Genetic variation in the Nrf2 promoter associates with defective spermatogenesis in humans

Journal of Molecular Medicine

Volumn 90, Issue 11, 2012, Pages 1333-1342

  Yu, Bolan ^a   Lin, Huanlan ^b   Yang, Lixia ^b   Chen, Kang ^a   Luo, Haihua ^b   Liu, Jianqiao ^a   Gao, Xingcheng ^a   Xia, Xuefeng ^a   Huang, Zhaofeng ^b,c  

^a GUANGZHOU MEDICAL UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c SUN YAT SEN UNIVERSITY   (China)

Author keywords

Male infertility; Nrf2; Oligoasthenozoospermia; SOD; Spermatogenesis

Indexed keywords

GLUTATHIONE TRANSFERASE M1; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; TRANSCRIPTION FACTOR NRF2;

ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; ASTHENOSPERMIA; CONTROLLED STUDY; ENZYME ACTIVITY; GENE FREQUENCY; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HUMAN; MAJOR CLINICAL STUDY; MALE; MALE INFERTILITY; OLIGOASTHENOZOOSPERMIA; PROMOTER REGION; SEMINAL PLASMA; SINGLE NUCLEOTIDE POLYMORPHISM; SMOKING; SPERMATOGENESIS;

ADULT; ASTHENOZOOSPERMIA; GENES, REPORTER; GENETIC VARIATION; GENOTYPE; GLUTATHIONE TRANSFERASE; HAPLOTYPES; HUMANS; INFERTILITY, MALE; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; NF-E2-RELATED FACTOR 2; POLYMORPHISM, SINGLE NUCLEOTIDE; REACTIVE OXYGEN SPECIES; RISK; SMOKING; SPERMATOGENESIS; SUPEROXIDE DISMUTASE;

EID: 84868103295     PISSN: 09462716     EISSN: 14321440     Source Type: Journal    
DOI: 10.1007/s00109-012-0914-z     Document Type: Article

References (35)

