Heme oxygenase-1 deficiency promotes epithelial-mesenchymal transition and renal fibrosis

Journal of the American Society of Nephrology

Volumn 19, Issue 9, 2008, Pages 1681-1691

  Kie, Jeong Hae ^a,c   Kapturczak, Matthias H ^a   Traylor, Amie ^a   Agarwal, Anupam ^a,b   Hill Kapturczak, Nathalie ^a,b  

^a University of Alabama at Birmingham   (United States)

^b University of Alabama at Birmingham   (United States)

^c National Health Insurance Corporation   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CALVASCULIN; HEME OXYGENASE 1; TRANSFORMING GROWTH FACTOR BETA1; BIOLOGICAL MARKER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; ENZYME INDUCTION; HYDRONEPHROSIS; KIDNEY FIBROSIS; KIDNEY TUBULE CELL; MACROPHAGE; MESENCHYME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; URETER OBSTRUCTION; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL TRANSDIFFERENTIATION; ENZYMOLOGY; FIBROSIS; IMMUNOLOGY; KIDNEY; KIDNEY PROXIMAL TUBULE; METABOLISM; MOUSE MUTANT; NEPHROSCLEROSIS; PATHOLOGY; PHYSIOLOGY;

ANIMALS; BIOLOGICAL MARKERS; CELL TRANSDIFFERENTIATION; CELLS, CULTURED; FIBROSIS; HEME OXYGENASE-1; KIDNEY; KIDNEY TUBULES, PROXIMAL; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEPHROSCLEROSIS; TRANSFORMING GROWTH FACTOR BETA1; URETERAL OBSTRUCTION;

EID: 54749083116     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2007101099     Document Type: Article

References (61)

