Bacterial DNA damage effectors in host cells

Cover Page

Cite item

Full Text

Abstract

The microbiota has a significant, and sometimes decisive, effect on the host's homeostasis. The results of recent metagenomic studies confirm the importance of microbiota in maintaining health or its impact on the development of acute, chronic and neoplastic diseases. One of the important aspects of microbiota exposure is the ability of many bacterial species to induce mutations or modulate a mutation process in the cells of the host organism. This review summarizes the main experimental data revealing various mechanisms of genotoxic action of a bacterial microbiota, including direct damage to the DNA structure, induction of oxidative stress, delay in replication, and a decrease in repair efficiency. It is emphasized that bacteria use different strategies to ensure their own survival and replication, including. by suppressing the repair of host cell DNA, by promoting the survival of infected cells, despite the presence of DNA damage therein.

About the authors

Vladimir G. Druzhinin

Kemerovo State University; Federal Research Center of Coal and Coal Chemistry of Siberian Branch of RAS

Author for correspondence.
Email: druzhinin_vladim@mail.ru
ORCID iD: 0000-0002-5534-2062
SPIN-code: 6277-4704

Sci. Doctor, Professor, Head, Department of Genetics

Russian Federation, 6, Krasnaya street, Kemerovo, 650000; 18, Sovetsky pr., Kemerovo, 650000

Elizaveta D. Baranova

Kemerovo State University

Email: laveivana@mail.ru
ORCID iD: 0000-0001-9503-8500

Bachelor Student, Department of Genetics

Russian Federation, 6, Krasnaya street, Kemerovo, 650000

Vladislav Yu. Buslaev

Kemerovo State University

Email: vladislasbus2358@yandex.ru

Master Student, Department of Genetics

Russian Federation, 6, Krasnaya street, Kemerovo, 650000

Lyudmila V. Matskova

Kemerovo State University; Karolinska Institute

Email: liudmila.matskova@ki.se
SPIN-code: 4756-7437

Scientific Researcher, Department of Bionanotechnology; Department of Microbiology and Tumor Biology

