Chronic intermittent hypoxia exposure induces atherosclerosis in ApoE knockout mice: Role of NF-κB p50

American Journal of Pathology

Volumn 181, Issue 5, 2012, Pages 1530-1539

  Fang, Guoqiang ^a   Song, Dongmei ^a   Ye, Xiaobing ^a   Mao, Sun Zhong ^a   Liu, Gang ^a   Liu, Shu Fang ^a  

^a FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; CHOLESTEROL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA ROOT; ARTICLE; ATHEROSCLEROSIS; CELL INFILTRATION; CHOLESTEROL BLOOD LEVEL; CHRONIC INTERMITTENT HYPOXIA; CONTROLLED STUDY; DIET; DOWN REGULATION; FEMALE; GENE DELETION; MACROPHAGE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ANOXIA; AORTA; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BODY WEIGHT; CHOLESTEROL; CHRONIC DISEASE; DOWN-REGULATION; FEMALE; GENE DELETION; HYPERCHOLESTEROLEMIA; INFLAMMATION; MALE; MICE; MICE, KNOCKOUT; NF-KAPPA B P50 SUBUNIT; NITRIC OXIDE SYNTHASE TYPE II; OXYGEN; RECEPTORS, LDL; SIGNAL TRANSDUCTION; TIME FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84868120046     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.07.024     Document Type: Article

References (50)

