vavilovВавиловский журнал генетики и селекцииVavilov Journal of Genetics and Breeding2500-3259Institute of Cytology and Genetics of Siberian Branch of the RAS10.18699/vjgb-24-48vavilov-4185Research ArticleБИОТЕХНОЛОГИЯ В ПОСТГЕНОМНУЮ ЭРУMEDICAL GENETICSАнализ ассоциаций полиморфных вариантов генов hOGG1, APEX1, XPD, SOD2 и CAT, участвующих в процессах репарации ДНК и антиоксидантной защите, с риском развития рака молочной железыPolymorphic variants of the hOGG1, APEX1, XPD, SOD2, and CAT genes involved in DNA repair processes and antioxidant defense and their association with breast cancer riskhttps://orcid.org/0000-0002-9063-0158ТимофееваА. А.TimofeevaА. А.

Кемерово

Kemerovo

annateam86@gmail.comhttps://orcid.org/0000-0003-3485-9123МининаВ. И.MininaV. I.

Кемерово

Kemerovo

https://orcid.org/0000-0001-5643-5001ТоргунаковаА. В.TorgunakovaA. V.

Кемерово

Kemerovo

https://orcid.org/0000-0001-7183-6647СоболеваО. А.SobolevaО. А.

Кемерово

Kemerovo

https://orcid.org/0000-0002-5485-9318ТитовР. А.ТitovR. А.

Кемерово

Kemerovo

https://orcid.org/0000-0003-0754-306XЗахароваЯ. А.ZakharovaYa. А.

Кемерово

Kemerovo

https://orcid.org/0000-0002-1238-2427БакановаМ. Л.BakanovaM. L.

Кемерово

Kemerovo

https://orcid.org/0000-0002-8560-6719ГлушковА. Н.GlushkovА. N.

Кемерово

Kemerovo

Федеральный исследовательский центр угля и углехимии Сибирского отделения Российской академии наукРоссияFederal Research Center of Coal and Coal Chemistry of the Siberian Branch of the Russian Academy of SciencesRussian FederationФедеральный исследовательский центр угля и углехимии Сибирского отделения Российской академии наук ; Кемеровский государственный университетРоссияFederal Research Center of Coal and Coal Chemistry of the Siberian Branch of the Russian Academy of Sciences ; Kemerovo State UniversityRussian Federation202411072024284424432Copyright © Тимофеева А.А., Минина В.И., Торгунакова А.В., Соболева О.А., Титов Р.А., Захарова Я.А., Баканова М.Л., Глушков А.Н., 20242024Тимофеева А.А., Минина В.И., Торгунакова А.В., Соболева О.А., Титов Р.А., Захарова Я.А., Баканова М.Л., Глушков А.Н.Timofeeva А.А., Minina V.I., Torgunakova A.V., Soboleva О.А., Тitov R.А., Zakharova Y.А., Bakanova M.L., Glushkov А.N.This work is licensed under a Creative Commons Attribution 4.0 License.https://vavilov.elpub.ru/jour/article/view/4185

Онкологические заболевания молочной железы – одна из ведущих причин смертности у женщин. Рак молочной железы относится к числу распространенных мультифакториальных полигенных заболеваний, реализующихся в результате сочетанного взаимодействия генетических и средовых факторов. Наиболее часто встречаются люминальные опухоли. Люминальный подтип В рака молочной железы характеризуется худшим прогнозом и ранними рецидивами. Для изучения генетических факторов риска развития злокачественных новообразований молочной железы необходимо определить полиморфные варианты генов, играющих важную роль в канцерогенезе, к числу которых относятся гены репарации ДНК и системы антиоксидантной защиты. Изучены ассоциации полиморфизмов генов hOGG1 (rs1052133), APEX1 (rs1130409), XPD (rs13181), SOD2 (rs4880) и CAT (rs1001179) у 313 некурящих пациенток в постменопаузе с диагнозом люминального подтипа В Her2-негативного рака молочной железы. В контрольную группу вошли 233 здоровые некурящие женщины в постменопаузе. Зарегистрированы с поправкой на возраст статистически значимые ассоциации полиморфных вариантов генов XPD (rs13181) и APEX1 (rs1130409) с риском развития люминального подтипа В Her2-негативного рака молочной железы в лог-аддитивной модели наследования, гена CAT (rs1001179) – в доминантной модели OR = 1.41; CI 95 %: 1.08–1.85; Padj = 0.011; OR = 1.39; CI 95 %: 1.07–1.81; Padj = 0.013 и OR = 1.70; CI 95 %: 1.19–2.43; Padj = 0.004 соответственно). В группе женщин пожилого возраста (60–74 года) выявлена ассоциация вариантов гена CAT (rs1001179) с риском развития рака молочной железы в лог-аддитивной модели наследования (OR = 1.87; CI 95 %: 1.22–2.85; Padj = 0.0024). С помощью MDR-анализа найдена наиболее оптимальная статистически значимая 3-локусная модель межгенных взаимодействий при развитии онкозаболеваний молочной железы люминального подтипа В. MDR-анализ показал также тесное взаимодействие и взаимное усиление эффектов между локусами APEX1 и SOD2 и независимость эффектов данных локусов от эффекта локуса САТ при формировании люминального подтипа В рака молочной железы.

