Endocrine disruptive actions of inhaled benzo(a)pyrene on ovarian function and fetal survival in fisher F-344 adult rats

Reproductive Toxicology

Volumn 34, Issue 4, 2012, Pages 635-643

  Archibong, Anthony E ^a   Ramesh, Aramandla ^a   Inyang, Frank ^a   Niaz, Mohammad S ^a   Hood, Darryl B ^a   Kopsombut, Prapaporn ^b  

^a MEHARRY MEDICAL COLLEGE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Benzo(a)pyrene; Estrogen; Follicle stimulating hormone; Inhalation; Luteinizing hormone; Meiotic maturation; Ovulation; Progesterone

Indexed keywords

BENZO[A]PYRENE; ENDOCRINE DISRUPTOR; ESTROGEN; FOLLITROPIN; LUTEINIZING HORMONE; PROGESTERONE; UNSPECIFIC MONOOXYGENASE;

ANIMAL CELL; ARTICLE; CELL MATURATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVITY; ESTRUS; ESTRUS CYCLE; FEMALE; FEMALE GENITAL SYSTEM; FEMALE INFERTILITY; FETUS; FETUS WASTAGE; LIVER; LUNG; MEIOSIS; NONHUMAN; OVARY FUNCTION; OVULATION; RAT; SURVIVAL RATE;

ADMINISTRATION, INHALATION; ANIMALS; ARYL HYDROCARBON HYDROXYLASES; BENZO(A)PYRENE; CARCINOGENS; ENDOCRINE DISRUPTORS; ESTRADIOL; ESTROUS CYCLE; FEMALE; FERTILITY; FETUS; FOLLICLE STIMULATING HORMONE; LITTER SIZE; LIVER; LUNG; LUTEINIZING HORMONE; MALE; OVARY; OVULATION; PROGESTERONE; RATS; RATS, INBRED F344;

RATTUS;

EID: 84867766566     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2012.09.003     Document Type: Article

References (95)

