Cyclophilin a is required for angiotensin II-induced p47phox translocation to caveolae in vascular smooth muscle cells

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 9, 2013, Pages 2147-2153

  Soe, Nwe Nwe ^a   Sowden, Mark ^a   Baskaran, Padmamalini ^b   Smolock, Elaine M ^a   Kim, Yeonghwan ^a   Nigro, Patrizia ^c   Berk, Bradford C ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b UNIVERSITY OF WYOMING COLLEGE OF HEALTH SCIENCES   (United States)

^c CENTRO CARDIOLOGICO MONZINO   (Italy)

Author keywords

angiotensin II; cyclophilin A; cytoskeleton; p47phox protein, mouse; reactive oxygen species

Indexed keywords

ACTIN; ANGIOTENSIN II; CYCLOPHILIN A; CYCLOSPORIN A; DIPHENYLIODONIUM SALT; MEMBRANE PROTEIN; P47PHOX PROTEIN; PEPTIDYLPROLYL ISOMERASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; CAVEOLA; CELL FRACTIONATION; CELL MEMBRANE; CELL MEMBRANE TRANSPORT; CELL STIMULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; SMOOTH MUSCLE FIBER; SUCROSE GRADIENT; VASCULAR SMOOTH MUSCLE; WILD TYPE;

ANGIOTENSIN II; CYCLOPHILIN A; CYTOSKELETON; P47PHOX PROTEIN, MOUSE; REACTIVE OXYGEN SPECIES;

ACTIN CYTOSKELETON; ANGIOTENSIN II; ANIMALS; BLOTTING, WESTERN; CAVEOLAE; CYCLOPHILIN A; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; MUSCLE, SMOOTH, VASCULAR; MUTATION; MYOCYTES, SMOOTH MUSCLE; NADPH OXIDASE; PEPTIDES; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; PROTEIN TRANSPORT; RATS; REACTIVE OXYGEN SPECIES; RECEPTOR, ANGIOTENSIN, TYPE 1; RECOMBINANT FUSION PROTEINS; TIME FACTORS;

EID: 84883277660     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.113.301894     Document Type: Article

References (33)

