The role of the microbiota in inflammation, carcinogenesis, and cancer therapy

European Journal of Immunology

Volumn 45, Issue 1, 2015, Pages 17-31

  Dzutsev, Amiran ^a,b   Goldszmid, Romina S ^a   Viaud, Sophie ^c,d   Zitvogel, Laurence ^c,d   Trinchieri, Giorgio ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^c INSERM   (France)

^d UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Cancer; Cancer therapy; Cancerogenesis; Inflammation; Microbiota

Indexed keywords

ADAPTIVE IMMUNITY; ARTICLE; AUTOIMMUNITY; CANCER GROWTH; CANCER RESISTANCE; CANCER SUSCEPTIBILITY; CANCER THERAPY; CARCINOGENESIS; COMMENSAL; DYSBIOSIS; ENTERITIS; GENETIC ASSOCIATION; HUMAN; IMMUNE EVASION; IMMUNOMODULATION; INNATE IMMUNITY; INTESTINE FLORA; MALIGNANT NEOPLASTIC DISEASE; MEMBRANE PERMEABILITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; ANIMAL; AUTOIMMUNE DISEASES; EVOLUTION; IMMUNOLOGY; INFLAMMATION; METAGENOME; MICROBIOLOGY; MICROFLORA; MOUSE; NEOPLASMS; PATHOLOGY; SYMBIOSIS; TUMOR ESCAPE;

ANTINEOPLASTIC AGENT;

ADAPTIVE IMMUNITY; ANIMALS; ANTINEOPLASTIC AGENTS; AUTOIMMUNE DISEASES; BIOLOGICAL EVOLUTION; CARCINOGENESIS; HUMANS; IMMUNITY, INNATE; IMMUNOMODULATION; INFLAMMATION; METAGENOME; MICE; MICROBIOTA; NEOPLASMS; SYMBIOSIS; TUMOR ESCAPE;

EID: 84920973141     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201444972     Document Type: Article

References (185)

1. McInerney, J. O., O'Connell, M. J. and Pisani, D., The hybrid nature of the eukaryota and a consilient view of life on Earth. Nat. Rev. Microbiol. 2014. 12: 449-455.
2. McFall-Ngai, M., Hadfield, M. G., Bosch, T. C., Carey, H. V., Domazet-Loso, T., Douglas, A. E., Dubilier, N. et al., Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl. Acad. Sci. USA 2013. 110: 3229-3236.
3. Turnbaugh, P. J., Ley, R. E., Hamady, M., Fraser-Liggett, C. M., Knight, R. and Gordon, J. I., The human microbiome project. Nature 2007. 449: 804-810.
4. Maynard, C. L., Elson, C. O., Hatton, R. D. and Weaver, C. T., Reciprocal interactions of the intestinal microbiota and immune system. Nature 2012. 489: 231-241.
5. Costello, E. K., Stagaman, K., Dethlefsen, L., Bohannan, B. J. and Relman, D. A., The application of ecological theory toward an understanding of the human microbiome. Science 2012. 336: 1255-1262.
6. Bosch, T. C. and McFall-Ngai, M. J., Metaorganisms as the new frontier. Zoology (Jena) 2011. 114: 185-190.
7. Zhang, Q., Zmasek, C. M., Cai, X. and Godzik, A., TIR domain-containing adaptor SARM is a late addition to the ongoing microbe-host dialog. Dev. Comp. Immunol. 2011. 35: 461-468.
8. Lange, C., Hemmrich, G., Klostermeier, U. C., Lopez-Quintero, J. A., Miller, D. J., Rahn, T., Weiss, Y. et al., Defining the origins of the NOD-like receptor system at the base of animal evolution. Mol. Biol. Evol. 2011. 28: 1687-1702.
9. Chu, H. and Mazmanian, S. K., Innate immune recognition of the microbiota promotes host-microbial symbiosis. Nat. Immunol. 2013. 14: 668-675.
10. Kremer, N., Philipp, E. E., Carpentier, M. C., Brennan, C. A., Kraemer, L., Altura, M. A., Augustin, R. et al., Initial symbiont contact orchestrates host-organ-wide transcriptional changes that prime tissue colonization. Cell Host Microbe 2013. 14: 183-194.
11. Hansen, C. H., Nielsen, D. S., Kverka, M., Zakostelska, Z., Klimesova, K., Hudcovic, T., Tlaskalova-Hogenova, H. et al., Patterns of early gut colonization shape future immune responses of the host. PLoS ONE 2012. 7: e34043.
12. Stappenbeck, T. S., Hooper, L. V. and Gordon, J. I., Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc. Natl. Acad. Sci. USA 2002. 99: 15451-15455.
13. Yutin, N., Wolf, M. Y., Wolf, Y. I. and Koonin, E. V., The origins of phagocytosis and eukaryogenesis. Biol. Direct 2009. 4: 9.
14. Underhill, D. M. and Goodridge, H. S., Information processing during phagocytosis. Nat. Rev. Immunol. 2012. 12: 492-502.
15. Tauber, A. I., Metchnikoff and the phagocytosis theory. Nat. Rev. Mol. Cell Biol. 2003. 4: 897-901.
16. Murray, P. J., Allen, J. E., Biswas, S. K., Fisher, E. A., Gilroy, D. W., Goerdt, S., Gordon, S. et al., Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 2014. 41: 14-20.
17. Mukherji, A., Kobiita, A., Ye, T. and Chambon, P., Homeostasis in intestinal epithelium is orchestrated by the circadian clock and microbiota cues transduced by TLRs. Cell 2013. 153: 812-827.