1. Abma J.C., Chandra A., Mosher W.D., Peterson L.J., Piccinino L.J. Fertility, family planning, and women's health: estimates from the 1995 National Survey of Family Growth. Vital Health Statistics 1997, 23:19.
2. Stephen E.H., Chandra A. Updated projections of infertility in the United States: 1995-2025. Fertility and Sterility 1998, 70:30-34.
3. Sharara F.I., Seifer D.B., Flaws J.A. Environmental toxicants and female reproduction. Fertility and Sterility 1998, 70:613-622.
4. Mark-Kappeler C.J., Hoyer P.B., Devine P.J. Xenobiotic effects on ovarian preantral follicles. Biology of Reproduction 2011, 85:871-883.
5. Makuc D, Lalich N. Employment characteristics of mothers during pregnancy. National Center for Health Statistics, DHHS Publication No. 841232. Washington, DC: Public Health Service, US Government Printing Office; 1983. p. 25-32.
6. Hirshfield A.N. Development of follicles in the mammalian ovary. International Review of Cytology 1991, 124:43-101.
7. Mattison D.R., White N.B., Nightingale M.R. The effect of benzo(a)pyrene on fertility, primordial oocyte number, and ovarian response to pregnant mare's serum gonadotropin. Pediatric Pharmacology 1980, 1:143-151.
8. 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. Toxicology and Applied Pharmacology 2000, 167:191-198.
9. Jick H., Porter J. Relation between smoking and age of natural menopause. Report from the Boston Collaborative Drug Surveillance Program, Boston University Medical Center. Lancet 1977, 1:1354-1355.
10. Howe G., Westhoff C., Vessey M., Yeates D. Effects of age, cigarette smoking, and other factors on fertility: findings in a large prospective study. British Medical Journal (Clinical Research Edition) 1985, 290:1697-1700.
11. Baird D.T., Collins J., Egozcue J., Evers L.H., Gianaroli L., Leridon H., et al. Fertility and ageing. Human Reproduction Update 2005, 11:261-276.
12. Pattinson H.A., Taylor P.J., Pattinson M.H. The effect of cigarette smoking on ovarian function and early pregnancy outcome of in vitro fertilization treatment. Fertility and Sterility 1991, 55:780-783.
13. Seltzer V. Smoking as a risk factor in the health of women. International Journal of Gynaecology and Obstetrics 2003, 82:393-397.
14. Zenzes M.T., Wang P., Casper R.F. Cigarette smoking may affect meiotic maturation of human oocytes. Human Reproduction 1995, 10:3213-3217.
15. Neal M.S., Hughes E.G., Holloway A.C., Foster W.G. Sidestream smoking is equally as damaging as mainstream smoking on IVF outcomes. Human Reproduction 2005, 20:2531-2535.
16. Rustemeier K., Stabbert R., Haussmann H.J., Roemer E., Carmines E.L. Evaluation of the potential effects of ingredients added to cigarettes. Part 2: chemical composition of mainstream smoke. Food and Chemical Toxicology 2002, 40:93-104.
17. Lodovici M., Akpan V., Evangelisti C., Dolara P. Sidestream tobacco smoke as the main predictor of exposure to polycyclic aromatic hydrocarbons. Journal of Applied Toxicology 2004, 24:277-281.
18. Zenzes M.T. Smoking and reproduction: gene damage to human gametes and embryos. Human Reproduction Update 2000, 6:122-131.
19. Archibong A.E., Inyang F., Ramesh A., Greenwood M., Nayyar T., Kopsombut P., et al. Alteration of pregnancy related hormones and fetal survival in F-344 rats exposed by inhalation to benzo(a)pyrene. Reproductive Toxicology 2002, 16:801-808.
20. Ramesh A., Archibong A. Reproductive toxicity of polycyclic aromatic hydrocarbons: occupational relevance. Reproductive and developmental toxicology 2011, 577-592. Academic Press, London. R.C. Gupta (Ed.).
21. Ramesh A., Walker S.A., Hood D.B., Guillen M.D., Schneider H., Weyand E.H. Bioavailability and risk assessment of orally ingested polycyclic aromatic hydrocarbons. International Journal of Toxicology 2004, 23:301-333.
22. 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-α reporter gene assay. Toxicological Sciences 2000, 55:320-326.
