Microbiome and colorectal cancer: Unraveling host-microbiota interactions in colitis-associated colorectal cancer development

Seminars in Immunology

Volumn 32, Issue , 2017, Pages 3-13

  Kang, Mingsong ^a   Martin, Alberto ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Colon cancer; Inflammation; Microbiota

Indexed keywords

PREBIOTIC AGENT; PROBIOTIC AGENT;

CARCINOGENESIS; CHRONIC INFLAMMATION; COLITIS; COLORECTAL CANCER; COMMENSAL; DIET; DYSBIOSIS; ENTERITIS; FECAL MICROBIOTA TRANSPLANTATION; GENE EXPRESSION; GENETIC DISORDER; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREGULATION; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; METABOLISM; NONHUMAN; NUTRIENT SUPPLY; OPPORTUNISTIC INFECTION; REVIEW; SPECIES COMPOSITION; ANIMAL; BIOLOGICAL THERAPY; COLORECTAL TUMOR; COMPLICATION; IMMUNOLOGY; INFLAMMATION; MICROBIOLOGY; MICROFLORA;

ANIMALS; BIOLOGICAL THERAPY; COLITIS; COLORECTAL NEOPLASMS; DYSBIOSIS; GASTROINTESTINAL MICROBIOME; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; MICROBIOTA;

EID: 85018396001     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2017.04.003     Document Type: Review

References (175)

1. Li, S.K., Martin, A., Mismatch repair and colon cancer: mechanisms and therapies explored. Trends Mol. Med. 22:4 (2016), 274–289.
2. Key Statistics for Colorectal Cancer, The American Cancer Society https://www.cancer.org/cancer/colon-rectal-cancer/about/key-statistics.html.
3. Colorectal cancer statistics, Canadian Cancer Society http://www.cancer.ca/en/cancer-information/cancer-type/colorectal/statistics/?region=on.
4. Arnold, M., Sierra, M.S., Laversanne, M., Soerjomataram, I., Jemal, A., Bray, F., Global patterns and trends in colorectal cancer incidence and mortality. Gut 66:4 (2017), 683–691.
5. Mariotto, A.B., Yabroff, K.R., Shao, Y., Feuer, E.J., Brown, M.L., Projections of the cost of cancer care in the United States: 2010–2020. J. Natl. Cancer Inst. 103:2 (2011), 117–128.
6. Lasry, A., Zinger, A., Ben-Neriah, Y., Inflammatory networks underlying colorectal cancer. Nat. Immunol. 7:3 (2016), 230–240.
7. Molodecky, N.A., Kaplan, G.G., Environmental risk factors for inflammatory bowel disease. Gastroenterol. Hepatol. 6:5 (2010), 339–346.
8. Raffals, L.E., Chang, E.B., Navigating the microbial basis of inflammatory bowel diseases: seeing the light at the end of the tunnel. Gut Liver 10:4 (2016), 502–508.
9. Dalal, S.R., Chang, E.B., The microbial basis of inflammatory bowel diseases. J. Clin. Invest. 24:10 (2014), 4190–4196.
10. Tamboli, C.P., Neut, C., Desreumaux, P., Colombel, J.F., Dysbiosis in inflammatory bowel disease. Gut 53:1 (2004), 1–4.
11. Kaiko, G.E., Stappenbeck, T.S., Host-microbe interactions shaping the gastrointestinal environment. Trends Immunol. 5:11 (2014), 538–548.
12. O'Hara, A.M., Shanahan, F., The gut flora as a forgotten organ. EMBO Rep. 7:7 (2006), 688–693.
13. Hakansson, A., Molin, G., Gut microbiota and inflammation. Nutrients 3:6 (2011), 637–682.
14. Jandhyala, S.M., Talukdar, R., Subramanyam, C., Vuyyuru, H., Sasikala, M., Nageshwar Reddy, D., Role of the normal gut microbiota. World J. Gastroenterol. 21:29 (2015), 8787–8803.
15. Guinane, C.M., Cotter, P.D., Role of the gut microbiota in health and chronic gastrointestinal disease: understanding a hidden metabolic organ. Ther. Adv. Gastroenterol. 6:4 (2013), 295–308.
16. Pessione, E., Lactic acid bacteria contribution to gut microbiota complexity: lights and shadows. Front. Cell. Infect. Microbiol., 2, 2012, 86.
17. Rooks, M.G., Garrett, W.S., Gut microbiota, metabolites and host immunity. Nat. Rev. Immunol. 16:6 (2016), 341–352.
18. Peterson, L.W., Artis, D., Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat. Rev. Immunol. 14:3 (2014), 141–153.
19. Muniz, L.R., Knosp, C., Yeretssian, G., Intestinal antimicrobial peptides during homeostasis, infection, and disease. Front. Immunol., 3(310), 2012.
20. Kamada, N., Chen, G.Y., Inohara, N., Nunez, G., Control of pathogens and pathobionts by the gut microbiota. Nat. Immunol. 14:7 (2013), 685–690.
21. Kato, L.M., Kawamoto, S., Maruya, M., Fagarasan, S., The role of the adaptive immune system in regulation of gut microbiota. Immunol. Rev. 260:1 (2014), 67–75.
22. Wells, J.M., Rossi, O., Meijerink, M., van Baarlen, P., Epithelial crosstalk at the microbiota-mucosal interface. Proc. Natl. Acad. Sci. U. S. A. 108:Suppl. 1 (2011), 4607–4614.
23. Iliev, I.D., Mileti, E., Matteoli, G., Chieppa, M., Rescigno, M., Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning. Mucosal Immunol. 2:4 (2009), 340–350.
24. Harrison, O.J., Powrie, F.M., Regulatory T cells and immune tolerance in the intestine. Cold Spring Harbor Perspect. Biol., 5(7), 2013.
25. Round, J.L., Mazmanian, S.K., The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9:5 (2009), 313–323.
26. Correa-Oliveira, R., Fachi, J.L., Vieira, A., Sato, F.T., Vinolo, M.A., Regulation of immune cell function by short-chain fatty acids. Clin. Transl. Immunol., 5(4), 2016, e73.
