2021, Number 3
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Rev Educ Bioquimica 2021; 40 (3)
La función de la O-β-N Acetilglucosamina (O-GLCNAC) en los procesos de enfermedad
Fuentes-García G, Patlán-Castañeda C, Lefebvre T, Robles-Flores M
Language: Spanish
References: 159
Page: 128-144
PDF size: 476.87 Kb.
ABSTRACT
O-GlcNAcylation is a non-canonical glycosylation that consists of a linkage of
OGlcNAc
motif to Serine and Threonine residues of different proteins. Since
O-GlcNAc
depends on the flux of glucose, amino acids, fatty acids, and nucleotides, it has been
postulated as a nutrient status sensor within the cell. However, literature describing
its role in the regulation of several cellular processes has greatly increased since
the discovery of
O-GlcNAc. Now,
O-GlcNAc is not only considered as a nutritional
sensor, but as a posttranslational modification (PTM) which interacts with other
PTMs, such as phosphorylation, methylation, ubiquitinylation to maintain cellular
homeostasis. Likewise, it has been widely described that a disturbance in the levels
of
O-GlcNAc is associated with several pathologies. Thus, the present review
is aimed to summarize some of the main roles of O-GlcNAcylation during different
pathologies and cellular processes.
REFERENCES
Hart GW, Slawson C, Ramirez-Correa G, Lagerlof O (2011) Cross talk between O-GlcNAcylation and phosphorylation: roles in signaling, transcription, and chronic disease. Annu Rev Biochem 80:825–858.
Hart GW, Housley MP, Slawson C (2007) Cycling of O-linked-β-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446:1017- 1022.
Yang X, Qian K (2017) Protein O-GlcNAcylation: emerging mechanisms and functions. Nat Rev Mol Cell Biol 18:452–465.
Ma J, Hart W, (2014) O-GlcNAc profiling: from proteins to proteomes. Clin Proteomics 11:8.
Comer FI, Hart GW (1999) O-GlcNAc and the control of gene expression. Biochim Biophys Acta 1:161–171.
Ozcan S, Andrali SS, Cantrell JE (2010) Modulation of transcription factor function by O-GlcNAc modification. Biochim Biophys Acta 5-6:353–364.
Kelly WG, Dahmus ME, Hart GW (1993) RNA polymerase II is a glycoprotein. Modification of the COOH-terminal domain by O-GlcNAc. J Biol Chem 268:10416–10424.
Lewis BA, Burlingame AL, Myers SA (2016) Human RNA polymerase II promoter recruitment in vitro is regulated by OGT. J Biol Chem 291:14056–14061.
Lewis BA, Hanover JA (2014) O-GlcNAc and the epigenetic regulation of gene expression. J Biol Chem 289:34440–34448.
Noach N, Segev Y, Levi I, Segal S, Priel E (2007) Modification of topoisomerase I activity by glucose and by O-GlcNAcylation of the enzyme protein. Glycobiology 17:1357–1364.
Chen Q, Yu X (2016) OGT restrains the expansion of DNA damage signaling. Nucleic Acids Res 44:9266–9278.
Ruan HB, Han X, Li MD, Wu J, Yates II JR, Yang X (2012) O-GlcNAc transferase/host cell factor C1 complex regulates gluconeogenesis by modulating PGC-1α stability. Cell Metab 16:226–237.
Dentin R, Hedrick S, Xie J, Yates III J, Montminy M (2008) Hepatic glucose sensing via the CREB coactivator CRTC2. Science 319:1402–1405.
Housley MP, Rodgers JT, Udeshi ND, Kelly TJ, Shabanowitz J, Hunt DF, Puigserver P, Hart GW (2008) O-GlcNAc regulates FoxO activation in response to glucose. J Biol Chem 283:16283– 16292.
Yang WH, Park SY, Nam HW, Kin DH, Kang JG, Kang ES, Kin YS, Lee HC, Kim KS, Cho JW (2008) NFκB activation is associated with its O-GlcNAcylation state under hyperglycemic conditions. Proc Natl Acad Sci USA 105:17345– 17350.
Ramakrishnan P, Clark PM, Mason DE, Peters EC, Hsieh-Wilson LC Baltimore D (2013) Activation of the transcriptional function of the NF-κB protein c-Rel by O-GlcNAc glycosylation. Sci Signal 290:ra75.
Daou S, Mashtalir N, Hammond-Martel I, Pak H, Yu H, Sui G, Vogel JL, Kristie TM, Affar EB (2011) Crosstalk between O-GlcNAcylation and proteolytic cleavage regulates the host cell factor-1 maturation pathway. Proc Natl Acad Sci USA 108:2747–2752.
Scheuermann JC, Gaytan-de-Ayala-Alonso A, Oktaba K, Ly-Hartig N, McGinty RK, Fraterman S, Wilm M, Muir TW, Müller J (2010) Histone H2A deubiquitinase activity of the Polycomb repressive complex PR-DUB. Nature 465:243– 247.
