Lenalidomide and pomalidomide potently interfere with induction of myeloid‐derived suppressor cells in multiple myeloma
Summary An increase in immunosuppressive myeloid‐derived suppressor cells (MDSCs) is associated with disease progression and treatment resistance in multiple myeloma (MM). We investigated the mechanisms underlying MDSC induction, and sought to discover a strategy for prevention of MDSC induction in...
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| Veröffentlicht in: | British journal of haematology 2020-12, Vol.191 (5), p.784-795 |
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| creator | Kuwahara‐Ota, Saeko Shimura, Yuji Steinebach, Christian Isa, Reiko Yamaguchi, Junko Nishiyama, Daichi Fujibayashi, Yuto Takimoto‐Shimomura, Tomoko Mizuno, Yoshimi Matsumura‐Kimoto, Yayoi Tsukamoto, Taku Chinen, Yoshiaki Kobayashi, Tsutomu Horiike, Shigeo Taniwaki, Masafumi Gütschow, Michael Kuroda, Junya |
| description | Summary
An increase in immunosuppressive myeloid‐derived suppressor cells (MDSCs) is associated with disease progression and treatment resistance in multiple myeloma (MM). We investigated the mechanisms underlying MDSC induction, and sought to discover a strategy for prevention of MDSC induction in MM. Using a transwell co‐culture system, four of nine examined human myeloma‐derived cell lines (HMCLs) were potent in inducing monocytic (M)‐MDSCs from normal peripheral blood mononuclear cells (PBMCs). As the results, we identified that secretion of C‐C motif chemokine ligand 5 (CCL5) and macrophage migration inhibitory factor (MIF) by myeloma cells is a prerequisite for induction of MDSCs in MM. The immunomodulatory drug (IMiD) compounds, such as lenalidomide (LEN) and pomalidomide (POM), were identified as potent inhibitors of MDSC induction through bidirectional molecular effects of cereblon (CRBN)‐dependent and ‐independent downregulation of CCL5 and MIF in myeloma cells; and downregulation of C‐C motif chemokine receptor 5, a receptor for CCL5, and induction of interferon regulatory factor 8, a critical transcription factor for monocytic differentiation, in PBMCs. In the present study of the molecular mechanisms underlying MDSC induction, we identified a novel effect of LEN and POM of inhibiting MDSC induction via overlapping regulatory effects in myeloma cells and normal PBMCs. |
| doi_str_mv | 10.1111/bjh.16881 |
| format | Article |
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An increase in immunosuppressive myeloid‐derived suppressor cells (MDSCs) is associated with disease progression and treatment resistance in multiple myeloma (MM). We investigated the mechanisms underlying MDSC induction, and sought to discover a strategy for prevention of MDSC induction in MM. Using a transwell co‐culture system, four of nine examined human myeloma‐derived cell lines (HMCLs) were potent in inducing monocytic (M)‐MDSCs from normal peripheral blood mononuclear cells (PBMCs). As the results, we identified that secretion of C‐C motif chemokine ligand 5 (CCL5) and macrophage migration inhibitory factor (MIF) by myeloma cells is a prerequisite for induction of MDSCs in MM. The immunomodulatory drug (IMiD) compounds, such as lenalidomide (LEN) and pomalidomide (POM), were identified as potent inhibitors of MDSC induction through bidirectional molecular effects of cereblon (CRBN)‐dependent and ‐independent downregulation of CCL5 and MIF in myeloma cells; and downregulation of C‐C motif chemokine receptor 5, a receptor for CCL5, and induction of interferon regulatory factor 8, a critical transcription factor for monocytic differentiation, in PBMCs. In the present study of the molecular mechanisms underlying MDSC induction, we identified a novel effect of LEN and POM of inhibiting MDSC induction via overlapping regulatory effects in myeloma cells and normal PBMCs.