Three decades of research on O-GlcNAcylation - A major nutrient sensor that regulates signaling, transcription and cellular metabolism

Frontiers in Endocrinology

Volumn 5, Issue OCT, 2014, Pages

  Hart, Gerald W ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Cancer; Diabetes; O GlcNAc transferase; O GlcNAcase; O GlcNAcylation; Signaling; Transcription

Indexed keywords

ACETYLGLUCOSAMINIDASE; GLYCOSYLTRANSFERASE; HYALURONIDASE; MENINGIOMA EXPRESSED ANTIGEN 5; N ACETYLGLUCOSAMINE; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ACYLATION; ARTICLE; CELL METABOLISM; DNA METHYLATION; HUMAN; MENINGIOMA; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TETRATRICOPEPTIDE REPEAT; TRANSCRIPTION REGULATION; UBIQUITINATION;

EID: 84926686351     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2014.00183     Document Type: Article

References (80)

1. Torres C-R, Hart GW. Topography and polypeptide distribution of terminal N-acetylglucosamine residues on the surfaces of intact lymphocytes. J Biol Chem (1984) 259:3308-17.
2. Holt GD, Hart GW. The subcellular distribution of terminal N-acetylglucosamine moieties. Localization of a novel protein-saccharide linkage, O-linked GlcNAc. J Biol Chem (1986) 261:8049-57.
3. Hanover JA, Cohen CK, Willingham MC, Park MK. O-linked N-acetylglucosamine is attached to proteins of the nuclear pore. Evidence for cytoplasmic and nucleoplasmic glycoproteins. J Biol Chem (1987) 262:9887-94.
4. Davis LI, Blobel G. Nuclear pore complex contains a family of glycoproteins that includes p62: glycosylation through a previously unidentified cellular pathway. Proc Natl Acad Sci U S A (1987) 84:7552-6. doi: 10.1073/pnas.84.21.7552
5. Holt GD, Snow CM, Senior A, Haltiwanger RS, Gerace L, Hart GW. Nuclear pore complex glycoproteins contain cytoplasmically disposed O-linked N-acetylglucosamine. J Cell Biol (1987) 104:1157-64. doi:10.1083/jcb.104.5.1157
6. Holt GD, Haltiwanger RS, Torres CR, Hart GW. Erythrocytes contain cytoplasmic glycoproteins. O-linked GlcNAc on Band 4.1. J Biol Chem (1987) 262:14847-50.
7. Benko DM, Haltiwanger RS, Hart GW, Gibson W. Virion basic phosphoprotein from human cytomegalovirus contains O-linked N-acetylglucosamine. Proc Natl Acad Sci U S A (1988) 85:2573-7. doi:10.1073/pnas.85.8.2573
8. Kelly WG, Hart GW. Glycosylation of chromosomal proteins: localization of O-linked N-acetylglucosamine in Drosophila chromatin. Cell (1989) 57:243-51. doi:10.1016/0092-8674(89)90962-8
9. Jackson SP, Tjian R. O-glycosylation of eukaryotic transcription factors: implications for mechanisms of transcriptional regulation. Cell (1988) 55:125-33. doi:10.1016/0092-8674(88)90015-3
10. Kelly WG, Dahmus ME, Hart GW. RNA polymerase II is a glycoprotein. Modification of the COOH-terminal domain by O-GlcNAc. J Biol Chem (1993) 268:10416-24.
11. Kearse KP, Hart GW. Lymphocyte activation induces rapid changes in nuclear and cytoplasmic glycoproteins. Proc Natl Acad Sci U S A (1991) 88:1701-5. doi:10.1073/pnas.88.5.1701
12. Roquemore EP, Chevrier MR, Cotter RJ, Hart GW. Dynamic O-GlcNAcylation of the small heat shock protein alpha B-crystallin. Biochemistry (1996) 35:3578-86. doi:10.1021/bi951918j
13. Haltiwanger RS, Holt GD, Hart GW. Enzymatic addition of O-GlcNAc to nuclear and cytoplasmic proteins. Identification of a uridine diphospho-N-acetylglucosamine:peptide beta-N-acetylglucosaminyltransferase. J Biol Chem (1990) 265:2563-8.
14. Haltiwanger RS, Blomberg MA, Hart GW. Glycosylation of nuclear and cytoplasmic proteins. Purification and characterization of a uridine diphospho-N-acetylglucosamine:polypeptide beta-N-acetylglucosaminyltransferase. J Biol Chem (1992) 267:9005-13.
