The alpha 2 chain of collagen type VI sequesters latent proforms of matrix-metalloproteinases and modulates their activation and activity

Matrix Biology

Volumn 28, Issue 8, 2009, Pages 480-489

  Freise, Christian ^a   Erben, Ulrike ^a   Muche, Marion ^a   Farndale, Richard ^b   Zeitz, Martin ^a   Somasundaram, Rajan ^a   Ruehl, Martin ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Collagen type VI; Extracellular matrix; Fibrosis; Matrix metalloproteinases

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 6; COLLAGENASE; COLLAGENASE 3; CYTOKINE; ENZYME PRECURSOR; GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE; NEUTROPHIL COLLAGENASE; PROTEINASE; SCLEROPROTEIN; STROMELYSIN;

ALPHA CHAIN; ARTICLE; BINDING AFFINITY; CHROMATOGRAPHY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INHIBITION; ENZYME SUBSTRATE; EXTRACELLULAR MATRIX; FIBROSIS; HUMAN; HUMAN TISSUE; LIVER FIBROSIS; NEOPLASM; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN IMMOBILIZATION; PROTEIN PURIFICATION; SURFACE PLASMON RESONANCE;

BINDING, COMPETITIVE; BIOCATALYSIS; CHROMATOGRAPHY, LIQUID; COLLAGEN; COLLAGEN TYPE I; COLLAGEN TYPE VI; ENZYME ACTIVATION; ENZYME PRECURSORS; FEMALE; HUMANS; LIVER; LIVER CIRRHOSIS; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 13; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 3; MATRIX METALLOPROTEINASE 8; MATRIX METALLOPROTEINASE 9; MATRIX METALLOPROTEINASES, SECRETED; PLACENTA; PREGNANCY; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN SUBUNITS; RECOMBINANT PROTEINS;

EID: 70449720597     PISSN: 0945053X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.matbio.2009.08.001     Document Type: Article

References (75)

