Mouse pulmonary interstitial macrophages mediate the pro-tumorigenic effects of IL-9

Although IL-9 has potent anti-tumor activity in adoptive cell transfer therapy, some models suggest that it can promote tumor growth. Here, we show that IL-9 signaling is associated with poor outcomes in patients with various forms of lung cancer, and is required for lung tumor growth in multiple mo...

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Published inNature communications Vol. 13; no. 1; pp. 3811 - 19
Main Authors Fu, Yongyao, Pajulas, Abigail, Wang, Jocelyn, Zhou, Baohua, Cannon, Anthony, Cheung, Cherry Cheuk Lam, Zhang, Jilu, Zhou, Huaxin, Fisher, Amanda Jo, Omstead, David T., Khan, Sabrina, Han, Lei, Renauld, Jean-Christophe, Paczesny, Sophie, Gao, Hongyu, Liu, Yunlong, Yang, Lei, Tighe, Robert M., Licona-Limón, Paula, Flavell, Richard A., Takatsuka, Shogo, Kitamura, Daisuke, Sun, Jie, Bilgicer, Basar, Sears, Catherine R., Yang, Kai, Kaplan, Mark H.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.07.2022
Nature Publishing Group
Nature Portfolio
Subjects
13
13/1
13/21
13/31
38
38/91
631/250/127/1213
631/250/1619/554/1898
631/250/2504/342
631/250/580
64
64/60
Adoptive transfer
Animal models
Animals
Anticancer properties
Antitumor agents
Arginase
Carcinogenesis - metabolism
CD11c antigen
CD4 antigen
Cell culture
Cytokines
Humanities and Social Sciences
Interleukin 9
Interleukin 9 receptors
Interleukin-9 - genetics
Interleukin-9 - metabolism
Lung cancer
Lung Neoplasms - metabolism
Lung Neoplasms - pathology
Lymphocytes
Lymphocytes T
Macrophages
Macrophages - metabolism
Macrophages - pathology
Macrophages, Alveolar - metabolism
Mice
multidisciplinary
Nanoparticles
Science
Science (multidisciplinary)
Signaling
Therapeutic applications
Therapeutic targets
Tumor microenvironment
Tumors
Online AccessGet full text

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Abstract Although IL-9 has potent anti-tumor activity in adoptive cell transfer therapy, some models suggest that it can promote tumor growth. Here, we show that IL-9 signaling is associated with poor outcomes in patients with various forms of lung cancer, and is required for lung tumor growth in multiple mouse models. CD4 + T cell-derived IL-9 promotes the expansion of both CD11c + and CD11c − interstitial macrophage populations in lung tumor models. Mechanistically, the IL-9/macrophage axis requires arginase 1 (Arg1) to mediate tumor growth. Indeed, adoptive transfer of Arg1 + but not Arg1 - lung macrophages to Il9r −/− mice promotes tumor growth. Moreover, targeting IL-9 signaling using macrophage-specific nanoparticles restricts lung tumor growth in mice. Lastly, elevated expression of IL-9R and Arg1 in tumor lesions is associated with poor prognosis in lung cancer patients. Thus, our study suggests the IL-9/macrophage/Arg1 axis is a potential therapeutic target for lung cancer therapy. The role of IL-9 in the tumor microenvironment and its effects on macrophages remains unclear. Here, the authors show that IL-9 promotes the expansion of pulmonary macrophages and that targeting the IL-9R/arginase 1 axis restricts tumor growth, thus identifying this cytokine pathway as a potential therapeutic target.
AbstractList Although IL-9 has potent anti-tumor activity in adoptive cell transfer therapy, some models suggest that it can promote tumor growth. Here, we show that IL-9 signaling is associated with poor outcomes in patients with various forms of lung cancer, and is required for lung tumor growth in multiple mouse models. CD4 T cell-derived IL-9 promotes the expansion of both CD11c and CD11c interstitial macrophage populations in lung tumor models. Mechanistically, the IL-9/macrophage axis requires arginase 1 (Arg1) to mediate tumor growth. Indeed, adoptive transfer of Arg1 but not Arg1 lung macrophages to Il9r mice promotes tumor growth. Moreover, targeting IL-9 signaling using macrophage-specific nanoparticles restricts lung tumor growth in mice. Lastly, elevated expression of IL-9R and Arg1 in tumor lesions is associated with poor prognosis in lung cancer patients. Thus, our study suggests the IL-9/macrophage/Arg1 axis is a potential therapeutic target for lung cancer therapy.