</description><identifier>ISSN: 0007-1048</identifier><identifier>EISSN: 1365-2141</identifier><identifier>DOI: 10.1111/bjh.16881</identifier><identifier>PMID: 32558939</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Cell culture ; Cell Line, Tumor ; cereblon ; Chemokine CCL5 - immunology ; Chemokines ; Coculture Techniques ; Disease resistance ; Hematology ; Humans ; Immunomodulation ; Immunotherapy ; Interferon ; Interferon regulatory factor ; Interferon Regulatory Factors - immunology ; Intramolecular Oxidoreductases - immunology ; lenalidomide ; Lenalidomide - pharmacology ; Leukocyte migration ; Leukocytes (mononuclear) ; Macrophage migration inhibitory factor ; Macrophage Migration-Inhibitory Factors - immunology ; Molecular modelling ; Monocytes ; Multiple myeloma ; Multiple Myeloma - drug therapy ; Multiple Myeloma - immunology ; Multiple Myeloma - pathology ; Myeloid-Derived Suppressor Cells - immunology ; Myeloid-Derived Suppressor Cells - pathology ; myeloid‐derived suppressor cell ; Neoplasm Proteins - immunology ; Peripheral blood mononuclear cells ; pomalidomide ; Suppressor cells ; Targeted cancer therapy ; Thalidomide - analogs & derivatives ; Thalidomide - pharmacology ; Tumor cell lines</subject><ispartof>British journal of haematology, 2020-12, Vol.191 (5), p.784-795</ispartof><rights>2020 British Society for Haematology and John Wiley & Sons Ltd</rights><rights>2020 British Society for Haematology and John Wiley & Sons Ltd.</rights><rights>Copyright © 2020 John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5421-e60d47e5a91b97b61c1b4b81a431cae22f76b5662a29111f60d96d51038f64483</citedby><cites>FETCH-LOGICAL-c5421-e60d47e5a91b97b61c1b4b81a431cae22f76b5662a29111f60d96d51038f64483</cites><orcidid>0000-0001-6130-1550 ; 0000-0001-8966-2876 ; 0000-0001-9309-7902</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fbjh.16881$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fbjh.16881$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32558939$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kuwahara‐Ota, Saeko</creatorcontrib><creatorcontrib>Shimura, Yuji</creatorcontrib><creatorcontrib>Steinebach, Christian</creatorcontrib><creatorcontrib>Isa, Reiko</creatorcontrib><creatorcontrib>Yamaguchi, Junko</creatorcontrib><creatorcontrib>Nishiyama, Daichi</creatorcontrib><creatorcontrib>Fujibayashi, Yuto</creatorcontrib><creatorcontrib>Takimoto‐Shimomura, Tomoko</creatorcontrib><creatorcontrib>Mizuno, Yoshimi</creatorcontrib><creatorcontrib>Matsumura‐Kimoto, Yayoi</creatorcontrib><creatorcontrib>Tsukamoto, Taku</creatorcontrib><creatorcontrib>Chinen, Yoshiaki</creatorcontrib><creatorcontrib>Kobayashi, Tsutomu</creatorcontrib><creatorcontrib>Horiike, Shigeo</creatorcontrib><creatorcontrib>Taniwaki, Masafumi</creatorcontrib><creatorcontrib>Gütschow, Michael</creatorcontrib><creatorcontrib>Kuroda, Junya</creatorcontrib><title>Lenalidomide and pomalidomide potently interfere with induction of myeloid‐derived suppressor cells in multiple myeloma</title><title>British journal of haematology</title><addtitle>Br J Haematol</addtitle><description>Summary
