MEF2B-Nox1 signaling is critical for stretch-induced phenotypic modulation of vascular smooth muscle cells

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 35, Issue 2, 2015, Pages 430-438

  Rodríguez, Andrés I ^a,c   Csányi, Gábor ^a   Ranayhossaini, Daniel J ^a   Feck, Douglas M ^a   Blose, Kory J ^b   Assatourian, Lillian ^a   Vorp, David A ^b   Pagano, Patrick J ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSIDAD DEL BÍO BÍO   (Chile)

Author keywords

MEF2B; Nox1; oxidative stress; vascular remodeling

Indexed keywords

CALPONIN; GELATINASE B; MESSENGER RNA; MYOCYTE ENHANCER FACTOR 2; OSTEOPONTIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; SMOOTHELIN; ACTIN BINDING PROTEIN; BIOLOGICAL MARKER; CALCIUM BINDING PROTEIN; CYTOSKELETON PROTEIN; ENZYME INHIBITOR; MMP9 PROTEIN, RAT; MUSCLE PROTEIN; OXIDOREDUCTASE; SMTN PROTEIN, RAT; SPP1 PROTEIN, RAT;

ARTICLE; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE SILENCING; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION; VASCULAR SMOOTH MUSCLE; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL MOTION; DRUG EFFECTS; GENETIC TRANSFECTION; GENETICS; MECHANOTRANSDUCTION; METABOLISM; PRESSORECEPTOR; RAT; RNA INTERFERENCE; SMOOTH MUSCLE FIBER; TIME; VASCULAR REMODELING;

ANIMALS; BIOMARKERS; CALCIUM-BINDING PROTEINS; CELL MOVEMENT; CELLS, CULTURED; CYTOSKELETAL PROTEINS; ENZYME INHIBITORS; MATRIX METALLOPROTEINASE 9; MECHANOTRANSDUCTION, CELLULAR; MEF2 TRANSCRIPTION FACTORS; MICROFILAMENT PROTEINS; MUSCLE PROTEINS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NADH, NADPH OXIDOREDUCTASES; OSTEOPONTIN; PHENOTYPE; PRESSORECEPTORS; RATS; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; RNA, MESSENGER; TIME FACTORS; TRANSFECTION; VASCULAR REMODELING;

EID: 84922017057     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.304936     Document Type: Article

References (58)

