Embryonic PCB Exposure Alters Phenotypic, Genetic, and Epigenetic Profiles in Turtle Sex Determination, a Biomarker of Environmental Contamination
Abstract
In species with temperature-dependent sex determination, embryonic gonadal differentiation can be modified by exposure to exogenous chemicals such as environmental contaminants. Although phenotypic outcomes of such events are well documented, the underlying molecular mechanisms are rarely described. Here we examine the genetic and epigenetic effect of the embryonic exposure to polychlorinated biphenyls (PCBs) on gonad differentiation in red-eared slider turtles (Trachemys scripta). Some PCB congeners are without effect whereas others synergize to alter sex determination in this species. Application of two potent PCB congeners alter the physiological processes of gonad development normally dictated by the male-producing temperature (MPT), resulting sex ratios significantly biased toward female hatchlings. Of these PCB-induced females, oviduct formation is prominently distorted regardless of ovary development. Further, gonadal expression of ovarian markers, aromatase, FoxL2, and Rspo1, is activated whereas testicular markers, Dmrt1 and Sox9, are suppressed compared with typical expression patterns observed at MPT. DNA methylation profiles of the aromatase promoter in PCB-treated gonads do not follow the typical methylation pattern observed in embryos incubating at female-producing temperature. Rather, the MPT-typical methylation profiles is retained despite the induced ovarian formation. Overall, our studies demonstrate that PCB exposure alters the transcriptional profiles of genes responsible for gonadal differentiation but does not re-establish the epigenetic marks of the aromatase promoter normally set by incubation temperatures in embryonic gonads.
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PCB-associated changes in DNA methylation have been shown to influence sexual development and alter sex-specific patterns of gene expression in the brain.
“PCB-associated changes in DNA methylation have been shown to influence sexual development and alter sex-specific patterns of gene expression in the brain [ 34 ].”
From DNA methylation: a mechanism linking environmental chemical exposures to risk of autism spectrum disorders? (2016) · cites this paper as [34]
Cites
1 retracted
Synergistic Activation of Estrogen Receptor with Combinations of Environmental Chemicals
Arnold, S. F., Klotz, D. M., Collins, B. M., Vonier, P. M., Guillette, L. J., & McLachlan, J. A. (1996) · Science · doi:10.1126/science.272.5267.1489 · Cited by 499 · see citing works
RetractedEndocrine-Disrupting Chemicals: An Endocrine Society Scientific Statement
Diamanti-Kandarakis, E., Bourguignon, J.-P., Giudice, L. C., Hauser, R., Prins, G. S., Soto, A. M., Zoeller, R. T., & Gore, A. C. (2009) · Endocrine Reviews · doi:10.1210/er.2009-0002 · Cited by 4,585 · see citing works
Epigenetic Transgenerational Actions of Endocrine Disruptors and Male Fertility
Anway, M. D., Cupp, A. S., Uzumcu, M., & Skinner, M. K. (2005) · Science · doi:10.1126/science.1108190 · Cited by 2,563 · see citing works
Müllerian-inhibiting substance function during mammalian sexual development.
