HIF-1α SUMOylation affects the stability and transcriptional activity of HIF-1α in human lens epithelial cells

Graefe's Archive for Clinical and Experimental Ophthalmology

Volumn 253, Issue 8, 2015, Pages 1279-1290

  Han, Xiao ^a   Wang, Xin Ling ^a   Li, Qin ^a   Dong, Xiao Xuan ^a   Zhang, Jin Song ^a   Yan, Qi Chang ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Cataract; Cbx4; HIF 1 ; PIASy; SUMO; SUMOylation

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; GLUCOSE; GLUCOSE TRANSPORTER 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; SUMO 1 PROTEIN; SUMO 2 PROTEIN; SUMO 3 PROTEIN; SUMO 4 PROTEIN; SUMO PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN A; CBX4 PROTEIN, HUMAN; PIAS4 PROTEIN, HUMAN; POLYCOMB GROUP PROTEIN; PROTEIN INHIBITOR OF ACTIVATED STAT; UBIQUITIN PROTEIN LIGASE;

ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; LENS EPITHELIUM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUMOYLATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; WESTERN BLOTTING; APOPTOSIS; CELL LINE; CYTOLOGY; DRUG EFFECTS; EPITHELIUM CELL; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; LENS; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

APOPTOSIS; BLOTTING, WESTERN; CELL LINE; EPITHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION REGULATION; GLUCOSE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LENS, CRYSTALLINE; POLYCOMB-GROUP PROTEINS; PROTEIN INHIBITORS OF ACTIVATED STAT; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUMOYLATION; UBIQUITIN-PROTEIN LIGASES;

EID: 84938417671     PISSN: 0721832X     EISSN: 1435702X     Source Type: Journal    
DOI: 10.1007/s00417-015-2999-x     Document Type: Article

References (42)

