RGS5 promotes arterial growth during arteriogenesis

EMBO Molecular Medicine

Volumn 6, Issue 8, 2014, Pages 1075-1089

  Arnold, Caroline ^a   Feldner, Anja ^a   Pfisterer, Larissa ^a   Hödebeck, Maren ^a   Troidl, Kerstin ^b   Genové, Guillem ^c   Wieland, Thomas ^a   Hecker, Markus ^a   Korff, Thomas ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

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

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Arteriogenesis; G protein; Remodelling; RGS5; Vascular smooth muscle cells

Indexed keywords

CALCIUM; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; MYOCARDIN; NITRIC OXIDE; PROTEIN; REGULATOR OF G PROTEIN SIGNALLING 5; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SMOOTH MUSCLE ACTIN; UNCLASSIFIED DRUG; RGS PROTEIN; RGS5 PROTEIN, MOUSE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTERIAL GROWTH; ARTERIOLE; ARTERY LIGATION; BLOOD PRESSURE MEASUREMENT; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL CULTURE; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FEMORAL ARTERY; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TISSUE GROWTH; UPREGULATION; VASCULAR SMOOTH MUSCLE; WILD TYPE; ANIMAL; GENETICS; GROWTH, DEVELOPMENT AND AGING; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

ANIMALS; ARTERIOLES; CELL PROLIFERATION; GENE KNOCKDOWN TECHNIQUES; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; GTP-BINDING PROTEIN ALPHA SUBUNITS, GQ-G11; MICE; MICE, KNOCKOUT; MYOCYTES, SMOOTH MUSCLE; RGS PROTEINS; RHOA GTP-BINDING PROTEIN;

EID: 84905376739     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.15252/emmm.201403864     Document Type: Review

References (66)

