Withaferin-A reduces type I collagen expression in vitro and inhibits development of myocardial fibrosis in vivo

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Challa, Azariyas A ^a   Vukmirovic, Milica ^a   Blackmon, John ^a   Stefanovic, Branko ^a  

^a FLORIDA STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; ISOPRENALINE; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA1; VIMENTIN; WITHAFERIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; EMBRYO; GENE EXPRESSION; GENETIC TRANSCRIPTION; HALF LIFE TIME; HEART MUSCLE FIBROSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STELLATE CELL;

ANIMALS; CELL LINE; COLLAGEN TYPE I; ENDOMYOCARDIAL FIBROSIS; FIBROBLASTS; GENE EXPRESSION REGULATION; GENE KNOCKOUT TECHNIQUES; HEPATIC STELLATE CELLS; HUMANS; ISOPROTERENOL; MALE; MICE; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEOLYSIS; RNA STABILITY; RNA, MESSENGER; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; VIMENTIN; WITHANOLIDES;

EID: 84865011936     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042989     Document Type: Article

References (69)

1. Bitterman PB, Henke CA, ((1991)) Fibroproliferative disorders. Chest 99:: 81S--84S.
2. Friedman SL, ((2010)) Evolving challenges in hepatic fibrosis. Nat Rev Gastroenterol Hepatol 7:: 425--436.
3. Diez J, ((2008)) Diagnosis and treatment of myocardial fibrosis in hypertensive heart disease. Circ J 72 (Suppl A):: A8--12.
4. Boor P, Ostendorf T, Floege J, ((2010)) Renal fibrosis: novel insights into mechanisms and therapeutic targets. Nat Rev Nephrol 6:: 643--656.
5. Brenner DA, Waterboer T, Choi SK, Lindquist JN, Stefanovic B, et al. ((2000)) New aspects of hepatic fibrosis. J Hepatol 32:: 32--38.
6. Wynn TA, ((2008)) Cellular and molecular mechanisms of fibrosis. J Pathol 214:: 199--210.
7. Hernandez-Gea V, Friedman SL, ((2011)) Pathogenesis of liver fibrosis. Annu Rev Pathol 6:: 425--456.
8. Wynn TA, ((2007)) Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest 117:: 524--529.
9. Scotton CJ, Chambers RC, ((2007)) Molecular targets in pulmonary fibrosis: the myofibroblast in focus. Chest 132:: 1311--1321.
10. Lindquist JN, Marzluff WF, Stefanovic B, ((2000)) Fibrogenesis. III. Posttranscriptional regulation of type I collagen. Am J Physiol Gastrointest Liver Physiol 279:: G471--476.
11. Penttinen RP, Kobayashi S, Bornstein P, ((1988)) Transforming growth factor beta increases mRNA for matrix proteins both in the presence and in the absence of changes in mRNA stability. Proc Natl Acad Sci U S A 85:: 1105--1108.
12. Stefanovic B, Hellerbrand C, Holcik M, Briendl M, Aliebhaber S, et al. ((1997)) Posttranscriptional regulation of collagen alpha1(I) mRNA in hepatic stellate cells. Mol Cell Biol 17:: 5201--5209.
13. Lindquist JN, Parsons CJ, Stefanovic B, Brenner DA, ((2004)) Regulation of alpha1(I) collagen messenger RNA decay by interactions with alphaCP at the 3'-untranslated region. J Biol Chem 279:: 23822--23829.
14. Trojanowska M, ((2009)) Noncanonical transforming growth factor beta signaling in scleroderma fibrosis. Curr Opin Rheumatol 21:: 623--629.
15. Cai L, Fritz D, Stefanovic L, Stefanovic B, ((2010)) Binding of LARP6 to the conserved 5' stem-loop regulates translation of mRNAs encoding type I collagen. J Mol Biol 395:: 309--326.
