Age‐dependent effect between MARCO and TLR4 on PMMA particle phagocytosis by macrophages
Progressive generation of total joint implant‐derived wear particles is one of the major risk factors in development of peri‐prosthetic osteolysis especially in the aging society. It is commonly accepted that macrophages predominantly drive the inflammatory response to wear debris particles. Among v...
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| creator | Yamada, Chiaki Beron‐Pelusso, Camila Algazzaz, Neira Heidari, Alireza Luz, Diogo Rawas‐Qalaji, Mutasem Toderas, Ion Mascarenhas, Ana Karina Kawai, Toshihisa Movila, Alexandru |
| description | Progressive generation of total joint implant‐derived wear particles is one of the major risk factors in development of peri‐prosthetic osteolysis especially in the aging society. It is commonly accepted that macrophages predominantly drive the inflammatory response to wear debris particles. Among various surface receptors that activate the macrophages to phagocytize particles, it is believed that the Toll‐like receptor 4 (TLR4) and the scavenger macrophage receptor with collagenous structure (MARCO) play key roles in recognition of wear debris particles. However, a strong body of evidence indicates an age‐dependent diminished function of human TLRs. Thus, we hypothesized that the MARCO receptor may be more engaged than TLRs in the phagocytosis of wear debris particles which in turn up‐regulate production of pro‐inflammatory cytokines from aged macrophages. We demonstrated that peritoneal macrophages isolated from aged mice show elevated expression of MARCO receptor compared to that from young mice. In contrast the expression of TLR4 was significantly decreased on the surface of aged macrophages. Furthermore, using anti‐MARCO and anti‐TLR4 neutralizing mAbs, we demonstrated the age‐dependent pathogenic role of MARCO, but not TLR4, receptor in promoting poly‐methyl methacrylate (PMMA) bone cement particles phagocytosis by macrophages leading to the release of pro‐inflammatory cytokines migration inhibitory factor and tumour necrosis factor in vitro. These data also suggest that the approach to neutralize MARCO may lead to the development of therapeutic regimen for the prevention of particle‐induced osteolysis in aged patients. |
| doi_str_mv | 10.1111/jcmm.14494 |
| format | Article |
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It is commonly accepted that macrophages predominantly drive the inflammatory response to wear debris particles. Among various surface receptors that activate the macrophages to phagocytize particles, it is believed that the Toll‐like receptor 4 (TLR4) and the scavenger macrophage receptor with collagenous structure (MARCO) play key roles in recognition of wear debris particles. However, a strong body of evidence indicates an age‐dependent diminished function of human TLRs. Thus, we hypothesized that the MARCO receptor may be more engaged than TLRs in the phagocytosis of wear debris particles which in turn up‐regulate production of pro‐inflammatory cytokines from aged macrophages. We demonstrated that peritoneal macrophages isolated from aged mice show elevated expression of MARCO receptor compared to that from young mice. In contrast the expression of TLR4 was significantly decreased on the surface of aged macrophages. Furthermore, using anti‐MARCO and anti‐TLR4 neutralizing mAbs, we demonstrated the age‐dependent pathogenic role of MARCO, but not TLR4, receptor in promoting poly‐methyl methacrylate (PMMA) bone cement particles phagocytosis by macrophages leading to the release of pro‐inflammatory cytokines migration inhibitory factor and tumour necrosis factor in vitro. These data also suggest that the approach to neutralize MARCO may lead to the development of therapeutic regimen for the prevention of particle‐induced osteolysis in aged patients.