Russian Federation, 6, Krasnaya street, Kemerovo, 650000; Stockholm, Sweden

Alina V. Tolstikova

Kemerovo State University

Email: tolstikova.alina@inbox.ru

Postgraduate Student, Department of Genetics

Russian Federation, 6, Krasnay street, Kemerovo, 650000

References

  1. Абилев С.К., Глазер В.М. Мутагенез с основами генотоксикологии: учебное пособие. – М.; СПб.: Нестор-История, 2015. [Abilev SK, Glazer VM. Mutagenez s osnovami genotoksikologii: uchebnoye posobie. Moscow, Saint Petersburg: Nestor-Istoriya; 2015. (In Russ.)]
  2. Human Microbiome Project C. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207-214. doi: 10.1038/nature11234.
  3. Rybojad P, Los R, Sawicki M, et al. Anaerobic bacteria colonizing the lower airways in lung cancer patients. Folia Histochem Cytobiol. 2011;49(2):263-266. doi: 10.5603/fhc.2011.0036.
  4. Sheflin AM, Whitney AK, Weir TL. Cancer-promoting effects of microbial dysbiosis. Curr Oncol Rep. 2014;16(10):406. doi: 10.1007/s11912-014-0406-0.
  5. Urbaniak C, Gloor GB, Brackstone M, et al. The Microbiota of Breast Tissue and Its Association with Breast Cancer. Appl Environ Microbiol. 2016;82(16):5039-48. doi: 10.1128/AEM.01235-16.
  6. Perera M, Al-Hebshi NN, Speicher DJ, et al. Emerging role of bacteria in oral carcinogenesis: a review with special reference to perio-pathogenic bacteria. J Oral Microbiol. 2016;8:32762. doi: 10.3402/jom.v8.32762.
  7. Lucas C, Barnich N, Nguyen HTT. Microbiota, Inflammation and Colorectal Cancer. Int J Mol Sci. 2017;18(6). doi: 10.3390/ijms18061310.
  8. Mima K, Nakagawa S, Sawayama H, et al. The microbiome and hepatobiliary-pancreatic cancers. Cancer Lett. 2017;402:9-15. doi: 10.1016/j.canlet.2017.05.001.
  9. Gao R, Gao Z, Huang L, Qin H. Gut microbiota and colorectal cancer. Eur J Clin Microbiol Infect Dis. 2017;36(5):757-769. doi: 10.1007/s10096-016-2881-8.
  10. Mao Q, Jiang F, Yin R, et al. Interplay between the lung microbiome and lung cancer. Cancer Lett. 2018;415:40-48. doi: 10.1016/j.canlet.2017.11.036.
  11. Grasso F, Frisan T. Bacterial Genotoxins: Merging the DNA Damage Response into Infection Biology. Biomolecules. 2015;5(3):1762-1782. doi: 10.3390/biom5031762.
  12. Haghjoo E, Galan JE. Salmonella typhi encodes a functional cytolethal distending toxin that is delivered into host cells by a bacterial-internalization pathway. Proc Natl Acad Sci USA. 2004;101(13):4614-4619. doi: 10.1073/pnas.0400932101.
  13. Guerra L, Cortes-Bratti X, Guidi R, Frisan T. The bio logy of the cytolethal distending toxins. Toxins (Basel). 2011;3(3):172-190. doi: 10.3390/toxins3030172.
  14. Nougayrede JP, Homburg S, Taieb F, et al. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science. 2006;313(5788):848-851. doi: 10.1126/science.1127059.
  15. Johnson WM, Lior H. Response of Chinese hamster ovary cells to a cytolethal distending toxin (CDT) ofEscherichia coliand possible misinterpretation as heat-labile (LT) enterotoxin. FEMS Microbiol Lett. 1987;43(1):19-23. doi: 10.1111/j.1574-6968.1987.tb02091.x.
  16. Nesic D, Hsu Y, Stebbins CE. Assembly and function of a bacterial genotoxin. Nature. 2004;429(6990):429-33. doi: 10.1038/nature02532.
  17. Elwell CA, Dreyfus LA. DNase I homologous residues in CdtB are critical for cytolethal distending toxin-mediated cell cycle arrest. Mol Microbiol. 2000;37(4):952-963. doi: 10.1046/j.1365-2958.2000.02070.x.
  18. Frisan T, Cortes-Bratti X, Chaves-Olarte E, et al. The Haemophilus ducreyi cytolethal distending toxin induces DNA double-strand breaks and promotes ATM-dependent activation of RhoA. Cell Microbiol. 2003;5(10):695-707. doi: 10.1046/j.1462-5822.2003.00311.x.
  19. Asakura M, Hinenoya A, Alam MS, et al. An inducible lambdoid prophage encoding cytolethal distending toxin (Cdt-I) and a type III effector protein in enteropathogenic Escherichia coli. Proc Natl Acad Sci USA. 2007;104(36):14483-14488. doi: 10.1073/pnas.0706695104.
