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Original Research Paper

Atrazine disrupts gonadal development in a live-bearing lizard

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Article: e1006071 | Received 24 Jun 2014, Accepted 07 Jan 2014, Published online: 18 Apr 2015

References

  • Guillette LJJ, Gross TS, Masson GR, Matter JM, Percival HF, Woodward AR. Developmental abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida. Environ Health Perspect 1994; 102:680-8; PMID:7895709; http://dx.doi.org/10.1289/ehp.94102680
  • 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; 99:5476-80; PMID:11960004; http://dx.doi.org/10.1073/pnas.082121499
  • Newbold RR. Lessons learned from perinatal exposure to diethylstilbestrol. Toxicol Appl Pharmacol 2004; 199:142-50; PMID:15313586; http://dx.doi.org/10.1016/j.taap.2003.11.033
  • Bergeron JM, Crews D, McLachlan JA. PCBs as environmental estrogens: turtle sex determination as a biomarker of environmental contamination. Environ Health Perspect 1994; 102:780-1; PMID:9657710; http://dx.doi.org/10.1289/ehp.94102780
  • Milnes MR, Bryan TA, Medina JG, Gunderson MP, Guillette LJ Jr. Developmental alterations as a result of in ovo exposure to the pesticide metabolite p,p′-DDE in Alligator mississippiensis. Gen Comp Endocrinol 2005; 144:257-63; PMID:16112671; http://dx.doi.org/10.1016/j.ygcen.2005.06.013
  • Guillette LJJ, Edwards TM. Environmental influences on fertility: can we learn lessons from studies of wildlife? Fertil Steril 2008; 89:e21-e4; PMID:18308053; http://dx.doi.org/10.1016/j.fertnstert.2007.12.019
  • Guillette LJJ, Guillette EA. Environmental contaminants and reproductive abnormalities in wildlife: implications for public health? Toxicol Ind Health 1996; 12:537-50; PMID:8843570; http://dx.doi.org/10.1177/074823379601200325
  • Giusti RM, Iwamoto K, Hatch EE. Diethylstilbestrol revisited: a review of the long-term health effects. An Int Med 1995; 122:778-88; http://dx.doi.org/10.7326/0003-4819-122-10-199505150-00008
  • Newbold RR, Jefferson WN, Padilla-Banks E. Prenatal Exposure to Bisphenol A at environmentally relevant doses adversely affects the murine female reproductive tract later in life. Environ Health Perspect 2009; 117:879-85; PMID:19590677; http://dx.doi.org/10.1289/ehp.0800045
  • Itonaga K, Wapstra E, Jones SM. Evidence for placental transfer of maternal corticosterone in a viviparous lizard. Comp Physol, A Mol Int Physiol 2011; 160:184-9.
  • Painter DL, Moore MC. Steroid hormone metabolism by the chorioallantoic placenta of the mountain spiny lizard Sceloporus jarrovi as a possible mechanism for buffering maternal-fetal hormone exchange. Physiol Biochem Zool 2005; 78:364-72; PMID:15887083; http://dx.doi.org/10.1086/430222
  • Pasqualini JR. Enzymes involved in the formation and transformation of steroid hormones in the fetal and placental compartments. J Steroid Biochem Mol Biol 2005; 97:401-15; PMID:16202579; http://dx.doi.org/10.1016/j.jsbmb.2005.08.004
  • Seckl JR. Glucocorticoid programming of the fetus; adult phenotypes and molecular mechanisms. Mol Cell Endocrinol 2001; 185:61-71; PMID:11738795; http://dx.doi.org/10.1016/S0303-7207(01)00633-5
  • Fan W, Yanase T, Morinaga H, Gondo S, Okabe T, Nomura M, Hayes TB, Takayanagi R, Nawata H. Herbicide atrazine activates SF-1 by direct affinity and concomitant co-activators recruitments to induce aromatase expression via promoter II. Biochem Biophys Res Commun 2007; 355:1012-8; PMID:17331471; http://dx.doi.org/10.1016/j.bbrc.2007.02.062
  • Fan WQ, Yanase T, Morinaga H, Gondo S, Okabe T, Nomura M, Komatsu T, Morohashi KI, Hayes TB, Takayanagi R, et al. Atrazine-induced aromatase expression is SF-1 dependent: implications for endocrine disruption in wildlife and reproductive cancers in humans. Environ Health Perspect 2007; 115:720-7; PMID:17520059; http://dx.doi.org/10.1289/ehp.9758