1. Iafusco D, Prisco F, Romano MR, Dell'omo R, Libondi T, Costagliola C (2011) Acute juvenile cataract in newly diagnosed type 1 diabetic patients: a description of six cases. Pediatr Diabetes 12:642–648. doi:10.1111/j.1399-5448.2010.00749.x
2. Jin YY, Huang K, Zou CC, Liang L, Wang XM, Jin J (2012) Reversible cataract as the presenting sign of diabetes mellitus: report of two cases and literature review. Iran J Pediatr 22:125–128
3. Grauslund J (2011) Eye complications and markers of morbidity and mortality in long-term type 1 diabetes. Acta Ophthalmol 89:1–19. doi:10.1111/j.1755-3768.2010.02105.x
4. Wu ZM, Yin XX, Ji L, Gao YY, Pan YM, Lu Q, Wang JY (2008) Ginkgo biloba extract prevents against apoptosis induced by high glucose in human lens epithelial cells. Acta Pharmacol Sin 29:1042–1050. doi:10.1111/j.1745-7254.2008.00837.x
5. Thiraphatthanavong P, Wattanathorn J, Muchimapura S, Wipawee TM, Wannanon P, Terdthai TU, Suriharn B, Lertrat K (2014) Preventive effect of Zea mays L. (purple waxy corn) on experimental diabetic cataract. Biomed Res Int 2014:507435. doi:10.1155/2014/507435
6. Park SE, Park JW, Cho YS, Ryu JH, Paick JS, Chun YS (2007) HIF-1alpha promotes survival of prostate cells at a high zinc environment. Prostate 67:1514–1523. doi:10.1002/pros.20641
7. Radreau P, Rhodes JD, Mithen RF, Kroon PA, Sanderson J (2009) Hypoxia-inducible factor-1 (HIF-1) pathway activation by quercetin in human lens epithelial cells. Exp Eye Res 89:995–1002. doi:10.1016/j.exer.2009.08.011
8. Sahin U, Ferhi O, Jeanne M, Benhenda S, Berthier C, Jollivet F, Niwa-Kawakita M, Faklaris O, Setterblad N, de Thé H, Lallemand-Breitenbach V (2014) Oxidative stress-induced assembly of PML nuclear bodies controls sumoylation of partner proteins. J Cell Biol 204:931–945. doi:10.1083/jcb.201305148
9. Feligioni M, Nisticò R (2013) SUMO: a (oxidative) stressed protein. Neuromolecular Med 15:707–719. doi:10.1007/s12017-013-8266-6
10. Chung HS, Wang SB, Venkatraman V, Murray CI, Van Eyk JE (2013) Cysteine oxidative posttranslational modifications: emerging regulation in the cardiovascular system. Circ Res 112:382–392. doi:10.1161/CIRCRESAHA.112.268680
11. Kerscher O, Felberbaum R, Hochstrasser M (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22:159–180. doi:10.1146/annurev.cellbio.22.010605.093503
12. Guo D, Li M, Zhang Y, Yang P, Eckenrode S, Hopkins D, Zheng W, Purohit S, Podolsky RH, Muir A, Wang J, Dong Z, Brusko T, Atkinson M, Pozzilli P, Zeidler A, Raffel LJ, Jacob CO, Park Y, Serrano-Rios M, Larrad MT, Zhang Z, Garchon HJ, Bach JF, Rotter JI, She JX, Wang CY (2004) A functional variant of SUMO4, a new I kappa B alpha modifier, is associated with type 1 diabetes. Nat Genet 36:837–841. doi:10.1038/ng1391
13. Dohmen RJ (2004) SUMO protein modification. Biochim Biophys Acta 1695:113–131. doi:10.1016/j.bbamcr.2004.09.021
14. Hay RT (2005) SUMO: a history of modification. Mol Cell 18:1–12. doi:10.1016/j.molcel.2005.03.012
15. Geiss-Friedlander R, Melchior F (2007) Concepts in sumoylation: a decade on. Nat Rev Mol Cell Biol 8:947–956. doi:10.1038/nrm2293
16. Johnson ES (2004) Protein modification by SUMO. Annu Rev Biochem 73:355–382. doi:10.1146/annurev.biochem.73.011303.074118
17. Li J, Xu Y, Long XD, Wang W, Jiao HK, Mei Z, Yin QQ, Ma LN, Zhou AW, Wang LS, Yao M, Xia Q, Chen GQ (2014) Cbx4 governs HIF-1alpha to potentiate angiogenesis of hepatocellular carcinoma by its SUMO E3 ligase activity. Cancer Cell 25:118–131. doi:10.1016/j.ccr.2013.12.008
18. Pugh CW, Ratcliffe PJ (2003) Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 9:677–684. doi:10.1038/nm0603-677
19. Merriman-Smith BR, Krushinsky A, Kistler J, Donaldson PJ (2003) Expression patterns for glucose transporters GLUT1 and GLUT3 in the normal rat lens and in models of diabetic cataract. Invest Ophthalmol Vis Sci 44:3458–3466. doi:10.1167/iovs. 02-1235
20. Garcia CM, Shui YB, Kamath M, DeVillar J, Johnson RS, Gerber HP, Ferrara N, Robinson ML, Beebe DC (2009) The function of VEGF-A in lens development: formation of the hyaloid capillary network and protection against transient nuclear cataracts. Exp Eye Res 88:270–276. doi:10.1016/j.exer.2008.07.017
21. McLaren AT, Marsden PA, Mazer CD, Baker AJ, Stewart DJ, Tsui AK, Li X, Yucel Y, Robb M, Boyd SR, Liu E, Yu J, Hare GM (2007) Increased expression of HIF-1alpha, nNOS, and VEGF in the cerebral cortex of anemic rats. Am J Physiol Regul Integr Comp Physiol 292:R403–R414. doi:10.1152/ajpregu.00403.2006
