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Gut Microbiota Alteration Influences Colorectal Cancer Metastasis to the Liver by Remodeling the Liver Immune Microenvironment

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Background/Aims:This study aimed to explore the effect of gut microbiota-regulated Kupffer cells (KCs) on colorectal cancer (CRC) liver metastasis. Methods: A series of in vivo and in vitro researches were showed to demonstrate the gut microbiota and its possible mechanism in CRC liver metastasis. Results: Fewer liver metastases were identified in the ampicillin-streptomycin-colistin and colistin groups. Increased proportions of Parabacteroides goldsteinii, Bacteroides vulgatus, Bacteroides thetaiotaomicron, and Bacteroides uniformis were observed in the colistin group. The significant expansion of KCs was identified in the ampicillin-streptomycin-colistin and colistin groups. B. vulgatus levels were positively correlated with KC levels. More liver metastases were observed in the vancomycin group. An increased abundance of Parabacteroides distasonis and Proteus mirabilis and an obvious reduction of KCs were noted in the vancomycin group. P. mirabilis levels were negatively related to KC levels. The number of liver metastatic nodules was increased in the P. mirabilis group and decreased in the B. vulgatus group. The number of KCs decreased in the P. mirabilis group and increased in the B. vulgatus group. In vitro, as P. mirabilis or B. vulgatus doses increased, there was an opposite effect on KC proliferation in dose- and time-dependent manners. P. mirabilis induced CT26 cell migration by controlling KC proliferation, whereas B. vulgatus prevented this migration. Conclusions: An increased abundance of P. mirabilis and decreased amount of B. vulgatus play key roles in CRC liver metastasis, which might be related to KC reductions in the liver.

Abstract

Background/Aims:This study aimed to explore the effect of gut microbiota-regulated Kupffer cells (KCs) on colorectal cancer (CRC) liver metastasis. Methods: A series of in vivo and in vitro researches were showed to demonstrate the gut microbiota and its possible mechanism in CRC liver metastasis. Results: Fewer liver metastases were identified in the ampicillin-streptomycin-colistin and colistin groups. Increased proportions of Parabacteroides goldsteinii, Bacteroides vulgatus, Bacteroides thetaiotaomicron, and Bacteroides uniformis were observed in the colistin group. The significant expansion of KCs was identified in the ampicillin-streptomycin-colistin and colistin groups. B. vulgatus levels were positively correlated with KC levels. More liver metastases were observed in the vancomycin group. An increased abundance of Parabacteroides distasonis and Proteus mirabilis and an obvious reduction of KCs were noted in the vancomycin group. P. mirabilis levels were negatively related to KC levels. The number of liver metastatic nodules was increased in the P. mirabilis group and decreased in the B. vulgatus group. The number of KCs decreased in the P. mirabilis group and increased in the B. vulgatus group. In vitro, as P. mirabilis or B. vulgatus doses increased, there was an opposite effect on KC proliferation in dose- and time-dependent manners. P. mirabilis induced CT26 cell migration by controlling KC proliferation, whereas B. vulgatus prevented this migration. Conclusions: An increased abundance of P. mirabilis and decreased amount of B. vulgatus play key roles in CRC liver metastasis, which might be related to KC reductions in the liver.

참고문헌 (46)