18. Nguyen, K. D., Fentress, S. J., Qiu, Y., Yun, K., Cox, J. S. and Chawla, A., Circadian gene Bmal1 regulates diurnal oscillations of Ly6C(hi) inflammatory monocytes. Science 2013. 341: 1483-1488.
19. Khosravi, A., Yanez, A., Price, J. G., Chow, A., Merad, M., Goodridge, H. S. and Mazmanian, S. K., Gut microbiota promote hematopoiesis to control bacterial infection. Cell Host Microbe 2014. 15: 374-381.
20. Ganal, S. C., Sanos, S. L., Kallfass, C., Oberle, K., Johner, C., Kirschning, C., Lienenklaus, S. et al., Priming of natural killer cells by nonmucosal mononuclear phagocytes requires instructive signals from commensal microbiota. Immunity 2012. 37: 171-186.
21. Abt, M. C., Osborne, L. C., Monticelli, L. A., Doering, T. A., Alenghat, T., Sonnenberg, G. F., Paley, M. A. et al., Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity 2012. 37: 158-170.
22. Iida, N., Dzutsev, A., Stewart, C. A., Smith, L., Bouladoux, N., Weingarten, R. A., Molina, D. A. et al., Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 2013. 342: 967-970.
23. Kuhn, K. A. and Stappenbeck, T. S., Peripheral education of the immune system by the colonic microbiota. Semin. Immunol. 2013. 25: 364-369.
24. Hooper, D. C., Molowitz, E. H., Bos, N. A., Ploplis, V. A. and Cebra, J. J., Spleen cells from antigen-minimized mice are superior to spleen cells from germ-free and conventional mice in the stimulation of primary in vitro proliferative responses to nominal antigens. Eur. J. Immunol. 1995. 25: 212-217.
25. Ichinohe, T., Pang, I. K., Kumamoto, Y., Peaper, D. R., Ho, J. H., Murray, T. S. and Iwasaki, A., Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc. Natl. Acad. Sci. USA 2011. 108: 5354-5359.
26. Mittrucker, H. W., Seidel, D., Bland, P. W., Zarzycka, A., Kaufmann, S. H., Visekruna, A. and Steinhoff, U., Lack of microbiota reduces innate responses and enhances adaptive immunity against Listeria monocytogenes infection. Eur. J. Immunol. 2014. 44: 1710-1715.
27. Chow, J. and Mazmanian, S. K., A pathobiont of the microbiota balances host colonization and intestinal inflammation. Cell Host Microbe 2010. 7: 265-276.
28. Kamada, N., Kim, Y. G., Sham, H. P., Vallance, B. A., Puente, J. L., Martens, E. C. and Nunez, G., Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science 2012. 336: 1325-1329.
29. Kamada, N., Chen, G. Y., Inohara, N. and Nunez, G., Control of pathogens and pathobionts by the gut microbiota. Nat. Immunol. 2013. 14: 685-690.
30. Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K. and Knight, R., Diversity, stability and resilience of the human gut microbiota. Nature 2012. 489: 220-230.
31. Underwood, M. A., Intestinal dysbiosis: novel mechanisms by which gut microbes trigger and prevent disease. Prev. Med. 2014. 65: 133-137.
32. Frank, D. N., St Amand, A. L., Feldman, R. A., Boedeker, E. C., Harpaz, N. and Pace, N. R., Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA 2007. 104: 13780-13785.
33. Serbina, N. V., Jia, T., Hohl, T. M. and Pamer, E. G., Monocyte-mediated defense against microbial pathogens. Annu. Rev. Immunol. 2008. 26: 421-452.
34. Ege, M. J., Mayer, M., Normand, A. C., Genuneit, J., Cookson, W. O., Braun-Fahrlander, C., Heederik, D. et al., Exposure to environmental microorganisms and childhood asthma. N. Engl. J. Med. 2011. 364: 701-709.
35. Lopez-Serrano, P., Perez-Calle, J. L., Perez-Fernandez, M. T., Fernandez-Font, J. M., Boixeda de Miguel, D. and Fernandez-Rodriguez, C. M., Environmental risk factors in inflammatory bowel diseases. Investigating the hygiene hypothesis: a Spanish case-control study. Scand. J. Gastroenterol. 2010. 45: 1464-1471.
36. Olszak, T., An, D., Zeissig, S., Vera, M. P., Richter, J., Franke, A., Glickman, J. N. et al., Microbial exposure during early life has persistent effects on natural killer T cell function. Science 2012. 336: 489-493.
37. Belkaid, Y. and Hand, T. W., Role of the microbiota in immunity and inflammation. Cell 2014. 157: 121-141.
38. Round, J. L. and Mazmanian, S. K., Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc. Natl. Acad. Sci. USA 2010. 107: 12204-12209.
39. Larsson, E., Tremaroli, V., Lee, Y. S., Koren, O., Nookaew, I., Fricker, A., Nielsen, J. et al., Analysis of gut microbial regulation of host gene expression along the length of the gut and regulation of gut microbial ecology through MyD88. Gut 2012. 61: 1124-1131.
40. Vaishnava, S., Behrendt, C. L., Ismail, A. S., Eckmann, L. and Hooper, L. V., Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc. Natl. Acad. Sci. USA 2008. 105: 20858-20863.
41. Kim, Y. G., Udayanga, K. G., Totsuka, N., Weinberg, J. B., Nunez, G. and Shibuya, A., Gut dysbiosis promotes M2 macrophage polarization and allergic airway inflammation via fungi-induced PGE(2). Cell Host Microbe 2014. 15: 95-102.