27. Sonnenburg, J.L., Backhed, F., Diet-microbiota interactions as moderators of human metabolism. Nature 535:7610 (2016), 56–64.
28. Morrison, D.J., Preston, T., Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism. Gut Microbes 7:3 (2016), 189–200.
29. Donohoe, D.R., Collins, L.B., Wali, A., Bigler, R., Sun, W., Bultman, S.J., The Warburg effect dictates the mechanism of butyrate-mediated histone acetylation and cell proliferation. Mol. Cell 8:4 (2012), 612–626.
30. Belcheva, A., Irrazabal, T., Robertson, S.J., Streutker, C., Maughan, H., Rubino, S., Moriyama, E.H., Copeland, J.K., Kumar, S., Green, B., Geddes, K., Pezo, R.C., Navarre, W.W., Milosevic, M., Wilson, B.C., Girardin, S.E., Wolever, T.M., Edelmann, W., Guttman, D.S., Philpott, D.J., Martin, A., Gut microbial metabolism drives transformation of MSH2-deficient colon epithelial cells. Cell 158:2 (2014), 288–299.
31. Neis, E.P., Dejong, C.H., Rensen, S.S., The role of microbial amino acid metabolism in host metabolism. Nutrients 7:4 (2015), 2930–2946.
32. Verbeke, K.A., Boobis, A.R., Chiodini, A., Edwards, C.A., Franck, A., Kleerebezem, M., Nauta, A., Raes, J., van Tol, E.A., Tuohy, K.M., Towards microbial fermentation metabolites as markers for health benefits of prebiotics. Nutr. Res. Rev. 28:1 (2015), 42–66.
33. LeBlanc, J.G., Milani, C., de Giori, G.S., Sesma, F., van Sinderen, D., Ventura, M., Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr. Opin. Biotechnol. 24:2 (2013), 160–168.
34. Sartor, R.B., Microbial influences in inflammatory bowel diseases. Gastroenterology 134:2 (2008), 577–594.
35. Ribet, D., Cossart, P., How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes Infect. 17:3 (2015), 173–183.
36. Pizarro-Cerda, J., Cossart, P., Bacterial adhesion and entry into host cells. Cell 124:4 (2006), 715–727.
37. Kang, M., Ko, Y.P., Liang, X., Ross, C.L., Liu, Q., Murray, B.E., Hook, M., Collagen-binding microbial surface components recognizing adhesive matrix molecule (MSCRAMM) of Gram-positive bacteria inhibit complement activation via the classical pathway. J. Biol. Chem. 88:28 (2013), 20520–20531.
38. Mogensen, T.H., Pathogen recognition and inflammatory signaling in innate immune defenses. Clin. Microbiol. Rev. 22:2 (2009), 240–273 (Table of Contents).
39. Perez-Lopez, A., Behnsen, J., Nuccio, S.P., Raffatellu, M., Mucosal immunity to pathogenic intestinal bacteria. Nat. Rev. Immunol. 16:3 (2016), 135–148.
40. Kim, M., Ashida, H., Ogawa, M., Yoshikawa, Y., Mimuro, H., Sasakawa, C., Bacterial interactions with the host epithelium. Cell Host Microbe 8:1 (2010), 20–35.
41. LaRock, D.L., Chaudhary, A., Miller, S.I., Salmonellae interactions with host processes. Nat. Rev. Microbiol. 13:4 (2015), 191–205.
42. Baumler, A.J., Sperandio, V., Interactions between the microbiota and pathogenic bacteria in the gut. Nature 35:7610 (2016), 85–93.
43. Buc, E., Dubois, D., Sauvanet, P., Raisch, J., Delmas, J., Darfeuille-Michaud, A., Pezet, D., Bonnet, R., High prevalence of mucosa-associated E. coli producing cyclomodulin and genotoxin in colon cancer. PLoS One, 8(2), 2013, e56964.
44. Bonnet, M., Buc, E., Sauvanet, P., Darcha, C., Dubois, D., Pereira, B., Dechelotte, P., Bonnet, R., Pezet, D., Darfeuille-Michaud, A., Colonization of the human gut by E. coli and colorectal cancer risk. Clin. Cancer Res. 20:4 (2014), 859–867.
45. Garrett, W.S., Gallini, C.A., Yatsunenko, T., Michaud, M., DuBois, A., Delaney, M.L., Punit, S., Karlsson, M., Bry, L., Glickman, J.N., Gordon, J.I., Onderdonk, A.B., Glimcher, L.H., Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe 8:3 (2010), 292–300.
46. Uzoigwe, J.C., Khaitsa, M.L., Gibbs, P.S., Epidemiological evidence for Mycobacterium avium subspecies paratuberculosis as a cause of Crohn's disease. Epidemiol. Infect. 35:7 (2007), 1057–1068.
47. Burich, A., Hershberg, R., Waggie, K., Zeng, W., Brabb, T., Westrich, G., Viney, J.L., Maggio-Price, L., Helicobacter-induced inflammatory bowel disease in IL-10- and T cell-deficient mice. Am. J. Physiol. Gastrointest. Liver Physiol. 281:3 (2001), G764–G778.
48. Nguyen, D.D., Muthupalani, S., Goettel, J.A., Eston, M.A., Mobley, M., Taylor, N.S., McCabe, A., Marin, R., Snapper, S.B., Fox, J.G., Colitis and colon cancer in WASP-deficient mice require helicobacter species. Inflamm. Bowel Dis. 9:10 (2013), 2041–2050.
49. Eaton, K.A., Opp, J.S., Gray, B.M., Bergin, I.L., Young, V.B., Ulcerative typhlocolitis associated with Helicobacter mastomyrinus in telomerase-deficient mice. Vet. Pathol. 48:3 (2011), 713–725.
50. Chichlowski, M., Sharp, J.M., Vanderford, D.A., Myles, M.H., Hale, L.P., Helicobacter typhlonius and Helicobacter rodentium differentially affect the severity of colon inflammation and inflammation-associated neoplasia in IL10-deficient mice. Comp. Med. 58:6 (2008), 534–541.
