Emerging role of metabolic reprogramming in tumor immune evasion and immunotherapy

doi:10.1007/s11427-019-1735-4

Review

. 2021 Apr;64(4):534-547.

doi: 10.1007/s11427-019-1735-4. Epub 2020 Aug 17.

Emerging role of metabolic reprogramming in tumor immune evasion and immunotherapy

Chunmei Fan^{1

2

3}, Shanshan Zhang⁴, Zhaojian Gong⁵, Xiayu Li³, Bo Xiang^{1

2}, Hao Deng³, Ming Zhou^{1

2}, Guiyuan Li^{1

2}, Yong Li⁶, Wei Xiong^{1

2}, Zhaoyang Zeng^{7

8}, Xiaoling Li^{9

10}

Affiliations

¹ NHC Key Laboratory of Carcinogenesis, Hunan Cancer Hospital and the Affiliated Cancer Hospital, Xiangya School of Medicine, Central South University, Changsha, 410013, China.
² Key Laboratory of Carcinogenesis and Cancer Invasion of the Chinese Ministry of Education, Cancer Research Institute and School of Basic Medical Science, Central South University, Changsha, 410078, China.
³ Hunan Key Laboratory of Nonresolving Inflammation and Cancer, Disease Genome Research Center, the Third Xiangya Hospital, Central South University, Changsha, 410013, China.
⁴ Department of Stomatology, Xiangya Hospital, Central South University, Changsha, 410078, China.
⁵ Department of Oral and Maxillofacial Surgery, The Second Xiangya Hospital, Central South University, Changsha, 410011, China.
⁶ Department of Medicine, Dan L Duncan Comprehensive Cancer Center, Baylor College of Medicine, Houston, Texas, USA.
⁷ NHC Key Laboratory of Carcinogenesis, Hunan Cancer Hospital and the Affiliated Cancer Hospital, Xiangya School of Medicine, Central South University, Changsha, 410013, China. zengzhaoyang@csu.edu.cn.
⁸ Key Laboratory of Carcinogenesis and Cancer Invasion of the Chinese Ministry of Education, Cancer Research Institute and School of Basic Medical Science, Central South University, Changsha, 410078, China. zengzhaoyang@csu.edu.cn.
⁹ NHC Key Laboratory of Carcinogenesis, Hunan Cancer Hospital and the Affiliated Cancer Hospital, Xiangya School of Medicine, Central South University, Changsha, 410013, China. lixiaoling@csu.edu.cn.
¹⁰ Key Laboratory of Carcinogenesis and Cancer Invasion of the Chinese Ministry of Education, Cancer Research Institute and School of Basic Medical Science, Central South University, Changsha, 410078, China. lixiaoling@csu.edu.cn.

PMID: 32815067
DOI: 10.1007/s11427-019-1735-4

Review

Emerging role of metabolic reprogramming in tumor immune evasion and immunotherapy

Chunmei Fan et al. Sci China Life Sci. 2021 Apr.

. 2021 Apr;64(4):534-547.

doi: 10.1007/s11427-019-1735-4. Epub 2020 Aug 17.

Authors

Affiliations

¹ NHC Key Laboratory of Carcinogenesis, Hunan Cancer Hospital and the Affiliated Cancer Hospital, Xiangya School of Medicine, Central South University, Changsha, 410013, China.
² Key Laboratory of Carcinogenesis and Cancer Invasion of the Chinese Ministry of Education, Cancer Research Institute and School of Basic Medical Science, Central South University, Changsha, 410078, China.
³ Hunan Key Laboratory of Nonresolving Inflammation and Cancer, Disease Genome Research Center, the Third Xiangya Hospital, Central South University, Changsha, 410013, China.
⁴ Department of Stomatology, Xiangya Hospital, Central South University, Changsha, 410078, China.
⁵ Department of Oral and Maxillofacial Surgery, The Second Xiangya Hospital, Central South University, Changsha, 410011, China.
⁶ Department of Medicine, Dan L Duncan Comprehensive Cancer Center, Baylor College of Medicine, Houston, Texas, USA.
⁷ NHC Key Laboratory of Carcinogenesis, Hunan Cancer Hospital and the Affiliated Cancer Hospital, Xiangya School of Medicine, Central South University, Changsha, 410013, China. zengzhaoyang@csu.edu.cn.
⁸ Key Laboratory of Carcinogenesis and Cancer Invasion of the Chinese Ministry of Education, Cancer Research Institute and School of Basic Medical Science, Central South University, Changsha, 410078, China. zengzhaoyang@csu.edu.cn.
⁹ NHC Key Laboratory of Carcinogenesis, Hunan Cancer Hospital and the Affiliated Cancer Hospital, Xiangya School of Medicine, Central South University, Changsha, 410013, China. lixiaoling@csu.edu.cn.
¹⁰ Key Laboratory of Carcinogenesis and Cancer Invasion of the Chinese Ministry of Education, Cancer Research Institute and School of Basic Medical Science, Central South University, Changsha, 410078, China. lixiaoling@csu.edu.cn.

