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PMID: 14715905 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Phthalate-induced Leydig cell hyperplasia is associated with multiple endocrine disturbances.

Akingbemi BT, Ge R, Klinefelter GR, Zirkin BR, Hardy MP

Abstract

The possibility that exposures to environmental agents are associated with reproductive disorders in human populations has generated much public interest recently. Phthalate esters are used most commonly as plasticizers in the food and construction industry, and di-(2-ethylhexyl) phthalate (DEHP) is the most abundant phthalate in the environment. Daily human exposure to DEHP in the U.S. is significant, and occupational and clinical exposures from DEHP-plasticized medical devices, e.g., blood bags, hemodialysis tubing, and nasogastric feeding tubes, increase body burden levels. We investigated the effects of chronic exposures to low environmentally relevant DEHP levels on testicular function. Our data show that prolonged exposures to this agent induced high levels of the gonadotropin luteinizing hormone and increased the serum concentrations of sex hormones [testosterone and 17beta-estradiol (E2)] by >50%. Increased proliferative activity in Leydig cells was evidenced by enhanced expression of cell cycle proteins, as determined by RT-PCR. The numbers of Leydig cells in the testis of DEHP-treated rats were 40-60% higher than in control rats, indicating induction of Leydig cell hyperplasia. DEHP-induced elevations in serum testosterone and E2 levels suggest the possibility of multiple crosstalks between androgen, estrogen, and steroid hormone receptors, whereas the presence of estrogen receptors in nonreproductive tissues, e.g., cardiovascular system and bones, implies that the increases in serum E2 levels have implications beyond reproduction, including systemic physiology. Analysis of the effects of phthalate exposures on gonadotropin and steroid hormone levels should form part of overall risk assessment in human populations.