23. Inyang F., Ramesh A., Kopsombut P., Niaz M.S., Hood D.B., Nyanda A.M., et al. Disruption of testicular steroidogenesis and epididymal function by inhaled benzo(a)pyrene. Reproductive Toxicology 2003, 17:527-537.
24. Kim J-C., Kim S-H., Shin D-H., Ahn T-H., Kim H-C., Kim Y-B., et al. Effects of prenatal exposure to the environmental pollutant 2-bromopropane on embryo-fetal development in rats. Toxicology 2004, 196:77-86.
25. Ramesh A., Archibong A.E., Niaz M.S. Ovarian susceptibility to benzo(a)pyrene: tissue burden of metabolites and DNA adducts in F-344 rats. Journal of Toxicology and Environmental Health. Part A 2010, 73:1611-1625.
26. Goldman J.M., Murr A.S., Cooper R.L. The rodent estrous cycle: characterization of vaginal cytology and its utility in toxicological studies. Birth Defects Research Part B: Developmental and Reproductive Toxicology 2007, 80:84-97.
27. Accardi-Dey A., Gschwend P.M. Reinterpreting literature sorption data considering both absorption into organic carbon and adsorption onto black carbon. Environmental Science and Technology 2003, 37:99-106.
28. Ramesh A., Greenwood M., Inyang F., Hood D.B. Toxicokinetics of inhaled benzo(a)pyrene: plasma and lung bioavailability. Inhalation Toxicology 2001, 13:533-553.
29. Wolff R.K., Bond J.A., Sun J.D., Henderson R.F., Harkema J.R., Griffith W.C., et al. Effects of adsorption of benzo(a)pyrene onto carbon black particles on levels of DNA adducts in lungs of rats exposed by inhalation. Toxicology and Applied Pharmacology 1989, 97:289-299.
30. US Environmental Protection Agency. Acute inhalation toxicity. TSCA 798; 40 CFR 790; 1989.
31. European Union Guideline 92/69/ECC. Acute toxicity inhalation. Office J Eur Comm Legal Spec L383A 1992;35:117.
32. Hood D.B., Nayyar T., Ramesh A., Greenwood M., Inyang F. Modulation in the developmental expression profile of SP1 subsequent to transplacental exposure of fetal rats to desorbed benzo(a)pyrene following maternal inhalation. Inhalation Toxicology 2000, 12:511-535.
33. Armstrong D.T., Zhang X., Vanderhyden B.C., Khamsi F. Hormonal actions during oocyte maturation influence fertilization and early embryonic development. Annals of the New York Academy of Sciences 1991, 626:137-158.
34. Yanagimachi R., Yanagimachi H., Rogers B.J. The use of zona-free animal ova as a test-system for the assessment of the fertilizing capacity of human spermatozoa. Biology of Reproduction 1976, 15:471-476.
35. Ramesh A., Inyang F., Hood D.B., Knuckles M.E. Aryl hydrocarbon hydroxylase activity in F-344 rats subchronically exposed to benzo(a)pyrene and fluoranthene through diet. Journal of Biochemical and Molecular Toxicology 2000, 14:155-161.
36. Bradford M. A rapid and sensitive method for the quantification of microgram quantities of protein, utilizing the principle of dye binding. Analytical Biochemistry 1976, 72:248-254.
37. Yang S-C., Jenq S-N., Kang Z.C., Lee H. Identification of benzo(a)pyrene 7,8-diol 9,10-epoxide N2-deoxyguanosine in human lung adenocarcinoma cells exposed to cooking oil fumes from frying fish under domestic conditions. Chemical Research in Toxicology 2000, 13:1046-1050.
38. ATSDR Toxicological profile for polycyclic aromatic hydrocarbons (PAHs) 1995, Agency for Toxic Substances and Disease Registry, US Department of Health and Human Services, US Public Health Service, Atlanta, GA, 271pp.
39. Ramesh A., Inyang F., Lunstra D.D., Niaz M.S., Kopsombut P., Jones K.M., et al. Alteration of fertility endpoints in adult male F-344 rats by subchronic exposure to inhaled benzo(a)pyrene. Experimental and Toxicologic Pathology 2008, 60:269-280.
40. Archibong A.E., Ramesh A., Niaz M.S., Brooks C.M., Roberson S.I., Lunstra D.D. Effects of benzo(a)pyrene on intratesticular function in F-344 rats. International Journal of Environmental Research and Public Health 2008, 5:32-40.
