Mice with an absent stress response are protected against ischemic renal injury

Kidney International

Volumn 86, Issue 3, 2014, Pages 515-524

  Sreedharan, Rajasree ^a   Chen, Shaoying ^a   Miller, Melody ^a   Haribhai, Dipica ^a   Williams, Calvin B ^a   Van Why, Scott K ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

acute kidney injury; inflammation; renal ischemia reperfusion; transcription factors

Indexed keywords

CREATININE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; HEAT SHOCK TRANSCRIPTION FACTOR 1; MONOCLONAL ANTIBODY; PC61 ANTIBODY; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; HSF1 PROTEIN, MOUSE; HSPB1 PROTEIN, MOUSE; INTERLEUKIN 2 RECEPTOR ALPHA; PC61 MONOCLONAL ANTIBODY; TRANSCRIPTION FACTOR; TUMOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CREATININE BLOOD LEVEL; FEMALE; FLOW CYTOMETRY; HISTOLOGY; IN VIVO STUDY; KIDNEY FUNCTION; KIDNEY INJURY; KIDNEY ISCHEMIA; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; LYMPHOCYTIC INFILTRATION; MALE; MONONUCLEAR CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; REGULATORY T LYMPHOCYTE; RENAL PROTECTION; STRESS; WILD TYPE; ACUTE KIDNEY FAILURE; ANIMAL; BLOOD; DRUG EFFECTS; GENETICS; IMMUNOLOGY; KIDNEY TUBULE; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGICAL STRESS; REPERFUSION INJURY;

ACUTE KIDNEY INJURY; ANIMALS; ANTIBODIES, MONOCLONAL; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CREATININE; DNA-BINDING PROTEINS; FORKHEAD TRANSCRIPTION FACTORS; HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; KIDNEY TUBULES; MALE; MICE; MICE, KNOCKOUT; NEOPLASM PROTEINS; REPERFUSION INJURY; STRESS, PHYSIOLOGICAL; T-LYMPHOCYTES, REGULATORY; TRANSCRIPTION FACTORS;

EID: 84907598808     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2014.73     Document Type: Article

References (58)