Chu CS, Lo PW, Yeh YH, Hsu PH, Peng SH, Teng YC, Kang ML, Wonf CH, Juan LJ (2014) O-GlcNAcylation regulates EZH2 protein stability and function. Proc Natl Acad Sci USA 111:1355–1360.
Gambetta MC, Oktaba K, Muller J (2009) Essential role of the glycosyltransferase sxc/ Ogt in polycomb repression. Science 325:93– 96.
Fujiki R, Hashiba W, Sekine H, Yokoyama A, Chikanishi T, Ito S, Imai Y, Kim J, He HH, Igarashi K, Kanno J, Ohtake F, Kitagawa H, Roeder RG, Brown M, Kato S (2011) GlcNAcylation of histone H2B facilitates its monoubiquitination. Nature 480:557–560.
Yang X, Zhang F, Kudlow JE (2002) Recruitment of O-GlcNAc transferase to promoters by corepressor mSin3A: coupling protein O-GlcNAcylation to transcriptional repression. Cell 110:69–80.
Shi FT, Kin H, Lu W, He Q, Liu D, Goodell MA, Wan M, Songyang Z (2013) 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 288:20776–20784.
Vella P, Scelfo A, Jammula S, Chiaccheira F, Williams K, Cuomo A, Roberto A, Christnsen J, Bonaldi T, Helin K, Pasini D (2013) Tet proteins connect the O-linked N-acetylglucosamine transferase Ogt to chromatin in embryonic stem cells. Mol Cell 49:645–656.
Zhang Q, Liu X, Gao W, Li P, Hou J, Li J, Wong J (2014) Differential regulation of the ten-eleven translocation (TET) family of dioxygenases by O-linked -N-acetylglucosamine transferase (OGT). J Biol Chem 289:5986 –5996.
Chen Q, Chen Y, Bian C, Fujiki R, Yu X (2013) TET2 promotes histone O-GlcNAcylation during gene transcription. Nature 493:561–564.
Nollen EAA, Morimoto RI (2002) Chaperoning signaling pathways: molecular chaperones as stress-sensing ‘heat shock’ proteins. J Cell Sci 14:2809–2816.
Morimoto RI (2012) The heat shock response: systems biology of proteotoxic stress in aging and disease. Cold Spring Harbor Symp Quant Biol 76:91–99.
Akerfelt M, Morimoto RI, Sistonen L (2010) Heat shock factors: integrators of cell stress, development, and lifespan. Nat Rev Mol Cell Biol 11:545–555.
Dai C, Dai S, Cao J (2012) Proteotoxic stress of cancer: implication of the heat-shock response in oncogenesis. J Cell Physiol 227:2982–2987.
Zachara NE, O’Donnell N, Cheung WD, Mercer JJ, Marth JD, Hart GW (2004) Dynamic O-GlcNAc modification of nucleocytoplasmic proteins in response to stress. A survival response of mammalian cells. J Biol Chem 279:30133–30142.
Kazemi Z., Chang H., Haserodt S., McKen C ., Zachara N. E. ( 2010 ). O-Linked-N-acetylglucosamine (O-GlcNAc) regulates stress-induced heat shock protein expression in a GSK-3-dependent manner. J. Biol. Chem. 285, 39096 –39107.
Gong J, Jing L (2011) Glutamine induces heat shock protein 70 expression via O-GlcNAc modification and subsequent increased expression and transcriptional activity of heat shock factor-1. Minerva Anestesiol 77:488- 495.
Walgren JL, Vincent TS, Schey KL, Buse MG (2003) High glucose and insulin promote O-GlcNAc modification of proteins, including beta-tubulin. Am J Physiol Endocrinol Metab 284: E424-E434.
Frank LA, Sutton-McDowall ML, Brown HM, Russell DL, Gilchrist RB, Thompson JG (2014) Hyperglycaemic conditions perturb mouse oocyte in vitro developmental competence via -O-linked glycosylation of heat shock protein 90. Hum Reprod 29:1292–1303.
Guinez C, Lemoine J, Michalski JC, Lefebvre T (2004) 70-kDa heat shock protein presents an adjustable lectinic activity towards O-linked N-acetylglucosamine. Biochem Biophys Res Commun 319:21–26.
Zhang F, Snead CM, Catravas JD (2012) Hsp90 regulates Olinked-N-acetylglucosamine transferase: a novel mechanism of modulation of protein O-linked -N-acetylglucosamine modification in endothelial cells. Am J Physiol Cell Physiol 302: C1786 –C1796.
Ma Z, Vosseller K (2014) Cancer metabolism and elevated O-GlcNAc in oncogenic signaling. J Biol Chem 50:34457-34465.
Kedersha N, Anderson P (2007) Mammalian stress granules and processing bodies. Meth Enzymol 431:61–81.
Ohn T, Kedersha N, Hickman T, Tisdale S, Anderson P (2008) A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat Cell Biol 10:1224–1231.
