The inflammatory cytokines TWEAK and TNFα reduce renal klotho expression through NFκB

Journal of the American Society of Nephrology

Volumn 22, Issue 7, 2011, Pages 1315-1325

  Moreno, Juan A ^a   Izquierdo, Maria C ^a   Sanchez Niño, Maria D ^a   Suárez Alvarez, Beatriz ^b   Lopez Larrea, Carlos ^b   Jakubowski, Aniela ^c   Blanco, Julia ^e   Ramirez, Rafael ^d   Selgas, Rafael ^f   Ruiz Ortega, Marta ^a   Egido, Jesus ^a   Ortiz, Alberto ^a   Sanz, Ana B ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b HOSPITAL UNIVERSITARIO CENTRAL DE ASTURIAS   (Spain)

^c BIOGEN   (United States)

^d HOSPITAL CLÍNICO SAN CARLOS   (Spain)

^e HOSPITAL UNIVERSITARIO REINA SOFÍA   (Spain)

^f HOSPITAL UNIVERSITARIO LA PAZ IDIPAZ   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

FOLIC ACID; HISTONE DEACETYLASE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; KLOTHO PROTEIN; PARTHENOLIDE; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR LIKE WEAK INDUCER OF APOPTOSIS; UNCLASSIFIED DRUG;

ACUTE KIDNEY FAILURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DEACETYLATION; DNA BINDING; DOWN REGULATION; GEL MOBILITY SHIFT ASSAY; HISTONE ACETYLATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 79960144041     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2010101073     Document Type: Article

References (62)

