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The impact of the gut microbiome on tumor immunotherapy: from mechanism to application strategies

Guo, Ciliang, Kong, Lingkai, Xiao, Lingjun, Liu, Kua, Cui, Huawei, Xin, Qilei, Gu, Xiaosong, Jiang, Chunping, Wu, Junhua·2023·Cell & Bioscience
DOI 10.1186/s13578-023-01135-yPMC PMC10571290
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Abstract

Immunotherapy is one of the fastest developing areas in the field of oncology. Many immunological treatment strategies for refractory tumors have been approved and marketed. Nevertheless, much clinical and preclinical experimental evidence has shown that the efficacy of immunotherapy in tumor treatment varies markedly among individuals. The commensal microbiome mainly colonizes the intestinal lumen in humans, is affected by a variety of factors and exhibits individual variation. Moreover, the gut is considered the largest immune organ of the body due to its influence on the immune system. In the last few decades, with the development of next-generation sequencing (NGS) techniques and in-depth research, the view that the gut microbiota intervenes in antitumor immunotherapy through the immune system has been gradually confirmed. Here, we review important studies published in recent years focusing on the influences of microbiota on immune system and the progression of malignancy. Furthermore, we discuss the mechanism by which microbiota affect tumor immunotherapy, including immune checkpoint blockade (ICB) and adoptive T-cell therapy (ACT), and strategies for modulating the microbial composition to facilitate the antitumor immune response. Finally, opportunity and some challenges are mentioned to enable a more systematic understanding of tumor treatment in the future and promote basic research and clinical application in related fields.

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Fig. 1 The gut microbiome interacts with the immune system locally in the gut and peripherally in the tumor microenvironment (TME). Within the gut, the gut microbiota plays an essential role in maintaining the mucosal barrier to protect the gut from pathogens. Microbes can interact with DCs directly and induce their maturation. Some microbiota-derived metabolites, such as SCFAs, inosine, and peptidoglycan, or invasive microbes can activate macrophages (Møs), T cells and B cells in the lamina propria or Peyer’s patches. Systemically, gut microbiota-derived metabolites can disseminate to distal sites, especially the TME, through the portal vein and interact with tumor-associated lymphocytes, including DCs, NK cells, Møs and T cells. CTL cytotoxic T lymphocyte
Fig. 1 The gut microbiome interacts with the immune system locally in the gut and peripherally in the tumor microenvironment (TME). Within the gut, the gut microbiota plays an essential role in maintaining the mucosal barrier to protect the gut from pathogens. Microbes can interact with DCs directly and induce their maturation. Some microbiota-derived metabolites, such as SCFAs, inosine, and peptidoglycan, or invasive microbes can activate macrophages (Møs), T cells and B cells in the lamina propria or Peyer’s patches. Systemically, gut microbiota-derived metabolites can disseminate to distal sites, especially the TME, through the portal vein and interact with tumor-associated lymphocytes, including DCs, NK cells, Møs and T cells. CTL cytotoxic T lymphocyteCC BY · PubMed Central
Fig. 2 Mechanism through which some gut microbiota-derived metabolites influence antitumor therapy. These metabolites, including TMAO from Clostridiales, c-di-AMP from Akkermansia, inosine from Bifidobacterium pseudolongum, peptidoglycan from Bifidobacterium bifidum, β-galactosidase from Streptococcus thermophilus and butyrate, are representative metabolites that have been reported in the last two years. They can spread to the TME through the circulatory system or interact with mutated enterocytes directly and mediate antitumor therapy by different mechanisms and pathways. TLRs Toll-like receptors, AhR aryl hydrocarbon receptor, A2AR: adenosine 2A receptor
Fig. 2 Mechanism through which some gut microbiota-derived metabolites influence antitumor therapy. These metabolites, including TMAO from Clostridiales, c-di-AMP from Akkermansia, inosine from Bifidobacterium pseudolongum, peptidoglycan from Bifidobacterium bifidum, β-galactosidase from Streptococcus thermophilus and butyrate, are representative metabolites that have been reported in the last two years. They can spread to the TME through the circulatory system or interact with mutated enterocytes directly and mediate antitumor therapy by different mechanisms and pathways. TLRs Toll-like receptors, AhR aryl hydrocarbon receptor, A2AR: adenosine 2A receptorCC BY · PubMed Central

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Metadata

Authors
Guo, C., Kong, L., Xiao, L., Liu, K., Cui, H., Xin, Q., Gu, X., Jiang, C., & Wu, J.
Venue
Cell & Bioscience
Publisher
Springer Science and Business Media LLC
Published
2023-10-13
Volume
13
Issue
1
ISSN
2045-3701
DOI
10.1186/s13578-023-01135-y
PMC
PMC10571290
Cited by
48
References
77
Language
en
Licence
Funders
  • National Natural Science Foundation of China (82272819, 81972888)
  • the Research Project of Jinan Microecological Biomedicine Shandong Laboratory (JNL202204A, JNL202219B, JNL-2023017D)
  • the Primary Research & Development Plan of Jiangsu Province (BE2022840)
  • Shandong Provincial Laboratory Project (SYS202202)
  • the Open Project of Chinese Materia Medica First-Class Discipline of Nanjing University of Chinese Medicine (2020YLXK007)

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