CLC number: Q-1
On-line Access: 2024-08-27
Received: 2023-10-17
Revision Accepted: 2024-05-08
Crosschecked: 2019-04-23
Cited: 0
Clicked: 3861
Hao Nie, Wen Yi. O-GlcNAcylation, a sweet link to the pathology of diseases[J]. Journal of Zhejiang University Science B, 2019, 20(5): 437-448.
@article{title="O-GlcNAcylation, a sweet link to the pathology of diseases",
author="Hao Nie, Wen Yi",
journal="Journal of Zhejiang University Science B",
volume="20",
number="5",
pages="437-448",
year="2019",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B1900150"
}
%0 Journal Article
%T O-GlcNAcylation, a sweet link to the pathology of diseases
%A Hao Nie
%A Wen Yi
%J Journal of Zhejiang University SCIENCE B
%V 20
%N 5
%P 437-448
%@ 1673-1581
%D 2019
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1900150
TY - JOUR
T1 - O-GlcNAcylation, a sweet link to the pathology of diseases
A1 - Hao Nie
A1 - Wen Yi
J0 - Journal of Zhejiang University Science B
VL - 20
IS - 5
SP - 437
EP - 448
%@ 1673-1581
Y1 - 2019
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1900150
Abstract: O-linked N-acetylglucosamine (O-GlcNAc) is a dynamic post-translational modification occurring on myriad proteins in the cell nucleus, cytoplasm, and mitochondria. The donor sugar for O-GlcNAcylation, uridine-diphosphate N-acetylglucosamine (UDP-GlcNAc), is synthesized from glucose through the hexosamine biosynthetic pathway (HBP). The recycling of O-GlcNAc on proteins is mediated by two enzymes in cells—O-GlcNAc transferase (OGT) and O-GlcNAcase (OGA), which catalyze the addition and removal of O-GlcNAc, respectively. O-GlcNAcylation is involved in a number of important cell processes including transcription, translation, metabolism, signal transduction, and apoptosis. Deregulation of O-GlcNAcylation has been reported to be associated with various human diseases such as cancer, diabetes, neurodegenerative diseases, and cardiovascular diseases. A better understanding of the roles of O-GlcNAcylation in physiopathological processes would help to uncover novel avenues for therapeutic intervention. The aim of this review is to discuss the recent updates on the mechanisms and impacts of O-GlcNAcylation on these diseases, and its potential as a new clinical target.
[1]Andrali SS, Qian QW, Özcan S, 2007. Glucose mediates the translocation of neurod1 by O-linked glycosylation. J Biol Chem, 282(21):15589-15596.
[2]Ball LE, Berkaw MN, Buse MG, 2006. Identification of the major site of O-linked β-N-acetylglucosamine modification in the C terminus of insulin receptor substrate-1. Mol Cell Proteom, 5(2):313-323.
[3]Banerjee PS, Lagerlöf O, Hart GW, 2016. Roles of O-GlcNAc in chronic diseases of aging. Mol Aspects Med, 51:1-15.
[4]Bond MR, Hanover JA, 2015. A little sugar goes a long way: the cell biology of O-GlcNAc. J Cell Biol, 208(7):869-880.
[5]Borghgraef P, Menuet C, Theunis C, et al., 2013. Increasing brain protein O-GlcNAc-ylation mitigates breathing defects and mortality of Tau.P301l mice. PLoS ONE, 8(12):e84442.
[6]Bray F, Ferlay J, Soerjomataram I, et al., 2018. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 68(6):394-424.
[7]Buono R, Longo VD, 2018. Starvation, stress resistance, and cancer. Trends Endocrinol Metab, 29(4):271-280.
[8]Butkinaree C, Park K, Hart GW, 2010. 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(2):96-106.
[9]Carpenter R, DiChiacchio T, Barker K, 2019. Interventions for self-management of type 2 diabetes: an integrative review. Int J Nurs Sci, 6(1):70-91.
[10]Cecioni S, Vocadlo DJ, 2013. Tools for probing and perturbing O-GlcNAc in cells and in vivo. Curr Opin Chem Biol, 17(5):719-728.
[11]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(1):C178-C187.
[12]Chen YX, Jin L, Xue B, et al., 2017. Nrage induces β-catenin/ Arm O-GlcNAcylation and negatively regulates Wnt signaling. Biochem Biophys Res Commun, 487(2):433-437.
[13]Chetan MR, Thrower SL, Narendran P, 2019. What is type 1 diabetes? Medicine, 47(1):5-9.
[14]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, 270(32):18961-18965.