MeSH Terms
Animals Diethylhexyl Phthalate/analogs & derivatives,toxicity Endocrine System Diseases/chemically induced,physiopathology Estradiol/biosynthesis,blood Humans Hyperplasia Leydig Cells/drug effects,metabolism,pathology Luteinizing Hormone/biosynthesis Male Plasticizers/toxicity Rats Rats, Long-Evans Receptor Cross-Talk/drug effects Testis/drug effects,pathology Testosterone/biosynthesis,blood
Chemicals
Plasticizers Testosterone Estradiol Luteinizing Hormone Diethylhexyl Phthalate mono-(2-ethylhexyl)phthalate
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Akingbemi Benson T
Center for Biomedical Research, Population Council, New York, NY 10021, USA.
Ge Renshan
Klinefelter Gary R
Zirkin Barry R
Hardy Matthew P
References (40)
40 references, click to expand
  1. Regulation of the aromatase gene expression in mature rat Leydig cells.
    Mol Cell Endocrinol. 2001 Jun 10;178(1-2):141-6 PMID: 11403903
  2. High-performance liquid chromatographic method for the determination of di(2-ethylhexyl) phthalate in total parenteral nutrition and in plasma.
    J Chromatogr B Biomed Sci Appl. 2001 May 5;755(1-2):297-303 PMID: 11393717
  3. Oestrogenic and antiandrogenic chemicals in the environment: effects on male reproductive health.
    Ann Med. 2001 Sep;33(6):391-403 PMID: 11585100
  4. Altered gene profiles in fetal rat testes after in utero exposure to di(n-butyl) phthalate.
    Toxicol Sci. 2001 Dec;64(2):233-42 PMID: 11719706
  5. Biological role of estrogen and estrogen receptors.
    Crit Rev Biochem Mol Biol. 2002;37(1):1-28 PMID: 11905545
  6. Accelerated progression of asbestos-induced mesotheliomas in heterozygous p53+/- mice.
    Toxicol Sci. 2002 Aug;68(2):331-8 PMID: 12151629
  7. Reproductive disturbances, pituitary lactotrope adenomas, and mammary gland tumors in transgenic female mice producing high levels of human chorionic gonadotropin.
    Endocrinology. 2002 Oct;143(10):4084-95 PMID: 12239120
  8. Overexpression of human chorionic gonadotropin causes multiple reproductive defects in transgenic mice.
    Biol Reprod. 2003 Jul;69(1):338-46 PMID: 12672665
  9. Assessing human exposure to phthalates using monoesters and their oxidized metabolites as biomarkers.
    Environ Health Perspect. 2003 Jul;111(9):1148-51 PMID: 12842765
  10. Luteinizing hormone receptors and testosterone synthesis in two distinct populations of Leydig cells.
    Endocrinology. 1980 May;106(5):1424-9 PMID: 6244930
  11. Chromatographic separation and quantitative determination of the metabolites of di-(2-ethylhexyl) phthalate from urine of laboratory animals.
    J Chromatogr. 1982 Jul 23;244(1):65-79 PMID: 7119075
  12. Effect of luteinizing hormone on Leydig cell structure and testosterone secretion.
    Endocrinology. 1983 May;112(5):1763-9 PMID: 6403335
  13. A single gene and a pseudogene for the cellular tumour antigen p53.
    Nature. 1983 Dec 8-14;306(5943):594-7 PMID: 6646235
  14. Comparative pharmacokinetics and subacute toxicity of di(2-ethylhexyl) phthalate (DEHP) in rats and marmosets: extrapolation of effects in rodents to man.
    Environ Health Perspect. 1986 Mar;65:299-307 PMID: 3086078
  15. Inhibition of human platelet phospholipase A2 by mono(2-ethylhexyl)phthalate.
    Environ Health Perspect. 1988 Jun;78:179-83 PMID: 3203637
  16. Mono-2-ethylhexyl phthalate, a metabolite of di-(2-ethylhexyl) phthalate, causally linked to testicular atrophy in rats.
    Toxicol Appl Pharmacol. 1989 Sep 1;100(2):193-200 PMID: 2781553
  17. The primary structure of rat ribosomal protein S16.
    FEBS Lett. 1990 Apr 9;263(1):85-8 PMID: 2332055
  18. Early indicators for carcinogenesis in sex-hormone-sensitive organs.
    Mutat Res. 1991 Jun;248(2):341-56 PMID: 2046690
  19. Hormonal control of Leydig cell differentiation.
    Ann N Y Acad Sci. 1991;637:152-63 PMID: 1785769
  20. Cyclin G: a new mammalian cyclin with homology to fission yeast Cig1.
    Oncogene. 1993 Aug;8(8):2113-8 PMID: 8336937
  21. Targeted overexpression of luteinizing hormone in transgenic mice leads to infertility, polycystic ovaries, and ovarian tumors.
    Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1322-6 PMID: 7877975
  22. Genetic heterogeneity of constitutively activating mutations of the human luteinizing hormone receptor in familial male-limited precocious puberty.
    Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):1906-10 PMID: 7892197
  23. Hormonal factors in carcinogenesis of the prostate and testis in humans and in animal models.
    Prog Clin Biol Res. 1996;394:309-52 PMID: 8778804
  24. Gonadotropin gene modulation by steroids and gonadotropin-releasing hormone.
    Biol Reprod. 1996 Feb;54(2):279-86 PMID: 8788177
  25. Hepatocarcinogenic potential of di(2-ethylhexyl)phthalate in rodents and its implications on human risk.
    Crit Rev Toxicol. 1996 Jun;26(4):365-481 PMID: 8817083
  26. Testicular cancer: a review.
    Oncol Nurs Forum. 1996 Sep;23(8):1203-11; quiz 1212-3 PMID: 8883069
  27. Di(2-ethylhexyl) phthalate induces a functional zinc deficiency during pregnancy and teratogenesis that is independent of peroxisome proliferator-activated receptor-alpha.
    Teratology. 1997 Nov;56(5):311-6 PMID: 9451755
  28. Expression of D-type cyclins in normal and neoplastic rat pituitary.
    Endocrinology. 1998 Apr;139(4):2058-67 PMID: 9528994
  29. Receptor and nonreceptor-mediated organ-specific toxicity of di(2-ethylhexyl)phthalate (DEHP) in peroxisome proliferator-activated receptor alpha-null mice.
    Toxicol Pathol. 1998 Mar-Apr;26(2):240-6 PMID: 9547862
  30. Testicular seminoma in a patient with a constitutively activating mutation of the luteinizing hormone/chorionic gonadotropin receptor.
    Eur J Endocrinol. 1998 Jul;139(1):101-6 PMID: 9703386
  31. Inhibition of androgen receptor-dependent transcriptional activity by DDT isomers and methoxychlor in HepG2 human hepatoma cells.
    Toxicol Appl Pharmacol. 1998 Jul;151(1):135-42 PMID: 9705896
  32. Caspases: the proteases of the apoptotic pathway.
    Oncogene. 1998 Dec 24;17(25):3237-45 PMID: 9916986
  33. Administration of potentially antiandrogenic pesticides (procymidone, linuron, iprodione, chlozolinate, p,p'-DDE, and ketoconazole) and toxic substances (dibutyl- and diethylhexyl phthalate, PCB 169, and ethane dimethane sulphonate) during sexual differentiation produces diverse profiles of reproductive malformations in the male rat.
    Toxicol Ind Health. 1999 Jan-Mar;15(1-2):94-118 PMID: 10188194
  34. Effect of deprival of LH on Leydig cell proliferation: involvement of PCNA, cyclin D3 and IGF-1.
    Mol Cell Endocrinol. 2000 Apr 25;162(1-2):113-20 PMID: 10854704
  35. Identification of phthalate esters in the serum of young Puerto Rican girls with premature breast development.
    Environ Health Perspect. 2000 Sep;108(9):895-900 PMID: 11017896
  36. Effect of activating and inactivating mutations on the phosphorylation and trafficking of the human lutropin/choriogonadotropin receptor.
    Mol Endocrinol. 2000 Nov;14(11):1797-810 PMID: 11075813
  37. Hormones and testis development and the possible adverse effects of environmental chemicals.
    Toxicol Lett. 2001 Mar 31;120(1-3):221-32 PMID: 11323180
  38. Abnormalities of sexual development in male rats with in utero and lactational exposure to the antiandrogenic plasticizer Di(2-ethylhexyl) phthalate.
    Environ Health Perspect. 2001 Mar;109(3):229-37 PMID: 11333183
  39. Effects of phthalate esters on the developing reproductive tract of male rats.
    Hum Reprod Update. 2001 May-Jun;7(3):231-5 PMID: 11392369
  40. Modulation of rat Leydig cell steroidogenic function by di(2-ethylhexyl)phthalate.
    Biol Reprod. 2001 Oct;65(4):1252-9 PMID: 11566751
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2004-01-20
Epub
2004-00-08
Pages
775-80
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC321757
Subset
IM
Grants
NIEHS NIH HHS · R01 ES010233 · United States
NIEHS NIH HHS · ES 10233 · United States
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