Endoplasmic reticulum stress response and inflammatory cytokines in type 2 diabetic nephropathy: Role of indoleamine 2,3-dioxygenase and programmed death-1

Experimental and Molecular Pathology

Volumn 94, Issue 2, 2013, Pages 343-351

  Baban, Babak ^a   Liu, Jun Yao ^a   Mozaffari, Mahmood S ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Cell death; Cytokines; Diabetes; ER stress response; Indoleamine 2,3 dioxygenase; Kidney; Programmed death 1

Indexed keywords

CASPASE 3; CYTOKINE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 17; INTERLEUKIN 23; LIPOCORTIN 5; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN JC1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD ANALYSIS; CELL COUNT; CELL DAMAGE; CELL DEATH; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIABETIC NEPHROPATHY; DISEASE ACTIVITY; DISEASE EXACERBATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; GLOMERULUS; KIDNEY CELL; KIDNEY INJURY; KIDNEY PARENCHYMA; MALE; MEMBRANE DAMAGE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NECROSIS; NEPHRITIS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN FUNCTION; TISSUE INJURY; UPREGULATION;

ACUTE KIDNEY INJURY; ANIMALS; ANNEXIN A5; APOPTOSIS; CASPASE 3; DIABETES MELLITUS, TYPE 2; DIABETIC NEPHROPATHIES; DOWN-REGULATION; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTERLEUKIN-17; INTERLEUKIN-23; KIDNEY GLOMERULUS; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; PROGRAMMED CELL DEATH 1 RECEPTOR; TRANSCRIPTION FACTOR CHOP;

EID: 84874476648     PISSN: 00144800     EISSN: 10960945     Source Type: Journal    
DOI: 10.1016/j.yexmp.2012.11.004     Document Type: Article

References (50)