51. Frank, D.N., St Amand, A.L., Feldman, R.A., Boedeker, E.C., Harpaz, N., Pace, N.R., Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. U. S. A. 104:34 (2007), 13780–13785.
52. Gagniere, J., Raisch, J., Veziant, J., Barnich, N., Bonnet, R., Buc, E., Bringer, M.A., Pezet, D., Bonnet, M., Gut microbiota imbalance and colorectal cancer. World J. Gastroenterol. 22:2 (2016), 501–518.
53. Grasso, F., Frisan, T., Bacterial genotoxins: merging the DNA damage response into infection biology. Biomolecules 5:3 (2015), 1762–1782.
54. Arthur, J.C., Perez-Chanona, E., Muhlbauer, M., Tomkovich, S., Uronis, J.M., Fan, T.J., Campbell, B.J., Abujamel, T., Dogan, B., Rogers, A.B., Rhodes, J.M., Stintzi, A., Simpson, K.W., Hansen, J.J., Keku, T.O., Fodor, A.A., Jobin, C., Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 38:6103 (2012), 120–123.
55. Arthur, J.C., Gharaibeh, R.Z., Muhlbauer, M., Perez-Chanona, E., Uronis, J.M., McCafferty, J., Fodor, A.A., Jobin, C., Microbial genomic analysis reveals the essential role of inflammation in bacteria-induced colorectal cancer. Nat. Commun., 5, 2014, 4724.
56. Guidi, R., Guerra, L., Levi, L., Stenerlow, B., Fox, J.G., Josenhans, C., Masucci, M.G., Frisan, T., Chronic exposure to the cytolethal distending toxins of Gram-negative bacteria promotes genomic instability and altered DNA damage response. Cell. Microbiol. 15:1 (2013), 98–113.
57. Haghjoo, E., Galan, J.E., Salmonella typhi encodes a functional cytolethal distending toxin that is delivered into host cells by a bacterial-internalization pathway. Proc. Natl. Acad. Sci. U. S. A. 101:13 (2004), 4614–4619.
58. Graillot, V., Dormoy, I., Dupuy, J., Shay, J.W., Huc, L., Mirey, G., Vignard, J., Genotoxicity of cytolethal distending toxin (CDT) on isogenic human colorectal cell lines: potential promoting effects for colorectal carcinogenesis. Front. Cell. Infect. Microbiol., 6, 2016, 34.
59. Buti, L., Spooner, E., Van der Veen, A.G., Rappuoli, R., Covacci, A., Ploegh, H.L., Helicobacter pylori cytotoxin-associated gene A (CagA) subverts the apoptosis-stimulating protein of p53 (ASPP2) tumor suppressor pathway of the host. Proc. Natl. Acad. Sci. U. S. A. 108:22 (2011), 9238–9243.
60. Housseau, F., Sears, C.L., Enterotoxigenic Bacteroides fragilis (ETBF)-mediated colitis in Min (Apc+/-) mice: a human commensal-based murine model of colon carcinogenesis. ABBV Cell Cycle 9:1 (2010), 3–5.
61. Wu, S., Morin, P.J., Maouyo, D., Sears, C.L., Bacteroides fragilis enterotoxin induces c-Myc expression and cellular proliferation. Gastroenterology 24:2 (2003), 392–400.
62. Gur, C., Ibrahim, Y., Isaacson, B., Yamin, R., Abed, J., Gamliel, M., Enk, J., Bar-On, Y., Stanietsky-Kaynan, N., Coppenhagen-Glazer, S., Shussman, N., Almogy, G., Cuapio, A., Hofer, E., Mevorach, D., Tabib, A., Ortenberg, R., Markel, G., Miklic, K., Jonjic, S., Brennan, C.A., Garrett, W.S., Bachrach, G., Mandelboim, O., Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity 42:2 (2015), 344–355.
63. Kostic, A.D., Chun, E., Robertson, L., Glickman, J.N., Gallini, C.A., Michaud, M., Clancy, T.E., Chung, D.C., Lochhead, P., Hold, G.L., El-Omar, E.M., Brenner, D., Fuchs, C.S., Meyerson, M., Garrett, W.S., Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 14:2 (2013), 207–215.
64. Rubinstein, M.R., Wang, X., Liu, W., Hao, Y., Cai, G., Han, Y.W., Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/beta-catenin signaling via its FadA adhesin. Cell Host Microbe 14:2 (2013), 195–206.
65. Abed, J., Emgard, J.E., Zamir, G., Faroja, M., Almogy, G., Grenov, A., Sol, A., Naor, R., Pikarsky, E., Atlan, K.A., Mellul, A., Chaushu, S., Manson, A.L., Earl, A.M., Ou, N., Brennan, C.A., Garrett, W.S., Bachrach, G., Fap2 mediates Gusobacterium nucleatum colorectal adenocarcinoma enrichment by binding to tumor-expressed Gal-GalNAc. Cell Host Microbe 20:2 (2016), 215–225.
66. Balish, E., Warner, T., Enterococcus faecalis induces inflammatory bowel disease in interleukin-10 knockout mice. Am. J. Pathol. 60:6 (2002), 2253–2257.
67. Mirza, N.N., McCloud, J.M., Cheetham, M.J., Clostridium septicum sepsis and colorectal cancer - a reminder. World J. Surg. Oncol., 7, 2009, 73.
68. Grahn, N., Hmani-Aifa, M., Fransen, K., Soderkvist, P., Monstein, H.J., Molecular identification of Helicobacter DNA present in human colorectal adenocarcinomas by 16S rDNA PCR amplification and pyrosequencing analysis. J. Med. Microbiol. 4:Pt 11 (2005), 1031–1035.
69. Zhang, Y., Hoffmeister, M., Weck, M.N., Chang-Claude, J., Brenner, H., Helicobacter pylori infection and colorectal cancer risk: evidence from a large population-based case-control study in Germany. Am. J. Epidemiol. 175:5 (2012), 441–450.
70. Zumkeller, N., Brenner, H., Zwahlen, M., Rothenbacher, D., Helicobacter pylori infection and colorectal cancer risk: a meta-analysis. Helicobacter 11:2 (2006), 75–80.
