Long-term maternal exposure to atrazine in the drinking water reduces penis length in the tammar wallaby Macropus eugenii
Laura E. Cook A , Yu Chen A , Marilyn B. Renfree
A and Andrew J. Pask A B
+ Author Affiliations
- Author Affiliations
A School of BioSciences, The University of Melbourne, Parkville, Vic. 3010, Australia.
B Corresponding author. Email: a.pask@unimelb.edu.au
Reproduction, Fertility and Development 32(13) 1099-1107 https://doi.org/10.1071/RD20158
Submitted: 17 June 2020 Accepted: 25 June 2020 Published: 5 August 2020
Abstract
Marsupials are experiencing devastating population declines across Australia. Exposure to environmental endocrine disruptors, through ingestion of contaminated resources in the environment, could be contributing to this decline. Atrazine (ATZ), a widely used herbicide in Australia, is an endocrine disruptor with the ability to cause reproductive abnormalities in a diverse range of vertebrates. We exposed adult female wallabies (Macropus eugenii) to drinking water containing ATZ (450 p.p.m) throughout pregnancy, parturition and lactation. We assessed the outcome of this exposure to the reproductive development of their young by assessing gonad and phallus development. Both these organs are especially sensitive to perturbations in the hormonal environment during development. Although no gross abnormalities were seen in gonad structure, exposure to ATZ did alter the expression of genes required for normal testis function. Furthermore, long-term exposure to ATZ resulted in a significant reduction in penis length. These results demonstrate that ATZ exposure during gestation and lactation can significantly affect the development of male young by affecting virilisation. Given the known vulnerability of macropodid marsupials to endocrine disruption, as well as their overlapping distribution with agricultural areas, these data raise major concerns for the use of pesticides in areas with fragile marsupial populations.
Additional keywords: endocrine disruptors, marsupial, phallus, pesticide, reproduction.
References
Abarikwu, S. O., Adesiyan, A. C., Oyeloja, T. O., Oyeyemi, M. O., and Farombi, E. O. (2010). Changes in sperm characteristics and induction of oxidative stress in the testis and epididymis of experimental rats by a herbicide, atrazine. Arch. Environ. Contam. Toxicol. 58, 874–882.| Changes in sperm characteristics and induction of oxidative stress in the testis and epididymis of experimental rats by a herbicide, atrazine.Crossref | GoogleScholarGoogle Scholar | 19672647PubMed |
Agopian, A. J., Lupo, P. J., Canfield, M. A., and Langlois, P. H. (2013). Case-control study of maternal residential atrazine exposure and male genital malformations. Am. J. Med. Genet. A. 161, 977–982.
| Case-control study of maternal residential atrazine exposure and male genital malformations.Crossref | GoogleScholarGoogle Scholar |
Agras, K., Willingham, E., Shiroyanagi, Y., Minasi, P., and Baskin, L. S. (2007). Estrogen receptor-alpha and beta are differentially distributed, expressed and activated in the fetal genital tubercle. J. Urol. 177, 2386–2392.
| Estrogen receptor-alpha and beta are differentially distributed, expressed and activated in the fetal genital tubercle.Crossref | GoogleScholarGoogle Scholar | 17509364PubMed |
Allinson, G., Bui, A., Zhang, P., Rose, G., Wightwick, A. M., Allinson, M., and Pettigrove, V. (2014). Investigation of 10 herbicides in surface waters of a horticultural production catchment in southeastern Australia. Arch. Environ. Contam. Toxicol. 67, 358–373.
| Investigation of 10 herbicides in surface waters of a horticultural production catchment in southeastern Australia.Crossref | GoogleScholarGoogle Scholar | 24935816PubMed |
Arnold, G. W., and Steven, D. E. (1988). Variations in distribution of western grey kangaroos, Macropus fuliginosus ocydromus, in the Tutanning Nature Reserve and their impact on adjacent farmland. Aust. Wildl. Res. 15, 119–128.
| Variations in distribution of western grey kangaroos, Macropus fuliginosus ocydromus, in the Tutanning Nature Reserve and their impact on adjacent farmland.Crossref | GoogleScholarGoogle Scholar |
Arnold, G. W., Steven, D. E., and Weeldenburg, J. R. (1989). The effect of daylength and weather conditions on the time spent by western grey kangaroos (Macropus fuliginosus) on farmland. Appl. Anim. Behav. Sci. 24, 353–360.
| The effect of daylength and weather conditions on the time spent by western grey kangaroos (Macropus fuliginosus) on farmland.Crossref | GoogleScholarGoogle Scholar |
Bancroft, J. D., and Stevens, A. (1990) ‘Theory and Practice of Histological Techniques.’ 3rd edn. (Churchill Livingstone: Edinburgh.)
