Hepatocyte growth factor preferentially activates the anti-inflammatory arm of NF-κB signaling to induce A20 and protect renal proximal tubular epithelial cells from inflammation

Journal of Cellular Physiology

Volumn 227, Issue 4, 2012, Pages 1382-1390

  da Silva, Cleide G ^a   Maccariello, Elizabeth R ^a,b   Wilson, Szuhuei Wu ^a   Putheti, Prabhakar ^a   Daniel, Soizic ^a   Damrauer, Scott M ^a   Peterson, Clayton R ^a   Siracuse, Jeffrey J ^a   Kaczmarek, Elzbieta ^a   Ferran, Christiane ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HOSPITAL UNIVERSITÁRIO PEDRO ERNESTO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; MESSENGER RNA; PROTEIN A20; SCATTER FACTOR; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

ARTICLE; GENE CONTROL; HUMAN; HUMAN CELL; KIDNEY INJURY; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; NEPHRITIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RENAL PROTECTION; UPREGULATION;

CELLS, CULTURED; EPITHELIAL CELLS; HEPATOCYTE GROWTH FACTOR; HUMANS; INFLAMMATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KIDNEY TUBULES, PROXIMAL; NF-KAPPA B; NUCLEAR PROTEINS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RNA, MESSENGER; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84855722915     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22851     Document Type: Article

References (83)

1. Akcay A, Nguyen Q, Edelstein CL. 2009. Mediators of inflammation in acute kidney injury. Mediators Inflamm 2009:137072.
2. Arvelo MB, Cooper JT, Longo C, Daniel S, Grey ST, Mahiou J, Czismadia E, Abu-Jawdeh G, Ferran C. 2002. A20 protects mice from galactosmine/lipopolysaccharide acute toxic lethal hepatitis. Hepatology 35:535-543.
3. Bach FH, Hancock WW, Ferran C. 1997. Protective genes expressed in endothelial cells: A regulatory response to injury. Immunol Today 18:483-486.
4. Bendinelli P, Matteucci E, Dogliotti G, Corsi MM, Banfi G, Maroni P, Desiderio MA. 2010. Molecular basis of anti-inflammatory action of platelet-rich plasma on human chondrocytes: Mechanisms of NF-kappaB inhibition via HGF. J Cell Physiol 225:757-766.
5. Beyaert R, Heyninck K, van Huffel S. 2000. A20 and A20-binding proteins as cellular inhibitors of nuclear factor-κB-dependent gene expression and apoptosis. Biochem Pharmacol 60:1143-1151.
6. Bonventre JV, Zuk A. 2004. Ischemic acute renal failure: An inflammatory disease? Kidney Int 66:480-485.
7. Cao CC, Ding XQ, Ou ZL, Liu CF, Li P, Wang L, Zhu CF. 2004. In vivo transfection of NF-kappaB decoy oligodeoxynucleotides attenuate renal ischemia/reperfusion injury in rats. Kidney Int 65:834-845.
8. Collins T, Read MA, Neish AS, Whitley MZ, Thanos D, Maniatis T. 1995. Transcriptional regulation of endothelial cell adhesion molecules - NF-κB and cytokine-inducible enhancers. FASEB J 9:899-909.
9. Comoglio PM, Giordano S, Trusolino L. 2008. Drug development of MET inhibitors: Targeting oncogene addiction and expedience. Nat Rev Drug Discov 7:504-516.
10. Cooper JT, Stroka DM, Brostjan C, Palmetshofer A, Bach FH, Ferran C. 1996. A20 blocks endothelial cell activation through a NF-κB-dependent mechanism. J Biol Chem 271:18068-18073.
11. Daniel S, Arvelo MB, Patel VI, Longo CR, Shrikhande G, Shukri T, Mahiou J, Sun DW, Mottley C, Grey ST, Ferran C. 2004. A20 protects endothelial cells from TNF-, Fas-, and NK-mediated cell death by inhibiting caspase 8 activation. Blood 104:2376-2384.
12. Dejardin E. 2006. The alternative NF-kappaB pathway from biochemistry to biology: Pitfalls and promises for future drug development. Biochem Pharmacol 72:1161-1179.