Breast cancer is one of the leading causes of mortality among women. The most frequently encountered tumors are luminal tumors. Associations of polymorphisms in the hOGG1 (rs1052133), APEX1 (rs1130409), XPD (rs13181), SOD2 (rs4880), and CAT (rs1001179) genes were studied in 313 nonsmoking postmenopausal patients with luminal B subtype breast cancer. The control group consisted of 233 healthy nonsmoking postmenopausal women. Statistically significant associations of the XPD and APEX1 gene polymorphisms with the risk of developing luminal B Her2- negative subtype of breast cancer were observed in a log-additive inheritance model, while the CAT gene polymorphism showed an association in a dominant inheritance model (OR = 1.41; CI 95 %: 1.08–1.85; Padj.= 0.011; OR = 1.39; CI 95 %: 1.07–1.81; Padj = 0.013 и OR = 1.70; CI 95 %: 1.19–2.43; Padj = 0.004, respectively). In the group of elderly women (aged 60–74 years), an association of the CAT gene polymorphism with the risk of developing luminal B subtype of breast cancer was found in a log-additive inheritance model (OR = 1.87; 95 % CI: 1.22–2.85; Padj = 0.0024). Using MDR analysis, the most optimal statistically significant 3-locus model of gene-gene interactions in the development of luminal B Her2-negative subtype breast cancer was found. MDR analysis also showed a close interaction and mutual enhancement of effects between the APEX1 and SOD2 loci and the independence of the effects of these loci from the CAT locus in the formation of luminal B subtype breast cancer.