  1. Kashyap D, "Molecular targets of celastrol in cancer : recent trends and advancements", Crit Rev Oncol Hematol, 128, pp.70~81 (2018)
  2. Lim CJ, "Multidimensional analyses reveal distinct immune microenvironment in hepatitis B virusrelated hepatocellular carcinoma", Gut, 68, pp.916~927 (2019)
  3. Imai K, "Early recurrence after hepatectomy for colorectal liver metastases : what optimal definition and what predictive factors?", Oncologist, 21, pp.887~894 (2016)
  4. Jia B, "Commentary : gut microbiome-mediated bile acid metabolism regulates liver cancer via NKT cells", Front Immunol, 10, pp.282~ (2019)
  5. Golonka RM, "Atypical immunometabolism and metabolic reprogramming in liver cancer : deciphering the role of gut microbiome", Adv Cancer Res, 149, pp.171~255 (2021)
  6. 김상훈, "The role of microbiome in colorectal carcinogenesis and its clinical potential as a target for cancer treatment", Intestinal research, 20(1), pp.31~42 (2022), 대한장연구학회[DOI]
  7. Li Y, "Apple polysaccharide protects ICR mice against colitis associated colorectal cancer through the regulation of microbial dysbiosis", Carbohydr Polym, 230, pp.115726~ (2020)
  8. Clarke TB, "Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity", Nat Med, 16, pp.228~231 (2010)
  9. Ma C, "Gut microbiome-mediated bile acid metabolism regulates liver cancer via NKT cells", Science, 360, pp.eaan5931~ (2018)
  10. Huang H, "Innate immune cells in immune tolerance after liver transplantation", Front Immunol, 9, pp.2401~ (2018)
  11. Kuniyasu Y, "Kupffer cells required for high affinity peptide-induced deletion, not retention, of activated CD8+ T cells by mouse liver", Hepatology, 39, pp.1017~1027 (2004)
  12. Tu Z, "TLR-dependent cross talk between human Kupffer cells and NK cells", J Exp Med, 205, pp.233~244 (2008)
  13. Chen Y, "Role of Kupffer cells in the induction of tolerance of orthotopic liver transplantation in rats", Liver Transpl, 14, pp.823~836 (2008)
  14. Gong J, "Role of programmed death ligand 1 and Kupffer cell in immune regulation after orthotopic liver transplantation in rats", Int Immunopharmacol, 48, pp.8~16 (2017)
  15. Lee WY, "An intravascular immune response to Borrelia burgdorferi involves Kupffer cells and iNKT cells", Nat Immunol, 11, pp.295~302 (2010)
  16. Okubo H, "Involvement of resistin-like molecule β in the development of methioninecholine deficient diet-induced non-alcoholic steatohepatitis in mice", Sci Rep, 6, pp.20157~ (2016)
  17. Ishida K, "Sulforaphane ameliorates ethanol plus carbon tetrachloride-induced liver fibrosis in mice through the Nrf2-mediated antioxidant response and acetaldehyde metabolization with inhibition of the LPS", TLR4signaling pathway, 2021, pp.89, 108573~
  18. Lai C, "Effect of Kupffer cells depletion on ABC phenomenon induced by Kupffer cells-targeted liposomes", Asian J Pharm Sci, 14, pp.455~464 (2019)
  19. Lee JG, "Role of the global gut microbial community in the development of colitis-associated cancer in a murine model", Biomed Pharmacother, 135, pp.111206~ (2021)
  20. Eggert T, "Distinct functions of senescence-associated immune responses in liver tumor surveillance and tumor progression", Cancer Cell, 30, pp.533~547 (2016)
  21. Wong SH, "Gavage of fecal samples from patients with colorectal cancer promotes intestinal carcinogenesis in germ-free and conventional mice", Gastroenterology, 153, pp.1621~1633 (2017)
  22. Qi X, "Gut microbiota-bile acid-interleukin-22 axis orchestrates polycystic ovary syndrome", Nat Med, 25, pp.1225~1233 (2019)
  23. Xu X, "Gut microbiome influences the efficacy of PD-1 antibody immunotherapy on MSS-type colorectal cancer via metabolic pathway", Front Microbiol, 11, pp.814~ (2020)
  24. Sethi V, "Gut microbiota promotes tumor growth in mice by modulating immune response", Gastroenterology, 155, pp.33~37 (2018)
