DNA repair genes polymorphisms and genetic susceptibility to Philadelphia-negative myeloproliferative neoplasms in a Portuguese population: The role of base excision repair genes polymorphisms

Azevedo,Ana  P.; Silva,Susana  N.; de Lima,João  P.; Reichert,Alice; Lima,Fernando; Júnior,Esmeraldina; Rueff,José

doi:10.3892/ol.2017.6065

DNA repair genes polymorphisms and genetic susceptibility to Philadelphia-negative myeloproliferative neoplasms in a Portuguese population: The role of base excision repair genes polymorphisms

Authors:
- Ana P. Azevedo
- Susana N. Silva
- João P. de Lima
- Alice Reichert
- Fernando Lima
- Esmeraldina Júnior
- José Rueff
View Affiliations

Affiliations: Centre for Toxicogenomics and Human Health (ToxOmics), Genetics, Oncology and Human Toxicology, NOVA Medical School, Faculty of Medical Sciences, NOVA University of Lisbon, 1169‑056 Lisbon, Portugal, Department of Clinical Haematology, Hospital of São Francisco Xavier, West Lisbon Hospital Centre, 1449‑005 Lisbon, Portugal, Department of Clinical Pathology, Hospital of São Francisco Xavier, West Lisbon Hospital Centre, 1449‑005 Lisbon, Portugal
Published online on: April 21, 2017 https://doi.org/10.3892/ol.2017.6065
Pages: 4641-4650
Copyright: © Azevedo et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

The role of base excision repair (BER) genes in Philadelphia-negative (PN)-myeloproliferative neoplasms (MPNs) susceptibility was evaluated by genotyping eight polymorphisms [apurinic/apyrimidinic endodeoxyribonuclease 1, mutY DNA glycosylase, earlier mutY homolog (E. coli) (MUTYH), 8‑oxoguanine DNA glycosylase 1, poly (ADP‑ribose) polymerase (PARP) 1, PARP4 and X‑ray repair cross‑complementing 1 (XRCC1)] in a case‑control study involving 133 Caucasian Portuguese patients. The results did not reveal a correlation between individual BER polymorphisms and PN‑MPNs when considered as a whole. However, stratification for essential thrombocythaemia revealed i) borderline effect/tendency to increased risk when carrying at least one variant allele for XRCC1_399 single‑nucleotide polymorphism (SNP); ii) decreased risk for Janus kinase 2‑positive patients carrying at least one variant allele for XRCC1_399 SNP; and iii) decreased risk in females carrying at least one variant allele for MUTYH SNP. Combination of alleles demonstrated an increased risk to PN‑MPNs for one specific haplogroup. These findings may provide evidence for gene variants in susceptibility to MPNs. Indeed, common variants in DNA repair genes may hamper the capacity to repair DNA, thus increasing cancer susceptibility.

View Figures

View References

1	Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J and Vardiman JW: WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. Fourth. IARC Press; Lyon: 2008
2	Arber DA, Orazi A, Hasserjian R, Thiele J, Borowitz MJ, Le Beau MM, Bloomfield CD, Cazzola M and Vardiman JW: The 2016 revision to the world health organization classification of myeloid neoplasms and acute leukemia. Blood. 127:2391–2405. 2016. View Article : Google Scholar : PubMed/NCBI
3	James C, Ugo V, Le Couédic JP, Staerk J, Delhommeau F, Lacout C, Garçon L, Raslova H, Berger R, Bennaceur-Griscelli A, et al: A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature. 434:1144–1148. 2005. View Article : Google Scholar : PubMed/NCBI
