Embryonic stem cell differentiation into smooth muscle cells is mediated by Nox4-produced H2O2

American Journal of Physiology - Cell Physiology

Volumn 296, Issue 4, 2009, Pages

  Xiao, Qingzhong ^a   Luo, Zhenling ^a   Pepe, Anna Elena ^a   Margariti, Andriani ^a   Zeng, Lingfang ^a   Xu, Qingbo ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Myocardin; NADPH oxidase; Serum response factor

Indexed keywords

COLLAGEN TYPE 4; HYDROGEN PEROXIDE; MYOCARDIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SERUM RESPONSE FACTOR; TRANSFORMING GROWTH FACTOR BETA1;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL LINE; CELL MATURATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; GENE ACTIVATION; GENE EXPRESSION; GENE INDUCTION; GENE OVEREXPRESSION; GENE TRANSLOCATION; GENETIC MARKER; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; IMMUNOFLUORESCENCE; IN VIVO STUDY; MOUSE; MUSCLE CONTRACTILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; SMOOTH MUSCLE FIBER; TISSUE ENGINEERING; UPREGULATION; VASCULAR TISSUE; VASCULARIZATION; WESTERN BLOTTING;

ANIMALS; AUTOCRINE COMMUNICATION; CELL DIFFERENTIATION; CELL LINE; COLLAGEN TYPE IV; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HYDROGEN PEROXIDE; MICE; MYOCYTES, SMOOTH MUSCLE; NADPH OXIDASE; NUCLEAR PROTEINS; PHENOTYPE; PHOSPHORYLATION; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RNA INTERFERENCE; RNA, SMALL INTERFERING; SERUM RESPONSE FACTOR; TIME FACTORS; TRANS-ACTIVATORS; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA1; UP-REGULATION;

EID: 65649128653     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00442.2008     Document Type: Article

References (41)