1. Remuzzi G, Ruggenenti P, Benigni A: Understanding the nature of renal disease progression. Kidney Int 51: 2-15, 1997
2. Grande MT, Perez-Barriocanal F, Lopez-Novoa JM: Role of inflammation in tubulo-interstitial damage associated to obstructive nephropathy. J Inflamm 7: 19, 2010
3. Locksley RM, Killeen N, Lenardo MJ: The TNF and TNF receptor superfamilies: Integrating mammalian biology. Cell 104: 487-501, 2001
4. Sanz AB, Sanchez-Nino MD, Ramos AM, Moreno JA, Santamaria B, Ruiz-Ortega M, Egido J, Ortiz A: NF-kappaB in renal inflammation. J Am Soc Nephrol 21: 1254-1262, 2010
5. Ortiz A, Bustos C, Alonso J, Alcazar R, Lopez-Armada MJ, Plaza JJ, Gonzalez E, Egido J: Involvement of tumor necrosis factor-alpha in the pathogenesis of experimental and human glomerulonephritis. Adv Nephrol Necker Hosp 24: 53-77, 1995
6. Justo P, Sanz A, Lorz C, Gomez-Garre D, Mezzano S, Egido J, Ortiz A: Expression of Smac/Diablo in tubular epithelial cells and during acute renal failure. Kidney Int Suppl S52-S56, 2003
7. Sanz AB, Justo P, Sanchez-Nino MD, Blanco-Colio LM, Winkles JA, Kreztler M, Jakubowski A, Blanco J, Egido J, Ruiz-Ortega M, Ortiz A: The cytokine TWEAK modulates renal tubulointerstitial inflammation. J Am Soc Nephrol 19: 695-703, 2008
8. Justo P, Sanz AB, Sanchez-Nino MD, Winkles JA, Lorz C, Egido J, Ortiz A: Cytokine cooperation in renal tubular cell injury: The role of TWEAK. Kidney Int 70: 1750-1758, 2006
9. Sanz AB, Sanchez-Nino MD, Izquierdo MC, Jakubowski A, Justo P, Blanco-Colio LM, Ruiz-Ortega M, Selgas R, Egido J, Ortiz A: TWEAK activates the non-canonical NFkappaB pathway in murine renal tubular cells: modulation of CCL21. PLoS One 5: e8955, 2010
10. Ortiz A, Lorz C, Catalan MP, Danoff TM, Yamasaki Y, Egido J, Neilson EG: Expression of apoptosis regulatory proteins in tubular epithelium stressed in culture or following acute renal failure. Kidney Int 57: 969-981, 2000
11. Sanz AB, Santamaria B, Ruiz-Ortega M, Egido J, Ortiz A: Mechanisms of renal apoptosis in health and disease. J Am Soc Nephrol 19: 1634-1642, 2008
12. Munoz-Garcia B, Martin-Ventura JL, Martinez E, Sanchez S, Hernandez G, Ortega L, Ortiz A, Egido J, Blanco-Colio LM: Fn14 is upregulated in cytokine-stimulated vascular smooth muscle cells and is expressed in human carotid atherosclerotic plaques: Modulation by atorvastatin. Stroke 37: 2044-2053, 2006
13. Munoz-Garcia B, Moreno JA, Lopez-Franco O, Sanz AB, Martin-Ventura JL, Blanco J, Jakubowski A, Burkly LC, Ortiz A, Egido J, Blanco-Colio LM: Tumor necrosis factor-like weak inducer of apoptosis (TWEAK) enhances vascular and renal damage induced by hyperlipidemic diet in ApoE-knockout mice. Arterioscler Thromb Vasc Biol 29: 2061-2068, 2009
14. Stenvinkel P, Carrero JJ, Axelsson J, Lindholm B, Heimburger O, Massy Z: Emerging biomarkers for evaluating cardiovascular risk in the chronic kidney disease patient: How do new pieces fit into the uremic puzzle? Clin J Am Soc Nephrol 3: 505-521, 2008
15. Kuro-o M, Matsumura Y, Aizawa H, Kawaguchi H, Suga T, Utsugi T, Ohyama Y, Kurabayashi M, Kaname T, Kume E, Iwasaki H, Iida A, Shiraki-Iida T, Nishikawa S, Nagai R, Nabeshima YI: Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature 390: 45-51, 1997
16. Kurosu H, Yamamoto M, Clark JD, Pastor JV, Nandi A, Gurnani P, McGuinness OP, Chikuda H, Yamaguchi M, Kawaguchi H, Shimomura I, Takayama Y, Herz J, Kahn CR, Rosenblatt KP, Kuro-o M: Suppression of aging in mice by the hormone Klotho. Science 309: 1829-1833, 2005