41. Lewtas J., Walsh D., Williams R., Dobias L. Air pollution exposure-DNA adduct dosimetry in humans and rodents: evidence for non-linearity at high doses. Mutation Research 1997, 378:51-63.
42. Li S., Olegario R.M., Banyasz J.L., Shafer K.H. Gas chromatography-mass spectrometry analysis of polycyclic aromatic hydrocarbons in single puff of cigarette smoke. Journal of Analytical and Applied Pyrolysis 2003, 66:155-163.
43. Besaratinia A., Maas L.M., Brouwer E.M.C., Moonen E.J.C., Dekok T.M.C.M., Wesseling G.J., et al. A molecular dosimetry approach to assess human exposure to environmental tobacco smoke in pubs. Carcinogenesis 2002, 23:1171-1176.
44. Chorazy M., Szeliga J., Strozyk M., Cimander B. Ambient air pollutants in upper Silesia: partial chemical composition and biological activity. Environmental Health Perspectives 1994, 102(Suppl. 4):61-66.
45. Chiang T-A., Wu P-F., Ko-Y-C. Identification of carcinogens in cooking oil fumes. Environmental Research Part A 1999, 81:18-22.
46. Viau C., Hakizimana G., Bouchard M. Indoor exposure to polycyclic aromatic hydrocarbons and carbon monoxide in traditional houses in Burundi. International Archives of Occupational and Environmental Health 2000, 73:331-338.
47. National Institute for Occupational Safety and Health (NIOSH) Pocket guide to chemical hazards 1997, U.S. Department of Health and Human Services, Public Health Service, Centers for Disease Control and Prevention, Cincinnati, OH.
48. Occupational Safety and Health Administration (OSHA). Occupational safety and health standards, toxic and hazardous substances. Code of Federal Regulations, 29 CFR 1910.1000; 1998.
49. American Conference of Governmental Industrial Hygienists (ACGIH) 1999 TLVs and BEIs 1999, Threshold limit values for chemical substances and physical agents, biological exposure indices, Cincinnati, OH.
50. Shivalingappa H., Satyanarayan N.D., Purohit M.G., Sharanabasappa A., Patil S.B. Effect of ethanol extract of Rivea hypocrateriformis on the estrous cycle of the rat. Journal of Ethnopharmacology 2002, 82:11-17.
51. Benedict J.C., Miller K.P., Lin T.M., Greenfeld C., Babus J.K., Peterson R.E., et al. Aryl hydrocarbon receptor regulates growth, but not atresia, of mouse preantral and antral follicles. Biology of Reproduction 2003, 68:1511-1517.
52. Ishigame H., Medan M.S., Watanabe G., Shi Z., Kishi H., Arai K.Y., et al. A new alternative method for superovulation using passive immunization against inhibin in adult rats. Biology of Reproduction 2004, 7:236-243.
53. McLean B.K., Rubel A., Nikitovitch-Winer M.B. The differential effects of exposure to tobacco smoke on the secretion of luteinizing hormone and prolactin in the proestrous rat. Endocrinology 1977, 100:1566-1570.
54. Naftolin F., Garcia-Segura L.M., Horvath T.L., Zsarnovszky A., Demir N., Fadiel A., et al. Estrogen-induced hypothalamic synaptic plasticity and pituitary sensitization in the control of the estrogen-induced gonadotrophin surge. Reproduction Science 2007, 14:101-116.
55. Peluso J.J., Steger R.W., Hafez E.S. Regulation of LH secretion in aged female rats. Biology of Reproduction 1977, 16:212-215.
56. Sadeu J.C., Foster W.G. Effect of in vitro exposure to benzo[a]pyrene, a component of cigarette smoke, on folliculogenesis, steroidogenesis and oocyte nuclear maturation. Reproductive Toxicology 2011, 31:402-408.
57. Pellicer A., Lightman A., Diamond M.P., Russell J.B., DeCherney A.H. Outcome of in vitro fertilization in women with low response to ovarian stimulation. Fertility and Sterility 1987, 47:812-815.
58. Wu J., Hou H., Ritz B., Chen Y. Exposure to polycyclic aromatic hydrocarbons and missed abortion in early pregnancy in a Chinese population. Science of the Total Environment 2010, 408:2312-2318.
