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An IL-4 signalling axis in bone marrow drives pro-tumorigenic myelopoiesis

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  • Barry, S. T., Gabrilovich, D. I., Sansom, O. J., Campbell, A. D. & Morton, J. P. Therapeutic targeting of tumour myeloid cells. Nat. Rev. Cancer 23, 216–237 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

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    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rabe, K. F. et al. Efficacy and safety of dupilumab in glucocorticoid-dependent severe asthma. N. Engl. J. Med. 378, 2475–2485 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Simpson, E. L. et al. Two phase 3 trials of dupilumab versus placebo in atopic dermatitis. N. Engl. J. Med. 375, 2335–2348 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Beck, K. M., Yang, E. J., Sekhon, S., Bhutani, T. & Liao, W. Dupilumab treatment for generalized prurigo nodularis. JAMA Dermatol. 155, 118–120 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Herbst, R. S., Morgensztern, D. & Boshoff, C. The biology and management of non-small cell lung cancer. Nature 553, 446–454 (2018).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Lavin, Y. et al. Innate immune landscape in early lung adenocarcinoma by paired single-cell analyses. Cell 169, 750–765.e717 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Leader, A. M. et al. Single-cell analysis of human non-small cell lung cancer lesions refines tumor classification and patient stratification. Cancer Cell 39, 1594–1609.e1512 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Casanova-Acebes, M. et al. Tissue-resident macrophages provide a pro-tumorigenic niche to early NSCLC cells. Nature 595, 578–584 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Loyher, P. L. et al. Macrophages of distinct origins contribute to tumor development in the lung. J. Exp. Med. 215, 2536–2553 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Maier, B. et al. A conserved dendritic-cell regulatory program limits antitumour immunity. Nature 580, 257–262 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Park, M. D. et al. TREM2 macrophages drive NK cell paucity and dysfunction in lung cancer. Nat. Immunol. 24, 792–801 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Loschko, J. et al. Absence of MHC class II on cDCs results in microbial-dependent intestinal inflammation. J. Exp. Med. 213, 517–534 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Karasawa, K. et al. Vascular-resident CD169-positive monocytes and macrophages control neutrophil accumulation in the kidney with ischemia-reperfusion injury. J. Am. Soc. Nephrol. 26, 896–906 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lee, P. P. et al. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15, 763–774 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Liu, Z. et al. Fate mapping via Ms4a3-expression history traces monocyte-derived cells. Cell 178, 1509–1525 e1519 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Horton, B. L. et al. Lack of CD8+ T cell effector differentiation during priming mediates checkpoint blockade resistance in non–small cell lung cancer. Sci. Immunol. 6, eabi8800 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Burger, M. L. et al. Antigen dominance hierarchies shape TCF1+ progenitor CD8 T cell phenotypes in tumors. Cell 184, 4996–5014.e4926 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chihara, N. et al. Induction and transcriptional regulation of the co-inhibitory gene module in T cells. Nature 558, 454–459 (2018).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Khan, O. et al. TOX transcriptionally and epigenetically programs CD8+ T cell exhaustion. Nature 571, 211–218 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Naluyima, P. et al. Terminal effector CD8 T cells defined by an IKZF2+IL-7R transcriptional signature express FcγRIIIA, expand in HIV infection, and mediate potent HIV-specific antibody-dependent cellular cytotoxicity. J Immunol 203, 2210–2221 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Akimova, T., Beier, U. H., Wang, L., Levine, M. H. & Hancock, W. W. Helios expression is a marker of T cell activation and proliferation. PLoS ONE 6, e24226 (2011).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Thome, M. Multifunctional roles for MALT1 in T-cell activation. Nat. Rev. Immunol. 8, 495–500 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yona, S. et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38, 79–91 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Passegue, E., Wagner, E. F. & Weissman, I. L. JunB deficiency leads to a myeloproliferative disorder arising from hematopoietic stem cells. Cell 119, 431–443 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Abram, C. L., Roberge, G. L., Hu, Y. & Lowell, C. A. Comparative analysis of the efficiency and specificity of myeloid-Cre deleting strains using ROSA-EYFP reporter mice. J. Immunol. Methods 408, 89–100 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mohrs, M., Shinkai, K., Mohrs, K. & Locksley, R. M. Analysis of type 2 immunity in vivo with a bicistronic IL-4 reporter. Immunity 15, 303–311 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hanna, R. N. et al. The transcription factor NR4A1 (Nur77) controls bone marrow differentiation and the survival of Ly6C monocytes. Nat. Immunol. 