McClain DA, Lubas WA, Cooksey RC, Hazel M, Parker GJ, Love DC, Handover JA (2002) Altered glycan-dependent signaling induces insulin resistance and hyperleptinemia. Proc Natl Acad Sci USA 99:10695–10699.
Vosseller K, Wells L, Lane MD, Hart GW (2002) Elevated nucleocytoplasmic glycosylation by O-GlcNAc results in insulin resistance associated with defects in Akt activation in 3T3-L1 adipocytes. Proc Natl Acad Sci USA 99:5313–5318.
Arias E.B., Kim J., Cartee G.D. (2004). Prolonged incubation in PUGNAc results in increased protein O-linked glycosylation and insulin resistance in rat skeletal muscle. Diabetes 53,921–930.
Park SY, Ryu J, Lee W (2005) O-GlcNAc modification on IRS-1 and Akt2 by PUGNAc inhibits their phosphorylation and induces insulin resistance in rat primary adipocytes. Exp Mol Med 37:220–229.
Perez-Cervera Y, Dehennaut V, Aquino-Gil M, Guedri K, Solorzano-Mata CJ, Olivier- Van Stichelen S, Foulquier F, Lefebvre T (2013) Insulin signaling controls the expression of O-GlcNAc transferase and its interaction with lipid microdomains. FASEB J 27:3478–3486.
Soesanto YA, Luo B, Jones D, Taylor R, Gabrielsen JS, Parker G, McClain DA (2008) Regulation of Akt signaling by O-GlcNAc in euglycemia. Am. J. Physiol. Endocrinol Metab 295: E974–E980.
Shi J, Gu J, Dai C, Gu J, Jin C, Sun J, Iqbal K, Liu F, Gong CX (2015) O-GlcNAcylation regulates ischemia-induced neuronal apoptosis through AKT signaling. Sci Rep 5:14500.
Lehman DM, Fu DJ, Freeman AB, Hunt KJ, Leach RJ, Johnson-Pais T, Hamlington J, Dyer TD, Arya R, Abboud H, Göring HHH, Duggirala R, Blangero J, Konrad RJ, Stern MP (2005) A single nucleotide polymorphism in MGEA5 encoding O-GlcNAc-selective N-acetyl-β-D glucosaminidase is associated with type 2 diabetes in Mexican Americans. Diabetes 54:1214–1221.
DeBerardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CB. (2008). The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab. 7(1):11–20
Osthus RC, Shim H, Kim S, Li Q, Reddy R, Mukherjee M, Xu Y, Wonsey D, Lee LA, Dang CV (2000) Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J Biol Chem 29:21797-21800.
Ying H, Kimmelman AC, Lyssiotis CA, Hua A, Chu GC, Fletcher-Sananikone E, Locasale JW, Son J, Zhang H, Coloff JL, Yan H, Wang W, Chen S, Viale A, Zheng H, Paik J, Lim C, Guimaraes AR, Martin ES, Chang J, Hezel AF, Perry SR, Hu J, Gan B, Xiao Y, Asara JM, Weissleder R, Wang YA, Chin L, Cantley LC, DePinho RA (2012) Oncogenic Kras maintains pancreatic tumors through regulation of anabolic glucose metabolism. Cell 3:656-70.
Yuneva M, Zamboni N, Oefner P, Sachidanandam R, Lazebnik Y (2007) Deficiency in glutamine but not glucose induces MYC-dependent apoptosis in human cells. J Cell Biol 178:93– 105.
Wise D.R., DeBerardinis R.J., Mancuso A., Sayed N., Zhang X.Y., Pfeiffer H.K., Nissim I., Daikhin E., Yudkoff M., McMahon S.B., Thompson C.B. (2008). Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc. Natl. Acad. Sci. U.S.A. 105, 18782–18787.
Wise DR, DeBerardinis RJ, Mancuso A, Sayed N, Zhang XY, Pfeiffer HK, Nissim I, Daikhin E, Yudkoff M, McMahon SB, Thompson CB (2008) Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc Natl Acad Sci USA 105:18782–18787.
Ma Z, Vocadlo DJ, Vosseller K (2013) Hyper-OGlcNAcylation is anti-apoptotic and maintains constitutive NF-κB activity in pancreatic cancer cells. J Biol Chem 21:15121-15130.
Caldwell SA, Jackson SR, Shahriari KS, Lynch TP, Sethi G, Walker S, Vosseller K, Reginato MJ (2010) Nutrient sensor O-GlcNAc transferase regulates breast cancer tumorigenesis through targeting of the oncogenic transcription factor FoxM1. Oncogene 29:2831–2842.
Gu Y, Mi W, Ge Y, Liu H, Fan Q, Han C, Yang J, Han F, Lu X, Yu W (2010) GlcNAcylation plays an essential role in breast cancer metastasis. Cancer Res 70:6344-6351.
Lynch TP, Ferrer CM, Jackson SR, Shahriari KS, Vosseller K, Reginato MJ (2012) Critical role of O-linked -N-acetylglucosamine transferase in prostate cancer invasion, angiogenesis, and metastasis. J Biol Chem 287:11070 –11081.