17. Urakawa I, Yamazaki Y, Shimada T, Iijima K, Hasegawa H, Okawa K, Fujita T, Fukumoto S, Yamashita T: Klotho converts canonical FGF receptor into a specific receptor for FGF23. Nature 444: 770-774, 2006
18. Prie D, Beck L, Urena P, Friedlander G: Recent findings in phosphate homeostasis. Curr Opin Nephrol Hypertens 14: 318-324, 2005
19. Liu H, Fergusson MM, Castilho RM, Liu J, Cao L, Chen J, Malide D, Rovira II, Schimel D, Kuo CJ, Gutkind JS, Hwang PM, Finkel T: Augmented Wnt signaling in a mammalian model of accelerated aging. Science 317: 803-806, 2007
20. Yamamoto M, Clark JD, Pastor JV, Gurnani P, Nandi A, Kurosu H, Miyoshi M, Ogawa Y, Castrillon DH, Rosenblatt KP, Kuro-o M: Regulation of oxidative stress by the anti-aging hormone klotho. J Biol Chem 280: 38029-38034, 2005
21. Aizawa H, Saito Y, Nakamura T, Inoue M, Imanari T, Ohyama Y, Matsumura Y, Masuda H, Oba S, Mise N, Kimura K, Hasegawa A, Kurabayashi M, Kuro-o M, Nabeshima Y, Nagai R: Downregulation of the Klotho gene in the kidney under sustained circulatory stress in rats. Biochem Biophys Res Commun 249: 865-871, 1998
22. Sugiura H, Yoshida T, Tsuchiya K, Mitobe M, Nishimura S, Shirota S, Akiba T, Nihei H: Klotho reduces apoptosis in experimental ischaemic acute renal failure. Nephrol Dial Transplant 20: 2636-2645, 2005
23. Canalejo R, Canalejo A, Martinez-Moreno JM, Rodriguez-Ortiz ME, Estepa JC, Mendoza FJ, Munoz-Castaneda JR, Shalhoub V, Almaden Y, Rodriguez M: FGF23 fails to inhibit uremic parathyroid glands. J Am Soc Nephrol 21: 1125-1135, 2010
24. Koh N, Fujimori T, Nishiguchi S, Tamori A, Shiomi S, Nakatani T, Sugimura K, Kishimoto T, Kinoshita S, Kuroki T, Nabeshima Y: Severely reduced production of klotho in human chronic renal failure kidney. Biochem Biophys Res Commun 280: 1015-1020, 2001
25. Ohyama Y, Kurabayashi M, Masuda H, Nakamura T, Aihara Y, Kaname T, Suga T, Arai M, Aizawa H, Matsumura Y, Kuro-o M, Nabeshima Y, Nagail R: Molecular cloning of rat klotho cDNA: Markedly decreased expression of klotho by acute inflammatory stress. Biochem Biophys Res Commun 251: 920-925, 1998
26. Mitani H, Ishizaka N, Aizawa T, Ohno M, Usui S, Suzuki T, Amaki T, Mori I, Nakamura Y, Sato M, Nangaku M, Hirata Y, Nagai R: In vivo klotho gene transfer ameliorates angiotensin II-induced renal damage. Hypertension 39: 838-843, 2002
27. Narumiya H, Sasaki S, Kuwahara N, Irie H, Kusaba T, Kameyama H, Tamagaki K, Hatta T, Takeda K, Matsubara H: HMG-CoA reductase inhibitors up-regulate anti-aging klotho mRNA via RhoA inactivation in IMCD3 cells. Cardiovasc Res 64: 331-336, 2004
28. Saito K, Ishizaka N, Mitani H, Ohno M, Nagai R: Iron chelation and a free radical scavenger suppress angiotensin II-induced downregulation of klotho, an anti-aging gene, in rat. FEBS Lett 551: 58-62, 2003
29. Mitobe M, Yoshida T, Sugiura H, Shirota S, Tsuchiya K, Nihei H: Oxidative stress decreases klotho expression in a mouse kidney cell line. Nephron Exp Nephrol 101: e67-e74, 2005
30. Ruiz-Ortega M, Lorenzo O, Ruperez M, Konig S, Wittig B, Egido J: Angiotensin II activates nuclear transcription factor kappaB through AT(1) and AT(2) in vascular smooth muscle cells: Molecular mechanisms. Circ Res 86: 1266-1272, 2000
31. Zhang W, Li Q, Wang L, Yang X: Simvastatin ameliorates glomerulosclerosis in Adriamycin-induced-nephropathy rats. Pediatr Nephrol 23: 2185-2194, 2008
