Loss of poly(ADP-ribose) polymerase 1 attenuates renal fibrosis and inflammation during unilateral ureteral obstruction

American Journal of Physiology - Renal Physiology

Volumn 301, Issue 2, 2011, Pages

  Kim, Jinu ^a   Padanilam, Babu J ^a,b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Mouse embryonic fibroblast; Necrosis; PARP1 inhibitor; Rat renal interstitial fibroblast; smooth muscle action

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN; FIBRONECTIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR RELA; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL DEATH; CELL INFILTRATION; CONTROLLED STUDY; FIBROBLAST CULTURE; GENE INACTIVATION; HISTOPATHOLOGY; KIDNEY FIBROSIS; KIDNEY PELVIS; KIDNEY TUBULE; KNOCKOUT MOUSE; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; URETER OBSTRUCTION; WILD TYPE;

EID: 79961146098     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00059.2011     Document Type: Article

References (59)

1. Abdelkarim GE, Gertz K, Harms C, Katchanov J, Dirnagl U, Szabo C, Endres M. Protective effects of PJ34, a novel, potent inhibitor of poly(ADP-ribose) polymerase (PARP) in in vitro and in vivo models of stroke. Int J Mol Med 7: 255-260, 2001.
2. Campbell MT, Hile KL, Zhang H, Asanuma H, Vanderbrink BA, Rink RR, Meldrum KK. Toll-like receptor 4: a novel signaling pathway during renal fibrogenesis. J Surg Res 168: e61-e69, 2011.
3. Chevalier RL, Thornhill BA, Wolstenholme JT. Renal cellular response to ureteral obstruction: role of maturation and angiotensin II. Am J Physiol Renal Physiol 277: F41-F47, 1999.
4. Chiarugi A, Moskowitz MA. Poly(ADP-ribose) polymerase-1 activity promotes NF-kappaB-driven transcription and microglial activation: implication for neurodegenerative disorders. J Neurochem 85: 306-317, 2003.
5. Edinger AL, Thompson CB. Death by design: apoptosis, necrosis and autophagy. Curr Opin Cell Biol 16: 663-669, 2004.
6. El Chaar M, Chen J, Seshan SV, Jha S, Richardson I, Ledbetter SR, Vaughan ED Jr, Poppas DP, Felsen D. Effect of combination therapy with enalapril and the TGF-fj antagonist 1D11 in unilateral ureteral obstruction. Am J Physiol Renal Physiol 292: F1291-F1301, 2007.
7. Endres M, Wang ZQ, Namura S, Waeber C, Moskowitz MA. Ischemic brain injury is mediated by the activation of poly(ADP-ribose)polymerase. J Cereb Blood Flow Metab 17: 1143-1151, 1997.
8. Fan CM, Maniatis T. Generation of p50 subunit of NF-kappa B by processing of p105 through an ATP-dependent pathway. Nature 354: 395-398, 1991.
9. Filipovic DM, Meng X, Reeves WB. Inhibition of PARP prevents oxidant-induced necrosis but not apoptosis in LLC-PK1 cells. Am J Physiol Renal Physiol 277: F428-F436, 1999.
10. Guo G, Morrissey J, McCracken R, Tolley T, Klahr S. Role of TNFR1 and TNFR2 receptors in tubulointerstitial fibrosis of obstructive nephropathy. Am J Physiol Renal Physiol 277: F766-F772, 1999.
11. Guo G, Morrissey J, McCracken R, Tolley T, Liapis H, Klahr S. Contributions of angiotensin II and tumor necrosis factor-a to the development of renal fibrosis. Am J Physiol Renal Physiol 280: F777-F785, 2001.
12. Ha HC, Snyder SH. Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc Natl Acad Sci USA 96: 13978-13982, 1999.