Mi W, Gu Y, Han C, Liu H, Fan Q, Zhang X, Cong Q, Yu W (2011) O-GlcNAcylation is a novel regulator of lung and colon cancer malignancy. Biochim Biophys Acta 1812:514 –519.
Yehezkel G, Cohen L, Kliger A, Manor E , and KhalailaI ( 2012 ) O-linked-N-acetylglucosaminylation (O-GlcNAcylation) in primary and metastatic colorectal cancer clones and effect of N-acetyl--Dglucosaminidase silencing on cell phenotype and transcriptome. J Biol Chem 287:28755– 28769.
Zhu Q, Zhou L, Yang Z, Lai M, Xie H, Wu L, Xing C, Zhang F, Zheng S (2012) O-GlcNAcylation plays a role in tumor recurrence of hepatocellular carcinoma following liver transplantation. Med Oncol 29:985–993.
Shi Y, Tomic, J, Wen F, Shaha S, Bahlo A, Harrison R, Dennis JW, Williams R, Gross BJ, Walker S, Zuccolo J, Deans JP, Hart GW, Spaner DE (2010) Aberrant O-GlcNAcylation characterizes chronic lymphocytic leukemia. Leukemia 24:1588-1598.
Handover JA, Weiping C, Bond MR (2017) O-GlcNAc in cancer: An oncometabolismfueled vicious cycle. J Bioenerg Biomembr 3:155-173.
Baldini SF, Steenackers A, Olivier-Van Stichelen S, Mir AM, Mortuaire M, Lefebvre T, Guinez C (2016) Glucokinase expression is regulated by glucose through O-GlcNAc glycosylation. Biochem Biophys Res Commun 478:942–948.
Yu X, Li S (2017) Non-metabolic functions of glycolytic enzymes in tumorigenesis. Oncogene 36:2629–2636.
Chaiyawat P, Chokchaichamnankit D, Lirdprapamongkol K, Srisomsap C, Svasti J, Champattanachai V (2015) Alteration of OGlcNAcylation affects serine phosphorylation and regulates gene expression and activity of pyruvate kinase M2 in colorectal cancer cells. Oncol Rep 34:1933–1942.
Lynch TP, Ferrer CM, Jackson SR, Shahriari KS, Vosseller K, Reginato MJ (2012) Critical role of O-linked -N-acetylglucosamine transferase in prostate cancer invasion, angiogenesis, and metastasis. J Biol Chem 287:11070 –11081.
Thiery JP, Acloque H, Huang RY, Nieto MA (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139:871– 890.
Thiery JP, Sleeman JP (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7:131–142.
Valastyan S, Weinberg RA (2011) Tumor metastasis: molecular insights and evolving paradigms. Cell 147:275–292.
Park SY, Kim HS, Kim NH, Ji S, Cha SY, Kang JG, Ota I, Shimada K, Konishi N, Nam HW, Hong SW, Yang WH, Roth J, Yook JI, Cho JW (2010) Snail1 is stabilized by O-GlcNAc modification in hyperglycaemic condition. EMBO J 29:3787–3796.
Zhu W, Leber B, Andrews DW (2001) Cytoplasmic O-glycosylation prevents cell surface transport of E-cadherin during apoptosis. EMBO J 20:5999-6007.
Chou TY, Hart GW, Dang CV (1995) C-Myc is glycosylated at threonine 58, a known phosphorylation site and a mutational hot spot in lymphomas. J Biol Chem 32:18961–18965.
Itkonen HM, Minner S, Guldvik IJ, Sandmann MJ, Tsourlakis MC, Berge V, Svindland A, Schlomm T, Mills IG (2013) O-GlcNAc transferase integrates metabolic pathways to regulate the stability of c-MYC in human prostate cancer cells. Cancer Res 16:5277–5287.
Zhang B, Zhou P, Li X, Shi Q, Li D, Ju X (2017) Bitterness in sugar: O-GlcNAcylation aggravates pre-B acute lymphocytic leukemia through glycolysis via the PI3K/Akt/c-Myc pathway. Am J Cancer Res 7:1337–1349.
Freund P, Kerenyi MA, Hager M, Wagner T, Wingelhofer B, Pham HTT, Elabd M, Han X, Valent P, Gouilleux F, Sexl V, Kramer OH, Groner B, Moriggl R (2017) O-GlcNAcylation of STAT5 controls tyrosine phosphorylation and oncogenic transcription in STAT5-dependent malignancies. Leukemia 31:2132–2142.
Allard, M. F., Schonekess, B. O., Henning, S. L., English, D. R., & Lopaschuk, G. D. (1994) Contribution of oxidative metabolism and glycolysis to ATP production in hypertrophied hearts. Am J Physiol 267, H742–H750.
Chatham, J. C., & Young, M. E. (2012. Metabolic remodeling in the hypertrophic heart: fuel for thought. Circ Res 111,666–668.
