Antifibrotic Effects of Roscovitine in Normal and Scleroderma Fibroblasts

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Steinman, Richard A ^a   Robinson, Andria Rasile ^a   Feghali Bostwick, Carol A ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; CONNECTIVE TISSUE GROWTH FACTOR; FIBRONECTIN; INTERLEUKIN 6; MATRIX PROTEIN; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; ROSCOVITINE; STAT3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; CASE REPORT; CELL CYCLE ARREST; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG ACTIVITY; FIBROBLAST; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; PROTEIN EXPRESSION; SCLERODERMA; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; COLLAGEN; CONNECTIVE TISSUE GROWTH FACTOR; FIBROBLASTS; FIBRONECTINS; FIBROSIS; HUMANS; INTERLEUKIN-6; MICE; NIH 3T3 CELLS; PHOSPHORYLATION; PURINES; SCLERODERMA, SYSTEMIC; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA; UP-REGULATION;

EID: 84869741998     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048560     Document Type: Article

References (59)

1. Pippin JW, Qu Q, Meijer L, Shankland SJ, (1997) Direct in vivo inhibition of the nuclear cell cycle cascade in experimental mesangial proliferative glomerulonephritis with Roscovitine, a novel cyclin-dependent kinase antagonist. J Clin Invest 100: 2512-2520.
2. Medsger TA Jr, (2003) Natural history of systemic sclerosis and the assessment of disease activity, severity, functional status, and psychologic well-being. Rheum Dis Clin North Am 29: 255-vi, 255-273, vi.
3. Bhattacharyya S, Wei J, Varga J, (2011) Understanding fibrosis in systemic sclerosis: shifting paradigms, emerging opportunities. Nat Rev Rheumatol 8: 42-54.
4. Gruschwitz M, Muller PU, Sepp N, Hofer E, Fontana A, et al. (1990) Transcription and expression of transforming growth factor type beta in the skin of progressive systemic sclerosis: a mediator of fibrosis? J Invest Dermatol 94: 197-203.
5. Hawinkels LJ, Ten Dijke P, (2011) Exploring anti-TGF-beta therapies in cancer and fibrosis. Growth Factors 29: 140-152.
6. Ihn H, (2008) Autocrine TGF-beta signaling in the pathogenesis of systemic sclerosis. J Dermatol Sci 49: 103-113.
7. Houglum K, Buck M, Adir V, Chojkier M, (1994) LAP (NF-IL6) transactivates the collagen alpha 1(I) gene from a 5′ regulatory region. J Clin Invest 94: 808-814.
8. Sato S, Hasegawa M, Takehara K, (2001) Serum levels of interleukin-6 and interleukin-10 correlate with total skin thickness score in patients with systemic sclerosis. J Dermatol Sci 27: 140-146.
9. Denton CP, Merkel PA, Furst DE, Khanna D, Emery P, et al. (2007) Recombinant human anti-transforming growth factor beta1 antibody therapy in systemic sclerosis: a multicenter, randomized, placebo-controlled phase I/II trial of CAT-192. Arthritis Rheum 56: 323-333.
10. Shima Y, Kuwahara Y, Murota H, Kitaba S, Kawai M, et al. (2010) The skin of patients with systemic sclerosis softened during the treatment with anti-IL-6 receptor antibody tocilizumab. Rheumatology (Oxford) 49: 2408-2412.
11. Asano Y, (2010) Future treatments in systemic sclerosis. J Dermatol 37: 54-70.
12. Fu AK, Fu WY, Cheung J, Tsim KW, Ip FC, et al. (2001) Cdk5 is involved in neuregulin-induced AChR expression at the neuromuscular junction. Nat Neurosci 4: 374-381.
13. Lania L, Majello B, Napolitano G, (1999) Transcriptional control by cell-cycle regulators: a review. J Cell Physiol 179: 134-141.
14. Wesierska-Gadek J, Krystof V, (2009) Selective cyclin-dependent kinase inhibitors discriminating between cell cycle and transcriptional kinases: future reality or utopia? Ann N Y Acad Sci 1171: 228-241.
15. Feghali CA, Bost KL, Boulware DW, Levy LS, (1992) Mechanisms of pathogenesis in scleroderma. I. Overproduction of interleukin 6 by fibroblasts cultured from affected skin sites of patients with scleroderma. J Rheumatol 19: 1207-1211.
16. De Azevedo WF, Leclerc S, Meijer L, Havlicek L, Strnad M, et al. (1997) Inhibition of cyclin-dependent kinases by purine analogues: crystal structure of human cdk2 complexed with roscovitine. Eur J Biochem 243: 518-526.
17. Meijer L, Borgne A, Mulner O, Chong JP, Blow JJ, et al. (1997) Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur J Biochem 243: 527-536.
18. Meijer L, Raymond E, (2003) Roscovitine and other purines as kinase inhibitors. From starfish oocytes to clinical trials. Acc Chem Res 36: 417-425.
