Disrupted Oogenesis in the Frog Xenopus tropicalis after Exposure to Environmental Progestin Concentrations

Biology of Reproduction

Volumn 86, Issue 4, 2012, Pages

  Säfholm, Moa ^a   Norder, Anna ^a   Fick, Jerker ^b   Berg, Cecilia ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

Amphibians; Endocrine disruption; Levonorgestrel; Meiosis; Oocyte development; Pharmaceuticals; Reproductive toxicology; Vitellogenesis

Indexed keywords

LEVONORGESTREL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FEMALE; HEALTH STATUS; HISTOPATHOLOGY; MEIOSIS; NONHUMAN; OOCYTE DEVELOPMENT; OOCYTE MATURATION; PRIORITY JOURNAL; PROPHASE; TISSUE STRUCTURE; VITELLOGENESIS; WATER CONTAMINATION; XENOPUS TROPICALIS;

AMPHIBIA; ANURA; XENOPUS TROPICALIS;

EID: 84875079683     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.111.097378     Document Type: Article

References (72)

1. Jobling S, Nolan M, Tyler CR, Brighty G, Sumpter JP. Widespread sexual disruption in wild fish. Environ Sci Technol 1998; 32:2498-2506.
2. Reeder AL, Foley GL, Nichols DK, Hansen LG, Wikoff B, Faeh S, Eisold J, Wheeler MB, Warner R, Murphy JE, Beasley VR. Forms and prevalence of intersexuality and effects of environmental contaminants on sexuality in cricket frogs (Acris crepitans). Environ Health Perspect 1998; 106:261-266.
3. Hayes T, Haston K, Tsui M, Hoang A, Haeffele C, Vonk A. Herbicides: feminization of male frogs in the wild. Nature 2002; 419:895-896.
4. Jobling S, Beresford N, Nolan M, Rodgers-Gray T, Brighty GC, Sumpter JP, Tyler CR. Altered sexual maturation and gamete production in wild roach (Rutilus rutilus) living in rivers that receive treated sewage effluents. Biol Reprod 2002; 66:272-281.
5. Noaksson E, Linderoth M, Bosveld ATC, Norrgren L, Zebühr Y, Balk L. Endocrine disruption in brook trout (Salvelinus fontinalis) exposed to leachate from a public refuse dump. Sci Total Environ 2003; 305:87-103.
6. Woodling JD, Lopez EM, Maldonado TA, Norris DO, Vajda AM. Intersex and other reproductive disruption of fish in wastewater effluent dominated Colorado streams. Comp Biochem Physiol C Toxicol Pharmacol 2006; 144:10-15.
7. McDaniel TV, Martin PA, Struger J, Sherry J, Marvin CH, McMaster ME, Clarence S, Tetreault G. Potential endocrine disruption of sexual development in free ranging male northern leopard frogs (Rana pipiens) and green frogs (Rana clamitans) from areas of intensive row crop agriculture. Aquat Toxicol 2008; 88:230-242.
8. Bugel SM, White LA, Cooper KR. Impaired reproductive health of killifish (Fundulus heteroclitus) inhabiting Newark Bay, NJ, a chronically contaminated estuary. Aquat Toxicol 2010; 96:182-193.
9. Viglino L, Aboulfadl K, Prévost M, Sauvé S. Analysis of natural and synthetic estrogenic endocrine disruptors in environmental waters using online preconcentration coupled with LC-APPI-MS/MS. Talanta 2008; 76: 1088-1096.
10. Vulliet E, Wiest L, Baudot R, Grenier-Loustalot M. Multi-residue analysis of steroids at sub-ng/L levels in surface and ground-waters using liquid chromatography coupled to tandem mass spectrometry. J Chromatogr A 2008; 1210:84-91.
11. Fick J, Lindberg R, Parkkonen J, Arvidsson B, Tysklind M, Larsson D. Therapeutic levels of levonorgestrel detected in blood plasma of fish: results from screening rainbow trout exposed to treated sewage effluents. Environ Sci Technol 2010; 44:2661-2666.
12. Paulos P, Runnalls TJ, Nallani G, La Point T, Scott AP, Sumpter JP, Huggett DB. Reproductive responses in fathead minnow and Japanese medaka following exposure to a synthetic progestin, Norethindrone. Aquat Toxicol 2010; 99:256-262.
