Potential role of bacterial pathogens in the immunopathogenesis of ovarian cancer

Wiktoria Wierzbińska; Olga Kuźmycz

doi:10.18778/1730-2366.18.15

Autor

Wiktoria Wierzbińska BioMedChem Doctoral School of the University of Lodz and Lodz Institutes of the Polish Academy of Sciences, Poland; University of Lodz, Faculty of Biology, Department of Molecular Microbiology, Poland
Olga Kuźmycz University of Lodz, Faculty of Biology, Department of Molecular Microbiology, Poland https://orcid.org/0000-0002-1709-2971

DOI:

https://doi.org/10.18778/1730-2366.18.15

Słowa kluczowe:

microbiota, TME, OC microbiota, ovarian microbiota

Abstrakt

The development of next-generation sequencing (NGS) techniques allowed conducting research with greater efficiency and determining the microbial pattern of niches in the human body that were previously considered sterile. Observed changes in the microbiome composition of patients with cancer lesions increasingly indicate the role of microorganisms in the tumour induction and progression. Overgrowth of certain pathogenic strains within the tissue may cause inflammation, which in its chronic form may lead to destabilization of host genome. Such changes may result in altering the expression of genes encoding proteins involved in significant metabolic pathways and promote pathogenic cell functions such as proliferation stimulation, apoptosis inhibition and modulation of inflammatory response. Consequently, these events may lead to tissue destruction, disruption of physiological processes and development of disease states including cancer. In light of emerging reports on the role of changes in the composition of the microbiota in tumorigenesis induction and the presence of pathogenic strains in the ovarian cancer (OC) tumour microenvironment (TME), the hypothesis of a potential role for bacteria in the pathogenesis of this cancer is also gaining interest. The following review presents a summary of scientific research indicating potential role of TME bacteria in the immunopathogenesis of OC.

Pobrania

Brak dostępnych danych do wyświetlenia.

Bibliografia

Anderson, N.M., Simon, M.C. 2020. The tumor microenvironment. Current biology: CB, 30(16), R921–R925.
Google Scholar DOI: https://doi.org/10.1016/j.cub.2020.06.081

Asangba, A.E., Chen, J., Goergen, K.M., Larson, M.C., Oberg, A.L., Casarin, J., Multinu, F., Kaufmann, S.H., Mariani, A., Chia, N., Walther-Antonio, M.R.S. 2023. Diagnostic and prognostic potential of the microbiome in ovarian cancer treatment response. Scientific Reports, 13(1), 730.
Google Scholar DOI: https://doi.org/10.1038/s41598-023-27555-x

Baker, J.M., Chase, D.M., Herbst-Kralovetz, M.M. 2018. Uterine Microbiota: Residents, Tourists, or Invaders? Frontiers in immunology, 9, 208.
Google Scholar DOI: https://doi.org/10.3389/fimmu.2018.00208

Banerjee, S., Tian, T., Wei, Z., Shih, N., Feldman, M.D., Alwine, J.C., Coukos, G., Robertson, E.S. 2017. The ovarian cancer oncobiome. Oncotarget, 8(22), 36225–36245.
Google Scholar DOI: https://doi.org/10.18632/oncotarget.16717

Basith, S., Manavalan, B., Yoo, T.H., Kim, S.G., Choi, S. 2012. Roles of toll-like receptors in cancer: a double-edged sword for defense and offense. Archives of Pharmacal Research, 35(8), 1297–1316.
Google Scholar DOI: https://doi.org/10.1007/s12272-012-0802-7

Bossowska-Nowicka M., Dembele K., Toka F. 2015. Udział receptorów Toll-podobnych w patogenezie atopowego zapalenia skóry u ludzi i zwierząt. Cz. 1 Rola receptorów Toll-podobnych w odporności. Życie Weterynaryjne. 2015:789–792.
Google Scholar

