Advertisement

Association of SOD2 A16V and PON2 S311C polymorphisms with polycystic ovary syndrome in Chinese women

  • Q. Liu
  • H. Liu
  • H. Bai
  • W. Huang
  • R. Zhang
  • J. Tan
  • L. Guan
  • P. Fan
Original Article

Abstract

Purpose

To investigate the relationship between superoxide dismutase 2 (SOD2) A16V and paraoxonase 2 (PON2) S311C gene variants and the risk of polycystic ovary syndrome (PCOS) and evaluate the effects of the genotypes on clinical, hormonal, metabolic and oxidative stress indexes in Chinese women.

Methods

This is a cross-sectional study of 932 patients with PCOS and 745 control women. For the clinical and metabolic association study of genotypes, 631 patients and 492 controls were included after excluding the subjects with interferential factors. Genotypes were determined by polymerase chain reaction (PCR) and restriction fragment length polymorphism analysis. Serum total oxidant status, total antioxidant capacity (T-AOC), oxidative stress index and malondialdehyde (MDA) levels, and clinical and metabolic parameters were also analyzed.

Results

The prevalence of the A allele of SOD2 A16V polymorphism was significantly greater in patients with PCOS than in control subjects. Genotype (AA + AV) remained a significant predictor for PCOS in prognostic models including age, body mass index, insulin resistance index, high-density lipoprotein (HDL), low-density lipoprotein (LDL), and triglycerides (TGs) as covariates. Patients carrying the A allele had significantly higher serum luteinizing hormone (LH) levels, and the ratio of LH to follicle-stimulating hormone compared with patients with the VV genotype. We also showed that patients carrying the C allele of the PON2 S311C polymorphism had lower T-AOC compared with patients carrying the SS genotype. However, no significant differences were observed in the frequencies of the S311C genotypes and alleles of the PON2 gene between PCOS and control groups.

Conclusion

The SOD2 A16V, but not PON2 S311C, polymorphism may be one of the genetic determinants for PCOS in Chinese women.

Keywords

Superoxide dismutase 2 Paraoxonase 2 Gene polymorphism Oxidative stress Polycystic ovary syndrome 

Notes

Acknowledgements

We thank women with or without PCOS who donated blood samples for this study. We are thankful to You Li, De Hua Wan, Qi Song, Feng Zhang, Ying Wang, Jinxia Zhang, and Yujin Zhang for work performed to support this study.

Funding

This work was funded by the Chinese National Natural Science Foundation (81370681) and the Program for Changjiang Scholars and Innovative Research Team in University, Ministry of Education (IRT0935).

