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pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation
Recent studies have demonstrated that activated microglia play an important role in dopamine (DA) neuronal degeneration in Parkinson disease (PD) by generating NADPH-oxidase (NADPHO)-derived superoxide. However, the molecular mechanisms that underlie microglial activation in DA cell death are still...
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| Published in: | The FASEB journal 2007-01, Vol.21 (1), p.179-187 |
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| creator | Kim, Yoon Seong Choi, Dong Hee Block, Michelle L Lorenzl, Stefan Yang, Lichuan Kim, Youn Jung Sugama, Shuei Cho, Byung Pil Hwang, Onyou Browne, Susan E Kim, Soo Yul Hong, Jau-Shyong Beal, M. Flint Joh, Tong H |
| description | Recent studies have demonstrated that activated microglia play an important role in dopamine (DA) neuronal degeneration in Parkinson disease (PD) by generating NADPH-oxidase (NADPHO)-derived superoxide. However, the molecular mechanisms that underlie microglial activation in DA cell death are still disputed. We report here that matrix metalloproteinase-3 (MMP-3) was newly induced and activated in stressed DA cells, and the active form of MMP-3 (actMMP-3) was released into the medium. The released actMMP-3, as well as catalytically active recombinant MMP-3 (cMMP-3) led to microglial activation and superoxide generation in microglia and enhanced DA cell death. cMMP-3 caused DA cell death in mesencephalic neuron-glia mixed culture of wild-type (WT) mice, but this was attenuated in the culture of NADPHO subunit null mice (gp91phox⁻/⁻), suggesting that NADPHO mediated the cMMP-3-induced microglial production of superoxide and DA cell death. Furthermore, in the N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-injected animal model of PD, nigrostriatal DA neuronal degeneration, microglial activation, and superoxide generation were largely attenuated in MMP-3-/- mice. These results indicate that actMMP-3 released from stressed DA neurons is responsible for microglial activation and generation of NADPHO-derived superoxide and eventually enhances nigrostriatal DA neuronal degeneration. Our results could lead to a novel therapeutic approach to PD.--Kim, Y. S., Choi, D. H., Block, M. L., Lorenzl, S., Yang, L., Kim, Y. J., Sugama, S., Cho, B. P., Ywang, O., Browne, S. E., Kim, S. Y., Hong, J.-S., Beal, M. F., Jon, T. H. A pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation. |
| doi_str_mv | 10.1096/fj.06-5865com |
| format | article |
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Flint ; Joh, Tong H</creator><creatorcontrib>Kim, Yoon Seong ; Choi, Dong Hee ; Block, Michelle L ; Lorenzl, Stefan ; Yang, Lichuan ; Kim, Youn Jung ; Sugama, Shuei ; Cho, Byung Pil ; Hwang, Onyou ; Browne, Susan E ; Kim, Soo Yul ; Hong, Jau-Shyong ; Beal, M. Flint ; Joh, Tong H</creatorcontrib><description>Recent studies have demonstrated that activated microglia play an important role in dopamine (DA) neuronal degeneration in Parkinson disease (PD) by generating NADPH-oxidase (NADPHO)-derived superoxide. However, the molecular mechanisms that underlie microglial activation in DA cell death are still disputed. We report here that matrix metalloproteinase-3 (MMP-3) was newly induced and activated in stressed DA cells, and the active form of MMP-3 (actMMP-3) was released into the medium. The released actMMP-3, as well as catalytically active recombinant MMP-3 (cMMP-3) led to microglial activation and superoxide generation in microglia and enhanced DA cell death. cMMP-3 caused DA cell death in mesencephalic neuron-glia mixed culture of wild-type (WT) mice, but this was attenuated in the culture of NADPHO subunit null mice (gp91phox⁻/⁻), suggesting that NADPHO mediated the cMMP-3-induced microglial production of superoxide and DA cell death. Furthermore, in the N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-injected animal model of PD, nigrostriatal DA neuronal degeneration, microglial activation, and superoxide generation were largely attenuated in MMP-3-/- mice. These results indicate that actMMP-3 released from stressed DA neurons is responsible for microglial activation and generation of NADPHO-derived superoxide and eventually enhances nigrostriatal DA neuronal degeneration. Our results could lead to a novel therapeutic approach to PD.