Developmental regulation of protein O-GlcNAcylation, O-GlcNAc transferase, and O-GlcNAcase in mammalian brain

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Liu, Ying ^a,c   Li, Xiaojing ^a   Yu, Yang ^a,d   Shi, Jianhua ^a,b   Liang, Zhihou ^a,e   Run, Xiaoqin ^a,e   Li, Yi ^a,f   Dai, Chun ling ^a   Grundke Iqbal, Inge ^a   Iqbal, Khalid ^a   Liu, Fei ^a,b   Gong, Cheng Xin ^a  

^a NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

^b NANTONG UNIVERSITY   (China)

^c Mount Vernon Hospital USA   (United States)

^d SHANGHAI JIAO TONG UNIVERSITY   (China)

^e HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^f HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA N ACETYLGLUCOSAMINE; N ACETYL BETA GLUCOSAMINIDASE; N ACETYLGLUCOSAMINE; O LINKED GLUCOSAMINE TRANSFERASE; O LINKED N ACETYLGLUCOSAMINE TRANSFERASE; TRANSFERASE; UNCLASSIFIED DRUG;

ACYLATION; ADULTHOOD; AGE DISTRIBUTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; FEMALE; GENE ACTIVITY; GENE EXPRESSION REGULATION; GENE LOCATION; GENETIC CORRELATION; MALE; MAMMAL; NEWBORN; NONHUMAN; PERIKARYON; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; RAT; RESIDUE ANALYSIS;

ACETYLGLUCOSAMINE; ANIMALS; BETA-N-ACETYLHEXOSAMINIDASES; BRAIN; FEMALE; ISOENZYMES; N-ACETYLGLUCOSAMINYLTRANSFERASES; PHOSPHORYLATION; PREGNANCY; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, WISTAR; TIME FACTORS;

EID: 84865191053     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043724     Document Type: Article

References (41)

