Exposure to mono-n-butyl phthalate disrupts the development of preimplantation embryos
Da-Peng Chu A B , Shi Tian C , Da-Guang Sun D , Chan-Juan Hao A B , Hong-Fei Xia A B E and Xu Ma A B E
+ Author Affiliations
- Author Affiliations
A Reproductive and Genetic Center of National Research Institute for Family Planning, Beijing 100081, China.
B Graduate School, Peking Union Medical College, Beijing 100730, China.
C Haidian Maternal & Child Health Hospital, Beijing 100080, China.
D Chongqing Key Laboratory of Birth Defects and Reproductive Health, Chongqing 400020, China.
E Corresponding authors. Emails: hongfeixia@yahoo.com.cn; genetic@263.net.cn
Reproduction, Fertility and Development 25(8) 1174-1184 https://doi.org/10.1071/RD12178
Submitted: 5 June 2012 Accepted: 14 November 2012 Published: 12 December 2012
Abstract
Dibutyl phthalate (DBP), a widely used phthalate, is known to cause many serious diseases, especially in the reproductive system. However, little is known about the effects of its metabolite, mono-n-butyl phthalate (MBP), on preimplantation embryo development. In the present study, we found that treatment of embryos with 10–3 M MBP impaired developmental competency, whereas exposure to 10–4 M MBP delayed the progression of preimplantation embryos to the blastocyst stage. Furthermore, reactive oxygen species (ROS) levels in embryos were significantly increased following treatment with 10–3 M MBP. In addition, 10–3 M MBP increased apoptosis via the release of cytochrome c, whereas immunofluorescent analysis revealed that exposure of preimplantation embryos to MBP concentration-dependently (10–5, 10–4 and 10–3 M) decreased DNA methylation. Together, the results indicate a possible relationship between MBP exposure and developmental failure in preimplantation embryos.
Additional keywords: DNA methylation, reactive oxygen species.
References
Ahmad, K. A., Wan, G., and Ahmed, K. (2006). Intracellular hydrogen peroxide production is an upstream event in apoptosis induced by down-regulation of casein kinase 2 in prostate cancer cells. Mol. Cancer Res. 4, 331–338.| Intracellular hydrogen peroxide production is an upstream event in apoptosis induced by down-regulation of casein kinase 2 in prostate cancer cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xktlymsb4%3D&md5=3c2593f7c5cc1d078eda08e171da83d1CAS | 16687488PubMed |
Al-Khtib, M., Perret, A., Khoueiry, R., Ibala-Romdhane, S., Blachère, T., Greze, C., Lornage, J., and Lefèvre, A. (2011). Vitrification at the germinal vesicle stage does not affect the methylation profile of H19 and KCNQ1OT1 imprinting centers in human oocytes subsequently matured in vitro. Fertil. Steril. 95, 1955–1960.
| Vitrification at the germinal vesicle stage does not affect the methylation profile of H19 and KCNQ1OT1 imprinting centers in human oocytes subsequently matured in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltFymt70%3D&md5=4b54f0475dde0be744f0a9d40293e131CAS | 21420679PubMed |
Alam, M. S., Ohsako, S., Tay, T. W., Tsunekawa, N., Kanai, Y., and Kurohmaru, M. (2010). Di (n-butyl) phthalate induces vimentin filaments disruption in rat sertoli cells: a possible relation with spermatogenic cell apoptosis. Anat. Histol. Embryol. 39, 186–193.
| Di (n-butyl) phthalate induces vimentin filaments disruption in rat sertoli cells: a possible relation with spermatogenic cell apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3czmtV2isg%3D%3D&md5=ce4fd3d491949069b36e2f1a13890c38CAS | 20331591PubMed |
Aldyreva, M. V., Klimova, T. S., Iziumova, A. S., and Timofeevskaia, L. A. (1975). The effect of phthalate plasticizers on the generative function. Gig. Tr. Prof. Zabol. 12, 25–29.
| 1213487PubMed |
Barboni, B., Russo, V., Cecconi, S., Curini, V., Colosimo, A., Garofalo, M. L., Capacchietti, G., Di Giacinto, O., and Mattioli, M. (2011). In vitro grown sheep preantral follicles yield oocytes with normal nuclear-epigenetic maturation. PLoS One 6, e27550.
| In vitro grown sheep preantral follicles yield oocytes with normal nuclear-epigenetic maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Wju7%2FN&md5=56fa8b0a33b5587948b34a93fcfc7d23CAS | 22132111PubMed |
Carruthers, C. M., and Foster, P. M. (2005). Critical window of male reproductive tract development in rats following gestational exposure to di-n-butyl phthalate. Birth Defects Res. B Dev. Reprod. Toxicol. 74, 277–285.
| Critical window of male reproductive tract development in rats following gestational exposure to di-n-butyl phthalate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVelu74%3D&md5=896307d34f1b7c7ca8a64f7ad86ecf46CAS | 15954088PubMed |
Chhabra, A., Mehrotra, S., Chakraborty, N. G., Dorsky, D. I., and Mukherji, B. (2006). Activation-induced cell death of human melanoma specific cytotoxic T lymphocytes is mediated by apoptosis-inducing factor. Eur. J. Immunol. 36, 3167–3174.
