DOI QR코드

DOI QR Code

Different Association of Manganese Superoxide Dismutase Gene Polymorphisms with Risk of Prostate, Esophageal, and Lung Cancers: Evidence from a Meta-analysis of 20,025 Subjects

  • Sun, Guo-Gui (Department of Chemoradiation Therapy, Tangshan People's Hospital) ;
  • Wang, Ya-Di (Department of Radiotherapy, The Military General Hospital of Beijing PLA) ;
  • Lu, Yi-Fang (Department of Endocrinology, Tangshan Workers Hospital) ;
  • Hu, Wan-Ning (Department of Chemoradiation Therapy, Tangshan People's Hospital)
  • Published : 2013.03.30

Abstract

Altered expression or function of manganese superoxide dismutase (MnSOD) has been shown to be associated with cancer risk but assessment of gene polymorphisms has resulted in inconclusive data. Here a search of published data was made and 22 studies were recruited, covering 20,025 case and control subjects, for meta-analyses of the association of MnSOD polymorphisms with the risk of prostate, esophageal, and lung cancers. The data on 12 studies of prostate cancer (including 4,182 cases and 6,885 controls) showed a statistically significant association with the risk of development in co-dominant models and dominant models, but not in the recessive model. Subgroup analysis showed there was no statistically significant association of MnSOD polymorphisms with aggressive or nonaggressive prostate cancer in different genetic models. In addition, the data on four studies of esophageal cancer containing 620 cases and 909 controls showed a statistically significant association between MnSOD polymorphisms and risk in all comparison models. In contrast, the data on six studies of lung cancer with 3,375 cases and 4,050 controls showed that MnSOD polymorphisms were significantly associated with the decreased risk of lung cancer in the homozygote and dominant models, but not the heterozygote model. A subgroup analysis of the combination of MnSOD polymorphisms with tobacco smokers did not show any significant association with lung cancer risk, histological type, or clinical stage of lung cancer. The data from the current study indicated that the Ala allele MnSOD polymorphism is associated with increased risk of prostate and esophageal cancers, but with decreased risk of lung cancer. The underlying molecular mechanisms warrant further investigation.