71. Lee, Y.K., Mazmanian, S.K., Has the microbiota played a critical role in the evolution of the adaptive immune system?. Science 30:6012 (2010), 1768–1773.
72. Tomasello, G., Tralongo, P., Damiani, P., Sinagra, E., Di Trapani, B., Zeenny, M.N., Hussein, I.H., Jurjus, A., Leone, A., Dismicrobism in inflammatory bowel disease and colorectal cancer: changes in response of colocytes. World J. Gastroenterol. 0:48 (2014), 18121–18130.
73. Hansen, J.J., Immune responses to intestinal microbes in inflammatory bowel diseases. Curr. Allergy Asthma Rep., 15(10), 2015, 61.
74. Schultsz, C., Van Den Berg, F.M., Ten Kate, F.W., Tytgat, G.N., Dankert, J., The intestinal mucus layer from patients with inflammatory bowel disease harbors high numbers of bacteria compared with controls. Gastroenterology 117:5 (1999), 1089–1097.
75. Trier, J.S., Mucosal flora in inflammatory bowel disease: intraepithelial bacteria or endocrine epithelial cell secretory granules?. Gastroenterology, 123(3), 2002, 955 (author reply 956).
76. Swidsinski, A., Ladhoff, A., Pernthaler, A., Swidsinski, S., Loening-Baucke, V., Ortner, M., Weber, J., Hoffmann, U., Schreiber, S., Dietel, M., Lochs, H., Mucosal flora in inflammatory bowel disease. Gastroenterology 22:1 (2002), 44–54.
77. Sobhani, I., Amiot, A., Le Baleur, Y., Levy, M., Auriault, M.L., Van Nhieu, J.T., Delchier, J.C., Microbial dysbiosis and colon carcinogenesis: could colon cancer be considered a bacteria-related disease?. Ther. Adv. Gastroenterol. 6:3 (2013), 215–229.
78. Nakatsu, G., Li, X., Zhou, H., Sheng, J., Wong, S.H., Wu, W.K., Ng, S.C., Tsoi, H., Dong, Y., Zhang, N., He, Y., Kang, Q., Cao, L., Wang, K., Zhang, J., Liang, Q., Yu, J., Sung, J.J., Gut mucosal microbiome across stages of colorectal carcinogenesis. Nat. Commun., 6, 2015, 8727.
79. Gordon, H., Trier Moller, F., Andersen, V., Harbord, M., Heritability in inflammatory bowel disease: from the first twin study to genome-wide association studies. Inflamm. Bowel Dis. 21:6 (2015), 1428–1434.
80. Khor, B., Gardet, A., Xavier, R.J., Genetics and pathogenesis of inflammatory bowel disease. Nature 474:7351 (2011), 307–317.
81. Blekhman, R., Goodrich, J.K., Huang, K., Sun, Q., Bukowski, R., Bell, J.T., Spector, T.D., Keinan, A., Ley, R.E., Gevers, D., Clark, A.G., Host genetic variation impacts microbiome composition across human body sites. Genome Biol., 16, 2015, 191.
82. Lewis, J.D., Chen, E.Z., Baldassano, R.N., Otley, A.R., Griffiths, A.M., Lee, D., Bittinger, K., Bailey, A., Friedman, E.S., Hoffmann, C., Albenberg, L., Sinha, R., Compher, C., Gilroy, E., Nessel, L., Grant, A., Chehoud, C., Li, H., Wu, G.D., Bushman, F.D., Inflammation, antibiotics, and diet as environmental stressors of the gut microbiome in pediatric Crohn's disease. Cell Host Microbe 18:4 (2015), 489–500.
83. Craven, M., Egan, C.E., Dowd, S.E., McDonough, S.P., Dogan, B., Denkers, E.Y., Bowman, D., Scherl, E.J., Simpson, K.W., Inflammation drives dysbiosis and bacterial invasion in murine models of ileal Crohn's disease. PLoS One, 7(7), 2012, e41594.
84. Dore, J., Blottiere, H., The influence of diet on the gut microbiota and its consequences for health. Curr. Opin. Biotechnol. 32 (2015), 195–199.
85. den Besten, G., van Eunen, K., Groen, A.K., Venema, K., Reijngoud, D.J., Bakker, B.M., The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J. Lipid Res. 54:9 (2013), 2325–2340.
86. Becattini, S., Taur, Y., Pamer, E.G., Antibiotic-induced changes in the intestinal microbiota and disease. Trends Mol. Med. 22:6 (2016), 458–478.
87. Abraham, C., Medzhitov, R., Interactions between the host innate immune system and microbes in inflammatory bowel disease. Gastroenterology 140:6 (2011), 1729–1737.
88. Michielan, A., D'Inca, R., Intestinal permeability in inflammatory bowel disease: pathogenesis clinical evaluation, and therapy of leaky gut. Mediators Inflamm., 2015, 2015, 628157.
89. Hammer, A.M., Morris, N.L., Earley, Z.M., Choudhry, M.A., The first line of defense: the effects of alcohol on post-burn intestinal barrier, immune cells, and microbiome. Alcohol Res.: Curr. Rev. 37:2 (2015), 209–222.
90. Fyderek, K., Strus, M., Kowalska-Duplaga, K., Gosiewski, T., Wedrychowicz, A., Jedynak-Wasowicz, U., Sladek, M., Pieczarkowski, S., Adamski, P., Kochan, P., Heczko, P.B., Mucosal bacterial microflora and mucus layer thickness in adolescents with inflammatory bowel disease. World J. Gastroenterol. 15:42 (2009), 5287–5294.
91. Van der Sluis, M., De Koning, B.A., De Bruijn, A.C., Velcich, A., Meijerink, J.P., Van Goudoever, J.B., Buller, H.A., Dekker, J., Van Seuningen, I., Renes, I.B., Einerhand, A.W., Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 131:1 (2006), 117–129.
92. Wenzel, U.A., Magnusson, M.K., Rydstrom, A., Jonstrand, C., Hengst, J., Johansson, M.E., Velcich, A., Ohman, L., Strid, H., Sjovall, H., Hansson, G.C., Wick, M.J., Spontaneous colitis in Muc2-deficient mice reflects clinical and cellular features of active ulcerative colitis. PLoS One, 9(6), 2014, e100217.
