Smooth muscle specific rac1 deficiency induces hypertension by preventing p116RIP3-dependent RhoA Inhibition

Journal of the American Heart Association

Volumn 3, Issue 3, 2014, Pages

  André, Gwennan ^a,b   Sandoval, Juan E ^a,b   Retailleau, Kevin ^c   Loufrani, Laurent ^c   Toumaniantz, Gilles ^a,b   Offermanns, Stefan ^d   Rolli Derkinderen, Malvyne ^a,b   Loirand, Gervaise ^a,b   Sauzeau, Vincent ^a,b  

^a L INSTITUT DU THORAX   (France)

^b UNIVERSITÉ DE NANTES   (France)

^c UNIVERSITÉ D'ANGERS   (France)

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

Author keywords

Blood pressure; Hypertension; Nitric oxide; Signal transduction; Vasoconstriction

Indexed keywords

BINDING PROTEIN; CYCLIC GMP; FASUDIL; NITRIC OXIDE; PHOSPHODIESTERASE V; PROTEIN P116RIP3; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; NEUROPEPTIDE; P116RIP PROTEIN, MOUSE; RAC1 PROTEIN, MOUSE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME DEFICIENCY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; ENZYME REACTIVATION; GENE DELETION; GENE LOCATION; HYPERTENSION; MALE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; RAC1 GENE; SIGNAL TRANSDUCTION; SYSTOLIC BLOOD PRESSURE; VASCULAR SMOOTH MUSCLE; VASODILATATION; ANIMAL; BLOOD PRESSURE; DEFICIENCY; ECHOCARDIOGRAPHY; KNOCKOUT MOUSE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BLOOD PRESSURE; ECHOCARDIOGRAPHY; HYPERTENSION; MALE; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; MUSCLE, SMOOTH, VASCULAR; NEUROPEPTIDES; RAC1 GTP-BINDING PROTEIN; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; VASODILATION;

EID: 84922226051     PISSN: None     EISSN: 20479980     Source Type: Journal    
DOI: 10.1161/JAHA.114.000852     Document Type: Article

References (63)