  25. Gardiner KR, "Lactulose as an antiendotoxin in experimental colitis", Br J Surg, 82, pp.469~472 (1995)
  26. Percivalle E, "Colistin inhibits E. coli O157 : H7 Shiga-like toxin release, binds endotoxins and protects Vero cells", New Microbiol, 39, pp.119~123 (2016)
  27. Li R, "Gut microbiota-stimulated cathepsin K secretion mediates TLR4-dependent M2 macrophage polarization and promotes tumor metastasis in colorectal cancer", Cell Death Differ, 26, pp.2447~2463 (2019)
  28. Uronis JM, "Modulation of the intestinal microbiota alters colitis-associated colorectal cancer susceptibility", PLoS One, 4, pp.e6026~ (2009)
  29. Di Lorenzo F, "Pairing Bacteroides vulgatus LPS structure with its immunomodulatory effects on human cellular models", ACS Cent Sci, 6, pp.1602~1616 (2020)
  30. Vétizou M, "Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota", Science, 350, pp.1079~1084 (2015)
  31. Ma HY, "IL-17 signaling in steatotic hepatocytes and macrophages promotes hepatocellular carcinoma in alcohol-related liver disease", J Hepatol, 72, pp.946~959 (2020)
  32. Keirsse J, "The role of hepatic macrophages in liver metastasis", Cell Immunol, 330, pp.202~215 (2018)
  33. Li Q, "Intestinal dysbacteriosis-induced IL-25 promotes development of HCC via alternative activation of macrophages in tumor microenvironment", J Exp Clin Cancer Res, 38, pp.303~ (2019)
  34. Wang J, "Immunomodulatory effects of colistin on macrophages in rats by activating the p38", MAPK pathway, 2019, pp.10, 729~
  35. Hastir JF, "Hepatocarcinoma induces a tumor necrosis factor-dependent Kupffer cell death pathway that favors its proliferation upon partial hepatectomy", Front Oncol, 10, pp.547013~ (2020)
  36. Albassam MA, "Electron microscopic studies on the interaction between normal mice peritoneal phagocytes and Treponema hyodysenteriae, Treponema innocens and Bacteroides vulgatus", Can J Vet Res, 50, pp.88~95 (1986)
  37. Zhang H, "Proteus mirabilis inhibits cancer growth and pulmonary metastasis in a mouse breast cancer model", PLoS One, 12, pp.e0188960~ (2017)
  38. Heap JT, "Spores of Clostridium engineered for clinical efficacy and safety cause regression and cure of tumors in vivo", Oncotarget, 5, pp.1761~1769 (2014)
  39. Seo SU, "Distinct commensals induce interleukin-1β via NLRP3 inflammasome in inflammatory monocytes to promote intestinal inflammation in response to injury", Immunity, 42, pp.744~755 (2015)
  40. Weber G, "Modulation of effects of lipopolysaccharide on macrophages by a major outer membrane protein of Proteus mirabilis as measured in a chemiluminescence assay", Infect Immun, 60, pp.1069~1075 (1992)
  41. Lemoinne S, "Gut microbiota in PSC : from association to possible causality. Commentary to"Gut pathobionts underlie intestinal barrier dysfunction and liver T helper 17 cell immune response in primary sclerosing cholangitis"by Nakamoto et al., Nature Microbiology, January 2019", Clin Res Hepatol Gastroenterol, 44, pp.123~125 (2020)
  42. Chung IC, "Pretreatment with a heat-killed probiotic modulates the NLRP3 inflammasome and attenuates colitis-associated colorectal cancer in mice", Nutrients, 11, pp.516~ (2019)
  43. Wu Y, "Spatiotemporal immune landscape of colorectal cancer liver metastasis at single-cell level", Cancer Discov, 12, pp.134~153 (2022)
  44. Steimle A, "Weak agonistic LPS restores intestinal immune homeostasis", Mol Ther, 27, pp.1974~1991 (2019)
  45. Frick JS, "Colitogenic and noncolitogenic commensal bacteria differentially trigger DC maturation and Th cell polarization : an important role for IL-6", Eur J Immunol, 36, pp.1537~1547 (2006)
  46. Ó Cuív P, "The gut bacterium and pathobiont Bacteroides vulgatus activates NF-κB in a human gut epithelial cell line in a strain and growth phase dependent manner", Anaerobe, 47, pp.209~217 (2017)

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