O-GlcNAcylation, enemy or ally during cardiac hypertrophy development?

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1862, Issue 12, 2016, Pages 2232-2243

  Mailleux, Florence ^a   Gélinas, Roselle ^c,d   Beauloye, Christophe ^a,b   Horman, Sandrine ^a   Bertrand, Luc ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b CLINIQUES UNIVERSITAIRES SAINT LUC   (Belgium)

^c MONTREAL HEART INSTITUTE   (Canada)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Cardiac disease; Cardiac hypertrophy; Diabetes; Glucose; Protein O GlcNAcylation

Indexed keywords

CALCIUM; HEXOSAMINE; TRANSCRIPTION FACTOR;

ACYLATION; BIOSYNTHESIS; BLEEDING; DIABETES MELLITUS; HEART LEFT VENTRICLE FAILURE; HEART MUSCLE CONTRACTILITY; HEART MUSCLE ISCHEMIA; HEART VENTRICLE HYPERTROPHY; HUMAN; METABOLIC REGULATION; NITROSATIVE STRESS; NONHUMAN; O GLCNACYLATION; OXIDATIVE STRESS; PATHOLOGY; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW;

EID: 84993988689     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2016.08.012     Document Type: Review

References (117)

1. [1] Katholi, R.E., Couri, D.M., Left ventricular hypertrophy: major risk factor in patients with hypertension: update and practical clinical applications. Int. J. Hypertens., 2011, 2011, 495349.
2. [2] Lorell, B.H., Carabello, B.A., Left ventricular hypertrophy: pathogenesis, detection, and prognosis. Circulation 102 (2000), 470–479.
3. [3] van Berlo, J.H., Maillet, M., Molkentin, J.D., Signaling effectors underlying pathologic growth and remodeling of the heart. J. Clin. Invest. 123 (2013), 37–45.
4. [4] Heineke, J., Molkentin, J.D., Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat. Rev. Mol. Cell Biol. 7 (2006), 589–600.
5. [5] Stanley, W.C., Recchia, F.A., Lopaschuk, G.D., Myocardial substrate metabolism in the normal and failing heart. Physiol. Rev. 85 (2005), 1093–1129.
6. [6] van Bilsen, M., van Nieuwenhoven, F.A., van der Vusse, G.J., Metabolic remodelling of the failing heart: beneficial or detrimental?. Cardiovasc. Res. 81 (2009), 420–428.
7. [7] Bernardo, B.C., Weeks, K.L., Pretorius, L., McMullen, J.R., Molecular distinction between physiological and pathological cardiac hypertrophy: experimental findings and therapeutic strategies. Pharmacol. Ther. 128 (2010), 191–227.
8. [8] Wells, L., Whelan, S.A., Hart, G.W., O-GlcNAc: a regulatory post-translational modification. Biochem. Biophys. Res. Commun. 302 (2003), 435–441.
9. [9] Butkinaree, C., Park, K., Hart, G.W., O-linked beta-N-acetylglucosamine (O-GlcNAc): extensive crosstalk with phosphorylation to regulate signaling and transcription in response to nutrients and stress. Biochim. Biophys. Acta 1800 (2010), 96–106.
10. [10] Hanover, J.A., Krause, M.W., Love, D.C., Bittersweet memories: linking metabolism to epigenetics through O-GlcNAcylation. Nat. Rev. Mol. Cell Biol. 13 (2012), 312–321.
11. [11] Darley-Usmar, V.M., Ball, L.E., Chatham, J.C., Protein O-linked beta-N-acetylglucosamine: a novel effector of cardiomyocyte metabolism and function. J. Mol. Cell. Cardiol. 52 (2012), 538–549.
12. [12] Vercoutter-Edouart, A.S., Yazidi-Belkoura, I.E., Guinez, C., Baldini, S., Leturcq, M., Mortuaire, M., Mir, A.M., Steenackers, A., Dehennaut, V., Pierce, A., Lefebvre, T., Detection and identification of O-GlcNAcylated proteins by proteomic approaches. Proteomics 15 (2015), 1039–1050.
13. [13] Zachara, N.E., O'Donnell, N., Cheung, W.D., Mercer, J.J., Marth, J.D., Hart, G.W., Dynamic O-GlcNAc modification of nucleocytoplasmic proteins in response to stress. A survival response of mammalian cells. J. Biol. Chem. 279 (2004), 30133–30142.
14. [14] Champattanachai, V., Marchase, R.B., Chatham, J.C., Glucosamine protects neonatal cardiomyocytes from ischemia-reperfusion injury via increased protein-associated O-GlcNAc. Am. J. Physiol. Cell Physiol. 292 (2007), C178–C187.
