High-fat diet increases O-GlcNAc levels in cerebral arteries: Link to vascular dysfunction associated with hyperlipidaemia/obesity?

Clinical Science

Volumn 130, Issue 11, 2016, Pages 871-880

  Lima, Victor V ^a   Giachini, Fernanda R ^a   Matsumoto, Takayuki ^b   Li, Weiguo ^c   Bressan, Alecsander F M ^a   Chawla, Dhruv ^c   Webb, R Clinton ^c   Ergul, Adviye ^c   Tostes, Rita C ^d  

^a FEDERAL UNIVERSITY OF MATO GROSSO   (Brazil)

^b HOSHI UNIVERSITY   (Japan)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Basilar artery; Cerebral artery; High fat; O GlcNAc; Vascular contraction

Indexed keywords

15 HYDROXY 11ALPHA,9ALPHA EPOXYMETHANOPROSTA 5,13 DIENOIC ACID; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; SEROTONIN; TRIACYLGLYCEROL; BETA N ACETYLHEXOSAMINIDASE; HEXOSAMINIDASE C; MITOGEN ACTIVATED PROTEIN KINASE; N ACETYLGLUCOSAMINE; N ACETYLGLUCOSAMINYLTRANSFERASE; O-GLCNAC TRANSFERASE;

ANIMAL EXPERIMENT; ARTICLE; BASILAR ARTERY; BLOOD PRESSURE MEASUREMENT; BODY WEIGHT; BRAIN ARTERY; CEREBROVASCULAR DISEASE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME PHOSPHORYLATION; HYPERLIPIDEMIA; LIPID DIET; MALE; METABOLIC PARAMETERS; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN PROCESSING; RAT; TRIACYLGLYCEROL BLOOD LEVEL; WESTERN BLOTTING; ANIMAL; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; WISTAR RAT;

ACETYLGLUCOSAMINE; ANIMALS; BETA-N-ACETYLHEXOSAMINIDASES; CEREBRAL ARTERIES; DIET, HIGH-FAT; HYPERLIPIDEMIAS; MALE; MITOGEN-ACTIVATED PROTEIN KINASES; N-ACETYLGLUCOSAMINYLTRANSFERASES; OBESITY; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS, WISTAR;

EID: 85006131049     PISSN: 01435221     EISSN: 14708736     Source Type: Journal    
DOI: 10.1042/CS20150777     Document Type: Article

References (44)