1. Alfthan K. Surface plasmon resonance biosensors as a tool in antibody engineering. Biosens. Bioelectron. 13 (1998) 653-663
2. Allan J.A., Docherty A.J., Barker P.J., Huskisson N.S., Reynolds J.J., and Murphy G. Binding of gelatinases A and B to type-I collagen and other matrix components. Biochem. J. 309 Pt 1 (1995) 299-306
3. Atkinson J.C., Ruhl M., Becker J., Ackermann R., and Schuppan D. Collagen VI regulates normal and transformed mesenchymal cell proliferation in vitro. Exp. Cell Res. 228 (1996) 283-291
4. Baldock C., Sherratt M.J., Shuttleworth C.A., and Kielty C.M. The supramolecular organization of collagen VI microfibrils. J. Mol. Biol. 330 (2003) 297-307
5. Bannikov G.A., Karelina T.V., Collier I.E., Marmer B.L., and Goldberg G.I. Substrate binding of gelatinase B induces its enzymatic activity in the presence of intact propeptide. J. Biol. Chem. 277 (2002) 16022-16027
6. Becker J., Schuppan D., Benzian H., Bals T., Hahn E.G., Cantaluppi C., et al. Immunohistochemical distribution of collagens types IV, V, and VI and of pro-collagens types I and III in human alveolar bone and dentine. J. Histochem. Cytochem. 34 (1986) 1417-1429
7. Bergmann U., Tuuttila A., Stetler-Stevenson W.G., and Tryggvason K. Autolytic activation of recombinant human 72 kilodalton type IV collagenase. Biochemistry 34 (1995) 2819-2825
8. Billottet C., and Jouanneau J. Tumor-stroma interactions. Bull. Cancer 95 (2008) 51-56
9. Bjorklund M., and Koivunen E. Gelatinase-mediated migration and invasion of cancer cells. Biochim. Biophys. Acta 1755 (2005) 37-69
10. Briknarova K., Gehrmann M., Banyai L., Tordai H., Patthy L., and Llinas M. Gelatin-binding region of human matrix metalloproteinase-2: solution structure, dynamics, and function of the COL-23 two-domain construct. J. Biol. Chem. 276 (2001) 27613-27621
11. Chen E.I., Li W., Godzik A., Howard E.W., and Smith J.W. A residue in the S2 subsite controls substrate selectivity of matrix metalloproteinase-2 and matrix metalloproteinase-9. J. Biol. Chem. 278 (2003) 17158-17163
12. Chu M.L., Conway D., Pan T.C., Baldwin C., Mann K., Deutzmann R., et al. Amino acid sequence of the triple-helical domain of human collagen type VI. J. Biol. Chem. 263 (1988) 18601-18606
13. Chu M.L., Mann K., Deutzmann R., Pribula-Conway D., Hsu-Chen C.C., Bernard M.P., et al. Characterization of three constituent chains of collagen type VI by peptide sequences and cDNA clones. Eur. J. Biochem. 168 (1987) 309-317
14. Davis T.M., and Wilson W.D. Determination of the refractive index increments of small molecules for correction of surface plasmon resonance data. Anal. Biochem. 284 (2000) 348-353
15. Ellerbroek S.M., Wu Y.I., and Stack M.S. Type I collagen stabilization of matrix metalloproteinase-2. Arch. Biochem. Biophys. 390 (2001) 51-56
16. Furthmayr H., Wiedemann H., Timpl R., Odermatt E., and Engel J. Electron-microscopical approach to a structural model of intima collagen. Biochem. J. 211 (1983) 303-311
17. Gerling B., Becker M., Staab D., and Schuppan D. Prediction of liver fibrosis according to serum collagen VI level in children with cystic fibrosis. N. Engl. J. Med. 336 (1997) 1611-1612
18. Gioia M., Monaco S., Fasciglione G.F., Coletti A., Modesti A., Marini S., et al. Characterization of the mechanisms by which gelatinase A, neutrophil collagenase, and membrane-type metalloproteinase MMP-14 recognize collagen I and enzymatically process the two alpha-chains. J. Mol. Biol. 368 (2007) 1101-1113
19. Gressner A.M., and Weiskirchen R. Modern pathogenetic concepts of liver fibrosis suggest stellate cells and TGF-beta as major players and therapeutic targets. J. Cell. Mol. Med. 10 (2006) 76-99
20. Hemmann S., Graf J., Roderfeld M., and Roeb E. Expression of MMPs and TIMPs in liver fibrosis-a systematic review with special emphasis on anti-fibrotic strategies. J. Hepatol. 46 (2007) 955-975
