Activation of endoplasmic reticulum stress by hyperglycemia is essential for Müller cell-derived inflammatory cytokine production in diabetes

Diabetes

Volumn 61, Issue 2, 2012, Pages 492-504

  Zhong, Yimin ^a,b   Li, Jingming ^a   Chen, Yanming ^a,c   Wang, Joshua J ^a   Ratan, Rajiv ^d   Zhang, Sarah X ^a,e  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b SUN YAT SEN UNIVERSITY   (China)

^c SUN YAT SEN UNIVERSITY   (China)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; BIOLOGICAL MARKER; CYTOKINE; GLUCOSE; VASCULOTROPIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIABETES MELLITUS; DIABETIC RETINOPATHY; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION; HYPERGLYCEMIA; IMMUNE RESPONSE; IMMUNOCYTOCHEMISTRY; INFLAMMATION; MOUSE; MUELLER CELL; NONHUMAN; PRIORITY JOURNAL; RAT; RETINA CELL; STREPTOZOCIN DIABETES;

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELLS, CULTURED; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; ENDOPLASMIC RETICULUM STRESS; HYPERGLYCEMIA; INFLAMMATION MEDIATORS; INTERCELLULAR ADHESION MOLECULE-1; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE; MICE, INBRED C57BL; RATS; RETINA; STREPTOZOCIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84863081447     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db11-0315     Document Type: Article

References (37)

