NAD(P)H oxidase mediates TGF-β1-induced activation of kidney myofibroblasts

Journal of the American Society of Nephrology

Volumn 21, Issue 1, 2010, Pages 93-102

  Bondi, Corry D ^a   Manickam, Nagaraj ^a   Lee, Duck Yoon ^a   Block, Karen ^a   Gorin, Yves ^a   Abboud, Hanna E ^a,b   Barnes, Jeffrey L ^a,b  

^a Mays Cancer Center at UT Health San Antonio   (United States)

^b SOUTH TEXAS VETERANS HEALTH CARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CELL PROTEIN; DIPHENYLIODONIUM SALT; FN ED A PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SMAD3 PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME SYNTHESIS; IN VITRO STUDY; KIDNEY CELL; MYOFIBROBLAST; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RAT;

EID: 75149174337     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2009020146     Document Type: Article

References (69)

1. Desmouliere A, Darby I, Gabbiani G: Normal and pathologic soft tissue remodeling: Role of the myofibroblast, with special emphasis on liver and kidney fibrosis. Lab Invest 83: 1689-1707, 2003
2. Schnaper HW: Renal fibrosis. Methods Mol Med 117: 45-68, 2005
3. Okuda S, Languino LR, Ruoslahti E, Border WA: Elevated expression of transforming growth factor-beta and proteoglycan production in experimental glomerulonephritis: Possible role in expansion of the mesangial extracellular matrix. J Clin Invest 86: 453-462, 1990
4. Gaedeke J, Peters H, Noble NA, Border WA: Angiotensin II, TGF-beta, and renal fibrosis. Contrib Nephrol 135: 153-160, 2001
5. Sappino A-P, Schurch W, Gabbiani G: Differentiation repertoire of fibroblastic cells: Expression of cytoskeletal proteins as marker of phenotypic modulations. Lab Invest 63: 144-161, 1990
6. Borsi L, Castellani P, Risso AM, Leprini A, Zardi L: Transforming growth factor-β regulates the splicing pattern of fibronectin messenger RNA precursor. FEBS Lett 261: 175-178, 1990
7. Serini G, Bochaton-Piallat M-L, Ropraz P, Geinoz A, Borsi L, Zardi L, Gabbiani G: The fibronectin domain ED-A is crucial for myofibroblastic phenotype induction by transforming growth factor-β1. J Cell Biol 142: 873-881, 1998
8. Serini G, Gabbiani G: Mechanisms of myofibroblast activity and phenotypic modulation. Exp Cell Res 250: 273-283, 1999
9. Desmouliere A, Geinoz A, Gabbiani F, Gabbiani G: Transforming growth factor-β1 induces α-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol 122: 103-111, 1993
10. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA: Myofibroblasts and mechano-regulation of connective tissue remodeling. Nat Rev Mol Cell Biol 3: 349-363, 2002
11. Milani S, Herbst H, Schuppan D, Stein H, Surrenti C: Transforming growth factors β1 and β2 are differentially expressed in fibrotic liver disease. Am J Pathol 139: 1221-1229, 1991
12. Yamamoto T, Nakamura T, Noble NA, Ruoslahti E, Border WA: Expression of transforming growth factor β is elevated in human and experimental diabetic nephropathy. Proc Natl Acad Sci U S A 90: 1814-1818, 1993
13. Zhang H-Y, Gharaee-Kermani M, Zhang K, Karmiol S, Phan SH: Lung fibroblast alpha-smooth muscle actin expression and contractile phenotype in bleomycin-induced pulmonary fibrosis. Am J Pathol 148: 527-537, 1996
14. Barnes JL, Hastings RR, De La Garza MA: Sequential expression of cellular fibronectin by platelets, macrophages, and mesangial cells in proliferative glomerulonephritis. Am J Pathol 145: 585-597, 1994
15. Barnes JL, Torres ES, Mitchell RJ, Peters JH: Expression of alternatively spliced fibronectin variants during remodeling in proliferative glomerulonephritis. Am J Pathol 147: 1361-1371, 1995