1. Klahr S, Morrissey J: Obstructive nephropathy and renal fibrosis. Am J Physiol Renal Physiol 283: F861-F875, 2002
2. Bascands JL, Schanstra JP: Obstructive nephropathy: Insights from genetically engineered animals. Kidney Int 68: 925-937, 2005
3. Yang SP, Woolf AS, Quinn F, Winyard PJ: Deregulation of renal transforming growth factor-beta1 after experimental short-term ureteric obstruction in fetal sheep. Am J Pathol 159: 109-117, 2001
4. Docherty NG, O'Sullivan OE, Healy DA, Murphy M, O'Neill AJ, Fitzpatrick JM, Watson RW: TGF-β1 induced EMT can occur independently of its pro-apoptotic effects and is aided by EGF receptor activation. Am J Physiol Renal Physiol 290: F1202-F1212, 2006
5. Yang J, Liu Y: Dissection of key events in tubular epithelial to myofibroblast transition and its implications in renal interstitial fibrosis. Am J Pathol 159: 1465-1475, 2001
6. Hay ED: An overview of epithelio-mesenchymal transformation. Acta Anat (Basel) 154: 8-20, 1995
7. Okada H, Danoff TM, Kalluri R, Neilson EG: Early role of Fsp1 in epithelial-mesenchymal transformation. Am J Physiol 273: F563-F574, 1997
8. Zeisberg M, Bonner G, Maeshima Y, Colorado P, Muller GA, Strutz F, Kalluri R: Renal fibrosis: Collagen composition and assembly regulates epithelial-mesenchymal transdifferentiation. Am J Pathol 159: 1313-1321, 2001
9. Fan JM, Huang XR, Ng YY, Nikolic-Paterson DJ, Mu W, Atkins RC, Lan HY: Interleukin-1 induces tubular epithelial-myofibroblast transdifferentiation through a transforming growth factor-beta1-dependent mechanism in vitro. Am J Kidney Dis 37: 820-831, 2001
10. Strutz F, Zeisberg M, Ziyadeh FN, Yang CQ, Kalluri R, Muller GA, Neilson EG: Role of basic fibroblast growth factor-2 in epithelial-mesenchymal transformation. Kidney Int 61: 1714-1728, 2002
11. Park SH, Choi MJ, Song IK, Choi SY, Nam JO, Kim CD, Lee BH, Park RW, Park KM, Kim YJ, Kim IS, Kwon TH, Kim YL: Erythropoietin decreases renal fibrosis in mice with ureteral obstruction: Role of inhibiting TGF-beta-induced epithelial-to-mesenchymal transition. J Am Soc Nephrol 18: 1497-1507, 2007
12. Traylor A, Hock T, Hill-Kapturczak N: Specificity protein 1 and Smad-dependent regulation of human heme oxygenase-1 gene by transforming growth factor-beta1 in renal epithelial cells. Am J Physiol Renal Physiol 293: F885-F894, 2007
13. Hill-Kapturczak N, Truong L, Thamilselvan V, Visner GA, Nick HS, Agarwal A: Smad7-dependent regulation of heme oxygenase-1 by transforming growth factor-beta in human renal epithelial cells. J Biol Chem 275: 40904-40909, 2000
14. Maines MD: The heme oxygenase system: A regulator of second messenger gases. Annu Rev Pharmacol Toxicol 37: 517-554, 1997
15. Hill-Kapturczak N, Chang SH, Agarwal A: Heme oxygenase and the kidney. DNA Cell Biol 21: 307-321, 2002
16. Morimoto K, Ohta K, Yachie A, Yang Y, Shimizu M, Goto C, Toma T, Kasahara Y, Yokoyama H, Miyata T, Seki H, Koizumi S: Cytoprotective role of heme oxygenase (HO)-1 in human kidney with various renal diseases. Kidney Int 60: 1858-1866, 2001
17. Nath KA: Heme oxygenase-1: A provenance for cytoprotective pathways in the kidney and other tissues. Kidney Int 70: 432-443, 2006
18. Willis D, Moore AR, Frederick R, Willoughby DA: Heme oxygenase: A novel target for the modulation of the inflammatory response. Nat Med 2: 87-90, 1996
19. Jones EA, Shahed A, Shoskes DA: Modulation of apoptotic and inflammatory genes by bioflavonoids and angiotensin II inhibition in ureteral obstruction. Urology 56: 346-351, 2000
20. Kawada N, Moriyama T, Ando A, Fukunaga M, Miyata T, Kurokawa K, Imai E, Hori M: Increased oxidative stress in mouse kidneys with unilateral ureteral obstruction. Kidney Int 56: 1004-1013, 1999
21. Pat B, Yang T, Kong C, Watters D, Johnson DW, Gobe G: Activation of ERK in renal fibrosis after unilateral ureteral obstruction: Modulation by antioxidants. Kidney Int 67: 931-943, 2005
