Ammonium tetrathiomolybdate enhances the antitumor effects of cetuximab via the suppression of osteoclastogenesis in head and neck squamous carcinoma
Head and neck squamous cell carcinoma (HNSCC) poses a significant challenge clinically where one of the mechanisms responsible for the invasion into facial bones occurs via the activation of osteoclasts. Copper has been demonstrated to play a key role in skeletal remodeling. However, the role of cop...
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| Veröffentlicht in: | International journal of oncology 2018-03, Vol.52 (3), p.989-999 |
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| creator | Morisawa, Ayaka Okui, Tatsuo Shimo, Tsuyoshi Ibaragi, Soichiro Okusha, Yuka Ono, Mitsuaki Nguyen, Thi Thu Ha Hassan, Nur Mohammad Monsur Sasaki, Akira |
| description | Head and neck squamous cell carcinoma (HNSCC) poses a significant challenge clinically where one of the mechanisms responsible for the invasion into facial bones occurs via the activation of osteoclasts. Copper has been demonstrated to play a key role in skeletal remodeling. However, the role of copper in cancer-associated bone destruction is thus far unknown. Lysyl oxidase (LOX) is a copper-dependent enzyme that promotes osteoclastogenesis. In the present study, we investigated the effects of copper on HNSCC with bone invasion by the copper chelator, ammonium tetrathiomolybdate (TM) in vitro and in vivo. We demonstrate that TM blocks the proliferation of HNSCC cells, inhibits LOX activation and decreases the expression of the receptor activator of nuclear factor-κB ligand (RANKL) in osteoblasts and osteocytes, subsequently suppressing bone destruction. These findings suggest that copper is a potential target for the treatment of HNSCCs associated with bone destruction. |
| doi_str_mv | 10.3892/ijo.2018.4242 |
| format | Article |
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Copper has been demonstrated to play a key role in skeletal remodeling. However, the role of copper in cancer-associated bone destruction is thus far unknown. Lysyl oxidase (LOX) is a copper-dependent enzyme that promotes osteoclastogenesis. In the present study, we investigated the effects of copper on HNSCC with bone invasion by the copper chelator, ammonium tetrathiomolybdate (TM) in vitro and in vivo. We demonstrate that TM blocks the proliferation of HNSCC cells, inhibits LOX activation and decreases the expression of the receptor activator of nuclear factor-κB ligand (RANKL) in osteoblasts and osteocytes, subsequently suppressing bone destruction. These findings suggest that copper is a potential target for the treatment of HNSCCs associated with bone destruction.</description><identifier>ISSN: 1019-6439</identifier><identifier>EISSN: 1791-2423</identifier><identifier>DOI: 10.3892/ijo.2018.4242</identifier><identifier>PMID: 29328370</identifier><language>eng</language><publisher>Greece: Spandidos Publications</publisher><subject>Ammonia ; Animals ; Antineoplastic Agents, Immunological - pharmacology ; Antineoplastic Agents, Immunological - therapeutic use ; Bone marrow ; Bone Neoplasms - drug therapy ; Bone Neoplasms - pathology ; Bone Neoplasms - secondary ; Bone Resorption - drug therapy ; Bone Resorption - pathology ; Carcinoma, Squamous Cell - drug therapy ; Carcinoma, Squamous Cell - pathology ; Cetuximab ; Cetuximab - pharmacology ; Cetuximab - therapeutic use ; Chelating Agents - pharmacology ; Chelating Agents - therapeutic use ; Copper (Nutrient) ; Copper - metabolism ; Dosage and administration ; Drug Synergism ; Drug therapy ; Enzymes ; Female ; Fibroblasts ; Head & neck cancer ; Head and neck cancer ; Head and Neck Neoplasms - drug therapy ; Head and Neck Neoplasms - pathology ; Humans ; Immunotherapy ; Male ; Metabolic disorders ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Mice, Nude ; Molybdenum - pharmacology ; Molybdenum - therapeutic use ; Monoclonal antibodies ; Neoplasm Invasiveness - pathology ; Osteoclasts - drug effects ; Osteoclasts - physiology ; Osteogenesis ; Phosphatase ; Protein-Lysine 6-Oxidase - metabolism ; RANK Ligand - metabolism ; Squamous cell carcinoma ; Squamous Cell Carcinoma