16. Barnes VL, Musa J, Mitchell RJ, Barnes JL: Expression of embryonic fibronectin isoform EIIIA parallels α-smooth muscle actin in maturing and diseased kidney. J Histochem Cytochem 47: 787-797, 1999
17. Faulkner JL, Szcykalski LM, Springer F, Barnes JL: Origin of interstitial fibroblasts in an accelerated model of angiotensin II (Ang II)-induced renal fibrosis. Am J Pathol 167: 1193-1205, 2005
18. Taniyama Y, Griendling KK: Reactive oxygen species in the vasculature: Molecular and cellular mechanisms. Hypertension 42: 1075-1081, 2003
19. Rey FE, Pagano PJ: The reactive adventitia: Fibroblast oxidase in vascular function. Arterioscler Thromb Vasc Biol 22: 1962-1971, 2002
20. Lee HB, Yu MR, Yang Y, Jiang Z, Ha H: Reactive oxygen species-regulated signaling pathways in diabetic nephropathy. J Am Soc Nephrol 14[Suppl 3]: S241-S245, 2003
21. Cochrane AL, Ricardo SD: Oxidant stress and regulation of chemokines in the development of renal interstitial fibrosis. Contrib Nephrol 139: 102-119, 2003
22. Gaertner SA, Janssen U, Ostendorf T, Koch KM, Floege J, Gwinner W: Glomerular oxidative and antioxidative systems in experimental mesangioproliferative glomerulonephritis. J Am Soc Nephrol 13: 2930-2937, 2002
23. Budisavljevic MN, Hodge LA, Barber K, Fulmer JR, Durazo-Arvizu RA, Self SE, Kuhlmann M, Raymond JR, Greene EL: Oxidative stress in the pathogenesis of experimental proliferative glomerulonephritis. Am J Physiol 285: F1138-F1148, 2003
24. 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
25. Gorin Y, Block K, Hernandez J, Bhandari B, Wagner B, Barnes JL, Abboud HE: Nox4 NAD(P)H oxidase mediates hypertrophy and fibronectin expression in the diabetic kidney. J Biol Chem 280: 39616-39626, 2005
26. Griendling KK, Ushio-Fukai M: Redox control of vascular smooth muscle proliferation. J Lab Clin Med 132: 9-15, 1998
27. Weber DS, Seshiah PN, Taniyama Y, Griendling KK: Src-dependent migration of vascular smooth muscle cells by PDGF is reactive oxygen species dependent. Circulation 106: S260, 1995
28. Block K, Eid A, Griendling KK, Lee DY, Wittrant Y, Gorin Y: Nox4 NAD(P)H oxidase mediates Src-dependent tyrosine phosphorylation of PDK-1 in response to angiotensin II: Role in mesangial cell hypertrophy and fibronectin expression. J Biol Chem 283: 24061-24076, 2008
29. Griendling KK: Novel NAD(P)H oxidases in the cardiovascular system. Heart 90: 491-493, 2004
30. Lambeth J, Kawahara T, Diebold B: Regulation of Nox and Duox enzymatic activity and expression. Free Radic Biol Med 43: 319-331, 2007
31. Kitada M, Koya D, Sugimoto T, Isono M, Araki S, Kashiwagi A, Haneda M: Translocation of glomerular p47phox and p67phox by protein kinase C-beta activation is required for oxidative stress in diabetic nephropathy. Diabetes 52: 2603-2614, 2003
32. Etoh T, Inoguchi T, Kakimoto M, Sonoda N, Kobayashi K, Kuroda J, Sumimoto H, Nawata H: Increased expression of NAD(P)H oxidase subunits, NOX4 and p22phox, in the kidney of streptozotocin-induced diabetic rats and its reversibility by interventive insulin treatment. Diabetologia 46: 1428-1437, 2003
33. Fujii M, Inoguchi T, Maeda Y, Sasaki S, Sawada F, Saito R, Kobayashi K, Sumimoto H, Takayanagi R: Pitavastatin ameliorates albuminuria and renal mesangial expansion by downregulating NOX4 in db/db mice. Kidney Int 72: 473-480, 2007
34. Weaver M, Liu J, Pimentel D, Reddy DJ, Harding P, Peterson EL, Pagano PJ: Adventitial delivery of dominant-negative p67phox attenuates neointimal hyperplasia of the rat carotid artery. Am J Physiol Heart Circ Physiol 290: H1933-H1941, 2006
