Colorectal carcinoma: Importance of colonic environment for anti-cancer response and systemic immunity

Journal of Immunotoxicology

Volumn 6, Issue 4, 2009, Pages 217-226

  Vannucci, Luca ^a   Stepankova, Renata ^a   Grobarova, Valeria ^a   Kozakova, Hana ^a   Rossmann, Pavel ^a   Klimesova, Klara ^a   Benson, Veronika ^a   Sima, Petr ^a   Fiserova, Anna ^a   Tlaskalova Hogenova, Helena ^a  

^a INSTITUTE OF MICROBIOLOGY   (Czech Republic)

Author keywords

Colorectal cancer; Germ free animals; Gut microbiota; Mucosal immunity; Natural killer cells; Tolerance

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 6; PREBIOTIC AGENT; PROBIOTIC AGENT; STAT3 PROTEIN; TOLL LIKE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA;

ACHLORHYDRIA; ANTINEOPLASTIC ACTIVITY; B LYMPHOCYTE; BACTERIAL COLONIZATION; BACTERIAL FLORA; BACTERIAL STRAIN; BACTERIUM; BACTEROIDES THETAIOTAOMICRON; BIFIDOBACTERIUM LONGUM; CARCINOGENESIS; CELL ACTIVITY; COLON FLORA; COLORECTAL CARCINOMA; COMMENSAL; CYTOTOXICITY; DENDRITIC CELL; ESCHERICHIA COLI; EUBACTERIUM; GENE INDUCTION; GERMFREE ANIMAL; GNOTOBIOTICS; HELICOBACTER PYLORI; HOMEOSTASIS; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; INCIDENCE; INFLAMMATION; INNATE IMMUNITY; INTESTINE FLORA; INTESTINE LYMPHATIC TISSUE; LACTIC ACID BACTERIUM; LACTOBACILLUS; LAMINA PROPRIA; LYMPHOCYTE SUBPOPULATION; MESENTERY LYMPH NODE; MUCOSAL IMMUNITY; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; STOMACH ACID SECRETION; STOMACH CANCER; TH2 CELL; TUMOR IMMUNITY;

ADENOCARCINOMA; ANIMALS; COLON; COLORECTAL NEOPLASMS; DISEASE MODELS, ANIMAL; GERM-FREE LIFE; HUMANS; IMMUNE TOLERANCE; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; KILLER CELLS, NATURAL; MICE; RATS; RECEPTOR CROSS-TALK;

ANIMALIA; BACTERIA (MICROORGANISMS);

EID: 70450218687     PISSN: 1547691X     EISSN: 1547691X     Source Type: Journal    
DOI: 10.3109/15476910903334343     Document Type: Review

References (102)