Bowtell, D.D., Böhm, S., Ahmed, A.A., Aspuria, P.J., Bast, R.C., Jr, Beral, V., Berek, J.S., Birrer, M.J., Blagden, S., Bookman, M.A., Brenton, J.D., Chiappinelli, K.B., Martins, F.C., Coukos, G., Drapkin, R., Edmondson, R., Fotopoulou, C., Gabra, H., Galon, J., Gourley, C., Heong V, Huntsman, D.G., Iwanicki, M., Karlan, B.Y., Kaye, A., Lengyel, E., Levine, D.A., Lu, K.H., McNeish, I.A., Menon, U., Narod, S.A., Nelson, B.H., Nephew, K.P., Pharoah, P., Powell, D.J Jr., Ramos, P, Romero, I.L., Scott C.L., Sood, A.K., Stronach, E.A., Balkwill, F.R. 2015. Rethinking ovarian cancer II: reducing mortality from high-grade serous ovarian cancer. Nature Reviews. Cancer, 15(11), 668–679.
Google Scholar DOI: https://doi.org/10.1038/nrc4019

Brewster, W.R., Burkett, W.C., Ko, E.M., Bae-Jump, V., Nicole McCoy, A., Keku, T.O. 2022. An evaluation of the microbiota of the upper reproductive tract of women with and without epithelial ovarian cancer. Gynecologic Oncology Reports, 42, 101017.
Google Scholar DOI: https://doi.org/10.1016/j.gore.2022.101017

Carmeliet P. 2005. VEGF as a key mediator of angiogenesis in cancer. Oncology, 69 Suppl 3, 4–10.
Google Scholar DOI: https://doi.org/10.1159/000088478

Chen, C., Song, X., Wei, W., Zhong, H., Dai, J., Lan, Z., Li, F., Yu, X., Feng, Q., Wang, Z., Xie, H., Chen, X., Zeng, C., Wen, B., Zeng, L., Du, H., Tang, H., Xu, C., Xia, Y., Xia, H., Yang H, Wang J, Wang J, Madsen L, Brix S, Kristiansen K, Xu X, Li J, Wu R, Jia, H. 2017. The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases. Nature Communications, 8(1), 875.
Google Scholar DOI: https://doi.org/10.1038/s41467-017-00901-0

Chen, P., Guo, Y., Jia, L., Wan, J., He, T., Fang, C., Li, T. 2021. Interaction Between Functionally Activate Endometrial Microbiota and Host Gene Regulation in Endometrial Cancer. Frontiers in Cell and Developmental Biology, 9, 727286.
Google Scholar DOI: https://doi.org/10.3389/fcell.2021.727286

Crum, C.P., Drapkin, R., Miron, A., Ince, T.A., Muto, M., Kindelberger, D.W., Lee, Y. 2007. The distal fallopian tube: a new model for pelvic serous carcinogenesis. Current Opinion in Obstetrics & Gynecology, 19(1), 3–9.
Google Scholar DOI: https://doi.org/10.1097/GCO.0b013e328011a21f

Di Tucci C, De Vito I, Muzii L. 2023. Immune-Onco-Microbiome: A New Revolution for Gynecological Cancers. Biomedicines. 2023;11(3):782.
Google Scholar DOI: https://doi.org/10.3390/biomedicines11030782

Ding, D.N., Xie, L.Z., Shen, Y., Li, J., Guo, Y., Fu, Y., Liu, F. Y., Han, F. J. 2021. Insights into the Role of Oxidative Stress in Ovarian Cancer. Oxidative Medicine and Cellular Longevity, 2021, 8388258.
Google Scholar DOI: https://doi.org/10.1155/2021/8388258

Ducie, J., Dao, F., Considine, M., Olvera, N., Shaw, P.A., Kurman, R.J., Shih, I.M., Soslow, R.A., Cope, L., Levine, D. A. 2017. Molecular analysis of high-grade serous ovarian carcinoma with and without associated serous tubal intra-epithelial carcinoma. Nature Communications, 8(1), 990.
Google Scholar DOI: https://doi.org/10.1038/s41467-017-01217-9

