550
Views
29
CrossRef citations to date
0
Altmetric
Review Article

The regulatory roles of O-GlcNAcylation in mitochondrial homeostasis and metabolic syndrome

, , &
Pages 1080-1088 | Received 14 Aug 2016, Accepted 16 Sep 2016, Published online: 19 Oct 2016

References

  • Hart GW, Akimoto Y. The O-GlcNAc modification. In: Varki A, Cummings RD, Esko JD, et al., editors. Essentials of glycobiology. 2nd ed. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2009. Chapter 18. Available from: https://www.ncbi.nlm.nih.gov/books/NBK1954/.
  • Torres C-R, Hart GW. Topography and polypeptide distribution of terminal N-acetylglucosamine residues on the surfaces of intact lymphocytes. Evidence for O-linked GlcNAc. J Biol Chem 1984;259:3308–3317.
  • Vaidyanathan K, Durning S, Wells L. Functional O-GlcNAc modifications: implications in molecular regulation and pathophysiology. Crit Rev Biochem Mol Biol 2014;49:140–163.
  • Zeidan Q, Hart GW. The intersections between O-GlcNAcylation and phosphorylation: implications for multiple signaling pathways. J Cell Sci 2010;123(Pt 1):13–22.
  • Hanover JA, Krause MW, Love DC. Bittersweet memories: linking metabolism to epigenetics through O-GlcNAcylation. Nat Rev Mol Cell Biol 2012;13:312–321.
  • Hardiville S, Hart GW. Nutrient regulation of signaling, transcription, and cell physiology by O-GlcNAcylation. Cell Metab 2014;20:208–213.
  • Hanover JA, Krause MW, Love DC. The hexosamine signaling pathway: O-GlcNAc cycling in feast or famine. Biochim Biophys Acta 2010;1800:80–95.
  • Zachara NE, O’Donnell N, Cheung WD, Mercer JJ, Marth JD, Hart GW, et al. Dynamic O-GlcNAc modification of nucleocytoplasmic proteins in response to stress. A survival response of mammalian cells. J Biol Chem 2004;279:30133–30142.
  • Butkinaree C, Park K, Hart GW. 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 2010;1800:96–106.
  • Ngoh GA, Facundo HT, Zafir A, Jones SP. O-GlcNAc signaling in the cardiovascular system. Circ Res 2010;107:171–185.
  • Ngoh GA, Watson LJ, Facundo HT, Jones SP. Augmented O-GlcNAc signaling attenuates oxidative stress and calcium overload in cardiomyocytes. Amino Acids 2011;40:895–911.
  • Zhao L, Feng Z, Zou X, Cao K, Xu J, Liu J. Aging leads to elevation of O-GlcNAcylation and disruption of mitochondrial homeostasis in retina. Oxid Med Cell Longev 2014;2014:425705.
  • Zachara NE. The dynamic stress-induced “O-GlcNAc-ome” highlights functions for O-GlcNAc in regulating DNA damage/repair and other cellular pathways. Amino Acids 2011;40:793–808.
  • Gurel Z, Sieg KM, Shallow KD, Sorenson CM, Sheibani N. Retinal O-linked N-acetylglucosamine protein modifications: implications for postnatal retinal vascularization and the pathogenesis of diabetic retinopathy. Mol Vis 2013;19:1047.
  • Yang YR, Song M, Lee H, Jeon Y, Choi EJ, Jang HJ, et al. O-GlcNAcase is essential for embryonic development and maintenance of genomic stability. Aging Cell 2012;11:439–448.
  • Vaidyanathan K, Wells L. Multiple tissue-specific roles for the O-GlcNAc post-translational modification in the induction of and complications arising from type II diabetes. J Biol Chem 2014;289:34466–34471.
  • Zhang K, Yin R, Yang X. O-GlcNAc: a bittersweet switch in liver. Front Endocrinol 2014;5:221.
  • Yang X, Ongusaha PP, Miles PD, Havstad JCC, Zhang F, So WV, et al. Phosphoinositide signalling links O-GlcNAc transferase to insulin resistance. Nature 2008;451:964–969.