An increase in immunosuppressive myeloid‐derived suppressor cells (MDSCs) is associated with disease progression and treatment resistance in multiple myeloma (MM). We investigated the mechanisms underlying MDSC induction, and sought to discover a strategy for prevention of MDSC induction in MM. Using a transwell co‐culture system, four of nine examined human myeloma‐derived cell lines (HMCLs) were potent in inducing monocytic (M)‐MDSCs from normal peripheral blood mononuclear cells (PBMCs). As the results, we identified that secretion of C‐C motif chemokine ligand 5 (CCL5) and macrophage migration inhibitory factor (MIF) by myeloma cells is a prerequisite for induction of MDSCs in MM. The immunomodulatory drug (IMiD) compounds, such as lenalidomide (LEN) and pomalidomide (POM), were identified as potent inhibitors of MDSC induction through bidirectional molecular effects of cereblon (CRBN)‐dependent and ‐independent downregulation of CCL5 and MIF in myeloma cells; and downregulation of C‐C motif chemokine receptor 5, a receptor for CCL5, and induction of interferon regulatory factor 8, a critical transcription factor for monocytic differentiation, in PBMCs. In the present study of the molecular mechanisms underlying MDSC induction, we identified a novel effect of LEN and POM of inhibiting MDSC induction via overlapping regulatory effects in myeloma cells and normal PBMCs.</description><subject>Cell culture</subject><subject>Cell Line, Tumor</subject><subject>cereblon</subject><subject>Chemokine CCL5 - immunology</subject><subject>Chemokines</subject><subject>Coculture Techniques</subject><subject>Disease resistance</subject><subject>Hematology</subject><subject>Humans</subject><subject>Immunomodulation</subject><subject>Immunotherapy</subject><subject>Interferon</subject><subject>Interferon regulatory factor</subject><subject>Interferon Regulatory Factors - immunology</subject><subject>Intramolecular Oxidoreductases - immunology</subject><subject>lenalidomide</subject><subject>Lenalidomide - pharmacology</subject><subject>Leukocyte migration</subject><subject>Leukocytes (mononuclear)</subject><subject>Macrophage migration inhibitory factor</subject><subject>Macrophage Migration-Inhibitory Factors - immunology</subject><subject>Molecular modelling</subject><subject>Monocytes</subject><subject>Multiple myeloma</subject><subject>Multiple Myeloma - drug therapy</subject><subject>Multiple Myeloma - immunology</subject><subject>Multiple Myeloma - pathology</subject><subject>Myeloid-Derived Suppressor Cells - immunology</subject><subject>Myeloid-Derived Suppressor Cells - pathology</subject><subject>myeloid‐derived suppressor cell</subject><subject>Neoplasm Proteins - immunology</subject><subject>Peripheral blood mononuclear cells</subject><subject>pomalidomide</subject><subject>Suppressor cells</subject><subject>Targeted cancer therapy</subject><subject>Thalidomide - analogs & derivatives</subject><subject>Thalidomide - pharmacology</subject><subject>Tumor cell lines</subject><issn>0007-1048</issn><issn>1365-2141</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kMtKxDAUQIMoOj4W_oAEXLmo5rZppl2q-GTAja5L2twyGdKmJq3SnZ_gN_olRjvqymwuuRwO3EPIIbBTCO-sXC1PQWQZbJAZJCKNYuCwSWaMsXkEjGc7ZNf7FWOQsBS2yU4Sp2mWJ_mMjAtspdHKNlohla2inW3-Fp3tse3NSHXbo6vRIX3V_TJ81VD12rbU1rQZ0VitPt7eFTr9gor6oescem8drdAYH3jaDKbXncEJb-Q-2aql8Xiwnnvk6frq8fI2Wjzc3F2eL6Iq5TFEKJjic0xlDmU-LwVUUPIyA8kTqCTGcT0XZSpELOM8tKgDnguVAkuyWnCeJXvkePJ2zj4P6PtiZQcXjvZFzIUQWcKECNTJRFXOeu-wLjqnG-nGAljxFbkIkYvvyIE9WhuHskH1S_5UDcDZBLxqg-P_puLi_nZSfgJWLYjA</recordid><startdate>202012</startdate><enddate>202012</enddate><creator>Kuwahara‐Ota, Saeko</creator><creator>Shimura, Yuji</creator><creator>Steinebach, Christian</creator><creator>Isa, Reiko</creator><creator>Yamaguchi, Junko</creator><creator>Nishiyama, Daichi</creator><creator>Fujibayashi, Yuto</creator><creator>Takimoto‐Shimomura, Tomoko</creator><creator>Mizuno, Yoshimi</creator><creator>Matsumura‐Kimoto, Yayoi</creator><creator>Tsukamoto, Taku</creator><creator>Chinen, Yoshiaki</creator><creator>Kobayashi, Tsutomu</creator><creator>Horiike, Shigeo</creator><creator>Taniwaki, Masafumi</creator><creator>Gütschow, Michael</creator><creator>Kuroda, Junya</creator><general>Blackwell