Effect of in vitro exposure to benzo[a]pyrene, a component of cigarette smoke, on folliculogenesis, steroidogenesis and oocyte nuclear maturation

Reproductive Toxicology

Volumn 31, Issue 4, 2011, Pages 402-408

  Sadeu, J C ^a   Foster, W G ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Anti m llerian hormone; Benzo a pyrene; Cigarette smoking; Follicle culture; Folliculogenesis; Steroidogenesis

Indexed keywords

BENZO[A]PYRENE; CIGARETTE SMOKE; ESTRADIOL; MUELLERIAN INHIBITING FACTOR; PROGESTERONE; STEROID;

ANIMAL CELL; ARTICLE; CELL ISOLATION; CELL NUCLEUS; CELL SURVIVAL; CIGARETTE SMOKING; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOWN REGULATION; ESTROGEN SYNTHESIS; FEMALE; FEMALE INFERTILITY; MEIOSIS; MOUSE; NONHUMAN; OOCYTE MATURATION; OVARY FOLLICLE DEVELOPMENT; PROGESTERONE SYNTHESIS; REPRODUCTIVE TOXICITY; STEROIDOGENESIS; TOXICITY TESTING;

ANALYSIS OF VARIANCE; ANIMALS; ANTI-MULLERIAN HORMONE; BENZO(A)PYRENE; CELL NUCLEUS; CELL SURVIVAL; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; FEMALE; GONADAL STEROID HORMONES; LINEAR MODELS; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; OOCYTES; OOGENESIS; OVARIAN FOLLICLE; PROGESTERONE; SMOKE; SMOKING; TIME FACTORS;

MUS;

EID: 79956370667     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2010.12.006     Document Type: Article

References (48)