  • Ma Z, Vosseller K. O-GlcNAc in cancer biology. Amino Acids 2013;45:719–733.
  • Singh JP, Zhang K, Wu J, Yang X. O-GlcNAc signaling in cancer metabolism and epigenetics. Cancer Lett 2015;356(Pt A):244–250.
  • Gong CX, Liu F, Iqbal K. O-GlcNAc cycling modulates neurodegeneration. Proc Natl Acad Sci USA 2012;109:17319–17320.
  • Slawson C, Copeland RJ, Hart GW. O-GlcNAc signaling: a metabolic link between diabetes and cancer? Trend Biochem Sci 2010;35:547–555.
  • Bond MR, Hanover JA. O-GlcNAc cycling: a link between metabolism and chronic disease. Ann Rev Nutr 2013;33:205–229.
  • Makarem N, Scott M, Quatromoni P, Jacques P, Parekh N. Trends in dietary carbohydrate consumption from 1991 to 2008 in the Framingham Heart Study Offspring Cohort. Br J Nutr 2014:111:1–14.
  • Connor T, Martin SD, Howlett KF, McGee SL. Metabolic remodelling in obesity and type 2 diabetes: pathological or protective mechanisms in response to nutrient excess? Clin Exp Pharmacol Physiol 2015;42:109–115.
  • Bond MR, Hanover JA. O-GlcNAc cycling: a link between metabolism and chronic disease. Annu Rev Nutr 2013;33:205–229.
  • Medford HM, Chatham JC, Marsh SA. Chronic ingestion of a Western diet increases O-linked-beta-N-acetylglucosamine (O-GlcNAc) protein modification in the rat heart. Life Sci 2012;90:883–888.
  • Ruan H-B, Singh JP, Li MD, Wu J, Yang X. Cracking the O-GlcNAc code in metabolism. Trends Endocrinol Metab 2013;24:301–309.
  • Kim JA, Wei Y, Sowers JR. Role of mitochondrial dysfunction in insulin resistance. Circ Res 2008;102:401–414.
  • Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circ Res 2010;107:1058–1070.
  • Hanover JA, Yu S, Lubas WB, Shin SH, Ranano-Caracciola M, Kochran J, et al. Mitochondrial and nucleocytoplasmic isoforms of O-linked GlcNAc transferase encoded by a single mammalian gene. Arch Biochem Biophys 2003;409:287–297.
  • Banerjee PS, Ma J, Hart GW. Diabetes-associated dysregulation of O-GlcNAcylation in rat cardiac mitochondria. Proc Natl Acad Sci USA 2015;112:6050–6055.
  • Shin SH, Love DC, Hanover JA. Elevated O-GlcNAc-dependent signaling through inducible mOGT expression selectively triggers apoptosis. Amino Acids 2011;40:885–893.
  • Ruan HB, Han X, Li MD, Singh JP, Qian K, Azarhoush S, et al. O-GlcNAc transferase/host cell factor C1 complex regulates gluconeogenesis by modulating PGC-1alpha stability. Cell Metab 2012;16:226–237.
  • Lubas WA, Hanover JA. Functional expression of O-linked GlcNAc transferase. Domain structure and substrate specificity. J Biol Chem 2000;275:10983–10988.
  • Love DC, Kochan J, Cathey RL, Shin SH, Hanover JA. Mitochondrial and nucleocytoplasmic targeting of O-linked GlcNAc transferase. J Cell Sci 2003;116(Pt 4):647–654.
  • Ma J, Liu T, Wei AC, Banerjee P, O’Rourke B, Hart GW. O-GlcNAcomic profiling identifies widespread O-linked beta-N-acetylglucosamine modification (O-GlcNAcylation) in oxidative phosphorylation system regulating cardiac mitochondrial function. J Biol Chem 2015;290:29141–29153.
  • Tan EP, Villar MT, E L, Lu J, Selfridge JE, Artigues A, et al. Altering O-linked beta-N-acetylglucosamine cycling disrupts mitochondrial function. J Biol Chem 2014;289:14719–14730.
