Topical dose delivery in the reptilian egg treatment model

Environmental Toxicology and Chemistry

Volumn 26, Issue 5, 2007, Pages 914-919

  Muller, Jennifer K ^a   Gross, Timothy S ^b   Borgert, Christopher J ^a,b  

^a Applied Pharmacology and Toxicology Inc   (United States)

^b University of Florida   (United States)

Author keywords

Egg; In ovo exposure; Method validation; Reptile; Temperature dependent sex determination

Indexed keywords

BIOASSAY; ENDOCRINOLOGY; IMPURITIES; PHARMACOKINETICS;

EGGS; IN OVO EXPOSURE; METHOD VALIDATION; REPTILES; TEMPERATURE DEPENDENT SEX DETERMINATION;

TOXICITY;

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; ANDROGEN; ANTIANDROGEN; CHEMICAL COMPOUND; ESTRADIOL; ESTROGEN; GESTAGEN; POLYCHLORINATED BIPHENYL; PROGESTERONE; SEX HORMONE; TAMOXIFEN;

BIOASSAY; DOSE-RESPONSE RELATIONSHIP; EGG; ENDOCRINE DISRUPTOR; MODEL; POLLUTION EXPOSURE; REPTILE; SEX DETERMINATION; TEMPERATURE EFFECT; TOXICITY TEST;

CONCENTRATION RESPONSE; DOSE RESPONSE; EMBRYO MORTALITY; ENDOCRINE FUNCTION; HORMONE DETERMINATION; HORMONE RECEPTOR INTERACTION; INCUBATION TEMPERATURE; INFORMATION RETRIEVAL; NONHUMAN; PRENATAL EXPOSURE; PRENATAL SCREENING; PRIORITY JOURNAL; RADIOACTIVITY; REPTILE; REVIEW; SEX DETERMINATION; SEX DIFFERENCE; SEX RATIO; TEMPERATURE SENSITIVITY; TOXICOKINETICS;

ADMINISTRATION, TOPICAL; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCRINE DISRUPTORS; ENDOCRINE SYSTEM; ENVIRONMENTAL POLLUTANTS; GONADS; MODELS, BIOLOGICAL; OVUM; REPTILES; SEX DETERMINATION (ANALYSIS); SEX DIFFERENTIATION; TEMPERATURE; TREATMENT OUTCOME;

REPTILIA; SPONDIAS PURPUREA;

EID: 34249087711     PISSN: 07307268     EISSN: None     Source Type: Journal    
DOI: 10.1897/06-290R.1     Document Type: Review

References (94)

