Correlation between O-linked N-acetylglucosamine glycosylation modification and diabetic retinopathy_Chinese Journal of Ocular Fundus Diseases

Authors：

Zhang Yuan , Liu Kun ,  Chen Feng'e

Department of Ophthalmology, Shanghai General Hospital, Shanghai JiaoTong University School of Medicine, Shanghai 200080, China;

Corresponding author：

Chen Feng'e, Email: 13386259746@163.com

Keywords：

Diabetic retinopathy/etiology; Acetylglucosamine; Glycosylation; Review

DOI：

10.3760/cma.j.issn.1005-1015.2017.03.027

Video：

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O-linked N-acetylglucosamine (O-GlcNAc) glycosylation is an important form of post-translational protein modification, mainly intracellular. It is closely related to cellular signaling pathways, and is involved in signal transduction, gene transcription and other important biological processes. Studies have found that O-GlcNAc glycosylation is directly related with diabetic retinopathy (DR), further studies may help us to uncover the DR mechanism, and develop new strategies for the diagnosis and treatment of this disease.

Citation： Zhang Yuan, Liu Kun, Chen Feng'e. Correlation between O-linked N-acetylglucosamine glycosylation modification and diabetic retinopathy. Chinese Journal of Ocular Fundus Diseases, 2017, 33(3): 318-321. doi: 10.3760/cma.j.issn.1005-1015.2017.03.027 Copy