Fortner, R.T., Poole, E.M., Wentzensen, N.A., Trabert, B., White, E., Arslan, A.A., Patel, A.V., Setiawan, V.W., Visvanathan, K., Weiderpass, E., Adami, H.O., Black, A., Bernstein, L., Brinton, L.A., Buring, J., Clendenen, T.V., Fournier, A., Fraser, G., Gapstur, S.M., Gaudet, M.M., Giles, G.G., Gram, I.T., Hartge, P., Hoffman-Bolton, J., Idahl, A., Kaaks, R., Kirsh, V.A., Knutsen, S., Koh, W.P., Lacey, J.V.Jr., Lee, I.M., Lundin E., Merritt, M.A., Milne, R. L., Onland-Moret, N.C., Peters, U., Poynter, J. N., Rinaldi, S., Robien, K., Rohan, T., Sánchez, M.J., Schairer, C., Schouten, L.J., Tjonneland, A., Townsend, M.K., Travis, R.C., Trichopoulou, A., van den Brandt, P.A., Vineis, P., Wilkens, L., Wolk, A., Yang, H.P., Zeleniuch-Jacquotte, A., Tworoger, S.S. 2019. Ovarian cancer risk factors by tumor aggressiveness: An analysis from the Ovarian Cancer Cohort Consortium. International Journal of Cancer, 145(1), 58–69.
Google Scholar DOI: https://doi.org/10.1002/ijc.32075

Francescone R, Hou V, Grivennikov S.I. 2014. Microbiome, inflammation, and cancer. Cancer Journal. 2014;20(3):181-189.
Google Scholar DOI: https://doi.org/10.1097/PPO.0000000000000048

Galeano Niño, J.L., Wu, H., LaCourse, K.D., Kempchinsky, A.G., Baryiames, A., Barber, B., Futran, N., Houlton, J., Sather, C., Sicinska, E., Taylor, A., Minot, S.S., Johnston, C.D., Bullman, S. 2022. Effect of the intratumoral microbiota on spatial and cellular heterogeneity in cancer. Nature, 611(7937), 810–817.
Google Scholar DOI: https://doi.org/10.1038/s41586-022-05435-0

Hansen L.K., Becher N., Bastholm S., Glavind J., Ramsing M., Kim C.J., Romero R., Jensen J.S., Uldbjerg N. 2014. The cervical mucus plug inhibits, but does not block, the passage of ascending bacteria from the vagina during pregnancy. Acta Obstetricia et Gynecologica Scandinavica, 93(1):102–118.
Google Scholar DOI: https://doi.org/10.1111/aogs.12296

Human Microbiome Project Consortium. 2012. Structure, function and diversity of the healthy human microbiome. Nature, 486(7402), 207–214.
Google Scholar DOI: https://doi.org/10.1038/nature11234

Janeway, C.A. Jr, Medzhitov, R. 2002. Innate immune recognition. Annual Review of Immunology, 20, 197–216.
Google Scholar DOI: https://doi.org/10.1146/annurev.immunol.20.083001.084359

Knudson, A.G. Jr. 1971. Mutation and cancer: statistical study of retinoblastoma. Proceedings of the National Academy of Sciences of the United States of America, 68, 820–823.
Google Scholar DOI: https://doi.org/10.1073/pnas.68.4.820

Kostic A.D., Gevers D., Pedamallu C.S., Michaud M., Duke F., Earl A. M., Ojesina A.I., Jung J., Bass A.J., Tabernero J., Baselga J., Liu C., Shivdasani R.A., Ogino S., Birren B.W., Huttenhower C., Garrett W.S., Meyerson M. 2012. Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Research, 22(2), 292–298.
Google Scholar DOI: https://doi.org/10.1101/gr.126573.111

Kunz G., Leyendecker G. 2002. Uterine peristaltic activity during the menstrual cycle: characterization, regulation, function, and dysfunction. Reproductive BioMedicine Online, 4, 5–9.
Google Scholar DOI: https://doi.org/10.1016/S1472-6483(12)60108-4

Łaniewski, P., Ilhan, Z.E., Herbst-Kralovetz, M.M. 2020. The microbiome and gynaecological cancer development, prevention and therapy. Nature Reviews. Urology, 17(4), 232–250.
Google Scholar DOI: https://doi.org/10.1038/s41585-020-0286-z