Bolte, S., and Cordelieres, F. P. (2006). A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 224, 213–232.
| A guided tour into subcellular colocalization analysis in light microscopy.Crossref | GoogleScholarGoogle Scholar | 17210054PubMed |
Bolton, R. M., and Ahokas, J. T. (1995). Review: detoxification in Australia marsupials – ecotoxicological implications. Aust. J. Ecotoxicol. 1, 85–98.
Butler, C. M., Shaw, G., Clark, J., and Renfree, M. B. (2008). The functional development of Leydig cells in a marsupial. J. Anat. 212, 55–66.
| The functional development of Leydig cells in a marsupial.Crossref | GoogleScholarGoogle Scholar | 18069991PubMed |
Chen, Y., Yu, H., Pask, A. J., Fujiyama, A., Suzuki, Y., Sugano, S., Shaw, G., and Renfree, M. B. (2018). Hormone-responsive genes in the SHH and WNT/beta-catenin signaling pathways influence urethral closure and phallus growth. Biol. Reprod. 99, 806–816.
| 29767687PubMed |
Chen, Y., Yu, H. S., Pask, A., Fujiyama, A., Suzuki, Y., Sugano, S., Shaw, G., and Renfree, M. B. (2019). Effects of androgen and oestrogen on IGF pathways controlling phallus growth. Reproduction 157, 1–12.
| Effects of androgen and oestrogen on IGF pathways controlling phallus growth.Crossref | GoogleScholarGoogle Scholar | 30390614PubMed |
Chew, K. Y., Pask, A. J., Hickford, D., Shaw, G., and Renfree, M. B. (2014). A dual role for SHH during phallus development in a marsupial. Sex Dev. 8, 166–177.
| A dual role for SHH during phallus development in a marsupial.Crossref | GoogleScholarGoogle Scholar | 24480851PubMed |
Colborn, T., vom Saal, F. S., and Soto, A. M. (1993). Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ. Health Perspect. 101, 378–384.
| Developmental effects of endocrine-disrupting chemicals in wildlife and humans.Crossref | GoogleScholarGoogle Scholar | 8080506PubMed |
Cook, L. E., Finger, B. J., Green, M. P., and Pask, A. J. (2019). Exposure to atrazine during puberty reduces sperm viability, increases weight gain and alters the expression of key metabolic genes in the liver of male mice. Reprod. Fertil. Dev. 31, 920–931.
| Exposure to atrazine during puberty reduces sperm viability, increases weight gain and alters the expression of key metabolic genes in the liver of male mice.Crossref | GoogleScholarGoogle Scholar | 30636190PubMed |
Coveney, D., Shaw, G., and Renfree, M. B. (2001). Estrogen-induced gonadal sex reversal in the tammar wallaby. Biol. Reprod. 65, 613–621.
| Estrogen-induced gonadal sex reversal in the tammar wallaby.Crossref | GoogleScholarGoogle Scholar | 11466233PubMed |
Cunha, G. R., and Baskin, L. (2004). Development of the penile urethra. Adv. Exp. Med. Biol. 545, 87–102.
| Development of the penile urethra.Crossref | GoogleScholarGoogle Scholar | 15086022PubMed |
Davies, P. E., Cook, L. S. J., and Barton, J. L. (1994). Triazine herbicide contamination of Tasmanian streams: sources, concentrations and effects on biota. Mar. Freshwater Res. 45, 209–226.
| Triazine herbicide contamination of Tasmanian streams: sources, concentrations and effects on biota.Crossref | GoogleScholarGoogle Scholar |
Davis, L. K., Murr, A. S., Best, D. S., Fraites, M. J., Zorrilla, L. M., Narotsky, M. G., Stoker, T. E., Goldman, J. M., and Cooper, R. L. (2011). The effects of prenatal exposure to atrazine on pubertal and postnatal reproductive indices in the female rat. Reprod. Toxicol. 32, 43–51.
