Vitreous induces heme oxygenase-1 expression mediated by transforming growth factor-β and reactive oxygen species generation in human retinal pigment epithelial cells

Molecular Vision

Volumn 13, Issue , 2007, Pages 66-78

  Hartung, Ren ^a   Parapuram, Sunil K ^a,c   Ganti, Ramapriya ^a,d   Hunt, D Margaret ^a   Chalam, Kakarla V ^b   Hunt, Richard C ^a  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; 4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; ANTIOXIDANT; HEME OXYGENASE 1; MESSENGER RNA; METALLOTHIONEIN I; METALLOTHIONEIN II; MITOGEN ACTIVATED PROTEIN KINASE P38; NEUTRALIZING ANTIBODY; PROTEIN C FOS; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; TRANSFORMING GROWTH FACTOR BETA;

ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; VITREOUS BODY;

ACTIVIN RECEPTORS, TYPE I; BENZAMIDES; BIOLOGICAL TRANSPORT; CELL NUCLEUS; CELLS, CULTURED; DIOXOLES; ENZYME ACTIVATION; HEME OXYGENASE-1; HUMANS; METALLOTHIONEIN; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PIGMENT EPITHELIUM OF EYE; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS C-FOS; REACTIVE OXYGEN SPECIES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1; TRANSFORMING GROWTH FACTOR BETA; VITREOUS BODY;

EID: 33846531770     PISSN: None     EISSN: 10900535     Source Type: Journal    
DOI: None     Document Type: Article

References (89)