1. Joussen AM, Poulaki V, Le ML, et al. A central role for inflammation in the pathogenesis of diabetic retinopathy. FASEB J 2004;18:1450-1452 (Pubitemid 39561611)
2. Kern TS. Contributions of inflammatory processes to the development of the early stages of diabetic retinopathy. Exp Diabetes Res 2007;2007:95103
3. Li J, Wang JJ, Chen D, et al. Systemic administration of HMG-CoA reductase inhibitor protects the blood-retinal barrier and ameliorates retinal inflammation in type 2 diabetes. Exp Eye Res 2009;89:71-78
4. Zhang SX, Wang JJ, Gao G, Shao C, Mott R, Ma JX. Pigment epithelium-derived factor (PEDF) is an endogenous antiinflammatory factor. FASEB J 2006;20:323-325 (Pubitemid 46671158)
5. Mizutani M, Gerhardinger C, Lorenzi M. Müller cell changes in human diabetic retinopathy. Diabetes 1998;47:445-449 (Pubitemid 28104208)
6. Shelton MD, Distler AM, Kern TS, Mieyal JJ. Glutaredoxin regulates autocrine and paracrine proinflammatory responses in retinal glial (Müller) cells. J Biol Chem 2009;284:4760-4766
7. Wang J, Xu X, Elliott MH, Zhu M, Le YZ. Müller cell-derived VEGF is essential for diabetes-induced retinal inflammation and vascular leakage. Diabetes 2010;59:2297-2305
8. Yoshida H. ER stress and diseases. FEBS J 2007;274:630-658 (Pubitemid 46150855)
9. Ozcan U, Yilmaz E, Ozcan L, et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006;313:1137-1140 (Pubitemid 44300242)
10. Kaser A, Lee AH, Franke A, et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 2008;134:743-756
11. Li J, Wang JJ, Yu Q, Wang M, Zhang SX. Endoplasmic reticulum stress is implicated in retinal inflammation and diabetic retinopathy. FEBS Lett 2009;583:1521-1527
12. Li J, Wang JJ, Yu Q, Chen K, Mahadev K, Zhang SX. Inhibition of reactive oxygen species by Lovastatin downregulates vascular endothelial growth factor expression and ameliorates blood-retinal barrier breakdown in db/db mice: role of NADPH oxidase 4. Diabetes 2010;59:1528-1538
13. Lange PS, Chavez JC, Pinto JT, et al. ATF4 is an oxidative stress-inducible, prodeath transcription factor in neurons in vitro and in vivo. J Exp Med 2008;205:1227-1242 (Pubitemid 351679695)
14. Li J, Wang JJ, Zhang SX. Preconditioning with endoplasmic reticulum stress mitigates retinal endothelial inflammation via activation of X-box binding protein 1. J Biol Chem 2011;286:4912-4921
15. Malabanan KP, Khachigian LM. Activation transcription factor-4 and the acute vascular response to injury. J Mol Med (Berl) 2010;88:545-552
16. Gargalovic PS, Gharavi NM, Clark MJ, et al. The unfolded protein response is an important regulator of inflammatory genes in endothelial cells. Arterioscler Thromb Vasc Biol 2006;26:2490-2496 (Pubitemid 44607470)
17. Poulaki V, Qin W, Joussen AM, et al. Acute intensive insulin therapy exacerbates diabetic blood-retinal barrier breakdown via hypoxia-inducible factor-1alpha and VEGF. J Clin Invest 2002;109:805-815 (Pubitemid 34263157)
18. Kim H-T, Qiang W, Liu N, Scofield VL, Wong PK, Stoica G. Up-regulation of astrocyte cyclooxygenase-2, CCAAT/enhancer-binding protein-homology protein, glucose-related protein 78, eukaryotic initiation factor 2 alpha, and c-Jun N-terminal kinase by a neurovirulent murine retrovirus. J Neurovirol 2005;11:166-179 (Pubitemid 40852424)
19. Guma M, Rius J, Duong-Polk KX, Haddad GG, Lindsey JD, Karin M. Genetic and pharmacological inhibition of JNK ameliorates hypoxia-induced retinopathy through interference with VEGF expression. Proc Natl Acad Sci U S A 2009;106:8760-8765
20. Zhang SX, Sima J, Shao C, et al. Plasminogen kringle 5 reduces vascular leakage in the retina in rat models of oxygen-induced retinopathy and diabetes. Diabetologia 2004;47:124-131 (Pubitemid 38141948)
21. Zhang SX, Sima J, Wang JJ, Shao C, Fant J, Ma JX. Systemic and periocular deliveries of plasminogen kringle 5 reduce vascular leakage in rat models of oxygen-induced retinopathy and diabetes. Curr Eye Res 2005;30:681-689 (Pubitemid 41306390)
22. Deng J, Lu PD, Zhang Y, et al. Translational repression mediates activation of nuclear factor kappa B by phosphorylated translation initiation factor 2. Mol Cell Biol 2004;24:10161-10168 (Pubitemid 39507856)
23. Urano F, Wang X, Bertolotti A, et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000;287:664-666 (Pubitemid 30070916)
24. Zhang K, Kaufman RJ. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008;454:455-462
25. Liu G, Sun Y, Li Z, et al. Apoptosis induced by endoplasmic reticulum stress involved in diabetic kidney disease. Biochem Biophys Res Commun 2008;370:651-656
26. Kern TS, Barber AJ. Retinal ganglion cells in diabetes. J Physiol 2008;586:4401-4408
27. Shimazawa M, Inokuchi Y, Ito Y, et al. Involvement of ER stress in retinal cell death. Mol Vis 2007;13:578-587 (Pubitemid 46561917)
28. Jing G, Wang JJ, Zhang SX. ER stress and apoptosis: a new mechanism for retinal cell death. Exp Diabetes Res 2012;2012:589589
29. Amin RH, Frank RN, Kennedy A, Eliott D, Puklin JE, Abrams GW. Vascular endothelial growth factor is present in glial cells of the retina and optic nerve of human subjects with nonproliferative diabetic retinopathy. Invest Ophthalmol Vis Sci 1997;38:36-47 (Pubitemid 27051522)
30. Roybal CN, Yang S, Sun CW, et al. Homocysteine increases the expression of vascular endothelial growth factor by a mechanism involving endoplasmic reticulum stress and transcription factor ATF4. J Biol Chem 2004;279:14844-14852 (Pubitemid 38618874)
31. Roybal CN, Hunsaker LA, Barbash O, Vander Jagt DL, Abcouwer SF. The oxidative stressor arsenite activates vascular endothelial growth factor mRNA transcription by an ATF4-dependent mechanism. J Biol Chem 2005;280:20331-20339 (Pubitemid 40776731)
32. Malabanan KP, Kanellakis P, Bobik A, Khachigian LM. Activation transcription factor-4 induced by fibroblast growth factor-2 regulates vascular endothelial growth factor-A transcription in vascular smooth muscle cells and mediates intimal thickening in rat arteries following balloon injury. Circ Res 2008;103:378-387
33. Karin M, Gallagher E. From JNK to pay dirt: Jun kinases, their biochemistry, physiology and clinical importance. IUBMB Life 2005;57:283-295 (Pubitemid 40904256)
34. Srivastava RK, Sollott SJ, Khan L, Hansford R, Lakatta EG, Longo DL. Bcl-2 and Bcl-X(L) block thapsigargin-induced nitric oxide generation, c-Jun NH (2)-terminal kinase activity, and apoptosis. Mol Cell Biol 1999;19:5659-5674 (Pubitemid 29339923)
35. Vallerie SN, Furuhashi M, Fucho R, Hotamisligil GS. A predominant role for parenchymal c-Jun amino terminal kinase (JNK) in the regulation of systemic insulin sensitivity. PLoS ONE 2008;3:e3151
36. Zhang N, Khachigian LM. Injury-induced platelet-derived growth factor receptor-alpha expression mediated by interleukin-1beta (IL-1beta) release and cooperative transactivation by NF-kappaB and ATF-4: IL-1beta facilitates HDAC-1/2 dissociation from promoter [retracted in: J Biol Chem 2010;285:21902]. J Biol Chem 2009;284:27933-27943
37. Berg S, Serabe B, Aleksic A, et al. Pharmacokinetics and cerebrospinal fluid penetration of phenylacetate and phenylbutyrate in the nonhuman primate. Cancer Chemother Pharmacol 2001;47:385-390 (Pubitemid 32397613)