1. Baban B., Chandler P.R., Sharma M.D., Pihkala J., Koni P.A., Munn D.H., Mellor A.L. IDO activates regulatory T cells and blocks their conversion into Th17-like T cells. Journal of Immunology (Baltimore, Md.: 1950) 2009, 183:2475-2483.
2. Baban B., Chandler P.R., Johnson B.A., Huang L., Li M., Sharpe M.L., Francisco L.M., Sharpe A.H., Blazar B.R., Munn D.H., Mellor A.L. Physiologic control of IDO competence in splenic dendritic cells. Journal of Immunology (Baltimore, Md.: 1950) 2011, 187:2329-2335.
3. Baban B., Liu J.Y., Mozaffari M.S. Pressure overload regulates expression of cytokines, γH2AX, and growth arrest- and DNA-damage inducible protein 153 via Glycogen synthase kinase-3β in ischemic-reperfused hearts. Hypertension 2012, (Oct 29 [Epub ahead of print]).
4. Baban B., Liu J.Y., Mozaffari M.S. Aryl hydrocarbon receptor agonist, leflunomide, protects the ischemic-reperfused kidney: role of Tregs and stem cells. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 2012, 303(11):R1136-R1146.
5. Cheng W.P., Hung H.F., Wang B.W., Shyu K.G. The molecular regulation of GADD153 in apoptosis of cultured vascular smooth muscle cells by cyclic mechanical stretch. Cardiovascular Research 2008, 77:551-559.
6. Cossarizza A., Salvioli S. Flow cytometric analysis of mitochondrial membrane potential using JC-1. Current Protocols in Cytometry 2001, 9.14.1-9.14.7. (May).
7. Cua D.J., Tato C.M. Innate IL-17-producing cells: the sentinels of the immune system. Nature Reviews. Immunology 2010, 10:479-489.
8. Cunard R., Sharma K. The endoplasmic reticulum stress response and diabetic kidney disease. American Journal of Physiology. Renal Physiology 2011, 300:F1054-F1061.
9. D'Acquisto F., Maione F., Pederzoli-Ribeil M. From IL-15 to IL-33: the never-ending list of new players in inflammation. Is it time to forget the humble aspirin and move ahead?. Biochemical Pharmacology 2010, 79:525-534.
10. Devalaraja-Narashimha K., Diener A.M., Padanilam B.J. Cyclophilin D gene ablation protects mice from ischemic renal injury. American Journal of Physiology. Renal Physiology 2009, 297:F749-F759.
11. Elmarakby A.A., Abdelsayed R., Liu J., Mozaffari M.S. Inflammatory cytokines as predictive markers for diabetic nephropathy. The EPMA Journal 2010, 1:117-129.
12. Francisco L.M., Sage P.T., Sharpe A.H. The PD-1 pathway in tolerance and autoimmunity. Immunological Reviews 2010, 236:219-242.
13. Ghebeh H., Mohammed S., Al-Omair A., Qattan A., Lehe C., Al-Qudaihi G., Elkum N., Alshabanah M., Bin Amer S., Tulbah A., Ajarim D., Al-Tweigeri T., Dermime S. The B7-H1 (PD-L1) T lymphocyte-inhibitory molecule is expressed in breast cancer patients with infiltrating ductal carcinoma: correlation with important high-risk prognostic factors. Neoplasia 2006, 8:190-198.
14. Giacco F., Brownlee M. Oxidative stress and diabetic complications. Circulation Research 2010, 107:1058-1070.
15. Grace B.S., Clayton P., McDonald S.P. Increases in renal replacement therapy in Australia and New Zealand: understanding trends in diabetic nephropathy. Nephrology (Carlton) 2012, 17:76-84.
16. Harding H.P., Zeng H., Zhang Y., Jungries R., Chung P., Plesken H., Sabatini D.D., Ron D. Diabetes mellitus and exocrine pancreatic dysfunction in perk -/- mice reveals a role for translational control in secretory cell survival. Molecular Cell 2001, 7:1153-1163.
17. Hasnain S.Z., Lourie R., Das I., Chen A.C., McGuckin M.A. The interplay between endoplasmic reticulum stress and inflammation. Immunology and Cell Biology 2012, 90:260-270.
18. Higa A., Chevet E. Redox signaling loops in the unfolded protein response. Cellular Signalling 2012, 24:1548-1555.
19. Huang L., Baban B., Johnson B.A., Mellor A.L. Dendritic cells, indoleamine 2,3 dioxygenase and acquired immune privilege. International Reviews of Immunology 2010, 9:133-155.
20. Johnson G.G., White M.C., Grimaldi M. Stressed to death: targeting endoplasmic reticulum stress response induced apoptosis in gliomas. Current Pharmaceutical Design 2011, 17:284-292.
21. Koga N., Suzuki J., Kosuge H., Haraguchi G., Onai Y., Futamatsu H., Maejima Y., Gotoh R., Saiki H., Tsushima F., Azuma M., Isobe M. Blockade of the interaction between PD-1 and PD-L1 accelerates graft arterial disease in cardiac allografts. Arteriosclerosis, Thrombosis, and Vascular Biology 2004, 24:2057-2062.
22. Lindenmeyer M.T., Rastaldi M.P., Ikehata M., Neusser M.A., Kretzler M., Cohen C.D., Schlöndorff D. Proteinuria and hyperglycemia induce endoplasmic reticulum stress. Journal of the American Society of Nephrology 2008, 19:2225-2236.
23. Liu G., Sun Y., Li Z., Song T., Wang H., Zhang Y., Ge Z. Apoptosis induced by endoplasmic reticulum stress involved in diabetic kidney disease. Biochemical and Biophysical Research Communications 2008, 370:651-656.
24. Liu C.B., Chen L.H., Cheng A.C., Chen W.J., Tsai M.L., Liu Y., Ho C.T., Pan M.H. Hexahydro-β-acids induce apoptosis through mitochondrial pathway, GADD153 expression, and caspase activation in human leukemia cells. Food and Chemical Toxicology 2011, 49:1033-1042.
25. Maric C., Hall J.E. Obesity, metabolic syndrome and diabetic nephropathy. Contributions to Nephrology 2011, 170:28-35.
26. Mathur A., Hong Y., Kemp B.K., Barrientos A.A., Erusalimsky J.D. Evaluation of fluorescent dyes for the detection of mitochondrial membrane potential changes in cultured cardiomyocytes. Cardiovascular Research 2000, 46:126-138.
27. Mellor A.L., Baban B., Chandler P., Marshall B., Jhaver K., Hansen A., Koni P.A., Iwashima M., Munn D.H. Cutting edge: induced indoleamine 2,3 dioxygenase expression in dendritic cell subsets suppresses T cell clonal expansion. Journal of Immunology (Baltimore, Md.: 1950) 2003, 171:1652-1655.