15. [15] Ngoh, G.A., Facundo, H.T., Hamid, T., Dillmann, W., Zachara, N.E., Jones, S.P., Unique hexosaminidase reduces metabolic survival signal and sensitizes cardiac myocytes to hypoxia/reoxygenation injury. Circ. Res. 104 (2009), 41–49.
16. [16] Bond, M.R., Hanover, J.A., O-GlcNAc cycling: a link between metabolism and chronic disease. Annu. Rev. Nutr. 33 (2013), 205–229.
17. [17] Napoli, C., Lerman, L.O., de Nigris, F., Sica, V., c-Myc oncoprotein: a dual pathogenic role in neoplasia and cardiovascular diseases?. Neoplasia (New York, N.Y.) 4 (2002), 185–190.
18. [18] Chou, T.Y., Hart, G.W., Dang, C.V., c-Myc is glycosylated at threonine 58, a known phosphorylation site and a mutational hot spot in lymphomas. J. Biol. Chem. 270 (1995), 18961–18965.
19. [19] Torres, C.R., Hart, G.W., Topography and polypeptide distribution of terminal N-acetylglucosamine residues on the surfaces of intact lymphocytes. Evidence for O-linked GlcNAc. J. Biol. Chem. 259 (1984), 3308–3317.
20. [20] Ma, J., Hart, G.W., O-GlcNAc profiling: from proteins to proteomes. Clin. Proteomics, 11, 2014, 8.
21. [21] Boehmelt, G., Wakeham, A., Elia, A., Sasaki, T., Plyte, S., Potter, J., Yang, Y., Tsang, E., Ruland, J., Iscove, N.N., Dennis, J.W., Mak, T.W., Decreased UDP-GlcNAc levels abrogate proliferation control in EMeg32-deficient cells. EMBO J. 19 (2000), 5092–5104.
22. [22] Greig, K.T., Antonchuk, J., Metcalf, D., Morgan, P.O., Krebs, D.L., Zhang, J.G., Hacking, D.F., Bode, L., Robb, L., Kranz, C., de Graaf, C., Bahlo, M., Nicola, N.A., Nutt, S.L., Freeze, H.H., Alexander, W.S., Hilton, D.J., Kile, B.T., Agm1/Pgm3-mediated sugar nucleotide synthesis is essential for hematopoiesis and development. Mol. Cell. Biol. 27 (2007), 5849–5859.
23. [23] Dassanayaka, S., Jones, S.P., O-GlcNAc and the cardiovascular system. Pharmacol. Ther. 142 (2014), 62–71.
24. [24] Dong, D.L., Hart, G.W., Purification and characterization of an O-GlcNAc selective N-acetyl-beta-D-glucosaminidase from rat spleen cytosol. J. Biol. Chem. 269 (1994), 19321–19330.
25. [25] Gao, Y., Wells, L., Comer, F.I., Parker, G.J., Hart, G.W., Dynamic O-glycosylation of nuclear and cytosolic proteins: cloning and characterization of a neutral, cytosolic beta-N-acetylglucosaminidase from human brain. J. Biol. Chem. 276 (2001), 9838–9845.
26. [26] Kreppel, L.K., Blomberg, M.A., Hart, G.W., Dynamic glycosylation of nuclear and cytosolic proteins. Cloning and characterization of a unique O-GlcNAc transferase with multiple tetratricopeptide repeats. J. Biol. Chem. 272 (1997), 9308–9315.
27. [27] Keembiyehetty, C., Love, D.C., Harwood, K.R., Gavrilova, O., Comly, M.E., Hanover, J.A., Conditional knock-out reveals a requirement for O-linked N-acetylglucosaminase (O-GlcNAcase) in metabolic homeostasis. J. Biol. Chem. 290 (2015), 7097–7113.
28. [28] Yang, Y.R., Song, M., Lee, H., Jeon, Y., Choi, E.J., Jang, H.J., Moon, H.Y., Byun, H.Y., Kim, E.K., Kim, D.H., Lee, M.N., Koh, A., Ghim, J., Choi, J.H., Lee-Kwon, W., Kim, K.T., Ryu, S.H., Suh, P.G., O-GlcNAcase is essential for embryonic development and maintenance of genomic stability. Aging Cell 11 (2012), 439–448.
29. [29] Shafi, R., Iyer, S.P., Ellies, L.G., O'Donnell, N., Marek, K.W., Chui, D., Hart, G.W., Marth, J.D., 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. U. S. A. 97 (2000), 5735–5739.