1. Basile DP, Donohoe D, Roethe K et al. Renal ischemic injury results in permanent damage to peritubular capillaries and influences long-term function. Am J Physiol Renal Physiol 2001; 281: F887-F899.
2. Basile DP. Rarefaction of peritubular capillaries following ischemic acute renal failure: a potential factor predisposing to progressive nephropathy. Curr Opin Nephrol Hypertens 2004; 13: 1-7.
3. Sutton TA, Fisher CJ, Molitoris BA. Microvascular endothelial injury and dysfunction during ischemic acute renal failure. Kidney Int 2002; 62: 1539-1549.
4. Sutton TA, Mang HE, Campos SB et al. Injury of the renal microvascular endothelium alters barrier function after ischemia. Am J Physiol Renal Physiol 2003; 285: F191-F198.
5. Molitoris BA, Sutton TA. Endothelial injury and dysfunction: role in the extension phase of acute renal failure. Kidney Int 2004; 66: 496-499.
6. Devarajan P. Update on mechanisms of ischemic acute kidney injury. J Am Soc Nephrol 2006; 17: 1503-1520.
7. Avner ED, Harmon D, Niaudet WE, Yoshikawa P (eds Pediatric Nephrology. Springer 2009.
8. Jang HR, Rabb H. The innate immune response in ischemic acute kidney injury. Clin Immunol 2009; 130: 41-50.
9. Li L, Huang L, Sung SS et al. NKT cell activation mediates neutrophil IFN-gamma production and renal ischemia-reperfusion injury. J Immunol 2007; 178: 5899-5911.
10. Kinsey GR, Huang L, Vergis AL et al. Regulatory T cells contribute to the protective effect of ischemic preconditioning in the kidney. Kidney Int 77: 771-780.
11. Gandolfo MT, Jang HR, Bagnasco SM et al. Foxp3 + regulatory T cells participate in repair of ischemic acute kidney injury. Kidney Int 2009; 76: 717-729.
12. Yokota N, Daniels F, Crosson J et al. Protective effect of T cell depletion in murine renal ischemia-reperfusion injury. Transplantation 2002; 74: 759-763.
13. Burne-Taney MJ, Yokota-Ikeda N, Rabb H. Effects of combined T- and B-cell deficiency on murine ischemia reperfusion injury. Am J Transplant 2005; 5: 1186-1193.
14. Burne-Taney MJ, Ascon DB, Daniels F et al. B cell deficiency confers protection from renal ischemia reperfusion injury. J Immunol 2003; 171: 3210-3215.
15. Riordan M, Sreedharan R, Wang S et al. HSP70 binding modulates detachment of Na-K-ATPase following energy deprivation in renal epithelial cells. Am J Physiol Renal Physiol 2005; 288: F1236-F1242.
16. Van Why SK, Mann AS, Ardito T et al. Hsp27 associates with actin and limits injury in energy depleted renal epithelia. J Am Soc Nephrol 2003; 14: 98-106.
17. Mosser DD, Caron AW, Bourget L et al. The chaperone function of hsp70 is required for protection against stress-induced apoptosis. Mol Cell Biol 2000; 20: 7146-7159.
18. Van Why SK, Mann AS, Thulin G et al. Activation of heat-shock transcription factor by graded reductions in renal ATP, in vivo, in the rat. J Clin Invest 1994; 94: 1518-1523.
19. Eickelberg O, Seebach F, Riordan M et al. Functional activation of heat shock factor and hypoxia-inducible factor in the kidney. J Am Soc Nephrol 2002; 13: 2094-2101.
20. Kelly KJ, Baird NR, Greene AL. Induction of stress response proteins and experimental renal ischemia/reperfusion. Kidney Int 2001; 59: 1798-1802.
21. Aufricht C, Ardito T, Thulin G et al. Heat-shock protein 25 induction and redistribution during actin reorganization after renal ischemia. Am J Physiol 1998; 274(Pt 2): F215-F222.
22. Wang Y, Knowlton AA, Christensen TG et al. Prior heat stress inhibits apoptosis in adenosine triphosphate-depleted renal tubular cells. Kidney Int 1999; 55: 2224-2235.
23. Wang YH, Knowlton AA, Li FH et al. Hsp72 expression enhances survival in adenosine triphosphate-depleted renal epithelial cells. Cell Stress Chaperones 2002; 7: 137-145.
24. Wang YH, Borkan SC. Prior heat stress enhances survival of renal epithelial cells after ATP depletion. Am J Physiol 1996; 270(Pt 2): F1057-F1065.
25. Emami A, Schwartz JH, Borkan SC. Transient ischemia or heat stress induces a cytoprotectant protein in rat kidney. Am J Physiol 1991; 260(Pt 2): F479-F485.
26. Schober A, Muller E, Thurau K et al. The response of heat shock proteins 25 and 72 to ischaemia in different kidney zones. Pflugers Arch 1997; 434: 292-299.
27. Sreedharan R, Riordan M, Wang S et al. Reduced tolerance of immature renal tubules to anoxia by HSF-1 decoy. Am J Physiol Renal Physiol 2005; 288: F322-F326.
28. Fiorenza MT, Farkas T, Dissing M et al. Complex expression of murine heat shock transcription factors. Nucleic Acids Res 1995; 23: 467-474.
29. Aufricht C, Bidmon B, Ruffingshofer D et al. Ischemic conditioning prevents Na,K-ATPase dissociation from the cytoskeletal cellular fraction after repeat renal ischemia in rats. Pediatr Res 2002; 51: 722-727.
