The microbiome and colorectal neoplasia: Environmental modifiers of dysbiosis

Current Gastroenterology Reports

Volumn 15, Issue 9, 2013, Pages

  Turner, N D ^a   Ritchie, L E ^a   Bresalier, R S ^b   Chapkin, R S ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

Diet; Epigenetics; Intestinal microbiota; Metabolism; Transcriptional regulation

Indexed keywords

ANTIBIOTIC AGENT; CASPASE RECRUITMENT DOMAIN PROTEIN 15; INTERLEUKIN 6; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PROBIOTIC AGENT;

ARTICLE; BACTERIAL METABOLISM; CANCER GROWTH; CANCER RISK; CELL CYCLE REGULATION; COLITIS; COLON CARCINOGENESIS; COLON MUCOSA; COLON TUMOR; COLORECTAL TUMOR; DIETARY FIBER; DISEASE COURSE; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; EPITHELIUM CELL; HOST PATHOGEN INTERACTION; HUMAN; INTESTINE CELL; INTESTINE CRYPT; INTESTINE FLORA; METABOLITE; METABOLOMICS; MICROBIAL ACTIVITY; MICROBIAL COLONIZATION; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MICROBIOME; NONHUMAN; RADIATION ENTEROPATHY; RADIATION INJURY; RADIATION PROTECTION; RADIOSENSITIVITY; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; BACTERIA; BREAST FEEDING; COLON; COLORECTAL NEOPLASMS; DIET; DYSBIOSIS; ENVIRONMENT; INTESTINE; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; MICROFLORA; NEWBORN; PATHOPHYSIOLOGY; PHYSIOLOGY; SYMBIOSIS; BACTERIUM; REVIEW;

BACTERIA; BREAST FEEDING; COLON; COLORECTAL NEOPLASMS; DIET; DYSBIOSIS; ENVIRONMENT; HUMANS; INFANT, NEWBORN; INTESTINAL MUCOSA; INTESTINES; MICROBIOTA; SIGNAL TRANSDUCTION; SYMBIOSIS;

EID: 84881356086     PISSN: 15228037     EISSN: 1534312X     Source Type: Journal    
DOI: 10.1007/s11894-013-0346-0     Document Type: Article

References (100)

