Induction of heme oxygenase-1 can halt and even reverse renal tubule-interstitial fibrosis

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Correa Costa, Matheus ^a,b   Semedo, Patricia ^a   Monteiro, Ana Paula F S ^a   Silva, Reinaldo C ^a   Pereira, Rafael L ^a   Gonçalves, Giselle M ^b   Marques, Georgia Daniela Marcusso ^a   Cenedeze, Marcos A ^a   Faleiros, Ana C G ^c   Keller, Alexandre C ^a   Shimizu, Maria H M ^b   Seguro, Antônio C ^b   Reis, Marlene A ^c   Pacheco Silva, Alvaro ^a   Câmara, Niels O S ^a,b  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c FEDERAL UNIVERSITY OF TRIÂNGULO MINEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CREATININE; HEME OXYGENASE 1; HEMIN; INSULIN; TRANSFORMING GROWTH FACTOR BETA;

ALBUMINURIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE MEASUREMENT; BLOOD SAMPLING; CONTROLLED STUDY; CREATININE BLOOD LEVEL; CREATININE URINE LEVEL; CYTOKINE PRODUCTION; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INDUCTION; GENE EXPRESSION; HUMAN; HUMAN CELL; KIDNEY DYSFUNCTION; KIDNEY FIBROSIS; KIDNEY FUNCTION TEST; KIDNEY PARENCHYMA; KIDNEY TUBULE DISORDER; MALE; NEPHRITIS; NONHUMAN; PROTEIN EXPRESSION; PROTEINURIA; RAT; SPRAGUE DAWLEY RAT; THERAPY DELAY; URETER OBSTRUCTION; URINALYSIS; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; DISEASE COURSE; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBROSIS; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; INFLAMMATION; KIDNEY DISEASE; KIDNEY TUBULE; METABOLISM; METHODOLOGY; PATHOLOGY;

ANIMALIA; RATTUS;

ANIMALS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FIBROSIS; GENE EXPRESSION PROFILING; HEME OXYGENASE-1; HEMIN; IMMUNOHISTOCHEMISTRY; INFLAMMATION; KIDNEY DISEASES; KIDNEY TUBULES; MALE; MODELS, BIOLOGICAL; RATS; RATS, SPRAGUE-DAWLEY; TRANSFORMING GROWTH FACTOR BETA;

EID: 78650770176     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014298     Document Type: Article

References (54)