13. Eddy AA. 2005. Progression in chronic kidney disease. Adv Chronic Kidney Dis 12:353-365.
14. Fan S, Gao M, Meng Q, Laterra JJ, Symons MH, Coniglio S, Pestell RG, Goldberg ID, Rosen EM. 2005. Role of NF-kappaB signaling in hepatocyte growth factor/scatter factor-mediated cell protection. Oncogene 24:1749-1766.
15. Feng B, Chen G, Zheng X, Sun H, Zhang X, Zhang ZX, Xiang Y, Ichim TE, Garcia B, Luke P, Jevnikar AM, Min WP. 2009. Small interfering RNA targeting RelB protects against renal ischemia-reperfusion injury. Transplantation 87:1283-1289.
16. Ferran C, Stroka DM, Badrichani AZ, Cooper JT, Wrighton CJ, Soares M, Grey ST, Bach FH. 1998. A20 inhibits NF-kappaB activation in endothelial cells without sensitizing to tumor necrosis factor-mediated apoptosis. Blood 91:2249-2258.
17. Giannopoulou M, Dai C, Tan X, Wen X, Michalopoulos GK, Liu Y. 2008. Hepatocyte growth factor exerts its anti-inflammatory action by disrupting nuclear factor-kappaB signaling. Am J Pathol 173:30-41.
18. Gong R. 2008. Multi-target anti-inflammatory action of hepatocyte growth factor. Curr Opin Investig Drugs 9:1163-1170.
19. Gong R, Rifai A, Dworkin LD. 2005. Activation of PI3K-Akt-GSK3beta pathway mediates hepatocyte growth factor inhibition of RANTES expression in renal tubular epithelial cells. Biochem Biophys Res Commun 330:27-33.
20. Gong R, Rifai A, Dworkin LD. 2006a. Anti-inflammatory effect of hepatocyte growth factor in chronic kidney disease: Targeting the inflamed vascular endothelium. J Am Soc Nephrol 17:2464-2473.
21. Gong R, Rifai A, Dworkin LD. 2006b. Hepatocyte growth factor suppresses acute renal inflammation by inhibition of endothelial E-selectin. Kidney Int 69:1166-1174.
22. Gong R, Rifai A, Ge Y, Chen S, Dworkin LD. 2008. Hepatocyte growth factor suppresses proinflammatory NFkappaB activation through GSK3beta inactivation in renal tubular epithelial cells. J Biol Chem 283:7401-7410.
23. Gong R, Rifai A, Tolbert EM, Biswas P, Centracchio JN, Dworkin LD. 2004. Hepatocyte growth factor ameliorates renal interstitial inflammation in rat remnant kidney by modulating tubular expression of macrophage chemoattractant protein-1 and RANTES. J Am Soc Nephrol 15:2868-2881.
24. Grey ST, Arvelo MB, Hasenkamp W, Bach FH, Ferran C. 1999. A20 inhibits cytokine-induced apoptosis and nuclear factor κB-dependent gene activation in islets. J Exp Med 190:1135-1145.
25. Gueler F, Gwinner W, Schwarz A, Haller H. 2004. Long-term effects of acute ischemia and reperfusion injury. Kidney Int 66:523-527.
26. Gustin JA, Korgaonkar CK, Pincheira R, Li Q, Donner DB. 2006. Akt regulates basal and induced processing of NF-kappaB2 (p100) to p52. J Biol Chem 281:16473-16481.
27. Hacker H, Karin M. 2006. Regulation and function of IKK and IKK-related kinases. Sci STKE 2006:re13.
28. Ito W, Kanehiro A, Matsumoto K, Hirano A, Ono K, Maruyama H, Kataoka M, Nakamura T, Gelfand EW, Tanimoto M. 2005. Hepatocyte growth factor attenuates airway hyperresponsiveness, inflammation, and remodeling. Am J Respir Cell Mol Biol 32:268-280.
29. Kawaida K, Matsumoto K, Shimazu H, Nakamura T. 1994. Hepatocyte growth factor prevents acute renal failure and accelerates renal regeneration in mice. Proc Natl Acad Sci USA 91:4357-4361.