1. World Health Organization 2008 WHO Report on the Global Tobacco Epidemic. In the MPOWER package: Geneva.
2. Practice Committee of American Society for Reproductive Medicine Smoking and infertility. Fertil Steril 2004, 4:1181-1186.
3. Practice Committee of American Society for Reproductive Medicine Smoking and infertility. Fertil Steril 2008, 90:S254-S259.
4. Health Canada 2009 Canadian Tobacco Use Monitoring Survey. Canadian Tobacco Use Monitoring Survey.
5. Cohen B., Evers S., Manske S., Bercovitz K., Edward H.G. Smoking, physical activity and breakfast consumption among secondary school students in a southwestern Ontario community. Can J Public Health 2003, 94:41-44.
6. Roth L.K., Taylor H.S. Risks of smoking to reproductive health: assessment of women's knowledge. Am J Obstet Gynecol 2001, 184:934-939.
7. Dechanet C, Anahory T, Mathieu Daude JC, Quantin X, Reyftmann L, Hamamah S, et al. Effects of cigarette smoking on reproduction. Hum Reprod Update 2010 [Epub ahead of print].
8. Sadeu J.C., Hughes C.L., Agarwal S., Foster W.G. Alcohol, drugs, caffeine, tobacco, and environmental contaminant exposure: reproductive health consequences and clinical implications. Crit Rev Toxicol 2010, 40:633-652.
9. Cooper G.S., Baird D.D., Hulka B.S., Weinberg C.R., Savitz D.A., Hughes C.L. Follicle-stimulating hormone concentrations in relation to active and passive smoking. Obstet Gynecol 1995, 85:407-411.
10. Weathersbee P.S. Nicotine and its influence on the female reproductive system. J Reprod Med 1980, 25:243-250.
11. U.S.Department of Health and Human Services The health consequences of smoking for women: a report of the surgeon general 1980, U.S. Department of Health and Human Services, Public Health Service, Office of the Assistant Secretary for Health, Office on Smoking and Health, Rockville, MD.
12. Coghlin J., Gann P.H., Hammond S.K., Skipper P.L., Taghizadeh K., Paul M., et al. 4-Aminobiphenyl hemoglobin adducts in fetuses exposed to the tobacco smoke carcinogen in utero. J Natl Cancer Inst 1991, 83:274-280.
13. Detmar J., Rennie M.Y., Whiteley K.J., Qu D., Taniuchi Y., Shang X., et al. Fetal growth restriction triggered by polycyclic aromatic hydrocarbons is associated with altered placental vasculature and AhR-dependent changes in cell death. Am J Physiol Endocrinol Metab 2008, 295:519-530.
14. Adeno M., Gallagher H. Cigarette smoking and the age of menopause. Ann Hum Biol 1982, 9:121-130.
15. Freour T., Masson D., Mirallie S., Jean M., Bach K., Dejoie T., et al. Active smoking compromises IVF outcome and affects ovarian reserve. Reprod Biomed Online 2008, 16:96-102.
16. Sharara F.I., Beatse S.N., Leonardi M.R., Navot D., Scott R.T. Cigarette smoking accelerates the development of diminished ovarian reserve as evidenced by the clomiphene citrate challenge test. Fertil Steril 1994, 62:257-262.
17. El-Nemr A., Al-Shawaf T., Sabatini L., Wilson C., Lower A.M., Grudzinskas J.G. Effect of smoking on ovarian reserve and ovarian stimulation in in vitro fertilization and embryo transfer. Hum Reprod 1998, 13:2192-2198.
18. Mattison D.R., Thorgeirsson S.S. Smoking and industrial pollution, and their effects on menopause and ovarian cancer. Lancet 1978, 187-188.
19. Tuttle A.M., Stämpfli M., Foster W.G. Cigarette smoke causes follicle loss in mice ovaries at concentrations representative of human exposure. Hum Reprod 2009, 24:1452-1459.
20. EPA. Respiratory health effects of passive smoking: lung cancer and other disorders. Washington, DC; 1992 [Report/600/6-90/006F].
21. Charles G.D., Bartels M.J., Zacharewski T.R., Gollapudi B.B., Freshour N.L., Carney E.W. Activity of benzo(a)pyrene and its hydroxylated metabolites in an estrogen receptor-a reporter gene assay. Toxicol Sci 2000, 55:320-326.
22. ATSDR 1990 Toxicological Profile for Benzo(a)pyrene, May. Prepared by ICF-Clement under Contract No. 68-02-4235 for USDHHS, PHS, CDC, ATSDR, in collaboration with the United States Environmental Protection Agency (U.S. EPA), with technical editing/document preparation by Oak Ridge National Laboratory. ATSDR/TP-88/05. ATSDR, CDC. Atlanta, Georgia.
23. ATSDR 1995 Toxicological Profile for Polycyclic Aromatic Hydrocarbons (PAHs) (Update), August. Prepared by Research Triangle Institute for the Agency for Toxic Substances and Disease Registry (ATSDR), United States Department of Health and Human Services (USDHHS), Public Health Service (PHS), Centers for Disease Control (CDC) ATSDR, CDC. Atlanta, Georgia.
