The human microbiome and cancer

Cancer Prevention Research

Volumn 10, Issue 4, 2017, Pages 226-234

  Rajagopala, Seesandra V ^a   Vashee, Sanjay ^a   Oldfield, Lauren M ^a   Suzuki, Yo ^a   Venter, J Craig ^a,b   Telenti, Amalio ^a,b   Nelson, Karen E ^a,b  

^a J CRAIG VENTER INSTITUTE   (United States)

^b Human Longevity Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TOXIN;

AUTOPHAGY; CANCER GROWTH; CARCINOGENESIS; DISEASE ASSOCIATION; HUMAN; IMMUNITY; IMMUNOREGULATION; INTESTINE FLORA; MALIGNANT NEOPLASM; MICROBIOME; NONHUMAN; PRIORITY JOURNAL; REVIEW; MICROBIOLOGY; NEOPLASM;

GASTROINTESTINAL MICROBIOME; HUMANS; NEOPLASMS;

EID: 85017516223     PISSN: 19406207     EISSN: 19406215     Source Type: Journal    
DOI: 10.1158/1940-6207.CAPR-16-0249     Document Type: Review

References (100)

1. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, et al. Enterotypes of the human gut microbiome. Nature 2011;473:174-80.
2. Human Microbiome Project C. A framework for human microbiome research. Nature 2012;486:215-21.
3. Karlsson F, Tremaroli V, Nielsen J, Backhed F. Assessing the human gut microbiota in metabolic diseases. Diabetes 2013;62:3341-9.
4. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, et al. Richness of human gut microbiome correlates with metabolic markers. Nature 2013;500:541-6.
5. Pedersen HK, Gudmundsdottir V, Nielsen HB, Hyotylainen T, Nielsen T, Jensen BA, et al. Human gut microbes impact host serum metabolome and insulin sensitivity. Nature 2016;535:376-81.
6. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. A core gut microbiome in obese and lean twins. Nature 2009; 457:480-4.
7. Chen GY, Shaw MH, Redondo G, Nunez G. The innate immune receptor Nod1 protects the intestine from inflammation-induced tumorigenesis. Cancer Res 2008;68:10060-7.
8. Dapito DH, Mencin A, Gwak GY, Pradere JP, Jang MK, Mederacke I, et al. Promotion of hepatocellular carcinoma by the intestinal microbiota and TLR4. Cancer Cell 2012;21:504-16.
9. Dove WF, Clipson L, Gould KA, Luongo C, Marshall DJ, Moser AR, et al. Intestinal neoplasia in the ApcMin mouse: independence from the microbial and natural killer (beige locus) status. Cancer Res 1997;57:812-4.
10. Grivennikov SI, Wang K, Mucida D, Stewart CA, Schnabl B, Jauch D, et al. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature 2012;491:254-8.
11. Reddy BS, Narisawa T, Wright P, Vukusich D, Weisburger JH, Wynder EL. Colon carcinogenesis with azoxymethane and dimethylhydrazine in germ-free rats. Cancer Res 1975;35:287-90.
12. Garrett WS. Cancer and the microbiota. Science 2015;348:80-6.
13. Schwabe RF, Jobin C. The microbiome and cancer. Nat Rev Cancer 2013;13:800-12.
14. Columpsi P, Sacchi P, Zuccaro V, Cima S, Sarda C, Mariani M, et al. Beyond the gut bacterial microbiota: The gut virome. J Med Virol 2016;88:1467-72.
15. Hannigan GD, Meisel JS, Tyldsley AS, ZhengQ, Hodkinson BP, SanMiguel AJ, et al. The human skin double-stranded DNA virome: Topographical and temporal diversity, genetic enrichment, and dynamic associations with the host microbiome. mBio 2015;6:e01578-15.
16. Lopetuso LR, Ianiro G, Scaldaferri F, Cammarota G, Gasbarrini A. Gut virome and inflammatory bowel disease. Inflamm Bowel Dis 2016;22: 1708-12.
17. Pride DT, Salzman J, Haynes M, Rohwer F, Davis-Long C, White RAIII, et al. Evidence of a robust resident bacteriophage population revealed through analysis of the human salivary virome. ISME J 2012;6:915-26.
18. Yang JY, KimMS, KimE, Cheon JH, Lee YS, KimY, et al. Enteric viruses ameliorate gut inflammation via toll-like receptor 3 and toll-like receptor 7-mediated interferon-beta production. Immunity 2016;44: 889-900.