  20. Dlakic M. Is CdtB a nuclease or a phosphatase? Science. 2001;291(5504):547. doi: 10.1126/science.291.5504.547a.
  21. Frisan T. Bacterial genotoxins: The long journey to the nucleus of mammalian cells. Biochim Biophys Acta. 2016;1858(3):567-575. doi: 10.1016/j.bbamem.2015.08.016.
  22. Cortes-Bratti X, Karlsson C, Lagergard T, et al. The Haemophilus ducreyi cytolethal distending toxin induces cell cycle arrest and apoptosis via the DNA da mage checkpoint pathways. J Biol Chem. 2001;276(7):
  23. -5302. doi: 10.1074/jbc.M008527200.
  24. Fahrer J, Huelsenbeck J, Jaurich H, et al. Cytolethal distending toxin (CDT) is a radiomimetic agent and induces persistent levels of DNA double-strand breaks in human fibroblasts. DNA Repair (Amst). 2014;18:31-43. doi: 10.1016/j.dnarep.2014.03.002.
  25. Guidi R, Guerra L, Levi L, et al. Chronic exposure to the cytolethal distending toxins of Gram-negative bacteria promotes genomic instability and altered DNA damage response. Cell Microbiol. 2013;15(1):98-113. doi: 10.1111/cmi.12034.
  26. Fedor Y, Vignard J, Nicolau-Travers ML, et al. From single-strand breaks to double-strand breaks during S-phase: a new mode of action of the Escherichia coli Cytolethal Distending Toxin. Cell Microbiol. 2013;15(1):1-15. doi: 10.1111/cmi.12028.
  27. Fais T, Delmas J, Serres A, et al. Impact of CDT Toxin on Human Diseases. Toxins (Basel). 2016;8(7). doi: 10.3390/toxins8070220.
  28. Graillot V, Dormoy I, Dupuy J, et al. Genotoxicity of Cytolethal Distending Toxin (CDT) on Isogenic Human Colorectal Cell Lines: Potential Promoting Effects for Colorectal Carcinogenesis. Front Cell Infect Microbiol. 2016;6:34. doi: 10.3389/fcimb.2016.00034.
  29. Johnson JR, Johnston B, Kuskowski MA, et al. Molecular epidemiology and phylogenetic distribution of the Escherichia coli pks genomic island. J Clin Microbiol. 2008;46(12):3906-3911. doi: 10.1128/JCM.00949-08.
  30. Taieb F, Petit C, Nougayrede JP, Oswald E. The Enterobacterial Genotoxins: Cytolethal Distending Toxin and Colibactin. EcoSal Plus. 2016;7(1). doi: 10.1128/ecosalplus.ESP-0008-2016.
  31. Putze J, Hennequin C, Nougayrede JP, et al. Genetic structure and distribution of the colibactin genomic island among members of the family Enterobacteriaceae. Infect Immun. 2009;77(11):4696-4703. doi: 10.1128/IAI.00522-09.
  32. Lai YC, Lin AC, Chiang MK, et al. Genotoxic Klebsiella pneumoniae in Taiwan. PLoS One. 2014;9(5): e96292. doi: 10.1371/journal.pone.0096292.
  33. Lu MC, Chen YT, Chiang MK, et al. Colibactin Contributes to the Hypervirulence of pks(+) K1 CC23 Klebsiella pneumoniae in Mouse Meningitis Infections. Front Cell Infect Microbiol. 2017;7:103. doi: 10.3389/fcimb.2017.00103.
  34. Arthur JC, Perez-Chanona E, Muhlbauer M, et al. Intestinal inflammation targets cancer-inducing activity of the microbiota. Science. 2012;338(6103):120-123. doi: 10.1126/science.1224820.
  35. Vizcaino MI, Crawford JM. The colibactin warhead crosslinks DNA. Nat Chem. 2015;7(5):411-417. doi: 10.1038/nchem.2221.
  36. Healy AR, Herzon SB. Molecular Basis of Gut Microbiome-Associated Colorectal Cancer: A Synthetic Perspective. J Am Chem Soc. 2017;139(42):14817-14824. doi: 10.1021/jacs.7b07807.
  37. Cuevas-Ramos G, Petit CR, Marcq I, et al. Escheri chia coli induces DNA damage in vivo and triggers genomic instability in mammalian cells. Proc Natl Acad Sci USA. 2010;107(25):11537-11542. doi: 10.1073/pnas.1001261107.
  38. Cougnoux A, Dalmasso G, Martinez R, et al. Bacterial genotoxin colibactin promotes colon tumour growth by inducing a senescence-associated secretory phenotype. Gut. 2014;63(12):1932-1942. doi: 10.1136/gutjnl-2013-305257.