| The effects of prenatal exposure to atrazine on pubertal and postnatal reproductive indices in the female rat.Crossref | GoogleScholarGoogle Scholar | 21530638PubMed |
De Santa Barbara, P., Bonneaud, N., Boizet, B., Desclozeaux, M., Moniot, B., Sudbeck, P., Scherer, G., Poulat, F., and Berta, P. (1998). Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Mullerian hormone gene. Mol. Cell. Biol. 18, 6653–6665.
| Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Mullerian hormone gene.Crossref | GoogleScholarGoogle Scholar | 9774680PubMed |
Dixon, F. L., and Clay, D. V. (2004). Effect of herbicides applied pre- and post-emergence on forestry weeds grown from seed. Crop Prot. 23, 713–721.
| Effect of herbicides applied pre- and post-emergence on forestry weeds grown from seed.Crossref | GoogleScholarGoogle Scholar |
El-Merhibi, A., Ngo, S. N. T., Jones, B. R., Milic, N. L., Stupans, I., and McKinnon, R. A. (2007). Molecular insights into zenobiotics disposition in Australian marsupials. Aust. J. Ecotoxicol. 13, 7–8.
European Commission Health and Consumer Protection Directorate-General (2003). Review report for the active substance atrazine; Finalized in the Standing Committee on the Food Chain and Animal Health at its meeting on 3 October 2003 in support of a decision concerning the non-inclusion of atrazine in Annex I of Directive 91/414/EEC and the withdrawal of authorisation for plant protection products containing this active substance: European Commission Health and Consumer Protection Directorate-General; 2003. SANCO/10496/2003-final. Available at https://ec.europa.eu/food/sites/food/files/plant/docs/sc_phytopharmaceuticals_summary16_en.pdf
Fan, W., Yanase, T., Morinaga, H., Gondo, S., Okabe, T., Nomura, M., Hayes, T. B., Takayanagi, R., and Nawata, H. (2007a). Herbicide atrazine activates SF-1 by direct affinity and concomitant co-activators recruitments to induce aromatase expression via promoter II. Biochem. Biophys. Res. Commun. 355, 1012–1018.
| Herbicide atrazine activates SF-1 by direct affinity and concomitant co-activators recruitments to induce aromatase expression via promoter II.Crossref | GoogleScholarGoogle Scholar | 17331471PubMed |
Fan, W., Yanase, T., Morinaga, H., Gondo, S., Okabe, T., Nomura, M., Komatsu, T., Morohashi, K., Hayes, T. B., Takayanagi, R., and Nawata, H. (2007b). Atrazine-induced aromatase expression is SF-1 dependent: implications for endocrine disruption in wildlife and reproductive cancers in humans. Environ. Health Perspect. 115, 720–727.
| Atrazine-induced aromatase expression is SF-1 dependent: implications for endocrine disruption in wildlife and reproductive cancers in humans.Crossref | GoogleScholarGoogle Scholar | 17520059PubMed |
Farruggia, F. T., Rossmeisl, C. M., Hetrick, J. A., Biscoe, M., Louie-Juzwiak, R., and Spatz, D. (2016). Refined ecological risk assessment for atrazine. (US Environmental Protection Agency: Washington DC.) Available at https://www.biologicaldiversity.org/campaigns/pesticides_reduction/pdfs/AtrazinePreliminaryERA.pdf [verified 3 July 2020].
Gely-Pernot, A., Hao, C., Becker, E., Stuparevic, I., Kervarrec, C., Chalmel, F., Primig, M., Jegou, B., and Smagulova, F. (2015). The epigenetic processes of meiosis in male mice are broadly affected by the widely used herbicide atrazine. BMC Genomics 16, 885.
| The epigenetic processes of meiosis in male mice are broadly affected by the widely used herbicide atrazine.Crossref | GoogleScholarGoogle Scholar | 26518232PubMed |
Gely-Pernot, A., Saci, S., Kernanec, P. Y., Hao, C., Giton, F., Kervarrec, C., Tevosian, S., Mazaud-Guittot, S., and Smagulova, F. (2017). Embryonic exposure to the widely-used herbicide atrazine disrupts meiosis and normal follicle formation in female mice. Sci. Rep. 7, 3526.
| Embryonic exposure to the widely-used herbicide atrazine disrupts meiosis and normal follicle formation in female mice.Crossref | GoogleScholarGoogle Scholar | 28615648PubMed |
Govers, L. C., Phillips, T. R., Mattiske, D. M., Rashoo, N., Black, J. R., Sinclair, A., Baskin, L. S., Risbridger, G. P., and Pask, A. J. (2019). A critical role for estrogen signaling in penis development. FASEB J. 33, 10383–10392.
