3,867
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

Gut microbiome-derived butyrate inhibits the immunosuppressive factors PD-L1 and IL-10 in tumor-associated macrophages in gastric cancer

, , , , , , , , , , & ORCID Icon show all
Article: 2300846 | Received 27 Mar 2023, Accepted 27 Dec 2023, Published online: 10 Jan 2024

References

  • Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71:209–13. doi:10.3322/caac.21660.
  • Li Y, Feng A, Zheng S, Chen C, Lyu J. Recent estimates and predictions of 5-year survival in patients with gastric cancer: a model-based period analysis. Cancer Control. 2022;29:10732748221099227. doi:10.1177/10732748221099227.
  • Yaprak G, Tataroglu D, Dogan B, Pekyurek M. Prognostic factors for survival in patients with gastric cancer: single-centre experience. North Clin Istanb. 2020;7:146–152. doi:10.14744/nci.2019.73549.
  • Wang BC, Zhang ZJ, Fu C, Wang C. Efficacy and safety of anti-PD-1/PD-L1 agents vs chemotherapy in patients with gastric or gastroesophageal junction cancer: a systematic review and meta-analysis. Med. 2019;98(47):e18054. doi:10.1097/MD.0000000000018054.
  • Gu L, Huang T, Qiu S, Hong J, Fu R, Ni C, Dai S, Chen P, He N. Efficacy of PD-1/PD-L1 inhibitors in patients with advanced gastroesophageal cancer: an updated meta-analysis based on randomized controlled trials. Front Pharmacol. 2022;13:1009254. doi:10.3389/fphar.2022.1009254.
  • Lin Y, Xu J, Lan H. Tumor-associated macrophages in tumor metastasis: biological roles and clinical therapeutic applications. J Hematol Oncol. 2019;12(1):76. doi:10.1186/s13045-019-0760-3.
  • Sumitomo R, Hirai T, Fujita M, Murakami H, Otake Y, Huang CL. PD-L1 expression on tumor-infiltrating immune cells is highly associated with M2 TAM and aggressive malignant potential in patients with resected non-small cell lung cancer. Lung Cancer. 2019;136:136–44. doi:10.1016/j.lungcan.2019.08.023.
  • Li Y, Huang X, Tong D, Jiang C, Zhu X, Wei Z, Gong T, Jin C. Relationships among microbiota, gastric cancer, and immunotherapy. Front Microbiol. 2022;13:987763. doi:10.3389/fmicb.2022.987763.
  • Majewski M, Mertowska P, Mertowski S, Smolak K, Grywalska E, Torres K. Microbiota and the immune system—actors in the gastric cancer story. Cancers Basel. 2022;14(15):14. doi:10.3390/cancers14153832.
  • Jain T, Sharma P, Are AC, Vickers SM, Dudeja V. New insights into the cancer-microbiome-immune axis: decrypting a decade of discoveries. Front Immunol. 2021;12:622064. doi:10.3389/fimmu.2021.622064.
  • Liu S, Dai J, Lan X, Fan B, Dong T, Zhang Y, Han M. Intestinal bacteria are potential biomarkers and therapeutic targets for gastric cancer. Microb Pathog. 2021;151:104747. doi:10.1016/j.micpath.2021.104747.
  • Gopalakrishnan V, Spencer CN, Nezi L, Reuben A, Andrews MC, Karpinets TV, Prieto PA, Vicente D, Hoffman K, Wei SC, et al. Gut microbiome modulates response to anti–PD-1 immunotherapy in melanoma patients. Sci. 2018;359(6371):97–103. doi:10.1126/science.aan4236.
  • Krautkramer KA, Fan J, Backhed F. Gut microbial metabolites as multi-kingdom intermediates. Nat Rev Microbiol. 2021;19(2):77–94. doi:10.1038/s41579-020-0438-4.
  • Correa-Oliveira R, Fachi JL, Vieira A, Sato FT, Vinolo MA. Regulation of immune cell function by short-chain fatty acids. Clin Trans Immunol. 2016;5(4):e73. doi:10.1038/cti.2016.17.
  • Davie JR. Inhibition of histone deacetylase activity by butyrate. J Nutr. 2003;133(7):2485S–93S. doi:10.1093/jn/133.7.2485S.