4	Kralovics R, Passamonti F, Buser AS, Teo SS, Tiedt R, Passweg JR, Tichelli A, Cazzola M and Skoda RC: A gain-of-function mutation of JAK2 in myeloproliferative disorders. N Engl J Med. 352:1779–1790. 2005. View Article : Google Scholar : PubMed/NCBI
5	Levine RL, Wadleigh M, Cools J, Ebert BL, Wernig G, Huntly BJ, Boggon TJ, Wlodarska I, Clark JJ, Moore S, et al: Activating mutation in the tyrosine kinase JAK2 in polycythemia vera, essential thrombocythemia, and myeloid metaplasia with myelofibrosis. Cancer Cell. 7:387–397. 2005. View Article : Google Scholar : PubMed/NCBI
6	Baxter EJ, Scott LM, Campbell PJ, East C, Fourouclas N, Swanton S, Vassiliou GS, Bench AJ, Boyd EM, Curtin N, et al: Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. Lancet. 365:1054–1061. 2005. View Article : Google Scholar : PubMed/NCBI
7	Scott LM, Tong W, Levine RL, Scott MA, Beer PA, Stratton MR, Futreal PA, Erber WN, McMullin MF, Harrison CN, et al: JAK2 exon 12 mutations in polycythemia vera and idiopathic erythrocytosis. N Engl J Med. 356:459–468. 2007. View Article : Google Scholar : PubMed/NCBI
8	Chi J, Manoloukos M, Pierides C, Nicolaidou V, Nicolaou K, Kleopa M, Vassiliou G and Costeas P: Calreticulin mutations in myeloproliferative neoplasms and new methodology for their detection and monitoring. Ann Hematol. 94:399–408. 2015. View Article : Google Scholar : PubMed/NCBI
9	Ha JS and Kim YK: Calreticulin exon 9 mutations in myeloproliferative neoplasms. Ann Lab Med. 35:22–27. 2015. View Article : Google Scholar : PubMed/NCBI
10	Klampfl T, Gisslinger H, Harutyunyan AS, Nivarthi H, Rumi E, Milosevic JD, Them NC, Berg T, Gisslinger B, Pietra D, et al: Somatic mutations of calreticulin in myeloproliferative neoplasms. N Engl J Med. 369:2379–2390. 2013. View Article : Google Scholar : PubMed/NCBI
11	Rumi E, Pietra D, Ferretti V, Klampfl T, Harutyunyan AS, Milosevic JD, Them NC, Berg T, Elena C, Casetti IC, et al: JAK2 or CALR mutation status defines subtypes of essential thrombocythemia with substantially different clinical course and outcomes. Blood. 123:1544–1551. 2014. View Article : Google Scholar : PubMed/NCBI
12	Tefferi A and Pardanani A: Myeloproliferative neoplasms: A contemporary review. JAMA Oncol. 1:97–105. 2015. View Article : Google Scholar : PubMed/NCBI
13	Nangalia J, Massie CE, Baxter EJ, Nice FL, Gundem G, Wedge DC, Avezov E, Li J, Kollmann K, Kent DG, et al: Somatic CALR mutations in myeloproliferative neoplasms with nonmutated JAK2. N Engl J Med. 369:2391–2405. 2013. View Article : Google Scholar : PubMed/NCBI
14	Delhommeau F, Jeziorowska D, Marzac C and Casadevall N: Molecular aspects of myeloproliferative neoplasms. Int J Hematol. 91:165–173. 2010. View Article : Google Scholar : PubMed/NCBI
15	Levine RL: Mechanisms of mutations in myeloproliferative neoplasms. Best Pract Res Clin Haematol. 22:489–494. 2009. View Article : Google Scholar : PubMed/NCBI
16	Campregher PV, Santos FP, Perini GF and Hamerschlak N: Molecular biology of Philadelphia-negative myeloproliferative neoplasms. Rev Bras Hematol Hemoter. 34:150–155. 2012. View Article : Google Scholar : PubMed/NCBI
17	Rueff J and Rodrigues AS: Cancer drug resistance: A brief overview from a genetic viewpoint. Methods Mol Biol. 1395:1–18. 2016. View Article : Google Scholar : PubMed/NCBI