рак молочной железылюминальный подтип ВhOGG1APEX1XPDSOD2CAT.breast cancerluminal B subtypehOGG1APEX1XPDSOD2CAT.The work was carried out within the framework of the state assignment AAAA-A21-121011590009-9 “Immunohormonal Interactions in Breast Cancer” and with the use of grant funds for the establishment of a youth laboratory (Resolution of the Government of the Kemerovo Region No. 632 dated September 19, 2022).ReferencesAhn J., Gammon M.D., Santella R.M., Gaudet M.M., Britton J.A., Teitelbaum S.L., Terry M.B., Neugut A.I., Josephy P.D., Ambrosone C.B. Myeloperoxidase genotype, fruit and vegetable consumption, and breast cancer risk. Cancer Res. 2004;64(20):7634-7639. DOI 10.1158/0008-5472.CAN-04-1843Ahn J., Gammon M.D., Santella R.M., Gaudet M.M., Britton J.A., Teitelbaum S.L., Terry M.B., Neugut A.I., Josephy P.D., Ambrosone C.B. Myeloperoxidase genotype, fruit and vegetable consumption, and breast cancer risk. Cancer Res. 2004;64(20):7634-7639. DOI 10.1158/0008-5472.CAN-04-1843Ahn J., Gammon M.D., Santella R.M., Gaudet M.M., Britton J.A., Teitelbaum S.L., Terry M.B., Nowell S., Davis W., Garza C., Neugut A.I., Ambrosone C.B. Associations between breast cancer risk and the catalase genotype, fruit and vegetable consumption, and supplement use. Am. J. Epidemiol. 2005;162(10):943-952. DOI 10.1093/aje/kwi306Ahn J., Gammon M.D., Santella R.M., Gaudet M.M., Britton J.A., Teitelbaum S.L., Terry M.B., Nowell S., Davis W., Garza C., Neugut A.I., Ambrosone C.B. Associations between breast cancer risk and the catalase genotype, fruit and vegetable consumption, and supplement use. Am. J. Epidemiol. 2005;162(10):943-952. DOI 10.1093/aje/kwi306Alateyah N., Gupta I., Rusyniak R.S., Ouhtit A. SOD2, a potential transcriptional target underpinning CD44-promoted breast cancer progression. Molecules. 2022;27(3):811. DOI 10.3390/molecules27030811Alateyah N., Gupta I., Rusyniak R.S., Ouhtit A. SOD2, a potential transcriptional target underpinning CD44-promoted breast cancer progression. Molecules. 2022;27(3):811. DOI 10.3390/molecules27030811Ambrosone C.B. Oxidants and antioxidants in breast cancer. Antioxid. Redox Signal. 2000;2(4):903-917. DOI 10.1089/ars.2000.2.4-903Ambrosone C.B. Oxidants and antioxidants in breast cancer. Antioxid. Redox Signal. 2000;2(4):903-917. DOI 10.1089/ars.2000.2.4-903Bastaki M., Huen K., Manzanillo P., Chande N., Chen C., Balmes J.R., Tager I.B., Holland N. Genotype-activity relationship for Mn-superoxide dismutase, glutathione peroxidase 1 and catalase in humans. Pharmacogenet. Genomics. 2006;16(4):279-286. DOI 10.1097/01.fpc.0000199498.08725.9cBastaki M., Huen K., Manzanillo P., Chande N., Chen C., Balmes J.R., Tager I.B., Holland N. Genotype-activity relationship for Mn-superoxide dismutase, glutathione peroxidase 1 and catalase in humans. Pharmacogenet. Genomics. 2006;16(4):279-286. DOI 10.1097/01.fpc.0000199498.08725.9cBergman M., Ahnström M., Palmebäck Wegman P., Wingren S. Polymorphism in the manganese superoxide dismutase (MnSOD) gene and risk of breast cancer in young women. J. Cancer Res. Clin. Oncol. 2005;131(7):439-444. DOI 10.1007/s00432-004-0663-7Bergman M., Ahnström M., Palmebäck Wegman P., Wingren S. Polymorphism in the manganese superoxide dismutase (MnSOD) gene and risk of breast cancer in young women. J. Cancer Res. Clin. Oncol. 2005;131(7):439-444. DOI 10.1007/s00432-004-0663-7Breast Cancer Association Consortium. Breast cancer risk genes – association analysis in more than 113,000 women. N. Engl. J. Med. 2021;384(5):428-439. DOI 10.1056/NEJMoa1913948Breast Cancer Association Consortium. Breast cancer risk genes – association analysis in more than 113,000 women. N. Engl. J. Med. 2021;384(5):428-439. DOI 10.1056/NEJMoa1913948Calculation for the Chi-Square Test [Electronic resource]. URL: http://www.quantpsy.org/chisq/chisq.htm (accessed: 06.07.2023)Calculation for the Chi-Square Test [Electronic resource]. URL: http://www.quantpsy.org/chisq/chisq.htm (accessed: 06.07.2023)Caporaso N. The molecular epidemiology of oxidative damage to DNA and cancer. J. Natl. Cancer Inst. 2003;95(17):1263-1265. DOI 10.1093/jnci/djg065Caporaso N. The molecular epidemiology of oxidative damage to DNA and cancer. J. Natl. Cancer Inst. 2003;95(17):1263-1265. DOI 10.1093/jnci/djg065Dufloth R.M., Costa S., Schmitt F., Zeferino L.C. DNA repair gene polymorphisms and susceptibility to familial breast cancer in a group of patients from Campinas, Brazil. Genet. Mol. Res. 2005;4(4): 771-782Dufloth R.M., Costa S., Schmitt F., Zeferino L.C. DNA repair gene polymorphisms and susceptibility to familial breast cancer in a group of patients from Campinas, Brazil. Genet. Mol. Res. 2005;4(4): 771-782Ensembl [Electronic resource]. URL: http://www.ensembl.org/Homo_sapiens (accessed: 06.07.2023)Ensembl [Electronic resource]. URL: http://www.ensembl.org/Homo_sapiens (accessed: 06.07.2023)Ferreira M.A., Gamazon E.R., Al-Ejeh F., Aittomäki K., Andrulis I.L., Anton-Culver H., Arason A., Arndt V., Aronson K.J., Arun B.K., ... Yang X.R., Yannoukakos D., Ziogas A., Kraft P., Antoniou A.C., Zheng W., Easton D.F., Milne R.L., Beesley J., Chenevix-Trench G. Genome-wide association and transcriptome studies identify target genes and risk loci for breast cancer. Nat. Commun. 