  • Rada-Iglesias A, Enroth S, Ameur A, Koch CM, Clelland GK, Respuela-Alonso P, Wilcox S, Dovey OM, Ellis PD, Langford CF, et al. Butyrate mediates decrease of histone acetylation centered on transcription start sites and down-regulation of associated genes. Genome Res. 2007;17(6):708–19. doi:10.1101/gr.5540007.
  • Kang X, Li C, Liu S, Baldwin R, Liu GE, Li CJ. Genome-wide acetylation modification of H3K27ac in Bovine Rumen cell following butyrate exposure. Biomolecules. 2023;13(7):1137. doi:10.3390/biom13071137.
  • Jan G, Belzacq AS, Haouzi D, Rouault A, Metivier D, Kroemer G, Brenner C. Propionibacteria induce apoptosis of colorectal carcinoma cells via short-chain fatty acids acting on mitochondria. Cell Death Differ. 2002;9(2):179–188. doi:10.1038/sj.cdd.4400935.
  • Schug ZT, Peck B, Jones DT, Zhang Q, Grosskurth S, Alam IS, Goodwin L, Smethurst E, Mason S, Blyth K, et al. Acetyl-CoA synthetase 2 promotes acetate utilization and maintains cancer cell growth under metabolic stress. Cancer Cell. 2015;27(1):57–71. doi:10.1016/j.ccell.2014.12.002.
  • Wu X, Wu Y, He L, Wu L, Wang X, Liu Z. Effects of the intestinal microbial metabolite butyrate on the development of colorectal cancer. J Cancer. 2018;9(14):2510–7. doi:10.7150/jca.25324.
  • Kim K, Kwon O, Ryu TY, Jung CR, Kim J, Min JK, Kim D, Son M, Cho H. Propionate of a microbiota metabolite induces cell apoptosis and cell cycle arrest in lung cancer. Mol Med Rep. 2019;20:1569–1574. doi:10.3892/mmr.2019.10431.
  • Park HS, Han JH, Park JW, Lee DH, Jang KW, Lee M, Heo K-S, Myung C-S. Sodium propionate exerts anticancer effect in mice bearing breast cancer cell xenograft by regulating JAK2/STAT3/ROS/p38 MAPK signaling. Acta Pharmacol Sin. 2021;42(8):1311–1323. doi:10.1038/s41401-020-00522-2.
  • Geng HW, Yin FY, Zhang ZF, Gong X, Yang Y. Butyrate suppresses glucose metabolism of colorectal cancer cells via GPR109a-AKT signaling pathway and enhances chemotherapy. Front Mol Biosci. 2021;8:634874. doi:10.3389/fmolb.2021.634874.
  • Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37(8):852–7. doi:10.1038/s41587-019-0209-9.
  • Jeong Y, Kim JW, You HJ, Park SJ, Lee J, Ju JH, Park MS, Jin H, Cho M-L, Kwon B, et al. Gut microbial composition and function are altered in patients with early rheumatoid arthritis. J Clin Med. 2019;8(5):693. doi:10.3390/jcm8050693.
  • Liu J, Wu S, Zheng X, Zheng P, Fu Y, Wu C, Lu B, Ju J, Jiang J. Immune suppressed tumor microenvironment by exosomes derived from gastric cancer cells via modulating immune functions. Sci Rep. 2020;10(1):14749. doi:10.1038/s41598-020-71573-y.
  • Wang JB, Li P, Liu XL, Zheng QL, Ma YB, Zhao YJ, Xie J-W, Lin J-X, Lu J, Chen Q-Y, et al. An immune checkpoint score system for prognostic evaluation and adjuvant chemotherapy selection in gastric cancer. Nat Commun. 2020;11(1):6352. doi:10.1038/s41467-020-20260-7.
  • Eto S, Yoshikawa K, Nishi M, Higashijima J, Tokunaga T, Nakao T, Kashihara H, Takasu C, Iwata T, Shimada M, et al. Programmed cell death protein 1 expression is an independent prognostic factor in gastric cancer after curative resection. Gastric Cancer. 2016;19(2):466–71. doi:10.1007/s10120-015-0519-7.