  • Sanderson JT, Letcher RJ, Heneweer M, Giesy JP, Van Den Berg M. Effects of chloro-s-triazine herbicides and metabolites on aromatase activity in various human cell lines and on vitellogenin production in male carp hepatocytes. Environ Health Perspect 2001; 109:1027-31; PMID:11675267; http://dx.doi.org/10.1289/ehp.011091027
  • Sanderson JT, Seinen W, Giesy JP, Van Den Berg MD. 2-chloro-s-triazine herbicides induce aromatase (CYP19) activity in H295R human adrenocortical carcinoma cells: a novel mechanism for estrogenicity? Toxicol Sci 2000; 54:121-7; PMID:10746939; http://dx.doi.org/10.1093/toxsci/54.1.121
  • Simpson ER, Clyne C, Rubin G, Wah CB, Robertson K, Britt K, Speed C, Jones M. Aromatase – a brief overview. Annu Rev Physiol 2002; 64:93-127; PMID:11826265; http://dx.doi.org/10.1146/annurev.physiol.64.081601.142703
  • Cooper RL, Stoker TE, Tyrey L, Goldman JM, McElroy WK. Atrazine disrupts the hypothalamic control of pituitary-ovarian function. Toxicol Sci 2000; 53:297-307; PMID:10696778; http://dx.doi.org/10.1093/toxsci/53.2.297
  • Foradori CD, Hinds LR, Hanneman WH, Handa RJ. Effects of atrazine and its withdrawal on gonadotropin-releasing hormone neuroendocrine function in the adult female wistar rat. Biol Reprod 2009; 81:1099-105; PMID:19605789; http://dx.doi.org/10.1095/biolreprod.109.077453
  • Stoker TE, Laws SC, Guidici DL, Cooper RL. The effect of atrazine on puberty in male Wistar rats: an evaluation in the protocol for the assessment of pubertal development and thyroid function. Toxicol Sci 2000; 58:50-9; PMID:11053540; http://dx.doi.org/10.1093/toxsci/58.1.50
  • Hayes TB, Anderson LL, Beasley VR, De Solla SR, Iguchi T, Ingraham H, Kestemont P, Kniewald J, Kniewald Z, Langlois VS, et al. Demasculinization and feminization of male gonads by atrazine: consistent effects across vertebrate classes. J Steroid Biochem Mol Biol 2011; 127:64-73; PMID:21419222; http://dx.doi.org/10.1016/j.jsbmb.2011.03.015
  • Danzo BJ. Environmental xenobiotics may disrupt normal endocrine function by interfering with the binding of physiological ligands to steroid receptors and binding proteins. Environ Health Perspect 1997; 105:294-301; PMID:9171990; http://dx.doi.org/10.1289/ehp.97105294
  • Schimmer BP, White PC. Minireview: steroidogenic factor 1: its roles in differentiation, development, and disease. Mol Endocrinol 2010; 24:1322-37; PMID:20203099; http://dx.doi.org/10.1210/me.2009-0519
  • Davis LK, Murr AS, Best DS, Fraites MJP, Zorrilla LM, Narotsky MG, Stoker TE, Goldman JM, Cooper RL. The effects of prenatal exposure to atrazine on pubertal and postnatal reproductive indices in the female rat. Reprod Toxicol 2011; 32:43-51; PMID:21530638; http://dx.doi.org/10.1016/j.reprotox.2011.04.004
  • Fraites MJP, Narotsky MG, Best DS, Stoker TE, Davis LK, Goldman JM, Hotchkiss MG, Klinefelter GR, Kamel A, Qian Y, et al. Gestational atrazine exposure: effects on male reproductive development and metabolite distribution in the dam, fetus, and neonate. Reprod Toxicol 2011; 32:52-63; PMID:21530639; http://dx.doi.org/10.1016/j.reprotox.2011.04.003
  • Blackburn D, G. Chorioallantoic placentation in squamate reptiles: structure, function, development, and evolution. J Exp Zool 1993; 266:414-30; http://dx.doi.org/10.1002/jez.1402660508
  • Blackburn D, G. Reptilian viviparity: past research, future directions, and appropriate models. Comp Physol, A Mol Int Physiol 2000; 127:391-409.
  • Stewart JR. Fetal nutrition in lecithotrophic squamate reptiles: toward a comprehensive model for evolution of viviparity and placentation. J Morphol 2013; PMID:23520054
  • Stewart JR, Thompson MB. A novel pattern of embryonic nutrition in a viviparous reptile. J Exp Biol 1993; 174:97-108; http://dx.doi.org/10.1016/0022-0981(93)90253-K
  • Stewart JR, Thompson MB. Evolution of placentation among squamate reptiles: recent research and future directions. Comp Physol, A Mol Int Physiol 2000; 127:411-31.