--Kim, Y. S., Choi, D. H., Block, M. L., Lorenzl, S., Yang, L., Kim, Y. J., Sugama, S., Cho, B. P., Ywang, O., Browne, S. E., Kim, S. Y., Hong, J.-S., Beal, M. F., Jon, T. H. A pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation.</description><identifier>ISSN: 0892-6638</identifier><identifier>EISSN: 1530-6860</identifier><identifier>DOI: 10.1096/fj.06-5865com</identifier><identifier>PMID: 17116747</identifier><language>eng</language><publisher>United States: The Federation of American Societies for Experimental Biology</publisher><subject>1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine - administration & dosage ; Animals ; Cell Death ; Cells, Cultured ; Dopamine - metabolism ; dopamine neuron protection ; Matrix Metalloproteinase 3 - metabolism ; Membrane Glycoproteins - genetics ; Membrane Glycoproteins - physiology ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Microglia - metabolism ; NADPH Oxidase 2 ; NADPH Oxidases - genetics ; NADPH Oxidases - metabolism ; NADPH Oxidases - physiology ; Neurons - metabolism ; Neurons - pathology ; Parkinson Disease - enzymology ; Parkinson Disease - metabolism ; Parkinson Disease - pathology</subject><ispartof>The FASEB journal, 2007-01, Vol.21 (1), p.179-187</ispartof><rights>FASEB</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c468M-7daa74e78e7fbf51301a140c7a2edf8b528ab0180b791dece02516e558d6e83a3</citedby><cites>FETCH-LOGICAL-c468M-7daa74e78e7fbf51301a140c7a2edf8b528ab0180b791dece02516e558d6e83a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1096%2Ffj.06-5865com$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1096%2Ffj.06-5865com$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>315,786,790,27957,27958,50923,51032</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/17116747$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kim, Yoon Seong</creatorcontrib><creatorcontrib>Choi, Dong Hee</creatorcontrib><creatorcontrib>Block, Michelle L</creatorcontrib><creatorcontrib>Lorenzl, Stefan</creatorcontrib><creatorcontrib>Yang, Lichuan</creatorcontrib><creatorcontrib>Kim, Youn Jung</creatorcontrib><creatorcontrib>Sugama, Shuei</creatorcontrib><creatorcontrib>Cho, Byung Pil</creatorcontrib><creatorcontrib>Hwang, Onyou</creatorcontrib><creatorcontrib>Browne, Susan E</creatorcontrib><creatorcontrib>Kim, Soo Yul</creatorcontrib><creatorcontrib>Hong, Jau-Shyong</creatorcontrib><creatorcontrib>Beal, M. Flint</creatorcontrib><creatorcontrib>Joh, Tong H</creatorcontrib><title>pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation</title><title>The FASEB journal</title><addtitle>FASEB J</addtitle><description>Recent studies have demonstrated that activated microglia play an important role in dopamine (DA) neuronal degeneration in Parkinson disease (PD) by generating NADPH-oxidase (NADPHO)-derived superoxide. However, the molecular mechanisms that underlie microglial activation in DA cell death are still disputed. We report here that matrix metalloproteinase-3 (MMP-3) was newly induced and activated in stressed DA cells, and the active form of MMP-3 (actMMP-3) was released into the medium. The released actMMP-3, as well as catalytically active recombinant MMP-3 (cMMP-3) led to microglial activation and superoxide generation in microglia and enhanced DA cell death. cMMP-3 caused DA cell death in mesencephalic neuron-glia mixed culture of wild-type (WT) mice, but this was attenuated in the culture of NADPHO subunit null mice (gp91phox⁻/⁻), suggesting that NADPHO mediated the cMMP-3-induced microglial production of superoxide and DA cell death. Furthermore, in the N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-injected animal model of PD, nigrostriatal DA neuronal degeneration, microglial activation, and superoxide generation were largely attenuated in MMP-3-/- mice. These results indicate that actMMP-3 released from stressed DA neurons is responsible for microglial activation and generation of NADPHO-derived superoxide and eventually enhances nigrostriatal DA neuronal degeneration. Our results could lead to a novel therapeutic approach to PD.