19. deMartel C, Ferlay J, Franceschi S, Vignat J, Bray F, Forman D, et al. Global burden of cancers attributable to infections in 2008: A review and synthetic analysis. Lancet Oncol 2012;13:607-15.
20. Suerbaum S, Michetti P. Helicobacter pylori infection. N Engl J Med 2002;347:1175-86.
21. Parkin DM. The global health burden of infection-associated cancers in the year 2002. Int J Cancer 2006;118:3030-44.
22. Polk DB, Peek RMJr. Helicobacter pylori: gastric cancer and beyond. Nat Rev Cancer 2010;10:403-14.
23. Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 2001;345:784-9.
24. Hardbower DM, de Sablet T, Chaturvedi R, Wilson KT. Chronic inflammation and oxidative stress: The smoking gun for Helicobacter pylori-induced gastric cancer Gut Microbes 2013;4: 475-81.
25. Koeppel M, Garcia-Alcalde F, Glowinski F, Schlaermann P, Meyer TF. Helicobacter pylori infection causes characteristic DNA damage patterns in human cells. Cell Rep 2015;11:1703-13.
26. Wroblewski LE, Peek RMJr. Helicobacter pylori in gastric carcinogenesis: mechanisms. Gastroenterol Clin North Am 2013;42: 285-98.
27. Muller A. Multistep activation of the Helicobacter pylori effector CagA. J Clin Invest 2012;122:1192-5.
28. Machado AM, Figueiredo C, Touati E, Maximo V, Sousa S, Michel V, et al. Helicobacter pylori infection induces genetic instability of nuclear and mitochondrial DNA in gastric cells. Clin Cancer Res 2009;15:2995-3002.
29. Touati E, Michel V, Thiberge JM, Wuscher N, Huerre M, Labigne A. Chronic Helicobacter pylori infections induce gastric mutations in mice. Gastroenterology 2003;124:1408-19.
30. Lofgren JL, Whary MT, Ge Z, Muthupalani S, Taylor NS, Mobley M, et al. Lack of commensal flora in Helicobacter pylori-infected INS-GAS mice reduces gastritis and delays intraepithelial neoplasia. Gastroenterology 2011;140:210-20.
31. Lertpiriyapong K, Whary MT, Muthupalani S, Lofgren JL, Gamazon ER, Feng Y, et al. Gastric colonisationwith a restricted commensal microbiota replicates the promotion of neoplastic lesions by diverse intestinal microbiota in the Helicobacter pylori INS-GAS mouse model of gastric carcinogenesis. Gut 2014;63:54-63.
32. Xie FJ, Zhang YP, ZhengQQ, Jin HC, Wang FL, Chen M, et al. Helicobacter pylori infection and esophageal cancer risk: An updated meta-analysis. World J Gastroenterol 2013;19:6098-107.
33. Kostic AD, Gevers D, Pedamallu CS, Michaud M, Duke F, Earl AM, et al. Genomic analysis identifies association of Fusobacteriumwith colorectal carcinoma. Genome Res 2012;22:292-8.
34. McCoy AN, Araujo-Perez F, Azcarate-Peril A, Yeh JJ, Sandler RS, Keku TO. Fusobacterium is associated with colorectal adenomas. PLoS One 2013;8: e53653.
35. Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA, Michaud M, et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 2013;14:207-15.
36. Rubinstein MR, Wang X, Liu W, Hao Y, Cai G, Han YW. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/ beta-catenin signaling via its FadA adhesin. Cell Host Microbe 2013;14:195-206.
37. Abed J, Emgard JE, Zamir G, Faroja M, Almogy G, Grenov A, et al. Fap2 mediates fusobacterium nucleatum colorectal adenocarcinoma enrichment by binding to tumor-expressed Gal-GalNAc. Cell Host Microbe 2016;20:215-25.
38. Pagano JS, Blaser M, Buendia MA, Damania B, Khalili K, Raab-Traub N, et al. Infectious agents and cancer: criteria for a causal relation. Semin Cancer Biol 2004;14:453-71.
39. Weitzman MD, Weitzman JB. What's the damage The impact of pathogens on pathways that maintain host genome integrity. Cell HostMicrobe 2014;15:283-94.