Behringer, R., Finegold, M., & Cate, R. (1994) · Cell · doi:10.1016/0092-8674(94)90251-8 · Cited by 706 · see citing works
Ten Years of Mixing Cocktails: A Review of Combination Effects of Endocrine-Disrupting Chemicals
Kortenkamp, A. (2007) · Environmental Health Perspectives · doi:10.1289/ehp.9357 · Cited by 664 · see citing works
DMRT1 prevents female reprogramming in the postnatal mammalian testis
Matson, C. K., Murphy, M. W., Sarver, A. L., Griswold, M. D., Bardwell, V. J., & Zarkower, D. A. (2011) · Nature · doi:10.1038/nature10239 · Cited by 634 · see citing works
Navarro‐Martín, L., Viñas, J., Ribas, L., Díaz, N., Gutiérrez, A., Croce, L. D., & Piferrer, F. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002447 · Cited by 554 · see citing works
Fertilizing ability of DNA-damaged spermatozoa
Ahmadi, A., & Ng, S.-C. (1999) · Journal of Experimental Zoology · doi:10.1002/(sici)1097-010x(19991101)284:6 · Cited by 497 · see citing works
Female reproductive disorders: the roles of endocrine-disrupting compounds and developmental timing
Crain, D. A., Janssen, S. J., Edwards, T. M., Heindel, J., Ho, S.-M., Hunt, P., Iguchi, T., Juul, A., McLachlan, J. A., Schwartz, J., et al. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.08.067 · Cited by 465 · see citing works
Harner, T., Shoeib, M., Diamond, M. L., Stern, G. A., & Rosenberg, B. (2004) · Environmental Science & Technology · doi:10.1021/es040302r · Cited by 409 · see citing works
Bergeron, J. M., Crews, D. P., & McLachlan, J. A. (1994) · Environmental Health Perspectives · doi:10.1289/ehp.94102780 · Cited by 356 · see citing works
Self-citationMullerian Inhibiting Substance: A Gonadal Hormone with Multiple Functions*
Lee, M., & Donahoe, P. K. (1993) · Endocrine Reviews · doi:10.1210/edrv-14-2-152 · Cited by 333 · see citing works
The public health implications of polychlorinated biphenyls (PCBs) in the environment
Ross, G. L. (2004) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2004.06.003 · Cited by 329 · see citing works
Selective retention of hydroxylated PCB metabolites in blood.
Bergman, Å., Klasson‐Wehler, E., & Kuroki, H. (1994) · Environmental Health Perspectives · doi:10.1289/ehp.94102464 · Cited by 304 · see citing works
Anti-Müllerian Hormone: The Jost Factor
Josso, N., Cate, R. L., Picard, J., Vigier, B., di Clemente, N., Wilson, C. A., Imbeaud, S., Pepinsky, R. B., Guerrier, D., Boussin, L., et al. (1993) · Elsevier eBooks · doi:10.1016/b978-0-12-571148-7.50005-1 · Cited by 250 · see citing works
Polychlorinated biphenyls (PCBs) in the British environment: Sinks, sources and temporal trends
Harrad, S. J., Sewart, A. P., Alcock, R. E., Boumphrey, R., Burnett, V., Duarte‐Davidson, R., Halsall, C. J., Sanders, G., Waterhouse, K. S., Wild, S. R., et al. (1994) · Environmental Pollution · doi:10.1016/0269-7491(94)90079-5 · Cited by 242 · see citing works
Alligators and Endocrine Disrupting Contaminants: A Current Perspective
Guillette, L. J., Crain, D. A., Gunderson, M. P., Kools, S. A. E., Milnes, M. R., Orlando, E. F., Rooney, A. A., & Woodward, A. R. (2000) · American Zoologist · doi:10.1093/icb/40.3.438 · Cited by 201 · see citing works
DMRT1 Is Upregulated in the Gonads During Female-to-Male Sex Reversal in ZW Chicken Embryos1
Smith, C. A., Katz, M., & Sinclair, A. H. (2003) · Biology of Reproduction · doi:10.1095/biolreprod.102.007294 · Cited by 182 · see citing works
Oestrogens and temperature-dependent sex determination in reptiles: all is in the gonads
Pieau, C., & Dorizzi, M. (2004) · Journal of Endocrinology · doi:10.1677/joe.0.1810367 · Cited by 171 · see citing works
Matsumoto, Y., Buemio, A., Chu, R. A., Vafaee, M., & Crews, D. P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0063599 · Cited by 146 · see citing works
Self-citationSmith, C. A., Shoemaker, C. M., Roeszler, K. N., Queen, J. H., Crews, D. P., & Sinclair, A. H. (2008) · BMC Developmental Biology · doi:10.1186/1471-213x-8-72 · Cited by 142 · see citing works
Self-citationJacobson, J. L., Humphrey, H. E. B., Jacobson, S. W., Schantz, S. L., Mullin, M. D., & Welch, R. (1989) · American Journal of Public Health · doi:10.2105/ajph.79.10.1401 · Cited by 136 · see citing works
Shoemaker, C. M., Ramsey, M. E., Queen, J. H., & Crews, D. P. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21096 · Cited by 131 · see citing works
Self-citationA standardized series of embryonic stages for the emydid turtleTrachemys scripta
Greenbaum, E. (2002) · Canadian Journal of Zoology · doi:10.1139/z02-111 · Cited by 126 · see citing works
Crews, D. H., & Bergeron, J. M. (1994) · Journal of Endocrinology · doi:10.1677/joe.0.1430279 · Cited by 124 · see citing works
Self-citationLevels and chiral signatures of persistent organochlorine pollutants in human tissues from Belgium
Chu, S., Covaci, A., & Schepens, P. (2003) · Environmental Research · doi:10.1016/s0013-9351(03)00016-1 · Cited by 119 · see citing works
Cloning and expression of cDNA for anti-müllerian hormone.