32. Meyer-Schwesinger C, Dehde S, von RC, Gatzemeier S, Klug P, Wenzel UO, Stahl RA, Thaiss F, Meyer TN: Rho kinase inhibition attenuates LPS-induced renal failure in mice in part by attenuation of NF-kappaB p65 signaling. Am J Physiol Renal Physiol 296: F1088-F1099, 2009
33. Hoffmann U, Bergler T, Rihm M, Pace C, Kruger B, Rummele P, Stoelcker B, Banas B, Mannel DN, Kramer BK: Upregulation of TNF receptor type 2 in human and experimental renal allograft rejection. Am J Transplant 9: 675-686, 2009
34. Misaki T, Yamamoto T, Suzuki S, Fukasawa H, Togawa A, Ohashi N, Suzuki H, Fujigaki Y, Oda T, Uchida C, Kitagawa K, Hattori T, Kitagawa M, Hishida A: Decrease in tumor necrosis factor-alpha receptor-associated death domain results from ubiquitin-dependent degradation in obstructive renal injury in rats. Am J Pathol 175: 74-83, 2009
35. Sanz AB, Sanchez-Nino MD, Izquierdo MC, Jakubowski A, Justo P, Blanco-Colio LM, Ruiz-Ortega M, Egido J, Ortiz A: Tweak induces proliferation in renal tubular epithelium: A role in uninephrectomy induced renal hyperplasia. J Cell Mol Med 13: 3329-3342, 2009
36. Hehner SP, Hofmann TG, Droge W, Schmitz ML: The antiinflammatory sesquiterpene lactone parthenolide inhibits NF-kappa B by targeting the I kappa B kinase complex. J Immunol 163: 5617-5623, 1999
37. Campbell KJ, Rocha S, Perkins ND: Active repression of antiapoptotic gene expression by RelA(p65) NF-kappa B. Mol Cell 13: 853-865, 2004
38. Ashburner BP, Westerheide SD, Baldwin AS, Jr.: The p65 (RelA) subunit of NF-kappaB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression. Mol Cell Biol 21: 7065-7077, 2001
39. Burkly LC, Michaelson JS, Hahm K, Jakubowski A, Zheng TS: TWEAKing tissue remodeling by a multifunctional cytokine: Role of TWEAK/Fn14 pathway in health and disease. Cytokine 40: 1-16, 2007
40. Carrero JJ, Ortiz A, Qureshi AR, Martin-Ventura JL, Barany P, Heimburger O, Marron B, Metry G, Snaedal S, Lindholm B, Egido J, Stenvinkel P, Blanco-Colio LM: Additive effects of soluble TWEAK and inflammation on mortality in hemodialysis patients. Clin J Am Soc Nephrol 4: 110-118, 2009
41. Kato Y, Arakawa E, Kinoshita S, Shirai A, Furuya A, Yamano K, Nakamura K, Iida A, Anazawa H, Koh N, Iwano A, Imura A, Fujimori T, Kuro-o M, Hanai N, Takeshige K, Nabeshima Y: Establishment of the anti-Klotho monoclonal antibodies and detection of Klotho protein in kidneys. Biochem Biophys Res Commun 267: 597-602, 2000
42. Hu MC, Shi M, Zhang J, Quinones H, Kuro-o M, Moe OW: Klotho deficiency is an early biomarker of renal ischemia-reperfusion injury and its replacement is protective. Kidney Int 78: 1240-1251, 2010
43. Stevens LA, Viswanathan G, Weiner DE: Chronic kidney disease and end-stage renal disease in the elderly population: Current prevalence, future projections, and clinical significance. Adv Chronic Kidney Dis 17: 293-301, 2010
44. Perry VH: Contribution of systemic inflammation to chronic neurodegeneration. Acta Neuropathol 2010
45. Roux C: Osteoporosis in inflammatory joint diseases. Osteoporos Int 22:421-433, 2011
46. Haruna Y, Kashihara N, Satoh M, Tomita N, Namikoshi T, Sasaki T, Fujimori T, Xie P, Kanwar YS: Amelioration of progressive renal injury by genetic manipulation of Klotho gene. Proc Natl Acad Sci U S A 104: 2331-2336, 2007
47. Witkowski JM, Soroczynska-Cybula M, Bryl E, Smolenska Z, Jozwik A: Klotho - a common link in physiological and rheumatoid arthritisrelated aging of human CD4+ lymphocytes. J Immunol 178: 771-777, 2007
