Skip to main content
NCBI home page
Environmental Health Perspectives logoLink to Environmental Health Perspectives
. 1995 May;103(Suppl 4):19–25. doi: 10.1289/ehp.95103s419

Vitellogenin induction by xenobiotic estrogens in the red-eared turtle and African clawed frog.

B D Palmer 1, S K Palmer 1
PMCID: PMC1519278  PMID: 7556019

Abstract

Many environmental pollutants have estrogenic activity in animals. Xenobiotic estrogens include many pesticides and industrial chemicals that biocumulate. The impact of these common pollutants on the reproductive success of wildlife may be considerable, particularly in threatened or endangered species. This research examined the use of plasma vitellogenin in males as a biomarker for estrogenic xenobiotics in reptiles and amphibians. Adult male turtles (Trachemys scripta) and frogs (Xenopus laevis) were given ip injections of estradiol-17 beta (E2), diethylstilbestrol (DES), or o,p'-DDT (1-chloro-2-[2,2,2-trichloro-1-(4-chlorophenyl)ethyl)benzene) daily for 7 days, and plasma was collected on day 14. The estrogenic activity of each compound was determined by measuring the induction of plasma vitellogenin. Vitellogenin was identified by precipitation, electrophoresis, Western blot, and enzyme-linked immunosorbant assay (ELISA). In both species, estradiol and DES treatments induced the most vitellogenin, whereas DDT treatments induced smaller amounts of vitellogenin in a dose-dependent fashion. These data indicate that induction of plasma vitellogenin in males may be a useful biomarker of xenobiotic estrogen activity in wild populations of reptiles and amphibians.