</description><identifier>ISSN: 1582-1838</identifier><identifier>EISSN: 1582-4934</identifier><identifier>DOI: 10.1111/jcmm.14494</identifier><identifier>PMID: 31225947</identifier><language>eng</language><publisher>England: John Wiley & Sons, Inc</publisher><subject>Age ; Aging ; Aging - metabolism ; Animals ; Antibodies, Monoclonal - pharmacology ; Antibodies, Neutralizing - pharmacology ; Bone cements ; Bone implants ; Cement ; Collagen ; Cytokines ; Detritus ; Gene expression ; Humans ; Inflammation ; Inflammation - pathology ; Inflammatory response ; Joint surgery ; Leukocyte migration ; Macrophage migration inhibitory factor ; Macrophages ; Macrophages, Peritoneal - drug effects ; Macrophages, Peritoneal - metabolism ; MARCO protein ; Mice ; Osteolysis ; Particulate matter ; Peritoneum ; Phagocytosis ; Phagocytosis - drug effects ; Polymethyl Methacrylate - chemistry ; Polymethylmethacrylate ; Receptors, Immunologic - metabolism ; Risk factors ; Senescence ; Short Communication ; Short Communications ; TLR4 protein ; Toll-Like Receptor 4 - metabolism ; Toll-like receptors ; Transplants & implants ; Tumor necrosis factor ; Tumor necrosis factor-TNF ; Tumors ; Wear particles</subject><ispartof>Journal of cellular and molecular medicine, 2019-08, Vol.23 (8), p.5827-5831</ispartof><rights>2019 The Authors. Journal of Cellular and Molecular Medicine published by John Wiley & Sons Ltd and Foundation for Cellular and Molecular Medicine.</rights><rights>2019. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5424-94cd77e0f9571d8461f7c283038532fa653fe3d009193901a95838b96ffb75793</citedby><cites>FETCH-LOGICAL-c5424-94cd77e0f9571d8461f7c283038532fa653fe3d009193901a95838b96ffb75793</cites><orcidid>0000-0001-9827-7347</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6653467/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6653467/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,1411,11542,27903,27904,45553,45554,46030,46454,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31225947$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yamada, Chiaki</creatorcontrib><creatorcontrib>Beron‐Pelusso, Camila</creatorcontrib><creatorcontrib>Algazzaz, Neira</creatorcontrib><creatorcontrib>Heidari, Alireza</creatorcontrib><creatorcontrib>Luz, Diogo</creatorcontrib><creatorcontrib>Rawas‐Qalaji, Mutasem</creatorcontrib><creatorcontrib>Toderas, Ion</creatorcontrib><creatorcontrib>Mascarenhas, Ana Karina</creatorcontrib><creatorcontrib>Kawai, Toshihisa</creatorcontrib><creatorcontrib>Movila, Alexandru</creatorcontrib><title>Age‐dependent effect between MARCO and TLR4 on PMMA particle phagocytosis by macrophages</title><title>Journal of cellular and molecular medicine</title><addtitle>J Cell Mol Med</addtitle><description>Progressive generation of total joint implant‐derived wear particles is one of the major risk factors in development of peri‐prosthetic osteolysis especially in the aging society. It is commonly accepted that macrophages predominantly drive the inflammatory response to wear debris particles. Among various surface receptors that activate the macrophages to phagocytize particles, it is believed that the Toll‐like receptor 4 (TLR4) and the scavenger macrophage receptor with collagenous structure (MARCO) play key roles in recognition of wear debris particles. However, a strong body of evidence indicates an age‐dependent diminished function of human TLRs. Thus, we hypothesized that the MARCO receptor may be more engaged than TLRs in the phagocytosis of wear debris particles which in turn up‐regulate production of pro‐inflammatory cytokines from aged macrophages. We demonstrated that peritoneal macrophages isolated from aged mice show elevated expression of MARCO receptor compared to that from young mice. In contrast the expression of TLR4 was significantly decreased on the surface of aged macrophages. Furthermore, using anti‐MARCO and anti‐TLR4 neutralizing mAbs, we demonstrated the age‐dependent pathogenic role of MARCO, but not TLR4, receptor in promoting poly‐methyl methacrylate (PMMA) bone cement particles phagocytosis by macrophages leading to the release of pro‐inflammatory cytokines migration inhibitory factor and tumour necrosis factor in vitro. These data also suggest that the approach to neutralize MARCO may lead to the development of therapeutic regimen for the prevention of particle‐induced osteolysis in aged patients.