Beyond the marrow: insights from comprehensive next-generation sequencing of extramedullary multiple myeloma tumors
Extramedullary multiple myeloma (EMM) is an aggressive form of multiple myeloma (MM). This study represents the most comprehensive next-generation sequencing analysis of EMM tumors ( N = 14) to date, uncovering key molecular features and describing the tumor microenvironment. We observed the co-occ...
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| Veröffentlicht in: | Leukemia 2024-06, Vol.38 (6), p.1323-1333 |
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| creator | Jelinek, T. Zihala, D. Sevcikova, T. Anilkumar Sithara, A. Kapustova, V. Sahinbegovic, H. Venglar, O. Muronova, L. Broskevicova, L. Nenarokov, S. Bilek, D. Popkova, T. Plonkova, H. Vrana, J. Zidlik, V. Hurnik, P. Havel, M. Hrdinka, M. Chyra, Z. Stracquadanio, G. Simicek, M. Hajek, R. |
| description | Extramedullary multiple myeloma (EMM) is an aggressive form of multiple myeloma (MM). This study represents the most comprehensive next-generation sequencing analysis of EMM tumors (
N
= 14) to date, uncovering key molecular features and describing the tumor microenvironment. We observed the co-occurrence of 1q21 gain/amplification and MAPK pathway mutations in 79% of EMM samples, suggesting that these are crucial mutational events in EMM development. We also demonstrated that patients with mutated
KRAS
and 1q21 gain/amplification at the time of diagnosis have a significantly higher risk of EMM development (HR = 2.4,
p
= 0.011) using data from a large CoMMpass dataset. We identified downregulation of CXCR4 and enhanced cell proliferation, along with reduced expression of therapeutic targets (CD38, SLAMF7, GPRC5D, FCRH5), potentially explaining diminished efficacy of immunotherapy. Conversely, we identified significantly upregulated EZH2 and CD70 as potential future therapeutic options. For the first time, we report on the tumor microenvironment of EMM, revealing CD8+ T cells and NK cells as predominant immune effector cells using single-cell sequencing. Finally, this is the first longitudinal study in EMM revealing the molecular changes from the time of diagnosis to EMM relapse. |
| doi_str_mv | 10.1038/s41375-024-02206-w |
| format | Article |
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N
= 14) to date, uncovering key molecular features and describing the tumor microenvironment. We observed the co-occurrence of 1q21 gain/amplification and MAPK pathway mutations in 79% of EMM samples, suggesting that these are crucial mutational events in EMM development. We also demonstrated that patients with mutated
KRAS
and 1q21 gain/amplification at the time of diagnosis have a significantly higher risk of EMM development (HR = 2.4,
p
= 0.011) using data from a large CoMMpass dataset. We identified downregulation of CXCR4 and enhanced cell proliferation, along with reduced expression of therapeutic targets (CD38, SLAMF7, GPRC5D, FCRH5), potentially explaining diminished efficacy of immunotherapy. Conversely, we identified significantly upregulated EZH2 and CD70 as potential future therapeutic options. For the first time, we report on the tumor microenvironment of EMM, revealing CD8+ T cells and NK cells as predominant immune effector cells using single-cell sequencing. Finally, this is the first longitudinal study in EMM revealing the molecular changes from the time of diagnosis to EMM relapse.</description><identifier>ISSN: 0887-6924</identifier><identifier>ISSN: 1476-5551</identifier><identifier>EISSN: 1476-5551</identifier><identifier>DOI: 10.1038/s41375-024-02206-w</identifier><identifier>PMID: 38493239</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>13/31 ; 45/23 ; 45/91 ; 631/67/69 ; 692/699/67/1990 ; Amplification ; Cancer Research ; CD38 antigen ; CD70 antigen ; CD8 antigen ; Cell proliferation ; Critical Care Medicine ; CXCR4 protein ; Diagnosis ; Effector cells ; Hematology ; Immunotherapy ; Intensive ; Internal Medicine ; Longitudinal studies ; Lymphocytes ; Lymphocytes T ; MAP kinase ; Medicine ; Medicine & Public Health ; Multiple myeloma ; Next-generation sequencing ; Oncology ; Sequence analysis ; Therapeutic targets ; Tumor microenvironment ; Tumors</subject><ispartof>Leukemia, 2024-06, Vol.38 (6), p.1323-1333</ispartof><rights>The Author(s) 2024</rights><rights>2024. The Author(s).