Picard, J., Bénarous, R., Guerrier, D., Josso, N., & Kahn, A. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.15.5464 · Cited by 108 · see citing works
The role of estrogen in turtle sex determination and the effect of PCBs.
Crews, D. P., Bergeron, J. M., & McLachlan, J. A. (1995) · Environmental Health Perspectives · doi:10.1289/ehp.95103s773 · Cited by 105 · see citing works
Self-citationMullerian inhibiting substance: a gonadal hormone with multiple functions
Lee, M. M. (1993) · Endocrine Reviews · doi:10.1210/er.14.2.152 · Cited by 105 · see citing works
Merchant‐Larios, H., Ruiz-Ramírez, S., Moreno-Méndoza, N., & Marmolejo-Valencia, A. (1997) · General and Comparative Endocrinology · doi:10.1006/gcen.1997.6946 · Cited by 101 · see citing works
Berg, C., Holm, L., Brandt, I., & Brunström, B. (2001) · Reproduction · doi:10.1530/rep.0.1210155 · Cited by 100 · see citing works
Torres, L., Piedra, A. L., Mendoza, N., Valencia, A. M., Martı́nez, A. M., & Merchant‐Larios, H. (2002) · General and Comparative Endocrinology · doi:10.1016/s0016-6480(02)00511-7 · Cited by 99 · see citing works
Estrogen represses SOX9 during sex determination in the red-eared slider turtle Trachemys scripta
Barske, L. A., & Capel, B. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.02.010 · Cited by 97 · see citing works
Matsumoto, Y., & Crews, D. P. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.10.012 · Cited by 97 · see citing works
Self-citationParrott, B. B., Kohno, S., McCoy, J. A., & Guillette, L. J. (2013) · Biology of Reproduction · doi:10.1095/biolreprod.113.111468 · Cited by 94 · see citing works
Lance, V. A. (2008) · Journal of Experimental Zoology Part A Ecological Genetics and Physiology · doi:10.1002/jez.465 · Cited by 90 · see citing works
Ramsey, M. E., Shoemaker, C. M., & Crews, D. P. (2007) · Differentiation · doi:10.1111/j.1432-0436.2007.00182.x · Cited by 86 · see citing works
Self-citationSpecificity of steroid hormone-induced sex determination in a turtle
Wibbels, T., & Crews, D. P. (1992) · Journal of Endocrinology · doi:10.1677/joe.0.1330121 · Cited by 82 · see citing works
Self-citationPolychlorinated biphenyl levels in the tissues of exposed and nonexposed humans.