1. Abdulkareem, F. B., Abudu, E. K., Awolola, N. A., Elesh,a S. O., Rotimi, O., Akinde, O. R., Atoyebi, A. O., Adesanya, A. A., Daramola, A. O., Banjo, A. A., and Anunobi, C. C. 2008. Colorectal carcinoma in Lagos and Sagamu, Southwest Nigeria: A histopathological review. World J. Gastroenterol. 14:6531-6535.
2. Amith, S. R., Jayanth, P., Franchuk, S., Siddiqui, S., Seyrantepe, V., Gee, K., Basta, S., Beyaert, R., Pshezhetsky, A. V., and Szewczuk, M. R. 2009. Dependence of pathogen molecule-induced Toll-like receptor activation and cell function on Neu1 sialidase. Glycoconj. J. [Epub ahead of print].
3. Asonuma, S., Imatani, A., Asano, N., Oikawa, T., Konishi, H., Iijima, K., Koike, T., Ohara, S., and Shimosegawa, T. 2009. Helicobacter pylori induces gastric mucosal intestinal metaplasia through the inhibition of interleukin-4-mediated HMG box protein Sox2 expression. Am. J. Physiol. 297:G312-G322.
4. Atherton, J. C. 1998. Helicobacter pylori virulence factors. Br. Med. Bull. 54:105-120.
5. Baba, N., Samson, S., Bourdet-Sicard, R., Rubio, M., and Sarfati, M. 2008. Commensal bacteria trigger a full dendritic cell maturation program that promotes the expansion of non-Tr1 suppressor T-cells. J. Leukocyte Biol. 84:468-476.
6. Balkwill, F., and Mantovani, A. 2001. Inflammation and cancer: Back to Virchow? Lancet 357:539-545.
7. Bilsborough, J., and Viney, J. L. 2004. Gastrointestinal dendritic cells play a role in immunity, tolerance, and disease. Gastroenterology 127:300-309.
8. Blennerhassett, M. G., Vignjevic, P., Vermillion, D. L., and Collins, S. M. 1992. Inflammation causes hyperplasia and hypertrophy in smooth muscle of rat small intestine. Am. J. Physiol. 262:G1041-1046.
9. Blennerhassett, M. G., Bovell, F. M., Lourenssen, S., and McHugh, K. M. 1999. Characteristics of inflammation-induced hypertrophy of rat intestinal smooth muscle cell. Dig. Dis. Sci. 44:1265-1272.
10. Borrello, M. G., Degl'Innocenti, D., and Pierotti, M. A. 2008. Inflammation and cancer: The oncogene-driven connection. Cancer Lett. 267:262-270.
11. Boudry, G., Peron, V., Le Huerou-Luron, I., Lalles, J. P., and Seve, B. 2004. Weaning induces both transient and long-lasting modifications of absorptive, secretory, and barrier properties of piglet intestine. J. Nutr. 134:2256-2262.
12. Bromberg, J., and Wang, T. C. 2009. Inflammation and cancer: IL-6 and STAT3 complete the link. Cancer Cell. 15:79-80.
13. Cario, E., and Podolsky, D. K. 2005. Intestinal epithelial TOLLerance versus inTOLLerance of commensals. Mol. Immunol. 42:887-893.
14. Cebra, J. J., Jiang, H. Q., Boiko, N., and Tlaskalova-Hogenova, H. 2005. The role of mucosal microbiota in the development, maintenance, and pathologies of the mucosal immune system. In: Mucosal Immunology. 3rd Edition (Mestecky, J., Bienenstock, J., Lamm, M. E., Mayer, L., McGhee, J. R., and Strober, W., Eds), Amsterdam: Elsevier/Academic Press, pp. 335-368.
15. Chiappara, G., Gagliardo, R., Siena, A., Bonsignore, M. R., Bousquet, J., Bonsignore, G., and Vignola, A. M. 2001. Airway remodeling in the pathogenesis of asthma. Curr. Opin. Allergy Clin. Immunol. 1:85-93.
16. Choi, S. S., Kim, Y., Han, K. S., You, S., Oh, S., and Kim, S. H. 2006. Effects of Lactobacillus strains on cancer cell proliferation and oxidative stress in vitro. Lett. Appl. Microbiol. 42:452-458.