</rights><rights>The Author(s) 2024. 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-c475t-c55b4ceeb8374163ce5782806cd5a18d72f0e810b9c601b4d9a9e5b50283c0033</citedby><cites>FETCH-LOGICAL-c475t-c55b4ceeb8374163ce5782806cd5a18d72f0e810b9c601b4d9a9e5b50283c0033</cites><orcidid>0000-0001-9819-3645 ; 0000-0001-7444-5422 ; 0000-0003-2388-2723 ; 0000-0002-2981-2825 ; 0000-0001-5885-4218 ; 0000-0003-2540-6966 ; 0000-0002-5467-9253 ; 0000-0001-6955-6267</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41375-024-02206-w$$EPDF$$P50$$Gspringer$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41375-024-02206-w$$EHTML$$P50$$Gspringer$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38493239$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jelinek, T.</creatorcontrib><creatorcontrib>Zihala, D.</creatorcontrib><creatorcontrib>Sevcikova, T.</creatorcontrib><creatorcontrib>Anilkumar Sithara, A.</creatorcontrib><creatorcontrib>Kapustova, V.</creatorcontrib><creatorcontrib>Sahinbegovic, H.</creatorcontrib><creatorcontrib>Venglar, O.</creatorcontrib><creatorcontrib>Muronova, L.</creatorcontrib><creatorcontrib>Broskevicova, L.</creatorcontrib><creatorcontrib>Nenarokov, S.</creatorcontrib><creatorcontrib>Bilek, D.</creatorcontrib><creatorcontrib>Popkova, T.</creatorcontrib><creatorcontrib>Plonkova, H.</creatorcontrib><creatorcontrib>Vrana, J.</creatorcontrib><creatorcontrib>Zidlik, V.</creatorcontrib><creatorcontrib>Hurnik, P.</creatorcontrib><creatorcontrib>Havel, M.</creatorcontrib><creatorcontrib>Hrdinka, M.</creatorcontrib><creatorcontrib>Chyra, Z.</creatorcontrib><creatorcontrib>Stracquadanio, G.</creatorcontrib><creatorcontrib>Simicek, M.</creatorcontrib><creatorcontrib>Hajek, R.</creatorcontrib><title>Beyond the marrow: insights from comprehensive next-generation sequencing of extramedullary multiple myeloma tumors</title><title>Leukemia</title><addtitle>Leukemia</addtitle><addtitle>Leukemia</addtitle><description>Extramedullary multiple myeloma (EMM) is an aggressive form of multiple myeloma (MM). This study represents the most comprehensive next-generation sequencing analysis of EMM tumors (
N
= 14) to date, uncovering key molecular features and describing the tumor microenvironment. We observed the co-occurrence of 1q21 gain/amplification and MAPK pathway mutations in 79% of EMM samples, suggesting that these are crucial mutational events in EMM development. We also demonstrated that patients with mutated
KRAS
and 1q21 gain/amplification at the time of diagnosis have a significantly higher risk of EMM development (HR = 2.4,
p
= 0.011) using data from a large CoMMpass dataset. We identified downregulation of CXCR4 and enhanced cell proliferation, along with reduced expression of therapeutic targets (CD38, SLAMF7, GPRC5D, FCRH5), potentially explaining diminished efficacy of immunotherapy. Conversely, we identified significantly upregulated EZH2 and CD70 as potential future therapeutic options. For the first time, we report on the tumor microenvironment of EMM, revealing CD8+ T cells and NK cells as predominant immune effector cells using single-cell sequencing. Finally, this is the first longitudinal study in EMM revealing the molecular changes from the time of diagnosis to EMM relapse.</description><subject>13/31</subject><subject>45/23</subject><subject>45/91</subject><subject>631/67/69</subject><subject>692/699/67/1990</subject><subject>Amplification</subject><subject>Cancer Research</subject><subject>CD38 antigen</subject><subject>CD70 antigen</subject><subject>CD8 antigen</subject><subject>Cell proliferation</subject><subject>Critical Care Medicine</subject><subject>CXCR4 protein</subject><subject>Diagnosis</subject><subject>Effector cells</subject><subject>Hematology</subject><subject>Immunotherapy</subject><subject>Intensive</subject><subject>Internal Medicine</subject><subject>Longitudinal studies</subject><subject>Lymphocytes</subject><subject>Lymphocytes T</subject><subject>MAP kinase</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Multiple myeloma</subject><subject>Next-generation sequencing</subject><subject>Oncology</subject><subject>Sequence analysis</subject><subject>Therapeutic targets</subject><subject>Tumor