The Activity of Collagenase-1 Is Required for Keratinocyte Migration on a Type I Collagen Matrix

Pilcher, Brian K.; Dumin, Jo Ann; Sudbeck, Barry D.; Krane, Stephen M.; Welgus, Howard G.; Parks, William C.

doi:10.1083/jcb.137.6.1445

Cited by 535 publications

(440 citation statements)

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“…The highest expression of tenascin is observed in unstable environments such as during cell migration, in active areas of epithelialmesenchymal interactions, and in neoplastic stroma [14,16,18,24]. Type I collagen is found throughout the connective tissue and is one of the most abundant components of the interstitial ECM [5,23,25], being highly resistant to proteases due to its unique supercoiled triple helix structure [26][27][28].…”

Section: Discussionmentioning

confidence: 99%

Expression of extracellular matrix proteins in ameloblastomas and adenomatoid odontogenic tumors

Medeiros

Nonaka

Galvão

et al. 2009

Eur Arch Otorhinolaryngol

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This study evaluated the expression of Wbronectin, tenascin and type I collagen in ameloblastomas and adenomatoid odontogenic tumors (AOTs) aiming to contribute with the comprehension of the diVerences in the biological behavior of these tumors. Immunohistochemical technique was performed in 20 cases of ameloblastoma (16 solid and 4 desmoplastic) and in 10 cases of AOT. All tumors presented moderate Wbronectin expression in the stroma. Solid ameloblastomas showed intense expression of Wbronectin at the epithelial-mesenchymal interface, whereas desmoplastic ameloblastomas revealed no immunoexpression of Wbronectin at this site. Ameloblastomas presented stronger immunoreactivity to tenascin than AOTs, especially at the epithelial-mesenchymal interface. AOTs and desmoplastic ameloblastomas showed intense labeling for type I collagen. The patterns of expression of the proteins studied agree with the locally more invasive behavior of ameloblastomas in comparison to AOTs. Our results might suggest a less invasive behavior of desmoplastic ameloblastoma in comparison to solid ameloblastoma.

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Section: Discussionmentioning

confidence: 99%

Expression of extracellular matrix proteins in ameloblastomas and adenomatoid odontogenic tumors

Medeiros

Nonaka

Galvão

et al. 2009

Eur Arch Otorhinolaryngol

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“…For example, the cleavage of laminin-5 or collagen IV results in the exposure of cryptic sites that promote migration 18,19 . Type I collagen degradation that is mediated by MMP1 is necessary for epithelial cell migration and wound healing in culture models 20 . Cleavage of ECM proteins by MMPs can also release ECM-bound growth factors, including insulin growth factors and fibroblast growth factors 21,22 .…”

Section: Functions Of Mmp Proteolysismentioning

confidence: 99%

Matrix metalloproteinases and the regulation of tissue remodelling

Page-McCaw

Ewald

Werb

2007

Nat Rev Mol Cell Biol

2,521

2,180

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Matrix metalloproteinases (MMPs) were discovered because of their role in amphibian metamorphosis, yet they have attracted more attention because of their roles in disease. Despite intensive scrutiny in vitro, in cell culture and in animal models, the normal physiological roles of these extracellular proteases have been elusive. Recent studies in mice and flies point to essential roles of MMPs as mediators of change and physical adaptation in tissues, whether developmentally regulated, environmentally induced or disease associated.The founding member of the matrix metalloproteinase (MMP) family, collagenase, was identified in 1962 by Gross and Lapiere, who found that tadpole tails during metamorphosis contained an enzyme that could degrade fibrillar collagen 1,2 . Subsequently, an interstitial collagenase, collagenase-1 or MMP1, was found in diseased skin and synovium 3 . In vitro, MMP1 initiates degradation of native fibrillar collagens, crucial components of vertebrate extracellular matrix (ECM), by cleaving the peptide bond between Gly775-Ile776 or Gly775-Lys776 in native type I, II or III collagen molecules 3,4 . Further research led to the discovery of a family of structurally related proteinases (23 in human, 24 in mice), now referred to as the MMP family.Interest in MMPs increased in the late 1960s and early 1970s following observations that MMPs are upregulated in diverse human diseases including rheumatoid arthritis and cancer. Importantly, high levels of MMPs often correlated with poor prognosis in human patients (reviewed in REF. 5 ). However, recent clinical data indicate that the relationship between § These authors contributed equally to this paper. Competing interests statementThe authors declare no competing financial interests. DATABASESThe following terms in this article are linked online to: Entrez Genome: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=gene DmMmp1 | DmMmp2 NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author ManuscriptMMPs and disease is not simple; for example, increased MMP activity can enhance tumour progression or can inhibit it (reviewed in REF. 6 ). This complex relationship between MMP expression and cancer has increased the basic and clinical interest in understanding MMP function in vivo, but it has also focused attention on MMPs and pathology, and relatively less attention has been focused on the normal roles of these enzymes. MMP proteolysisMMPs are members of the metzincin group of proteases, which are named after the zinc ion and the conserved Met residue at the active site 11,12 . Recent work has generated a unified peptidase nomenclature 13 Functions of MMP proteolysisHistorically, MMPs were thought to function mainly as enzymes that degrade structural components of the ECM. However, MMP proteolysis can create space for cells to migrate, can produce specific substrate-cleavage fragments with independent biological activity, can MMPs in bone modelling and remodellingBone is an important site of ongoing tissue remodelling during development...