17. Christensen, H. R., Froekiaer, H., and Pestka, J. J. 2002. Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J. Immunol. 168:171-178.
18. Cinchi, F., Cortesini, C., Fantappie, O., Messerini, L., Sardi, I., Lasagna, N., Perna, F., Fabbroni, V., Di Felice, A., Perigli, G., Mazzanti, R., and Masini, E. 2004. Cycoloygenase-2 activation mediates the pro-angiogenic effect of nitric oxide in colorectal cancer. Clin. Cancer Res. 10:2694-2704.
19. Dubois, B., Goubier, A., Joubert, G., and Kaiserlian, D. 2005. Oral tolerance and regulation of mucosal immunity. Cell. Mol. Life Sci. 62:1322-1332.
20. Fanaro, S., Chierici, R., Guerrini, P., and Vigi, V. 2003. Intestinal microflora in early infancy: Composition and development. Acta Paediatr. Suppl. 91:48-55.
21. Ferlay, J., Autier, P., Boniol, M., Heanue, M., Colombat, M. and Boyle P., 2006. Estimates of cancer incidence and mortality in Europe in 2006. Ann. Oncol. 18:581--592.
22. Forchielli, M. L., and Walker, W. A. 2005. The role of gut-associated lymphoid tissues and mucosal defence. Br. J. Nutr. 93(S1):41-48.
23. Fort, M. M., Leach, M. W., and Rennick, D. M. 1998. A role for NK cells as regulators of CD4+ T-cells in a transfer model of colitis. J. Immunol. 161:3256-3261.
24. Gallucci, S., and Matzinger, P. 2001. Danger signals: SOS to the immune system. Curr. Opin. Immunol. 13:114-119.
25. Goodrich, M. E., and McGee, D. W. 1998. Regulation of mucosal B-cell immunoglobulin secretion by intestinal epithelial cell-derived cytokines. Cytokine 10:948-955.
26. Gordon, H. A., and Pesti, L. 1971. The gnotobiotic animal as a tool in the study of host-microbial relationships. Bacteriol. Rev. 35:390-429.
27. Guarner, F., and Malagelada, J. R. 2003. Gut flora in health and disease. Lancet 361:512-519.
28. Hambly, R. J., Rumney, C. J., Cunninghame, M., Fletcher, J. M., Rijken, P. J., and Rowland, I. R. 1997. Influence of diets containing high and low risk factors for colon cancer on early stages of carcinogenesis in human floraassociated (HFA) rats. Carcinogenesis 18:1535-1539.
29. Hanada, T, and Yoshimura, A. 2002. Regulation of cytokine signaling and inflammation. Cytokine Growth Factor Rev. 13:413-421.
30. Handelsman, J. 2004. Metagenomics: Application of genomics to uncultured microorganisms. Microbiol. Mol. Biol. Rev. 68:669-685.
31. Heavey, P. M., and Rowland, I. R. 2004. Microbial-gut interactions in health and disease. Gastrointestinal cancer. Best Practice Res. Clin. Gastroenterol. 18:323-e36.
32. Hewitson, P., Glasziou, P., Irwig, L., Towler, B., and Watson, E. 2007. Screening for colorectal cancer using the fecal occult blood test, Hemoccult. Cochrane Database System. Rev. (1):CD001216.
33. Hope, M. E., Hold, G. L., Kain, R., and El-Omar, E. M. 2005. Sporadic colorectal cancer-role of the commensal microbiota. FEMS Microbiol. Lett. 244:1-7.
34. Hord, N. G. 2008. Eukaryotic-microbiota cross-talk: Potential mechanisms for health benefits of prebiotics and probiotics. Annu. Rev. Nutr. 28:215-231.
35. Horie, H., Kanazawa, K., Okada, M., Narushima, S., Itoh, K., and Terada, A. 1999. Effects of intestinal bacteria on the development of colonic neoplasm: An experimental study. Eur. J. Cancer Prev. 8:237-245.
36. Hrncir, T., Stepankova, R., Kozakova, H., Hudcovic, T., and Tlaskalova-Hogenova, H. 2008. Gut microbiota and lipopolysaccharide content of the diet influence development of regulatory T-cells: Studies in germfree mice. BMC Immunol. 6;9:65.