30. Ling H, Edelstein C, Gengaro P et al. Attenuation of renal ischemia-reperfusion injury in inducible nitric oxide synthase knockout mice. Am J Physiol 1999; 277(Pt 2): F383-F390.
31. Park KM, Kramers C, Vayssier-Taussat M et al. Prevention of kidney ischemia/reperfusion-induced functional injury, MAPK and MAPK kinase activation, and inflammation by remote transient ureteral obstruction. J Biol Chem 2002; 277: 2040-2049.
32. Xiao X, Zuo X, Davis AA et al. HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. EMBO J 1999; 18: 5943-5952.
33. McMillan DR, Xiao X, Shao L et al. Targeted disruption of heat shock transcription factor 1 abolishes thermotolerance and protection against heat-inducible apoptosis. J Biol Chem 1998; 273: 7523-7528.
34. Yan LJ, Christians ES, Liu L et al. Mouse heat shock transcription factor 1 deficiency alters cardiac redox homeostasis and increases mitochondrial oxidative damage. EMBO J 2002; 21: 5164-5172.
35. Rupik W, Jasik K, Bembenek J et al. The expression patterns of heat shock genes and proteins and their role during vertebrate's development. Comp Biochem Physiol A Mol Integr Physiol 2011; 159: 349-366.
36. Feder ME, Hofmann GE. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 1999; 61: 243-282.
37. Riordan M, Garg V, Thulin G et al. Differential inhibition of HSP72 and HSP25 produces profound impairment of cellular integrity. J Am Soc Nephrol 2004; 15: 1557-1566.
38. Goligorsky MS. Whispers and shouts in the pathogenesis of acute renal ischaemia. Nephrol Dial Transplant 2005; 20: 261-266.
39. Faubel S, Lewis EC, Reznikov L et al. Cisplatin-induced acute renal failure is associated with an increase in the cytokines interleukin (IL)-1beta, IL-18, IL-6, and neutrophil infiltration in the kidney. J Pharmacol Exp Ther 2007; 322: 8-15.
40. Friedewald JJ, Rabb H. Inflammatory cells in ischemic acute renal failure. Kidney Int 2004; 66: 486-491.
41. Ysebaert DK, De Greef KE, De Beuf A et al. T cells as mediators in renal ischemia/reperfusion injury. Kidney Int 2004; 66: 491-496.
42. Rabb H, Daniels F, O'Donnell M et al. Pathophysiological role of T lymphocytes in renal ischemia-reperfusion injury in mice. Am J Physiol Renal Physiol 2000; 279: F525-F531.
43. Jang HR, Ko GJ, Wasowska BA et al. The interaction between ischemia-reperfusion and immune responses in the kidney. J Mol Med (Berl) 2009; 87: 859-864.
44. Kim BS, Lim SW, Li C et al. Ischemia-reperfusion injury activates innate immunity in rat kidneys. Transplantation 2005; 79: 1370-1377.
45. Wolfs TG, Buurman WA, van Schadewijk A et al. In vivo expression of Toll-like receptor 2 and 4 by renal epithelial cells: IFN-gamma and TNF-alpha mediated up-regulation during inflammation. J Immunol 2002; 168: 1286-1293.
46. Asea A. Heat shock proteins and toll-like receptors. Handb Exp Pharmacol 2008; 183: 111-127.
47. Osterloh A, Geisinger F, Piedavent M et al. Heat shock protein 60 (HSP60) stimulates neutrophil effector functions. J Leukoc Biol 2009; 86: 423-434.
48. Tsan MF, Gao B. Heat shock proteins and immune system. J Leukoc Biol 2009; 85: 905-910.
49. Kinsey GR, Sharma R, Huang L et al. Regulatory T cells suppress innate immunity in kidney ischemia-reperfusion injury. J Am Soc Nephrol 2009; 20: 1744-1753.
50. Lai LW, Yong KC, Igarashi S et al. A sphingosine-1-phosphate type 1 receptor agonist inhibits the early T-cell transient following renal ischemia-reperfusion injury. Kidney Int 2007; 71: 1223-1231.
51. Singh IS, Gupta A, Nagarsekar A et al. Heat shock co-activates interleukin-8 transcription. Am J Respir Cell Mol Biol 2008; 39: 235-242.
52. Inouye S, Izu H, Takaki E et al. Impaired IgG production in mice deficient for heat shock transcription factor 1. J Biol Chem 2004; 279: 38701-38709.
53. Chen SW, Kim M, Song JH et al. Mice that overexpress human heat shock protein 27 have increased renal injury following ischemia reperfusion. Kidney Int 2009; 75: 499-510.
54. Kim M, Park SW, Chen SW et al. Selective renal overexpression of human heat shock protein 27 reduces renal ischemia-reperfusion injury in mice. Am J Physiol Renal Physiol 2010; 299: F347-F358.
55. Haribhai D, Lin W, Relland LM et al. Regulatory T cells dynamically control the primary immune response to foreign antigen. J Immunol 2007; 178: 2961-2972.
56. Basile DP, Donohoe D, Cao X et al. Resistance to ischemic acute renal failure in the Brown Norway rat: a new model to study cytoprotection. Kidney Int 2004; 65: 2201-2211.
57. Kelly KJ, Williams WW Jr., Colvin RB et al. Intercellular adhesion molecule-1-deficient mice are protected against ischemic renal injury. J Clin Invest 1996; 97: 1056-1063.
58. Sreedharan R, Riordan M, Thullin G et al. The maximal cytoprotective function of the heat shock protein 27 is dependent on heat shock protein 70. Biochim Biophys Acta 2011; 1813: 129-135.