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Ethical approval

All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki Declaration and its later amendments.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. 1.
    Pasquali R, Gambineri A (2018) New perspectives on the definition and management of polycystic ovary syndrome. J Endocrinol Invest 41(10):1123–1135.  https://doi.org/10.1007/s40618-018-0832-1 CrossRefPubMedGoogle Scholar
  2. 2.
    Azziz R (2016) Introduction: determinants of polycystic ovary syndrome. Fertil Steril 106(1):4–5.  https://doi.org/10.1016/j.fertnstert.2016.05.009 CrossRefPubMedGoogle Scholar
  3. 3.
    The Amsterdam ESHRE/ASRM-Sponsored 3rd PCOS Consensus Workshop Group (2012) Consensus on women’s health aspects of polycystic ovary syndrome (PCOS). Hum Reprod 27(1):14–24.  https://doi.org/10.1093/humrep/der396 CrossRefGoogle Scholar
  4. 4.
    Pappalardo MA, Vita R, Di Bari F, Le Donne M, Trimarchi F, Benvenga S (2017) Gly972Arg of IRS-1 and Lys121Gln of PC-1 polymorphisms act in opposite way in polycystic ovary syndrome. J Endocrinol Invest 40(4):367–376.  https://doi.org/10.1007/s40618-016-0569-7 CrossRefPubMedGoogle Scholar
  5. 5.
    Dona S, Bacchi E, Moghetti P (2017) Is cardiorespiratory fitness impaired in PCOS women? A review of the literature. J Endocrinol Invest 40(5):463–469.  https://doi.org/10.1007/s40618-016-0599-1 CrossRefPubMedGoogle Scholar
  6. 6.
    Behboudi-Gandevani S, Ramezani Tehrani F, Bidhendi Yarandi R, Noroozzadeh M, Hedayati M, Azizi F (2017) The association between polycystic ovary syndrome, obesity, and the serum concentration of adipokines. J Endocrinol Invest 40(8):859–866.  https://doi.org/10.1007/s40618-017-0650-x CrossRefPubMedGoogle Scholar
  7. 7.
    Murri M, Luque-Ramirez M, Insenser M, Ojeda-Ojeda M, Escobar-Morreale HF (2013) Circulating markers of oxidative stress and polycystic ovary syndrome (PCOS): a systematic review and meta-analysis. Hum Reprod Update 19(3):268–288.  https://doi.org/10.1093/humupd/dms059 CrossRefPubMedGoogle Scholar
  8. 8.
    Repaci A, Gambineri A, Pasquali R (2011) The role of low-grade inflammation in the polycystic ovary syndrome. Mol Cell Endocrinol 335(1):30–41.  https://doi.org/10.1016/j.mce.2010.08.002 CrossRefPubMedGoogle Scholar
  9. 9.
    de Groot PC, Dekkers OM, Romijn JA, Dieben SW, Helmerhorst FM (2011) PCOS, coronary heart disease, stroke and the influence of obesity: a systematic review and meta-analysis. Hum Reprod Update 17(4):495–500.  https://doi.org/10.1093/humupd/dmr001 CrossRefPubMedGoogle Scholar
  10. 10.
    Mykhalchenko K, Lizneva D, Trofimova T, Walker W, Suturina L, Diamond MP, Azziz R (2017) Genetics of polycystic ovary syndrome. Expert Rev Mol Diagn 17(7):723–733.  https://doi.org/10.1080/14737159.2017.1340833 CrossRefPubMedGoogle Scholar
  11. 11.
    Filippou P, Homburg R (2017) Is foetal hyperexposure to androgens a cause of PCOS? Hum Reprod Update 23(4):421–432.  https://doi.org/10.1093/humupd/dmx013 CrossRefPubMedGoogle Scholar
  12. 12.
    Rosenfield RL, Ehrmann DA (2016) The pathogenesis of polycystic ovary syndrome (PCOS): the hypothesis of PCOS as functional ovarian hyperandrogenism revisited. Endocr Rev 37(5):467–520.  https://doi.org/10.1210/er.2015-1104 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Merkin SS, Phy JL, Sites CK, Yang D (2016) Environmental determinants of polycystic ovary syndrome. Fertil Steril 106(1):16–24.  https://doi.org/10.1016/j.fertnstert.2016.05.011 CrossRefPubMedGoogle Scholar