[15]Cooper C, Sommerlad A, Lyketsos CG, et al., 2015. Modifiable predictors of dementia in mild cognitive impairment: a systematic review and meta-analysis. Am J Psychiatry, 172(4):323-334.
[16]Cui C, Zhou XL, Zhang WD, et al., 2018. Is β-catenin a druggable target for cancer therapy? Trends Biochem Sci, 43(8):623-634.
[17]Darley-Usmar VM, Ball LE, Chatham JC, 2012. Protein O-linked β-N-acetylglucosamine: a novel effector of cardiomyocyte metabolism and function. J Mol Cell Cardiol, 52(3):538-549.
[18]Dassanayaka S, Jones SP, 2014. O-GlcNAc and the cardiovascular system. Pharmacol Ther, 142(1):62-71.
[19]de Jesus T, Shukla S, Ramakrishnan P, 2018. Too sweet to resist: control of immune cell function by O-GlcNAcylation. Cell Immunol, 333:85-92.
[20]Dubois-Deruy E, Belliard A, Mulder P, et al., 2015. Interplay between troponin T phosphorylation and O-N-acetylglucosaminylation in ischaemic heart failure. Cardiovasc Res, 107(1):56-65.
[21]Durning SP, Flanagan-Steet H, Prasad N, et al., 2016. O-linked β-N-acetylglucosamine (O-GlcNAc) acts as a glucose sensor to epigenetically regulate the insulin gene in pancreatic beta cells. J Biol Chem, 291(5):2107-2118.
[22]Ferrer CM, Sodi VL, Reginato MJ, 2016. O-GlcNAcylation in cancer biology: linking metabolism and signaling. J Mol Biol, 428(16):3282-3294.
[23]Ferron M, Denis M, Persello A, et al., 2018. Protein O-GlcNAcylation in cardiac pathologies: past, present, future. Front Endocrinol (Lausanne), 9:819.
[24]Gao Y, Miyazaki JI, Hart GW, 2003. The transcription factor PDX-1 is post-translationally modified by O-linked N-acetylglucosamine and this modification is correlated with its DNA binding activity and insulin secretion in Min6 β-cells. Arch Biochem Biophys, 415(2):155-163.
[25]Graham DL, Gray AJ, Joyce JA, et al., 2014. Increased O-GlcNAcylation reduces pathological tau without affecting its normal phosphorylation in a mouse model of tauopathy. Neuropharmacology, 79:307-313.
[26]Gudala K, Bansal D, Schifano F, et al., 2013. Diabetes mellitus and risk of dementia: a meta-analysis of prospective observational studies. J Diabetes Investig, 4(6):640-650.
[27]Ha JR, Hao L, Venkateswaran G, et al., 2014. β-Catenin is O-GlcNAc glycosylated at serine 23: implications for β-catenin’s subcellular localization and transactivator function. Exp Cell Res, 321(2):153-166.
[28]Harosh-Davidovich SB, Khalaila I, 2018. O-GlcNAcylation affects β-catenin and E-cadherin expression, cell motility and tumorigenicity of colorectal cancer. Exp Cell Res, 364(1):42-49.
[29]Hurtado MD, Vella A, 2019. What is type 2 diabetes? Medicine, 47(1):10-15.
[30]Hwang H, Rhim H, 2018. Functional significance of O-GlcNAc modification in regulating neuronal properties. Pharmacol Res, 129:295-307.
[31]Issad T, Masson E, Pagesy P, 2010. O-GlcNAc modification, insulin signaling and diabetic complications. Diabetes Metab, 36(6):423-435.
[32]Itkonen HM, Minner S, Guldvik IJ, et al., 2013. O-GlcNAc transferase integrates metabolic pathways to regulate the stability of c-MYC in human prostate cancer cells. Cancer Res, 73(16):5277-5287.
[33]Jiang JY, Lazarus MB, Pasquina L, et al., 2011. A neutral diphosphate mimic crosslinks the active site of human O-GlcNAc transferase. Nat Chem Biol, 8(1):72-77.
[34]Joiner CM, Li H, Jiang JY, et al., 2019. Structural characterization of the O-GlcNAc cycling enzymes: insights into substrate recognition and catalytic mechanisms. Curr Opin Struct Biol, 56:97-106.
[35]Jones SP, Zachara NE, Ngoh GA, et al., 2008. Cardioprotection by N-acetylglucosamine linkage to cellular proteins. Circulation, 117(9):1172-1182.
