Fibrodysplasia induced in dog skin by a matrix metalloproteinase (MMP) inhibitor-a mechanistic analysis

Toxicological Sciences

Volumn 127, Issue 1, 2012, Pages 236-245

  Tugwood, Jonathan D ^a   Kelsall, Janet ^a   Coverley, Lucy C ^a   Westwood, F Russell ^a   Haque, Kemal ^b   Huby, Russell D J ^a  

^a ASTRAZENECA   (United Kingdom)

^b Prosidion Ltd   (United Kingdom)

Author keywords

ECM remodeling; Fibrosis; Gene expression; Matrix metalloproteinases

Indexed keywords

AZM 551248; COLLAGEN; GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE INHIBITOR; PROTEINASE; STROMELYSIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DOG; EXTRACELLULAR MATRIX; FEMALE; FIBROSIS; FIBROUS DYSPLASIA; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; NONHUMAN; SKIN; SUBCUTANEOUS FAT; UPREGULATION;

EID: 84860154893     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfs075     Document Type: Article

References (40)

1. Asano, Y., Ihn, H., Yamane, K., Jinnin, M., and Tamaki, K. (2006). Increased expression of integrin alphavbeta5 induces the myofibroblastic differentiation of dermal fibroblasts. Am. J. Pathol. 168, 499-510.
2. Bank, U., Heimburg, A., Helmuth, M., Stefin, S., Lendeckel, U., Reinhold, D., Faust, J., Fuchs, P., Sens, B., Neubert, K., et al. (2006). Triggering endogenous immunosuppressive mechanisms by combined targeting of dipeptidyl peptidase IV (DPIV/CD26) and aminopeptidase N (APN/ CD13)-A novel approach for the treatment of inflammatory bowel disease. Int. Immunopharmacol. 6, 1925-1934.
3. Baragi, V. M., Becher, G., Bendele, A. M., Biesinger, R., Bluhm, H., Boer, J., Deng, H., Dodd, R., Essers, M., Feuerstein, T., et al. (2009). A new class of potent matrix metalloproteinase 13 inhibitors for potential treatment of osteoarthritis: Evidence of histologic and clinical efficacy without musculoskeletal toxicity in rat models. Arthritis Rheum. 60, 2008-2018.
4. Bignon, M., Pichol-Thievend, C., Hardouin, J., Malbouyres, M., Brechot, N., Nasciutti, L., Barret, A., Teillon, J., Guillon, E., Etienne, E., et al. (2011). Lysyl oxidase-like protein-2 regulates sprouting angiogenesis and type IV collagen assembly in the endothelial basement membrane. Blood 118, 3979-3989.
5. Border, W. A., and Noble, N. A. (1998). Evidence that TGF-beta should be a therapeutic target in diabetic nephropathy. Kidney Int. 54, 1390-1391.
6. Brinckerhoff, C. E., and Matrisian, L. M. (2002). Matrix metalloproteinases: A tail of a frog that became a prince. Nat. Rev. Mol. Cell Biol. 3, 207-214.
7. Chambers, R. C., Leoni, P., Kaminski, N., Laurent, G. J., and Heller, R. A. (2003). Global expression profiling of fibroblast responses to transforming growth factor-beta1 reveals the induction of inhibitor of differentiation-1 and provides evidence of smooth muscle cell phenotypic switching. Am. J. Pathol. 162, 533-546.
8. Chu, S., and Ferro, T. J. (2005). Sp1: Regulation of gene expression by phosphorylation. Gene 348, 1-11.
9. Clark, I. M., and Parker, A. E. (2003). Metalloproteinases: Their role in arthritis and potential as therapeutic targets. Expert Opin. Ther. Targets 7, 19-34.
10. Coussens, L. M., Fingleton, B., and Matrisian, L. M. (2002). Matrix metalloproteinase inhibitors and cancer: Trials and tribulations. Science 295, 2387-2392.
11. Drummond, A. H., Beckett, P., Brown, P. D., Bone, E. A., Davidson, A. H., Galloway, W. A., Gearing, A. J., Huxley, P., Laber, D., McCourt, M., et al. (1999). Preclinical and clinical studies of MMP inhibitors in cancer. Ann. N. Y. Acad. Sci. 878, 228-235.
12. Ge, G., and Greenspan, D. S. (2006). BMP1 controls TGFbeta1 activation via cleavage of latent TGFbeta-binding protein. J. Cell Biol. 175, 111-120.