42. Young, G. R., Eksmond, U., Salcedo, R., Alexopoulou, L., Stoye, J. P. and Kassiotis, G., Resurrection of endogenous retroviruses in antibody-deficient mice. Nature 2012. 491: 774-778.
43. Mangeney, M., Pothlichet, J., Renard, M., Ducos, B. and Heidmann, T., Endogenous retrovirus expression is required for murine melanoma tumor growth in vivo. Cancer Res. 2005. 65: 2588-2591.
44. Singh, N., Gurav, A., Sivaprakasam, S., Brady, E., Padia, R., Shi, H., Thangaraju, M. et al., Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity 2014. 40: 128-139.
45. Kalina, U., Koyama, N., Hosoda, T., Nuernberger, H., Sato, K., Hoelzer, D., Herweck, F. et al., Enhanced production of IL-18 in butyrate-treated intestinal epithelium by stimulation of the proximal promoter region. Eur. J. Immunol. 2002. 32: 2635-2643.
46. Smith, P. M., Howitt, M. R., Panikov, N., Michaud, M., Gallini, C. A., Bohlooly, Y. M., Glickman, J. N. et al., The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013. 341: 569-573.
47. Mazmanian, S. K., Round, J. L. and Kasper, D. L., A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 2008. 453: 620-625.
48. Talham, G. L., Jiang, H. Q., Bos, N. A. and Cebra, J. J., Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system. Infect. Immun. 1999. 67: 1992-2000.
49. Gaboriau-Routhiau, V., Rakotobe, S., Lecuyer, E., Mulder, I., Lan, A., Bridonneau, C., Rochet, V. et al., The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 2009. 31: 677-689.
50. Ivanov, II, Atarashi, K., Manel, N., Brodie, E. L. and Shima, T., Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009. 139: 485-498.
51. Garland, C. D., Lee, A. and Dickson, M. R., Segmented filamentous bacteria in the rodent small intestine: their colonization of growing animals and possible role in host resistance to Salmonella. Microb. Ecol. 1982. 8: 181-190.
52. Grice, E. A., Kong, H. H., Conlan, S., Deming, C. B., Davis, J., Young, A. C., Bouffard, G. G. et al., Topographical and temporal diversity of the human skin microbiome. Science 2009. 324: 1190-1192.
53. Naik, S., Bouladoux, N., Wilhelm, C., Molloy, M. J., Salcedo, R., Kastenmuller, W., Deming, C. et al., Compartmentalized control of skin immunity by resident commensals. Science 2012. 337: 1115-1119.
54. Avila, M., Ojcius, D. M. and Yilmaz, O., The oral microbiota: living with a permanent guest. DNA Cell Biol. 2009. 28: 405-411.
55. Hajishengallis, G., Liang, S., Payne, M. A., Hashim, A., Jotwani, R., Eskan, M. A., McIntosh, M. L. et al., Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe 2011. 10: 497-506.
56. Hajishengallis, G. and Lamont, R. J., Breaking bad: manipulation of the host response by Porphyromonas gingivalis. Eur. J. Immunol. 2014. 44: 328-338.
57. Belkaid, Y. and Naik, S., Compartmentalized and systemic control of tissue immunity by commensals. Nat. Immunol. 2013. 14: 646-653.
58. Archambaud, C., Sismeiro, O., Toedling, J., Soubigou, G., Becavin, C., Lechat, P., Lebreton, A. et al., The intestinal microbiota interferes with the microRNA response upon oral Listeria infection. mBio 2013. 4: e00707-e00713.
59. Chervonsky, A. V., Microbiota and autoimmunity. Cold Spring Harb. Perspect. Biol. 2013. 5: a007294.
60. Lee, Y. K., Menezes, J. S., Umesaki, Y. and Mazmanian, S. K., Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA 2011. 108(Suppl 1): 4615-4622.
61. Wu, H. J., Ivanov, II, Darce, J., Hattori, K., Shima, T., Umesaki, Y., Littman, D. R. et al., Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 2010. 32: 815-827.
62. Viaud, S., Saccheri, F., Mignot, G., Yamazaki, T., Daillere, R., Hannani, D., Enot, D. P. et al., The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science 2013. 342: 971-976.
63. Human_Microbiome_Project_Consortium, Structure, function and diversity of the healthy human microbiome. Nature 2012. 486: 207-214.
64. Ding, T. and Schloss, P. D., Dynamics and associations of microbial community types across the human body. Nature 2014. 509: 357-360.
65. Menard, S., Cerf-Bensussan, N. and Heyman, M., Multiple facets of intestinal permeability and epithelial handling of dietary antigens. Mucosal Immunol. 2010. 3: 247-259.
66. Mortha, A., Chudnovskiy, A., Hashimoto, D., Bogunovic, M., Spencer, S. P., Belkaid, Y. and Merad, M., Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 2014. 343: 1249288.
67. Wanke, I., Skabytska, Y., Kraft, B., Peschel, A., Biedermann, T. and Schittek, B., Staphylococcus aureus skin colonization is promoted by barrier disruption and leads to local inflammation. Exp. Dermatol. 2013. 22: 153-155.
68. Hahn, B. L. and Sohnle, P. G., Direct translocation of staphylococci from the skin surface to deep organs. Microb. Pathog. 2013. 63: 24-29.