1. Anilkumar N, Weber R, Zhang M, Brewer A, Shah AM. Nox4 and Nox2 NADPH oxidases mediate distinct cellular redox signaling responses to agonist stimulation. Arterioscler Thromb Vasc Biol 28: 1347-1354, 2008.
2. Cave AC, Brewer AC, Narayanapanicker A, Ray R, Grieve DJ, Walker S, Shah AM. NADPH oxidases in cardiovascular health and disease. Antioxid Redox Signal 8: 691-728, 2006. (Pubitemid 44043102)
3. Chen J, Kitchen CM, Streb JW, Miano JM. Myocardin: a component of a molecular switch for smooth muscle differentiation. J Mol Cell Cardiol 34: 1345-1356, 2002. (Pubitemid 35244412)
4. Chen S, Crawford M, Day RM, Briones VR, Leader JE, Jose PA, Lechleider RJ. RhoA modulates Smad signaling during transforming growth factor-beta-induced smooth muscle differentiation. J Biol Chem 281: 1765-1770, 2006. (Pubitemid 43752494)
5. Clempus RE, Griendling KK. Reactive oxygen species signaling in vascular smooth muscle cells. Cardiovasc Res 71: 216-225, 2006.
6. Clempus RE, Sorescu D, Dikalova AE, Pounkova L, Jo P, Sorescu GP, Schmidt HH, Lassegue B, Griendling KK. Nox4 is required for maintenance of the differentiated vascular smooth muscle cell phenotype. Arterioscler Thromb Vasc Biol 27: 42-48, 2007. (Pubitemid 46360379)
7. Cucoranu I, Clempus R, Dikalova A, Phelan PJ, Ariyan S, Dikalov S, Sorescu D. NAD(P)H oxidase 4 mediates transforming growth factor-beta1-induced differentiation of cardiac fibroblasts into myofibroblasts. Circ Res 97: 900-907, 2005. (Pubitemid 41552675)
8. Deliri H, McNamara CA. Nox4 regulation of vascular smooth muscle cell differentiation marker gene expression. Arterioscler Thromb Vasc Biol 27: 12-14, 2007. (Pubitemid 46360376)
9. Doi H, Iso T, Yamazaki M, Akiyama H, Kanai H, Sato H, Kawai- Kowase K, Tanaka T, Maeno T, Okamoto E, Arai M, Kedes L, Kurabayashi M. HERP1 inhibits myocardin-induced vascular smooth muscle cell differentiation by interfering with SRF binding to CArG box. Arterioscler Thromb Vasc Biol 25: 2328-2334, 2005. (Pubitemid 41552650)
10. Du KL, Ip HS, Li J, Chen M, Dandre F, Yu W, Lu MM, Owens GK, Parmacek MS. Myocardin is a critical serum response factor cofactor in the transcriptional program regulating smooth muscle cell differentiation. Mol Cell Biol 23: 2425-2437, 2003. (Pubitemid 36351024)
11. Forman HJ, Fukuto JM, Torres M. Redox signaling: thiol chemistry defines which reactive oxygen and nitrogen species can act as second messengers. Am J Physiol Cell Physiol 287: C246-C256, 2004. (Pubitemid 38955213)
12. Gawaziuk JP, Sheikh F, Cheng ZQ, Cattini PA, Stephens NL. Transforming growth factor-beta as a differentiating factor for cultured smooth muscle cells. Eur Respir J 30: 643-652, 2007.
13. Gutierrez J, Ballinger SW, Darley-Usmar VM, Landar A. Free radicals, mitochondria, and oxidized lipids: the emerging role in signal transduction in vascular cells. Circ Res 99: 924-932, 2006. (Pubitemid 44657795)
14. Hilenski LL, Clempus RE, Quinn MT, Lambeth JD, Griendling KK. Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 24: 677-683, 2004.
15. Hinson JS, Medlin MD, Lockman K, Taylor JM, Mack CP. Smooth muscle cell-specific transcription is regulated by nuclear localization of the myocardin-related transcription factors. Am J Physiol Heart Circ Physiol 292: H1170-H1180, 2007. (Pubitemid 46246971)
16. Hu Y, Zhang Z, Torsney E, Afzal AR, Davison F, Metzler B, Xu Q. Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice. J Clin Invest 113: 1258-1265, 2004. (Pubitemid 39069924)
17. Jeon ES, Moon HJ, Lee MJ, Song HY, Kim YM, Bae YC, Jung JS, Kim JH. Sphingosylphosphorylcholine induces differentiation of human mesenchymal stem cells into smooth-muscle-like cells through a TGF-beta-dependent mechanism. J Cell Sci 119: 4994-5005, 2006.
18. Lassegue B, Clempus RE. Vascular NAD(P)H oxidases: specific features, expression, and regulation. Am J Physiol Regul Integr Comp Physiol 285: R277-R297, 2003. (Pubitemid 36898897)
19. Li S, Wang DZ, Wang Z, Richardson JA, Olson EN. The serum response factor coactivator myocardin is required for vascular smooth muscle development. Proc Natl Acad Sci USA 100: 9366-9370, 2003. (Pubitemid 37033934)
20. Long X, Creemers EE, Wang DZ, Olson EN, Miano JM. Myocardin is a bifunctional switch for smooth versus skeletal muscle differentiation. Proc Natl Acad Sci USA 104: 16570-16575, 2007. (Pubitemid 350211059)