  • Kim ST, Cristescu R, Bass AJ, Kim KM, Odegaard JI, Kim K, Liu XQ, Sher X, Jung H, Lee M, et al. Comprehensive molecular characterization of clinical responses to PD-1 inhibition in metastatic gastric cancer. Nat Med. 2018;24(9):1449–58. doi:10.1038/s41591-018-0101-z.
  • Suh KJ, Kim JW, Kim JE, Sung JH, Koh J, Kim KJ, Kim J-W, Ahn S-H, Park DJ, Kim H-H, et al. Correlation between tumor infiltrating immune cells and peripheral regulatory T cell determined using methylation analyses and its prognostic significance in resected gastric cancer. PLoS ONE. 2021;16(6):e0252480. doi:10.1371/journal.pone.0252480.
  • Kodukula K, Faller DV, Harpp DN, Kanara I, Pernokas J, Pernokas M, Powers WR, Soukos NS, Steliou K, Moos WH, et al. Gut microbiota and salivary diagnostics: the mouth is salivating to tell us something. Biores Open Access. 2017;6(1):123–32. doi:10.1089/biores.2017.0020.
  • Martinez JE, Kahana DD, Ghuman S, Wilson HP, Wilson J, Kim SCJ, Lagishetty V, Jacobs JP, Sinha-Hikim AP, Friedman TC, et al. Unhealthy lifestyle and Gut Dysbiosis: a better understanding of the effects of poor diet and nicotine on the intestinal microbiome. Front Endocrinol (Lausanne). 2021;12:667066. doi:10.3389/fendo.2021.667066.
  • Fan Y, Pedersen O. Gut microbiota in human metabolic health and disease. Nat Rev Microbiol. 2021;19(1):55–71. doi:10.1038/s41579-020-0433-9.
  • Durack J, Lynch SV. The gut microbiome: relationships with disease and opportunities for therapy. J Exp Med. 2019;216(1):20–40. doi:10.1084/jem.20180448.
  • Castano-Rodriguez N, Goh KL, Fock KM, Mitchell HM, Kaakoush NO. Dysbiosis of the microbiome in gastric carcinogenesis. Sci Rep. 2017;7(1):15957. doi:10.1038/s41598-017-16289-2.
  • Park JY, Seo H, Kang CS, Shin TS, Kim JW, Park JM, Kim JG, Kim Y-K. Dysbiotic change in gastric microbiome and its functional implication in gastric carcinogenesis. Sci Rep. 2022;12(1):4285. doi:10.1038/s41598-022-08288-9.
  • Yang J, Zhou X, Liu X, Ling Z, Ji F. Role of the gastric microbiome in gastric cancer: from carcinogenesis to treatment. Front Microbiol. 2021;12:641322. doi:10.3389/fmicb.2021.641322.
  • Coker OO, Dai Z, Nie Y, Zhao G, Cao L, Nakatsu G, Wu WK, Wong SH, Chen Z, Sung JJY, et al. Mucosal microbiome dysbiosis in gastric carcinogenesis. Gut. 2018;67(6):1024–32. doi:10.1136/gutjnl-2017-314281.
  • Gunathilake M, Lee J, Choi IJ, Kim YI, Yoon J, Sul WJ, Kim JF, Kim J. Alterations in gastric microbial communities are associated with risk of gastric cancer in a Korean population: a case-control study. Cancers Basel. 2020;12(9):2619. doi:10.3390/cancers12092619.
  • Sarhadi V, Mathew B, Kokkola A, Karla T, Tikkanen M, Rautelin H, Lahti L, Puolakkainen P, Knuutila S. Gut microbiota of patients with different subtypes of gastric cancer and gastrointestinal stromal tumors. Gut Pathog. 2021;13(1):11. doi:10.1186/s13099-021-00403-x.
  • Dikeocha IJ, Al-Kabsi AM, Chiu HT, Alshawsh MA. Faecalibacterium prausnitzii Ameliorates Colorectal Tumorigenesis and Suppresses Proliferation of HCT116 Colorectal Cancer Cells. Biomedicines. 2022;10(5). doi: 10.3390/biomedicines10051128.
