946
Views
0
CrossRef citations to date
0
Altmetric
Research Paper

Biofilms and core pathogens shape the tumor microenvironment and immune phenotype in colorectal cancer

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, , , , ORCID Icon & ORCID Icon show all
Article: 2350156 | Received 10 Nov 2023, Accepted 26 Apr 2024, Published online: 10 May 2024

References

  • Yu J, Feng Q, Wong SH, Zhang D, Liang QY, Qin Y, Tang L, Zhao H, Stenvang J, Li Y. et al. Metagenomic analysis of faecal microbiome as a tool towards targeted non-invasive biomarkers for colorectal cancer. Gut. 2017;66(1):70–19. [ published Online First: 2015/09/27]. doi:10.1136/gutjnl-2015-309800.
  • Yachida S, Mizutani S, Shiroma H, Shiba S, Nakajima T, Sakamoto T, Watanabe H, Masuda K, Nishimoto Y, Kubo M. et al. Metagenomic and metabolomic analyses reveal distinct stage-specific phenotypes of the gut microbiota in colorectal cancer. Nat Med. 2019;25(6):968–976. [ published Online First: 2019/06/07]. doi:10.1038/s41591-019-0458-7.
  • Zhao L, Grimes SM, Greer SU, Kubit M, Lee H, Nadauld L, Ji H. Characterization of the consensus mucosal microbiome of colorectal cancer. NAR Cancer. 2021;3(4):zcab049. [ published Online First: 2022/01/07]. doi: 10.1093/narcan/zcab049.
  • Amitay EL, Krilaviciute A, Brenner H. Systematic review: gut microbiota in fecal samples and detection of colorectal neoplasms. Gut Microbes. 2018;9(4):293–307. [ published Online First: 2018/03/16]. doi: 10.1080/19490976.2018.1445957.
  • Janney A, Powrie F, Mann EH. Host–microbiota maladaptation in colorectal cancer. Nature. 2020;585(7826):509–517. [ published Online First: 2020/09/23]. doi:10.1038/s41586-020-2729-3.
  • Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002;420(6917):860–867. [ published Online First: 2002/12/20]. doi:10.1038/nature01322.
  • Tjalsma H, Boleij A, Marchesi JR, Dutilh BE. A bacterial driver–passenger model for colorectal cancer: beyond the usual suspects. Nat Rev Microbiol. 2012;10(8):575–582. doi:10.1038/nrmicro2819.
  • Geis AL, Fan H, Wu X, Wu S, Huso DL, Wolfe JL, Sears CL, Pardoll DM, Housseau F. Regulatory T-cell response to enterotoxigenic Bacteroides fragilis colonization triggers IL17-dependent colon carcinogenesis. Cancer Discov. 2015;5(10):1098–1109. [ published Online First: 2015/07/24]. doi: 10.1158/2159-8290.Cd-15-0447.
  • Wu J, Li Q, Fu X. Fusobacterium nucleatum contributes to the carcinogenesis of colorectal cancer by inducing inflammation and suppressing host immunity. Transl Oncol. 2019;12(6):846–851. [ published Online First: 2019/04/16]. doi:10.1016/j.tranon.2019.03.003.
  • Kostic AD, Chun E, Robertson L, Glickman J, Gallini C, Michaud M, Clancy T, Chung D, Lochhead P, Hold G. et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe. 2013;14(2):207–215. [ published Online First: 2013/08/21]. doi:10.1016/j.chom.2013.07.007.
  • Gur C, Maalouf N, Shhadeh A, Berhani O, Singer BB, Bachrach G, Mandelboim O. Fusobacterium nucleatum supresses anti-tumor immunity by activating CEACAM1. Oncoimmunology. 2019;8(6):e1581531. [ published Online First: 2019/05/10]. doi: 10.1080/2162402x.2019.1581531.
  • Xue Y, Xiao H, Guo S, Xu B, Liao Y, Wu Y, Zhang G. Indoleamine 2,3-dioxygenase expression regulates the survival and proliferation of Fusobacterium nucleatum in THP-1-derived macrophages. Cell Death Disease. 2018;9(3):355. [ published Online First: 2018/03/04]. doi: 10.1038/s41419-018-0389-0.
