Fusobacterium nucleatum promotes colorectal cancer by inducing Wnt/β-catenin modulator Annexin A1

EMBO Reports

Volumn 20, Issue 4, 2019, Pages

  Rubinstein, Mara Roxana ^a   Baik, Jung Eun ^a   Lagana, Stephen M ^b   Han, Richard P ^c   Raab, William J ^b   Sahoo, Debashis ^d   Dalerba, Piero ^a,b   Wang, Timothy C ^a   Han, Yiping W ^a,b  

^a Columbia University ^*  (United States)

^b New York Presbyterian Columbia University Medical Center   (United States)

^c Horace Mann School   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Annexin A1; colorectal cancer; FadA; Fusobacterium nucleatum; two hit model

Indexed keywords

BETA CATENIN; CYCLIN D1; DESMOPLAKIN; LIPOCORTIN 1; MESSENGER RNA; TUMOR MARKER; UNCLASSIFIED DRUG; UVOMORULIN; VILLIN; VILLIN 1; WNT PROTEIN; PROTEIN BINDING;

22RV1 CELL LINE; ARTICLE; CANCER GROWTH; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; CELL PROLIFERATION; COLON CARCINOGENESIS; COLORECTAL ADENOMA; COLORECTAL CANCER; COLORECTAL CANCER CELL LINE; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE FREE SURVIVAL; DOWN REGULATION; FEMALE; FUSOBACTERIUM NUCLEATUM; HUMAN; HUMAN CELL; LARGE INTESTINE EPITHELIUM; MAJOR CLINICAL STUDY; MALE; MCF-7 CELL LINE; MOLECULAR PATHOLOGY; MRNA EXPRESSION LEVEL; NONHUMAN; PC-9 CELL LINE; POSITIVE FEEDBACK; PRECANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; UM-UC-3 CELL LINE; UPREGULATION; WNT SIGNALING; ANIMAL; BIOLOGICAL MODEL; CELL TRANSFORMATION; COLORECTAL TUMOR; COMPLICATION; DISEASE MODEL; DISEASE PREDISPOSITION; FUSOBACTERIUM INFECTION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MORTALITY; MOUSE; PATHOLOGY; PHYSIOLOGICAL FEEDBACK; PHYSIOLOGY; PROGNOSIS; SIGNAL TRANSDUCTION; XENOGRAFT;

ANIMALS; ANNEXIN A1; BETA CATENIN; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; COLORECTAL NEOPLASMS; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; FEEDBACK, PHYSIOLOGICAL; FUSOBACTERIUM INFECTIONS; FUSOBACTERIUM NUCLEATUM; HETEROGRAFTS; HOST-PATHOGEN INTERACTIONS; HUMANS; MICE; MODELS, BIOLOGICAL; PROGNOSIS; PROTEIN BINDING; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 85062454137     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201847638     Document Type: Article

References (45)