1. Siegel R, Ward E, Brawley O, Jemal A. Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin. 2011;61:212-36.
2. Smith BD, Smith GL, Hurria A, et al. Future of cancer incidence in the United States: burdens upon an aging, changing nation. J Clin Oncol. 2009;27:2758-65.
3. Kau AL, Ahern PP, Griffin NW, et al. Human nutrition, the gut microbiome and the immune system. Nature. 2011;474:327-36.
4. Man SM, Kaakoush NO, Mitchell HM. The role of bacteria and pattern-recognition receptor's in Crohn's disease. Nat Rev Gastroenterol Hepatol. 2011;8:152-68.
5. Candela M, Guidotti M, Fabbri A, et al. Human intestinal microbiota: cross talk with the host and its potential role in colorectal cancer. Crit Rev Micro. 2011;37:1-14.
6. Hamer HM, De Preter V, Windey K, Verbeke K. Functional analysis of colonic bacterial metabolism: relevant to health? Amer J Physiol Gastrointest Liver Physiol. 2012;302:G1-9.
7. Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat Rev Genet. 2012;13:260-70.
8. Shen XJ, Rawls JF, Randall T, et al. Molecular characterization of mucosal adherent bacteria and associations with colorectal adenomas. Gut Microbes. 2010;1:138-47.
9. Sobhani I, Tap J, Roudot-Thoraval F, et al. Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS One. 2011;6:e16393.
10. Ellmerich S, Schöller M, Duranton B, et al. Promotion of intestinal carcinogenesis by Streptococcus bovis. Carcinogenesis. 2000;21:753-6. (Pubitemid 30214033)
11. Duncan CG, Leary RJ, Lin J, et al. Identification of microbial DNA in human cancer. BMC Med Genomics. 2009;2:22. doi: 10.1186/1755-8794-2-22.
12. Fukata M, Abreau MT. Microflora in colorectal cancer: a friend to fear. Nat Med. 2010;16:639-41.
13. Compare D, Nardone G. Contribution of gut microbiota to colonic and extracolonic cancer development. Dig Dis. 2011;29:554-61.
14. Vipperia K, O'Keefe SJ. The microbiota and its metabolites in colonic mucosal health and cancer risk. Nutr Clin Practice. 2013;27:624-35.
15. Gold JS, Bayar S, Salem RR. Association of Streptococcus bovis bacteremia with colonic neoplasia and extracolonic malignancy. Arch Surg. 2004;139:760-5. (Pubitemid 38886513)
16. Bibiloni R, Mangold M, Madsen KL, et al. The bacteriology of biopsies differs between newly diagnosed, untreated, Crohn's disease and ulcerative colitis patients. J Med Microbiol. 2006;55:1141-9. (Pubitemid 44215574)
17. •• Hajishengallis G, Darveau RP, Curtis MA. The keystone-pathogen hypothesis. Nature Rev Microbiol. 2012;10:717-25. This paper proposes a new theory describing how low-abundance pathogens may be capable of causing inflammation.
18. McDonald SA, Preston SI, Lovell MJ, et al. Mechanisms of disease: from stem cells to colorectal cancer. Nat Clin Pract Gastroenterol Hepatol. 2006;3:267-74. (Pubitemid 43675023)
19. Willis ND, Przyborski SA, Hutchinson CJ, Wilson RG. Colonic and colorectal cancer stem cells: progress in the search of putative biomarkers. J Anat. 2008;213:59-65. (Pubitemid 352044396)
20. •• Pédron T, Mulet C, Dauga C, et al. A crypt-specific core microbiota resides in the mouse colon. mBIO. 2012;3(3):e00116-12. This paper points out the critical need to characterize specific niche microbial populations if we are going to fully understand the contribution of microbiota to colon cancer. It will be necessary to perform this type of work if we are going to identify chemoprotective interventions.
21. Macfarlane S, Woodmansey EJ, Macfarlane GT. Colonization of mucin by human intestinal bacteria and establishment of biofilm communities in a two-stage continuous culture system. Appl Environ Microbiol. 2005;71:7483-92. (Pubitemid 43194242)
22. Kosiewicz MM, Zirnheld AL, Alard P. Gut microbiota, immunity, and disease: A complex relationship. Front Microbiol. 2011;2:180. doi: 10.3389/fmicb.2011.00180.
23. Wells JM, Rossi O, Meijerink M, van Baarlen P. Epithelial crosstalk at the microbiota-mucosal interface. Proc Natl Acad Sci USA. 2011;108 Suppl 1:4607-14.
24. Smythies LD, Shen R, Bimczok D, et al. Inflammation anergy in human intestinal macrophages is due to Smad-induced IκBα expression and NF-κB inactivation. J Biol Chem. 2010;285:19593-604.
25. Saleh M, Trinchieri G. Innate immune mechanisms of colitis and colitis-associated colorectal cancer. Nat Rev Immunol. 2011;11:9-20.
26. Abreu MT. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol. 2010;10:131-44.
27. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, et al. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004;118:229-41. (Pubitemid 38962578)
28. Brint EK, MacSharry J, Fanning A, et al. Differential expression of toll-like receptors in patients with irritable bowel syndrome. Am J Gastroenterol. 2011;106:329-36.
29. Pimentel-Nunes P, Gonçalves N, Boal-Carvalho I, et al. Decreased toll-interacting protein and peroxisome proliferator-activated receptor γ are associated with increased expression of toll-like receptors in colon carcinogenesis. J Clin Pathol. 2012;65:302-8.
30. Lee J, Mo J-H, Katakura K, et al. Maintenance of colonic homeostasis by distinctive apical TLR9 signalling in intestinal epithelial cells. Nat Cell Biol. 2006;8:1327-36. (Pubitemid 44835107)
31. Chen GY, Shaw MH, Redondo G, Núñez G. The innate immune receptor Nod1 protects the intestine from inflammation-induced tumorigenesis. Cancer Res. 2008;68:10060-7.
32. Arthur JC, Jobin C. The struggle within: Microbial influences on colorectal cancer. Inflamm Bowel Dis. 2011;17:396-409.
33. Couturier-Maillard A, Secher T, Rehman A, et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J Clin Invest. 2013;123:700-11.
34. Langowski JL, Zhang X, Wu L, et al. IL-23 promotes tumour incidence and growth. Nature. 2006;442:461-5. (Pubitemid 44264796)
35. Grivennikov SI, Wang K, Mucida D, et al. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature. 2012;491:254-8.
36. Wu S, Rhee K-J, Albesiano E, et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med. 2009;15:1016-22.
37. Jobin C. Colorectal cancer: CRC - all about microbial products and barrier function? Nat Rev Gastroenterol Hepatol. 2012;9:694-6.
38. Tjalsma H, Boleij A, Marchesi JR, et al. A bacterial driver-passenger model for colorectal cancer: Beyond the usual suspects. Nat Rev Microbiol. 2012;10:575-82.
39. Wang L, Yi T, Zhang W, et al. IL-17 enhances tumor development in carcinogen-induced skin cancer. Cancer Res. 2010;70:10112-20.
40. Ji Y, Zhang W. Th17 cells: Positive or negative role in tumor? Cancer Immunol Immunother. 2010;59:979-87.
41. Murugaiyan G, Saha B. Protumor vs antitumor functions of IL-17. J Immunol. 2009;183:4169-75.
42. Yang S, Wang B, Guan C, et al. Foxp3 + IL-17+ T cells promote development of cancer-initiating cells in colorectal cancer. J Leuk Biol. 2011;89:85-91.
43. Macfarlane GT, Macfarlane S. Bacteria, colonic fermentation, and gastrointestinal health. J AOAC Int. 2012;95:50-60.
44. De Preter V, Arjis I, Windey K, et al. Imparied butyrate oxidation in ulcerative colitis is due to decreased butyrate uptake and a defect in the oxidation pathway. Infl Bowel Dis. 2012;18:1127-36.
45. O'Keefe SJD. Nutrition and colonic health: The critical role of microbiota. Curr Opin Gastroenterol. 2008;24:51-8. (Pubitemid 350190898)
46. Walton GE, van den Heuvel EGHM, Kosters MHW, et al. A randomized crossover study investigating the effects of galacto-oligosaccharides on the faecal microbiota in men and women over 50 years of age. Br J Nutr. 2012;107:1466-75.
47. Modis K, Coletta C, Erdelyi K, et al. Intramitochondrial hydrogen sulfide production by 3-mercaptopyruvate sulfurtransferase maintains mitochondrial electron flow and supports cellular bioenergetics. FASEB J. 2013;27:601-11.
48. •• Maurice CF, Haiser HJ, Turnbaugh PJ. Xenobiotics shape the physiology and gene expression of the active human gut microbiome. Cell. 2013;152:39-50. This paper demonstrates the importance of characterizing the functional changes in microbiota, in addition to determining microbial diversity when exposed to exogenous compounds.
49. • van Duynhoven J, Vaughan EE, Jacobs DM, et al. Metabolic fate of polyphenols in the human superorganism. Proc Natl Acad Sci. 2011;108:4531-8. This review provides an excellent overview of the multiple ways in which dietary polyphenols influence the dynamic relationship between microbiota and the host.
50. Cueva C, Sánchez-Patán F, Monagas M, et al. In vitro fermentation of grape seed flavan-3-ol fractions by human faecal microbiota: changes in microbial groups and phenolic metabolites. FEMS Microbiol Ecol. 2012;83:792-805.
51. Gall WE, Beebe K, Lawton KA, et al. α-hydroxybutyrate is an early biomarker of insulin resistance and glucose intolerance in a nondiabetic population. PLoS One. 2010;5:e10883.