Schecter, A. J., Stanley, J. S., Boggess, K. E., Masuda, Y., Mes, J. C., Wolff, M. S., Fürst, P., Fürst, C., Wilson-Yang, K. M., & Chisholm, B. (1994) · Environmental Health Perspectives · doi:10.1289/ehp.94102s1149 · Cited by 78 · see citing works
Oestrogen blocks the nuclear entry of SOX9 in the developing gonad of a marsupial mammal
Pask, A. J., Calatayud, N. E., Shaw, G., Wood, W. M., & Renfree, M. B. (2010) · BMC Biology · doi:10.1186/1741-7007-8-113 · Cited by 67 · see citing works
Hardell, S., Tilander, H., Welfinger‐Smith, G., Burger, J., & Carpenter, D. O. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012396 · Cited by 66 · see citing works
Naert, C., Piette, M. H. A., Bruneel, N., & Peteghem, C. V. (2006) · Archives of Environmental Contamination and Toxicology · doi:10.1007/s00244-004-0234-6 · Cited by 59 · see citing works
Willingham, E. J., Rhen, T., Sakata, J. T., & Crews, D. P. (2000) · Environmental Health Perspectives · doi:10.1289/ehp.00108329 · Cited by 52 · see citing works
Self-citationRamsey, M., & Crews, D. P. (2007) · Sexual Development · doi:10.1159/000102107 · Cited by 50 · see citing works
Self-citation[Polychlorinated biphenyls and organochlorine pesticides in soils in Poland].
Kawano, M., Brudnowska, B., Falandysz, J., & Wakimoto, T. (2000) · PubMed · Cited by 48 · see citing works
Power, S. C., Lancman, J. J., & Smith, S. M. (1999) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(199912)216:4/5 · Cited by 44 · see citing works
Carlson, D. B., & Williams, D. E. J. (2001) · Environmental Toxicology and Chemistry · doi:10.1002/etc.5620200216 · Cited by 39 · see citing works
The Role of Estrogen in Turtle Sex Determination and the Effect of PCBs
Crews, D. P., Bergeron, J. M., & McLachlan, J. A. (1995) · Environmental Health Perspectives · doi:10.2307/3432512 · Cited by 34 · see citing works
Self-citationEllis, H., Shioda, K., Rosenthal, N. F., Coser, K. R., & Shioda, T. (2012) · Biology of Reproduction · doi:10.1095/biolreprod.112.099747 · Cited by 31 · see citing works
Changes in gonadal gene network by exogenous ligands in temperature-dependent sex determination
Matsumoto, Y., Yatsu, R., Taylor, C., & Crews, D. P. (2013) · Journal of Molecular Endocrinology · doi:10.1530/jme-12-0260 · Cited by 25 · see citing works
Self-citationCrews, D., Putz, O., Thomas, P., Hayes, T. B., & Howdeshell, K. L. (2003) · Pure and Applied Chemistry · doi:10.1351/pac200375112305 · Cited by 21 · see citing works
Self-citationIn ovo exposure quail assay for risk assessment of endocrine disrupting chemicals
Kamata, R., Takahashi, S., Shimizu, A., Morita, M., & Shiraishi, F. (2006) · Archives of Toxicology · doi:10.1007/s00204-006-0113-1 · Cited by 20 · see citing works
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Cited by
Sorted by citations
Vertebrate sex determination: evolutionary plasticity of a fundamental switch
Capel, B. (2017) · Nature reviews genetics · doi:10.1038/nrg.2017.60 · Cited by 456 · see citing works
Plastic and marine turtles: a review and call for research
Nelms, S. E., Duncan, E. M., Broderick, A. C., Galloway, T. S., Godfrey, M. H., Hamann, M., Lindeque, P. K., & Godley, B. J. (2015) · ICES Journal of Marine Science · doi:10.1093/icesjms/fsv165 · Cited by 434 · see citing works
Sex determination, gonadal sex differentiation, and plasticity in vertebrate species
Nagahama, Y., Chakraborty, T., Paul‐Prasanth, B., Ohta, K., & Nakamura, M. (2020) · Physiological Reviews · doi:10.1152/physrev.00044.2019 · Cited by 361 · see citing works