of Head and Neck ; Targeted cancer therapy ; Tumor Cells, Cultured ; Xenograft Model Antitumor Assays</subject><ispartof>International journal of oncology, 2018-03, Vol.52 (3), p.989-999</ispartof><rights>COPYRIGHT 2018 Spandidos Publications</rights><rights>Copyright Spandidos Publications UK Ltd. 2018</rights><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c524t-100ddef3cda4ce54b8db66d01a487ed553edeb2d9a3250b6a460bc6c0737e7a53</citedby><cites>FETCH-LOGICAL-c524t-100ddef3cda4ce54b8db66d01a487ed553edeb2d9a3250b6a460bc6c0737e7a53</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,777,781,27905,27906</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29328370$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Morisawa, Ayaka</creatorcontrib><creatorcontrib>Okui, Tatsuo</creatorcontrib><creatorcontrib>Shimo, Tsuyoshi</creatorcontrib><creatorcontrib>Ibaragi, Soichiro</creatorcontrib><creatorcontrib>Okusha, Yuka</creatorcontrib><creatorcontrib>Ono, Mitsuaki</creatorcontrib><creatorcontrib>Nguyen, Thi Thu Ha</creatorcontrib><creatorcontrib>Hassan, Nur Mohammad Monsur</creatorcontrib><creatorcontrib>Sasaki, Akira</creatorcontrib><title>Ammonium tetrathiomolybdate enhances the antitumor effects of cetuximab via the suppression of osteoclastogenesis in head and neck squamous carcinoma</title><title>International journal of oncology</title><addtitle>Int J Oncol</addtitle><description>Head and neck squamous cell carcinoma (HNSCC) poses a significant challenge clinically where one of the mechanisms responsible for the invasion into facial bones occurs via the activation of osteoclasts. Copper has been demonstrated to play a key role in skeletal remodeling. However, the role of copper in cancer-associated bone destruction is thus far unknown. Lysyl oxidase (LOX) is a copper-dependent enzyme that promotes osteoclastogenesis. In the present study, we investigated the effects of copper on HNSCC with bone invasion by the copper chelator, ammonium tetrathiomolybdate (TM) in vitro and in vivo. We demonstrate that TM blocks the proliferation of HNSCC cells, inhibits LOX activation and decreases the expression of the receptor activator of nuclear factor-κB ligand (RANKL) in osteoblasts and osteocytes, subsequently suppressing bone destruction. These findings suggest that copper is a potential target for the treatment of HNSCCs associated with bone destruction.</description><subject>Ammonia</subject><subject>Animals</subject><subject>Antineoplastic Agents, Immunological - pharmacology</subject><subject>Antineoplastic Agents, Immunological - therapeutic use</subject><subject>Bone marrow</subject><subject>Bone Neoplasms - drug therapy</subject><subject>Bone Neoplasms - pathology</subject><subject>Bone Neoplasms - secondary</subject><subject>Bone Resorption - drug therapy</subject><subject>Bone Resorption - pathology</subject><subject>Carcinoma, Squamous Cell - drug therapy</subject><subject>Carcinoma, Squamous Cell - pathology</subject><subject>Cetuximab</subject><subject>Cetuximab - pharmacology</subject><subject>Cetuximab - therapeutic use</subject><subject>Chelating Agents - pharmacology</subject><subject>Chelating Agents - therapeutic use</subject><subject>Copper (Nutrient)</subject><subject>Copper - metabolism</subject><subject>Dosage and administration</subject><subject>Drug Synergism</subject><subject>Drug therapy</subject><subject>Enzymes</subject><subject>Female</subject><subject>Fibroblasts</subject><subject>Head & neck cancer</subject><subject>Head and neck cancer</subject><subject>Head and Neck Neoplasms - drug therapy</subject><subject>Head and Neck Neoplasms - pathology</subject><subject>Humans</subject><subject>Immunotherapy</subject><subject>Male</subject><subject>Metabolic disorders</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Nude</subject><subject>Molybdenum - pharmacology</subject><subject>Molybdenum - therapeutic use</subject><subject>Monoclonal antibodies</subject><subject>Neoplasm Invasiveness - pathology</subject><subject>Osteoclasts - drug effects</subject><subject>Osteoclasts - physiology</subject><subject>Osteogenesis</subject><subject>Phosphatase</subject><subject>Protein-Lysine 