Invasive Fusobacterium nucleatum may play a role in the carcinogenesis of proximal colon cancer through the serrated neoplasia pathway

International Journal of Cancer

Volumn 139, Issue 6, 2016, Pages 1318-1326

  Yu, Jiahui ^a   Chen, Yongyu ^a   Fu, Xiangsheng ^a   Zhou, Xian ^a   Peng, Yan ^a   Shi, Lei ^a   Chen, Ting ^a   Wu, Yaxin ^a  

^a THE AFFILIATED HOSPITAL OF SOUTHWEST MEDICAL UNIVERSITY   (China)

Author keywords

biofilms; colorectal cancer; Fusobacterium nucleatum; sessile serrated adenoma

Indexed keywords

RNA 16S;

ADULT; AGED; ARTICLE; BACTERIUM DETECTION; BIOFILM; CELL INVASION; COLON CANCER; COLON CARCINOGENESIS; COLON MUCOSA; COLON POLYP; COLORECTAL CANCER; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; FUSOBACTERIUM NUCLEATUM; HUMAN; HUMAN TISSUE; HYPERPLASIA; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; RECTUM ADENOMA; SCANNING ELECTRON MICROSCOPY; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY;

EID: 84977564759     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.30168     Document Type: Article

References (42)

1. Abreu MT, Peek RM. Jr. Gastrointestinal malignancy and the microbiome. Gastroenterology 2014; 146:1534–1546. e1533.
2. Strauss J, Kaplan GG, Beck PL, et al. Invasive potential of gut mucosa-derived Fusobacterium nucleatum positively correlates with IBD status of the host. Inflamm Bowel Dis 2011; 17:1971–1978.
3. Swidsinski A, Dorffel Y, Loening-Baucke V, et al. Acute appendicitis is characterised by local invasion with Fusobacterium nucleatum/necrophorum. Gut 2011; 60:34–40.
4. Kostic AD, Gevers D, Pedamallu CS, et al. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res 2012; 22:292–298.
5. Castellarin M, Warren RL, Freeman JD, et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res 2012; 22:299–306.
6. Sears CL, Garrett WS. Microbes, microbiota, and colon cancer. Cell Host Microbe 2014; 15:317–328.
7. Tahara T, Yamamoto E, Suzuki H, et al. Fusobacterium in colonic flora and molecular features of colorectal carcinoma. Cancer Res 2014; 74:1311–1318.
8. Jobin C. Colorectal cancer: looking for answers in the microbiota. Cancer Discov 2013; 3:384–387.
9. Kostic AD, Chun E, Robertson L, et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 2013; 14:207–215.
10. Grady WM. CIMP and colon cancer gets more complicated. Gut 2007; 56:1498–1500.
11. Makinen MJ. Colorectal serrated adenocarcinoma. Histopathology 2007; 50:131–150.
12. Torlakovic E, Skovlund E, Snover DC, et al. Morphologic reappraisal of serrated colorectal polyps. Am J Surg Pathol 2003; 27:65–81.
13. Rex DK, Bond JH, Winawer S, et al. Quality in the technical performance of colonoscopy and the continuous quality improvement process for colonoscopy: recommendations of the U.S. Multi-Society Task Force on Colorectal Cancer. Am J Gastroenterol 2002; 97:1296–1308.
14. Goldstein NS. Small colonic microsatellite unstable adenocarcinomas and high-grade epithelial dysplasias in sessile serrated adenoma polypectomy specimens: a study of eight cases. Am J Clin Pathol 2006; 125:132–145.
15. Lazarus R, Junttila OE, Karttunen TJ, et al. The risk of metachronous neoplasia in patients with serrated adenoma. Am J Clin Pathol 2005; 123:349–359.
16. Lu FI, van Niekerk de W, Owen D, et al. Longitudinal outcome study of sessile serrated adenomas of the colorectum: an increased risk for subsequent right-sided colorectal carcinoma. Am J Surg Pathol 2010; 34:927–934.
17. Rosty C, Hewett DG, Brown IS, et al. Serrated polyps of the large intestine: current understanding of diagnosis, pathogenesis, and clinical management. J Gastroenterol 2013; 48:287–302.
