Invasive Fusobacterium nucleatum activates beta-catenin signaling in colorectal cancer via a TLR4/P-PAK1 cascade

Oncotarget

Volumn 8, Issue 19, 2017, Pages 31802-31814

  Chen, Yongyu ^a   Peng, Yan ^a   Yu, Jiahui ^a   Chen, Ting ^a   Wu, Yaxin ^a   Shi, Lei ^a   Li, Qing ^a   Wu, Jiao ^a   Fu, Xiangsheng ^a  

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

Author keywords

Colorectal cancer; Fusobacterium nucleatum; P21 activated kinase 1; Toll like receptor 4; catenin signaling

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; BETA CATENIN; CYCLIN D1; MYC PROTEIN; P21 ACTIVATED KINASE 1; TOLL LIKE RECEPTOR 4; P21 ACTIVATED KINASE; PAK1 PROTEIN, HUMAN; PROTEIN BINDING;

ADULT; AGED; ARTICLE; CANCER TISSUE; CLINICAL ARTICLE; COLON CANCER CELL LINE; COLORECTAL CANCER; CONTROLLED STUDY; DRUG TARGETING; FEMALE; FUSOBACTERIUM NUCLEATUM; HUMAN; MALE; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; CANCER GRADING; COLORECTAL TUMOR; COMPLICATION; DRUG EFFECT; FLUORESCENCE IN SITU HYBRIDIZATION; FUSOBACTERIUM INFECTION; GENETICS; METABOLISM; METASTASIS; MICROBIOLOGY; MIDDLE AGED; PATHOLOGY; TUMOR CELL LINE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; BETA CATENIN; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; FEMALE; FUSOBACTERIUM INFECTIONS; FUSOBACTERIUM NUCLEATUM; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM METASTASIS; P21-ACTIVATED KINASES; PROTEIN BINDING; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 85019114427     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.15992     Document Type: Article

References (40)