30. Khwaja A, Lehmann K, Marte BM, Downward J. 1998. Phosphoinositide 3-kinase induces scattering and tubulogenesis in epithelial cells through a novel pathway. J Biol Chem 273:18793-18801.
31. Krikos A, Laherty CD, Dixit VM. 1992. Transcriptional activation of the TNFα-inducible zinc finger protein, A20, is mediated by κB elements. J Biol Chem 267:17971-17976.
32. Kroening S, Neubauer E, Wullich B, Aten J, Goppelt-Struebe M. 2010. Characterization of connective tissue growth factor expression in primary cultures of human tubular epithelial cells: Modulation by hypoxia. Am J Physiol Renal Physiol 298:F796-F806.
33. Kunter U, Daniel S, Arvelo MB, Choi J, Shukri T, Patel VI, Longo CR, Scali ST, Shrikhande G, Rocha E, Czismadia E, Mottley C, Grey ST, Floege J, Ferran C. 2005. Combined expression of A1 and A20 achieves optimal protection of renal proximal tubular epithelial cells. Kidney Int 68:1520-1532.
34. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
35. Laherty CD, Hu HM, Opipari AW, Wang F, Dixit VM. 1992. The Epstein-Barr virus LMP1 gene product induces A20 zinc finger protein expression by activating NF-κB. J Biol Chem 267:24157-24160.
36. Laherty CD, Perkins ND, Dixit VM. 1993. Human T cell leukemia virus type I Tax and phorbol 12-myristate 13-acetate induce expression of the A20 zinc finger protein by distinct mechanisms involving nuclear factor κB. J Biol Chem 268:5032-5039.
37. Lawrence T. 2009. The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol 1:a001651.
38. Lawrence T, Fong C. 2010. The resolution of inflammation: Anti-inflammatory roles for NF-kappaB. Int J Biochem Cell Biol 42:519-523.
39. Lee EG, Boone DL, Chai S, Libby SL, Chien M, Lodolce JP, Ma A. 2000. Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science 289:2350-2354.
40. Lee HT, Kim M, Jan M, Emala CW. 2006. Anti-inflammatory and antinecrotic effects of the volatile anesthetic sevoflurane in kidney proximal tubule cells. Am J Physiol Renal Physiol 291:F67-F78.
41. Leroy C, Deheuninck J, Reveneau S, Foveau B, Ji Z, Villenet C, Quief S, Tulasne D, Kerckaert JP, Fafeur V. 2006. HGF/SF regulates expression of apoptotic genes in MCF-10A human mammary epithelial cells. Ann N Y Acad Sci 1090:188-202.
42. Linas SL, Shanley PF, Whittenburg D, Berger E, Repine JE. 1988. Neutrophils accentuate ischemia-reperfusion injury in isolated perfused rat kidneys. Am J Physiol 255:F728-F735.
43. Liu Y. 1999. Hepatocyte growth factor promotes renal epithelial cell survival by dual mechanisms. Am J Physiol 277:F624-F633.
44. Liu Y. 2002. Hepatocyte growth factor and the kidney. Curr Opin Nephrol Hypertens 11:23-30.
45. Longo CR, Arvelo MB, Patel VI, Daniel S, Mahiou J, Grey ST, Ferran C. 2003. A20 protects from CD40-CD40 ligand-mediated endothelial cell activation and apoptosis. Circulation 108:1113-1118.
46. Lutz J, Luong le A, Strobl M, Deng M, Huang H, Anton M, Zakkar M, Enesa K, Chaudhury H, Haskard DO, Baumann M, Boyle J, Harten S, Maxwell PH, Pusey C, Heemann U, Evans PC. 2008. The A20 gene protects kidneys from ischaemia/reperfusion injury by suppressing pro-inflammatory activation. J Mol Med 86:1329-1339.
47. Marienfeld R, Berberich-Siebelt F, Berberich I, Denk A, Serfling E, Neumann M. 2001. Signal-specific and phosphorylation-dependent RelB degradation: A potential mechanism of NF-kappaB control. Oncogene 20:8142-8147.
48. Matsumoto K, Nakamura T. 1996. Emerging multipotent aspects of hepatocyte growth factor. J Biochem 119:591-600.
49. Matsumoto K, Nakamura T. 2001. Hepatocyte growth factor: Renotropic role and potential therapeutics for renal diseases. Kidney Int 59:2023-2038.