</description><subject>Age</subject><subject>Aging</subject><subject>Aging - metabolism</subject><subject>Animals</subject><subject>Antibodies, Monoclonal - pharmacology</subject><subject>Antibodies, Neutralizing - pharmacology</subject><subject>Bone cements</subject><subject>Bone implants</subject><subject>Cement</subject><subject>Collagen</subject><subject>Cytokines</subject><subject>Detritus</subject><subject>Gene expression</subject><subject>Humans</subject><subject>Inflammation</subject><subject>Inflammation - pathology</subject><subject>Inflammatory response</subject><subject>Joint surgery</subject><subject>Leukocyte migration</subject><subject>Macrophage migration inhibitory factor</subject><subject>Macrophages</subject><subject>Macrophages, Peritoneal - drug effects</subject><subject>Macrophages, Peritoneal - metabolism</subject><subject>MARCO protein</subject><subject>Mice</subject><subject>Osteolysis</subject><subject>Particulate matter</subject><subject>Peritoneum</subject><subject>Phagocytosis</subject><subject>Phagocytosis - drug effects</subject><subject>Polymethyl Methacrylate - chemistry</subject><subject>Polymethylmethacrylate</subject><subject>Receptors, Immunologic - metabolism</subject><subject>Risk factors</subject><subject>Senescence</subject><subject>Short Communication</subject><subject>Short Communications</subject><subject>TLR4 protein</subject><subject>Toll-Like Receptor 4 - metabolism</subject><subject>Toll-like receptors</subject><subject>Transplants & implants</subject><subject>Tumor necrosis factor</subject><subject>Tumor necrosis factor-TNF</subject><subject>Tumors</subject><subject>Wear particles</subject><issn>1582-1838</issn><issn>1582-4934</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kctu1DAYRiNERUthwwMgS2wQ0rS-XzZIoxFXTVRUlQ0by3F-TzNK4hBnqGbHI_CMPAkeZloVFvXGln107M9fUbwg-Izkcb72XXdGODf8UXFChKYzbhh_fFgTzfRx8TSlNcZMEmaeFMeMUCoMVyfFt_kKfv_8VcMAfQ39hCAE8BOqYLoB6FE5v1xcINfX6Gp5yVHs0ZeynKPBjVPjW0DDtVtFv51iahKqtqhzfoy7TUjPiqPg2gTPD_Np8fX9u6vFx9ny4sOnxXw584JTPjPc10oBDkYoUmsuSVCeaoaZFowGJwULwGqMDTHMYOKMyIkqI0OolFCGnRZv995hU3VQ-5xidK0dxqZz49ZG19h_T_rm2q7iDyuzmkuVBa8PgjF-30CabNckD23reoibZCnlQjKuKMvoq__QddyMfY5nKTfSYKP1wxQjkmnCxe7aN3sq_1hKI4S7JxNsd8XaXbH2b7EZfnk_5B1622QGyB64aVrYPqCynxdluZf-AetArDo</recordid><startdate>201908</startdate><enddate>201908</enddate><creator>Yamada, Chiaki</creator><creator>Beron‐Pelusso, Camila</creator><creator>Algazzaz, Neira</creator><creator>Heidari, Alireza</creator><creator>Luz, Diogo</creator><creator>Rawas‐Qalaji, Mutasem</creator><creator>Toderas, Ion</creator><creator>Mascarenhas, Ana Karina</creator><creator>Kawai, Toshihisa</creator><creator>Movila, Alexandru</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</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>3V.</scope><scope>7QP</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9827-7347</orcidid></search><sort><creationdate>201908</creationdate><title>Age‐dependent effect between MARCO and TLR4 on PMMA particle phagocytosis by macrophages</title><author>Yamada, Chiaki ; Beron‐Pelusso, Camila ; Algazzaz, Neira ; Heidari, Alireza ; Luz, Diogo ; Rawas‐Qalaji, Mutasem ; Toderas, Ion ; Mascarenhas, Ana Karina ; Kawai, Toshihisa ; Movila, Alexandru</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5424-94cd77e0f9571d8461f7c283038532fa653fe3d009193901a95838b96ffb75793</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Age</topic><topic>Aging</topic><topic>Aging - metabolism</topic><topic>Animals</topic><topic>Antibodies, Monoclonal - pharmacology</topic><topic>Antibodies, Neutralizing - pharmacology</topic><topic>Bone cements</topic><topic>Bone implants</topic><topic>Cement</topic><topic>Collagen</topic><topic>Cytokines</topic><topic>Detritus</topic><topic>Gene expression</topic><topic>Humans</topic><topic>Inflammation</topic><topic>Inflammation - pathology</topic><topic>Inflammatory response</topic><topic>Joint surgery</topic><topic>Leukocyte migration</topic><topic>Macrophage migration inhibitory factor</topic><topic>Macrophages</topic><topic>Macrophages, Peritoneal - drug effects</topic><topic>Macrophages, Peritoneal - metabolism</topic><topic>MARCO protein</topic><topic>Mice</topic><topic>Osteolysis</topic><topic>Particulate matter</topic><topic>Peritoneum</topic><topic>Phagocytosis</topic><topic>Phagocytosis - drug effects</topic><topic>Polymethyl Methacrylate - chemistry</topic><topic>Polymethylmethacrylate</topic><topic>Receptors, Immunologic - metabolism</topic><topic>Risk factors</topic><topic>Senescence</topic><topic>Short Communication</topic><topic>Short Communications</topic><topic>TLR4 protein</topic><topic>Toll-Like Receptor 4 - metabolism</topic><topic>Toll-like receptors</topic><topic>Transplants & implants</topic><topic>Tumor necrosis factor</topic><topic>Tumor necrosis factor-TNF</topic><topic>Tumors</topic><topic>Wear