18	Mesa R, Miller CB, Thyne M, Mangan J, Goldberger S, Fazal S, Ma X, Wilson W, Paranagama DC, Dubinski DG, et al: Myeloproliferative neoplasms (MPNs) have a significant impact on patients' overall health and productivity: The MPN landmark survey. BMC Cancer. 16:1672016. View Article : Google Scholar : PubMed/NCBI
19	Passamonti F, Rumi E, Pungolino E, Malabarba L, Bertazzoni P, Valentini M, Orlandi E, Arcaini L, Brusamolino E, Pascutto C, et al: Life expectancy and prognostic factors for survival in patients with polycythemia vera and essential thrombocythemia. Am J Med. 117:755–761. 2004. View Article : Google Scholar : PubMed/NCBI
20	Wolanskyj AP, Schwager SM, McClure RF, Larson DR and Tefferi A: Essential thrombocythemia beyond the first decade: Life expectancy, long-term complication rates, and prognostic factors. Mayo Clin Proc. 81:159–166. 2006. View Article : Google Scholar : PubMed/NCBI
21	Björkholm M, Hultcrantz M and Derolf ÅR: Leukemic transformation in myeloproliferative neoplasms: Therapy-related or unrelated? Best Pract Res Clin Haematol. 27:141–153. 2014. View Article : Google Scholar : PubMed/NCBI
22	Rampal R, Ahn J, Abdel-Wahab O, Nahas M, Wang K, Lipson D, Otto GA, Yelensky R, Hricik T, McKenney AS, et al: Genomic and functional analysis of leukemic transformation of myeloproliferative neoplasms. Proc Natl Acad Sci USA. 111:pp. E5401–E5410. 2014; View Article : Google Scholar : PubMed/NCBI
23	Björkholm M, Hultcrantz M and Derolf ÅR: Leukemic transformation in myeloproliferative neoplasms: Therapy-related or unrelated? Best Pract Res Clin Haematol. 27:141–153. 2014. View Article : Google Scholar : PubMed/NCBI
24	Hernández-Boluda JC, Pereira A, Cervantes F, Alvarez-Larrán A, Collado M, Such E, Arilla MJ, Boqué C, Xicoy B, Maffioli M, et al: A polymorphism in the XPD gene predisposes to leukemic transformation and new nonmyeloid malignancies in essential thrombocythemia and polycythemia vera. Blood. 119:5221–5228. 2012. View Article : Google Scholar : PubMed/NCBI
25	Bolufer P, Barragan E, Collado M, Cervera J, López JA and Sanz MA: Influence of genetic polymorphisms on the risk of developing leukemia and on disease progression. Leuk Res. 30:1471–1491. 2006. View Article : Google Scholar : PubMed/NCBI
26	Beer PA, Delhommeau F, LeCouédic JP, Dawson MA, Chen E, Bareford D, Kusec R, McMullin MF, Harrison CN, Vannucchi AM, et al: Two routes to leukemic transformation after a JAK2 mutation-positive myeloproliferative neoplasm. Blood. 115:2891–2900. 2010. View Article : Google Scholar : PubMed/NCBI
27	Hasselbalch HC, Thomassen M, Riley CH, Kjær L, Larsen TS, Jensen MK, Bjerrum OW, Kruse TA and Skov V: Whole blood transcriptional profiling reveals deregulation of oxidative and antioxidative defence genes in myelofibrosis and related neoplasms. Potential implications of downregulation of Nrf2 for genomic instability and disease progression. PLoS One. 9:e1127862014. View Article : Google Scholar : PubMed/NCBI
28	Kilpivaara O and Levine RL: JAK2 and MPL mutations in myeloproliferative neoplasms: Discovery and science. Leukemia. 22:1813–1817. 2008. View Article : Google Scholar : PubMed/NCBI