  • Blackburn DG. Standardized criteria for the recognition of embryonic nutritional patterns in squamate reptiles. Copeia 1994:925-35; http://dx.doi.org/10.2307/1446715
  • Herrel A, Meyers JJ, Nishikawa KC, De Vree F. The allantoplacenta of Mabuya mabouya (Sauria, Scincidae). J Morphol 2001; 249:132-46; PMID:11466741; http://dx.doi.org/10.1002/jmor.1047
  • Parsley LM, Wapstra E, Jones SM. Yolk contributes steroid to the multidimensional endocrine environment of embryos of Niveoscincus metallicus, a viviparous skink with a moderately complex placenta. Comp Physol, A Mol Int Physiol 2014; 171:51-6.
  • Painter D, Jennings DH, Moore MC. Placental buffering of maternal steroid hormone effects on fetal and yolk hormone levels: a comparative study of a viviparous lizard, Sceloporus jarrovi, and an oviparous lizard, Sceloporus graciosus. Gen Comp Endocrinol 2002; 127:105-16; PMID:12383438; http://dx.doi.org/10.1016/S0016-6480(02)00075-8
  • Parsley LM, Wapstra E, Jones SM. Placental and embryonic tissues exhibit aromatase activity in the viviparous lizard Niveoscincus metallicus. Gen Comp Endocrinol 2014; 200:61-6; PMID:24631640; http://dx.doi.org/10.1016/j.ygcen.2014.02.020
  • Jones SM, Bennett EJ, Swadling KM. Lipids in yolks and neonates of the viviparous lizard Niveoscincus metallicus. Comp Biochem Physiol B: Biochem Mol Biol 1998; 121:465-70; http://dx.doi.org/10.1016/S0305-0491(98)10136-0
  • Jones SM, Swain R. Annual reproductive cycle and annual cycles of reproductive hormones in plasma of female Niveoscincus metallicus (Scincidae) from Tasmania. J Herpetol 1996; 30:140-6; http://dx.doi.org/10.2307/1565504
  • Swain R, Jones SM. Facultative placentotrophy: half-way house or strategic solution? Comp Physol, A Mol Int Physiol 2000; 127:441-51.
  • Stewart JR. Placental structure and nutritional provision to embryos in predominantly lecithotrophic viviparous reptiles. Amer Zool 1992; 32:303-12.
  • The Department of Primary Industries, Parks, Water and the Environment. Agricultural and Veterinary Chemcials. Hobart, 2009.
  • Hutchinson MN, Donnella SC, Baverstock PR, Krieg M, Simms S, Burgin S. Immunological relationships and generic revision of the Australian lizards assigned to the genus Leiolopisma (Scincidae: Lygosominae). Aust J Zool 1990; 38:535-54; http://dx.doi.org/10.1071/ZO9900535
  • Parsley LM, Wapstra E, Jones SM. In utero exposure to the oestrogen mimic diethylstilbestrol disrupts gonadal development in a viviparous reptile. Reprod Fertil Dev 2014; PMID:24718097
  • Le Galllard JF, Clobert J, Ferrière R. Physical performance and darwinian fitness in lizards. Nature 2004; 432:502-5; PMID:15565154; http://dx.doi.org/10.1038/nature03057
  • Wapstra E. Maternal basking opportunity affects juvenile phenotype in a viviparous lizard. Funct Ecol 2000; 14:345-52; http://dx.doi.org/10.1046/j.1365-2435.2000.00428.x
  • Adkins-Regan E, Ottinger MA, Park J. Maternal transfer of estradiol to egg yolks alters sexual differentiation of avian offspring. J Exp Zool 1995; 271:466-70; http://dx.doi.org/10.1002/jez.1402710608
  • Lipar JL, Ketterson ED. Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Agelaius phoeniceus. Proc R Soc B Biol Sci 2000; 267:2005-10; http://dx.doi.org/10.1098/rspb.2000.1242
  • Atkins N, Swain R, Jones SM. Does date of birth or a capacity for facultative placentotrophy influence offspring quality in a viviparous skink, Niveoscincus microlepidotus? Aust J Zool 2006; 54:369-74; http://dx.doi.org/10.1071/ZO06041
  • Atkins N, Swain R, Jones SMJ. Are babies better in autumn or spring? The consequences of extending gestation in a biennially reproducing viviparous lizard. J Exp Zool A Ecol Gen Phys 2007; 307A:397-405; http://dx.doi.org/10.1002/jez.394
  • Holmes MM, Wade J. Sexual differentiation of the copulatory neuromuscular system in green anoles (Anolis carolinensis): normal ontogeny and manipulation of steroid hormones. J Comp Neurol 2005; 489:480-90; PMID:16025462; http://dx.doi.org/10.1002/cne.20645
  • Inamdar LS, Vani VV, Rao GMA. Dimorphic hemipenis correlates the pathways of gonadal sex differentiation in the lizard, Calotes versicolor (Daud.). J Adv Zool 2012; 33:31-7.