1. U.S. Environmental Protection Agency. 1998. Endocrine Disruptor Screening and Testing Advisory Committee (EDSTAC) Final Report. Washington, DC.
2. Bull JJ, Vogt RC. 1979. Temperature-dependent sex determination in turtles. Science 206:1186-1188.
3. Ewert MA, Nelson CE. 1991. Sex determination in turtles: Diverse patterns and some possible adaptive values. Copeia 1:50-69.
4. Wibbels T, Bull JJ, Crews D. 1991. Chronology and morphology of temperature-dependent sex determination. J Exp Zool 260:371-381.
5. Ferguson MWJ, Joanen T. 1983. Temperature-dependent sex determination in Alligator mississippiensis. J Zool 200:143-177.
6. Bull JJ, Vogt RC. 1981. Temperature-sensitive periods of sex determination in emydid turtles. J Exp Zool 218:435-440.
7. Pieau C, Dorizzi M. 1981. Determination of temperature-sensitive stages for sexual differentiation of the gonads in embryos of the turtle, Emys orbicularis. J Morphol 170:373-382.
8. Wibbels T, Bull JJ, Crews D. 1991. Synergism between temperature and estradiol: A common pathway in turtle sex determination? J Exp Zool 260:130-134.
9. Yntema CL. 1979. Temperature levels and periods of sex determination during incubation of eggs of Chelydra serpentina. J Morphol 159:17-28.
10. Davenport J. 1997. Temperature and the life-history strategies of sea turtles. J Therm Biol 22:479-488.
11. Lang JW, Andrews HJ. 1994. Temperature-dependent sex determination in crocodilians. J Exp Zool 270:28-44.
12. Smith CA, Elf PK, Lang JW, Joss JM. 1995. Aromatase enzyme activity during gonadal sex differentiation in alligator embryos. Differentiation 58:281-290.
13. Gutzke WH, Bull JJ. 1986. Steroid hormones reverse sex in turtles. Gen Comp Endocrinol 64:368-372.
14. Bull JJ, Gutzke WH, Crews D. 1988. Sex reversal by estradiol in three reptilian orders. Gen Comp Endocrinol 70:425-428.
15. Crews D, Wibbels T, Gutzke WH. 1989. Action of sex steroid hormones on temperature-induced sex determination in the snapping turtle (Chelydra serpentina). Gen Comp Endocrinol 76:159-166.
16. Crews D, Bull JJ, Wibbels T. 1991. Estrogen and sex reversal in turtles: A dose-dependent phenomenon. Gen Comp Endocrinol 81:357-364.
17. Crews D, Bergeron JM, McLachlan JA. 1995. The role of estrogen in turtle sex determination and the effect of PCBs. Environ Health Perspect 103 (Suppl. 7):73-77.
18. Crews D, Cantu AR, Rhen T, Vohra R. 1996. The relative effectiveness of estrone, estradiol-17β, and estriol in sex reversal in the red-eared slider (Trachemys scripta), a turtle with temperature-dependent sex determination. Gen Comp Endocrinol 102:317-326.
19. Wibbels T, Bull JJ, Crews D. 1992. Steroid hormone-induced male sex determination in an amniotic vertebrate. J Exp Zool 262:454-457.
20. Wibbels T, Gideon P, Bull JJ, Crews D. 1993. Estrogen- and temperature-induced medullary cord regression during gonadal differentiation in a turtle. Differentiation 53:149-154.
21. Lance VA, Bogart MH. 1992. Disruption of ovarian development in alligator embryos treated with an aromatase inhibitor. Gen Comp Endocrinol 86:59-71.
22. Wibbels T, Crews D. 1992. Specificity of steroid hormone-induced sex determination in a turtle. J Endocrinol 133:121-129.
23. Wibbels T, Crews D. 1995. Steroid-induced sex determination at incubation temperatures producing mixed sex ratios in a turtle with TSD. Gen Comp Endocrinol 100:53-60.
24. Tousignant A, Crews D. 1994. Effect of exogenous estradiol applied at different embryonic stages on sex determination, growth, and mortality in the leopard gecko (Eublepharis macularius). J Exp Zool 268:17-21.
25. Crain DA, Guillette LJJ, Rooney AA, Pickford DB. 1997. Alterations in steroidogenesis in alligators (Alligator mississippiensis) exposed naturally and experimentally to environmental contaminants. Environ Health Perspect 105:528-533.
26. Bergeron JM, Willingham E, Osborn CT, Rhen T, Crews D. 1999. Developmental synergism of steroidal estrogens in sex determination. Environ Health Perspect 107:93-97.
27. Sheehan DM, Willingham E, Gaylor D, Bergeron JM, Crews D. 1999. No threshold dose for estradiol-induced sex reversal of turtle embryos: How little is too much? Environ Health Perspect 107:155-159.
28. Spiteri ID, Guillette LJ Jr, Crain DA. 1999. The functional and structural observations of the neonatal reproductive system of alligators exposed in ovo to atrazine, 2,4-D, or estradiol. Toxicol Ind Health 15:180-185.
