POLYMORPHISM OF DNA REPAIR SYSTEM PROTEIN GENES AND ITS ASSOCIATION WITH CHRONIC VIRAL HEPATITIS C



Cite item

Full Text

Abstract

Abstract

Hepatitis C is an infectious disease that causes liver inflammation and often leads to a chronic process. The genes encoding proteins involved in DNA repair systems participate in developing immune responses and inflammation, making them promising candidates for studying genetic predisposition to a wide range of common diseases, including infections. However, this group of genes is rarely studied to assess their role in genetic susceptibility to infectious diseases.

In the present study, we investigated a role for polymorphisms in DNA repair system protein genes (ATM (rs189037 and rs1801516), NBN (rs709816 and rs1805800), MRE11 (rs473297), TP53BP1 (rs560191), MLH1 (rs1799977), PMS2 (rs1805321)) in the pathogenesis of chronic hepatitis C. As a result, associations were found both between some studied markers (rs1805321 in the PMS2 gene and rs1801516 in the ATM gene) and chronic hepatitis C as well as relations of various quantitative traits and the polymorphisms of these genes.

For example, variability in blood biochemical parameters (levels of cholesterol, glucose, iron, prothrombin index values, and thymol test results) was shown to depend on genotypes of two markers in the NBN gene (rs709816 and rs1805800). Clinical and morphological indicators are associated with variants in the NBN (rs1805800), MRE11 (rs473297), and PMS2 (rs1805321) genes. The absolute and relative levels of neutrophils are influenced by rs1805800 (NBN), rs473297 (MRE11), and rs1799977 (MLH1), whereas lymphocyte counts are affected by both markers in the NBN gene, rs473297 (MRE11), rs1799977 (MLH1), and rs1805321 (PMS2).

The lowest post-treatment IgG levels are observed in carriers of rarer genotypes in rs1805800 and rs709816 in NBN gene. Thus, our study demonstrates an impact of the studied genes on the pathogenesis of chronic hepatitis C, although the mechanism underlying such associations is not always clear. Nevertheless, our findings suggest about pleiotropic effects of DNA repair protein genes and their involvement in developing chronic hepatitis C.

About the authors

Nadezhda P. Babushkina

Research Institute of Medical Genetics, Tomsk National Research Medical Center

Email: nad.babushkina@medgenetics.ru
ORCID iD: 0000-0001-6133-8986
SPIN-code: 4639-1490
Scopus Author ID: 39961071300
ResearcherId: B-3106-2014

PhD in Biology, Senior Researcher, Population Genetics Laboratory, Research Institute of Medical Genetics, Tomsk National Research Medical Center

Россия

Valentina Evgenievna Shavrak

Research Institute of Medical Genetics, Tomsk National Research Medical Center

Email: laminatria21@gmail.com

Junior Researcher, Laboratory of Genomics of Orphan Diseases

Россия, Ushaiki River Embankment, 10; 634050, Tomsk, Russia

Шкштф Alexandrovna Goncharova

Research Institute of Medical Genetics, Tomsk National Research Medical Center

Email: irina.goncharova@medgenetics.ru
ORCID iD: 0000-0002-9527-7015
SPIN-code: 9399-9766
Scopus Author ID: 7003515492
ResearcherId: A-7918-2014

PhD in Biology, Researcher, Population Genetics Laboratory

Россия, Ushaiki River Embankment, 10; 634050, Tomsk, Russia

Ekaterina V. Beloborodova

Siberian State Medical University

Author for correspondence.
Email: beloborodova.ev@ssmu.ru
ORCID iD: 0000-0002-8776-5924
SPIN-code: 3905-2439
Scopus Author ID: 8914650400
ResearcherId: P-7915-2016

Professor, Department of Hospital Therapy with a course of rehabilitation, physiotherapy and sports medicine

