References

tumors

Malignant tumours

2224-50572587-6813

Rosoncoweb

10.18027/2224-5057-2023-13-3s1-64-71

tumors-1186

Research Article

Статьи

Роль микробиоты в канцерогенезе

Ковалева

О. В.

Ковалева

О. В.

Москва

ovkovaleva@gmail.com

Подлесная

П. А.

Подлесная

П. А.

Москва

Грачев

А. Н.

Грачев

А. Н.

Москва

ФГБУ «НМИЦ онкологии имени Н.Н. Блохина» Минздрава РоссииРоссияФГБУ «НМИЦ онкологии имени Н.Н. Блохина» Минздрава РоссииRussian Federation

2023

23112023

133s16471

2023

Ковалева О.В., Подлесная П.А., Грачев А.Н.

Данная работа распространяется под лицензией Creative Commons Attribution 4.0.

This work is licensed under a Creative Commons Attribution 4.0 License.

https://www.malignanttumors.org/jour/article/view/1186

Последнее десятилетие может по праву называться десятилетием микробиома. Развитие технологий позволило изучить микробиом различных органов и тканей организма человека и выявить взаимосвязь микробиома и широкого спектра заболеваний, в том числе онкологических. Так каким же образом микробиом может влиять на развитие и прогрессию опухолей? Бактерии могут взаимодействовать с клетками как непосредственно, так и с помощью секретируемых факторов. Также они могут вызывать локальное неспецифичное воспаление, что при переходе его в хроническую форму способно привести к злокачественной трансформации. Помимо влияния непосредственно на эпителиальные клетки, бактерии взаимодействуют с резидентными клетками иммунной системы, а именно макрофагами, и влияют на их свойства. Таксономическая идентификация микроорганизмов в опухоли позволяет находить новые прогностические маркеры, выбирать стратегию терапии или изучать взаимодействие данных микроорганизмов с организмом хозяином. На сегодняшний день показано, что качественный и количественный состав микробиома имеет клиническое и прогностическое значения для опухолей различных типов. Для внедрения этих результатов фундаментальных исследований необходима разработка комплексных диагностических подходов, включающих анализ особенностей опухолевых клеток, иммунофенотип стромальных клеток и состав опухолевого микробиома.

микробиомстромаопухольпрогноз

Исследование выполнено за счет гранта Российского научного фонда № 22-15-00291, https://rscf.ru/project/ 22-15-00291

References1

Yu G, Gail MH, Consonni D, Carugno M, Humphrys M, Pesatori AC, Caporaso NE, Goedert JJ, Ravel J, and Landi MT. Characterizing human lung tissue microbiota and its relationship to epidemiological and clinical features // Genome Biol. 2016. Vol. 17, N 1 : P. 163 doi: 10.1186/s13059-016-1021-1.

Dong Q, Chen ES, Zhao C, and Jin C. Host-Microbiome Interaction in Lung Cancer // Front Immunol. 2021. Vol. 12, N : P. 679829 doi: 10.3389/fimmu.2021.679829.

Beck JM, Young VB, and Huffnagle GB. The microbiome of the lung // Transl Res. 2012. Vol. 160, N 4 : P. 258–66 doi: 10.1016/j.trsl.2012.02.005.

Kovaleva OV, Romashin D, Zborovskaya IB, Davydov MM, Shogenov MS, and Gratchev A. Human Lung Microbiome on the Way to Cancer // J Immunol Res. 2019. Vol. 2019, N : P. 1394191 doi: 10.1155/2019/1394191.

Kovaleva O, Podlesnaya P, Rashidova M, Samoilova D, Petrenko A, Zborovskaya I, Mochalnikova V, Kataev V, Khlopko Y, Plotnikov A, and Gratchev A. Lung Microbiome Differentially Impacts Survival of Patients with Non-Small Cell Lung Cancer Depending on Tumor Stroma Phenotype // Biomedicines. 2020. Vol. 8, N 9 : P. doi: 10.3390/biomedicines8090349.

