Gavage of Fecal Samples From Patients With Colorectal Cancer Promotes Intestinal Carcinogenesis in Germ-Free and Conventional Mice

Gastroenterology

Volumn 153, Issue 6, 2017, Pages 1621-1633.e6

  Wong, Sunny H ^a   Zhao, Liuyang ^a   Zhang, Xiang ^a   Nakatsu, Geicho ^a   Han, Juqiang ^a,b   Xu, Weiqi ^a   Xiao, Xue ^a   Kwong, Thomas N Y ^a   Tsoi, Ho ^a   Wu, William K K ^a   Zeng, Benhua ^c   Chan, Francis K L ^a   Sung, Joseph J Y ^a   Wei, Hong ^c   Yu, Jun ^a  

^a CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^b CHINESE PLA GENERAL HOSPITAL   (China)

^c THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Carcinogenesis; Colon Cancer; Germ Free; Stool Transplantation

Indexed keywords

CHEMOKINE RECEPTOR CCR1; CHEMOKINE RECEPTOR CCR2; GAMMA INTERFERON; INTERLEUKIN 17; KI 67 ANTIGEN; RNA 16S; TOLL LIKE RECEPTOR 5; AUTACOID; AZOXYMETHANE;

ADULT; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CHINA; COHORT ANALYSIS; COLON CELL; COLORECTAL CANCER; COLORECTAL CARCINOGENESIS; CONTROLLED STUDY; DYSPLASIA; FECES MICROFLORA; FEEDING; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; GENE SEQUENCE; GERMFREE MOUSE; HIGH GRADE DYSPLASIA; HONG KONG; HUMAN; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INTESTINE TISSUE; MALE; METAGENOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; TH1 CELL; TH17 CELL; UPREGULATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CASE CONTROL STUDY; CELL TRANSFORMATION; CHEMICALLY INDUCED; COLON; COLON POLYP; COLORECTAL TUMOR; DISEASE MODEL; FECES; GENE EXPRESSION REGULATION; GERMFREE ANIMAL; HOST PATHOGEN INTERACTION; INTESTINE FLORA; METABOLISM; MICROBIOLOGY; PATHOLOGY; TUMOR ASSOCIATED LEUKOCYTE;

ANIMALS; AZOXYMETHANE; CASE-CONTROL STUDIES; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; COLON; COLONIC POLYPS; COLORECTAL NEOPLASMS; DISEASE MODELS, ANIMAL; FECES; GASTROINTESTINAL MICROBIOME; GENE EXPRESSION REGULATION, NEOPLASTIC; GERM-FREE LIFE; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLAMMATION MEDIATORS; KI-67 ANTIGEN; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MICE, INBRED C57BL; TH1 CELLS; TH17 CELLS;

EID: 85035071123     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2017.08.022     Document Type: Article

References (35)