22. Kim JH, Yang JI, Jung MH, Hwa JS, Kang KR, Park DJ, Roh GS, Cho GJ, Choi WS, Chang SH: Heme oxygenase-1 protects rat kidney from ureteral obstruction via an antiapoptotic pathway. J Am Soc Nephrol 17: 1373-1381, 2006
23. Chakder S, Rathi S, Ma XL, Rattan S: Heme oxygenase inhibitor zinc protoporphyrin IX causes an activation of nitric oxide synthase in the rabbit internal anal sphincter. J Pharmacol Exp Ther 277: 1376-1382, 1996
24. Jozkowicz A, Dulak J: Effects of protoporphyrins on production of nitric oxide and expression of vascular endothelial growth factor in vascular smooth muscle cells and macrophages. Acta Biochim Pol 50: 69-79, 2003
25. Wolff DJ, Naddelman RA, Lubeskie A, Saks DA: Inhibition of nitric oxide synthase isoforms by porphyrins. Arch Biochem Biophys 333: 27-34, 1996
26. Vora JP, Zimsen SM, Houghton DC, Anderson S: Evolution of metabolic and renal changes in the ZDF/Drt-fa rat model of type II diabetes. J Am Soc Nephrol 7: 113-117, 1996
27. Taub M, Sato G: Growth of functional primary cultures of kidney epithelial cells in defined medium. J Cell Physiol 105: 369-378, 1980
28. Burns WC, Kantharidis P, Thomas MC: The role of tubular epithelial-mesenchymal transition in progressive kidney disease. Cells Tissues Organs 185: 222-231, 2007
29. Yoo KH, Thornhill BA, Forbes MS, Coleman CM, Marcinko ES, Liaw L, Chevalier RL: Osteopontin regulates renal apoptosis and interstitial fibrosis in neonatal chronic unilateral ureteral obstruction. Kidney Int 70: 1735-1741, 2006
30. Kida Y, Asahina K, Teraoka H, Gitelman I, Sato T: Twist relates to tubular epithelial-mesenchymal transition and interstitial fibrogenesis in the obstructed kidney. J Histochem Cytochem 55: 661-673, 2007
31. Klahr S: Obstructive nephropathy. Kidney Int 54: 286-300, 1998
32. Klahr S, Morrissey J: Obstructive nephropathy and renal fibrosis: The role of bone morphogenic protein-7 and hepatocyte growth factor. Kidney Int Suppl S105-S112, 2003
33. Diamond JR, Kees-Folts D, Ding G, Frye JE, Restrepo NC: Macrophages, monocyte chemoattractant peptide-1, and TGF-beta 1 in experimental hydronephrosis. Am J Physiol Renal Physiol 266: F926-F933, 1994
34. Diamond JR, van Goor H, Ding G, Engelmyer E: Myofibroblasts in experimental hydronephrosis. Am J Pathol 146: 121-129, 1995
35. Diamond JR: Macrophages and progressive renal disease in experimental hydronephrosis. Am J Kidney Dis 26: 133-140, 1995
36. Diamond JR, Kees-Folts D, Ding G, Frye JE, Restrepo NC: Macrophages, monocyte chemoattractant peptide-1, and TGF-beta 1 in experimental hydronephrosis. Am J Physiol 266: F926-F933, 1994
37. Yamate J, Okado A, Kuwamura M, Tsukamoto Y, Ohashi F, Kiso Y, Nakatsuji S, Kotani T, Sakuma S, Lamarre J: Immunohistochemical analysis of macrophages, myofibroblasts, and transforming growth factor-beta localization during rat renal interstitial fibrosis following long-term unilateral ureteral obstruction. Toxicol Pathol 26: 793-801, 1998
38. Vogt BA, Shanley TP, Croatt A, Alam J, Johnson KJ, Nath KA: Glomerular inflammation induces resistance to tubular injury in the rat: A novel form of acquired, heme oxygenase-dependent resistance to renal injury. J Clin Invest 98: 2139-2145, 1996
39. Nath KA, Vercellotti GM, Grande JP, Miyoshi H, Paya CV, Manivel JC, Haggard JJ, Croatt AJ, Payne WD, Alam J: Heme protein-induced chronic renal inflammation: Suppressive effect of induced heme oxygenase-1. Kidney Int 59: 106-117, 2001
40. Murali NS, Ackerman AW, Croatt AJ, Cheng J, Grande JP, Sutor SL, Bram RJ, Bren GD, Badley AD, Alam J, Nath KA: Renal upregulation of HO-1 reduces albumin-driven MCP-1 production: Implications for chronic kidney disease. Am J Physiol Renal Physiol 292: F837-F844, 2007
41. Pittock ST, Norby SM, Grande JP, Croatt AJ, Bren GD, Badley AD, Caplice NM, Griffin MD, Nath KA: MCP-1 is up-regulated in unstressed and stressed HO-1 knockout mice: Pathophysiologic correlates. Kidney Int 68: 611-622, 2005