21. Howard E.W., Bullen E.C., and Banda M.J. Regulation of the auto-activation of human 72-kDa progelatinase by tissue inhibitor of metalloproteinases-2. J. Biol. Chem. 266 (1991) 13064-13069
22. Howell S.J., and Doane K.J. Type VI collagen increases cell survival and prevents anti-beta 1 integrin-mediated apoptosis. Exp. Cell Res. 241 (1998) 230-241
23. Iyengar P., Combs T.P., Shah S.J., Gouon-Evans V., Pollard J.W., Albanese C., et al. Adipocyte-secreted factors synergistically promote mammary tumorigenesis through induction of anti-apoptotic transcriptional programs and proto-oncogene stabilization. Oncogene 22 (2003) 6408-6423
24. Iyengar P., Espina V., Williams T.W., Lin Y., Berry D., Jelicks L.A., et al. Adipocyte-derived collagen VI affects early mammary tumor progression in vivo, demonstrating a critical interaction in the tumor/stroma microenvironment. J. Clin. Invest. 115 (2005) 1163-1176
25. Jozic D., Bourenkov G., Lim N.H., Visse R., Nagase H., Bode W., et al. X-ray structure of human proMMP-1: new insights into procollagenase activation and collagen binding. J. Biol. Chem. 280 (2005) 9578-9585
26. Khan T., Muise E.S., Iyengar P., Wang Z.V., Chandalia M., Abate N., et al. Metabolic dysregulation and adipose tissue fibrosis: role of collagen VI. Mol. Cell. Biol. 29 (2009) 1575-1591
27. Kielty C.M., Lees M., Shuttleworth C.A., and Woolley D. Catabolism of intact type VI collagen microfibrils: susceptibility to degradation by serine proteinases. Biochem. Biophys. Res. Commun. 191 (1993) 1230-1236
28. Knight C.G., Willenbrock F., and Murphy G. A novel coumarin-labelled peptide for sensitive continuous assays of the matrix metalloproteinases. FEBS Lett. 296 (1992) 263-266
29. Kremer E.A., Chen Y., Suzuki K., Nagase H., and Gorski J.P. Hydroxyapatite induces autolytic degradation and inactivation of matrix metalloproteinase-1 and -3. J. Bone Miner. Res. 13 (1998) 1890-1902
30. Kuo H.J., Keene D.R., and Glanville R.W. Orientation of type VI collagen monomers in molecular aggregates. Biochemistry 28 (1989) 3757-3762
31. Lauer-Fields J.L., Juska D., and Fields G.B. Matrix metalloproteinases and collagen catabolism. Biopolymers 66 (2002) 19-32
32. Lauer-Fields J.L., Whitehead J.K., Li S., Hammer R.P., Brew K., and Fields G.B. Selective modulation of matrix metalloproteinase 9 (MMP-9) functions via exosite inhibition. J. Biol. Chem. 283 (2008) 20087-20095
33. Li J., Zhang Y.P., and Kirsner R.S. Angiogenesis in wound repair: angiogenic growth factors and the extracellular matrix. Microsc. Res. Tech. 60 (2003) 107-114
34. Lichtinghagen R., Bahr M.J., Wehmeier M., Michels D., Haberkorn C.I., Arndt B., et al. Expression and coordinated regulation of matrix metalloproteinases in chronic hepatitis C and hepatitis C virus-induced liver cirrhosis. Clin. Sci. (Lond). 105 (2003) 373-382
35. Lieber C.S., Weiss D.G., and Paronetto F. Value of fibrosis markers for staging liver fibrosis in patients with precirrhotic alcoholic liver disease. Alcohol Clin. Exp. Res. 32 (2008) 1031-1039
36. Loreal O., Clement B., Schuppan D., Rescan P.Y., Rissel M., and Guillouzo A. Distribution and cellular origin of collagen VI during development and in cirrhosis. Gastroenterology 102 (1992) 980-987
37. Maquoi E., Frankenne F., Noel A., Krell H.W., Grams F., and Foidart J.M. Type IV collagen induces matrix metalloproteinase 2 activation in HT1080 fibrosarcoma cells. Exp. Cell Res. 261 (2000) 348-359
38. Morgunova E., Tuuttila A., Bergmann U., Isupov M., Lindqvist Y., Schneider G., et al. Structure of human pro-matrix metalloproteinase-2: activation mechanism revealed. Science 284 (1999) 1667-1670
39. Motrescu E.R., Blaise S., Etique N., Messaddeq N., Chenard M.P., Stoll I., et al. Matrix metalloproteinase-11/stromelysin-3 exhibits collagenolytic function against collagen VI under normal and malignant conditions. Oncogene 14 (2008) 14
