Assessment of an association between an aryl hydrocarbon receptor gene (AHR) polymorphism and risk of male infertility

Toxicological Sciences

Volumn 122, Issue 2, 2011, Pages 415-421

  Gu, Aihua ^a,b   Ji, Guixiang ^a,b   Long, Yan ^a,b   Zhou, Yong ^c   Shi, Xiangguo ^a,b   Song, Ling ^a,b   Wang, Xinru ^a,b  

^a NANJING MEDICAL UNIVERSITY   (China)

^b Nanjing Medical University   (China)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

AHR; DNA adduct; DNA fragmentation; Male infertility; PAHs; Polymorphisms

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; BENZO[A]PYRENE DERIVATIVE; BENZO[A]PYRENE DIOLEPOXIDE; DIOXIN; POLYCYCLIC AROMATIC HYDROCARBON; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CONTROLLED STUDY; DISEASE PREDISPOSITION; DNA ADDUCT; DNA FRAGMENTATION; FLOW CYTOMETRY; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENOTYPE; HUMAN; IMMUNOFLUORESCENCE; MAJOR CLINICAL STUDY; MALE; MALE INFERTILITY; NICK END LABELING; SINGLE NUCLEOTIDE POLYMORPHISM; SPERM; TOXICITY;

ADULT; BENZOPYRENES; CASE-CONTROL STUDIES; DNA ADDUCTS; DNA FRAGMENTATION; DNA NUCLEOTIDYLEXOTRANSFERASE; FLOW CYTOMETRY; GENE FREQUENCY; GENOTYPE; HUMANS; IN SITU NICK-END LABELING; INFERTILITY, MALE; MALE; POLYCYCLIC HYDROCARBONS, AROMATIC; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, ARYL HYDROCARBON; RISK FACTORS; SEMEN ANALYSIS; SPERMATOZOA; YOUNG ADULT;

EID: 80051683780     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr137     Document Type: Article

References (43)

