Mechanisms of vascular smooth muscle NADPH oxidase 1 (Nox1) contribution to injury-induced neointimal formation

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 29, Issue 4, 2009, Pages 480-487

  Lee, Moo Yeol ^a,d   Martin, Alejandra San ^a   Mehta, Puja K ^a   Dikalova, Anna E ^a   Garrido, Abel Martin ^a   Datla, S Raju ^e   Lyons, Erin ^a   Krause, Karl Heinz ^b   Banfi, Botond ^c   Lambeth, J David ^a   Lassègue, Bernard ^a   Griendling, Kathy K ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c UNIVERSITY OF IOWA   (United States)

^d Chonnam National University   (South Korea)

^e 319 WMB ^*

Author keywords

Migration; NADPH oxidase 1; Neointima; Reactive oxygen species; Vascular smooth muscle

Indexed keywords

BETA TUBULIN; COFILIN; COLLAGEN TYPE 1; CYCLIN DEPENDENT KINASE 4; FIBRONECTIN; P21 ACTIVATED KINASE 1; PROTEIN MDIA1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; UNCLASSIFIED DRUG; CARRIER PROTEIN; CFL2 PROTEIN, MOUSE; COFILIN 2; DIAP1 PROTEIN, MOUSE; OXIDOREDUCTASE; P21 ACTIVATED KINASE; PAK1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTERY INTIMA PROLIFERATION; ARTICLE; CARDIOVASCULAR DISEASE; CELL ADHESION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEMORAL ARTERY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; VASCULAR SMOOTH MUSCLE; WESTERN BLOTTING; WILD TYPE; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL MOTION; DISEASE MODEL; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; HYPERPLASIA; INJURY; INTIMA; METABOLISM; MOUSE MUTANT; PATHOLOGY; PHOSPHORYLATION; TIME;

ANIMALS; APOPTOSIS; CARRIER PROTEINS; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; COFILIN 2; COLLAGEN TYPE I; DISEASE MODELS, ANIMAL; FEMORAL ARTERY; FIBRONECTINS; HYPERPLASIA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; NADH, NADPH OXIDOREDUCTASES; P21-ACTIVATED KINASES; PHOSPHORYLATION; TIME FACTORS; TRANSFECTION; TUNICA INTIMA;

EID: 63449105018     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.108.181925     Document Type: Article

References (47)