40. Murphy G., and Nagase H. Progress in matrix metalloproteinase research. Mol. Aspects Med. 29 (2008) 290-308 Electronic publication 2008 May 24
41. Myint E., Brown D.J., Ljubimov A.V., Kyaw M., and Kenney M.C. Cleavage of human corneal type VI collagen alpha 3 chain by matrix metalloproteinase-2. Cornea 15 (1996) 490-496
42. Nagase H., Enghild J.J., Suzuki K., and Salvesen G. Stepwise activation mechanisms of the precursor of matrix metalloproteinase 3 (stromelysin) by proteinases and (4-aminophenyl)mercuric acetate. Biochemistry 29 (1990) 5783-5789
43. Netzel-Arnett S., Mallya S.K., Nagase H., Birkedal-Hansen H., and Van Wart H.E. Continuously recording fluorescent assays optimized for five human matrix metalloproteinases. Anal. Biochem. 195 (1991) 86-92
44. Odermatt E., Risteli J., van Delden V., and Timpl R. Structural diversity and domain composition of a unique collagenous fragment (intima collagen) obtained from human placenta. Biochem. J. 211 (1983) 295-302
45. Okada Y., Naka K., Minamoto T., Ueda Y., Oda Y., Nakanishi I., et al. Localization of type VI collagen in the lining cell layer of normal and rheumatoid synovium. Lab. Invest. 63 (1990) 647-656
46. Overall C.M. Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Mol. Biotechnol. 22 (2002) 51-86
47. Overall C.M., and Dean R.A. Degradomics: systems biology of the protease web. Pleiotropic roles of MMPs in cancer. Cancer Metastasis Rev. 25 (2006) 69-75
48. Patterson M.L., Atkinson S.J., Knauper V., and Murphy G. Specific collagenolysis by gelatinase A, MMP-2, is determined by the hemopexin domain and not the fibronectin-like domain. FEBS Lett. 503 (2001) 158-162
49. Ra H.J., and Parks W.C. Control of matrix metalloproteinase catalytic activity. Matrix Biol. 26 (2007) 587-596
50. Ray S., Lukyanov P., and Ochieng J. Members of the cystatin superfamily interact with MMP-9 and protect it from autolytic degradation without affecting its gelatinolytic activities. Biochim. Biophys. Acta 1652 (2003) 91-102
51. Ruehl M., Erben U., Schuppan D., Wagner C., Zeller A., Freise C., et al. The elongated first fibronectin type III domain of collagen XIV is an inducer of quiescence and differentiation in fibroblasts and preadipocytes. J. Biol. Chem. 280 (2005) 38537-38543
52. Ruehl M., Johannsen M., Atkinson J., Manski D., Sahin E., Somasundaram R., et al. Soluble collagen VI induces tyrosine phosphorylation of paxillin and focal adhesion kinase and activates the MAP kinase erk2 in fibroblasts. Exp. Cell Res. 250 (1999) 548-557
53. Ruehl M., Kluge M., and Dagdelen T. A fragment of collagen type VI released from cirrhotic liver induces collagen + TIMP-1 synthesis, paralleled by collagenase-3 downregulation: involvement of the TGF-beta pathway. J. Hepatol. 42 S2 (2005) 121-122
54. Ruehl M., Sahin E., Bauer M., Zeitz M., Somasundaram R., and Schuppan D. Binding of collagen VI to hepatic stellate cells co-activates platelet-derived growth factor-receptor alpha (PDGFR-alpha). J. Hepatol. 38 (2003) 82
55. Ruehl M., Somasundaram R., Schoenfelder I., Farndale R.W., Knight C.G., Schmid M., et al. The epithelial mitogen keratinocyte growth factor binds to collagens via the consensus sequence glycine-proline-hydroxyproline. J. Biol. Chem. 277 (2002) 26872-26878
56. Scherer P.E., Bickel P.E., Kotler M., and Lodish H.F. Cloning of cell-specific secreted and surface proteins by subtractive antibody screening. Nat. Biotechnol. 16 (1998) 581-586
57. Schuppan D. Connective tissue polypeptides in serum as parameters to monitor antifibrotic treatment in hepatic fibrogenesis. J. Hepatol. 13 (1991) S17-S25
58. Schuppan D., Cantaluppi M.C., Becker J., Veit A., Bunte T., Troyer D., et al. Undulin, an extracellular matrix glycoprotein associated with collagen fibrils. J. Biol. Chem. 265 (1990) 8823-8832