29	Batar B, Güven M, Bariş S, Celkan T and Yildiz I: DNA repair gene XPD and XRCC1 polymorphisms and the risk of childhood acute lymphoblastic leukemia. Leuk Res. 33:759–763. 2009. View Article : Google Scholar : PubMed/NCBI
30	Bănescu C, Trifa AP, Demian S, Lazar E Benedek, Dima D, Duicu C and Dobreanu M: Polymorphism of XRCC1, XRCC3, and XPD genes and risk of chronic myeloid leukemia. Biomed Res Int. 2014:2137902014. View Article : Google Scholar : PubMed/NCBI
31	Hoeijmakers JH: Genome maintenance mechanisms for preventing cancer. Nature. 411:366–374. 2001. View Article : Google Scholar : PubMed/NCBI
32	Wang CQ, Krishnan V, Tay LS, Chin DW, Koh CP, Chooi JY, Nah GS, Du L, Jacob B, Yamashita N, et al: Disruption of Runx1 and Runx3 leads to bone marrow failure and leukemia predisposition due to transcriptional and DNA repair defects. Cell Rep. 8:767–782. 2014. View Article : Google Scholar : PubMed/NCBI
33	Silva SN, Moita R, Azevedo AP, Gouveia R, Manita I, Pina JE, Rueff J and Gaspar J: Menopausal age and XRCC1 gene polymorphisms: Role in breast cancer risk. Cancer Detect Prev. 31:303–309. 2007. View Article : Google Scholar : PubMed/NCBI
34	Santos LS, Branco SC, Silva SN, Azevedo AP, Gil OM, Manita I, Ferreira TC, Limbert E, Rueff J and Gaspar JF: Polymorphisms in base excision repair genes and thyroid cancer risk. Oncol Rep. 28:1859–1868. 2012.PubMed/NCBI
35	Yan L, Li Q, Li X, Ji H and Zhang L: Association studies between XRCC1, XRCC2, XRCC3 polymorphisms and differentiated thyroid carcinoma. Cell Physiol Biochem. 38:1075–1084. 2016. View Article : Google Scholar : PubMed/NCBI
36	Baute J and Depicker A: Base excision repair and its role in maintaining genome stability. Crit Rev Biochem Mol Biol. 43:239–276. 2008. View Article : Google Scholar : PubMed/NCBI
37	Annamaneni S, Gorre M, Kagita S, Addepalli K, Digumarti RR, Satti V and Battini MR: Association of XRCC1 gene polymorphisms with chronic myeloid leukemia in the population of Andhra Pradesh, India. Hematology. 18:163–168. 2013. View Article : Google Scholar : PubMed/NCBI
38	Tefferi A and Vardiman JW: Classification and diagnosis of myeloproliferative neoplasms: The 2008 world health organization criteria and point-of-care diagnostic algorithms. Leukemia. 22:14–22. 2008. View Article : Google Scholar : PubMed/NCBI
39	Bastos HN, Antão MR, Silva SN, Azevedo AP, Manita I, Teixeira V, Pina JE, Gil OM, Ferreira TC, Limbert E, et al: Association of polymorphisms in genes of the homologous recombination DNA repair pathway and thyroid cancer risk. Thyroid. 19:1067–1075. 2009. View Article : Google Scholar : PubMed/NCBI
40	Conde J, Silva SN, Azevedo AP, Teixeira V, Pina JE, Rueff J and Gaspar JF: Association of common variants in mismatch repair genes and breast cancer susceptibility: A multigene study. BMC Cancer. 9:3442009. View Article : Google Scholar : PubMed/NCBI
41	Gomes BC, Silva SN, Azevedo AP, Manita I, Gil OM, Ferreira TC, Limbert E, Rueff J and Gaspar JF: The role of common variants of non-homologous end-joining repair genes XRCC4, LIG4 and Ku80 in thyroid cancer risk. Oncol Rep. 24:1079–1085. 2010.PubMed/NCBI
42	Silva SN, Azevedo AP, Teixeira V, Pina JE, Rueff J and Gaspar JF: The role of GSTA2 polymorphisms and haplotypes in breast cancer susceptibility: A case-control study in the Portuguese population. Oncol Rep. 22:593–598. 2009.PubMed/NCBI
