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Cell and Tissue Research

, Volume 351, Issue 2, pp 255–268 | Cite as

Matrix metalloproteinases and epidermal wound repair

  • Vera L. Martins
  • Matthew Caley
  • Edel A. O’TooleEmail author
Review

Abstract

Epidermal wound healing is a complex and highly coordinated process where several different cell types and molecules, such as growth factors and extracellular matrix (ECM) components, play an important role. Among the many proteins that are essential for the restoration of tissue integrity is the metalloproteinase (MMP) family. MMPs can act on ECM and non-ECM components affecting degradation and modulation of the ECM, growth-factor activation and cell–cell and cell–matrix signalling. MMPs are secreted by different cell types such as keratinocytes, fibroblasts and inflammatory cells at different stages and locations during wound healing, thereby regulating this process in a very coordinated and controlled way. In this article, we review the role of MMPs and their inhibitors (TIMPs), as well as the disintegrin and metalloproteinase with the thrombospondin motifs (ADAMs) family, in epithelial wound repair.

Keywords

Wound Epidermis Keratinocyte MMP TIMPs 

References

  1. Ahokas K, Skoog T, Suomela S, Jeskanen L, Impola U et al (2005) Matrilysin-2 (matrix metalloproteinase-26) is upregulated in keratinocytes during wound repair and early skin carcinogenesis. J Invest Dermatol 124:849–856PubMedCrossRefGoogle Scholar
  2. Atkinson JJ, Toennies HM, Holmbeck K, Senior RM (2007) Membrane type 1 matrix metalloproteinase is necessary for distal airway epithelial repair and keratinocyte growth factor receptor expression after acute injury. Am J Physiol Lung Cell Mol Physiol 293:L600–L610PubMedCrossRefGoogle Scholar
  3. Baker AH, Edwards DR, Murphy G (2002) Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci 115:3719–3727PubMedCrossRefGoogle Scholar
  4. Betsuyaku T, Fukuda Y, Parks WC, Shipley JM, Senior RM (2000) Gelatinase B is required for alveolar bronchiolization after intratracheal bleomycin. Am J Pathol 157:525–535PubMedCrossRefGoogle Scholar
  5. Blaydon DC, Biancheri P, Di WL, Plagnol V, Cabral RM et al (2011) Inflammatory skin and bowel disease linked to ADAM17 deletion. N Engl J Med 365:1502–1508PubMedCrossRefGoogle Scholar
  6. Bullard KM, Lund L, Mudgett JS, Mellin TN, Hunt TK et al (1999a) Impaired wound contraction in stromelysin-1-deficient mice. Ann Surg 230:260–265PubMedCrossRefGoogle Scholar
  7. Bullard KM, Mudgett J, Scheuenstuhl H, Hunt TK, Banda MJ (1999b) Stromelysin-1-deficient fibroblasts display impaired contraction in vitro. J Surg Res 84:31–34PubMedCrossRefGoogle Scholar
  8. Bullen EC, Longaker MT, Updike DL, Benton R, Ladin D et al (1995) Tissue inhibitor of metalloproteinases-1 is decreased and activated gelatinases are increased in chronic wounds. J Invest Dermatol 104:236–240PubMedCrossRefGoogle Scholar
  9. Castaneda FE, Walia B, Vijay-Kumar M, Patel NR, Roser S et al (2005) Targeted deletion of metalloproteinase 9 attenuates experimental colitis in mice: central role of epithelial-derived MMP. Gastroenterology 129:1991–2008PubMedCrossRefGoogle Scholar
  10. Chen P, Parks WC (2009) Role of matrix metalloproteinases in epithelial migration. J Cell Biochem 108:1233–1243PubMedCrossRefGoogle Scholar
  11. Chen P, Abacherli LE, Nadler ST, Wang Y, Li Q, Parks WC (2009) MMP7 shedding of syndecan-1 facilitates re-epithelialization by affecting alpha(2)beta(1) integrin activation. PLoS One 4:e6565PubMedCrossRefGoogle Scholar
  12. Chin GA, Thigpin TG, Perrin KJ, Moldawer LL, Schultz GS (2003) Treatment of chronic ulcers in diabetic patients with a topical metalloproteinase inhibitor, doxycycline. Wounds 15:315–323Google Scholar
  13. Clark RAF (1995) Wound repair: overview and general considerations. In: Clark RAF (ed) The molecular and cellular biology of wound repair (second edition). Plenum, New York, pp 3–50Google Scholar
