Immunoediting instructs tumor metabolic reprogramming to support immune evasion

Chin Hsien Tsai; Yu Ming Chuang; Xiaoyun Li; Yi Ru Yu; Sheue Fen Tzeng; Shao Thing Teoh; Katherine E. Lindblad; Mario Di Matteo; Wan Chen Cheng; Pei Chun Hsueh; Kung Chi Kao; Hana Imrichova; Likun Duan; Hector Gallart-Ayala; Pei Wen Hsiao; Massimiliano Mazzone; Julijana Ivanesevic; Xiaojing Liu; Karin E. de Visser; Amaia Lujambio; Sophia Y. Lunt; Susan M. Kaech; Ping Chih Ho

doi:10.1016/j.cmet.2022.12.003

Immunoediting instructs tumor metabolic reprogramming to support immune evasion

Chin Hsien Tsai, Yu Ming Chuang, Xiaoyun Li, Yi Ru Yu, Sheue Fen Tzeng, Shao Thing Teoh, Katherine E. Lindblad, Mario Di Matteo, Wan Chen Cheng, Pei Chun Hsueh, Kung Chi Kao, Hana Imrichova, Likun Duan, Hector Gallart-Ayala, Pei Wen Hsiao, Massimiliano Mazzone, Julijana Ivanesevic, Xiaojing Liu, Karin E. de Visser, Amaia LujambioSophia Y. Lunt, Susan M. Kaech, Ping Chih Ho

Research output: Contribution to journal › Article › peer-review

33 Scopus citations

Abstract

Immunoediting sculpts immunogenicity and thwarts host anti-tumor responses in tumor cells during tumorigenesis; however, it remains unknown whether metabolic programming of tumor cells can be guided by immunosurveillance. Here, we report that T cell-mediated immunosurveillance in early-stage tumorigenesis instructs c-Myc upregulation and metabolic reprogramming in tumor cells. This previously unexplored tumor-immune interaction is controlled by non-canonical interferon gamma (IFNγ)-STAT3 signaling and supports tumor immune evasion. Our findings uncover that immunoediting instructs deregulated bioenergetic programs in tumor cells to empower them to disarm the T cell-mediated immunosurveillance by imposing metabolic tug-of-war between tumor and infiltrating T cells and forming the suppressive tumor microenvironment.

Original language	English
Pages (from-to)	118-133.e7
Journal	Cell Metabolism
Volume	35
Issue number	1
DOIs	https://doi.org/10.1016/j.cmet.2022.12.003
State	Published - 3 Jan 2023

Keywords

IFNγ
Myc
STAT3
immunoediting
immunosurveillance
tumor immunology

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10.1016/j.cmet.2022.12.003

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Tsai, C. H., Chuang, Y. M., Li, X., Yu, Y. R., Tzeng, S. F., Teoh, S. T., Lindblad, K. E., Di Matteo, M., Cheng, W. C., Hsueh, P. C., Kao, K. C., Imrichova, H., Duan, L., Gallart-Ayala, H., Hsiao, P. W., Mazzone, M., Ivanesevic, J., Liu, X., de Visser, K. E., ... Ho, P. C. (2023). Immunoediting instructs tumor metabolic reprogramming to support immune evasion. Cell Metabolism, 35(1), 118-133.e7. https://doi.org/10.1016/j.cmet.2022.12.003

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title = "Immunoediting instructs tumor metabolic reprogramming to support immune evasion",

abstract = "Immunoediting sculpts immunogenicity and thwarts host anti-tumor responses in tumor cells during tumorigenesis; however, it remains unknown whether metabolic programming of tumor cells can be guided by immunosurveillance. Here, we report that T cell-mediated immunosurveillance in early-stage tumorigenesis instructs c-Myc upregulation and metabolic reprogramming in tumor cells. This previously unexplored tumor-immune interaction is controlled by non-canonical interferon gamma (IFNγ)-STAT3 signaling and supports tumor immune evasion. Our findings uncover that immunoediting instructs deregulated bioenergetic programs in tumor cells to empower them to disarm the T cell-mediated immunosurveillance by imposing metabolic tug-of-war between tumor and infiltrating T cells and forming the suppressive tumor microenvironment.",

keywords = "IFNγ, Myc, STAT3, immunoediting, immunosurveillance, tumor immunology",