microenvironment</subject><subject>Tumors</subject><issn>0887-6924</issn><issn>1476-5551</issn><issn>1476-5551</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><recordid>eNp9UUtv1DAYtBCILgt_gAOyxIVLwO_YXBBUvKRKXOBsOc6XrKvEXuyky_573G4pjwOHT5Y8841nPAg9peQlJVy_KoLyVjaEiTqMqOZwD22oaFUjpaT30YZo3TbKMHGGHpVyScg1qB6iM66F4YybDSrv4Jhij5cd4NnlnA6vcYgljLul4CGnGfs07zPsoF5eAY7wY2lGiJDdElLEBb6vEH2II04DrmB2M_TrNLl8xPM6LWE_VeUjTGl2eFnnlMtj9GBwU4Ent-cWffvw_uv5p-biy8fP528vGi9auTReyk54gE7zVlDFPchWM02U76Wjum_ZQEBT0hmvCO1Eb5wB2UnCNPeEcL5Fb066-7WrpjzE6m6y-xxq0qNNLti_kRh2dkxXltL6Ua2iVeHFrUJONWdZ7ByKh5ouQlqLZUZqZjips0XP_6FepjXHms9yorjhVN5YYieWz6mUDMOdG0rsdan2VKqtpdqbUu2hLj37M8fdyq8WK4GfCKVCcYT8--3_yP4EFeSw9Q</recordid><startdate>20240601</startdate><enddate>20240601</enddate><creator>Jelinek, T.</creator><creator>Zihala, D.</creator><creator>Sevcikova, T.</creator><creator>Anilkumar Sithara, A.</creator><creator>Kapustova, V.</creator><creator>Sahinbegovic, H.</creator><creator>Venglar, O.</creator><creator>Muronova, L.</creator><creator>Broskevicova, L.</creator><creator>Nenarokov, S.</creator><creator>Bilek, D.</creator><creator>Popkova, T.</creator><creator>Plonkova, H.</creator><creator>Vrana, J.</creator><creator>Zidlik, V.</creator><creator>Hurnik, P.</creator><creator>Havel, M.</creator><creator>Hrdinka, M.</creator><creator>Chyra, Z.</creator><creator>Stracquadanio, G.</creator><creator>Simicek, M.</creator><creator>Hajek, R.</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>C6C</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7T5</scope><scope>7T7</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>NAPCQ</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9819-3645</orcidid><orcidid>https://orcid.org/0000-0001-7444-5422</orcidid><orcidid>https://orcid.org/0000-0003-2388-2723</orcidid><orcidid>https://orcid.org/0000-0002-2981-2825</orcidid><orcidid>https://orcid.org/0000-0001-5885-4218</orcidid><orcidid>https://orcid.org/0000-0003-2540-6966</orcidid><orcidid>https://orcid.org/0000-0002-5467-9253</orcidid><orcidid>https://orcid.org/0000-0001-6955-6267</orcidid></search><sort><creationdate>20240601</creationdate><title>Beyond the marrow: insights from comprehensive next-generation sequencing of extramedullary multiple myeloma tumors</title><author>Jelinek, T. ; Zihala, D. ; Sevcikova, T. ; Anilkumar Sithara, A. ; Kapustova, V. ; Sahinbegovic, H. ; Venglar, O. ; Muronova, L. ; Broskevicova, L. ; Nenarokov, S. ; Bilek, D. ; Popkova, T. ; Plonkova, H. ; Vrana, J. ; Zidlik, V. ; Hurnik, P. ; Havel, M. ; Hrdinka, M. ; Chyra, Z. ; Stracquadanio, G. ; Simicek, M. ; Hajek, R.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c475t-c55b4ceeb8374163ce5782806cd5a18d72f0e810b9c601b4d9a9e5b50283c0033</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>13/31</topic><topic>45/23</topic><topic>45/91</topic><topic>631/67/69</topic><topic>692/699/67/1990</topic><topic>Amplification</topic><topic>Cancer Research</topic><topic>CD38 antigen</topic><topic>CD70 antigen</topic><topic>CD8 antigen</topic><topic>Cell proliferation</topic><topic>Critical Care Medicine</topic><topic>CXCR4 protein</topic><topic>Diagnosis</topic><topic>Effector cells</topic><topic>Hematology</topic><topic>Immunotherapy</topic><topic>Intensive</topic><topic>Internal Medicine</topic><topic>Longitudinal studies</topic><topic>Lymphocytes</topic><topic>Lymphocytes T</topic><topic>MAP kinase</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Multiple myeloma</topic><topic>Next-generation sequencing</topic><topic>Oncology</topic><topic>Sequence analysis</topic><topic>Therapeutic targets</topic><topic>Tumor microenvironment</topic><topic>Tumors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jelinek, T.</creatorcontrib><creatorcontrib>Zihala, D.</creatorcontrib><creatorcontrib>Sevcikova, T.</creatorcontrib><creatorcontrib>Anilkumar Sithara, A.</creatorcontrib><creatorcontrib>Kapustova, V.</creatorcontrib><creatorcontrib>Sahinbegovic, H.</creatorcontrib><creatorcontrib>Venglar, O.</creatorcontrib><creatorcontrib>Muronova, L.</creatorcontrib><creatorcontrib>Broskevicova, L.</creatorcontrib><creatorcontrib>Nenarokov, S.</creatorcontrib><creatorcontrib>Bilek, D.</creatorcontrib><creatorcontrib>Popkova, T.</creatorcontrib><creatorcontrib>Plonkova, H.