Identification of O-GlcNAc modification targets in mouse retinal pericytes: Implication of p53 in pathogenesis of diabetic retinopathy

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Gurel, Zafer ^a   Zaro, Balyn W ^b   Pratt, Matthew R ^b   Sheibani, Nader ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOSUGAR; GLUCOSE; O LINKED BETA N ACETYLGLUCOSAMINE; PROTEIN P53; UNCLASSIFIED DRUG; ALLOXAN; N ACETYLGLUCOSAMINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CLICK CHEMISTRY; CONTROLLED STUDY; DIABETIC RETINOPATHY; DISEASE COURSE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOUSE; NONHUMAN; PATHOGENESIS; PERICYTE; PROTEIN ANALYSIS; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN TARGETING; RETINA CELL; SIGNAL TRANSDUCTION; ANIMAL; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; ENDOTHELIUM CELL; GLYCOSYLATION; HYPERGLYCEMIA; METABOLISM; RETINA;

ACETYLGLUCOSAMINE; ALLOXAN; ANIMALS; APOPTOSIS; DIABETIC RETINOPATHY; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; GLUCOSE; GLYCOSYLATION; HYPERGLYCEMIA; MICE; PERICYTES; RETINA; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84900391018     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095561     Document Type: Article

References (64)

1. Rathmann W, Giani G (2004) Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27: 2568-2569; author reply 2569.
2. Frank RN (2004) Diabetic retinopathy. N Engl J Med 350: 48-58.
3. Gardner TW, Antonetti DA (2007) A prize catch for diabetic retinopathy. Nat Med 13: 131-132.
4. Cheung N, Mitchell P, Wong TY (2010) Diabetic retinopathy. Lancet 376: 124-136.
5. Aiello LP (2005) Angiogenic pathways in diabetic retinopathy. The New England journal of medicine 353: 839-841.
6. Ngoh GA, Jones SP (2008) New insights into metabolic signaling and cell survival: the role of beta-O-linkage of N-acetylglucosamine. J Pharmacol Exp Ther 327: 602-609.
7. Ngoh GA, Facundo HT, Zafir A, Jones SP (2010) O-GlcNAc signaling in the cardiovascular system. Circ Res 107: 171-185.
8. McClain DA, Lubas WA, Cooksey RC, Hazel M, Parker GJ, et al. (2002) Altered glycan-dependent signaling induces insulin resistance and hyperleptinemia. Proc Natl Acad Sci U S A 99: 10695-10699.
9. Whelan SA, Lane MD, Hart GW (2008) Regulation of the O-linked beta-N-acetylglucosamine transferase by insulin signaling. J Biol Chem 283: 21411-21417.
10. Yang X, Ongusaha PP, Miles PD, Havstad JC, Zhang F, et al. (2008) Phosphoinositide signalling links O-GlcNAc transferase to insulin resistance. Nature 451: 964-969. (Pubitemid 351301737)
11. Gurel Z, Sieg KM, Shallow KD, Sorenson CM, Sheibani N (2013) Retinal O-linked N-acetylglucosamine protein modifications: implications for postnatal retinal vascularization and the pathogenesis of diabetic retinopathy. Mol Vis 19: 1047-1059.
12. Cogan DG, Toussaint D, Kuwabara T (1961) Retinal vascular patterns. IV. Diabetic retinopathy. Arch Ophthalmol 66: 366-378.
13. Scheef E, Wang S, Sorenson CM, Sheibani N (2005) Isolation and characterization of murine retinal astrocytes. Mol Vis 11: 613-624. (Pubitemid 41410213)
14. Scheef EA, Sorenson CM, Sheibani N (2009) Attenuation of proliferation and migration of retinal pericytes in the absence of thrombospondin-1. Am J Physiol Cell Physiol 296: C724-734.
15. Su X, Sorenson CM, Sheibani N (2003) Isolation and characterization of murine retinal endothelial cells. Mol Vis 9: 171-178. (Pubitemid 38097583)
16. Gurcel C, Vercoutter-Edouart AS, Fonbonne C, Mortuaire M, Salvador A, et al. (2008) Identification of new O-GlcNAc modified proteins using a click-chemistry-based tagging. Anal Bioanal Chem 390: 2089-2097.
17. Zaro BW, Yang YY, Hang HC, Pratt MR (2011) Chemical reporters for fluorescent detection and identification of O-GlcNAc-modified proteins reveal glycosylation of the ubiquitin ligase NEDD4-1. Proc Natl Acad Sci U S A 108: 8146-8151.
18. Charron G, Zhang MM, Yount JS, Wilson J, Raghavan AS, et al. (2009) Robust fluorescent detection of protein fatty-acylation with chemical reporters. J Am Chem Soc 131: 4967-4975.
19. Hahne H, Sobotzki N, Nyberg T, Helm D, Borodkin VS, et al. (2013) Proteome wide purification and identification of O-GlcNAc-modified proteins using click chemistry and mass spectrometry. J Proteome Res 12: 927-936.