| A critical role for estrogen signaling in penis development.Crossref | GoogleScholarGoogle Scholar | 31225966PubMed |
Govers, L. C., Harper, A. P., Finger, B. J., Mattiske, D. M., Pask, A. J., and Green, M. P. (2020). Atrazine induces penis abnormalities including hypospadias in mice. J. Dev. Orig. Health Dis. 11, 246–249.
| Atrazine induces penis abnormalities including hypospadias in mice.Crossref | GoogleScholarGoogle Scholar | 31475654PubMed |
Harry, J. L., Koopman, P., Brennan, F. E., Graves, J. A., and Renfree, M. B. (1995). Widespread expression of the testis-determining gene SRY in a marsupial. Nat. Genet. 11, 347–349.
| Widespread expression of the testis-determining gene SRY in a marsupial.Crossref | GoogleScholarGoogle Scholar | 7581465PubMed |
Hayes, T. B., Anderson, L. L., Beasley, V. R., de Solla, S. R., Iguchi, T., Ingraham, H., Kestemont, P., Kniewald, J., Kniewald, Z., Langlois, V. S., Luque, E. H., McCoy, K. A., Munoz-de-Toro, M., Oka, T., Oliveira, C. A., Orton, F., Ruby, S., Suzawa, M., Tavera-Mendoza, L. E., Trudeau, V. L., Victor-Costa, A. B., and Willingham, E. (2011). Demasculinization and feminization of male gonads by atrazine: consistent effects across vertebrate classes. J. Steroid Biochem. Mol. Biol. 127, 64–73.
| Demasculinization and feminization of male gonads by atrazine: consistent effects across vertebrate classes.Crossref | GoogleScholarGoogle Scholar | 21419222PubMed |
Heneweer, M., van den Berg, M., and Sanderson, J. T. (2004). A comparison of human H295R and rat R2C cell lines as in vitro screening tools for effects on aromatase. Toxicol. Lett. 146, 183–194.
| A comparison of human H295R and rat R2C cell lines as in vitro screening tools for effects on aromatase.Crossref | GoogleScholarGoogle Scholar | 14643970PubMed |
Holloway, A. C., Anger, D. A., Crankshaw, D. J., Wu, M., and Foster, W. G. (2008). Atrazine-induced changes in aromatase activity in estrogen sensitive target tissues. J. Appl. Toxicol. 28, 260–270.
| Atrazine-induced changes in aromatase activity in estrogen sensitive target tissues.Crossref | GoogleScholarGoogle Scholar | 17685393PubMed |
Jin, Y., Lin, X., Miao, W., Wang, L., Wu, Y., and Fu, Z. (2015). Oral exposure of pubertal male mice to endocrine-disrupting chemicals alters fat metabolism in adult livers. Environ. Toxicol. 30, 1434–1444.
| Oral exposure of pubertal male mice to endocrine-disrupting chemicals alters fat metabolism in adult livers.Crossref | GoogleScholarGoogle Scholar | 24916741PubMed |
Kniewald, J., Osredecki, V., Gojmerac, T., Zechner, V., and Kniewald, Z. (1995). Effect of s-triazine compounds on testosterone metabolism in the rat prostate. J. Appl. Toxicol. 15, 215–218.
| Effect of s-triazine compounds on testosterone metabolism in the rat prostate.Crossref | GoogleScholarGoogle Scholar | 7560742PubMed |
Kojima, Y., Kohri, K., and Hayashi, Y. (2010). Genetic pathway of external genitalia formation and molecular etiology of hypospadias. J. Pediatr. Urol. 6, 346–354.
| Genetic pathway of external genitalia formation and molecular etiology of hypospadias.Crossref | GoogleScholarGoogle Scholar | 19995686PubMed |
Leihy, M. W., Shaw, G., Renfree, M. B., and Wilson, J. D. (2002). Administration of 5alpha-androstane-3alpha,17beta-diol to female tammar wallaby pouch young causes development of a mature prostate and male urethra. Endocrinology 143, 2643–2651.
| Administration of 5alpha-androstane-3alpha,17beta-diol to female tammar wallaby pouch young causes development of a mature prostate and male urethra.Crossref | GoogleScholarGoogle Scholar | 12072397PubMed |
Leihy, M. W., Shaw, G., Wilson, J. D., and Renfree, M. B. (2004). Penile development is initiated in the tammar wallaby pouch young during the period when 5 alpha-androstane-3 alpha,17 beta-diol is secreted by the testes. Endocrinology 145, 3346–3352.
