Fusobacterium nucleatum tumor DNA levels are associated with survival in colorectal cancer patients

. 2019 Oct ; 38 (10) : 1891-1899. [epub] 20190731

Jazyk angličtina Země Německo Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid31367996

Grantová podpora
HRA-PHS/2015/1142 Health Research Board of Ireland (HRB)
13/ISCA/2843 Science Foundation Ireland - Ireland
AZV 15-27580A; AZV NV 18-03-00199 Ministry of Health of the Czech Republic

Odkazy

PubMed 31367996
PubMed Central PMC6778531
DOI 10.1007/s10096-019-03649-1
PII: 10.1007/s10096-019-03649-1
Knihovny.cz E-zdroje

There is increasing evidence indicating a role for Fusobacterium nucleatum (F. nucleatum) in colorectal cancer (CRC) development and prognosis. This study evaluated F. nucleatum as a prognostic biomarker, by assessing its association with post-diagnosis survival from CRC. From September 2008 to April 2012 CRC patients (n = 190) were recruited from three hospitals within the Czech Republic. F. nucleatum DNA copies were measured in adjacent non-malignant and colorectal tumor tissues using quantitative real-time PCR. Cox Proportional Hazards (HR) models were applied to evaluate the association between F. nucleatum DNA and overall survival, adjusting for key confounders. Risk prediction modeling was conducted to evaluate the ability to predict survival based on F. nucleatum status. High, compared with low, levels of F. nucleatum in colorectal tumor tissues were associated with poorer overall survival (adjusted HR 1.68, 95% CI 1.02-2.77), which was slightly attenuated after additional adjustment for microsatellite instability status. However, inclusion of F. nucleatum in risk prediction models did not improve the ability to identify patients who died beyond known prognostic factors such as disease pathology staging. Although the increased presence of F. nucleatum was associated with poorer prognosis in CRC patients, this may have limited clinical relevance as a prognostic biomarker.

Zobrazit více v PubMed

Gao R, Gao Z, Huang L, Qin H. Gut microbiota and colorectal cancer. Eur J Clin Microbiol Infect Dis. 2017;36:757–769. doi: 10.1007/s10096-016-2881-8. PubMed DOI PMC

Tilg H, Adolph TE, Gerner RR, Moschen AR. The intestinal microbiota in colorectal cancer. Cancer Cell. 2018;33:954–964. doi: 10.1016/j.ccell.2018.03.004. PubMed DOI

Han YW. Fusobacterium nucleatum: a commensal-turned pathogen. Curr Opin Microbiol. 2015;23:141–147. doi: 10.1016/j.mib.2014.11.013. PubMed DOI PMC

Signat B, Roques C, Poulet P, Duffaut D. Fusobacterium nucleatum in periodontal health and disease. Curr Issues Mol Biol. 2011;13:25–36. PubMed

Rubinstein MR, Wang X, Liu W, Hao Y, Cai G, Han YW. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/beta-catenin signaling via its FadA adhesin. Cell Host Microbe. 2013;14:195–206. doi: 10.1016/j.chom.2013.07.012. PubMed DOI PMC

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(2):299–306. doi: 10.1101/gr.126516.111. PubMed DOI PMC

Brennan CA, Garrett WS. Fusobacterium nucleatum - symbiont, opportunist and oncobacterium. Nat Rev Microbiol. 2019;17(3):156–166. doi: 10.1038/s41579-018-0129-6. PubMed DOI PMC

Amitay EL, Werner S, Vital M, Pieper DH, Höfler D, Gierse IJ, Butt J, Balavarca Y, Cuk K, Brenner H. Fusobacterium and colorectal cancer: causal factor or passenger? Results from a large colorectal cancer screening study. Carcinogenesis. 2017;38(8):781–788. doi: 10.1093/carcin/bgx053. PubMed DOI

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, Li J, Xiao L, Huber-Schönauer U, Niederseer D, Xu X, Al-Aama JY, Yang H, Wang J, Kristiansen K, Arumugam M, Tilg H, Datz C, Wang J. Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat Commun. 2015;6:6528. doi: 10.1038/ncomms7528. PubMed DOI

Yu J, 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, Wu WK, Al-Aama J, Nielsen HJ, Kiilerich P, Jensen BA, Yau TO, Lan Z, Jia H, Li J, Xiao L, Lam TY, Ng SC, Cheng AS, Wong VW, Chan FK, Xu X, Yang H, Madsen L, Datz C, Tilg H, Wang J, Brünner N, Kristiansen K, Arumugam M, Sung JJ, Wang J. Metagenomic analysis of faecal microbiome as a tool towards targeted non-invasive biomarkers for colorectal cancer. Gut. 2015;66(1):70–78. doi: 10.1136/gutjnl-2015-309800. PubMed DOI