20. Yang WH, Kim JE, Nam HW, Ju JW, Kim HS, et al. (2006) Modification of p53 with O-linked N-acetylglucosamine regulates p53 activity and stability. Nat Cell Biol 8: 1074-1083. (Pubitemid 44473602)
21. Zachara NE, O'Donnell N, Cheung WD, Mercer JJ, Marth JD, et al. (2004) Dynamic O-GlcNAc modification of nucleocytoplasmic proteins in response to stress. A survival response of mammalian cells. The Journal of biological chemistry 279: 30133-30142. (Pubitemid 38937936)
22. Kim YH, Kim YS, Kang SS, Noh HS, Kim HJ, et al. (2005) Expression of 14-3-3 zeta and interaction with protein kinase C in the rat retina in early diabetes. Diabetologia 48: 1411-1415. (Pubitemid 41186109)
23. Gao XY, Kuang HY, Zou W, Liu XM, Lin HB, et al. (2009) The timing of reinstitution of good blood glucose control affects apoptosis and expression of Bax and Bcl-2 in the retina of diabetic rats. Molecular biology reports 36: 1977-1982.
24. Kubota S, Ozawa Y, Kurihara T, Sasaki M, Yuki K, et al. (2011) Roles of AMP-activated protein kinase in diabetes-induced retinal inflammation. Investigative ophthalmology & visual science 52: 9142-9148.
25. Ruan HB, Nie Y, Yang X (2013) Regulation of protein degradation by O-GlcNAcylation: crosstalk with ubiquitination. Mol Cell Proteomics.
26. Morrison DK (2009) The 14-3-3 proteins: integrators of diverse signaling cues that impact cell fate and cancer development. Trends Cell Biol 19: 16-23.
27. Porter GW, Khuri FR, Fu H (2006) Dynamic 14-3-3/client protein interactions integrate survival and apoptotic pathways. Semin Cancer Biol 16: 193-202. (Pubitemid 43796125)
28. Kim EJ, Kho JH, Kang MR, Um SJ (2007) Active regulator of SIRT1 cooperates with SIRT1 and facilitates suppression of p53 activity. Mol Cell 28: 277-290.
29. Burastero SE, Fabbri M (2012) Aminoacyl-tRNA synthetase-interacting multifunctional protein-1 (AIMP1): the member of a molecular hub with unexpected functions, including CD4 T cell homeostasis. Clin Immunol 143: 207-209.
30. Berger AC, Tang G, Alexander HR, Libutti SK (2000) Endothelial monocyte-activating polypeptide II, a tumor-derived cytokine that plays an important role in inflammation, apoptosis, and angiogenesis. J Immunother 23: 519-527.
31. Yang Z, Wang WE, Zhang Q (2013) CIAPIN1 siRNA inhibits proliferation, migration and promotes apoptosis of VSMCs by regulating Bcl-2 and Bax. Curr Neurovasc Res 10: 4-10.
32. Renault TT, Manon S (2011) Bax: Addressed to kill. Biochimie 93: 1379-1391.
33. Jablonski EM, Webb AN, McConnell NA, Riley MC, Hughes FM Jr (2004) Plasma membrane aquaporin activity can affect the rate of apoptosis but is inhibited after apoptotic volume decrease. Am J Physiol Cell Physiol 286: C975-985. (Pubitemid 38543826)
34. Ammirante M, De Laurenzi V, Graziano V, Turco MC, Rosati A (2010) BAG3 is required for IKKalpha nuclear translocation and emergence of castration resistant prostate cancer. Cell Death Dis 2: e139.
35. Rosati A, Graziano V, De Laurenzi V, Pascale M, Turco MC (2011) BAG3: a multifaceted protein that regulates major cell pathways. Cell Death Dis 2: e141.
36. Festa M, Del Valle L, Khalili K, Franco R, Scognamiglio G, et al. (2011) BAG3 protein is overexpressed in human glioblastoma and is a potential target for therapy. Am J Pathol 178: 2504-2512.
37. Benjamin JM, Nelson WJ (2008) Bench to bedside and back again: molecular mechanisms of alpha-catenin function and roles in tumorigenesis. Semin Cancer Biol 18: 53-64. (Pubitemid 350266369)
38. Cheung CT, Singh R, Yoon AR, Hasan MK, Yaguchi T, et al. (2011) Molecular characterization of apoptosis induced by CARF silencing in human cancer cells. Cell Death Differ 18: 589-601.
39. Kaul SC, Hasan K, Wadhwa R (2006) CARF regulates p19ARF-p53-p21WAF1 senescence pathway by multiple checkpoints. Ann N Y Acad Sci 1067: 217-219. (Pubitemid 43806326)
40. Cheung CT, Hasan MK, Widodo N, Kaul SC, Wadhwa R (2009) CARF: an emerging regulator of p53 tumor suppressor and senescence pathway. Mech Ageing Dev 130: 18-23.