1. Strutz F, Neilson EG (2003) New insights into mechanisms of fibrosis in immune renal injury. Springer Semin Immunopathol 24: 459-476.
2. Nath KA (1992) Tubulointerstitial changes as a major determinant in the progression of renal damage. Am J Kidney Dis 20: 1-17.
3. Klahr S, Morrissey J (2002) Obstructive nephropathy and renal fibrosis. Am J Physiol Renal Physiol 283: F861-875.
4. Bascands JL, Schanstra JP (2005) Obstructive nephropathy: insights from genetically engineered animals. Kidney Int 68: 925-937.
5. Bombara MP, Webb DL, Conrad P, Marlor CW, Sarr T, et al. (1993) Cell contact between T cells and synovial fibroblasts causes induction of adhesion molecules and cytokines. J Leukoc Biol 54: 399-406.
6. Burger D, Rezzonico R, Li JM, Modoux C, Pierce RA, et al. (1998) Imbalance between interstitial collagenase and tissue inhibitor of metalloproteinases 1 in synoviocytes and fibroblasts upon direct contact with stimulated T lymphocytes: involvement of membrane-associated cytokines. Arthritis Rheum 41: 1748-1759.
7. Hill-Kapturczak N, Chang SH, Agarwal A (2002) Heme oxygenase and the kidney. DNA Cell Biol 21: 307-321.
8. Kirkby KA, Adin CA (2006) Products of heme oxygenase and their potential therapeutic applications. Am J Physiol Renal Physiol 290: F563-571.
9. Kim JH, Yang JI, Jung MH, Hwa JS, Kang KR, et al. (2006) Heme oxygenase-1 protects rat kidney from ureteral obstruction via an antiapoptotic pathway. J Am Soc Nephrol 17: 1373-1381.
10. Desbuards N, Hyvelin JM, Machet MC, Eder V, Garrigue MA, et al. (2009) Heme Oxygenase-1 Inducer Hemin Attenuates the Progression of Remnant Kidney Model. Nephron Exp Nephrol 113: e35-e44.
11. Goncalves GM, Cenedeze MA, Feitoza CQ, Wang PM, Bertocchi AP, et al. (2006) The role of heme oxygenase 1 in rapamycin-induced renal dysfunction after ischemia and reperfusion injury. Kidney Int 70: 1742-1749.
12. Goodman AI, Olszanecki R, Yang LM, Quan S, Li M, et al. (2007) Heme oxygenase-1 protects against radiocontrast-induced acute kidney injury by regulating anti-apoptotic proteins. Kidney Int 72: 945-953.
13. Rezzani R, Rodella L, Buffoli B, Goodman AA, Abraham NG, et al. (2005) Change in renal heme oxygenase expression in cyclosporine A-induced injury. J Histochem Cytochem 53: 105-112.
14. Shiraishi F, Curtis LM, Truong L, Poss K, Visner GA, et al. (2000) Heme oxygenase-1 gene ablation or expression modulates cisplatin-induced renal tubular apoptosis. Am J Physiol Renal Physiol 278: F726-736.
15. Kie JH, Kapturczak MH, Traylor A, Agarwal A, Hill-Kapturczak N (2008) Heme oxygenase-1 deficiency promotes epithelial-mesenchymal transition and renal fibrosis. J Am Soc Nephrol 19: 1681-1691.
16. Giannico G, Yang H, Neilson EG, Fogo AB (2009) Dystroglycan in the diagnosis of FSGS. Clin J Am Soc Nephrol 4: 1747-1753.
17. Ruggenenti P, Schieppati A, Remuzzi G (2001) Progression, remission, regression of chronic renal diseases. Lancet 357: 1601-1608.
18. Noris M, Mister M, Pezzotta A, Azzollini N, Cassis P, et al. (2003) ACE inhibition limits chronic injury of kidney transplant even with treatment started when lesions are established. Kidney Int 64: 2253-2261.
19. Grimm PC, Nickerson P, Gough J, McKenna R, Stern E, et al. (2003) Computerized image analysis of Sirius Red-stained renal allograft biopsies as a surrogate marker to predict long-term allograft function. J Am Soc Nephrol 14: 1662-1668.
20. Chevalier RL, Forbes MS, Thornhill BA (2009) Ureteral obstruction as a model of renal interstitial fibrosis and obstructive nephropathy. Kidney Int 75: 1145-1152.
21. Moriyama T, Kawada N, Nagatoya K, Takeji M, Horio M, et al. (2001) Fluvastatin suppresses oxidative stress and fibrosis in the interstitium of mouse kidneys with unilateral ureteral obstruction. Kidney Int 59: 2095-2103.
22. Keyse SM, Tyrrell RM (1989) Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc Natl Acad Sci U S A 86: 99-103.
23. Opanashuk LA, Finkelstein JN (1995) Relationship of lead-induced proteins to stress response proteins in astroglial cells. J Neurosci Res 42: 623-632.
24. Vile GF, Basu-Modak S, Waltner C, Tyrrell RM (1994) Heme oxygenase 1 mediates an adaptive response to oxidative stress in human skin fibroblasts. Proc Natl Acad Sci U S A 91: 2607-2610.
25. Vogt BA, Alam J, Croatt AJ, Vercellotti GM, Nath KA (1995) Acquired resistance to acute oxidative stress. Possible role of heme oxygenase and ferritin. Lab Invest 72: 474-483.
26. Abraham NG, Cao J, Sacerdoti D, Li X, Drummond G (2009) Heme oxygenase: the key to renal function regulation. Am J Physiol Renal Physiol 297: F1137-1152.
27. Blancou P, Tardif V, Simon T, Remy S, Carreno L, et al. Immunoregulatory properties of heme oxygenase-1. Methods Mol Biol 677: 247-268.