48. Goodwin BL, Pendleton LC, Levy MM, Solomonson LP, Eichler DC: Tumor necrosis factor-alpha reduces argininosuccinate synthase expression and nitric oxide production in aortic endothelial cells. Am J Physiol Heart Circ Physiol 293: H1115-H1121, 2007
49. Anderson HD, Rahmutula D, Gardner DG: Tumor necrosis factor-alpha inhibits endothelial nitric-oxide synthase gene promoter activity in bovine aortic endothelial cells. J Biol Chem 279: 963-969, 2004
50. Zhu NL, Li C, Huang HH, Sebald M, Londhe VA, Heisterkamp N, Warburton D, Bellusci S, Minoo P: TNF-alpha represses transcription of human bone morphogenetic protein-4 in lung epithelial cells. Gene 393: 70-80, 2007
51. Saitoh T, Nakayama M, Nakano H, Yagita H, Yamamoto N, Yamaoka S: TWEAK induces NF-kappaB2 p100 processing and long lasting NF-kappaB activation. J Biol Chem 278: 36005-36012, 2003
52. Natoli G, Saccani S, Bosisio D, Marazzi I: Interactions of NF-kappaB with chromatin: The art of being at the right place at the right time. Nat Immunol 6: 439-445, 2005
53. Aarenstrup L, Flindt EN, Otkjaer K, Kirkegaard M, Andersen JS, Kristiansen K: HDAC activity is required for p65/RelA-dependent repression of PPARdelta-mediated transactivation in human keratinocytes. J Invest Dermatol 128: 1095-1106, 2008
54. Liu MY, Khachigian LM: Histone deacetylase-1 is enriched at the platelet-derived growth factor-D promoter in response to interleukin-1beta and forms a cytokine-inducible gene-silencing complex with NF-kappab p65 and interferon regulatory factor-1. J Biol Chem 284: 35101-35112, 2009
55. Haruna Y, Kashihara N, Satoh M, Tomita N, Namikoshi T, Sasaki T, Fujimori T, Xie P, Kanwar YS: Amelioration of progressive renal injury by genetic manipulation of Klotho gene. Proc Natl Acad Sci U S A 104: 2331-2336, 2007
56. Sugiura H, Yoshida T, Tsuchiya K, Mitobe M, Nishimura S, Shirota S, Akiba T, Nihei H: Klotho reduces apoptosis in experimental ischaemic acute renal failure. Nephrol Dial Transplant 20: 2636-2645, 2005
57. Ortega A, Ramila D, Ardura JA, Esteban V, Ruiz-Ortega M, Barat A, Gazapo R, Bosch RJ, Esbrit P: Role of parathyroid hormone-related protein in tubulointerstitial apoptosis and fibrosis after folic acid-induced nephrotoxicity. J Am Soc Nephrol 17: 1594-1603, 2006
58. Fang TC, Alison MR, Cook HT, Jeffery R, Wright NA, Poulsom R: Proliferation of bone marrow-derived cells contributes to regeneration after folic acid-induced acute tubular injury. J Am Soc Nephrol 16: 1723-1732, 2005
59. Doi K, Okamoto K, Negishi K, Suzuki Y, Nakao A, Fujita T, Toda A, Yokomizo T, Kita Y, Kihara Y, Ishii S, Shimizu T, Noiri E: Attenuation of folic acid-induced renal inflammatory injury in platelet-activating factor receptor-deficient mice. Am J Pathol 168: 1413-1424, 2006
60. Campbell S, Michaelson J, Burkly L, Putterman C: The role of TWEAK/Fn14 in the pathogenesis of inflammation and systemic autoimmunity. Front Biosci 9: 2273-2284, 2004
61. Suarez-Alvarez B, Rodriguez RM, Calvanese V, Blanco-Gelaz MA, Suhr ST, Ortega F, Otero J, Cibelli JB, Moore H, Fraga MF, Lopez-Larrea C: Epigenetic mechanisms regulate MHC and antigen processing molecules in human embryonic and induced pluripotent stem cells. PLoS One 5: e10192, 2010
62. Sanchez-Nino MD, Sanz AB, Lorz C, Gnirke A, Rastaldi MP, Nair V, Egido J, Ruiz-Ortega M, Kretzler M, Ortiz A: BASP1 promotes apoptosis in diabetic nephropathy. J Am Soc Nephrol 21: 610-621, 2010