| Penile development is initiated in the tammar wallaby pouch young during the period when 5 alpha-androstane-3 alpha,17 beta-diol is secreted by the testes.Crossref | GoogleScholarGoogle Scholar | 15059957PubMed |
Leihy, M. W., Shaw, G., Wilson, J. D., and Renfree, M. B. (2011). Development of the penile urethra in the tammar wallaby. Sex Dev. 5, 241–249.
| Development of the penile urethra in the tammar wallaby.Crossref | GoogleScholarGoogle Scholar | 22116535PubMed |
Lim, S., Ahn, S. Y., Song, I. C., Chung, M. H., Jang, H. C., Park, K. S., Lee, K. U., Pak, Y. K., and Lee, H. K. (2009). Chronic exposure to the herbicide, atrazine, causes mitochondrial dysfunction and insulin resistance. PLoS One 4, e5186.
| Chronic exposure to the herbicide, atrazine, causes mitochondrial dysfunction and insulin resistance.Crossref | GoogleScholarGoogle Scholar | 19787048PubMed |
Mahawong, P., Sinclair, A., Li, Y., Schlomer, B., Rodriguez, E., Ferretti, M. M., Liu, B., Baskin, L. S., and Cunha, G. R. (2014). Comparative effects of neonatal diethylstilbestrol on external genitalia development in adult males of two mouse strains with differential estrogen sensitivity. Differentiation 88, 70–83.
| Comparative effects of neonatal diethylstilbestrol on external genitalia development in adult males of two mouse strains with differential estrogen sensitivity.Crossref | GoogleScholarGoogle Scholar | 25449353PubMed |
Mizota, K., and Ueda, H. (2006). Endocrine disrupting chemical atrazine causes degranulation through Gq/11 protein-coupled neurosteroid receptor in mast cells. Toxicol. Sci. 90, 362–368.
| Endocrine disrupting chemical atrazine causes degranulation through Gq/11 protein-coupled neurosteroid receptor in mast cells.Crossref | GoogleScholarGoogle Scholar | 16381660PubMed |
Monniaux, D., Drouilhet, L., Rico, C., Estienne, A., Jarrier, P., Touze, J. L., Sapa, J., Phocas, F., Dupont, J., Dalbies-Tran, R., and Fabre, S. (2013). Regulation of anti-Mullerian hormone production in domestic animals. Reprod. Fertil. Dev. 25, 1–16.
| Regulation of anti-Mullerian hormone production in domestic animals.Crossref | GoogleScholarGoogle Scholar |
National Health and Medical Research Council (2013). ‘Australian Code for the Care and Use of Animals for Scientific Purposes, 8th edition.’ (National Health and Medical Research Council: Canberra.)
Pask, A. J. (2012). A role for estrogen in somatic cell fate of the mammalian gonad. Chromosome Res. 20, 239–245.
| A role for estrogen in somatic cell fate of the mammalian gonad.Crossref | GoogleScholarGoogle Scholar | 22161125PubMed |
Pask, A. J., Calatayud, N. E., Shaw, G., Wood, W. M., and Renfree, M. B. (2010). Oestrogen blocks the nuclear entry of SOX9 in the developing gonad of a marsupial mammal. BMC Biol. 8, 113.
| Oestrogen blocks the nuclear entry of SOX9 in the developing gonad of a marsupial mammal.Crossref | GoogleScholarGoogle Scholar | 20807406PubMed |
Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
| A new mathematical model for relative quantification in real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar | 11328886PubMed |
Pogrmic, K., Fa, S., Dakic, V., Kaisarevic, S., and Kovacevic, R. (2009). Atrazine oral exposure of peripubertal male rats downregulates steroidogenesis gene expression in Leydig cells. Toxicol. Sci. 111, 189–197.
| Atrazine oral exposure of peripubertal male rats downregulates steroidogenesis gene expression in Leydig cells.Crossref | GoogleScholarGoogle Scholar | 19541795PubMed |
Poole, W. E., Simms, N. G., Wood, J. T., and Lubulwa, M. (1991). Tables for age determination of the Kangaroo Island wallaby (tammar), Macropus eugenii, from body measurements. Technical Memorandum 32, CSIRO Division of Wildlife and Ecology, Canberra. Available at https://publications.csiro.au/rpr/download?pid=procite:7e7ff855-393f-4ffb-aa83-c3fda4669304&dsid=DS1 [verified 3 July 2020].