1. Bustelo XR, Ojeda V, Barreira M, Sauzeau V, Castro-Castro A. Rac-ing to the plasma membrane: the long and complex work commute of rac1 during cell signaling. Small GTPases. 2012;3:60-66.
2. Bustelo XR, Sauzeau V, Berenjeno IM. Gtp-binding proteins of the rho/rac family: regulation, effectors and functions in vivo. BioEssays. 2007;29:356-370.
3. Heasman SJ, Ridley AJ. Mammalian rho gtpases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol. 2008;9:690-701.
4. Ridley AJ, Hall A. The small gtp-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell. 1992;70:389-399.
5. Guo F, Debidda M, Yang L, Williams DA, Zheng Y. Genetic deletion of rac1 gtpase reveals its critical role in actin stress fiber formation and focal adhesion complex assembly. J Biol Chem. 2006;281:18652-18659.
6. Ohta Y, Hartwig JH, Stossel TP. Filgap, a rho-and rock-regulated gap for rac binds filamin a to control actin remodelling. Nat Cell Biol. 2006;8:803-814.
7. Guilluy C, Garcia-Mata R, Burridge K. Rho protein crosstalk: another social network? Trends Cell Biol. 2011;21:718-726.
8. Machacek M, Hodgson L, Welch C, Elliott H, Pertz O, Nalbant P, Abell A, Johnson GL, Hahn KM, Danuser G. Coordination of rho gtpase activities during cell protrusion. Nature. 2009;461:99-103.
9. Rolli-Derkinderen M, Toumaniantz G, Pacaud P, Loirand G. Rhoa phosphorylation induces rac1 release from guanine dissociation inhibitor alpha and stimulation of vascular smooth muscle cell migration. Mol Cell Biol. 2010; 30:4786-4796.
10. Laufs U, Liao JK. Post-transcriptional regulation of endothelial nitric oxide synthase mrna stability by rho gtpase. J Biol Chem. 1998;273:24266-24271.
11. Wolfrum S, Dendorfer A, Rikitake Y, Stalker TJ, Gong Y, Scalia R, Dominiak P, Liao JK. Inhibition of rho-kinase leads to rapid activation of phosphatidylinositol 3-kinase/protein kinase akt and cardiovascular protection. Arterioscler Thromb Vasc Biol. 2004;24:1842-1847.
12. Sawada N, Salomone S, Kim HH, Kwiatkowski DJ, Liao JK. Regulation of endothelial nitric oxide synthase and postnatal angiogenesis by rac1. Circ Res. 2008;103:360-368.
13. Selvakumar B, Hess DT, Goldschmidt-Clermont PJ, Stamler JS. Co-regulation of constitutive nitric oxide synthases and nadph oxidase by the small gtpase rac. FEBS Lett. 2008;582:2195-2202.
14. Adamson RH, Sarai RK, Clark JF, Altangerel A, Thirkill TL, Curry FE. Attenuation by sphingosine-1-phosphate of rat microvessel acute permeability response to bradykinin is rapidly reversible. Am J Physiol Heart Circ Physiol. 2012;302: H1929-H1935.
15. Monaghan-Benson E, Burridge K. The regulation of vascular endothelial growth factor-induced microvascular permeability requires rac and reactive oxygen species. J Biol Chem. 2009;284:25602-25611.
16. Gavard J, Gutkind JS. Vegf controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of ve-cadherin. Nat Cell Biol. 2006; 8:1223-1234.
17. Loirand G, Guerin P, Pacaud P. Rho kinases in cardiovascular physiology and pathophysiology. Circ Res. 2006;98:322-334.
18. Loirand G, Pacaud P. The role of rho protein signaling in hypertension. Nat Rev Cardiol. 2010;7:637-647.
19. Shirai HAM, Eguchi S. Small gtp-binding proteins and mitogen-activated protein kinases as promising therapeutic targets of vascular remodeling. Curr Opin Nephrol Hypertens. 2007;16:111-115.
20. Sanders LC, Matsumura F, Bokoch GM, de Lanerolle P. Inhibition of myosin light chain kinase by p21-activated kinase. Science. 1999;283:2083-2085.
21. Wirth A, Schroeter M, Kock-Hauser C, Manser E, Chalovich JM, De Lanerolle P, Pfitzer G. Inhibition of contraction and myosin light chain phosphorylation in guinea-pig smooth muscle by p21-activated kinase 1. J Physiol. 2003;549: 489-500.
22. Foster DB, Shen LH, Kelly J, Thibault P, Van Eyk JE, Mak AS. Phosphorylation of caldesmon by p21-activated kinase. Implications for the ca(2+) sensitivity of smooth muscle contraction. J Biol Chem. 2000;275:1959-1965.
23. Rahman A, Davis B, Lovdahl C, Hanumaiah VT, Feil R, Brakebusch C, Arner A. The small gtpase rac1 is required for smooth muscle contraction. J Physiol 2014;592:(Pt 5)915-926.
