O-GlcNAcase overexpression reverses coronary endothelial cell dysfunction in type 1 diabetic mice

American Journal of Physiology - Cell Physiology

Volumn 309, Issue 9, 2015, Pages C593-C599

  Makino, Ayako ^a,b,c   Dai, Anzhi ^b,c   Han, Ying ^a,b   Youssef, Katia D ^a   Wang, Weihua ^a   Donthamsetty, Reshma ^b   Scott, Brian T ^c   Wang, Hong ^c   Dillmann, Wolfgang H ^c  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Diabetic vascular complications; Endothelial cell dysfunction; Endothelium dependent hyperpolarization; GCA; Vascular rarefaction

Indexed keywords

ANGIOPOIETIN RECEPTOR; CONNEXIN 40; DOXYCYCLINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MESSENGER RNA; N ACETYLGLUCOSAMINE; O LINKED N ACETYLGLUCOSAMINE; TETRACYCLINE; UNCLASSIFIED DRUG; BETA N ACETYLHEXOSAMINIDASE; ENZYME INHIBITOR; GAP JUNCTION PROTEIN; HEXOSAMINIDASE C; HISTONE ACETYLTRANSFERASE; HYALURONOGLUCOSAMINIDASE; MGEA5 PROTEIN, HUMAN; N ACETYLGLUCOSAMINYLTRANSFERASE; TUMOR ANTIGEN;

ACYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAPILLARY DENSITY; CELL COUNT; CELL FUNCTION; CELL ISOLATION; CONTROLLED STUDY; CORONARY ARTERY DILATATION; DOWN REGULATION; ENDOTHELIAL DYSFUNCTION; ENZYME INHIBITION; GAP JUNCTION; GENE CONTROL; GENE OVEREXPRESSION; HUMAN; HYPERGLYCEMIA; HYPERPOLARIZATION; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; UPREGULATION; ANGIOGENESIS; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL CULTURE; CORONARY ARTERY DISEASE; CORONARY BLOOD VESSEL; DIABETIC ANGIOPATHY; DRUG EFFECTS; ENDOTHELIUM CELL; ENZYME INDUCTION; ENZYMOLOGY; EXPERIMENTAL DIABETES MELLITUS; GENETICS; GLYCOSYLATION; METABOLISM; PATHOPHYSIOLOGY; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; VASCULAR ENDOTHELIUM; VASODILATATION;

ANIMALS; ANTIGENS, NEOPLASM; BETA-N-ACETYLHEXOSAMINIDASES; CELLS, CULTURED; CONNEXINS; CORONARY ARTERY DISEASE; CORONARY VESSELS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIABETIC ANGIOPATHIES; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; ENZYME INDUCTION; ENZYME INHIBITORS; GLYCOSYLATION; HISTONE ACETYLTRANSFERASES; HUMANS; HYALURONOGLUCOSAMINIDASE; MALE; MICE, TRANSGENIC; N-ACETYLGLUCOSAMINYLTRANSFERASES; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; VASODILATION;

EID: 84946067197     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00069.2015     Document Type: Article

References (34)