69. Venkatesh, M., Mukherjee, S., Wang, H., Li, H., Sun, K., Benechet, A. P., Qiu, Z. et al., Symbiotic bacterial metabolites regulate gastrointestinal barrier function via the xenobiotic sensor PXR and Toll-like receptor 4. Immunity 2014. 41: 296-310.
70. Shen, W., Li, W., Hixon, J. A., Bouladoux, N., Belkaid, Y., Dzutzev, A. and Durum, S. K., Adaptive immunity to murine skin commensals. Proc. Natl. Acad. Sci. USA 2014. 111: E2977-E2986.
71. Brusca, S. B., Abramson, S. B. and Scher, J. U., Microbiome and mucosal inflammation as extra-articular triggers for rheumatoid arthritis and autoimmunity. Curr. Opin. Rheumatol. 2014. 26: 101-107.
72. Klaasen, H. L., Koopman, J. P., Van den Brink, M. E., Bakker, M. H., Poelma, F. G. and Beynen, A. C., Intestinal, segmented, filamentous bacteria in a wide range of vertebrate species. Lab. Anim. 1993. 27: 141-150.
73. Snel, J., Heinen, P. P., Blok, H. J., Carman, R. J., Duncan, A. J., Allen, P. C. and Collins, M. D., Comparison of 16S rRNA sequences of segmented filamentous bacteria isolated from mice, rats, and chickens and proposal of "Candidatus Arthromitus". Int. J. Syst. Bacteriol. 1995. 45: 780-782.
74. Yin, Y., Wang, Y., Zhu, L., Liu, W., Liao, N., Jiang, M., Zhu, B. et al., Comparative analysis of the distribution of segmented filamentous bacteria in humans, mice and chickens. ISME J. 2013. 7: 615-621.
75. Jonsson, H., Segmented filamentous bacteria in human ileostomy samples after high-fiber intake. FEMS Microbiol. Lett. 2013. 342: 24-29.
76. Kanther, M., Tomkovich, S., Xiaolun, S., Grosser, M. R., Koo, J., Flynn, E. J., 3rd, Jobin, C. et al., Commensal microbiota stimulate systemic neutrophil migration through induction of Serum amyloid A. Cell. Microbiol. 2013. 16: 1053-1067.
77. Karmarkar, D. and Rock, K. L., Microbiota signalling through MyD88 is necessary for a systemic neutrophilic inflammatory response. Immunology 2013. 140: 483-492.
78. Hanahan, D. and Weinberg, R. A., The hallmarks of cancer. Cell 2000. 100: 57-70.
79. Vogelstein, B., Papadopoulos, N., Velculescu, V. E., Zhou, S., Diaz, L. A., Jr. and Kinzler, K. W., Cancer genome landscapes. Science 2013. 339: 1546-1558.
80. Schetter, A. J., Heegaard, N. H. and Harris, C. C., Inflammation and cancer: interweaving microRNA, free radical, cytokine and p53 pathways. Carcinogenesis 2010. 31: 37-49.
81. Trinchieri, G., Cancer and inflammation: an old intuition with rapidly evolving new concepts. Annu. Rev. Immunol. 2012. 30: 677-706.
82. Schreiber, R. D., Old, L. J. and Smyth, M. J., Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011. 331: 1565-1570.
83. Galon, J., Angell, H. K., Bedognetti, D. and Marincola, F. M., The continuum of cancer immunosurveillance: prognostic, predictive, and mechanistic signatures. Immunity 2013. 39: 11-26.
84. Wall, B. M., Dmochowski, R. R., Malecha, M., Mangold, T., Bobal, M. A. and Cooke, C. R., Inducible nitric oxide synthase in the bladder of spinal cord injured patients with a chronic indwelling urinary catheter. J. Urol. 2001. 165: 1457-1461.
85. Ameille, J., Brochard, P., Letourneux, M., Paris, C. and Pairon, J. C., Asbestos-related cancer risk in patients with asbestosis or pleural plaques. Rev. Mal. Respir. 2011. 28: e11-e17.
86. Rebours, V., Boutron-Ruault, M. C., Jooste, V., Bouvier, A. M., Hammel, P., Ruszniewski, P. and Levy, P., Mortality rate and risk factors in patients with hereditary pancreatitis: uni- and multidimensional analyses. Am. J. Gastroenterol. 2009. 104: 2312-2317.
87. Hussain, S. P., Hofseth, L. J. and Harris, C. C., Radical causes of cancer. Nat. Rev. Cancer 2003. 3: 276-285.
88. Phillips, L. L., Effect of free radicals on chromosomes of barley. Science 1956. 124: 889-890.
89. Wiseman, H. and Halliwell, B., Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochem. J. 1996. 313(Pt 1): 17-29.
90. Ruffell, B., Affara, N. I. and Coussens, L. M., Differential macrophage programming in the tumor microenvironment. Trends Immunol. 2012. 33: 119-126.
91. Qian, B. Z. and Pollard, J. W., Macrophage diversity enhances tumor progression and metastasis. Cell 2010. 141: 39-51.
92. Yan, H. H., Pickup, M., Pang, Y., Gorska, A. E., Li, Z., Chytil, A., Geng, Y. et al., Gr-1+CD11b +myeloid cells tip the balance of immune protection to tumor promotion in the premetastatic lung. Cancer Res. 2010. 70: 6139-6149.
93. Andreu, P., Johansson, M., Affara, N. I., Pucci, F., Tan, T., Junankar, S., Korets, L. et al., FcRgamma activation regulates inflammation-associated squamous carcinogenesis. Cancer Cell 2010. 17: 121-134.