2019;10(1): 1741. DOI 10.1038/s41467-018-08053-5Ferreira M.A., Gamazon E.R., Al-Ejeh F., Aittomäki K., Andrulis I.L., Anton-Culver H., Arason A., Arndt V., Aronson K.J., Arun B.K., ... Yang X.R., Yannoukakos D., Ziogas A., Kraft P., Antoniou A.C., Zheng W., Easton D.F., Milne R.L., Beesley J., Chenevix-Trench G. Genome-wide association and transcriptome studies identify target genes and risk loci for breast cancer. Nat. Commun. 2019;10(1): 1741. DOI 10.1038/s41467-018-08053-5Fontana L., Bosviel R., Delort L., Guy L., Chalabi N., Kwiatkowski F., Satih S., Rabiau N., Boiteux J.P., Chamoux A., Bignon Y.J., BernardGallon D.J. DNA repair gene ERCC2, XPC, XRCC1, XRCC3 polymorphisms and associations with bladder cancer risk in a French cohort. Anticancer Res. 2008;28(3B):1853-1856Fontana L., Bosviel R., Delort L., Guy L., Chalabi N., Kwiatkowski F., Satih S., Rabiau N., Boiteux J.P., Chamoux A., Bignon Y.J., BernardGallon D.J. DNA repair gene ERCC2, XPC, XRCC1, XRCC3 polymorphisms and associations with bladder cancer risk in a French cohort. Anticancer Res. 2008;28(3B):1853-1856Forsberg L., Lyrenäs L., de Faire U., Morgenstern R. A common functional C-T substitution polymorphism in the promoter region of the human catalase gene influences transcription factor binding, reporter gene transcription and is correlated to blood catalase levels. Free Radic. Biol. Med. 2001;30(5):500-505. DOI 10.1016/s0891-5849(00)00487-1Forsberg L., Lyrenäs L., de Faire U., Morgenstern R. A common functional C-T substitution polymorphism in the promoter region of the human catalase gene influences transcription factor binding, reporter gene transcription and is correlated to blood catalase levels. Free Radic. Biol. Med. 2001;30(5):500-505. DOI 10.1016/s0891-5849(00)00487-1Gallegos-Arreola M.P., Ramírez-Patiño R., Sánchez-López J.Y., Zúñiga-González G.M., Figuera L.E., Delgado-Saucedo J.I., GómezMeda B.C., Rosales-Reynoso M.A., Puebla-Pérez A.M., Lemus-Varela M.L., Garibaldi-Ríos A.F., Marín-Domínguez N.A., Pacheco-Verduzco D.P., Mohamed-Flores E.A. SOD2 gene variants (rs4880 and rs5746136) and their association with breast cancer risk. Curr. Issues Mol. Biol. 2022;44(11):5221-5233. DOI 10.3390/cimb44110355Gallegos-Arreola M.P., Ramírez-Patiño R., Sánchez-López J.Y., Zúñiga-González G.M., Figuera L.E., Delgado-Saucedo J.I., GómezMeda B.C., Rosales-Reynoso M.A., Puebla-Pérez A.M., Lemus-Varela M.L., Garibaldi-Ríos A.F., Marín-Domínguez N.A., Pacheco-Verduzco D.P., Mohamed-Flores E.A. SOD2 gene variants (rs4880 and rs5746136) and their association with breast cancer risk. Curr. Issues Mol. Biol. 2022;44(11):5221-5233. DOI 10.3390/cimb44110355Goldhirsch A., Winer E.P., Coates A.S., Gelber R.D., Piccart-Gebhart M., Thürlimann B., Senn Y.-J. Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2013. Ann. Oncol. 2013;24(9):2206-2223. DOI 10.1093/annonc/mdt303Goldhirsch A., Winer E.P., Coates A.S., Gelber R.D., Piccart-Gebhart M., Thürlimann B., Senn Y.-J. Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2013. Ann. Oncol. 2013;24(9):2206-2223. DOI 10.1093/annonc/mdt303Hadi M.Z., Coleman M.A., Fidelis K., Mohrenweiser H.W., Wilson D.M. 3rd. Functional characterization of Ape1 variants identified in the human population. Nucleic Acids Res. 2000;28(20):3871- 3879. DOI 10.1093/nar/28.20.3871Hadi M.Z., Coleman M.A., Fidelis K., Mohrenweiser H.W., Wilson D.M. 3rd. Functional characterization of Ape1 variants identified in the human population. Nucleic Acids Res. 2000;28(20):3871- 3879. DOI 10.1093/nar/28.20.3871Hanawalt P.C. Subpathways of nucleotide excision repair and their regulation. Oncogene. 2002;21(58):8949-8956. DOI 10.1038/sj.onc.1206096Hanawalt P.C. Subpathways of nucleotide excision repair and their regulation. Oncogene. 2002;21(58):8949-8956. DOI 10.1038/sj.onc.1206096Hardy-Weinberg equilibrium [Electronic resource]. URL: https://genecalc.pl/hardy-weinberg-page (accessed: 06.07.2023)Hardy-Weinberg equilibrium [Electronic resource]. URL: https://genecalc.pl/hardy-weinberg-page (accessed: 06.07.2023)Ignatiadis M., Sotiriou C. Luminal breast cancer: from biology to treatment. Nat. Rev. Clin. Oncol. 2013;10(9):494-506. DOI 10.1038/nrclinonc.2013.124Ignatiadis M., Sotiriou C. Luminal breast cancer: from biology to treatment. Nat. Rev. Clin. Oncol. 2013;10(9):494-506. DOI 10.1038/nrclinonc.2013.124Jabir F.A., Hoidy W.H. Pharmacogenetics as personalized medicine: association investigation of SOD2 rs4880, CYP2C19 rs4244285, and FCGR2A rs1801274 polymorphisms in a breast cancer population in Iraqi women. Clin. Breast Cancer. 