1. T. Mooe, K.A. Franklin, K. Holmstrom, T. Rabben, U. Wiklund Sleep-disordered breathing and coronary artery disease: long-term prognosis Am J Respir Crit Care Med 164 2001 1910 1913 (Pubitemid 33152329)
2. H.K. Yaggi, J. Concato, W.N. Kernan, J.H. Lichtman, L.M. Brass, V. Mohsenin Obstructive sleep apnea as a risk factor for stroke and death N Engl J Med 353 2005 2034 2041 (Pubitemid 41609096)
3. S.F. Quan, B.J. Gersh Cardiovascular consequences of sleep-disordered breathing: past, present and future: report of a workshop from the National Center on Sleep Disorders Research and the National Heart, Lung, and Blood Institute Circulation 109 2004 951 957 (Pubitemid 38282845)
4. V.K. Somers, D.P. White, R. Amin, W.T. Abraham, F. Costa, A. Culebras, S. Daniels, J.S. Floras, C.E. Hunt, L.J. Olson, T.G. Pickering, R. Russell, M. Woo, T. Young Sleep apnea and cardiovascular disease: an American Heart Association/American College of Cardiology Foundation scientific statement from the American Heart Association Circulation 118 2008 1080 1111
5. B. Mokhlesi, D. Gozal Update in sleep medicine 2010 Am J Respir Crit Care Med 181 2010 545 549
6. P. Lévy, J.L. Pépin, C. Arnaud, J.P. Baguet, M. Dematteis, F. Mach Obstructive sleep apnea and atherosclerosis Prog Cardiovasc Dis 51 2009 400 410
7. T.D. Bradley, J.S. Floras Obstructive sleep apnea and its cardiovascular consequences Lancet 373 2009 82 93
8. E.C. Fletcher, C. Costarangos, T. Miller The rate of fall of arterial oxyhemoglobin saturation in obstructive sleep apnea Chest 96 1989 717 722 (Pubitemid 19256166)
9. W.W. Flemons Clinical practice: obstructive sleep apnea N Engl J Med 347 2002 498 504 (Pubitemid 34879338)
10. V. Savransky, A. Nanayakkara, J. Li, S. Bevans, P.L. Smith, A. Rodriguez, V.Y. Polotsky Chronic intermittent hypoxia induces atherosclerosis Am J Respir Crit Care Med 175 2007 1290 1297 (Pubitemid 46905755)
11. V. Savransky, J. Jun, J. Li, A. Nanayakkara, S. Fonti, A.B. Moser, K.E. Steele, M.A. Schweitzer, S.P. Patil, S. Bhanot, A.R. Schwartz, V.Y. Polotsky Dyslipidemia and atherosclerosis induced by chronic intermittent hypoxia are attenuated by deficiency of stearoyl coenzyme A desaturase Circ Res 103 2008 1173 1180
12. J. Jun, C. Reinke, D. Bedja, D. Berkowitz, S. Bevans-Fonti, J. Li, L.A. Barouch, K. Gabrielson, V.Y. Polotsky Effect of intermittent hypoxia on atherosclerosis in apolipoprotein E-deficient mice Atherosclerosis 209 2010 381 386
13. R.C. Li, B. Haribabu, S.P. Mathis, J. Kim, D. Gozal Leukotriene B4 receptor-1 mediates intermittent hypoxia-induced atherogenesis Am J Respir Crit Care Med 184 2011 124 131
14. C. Arnaud, L. Poulain, P. Lévy, M. Dematteis Inflammation contributes to the atherogenic role of intermittent hypoxia in apolipoprotein-E knock out mice Atherosclerosis 219 2011 425 431
15. Fletcher EC. Invited review: physiological consequences of intermittent hypoxia: systemic blood pressure. J Appl Physiol 200, 90:1600-1605
16. S. de Frutos, L. Duling, D. AlÒ, T. Berry, O. Jackson-Weaver, M. Walker, N. Kanagy, L. González Bosc NFATc3 is required for intermittent hypoxia-induced hypertension Am J Physiol Heart Circ Physiol 294 2008 H2382 H2390
17. J. Li, L.N. Thorne, N.M. Punjabi, C.K. Sun, A.R. Schwartz, P.L. Smith, R.L. Marino, A. Rodriguez, W.C. Hubbard, C.P. O'Donnell, V.Y. Polotsky Intermittent hypoxia induces hyperlipidemia in lean mice Circ Res 97 2005 698 706 (Pubitemid 41416339)
18. J. Li, M. Bosch-Marce, A. Nanayakkara, V. Savransky, S.K. Fried, G.L. Semenza, V.Y. Polotsky Altered metabolic responses to intermittent hypoxia in mice with partial deficiency of hypoxia-inducible factor-1alpha Physiol Genomics 25 2006 450 457 (Pubitemid 43764766)
19. H. Greenberg, X. Ye, D. Wilson, A.K. Htoo, T. Henderson, S.F. Liu Chronic intermittent hypoxia activates nuclear factor-kappaB in cardiovascular tissues in vivo Biochem Biophys Res Commun 343 2006 591 596
20. C. Arnaud, P.C. Beguin, S. Lantuejoul, J.L. Pepin, C. Guillermet, G. Pelli, F. Burger, V. Buatois, C. Ribuot, J.P. Baguet, F. Mach, P. Levy, M. Dematteis The inflammatory preatherosclerotic remodeling induced by intermittent hypoxia is attenuated by RANTES/CCL5 inhibition Am J Respir Crit Care Med 184 2011 724 731
21. G. Fang, D. Song, G. Liu, X. Ye, S.F. Liu Chronic intermittent hypoxia facilitates high fat diet-induced atherosclerosis by an NF-κB-dependent mechanism Am J Respir Crit Care Med 181 2010 A6636
22. A. Daugherty Mouse models of atherosclerosis Am J Med Sci 323 2002 3 10 (Pubitemid 34650115)
23. N. Maeda Development of apolipoprotein E-deficient mice Arterioscler Thromb Vasc Biol 31 2011 1957 1962
24. A.K. Htoo, H. Greenberg, S. Tongia, G. Chen, T. Henderson, D. Wilson, S.F. Liu Activation of nuclear factor kappaB in obstructive sleep apnea: a pathway leading to systemic inflammation Sleep Breath 10 2006 43 50 (Pubitemid 44193436)
25. S. Ryan, C.T. Taylor, W.T. McNicholas Selective activation of inflammatory pathways by intermittent hypoxia in obstructive sleep apnea syndrome Circulation 112 2005 2660 2667 (Pubitemid 41532603)
26. L. Dyugovskaya, A. Polyakov, D. Ginsberg, P. Lavie, L. Lavie Molecular pathways of spontaneous and TNF-{alpha}-mediated neutrophil apoptosis under intermittent hypoxia Am J Respir Cell Mol Biol 45 2011 154 162