Full text

PDF
19

Images in this article

21Figure 1.
on p.21
22Figure 3.
on p.22

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arai Y., Chen C. Y., Nishizuka Y. Cancer development in male reproductive tract in rats given diethylstilbestrol at neonatal age. Gan. 1978 Dec;69(6):861–862. [PubMed] [Google Scholar]
  2. Bern H. A., Edery M., Mills K. T., Kohrman A. F., Mori T., Larson L. Long-term alterations in histology and steroid receptor levels of the genital tract and mammary gland following neonatal exposure of female BALB/cCrgl mice to various doses of diethylstilbestrol. Cancer Res. 1987 Aug 1;47(15):4165–4172. [PubMed] [Google Scholar]
  3. Bishop C. A., Brooks R. J., Carey J. H., Ng P., Norstrom R. J., Lean D. R. The case for a cause-effect linkage between environmental contamination and development in eggs of the common snapping turtle (Chelydra S.serpentina) from Ontario, Canada. J Toxicol Environ Health. 1991 Aug;33(4):521–547. doi: 10.1080/15287399109531539. [DOI] [PubMed] [Google Scholar]
  4. Bradley J. T., Grizzle J. M. Vitellogenin induction by estradiol in channel catfish, Ictalurus punctatus. Gen Comp Endocrinol. 1989 Jan;73(1):28–39. doi: 10.1016/0016-6480(89)90052-x. [DOI] [PubMed] [Google Scholar]
  5. Bulger W. H., Kupfer D. Estrogenic action of DDT analogs. Am J Ind Med. 1983;4(1-2):163–173. [PubMed] [Google Scholar]
  6. Clark D. R., Jr, Krynitsky A. J. DDE residues and artificial incubation of loggerhead sea turtle eggs. Bull Environ Contam Toxicol. 1985 Jan;34(1):121–125. doi: 10.1007/BF01609712. [DOI] [PubMed] [Google Scholar]
  7. Colborn T., vom Saal F. S., Soto A. M. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect. 1993 Oct;101(5):378–384. doi: 10.1289/ehp.93101378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Crews D., Bull J. J., Wibbels T. Estrogen and sex reversal in turtles: a dose-dependent phenomenon. Gen Comp Endocrinol. 1991 Mar;81(3):357–364. doi: 10.1016/0016-6480(91)90162-y. [DOI] [PubMed] [Google Scholar]
  9. Driscoll S. G., Taylor S. H. Effects of prenatal maternal estrogen on the male urogenital system. Obstet Gynecol. 1980 Nov;56(5):537–542. [PubMed] [Google Scholar]
  10. Fry D. M., Toone C. K. DDT-induced feminization of gull embryos. Science. 1981 Aug 21;213(4510):922–924. doi: 10.1126/science.7256288. [DOI] [PubMed] [Google Scholar]
  11. Goodwin A. E., Grizzle J. M., Bradley J. T., Estridge B. H. Monoclonal antibody-based immunoassay of vitellogenin in the blood of male channel catfish (Ictalurus punctatus). Comp Biochem Physiol B. 1992 Mar;101(3):441–446. doi: 10.1016/0305-0491(92)90025-m. [DOI] [PubMed] [Google Scholar]
  12. Gorski J., Furlow J. D., Murdoch F. E., Fritsch M., Kaneko K., Ying C., Malayer J. R. Perturbations in the model of estrogen receptor regulation of gene expression. Biol Reprod. 1993 Jan;48(1):8–14. doi: 10.1095/biolreprod48.1.8. [DOI] [PubMed] [Google Scholar]
  13. Guillette L. J., Jr, Gross T. S., Masson G. R., Matter J. M., Percival H. F., Woodward A. R. Developmental abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida. Environ Health Perspect. 1994 Aug;102(8):680–688. doi: 10.1289/ehp.94102680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Herbst A. L., Ulfelder H., Poskanzer D. C. Adenocarcinoma of the vagina. Association of maternal stilbestrol therapy with tumor appearance in young women. N Engl J Med. 1971 Apr 15;284(15):878–881. doi: 10.1056/NEJM197104222841604. [DOI] [PubMed] [Google Scholar]
  15. Ho S. M., Danko D., Callard I. P. Effect of exogenous estradiol-17beta on plasma vitellogenin levels in male and female Chrysemys and its modulation by testosterone and progesterone. Gen Comp Endocrinol. 1981 Apr;43(4):413–421. doi: 10.1016/0016-6480(81)90224-0. [DOI] [PubMed] [Google Scholar]
  16. Ho S. M., Taylor S., Callard I. P. Effect of hypophysectomy and growth hormone on estrogen-induced vitellogenesis in the freshwater turtle, Chrysemys picta. Gen Comp Endocrinol. 1982 Oct;48(2):254–260. doi: 10.1016/0016-6480(82)90024-7. [DOI] [PubMed] [Google Scholar]
  17. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  18. Le Guellec K., Lawless K., Valotaire Y., Kress M., Tenniswood M. Vitellogenin gene expression in male rainbow trout (Salmo gairdneri). Gen Comp Endocrinol. 1988 Sep;71(3):359–371. doi: 10.1016/0016-6480(88)90264-x. [DOI] [PubMed] [Google Scholar]