Although IL-9 has potent anti-tumor activity in adoptive cell transfer therapy, some models suggest that it can promote tumor growth. Here, we show that IL-9 signaling is associated with poor outcomes in patients with various forms of lung cancer, and is required for lung tumor growth in multiple mouse models. CD4 + T cell-derived IL-9 promotes the expansion of both CD11c + and CD11c − interstitial macrophage populations in lung tumor models. Mechanistically, the IL-9/macrophage axis requires arginase 1 (Arg1) to mediate tumor growth. Indeed, adoptive transfer of Arg1 + but not Arg1 - lung macrophages to Il9r −/− mice promotes tumor growth. Moreover, targeting IL-9 signaling using macrophage-specific nanoparticles restricts lung tumor growth in mice. Lastly, elevated expression of IL-9R and Arg1 in tumor lesions is associated with poor prognosis in lung cancer patients. Thus, our study suggests the IL-9/macrophage/Arg1 axis is a potential therapeutic target for lung cancer therapy. The role of IL-9 in the tumor microenvironment and its effects on macrophages remains unclear. Here, the authors show that IL-9 promotes the expansion of pulmonary macrophages and that targeting the IL-9R/arginase 1 axis restricts tumor growth, thus identifying this cytokine pathway as a potential therapeutic target.
Although IL-9 has potent anti-tumor activity in adoptive cell transfer therapy, some models suggest that it can promote tumor growth. Here, we show that IL-9 signaling is associated with poor outcomes in patients with various forms of lung cancer, and is required for lung tumor growth in multiple mouse models. CD4+ T cell-derived IL-9 promotes the expansion of both CD11c+ and CD11c- interstitial macrophage populations in lung tumor models. Mechanistically, the IL-9/macrophage axis requires arginase 1 (Arg1) to mediate tumor growth. Indeed, adoptive transfer of Arg1+ but not Arg1- lung macrophages to Il9r-/- mice promotes tumor growth. Moreover, targeting IL-9 signaling using macrophage-specific nanoparticles restricts lung tumor growth in mice. Lastly, elevated expression of IL-9R and Arg1 in tumor lesions is associated with poor prognosis in lung cancer patients. Thus, our study suggests the IL-9/macrophage/Arg1 axis is a potential therapeutic target for lung cancer therapy.Although IL-9 has potent anti-tumor activity in adoptive cell transfer therapy, some models suggest that it can promote tumor growth. Here, we show that IL-9 signaling is associated with poor outcomes in patients with various forms of lung cancer, and is required for lung tumor growth in multiple mouse models. CD4+ T cell-derived IL-9 promotes the expansion of both CD11c+ and CD11c- interstitial macrophage populations in lung tumor models. Mechanistically, the IL-9/macrophage axis requires arginase 1 (Arg1) to mediate tumor growth. Indeed, adoptive transfer of Arg1+ but not Arg1- lung macrophages to Il9r-/- mice promotes tumor growth. Moreover, targeting IL-9 signaling using macrophage-specific nanoparticles restricts lung tumor growth in mice. Lastly, elevated expression of IL-9R and Arg1 in tumor lesions is associated with poor prognosis in lung cancer patients. Thus, our study suggests the IL-9/macrophage/Arg1 axis is a potential therapeutic target for lung cancer therapy.
The role of IL-9 in the tumor microenvironment and its effects on macrophages remains unclear. Here, the authors show that IL-9 promotes the expansion of pulmonary macrophages and that targeting the IL-9R/arginase 1 axis restricts tumor growth, thus identifying this cytokine pathway as a potential therapeutic target.
Abstract Although IL-9 has potent anti-tumor activity in adoptive cell transfer therapy, some models suggest that it can promote tumor growth. Here, we show that IL-9 signaling is associated with poor outcomes in patients with various forms of lung cancer, and is required for lung tumor growth in multiple mouse models. CD4 + T cell-derived IL-9 promotes the expansion of both CD11c + and CD11c − interstitial macrophage populations in lung tumor models. Mechanistically, the IL-9/macrophage axis requires arginase 1 (Arg1) to mediate tumor growth. Indeed, adoptive transfer of Arg1 + but not Arg1 - lung macrophages to Il9r −/− mice promotes tumor growth. Moreover, targeting IL-9 signaling using macrophage-specific nanoparticles restricts lung tumor growth in mice. Lastly, elevated expression of IL-9R and Arg1 in tumor lesions is associated with poor prognosis in lung cancer patients. Thus, our study suggests the IL-9/macrophage/Arg1 axis is a potential therapeutic target for lung cancer therapy.