2018;18(5):e863-e868. DOI 10.1016/j.clbc.2018.01.009Jabir F.A., Hoidy W.H. Pharmacogenetics as personalized medicine: association investigation of SOD2 rs4880, CYP2C19 rs4244285, and FCGR2A rs1801274 polymorphisms in a breast cancer population in Iraqi women. Clin. Breast Cancer. 2018;18(5):e863-e868. DOI 10.1016/j.clbc.2018.01.009Jablonska E., Gromadzinska J., Peplonska B., Fendler W., Reszka E., Krol M.B., Wieczorek E., Bukowska A., Gresner P., Galicki M., Zambrano Quispe O., Morawiec Z., Wasowicz W. Lipid peroxidation and glutathione peroxidase activity relationship in breast cancer depends on functional polymorphism of GPX1. BMC Cancer. 2015;15:657. DOI 10.1186/s12885-015-1680-4Jablonska E., Gromadzinska J., Peplonska B., Fendler W., Reszka E., Krol M.B., Wieczorek E., Bukowska A., Gresner P., Galicki M., Zambrano Quispe O., Morawiec Z., Wasowicz W. Lipid peroxidation and glutathione peroxidase activity relationship in breast cancer depends on functional polymorphism of GPX1. BMC Cancer. 2015;15:657. DOI 10.1186/s12885-015-1680-4Ji M., Tang J., Zhao J., Xu B., Qin J., Lu J. Polymorphisms in genes involved in drug detoxification and clinical outcomes of anthracycline-based neoadjuvant chemotherapy in Chinese Han breast cancer patients. Cancer Biol. Ther. 2012;13(5):264-271. DOI 10.4161/cbt.18920Ji M., Tang J., Zhao J., Xu B., Qin J., Lu J. Polymorphisms in genes involved in drug detoxification and clinical outcomes of anthracycline-based neoadjuvant chemotherapy in Chinese Han breast cancer patients. Cancer Biol. Ther. 2012;13(5):264-271. DOI 10.4161/cbt.18920Kakkoura M.G., Demetriou C.A., Loizidou M.A., Loucaides G., Neophytou I., Malas S., Kyriacou K., Hadjisavvas A. MnSOD and CAT polymorphisms modulate the effect of the Mediterranean diet on breast cancer risk among Greek-Cypriot women. Eur. J. Nutr. 2016;55(4):1535-1544. DOI 10.1007/s00394-015-0971-5Kakkoura M.G., Demetriou C.A., Loizidou M.A., Loucaides G., Neophytou I., Malas S., Kyriacou K., Hadjisavvas A. MnSOD and CAT polymorphisms modulate the effect of the Mediterranean diet on breast cancer risk among Greek-Cypriot women. Eur. J. Nutr. 2016;55(4):1535-1544. DOI 10.1007/s00394-015-0971-5Kamali M., Kargar S., Heiranizadeh N., Zare M., Kargar Sh., Zare Shehneh M., Neamatzadeh H. Lack of any association between the Hogg1 Ser326Cys polymorphism and breast cancer risk: a systematic review and meta-analysis of 18 studies. Asian Pac. J. Cancer Prev. 2017;18(1):245-251. DOI 10.22034/APJCP.2017.18.1.245Kamali M., Kargar S., Heiranizadeh N., Zare M., Kargar Sh., Zare Shehneh M., Neamatzadeh H. Lack of any association between the Hogg1 Ser326Cys polymorphism and breast cancer risk: a systematic review and meta-analysis of 18 studies. Asian Pac. J. Cancer Prev. 2017;18(1):245-251. DOI 10.22034/APJCP.2017.18.1.245Kelley M.R., Georgiadis M.M., Fishel M.L. APE1/Ref-1 role in redox signaling: translational applications of targeting the redox function of the DNA repair/redox protein APE1/Ref-1. Curr. Mol. Pharmacol. 2012;5(1):36-53. DOI 10.2174/1874467211205010036Kelley M.R., Georgiadis M.M., Fishel M.L. APE1/Ref-1 role in redox signaling: translational applications of targeting the redox function of the DNA repair/redox protein APE1/Ref-1. Curr. Mol. Pharmacol. 2012;5(1):36-53. DOI 10.2174/1874467211205010036Kim K.Y., Han W., Noh D.Y., Kang D., Kwack K. Impact of genetic polymorphisms in base excision repair genes on the risk of breast cancer in a Korean population. Gene. 2013;532(2):192-196. DOI 10.1016/j.gene.2013.09.069Kim K.Y., Han W., Noh D.Y., Kang D., Kwack K. Impact of genetic polymorphisms in base excision repair genes on the risk of breast cancer in a Korean population. Gene. 2013;532(2):192-196. DOI 10.1016/j.gene.2013.09.069Li Y., Ambrosone C.B., McCullough M.J., Ahn J., Stevens V.L., Thun M.J., Hong C.C. Oxidative stress-related genotypes, fruit and vegetable consumption and breast cancer risk. Carcinogenesis. 2009;30(5):777-784. DOI 10.1093/carcin/bgp053Li Y., Ambrosone C.B., McCullough M.J., Ahn J., Stevens V.L., Thun M.J., Hong C.C. Oxidative stress-related genotypes, fruit and vegetable consumption and breast cancer risk. Carcinogenesis. 2009;30(5):777-784. DOI 10.1093/carcin/bgp053Liou G.Y., Storz P. Reactive oxygen species in cancer. Free Radic. Res. 2010;44(5):479-496. DOI 10.3109/10715761003667554Liou G.Y., Storz P. Reactive oxygen species in cancer. Free Radic. Res. 2010;44(5):479-496. DOI 10.3109/10715761003667554Martucci C.P., Fishman J. P450 enzymes of estrogen metabolism. Pharmacol. Ther. 1993;57(2-3):237-257. DOI 10.1016/0163-7258(93)90057-kMartucci C.P., Fishman J. P450 enzymes of estrogen metabolism. Pharmacol. Ther. 1993;57(2-3):237-257. DOI 10.1016/0163-7258(93)90057-kMcCullough L.E., Eng S.M., Bradshaw P.T., Cleveland R.J., Steck S.E., Terry M.B., Shen J., Crew K.D., Rossner P. Jr., Ahn J., Ambrosone C.B., Teitelbaum S.L., Neugut A.I., Santella R.M., Gammon M.D. Genetic polymorphisms in DNA repair and oxidative stress pathways may modify the association between body size and postmenopausal breast cancer. Ann. Epidemiol. 