  39. Hayashi T. Microbiology. Breaking the barrier between commensalism and pathogenicity. Science. 2006;313(5788):772-773. doi: 10.1126/science.1131752.
  40. Nowrouzian FL, Oswald E. Escherichia coli strains with the capacity for long-term persistence in the bowel microbiota carry the potentially genotoxic pks island. Microb Pathog. 2012;53(3-4):180-182. doi: 10.1016/j.micpath.2012.05.011.
  41. Olier M, Marcq I, Salvador-Cartier C, et al. Genotoxicity of Escherichia coli Nissle 1917 strain cannot be dissociated from its probiotic activity. Gut Microbes. 2012;3(6):501-509. doi: 10.4161/gmic.21737.
  42. Peek RM, Jr., Blaser MJ. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer. 2002;2(1):28-37. doi: 10.1038/nrc703.
  43. Kim JM, Kim JS, Lee JY, et al. Vacuolating cytotoxin in Helicobacter pylori water-soluble proteins upregulates chemokine expression in human eosinophils via Ca2+ influx, mitochondrial reactive oxygen intermediates, and NF-kappaB activation. Infect Immun. 2007;75(7):3373-3381. doi: 10.1128/IAI.01940-06.
  44. Eftang LL, Esbensen Y, Tannaes TM, et al. Interleukin-8 is the single most up-regulated gene in whole genome profiling of H. pylori exposed gastric epithelial cells. BMC Microbiol. 2012;12:9. doi: 10.1186/1471-2180-12-9.
  45. Arabski M, Klupinska G, Chojnacki J, et al. DNA damage and repair in Helicobacter pylori-infected gastric mucosa cells. Mutat Res. 2005;570(1):129-135. doi: 10.1016/j.mrfmmm.2004.10.006.
  46. Arabski M, Kazmierczak P, Wisniewska-Jarosinska M, et al. Helicobacter pylori infection can modulate the susceptibility of gastric mucosa cells to MNNG. Cell Mol Biol Lett. 2006;11(4):570-578. doi: 10.2478/s11658-006-0045-z.
  47. Poplawski T, Chojnacki C, Czubatka A, et al. Helicobacter pylori infection and antioxidants can modulate the genotoxic effects of heterocyclic amines in gastric mucosa cells. Mol Biol Rep. 2013;40(8):5205-5212. doi: 10.1007/s11033-013-2622-3.
  48. Gologan A, Graham DY, Sepulveda AR. Molecular markers in Helicobacter pylori-associated gastric carcinogenesis. Clin Lab Med. 2005;25(1):197-222. doi: 10.1016/j.cll.2004.12.002.
  49. Китаева Л.В., Михайлова И.А., Семов Д.М., и др. Мукоциты с микроядрами и обсемененность кокковыми формами Helicobacter pylori в слизистой оболочке желудка человека // Цитология. 2008. - Т. 50. – № 2. – С. 160–163. [Kitayeva LV, Mikhaylova IA, Semov DM, et al. Mucocytes with micronuclei and sowing with the coccoid forms of Helicobacter pylori in a mucous membrane of human stomach. Cell and tissue biology. 2008;50(2):160-163. (In Russ.)]
  50. Китаева Л.В. Цитогенетические нарушения в слизистой оболочке фундального отдела желудка у пациентов с хроническим гастритом // Экологическая генетика. – 2010. – Т. 8. – № 1. – С. 36–41. [Kitayeva LV. Cytogenetic anomalies in gastric epithelial cells of fundic stomach region of the patients with chronic gastritis. Ecological genetics. 2010;8(1): 36-41. (In Russ.)]
  51. Machado AM, Figueiredo C, Touati E, et al. Helicobacter pylori infection induces genetic instability of nuclear and mitochondrial DNA in gastric cells. Clin Cancer Res. 2009;15(9):2995-3002. doi: 10.1158/1078-0432.CCR-08-2686.
  52. Toller IM, Neelsen KJ, Steger M, et al. Carcinogenic bacterial pathogen Helicobacter pylori triggers DNA double-strand breaks and a DNA damage response in its host cells. Proc Natl Acad Sci USA. 2011;108(36):14944-14949. doi: 10.1073/pnas.1100959108.
  53. Kalisperati P, Spanou E, Pateras IS, et al. Inflammation, DNA Damage, Helicobacter pylori and Gastric Tumorigenesis. Front Genet. 2017;8:20. doi: 10.3389/fgene.2017.00020.
  54. Kerr KG, Snelling AM. Pseudomonas aeruginosa: a formidable and ever-present adversary. J Hosp Infect. 2009;73(4):338-344. doi: 10.1016/j.jhin.2009.04.020.
  55. Wu M, Huang H, Zhang W, et al. Host DNA repair proteins in response to Pseudomonas aeruginosa in lung epithelial cells and in mice. Infect Immun. 2011;79(1):75-87. doi: 10.1128/IAI.00815-10.