1. Dove, W.F., Clipson, L., Gould, K.A., et al. Intestinal neoplasia in the ApcMin mouse: independence from the microbial and natural killer (beige locus) status. Cancer Res 57 (1997), 812–814.
2. Reddy, B.S., Narisawa, T., Wright, P., et al. Colon carcinogenesis with azoxymethane and dimethylhydrazine in germ-free rats. Cancer Res 35 (1975), 287–290.
3. Arthur, J.C., Perez-Chanona, E., Muhlbauer, M., et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science 338 (2012), 120–123.
4. Cuevas-Ramos, G., Petit, C.R., Marcq, I., et al. Escherichia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci U S A 107 (2010), 11537–11542.
5. 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 15 (2009), 1016–10122.
6. Kostic, A.D., Chun, E., Robertson, L., et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 14 (2013), 207–215.
7. Rubinstein, M.R., Wang, X., Liu, W., et al. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/beta-catenin signaling via its FadA adhesin. Cell Host Microbe 14 (2013), 195–206.
8. Tsoi, H., Chu, E.S., Zhang, X., et al. Peptostreptococcus anaerobius induces intracellular cholesterol biosynthesis in colon cells to induce proliferation and causes dysplasia in mice. Gastroenterology 152 (2017), 1419–1433.e5.
9. Zeller, G., Tap, J., Voigt, A.Y., et al. Potential of fecal microbiota for early-stage detection of colorectal cancer. Mol Syst Biol, 10, 2014, 766.
10. Feng, Q., Liang, S., Jia, H., et al. Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat Commun, 6, 2015, 6528.
11. Nakatsu, G., Li, X., Zhou, H., et al. Gut mucosal microbiome across stages of colorectal carcinogenesis. Nat Commun, 6, 2015, 8727.
12. Yu, J., Feng, Q., Wong, S.H., et al. Metagenomic analysis of faecal microbiome as a tool towards targeted non-invasive biomarkers for colorectal cancer. Gut 66 (2017), 70–78.
13. Schloss, P.D., Westcott, S.L., Ryabin, T., et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75 (2009), 7537–7541.
14. Needleman, S.B., Wunsch, C.D., A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48 (1970), 443–453.
15. Quast, C., Pruesse, E., Yilmaz, P., et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41 (2013), D590–D596.
16. DeSantis, T.Z. Jr., Hugenholtz, P., Keller, K., et al. NAST: a multiple sequence alignment server for comparative analysis of 16S rRNA genes. Nucleic Acids Res 34 (2006), W394–W399.
17. Edgar, R.C., Haas, B.J., Clemente, J.C., et al. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27 (2011), 2194–2200.
18. Cole, J.R., Wang, Q., Fish, J.A., et al. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42 (2014), D633–D642.
19. Westcott, S.L., Schloss, P.D., OptiClust, an Improved method for assigning amplicon-based sequence data to operational taxonomic units. mSphere, 2017, 2.
20. Segata, N., Izard, J., Waldron, L., et al. Metagenomic biomarker discovery and explanation. Genome Biol, 12, 2011, R60.
21. Dembele, D., Kastner, P., Fold change rank ordering statistics: a new method for detecting differentially expressed genes. BMC Bioinformatics, 15, 2014, 14.
22. Hajishengallis, G., Darveau, R.P., Curtis, M.A., The keystone-pathogen hypothesis. Nat Rev Microbiol 10 (2012), 717–725.
23. Baxter, N.T., Zackular, J.P., Chen, G.Y., et al. Structure of the gut microbiome following colonization with human feces determines colonic tumor burden. Microbiome, 2, 2014, 20.
24. Neufert, C., Becker, C., Neurath, M.F., An inducible mouse model of colon carcinogenesis for the analysis of sporadic and inflammation-driven tumor progression. Nat Protoc 2 (2007), 1998–2004.
25. Hakansson, A., Tormo-Badia, N., Baridi, A., et al. Immunological alteration and changes of gut microbiota after dextran sulfate sodium (DSS) administration in mice. Clin Exp Med 15 (2015), 107–120.
26. De Robertis, M., Massi, E., Poeta, M.L., et al. The AOM/DSS murine model for the study of colon carcinogenesis: From pathways to diagnosis and therapy studies. J Carcinog, 10, 2011, 9.
27. Grivennikov, S.I., Wang, K., Mucida, D., et al. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature 491 (2012), 254–258.
28. Huber, S., Gagliani, N., Zenewicz, L.A., et al. IL-22BP is regulated by the inflammasome and modulates tumorigenesis in the intestine. Nature 491 (2012), 259–263.
29. Chae, W.J., Gibson, T.F., Zelterman, D., et al. Ablation of IL-17A abrogates progression of spontaneous intestinal tumorigenesis. Proc Natl Acad Sci U S A 107 (2010), 5540–5544.
30. Zhong, N., Shi, S., Wang, H., et al. Silencing Aurora-A with siRNA inhibits cell proliferation in human lung adenocarcinoma cells. Int J Oncol 49 (2016), 1028–1038.
31. Monn, M.F., Cheng, L., Emerging trends in the evaluation and management of small cell prostate cancer: a clinical and molecular perspective. Expert Rev Anticancer Ther 16 (2016), 1029–1037.
32. Hou, L., Chen, M., Wang, M., et al. Systematic analyses of key genes and pathways in the development of invasive breast cancer. Gene 593 (2016), 1–12.
33. Sobhani, I., Tap, J., Roudot-Thoraval, F., et al. Microbial dysbiosis in colorectal cancer (CRC) patients. PLoS One, 6, 2011, e16393.
34. van der Waaij, L.A., Harmsen, H.J., Madjipour, M., et al. Bacterial population analysis of human colon and terminal ileum biopsies with 16S rRNA-based fluorescent probes: commensal bacteria live in suspension and have no direct contact with epithelial cells. Inflamm Bowel Dis 11 (2005), 865–871.
35. Abed, J., Emgard, J.E., Zamir, G., et al. Fap2 mediates Fusobacterium nucleatum colorectal adenocarcinoma enrichment by binding to tumor-expressed Gal-GalNAc. Cell Host Microbe 20 (2016), 215–225.