NAD(P)H oxidase and eNOS play differential roles in cytomegalovirus infection-induced microvascular dysfunction

Free Radical Biology and Medicine

Volumn 51, Issue 12, 2011, Pages 2300-2308

  Leskov, Igor L ^a   Whitsett, Jennifer ^b   Vasquez Vivar, Jeannette ^b   Stokes, Karen Y ^a,c  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

Arteriolar vasodilation; Cardiovascular disease; Cytomegalovirus infection; eNOS; Free radicals; Microvasculature; NAD(P)H oxidase; Platelet adhesion

Indexed keywords

APOCYNIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SEPIAPTERIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIOLE; ARTICLE; BLOOD CELL; CAPILLARY; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; ENDOTHELIUM; ENZYME ACTIVITY; ENZYME INHIBITION; LEUKOCYTE; MICROANGIOPATHY; MOUSE; NONHUMAN; PRIORITY JOURNAL; THROMBOCYTE ADHESION; VASODILATATION;

ANIMALS; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; MICE; MICE, CONGENIC; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROVESSELS; NADPH OXIDASE; NITRIC OXIDE SYNTHASE TYPE III; RECEPTORS, IMMUNOLOGIC;

CYTOMEGALOVIRUS; MURINAE; MUS;

EID: 81855198908     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.09.039     Document Type: Article

References (63)