1. Andersson, A. M., Jorgensen, N., Main, K. M., Toppari, J., Rajpert-De Meyts, E., Leffers, H., Juul, A., Jensen, T. K., and Skakkebaek, N. E. (2008). Adverse trends in male reproductive health: we may have reached a crucial 'tipping point'. Int. J. Androl. 31, 74-80.
2. Arima, A., Kato, H., Ooshima, Y., Tateishi, T., Inoue, A., Muneoka, A., Ihara, T., Kamimura, S., Fukusato, T., and Kubota, S. (2009). In utero and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) induces a reduction in epididymal and ejaculated sperm number in rhesus monkeys. Reprod. Toxicol. 28, 495-502.
3. Baba, T., Shima, Y., Owaki, A., Mimura, J., Oshima, M., Fujii-Kuriyama, Y., and Morohashi, K. I. (2008). Disruption of aryl hydrocarbon receptor (AhR) induces regression of the seminal vesicle in aged male mice. Sex Dev. 2, 1-11.
4. Barrett, J. C., Fry, B., Maller, J., and Daly, M. J. (2005). Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263-265.
5. Billiard, S. M., Timme-Laragy, A. R., Wassenberg, D. M., Cockman, C., and Di Giulio, R. T. (2006). The role of the aryl hydrocarbon receptor pathway in mediating synergistic developmental toxicity of polycyclic aromatic hydrocarbons to zebrafish. Toxicol. Sci. 92, 526-536.
6. Buchanan, D. L., Sato, T., Peterson, R. E., and Cooke, P. S. (2000). Antiestrogenic effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin in mouse uterus: critical role of the aryl hydrocarbon receptor in stromal tissue. Toxicol. Sci. 57, 302-311.
7. Celius, T., and Matthews, J. (2010). Functional analysis of six human aryl hydrocarbon receptor variants in human breast cancer and mouse hepatoma cell lines. Toxicology 277, 59-65.
8. Chen, D., Tian, T., Wang, H., Liu, H., Hu, Z., Wang, Y., Liu, Y., Ma, H., Fan, W., and Miao, R. (2009). Association of human aryl hydrocarbon receptor gene polymorphisms with risk of lung cancer among cigarette smokers in a Chinese population. Pharmacogenet. Genomics 19, 25-34.
9. Eaton, D. L., and Bammler, T. K. (1999). Concise review of the glutathione S-transferases and their significance to toxicology. Toxicol. Sci. 49, 156-164.
10. Fernandez-Salguero, P. M., Hilbert, D. M., Rudikoff, S., Ward, J. M., and Gonzalez, F. J. (1996). Aryl-hydrocarbon receptor-deficient mice are resistant to 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced toxicity. Toxicol. Appl. Pharmacol. 140, 173-179.
11. Foster, W. G., Maharaj-Briceno, S., and Cyr, D. G. (2010). Dioxin-induced changes in epididymal sperm count and spermatogenesis. Environ. Health Perspect. 118, 458-464.
12. Han, X., Zhou, N., Cui, Z., Ma, M., Li, L., Cai, M., Li, Y., Lin, H., Li, Y., Ao, L., et al. (2011). Association between urinary polycyclic aromatic hydrocarbon metabolites and sperm DNA damage: a population study in Chongqing, China. Environ. Health Perspect. 5, 652-657.
13. Hauser, R., and Sokol, R. (2008). Science linking environmental contaminant exposures with fertility and reproductive health impacts in the adult male. Fertil. Steril. 89, e59-e65.
14. Hirose, Y., Chiba, K., Karasugi, T., Nakajima, M., Kawaguchi, Y., Mikami, Y., Furuichi, T., Mio, F., Miyake, A., and Miyamoto, T. (2008). A functional polymorphism in THBS2 that affects alternative splicing and MMP binding is associated with lumbar-disc herniation. Am. J. Hum. Genet. 82, 1122-1129.
15. Inyang, F., Ramesh, A., Kopsombut, P., Niaz, M. S., Hood, D. B., Nyanda, A. M., and Archibong, A. E. (2003). Disruption of testicular steroidogenesis and epididymal function by inhaled benzo(a)pyrene. Reprod. Toxicol. 17, 527-537.
16. Izawa, H., Kohara, M., Watanabe, G., Taya, K., and Sagai, M. (2007). Diesel exhaust particle toxicity on spermatogenesis in the mouse is aryl hydrocarbon receptor dependent. J. Reprod. Dev. 53, 1069-1078.
17. Kee, K., Flores, M., Cedars, M. I., and Reijo Pera, R. A. (2010). Human primordial germ cell formation is diminished by exposure to environmental toxicants acting through the AHR signaling pathway. Toxicol. Sci. 117, 218-224.
18. Khorram, O., Garthwaite, M., Jones, J., and Golos, T. (2004). Expression of aryl hydrocarbon receptor (AHR) and aryl hydrocarbon receptor nuclear translocator (ARNT) mRNA expression in human spermatozoa. Med. Sci. Monit. 10, BR135-BR138.
19. Koyano, S., Saito, Y., Fukushima-Uesaka, H., Ishida, S., Ozawa, S., Kamatani, N., Minami, H., Ohtsu, A., Hamaguchi, T., and Shirao, K. (2005). Functional analysis of six human aryl hydrocarbon receptor variants in a Japanese population. Drug Metab. Dispos. 33, 1254-1260.
20. Lu, C., Zhang, J., Li, Y., Xia, Y., Zhang, F., Wu, B., Wu, W., Ji, G., Gu, A., Wang, S., et al. (2009). The b2/b3 subdeletion shows higher risk of spermatogenic failure and higher frequency of complete AZFc deletion than the gr/gr subdeletion in a Chinese population. Hum. Mol. Genet. 18, 1122-1130.
21. Matsumoto, Y., Ide, F., Kishi, R., Akutagawa, T., Sakai, S., Nakamura, M., Ishikawa, T., Fujii-Kuriyama, Y., and Nakatsuru, Y. (2007). Aryl hydrocarbon receptor plays a significant role in mediating airborne particulate-induced carcinogenesis in mice. Environ. Sci. Technol. 41, 3775-3780.