  14. Cook H, Davies KJ, Harding KG, Thomas DW (2000) Defective extracellular matrix reorganization by chronic wound fibroblasts is associated with alterations in TIMP-1, TIMP-2, and MMP-2 activity. J Invest Dermatol 115:225–233PubMedCrossRefGoogle Scholar
  15. Cornelius LA, Nehring LC, Harding E, Bolanowski M, Welgus HG et al (1998) Matrix metalloproteinases generate angiostatin: effects on neovascularization. J Immunol 161:6845–6852PubMedGoogle Scholar
  16. Coussens LM, Fingleton B, Matrisian LM (2002) Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 295:2387–2392PubMedCrossRefGoogle Scholar
  17. Dallas SL, Rosser JL, Mundy GR, Bonewald LF (2002) Proteolysis of latent transforming growth factor-beta (TGF-beta)-binding protein-1 by osteoclasts. A cellular mechanism for release of TGF-beta from bone matrix. J Biol Chem 277:21352–21360PubMedCrossRefGoogle Scholar
  18. Deryugina EI, Ratnikov B, Monosov E, Postnova TI, DiScipio R et al (2001) MT1-MMP initiates activation of pro-MMP-2 and integrin alphavbeta3 promotes maturation of MMP-2 in breast carcinoma cells. Exp Cell Res 263:209–223PubMedCrossRefGoogle Scholar
  19. Dunsmore SE, Saarialho-Kere UK, Roby JD, Wilson CL, Matrisian LM et al (1998) Matrilysin expression and function in airway epithelium. J Clin Invest 102:1321–1331PubMedCrossRefGoogle Scholar
  20. Edwards DR, Murphy G, Reynolds JJ, Whitham SE, Docherty AJ et al (1987) Transforming growth factor beta modulates the expression of collagenase and metalloproteinase inhibitor. EMBO J 6:1899–1904PubMedGoogle Scholar
  21. Edwards DR, Handsley MM, Pennington CJ (2008) The ADAM metalloproteinases. Mol Aspects Med 29:258–289PubMedCrossRefGoogle Scholar
  22. Endo K, Takino T, Miyamori H, Kinsen H, Yoshizaki T et al (2003) Cleavage of syndecan-1 by membrane type matrix metalloproteinase-1 stimulates cell migration. J Biol Chem 278:40764–40770PubMedCrossRefGoogle Scholar
  23. Fini ME, Parks WC, Rinehart WB, Girard MT, Matsubara M et al (1996) Role of matrix metalloproteinases in failure to re-epithelialize after corneal injury. Am J Pathol 149:1287–1302PubMedGoogle Scholar
  24. Franzke CW, Tasanen K, Borradori L, Huotari V, Bruckner-Tuderman L (2004) Shedding of collagen XVII/BP180: structural motifs influence cleavage from cell surface. J Biol Chem 279:24521–24529PubMedCrossRefGoogle Scholar
  25. Giannelli G, Falk-Marzillier J, Schiraldi O, Stetler-Stevenson WG, Quaranta V (1997) Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 277:225–228PubMedCrossRefGoogle Scholar
  26. Gill SE, Parks WC (2008) Metalloproteinases and their inhibitors: regulators of wound healing. Int J Biochem Cell Biol 40:1334–1347PubMedCrossRefGoogle Scholar
  27. Gill SE, Pape MC, Khokha R, Watson AJ, Leco KJ (2003) A null mutation for tissue inhibitor of metalloproteinases-3 (Timp-3) impairs murine bronchiole branching morphogenesis. Dev Biol 261:313–323PubMedCrossRefGoogle Scholar
  28. Gilles C, Polette M, Coraux C, Tournier JM, Meneguzzi G et al (2001) Contribution of MT1-MMP and of human laminin-5 gamma2 chain degradation to mammary epithelial cell migration. J Cell Sci 114:2967–2976PubMedGoogle Scholar
  29. Gross J, Lapiere CM (1962) Collagenolytic activity in amphibian tissues: a tissue culture assay. Proc Natl Acad Sci U S A 48:1014–1022PubMedCrossRefGoogle Scholar
  30. Gutierrez-Fernandez A, Inada M, Balbin M, Fueyo A, Pitiot AS et al (2007) Increased inflammation delays wound healing in mice deficient in collagenase-2 (MMP-8). FASEB J 21:2580–2591PubMedCrossRefGoogle Scholar
  31. Haines P, Samuel GH, Cohen H, Trojanowska M, Bujor AM (2011) Caveolin-1 is a negative regulator of MMP-1 gene expression in human dermal fibroblasts via inhibition of Erk1/2/Ets1 signaling pathway. J Dermatol Sci 64:210–216PubMedCrossRefGoogle Scholar
  32. Hakkinen L, Uitto VJ, Larjava H (2000) Cell biology of gingival wound healing. Periodontol 2000(24):127–152CrossRefGoogle Scholar
  33. Harsha A, Stojadinovic O, Brem H, Sehara-Fujisawa A, Wewer U et al (2008) ADAM12: a potential target for the treatment of chronic wounds. J Mol Med (Berl) 86:961–969CrossRefGoogle Scholar