35. Pagano PJ, Clark JK, Cifuentes-Pagano ME, Clark SM, Callis GM, Quinn MT: Localization of a constitutively active, phagocyte-like NADPH oxidase in rabbit aortic adventitia: Enhancement by angiotensin II. Proc Natl Acad Sci U S A 94: 14483-14488, 1997
36. Haurani MJ, Cifuentes ME, Shepard AD, Pagano PJ: Nox4 oxidase overexpression specifically decreases endogenous Nox4 mRNA and inhibits angiotensin II-induced adventitial myofibroblast migration. Hypertension 52: 143-149, 2008
37. Lloyd CM, Minto AW, Dorf ME, Proudfoot A, Wells TN, Salant DJ, Gutierrez-Ramos JC: RANTES and monocyte chemoattractant protein-1 (MCP-1) play an important role in the inflammatory phase of crescentic nephritis, but only MCP-1 is involved in crescent formation and interstitial fibrosis. J Exp Med 185: 1371-1380, 1997
38. Wiggins R, Goyal M, Merritt S, Killen PD: Vascular adventitial cell expression of collagen I messenger ribonucleic acid in anti-glomerular basement membrane antibody-induced crescentic nephritis in the rabbit: A cellular source for interstitial collagen synthesis in inflammatory renal disease. Lab Invest 68: 557-565, 1993
39. Lin S-L, Kisseleva T, Brenner DA, Duffield JS: Pericytes and perivascular fibroblasts are the primary source of collagen-producing cells in obstructive fibrosis of the kidney. Am J Pathol 173: 1617-1627, 2008
40. Cucoranu I, Clempus R, Dikalova A, Phelan PJ, Ariyan S, Dikalov S, Sorescu D: NAD(P)H Oxidase 4 mediates transforming growth factor-β-1- induced differentiation of cardiac fibroblasts into myofibroblasts. Circ Res 97: 900-907, 2005
41. Shen WL, Gao PJ, Che ZQ, Ji KD, Yin M, Yan C, Berk BC, Zhu DL: NAD(P)H oxidase-derived reactive oxygen species regulate angiotensin-II induced adventitial fibroblast phenotypic differentiation. Biochem Biophys Res Commun 339: 337-343, 2006
42. Clempus RE, Sorescu D, Dikalova AE, Pounkova L, Jo P, Sorescu GP, Lassegue B, Griendling KK: Nox4 is required for maintenance of the differentiated vascular smooth muscle cell phenotype. Arterioscler Thromb Vasc Biol 27: 42-48, 2007
43. Massague J, Gomis RR: The logic of TGF-beta signaling. FEBS Lett 580: 2811-2820, 2006
44. Attisano L, Wrana JL: Signal transduction by the TGF-beta superfamily. Science 296: 1646-1647, 2002
45. Schnaper HW, Hayashida T, Poncelet AC: It's a Smad world: Regulation of TGF-beta signaling in the kidney. J Am Soc Nephrol 13: 1126-1128, 2002
46. Yue J, Mulder KM: Requirement of Ras/MAPK pathway activation by transforming growth factor beta for transforming growth factor beta 1 production in a Smad-dependent pathway. J Biol Chem 275: 30765-30773, 2000
47. Xie Z, Singh M, Singh K: ERK1/2 and JNKs, but not p38 kinase, are involved in reactive oxygen species-mediated induction of osteopontin gene expression by angiotensin II and interleukin-1 beta in adult rat cardiac fibroblasts. J Cell Physiol 198: 399-407, 2004
48. Frank GD, Eguchi S, Yamakawa T, Tanaka S, Inagami T, Motley ED: Involvement of reactive oxygen species in the activation of tyrosine kinase and extracellular signal-regulated kinase by angiotensin II. Endocrinology 141: 3120-3126, 2000
49. Hanna IR, Hilenski LL, Dikalova A, Taniyama Y, Dikalov S, Lyle A, Quinn MT, Lassegue B, Griendling KK: Functional association of nox1 with p22phox in vascular smooth muscle cells. Free Radic Biol Med 37: 1542-1549, 2004
50. Dhaunsi GS, Paintlia MK, Kaur J, Turner RB: NADPH oxidase in human lung fibroblasts. J Biomed Sci 11: 617-622, 2004
51. Colston JT, de la Rosa SD, Strader JR, Anderson MA, Freeman GL: H2O2 activates Nox4 through PLA2-dependent arachidonic acid production in adult cardiac fibroblasts. FEBS Lett 579: 2533-2540, 2005