  14. 14.
    Fukai T, Ushio-Fukai M (2011) Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid Redox Signal 15(6):1583–1606.  https://doi.org/10.1089/ars.2011.3999 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Furlong CE, Marsillach J, Jarvik GP, Costa LG (2016) Paraoxonases-1, -2 and -3: what are their functions? Chem Biol Interact 259(Pt B):51–62.  https://doi.org/10.1016/j.cbi.2016.05.036 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Precourt LP, Amre D, Denis MC, Lavoie JC, Delvin E, Seidman E, Levy E (2011) The three-gene paraoxonase family: physiologic roles, actions and regulation. Atherosclerosis 214(1):20–36.  https://doi.org/10.1016/j.atherosclerosis.2010.08.076 CrossRefPubMedGoogle Scholar
  17. 17.
    Draganov DI, Teiber JF, Speelman A, Osawa Y, Sunahara R, La Du BN (2005) Human paraoxonases (PON1, PON2, and PON3) are lactonases with overlapping and distinct substrate specificities. J Lipid Res 46(6):1239–1247.  https://doi.org/10.1194/jlr.M400511-JLR200 CrossRefPubMedGoogle Scholar
  18. 18.
    Bresciani G, Cruz IB, de Paz JA, Cuevas MJ, Gonzalez-Gallego J (2013) The MnSOD Ala16Val SNP: relevance to human diseases and interaction with environmental factors. Free Radic Res 47(10):781–792.  https://doi.org/10.3109/10715762.2013.836275 CrossRefPubMedGoogle Scholar
  19. 19.
    Sutton A, Khoury H, Prip-Buus C, Cepanec C, Pessayre D, Degoul F (2003) The Ala16Val genetic dimorphism modulates the import of human manganese superoxide dismutase into rat liver mitochondria. Pharmacogenetics 13(3):145–157.  https://doi.org/10.1097/01.fpc.0000054067.64000.8f CrossRefPubMedGoogle Scholar
  20. 20.
    Shimoda-Matsubayashi S, Matsumine H, Kobayashi T, Nakagawa-Hattori Y, Shimizu Y, Mizuno Y (1996) Structural dimorphism in the mitochondrial targeting sequence in the human manganese superoxide dismutase gene. A predictive evidence for conformational change to influence mitochondrial transport and a study of allelic association in Parkinson’s disease. Biochem Biophys Res Commun 226(2):561–565.  https://doi.org/10.1006/bbrc.1996.1394 CrossRefPubMedGoogle Scholar
  21. 21.
    Tian C, Fang S, Du X, Jia C (2011) Association of the C47T polymorphism in SOD2 with diabetes mellitus and diabetic microvascular complications: a meta-analysis. Diabetologia 54(4):803–811.  https://doi.org/10.1007/s00125-010-2004-5 CrossRefPubMedGoogle Scholar
  22. 22.
    Montano MA, Barrio Lera JP, Gottlieb MG, Schwanke CH, da Rocha MI, Manica-Cattani MF, dos Santos GF, da Cruz IB (2009) Association between manganese superoxide dismutase (MnSOD) gene polymorphism and elderly obesity. Mol Cell Biochem 328(1–2):33–40.  https://doi.org/10.1007/s11010-009-0071-z CrossRefPubMedGoogle Scholar
  23. 23.
    Bica CG, de Moura da Silva LL, Toscani NV, da Cruz IB, Sa G, Graudenz MS, Zettler CG (2009) MnSOD gene polymorphism association with steroid-dependent cancer. Pathol Oncol Res 15(1):19–24.  https://doi.org/10.1007/s12253-008-9064-6 CrossRefPubMedGoogle Scholar
  24. 24.