1. M.A. Jarvis, and J.A. Nelson Human cytomegalovirus persistence and latency in endothelial cells and macrophages Curr. Opin. Microbiol. 5 2002 403 407
2. C. Sinzger, and G. Jahn Human cytomegalovirus cell tropism and pathogenesis Intervirology 39 1996 302 319 (Pubitemid 27174134)
3. A. Blum, M. Giladi, M. Weinberg, G. Kaplan, H. Pasternack, S. Laniado, and H. Miller High anti-cytomegalovirus (CMV) IgG antibody titer is associated with coronary artery disease and may predict post-coronary balloon angioplasty restenosis Am. J. Cardiol. 81 1998 866 868 (Pubitemid 28204640)
4. C. Espinola-Klein, H.J. Rupprecht, S. Blankenberg, C. Bickel, H. Kopp, A. Victor, G. Hafner, W. Prellwitz, W. Schlumberger, and J. Meyer Impact of infectious burden on progression of carotid atherosclerosis Stroke 33 2002 2581 2586 (Pubitemid 35266427)
5. B. Gabrylewicz, U. Mazurek, A. Ochala, E. Sliupkas-Dyrda, P. Garbocz, A. Pyrlik, I. Mroz, T. Wilczok, and M. Tendera Cytomegalovirus infection in acute myocardial infarction: is there a causative relationship? Kardiol. Pol. 59 2003 283 292 (Pubitemid 37328509)
6. M.T. Grattan, C.E. Moreno-Cabral, V.A. Starnes, P.E. Oyer, E.B. Stinson, and N.E. Shumway Cytomegalovirus infection is associated with cardiac allograft rejection and atherosclerosis JAMA 261 1989 3561 3566 (Pubitemid 19155945)
7. M.S. Burnett, S. Durrani, E. Stabile, M. Saji, C.W. Lee, T.D. Kinnaird, E.P. Hoffman, and S.E. Epstein Murine cytomegalovirus infection increases aortic expression of proatherosclerotic genes Circulation 109 2004 893 897 (Pubitemid 38252742)
8. E. Hsich, Y.F. Zhou, B. Paigen, T.M. Johnson, M.S. Burnett, and S.E. Epstein Cytomegalovirus infection increases development of atherosclerosis in apolipoprotein-E knockout mice Atherosclerosis 156 2001 23 28 (Pubitemid 32429591)
9. I. Vliegen, F. Stassen, G. Grauls, R. Blok, and C. Bruggeman MCMV infection increases early T-lymphocyte influx in atherosclerotic lesions in apoE knockout mice J. Clin. Virol. 25 Suppl. 2 2002 S159 S171
10. I. Vliegen, A. Duijvestijn, G. Grauls, S. Herngreen, C. Bruggeman, and F. Stassen Cytomegalovirus infection aggravates atherogenesis in apoE knockout mice by both local and systemic immune activation Microbes Infect. 6 2004 17 24 (Pubitemid 38114817)
11. A.D. Yurochko, and E.S. Huang Human cytomegalovirus binding to human monocytes induces immunoregulatory gene expression J. Immunol. 162 1999 4806 4816 (Pubitemid 29314884)
12. M.S. Smith, G.L. Bentz, J.S. Alexander, and A.D. Yurochko Human cytomegalovirus induces monocyte differentiation and migration as a strategy for dissemination and persistence J. Virol. 78 2004 4444 4453 (Pubitemid 38501064)
13. L.J. Burns, J.C. Pooley, D.J. Walsh, G.M. Vercellotti, M.L. Weber, and A. Kovacs Intercellular adhesion molecule-1 expression in endothelial cells is activated by cytomegalovirus immediate early proteins [see comment] Transplantation 67 1999 137 144 (Pubitemid 29061151)
14. T.J. Dengler, M.J. Raftery, M. Werle, R. Zimmermann, and G. Schonrich Cytomegalovirus infection of vascular cells induces expression of pro-inflammatory adhesion molecules by paracrine action of secreted interleukin-1beta Transplantation 69 2000 1160 1168 (Pubitemid 30217601)
15. D.A. Knight, W.J. Waldman, and D.D. Sedmak Cytomegalovirus-mediated modulation of adhesion molecule expression by human arterial and microvascular endothelial cells Transplantation 68 1999 1814 1818 (Pubitemid 30004818)
16. J.E. Grundy, K.M. Lawson, L.P. MacCormac, J.M. Fletcher, and K.L. Yong Cytomegalovirus-infected endothelial cells recruit neutrophils by the secretion of C-X-C chemokines and transmit virus by direct neutrophil-endothelial cell contact and during neutrophil transendothelial migration J. Infect. Dis. 177 1998 1465 1474 (Pubitemid 28243567)