  • Kim S, Lee HH, Choi W, Kang CH, Kim GH, Cho H. Anti-Tumor Effect of Heat-Killed Bifidobacterium bifidum on Human Gastric Cancer through Akt-p53-Dependent Mitochondrial Apoptosis in Xenograft Models. Int J Mol Sci. 2022;23(17). doi: 10.3390/ijms23179788.
  • Encarnacao JC, Pires AS, Amaral RA, Goncalves TJ, Laranjo M, Casalta-Lopes JE, Gonçalves AC, Sarmento-Ribeiro AB, Abrantes AM, Botelho MF, et al. Butyrate, a dietary fiber derivative that improves irinotecan effect in colon cancer cells. J Nutr Biochem. 2018;56:183–92. doi:10.1016/j.jnutbio.2018.02.018.
  • Park M, Kwon J, Shin HJ, Moon SM, Kim SB, Shin U, Han Y, Kim Y. Butyrate enhances the efficacy of radiotherapy via FOXO3A in colorectal cancer patient‑derived organoids. Int J Oncol. 2020;57(6):1307–1318. doi:10.3892/ijo.2020.5132.
  • Liang Y, Rao Z, Du D, Wang Y, Fang T. Butyrate prevents the migration and invasion, and aerobic glycolysis in gastric cancer via inhibiting Wnt/β-catenin/c-myc signaling. Drug Dev Res. 2023;84(3):532–541. doi:10.1002/ddr.22043.
  • Faden H. The role of Faecalibacterium, Roseburia, and butyrate in inflammatory bowel disease. Dig Dis. 2022;40:793–5. doi:10.1159/000522247.
  • Qin P, Zou Y, Dai Y, Luo G, Zhang X, Xiao L. Characterization a Novel Butyric Acid-Producing Bacterium Collinsella aerofaciens subsp. Shenzhenensis subsp. Nov. Shenzhenensis Subsp Nov Microorganisms. 2019;7(3):78. doi:10.3390/microorganisms7030078.
  • Zerdes I, Wallerius M, Sifakis EG, Wallmann T, Betts S, Bartish M, Tsesmetzis N, Tobin N, Coucoravas C, Bergh J, et al. STAT3 activity promotes programmed-death Ligand 1 expression and suppresses immune responses in breast cancer. Cancers Basel. 2019;11(10). doi:10.3390/cancers11101479.
  • Antonangeli F, Natalini A, Garassino MC, Sica A, Santoni A, Di Rosa F. Regulation of PD-L1 Expression by NF-kappaB in cancer. Front Immunol. 2020;11:584626. doi:10.3389/fimmu.2020.584626.
  • Patel SA, Nilsson MB, Le X, Cascone T, Jain RK, Heymach JV. Molecular mechanisms and future implications of VEGF/VEGFR in cancer therapy. Clin Cancer Res. 2023;29(1):30–9. doi:10.1158/1078-0432.CCR-22-1366.
  • Joo M, Kim D, Lee MW, Lee HJ, Kim JM. GDF15 promotes cell growth, migration, and invasion in gastric cancer by inducing STAT3 activation. Int J Mol Sci. 2023;24(3). doi: 10.3390/ijms24032925.
  • Kommineni VK, Nagineni CN, William A, Detrick B, Hooks JJ. IFN-γ acts as anti-angiogenic cytokine in the human cornea by regulating the expression of VEGF-A and sVEGF-R1. Biochem Biophys Res Commun. 2008;374(3):479–484. doi:10.1016/j.bbrc.2008.07.042.
  • Park MJ, Park Y, Choi JW, Baek JA, Jeong HY, Na HS, Moon Y-M, Cho M-L, Park S-H. Establishment of a humanized animal model of systemic sclerosis in which T helper-17 cells from patients with systemic sclerosis infiltrate and cause fibrosis in the lungs and skin. Experimental & Molecular Medicine. 2022;54(9):1577–1585. doi:10.1038/s12276-022-00860-7.
  • Lee SK, Park MJ, Choi JW, Baek JA, Kim SY, Choi HJ, You YK, Jang JW, Sung PS, Bae SH, et al. Patient-derived avatar mouse model to predict the liver immune homeostasis of long-term stable liver transplant patients. Front Immunol. 2022;13:817006. doi:10.3389/fimmu.2022.817006.