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(8):1381–1390. doi: 10.1007/s10096-014-2081-3. PubMed DOI

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(1):16. doi: 10.1186/2049-2618-1-16. PubMed DOI PMC

Hussan H, Clinton SK, Roberts K, Bailey MT. Fusobacterium’s link to colorectal neoplasia sequenced: a systematic review and future insights. World J Gastroenterol. 2017;23(48):8626–8650. doi: 10.3748/wjg.v23.i48.8626. PubMed DOI PMC

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, Meyerson M, Garrett WS. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe. 2013;14(2):207–215. doi: 10.1016/j.chom.2013.07.007. PubMed DOI PMC

Abed J, Emgård JE, Zamir G, Faroja M, Almogy G, Grenov A, Sol A, Naor R, Pikarsky E, Atlan KA, Mellul A, Chaushu S, Manson AL, Earl AM, Ou N, Brennan CA, Garrett WS, Bachrach G. Fap2 mediates fusobacterium nucleatum colorectal adenocarcinoma enrichment by binding to tumor-expressed Gal-GalNAc. Cell Host Microbe. 2016;20(2):215–225. doi: 10.1016/j.chom.2016.07.006. PubMed DOI PMC

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, Bullman S, Milner DA, Harris CC, Giovannucci E, Garraway LA, Freeman GJ, Dranoff G, Chan AT, Garrett WS, Huttenhower C, Fuchs CS, Ogino S. Fusobacterium nucleatum and T Cells in colorectal carcinoma. JAMA Oncol. 2015;1(5):653–661. doi: 10.1001/jamaoncol.2015.1377. PubMed DOI PMC

Gur C, Ibrahim Y, Isaacson B, Yamin R, Abed J, Gamliel M, Enk J, Bar-On Y, Stanietsky-Kaynan N, Coppenhagen-Glazer S, Shussman N, Almogy G, Cuapio A, Hofer E, Mevorach D, Tabib A, Ortenberg R, Markel G, Miklić K, Jonjic S, Brennan CA, Garrett WS, Bachrach G, Mandelboim O. Binding of the Fap2 protein of fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity. 2015;42(2):344–355. doi: 10.1016/j.immuni.2015.01.010. PubMed DOI PMC

Kelly D, Yang L, Pei Z. Gut microbiota, fusobacteria, and colorectal cancer. Diseases. 2018;6(4):E109. doi: 10.3390/diseases6040109. PubMed DOI PMC

Zhang S, Cai S, Ma Y. Association between fusobacterium nucleatum and colorectal cancer: progress and future directions. J Cancer. 2018;9(9):1652–1659. doi: 10.7150/jca.24048. PubMed DOI PMC

Shang FM, Liu HL. Fusobacterium nucleatum and colorectal cancer: a review. World J Gastrointest Oncol. 2018;10(3):71–81. doi: 10.4251/wjgo.v10.i3.71. PubMed DOI PMC

Sun Y, An QM, Tian XY, Wang ZL, Guan XY, Dong B, Zhao M, Hao CY. Fusobacterium nucleatum infection is correlated with tumor metastasis and postoperative survival of colorectal cancer patients in China. Transl Cancer Res. 2016;5(5):579–588. doi: 10.21037/tcr.2016.10.45. DOI

Wei Z, Cao S, Liu S, Yao Z, Sun T, Li Y, Li J, Zhang D, Zhou Y. Could gut microbiota serve as prognostic biomarker associated with colorectal cancer patients’ survival? A pilot study on relevant mechanism. Oncotarget. 2016;7(29):46158–46172. doi: 10.18632/oncotarget.10064. PubMed DOI PMC

Yamaoka Y, Suehiro Y, Hashimoto S, Hoshida T, Fujimoto M, Watanabe M, Imanaga D, Sakai K, Matsumoto T, Nishioka M, Takami T, Suzuki N, Hazama S, Nagano H, Sakaida I, Yamasaki T. Fusobacterium nucleatum as a prognostic marker of colorectal cancer in a Japanese population. J Gastroenterol. 2018;53(4):517–524. doi: 10.1007/s00535-017-1382-6. PubMed DOI

Lee DW, Han SW, Kang JK, Bae JM, Kim HP, Won JK, Jeong SY, Park KJ, Kang GH, Kim TY. Association between fusobacterium nucleatum, pathway mutation, and patient prognosis in colorectal cancer. Ann Surg Oncol. 2018;25(11):3389–3395. doi: 10.1245/s10434-018-6681-5. PubMed DOI

