Differential modulation of the cytokine-induced MMP-9/TIMP-1 protease-antiprotease system by the mTOR inhibitor rapamycin

Biochemical Pharmacology

Volumn 81, Issue 1, 2011, Pages 134-143

  Osman, Bashier ^a   Akool, El Sayed ^a   Doller, Anke ^a   Müller, Roswitha ^a   Pfeilschifter, Josef ^a   Eberhardt, Wolfgang ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

Fibrosis; Matrix metalloproteinase 9; Posttranscriptional gene regulation; Rapamycin; Transcription factors

Indexed keywords

CYTOKINE; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; RAPAMYCIN; RECOMBINANT INTERLEUKIN 1BETA; SMAD PROTEIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSCRIPTION FACTOR AP 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENTIATION; IMMUNOMODULATION; KIDNEY FIBROSIS; MESANGIUM CELL; NEPHRITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STEADY STATE; ZYMOGRAPHY;

3' UNTRANSLATED REGIONS; ANIMALS; CELLS, CULTURED; CYTOKINES; DACTINOMYCIN; GENE EXPRESSION REGULATION; IMMUNOSUPPRESSIVE AGENTS; MATRIX METALLOPROTEINASE 9; MESANGIAL CELLS; NEOPLASM PROTEINS; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; PROTO-ONCOGENE PROTEINS C-JUN; RATS; RNA, MESSENGER; SIROLIMUS; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TOR SERINE-THREONINE KINASES;

EID: 78549260675     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2010.09.011     Document Type: Article

References (37)