24. Sauzeau V, Sevilla MA, Rivas-Elena JV, de Alava E, Montero MJ, Lopez-Novoa JM, Bustelo XR. Vav3 proto-oncogene deficiency leads to sympathetic hyperactivity and cardiovascular dysfunction. Nat Med. 2006;12:841-845.
25. Sauzeau V, Jerkic M, Lopez-Novoa JM, Bustelo XR. Loss of vav2 protooncogene causes tachycardia and cardiovascular disease in mice. Mol Biol Cell. 2007;18:943-952.
26. Wirth A, Benyo Z, Lukasova M, Leutgeb B, Wettschureck N, Gorbey S, Orsy P, Horvath B, Maser-Gluth C, Greiner E, Lemmer B, Schutz G, Gutkind JS, Offermanns S. G12-G13-larg-mediated signaling in vascular smooth muscle is required for salt-induced hypertension. Nat Med. 2008;14:64-68.
27. Guilluy C, Bregeon J, Toumaniantz G, Rolli-Derkinderen M, Retailleau K, Loufrani L, Henrion D, Scalbert E, Bril A, Torres RM, Offermanns S, Pacaud P, Loirand G. The rho exchange factor arhgef1 mediates the effects of angiotensin ii on vascular tone and blood pressure. Nat Med. 2010;16:183-190.
28. Mills PA, Huetteman DA, Brockway BP, Zwiers LM, Gelsema AJ, Schwartz RS, Kramer K. A new method for measurement of blood pressure, heart rate, and activity in the mouse by radiotelemetry. J Appl Physiol. 2000;88:1537-1544.
29. Loufrani L, Levy BI, Henrion D. Defect in microvascular adaptation to chronic changes in blood flow in mice lacking the gene encoding for dystrophin. Circ Res. 2002;91:1183-1189.
30. Guilluy C, Dubash AD, Garcia-Mata R. Analysis of rhoa and rho gef activity in whole cells and the cell nucleus. Nat Protoc. 2011;6:2050-2060.
31. Gayard M, Guilluy C, Rousselle A, Viollet B, Henrion D, Pacaud P, Loirand G, Rolli-Derkinderen M. Ampk alpha 1-induced rhoa phosphorylation mediates vasoprotective effect of estradiol. Arterioscler Thromb Vasc Biol. 2011;31:2634-2642.
32. Lifton RP, Gharavi AG, Geller DS. Molecular mechanisms of human hypertension. Cell. 2001;104:545-556.
33. Sauzeau V, Le Jeune H, Cario-Toumaniantz C, Smolenski A, Lohmann SM, Bertoglio J, Chardin P, Pacaud P, Loirand G. Cyclic gmp-dependent protein kinase signaling pathway inhibits rhoa-induced ca2+ sensitization of contraction in vascular smooth muscle. J Biol Chem. 2000;275:21722-21729.
34. Sauzeau V, Sevilla MA, Montero MJ, Bustelo XR. The rho/rac exchange factor vav2 controls nitric oxide-dependent responses in mouse vascular smooth muscle cells. J Clin Invest. 2010;120:315-330.
35. Surks HK, Richards CT, Mendelsohn ME. Myosin phosphatase-rho interacting protein. A new member of the myosin phosphatase complex that directly binds rhoa. J Biol Chem. 2003;278:51484-51493.
36. Shesely EG, Maeda N, Kim HS, Desai KM, Krege JH, Laubach VE, Sherman PA, Sessa WC, Smithies O. Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci USA. 1996;93:13176-13181.
37. Stauss HM, Godecke A, Mrowka R, Schrader J, Persson PB. Enhanced blood pressure variability in enos knockout mice. Hypertension. 1999;33:1359-1363.
38. Van Vliet BN, Chafe LL, Montani JP. Characteristics of 24 h telemetered blood pressure in enos-knockout and c57bl/6j control mice. J Physiol. 2003;549:313-325.
39. Pfeifer A, Klatt P, Massberg S, Ny L, Sausbier M, Hirneiss C, Wang GX, Korth M, Aszodi A, Andersson KE, Krombach F, Mayerhofer A, Ruth P, Fassler R, Hofmann F. Defective smooth muscle regulation in cgmp kinase i-deficient mice. EMBO J. 1998;17:3045-3051.
40. Isabelle M, Simonet S, Ragonnet C, Sansilvestri-Morel P, Clavreul N, Vayssettes-Courchay C, Verbeuren TJ. Chronic reduction of nitric oxide level in adult spontaneously hypertensive rats induces aortic stiffness similar to old spontaneously hypertensive rats. J Vasc Res. 2012;49:309-318.
41. Nakmareong S, Kukongviriyapan U, Pakdeechote P, Kukongviriyapan V, Kongyingyoes B, Donpunha W, Prachaney P, Phisalaphong C. Tetrahydrocurcumin alleviates hypertension, aortic stiffening and oxidative stress in rats with nitric oxide deficiency. Hypertens Res. 2012;35:418-425.
42. Figueiredo VN, Yugar-Toledo JC, Martins LC, Martins LB, de Faria AP, de Haro Moraes C, Sierra C, Coca A, Moreno H. Vascular stiffness and endothelial dysfunction: correlations at different levels of blood pressure. Blood Press 2012;21:31-38.
