Acute O-GlcNAcylation prevents inflammation-induced vascular dysfunction

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 303, Issue 5, 2012, Pages

  Hilgers, Rob H P ^a   Xing, Dongqi ^a   Gong, Kaizheng ^a,c   Chen, Yiu Fai ^a   Chatham, John C ^b   Oparil, Suzanne ^a  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c YANGZHOU UNIVERSITY   (China)

Author keywords

Aortic ring; D glucosamine; Endothelial dysfunction; O linked N acetyl glucosamine; Rat; Tumor necrosis factor

Indexed keywords

ACETYLCHOLINE; GLUCOSAMINE; INDUCIBLE NITRIC OXIDE SYNTHASE; LEVO GLUCOSE; N ACETYLGLUCOSAMINE; NITROPRUSSIDE SODIUM; PEROXYNITRITE; PHENYLEPHRINE; SUBSTANCE P; TUMOR NECROSIS FACTOR ALPHA;

ACYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA WALL; ARTICLE; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; MUSCLE CONTRACTILITY; MYOGRAPHY; NONHUMAN; OSMOSIS; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; VASCULAR RING;

ACETYLGLUCOSAMINE; ACYLATION; ANIMALS; AORTA, THORACIC; AORTIC DISEASES; BETA-N-ACETYLHEXOSAMINIDASES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INFLAMMATION MEDIATORS; MALE; MYOGRAPHY; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; PEROXYNITROUS ACID; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS; TISSUE CULTURE TECHNIQUES; TUMOR NECROSIS FACTOR-ALPHA; TYROSINE; VASOCONSTRICTION; VASOCONSTRICTOR AGENTS; VASODILATION; VASODILATOR AGENTS;

EID: 84865754804     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01175.2011     Document Type: Article

References (53)