13. Zeilinger J, Steger-Hartmann T, Maser E, Goller S, Vonk R, Länge R. Effects of synthetic gestagens on fish reproduction. Environ Toxicol Chem 2010; 28:2663-2670.
14. Croxatto HB. Mechanisms that explain the contraceptive action of progestin implants for women. Contraception 2002; 65:21-27.
15. Sitruk-Ware R. Pharmacological profile of progestins. Maturitas 2004; 47: 277-283.
16. Erkkola R, Landgren BM. Role of progestins in contraception. Acta Obstet Gynecol Scand 2005; 84:207-216.
17. Lukola A, Punnonen R. Estrogen and progesterone receptors in human uterus and oviduct. J Endocrinol Invest 1983; 6:179-183.
18. Roy E, Wilson M, Kelley D. Estrogen-induced progestin receptors in the brain and pituitary of the South African clawed frog, Xenopus laevis. Neuroendocrinology 1986; 42:51-56.
19. Iwai T, Nanbu Y, Iwai M, Taii S, Fujii S, Mori T. Immunohistochemical localization of oestrogen receptors and progesterone receptors in the human ovary throughout the menstrual cycle. Virchows Arch A Pathol Anat Histopathol 1990; 417:369-375.
20. Slomczynska M, Krok M, Pierscinski A. Localization of the progesterone receptor in the porcine ovary. Acta Histochem 2000; 102:183-191.
21. Gava N, Clarke CL, Byth K, Arnett-Mansfield RL, deFazio A. Expression of progesterone receptors A and B in the mouse ovary during the estrous cycle. Endocrinology 2004; 145:3487-3494.
22. Anzaldúa SR, Camacho-Arroyo I, Reyna-Neyra A, Pérez-Marti{dotless}́nez M, Cerbón M. Regional differences in expression of progesterone receptor in oviduct and uterus of rabbit during early pregnancy. Comp Biochem Physiol A Mol Integr Physiol 2007; 147:685-690.
23. Josefsberg Ben-Yehoshua L, Lewellyn AL, Thomas P, Maller JL. The role of Xenopus membrane progesterone receptor b in mediating the effect of progesterone on oocyte maturation. Mol Endocrinol 2007; 21:664-673.
24. Brinton RD, Thompson RF, Foy MR, Baudry M, Wang J, Finch CE, Morgan TE, Pike CJ, Mack WJ, Stanczyk FZ, Nilsen J. Progesterone receptors: form and function in brain. Front Neuroendocrinol 2008; 29: 313-339.
25. Han Y, Feng HL, Sandlow JI, Haines CJ. Comparing expression of progesterone and estrogen receptors in testicular tissue from men with obstructive and nonobstructive azoospermia. J Androl 2009; 30:127-133.
26. Hanna RN, Zhu Y. Expression of membrane progestin receptors in zebrafish (Danio rerio) oocytes, testis and pituitary. Gen Comp Endocr 2009; 161:153-157.
27. Nutu M, Weijdegard B, Thomas P, Thurin-Kjellberg A, Billig H, Larsson DJ. Distribution and hormonal regulation of membrane progesterone receptors beta and gamma in ciliated epithelial cells of mouse and human fallopian tubes. Reprod Biol Endocrinol 2009; 7:89.
28. Hayes TB, Collins A, Lee M, Mendoza M, Noriega N, Stuart AA, Vonk A. Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc Natl Acad Sci U S A 2002; 99:5476-5480.
29. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues AS, Fischman DL, Waller RW. Status and trends of amphibian declines and extinctions worldwide. Science 2004; 306:1783-1786.
30. Pettersson I, Berg C. Environmentally relevant concentrations of ethynylestradiol cause female-biased sex ratios in Xenopus tropicalis and Rana temporaria. Environ Toxicol Chem 2007; 26:1005-1009.
31. Gyllenhammar I, Holm L, Eklund R, Berg C. Reproductive toxicity in Xenopus tropicalis after developmental exposure to environmental concentrations of ethynylestradiol. Aquat Toxicol 2009; 91:171-178.
32. Kvarnryd M, Grabic R, Brandt I, Berg C. Early life progestin exposure causes arrested oocyte development, oviductal agenesis and sterility in adult Xenopus tropicalis frogs. Aquat Toxicol 2011; 103:18-24.
33. Hammes SR. Steroids and oocyte maturation-a new look at an old story. Mol Endocrinol 2004; 18:769-775.