15. Dong DL, Hart GW. Purification and characterization of an O-GlcNAc selective N-acetyl-beta-d-glucosaminidase from rat spleen cytosol. J Biol Chem (1994) 269:19321-30.
16. Overdijk B, Van der Kroef WM, Van Steijn GJ, Lisman JJ. Isolation and further characterization of bovine brain hexosaminidase C. Biochim Biophys Acta (1981) 659:255-66. doi:10.1016/0005-2744(81)90052-8
17. Braidman I, Carroll M, Dance N, Robinson D, Poenaru L, Weber A, et al. Characterisation of human N-acetyl-beta-hexosaminidase C. FEBS Lett (1974) 41:181-4. doi:10.1016/0014-5793(74)81206-8
18. Kreppel LK, Blomberg MA, Hart GW. Dynamic glycosylation of nuclear and cytosolic proteins. Cloning and characterization of a unique O-GlcNAc transferase with multiple tetratricopeptide repeats. J Biol Chem (1997) 272:9308-15. doi:10.1074/jbc.272.14.9308
19. Lubas WA, Frank DW, Krause M, Hanover JA. O-linked GlcNAc transferase is a conserved nucleocytoplasmic protein containing tetratricopeptide repeats. J Biol Chem (1997) 272:9316-24. doi:10.1074/jbc.272.14.9316
20. Gao Y, Wells L, Comer FI, Parker GJ, Hart GW. Dynamic O-glycosylation of nuclear and cytosolic proteins: cloning and characterization of a neutral, cytosolic beta-N-acetylglucosaminidase from human brain. J Biol Chem (2001) 276:9838-45. doi:10.1074/jbc. M010420200
21. Comtesse N, Maldener E, Meese E. Identification of a nuclear variant of MGEA5, a cytoplasmic hyaluronidase and a beta-N-acetylglucosaminidase. Biochem Biophys Res Commun (2001) 283:634-40. doi:10.1006/bbrc.2001.4815
22. Hart GW. Dynamic O-linked glycosylation of nuclear and cytoskeletal proteins. Ann Rev Biochem (1997) 66:315-35. doi:10.1146/annurev.biochem.66.1.315
23. Hart GW, Slawson C, Ramirez-Correa G, Lagerlof O. Cross talk between O-GlcNAcylation and phosphorylation: roles in signaling, transcription, and chronic disease. Annu Rev Biochem (2011) 80:825-58. doi:10.1146/annurev-biochem-060608-102511
24. Hardiville S, Hart GW. Nutrient regulation of signaling, transcription, and cell physiology by O-GlcNAcylation. Cell Metab (2014) 20:208-13. doi:10.1016/j.cmet.2014.07.014
25. Shafi R, Iyer SP, Ellies LG, O'Donnell N, Marek KW, Chui D, et al. 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 (2000) 97:5735-9. doi:10.1073/pnas.100471497
26. Hartweck LM, Scott CL, Olszewski NE. Two O-linked N-acetylglucosamine transferase genes of Arabidopsis thaliana L. Heynh. have overlapping functions necessary for gamete and seed development. Genetics (2002) 161:1279-91.
27. Olszewski NE, West CM, Sassi SO, Hartweck LM. O-GlcNAc protein modification in plants: evolution and function. Biochim Biophys Acta (2010) 1800:49-56. doi:10.1016/j.bbagen.2009.11.016
28. Golks A, Tran TT, Goetschy JF, Guerini D. Requirement for O-linked N-acetylglucosaminyltransferase in lymphocytes activation. EMBO J (2007) 26:4368-79. doi:10.1038/sj.emboj.7601845
29. Hiromura M, Choi CH, Sabourin NA, Jones H, Bachvarov D, Usheva A. YY1 is regulated by O-linked N-acetylglucosaminylation (O-glcNAcylation). J Biol Chem (2003) 278:14046-52. doi:10.1074/jbc. M300789200
30. Ozcan S, Andrali SS, Cantrell JE. Modulation of transcription factor function by O-GlcNAc modification. Biochim Biophys Acta (2010) 1799:353-64. doi:10.1016/j.bbagrm.2010.02.005
31. Durgan DJ, Pat BM, Laczy B, Bradley JA, Tsai JY, Grenett MH, et al. O-GlcNAcylation, novel post-translational modification linking myocardial metabolism and cardiomyocyte circadian clock. J Biol Chem (2011) 286:44606-19. doi:10.1074/jbc. M111.278903