1. Aoki N, Siegfried M, Lefer M. Anti-EDRF effect of tumor necrosis factor in isolated, perfused cat carotid arteries. Am J Physiol Heart Circ Physiol 256: H1509-H1512, 1989.
2. Busse R, Mülsch A. Induction of nitric oxide synthase by cytokines in vascular smooth muscle cells. FEBS Lett 275: 87-90, 1990.
3. Champattanachai V, Marchase RB, Chatham JC. Glucosamine protects neonatal cardiomyocytes from ischemia-reperfusion injury via increased protein-associated O-GlcNAc. Am J Physiol Cell Physiol 292: C178-C187, 2007.
4. Chatham JC, Nöt LG, F-ulöp N, Marchase RB. Hexosamine biosynthesis: the first line of defense against stress, ischemia and trauma. Shock 29: 431-440, 2008.
5. Chatham JC, Marchase RB. The role of protein O-linked β-N-acetylglucosamine in mediating cardiac stress responses. Biochim Biophys Acta 1800: 57-66, 2010.
6. Chen JT, Chen PL, Chang YH, Chien MW, Chen YH, Lu DW. Glucosamine sulphate inhibits leukocyte adhesion in response to cytokine stimulation of retinal pigment epithelial cells in vitro. Exp Eye Res 83: 1052-1062, 2006.
7. Chou MM, Vergnolle N, McDougall JJ, Wallace JL, Marty S, Teskey V, Buret AG. Effects of chondroitin and glucosamine sulphate in a dietary bar formulation on inflammation, interleukin-1β, matrix metallopro-tease-9, and cartilage damage in arthritis. Exp Biol Med (Maywood) 230: 255-262, 2005.
8. Copeland RJ, Bullen JW, Hart GW. Cross-talk between GlcNAcylation and phosphorylation: roles in insulin resistance and glucose toxicity. Am J Physiol Endocrinol Metab 295: E17-E28, 2008.
9. Di Wang H, Pagano PJ, Du Y, Cayatte AJ, Quinn MT, Brecher P, Cohen RA. Superoxide anion from the adventitia of the rat thoracic aorta inactivates nitric oxide. Circ Res 82: 810-818, 1998.
10. Félétou M, Köhler R, Vanhoutte PM. Endothelium-derived vasoactive factors and hypertension: possible roles in pathogenesis and as treatment targets. Curr Hypertens Rep 12: 267-275, 2010.
11. Fülöp N, Zhang Z, Marchase RB, Chatham JC. Glucosamine cardioprotection in perfused rat hearts associated with increased O-linked Nacetylglucosamine protein modification and altered p38 activation. Am J Physiol Heart Circ Physiol 292: H2227-H2236, 2007.
12. Garvey EP, Oplinger JA, Furfine ES, Kiff RJ, Laszlo F, Whittle BJ, Knowles RG. 1400W is a slow, tight binding, and highly selective inhibitor of inducible nitric oxide in vitro and in vivo. J Biol Chem 272: 4959-4963, 1997.
13. Goldberg H, Whiteside C, Fantus IG. O-linked β-N-acetylglucosamine (O-GlcNAc) supports p38 MAPK activation by glucose in glomerular mesangial cells. Am J Physiol Endocrinol Metab 301: E713-E726, 2011.
14. Goossens V, Grooten J, De Vos K, Fiers W. Direct evidence for tumor necrosis factor-induced mitochondrial reactive oxygen intermediates and their involvement in cytotoxicity. Proc Natl Acad Sci USA 92: 8115-8119, 1995.
15. Gryglewski RJ, Palmer RMJ, Moncada S. Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature 320: 454-456, 1986.
16. Gunnett CA, Lund DD, Chu Y, Brooks RMII, Faraci FM, Heistad DD. NO-dependent vasorelaxation is impaired after gene transfer of inducible NO-synthase. Arterioscler Thromb Vasc Biol 21: 1281-1287, 2001.
17. Harrison DG, Vinh A, Lob H, Madhur MS. Role of the adaptive immune system in hypertension. Curr Opin Pharmacol 20: 203-207, 2010.
18. Hart GW, Housley MP, Slawson C. Cycling of O-linked β-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446: 1017-1022, 2007.
19. Hoque AM, Papapetropoulos A, Venema RC, Catravas JD, Fuchs LC. Effects of antisense oligonucleotide to iNOS on hemodynamic and vascular changes induced by LPS. Am J Physiol Heart Circ Physiol 275: H1078-H1083, 1998.
