17β-Estradiol Exposure Accelerates Skeletal Development in Xenopus laevis Tadpoles

Anatomical Record

Volumn 293, Issue 11, 2010, Pages 1880-1886

  Bauer Dantoin, Angela C ^a   Meinhardt, Daniel J ^a  

^a UNIVERSITY OF WISCONSIN GREEN BAY   (United States)

Author keywords

Bone; Development; Estradiol; Metamorphosis; Ossification; Skeleton; Xenopus laevis

Indexed keywords

ESTRADIOL;

ARTICLE; BONE; BONE DEVELOPMENT; CARTILAGE; FERTILIZATION; LARVAL STAGE; NONHUMAN; OSSIFICATION; PRIORITY JOURNAL; TADPOLE; XENOPUS LAEVIS;

ANIMALS; BONE AND BONES; BONE DEVELOPMENT; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; ESTROGENS; FEMALE; LARVA; MALE; OSTEOGENESIS; TIME FACTORS; XENOPUS LAEVIS;

AMPHIBIA; ANIMALIA; MAMMALIA; XENOPUS LAEVIS;

EID: 78049464038     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.21226     Document Type: Article

References (55)

1. Alford RA. 1999. Ecology, resource use, competition, and predation. In: McDiarmid, Altig editors. Tadpoles: The Biology of Anuran Larvae. Chicago: The University of Chicago Press.
2. Banu SK, Govindarajulu P, Aruldhas MM. 2002. Testosterone and estradiol differentially regulate TSH-induced thyrocyte proliferation in immature and adult rats. Steroids 67: 573-579.
3. Beber EH, Capelo LP, Fonseca TL, Costa CC, Lotfi CF, Scanlan TS, Gouveia CH. 2009. The thyroid hormone receptor (TR) beta receptor agonist GC-1 inhibits proliferation but induces differentiation and TR beta mRNA expression in mouse and rat osteoblast-like cells. Calcif Tissue Int 84: 324-333.
4. Budy AM, Urist MR, McLean FC. 1952. The effect of estrogens on the growth apparatus of the bones of immature rats. Am J Pathol 28: 1143-1153.
5. Chagin AS, Chrysis D, Takigawa M, Ritzen EM, Savendahl L. 2006. Locally produced estrogen promotes fetal rat metatarsal bone growth; an effect mediated through increased chondrocyte proliferation and decreased apoptosis. J Endocrinol 188: 193-203.
6. Chagin AS, Karimian E, Zaman F, Takigawa M, Chrysis D, Savendahl L. 2007. Tamoxifen induces permanent growth arrest through selective induction of apoptosis in growth plate chondrocytes in cultured rat metatarsal bones. Bone 40: 1415-1424.
7. Colborn T, Dumanoski D, Meyers JP. 1996. Our stolen future: are we threatening our fertility, intelligence, and survival?-A scientific detective story. New York: Dutton Publishing.
8. Cutler GB, Jr. 1997. The role of estrogen in bone growth and maturation during childhood and adolescence. J Steroid Biochem Mol Biol 61: 141-144.
9. Dodd MHI, Dodd JM. 1976. The biology of metamorphosis. In: Lofts B, editor.Physiology of the Amphibia, Vol. 3. New York: Academic Press.
10. Etheridge AL, Richter SMA. 2005. Rearing and Breeding the African Clawed Frog. Fort Atkinson, WI: Nasco.
11. Grumbach MM. 2000. Estrogen, bone, growth and sex: a sea change in conventional wisdom. J Pediatr Endocrinol Metab 13 (suppl 6): 1430-1455.
12. Gruning T, Zophel K, Wunderlich G, Franke WG. 2007. Influence of female sex hormones on thyroid parameters determined in a thyroid screening. Clin Lab 53: 547-553.
13. Hanken J, Hall BK. 1988. Skull development during anuran metamorphosis: II. Role of thyroid hormone in osteogenesis. Anat Embryol 178: 219-227.
14. Hanken J, Summers CH. 1988. Skeletal development during anuran metamorphosis: III. Role of thyroid hormone in chondrogenesis. J Exp Zool 246: 156-170.
15. Hayes TB. 2005. Welcome to the revolution: integrative biology and assessing the impact of endocrine disruptors on environmental and public health. Integr Comp Biol 45: 321-329.
16. Huang H, Brown DD. 2000. Overexpression of Xenopus laevis growth hormone stimulates growth of tadpoles and frogs. Proc Natl Acad Sci USA 97: 190-194.