author = "Tsai, {Chin Hsien} and Chuang, {Yu Ming} and Xiaoyun Li and Yu, {Yi Ru} and Tzeng, {Sheue Fen} and Teoh, {Shao Thing} and Lindblad, {Katherine E.} and {Di Matteo}, Mario and Cheng, {Wan Chen} and Hsueh, {Pei Chun} and Kao, {Kung Chi} and Hana Imrichova and Likun Duan and Hector Gallart-Ayala and Hsiao, {Pei Wen} and Massimiliano Mazzone and Julijana Ivanesevic and Xiaojing Liu and {de Visser}, {Karin E.} and Amaia Lujambio and Lunt, {Sophia Y.} and Kaech, {Susan M.} and Ho, {Ping Chih}",

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year = "2023",

month = jan,

day = "3",

doi = "10.1016/j.cmet.2022.12.003",

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Tsai, CH, Chuang, YM, Li, X, Yu, YR, Tzeng, SF, Teoh, ST, Lindblad, KE, Di Matteo, M, Cheng, WC, Hsueh, PC, Kao, KC, Imrichova, H, Duan, L, Gallart-Ayala, H, Hsiao, PW, Mazzone, M, Ivanesevic, J, Liu, X, de Visser, KE, Lujambio, A, Lunt, SY, Kaech, SM & Ho, PC 2023, 'Immunoediting instructs tumor metabolic reprogramming to support immune evasion', Cell Metabolism, vol. 35, no. 1, pp. 118-133.e7. https://doi.org/10.1016/j.cmet.2022.12.003

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AU - Tsai, Chin Hsien

AU - Chuang, Yu Ming

AU - Li, Xiaoyun

AU - Yu, Yi Ru

AU - Tzeng, Sheue Fen

AU - Teoh, Shao Thing

AU - Lindblad, Katherine E.

AU - Di Matteo, Mario

AU - Cheng, Wan Chen

AU - Hsueh, Pei Chun

AU - Kao, Kung Chi

AU - Imrichova, Hana

AU - Duan, Likun

AU - Gallart-Ayala, Hector

AU - Hsiao, Pei Wen

AU - Mazzone, Massimiliano

AU - Ivanesevic, Julijana

AU - Liu, Xiaojing

AU - de Visser, Karin E.

AU - Lujambio, Amaia

AU - Lunt, Sophia Y.

AU - Kaech, Susan M.

AU - Ho, Ping Chih

PY - 2023/1/3

Y1 - 2023/1/3

N2 - Immunoediting sculpts immunogenicity and thwarts host anti-tumor responses in tumor cells during tumorigenesis; however, it remains unknown whether metabolic programming of tumor cells can be guided by immunosurveillance. Here, we report that T cell-mediated immunosurveillance in early-stage tumorigenesis instructs c-Myc upregulation and metabolic reprogramming in tumor cells. This previously unexplored tumor-immune interaction is controlled by non-canonical interferon gamma (IFNγ)-STAT3 signaling and supports tumor immune evasion. Our findings uncover that immunoediting instructs deregulated bioenergetic programs in tumor cells to empower them to disarm the T cell-mediated immunosurveillance by imposing metabolic tug-of-war between tumor and infiltrating T cells and forming the suppressive tumor microenvironment.

AB - Immunoediting sculpts immunogenicity and thwarts host anti-tumor responses in tumor cells during tumorigenesis; however, it remains unknown whether metabolic programming of tumor cells can be guided by immunosurveillance. Here, we report that T cell-mediated immunosurveillance in early-stage tumorigenesis instructs c-Myc upregulation and metabolic reprogramming in tumor cells. This previously unexplored tumor-immune interaction is controlled by non-canonical interferon gamma (IFNγ)-STAT3 signaling and supports tumor immune evasion. Our findings uncover that immunoediting instructs deregulated bioenergetic programs in tumor cells to empower them to disarm the T cell-mediated immunosurveillance by imposing metabolic tug-of-war between tumor and infiltrating T cells and forming the suppressive tumor microenvironment.

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KW - Myc

KW - STAT3

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DO - 10.1016/j.cmet.2022.12.003

M3 - Article

AN - SCOPUS:85144970861

SN - 1550-4131

VL - 35

SP - 118-133.e7

JO - Cell Metabolism

JF - Cell Metabolism

IS - 1

ER -

Immunoediting instructs tumor metabolic reprogramming to support immune evasion

Abstract

Keywords

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