[36]Kim C, Nam DW, Park SY, et al., 2013. O-linked β-N-acetylglucosaminidase inhibitor attenuates β-amyloid plaque and rescues memory impairment. Neurobiol Aging, 34(1):275-285.
[37]Lee TN, Alborn WE, Knierman MD, et al., 2006. Alloxan is an inhibitor of O-GlcNAc-selective N-acetyl-β-
[38]Leney AC, el Atmioui D, Wu W, et al., 2017. Elucidating crosstalk mechanisms between phosphorylation and O-GlcNAcylation. Proc Natl Acad Sci USA, 114(35):E7255-E7261.
[39]Liberti MV, Locasale JW, 2016. The Warburg effect: how does it benefit cancer cells? Trends Biochem Sci, 41(3):211-218.
[40]Lim S, Haque MM, Nam G, et al., 2015. Monitoring of intracellular tau aggregation regulated by OGA/OGT inhibitors. Int J Mol Sci, 16(9):20212-20224.
[41]Lin G, Wang LP, Marcogliese PC, et al., 2019. Sphingolipids in the pathogenesis of Parkinson’s disease and Parkinsonism. Trends Endocrinol Metab, 30(2):106-117.
[42]Liu Y, Dai SJ, Xing LJ, et al., 2015. O-linked β-N-acetylglucosamine modification and its biological functions. Sci Bull, 60(12):1055-1061.
[43]Ma ZY, Vocadlo DJ, Vosseller K, 2013. Hyper-O-GlcNAcylation is anti-apoptotic and maintains constitutive NF-κB activity in pancreatic cancer cells. J Biol Chem, 288(21):15121-15130.
[44]Macauley MS, Vocadlo DJ, 2010. Increasing O-GlcNAc levels: an overview of small-molecule inhibitors of O-GlcNAcase. Biochim Biophys Acta, 1800(2):107-121.
[45]Macauley MS, Shan XY, Yuzwa SA, et al., 2010. Elevation of global O-GlcNAc in rodents using a selective O-GlcNAcase inhibitor does not cause insulin resistance or perturb glucohomeostasis. Chem Biol, 17(9):949-958.
[46]Mailleux F, Gélinas R, Beauloye C, et al., 2016. O-GlcNAcylation, enemy or ally during cardiac hypertrophy development? Biochim Biophys Acta, 1862(12):2232-2243.
[47]Marotta NP, Cherwien CA, Abeywardana T, et al., 2012. O-GlcNAc modification prevents peptide-dependent acceleration of α-synuclein aggregation. Chembiochem, 13(18):2665-2670.
[48]Marotta NP, Lin YH, Lewis YE, et al., 2015. O-GlcNAc modification blocks the aggregation and toxicity of the protein α-synuclein associated with Parkinson’s disease. Nat Chem, 7(11):913-920.
[49]Marsh SA, Collins HE, Chatham JC, 2014. Protein O-GlcNAcylation and cardiovascular (patho)physiology. J Biol Chem, 289(50):34449-34456.
[50]McClain DA, Lubas WA, Cooksey RC, et al., 2002. Altered glycan-dependent signaling induces insulin resistance and hyperleptinemia. Proc Natl Acad Sci USA, 99(16):10695-10699.
[51]Ngoh GA, Hamid T, Prabhu SD, et al., 2009. O-GlcNAc signaling attenuates ER stress-induced cardiomyocyte death. Am J Physiol Heart Circ Physiol, 297(5):H1711-H1719.
[52]Özcan S, Andrali SS, Cantrell JEL, 2010. Modulation of transcription factor function by O-GlcNAc modification. Biochim Biophys Acta, 1799(5-6):353-364.
[53]Patel M, Horgan PG, McMillan DC, et al., 2018. NF-κB pathways in the development and progression of colorectal cancer. Transl Res, 197:43-56.
[54]Peterson SB, Hart GW, 2016. New insights: a role for O-GlcNAcylation in diabetic complications. Crit Rev Biochem Mol Biol, 51(3):150-161.
[55]Pinho TS, Verde DM, Correia SC, et al., 2018. O-GlcNAcylation and neuronal energy status: implications for Alzheimer’s disease. Ageing Res Rev, 46:32-41.
[56]Ramirez-Correa GA, Ma JF, Slawson C, et al., 2015. Removal of abnormal myofilament O-GlcNAcylation restores Ca2+ sensitivity in diabetic cardiac muscle. Diabetes, 64(10):3573-3587.
[57]Rao XJ, Duan XT, Mao WM, et al., 2015. O-GlcNAcylation of G6PD promotes the pentose phosphate pathway and tumor growth. Nat Commun, 6:8468.