1. Zargham R. Preventing restenosis after angioplasty: a multistage approach. Clin Sci (Lond). 2008;114:257-264.
2. Ferns GA, Raines EW, Sprugel KH, Motani AS, Reidy MA, Ross R. Inhibition of neointimal smooth muscle accumulation after angioplasty by an antibody to PDGF. Science. 1991;253:1129-1132.
3. Clempus RE, Griendling KK. Reactive oxygen species signaling in vascular smooth muscle cells. Cardiovasc Res. 2006;71:216-225.
4. Lassègue B, Sorescu D, Szöcs K, Yin Q, Akers M, Zhang Y, Grant SL, Lambeth JD, Griendling KK. Novel gp91phox homologues in vascular smooth muscle cells: nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways. Circ Res. 2001;88:888-894.
5. 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. 2002;90:1205-1213.
6. Lyle AN, Griendling KK. Modulation of vascular smooth muscle signaling by reactive oxygen species. Physiology (Bethesda). 2006;21:269-280.
7. 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. 2004;24:677-683.
8. Dikalova A, Clempus R, Lassègue B, Cheng G, McCoy J, Dikalov S, San Martin A, Lyle A, Weber DS, Weiss D, Taylor WR, Schmidt HHW, Owens GK, Lambeth JD, Griendling KK. Nox1 overexpression potentiates angiotensin II-induced hypertension and vascular smooth muscle hypertrophy in transgenic mice. Circulation. 2005;112:2668-2676.
9. Gavazzi G, Deffert C, Trocme C, Schappi M, Herrmann FR, Krause KH. NOX1 deficiency protects from aortic dissection in response to angiotensin II. Hypertension. 2007;50:189-196.
10. Schroder K, Helmcke I, Palfi K, Krause KH, Busse R, Brandes RP. Nox1 mediates basic fibroblast growth factor-induced migration of vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2007;27:1736-1743.
11. Szöcs K, Lassègue 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.
12. Shi Y, Niculescu R, Wang D, Patel S, Davenpeck KL, Zalewski A. Increased NAD(P)H oxidase and reactive oxygen species in coronary arteries after balloon injury. Arterioscler Thromb Vasc Biol. 2001;21:739-745.
13. West N, Guzik T, Black E, Channon K. Enhanced superoxide production in experimental venous bypass graft intimal hyperplasia: role of NAD(P)H oxidase. Arterioscler Thromb Vasc Biol. 2001;21:189-194.
14. Kappert K, Sparwel J, Sandin A, Seiler A, Siebolts U, Leppanen O, Rosenkranz S, Ostman A. Antioxidants relieve phosphatase inhibition and reduce PDGF signaling in cultured VSMCs and in restenosis. Arterioscler Thromb Vasc Biol. 2006;26:2644-2651.
15. Zebda N, Bernard O, Bailly M, Welti S, Lawrence DS, Condeelis JS. Phosphorylation of ADF/cofilin abolishes EGF-induced actin nucleation at the leading edge and subsequent lamellipod extension. J Cell Biol. 2000;151:1119-1128.
16. Gavazzi G, Banfi B, Deffert C, Fiette L, Schappi M, Herrmann F, Krause KH. Decreased blood pressure in NOX1-deficient mice. FEBS Lett. 2006;580:497-504.
17. Sata M, Maejima Y, Adachi F, Fukino K, Saiura A, Sugiura S, Aoyagi T, Imai Y, Kurihara H, Kimura K, Omata M, Makuuchi M, Hirata Y, Nagai R. A mouse model of vascular injury that induces rapid onset of medial cell apoptosis followed by reproducible neointimal hyperplasia. J Mol Cell Cardiol. 2000;32:2097-2104.
18. Ohmi K, Masuda T, Yamaguchi H, Sakurai T, Kudo Y, Katsuki M, Nonomura Y. A novel aortic smooth muscle cell line obtained from p53 knock out mice expresses several differentiation characteristics. Biochem Biophys Res Commun. 1997;238:154-158.
19. Hanna IR, Dikalova A, Hilenski L, Quinn MT, Griendling KK. Nox 1 binds p22phox to form a functional oxidase in vascular smooth muscle cells (VSMCs). Circulation. 2002;106:II-164.
20. Suh Y, Arnold RS, Lassègue B, Shi J, Xu X, Sorescu D, Chung AB, Griendling KK, Lambeth JD. Cell transformation by the superoxide-generating oxidase mox1. Nature. 1999;401:79-82.
21. 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. 2007;27:42-48.
22. Farb A, Kolodgie FD, Hwang JY, Burke AP, Tefera K, Weber DK, Wight TN, Virmani R. Extracellular matrix changes in stented human coronary arteries. Circulation. 2004;110:940-947.
23. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362:801-809.
24. Schwartz SM. Perspectives series: cell adhesion in vascular biology. Smooth muscle migration in atherosclerosis and restenosis. J Clin Invest. 1997;99:2814-2816.