Young ME, Yan J, Razeghi P, Cooksey RC, Guthrie P H, Stepkowski SM, McClain DA, Tian R, Taegtmeyer H (2007) Proposed regulation of gene expression by glucose in rodent heart. Gene Regul Syst Biol 1:251–262.
Fulop N, Feng W, Xing D, He K, Not LG, Brocks CA, Marchase RB, Miller AP, Chatham JC (2008) Aging leads to increased levels of protein o-linked n-acetylglucosamine in heart, aorta, brain, and skeletal muscle in Brown- Norway rats. Biogerontology 9:139–151.
Facundo HT, Brainard RE, Watson LJ, Ngoh GA, Hamid T, Prabhu SD, Jones SP (2012) O-GlcNAc signaling is essential for NFATmediated transcriptional reprogramming during cardiomyocyte hypertrophy. Am J Physiol Heart Circ Physiol 302:H2122-H2130.
Watson LJ, Facundo HT, Ngoh GA, Ameen M, Brainard RE, Lemma KM, Long BW, Prabhu SD, Xuan YT, Jones SP (2010) O-linked beta-Nacetylglucosamine transferase is indispensable in the failing heart. Proc Natl Acad Sci USA 107:17797–17802.
Hu Y, Suarez J, Fricovsky E, Wang H, Scott BT, Trauger SA, Han W, Hu Y, Oyeleye MO, Dillmann WH (2009) Increased enzymatic OGlcNAcylation of mitochondrial proteins impairs mitochondrial function in cardiac myocytes exposed to high glucose. J Biol Chem 284:547-555.
Clark RJ, McDonough PM, Swanson E, Trost SU, Suzuki M, Fukuda M, Dillmann WH (2003) Diabetes and the accompanying hyperglycemia impairs cardiomyocyte calcium cycling through increased nuclear O-GlcNAcylation. J Biol Chem 278:44230–44237.
Hu Y, Belke D, Suarez J, Swanson E, Clark R, Hoshijima M, DIllmann WH (2005) Adenovirusmediated overexpression of O-GlcNAcase improves contractile function in the diabetic heart. Circ Res 96:1006–1013.
Ngoh GA, Facundo HT, Hamid T, Dillmann W, Zachara NE, Jones SP (2009) Unique hexosaminidase reduces metabolic survival signal and sensitizes cardiac myocytes to hypoxia/reoxygenation injury. Circ Res 104:41–49.
Mattiazii A, Kranias G (2014) The role of CaMKII regulation of phospholamban activity in heart disease. Front Pharmacol 27; 5:5.
Yokoe S, Asahi M, Takeda T, Otsu K, Taniguchi N, Miyoshi E, Suzuki K (2010) Inhibition of phospholamban phosphorylation by O-GlcNAcylation: implications for diabetic cardiomyopathy. Glycobiology 20:1217– 1226.
Dassanayaka S, Jones SP (2014) O-GlcNAc and the cardiovascular system. Pharmacology & Therapeutics 142:62–71.
Liu J, Pang Y, Chang T, Bounelis P, Chatham JC, Marchase RB (2006) Increased hexosamine biosynthesis and protein O-GlcNAc levels associated with myocardial protection against calcium paradox and ischemia. J Mol Cell Cardiol 40:303–312.
Champattanachai V, Marchase RB, Chatham JC (2007) Glucosamine protects neonatal cardiomyocytes from ischemia–reperfusion injury via increased protein associated O-GlcNAc. Am J Physiol Cell Physiol 292:C178– C187.
Fulop N, Zhang Z, Marchase RB, Chatham JC (2007) 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:H2227–H2236.
Champattanachai V, Marchase RB, Chatham JC (2008) Glucosamine protects neonatal cardiomyocytes from ischemia–reperfusion injury via increased protein O-GlcNAc and increased mitochondrial Bcl-2. Am J Physiol Cell Physiol 294:C1509–C1520.
Ngoh GA, Watson LJ, Facundo HT, Dillmann W, Jones SP ( 2008 ) Non-canonical glycosyltransferase modulates post-hypoxic cardiac myocyte death and mitochondrial permeability transition. J Mol Cell Cardiol 45:313–325.
Jensen RV, Johnsen J, Kristiansen SB, Zachara NE, Botker HE (2013) Ischemic preconditioning increases myocardial O-GlcNAc glycosylation. Scand Cardiovasc J 47:168–174.
Jones SP, Zachara NE, Ngoh GA, Hill BG, Teshima Y, Bhatnagar A, Hart GW, Marban E (2008) Cardioprotection by n-acetylglucosamine linkage to cellular proteins. Circulation 117:1172–1182.
Zafir A, Readnower R, Long BW, McCracken J, Aird A, Alvarez A, Cummins TD, Li Q, Hill BG, Bhathagar A, Prabhu SD, Bolli R, Jones SP (2013) Protein O-GlcNAcylation is a novel cytoprotective signal in cardiac stem cells. Stem Cells 31:765–775.