Россия, 2 Moskovsky trakt, 634050, Tomsk

References

  1. Бабушкина Н.П., Гончарова И.А., Постригань А.Е., Кучер А.Н. Ген PMS2 ассоциирован с хроническим вирусным гепатитом С // Медицинская генетика. 2022. Т. 21, № 7, с. 19-23. Babushkina N.P., Goncharova I.A., Postrigan' A.E., Kucher A.N. The PMS2 gene is associated with HCVC // Medical Genetics. 2022. vol. 21, no. 7, pp. 19-23. doi: 10.25557/2073-7998.2022.07.19-23
  2. Белобородова Е.В., Гончарова И.А., Белобородова Э.И., Пурлик И.Л., Калачева Т.П., Акбашева О.Е., Рачковский М.И., Бурковская В.А. Иммуногенетика и прогрессирование хронических вирусных гепатитов // Экспериментальная и клиническая гастроэнтерология. 2015. Т. 3, № 115, С. 45-49. Beloborodova E.V., Goncharova I.A., Beloborodova Je.I., Purlik I.L., Kalacheva T.P., Akbasheva O.E., Rachkovskij M.I., Burkovskaja V.A. Immunogenetics and progression of chronic viral hepatitis // Experimental and clinical gastroenterology. 2015. vol. 3, no 115, pp. 45-49. URL: https://cyberleninka.ru/article/n/immunogenetika-i-progressirovanie-hronicheskih-virusnyh-gepatitov
  3. Белобородова Е.В., Гончарова И.А., Рязанцева Н.В., Белобородова Э.И., Пурлик И.Л., Калачева Т.П. Роль иммуногенетики в прогрессировании хронических вирусных гепатитов. Клинические перспективы гастроэнтерологии, гепатологии. 2014. № 2, С. 11-14. Beloborodova E.V., Goncharova I.A., Rjazanceva N.V., Beloborodova Je.I., Purlik I.L., Kalacheva T.P. Role of immunogenetics in progression of chronic viral hepatitis // Clinical Perspectives of Gastroenterology, Hepatology. 2014, no. 2, pp. 11-14. URL: https://www.elibrary.ru/item.asp?id=21252685
  4. Гепатит С // Всемирная организация здравоохранения – интернет-ресурс Hepatitis C // World Health Organization - Internet resource URL: https://www.who.int/ru/news-room/fact-sheets/detail/hepatitis-c
  5. Гончарова И.А., Белобородова Е.В., Фрейдин М.Б., Белобородова Э.И., Черногорюк Г.Э., Пузырев В.П. Генетические факторы подверженности к хронизации вирусного гепатита и фиброзу в печени. Молекулярная биология. 2008., Т. 42, № 2, С. 238-241. Goncharova I.A., Beloborodova E.V., Frejdin M.B., Beloborodova Je.I., Chernogorjuk G.Je., Puzyrev V.P. Genetic factors of susceptibility to chronic viral hepatitis and liver fibrosis // Molecular biology. 2008. vol. 42, no. 2, pp. 238-241. URL: https://www.elibrary.ru/item.asp?id=9934477
  6. Гончарова И.А., Назаренко М.С., Тарасенко Н.В., Марков А.В., Белобородова Е.В., Пузырев В.П. Генетические маркеры фиброгенеза при хроническом вирусном гепатите С // Медицинская генетика. 2016. Т. 15, № 12, С. 29-36. Goncharova I.A., Nazarenko M.S., Tarasenko N.V., Markov A.V., Beloborodova E.V., Puzyrev V.P. Genetic markers of fibrogenesis in determining susceptibility to chronic hepatitis C virus infection. Medical genetics. 2016, vol. 15, no. 12, pp. 29-36. URL: https://www.elibrary.ru/item.asp?id=27683654
  7. Гончарова И.А., Фрейдин М.Б., Дунаева Л.Е., Белобородова Е.В., Белобородова Э.И., Пузырев В.П. Анализ связи полиморфизма Ile50Val гена рецептора интерлейкина-4 (IL4RA) с хроническим вирусным гепатитом // Молекулярная биология. 2005. Т. 39. № 3, С. 379-384. Goncharova I.A., Frejdin M.B., Dunaeva L.E., Beloborodova E.V., Beloborodova Je.I., Puzyrev V.P. Association of the ile50Val polymorphism of the interleukin-4 receptor gene IL4RA with chronic viral hepatitis // Molecular Biology. 2005. vol. 39. No. 3, pp. 379-384. URL: https://www.elibrary.ru/item.asp?id=9148188