  56. Elsen S, Collin-Faure V, Gidrol X, Lemercier C. The opportunistic pathogen Pseudomonas aeruginosa activates the DNA double-strand break signaling and repair pathway in infected cells. Cell Mol Life Sci. 2013;70(22):4385-4397. doi: 10.1007/s00018-013-1392-3.
  57. Hauser AR. The type III secretion system of Pseudomonas aeruginosa: infection by injection. Nat Rev Microbiol. 2009;7(9):654-665. doi: 10.1038/nrmicro2199.
  58. Al-Hebshi NN, Nasher AT, Maryoud MY, et al. Inflammatory bacteriome featuring Fusobacterium nucleatum and Pseudomonas aeruginosa identified in association with oral squamous cell carcinoma. Sci Rep. 2017;7(1):1834. doi: 10.1038/s41598-017-02079-3.
  59. Sears CL. Enterotoxigenic Bacteroides fragilis: a rogue among symbiotes. Clin Microbiol Rev. 2009;22(2):349-69, Table of Contents. doi: 10.1128/CMR.00053-08.
  60. Goodwin AC, Destefano Shields CE, Wu S, et al. Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc Natl Acad Sci USA. 2011;108(37):15354-15359. doi: 10.1073/pnas.1010203108.
  61. Huycke MM, Joyce W, Wack MF. Augmented Production of Extracellular Superoxide by Blood Isolates of Enterococcus faecalis. J Infect Dis. 1996;173(3):743-745. doi: 10.1093/infdis/173.3.743.
  62. Huycke MM, Moore D, Joyce W, et al. Extracellular superoxide production by Enterococcus faecalis requires demethylmenaquinone and is attenuated by functional terminal quinol oxidases. Mol Microbiol. 2008;42(3):729-740. doi: 10.1046/j.1365-2958.2001.02638.x.
  63. Goodwin AC, Destefano Shields CE, Wu S, et al. Polyamine catabolism contributes to enterotoxigenic Bacteroides fragilis-induced colon tumorigenesis. Proc Natl Acad Sci USA. 2011;108(37):15354-15359. doi: 10.1073/pnas.1010203108.
  64. Wang X, Huycke MM. Extracellular superoxide production by Enterococcus faecalis promotes chromosomal instability in mammalian cells. Gastroenterology. 2007;132(2):551-561. doi: 10.1053/j.gastro.2006.11.040.
  65. Strickertsson JA, Desler C, Martin-Bertelsen T, et al. Enterococcus faecalis infection causes inflammation, intracellular oxphos-independent ROS production, and DNA damage in human gastric cancer cells. PLoS One. 2013;8(4): e63147. doi: 10.1371/journal.pone.0063147.
  66. Wang X, Yang Y, Huycke MM. Microbiome-driven carcinogenesis in colorectal cancer: Models and mechanisms. Free Radic Biol Med. 2017;105:3-15. doi: 10.1016/j.freeradbiomed.2016.10.504.
  67. Wang X, Allen TD, May RJ, et al. Enterococcus faecalis induces aneuploidy and tetraploidy in colonic epithelial cells through a bystander effect. Cancer Res. 2008;68(23):9909-9917. doi: 10.1158/0008-5472.CAN-08-1551.
  68. Yang Y, Wang X, Huycke T, et al. Colon Macrophages Polarized by Commensal Bacteria Cause Colitis and Cancer through the Bystander Effect. Transl Oncol. 2013;6(5):596-IN598. doi: 10.1593/tlo.13412.
  69. Tattoli I, Carneiro LA, Jéhanno M, et al. NLRX1 is a mitochondrial NOD-like receptor that amplifies NF-κB and JNK pathways by inducing reactive oxygen species production. EMBO Rep. 2008;9(3):293-300. doi: 10.1038/sj.embor.7401161.
  70. Bergounioux J, Elisee R, Prunier AL, et al. Calpain activation by the Shigella flexneri effector VirA regulates key steps in the formation and life of the bacterium’s epithelial niche. Cell Host Microbe. 2012;11(3):240-252. doi: 10.1016/j.chom.2012.01.013.
  71. Rudel T. To die or not to die: Shigella has an answer. Cell Host Microbe. 2012;11(3):219-221. doi: 10.1016/j.chom.2012.02.004.
  72. Vielfort K, Soderholm N, Weyler L, et al. Neisseria gonorrhoeae infection causes DNA damage and affects the expression of p21, p27 and p53 in non-tumor epithelial cells. J Cell Sci. 2013;126(Pt 1):339-347. doi: 10.1242/jcs.117721.