37. IARC (International Agency for Research on Cancer). 1997. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Volume 61. Schistosomes, Liver Flukes and Helicobacter pylori. Geneva: World Health Organization.
38. Kelly, D., Conway, S., and Aminov, R. 2005. Commensal gut bacteria: Mechanisms of immune modulation. Trends Immunol. 26:326-333.
39. Kikuchi, S., Wada, O., Nakajaima, T., Nishi, T., Kobayashi, O., Konishi, T., and Inaba, Y. 1995. Serum anti-Helicobacter pylori antibody and gastric carcinoma among young adults. Research group on prevention of gastric carcinoma among young adults. Cancer 75:2789-2793.
40. Kinross, J. M., von Roon, A. C., Holmes, E., Darzi, A., and Nicholson, J. K. 2008. The human gut microbiome: implications for future health care. Curr. Gastroenterol. Rep. 10:396-403.
41. Koizumi, S., Wakita, D., Sato, T., Mitamura, R., Izumo, T., Shibata, H., Kiso, Y., Chamoto, K., Togashi, Y., Kitamura, H., and Nishimura, T. 2008. Essential role of Toll-like receptors for dendritic cell and NK1.1+ cell-dependent activation of Type 1 immunity by Lactobacillus pentosus strain S-PT84. Immunol. Lett. 120:14-19.
42. Kuper, H., Adami, H. O., and Tricopoulos, D. 2000. Infections as a major preventable cause of human cancer. J. Intern. Med. 248:171-183.
43. Lin, W.W., and Karin, M. 2007. A cytokine-mediated link between innate immunity, inflammation, and cancer. J. Clin. Invest. 117:1175-1183.
44. Liu, X., Conner, H., Kobayashi, T., Abe, S., Fang, Q., Wen, F. Q., and Rennard, S. I. 2003. Synergetic effect of interleukin-4 and transforming growth factor- β1 on type I collagen gel contraction and degradation by HFL-1 cells: Implication in tissue remodeling. Chest 123(S3):427S-428S.
45. McGarr, S. E., Ridlon, J. M., and Hylemon, P. B. 2005. Diet, anaerobic bacterial metabolism, and colon cancer: A review of the literature. J. Clin. Gastroenterol. 39:98-109.
46. Macpherson, A.J., and Harris, N. L. 2004. Opinion: Interactions between commensal intestinal bacteria and the immune system. Nat. Rev. Immunol. 4:478-485.
47. Macpherson, A. J., and Uhr, T. 2004. Compartmentalization of the mucosal immune responses to commensal intestinal bacteria. Ann. N.Y. Acad. Sci. 1029:36-43.
48. Macpherson, A. J., Geuking, M. B., and McCoy, K. D. 2005. Immune responses that adapt the intestinal mucosa to commensal intestinal bacteria. Immunology 115: 153-162.
49. Makita, S., Kanai, T., Nemoto, Y., Totsuka, T., Okamoto, R., Tsuchiya, K., Yamamoto, M., Kimono, H., and Watanabe M. 2007. Intestinal lamina propria retaining CD4+CD25+ regulatory T-cells is a suppressive site of intestinal inflammation. J. Immunol. 178:4937-4946.
50. Mantovani, A., Allavena, P., Sica, A., and Balkwill, F. 2008. Cancer-related inflammation. Nature 454:436-444.
51. Mastromarino, A., Reddy, B. S., and Wynder, E. L. 1976. Metabolic epidemiology of colon cancer: Enzymic activity of fecal flora. Am. J. Clin. Nutr. 29:1455-1460.
52. Moss, S. F. 1999. The carcinogenic effect of H. pylori on the gastric epithelial cell. J. Physiol. Pharmacol. 50:847-856.
53. Mowat, A. M. 2003. Anatomical basis of tolerance and immunity to intestinal antigens. Nat. Rev. Immunol. 3:331-341.
54. Nicklin, S., and Miller, K. 1983. Local and systemic immune responses to intestinally-presented antigen. Int. Arch. Allergy Appl. Immunol. 72:87-90.
