Halofuginone inhibition of COL1A2 promoter activity via a c-Jun-dependent mechanism

Arthritis and Rheumatism

Volumn 46, Issue 10, 2002, Pages 2748-2761

  McGaha, Tracy L ^c   Kodera, Takao ^c   Spiera, Harry ^c   Stan, Alexandru C ^a   Pines, Mark ^b   Bona, Constantin A ^c  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b VOLCANI CENTER   (Israel)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; HALOFUGINONE; LUCIFERASE; MESSENGER RNA; MITOGENIC AGENT; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 1; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; FIBROBLAST; GEL MOBILITY SHIFT ASSAY; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; NORTHERN BLOTTING; ONCOGENE C FOS; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION; SKIN FIBROSIS; SKINFOLD THICKNESS; WESTERN BLOTTING;

ADMINISTRATION, TOPICAL; ANIMALS; CELLS, CULTURED; COLLAGEN; DRUG SYNERGISM; FIBROBLASTS; GENE EXPRESSION; MALE; MICE; MICE, MUTANT STRAINS; MITOGENS; PHOSPHORYLATION; PIPERIDINES; PROMOTER REGIONS (GENETICS); PROTEIN SYNTHESIS INHIBITORS; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-JUN; QUINAZOLINES; QUINAZOLINONES; RNA, MESSENGER; SCLERODERMA, SYSTEMIC; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTOR AP-1; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1;

EID: 0036822655     PISSN: 00043591     EISSN: None     Source Type: Journal    
DOI: 10.1002/art.10549     Document Type: Article

References (62)