1. Wilde, D.W., Massey, K.D., Walker, G.K., Vollmer, A. and Grekin, R.J. (2000) High-fat diet elevates blood pressure and cerebrovascular muscle Ca2+ current. Hypertension 35, 832-837
2. Li, W., Prakash, R., Chawla, D., Du, W., Didion, S.P., Filosa, J.A., Zhang, Q., Brann, D.W., Lima, V.V., Tostes, R.C. et al. (2013) Early effects of high-fat diet on neurovascular function and focal ischemic brain injury. Am. J. Physiol. Regul. Integr. Comp. Physiol. 304, R1001-R1008
3. d'Uscio, L.V., Smith, L.A. and Katusic, Z.S. (2001) Hypercholesterolemia impairs endothelium-dependent relaxations in common carotid arteries of apolipoprotein e-deficient mice. Stroke 32, 2658-2664
4. Osmond, J.M., Mintz, J.D., Dalton, B. and Stepp, D.W. (2009) Obesity increases blood pressure, cerebral vascular remodeling, and severity of stroke in the Zucker rat. Hypertension 53, 381-386
5. Kitayama, J., Faraci, F.M., Lentz, S.R. and Heistad, D.D. (2007) Cerebral vascular dysfunction during hypercholesterolemia. Stroke 38, 2136-2141
6. Langdon, K.D., Clarke, J. and Corbett, D. (2011) Long-term exposure to high fat diet is bad for your brain: exacerbation of focal ischemic brain injury. Neuroscience 182, 82-87
7. Deutsch, C., Portik-Dobos, V., Smith, A.D., Ergul, A. and Dorrance, A.M. (2009) Diet-induced obesity causes cerebral vessel remodeling and increases the damage caused by ischemic stroke. Microvasc. Res. 78, 100-106
8. Sachidanandam, K., Hutchinson, J.R., Elgebaly, M.M., Mezzetti, E.M., Wang, M.H. and Ergul, A. (2009) Differential effects of diet-induced dyslipidemia and hyperglycemia on mesenteric resistance artery structure and function in type 2 diabetes. J. Pharmacol. Exp. Ther. 328, 123-130
9. Torres, C.R. and Hart, G.W. (1984) Topography and polypeptide distribution of terminal N-acetylglucosamine residues on the surfaces of intact lymphocytes. Evidence for O-linked GlcNAc. J. Biol. Chem. 259, 3308-3317
10. Lima, V.V., Giachini, F.R., Carneiro, F.S., Carneiro, Z.N., Saleh, M.A., Pollock, D.M., Fortes, Z.B., Carvalho, M.H., Ergul, A., Webb, R.C. et al. (2010) O-GlcNAcylation contributes to augmented vascular reactivity induced by endothelin 1. Hypertension 55, 180-188
11. Lima, V.V., Giachini, F.R., Choi, H., Carneiro, F.S., Carneiro, Z.N., Fortes, Z.B., Carvalho, M.H., Webb, R.C. and Tostes, R.C. (2009) Impaired vasodilator activity in deoxycorticosterone acetate-salt hypertension is associated with increased protein O-GlcNAcylation. Hypertension 53, 166-174
12. Kim do, H., Seok, Y.M., Kim, I.K., Lee, I.K., Jeong, S.Y. and Jeoung, N.H. (2011) Glucosamine increases vascular contraction through activation of RhoA/Rho kinase pathway in isolated rat aorta. BMB Rep. 44, 415-420
13. Beleznai, T. and Bagi, Z. (2012) Activation of hexosamine pathway impairs nitric oxide (NO)-dependent arteriolar dilations by increased protein O-GlcNAcylation. Vascul. Pharmacol. 56, 115-121
14. Hilgers, R.H., Xing, D., Gong, K., Chen, Y.F., Chatham, J.C. and Oparil, S. (2012) Acute O-GlcNAcylation prevents inflammation-induced vascular dysfunction. Am. J. Physiol. Heart Circ. Physiol. 303, H513-H522
15. Yang, Y.R., Jang, H.J., Lee, Y.H., Kim, I.S., Lee, H., Ryu, S.H. and Suh, P.G. (2015) O-GlcNAc cycling enzymes control vascular development of the placenta by modulating the levels of HIF-1a. Placenta 15, 1-6
16. Vosseller, K. (2010) O-GlcNAc and aging: C. elegans as a genetic model to test O-GlcNAc roles in type II diabetic insulin resistance. Aging (Albany NY) 2, 749-751
17. Li, S.Y., Liu, Y., Sigmon, V.K., McCort, A. and Ren, J. (2005) High-fat diet enhances visceral advanced glycation end products, nuclear O-Glc-Nac modification, p38 mitogen-activated protein kinase activation and apoptosis. Diabetes Obes. Metab. 7, 448-454
18. Laczy, B., Hill, B.G., Wang, K., Paterson, A.J., White, C.R., Xing, D., Chen, Y.F., Darley-Usmar, V., Oparil, S. and Chatham, J.C. (2009) Protein O-GlcNAcylation: a new signaling paradigm for the cardiovascular system. Am. J. Physiol. Heart Circ. Physiol. 296, H13-H28
19. Dias, W.B. and Hart, G.W. (2007) O-GlcNAc modification in diabetes and Alzheimer's disease. Mol. Biosyst. 3, 766-772
20. Fulop, N., Marchase, R.B. and Chatham, J.C. (2007) Role of protein O-linked N-acetyl-glucosamine in mediating cell function and survival in the cardiovascular system. Cardiovasc. Res. 73, 288-297
21. Medford, H.M., Chatham, J.C. and Marsh, S.A. (2012) Chronic ingestion of a Western diet increases O-linked-beta-N-acetylglucosamine (O-GlcNAc) protein modification in the rat heart. Life Sci. 90, 883-888