</creatorcontrib><creatorcontrib>Vrana, J.</creatorcontrib><creatorcontrib>Zidlik, V.</creatorcontrib><creatorcontrib>Hurnik, P.</creatorcontrib><creatorcontrib>Havel, M.</creatorcontrib><creatorcontrib>Hrdinka, M.</creatorcontrib><creatorcontrib>Chyra, Z.</creatorcontrib><creatorcontrib>Stracquadanio, G.</creatorcontrib><creatorcontrib>Simicek, M.</creatorcontrib><creatorcontrib>Hajek, R.</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Immunology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Leukemia</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jelinek, T.</au><au>Zihala, D.</au><au>Sevcikova, T.</au><au>Anilkumar Sithara, A.</au><au>Kapustova, V.</au><au>Sahinbegovic, H.</au><au>Venglar, O.</au><au>Muronova, L.</au><au>Broskevicova, L.</au><au>Nenarokov, S.</au><au>Bilek, D.</au><au>Popkova, T.</au><au>Plonkova, H.</au><au>Vrana, J.</au><au>Zidlik, V.</au><au>Hurnik, P.</au><au>Havel, M.</au><au>Hrdinka, M.</au><au>Chyra, Z.</au><au>Stracquadanio, G.</au><au>Simicek, M.</au><au>Hajek, R.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Beyond the marrow: insights from comprehensive next-generation sequencing of extramedullary multiple myeloma tumors</atitle><jtitle>Leukemia</jtitle><stitle>Leukemia</stitle><addtitle>Leukemia</addtitle><date>2024-06-01</date><risdate>2024</risdate><volume>38</volume><issue>6</issue><spage>1323</spage><epage>1333</epage><pages>1323-1333</pages><issn>0887-6924</issn><issn>1476-5551</issn><eissn>1476-5551</eissn><abstract>Extramedullary multiple myeloma (EMM) is an aggressive form of multiple myeloma (MM). This study represents the most comprehensive next-generation sequencing analysis of EMM tumors (
N
= 14) to date, uncovering key molecular features and describing the tumor microenvironment. We observed the co-occurrence of 1q21 gain/amplification and MAPK pathway mutations in 79% of EMM samples, suggesting that these are crucial mutational events in EMM development. We also demonstrated that patients with mutated
KRAS
and 1q21 gain/amplification at the time of diagnosis have a significantly higher risk of EMM development (HR = 2.4,
p
= 0.011) using data from a large CoMMpass dataset. We identified downregulation of CXCR4 and enhanced cell proliferation, along with reduced expression of therapeutic targets (CD38, SLAMF7, GPRC5D, FCRH5), potentially explaining diminished efficacy of immunotherapy. Conversely, we identified significantly upregulated EZH2 and CD70 as potential future therapeutic options. For the first time, we report on the tumor microenvironment of EMM, revealing CD8+ T cells and NK cells as predominant immune effector cells using single-cell sequencing. Finally, this is the first longitudinal study in EMM revealing the molecular changes from the time of diagnosis to EMM relapse.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>38493239</pmid><doi>10.1038/s41375-024-02206-w</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0001-9819-3645</orcidid><orcidid>https://orcid.org/0000-0001-7444-5422</orcidid><orcidid>https://orcid.org/0000-0003-2388-2723</orcidid><orcidid>https://orcid.org/0000-0002-2981-2825</orcidid><orcidid>https://orcid.org/0000-0001-5885-4218</orcidid><orcidid>https://orcid.org/0000-0003-2540-6966</orcidid><orcidid>https://orcid.org/0000-0002-5467-9253</orcidid><orcidid>https://orcid.org/0000-0001-6955-6267</orcidid><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 0887-6924 |
| ispartof | Leukemia, 2024-06, Vol.38 (6), p.1323-1333 |
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| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_11147761 |
| source | SpringerLink Journals (MCLS) |
| subjects | 13/31 45/23 45/91 631/67/69 692/699/67/1990 Amplification Cancer Research CD38 antigen CD70 antigen CD8 antigen Cell proliferation Critical Care Medicine CXCR4 protein Diagnosis Effector cells Hematology Immunotherapy Intensive Internal Medicine Longitudinal studies Lymphocytes Lymphocytes T MAP kinase Medicine Medicine & Public Health Multiple myeloma Next-generation sequencing Oncology Sequence analysis Therapeutic targets Tumor microenvironment Tumors |
| title | Beyond the marrow: insights from comprehensive next-generation sequencing of extramedullary multiple myeloma tumors |
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