  8. Лифшиц В.М., Сидельникова В.И. Биохимические анализы в клинике. Медицинское информационное агентство, 2001, 2-е изд., 303 c. Lifshic V.M., Sidel'nikova V.I. Biohimicheskie analizy v klinike. Medicinskoe informacionnoe agentstvo, 2001, 2-e izd., 303 c. chrome-extension://efaidnbmnnnibpcajpcglclefindmkaj/https://e-library.sammu.uz/uploads/books/Rus%20tilidagi%20adabiyotlar/%D0%9A%D0%BB%D0%B8%D0%BD%D0%B8%D1%87%D0%B5%D1%81%D0%BA%D0%B0%D1%8F%20%D0%BB%D0%B0%D0%B1%D0%B0%D1%80%D0%B0%D1%82%D0%BE%D1%80%D0%BD%D0%B0%D1%8F%20%D0%B4%D0%B8%D0%B0%D0%B3%D0%BD%D0%BE%D1%81%D1%82%D0%B8%D0%BA%D0%B0/%D0%9B%D0%B8%D1%84%D1%89%D0%B8%D1%86_%D0%92_%D0%9C_%D0%91%D0%B8%D0%BE%D1%85%D0%B8%D0%BC%D0%B8%D1%87%D0%B5%D1%81%D0%BA%D0%B8%D0%B5_%D0%B0%D0%BD%D0%B0%D0%BB%D0%B8%D0%B7%D1%8B_%D0%B2_%D0%BA%D0%BB%D0%B8%D0%BD%D0%B8%D0%BA%D0%B5_2001.pdf
  9. Нурмагомаев М.С., Магомедова З.С., Каграманова З.С. Хронические гепатиты в клинике внутренних болезней. Научное обозрение // Медицинские науки. 2016. № 5, С. 77-91. Nurmagomaev M.S., Magomedova Z.S., Kagramanova Z.S. Chronic hepatitis in the clinic of internal diseases. Scientific review // Medical sciences. 2016. No. 5, pp. 77-91. URL: https://science-medicine.ru/ru/article/view?id=932
  10. Офицеров В.И. Подклассы иммуноглобулина G: возможности использования в диагностической практике. Методическое пособие ЗАО «Вектор-Бест», Кольцово 2005 г. Oficerov V.I. Podklassy immunoglobulina G: vozmozhnosti ispol'zovanija v diagnosticheskoj praktike. Metodicheskoe posobie ZAO «Vektor-Best», Kol'covo 2005 g. https://natmedlib.uz/fm/?sitemap/file/9p8vkXmg&view=%D0%90%D0%BB%D0%BB%D0%B5%D1%80%D0%B3%D0%BE%D0%BB%D0%BE%D0%B3%D0%B8%D1%8F%20%D0%B8%20%D0%B8%D0%BC%D0%BC%D1%83%D0%BD%D0%BE%D0%BB%D0%BE%D0%B3%D0%B8%D1%8F/%D0%9F%D0%BE%D0%B4%D0%BA%D0%BB%D0%B0%D1%81%D1%81%D1%8B%20%D0%B8%D0%BC%D0%BC%D1%83%D0%BD%D0%BE%D0%B3%D0%BB%D0%BE%D0%B1%D1%83%D0%BB%D0%B8%D0%BD%D0%B0%20G%20-%20%D0%B2%D0%BE%D0%B7%D0%BC%D0%BE%D0%B6%D0%BD%D0%BE%D1%81%D1%82%D0%B8%20%D0%B8%D1%81%D0%BF%D0%BE%D0%BB%D1%8C%D0%B7%D0%BE%D0%B2%D0%B0%D0%BD%D0%B8%D1%8F%20%D0%B2%20%D0%B4%D0%B8%D0%B0%D0%B3%D0%BD%D0%BE%D1%81%D1%82%D0%B8%D1%87%D0%B5%D1%81%D0%BA%D0%BE%D0%B9%20%D0%BF%D1%80%D0%B0%D0%BA%D1%82%D0%B8%D0%BA%D0%B5%20%D0%9E%D1%84%D0%B8%D1%86%D0%B5%D1%80%D0%BE%D0%B2%20%D0%92.%D0%98..pdf
  11. Стяжкина С.Н., Глушкова Т.Г., Кирьянов Н.А., Зайцев Д.В., Ленцова С.И., Горбунова М.А.. Морфофункциональная характеристика печени и поджелудочной железы при воздействии гепатопротектора Ремаксол на фоне острого алкогольного воздействия у крыс // Эффективная фармакотерапия. 2024. Т. 20, № 2, С. 26-29. Stjazhkina S.N., Glushkova T.G., Kir'janov N.A., Zajcev D.V., Lencova S.I., Gorbunova M.A. Morphofunctional Characteristic of the Hepar and Pancreas When Exposed to the Hepatoprotector Remaxol in Cases of Acute Alcohol Damage in Rats // Effective pharmacotherapy. 2024. vol. 20, no. 2, pp. 26-29. doi: 10.33978/2307-3586-2024-20-2-26-29