17. D. Ricotta, G. Alessandri, C. Pollara, S. Fiorentini, F. Favilli, M. Tosetti, A. Mantovani, M. Grassi, E. Garrafa, L. Dei Cas, C. Muneretto, and A. Caruso Adult human heart microvascular endothelial cells are permissive for non-lytic infection by human cytomegalovirus Cardiovasc. Res. 49 2001 440 448 (Pubitemid 32119561)
18. S. Shahgasempour, S.B. Woodroffe, and H.M. Garnett Alterations in the expression of ELAM-1, ICAM-1 and VCAM-1 after in vitro infection of endothelial cells with a clinical isolate of human cytomegalovirus Microbiol. Immunol. 41 1997 121 129 (Pubitemid 27093270)
19. A. Rahbar, and C. Soderberg-Naucler Human cytomegalovirus infection of endothelial cells triggers platelet adhesion and aggregation J. Virol. 79 2005 2211 2220 (Pubitemid 40204578)
20. M.V. Khoretonenko, I.L. Leskov, S.R. Jennings, A.D. Yurochko, and K.Y. Stokes Cytomegalovirus infection leads to microvascular dysfunction and exacerbates hypercholesterolemia-induced responses Am. J. Pathol. 177 2010 2134 2144
21. E. Senchenkov, M.V. Khoretonenko, I.L. Leskov, D.V. Ostanin, and K.Y. Stokes P-selectin mediates the microvascular dysfunction associated with persistent cytomegalovirus infection in normocholesterolemic and hypercholesterolemic mice Microcirculation 18 2011 452 462
22. K. Stokes, D. Cooper, A. Tailor, and D. Granger Hypercholesterolemia promotes inflammation and microvascular dysfunction: role of nitric oxide and superoxide Free Radic. Biol. Med. 33 2002 1026 1036
23. K.K. Griendling, D. Sorescu, and M. Ushio-Fukai NAD(P)H oxidase: role in cardiovascular biology and disease Circ. Res. 86 2000 494 501 (Pubitemid 30165039)
24. A. Warnholtz, G. Nickenig, E. Schulz, R. Macharzina, J.H. Brasen, M. Skatchkov, T. Heitzer, J.P. Stasch, K.K. Griendling, D.G. Harrison, M. Bohm, T. Meinertz, and T. Munzel Increased NADH-oxidase-mediated superoxide production in the early stages of atherosclerosis: evidence for involvement of the renin-angiotensin system Circulation 99 1999 2027 2033 (Pubitemid 29183901)
25. G. Muller, and H. Morawietz Nitric oxide, NAD(P)H oxidase, and atherosclerosis Antioxid. Redox Signal. 11 2009 1711 1731
26. K.Y. Stokes, J.M. Russell, M.H. Jennings, J.S. Alexander, and D.N. Granger Platelet-associated NAD(P)H oxidase contributes to the thrombogenic phenotype induced by hypercholesterolemia Free Radic. Biol. Med. 43 2007 22 30 (Pubitemid 46874832)
27. K.Y. Stokes, E.C. Clanton, J.M. Russell, C.R. Ross, and D.N. Granger NAD(P)H oxidase-derived superoxide mediates hypercholesterolemia-induced leukocyte-endothelial cell adhesion Circ. Res. 88 2001 499 505 (Pubitemid 32240913)
28. J. Vasquez-Vivar, D. Duquaine, J. Whitsett, B. Kalyanaraman, and S. Rajagopalan Altered tetrahydrobiopterin metabolism in atherosclerosis: implications for use of oxidized tetrahydrobiopterin analogues and thiol antioxidants Arterioscler. Thromb. Vasc. Biol. 22 2002 1655 1661
29. J. Vasquez-Vivar, B. Kalyanaraman, P. Martasek, N. Hogg, B.S. Masters, H. Karoui, P. Tordo, and K.A. Pritchard Jr. Superoxide generation by endothelial nitric oxide synthase: the influence of cofactors Proc. Natl. Acad. Sci. U. S. A. 95 1998 9220 9225 (Pubitemid 28506212)
30. W. Engels, G. Grauls, P.J. Lemmens, W.J. Mullers, and C.A. Bruggeman Influence of a cytomegalovirus infection on functions and arachidonic acid metabolism of rat peritoneal macrophages J. Leukoc. Biol. 45 1989 466 473 (Pubitemid 19135470)
31. E.L. Yourtee, F.J. Bia, B.P. Griffith, and R.K. Root Neutrophil response and function during acute cytomegalovirus infection in guinea pigs Infect. Immun. 36 1982 11 16 (Pubitemid 12156398)
