross BJ, Blank RS, Thompson MM, Peach MJ, Owens GK. Platelet-derived growth factor-BB-induced suppression of smooth muscle cell differentiation. Circ Res 71: 1525-1532, 1992.
40. Kalmes A, Daum G, Clowes AW. EGFR transactivation in the regulation of SMC function. Ann NY Acad Sci 947: 42-54, 2001.
41. Li H, He C, Feng J, Zhang Y, Tang Q, Bian Z, Bai X, Zhou H, Jiang H, Heximer SP, Qin M, Huang H, Liu PP, Huang C. Regulator of G protein signaling 5 protects against cardiac hypertrophy and fibrosis during biomechanical stress of pressure overload. Proc Natl Acad Sci USA 107: 13818-13823, 2010.
42. Li S, Moon JJ, Miao H, Jin G, Chen BP, Yuan S, Hu Y, Usami S, Chien S. Signal transduction in matrix contraction and the migration of vascular smooth muscle cells in three-dimensional matrix. J Vasc Res 40: 378-388, 2003.
43. Li Y, Hashim S, Anand-Srivastava MB. Angiotensin II-evoked enhanced expression of RGS2 attenuates Gi-mediated adenylyl cyclase signaling in A10 cells. Cardiovasc Res 66: 503-511, 2005.
44. Liang KW, Ting CT, Yin SC, Chen YT, Lin SJ, Liao JK, Hsu SL. Berberine suppresses MEK/ERK-dependent Egr-1 signaling pathway and inhibits vascular smooth muscle cell regrowth after in vitro mechanical injury. Biochem Pharmacol 71: 806-817, 2006.
45. Lindblom P, Gerhardt H, Liebner S, Abramsson A, Enge M, Hellstrom M, Backstrom G, Fredriksson S, Landegren U, Nystrom HC, Bergstrom G, Dejana E, Ostman A, Lindahl P, Betsholtz C. Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall. Genes Dev 17: 1835-1840, 2003.
46. Liu Y, Sinha S, McDonald OG, Shang Y, Hoofnagle MH, Owens GK. Kruppel-like factor 4 abrogates myocardin-induced activation of smooth muscle gene expression. J Biol Chem 280: 9719-9727, 2005.
47. Liu Y, Suzuki YJ, Day RM, Fanburg BL. Rho kinase-induced nuclear translocation of ERK1/ERK2 in smooth muscle cell mitogenesis caused by serotonin. Circ Res 95: 579-586, 2004.
48. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408, 2001.
49. Majack RA, Grieshaber NA, Cook CL, Weiser MC, McFall RC, Grieshaber SS, Reidy MA, Reilly CF. Smooth muscle cells isolated from the neointima after vascular injury exhibit altered responses to plateletderived growth factor and other stimuli. J Cell Physiol 167: 106-112, 1996.
50. Majesky MW. Neointima formation after acute vascular injury. Role of counteradhesive extracellular matrix proteins. Tex Heart Inst J 21: 78-85, 1994.
51. Manzur M, Ganss R. Regulator of g protein signaling 5: a new player in vascular remodeling. Trends Cardiovasc Med 19: 26-30, 2009.
52. Mehta PK, Griendling KK. Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. Am J Physiol Cell Physiol 292: C82-C97, 2007.
53. Mitchell TS, Bradley J, Robinson GS, Shima DT, Ng YS. RGS5 expression is a quantitative measure of pericyte coverage of blood vessels. Angiogenesis 11: 141-151, 2008.
54. Natarajan K, Berk BC. Crosstalk coregulation mechanisms of G proteincoupled receptors and receptor tyrosine kinases. Methods Mol Biol 332: 51-77, 2006.
55. Nisancioglu MH, Mahoney WM,Jr, Kimmel DD, Schwartz SM, Betsholtz C, Genove G. Generation and characterization of rgs5 mutant mice. Mol Cell Biol 28: 2324-2331, 2008.
56. Obst M, Tank J, Plehm R, Blumer KJ, Diedrich A, Jordan J, Luft FC, Gross V. NO-dependent blood pressure regulation in RGS2-deficient mice. Am J Physiol Regul Integr Comp Physiol 290: R1012-R1019, 2006.