22. Li S, Yang X, Wang P, Ran X (2013) The effects of GLUT1 on the survival of head and neck squamous cell carcinoma. Cell Physiol Biochem 32:624–634. doi:10.1159/000354466
23. Berra E, Richard DE, Gothié E, Pouysségur J (2001) HIF-1-dependent transcriptional activity is required for oxygen-mediated HIF-1alpha degradation. FEBS Lett 491:85–90. doi:10.1016/S0014-5793(01)02159-7
24. Bae SH, Jeong JW, Park JA, Kim SH, Bae MK, Choi SJ, Kim KW (2004) Sumoylation increases HIF-1alpha stability and its transcriptional activity. Biochem Biophys Res Commun 324:394–400. doi:10.1016/j.bbrc.2004.09.068
25. Shao R, Zhang FP, Tian F, Anders Friberg P, Wang X, Sjöland H, Billig H (2004) Increase of SUMO-1 expression in response to hypoxia: direct interaction with HIF-1alpha in adult mouse brain and heart in vivo. FEBS Lett 569:293–300. doi:10.1016/j.febslet.2004.05.079
26. Carbia-Nagashima A, Gerez J, Perez-Castro C, Paez-Pereda M, Silberstein S, Stalla GK, Holsboer F, Arzt E (2007) RSUME, a small RWD-containing protein, enhances SUMO conjugation and stabilizes HIF-1alpha during hypoxia. Cell 131:309–323. doi:10.1016/j.cell.2007.07.044
27. Cai Q, Verma SC, Kumar P, Ma M, Robertson ES (2010) Hypoxia inactivates the VHL tumor suppressor through PIASy-mediated SUMO modification. PLoS One 5:e9720. doi:10.1371/journal.pone.0009720
28. Germán RA, William KR, Adeline D, David HR, Wilson VG (2005) A universal strategy for proteomic studies of SUMO and other ubiquitin-like modifiers. Mol Cell Proteomics 4:56–72. doi:10.1074/mcp. M400149-MCP200
29. Chen XL, Reindle A, Johnson ES (2005) Misregulation of 2 microm circle copy number in a SUMO pathway mutant. Mol Cell Biol 25:4311–4320. doi:10.1128/MCB. 25.10.4311-4320.2005
30. Huang W, Xu L, Zhou X, Gao C, Yang M, Chen G, Zhu J, Jiang L, Gan H, Gou F, Feng H, Peng J, Xu Y (2013) High glucose induces activation of NF-kappaB inflammatory signaling through IkappaBalpha sumoylation in rat mesangial cells. Biochem Biophys Res Commun 438:568–574. doi:10.1016/j.bbrc.2013.07.065
31. Gill G (2004) SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes Dev 18:2046–2059. doi:10.1101/gad.1214604
32. Saitoh H, Hinchey J (2000) Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J Biol Chem 275:6252–6258. doi:10.1074/jbc.275.9.6252
33. Girdwood DW, Tatham MH, Hay RT (2004) SUMO and transcriptional regulation. Semin Cell Dev Biol 15:201–210. doi:10.1016/j.semcdb.2003.12.001
34. Harris AL (2002) Hypoxia–a key regulatory factor in tumour growth. Nat Rev Cancer 2:38–47. doi:10.1038/nrc704
35. Semenza G (2002) Signal transduction to hypoxia-inducible factor 1. Biochem Pharmacol 64:993–998. doi:10.1016/S0006-2952(02)01168-1
36. Shui YB, Beebe DC (2008) Age-dependent control of lens growth by hypoxia. Invest Ophthalmol Vis Sci 49:1023–1029. doi:10.1167/iovs. 07-1164
37. Schimmel J, Larsen KM, Matic I, van Hagen M, Cox J, Mann M, Andersen JS, Vertegaal AC (2008) The ubiquitin-proteasome system is a key component of the SUMO-2/3 cycle. Mol Cell Proteomics 7:2107–2122. doi:10.1074/mcp. M800025-MCP200
38. Uzunova K, Göttsche K, Miteva M, Weisshaar SR, Glanemann C, Schnellhardt M, Niessen M, Scheel H, Hofmann K, Johnson ES, Praefcke GJ, Dohmen RJ (2007) Ubiquitin-dependent proteolytic control of SUMO conjugates. J Biol Chem 282:34167–34175. doi:10.1074/jbc.M706505200
39. Castorálová M, Březinová D, Svéda M, Lipov J, Ruml T, Knejzlík Z (2012) SUMO-2/3 conjugates accumulating under heat shock or MG132 treatment result largely from new protein synthesis. Biochim Biophys Acta 1823:911–919. doi:10.1016/j.bbamcr.2012.01.010
40. Cui W, Bai Y, Luo P, Miao L, Cai L (2013) Preventive and therapeutic effects of MG132 by activating Nrf2-ARE signaling pathway on oxidative stress-induced cardiovascular and renal injury. Oxid Med Cell Longev 2013:306073. doi:10.1155/2013/306073
41. Wang Y, Sun W, Du B, Miao X, Bai Y, Xin Y, Tan Y, Cui W, Liu B, Cui T, Epstein PN, Fu Y, Cai L (2013) Therapeutic effect of MG-132 on diabetic cardiomyopathy is associated with its suppression of proteasomal activities: roles of Nrf2 and NF-κB. Am J Physiol Heart Circ Physiol 304:H567–H578. doi:10.1152/ajpheart.00650.2012
42. Cui W, Li B, Bai Y, Miao X, Chen Q, Sun W, Tan Y, Luo P, Zhang C, Zheng S, Epstein PN, Miao L, Cai L (2013) Potential role for Nrf2 activation in the therapeutic effect of MG132 on diabetic nephropathy in OVE26 diabetic mice. Am J Physiol Endocrinol Metab 304:E87–E99. doi:10.1152/ajpendo.00430.2012