1. Strauss O. The retinal pigment epithelium in visual function. Physiol Rev 2005; 85:845-81.
2. Campochiaro P.A. Pathogenesis of proliferative vitreoretinopathy. In: Wilkinson CP, ed. Ryan, SJ. series ed. Retina 3rd edition. Volume 3. St Louis: Mosby; 2001; 2221-27
3. Pastor JC. Proliferative vitreoretinopathy: an overview. Surv Ophthalmol 1998; 43:3-18.
4. Nagasaki H, Shinagawa K, Mochizuki M. Risk factors for proliferative vitreoretinopathy. Prog Retin Eye Res 1998; 17:77-98.
5. Campochiaro PA. Pathogenic mechanisms in proliferative vitreoretinopathy. Arch Ophthalmol 1997; 115:237-41.
6. Fan W, Zheng JJ, Peiper SC, McLaughlin BJ. Changes in gene expression of ARPE-19 cells in response to vitreous treatment. Ophthalmic Res 2002; 34:357-65.
7. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 2006; 86:583-650.
8. Kutty RK, Nagineni CN, Kutty G, Hooks JJ, Chader GJ, Wiggert B. Increased expression of heme oxygenase-1 in human retinal pigment epithelial cells by transforming growth factor-beta. J Cell Physiol 1994; 159:371-8.
9. Chen W, Hunt DM, Lu H, Hunt RC. Expression of anti-oxidant protective proteins in the rat retina during prenatal and postnatal development. Invest Ophthalmol Vis Sci 1999; 40:744-51.
10. Udono-Fujimori R, Takahashi K, Takeda K, Furuyama K, Kaneko K, Takahashi S, Tamai M, Shibahara S. Expression of heme oxygenase-1 is repressed by interferon-gamma and induced by hypoxia in human retinal pigment epithelial cells. Eur J Biochem 2004; 271:3076-84.
11. Miyamura N, Ogawa T, Boylan S, Morse LS, Handa JT, Hjelmeland LM. Topographic and age-dependent expression of heme oxygenase-1 and catalase in the human retinal pigment epithelium. Invest Ophthalmol Vis Sci 2004; 45:1562-5.
12. Hunt RC, Handy I, Smith A. Heme-mediated reactive oxygen species toxicity to retinal pigment epithelial cells is reduced by hemopexin. J Cell Physiol 1996; 168:81-6.
13. Vasak M. Advances in metallothionein structure and functions. J Trace Elem Med Biol 2005; 19:13-7.
14. Lu H, Hunt DM, Ganti R, Davis A, Dutt K, Alam J, Hunt RC. Metallothionein protects retinal pigment epithelial cells against apoptosis and oxidative stress. Exp Eye Res 2002; 74:83-92.
15. Saika S. TGFbeta pathobiology in the eye. Lab Invest 2006; 86:106-15.
16. Aggeli IK, Gaitanaki C, Beis I. Involvement of JNKs and p38-MAPK/MSK1 pathways in H2O2-induced upregulation of heme oxygenase-1 mRNA in H9c2 cells. Cell Signal 2006; 18:1801-12.
17. Lu TH, Shan Y, Pepe J, Lambrecht RW, Bonkovsky HL. Upstream regulatory elements in chick heme oxygenase-1 promoter: a study in primary cultures of chick embryo liver cells. Mol Cell Biochem 2000; 209:17-27.
18. Lee PJ, Camhi SL, Chin BY, Alam J, Choi AM. AP-1 and STAT mediate hyperoxia-induced gene transcription of heme oxygenase-1. Am J Physiol Lung Cell Mol Physiol 2000; 279:L175-82.
19. Yu CW, Lin LY. Cloning and characterization of the 5′-flanking region of metallothionein-I gene from Chinese hamster ovary cells. Biochim Biophys Acta 1995; 1262:150-4.
20. Tang CM, Westling J, Seto E. trans repression of the human metallothionein IIA gene promoter by PZ120, a novel 120-kilodalton zinc finger protein. Mol Cell Biol 1999; 19:680-9.
21. Parapuram SK, Ganti R, Hunt RC, Hunt DM. Vitreous induces components of the prostaglandin E2 pathway in human retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 2003; 44:1767-74.
22. Davis AA, Bernstein PS, Bok D, Turner J, Nachtigal M, Hunt RC. A human retinal pigment epithelial cell line that retains epithelial characteristics after prolonged culture. Invest Ophthalmol Vis Sci 1995; 36:955-64.
23. Hunt RC, Davis AA. Altered expression of keratin and vimentin in human retinal pigment epithelial cells in vivo and in vitro. J Cell Physiol 1990; 145:187-99.
24. Hunt RC, Dewey A, Davis AA. Transferrin receptors on the surfaces of retinal pigment epithelial cells are associated with the cytoskeleton. J Cell Sci 1989; 92:655-66.
25. Laping NJ, Grygielko E, Mathur A, Butter S, Bomberger J, Tweed C, Martin W, Fornwald J, Lehr R, Harling J, Gaster L, Callahan JF, Olson BA. Inhibition of transforming growth factor (TGF)-beta1-induced extracellular matrix with a novel inhibitor of the TGF-beta type I receptor kinase activity: SB-431542. Mol Pharmacol 2002; 62:58-64.
26. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001; 29:e45.
27. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002; 30:e36.
28. 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) 2005; 51:357-62.
29. Ning W, Song R, Li C, Park E, Mohsenin A, Choi AM, Choi ME. TGF-beta1 stimulates HO-1 via the p38 mitogen-activated protein kinase in A549 pulmonary epithelial cells. Am J Physiol Lung Cell Mol Physiol 2002; 283:L1094-102.
30. 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 2000; 275:40904-9.
31. Hu T, Ramachandrarao SP, Siva S, Valancius C, Zhu Y, Mahadev K, Toh I, Goldstein BJ, Woolkalis M, Sharma K. Reactive oxygen species production via NADPH oxidase mediates TGF-beta-induced cytoskeletal alterations in endothelial cells. Am J Physiol Renal Physiol 2005; 289:F816-25.
