Alice Y Zhou, Nancy D Marin, Sadia Afrin, Pamela Wong, Jennifer Tran, Miriam T Jacobs, Michelle Becker-Hapak, Lynne Marsala, Mark Foster, Jennifer A Foltz, Carly C Neal, David A Russler-Germain, Lyra Morina, Yeeun Paik, Celia C Cubitt, Timothy Schappe, Patrick Pence, Ethan McClain, Sarah Kelley, Julie Fortier, Mark Fiala, Michael Slade, Mark Schroeder, Keith Stockerl-Goldstein, Ravi Vij, Feng Gao, Melissa M Berrien-Elliott, Todd A Fehniger
{"title":"记忆样NK细胞分化,抑制NKG2A阻断,以及通过抗体或CAR工程提高识别,共同增强NK细胞对多发性骨髓瘤的攻击。","authors":"Alice Y Zhou, Nancy D Marin, Sadia Afrin, Pamela Wong, Jennifer Tran, Miriam T Jacobs, Michelle Becker-Hapak, Lynne Marsala, Mark Foster, Jennifer A Foltz, Carly C Neal, David A Russler-Germain, Lyra Morina, Yeeun Paik, Celia C Cubitt, Timothy Schappe, Patrick Pence, Ethan McClain, Sarah Kelley, Julie Fortier, Mark Fiala, Michael Slade, Mark Schroeder, Keith Stockerl-Goldstein, Ravi Vij, Feng Gao, Melissa M Berrien-Elliott, Todd A Fehniger","doi":"10.1093/jimmun/vkae004","DOIUrl":null,"url":null,"abstract":"<p><p>Natural killer (NK) cells are a promising approach for cellular cancer immunotherapy and are being investigated to treat patients with multiple myeloma (MM). We found that MM patient blood NK cell frequencies were normal with increased activating receptors and cytotoxic granules, without evidence of functional exhaustion. Despite this activated state, MM target cells were resistant to conventional NK cells by unclear mechanisms. Memory-like (ML) NK cells are generated after brief activation via the interleukin (IL)-12, IL-15, and IL-18 receptors and exhibit multiple enhanced antitumor properties. ML NK cell differentiation improved healthy donor and MM patient NK cell responses against MM target cells, in vitro and in vivo in immunodeficient murine xenograft models. Moreover, incorporating NKG2A checkpoint blockade to overcome HLA-E-induced inhibition further enhanced ML NK cell responses against MM in vitro and in vivo. Because activating receptor recognition of MM by ML NK cells was inadequate, strategies to improve this were investigated. Utilizing anti-SLAMF7 monoclonal antibody (elotuzumab) or anti-BCMA chimeric antigen receptors resulted in robust increases in ML NK cell functional responses against MM. In summary, ML differentiation enhances NK cell attack against myeloma, and combination with approaches to block inhibitory checkpoints and promote MM-specific activation are promising translational NK cell strategies for MM immunotherapy.</p>","PeriodicalId":16045,"journal":{"name":"Journal of immunology","volume":"214 1","pages":"1-11"},"PeriodicalIF":3.6000,"publicationDate":"2025-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11844139/pdf/","citationCount":"0","resultStr":"{\"title\":\"Memory-like NK cell differentiation, inhibitory NKG2A blockade, and improved recognition via antibody or CAR engineering combine to enhance NK cell attack against multiple myeloma.\",\"authors\":\"Alice Y Zhou, Nancy D Marin, Sadia Afrin, Pamela Wong, Jennifer Tran, Miriam T Jacobs, Michelle Becker-Hapak, Lynne Marsala, Mark Foster, Jennifer A Foltz, Carly C Neal, David A Russler-Germain, Lyra Morina, Yeeun Paik, Celia C Cubitt, Timothy Schappe, Patrick Pence, Ethan McClain, Sarah Kelley, Julie Fortier, Mark Fiala, Michael Slade, Mark Schroeder, Keith Stockerl-Goldstein, Ravi Vij, Feng Gao, Melissa M Berrien-Elliott, Todd A Fehniger\",\"doi\":\"10.1093/jimmun/vkae004\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Natural killer (NK) cells are a promising approach for cellular cancer immunotherapy and are being investigated to treat patients with multiple myeloma (MM). We found that MM patient blood NK cell frequencies were normal with increased activating receptors and cytotoxic granules, without evidence of functional exhaustion. Despite this activated state, MM target cells were resistant to conventional NK cells by unclear mechanisms. Memory-like (ML) NK cells are generated after brief activation via the interleukin (IL)-12, IL-15, and IL-18 receptors and exhibit multiple enhanced antitumor properties. ML NK cell differentiation improved healthy donor and MM patient NK cell responses against MM target cells, in vitro and in vivo in immunodeficient murine xenograft models. Moreover, incorporating NKG2A checkpoint blockade to overcome HLA-E-induced inhibition further enhanced ML NK cell responses against MM in vitro and in vivo. Because activating receptor recognition of MM by ML NK cells was inadequate, strategies to improve this were investigated. Utilizing anti-SLAMF7 monoclonal antibody (elotuzumab) or anti-BCMA chimeric antigen receptors resulted in robust increases in ML NK cell functional responses against MM. In summary, ML differentiation enhances NK cell attack against myeloma, and combination with approaches to block inhibitory checkpoints and promote MM-specific activation are promising translational NK cell strategies for MM immunotherapy.</p>\",\"PeriodicalId\":16045,\"journal\":{\"name\":\"Journal of immunology\",\"volume\":\"214 1\",\"pages\":\"1-11\"},\"PeriodicalIF\":3.6000,\"publicationDate\":\"2025-01-01\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11844139/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Journal of immunology\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1093/jimmun/vkae004\",\"RegionNum\":3,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q2\",\"JCRName\":\"IMMUNOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of immunology","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1093/jimmun/vkae004","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"IMMUNOLOGY","Score":null,"Total":0}
Memory-like NK cell differentiation, inhibitory NKG2A blockade, and improved recognition via antibody or CAR engineering combine to enhance NK cell attack against multiple myeloma.
Natural killer (NK) cells are a promising approach for cellular cancer immunotherapy and are being investigated to treat patients with multiple myeloma (MM). We found that MM patient blood NK cell frequencies were normal with increased activating receptors and cytotoxic granules, without evidence of functional exhaustion. Despite this activated state, MM target cells were resistant to conventional NK cells by unclear mechanisms. Memory-like (ML) NK cells are generated after brief activation via the interleukin (IL)-12, IL-15, and IL-18 receptors and exhibit multiple enhanced antitumor properties. ML NK cell differentiation improved healthy donor and MM patient NK cell responses against MM target cells, in vitro and in vivo in immunodeficient murine xenograft models. Moreover, incorporating NKG2A checkpoint blockade to overcome HLA-E-induced inhibition further enhanced ML NK cell responses against MM in vitro and in vivo. Because activating receptor recognition of MM by ML NK cells was inadequate, strategies to improve this were investigated. Utilizing anti-SLAMF7 monoclonal antibody (elotuzumab) or anti-BCMA chimeric antigen receptors resulted in robust increases in ML NK cell functional responses against MM. In summary, ML differentiation enhances NK cell attack against myeloma, and combination with approaches to block inhibitory checkpoints and promote MM-specific activation are promising translational NK cell strategies for MM immunotherapy.
期刊介绍:
The JI publishes novel, peer-reviewed findings in all areas of experimental immunology, including innate and adaptive immunity, inflammation, host defense, clinical immunology, autoimmunity and more. Special sections include Cutting Edge articles, Brief Reviews and Pillars of Immunology. The JI is published by The American Association of Immunologists (AAI)