Radcliffe, J. C. (2002). Pesticide use in Australia. (Australian Academy of Technological Sciences and Engineering.) Available at https://www.atse.org.au/wp-content/uploads/2019/01/pesticide-use-australia.pdf [verified 3 July 2020].
Renfree, M. B. (2000). Maternal recognition of pregnancy in marsupials. Rev. Reprod. 5, 6–11.
| Maternal recognition of pregnancy in marsupials.Crossref | GoogleScholarGoogle Scholar | 10711730PubMed |
Renfree, M. B. (2006). Society for Reproductive Biology Founders’ Lecture 2006 – life in the pouch: womb with a view. Reprod. Fertil. Dev. 18, 721–734.
| Society for Reproductive Biology Founders’ Lecture 2006 – life in the pouch: womb with a view.Crossref | GoogleScholarGoogle Scholar | 17032580PubMed |
Renfree, M. B. (2010). Review: marsupials: placental mammals with a difference. Placenta 31, S21–S26.
| Review: marsupials: placental mammals with a difference.Crossref | GoogleScholarGoogle Scholar | 20079531PubMed |
Renfree, M. B., and Pask, A. J. (2011). Reproductive and developmental manipulation of the marsupial, the tammar wallaby Macropus eugenii. Methods Mol. Biol. 770, 457–473.
| Reproductive and developmental manipulation of the marsupial, the tammar wallaby Macropus eugenii.Crossref | GoogleScholarGoogle Scholar | 21805276PubMed |
Renfree, M. B., Wilson, J. D., Short, R. V., Shaw, G., and George, F. W. (1992). Steroid hormone content of the gonads of the tammar wallaby during sexual differentiation. Biol. Reprod. 47, 644–647.
| Steroid hormone content of the gonads of the tammar wallaby during sexual differentiation.Crossref | GoogleScholarGoogle Scholar | 1391352PubMed |
Renfree, M. B., Coveney, D., and Shaw, G. (2001). The influence of estrogen on the developing male marsupial. Reprod. Fertil. Dev. 13, 231–240.
| The influence of estrogen on the developing male marsupial.Crossref | GoogleScholarGoogle Scholar | 11800162PubMed |
Renfree, M. B., Chew, K. Y., and Shaw, G. (2014). Inducing sex reversal of the urogenital system of marsupials. Differentiation 87, 23–31.
| Inducing sex reversal of the urogenital system of marsupials.Crossref | GoogleScholarGoogle Scholar | 24433705PubMed |
Roberge, M., Hakk, H., and Larsen, G. (2004). Atrazine is a competitive inhibitor of phosphodiesterase but does not affect the estrogen receptor. Toxicol. Lett. 154, 61–68.
| Atrazine is a competitive inhibitor of phosphodiesterase but does not affect the estrogen receptor.Crossref | GoogleScholarGoogle Scholar | 15475179PubMed |
Rosenberg, B. G., Chen, H., Folmer, J., Liu, J., Papadopoulos, V., and Zirkin, B. R. (2008). Gestational exposure to atrazine: effects on the postnatal development of male offspring. J. Androl. 29, 304–311.
| Gestational exposure to atrazine: effects on the postnatal development of male offspring.Crossref | GoogleScholarGoogle Scholar | 17978342PubMed |
Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675.
| NIH Image to ImageJ: 25 years of image analysis.Crossref | GoogleScholarGoogle Scholar | 22930834PubMed |
Sekido, R., and Lovell-Badge, R. (2008). Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453, 930–934.
| Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer.Crossref | GoogleScholarGoogle Scholar | 18454134PubMed |
Shapiro, S. S., and Wilk, M. B. (1965). An analysis of variance test for normality (complete samples). Biometrika 52, 591–611.
| An analysis of variance test for normality (complete samples).Crossref | GoogleScholarGoogle Scholar |
Spanò, L., Tyler, C. R., van Aerle, R., Devos, P., Mandiki, S. N., Silvestre, F., Thomé, J. P., and Kestemont, P. (2004). Effects of atrazine on sex steroid dynamics, plasma vitellogenin concentration and gonad development in adult goldfish (Carassius auratus). Aquat. Toxicol. 66, 369–379.