PMID: 32815067
DOI: 10.1007/s11427-019-1735-4

Abstract

Mounting evidence has revealed that the therapeutic efficacy of immunotherapies is restricted to a small portion of cancer patients. A deeper understanding of how metabolic reprogramming in the tumor microenvironment (TME) regulates immunity remains a major challenge to tumor eradication. It has been suggested that metabolic reprogramming in the TME may affect metabolism in immune cells and subsequently suppress immune function. Tumor cells compete with infiltrating immune cells for nutrients and metabolites. Notably, the immunosuppressive TME is characterized by catabolic and anabolic processes that are critical for immune cell function, and elevated inhibitory signals may favor cancer immune evasion. The major energy sources that supply different immune cell subtypes also undergo reprogramming. We herein summarize the metabolic remodeling in tumor cells and different immune cell subtypes and the latest advances underlying the use of metabolic checkpoints in antitumor immunotherapies. In this context, targeting both tumor and immune cell metabolic reprogramming may enhance therapeutic efficacy.

Keywords: antitumor immunotherapy; infiltrating immune cells; metabolic reprogramming; tumor immune evasion; tumor microenvironment.

PubMed Disclaimer

Cited by

The role of microenvironment in tumor angiogenesis.
Jiang X, Wang J, Deng X, Xiong F, Zhang S, Gong Z, Li X, Cao K, Deng H, He Y, Liao Q, Xiang B, Zhou M, Guo C, Zeng Z, Li G, Li X, Xiong W. Jiang X, et al. J Exp Clin Cancer Res. 2020 Sep 30;39(1):204. doi: 10.1186/s13046-020-01709-5. J Exp Clin Cancer Res. 2020. PMID: 32993787 Free PMC article. Review.
Advances in regulation and function of stearoyl-CoA desaturase 1 in cancer, from bench to bed.
Guo Z, Huo X, Li X, Jiang C, Xue L. Guo Z, et al. Sci China Life Sci. 2023 Dec;66(12):2773-2785. doi: 10.1007/s11427-023-2352-9. Epub 2023 Jul 11. Sci China Life Sci. 2023. PMID: 37450239 Review.
Aldehyde dehydrogenase 2-mediated aldehyde metabolism promotes tumor immune evasion by regulating the NOD/VISTA axis.
Chen Y, Sun J, Liu J, Wei Y, Wang X, Fang H, Du H, Huang J, Li Q, Ren G, Wang X, Li H. Chen Y, et al. J Immunother Cancer. 2023 Dec 7;11(12):e007487. doi: 10.1136/jitc-2023-007487. J Immunother Cancer. 2023. PMID: 38088186 Free PMC article.
A new 4-gene-based prognostic model accurately predicts breast cancer prognosis and immunotherapy response by integrating WGCNA and bioinformatics analysis.
Chen W, Kang Y, Sheng W, Huang Q, Cheng J, Pei S, Meng Y. Chen W, et al. Front Immunol. 2024 Feb 2;15:1331841. doi: 10.3389/fimmu.2024.1331841. eCollection 2024. Front Immunol. 2024. PMID: 38370403 Free PMC article.
Identification of metabolism-related long non-coding RNA (lncRNA) signature predicts prognosis and immune infiltrates in hepatocellular carcinoma.
Wang X, Qian J, Yao N, Pocha C, Kang KJ, Angelico R, Zhu G. Wang X, et al. Ann Transl Med. 2022 May;10(10):595. doi: 10.21037/atm-22-2194. Ann Transl Med. 2022. PMID: 35722420 Free PMC article.