  • Bennedsen ALB, Furbo S, Bjarnsholt T, Raskov H, Gögenur I, Kvich L. The gut microbiota can orchestrate the signaling pathways in colorectal cancer. APMIS: acta pathologica, microbiologica, et immunologica Scandinavica. APMIS. 2022;130(3):121–139. [ published Online First: 2022/01/11]. doi: 10.1111/apm.13206.
  • Brennan CA, Garrett WS. Gut microbiota, inflammation, and colorectal cancer. Annu Rev Microbiol. 2016;70:395–411. [ published Online First: 2016/09/09]. doi:10.1146/annurev-micro-102215-095513.
  • Liu N-N, Jiao N, Tan J-C, Wang Z, Wu D, Wang A-J, Chen J, Tao L, Zhou C, Fang W. et al. Multi-kingdom microbiota analyses identify bacterial–fungal interactions and biomarkers of colorectal cancer across cohorts. Nat Microbiol. 2022;7(2):238–250. [ published Online First: 2022/01/27]. doi:10.1038/s41564-021-01030-7.
  • Westermann AJ, Barquist L, Vogel J, Bliska JB. Resolving host–pathogen interactions by dual RNA-seq. PLOS Pathog. 2017;13(2):e1006033. [ published Online First: 2017/02/17]. doi: 10.1371/journal.ppat.1006033.
  • Fritz BG, Kirkegaard JB, Nielsen CH, Kirketerp‐Møller K, Malone M, Bjarnsholt T. Transcriptomic fingerprint of bacterial infection in lower extremity ulcers. APMIS: acta pathologica, microbiologica, et immunologica Scandinavica. APMIS. 2022;130(8):524–534. published Online First: 2022/05/15]. doi: 10.1111/apm.13234.
  • Cornforth DM, Dees JL, Ibberson CB, Huse HK, Mathiesen IH, Kirketerp-Møller K, Wolcott RD, Rumbaugh KP, Bjarnsholt T, Whiteley M. et al. Pseudomonas aeruginosa transcriptome during human infection. Proc Natl Acad Sci U S A. 2018;115(22):E5125–e34. [ published Online First: 2018/05/16]. doi:10.1073/pnas.1717525115.
  • Saus E, Iraola-Guzmán S, Willis JR, Brunet-Vega A, Gabaldón T. Microbiome and colorectal cancer: roles in carcinogenesis and clinical potential. Mol Aspects Med. 2019;69:93–106. [ published Online First: 2019/05/15]. doi:10.1016/j.mam.2019.05.001.
  • Aitmanaitė L, Širmonaitis K, Russo RG. Microbiomes, their function, and cancer: how metatranscriptomics can close the knowledge gap. Int J Mol Sci. 2023;24(18):13786. [ published Online First: 2023/09/28]. doi: 10.3390/ijms241813786.
  • Ghetti FF, De Oliveira DG, De Oliveira JM, Ferreira LEVVDC, Cesar DE, Moreira APB. Effects of dietary intervention on gut microbiota and metabolic-nutritional profile of outpatients with Non-Alcoholic Steatohepatitis: a randomized clinical trial. J Gastrointestin Liver Dis. 2019;28(3):279–287. [ published Online First: 2019/09/14]. doi: 10.15403/jgld-197.
  • Valm AM, Welch JLM, Rieken CW, Hasegawa Y, Sogin ML, Oldenbourg R, Dewhirst FE, Borisy GG. Systems-level analysis of microbial community organization through combinatorial labeling and spectral imaging. Proc Natl Acad Sci. 2011;108(10):4152–4157. [ published Online First: 2011/02/16]. doi: 10.1073/pnas.1101134108.
  • Kragh KN, Alhede M, Kvich L, Bjarnsholt T. Into the well—A close look at the complex structures of a microtiter biofilm and the crystal violet assay. Biofilm. 2019;1:100006. [ published Online First: 2019/09/12]. doi:10.1016/j.bioflm.2019.100006.
