Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9): The next decade
Abstract Research on matrix metalloproteinases (MMPs) and in particular on gelatinase B, alias MMP-9, has grown exponentially in the decade 2003-2012. Structural details about flexibility of MMP-9 monomers, together with glycosylation, oligomerization, heterogeneity and instability of the wildtype e...
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| Published in | Critical reviews in biochemistry and molecular biology Vol. 48; no. 3; pp. 222 - 272 |
|---|---|
| Main Authors | , , |
| Format | Journal Article |
| Language | English |
| Published |
England
Informa Healthcare USA, Inc
01.05.2013
Taylor & Francis |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Abstract
Research on matrix metalloproteinases (MMPs) and in particular on gelatinase B, alias MMP-9, has grown exponentially in the decade 2003-2012. Structural details about flexibility of MMP-9 monomers, together with glycosylation, oligomerization, heterogeneity and instability of the wildtype enzyme explain why crystallography experiments have not yet been successful for the intact enzyme. MMP-9 may be viewed as a multidomain enzyme in which the hemopexin, the O-glycosylated and the catalytic domains yield support for attachment, articulation and catalysis, respectively. The stepwise proteolytic activation of the inactive zymogen into a catalytically active form becomes gradually better understood. Priming of activation by MMP-3 may be executed by meprins that destabilize the interaction of the aminoterminus with the third fibronectin repeat. Alternatively, autocatalytic activation may occur in the presence of molecules that tightly bind to the catalytic site and that push the cystein residue in the prodomain away from the catalytic zinc ion. Thanks to the development of degradomics technologies, substrate repertoires of MMP-9 have been defined, but it remains a challenge to determine and prove which substrates are biologically relevant. The substrate repertoire has been enlarged from extracellular to membrane-bound and efficient intracellular substrates, such as crystallins, tubulins and actins. Biological studies of MMP-9 have tuned the field from being primarily cancer-oriented towards vascular and inflammatory research. In tumor biology, it has been increasingly appreciated that MMP-9 from inflammatory cells, particularly neutrophils, co-determines prognosis and outcome. Aside from the catalytic functions executed by aminoterminal domains of MMP-9, the carboxyterminal hemopexin (PEX) domain of gelatinase B exerts non-catalytic anti-apoptotic signaling effects. The recognition that gelatinase B is induced by many pro-inflammatory cytokines, whereas its inhibitors are increased by anti-inflammatory cytokines, has generated interest to target MMP-9 in acute lethal conditions, such as bacterial meningitis, sepsis and endotoxin shock, and in acute exacerbations of chronic diseases. Previously described transcriptional regulation of MMP-9 is complemented by epigenetic checkpoints, including histone modifications and microRNAs. Because activation of proMMP-9 may be executed by other MMPs, the therapeutic dogma that MMP inhibitors need to be highly selective may be keyed down for the treatment of life-threatening conditions. When inflammation and MMP-9 fulfill beneficial functions to clear damaging protein complexes, such as in systemic autoimmune diseases, therapeutic MMP inhibition has to be avoided. In Mmp9 gene knockout mice, specific spontaneous phenotypes emerged with effects on the skeletal, reproductive and nervous systems. These findings not only have clinical correlates in bone growth and fertility, but also stimulate research on the roles of MMPs and MMP-9 in endocrinology, immunology and the neurosciences. Mmp9-deficient mice are valuable tools to define MMP-9 substrates in vivo and to study the role of this enzyme in animal models of inflammatory, vascular, neoplastic and degenerative diseases. Future challenges include solving the crystal structure, definition of the functions of covalent oligomers and heteromers in biology and pathology, life-imaging of MMP-9 activity, substrate determination in situ and the study of inhibitor effects on fertility, cancer and inflammation and in neurobiology and regenerative medicine. Such studies will better define conditions in which inhibition of MMP-9 is beneficial or has to be avoided. |
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| AbstractList | Abstract
Research on matrix metalloproteinases (MMPs) and in particular on gelatinase B, alias MMP-9, has grown exponentially in the decade 2003-2012. Structural details about flexibility of MMP-9 monomers, together with glycosylation, oligomerization, heterogeneity and instability of the wildtype enzyme explain why crystallography experiments have not yet been successful for the intact enzyme. MMP-9 may be viewed as a multidomain enzyme in which the hemopexin, the O-glycosylated and the catalytic domains yield support for attachment, articulation and catalysis, respectively. The stepwise proteolytic activation of the inactive zymogen into a catalytically active form becomes gradually better understood. Priming of activation by MMP-3 may be executed by meprins that destabilize the interaction of the aminoterminus with the third