30. [30] Marshall, S., Bacote, V., Traxinger, R.R., Discovery of a metabolic pathway mediating glucose-induced desensitization of the glucose transport system. Role of hexosamine biosynthesis in the induction of insulin resistance. J. Biol. Chem. 266 (1991), 4706–4712.
31. [31] Ortiz-Meoz, R.F., Jiang, J., Lazarus, M.B., Orman, M., Janetzko, J., Fan, C., Duveau, D.Y., Tan, Z.W., Thomas, C.J., Walker, S., A small molecule that inhibits OGT activity in cells. ACS Chem. Biol. 10 (2015), 1392–1397.
32. [32] Haltiwanger, R.S., Grove, K., Philipsberg, G.A., Modulation of O-linked N-acetylglucosamine levels on nuclear and cytoplasmic proteins in vivo using the peptide O-GlcNAc-beta-N-acetylglucosaminidase inhibitor O-(2-acetamido-2-deoxy-D-glucopyranosylidene)amino-N-phenylcarbamate. J. Biol. Chem. 273 (1998), 3611–3617.
33. [33] Ostrowski, A., van Aalten, D.M., Chemical tools to probe cellular O-GlcNAc signalling. Biochem. J. 456 (2013), 1–12.
34. [34] Macauley, M.S., Whitworth, G.E., Debowski, A.W., Chin, D., Vocadlo, D.J., O-GlcNAcase uses substrate-assisted catalysis: kinetic analysis and development of highly selective mechanism-inspired inhibitors. J. Biol. Chem. 280 (2005), 25313–25322.
35. [35] Dorfmueller, H.C., Borodkin, V.S., Schimpl, M., Shepherd, S.M., Shpiro, N.A., van Aalten, D.M., GlcNAcstatin: a picomolar, selective O-GlcNAcase inhibitor that modulates intracellular O-glcNAcylation levels. J. Am. Chem. Soc. 128 (2006), 16484–16485.
36. [36] Yuzwa, S.A., Macauley, M.S., Heinonen, J.E., Shan, X., Dennis, R.J., He, Y., Whitworth, G.E., Stubbs, K.A., McEachern, E.J., Davies, G.J., Vocadlo, D.J., A potent mechanism-inspired O-GlcNAcase inhibitor that blocks phosphorylation of tau in vivo. Nat. Chem. Biol. 4 (2008), 483–490.
37. [37] Persiani, S., Roda, E., Rovati, L.C., Locatelli, M., Giacovelli, G., Roda, A., Glucosamine oral bioavailability and plasma pharmacokinetics after increasing doses of crystalline glucosamine sulfate in man. Osteoarthr. Cartil. 13 (2005), 1041–1049.
38. [38] Watson, L.J., Long, B.W., DeMartino, A.M., Brittian, K.R., Readnower, R.D., Brainard, R.E., Cummins, T.D., Annamalai, L., Hill, B.G., Jones, S.P., Cardiomyocyte Ogt is essential for postnatal viability. Am. J. Physiol. Heart Circ. Physiol. 306 (2014), H142–H153.
39. [39] Ngoh, G.A., Watson, L.J., Facundo, H.T., Dillmann, W., Jones, S.P., Non-canonical glycosyltransferase modulates post-hypoxic cardiac myocyte death and mitochondrial permeability transition. J. Mol. Cell. Cardiol. 45 (2008), 313–325.
40. [40] Champattanachai, V., Marchase, R.B., Chatham, J.C., Glucosamine protects neonatal cardiomyocytes from ischemia-reperfusion injury via increased protein O-GlcNAc and increased mitochondrial Bcl-2. Am. J. Physiol. Cell Physiol. 294 (2008), C1509–C1520.
41. [41] Liu, J., Pang, Y., Chang, T., Bounelis, P., Chatham, J.C., Marchase, R.B., Increased hexosamine biosynthesis and protein O-GlcNAc levels associated with myocardial protection against calcium paradox and ischemia. J. Mol. Cell. Cardiol. 40 (2006), 303–312.
42. [42] Fulop, N., Zhang, Z., Marchase, R.B., Chatham, J.C., Glucosamine cardioprotection in perfused rat hearts associated with increased O-linked N-acetylglucosamine protein modification and altered p38 activation. Am. J. Physiol. Heart Circ. Physiol. 292 (2007), H2227–H2236.