    Xu M, Xu M, Han L, Yuan C, Mei Y, Zhang H, Chen S, Sun K, Zhu B (2017) Role for functional SOD2 polymorphism in pulmonary arterial hypertension in a Chinese population. Int J Environ Res Public Health.  https://doi.org/10.3390/ijerph14030266 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Abello D, Sancho E, Camps J, Joven J (2014) Exploring the role of paraoxonases in the pathogenesis of coronary artery disease: a systematic review. Int J Mol Sci 15(11):20997–21010.  https://doi.org/10.3390/ijms151120997 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Stoltz DA, Ozer EA, Recker TJ, Estin M, Yang X, Shih DM, Lusis AJ, Zabner J (2009) A common mutation in paraoxonase-2 results in impaired lactonase activity. J Biol Chem 284(51):35564–35571.  https://doi.org/10.1074/jbc.M109.051706 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Zhang R, Liu H, Bai H, Zhang Y, Liu Q, Guan L, Fan P (2017) Oxidative stress status in Chinese women with different clinical phenotypes of polycystic ovary syndrome. Clin Endocrinol (Oxf) 86(1):88–96.  https://doi.org/10.1111/cen.13171 CrossRefGoogle Scholar
  28. 28.
    Zhang J, Zhang Y, Liu H, Bai H, Wang Y, Jiang C, Fan P (2015) Antioxidant properties of high-density lipoproteins are impaired in women with polycystic ovary syndrome. Fertil Steril 103(5):1346–1354.  https://doi.org/10.1016/j.fertnstert.2015.02.024 CrossRefPubMedGoogle Scholar
  29. 29.
    Liao D, Yu H, Han L, Zhong C, Ran X, Wang D, Mo L (2018) Association of PON1 gene polymorphisms with polycystic ovarian syndrome risk: a meta-analysis of case-control studies. J Endocrinol Invest 41(11):1289–1300.  https://doi.org/10.1007/s40618-018-0866-4 CrossRefPubMedGoogle Scholar
  30. 30.
    Wang Y, Liu H, Fan P, Bai H, Zhang J, Zhang F (2012) Evidence for association between paraoxonase 1 gene polymorphisms and polycystic ovarian syndrome in southwest Chinese women. Eur J Endocrinol 166(5):877–885.  https://doi.org/10.1530/EJE-11-0986 CrossRefPubMedGoogle Scholar
  31. 31.
    Fan P, Liu HW, Wang XS, Zhang F, Song Q, Li Q, Wu HM, Bai H (2010) Identification of the G994T polymorphism in exon 9 of plasma platelet-activating factor acetylhydrolase gene as a risk factor for polycystic ovary syndrome. Hum Reprod 25(5):1288–1294.  https://doi.org/10.1093/humrep/deq047 CrossRefPubMedGoogle Scholar
  32. 32.
    The Rotterdam ESHRE/ASRM-Sponsored PCOS Consensus Workshop Group (2004) Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome. Fertil Steril 81(1):19–25CrossRefGoogle Scholar
  33. 33.
    Teede HJ, Misso ML, Costello MF, Dokras A, Laven J, Moran L, Piltonen T, Norman RJ, International PN (2018) Recommendations from the international evidence-based guideline for the assessment and management of polycystic ovary syndrome. Hum Reprod 33(9):1602–1618.  https://doi.org/10.1093/humrep/dey256 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Zhang Y, Liu H, He J, Xu K, Bai H, Wang Y, Zhang F, Zhang J, Cheng L, Fan P (2015) Lactonase activity and status of paraoxonase 1 in Chinese women with polycystic ovarian syndrome. Eur J Endocrinol 172(4):391–402.  https://doi.org/10.1530/EJE-14-0863 CrossRefPubMedGoogle Scholar
  35. 35.
    Zhang J, Fan P, Liu H, Bai H, Wang Y, Zhang F (2012) Apolipoprotein A-I and B levels, dyslipidemia and metabolic syndrome in south-west Chinese women with PCOS. Hum Reprod 27(8):2484–2493.  https://doi.org/10.1093/humrep/des191 CrossRefPubMedGoogle Scholar
  36. 36.