40. Xu W, Liu Z, Bao Q, Qian Z. Viruses, other pathogenic microorganisms and esophageal cancer. Gastrointest Tumors 2015;2:2-13.
41. Liu W, MacDonald M, You J. Merkel cell polyomavirus infection and Merkel cell carcinoma. Curr Opin Virol 2016;20:20-7.
42. Shuda M, Kwun HJ, Feng H, Chang Y, Moore PS. Human Merkel cell polyomavirus small T antigen is an oncoprotein targeting the 4E-BP1 translation regulator. J Clin Invest 2011;121:3623-34.
43. Wu JH, Simonette RA, Nguyen HP, Rady PL, Tyring SK. Merkel cell polyomavirus in Merkel cell carcinogenesis: small T antigen-mediates c-Jun phosphorylation. Virus Genes 2016;52:397-9.
44. Dowd JB, Palermo T, Brite J, McDade TW, Aiello A. Seroprevalence of Epstein-Barr virus infection in U. S. children ages 6-19, 2003-2010. PLoS One 2013;8:e64921.
45. Thorley-Lawson DA, Allday MJ. The curious case of the tumour virus: 50 years of Burkitt's lymphoma. Nat Rev Microbiol 2008;6:913-24.
46. Anderton E, Yee J, Smith P, Crook T, White RE, Allday MJ. Two Epstein-Barr virus (EBV) oncoproteins cooperate to repress expression of the proapoptotic tumour-suppressor Bim: clues to the pathogenesis of Burkitt's lymphoma. Oncogene 2008;27:421-33.
47. Torgbor C, Awuah P, Deitsch K, Kalantari P, Duca KA, Thorley-Lawson DA. A multifactorial role for P. falciparum malaria in endemic Burkitt's lymphoma pathogenesis. PLoS Pathog 2014;10: e1004170.
48. Johansson ME, Phillipson M, Petersson J, Velcich A, Holm L, Hansson GC. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci U S A 2008;105: 15064-9.
49. Kim YS, Ho SB. Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr Gastroenterol Rep 2010;12: 319-30.
50. Salzman NH, Underwood MA, Bevins CL. Paneth cells, defensins, and the commensal microbiota: A hypothesis on intimate interplay at the intestinal mucosa. Semin Immunol 2007;19:70-83.
51. Bergstrom K, Liu X, Zhao Y, Gao N, Wu Q, Song K, et al. Defective intestinal mucin-type O-glycosylation causes spontaneous colitis-associated cancer in mice. Gastroenterology 2016;151:152-64.
52. HollanderD, Vadheim CM, Brettholz E, Petersen GM, Delahunty T, Rotter JI. Increased intestinal permeability in patients with Crohn's disease and their relatives. A possible etiologic factor. Ann Intern Med 1986;105: 883-5.
53. Jess T, Rungoe C, Peyrin-Biroulet L. Risk of colorectal cancer in patients with ulcerative colitis: A meta-analysis of population-based cohort studies. Clin Gastroenterol Hepatol 2012;10:639-45.
54. Peters U, Jiao S, Schumacher FR, Hutter CM, Aragaki AK, Baron JA, et al. Identification of genetic susceptibility Loci for colorectal tumors in a genome-wide meta-analysis. Gastroenterology 2013;144:799-807.
55. Velcich A, Yang W, Heyer J, Fragale A, Nicholas C, Viani S, et al. Colorectal cancer in mice genetically deficient in the mucin Muc2. Science 2002;295:1726-9.
56. Lin JE, Snook AE, Li P, Stoecker BA, Kim GW, Magee MS, et al. GUCY2C opposes systemic genotoxic tumorigenesis by regulating AKT-dependent intestinal barrier integrity. PLoS One 2012;7:e31686.
57. Arthur JC, Perez-Chanona E, Muhlbauer M, Tomkovich S, Uronis JM, Fan TJ, et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 2012;338:120-3.
58. Prindiville TP, Sheikh RA, Cohen SH, Tang YJ, Cantrell MC, Silva J Jr. Bacteroidesfragilis enterotoxin gene sequences in patients with inflammatory bowel disease. Emerg Infect Dis 2000;6:171-4.
59. Boleij A, Hechenbleikner EM, Goodwin AC, Badani R, Stein EM, Lazarev MG, et al. The Bacteroidesfragilis toxin gene is prevalent in the colon mucosa of colorectal cancer patients. Clin Infect Dis 2015;60:208-15.