  • Klopfleisch R. Multiparametric and semiquantitative scoring systems for the evaluation of mouse model histopathology–a systematic review. BMC Vet Res. 2013;9(1):123. [ published Online First: 2013/06/27]. doi: 10.1186/1746-6148-9-123.
  • Kolpen M, Kragh KN, Enciso JB, Faurholt-Jepsen D, Lindegaard B, Egelund GB, Jensen AV, Ravn P, Mathiesen IHM, Gheorge AG. et al. Bacterial biofilms predominate in both acute and chronic human lung infections. Thorax. 2022;77(10):1015–1022. [ published Online First: 2022/01/13]. doi:10.1136/thoraxjnl-2021-217576.
  • Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol. 2019;20(1):257. [ published Online First: 2019/11/28]. doi:10.1186/s13059-019-1891-0.
  • Lu J, Breitwieser FP, Thielen P, Salzberg SL. Bracken: estimating species abundance in metagenomics data. PeerJ Comput Sci. 2017;3:e104. [ published Online First: 2017/01/02]. doi:10.7717/peerj-cs.104.
  • Durinck S, Moreau Y, Kasprzyk A, Davis S, De Moor B, Brazma A, Huber W. BioMart and Bioconductor: a powerful link between biological databases and microarray data analysis. Bioinformatics. 2005;21(16):3439–3440. [ published Online First: 2005/08/06]. doi: 10.1093/bioinformatics/bti525.
  • Priya S, Burns MB, Ward T, Mars RAT, Adamowicz B, Lock EF, Kashyap PC, Knights D, Blekhman R. Identification of shared and disease-specific host gene–microbiome associations across human diseases using multi-omic integration. Nat Microbiol. 2022;7(6):780–795. [ published Online First: 2022/05/16]. doi: 10.1038/s41564-022-01121-z.
  • Nederlof I, De Bortoli D, Bareche Y, Nguyen B, de Maaker M, Hooijer GKJ, Buisseret L, Kok M, Smid M, Van den Eynden GGGM. et al. Comprehensive evaluation of methods to assess overall and cell-specific immune infiltrates in breast cancer. Breast Cancer Res. 2019;21(1):151. [ published Online First: 2019/12/28]. doi:10.1186/s13058-019-1239-4.
  • Finotello F, Trajanoski Z. Quantifying tumor-infiltrating immune cells from transcriptomics data. Cancer Immunol Immunother. 2018;67(7):1031–1040. [ published Online First: 2018/03/16]. doi: 10.1007/s00262-018-2150-z.
  • Sturm G, Finotello F, List M. Immunedeconv: an R package for unified access to computational methods for estimating immune cell fractions from bulk RNA-Sequencing data. Methods Mol Biol. 2020;2120:223–232. [ published Online First: 2020/03/04]. doi:10.1007/978-1-0716-0327-7_16.
  • Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43(7):e47–e47. [ published Online First: 2015/01/20]. doi: 10.1093/nar/gkv007.
  • Dejea CM, Wick EC, Hechenbleikner EM, White JR, Mark Welch JL, Rossetti BJ, Peterson SN, Snesrud EC, Borisy GG, Lazarev M. et al. Microbiota organization is a distinct feature of proximal colorectal cancers. Proc Natl Acad Sci U S A. 2014;111(51):18321–18326. [ published Online First: 2014/12/10]. doi:10.1073/pnas.1406199111.
  • Harvey KL, Jarocki VM, Charles IG, Djordjevic SP. The diverse functional roles of elongation factor tu (EF-Tu) in microbial pathogenesis. Front Microbiol. 2019;10:2351. [ published Online First: 2019/11/12.] doi:10.3389/fmicb.2019.02351.
  • Lima BP, Shi W, Lux R. Identification and characterization of a novel Fusobacterium nucleatum adhesin involved in physical interaction and biofilm formation with streptococcus gordonii. Microbiologyopen. 2017;6(3):e00444. [ published Online First: 2017/02/07]. doi:10.1002/mbo3.444.