--Kim, Y. S., Choi, D. H., Block, M. L., Lorenzl, S., Yang, L., Kim, Y. J., Sugama, S., Cho, B. P., Ywang, O., Browne, S. E., Kim, S. Y., Hong, J.-S., Beal, M. F., Jon, T. H. A pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation.</description><subject>1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine - administration & dosage</subject><subject>Animals</subject><subject>Cell Death</subject><subject>Cells, Cultured</subject><subject>Dopamine - metabolism</subject><subject>dopamine neuron protection</subject><subject>Matrix Metalloproteinase 3 - metabolism</subject><subject>Membrane Glycoproteins - genetics</subject><subject>Membrane Glycoproteins - physiology</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Microglia - metabolism</subject><subject>NADPH Oxidase 2</subject><subject>NADPH Oxidases - genetics</subject><subject>NADPH Oxidases - metabolism</subject><subject>NADPH Oxidases - physiology</subject><subject>Neurons - metabolism</subject><subject>Neurons - pathology</subject><subject>Parkinson Disease - enzymology</subject><subject>Parkinson Disease - metabolism</subject><subject>Parkinson Disease - pathology</subject><issn>0892-6638</issn><issn>1530-6860</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2007</creationdate><recordtype>article</recordtype><recordid>eNp9kDFv2zAQRomiReOkGbu2nLopvaNMip6KxIjTFgkyOJkJSjoaNCTRJWU3_vehYwPdOh3w3ePD8WPsM8IVwkx9d-srUIXUSjahf8cmKEsolFbwnk1Az0ShVKnP2HlKawBAQPWRnWGFqKppNWFp43dhtB2PoSMeHO_tGP0L7ymHXdjEMJIfbKKi5LYZ_c6Pe-4H3oaN7f1AceUbPtA2hiFLWlpRzuzow8B33vLeNzGsOp93b6_fNp_YB2e7RJenecGeF7dP85_F_ePdr_n1fdFMlX4oqtbaakqVpsrVTmIJaHEKTWUFtU7XUmhbA2qoqxm21BAIiYqk1K0iXdrygn07evMv_mwpjab3qaGuswOFbTIChC4F6gwWRzAfm1IkZzbR9zbuDYI5tGzc2oAyp5Yz_-Uk3tY9tf_oU60Z-HEE_vqO9v-3mcXyRiyul7c3vwXiIZw_PmTD16PB2WDsKvpknpcCDiWgkKLE8hVjBZiy</recordid><startdate>200701</startdate><enddate>200701</enddate><creator>Kim, Yoon Seong</creator><creator>Choi, Dong Hee</creator><creator>Block, Michelle L</creator><creator>Lorenzl, Stefan</creator><creator>Yang, Lichuan</creator><creator>Kim, Youn Jung</creator><creator>Sugama, Shuei</creator><creator>Cho, Byung Pil</creator><creator>Hwang, Onyou</creator><creator>Browne, Susan E</creator><creator>Kim, Soo Yul</creator><creator>Hong, Jau-Shyong</creator><creator>Beal, M. Flint</creator><creator>Joh, Tong H</creator><general>The Federation of American Societies for Experimental Biology</general><general>Federation of American Societies for Experimental Biology</general><scope>FBQ</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope></search><sort><creationdate>200701</creationdate><title>pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation</title><author>Kim, Yoon Seong ; Choi, Dong Hee ; Block, Michelle L ; Lorenzl, Stefan ; Yang, Lichuan ; Kim, Youn Jung ; Sugama, Shuei ; Cho, Byung Pil ; Hwang, Onyou ; Browne, Susan E ; Kim, Soo Yul ; Hong, Jau-Shyong ; Beal, M. Flint ; Joh, Tong H</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c468M-7daa74e78e7fbf51301a140c7a2edf8b528ab0180b791dece02516e558d6e83a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2007</creationdate><topic>1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine - administration & dosage</topic><topic>Animals</topic><topic>Cell Death</topic><topic>Cells, Cultured</topic><topic>Dopamine - metabolism</topic><topic>dopamine neuron protection</topic><topic>Matrix Metalloproteinase 3 - metabolism</topic><topic>Membrane Glycoproteins - genetics</topic><topic>Membrane Glycoproteins - physiology</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>Microglia - metabolism</topic><topic>NADPH Oxidase 2</topic><topic>NADPH Oxidases - genetics</topic><topic>NADPH Oxidases - metabolism</topic><topic>NADPH Oxidases - physiology</topic><topic>Neurons - metabolism</topic><topic>Neurons - pathology</topic><topic>Parkinson Disease - enzymology</topic><topic>Parkinson Disease - metabolism</topic><topic>Parkinson Disease - pathology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kim, Yoon Seong</creatorcontrib><creatorcontrib>Choi, Dong