93. An, G., Wei, B., Xia, B., McDaniel, J.M., Ju, T., Cummings, R.D., Braun, J., Xia, L., Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans. J. Exp. Med. 204:6 (2007), 1417–1429.
94. Bergstrom, K., Liu, X., Zhao, Y., Gao, N., Wu, Q., Song, K., Cui, Y., Li, Y., McDaniel, J.M., McGee, S., Chen, W., Huycke, M.M., Houchen, C.W., Zenewicz, L.A., West, C.M., Chen, H., Braun, J., Fu, J., Xia, L., Defective intestinal mucin-type O-glycosylation causes spontaneous colitis-associated cancer in mice. Gastroenterology 151:1 (2016), 152–164 (e11).
95. Velcich, A., Yang, W., Heyer, J., Fragale, A., Nicholas, C., Viani, S., Kucherlapati, R., Lipkin, M., Yang, K., Augenlicht, L., Colorectal cancer in mice genetically deficient in the mucin Muc2. Science 295:5560 (2002), 1726–1729.
96. Desai, M.S., Seekatz, A.M., Koropatkin, N.M., Kamada, N., Hickey, C.A., Wolter, M., Pudlo, N.A., Kitamoto, S., Terrapon, N., Muller, A., Young, V.B., Henrissat, B., Wilmes, P., Stappenbeck, T.S., Nunez, G., Martens, E.C., A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell 167:5 (2016), 1339–1353 (e21).
97. McCole, D.F., IBD candidate genes and intestinal barrier regulation. Inflamm. Bowel Dis. 0:10 (2014), 1829–1849.
98. Whitcomb, D.C., LaRusch, J., Krasinskas, A.M., Klei, L., Smith, J.P., Brand, R.E., Neoptolemos, J.P., Lerch, M.M., Tector, M., Sandhu, B.S., Guda, N.M., Orlichenko, L., Alzheimer's Disease Genetics, C., Alkaade, S., Amann, S.T., Anderson, M.A., Baillie, J., Banks, P.A., Conwell, D., Cote, G.A., Cotton, P.B., DiSario, J., Farrer, L.A., Forsmark, C.E., Johnstone, M., Gardner, T.B., Gelrud, A., Greenhalf, W., Haines, J.L., Hartman, D.J., Hawes, R.A., Lawrence, C., Lewis, M., Mayerle, J., Mayeux, R., Melhem, N.M., Money, M.E., Muniraj, T., Papachristou, G.I., Pericak-Vance, M.A., Romagnuolo, J., Schellenberg, G.D., Sherman, S., Simon, P., Singh, V.P., Slivka, A., Stolz, D., Sutton, R., Weiss, F.U., Wilcox, C.M., Zarnescu, N.O., Wisniewski, S.R., O'Connell, M.R., Kienholz, M.L., Roeder, K., Barmada, M.M., Yadav, D., Devlin, B., Common genetic variants in the CLDN2 and PRSS1-PRSS2 loci alter risk for alcohol-related and sporadic pancreatitis. Nat. Genet. 44:12 (2012), 1349–1354.
99. Luettig, J., Rosenthal, R., Barmeyer, C., Schulzke, J.D., Claudin-2 as a mediator of leaky gut barrier during intestinal inflammation. Tissue Barriers, 3(1–2), 2015, e977176.
100. Soderman, J., Noren, E., Christiansson, M., Bragde, H., Thiebaut, R., Hugot, J.P., Tysk, C., O'Morain, C.A., Gassull, M., Finkel, Y., Colombel, J.F., Lemann, M., Almer, S., Analysis of single nucleotide polymorphisms in the region of CLDN2-MORC4 in relation to inflammatory bowel disease. World J. Gastroenterol. 9:30 (2013), 4935–4943.
101. Chellappa, K., Deol, P., Evans, J.R., Vuong, L.M., Chen, G., Briancon, N., Bolotin, E., Lytle, C., Nair, M.G., Sladek, F.M., Opposing roles of nuclear receptor HNF4alpha isoforms in colitis and colitis-associated colon cancer. eLife, 5, 2016.
102. Ahn, S.H., Shah, Y.M., Inoue, J., Morimura, K., Kim, I., Yim, S., Lambert, G., Kurotani, R., Nagashima, K., Gonzalez, F.J., Inoue, Y., Hepatocyte nuclear factor 4alpha in the intestinal epithelial cells protects against inflammatory bowel disease. Inflamm. Bowel Dis. 14:7 (2008), 908–920.
103. Spalinger, M.R., McCole, D.F., Rogler, G., Scharl, M., Protein tyrosine phosphatase non-receptor type 2 and inflammatory bowel disease. World J. Gastroenterol. 22:3 (2016), 1034–1044.
104. Wehkamp, J., Fellermann, K., Stange, E.F., Human defensins in Crohn's disease. Chem. Immunol. Allergy 86 (2005), 42–54.
105. Ramasundara, M., Leach, S.T., Lemberg, D.A., Day, A.S., Defensins and inflammation: the role of defensins in inflammatory bowel disease. J. Gastroenterol. Hepatol. 24:2 (2009), 202–208.
106. McGovern, D.P., van Heel, D.A., Ahmad, T., Jewell, D.P., NOD2 (CARD15), the first susceptibility gene for Crohn's disease. Gut 49:6 (2001), 752–754.
107. Rogler, G., The effects of NOD2/CARD15 mutations on the function of the intestinal barrier. J. Crohns Colitis 1:2 (2007), 53–60.
108. Tan, G., Zeng, B., Zhi, F.C., Regulation of human enteric alpha-defensins by NOD2 in the Paneth cell lineage. Eur. J. Cell Biol. 4:1 (2015), 60–66.
109. Rocha, J.D., Schlossmacher, M.G., Philpott, D.J., LRRK2 and Nod2 promote lysozyme sorting in Paneth cells. Nat. Immunol. 16:9 (2015), 898–900.