Fox JG, and Wang TC. Inflammation, atrophy, and gastric cancer // J Clin Invest. 2007. Vol. 117, N 1 : P. 60–9 doi: 10.1172/JCI30111.

Huang JQ, Zheng GF, Sumanac K, Irvine EJ, and Hunt RH. Meta-analysis of the relationship between cagA seropositivity and gastric cancer // Gastroenterology. 2003. Vol. 125, N 6 : P. 1636–44

Ye W, Held M, Lagergren J, Engstrand L, Blot WJ, McLaughlin JK, and Nyren O. Helicobacter pylori infection and gastric atrophy : risk of adenocarcinoma and squamous-cell carcinoma of the esophagus and adenocarcinoma of the gastric cardia // J Natl Cancer Inst. 2004. Vol. 96, N 5 : P. 388–96

Rubinstein MR, Wang X, Liu W, Hao Y, Cai G, and Han YW. Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin / beta-catenin signaling via its FadA adhesin // Cell Host Microbe. 2013. Vol. 14, N 2 : P. 195–206 doi: 10.1016/j.chom.2013.07.012.

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, and Fang JY. Fusobacterium nucleatum Promotes Chemoresistance to Colorectal Cancer by Modulating Autophagy // Cell. 2017. Vol. 170, N 3 : P. 548–63 e16 doi: 10.1016/j.cell.2017.07.008.

Gocyk W, Niklinski T, Olechnowicz H, Duda A, Bielanski W, Konturek PC, and Konturek SJ. Helicobacter pylori, gastrin and cyclooxygenase-2 in lung cancer // Med Sci Monit. 2000. Vol. 6, N 6 : P. 1085–92

Kanbay M, Kanbay A, and Boyacioglu S. Helicobacter pylori infection as a possible risk factor for respiratory system disease : a review of the literature // Respir Med. 2007. Vol. 101, N 2 : P. 203–9 doi: 10.1016/j.rmed.2006.04.022.

Cheng M, Qian L, Shen G, Bian G, Xu T, Xu W, Shen G, and Hu S. Microbiota modulate tumoral immune surveillance in lung through a gammadeltaT17 immune cell-dependent mechanism // Cancer Res. 2014. Vol. 74, N 15 : P. 4030–41 doi: 10.1158/0008-5472.CAN-13-2462.

Jungnickel C, Schmidt LH, Bittigkoffer L, Wolf L, Wolf A, Ritzmann F, Kamyschnikow A, Herr C, Menger MD, Spieker T, Wiewrodt R, Bals R, and Beisswenger C. IL-17C mediates the recruitment of tumor-associated neutrophils and lung tumor growth // Oncogene. 2017. Vol. 36, N 29 : P. 4182–90 doi: 10.1038/onc.2017.28.

Travaglione S, Fabbri A, and Fiorentini C. The Rho-activating CNF1 toxin from pathogenic E. coli : a risk factor for human cancer development? // Infect Agent Cancer. 2008. Vol. 3, N : P. 4 doi: 10.1186/1750-9378-3-4.

Nesic D, Hsu Y, and Stebbins CE. Assembly and function of a bacterial genotoxin // Nature. 2004. Vol. 429, N 6990 : P. 429–33 doi: 10.1038/nature02532.

Yaghoobi H, Bandehpour M, and Kazemi B. Apoptotic Effects of the B Subunit of Bacterial Cytolethal Distending Toxin on the A549 Lung Cancer Cell Line // Asian Pac J Cancer Prev. 2016. Vol. 17, N S3 : P. 299–304

Apopa PL, Alley L, Penney RB, Arnaoutakis K, Steliga MA, Jeffus S, Bircan E, Gopalan B, Jin J, Patumcharoenpol P, Jenjaroenpun P, Wongsurawat T, Shah N, Boysen G, Ussery D, Nookaew I, Fagan P, Bebek G, and Orloff MS. PARP1 Is Up-Regulated in Non-small Cell Lung Cancer Tissues in the Presence of the Cyanobacterial Toxin Microcystin // Front Microbiol. 2018. Vol. 9, N : P. 1757 doi: 10.3389/fmicb.2018.01757.