55. Nieuwenhuis, E. E., Matsumoto, T., Lindenbergh, D., Willemsen, R., Kaser, A., Simons-Oosterhuis, Y., Brugman, S., Yamaguchi, K., Ishikawa, H., Aiba, Y., Koga, Y., Samsom, J. N., Oshima, K.,Kikuchi, M., Escher, J. C., Hattori, M., Onderdonk, A. B., and Blumberg, R. S. 2009. Cd1d-dependent regulation of bacterial colonization in the intestine of mice. J. Clin. Invest. 119:1241-1250.
56. Ogawa, T., Asai, Y., Tamai, R., Makimura, Y., Sakamoto, H., Hashikawa, S., and Yasuda, K. 2006. Natural killer cell activities of synbiotic Lactobacillus casei ssp. casei in conjunction with dextran. Clin. Exp. Immunol. 143:103-109.
57. Olaya, J., Neopikhanov, V., and Uribe, A. 1999. Lipopolysaccharide of Escherichia coli, polyamines, and acetic acid stimulate cell proliferation in intestinal epithelial cells. In Vitro Cell. Dev. Biol. Anim. 35:43-48.
58. Onoue, M., Kado, S., Sakaitani, Y., Uchida, K., and Morotomi, M. 1997. Specific species of intestinal bacteria influence the induction of aberrant crypt foci by 1,2-dimethylhydrazine in rats. Cancer Lett. 113:179-186.
59. Potter, J. D. 1995. Risk factors for colon neoplasia - epidemiology and biology. Eur. J. Cancer 31A:1033--1038.
60. Prescott, S. L., and Holt, P. G. 1998. Abnormalities in cord blood mononuclear cytokine production as a predictor of later atopic disease in childhood. Clin. Exp. Allergy 28:1313-1316.
61. Rao, C. V., Hirose, Y., Indranie, C., and Reddy, B. S. 2001. Modulation of experimental colon tumorigenesis by types and amounts of dietary fatty acids. Cancer Res. 61:1927-1933.
62. Reddy, B. S., Narisawa, T., Maronpot, R., Weisburger, J. H., and Wynder, E. L. 1975. Animal models for the study of dietary factors and cancer of the large bowel. Cancer Res. 35:3421-3426.
63. Reddy, B. S., Narisawa, T., Wright, P., Vukusich, D., Weisburger, J. H., and Wynder, E. L. 1975. Colon carcinogenesis with azoxymethane and dimethylhydrazine in germ-free rats. Cancer Res. 35:287-290.
64. Reddy, B. S., Narisawa, T., and Weisburger, J. H. 1976. Colon carcinogenesis in germ-free rats with intra-rectal 1,2-dimethylhydrazine and subcutaneous azoxymethane. Cancer Res. 36:2874-2876.
65. Reddy, B. S., Sharma, C., Darby, L., Laakso, K., and Wynder, E. L. 1980. Metabolic epidemiology of large bowel cancer. Fecal mutagens in highand low-risk population for colon cancer. A preliminary report. Mutat. Res. 72:511-522.
66. Reddy, B. S., and Ohmori, T. 1981. Effect of intestinal microflora and dietary fat on 3,2′-dimethyl-4-aminobiphenyl-induced colon carcinogenesis in F344 rats. Cancer Res. 41:1363-1367.
67. Rohrmann, S., Hermann, S., and Linseisen, J. 2009. Heterocyclic aromatic amine intake increases colorectal adenoma risk: Findings from a prospective European cohort study. Am. J. Clin. Nutr. 89:1418-1424.
68. Roller, M., Pietro Femia, A., Caderni, G., Rechkemmer, G., and Watzl, B. 2004. Intestinal immunity of rats with colon cancer is modulated by oligofructose-enriched inulin combined with Lactobacillus rhamnosus and Bifidobacterium lactis. Br. J. Nutr. 92:931-938. (Pubitemid 40028854)
69. Rowland, I. R. 2009. The role of the gastrointestinal microbiota in colorectal cancer. Curr. Pharm. Des. 15:1524-1527.
70. Rumney, C. J., Rowland, I. R., Coutts, T. M., Randerath, K., Reddy, R., Shah, A. B., Ellul, A., and O'Neill, I. K. 1993. Effects of risk-associated human dietary macrocomponents on processes related to carcinogenesis in human flora-associated (HFA) rats. Carcinogenesis 14:79-84.