94. DeNardo, D. G., Barreto, J. B., Andreu, P., Vasquez, L., Tawfik, D., Kolhatkar, N. and Coussens, L. M., CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 2009. 16: 91-102.
95. Borrello, M. G., Degl'Innocenti, D. and Pierotti, M. A., Inflammation and cancer: the oncogene-driven connection. Cancer Lett. 2008. 267: 262-270.
96. Cataisson, C., Salcedo, R., Hakim, S., Moffitt, B. A., Wright, L., Yi, M., Stephens, R. et al., IL-1R-MyD88 signaling in keratinocyte transformation and carcinogenesis. J. Exp. Med. 2012. 209: 1689-1702.
97. Tchkonia, T., Zhu, Y., van Deursen, J., Campisi, J. and Kirkland, J. L., Cellular senescence and the senescent secretory phenotype: therapeutic opportunities. J. Clin. Invest. 2013. 123: 966-972.
98. Vizioli, M. G., Possik, P. A., Tarantino, E., Meissl, K., Borrello, M. G., Miranda, C., Anania, M. C. et al., Evidence of oncogene-induced senescence in thyroid carcinogenesis. Endocr. Relat. Cancer 2011. 18: 743-757.
99. Ling, J., Kang, Y., Zhao, R., Xia, Q., Lee, D. F., Chang, Z., Li, J. et al., KrasG12D-induced IKK2/beta/NF-kappaB activation by IL-1alpha and p62 feed forward loops is required for development of pancreatic ductal adenocarcinoma. Cancer Cell 2012. 21: 105-120.
100. Franklin, R. A., Liao, W., Sarkar, A., Kim, M. V., Bivona, M. R., Liu, K., Pamer, E. G. et al., The cellular and molecular origin of tumor-associated macrophages. Science 2014. 344: 921-925.
101. Solinas, G., Germano, G., Mantovani, A. and Allavena, P., Tumor-associated macrophages (TAM) as major players of the cancer-related inflammation. J. Leukoc. Biol. 2009. 86: 1065-1073.
102. Sica, A. and Bronte, V., Altered macrophage differentiation and immune dysfunction in tumor development. J. Clin. Invest. 2007. 117: 1155-1166.
103. Grivennikov, S. I., Greten, F. R. and Karin, M., Immunity, inflammation, and cancer. Cell 2010. 140: 883-899.
104. Gabrilovich, D. I., Ostrand-Rosenberg, S. and Bronte, V., Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 2012. 12: 253-268.
105. Stewart, C. A., Metheny, H., Iida, N., Smith, L., Hanson, M., Steinhagen, F., Leighty, R. M. et al., Interferon-dependent IL-10 production by Tregs limits tumor Th17 inflammation. J. Clin. Invest. 2013. 123: 4859-4874.
106. Pang, Y., Gara, S. K., Achyut, B. R., Li, Z., Yan, H. H., Day, C. P., Weiss, J. M. et al., TGF-beta signaling in myeloid cells is required for tumor metastasis. Cancer Discov. 2013. 3: 936-951.
107. Brahmer, J. R. and Pardoll, D. M., Immune checkpoint inhibitors: making immunotherapy a reality for the treatment of lung cancer. Cancer Immunol. Res. 2013. 1: 85-91.
108. Hanahan, D. and Weinberg, R. A., Hallmarks of cancer: the next generation. Cell 2011. 144: 646-674.
109. de Martel, C., Ferlay, J., Franceschi, S., Vignat, J., Bray, F., Forman, D. and Plummer, M., Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol. 2012. 13: 607-615.
110. Zhang, X., Zhang, Z., Zheng, B., He, Z., Winberg, G. and Ernberg, I., An update on viral association of human cancers. Arch. Virol. 2013. 158: 1433-1443.
111. Ng, J. and Wu, J., Hepatitis B- and hepatitis C-related hepatocellular carcinomas in the United States: similarities and differences. Hepat. Mon. 2012. 12: e7635.
112. Psyrri, A., Rampias, T. and Vermorken, J. B., The current and future impact of human papillomavirus on treatment of squamous cell carcinoma of the head and neck. Ann. Oncol. 2014. 25: 2101-2115.
113. Tommasino, M., The human papillomavirus family and its role in carcinogenesis. Semin. Cancer Biol. 2014. 26: 13-21.
114. Ciminale, V., Rende, F., Bertazzoni, U. and Romanelli, M. G., HTLV-1 and HTLV-2: highly similar viruses with distinct oncogenic properties. Front Microbiol. 2014. 5: 398.
115. Fenizia, C., Fiocchi, M., Jones, K., Parks, R. W., Ceribelli, M., Chevalier, S. A., Edwards, D. et al., Human T-cell leukemia/lymphoma virus type 1 p30, but not p12/p8, counteracts Toll-like receptor 3 (TLR3) and TLR4 signaling in human monocytes and dendritic cells. J. Virol. 2014. 88: 393-402.
116. Schowalter, R. M., Pastrana, D. V., Pumphrey, K. A., Moyer, A. L. and Buck, C. B., Merkel cell polyomavirus and two previously unknown polyomaviruses are chronically shed from human skin. Cell Host Microbe 2010. 7: 509-515.
117. Wieland, U., Silling, S., Scola, N., Potthoff, A., Gambichler, T., Brockmeyer, N. H., Pfister, H. et al., Merkel cell polyomavirus infection in HIV-positive men. Arch. Dermatol. 2011. 147: 401-406.
118. Zheng, Z. M., Viral oncogenes, noncoding RNAs, and RNA splicing in human tumor viruses. Int. J. Biol. Sci. 2010. 6: 730-755.