32. S. Suzuki, M. Kameoka, T. Nakaya, T. Kimura, N. Nishi, K. Hirai, and K. Ikuta Superoxide generation by monocytes following infection with human cytomegalovirus Immunopharmacology 37 1997 185 190 (Pubitemid 27471035)
33. E. Speir Cytomegalovirus gene regulation by reactive oxygen species: agents in atherosclerosis Ann. N. Y. Acad. Sci. 899 2000 363 374 (Pubitemid 30352800)
34. J.J. Bouwman, F.L. Visseren, L.M. Bevers, W.E. van der Vlist, K.P. Bouter, and R.J. Diepersloot Azithromycin reduces Chlamydia pneumoniae-induced attenuation of eNOS and cGMP production by endothelial cells Eur. J. Clin. Invest. 35 2005 573 582 (Pubitemid 41243301)
35. M. Weis, T.N. Kledal, K.Y. Lin, S.N. Panchal, S.Z. Gao, H.A. Valantine, E.S. Mocarski, and J.P. Cooke Cytomegalovirus infection impairs the nitric oxide synthase pathway: role of asymmetric dimethylarginine in transplant arteriosclerosis Circulation 109 2004 500 505 (Pubitemid 38168513)
36. G.S. Dhaunsi, J. Kaur, and R.B. Turner Role of NADPH oxidase in cytomegalovirus-induced proliferation of human coronary artery smooth muscle cells J. Biomed. Sci. 10 2003 505 509 (Pubitemid 37025960)
37. X. Zhou, H.G. Bohlen, S.J. Miller, and J.L. Unthank NAD(P)H oxidase-derived peroxide mediates elevated basal and impaired flow-induced NO production in SHR mesenteric arteries in vivo Am. J. Physiol. Heart Circ. Physiol. 295 2008 H1008 H1016
38. K.C. Wood, R.P. Hebbel, D.J. Lefer, and D.N. Granger Critical role of endothelial cell-derived nitric oxide synthase in sickle cell disease-induced microvascular dysfunction Free Radic. Biol. Med. 40 2006 1443 1453
39. Y. Tomita, D.H. Sachs, and M. Sykes Myelosuppressive conditioning is required to achieve engraftment of pluripotent stem cells contained in moderate doses of syngeneic bone marrow Blood 83 1994 939 948 (Pubitemid 24058543)
40. K.Y. Stokes, S. Gurwara, and D.N. Granger T-cell derived interferon-gamma contributes to arteriolar dysfunction during acute hypercholesterolemia Arterioscler. Thromb. Vasc. Biol. 27 2007 1998 2004 (Pubitemid 47312310)
41. D. Cooper, K.D. Chitman, M.C. Williams, and D.N. Granger Time-dependent platelet-vessel wall interactions induced by intestinal ischemia-reperfusion Am. J. Physiol. Gastrointest. Liver Physiol. 284 2003 G1027 G1033
42. J. Whitsett, M.J. Picklo Sr., and J. Vasquez-Vivar 4-Hydroxy-2-nonenal increases superoxide anion radical in endothelial cells via stimulated GTP cyclohydrolase proteasomal degradation Arterioscler. Thromb. Vasc. Biol. 27 2007 2340 2347 (Pubitemid 350203948)
43. S. Heumuller, S. Wind, E. Barbosa-Sicard, H.H. Schmidt, R. Busse, K. Schroder, and R.P. Brandes Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant Hypertension 51 2008 211 217 (Pubitemid 351159930)
44. B.M. Babior The leukocyte NADPH oxidase Isr. Med. Assoc. J. 4 2002 1023 1024
45. P. Pignatelli, V. Sanguigni, L. Lenti, D. Ferro, A. Finocchi, P. Rossi, and F. Violi gp91phox-dependent expression of platelet CD40 ligand Circulation 110 2004 1326 1329 (Pubitemid 39202353)
46. R.D. Plumb, N.A. El-Sherbeeny, L.J. Dixon, S.M. Hughes, A.B. Devine, W.J. Leahey, and G.E. McVeigh NAD(P)H-dependent superoxide production in platelets: the role of angiotensin II and protein kinase C Clin. Biochem. 38 2005 607 613 (Pubitemid 40961629)
47. A. Gorlach, R.P. Brandes, K. Nguyen, M. Amidi, F. Dehghani, and R. Busse A gp91phox containing NADPH oxidase selectively expressed in endothelial cells is a major source of oxygen radical generation in the arterial wall Circ. Res. 87 2000 26 32 (Pubitemid 30456931)
48. R.M. Touyz, X. Chen, F. Tabet, G. Yao, G. He, M.T. Quinn, P.J. Pagano, and E.L. Schiffrin 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 2002 1205 1213 (Pubitemid 34786906)