1. Martin P. Wound healing: aiming for perfect skin regeneration. Science 1997;276:75-81.
2. Steen VD. Clinical manifestations of systemic sclerosis. Semin Cutan Med Surgery 1998;17:48-54.
3. Gharaee-Kermani M, Nozaki Y, Hatano K, Phan SH. Lung interleukin-4 gene expression in a murine model for bleomycin-induced pulmonary fibrosis. Cytokine 2001;15:138-47.
4. McCormick LL, Zhang Y, Tootel E, Gilliam AC. Anti-TGF-β treatment prevents skin and lung fibrosis in murine sclerodermatous graft-versus-host disease: a model for human scleroderma. J Immunol 1999;163:5693-9.
5. Mueller R, Krahl T, Sarvetnick N. Pancreatic expression of interleukin-4 abrogates insulitis and autoimmune diabetes in NOD mice. J Exp Med 1999;184:1093-9.
6. Lee CG, Homer RJ, Zhu Z, Lanone S, Wang X, Koteliansky V, et al. Interleukin-13 induces tissue fibrosis by selectively stimulating and activating transforming growth factor β1. J Exp Med 2001;194:809-21.
7. Sakai LY, Keene DR, Engvall E. Fibrillin, a new 350-kD glycoprotein, is a component of extracellular microfibrils. J Cell Biol 1996;103:2499-509.
8. Siracusa LD, McGrath R, Ma O, Moskow JJ, Manne J, Christner PJ, et al. A tandem duplication within the fibrillin 1 gene is associated with the mouse tight skin mutation. Genomic Res 1996;6:300-17.
9. Bona CA, Saito S. Fibrillin-1 protein in tight skin mice and scleroderma. Clin Rev Allergy Immunol 2000;18:119-26.
10. Granot I, Bartov I, Plavnik I, Wax E, Hurwitz S, Pines M. Increased skin tearing in broilers and reduced collagen synthesis in skin in vivo and in vitro in response to the coccidiostat halofuginone. Poult Sci 1991;70:1559-63.
11. Granot I, Halevy O, Hurwitz S, Pines M. Halofuginone: an inhibitor of collagen type I synthesis. Biochem Biophys Acta 1993;1156:107-12.
12. Halevy O, Nagler A, Levi-Schaffer F, Genina O, Pines M. Inhibition of collagen type I synthesis by skin fibroblasts of graft versus host disease and scleroderma patients: effect of halofuginone. Biochem Pharmacol 1996;52:1057-63.
13. Bruck R, Genina O, Aeed H, Alexiev R, Nagler A, Avni Y, et al. Halofuginone to prevent and treat thioacetamide-induced liver fibrosis in rats. Hepatology 2001;33:379-86.
14. Nagler A, Genina O, Lavelin I, Ohana M, Pines M. Halofuginone, an inhibitor of collagen type-I synthesis, prevents postoperative adhesion formation in the rat uterine horn model. Am J Obstet Gynecol 1999;180:558-63.
15. McGaha TL, Phelps RG, Spiera H, Bona C. Halofuginone, an inhibitor of type-I collagen synthesis and skin sclerosis, blocks TGF-β mediated Smad3 activation in fibroblasts. J Invest Dermatol 2002;118:461-70.
16. Pines M, Domb A, Ohana M, Inbar J, Genina O, Alexiev R, et al. Reduction in dermal fibrosis in the tight-skin (Tsk) mouse after local application of halofuginone. Biochem Pharmacol 2001;62:1221-7.
17. Zhang W, Ou J, Ingaki Y, Greenwel P, Ramirez F. Synergistic cooperation between Sp1 and Smad3/Smad4 mediates transforming growth factor β1 stimulation of α2(I)-collagen (COL1A2) transcription. J Biol Chem 2000;275:39237-45.
18. Greenwel P, Inagaki Y, Hu W, Walsh M, Ramirez F. Sp1 is required for the early response of α2(I) collagen to transforming growth factor-β1. J Biol Chem 1997;272:19738-45.
19. Ihn H, LeRoy EC, Trojanowska M. Oncostatin M stimulates transcription of the human α2(I) collagen gene via the Sp1/Sp3-binding site. J Biol Chem 1997;272:24666-72.
20. Ihn H, Tamaki K. Increased phosphorylation of transcription factor Sp1 in scleroderma fibroblasts: association with increased expression of the type I collagen gene. Arthritis Rheum 2000;43:2240-7.
21. Levy MT, Trojanowska M, Reuben A. Oncostatin M: a cytokine upregulated in human cirrhosis, increases collagen production by human hepatic stellate cells. Hepatology 2000;32:218-26.
22. Chung K, Agarwal A, Uitto J, Mauviel A. An AP-1 binding sequence is essential for regulation of the human α2(I) collagen (COL1A2) promoter activity by transforming growth factor-β. J Biol Chem 1996;271:3272-8.