42. Medici D, Hay ED, Goodenough DA: Cooperation between snail and LEF-1 transcription factors is essential for TGF-beta1-induced epithelial-mesenchymal transition. Mol Biol Cell 17: 1871-1879, 2006
43. Vongwiwatana A, Tasanarong A, Rayner DC, Melk A, Halloran PF: Epithelial to mesenchymal transition during late deterioration of human kidney transplants: The role of tubular cells in fibrogenesis. Am J Transplant 5: 1367-1374, 2005
44. Donato R: Intracellular and extracellular roles of S100 proteins. Microsc Res Tech 60: 540-551, 2003
45. Iwano M, Plieth D, Danoff TM, Xue C, Okada H, Neilson EG: Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 110: 341-350, 2002
46. Zeisberg M, Hanai J, Sugimoto H, Mammoto T, Charytan D, Strutz F, Kalluri R: BMP-7 counteracts TGF-beta1-induced epithelial-to-mesenchymal transition and reverses chronic renal injury. Nat Med 9: 964-968, 2003
47. Sato M, Muragaki Y, Saika S, Roberts AB, Ooshima A: Targeted disruption of TGF-beta1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. J Clin Invest 112: 1486-1494, 2003
48. Rhyu DY, Yang Y, Ha H, Lee GT, Song JS, Uh S-t, Lee HB: Role of reactive oxygen species in TGF-β1-induced mitogen-activated protein kinase activation and epithelial-mesenchymal transition in renal tubular epithelial cells. J Am Soc Nephrol 16: 667-675, 2005
49. Radisky DC, Kenny PA, Bissell MJ: Fibrosis and cancer: Do myofibroblasts come also from epithelial cells via EMT? J Cell Biochem 101: 830-839, 2007
50. Tsui TY, Wu X, Lau CK, Ho DW, Xu T, Siu YT, Fan ST: Prevention of chronic deterioration of heart allograft by recombinant adeno-associated virus-mediated heme oxygenase-1 gene transfer. Circulation 107: 2623-2629, 2003
51. Mark A, Hock T, Kapturczak MH, Agarwal A, Hill-Kapturczak N: Induction of heme oxygenase-1 modulates the profibrotic effects of transforming growth factor-beta in human renal tubular epithelial cells. Cell Mol Biol (Noisy-le-grand) 51: 357-362, 2005
52. Fujita T, Toda K, Karimova A, Yan SF, Naka Y, Yet SF, Pinsky DJ: Paradoxical rescue from ischemic lung injury by inhaled carbon monoxide driven by derepression of fibrinolysis. Nat Med 7: 598-604, 2001
53. Gong LM, Du JB, Shi L, Shi Y, Tang CS: Effects of endogenous carbon monoxide on collagen synthesis in pulmonary artery in rats under hypoxia. Life Sci 74: 1225-1241, 2004
54. Morse D, Choi AM: Heme oxygenase-1: The "emerging molecule" has arrived. Am J Respir Cell Mol Biol 27: 8-16, 2002
55. Li L, Grenard P, Nhieu JT, Julien B, Mallat A, Habib A, Lotersztajn S: Heme oxygenase-1 is an antifibrogenic protein in human hepatic myofibroblasts. Gastroenterology 125: 460-469, 2003
56. Wang HD, Yamaya M, Okinaga S, Jia YX, Kamanaka M, Takahashi H, Guo LY, Ohrui T, Sasaki H: Bilirubin ameliorates bleomycin-induced pulmonary fibrosis in rats. Am J Respir Crit Care Med 165: 406-411, 2002
57. Zhou Z, Song R, Fattman CL, Greenhill S, Alber S, Oury TD, Choi AM, Morse D: Carbon monoxide suppresses bleomycin-induced lung fibrosis. Am J Pathol 166: 27-37, 2005
58. Abdel-Aziz MT, el-Asmar MF, el-Miligy D, Atta H, Shaker O, Ghattas MH, Hosni H, Kamal N: Retrovirus-mediated human heme oxygenase-1 (HO-1) gene transfer into rat endothelial cells: The effect of HO-1 inducers on the expression of cytokines. Int J Biochem Cell Biol 35: 324-332, 2003
59. Kapturczak MH, Wasserfall C, Brusko T, Campbell-Thompson M, Ellis TM, Atkinson MA, Agarwal A: Heme oxygenase-1 modulates early inflammatory responses: Evidence from the heme oxygenase-1-deficient mouse. Am J Pathol 165: 1045-1053, 2004
60. Matsuo S, Lopez-Guisa JM, Cai X, Okamura DM, Alpers CE, Bumgarner RE, Peters MA, Zhang G, Eddy AA: Multifunctionality of PAI-1 in fibrogenesis: Evidence from obstructive nephropathy in PAI-1-overexpressing mice. Kidney Int 67: 2221-2238, 2005
61. Chen S, Hoffman BB, Lee JS, Kasama Y, Jim B, Kopp JB, Ziyadeh FN: Cultured tubule cells from TGF-beta1 null mice exhibit impaired hypertrophy and Fn expression in high glucose. Kidney Int 65: 1191-1204, 2004