1.	Wells L, Vosseller K, Hart GW. Glycosylation of nucleocytoplasmic proteins: signal transduction and O-GlcNAc[J]. Science, 2001, 291(5512): 2376-2378.
2.	Hu Y, Belke D, Suarez J, et al. Adenovirus-mediated over expression of O-GlcNAcase improves contractile function in the diabetic heart[J]. Circ Res, 2005, 96(9): 1006-1013. DOI: 10.1161/01.RES.0000165478.06813.58.
3.	Fricovsky ES, Suarez J, Ihm SH, et al. Excess protein O-GlcNAcylation and the progression of diabetic cardiomyopathy[J]. Am J Physiol Regul Integr Comp Physiol, 2012, 303(7): 689-699. DOI: 10.1152/ajpregu.00548.2011.
4.	Degrell P, Cseh J, Mohas M, et al. Evidence of O-linked N-acetylglucosamine in diabetic nephropathy[J]. Life Sci, 2009, 84(13-14): 389-393. DOI: 10.1016/j.lfs.2009.01.007.
5.	Zhang Y, Qu Y, Niu T, et al. O-GlcNAc modification of Sp1 mediates hyperglycaemia-induced ICAM-1 up-regulation in endothelial cells[J]. Biochem Biophys Res Commun, 2017, 484(1): 79-84. DOI: 10.1016/j.bbrc.2017.01.068.
6.	Iyer SP, Hart GW. Roles of the tetratricopeptide repeat domain in O-GlcNAc transferase targeting and protein substrate specificity[J]. J Biol Chem, 2003, 278(27): 24608-24616. DOI: 10.1074/jbc.M300036200.
7.	Zeidan Q, Hart GW. The intersections between O-GlcNAcylation and phosphorylation: implications for multiple signaling pathways[J]. J Cell Sci, 2010, 123(Pt 1): 13-22. DOI: 10.1242/jcs.053678.
8.	Torres CR, Hart GW. Topography and polypeptide distribution of terminal N-acetylglucosamine residues on the surfaces of intact lymphocytes: evidence for O-linked GlcNAc[J]. J Biol Chem, 1984, 259(5): 3308-3317.
9.	Xu J, Zhou JY, Wei WZ, et al. Sp1-mediated TRAIL induction in chemosensitization[J]. Cancer Res, 2008, 68(16): 6718-6726. DOI: 10.1158/0008-5472.CAN-08-0657.
10.	Grinstein E, Jundt F, Weinert I, et al. Sp1 as G1 cell cycle phase specific transcription factor in epithelial cells[J]. Oncogene, 2002, 21(10): 1485-1492. DOI: 10.1038/sj.onc.1205211.
11.	Zhang F, Su K, Yang X, et al. O-GlcNAc modification is an endogenous inhibitor of the proteasome[J]. Cell, 2003, 115(6): 715-725.
12.	Donovan K, Alekseev O, Qi X, et al. O-GlcNAc modification of transcription factor Sp1 mediates hyperglycemia-induced VEGF-A upregulation in retinal cells[J]. Invest Ophthalmol Vis Sci, 2014, 55(12): 7862-7873. DOI: 10.1167/iovs.14-14048.
13.	Du XL, Edelstein D, Rossetti L, et al. Hyperglycemia-induced mitochondrial superoxide overproduction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation[J]. Proc Natl Acad Sci USA, 2000, 97(22): 12222-12226. DOI: 10.1073/pnas.97.22.12222.
14.	Sebban H, Courtois G. NF-kappaB and inflammation in genetic disease[J]. Biochem Pharmacol, 2006, 72(9): 1153-1160. DOI: 10.1016/j.bcp.2006.08.006.
15.	Baker RG, Hayden MS, Ghosh S. NF-kappa B, inflammation, and metabolic disease[J]. Cell Metab, 2011, 13(1): 11-22. DOI: 10.1016/j.cmet.2010.12.008.
16.	Zou L, Yang S, Champattanachai V, et al. Glucosamine improves cardiac function following trauma-hemorrhage by increased protein O-GlcNAcylation and attenuation of NF-kappaB signaling[J]. Am J Physiol Heart Circ Physiol, 2009, 296(2): 515-523. DOI: 10.1152/ajpheart.01025.2008.
17.	Hart GW. Nutrient regulation of immunity: O-GlcNAcylation regulates stimulus-specific NF-kappaB-dependent transcription[J]. Sci Signal, 2013, 6(290): 26. DOI: 10.1126/scisignal.2004596.