32. Liu RM, Liu Y, Forman HJ, Olman M, Tarpey MM. Glutathione regulates transforming growth factor-beta-stimulated collagen production in fibroblasts. Am J Physiol Lung Cell Mol Physiol 2004; 286:L121-8.
33. Lafon C, Mathieu C, Guerrin M, Pierre O, Vidal S, Valette A. Transforming growth factor beta 1-induced apoptosis in human ovarian carcinoma cells: protection by the antioxidant N-acetylcysteine and bcl-2. Cell Growth Differ 1996; 7:1095-104.
34. Li WQ, Qureshi HY, Liacini A, Dehnade F, Zafarullah M. Transforming growth factor Beta1 induction of tissue inhibitor of metalloproteinases 3 in articular chondrocytes is mediated by reactive oxygen species. Free Radic Biol Med 2004; 37:196-207.
35. Meurer SK, Lahme B, Tihaa L, Weiskirchen R, Gressner AM. N-acetyl-L-cysteine suppresses TGF-beta signaling at distinct molecular steps: the biochemical and biological efficacy of a multifunctional, antifibrotic drug. Biochem Pharmacol 2005; 70:1026-34.
36. Moustakas A, Heldin CH. Non-Smad TGF-beta signals. J Cell Sci 2005; 118:3573-84.
37. Cuenda A, Rouse J, Doza YN, Meier R, Cohen P, Gallagher TF, Young PR, Lee JC. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett 1995; 364:229-33.
38. Correze C, Blondeau JP, Pomerance M. p38 mitogen-activated protein kinase contributes to cell cycle regulation by cAMP in FRTL-5 thyroid cells. Eur J Endocrinol 2005; 153:123-33.
39. Hall MC, Young DA, Waters JG, Rowan AD, Chantry A, Edwards DR, Clark IM. The comparative role of activator protein 1 and Smad factors in the regulation of Timp-1 and MMP-1 gene expression by transforming growth factor-beta 1. J Biol Chem 2003; 278:10304-13.
40. Zhang Y, Feng XH, Derynck R. Smad3 and Smad4 cooperate with c-Jun/c-Fos to mediate TGF-beta-induced transcription. Nature 1998; 394:909-13.
41. Derynck R, Zhang YE. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 2003; 425:577-84.
42. Lavrovsky Y, Schwartzman ML, Levere RD, Kappas A, Abraham NG. Identification of binding sites for transcription factors NF-kappa B and AP-2 in the promoter region of the human heme oxygenase 1 gene. Proc Natl Acad Sci U S A 1994; 91:5987-91.
43. Yang G, Shegog ML, Dennery PA. Effect of glutathione on lung activator protein-1 activation and heme oxygenase-1 induction in the immature rat. Pediatr Res 2002; 52:34-9.
44. Lee PJ, Alam J, Sylvester SL, Inamdar N, Otterbein L, Choi AM. Regulation of heme oxygenase-1 expression in vivo and in vitro in hyperoxic lung injury. Am J Respir Cell Mol Biol 1996; 14:556-68.
45. Hess J, Angel P, Schorpp-Kistner M. AP-1 subunits: quarrel and harmony among siblings. J Cell Sci 2004; 117:5965-73.
46. Wisdom R. AP-1: one switch for many signals. Exp Cell Res 1999; 253:180-5.
47. Assoian RK. Common sense signalling. Nat Cell Biol 2002; 4:E187-8.
48. Vidaurri-Leal J, Hohman R, Glaser BM. Effect of vitreous on morphologic characteristics of retinal pigment epithelial cells. A new approach to the study of proliferative vitreoretinopathy. Arch Ophthalmol 1984; 102:1220-3.
49. Grisanti S, Guidry C. Transdifferentiation of retinal pigment epithelial cells from epithelial to mesenchymal phenotype. Invest Ophthalmol Vis Sci 1995; 36:391-405.
50. Pastor JC, de la Rua ER, Martin F. Proliferative vitreoretinopathy: risk factors and pathobiology. Prog Retin Eye Res 2002; 21:127-44.
51. Willoughby DA, Moore AR, Colville-Nash PR, Gilroy D. Resolution of inflammation. Int J Immunopharmacol 2000; 22:1131-5.
52. Wagener FA, Volk HD, Willis D, Abraham NG, Soares MP, Adema GJ, Figdor CG. Different faces of the heme-heme oxygenase system in inflammation. Pharmacol Rev 2003; 55:551-71.
53. Alcaraz MJ, Fernandez P, Guillen MI. Anti-inflammatory actions of the heme oxygenase-1 pathway. Curr Pharm Des 2003; 9:2541-51.
54. Penkowa M. Metallothioneins are multipurpose neuroprotectants during brain pathology. FEBS J 2006; 273:1857-70.
55. Morse D, Pischke SE, Zhou Z, Davis RJ, Flavell RA, Loop T, Otterbein SL, Otterbein LE, Choi AM. Suppression of inflammatory cytokine production by carbon monoxide involves the JNK pathway and AP-1. J Biol Chem 2003; 278:36993-8.
56. Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, Wysk M, Davis RJ, Flavell RA, Choi AM. Carbon monoxide has antiinflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 2000; 6:422-8.
57. Brouard S, Berberat PO, Tobiasch E, Seldon MP, Bach FH, Soares MP. Heme oxygenase-1-derived carbon monoxide requires the activation of transcription factor NF-kappa B to protect endothelial cells from tumor necrosis factor-alpha-mediated apoptosis. J Biol Chem 2002; 277:17950-61.
58. Wesselkamper SC, McDowell SA, Medvedovic M, Dalton TP, Deshmukh HS, Sartor MA, Case LM, Henning LN, Borchers MT, Tomlinson CR, Prows DR, Leikauf GD. The role of metallothionein in the pathogenesis of acute lung injury. Am J Respir Cell Mol Biol 2006; 34:73-82.