110. Zhang, Q., Pan, Y., Yan, R., Zeng, B., Wang, H., Zhang, X., Li, W., Wei, H., Liu, Z., Commensal bacteria direct selective cargo sorting to promote symbiosis. Nat. Immunol. 6:9 (2015), 918–926.
111. Agarwal, S., Mayer, L., Diagnosis and treatment of gastrointestinal disorders in patients with primary immunodeficiency. Clin. Gastroenterol. Hepatol. 11:9 (2013), 1050–1063.
112. Bianco, A.M., Girardelli, M., Tommasini, A., Genetics of inflammatory bowel disease from multifactorial to monogenic forms. World J. Gastroenterol. 21:43 (2015), 12296–12310.
113. Kamada, N., Seo, S.U., Chen, G.Y., Nunez, G., Role of the gut microbiota in immunity and inflammatory disease. Nat. Rev. Immunol. 13:5 (2013), 321–335.
114. Sojka, D.K., Huang, Y.H., Fowell, D.J., Mechanisms of regulatory T-cell suppression - a diverse arsenal for a moving target. Immunology 124:1 (2008), 13–22.
115. Barnes, M.J., Powrie, F., Regulatory T cells reinforce intestinal homeostasis. Immunity 31:3 (2009), 401–411.
116. Kiesler, P., Fuss, I.J., Strober, W., Experimental models of inflammatory bowel diseases. Cell. Mol. Gastroenterol. Hepatol. 1:2 (2015), 154–170.
117. Mayne, C.G., Williams, C.B., Induced and natural regulatory T cells in the development of inflammatory bowel disease. Inflamm. Bowel Dis. 19:8 (2013), 1772–1788.
118. Bacchetta, R., Passerini, L., Gambineri, E., Dai, M., Allan, S.E., Perroni, L., Dagna-Bricarelli, F., Sartirana, C., Matthes-Martin, S., Lawitschka, A., Azzari, C., Ziegler, S.F., Levings, M.K., Roncarolo, M.G., Defective regulatory and effector T cell functions in patients with FOXP3 mutations. J. Clin. Invest. 116:6 (2006), 1713–1722.
119. McMurchy, A.N., Di Nunzio, S., Roncarolo, M.G., Bacchetta, R., Levings, M.K., Molecular regulation of cellular immunity by FOXP3. Adv. Exp. Med. Biol. 665 (2009), 30–46.
120. Moran, C.J., Walters, T.D., Guo, C.H., Kugathasan, S., Klein, C., Turner, D., Wolters, V.M., Bandsma, R.H., Mouzaki, M., Zachos, M., Langer, J.C., Cutz, E., Benseler, S.M., Roifman, C.M., Silverberg, M.S., Griffiths, A.M., Snapper, S.B., Muise, A.M., IL-10R polymorphisms are associated with very-early-onset ulcerative colitis. Inflamm. Bowel Dis. 9:1 (2013), 115–123.
121. Rivas, M.A., Beaudoin, M., Gardet, A., Stevens, C., Sharma, Y., Zhang, C.K., Boucher, G., Ripke, S., Ellinghaus, D., Burtt, N., Fennell, T., Kirby, A., Latiano, A., Goyette, P., Green, T., Halfvarson, J., Haritunians, T., Korn, J.M., Kuruvilla, F., Lagace, C., Neale, B., Lo, K.S., Schumm, P., Torkvist, L., National Institute of, D., Digestive Kidney Diseases Inflammatory Bowel Disease Genetics, C., United Kingdom Inflammatory Bowel Disease Genetics, C., International Inflammatory Bowel Disease Genetics, C., Dubinsky, M.C., Brant, S.R., Silverberg, M.S., Duerr, R.H., Altshuler, D., Gabriel, S., Lettre, G., Franke, A., D'Amato, M., McGovern, D.P., Cho, J.H., Rioux, J.D., Xavier, R.J., Daly, M.J., Deep resequencing of GWAS loci identifies independent rare variants associated with inflammatory bowel disease. Nat. Genet. 43:11 (2011), 1066–1073.
122. Muzes, G., Molnar, B., Sipos, F., Regulatory T cells in inflammatory bowel diseases and colorectal cancer. World J. Gastroenterol. 18:40 (2012), 5688–5694.
123. Kayama, H., Ueda, Y., Sawa, Y., Jeon, S.G., Ma, J.S., Okumura, R., Kubo, A., Ishii, M., Okazaki, T., Murakami, M., Yamamoto, M., Yagita, H., Takeda, K., Intestinal CX3C chemokine receptor 1(high) (CX3CR1(high)) myeloid cells prevent T-cell-dependent colitis. Proc. Natl. Acad. Sci. U. S. A. 109:13 (2012), 5010–5015.
124. Crusz, S.M., Balkwill, F.R., Inflammation and cancer: advances and new agents. Nat. Rev. Clin. Oncol. 12:10 (2015), 584–596.
125. Grivennikov, S.I., Inflammation and colorectal cancer: colitis-associated neoplasia. Semin. Immunopathol. 35:2 (2013), 229–244.
126. Hussain, S.P., Amstad, P., Raja, K., Ambs, S., Nagashima, M., Bennett, W.P., Shields, P.G., Ham, A.J., Swenberg, J.A., Marrogi, A.J., Harris, C.C., Increased p53 mutation load in noncancerous colon tissue from ulcerative colitis: a cancer-prone chronic inflammatory disease. Cancer Res. 60:13 (2000), 3333–3337.
127. Brentnall, T.A., Crispin, D.A., Rabinovitch, P.S., Haggitt, R.C., Rubin, C.E., Stevens, A.C., Burmer, G.C., Mutations in the p53 gene: an early marker of neoplastic progression in ulcerative colitis. Gastroenterology 07:2 (1994), 369–378.
128. Yin, J., Harpaz, N., Tong, Y., Huang, Y., Laurin, J., Greenwald, B.D., Hontanosas, M., Newkirk, C., Meltzer, S.J., p53 point mutations in dysplastic and cancerous ulcerative colitis lesions. Gastroenterology 04:6 (1993), 1633–1639.