119. Castle, P. E., Hillier, S. L., Rabe, L. K., Hildesheim, A., Herrero, R., Bratti, M. C., Sherman, M. E. et al., An association of cervical inflammation with high-grade cervical neoplasia in women infected with oncogenic human papillomavirus (HPV). Cancer Epidemiol. Biomarkers Prev. 2001. 10: 1021-1027.
120. Koshiol, J., Sklavos, M., Wentzensen, N., Kemp, T., Schiffman, M., Dunn, S. T., Wang, S. S. et al., Evaluation of a multiplex panel of immune-related markers in cervical secretions: a methodologic study. Int. J. Cancer 2014. 134: 411-425.
121. Rehermann, B. and Nascimbeni, M., Immunology of hepatitis B virus and hepatitis C virus infection. Nat. Rev. Immunol. 2005. 5: 215-229.
122. Wieland, S., Thimme, R., Purcell, R. H. and Chisari, F. V., Genomic analysis of the host response to hepatitis B virus infection. Proc. Natl. Acad. Sci. USA 2004. 101: 6669-6674.
123. Foy, E., Li, K., Wang, C., Sumpter, R., Jr., Ikeda, M., Lemon, S. M. and Gale, M., Jr., Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science 2003. 300: 1145-1148.
124. Taylor, D. R., Shi, S. T., Romano, P. R., Barber, G. N. and Lai, M. M., Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science 1999. 285: 107-110.
125. Ferrari, C., Penna, A., Bertoletti, A., Valli, A., Antoni, A. D., Giuberti, T., Cavalli, A. et al., Cellular immune response to hepatitis B virus-encoded antigens in acute and chronic hepatitis B virus infection. J. Immunol. 1990. 145: 3442-3449.
126. Chen, Y., Chen, Z., Guo, R., Chen, N., Lu, H., Huang, S., Wang, J. and Li, L., Correlation between gastrointestinal fungi and varying degrees of chronic hepatitis B virus infection. Diagn. Microbiol. Infect. Dis. 2011. 70: 492-498.
127. Xu, M., Wang, B., Fu, Y., Chen, Y., Yang, F., Lu, H., Xu, J. and Li, L., Changes of fecal Bifidobacterium species in adult patients with hepatitis B virus-induced chronic liver disease. Microb. Ecol. 2012. 63: 304-313.
128. Henao-Mejia, J., Elinav, E., Thaiss, C. A., Licona-Limon, P. and Flavell, R. A., Role of the intestinal microbiome in liver disease. J. Autoimmun. 2013. 46: 66-73.
129. Moore, P. S. and Chang, Y., Why do viruses cause cancer? Highlights of the first century of human tumour virology. Nat. Rev. Cancer 2010. 10: 878-889.
130. Dolberg, D. S., Hollingsworth, R., Hertle, M. and Bissell, M. J., Wounding and its role in RSV-mediated tumor formation. Science 1985. 230: 676-678.
131. Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7-14 June 1994. IARC Monogr. Eval. Carcinog. Risks Hum. 1994. 61: 1-241.
132. Kim, D. J., Park, J. H., Franchi, L., Backert, S. and Nunez, G., The Cag pathogenicity island and interaction between TLR2/NOD2 and NLRP3 regulate IL-1beta production in Helicobacter pylori infected dendritic cells. Eur. J. Immunol. 2013. 43: 2650-2658.
133. Peek, R. M., Jr. and Blaser, M. J., Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat. Rev. Cancer 2002. 2: 28-37.
134. Hongyo, T., Buzard, G. S., Palli, D., Weghorst, C. M., Amorosi, A., Galli, M., Caporaso, N. E. et al., Mutations of the K-ras and p53 genes in gastric adenocarcinomas from a high-incidence region around Florence, Italy. Cancer Res. 1995. 55: 2665-2672.
135. Maesawa, C., Tamura, G., Suzuki, Y., Ogasawara, S., Sakata, K., Kashiwaba, M. and Satodate, R., The sequential accumulation of genetic alterations characteristic of the colorectal adenoma-carcinoma sequence does not occur between gastric adenoma and adenocarcinoma. J. Pathol. 1995. 176: 249-258.
136. Karnes, W. E., Jr., Samloff, I. M., Siurala, M., Kekki, M., Sipponen, P., Kim, S. W. and Walsh, J. H., Positive serum antibody and negative tissue staining for Helicobacter pylori in subjects with atrophic body gastritis. Gastroenterology 1991. 101: 167-174.
137. Plottel, C. S. and Blaser, M. J., Microbiome and malignancy. Cell Host Microbe 2011. 10: 324-335.
138. Goldszmid, R. S. and Trinchieri, G., The price of immunity. Nat. Immunol. 2012. 13: 932-938.
139. Jobin, C., Colorectal cancer: CRC-all about microbial products and barrier function? Nat. Rev. Gastroenterol. Hepatol. 2012. 9: 694-696.
140. Rao, V. P., Poutahidis, T., Ge, Z., Nambiar, P. R., Boussahmain, C., Wang, Y. Y., Horwitz, B. H. et al., Innate immune inflammatory response against enteric bacteria Helicobacter hepaticus induces mammary adenocarcinoma in mice. Cancer Res. 2006. 66: 7395-7400.
141. Salcedo, R., Worschech, A., Cardone, M., Jones, Y., Gyulai, Z., Dai, R. M., Wang, E. et al., MyD88-mediated signaling prevents development of adenocarcinomas of the colon: role of interleukin 18. J. Exp. Med. 2010. 207: 1625-1636.
