Targeted deletion of p53 in the proximal tubule prevents ischemic renal injury

Journal of the American Society of Nephrology

Volumn 25, Issue 12, 2014, Pages 2707-2716

  Ying, Yuan ^a   Kim, Jinu ^a   Westphal, Sherry N ^a   Long, Kelly E ^a   Padanilam, Babu J ^a,b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b Jeju National University School of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CREATININE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PIFITHRIN ALPHA; PROTEIN BAX; PROTEIN BID; PROTEIN P53; SIVA PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; ACTIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; TP53 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL INFILTRATION; CONTROLLED STUDY; CREATININE BLOOD LEVEL; G2 PHASE CELL CYCLE CHECKPOINT; GENE DELETION; GENE EXPRESSION; KIDNEY FIBROSIS; KIDNEY FUNCTION; KIDNEY INJURY; KIDNEY ISCHEMIA; KIDNEY PROXIMAL TUBULE; MACROPHAGE; MOUSE; NEPHRITIS; NEUTROPHIL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; UREA NITROGEN BLOOD LEVEL; ANIMAL; BLOOD; CELL CYCLE; FLUORESCENCE MICROSCOPY; GENETICS; HUMAN; INFLAMMATION; KIDNEY; KNOCKOUT MOUSE; MALE; METABOLISM; NECROSIS; PATHOLOGY; REPERFUSION INJURY; TUMOR SUPPRESSOR GENE;

ACTINS; ANIMALS; APOPTOSIS; BLOOD UREA NITROGEN; CELL CYCLE; CREATININE; GENE DELETION; GENES, P53; HUMANS; INFLAMMATION; KIDNEY; KIDNEY TUBULES, PROXIMAL; MALE; MICE; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; NECROSIS; NEUTROPHILS; OXIDATIVE STRESS; POLY(ADP-RIBOSE) POLYMERASES; REPERFUSION INJURY; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84922873973     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2013121270     Document Type: Article

References (48)