1. Adams LD, Geary RL, McManus B, Schwartz SM (2000) 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
2. 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
3. Banai S, Wolf Y, Golomb G, Pearle A, Waltenberger J, Fishbein I, Schneider A, Gazit A, Perez L, Huber R et al (1998) PDGF-receptor tyrosine kinase blocker AG1295 selectively attenuates smooth muscle cell growth in vitro and reduces neointimal formation after balloon angioplasty in swine. Circulation 97: 1960-1969
4. Berger M, Bergers G, Arnold B, Hammerling GJ, Ganss R (2005) Regulator of G-protein signaling-5 induction in pericytes coincides with active vessel remodeling during neovascularization. Blood 105: 1094-1101
5. Berman DM, Wilkie TM, Gilman AG (1996) GAIP and RGS4 are GTPase-activating proteins for the Gi subfamily of G protein alpha subunits. Cell 86: 445-452
6. Busse R, Trogisch G, Bassenge E (1985) The role of endothelium in the control of vascular tone. Basic Res Cardiol 80: 475-490
7. Cattaruzza M, Eberhardt I, Hecker M (2001) Mechanosensitive transcription factors involved in endothelin B receptor expression. J Biol Chem 276: 36999-37003
8. Cho H, Kozasa T, Bondjers C, Betsholtz C, Kehrl JH (2003) Pericyte-specific expression of Rgs5: implications for PDGF and EDG receptor signaling during vascular maturation. FASEB J 17: 440-442
9. Cho H, Park C, Hwang IY, Han SB, Schimel D, Despres D, Kehrl JH (2008) Rgs5 targeting leads to chronic low blood pressure and a lean body habitus. Mol Cell Biol 28: 2590-2597
10. Dai X, Faber JE (2010) Endothelial nitric oxide synthase deficiency causes collateral vessel rarefaction and impairs activation of a cell cycle gene network during arteriogenesis. Circ Res 106: 1870-1881
11. Davis-Dusenbery BN, Wu C, Hata A (2011) Micromanaging vascular smooth muscle cell differentiation and phenotypic modulation. Arterioscler Thromb Vasc Biol 31: 2370-2377
12. Demicheva E, Hecker M, Korff T (2008) Stretch-induced activation of the transcription factor activator protein-1 controls monocyte chemoattractant protein-1 expression during arteriogenesis. Circ Res 103: 477-484
13. Dubroca C, You D, Levy BI, Loufrani L, Henrion D (2005) Involvement of RhoA/Rho kinase pathway in myogenic tone in the rabbit facial vein. Hypertension 45: 974-979
14. Eitenmuller I, Volger O, Kluge A, Troidl K, Barancik M, Cai WJ, Heil M, Pipp F, Fischer S, Horrevoets AJ et al (2006) The range of adaptation by collateral vessels after femoral artery occlusion. Circ Res 99: 656-662
15. Gross V, Tank J, Obst M, Plehm R, Blumer KJ, Diedrich A, Jordan J, Luft FC (2005) Autonomic nervous system and blood pressure regulation in RGS2-deficient mice. Am J Physiol Regul Integr Comp Physiol 288: R1134-R1142
16. Gu S, Cifelli C, Wang S, Heximer SP (2009) RGS proteins: identifying new GAPs in the understanding of blood pressure regulation and cardiovascular function. Clin Sci 116: 391-399
17. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B (1998) A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 95: 2509-2514
18. Heerkens EH, Izzard AS, Heagerty AM (2007) Integrins, vascular remodeling, and hypertension. Hypertension 49: 1-4
19. Heil M, Schaper W (2004) Pathophysiology of collateral development. Coron Artery Dis 15: 373-378
20. Heil M, Ziegelhoeffer T, Wagner S, Fernandez B, Helisch A, Martin S, Tribulova S, Kuziel WA, Bachmann G, Schaper W (2004) Collateral artery growth (arteriogenesis) after experimental arterial occlusion is impaired in mice lacking CC-chemokine receptor-2. Circ Res 94: 671-677
21. Heil M, Eitenmuller I, Schmitz-Rixen T, Schaper W (2006) Arteriogenesis versus angiogenesis: similarities and differences. J Cell Mol Med 10: 45-55
22. Hepler JR, Berman DM, Gilman AG, Kozasa T (1997) RGS4 and GAIP are GTPase-activating proteins for Gq alpha and block activation of phospholipase C beta by gamma-thio-GTP-Gq alpha. Proc Natl Acad Sci USA 94: 428-432
23. Heximer SP, Knutsen RH, Sun X, Kaltenbronn KM, Rhee MH, Peng N, Oliveira-dos-Santos A, Penninger JM, Muslin AJ, Steinberg TH et al (2003) Hypertension and prolonged vasoconstrictor signaling in RGS2-deficient mice. J Clin Invest 111: 1259