Ngoh GA, Hamid T, Prabhu SD, Jones SP (2009) O-GlcNAc signaling attenuates ER stress-induced cardiomyocyte death. Am J Physiol Heart Circ Physiol 297:H1711–H1719.
Hwangh, Rhim H (2018) Functional significance of O-GlcNAc neuronal modification in regulating properties. Pharmacological Research 129:295–307.
Taylor EW, Wang K, Nelson AR, Puckett R, Bredemann TM, Fraser KB, Clinton SM, Marchase RB, Chatham JC, McMahon ALL (2014) O-GlcNAcylation of receptor GluA2 is associated depression with a novel form of long-term at hippocampal synapses. J Neurosci. 1:10–21.
Yang YR, Song S, Hwang H, Lee JH, Jung SJ, Kim SJ, Yoon S, Hur JH, Park JI, Nam CD, Seo YK, Kim JH, Rhim H, Suh PG (2017) Memory and synaptic plasticity are impaired by dysregulated hippocampal O-GlcNAcylation Sci. Rep 7:44921.
Wang AC, Jensen eH, Rexach JE, Vinters HV, Hsieh-Wilson LC (2016) Loss of O-GlcNAc glycosylation in forebrain excitatory neurons induces neurodegeneration. Proc Nat Acad Sc USA 52:15120–15125.
Liu Y, Li X, Yu Y, Shi J, Liang Z, Run X, Li Y, Dai CL, Grundke-Iqbal I, Iqbal KF, Liu F, Gong CX (2012) Developmental regulation of protein O-GlcNAcylation, O-GlcNAc transferase and O-GlcNAcase in mammalian brain. PLoS One 8: e43724.
105.Olivier-Van Stichelen S, Wang P, Comly M, Love DC, Hanover JA (2017) Nutrient-driven O-linked N-Acetylglucosamine (O-GlcNAc) cycling impacts neurodevelopmental timing and metabolism. J Biol Chem 15:6076– 6085.
Rexach JE, Clark PM, Mason DE, Neve RL, Peters EC, Hsieh-Wilson LC (2012) Dynamic O-GlcNAc modification regulates CREB-mediated gene expression and memory formation. Nat Chem Biol 3:253–261.
Atasoy D, Betley JN, Su HH, Sternson SM (2012) Deconstruction of a neural circuit for hunger. Nature 7410:172–177.
Ruan HB, Dietrich MO, Liu ZW, Zimmer MR, Li MD, Singh JP, Zhang K, Wu J, Horvath TL, Yang X (2014) O-GlcNAc transferase enables AgRP Neurons to suppress browning of white fat. Cell 2: 306–317.
Khidekel N, Ficarro SB, Peters EC, Hsieh-Wilson LC (2004) Exploring the O-GlcNAc proteome: direct identification of O-GlcNAc-modified proteins from the brain. Proc Nat. Acad Sci USA 36:13132–13137.
Trinidad JC, Barkan DT, Gulledge BF, Thalhammer A, Sali A, Schoepfer R, Burlingame AL (2012) Global identification and characterization of both O-GlcNAcylation and phosphorylation at the murine synapse. Mol Cel. Proteomics 8:215–229.
Avila J, Lucas JJ, Perez M, Hernandez F (2004) Role of tau protein inboth physiological and pathological conditions. Physiol Rev 2:361– 384.
Hanger DP, Noble W (2011) Functional implications of glycogen synthase kinase-3- mediated tau phosphorylation. Int J Alzheimers Dis 2011:352805.
Noble W, Hanger DP, Miller CC, Lovestone S (2013) The importance of tau phosphorylation for neurodegenerative diseases. Front Neurol 4:83.
Dixit R, Ross JL, Goldmanv YE, Holzbaur EL (2008) Differential regulation of dynein and kinesin motor proteins by tau. Science 5866:1086–1089.
Cho JH, Johnson GV (2003) Glycogen synthase kinase 3beta phosphorylates tau at both primed and unprimed sites. Differential impact on microtubule binding. J Biol Chem 1:187– 193.
Sultan A, Nesslany F, Violet M, Begard S, Loyens A, Talahari S, Mansuroglu Z, Marzin D, Sergeant N, Humez S, Colin M, Bonnefoy E, Buee L, Galas MC (2011) Nuclear tau, a key player in neuronal DNA protection. J Biol Chem 6:4566–4575.
Mondragon-Rodriguez S, Trillaud-Doppia E, Dudilot A, Bourgeois C, Lauzon M, Leclerc N, Boehm J (2012) Interaction of endogenous tau protein with synaptic proteins is regulated by tauphosphorylation, N-methyl-D-aspartate receptor-dependent. J Biol Chem 38:32040– 32053.
118.Kimura T, Whitcomb DJ, Jo J, Regan P, Piers T, Heo S, Brown C, Hashikawa T, Murayama M, Seok M, Sotiropoulos I, Kim E, Collingridge GL, Takashima A, Cho K (2014) Microtubule-associated protein tau is essential for long-term depression in the hippocampus. Philos Trans R Soc Lond B Biol Sci 1633:20130144.