1. ACS (2012) Cancer Facts & Figures 2012. In pp 1–66. American Cancer Society (ACS)
2. Vogelstein B, Kinzler KW (1993) The multistep nature of cancer. Trends Genet 9: 138–141
3. Abreu MT, Peek Jr RM (2014) Gastrointestinal malignancy and the microbiome. Gastroenterology 146: 1534–1546.e3
4. Akkari L, Gocheva V, Kester JC, Hunter KE, Quick ML, Sevenich L, Wang HW, Peters C, Tang LH, Klimstra DS et al (2014) Distinct functions of macrophage-derived and cancer cell-derived cathepsin Z combine to promote tumor malignancy via interactions with the extracellular matrix. Genes Dev 28: 2134–2150
5. Schwabe RF, Jobin C (2013) The microbiome and cancer. Nat Rev Cancer 13: 800–812
6. Dulal S, Keku TO (2014) Gut microbiome and colorectal adenomas. Cancer J 20: 225–231
7. Keku TO, Dulal S, Deveaux A, Jovov B, Han X (2015) The gastrointestinal microbiota and colorectal cancer. Am J Physiol Gastrointest Liver Physiol 308: G351–G363
8. Keku TO, McCoy AN, Azcarate-Peril AM (2013) Fusobacterium spp. and colorectal cancer: cause or consequence? Trends Microbiol 21: 506–508
9. McCoy AN, Araujo-Perez F, Azcarate-Peril A, Yeh JJ, Sandler RS, Keku TO (2013) Fusobacterium is associated with colorectal adenomas. PLoS ONE 8: e53653
10. Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA, Michaud M, Clancy TE, Chung DC, Lochhead P, Hold GL et al (2013) Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-Immune microenvironment. Cell Host Microbe 14: 207–215
11. Kostic AD, Gevers D, Pedamallu CS, Michaud M, Duke F, Earl AM, Ojesina AI, Jung J, Bass AJ, Tabernero J et al (2012) Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res 22: 292–298
12. Rubinstein MR, Wang X, Liu W, Hao Y, Cai G, Han YW (2013) Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe 14: 195–206
13. Gur C, Ibrahim Y, Isaacson B, Yamin R, Abed J, Gamliel M, Enk J, Bar-On Y, Stanietsky-Kaynan N, Coppenhagen-Glazer S et al (2015) Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity 42: 344–355
14. Yu T, Guo F, Yu Y, Sun T, Ma D, Han J, Qian Y, Kryczek I, Sun D, Nagarsheth N et al (2017) Fusobacterium nucleatum promotes chemoresistance to colorectal cancer by modulating autophagy. Cell 170: 548–563 e16
15. Tahara T, Yamamoto E, Suzuki H, Maruyama R, Chung W, Garriga J, Jelinek J, Yamano HO, Sugai T, An B et al (2014) Fusobacterium in colonic flora and molecular features of colorectal carcinoma. Can Res 74: 1311–1318
16. Mima K, Cao Y, Chan AT, Qian ZR, Nowak JA, Masugi Y, Shi Y, Song M, da Silva A, Gu M et al (2016) Fusobacterium nucleatum in colorectal carcinoma tissue according to tumor location. Clin Transl Gastroenterol 7: e200
17. Yu J, Chen Y, Fu X, Zhou X, Peng Y, Shi L, Chen T, Wu Y (2016) Invasive Fusobacterium nucleatum may play a role in the carcinogenesis of proximal colon cancer through the serrated neoplasia pathway. Int J Cancer 139: 1318–1326
18. Mima K, Nishihara R, Qian ZR, Cao Y, Sukawa Y, Nowak JA, Yang J, Dou R, Masugi Y, Song M et al (2016) Fusobacterium nucleatum in colorectal carcinoma tissue and patient prognosis. Gut 65: 1973–1980
19. Bullman S, Pedamallu CS, Sicinska E, Clancy TE, Zhang X, Cai D, Neuberg D, Huang K, Guevara F, Nelson T et al (2017) Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer. Science 358: 1443–1448
20. Flanagan L, Schmid J, Ebert M, Soucek P, Kunicka T, Liska V, Bruha J, Neary P, Dezeeuw N, Tommasino M et al (2014) Fusobacterium nucleatum associates with stages of colorectal neoplasia development, colorectal cancer and disease outcome. Eur J Clin Microbiol Infect Dis 33: 1381–1390
21. Abed J, Emgard JE, Zamir G, Faroja M, Almogy G, Grenov A, Sol A, Naor R, Pikarsky E, Atlan KA et al (2016) Fap2 mediates Fusobacterium nucleatum colorectal adenocarcinoma enrichment by binding to tumor-expressed Gal-GalNAc. Cell Host Microbe 20: 215–225
22. Xu M, Yamada M, Li M, Liu H, Chen SG, Han YW (2007) FadA from Fusobacterium nucleatum utilizes both secreted and nonsecreted forms for functional oligomerization for attachment and invasion of host cells. J Biol Chem 282: 25000–25009
23. Gerke V, Moss SE (2002) Annexins: from structure to function. Physiol Rev 82: 331–371
24. Guo C, Liu S, Sun MZ (2013) Potential role of Anxa1 in cancer. Fut Oncol 9: 1773–1793
