Browse > Article
http://dx.doi.org/10.4014/jmb.2002.02032

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)
Publication Information
Journal of Microbiology and Biotechnology / v.30, no.11, 2020 , pp. 1607-1613 More about this Journal
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
Gut microbiota; gut microbial metabolites; bacteria components; colorectal cancer; anticancer effect;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 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.   DOI
2 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.
3 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.
4 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.   DOI
5 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.   DOI
6 Volman JJ, Ramakers JD, Plat J. 2008. Dietary modulation of immune function by β-glucans. Physiol. Behav. 94: 276-284.   DOI
7 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.
8 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.
9 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.   DOI
10 Siegel RL, Miller KD,Jemal A. 2020. Cancer statistics, 2020. CA Cancer J. Clin. 70: 7-30.   DOI
11 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.   DOI
12 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.
13 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.   DOI
14 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.   DOI
15 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.   DOI
16 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.   DOI
17 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.   DOI
18 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.   DOI
19 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.   DOI
20 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.   DOI
21 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.   DOI
22 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.   DOI
23 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.   DOI
24 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.   DOI
25 Zitvogel L, Daillere R, Roberti MP, Routy B,Kroemer G. 2017. Anticancer effects of the microbiome and its products. Nat. Rev. Microbiol. 15: 465.   DOI
26 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,
27 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.
28 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.   DOI
29 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.   DOI
30 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.   DOI
31 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.   DOI
32 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.   DOI
33 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.
34 Louis P, Hold GL,Flint HJ. 2014. The gut microbiota, bacterial metabolites and colorectal cancer. Nat. Rev. Microbiol. 12: 661-672.   DOI
35 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.   DOI
36 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.   DOI
37 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.   DOI
38 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.
39 Goncalves P,Martel F. 2013. Butyrate and colorectal cancer: the role of butyrate transport. Curr. Drug Metab. 14: 994-1008.   DOI
40 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.   DOI
41 Haque S,Morris JC. 2017. Transforming growth factor-β: A therapeutic target for cancer. Hum. Vaccin. Immunother. 13: 1741-1750.   DOI
42 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.   DOI
43 Bordonaro M,Lazarova DL. 2015. CREB-binding protein, p300, butyrate, and Wnt signaling in colorectal cancer. World J. Gastroenterol. 21: 8238.   DOI
44 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.   DOI
45 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.   DOI
46 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.   DOI
47 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.   DOI
48 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.   DOI
49 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.
50 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.   DOI
51 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.   DOI
52 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.   DOI
53 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.   DOI
54 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.   DOI
55 Bultman SJ. 2016. Presented at the Seminars in oncology.
56 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.   DOI
57 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.   DOI
58 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.
59 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.   DOI
60 Dilzer A,Park Y. 2012. Implication of conjugated linoleic acid (CLA) in human health. Crit Rev. Food Sci. Nutr. 52: 488-513.   DOI
61 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.   DOI
62 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.   DOI
63 Karpinski TM,Szkaradkiewicz AK. 2013. Characteristic of bacteriocines and their application. Pol. J. Microbiol. 62: 223-235.   DOI
64 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.   DOI
65 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.
66 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.
67 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.   DOI
68 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.   DOI
69 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.   DOI
70 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.
71 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.   DOI