fibronectin repeat. Alternatively, autocatalytic activation may occur in the presence of molecules that tightly bind to the catalytic site and that push the cystein residue in the prodomain away from the catalytic zinc ion. Thanks to the development of degradomics technologies, substrate repertoires of MMP-9 have been defined, but it remains a challenge to determine and prove which substrates are biologically relevant. The substrate repertoire has been enlarged from extracellular to membrane-bound and efficient intracellular substrates, such as crystallins, tubulins and actins. Biological studies of MMP-9 have tuned the field from being primarily cancer-oriented towards vascular and inflammatory research. In tumor biology, it has been increasingly appreciated that MMP-9 from inflammatory cells, particularly neutrophils, co-determines prognosis and outcome. Aside from the catalytic functions executed by aminoterminal domains of MMP-9, the carboxyterminal hemopexin (PEX) domain of gelatinase B exerts non-catalytic anti-apoptotic signaling effects. The recognition that gelatinase B is induced by many pro-inflammatory cytokines, whereas its inhibitors are increased by anti-inflammatory cytokines, has generated interest to target MMP-9 in acute lethal conditions, such as bacterial meningitis, sepsis and endotoxin shock, and in acute exacerbations of chronic diseases. Previously described transcriptional regulation of MMP-9 is complemented by epigenetic checkpoints, including histone modifications and microRNAs. Because activation of proMMP-9 may be executed by other MMPs, the therapeutic dogma that MMP inhibitors need to be highly selective may be keyed down for the treatment of life-threatening conditions. When inflammation and MMP-9 fulfill beneficial functions to clear damaging protein complexes, such as in systemic autoimmune diseases, therapeutic MMP inhibition has to be avoided. In Mmp9 gene knockout mice, specific spontaneous phenotypes emerged with effects on the skeletal, reproductive and nervous systems. These findings not only have clinical correlates in bone growth and fertility, but also stimulate research on the roles of MMPs and MMP-9 in endocrinology, immunology and the neurosciences. Mmp9-deficient mice are valuable tools to define MMP-9 substrates in vivo and to study the role of this enzyme in animal models of inflammatory, vascular, neoplastic and degenerative diseases. Future challenges include solving the crystal structure, definition of the functions of covalent oligomers and heteromers in biology and pathology, life-imaging of MMP-9 activity, substrate determination in situ and the study of inhibitor effects on fertility, cancer and inflammation and in neurobiology and regenerative medicine. Such studies will better define conditions in which inhibition of MMP-9 is beneficial or has to be avoided. Research on matrix metalloproteinases (MMPs) and in particular on gelatinase B, alias MMP-9, has grown exponentially in the decade 2003-2012. Structural details about flexibility of MMP-9 monomers, together with glycosylation, oligomerization, heterogeneity and instability of the wildtype enzyme explain why crystallography experiments have not yet been successful for the intact enzyme. MMP-9 may be viewed as a multidomain enzyme in which the hemopexin, the O-glycosylated and the catalytic domains yield support for attachment, articulation and catalysis, respectively. The stepwise proteolytic activation of the inactive zymogen into a catalytically active form becomes gradually better understood. Priming of activation by MMP-3 may be executed by meprins that destabilize the interaction of the aminoterminus with the third fibronectin repeat. Alternatively, autocatalytic activation may occur in the presence of molecules that tightly bind to the catalytic site and that push the cystein residue in the prodomain away from the catalytic zinc ion. Thanks to the development of degradomics technologies, substrate repertoires of MMP-9 have been defined, but it remains a challenge to determine and prove which substrates are biologically relevant. The substrate repertoire has been enlarged from extracellular to membrane-bound and efficient intracellular substrates, such as crystallins, tubulins and actins. Biological studies of MMP-9 have tuned the field from being primarily cancer-oriented towards vascular and inflammatory research. In tumor biology, it has been increasingly appreciated that MMP-9 from inflammatory cells, particularly neutrophils, co-determines prognosis and outcome. Aside from the catalytic functions executed by aminoterminal domains of MMP-9, the carboxyterminal hemopexin (PEX) domain of gelatinase B exerts non-catalytic anti-apoptotic signaling effects. The recognition that gelatinase B is induced by many pro-inflammatory cytokines, whereas its inhibitors are increased by anti-inflammatory cytokines, has generated interest to target MMP-9 in acute lethal conditions, such as bacterial meningitis, sepsis and endotoxin shock, and in acute exacerbations of chronic diseases. Previously described transcriptional regulation of MMP-9 is complemented by epigenetic checkpoints, including histone modifications and microRNAs. Because activation of proMMP-9 may be executed by other MMPs, the therapeutic dogma that MMP inhibitors need to be highly selective may