19. Whittaker SR, Walton MI, Garrett MD, Workman P, (2004) The Cyclin-dependent kinase inhibitor CYC202 (R-roscovitine) inhibits retinoblastoma protein phosphorylation, causes loss of Cyclin D1, and activates the mitogen-activated protein kinase pathway. Cancer Res 64: 262-272.
20. Wesierska-Gadek J, Schmitz ML, Ranftler C, (2007) Roscovitine-activated HIP2 kinase induces phosphorylation of wt p53 at Ser-46 in human MCF-7 breast cancer cells. J Cell Biochem 100: 865-874.
21. Aldoss IT, Tashi T, Ganti AK, (2009) Seliciclib in malignancies. Expert Opin Investig Drugs 18: 1957-1965.
22. Krystof V, Uldrijan S, (2010) Cyclin-dependent kinase inhibitors as anticancer drugs. Curr Drug Targets 11: 291-302.
23. Alessi F, Quarta S, Savio M, Riva F, Rossi L, et al. (1998) The cyclin-dependent kinase inhibitors olomoucine and roscovitine arrest human fibroblasts in G1 phase by specific inhibition of CDK2 kinase activity. Exp Cell Res 245: 8-18.
24. Lam LT, Pickeral OK, Peng AC, Rosenwald A, Hurt EM, et al. (2001) Genomic-scale measurement of mRNA turnover and the mechanisms of action of the anti-cancer drug flavopiridol. Genome Biol 2: RESEARCH0041.
25. Alvi AJ, Austen B, Weston VJ, Fegan C, MacCallum D, et al. (2005) A novel CDK inhibitor, CYC202 (R-roscovitine), overcomes the defect in p53-dependent apoptosis in B-CLL by down-regulation of genes involved in transcription regulation and survival. Blood 105: 4484-4491.
26. Nagahara H, Vocero-Akbani AM, Snyder EL, Ho A, Latham DG, et al. (1998) Transduction of full-length TAT fusion proteins into mammalian cells: TAT-p27Kip1 induces cell migration. Nat Med 4: 1449-1452.
27. Wang X, Shaw S, Amiri F, Eaton DC, Marrero MB, (2002) Inhibition of the Jak/STAT signaling pathway prevents the high glucose-induced increase in tgf-beta and fibronectin synthesis in mesangial cells. Diabetes 51: 3505-3509.
28. Zhang YE, (2009) Non-Smad pathways in TGF-beta signaling. Cell Res 19: 128-139.
29. Feghali CA, Bost KL, Boulware DW, Levy LS, (1994) Control of IL-6 expression and response in fibroblasts from patients with systemic sclerosis. Autoimmunity 17: 309-318.
30. Yamamoto T, Takagawa S, Katayama I, Nishioka K, (1999) Anti-sclerotic effect of transforming growth factor-beta antibody in a mouse model of bleomycin-induced scleroderma. Clin Immunol 92: 6-13.
31. Kawaguchi Y, Hara M, Wright TM, (1999) Endogenous IL-1alpha from systemic sclerosis fibroblasts induces IL-6 and PDGF-A. J Clin Invest 103: 1253-1260.
32. Greenwel P, Iraburu MJ, Reyes-Romero M, Meraz-Cruz N, Casado E, et al. (1995) Induction of an acute phase response in rats stimulates the expression of alpha 1(I) procollagen messenger ribonucleic acid in their livers. Possible role of interleukin-6. Lab Invest 72: 83-91.
33. Ghazizadeh M, Tosa M, Shimizu H, Hyakusoku H, Kawanami O, (2007) Functional implications of the IL-6 signaling pathway in keloid pathogenesis. J Invest Dermatol 127: 98-105.
34. Lim CP, Phan TT, Lim IJ, Cao X, (2006) Stat3 contributes to keloid pathogenesis via promoting collagen production, cell proliferation and migration. Oncogene 25: 5416-5425.
35. Chang ZF, Huang DY, Hu SF, (1999) NF-Y-mediated trans-activation of the human thymidine kinase promoter is closely linked to activation of cyclin-dependent kinase. J Cell Biochem 75: 300-309.
36. Katula KS, Wright KL, Paul H, Surman DR, Nuckolls FJ, et al. (1997) Cyclin-dependent kinase activation and S-phase induction of the cyclin B1 gene are linked through the CCAAT elements. Cell Growth Differ 8: 811-820.
37. Lindahl GE, Chambers RC, Papakrivopoulou J, Dawson SJ, Jacobsen MC, et al. (2002) Activation of fibroblast procollagen alpha 1(I) transcription by mechanical strain is transforming growth factor-beta-dependent and involves increased binding of CCAAT-binding factor (CBF/NF-Y) at the proximal promoter. J Biol Chem 277: 6153-6161.
38. Collins M, Leaner VD, Madikizela M, Parker MI, (1997) Regulation of the human alpha 2(1) procollagen gene by sequences adjacent to the CCAAT box. Biochem J 322: 199-206.
39. Hu Q, Maity SN, (2000) Stable expression of a dominant negative mutant of CCAAT binding factor/NF-Y in mouse fibroblast cells resulting in retardation of cell growth and inhibition of transcription of various cellular genes. J Biol Chem 275: 4435-4444.