22. Mocarelli, P., Gerthoux, P. M., Patterson, D. G., Jr., Milani, S., Limonta, G., Bertona, M., Signorini, S., Tramacere, P., Colombo, L., and Crespi, C. (2008). Dioxin exposure, from infancy through puberty, produces endocrine disruption and affects human semen quality. Environ. Health Perspect. 116, 70-77.
23. Muratori, M., Forti, G., and Baldi, E. (2008). Comparing flow cytometry and fluorescence microscopy for analyzing human sperm DNA fragmentation by TUNEL labeling. Cytometry A 73, 785-787.
24. Perdew, G. H. (2008). Ah receptor binding to its cognate response element is required for dioxin-mediated toxicity. Toxicol. Sci. 106, 301-303.
25. Perry, M. J. (2008). Effects of environmental and occupational pesticide exposure on human sperm: a systematic review. Hum. Reprod. Update 14, 233-242.
26. Peters, J. M., Narotsky, M. G., Elizondo, G., Fernandez-Salguero, P. M., Gonzalez, F. J., and Abbott, B. D. (1999). Amelioration of TCDD-induced teratogenesis in aryl hydrocarbon receptor (AhR)-nullmice.Toxicol. Sci. 47, 86-92.
27. Revel, A., Raanani, H., Younglai, E., Xu, J., Han, R., Savouret, J. F., and Casper, R. F. (2001). Resveratrol, a natural aryl hydrocarbon receptor antagonist, protects sperm from DNA damage and apoptosis caused by benzo(a)pyrene. Reprod. Toxicol. 15, 479-486.
28. Rowlands, J. C., and Gustafsson, J. A. (1997). Aryl hydrocarbon receptormediated signal transduction. Crit. Rev. Toxicol. 27, 109-134.
29. Sadeu, J. C., Hughes, C. L., Agarwal, S., and Foster, W. G. (2010). Alcohol, drugs, caffeine, tobacco, and environmental contaminant exposure: reproductive health consequences and clinical implications. Crit. Rev. Toxicol. 40, 633-652.
30. Sergerie, M., Ouhilal, S., Bissonnette, F., Brodeur, J., and Bleau, G. (2000). Lack of association between smoking and DNA fragmentation in the spermatozoa of normal men. Hum. Reprod. 15, 1314-1321.
31. Shimizu, Y., Nakatsuru, Y., Ichinose, M., Takahashi, Y., Kume, H., Mimura, J., Fujii-Kuriyama, Y., and Ishikawa, T. (2000). Benzo[a]pyrene carcinogenicity is lost in mice lacking the aryl hydrocarbon receptor. Cancer Epidemiol. Biomarkers Prev. 97, 779-782.
32. Simanainen, U., Adamsson, A., Tuomisto, J. T., Miettinen, H. M., Toppari, J., Tuomisto, J., and Viluksela, M. (2004). Adult 2,3,7,8-tetrachlorodibenzop-dioxin (TCDD) exposure and effects on male reproductive organs in three differentially TCDD-susceptible rat lines. Toxicol. Sci. 81, 401-407.
33. Smart, J., and Daly, A. K. (2000). Variation in induced CYP1A1 levels: relationship to CYP1A1, Ah receptor and GSTM1 polymorphisms. Pharmacogenetics 10, 11-24.
34. Swan, S. H., Elkin, E. P., and Fenster, L. (2000). The question of declining sperm density revisited: an analysis of 101 studies published 1934-1996. Environ. Health Perspect. 108, 961-966.
35. Thurmond, T. S., Silverstone, A. E., Baggs, R. B., Quimby, F. W., Staples, J. E., and Gasiewicz, T. A. (1999). A chimeric aryl hydrocarbon receptor knockout mouse model indicates that aryl hydrocarbon receptor activation in hematopoietic cells contributes to the hepatic lesions induced by 2,3,7, 8-tetrachlorodibenzo-p-dioxin. Toxicol. Appl. Pharmacol. 158, 33-40.
36. Verhofstad, N., van Oostrom, C. T., Zwart, E., Maas, L. M., van Benthem, J., van Schooten, F. J., van Steeg, H., and Godschalk, R. W. (2011). Evaluation of benzo(a)pyrene-induced gene mutations in male germ cells. Toxicol. Sci. 119, 218-223.
37. Wong, J. M., Harper, P. A., Meyer, U. A., Bock, K. W., Morike, K., Lagueux, J., Ayotte, P., Tyndale, R. F., Sellers, E. M., Manchester, D. K., et al. (2001). Ethnic variability in the allelic distribution of human aryl hydrocarbon receptor codon 554 and assessment of variant receptor function in vitro. Pharmacogenetics 11, 85-94.
38. World Health Organization. (1999). WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction. Ann. Ist Super Sanita. 37, I- XII; 1-123.
39. Wu, B., Lu, N. X., Xia, Y. K., Gu, A. H., Lu, C. C., Wang, W., Song, L., Wang, S. L., Shen, H. B., and Wang, X. R. (2007). A frequent Y chromosome b2/b3 subdeletion shows strong association with male infertility in Han-Chinese population. Hum. Reprod. 22, 1107-1113.
40. Xia, Y., Han, Y., Zhu, P., Wang, S., Gu, A., Wang, L., Lu, C., Fu, G., Song, L., and Wang, X. (2009a). Relation between urinary metabolites of polycyclic aromatic hydrocarbons and human semen quality. Environ. Sci. Technol. 43, 4567-4573.
41. Xia, Y., Zhu, P., Han, Y., Lu, C., Wang, S., Gu, A., Fu, G., Zhao, R., Song, L., and Wang, X. (2009b). Urinary metabolites of polycyclic aromatic hydrocarbons in relation to idiopathic male infertility. Hum. Reprod. 24, 1067-1074.
42. Xue, W., and Warshawsky, D. (2005). Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: a review. Toxicol. Appl. Pharmacol. 206, 73-93.
43. Zhang, F., Lu, C., Li, Z., Xie, P., Xia, Y., Zhu, X., Wu, B., Cai, X., Wang, X., and Qian, J. (2007). Partial deletions are associated with an increased risk of complete deletion in AZFc: a new insight into the role of partial AZFc deletions in male infertility. J. Med. Genet. 44, 437-444.