12, 778–785 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kurotaki, D. et al. Transcription factor IRF8 governs enhancer landscape dynamics in mononuclear phagocyte progenitors. Cell Rep. 22, 2628–2641 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhao, F. et al. S100A9 a new marker for monocytic human myeloid-derived suppressor cells. Immunology 136, 176–183 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hegde, S., Leader, A. M. & Merad, M. MDSC: markers, development, states, and unaddressed complexity. Immunity 54, 875–884 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Seita, J. & Weissman, I. L. Hematopoietic stem cell: self-renewal versus differentiation. Wiley Interdiscip. Rev. Syst. Biol. Med. 2, 640–653 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yanez, A. et al. Granulocyte-monocyte progenitors and monocyte-dendritic cell progenitors independently produce functionally distinct monocytes. Immunity 47, 890–902 e894 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mastio, J. et al. Identification of monocyte-like precursors of granulocytes in cancer as a mechanism for accumulation of PMN-MDSCs. J. Exp. Med. 216, 2150–2169 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nelms, K., Keegan, A. D., Zamorano, J., Ryan, J. J. & Paul, W. E. The IL-4 receptor: signaling mechanisms and biologic functions. Annu. Rev. Immunol. 17, 701–738 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jenkins, S. J. et al. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332, 1284–1288 (2011).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Paul, F. et al. Transcriptional heterogeneity and lineage commitment in myeloid progenitors. Cell 163, 1663–1677 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kwok, I. et al. Combinatorial single-cell analyses of granulocyte-monocyte progenitor heterogeneity reveals an early uni-potent neutrophil progenitor. Immunity 53, 303–318.e305 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Olsson, A. et al. Single-cell analysis of mixed-lineage states leading to a binary cell fate choice. Nature 537, 698–702 (2016).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Anderson, K. G. et al. Intravascular staining for discrimination of vascular and tissue leukocytes. Nat. Protoc. 9, 209–222 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tsutsui, H. et al. The basophil-specific protease mMCP-8 provokes an inflammatory response in the skin with microvascular hyperpermeability and leukocyte infiltration. J. Biol. Chem. 292, 1061–1067 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Cohen, M. et al. Lung single-cell signaling interaction map reveals basophil role in macrophage imprinting. Cell 175, 1031–1044.e1018 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Obata, K. et al. Basophils are essential initiators of a novel type of chronic allergic inflammation. Blood 110, 913–920 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Schultze, J. L., Mass, E. & Schlitzer, A. Emerging principles in myelopoiesis at homeostasis and during infection and inflammation. Immunity 50, 288–301 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Veglia, F., Sanseviero, E. & Gabrilovich, D. I. Myeloid-derived suppressor cells in the era of increasing myeloid cell diversity. Nat. Rev. Immunol. 21, 485–498 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pellefigues, C. et al. Diverse innate stimuli activate basophils through pathways involving Syk and IkappaB kinases. Proc. Natl Acad. Sci. USA 118, e2019524118 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gandhi, L. et al. Pembrolizumab plus chemotherapy in metastatic non-small-cell lung cancer. N. Engl. J. Med. 378, 2078–2092 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Spigel, D. R. et al. Five-year survival outcomes from the PACIFIC trial: durvalumab after chemoradiotherapy in stage III non-small-cell lung cancer. J. Clin. Oncol. 40, 1301–1311 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Herbst, R. S. et al. Five year survival update from KEYNOTE-010: pembrolizumab versus docetaxel for previously treated, programmed death-ligand 1-positive advanced NSCLC. J. Thorac. Oncol. 16, 1718–1732 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

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    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Patil, N. S. et al. Intratumoral plasma cells predict outcomes to PD-L1 blockade in non-small cell lung cancer. Cancer Cell 40, 289–300.e284 (2022).