Publishing 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>7T5</scope><scope>H94</scope><orcidid>https://orcid.org/0000-0001-6130-1550</orcidid><orcidid>https://orcid.org/0000-0001-8966-2876</orcidid><orcidid>https://orcid.org/0000-0001-9309-7902</orcidid></search><sort><creationdate>202012</creationdate><title>Lenalidomide and pomalidomide potently interfere with induction of myeloid‐derived suppressor cells in multiple myeloma</title><author>Kuwahara‐Ota, Saeko ; Shimura, Yuji ; Steinebach, Christian ; Isa, Reiko ; Yamaguchi, Junko ; Nishiyama, Daichi ; Fujibayashi, Yuto ; Takimoto‐Shimomura, Tomoko ; Mizuno, Yoshimi ; Matsumura‐Kimoto, Yayoi ; Tsukamoto, Taku ; Chinen, Yoshiaki ; Kobayashi, Tsutomu ; Horiike, Shigeo ; Taniwaki, Masafumi ; Gütschow, Michael ; Kuroda, Junya</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5421-e60d47e5a91b97b61c1b4b81a431cae22f76b5662a29111f60d96d51038f64483</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Cell culture</topic><topic>Cell Line, Tumor</topic><topic>cereblon</topic><topic>Chemokine CCL5 - immunology</topic><topic>Chemokines</topic><topic>Coculture Techniques</topic><topic>Disease resistance</topic><topic>Hematology</topic><topic>Humans</topic><topic>Immunomodulation</topic><topic>Immunotherapy</topic><topic>Interferon</topic><topic>Interferon regulatory factor</topic><topic>Interferon Regulatory Factors - immunology</topic><topic>Intramolecular Oxidoreductases - immunology</topic><topic>lenalidomide</topic><topic>Lenalidomide - pharmacology</topic><topic>Leukocyte migration</topic><topic>Leukocytes (mononuclear)</topic><topic>Macrophage migration inhibitory factor</topic><topic>Macrophage Migration-Inhibitory Factors - immunology</topic><topic>Molecular modelling</topic><topic>Monocytes</topic><topic>Multiple myeloma</topic><topic>Multiple Myeloma - drug therapy</topic><topic>Multiple Myeloma - immunology</topic><topic>Multiple Myeloma - pathology</topic><topic>Myeloid-Derived Suppressor Cells - immunology</topic><topic>Myeloid-Derived Suppressor Cells - pathology</topic><topic>myeloid‐derived suppressor cell</topic><topic>Neoplasm Proteins - immunology</topic><topic>Peripheral blood mononuclear cells</topic><topic>pomalidomide</topic><topic>Suppressor cells</topic><topic>Targeted cancer therapy</topic><topic>Thalidomide - analogs & derivatives</topic><topic>Thalidomide - pharmacology</topic><topic>Tumor cell lines</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kuwahara‐Ota, Saeko</creatorcontrib><creatorcontrib>Shimura, Yuji</creatorcontrib><creatorcontrib>Steinebach, Christian</creatorcontrib><creatorcontrib>Isa, Reiko</creatorcontrib><creatorcontrib>Yamaguchi, Junko</creatorcontrib><creatorcontrib>Nishiyama, Daichi</creatorcontrib><creatorcontrib>Fujibayashi, Yuto</creatorcontrib><creatorcontrib>Takimoto‐Shimomura, Tomoko</creatorcontrib><creatorcontrib>Mizuno, Yoshimi</creatorcontrib><creatorcontrib>Matsumura‐Kimoto, Yayoi</creatorcontrib><creatorcontrib>Tsukamoto, Taku</creatorcontrib><creatorcontrib>Chinen, Yoshiaki</creatorcontrib><creatorcontrib>Kobayashi, Tsutomu</creatorcontrib><creatorcontrib>Horiike, Shigeo</creatorcontrib><creatorcontrib>Taniwaki, Masafumi</creatorcontrib><creatorcontrib>Gütschow, Michael</creatorcontrib><creatorcontrib>Kuroda, Junya</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Immunology Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><jtitle>British journal of