  • Coppenhagen-Glazer S, Sol A, Abed J, Naor R, Zhang X, Han YW, Bachrach G. Fap2 of Fusobacterium nucleatum is a galactose-inhibitable adhesin involved in coaggregation, cell adhesion, and preterm birth. Infect Immun. 2015;83(3):1104–1113. [ published Online First: 2015/01/07]. doi: 10.1128/iai.02838-14.
  • Kaplan CW, Lux R, Haake SK, Shi W. The Fusobacterium nucleatum outer membrane protein RadD is an arginine-inhibitable adhesin required for inter-species adherence and the structured architecture of multispecies biofilm. Mol Microbiol. 2009;71(1):35–47. [ published Online First: 2008/11/15]. doi: 10.1111/j.1365-2958.2008.06503.x.
  • Liu PF, Shi W, Zhu W, Smith JW, Hsieh S-L, Gallo RL, Huang C-M. Vaccination targeting surface FomA of Fusobacterium nucleatum against bacterial co-aggregation: implication for treatment of periodontal infection and halitosis. Vaccine. 2010;28(19):3496–3505. [ published Online First: 2010/03/02]. doi: 10.1016/j.vaccine.2010.02.047.
  • Boleij A, Hechenbleikner EM, Goodwin AC, Badani R, Stein EM, Lazarev MG, Ellis B, Carroll KC, Albesiano E, Wick EC. et al. The Bacteroides fragilis toxin gene is prevalent in the colon mucosa of colorectal cancer patients. Clin Infect Dis. 2015;60(2):208–215. [ published Online First: 2014/10/12]. doi:10.1093/cid/ciu787.
  • Maeda K, Nagata H, Yamamoto Y, Tanaka M, Tanaka J, Minamino N, Shizukuishi S. Glyceraldehyde-3-phosphate dehydrogenase of Streptococcus oralis functions as a coadhesin for Porphyromonas gingivalis major fimbriae. Infect Immun. 2004;72(3):1341–1348. [ published Online First: 2004/02/24]. doi: 10.1128/iai.72.3.1341-1348.2004.
  • Benedetti F, Cocchi F, Latinovic OS, Curreli S, Krishnan S, Munawwar A, Gallo RC, Zella D. Role of mycoplasma chaperone DnaK in cellular transformation. Int J Mol Sci. 2020;21(4):1311. [ published Online First: 2020/02/23]. doi: 10.3390/ijms21041311.
  • Kinross J, Mirnezami R, Alexander J, Brown R, Scott A, Galea D, Veselkov K, Goldin R, Darzi A, Nicholson J. et al. A prospective analysis of mucosal microbiome-metabonome interactions in colorectal cancer using a combined MAS 1HNMR and metataxonomic strategy. Sci Rep. 2017;7(1):8979. [ published Online First: 2017/08/21]. doi:10.1038/s41598-017-08150-3.
  • Drewes JL, White JR, Dejea CM, Fathi P, Iyadorai T, Vadivelu J, Roslani AC, Wick EC, Mongodin EF, Loke MF. et al. High-resolution bacterial 16S rRNA gene profile meta-analysis and biofilm status reveal common colorectal cancer consortia. Npj Biofilms Microbiomes. 2017;3(1):34. [ published Online First: 2017/12/08]. doi:10.1038/s41522-017-0040-3.
  • Saffarian A, Mulet C, Regnault B, Amiot A, Tran-Van-Nhieu J, Ravel J, Sobhani I, Sansonetti PJ, Pédron T. et al. Crypt- and mucosa-associated core microbiotas in humans and their alteration in colon cancer patients. mBio. 2019;10(4). [ published Online First: 2019/07/18]. doi: 10.1128/mBio.01315-19.
  • Tahara T, Yamamoto E, Suzuki H, Maruyama R, Chung W, Garriga J, Jelinek J, Yamano H-O, Sugai T, An B. et al. Fusobacterium in colonic flora and molecular features of colorectal carcinoma. Cancer Res. 2014;74(5):1311–1318. [ published Online First: 2014/01/05]. doi:10.1158/0008-5472.can-13-1865.
  • Bullman S, Pedamallu CS, Sicinska E, Clancy TE, Zhang X, Cai D, Neuberg D, Huang K, Guevara F, Nelson T. et al. Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer. Science. 2017;358(6369):1443–1448. [ published Online First: 2017/11/25]. doi:10.1126/science.aal5240.