  12. Трошина Е.А., Сенюшкина Е.С. Вклад центральных регуляторов иммунного ответа в развитие заболеваний щитовидной железы // Проблемы Эндокринологии, 2019. Т. 65, № 6, С. 458-465. Troshina E.A., Senjushkina E.S. The value of central regulators of the immune response in the development of autoimmune thyroid diseases // Problems of Endocrinology. 2019. vol. 65. No. 6, pp. 458-465. URL: https://doi.org/10.14341/probl10304
  13. Яковенко Э.П., Григорьев П.Я. Хронические заболевания печени: диагностика и лечение // Р.М.Ж. 2003. Т. 5, С. 291. Yakovenko E.P., Grigoriev P.Ya. Chronic liver diseases: diagnosis and treatment // R.M.J. 2003. vol. 5, pp. 291. URL: https://www.rmj.ru/articles/gastroenterologiya/Hronicheskie_zabolevaniya_pecheni_diagnostika_i_lechenie/
  14. Almeida Pereira Leite S.T., Marques-Guimarães N., Silva-Oliveira J.C., Dutra-Souto F.J., Alves-dos-Santos R., Bassi-Branco C.L. The X-ray repair cross complementing protein 1 (XRCC1) rs25487 polymorphism and susceptibility to cirrhosis in Brazilian patients with chronic viral hepatitis. Ann. Hepatol., 2013, vol. 12, no. 5, pp. 733-739. - PMID: 24018491.
  15. Ariumi Y., Kuroki M., Dansako H., Abe K., Ikeda M., Wakita T., Kato N. The DNA damage sensors ataxia-telangiectasia mutated kinase and checkpoint kinase 2 are required for hepatitis C virus RNA replication. J. Virol., 2008, vol. 82, no. 19, pp. 9639-9646. - doi: 10.1128/JVI.00351-08.
  16. Basyte-Bacevice V., Skieceviciene J., Valantiene I., Sumskiene J., Petrenkiene V. Kondrackiene J., Petrauskas D., Lammert F., Kupcinskas J. SERPINA1 and HSD17B13 Gene Variants in Patients with Liver Fibrosis and Cirrhosis. J. Gastrointestin Liver Dis., 2019, vol. 28, no. 3, pp. 297-302. - doi: 10.15403/jgld-168.
  17. Bochud P.Y., Bibert S., Kutalik Z., Patin E., Guergnon J., Nalpas B., Goossens N., Kuske L., Müllhaupt B., Gerlach T., Heim M.H., Moradpour D., Cerny A., Malinverni R., Regenass S., Dollenmaier G., Hirsch H., Martinetti G., Gorgiewski M., Bourlière M., Poynard T., Theodorou I., Abel L., Pol S., Dufour J.F., Negro F. Swiss Hepatitis C Cohort Study Group; ANRS HC EP 26 Genoscan Study Group. IL28B alleles associated with poor hepatitis C virus (HCV) clearance protect against inflammation and fibrosis in patients infected with non-1 HCV genotypes. Hepatology, 2012, vol. 55, no. 2, pp. 384-394. - doi: 10.1002/hep.24678.
  18. Bredemeyer A.L., Sharma G.G., Huang C.Y., Helmink B.A., Walker L.M., Khor K.C., Nuskey B., Sullivan K.E., Pandita T.K., Bassing C.H., Sleckman B.P. ATM stabilizes DNA double-strand-break complexes during V(D)J recombination. Nature., 2006, vol. 442, pp. 466 - 470. - doi: 10.1038/nature04866.
  19. Chahwan R., Edelmann W., Scharff M.D., Roa S. Mismatch-mediated error prone repair at the immunoglobulin genes. Biomed Pharmacother., 2011, vol. 65, pp. 529-536. - doi: 10.1016/j.biopha.2011.09.001.
  20. Chahwan R., van Oers J.M., Avdievich E., Zhao C., Edelmann W., Scharff M.D., Roa S. The ATPase activity of MLH1 is required to orchestrate DNA double-strand breaks and end processing during class switch recombination. J. Exp. Med., 2012, vol. 209, pp. 671-678. - doi: 10.1084/jem.20111531.
  21. Chen H.T., Bhandoola A., Difilippantonio M.J., Zhu J., Brown M.J., Tai X., Rogakou E.P., Brotz T.M., Bonner W.M., Ried T., Nussenzweig A. Response to RAG-mediated VDJ cleavage by NBS1 and gamma-H2AX. Science., 2000, vol. 290, pp. 1962-1965. - doi: 10.1126/science.290.5498.1962.