Chow SC, Gowing SD, Cools-Lartigue JJ, Chen CB, Berube J, Yoon HW, Chan CH, Rousseau MC, Bourdeau F, Giannias B, Roussel L, Qureshi ST, Rousseau S, and Ferri LE. Gram negative bacteria increase non-small cell lung cancer metastasis via Toll-like receptor 4 activation and mitogen-activated protein kinase phosphorylation // Int J Cancer. 2015. Vol. 136, N 6 : P. 1341–50 doi: 10.1002/ijc.29111.

Greathouse KL, White JR, Vargas AJ, Bliskovsky VV, Beck JA, von Muhlinen N, Polley EC, Bowman ED, Khan MA, Robles AI, Cooks T, Ryan BM, Padgett N, Dzutsev AH, Trinchieri G, Pineda MA, Bilke S, Meltzer PS, Hokenstad AN, Stickrod TM, Walther-Antonio MR, Earl JP, Mell JC, Krol JE, Balashov SV, Bhat AS, Ehrlich GD, Valm A, Deming C, Conlan S, Oh J, Segre JA, and Harris CC. Interaction between the microbiome and TP53 in human lung cancer // Genome Biol. 2018. Vol. 19, N 1 : P. 123 doi: 10.1186/s13059-018-1501-6.

Lee EY, Bang JY, Park GW, Choi DS, Kang JS, Kim HJ, Park KS, Lee JO, Kim YK, Kwon KH, Kim KP, and Gho YS. Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli // Proteomics. 2007. Vol. 7, N 17 : P. 3143–53 doi: 10.1002/pmic.200700196.

Kim JH, Lee J, Park J, and Gho YS. Gram-negative and Gram-positive bacterial extracellular vesicles // Semin Cell Dev Biol. 2015. Vol. 40, N:P. 97–104 doi: 10.1016/j.semcdb.2015.02.006.

Choi Y, Park H, Park HS, and Kim YK. Extracellular Vesicles, a Key Mediator to Link Environmental Microbiota to Airway Immunity // Allergy Asthma Immunol Res. 2017. Vol. 9, N 2 : P. 101–6 doi: 10.4168/aair.2017.9.2.101.

Brune B, Dehne N, Grossmann N, Jung M, Namgaladze D, Schmid T, von Knethen A, and Weigert A. Redox control of inflammation in macrophages // Antioxid Redox Signal. 2013. Vol. 19, N 6 : P. 595–637 doi: 10.1089/ars.2012.4785.

Hibbs JB, Jr., Taintor RR, and Vavrin Z. Macrophage cytotoxicity : role for L-arginine deiminase and imino nitrogen oxidation to nitrite // Science. 1987. Vol. 235, N 4787 : P. 473–6 doi: 10.1126/science.2432665.

Lambeth JD, Kawahara T, and Diebold B. Regulation of Nox and Duox enzymatic activity and expression // Free Radic Biol Med. 2007. Vol. 43, N 3 : P. 319–31 doi: 10.1016/j.freeradbiomed.2007.03.028.

Leto TL, Morand S, Hurt D, and Ueyama T. Targeting and regulation of reactive oxygen species generation by Nox family NADPH oxidases // Antioxid Redox Signal. 2009. Vol. 11, N 10 : P. 2607–19 doi: 10.1089/ARS.2009.2637.

Li B, Bedard K, Sorce S, Hinz B, Dubois-Dauphin M, and Krause KH. NOX4 expression in human microglia leads to constitutive generation of reactive oxygen species and to constitutive IL-6 expression // J Innate Immun. 2009. Vol. 1, N 6 : P. 570–81 doi: 10.1159/000235563.