43. [43] Liu, J., Marchase, R.B., Chatham, J.C., Increased O-GlcNAc levels during reperfusion lead to improved functional recovery and reduced calpain proteolysis. Am. J. Physiol. Heart Circ. Physiol. 293 (2007), H1391–H1399.
44. [44] Lauzier, B., Vaillant, F., Merlen, C., Gelinas, R., Bouchard, B., Rivard, M.E., Labarthe, F., Dolinsky, V.W., Dyck, J.R., Allen, B.G., Chatham, J.C., Des Rosiers, C., Metabolic effects of glutamine on the heart: anaplerosis versus the hexosamine biosynthetic pathway. J. Mol. Cell. Cardiol. 55 (2013), 92–100.
45. [45] Liu, J., Marchase, R.B., Chatham, J.C., Glutamine-induced protection of isolated rat heart from ischemia/reperfusion injury is mediated via the hexosamine biosynthesis pathway and increased protein O-GlcNAc levels. J. Mol. Cell. Cardiol. 42 (2007), 177–185.
46. [46] Khogali, S.E., Harper, A.A., Lyall, J.A., Rennie, M.J., Effects of L-glutamine on post-ischaemic cardiac function: protection and rescue. J. Mol. Cell. Cardiol. 30 (1998), 819–827.
47. [47] Jones, S.P., Zachara, N.E., Ngoh, G.A., Hill, B.G., Teshima, Y., Bhatnagar, A., Hart, G.W., Marban, E., Cardioprotection by N-acetylglucosamine linkage to cellular proteins. Circulation 117 (2008), 1172–1182.
48. [48] Dubois-Deruy, E., Belliard, A., Mulder, P., Bouvet, M., Smet-Nocca, C., Janel, S., Lafont, F., Beseme, O., Amouyel, P., Richard, V., Pinet, F., Interplay between troponin T phosphorylation and O-N-acetylglucosaminylation in ischaemic heart failure. Cardiovasc. Res. 107 (2015), 56–65.
49. [49] Dubois-Deruy, E., Belliard, A., Mulder, P., Chwastyniak, M., Beseme, O., Henry, J.P., Thuillez, C., Amouyel, P., Richard, V., Pinet, F., Circulating plasma serine208-phosphorylated troponin T levels are indicator of cardiac dysfunction. J. Cell. Mol. Med. 17 (2013), 1335–1344.
50. [50] Zou, L., Yang, S., Hu, S., Chaudry, I.H., Marchase, R.B., Chatham, J.C., The protective effects of PUGNAc on cardiac function after trauma-hemorrhage are mediated via increased protein O-GlcNAc levels. Shock (Augusta, Ga.) 27 (2007), 402–408.
51. [51] Yang, S., Zou, L.Y., Bounelis, P., Chaudry, I., Chatham, J.C., Marchase, R.B., Glucosamine administration during resuscitation improves organ function after trauma hemorrhage. Shock (Augusta, Ga.) 25 (2006), 600–607.
52. [52] Zou, L., Yang, S., Champattanachai, V., Hu, S., Chaudry, I.H., Marchase, R.B., Chatham, J.C., Glucosamine improves cardiac function following trauma-hemorrhage by increased protein O-GlcNAcylation and attenuation of NF-{kappa}B signaling. Am. J. Physiol. Heart Circ. Physiol. 296 (2009), H515–H523.
53. [53] Clark, R.J., McDonough, P.M., Swanson, E., Trost, S.U., Suzuki, M., Fukuda, M., Dillmann, W.H., Diabetes and the accompanying hyperglycemia impairs cardiomyocyte calcium cycling through increased nuclear O-GlcNAcylation. J. Biol. Chem. 278 (2003), 44230–44237.
54. [54] Hu, Y., Belke, D., Suarez, J., Swanson, E., Clark, R., Hoshijima, M., Dillmann, W.H., Adenovirus-mediated overexpression of O-GlcNAcase improves contractile function in the diabetic heart. Circ. Res. 96 (2005), 1006–1013.
55. [55] Yokoe, S., Asahi, M., Takeda, T., Otsu, K., Taniguchi, N., Miyoshi, E., Suzuki, K., Inhibition of phospholamban phosphorylation by O-GlcNAcylation: implications for diabetic cardiomyopathy. Glycobiology 20 (2010), 1217–1226.
56. [56] Lunde, I.G., Aronsen, J.M., Kvaloy, H., Qvigstad, E., Sjaastad, I., Tonnessen, T., Christensen, G., Gronning-Wang, L.M., Carlson, C.R., Cardiac O-GlcNAc signaling is increased in hypertrophy and heart failure. Physiol. Genomics 44 (2012), 162–172.