23. Lee H, Klien L, Raser J, Eghbali-Webb M. An activator protein-1 (AP-1) response element on pro-collagen α1(I) collagen gene is necessary for thyroid hormone-induced inhibition of promoter activity in cardiac fibroblasts. J Mol Cell Cardiol 1998;30:2495-506.
24. Slack JL, Parker MI, Bornstein P. Transcriptional repression of the alpha 1(I) collagen gene by ras is mediated in part by an intronic AP1 site. J Cell Biochem 1995;58:380-92.
25. Philips N, Bashey RI, Jimenez SA. Increased α1(I) procollagen gene expression in tight skin (TSK) mice myocardial fibroblasts is due to a reduced interaction of a negative regulatory sequence with AP-1 transcription factor. J Biol Chem 1995;270:9313-21.
26. Fisher GJ, Talwar HS, Lin J, Lin P, McPhillips F, Wang Z, et al. Retinoic acid inhibits induction of c-Jun protein by ultraviolet radiation that occurs subsequent to activation of mitogen-activated protein kinase pathways in human skin in vivo. J Clin Invest 1998;101:1432-40.
27. Fisher GJ, Datta S, Wang Z, Li X, Quan T, Chung JH, et al. c-Jun-dependent inhibition of cutaneous procollagen transcription following ultraviolet irradiation is reversed by all-trans retinoic acid. J Clin Invest 2000;106:663-70.
28. Eickelberg O, Pansky A, Koehler E, Bihl M, Tamm M, Hildebrand P, et al. Molecular mechanisms of TGF-β antagonism by interferon γ and cyclosporine A in lung fibroblasts. FASEB J 2001;15:797-806.
29. Silbiger S, Lei J, Neugarten J. Estradiol suppresses type-I collagen synthesis in mesangial cells via activation of activator protein-1. Kidney Int 1999;55:1268-76.
30. Landschulz WH, Johnson PF, McKnight SL. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science 1988;240:1759-64.
31. Lallemand D, Spyrou G, Yaniv M, Pfarr CM. Variations in Jun and Fos protein expression and AP-1 activity in cycling, resting and stimulated fibroblasts. Oncogene 1997;14:819-30.
32. Kovary K, Bravo R. Existence of different Fos/Jun complexes during the G0-to-G1 transition and during exponential growth in mouse fibroblasts: differential role of Fos proteins. Mol Cell Biol 1992;12:5015-23.
33. Hai T, Curran T. Cross-family dimerization of transcription factors FOS/Jun and ATF/CREB alters DNA binding specificity. Proc Natl Acad Sci U S A 1991;88:3270-4.
34. Zhang Y, Feng X, Derynck R. Smad3 and Smad4 cooperate with c-Jun/c-Fos to mediate TGF-β-induced transcription. Nature 1998;394:909-13.
35. Chinenov Y, Kerppola T. Close encounters of many kinds: Fos-Jun interactions that mediate transcription regulatory specificity. Oncogene 2001;20:2438-52.
36. Funk WD, Pak DT, Karas RH, Wright WE, Shay JW. A transcriptionally active DNA-binding site for human p53 protein complexes. Mol Cell Biol 1992;12:2866-71.
37. Brown PH, Chen TK, Birrer MJ. Mechanism of action of a dominant-negative mutant of c-Jun. Oncogene 1994;9:791-9.
38. Chen S-J, Yuan W, Mori Y, Levenson A, Trojanowska M, Varga J. Stimulation of type-I collagen transcription in human skin fibroblasts by TGF-β: involvement of Smad3. J Invest Dermatol 1999;112:49-57.
39. Chen S-J, Yuan W, Lo S, Trojanowska M, Varga J. Interaction of Smad3 with a proximal smad-binding element of the human α2(I) procollagen gene promoter required for transcriptional activation by TGF-β. J Cell Physiol 2000;183:381-92.
40. Vergeer WP, Sogo JM, Pretorius PJ, de Vries WN. Interaction of Apl, Ap2, and Sp1 with the regulatory regions of the human pro-α1(I) collagen gene. Arch Biochem Biophysics 2000;377:69-79.
41. Verrecchia F, Tacheau C, Schorpp-Kistner M, Angel P, Mauviel A. Induction of the AP-1 members c-Jun and JunB by TGF-β/ Smad suppresses early Smad-driven gene activation. Oncogene 2001;20:2205-11.
42. Saed GM, Ladin D, Olson J. Analysis of p53 gene mutations in keloids using polymerase chain reaction-based single-strand conformational polymorphism and DNA sequencing. Arch Dermatol 1998;134:963-7.
43. Kawakami T, Inh H, Xu W, Smith E, LeRoy C, Trojanowska M. Increased expression of TGF-beta receptors by scleroderma fibroblasts: evidence for contribution of autocrine TGF-beta signaling to scleroderma phenotype. J Invest Dermatol 1998;110:47-51.