59. Sun F., Betzendahl I., Shen Y., Cortvrindt R., Smitz J., Eichenlaub-Ritter U. Preantral follicle culture as a novel in vitro assay in reproductive toxicology testing in mammalian oocytes. Mutagenesis 2004, 19:13-25.
60. Uno S., Endo K., Ishida Y., Tateno C., Makishima M., Yoshizato K., et al. CYP1A1 and CYP1A2 expression: comparing 'humanized' mouse lines and wild-type mice; comparing human and mouse hepatoma-derived cell lines. Toxicology and Applied Pharmacology 2009, 237:119-126.
61. Zelinski-Wooten M.B., Hess D.L., Baughman W.L., Molskness T.A., Wolf D.P., Stouffer R.L. Administration of an aromatase inhibitor during the late follicular phase of gonadotrophin-treated cycles in rhesus monkeys: effects on follicle development, oocyte maturation, and subsequent luteal function. Journal of Clinical Endocrinology and Metabolism 1993, 76:988-995.
62. Tatemoto H., Ootaki K., Shigeta K., Muto N. Enhancement of developmental competence after in vitro fertilization of porcine oocytes by treatment with ascorbic acid 2-O-alpha-glucoside during in vitro maturation. Biology of Reproduction 2001, 65:1800-1806.
63. Campbell B.K., McNeilly A.S. Follicular dominance and oocyte maturation. Zygote 1996, 4:327-334.
64. Fulvio C. Intra-ovarian regulation of oocyte developmental competence in cattle. Zygote 1996, 4:323-326.
65. Richards J.S., Jahnsen T., Hedin L., Lifka J., Ratoosh S., Durica J.M., et al. Ovarian follicular development: from physiology to molecular biology. Recent Progress in Hormone Research 1987, 43:231-276.
66. Suzuki S., Endo Y., Tanaka S., Iizuka R. Indirect immunofluorescence studies on the steroid-producing activity of hamster ova. American Journal of Obstetrics and Gynecology 1984, 148:76-85.
67. Yoshimura Y., Hosoi Y., Atlas S.J., Bongiovanni A.M., Santulli R., Wallach E.E. The effect of ovarian steroidogenesis on ovulation and fertilizability in the in vitro perfused rabbit ovary. Biology of Reproduction 1986, 35:943-948.
68. Saeki K., Kato H., Hosoi Y., Miyake M., Utsumi K., Iritani A. Early morphological events of in vitro fertilized bovine oocytes with frozen-thawed spermatozoa. Theriogenology 1991, 35:1051-1058.
69. Zheng P., Wei S., Bavister B.D., Yang J., Ding C., Ji W. 17b-Estradiol and progesterone improve in vitro cytoplasmic maturation of oocytes from unstimulated prepubertal and adult rhesus monkeys. Human Reproduction 2003, 18:2137-2144.
70. Zelinski-Wooten M.B., Hess D.L., Wolf D.P., Stouffer R.L. Steroid reduction during ovarian stimulation impairs oocyte fertilization, but not folliculogenesis, in rhesus monkeys. Fertility and Sterility 1994, 61:1147-1155.
71. Carson D.D., Bagchi I., Dey S.K., Enders A.C., Fazleabas A.T., Lessey B.A., et al. Embryo implantation. Developmental Biology 2000, 223:217-237.
72. Das A., Mantena S.R., Kannan A., Evans D.B., Bagchi M.K., Bagchi I.C. De novo synthesis of estrogen in pregnant uterus is critical for stromal decidualization and angiogenesis. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:12542-12547.
73. Archibong A.E., England D.C., Stormshak F. Factors contributing to early embryonic mortality in gilts bred at pubertal estrus. Journal of Animal Science 1987, 64:474-478.
74. Kanety H., Moshe S., Shafrir E., Lunenfeld B., Karasik A. Hyperinsulinemia induces a reversible impairment in insulin receptor function leading to diabetes in the sand rat model of non-insulin-dependent diabetes mellitus. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:1853-1857.
75. Eppig J.J., O'Brien M.J., Pendola F.L., Watanabe S. Factors affecting the developmental competence of mouse oocytes grown in vitro: follicle-stimulating hormone and insulin. Biology of Reproduction 1998, 59:1445-1453.
76. Eppig J.J., Hosoe M., O'Brien M.J., Pendola F.M., Requena A., Watanabe S. Conditions that affect acquisition of developmental competence by mouse oocytes in vitro: FSH, insulin, glucose and ascorbic acid. Molecular and Cellular Endocrinology 2000, 163:109-116.
