Tumor necrosis factor-α-accelerated degradation of type I collagen in human skin is associated with elevated matrix metalloproteinase (MMP)-1 and MMP-3 ex vivo

European Journal of Cell Biology

Volumn 94, Issue 1, 2015, Pages 12-21

  Ågren, Magnus S ^a,b   Schnabel, Reinhild ^c   Christensen, Lise H ^a   Mirastschijski, Ursula ^d,e  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d KLINIKUM BREMEN MITTE   (Germany)

^e UNIVERSITY OF BREMEN   (Germany)

Author keywords

Aging; C terminal telopeptide of type I collagen; Cytokine; Extracellular matrix proteins; Protease inhibitors; Type I C terminal collagen propeptide; UK370106

Indexed keywords

COLLAGEN TYPE 1; COLLAGENASE 3; GELATINASE A; ILOMASTAT; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE 14; MONOCLONAL ANTIBODY; NEUTROPHIL COLLAGENASE; STROMELYSIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TUMOR NECROSIS FACTOR ALPHA; MMP1 PROTEIN, HUMAN;

ADULT; APOPTOSIS; ARTICLE; COLLAGEN DEGRADATION; COLLAGEN METABOLISM; COLLAGEN SYNTHESIS; CONTROLLED STUDY; DOWN REGULATION; EPIDERMIS; EX VIVO STUDY; EXPLANT; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MIDDLE AGED; SKIN; TISSUE LEVEL; UPREGULATION; YOUNG ADULT; AGE; AGED; CYTOLOGY; DRUG EFFECTS; ENZYMOLOGY; IN VITRO STUDY; METABOLISM;

ADULT; AGE FACTORS; AGED; APOPTOSIS; COLLAGEN TYPE I; HUMANS; IN VITRO TECHNIQUES; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 3; MIDDLE AGED; SKIN; TUMOR NECROSIS FACTOR-ALPHA; YOUNG ADULT;

EID: 84939257251     PISSN: 01719335     EISSN: 16181298     Source Type: Journal    
DOI: 10.1016/j.ejcb.2014.10.001     Document Type: Article

References (40)