57. [57] Sansbury, B.E., DeMartino, A.M., Xie, Z., Brooks, A.C., Brainard, R.E., Watson, L.J., DeFilippis, A.P., Cummins, T.D., Harbeson, M.A., Brittian, K.R., Prabhu, S.D., Bhatnagar, A., Jones, S.P., Hill, B.G., Metabolomic analysis of pressure-overloaded and infarcted mouse hearts. Circ. Heart Fail. 7 (2014), 634–642.
58. [58] Ledee, D., Smith, L., Bruce, M., Kajimoto, M., Isern, N., Portman, M.A., Olson, A.K., c-Myc alters substrate utilization and O-GlcNAc protein posttranslational modifications without altering cardiac function during early aortic constriction. PLoS One, 10, 2015, e0135262.
59. [59] Facundo, H.T., Brainard, R.E., Watson, L.J., Ngoh, G.A., Hamid, T., Prabhu, S.D., Jones, S.P., O-GlcNAc signaling is essential for NFAT-mediated transcriptional reprogramming during cardiomyocyte hypertrophy. Am. J. Physiol. Heart Circ. Physiol. 302 (2012), H2122–H2130.
60. [60] Cannon, M.V., Sillje, H.H., Sijbesma, J.W., Vreeswijk-Baudoin, I., Ciapaite, J., van der Sluis, B., van Deursen, J., Silva, G.J., de Windt, L.J., Gustafsson, J.A., van der Harst, P., van Gilst, W.H., de Boer, R.A., Cardiac LXRalpha protects against pathological cardiac hypertrophy and dysfunction by enhancing glucose uptake and utilization. EMBO Mol. Med. 7 (2015), 1229–1243.
61. [61] Watson, L.J., Facundo, H.T., Ngoh, G.A., Ameen, M., Brainard, R.E., Lemma, K.M., Long, B.W., Prabhu, S.D., Xuan, Y.T., Jones, S.P., O-linked beta-N-acetylglucosamine transferase is indispensable in the failing heart. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 17797–17802.
62. [62] Young, M.E., Yan, J., Razeghi, P., Cooksey, R.C., Guthrie, P.H., Stepkowski, S.M., McClain, D.A., Tian, R., Taegtmeyer, H., Proposed regulation of gene expression by glucose in rodent heart. Gene Regul. Syst. Biol. 1 (2007), 251–262.
63. [63] Ding, F., Yu, L., Wang, M., Xu, S., Xia, Q., Fu, G., O-GlcNAcylation involvement in high glucose-induced cardiac hypertrophy via ERK1/2 and cyclin D2. Amino Acids 45 (2013), 339–349.
64. [64] Eguchi, K., Boden-Albala, B., Jin, Z., Rundek, T., Sacco, R.L., Homma, S., Di Tullio, M.R., Association between diabetes mellitus and left ventricular hypertrophy in a multiethnic population. Am. J. Cardiol. 101 (2008), 1787–1791.
65. [65] Joffe, I.I., Travers, K.E., Perreault-Micale, C.L., Hampton, T., Katz, S.E., Morgan, J.P., Douglas, P.S., Abnormal cardiac function in the streptozotocin-induced non-insulin-dependent diabetic rat: noninvasive assessment with doppler echocardiography and contribution of the nitric oxide pathway. J. Am. Coll. Cardiol. 34 (1999), 2111–2119.
66. [66] Marsh, S.A., Powell, P.C., Dell'italia, L.J., Chatham, J.C., Cardiac O-GlcNAcylation blunts autophagic signaling in the diabetic heart. Life Sci. 92 (2013), 648–656.
67. [67] Pang, Y., Hunton, D.L., Bounelis, P., Marchase, R.B., Hyperglycemia inhibits capacitative calcium entry and hypertrophy in neonatal cardiomyocytes. Diabetes 51 (2002), 3461–3467.
68. [68] Marsh, S.A., Dell'Italia, L.J., Chatham, J.C., Activation of the hexosamine biosynthesis pathway and protein O-GlcNAcylation modulate hypertrophic and cell signaling pathways in cardiomyocytes from diabetic mice. Amino Acids 40 (2011), 819–828.
69. [69] Belke, D.D., Swim-exercised mice show a decreased level of protein O-GlcNAcylation and expression of O-GlcNAc transferase in heart. J. Appl. Physiol. 111 (2011), 157–162.
70. [70] Medford, H.M., Porter, K., Marsh, S.A., Immediate effects of a single exercise bout on protein O-GlcNAcylation and chromatin regulation of cardiac hypertrophy. Am. J. Physiol. Heart Circ. Physiol. 305 (2013), H114–H123.