77. Dullaart J., Kent J., Ryle M. Serum gonadotrophin concentrations in infantile female mice. Reproduction and Fertility 1975, 43:189-192.
78. Halpin D.M., Charlton H.M., Faddy M.J. Effects of gonadotrophin deficiency on follicular development in hypogonadal (hpg) mice. Reproduction and Fertility 1986, 78:119-125.
79. Harris D.L., Huderson A.C., Niaz M.S., Ford J.J., Archibong A.E., Ramesh A. Comparative metabolism of benzo(a)pyrene by ovarian microsomes of various species. Environmental Toxicology 2009, 24:603-609.
80. Antonsson C., Arulampalam V., Whitelaw M.L., Pettersson S., Poellinger L. Constitutive function of the basic helix-loop-helix/PAS factor Arnt. Regulation of target promoters via the E box motif. Journal of Biological Chemistry 1995, 270:13968-13972.
81. Blackwell T.S., Christman J.W. The role of nuclear factor-kappa B in cytokine gene regulation. American Journal of Respiratory Cell and Molecular Biology 1997, 17:3-9.
82. Calogero A.E., Nicoletti F., Palumbo M.A., Burrello N., Di Mauro M., Lunetta M., et al. Macrophage-derived cytokines in the follicular fluids of women with infertility due to immunological causes. Elevated levels of interleukin 6 and low levels of granulocyte-macrophage colony-stimulating factor. Cytokine 1998, 10:814-818.
83. Albalak R., Keeler G.J., Frisancho A.R., Haber M. Assessment of PM10 concentrations from domestic biomass fuel combustion in rural Bolivian highland villages. Environmental Science and Technology 1999, 33:2505-2509.
84. Ezzati M., Saleh H., Kammen D.M. The contributions of emissions and spatial microenvironments to exposure to indoor air pollution from biomass combustion in Kenya. Environmental Health Perspectives 2000, 108:833-839.
85. Balakrishnan K., Parikh J., Sankar S., Padmavathi R., Srividya K., Venugopal V., et al. Daily average exposures to respirable particulate matter from combustion of biomass fuels in rural households of southern India. Environmental Health Perspectives 2002, 110:1069-1075.
86. Reddy A.K.N., Williams R.H., Johansson T.B. Energy after rio: prospects and challenges 1996, United Nations Publications, New York.
87. Oanh N., Reutergardh L., Dung N. Emission of polycyclic aromatic hydrocarbons and particulate matter from domestic combustion of selected fuels. Environmental Science and Technology 1999, 33:2703-2709.
88. Zhang J., Smith K.R. Hydrocarbon emissions and health risks from cook stoves in developing countries. Journal of Exposure Analysis and Environmental Epidemiology 1996, 6:147-161.
89. Wu M-T., Lee L-H., Ho C-K., Wu S-C., Lin L-Y., Cheng B-H., et al. Environmental exposure to cooking oil fumes and cervical intraepithelial neoplasm. Environmental Research 2004, 94:25-32.
90. Chiang T.A., Wu P.F., Ko Y.C. Identification of carcinogens in cooking oil fumes. Environmental Research 1999, 81:18-22.
91. Guerrin M.R. Environmental tobacco smoke exposure assessment. Tobacco smoke 1993, Springer-Verlag, New York.
92. Shuguang L., Dinhua P., Guoxiong W. Analysis of polycyclic aromatic hydrocarbons in cooking oil fumes. Archives of Environmental Health 1994, 49:119-122.
93. Yang S.C., Jenq S.N., Kang Z.C., Lee H. Identification of benzo[a]pyrene 7,8-diol 9,10-epoxide N2-deoxyguanosine in human lung adenocarcinoma cells exposed to cooking oil fumes from frying fish under domestic conditions. Chemical Research in Toxicology 2000, 13:1046-1050.
94. Seow A., Poh W.T., The M., Eng P., Wang Y.T., Tan W.C., et al. Fumes from meat cooking and lung cancer risk in Chinese women. Cancer Epidemiology, Biomarkers and Prevention 2000, 9:1215-1221.
95. Wu M.T., Lee L.H., Ho C.K., Wu S.C., Lin L.Y., Cheng B.H., et al. Environmental exposure to cooking oil fumes and cervical intraepithelial neoplasm. Environmental Research 2004, 94:25-32.