Acknowledgement

Supported by : National Natural Science Foundation

References

  1. Ambrosone CB, Freudenheim JL, Thompson PA, et al (1999), Manganese superoxide dismutase (MnSOD) genetic polymorphisms, dietary antioxidants, and risk of breast cancer. Cancer Res, 59, 602-6.
  2. Arsova-Sarafinovska Z, Matevska N, Petrovski D, et al (2008). Manganese superoxide dismutase (MnSOD) genetic polymorphism is associated with risk of early-onset prostate cancer. Cell Biochem Funct, 26, 771-7. https://doi.org/10.1002/cbf.1504
  3. Bica CG, de Moura da Silva LL, et al (2009). MnSOD gene polymorphism association with steroid-dependent cancer. Pathol Oncol Res, 15, 19-24. https://doi.org/10.1007/s12253-008-9064-6
  4. Cai Q, Shu XO, Wen W, et al (2004). Genetic polymorphism in the manganese superoxide dismutase gene, antioxidant intake, and breast cancer risk, results from the Shanghai Breast Cancer Study. Breast Cancer Res, 6, 647-55. https://doi.org/10.1186/bcr929
  5. Cheng YJ, Wang YD, Liu Q, et al (2009). Occurrence and development relation between superoxide dismutase gene polymorphism and esophagus. Chin J Oncol, 31, 831-5.
  6. Choi JY, Neuhouser ML, Barnett M, et al (2007). polymorphisms in oxidative stress-related genes are not associated with prostate cancer risk in heavy smokers. Cancer Epidemiol Biomarkers Prev, 16, 1115-20. https://doi.org/10.1158/1055-9965.EPI-07-0040
  7. Choi JY, Neuhouser ML, Barnett MJ, et al (2008). Iron intake, oxidative stress-related genes (MnSOD and MPO) and prostate cancer risk in CARET cohort. Carcinogenesis, 29, 964-70. https://doi.org/10.1093/carcin/bgn056
  8. DerSimonian R, Laird N (1986). Meta-analysis in clinical trials. Control Clin Trials, 7, 177-88. https://doi.org/10.1016/0197-2456(86)90046-2
  9. di Martino E, Hardie LJ, Wild CP, et al (2007). The NAD(P)H, quinone oxidoreductase I C609T polymorphism modifies the risk of Barrett esophagus and esophageal adenocarcinoma. Genet Med, 9, 341-7. https://doi.org/10.1097/GIM.0b013e3180654ccd
  10. Egan KM, Thompson PA, Titus-Ernstoff L, Moore JH, Ambrosone CB (2003). MnSOD polymorphism and breast cancer in a population-based case-control study. Cancer Lett, 199, 27-33. https://doi.org/10.1016/S0304-3835(03)00349-5
  11. Ergen HA, Narter F, Timirci O, Isbir T (2007). Effects of manganese superoxide dismutase Val-9Ala polymorphism on prostate cancer. Anticancer Res, 27, 1227-30.
  12. Ho JC, Mak JC, Ho SP, et al (2006). Manganese superoxide dismutase and catalase genetic polymorphisms, activity levels, and lung cancer risk in Chinese in Hong Kong. J Thorac Oncol, 1, 648-53. https://doi.org/10.1097/01243894-200609000-00008
  13. Hung RJ, Boffetta P, Brennan P, et al (2004). Genetic polymorphisms of MPO, COMT, MnSOD, NQO1, interactions with environmental exposures and bladder cancer risk. Carcinogenesis, 25, 973-8. https://doi.org/10.1093/carcin/bgh080
  14. Iguchi T, Sugita S, Wang CY, et al (2009). MnSOD genotype and prostate cancer risk as a function of NAT genotype and smoking status. In Vivo, 23, 7-12.
  15. Iguchi T, Wang CY, Delongchamps NB, et al (2008). Association of prostate cancer and manganese superoxide dismutase AA genotype influenced by presence of occult cancer in control group. Urology, 72, 238-41. https://doi.org/10.1016/j.urology.2008.03.064
  16. Kang D, Lee KM, Park SK, et al (2007). Functional variant of manganese superoxide dismutase (SOD2 V16A) polymorphism is associated with prostate cancer risk in the prostate, lung, colorectal, and ovarian cancer study. Cancer Epidemiol Biomarkers Prev, 16, 1581-6. https://doi.org/10.1158/1055-9965.EPI-07-0160
  17. Komatsu M, Kuroda M, Wang Y, et al (2005). Manganese superoxide dismutase overexpression changes plating efficiency bidirectionally according to change in redox for SaOS2 human osteosarcoma cell line. Int J Oncology, 26, 853-62.
  18. Li H, Kantoff PW, Giovannucci E, et al (2005). Manganese superoxide dismutase polymorphism, prediagnostic antioxidant status, and risk of clinical significant prostate cancer. Cancer Res, 65, 2498-504. https://doi.org/10.1158/0008-5472.CAN-04-3535
  19. Li N, Oberley TD, Oberley LW, Zhong W (1998). Overexpression of manganese superoxide dismutase in DU145 human prostate carcinoma cells has multiple effects on cell phenotype. Prostate, 35, 221-33. https://doi.org/10.1002/(SICI)1097-0045(19980515)35:3<221::AID-PROS8>3.0.CO;2-J
  20. Lin P, Hsueh YM, Ko JL, et al (2003). Analysis of NQO1, GSTP1, and MnSOD genetic polymorphisms on lung cancer risk in Taiwan. Lung Cancer, 40, 123-9. https://doi.org/10.1016/S0169-5002(03)00027-8
  21. Liu G, Zhou W, Park S, et al (2004). The SOD2 Val/Val genotype enhances the risk of nonsmall cell lung carcinoma by p53 and XRCC1 polymorphisms. Cancer, 101, 2802-8. https://doi.org/10.1002/cncr.20716
  22. Mantel-Haenszel, Mantel N, Haenszel W (1959). Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst, 22, 719-48.
  23. Mikhak B, Hunter DJ, Spiegelman D, et al (2008). Manganese superoxide dismutase (MnSOD) gene polymorphism, interactions with carotenoid levels and prostate cancer risk. Carcinogenesis, 29, 2335-40. https://doi.org/10.1093/carcin/bgn212
  24. Mitrunen K, Sillanpaa V, Kataja M, et al (2001). Association between manganese superoxide dismutase (MnSOD) gene polymorphism and breast cancer risk. Carcinogenesis, 22, 827-9. https://doi.org/10.1093/carcin/22.5.827