be keyed down for the treatment of life-threatening conditions. When inflammation and MMP-9 fulfill beneficial functions to clear damaging protein complexes, such as in systemic autoimmune diseases, therapeutic MMP inhibition has to be avoided. In Mmp9 gene knockout mice, specific spontaneous phenotypes emerged with effects on the skeletal, reproductive and nervous systems. These findings not only have clinical correlates in bone growth and fertility, but also stimulate research on the roles of MMPs and MMP-9 in endocrinology, immunology and the neurosciences. Mmp9-deficient mice are valuable tools to define MMP-9 substrates in vivo and to study the role of this enzyme in animal models of inflammatory, vascular, neoplastic and degenerative diseases. Future challenges include solving the crystal structure, definition of the functions of covalent oligomers and heteromers in biology and pathology, life-imaging of MMP-9 activity, substrate determination in situ and the study of inhibitor effects on fertility, cancer and inflammation and in neurobiology and regenerative medicine. Such studies will better define conditions in which inhibition of MMP-9 is beneficial or has to be avoided.Research on matrix metalloproteinases (MMPs) and in particular on gelatinase B, alias MMP-9, has grown exponentially in the decade 2003-2012. Structural details about flexibility of MMP-9 monomers, together with glycosylation, oligomerization, heterogeneity and instability of the wildtype enzyme explain why crystallography experiments have not yet been successful for the intact enzyme. MMP-9 may be viewed as a multidomain enzyme in which the hemopexin, the O-glycosylated and the catalytic domains yield support for attachment, articulation and catalysis, respectively. The stepwise proteolytic activation of the inactive zymogen into a catalytically active form becomes gradually better understood. Priming of activation by MMP-3 may be executed by meprins that destabilize the interaction of the aminoterminus with the third fibronectin repeat. Alternatively, autocatalytic activation may occur in the presence of molecules that tightly bind to the catalytic site and that push the cystein residue in the prodomain away from the catalytic zinc ion. Thanks to the development of degradomics technologies, substrate repertoires of MMP-9 have been defined, but it remains a challenge to determine and prove which substrates are biologically relevant. The substrate repertoire has been enlarged from extracellular to membrane-bound and efficient intracellular substrates, such as crystallins, tubulins and actins. Biological studies of MMP-9 have tuned the field from being primarily cancer-oriented towards vascular and inflammatory research. In tumor biology, it has been increasingly appreciated that MMP-9 from inflammatory cells, particularly neutrophils, co-determines prognosis and outcome. Aside from the catalytic functions executed by aminoterminal domains of MMP-9, the carboxyterminal hemopexin (PEX) domain of gelatinase B exerts non-catalytic anti-apoptotic signaling effects. The recognition that gelatinase B is induced by many pro-inflammatory cytokines, whereas its inhibitors are increased by anti-inflammatory cytokines, has generated interest to target MMP-9 in acute lethal conditions, such as bacterial meningitis, sepsis and endotoxin shock, and in acute exacerbations of chronic diseases. Previously described transcriptional regulation of MMP-9 is complemented by epigenetic checkpoints, including histone modifications and microRNAs. Because activation of proMMP-9 may be executed by other MMPs, the therapeutic dogma that MMP inhibitors need to be highly selective may be keyed down for the treatment of life-threatening conditions. When inflammation and MMP-9 fulfill beneficial functions to clear damaging protein complexes, such as in systemic autoimmune diseases, therapeutic MMP inhibition has to be avoided. In Mmp9 gene knockout mice, specific spontaneous phenotypes emerged with effects on the skeletal, reproductive and nervous systems. These findings not only have clinical correlates in bone growth and fertility, but also stimulate research on the roles of MMPs and MMP-9 in endocrinology, immunology and the neurosciences. Mmp9-deficient mice are valuable tools to define MMP-9 substrates in vivo and to study the role of this enzyme in animal models of inflammatory, vascular, neoplastic and degenerative diseases. Future challenges include solving the crystal structure, definition of the functions of covalent oligomers and heteromers in biology and pathology, life-imaging of MMP-9 activity, substrate determination in situ and the study of inhibitor effects on fertility, cancer and inflammation and in neurobiology and regenerative medicine. Such studies will better define conditions in which inhibition of MMP-9 is beneficial or has to be avoided. Research on matrix metalloproteinases (MMPs) and in particular on gelatinase B, alias MMP-9, has grown exponentially in the decade 2003-2012. Structural details about flexibility of MMP-9 monomers, together with glycosylation, oligomerization, heterogeneity and instability of the wildtype enzyme explain why crystallography experiments have not yet been successful for the intact enzyme. MMP-9 may be viewed as a multidomain enzyme in which the hemopexin, the O-glycosylated