142. Allen, I. C., TeKippe, E. M., Woodford, R. M., Uronis, J. M., Holl, E. K., Rogers, A. B., Herfarth, H. H. et al., The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitis-associated cancer. J. Exp. Med. 2010. 207: 1045-1056.
143. Elinav, E., Strowig, T., Kau, A. L., Henao-Mejia, J., Thaiss, C. A., Booth, C. J., Peaper, D. R. et al., NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 2011. 145: 745-757.
144. Huber, S., Gagliani, N., Zenewicz, L. A., Huber, F. J., Bosurgi, L., Hu, B., Hedl, M. et al., IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine. Nature 2012. 491: 259-263.
145. Kirchberger, S., Royston, D. J., Boulard, O., Thornton, E., Franchini, F., Szabady, R. L., Harrison, O. et al., Innate lymphoid cells sustain colon cancer through production of interleukin-22 in a mouse model. J. Exp. Med. 2013. 210: 917-931.
146. Salcedo, R., Cataisson, C., Hasan, U., Yuspa, S. H. and Trinchieri, G., MyD88 and its divergent toll in carcinogenesis. Trends Immunol. 2013. 34: 379-389.
147. Saleh, M. and Trinchieri, G., Innate immune mechanisms of colitis and colitis-associated colorectal cancer. Nat. Rev. Immunol. 2011. 11: 9-20.
148. Wlodarska, M., Thaiss, C. A., Nowarski, R., Henao-Mejia, J., Zhang, J. P., Brown, E. M., Frankel, G. et al., NLRP6 inflammasome orchestrates the colonic host-microbial interface by regulating goblet cell mucus secretion. Cell 2014. 156: 1045-1059.
149. Sears, C. L. and Garrett, W. S., Microbes, microbiota, and colon cancer. Cell Host Microbe 2014. 15: 317-328.
150. Kostic, A. D., Chun, E., Robertson, L., Glickman, J. N., Gallini, C. A., Michaud, M., Clancy, T. E. et al., Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 2013. 14: 207-215.
151. Rubinstein, M. R., Wang, X., Liu, W., Hao, Y., Cai, G. and Han, Y. W., Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/beta-catenin signaling via its FadA adhesin. Cell Host Microbe 2013. 14: 195-206.
152. Zackular, J. P., Baxter, N. T., Iverson, K. D., Sadler, W. D., Petrosino, J. F., Chen, G. Y. and Schloss, P. D., The gut microbiome modulates colon tumorigenesis. mBio 2013. 4: e00692-e00713.
153. Mira-Pascual, L., Cabrera-Rubio, R., Ocon, S., Costales, P., Parra, A., Suarez, A., Moris, F. et al., Microbial mucosal colonic shifts associated with the development of colorectal cancer reveal the presence of different bacterial and archaeal biomarkers. J. Gastroenterol. 2014. DOI: 10.1007/s00535-014-0963-x.
154. Grivennikov, S. I., Wang, K., Mucida, D., Stewart, C. A., Schnabl, B., Jauch, D., Taniguchi, K. et al., Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature 2012. 491: 254-258.
155. Bongers, G., Pacer, M. E., Geraldino, T. H., Chen, L., He, Z., Hashimoto, D., Furtado, G. C. et al., Interplay of host microbiota, genetic perturbations, and inflammation promotes local development of intestinal neoplasms in mice. J. Exp. Med. 2014. 211: 457-472.
156. Vannucci, L., Stepankova, R., Kozakova, H., Fiserova, A., Rossmann, P. and Tlaskalova-Hogenova, H., Colorectal carcinogenesis in germ-free and conventionally reared rats: different intestinal environments affect the systemic immunity. Int. J. Oncol. 2008. 32: 609-617.
157. Zhan, Y., Chen, P. J., Sadler, W. D., Wang, F., Poe, S., Nunez, G., Eaton, K. A. et al., Gut microbiota protects against gastrointestinal tumorigenesis caused by epithelial injury. Cancer Res. 2013. 73: 7199-7210.
158. Maddocks, O. D., Short, A. J., Donnenberg, M. S., Bader, S. and Harrison, D. J., Attaching and effacing Escherichia coli downregulate DNA mismatch repair protein in vitro and are associated with colorectal adenocarcinomas in humans. PLoS ONE 2009. 4: e5517.
159. Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S. and Medzhitov, R., Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell 2004. 118: 229-241.
160. Nagamine, C. M., Sohn, J. J., Rickman, B. H., Rogers, A. B., Fox, J. G. and Schauer, D. B., Helicobacter hepaticus infection promotes colon tumorigenesis in the BALB/c-Rag2(-/-) Apc(Min/+) mouse. Infect. Immun. 2008. 76: 2758-2766.
161. Poutahidis, T., Cappelle, K., Levkovich, T., Lee, C. W., Doulberis, M., Ge, Z., Fox, J. G. et al., Pathogenic intestinal bacteria enhance prostate cancer development via systemic activation of immune cells in mice. PLoS ONE 2013. 8: e73933.
162. Fox, J. G., Feng, Y., Theve, E. J., Raczynski, A. R., Fiala, J. L., Doernte, A. L., Williams, M. et al., Gut microbes define liver cancer risk in mice exposed to chemical and viral transgenic hepatocarcinogens. Gut 2010. 59: 88-97.
163. Erdman, S. E., Poutahidis, T., Tomczak, M., Rogers, A. B., Cormier, K., Plank, B., Horwitz, B. H. et al., CD4+ CD25+ regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice. Am. J. Pathol. 2003. 162: 691-702.