22. Lagerlof, O. and Hart, G.W. (2014) O-GlcNAcylation of neuronal proteins: roles in neuronal functions and in neurodegeneration. Adv. Neurobiol. 9, 343-366
23. Liu, Y., Li, X., Yu, Y., Shi, J., Liang, Z., Run, X., Li, Y., Dai, C.L., Grundke-Iqbal, I., Iqbal, K. et al. (2012) Developmental regulation of protein O-GlcNAcylation, O-GlcNAc transferase, and O-GlcNAcase in mammalian brain. PLoS One 7, e43724
24. Faraci, F.M. and Heistad, D.D. (1990) Regulation of large cerebral arteries and cerebral microvascular pressure. Circ. Res. 66, 8-17
25. Devuyst, G., Bogousslavsky, J., Meuli, R., Moncayo, J., de Freitas, G. and van Melle, G. (2002) Stroke or transient ischemic attacks with basilar artery stenosis or occlusion: clinical patterns and outcome. Arch. Neurol. 59, 567-573
26. Renaud, S.C. (2001) Diet and stroke. J. Nutr. Health Aging. 5, 167-172
27. Lima, V.V., Giachini, F.R., Carneiro, F.S., Carneiro, Z.N., Fortes, Z.B., Carvalho, M.H.C., Webb, R.C. and Tostes, R.C. (2008) Increased vascular O-GlcNAcylation augments reactivity to constrictor stimuli. J. Am. Soc. Hypertens. 2, 410-417
28. Lima, V.V., Giachini, F.R., Carneiro, F.S., Carvalho, M.H., Fortes, Z.B., Webb, R.C. and Tostes, R.C. (2011) O-GlcNAcylation contributes to the vascular effects of ET-1 via activation of the RhoA/Rho-kinase pathway. Cardiovasc. Res. 89, 614-622
29. Whitworth, G.E., Macauley, M.S., Stubbs, K.A., Dennis, R.J., Taylor, E.J., Davies, G.J., Greig, I.R. and Vocadlo, D.J. (2007) Analysis of PUGNAc and NAG-thiazoline as transition state analogues for human O-GlcNAcase: mechanistic and structural insights into inhibitor selectivity and transition state poise. J. Am. Chem. Soc. 129, 635-644
30. Hu, P., Shimoji, S. and Hart, G.W. (2010) Site-specific interplay between O-GlcNAcylation and phosphorylation in cellular regulation. FEBS Lett. 584, 2526-2538
31. Chen, Q.W., Edvinsson, L. and Xu, C.B. (2009) Role of ERK/MAPK in endothelin receptor signaling in human aortic smooth muscle cells. BMC Cell Biol. 10, 52
32. Naderali, E.K., Brown, M.J., Pickavance, L.C., Wilding, J.P., Doyle, P.J. and Williams, G. (2001) Dietary obesity in the rat induces endothelial dysfunction without causing insulin resistance: a possible role for triacylglycerols. Clin. Sci. (Lond.) 101, 499-506
33. Naderali, E.K. and Williams, G. (2001) Effects of short-term feeding of a highly palatable diet on vascular reactivity in rats. Eur. J. Clin. Invest. 31, 1024-1028
34. Wang, Z., Gucek, M. and Hart, G.W. (2008) Cross-talk between GlcNAcylation and phosphorylation: site-specific phosphorylation dynamics in response to globally elevated O-GlcNAc. Proc. Natl. Acad. Sci. U.S.A. 105, 13793-13798
35. Buse, M.G., Robinson, K.A., Gettys, T.W., McMahon, E.G. and Gulve, E.A. (1997) Increased activity of the hexosamine synthesis pathway in muscles of insulin-resistant ob/ob mice. Am. J. Physiol. 272, E1080-E1088
36. Wang, J., Liu, R., Hawkins, M., Barzilai, N. and Rossetti, L. (1998) A nutrient-sensing pathway regulates leptin gene expression in muscle and fat. Nature 393, 684-688
37. Lima, V.V., Rigsby, C.S., Hardy, D.M., Webb, R.C. and Tostes, R.C. (2009) O-GlcNAcylation: a novel post-translational mechanism to alter vascular cellular signaling in health and disease: focus on hypertension. J. Am. Soc. Hypertens. 3, 374-387
38. Hart, G.W., Housley, M.P. and Slawson, C. (2007) Cycling of O-linked beta-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446, 1017-1022
39. Spiro, R.G. (2002) Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology 12, 43R-56R
40. Wang, Y., Yan, T., Wang, Q., Wang, W., Xu, J., Wu, X. and Ji, H. (2008) PKC-dependent extracellular signal-regulated kinase 1/2 pathway is involved in the inhibition of Ib on AngiotensinII-induced proliferation of vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 375, 151-155
41. Dias, W.B., Cheung, W.D., Wang, Z. and Hart, G.W. (2009) Regulation of calcium/calmodulin-dependent kinase IV by O-glcnac modification. J. Biol. Chem. 284, 21327-21337
42. Pearson, G., Robinson, F., Beers Gibson, T., Xu, B.E., Karandikar, M., Berman, K. and Cobb, M.H. (2001) Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 22, 153-183
43. Gross, B.J., Kraybill, B.C. and Walker, S. (2005) Discovery of O-GlcNAc transferase inhibitors. J. Am. Chem. Soc. 127, 14588-14589
44. Li, S.Y., Sigmon, V.K., Babcock, S.A. and Ren, J. (2007) Advanced glycation endproduct induces ROS accumulation, apoptosis, MAP kinase activation and nuclear O-GlcNAcylation in human cardiac myocytes. Life Sci. 80, 1051-1056