1. Bonventre JV, Weinberg JM: Recent advances in the pathophysiology of ischemic acute renal failure. J Am Soc Nephrol 14: 2199-2210, 2003
2. Liaño F, Pascual J; Madrid Acute Renal Failure Study Group: Epidemiology of acute renal failure: A prospective, multicenter, community-based study. Kidney Int 50: 811-818, 1996
3. Liaño F, Pascual J: Outcomes in acute renal failure. Semin Nephrol 18: 541-550, 1998
4. Mason J, Torhorst J, Welsch J: Role of the medullary perfusion defect in the pathogenesis of ischemic renal failure. Kidney Int 26: 283-293, 1984
5. Venkatachalam MA, Bernard DB, Donohoe JF, Levinsky NG: Ischemic damage and repair in the rat proximal tubule: Differences among the S1, S2, and S3 segments. Kidney Int 14: 31-49, 1978
6. Yamamoto K, Wilson DR, Baumal R: Outer medullary circulatory defect in ischemic acute renal failure. Am J Pathol 116: 253-261, 1984
7. Devalaraja-Narashimha K, Padanilam BJ: PARP-1 inhibits glycolysis in ischemic kidneys. J Am Soc Nephrol 20: 95-103, 2009
8. Kelly KJ, Plotkin Z, Dagher PC: Guanosine supplementation reduces apoptosis and protects renal function in the setting of ischemic injury. J Clin Invest 108: 1291-1298, 2001
9. Kelly KJ, Plotkin Z, Vulgamott SL, Dagher PC: P53 mediates the apoptotic response to GTP depletion after renal ischemia-reperfusion: Protective role of a p53 inhibitor. J Am Soc Nephrol 14: 128-138, 2003
10. Howard C, Tao S, Yang HC, Fogo AB, Woodgett JR, Harris RC, Rao R: Specific deletion of glycogen synthase kinase-3β in the renal proximal tubule protects against acute nephrotoxic injury in mice. Kidney Int 82: 1000-1009, 2012
11. Chien CT, Chang TC, Tsai CY, Shyue SK, Lai MK: Adenovirus-mediated bcl-2 gene transfer inhibits renal ischemia/reperfusion induced tubular oxidative stress and apoptosis. Am J Transplant 5: 1194-1203, 2005
12. Youle RJ, Strasser A: The BCL-2 protein family: Opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9: 47-59, 2008
13. Faubel S, Ljubanovic D, Reznikov L, Somerset H, Dinarello CA, Edelstein CL: Caspase-1-deficient mice are protected against cisplatin-induced apoptosis and acute tubular necrosis. Kidney Int 66: 2202-2213, 2004
14. Kunduzova OR, Escourrou G, Seguelas MH, Delagrange P, De La Farge F, Cambon C, Parini A: Prevention of apoptotic and necrotic cell death, caspase-3 activation, and renal dysfunction by melatonin after ischemia/reperfusion. FASEB J 17: 872-874, 2003
15. Vousden KH, Lane DP: p53 in health and disease. Nat Rev Mol Cell Biol 8: 275-283, 2007
16. Kruse JP, Gu W: Modes of p53 regulation. Cell 137: 609-622, 2009
17. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, Green DR: Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303: 1010-1014, 2004
18. Zhou L, Fu P, Huang XR, Liu F, Lai KN, Lan HY: Activation of p53 promotes renal injury in acute aristolochic acid nephropathy. J Am Soc Nephrol 21: 31-41, 2010
19. Wei Q, Dong G, Yang T, Megyesi J, Price PM, Dong Z: Activation and involvement of p53 in cisplatin-induced nephrotoxicity. Am J Physiol Renal Physiol 293: F1282-F1291, 2007
20. Molitoris BA, Dagher PC, Sandoval RM, Campos SB, Ashush H, Fridman E, Brafman A, Faerman A, Atkinson SJ, Thompson JD, Kalinski H, Skaliter R, Erlich S, Feinstein E: siRNA targeted to p53 attenuates ischemic and cisplatin-induced acute kidney injury. J Am Soc Nephrol 20: 1754-1764, 2009
21. Dagher PC, Mai EM, Hato T, Lee SY, Anderson MD, Karozos SC, Mang HE, Knipe NL, Plotkin Z, Sutton TA: The p53 inhibitor pifithrin-α can stimulate fibrosis in a rat model of ischemic acute kidney injury. Am J Physiol Renal Physiol 302: F284-F291, 2012
22. Sutton TA, Hato T, Mai E, Yoshimoto M, Kuehl S, Anderson M, Mang H, Plotkin Z, Chan RJ, Dagher PC: p53 is renoprotective after ischemic kidney injury by reducing inflammation. J Am Soc Nephrol 24: 113-124, 2013
23. Scrittori L, Hans F, Angelov D, Charra M, Prigent C, Dimitrov S: pEg2 aurora-A kinase, histone H3 phosphorylation, and chromosome assembly in Xenopus egg extract. J Biol Chem 276: 30002-30010, 2001
24. Westendorf JM, Rao PN, Gerace L: Cloning of cDNAs for M-phase phosphoproteins recognized by the MPM2 monoclonal antibody and determination of the phosphorylated epitope. Proc Natl Acad Sci U S A 91: 714-718, 1994
25. Kuang J, Ashorn CL, Gonzalez-Kuyvenhoven M, Penkala JE: cdc25 is one of the MPM-2 antigens involved in the activation of maturation-promoting factor. Mol Biol Cell 5: 135-145, 1994