    Legro RS, Arslanian SA, Ehrmann DA, Hoeger KM, Murad MH, Pasquali R, Welt CK, Endocrine S (2013) Diagnosis and treatment of polycystic ovary syndrome: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 98(12):4565–4592.  https://doi.org/10.1210/jc.2013-2350 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Zhang R, Song Q, Liu H, Bai H, Zhang Y, Liu Q, Guan L, Fan P (2017) Effect of the R92H and A379V genotypes of platelet-activating factor acetylhydrolase on its enzyme activity, oxidative stress and metabolic profile in Chinese women with polycystic ovary syndrome. Lipids Health Dis 16(1):57.  https://doi.org/10.1186/s12944-017-0448-z CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Mitrunen K, Sillanpaa P, Kataja V, Eskelinen M, Kosma VM, Benhamou S, Uusitupa M, Hirvonen A (2001) Association between manganese superoxide dismutase (MnSOD) gene polymorphism and breast cancer risk. Carcinogenesis 22(5):827–829CrossRefGoogle Scholar
  39. 39.
    Dasgupta S, Demirci FY, Dressen AS, Kao AH, Rhew EY, Ramsey-Goldman R, Manzi S, Kammerer CM, Kamboh MI (2011) Association analysis of PON2 genetic variants with serum paraoxonase activity and systemic lupus erythematosus. BMC Med Genet 12:7.  https://doi.org/10.1186/1471-2350-12-7 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Zhang R, Liu Q, Liu H, Bai H, Zhang Y, Guan L, Fan P (2018) Effects of apoC1 genotypes on the hormonal levels, metabolic profile and PAF-AH activity in Chinese women with polycystic ovary syndrome. Lipids Health Dis 17(1):77.  https://doi.org/10.1186/s12944-018-0725-5 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Lujan ME, Bloski TG, Chizen DR, Lehotay DC, Pierson RA (2010) Digit ratios do not serve as anatomical evidence of prenatal androgen exposure in clinical phenotypes of polycystic ovary syndrome. Hum Reprod 25(1):204–211.  https://doi.org/10.1093/humrep/dep363 CrossRefPubMedGoogle Scholar
  42. 42.
    Ambrosone CB, Freudenheim JL, Thompson PA, Bowman E, Vena JE, Marshall JR, Graham S, Laughlin R, Nemoto T, Shields PG (1999) Manganese superoxide dismutase (MnSOD) genetic polymorphisms, dietary antioxidants, and risk of breast cancer. Cancer Res 59(3):602–606PubMedGoogle Scholar
  43. 43.
    Vats P, Sagar N, Singh TP, Banerjee M (2015) Association of Superoxide dismutases (SOD1 and SOD2) and Glutathione peroxidase 1 (GPx1) gene polymorphisms with type 2 diabetes mellitus. Free Radic Res 49(1):17–24.  https://doi.org/10.3109/10715762.2014.971782 CrossRefPubMedGoogle Scholar
  44. 44.
    Kangas-Kontio T, Vavuli S, Kakko SJ, Penna J, Savolainen ER, Savolainen MJ, Liinamaa MJ (2009) Polymorphism of the manganese superoxide dismutase gene but not of vascular endothelial growth factor gene is a risk factor for diabetic retinopathy. Br J Ophthalmol 93(10):1401–1406.  https://doi.org/10.1136/bjo.2009.159012 CrossRefPubMedGoogle Scholar
  45. 45.
    Nomiyama T, Tanaka Y, Piao L, Nagasaka K, Sakai K, Ogihara T, Nakajima K, Watada H, Kawamori R (2003) The polymorphism of manganese superoxide dismutase is associated with diabetic nephropathy in Japanese type 2 diabetic patients. J Hum Genet 48(3):138–141.  https://doi.org/10.1007/s100380300021 CrossRefPubMedGoogle Scholar
  46. 46.
    Lee SJ, Choi MG (2006) Association of manganese superoxide dismutase gene polymorphism (V16A) with diabetic macular edema in Korean type 2 diabetic patients. Metabolism 55(12):1681–1688.  https://doi.org/10.1016/j.metabol.2006.08.011 CrossRefPubMedGoogle Scholar