40. Ghosh AK, Yuan W, Mori Y, Varga J, (2000) Smad-dependent stimulation of type I collagen gene expression in human skin fibroblasts by TGF-beta involves functional cooperation with p300/CBP transcriptional coactivators [In Process Citation]. Oncogene 19: 3546-3555.
41. Jordan-Sciutto KL, Logan TJ, Norton PA, Derfoul A, Dodge GR, et al. (1997) Reduction in fibronectin expression and alteration in cell morphology are coincident in NIH3T3 cells expressing a mutant E2F1 transcription factor. Exp Cell Res 236: 527-536.
42. Morris L, Allen KE, La Thangue NB, (2000) Regulation of E2F transcription by cyclin E-Cdk2 kinase mediated through p300/CBP co-activators. Nat Cell Biol 2: 232-239.
43. Haidweger E, Novy M, Rotheneder H, (2001) Modulation of Sp1 activity by a cyclin A/CDK complex. J Mol Biol 306: 201-212.
44. Sysa P, Potter JJ, Liu X, Mezey E, (2009) Transforming growth factor-beta1 up-regulation of human alpha(1)(I) collagen is mediated by Sp1 and Smad2 transacting factors. DNA Cell Biol 28: 425-434.
45. Rossert J, Terraz C, Dupont S, (2000) Regulation of type I collagen genes expression. Nephrol Dial Transplant 15 Suppl 6: 66-68.
46. Zhang X, Wharton W, Donovan M, Coppola D, Croxton R, et al. (2000) Density-dependent growth inhibition of fibroblasts ectopically expressing p27(kip1). Mol Biol Cell 11: 2117-2130.
47. Steinman RA, Wentzel A, Lu Y, Stehle C, Grandis JR, (2003) Activation of Stat3 by cell confluence reveals negative regulation of Stat3 by cdk2. Oncogene 22: 3608-3615.
48. Hou T, Ray S, Brasier AR, (2007) The functional role of an interleukin 6-inducible CDK9.STAT3 complex in human gamma-fibrinogen gene expression. J Biol Chem 282: 37091-37102.
49. Alarcon C, Zaromytidou AI, Xi Q, Gao S, Yu J, et al. (2009) Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-beta pathways. Cell 139: 757-769.
50. Hein N, Jiang K, Cornelissen C, Luscher B, (2011) TGFbeta1 enhances MAD1 expression and stimulates promoter-bound Pol II phosphorylation: basic functions of C/EBP, SP and SMAD3 transcription factors. BMC Mol Biol 12: 9.
51. Grotendorst GR, Okochi H, Hayashi N, (1996) A novel transforming growth factor beta response element controls the expression of the connective tissue growth factor gene. Cell Growth Differ 7: 469-480.
52. Mori T, Kawara S, Shinozaki M, Hayashi N, Kakinuma T, et al. (1999) Role and interaction of connective tissue growth factor with transforming growth factor-beta in persistent fibrosis: A mouse fibrosis model. J Cell Physiol 181: 153-159.
53. Shinozaki M, Kawara S, Hayashi N, Kakinuma T, Igarashi A, et al. (1997) Induction of subcutaneous tissue fibrosis in newborn mice by transforming growth factor beta-simultaneous application with basic fibroblast growth factor causes persistent fibrosis [corrected and republished article originally printed in Biochem Biophys Res Commun 1997 Aug 18;237(2):292-6]. Biochem Biophys Res Commun 240: 292-297.
54. Balomenos D, Martin-Caballero J, Garcia MI, Prieto I, Flores JM, et al. (2000) The cell cycle inhibitor p21 controls T-cell proliferation and sex-linked lupus development. Nat Med 6: 171-176.
55. Le Tourneau C, Faivre S, Laurence V, Delbaldo C, Vera K, et al. (2010) Phase I evaluation of seliciclib (R-roscovitine), a novel oral cyclin-dependent kinase inhibitor, in patients with advanced malignancies. Eur J Cancer 46: 3243-3250.
56. Milovanceva-Popovska M, Kunter U, Ostendorf T, Petermann A, Rong S, et al. (2005) R-roscovitine (CYC202) alleviates renal cell proliferation in nephritis without aggravating podocyte injury. Kidney Int 67: 1362-1370.
57. Benson C, White J, De Bono J, O'Donnell A, Raynaud F, et al. (2007) A phase I trial of the selective oral cyclin-dependent kinase inhibitor seliciclib (CYC202; R-Roscovitine), administered twice daily for 7 days every 21 days. Br J Cancer 96: 29-37.
58. Pilewski JM, Liu L, Henry AC, Knauer AV, Feghali-Bostwick CA, (2005) Insulin-like growth factor binding proteins 3 and 5 are overexpressed in idiopathic pulmonary fibrosis and contribute to extracellular matrix deposition. Am J Pathol 166: 399-407.
59. Chang ZF, Huang DY, (2001) Regulation of thymidine kinase expression during cellular senescence. J Biomed Sci 8: 176-183.