43	Sole X, Guinó E, Valls J, Iniesta R and Moreno V: SNPStats: A web tool for the analysis of association studies. Bioinformatics. 22:1928–1929. 2006. View Article : Google Scholar : PubMed/NCBI
44	Geyer HL, Kosiorek H, Dueck AC, Scherber R, Slot S, Zweegman S, Te Boekhorst PA, Senyak Z, Schouten HC, Sackmann F, et al: Associations between gender, disease features and symptom burden in patients with myeloproliferative neoplasms: An analysis by the MPN QOL international working group. Haematologica. 102:85–93. 2017. View Article : Google Scholar : PubMed/NCBI
45	Figueroa JD, Malats N, Real FX, Silverman D, Kogevinas M, Chanock S, Welch R, Dosemeci M, Tardón A, Serra C, et al: Genetic variation in the base excision repair pathway and bladder cancer risk. Hum Genet. 121:233–242. 2007. View Article : Google Scholar : PubMed/NCBI
46	Wilson DM, Kim D, Berquist BR and Sigurdson AJ: Variation in base excision repair capacity. Mutat Res. 711:100–112. 2011. View Article : Google Scholar : PubMed/NCBI
47	Walter D, Lier A, Geiselhart A, Thalheimer FB, Huntscha S, Sobotta MC, Moehrle B, Brocks D, Bayindir I, Kaschutnig P, et al: Exit from dormancy provokes DNA-damage-induced attrition in haematopoietic stem cells. Nature. 520:549–552. 2015. View Article : Google Scholar : PubMed/NCBI
48	Hirotsu Y, Nakagomi H, Sakamoto I, Amemiya K, Oyama T, Mochizuki H and Omata M: Multigene panel analysis identified germline mutations of DNA repair genes in breast and ovarian cancer. Mol Genet Genomic Med. 3:459–466. 2015. View Article : Google Scholar : PubMed/NCBI
49	Cheadle JP and Sampson JR: MUTYH-associated polyposis-from defect in base excision repair to clinical genetic testing. DNA Repair (Amst). 6:274–279. 2007. View Article : Google Scholar : PubMed/NCBI
50	Picelli S, Zajac P, Zhou XL, Edler D, Lenander C, Dalén J, Hjern F, Lundqvist N, Lindforss U, Påhlman L, et al: Common variants in human CRC genes as low-risk alleles. Eur J Cancer. 46:1041–1048. 2010. View Article : Google Scholar : PubMed/NCBI
51	Przybylowska K, Kabzinski J, Sygut A, Dziki L, Dziki A and Majsterek I: An association selected polymorphisms of XRCC1, OGG1 and MUTYH gene and the level of efficiency oxidative DNA damage repair with a risk of colorectal cancer. Mutat Res. 745–746. 6–15. 2013.
52	Tao H, Shinmura K, Suzuki M, Kono S, Mibu R, Tanaka M, Kakeji Y, Maehara Y, Okamura T, Ikejiri K, et al: Association between genetic polymorphisms of the base excision repair gene MUTYH and increased colorectal cancer risk in a Japanese population. Cancer Sci. 99:355–360. 2008. View Article : Google Scholar : PubMed/NCBI
53	Qian B, Zhang H, Zhang L, Zhou X, Yu H and Chen K: Association of genetic polymorphisms in DNA repair pathway genes with non-small cell lung cancer risk. Lung Cancer. 73:138–146. 2011. View Article : Google Scholar : PubMed/NCBI
54	Huang M, Dinney CP, Lin X, Lin J, Grossman HB and Wu X: High-order interactions among genetic variants in DNA base excision repair pathway genes and smoking in bladder cancer susceptibility. Cancer Epidemiol Biomarkers Prev. 16:84–91. 2007. View Article : Google Scholar : PubMed/NCBI
