Микробиота в диагностике, терапии и профилактике рака
https://doi.org/10.17650/1726-9784-2024-23-4-10-21
Аннотация
Введение. Углубленное изучение участия микробиоты в патогенезе опухолей открыло новые возможности для разработки альтернативных подходов к диагностике, терапии и профилактике злокачественных новообразований.
Цель исследования – обобщить данные практического использования особенностей профиля микробиоты в качестве маркера канцерогенеза и диагностики, а также рассмотреть ее участие в комбинированном лечении и профилактике рака.
Материалы и методы. Проведен поиск литературы по базам данных NCBI MedLine (PubMed), Scopus, web of Science с использованием ключевых слов, определяющих цель исследования. Анализировали результаты оригинальных исследований, метаанализов, рандомизированных контролируемых клинических исследований, рассматривали традиционные, систематические и зонтичные обзоры, опубликованные в последние годы.
Результаты. Качественные и количественные изменения состава микробиоты, связанные с патогенезом онкологических заболеваний, дают возможность их использования в качестве маркеров для определения риска злокачественных новообразований и прогноза широкого спектра опухолей. Механизмы, определяющие использование микробиоты в противоопухолевой терапии, разнообразны. Действие на иммунную систему является наиболее значимым. Большой интерес представляют искусственно создаваемые гибридные наночастицы, покрытые мембраной бактериальных везикул и опухолевых клеток для активации специфического противоопухолевого иммунитета. Для профилактики рака фундаментальное обоснование получило использование про-, преи синбиотиков, открытых И.И. Мечниковым.
Заключение. Комплекс научных геномных и эпигенетических данных, полученных в механистических и эпидемиологических исследованиях, посвященных роли микробиоты в патогенезе опухолей, в настоящее время оценивается как наиболее значимый результат, обосновывающий ее практическое применение в качестве компонента диагностики, терапии и профилактики рака.
Ключевые слова
Об авторах
Л. Г. СоленоваРоссия
Лия Геннадьевна Соленова
115522 Москва, Каширское шоссе, 24
Н. И. Рыжова
Россия
115522 Москва, Каширское шоссе, 24
Г. А. Белицкий
Россия
115522 Москва, Каширское шоссе, 24
И. А. Антонова
Россия
115522 Москва, Каширское шоссе, 24
К. И. Кирсанов
Россия
115522 Москва, Каширское шоссе, 24; 117198 Москва, ул. Миклухо-Маклая, 6
М. Г. Якубовская
Россия
115522 Москва, Каширское шоссе, 24; 117198 Москва, ул. Миклухо-Маклая, 6
Список литературы
1. Busch W. Aus der Sitzung der medicinischen Section vom 13 November 1867. Berlin Klin Wochenschr. 1868;5:137. (Ger).
2. Fehleisen F. Ueber die Züchtung der Erysipelkokken auf künstlichem Nährboden und ihre Übertragbarkeit auf den Menschen. Dtsch Med Wochenschr 1882;8:553–4. (In Germ.).
3. Coley W.B. The treatment of malignant inoperable tumors with the mixed toxins of erysipelas and Bacillus prodigiosus. Brussels: M Weissenbruch, 1914. URL: https://archive.org/details/McGillLibrary-osl_treatment-tumors_C69588t1914-17842/ page/n3/mode/2up
4. Yen S., Johnson J.S. Metagenomics: a path to understanding the gut microbiome. Mamm Genome 2021;32(4):282–96. DOI: 10.1007/s00335-021-09889-x
5. Wensel C.R., Pluznick J.L., Salzberg S.L., Sears C.L. Nextgeneration sequencing: insights to advance clinical investigations of the microbiome. J Clin Invest 2022;132(7):e154944. DOI: 10.1172/JCI154944
6. Shirazi M.S.R, Al-Alo K.Z.K., Al-Yasiri M.H. et al. Microbiome dysbiosis and predominant bacterial species as human cancer biomarkers. J Gastrointest Cancer 2020;51(3):725–8. DOI: 10.1007/s12029-019-00311-z