27. S. Ryan, C.T. Taylor, W.T. McNicholas Systemic inflammation: a key factor in the pathogenesis of cardiovascular complications in obstructive sleep apnea syndrome Thorax 64 2009 631 636
28. M.P. de Winther, E. Kanters, G. Kraal, M.H. Hofker Nuclear factor kappaB signaling in atherogenesis Arterioscler Thromb Vasc Biol 25 2005 904 914 (Pubitemid 40627833)
29. B. Pamukcu, G.Y. Lip, E. Shantsila The nuclear factor-kappa B pathway in atherosclerosis: a potential therapeutic target for atherothrombotic vascular disease Thromb Res 128 2011 117 123
30. H. Yang, L.J. Roberts, M.J. Shi, L.C. Zhou, B.R. Ballard, A. Richardson, Z.M. Guo Retardation of atherosclerosis by overexpression of catalase or both Cu/Zn- superoxide dismutase and catalase in mice lacking apolipoprotein E Circ Res 95 2004 1075 1081 (Pubitemid 39557894)
31. B.J. van Vlijmen, A.M. van den Maagdenberg, M.J. Gijbels, H. van der Boom, H. HogenEsch, R.R. Frants, M.H. Hofker, L.M. Havekes Diet-induced hyperlipoproteinemia and atherosclerosis in apolipoprotein E3-Leiden transgenic mice J Clin Invest 93 1994 1403 1410 (Pubitemid 24116375)
32. X. Ye, D. Ding, Z. Zhou, G. Chen, S.F. Liu Divergent roles of endothelial NF-κB in multiple organ injury and bacterial clearance in murine models of sepsis J Exp Med 205 2008 1303 1315 (Pubitemid 351831488)
33. J. Ding, D. Song, X. Ye, S.F. Liu A pivotal role of endothelial-specific NF-κB signaling in the pathogenesis of septic shock and septic vascular dysfunction J Immunol 183 2009 4031 4038
34. E.J. Lee, M.E. Woodske, B. Zou, C.P. O'Donnell Dynamic arterial blood gas analysis in conscious, unrestrained C57BL/6J mice during exposure to intermittent hypoxia J Appl Physiol 107 2009 290 294
35. S.F. Liu, A.B. Malik NF-κB activation as a pathologic mechanism of septic shock and inflammation Am J. Physiol Lung Cell Mol Physiol 290 2006 L622 L645
36. S. Vallabhapurapu, A. Matsuzawa, W. Zhang, P.H. Tseng, J.J. Keats, H. Wang, D.A. Vignali, P.L. Bergsagel, M. Karin Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-kappaB signaling Nat Immunol 9 2008 1364 1370
37. L. Brånén, L. Hovgaard, M. Nitulescu, E. Bengtsson, J. Nilsson, S. Jovinge Inhibition of tumor necrosis factor-alpha reduces atherosclerosis in apolipoprotein E knockout mice Arterioscler Thromb Vasc Biol 24 2004 2137 2142 (Pubitemid 39482442)
38. S.A. Huber, P. Sakkinen, D. Conze, N. Hardin, R. Tracy Interleukin-6 exacerbates early atherosclerosis in mice Arterioscler Thromb Vasc Biol 19 1999 2364 2367 (Pubitemid 29477837)
39. P.J. Kuhlencordt, J. Chen, F. Han, J. Astern, P.L. Huang Genetic deficiency of inducible nitric oxide synthase reduces atherosclerosis and lowers plasma lipid peroxides in apolipoprotein E-knockout mice Circulation 103 2001 3099 3104 (Pubitemid 32587858)
40. D. Steinberg Hypercholesterolemia and inflammation in atherogenesis: two sides of the same coin Mol Nutr Food Res 49 2005 995 998 (Pubitemid 41735560)
41. E. Signori, M. Rinaldi, D. Fioretti, S. Iurescia, D. Seripa, G. Perrone, G.D. Norata, A.L. Catapano, V.M. Fazio ApoE gene delivery inhibits severe hypercholesterolemia in newborn ApoE-KO mice Biochem Biophys Res Commun 361 2007 543 548 (Pubitemid 47193118)
42. A.M. Elsharkawy, F. Oakley, F. Lin, G. Packham, D.A. Mann, J. Mann The NF-kappaB p50: p50:HDAC-1 repressor complex orchestrates transcriptional inhibition of multiple pro-inflammatory genes J Hepatol 53 2010 519 527
43. H.T. Yang, Y. Wang, X. Zhao, E. Demissie, S. Papoutsopoulou, A. Mambole, A. O'Garra, M.F. Tomczak, S.E. Erdman, J.G. Fox, S.C. Ley, B.H. Horwitz NF-κB1 inhibits TLR-induced IFN-β production in macrophages through TPL-2-dependent ERK activation J Immunol 186 2011 1989 1996
44. S. Rajendrasozhan, S. Chung, I.K. Sundar, H. Yao, I. Rahman Targeted disruption of NF-{kappa}B1 (p50) augments cigarette smoke-induced lung inflammation and emphysema in mice: a critical role of p50 in chromatin remodeling Am J Physiol Lung Cell Mol Physiol 298 2010 L197 L209
45. S. Cao, X. Zhang, J.P. Edwards, D.M. Mosser NF-kappaB1 (p50) homodimers differentially regulate pro- and anti-inflammatory cytokines in macrophages J Biol Chem 281 2006 26041 26050 (Pubitemid 44401810)
46. D. Wang, I. Paz-Priel, A.D. Friedman NF-kappa B p50 regulates C/EBP alpha expression and inflammatory cytokine-induced neutrophil production J Immunol 182 2009 5757 5762
47. L. Fakhrzadeh, J.D. Laskin, D.L. Laskin Ozone-induced production of nitric oxide and TNF-alpha and tissue injury are dependent on NF-kappaB p50 Am J Physiol Lung Cell Mol Physiol 287 2004 L279 L285
48. S. Grundström, P. Anderson, P. Scheipers, A. Sundstedt Bcl-3 and NFkappaB p50-p50 homodimers act as transcriptional repressors in tolerant CD4+ T cells J Biol Chem 279 2004 8460 8468 (Pubitemid 38294739)
49. N.D. Perkins Integrating cell-signalling pathways with NF-kappaB and IKK function Nat Rev Mol Cell Biol 8 2007 49 62 (Pubitemid 46012014)
50. S.E. Lamhamedi-Cherradi, S. Zheng, B.A. Hilliard, L. Xu, J. Sun, S. Alsheadat, H.C. Liou, Y.H. Chen Transcriptional regulation of type I diabetes by NF-kappa B J Immunol 171 2003 4886-4592