  • Younginger BS, Mayba O, Reeder J, Nagarkar DR, Modrusan Z, Albert ML, Byrd AL. Enrichment of oral-derived bacteria in inflamed colorectal tumors and distinct associations of Fusobacterium in the mesenchymal subtype. Cell Rep Med. 2023;4(2):100920. [ published Online First: 2023/01/28]. doi: 10.1016/j.xcrm.2023.100920.
  • Chen Y, Huang Z, Tang Z, Huang Y, Huang M, Liu H, Ziebolz D, Schmalz G, Jia B, Zhao J. et al. More than just a periodontal pathogen –the research progress on Fusobacterium nucleatum. Front Cell Infect Microbiol. 2022;12:815318. [ published Online First: 2022/02/22]. doi:10.3389/fcimb.2022.815318.
  • Salvucci M, Crawford N, Stott K, Bullman S, Longley DB, Prehn JHM. Patients with mesenchymal tumours and high fusobacteriales prevalence have worse prognosis in colorectal cancer (CRC). Gut. 2022;71(8):1600–1612. [ published Online First: 2021/09/10]. doi:10.1136/gutjnl-2021-325193.
  • Zhao H, Wu L, Yan G, Chen Y, Zhou M, Wu Y, Li Y. Inflammation and tumor progression: signaling pathways and targeted intervention. Signal Transduct Target Ther. 2021;6(1):263. [ published Online First: 2021/07/13]. doi: 10.1038/s41392-021-00658-5.
  • Zhou J, Nefedova Y, Lei A, Gabrilovich D. Neutrophils and PMN-MDSC: their biological role and interaction with stromal cells. Semin Immunol. 2018;35:19–28. [ published Online First: 2017/12/20]. doi:10.1016/j.smim.2017.12.004.
  • Waldner MJ, Foersch S, Neurath MF. Interleukin-6–a key regulator of colorectal cancer development. Int J Biol Sci. 2012;8(9):1248–1253. [ published Online First: 2012/11/09]. doi: 10.7150/ijbs.4614.
  • Löwenmark T, Li X, Löfgren-Burström A, Zingmark C, Ling A, Kellgren TG, Larsson P, Ljuslinder I, Wai SN, Edin S. et al. Parvimonas micra is associated with tumour immune profiles in molecular subtypes of colorectal cancer. Cancer Immunol Immunother. 2022;71(10):2565–2575. [ published Online First: 2022/03/19]. doi:10.1007/s00262-022-03179-4.
  • Qiao H, Li H, Wen X, Tan X, Yang C, Liu N. Multi-omics integration reveals the crucial role of Fusobacterium in the inflammatory immune microenvironment in head and neck squamous cell carcinoma. Microbiol Spectr. 2022;10(4):e0106822. [ published Online First: 2022/07/22]. doi: 10.1128/spectrum.01068-22.
  • Brennan CA, Clay SL, Lavoie SL, Bae S, Lang JK, Fonseca-Pereira D, Rosinski KG, Ou N, Glickman JN, Garrett WS. et al. Fusobacterium nucleatum drives a pro-inflammatory intestinal microenvironment through metabolite receptor-dependent modulation of IL-17 expression. Gut Microbes. 2021;13(1):1987780. [ published Online First: 2021/11/17]. doi:10.1080/19490976.2021.1987780.
  • Lee JA, Yoo SY, Oh HJ, Jeong S, Cho N-Y, Kang GH, Kim JH. Differential immune microenvironmental features of microsatellite-unstable colorectal cancers according to Fusobacterium nucleatum status. Cancer Immunol Immunother. 2021;70(1):47–59. [ published Online First: 2020/07/06]. doi: 10.1007/s00262-020-02657-x.
  • Queen J, Zhang J, Sears CL. Oral antibiotic use and chronic disease: long-term health impact beyond antimicrobial resistance and Clostridioides difficile. Gut Microbes. 2020;11(4):1092–1103. [ published Online First: 2020/02/11]. doi:10.1080/19490976.2019.1706425.