1. Fisher SA. Vascular smooth muscle phenotypic diversity and function. Physiol Genomics. 2010;42A:169-187. doi: 10.1152/ physiolgenomics.00111.2010.
2. Ogut O, Brozovich FV. Regulation of force in vascular smooth muscle. J Mol Cell Cardiol. 2003;35:347-355.
3. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev. 2004;84:767-801. doi: 10.1152/physrev.00041.2003.
4. Miano JM. Mammalian smooth muscle differentiation: origins, markers and transcriptional control. Results Probl Cell Differ. 2002;38:39-59.
5. Spin JM, Maegdefessel L, Tsao PS. Vascular smooth muscle cell phenotypic plasticity: focus on chromatin remodelling. Cardiovasc Res. 2012;95:147-155. doi: 10.1093/cvr/cvs098.
6. Alexander MR, Owens GK. Epigenetic control of smooth muscle cell differentiation and phenotypic switching in vascular development and disease. Annu Rev Physiol. 2012;74:13-40. doi: 10.1146/ annurev-physiol-012110-142315.
7. Gomez D, Owens GK. Smooth muscle cell phenotypic switching in atherosclerosis. Cardiovasc Res. 2012;95:156-164. doi: 10.1093/cvr/cvs115.
8. Davis-Dusenbery BN, Wu C, Hata A. Micromanaging vascular smooth muscle cell differentiation and phenotypic modulation. Arterioscler Thromb Vasc Biol. 2011;31:2370-2377. doi: 10.1161/ATVBAHA.111.226670.
9. Maul TM, Chew DW, Nieponice A, Vorp DA. Mechanical stimuli differentially control stem cell behavior: morphology, proliferation, and differentiation. Biomech Model Mechanobiol. 2011;10:939-953. doi: 10.1007/ s10237-010-0285-8.
10. Shyu KG. Cellular and molecular effects of mechanical stretch on vascular cells and cardiac myocytes. Clin Sci (Lond). 2009;116:377-389. doi: 10.1042/CS20080163.
11. Shaw A, Xu Q. Biomechanical stress-induced signaling in smooth muscle cells: an update. Curr Vasc Pharmacol. 2003;1:41-58.
12. Zhu JH, Chen CL, Flavahan S, Harr J, Su B, Flavahan NA. Cyclic stretch stimulates vascular smooth muscle cell alignment by redox-dependent activation of Notch3. Am J Physiol Heart Circ Physiol. 2011;300:H1770-H1780. doi: 10.1152/ajpheart.00535.2010.
13. Al Ghouleh I, Khoo NK, Knaus UG, et al. Oxidases and peroxidases in cardiovascular and lung disease: new concepts in reactive oxygen species signaling. Free Radic Biol Med. 2011;51:1271-1288. doi: 10.1016/j. freeradbiomed.2011.06.011.
14. Szocs K, Lassegue B, Sorescu D, Hilenski LL, Valppu L, Couse TL, Wilcox JN, Quinn MT, Lambeth JD, Griendling KK. Upregulation of nox-based nad(p)h oxidases in restenosis after carotid injury. Arterioscler Thromb Vasc Biol. 2002;22:21-27.
15. Lassègue B, San Martín A, Griendling KK. Biochemistry, physiology, and pathophysiology of NADPH oxidases in the cardiovascular system. Circ Res. 2012;110:1364-1390. doi: 10.1161/CIRCRESAHA.111.243972.
16. Katoh Y, Molkentin JD, Dave V, Olson EN, Periasamy M. MEF2B is a component of a smooth muscle-specific complex that binds an A/T-rich element important for smooth muscle myosin heavy chain gene expression. J Biol Chem. 1998;273:1511-1518.
17. Black BL, Olson EN. Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annu Rev Cell Dev Biol. 1998;14:167-196. doi: 10.1146/annurev.cellbio.14.1.167.
18. Potthoff MJ, Olson EN. MEF2: a central regulator of diverse developmental programs. Development. 2007;134:4131-4140. doi: 10.1242/ dev.008367.
19. Firulli AB, Miano JM, Bi W, Johnson AD, Casscells W, Olson EN, Schwarz JJ. Myocyte enhancer binding factor-2 expression and activity in vascular smooth muscle cells. Association with the activated phenotype. Circ Res. 1996;78:196-204.
20. Martin JF, Miano JM, Hustad CM, Copeland NG, Jenkins NA, Olson EN. A Mef2 gene that generates a muscle-specific isoform via alternative mRNA splicing. Mol Cell Biol. 1994;14:1647-1656.
21. Katsuyama M, Ozgur Cevik M, Arakawa N, Kakehi T, Nishinaka T, Iwata K, Ibi M, Matsuno K, Yabe-Nishimura C. Myocyte enhancer factor 2B is involved in the inducible expression of NOX1/NADPH oxidase, a vascular superoxide-producing enzyme. FEBS J. 2007;274:5128-5136. doi: 10.1111/j.1742-4658.2007.06034.x.
22. Ranayhossaini DJ, Rodriguez AI, Sahoo S, Chen BB, Mallampalli RK, Kelley EE, Csanyi G, Gladwin MT, Romero G, Pagano PJ. Selective recapitulation of conserved and nonconserved regions of putative NOXA1 protein activation domain confers isoform-specific inhibition of Nox1 oxidase and attenuation of endothelial cell migration. J Biol Chem. 2013;288:36437-36450. doi: 10.1074/jbc.M113.521344.