55	Zhang Y, Newcomb PA, Egan KM, Titus-Ernstoff L, Chanock S, Welch R, Brinton LA, Lissowska J, Bardin-Mikolajczak A, Peplonska B, et al: Genetic polymorphisms in base-excision repair pathway genes and risk of breast cancer. Cancer Epidemiol Biomarkers Prev. 15:353–358. 2006. View Article : Google Scholar : PubMed/NCBI
56	Das S, Bhowmik A, Bhattacharjee A, Choudhury B, Naiding M, Laskar AK, Ghosh SK and Choudhury Y: XPD, APE1, and MUTYH polymorphisms increase head and neck cancer risk: Effect of gene-gene and gene-environment interactions. Tumour Biol. 36:7569–7579. 2015. View Article : Google Scholar : PubMed/NCBI
57	Picelli S, Bermejo J Lorenzo, Chang-Claude J, Hoffmeister M, Fernández-Rozadilla C, Carracedo A, Castells A, Castellví-Bel S and of EPICOLON Memebers: Consortium-Gastrointestinal Oncology Group of the Spanish Gastroenterological Association and Naccarati A et al. Meta-analysis of mismatch repair polymorphisms within the cogent consortium for colorectal cancer susceptibility. PLoS One. 8:e720912013. View Article : Google Scholar : PubMed/NCBI
58	Lévy N, Martz A, Bresson A, Spenlehauer C, de Murcia G and Ménissier-de Murcia J: XRCC1 is phosphorylated by DNA-dependent protein kinase in response to DNA damage. Nucleic Acids Res. 34:32–41. 2006. View Article : Google Scholar : PubMed/NCBI
59	Hung RJ, Hall J, Brennan P and Boffetta P: Genetic polymorphisms in the base excision repair pathway and cancer risk: A HuGE review. Am J Epidemiol. 162:925–942. 2005. View Article : Google Scholar : PubMed/NCBI
60	Ginsberg G, Angle K, Guyton K and Sonawane B: Polymorphism in the DNA repair enzyme XRCC1: Utility of current database and implications for human health risk assessment. Mutat Res. 727:1–15. 2011. View Article : Google Scholar : PubMed/NCBI
61	Jiang J, Zhang X, Yang H and Wang W: Polymorphisms of DNA repair genes: ADPRT, XRCC1, and XPD and cancer risk in genetic epidemiology. Methods Mol Biol. 471:305–333. 2009. View Article : Google Scholar : PubMed/NCBI
62	Miao X, Zhang X, Zhang L, Guo Y, Hao B, Tan W, He F and Lin D: Adenosine diphosphate ribosyl transferase and x-ray repair cross-complementing 1 polymorphisms in gastric cardia cancer. Gastroenterology. 131:420–427. 2006. View Article : Google Scholar : PubMed/NCBI
63	Zhai X, Liu J, Hu Z, Wang S, Qing J, Wang X, Jin G, Gao J, Wang X and Shen H: Polymorphisms of ADPRT Val762Ala and XRCC1 Arg399Glu and risk of breast cancer in Chinese women: A case control analysis. Oncol Rep. 15:247–252. 2006.PubMed/NCBI
64	Hu Z, Ma H, Chen F, Wei Q and Shen H: XRCC1 polymorphisms and cancer risk: A meta-analysis of 38 case-control studies. Cancer Epidemiol Biomarkers Prev. 14:1810–1818. 2005. View Article : Google Scholar : PubMed/NCBI
65	Srivastava A, Srivastava K, Pandey SN, Choudhuri G and Mittal B: Single-nucleotide polymorphisms of DNA repair genes OGG1 and XRCC1: Association with gallbladder cancer in North Indian population. Ann Surg Oncol. 16:1695–1703. 2009. View Article : Google Scholar : PubMed/NCBI
66	Chen B, Zhou Y, Yang P and Wu XT: Polymorphisms of XRCC1 and gastric cancer susceptibility: A meta-analysis. Mol Biol Rep. 39:1305–1313. 2012. View Article : Google Scholar : PubMed/NCBI
67	Zou H, Li Q, Xia W, Liu Y, Wei X and Wang D: Association between the OGG1 Ser326Cys polymorphism and cancer risk: Evidence from 152 Case-Control studies. J Cancer. 7:1273–1280. 2016. View Article : Google Scholar : PubMed/NCBI