52. Zhao C, Ivanov I, Dougherty ER, et al. Non-invasive detection of candidate molecular biomarkers in subjects with a history of insulin resistance and colorectal adenomas. Cancer Prev Res. 2009;2:590-7.
53. Yehuda-Shnaidman E, Schwartz B. Mechanisms linking obesity, inflammation and altered metabolism to colon carcinogenesis. Obesity Rev. 2012;13:1083-95.
54. Calani L, Dall'Asta M, Derlindati E, et al. Colonic metabolism of polyphenols from coffee, green tea, and hazelnut skins. J Clin Gastroenterol. 2012;46 Suppl 1:S95-9.
55. Holmes E, Kinross J, Gibson GR, et al. Therapeutic modulation of microbiota-host metabolic interactions. Sci Trans Med. 2012;4:137rv6.
56. Nicholson JK, Holmes E, Kinross J, et al. Host-gut microbiota metabolic interactions. Science. 2012;336:1262-7.
57. • Donohoe DR, Garge N, Zhang X, et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab. 2011;13:517-26. This paper describes a well-controlled set of experiments that identify the role of butyrate in colonocyte homeostasis.
58. Dumas M-E. The microbial-mammalian metabolic axis: Beyond simple metabolism. Cell Metab. 2011;13:489-90.
59. Cho Y, Kim H, Turner ND, et al. A chemoprotective fish oil- and pectin-containing diet temporally alters gene expression profiles in exfoliated rat colonocytes throughout oncogenesis. J Nutr. 2011;141:1029-35.
60. Waf1/Cip1 expression in vivo by butyrate administration can be chemoprotective or chemopromotive depending on the lipid component of the diet. Carcinogenesis. 2008;29:1415-20.
61. Barrasa JI, Santiago-Gómez A, Olmo N, et al. Resistance to butyrate impairs bile acid-induced apoptosis in human colon adenocarcinoma cells via up-regulation of Bcl-2 and inactivation of Bax. Biochim Biophys Acta. 2012;1823:2201-9.
62. Turk HF, Kolar SS, Fan YY, et al. Linoleic acid and butyrate synergize to increase Bcl-2 levels in colonocytes. Int J Cancer. 2011;128:63-71.
63. Cherbuy C, Honvo-Houeto E, Bruneau A, et al. Microbiota matures colonic epithelium through a coordinated induction of cell cycle-related proteins in gnotobiotic rat. Am J Physiol Gastrointest Liver Physiol. 2010;299:G348-57.
64. Cho Y, Turner ND, Davidson LA, et al. A chemoprotective fish oil/pectin diet enhances apoptosis via Bcl-2 promoter methylation in rat azoxymethane-induced carcinomas. Exp Biol Med. 2012;237:1387-93.
65. Davidson LA, Nguyen DV, Hokanson RM, et al. Chemopreventive n-3 polyunsaturated fatty acids reprogram genetic signatures during colon cancer initiation and progression in the rat. Cancer Res. 2004;64:6797-804. (Pubitemid 39297944)
66. Davidson LA, Wang N, Ivanov I, et al. Identification of actively translated mRNA transcripts in a rat model of early-stage colon carcinogenesis. Cancer Prev Res. 2009;2:984-94.
67. Wilson AJ, Chueh AC, Tögel L, et al. Apoptotic sensitivity of colon cancer cells to histone deacetylase inhibitors is mediated by an Sp1/Sp3-activated transcriptional program involving immediate-early gene induction. Cancer Res. 2010;70:609-20.
68. Rajendran P, Williams DE, Ho E, Dashwood RH. Metabolism as a key to histone deacetylase inhibition. Crit Rev Biochem Mol Biol. 2011;46:181-99.
69. Wu S, Li RW, Li W, Li C. Transcriptome characterization by RNA-seq unravels the mechanisms of butyrate-induced epigenomic regulation in bovine cells. PLoS One. 2012;7:e36940.
70. Wilson AJ, Byun DS, Nasser S, et al. HDAC4 promotes growth of colon cancer cells via repression of p21. Mol Biol Cell. 2008;19:4062-75.
71. Min/+ mice. Carcinogenesis. 2012;33:1231-8.
72. Arthur JC, Perez-Chanona E, Mühlbauer M, et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science. 2012;338:120-3.
73. Chen H-M, Yu Y-N, Wang J-L, et al. Decreased dietary fiber intake and structural alteration of gut microbiota in patients with advanced colorectal adenoma. Am J Clin Nutr. 2013;97:1044-52.
74. Conlon MA, Kerr CA, McSweeney CS, et al. Resistant starches protect against colonic DNA damage and alter microbiota and gene expression in rats fed a Western diet. J Nutr. 2012;142:832-40.
75. Hooda S, Boler BMV, Serao MCR, et al. 454 pyrosequencing reveals a shift in fecal microbiota of healthy adult men consuming polydextrose or soluble corn fiber. J Nutr. 2012;142:1259-65.
76. Kuo S-M. The interplay between fiber and the intestinal microbiota in the inflammatory response. Adv Nutr. 2013;4:16-28.