18. Bettington M, Walker N, Clouston A, et al. The serrated pathway to colorectal carcinoma: current concepts and challenges. Histopathology 2013; 62:367–386.
19. Kim KM, Lee EJ, Ha S, et al. Molecular features of colorectal hyperplastic polyps and sessile serrated adenoma/polyps from Korea. Am J Surg Pathol 2011; 35:1274–1286.
20. Snover DC. Update on the serrated pathway to colorectal carcinoma. Hum Pathol 2011; 42:1–10.
21. Ito M, Kanno S, Nosho K, et al. Association of Fusobacterium nucleatum with clinical and molecular features in colorectal serrated pathway. Int J Cancer 2015; 137:1258–1268.
22. Dejea CM, Wick EC, Hechenbleikner EM, et al. Microbiota organization is a distinct feature of proximal colorectal cancers. Proc Natl Acad Sci U S A 2014; 111:18321–18326.
23. Snover D, Ahnen D, Burt R, et al. Serrated polyps of the colon and rectum and serrated polyposis. WHO Classification of Tumours of the Digestive System, 4th Edn IARC, Lyon 2010; 160–165.
24. Loy A, Arnold R, Tischler P, et al. probeCheck–a central resource for evaluating oligonucleotide probe coverage and specificity. Environ Microbiol 2008; 10:2894–2898.
25. Strauss J, White A, Ambrose C, et al. Phenotypic and genotypic analyses of clinical Fusobacterium nucleatum and Fusobacterium periodonticum isolates from the human gut. Anaerobe 2008; 14:301–309.
26. Park SN, Lim YK, Kook JK. Development of quantitative real-time PCR primers for detecting 42 oral bacterial species. Arch Microbiol 2013; 195:473–482.
27. Swidsinski A, Ladhoff A, Pernthaler A, et al. Mucosal flora in inflammatory bowel disease. Gastroenterology 2002; 122:44–54.
28. Chen W, Liu F, Ling Z, et al. Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PLoS One 2012; 7:e39743
29. Rubinstein MR, 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 2013; 14:195–206.
30. Gur C, Ibrahim Y, Isaacson B, et al. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity 2015; 42:344–355.
31. Glebov OK, Rodriguez LM, Nakahara K, et al. Distinguishing right from left colon by the pattern of gene expression. Cancer Epidemiol Biomarkers Prev 2003; 12:755–762.
32. Papagiorgis P. Colorectal cancer: dichotomous or continuum model? Perhaps, a combination of both. Gut 2013; 62:1519–1520.
33. Schetter AJ, Heegaard NH, Harris CC. Inflammation and cancer: interweaving microRNA, free radical, cytokine and p53 pathways. Carcinogenesis 2010; 31:37–49.
34. Li L, Fu X, Zhang W, et al. Wnt signaling pathway is activated in right colon serrated polyps correlating to specific molecular form of β-catenin. Hum Pathol 2013; 44:1079–1088.
35. Feng Q, Liang S, Jia H, et al. Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat Commun 2015; 6:6528
36. Yu J, Feng Q, Wong SH, et al. Metagenomic analysis of faecal microbiome as a tool towards targeted non-invasive biomarkers for colorectal cancer. Gut 2015; doi:10.1136/gutjnl-2015-309800.
37. Zeller G, Tap J, Voigt AY, et al. Potential of fecal microbiota for early-stage detection of colorectal cancer. Mol Syst Biol 2014; 10:766
38. Lyra A, Forssten S, Rolny P, et al. Comparison of bacterial quantities in left and right colon biopsies and faeces. World J Gastroenterol 2012; 18:4404–4411.
39. Zoetendal EG, von Wright A, Vilpponen-Salmela T, et al. Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces. Appl Environ Microbiol 2002; 68:3401–3407.
40. Conte MP, Schippa S, Zamboni I, et al. Gut-associated bacterial microbiota in paediatric patients with inflammatory bowel disease. Gut 2006; 55:1760–1767.
41. Johansson ME, Gustafsson JK, Holmen-Larsson J, et al. Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis. Gut 2014; 63:281–291.
42. Colucci F. An oral commensal associates with disease: chicken, egg, or red herring? Immunity 2015; 42:208–210.