Josephs DH, Nakamura M, Bax HJ, Dodev TS, Muirhead G, Saul L, Karagiannis P, Ilieva KM, Crescioli S, Gazinska P, Woodman N, Lombardelli C, Kareemaghay S, Selkirk C, Lentfer H, Barton C, Canevari S, Figini M, Downes N, Dombrowicz D, Corrigan CJ, Nestle FO, Jones PS, Gould HJ, Blower PJ, Tsoka S, Spicer JF, and Karagiannis SN. An immunologically relevant rodent model demonstrates safety of therapy using a tumour-specific IgE // Allergy. 2018. Vol. 73, N 12 : P. 2328–41 doi: 10.1111/all.13455.

Weiskopf K, and Weissman IL. Macrophages are critical effectors of antibody therapies for cancer // MAbs. 2015. Vol. 7, N 2 : P. 303–10 doi: 10.1080/19420862.2015.1011450.

Gao J, Wang D, Liu D, Liu M, Ge Y, Jiang M, Liu Y, and Zheng D. Tumor necrosis factor-related apoptosis-inducing ligand induces the expression of proinflammatory cytokines in macrophages and re-educates tumor-associated macrophages to an antitumor phenotype // Mol Biol Cell. 2015. Vol. 26, N 18 : P. 3178–89 doi: 10.1091/mbc.E15-04-0209.

Taganov KD, Boldin MP, Chang KJ, and Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses // Proc Natl Acad Sci U S A. 2006. Vol. 103, N 33 : P. 12481–6 doi: 10.1073/pnas.0605298103.

Wang D, Liu D, Gao J, Liu M, Liu S, Jiang M, Liu Y, and Zheng D. TRAIL-induced miR-146a expression suppresses CXCR4-mediated human breast cancer migration // FEBS J. 2013. Vol. 280, N 14 : P. 3340–53 doi: 10.1111/febs.12323.

Zhou Z, Zhang C, Zhang J, and Tian Z. Macrophages help NK cells to attack tumor cells by stimulatory NKG2D ligand but protect themselves from NK killing by inhibitory ligand Qa-1 // PLoS One. 2012. Vol. 7, N 5:P. e36928 doi: 10.1371/journal.pone.0036928.

Benimetskaya L, Loike JD, Khaled Z, Loike G, Silverstein SC, Cao L, el Khoury J, Cai TQ, and Stein CA. Mac-1 (CD11b / CD18) is an oligodeoxynucleotide-binding protein // Nat Med. 1997. Vol. 3, N 4 : P. 414–20 doi: 10.1038/nm0497-414.

Canli O, Nicolas AM, Gupta J, Finkelmeier F, Goncharova O, Pesic M, Neumann T, Horst D, Lower M, Sahin U, and Greten FR. Myeloid Cell-Derived Reactive Oxygen Species Induce Epithelial Mutagenesis // Cancer Cell. 2017. Vol. 32, N 6 : P. 869–83 e5 doi: 10.1016/j.ccell.2017.11.004.

Landsberg J, Kohlmeyer J, Renn M, Bald T, Rogava M, Cron M, Fatho M, Lennerz V, Wolfel T, Holzel M, and Tuting T. Melanomas resist T-cell therapy through inflammation-induced reversible dedifferentiation // Nature. 2012. Vol. 490, N 7420 : P. 412–6 doi: 10.1038/nature11538.

Zhou X, Hao Q, Liao P, Luo S, Zhang M, Hu G, Liu H, Zhang Y, Cao B, Baddoo M, Flemington EK, Zeng SX, and Lu H. Nerve growth factor receptor negates the tumor suppressor p53 as a feedback regulator // Elife. 2016. Vol. 5, N : P. doi: 10.7554/eLife.15099.

Ifrim DC, Quintin J, Joosten LA, Jacobs C, Jansen T, Jacobs L, Gow NA, Williams DL, van der Meer JW, and Netea MG. Trained immunity or tolerance : opposing functional programs induced in human monocytes after engagement of various pattern recognition receptors // Clin Vaccine Immunol. 2014. Vol. 21, N 4 : P. 534–45 doi: 10.1128/CVI.00688-13.