17. Johnson KE, Knopper LD, Schneider DC, Ollson CA, Reimer KJ. 2009. Effects of local point source polychlorinated biphenyl (PCB) contamination on bone mineral density in deer mice (Peromyscus maniculatus). Sci Total Environ 407: 5050-5055.
18. Laue L, Kenigsberg D, Pescovitz OH, Hench KD, Barnes KM, Loriaux DL, Cutler GB, Jr. 1989. Treatment of familial male precocious puberty with spironolactone and testolactone. N Engl J Med 320: 496-502.
19. Li L, Andersen ME, Heber S, Zhang Q. 2007. Non-monotonic dose-response relationship in steroid hormone receptor-mediated gene expression. J Mol Endocrinol 38: 569-585.
20. Lima LP, Barros IA, Lisboa PC, Araujo RL, Silva AC, Rosenthal D, Ferreira AC, Carvalho DP. 2006. Estrogen effects on thyroid iodide uptake and thyroperoxidase activity in normal and ovariectomized rats. Steroids 71: 653-659.
21. Lindberg MK, Alatalo SL, Halleen JM, Mohan S, Gustafsson JA, Ohlsson C. 2001. Estrogen receptor specificity in the regulation of the skeleton in female mice. J Endocrinol 171: 229-236.
22. Lindsay R, Hart DM, Clark DM. 1984. The minimum effective dose of estrogen for prevention of postmenopausal bone loss. Obstet Gynecol 63: 759-763.
23. Manolagas SC, Kousteni S, Jilka RL. 2002. Sex Steroids and Bone. Recent Prog Horm Res 57: 385-409.
24. Mauras N, Rogol AD, Veldhuis JD. 1990. Increased hGH production rate after low-dose estrogen therapy in prepubertal girls with Turner's syndrome. Pediatr Res 28: 626-630.
25. Markey CM, Michaelson CL, Veson EC, Sonnenschein C, Soto AM. 2001. The mouse uterotrophic assay: a reevaluation of its validity in assessing the estrogenicity of bisphenol A. Environ Health Perspect 109: 55-60.
26. Metzger DL, Kerrigan JR. 1993. Androgen receptor blockade with flutamide enhances growth hormone secretion in late pubertal males: evidence for independent actions of estrogen and androgen. J Clin Endocrinol Metab 76: 1147-1152.
27. Metzger DL, Kerrigan JR. 1994. Estrogen receptor blockade with tamoxifen diminishes growth hormone secretion in boys: evidence for a stimulatory role of endogenous estrogens during male adolescence. J Clin Endocrinol Metab 79: 513-518.
28. Migliaccio S, Newbold RR, Bullock BC, McLachlan JA, Korach KS. 1992. Developmental exposure to estrogens induces persistent changes in skeletal tissue. Endocrinology 130: 1756-1758.
29. Miller SC, Bowman BM. 1981. Medullary bone osteogenesis following estrogen administration to mature male Japanese quail. Dev Biol 87: 52-63.
30. Morishima A, Grumsbach MM, Simpson ER, Fisher C, Qin K. 1995. Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of estrogens. Clin Endocrinol Metab 80: 3689-3698.
31. Nieuwkoop PD, Faber J. 1967. Normal Stable of Xenopus laevis (Daudin). 2nd ed. Amsterdam: North Holland Publ. Co.
32. Nilsson O, Chrysis D, Pajulo O, Boman A, Holst M, Rubinstein J, Martin Ritzen E, Savendahl L. 2003. Localization of estrogen receptors-α and -β and androgen receptor in the human growth plate at different pubertal stages. J Endocrinol 177: 319-326.
33. Nilsson O, Marino R, De Luca F, Phillip M, Baron J. 2005. Endocrine regulation of the growth plate. Horm Res 64: 157-165.
34. Ostadalova I. 1976. The effect of single dose of oestrogens administered during the early postnatal period on the DNA content of rat bone epiphyses. Physiol Bohemoslov 25: 97-102.
35. Ramajayam G, Sridhar M, Karthikeyan S, Lavanya R, Veni S, Vignesh RC, Ilangovan R, Djody SS, Gopalakrishnan V, Arunakaran J, Srinivasan N. 2007. Effects of Aroclor 1254 on femoral bone metabolism in adult male Wistar rats. Toxicology 241: 99-105.