  • Neaves L, Wapstra E, Birch D, Girling JE, Joss JMP. Embryonic gonadal and sexual organ development in a small viviparous skink, Niveoscincus ocellatus. J Exp Zool A Comp Exp Biol 2006; 305 A:74-82; http://dx.doi.org/10.1002/jez.a.249
  • Guillette LJJ, Brock JW, Rooney AA, Woodward AR. Serum concentrations of various environmental contaminants and their relationship to sex steroid concentrations and phallus size in juvenile American alligators. Arch Environ Contam Toxicol 1999; 36:447-55; PMID:10227864; http://dx.doi.org/10.1007/PL00006617
  • Wapstra E, Uller T, While GM, Olsson M, Shine R. Giving offspring a head start in life: field and experimental evidence for selection on maternal basking behaviour in lizards. J Evol Biol 2010; 23:651-7; PMID:20074306; http://dx.doi.org/10.1111/j.1420-9101.2009.01924.x
  • Warner DA, Shine R. Fitness of juvenile lizards depends on seasonal timing of hatching, not offspring body size. Oecologia 2007; 154:65-73; PMID:17653771; http://dx.doi.org/10.1007/s00442-007-0809-9
  • Ferguson GW, Fox SF. Annual variation of survival advantage of large juvenile side- blotched lizards, Uta stansburiana: its causes and evolutionary significance. Evolution 1984; 38:342-9; http://dx.doi.org/10.2307/2408492
  • Crain DA, Spiteri ID, Guillette LJ Jr. 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 1999; 15:180-5; PMID:10188200; http://dx.doi.org/10.1191/074823399678846565
  • Matsushita S, Yamashita J, Iwasawa T, Tomita T, Ikeda M. Effects of in ovo exposure to imazalil and atrazine on sexual differentiation in chick gonads. Poult Sci 2006; 85:1641-7; PMID:16977851; http://dx.doi.org/10.1093/ps/85.9.1641
  • Stoker C, Beldoménico PM, Bosquiazzo VL, Zayas MA, Rey F, Rodríguez H, Muñoz-de-Toro M, Luque EH. Developmental exposure to endocrine disruptor chemicals alters follicular dynamics and steroid levels in Caiman latirostris. Gen Comp Endocrinol 2008; 156:603-12; PMID:18384790; http://dx.doi.org/10.1016/j.ygcen.2008.02.011
  • Dufaure JP, Hubert J. Table de Developpement du lezard vivipare-lacerta (Zootaca) Vivipara Jacquin. Arch Anat Micros Exp Exp 1961; 50:309-10.
  • Jones SM. Hormonal regulation of ovarian function in reptiles. In: Norris DO, Lopez KH, eds. Hormones and Reproduction of Vertebrates Burlington. San Diego, CA: Academic Press, 2011:89-115.
  • Kipfer S, Segner H, Wenger M, Wahli T, Bernet D. Long-term estrogen exposure of whitefish coregonus lavaretus induces intersex but not Lake Thun-typical gonad malformations. Dis Aquat Organ 2009; 84:43-56; PMID:19419006; http://dx.doi.org/10.3354/dao02031
  • Kummer V, Mašková J, Zralý Z, Faldyna M. Ovarian disorders in immature rats after postnatal exposure to environmental polycyclic aromatic hydrocarbons. J Appl Toxicol 2013; 33:90-9; PMID:23280776; http://dx.doi.org/10.1002/jat.1714
  • Jefferson W, Newbold R, Padilla-Banks E, Pepling M. Neonatal genistein treatment alters ovarian differentiation in the mouse: inhibition of oocyte nest breakdown and increased oocyte survival. Biol Reprod 2006; 74:161-8; PMID:16192398; http://dx.doi.org/10.1095/biolreprod.105.045724
  • Kim H, Nakajima T, Hayashi S, Chambon P, Watanabe H, Iguchi T, Sato T. Effects of diethylstilbestrol on programmed oocyte death and induction of polyovular follicles in neonatal mouse ovaries. Biol Reprod 2009; 81:1002-9; PMID:19553606; http://dx.doi.org/10.1095/biolreprod.108.070599
  • Hayes TB, Khoury V, Narayan A, Nazir M, Parka A, Brown T, Adame L, Chan E, Buchholz D, Stueve T, et al. Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopus laevis). Proc Natl Acad Sci U S A 2010; 107:4612-7; PMID:20194757; http://dx.doi.org/10.1073/pnas.0909519107