  47. 47.
    Ascencio-Montiel Ide J, Parra EJ, Valladares-Salgado A, Gomez-Zamudio JH, Kumate-Rodriguez J, Escobedo-de-la-Pena J, Cruz M (2013) SOD2 gene Val16Ala polymorphism is associated with macroalbuminuria in Mexican type 2 diabetes patients: a comparative study and meta-analysis. BMC Med Genet 14:110.  https://doi.org/10.1186/1471-2350-14-110 CrossRefPubMedGoogle Scholar
  48. 48.
    Valdivia A, Perez-Alvarez S, Aroca-Aguilar JD, Ikuta I, Jordan J (2009) Superoxide dismutases: a physiopharmacological update. J Physiol Biochem 65(2):195–208CrossRefGoogle Scholar
  49. 49.
    Pesta D, Roden M (2017) The Janus head of oxidative stress in metabolic diseases and during physical exercise. Curr Diab Rep 17(6):41.  https://doi.org/10.1007/s11892-017-0867-2 CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Janus A, Szahidewicz-Krupska E, Mazur G, Doroszko A (2016) Insulin resistance and endothelial dysfunction constitute a common therapeutic target in cardiometabolic disorders. Mediat Inflamm 2016:3634948.  https://doi.org/10.1155/2016/3634948 CrossRefGoogle Scholar
  51. 51.
    Ding Y, Xia BH, Zhang CJ, Zhuo GC (2017) Mutations in mitochondrial tRNA genes may be related to insulin resistance in women with polycystic ovary syndrome. Am J Transl Res 9(6):2984–2996PubMedPubMedCentralGoogle Scholar
  52. 52.
    Banuls C, Rovira-Llopis S, Martinez de Maranon A, Veses S, Jover A, Gomez M, Rocha M, Hernandez-Mijares A, Victor VM (2017) Metabolic syndrome enhances endoplasmic reticulum, oxidative stress and leukocyte-endothelium interactions in PCOS. Metabolism 71:153–162.  https://doi.org/10.1016/j.metabol.2017.02.012 CrossRefPubMedGoogle Scholar
  53. 53.
    Chen CC, Chen CC, Tu JD, Wu YL, Leu SJ (2013) Associations between genetic polymorphisms of paraoxonase genes and coronary artery disease in a Taiwanese population. Clin Biochem 46(16–17):1664–1667.  https://doi.org/10.1016/j.clinbiochem.2013.05.066 CrossRefPubMedGoogle Scholar
  54. 54.
    Chen Q, Reis SE, Kammerer CM, McNamara DM, Holubkov R, Sharaf BL, Sopko G, Pauly DF, Merz CN, Kamboh MI, Group WS (2003) Association between the severity of angiographic coronary artery disease and paraoxonase gene polymorphisms in the National Heart, Lung, and Blood Institute-sponsored Women’s Ischemia Syndrome Evaluation (WISE) study. Am J Hum Genet 72(1):13–22.  https://doi.org/10.1086/345312 CrossRefPubMedGoogle Scholar
  55. 55.
    Wang Y, Luk AO, Ma RC, So WY, Tam CH, Ng MC, Yang X, Lam V, Tong PC, Chan JC (2012) Predictive role of multilocus genetic polymorphisms in cardiovascular disease and inflammation-related genes on chronic kidney disease in Type 2 diabetes—an 8-year prospective cohort analysis of 1163 patients. Nephrol Dial Transplant 27(1):190–196.  https://doi.org/10.1093/ndt/gfr343 CrossRefPubMedGoogle Scholar
  56. 56.
    Marchegiani F, Spazzafumo L, Provinciali M, Cardelli M, Olivieri F, Franceschi C, Lattanzio F, Antonicelli R (2009) Paraoxonase2 C311S polymorphism and low levels of HDL contribute to a higher mortality risk after acute myocardial infarction in elderly patients. Mol Genet Metab 98(3):314–318.  https://doi.org/10.1016/j.ymgme.2009.05.008 CrossRefPubMedGoogle Scholar
  57. 57.