71. [71] Johnsen, V.L., Belke, D.D., Hughey, C.C., Hittel, D.S., Hepple, R.T., Koch, L.G., Britton, S.L., Shearer, J., Enhanced cardiac protein glycosylation (O-GlcNAc) of selected mitochondrial proteins in rats artificially selected for low running capacity. Physiol. Genomics 45 (2013), 17–25.
72. [72] Bennett, C.E., Johnsen, V.L., Shearer, J., Belke, D.D., Exercise training mitigates aberrant cardiac protein O-GlcNAcylation in streptozotocin-induced diabetic mice. Life Sci. 92 (2013), 657–663.
73. [73] Cox, E.J., Marsh, S.A., Exercise and diabetes have opposite effects on the assembly and O-GlcNAc modification of the mSin3A/HDAC1/2 complex in the heart. Cardiovasc. Diabetol., 12, 2013, 101.
74. [74] Ramirez-Correa, G.A., Jin, W., Wang, Z., Zhong, X., Gao, W.D., Dias, W.B., Vecoli, C., Hart, G.W., Murphy, A.M., O-linked GlcNAc modification of cardiac myofilament proteins: a novel regulator of myocardial contractile function. Circ. Res. 103 (2008), 1354–1358.
75. 2 + sensitivity in diabetic cardiac muscle. Diabetes 64 (2015), 3573–3587.
76. 2 + ATPase of cardiac sarcoplasmic reticulum: physiological role and relevance to diseases. Biochem. Biophys. Res. Commun. 369 (2008), 182–187.
77. [77] Putney, J.W. Jr., Broad, L.M., Braun, F.J., Lievremont, J.P., Bird, G.S., Mechanisms of capacitative calcium entry. J. Cell Sci. 114 (2001), 2223–2229.
78. [78] Hunton, D.L., Lucchesi, P.A., Pang, Y., Cheng, X., Dell'Italia, L.J., Marchase, R.B., Capacitative calcium entry contributes to nuclear factor of activated T-cells nuclear translocation and hypertrophy in cardiomyocytes. J. Biol. Chem. 277 (2002), 14266–14273.
79. 2 + elevation in neonatal cardiomyocytes via protein-associated O-linked N-acetylglucosamine. Am. J. Physiol. Cell Physiol. 290 (2006), C57–C65.
80. [80] Hulot, J.S., Fauconnier, J., Ramanujam, D., Chaanine, A., Aubart, F., Sassi, Y., Merkle, S., Cazorla, O., Ouille, A., Dupuis, M., Hadri, L., Jeong, D., Muhlstedt, S., Schmitt, J., Braun, A., Benard, L., Saliba, Y., Laggerbauer, B., Nieswandt, B., Lacampagne, A., Hajjar, R.J., Lompre, A.M., Engelhardt, S., Critical role for stromal interaction molecule 1 in cardiac hypertrophy. Circulation 124 (2011), 796–805.
81. [81] Benard, L., Oh, J.G., Cacheux, M., Lee, A., Nonnenmacher, M., Matasic, D.S., Kohlbrenner, E., Kho, C., Pavoine, C., Hajjar, R.J., Hulot, J.S., Cardiac Stim1 silencing impairs adaptive hypertrophy and promotes heart failure through inactivation of mTORC2/Akt signaling. Circulation 133 (2016), 1458–1471.
82. [82] Zhu-Mauldin, X., Marsh, S.A., Zou, L., Marchase, R.B., Chatham, J.C., Modification of STIM1 by O-linked N-acetylglucosamine (O-GlcNAc) attenuates store-operated calcium entry in neonatal cardiomyocytes. J. Biol. Chem. 287 (2012), 39094–39106.
83. [83] Erickson, J.R., Pereira, L., Wang, L., Han, G., Ferguson, A., Dao, K., Copeland, R.J., Despa, F., Hart, G.W., Ripplinger, C.M., Bers, D.M., Diabetic hyperglycaemia activates CaMKII and arrhythmias by O-linked glycosylation. Nature 502 (2013), 372–376.
84. [84] Zhong, W., Mao, S., Tobis, S., Angelis, E., Jordan, M.C., Roos, K.P., Fishbein, M.C., de Alboran, I.M., MacLellan, W.R., Hypertrophic growth in cardiac myocytes is mediated by Myc through a cyclin D2-dependent pathway. EMBO J. 25 (2006), 3869–3879.