36. Riggs BL, Khosla S, Melton LJ, III. 2002. Sex steroids and the construction and conservation of the adult skeleton. Endocrinol Rev 23: 279-302.
37. 35S]sulfate by cartilage of Xenopus laevis tadpoles. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 117: 317-322.
38. Shah N, Evans WS, Veldhuis JD. 1999. Actions of estrogen on pulsatile, nyctohemeral, and entropic modes of growth hormone secretion. Am J Physiol Regul Integr Comp Physiol 276: R1351-R1358.
39. Shao YY, Wang L, Ballock RT. 2006. Thyroid bone and the growth plate. Rev Endocr Metab Disord 7: 265-271.
40. Shareef A, Angove JM, Wells JD, Johnson BB. 2006. Aqueous solubilities of estrone, 17β-estradiol, 17α-ethynylestradiol, and bisphenol A. J Chem Eng Data 51: 879-881.
41. Smith EP, Boyd J, Frank GR, Takahashi H, Cohen RM, Specker B, Williams TC, Lubahn DB, Korach KS. 1994. Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N engl J Med 331: 1056-1061.
42. Takano H, Aizawa T, Irie T, Itoi E, Kokubun S, Roach HI. 2008. Normal bone growth requires optimal estrogen levels: negative effects of both high and low dose estrogen on the number of growth plate chondrocytes. Tohoku J Exp Med 214: 269-280.
43. Tsukamoto Y, Ishihara Y, Miyagawa-Tomita S, Hagiwara H. 2004. Inhibition of ossification in vivo and differentiation of osteoblasts in vitro by tributylin. Biochem Pharmacol 68: 739-746.
44. Trueb L, Hanken J. 1992. Skeletal development in Xenopus laevis (Anura: Pipidae). J Morphol 214: 1-41.
45. Turner RT, Riggs LB, Spelsberg TC. 1994. Skeletal Effects of Estrogen. Endocrinol Rev 15: 275-300.
46. Turner RT, Vandersteenhoven JJ, Bell NH. 1987. The effects of ovariectomy and 17β-estradiol on cortical bone histomorphometry in male and female rats. J Bone Miner Res 2: 115-122.
47. Venken K, Schuit F, Van Lommel L, Tsukamoto K, Kopchick JJ, Coschigano K, Ohlsson C, Moverare S, Boonen S, Bouillon R, Vanderschueren D. 2005. Growth without growth hormone receptor: estradiol is a major growth hormone-independent regulator of hepatic IGF-1 synthesis. J Bone Miner Res 20: 2138-2149.
48. Warner KE, Jenkins JJ. 2007. Effects of 17α-ethinylestradiol and bisphenol A on vertebral development in the fathead minnow (Pimephales promelas). Environ Toxicol Chem 26: 732-737.
49. Wassersug RJ. 1976. A procedure for differential staining of cartilage and bone in whole formalin-fixed vertebrates. Stain Technol 51: 131-134.
50. Weise M, De-Levi S, Barnes KM, Gafni RI, Abad V, Baron J. 2001. Effects of estrogen on growth plate senescence and epiphyseal fusion. Proc Natl Acad Sci USA 98: 6871-6876.
51. Welshons WV, Thayer KA, Judy BM, Taylor JA, Curran EM, vom Saal FM. 2003. Large effects from small exposures. I. Mechanisms for endocrine disrupting chemicals with estrogenic activity. Environ Health Perspect 111: 994-1006.
52. White BA, Nicoll CS. 1981. Hormonal control of amphibian metamorphosis. In: Gilbert LI, Frieden E, editors. Metamorphosis: A Problem in Developmental Biology. New York: Plenum Press. pp 363-396.
53. Wiren KM, Chapman Evans A, Zhan X-W. 2002. Osteoblast differentiation influences androgen and estrogen receptor-α and -β expression. J Endocrinol 175: 683-694.
54. Yilmaz B, Seyran AD, Sandal S, Aydin M, Colakoglu N, Kocer M, Carpenter DO. 2006. Modulatory effects of Aroclor 1221 and 1254 on bone turnover and vertebral histology in intact and ovariectomized rats. Toxicol Lett 166: 276-284.
55. Zsarnovszky A, Le HH, Wang HS, Belcher S. 2005. Ontogeny of rapid estrogen-mediated extracellular signal-regulated kinase signaling in the rat cerebellar cortex: potent nongenomic agonist and endocrine disrupting activity of the xenoestrogen bisphenol A. Endocrinology 146: 5388-5396.