7. Dan W., Peng L., Yan B. et al. Human microbiota in esophageal adenocarcinoma: pathogenesis, diagnosis, prognosis and therapeutic implications. Front Microbiol 2022;12:791274. DOI: 10.3389/fmicb.2021.791274
8. Zhang X., Hoffman K.L., Wei P. et al. Baseline oral microbiome and all-cancer incidence in a cohort of nonsmoking Mexican American women. Cancer Prev Res (Phila) 2021;14(3):383–92. DOI: 10.1158/1940-6207.CAPR-20-0405
9. Su S.C., Chang L.C., Huang H.D. et al. Oral microbial dysbiosis and its performance in predicting oral cancer. Carcinogenesis 2021;42(1):127–35. DOI: 10.1093/carcin/bgaa062
10. Rai A.K., Panda M., Das A.K. et al. Dysbiosis of salivary microbiome and cytokines influence oral squamous cell carcinoma through inflammation. Arch Microbiol 2021;203(1):137–52. DOI: 10.1007/s00203-020-02011-w
11. Park S.Y., Hwang B.O., Lim M. et al. Oral-gut microbiome axis in gastrointestinal disease and cancer. Cancers (Basel) 2021;13(9):2124. DOI: 10.3390/cancers13092124
12. Sun J., Tang Q., Yu S. et al. Role of the oral microbiota in cancer evolution and progression. Cancer Med 2020;9(17):6306–21. DOI: 10.1002/cam4.3206
13. Stasiewicz M., Kwaśniewski M., Karpiński T.M. Microbial associations with pancreatic cancer: a new frontier in biomarkers. Cancers (Basel) 2021;13(15):3784. DOI: 10.3390/cancers13153784
14. Yamamura K., Baba Y., Nakagawa S. et al. Human microbiome Fusobacterium nucleatum in esophageal cancer tissue is associated with prognosis. Clin Cancer Res 2016;22(22):5574–81. DOI: 10.1158/1078-0432.CCR-16-1786
15. Zhang S., Kong C., Yang Y. et al. Human oral microbiome dysbiosis as a novel non-invasive biomarker in detection of colorectal cancer. Theranostics 2020;10(25):11595–606. DOI: 10.7150/thno.49515
16. Kim M., Vogtmann E., Ahlquist D.A. et al. Fecal metabolomic signatures in colorectal adenoma patients are associated with gut microbiota and early events of colorectal cancer pathogenesis. mBio 2020;11(1):e03186–19. DOI: 10.1128/mBio.03186-19
17. Gao R., Wang Z., Li H. et al. Gut microbiota dysbiosis signature is associated with the colorectal carcinogenesis sequence and improves the diagnosis of colorectal lesions. J Gastroenterol Hepatol 2020;35(12):2109–21. DOI: 10.1111/jgh.15077
18. Li N., Bai C., Zhao L. et al. Characterization of the fecal microbiota in gastrointestinal cancer patients and healthy people. Clin Transl Oncol 2022;24(6):1134–47. DOI: 10.1007/s12094-021-02754-y
19. Ren Z., Li A., Jiang J. et al. Gut microbiome analysis as a tool towards targeted non-invasive biomarkers for early hepatocellular carcinoma. Gut 2019;68(6):1014–23. DOI: 10.1136/gutjnl-2017-315084
20. Wheatley R.C., Kilgour E., Jacobs T. et al. Potential influence of the microbiome environment in patients with biliary tract cancer and implications for therapy. Br J Cancer 2022;126(5):693–705. DOI: 10.1038/s41416-021-01583-8
21. Kirishima M., Yokoyama S., Matsuo K. et al. Gallbladder microbiota composition is associated with pancreaticobiliary and gallbladder cancer prognosis. BMC Microbiol 2022;22(1):147. DOI: 10.1186/s12866-022-02557-3
22. Zhuang H., Cheng L., Wang Y. et al. Dysbiosis of the gut microbiome in lung cancer. Front Cell Infect Microbiol 2019;9:112. DOI: 10.3389/fcimb.2019.00112
23. Zheng Y., Fang Z., Xue Y. et al. Specific gut microbiome signature predicts the early-stage lung cancer. Gut Microbes 2020;11(4):1030–42. DOI: 10.1080/19490976.2020.1737487
24. Zhao F., An R., Wang L. et al. Specific gut microbiome and serum metabolome changes in lung cancer patients. Front Cell Infect Microbiol 2021;11:725284. DOI: 10.3389/fcimb.2021.725284