6-Oxidase - metabolism</subject><subject>RANK Ligand - metabolism</subject><subject>Squamous cell carcinoma</subject><subject>Squamous Cell Carcinoma of Head and Neck</subject><subject>Targeted cancer therapy</subject><subject>Tumor Cells, Cultured</subject><subject>Xenograft Model Antitumor Assays</subject><issn>1019-6439</issn><issn>1791-2423</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><recordid>eNptkstrFTEUhwex2Icu3UpA6G6uecxzeSlaCwU3dh0yyZlOrpPkNieR9g_x_zXX1kdBssghfOeEfPlV1VtGN2IY-Qe7CxtO2bBpeMNfVCesH1ldSvGy1JSNddeI8bg6RdxRytuWslfVMR8FH0RPT6ofW-eCt9mRBCmqtNjgwvowGZWAgF-U14AkLUCUTzZlFyKBeQadkISZaEj53jo1ke9W_cIw7_cREG3wByBggqBXhSncgge0SKwnCyhTBhriQX8jeJeVCxmJVlFbH5x6XR3NakV487SfVTefPn69-Fxff7m8uthe17rlTaoZpcbALLRRjYa2mQYzdZ2hTDVDD6ZtBRiYuBmV4C2dOtV0dNKdpr3ooVetOKveP87dx3CXAZPchRx9uVJyShkfilj-l7pVK0jr51BMaWdRy23LR96PRXehNv-hyjLgrA4eZlvOnzWc_9NQlKxpwbDmVNThc7B-BHUMiBFmuY_FeXyQjMpDCGQJgTyEQB5CUPh3T6_KkwPzh_796-InJ2Svgw</recordid><startdate>20180301</startdate><enddate>20180301</enddate><creator>Morisawa, Ayaka</creator><creator>Okui, Tatsuo</creator><creator>Shimo, Tsuyoshi</creator><creator>Ibaragi, Soichiro</creator><creator>Okusha, Yuka</creator><creator>Ono, Mitsuaki</creator><creator>Nguyen, Thi Thu Ha</creator><creator>Hassan, Nur Mohammad Monsur</creator><creator>Sasaki, Akira</creator><general>Spandidos Publications</general><general>Spandidos Publications UK Ltd</general><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>7RV</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AN0</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>K9.</scope><scope>KB0</scope><scope>M0S</scope><scope>M1P</scope><scope>NAPCQ</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope></search><sort><creationdate>20180301</creationdate><title>Ammonium tetrathiomolybdate enhances the antitumor effects of cetuximab via the suppression of osteoclastogenesis in head and neck squamous carcinoma</title><author>Morisawa, Ayaka ; Okui, Tatsuo ; Shimo, Tsuyoshi ; Ibaragi, Soichiro ; Okusha, Yuka ; Ono, Mitsuaki ; Nguyen, Thi Thu Ha ; Hassan, Nur Mohammad Monsur ; Sasaki, Akira</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c524t-100ddef3cda4ce54b8db66d01a487ed553edeb2d9a3250b6a460bc6c0737e7a53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Ammonia</topic><topic>Animals</topic><topic>Antineoplastic Agents, Immunological - pharmacology</topic><topic>Antineoplastic Agents, Immunological - therapeutic use</topic><topic>Bone marrow</topic><topic>Bone Neoplasms - drug therapy</topic><topic>Bone Neoplasms - pathology</topic><topic>Bone Neoplasms - secondary</topic><topic>Bone Resorption - drug therapy</topic><topic>Bone Resorption - pathology</topic><topic>Carcinoma, Squamous Cell - drug therapy</topic><topic>Carcinoma, Squamous Cell - pathology</topic><topic>Cetuximab</topic><topic>Cetuximab - pharmacology</topic><topic>Cetuximab - therapeutic use</topic><topic>Chelating Agents - pharmacology</topic><topic>Chelating Agents - therapeutic use</topic><topic>Copper (Nutrient)</topic><topic>Copper - metabolism</topic><topic>Dosage and administration</topic><topic>Drug Synergism</topic><topic>Drug therapy</topic><topic>Enzymes</topic><topic>Female</topic><topic>Fibroblasts</topic><topic>Head & neck cancer</topic><topic>Head and neck cancer</topic><topic>Head and Neck Neoplasms - drug therapy</topic><topic>Head and Neck Neoplasms - pathology</topic><topic>Humans</topic><topic>Immunotherapy</topic><topic>Male</topic><topic>Metabolic disorders</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Nude</topic><topic>Molybdenum - pharmacology</topic><topic>Molybdenum - therapeutic use</topic><topic>Monoclonal antibodies</topic><topic>Neoplasm Invasiveness - pathology</topic><topic>Osteoclasts - drug effects</topic><topic>Osteoclasts - physiology</topic><topic>Osteogenesis</topic><topic>Phosphatase</topic><topic>Protein-Lysine 6-Oxidase - metabolism</topic><topic>RANK Ligand - metabolism</topic><topic>Squamous cell carcinoma</topic><topic>Squamous Cell Carcinoma of Head and Neck</topic><topic>Targeted cancer therapy</topic><topic>Tumor Cells, Cultured</topic><topic>Xenograft Model Antitumor