24. Holobotovskyy V, Manzur M, Tare M, Burchell J, Bolitho E, Viola H, Hool LC, Arnolda LF, McKitrick DJ, Ganss R (2013) Regulator of G-protein signaling 5 controls blood pressure homeostasis and vessel wall remodeling. Circ Res 112: 781-791
25. Ketsawatsomkron P, Lorca RA, Keen HL, Weatherford ET, Liu X, Pelham CJ, Grobe JL, Faraci FM, England SK, Sigmund CD (2012) PPARgamma regulates resistance vessel tone through a mechanism involving RGS5-mediated control of protein kinase C and BKCa channel activity. Circ Res 111: 1446-1458
26. Kumar A, Hoover JL, Simmons CA, Lindner V, Shebuski RJ (1997) Remodeling and neointimal formation in the carotid artery of normal and P-selectin-deficient mice. Circulation 96: 4333-4342
27. Kumar A, Lindner V (1997) Remodeling with neointima formation in the mouse carotid artery after cessation of blood flow. Arterioscler Thromb Vasc Biol 17: 2238-2244
28. Li J, Adams LD, Wang X, Pabon L, Schwartz SM, Sane DC, Geary RL (2004) Regulator of G protein signaling 5 marks peripheral arterial smooth muscle cells and is downregulated in atherosclerotic plaque. J Vasc Surg 40: 519-528
29. Liu WF, Nelson CM, Tan JL, Chen CS (2007) Cadherins, RhoA, and Rac1 are differentially required for stretch-mediated proliferation in endothelial versus smooth muscle cells. Circ Res 101: e44-e52
30. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408
31. Matsumoto Y, Uwatoku T, Oi K, Abe K, Hattori T, Morishige K, Eto Y, Fukumoto Y, Nakamura K, Shibata Y et al (2004) Long-term inhibition of Rho-kinase suppresses neointimal formation after stent implantation in porcine coronary arteries: involvement of multiple mechanisms. Arterioscler Thromb Vasc Biol 24: 181-186
32. Meier P, Hemingway H, Lansky AJ, Knapp G, Pitt B, Seiler C (2012) The impact of the coronary collateral circulation on mortality: a meta-analysis. Eur Heart J 33: 614-621
33. Mills PA, Huetteman DA, Brockway BP, Zwiers LM, Gelsema AJ, Schwartz RS, Kramer K (2000) A new method for measurement of blood pressure, heart rate, and activity in the mouse by radiotelemetry. J Appl Physiol 88: 1537-1544
34. Mittmann C, Chung CH, Hoppner G, Michalek C, Nose M, Schuler C, Schuh A, Eschenhagen T, Weil J, Pieske B et al (2002) Expression of ten RGS proteins in human myocardium: functional characterization of an upregulation of RGS4 in heart failure. Cardiovasc Res 55: 778-786
35. Mohamed JS, Boriek AM (2010) Stretch augments TGF-beta1 expression through RhoA/ROCK1/2, PTK, and PI3K in airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 299: L413-L424
36. Nisancioglu MH, Mahoney WM Jr, Kimmel DD, Schwartz SM, Betsholtz C, Genove G (2008) Generation and characterization of rgs5 mutant mice. Mol Cell Biol 28: 2324-2331
37. Numaguchi K, Eguchi S, Yamakawa T, Motley ED, Inagami T (1999) Mechanotransduction of rat aortic vascular smooth muscle cells requires RhoA and intact actin filaments. Circ Res 85: 5-11
38. Pagiatakis C, Gordon JW, Ehyai S, McDermott JC (2012) A novel RhoA/ROCK-CPI-17-MEF2C signaling pathway regulates vascular smooth muscle cell gene expression. J Biol Chem 287: 8361-8370
39. Parmacek MS (2007) Myocardin-related transcription factors: critical coactivators regulating cardiovascular development and adaptation. Circ Res 100: 633-644
40. Pfisterer L, Feldner A, Hecker M, Korff T (2012) Hypertension impairs myocardin function - a novel mechanism facilitating arterial remodeling. Cardiovasc Res 96: 120-129
41. 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
42. Roman DL, Talbot JN, Roof RA, Sunahara RK, Traynor JR, Neubig RR (2007) Identification of small-molecule inhibitors of RGS4 using a high-throughput flow cytometry protein interaction assay. Mol Pharmacol 71: 169-175
43. Ross EM, Wilkie TM (2000) GTPase-activating proteins for heterotrimeric G proteins: regulators of G protein signaling (RGS) and RGS-like proteins. Annu Rev Biochem 69: 795-827
44. Schaper W (2012) Collateral vessels reduce mortality. Eur Heart J 33: 564-566
45. Scholz D, Ito W, Fleming I, Deindl E, Sauer A, Wiesnet M, Busse R, Schaper J, Schaper W (2000) Ultrastructure and molecular histology of rabbit hind-limb collateral artery growth (arteriogenesis). Virchows Arch 436: 257-270
46. 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