71. Sacksteder, M. R. 1976. Occurrence of spontaneous tumors in the germ-free F344 rat. J. Natl. Cancer Inst. 57:1371-1373.
72. Samavati, L., Rastogi, R., Du, W., Hüttemann, M., Fite, A., and Franchi, L. 2009. STAT3 tyrosine phosphorylation is critical for interleukin-1β and interleukin-6 production in response to lipopolysaccharide and live bacteria. Mol. Immunol. 46:1867-1877.
73. Slattery, M. L., Wolff, R. K., Herrick, J. S., Caan, B. J., and Potter, J. D. 2007. IL-6 genotypes and colon and rectal cancer. Cancer Causes Control 18:1095-1105.
74. Smith, K., McCoy, K. D., and Macpherson, A. J. 2007. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin. Immunol. 19:59-69.
75. Smythies, L. E., Maheshwari, A., Clements, R., Eckhoff, D., Novak, L., Vu, H. L., Mosteller-Barnum, L. M., Sellers, M., and Smith, P. D. 2006. Mucosal IL-8 and TGF? recruit blood monocytes: Evidence for cross-talk between the lamina propria stroma and myeloid cells. J. Leukocyte Biol. 80:492-499.
76. Steinman, R. M., Hawiger, D., and Nussenzweig, M. C. 2003. Tolerogenic dendritic cells. Annu. Rev. Immunol. 21:685-711.
77. Stepankova, R. 1997. Rearing germ-free rats, mice, and rabbits. In: Immunology Methods Manual, Vol.3. Gnotobiologic Models (Lefkovits, I., Tlaskalova, H., and Sterzl, J., Eds). New York: Academy Press, pp. 1537-1542.
78. Stepankova, R., Sinkora, J., Hudcovic, T., Kozakova, H., and Tlaskalova-Hogenova, H. 1998. Differences in development of lymphocyte subpopulations from gut-associated lymphatic tissue (GALT) of germfree and conventional rats: effect of aging. Folia Microbiol (Praha) 43:531-534.
79. Sung, J. J., Lau, J. Y., Goh, K. L., Leung, W. K., and the Asia Pacific Working Group on Colorectal Cancer. 2005. Increasing incidence of colorectal cancer in Asia: Implications for screening. Lancet Oncol. 6:871-876.
80. Swidsinski, A., Khilkin, M., Kerjaschki, D., Schreiber, S., Ortner, M., Weber, J., and Lochs, H. 1998. Association between intraepithelial Escherichia coli and colorectal cancer. Gastroenterology 115:281-286.
81. Takahashi, S., Kawamura, T., Kanda, Y., Taniguchi, T., Nishizawa, T., Iiai, T., Hatakeyama, K., and Abo, T. 2006. Activation of CD1d-independent NK1.1+ T-cells in the large intestine by Lactobacilli. Immunol. Lett. 102:74-78.
82. Tannock, G. W. 2007. What immunologists should know about bacterial communities of the human bowel. Sem.Immunol. 19:94-105.
83. Tezuka, H., Abe, Y., Iwata, M., Takeuchi, H., Ishikawa, H., Matsushita, M., Shiohara, T., Akira, S., and Ohteki, T. 2007. Regulation of IgA production by naturally-occurring TNF-/iNOS-producing dendritic cells. Nature 448:929-933.
84. Tlaskalova-Hogenova, H., Sterzl, J., Stepankova, R., Dlabac, V., Vetvicka, V., Rossmann, P., Mandel, L., and Rejnek, J. 1983. Development of immunological capacity under germfree and conventional conditions. Ann. N.Y. Acad. Sci. 409:96-113.
85. Tlaskalova-Hogenova H. 1997. Gnotobiology as a tool - An introduction. In: Immunology Methods Manual, Vol.3. Gnotobiologic Models (Lefkovits, I., Tlaskalova, H., and Sterzl, J., Eds). New York: Academic Press, pp. 1524-1529.