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, Milner DA, Baba H, Giovannucci EL, Garraway LA, Freeman GJ, Dranoff G, Garrett WS, Huttenhower C, Meyerson M, Meyerhardt JA, Chan AT, Fuchs CS, Ogino S. Fusobacterium nucleatum in colorectal carcinoma tissue and patient prognosis. Gut. 2016;65(12):1973–1980. doi: 10.1136/gutjnl-2015-310101. PubMed DOI PMC

Suraweera N, Duval A, Reperant M, Vaury C, Furlan D, Leroy K, Seruca R, Iacopetta B, Hamelin R. Evaluation of tumor microsatellite instability using five quasimonomorphic mononucleotide repeats and pentaplex PCR. Gastroenterology. 2002;123(6):1804–1811. doi: 10.1053/gast.2002.37070. PubMed DOI

Lemstrova R, Brynychova V, Hughes DJ, Hlavac V, Dvorak P, Doherty JE, Murray HA, Crockard M, Oliverius M, Hlavsa J, Honsova E, Mazanec J, Kala Z, Lovecek M, Havlik R, Ehrmann J, Strouhal O, Soucek P, Melichar B, Mohelnikova-Duchonova B. Dysregulation of KRAS signaling in pancreatic cancer is not associated with KRAS mutations and outcome. Oncol Lett. 2017;14(5):5980–5988. doi: 10.3892/ol.2017.694. PubMed DOI PMC

Oh HJ, Kim JH, Bae JM, Kim HJ, Cho NY, Kang GH. Prognostic impact of fusobacterium nucleatum depends on combined tumor location and microsatellite instability status in stage II/III colorectal cancers treated with adjuvant chemotherapy. J Pathol Transl Med. 2019;53(1):40–49. doi: 10.4132/jptm.2018.11.29. PubMed DOI PMC

Bullman S, Pedamallu CS, Sicinska E, Clancy TE, Zhang X, Cai D, Neuberg D, Huang K, Guevara F, Nelson T, Chipashvili O, Hagan T, Walker M, Ramachandran A, Diosdado B, Serna G, Mulet N, Landolfi S, Ramon Y, Cajal S, Fasani R, Aguirre AJ, Ng K, Élez E, Ogino S, Tabernero J, Fuchs CS, Hahn WC, Nuciforo P, Meyerson M. Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer. Science. 2017;358(6369):1443–1448. doi: 10.1126/science.aal5240. PubMed DOI PMC

Yu T, Guo F, Yu Y, Sun T, Ma D, Han J, Qian Y, Kryczek I, Sun D, Nagarsheth N, Chen Y, Chen H, Hong J, Zou W, Fang JY. Fusobacterium nucleatum promotes chemoresistance to colorectal cancer by modulating autophagy. Cell. 2017;170(3):548–563.e16. doi: 10.1016/j.cell.2017.07.008. PubMed DOI PMC

Proença MA, Biselli JM, Succi M, Severino FE, Berardinelli GN, Caetano A, Reis RM, Hughes DJ, Silva AE. Relationship between Fusobacterium nucleatum, inflammatory mediators and microRNAs in colorectal carcinogenesis. World J Gastroenterol. 2018;24(47):5351–5365. doi: 10.3748/wjg.v24.i47.5351. PubMed DOI PMC

Yu YN, Yu TC, Zhao HJ, Sun TT, Chen HM, Chen HY, An HF, Weng YR, Yu J, Li M, Qin WX, Ma X, Shen N, Hong J, Fang JY. Berberine may rescue Fusobacterium nucleatum-induced colorectal tumorigenesis by modulating the tumor microenvironment. Oncotarget. 2015;6(31):32013–32026. doi: 10.18632/oncotarget.5166. PubMed DOI PMC

Hynes SO, Coleman HG, Kelly PJ, Irwin S, O'Neill RF, Gray RT, McGready C, Dunne PD, McQuaid S, James JA, Salto-Tellez M, Loughrey MB. Back to the future: routine morphological assessment of the tumour microenvironment is prognostic in stage II/III colon cancer in a large population-based study. Histopathology. 2017;71(1):12–26. doi: 10.1111/his.13181. PubMed DOI

Hamada T, Zhang X, Mima K, Bullman S, Sukawa Y, Nowak JA, Kosumi K, Masugi Y, Twombly TS, Cao Y, Song M, Liu L, da Silva A, Shi Y, Gu M, Li W, Koh H, Nosho K, Inamura K, Keum N, Wu K, Meyerhardt JA, Kostic AD, Huttenhower C, Garrett WS, Meyerson M, Giovannucci EL, Chan AT, Fuchs CS, Nishihara R, Giannakis M, Ogino S. Fusobacterium nucleatum in colorectal cancer relates to immune response differentially by tumor microsatellite instability status. Cancer Immunol Res. 2018;6(11):1327–1336. doi: 10.1158/2326-6066.CIR-18-0174. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...