13. Hassa PO, Covic M, Hasan S, Imhof R, Hottiger MO. The enzymatic and DNA binding activity of PARP-1 are not required for NF-kappa B coactivator function. J Biol Chem 276: 45588-45597, 2001.
14. Hirsch T, Marchetti P, Susin SA, Dallaporta B, Zamzami N, Marzo I, Geuskens M, Kroemer G. The apoptosis-necrosis paradox. Apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene 15: 1573-1581, 1997.
15. Hu K, Wu C, Mars WM, Liu Y. Tissue-type plasminogen activator promotes murine myofibroblast activation through LDL receptor-related protein 1-mediated integrin signaling. J Clin Invest 117: 3821-3832, 2007.
16. Kauppinen TM, Swanson RA. Poly(ADP-ribose) polymerase-1 promotes microglial activation, proliferation, and matrix metalloproteinase-9-mediated neuron death. J Immunol 174: 2288-2296, 2005.
17. Kim J, Jang HS, Park KM. Reactive oxygen species generated by renal ischemia and reperfusion trigger protection against subsequent renal ischemia and reperfusion injury in mice. Am J Physiol Renal Physiol 298: F158-F166, 2010.
18. Kim J, Jung KJ, Park KM. Reactive oxygen species differently regulate renal tubular epithelial and interstitial cell proliferation after ischemia and reperfusion injury. Am J Physiol Renal Physiol 298: F1118-F1129, 2010.
19. Kim J, Kil IS, Seok YM, Yang ES, Kim DK, Lim DG, Park JW, Bonventre JV, Park KM. Orchiectomy attenuates postischemic oxidative stress and ischemia/reperfusion injury in mice. A role for manganese superoxide dismutase. J Biol Chem 281: 20349-20356, 2006.
20. Kim J, Kim DS, Park MJ, Cho HJ, Zervos AS, Bonventre JV, Park KM. Omi/HtrA2 protease is associated with tubular cell apoptosis and fibrosis induced by unilateral ureteral obstruction. Am J Physiol Renal Physiol 298: F1332-F1340, 2010.
21. Kim J, Kim KY, Jang HS, Yoshida T, Tsuchiya K, Nitta K, Park JW, Bonventre JV, Park KM. Role of cytosolic NADP+-dependent isocitrate dehydrogenase in ischemia-reperfusion injury in mouse kidney. Am J Physiol Renal Physiol 296: F622-F633, 2009.
22. Kim J, Park JW, Park KM. Increased superoxide formation induced by irradiation preconditioning triggers kidney resistance to ischemia-reperfusion injury in mice. Am J Physiol Renal Physiol 296: F1202-F1211, 2009.
23. Kim J, Seok YM, Jung KJ, Park KM. Reactive oxygen species/ oxidative stress contributes to progression of kidney fibrosis following transient ischemic injury in mice. Am J Physiol Renal Physiol 297: F461-F470, 2009.
24. Kitagawa K, Wada T, Furuichi K, Hashimoto H, Ishiwata Y, Asano M, Takeya M, Kuziel WA, Matsushima K, Mukaida N, Yokoyama H. Blockade of CCR2 ameliorates progressive fibrosis in kidney. Am J Pathol 165: 237-246, 2004.
25. Klahr S, Morrissey J. Obstructive nephropathy and renal fibrosis. Am J Physiol Renal Physiol 283: F861-F875, 2002.
26. Krishnakumar R, Gamble MJ, Frizzell KM, Berrocal JG, Kininis M, Kraus WL. Reciprocal binding of PARP-1 and histone H1 at promoters specifies transcriptional outcomes. Science 319: 819-821, 2008.
27. Li Y, Spataro BC, Yang J, Dai C, Liu Y. 1,25-Dihydroxyvitamin D inhibits renal interstitial myofibroblast activation by inducing hepatocyte growth factor expression. Kidney Int 68: 1500-1510, 2005.
28. Liaudet L, Pacher P, Mabley JG, Virag L, Soriano FG, Hasko G, Szabo C. Activation of poly(ADP-Ribose) polymerase-1 is a central mechanism of lipopolysaccharide-induced acute lung inflammation. Am J Respir Crit Care Med 165: 372-377, 2002.