86. Tlaskalova-Hogenova, H., Stepankova, R., Hudcovic, T., Tuckova, L., Cukrowska, B., Lodinova-Zadnikova, R., Kozakova, H., Rossmann, P., Bartova, J., Sokol, D., Funda, D. P., Borovska, D., Rehakova, Z., Sinkora, J., Hofman, J., Drastich, P., and Kokesova, A. 2004. Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases. Immunol. Lett. 93:97-108.
87. Trexler, P. C. 1978. A rationale for the development of gnotobiotics. Lab. Anim. 12:257-262.
88. Tuohy K. M., Gougoulias C., Shen Q., Walton G., Fava F., and Ramnani P. 2009. Studying the human gut microbiota in the trans-omics era - focus on metagenomics and metabonomics. Curr. Pharm. Des. 15:1415-1427.
89. Umesaki, Y., and Setoyama, H. 2000. Structure of the intestinal flora responsible for development of the gut immune system in a rodent model. Microb. Infect. 2:1343-1351.
90. Vannucci, L., Fiserova, A., Horvath, O., Rossmann, P., Mosca, F., and Pospisil, M. 2004. Cancer evolution and immunity in a rat colorectal carcinogenesis model. Int. J. Oncol. 25:973-981.
91. Vannucci, L., Stepankova, R., Kozakova, H., Fiserova, A., Rossmann, P., and Tlaskalova-Hogenova H. 2008. Colorectal carcinogenesis in germ-free and conventionally-reared rats: Different intestinal environments affect the systemic immunity. Int. J. Oncol. 32:609-617.
92. Venturi, M., Hambly, R. J., Glinghammar, B., Rafter, J. J., and Rowland, I. R. 1997. Genotoxic activity in human fecal water and the role of bile acids: A study using the alkaline comet assay. Carcinogenesis 18:2353-2359.
93. Wang, X., and Huycke, M. M. 2007. Extracellular superoxide production by Enterococcus faecalis promotes chromosomal instability in mammalian cells. Gastroenterology 132:551-561.
94. Wang, X., Allen, T. D., May, R. J., Lightfoot, S., Houchen, C. W., and Huycke, M. M. 2008. Enterococcus faecalis induces aneuploidy and tetraploidy in colonic epithelial cells through a bystander effect. Cancer Res. 68:9909-9917.
95. Watzl, B., Girrbach, S., and Roller M. 2005. Inulin, oligofructose, and immunomodulation. Br. J. Nutr. 93(S1):S49-S55.
96. Wedeima, W. F., Deschner, E. E., Cohen, B. I., and DeCosse, J. J. 1985. Acute effects of dietary cholic acid and methylazoxymethanol acetate on colon epithelial cell proliferation; Metabolism of bile salts and neutral sterols in conventional and germ-free SD rats. J. Natl. Cancer Inst. 74:665-670.
97. Williams, A. M., Probert, C. S., Stepankova, R., Tlaskalova-Hogenova, H., Phillips, A., and Bland, P. W. 2006. Effects of microflora on the neonatal development of gut mucosal T-cells and myeloid cells in the mouse. Immunology 119:470-478.
98. Wilks, M. 2007. Bacteria and early human development. Early Hum. Dev. 83:165-170.
99. Woof, J. M., and Mestecky, J. 2005. Mucosal immunoglobulins. Immunol. Rev. 206:64-82.
100. Woolverton, C. J., Holt, L. C., Mitchell, D., and Sartor, R. B. 1992. Identification and characterization of rat intestinal lamina propria cells: Consequences of microbial colonization. Vet. Immunol. Immunopathol. 34:127-138.
101. Wu, M. S., Lin, J. T., Hsu, P. N., Lin, C. Y., Hsieh, Y. T., Chiu, Y. H., Hsueh, P. R., and Liao, K. W. 2007. Preferential induction of transforming growth factor-beta production in gastric epithelial cells and monocytes by Helicobacter pylori soluble proteins. J. Infect. Dis. 196:1386-1393.
102. Yu, L, Wang, L, and Chen, S. 2009. Toll-like receptors, inflammation and tumor in the human female reproductive tract. Am. J. Reprod. Immunol. 62:1-8.