2015;25(4):263-269. DOI 10.1016/j.annepidem.2015.01.009McCullough L.E., Eng S.M., Bradshaw P.T., Cleveland R.J., Steck S.E., Terry M.B., Shen J., Crew K.D., Rossner P. Jr., Ahn J., Ambrosone C.B., Teitelbaum S.L., Neugut A.I., Santella R.M., Gammon M.D. Genetic polymorphisms in DNA repair and oxidative stress pathways may modify the association between body size and postmenopausal breast cancer. Ann. Epidemiol. 2015;25(4):263-269. DOI 10.1016/j.annepidem.2015.01.009Michailidou K., Lindström S., Dennis J., Beesley J., Hui S., Kar S., Lemaçon A., Soucy P., Glubb D., Rostamianfar A., … García-Closas M., Schmidt M.K., Chanock S.J., Dunning A.M., Edwards S.L., Bader G.D., Chenevix-Trench G., Simard J., Kraft P., Easton D.F. Association analysis identifies 65 new breast cancer risk loci. Nature. 2017;551(7678):92-94. DOI 10.1038/nature24284Michailidou K., Lindström S., Dennis J., Beesley J., Hui S., Kar S., Lemaçon A., Soucy P., Glubb D., Rostamianfar A., … García-Closas M., Schmidt M.K., Chanock S.J., Dunning A.M., Edwards S.L., Bader G.D., Chenevix-Trench G., Simard J., Kraft P., Easton D.F. Association analysis identifies 65 new breast cancer risk loci. Nature. 2017;551(7678):92-94. DOI 10.1038/nature24284Mitra A.K., Singh N., Singh A., Garg V.K., Agarwal A., Sharma M., Chaturvedi R., Rath S.K. Association of polymorphisms in base excision repair genes with the risk of breast cancer: a case-control study in North Indian women. Oncol. Res. 2008;17(3):127-135. DOI 10.3727/096504008785055567Mitra A.K., Singh N., Singh A., Garg V.K., Agarwal A., Sharma M., Chaturvedi R., Rath S.K. Association of polymorphisms in base excision repair genes with the risk of breast cancer: a case-control study in North Indian women. Oncol. Res. 2008;17(3):127-135. DOI 10.3727/096504008785055567Moore J.H., Gilbert J.C., Tsai C.T., Chiang F.T., Holden T., Barney N., White B.C. A flexible computational framework for detecting, characterizing, and interpreting statistical patterns of epistasis in genetic studies of human disease susceptibility. J. Theor. Biol. 2006; 241(2):252-261. DOI 10.1016/j.jtbi.2005.11.036Moore J.H., Gilbert J.C., Tsai C.T., Chiang F.T., Holden T., Barney N., White B.C. A flexible computational framework for detecting, characterizing, and interpreting statistical patterns of epistasis in genetic studies of human disease susceptibility. J. Theor. Biol. 2006; 241(2):252-261. DOI 10.1016/j.jtbi.2005.11.036Nishimura R., Osako T., Okumura Y., Hayashi M., Toyozumi Y., Arima N. Ki-67 as a prognostic marker according to breast cancer subtype and a predictor of recurrence time in primary breast cancer. Exp. Ther. Med. 2010;1(5):747-754. DOI 10.3892/etm.2010.133Nishimura R., Osako T., Okumura Y., Hayashi M., Toyozumi Y., Arima N. Ki-67 as a prognostic marker according to breast cancer subtype and a predictor of recurrence time in primary breast cancer. Exp. Ther. Med. 2010;1(5):747-754. DOI 10.3892/etm.2010.133Niu Y., Li F., Tang B., Shi Y., Yu P. Association of hOGG1 Ser326Cys polymorphism with gastric cancer risk: a meta-analysis. Mol. Biol. Rep. 2012;39(6):6563-6568. DOI 10.1007/s11033-012-1485-3Niu Y., Li F., Tang B., Shi Y., Yu P. Association of hOGG1 Ser326Cys polymorphism with gastric cancer risk: a meta-analysis. Mol. Biol. Rep. 2012;39(6):6563-6568. DOI 10.1007/s11033-012-1485-3Nyaga S.G., Lohani A., Jaruga P., Trzeciak A.R., Dizdaroglu M., Evans M.K. Reduced repair of 8-hydroxyguanine in the human breast cancer cell line, HCC1937. BMC Cancer. 2006;6:297. DOI 10.1186/1471-2407-6-297Nyaga S.G., Lohani A., Jaruga P., Trzeciak A.R., Dizdaroglu M., Evans M.K. Reduced repair of 8-hydroxyguanine in the human breast cancer cell line, HCC1937. BMC Cancer. 2006;6:297. DOI 10.1186/1471-2407-6-297Onay V.U., Briollais L., Knight J.A., Shi E., Wang Y., Wells S., Li H., Rajendram I., Andrulis I.L., Ozcelik H. SNP-SNP interactions in breast cancer susceptibility. BMC Cancer. 2006;6:114. DOI 10.1186/1471-2407-6-114Onay V.U., Briollais L., Knight J.A., Shi E., Wang Y., Wells S., Li H., Rajendram I., Andrulis I.L., Ozcelik H. SNP-SNP interactions in breast cancer susceptibility. BMC Cancer. 