20. Hua J, Suguro S, Hirano S, Sakamoto K, Nagaoka I. Preventive actions of a high dose of glucosamine on adjuvant arthritis in rats. Inflamm Res 54: 127-132, 2005.
21. Ischiropoulos H, Zhu L, Chen J, Tsai M, Martin JC, Smith CD, Beckman JS. Peroxynitrite-mediated tyrosine nitration catalyzed by superoxide dismutatase. Arch Biochem Biophys 298: 431-437, 1992.
22. Kessler P, Bauersachs J, Busse R, Schini-Kerth VB. Inhibition of inducible nitric oxide synthase restores endothelium-dependent relaxations in proinflammatory mediator-induced blood vessels. Arterioscler Thromb Vasc Biol 17: 1746-1755, 1997.
23. Kilbourn RG, Gross SS, Jubran A, Adams J, Griffith OW, Levi R, Lodato RF. NG-methyl-L-arginine inhibits tumor necrosis factor-induced hypotension: implications for the involvement of nitric oxide. Proc Natl Acad Sci USA 87: 3629-3632, 1990.
24. Kooy NW, Lewis SJ, Royall JA, Ye YZ, Kelly DR, Beckman JS. Extensive tyrosine nitration in human myocardial inflammation: evidence for the presence of peroxynitrite. Crit Care Med 25: 812-819, 1997.
25. Laczy B, Hill BG, Wang K, Paterson AJ, White CR, Xing D, Chen YF, Darley-Usmar V, Oparil S, Chatham JC. Protein O-GlcNAcylation: a new signaling paradigm for the cardiovascular system. Am J Physiol Heart Circ Physiol 296: H13-H28, 2009.
26. Lima VV, Giachini FR, Carneiro FS, Carneiro ZN, Saleh MA, Pollock DM, Fortes ZB, Carvalho MHC, Ergul A, Webb RC, Tostes RC. O-GlcNAcylation contributes to augmented vascular reactivity induced by endothelin 1. Hypertension 55: 180-188, 2010.
27. Lima VV, Giachini FR, Choi H, Carneiro FS, Carneiro ZN, Fortes ZB, Carvalho MH, Webb RC, Tostes RC. Impaired vasodilator activity in deoxycorticosterone acetate-salt hypertension is associated with increased protein O-GlcNAcylation. Hypertension 53: 166-174, 2009.
28. Lima VV, Giachini FR, Hardy DM, Webb RC, Tostes RC. O-GlcNacylation: a novel pathway contributes to the effects of endothelin in the vasculature. Am J Physiol Regul Integr Comp Physiol 300: R236-R250, 2011.
29. Liu J, Marchase RB, Chathan JC. Increased O-GlcNAc levels during reperfusion lead to improved functional recovery and reduced calpain proteolysis. Am J Physiol Heart Circ Physiol 293: H1391-H1396, 2007.
30. Ma L, Rudert WA, Harnaha J, Wright Machen J M, Lakomy R, Qian S, Lu L, Robbins PD, Trucco M, Giannoukakis N. Immunosuppresive effects of glucosamine. J Biol Chem 277: 39343-39349, 2002.
31. Marsh SA, Dell'Italia LJ, Chatham JC. Activation of the hexosamine biosynthesis pathway and protein O-GlcNAcylation modulate hypertrophic and cell signaling pathways in cardiomyocytes from diabetic mice. Amino Acids 40, 819-828, 2011.
32. McClain DA, Crook ED. Hexosamines and insuline resistance. Diabetes 45: 1003-1009, 1996.
33. Meininger CJ, Kelly KA, Li H, Haynes TE, Wu G. Glucosamine inhibits inducible nitric oxide synthesis. Biochem Biophys Res Commun 279: 234-239, 2000.
34. Moritz T, Niederle N, Baumann J, May D, Kurschel E, Osieka R, Kempeni J, Schlick E, Schmidt CG. Phase I study of recombinant human necrosis factor alpha in advanced malignant disease. Cancer Immunol Immunother 29: 144-150, 1989.
35. Ohtsuda T, Kubota A, Hirano T, Watanabe K, Yoshida H, Tsurufuji M, Iizuka Y, Konishi K, Tsurufuji S. Glucocorticoid-mediated gene suppression of rat cytokine-induced neutrophil chemoattractant CINC/gro, a member of the interleukin-8 family, through impairment of NF-κB activation. J Biol Chem 271: 1651-1659, 1996.
36. Rafi MM, Yadav PN, Rossi AO. Glucosamine inhibits LPS-induced COX-2 and iNOS expression in mouse macrophage cells (RAW 264.7) by inhibition of p38-MAP kinase and transcription factor NF-κB. Mol Nutr Food Res 51: 587-593, 2007.