Li C., Gu Y., He Q., Huang, J., Song Y., Wan X., Li Y. 2021. Integrated Analysis of Microbiome and Transcriptome Data Reveals the Interplay Between Commensal Bacteria and Fibrin Degradation in Endometrial Cancer. Frontiers in Cellular and Infection Microbiology, 11:748558.
Google Scholar DOI: https://doi.org/10.3389/fcimb.2021.748558

Liu, T., Zhang, L., Joo, D., Sun, S.C. 2017. NF-κB signaling in inflammation. Signal transduction and targeted therapy, 2, 17023.
Google Scholar DOI: https://doi.org/10.1038/sigtrans.2017.23

Lu, W., He, F., Lin, Z., Liu, S., Tang, L., Huang, Y., Hu, Z. 2021. Dysbiosis of the endometrial microbiota and its association with inflammatory cytokines in endometrial cancer. International Journal of Cancer, 148(7), 1708–1716.
Google Scholar DOI: https://doi.org/10.1002/ijc.33428

Majewska M, Szczepanik M. 2006. Rola receptorów toll-podobnych (TLR) w odporności wrodzonej i nabytej oraz ich funkcja w regulacji odpowiedzi immunologicznej. Postępy Higieny i Medycyny Doświadczalnej 60(null):52–63.
Google Scholar

Miles, S.M., Hardy, B.L., Merrell, D.S. 2017. Investigation of the microbiota of the reproductive tract in women undergoing a total hysterectomy and bilateral salpingo-oopherectomy. Fertility and Sterility, 107(3), 813–820.e1.
Google Scholar DOI: https://doi.org/10.1016/j.fertnstert.2016.11.028

Nomura A., Stemmermann G.N., Chyou P.H., Kato I., Perez-Perez G.I., Blaser M.J. 1991. Helicobacter pylori infection and gastric carcinoma among Japanese Americans in Hawaii. New England Journal of Medicine, 17, 325(16), 1132–1136.
Google Scholar DOI: https://doi.org/10.1056/NEJM199110173251604

Pan, Z., Xie, X. 2017. BRCA mutations in the manifestation and treatment of ovarian cancer. Oncotarget, 8(57), 97657–97670.
Google Scholar DOI: https://doi.org/10.18632/oncotarget.18280

Pelzer, E.S., Allan, J A., Waterhouse, M.A., Ross, T., Beagley, K.W., Knox, C.L. 2013. Microorganisms within human follicular fluid: effects on IVF. PloS one, 8(3), e59062.
Google Scholar DOI: https://doi.org/10.1371/journal.pone.0059062

Pelzer, E.S., Allan, J.A., Cunningham, K., Mengersen, K., Allan, J.M., Launchbury, T., Beagley, K., Knox, C.L. 2011. Microbial colonization of follicular fluid: alterations in cytokine expression and adverse assisted reproduction technology outcomes. Human Reproduction (Oxford, England), 26(7), 1799–1812.
Google Scholar DOI: https://doi.org/10.1093/humrep/der108

Punzón-Jiménez P., Labarta E. 2021. The impact of the female genital tract microbiome in women health and reproduction: a review. Journal of Assisted Reproduction and Genetics, 38(10), 2519–2541.
Google Scholar DOI: https://doi.org/10.1007/s10815-021-02247-5

Rudnicka K., Backert S., Chmiela M. 2019. Genetic Polymorphisms in Inflammatory and Other Regulators in Gastric Cancer: Risks and Clinical Consequences. Current topics in microbiology and immunology, 421, 53–76.
Google Scholar DOI: https://doi.org/10.1007/978-3-030-15138-6_3

Schwabe, R.F., Jobin, C. 2013. The microbiome and cancer. Nature Reviews. Cancer, 13(11), 800–812.
Google Scholar DOI: https://doi.org/10.1038/nrc3610