  22. Cui A., Li B., Wallace M.S., Gonye A.L.K., Oetheimer C., Patel H., Tonnerre P., Holmes J.A., Lieb D., Yao B.S., Ma A., Roberts K., Damasio M., Chen J.H., Piou D., Carlton-Smith C., Brown J., Mylvaganam R., Hon Fung J.M., Sade-Feldman M., Aneja J., Gustafson J., Epstein E.T., Salloum S., Brisac C., Thabet A., Kim A.Y., Lauer G.M., Hacohen N., Chung R.T., Alatrakchi N. Single-cell atlas of the liver myeloid compartment before and after cure of chronic viral hepatitis. J. Hepatol., 2024, vol. 80, no. 2, pp. 251-267. - doi: 10.1016/j.jhep.2023.02.040.
  23. Desbois A.C., Cacoub P. Diabetes mellitus, insulin resistance and hepatitis C virus infection: A contemporary review. World J Gastroenterol., 2017, vol. 23m no. 9, pp. 1697-1711. - doi: 10.3748/wjg.v23.i9.1697.
  24. Dinkelmann M., Spehalski E., Stoneham T., Buis J., Wu Y., Sekiguchi J.M., Ferguson D.O. Multiple functions of MRN in end-joining pathways during isotype class switching. Nat. Struct. Mol. Biol., 2009, vol. 16, pp. 808-813. - doi: 10.1038/nsmb.1639.
  25. Douam F., Bobay L.M., Maurin G., Fresquet J., Calland N., Maisse C., Durand T., Cosset F.L., Féray C., Lavillette D. Specialization of Hepatitis C Virus Envelope Glycoproteins for B Lymphocytes in Chronically Infected Patients. J. Virol., 2015, vol. 90, no. 2, pp. 992-1008. - doi: 10.1128/JVI.02516-15.
  26. Du F., Zhang M., Li X., Yang C., Meng H., Wang D., Chang S., Xu Y., Price B., Sun Y. Dimer monomer transition and dimer re-formation play important role for ATM cellular function during DNA repair. Biochem. Biophys. Res. Commun., 2014, vol. 452, 4, pp. 1034-1039. - doi: 10.1016/j.bbrc.2014.09.038.
  27. Durand T., Di Liberto G., Colman H., Cammas A., Boni S., Marcellin P., Cahour A., Vagner S., Féray C. Occult infection of peripheral B cells by hepatitis C variants which have low translational efficiency in cultured hepatocytes. Gut., 2010, vol. 59, no. 7, pp. 934-942. - doi: 10.1136/gut.2009.192088.
  28. Elgretli W., Chen T., Kronfli N., Sebastiani G. Hepatitis C Virus-Lipid Interplay: Pathogenesis and Clinical Impact. Biomedicines., 2023, vol. 11, no. 2, p. 271. - doi: 10.3390/biomedicines11020271.
  29. Fabris C., Falleti E., Cussigh A., Bitetto D., Fontanini E., Colletta C., Vandelli C., Cmet S., Ceriani E., Smirne C., Toniutto P., Pirisi M. The interleukin 28B rs12979860 C/T polymorphism and serum cholesterol as predictors of fibrosis progression in patients with chronic hepatitis C and persistently normal transaminases. J. Med. Virol., 2012, vol. 84, no. 5, pp. 747-755. - doi: 10.1002/jmv.23259.
  30. Ferreira J., Bicho M., Serejo F. ABCA1 Polymorphism R1587K in Chronic Hepatitis C Is Gender-Specific and Modulates Liver Disease Severity through Its Influence on Cholesterol Metabolism and Liver Function: A Preliminary Study. Genes (Basel), 2022, vol. 13, no. 11, pp. 2095. - doi: 10.3390/genes13112095.
  31. Frey S., Bertocci B., Delbos F., Quint L., Weill J.C., Reynaud C.A. Mismatch repair deficiency interferes with the accumulation of mutations in chronically stimulated B cells and not with the hypermutation process. Immunity., 1998, vol. 9, no. 1, pp. 127-134. - doi: 10.1016/s1074-7613(00)80594-4.