1. Ågren M.S., Andersen T.L., Andersen L., Schiødt C.B., Surve V., Andreassen T.T., et al. Nonselective matrix metalloproteinase but not tumor necrosis factor-alpha inhibition effectively preserves the early critical colon anastomotic integrity. Int. J. Colorectal Dis. 2011, 26:329-337.
2. Ågren M.S., Andersen T.L., Mirastschijski U., Syk I., Schiødt C.B., Surve V., et al. Action of matrix metalloproteinases at restricted sites in colon anastomosis repair: an immunohistochemical and biochemical study. Surgery 2006, 140:72-82.
3. Bashir M.M., Sharma M.R., Werth V.P. TNF-alpha production in the skin. Arch. Dermatol. Res. 2009, 301:87-91.
4. Boström P., Söderström M., Vahlberg T., Söderström K.O., Roberts P.J., Carpén O., et al. MMP-1 expression has an independent prognostic value in breast cancer. BMC Cancer 2011, 11:348.
5. Brew K., Nagase H. The tissue inhibitors of metalloproteinases (TIMPs): an ancient family with structural and functional diversity. Biochim. Biophys. Acta 2010, 1803:55-71.
6. Canty E.G., Kadler K.E. Procollagen trafficking, processing and fibrillogenesis. J. Cell Sci. 2005, 118:1341-1353.
7. Crabbe T., O'Connell J.P., Smith B.J., Docherty A.J. Reciprocated matrix metalloproteinase activation: a process performed by interstitial collagenase and progelatinase A. Biochemistry 1994, 33:14419-14425.
8. Fields G.B. Interstitial collagen catabolism. J. Biol. Chem. 2013, 288:8785-8793.
9. Fitzpatrick T.B. The validity and practicality of sun-reactive skin types I through VI. Arch. Dermatol. 1988, 124:869-871.
10. Fray M.J., Dickinson R.P., Huggins J.P., Occleston N.L. A potent, selective inhibitor of matrix metalloproteinase-3 for the topical treatment of chronic dermal ulcers. J. Med. Chem. 2003, 46:3514-3525.
11. Furukawa F., Huff J.C., Weston W.L., Norris D.A. Serum-free serial culture of adult human keratinocytes from suction-blister roof epidermis. J. Invest. Dermatol. 1987, 89:460-463.
12. Garnero P., Ferreras M., Karsdal M.A., Nicamhlaoibh R., Risteli J., Borel O., et al. The type I collagen fragments ICTP and CTX reveal distinct enzymatic pathways of bone collagen degradation. J. Bone Miner. Res. 2003, 18:859-867.
13. Han Y.P., Nien Y.D., Garner W.L. Tumor necrosis factor-alpha-induced proteolytic activation of pro-matrix metalloproteinase-9 by human skin is controlled by down-regulating tissue inhibitor of metalloproteinase-1 and mediated by tissue-associated chymotrypsin-like proteinase. J. Biol. Chem. 2002, 277:27319-27327.
14. Han Y.P., Tuan T.L., Wu H., Hughes M., Garner W.L. TNF-alpha stimulates activation of pro-MMP2 in human skin through NF-(kappa)B mediated induction of MT1-MMP. J. Cell Sci. 2001, 114:131-139.
15. Harrison C.A., Gossiel F., Bullock A.J., Sun T., Blumsohn A., Mac Neil S. Investigation of keratinocyte regulation of collagen I synthesis by dermal fibroblasts in a simple in vitro model. Br. J. Dermatol. 2006, 154:401-410.
16. Henriksen N.A., Sørensen L.T., Jorgensen L.N., Ågren M.S. Circulating levels of matrix metalloproteinases and tissue inhibitors of metalloproteinases in patients with incisional hernia. Wound Repair Regen. 2013, 21:661-666.
17. Kerkvliet E.H., Docherty A.J., Beertsen W., Everts V. Collagen breakdown in soft connective tissue explants is associated with the level of active gelatinase A (MMP-2) but not with collagenase. Matrix Biol. 1999, 18:373-380.
18. Kleszczyski K., Fischer T.W. Development of a short-term human full-thickness skin organ culture model in vitro under serum-free conditions. Arch. Dermatol. Res. 2012, 304:579-587.
19. Koob T.J., Jeffrey J.J., Eisen A.Z., Bauer E.A. Hormonal interactions in mammalian collagenase regulation. Comparative studies in human skin and rat uterus. Biochim. Biophys. Acta 1980, 629:13-23.
20. Kopanska K.S., Powell J.J., Jugdaohsingh R., Bruggraber S.F. Filtration of dermal fibroblast-conditioned culture media is required for the reliable quantitation of cleaved carboxy-terminal peptide of collagen type I (CICP) by ELISA. Arch. Dermatol. Res. 2013, 305:741-745.