18.	Xing D, Gong K, Feng W, et al. O-GlcNAc modification of NF kappaB p65 inhibits TNF-alpha-induced inflammatory mediator expression in rat aortic smooth muscle cells[J/OL]. PLoS One, 2011, 6(8): 24021[2011-08-31]. . DOI: 10.1371/journal.pone.0024021.
19.	Rockwell LC, Pillai S, Olson CE, et al. Inhibition of vascular endothelial growth factor/vascular permeability factor action blocks estrogen-induced uterine edema and implantation in rodents[J]. Biol Reprod, 2002, 67(6): 1804-1810.
20.	Amin RH, Frank RN, Kennedy A, et al. Vascular endothelial growth factor is present in glial cells of the retina and optic nerve of human subjects with nonproliferative diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 1997, 38(1): 36-47.
21.	Sundstrom JM, Tash BR, Murakami T, et al. Identification and analysis of occludin phosphosites: a combined mass spectrometry and bioinformatics approach[J]. J Proteome Res, 2009, 8(2): 808-817. DOI: 10.1021/pr7007913.
22.	Mee CJ, Farquhar MJ, Harris HJ, et al. Hepatitis C virus infection reduces hepatocellular polarity in a vascular endothelial growth factor-dependent manner[J]. Gastroenterology, 2010, 138(3): 1134-1142. DOI: 10.1053/j.gastro.2009.11.047.
23.	Butt AM, Feng D, Nasrullah I, et al. Computational identification of interplay between phosphorylation and O-beta-glycosylation of human occludin as potential mechanism to impair hepatitis C virus entry[J]. Infect Genet Evol, 2012, 12(6): 1235-1245. DOI: 10.1016/j.meegid.2012.04.001.
24.	Patel JI, Tombran-Tink J, Hykin PG, et al. Vitreous and aqueous concentrations of proangiogenic, antiangiogenic factors and other cytokines in diabetic retinopathy patients with macular edema: implications for structural differences in macular profiles[J]. Exp Eye Res, 2006, 82(5): 798-806. DOI: 10.1016/j.exer.2005.10.002.
25.	Yuzwa SA, Macauley MS, Heinonen JE, et al. A potent mechanism-inspired O-GlcNAcase inhibitor that blocks phosphorylation of tau in vivo[J]. Nat Chem Biol, 2008, 4(8): 483-490. DOI: 10.1038/nchembio.96.
26.	Arnold CS, Johnson GV, Cole RN, et al. The microtubule-associated protein tau is extensively modified with O-linked N-acetylglucosamine[J]. J Biol Chem, 1996, 271(46): 28741-28744.
27.	Vinores SA, Derevjanik NL, Mahlow J, et al. Class Ⅲ beta-tubulin in human retinal pigment epithelial cells in culture and in epiretinal membranes[J]. Exp Eye Res, 1995, 60(4): 385-400.
28.	Chung EJ, Chun JN, Jung SA, et al. TGF-beta-stimulated aberrant expression of class Ⅲ beta-tubulin via the ERK signaling pathway in cultured retinal pigment epithelial cells[J]. Biochem Biophys Res Commun, 2011, 415(2): 367-372. DOI: 10.1016/j.bbrc.2011.10.074.
29.	Matthews JA, Acevedo-Duncan M, Potter RL. Selective decrease of membrane-associated PKC-alpha and PKC-epsilon in response to elevated intracellular O-GlcNAc levels in transformed human glial cells[J]. Biochim Biophys Acta, 2005, 1743(3): 305-315. DOI: 10.1016/j.bbamcr.2004.11.001.
30.	Gurel Z, Sieg KM, Shallow KD, et al. Retinal O-linked N-acetylglucosamine protein modifications: implications for postnatal retinal vascularization and the pathogenesis of diabetic retinopathy[J]. Mol Vis, 2013, 19: 1047-1059.