32. Kim EY, Jeong EH, Park S, Jeong HJ, Edery I, Cho JW. A role for O-GlcNAcylation in setting circadian clock speed. Genes Dev (2012) 26:490-502. doi:10.1101/gad.182378.111
33. Kaasik K, Kivimae S, Allen JJ, Chalkley RJ, Huang Y, Baer K, et al. Glucose sensor O-GlcNAcylation coordinates with phosphorylation to regulate circadian clock. Cell Metab (2013) 17:291-302. doi:10.1016/j.cmet.2012.12.017
34. Hart GW. How sugar tunes your clock. Cell Metab (2013) 17:155-6. doi:10.1016/j.cmet.2013.01.008
35. Sumegi M, Hunyadi-Gulyas E, Medzihradszky KF, Udvardy A. 26S proteasome subunits are O-linked N-acetylglucosamine-modified in Drosophila melanogaster. Biochem Biophys Res Commun (2003) 312:1284-9. doi:10.1016/j.bbrc.2003.11.074
36. Liu K, Paterson AJ, Zhang F, McAndrew J, Fukuchi K, Wyss JM, et al. Accumulation of protein O-GlcNAc modification inhibits proteasomes in the brain and coincides with neuronal apoptosis in brain areas with high O-GlcNAc metabolism. J Neurochem (2004) 89:1044-55. doi:10.1111/j.1471-4159.2004.02389.x
37. Kudlow JE. Post-translational modification by O-GlcNAc: another way to change protein function. J Cell Biochem (2006) 98:1062-75. doi:10.1002/jcb.20926
38. Bowe DB, Sadlonova A, Toleman CA, Novak Z, Hu Y, Huang P, et al. O-GlcNAc integrates the proteasome and transcriptome to regulate nuclear hormone receptors. Mol Cell Biol (2006) 26:8539-50. doi:10.1128/MCB.01053-06
39. Zhang F, Su K, Yang X, Bowe DB, Paterson AJ, Kudlow JE. O-GlcNAc modification is an endogenous inhibitor of the proteasome. Cell (2003) 115:715-25. doi:10.1016/S0092-8674(03)00974-7
40. Guinez C, Mir AM, Dehennaut V, Cacan R, Harduin-Lepers A, Michalski JC, et al. Protein ubiquitination is modulated by O-GlcNAc glycosylation. FASEB J (2008) 22:2901-11. doi:10.1096/fj.07-102509
41. Ruan HB, Nie Y, Yang X. Regulation of protein degradation by O-GlcNAcylation: crosstalk with ubiquitination. Mol Cell Proteomics (2013) 12:3489-97. doi:10.1074/mcp. R113.029751
42. Tallent MK, Varghis N, Skorobogatko Y, Hernandez-Cuebas L, Whelan K, Vocadlo DJ, et al. In vivo modulation of O-GlcNAc levels regulates hippocampal synaptic plasticity through interplay with phosphorylation. J Biol Chem (2009) 284:174-81. doi:10.1074/jbc. M807431200
43. Francisco H, Kollins K, Varghis N, Vocadlo D, Vosseller K, Gallo G. O-GLcNAc post-translational modifications regulate the entry of neurons into an axon branching program. Dev Neurobiol (2009) 69:162-73. doi:10.1002/dneu.20695
44. Skorobogatko Y, Landicho A, Chalkley RJ, Kossenkov AV, Gallo G, Vosseller K. O-linked beta-N-acetylglucosamine (O-GlcNAc) site thr-87 regulates synapsin I localization to synapses and size of the reserve pool of synaptic vesicles. J Biol Chem (2014) 289:3602-12. doi:10.1074/jbc. M113.512814
45. Vosseller K, Trinidad JC, Chalkley RJ, Specht CG, Thalhammer A, Lynn AJ, et al. O-linked N-acetylglucosamine proteomics of postsynaptic density preparations using lectin weak affinity chromatography and mass spectrometry. Mol Cell Proteomics (2006) 5:923-34. doi:10.1074/mcp. T500040-MCP200
46. Trinidad JC, Barkan DT, Gulledge BF, Thalhammer A, Sali A, Schoepfer R, et al. Global identification and characterization of both O-GlcNAcylation and phosphorylation at the murine synapse. Mol Cell Proteomics (2012) 11:215-29. doi:10.1074/mcp. O112.018366