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  • Barry, S. T., Gabrilovich, D. I., Sansom, O. J., Campbell, A. D. & Morton, J. P. Therapeutic targeting of tumour myeloid cells. Nat. Rev. Cancer 23, 216–237 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Castro, M. et al. Dupilumab efficacy and safety in moderate-to-severe uncontrolled asthma. N. Engl. J. Med. 378, 2486–2496 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rabe, K. F. et al. Efficacy and safety of dupilumab in glucocorticoid-dependent severe asthma. N. Engl. J. Med. 378, 2475–2485 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Simpson, E. L. et al. Two phase 3 trials of dupilumab versus placebo in atopic dermatitis. N. Engl. J. Med. 375, 2335–2348 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Beck, K. M., Yang, E. J., Sekhon, S., Bhutani, T. & Liao, W. Dupilumab treatment for generalized prurigo nodularis. JAMA Dermatol. 155, 118–120 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Herbst, R. S., Morgensztern, D. & Boshoff, C. The biology and management of non-small cell lung cancer. Nature 553, 446–454 (2018).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Lavin, Y. et al. Innate immune landscape in early lung adenocarcinoma by paired single-cell analyses. Cell 169, 750–765.e717 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Leader, A. M. et al. Single-cell analysis of human non-small cell lung cancer lesions refines tumor classification and patient stratification. Cancer Cell 39, 1594–1609.e1512 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Casanova-Acebes, M. et al. Tissue-resident macrophages provide a pro-tumorigenic niche to early NSCLC cells. Nature 595, 578–584 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Loyher, P. L. et al. Macrophages of distinct origins contribute to tumor development in the lung. J. Exp. Med. 215, 2536–2553 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Maier, B. et al. A conserved dendritic-cell regulatory program limits antitumour immunity. Nature 580, 257–262 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Park, M. D. et al. TREM2 macrophages drive NK cell paucity and dysfunction in lung cancer. Nat. Immunol. 24, 792–801 (2023).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Loschko, J. et al. Absence of MHC class II on cDCs results in microbial-dependent intestinal inflammation. J. Exp. Med. 213, 517–534 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Karasawa, K. et al. Vascular-resident CD169-positive monocytes and macrophages control neutrophil accumulation in the kidney with ischemia-reperfusion injury. J. Am. Soc. Nephrol. 26, 896–906 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lee, P. P. et al. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15, 763–774 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Liu, Z. et al. Fate mapping via Ms4a3-expression history traces monocyte-derived cells. Cell 178, 1509–1525 e1519 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Horton, B. L. et al. Lack of CD8+ T cell effector differentiation during priming mediates checkpoint blockade resistance in non–small cell lung cancer. Sci. Immunol. 6, eabi8800 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Burger, M. L. et al. Antigen dominance hierarchies shape TCF1+ progenitor CD8 T cell phenotypes in tumors. Cell 184, 4996–5014.e4926 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chihara, N. et al. Induction and transcriptional regulation of the co-inhibitory gene module in T cells. Nature 558, 454–459 (2018).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Khan, O. et al. TOX transcriptionally and epigenetically programs CD8+ T cell exhaustion. Nature 571, 211–218 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Naluyima, P. et al. Terminal effector CD8 T cells defined by an IKZF2+IL-7R transcriptional signature express FcγRIIIA, expand in HIV infection, and mediate potent HIV-specific antibody-dependent cellular cytotoxicity. J Immunol 203, 2210–2221 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Akimova, T., Beier, U. H., Wang, L., Levine, M. H. & Hancock, W. W. Helios expression is a marker of T cell activation and proliferation. PLoS ONE 6, e24226 (2011).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Thome, M. Multifunctional roles for MALT1 in T-cell activation. Nat. Rev. Immunol. 8, 495–500 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yona, S. et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38, 79–91 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Passegue, E., Wagner, E. F. & Weissman, I. L. JunB deficiency leads to a myeloproliferative disorder arising from hematopoietic stem cells. Cell 119, 431–443 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Abram, C. L., Roberge, G. L., Hu, Y. & Lowell, C. A. Comparative analysis of the efficiency and specificity of myeloid-Cre deleting strains using ROSA-EYFP reporter mice. J. Immunol. Methods 408, 89–100 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mohrs, M., Shinkai, K., Mohrs, K. & Locksley, R. M. Analysis of type 2 immunity in vivo with a bicistronic IL-4 reporter. Immunity 15, 303–311 (2001).