Amir, S., Shah, S. T. A., Mamoulakis, C., Docea, A. O., Kalantzi, O., Zachariou, A., Călina, D. C., Carvalho, F. D., Sofikitis, N., Makrigiannakis, A., et al. (2021) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph18041464 · Cited by 203 · see citing works
Sex determination mechanisms and sex control approaches in aquaculture animals
Li, X., Mei, J., Ge, C., Liu, X., & Gui, J. (2022) · Science China Life Sciences · doi:10.1007/s11427-021-2075-x · Cited by 173 · see citing works
Keil, K. P., & Lein, P. J. (2016) · Environmental Epigenetics · doi:10.1093/eep/dvv012 · Cited by 167 · see citing works
Yatsu, R., Miyagawa, S., Kohno, S., Parrott, B. B., Yamaguchi, K., Ogino, Y., Miyakawa, H., Lowers, R. H., Shigenobu, S., Guillette, L. J., et al. (2016) · BMC Genomics · doi:10.1186/s12864-016-2396-9 · Cited by 96 · see citing works
Chung, F. F., & Herceg, Z. (2020) · Environmental Health Perspectives · doi:10.1289/ehp6104 · Cited by 86 · see citing works
Marked for Life: Epigenetic Effects of Endocrine Disrupting Chemicals
Jacobs, M. N., Marczylo, E. L., Guerrero‐Bosagna, C., & Rüegg, J. (2017) · Annual Review of Environment and Resources · doi:10.1146/annurev-environ-102016-061111 · Cited by 81 · see citing works
Incorporating Transgenerational Epigenetic Inheritance into Ecological Risk Assessment Frameworks
Shaw, J. L. A., Judy, J. D., Kumar, A., Bertsch, P. M., Wang, M., & Kirby, J. K. (2017) · Environmental Science & Technology · doi:10.1021/acs.est.7b01094 · Cited by 59 · see citing works
Rosenfeld, C. S., Denslow, N. D., Orlando, E. F., Gutierrez-Villagomez, J. M., & Trudeau, V. L. (2017) · Journal of Toxicology and Environmental Health Part B · doi:10.1080/10937404.2017.1370083 · Cited by 57 · see citing works
Jandegian, C. M., Deem, S. L., Bhandari, R. K., Holliday, C. M., Nicks, D. K., Rosenfeld, C. S., Selcer, K. W., Tillitt, D. E., Saal, F. S. V., Vélez-Rivera, V., et al. (2015) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2015.04.003 · Cited by 56 · see citing works
Kohno, S., Bernhard, M. C., Katsu, Y., Zhu, J., Bryan, T. A., Doheny, B. M., Iguchi, T., & Guillette, L. J. (2015) · Endocrinology · doi:10.1210/en.2014-1852 · Cited by 56 · see citing works
Matsumoto, Y., Hannigan, B., & Crews, D. P. (2016) · PLoS ONE · doi:10.1371/journal.pone.0167362 · Cited by 55 · see citing works
Self-citationToxicological effects of polychlorinated biphenyls (PCBs) on freshwater turtles in the United States
Adams, C. I. M., Baker, J. E., & Kjellerup, B. V. (2016) · Chemosphere · doi:10.1016/j.chemosphere.2016.03.102 · Cited by 50 · see citing works
Sex determination without sex chromosomes
Weber, C. J., & Capel, B. (2021) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2020.0109 · Cited by 45 · see citing works
Roles of estrogens, estrogen-like compounds, and endocrine disruptors in adipocytes
Lizcano, F. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.921504 · Cited by 45 · see citing works
Barraza, A. D., Finlayson, K. A., Leusch, F. D. L., & van de Merwe, J. P. (2021) · Environmental Pollution · doi:10.1016/j.envpol.2021.117470 · Cited by 40 · see citing works
Ding, L., Huang, Z., Lu, Y., Liang, L., Li, N., Xu, Z., Zhang, J., Shi, H., & Hong, M. (2021) · Chemosphere · doi:10.1016/j.chemosphere.2021.130630 · Cited by 35 · see citing works