85. [85] Lee, H.G., Chen, Q., Wolfram, J.A., Richardson, S.L., Liner, A., Siedlak, S.L., Zhu, X., Ziats, N.P., Fujioka, H., Felsher, D.W., Castellani, R.J., Valencik, M.L., McDonald, J.A., Hoit, B.D., Lesnefsky, E.J., Smith, M.A., Cell cycle re-entry and mitochondrial defects in myc-mediated hypertrophic cardiomyopathy and heart failure. PLoS One, 4, 2009, e7172.
86. [86] Chou, T.Y., Dang, C.V., Hart, G.W., Glycosylation of the c-Myc transactivation domain. Proc. Natl. Acad. Sci. U. S. A. 92 (1995), 4417–4421.
87. [87] Swamy, M., Pathak, S., Grzes, K.M., Damerow, S., Sinclair, L.V., van Aalten, D.M., Glucose and glutamine fuel protein O-GlcNAcylation to control T cell self-renewal and malignancy., 2016.
88. [88] Flesch, M., On the trail of cardiac specific transcription factors. Cardiovasc. Res. 50 (2001), 3–6.
89. [89] Karns, L.R., Kariya, K., Simpson, P.C., M-CAT, CArG, and Sp1 elements are required for alpha 1-adrenergic induction of the skeletal alpha-actin promoter during cardiac myocyte hypertrophy. Transcriptional enhancer factor-1 and protein kinase C as conserved transducers of the fetal program in cardiac growth. J. Biol. Chem. 270 (1995), 410–417.
90. [90] Han, I., Kudlow, J.E., Reduced O glycosylation of Sp1 is associated with increased proteasome susceptibility. Mol. Cell. Biol. 17 (1997), 2550–2558.
91. [91] Lim, K., Yoon, B.H., Ha, C.H., O-linked N-acetylglucosaminylation of Sp1 interferes with Sp1 activation of glycolytic genes. Biochem. Biophys. Res. Commun. 468 (2015), 349–353.
92. [92] Yang, X., Su, K., Roos, M.D., Chang, Q., Paterson, A.J., Kudlow, J.E., O-linkage of N-acetylglucosamine to Sp1 activation domain inhibits its transcriptional capability. Proc. Natl. Acad. Sci. U. S. A. 98 (2001), 6611–6616.
93. [93] Aguilar, H., Fricovsky, E., Ihm, S., Schimke, M., Maya-Ramos, L., Aroonsakool, N., Ceballos, G., Dillmann, W., Villarreal, F., Ramirez-Sanchez, I., Role for high-glucose-induced protein O-GlcNAcylation in stimulating cardiac fibroblast collagen synthesis. Am. J. Physiol. Cell Physiol. 306 (2014), C794–C804.
94. [94] Wu, S., Yin, R., Ernest, R., Li, Y., Zhelyabovska, O., Luo, J., Yang, Y., Yang, Q., Liver X receptors are negative regulators of cardiac hypertrophy via suppressing NF-kappaB signalling. Cardiovasc. Res. 84 (2009), 119–126.
95. [95] Nakagami, H., Takemoto, M., Liao, J.K., NADPH oxidase-derived superoxide anion mediates angiotensin II-induced cardiac hypertrophy. J. Mol. Cell. Cardiol. 35 (2003), 851–859.
96. [96] Nakamura, K., Fushimi, K., Kouchi, H., Mihara, K., Miyazaki, M., Ohe, T., Namba, M., Inhibitory effects of antioxidants on neonatal rat cardiac myocyte hypertrophy induced by tumor necrosis factor-alpha and angiotensin II. Circulation 98 (1998), 794–799.
97. [97] Delbosc, S., Cristol, J.P., Descomps, B., Mimran, A., Jover, B., Simvastatin prevents angiotensin II-induced cardiac alteration and oxidative stress. Hypertension 40 (2002), 142–147.
98. [98] Goldberg, H., Whiteside, C., Fantus, I.G., O-linked beta-N-acetylglucosamine supports p38 MAPK activation by high glucose in glomerular mesangial cells. Am. J. Physiol. Endocrinol. Metab. 301 (2011), E713–E726.
99. [99] Lima, V.V., Spitler, K., Choi, H., Webb, R.C., Tostes, R.C., O-GlcNAcylation and oxidation of proteins: is signalling in the cardiovascular system becoming sweeter?. Clin. Sci. (Lond.) 123:2012 (1979), 473–486.
100. [100] Ngoh, G.A., Watson, L.J., Facundo, H.T., Jones, S.P., Augmented O-GlcNAc signaling attenuates oxidative stress and calcium overload in cardiomyocytes. Amino Acids 40 (2011), 895–911.