44. Sato S, Nagaoka T, Hasegawa M, Tamatani T, Nakanishi T, Takigawa M, et al. Serum levels of connective tissue growth factor are elevated in patients with systemic sclerosis: association with extent of skin sclerosis and severity of pulmonary fibrosis. J Rheumatol 2000;27:149-54.
45. Holmes A, Abraham DJ, Sa S, Shiwen X, Black CM, Leask A. CTGF and Smads, maintenance of scleroderma phenotype is independent of Smad signaling. J Biol Chem 2001;276:10594-601.
46. Salmon-Ehr V, Serpier H, Nawrocki B, Gillery PH, Clavel C, Kalis B, et al. Expression of interleukin-4 in scleroderma skin specimens in fibroblast culture. Arch Dermatol 1996;132:802-6.
47. Serpier H, Gillery PH, Salmon-Ehr V, Garnotel R, Georges N, Kalis B, et al. Antagonistic effects of interferon-γ and interleukin-4 on fibroblast cultures. J Invest Dermatol 1997;109:158-162.
48. Skuballa W, Raduchel B, Vorbruggen H. Chemistry of stable prostacyclin analogs: synthesis of iloprost. In: Gryglewski RG, Stock G, editors. Prostacyclin and its stable analog iloprost. Berlin: Springer-Verlag; 1985. p. 17-24.
49. McHugh NJ, Csuka M, Watson H, Belcher G, Amadi A, Ring EF, et al. Infusion of iloprost, a prostacyclin analog, for treatment of Raynaud's phenomenon in systemic sclerosis. Ann Rheum Dis 1988;47:43-7.
50. Stratton R, Shiwen X, Martini G, Holmes A, Leask A, Haberberger T, et al. Iloprost suppresses connective tissue growth factor production in fibroblasts and in the skin of scleroderma patients. J Clin Invest 2001;108:241-50.
51. Anderson MB, Vaupel MR, Sherwood OD. Pregnant mouse corpora lutea: immunocytochemical localization of relaxin and ultrastructure. Biol Reprod 1984;31:391-7.
52. Vaupel MR, Sherwood OD, Anderson MB. Immunocytochemical studies of relaxin in ovaries of pregnant and cycling mice. J Histochem Cytochem 1985;33:303-8.
53. Unemori EN, Bauer EA, Amento EP. Relaxin alone and in conjunction with interferon-γ decreases collagen synthesis by cultured human scleroderma fibroblasts. J Invest Dermatol 1992;99:337-42.
54. Piccinni M, Bani D, Beloni L, Manuelli C, Mavilia C, Vocioni F, et al. Relaxin favors the development of activated human T cells into Thl-like effectors. Eur J Immunol 1999;29:2241-7.
55. Seibold JR, Clements PJ, Furst DE, Mayes MD, McCloskey DA, Moreland LW, et al. Safety and pharmacokinetics of recombinant human relaxin in systemic sclerosis. J Rheumatol 1997;25:302-7.
56. Underwood DC, Osborn RR, Bochnowicz S, Webb EF, Rieman DJ, Lee JC, et al. SB239063, a p38 MAPK inhibitor, reduces neutrophilia, inflammatory cytokines, MMP-9, and fibrosis in the lung. Am J Physiol Lung Cell Mol Physiol 2000;279:L895-902.
57. Romanelli RG, Caligiuri A, Carloni V, DeFranco R, Montalto P, Ceni E, et al. Effect of pentoxifyllinc on the degradation of procollagen type-I produced by human hepatic stellate cells in response to transforming growth factor-β1. Br J Pharmacol 1997;122:1047-54.
58. Fang C, Yen C, Chen Y, Shyu R, Tsai T, Lee P, et al. Pentoxifylline inhibits human peritoneal mesothelial cell growth and collagen synthesis: effects on TGF-β. Kidney Int 2000;57:2626-33.
59. Elkin M, Ariel H, Miao H, Pines M, de-Groot N, Hochberg A, et al. Inhibition of bladder carcinoma angiogenesis, stromal support, and tumor growth by halofuginone. Cancer Res 1999;59:4111-8.
60. Elkin M, Miao H, Nagler A, Aingorn E, Reich R, Hemo I, et al. Halofuginone: a potent inhibitor of critical steps in angiogenesis progression. FASEB J 2000;14:2477-85.
61. Szabowski A, Maas-Szabowski N, Andrecht S, Kolbus A, Schorpp-Kistner M, Fusenig NE, et al. c-Jun and JunB antagonistically control cytokine-regulated mesenchymal-epidermal interaction in skin. Cell 2000;103:745-55.
62. Dennler S, Prunier C, Ferrand N, Gauthier J, Atfi A. c-Jun inhibits transforming growth factor β-mediated transcription by repressing Smad-3 transcriptional activity. J Biol Chem 2000;275:28858-65.