68	Wei B, Zhou Y, Xu Z, Xi B, Cheng H, Ruan J, Zhu M, Hu Q, Wang Q, Wang Z, et al: The effect of hOGG1 Ser326Cys polymorphism on cancer risk: Evidence from a meta-analysis. PLoS One. 6:e275452011. View Article : Google Scholar : PubMed/NCBI
69	Kumar A, Pant MC, Singh HS and Khandelwal S: Role of OGG1 Ser326Cys polymorphism and 8-oxoguanine DNA damage in risk assessment of squamous cell carcinoma of head and neck in North Indian population. Mutat Res. 726:227–233. 2011. View Article : Google Scholar : PubMed/NCBI
70	Wang W, Wang M, Chen Y and Zhang Z, Wang S, Xu M, Wang B, Zhao Q and Zhang Z: The hOGG1 Ser326Cys polymorphism contributes to cancer susceptibility: Evidence from 83 case-control studies. Mutagenesis. 27:329–336. 2012. View Article : Google Scholar : PubMed/NCBI
71	Canbay E, Cakmakoglu B, Zeybek U, Sozen S, Cacina C, Gulluoglu M, Balik E, Bulut T, Yamaner S and Bugra D: Association of APE1 and hOGG1 polymorphisms with colorectal cancer risk in a Turkish population. Curr Med Res Opin. 27:1295–1302. 2011. View Article : Google Scholar : PubMed/NCBI
72	Srivastava K, Srivastava A and Mittal B: Polymorphisms in ERCC2, MSH2, and OGG1 DNA repair genes and gallbladder cancer risk in a population of Northern India. Cancer. 116:3160–3169. 2010. View Article : Google Scholar : PubMed/NCBI
73	Gu D, Wang M, Zhang Z and Chen J: Lack of association between the hOGG1 Ser326Cys polymorphism and breast cancer risk: Evidence from 11 case-control studies. Breast Cancer Res Treat. 122:527–531. 2010. View Article : Google Scholar : PubMed/NCBI
74	Fahmideh M Adel, Schwartzbaum J, Frumento P and Feychting M: Association between DNA repair gene polymorphisms and risk of glioma: A systematic review and meta-analysis. Neuro Oncol. 16:807–814. 2014. View Article : Google Scholar : PubMed/NCBI
75	Das S, Nath S, Bhowmik A, Ghosh SK and Choudhury Y: Association between OGG1 Ser326Cys polymorphism and risk of upper aero-digestive tract and gastrointestinal cancers: A meta-analysis. Springerplus. 5:2272016. View Article : Google Scholar : PubMed/NCBI
76	Wenjuan C, Jianzhong L, Chong L, Yanjun G, Keqing L, Hanzhang W and Zhiping W: The hOGG1 Ser326Cys gene polymorphism and susceptibility for bladder cancer: A meta-analysis. Int Braz J Urol. 42:883–896. 2016. View Article : Google Scholar : PubMed/NCBI
77	Abbotts R and Madhusudan S: Human AP endonuclease 1 (APE1): From mechanistic insights to druggable target in cancer. Cancer Treat Rev. 36:425–435. 2010. View Article : Google Scholar : PubMed/NCBI
78	Dyrkheeva NS, Lebedeva NA and Lavrik OI: AP endonuclease 1 as a key enzyme in repair of Apurinic/Apyrimidinic sites. Biochemistry (Mosc). 81:951–967. 2016. View Article : Google Scholar : PubMed/NCBI
79	Peng Q, Lu Y, Lao X, Chen Z, Li R, Sui J, Qin X and Li S: Association between OGG1 Ser326Cys and APEX1 Asp148Glu polymorphisms and breast cancer risk: A meta-analysis. Diagn Pathol. 9:1082014. View Article : Google Scholar : PubMed/NCBI
80	Zhao Z, Liu C, Zeng Y, Gu L, Ying M, Wang N, Hao B, Yao H, Su C, Wang Y and Ma Y: The association between the APE1 Asp148Glu polymorphism and breast cancer susceptibility: A meta-analysis based on case-control studies. Tumour Biol. 35:4727–4734. 2014. View Article : Google Scholar : PubMed/NCBI