1. Faivre S., Kroemer G., Raymond E. Current development of mTOR inhibitors as anticancer agents. Nat Rev Drug Discov 2006, 5:671-688.
2. Saunders R.N., Metcalfe M.S., Nicholson M.L. Rapamycin in transplantation: a review of the evidence. Kidney Int 2001, 59:3-16.
3. Shihab F.S., Bennett W.M., Yi H., Choi S.O., Andoh T.F. Sirolimus increases transforming growth factor-beta1 expression and potentiates chronic cyclosporine nephrotoxicity. Kidney Int 2004, 65:1262-1271.
4. Ninova D., Covarrubias M., Rea D.J., Park W.D., Grande J.P., Stegall M.D. Acute nephrotoxicity of tacrolimus and sirolimus in renal isografts: differential intragraft expression of transforming growth factor-β1 and α-smooth muscle actin. Transplantation 2004, 78:338-344.
5. Osman B., Doller A., Akool el-S., Holdener M., Hintermann E., Pfeilschifter J., et al. Rapamycin induces the TGFβ1/Smad signaling cascade in renal mesangial cells upstream of mTOR. Cell Signal 2009, 21:1806-1817.
6. Eddy A.A. Molecular insights into renal interstitial fibrosis. J Am Soc Nephrol 1996, 7:2495-2508.
7. Eddy A.A., Fogo A.B. Plasminogen activator inhibitor-1 in chronic kidney disease: evidence and mechanisms of action. J Am Soc Nephrol 2006, 17:2999-3012.
8. Nagase H., Woessner J.F. Matrix metalloproteinases. J Biol Chem 1999, 274:21491-21494.
9. Lenz O., Elliot S.J., Stetler-Stevenson W.G. Matrix metalloproteinases in renal development and disease. Am Soc Nephrol 2000, 11:574-581.
10. Van Ranst M., Norga K., Masure S., Proost P., Vandekerckhove F., Auwerx J., et al. The cytokine-protease connection: identification of a 96-kD THP-1 gelatinase and regulation by interleukin-1 and cytokine inducers. Cytokine 1991, 3:231-239.
11. Opdenakker G., Masure S., Grillet B., Van Damme J. Cytokine-mediated regulation of human leukocyte gelatinases and role in arthritis. Lymphokine Cytokine Res 1991, 10:317-324.
12. Eberhardt W., Schulze M., Engels C., Klasmeier E., Pfeilschifter J. Glucocorticoid-mediated suppression of cytokine-induced matrix metalloproteinase-9 expression in rat mesangial cells: involvement of nuclear factor-κB and Ets transcription factors. Mol Endocrinol 2002, 16:1752-1766.
13. Doller A., Akool el-S., Müller R., Gutwein P., Kurowski C., Pfeilschifter J., et al. Molecular mechanisms of cyclosporin A inhibition of the cytokine-induced matrix metalloproteinase-9 in glomerular mesangial cells. J Am Soc Nephrol 2007, 18:581-592.
14. Eberhardt W., Huwiler A., Beck K.F., Walpen S., Pfeilschifter J. Amplification of IL-1 β-induced matrix metalloproteinase-9 expression by superoxide in rat glomerular mesangial cells is mediated by increased activities of NF-κB and activating protein-1 and involves activation of the mitogen-activated protein kinase pathways. J Immunol 2000, 165:5788-5797.
15. Akool el-S., Kleinert H., Hamada F.M., Abdelwahab M.H., Förstermann U., Pfeilschifter J., et al. Nitric oxide increases the decay of matrix metalloproteinase 9 mRNA by inhibiting the expression of mRNA-stabilizing factor HuR. Mol Cell Biol 2003, 23:4901-4916.
16. Iyer V., Pumiglia K., DiPersio C.M. Alpha3beta1 integrin regulates MMP-9 mRNA stability in immortalized keratinocytes: a novel mechanism of integrin-mediated MMP gene expression. J Cell Sci 2005, 118:1185-1195.
17. Jiang Y., Muschel R.J. Regulation of matrix metalloproteinase-9 (MMP-9) by translational efficiency in murine prostate carcinoma cells. Cancer Res 2002, 62:1910-1914.
18. Sehgal I., Thompson T.C. Novel regulation of type IV collagenase (matrix metalloproteinase-9 and -2) activities by transforming growth factor-β1 in human prostate cancer cell lines. Mol Biol Cell 1999, 10:407-416.
19. Fähling M., Steege A., Perlewitz A., Nafz B., Mrowka R., Persson P.B., et al. Role of nucleolin in posttranscriptional control of MMP-9 expression. Biochim Biophys Acta 2005, 1731:32-40.
20. Jespersen C., Doller A., Akool el-S., Bachmann M., Müller R., Gutwein P., et al. Molecular mechanisms of nitric oxide-dependent inhibition of TPA-induced matrix metalloproteinase-9 (MMP-9) in MCF-7 cells. J Cell Physiol 2009, 219:276-287.
21. Pfeilschifter J., Vosbeck K. Transforming growth factor β 2 inhibits interleukin 1 β- and tumour necrosis factor α induction of nitric oxide synthase in rat renal mesangial cells. Biochem Biophys Res Commun 1991, 175:372-379.
22. Eberhardt W., Beeg T., Beck K.F., Walpen S., Gauer S., Böhles H., et al. Nitric oxide modulates expression of matrix metalloproteinase-9 in rat mesangial cells. Kidney Int 2000, 57:59-69.
23. Van den Steen P.E., Dubois B., Nelissen I., Rudd P.M., Dwek R.A., Opdenakker G. Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9). Crit Rev Biochem Mol Biol 2002, 37:375-536.
24. Akool el-S., Doller A., Müller R., Gutwein P., Xin C., Huwiler A., et al. Nitric oxide induces TIMP-1 expression by activating the transforming growth factor beta-Smad signaling pathway. J Biol Chem 2005, 280:39403-39416.
25. Banholzer R., Nair A.P., Hirsch H.H., Ming X.F., Moroni C. Rapamycin destabilizes interleukin-3 mRNA in autocrine tumor cells by a mechanism requiring an intact 3' untranslated region. Mol Cell Biol 1997, 17:3254-3260.
26. Yokoo T., Kitamura M. Dual regulation of IL-1 β-mediated matrix metalloproteinase-9 expression in mesangial cells by NF-kappa B and AP-1. Am J Physiol 1996, 270:F123-F130.
27. Huang S., Shu L., Dilling M.B., Easton J., Harwood F.C., Ichijo H., et al. Sustained activation of the JNK cascade and rapamycin-induced apoptosis are suppressed by p53/p21(Cip1). Mol Cell 2003, 11:1491-1501.
28. Poulalhon N., Farge D., Roos N., Tacheau C., Neuzillet C., Michel L., et al. Modulation of collagen and MMP-1 gene expression in fibroblasts by the immunosuppressive drug rapamycin. A direct role as an antifibrotic agent?. J Biol Chem 2006, 281:33045-33052.
29. Ogawa K., Chen F., Kuang C., Chen Y. Suppression of matrix metalloproteinase-9 transcription by transforming growth factor-β is mediated by a nuclear factor-κB site. Biochem J 2004, 381:413-422.
30. Huwiler A., Akool el-S., Aschrafi A., Hamada F.M., Pfeilschifter J., Eberhardt W. ATP potentiates interleukin-1 beta-induced MMP-9 expression in mesangial cells via recruitment of the ELAV protein HuR. J Biol Chem 2003, 278:51758-51769.
31. Eberhardt W., Doller A., Akool el-S., Pfeilschifter J. Modulation of mRNA stability as a novel therapeutic approach. Pharmacol Ther 2007, 114:56-73.
32. Shegogue D., Trojanowska M. Mammalian target of rapamycin positively regulates collagen type I production via a phosphatidylinositol 3-kinase-independent pathway. J Biol Chem 2004, 279:23166-23175.
33. Pallet N., Thervet E., Le Corre D., Knebelmann B., Nusbaum P., Tomkiewicz C., et al. Rapamycin inhibits human renal epithelial cell proliferation: effect on cyclin D3 mRNA expression and stability. Kidney Int 2005, 67:2422-2433.
34. Zhang W., Wagner B.J., Ehrenman K., Schaefer A.W., DeMaria C.T., Crater D., et al. Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1. Mol Cell Biol 1993, 13:7652-7665.
35. Blackshear P.J. Tristetraprolin and other CCCH tandem zinc-finger proteins in the regulation of mRNA turnover. Biochem Soc Trans 2002, 30:945-952.
36. Gherzi R., Trabucchi M., Ponassi M., Ruggiero T., Corte G., Moroni C., et al. The RNA-binding protein KSRP promotes decay of beta-catenin mRNA and is inactivated by PI3K-AKT signaling. PLoS Biol 2006, 5:e5.
37. Berthier C.C., Wahl P.R., Le Hir M., Marti H.P., Wagner U., Rehrauer H., et al. Sirolimus ameliorates the enhanced expression of metalloproteinases in a rat model of autosomal dominant polycystic kidney disease. Nephrol Dial Transplant 2008, 23:880-889.