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hanna, R. N. et al. The transcription factor NR4A1 (Nur77) controls bone marrow differentiation and the survival of Ly6C monocytes. Nat. Immunol. 12, 778–785 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kurotaki, D. et al. Transcription factor IRF8 governs enhancer landscape dynamics in mononuclear phagocyte progenitors. Cell Rep. 22, 2628–2641 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhao, F. et al. S100A9 a new marker for monocytic human myeloid-derived suppressor cells. Immunology 136, 176–183 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hegde, S., Leader, A. M. & Merad, M. MDSC: markers, development, states, and unaddressed complexity. Immunity 54, 875–884 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Seita, J. & Weissman, I. L. Hematopoietic stem cell: self-renewal versus differentiation. Wiley Interdiscip. Rev. Syst. Biol. Med. 2, 640–653 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yanez, A. et al. Granulocyte-monocyte progenitors and monocyte-dendritic cell progenitors independently produce functionally distinct monocytes. Immunity 47, 890–902 e894 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mastio, J. et al. Identification of monocyte-like precursors of granulocytes in cancer as a mechanism for accumulation of PMN-MDSCs. J. Exp. Med. 216, 2150–2169 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nelms, K., Keegan, A. D., Zamorano, J., Ryan, J. J. & Paul, W. E. The IL-4 receptor: signaling mechanisms and biologic functions. Annu. Rev. Immunol. 17, 701–738 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Jenkins, S. J. et al. Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332, 1284–1288 (2011).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Paul, F. et al. Transcriptional heterogeneity and lineage commitment in myeloid progenitors. Cell 163, 1663–1677 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kwok, I. et al. Combinatorial single-cell analyses of granulocyte-monocyte progenitor heterogeneity reveals an early uni-potent neutrophil progenitor. Immunity 53, 303–318.e305 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Olsson, A. et al. Single-cell analysis of mixed-lineage states leading to a binary cell fate choice. Nature 537, 698–702 (2016).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Anderson, K. G. et al. Intravascular staining for discrimination of vascular and tissue leukocytes. Nat. Protoc. 9, 209–222 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tsutsui, H. et al. The basophil-specific protease mMCP-8 provokes an inflammatory response in the skin with microvascular hyperpermeability and leukocyte infiltration. J. Biol. Chem. 292, 1061–1067 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Cohen, M. et al. Lung single-cell signaling interaction map reveals basophil role in macrophage imprinting. Cell 175, 1031–1044.e1018 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Obata, K. et al. Basophils are essential initiators of a novel type of chronic allergic inflammation. Blood 110, 913–920 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Schultze, J. L., Mass, E. & Schlitzer, A. Emerging principles in myelopoiesis at homeostasis and during infection and inflammation. Immunity 50, 288–301 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Veglia, F., Sanseviero, E. & Gabrilovich, D. I. Myeloid-derived suppressor cells in the era of increasing myeloid cell diversity. Nat. Rev. Immunol. 21, 485–498 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pellefigues, C. et al. Diverse innate stimuli activate basophils through pathways involving Syk and IkappaB kinases. Proc. Natl Acad. Sci. USA 118, e2019524118 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gandhi, L. et al. Pembrolizumab plus chemotherapy in metastatic non-small-cell lung cancer. N. Engl. J. Med. 378, 2078–2092 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Spigel, D. R. et al. Five-year survival outcomes from the PACIFIC trial: durvalumab after chemoradiotherapy in stage III non-small-cell lung cancer. J. Clin. Oncol. 40, 1301–1311 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Herbst, R. S. et al. Five year survival update from KEYNOTE-010: pembrolizumab versus docetaxel for previously treated, programmed death-ligand 1-positive advanced NSCLC. J. Thorac. Oncol. 16, 1718–1732 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Choi, H. et al. Transcriptome analysis of individual stromal cell populations identifies stroma–tumor crosstalk in mouse lung cancer model. Cell Rep. 10, 1187–1201 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Patil, N. S. et al. Intratumoral plasma cells predict outcomes to PD-L1 blockade in non-small cell lung cancer. Cancer Cell 40, 289–300.e284 (2022).

    Article 
    CAS 
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