50. Matthews N, Neale ML, Jackson SK, Stark JM. 1987. Tumour cell killing by tumour necrosis factor: Inhibition by anaerobic conditions, free-radical scavengers and inhibitors of arachidonate metabolism. Immunology 62:153-155.
51. Miller SB, Martin DR, Kissane J, Hammerman MR. 1994. Hepatocyte growth factor accelerates recovery from acute ischemic renal injury in rats. Am J Physiol 266:F129-F134.
52. Min JK, Lee YM, Kim JH, Kim YM, Kim SW, Lee SY, Gho YS, Oh GT, Kwon YG. 2005. Hepatocyte growth factor suppresses vascular endothelial growth factor-induced expression of endothelial ICAM-1 and VCAM-1 by inhibiting the nuclear factor-kappaB pathway. Circ Res 96:300-307.
53. Mizuno S, Matsumoto K, Nakamura T. 2001. Hepatocyte growth factor suppresses interstitial fibrosis in a mouse model of obstructive nephropathy. Kidney Int 59:1304-1314.
54. Mizuno S, Nakamura T. 2004. Suppressions of chronic glomerular injuries and TGF-beta 1 production by HGF in attenuation of murine diabetic nephropathy. Am J Physiol Renal Physiol 286:F134-F143.
55. Muller M, Morotti A, Ponzetto C. 2002. Activation of NF-kappaB is essential for hepatocyte growth factor-mediated proliferation and tubulogenesis. Mol Cell Biol 22:1060-1072.
56. Nakagami H, Morishita R, Yamamoto K, Taniyama Y, Aoki M, Matsumoto K, Nakamura T, Kaneda Y, Horiuchi M, Ogihara T. 2001. Mitogenic and antiapoptotic actions of hepatocyte growth factor through ERK, STAT3, and AKT in endothelial cells. Hypertension 37:581-586.
57. Nakamura Y, Morishita R, Higaki J, Kida I, Aoki M, Moriguchi A, Yamada K, Hayashi S, Yo Y, Matsumoto K., et al. 1995. Expression of local hepatocyte growth factor system in vascular tissues. Biochem Biophys Res Commun 215:483-488.
58. National Institutes of Health 2002. Assessment of adenoviral vector safety and toxicity: Report of the National Institutes of Health Recombinant DNA Advisory Committee. Hum Gene Ther 13:3-13.
59. Ohda Y, Hori K, Tomita T, Hida N, Kosaka T, Fukuda Y, Miwa H, Matsumoto T. 2005. Effects of hepatocyte growth factor on rat inflammatory bowel disease models. Dig Dis Sci 50:914-921.
60. Opipari AJ, Boguski MS, Dixit VM. 1990. The A20 cDNA induced by tumor necrosis factor alpha encodes a novel type of zinc finger protein. J Biol Chem 265:14705-14708.
61. Opipari AJ, Hu HM, Yabkowitz R, Dixit VM. 1992. The A20 zinc finger protein protects cells from TNF cytotoxicity. J Biol Chem 267:12424-12427.
62. Ozes ON, Mayo LD, Gustin JA, Pfeffer SR, Pfeffer LM, Donner DB. 1999. NF-kappaB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 401:82-85.
63. Pasparakis M. 2009. Regulation of tissue homeostasis by NF-kappaB signalling: Implications for inflammatory diseases. Nat Rev Immunol 9:778-788.
64. Patel VI, Daniel S, Longo CR, Shrikhande GV, Scali ST, Czismadia E, Groft CM, Shukri T, Motley-Dore C, Ramsey HE, Fisher MD, Grey ST, Arvelo MB, Ferran C. 2006. A20, a modulator of smooth muscle cell proliferation and apoptosis, prevents and induces regression of neointimal hyperplasia. FASEB J 20:1418-1430.
65. Remuzzi G, Bertani T. 1998. Pathophysiology of progressive nephropathies. N Engl J Med 339:1448-1456.
66. Remuzzi G, Ruggenenti P, Benigni A. 1997. Understanding the nature of renal disease progression. Kidney Int 51:2-15.
67. Robertson H, Kirby JA. 2003. Post-transplant renal tubulitis: The recruitment, differentiation and persistence of intra-epithelial T cells. Am J Transplant 3:3-10.