34. Zhang M, Ouyang H, Xia G. The signal pathway of gonadotrophinsinduced mammalian oocyte meiotic resumption. Mol Hum Reprod 2009; 15:399-409.
35. Al-Mukhtar KA, Webb AC. An ultrastructural study of primordial germ cells, oogonia and early oocytes in Xenopus laevis. J Embryol Exp Morphol 1971; 26:195-217.
36. Tyler CR, Sumpter JP. Oocyte growth and development in teleosts. Rev Fish Biol Fisher 1996; 6:287-318.
37. Ogielska M, Rozenblut B, Augustyńska R, Kotusz A. Degeneration of germ line cells in amphibian ovary. Acta Zool 2010; 91:319-327.
38. Miura C, Higashino T, Miura TA. Progestin and an estrogen regulate early stages of oogenesis in fish. Biol Reprod 2007; 77:822-828.
39. Kezele P, Skinner MK. Regulation of ovarian primordial follicle assembly and development by estrogen and progesterone: endocrine model of follicle assembly. Endocrinology 2003; 144:3329-3337.
40. Chen Y, Jefferson WN, Newbold RR, Padilla-Banks E, Pepling ME. Estradiol, progesterone, and genistein inhibit oocyte nest breakdown and primordial follicle assembly in the neonatal mouse ovary in vitro and in vivo. Endocrinology 2007; 148:3580-3590.
41. Nilsson EE, Skinner MK. Progesterone regulation of primordial follicle assembly in bovine fetal ovaries. Mol Cell Endocrinol 2009; 313:9-16.
42. Callard IP, Bayne CG, McConnell WF. Hormones and reproduction in the female lizard Sceloporus cyanogenys. Gen Comp Endocr 1972; 18: 175-194.
43. Schuetz AW, Wallace RA, Dumont JN. Steroid inhibition of protein incorporation by isolated amphibian oocytes. J Cell Biol 1974; 61:26-34.
44. Callard IP, Fileti LA, Perez LE, Sorbera LA, Giannoukos G, Klosterman LL, Paul T, Mccracken JA. Role of the corpus luteum and progesterone in the evolution of vertebrate viviparity. Am Zool 1992; 32:264-275.
45. Giannoukos G, Callard IP. Reptilian (Chrysemys picta) hepatic progesterone receptors: relationship to plasma steroids and the vitellogenic cycle. J Steroid Biochem Mol Biol 1995; 55:93-106.
46. Prisco M, Valiante S, Di Fiore M, Raucci F, Del Giudice G, Romano M, Laforgia V, Limatola E, Andreuccetti P. Effect of 17[beta]-estradiol and progesterone on vitellogenesis in the spotted ray Torpedo marmorata Risso 1810 (Elasmobranchii: Torpediniformes): studies on females and on estrogen-treated males. Gen Comp Endocr 2008; 157:125-132.
47. Guerriero G, Roselli CE, Ciarcia G. The amphibian (Rana esculenta) brain progesterone receptor: relationship to plasma steroids and vitellogenic cycle during the gonadal recovery phase. Ann N Y Acad Sci 2009; 1163: 407-409.
48. Kostellow AB, Morrill GA. Progesterone and subsequent polar metabolites are essential for completion of the first meiotic division in amphibian oocytes. Mol Cell Endocrinol 2008; 291:50-56.
49. Lutz LB, Cole LM, Gupta MK, Kwist KW, Auchus RJ, Hammes SR. Evidence that androgens are the primary steroids produced by Xenopus laevis ovaries and may signal through the classical androgen receptor to promote oocyte maturation. Proc Natl Acad Sci U S A 2001; 98: 13728-13733.
50. Liu Z, Patino R. High-affinity binding of progesterone to the plasma membrane of Xenopus oocytes: characteristics of binding and hormonal and developmental control. Biol Reprod 1993; 49:980-988.
51. Berg C, Gyllenhammar I, Kvarnryd M. Xenopus tropicalis as a test system for developmental and reproductive toxicity. J Toxicol Environ Health A 2009; 72:219-225.
52. Gyllenhammar I, Eriksson H, Söderqvist A, Lindberg RH, Fick J, Berg C. Clotrimazole exposure modulates aromatase activity in gonads and brain during gonadal differentiation in Xenopus tropicalis frogs. Aquat Toxicol 2009; 91:102-109.
53. Rasar M, Hammes S. The physiology of the Xenopus laevis ovary. Methods Mol Biol 2006; 322:17-30.