29. Stoker C, Rey F, Rodriguez H, Ramos JG, Sirosky P, Larriera A, Luque EH, Munoz-De Toro M. 2003. Sex reversal effects on Caiman latirostris exposed to environmentally relevant doses of the xenoestrogen bisphenol A. Gen Comp Endocrinol 133:287-296.
30. Milnes MR, Bryan TA, Medina JG, Gunderson MP, Guillette LJ Jr. 2005. Developmental alterations as a result of in ovo exposure to the pesticide metabolite p,p′-DDE in Alligator mississippiensis. Gen Comp Endocrinol 144:257-263.
31. Rhen T, Lang JW. 1994. Temperature-dependent sex determination in the snapping turtle: Manipulation of the embryonic sex steroid environment. Gen Comp Endocrinol 96:243-254.
32. Crews D, Cantu AR, Bergeron JM. 1996. Temperature and non-aromatizable androgens: A common pathway in male sex determination in a turtle with temperature-dependent sex determination? J Endocrinol 149:457-463.
33. Crews D, Bergeron JM. 1994. Role of reductase and aromatase in sex determination in the red-eared slider (Trachemys scripta), a turtle with temperature-dependent sex determination. J Endocrinol 143:279-289.
34. Dorizzi M, Richard-Mercier N, Desvages G, Girondot M, Pieau C. 1994. Masculinization of gonads by aromatase inhibitors in a turtle with temperature-dependent sex determination. Differentiation 58:1-8.
35. Wibbels T, Crews D. 1994. Putative aromatase inhibitor induces male sex determination in a female unisexual lizard and in a turtle with temperature-dependent sex determination. J Endocrinol 141:295-299.
36. Richard-Mercier N, Dorizzi M, Desvages G, Girondot M, Pieau C. 1995. Endocrine sex reversal of gonads by the aromatase inhibitor letrozole (CGS 20267) in Emys orbicularis, a turtle with temperature-dependent sex determination. Gen Comp Endocrinol 100:314-326.
37. Fleming A, Crews D. 2001. Estradiol and incubation temperature modulate regulation of steroidogenic factor 1 in the developing gonad of the red-eared slider turtle. Endocrinology 142:1403-1411.
38. Murdock C, Wibbels T. 2003. Cloning and expression of aromatase in a turtle with temperature-dependent sex determination. Gen Comp Endocrinol 130:109-119.
39. Crews D, Fleming A, Willingham E, Baldwin R, Skipper JK. 2001. Role of steroidogenic factor 1 and aromatase in temperature-dependent sex determination in the red-eared slider turtle. J Exp Zool 290:597-606.
40. White RB, Thomas P. 1992. Adrenal-kidney and gonadal steroidogenesis during differentiation of a reptile with temperature-dependent sex determination. Gen Comp Endocrinol 88:10-19.
41. Jeyasuria P, Place AR. 1998. Embryonic brain-gonadal axis in temperature-dependent sex determination of reptiles: A role for P450 aromatase (CYP19). J Exp Zool 281:428-429.
42. Salame-Mendez A, Herrera-Munoz J, Moreno-Mendoza N, Merchant-Larios H. 1998. Response of diencephalons but not the gonad to female-producing temperature with elevated estradiol levels in the sea turtle Lepidochelys olivacea. J Exp Zool 280:304-313.
43. Spotila LD, Spotila JR, Hall SE. 1998. Sequence and expression of analysis of WT1 and Sox9 in the red-eared slider turtle, Trachemys scripta. J Exp Zool 281:417-427.
44. Fleming A, Wibbels T, Skipper JK, Crews D. 1999. Developmental expression of steroidogenic factor 1 in a turtle with temperature-dependent sex determination. Gen Comp Endocrinol 116:336-346.
45. Western PS, Harry JL, Graves JA, Sinclair AH. 1999. Temperature-dependent sex determination: Upregulation of SOX9 expression after commitment to male development. Dev Dyn 214:171-177.
46. Western PS, Harry JL, Graves JA, Sinclair AH. 1999. Temperature-dependent sex determination in the American alligator: AMH precedes SOX9 expression. Dev Dyn 216:411-419.
47. Kettlewell JR, Raymond CS, Zarkower D. 2000. Temperature-dependent expression of turtle Dmrt1 prior to sexual differentiation. Genesis 26:174-178.
48. Western PS, Harry JL, Marshall-Graves JA, Sinclair AH. 2000. Temperature-dependent sex determination in the American alligator: Expression of SF1, WT1, and DAX1 during gonadogenesis. Gene 241:223-232.
49. Gabriel WN, Blumberg B, Sutton S, Place AR, Lance VA. 2001. Alligator aromatase cDNA sequence and its expression in embryos at male and female incubation temperatures. J Exp Zool 290:439-448.
50. Schmahl J, Yao HH, Pierucci-Alves F, Capel B. 2003. Colocalization of WT1 and cell proliferation reveals conserved mechanisms in temperature-dependent sex determination. Genesis 35:193-201.