26. Yang L, Besschetnova TY, Brooks CR, Shah JV, Bonventre JV: Epithelial cell cycle arrest in G2/M mediates kidney fibrosis after injury. Nat Med 16: 535-543, 2010
27. Wei Q, Dong G, Chen JK, Ramesh G, Dong Z: Bax and Bak have critical roles in ischemic acute kidney injury in global and proximal tubule-specific knockout mouse models. Kidney Int 84: 138-148, 2013
28. Wei Q, Yin XM, Wang MH, Dong Z: Bid deficiency ameliorates ischemic renal failure and delays animal death in C57BL/6 mice. Am J Physiol Renal Physiol 290: F35-F42, 2006
29. Singaravelu K, Padanilam BJ: p53 target Siva regulates apoptosis in ischemic kidneys. Am J Physiol Renal Physiol 300: F1130-F1141, 2011
30. Vaseva AV, Marchenko ND, Ji K, Tsirka SE, Holzmann S, Moll UM: p53 opens the mitochondrial permeability transition pore to trigger necrosis. Cell 149: 1536-1548, 2012
31. Devalaraja-Narashimha K, Diener AM, Padanilam BJ: Cyclophilin D gene ablation protects mice from ischemic renal injury. Am J Physiol Renal Physiol 297: F749-F759, 2009
32. Linkermann A, Bräsen JH, Darding M, Jin MK, Sanz AB, Heller JO, De Zen F, Weinlich R, Ortiz A, Walczak H, Weinberg JM, Green DR, Kunzendorf U, Krautwald S: Two independent pathways of regulated necrosis mediate ischemia-reperfusion injury. Proc Natl Acad Sci U S A 110: 12024-12029, 2013
33. Ha HC, Snyder SH: Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc Natl Acad Sci U S A 96: 13978-13982, 1999
34. Moubarak RS, Yuste VJ, Artus C, Bouharrour A, Greer PA, Menissier-de Murcia J, Susin SA: Sequential activation of poly(ADP-ribose) polymerase 1, calpains, and Bax is essential in apoptosis-inducing factor-mediated programmed necrosis. Mol Cell Biol 27: 4844-4862, 2007
35. Martin DR, Lewington AJ, Hammerman MR, Padanilam BJ: Inhibition of poly(ADP-ribose) polymerase attenuates ischemic renal injury in rats. Am J Physiol Regul Integr Comp Physiol 279: R1834-R1840, 2000
36. Kim J, Long KE, Tang K, Padanilam BJ: Poly(ADP-ribose) polymerase 1 activation is required for cisplatin nephrotoxicity. Kidney Int 82: 193-203, 2012
37. Whelan RS, Konstantinidis K, Wei AC, Chen Y, Reyna DE, Jha S, Yang Y, Calvert JW, Lindsten T, Thompson CB, Crow MT, Gavathiotis E, Dorn GW 2nd, O'Rourke B, Kitsis RN: Bax regulates primary necrosis through mitochondrial dynamics. Proc Natl Acad Sci U S A 109: 6566-6571, 2012
38. Karch J, Kwong JQ, Burr AR, Sargent MA, Elrod JW, Peixoto PM, Martinez-Caballero S, Osinska H, Cheng EH, Robbins J, Kinnally KW, Molkentin JD: Bax and Bak function as the outermembrane component of the mitochondrial permeability pore in regulating necrotic cell death in mice. Elife 2: e00772, 2013
39. Awad AS, Ye H, Huang L, Li L, Foss FW Jr., Macdonald TL, Lynch KR, Okusa MD: Selective sphingosine 1-phosphate 1 receptor activation reduces ischemia-reperfusion injury in mouse kidney. Am J Physiol Renal Physiol 290: F1516-F1524, 2006
40. Awad AS, Rouse M, Huang L, Vergis AL, Reutershan J, Cathro HP, Linden J, Okusa MD: Compartmentalization of neutrophils in the kidney and lung following acute ischemic kidney injury. Kidney Int 75: 689-698, 2009
41. Kelly KJ, Williams WW Jr., Colvin RB, Meehan SM, Springer TA, Gutierrez-Ramos JC, Bonventre JV: Intercellular adhesion molecule-1-deficient mice are protected against ischemic renal injury. J Clin Invest 97: 1056-1063, 1996
42. Solez K, Morel-Maroger L, Sraer JD: The morphology of "acute tubular necrosis" in man: Analysis of 57 renal biopsies and a comparison with the glycerol model. Medicine (Baltimore) 58: 362-376, 1979
43. Rankin EB, Tomaszewski JE, Haase VH: Renal cyst development inmice with conditional inactivation of the von Hippel-Lindau tumor suppressor. Cancer Res 66: 2576-2583, 2006
44. Zheng J, Devalaraja-Narashimha K, Singaravelu K, Padanilam BJ: Poly(ADP-ribose) polymerase-1 gene ablation protects mice from ischemic renal injury. Am J Physiol Renal Physiol 288: F387-F398, 2005
45. Kim J, Padanilam BJ: Loss of poly(ADP-ribose) polymerase 1 attenuates renal fibrosis and inflammation during unilateral ureteral obstruction. Am J Physiol Renal Physiol 301: F450-F459, 2011
46. Hara-Chikuma M, Verkman AS: Aquaporin-1 facilitates epithelial cell migration in kidney proximal tubule. J Am Soc Nephrol 17: 39-45, 2006
47. Polosukhina D, Singaravelu K, Padanilam BJ: Activation of protein kinase C isozymes protects LLCPK1 cells from H2O2 induced necrotic cell death. Am J Nephrol 23: 380-389, 2003
48. Montero J, Dutta C, van Bodegom D, Weinstock D, Letai A: p53 regulates a non-apoptotic death induced by ROS. Cell Death Differ 20: 1465-1474, 2013