54. Kloas W, Lutz I. Amphibians as model to study endocrine disrupters. J Chromatogr A 2006; 1130:16-27.
55. Hausen P, Riebesell M. The Early Development of Xenopus laevis, an Atlas of the Histology. Berlin, Germany: Verlag der Zeitschrift für Naurforschung; 1991.
56. Chie EJ, Kostello AB, Morril GA. Progesterone induction of phospholipi methylation and arachidonic acid turnover during the first meiotic division in amphibian oocytes. Life Sci 1986; 39:1501-1508.
57. Bugel SM, White LA, Cooper KR. Decreased vitellogenin inducibility and 17beta-estradiol levels correlated with reduced egg production in killifish (Fundulus heteroclitus) from Newark Bay, NJ. Aquat Toxicol 2011; 105: 1-12.
58. Tucciarone LM, Lanclos KD. Endocytosis of yolk proteins by Xenopus laevis oocytes: kinetics of uptake of estrogen and gonadotropin-induced vitellogenins. Gen Comp Endocrinol 1982; 47:94-98.
59. Carnevali O, Mosconi G. In vitro induction of vitellogenin synthesis in Rana esculenta: role of the pituitary. Gen Comp Endocrinol 1992; 86: 352-358.
60. Carnevali O, Mosconi G, Yamamot, K, Kobayash, T, Kikuyam, S, Polzonetti-Magn, AM. Hormonal control of in vitro vitellogenin synthesis in Rana esculenta liver: effects of mammalian and amphibian growth hormone. Gen Comp Endocrinol 1992; 88:406-414.
61. Polzonetti-Magni AM, Mosconi G, Carnevali O, Yamamoto K, Hanaoka Y, Kikuyama S. Gonadotropins and reproductive function in the anuran amphibian, Rana esculenta. Biol Reprod 1998; 58:88-93.
62. Rouhani Rankouhi T, Sanderson JT, van Holsteijn I, van Kooten P, Bosveld ATC, van den Berg M. Effects of environmental and natural estrogens on vitellogenin production in hepatocytes of the brown frog (Rana temporaria). Aquat Toxicol 2005; 71:97-101.
63. Custodia-Lora N, Novillo A, Callard IP. Regulation of hepatic progesterone and estrogen receptors in the female turtle, Chrysemys picta: relationship to vitellogenesis. Gen Comp Endocrinol 2004; 136:232-240.
64. Lora NC, Novillo A, Callard IP. Synergistic role for pituitary growth hormone in the regulation of hepatic estrogen and progesterone receptors and vitellogenesis in female freshwater turtles, Chrysemys picta. Gen Comp Endocr 2005; 140:25-32.
65. Ö rn S, Andersson PL, Fö rlin L, Tysklind M, Norrgren L. The impact on reproduction of an orally administered mixture of selected PCBs in zebrafish (Danio rerio). Arch Environ Contam Toxicol 1998; 35:52-57.
66. van der Ven LT, Wester PW, Vos JG. Histopathology as a tool for the evaluation of endocrine disruption in zebrafish (Danio rerio). Environ Toxicol Chem 2003; 22:908-913.
67. King Heiden T, Carvan MJ, Hutz RJ. Inhibition of follicular development, vitellogenesis, and serum 17beta-estradiol concentrations in zebrafish following chronic, sublethal dietary exposure to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin. Toxicol Sci 2006; 90:490-499.
68. Foster WG, Hughes CL. Gene expression in oogenesis and implications for transgenerational effects of environmental toxicants. Biol Reprod 2011; 84:2-4.
69. Lawson C, Gieske M, Murdoch B, Ye P, Li Y, Hassold T, Hunt PA. Gene expression in the fetal mouse ovary is altered by exposure to low doses of bisphenol A. Biol Reprod 2011; 84:79-86.
70. Lynch LC, Blackburn DG. Effects of testosterone administration and gonadectomy on nuptial pad morphology in overwintering male leopard frogs, Rana pipiens. Amphibi Reptil 1995; 16:113-121.
71. Sitruk-Ware R. New progestagens for contraceptive use. Hum Reprod Update 2006; 12:169-178.
72. Kelley DB. Sexual differentiation in Xenopus laevis. In: Tinsley RC, Kobel HR (eds.), The Biology of Xenopus. Oxford: Clarendon Press; 1996:144-176.