Assays</topic><toplevel>online_resources</toplevel><creatorcontrib>Morisawa, Ayaka</creatorcontrib><creatorcontrib>Okui, Tatsuo</creatorcontrib><creatorcontrib>Shimo, Tsuyoshi</creatorcontrib><creatorcontrib>Ibaragi, Soichiro</creatorcontrib><creatorcontrib>Okusha, Yuka</creatorcontrib><creatorcontrib>Ono, Mitsuaki</creatorcontrib><creatorcontrib>Nguyen, Thi Thu Ha</creatorcontrib><creatorcontrib>Hassan, Nur Mohammad Monsur</creatorcontrib><creatorcontrib>Sasaki, Akira</creatorcontrib><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>Nursing & Allied Health Database</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</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>British Nursing Database</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Nursing & Allied Health Premium</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><jtitle>International journal of oncology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Morisawa, Ayaka</au><au>Okui, Tatsuo</au><au>Shimo, Tsuyoshi</au><au>Ibaragi, Soichiro</au><au>Okusha, Yuka</au><au>Ono, Mitsuaki</au><au>Nguyen, Thi Thu Ha</au><au>Hassan, Nur Mohammad Monsur</au><au>Sasaki, Akira</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Ammonium tetrathiomolybdate enhances the antitumor effects of cetuximab via the suppression of osteoclastogenesis in head and neck squamous carcinoma</atitle><jtitle>International journal of oncology</jtitle><addtitle>Int J Oncol</addtitle><date>2018-03-01</date><risdate>2018</risdate><volume>52</volume><issue>3</issue><spage>989</spage><epage>999</epage><pages>989-999</pages><issn>1019-6439</issn><eissn>1791-2423</eissn><abstract>Head and neck squamous cell carcinoma (HNSCC) poses a significant challenge clinically where one of the mechanisms responsible for the invasion into facial bones occurs via the activation of osteoclasts. Copper has been demonstrated to play a key role in skeletal remodeling. However, the role of copper in cancer-associated bone destruction is thus far unknown. Lysyl oxidase (LOX) is a copper-dependent enzyme that promotes osteoclastogenesis. In the present study, we investigated the effects of copper on HNSCC with bone invasion by the copper chelator, ammonium tetrathiomolybdate (TM) in vitro and in vivo. We demonstrate that TM blocks the proliferation of HNSCC cells, inhibits LOX activation and decreases the expression of the receptor activator of nuclear factor-κB ligand (RANKL) in osteoblasts and osteocytes, subsequently suppressing bone destruction. These findings suggest that copper is a potential target for the treatment of HNSCCs associated with bone destruction.</abstract><cop>Greece</cop><pub>Spandidos Publications</pub><pmid>29328370</pmid><doi>10.3892/ijo.2018.4242</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Ammonia Animals Antineoplastic Agents, Immunological - pharmacology Antineoplastic Agents, Immunological - therapeutic use Bone marrow Bone Neoplasms - drug therapy Bone Neoplasms - pathology Bone Neoplasms - secondary Bone Resorption - drug therapy Bone Resorption - pathology Carcinoma, Squamous Cell - drug therapy Carcinoma, Squamous Cell - pathology Cetuximab Cetuximab - pharmacology Cetuximab - therapeutic use Chelating Agents - pharmacology Chelating Agents - therapeutic use Copper (Nutrient) Copper - metabolism Dosage and administration Drug Synergism Drug therapy Enzymes Female Fibroblasts Head & neck cancer Head and neck cancer Head and Neck Neoplasms - drug therapy Head and Neck Neoplasms - pathology Humans Immunotherapy Male Metabolic disorders Mice Mice, Inbred BALB C Mice, Inbred C57BL Mice, Nude Molybdenum - pharmacology Molybdenum - therapeutic use Monoclonal antibodies Neoplasm Invasiveness - pathology Osteoclasts - drug effects Osteoclasts - physiology Osteogenesis Phosphatase Protein-Lysine 6-Oxidase - metabolism RANK Ligand - metabolism Squamous cell carcinoma Squamous Cell Carcinoma of Head and Neck Targeted cancer therapy Tumor Cells, Cultured Xenograft Model Antitumor Assays |
| title | Ammonium tetrathiomolybdate enhances the antitumor effects of cetuximab via the suppression of osteoclastogenesis in head and neck squamous carcinoma |
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