16. Challa AA, Stefanovic B, ((2011)) A Novel Role of Vimentin Filaments: Binding and Stabilization of Collagen mRNAs. Mol Cell Biol 31:: 3773--3789.
17. Mirjalili MH, Moyano E, Bonfill M, Cusido RM, Palazon J, ((2009)) Steroidal lactones from Withania somnifera, an ancient plant for novel medicine. Molecules 14:: 2373--2393.
18. Bargagna-Mohan P, Hamza A, Kim YE, Khuan Abby Ho Y, Mor-Vaknin N, et al. ((2007)) The tumor inhibitor and antiangiogenic agent withaferin A targets the intermediate filament protein vimentin. Chem Biol 14:: 623--634.
19. Yamada N, Castro A, Farber R, ((2003)) Variation in the extent of microsatellite instability in human cell lines with defects in different mismatch repair genes. Mutagenesis 18:: 277--282.
20. Holwell T, Schweitzer S, Evans R, ((1997)) Tetracycline regulated expression of vimentin in fibroblasts derived from vimentin null mice. J Cell Sci 110 (Pt 16):: 1947--1956.
21. Agocha AE, Eghbali-Webb M, ((1997)) A simple method for preparation of cultured cardiac fibroblasts from adult human ventricular tissue. Mol Cell Biochem 172:: 195--198.
22. Weiskirchen R, Gressner AM, ((2005)) Isolation and culture of hepatic stellate cells. Methods Mol Med 117:: 99--113.
23. Yang H, Shi G, Dou QP, ((2007)) The tumor proteasome is a primary target for the natural anticancer compound Withaferin A isolated from "Indian winter cherry". Mol Pharmacol 71:: 426--437.
24. Cuenda A, Rouse J, Doza YN, Meier R, Cohen P, et al. ((1995)) SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett 364:: 229--233.
25. Smaldone S, Olivieri J, Gusella GL, Moroncini G, Gabrielli A, et al. ((2011)) Ha-Ras stabilization mediates pro-fibrotic signals in dermal fibroblasts. Fibrogenesis Tissue Repair 4:: 8.
26. Dennler S, Itoh S, Vivien D, ten Dijke P, Huet S, et al. ((1998)) Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J 17:: 3091--3100.
27. Zhang X, Bremer H, ((1995)) Control of the Escherichia coli rrnB P1 promoter strength by ppGpp. J Biol Chem 270:: 11181--11189.
28. Abe M, Harpel JG, Metz CN, Nunes I, Loskutoff DJ, et al. ((1994)) An assay for transforming growth factor-beta using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct. Anal Biochem 216:: 276--284.
29. Stefanovic B, Hellerbrand C, Holcik M, Briendl M, Aliebhaber S, et al. ((1997)) Posttranscriptional regulation of collagen alpha1(I) mRNA in hepatic stellate cells. Mol Cell Biol 17:: 5201--5209.
30. Bargagna-Mohan P, Paranthan RR, Hamza A, Dimova N, Trucchi B, et al. ((2010)) Withaferin A targets intermediate filaments glial fibrillary acidic protein and vimentin in a model of retinal gliosis. J Biol Chem 285:: 7657--7669.
31. Thaiparambil JT, Bender L, Ganesh T, Kline E, Patel P,et al. (2011) Withaferin A inhibits breast cancer invasion and metastasis at sub-cytotoxic doses by inducing vimentin disassembly and serine 56 phosphorylation. Int J Cancer.
32. Lee TJ, Um HJ, Min do S, Park JW, Choi KS, et al. ((2009)) Withaferin A sensitizes TRAIL-induced apoptosis through reactive oxygen species-mediated up-regulation of death receptor 5 and down-regulation of c-FLIP. Free Radic Biol Med 46:: 1639--1649.
33. Ignotz RA, Endo T, Massague J, ((1987)) Regulation of fibronectin and type I collagen mRNA levels by transforming growth factor-beta. J Biol Chem 262:: 6443--6446.