59. Inoue K, Takano H, Shimada A, Wada E, Yanagisawa R, Sakurai M, Satoh M, Yoshikawa T. Role of metallothionein in coagulatory disturbance and systemic inflammation induced by lipopolysaccharide in mice. FASEB J 2006; 20:533-5.
60. Rizzardini M, Terao M, Falciani F, Cantoni L. Cytokine induction of haem oxygenase mRNA in mouse liver. Interleukin 1 transcriptionally activates the haem oxygenase gene. Biochem J 1993; 290:343-7.
61. Cantoni L, Rossi C, Rizzardini M, Gadina M, Ghezzi P. Interleukin-1 and tumour necrosis factor induce hepatic haem oxygenase. Feedback regulation by glucocorticoids. Biochem J 1991; 279:891-4.
62. Hanada T, Yoshimura A. Regulation of cytokine signaling and inflammation. Cytokine Growth Factor Rev 2002; 13:413-21.
63. De SK, McMaster MT, Andrews GK. Endotoxin induction of murine metallothionein gene expression. J Biol Chem 1990; 265:15267-74.
64. Thiery JP, Sleeman JP. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 2006; 7:131-42.
65. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003; 113:685-700.
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 2006; 290:L661-L673.
67. Cucoranu I, Clempus R, Dikalova A, Phelan PJ, Ariyan S, Dikalov S, Sorescu D. NAD(P)H oxidase 4 mediates transforming growth factor-beta1-induced differentiation of cardiac fibroblasts into myofibroblasts. Circ Res 2005; 97:900-7.
68. Groth S, Schulze M, Kalthoff H, Fandrich F, Ungefroren H. Adhesion and Rac1-dependent regulation of biglycan gene expression by transforming growth factor-beta. Evidence for oxidative signaling through NADPH oxidase. J Biol Chem 2005; 280:33190-9.
69. Aruoma OI, Halliwell B, Hoey BM, Butler J. The anti-oxidant action of N-acetylcysteine: its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid. Free Radic Biol Med 1989; 6:593-7.
70. Lourenco R, Camilo ME. Taurine: a conditionally essential amino acid in humans? An overview in health and disease. Nutr Hosp 2002; 17:262-70.
71. Abello PA, Fidler SA, Bulkley GB, Buchman TG. Anti-oxidants modulate induction of programmed endothelial cell death (apoptosis) by endotoxin. Arch Surg 1994; 129:134-40.
72. Massague J. How cells read TGF-beta signals. Nat Rev Mol Cell Biol 2000; 1:169-78.
73. Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K, Cobb MH. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 2001; 22:153-83.
74. Saika S. TGF-beta signal transduction in corneal wound healing as a therapeutic target. Cornea 2004; 23:S25-30.
75. Yu L, Hebert MC, Zhang YE. TGF-beta receptor-activated p38 MAP kinase mediates Smad-independent TGF-beta responses. EMBO J 2002; 21:3749-59.
76. Singh NN, Ramji DP. Transforming growth factor-beta-induced expression of the apolipoprotein E gene requires c-Jun N-terminal kinase, p38 kinase, and casein kinase 2. Arterioscler Thromb Vasc Biol 2006; 26:1323-9.
77. Chen Q, Coffey A, Bourgoin SG, Gadina M. Cytohesin binder and regulator augments T cell receptor-induced nuclear factor of activated T Cells.AP-1 activation through regulation of the JNK pathway. J Biol Chem 2006; 281:19985-94.
78. Whitmarsh AJ, Davis RJ. Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J Mol Med 1996; 74:589-607.
79. Engel ME, McDonnell MA, Law BK, Moses HL. Interdependent SMAD and JNK signaling in transforming growth factor-beta-mediated transcription. J Biol Chem 1999; 274:37413-20.
80. Bennett BL, Satoh Y, Lewis AJ. JNK: a new therapeutic target for diabetes. Curr Opin Pharmacol 2003; 3:420-5.
81. Shen G, Jeong WS, Hu R, Kong AN. Regulation of Nrf2, NF-kappaB, and AP-1 signaling pathways by chemopreventive agents. Antioxid Redox Signal 2005; 7:1648-63.
82. Elbirt KK, Bonkovsky HL. Heme oxygenase: recent advances in understanding its regulation and role. Proc Assoc Am Physicians 1999; 111:438-47.
83. Chan PC, Shiu CK, Wong FW, Wong JK, Lam KL, Chan KM. Common carp metallothionein-1 gene: cDNA cloning, gene structure and expression studies. Biochim Biophys Acta 2004; 1676:162-71.
84. Sciavolino PJ, Vilcek J. Regulation of metallothionein gene expression by TNF-alpha and IFN-beta in human fibroblasts. Cytokine 1995; 7:242-50.
85. Lee W, Haslinger A, Karin M, Tjian R. Activation of transcription by two factors that bind promoter and enhancer sequences of the human metallothionein gene and SV40. Nature 1987; 325:368-72.
86. Lee W, Mitchell P, Tjian R. Purified transcription factor AP-1 interacts with TPA-inducible enhancer elements. Cell 1987; 49:741-52.
87. Terry CM, Clikeman JA, Hoidal JR, Callahan KS. Effect of tumor necrosis factor-alpha and interleukin-1 alpha on heme oxygenase-1 expression in human endothelial cells. Am J Physiol 1998; 274:H883-91.
88. Keeton MR, Curriden SA, van Zonneveld AJ, Loskutoff DJ. Identification of regulatory sequences in the type 1 plasminogen activator inhibitor gene responsive to transforming growth factor beta. J Biol Chem 1991; 266:23048-52.
89. Shih SC, Claffey KP. Role of AP-1 and HIF-1 transcription factors in TGF-beta activation of VEGF expression. Growth Factors 2001; 19:19-34.