43. Sindler AL, Fleenor BS, Calvert JW, Marshall KD, Zigler ML, Lefer DJ, Seals DR. Nitrite supplementation reverses vascular endothelial dysfunction and large elastic artery stiffness with aging. Aging Cell. 2011;10:429-437.
44. Wilkinson IB, Franklin SS, Cockcroft JR. Nitric oxide and the regulation of large artery stiffness: from physiology to pharmacology. Hypertension. 2004;44:112-116.
45. Brandes RP, Fleming I, Busse R. Endothelial aging. Cardiovasc Res. 2005;66:286-294.
46. Takefuji M, Asano H, Mori K, Amano M, Kato K, Watanabe T, Morita Y, Katsumi A, Itoh T, Takenawa T, Hirashiki A, Izawa H, Nagata K, Hirayama H, Takatsu F, Naoe T, Yokota M, Kaibuchi K. Mutation of arhgap9 in patients with coronary spastic angina. J Hum Genet. 2010;55:42-49.
47. Nowicki PT, Flavahan S, Hassanain H, Mitra S, Holland S, Goldschmidt-Clermont PJ, Flavahan NA. Redox signaling of the arteriolar myogenic response. Circ Res. 2001;89:114-116.
48. Hassanain HH, Gregg D, Marcelo ML, Zweier JL, Souza HP, Selvakumar B, Ma Q, Moustafa-Bayoumi M, Binkley PF, Flavahan NA, Morris M, Dong C, Goldschmidt-Clermont PJ. Hypertension caused by transgenic overexpression of rac1. Antioxid Redox Signal. 2007;9:91-100.
49. Guo D, Zhang JJ, Huang XY. A new rac/pak/gc/cgmp signaling pathway. Mol Cell Biochem. 2010;334:99-103.
50. Jennissen K, Siegel F, Liebig-Gonglach M, Hermann MR, Kipschull S, van Dooren S, Kunz WS, Fassler R, Pfeifer A. A vasp-rac-soluble guanylyl cyclase pathway controls cgmp production in adipocytes. Sci Signal. 2012;5:ra62.
51. Baek EB, Kim SJ. Mechanisms of myogenic response: Ca(2+)-dependent and-independent signaling. J Smooth Muscle Res. 2011;47:55-65.
52. Hilgers RH, Webb RC. Molecular aspects of arterial smooth muscle contraction: focus on rho. Exp Biol Med (Maywood). 2005;230:829-835.
53. Wang Y, Zheng XR, Riddick N, Bryden M, Baur W, Zhang X, Surks HK. Rock isoform regulation of myosin phosphatase and contractility in vascular smooth muscle cells. Circ Res. 2009;104:531-540.
54. Somlyo AP, Somlyo AV. Ca2+ sensitivity of smooth muscle and nonmuscle myosin ii: modulated by g proteins, kinases, and myosin phosphatase. Physiol Rev. 2003;83:1325-1358.
55. Bolz SS, Vogel L, Sollinger D, Derwand R, de Wit C, Loirand G, Pohl U. Nitric oxide-induced decrease in calcium sensitivity of resistance arteries is attributable to activation of the myosin light chain phosphatase and antagonized by the rhoa/rho kinase pathway. Circulation. 2003;107: 3081-3087.
56. Sauzeau V, Le Jeune H, Cario-Toumaniantz C, Vaillant N, Gadeau AP, Desgranges C, Scalbert E, Chardin P, Pacaud P, Loirand G. P2y(1), p2y(2), p2y(4), and p2y(6) receptors are coupled to rho and rho kinase activation in vascular myocytes. Am J Physiol Heart Circ Physiol. 2000;278:H1751-H1761.
57. Priviero FB, Jin LM, Ying Z, Teixeira CE, Webb RC. Up-regulation of the rhoa/rho-kinase signaling pathway in corpus cavernosum from endothelial nitricoxide synthase (nos), but not neuronal nos, null mice. J Pharmacol Exp Ther. 2010;333:184-192.
58. Williams J, Bogwu J, Oyekan A. The role of the rhoa/rho-kinase signaling pathway in renal vascular reactivity in endothelial nitric oxide synthase null mice. J Hypertens. 2006;24:1429-1436.
59. Gebbink MF, Kranenburg O, Poland M, van Horck FP, Houssa B, Moolenaar WH. Identification of a novel, putative rho-specific gdp/gtp exchange factor and a rhoa-binding protein: control of neuronal morphology. J Cell Biol. 1997;137:1603-1613.
60. Mulder J, Poland M, Gebbink MF, Calafat J, Moolenaar WH, Kranenburg O. P116rip is a novel filamentous actin-binding protein. J Biol Chem. 2003;278:27216-27223.
61. Koga Y, Ikebe M. P116rip decreases myosin ii phosphorylation by activating myosin light chain phosphatase and by inactivating rhoa. J Biol Chem. 2005;280:4983-4991.
62. Mulder J, Ariaens A, van Horck FP, Moolenaar WH. Inhibition of rhoa-mediated srf activation by p116rip. FEBS Lett. 2005;579:6121-6127.
63. Vallenius T, Vaahtomeri K, Kovac B, Osiceanu AM, Viljanen M, Makela TP. An association between nuak2 and mrip reveals a novel mechanism for regulation of actin stress fibers. J Cell Sci. 2011;124:384-393.