13. Ghersi, G., Zhao, Q., Salamone, M., Yeh, Y., Zucker, S., and Chen, W. (2006). The protease complex consisting of dipeptidyl peptidase IV and seprase plays a role in the migration and invasion of human endothelial cells in collagenous matrices. Cancer Res. 66, 4652-4661.
14. Hutchinson, J. W., Tierney, G. M., Parsons, S. L., and Davis, T. R. (1998). Dupuytren's disease and frozen shoulder induced by treatment with a matrix metalloproteinase inhibitor. J. Bone Joint Surg. Br. 80, 907-908.
15. Johnson, A. R., Pavlovsky, A. G., Ortwine, D. F., Prior, F., Man, C., Bornemeier, D. A., Banotai, C. A., Mueller, W. T., McConnell, P., Yan, C., et al. (2007). Discovery and characterization of a novel inhibitor of matrix metalloprotease-13 that reduces cartilage damage in vivo without joint fibroplasia side effects. J. Biol. Chem. 282, 27781-27791.
16. Juillerat-Jeanneret, L., and Gerber-Lemaire, S. (2009).The prolyl-aminodipeptidases and their inhibitors as therapeutic targets for fibrogenic disorders. Mini Rev. Med. Chem. 9, 215-226.
17. Kahari, V. M., Hakkinen, L., Westermarck, J., and Larjava, H. (1995). Differential regulation of decorin and biglycan gene expression by dexamethasone and retinoic acid in cultured human skin fibroblasts. J. Invest. Dermatol. 104, 503-508.
18. King, J., Zhao, J., Clingan, P., and Morris, D. (2003). Randomised double blind placebo control study of adjuvant treatment with the metalloproteinase inhibitor, Marimastat in patients with inoperable colorectal hepatic metastases: Significant survival advantage in patients with musculoskeletal side-effects. Anticancer Res. 23, 639-645.
19. Kocarek, T. A., Dahn, M. S., Cai, H., Strom, S. C., and Mercer-Haines, N. A. (2002). Regulation of CYP2B6 and CYP3A expression by hydroxymethylglutaryl coenzyme A inhibitors in primary cultured human hepatocytes. Drug Metab. Dispos. 30, 1400-1405.
20. Konttinen, Y. T., Salo, T., Hanemaaijer, R., Valleala, H., Sorsa, T., Sutinen, M., Ceponis, A., Xu, J. W., Santavirta, S., Teronen, O., et al. (1999). Collagenase-3 (MMP-13) and its activators in rheumatoid arthritis: Localization in the pannus-hard tissue junction and inhibition by alendronate. Matrix Biol. 18, 401-412.
21. Krzeski, P., Buckland-Wright, C., Balint, G., Cline, G. A., Stoner, K., Lyon, R., Beary, J., Aronstein, W. S., and Spector, T. D. (2007). Development of musculoskeletal toxicity without clear benefit after administration of PG-116800, a matrix metalloproteinase inhibitor, to patients with knee osteoarthritis: A randomized, 12-month, double-blind, placebo-controlled study. Arthritis Res. Ther. 9, R109.
22. Ma, J., Wang, Q., Fei, T., Han, J. D. J., and Chen, Y. G. (2007). MCP-1 mediates TGF-beta-induced angiogenesis by stimulating vascular smooth muscle cell migration. Blood 109, 987-994.
23. Murphy, G., Knauper, V., Atkinson, S., Butler, G., English, W., Hutton, M., Stracke, J., and Clark, I. (2002). Matrix metalloproteinases in arthritic disease. Arthritis Res. 4, S39-S49.
24. Overall, C. M., and Kleifeld, O. (2006). Tumour microenvironment-opinion: Validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy. Nat. Rev. Cancer 6, 227-239.
25. Peterson, J. T. (2006). The importance of estimating the therapeutic index in the development of matrix metalloproteinase inhibitors. Cardiovasc. Res. 69, 677-687.
26. Renkiewicz, R., Qiu, L., Lesch, C., Sun, X., Devalaraja, R., Cody, T., Kaldjian, E., Welgus, H., and Baragi, V. (2003). Broad-spectrum matrix metalloproteinase inhibitor marimastat-induced musculoskeletal side effects in rats. Arthritis Rheum. 48, 1742-1749.