21. Martyn KD, Frederick LM, von Loehneysen K, Dinauer MC, Knaus UG. Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell Signal 18: 69-82, 2006. (Pubitemid 41415716)
22. McDonald OG, Owens GK. Programming smooth muscle plasticity with chromatin dynamics. Circ Res 100: 1428-1441, 2007.
23. McDonald OG, Wamhoff BR, Hoofnagle MH, Owens GK. Control of SRF binding to CArG box chromatin regulates smooth muscle gene expression in vivo. J Clin Invest 116: 36-48, 2006.
24. Miano JM, Long X, Fujiwara K. Serum response factor: master regulator of the actin cytoskeleton and contractile apparatus. Am J Physiol Cell Physiol 292: C70-C81, 2007. (Pubitemid 46115122)
25. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84: 767-801, 2004.
26. Ross JJ, Hong Z, Willenbring B, Zeng L, Isenberg B, Lee EH, Reyes M, Keirstead SA, Weir EK, Tranquillo RT, Verfaillie CM. Cytokine-induced differentiation of multipotent adult progenitor cells into functional smooth muscle cells. J Clin Invest 116: 3139-3149, 2006.
27. Rotmans JI, Heyligers JM, Verhagen HJ, Velema E, Nagtegaal MM, de Kleijn DP, de Groot FG, Stroes ES, Pasterkamp G. In vivo cell seeding with anti-CD34 antibodies successfully accelerates endothelialization but stimulates intimal hyperplasia in porcine arteriovenous expanded polytetrafluoroethylene grafts. Circulation 112: 12-18, 2005. (Pubitemid 40962563)
28. Sorescu D, Weiss D, Lassegue B, Clempus RE, Szocs K, Sorescu GP, Valppu L, Quinn MT, Lambeth JD, Vega JD, Taylor WR, Griendling KK. Superoxide production and expression of nox family proteins in human atherosclerosis. Circulation 105: 1429-1435, 2002. (Pubitemid 34263273)
29. Su B, Mitra S, Gregg H, Flavahan S, Chotani MA, Clark KR, Goldschmidt-Clermont PJ, Flavahan NA. Redox regulation of vascular smooth muscle cell differentiation. Circ Res 89: 39-46, 2001. (Pubitemid 34135490)
30. Sumimoto H, Miyano K, Takeya R. Molecular composition and regulation of the Nox family NAD(P)H oxidases. Biochem Biophys Res Commun 338: 677-686, 2005. (Pubitemid 41540615)
31. 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 22: 21-27, 2002. (Pubitemid 34076227)
32. Taniyama Y, Griendling KK. Reactive oxygen species in the vasculature: molecular and cellular mechanisms. Hypertension 42: 1075-1081, 2003. (Pubitemid 37549058)
33. Touyz RM, Chen X, Tabet F, Yao G, He G, Quinn MT, Pagano PJ, Schiffrin EL. Expression of a functionally active gp91phox-containing neutrophil-type NAD (P)H oxidase in smooth muscle cells from human resistance arteries: regulation by angiotensin II. Circ Res 90: 1205-1213, 2002.
34. Wang CH, Cherng WJ, Yang NI, Kuo LT, Hsu CM, Yeh HI, Lan YJ, Yeh CH, Stanford WL. Late-outgrowth endothelial cells attenuate intimal hyperplasia contributed by mesenchymal stem cells after vascular injury. Arterioscler Thromb Vasc Biol 28: 54-60, 2008.
35. Wang Z, Wang DZ, Hockemeyer D, McAnally J, Nordheim A, Olson EN. Myocardin and ternary complex factors compete for SRF to control smooth muscle gene expression. Nature 428: 185-189, 2004. (Pubitemid 38374315)
36. Xiao Q, Zeng L, Zhang Z, Hu Y, Xu Q. Stem cell-derived Sca-1+ progenitors differentiate into smooth muscle cells, which is mediated by collagen IV-integrin α1/β1αv and PDGF receptor pathways. Am J Physiol Cell Physiol 292: C342-C352, 2007.
37. Xiao Q, Zeng L, Zhang Z, Margariti A, Ali ZA, Channon KM, Xu Q, Hu Y. Sca-1+ progenitors derived from embryonic stem cells differentiate into endothelial cells capable of vascular repair after arterial injury. Arterioscler Thromb Vasc Biol 26: 2244-2251, 2006. (Pubitemid 44465718)
38. Xie CQ, Zhang J, Villacorta L, Cui T, Huang H, Chen YE. A highly efficient method to differentiate smooth muscle cells from human embryonic stem cells. Arterioscler Thromb Vasc Biol 27: e311-e312, 2007. (Pubitemid 350158939)
39. Yoshida T, Owens GK. Molecular determinants of vascular smooth muscle cell diversity. Circ Res 96: 280-291, 2005. (Pubitemid 40279902)
40. Yoshida T, Sinha S, Dandre F, Wamhoff BR, Hoofnagle MH, Kremer BE, Wang DZ, Olson EN, Owens GK. Myocardin is a key regulator of CArG-dependent transcription of multiple smooth muscle marker genes. Circ Res 92: 856-864, 2003. (Pubitemid 36542526)
41. Zeng L, Xiao Q, Margariti A, Zhang Z, Zampetaki A, Patel S, Capogrossi MC, Hu Y, Xu Q. HDAC3 is crucial in shear- and VEGF-induced stem cell differentiation toward endothelial cells. J Cell Biol 174: 1059-1069, 2006. (Pubitemid 44455193)