  • Tan EP, Lanza C, Swerdlow, Slawson C. Interplay between O-GlcNAc and acetylation regulates mitochondrial function (756.7). FASEB J 2014;28(Suppl. 1):756.7.
  • Lozano L, Lara-Lemus R, Zenteno E, Alvarado-Vasquez N. The mitochondrial O-linked N-acetylglucosamine transferase (mOGT) in the diabetic patient could be the initial trigger to develop Alzheimer disease. Exp Gerontol 2014;58:198–202.
  • Pekkurnaz G, Trinidad JC, Wang X, Kong D, Schwarz TL. Glucose regulates mitochondrial motility via Milton modification by O-GlcNAc transferase. Cell 2014;158:54–68.
  • Gawlowski T, Suarez J, Scott B, Torres-Gonzalez M, Wang H, Schwappacher R, et al. Modulation of dynamin-related protein 1 (DRP1) function by increased O-linked-beta-N-acetylglucosamine modification (O-GlcNAc) in cardiac myocytes. J Biol Chem 2012;287:30024–30034.
  • Bond MR, Hanover JA. A little sugar goes a long way: the cell biology of O-GlcNAc. J Cell Biol 2015;208:869–880.
  • Hu Y, Suarez J, Fricovsky E, Wang H, Scott BT, Trauger SA, et al. Increased enzymatic O-GlcNAcylation of mitochondrial proteins impairs mitochondrial function in cardiac myocytes exposed to high glucose. J Biol Chem 2009;284:547–555.
  • Johnsen VL, Belke DD, Hughey CC, Hittel DS, Hepple RT, Koch LG, et al. Enhanced cardiac protein glycosylation (O-GlcNAc) of selected mitochondrial proteins in rats artificially selected for low running capacity. Physiol Genom 2013;45:17–25.
  • Ma J, Liu T, Wei A-C, O’Rourke B, Hart G. O-GlcNAcomic profiling reveals altered O-GlcNAcylation of mitochondrial proteins in diabetes (608.4). FASEB J 2014;28(Suppl. 1):608.4.
  • Dassanayaka S, Readnower RD, Salabei JK, Long BW, Aird AL, Zheng Y-T, et al. High glucose induces mitochondrial dysfunction independently of protein O-GlcNAcylation. Biochem J 2015;467:115–126.
  • Jones SP, Zachara NE, Ngoh GA, Hill BG, Teshima Y, Bhatnagar A, et al. Cardioprotection by N-acetylglucosamine linkage to cellular proteins. Circulation 2008;117:1172–1182.
  • Wright J, Kramer P, Darley-Ushmer V, Chatham J. Role of O-GlcNAcylation in regulating mitophagy in cardiomyocytes. FASEB J 2015;29(Suppl. 1):954.5.
  • Styskal J, van Remmen H, Richardson A, Salmon AB. Oxidative stress and diabetes: what can we learn about insulin resistance from antioxidant mutant mouse models? Free Radic Biol Med 2012;52:46–58.
  • Candas D, Li JJ. MnSOD in oxidative stress response-potential regulation via mitochondrial protein influx. Antioxid Redox Signal 2014;20:1599–1617.
  • Ozden O, Park SH, Kim HS, Jiang H, Coleman MC, Spitz DR, et al. Acetylation of MnSOD directs enzymatic activity responding to cellular nutrient status or oxidative stress. Aging 2011;3:102–107.
  • Dinic S, Arambasic J, Mihailovic M, Uskokovic A, Grdovic N, Markovic J, et al. Decreased O-GlcNAcylation of the key proteins in kinase and redox signalling pathways is a novel mechanism of the beneficial effect of alpha-lipoic acid in diabetic liver. Br J Nutr 2013;110:401–412.
  • Arambasic J, Mihailovic M, Uskokovic A, Dinic S, Grdovic N, Markovic J, et al. Alpha-lipoic acid upregulates antioxidant enzyme gene expression and enzymatic activity in diabetic rat kidneys through an O-GlcNAc-dependent mechanism. Eur J Nutr 2013;52:1461–1473.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.