[58]Rowe EM, Xing V, Biggar KK, 2019. Lysine methylation: implications in neurodegenerative disease. Brain Res, 1707:164-171.
[59]Smet-Nocca C, Broncel M, Wieruszeski JM, et al., 2011. Identification of O-GlcNAc sites within peptides of the Tau protein and their impact on phosphorylation. Mol Biosyst, 7(5):1420-1429.
[60]Snipelisky D, Chaudhry SP, Stewart GC, 2019. The many faces of heart failure. Card Electrophysiol Clin, 11(1):11-20.
[61]Tan JZA, Gleeson PA, 2019. The role of membrane trafficking in the processing of amyloid precursor protein and production of amyloid peptides in Alzheimer’s disease. Biochim Biophys Acta, 1861(4):697-712.
[62]Teo CF, Wollaston-Hayden EE, Wells L, 2010. Hexosamine flux, the O-GlcNAc modification, and the development of insulin resistance in adipocytes. Mol Cell Endocrinol, 318(1-2):44-53.
[63]van Giau V, An SSA, Hulme JP, 2018. Mitochondrial therapeutic interventions in Alzheimer’s disease. J Neurol Sci, 395:62-70.
[64]Vosseller K, Wells L, Lane MD, et al., 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(8):5313-5318.
[65]Wang Y, Liu J, Jin X, et al., 2017. O-GlcNAcylation destabilizes the active tetrameric PKM2 to promote the Warburg effect. Proc Natl Acad Sci USA, 114(52):13732-13737.
[66]Wani WY, Chatham JC, Darley-Usmar V, et al., 2017. O-GlcNAcylation and neurodegeneration. Brain Res Bull, 133:80-87.
[67]Watson LJ, Facundo HT, Ngoh GA, et al., 2010. O-linked β-N-acetylglucosamine transferase is indispensable in the failing heart. Proc Natl Acad Sci USA, 107(41):17797-17802.
[68]Whelan SA, Dias WB, Thiruneelakantapillai L, et al., 2010. Regulation of insulin receptor substrate 1 (IRS-1)/AKT kinase-mediated insulin signaling by O-linked β-N-acetylglucosamine in 3T3-L1 adipocytes. J Biol Chem, 285(8):5204-5211.
[69]Xu WQ, Zhang X, Wu JL, et al., 2017. O-GlcNAc transferase promotes fatty liver-associated liver cancer through inducing palmitic acid and activating endoplasmic reticulum stress. J Hepatol, 67(2):310-320.
[70]Yang SL, Zou LY, Bounelis P, et al., 2006. Glucosamine administration during resuscitation improves organ function after trauma hemorrhage. Shock, 25(6):600-607.
[71]Yang WH, Park SY, Nam HW, et al., 2008a. NFκB activation is associated with its O-GlcNAcylation state under hyperglycemic conditions. Proc Natl Acad Sci USA, 105(45):17345-17350.
[72]Yang XY, Ongusaha PP, Miles PD, et al., 2008b. Phosphoinositide signalling links O-GlcNAc transferase to insulin resistance. Nature, 451(7181):964-969.
[73]Yi W, Clark PM, Mason DE, et al., 2012. Phosphofructokinase 1 glycosylation regulates cell growth and metabolism. Science, 337(6097):975-980.
[74]Yuzwa SA, Macauley MS, Heinonen JE, et al., 2008. A potent mechanism-inspired O-GlcNAcase inhibitor that blocks phosphorylation of tau in vivo. Nat Chem Biol, 4(8):483-490.
[75]Zachou G, Armeni E, Lambrinoudaki I, 2019. Lactation and maternal cardiovascular disease risk in later life. Maturitas, 122:73-79.
[76]Zhu YP, Shan XY, Yuzwa SA, et al., 2014. The emerging link between O-GlcNAc and Alzheimer disease. J Biol Chem, 289(50):34472-34481.
[77]Zou LY, Yang SL, Hu SH, et al., 2007. The protective effects of PUGNAc on cardiac function after trauma-hemorrhage are mediated via increased protein O-GlcNAc levels. Shock, 27(4):402-408.
[78]Zou LY, Yang SL, Champattanachai V, et al., 2009. Glucosamine improves cardiac function following trauma-hemorrhage by increased protein O-GlcNAcylation and attenuation of NF-κB signaling. Am J Physiol Heart Circ Physiol, 296(2):H515-H523.
Open peer comments: Debate/Discuss/Question/Opinion
<1>