51. Vonier PM, Crain DA, McLachlan JA, Guillette LJ Jr, Arnold SF. 1996. Interaction of environmental chemicals with the estrogen and progesterone receptors from the oviduct of the American alligator. Environ Health Perspect 104:1318-1322.
52. Portelli MJ, de Solla SR, Brooks RJ, Bishop CA. 1999. Effect of dichlorodiphenyltrichloroethane on sex determination of the common snapping turtle (Chelydra serpentina). Ecotoxicol Environ Saf 43:284-291.
53. Gale RW, Bergeron JM, Willingham EJ, Crews D. 2002. Turtle sex determination assay: Mass balance and responses to 2,3,7,8-tetrachlorodibenzo- p-dioxin and 3,3′,4,4′,5-pentachlorobiphenyl. Environ Toxicol Chem 21:2477-2482.
54. Bowden RM, Ewert MA, Nelson CE. 2000. Environmental sex determination in a reptile varies seasonally and with yolk hormones. Proc R Soc Lond B Biol Sci 267:1745-1749.
55. Elf PK, Lang JW, Fivizzani AJ. 2002. Dynamics of yolk steroid hormones during development in a reptile with temperature-dependent sex determination. Gen Comp Endocrinol 127:34-39.
56. Muller JK, Gross TS, Borgert CJ. 2007. Dose verification following topical treatment of alligator eggs. Environ Toxicol Chem 26:908-913.
57. Podreka S, Georges A, Maher B, Limpus CJ. 1998. The environmental contaminant DDE fails to influence the outcome of sexual differentiation in the marine turtle Chelonia mydas. Environ Health Perspect 106:185-188.
58. Matter JM, McMurry CS, Anthony AB, Dickerson RL. 1998. Development and implementation of endocrine biomarkers of exposure and effects in American alligators (Alligator mississippiensis). Chemosphere 37:1905-1914.
59. Milnes MR, Allen D, Bryan TA, Sedacca CD, Guillette LJ Jr. 2004. Developmental effects of embryonic exposure to toxaphene in the American alligator (Alligator mississippiensis). Comp Biochem Physiol C Toxicol Pharmacol 138:81-87.
60. Lance VA, Bogart MH. 1991. Tamoxifen 'sex reverses' alligator embryos at male producing temperature, but is an antiestrogen in female hatchlings. Experientia 47:263-266.
61. Crews D, Cantu AR, Bergeron JM, Rhen T. 1995. The relative effectiveness of androstenedione, testosterone, and estrone, precursors to estradiol, in sex reversal in the red-eared slider (Trachemys scripta), a turtle with temperature-dependent sex determination. Gen Comp Endocrinol 100:119-127.
62. Willingham E. 2004. Endocrine-disrupting compounds and mixtures: Unexpected dose-response. Arch Environ Contam Toxicol 46:265-269.
63. Bergeron JM, Crews D, McLachlan JA. 1994. PCBs as environmental estrogens: Turtle sex determination as a biomarker of environmental contamination. Environ Health Perspect 102:780-781.
64. Willingham E, Crews D. 1999. Sex reversal effects of environmentally relevant xenobiotic concentrations on the red-eared slider turtle, a species with temperature-dependent sex determination. Gen Comp Endocrinol 113:429-435.
65. Willingham E, Baldwin R, Skipper JK, Crews D. 2000. Aromatase activity during embryogenesis in the brain and adrenal-kidney-gonad of the red-eared slider turtle, a species with temperature-dependent sex determination. Gen Comp Endocrinol 119:202-207.
66. Willingham E. 2001. Embryonic exposure to low-dose pesticides: Effects on growth rate in the hatchling red-eared slider turtle. J Toxicol Environ Health A 64:257-272.
67. Somers J, Moran ET Jr, Reinhart BS, Stephenson GR. 1974. Effect of external application of pesticides to the fertile egg on hatching success and early chick performance. 1. Preincubation spraying with DDT and commercial mixtures of 2,4-D:picloram and 2,4-D:2,4,5-T. Bull Environ Contam Toxicol 11:33-38.
68. Somers J, Moran ET Jr, Reinhart BS. 1974. Effect of external application of pesticides to the fertile egg on hatching success and early chick performance. 2. Commercial-herbicide mixtures of 2,4-D with picloram or 2,4,5-T using the pheasant. Bull Environ Contam Toxicol 11:339-342.
69. Somers JD, Moran ET Jr, Reinhart BS. 1974. Effect of external application of pesticides to the fertile egg on hatching success and early chick performance. 3. Consequences of combining 2,4-D with picloram and extremes in contamination. Bull Environ Contam Toxicol 11:511-516.
70. Somers JD, Moran ET Jr, Reinhart BS. 1978. Reproductive success of hens and cockerels originating from eggs sprayed with 2,4-D, 2,4-5-T, and picloram followed by early performance of their progeny after a comparable in ovo exposure. Bull Environ Contam Toxicol 20:111-119.