1. Kostic AD, Gevers D, Pedamallu CS, Michaud M, Duke F, Earl AM, Ojesina AI, Jung J, Bass AJ, Tabernero J, Baselga J, Liu C, Shivdasani RA, et al. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res. 2012; 22:292-98
2. Mima K, Nishihara R, Qian ZR, Cao Y, Sukawa Y, Nowak JA, Yang J, Dou R, Masugi Y, Song M, Kostic AD, Giannakis M, Bullman S, et al. Fusobacterium nucleatum in colorectal carcinoma tissue and patient prognosis. Gut. 2016; 65:1973-1980
3. Mima K, Sukawa Y, Nishihara R, Qian ZR, Yamauchi M, Inamura K, Kim SA, Masuda A, Nowak JA, Nosho K, Kostic AD, Giannakis M, Watanabe H, et al. Fusobacterium nucleatum and T Cells in Colorectal Carcinoma. JAMA Oncol. 2015; 1:653-61
4. Kostic AD, Chun E, Robertson L, Glickman JN, Gallini CA, Michaud M, Clancy TE, Chung DC, Lochhead P, Hold GL, El-Omar EM, Brenner D, Fuchs CS, et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe. 2013; 14:207-15
5. Liu H, Redline RW, Han YW. Fusobacterium nucleatum induces fetal death in mice via stimulation of TLR4-mediated placental inflammatory response. J Immunol. 2007; 179:2501-08
6. Fukata M, Shang L, Santaolalla R, Sotolongo J, Pastorini C, España C, Ungaro R, Harpaz N, Cooper HS, Elson G, Kosco-Vilbois M, Zaias J, Perez MT, et al. Constitutive activation of epithelial TLR4 augments inflammatory responses to mucosal injury and drives colitis-associated tumorigenesis. Inflamm Bowel Dis. 2011; 17:1464-73
7. Fukata M, Chen A, Vamadevan AS, Cohen J, Breglio K, Krishnareddy S, Hsu D, Xu R, Harpaz N, Dannenberg AJ, Subbaramaiah K, Cooper HS, Itzkowitz SH, Abreu MT. Toll-like receptor-4 promotes the development of colitisassociated colorectal tumors. Gastroenterology. 2007; 133:1869-81
8. Cammarota R, Bertolini V, Pennesi G, Bucci EO, Gottardi O, Garlanda C, Laghi L, Barberis MC, Sessa F, Noonan DM, Albini A. The tumor microenvironment of colorectal cancer: stromal TLR-4 expression as a potential prognostic marker. J Transl Med. 2010; 8:112
9. Wang EL, Qian ZR, Nakasono M, Tanahashi T, Yoshimoto K, Bando Y, Kudo E, Shimada M, Sano T. High expression of Toll-like receptor 4/myeloid differentiation factor 88 signals correlates with poor prognosis in colorectal cancer. Br J Cancer. 2010; 102:908-15
10. Giles RH, van Es JH, Clevers H. Caught up in a Wnt storm: Wnt signaling in cancer. Biochim Biophys Acta. 2003; 1653:1-24
11. Valenta T, Hausmann G, Basler K. The many faces and functions of β-catenin. EMBO J. 2012; 31:2714-36
12. Sun J. Enteric bacteria and cancer stem cells. Cancers (Basel). 2010; 3:285-97
13. Molli PR, Li DQ, Murray BW, Rayala SK, Kumar R. PAK signaling in oncogenesis. Oncogene. 2009; 28:2545-55
14. Carter JH, Douglass LE, Deddens JA, Colligan BM, Bhatt TR, Pemberton JO, Konicek S, Hom J, Marshall M, GraffJR. Pak-1 expression increases with progression of colorectal carcinomas to metastasis. Clin Cancer Res. 2004; 10:3448-56
15. Zhu G, Wang Y, Huang B, Liang J, Ding Y, Xu A, Wu W. A Rac1/PAK1 cascade controls β-catenin activation in colon cancer cells. Oncogene. 2012; 31:1001-12
16. Santaolalla R, Sussman DA, Ruiz JR, Davies JM, Pastorini C, España CL, Sotolongo J, Burlingame O, Bejarano PA, Philip S, Ahmed MM, Ko J, Dirisina R, et al. TLR4 activates the β-catenin pathway to cause intestinal neoplasia. PLoS One. 2013; 8:e63298
17. Yu J, Feng Q, Wong SH, Zhang D, Liang QY, Qin Y, Tang L, Zhao H, Stenvang J, Li Y, Wang X, Xu X, Chen N, et al. Metagenomic analysis of faecal microbiome as a tool towards targeted non-invasive biomarkers for colorectal cancer. Gut. 2017; 66:70-78
18. Zeller G, Tap J, Voigt AY, Sunagawa S, Kultima JR, Costea PI, Amiot A, Böhm J, Brunetti F, Habermann N, Hercog R, Koch M, Luciani A, et al. Potential of fecal microbiota for early-stage detection of colorectal cancer. Mol Syst Biol. 2014; 10:766