129. Cooks, T., Pateras, I.S., Tarcic, O., Solomon, H., Schetter, A.J., Wilder, S., Lozano, G., Pikarsky, E., Forshew, T., Rosenfeld, N., Harpaz, N., Itzkowitz, S., Harris, C.C., Rotter, V., Gorgoulis, V.G., Oren, M., Mutant p53 prolongs NF-kappaB activation and promotes chronic inflammation and inflammation-associated colorectal cancer. Cancer Cell 23:5 (2013), 634–646.
130. Foran, E., Garrity-Park, M.M., Mureau, C., Newell, J., Smyrk, T.C., Limburg, P.J., Egan, L.J., Upregulation of DNA methyltransferase-mediated gene silencing, anchorage-independent growth, and migration of colon cancer cells by interleukin-6. Mol. Cancer Res. 8:4 (2010), 471–481.
131. Li, Y., Deuring, J., Peppelenbosch, M.P., Kuipers, E.J., de Haar, C., van der Woude, C.J., IL-6-induced DNMT1 activity mediates SOCS3 promoter hypermethylation in ulcerative colitis-related colorectal cancer. Carcinogenesis 3:10 (2012), 1889–1896.
132. Hartnett, L., Egan, L.J., Inflammation, DNA methylation and colitis-associated cancer. Carcinogenesis 33:4 (2012), 723–731.
133. Saleh, M., Trinchieri, G., Innate immune mechanisms of colitis and colitis-associated colorectal cancer. Nat. Rev. Immunol. 11:1 (2011), 9–20.
134. Perucho, M., Tumors with microsatellite instability: many mutations, targets and paradoxes. Oncogene 22:15 (2003), 2223–2225.
135. Li, Y., de Haar, C., Peppelenbosch, M.P., van der Woude, C.J., SOCS3 in immune regulation of inflammatory bowel disease and inflammatory bowel disease-related cancer. Cytokine Growth Factor Rev. 23:3 (2012), 127–138.
136. Grivennikov, S.I., Greten, F.R., Karin, M., Immunity, inflammation, and cancer. Cell 140:6 (2010), 883–899.
137. Hemarajata, P., Versalovic, J., Effects of probiotics on gut microbiota: mechanisms of intestinal immunomodulation and neuromodulation. Ther. Adv. Gastroenterol. 6:1 (2013), 39–51.
138. Hosono, Usman A., Desmutagenicity of milk cultured with Lactobacillus acidophilus strains against mutagenic heated tauco. Food Chem. Toxicol. 36:9–10 (1998), 805–810.
139. Rao, R.K., Samak, G., Protection and restitution of gut barrier by probiotics: nutritional and clinical implications. Curr. Nutr. Food Sci. 9:2 (2013), 99–107.
140. Karthik, S.V., Probiotics in inflammatory bowel disease. J. R. Soc. Med., 96(7), 2003, 370.
141. Celiberto, L.S., Bedani, R., Rossi, E.A., Cavallini, D.C., Probiotics: the scientific evidence in the context of inflammatory bowel disease. Crit. Rev. Food Sci. Nutr. 57:9 (2017), 1759–1768.
142. Sheil, B., Shanahan, F., O'Mahony, L., Probiotic effects on inflammatory bowel disease. J. Nutr. 137:3 Suppl. 2 (2007), 819S–824S.
143. Tamboli, C.P., Caucheteux, C., Cortot, A., Colombel, J.F., Desreumaux, P., Probiotics in inflammatory bowel disease: a critical review. Best Pract. Res. Clin. Gastroenterol. 17:5 (2003), 805–820.
144. Bibiloni, R., Fedorak, R.N., Tannock, G.W., Madsen, K.L., Gionchetti, P., Campieri, M., De Simone, C., Sartor, R.B., VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am. J. Gastroenterol. 100:7 (2005), 1539–1546.
145. Kruis, W., Fric, P., Pokrotnieks, J., Lukas, M., Fixa, B., Kascak, M., Kamm, M.A., Weismueller, J., Beglinger, C., Stolte, M., Wolff, C., Schulze, J., Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 53:11 (2004), 1617–1623.
146. Verna, E.C., Lucak, S., Use of probiotics in gastrointestinal disorders: what to recommend?. Ther. Adv. Gastroenterol. 3:5 (2010), 307–319.
147. Zhang, J.W., Du, P., Gao, J., Yang, B.R., Fang, W.J., Ying, C.M., Preoperative probiotics decrease postoperative infectious complications of colorectal cancer. Am. J. Med. Sci. 343:3 (2012), 199–205.
148. Zhu, D., Chen, X., Wu, J., Ju, Y., Feng, J., Lu, G., Ouyang, M., Ren, B., Li, Y., Effect of perioperative intestinal probiotics on intestinal flora and immune function in patients with colorectal cancer. Nan fang yi ke da xue xue bao = Journal of Southern Medical University 32:8 (2012), 1190–1193.
149. Gamallat, Y., Meyiah, A., Kuugbee, E.D., Hago, A.M., Chiwala, G., Awadasseid, A., Bamba, D., Zhang, X., Shang, X., Luo, F., Xin, Y., Lactobacillus rhamnosus induced epithelial cell apoptosis, ameliorates inflammation and prevents colon cancer development in an animal model. Biomed. Pharmacother. 83 (2016), 536–541.
150. Orlando, A., Messa, C., Linsalata, M., Cavallini, A., Russo, F., Effects of Lactobacillus rhamnosus GG on proliferation and polyamine metabolism in HGC-27 human gastric and DLD-1 colonic cancer cell lines. Immunopharmacol. Immunotoxicol. 31:1 (2009), 108–116.
151. Elfahri, K.R., Vasiljevic, T., Yeager, T., Donkor, O.N., Anti-colon cancer and antioxidant activities of bovine skim milk fermented by selected Lactobacillus helveticus strains. J. Dairy Sci. 99:1 (2016), 31–40.
152. Macfarlane, G.T., Cummings, J.H., Probiotics and prebiotics: can regulating the activities of intestinal bacteria benefit health?. West. J. Med. 171:3 (1999), 187–191.