1. Hart GW, ((1997)) Dynamic O-linked glycosylation of nuclear and cytoskeletal proteins. Annu Rev Biochem 66:: 315--335.
2. Zeidan Q, Hart GW, ((2010)) The intersections between O-GlcNAcylation and phosphorylation: implications for multiple signaling pathways. J Cell Sci 123:: 13--22.
3. Hart GW, Housley MP, Slawson C, ((2007)) Cycling of O-linked beta-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446:: 1017--1022.
4. Alfaro JF GC, Monroe ME, Aldrich JT, Clauss TR, Purvine SO, et al. ((2012)) Tandem mass spectrometry identifies many mouse brain O-GlcNAcylated proteins including EGF domain-specific O-GlcNAc transferase targets. Proc Natl Acad Sci U S A 109:: 7280--7285.
5. Dong DL, Xu ZS, Chevrier MR, Cotter RJ, Cleveland DW, et al. ((1993)) Glycosylation of mammalian neurofilaments. Localization of multiple O-linked N-acetylglucosamine moieties on neurofilament polypeptides L and M. J Biol Chem 268:: 16679--16687.
6. Liu F, Iqbal K, Grundke-Iqbal I, Hart GW, Gong CX, ((2004)) O-GlcNAcylation regulates phosphorylation of tau: a mechanism involved in Alzheimer's disease. Proc Natl Acad Sci U S A 101:: 10804--10809.
7. Deng Y, Li B, Liu F, Iqbal K, Grundke-Iqbal I, et al. ((2008)) Regulation between O-GlcNAcylation and phosphorylation of neurofilament-M and their dysregulation in Alzheimer disease. Faseb J 22:: 138--145.
8. Skorobogatko YV, Deuso J, Adolf-Bergfoyle J, Nowak MG, Gong Y, et al. ((2011)) Human Alzheimer's disease synaptic O-GlcNAc site mapping and iTRAQ expression proteomics with ion trap mass spectrometry. Amino Acids 40:: 765--779.
9. Khidekel N, Ficarro SB, Clark PM, Bryan MC, Swaney DL, et al. ((2007)) Probing the dynamics of O-GlcNAc glycosylation in the brain using quantitative proteomics. Nat Chem Biol 3:: 339--348.
10. Clark PM DJ, Mason DE, Hart CR, Buck SB, Peters EC, et al. ((2008)) Direct in-gel fluorescence detection and cellular imaging of O-GlcNAc-modified proteins. J Am Chem Soc 130:: 11576--11577.
11. Tallent MK VN, Skorobogatko Y, Hernandez-Cuebas L, Whelan K, Vocadlo DJ, et al. ((2009)) In vivo modulation of O-GlcNAc levels regulates hippocampal synaptic plasticity through interplay with phosphorylation. J Biol Chem 284:: 178--181.
12. Yuzwa SA, Shan X, Macauley MS, Clark T, Skorobogatko Y, et al. ((2012)) Increasing O-GlcNAc slows neurodegeneration and stabilizes tau against aggregation. Nat Chem Biol 8:: 393--399.
13. Liu F, Shi J, Tanimukai H, Gu J, Gu J, et al. ((2009)) Reduced O-GlcNAcylation links lower brain glucose metabolism and tau pathology in Alzheimer's disease. Brain 132:: 1820--1832.
14. Liu Y, Liu F, Grundke-Iqbal I, Iqbal K, Gong CX, ((2009)) Brain glucose transporters, O-GlcNAcylation and phosphorylation of tau in diabetes and Alzheimer's disease. J Neurochem 111:: 242--249.
15. 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.
16. Shafi R, Iyer SP, Ellies LG, O'Donnell N, Marek KW, et al. ((2000)) 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:: 5735--5739.
17. Bensadoun A, Weinstein D, ((1976)) Assay of proteins in the presence of interfering materials. Anal Biochem 70:: 241--250.
18. Liu F, Zaidi T, Iqbal K, Grundke-Iqbal I, Gong CX, ((2002)) Aberrant glycosylation modulates phosphorylation of tau by protein kinase A and dephosphorylation of tau by protein phosphatase 2A and 5. Neuroscience 115:: 829--837.
19. Lee TN, Alborn WE, Knierman MD, Konrad RJ, ((2006)) Alloxan is an inhibitor of O-GlcNAc-selective N-acetyl-beta-D-glucosaminidase. Biochem Biophys Res Commun 350:: 1038--1043.
20. Gao Y, Wells L, Comer FI, Parker GJ, Hart GW, ((2001)) 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:: 9838--9845.
21. Hanover JA, Yu S, Lubas WB, Shin SH, Ragano-Caracciola M, et al. ((2003)) Mitochondrial and nucleocytoplasmic isoforms of O-linked GlcNAc transferase encoded by a single mammalian gene. Arch Biochem Biophys 409:: 287--297.
22. Macauley MS, Vocadlo DJ, ((2009)) Enzymatic characterization and inhibition of the nuclear variant of human O-GlcNAcase. Carbohydr Res 344:: 1079--1084.
23. Hanover JA KM, Love DC, ((2010)) The hexosamine signaling pathway: O-GlcNAc cycling in feast or famine. Biochim Biophys Acta 1800:: 80--95.
24. Fulop N, Feng W, Xing D, He K, Not LG, et al. ((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.
25. Rex-Mathes M, Werner S, Strutas D, Griffith LS, Viebahn C, et al. ((2001)) O-GlcNAc expression in developing and ageing mouse brain. Biochimie 83:: 583--590.
26. Kreppel LK, Blomberg MA, Hart GW, ((1997)) Dynamic glycosylation of nuclear and cytosolic proteins. Cloning and characterization of a unique O-GlcNAc transferase with multiple tetratricopeptide repeats. J Biol Chem 272:: 9308--9315.
27. Lubas WA, Hanover JA, ((2000)) Functional expression of O-linked GlcNAc transferase. Domain structure and substrate specificity. J Biol Chem 275:: 10983--10988.
28. Tai HC, Khidekel N, Ficarro SB, Peters EC, Hsieh-Wilson LC, ((2004)) Parallel identification of O-GlcNAc-modified proteins from cell lysates. J Am Chem Soc 126:: 10500--10501.
29. Beausoleil SA, Jedrychowski M, Schwartz D, Elias JE, Villen J, et al. ((2004)) Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc Natl Acad Sci U S A 101:: 12130--12135.
30. Dephoure N, Zhou C, Villen J, Beausoleil SA, Bakalarski CE, et al. ((2008)) A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci U S A 105:: 10762--10767.
31. Olsen JV, Vermeulen M, Santamaria A, Kumar C, Miller ML, et al. ((2010)) Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci Signal 3:: ra3.
32. Okuyama R, Marshall S, ((2003)) UDP-N-acetylglucosaminyl transferase (OGT) in brain tissue: temperature sensitivity and subcellular distribution of cytosolic and nuclear enzyme. J Neurochem 86:: 1271--1280.
33. 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 Natl Acad Sci U S A 101:: 13132--13137.
34. Francisco H, Kollins K, Varghis N, Vocadlo D, Vosseller K, et al. ((2009)) O-GLcNAc post-translational modifications regulate the entry of neurons into an axon branching program. Dev Neurobiol 69:: 162--173.
35. Kreppel LK, Hart GW, ((1999)) Regulation of a cytosolic and nuclear O-GlcNAc transferase. Role of the tetratricopeptide repeats. J Biol Chem 274:: 32015--32022.
36. Lefebvre T, Dehennaut V, Guinez C, Olivier S, Drougat L, et al. ((2010)) 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 1800:: 67--79.
37. Griffith LS, Schmitz B, ((1999)) O-linked N-acetylglucosamine levels in cerebellar neurons respond reciprocally to pertubations of phosphorylation. Eur J Biochem 262:: 824--831.
38. Li X, Lu F, Wang JZ, Gong CX, ((2006)) Concurrent alterations of O-GlcNAcylation and phosphorylation of tau in mouse brains during fasting. Eur J Neurosci 23:: 2078--2086.
39. Wang Z, Pandey A, Hart GW, ((2007)) Dynamic interplay between O-linked N-acetylglucosaminylation and glycogen synthase kinase-3-dependent phosphorylation. Mol Cell Proteomics 6:: 1365--1379.
40. Wang Z, Gucek M, Hart GW, ((2008)) Cross-talk between GlcNAcylation and phosphorylation: site-specific phosphorylation dynamics in response to globally elevated O-GlcNAc. Proc Natl Acad Sci U S A 105:: 13793--13798.
41. Crawford GL, Hart GW, Whiteheart SW, ((2008)) Murine platelets are not regulated by O-linked beta-N-acetylglucosamine. Arch Biochem Biophys 474:: 220--224.