  32. Ge D., Fellay J., Thompson A.J., Simon J.S., Shianna K.V., Urban T.J., Heinzen E.L., Qiu P., Bertelsen A.H., Muir A.J., Sulkowski M., McHutchison J.G., Goldstein D.B. Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature, 2009, vol. 461, no. 7262, pp. 399-401. - doi: 10.1038/nature08309.
  33. GTExPortal - The Genotype-Tissue Expression (GTEx) Portal (Internet resource) - URL: https://www.gtexportal.org/home/
  34. GWAS Catalog - The NHGRI-EBI Catalog of human genome-wide association studies (Internet resource)
  35. - URL: https://www.ebi.ac.uk/gwas/efotraits/EFO_0003047 GWAS Catalog
  36. Hardy L.C., Smeekens J.M., Raghuwanshi D., Sarkar S., Daskhan G.C., Rogers S., Nycholat C., Maleki S., Burks A.W., Paulson J.C., Macauley M.S., Kulis M.D. Targeting CD22 on memory B cells to induce tolerance to peanut allergens. J Allergy. Clin. Immunol., 2022, vol. 150, no. 6, pp. 1476-1485. - doi: 10.1016/j.jaci.2022.06.022.
  37. Helmink B.A., Bredemeyer A.L., Lee B.-S., Huang C.-Y., Sharma G.G., Walker L.M., Bednarski J.J., Lee W.-L., Pandita T.K., Bassing C.H., Sleckman B.P. MRN complex function in the repair of chromosomal Rag-mediated DNA double-strand breaks. J. Exp. Med. 2009, vol. 206, pp. 669-679. - doi: 10.1084/jem.20081326
  38. Hesselink L., Spijkerman R., van Wessem K.J.P., Koenderman L., Leenen L.P.H., Huber-Lang M., Hietbrink F. Neutrophil heterogeneity and its role in infectious complications after severe trauma. World J. Emerg. Surg., 2019, vol. 14, p. 24. - doi: 10.1186/s13017-019-0244-3.
  39. Hinrichsen I., Kemp M., Peveling-Oberhag J. Passmann S., Plotz G., Zeuzem S., Brieger A. Promoter methylation of MLH1, PMS2, MSH2 and p16 is a phenomenon of advanced-stage HCCs. PLoS One., 2014, vol. 9, no. 1, e84453. - doi: 10.1371/journal.pone.0084453.
  40. Lahdesmaki A., Taylor A.M., Chrzanowska K.H., Pan-Hammarstrom Q. Delineation of the role of the Mre11 complex in class switch recombination. J Biol. Chem., 2004, vol. 279, pp. 16479-16487. - doi: 10.1074/jbc.M312796200.
  41. Li F., Qu H., Li Y., Liu J., Fu H. Establishment and assessment of mortality risk prediction model in patients with sepsis based on early-stage peripheral lymphocyte subsets. Aging (Albany NY)., 2024, vol. 16, no. 8, pp. 7460-7473. - doi: 10.18632/aging.205772.
  42. Liu B., Wang K., Wu J., Hu Y., Yang X., Xu L., Sun W., Jia X., Wu J., Fu S., Qiao Y., Zhang X. Association of APEX1 and XRCC1 Gene Polymorphisms With HIV-1 Infection Susceptibility and AIDS Progression in a Northern Chinese MSM Population. Front. Genet., 2022, vol. 13, e861355. - doi: 10.3389/fgene.2022.861355.
  43. Liu C., Qiao Y., Xu L., Wu J., Mei Q., Zhang X., Wang K., Li Q., Jia X., Sun H., Wu J., Sun W., Fu S. Association between polymorphisms in MRE11 and HIV-1 susceptibility and AIDS progression in a northern Chinese MSM population. J. Antimicrob. Chemother., 2019, vol. 74, no. 7, pp. 2009-2018. - doi: 10.1093/jac/dkz132. PMID: 30989233.
  44. Liu Y., Dong J., Zhang Z., Liu Y., Wang Y. Regulatory T cells: A suppressor arm in post-stroke immune homeostasis. Neurobiol. Dis., 2023, vol. 189, e106350. - doi: 10.1016/j.nbd.2023.106350.