  • Rey F, Gonzalez M, Zayas MA, Stoker C, Durando M, Luque EH, Munoz-de-Toro M. Prenatal exposure to pesticides disrupts testicular histoarchitecture and alters testosterone levels in male Caiman latirostris. Gen Comp Endocrinol 2009; 162:286-92; PMID:19364509; http://dx.doi.org/10.1016/j.ygcen.2009.03.032
  • Kniewald J, Jakominić M, Tomljenović A, Šimić B, Romac P, Vranešić D, Kniewald Z. Disorders of male rat reproductive tract under the influence of atrazine. J Appl Toxicol 2000; 20:61-8; PMID:10641017; http://dx.doi.org/10.1002/(SICI)1099-1263(200001/02)20:1%3c61::AID-JAT628%3e3.0.CO;2-3
  • Victor-Costa AB, Bandeira SMC, Oliveira AG, Mahecha GAB, Oliveira CA. Changes in testicular morphology and steroidogenesis in adult rats exposed to Atrazine. Reprod Toxicol 2010; 29:323-31; PMID:20045047; http://dx.doi.org/10.1016/j.reprotox.2009.12.006
  • Spanò L, Tyler CR, Van Aerle R, Devos P, Mandiki SNM, Silvestre F, Thomé JP, Kestemont P. Effects of atrazine on sex steroid dynamics, plasma vitellogenin concentration and gonad development in adult goldfish (Carassius auratus). Aquat Toxicol 2004; 66:369-79; PMID:Can't; http://dx.doi.org/10.1016/j.aquatox.2003.10.009
  • Sanderson JT, Hordijk J, Denison MS, Springsteel MF, Nantz MH, van den Berg M. Induction and inhibition of aromatase (CYP19) activity by natural and synthetic flavonoid compounds in H295R human adrenocortical carcinoma cells. Toxicol Sci 2004; 82:70-9; PMID:15319488; http://dx.doi.org/10.1093/toxsci/kfh257
  • Kniewald J, Osredecki V, Gojmerac T, Zechner V, Kniewald Z. Effect of s-triazine compounds on testosterone metabolism in the rat prostate. J Appl Toxicol 1995; 15:215-8; PMID:7560742; http://dx.doi.org/10.1002/jat.2550150312
  • Crews D, Cantú AR, Bergeron, JM, Texas. Temperature and non-aromatizable androgens: a common pathway in male sex determination in a turtle with temperature-dependent sex determination? J Endocrinol 1996; 149:457-63; PMID:8691104; http://dx.doi.org/10.1677/joe.0.1490457
  • Pieau C, Mignot TM, Dorizzi M, Guichard A. Gonadal steroid levels in the turtle Emys orbicularis L.: a preliminary study in embryos, hatchlings, and young as a function of the incubation temperature of eggs. Gen Comp Endocrinol 1982; 47:392-8; PMID:7106557; http://dx.doi.org/10.1016/0016-6480(82)90249-0
  • Andrews JE, Smith CA, Sinclair AH. Sites of estrogen receptor and aromatase expression in the chicken embryo. Gen Comp Endocrinol 1997; 108:182-90; PMID:9356214; http://dx.doi.org/10.1006/gcen.1997.6978
  • Pieau C, Dorizzi M. Oestrogens and temperature-dependent sex determination in reptiles: all is in the gonads. J Endocrinol 2004; 181:367-77; PMID:15171684; http://dx.doi.org/10.1677/joe.0.1810367
  • Orlando EF, Guillette LJ Jr. Sexual dimorphic responses in wildlife exposed to endocrine disrupting chemicals. Environ Res 2007; 104:163-73; PMID:16890221; http://dx.doi.org/10.1016/j.envres.2006.06.002
  • Wu MQ, Mayra; Sass, Jennifer; Wetzler, Andrew. Still poisoning the well: atrazine continues to contaminate drinking water in the United States. Natural Resources Defence Council 2010.
  • Cale WGJ, Whitfield Gibbons J. Relationships between body size, size of the fat bodies, and total lipid content in the canebrake rattlesnake (Crotalus horridus) and the black racer (Coluber constrictor). Herpetologica 1972; 28:51-3.
  • Iguchi T, Fukazawa Y, Uesugi Y, Takasugi N. Polyovular follicles in mouse ovaries exposed neonatally to diethylstilbestrol in vivo and in vitro. Biol Reprod 1990; 43:478-84; PMID:2271729; http://dx.doi.org/10.1095/biolreprod43.3.478