23. Al Ghouleh I, Frazziano G, Rodriguez AI, Csányi G, Maniar S, St Croix CM, Kelley EE, Egaña LA, Song GJ, Bisello A, Lee YJ, Pagano PJ. Aquaporin 1, Nox1, and Ask1 mediate oxidant-induced smooth muscle cell hypertrophy. Cardiovasc Res. 2013;97:134-142. doi: 10.1093/cvr/cvs295.
24. Filippov S, Koenig GC, Chun TH, Hotary KB, Ota I, Bugge TH, Roberts JD, Fay WP, Birkedal-Hansen H, Holmbeck K, Sabeh F, Allen ED, Weiss SJ. MT1-matrix metalloproteinase directs arterial wall invasion and neointima formation by vascular smooth muscle cells. J Exp Med. 2005;202:663-671. doi: 10.1084/jem.20050607.
25. Lehti K, Rose NF, Valavaara S, Weiss SJ, Keski-Oja J. MT1-MMP promotes vascular smooth muscle dedifferentiation through LRP1 processing. J Cell Sci. 2009;122(Pt 1):126-135. doi: 10.1242/jcs.035279.
26. Kirby BJ. Micro-and Nanoscale Fluid Mechanics: Transport in Microfluidic Devices. Cambridge University Press: Cambridge, United Kingdom; 2010.
27. Mongardon N, Dyson A, Singer M. Pharmacological optimization of tissue perfusion. Br J Anaesth. 2009;103:82-88. doi: 10.1093/bja/aep135.
28. Levy BI, Schiffrin EL, Mourad JJ, Agostini D, Vicaut E, Safar ME, Struijker-Boudier HA. Impaired tissue perfusion: a pathology common to hypertension, obesity, and diabetes mellitus. Circulation. 2008;118:968-976. doi: 10.1161/CIRCULATIONAHA.107.763730.
29. Ardanaz N, Pagano PJ. Hydrogen peroxide as a paracrine vascular mediator: regulation and signaling leading to dysfunction. Exp Biol Med (Maywood). 2006;231:237-251.
30. Cascino T, Csanyi G, Al Ghouleh I, Montezano AC, Touyz RM, Haurani MJ, Pagano PJ. Adventitia-derived hydrogen peroxide impairs relaxation of the rat carotid artery via smooth muscle cell p38 mitogen-activated protein kinase. Antioxid Redox Signal. 2011;15:1507-1515. doi: 10.1089/ ars.2010.3631.
31. Lassègue B, Clempus RE. Vascular NAD(P)H oxidases: specific features, expression, and regulation. Am J Physiol Regul Integr Comp Physiol. 2003;285:R277-R297. doi: 10.1152/ajpregu.00758.2002.
32. Sedeek M, Hébert RL, Kennedy CR, Burns KD, Touyz RM. Molecular mechanisms of hypertension: role of Nox family NADPH oxidases. Curr Opin Nephrol Hypertens. 2009;18:122-127. doi: 10.1097/ MNH.0b013e32832923c3.
33. Azumi H, Inoue N, Takeshita S, Rikitake Y, Kawashima S, Hayashi Y, Itoh H, Yokoyama M. Expression of NADH/NADPH oxidase p22phox in human coronary arteries. Circulation. 1999;100:1494-1498.
34. Ohmine T, Miwa Y, Takahashi-Yanaga F, Morimoto S, Maehara Y, Sasaguri T. The involvement of aldosterone in cyclic stretch-mediated activation of NADPH oxidase in vascular smooth muscle cells. Hypertens Res. 2009;32:690-699. doi: 10.1038/hr.2009.76.
35. Wang BW, Chang H, Shyu KG. Regulation of resistin by cyclic mechanical stretch in cultured rat vascular smooth muscle cells. Clin Sci (Lond). 2010;118:221-230.
36. Chen Q, Li W, Quan Z, Sumpio BE. Modulation of vascular smooth muscle cell alignment by cyclic strain is dependent on reactive oxygen species and P38 mitogen-activated protein kinase. J Vasc Surg. 2003;37:660-668. doi: 10.1067/mva.2003.95.
37. Paravicini TM, Montezano AC, Yusuf H, Touyz RM. Activation of vascular p38MAPK by mechanical stretch is independent of c-Src and NADPH oxidase: influence of hypertension and angiotensin II. J Am Soc Hypertens. 2012;6:169-178. doi: 10.1016/j.jash.2012.01.002.
38. Csányi G, Yao M, Rodríguez AI, Al Ghouleh I, Sharifi-Sanjani M, Frazziano G, Huang X, Kelley EE, Isenberg JS, Pagano PJ. Thrombospondin-1 regulates blood flow via CD47 receptor-mediated activation of NADPH oxidase 1 Arterioscler Thromb Vasc Biol. 2012;32:2966-2973. doi: 10.1161/ ATVBAHA.112.300031.
39. Wang L, Zhang J, Fu W, Guo D, Jiang J, Wang Y. Association of smooth muscle cell phenotypes with extracellular matrix disorders in thoracic aortic dissection. J Vasc Surg. 2012;56:1698-709, 1709.e1. doi: 10.1016/j. jvs.2012.05.084.
40. Wang L, Zheng J, Du Y, Huang Y, Li J, Liu B, Liu CJ, Zhu Y, Gao Y, Xu Q, Kong W, Wang X. Cartilage oligomeric matrix protein maintains the contractile phenotype of vascular smooth muscle cells by interacting with alpha(7)beta(1) integrin. Circ Res. 2010;106:514-525. doi: 10.1161/ CIRCRESAHA.109.202762.