particles</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yamada, Chiaki</creatorcontrib><creatorcontrib>Beron‐Pelusso, Camila</creatorcontrib><creatorcontrib>Algazzaz, Neira</creatorcontrib><creatorcontrib>Heidari, Alireza</creatorcontrib><creatorcontrib>Luz, Diogo</creatorcontrib><creatorcontrib>Rawas‐Qalaji, Mutasem</creatorcontrib><creatorcontrib>Toderas, Ion</creatorcontrib><creatorcontrib>Mascarenhas, Ana Karina</creatorcontrib><creatorcontrib>Kawai, Toshihisa</creatorcontrib><creatorcontrib>Movila, Alexandru</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of cellular and molecular medicine</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yamada, Chiaki</au><au>Beron‐Pelusso, Camila</au><au>Algazzaz, Neira</au><au>Heidari, Alireza</au><au>Luz, Diogo</au><au>Rawas‐Qalaji, Mutasem</au><au>Toderas, Ion</au><au>Mascarenhas, Ana Karina</au><au>Kawai, Toshihisa</au><au>Movila, Alexandru</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Age‐dependent effect between MARCO and TLR4 on PMMA particle phagocytosis by macrophages</atitle><jtitle>Journal of cellular and molecular medicine</jtitle><addtitle>J Cell Mol Med</addtitle><date>2019-08</date><risdate>2019</risdate><volume>23</volume><issue>8</issue><spage>5827</spage><epage>5831</epage><pages>5827-5831</pages><issn>1582-1838</issn><eissn>1582-4934</eissn><abstract>Progressive generation of total joint implant‐derived wear particles is one of the major risk factors in development of peri‐prosthetic osteolysis especially in the aging society. It is commonly accepted that macrophages predominantly drive the inflammatory response to wear debris particles. Among various surface receptors that activate the macrophages to phagocytize particles, it is believed that the Toll‐like receptor 4 (TLR4) and the scavenger macrophage receptor with collagenous structure (MARCO) play key roles in recognition of wear debris particles. However, a strong body of evidence indicates an age‐dependent diminished function of human TLRs. Thus, we hypothesized that the MARCO receptor may be more engaged than TLRs in the phagocytosis of wear debris particles which in turn up‐regulate production of pro‐inflammatory cytokines from aged macrophages. We demonstrated that peritoneal macrophages isolated from aged mice show elevated expression of MARCO receptor compared to that from young mice. In contrast the expression of TLR4 was significantly decreased on the surface of aged macrophages. Furthermore, using anti‐MARCO and anti‐TLR4 neutralizing mAbs, we demonstrated the age‐dependent pathogenic role of MARCO, but not TLR4, receptor in promoting poly‐methyl methacrylate (PMMA) bone cement particles phagocytosis by macrophages leading to the release of pro‐inflammatory cytokines migration inhibitory factor and tumour necrosis factor in vitro. These data also suggest that the approach to neutralize MARCO may lead to the development of therapeutic regimen for the prevention of particle‐induced osteolysis in aged patients.</abstract><cop>England</cop><pub>John Wiley & Sons, Inc</pub><pmid>31225947</pmid><doi>10.1111/jcmm.14494</doi><tpages>5</tpages><orcidid>https://orcid.org/0000-0001-9827-7347</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Journal of cellular and molecular medicine, 2019-08, Vol.23 (8), p.5827-5831 |
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| source | MEDLINE; DOAJ Directory of Open Access Journals; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Wiley Online Library Open Access; PubMed Central |
| subjects | Age Aging Aging - metabolism Animals Antibodies, Monoclonal - pharmacology Antibodies, Neutralizing - pharmacology Bone cements Bone implants Cement Collagen Cytokines Detritus Gene expression Humans Inflammation Inflammation - pathology Inflammatory response Joint surgery Leukocyte migration Macrophage migration inhibitory factor Macrophages Macrophages, Peritoneal - drug effects Macrophages, Peritoneal - metabolism MARCO protein Mice Osteolysis Particulate matter Peritoneum Phagocytosis Phagocytosis - drug effects Polymethyl Methacrylate - chemistry Polymethylmethacrylate Receptors, Immunologic - metabolism Risk factors Senescence Short Communication Short Communications TLR4 protein Toll-Like Receptor 4 - metabolism Toll-like receptors Transplants & implants Tumor necrosis factor Tumor necrosis factor-TNF Tumors Wear particles |
| title | Age‐dependent effect between MARCO and TLR4 on PMMA particle phagocytosis by macrophages |
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