    Rodriguez-Esparragon F, Lopez-Fernandez JC, Buset-Rios N, Garcia-Bello MA, Hernandez-Velazquez E, Cappiello L, Rodriguez-Perez JC (2017) Paraoxonase 1 and 2 gene variants and the ischemic stroke risk in Gran Canaria population: an association study and meta-analysis. Int J Neurosci 127(3):191–198.  https://doi.org/10.3109/00207454.2016.1165675 CrossRefPubMedGoogle Scholar
  58. 58.
    Lazaros L, Markoula S, Kyritsis A, Georgiou I (2010) Paraoxonase gene polymorphisms and stroke severity. Eur J Neurol 17(5):757–759.  https://doi.org/10.1111/j.1468-1331.2009.02860.x CrossRefPubMedGoogle Scholar
  59. 59.
    Shi J, Zhang S, Tang M, Liu X, Li T, Han H, Wang Y, Guo Y, Zhao J, Li H, Ma C (2004) Possible association between Cys311Ser polymorphism of paraoxonase 2 gene and late-onset Alzheimer’s disease in Chinese. Brain Res Mol Brain Res 120(2):201–204CrossRefGoogle Scholar
  60. 60.
    Becer E, Cirakoglu A (2015) Association of the Ala16Val MnSOD gene polymorphism with plasma leptin levels and oxidative stress biomarkers in obese patients. Gene 568(1):35–39.  https://doi.org/10.1016/j.gene.2015.05.009 CrossRefPubMedGoogle Scholar
  61. 61.
    Lou-Bonafonte JM, Gabas-Rivera C, Navarro MA, Osada J (2017) The search for dietary supplements to elevate or activate circulating paraoxonases. Int J Mol Sci.  https://doi.org/10.3390/ijms18020416 CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Simo R, Saez-Lopez C, Lecube A, Hernandez C, Fort JM, Selva DM (2014) Adiponectin upregulates SHBG production: molecular mechanisms and potential implications. Endocrinology 155(8):2820–2830.  https://doi.org/10.1210/en.2014-1072 CrossRefPubMedGoogle Scholar
  63. 63.
    Saez-Lopez C, Soriguer F, Hernandez C, Rojo-Martinez G, Rubio-Martin E, Simo R, Selva DM (2014) Oleic acid increases hepatic sex hormone binding globulin production in men. Mol Nutr Food Res 58(4):760–767.  https://doi.org/10.1002/mnfr.201300304 CrossRefPubMedGoogle Scholar
  64. 64.
    Duarte T, da Cruz IB, Barbisan F, Capelleto D, Moresco RN, Duarte MM (2016) The effects of rosuvastatin on lipid-lowering, inflammatory, antioxidant and fibrinolytics blood biomarkers are influenced by Val16Ala superoxide dismutase manganese-dependent gene polymorphism. Pharmacogenom J 16(6):501–506.  https://doi.org/10.1038/tpj.2015.91 CrossRefGoogle Scholar
  65. 65.
    Chen H, Yu M, Li M, Zhao R, Zhu Q, Zhou W, Lu M, Lu Y, Zheng T, Jiang J, Zhao W, Xiang K, Jia W, Liu L (2012) Polymorphic variations in manganese superoxide dismutase (MnSOD), glutathione peroxidase-1 (GPX1), and catalase (CAT) contribute to elevated plasma triglyceride levels in Chinese patients with type 2 diabetes or diabetic cardiovascular disease. Mol Cell Biochem 363(1–2):85–91.  https://doi.org/10.1007/s11010-011-1160-3 CrossRefPubMedGoogle Scholar

Copyright information

© Italian Society of Endocrinology (SIE) 2019

Authors and Affiliations

  1. 1.Laboratory of Genetic Disease and Perinatal Medicine, Key Laboratory of Birth Defects and Related Diseases of Women and Children, Ministry of Education, West China Second University HospitalSichuan UniversityChengduPeople’s Republic of China
  2. 2.Department of Obstetrics and Gynecology, West China Second University HospitalSichuan UniversityChengduPeople’s Republic of China
  3. 3.Laboratory of Genetic Disease and Perinatal Medicine, West China Second University HospitalSichuanUniversityChengduPeople’s Republic of China

Personalised recommendations