Kobayashi, S., Sata, F., Miyashita, C., Miura, R., Azumi, K., Kobayashi, S., Goudarzi, H., Araki, A., Ishizuka, M., Todaka, T., et al. (2017) · Toxicology · doi:10.1016/j.tox.2017.08.010 · Cited by 23 · see citing works
Tam, N. Y.-K., Kong, R. Y. C., & Lai, K. P. (2023) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2023.162401 · Cited by 16 · see citing works
Durando, M., Canesini, G., Cocito, L. L., Galoppo, G. H., Zayas, M. A., Luque, E. H., & Muñoz‐de‐Toro, M. (2015) · Journal of Experimental Zoology Part A Ecological Genetics and Physiology · doi:10.1002/jez.1999 · Cited by 16 · see citing works
Dhulkifle, H., Agouni, A., Zeidan, A., Al-Kuwari, M. B. S., Parray, A., Tolefat, M., & Korashy, H. M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179258 · Cited by 15 · see citing works
Roush, D., & Rhen, T. (2018) · Journal of Experimental Zoology Part A Ecological and Integrative Physiology · doi:10.1002/jez.2194 · Cited by 13 · see citing works
McCoy, J. A., Hamlin, H. J., Thayer, L., Guillette, L. J., & Parrott, B. B. (2016) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2016.04.011 · Cited by 12 · see citing works
Toyota, K., Masuda, S., Sugita, S., Miyaoku, K., Yamagishi, G., Akashi, H. D., & Miyagawa, S. (2020) · PubMed Central · doi:10.6620/zs.2020.59-54 · Cited by 12 · see citing works
Endocrine disrupting chemicals (EDCs) and sex steroid receptors
Hall, J. M., & Korach, K. S. (2021) · Advances in pharmacology · doi:10.1016/bs.apha.2021.04.001 · Cited by 12 · see citing works
Lourenço‐de‐Moraes, R., Campos, F. S., Carnaval, A. C., Otani, M., França, F. G. R., Cabral, P., & Benedito, E. (2021) · Biological Conservation · doi:10.1016/j.biocon.2021.109241 · Cited by 12 · see citing works
Organic contaminants in western pond turtles in remote habitat in California
Meyer, E. W., Eskew, E. A., Chibwe, L., Schrlau, J. E., Simonich, S. L. M., & Todd, B. D. (2016) · Chemosphere · doi:10.1016/j.chemosphere.2016.03.128 · Cited by 11 · see citing works
Hazards inherent in interdisciplinary behavioral research
Crews, D. P., Weisberg, S. A., & Sarkar, S. (2015) · Frontiers in Zoology · doi:10.1186/1742-9994-12-s1-s21 · Cited by 11 · see citing works
Self-citationSmaga, C. R., Bock, S. L., Johnson, J. M., & Parrott, B. B. (2022) · Sexual Development · doi:10.1159/000526009 · Cited by 9 · see citing works
Barraza, A. D., Young, L., Smith, C. E., Booth, D. T., Hof, C. A. M., Finlayson, K. A., Leusch, F. D. L., & van de Merwe, J. P. (2023) · Frontiers in Marine Science · doi:10.3389/fmars.2023.1238837 · Cited by 8 · see citing works
Hormones, Brain, and Behavior in Reptiles
Kabelik, D., & Crews, D. P. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00027-4 · Cited by 7 · see citing works
Self-citationEnvironmental Control of Sex Determination and Differentiation in Reptiles
Miyagawa, S., Yatsu, R., & Iguchi, T. (2018) · Diversity and commonality in animals · doi:10.1007/978-4-431-56609-0_18 · Cited by 7 · see citing works
Ortega, M. T., Bivens, N. J., Jogahara, T., Kuroiwa, A., Givan, S. A., & Rosenfeld, C. S. (2019) · BMC Genomics · doi:10.1186/s12864-019-5426-6 · Cited by 6 · see citing works
Colson, T. L., de Solla, S. R., & Langlois, V. S. (2020) · Chemosphere · doi:10.1016/j.chemosphere.2020.128146 · Cited by 6 · see citing works
Zhang, B., Miao, B., Fu, S., Coarfa, C., Kumar, R., Kuntala, P. K., Park, B., Grimm, S. L., Jangid, R. K., Colacino, J. A., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.07.28.667191 · Cited by 4 · see citing works