34. Oh JH, Lee TJ, Park JW, Kwon TK, ((2008)) Withaferin A inhibits iNOS expression and nitric oxide production by Akt inactivation and down-regulating LPS-induced activity of NF-kappaB in RAW 264.7 cells. Eur J Pharmacol 599:: 11--17.
35. Tsukada S, Westwick JK, Ikejima K, Sato N, Rippe RA, ((2005)) SMAD and p38 MAPK signaling pathways independently regulate alpha1(I) collagen gene expression in unstimulated and transforming growth factor-beta-stimulated hepatic stellate cells. J Biol Chem 280:: 10055--10064.
36. Parsons CJ, Takashima M, Rippe RA, ((2007)) Molecular mechanisms of hepatic fibrogenesis. J Gastroenterol Hepatol 22 (Suppl 1):: S79--84.
37. Hellerbrand C, Stefanovic B, Giordano F, Burchardt ER, Brenner DA, ((1999)) The role of TGFbeta1 in initiating hepatic stellate cell activation in vivo. J Hepatol 30:: 77--87.
38. Brooks WW, Conrad CH, ((2009)) Isoproterenol-induced myocardial injury and diastolic dysfunction in mice: structural and functional correlates. Comp Med 59:: 339--343.
39. Pick R, Jalil JE, Janicki JS, Weber KT, ((1989)) The fibrillar nature and structure of isoproterenol-induced myocardial fibrosis in the rat. Am J Pathol 134:: 365--371.
40. Faulx MD, Ernsberger P, Vatner D, Hoffman RD, Lewis W, et al. ((2005)) Strain-dependent beta-adrenergic receptor function influences myocardial responses to isoproterenol stimulation in mice. Am J Physiol Heart Circ Physiol 289:: H30--36.
41. Rona G, ((1985)) Catecholamine cardiotoxicity. J Mol Cell Cardiol 17:: 291--306.
42. Ghiassi-Nejad Z, Friedman SL, ((2008)) Advances in antifibrotic therapy. Expert Rev Gastroenterol Hepatol 2:: 803--816.
43. Fallowfield JA, ((2011)) Therapeutic targets in liver fibrosis. Am J Physiol Gastrointest Liver Physiol 300:: G709--715.
44. Leask A, ((2010)) Potential therapeutic targets for cardiac fibrosis: TGFbeta, angiotensin, endothelin, CCN2, and PDGF, partners in fibroblast activation. Circ Res 106:: 1675--1680.
45. Thompson AJ, Patel K, ((2010)) Antifibrotic therapies: will we ever get there? Curr Gastroenterol Rep 12:: 23--29.
46. Fritz D, Cai L, Stefanovic L, Stefanovic B, ((2011)) Progress towards discovery of antifibrotic drugs targeting synthesis of type I collagen. Curr Med Chem 18:: 3410--3416.
47. Stefanovic B, Hellerbrand C, Brenner DA, ((1999)) Regulatory role of the conserved stem-loop structure at the 5' end of collagen alpha1(I) mRNA. Mol Cell Biol 19:: 4334--4342.
48. Bauer M, Schuppan D, ((2001)) TGFbeta1 in liver fibrosis: time to change paradigms? FEBS Lett 502:: 1--3.
49. Ihn H, ((2002)) Pathogenesis of fibrosis: role of TGF-beta and CTGF. Curr Opin Rheumatol 14:: 681--685.
50. Lijnen PJ, Petrov VV, Fagard RH, ((2000)) Induction of cardiac fibrosis by transforming growth factor-beta(1). Mol Genet Metab 71:: 418--435.
51. Petrov VV, Fagard RH, Lijnen PJ, ((2002)) Stimulation of collagen production by transforming growth factor-beta1 during differentiation of cardiac fibroblasts to myofibroblasts. Hypertension 39:: 258--263.