1. Wells L, Vosseller K, Hart GW. Glycosylation of nucleocytoplasmic proteins: signal transduction and O-GlcNAc[J]. Science, 2001, 291(5512): 2376-2378.
2. Hu Y, Belke D, Suarez J, et al. Adenovirus-mediated over expression of O-GlcNAcase improves contractile function in the diabetic heart[J]. Circ Res, 2005, 96(9): 1006-1013. DOI: 10.1161/01.RES.0000165478.06813.58.
3. Fricovsky ES, Suarez J, Ihm SH, et al. Excess protein O-GlcNAcylation and the progression of diabetic cardiomyopathy[J]. Am J Physiol Regul Integr Comp Physiol, 2012, 303(7): 689-699. DOI: 10.1152/ajpregu.00548.2011.
4. Degrell P, Cseh J, Mohas M, et al. Evidence of O-linked N-acetylglucosamine in diabetic nephropathy[J]. Life Sci, 2009, 84(13-14): 389-393. DOI: 10.1016/j.lfs.2009.01.007.
5. Zhang Y, Qu Y, Niu T, et al. O-GlcNAc modification of Sp1 mediates hyperglycaemia-induced ICAM-1 up-regulation in endothelial cells[J]. Biochem Biophys Res Commun, 2017, 484(1): 79-84. DOI: 10.1016/j.bbrc.2017.01.068.
6. Iyer SP, Hart GW. Roles of the tetratricopeptide repeat domain in O-GlcNAc transferase targeting and protein substrate specificity[J]. J Biol Chem, 2003, 278(27): 24608-24616. DOI: 10.1074/jbc.M300036200.
7. Zeidan Q, Hart GW. The intersections between O-GlcNAcylation and phosphorylation: implications for multiple signaling pathways[J]. J Cell Sci, 2010, 123(Pt 1): 13-22. DOI: 10.1242/jcs.053678.
8. Torres CR, Hart GW. Topography and polypeptide distribution of terminal N-acetylglucosamine residues on the surfaces of intact lymphocytes: evidence for O-linked GlcNAc[J]. J Biol Chem, 1984, 259(5): 3308-3317.
9. Xu J, Zhou JY, Wei WZ, et al. Sp1-mediated TRAIL induction in chemosensitization[J]. Cancer Res, 2008, 68(16): 6718-6726. DOI: 10.1158/0008-5472.CAN-08-0657.
10. Grinstein E, Jundt F, Weinert I, et al. Sp1 as G1 cell cycle phase specific transcription factor in epithelial cells[J]. Oncogene, 2002, 21(10): 1485-1492. DOI: 10.1038/sj.onc.1205211.
11. Zhang F, Su K, Yang X, et al. O-GlcNAc modification is an endogenous inhibitor of the proteasome[J]. Cell, 2003, 115(6): 715-725.
12. Donovan K, Alekseev O, Qi X, et al. O-GlcNAc modification of transcription factor Sp1 mediates hyperglycemia-induced VEGF-A upregulation in retinal cells[J]. Invest Ophthalmol Vis Sci, 2014, 55(12): 7862-7873. DOI: 10.1167/iovs.14-14048.
13. Du XL, Edelstein D, Rossetti L, et al. Hyperglycemia-induced mitochondrial superoxide overproduction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation[J]. Proc Natl Acad Sci USA, 2000, 97(22): 12222-12226. DOI: 10.1073/pnas.97.22.12222.
14. Sebban H, Courtois G. NF-kappaB and inflammation in genetic disease[J]. Biochem Pharmacol, 2006, 72(9): 1153-1160. DOI: 10.1016/j.bcp.2006.08.006.
15. Baker RG, Hayden MS, Ghosh S. NF-kappa B, inflammation, and metabolic disease[J]. Cell Metab, 2011, 13(1): 11-22. DOI: 10.1016/j.cmet.2010.12.008.
16. Zou L, Yang S, Champattanachai V, et al. Glucosamine improves cardiac function following trauma-hemorrhage by increased protein O-GlcNAcylation and attenuation of NF-kappaB signaling[J]. Am J Physiol Heart Circ Physiol, 2009, 296(2): 515-523. DOI: 10.1152/ajpheart.01025.2008.
17. Hart GW. Nutrient regulation of immunity: O-GlcNAcylation regulates stimulus-specific NF-kappaB-dependent transcription[J]. Sci Signal, 2013, 6(290): 26. DOI: 10.1126/scisignal.2004596.
18. Xing D, Gong K, Feng W, et al. O-GlcNAc modification of NF kappaB p65 inhibits TNF-alpha-induced inflammatory mediator expression in rat aortic smooth muscle cells[J/OL]. PLoS One, 2011, 6(8): 24021[2011-08-31]. . DOI: 10.1371/journal.pone.0024021.
19. Rockwell LC, Pillai S, Olson CE, et al. Inhibition of vascular endothelial growth factor/vascular permeability factor action blocks estrogen-induced uterine edema and implantation in rodents[J]. Biol Reprod, 2002, 67(6): 1804-1810.
20. Amin RH, Frank RN, Kennedy A, et al. Vascular endothelial growth factor is present in glial cells of the retina and optic nerve of human subjects with nonproliferative diabetic retinopathy[J]. Invest Ophthalmol Vis Sci, 1997, 38(1): 36-47.
21. Sundstrom JM, Tash BR, Murakami T, et al. Identification and analysis of occludin phosphosites: a combined mass spectrometry and bioinformatics approach[J]. J Proteome Res, 2009, 8(2): 808-817. DOI: 10.1021/pr7007913.
22. Mee CJ, Farquhar MJ, Harris HJ, et al. Hepatitis C virus infection reduces hepatocellular polarity in a vascular endothelial growth factor-dependent manner[J]. Gastroenterology, 2010, 138(3): 1134-1142. DOI: 10.1053/j.gastro.2009.11.047.
23. Butt AM, Feng D, Nasrullah I, et al. Computational identification of interplay between phosphorylation and O-beta-glycosylation of human occludin as potential mechanism to impair hepatitis C virus entry[J]. Infect Genet Evol, 2012, 12(6): 1235-1245. DOI: 10.1016/j.meegid.2012.04.001.
24. Patel JI, Tombran-Tink J, Hykin PG, et al. Vitreous and aqueous concentrations of proangiogenic, antiangiogenic factors and other cytokines in diabetic retinopathy patients with macular edema: implications for structural differences in macular profiles[J]. Exp Eye Res, 2006, 82(5): 798-806. DOI: 10.1016/j.exer.2005.10.002.
25. Yuzwa SA, Macauley MS, Heinonen JE, et al. A potent mechanism-inspired O-GlcNAcase inhibitor that blocks phosphorylation of tau in vivo[J]. Nat Chem Biol, 2008, 4(8): 483-490. DOI: 10.1038/nchembio.96.
26. Arnold CS, Johnson GV, Cole RN, et al. The microtubule-associated protein tau is extensively modified with O-linked N-acetylglucosamine[J]. J Biol Chem, 1996, 271(46): 28741-28744.
27. Vinores SA, Derevjanik NL, Mahlow J, et al. Class Ⅲ beta-tubulin in human retinal pigment epithelial cells in culture and in epiretinal membranes[J]. Exp Eye Res, 1995, 60(4): 385-400.
28. Chung EJ, Chun JN, Jung SA, et al. TGF-beta-stimulated aberrant expression of class Ⅲ beta-tubulin via the ERK signaling pathway in cultured retinal pigment epithelial cells[J]. Biochem Biophys Res Commun, 2011, 415(2): 367-372. DOI: 10.1016/j.bbrc.2011.10.074.
29. Matthews JA, Acevedo-Duncan M, Potter RL. Selective decrease of membrane-associated PKC-alpha and PKC-epsilon in response to elevated intracellular O-GlcNAc levels in transformed human glial cells[J]. Biochim Biophys Acta, 2005, 1743(3): 305-315. DOI: 10.1016/j.bbamcr.2004.11.001.
30. Gurel Z, Sieg KM, Shallow KD, et al. Retinal O-linked N-acetylglucosamine protein modifications: implications for postnatal retinal vascularization and the pathogenesis of diabetic retinopathy[J]. Mol Vis, 2013, 19: 1047-1059.

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