101. [101] van Deel, E.D., Octavia, Y., de Boer, M., Juni, R.P., Tempel, D., van Haperen, R., de Crom, R., Moens, A.L., Merkus, D., Duncker, D.J., Normal and high eNOS levels are detrimental in both mild and severe cardiac pressure-overload. J. Mol. Cell. Cardiol. 88 (2015), 145–154.
102. [102] Du, X.L., 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 (2001), 1341–1348.
103. [103] Yang, X., Ongusaha, P.P., Miles, P.D., Havstad, J.C., Zhang, F., So, W.V., Kudlow, J.E., Michell, R.H., Olefsky, J.M., Field, S.J., Evans, R.M., Phosphoinositide signalling links O-GlcNAc transferase to insulin resistance. Nature 451 (2008), 964–969.
104. [104] Kim, J.K., Levin, E.R., Estrogen signaling in the cardiovascular system. Nucl. Recept. Signal., 4, 2006, e013.
105. [105] Cheng, X., Hart, G.W., Glycosylation of the murine estrogen receptor-alpha. J. Steroid Biochem. Mol. Biol. 75 (2000), 147–158.
106. [106] Cheng, X., Cole, R.N., Zaia, J., Hart, G.W., Alternative O-glycosylation/O-phosphorylation of the murine estrogen receptor beta. Biochemistry 39 (2000), 11609–11620.
107. [107] Eguchi, S., Oshiro, N., Miyamoto, T., Yoshino, K., Okamoto, S., Ono, T., Kikkawa, U., Yonezawa, K., AMP-activated protein kinase phosphorylates glutamine: fructose-6-phosphate amidotransferase 1 at Ser243 to modulate its enzymatic activity. Genes Cells 14 (2009), 179–189.
108. [108] Bullen, J.W., Balsbaugh, J.L., Chanda, D., Shabanowitz, J., Hunt, D.F., Neumann, D., Hart, G.W., Cross-talk between two essential nutrient-sensitive enzymes: O-GlcNAc transferase (OGT) and AMP-activated protein kinase (AMPK). J. Biol. Chem. 289 (2014), 10592–10606.
109. [109] Horman, S., Beauloye, C., Vanoverschelde, J.L., Bertrand, L., AMP-activated protein kinase in the control of cardiac metabolism and remodeling. Curr. Heart Fail. Rep. 9 (2012), 164–173.
110. [110] Daskalopoulos, E.P., Dufeys, C., Bertrand, L., Beauloye, C., Horman, S., AMPK in cardiac fibrosis and repair: actions beyond metabolic regulation. J. Mol. Cell. Cardiol., 2016.
111. [111] Ngoh, G.A., Facundo, H.T., Zafir, A., Jones, S.P., O-GlcNAc signaling in the cardiovascular system. Circ. Res. 107 (2010), 171–185.
112. [112] Wang, S., Yang, F., Camp, D.G. II, Rodland, K., Qian, W.J., Liu, T., Smith, R.D., Proteomic approaches for site-specific O-GlcNAcylation analysis. Bioanalysis 6 (2014), 2571–2580.
113. [113] Fardini, Y., Perez-Cervera, Y., Camoin, L., Pagesy, P., Lefebvre, T., Issad, T., Regulatory O-GlcNAcylation sites on FoxO1 are yet to be identified. Biochem. Biophys. Res. Commun. 462 (2015), 151–158.
114. [114] Stitt, T.N., Drujan, D., Clarke, B.A., Panaro, F., Timofeyva, Y., Kline, W.O., Gonzalez, M., Yancopoulos, G.D., Glass, D.J., The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol. Cell 14 (2004), 395–403.
115. [115] Kuo, M., Zilberfarb, V., Gangneux, N., Christeff, N., Issad, T., O-glycosylation of FoxO1 increases its transcriptional activity towards the glucose 6-phosphatase gene. FEBS Lett. 582 (2008), 829–834.
116. [116] Housley, M.P., Udeshi, N.D., Rodgers, J.T., Shabanowitz, J., Puigserver, P., Hunt, D.F., Hart, G.W., A PGC-1alpha-O-GlcNAc transferase complex regulates FoxO transcription factor activity in response to glucose. J. Biol. Chem. 284 (2009), 5148–5157.
117. [117] Crozatier, B., Ventura-Clapier, R., Inhibition of hypertrophy, per se, may not be a good therapeutic strategy in ventricular pressure overload: other approaches could be more beneficial. Circulation 131 (2015), 1448–1457.