164. Yamamoto, M. L., Maier, I., Dang, A. T., Berry, D., Liu, J., Ruegger, P. M., Yang, J. I. et al., Intestinal bacteria modify lymphoma incidence and latency by affecting systemic inflammatory state, oxidative stress, and leukocyte genotoxicity. Cancer Res. 2013. 73: 4222-4232.
165. Westbrook, A. M., Wei, B., Hacke, K., Xia, M., Braun, J. and Schiestl, R. H., The role of tumour necrosis factor-alpha and tumour necrosis factor receptor signalling in inflammation-associated systemic genotoxicity. Mutagenesis 2012. 27: 77-86.
166. Sergentanis, T. N., Zagouri, F. and Zografos, G. C., Is antibiotic use a risk factor for breast cancer? A meta-analysis. Pharmacoepidemiol. Drug Saf. 2010. 19: 1101-1107.
167. Guiducci, C., Vicari, A. P., Sangaletti, S., Trinchieri, G. and Colombo, M. P., Redirecting in vivo elicited tumor infiltrating macrophages and dendritic cells towards tumor rejection. Cancer Res. 2005. 65: 3437-3446.
168. Siddik, Z. H., Cisplatin: mode of cytotoxic action and molecular basis of resistance. Oncogene 2003. 22: 7265-7279.
169. Apetoh, L., Ghiringhelli, F., Tesniere, A., Obeid, M., Ortiz, C., Criollo, A., Mignot, G. et al., Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat. Med. 2007. 13: 1050-1059.
170. Martins, I., Kepp, O., Schlemmer, F., Adjemian, S., Tailler, M., Shen, S., Michaud, M. et al., Restoration of the immunogenicity of cisplatin-induced cancer cell death by endoplasmic reticulum stress. Oncogene 2011. 30: 1147-1158.
171. Laurent, A., Nicco, C., Chereau, C., Goulvestre, C., Alexandre, J., Alves, A., Levy, E. et al., Controlling tumor growth by modulating endogenous production of reactive oxygen species. Cancer Res. 2005. 65: 948-956.
172. Ozben, T., Oxidative stress and apoptosis: impact on cancer therapy. J. Pharm. Sci. 2007. 96: 2181-2196.
173. Zwielehner, J., Lassl, C., Hippe, B., Pointner, A., Switzeny, O. J., Remely, M., Kitzweger, E. et al., Changes in human fecal microbiota due to chemotherapy analyzed by TaqMan-PCR, 454 sequencing and PCR-DGGE fingerprinting. PLoS ONE 2011. 6: e28654.
174. Yang, J., Liu, K. X., Qu, J. M. and Wang, X. D., The changes induced by cyclophosphamide in intestinal barrier and microflora in mice. Eur. J. Pharmacol. 2013. 714: 120-124.
175. Paulos, C. M., Wrzesinski, C., Kaiser, A., Hinrichs, C. S., Chieppa, M., Cassard, L., Palmer, D. C. et al., Microbial translocation augments the function of adoptively transferred self/tumor-specific CD8+ T cells via TLR4 signaling. J. Clin. Invest. 2007. 117: 2197-2204.
176. Dudley, M. E., Yang, J. C., Sherry, R., Hughes, M. S., Royal, R., Kammula, U., Robbins, P. F. et al., Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. J. Clin. Oncol. 2008. 26: 5233-5239.
177. Viaud, S., Flament, C., Zoubir, M., Pautier, P., LeCesne, A., Ribrag, V., Soria, J. C. et al., Cyclophosphamide induces differentiation of Th17 cells in cancer patients. Cancer Res. 2011. 71: 661-665.
178. Kroemer, G., Galluzzi, L., Kepp, O. and Zitvogel, L., Immunogenic cell death in cancer therapy. Annu. Rev. Immunol. 2013. 31: 51-72.
179. Belcheva, A., Irrazabal, T., Robertson, S. J., Streutker, C., Maughan, H., Rubino, S., Moriyama, E. H. et al., Gut microbial metabolism drives transformation of msh2-deficient colon epithelial cells. Cell 2014. 158: 288-299.
180. Elangovan, S., Pathania, R., Ramachandran, S., Ananth, S., Padia, R. N., Lan, L., Singh, N. et al., The niacin/butyrate receptor GPR109A suppresses mammary tumorigenesis by inhibiting cell survival. Cancer Res. 2014. 74: 1166-1178.
181. Ursell, L. K., Van Treuren, W., Metcalf, J. L., Pirrung, M., Gewirtz, A. and Knight, R., Replenishing our defensive microbes. Bioessays 2013. 35: 810-817.
182. van Nood, E., Vrieze, A., Nieuwdorp, M., Fuentes, S., Zoetendal, E. G., de Vos, W. M., Visser, C. E. et al., Duodenal infusion of donor feces for recurrent Clostridium difficile. N. Engl. J. Med. 2013. 368: 407-415.
183. Vrieze, A., Van Nood, E., Holleman, F., Salojarvi, J., Kootte, R. S., Bartelsman, J. F., Dallinga-Thie, G. M. et al., Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 2012. 143: 913-916.e7.
184. Allegretti, J. R. and Hamilton, M. J., Restoring the gut microbiome for the treatment of inflammatory bowel diseases. World J. Gastroenterol. 2014. 20: 3468-3474.
185. Pamer, E. G., Fecal microbiota transplantation: effectiveness, complexities, and lingering concerns. Mucosal Immunol. 2014. 7: 210-214.