| Effects of atrazine on sex steroid dynamics, plasma vitellogenin concentration and gonad development in adult goldfish (Carassius auratus).Crossref | GoogleScholarGoogle Scholar | 15168945PubMed |
Stanko, J. P., Enoch, R. R., Rayner, J. L., Davis, C. C., Wolf, D. C., Malarkey, D. E., and Fenton, S. E. (2010). Effects of prenatal exposure to a low dose atrazine metabolite mixture on pubertal timing and prostate development of male Long-Evans rats. Reprod. Toxicol. 30, 540–549.
| Effects of prenatal exposure to a low dose atrazine metabolite mixture on pubertal timing and prostate development of male Long-Evans rats.Crossref | GoogleScholarGoogle Scholar | 20727709PubMed |
Stefanidou, M., Maravelias, C., and Spiliopoulou, C. (2009). Human exposure to endocrine disruptors and breast milk. Endocr. Metab. Immune Disord. Drug Targets 9, 269–276.
| Human exposure to endocrine disruptors and breast milk.Crossref | GoogleScholarGoogle Scholar | 19594415PubMed |
Stewart, M. K., Mattiske, D. M., and Pask, A. J. (2018). In utero exposure to both high- and low-dose diethylstilbestrol disrupts mouse genital tubercle development. Biol. Reprod. 99, 1184–1193.
| In utero exposure to both high- and low-dose diethylstilbestrol disrupts mouse genital tubercle development.Crossref | GoogleScholarGoogle Scholar | 29931162PubMed |
Suzawa, M., and Ingraham, H. A. (2008). The herbicide atrazine activates endocrine gene networks via non-steroidal NR5A nuclear receptors in fish and mammalian cells. PLoS One 3, e2117.
| The herbicide atrazine activates endocrine gene networks via non-steroidal NR5A nuclear receptors in fish and mammalian cells.Crossref | GoogleScholarGoogle Scholar | 18461179PubMed |
Tyndale-Biscoe, H., and Renfree, M. (1987). ‘Reproductive Physiology of Marsupials.’ (Cambridge University Press.)
Viger, R. S., Mertineit, C., Trasler, J. M., and Nemer, M. (1998). Transcription factor GATA-4 is expressed in a sexually dimorphic pattern during mouse gonadal development and is a potent activator of the Mullerian inhibiting substance promoter. Development 125, 2665–2675.
| 9636081PubMed |
Wilhelm, D., Martinson, F., Bradford, S., Wilson, M. J., Combes, A. N., Beverdam, A., Bowles, J., Mizusaki, H., and Koopman, P. (2005). Sertoli cell differentiation is induced both cell-autonomously and through prostaglandin signaling during mammalian sex determination. Dev. Biol. 287, 111–124.
| Sertoli cell differentiation is induced both cell-autonomously and through prostaglandin signaling during mammalian sex determination.Crossref | GoogleScholarGoogle Scholar | 16185683PubMed |
Wilhelm, D., Hiramatsu, R., Mizusaki, H., Widjaja, L., Combes, A. N., Kanai, Y., and Koopman, P. (2007). SOX9 regulates prostaglandin D synthase gene transcription in vivo to ensure testis development. J. Biol. Chem. 282, 10553–10560.
| SOX9 regulates prostaglandin D synthase gene transcription in vivo to ensure testis development.Crossref | GoogleScholarGoogle Scholar | 17277314PubMed |
Wilson, J. D., Shaw, G., Leihy, M. L., and Renfree, M. B. (2002). The marsupial model for male phenotypic development. Trends Endocrinol. Metab. 13, 78–83.
| The marsupial model for male phenotypic development.Crossref | GoogleScholarGoogle Scholar | 11854023PubMed |
Wilson, J. D., Leihy, M. W., Shaw, G., and Renfree, M. B. (2003). Unsolved problems in male physiology: studies in a marsupial. Mol. Cell. Endocrinol. 211, 33–36.
| Unsolved problems in male physiology: studies in a marsupial.Crossref | GoogleScholarGoogle Scholar | 14656473PubMed |
Woinarski, J. C., Burbidge, A. A., and Harrison, P. L. (2015). Ongoing unraveling of a continental fauna: decline and extinction of Australian mammals since European settlement. Proc. Natl Acad. Sci. USA 112, 4531–4540.
| Ongoing unraveling of a continental fauna: decline and extinction of Australian mammals since European settlement.Crossref | GoogleScholarGoogle Scholar | 25675493PubMed |