37. Singer II, Kawka DW, Scott S, Weidner JR, Mumford RA, Riehl TE, Stenson WF. Expression of inducible nitric oxide synthase and nitrotyrosine in colonic epithelium in inflammatory bowel disease. Gastroenterology 111: 871-885, 1996.
38. Takahashi K, Ando K, Ono A, Shimosawa T, Ogata E, Fujita T. Tumor necrosis factor-α induces vascular hyporesponsiveness in Sprague-Dawley rats. Life Sci 50: 1437-1444, 1992.
39. Takahashi M, Suzuki E, Takeda R, Oba S, Nishimatsu H, Kimura K, Nagano T, Nagai R, Hirata Y. Angiotensin II and tumor necrosis factor-α synergistically promote monocyte chemoattractant protein-1 expression: roles of NF-κB, p38, and reactive oxygen species. Am J Physiol Heart Circ Physiol 294: H2879-H2888, 2008.
40. Thiemermann C, Szabó C, Mitchell JA, Vane JR. Vascular hyporeactivity to vasoconstrictor agents and hemodynamic decompensation in hemorrhagic shock is mediated by nitric oxide. Proc Natl Acad Sci USA 90: 267-271, 1993.
41. Traxinger RR, Marshall S. Coordinated regulation of glutamine:fructose-6-phosphate amidotransferase activity by insulin, glucose and glutamine. Role of hexosamine biosynthesis in enzyme regulation. J Biol Chem 266: 10148-10154, 1991.
42. Ungvari Z, Csiszar A, Edwards JG, Kaminski PM, Wolin MS, Kaley G, Koller A. Increased superoxide production in coronary arteries in hyperhomocysteinemia: role of tumor necrosis factor-α, NAD(P)H oxidase, and inducible nitric oxide synthase. Arterioscler Thromb Vasc Biol 23: 418-424, 2003.
43. phox and iNOS expression. Rheumatology (Oxford) 47: 31-35, 2008.
44. Wimalasundera R, Fexby S, Regan L, Thom SA, Hughes AD. Effect of tumour necrosis factor-α and interleukin 1β on endothelium-dependent relaxation in rat mesenteric resistance arteries in vitro. Br J Pharmacol 138: 1285-1294, 2003.
45. Xie QW, Whisnant R, Nathan C. Promotor of the mouse gene encoding calcium-independent nitric oxide synthase confers inducibility by interferon gamma and bacterial polysaccharide. J Exp Med 177: 1779-1784, 1993.
46. Xing D, Feng W, Nöt LG, Miller AP, Zhang Y, Chen YF, Majid-Hassan E, Chatham JC, Oparil S. Increased protein O-GlcNAc modification inhibits inflammatory and neointimal responses to acute endoluminal arterial injury. Am J Physiol Heart Circ Physiol 295: H335-H342, 2008.
47. Xing D, Gong K, Feng W, Nozell SE, Chen YF, Chatham JC, Oparil S. O-GlcNAc modification of NFkB p65 inhibits TNFα-induced inflammatory mediator expression in rat aortic smooth muscle cells. PLos One 6: e24021, 2011.
48. Yang S, Zou LY, Bounelis P, Chaudry I, Chatham JC, Marchase RB. Glucosamine administration during resuscitation improves organ function following trauma-hemorrhage. Shock 25: 600-607, 2006.
49. Yuzwa SA, Macauley MS, Heinonen JE, Shan X, Dennis RJ, He Y, Whitworth GE, Stubbs KA, McEachern EJ, Davies GJ, Vocadlo DJ. A potent mechanism-inspired O-GlcNAcase inhibitor that blocks tau in vivo. Nat Chem Biol 4 483-490, 2008.
50. Zemse SM, Chiao CW, Hilgers RH, Webb RC. Interleukin-10 inhibits the in vivo and in vitro adverse effects of TNF-α on the endothelium of murine aorta. Am J Physiol Heart Circ Physiol 299: H1160-H1167, 2010.
51. Zeidan Q, Hart GW. The intersections between O-GlcNAcylation and phosphorylation: implications for multiple signaling pathways. J Cell Sci 123: 13-22, 2010.
52. Zhang GX, Yu S, Gran B, Rostami A. Glucosamine abrogates the acute phase of experimental autoimmune encephalomyelitis by induction of Th2 response. J Immunol 175: 7202-7208, 2005.
53. Zou L, Yang S, Champattanachai V, Hu S, Chaudry IH, Marchase RB, Chatham JC. Glucosamine improves cardiac function following trauma-hemorrhage by increased protein O-GlcNAcylation of NF-κB signaling. Am J Physiol Heart Circ Physiol 296: H515-H523, 2009.