60. Guidi R, Guerra L, Levi L, Stenerlow B, Fox JG, Josenhans C, et al. Chronic exposure to the cytolethal distending toxins of Gram-negative bacteria promotes genomic instability and altered DNA damage response. Cell Microbiol 2013;15:98-113.
61. Yu LX, Yan HX, Liu Q, Yang W, Wu HP, Dong W, et al. Endotoxin accumulation prevents carcinogen-induced apoptosis and promotes liver tumorigenesis in rodents. Hepatology 2010;52:1322-33.
62. Donohoe DR, Holley D, Collins LB, Montgomery SA, Whitmore AC, Hillhouse A, et al. A gnotobiotic mouse model demonstrates that dietary fiber protects against colorectal tumorigenesis in a microbiota-and butyrate-dependent manner. Cancer Discov 2014;4:1387-97.
63. Lupton JR. Microbial degradation products influence colon cancer risk: The butyrate controversy. J Nutr 2004;134:479-82.
64. Singh N, Gurav A, Sivaprakasam S, Brady E, Padia R, ShiH, et al. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity 2014; 40:128-39.
65. Belcheva A, Irrazabal T, Robertson SJ, Streutker C, Maughan H, Rubino S, et al. Gut microbial metabolismdrives transformation ofMSH2-deficient colon epithelial cells. Cell 2014;158:288-99.
66. Moons LM, Kusters JG, van Delft JH, Kuipers EJ, Gottschalk R, Geldof H, et al. A pro-inflammatory genotype predisposes to Barrett's esophagus. Carcinogenesis 2008;29:926-31.
67. Souza RF, Huo X, Mittal V, Schuler CM, Carmack SW, Zhang HY, et al. Gastroesophageal reflux might cause esophagitis through a cytokinemediated mechanism rather than caustic acid injury. Gastroenterology 2009;137:1776-84.
68. Snider EJ, Freedberg DE, Abrams JA. Potential role of the microbiome in Barrett's Esophagus and esophageal adenocarcinoma. Dig Dis Sci 2016; 61:2217-25.
69. Yang L, Lu X, Nossa CW, Francois F, Peek RM, Pei Z. Inflammation and intestinal metaplasia of the distal esophagus are associated with alterations in the microbiome. Gastroenterology 2009;137:588-97.
70. Gall A, Fero J, McCoy C, Claywell BC, Sanchez CA, Blount PL, et al. Bacterial composition of the human upper gastrointestinal tract microbiome is dynamic and associated with genomic instability in a Barrett's Esophagus Cohort. PLoS One 2015;10:e0129055.
71. Fernandez-Garcia B, Eiro N, Gonzalez-Reyes S, Gonzalez L, Aguirre A, Gonzalez LO, et al. Clinical significance of toll-like receptor 3, 4, and 9 in gastric cancer. J Immunother 2014;37:77-83.
72. Pimentel-Nunes P, Afonso L, Lopes P, Roncon-Albuquerque R Jr, Goncalves N, Henrique R, et al. Increased expression of toll-like receptors (TLR) 2, 4 and 5 in gastric dysplasia. Pathol Oncol Res 2011;17:677-83.
73. Pimentel-Nunes P, Goncalves N, Boal-Carvalho I, Afonso L, Lopes P, Roncon-Albuquerque R Jr, et al. Helicobacter pylori induces increased expression of Toll-like receptors and decreased Toll-interacting protein in gastric mucosa that persists throughout gastric carcinogenesis. Helicobacter 2013;18:22-32.
74. Schmausser B, Andrulis M, Endrich S, Muller-Hermelink HK, EckM. Tolllike receptors TLR4, TLR5 and TLR9 on gastric carcinoma cells: An implication for interaction with Helicobacter pylori. Int J MedMicrobiol 2005;295:179-85.
75. Huhta H, Helminen O, Lehenkari PP, Saarnio J, Karttunen TJ, Kauppila JH. Toll-like receptors 1, 2, 4 and 6 in esophageal epithelium, Barrett's esophagus, dysplasia and adenocarcinoma. Oncotarget 2016;7:23658-67.
76. Kauppila JH, Karttunen TJ, Saarnio J, Nyberg P, Salo T, Graves DE, et al. Short DNA sequences and bacterial DNA induce esophageal, gastric, and colorectal cancer cell invasion. APMIS 2013;121:511-22.
77. Castellarin M, Warren RL, Freeman JD, Dreolini L, Krzywinski M, Strauss J, et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res 2012;22:299-306.