1. de Kretser DM (1997) Male infertility. Lancet 349:787-790
2. Bashamboo A, Ferraz-de-Souza B, Lourenco D, Lin L, Sebire NJ, Montjean D, Bignon-Topalovic J, Mandelbaum J, Siffroi JP, Christin-Maitre S et al (2010) Human male infertility associated with mutations in NR5A1 encoding steroidogenic factor 1. Am J Hum Genet 87:505-512
3. Carlsen E, Giwercman A, Keiding N, Skakkebaek NE (1992) Evidence for decreasing quality of semen during past 50 years. BMJ 305:609-613
4. Auger J, Kunstmann JM, Czyglik F, Jouannet P (1995) Decline in semen quality among fertile men in Paris during the past 20 years. N Engl J Med 332:281-285
5. Ochsendorf FR (1999) Infections in the male genital tract and reactive oxygen species. Hum Reprod Update 5:399-420
6. Fridovich I (1978) The biology of oxygen radicals. Science 201:875-880
7. Zalata AA, Christophe AB, Depuydt CE, Schoonjans F, Comhaire FH (1998) The fatty acid composition of phospholipids of spermatozoa from infertile patients. Mol Hum Reprod 4:111-118
8. Storey BT (1997) Biochemistry of the induction and prevention of lipoperoxidative damage in human spermatozoa. Mol Hum Reprod 3:203-213
9. Jones R, Mann T, Sherins R (1979) Peroxidative breakdown of phospholipids in human spermatozoa, spermicidal properties of fatty acid peroxides, and protective action of seminal plasma. Fertil Steril 31:531-537
10. Kensler TW, Wakabayashi N, Biswal S (2007) Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47:89-116
11. Holland R, Fishbein JC (2010) Chemistry of the cysteine sensors in Kelch-like ECH-associated protein 1. Antioxid Redox Signal 13:1749-1761
12. Zhang DD, Hannink M (2003) Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol Cell Biol 23:8137-8151
13. Chan K, Kan YW (1999) Nrf2 is essential for protection against acute pulmonary injury in mice. Proc Natl Acad Sci U S A 96:12731-12736
14. McMahon M, Itoh K, Yamamoto M, Chanas SA, Henderson CJ, McLellan LI, Wolf CR, Cavin C, Hayes JD (2001) The Cap'n'Collar basic leucine zipper transcription factor Nrf2 (NF-E2 p45-related factor 2) controls both constitutive and inducible expression of intestinal detoxification and glutathione biosynthetic enzymes. Cancer Res 61:3299-3307
15. Blake DJ, Singh A, Kombairaju P, Malhotra D, Mariani TJ, Tuder RM, Gabrielson E, Biswal S (2009) Deletion of Keap1 in the lung attenuates acute cigarette smoke-induced oxidative stress and inflammation. Am J Respir Cell Mol Biol 42:524-536
16. Zhao Z, Chen Y, Wang J, Sternberg P, Freeman ML, Grossniklaus HE, Cai J (2011) Age-related retinopathy in NRF2-deficient mice. PLoS One 6:e19456
17. Wang B, Cao W, Biswal S, Dore S (2011) Carbon monoxide-activated nrf2 pathway leads to protection against permanent focal cerebral ischemia. Stroke 42:2605-2610
18. Arisawa T, Tahara T, Shibata T, Nagasaka M, Nakamura M, Kamiya Y, Fujita H, Yoshioka D, Okubo M, Sakata M et al (2008) Nrf2 gene promoter polymorphism is associated with ulcerative colitis in a Japanese population. Hepatogastroenterology 55:394-397
19. Guan CP, Zhou MN, Xu AE, Kang KF, Liu JF, Wei XD, Li YW, Zhao DK, Hong WS (2008) The susceptibility to vitiligo is associated with NF-E2-related factor2 (Nrf2) gene polymorphisms: a study on Chinese Han population. Exp Dermatol 17:1059-1062
20. Hong CC, Ambrosone CB, Ahn J, Choi JY, McCullough ML, Stevens VL, Rodriguez C, Thun MJ, Calle EE (2007) Genetic variability in iron-related oxidative stress pathways (Nrf2, NQ01, NOS3, and HO-1), iron intake, and risk of postmenopausal breast cancer. Cancer Epidemiol Biomarkers Prev 16:1784-1794
21. Marzec JM, Christie JD, Reddy SP, Jedlicka AE, Vuong H, Lanken PN, Aplenc R, Yamamoto T, Yamamoto M, Cho HY et al (2007) Functional polymorphisms in the transcription factor NRF2 in humans increase the risk of acute lung injury. FASEB J 21:2237-2246
22. Nakamura BN, Lawson G, Chan JY, Banuelos J, Cortes MM, Hoang YD, Ortiz L, Rau BA, Luderer U (2010) Knockout of the transcription factor NRF2 disrupts spermatogenesis in an age-dependent manner. Free Radic Biol Med 49:1368-1379
23. World Health Organization (1999) Laboratory manual for the examination of human semen and sperm-cervical mucus interaction, 4th edn. Cambridge University Press, New York
24. Garbin U, Fratta Pasini A, Stranieri C, Cominacini M, Pasini A, Manfro S, Lugoboni F, Mozzini C, Guidi G, Faccini G et al (2009) Cigarette smoking blocks the protective expression of Nrf2/ARE pathway in peripheral mononuclear cells of young heavy smokers favouring inflammation. PLoS One 4:e8225
25. Corrales RM, Galarreta D, Herreras J, Calonge M, Chaves F Antioxidant enzyme mRNA expression in conjunctival epithelium of healthy human subjects. Can J Ophthalmol 46: 35-39
26. Wan J, Diaz-Sanchez D (2006) Phase II enzymes induction blocks the enhanced IgE production in B cells by diesel exhaust particles. J Immunol 177:3477-3483
27. Ji G, Gu A, Wang Y, Huang C, Hu F, Zhou Y, Song L, Wang X (2012) Genetic variants in antioxidant genes are associated with sperm DNA damage and risk of male infertility in a Chinese population. Free Radic Biol Med 52: 775-780
28. Aitken RJ, Buckingham DW, Carreras A, Irvine DS (1996) Superoxide dismutase in human sperm suspensions: relationship with cellular composition, oxidative stress, and sperm function. Free Radic Biol Med 21:495-504
29. Siciliano L, Tarantino P, Longobardi F, Rago V, De Stefano C, Carpino A (2001) Impaired seminal antioxidant capacity in human semen with hyperviscosity or oligoasthenozoospermia. J Androl 22:798-803
30. Yamamoto T, Yoh K, Kobayashi A, Ishii Y, Kure S, Koyama A, Sakamoto T, Sekizawa K, Motohashi H, Yamamoto M (2004) Identification of polymorphisms in the promoter region of the human NRF2 gene. Biochem Biophys Res Commun 321:72-79
31. Ramos-Gomez M, Kwak MK, Dolan PM, Itoh K, Yamamoto M, Talalay P, Kensler TW (2001) Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc Natl Acad Sci U S A 98:3410-3415
32. Peeker R, Abramsson L, Marklund SL (1997) Superoxide dismutase isoenzymes in human seminal plasma and spermatozoa. Mol Hum Reprod 3:1061-1066
33. Kawakami E, Takemura A, Sakuma M, Takano M, Hirano T, Hori T, Tsutsui T (2007) Superoxide dismutase and catalase activities in the seminal plasma of normozoospermic and asthenozoospermic Beagles. J Vet Med Sci 69:133-136
34. Kobayashi T, Miyazaki T, Natori M, Nozawa S (1991) Protective role of superoxide dismutase in human sperm motility: superoxide dismutase activity and lipid peroxide in human seminal plasma and spermatozoa. Hum Reprod 6:987-991
35. Kidd SA, Eskenazi B, Wyrobek AJ (2001) Effects of male age on semen quality and fertility: a review of the literature. Fertil Steril 75:237-248