Lim S, Haque MM, Nam G, Ryoo N, Rhim H, Kim YK (2015) Monitoring of intracellular tau aggregation regulated by OGA/OGT inhibitors, Int. J. Mol. Sci. 6 (9) (2015) 20212–20224.
LaFerla FM, Green KN, Oddo S (2007) Intracellular amyloid-beta in Alzheimer’s disease. Nat Rev Neurosci 7:499–509.
Wang Y, Mandelkow E (2016) Tau in Physiology and pathology. Nat Rev Neurosci 1: 5–21.
Griffith LS, Mathes M, Schmitz B (1995) Betaamyloid precursor protein is modified with O-linked N-acetylglucosamine. J Neurosci Res 2:270–278.
123.Jacobsen KT, Iverfeldt K (2011) O-GlcNAcylation increases non-amyloidogenic processing of the amyloid-beta precursor protein (APP). Biochem Biophys Res Commun 3:882–886.
124.Maries E, Dass B, Collier TJ, Kordower JH, Steece-Collier K (2003) The role of alphasynuclein in Parkinson’s disease: insights from animal models. Nat Rev Neurosci 9: 727–738.
Marotta NP, Lin YH, Lewis YE, Ambroso MR, Zaro BW, Roth MT, Arnold DB, Langen R, Pratt MR (2015) O-GlcNAc modification blocks the aggregation and toxicity of the protein alphasynuclein associated with Parkinson’s disease. Nat Chem 11:913–920.
126.Folmes CD, Dzeja PP, Nelson TJ, Terzic A (2012) Metabolic plasticity in stem cell homeostasis and differentiation. Cell Stem Cell 5:596-606.
127.Zhang H, Badur MG, Divakaruni AS, Parker SJ, Jager C, Hiller K, Murphy AN, Metallo CM (2016) Distinct metabolic states can support self-renewal and Lipogenesis in human pluripotent stem cells under different culture conditions. Cell Rep 16:1536–1547.
Chen CT, Shih YR, Kuo TK, Lee OK, Wei YH (2008) Coordinated changes of mitochondrial biogenesisandanti oxidante n z yme s during osteogenic differentiation of human mesenchymal stem cells. Stem Cells 4:960– 968.
Turner WS, Seagle C, Galanko JA, Favorov O, Prestwich GD, Macdonald JM, Reid LM (2008) Nuclear magnetic resonance metabolomic footprinting of human hepatic stem cells and hepatoblasts cultured in hyaluronan-matrix hydrogels. Stem Cells 6:1547–1555.
Simsek T, Kocabas F, Zheng J, Deberardinis RJ, Mahmoud AI, Olson EN, Schneider JW, Zang CC, Sadek H (2010) The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell 3:380–390.
Mohyeldin A, Garzon-Muvdi T, Quinones- Hinojosa A (2010) Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell 2:150–161.
Varum S, Momcilovic O, Castro C, Ben- Yehudah A, Ramalho-Santos J, Navara CS (2009) Enhancement of human embryonic stem cell pluripotency through inhibition of the mitochondrial respiratory chain. Stem Cell Res 2–3:142–156
Chen G, Gulbranson DR, Hou Z, Bolin JM, Ruotti V, Probasco MD, Smuga-Otto K, Howden SE, Diol NR, Popson NE, Wagner R, Lee GO, Antonsiewics-Bourget J, Teng JMC, Thomson JA (2011) Chemically defined conditions for human iPSC derivation and culture. Nat Methods 5:424–429.
134.Kondoh H, Lleonart ME, Nakashima Y, Yokode M, Tanaka M, Bernard D, Gil J, Beach D (2007) A high glycolytic flux supports the proliferative potential of murine embryonic stem cells. Antioxid Redox Signal 3:293–299.
135.Marsboom G, Zhang GF, Pohl-Avila N, Zhang Y, Yuan Y, Kang H, Hao B, Brunengraber H, Malik AB, Rehman J (2016) Glutamine metabolism regulates the pluripotency transcription factor OCT4. Cell Rep 2:323–332.
136.Sharma NS, Saluja AK, Banerjee S (2018) Nutrient-sensing and self-renewal: O-GlcNAc in a new role. J Bioenerg Biomembr 50: 205–211.
Shafi R, Iyer SPN, Ellies LG, O’Donnell N, Marek KW, Chui D, Hart GW, Marth JD (2000) The O-GlcNAc transferase gene resides on the X chromosome and is essential for embryonic stem cell viability and mouse ontogeny. PNAS 11:5735-5739.
Jang H, Kim TW, Yoon S, Choi SY, Kang TW, Kim SY, Kwon YW, Cho EJ Youn HD (2012) O-GlcNAc regulates pluripotency and reprogramming by directly acting on core components of the pluripotency network. Cell Stem Cell 11:62– 74.
Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663-76.