Although IL-9 has potent anti-tumor activity in adoptive cell transfer therapy, some models suggest that it can promote tumor growth. Here, we show that IL-9 signaling is associated with poor outcomes in patients with various forms of lung cancer, and is required for lung tumor growth in multiple mouse models. CD4+ T cell-derived IL-9 promotes the expansion of both CD11c+ and CD11c− interstitial macrophage populations in lung tumor models. Mechanistically, the IL-9/macrophage axis requires arginase 1 (Arg1) to mediate tumor growth. Indeed, adoptive transfer of Arg1+ but not Arg1- lung macrophages to Il9r−/− mice promotes tumor growth. Moreover, targeting IL-9 signaling using macrophage-specific nanoparticles restricts lung tumor growth in mice. Lastly, elevated expression of IL-9R and Arg1 in tumor lesions is associated with poor prognosis in lung cancer patients. Thus, our study suggests the IL-9/macrophage/Arg1 axis is a potential therapeutic target for lung cancer therapy.The role of IL-9 in the tumor microenvironment and its effects on macrophages remains unclear. Here, the authors show that IL-9 promotes the expansion of pulmonary macrophages and that targeting the IL-9R/arginase 1 axis restricts tumor growth, thus identifying this cytokine pathway as a potential therapeutic target.
ArticleNumber 3811
Author Zhou, Huaxin
Takatsuka, Shogo
Wang, Jocelyn
Zhou, Baohua
Fisher, Amanda Jo
Renauld, Jean-Christophe
Paczesny, Sophie
Cheung, Cherry Cheuk Lam
Tighe, Robert M.
Pajulas, Abigail
Omstead, David T.
Cannon, Anthony
Fu, Yongyao
Zhang, Jilu
Flavell, Richard A.
Han, Lei
Bilgicer, Basar
Sun, Jie
Gao, Hongyu
Sears, Catherine R.
Khan, Sabrina
Yang, Lei
Liu, Yunlong
Kaplan, Mark H.
Kitamura, Daisuke
Yang, Kai
Licona-Limón, Paula
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/35778404$$D View this record in MEDLINE/PubMed
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SSID ssj0000391844
Score 2.504699
Snippet Although IL-9 has potent anti-tumor activity in adoptive cell transfer therapy, some models suggest that it can promote tumor growth. Here, we show that IL-9...
Abstract Although IL-9 has potent anti-tumor activity in adoptive cell transfer therapy, some models suggest that it can promote tumor growth. Here, we show...
The role of IL-9 in the tumor microenvironment and its effects on macrophages remains unclear. Here, the authors show that IL-9 promotes the expansion of...
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Adoptive transfer
Animal models
Animals
Anticancer properties
Antitumor agents
Arginase
Carcinogenesis - metabolism
CD11c antigen
CD4 antigen
Cell culture
Cytokines
Humanities and Social Sciences
Interleukin 9
Interleukin 9 receptors
Interleukin-9 - genetics
Interleukin-9 - metabolism
Lung cancer
Lung Neoplasms - metabolism
Lung Neoplasms - pathology
Lymphocytes
Lymphocytes T
Macrophages
Macrophages - metabolism
Macrophages - pathology
Macrophages, Alveolar - metabolism
Mice
multidisciplinary
Nanoparticles
Science
Science (multidisciplinary)
Signaling
Therapeutic applications
Therapeutic targets
Tumor microenvironment
Tumors
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Title Mouse pulmonary interstitial macrophages mediate the pro-tumorigenic effects of IL-9
URI https://link.springer.com/article/10.1038/s41467-022-31596-7
https://www.ncbi.nlm.nih.gov/pubmed/35778404
https://www.proquest.com/docview/2683055602
https://www.proquest.com/docview/2684096800
https://pubmed.ncbi.nlm.nih.gov/PMC9249769
https://doaj.org/article/a1f3ef8fb84c42fd82f0039ff02e0d71
Volume 13
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