25. Magnusson MK, Mosher DF. Fibronectin: structure, assembly, and cardiovascular implications. Arterioscler Thromb Vasc Biol. 1998;18:1363-1370.
26. Raines EW. The extracellular matrix can regulate vascular cell migration, proliferation, and survival: relationships to vascular disease. Int J Exp Pathol. 2000;81:173-182.
27. Arnold RS, Shi J, Murad E, Whalen AM, Sun CQ, Polavarapu R, Parthasarathy S, Petros JA, Lambeth JD. Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Nox1. Proc Natl Acad Sci U S A. 2001;98:5550-5555.
28. Ranjan P, Anathy V, Burch PM, Weirather K, Lambeth JD, Heintz NH. Redox-dependent expression of cyclin D1 and cell proliferation by Nox1 in mouse lung epithelial cells. Antioxid Redox Signal. 2006;8:1447-1459.
29. Chen H, Bernstein BW, Bamburg JR. Regulating actin-filament dynamics in vivo. Trends Biochem Sci. 2000;25:19-23.
30. Pollman MJ, Hall JL, Gibbons GH. Determinants of vascular smooth muscle cell apoptosis after balloon angioplasty injury. Influence of redox state and cell phenotype. Circ Res. 1999;84:113-121.
31. Mayr M, Xu Q. Smooth muscle cell apoptosis in arteriosclerosis. Exp Gerontol. 2001;36:969-987.
32. ten Freyhaus H, Huntgeburth M, Wingler K, Schnitker J, Baumer AT, Vantler M, Bekhite MM, Wartenberg M, Sauer H, Rosenkranz S. Novel Nox inhibitor VAS2870 attenuates PDGF-dependent smooth muscle cell chemotaxis, but not proliferation. Cardiovasc Res. 2006;71:331-341.
33. Weber DS, Taniyama Y, Rocic P, Seshiah PN, Dechert MA, Gerthoffer WT, Griendling KK. Phosphoinositide-dependent kinase 1 and p21-activated protein kinase mediate reactive oxygen species-dependent regulation of platelet-derived growth factor-induced smooth muscle cell migration. Circ Res. 2004;94:1219-1226.
34. Wang Z, Castresana MR, Newman WH. Reactive oxygen species-sensitive p38 MAPK controls thrombin-induced migration of vascular smooth muscle cells. J Mol Cell Cardiol. 2004;36:49-56.
35. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR. Cell migration: integrating signals from front to back. Science. 2003;302:1704-1709.
36. Burridge K, Wennerberg K. Rho and Rac take center stage. Cell. 2004;116:167-179.
37. Wang W, Mouneimne G, Sidani M, Wyckoff J, Chen X, Makris A, Goswami S, Bresnick AR, Condeelis JS. The activity status of cofilin is directly related to invasion, intravasation, and metastasis of mammary tumors. J Cell Biol. 2006;173:395-404.
38. Shinohara M, Shang WH, Kubodera M, Harada S, Mitsushita J, Kato M, Miyazaki H, Sumimoto H, Kamata T. Nox1 redox signaling mediates oncogenic Ras-induced disruption of stress fibers and focal adhesions by down-regulating Rho. J Biol Chem. 2007;282:17640-17648.
39. Li F, Higgs HN. The mouse Formin mDia1 is a potent actin nucleation factor regulated by autoinhibition. Curr Biol. 2003;13:1335-1340.
40. Wen Y, Eng CH, Schmoranzer J, Cabrera-Poch N, Morris EJ, Chen M, Wallar BJ, Alberts AS, Gundersen GG. EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat Cell Biol. 2004;6:820-830.
41. Sakata D, Taniguchi H, Yasuda S, Adachi-Morishima A, Hamazaki Y, Nakayama R, Miki T, Minato N, Narumiya S. Impaired T lymphocyte trafficking in mice deficient in an actin-nucleating protein, mDia1. J Exp Med. 2007;204:2031-2038.
42. San Martin A, Lee MY, Williams HC, Mizuno K, Lassègue B, Griendling KK. Dual regulation of cofilin activity by LIMK and slingshot 1L phosphatase controls PDGF-induced migration of human aortic smooth muscle cells. Circ Res. 2008;102:432-438.
43. Chandrasekar B, Tanguay JF. Platelets and restenosis. J Am Coll Cardiol. 2000;35:555-562.
44. Irani K. Oxidant signaling in vascular cell growth, death, and survival: a review of the roles of reactive oxygen species in smooth muscle and endothelial cell mitogenic and apoptotic signaling. Circ Res. 2000;87:179-183.
45. Li G, Chen SJ, Oparil S, Chen YF, Thompson JA. Direct in vivo evidence demonstrating neointimal migration of adventitial fibroblasts after balloon injury of rat carotid arteries. Circulation. 2000;101:1362-1365.
46. Welt FG, Rogers C. Inflammation and restenosis in the stent era. Arterioscler Thromb Vasc Biol. 2002;22:1769-1776.
47. Tanaka K, Sata M, Natori T, Kim-Kaneyama JR, Nose K, Shibanuma M, Hirata Y, Nagai R. Circulating progenitor cells contribute to neointimal formation in nonirradiated chimeric mice. FASEB J. 2008;22:428-436.