and the catalytic domains yield support for attachment, articulation and catalysis, respectively. The stepwise proteolytic activation of the inactive zymogen into a catalytically active form becomes gradually better understood. Priming of activation by MMP-3 may be executed by meprins that destabilize the interaction of the aminoterminus with the third fibronectin repeat. Alternatively, autocatalytic activation may occur in the presence of molecules that tightly bind to the catalytic site and that push the cystein residue in the prodomain away from the catalytic zinc ion. Thanks to the development of degradomics technologies, substrate repertoires of MMP-9 have been defined, but it remains a challenge to determine and prove which substrates are biologically relevant. The substrate repertoire has been enlarged from extracellular to membrane-bound and efficient intracellular substrates, such as crystallins, tubulins and actins. Biological studies of MMP-9 have tuned the field from being primarily cancer-oriented towards vascular and inflammatory research. In tumor biology, it has been increasingly appreciated that MMP-9 from inflammatory cells, particularly neutrophils, co-determines prognosis and outcome. Aside from the catalytic functions executed by aminoterminal domains of MMP-9, the carboxyterminal hemopexin (PEX) domain of gelatinase B exerts non-catalytic anti-apoptotic signaling effects. The recognition that gelatinase B is induced by many pro-inflammatory cytokines, whereas its inhibitors are increased by anti-inflammatory cytokines, has generated interest to target MMP-9 in acute lethal conditions, such as bacterial meningitis, sepsis and endotoxin shock, and in acute exacerbations of chronic diseases. Previously described transcriptional regulation of MMP-9 is complemented by epigenetic checkpoints, including histone modifications and microRNAs. Because activation of proMMP-9 may be executed by other MMPs, the therapeutic dogma that MMP inhibitors need to be highly selective may be keyed down for the treatment of life-threatening conditions. When inflammation and MMP-9 fulfill beneficial functions to clear damaging protein complexes, such as in systemic autoimmune diseases, therapeutic MMP inhibition has to be avoided. In Mmp9 gene knockout mice, specific spontaneous phenotypes emerged with effects on the skeletal, reproductive and nervous systems. These findings not only have clinical correlates in bone growth and fertility, but also stimulate research on the roles of MMPs and MMP-9 in endocrinology, immunology and the neurosciences. Mmp9-deficient mice are valuable tools to define MMP-9 substrates in vivo and to study the role of this enzyme in animal models of inflammatory, vascular, neoplastic and degenerative diseases. Future challenges include solving the crystal structure, definition of the functions of covalent oligomers and heteromers in biology and pathology, life-imaging of MMP-9 activity, substrate determination in situ and the study of inhibitor effects on fertility, cancer and inflammation and in neurobiology and regenerative medicine. Such studies will better define conditions in which inhibition of MMP-9 is beneficial or has to be avoided. |
| Author | Opdenakker, Ghislain Vandooren, Jennifer Van den Steen, Philippe E. |
| Author_xml | – sequence: 1 givenname: Jennifer surname: Vandooren fullname: Vandooren, Jennifer email: Ghislain.Opdenakker@rega.kuleuven.be, Ghislain.Opdenakker@rega.kuleuven.be organization: Laboratory of Immunobiology, Rega Institute for Medical Research, University of Leuven, KU Leuven, Belgium – sequence: 2 givenname: Philippe E. surname: Van den Steen fullname: Van den Steen, Philippe E. email: Ghislain.Opdenakker@rega.kuleuven.be, Ghislain.Opdenakker@rega.kuleuven.be organization: Laboratory of Immunobiology, Rega Institute for Medical Research, University of Leuven, KU Leuven, Belgium – sequence: 3 givenname: Ghislain surname: Opdenakker fullname: Opdenakker, Ghislain email: Ghislain.Opdenakker@rega.kuleuven.be, Ghislain.Opdenakker@rega.kuleuven.be organization: Laboratory of Immunobiology, Rega Institute for Medical Research, University of Leuven, KU Leuven, Belgium |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23547785$$D View this record in MEDLINE/PubMed |
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Research on matrix metalloproteinases (MMPs) and in particular on gelatinase B, alias MMP-9, has grown exponentially in the decade 2003-2012.... Research on matrix metalloproteinases (MMPs) and in particular on gelatinase B, alias MMP-9, has grown exponentially in the decade 2003-2012. Structural... |
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| SubjectTerms | Amino Acid Sequence Animals Enzyme Activation Gelatinase B Gene Expression Regulation Humans Matrix Metalloproteinase 9 - chemistry Matrix Metalloproteinase 9 - genetics Matrix Metalloproteinase 9 - metabolism MMP-9 Models, Molecular Molecular Sequence Data pathology physiology Protein Processing, Post-Translational regulation structure |
| Title | Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9): The next decade |
| URI | https://www.tandfonline.com/doi/abs/10.3109/10409238.2013.770819 https://www.ncbi.nlm.nih.gov/pubmed/23547785 https://www.proquest.com/docview/1357497781 |
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