19. Feng Q, Liang S, Jia H, Stadlmayr A, Tang L, Lan Z, Zhang D, Xia H, Xu X, Jie Z, Su L, Li X, Li X, et al. Gut microbiome development along the colorectal adenomacarcinoma sequence. Nat Commun. 2015; 6:6528
20. Park MH, Kim DJ, You ST, Lee CS, Kim HK, Park SM, Shin EY, Kim EG. Phosphorylation of β-catenin at serine 663 regulates its transcriptional activity. Biochem Biophys Res Commun. 2012; 419:543-49
21. Dammann K, Khare V, Gasche C. Tracing PAKs from GI inflammation to cancer. Gut. 2014; 63:1173-84
22. Manser E, Leung T, Salihuddin H, Zhao ZS, Lim L. A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature. 1994; 367:40-46
23. Quah SY, Bergenholtz G, Tan KS. Fusobacterium nucleatum induces cytokine production through Toll-like-receptorindependent mechanism. Int Endod J. 2014; 47:550-59
24. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 1998; 282:2085-88
25. Strauss J, Kaplan GG, Beck PL, Rioux K, Panaccione R, Devinney R, Lynch T, Allen-Vercoe E. Invasive potential of gut mucosa-derived Fusobacterium nucleatum positively correlates with IBD status of the host. Inflamm Bowel Dis. 2011; 17:1971-78
26. Ding T, Schloss PD. Dynamics and associations of microbial community types across the human body. Nature. 2014; 509:357-60
27. Abreu MT, Peek RM, Jr. Gastrointestinal malignancy and the microbiome. Gastroenterology. 2014; 146:1534-1546 e1533. https://doi.org/10.1053/j.gastro.2014.01.001
28. Flanagan L, Schmid J, Ebert M, Soucek P, Kunicka T, Liska V, Bruha J, Neary P, Dezeeuw N, Tommasino M, Jenab M, Prehn JH, Hughes DJ. Fusobacterium nucleatum associates with stages of colorectal neoplasia development, colorectal cancer and disease outcome. Eur J Clin Microbiol Infect Dis. 2014; 33:1381-90
29. Warren RL, Freeman DJ, Pleasance S, Watson P, Moore RA, Cochrane K, Allen-Vercoe E, Holt RA. Co-occurrence of anaerobic bacteria in colorectal carcinomas. Microbiome. 2013; 1:16
30. Guo J, Fu X, Liao H, Hu Z, Long L, Yan W, Ding Y, Zha L, Guo Y, Yan J, Chang Y, Cai J. Potential use of bacterial community succession for estimating post-mortem interval as revealed by high-throughput sequencing. Sci Rep. 2016; 6:24197
31. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012; 6:1621-24
32. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010; 7:335-36
33. Yu J, Chen Y, Fu X, Zhou X, Peng Y, Shi L, Chen T, Wu Y. Invasive Fusobacterium nucleatum may play a role in the carcinogenesis of proximal colon cancer through the serrated neoplasia pathway. Int J Cancer. 2016; 139:1318-26
34. Loy A, Arnold R, Tischler P, Rattei T, Wagner M, Horn M. probeCheck-a central resource for evaluating oligonucleotide probe coverage and specificity. Environ Microbiol. 2008; 10:2894-98
35. Li L, Fu X, Zhang W, Xiao L, Qiu Y, Peng Y, Shi L, Chen X, Zhou X, Deng M. Wnt signaling pathway is activated in right colon serrated polyps correlating to specific molecular form of β-catenin. Hum Pathol. 2013; 44:1079-88
36. Li H, Liu N, Wang S, Wang L, Zhao J, Su L, Zhang Y, Zhang S, Xu Z, Zhao B, et al. Identification of a small molecule targeting annexin A7. Biochim Biophys Acta. 2013; 1833:2092-2099
37. Castellarin M, Warren RL, Freeman JD, Dreolini L, Krzywinski M, Strauss J, Barnes R, Watson P, Allen-Vercoe E, Moore RA, Holt RA. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res. 2012; 22:299-306
38. Park SN, Lim YK, Kook JK. Development of quantitative real-time PCR primers for detecting 42 oral bacterial species. Arch Microbiol. 2013; 195:473-82
39. Zhao SY, Jiang DY, Xu PC, Zhang YK, Shi HF, Cao HL, Wu Q. An investigation of drug-resistant Acinetobacter baumannii infections in a comprehensive hospital of East China. Ann Clin Microbiol Antimicrob. 2015; 14:7
40. Mendes RT, Nguyen D, Stephens D, Pamuk F, Fernandes D, Van Dyke TE, Kantarci A. Endothelial Cell Response to Fusobacterium nucleatum. Infect Immun. 2016; 84:2141-48