68. Romashkova JA, Makarov S. 1999. NF-κB is a target of AKT in anti-apoptotic PDGF signalling. Nature 401:86-89.
69. Rubin JS, Chan AM, Bottaro DP, Burgess WH, Taylor WG, Cech AC, Hirschfield DW, Wong J, Miki T, Finch PW., et al. 1991. A broad-spectrum human lung fibroblast-derived mitogen is a variant of hepatocyte growth factor. Proc Natl Acad Sci USA 88:415-419.
70. Sanes JR, Rubenstein JL, Nicolas JF. 1986. Use of a recombinant retrovirus to study post-implantation cell lineage in mouse embryos. EMBO J 5:3133-3142.
71. Scheidereit C. 2006. IkappaB kinase complexes: Gateways to NF-kappaB activation and transcription. Oncogene 25:6685-6705.
72. Segerer S, Nelson PJ, Schlondorff D. 2000. Chemokines, chemokine receptors, and renal disease: From basic science to pathophysiologic and therapeutic studies. J Am Soc Nephrol 11:152-176.
73. Shigematsu H, Yasuda K, Iwai T, Sasajima T, Ishimaru S, Ohashi Y, Yamaguchi T, Ogihara T, Morishita R. 2010. Randomized, double-blind, placebo-controlled clinical trial of hepatocyte growth factor plasmid for critical limb ischemia. Gene Ther 17:1152-1161.
74. Sizemore N, Leung S, Stark GR. 1999. Activation of phosphatidylinositol 3-kinase in response to interleukin-1 leads to phosphorylation and activation of the NF-kappaB p65/RelA subunit. Mol Cell Biol 19:4798-4805.
75. Suzuki A, Hayashida M, Kawano H, Sugimoto K, Nakano T, Shiraki K. 2000. Hepatocyte growth factor promotes cell survival from fas-mediated cell death in hepatocellular carcinoma cells via Akt activation and Fas-death-inducing signaling complex suppression. Hepatology 32:796-802.
76. Tamada S, Nakatani T, Asai T, Tashiro K, Komiya T, Sumi T, Okamura M, Kim S, Iwao H, Kishimoto T, Yamanaka S, Miura K. 2003. Inhibition of nuclear factor-kappaB activation by pyrrolidine dithiocarbamate prevents chronic FK506 nephropathy. Kidney Int 63:306-314.
77. Tashiro K, Tamada S, Kuwabara N, Komiya T, Takekida K, Asai T, Iwao H, Sugimura K, Matsumura Y, Takaoka M, Nakatani T, Miura K. 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.
78. Thompson JE, Phillips RJ, Erdjument-Bromage H, Tempst P, Ghosh S. 1995. I kappa B-beta regulates the persistent response in a biphasic activation of NF-kappa B. Cell 80:573-582.
79. van Kooten C, Daha MR, van Es LA. 1999. Tubular epithelial cells: A critical cell type in the regulation of renal inflammatory processes. Exp Nephrol 7:429-437.
80. Vielhauer V, Berning E, Eis V, Kretzler M, Segerer S, Strutz F, Horuk R, Grone HJ, Schlondorff D, Anders HJ. 2004. CCR1 blockade reduces interstitial inflammation and fibrosis in mice with glomerulosclerosis and nephrotic syndrome. Kidney Int 66:2264-2278.
81. Wrighton CJ, Hofer-Warbinek R, Moll T, Eytner R, Bach FH, de Martin R. 1996. Inhibition of endothelial cell activation by adenovirus-mediated expression of I kappa B alpha, an inhibitor of the transcription factor NF-kappa B. J Exp Med 183:1013-1022.
82. Yamada YIaK. 2005. HGF gene transfer increases kidney graft survival. Kidney International 68:1971-1972.
83. Zhang J, Yang J, Liu Y. 2008. Role of Bcl-xL induction in HGF-mediated renal epithelial cell survival after oxidant stress. Int J Clin Exp Pathol 1:242-253.