25. Laliani G., Ghasemian Sorboni S., Lari R. et al. Bacteria and cancer: different sides of the same coin. Life Sci 2020;246:117398. DOI: 10.1016/j.lfs.2020.117398
26. Nomura M. Association of the gut microbiome with cancer immunotherapy. Int J Clin Oncol 2023;28(3):347–53. DOI: 10.1007/s10147-022-02180-2
27. Matson V., Fessler J., Bao R. et al. The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science 2018;359(6371):104–8. DOI: 10.1126/science.aao3290
28. Davar D., Dzutsev A.K., McCulloch J.A. et al. Fecal microbiota transplant overcomes resistance to anti-PD-1 therapy in melanoma patients. Science 2021;371(6529):595–602. DOI: 10.1126/science.abf3363
29. Tomita Y., Ikeda T., Sakata S. et al. Association of probiotic Clostridium butyricum therapy with survival and response to immune checkpoint blockade in patients with lung cancer. Cancer Immunol Res 2020;8(10):1236–42. DOI: 10.1158/2326-6066.CIR-20-0051
30. Gupta K.H., Nowicki C., Giurini E.F. et al. Bacterial-based cancer therapy (BBCT): recent advances, current challenges, and future prospects for cancer immunotherapy. Vaccines (Basel) 2021;9(12):1497. DOI: 10.3390/vaccines9121497
31. Routy B., Le Chatelier E., Derosa L. et al. Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors. Science 2018;359(6371):91–7. DOI: 10.1126/science.aan3706
32. Лаптева О.Г. Разработка способа глубинного культивирования вакцинного штамма Mycoplasma mycoides subsp. mycoides. Ветеринария сегодня 2023;12(2):158–63. DOI: 10.29326/2304-196X-2023-12-2-158-163
33. Huang X., Li M., Hou S., Tian B. Role of the microbiome in systemic therapy for pancreatic ductal adenocarcinoma (Review). Int J Oncol 2021;59(6):101. DOI: 10.3892/ijo.2021.5281
34. Vitiello G.A., Cohen D.J., Miller G. Harnessing the microbiome for pancreatic cancer immunotherapy. Trends Cancer 2019;5(11):670–6. DOI: 10.1016/j.trecan.2019.10.005
35. Leinwand J., Miller G. Regulation and modulation of antitumor immunity in pancreatic cancer. Nat Immunol 2020;21(10): 1152–9. DOI: 10.1038/s41590-020-0761-y
36. Gopalakrishnan V., Spencer C.N., Nezi L. et al. Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients. Science 2018;359(6371):97–103. DOI: 10.1126/science.aan4236
37. Limeta A., Ji B., Levin M. et al. Meta-analysis of the gut microbiota in predicting response to cancer immunotherapy in metastatic melanoma. JCI Insight 2020;5(23):e140940. DOI: 10.1172/jci.insight.140940
38. Szczyrek M., Bitkowska P., Chunowski P. et al. Diet, microbiome, and cancer immunotherapy – a comprehensive review. Nutrients 2021;13(7):2217. DOI: 10.3390/nu13072217
39. Peters B.A., Wilson M., Moran U. et al. Relating the gut metagenome and metatranscriptome to immunotherapy responses in melanoma patients. Genome Med 2019;11(1):61. DOI: 10.1186/s13073-019-0672-4
40. Sharma P.C., Sharma D., Sharma A. et al. Recent advances in microbial toxin-related strategies to combat cancer. Semin Cancer Biol 2022;86(Pt 3):753–68. DOI: 10.1016/j.semcancer.2021.07.007
41. Khoshnood S., Fathizadeh H., Neamati F. et al. Bacteria-derived chimeric toxins as potential anticancer agents. Front Oncol 2022;12:953678. DOI: 10.3389/fonc.2022.953678
42. Erwert R.D, Eiting K.T., Tupper J.C. et al. Shiga toxin induces decreased expression of the anti-apoptotic protein Mcl-1 concomitant with the onset of endothelial apoptosis. Microb Pathog 2003;35(2):87–93. DOI: 10.1016/s0882-4010(03)00100-1
43. Robert A., Wiels J. Shiga toxins as antitumor tools. Toxins (Basel) 2021;13(10):690. DOI: 10.3390/toxins13100690