Dobrovolskaia MA, Medvedev AE, Thomas KE, Cuesta N, Toshchakov V, Ren T, Cody MJ, Michalek SM, Rice NR, and Vogel SN. Induction of in vitro reprogramming by Toll-like receptor (TLR) 2 and TLR4 agonists in murine macrophages : effects of TLR “homotolerance” versus “heterotolerance” on NF-kappa B signaling pathway components // J Immunol. 2003. Vol. 170, N 1 : P. 508–19 doi: 10.4049/jimmunol.170.1.508.

Dobrovolskaia MA, and Vogel SN. Toll receptors, CD14, and macrophage activation and deactivation by LPS // Microbes Infect. 2002. Vol. 4, N 9 : P. 903–14 doi: 10.1016/s1286-4579(02)01613-1.

Medvedev AE, Sabroe I, Hasday JD, and Vogel SN. Tolerance to microbial TLR ligands : molecular mechanisms and relevance to disease // J Endotoxin Res. 2006. Vol. 12, N 3 : P. 133–50 doi: 10.1179/096805106X102255.

Biswas SK, and Lopez-Collazo E. Endotoxin tolerance : new mechanisms, molecules and clinical significance // Trends Immunol. 2009. Vol. 30, N 10 : P. 475–87 doi: 10.1016/j.it.2009.07.009.

Sly LM, Rauh MJ, Kalesnikoff J, Song CH, and Krystal G. LPS-induced upregulation of SHIP is essential for endotoxin tolerance // Immunity. 2004. Vol. 21, N 2 : P. 227–39 doi: 10.1016/j.immuni.2004.07.010.

Piao W, Song C, Chen H, Diaz MA, Wahl LM, Fitzgerald KA, Li L, and Medvedev AE. Endotoxin tolerance dysregulates MyD88-and Toll / IL-1R domain-containing adapter inducing IFN-beta-dependent pathways and increases expression of negative regulators of TLR signaling // J Leukoc Biol. 2009. Vol. 86, N 4 : P. 863–75 doi: 10.1189/jlb.0309189.

Kobayashi K, Hernandez LD, Galan JE, Janeway CA, Jr., Medzhitov R, and Flavell RA. IRAK-M is a negative regulator of Toll-like receptor signaling // Cell. 2002. Vol. 110, N 2 : P. 191–202 doi: 10.1016/s0092-8674(02)00827-9.

Nimah M, Zhao B, Denenberg AG, Bueno O, Molkentin J, Wong HR, and Shanley TP. Contribution of MKP-1 regulation of p38 to endotoxin tolerance // Shock. 2005. Vol. 23, N 1 : P. 80–7 doi: 10.1097/01.shk.0000145206.28812.60.

Foster SL, Hargreaves DC, and Medzhitov R. Gene-specific control of inflammation by TLR-induced chromatin modifications // Nature. 2007. Vol. 447, N 7147 : P. 972–8 doi: 10.1038/nature05836.

Zwergal A, Quirling M, Saugel B, Huth KC, Sydlik C, Poli V, Neumeier D, Ziegler-Heitbrock HW, and Brand K. C / EBP beta blocks p65 phosphorylation and thereby NF-kappa B-mediated transcription in TNF-tolerant cells // J Immunol. 2006. Vol. 177, N 1 : P. 665–72 doi: 10.4049/jimmunol.177.1.665.

Park SH, Park-Min KH, Chen J, Hu X, and Ivashkiv LB. Tumor necrosis factor induces GSK3 kinase-mediated cross-toleranceto endotoxin in macrophages // Nat Immunol. 2011. Vol. 12, N 7 : P. 607–15 http://doi.org/10.1038/ni.2043.

Chen J, and Ivashkiv LB. IFN-gamma abrogates endotoxin tolerance by facilitating Toll-like receptor-induced chromatin remodeling // Proc Natl Acad Sci U S A. 2010. Vol. 107, N 45 : P. 19438–43 doi: 10.1073/pnas.1007816107.