52. Cheng K, Yang N, Mahato RI, ((2009)) TGF-beta1 gene silencing for treating liver fibrosis. Mol Pharm 6:: 772--779.
53. de Gouville AC, Boullay V, Krysa G, Pilot J, Brusq JM, et al. ((2005)) Inhibition of TGF-beta signaling by an ALK5 inhibitor protects rats from dimethylnitrosamine-induced liver fibrosis. Br J Pharmacol 145:: 166--177.
54. Brown RD, Ambler SK, Mitchell MD, Long CS, ((2005)) The cardiac fibroblast: therapeutic target in myocardial remodeling and failure. Annu Rev Pharmacol Toxicol 45:: 657--687.
55. Grover A, Shandilya A, Punetha A, Bisaria VS, Sundar D, ((2010)) Inhibition of the NEMO/IKKbeta association complex formation, a novel mechanism associated with the NF-kappaB activation suppression by Withania somnifera's key metabolite withaferin A. BMC Genomics. 11 (Suppl 4):: S25.
56. Gonzalez A, Lopez B, Diez J, ((2005)) New directions in the assessment and treatment of hypertensive heart disease. Curr Opin Nephrol Hypertens 14:: 428--434.
57. Diez J, ((2007)) Mechanisms of cardiac fibrosis in hypertension. J Clin Hypertens (Greenwich) 9:: 546--550.
58. Cuspidi C, Ciulla M, Zanchetti A, ((2006)) Hypertensive myocardial fibrosis. Nephrol Dial Transplant 21:: 20--23.
59. Heling A, Zimmermann R, Kostin S, Maeno Y, Hein S, et al. ((2000)) Increased expression of cytoskeletal, linkage, and extracellular proteins in failing human myocardium. Circ Res 86:: 846--853.
60. Lombardi R, Betocchi S, Losi MA, Tocchetti CG, Aversa M, et al. ((2003)) Myocardial collagen turnover in hypertrophic cardiomyopathy. Circulation 108:: 1455--1460.
61. Querejeta R, Lopez B, Gonzalez A, Sanchez E, Larman M, et al. ((2004)) Increased collagen type I synthesis in patients with heart failure of hypertensive origin: relation to myocardial fibrosis. Circulation 110:: 1263--1268.
62. Berk BC, Fujiwara K, Lehoux S, ((2007)) ECM remodeling in hypertensive heart disease. J Clin Invest 117:: 568--575.
63. Brilla CG, Funck RC, Rupp H, ((2000)) Lisinopril-mediated regression of myocardial fibrosis in patients with hypertensive heart disease. Circulation 102:: 1388--1393.
64. Zannad F, Alla F, Dousset B, Perez A, Pitt B, ((2000)) Limitation of excessive extracellular matrix turnover may contribute to survival benefit of spironolactone therapy in patients with congestive heart failure: insights from the randomized aldactone evaluation study (RALES). Rales Investigators. Circulation 102:: 2700--2706.
65. Diez J, Querejeta R, Lopez B, Gonzalez A, Larman M, et al. ((2002)) Losartan-dependent regression of myocardial fibrosis is associated with reduction of left ventricular chamber stiffness in hypertensive patients. Circulation 105:: 2512--2517.
66. Maitra R, Porter MA, Huang S, Gilmour BP, ((2009)) Inhibition of NFkappaB by the natural product Withaferin A in cellular models of Cystic Fibrosis inflammation. J Inflamm (Lond) 6:: 15.
67. Csermely P, Agoston V, Pongor S, ((2005)) The efficiency of multi-target drugs: the network approach might help drug design. Trends Pharmacol Sci 26:: 178--182.
68. Stan SD, Hahm ER, Warin R, Singh SV, ((2008)) Withaferin A causes FOXO3a- and Bim-dependent apoptosis and inhibits growth of human breast cancer cells in vivo. Cancer Res 68:: 7661--7669.
69. Sharada AC, Solomon FE, Devi PU, Udupa N, Srinivasan KK, ((1996)) Antitumor and radiosensitizing effects of withaferin A on mouse Ehrlich ascites carcinoma in vivo. Acta Oncol 35:: 95--100.