Matsumoto, Y., & Crews, D. P. (2017) · Sexual Development · doi:10.1159/000471940 · Cited by 3 · see citing works
Self-citationEffects of EDCs on female reproductive system in reptiles
Kohno, S., Nguyen, J., Jakobson, C. L., Lange, K. L., Hafferman, A. C., Molla, M. A., & Miyagawa, S. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-824464-7.00021-0 · Cited by 2 · see citing works
Zhang, T., Liu, L., Li, D., Li, J., Li, R., Wang, J., & Shi, H. (2022) · Environmental Science and Pollution Research · doi:10.1007/s11356-022-21057-5 · Cited by 2 · see citing works
de Macêdo, L. B., Magalhães, M. D. S., Dias, L. C., Lemos, K. K. D. A., Borges, R. S. D. M., Saraiva, M. V. A., de Oliveira, M. F., Neto, A. C. D. A., & de Moura, C. E. B. (2022) · Animal Reproduction · doi:10.1590/1984-3143-ar2022-0011 · Cited by 2 · see citing works
Gal, A.-S. L., Georges, J., Sotin, C., Charrìère, B., & Verneau, O. (2024) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2024.172077 · Cited by 2 · see citing works
Dirty Turtles: Examining the Effects of Persistent Pollutants on Embryonic Turtle Development
Ford, J. (2017) · McGill Science Undergraduate Research Journal · doi:10.26443/msurj.v12i1.41 · Cited by 1 · see citing works
Epigenetic Regulation of Sex Determination and Toxicity in Non‐mammalian Vertebrates
Yamagishi, G., Iguchi, T., & Miyagawa, S. (2022) · doi:10.1002/9781119807704.ch19 · Cited by 1 · see citing works
Colson, T. L. (2017) · QSpace (Queen's University Library)
Malformação no membro torácico direito em Trachemys dorbigni
Carniatto, C. H. D. O., Carniatto, C. H. D. O., Leonardo, J. M. L. O., & Lourenço‐de‐Moraes, R. (2017) · PubVet · doi:10.22256/pubvet.v11n6.607-609
Leveraging nature's experiments: David Crews' legacy in behavioral neuroendocrinology
Sakata, J. T., Woolley, S. C., Gillette, R., Nelson, R. J., & Rhen, T. (2026) · Hormones and Behavior · doi:10.1016/j.yhbeh.2026.105908
Lui, M., Minuti, A., D’Angiolini, S., Scuruchi, M., Silvestro, S., & Artimagnella, O. (2026) · Genes · doi:10.3390/genes17060692
- Authors
- Matsumoto, Y., Hannigan, B., & Crews, D.
- Affiliations
- The University of Texas at Austin (US)
- Corresponding author
- Crews, David
- Venue
- Endocrinology
- Publisher
- The Endocrine Society
- Published
- 2014-11-01
- Volume
- 155
- Issue
- 11
- Pages
- 4168-4177
- ISSN
- 0013-7227 (ISSN-L)
- 1945-7170
- OpenAlex
- W2130767568
- Cited by
- 50
- References
- 50
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 1 · 2023: 4 · 2022: 6 · 2021: 7 · 2020: 4 · 2019: 1 · 2018: 3 · 2017: 9 · 2016: 7 · 2015: 5
- FWCI
- 4.59
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- Department of Mechanical Engineering, University of Texas at Austin
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Reproductive biology and impacts on aquatic species
- Keywords
- polychlorinated biphenyls, embryonic exposure, temperature-dependent sex determination, gonadal differentiation, red-eared slider turtle, Trachemys scripta, DNA methylation, sex reversal, FOXL2, RSPO1, DMRT1, SOX9, environmental pollutants, sex ratio bias, epigenetic inheritance
- MeSH terms
- Animals, Embryo, Nonmammalian, Environmental Exposure, Environmental Monitoring, Female, Male, Phenotype, Polychlorinated Biphenyls, Turtles, Water Pollutants, Chemical, Biomarkers, Gene Expression Regulation, Developmental, Sex Determination Processes, Epigenesis, Genetic, Endocrine Disruptors
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