47. Tamirisa P, Blumer KJ, Muslin AJ (1999) RGS4 inhibits G-protein signaling in cardiomyocytes. Circulation 99: 441-447
48. 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
49. Teramoto H, Crespo P, Coso OA, Igishi T, Xu N, Gutkind JS (1996) The small GTP-binding protein rho activates c-Jun N-terminal kinases/stress-activated protein kinases in human kidney 293T cells. Evidence for a Pak-independent signaling pathway. J Biol Chem 271: 25731-25734
50. Tokudome T, Kishimoto I, Horio T, Arai Y, Schwenke DO, Hino J, Okano I, Kawano Y, Kohno M, Miyazato M et al (2008) Regulator of G-protein signaling subtype 4 mediates antihypertrophic effect of locally secreted natriuretic peptides in the heart. Circulation 117: 2329-2339
51. Troidl K, Ruding I, Cai WJ, Mucke Y, Grossekettler L, Piotrowska I, Apfelbeck H, Schierling W, Volger OL, Horrevoets AJ et al (2009a) Actin-binding rho activating protein (Abra) is essential for fluid shear stress-induced arteriogenesis. Arterioscler Thromb Vasc Biol 29: 2093-2101
52. Troidl K, Tribulova S, Cai WJ, Eitenmuller I, Wustrack H, Schierling W, Troidl C, Schmitz-Rixen T, Schaper W (2009b) Effects of endogenous NO and of DETA NONOate in Arteriogenesis. J Cardiovasc Pharmacol 55: 153-160
53. Unthank JL, Nixon JC, Dalsing MC (1996) Inhibition of NO synthase prevents acute collateral artery dilation in the rat hindlimb. J Surg Res 61: 463-468
54. Waltenberger J, Uecker A, Kroll J, Frank H, Mayr U, Bjorge JD, Fujita D, Gazit A, Hombach V, Levitzki A et al (1999) A dual inhibitor of platelet-derived growth factor beta-receptor and Src kinase activity potently interferes with motogenic and mitogenic responses to PDGF in vascular smooth muscle cells. A novel candidate for prevention of vascular remodeling. Circ Res 85: 12-22
55. 2+ channels modulate expression of smooth muscle differentiation marker genes via a rho kinase/myocardin/SRF-dependent mechanism. Circ Res 95: 406-414
56. Wang X, Adams LD, Pabon LM, Mahoney WM Jr, Beaudry D, Gunaje J, Geary RL, Deblois D, Schwartz SM (2008) RGS5, RGS4, and RGS2 expression and aortic contractibility are dynamically co-regulated during aortic banding-induced hypertrophy. J Mol Cell Cardiol 44: 539-550
57. Wieland T, Mittmann C (2003) Regulators of G-protein signalling: multifunctional proteins with impact on signalling in the cardiovascular system. Pharmacol Ther 97: 95-115
58. Wieland T, Lutz S, Chidiac P (2007) Regulators of G protein signalling: a spotlight on emerging functions in the cardiovascular system. Curr Opin Pharmacol 7: 201-207
59. Wojtowicz A, Babu SS, Li L, Gretz N, Hecker M, Cattaruzza M (2010) Zyxin mediation of stretch-induced gene expression in human endothelial cells. Circ Res 107: 898-902
60. 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
61. Yang Z, Balenga N, Cooper PR, Damera G, Edwards R, Brightling CE, Panettieri RA Jr, Druey KM (2012) RGS5 inhibits bronchial smooth muscle contraction in severe asthma. Am J Respir Cell Mol Biol 46: 823-832
62. Yu J, deMuinck ED, Zhuang Z, Drinane M, Kauser K, Rubanyi GM, Qian HS, Murata T, Escalante B, Sessa WC (2005) Endothelial nitric oxide synthase is critical for ischemic remodeling, mural cell recruitment, and blood flow reserve. Proc Natl Acad Sci USA 102: 10999-11004
63. Zhang S, Han J, Sells MA, Chernoff J, Knaus UG, Ulevitch RJ, Bokoch GM (1995) Rho family GTPases regulate p38 mitogen-activated protein kinase through the downstream mediator Pak1. J Biol Chem 270: 23934-23936
64. Zhang W, Huang Y, Gunst SJ (2012) The small GTPase RhoA regulates the contraction of smooth muscle tissues by catalyzing the assembly of cytoskeletal signaling complexes at membrane adhesion sites. J Biol Chem 287: 33996-34008
65. Zhao S, Suciu A, Ziegler T, Moore JE Jr, Burki E, Meister JJ, Brunner HR (1995) Synergistic effects of fluid shear stress and cyclic circumferential stretch on vascular endothelial cell morphology and cytoskeleton. Arterioscler Thromb Vasc Biol 15: 1781-1786
66. Zuckerbraun BS, Shapiro RA, Billiar TR, Tzeng E (2003) RhoA influences the nuclear localization of extracellular signal-regulated kinases to modulate p21Waf/Cip1 expression. Circulation 108: 876-881