  45. Mirman Z., de Lange T. 53BP1: a DSB escort. Genes Dev., 2020, vol. 34, no. 1-2, pp. 7-23. - doi: 10.1101/gad.333237.119.
  46. Mizutani T., Kato N., Ikeda M., Sugiyama K., Shimotohno K. Long-term human T-cell culture system supporting hepatitis C virus replication. Biochem Biophys Res Commun., 1996, vol. 227, no. 3, pp. 822-826. - doi: 10.1006/bbrc.1996.1591.
  47. Ohta K., Ito M., Chida T., Nakashima K., Sakai S., Kanegae Y., Kawasaki H., Aoshima T., Takabayashi S., Takahashi H., Kawata K., Shoji I., Sawasaki T., Suda T., Suzuki T. Role of hepcidin upregulation and proteolytic cleavage of ferroportin 1 in hepatitis C virus-induced iron accumulation. PLoS Pathog., 2023, vol. 19, no. 8, e1011591. - doi: 10.1371/journal.ppat.1011591.
  48. Pan-Hammarström Q., Dai S., Zhao Y., van Dijk-Härd I.F., Gatti R.A., Børresen-Dale A.L., Hammarström L. ATM is not required in somatic hypermutation of VH, but is involved in the introduction of mutations in the switch mu region. J. Immunol., 2003, vol. 170, no. 7, pp. 3707-3716. - doi: 10.4049/jimmunol.170.7.3707.
  49. Peron S., Metin A., Gardes P., Alyanakian M.A., Sheridan E., Kratz C.P., Fischer A., Durandy A. Human PMS2 deficiency is associated with impaired immunoglobulin class switch recombination. J. Exp. Med., 2008, vol. 205, pp. 2465-2472. - doi: 10.1084/jem.20080789.
  50. Reina-San-Martin B., Chen J., Nussenzweig A., Nussenzweig M.C. Enhanced intra-switch region recombination during immunoglobulin class switch recombination in 53BP1−/− B cells. Eur. J. Immunol., 2007, vol. 37, pp. 235-239. - doi: 10.1002/eji.200636789
  51. Rybicka M., Woziwodzka A., Sznarkowska A., Romanowski T., Stalke P., Dręczewski M., Verrier E.R., Baumert T.F., Bielawski K.P. Liver Cirrhosis in Chronic Hepatitis B Patients Is Associated with Genetic Variations in DNA Repair Pathway Genes. Cancers (Basel)., 2020, vol. 12, no. 11, e3295. - doi: 10.3390/cancers12113295.
  52. Saidi A., Li T., Weih F., Concannon P., Wang Z.Q. Dual functions of Nbs1 in the repair of DNA breaks and proliferation ensure proper V(D)J recombination and T-cell development. Mol. Cell. Biol., 2010, vol. 30, pp. 5572-5581. - doi: 10.1128/MCB.00917-10.
  53. Sarhan M.A., Pham T.N., Chen A.Y., Michalak T.I. Hepatitis C virus infection of human T lymphocytes is mediated by CD5. J Virol., 2012, vol. 86, no. 7, pp. 3723-3735. - doi: 10.1128/JVI.06956-11.
  54. Schrader C.E., Edelmann W., Kucherlapati R., Stavnezer J. Reduced isotype switching in splenic B cells from mice deficient in mismatch repair enzymes. J. Exp. Med., 1999, vol. 190, pp. 323-330. - doi: 10.1084/jem.190.3.323.
  55. Sharkawy R.E., Bayoumi A., Metwally M., Mangia A., Berg T., Romero-Gomez M., Abate M.L., Irving W.L., Sheridan D., Dore G.J., Spengler U., Lampertico P., Bugianesi E., Weltman M., Mollison L., Cheng W., Riordan S., Santoro R., Gallego-Durán R., Fischer J., Nattermann J., D'Ambrosio R., McLeod D., Powell E., Latchoumanin O., Thabet K., Najim M.A.M., Douglas M.W., Liddle C., Qiao L., George J., Eslam M. International Liver Disease Genetics Consortium (ILDGC). A variant in the MICA gene is associated with liver fibrosis progression in chronic hepatitis C through TGF-β1 dependent mechanisms. Sc.i Rep., 2019, vol. 9, no. 1, pp. 1439. - doi: 10.1038/s41598-018-35736-2.