52. Griendling KK: NADPH oxidases: New regulators of old functions. Antioxid Redox Signal 8: 1443-1445, 2006
53. Ritsick DR, Edens WA, Finnerty V, Lambeth JD: Nox regulation of smooth muscle contraction. Free Radic Biol Med 43: 31-38, 2007
54. Moldovan L, Mythreye K, Goldschmidt-Clermont PJ, Satterwhite L: Reactive oxygen species in vascular endothelial cell motility: Roles of NAD(P)H oxidase and Rac1. Cardiovasc Res 71: 236-246, 2006
55. Hilenski LL, Clempus RE, Quinn MT, Lambeth JD, Griendling KK: Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 24: 677-683, 2004
56. Szocs K, Lassegue B, Sorescu D, Hilenski LL, Valppu L, Couse TL, Wilcox JN, Quinn MT, Lambeth JD, Griendling KK: Upregulation of Nox-based NAD(P)H oxidases in restenosis after carotid injury. Arterioscler Thromb Vasc Biol 22: 21-27, 2002
57. Griendling KK, Ushio-Fukai M: Reactive oxygen species as mediators of angiotensin II signaling. Regul Pept 91: 21-27, 2000
58. Sauer H, Wartenberg M, Hescheler J: Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell Physiol Biochem 11: 173-186, 2001
59. Seshiah PN, Weber DS, Rocic P, Valppu L, Taniyama Y, Griendling KK: Angiotensin II stimulation of NAD(P)H oxidase activity: Upstream mediators. Circ Res 91: 406-413, 2002
60. Guyton KZ, Liu Y, Gorospe M, Xu Q, Holbrook NJ: Activation of mitogen-activated protein kinase by H2O2: Role in cell survival following oxidant injury. J Biol Chem 271: 4138-4142, 1996
61. Kim YK, Bae GU, Kang JK, Park JW, Lee EK, Lee HY, Choi WS, Lee HW, Han JW: Cooperation of H2O2-mediated ERK activation with Smad pathway in TGF-beta1 induction of p21WAF1/Cip1. Cell Signal 18: 236-243, 2006
62. Hayama M, Inoue R, Akiba S, Sato T: ERK and p38 MAP kinase are involved in arachidonic acid release induced by H(2)O(2) and PDGF in mesangial cells. Am J Physiol Renal Physiol 282: F485-F491, 2002
63. Adachi T, Togashi H, Suzuki A, Kasai S, Ito J, Sugahara K, Kawata S: NAD(P)H oxidase plays a crucial role in PDGF-induced proliferation of hepatic stellate cells. Hepatology 41: 1272-1281, 2005
64. Gorin Y, Ricono JM, Kim NH, Bhandari B, Choudhury GG, Abboud HE: Nox4 mediates angiotensin II-induced activation of Akt/protein kinase B in mesangial cells. Am J Physiol Renal Physiol 285: F219-F229, 2003
65. Gorin Y, Ricono JM, Wagner B, Kim NH, Bhandari B, Choudhury GG, Abboud HE: Angiotensin II-induced ERK1/ERK2 activation and protein synthesis are redox-dependent in glomerular mesangial cells. Biochem J 381: 231-239, 2004
66. Sturrock A, Cahill B, Norman K, Huecksteadt TP, Hill K, Sanders K, Karwande SV, Stringham JC, Bull DA, Gleich M, Kennedy TP, Hoidal JR: Transforming growth factor-beta1 induces Nox4 NAD(P)H oxidase and reactive oxygen species-dependent proliferation in human pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 290: L673, 2006
67. Isono M, Chen S, Hong SW, Iglesias-de la Cruz MC, Ziyadeh FN: Smad pathway is activated in the diabetic mouse kidney and Smad3 mediates TGF-beta-induced fibronectin in mesangial cells. Biochem Biophys Res Commun 296: 1356-1365, 2002
68. Fujimoto M, Maezawa Y, Yokote K, Joh K, Kobayashi K, Kawamura H, Nishimura M, Roberts AB, Saito Y, Mori S: Mice lacking Smad3 are protected against streptozotocin-induced diabetic glomerulopathy. Biochem Biophys Res Commun 305: 1002-1007, 2003
69. Rodriguez-Pena AB, Grande MT, Eleno N, Arevalo M, Guerrero C, Santos E, Lopez-Novoa JM: Activation of Erk1/2 and Akt following unilateral ureteral obstruction. Kidney Int 74: 196-209, 2008