haematology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kuwahara‐Ota, Saeko</au><au>Shimura, Yuji</au><au>Steinebach, Christian</au><au>Isa, Reiko</au><au>Yamaguchi, Junko</au><au>Nishiyama, Daichi</au><au>Fujibayashi, Yuto</au><au>Takimoto‐Shimomura, Tomoko</au><au>Mizuno, Yoshimi</au><au>Matsumura‐Kimoto, Yayoi</au><au>Tsukamoto, Taku</au><au>Chinen, Yoshiaki</au><au>Kobayashi, Tsutomu</au><au>Horiike, Shigeo</au><au>Taniwaki, Masafumi</au><au>Gütschow, Michael</au><au>Kuroda, Junya</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Lenalidomide and pomalidomide potently interfere with induction of myeloid‐derived suppressor cells in multiple myeloma</atitle><jtitle>British journal of haematology</jtitle><addtitle>Br J Haematol</addtitle><date>2020-12</date><risdate>2020</risdate><volume>191</volume><issue>5</issue><spage>784</spage><epage>795</epage><pages>784-795</pages><issn>0007-1048</issn><eissn>1365-2141</eissn><abstract>Summary
An increase in immunosuppressive myeloid‐derived suppressor cells (MDSCs) is associated with disease progression and treatment resistance in multiple myeloma (MM). We investigated the mechanisms underlying MDSC induction, and sought to discover a strategy for prevention of MDSC induction in MM. Using a transwell co‐culture system, four of nine examined human myeloma‐derived cell lines (HMCLs) were potent in inducing monocytic (M)‐MDSCs from normal peripheral blood mononuclear cells (PBMCs). As the results, we identified that secretion of C‐C motif chemokine ligand 5 (CCL5) and macrophage migration inhibitory factor (MIF) by myeloma cells is a prerequisite for induction of MDSCs in MM. The immunomodulatory drug (IMiD) compounds, such as lenalidomide (LEN) and pomalidomide (POM), were identified as potent inhibitors of MDSC induction through bidirectional molecular effects of cereblon (CRBN)‐dependent and ‐independent downregulation of CCL5 and MIF in myeloma cells; and downregulation of C‐C motif chemokine receptor 5, a receptor for CCL5, and induction of interferon regulatory factor 8, a critical transcription factor for monocytic differentiation, in PBMCs. In the present study of the molecular mechanisms underlying MDSC induction, we identified a novel effect of LEN and POM of inhibiting MDSC induction via overlapping regulatory effects in myeloma cells and normal PBMCs.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>32558939</pmid><doi>10.1111/bjh.16881</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-6130-1550</orcidid><orcidid>https://orcid.org/0000-0001-8966-2876</orcidid><orcidid>https://orcid.org/0000-0001-9309-7902</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Cell culture Cell Line, Tumor cereblon Chemokine CCL5 - immunology Chemokines Coculture Techniques Disease resistance Hematology Humans Immunomodulation Immunotherapy Interferon Interferon regulatory factor Interferon Regulatory Factors - immunology Intramolecular Oxidoreductases - immunology lenalidomide Lenalidomide - pharmacology Leukocyte migration Leukocytes (mononuclear) Macrophage migration inhibitory factor Macrophage Migration-Inhibitory Factors - immunology Molecular modelling Monocytes Multiple myeloma Multiple Myeloma - drug therapy Multiple Myeloma - immunology Multiple Myeloma - pathology Myeloid-Derived Suppressor Cells - immunology Myeloid-Derived Suppressor Cells - pathology myeloid‐derived suppressor cell Neoplasm Proteins - immunology Peripheral blood mononuclear cells pomalidomide Suppressor cells Targeted cancer therapy Thalidomide - analogs & derivatives Thalidomide - pharmacology Tumor cell lines |
| title | Lenalidomide and pomalidomide potently interfere with induction of myeloid‐derived suppressor cells in multiple myeloma |
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