Shahanavaj K., Gil-Bazo I., Castiglia M., Bronte G., Passiglia F., Carreca A.P., del Pozo J.L., Russo A., Peeters M., Rolfo C. 2015. Cancer and the microbiome: Potential applications as new tumor biomarker. Expert review of anticancer therapy, 2015; 15:317–330.
Google Scholar DOI: https://doi.org/10.1586/14737140.2015.992785

Sudipta P., Jacek R. Wilczyński J.R., Paradowska E. 2020. Factors in Oncogenesis: Viral Infections in Ovarian Cancer. Cancers, 12(3), 561.
Google Scholar DOI: https://doi.org/10.3390/cancers12030561

Sung, H., Ferlay, J., Siegel, R.L., Laversanne, M., Soerjomataram, I., Jemal, A., Bray, F. 2021. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA: A Cancer Journal for Clinicians, 71(3), 209–249.
Google Scholar DOI: https://doi.org/10.3322/caac.21660

Swidsinski A., Verstraelen H., Loening-Baucke V., Swidsinski S., Mendling W., Halwani Z. 2013. Presence of a polymicrobial endometrial biofilm in patients with bacterial vaginosis. PLOS One, 8(1): e53997.
Google Scholar DOI: https://doi.org/10.1371/journal.pone.0053997

Tao X., Franasiak J. M., Zhan Y., Scott R. T., Rajchel J., Bedard J., Newby R. J., Treff N. R., Chu T. 2017. Characterizing the endometrial microbiome by analyzing the ultra-low bacteria from embryo transfer catheter tips in IVF cycles: next generation sequencing (NGS) analysis of the 16S ribosomal gene. Human Microbiome Journal, 3: 15-21.
Google Scholar DOI: https://doi.org/10.1016/j.humic.2017.01.004

Vakkila, J., Lotze, M.T. 2004. Inflammation and necrosis promote tumour growth. Nature Reviews. Immunology, 4(8), 641–648.
Google Scholar DOI: https://doi.org/10.1038/nri1415

Walsh, D.M., Hokenstad, A.N., Chen, J., Sung, J., Jenkins, G. D., Chia, N., Nelson, H., Mariani, A., Walther-Antonio, M.R.S. 2019. Postmenopause as a key factor in the composition of the Endometrial Cancer Microbiome (ECbiome). Scientific Reports, 9(1), 19213.
Google Scholar DOI: https://doi.org/10.1038/s41598-019-55720-8

Walther-António, M.R., Chen, J., Multinu, F., Hokenstad, A., Distad, T.J., Cheek, E.H., Keeney, G.L., Creedon, D.J., Nelson, H., Mariani, A., Chia, N. 2016. Potential contribution of the uterine microbiome in the development of endometrial cancer. Genome Medicine, 8(1), 122.
Google Scholar DOI: https://doi.org/10.1186/s13073-016-0368-y

Wang, Q., Zhao, L., Han, L., Fu, G., Tuo, X., Ma, S., Li, Q., Wang, Y., Liang, D., Tang, M., Sun, C., Wang, Q., Song, Q., Li, Q. 2020. The differential distribution of bacteria between cancerous and noncancerous ovarian tissues in situ. Journal of Ovarian Research, 13(1), 8.
Google Scholar DOI: https://doi.org/10.1186/s13048-019-0603-4

Zervomanolakis, I., Ott, H.W., Hadziomerovic, D., Mattle, V., Seeber, B.E., Virgolini, I., Heute, D., Kissler, S., Leyendecker, G., Wildt, L. 2007. Physiology of upward transport in the human female genital tract. Annals of the New York Academy of Sciences, 1101, 1–20.
Google Scholar DOI: https://doi.org/10.1196/annals.1389.032

Zhou, B., Sun, C., Huang, J., Xia, M., Guo, E., Li, N., Lu, H., Shan, W., Wu, Y., Li, Y., Xu, X., Weng, D., Meng, L., Hu, J., Gao, Q., Ma, D., Chen, G. 2019. The biodiversity Composition of Microbiome in Ovarian Carcinoma Patients. Scientific Reports, 9(1), 1691.
Google Scholar DOI: https://doi.org/10.1038/s41598-018-38031-2