  34. Hartenstein B, Dittrich BT, Stickens D, Heyer B, Vu TH et al (2006) Epidermal development and wound healing in matrix metalloproteinase 13-deficient mice. J Invest Dermatol 126:486–496PubMedCrossRefGoogle Scholar
  35. Hasty KA, Hibbs MS, Kang AH, Mainardi CL (1986) Secreted forms of human neutrophil collagenase. J Biol Chem 261:5645–5650PubMedGoogle Scholar
  36. Hattori N, Mochizuki S, Kishi K, Nakajima T, Takaishi H et al (2009) MMP-13 plays a role in keratinocyte migration, angiogenesis, and contraction in mouse skin wound healing. Am J Pathol 175:533–546PubMedCrossRefGoogle Scholar
  37. Heckmann M, Adelmann-Grill BC, Hein R, Krieg T (1993) Biphasic effects of interleukin-1 alpha on dermal fibroblasts: enhancement of chemotactic responsiveness at low concentrations and of mRNA expression for collagenase at high concentrations. J Invest Dermatol 100:780–784PubMedCrossRefGoogle Scholar
  38. Heljasvaara R, Nyberg P, Luostarinen J, Parikka M, Heikkila P et al (2005) Generation of biologically active endostatin fragments from human collagen XVIII by distinct matrix metalloproteases. Exp Cell Res 307:292–304PubMedCrossRefGoogle Scholar
  39. Hieta N, Impola U, Lopez-Otin C, Saarialho-Kere U, Kahari VM (2003) Matrix metalloproteinase-19 expression in dermal wounds and by fibroblasts in culture. J Invest Dermatol 121:997–1004PubMedCrossRefGoogle Scholar
  40. Higashiyama S, Nanba D (2005) ADAM-mediated ectodomain shedding of HB-EGF in receptor cross-talk. Biochim Biophys Acta 1751:110–117PubMedCrossRefGoogle Scholar
  41. Holmbeck K, Bianco P, Caterina J, Yamada S, Kromer M et al (1999) MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 99:81–92PubMedCrossRefGoogle Scholar
  42. Igata T, Jinnin M, Makino T, Moriya C, Muchemwa FC et al (2010) Up-regulated type I collagen expression by the inhibition of Rac1 signaling pathway in human dermal fibroblasts. Biochem Biophys Res Commun 393:101–105PubMedCrossRefGoogle Scholar
  43. Imai K, Hiramatsu A, Fukushima D, Pierschbacher MD, Okada Y (1997) Degradation of decorin by matrix metalloproteinases: identification of the cleavage sites, kinetic analyses and transforming growth factor-beta1 release. Biochem J 322(Pt 3):809–814PubMedGoogle Scholar
  44. Inoue M, Kratz G, Haegerstrand A, Stahle-Backdahl M (1995) Collagenase expression is rapidly induced in wound-edge keratinocytes after acute injury in human skin, persists during healing, and stops at re-epithelialization. J Invest Dermatol 104:479–483PubMedCrossRefGoogle Scholar
  45. Johnsen M, Lund LR, Romer J, Almholt K, Dano K (1998) Cancer invasion and tissue remodeling: common themes in proteolytic matrix degradation. Curr Opin Cell Biol 10:667–671PubMedCrossRefGoogle Scholar
  46. Juncker-Jensen A, Lund LR (2011) Phenotypic overlap between MMP-13 and the plasminogen activation system during wound healing in mice. PLoS One 6:e16954PubMedCrossRefGoogle Scholar
  47. Kajita M, Itoh Y, Chiba T, Mori H, Okada A et al (2001) Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J Cell Biol 153:893–904PubMedCrossRefGoogle Scholar
  48. Kato T, Kure T, Chang JH, Gabison EE, Itoh T et al (2001) Diminished corneal angiogenesis in gelatinase A-deficient mice. FEBS Lett 508:187–190PubMedCrossRefGoogle Scholar
  49. Kivisaari AK, Kallajoki M, Mirtti T, McGrath JA, Bauer JW et al (2008) Transformation-specific matrix metalloproteinases (MMP)-7 and MMP-13 are expressed by tumour cells in epidermolysis bullosa-associated squamous cell carcinomas. Br J Dermatol 158:778–785PubMedCrossRefGoogle Scholar
  50. Kivisaari AK, Kallajoki M, Ala-aho R, McGrath JA, Bauer JW et al (2010) Matrix metalloproteinase-7 activates heparin-binding epidermal growth factor-like growth factor in cutaneous squamous cell carcinoma. Br J Dermatol 163:726–735PubMedCrossRefGoogle Scholar
  51. Klein T, Bischoff R (2011) Active metalloproteases of the A Disintegrin and Metalloprotease (ADAM) family: biological function and structure. J Proteome Res 10:17–33PubMedCrossRefGoogle Scholar
  52. Koshikawa N, Giannelli G, Cirulli V, Miyazaki K, Quaranta V (2000) Role of cell surface metalloprotease MT1-MMP in epithelial cell migration over laminin-5. J Cell Biol 148:615–624PubMedCrossRefGoogle Scholar
  53. Krampert M, Bloch W, Sasaki T, Bugnon P, Rulicke T et al (2004) Activities of the matrix metalloproteinase stromelysin-2 (MMP-10) in matrix degradation and keratinocyte organization in wounded skin. Mol Biol Cell 15:5242–5254PubMedCrossRefGoogle Scholar
  54. Krampert M, Kuenzle S, Thai SN, Lee N, Iruela-Arispe ML, Werner S (2005) ADAMTS1 proteinase is up-regulated in wounded skin and regulates migration of fibroblasts and endothelial cells. J Biol Chem 280:23844–23852PubMedCrossRefGoogle Scholar
  55. Kure T, Chang JH, Kato T, Hernandez-Quintela E, Ye H et al (2003) Corneal neovascularization after excimer keratectomy wounds in matrilysin-deficient mice. Invest Ophthalmol Vis Sci 44:137–144PubMedCrossRefGoogle Scholar
  56. Larjava H, Haapasalmi K, Salo T, Wiebe C, Uitto VJ (1996) Keratinocyte integrins in wound healing and chronic inflammation of the human periodontium. Oral Dis 2:77–86PubMedCrossRefGoogle Scholar
  57. Lechapt-Zalcman E, Pruliere-Escabasse V, Advenier D, Galiacy S, Charriere-Bertrand C et al (2006) Transforming growth factor-beta1 increases airway wound repair via MMP-2 upregulation: a new pathway for epithelial wound repair? Am J Physiol Lung Cell Mol Physiol 290:L1277–L1282PubMedCrossRefGoogle Scholar
  58. Levi E, Fridman R, Miao HQ, Ma YS, Yayon A, Vlodavsky I (1996) Matrix metalloproteinase 2 releases active soluble ectodomain of fibroblast growth factor receptor 1. Proc Natl Acad Sci U S A 93:7069–7074PubMedCrossRefGoogle Scholar
  59. Li Q, Park PW, Wilson CL, Parks WC (2002) Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 111:635–646PubMedCrossRefGoogle Scholar
  60. Madlener M, Parks WC, Werner S (1998) Matrix metalloproteinases (MMPs) and their physiological inhibitors (TIMPs) are differentially expressed during excisional skin wound repair. Exp Cell Res 242:201–210PubMedCrossRefGoogle Scholar
  61. Maretzky T, Reiss K, Ludwig A, Buchholz J, Scholz F et al (2005) ADAM10 mediates E-cadherin shedding and regulates epithelial cell-cell adhesion, migration, and beta-catenin translocation. Proc Natl Acad Sci U S A 102:9182–9187PubMedCrossRefGoogle Scholar
  62. Matthews RT, Gary SC, Zerillo C, Pratta M, Solomon K et al (2000) Brain-enriched hyaluronan binding (BEHAB)/brevican cleavage in a glioma cell line is mediated by a disintegrin and metalloproteinase with thrombospondin motifs (ADAMTS) family member. J Biol Chem 275:22695–22703PubMedCrossRefGoogle Scholar
  63. Mauch C, Zamek J, Abety AN, Grimberg G, Fox JW, Zigrino P (2010) Accelerated wound repair in ADAM-9 knockout animals. J invest Dermatol 130:2120–2130PubMedCrossRefGoogle Scholar
  64. Mauviel A (1993) Cytokine regulation of metalloproteinase gene expression. J Cell Biochem 53:288–295PubMedCrossRefGoogle Scholar
  65. Mauviel A, Uitto J (1993) The extracellular-matrix in wound-healing — role of the cytokine network. Wounds 5:137–152Google Scholar
  66. Mazzocca A, Coppari R, De Franco R, Cho JY, Libermann TA et al (2005) A secreted form of ADAM9 promotes carcinoma invasion through tumor-stromal interactions. Cancer Res 65:4728–4738PubMedCrossRefGoogle Scholar
  67. McCawley LJ, O'Brien P, Hudson LG (1998) Epidermal growth factor (EGF)- and scatter factor/hepatocyte growth factor (SF/HGF)- mediated keratinocyte migration is coincident with induction of matrix metalloproteinase (MMP)-9. J Cell Physiol 176:255–265PubMedCrossRefGoogle Scholar
  68. McGuire JK, Li Q, Parks WC (2003) Matrilysin (matrix metalloproteinase-7) mediates E-cadherin ectodomain shedding in injured lung epithelium. Am J Pathol 162:1831–1843PubMedCrossRefGoogle Scholar
  69. Menke NB, Ward KR, Witten TM, Bonchev DG, Diegelmann RF (2007) Impaired wound healing. Clin Dermatol 25:19–25PubMedCrossRefGoogle Scholar
  70. Mignatti P, Rifkin DB (1993) Biology and biochemistry of proteinases in tumor invasion. Physiol Rev 73:161–195PubMedGoogle Scholar
  71. Mohan R, Chintala SK, Jung JC, Villar WV, McCabe F et al (2002) Matrix metalloproteinase gelatinase B (MMP-9) coordinates and effects epithelial regeneration. J Biol Chem 277:2065–2072PubMedCrossRefGoogle Scholar
  72. Moses MA, Marikovsky M, Harper JW, Vogt P, Eriksson E et al (1996) Temporal study of the activity of matrix metalloproteinases and their endogenous inhibitors during wound healing. J Cell Biochem 60:379–386PubMedCrossRefGoogle Scholar
  73. Mulholland B, Tuft SJ, Khaw PT (2005) Matrix metalloproteinase distribution during early corneal wound healing. Eye 19:584–588PubMedCrossRefGoogle Scholar
  74. Murphy G, Cockett MI, Ward RV, Docherty AJ (1991) Matrix metalloproteinase degradation of elastin, type IV collagen and proteoglycan. A quantitative comparison of the activities of 95 kDa and 72 kDa gelatinases, stromelysins-1 and -2 and punctuated metalloproteinase (PUMP). Biochem J 277(Pt 1):277–279PubMedGoogle Scholar
  75. Nagase H, Woessner JF Jr (1999) Matrix metalloproteinases. J Biol Chem 274:21491–21494PubMedCrossRefGoogle Scholar
  76. Nwomeh BC, Liang HX, Cohen IK, Yager DR (1999) MMP-8 is the predominant collagenase in healing wounds and nonhealing ulcers. J Surg Res 81:189–195PubMedCrossRefGoogle Scholar
  77. Oh J, Seo DW, Diaz T, Wei B, Ward Y et al (2004) Tissue inhibitors of metalloproteinase 2 inhibits endothelial cell migration through increased expression of RECK. Cancer Res 64:9062–9069PubMedCrossRefGoogle Scholar
  78. Okada A, Tomasetto C, Lutz Y, Bellocq JP, Rio MC, Basset P (1997) Expression of matrix metalloproteinases during rat skin wound healing: evidence that membrane type-1 matrix metalloproteinase is a stromal activator of pro-gelatinase A. J Cell Biol 137:67–77PubMedCrossRefGoogle Scholar
  79. O'Reilly MS, Wiederschain D, Stetler-Stevenson WG, Folkman J, Moses MA (1999) Regulation of angiostatin production by matrix metalloproteinase-2 in a model of concomitant resistance. J Biol Chem 274:29568–29571PubMedCrossRefGoogle Scholar
  80. O'Toole EA, Marinkovich MP, Peavey CL, Amieva MR, Furthmayr H et al (1997) Hypoxia increases human keratinocyte motility on connective tissue. J Clin Invest 100:2881–2891PubMedCrossRefGoogle Scholar
  81. O'Toole EA, van Koningsveld R, Chen M, Woodley DT (2008) Hypoxia induces epidermal keratinocyte matrix metalloproteinase-9 secretion via the protein kinase C pathway. J Cell Physiol 214:47–55PubMedCrossRefGoogle Scholar
  82. Overall CM, Lopez-Otin C (2002) Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat Rev Cancer 2:657–672PubMedCrossRefGoogle Scholar
  83. Parks WC, Wilson CL, Lopez-Boado YS (2004) Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 4:617–629PubMedCrossRefGoogle Scholar
  84. Pilcher BK, Dumin JA, Sudbeck BD, Krane SM, Welgus HG, Parks WC (1997) The activity of collagenase-1 is required for keratinocyte migration on a type I collagen matrix. J Cell Biol 137:1445–1457PubMedCrossRefGoogle Scholar
  85. Pilcher BK, Dumin J, Schwartz MJ, Mast BA, Schultz GS et al (1999) Keratinocyte collagenase-1 expression requires an epidermal growth factor receptor autocrine mechanism. J Biol Chem 274:10372–10381PubMedCrossRefGoogle Scholar
  86. Porras-Reyes BH, Blair HC, Jeffrey JJ, Mustoe TA (1991) Collagenase production at the border of granulation tissue in a healing wound: macrophage and mesenchymal collagenase production in vivo. Connect Tissue Res 27:63–71PubMedCrossRefGoogle Scholar
  87. Porter S, Clark IM, Kevorkian L, Edwards DR (2005) The ADAMTS metalloproteinases. Biochem J 386:15–27PubMedCrossRefGoogle Scholar
  88. Puente XS, Sanchez LM, Overall CM, Lopez-Otin C (2003) Human and mouse proteases: a comparative genomic approach. Nat Rev Genet 4:544–558PubMedCrossRefGoogle Scholar
  89. Qi JH, Ebrahem Q, Moore N, Murphy G, Claesson-Welsh L et al (2003) A novel function for tissue inhibitor of metalloproteinases-3 (TIMP3): inhibition of angiogenesis by blockage of VEGF binding to VEGF receptor-2. Nat Med 9:407–415PubMedCrossRefGoogle Scholar
  90. Rechardt O, Elomaa O, Vaalamo M, Paakkonen K, Jahkola T et al (2000) Stromelysin-2 is upregulated during normal wound repair and is induced by cytokines. J Invest Dermatol 115:778–787PubMedCrossRefGoogle Scholar
  91. Roy R, Wewer UM, Zurakowski D, Pories SE, Moses MA (2004) ADAM 12 cleaves extracellular matrix proteins and correlates with cancer status and stage. J Biol Chem 279:51323–51330PubMedCrossRefGoogle Scholar
  92. Ryan MC, Tizard R, VanDevanter DR, Carter WG (1994) Cloning of the LamA3 gene encoding the alpha 3 chain of the adhesive ligand epiligrin. Expression in wound repair. J Biol Chem 269:22779–22787PubMedGoogle Scholar
  93. Saarialho-Kere UK, Kovacs SO, Pentland AP, Olerud JE, Welgus HG, Parks WC (1993) Cell–matrix interactions modulate interstitial collagenase expression by human keratinocytes actively involved in wound healing. J Clin Invest 92:2858–2866PubMedCrossRefGoogle Scholar
  94. Saarialho-Kere UK, Pentland AP, Birkedal-Hansen H, Parks WC, Welgus HG (1994) Distinct populations of basal keratinocytes express stromelysin-1 and stromelysin-2 in chronic wounds. J Clin Invest 94:79–88PubMedCrossRefGoogle Scholar
  95. Saarialho-Kere UK, Vaalamo M, Puolakkainen P, Airola K, Parks WC, Karjalainen-Lindsberg ML (1996) Enhanced expression of matrilysin, collagenase, and stromelysin-1 in gastrointestinal ulcers. Am J Pathol 148:519–526PubMedGoogle Scholar
  96. Saarialho-Kere U, Kerkela E, Jahkola T, Suomela S, Keski-Oja J, Lohi J (2002) Epilysin (MMP-28) expression is associated with cell proliferation during epithelial repair. J Invest Dermatol 119:14–21PubMedCrossRefGoogle Scholar
  97. Sadowski T, Dietrich S, Koschinsky F, Sedlacek R (2003) Matrix metalloproteinase 19 regulates insulin-like growth factor-mediated proliferation, migration, and adhesion in human keratinocytes through proteolysis of insulin-like growth factor binding protein-3. Mol Biol Cell 14:4569–4580PubMedCrossRefGoogle Scholar
  98. Sahin U, Blobel CP (2007) Ectodomain shedding of the EGF-receptor ligand epigen is mediated by ADAM17. FEBS letters 581:41–44PubMedCrossRefGoogle Scholar
  99. Sahin U, Weskamp G, Kelly K, Zhou HM, Higashiyama S et al (2004) Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J Cell Biol 164:769–779PubMedCrossRefGoogle Scholar
  100. Salo T, Makela M, Kylmaniemi M, Autio-Harmainen H, Larjava H (1994) Expression of matrix metalloproteinase-2 and -9 during early human wound healing. Lab Invest 70:176–182PubMedGoogle Scholar
  101. Sandy JD, Westling J, Kenagy RD, Iruela-Arispe ML, Verscharen C et al (2001) Versican V1 proteolysis in human aorta in vivo occurs at the Glu441-Ala442 bond, a site that is cleaved by recombinant ADAMTS-1 and ADAMTS-4. J Biol Chem 276:13372–13378PubMedCrossRefGoogle Scholar
  102. Sawicki G, Marcoux Y, Sarkhosh K, Tredget EE, Ghahary A (2005) Interaction of keratinocytes and fibroblasts modulates the expression of matrix metalloproteinases-2 and -9 and their inhibitors. Mol Cell Biochem 269:209–216PubMedCrossRefGoogle Scholar
  103. Scholz F, Schulte A, Adamski F, Hundhausen C, Mittag J et al (2007) Constitutive expression and regulated release of the transmembrane chemokine CXCL16 in human and murine skin. J Invest Dermatol 127:1444–1455PubMedCrossRefGoogle Scholar
  104. Seiki M (2002) The cell surface: the stage for matrix metalloproteinase regulation of migration. Curr Opin Cell Biol 14:624–632PubMedCrossRefGoogle Scholar
  105. Sottrup-Jensen L, Birkedal-Hansen H (1989) Human fibroblast collagenase-alpha-macroglobulin interactions. Localization of cleavage sites in the bait regions of five mammalian alpha-macroglobulins. J Biol Chem 264:393–401PubMedGoogle Scholar
  106. Steffensen B, Hakkinen L, Larjava H (2001) Proteolytic events of wound-healing–coordinated interactions among matrix metalloproteinases (MMPs), integrins, and extracellular matrix molecules. Crit Rev Oral Biol Med 12:373–398PubMedCrossRefGoogle Scholar
  107. Sternlicht MD, Werb Z (2001) How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17:463–516PubMedCrossRefGoogle Scholar
  108. Stocker W, Grams F, Baumann U, Reinemer P, Gomis-Ruth FX et al (1995) The metzincins—topological and sequential relations between the astacins, adamalysins, serralysins, and matrixins (collagenases) define a superfamily of zinc-peptidases. Protein Sci 4:823–840PubMedCrossRefGoogle Scholar
  109. Strachan L, Murison JG, Prestidge RL, Sleeman MA, Watson JD, Kumble KD (2001) Cloning and biological activity of epigen, a novel member of the epidermal growth factor superfamily. J Biol Chem 276:18265–18271PubMedCrossRefGoogle Scholar
  110. Strongin AY, Collier I, Bannikov G, Marmer BL, Grant GA, Goldberg GI (1995) Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J Biol Chem 270:5331–5338PubMedCrossRefGoogle Scholar
  111. Sudbeck BD, Pilcher BK, Welgus HG, Parks WC (1997) Induction and repression of collagenase-1 by keratinocytes is controlled by distinct components of different extracellular matrix compartments. J Biol Chem 272:22103–22110PubMedCrossRefGoogle Scholar
  112. Surendran K, Simon TC, Liapis H, McGuire JK (2004) Matrilysin (MMP-7) expression in renal tubular damage: association with Wnt4. Kidney Int 65:2212–2222PubMedCrossRefGoogle Scholar
  113. Takahashi C, Sheng Z, Horan TP, Kitayama H, Maki M et al (1998) Regulation of matrix metalloproteinase-9 and inhibition of tumor invasion by the membrane-anchored glycoprotein RECK. Proc Natl Acad Sci U S A 95:13221–13226PubMedCrossRefGoogle Scholar
  114. Takeuchi T, Hisanaga M, Nagao M, Ikeda N, Fujii H et al (2004) The membrane-anchored matrix metalloproteinase (MMP) regulator RECK in combination with MMP-9 serves as an informative prognostic indicator for colorectal cancer. Clin Cancer Res 10:5572–5579PubMedCrossRefGoogle Scholar
  115. Tang BL (2001) ADAMTS: a novel family of extracellular matrix proteases. Int J Biochem Cell Biol 33:33–44PubMedCrossRefGoogle Scholar
  116. Terasaki K, Kanzaki T, Aoki T, Iwata K, Saiki I (2003) Effects of recombinant human tissue inhibitor of metalloproteinases-2 (rh-TIMP-2) on migration of epidermal keratinocytes in vitro and wound healing in vivo. J Dermatol 30:165–172PubMedGoogle Scholar
  117. Toriseva M, Kahari VM (2009) Proteinases in cutaneous wound healing. Cell Mol Life Sci 66:203–224PubMedCrossRefGoogle Scholar
  118. Tu G, Xu W, Huang H, Li S (2008) Progress in the development of matrix metalloproteinase inhibitors. Curr Med Chem 15:1388–1395PubMedCrossRefGoogle Scholar
  119. Unemori EN, Hibbs MS, Amento EP (1991) Constitutive expression of a 92-kD gelatinase (type V collagenase) by rheumatoid synovial fibroblasts and its induction in normal human fibroblasts by inflammatory cytokines. J Clin Invest 88:1656–1662PubMedCrossRefGoogle Scholar
  120. Vaalamo M, Weckroth M, Puolakkainen P, Kere J, Saarinen P et al (1996) Patterns of matrix metalloproteinase and TIMP-1 expression in chronic and normally healing human cutaneous wounds. Br J Dermatol 135:52–59PubMedCrossRefGoogle Scholar
  121. Vaalamo M, Leivo T, Saarialho-Kere U (1999) Differential expression of tissue inhibitors of metalloproteinases (TIMP-1, -2, -3, and -4) in normal and aberrant wound healing. Hum Pathol 30:795–802PubMedCrossRefGoogle Scholar
  122. Van Lint P, Libert C (2007) Chemokine and cytokine processing by matrix metalloproteinases and its effect on leukocyte migration and inflammation. J Leukoc Biol 82:1375–1381PubMedCrossRefGoogle Scholar
  123. Van Wart HE, Birkedal-Hansen H (1990) 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 87:5578–5582PubMedCrossRefGoogle Scholar
  124. Vartak DG, Gemeinhart RA (2007) Matrix metalloproteases: underutilized targets for drug delivery. J Drug Target 15:1–20PubMedCrossRefGoogle Scholar
  125. Velasco J, Li J, DiPietro L, Stepp MA, Sandy JD, Plaas A (2011) Adamts5 deletion blocks murine dermal repair through CD44-mediated aggrecan accumulation and modulation of transforming growth factor beta1 (TGFbeta1) signaling. J Biol Chem 286:26016–26027PubMedCrossRefGoogle Scholar
  126. Veves A, Sheehan P, Pham HT (2002) A randomized, controlled trial of Promogran (a collagen/oxidized regenerated cellulose dressing) vs standard treatment in the management of diabetic foot ulcers. Arch Surg 137:822–827PubMedCrossRefGoogle Scholar
  127. Vin F, Teot L, Meaume S (2002) The healing properties of Promogran in venous leg ulcers. J Wound Care 11:335–341PubMedGoogle Scholar
  128. Visse R, Nagase H (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 92:827–839PubMedCrossRefGoogle Scholar
  129. Wall SJ, Bevan D, Thomas DW, Harding KG, Edwards DR, Murphy G (2002) Differential expression of matrix metalloproteinases during impaired wound healing of the diabetes mouse. J Invest Dermatol 119:91–98PubMedCrossRefGoogle Scholar
  130. Whitelock JM, Murdoch AD, Iozzo RV, Underwood PA (1996) The degradation of human endothelial cell-derived perlecan and release of bound basic fibroblast growth factor by stromelysin, collagenase, plasmin, and heparanases. J Biol Chem 271:10079–10086PubMedCrossRefGoogle Scholar
  131. Widgerow AD (2011) Chronic wound fluid—thinking outside the box. Wound Repair Regen 19:287–291PubMedCrossRefGoogle Scholar
  132. Wild-Bode C, Fellerer K, Kugler J, Haass C, Capell A (2006) A basolateral sorting signal directs ADAM10 to adherens junctions and is required for its function in cell migration. J Biol Chem 281:23824–23829PubMedCrossRefGoogle Scholar
  133. Wilson CL, Ouellette AJ, Satchell DP, Ayabe T, Lopez-Boado YS et al (1999) Regulation of intestinal alpha-defensin activation by the metalloproteinase matrilysin in innate host defense. Science 286:113–117PubMedCrossRefGoogle Scholar
  134. Wolfsberg TG, Straight PD, Gerena RL, Huovila A-PJ, Primakoff P et al (1995) ADAM, a widely distributed and developmentally regulated gene family encoding membrane proteins with a disintegrin and metalloprotease domain. Dev Biol 169:378–383PubMedCrossRefGoogle Scholar
  135. Wysocki AB, Staiano-Coico L, Grinnell F (1993) Wound fluid from chronic leg ulcers contains elevated levels of metalloproteinases MMP-2 and MMP-9. J Invest Dermatol 101:64–68PubMedCrossRefGoogle Scholar
  136. Yager DR, Zhang LY, Liang HX, Diegelmann RF, Cohen IK (1996) Wound fluids from human pressure ulcers contain elevated matrix metalloproteinase levels and activity compared to surgical wound fluids. J Invest Dermatol 107:743–748PubMedCrossRefGoogle Scholar
  137. Yan C, Boyd DD (2007) Regulation of matrix metalloproteinase gene expression. J Cell Physiol 211:19–26PubMedCrossRefGoogle Scholar
  138. Yin J, Yu FS (2009) ERK1/2 mediate wounding- and G-protein-coupled receptor ligands-induced EGFR activation via regulating ADAM17 and HB-EGF shedding. Invest Ophthalmol Vis Sci 50:132–139PubMedCrossRefGoogle Scholar
  139. Yu Q, Stamenkovic I (2000) Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev 14:163–176PubMedGoogle Scholar
  140. Zhang X, Nothnick WB (2005) The role and regulation of the uterine matrix metalloproteinase system in menstruating and non-menstruating species. Front Biosci 10:353–366PubMedCrossRefGoogle Scholar
  141. Zhou Z, Apte SS, Soininen R, Cao R, Baaklini GY et al (2000) Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc Natl Acad Sci U S A 97:4052–4057PubMedCrossRefGoogle Scholar
  142. Zweers MC, Davidson JM, Pozzi A, Hallinger R, Janz K et al (2007) Integrin alpha2beta1 is required for regulation of murine wound angiogenesis but is dispensable for reepithelialization. J Invest Dermatol 127:467–478PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Vera L. Martins
    • 1
  • Matthew Caley
    • 1
  • Edel A. O’Toole
    • 1
    Email author
  1. 1.Centre for Cutaneous Research, Blizard Institute, Barts and the London School of Medicine and DentistryQueen Mary University of LondonLondonUK

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