  25. Murphy SJ, Hughes AE, Patterson CC, et al (2007). A populationbased association study of SNPs of GSTP1, MnSOD, GPX2 and Barrett's esophagus and esophageal adenocarcinoma. Carcinogenesis, 28, 1323-28. https://doi.org/10.1093/carcin/bgm007
  26. Oberley TD (2004). Mitochondria, manganese superoxide dismutase, and cancer. Antioxid Redox Signal, 6, 483-7. https://doi.org/10.1089/152308604773934242
  27. Orrenius S, Gogvadze V, Zhivotovsky B (2007). Mitochondrial oxidative stress, implications for cell death. Annu Rev Pharmacol Toxicol, 47, 143-83. https://doi.org/10.1146/annurev.pharmtox.47.120505.105122
  28. Soini Y, Vakkala M, Kahlos K Pääkkö P, Kinnula V (2001). MnSOD expression is less frequent in tumour cells of invasive breast carcinomas than in situ carcinomas or nonneoplastic breast epithelial cells. J Pathol, 195, 156-62. https://doi.org/10.1002/path.946
  29. Sun GG,Hu WN,Wang YD,Yang CR,Lu YF (2012). Bidirectional regulation of manganese superoxide dismutase (MnSOD) on the radiosensitivity of esophageal cancer cells. Asian Pac J Cancer Prev, 13, 1-9. https://doi.org/10.7314/APJCP.2012.13.7.3015
  30. Sun L, Konig IR, Homann N (2009). Manganese superoxide dismutase (MnSOD) polymorphism, alcohol, cigarette smoking and risk of oesophageal cancer. Alcohol Alcohol, 44, 353-7. https://doi.org/10.1093/alcalc/agp025
  31. Sutton A, Khoury H, Prip-Buus C, et al (2003). The Ala16Val genetic dimorphism modulates the import of human manganese superoxide dismutase into rat liver mitochondria. Pharmacogenetics, 13, 145-57. https://doi.org/10.1097/00008571-200303000-00004
  32. Swerissen H, Belfrage J, Weeks A, et al (2006). A randomised control trial of a self-management program for people with a chronic illness from Vientnamese, Chinese, Italian and Greek backgrounds. Patient Educ Couns, 64, 360-8. https://doi.org/10.1016/j.pec.2006.04.003
  33. Taufer M, Peres A, de Andrade VM, et al (2005). Is the Val16Ala manganese superoxide dismutase polymorphism associated with the aging process? J Gerontol A Biol Sci Med Sci, 60, 432-438. https://doi.org/10.1093/gerona/60.4.432
  34. Tong SY, Lee JM, Song ES, et al (2009). Functional polymorphism in manganese superoxide dismutase and antioxidant status, their interactions on the risk of cervical intraepithelial neoplasia and cervical cancer. Gynecol Oncol, 115, 272-6. https://doi.org/10.1016/j.ygyno.2009.07.032
  35. Trachootham D, Lu W, Ogasawara MA, Nilsa RD, Huang P (2009). Redox regulation of cell Survival. Antioxid Redox Signal, 10, 1343-74.
  36. Wang LI, Miller DP, Sai Y, et al (2001). Manganese superoxide dismutase alanine-to-valine polymorphism at codon 16 and lung cancer risk. J Natl Cancer Inst, 93, 1818-21. https://doi.org/10.1093/jnci/93.23.1818
  37. Wang LI, Neuberg D, Christiani DC (2004). Asbestos exposure, manganese superoxide dismutase (MnSOD) genotype, and lung cancer risk. J Occup Environ Med, 46, 556-64. https://doi.org/10.1097/01.jom.0000128155.86648.a4
  38. Wang MC, Guo MF, Zhao GQ (2006). Research on mRNA expression level of MnSOD gene in prostate cancer and benign prostatic hyperplasia tissue. Chin J Gerontol, 26, 164-5.
  39. Wang S, Wang F, Shi X, et al (2009). Association between manganese superoxide dismutase (MnSOD) Val-9Ala polymorphism and cancer risk-A meta-analysis. Eur J Cancer, 45, 2874-81. https://doi.org/10.1016/j.ejca.2009.04.024
  40. Wang Y, Kuroda M, Gao XS, et al (2005). Hydrogen peroxide overload increases adriamycin-induced apoptosis of SaOS2FM, a manganese superoxide dismutaseoverexpressing human osteosarcoma cell line. Int J Oncol, 26, 1291-300.
  41. Woodson K, Tangrea JA, Lehman TA, et al (2001). Manganese superoxide dismutase (MnSOD) polymorphism, alphatocopherol supplementation and prostate cancer risk in the alpha-tocopherol, beta-carotene cancer prevention study (Finland). Cancer Causes Control, 14, 513-8.
  42. Yan T, Oberley LW, Zhong W, St Clair DK (1996). Manganesecontaining superoxide dismutase overexpression causes phenotypic reversion in SV-40 transformed human lung fibroblasts. Cancer Res, 56, 2864-71.
  43. Zejnilovic J, Akev N, Yilmaz H, Isbir T (2009). Association between manganese superoxide dismutase polymorphism and risk of lung cancer. Cancer Genet Cytogenet, 189, 1-4 https://doi.org/10.1016/j.cancergencyto.2008.06.017
  44. Zhang HJ, Yan T, Oberley TD, Oberley LW (1999). Comparison of effects of two polymorphic variants of manganese superoxide dismutase on human breast MCF-7 cancer cell phenotype. Cancer Res, 59, 6276-83,.
  45. Zhao Y, Xuo Y, Oberley LW (2001). Overexpression of manganese superoxide dismutase suppresses tumor formation by modulation of activator protein-1 signaling in a multistage skin carcinogenesis mode. Cancer Res, 61, 6082-8.
  46. Zhong W, Oberley LW, Oberley TD, St Clair DK (1997). Suppression of the malignant phenotype of human glioma cells by overexpression of manganese superoxide dismutase. Oncogene, 14, 481-90. https://doi.org/10.1038/sj.onc.1200852
  47. Zhong W, Oberley LW(2005). Suppression of malignant phenotype of human glioma cells by overexpression of Manganese superoxide dismutase. Oncogene, 14, 481-90.
  48. Zwacka RM, Duds L, Epperly MW, et al (1993). Increased manganese superoxide dismutase expression suppresses the malignant phenotype of human melanoma cells. Proc Nate Acad Sci USA, 90, 3113-7. https://doi.org/10.1073/pnas.90.7.3113