24. Neal M.S., Zhu J., Foster W.G. Quantification of benzo[a]pyrene and other PAHs in the serum and follicular fluid of smokers versus non-smokers. Reprod Toxicol 2008, 25:100-106.
25. Neal M.S., Hughes E.G., Holloway A.C., Foster W.G. Sidestream smoking is equally as damaging as mainstream smoking on IVF outcomes. Hum Reprod 2005, 20:2531-2535.
26. Neal M.S., Zhu J., Holloway A.C., Foster W.G. Follicle growth is inhibited by benzo-[a]-pyrene, at concentrations representative of human exposure, in an isolated rat follicle culture assay. Hum Reprod 2007, 22:961-967.
27. Mackenzie K.M., Angevine D.M. Infertility in mice exposed in utero to benzo(a)pyrene. Biol Reprod 1981, 24:183-191.
28. Kristensen P., Eilertsen E., Einarsdottir E., Haugen A., Skaug V., Ovrebo S. Fertility in mice after prenatal exposure to benzo(a)pyrene and inorganic lead. Environ Health Perspect 1995, 103:588-590.
29. Swartz W.J., Mattison D.R. Benzo(a)pyrene inhibits ovulation in C57BL/6N mice. Anat Rec 1985, 212:268-276.
30. TOMES PLUS® system 1997, Micromedex, Inc., Englewood, Colorado. A.H. Hall, Rumack BH (Eds.).
31. Mattison D.R., Thorgeirsson S.S. Ovarian aryl hydrocarbon hydroxylase activity and primordial oocyte toxicity of polycyclic aromatic hydrocarbons in mice. Cancer Res 1979, 39:3471-3475.
32. Borman S.M., Christian P.J., Sipes I.G., Hoyer P.B. Ovotoxicity in female Fischer rats and B6 mice induced by low-dose exposure to three polycyclic aromatic hydrocarbons: comparison through calculation of an ovotoxic index. Toxicol Appl Pharmacol 2000, 167:191-198.
33. Cortvrindt R.G., Smitz J.E., Van Steirteghem A.C. In-vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepuberal mice in a simplified culture system. Hum Reprod 1996, 11:2656-2666.
34. Cortvrindt R.G., Smitz J.E. Follicle culture in reproductive toxicology: a tool for in-vitro testing of ovarian function?. Hum Reprod Update 2002, 8:43-254.
35. Mattison D.R., Nightingale M.S. Oocyte destruction by polycyclic aromatic hydrocarbons is not linked to the inducibility of ovarian aryl hydrocarbon (benzo(a)pyrene) hydroxylase activity in (DBA/2N X C57BL/6N) F1 X DBA/2N backcross mice. Pediatr Pharmacol (New York) 1982, 2:11-21.
36. Mattison D.R., Shiromizu K., Nightingale M.S. Oocyte destruction by polycyclic aromatic hydrocarbons. Am J Ind Med 1983, 4:191-202.
37. Jurisicova A., Taniuchi A., Li H., Shang Y., Antenos M., Detmar J., et al. Maternal exposure to polycyclic aromatic hydrocarbons diminishes murine ovarian reserve via induction of Harakiri. J Clin Invest 2007, 117:3971-3978.
38. Barbieri R.L., McShane P.M., Ryan K.J. Constituents of cigarette smoke inhibit human granulosa cell aromatase. Fertil Steril 1986, 46:232-236.
39. Weiss T., Eckert A. Cotinine levels in follicular fluid and serum of IVF patients: effect on granulosa-luteal cell function in vitro. Hum Reprod 1989, 4:482-485.
40. Bódis J., Hanf V., Török A., Tinneberg H.R., Borsay P., Szabó I. Influence of nicotine on progesterone and estradiol production of cultured human granulosa cells. Early Pregnancy 1997, 3:34-37.
41. Oktem O., Oktay K. The ovary: anatomy and function throughout human life. Ann NY Acad Sci 2008, 1127:1-9.
42. Behringer R.R., Cate R.L., Froelick G.J., Palmiter R.D., Brinster R.L. Abnormal sexual development in transgenic mice chronically expressing müllerian inhibiting substance. Nature 1990, 345:167-170.
43. Durlinger A.L., Gruijters M.J., Kramer P., Karels B., Ingraham H.A., Nachtigal M.W., et al. Anti-mullerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology 2002, 143:1076-1084.
44. Neal M.S., Mulligan Tuttle A.M., Casper R.F., Lagunov A., Foster W.G. Aryl hydrocarbon receptor antagonists attenuate the deleterious effects of benzo[a]pyrene on isolated rat follicle development. Reprod Biomed Online 2010, 21:100-108.
45. Durlinger A.L., Visser J.A., Themmen A.P. Regulation of ovarian function: the role of anti-mullerian hormone. Reproduction 2002, 124:601-609.
46. Plante B.J., Cooper G.S., Baird D.D., Steiner A.Z. The impact of smoking on antimüllerian hormone levels in women aged 38 to 50 years. Menopause 2010, 17:571-576.
47. Nardo L.G., Christodoulou D., Gould D., Roberts S.A., Fitzgerald C.T., Laing I. Anti-müllerian hormone levels and antral follicle count in women enrolled in in vitro fertilization cycles: relationship to lifestyle factors, chronological age and reproductive history. Gynecol Endocrinol 2007, 23:486-493.
48. Zenzes M.T., Krishnan S., Krishnan B., Zhang H., Casper R.F. Cadmium accumulation in follicular fluid of women in in vitro fertilization-embryo transfer is higher in smokers. Fertil Steril 1995, 64:599-603.