29. Liu Y. New insights into epithelial-mesenchymal transition in kidney fibrosis. J Am Soc Nephrol 21: 212-222, 2010.
30. Ma FY, Liu J, Kitching AR, Manthey CL, Nikolic-Paterson DJ. Targeting renal macrophage accumulation via c-fms kinase reduces tubular apoptosis but fails to modify progressive fibrosis in the obstructed rat kidney. Am J Physiol Renal Physiol 296: F177-F185, 2009.
31. Mabley JG, Jagtap P, Perretti M, Getting SJ, Salzman AL, Virag L, Szabo E, Soriano FG, Liaudet L, Abdelkarim GE, Hasko G, Marton A, Southan GJ, Szabo C. Anti-inflammatory effects of a novel, potent inhibitor of poly (ADP-ribose) polymerase. Inflamm Res 50: 561-569, 2001.
32. 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.
33. Meldrum KK, Metcalfe P, Leslie JA, Misseri R, Hile KL, Meldrum DR. TNF-alpha neutralization decreases nuclear factor-kappaB activation and apoptosis during renal obstruction. J Surg Res 131: 182-188, 2006.
34. Melotti P, Nicolis E, Tamanini A, Rolfini R, Pavirani A, Cabrini G. Activation of NF-kB mediates ICAM-1 induction in respiratory cells exposed to an adenovirus-derived vector. Gene Ther 8: 1436-1442, 2001.
35. Menissier de Murcia J, Ricoul M, Tartier L, Niedergang C, Huber A, Dantzer F, Schreiber V, Ame JC, Dierich A, LeMeur M, Sabatier L, Chambon P, de Murcia G. Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. EMBO J 22: 2255-2263, 2003.
36. Misseri R, Meldrum DR, Dinarello CA, Dagher P, Hile KL, Rink RC, Meldrum KK. TNF-a mediates obstruction-induced renal tubular cell apoptosis and proapoptotic signaling. Am J Physiol Renal Physiol 288: F406-F411, 2005.
37. Morimoto Y, Gai Z, Tanishima H, Kawakatsu M, Itoh S, Hatamura I, Muragaki Y. TNF-alpha deficiency accelerates renal tubular interstitial fibrosis in the late stage of ureteral obstruction. Exp Mol Pathol 85: 207-213, 2008.
38. Moroni F, Meli E, Peruginelli F, Chiarugi A, Cozzi A, Picca R, Romagnoli P, Pellicciari R, Pellegrini-Giampietro DE. Poly(ADP-ribose) polymerase inhibitors attenuate necrotic but not apoptotic neuronal death in experimental models of cerebral ischemia. Cell Death Differ 8: 921-932, 2001.
39. Morrissey JJ, Klahr S. Rapid communication. Enalapril decreases nuclear factor kappa B activation in the kidney with ureteral obstruction. Kidney Int 52: 926-933, 1997.
40. Oliver FJ, Menissier-de Murcia J, Nacci C, Decker P, Andriantsito-haina R, Muller S, de la Rubia G, Stoclet JC, de Murcia G. Resistance to endotoxic shock as a consequence of defective NF-kappaB activation in poly (ADP-ribose) polymerase-1 deficient mice. EMBO J 18: 4446-4454, 1999.
41. Panzer U, Steinmetz OM, Turner JE, Meyer-Schwesinger C, von Ruffer C, Meyer TN, Zahner G, Gomez-Guerrero C, Schmid RM, Helmchen U, Moeckel GW, Wolf G, Stahl RA, Thaiss F. Resolution of renal inflammation: a new role for NF-kB1 (p50) in inflammatory kidney diseases. Am J Physiol Renal Physiol 297: F429-F439, 2009.
42. Park KM, Kramers C, Vayssier-Taussat M, Chen A, Bonventre JV. Prevention of kidney ischemia/reperfusion-induced functional injury, MAPK and MAPK kinase activation, and inflammation by remote transient ureteral obstruction. J Biol Chem 277: 2040-2049, 2002.