Hee</creatorcontrib><creatorcontrib>Block, Michelle L</creatorcontrib><creatorcontrib>Lorenzl, Stefan</creatorcontrib><creatorcontrib>Yang, Lichuan</creatorcontrib><creatorcontrib>Kim, Youn Jung</creatorcontrib><creatorcontrib>Sugama, Shuei</creatorcontrib><creatorcontrib>Cho, Byung Pil</creatorcontrib><creatorcontrib>Hwang, Onyou</creatorcontrib><creatorcontrib>Browne, Susan E</creatorcontrib><creatorcontrib>Kim, Soo Yul</creatorcontrib><creatorcontrib>Hong, Jau-Shyong</creatorcontrib><creatorcontrib>Beal, M. Flint</creatorcontrib><creatorcontrib>Joh, Tong H</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><jtitle>The FASEB journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kim, Yoon Seong</au><au>Choi, Dong Hee</au><au>Block, Michelle L</au><au>Lorenzl, Stefan</au><au>Yang, Lichuan</au><au>Kim, Youn Jung</au><au>Sugama, Shuei</au><au>Cho, Byung Pil</au><au>Hwang, Onyou</au><au>Browne, Susan E</au><au>Kim, Soo Yul</au><au>Hong, Jau-Shyong</au><au>Beal, M. Flint</au><au>Joh, Tong H</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation</atitle><jtitle>The FASEB journal</jtitle><addtitle>FASEB J</addtitle><date>2007-01</date><risdate>2007</risdate><volume>21</volume><issue>1</issue><spage>179</spage><epage>187</epage><pages>179-187</pages><issn>0892-6638</issn><eissn>1530-6860</eissn><notes>http://www.fasebj.org/</notes><notes>These authors contributed equally to this work.</notes><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><abstract>Recent studies have demonstrated that activated microglia play an important role in dopamine (DA) neuronal degeneration in Parkinson disease (PD) by generating NADPH-oxidase (NADPHO)-derived superoxide. However, the molecular mechanisms that underlie microglial activation in DA cell death are still disputed. We report here that matrix metalloproteinase-3 (MMP-3) was newly induced and activated in stressed DA cells, and the active form of MMP-3 (actMMP-3) was released into the medium. The released actMMP-3, as well as catalytically active recombinant MMP-3 (cMMP-3) led to microglial activation and superoxide generation in microglia and enhanced DA cell death. cMMP-3 caused DA cell death in mesencephalic neuron-glia mixed culture of wild-type (WT) mice, but this was attenuated in the culture of NADPHO subunit null mice (gp91phox⁻/⁻), suggesting that NADPHO mediated the cMMP-3-induced microglial production of superoxide and DA cell death. Furthermore, in the N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-injected animal model of PD, nigrostriatal DA neuronal degeneration, microglial activation, and superoxide generation were largely attenuated in MMP-3-/- mice. These results indicate that actMMP-3 released from stressed DA neurons is responsible for microglial activation and generation of NADPHO-derived superoxide and eventually enhances nigrostriatal DA neuronal degeneration. Our results could lead to a novel therapeutic approach to PD.--Kim, Y. S., Choi, D. H., Block, M. L., Lorenzl, S., Yang, L., Kim, Y. J., Sugama, S., Cho, B. P., Ywang, O., Browne, S. E., Kim, S. Y., Hong, J.-S., Beal, M. F., Jon, T. H. A pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation.</abstract><cop>United States</cop><pub>The Federation of American Societies for Experimental Biology</pub><pmid>17116747</pmid><doi>10.1096/fj.06-5865com</doi><tpages>9</tpages></addata></record> |
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| subjects | 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine - administration & dosage Animals Cell Death Cells, Cultured Dopamine - metabolism dopamine neuron protection Matrix Metalloproteinase 3 - metabolism Membrane Glycoproteins - genetics Membrane Glycoproteins - physiology Mice Mice, Inbred C57BL Mice, Knockout Microglia - metabolism NADPH Oxidase 2 NADPH Oxidases - genetics NADPH Oxidases - metabolism NADPH Oxidases - physiology Neurons - metabolism Neurons - pathology Parkinson Disease - enzymology Parkinson Disease - metabolism Parkinson Disease - pathology |
| title | pivotal role of matrix metalloproteinase-3 activity in dopaminergic neuronal degeneration via microglial activation |
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