28. Eyssen-Hernandez R, Ladoux A, Frelin C (1996) Differential regulation of cardiac heme oxygenase-1 and vascular endothelial growth factor mRNA expressions by hemin, heavy metals, heat shock and anoxia. FEBS Lett 382: 229-233.
29. Ishikawa K, Navab M, Leitinger N, Fogelman AM, Lusis AJ (1997) Induction of heme oxygenase-1 inhibits the monocyte transmigration induced by mildly oxidized LDL. J Clin Invest 100: 1209-1216.
30. Shibahara S, Muller RM, Taguchi H (1987) Transcriptional control of rat heme oxygenase by heat shock. J Biol Chem 262: 12889-12892.
31. Jarmi T, Agarwal A (2009) Heme oxygenase and renal disease. Curr Hypertens Rep 11: 56-62.
32. Kliem V, Johnson RJ, Alpers CE, Yoshimura A, Couser WG, et al. (1996) Mechanisms involved in the pathogenesis of tubulointerstitial fibrosis in 5/6-nephrectomized rats. Kidney Int 49: 666-678.
33. Magnasco A, Corselli M, Bertelli R, Ibatici A, Peresi M, et al. (2008) Mesenchymal stem cells protective effect in adriamycin model of nephropathy. Cell Transplant 17: 1157-1167.
34. Chung AC, Huang XR, Zhou L, Heuchel R, Lai KN, et al. (2009) Disruption of the Smad7 gene promotes renal fibrosis and inflammation in unilateral ureteral obstruction (UUO) in mice. Nephrol Dial Transplant 24: 1443-1454.
35. Meldrum KK, Misseri R, Metcalfe P, Dinarello CA, Hile KL, et al. (2007) TNFalpha neutralization ameliorates obstruction-induced renal fibrosis and dysfunction. Am J Physiol Regul Integr Comp Physiol 292: R1456-1464.
36. Wang PH, Cenedeze MA, Campanholle G, Malheiros DM, Torres HA, et al. (2009) Deletion of bradykinin B1 receptor reduces renal fibrosis. Int Immunopharmacol 9: 653-657.
37. Tashiro K, Tamada S, Kuwabara N, Komiya T, Takekida K, et al. (2003) Attenuation of renal fibrosis by proteasome inhibition in rat obstructive nephropathy: possible role of nuclear factor kappaB. Int J Mol Med 12: 587-592.
38. Miyajima A, Kosaka T, Seta K, Asano T, Umezawa K, et al. (2003) Novel nuclear factor kappa B activation inhibitor prevents inflammatory injury in unilateral ureteral obstruction. J Urol 169: 1559-1563.
39. Murphy JE, Robert C, Kupper TS (2000) Interleukin-1 and cutaneous inflammation: a crucial link between innate and acquired immunity. J Invest Dermatol 114: 602-608.
40. Eddy AA (2000) Molecular basis of renal fibrosis. Pediatr Nephrol 15: 290-301.
41. Wang L, Lee JY, Kwak JH, He Y, Kim SI, et al. (2008) Protective effects of lowdose carbon monoxide against renal fibrosis induced by unilateral ureteral obstruction. Am J Physiol Renal Physiol 294: F508-517.
42. Gaudio KM, Siegel NJ, Hayslett JP, Kashgarian M (1980) Renal perfusion and intratubular pressure during ureteral occlusion in the rat. Am J Physiol 238: F205-209.
43. Lennon GM, Ryan PC, Fitzpatrick JM (1993) Recovery of ureteric motility following complete and partial ureteric obstruction. Br J Urol 72: 702-707.
44. Matsuo S, Lopez-Guisa JM, Cai X, Okamura DM, Alpers CE, et al. (2005) Multifunctionality of PAI-1 in fibrogenesis: evidence from obstructive nephropathy in PAI-1-overexpressing mice. Kidney Int 67: 2221-2238.
45. Matsumoto H, Ishikawa K, Itabe H, Maruyama Y (2006) Carbon monoxide and bilirubin from heme oxygenase-1 suppresses reactive oxygen species generation and plasminogen activator inhibitor-1 induction. Mol Cell Biochem 291: 21-28.
46. Bataller R, Brenner DA (2005) Liver fibrosis. J Clin Invest 115: 209-218.
47. Hwang M, Kim HJ, Noh HJ, Chang YC, Chae YM, et al. (2006) TGF-beta1 siRNA suppresses the tubulointerstitial fibrosis in the kidney of ureteral obstruction. Exp Mol Pathol 81: 48-54.
48. Kawai T, Masaki T, Doi S, Arakawa T, Yokoyama Y, et al. (2009) PPARgamma agonist attenuates renal interstitial fibrosis and inflammation through reduction of TGF-beta. Lab Invest 89: 47-58.
49. Iwai T, Kitamoto K, Teramoto K, Machida Y, Tamada S, et al. (2008) Cobalt protoporphyrin attenuates rat obstructive nephropathy: role of cellular infiltration. Urology 72: 432-438.
50. Xu Y, Wan J, Jiang D, Wu X (2009) BMP-7 counteracts TGF-beta1-induced epithelial-to-mesenchymal transition in human renal proximal tubular epithelial cells. J Nephrol 22: 403-410.
51. Yan JD, Yang S, Zhang J, Zhu TH (2009) BMP6 reverses TGF-beta1-induced changes in HK-2 cells: implications for the treatment of renal fibrosis. Acta Pharmacol Sin 30: 994-1000.
52. Fioretto P, Kim Y, Mauer M (1998) Diabetic nephropathy as a model of reversibility of established renal lesions. Curr Opin Nephrol Hypertens 7: 489-494.
53. Ma LJ, Nakamura S, Aldigier JC, Rossini M, Yang H, et al. (2005) Regression of glomerulosclerosis with high-dose angiotensin inhibition is linked to decreased plasminogen activator inhibitor-1. J Am Soc Nephrol 16: 966-976.
54. Shin DH, Park HM, Jung KA, Choi HG, Kim JA, et al. The NRF2-heme oxygenase-1 system modulates cyclosporin A-induced epithelial-mesenchymal transition and renal fibrosis. Free Radic Biol Med 48: 1051-1063.