59. Schuppan D., Ruhlmann T., and Hahn E.G. Radioimmunoassay for human type VI collagen and its application to tissue and body fluids. Anal. Biochem. 149 (1985) 238-247
60. Schuppan D., Schmid M., Somasundaram R., Ackermann R., Ruehl M., Nakamura T., et al. Collagens in the liver extracellular matrix bind hepatocyte growth factor. Gastroenterology 114 (1998) 139-152
61. Shahin M., Schuppan D., Waldherr R., Risteli J., Risteli L., Savolainen E.R., et al. Serum procollagen peptides and collagen type VI for the assessment of activity and degree of hepatic fibrosis in schistosomiasis and alcoholic liver disease. Hepatology 15 (1992) 637-644
62. Sherman-Baust C.A., Weeraratna A.T., Rangel L.B., Pizer E.S., Cho K.R., Schwartz D.R., et al. Remodeling of the extracellular matrix through overexpression of collagen VI contributes to cisplatin resistance in ovarian cancer cells. Cancer Cells 3 (2003) 377-386
63. Somasundaram R., Ruehl M., Schaefer B., Schmid M., Ackermann R., Riecken E.O., et al. Interstitial collagens I, III, and VI sequester and modulate the multifunctional cytokine oncostatin M. J. Biol. Chem. 277 (2002) 3242-3246
64. Somasundaram R., Ruehl M., Tiling N., Ackermann R., Schmid M., Riecken E.O., et al. Collagens serve as an extracellular store of bioactive interleukin 2. J. Biol. Chem. 275 (2000) 38170-38175
65. Somasundaram R., and Schuppan D. Type I, II, III, IV, V, and VI collagens serve as extracellular ligands for the isoforms of platelet-derived growth factor (AA, BB, and AB). J. Biol. Chem. 271 (1996) 26884-26891
66. Steffensen B., Bigg H.F., and Overall C.M. The involvement of the fibronectin type II-like modules of human gelatinase A in cell surface localization and activation. J. Biol. Chem. 273 (1998) 20622-20628
67. Steffensen B., Wallon U.M., and Overall C.M. Extracellular matrix binding properties of recombinant fibronectin type II-like modules of human 72-kDa gelatinase/type IV collagenase. High affinity binding to native type I collagen but not native type IV collagen. J. Biol. Chem. 270 (1995) 11555-11566
68. Stickel F., Urbaschek R., Schuppan D., Poeschl G., Oesterling C., Conradt C., et al. Serum collagen type VI and XIV and hyaluronic acid as early indicators for altered connective tissue turnover in alcoholic liver disease. Dig. Dis. Sci. 46 (2001) 2025-2032
69. Suzuki K., Enghild J.J., Morodomi T., Salvesen G., and Nagase H. Mechanisms of activation of tissue procollagenase by matrix metalloproteinase 3 (stromelysin). Biochemistry 29 (1990) 10261-10270
70. Takasaki S., Fujiwara S., Shinkai H., and Ooshima A. Human type VI collagen: purification from human subcutaneous fat tissue and an immunohistochemical study of morphea and systemic sclerosis. J. Dermatol. 22 (1995) 480-485
71. Timpl R., and Engel J. Type VI collagen. In: Mayne R., and Burgeson R.E. (Eds). Structure and Function of Collagen Types (1987), Academic Press, Orlando, FL, USA 105-143
72. Van den Steen P.E., Van Aelst I., Hvidberg V., Piccard H., Fiten P., Jacobsen C., et al. The hemopexin and O-glycosylated domains tune gelatinase B/MMP-9 bioavailability via inhibition and binding to cargo receptors. J. Biol. Chem. 281 (2006) 18626-18637
73. Van Wart H.E., and Birkedal-Hansen H. The cysteine switch: a principle of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 5578-5582
74. Xu X., Chen Z., Wang Y., Yamada Y., and Steffensen B. Functional basis for the overlap in ligand interactions and substrate specificities of matrix metalloproteinases-9 and -2. Biochem. J. 392 (2005) 127-134
75. Xu Y., Gurusiddappa S., Rich R.L., Owens R.T., Keene D.R., Mayne R., et al. Multiple binding sites in collagen type I for the integrins alpha1beta1 and alpha2beta1. J. Biol. Chem. 275 (2000) 38981-38989