47. Zachara NE, O'Donnell N, Cheung WD, Mercer JJ, Marth JD, Hart GW. Dynamic O-GlcNAc modification of nucleocytoplasmic proteins in response to stress. A survival response of mammalian cells. J Biol Chem (2004) 279:30133-42. doi:10.1074/jbc. M403773200
48. Slawson C, Zachara NE, Vosseller K, Cheung WD, Lane MD, Hart GW. Perturbations in O-linked beta-N-acetylglucosamine protein modification cause severe defects in mitotic progression and cytokinesis. J Biol Chem (2005) 280:32944-56. doi:10.1074/jbc. M503396200
49. Banerjee S, Robbins PW, Samuelson J. Molecular characterization of nucleocytosolic O-GlcNAc transferases of Giardia lamblia and Cryptosporidium parvum. Glycobiology (2009) 19:331-6. doi:10.1093/glycob/cwn107
50. Acosta DM, Soprano LL, Ferrero M, Landoni M, Esteva MI, Couto AS, et al. A striking common O-linked N-acetylglucosaminyl moiety between cruzipain and myosin. Parasite Immunol (2011) 33:363-70. doi:10.1111/j.1365-3024.2011.01291.x
51. Perez-Cervera Y, Harichaux G, Schmidt J, Debierre-Grockiego F, Dehennaut V, Bieker U, et al. Direct evidence of O-GlcNAcylation in the apicomplexan Toxoplasma gondii: a biochemical and bioinformatic study. Amino Acids (2011) 40:847-56. doi:10.1007/s00726-010-0702-4
52. Uddin N, Hoessli DC, Butt A, Kaleem A, Iqbal Z, Afzal I, et al. O-GlcNAc modification of the anti-malarial vaccine candidate PfAMA1: in silico-defined structural changes and potential to generate a better vaccine. Mol Biol Rep (2012) 39:4663-72. doi:10.1007/s11033-011-1258-4
53. Shen A, Kamp HD, Grundling A, Higgins DE. A bifunctional O-GlcNAc transferase governs flagellar motility through anti-repression. Genes Dev (2006) 20:3283-95. doi:10.1101/gad.1492606
54. Shi WW, Jiang YL, Zhu F, Yang YH, Shao QY, Yang HB, et al. Structure of a novel O-linked N-acetyl-d-glucosamine (O-GlcNAc) transferase, GtfA, reveals insights into the glycosylation of pneumococcal serine-rich repeat adhesins. J Biol Chem (2014) 289:20898-907. doi:10.1074/jbc. M114.581934
55. Lewis BA. O-GlcNAcylation at promoters, nutrient sensors, and transcriptional regulation. Biochim Biophys Acta (2013) 1829:1202-6. doi:10.1016/j.bbagrm.2013.09.003
56. Ranuncolo SM, Ghosh S, Hanover JA, Hart GW, Lewis BA. Evidence of the involvement of O-GlcNAc-modified human RNA polymerase II CTD in transcription in vitro and in vivo. J Biol Chem (2012) 287:23549-61. doi:10.1074/jbc. M111.330910
57. Chen Q, Chen Y, Bian C, Fujiki R, Yu X. TET2 promotes histone O-GlcNAcylation during gene transcription. Nature (2013) 493:561-4. doi:10.1038/nature11742
58. Deplus R, Delatte B, Schwinn MK, Defrance M, Mendez J, Murphy N, et al. TET2 and TET3 regulate GlcNAcylation and H3K4 methylation through OGT and SET1/COMPASS. EMBO J (2013) 32:645-55. doi:10.1038/emboj.2012.357
59. Shi FT, Kim H, Lu W, He Q, Liu D, Goodell MA, et al. Ten-eleven translocation 1 (Tet1) is regulated by O-linked N-acetylglucosamine transferase (Ogt) for target gene repression in mouse embryonic stem cells. J Biol Chem (2013) 288:20776-84. doi:10.1074/jbc. M113.460386
60. Zhang Q, Liu X, Gao W, Li P, Hou J, Li J, et al. Differential regulation of the ten-eleven translocation (TET) family of dioxygenases by O-linked beta-N-acetylglucosamine transferase (OGT). J Biol Chem (2014) 289:5986-96. doi:10.1074/jbc. M113.524140
61. Fujiki R, Chikanishi T, Hashiba W, Ito H, Takada I, Roeder RG, et al. GlcNAcylation of a histone methyltransferase in retinoic-acid-induced granulopoiesis. Nature (2009) 459:455-9. doi:10.1038/nature07954