41. Marcel V, Dichtel-Danjoy ML, Sagne C, Hafsi H, Ma D, et al. (2011) Biological functions of p53 isoforms through evolution: lessons from animal and cellular models. Cell Death Differ 18: 1815-1824.
42. Pietsch EC, Sykes SM, McMahon SB, Murphy ME (2008) The p53 family and programmed cell death. Oncogene 27: 6507-6521.
43. McPherson JP, Goldenberg GJ (1998) Induction of apoptosis by deregulated expression of DNA topoisomerase IIalpha. Cancer Res 58: 4519-4524. (Pubitemid 28480606)
44. Otera H, Ishihara N, Mihara K (2013) New insights into the function and regulation of mitochondrial fission. Biochim Biophys Acta 1833: 1256-1268.
45. Hsu DK, Yang RY, Liu FT (2006) Galectins in apoptosis. Methods Enzymol 417: 256-273. (Pubitemid 44792714)
46. Joly AL, Wettstein G, Mignot G, Ghiringhelli F, Garrido C (2010) Dual role of heat shock proteins as regulators of apoptosis and innate immunity. J Innate Immun 2: 238-247.
47. Meares GP, Zmijewska AA, Jope RS (2008) HSP105 interacts with GRP78 and GSK3 and promotes ER stress-induced caspase-3 activation. Cell Signal 20: 347-358.
48. Li Y, Shin D, Kwon SH (2013) Histone deacetylase 6 plays a role as a distinct regulator of diverse cellular processes. FEBS J 280: 775-793.
49. Sahlgren CM, Pallari HM, He T, Chou YH, Goldman RD, et al. (2006) A nestin scaffold links Cdk5/p35 signaling to oxidant-induced cell death. EMBO J 25: 4808-4819. (Pubitemid 44607026)
50. Li Z, Hann SR (2009) The Myc-nucleophosmin-ARF network: a complex web unveiled. Cell Cycle 8: 2703-2707.
51. Chae HZ, Oubrahim H, Park JW, Rhee SG, Chock PB (2012) Protein glutathionylation in the regulation of peroxiredoxins: a family of thiol-specific peroxidases that function as antioxidants, molecular chaperones, and signal modulators. Antioxid Redox Signal 16: 506-523.
52. Brigelius-Flohe R, Maiorino M (2013) Glutathione peroxidases. Biochim Biophys Acta 1830: 3289-3303.
53. Shahzidi S, Brech A, Sioud M, Li X, Suo Z, et al. (2013) Lamin A/C cleavage by caspase-6 activation is crucial for apoptotic induction by photodynamic therapy with hexaminolevulinate in human B-cell lymphoma cells. Cancer Lett 339: 25-32.
54. Fuller-Pace FV (2013) The DEAD box proteins DDX5 (p68) and DDX17 (p72): multi-tasking transcriptional regulators. Biochim Biophys Acta 1829: 756-763.
55. Strappazzon F, Torch S, Chatellard-Causse C, Petiot A, Thibert C, et al. (2010) Alix is involved in caspase 9 activation during calcium-induced apoptosis. Biochem Biophys Res Commun 397: 64-69.
56. Mahul-Mellier AL, Strappazzon F, Petiot A, Chatellard-Causse C, Torch S, et al. (2008) Alix and ALG-2 are involved in tumor necrosis factor receptor 1-induced cell death. J Biol Chem 283: 34954-34965.
57. Wan Q, Kuang E, Dong W, Zhou S, Xu H, et al. (2007) Reticulon 3 mediates Bcl-2 accumulation in mitochondria in response to endoplasmic reticulum stress. Apoptosis 12: 319-328. (Pubitemid 46169912)
58. Inohara N, del Peso L, Koseki T, Chen S, Nunez G (1998) RICK, a novel protein kinase containing a caspase recruitment domain, interacts with CLARP and regulates CD95-mediated apoptosis. J Biol Chem 273: 12296-12300. (Pubitemid 28240597)
59. Romeo Y, Zhang X, Roux PP (2012) Regulation and function of the RSK family of protein kinases. Biochem J 441: 553-569.
60. Zhou A, Ou AC, Cho A, Benz EJ Jr, Huang SC (2008) Novel splicing factor RBM25 modulates Bcl-x pre-mRNA 59 splice site selection. Mol Cell Biol 28: 5924-5936.
61. Seshacharyulu P, Pandey P, Datta K, Batra SK (2013) Phosphatase: PP2A structural importance, regulation and its aberrant expression in cancer. Cancer Lett 335: 9-18.
62. Yan L, Lavin VA, Moser LR, Cui Q, Kanies C, et al. (2008) PP2A regulates the pro-apoptotic activity of FOXO1. J Biol Chem 283: 7411-7420.
63. Chen W, Wang H, Tao S, Zheng Y, Wu W, et al. (2013) Tumor protein translationally controlled 1 is a p53 target gene that promotes cell survival. Cell Cycle 12: 2321-2328.
64. Emami S (2011) Interplay between p53-family, their regulators, and PARPs in DNA repair. Clin Res Hepatol Gastroenterol 35: 98-104.