78. Gur C, Ibrahim Y, Isaacson B, Yamin R, Abed J, Gamliel M, et al. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity 2015;42:344-55.
79. Warren RL, Freeman DJ, Pleasance S, Watson P, Moore RA, Cochrane K, et al. Co-occurrence of anaerobic bacteria in colorectal carcinomas. Microbiome 2013;1:16.
80. Zackular JP, Rogers MA, Ruffin MTt, Schloss PD. The human gut microbiome as a Screening tool for colorectal cancer. Cancer Prev Res (Phila) 2014;7:1112-21.
81. Zeller G, Tap J, Voigt AY, Sunagawa S, Kultima JR, Costea PI, et al. Potential of fecal microbiota for early-stage detection of colorectal cancer. Mol Syst Biol 2014;10:766.
82. Schmidt BL, Kuczynski J, Bhattacharya A, Huey B, Corby PM, Queiroz EL, et al. Changes in abundance of oral microbiota associated with oral cancer. PLoS One 2014;9:e98741.
83. Kado S, Uchida K, Funabashi H, Iwata S, Nagata Y, Ando M, et al. Intestinal microflora are necessary for development of spontaneous adenocarcinoma of the large intestine in T-cell receptor beta chain and p53 doubleknockout mice. Cancer Res 2001;61:2395-8.
84. Li Y, Kundu P, Seow SW, de Matos CT, Aronsson L, Chin KC, et al. Gut microbiota accelerate tumor growth via c-jun and STAT3 phosphorylation in APCMin/ mice. Carcinogenesis 2012;33:1231-8.
85. Tanaka T, Kohno H, Suzuki R, Yamada Y, Sugie S, Mori H. A novel inflammation-related mouse colon carcinogenesis model induced by azoxymethane and dextran sodium sulfate. Cancer Sci 2003;94: 965-73.
86. Zackular JP, Baxter NT, Iverson KD, Sadler WD, Petrosino JF, Chen GY, et al. The gutmicrobiome modulates colon tumorigenesis. mBio 2013;4: e00692-13.
87. Thaiss CA, Zmora N, Levy M, Elinav E. The microbiome and innate immunity. Nature 2016;535:65-74.
88. Honda K, Littman DR. The microbiota in adaptive immune homeostasis and disease. Nature 2016;535:75-84.
89. Tamburini S, Shen N, Wu HC, Clemente JC. The microbiome in early life: implications for health outcomes. Nat Med 2016;22:713-22.
90. Kayama H, Takeda K. Functions of innate immune cells and commensal bacteria in gut homeostasis. J Biochem 2016;159:141-9.
91. Levy M, Thaiss CA, Elinav E. Metabolites: messengers between the microbiota and the immune system. Genes Dev 2016;30:1589-97.
92. Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 2013;342: 967-70.
93. Hamm AK, Weir TL. Editorial on "Cancer and the microbiota" published in Science. Ann Transl Med 2015;3:175.
94. Karin M, Jobin C, Balkwill F. Chemotherapy, immunity and microbiota-a new triumvirate Nat Med 2014;20:126-7.
95. Galluzzi L, Pietrocola F, Bravo-San Pedro JM, Amaravadi RK, Baehrecke EH, Cecconi F, et al. Autophagy in malignant transformation and cancer progression. EMBO J 2015;34:856-80.
96. Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol 2013;13:722-37.
97. Huang J, Brumell JH. Bacteria-autophagy interplay: A battle for survival. Nat Rev Microbiol 2014;12:101-14.
98. Greenfield LK, Jones NL. Modulation of autophagy by Helicobacter pylori and its role in gastric carcinogenesis. Trends Microbiol 2013; 21:602-12.
99. Levy J, Cacheux W, Bara MA, L'Hermitte A, Lepage P, Fraudeau M, et al. Intestinal inhibition of Atg7 prevents tumour initiation through amicrobiome-influenced immune response and suppresses tumour growth. Nat Cell Biol 2015;17:1062-73.
100. Rajagopala SV, Yooseph S, Harkins DM, Moncera KJ, Zabokrtsky KB, Torralba MG, et al. Gastrointestinal microbial populations can distinguish pediatric and adolescent Acute Lymphoblastic Leukemia (ALL) at the time of disease diagnosis. BMC Genomics 2016;17:635.