28. Mondal A.K., Das S.K., Varma V., Nolen G.T., McGehee R.E., Elbein S.C., Wei J.Y., Ranganathan G. Effect of endoplasmic reticulum stress on inflammation and adiponectin regulation in human adipocytes. Metabolic Syndrome and Related Disorders 2012, 10:297-306.
29. Mozaffari M.S., Baban B., Abdelsayed R., Liu J.Y., Wimborne H., Rodriguez N., Abebe W. Renal and glycemic effects of high-dose chromium picolinate in db/db mice: assessment of DNA damage. The Journal of Nutritional Biochemistry 2012, 23:977-985.
30. Mozaffari M.S., Abdelsayed R., Liu J.Y., Zakhary I., Baban B. Renal distal tubule proliferation and increased aquaporin 2 level but decreased urine osmolality in db/db mouse: treatment with chromium picolinate. Experimental and Molecular Pathology 2012, 92:54-58.
31. Munn D.H., Sharma M.D., Hou D., Baban B., Lee J.R., Antonia S.J., Messina J.L., Chandler P., Koni P.A., Mellor A.L. Expression of indoleamine 2,3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. The Journal of Clinical Investigation 2004, 114:280-290.
32. Nakanishi J., Wada Y., Matsumoto K., Azuma M., Kikuchi K., Ueda S. Overexpression of B7-H1 (PD-L1) significantly associates with tumor grade and postoperative prognosis in human urothelial cancers. Cancer Immunology, Immunotherapy 2007, 56:1173-1182.
33. Nishimura H., Okazaki T., Tanaka Y., Nakatani K., Hara M., Matsumori A., Sasayama S., Mizoguchi A., Hiai H., Minato N., Honjo T. Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 2001, 291:319-322.
34. Ozcan U., Cao Q., Yilmaz E., Lee A.H., Iwakoshi N.N., Ozdelen E., Tuncman G., Görgün C., Glimcher L.H., Hotamisligil G.S. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004, 306:457-461.
35. Ozcan U., Yilmaz E., Ozcan L., Furuhashi M., Vaillancourt E., Smith R.O., Görgün C.Z., Hotamisligil G.S. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006, 313:1137-1140.
36. Ravishankar B., Liu H., Shinde R., Chandler P., Baban B., Tanaka M., Munn D.H., Mellor A.L., Karlsson M.C., McGaha T.L. Tolerance to apoptotic cells is regulated by indoleamine 2,3-dioxygenase. Proceedings of the National Academy of Sciences 2012, 109:3909-3914.
37. Schaffer S.W., Jong C.J., Mozaffari M. Role of oxidative stress in diabetes-mediated vascular dysfunction: Unifying hypothesis of diabetes revisited. Vascular Pharmacology 2012, 57(5-6). 139-139.
38. Scheuner D., Song B., McEwen E., Liu C., Laybutt R., Gillespie P., Saunders T., Bonner-Weir S., Kaufman R.J. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Molecular Cell 2001, 7:1165-1176.
39. Song B., Scheuner D., Ron D., Pennathur S., Kaufman R.J. Chop deletion reduces oxidative stress, improves beta cell function, and promotes cell survival in multiple mouse models of diabetes. The Journal of Clinical Investigation 2008, 118:3378-3389.
40. Sun L., Xiao L., Nie J., Liu F.Y., Ling G.H., Zhu X.J., Tang W.B., Chen W.C., Xia Y.C., Zhan M., Ma M.M., Peng Y.M., Liu H., Liu Y.H., Kanwar Y.S. p66Shc mediates high-glucose and angiotensin II-induced oxidative stress renal tubular injury via mitochondrial-dependent apoptotic pathway. American Journal of Physiology. Renal Physiology 2010, 299:F1014-F1025.
41. Sylvester S.L., ap Rhys C.M., Luethy-Martindale J.D., Holbrook N.J. Induction of GADD153, a CCAAT/enhancer-binding protein (C/EBP)-related gene, during the acute phase response in rats. Evidence for the involvement of C/EBPs in regulating its expression. The Journal of Biological Chemistry 1994, 269:20119-21025.
42. Szabo C. Role of nitrosative stress in the pathogenesis of diabetic vascular dysfunction. British Journal of Pharmacology 2009, 156:713-727.
43. Tarrio M.L., Grabie N., Bu D., Sharpe A.H., Lichtman A.H. PD-1 protects against inflammation and myocyte damage in T cell-mediated myocarditis. Journal of Immunology (Baltimore, Md.: 1950) 2012, 188:4876-4884.
44. Tesch G.H., Lim A.K. Recent insights into diabetic renal injury from the db/db mouse model of type 2 diabetic nephropathy. American Journal of Physiology. Renal Physiology 2011, 300:F301-F310.
45. Tipton A.J., Baban B., Sullivan J.C. Female spontaneously hypertensive rats have greater renal anti-inflammatory T lymphocyte infiltration than males. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 2012, 303(4):R359-R367.
46. Verfaillie T., Rubio N., Garg A.D., Bultynck G., Rizzuto R., Decuypere J.P., Piette J., Linehan C., Gupta S., Samali A., Agostinis P. PERK is required at the ER-mitochondrial contact sites to convey apoptosis after ROS-based ER stress. Cell Death and Differentiation 2012, 19(11):1880-1891.
47. Vermes I., Haanen C., Steffens-Nakken H., Reutelingsperger C. A novel assay for apoptosis. Flow7 cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labeled Annexin V. Journal of Immunological Methods 1995, 184:39-51.
48. Wang L., Han R., Hancock W.W. Programmed cell death 1 (PD-1) and its ligand PD-L1 are required for allograft tolerance. European Journal of Immunology 2007, 37:2983-2990.
49. Wang W., Carper K., Malone F., Latchman Y., Perkins J., Fu Y., Reyes J., Li W. PD-L1/PD-1 signal deficiency promotes allogeneic immune responses and accelerates heart allograft rejection. Transplantation 2008, 86:836-844.
50. Wu J., Zhang R., Torreggiani M., Ting A., Xiong H., Striker G.E., Vlassara H., Zheng F. Induction of diabetes in aged C57B6 mice results in severe nephropathy: an association with oxidative stress, endoplasmic reticulum stress, and inflammation. The American Journal of Pathology 2010, 176:2163-2276.