57. Raines EW. PDGF and cardiovascular disease. Cytokine Growth Factor Rev 15: 237-254, 2004.
58. Riddle EL, Schwartzman RA, Bond M, Insel PA. Multi-tasking RGS proteins in the heart: the next therapeutic target? Circ Res 96: 401-411, 2005.
59. Rogers JH, Tamirisa P, Kovacs A, Weinheimer C, Courtois M, Blumer KJ, Kelly DP, Muslin AJ. RGS4 causes increased mortality and reduced cardiac hypertrophy in response to pressure overload. J Clin Invest 104: 567-576, 1999.
60. Rogers JH, Tsirka A, Kovacs A, Blumer KJ, Dorn GW, Muslin AJ. RGS4 reduces contractile dysfunction and hypertrophic gene induction in Galpha q overexpressing mice. J Mol Cell Cardiol 33: 209-218, 2001.
61. Romero DG, Plonczynski MW, Gomez-Sanchez EP, Yanes LL, Gomez-Sanchez CE. RGS2 is regulated by angiotensin II and functions as a negative feedback of aldosterone production in H295R human adrenocortical cells. Endocrinology 147: 3889-3897, 2006.
62. Ross EM, Wilkie TM. GTPase-activating proteins for heterotrimeric G proteins: regulators of G protein signaling (RGS) and RGS-like proteins. Annu Rev Biochem 69: 795-827, 2000.
63. Roy AA, Lemberg KE, Chidiac P. Recruitment of RGS2 and RGS4 to the plasma membrane by G proteins and receptors reflects functional interactions. Mol Pharmacol 64: 587-593, 2003.
64. Sapienza P, di Marzo L, Cucina A, Corvino V, Mingoli A, Giustiniani Q, Ziparo E, Cavallaro A. Release of PDGF-BB and bFGF by human endothelial cells seeded on expanded polytetrafluoroethylene vascular grafts. J Surg Res 75: 24-29, 1998.
65. Seger R, Seger D, Reszka AA, Munar ES, Eldar-Finkelman H, Dobrowolska G, Jensen AM, Campbell JS, Fischer EH, Krebs EG. Overexpression of mitogen-activated protein kinase kinase (MAPKK) and its mutants in NIH 3T3 cells. Evidence that MAPKK involvement in cellular proliferation is regulated by phosphorylation of serine residues in its kinase subdomains VII and VIII. J Biol Chem 269: 25699-25709, 1994.
66. Semplicini A, Lenzini L, Sartori M, Papparella I, Calo LA, Pagnin E, Strapazzon G, Benna C, Costa R, Avogaro A, Ceolotto G, Pessina AC. Reduced expression of regulator of G-protein signaling 2 (RGS2) in hypertensive patients increases calcium mobilization and ERK1/2 phosphorylation induced by angiotensin II. J Hypertens 24: 1115-1124, 2006.
67. Servant MJ, Giasson E, Meloche S. Inhibition of growth factor-induced protein synthesis by a selective MEK inhibitor in aortic smooth muscle cells. J Biol Chem 271: 16047-16052, 1996.
68. Shimizu RT, Blank RS, Jervis R, Lawrenz-Smith SC, Owens GK. The smooth muscle alpha-actin gene promoter is differentially regulated in smooth muscle versus non-smooth muscle cells. J Biol Chem 270: 7631-7643, 1995.
69. Sierra DA, Gilbert DJ, Householder D, Grishin NV, Yu K, Ukidwe P, Barker SA, He W, Wensel TG, Otero G, Brown G, Copeland NG, Jenkins NA, Wilkie TM. Evolution of the regulators of G-protein signaling multigene family in mouse and human. Genomics 79: 177-185, 2002.
70. Sun X, Kaltenbronn KM, Steinberg TH, Blumer KJ. RGS2 is a mediator of nitric oxide action on blood pressure and vasoconstrictor signaling. Mol Pharmacol 67: 631-639, 2005.