153. Gustaw, W., Kordowska-Wiater, M., Koziol, J., The influence of selected prebiotics on the growth of lactic acid bacteria for bio-yoghurt production. Acta Sci. Pol. Technol. Aliment. 10:4 (2011), 455–466.
154. Weitkunat, K., Schumann, S., Petzke, K.J., Blaut, M., Loh, G., Klaus, S., Effects of dietary inulin on bacterial growth, short-chain fatty acid production and hepatic lipid metabolism in gnotobiotic mice. J. Nutr. Biochem. 26:9 (2015), 929–937.
155. Costabile, A., Fava, F., Roytio, H., Forssten, S.D., Olli, K., Klievink, J., Rowland, I.R., Ouwehand, A.C., Rastall, R.A., Gibson, G.R., Walton, G.E., Impact of polydextrose on the faecal microbiota: a double-blind, crossover, placebo-controlled feeding study in healthy human subjects. Br. J. Nutr. 108:3 (2012), 471–481.
156. Vinolo, M.A., Rodrigues, H.G., Nachbar, R.T., Curi, R., Regulation of inflammation by short chain fatty acids. Nutrients 3:10 (2011), 858–876.
157. Shi, Y., Dong, Y., Huang, W., Zhu, D., Mao, H., Su, P., Fecal microbiota transplantation for ulcerative colitis: a systematic review and meta-analysis. PLoS One, 11(6), 2016, e0157259.
158. Lopez, J., Grinspan, A., Fecal microbiota transplantation for inflammatory bowel disease. Gastroenterol. Hepatol. 12:6 (2016), 374–379.
159. Rossen, N.G., MacDonald, J.K., de Vries, E.M., D'Haens, G.R., de Vos, W.M., Zoetendal, E.G., Ponsioen, C.Y., Fecal microbiota transplantation as novel therapy in gastroenterology: a systematic review. World J. Gastroenterol. 1:17 (2015), 5359–5371.
160. M'Koma, A.E., Inflammatory bowel disease: an expanding global health problem. Clin. Med Insights Gastroenterol. 6 (2013), 33–47.
161. Hu, P.J., Inflammatory bowel disease in Asia: the challenges and opportunities. Intest. Res. 13:3 (2015), 188–190.
162. Ye, L., Cao, Q., Cheng, J., Review of inflammatory bowel disease in China. Sci. World J., 2013, 2013, 296470.
163. Zhiqin, W., Palaniappan, S., Raja Ali, R.A., Inflammatory bowel disease-related colorectal cancer in the Asia-Pacific region: past, present, and future. Intest. Res. 12:3 (2014), 194–204.
164. Knight-Sepulveda, K., Kais, S., Santaolalla, R., Abreu, M.T., Diet and inflammatory bowel disease. Gastroenterol. Hepatol. 11:8 (2015), 511–520.
165. Devkota, S., Wang, Y., Musch, M.W., Leone, V., Fehlner-Peach, H., Nadimpalli, A., Antonopoulos, D.A., Jabri, B., Chang, E.B., Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10-/- mice. Nature 487:7405 (2012), 104–108.
166. Day, S.D., Enos, R.T., McClellan, J.L., Steiner, J.L., Velazquez, K.T., Murphy, E.A., Linking inflammation to tumorigenesis in a mouse model of high-fat-diet-enhanced colon cancer. Cytokine 64:1 (2013), 454–462.
167. Dougherty, U., Mustafi, R., Wang, Y., Musch, M.W., Wang, C.Z., Konda, V.J., Kulkarni, A., Hart, J., Dawson, G., Kim, K.E., Yuan, C.S., Chang, E.B., Bissonnette, M., American ginseng suppresses Western diet-promoted tumorigenesis in model of inflammation-associated colon cancer: role of EGFR. BMC Complement. Altern. Med., 11, 2011, 111.
168. Yang, K., Kurihara, N., Fan, K., Newmark, H., Rigas, B., Bancroft, L., Corner, G., Livote, E., Lesser, M., Edelmann, W., Velcich, A., Lipkin, M., Augenlicht, L., Dietary induction of colonic tumors in a mouse model of sporadic colon cancer. Cancer Res. 68:19 (2008), 7803–7810.
169. Newmark, H.L., Yang, K., Kurihara, N., Fan, K., Augenlicht, L.H., Lipkin, M., Western-style diet-induced colonic tumors and their modulation by calcium and vitamin D in C57Bl/6 mice: a preclinical model for human sporadic colon cancer. Carcinogenesis 0:1 (2009), 88–92.
170. Kampman, E., Slattery, M.L., Bigler, J., Leppert, M., Samowitz, W., Caan, B.J., Potter, J.D., Meat consumption, genetic susceptibility, and colon cancer risk: a United States multicenter case-control study. Cancer Epidemiol. Biomarkers Prev. 8:1 (1999), 15–24.
171. Fuchs, C.S., Giovannucci, E.L., Colditz, G.A., Hunter, D.J., Stampfer, M.J., Rosner, B., Speizer, F.E., Willett, W.C., Dietary fiber and the risk of colorectal cancer and adenoma in women. N. Engl. J. Med. 40:3 (1999), 169–176.
172. Pietinen, P., Malila, N., Virtanen, M., Hartman, T.J., Tangrea, J.A., Albanes, D., Virtamo, J., Diet and risk of colorectal cancer in a cohort of Finnish men. Cancer Causes Control 10:5 (1999), 387–396.
173. Dieleman, L.A., Arends, A., Tonkonogy, S.L., Goerres, M.S., Craft, D.W., Grenther, W., Sellon, R.K., Balish, E., Sartor, R.B., Helicobacter hepaticus does not induce or potentiate colitis in interleukin-10-deficient mice. Infect. Immun. 68:9 (2000), 5107–5113.
174. Thomas, R.M., Jobin, C., The microbiome and cancer: is the ‘Oncobiome’ mirage real?. Trends Cancer 1:1 (2015), 24–35.
175. Drago, L., Toscano, M., De Grandi, R., Grossi, E., Padovani, E.M., Peroni, D.G., Microbiota network and mathematic microbe mutualism in colostrum and mature milk collected in two different geographic areas: Italy versus Burundi. ISME J. 11:4 (2017), 875–884.