Speakman CM, Domke TC, Wongpaiboonwattana W, Sanders K, Mudaliar M, van Aalten DM, Barton GJ, Stavridis MP (2014) Elevated O-GlcNAc levels activate epigenetically repressed genes and delay mouse ESC differentiation without affecting naive to primed cell transition. Stem Cells 32(10):2605–2615.
Pathak S, Borodkin VS, Albarbarawi O, Campbell DG, Ibrahim A, van Aalten DM (2012) O-GlcNAcylation of TAB1 modulates TAK1-mediated cytokine release. EMBO J 31:1394–1404.
Chikanishi T, Fujiki R, Hashiba W, Sekine H, Yokoyama A, Kato S (2010) Glucose induced expression of MIP-1 genes requires O-GlcNAc transferase in monocytes. Biochem Biophys Res Commun 394:865–870.
Dias WB, Cheung WD, Wang Z, Hart GW (2009) Regulation of calcium/calmodulin dependent kinase IV by O-GlcNAc modification. J Biol Chem 284:21327–21337.
Yao AY, Tang HY, Wang Y, Feng MF, Zhou RL (2004) Inhibition of the activating signals in NK92 cells by recombinant GST-sHLA-G1a chain. Cell Res 14:155–160.
Hwang SY, Hwang JS, Kim SY, Han IO (2013) O-GlcNAc transferase inhibits LPSmediated expression of inducible nitric oxide synthase through an increased interaction with mSin3A in RAW264.7 cells. Am J Physiol Cell Physiol 305:C601-C608.
Li X, Gong W, Li L, Wen H (2017) Downregulation of the O-GlcNAc signaling promotes activation of the innate immune response in microbial sepsis. J Immunol 70:78.
Ryu IH, Do SI (2011) Denitrosylation of S-nitrosylated OGT is triggered in LPSstimulated innate immune response. Biochem Biophys Res Commun 408:52–57.
Li X, Zhang Z, Li L, Gong W, Lazenby AJ, Swanson BJ, Herring LE, Asara JM, Singer JD, Wen H (2017) Myeloid-derived cullin 3 promotes STAT3 phosphorylation by inhibiting OGT expression and protects against intestinal inflammation. J Exp Med 214:1093–1109.
de Jesus T, Shukla S, Ramakrishnan P (2018) Too sweet to resist: Control of immune cell function by O-GlcNAcylation. Cellular Immunology 333:85–92.
Kneass ZT, Marchase RB (2005) Protein O-GlcNAc modulates motility-associated signaling intermediates in neutrophils. J Biol Chem 280:14579–14585.
O’Donnell N, Zachara NE, Hart GW, Marth JD (2004) Ogt-dependent X-chromosome-linked protein glycosylation is a requisite modification in somatic cell function and embryo viability. Mol Cell Biol 24:1680–1690.
Golks A, Tran TT, Goetschy JF, Guerini D (2007) Requirement for O-linked N-acetylglucosaminy l t ransferase in lymphocytes activation. EMBO J 26:4368– 4379.
Ramakrishnan P, Clark PM, Mason DE, Peters EC, Hsieh-Wilson LC, Baltimore D (2013) Activation of the transcriptional function of the NF-kappaB protein c-Rel by O-GlcNAc glycosylation. Sci Signal 6:ra75.
Johnson B, Opimba M, Bernier J (2014) Implications of the O-GlcNAc modification in the regulation of nuclear apoptosis in T cells. Biochim Biophys Acta 1840:191–198.
Lund PJ, Elias JE, Davis MM (2016) Global analysis of O-GlcNAc glycoproteins in activated human T cells. J Immunol 197:3086–3098.
Swamy M, Pathak S, Grzes KM, Damerow S, Sinclair LV, van Aalten DM, Cantrell DA (2016) Glucose and glutamine fuel protein O-GlcNAcylation to control T cell self-renewal and malignancy. Nat Immunol 17:712–720.
Liu R, Ma X, Chen L, Yang Y, Zeng Y, Gao J, Jiang W, Zhang F, Li D, Han B, Han R, Qiu R, Huang W, Wang Y, Hao J (2017) MicroRNA- 15b suppresses Th17 differentiation and is associated with pathogenesis of multiple sclerosis by targeting O-GlcNAc transferase. J Immunol 198:2626–2639.
Wu JL, Chiang MF, Hsu PH, Tsai DY, Hung KH, Wang YH, Angata T, Lin KI (2017) O-GlcNAcylation is required for B cell homeostasis and antibody responses. Nat Commun 8:1854.
Martinez MR, Dias TB, Natov PS, Zachara NE (2017) Stress-induced O-GlcNAcylation: an adaptive process of injured cells. Biochemical Society Transactions 45:237–249
Yuzwa SA, Shan X, Macauley MS, Clark T, Skorobogatko Y, Vosseller K, Vocadlo DJ (2012) Increasing O-GlcNAc slows neurodegeneration and stabilizes tau against aggregation. Nat Chem Biol 8:393–399.