27. Samarakoon, R., Higgins, C. E., Higgins, S. P., and Higgins, P. J. (2009). TGFbeta1-induced expression of the poor prognosis SERPINE1/PAI-1 gene requires EGFR signaling: A new target for anti-EGFR therapy. J. Oncol. 2009, 342391.
28. Stefan, M., Simmons, R. A., Bertera, S., Trucco, M., Esni, F., Drain, P., and Nicholls, R. D. (2011). Global deficits in development, function, and gene expression in the endocrine pancreas in a deletion mouse model of Prader-Willi syndrome. Am. J. Physiol. Endocrinol. Metab. 300, E909-E922.
29. Taguchi, T., Nazneen, A., Al-Shihri, A. A., Turkistani, K. A., and Razzaque, M. S. (2011). Heat shock protein 47: A novel biomarker of phenotypically altered collagen-producing cells. Acta Histochem. Cytochem. 44, 35-41.
30. Thielitz, A., Reinhold, D., Vetter, R., Bank, U., Helmuth, M., Hartig, R., Wrenger, S., Wiswedel, I., Lendeckel, U., Kahne, T., et al. (2006). Inhibitors of dipeptidyl peptidase IV and aminopeptidase N target major pathogenetic steps in acne initiation. J. Invest. Dermatol. 127, 1042-1051.
31. Thielitz, A., Vetter, R. W., Schultze, B., Wrenger, S., Simeoni, L., Ansorge, S., Neubert, K., Faust, J., Lindenlaub, P., Gollnick, H. P. M., et al. (2007). Inhibitors of dipeptidyl peptidase IV-like activity mediate antifibrotic effects in normal and keloid-derived skin fibroblasts. J. Invest. Dermatol. 128, 855-866.
32. Tierney, G. M., Griffin, N. R., Stuart, R. C., Kasem, H., Lynch, K. P., Lury, J. T., Brown, P. D., Millar, A. W., Steele, R. J., and Parsons, S. L. (1999). A pilot study of the safety and effects of the matrix metalloproteinase inhibitor marimastat in gastric cancer. Eur. J. Cancer 35, 563-568.
33. Verrecchia, F., Chu, M. L., and Mauviel, A. (2001). Identification of novel TGF-beta/Smad gene targets in dermal fibroblasts using a combined cDNA microarray/promoter transactivation approach. J. Biol. Chem. 276, 17058-17062.
34. Visse, R., and Nagase, H. (2003). Matrix metalloproteinases and tissue inhibitors of metalloproteinases: Structure, function, and biochemistry. Circ. Res. 92, 827-839.
35. Webster, N. L., and Crowe, S. M. (2006). Matrix metalloproteinases, their production by monocytes and macrophages and their potential role in HIVrelated diseases. J. Leukoc. Biol. 80, 1052-1066.
36. Wernicke, D., Seyfert, C., Gromnica-Ihle, E., and Stiehl, P. (2006). The expression of collagenase 3 (MMP-13) mRNA in the synovial tissue is associated with histopathologic type II synovitis in rheumatoid arthritis. Autoimmunity 39, 307-313.
37. Westhoff, C. S., Freudiger, D., Petrow, P., Seyfert, C., Zacher, J., Kriegsmann, J., Pap, T., Gay, S., Stiehl, P., Gromnica-Ihle, E., et al. (1999). Characterization of collagenase 3 (matrix metalloproteinase 13) messenger RNA expression in the synovial membrane and synovial fibroblasts of patients with rheumatoid arthritis. Arthritis Rheum. 42, 1517-1527.
38. Westwood, R., Scott, R. C., Somers, R. L., Coulson, M., and Maciewicz, R. A. (2009). Characterization of fibrodysplasia in the dog following inhibition of metalloproteinases. Toxicol. Pathol. 37, 860-872.
39. Wu, W., Billinghurst, R. C., Pidoux, I., Antoniou, J., Zukor, D., Tanzer, M., and Poole, A. R. (2002). Sites of collagenase cleavage and denaturation of type II collagen in aging and osteoarthritic articular cartilage and their relationship to the distribution of matrix metalloproteinase 1 and matrix metalloproteinase 13. Arthritis Rheum. 46, 2087-2094.
40. Zeisberg, M., and Neilson, E. G. (2009). Biomarkers for epithelialmesenchymal transitions. J. Clin. Investig. 119, 1429-1437.