See all "Cited by" articles

References

1. Abu-Elheiga, L., Brinkley, W.R., Zhong, L., Chirala, S.S., Woldegiorgis, G., and Wakil, S.J. (2000). The subcellular localization of acetyl-coa carboxylase 2. Proc Natl Acad Sci USA 97, 1444–1449. - PubMed
1. Ahluwalia, G.S., Grem, J.L., Hao, Z., and Cooney, D.A. (1990). Metabolism and action of amino acid analog anti-cancer agents. Pharmacol Ther 46, 243–271. - PubMed
1. Al-Khami, A.A., Rodriguez, P.C., and Ochoa, A.C. (2016). Metabolic reprogramming of myeloid-derived suppressor cells (MDSC) in cancer. Oncoimmunology 5, e1200771. - PubMed - PMC
1. Bahrambeigi, S., and Shafiei-Irannejad, V. (2020). Immune-mediated antitumor effects of metformin; targeting metabolic reprogramming of T cells as a new possible mechanism for anti-cancer effects of metformin. Biochem Pharmacol 174, 113787. - PubMed
1. Bensinger, S.J., Bradley, M.N., Joseph, S.B., Zelcer, N., Janssen, E.M., Hausner, M.A., Shih, R., Parks, J.S., Edwards, P.A., Jamieson, B.D., et al. (2008). LXR signaling couples sterol metabolism to proliferation in the acquired immune response. Cell 134, 97–111. - PubMed - PMC

Publication types

Actions

MeSH terms

Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions

Substances

Actions

LinkOut - more resources

Full Text Sources
- Springer
Medical
- MedlinePlus Health Information

[1] Abu-Elheiga, L., Brinkley, W.R., Zhong, L., Chirala, S.S., Woldegiorgis, G., and Wakil, S.J. (2000). The subcellular localization of acetyl-coa carboxylase 2. Proc Natl Acad Sci USA 97, 1444–1449. - PubMed

[2] Abu-Elheiga, L., Brinkley, W.R., Zhong, L., Chirala, S.S., Woldegiorgis, G., and Wakil, S.J. (2000). The subcellular localization of acetyl-coa carboxylase 2. Proc Natl Acad Sci USA 97, 1444–1449. - PubMed

[3] Ahluwalia, G.S., Grem, J.L., Hao, Z., and Cooney, D.A. (1990). Metabolism and action of amino acid analog anti-cancer agents. Pharmacol Ther 46, 243–271. - PubMed

[4] Ahluwalia, G.S., Grem, J.L., Hao, Z., and Cooney, D.A. (1990). Metabolism and action of amino acid analog anti-cancer agents. Pharmacol Ther 46, 243–271. - PubMed

[5] Al-Khami, A.A., Rodriguez, P.C., and Ochoa, A.C. (2016). Metabolic reprogramming of myeloid-derived suppressor cells (MDSC) in cancer. Oncoimmunology 5, e1200771. - PubMed - PMC

[6] Al-Khami, A.A., Rodriguez, P.C., and Ochoa, A.C. (2016). Metabolic reprogramming of myeloid-derived suppressor cells (MDSC) in cancer. Oncoimmunology 5, e1200771. - PubMed - PMC

[7] Bahrambeigi, S., and Shafiei-Irannejad, V. (2020). Immune-mediated antitumor effects of metformin; targeting metabolic reprogramming of T cells as a new possible mechanism for anti-cancer effects of metformin. Biochem Pharmacol 174, 113787. - PubMed

[8] Bahrambeigi, S., and Shafiei-Irannejad, V. (2020). Immune-mediated antitumor effects of metformin; targeting metabolic reprogramming of T cells as a new possible mechanism for anti-cancer effects of metformin. Biochem Pharmacol 174, 113787. - PubMed

[9] Bensinger, S.J., Bradley, M.N., Joseph, S.B., Zelcer, N., Janssen, E.M., Hausner, M.A., Shih, R., Parks, J.S., Edwards, P.A., Jamieson, B.D., et al. (2008). LXR signaling couples sterol metabolism to proliferation in the acquired immune response. Cell 134, 97–111. - PubMed - PMC

[10] Bensinger, S.J., Bradley, M.N., Joseph, S.B., Zelcer, N., Janssen, E.M., Hausner, M.A., Shih, R., Parks, J.S., Edwards, P.A., Jamieson, B.D., et al. (2008). LXR signaling couples sterol metabolism to proliferation in the acquired immune response. Cell 134, 97–111. - PubMed - PMC

Save citation to file

Email citation

Add to Collections

Add to My Bibliography

Your saved search

Create a file for external citation management software

Your RSS Feed

Emerging role of metabolic reprogramming in tumor immune evasion and immunotherapy

Affiliations

Emerging role of metabolic reprogramming in tumor immune evasion and immunotherapy

Authors

Affiliations

Abstract

Similar articles

Cited by

References

Publication types

MeSH terms

Substances

LinkOut - more resources

Full Text Sources

Medical