71. Tallquist M, Kazlauskas A. PDGF signaling in cells and mice. Cytokine Growth Factor Rev 15: 205-213, 2004.
72. Tani K, Ogushi F, Takahashi H, Kawano T, Endo T, Sone S. Thrombin stimulates platelet-derived growth factor release by alveolar macrophages in rats-significance in bleomycin-induced pulmonary fibrosis. J Med Invest 44: 59-65, 1997.
73. Thomas JA, Deaton RA, Hastings NE, Shang Y, Moehle CW, Eriksson U, Topouzis S, Wamhoff BR, Blackman BR, Owens GK. PDGF-DD, a novel mediator of smooth muscle cell phenotypic modulation, is upregulated in endothelial cells exposed to atherosclerosis-prone flow patterns. Am J Physiol Heart Circ Physiol 296: H442-H452, 2009.
74. Touyz RM, Schiffrin EL. Signal transduction mechanisms mediating the physiological and pathophysiological actions of angiotensin II in vascular smooth muscle cells. Pharmacol Rev 52: 639-672, 2000.
75. Ushio-Fukai M, Griendling KK, Becker PL, Hilenski L, Halleran S, Alexander RW. Epidermal growth factor receptor transactivation by angiotensin II requires reactive oxygen species in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 21: 489-495, 2001.
76. von TD, Armulik A, Betsholtz C. Pericytes and vascular stability. Exp Cell Res 312: 623-629, 2006.
77. Wallasch C, Crabtree JE, Bevec D, Robinson PA, Wagner H, Ullrich A. Helicobacter pylori-stimulated EGF receptor transactivation requires metalloprotease cleavage of HB-EGF. Biochem Biophys Res Commun 295: 695-701, 2002.
78. Wang C, Wu LL, Liu J, Zhang ZG, Fan D, Li L. Crosstalk between angiotensin II and platelet derived growth factor-BB mediated signal pathways in cardiomyocytes. Chin Med J (Engl) 121: 236-240, 2008.
79. Wang X, Adams LD, Pabon LM, Mahoney WM,Jr, Beaudry D, Gunaje J, Geary RL, deBlois D, Schwartz SM. RGS5, RGS4, and RGS2 expression and aortic contractibility are dynamically co-regulated during aortic bandinginduced hypertrophy. J Mol Cell Cardiol 44: 539-550, 2008.
80. Wang X, Zeng W, Soyombo AA, Tang W, Ross EM, Barnes AP, Milgram SL, Penninger JM, Allen PB, Greengard P, Muallem S. Spinophilin regulates Ca2+ signalling by binding the N-terminal domain of RGS2 and the third intracellular loop of G-protein-coupled receptors. Nat Cell Biol 7: 405-411, 2005.
81. Wetzker R, Bohmer FD. Transactivation joins multiple tracks to the ERK/MAPK cascade. Nat Rev Mol Cell Biol 4: 651-657, 2003.
82. Wieland T, Lutz S, Chidiac P. Regulators of G protein signalling: a spotlight on emerging functions in the cardiovascular system. Curr Opin Pharmacol 7: 201-207, 2007.
83. Wieland T, Mittmann C. Regulators of G-protein signalling: multifunctional proteins with impact on signalling in the cardiovascular system. Pharmacol Ther 97: 95-115, 2003.
84. Yin G, Yan C, Berk BC. Angiotensin II signaling pathways mediated by tyrosine kinases. Int J Biochem Cell Biol 35: 780-783, 2003.
85. Yoshida T, Kaestner KH, Owens GK. Conditional deletion of Kruppellike factor 4 delays downregulation of smooth muscle cell differentiation markers but accelerates neointimal formation following vascular injury. Circ Res 102: 1548-1557, 2008.
86. Zhang H, Chalothorn D, Jackson LF, Lee DC, Faber JE. Transactivation of epidermal growth factor receptor mediates catecholamineinduced growth of vascular smooth muscle. Circ Res 95: 989-997, 2004.
87. Zhou J, Moroi K, Nishiyama M, Usui H, Seki N, Ishida J, Fukamizu A, Kimura S. Characterization of RGS5 in regulation of G proteincoupled receptor signaling. Life Sci 68: 1457-1469, 2001.