Cited by

  1. Interactions between Filamin A and MMP-9 Regulate Proliferation and Invasion in Renal Cell Carcinoma vol.15, pp.8, 2014, https://doi.org/10.7314/APJCP.2014.15.8.3789
  2. The P275A Polymorphism in the Macrophage Scavenger Receptor 1 Gene and Prostate Cancer Risk: a Meta-Analysis vol.16, pp.13, 2015, https://doi.org/10.7314/APJCP.2015.16.13.5407
  3. Manganese Superoxide Dismutase (MnSOD Val-9Ala) Gene Polymorphism and Susceptibility to Gastric Cancer vol.16, pp.2, 2015, https://doi.org/10.7314/APJCP.2015.16.2.485
  4. The effect of superoxide anion and hydrogen peroxide imbalance on prostate cancer: an integrative in vivo and in vitro analysis vol.32, pp.11, 2015, https://doi.org/10.1007/s12032-015-0700-1
  5. Association between Manganese Superoxide Dismutase (MnSOD) Polymorphism and Prostate Cancer Susceptibility: A Meta-Analysis vol.31, pp.4, 2016, https://doi.org/10.5301/jbm.5000188
  6. Antioxidant defence-related genetic variants are not associated with higher risk of secondary thyroid cancer after treatment of malignancy in childhood or adolescence vol.50, pp.1, 2016, https://doi.org/10.1515/raon-2015-0026
  7. Val16Ala Polymorphism and Cancer Risk: Evidence from 33,098 Cases and 37,831 Controls vol.2018, pp.1875-8630, 2018, https://doi.org/10.1155/2018/3061974
  8. Meta-analysis of the relationship between MnSOD polymorphism and cancer in the Turkish and Cypriot population vol.43, pp.2, 2018, https://doi.org/10.1515/tjb-2017-0161
  9. Cumulative evidence for association between genetic polymorphisms and esophageal cancer susceptibility: A review with evidence from meta-analysis and genome-wide association studies pp.20457634, 2019, https://doi.org/10.1002/cam4.1972