43. Pieper AA, Brat DJ, Krug DK, Watkins CC, Gupta A, Blackshaw S, Verma A, Wang ZQ, Snyder SH. Poly(ADP-ribose) polymerase-defi-cient mice are protected from streptozotocin-induced diabetes. Proc Natl Acad Sci USA 96: 3059-3064, 1999.
44. Pulskens WP, Rampanelli E, Teske GJ, Butter LM, Claessen N, Luirink IK, van der Poll T, Florquin S, Leemans JC. TLR4 promotes fibrosis but attenuates tubular damage in progressive renal injury. J Am Soc Nephrol 21: 1299-1308, 2010.
45. Reddy GK, Enwemeka CS. A simplified method for the analysis of hydroxyproline in biological tissues. Clin Biochem 29: 225-229, 1996.
46. Ruiz-Deya G, Sikka SC, Thomas R, Abdel-Mageed AB. Potential role for the nuclear transcription factor NF-kappa B in the pathogenesis of ureteropelvic junction obstruction. J Endourol 16: 611-615, 2002.
47. Shappell SB, Mendoza LH, Gurpinar T, Smith CW, Suki WN, Truong LD. Expression of adhesion molecules in kidney with experimental chronic obstructive uropathy: the pathogenic role of ICAM-1 and VCAM-1. Nephron 85: 156-166, 2000.
48. Sharma AK, Mauer SM, Kim Y, Michael AF. Interstitial fibrosis in obstructive nephropathy. Kidney Int 44: 774-788, 1993.
49. Sharp C, Warren A, Oshima T, Williams L, Li JH, Alexander JS. Poly ADP ribose-polymerase inhibitors prevent the upregulation of ICAM-1 and E-selectin in response to Th1 cytokine stimulation. Inflammation 25: 157-163, 2001.
50. Smith JM, Stablein DM, Munoz R, Hebert D, McDonald RA. Contributions of the transplant registry: the 2006 Annual Report of the North American Pediatric Renal Trials and Collaborative Studies (NAPRTCS). Ped Transpl 11: 366-373, 2007.
51. Sweat F, Puchtler H, Rosenthal SI. Sirius red F3ba as a stain for connective tissue. Arch Pathol 78: 69-72, 1964.
52. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676, 2006.
53. Tashiro K, Tamada S, Kuwabara N, Komiya T, Takekida K, Asai T, Iwao H, Sugimura K, Matsumura Y, Takaoka M, Nakatani T, Miura K. Attenuation of renal fibrosis by proteasome inhibition in rat obstructive nephropathy: possible role of nuclear factor kappaB. Int J Mol Med 12: 587-592, 2003.
54. Tulin A, Spradling A. Chromatin loosening by poly(ADP)-ribose polymerase (PARP) at Drosophila puff loci. Science 299: 560-562, 2003.
55. Zaniolo K, Desnoyers S, Leclerc S, Guerin SL. Regulation of poly-(ADP-ribose) polymerase-1 (PARP-1) gene expression through the post-translational modification of Sp1: a nuclear target protein of PARP-1. BMC Mol Biol 8: 96, 2007.
56. Zerfaoui M, Errami Y, Naura AS, Suzuki Y, Kim H, Ju J, Liu T, Hans CP, Kim JG, Abd Elmageed ZY, Koochekpour S, Catling A, Boulares AH. Poly(ADP-ribose) polymerase-1 is a determining factor in Crm1-mediated nuclear export and retention of p65 NF-kappa B upon TLR4 stimulation. J Immunol 185: 1894-1902, 2010.
57. 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.
58. Zingarelli B, Cuzzocrea S, Zsengeller Z, Salzman AL, Szabo C. Protection against myocardial ischemia and reperfusion injury by 3-ami-nobenzamide, an inhibitor of poly (ADP-ribose) synthetase. Cardiovasc Res 36: 205-215, 1997.
59. Zingarelli B, O'Connor M, Hake PW. Inhibitors of poly (ADP-ribose) polymerase modulate signal transduction pathways in colitis. Eur J Pharmacol 469: 183-194, 2003.