25. Boudhraa Z, Bouchon B, Viallard C, D'Incan M, Degoul F (2016) Annexin A1 localization and its relevance to cancer. Clin Sci 130: 205–220
26. Su N, Xu XY, Chen H, Gao WC, Ruan CP, Wang Q, Sun YP (2010) Increased expression of annexin A1 is correlated with K-ras mutation in colorectal cancer. Tohoku J Exp Med 222: 243–250
27. Duncan R, Carpenter B, Main LC, Telfer C, Murray GI (2008) Characterisation and protein expression profiling of annexins in colorectal cancer. Br J Cancer 98: 426–433
28. Shimoyama Y, Nagafuchi A, Fujita S, Gotoh M, Takeichi M, Tsukita S, Hirohashi S (1992) Cadherin dysfunction in a human cancer cell line: possible involvement of loss of alpha-catenin expression in reduced cell-cell adhesiveness. Can Res 52: 5770–5774
29. Tiang JM, Butcher NJ, Cullinane C, Humbert PO, Minchin RF (2011) RNAi-mediated knock-down of arylamine N-acetyltransferase-1 expression induces E-cadherin up-regulation and cell-cell contact growth inhibition. PLoS ONE 6: e17031
30. Luo Y, Zhu YT, Ma LL, Pang SY, Wei LJ, Lei CY, He CW, Tan WL (2016) Characteristics of bladder transitional cell carcinoma with E-cadherin and N-cadherin double-negative expression. Oncol Lett 12: 530–536
31. Chao YL, Shepard CR, Wells A (2010) Breast carcinoma cells re-express E-cadherin during mesenchymal to epithelial reverting transition. Mol Cancer 9: 179
32. Williams AC, Harper SJ, Paraskeva C (1990) Neoplastic transformation of a human colonic epithelial cell line: in vitro evidence for the adenoma to carcinoma sequence. Can Res 50: 4724–4730
33. Roth U, Razawi H, Hommer J, Engelmann K, Schwientek T, Muller S, Baldus SE, Patsos G, Corfield AP, Paraskeva C et al (2010) Differential expression proteomics of human colorectal cancer based on a syngeneic cellular model for the progression of adenoma to carcinoma. Proteomics 10: 194–202
34. Dalerba P, Sahoo D, Paik S, Guo X, Yothers G, Song N, Wilcox-Fogel N, Forgo E, Rajendran PS, Miranda SP et al (2016) CDX2 as a prognostic biomarker in stage II and stage III colon cancer. N Engl J Med 374: 211–222
35. Dalerba P, Kalisky T, Sahoo D, Rajendran PS, Rothenberg ME, Leyrat AA, Sim S, Okamoto J, Johnston DM, Qian D et al (2011) Single-cell dissection of transcriptional heterogeneity in human colon tumors. Nat Biotechnol 29: 1120–1127
36. Sahoo D, Dill DL, Tibshirani R, Plevritis SK (2007) Extracting binary signals from microarray time-course data. Nucleic Acids Res 35: 3705–3712
37. Fardini Y, Wang X, Temoin S, Nithianantham S, Lee D, Shoham M, Han YW (2011) Fusobacterium nucleatum adhesin FadA binds vascular endothelial cadherin and alters endothelial integrity. Mol Microbiol 82: 1468–1480
38. Fearon ER, Vogelstein B (1990) A genetic model for colorectal tumorigenesis. Cell 61: 759–767
39. Dejea CM, Fathi P, Craig JM, Boleij A, Taddese R, Geis AL, Wu X, DeStefano Shields CE, Hechenbleikner EM, Huso DL et al (2018) Patients with familial adenomatous polyposis harbor colonic biofilms containing tumorigenic bacteria. Science 359: 592–597
40. Scanu T, Spaapen RM, Bakker JM, Pratap CB, Wu LE, Hofland I, Broeks A, Shukla VK, Kumar M, Janssen H et al (2015) Salmonella manipulation of host signaling pathways provokes cellular transformation associated with gallbladder carcinoma. Cell Host Microbe 17: 763–774
41. Novellasdemunt L, Antas P, Li VS (2015) Targeting Wnt signaling in colorectal cancer. A review in the theme: cell signaling: proteins, pathways and mechanisms. Am J Physiol Cell Physiol 309: C511–C521
42. Krishnamurthy N, Kurzrock R (2018) Targeting the Wnt/beta-catenin pathway in cancer: update on effectors and inhibitors. Cancer Treat Rev 62: 50–60
43. Onozawa H, Saito M, Saito K, Kanke Y, Watanabe Y, Hayase S, Sakamoto W, Ishigame T, Momma T, Ohki S et al (2017) Annexin A1 is involved in resistance to 5-FU in colon cancer cells. Oncol Rep 37: 235–240
44. Han YW, Shi W, Huang GT, Kinder Haake S, Park NH, Kuramitsu H, Genco RJ (2000) Interactions between periodontal bacteria and human oral epithelial cells: Fusobacterium nucleatum adheres to and invades epithelial cells. Infect Immun 68: 3140–3146
45. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408