81	Wu B, Liu HL, Zhang S, Dong XR and Wu G: Lack of an association between two BER gene polymorphisms and breast cancer risk: A meta-analysis. PLoS One. 7:e508572012. View Article : Google Scholar : PubMed/NCBI
82	Zhou X, Wei L, Jiao G, Gao W, Ying M, Wang N, Wang Y and Liu C: The association between the APE1 Asp148Glu polymorphism and prostate cancer susceptibility: A meta-analysis based on case-control studies. Mol Genet Genomics. 290:281–288. 2015. View Article : Google Scholar : PubMed/NCBI
83	Li X, Zhang G, Huai YJ and Cao ZQ: Association between APE1 T1349G polymorphism and prostate cancer risk: Evidence from a meta-analysis. Tumour Biol. 35:10111–10119. 2014. View Article : Google Scholar : PubMed/NCBI
84	Li H, Zou J, Mi J, Wei X, Zhao D, Zhang S and Tian G: Association of APE1 Gene Asp148Glu variant with digestive cancer: A meta-analysis. Med Sci Monit. 21:2456–2466. 2015. View Article : Google Scholar : PubMed/NCBI
85	Dai ZJ, Shao YP, Kang HF, Tang W, Xu D, Zhao Y, Liu D, Wang M, Yang PT and Wang XJ: Relationship between apurinic endonuclease 1 Asp148Glu polymorphism and gastrointestinal cancer risk: An updated meta-analysis. World J Gastroenterol. 21:5081–5089. 2015. View Article : Google Scholar : PubMed/NCBI
86	Jin F, Qian C, Qing Y, Zhang Z, Wang G, Shan J, Dai N, Li Z and Wang D: Genetic polymorphism of APE1 rs1130409 can contribute to the risk of lung cancer. Tumour Biol. 35:6665–6671. 2014. View Article : Google Scholar : PubMed/NCBI
87	Hu D, Lin X, Zhang H, Zheng X and Niu W: APEX nuclease (multifunctional DNA repair enzyme) 1 gene Asp148Glu polymorphism and cancer risk: A meta-analysis involving 58 articles and 48903 participants. PLoS One. 8:e835272013. View Article : Google Scholar : PubMed/NCBI
88	Talhaoui I, Lebedeva NA, Zarkovic G, Saint-Pierre C, Kutuzov MM, Sukhanova MV, Matkarimov BT, Gasparutto D, Saparbaev MK, Lavrik OI and Ishchenko AA: Poly(ADP-ribose) polymerases covalently modify strand break termini in DNA fragments in vitro. Nucleic Acids Res. 44:9279–9295. 2016.PubMed/NCBI
89	Wei H and Yu X: Functions of PARylation in DNA damage repair pathways. Genomics Proteomics Bioinformatics. 14:131–139. 2016. View Article : Google Scholar : PubMed/NCBI
90	Qin Q, Lu J, Zhu H, Xu L, Cheng H, Zhan L, Yang X, Zhang C and Sun X: PARP-1 Val762Ala polymorphism and risk of cancer: A meta-analysis based on 39 case-control studies. PLoS One. 9:e980222014. View Article : Google Scholar : PubMed/NCBI
91	Hua RX, Li HP, Liang YB, Zhu JH, Zhang B, Ye S, Dai QS, Xiong SQ, Gu Y and Sun XZ: Association between the PARP1 Val762Ala polymorphism and cancer risk: Evidence from 43 studies. PLoS One. 9:e870572014. View Article : Google Scholar : PubMed/NCBI
92	Hu Y, Zhou M, Li K, Zhang K, Kong X, Zheng Y, Li J and Liu L: Two DNA repair gene polymorphisms on the risk of gastrointestinal cancers: A meta-analysis. Tumour Biol. 35:1715–1725. 2014. View Article : Google Scholar : PubMed/NCBI
93	Lindholm Sørensen A and Hasselbalch HC: Smoking and philadelphia-negative chronic myeloproliferative neoplasms. Eur J Haematol. 97:63–69. 2016. View Article : Google Scholar : PubMed/NCBI
94	Hasselbalch HC: Smoking as a contributing factor for development of polycythemia vera and related neoplasms. Leuk Res pii. S0145–2126. 2015.