49. B. Lassegue, and K.K. Griendling NADPH oxidases: functions and pathologies in the vasculature Arterioscler. Thromb. Vasc. Biol. 30 2010 653 661
50. P. Pignatelli, V. Sanguigni, L. Lenti, L. Loffredo, R. Carnevale, R. Sorge, and F. Violi Oxidative stress-mediated platelet CD40 ligand upregulation in patients with hypercholesterolemia: effect of atorvastatin J. Thromb. Haemost. 5 2007 1170 1178 (Pubitemid 46902118)
51. J.B. Laursen, M. Somers, S. Kurz, L. McCann, A. Warnholtz, B.A. Freeman, M. Tarpey, T. Fukai, and D.G. Harrison Endothelial regulation of vasomotion in apoE-deficient mice: implications for interactions between peroxynitrite and tetrahydrobiopterin Circulation 103 2001 1282 1288 (Pubitemid 32221353)
52. C.P. Tiefenbacher, T. Bleeke, C. Vahl, K. Amann, A. Vogt, and W. Kubler Endothelial dysfunction of coronary resistance arteries is improved by tetrahydrobiopterin in atherosclerosis Circulation 102 2000 2172 2179
53. U. Landmesser, S. Dikalov, S.R. Price, L. McCann, T. Fukai, S.M. Holland, W.E. Mitch, and D.G. Harrison Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension J. Clin. Invest. 111 2003 1201 1209 (Pubitemid 36519937)
54. J.E. Hungerford, W.C. Sessa, and S.S. Segal Vasomotor control in arterioles of the mouse cremaster muscle FASEB J. 14 2000 197 207 (Pubitemid 30051537)
55. C. Grahame-Clarke, N.N. Chan, D. Andrew, G.L. Ridgway, D.J. Betteridge, V. Emery, H.M. Colhoun, and P. Vallance Human cytomegalovirus seropositivity is associated with impaired vascular function Circulation 108 2003 678 683 (Pubitemid 36999251)
56. G.M. Pieper, I.A. Ionova, B.C. Cooley, R.Q. Migrino, A.K. Khanna, J. Whitsett, and J. Vasquez-Vivar Sepiapterin decreases acute rejection and apoptosis in cardiac transplants independently of changes in nitric oxide and inducible nitric-oxide synthase dimerization J. Pharmacol. Exp. Ther. 329 2009 890 899
57. M.J. Crabtree, C.L. Smith, G. Lam, M.S. Goligorsky, and S.S. Gross Ratio of 5,6,7,8-tetrahydrobiopterin to 7,8-dihydrobiopterin in endothelial cells determines glucose-elicited changes in NO vs. superoxide production by eNOS Am. J. Physiol. Heart Circ. Physiol. 294 2008 H1530 H1540
58. J. Vasquez-Vivar, P. Martasek, J. Whitsett, J. Joseph, and B. Kalyanaraman The ratio between tetrahydrobiopterin and oxidized tetrahydrobiopterin analogues controls superoxide release from endothelial nitric oxide synthase: an EPR spin trapping study Biochem. J. 362 2002 733 739 (Pubitemid 34242326)
59. L.J. Dixon, D.R. Morgan, S.M. Hughes, L.T. McGrath, N.A. El-Sherbeeny, R.D. Plumb, A. Devine, W. Leahey, G.D. Johnston, and G.E. McVeigh Functional consequences of endothelial nitric oxide synthase uncoupling in congestive cardiac failure Circulation 107 2003 1725 1728 (Pubitemid 36418350)
60. Y.H. Shen, L. Zhang, B. Utama, J. Wang, Y. Gan, X. Wang, L. Chen, G.M. Vercellotti, J.S. Coselli, J.L. Mehta, and X.L. Wang Human cytomegalovirus inhibits Akt-mediated eNOS activation through upregulating PTEN (phosphatase and tensin homolog deleted on chromosome 10) Cardiovasc. Res. 69 2006 502 511 (Pubitemid 43098806)
61. G.L. Bentz, M. Jarquin-Pardo, G. Chan, M.S. Smith, C. Sinzger, and A.D. Yurochko Human cytomegalovirus (HCMV) infection of endothelial cells promotes naive monocyte extravasation and transfer of productive virus to enhance hematogenous dissemination of HCMV J. Virol. 80 2006 11539 11555 (Pubitemid 44788869)
62. M. Ishikawa, K.Y. Stokes, J.H. Zhang, A. Nanda, and D.N. Granger Cerebral microvascular responses to hypercholesterolemia: roles of NADPH oxidase and P-selectin Circ. Res. 94 2004 239 244 (Pubitemid 38197457)
63. A. Tailor, and D.N. Granger Hypercholesterolemia promotes leukocyte-dependent platelet adhesion in murine postcapillary venules Microcirculation 11 2004 597 603 (Pubitemid 39618631)