2006;6:114. DOI 10.1186/1471-2407-6-114Pan Q., Liu Y.J., Bai X.F., Han X.L., Jiang Y., Ai B., Shi S.S., Wang F., Xu M.C., Wang Y.Z., Zhao J., Chen J.X., Zhang J., Li X.C., Zhu J., Zhang G.R., Wang Q.Y., Li C.Q. VARAdb: a comprehensive variation annotation database for human. Nucleic Acids Res. 2021; 49(D1):D1431-D1444. DOI 10.1093/nar/gkaa922Pan Q., Liu Y.J., Bai X.F., Han X.L., Jiang Y., Ai B., Shi S.S., Wang F., Xu M.C., Wang Y.Z., Zhao J., Chen J.X., Zhang J., Li X.C., Zhu J., Zhang G.R., Wang Q.Y., Li C.Q. VARAdb: a comprehensive variation annotation database for human. Nucleic Acids Res. 2021; 49(D1):D1431-D1444. DOI 10.1093/nar/gkaa922Rodrigues P., Furriol J., Bermejo B., Chaves F.J., Lluch A., Eroles P. Identification of candidate polymorphisms on stress oxidative and DNA damage repair genes related with clinical outcome in breast cancer patients. Int. J. Mol. Sci. 2012;13(12):16500-16513. DOI 10.3390/ijms131216500Rodrigues P., Furriol J., Bermejo B., Chaves F.J., Lluch A., Eroles P. Identification of candidate polymorphisms on stress oxidative and DNA damage repair genes related with clinical outcome in breast cancer patients. Int. J. Mol. Sci. 2012;13(12):16500-16513. DOI 10.3390/ijms131216500Romanowicz H., Pyziak Ł., Jabłoński F., Bryś M., Forma E., Smolarz B. Analysis of DNA repair genes polymorphisms in breast cancer. Pathol. Oncol. Res. 2017;23(1):117-123. DOI 10.1007/s12253-016-0110-5Romanowicz H., Pyziak Ł., Jabłoński F., Bryś M., Forma E., Smolarz B. Analysis of DNA repair genes polymorphisms in breast cancer. Pathol. Oncol. Res. 2017;23(1):117-123. DOI 10.1007/s12253-016-0110-5Romaniuk O.P., Nikitchenko N.V., Savina N.V., Kuzhir T.D., Goncharova R.I. The polymorphism of DNA repair genes XPD, XRCC1, OGG1, and ERCC6, life expectancy, and the inclination to smoke. Russ. J. Genet. 2014;50(8):860-869. DOI 10.1134/S1022795414080067Romaniuk O.P., Nikitchenko N.V., Savina N.V., Kuzhir T.D., Goncharova R.I. The polymorphism of DNA repair genes XPD, XRCC1, OGG1, and ERCC6, life expectancy, and the inclination to smoke. Russ. J. Genet. 2014;50(8):860-869. DOI 10.1134/S1022795414080067Sambrook J., Fritsch E.R., Maniatis T. Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press, 1989Sambrook J., Fritsch E.R., Maniatis T. Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press, 1989Samson M., Singh S.S., Rama R., Sridevi V., Rajkumar T. XPD Lys751Gln increases the risk of breast cancer. Oncol. Lett. 2011; 2(1):155-159. DOI 10.3892/ol.2010.220Samson M., Singh S.S., Rama R., Sridevi V., Rajkumar T. XPD Lys751Gln increases the risk of breast cancer. Oncol. Lett. 2011; 2(1):155-159. DOI 10.3892/ol.2010.220Siegel R.L., Miller K.D., Fuchs H.E., Jemal A. Cancer statistics, 2021. CA Cancer J. Clin. 2021;71(1):7-33. DOI 10.3322/caac.21654Siegel R.L., Miller K.D., Fuchs H.E., Jemal A. Cancer statistics, 2021. CA Cancer J. Clin. 2021;71(1):7-33. DOI 10.3322/caac.21654Silva S.N., Cabral M.N., Bezerra de Castro G., Pires M., Azevedo A.P., Manita I., Pina J.E., Rueff J., Gaspar J. Breast cancer risk and polymorphisms in genes involved in metabolism of estrogens (CYP17, HSD17beta1, COMT and MnSOD): possible protective role of MnSOD gene polymorphism Val/Ala and Ala/Ala in women that never breast fed. Oncol. Rep. 2006;16(4):781-788Silva S.N., Cabral M.N., Bezerra de Castro G., Pires M., Azevedo A.P., Manita I., Pina J.E., Rueff J., Gaspar J. Breast cancer risk and polymorphisms in genes involved in metabolism of estrogens (CYP17, HSD17beta1, COMT and MnSOD): possible protective role of MnSOD gene polymorphism Val/Ala and Ala/Ala in women that never breast fed. Oncol. Rep. 2006;16(4):781-788Smith T.R., Levine E.A., Freimanis R.I., Akman S.A., Allen G.O., Hoang K.N., Liu-Mares W., Hu J.J. Polygenic model of DNA repair genetic polymorphisms in human breast cancer risk. Carcinogenesis. 2008;29(11):2132-2138. DOI 10.1093/carcin/bgn193Smith T.R., Levine E.A., Freimanis R.I., Akman S.A., Allen G.O., Hoang K.N., Liu-Mares W., Hu J.J. Polygenic model of DNA repair genetic polymorphisms in human breast cancer risk. Carcinogenesis. 2008;29(11):2132-2138. DOI 10.1093/carcin/bgn193Smolarz B., Michalska M.M., Samulak D., Romanowicz H., Wójcik L. Polymorphism of DNA repair genes in breast cancer. Oncotarget. 2019;10(4):527-535. DOI 10.18632/oncotarget.26568Smolarz B., Michalska M.M., Samulak D., Romanowicz H., Wójcik L. Polymorphism of DNA repair genes in breast cancer. Oncotarget. 2019;10(4):527-535. DOI 10.18632/oncotarget.26568SNPStats [Electronic resource]. URL: http://bioinfo.iconcologia.net/SNPstats (accessed: 06.07.2023)SNPStats [Electronic resource]. URL: http://bioinfo.iconcologia.net/SNPstats (accessed: 06.07.2023)Sugasawa K. Regulation of damage recognition in mammalian global genomic nucleotide excision repair. Mutat. Res. 2010;685(1-2): 29-37. DOI 10.1016/j.mrfmmm.2009.08.004Sugasawa K. Regulation of damage recognition in mammalian global genomic nucleotide excision repair. Mutat. Res. 2010;685(1-2): 29-37. DOI 10.1016/j.mrfmmm.2009.08.004Sutton A., Imbert A., Igoudjil A., Descatoire V., Cazanave S., Pessayre D., Degoul F. The manganese superoxide dismutase Ala16Val dimorphism modulates both mitochondrial import and mRNA stability. Pharmacogenet. Genomics. 2005;15(5):311-319. DOI 10.1097/01213011-200505000-00006Sutton A., Imbert A., Igoudjil A., Descatoire V., Cazanave S., Pessayre D., Degoul F. The manganese superoxide dismutase Ala16Val dimorphism modulates both mitochondrial import and mRNA stability. Pharmacogenet. Genomics. 2005;15(5):311-319. DOI 10.1097/01213011-200505000-00006Tas F., Hansel H., Belce A., Ilvan S., Argon A., Camlica H., Topuz E. Oxidative stress in breast cancer. Med. Oncol. 2005;22(1):11-15. DOI 10.1385/MO:22:1:011Tas F., Hansel H., Belce A., Ilvan S., Argon A., Camlica H., Topuz E. Oxidative stress in breast cancer. Med. Oncol. 2005;22(1):11-15. DOI 10.1385/MO:22:1:011Tjønneland A., Christensen J., Thomsen B.L., Olsen A., Overvad K., Ewertz M., Mellemkjaer L. Hormone replacement therapy in relation to breast carcinoma incidence rate ratios: a prospective Danish cohort study. Cancer. 2004; 100(11):2328-2337. DOI 10.1002/cncr.20250Tjønneland A., Christensen J., Thomsen B.L., Olsen A., Overvad K., Ewertz M., Mellemkjaer L. Hormone replacement therapy in relation to breast carcinoma incidence rate ratios: a prospective Danish cohort study. Cancer. 2004; 100(11):2328-2337. DOI 10.1002/cncr.20250Tsai S.M., Wu S.H., Hou M.F., Chen Y.L., Ma H., Tsai L.Y. Oxidative stress-related enzyme gene polymorphisms and susceptibility to breast cancer in non-smoking, non-alcohol-consuming Taiwanese women: a case-control study. Ann. Clin. Biochem. 2012;49(Pt. 2): 152-158. DOI 10.1258/acb.2011.011098Tsai S.M., Wu S.H., Hou M.F., Chen Y.L., Ma H., Tsai L.Y. Oxidative stress-related enzyme gene polymorphisms and susceptibility to breast cancer in non-smoking, non-alcohol-consuming Taiwanese women: a case-control study. Ann. Clin. Biochem. 2012;49(Pt. 2): 152-158. DOI 10.1258/acb.2011.011098Wang T., Wang H., Yang S., Guo H., Zhang B., Guo H., Wang L., Zhu G., Zhang Y., Zhou H., Zhang X., Li H., Su H. Association of APEX1 and OGG1 gene polymorphisms with breast cancer risk among Han women in the Gansu Province of China. BMC Med. Genet. 2018;19(1):67. DOI 10.1186/s12881-018-0578-9Wang T., Wang H., Yang S., Guo H., Zhang B., Guo H., Wang L., Zhu G., Zhang Y., Zhou H., Zhang X., Li H., Su H. Association of APEX1 and OGG1 gene polymorphisms with breast cancer risk among Han women in the Gansu Province of China. BMC Med. Genet. 2018;19(1):67. DOI 10.1186/s12881-018-0578-9Wang Z., Ayoub E., Mazouzi A., Grin I., Ishchenko A.A., Fan J., Yang X., Harihar T., Saparbaev M., Ramotar D. Functional variants of human APE1 rescue the DNA repair defects of the yeast AP endonuclease/3′-diesterase-deficient strain. DNA Repair. 2014;22: 53-66. DOI 10.1016/j.dnarep.2014.07.010Wang Z., Ayoub E., Mazouzi A., Grin I., Ishchenko A.A., Fan J., Yang X., Harihar T., Saparbaev M., Ramotar D. Functional variants of human APE1 rescue the DNA repair defects of the yeast AP endonuclease/3′-diesterase-deficient strain. DNA Repair. 2014;22: 53-66. DOI 10.1016/j.dnarep.2014.07.010World Health Organization. [Electronic resource]. URL: https://www.who.int/ru (accessed: 03.10.2023)World Health Organization. [Electronic resource]. URL: https://www.who.int/ru (accessed: 03.10.2023)Yan Y., Liang H., Light M., Li T., Deng Y., Li M., Li S., Qin X. XPD Asp312Asn and Lys751Gln polymorphisms and breast cancer susceptibility: a meta-analysis. Tumour Biol. 2014;35(3):1907-1915. DOI 10.1007/s13277-013-1256-3Yan Y., Liang H., Light M., Li T., Deng Y., Li M., Li S., Qin X. XPD Asp312Asn and Lys751Gln polymorphisms and breast cancer susceptibility: a meta-analysis. Tumour Biol. 2014;35(3):1907-1915. DOI 10.1007/s13277-013-1256-3Zhang H., Ahearn T.U., Lecarpentier J., Barnes D., Beesley J., Qi G., Jiang X., O’Mara T.A., Zhao N., Bolla M.K., … Kraft P., Simard J., Pharoah P.D.P., Michailidou K., Antoniou A.C., Schmidt M.K., Chenevix-Trench G., Easton D.F., Chatterjee N., García-Closas M. Genome-wide association study identifies 32 novel breast cancer susceptibility loci from overall and subtype-specific analyses. Nat. Genet. 2020;52(6):572-581. DOI 10.1038/s41588-020-0609-2Zhang H., Ahearn T.U., Lecarpentier J., Barnes D., Beesley J., Qi G., Jiang X., O’Mara T.A., Zhao N., Bolla M.K., … Kraft P., Simard J., Pharoah P.D.P., Michailidou K., Antoniou A.C., Schmidt M.K., Chenevix-Trench G., Easton D.F., Chatterjee N., García-Closas M. Genome-wide association study identifies 32 novel breast cancer susceptibility loci from overall and subtype-specific analyses. Nat. Genet. 2020;52(6):572-581. DOI 10.1038/s41588-020-0609-2Zhang L., Zhang Z., Yan W. Single nucleotide polymorphisms for DNA repair genes in breast cancer patients. Clin. Chim. Acta. 2005; 359(1-2):150-155. DOI 10.1016/j.cccn.2005.03.047Zhang L., Zhang Z., Yan W. Single nucleotide polymorphisms for DNA repair genes in breast cancer patients. Clin. Chim. Acta. 2005; 359(1-2):150-155. DOI 10.1016/j.cccn.2005.03.047

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