  73. Leitao E, Costa AC, Brito C, et al. Listeria monocytogenes induces host DNA damage and delays the host cell cycle to promote infection. Cell Cycle. 2014;13(6):928-940. doi: 10.4161/cc.27780.
  74. Samba-Louaka A, Pereira JM, Nahori MA, et al. Listeria monocytogenes dampens the DNA damage response. PLoS Pathog. 2014;10(10): e1004470. doi: 10.1371/journal.ppat.1004470.
  75. Lam GY, Fattouh R, Muise AM, et al. Listeriolysin O suppresses phospholipase C-mediated activation of the microbicidal NADPH oxidase to promote Listeria monocytogenes infection. Cell Host Microbe. 2011;10(6):627-34. doi: 10.1016/j.chom.2011.11.005.
  76. Eskandarian HA, Impens F, Nahori MA, et al. A role for SIRT2-dependent histone H3K18 deacetylation in bacterial infection. Science. 2013;341(6145):1238858. doi: 10.1126/science.1238858.
  77. Bastidas RJ, Elwell CA, Engel JN, Valdivia RH. Chlamydial intracellular survival strategies. Cold Spring Harb Perspect Med. 2013;3(5): a010256. doi: 10.1101/cshperspect.a010256.
  78. Chumduri C, Gurumurthy RK, Zadora PK, et al. Chlamydia infection promotes host DNA damage and proliferation but impairs the DNA damage response. Cell Host Microbe. 2013;13(6):746-758. doi: 10.1016/j.chom.2013.05.010.
  79. Azenabor AA, Mahony JB. Generation of reactive oxygen species and formation of membrane lipid peroxides in cells infected with Chlamydia trachomatis. Int J Infect Dis. 2000;4(1):46-50. doi: 10.1016/s1201-9712(00)90066-3.
  80. Rai P, Parrish M, Tay IJ, et al. Streptococcus pneumoniae secretes hydrogen peroxide leading to DNA damage and apoptosis in lung cells. Proc Natl Acad Sci U S A. 2015;112(26): E3421-3430. doi: 10.1073/pnas.1424144112.
  81. Rai P, He F, Kwang J, et al. Pneumococcal Pneumolysin Induces DNA Damage and Cell Cycle Arrest. Sci Rep. 2016;6:22972. doi: 10.1038/srep22972.
  82. Loubinoux J, Bronowicki JP, Pereira IA, et al. Sulfate-reducing bacteria in human feces and their association with inflammatory bowel diseases. FEMS Microbiol Ecol. 2002;40(2):107-112. doi: 10.1111/j.1574-6941.2002.tb00942.x.
  83. Rey FE, Gonzalez MD, Cheng J, et al. Metabolic niche of a prominent sulfate-reducing human gut bacterium. Proc Natl Acad Sci USA. 2013;110(33):13582-13587. doi: 10.1073/pnas.1312524110.
  84. Attene-Ramos MS, Wagner ED, Plewa MJ, Gaskins HR. Evidence that hydrogen sulfide is a genotoxic agent. Mol Cancer Res. 2006;4(1):9-14. doi: 10.1158/1541-7786.MCR-05-0126.
  85. Attene-Ramos MS, Nava GM, Muellner MG, et al. DNA damage and toxicogenomic analyses of hydrogen sulfide in human intestinal epithelial FHs 74 Int cells. Environ Mol Mutagen. 2010;51(4):304-314. doi: 10.1002/em.20546.
  86. Ridlon JM, Wolf PG, Gaskins HR. Taurocholic acid metabolism by gut microbes and colon cancer. Gut Microbes. 2016;7(3):201-215. doi: 10.1080/19490976.2016.1150414.
  87. Castellarin M, Warren RL, Freeman JD, et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res. 2012;22(2):299-306. doi: 10.1101/gr.126516.111.
  88. Kostic AD, Chun E, Robertson L, et al. Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe. 2013;14(2):207-15. doi: 10.1016/j.chom.2013.07.007.
  89. Lemercier C. When our genome is targeted by pathogenic bacteria. Cell Mol Life Sci. 2015;72(14):2665-76. doi: 10.1007/s00018-015-1900-8.
  90. Chumduri C, Gurumurthy RK, Zietlow R, Meyer TF. Subversion of host genome integrity by bacterial pathogens. Nat Rev Mol Cell Biol. 2016;17(10):659-73. doi: 10.1038/nrm.2016.100.
  91. Druzhinin VG, Matskova LV, Fucic A. Induction and modulation of genotoxicity by the bacteriome in mammals. Mutat Res. 2018;776:70-77. doi: 10.1016/j.mrrev.2018.04.002.

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2018 Druzhinin V.G., Baranova E.D., Buslaev V.Y., Matskova L.V., Tolstikova A.V.

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


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies