Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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The Inhibitory Effect of Gut Microbiota and Its Metabolites on Colorectal Cancer

  • Chen, Chao (Department of Colorectal Surgery, the Second Affiliated Hospital, Zhejiang University School of Medicine) ;
  • Li, Huajun (Department of Microecology, College of Basic Medical Sciences, Dalian Medical University)
  • Received : 2020.02.17
  • Accepted : 2020.05.31
  • Published : 2020.11.28
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Abstract

Colorectal cancer (CRC) is regarded as one of the most common and deadly forms of cancer. Gut microbiota is vital to retain and promote several functions of intestinal. Although previous researches have shown that some gut microbiota have the abilities to inhibit tumorigenesis and prevent cancer from progressing, they have not yet clearly identified associative mechanisms. This review not only concentrates on the antitumor effects of metabolites produced by gut microbiota, for example, SCFA, ferrichrome, urolithins, equol and conjugated linoleic acids, but also the molecules which constituted the bacterial cell wall have the antitumor effect in the host, including lipopolysaccharide, lipoteichoic acid, β-glucans and peptidoglycan. The aim of our review is to develop a possible therapeutic method, which use the products of gut microbiota metabolism or gut microbiota constituents to help treat or prevent colorectal cancer.

Keywords

References

  1. Siegel RL, Miller KD,Jemal A. 2020. Cancer statistics, 2020. CA Cancer J. Clin. 70: 7-30. https://doi.org/10.3322/caac.21590
  2. Lee C, Ho JW, Fong DY, Macfarlane DJ, Cerin E, Lee AM, et al. 2018. Dietary and physical activity interventions for colorectal cancer survivors: a randomized controlled trial. Sci. Rep. 8: 1-9. https://doi.org/10.1038/s41598-017-17765-5
  3. Staley C, Weingarden AR, Khoruts A,Sadowsky MJ. 2017. Interaction of gut microbiota with bile acid metabolism and its influence on disease states. Appl. Microbiol. Biotechnol. 101: 47-64. https://doi.org/10.1007/s00253-016-8006-6
  4. Yu J, Feng Q, Wong SH, Zhang D, yi Liang Q, Qin Y, et al. 2017. Metagenomic analysis of faecal microbiome as a tool towards targeted non-invasive biomarkers for colorectal cancer. Gut 66: 70-78. https://doi.org/10.1136/gutjnl-2015-309800
  5. Zhang Y-J, Li S, Gan R-Y, Zhou T, Xu D-P,Li H-B. 2015. Impacts of gut bacteria on human health and diseases. Int. J. Mol. Sci. 16: 7493-7519. https://doi.org/10.3390/ijms16047493
  6. Knight R, Callewaert C, Marotz C, Hyde ER, Debelius JW, McDonald D, et al. 2017. The microbiome and human biology. Annu. Rev. Genomics Hum. Genet. 18: 65-86. https://doi.org/10.1146/annurev-genom-083115-022438
  7. Magnusdottir S, Ravcheev D, de Crecy-Lagard V,Thiele I. 2015. Systematic genome assessment of B-vitamin biosynthesis suggests co-operation among gut microbes. Front. Genet. 6: 148. https://doi.org/10.3389/fgene.2015.00148
  8. Zitvogel L, Daillere R, Roberti MP, Routy B,Kroemer G. 2017. Anticancer effects of the microbiome and its products. Nat. Rev. Microbiol. 15: 465. https://doi.org/10.1038/nrmicro.2017.44
  9. Farhana L, Banerjee HN, Verma M,Majumdar AP. 2018. Role of microbiome in carcinogenesis process and epigenetic regulation of colorectal cancer, pp. 35-55. Cancer Epigenetics for Precision Medicine, Ed. Springer,
  10. van der Beek CM, Dejong CH, Troost FJ, Masclee AA,Lenaerts K. 2017. Role of short-chain fatty acids in colonic inflammation, carcinogenesis, and mucosal protection and healing. Nutr. Rev. 75: 286-305. https://doi.org/10.1093/nutrit/nuw067
  11. Ma Y, Hu M, Zhou L, Ling S, Li Y, Kong B, et al. 2018. Dietary fiber intake and risks of proximal and distal colon cancers: A metaanalysis. Medicine 97: e11678. https://doi.org/10.1097/MD.0000000000011678
  12. Louis P, Hold GL,Flint HJ. 2014. The gut microbiota, bacterial metabolites and colorectal cancer. Nat. Rev. Microbiol. 12: 661-672. https://doi.org/10.1038/nrmicro3344
  13. Koh A, De Vadder F, Kovatcheva-Datchary P,Backhed F. 2016. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 165: 1332-1345. https://doi.org/10.1016/j.cell.2016.05.041
  14. Donohoe DR, Garge N, Zhang X, Sun W, O'Connell TM, Bunger MK, et al. 2011. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab. 13: 517-526. https://doi.org/10.1016/j.cmet.2011.02.018
  15. Perego S, Sansoni V, Banfi G,Lombardi G. 2018. Sodium butyrate has anti-proliferative, pro-differentiating, and immunomodulatory effects in osteosarcoma cells and counteracts the TNFα-induced low-grade inflammation. Int. J. Immunopathol. Pharmacol. 31: 0394632017752240.
  16. Zeng H, Taussig DP, Cheng W-H, Johnson LK,Hakkak R. 2017. Butyrate inhibits cancerous HCT116 colon cell proliferation but to a lesser extent in noncancerous NCM460 colon cells. Nutrients 9: 25. https://doi.org/10.3390/nu9010025
  17. Goncalves P,Martel F. 2013. Butyrate and colorectal cancer: the role of butyrate transport. Curr. Drug Metab. 14: 994-1008. https://doi.org/10.2174/1389200211314090006
  18. Macia L, Tan J, Vieira AT, Leach K, Stanley D, Luong S, et al. 2015. Metabolite-sensing receptors GPR43 and GPR109A facilitate dietary fibre-induced gut homeostasis through regulation of the inflammasome. Nat. Commun. 6: 6734. https://doi.org/10.1038/ncomms7734
  19. Haque S,Morris JC. 2017. Transforming growth factor-β: A therapeutic target for cancer. Hum. Vaccin. Immunother. 13: 1741-1750. https://doi.org/10.1080/21645515.2017.1327107
  20. Zeng H, Claycombe KJ,Reindl KM. 2015. Butyrate and deoxycholic acid play common and distinct roles in HCT116 human colon cell proliferation. J. Nutr. Biochem. 26: 1022-1028. https://doi.org/10.1016/j.jnutbio.2015.04.007
  21. Bordonaro M,Lazarova DL. 2015. CREB-binding protein, p300, butyrate, and Wnt signaling in colorectal cancer. World J. Gastroenterol. 21: 8238. https://doi.org/10.3748/wjg.v21.i27.8238
  22. Wu GD, Compher C, Chen EZ, Smith SA, Shah RD, Bittinger K, et al. 2016. Comparative metabolomics in vegans and omnivores reveal constraints on diet-dependent gut microbiota metabolite production. Gut 65: 63-72. https://doi.org/10.1136/gutjnl-2014-308209
  23. Yousefi B, Eslami M, Ghasemian A, Kokhaei P, Salek Farrokhi A,Darabi N. 2019. Probiotics importance and their immunomodulatory properties. J. Cell. Physiol. 234: 8008-8018. https://doi.org/10.1002/jcp.27559
  24. Jacouton E, Chain F, Sokol H, Langella P,Bermudez-Humaran LG. 2017. Probiotic strain Lactobacillus casei BL23 prevents colitisassociated colorectal cancer. Front. Immunol. 8: 1553. https://doi.org/10.3389/fimmu.2017.01553
  25. Belcheva A, Irrazabal T, Robertson SJ, Streutker C, Maughan H, Rubino S, et al. 2014. Gut microbial metabolism drives transformation of MSH2-deficient colon epithelial cells. Cell 158: 288-299. https://doi.org/10.1016/j.cell.2014.04.051
  26. Grivennikov SI, Wang K, Mucida D, Stewart CA, Schnabl B, Jauch D, et al. 2012. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature 491: 254-258. https://doi.org/10.1038/nature11465
  27. Ryu TY, Kim K, Son M-Y, Min J-K, Kim J, Han T-S, et al. 2019. Downregulation of PRMT1, a histone arginine methyltransferase, by sodium propionate induces cell apoptosis in colon cancer. Oncol.Rep. 41: 1691-1699.
  28. Kimura I, Inoue D, Maeda T, Hara T, Ichimura A, Miyauchi S, et al. 2011. Short-chain fatty acids and ketones directly regulate sympathetic nervous system via G protein-coupled receptor 41 (GPR41). Proc. Natl. Acad. Sci. USA 108: 8030-8035. https://doi.org/10.1073/pnas.1016088108
  29. Orlando A, Messa C, Linsalata M, Cavallini A,Russo F. 2009. Effects of Lactobacillus rhamnosus GG on proliferation and polyamine metabolism in HGC-27 human gastric and DLD-1 colonic cancer cell lines. Immunopharmacol. Immunotoxicol. 31: 108-116. https://doi.org/10.1080/08923970802443631
  30. Miene C, Weise A,Glei M. 2011. Impact of polyphenol metabolites produced by colonic microbiota on expression of COX-2 and GSTT2 in human colon cells (LT97). Nutr. Cancer 63: 653-662. https://doi.org/10.1080/01635581.2011.552157
  31. Cardona F, Andres-Lacueva C, Tulipani S, Tinahones FJ,Queipo-Ortuno MI. 2013. Benefits of polyphenols on gut microbiota and implications in human health. J. Nutr. Biochem. 24: 1415-1422. https://doi.org/10.1016/j.jnutbio.2013.05.001
  32. Bultman SJ. 2016. Presented at the Seminars in oncology.
  33. Gonzalez-Sarrias A, Gimenez-Bastida JA, Nunez-Sanchez MA, Larrosa M, Garcia-Conesa MT, Tomas-Barberan FA, et al. 2014. Phase-II metabolism limits the antiproliferative activity of urolithins in human colon cancer cells. Eur. J. Nutr. 53: 853-864. https://doi.org/10.1007/s00394-013-0589-4
  34. Zhao W, Shi F, Guo Z, Zhao J, Song X,Yang H. 2018. Metabolite of ellagitannins, urolithin A induces autophagy and inhibits metastasis in human sw620 colorectal cancer cells. Mol. Carcinog. 57: 193-200. https://doi.org/10.1002/mc.22746
  35. Yan L, Spitznagel EL,Bosland MC. 2010. Soy consumption and colorectal cancer risk in humans: a meta-analysis. Cancer Epidemiol. Biomarkers Prev. 19: 148-158. https://doi.org/10.1158/1055-9965.EPI-09-0856
  36. Cai Y, Zhang H, Niu W, Zou Y,Ma D. 2017. Effects of equol on colon cancer cell proliferation. Beijing Da Xue Xue Bao. 49: 383-387.
  37. Wlodarska M, Luo C, Kolde R, d'Hennezel E, Annand JW, Heim CE, et al. 2017. Indoleacrylic acid produced by commensal peptostreptococcus species suppresses inflammation. Cell Host Microbe. 22: 25-37. e26. https://doi.org/10.1016/j.chom.2017.06.007
  38. Dilzer A,Park Y. 2012. Implication of conjugated linoleic acid (CLA) in human health. Crit Rev. Food Sci. Nutr. 52: 488-513. https://doi.org/10.1080/10408398.2010.501409
  39. Kim EJ, Kang I-J, Cho HJ, Kim WK, Ha Y-L,Park JHY. 2003. Conjugated linoleic acid downregulates insulin-like growth factor-I receptor levels in HT-29 human colon cancer cells. J. Nutr. 133: 2675-2681. https://doi.org/10.1093/jn/133.8.2675
  40. Kim K-J, Lee J, Park Y,Lee S-H. 2015. ATF3 mediates anti-cancer activity of trans-10, cis-12-conjugated linoleic acid in human colon cancer cells. Biomol. Ther. 23: 134-140. https://doi.org/10.4062/biomolther.2014.107
  41. Kuniyasu H, Yoshida K, Sasaki T, Sasahira T, Fujii K,Ohmori H. 2006. Conjugated linoleic acid inhibits peritoneal metastasis in human gastrointestinal cancer cells. Int. J. Cancer 118: 571-576. https://doi.org/10.1002/ijc.21368
  42. Ijiri M, Fujiya M, Konishi H, Tanaka H, Ueno N, Kashima S, et al. 2017. Ferrichrome identified from Lactobacillus casei ATCC334 induces apoptosis through its iron-binding site in gastric cancer cells. Tumor Biol. 39: 1010428317711311.
  43. Konishi H, Fujiya M, Tanaka H, Ueno N, Moriichi K, Sasajima J, et al. 2016. Probiotic-derived ferrichrome inhibits colon cancer progression via JNK-mediated apoptosis. Nat. Commun. 7: 1-12.
  44. Karpinski TM,Szkaradkiewicz AK. 2013. Characteristic of bacteriocines and their application. Pol. J. Microbiol. 62: 223-235. https://doi.org/10.33073/pjm-2013-030
  45. Nielsen DS, Cho G-S, Hanak A, Huch M, Franz CM,Arneborg N. 2010. The effect of bacteriocin-producing Lactobacillus plantarum strains on the intracellular pH of sessile and planktonic Listeria monocytogenes single cells. Int. J. Food Microbiol. 141: S53-S59. https://doi.org/10.1016/j.ijfoodmicro.2010.03.040
  46. Lievin V, Peiffer I, Hudault S, Rochat F, Brassart D, Neeser J, et al. 2000. Bifidobacterium strains from resident infant human gastrointestinal microflora exert antimicrobial activity. Gut 47: 646-652. https://doi.org/10.1136/gut.47.5.646
  47. Balgir PP, Bhatia P,Kaur B. 2010. Sequence analysis and homology based modeling to assess structure-function relationship of pediocin CP2 of Pediococcus acidilactici MTCC 5101. IJBT 9: 431-434.
  48. Knychalski B,Lukienczuk T. 2012. The evaluation of diagnostic value of the tumor markers: CCSA-2 and CEA in colorectal cancer. Pol. Przegl. Chir. 84: 86-92. https://doi.org/10.2478/v10035-012-0014-3
  49. Norouzi Z, Salimi A, Halabian R,Fahimi H. 2018. Nisin, a potent bacteriocin and anti-bacterial peptide, attenuates expression of metastatic genes in colorectal cancer cell lines. J. Microb. Pathog. 123: 183-189. https://doi.org/10.1016/j.micpath.2018.07.006
  50. Ahmadi S, Ghollasi M,Hosseini HMJMp. 2017. The apoptotic impact of nisin as a potent bacteriocin on the colon cancer cells. Microb. Pathog. 111: 193-197. https://doi.org/10.1016/j.micpath.2017.08.037
  51. Paulos CM, Wrzesinski C, Kaiser A, Hinrichs CS, Chieppa M, Cassard L, et al. 2007. Microbial translocation augments the function of adoptively transferred self/tumor-specific CD8+ T cells via TLR4 signaling. J. Clin. Invest 117: 2197-2204. https://doi.org/10.1172/JCI32205
  52. Ryu TY, Kim K, Son M-Y, Min J-K, Kim J, Han T-S, et al. 2019. Downregulation of PRMT1, a histone arginine methyltransferase, by sodium propionate induces cell apoptosis in colon cancer. Oncol. Rep. 41: 1691-1699.
  53. Wang SM, Zhang LW, Gu W, Xue CH, Zhang YC, et al. 2012. Screening for antiproliferative effect of lactobacillus strains against colon cancer HT-29 cells. Adv. Mater. Res. 573: 1039-1043.
  54. Dongarra ML, Rizzello V, Muccio L, Fries W, Cascio A, Bonaccorsi I, et al. 2013. Mucosal immunology and probiotics. Curr. Allergy Asthma Rep. 13: 19-26. https://doi.org/10.1007/s11882-012-0313-0
  55. Kim H-J, Kim Y-J, Lee S-H, Yu J, Jeong SK,Hong S-J. 2014. Effects of Lactobacillus rhamnosus on allergic march model by suppressing Th2, Th17, and TSLP responses via CD4+ CD25+ Foxp3+ Tregs. Clin. Immunol. 153: 178-186. https://doi.org/10.1016/j.clim.2014.04.008
  56. Volman JJ, Ramakers JD, Plat J. 2008. Dietary modulation of immune function by β-glucans. Physiol. Behav. 94: 276-284. https://doi.org/10.1016/j.physbeh.2007.11.045
  57. Hong F, Hansen RD, Yan J, Allendorf DJ, Baran JT, Ostroff GR, et al. 2003. β-Glucan functions as an adjuvant for monoclonal antibody immunotherapy by recruiting tumoricidal granulocytes as killer cells. Cancer Res. 63: 9023-9031.
  58. Artur Javmen, Ausra Nemeikaite-Ceniene, Maksim Bratchikov, Saulius Grigiskis, Fortunatas Grigas, Irena Jonauskiene, et al. 2015. β-Glucan from Saccharomyces cerevisiae induces IFN-γ production in vivo in BALB/c mice. In Vivo. 29: 359-363.
  59. Wang S, Han X, Zhang L, Zhang Y, Li H,Jiao Y. 2018. Whole peptidoglycan extracts from the lactobacillus paracasei subsp. Paracasei M5 strain exert anticancer activity in vitro. Biomed. Res. Int. 2018: 2871710.
  60. Rong J, Liu S, Hu C,Liu C. 2019. Single probiotic supplement suppresses colitis-associated colorectal tumorigenesis by modulating inflammatory development and microbial homeostasis. J. Gastroenterol. Hepatol. 34: 1182-1192. https://doi.org/10.1111/jgh.14516
  61. Ghoneum,Mamdooh. 2014. Apoptotic effect of a novel kefir product, PFT, on multidrug-resistant myeloid leukemia cells via a holepiercing mechanism. Int. J. Oncol. 44: 830-837. https://doi.org/10.3892/ijo.2014.2258
  62. Yousef N, Babak H, Minoo H, Norhafizah A,Ahmad YK. 2015. The prophylactic effect of probiotic Enterococcus lactis IW5 against different human cancer cells. Front. Microbiol. 6: 1317. https://doi.org/10.3389/fmicb.2015.01317
  63. Orlando A, Refolo M, Messa C, Amati L, Lavermicocca P, Guerra V, et al. 2012. Antiproliferative and proapoptotic effects of viable or heat-killed Lactobacillus paracasei IMPC2. 1 and Lactobacillus rhamnosus GG in HGC-27 gastric and DLD-1 colon cell lines. Nutr. Cancer 64: 1103-1111. https://doi.org/10.1080/01635581.2012.717676
  64. Al‐Busaidi IS, Bailey T, Dobbs B, Eglinton TW, Wakeman CJ,Frizelle FA. 2019. Complete resection of colorectal cancer with ovarian metastases combined with chemotherapy is associated with improved survival. ANZ J. Surg. 89: 1091-1096. https://doi.org/10.1111/ans.14930
  65. Chung I-C, OuYang C-N, Yuan S-N, Lin H-C, Huang K-Y, Wu P-S, et al. 2019. Pretreatment with a heat-killed probiotic modulates the NLRP3 inflammasome and attenuates colitis-associated colorectal cancer in mice. Nutrients 11: 516. https://doi.org/10.3390/nu11030516
  66. Agah S, Alizadeh AM, Mosavi M, Ranji P, Khavari-Daneshvar H, Ghasemian F, et al. 2019. More protection of Lactobacillus acidophilus than Bifidobacterium bifidum probiotics on azoxymethane-induced mouse colon cancer. Probiotics Antimicrob. Proteins 11: 857-864. https://doi.org/10.1007/s12602-018-9425-8
  67. Aisu N, Tanimura S, Yamashita Y, Yamashita K, Maki K, Yoshida Y, et al. 2015. Impact of perioperative probiotic treatment for surgical site infections in patients with colorectal cancer. Exp. Ther. Med. 10: 966-972. https://doi.org/10.3892/etm.2015.2640
  68. Theodoropoulos GE, Memos NA, Peitsidou K, Karantanos T, Spyropoulos BG,Zografos G. 2016. Synbiotics and gastrointestinal function-related quality of life after elective colorectal cancer resection. Ann. Gastroenterol. 29: 56-62.
  69. Consoli MLD, da Silva RS, Nicoli JR, Bruna‐Romero O, da Silva RG, de Vasconcelos Generoso S, et al. 2016. Randomized clinical trial: impact of oral administration of Saccharomyces boulardii on gene expression of intestinal cytokines in patients undergoing colon resection. JPEN J. Parenter Enteral Nutr. 40: 1114-1121. https://doi.org/10.1177/0148607115584387
  70. Hibberd AA, Lyra A, Ouwehand AC, Rolny P, Lindegren H, Cedgard L, et al. 2017. Intestinal microbiota is altered in patients with colon cancer and modified by probiotic intervention. BMJ Open Gastroenterol. 4: e000145. https://doi.org/10.1136/bmjgast-2017-000145
  71. Flesch AT, Tonial ST, Contu PDC, Damin DC. 2017. Perioperative synbiotics administration decreases postoperative infections in patients with colorectal cancer: a randomized, double-blind clinical trial. Randomized Controlled Trial 44: 567-573.

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