21. Limb G.A., Matter K., Murphy G., Cambrey A.D., Bishop P.N., Morris G.E., et al. Matrix metalloproteinase-1 associates with intracellular organelles and confers resistance to lamin A/C degradation during apoptosis. Am. J. Pathol. 2005, 166:1555-1563.
22. Lovell C.R., Smolenski K.A., Duance V.C., Light N.D., Young S., Dyson M. Type I and III collagen content and fibre distribution in normal human skin during ageing. Br. J. Dermatol. 1987, 117:419-428.
23. Meikle M.C., Atkinson S.J., Ward R.V., Murphy G., Reynolds J.J. Gingival fibroblasts degrade type I collagen films when stimulated with tumor necrosis factor and interleukin 1: evidence that breakdown is mediated by metalloproteinases. J. Periodont. Res. 1989, 24:207-213.
24. Mirastschijski U., Impola U., Karsdal M.A., Saarialho-Kere U., Ågren M.S. Matrix metalloproteinase inhibitor BB-3103 unlike the serine proteinase inhibitor aprotinin abrogates epidermal healing of human skin wounds ex vivo. J. Invest. Dermatol 2002, 118:55-64.
25. Mol M.A., van den Berg R.M., Benschop H.P. Involvement of caspases and transmembrane metalloproteases in sulphur mustard-induced microvesication in adult human skin in organ culture: directions for therapy. Toxicology 2009, 258:39-46.
26. Murphy G., Allan J.A., Willenbrock F., Cockett M.I., O'Connell J.P., Docherty A.J. The role of the C-terminal domain in collagenase and stromelysin specificity. J. Biol. Chem. 1992, 267:9612-9618.
27. Nagase H., Visse R., Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc. Res. 2006, 69:562-573.
28. Ovens A., Joule J.A., Kadler K.E. Design and synthesis of acidic dipeptide hydroxamate inhibitors of procollagen C-proteinase. J. Pept. Sci. 2000, 6:489-495.
29. Ra H.J., Parks W.C. Control of matrix metalloproteinase catalytic activity. Matrix Biol. 2007, 26:587-596.
30. Ravanti L., Heino J., López-Otin C., Kähäri V.M. Induction of collagenase-3 (MMP-13) expression in human skin fibroblasts by three-dimensional collagen is mediated by p38 mitogen-activated protein kinase. J. Biol. Chem. 1999, 274:2446-2455.
31. Sabeh F., Li X.Y., Saunders T.L., Rowe R.G., Weiss S.J. Secreted versus membrane-anchored collagenases: relative roles in fibroblast-dependent collagenolysis and invasion. J. Biol. Chem. 2009, 284:23001-23011.
32. Salsas-Escat R., Nerenberg P.S., Stultz C.M. Cleavage site specificity and conformational selection in type I collagen degradation. Biochemistry 2010, 49:4147-4158.
33. Skaland I., Nordhus M., Gudlaugsson E., Klos J., Kjellevold K.H., Janssen E.A., et al. Evaluation of 5 different labeled polymer immunohistochemical detection systems. Appl. Immunohistochem. Mol. Morphol. 2010, 18:90-96.
34. Suzuki K., Enghild J.J., Morodomi T., Salvesen G., Nagase H. Mechanisms of activation of tissue procollagenase by matrix metalloproteinase 3 (stromelysin). Biochemistry 1990, 29:10261-10270.
35. Tandara A.A., Mustoe T.A. MMP- and TIMP-secretion by human cutaneous keratinocytes and fibroblasts - impact of coculture and hydration. J. Plast. Reconstr. Aesthetic Surg. 2011, 64:108-116.
36. Tavakkol A., Varani J., Elder J.T., Zouboulis C.C. Maintenance of human skin in organ culture: role for insulin-like growth factor-1 receptor and epidermal growth factor receptor. Arch. Dermatol. Res. 1999, 291:643-651.
37. Wagenaar-Miller R.A., Engelholm L.H., Gavard J., Yamada S.S., Gutkind J.S., Behrendt N., et al. Complementary roles of intracellular and pericellular collagen degradation pathways in vivo. Mol. Cell. Biol. 2007, 27:6309-6322.
38. Welgus H.G., Jeffrey J.J., Eisen A.Z. The collagen substrate specificity of human skin fibroblast collagenase. J. Biol. Chem. 1981, 256:9511-9515.
39. Wong W.R., Kossodo S., Kochevar I.E. Influence of cytokines on matrix metalloproteinases produced by fibroblasts cultured in monolayer and collagen gels. J. Formos. Med. Assoc. 2001, 100:377-382.
40. Zimmermann M., Koreck A., Meyer N., Basinski T., Meiler F., Simone B., et al. TNF-like weak inducer of apoptosis (TWEAK) and TNF-alpha cooperate in the induction of keratinocyte apoptosis. J. Allergy Clin. Immunol. 2011, 127:200-207.