71. Somers JD, Moran ET Jr, Reinhart BS. 1978. Influence of hen dietary calcium and phosphorus on the integrity of the egg shell as it would influence hatching success and the consequences of preincubation 2,4,5-T spraying with and without a high TCDD level. Bull Environ Contam Toxicol 19:648-654.
72. Somers JD, Moran ET, Reinhart BS. 1978. Hatching success and early performance of chicks from eggs sprayed with 2,4-D, 2,4,5-T, and picloram at various stages of embryonic development. Bull Environ Contam Toxicol 20:289-293.
73. Hoffman DJ, Eastin WC Jr. 1981. Effects of malathion, diazinon, and parathion on mallard embryo development and Cholinesterase activity. Environ Res 26:472-485.
74. Hoffman DJ, Eastin WC Jr. 1982. Effects of lindane, paraquat, toxaphene, and 2,4,5-trichlorophenoxyacetic acid on mallard embryo development. Arch Environ Contam Toxicol 11:79-86.
75. Hoffman DJ, Albers PH. 1984. Evaluation of potential embryotoxicity and teratogenicity of 42 herbicides, insecticides, and petroleum contaminants to mallard eggs. Arch Environ Contam Toxicol 13:15-27.
76. Hoffman DJ, Sileo L. 1984. Neurotoxic and teratogenic effects of an organophosphorous insecticide (phenyl phosphonothioic acid-O-ethyl-O-[4-nitrophenyl] ester) on mallard development. Toxicol Appl Pharmacol 73:284-294.
77. Castro de Cantarmi SM, Evangelista de Duffard AM, Duffard RO. 1989. Penetration studies and residue determinations of 2,4-dichlorophenoxyacetic acid butyl ester in fertile hen eggs and chicks hatched from treated eggs. Drug Chem Toxicol 12:137-146.
78. Sewalk CJ, Brewer GL, Hoffman DJ. 2001. Effects of diquat, an aquatic herbicide, on the development of mallard embryos. J Toxicol Environ Health A 62:33-45.
79. Buscemi DM, Hoffman DJ, Vyas NB, Spann JW, Kuenzel WJ. 2002. Effects of Phos-Chek G75-F and Silv-Ex on developing northern bobwhite quail (Colinus virginianus). Arch Environ Contam Toxicol 43:330-337.
80. Albers PH, Hoffman DJ, Buscemi DM, Melancon MJ. 2003. Effects of the mosquito larvicide GB-1111 on red-winged blackbird embryos. Environ Pollut 125:447-451.
81. Hoffman DJ, Albers PH, Melancon MJ, Miles AK. 2004. Effects of the mosquito larvicide GB-1111 on bird eggs. Environ Pollut 127:353-358.
82. Keseru M, Budai P, Varnagy L, Szabo R, Juhasz E, Babinszky G, Pongracz A. 2004. Teratogenicity study of some pesticides in chicken embryos. Communications in Agricultural and Applied Biological Sciences 69:803-806.
83. Mayne GJ, Bishop CA, Martin PA, Boermans HJ, Hunter B. 2005. Thyroid function in nestling tree swallows and eastern bluebirds exposed to non-persistent pesticides and p,p′-DDE in apple orchards of southern Ontario, Canada. Ecotoxicology 14:381-396.
84. Marburger JE, Johnson WE, Gross TS, Douglas DR, Di J. 2002. Residual organochlorine pesticides in soils and fish from wetland restoration areas in Central Florida, USA. Wetlands 22:705-711.
85. Rauschenberger RH, Sepulveda MS, Wiebe JJ, Szabo NJ, Gross TS. 2004. Predicting maternal body burdens of organochlorine pesticides from eggs and evidence of maternal transfer in Alligator mississippiensis. Environ Toxicol Chem 23:2906-2915.
86. Gori GB. 1999. The EPA and the courts: Inching toward a showdown. Regul Toxicol Pharmacol 30:167-168.
87. Gori GB. 2001. The costly illusion of regulating unknowable risks. Regul Toxicol Pharmacol 34:205-212.
88. Gori GB. 2002. Considerations on guidelines of epidemiologic practice. Ann Epidemiol 12:73-78.
89. Austin HB. 1991. The effects of norethindrone on the Mullerian ducts of the American alligator. Gen Comp Endocrinol 84:300-307.
90. Gahr M, Wibbels T, Crews D. 1992. Sites of estrogen uptake in embryonic Trachemys scripta, a turtle with temperature-dependent sex determination. Biol Reprod 46:458-463.
91. Smith CA, Joss JM. 1994. Steroidogenic enzyme activity and ovarian differentiation in the saltwater crocodile, Crocodylus porosus. Gen Comp Endocrinol 93:232-245.
92. Belaid B, Richard-Mercier N, Pieau C, Dorizzi M. 2001. Sex reversal and aromatase in the European pond turtle: Treatment with letrozole after the thermosensitive period for sex determination. J Exp Zool 290:490-497.
93. Place AR, Lang J, Gavasso S, Jeyasuria P. 2001. Expression of P450(arom) in Malaclemys terrapin and Chelydra serpentina: A tale of two sites. J Exp Zool 290:673-690.
94. Milnes MRJ, Roberts RN, Guillette LJJ. 2002. Effects of incubation temperature and estrogen exposure on aromatase activity in the brain and gonads of embryonic alligators. Environ Health Perspect 110 (Suppl. 3):393-396.