1. Beleznai T, Bagi Z. Activation of hexosamine pathway impairs nitric oxide (NO)-dependent arteriolar dilations by increased protein O-GlcNAcylation. Vasc Pharmacol 56: 115-121, 2012.
2. Butkinaree C, Park K, Hart GW. O-linked β-N-acetylglucosamine (O-GlcNAc): extensive crosstalk with phosphorylation to regulate signaling and transcription in response to nutrients and stress. Biochim Biophys Acta 1800: 96-106, 2010.
3. Cho YE, Basu A, Dai A, Heldak M, Makino A. Coronary endothelial dysfunction and mitochondrial reactive oxygen species in type 2 diabetic mice. Am J Physiol Cell Physiol 305: C1033-C1040, 2013.
4. Cieniewski-Bernard C, Montel V, Stevens L, Bastide B. O-GlcNAcylation, an original modulator of contractile activity in striated muscle. J Muscle Res Cell Motil 30: 281-287, 2009.
5. De Vriese AS, Verbeuren TJ, Van de Voorde J, Lameire NH, Vanhoutte PM. Endothelial dysfunction in diabetes. Br J Pharmacol 130: 963-974, 2000.
6. Donovan K, Alekseev O, Qi X, Cho W, Azizkhan-Clifford J. OGlcNAc modification of transcription factor Sp1 mediates hyperglycemiainduced VEGF-A upregulation in retinal cells. Invest Ophthalmol Vis Sci 55: 7862-7873, 2014.
7. Du XL, Edelstein D, Dimmeler S, Ju Q, Sui C, Brownlee M. Hyperglycemia inhibits endothelial nitric oxide synthase activity by posttranslational modification at the Akt site. J Clin Invest 108: 1341-1348, 2001.
8. Estrada IA, Donthamsetty R, Debski P, Zhou MH, Zhang SL, Yuan JX, Han W, Makino A. STIM1 restores coronary endothelial function in type 1 diabetic mice. Circ Res 111: 1166-1175, 2012.
9. Federici M, Menghini R, Mauriello A, Hribal ML, Ferrelli F, Lauro D, Sbraccia P, Spagnoli LG, Sesti G, Lauro R. Insulin-dependent activation of endothelial nitric oxide synthase is impaired by O-linked glycosylation modification of signaling proteins in human coronary endothelial cells. Circulation 106: 466-472, 2002.
10. Gurel Z, Sieg KM, Shallow KD, Sorenson CM, Sheibani N. Retinal O-linked N-acetylglucosamine protein modifications: implications for postnatal retinal vascularization and the pathogenesis of diabetic retinopathy. Mol Vis 19: 1047-1059, 2013.
11. Hart GW, Housley MP, Slawson C. Cycling of O-linked β-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446: 1017-1022, 2007.
12. Hart GW, Kreppel LK, Comer FI, Arnold CS, Snow DM, Ye Z, Cheng X, DellaManna D, Caine DS, Earles BJ, Akimoto Y, Cole RN, Hayes BK. O-GlcNAcylation of key nuclear and cytoskeletal proteins: reciprocity with O-phosphorylation and putative roles in protein multimerization. Glycobiology 6: 711-716, 1996.
13. Hilgers RH, Xing D, Gong K, Chen YF, Chatham JC, Oparil S. Acute O-GlcNAcylation prevents inflammation-induced vascular dysfunction. Am J Physiol Heart Circ Physiol 303: H513-H522, 2012.
14. Issad T. O-GlcNAcylation of connexin 40: a sweet connection between diabetes and endothelial cell dysfunction? Focus on "O-GlcNAcase overexpression reverses coronary endothelial cell dysfunction in type 1 diabetic mice." Am J Physiol Cell Physiol (September 16, 2015). doi:10.1152/ ajpcell.00260.2015.
15. Issad T, Masson E, Pagesy P. O-GlcNAc modification, insulin signaling and diabetic complications. Diabetes Metab 36: 423-435, 2010.
16. Kim EJ, Kang DO, Love DC, Hanover JA. Enzymatic characterization of O-GlcNAcase isoforms using a fluorogenic GlcNAc substrate. Carbohydr Res 341: 971-982, 2006.
17. 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.
18. Li J, Huang CL, Zhang LW, Lin L, Li ZH, Zhang FW, Wang P. Isoforms of human O-GlcNAcase show distinct catalytic efficiencies. Biochemistry (Mosc) 75: 938-943, 2010.
19. Lima VV, Giachini FR, Carneiro FS, Carneiro ZN, Fortes ZB, Carvalho MH, Webb RC, Tostes RC. Increased vascular O-GlcNAcylation augments reactivity to constrictor stimuli. J Am Soc Hypertens 2: 410- 417, 2008.
20. 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.
21. Liu H, Yu S, Zhang H, Xu J. Identification of nitric oxide as an endogenous inhibitor of 26S proteasomes in vascular endothelial cells. PLos One 9: e98486, 2014.
22. Luo B, Soesanto Y, McClain DA. Protein modification by O-linked GlcNAc reduces angiogenesis by inhibiting Akt activity in endothelial cells. Arterioscler Thromb Vasc Biol 28: 651-657, 2008.
23. Makino A, Platoshyn O, Suarez J, Yuan JX, Dillmann WH. Downregulation of connexin40 is associated with coronary endothelial cell dysfunction in streptozotocin-induced diabetic mice. Am J Physiol Cell Physiol 295: C221-C230, 2008.
24. Mather KJ. The vascular endothelium in diabetes-a therapeutic target? Rev Endocr Metab Disord 14: 87-99, 2013.
25. Musicki B, Kramer MF, Becker RE, Burnett AL. Inactivation of phosphorylated endothelial nitric oxide synthase (Ser-1177) by O-GlcNAc in diabetes-associated erectile dysfunction. Proc Natl Acad Sci USA 102: 11870-11875, 2005.
26. Ngoh GA, Facundo HT, Zafir A, Jones SP. O-GlcNAc signaling in the cardiovascular system. Circ Res 107: 171-185, 2010.
27. Rakusan K, Hoofd L, Turek Z. The effect of cell size and capillary spacing on myocardial oxygen supply. Adv Exp Med Biol 180: 463-475, 1984.
28. Sasaki K, Donthamsetty R, Heldak M, Cho YE, Scott BT, Makino A. VDAC: old protein with new roles in diabetes. Am J Physiol Cell Physiol 303: C1055-C1060, 2012.
29. Shafi R, Iyer SP, Ellies LG, O'Donnell N, Marek KW, Chui D, Hart GW, Marth JD. The O-GlcNAc transferase gene resides on the X chromosome and is essential for embryonic stem cell viability and mouse ontogeny. Proc Natl Acad Sci USA 97: 5735-5739, 2000.
30. Shrikhande GV, Scali ST, da Silva CG, Damrauer SM, Csizmadia E, Putheti P, Matthey M, Arjoon R, Patel R, Siracuse JJ, Maccariello ER, Andersen ND, Monahan T, Peterson C, Essayagh S, Studer P, Guedes RP, Kocher O, Usheva A, Veves A, Kaczmarek E, Ferran C. O-glycosylation regulates ubiquitination and degradation of the antiinflammatory protein A20 to accelerate atherosclerosis in diabetic ApoEnull mice. PLos One 5: e14240, 2010.
31. Spiro RG. Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology 12: 43R-56R, 2002.
32. Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME. Essentials of Glycobiology (2nd ed.). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 2009.
33. Wang Y, Mehta PP, Rose B. Inhibition of glycosylation induces formation of open connexin-43 cell-to-cell channels and phosphorylation and Triton X-100 insolubility of connexin-43. J Biol Chem 270: 26581-26585, 1995.
34. Watson LJ, Long BW, DeMartino AM, Brittian KR, Readnower RD, Brainard RE, Cummins TD, Annamalai L, Hill BG, Jones SP. Cardiomyocyte Ogt is essential for postnatal viability. Am J Physiol Heart Circ Physiol 306: H142-H153, 2014.