  19. McBlain W. A. The levo enantiomer of o,p'-DDT inhibits the binding of 17 beta-estradiol to the estrogen receptor. Life Sci. 1987 Jan 12;40(2):215–221. doi: 10.1016/0024-3205(87)90361-4. [DOI] [PubMed] [Google Scholar]
  20. McKim J. M., Jr, Johnson K. L. Polychlorinated biphenyls and p,p'-DDE in Loggerhead and Green postyearling Atlantic sea turtles. Bull Environ Contam Toxicol. 1983 Jul;31(1):53–60. doi: 10.1007/BF01608766. [DOI] [PubMed] [Google Scholar]
  21. McLachlan J. A., Newbold R. R., Bullock B. Reproductive tract lesions in male mice exposed prenatally to diethylstilbestrol. Science. 1975 Dec 5;190(4218):991–992. doi: 10.1126/science.242076. [DOI] [PubMed] [Google Scholar]
  22. McLachlan J. A., Newbold R. R. Estrogens and development. Environ Health Perspect. 1987 Nov;75:25–27. doi: 10.1289/ehp.877525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Morales M. H., Osuna R., Sánchez E. Vitellogenesis in Anolis pulchellus: induction of VTG-like protein in liver explants from male and immature lizards. J Exp Zool. 1991 Oct;260(1):50–58. doi: 10.1002/jez.1402600107. [DOI] [PubMed] [Google Scholar]
  24. Pakdel F., Féon S., Le Gac F., Le Menn F., Valotaire Y. In vivo estrogen induction of hepatic estrogen receptor mRNA and correlation with vitellogenin mRNA in rainbow trout. Mol Cell Endocrinol. 1991 Mar;75(3):205–212. doi: 10.1016/0303-7207(91)90162-l. [DOI] [PubMed] [Google Scholar]
  25. Pelissero C., Flouriot G., Foucher J. L., Bennetau B., Dunoguès J., Le Gac F., Sumpter J. P. Vitellogenin synthesis in cultured hepatocytes; an in vitro test for the estrogenic potency of chemicals. J Steroid Biochem Mol Biol. 1993 Mar;44(3):263–272. doi: 10.1016/0960-0760(93)90086-c. [DOI] [PubMed] [Google Scholar]
  26. Riegel A. T., Aitken S. C., Martin M. B., Schoenberg D. R. Differential induction of hepatic estrogen receptor and vitellogenin gene transcription in Xenopus laevis. Endocrinology. 1987 Apr;120(4):1283–1290. doi: 10.1210/endo-120-4-1283. [DOI] [PubMed] [Google Scholar]
  27. Shapiro A. L., Viñuela E., Maizel J. V., Jr Molecular weight estimation of polypeptide chains by electrophoresis in SDS-polyacrylamide gels. Biochem Biophys Res Commun. 1967 Sep 7;28(5):815–820. doi: 10.1016/0006-291x(67)90391-9. [DOI] [PubMed] [Google Scholar]
  28. Sundararaj B. I., Nath P. Steroid-induced synthesis of vitellogenin in the catfish, Heteropneustes fossilis (Bloch). Gen Comp Endocrinol. 1981 Feb;43(2):201–210. doi: 10.1016/0016-6480(81)90313-0. [DOI] [PubMed] [Google Scholar]
  29. Tata J. R., Smith D. F. Vitellogenesis: a versatile model for hormonal regulation of gene expression. Recent Prog Horm Res. 1979;35:47–95. doi: 10.1016/b978-0-12-571135-7.50006-0. [DOI] [PubMed] [Google Scholar]
  30. Tata J. R. The expression of the vitellogenin gene. Cell. 1976 Sep;9(1):1–14. doi: 10.1016/0092-8674(76)90047-7. [DOI] [PubMed] [Google Scholar]
  31. Tousignant A., Crews D. Effect of exogenous estradiol applied at different embryonic stages on sex determination, growth, and mortality in the leopard gecko (Eublepharis macularius). J Exp Zool. 1994 Jan 1;268(1):17–21. doi: 10.1002/jez.1402680104. [DOI] [PubMed] [Google Scholar]
  32. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Vaillant C., Le Guellec C., Pakdel F., Valotaire Y. Vitellogenin gene expression in primary culture of male rainbow trout hepatocytes. Gen Comp Endocrinol. 1988 May;70(2):284–290. doi: 10.1016/0016-6480(88)90148-7. [DOI] [PubMed] [Google Scholar]
  34. Wahli W., Dawid I. B., Wyler T., Jaggi R. B., Weber R., Ryffel G. U. Vitellogenin in Xenopus laevis is encoded in a small family of genes. Cell. 1979 Mar;16(3):535–549. doi: 10.1016/0092-8674(79)90028-x. [DOI] [PubMed] [Google Scholar]
  35. Wake D. B. Declining amphibian populations. Science. 1991 Aug 23;253(5022):860–860. doi: 10.1126/science.253.5022.860. [DOI] [PubMed] [Google Scholar]
  36. Wangh L. J., Knowland J. Synthesis of vitellogenin in cultures of male and female frog liver regulated by estradiol treatment in vitro. Proc Natl Acad Sci U S A. 1975 Aug;72(8):3172–3175. doi: 10.1073/pnas.72.8.3172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wiley H. S., Opresko L., Wallace R. A. New methods for the purification of vertebrate vitellogenin. Anal Biochem. 1979 Aug;97(1):145–152. doi: 10.1016/0003-2697(79)90338-5. [DOI] [PubMed] [Google Scholar]

Articles from Environmental Health Perspectives are provided here courtesy of National Institute of Environmental Health Sciences

RESOURCES