62. Sakabe K, Hart GW. O-GlcNAc transferase regulates mitotic chromatin dynamics. J Biol Chem (2010) 285:34460-8. doi:10.1074/jbc. M110.158170
63. Sakabe K, Wang Z, Hart GW. Beta-N-acetylglucosamine (O-GlcNAc) is part of the histone code. Proc Natl Acad Sci U S A (2010) 107:19915-20. doi:10.1073/pnas.1009023107
64. Bullen JW, Balsbaugh JL, Chanda D, Shabanowitz J, Hunt DF, Neumann D, et al. Cross-talk between two essential nutrient-sensitive enzymes: O-GlcNAc transferase (OGT) and AMP-activated protein kinase (AMPK). J Biol Chem (2014) 289:10592-606. doi:10.1074/jbc. M113.523068
65. Erickson JR, Pereira L, Wang L, Han G, Ferguson A, Dao K, et al. Diabetic hyperglycaemia activates CaMKII and arrhythmias by O-linked glycosylation. Nature (2013) 502:372-6. doi:10.1038/nature12537
66. Yi W, Clark PM, Mason DE, Keenan MC, Hill C, Goddard WA III, et al. Phosphofructokinase 1 glycosylation regulates cell growth and metabolism. Science (2012) 337:975-80. doi:10.1126/science.1222278
67. Tarrant MK, Rho HS, Xie Z, Jiang YL, Gross C, Culhane JC, et al. Regulation of CK2 by phosphorylation and O-GlcNAcylation revealed by semisynthesis. Nat Chem Biol (2012) 8:262-9. doi:10.1038/nchembio.771
68. Dias WB, Cheung WD, Hart GW. O-GlcNAcylation of kinases. Biochem Biophys Res Commun (2012) 422:224-8. doi:10.1016/j.bbrc.2012.04.124
69. Dias WB, Cheung WD, Wang Z, Hart GW. Regulation of calcium/calmodulin-dependent kinase IV by O-GlcNAc modification. J Biol Chem (2009) 284:21327-37. doi:10.1074/jbc. M109.007310
70. Slawson C, Copeland RJ, Hart GW. O-GlcNAc signaling: a metabolic link between diabetes and cancer? Trends Biochem Sci (2010) 35:547-55. doi:10.1016/j.tibs.2010.04.005
71. Lefebvre T, Dehennaut V, Guinez C, Olivier S, Drougat L, Mir AM, et al. Dysregulation of the nutrient/stress sensor O-GlcNAcylation is involved in the etiology of cardiovascular disorders, type-2 diabetes and Alzheimer's disease. Biochim Biophys Acta (2010) 1800:67-79. doi:10.1016/j.bbagen.2009.08.008
72. Hanover JA, Krause MW, Love DC. The hexosamine signaling pathway: O-GlcNAc cycling in feast or famine. Biochim Biophys Acta (2010) 1800:80-95. doi:10.1016/j.bbagen.2009.07.017
73. Ma Z, Vosseller K. Cancer metabolism and elevated O-GlcNAc in oncogenic signaling. J Biol Chem (2014) 289.
74. Ma Z, Vosseller K. O-GlcNAc in cancer biology. Amino Acids (2013) 45:719-33. doi:10.1007/s00726-013-1543-8
75. Shi Y, Tomic J, Wen F, Shaha S, Bahlo A, Harrison R, et al. Aberrant O-GlcNAcylation characterizes chronic lymphocytic leukemia. Leukemia (2010) 24:1588-98. doi:10.1038/leu.2010.152
76. Lazarus BD, Love DC, Hanover JA. O-GlcNAc cycling: implications for neurodegenerative disorders. Int J Biochem Cell Biol (2009) 41:2134-46. doi:10.1016/j.biocel.2009.03.008
77. Yuzwa SA, Vocadlo DJ. O-GlcNAc and neurodegeneration: biochemical mechanisms and potential roles in Alzheimer's disease and beyond. Chem Soc Rev (2014) 43:6839-58. doi:10.1039/c4cs00038b
78. Lagerlof O, Hart GW. O-GlcNAcylation of neuronal proteins: roles in neuronal functions and in neurodegeneration. Adv Neurobiol (2014) 9:343-66. doi:10.1007/978-1-4939-1154-7_16
79. Kreppel LK, Hart GW. Regulation of a cytosolic and nuclear O-GlcNAc transferase. Role of the tetratricopeptide repeats. J Biol Chem (1999) 274:32015-22. doi:10.1074/jbc.274.45.32015
80. Cole RN, Hart GW. Cytosolic O-glycosylation is abundant in nerve terminals. J Neurochem (2001) 79:1080-9. doi:10.1046/j.1471-4159.2001.00655.x