  56. Sun Y., Lu Y., Li T., Xie L., Deng Y., Li S., Qin X. Interferon Gamma +874T/A Polymorphism Increases the Risk of Hepatitis Virus-Related Diseases: Evidence from a Meta-Analysis. PLoS One., 2015, vol. 10, no. 5, e0121168. - doi: 10.1371/journal.pone.0121168.
  57. Świątek-Kościelna B., Kałużna E., Strauss E., Nowak J., Bereszyńska I., Gowin E., Wysocki J., Rembowska J., Barcińska D., Mozer-Lisewska I., Januszkiewicz-Lewandowska D. Prevalence of IFNL3 rs4803217 single nucleotide polymorphism and clinical course of chronic hepatitis C. World J. Gastroenterol, 2017, vol. 23, no. 21, pp. 3815-3824. - doi: 10.3748/wjg.v23.i21.3815.
  58. Thanapirom K., Suksawatamnuay S., Sukeepaisarnjaroen W., Tangkijvanich P., Treeprasertsuk S., Thaimai P., Wasitthankasem R., Poovorawan Y., Komolmit P. Association between CXCL10 and DPP4 Gene Polymorphisms and a Complementary Role for Unfavorable IL28B Genotype in Prediction of Treatment Response in Thai Patients with Chronic Hepatitis C Virus Infection. PLoS. One., 2015, vol. 10, no. 9, e0137365. - doi: 10.1371/journal.pone.0137365.
  59. Thanapirom K., Suksawatamnuay S., Sukeepaisarnjaroen W., Tangkijvanich P., Treeprasertsuk S., Thaimai P., Wasitthankasem R., Poovorawan Y., Komolmit P. Vitamin D-related gene polymorphism predict treatment response to pegylated interferon-based therapy in Thai chronic hepatitis C patients. BMC Gastroenterol, 2017, vol. 17, no. 1, p. 54. - doi: 10.1186/s12876-017-0613-x.
  60. Ton Tran H.T., Li C., Chakraberty R., Cairo C.W. NEU1 and NEU3 enzymes alter CD22 organization on B cells. Biophys. Rep. (N Y)., 2022, vol. 2, no. 3, e100064. - doi: 10.1016/j.bpr.2022.100064.
  61. Wang J., Sadeghi C.A., Le L.V., Le Bouteiller M., Frock R.L. ATM and 53BP1 regulate alternative end joining-mediated V(D)J recombination. Sci. Adv., 2024, vol. 10, no. 31, e4682. - doi: 10.1126/sciadv.adn4682.
  62. WEB-based GEne SeT AnaLysis Toolkit - URL: https://www.webgestalt.org/
  63. Yang Y., Tu Z.K., Liu X.K., Zhang P. Mononuclear phagocyte system in hepatitis C virus infection. World Gastroenterol., 2018, vol. 24, no. 44, pp. 4962-4973. - doi: 10.3748/wjg.v24.i44.4962.
  64. Yee L.J., Im K., Borg B., Yang H., Liang T.J. Virahep-C Study. Interleukin-6 haplotypes and the response to therapy of chronic hepatitis C virus infection. Genes Immun., 2009, vol. 10, no. 4, pp. 365-372. - doi: 10.1038/gene.2009.26.
  65. Yun M.H., Hiom K. Understanding the functions of BRCA1 in the DNA-damage response. Biochem. Soc. Trans., 2009, vol. 37, pp. 597 - 604. - doi: 10.1042/BST0370597.
  66. Zhao J., Dang X., Zhang P., Nguyen L.N., Cao D., Wang L., Wu X., Morrison Z.D., Zhang Y., Jia Z., Xie Q., Wang L., Ning S., El Gazzar M., Moorman J.P., Yao Z.Q. Insufficiency of DNA repair enzyme ATM promotes naive CD4 T-cell loss in chronic hepatitis C virus infection. Cell Discov., 2018, vol. 4, no. 16. - doi: 10.1038/s41421-018-0015-4.

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) Babushkina N.P., Shavrak V.E., Goncharova Ш.A., Beloborodova E.V.

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

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 64788 от 02.02.2016.


This website uses cookies

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

About Cookies