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“…During cutaneous wound healing, human keratinocytes express MMP-1 while migrating over the type I collagen-rich dermis. This spatially and temporally confined expression of MMP-1 is induced by ligation of the ␣ 2 ␤ 1 integrin by dermal type I collagen (19). Both migration and MMP-1 expression induced by type I collagen are inhibited by function blocking antibodies against the ␣ 2 ␤ 1 integrin, but not by antibodies directed against the ␣ 1 ␤ 1 or ␣ 3 ␤ 1 integrins (19).…”

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confidence: 99%

“…This spatially and temporally confined expression of MMP-1 is induced by ligation of the ␣ 2 ␤ 1 integrin by dermal type I collagen (19). Both migration and MMP-1 expression induced by type I collagen are inhibited by function blocking antibodies against the ␣ 2 ␤ 1 integrin, but not by antibodies directed against the ␣ 1 ␤ 1 or ␣ 3 ␤ 1 integrins (19). Previous studies have established the role of the ␣ 2 ␤ 1 integrin as a receptor for type I collagen, as well as for type IV collagen, laminins, echovirus 1 and 8, and rotaviruses (20 -22).…”

mentioning

confidence: 99%

Structural Analysis of the α2 Integrin I Domain/Procollagenase-1 (Matrix Metalloproteinase-1) Interaction

Stricker¹,

Dumin²,

Dickeson³

et al. 2001

Journal of Biological Chemistry

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Previous studies have established that ligation of keratinocyte ␣ 2 ␤ 1 integrin by type I collagen induces expression of matrix metalloproteinase-1 (MMP-1) and that MMP-1 activity is required for the ␣ 2 ␤ 1 integrin-dependent migration of primary keratinocytes across collagenous matrices. We now present evidence that MMP-1 binds the ␣ 2 ␤ 1 integrin via the I domain of the ␣ 2 integrin subunit. Using an enzyme-linked immunosorbent assay with purified human MMP-1 and recombinant ␣ 2 integrin I domain, we showed that the ␣ 2 integrin I domain specifically bound in a divalent cation-dependent manner to both the pro and active forms of MMP-1, but not to MMP-3 or MMP-13. Although both the I domain and MMP-1 bind divalent cations, MMP-1 bound, in a divalent cation-dependent manner, to ␣ 2 integrin I domains containing metal ion-dependent adhesion sites motif mutations that prevent divalent cation binding to the I domain, demonstrating that the metal ion dependence is a function of MMP-1. Using a series of MMP-1-MMP-3 and MMP-1-MMP-13 chimeras, we determined that both the linker domain and the hemopexin-like domain of MMP-1 were required for optimal binding to the I domain. The ␣ 2 integrin/MMP-1 interaction described here extends an emerging paradigm in matrix biology involving anchoring of proteinases to the cell surface to regulate their biological activities.The extracellular matrix is not a static environment. Remodeling and degradation of the extracellular matrix is a vital component of physiological and pathophysiological processes, such as development and differentiation, cell migration, angiogenesis, wound healing, and metastasis. Matrix metalloproteinases (MMPs) 1 play a central role in the turnover of extracellular matrix components (1).MMPs constitute a large family of metal-dependent endoproteases with varying substrate specificities for many extracellular proteins. The structure of native triple helical type I collagen makes it resistant to proteolysis, and only six MMPs, MMP-1, MMP-8, MMP-13, MMP-14 (MT1-MMP), MMP-18, and MMP-2, exhibit an ability to cleave native fibrillar collagen within its triple helical domain (2-8). Similar to most MMPs, the collagenases (MMP-1, MMP-8, and MMP-13) have several structural features in common, including an N-terminal prodomain, a catalytic domain, and a short proline-rich linker connected to a hemopexin-like domain at the C terminus (9). The catalytic domain contains a Zn 2ϩ -binding site that is conserved in all MMPs and is required for catalytic activity (10, 11). The catalytic domain of the collagenases contains an additional structural Zn 2ϩ , as well as three structural Ca 2ϩ ions (12). The hemopexin-like domain contains a Ca 2ϩ and a Ca 2ϩ -Cl Ϫ ion pair (12).The three collagenases differ in patterns of tissue expression. In humans, MMP-1, which is expressed by epithelium, endothelium, fibroblasts, chondrocytes, and macrophages, seems to be the enzyme principally responsible for collagen turnover in most tissues (13-18). During cutaneous wound healing, human k...

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The Activity of Collagenase-1 Is Required for Keratinocyte Migration on a Type I Collagen Matrix

Cited by 535 publications

References 37 publications

Expression of extracellular matrix proteins in ameloblastomas and adenomatoid odontogenic tumors

Expression of extracellular matrix proteins in ameloblastomas and adenomatoid odontogenic tumors

Matrix metalloproteinases and the regulation of tissue remodelling

Structural Analysis of the α2 Integrin I Domain/Procollagenase-1 (Matrix Metalloproteinase-1) Interaction

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