44. Trivanović D., Pavelić K., Peršurić Ž. Fighting cancer with bacteria and their toxins. Int J Mol Sci 2021;22(23):12980. DOI: 10.3390/ijms222312980
45. LaCourse K.D., Zepeda-Rivera M., Kempchinsky A.G. et al. The cancer chemotherapeutic 5-fluorouracil is a potent Fusobacterium nucleatum inhibitor and its activity is modified by intratumoral microbiota. Cell Rep 2022;41(7):111625. DOI: 10.1016/j.celrep.2022.111625
46. Kim O.Y., Dinh N.T., Park H.T. et al. Bacterial protoplastderived nanovesicles for tumor targeted delivery of chemotherapeutics. Biomaterials 2017;113:68-79. DOI: 10.1016/j.biomaterials.2016.10.037
47. Sartorio M.G., Pardue E.J., Feldman M.F., Haurat M.F. Bacterial outer membrane vesicles: from discovery to applications. Annu Rev Microbiol 2021;75:609–30. DOI: 10.1146/annurev-micro-052821-031444
48. Tropini C., Earle K.A., Huang K.C., Sonnenburg J.L. The gut microbiome: connecting spatial organization to function. Cell Host Microbe 2017;21(4):433–42. DOI: 10.1016/j.chom.2017.03.010
49. Turner L., Bitto N.J., Steer D.L. et al. Helicobacter pylori outer membrane vesicle size determines their mechanisms of host cell entry and protein content. Front Immunol 2018;9:1466. DOI: 10.3389/fimmu.2018.01466
50. Patten D.A., Hussein E., Davies S.P. et al. Commensal-derived OMVs elicit a mild proinflammatory response in intestinal epithelial cells. Microbiology (Reading) 2017;163(5):702–11. DOI: 10.1099/mic.0.000468
51. Wang X., Ni J., You Y. et al. SNX10-mediated LPS sensing causes intestinal barrier dysfunction via a caspase-5-dependent signaling cascade. EMBO J 2021;40(24):e108080. DOI: 10.15252/embj.2021108080
52. Francescone R., Hou V., Grivennikov S.I. Cytokines, IBD, and colitis-associated cancer. Inflamm Bowel Dis 2015;21(2):409–18. DOI: 10.1097/MIB.0000000000000236
53. Wong S.H., Yu J. Gut microbiota in colorectal cancer: mechanisms of action and clinical applications. Nat Rev Gastroenterol Hepatol 2019;16(11):690–704. DOI: 10.1038/s41575-019-0209-8
54. Bian X., Yang L., Wu W. et al. Pediococcus pentosaceus LI05 alleviates DSS-induced colitis by modulating immunological profiles, the gut microbiota and short-chain fatty acid levels in a mouse model. Microb Biotechnol 2020;13(4):1228–44. DOI: 10.1111/1751-7915.13583
55. Shi Y., Meng L., Zhang C. et al. Extracellular vesicles of Lacticaseibacillus paracasei PC-H1 induce colorectal cancer cells apoptosis via PDK1/AKT/Bcl-2 signaling pathway. Microbiol Res 2021;255:126921. DOI: 10.1016/j.micres.2021.126921
56. Fernández-Borbolla A., García-Hevia L., Fanarraga M.L. Cell membrane-coated nanoparticles for precision medicine: a comprehensive review of coating techniques for tissue-specific therapeutics. Int J Mol Sci 2024;25(4):2071. DOI: 10.3390/ijms25042071
57. Liang X., Dai N., Sheng K. et al. Gut bacterial extracellular vesicles: important players in regulating intestinal microenvironment. Gut Microbes 2022;14(1):2134689. DOI: 10.1080/19490976.2022.2134689
58. Wang D., Liu C., You S. et al. Bacterial vesicle-cancer cell hybrid membrane-coated nanoparticles for tumor specific immune activation and photothermal therapy. ACS Appl Mater Interfaces 2020;12(37):41138–47. DOI: 10.1021/acsami.0c13169
59. Meng Y., Chen S., Wang C., Ni X. Advances in composite biofilm biomimetic nanodrug delivery systems for cancer treatment. Technol Cancer Res Treat 2024;23:15330338241250244. DOI: 10.1177/15330338241250244
60. Chen Q., Huang G., Wu W. et al. A hybrid eukaryotic-prokaryotic nanoplatform with photothermal modality for enhanced antitumor vaccination. Adv Mater 2020;32(16):e1908185. DOI: 10.1002/adma.201908185
61. Rommasi F. Bacterial-based methods for cancer treatment: what we know and where we are. Oncol Ther 2022;10(1):23–54. DOI: 10.1007/s40487-021-00177-x
62. Behrouzi A., Nafari A.H., Siadat S.D. The significance of microbiome in personalized medicine. Clin Transl Med 2019;8(1):16. DOI: 10.1186/s40169-019-0232-y
63. Partula V., Mondot S., Torres M.J. et al. Associations between usual diet and gut microbiota composition: results from the Milieu Intérieur cross-sectional study. Am J Clin Nutr 2019;109(5):1472–83. DOI: 10.1093/ajcn/nqz029
64. Koponen K.K., Salosensaari A., Ruuskanen M.O. et al. Associations of healthy food choices with gut microbiota profiles. Am J Clin Nutr 2021;114(2):605–16. DOI: 10.1093/ajcn/nqab077
65. da Silva T.F., Casarotti S.N., de Oliveira G.L.V., Penna A.L.B. The impact of probiotics, prebiotics, and synbiotics on the biochemical, clinical, and immunological markers, as well as on the gut microbiota of obese hosts. Crit Rev Food Sci Nutr 2021;61(2):337–55. DOI: 10.1080/10408398.2020.1733483
66. Serban D.E. Gastrointestinal cancers: influence of gut microbiota, probiotics and prebiotics. Cancer Lett 2014;345(2):258–70. DOI: 10.1016/j.canlet.2013.08.013
67. Vivarelli S., Falzone L., Basile M.S. et al. Benefits of using probiotics as adjuvants in anticancer therapy (Review). World Acad Sci J 2019;1(3):125–35. DOI: 10.3892/wasj.2019.13
68. Chen S., Chen Y., Ma S. et al. Dietary fibre intake and risk of breast cancer: A systematic review and meta-analysis of epidemiological studies. Oncotarget 2016;7(49):80980–9. DOI: 10.18632/oncotarget.13140
69. Cong J., Zhou P., Zhang R. Intestinal microbiota-derived short chain fatty acids in host health and disease. Nutrients 2022;14(9):1977. DOI: 10.3390/nu14091977
70. Davani-Davari D., Negahdaripour M., Karimzadeh I. et al. Prebiotics: definition, types, sources, mechanisms, and clinical applications. Foods 2019;8(3):92. DOI: 10.3390/foods8030092
71. Hamada T., Nowak J.A., Milner D.A. Jr. et al. Integration of microbiology, molecular pathology, and epidemiology: a new paradigm to explore the pathogenesis of microbiome-driven neoplasms. J Pathol 2019;247(5):615–28. DOI: 10.1002/path.5236
72. Yano Y., Abnet C.C., Poustchi H. et al. Oral health and risk of upper gastrointestinal cancers in a large prospective study from a high-risk region: golestan cohort study. Cancer Prev Res (Phila) 2021;14(7):709–18. DOI: 10.1158/1940-6207.CAPR-20-0577
73. Newman K.L., Kamada N. Pathogenic associations between oral and gastrointestinal diseases. Trends Mol Med 2022;28(12): 1030–9. DOI: 10.1016/j.molmed.2022.05.006
74. Teratani T., Mikami Y., Nakamoto N. et al. The liver-brain-gut neural arc maintains the Treg cell niche in the gut. Nature 2020;585(7826):591–6. DOI: 10.1038/s41586-020-2425-3
75. Mikami Y., Tsunoda J., Kiyohara H. et al. Vagus nerve-mediated intestinal immune regulation: therapeutic implications of inflammatory bowel diseases. Int Immunol 2022;34(2):97–106. DOI: 10.1093/intimm/dxab039
Рецензия
Для цитирования:
Соленова Л.Г., Рыжова Н.И., Белицкий Г.А., Антонова И.А., Кирсанов К.И., Якубовская М.Г. Микробиота в диагностике, терапии и профилактике рака. Российский биотерапевтический журнал. 2024;23(4):10-21. https://doi.org/10.17650/1726-9784-2024-23-4-10-21
For citation:
Solenova L.G., Ryzhova N.I., Belitsky G.A., Antonova I.A., Kirsanov K.I., Yakubovskaya M.G. Microbiota in cancer diagnosis, therapy and prevention. Russian Journal of Biotherapy. 2024;23(4):10-21. (In Russ.) https://doi.org/10.17650/1726-9784-2024-23-4-10-21