Shi L, Song L, Maurer K, Sharp J, Zhang Z, and Sullivan KE. Endotoxin tolerance in monocytes can be mitigated by alpha2-interferon // J Leukoc Biol. 2015. Vol. 98, N 4 : P. 651–9 doi: 10.1189/jlb.4A0914-450RR.

Shoji S, Nakano M, Sato H, Tang XY, Osamura YR, Terachi T, Uchida T, and Takeya K. The current status of tailor-made medicine with molecular biomarkers for patients with clear cell renal cell carcinoma // Clin Exp Metastasis. 2014. Vol. 31, N 1 : P. 111–34 doi: 10.1007/s10585-013-9612-7.

Dizon DS, Krilov L, Cohen E, Gangadhar T, Ganz PA, Hensing TA, Hunger S, Krishnamurthi SS, Lassman AB, Markham MJ, Mayer E, Neuss M, Pal SK, Richardson LC, Schilsky R, Schwartz GK, Spriggs DR, Villalona-Calero MA, Villani G, and Masters G. Clinical Cancer Advances 2016 : Annual Report on Progress Against Cancer From the American Society of Clinical Oncology // J Clin Oncol. 2016. Vol. 34, N 9 : P. 987–1011 doi: 10.1200/JCO.2015.65.8427.

Barata PC, and Rini BI. Treatment of renal cell carcinoma : Current status and future directions // CA Cancer J Clin. 2017. Vol. 67, N 6 : P. 507–24 doi: 10.3322/caac.21411.

Liu KG, Gupta S, and Goel S. Immunotherapy : incorporation in the evolving paradigm of renal cancer management and future prospects // Oncotarget. 2017. Vol. 8, N 10 : P. 17313–27 doi: 10.18632/oncotarget.14388.

Le DT, Uram JN, Wang H, Bartlett BR, Kemberling H, Eyring AD, Skora AD, Luber BS, Azad NS, Laheru D, Biedrzycki B, Donehower RC, Zaheer A, Fisher GA, Crocenzi TS, Lee JJ, Duffy SM, Goldberg RM, de la Chapelle A, Koshiji M, Bhaijee F, Huebner T, Hruban RH, Wood LD, Cuka N, Pardoll DM, Papadopoulos N, Kinzler KW, Zhou S, Cornish TC, Taube JM, Anders RA, Eshleman JR, Vogelstein B, and Diaz LA, Jr. PD-1 Blockade in Tumors with Mismatch-Repair Deficiency // N Engl J Med. 2015. Vol. 372, N 26 : P. 2509–20 doi: 10.1056/NEJMoa1500596.

Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, Molina DA, Salcedo R, Back T, Cramer S, Dai RM, Kiu H, Cardone M, Naik S, Patri AK, Wang E, Marincola FM, Frank KM, Belkaid Y, Trinchieri G, and Goldszmid RS. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment // Science. 2013. Vol. 342, N 6161 : P. 967–70 doi: 10.1126/science.1240527.

Geller LT, Barzily-Rokni M, Danino T, Jonas OH, Shental N, Nejman D, Gavert N, Zwang Y, Cooper ZA, Shee K, Thaiss CA, Reuben A, Livny J, Avraham R, Frederick DT, Ligorio M, Chatman K, Johnston SE, Mosher CM, Brandis A, Fuks G, Gurbatri C, Gopalakrishnan V, Kim M, Hurd MW, Katz M, Fleming J, Maitra A, Smith DA, Skalak M, Bu J, Michaud M, Trauger SA, Barshack I, Golan T, Sandbank J, Flaherty KT, Mandinova A, Garrett WS, Thayer SP, Ferrone CR, Huttenhower C, Bhatia SN, Gevers D, Wargo JA, Golub TR, and Straussman R. Potential role of intratumor bacteria in mediating tumor resistance to the chemotherapeutic drug gemcitabine // Science. 2017. Vol. 357, N 6356 : P. 1156–60 doi: 10.1126/science.aah5043

The authors declare that there are no conflicts of interest present.