77. Ghosh S, DeCoffe D, Brown K, et al. Fish oil attenuates omega-6 polyunsaturated fatty acid-induced dysbiosis and infectious colitis but impairs LPS dephosphorylation activity causing sepsis. PLoS One. 2013;8(2):e55468.
78. Chapkin RS, Seo J, McMurray DN, Lupton JR. Mechanisms by which docosahexaeonic acid and related fatty acids reduce colon cancer risk and inflammatory disorders of the intestine. Chem Phys Lipids. 2008;153:14-23.
79. 2+ accumulation in human colon cancer cells and primary cultures of rat colonic crypts. Am J Physiol Gastrointest Liver Physiol. 2007;293:G935-43. (Pubitemid 350106557)
80. 2+ loading and apoptosis in colonocytes. Cancer. 2011;117:5294-303.
81. Simoes CD, Maukonen J, Kaprio J, et al. Habitual dietary intake is associated with stool microbiota composition in monozygotic twins. J Nutr. 2013;143:417-23.
82. Azcárate-Peril MA, Sikes M, Bruno-Bárcena JM. The intestinal microbiota, gastrointestinal environment and colorectal cancer: A putative role for probiotics in prevention of colorectal cancer? Am J Physiol Gastrointest Liver Physiol. 2011;301:G401-24.
83. Zhu Y, Luo TM, Jobin C, Young HA. Gut microbiota and probiotics in colon tumorigenesis. Cancer Lett. 2011;309:119-27.
84. Gourbeyre P, Denery S, Bodinier M. Probiotics, prebiotics, and synbiotics: Impact on the gut immune system and allergic reactions. J Leukoc Biol. 2011;89:685-95.
85. Appleyard CB, Cruz ML, Isidro AA, et al. Pretreatemnt with the probiotic VSL#3 delays transition from inflammation to dysplasia in a rat model of colitis-associated cancer. Am J Physiol Gastrointest Liver Physiol. 2011;301:G1004-13.
86. Cho I, Yamanishi S, Cox L, et al. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature. 2012;488:621-6.
87. McLaughlin MM, Dacquisto MP, Jacobus DP, Horowitz RE. Effects of the germfree state on responses of mice to whole-body irradiation. Rad Res. 1964;23:333-49.
88. Crawford PA, Gordon JI. Microbial regulation of intestinal radiosensitivity. Proc Nat Acad Sci USA. 2005;102:13254-9. (Pubitemid 41325010)
89. Manichanh C, Varela E, Martinez C, et al. The gut microbiota predispose to the pathophysiology of acute postradiotherapy diarrhea. Am J Gastroenterol. 2008;103:1754-61.
90. Egan LJ, Eckmann L, Greten FR, et al. IκB-kinaseβ-dependent NF-κB activation provides radioprotection to the intestinal epithelium. Proc Nat Acad Sci USA. 2004;101:2452-7. (Pubitemid 38269332)
91. Palmer C, Bik EM, DiGiulio DB, et al. Development of the human infant intestinal microbiota. PLoS Biol. 2007;5:e177. (Pubitemid 47105346)
92. Donovan SM, Wang M, Li M, et al. Host-microbe interactions in the neonatal intestine: Role of human milk oligosaccharides. Adv Nutr. 2012;3:4505-55.
93. Marcobal A, Sonnenburg JL. Human milk oligosaccharide consumption by intestinal microbiota. Clin Microbiol Infect. 2012;18 Suppl 4:12-5.
94. Zivkovic AM, German JB, Lebrilla CB, Mills DA. Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc Natl Acad Sci USA. 2011;108 Suppl 1:4653-8.
95. • Schwartz S, Friedberg I, Ivanov IV, et al. A metagenomic study of diet-dependent interaction between gut microbiota and host in infants reveals differences in immune response. Genome Biol. 2012;13:r32. doi: 10.1186/gb-2012-13-4-r32. This paper describes the interplay between colonizing microbiota and gene expression in the developing neonatal intestinal tract.
96. Payne AN, Chassard C, Banz Y, Lacroix C. The composition and metabolic activity of child gut microbiota demonstrate differential adaptation to varied nutrient loads in an in vitro model of colonic fermentation. FEMS Microbiol Ecol. 2012;80:608-23.
97. Young W, Roy NC, Lee J, et al. Changes in bowel microbiota induced by feeding weanlings resistant starch stimulate transcriptomic and physiological responses. Appl Environ Microbiol. 2012;78:6656-64.
98. Fança-Berthon P, Hoebler C, Mouzet E, et al. Intrauterine growth restriction not only modifies the cecocolonic microbiota in neonatal rats but also affects its activity in young adult rats. J Ped Gastro Nutr. 2010;51:402-13.
99. Joss-Moore LA, Lane RH. The developmental origins of adult disease. Curr Opin Ped. 2009;21:230-4.
100. Ahlquist DA, Zou H, Domanico M, et al. Next-generation stool DNA accurately detects colorectal cancer and large adenomas. Gastroenterol. 2012;142:248-56.