41. Tsai MC, Chen L, Zhou J, Tang Z, Hsu TF, Wang Y, Shih YT, Peng HH, Wang N, Guan Y, Chien S, Chiu JJ. Shear stress induces synthetic-tocontractile phenotypic modulation in smooth muscle cells via peroxisome proliferator-activated receptor alpha/delta activations by prostacyclin released by sheared endothelial cells. Circ Res. 2009;105:471-480. doi: 10.1161/CIRCRESAHA.109.193656.
42. Rensen SS, Doevendans PA, van Eys GJ. Regulation and characteristics of vascular smooth muscle cell phenotypic diversity. Neth Heart J. 2007;15:100-108.
43. Nobrega MA, Shiozawa M, Koike G, Jacob HJ, Miano JM. Gene structure and chromosomal mapping of the rat smooth muscle calponin gene. Mamm Genome. 2000;11:115-119.
44. Rensen SS, Niessen PM, Long X, Doevendans PA, Miano JM, van Eys GJ. Contribution of serum response factor and myocardin to transcriptional regulation of smoothelins. Cardiovasc Res. 2006;70:136-145. doi: 10.1016/j.cardiores.2005.12.018.
45. Christen T, Bochaton-Piallat ML, Neuville P, Rensen S, Redard M, van Eys G, Gabbiani G. Cultured porcine coronary artery smooth muscle cells. A new model with advanced differentiation. Circ Res. 1999;85: 99-107.
46. Rangrez AY, Massy ZA, Metzinger-Le Meuth V, Metzinger L. miR-143 and miR-145: molecular keys to switch the phenotype of vascular smooth muscle cells. Circ Cardiovasc Genet. 2011;4:197-205. doi: 10.1161/ CIRCGENETICS.110.958702.
47. Boettger T, Beetz N, Kostin S, Schneider J, Krüger M, Hein L, Braun T. Acquisition of the contractile phenotype by murine arterial smooth muscle cells depends on the Mir143/145 gene cluster. J Clin Invest. 2009;119:2634-2647. doi: 10.1172/JCI38864.
48. Matchkov VV, Kudryavtseva O, Aalkjaer C. Intracellular Ca2+ signalling and phenotype of vascular smooth muscle cells. Basic Clin Pharmacol Toxicol. 2012;110:42-48. doi: 10.1111/j.1742-7843.2011.00818.x.
49. Beamish JA, He P, Kottke-Marchant K, Marchant RE. Molecular regulation of contractile smooth muscle cell phenotype: implications for vascular tissue engineering. Tissue Eng Part B Rev. 2010;16:467-491. doi: 10.1089/ten.TEB.2009.0630.
50. Jacobsen JC, Holstein-Rathlou NH. A life under pressure: circumferential stress in the microvascular wall. Basic Clin Pharmacol Toxicol. 2012;110:26-34. doi: 10.1111/j.1742-7843.2011.00796.x.
51. Liu B, Qu MJ, Qin KR, Li H, Li ZK, Shen BR, Jiang ZL. Role of cyclic strain frequency in regulating the alignment of vascular smooth muscle cells in vitro. Biophys J. 2008;94:1497-1507. doi: 10.1529/ biophysj.106.098574.
52. Lai CF, Seshadri V, Huang K, Shao JS, Cai J, Vattikuti R, Schumacher A, Loewy AP, Denhardt DT, Rittling SR, Towler DA. An osteopontin-NADPH oxidase signaling cascade promotes pro-matrix metalloproteinase 9 activation in aortic mesenchymal cells. Circ Res. 2006;98:1479-1489. doi: 10.1161/01.RES.0000227550.00426.60.
53. Koullias GJ, Ravichandran P, Korkolis DP, Rimm DL, Elefteriades JA. Increased tissue microarray matrix metalloproteinase expression favors proteolysis in thoracic aortic aneurysms and dissections. Ann Thorac Surg. 2004;78:2106-10; discussion 2110. doi: 10.1016/j. athoracsur.2004.05.088.
54. Patel MI, Melrose J, Ghosh P, Appleberg M. Increased synthesis of matrix metalloproteinases by aortic smooth muscle cells is implicated in the etiopathogenesis of abdominal aortic aneurysms. J Vasc Surg. 1996;24:82-92.
55. Xu S, Shriver AS, Jagadeesha DK, Chamseddine AH, Szocs K, Weintraub NL, Griendling KK, Bhalla RC, Miller FJ Jr. Increased expression of Nox1 in neointimal smooth muscle cells promotes activation of matrix metalloproteinase-9. J Vasc Res. 2012;49:242-248. doi: 10.1159/000332958.
56. Singh NK, Kundumani-Sridharan V, Kumar S, Verma SK, Kotla S, Mukai H, Heckle MR, Rao GN. Protein kinase N1 is a novel substrate of NFATc1-mediated cyclin D1-CDK6 activity and modulates vascular smooth muscle cell division and migration leading to inward blood vessel wall remodeling. J Biol Chem. 2012;287:36291-36304. doi: 10.1074/jbc. M112.361220.
57. Chae CU, Lee RT, Rifai N, Ridker PM. Blood pressure and inflammation in apparently healthy men. Hypertension. 2001;38:399-403.
58. Liu S, Li Y, Zhang Z, Xie F, Xu Q, Huang X, Huang J, Li C. α1-Adrenergic receptors mediate combined signals initiated by mechanical stretch stress and norepinephrine leading to accelerated mouse vein graft atherosclerosis. J Vasc Surg. 2013;57:1645-56, 1656.e1. doi: 10.1016/j.jvs.2012.09.061.