1. Taniyama Y, Griendling KK. Reactive oxygen species in the vasculature: molecular and cellular mechanisms. Hypertension. 2003;42:1075-1081. (Pubitemid 37549058)
2. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res. 1994;74:1141-1148. (Pubitemid 24176909)
3. Babior BM. NADPH oxidase: an update. Blood. 1999;93:1464-1476. (Pubitemid 29102471)
4. Ushio-Fukai M. Localizing NADPH oxidase-derived ROS. Sci STKE. 2006;2006:re8.
5. Lee SH, Dominguez R. Regulation of actin cytoskeleton dynamics in cells. Mol Cells. 2010;29:311-325.
6. Fernstrom K, Farmer P, Ali MS. Cytoskeletal remodeling in vascular smooth muscle cells in response to angiotensin II-induced activation of the SHP-2 tyrosine phosphatase. J Cell Physiol. 2005;205:402-413. (Pubitemid 41598855)
7. Ishida T, Ishida M, Suero J, Takahashi M, Berk BC. Agonist-stimulated cytoskeletal reorganization and signal transduction at focal adhesions in vascular smooth muscle cells require c-Src. J Clin Invest. 1999;103:789-797. (Pubitemid 29152624)
8. Touyz RM, Yao G, Quinn MT, Pagano PJ, Schiffrin EL. p47phox associates with the cytoskeleton through cortactin in human vascular smooth muscle cells: role in NAD(P)H oxidase regulation by angiotensin II. Arterioscler Thromb Vasc Biol. 2005;25:512-518. (Pubitemid 40315671)
9. Touyz RM, Yao G, Schiffrin EL. Role of the actin cytoskeleton in angiotensin II signaling in human vascular smooth muscle cells. Can J Physiol Pharmacol. 2005;83:91-97. (Pubitemid 40754780)
10. Handschumacher RE, Harding MW, Rice J, Drugge RJ, Speicher DW. Cyclophilin: a specific cytosolic binding protein for cyclosporin A. Science. 1984;226:544-547. (Pubitemid 14018525)
11. Takahashi N, Hayano T, Suzuki M. Peptidyl-prolyl cis-trans isomerase is the cyclosporin A-binding protein cyclophilin. Nature. 1989;337:473-475.
12. Schreiber SL. Chemistry and biology of the immunophilins and their immunosuppressive ligands. Science. 1991;251:283-287. (Pubitemid 21916873)
13. Zhu C, Wang X, Deinum J, Huang Z, Gao J, Modjtahedi N, Neagu MR, Nilsson M, Eriksson PS, Hagberg H, Luban J, Kroemer G, Blomgren K. Cyclophilin A participates in the nuclear translocation of apoptosis-inducing factor in neurons after cerebral hypoxia-ischemia. J Exp Med. 2007;204:1741-1748. (Pubitemid 47236312)
14. Brazin KN, Mallis RJ, Fulton DB, Andreotti AH. Regulation of the tyrosine kinase Itk by the peptidyl-prolyl isomerase cyclophilin A. Proc Natl Acad Sci USA. 2002;99:1899-1904. (Pubitemid 34168986)
15. Krummrei U, Bang R, Schmidtchen R, Brune K, Bang H. Cyclophilin-A is a zinc-dependent DNA binding protein in macrophages. FEBS Lett. 1995;371:47-51.
16. Satoh K, Nigro P, Matoba T, O'Dell MR, Cui Z, Shi X, Mohan A, Yan C, Abe J, Illig KA, Berk BC. Cyclophilin A enhances vascular oxidative stress and the development of angiotensin II-induced aortic aneurysms. Nat Med. 2009;15:649-656.
17. Satoh K, Nigro P, Zeidan A, Soe NN, Jaffré F, Oikawa M, O'Dell MR, Cui Z, Menon P, Lu Y, Mohan A, Yan C, Blaxall BC, Berk BC. Cyclophilin A promotes cardiac hypertrophy in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2011;31:1116-1123.
18. Nigro P, Satoh K, O'Dell MR, Soe NN, Cui Z, Mohan A, Abe J, Alexis JD, Sparks JD, Berk BC. Cyclophilin A is an inflammatory mediator that promotes atherosclerosis in apolipoprotein E-deficient mice. J Exp Med. 2011;208:53-66.
19. Yuan A, Mills RG, Bamburg JR, Bray JJ. Axonal transport and distribution of cyclophilin A in chicken neurons. Brain Res. 1997;771:203-212. (Pubitemid 27492098)
20. Galigniana MD, Morishima Y, Gallay PA, Pratt WB. Cyclophilin-A is bound through its peptidylprolyl isomerase domain to the cytoplasmic dynein motor protein complex. J Biol Chem. 2004;279:55754-55759. (Pubitemid 40066582)
21. Heine SJ, Olive D, Gao JL, Murphy PM, Bukrinsky MI, Constant SL. Cyclophilin A cooperates with MIP-2 to augment neutrophil migration. J Inflamm Res. 2011;4:93-104.
22. Calhoun CC, Lu YC, Song J, Chiu R. Knockdown endogenous CypA with siRNA in U2OS cells results in disruption of F-actin structure and alters tumor phenotype. Mol Cell Biochem. 2009;320:35-43.
23. Touyz RM, Yao G, Schiffrin EL. c-Src induces phosphorylation and translocation of p47phox: role in superoxide generation by angiotensin II in human vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2003;23:981-987. (Pubitemid 36717143)
24. Lungu AO, Jin ZG, Yamawaki H, Tanimoto T, Wong C, Berk BC. Cyclosporin A inhibits flow-mediated activation of endothelial nitricoxide synthase by altering cholesterol content in caveolae. J Biol Chem. 2004;279:48794-48800. (Pubitemid 39625758)
25. Satoh K, Matoba T, Suzuki J, O'Dell MR, Nigro P, Cui Z, Mohan A, Pan S, Li L, Jin ZG, Yan C, Abe J, Berk BC. Cyclophilin A mediates vascular remodeling by promoting inflammation and vascular smooth muscle cell proliferation. Circulation. 2008;117:3088-3098.
26. Lv P, Miao SB, Shu YN, Dong LH, Liu G, Xie XL, Gao M, Wang YC, Yin YJ, Wang XJ, Han M. Phosphorylation of smooth muscle 22? facilitates angiotensin II-induced ROS production via activation of the PKC?-P47phox axis through release of PKC? and actin dynamics and is associated with hypertrophy and hyperplasia of vascular smooth muscle cells in vitro and in vivo. Circ Res. 2012;111:697-707.
27. Usatyuk PV, Romer LH, He D, Parinandi NL, Kleinberg ME, Zhan S, Jacobson JR, Dudek SM, Pendyala S, Garcia JG, Natarajan V. Regulation of hyperoxia-induced NADPH oxidase activation in human lung endothelial cells by the actin cytoskeleton and cortactin. J Biol Chem. 2007;282:23284-23295. (Pubitemid 47311961)
28. Wu RF, Gu Y, Xu YC, Nwariaku FE, Terada LS. Vascular endothelial growth factor causes translocation of p47phox to membrane ruffles through WAVE1. J Biol Chem. 2003;278:36830-36840. (Pubitemid 37140017)
29. Kuroda J, Nakagawa K, Yamasaki T, Nakamura K, Takeya R, Kuribayashi F, Imajoh-Ohmi S, Igarashi K, Shibata Y, Sueishi K, Sumimoto H. The superoxide-producing NAD(P)H oxidase Nox4 in the nucleus of human vascular endothelial cells. Genes Cells. 2005;10:1139-1151. (Pubitemid 41830073)
30. Lavigne MC, Malech HL, Holland SM, Leto TL. Genetic demonstration of p47phox-dependent superoxide anion production in murine vascular smooth muscle cells. Circulation. 2001;104:79-84. (Pubitemid 32623293)
31. El-Benna J, Dang PM, Gougerot-Pocidalo MA, Marie JC, Braut-Boucher F. p47phox, the phagocyte NADPH oxidase/NOX2 organizer: structure, phosphorylation and implication in diseases. Exp Mol Med. 2009;41:217-225.
32. Li G, Cui Q. What is so special about Arg 55 in the catalysis of cyclophilin A? insights from hybrid QM/MM simulations. J Am Chem Soc. 2003;125:15028-15038. (Pubitemid 37509666)
33. Zander K, Sherman MP, Tessmer U, Bruns K, Wray V, Prechtel AT, Schubert E, Henklein P, Luban J, Neidleman J, Greene WC, Schubert U. Cyclophilin A interacts with HIV-1 Vpr and is required for its functional expression. J Biol Chem. 2003;278:43202-43213. (Pubitemid 37345939)