| Activation-induced cell death of human melanoma specific cytotoxic T lymphocytes is mediated by apoptosis-inducing factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlCnsr%2FJ&md5=89ea396c1787d7b088b551c004102898CAS | 17109472PubMed |
Dalman, A., Eimani, H., Sepehri, H., Ashtiani, S. K., Valojerdi, M. R., Eftekhari-Yazdi, P., and Shahverdi, A. (2008). Effect of mono-(2-ethylhexyl) phthalate (MEHP) on resumption of meiosis, in vitro maturation and embryo development of immature mouse oocytes. Biofactors 33, 149–155.
| Effect of mono-(2-ethylhexyl) phthalate (MEHP) on resumption of meiosis, in vitro maturation and embryo development of immature mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjslKrtL8%3D&md5=a4402fcfc80fcc715d3f136e02743a7aCAS | 19346590PubMed |
Duty, S. M., Silva, M. J., Barr, D. B., Brock, J. W., Ryan, L., Chen, Z., Herrick, R. F., Christiani, D. C., and Hauser, R. (2003). Phthalate exposure and human semen parameters. Epidemiology 14, 269–277.
| Phthalate exposure and human semen parameters.Crossref | GoogleScholarGoogle Scholar | 12859026PubMed |
Favetta, L. A., Madan, P., Mastromonaco, G. F., St John, E. J., King, W. A., and Betts, D. H. (2007). The oxidative stress adaptor p66Shc is required for permanent embryo arrest in vitro. BMC Dev. Biol. 7, 132.
| The oxidative stress adaptor p66Shc is required for permanent embryo arrest in vitro.Crossref | GoogleScholarGoogle Scholar | 18047664PubMed |
Fennell, T. R., Krol, W. L., Sumner, S. C., and Snyder, R. W. (2004). Pharmacokinetics of dibutylphthalate in pregnant rats. Toxicol. Sci. 82, 407–418.
| Pharmacokinetics of dibutylphthalate in pregnant rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVSqsr7E&md5=be2e647463cf04b20a1eb053a1a47d8aCAS | 15456918PubMed |
Foster, P. M. D., Mylchreest, E., Gaido, K. W., and Sar, M. (2001). Effects of phthalate esters on the developing reproductive tract of male rats. Hum. Reprod. Update 7, 231–235.
| Effects of phthalate esters on the developing reproductive tract of male rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1Oktbk%3D&md5=d78e4414cb7298bbc58440367672d91bCAS |
Frederiksen, H., Sørensen, K., Mouritsen, A., Aksglaede, L., Hagen, C. P., Petersen, J. H., Skakkebaek, N. E., Andersson, A. M., and Juul, A. (2012). High urinary phthalate concentration associated with delayed pubarche in girls. Int. J. Androl. 35, 216–226.
| High urinary phthalate concentration associated with delayed pubarche in girls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFCisrjL&md5=dd131ffdd4a7723a643f50b145db0656CAS | 22428786PubMed |
Green, D. R., and Reed, J. C. (1998). Mitochondria and apoptosis. Science 281, 1309–1312.
| Mitochondria and apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlvVegsLo%3D&md5=9d9aa66b35c65ed294d12c2a8914033dCAS | 9721092PubMed |
Hauser, R., Meeker, J. D., Duty, S., Silva, M. J., and Calafat, A. M. (2006). Altered semen quality in relation to urinary concentrations of phthalate monoester and oxidative metabolites. Epidemiology 17, 682–691.
| Altered semen quality in relation to urinary concentrations of phthalate monoester and oxidative metabolites.Crossref | GoogleScholarGoogle Scholar | 17003688PubMed |
Heinzmann, J., Hansmann, T., Herrmann, D., Wrenzycki, C., Zechner, U., Haaf, T., and Niemann, H. (2011). Epigenetic profile of developmentally important genes in bovine oocytes. Mol. Reprod. Dev. 78, 188–201.
| Epigenetic profile of developmentally important genes in bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsVKmsL8%3D&md5=0b59b9b0efcacbce8a25cecb5166732aCAS | 21290475PubMed |
Herrera, B., Alvarez, A. M., Sánchez, A., Fernández, M., Roncero, C., Benito, M., and Fabregat, I. (2001). Reactive oxygen species (ROS) mediates the mitochondrial-dependent apoptosis induced by transforming growth factor (beta) in fetal hepatocytes. FASEB J. 15, 741–751.
| Reactive oxygen species (ROS) mediates the mitochondrial-dependent apoptosis induced by transforming growth factor (beta) in fetal hepatocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXitFWmsLc%3D&md5=b301bf6fc1ca1e78ea50f6a53fbc1858CAS | 11259392PubMed |
Jones, P. A., and Takai, D. (2001). The role of DNA methylation in mammalian epigenetics. Science 293, 1068–1070.
| The role of DNA methylation in mammalian epigenetics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtVWlsbY%3D&md5=678a9edba29de28c8acdf3453bc77172CAS | 11498573PubMed |
Jurewicz, J., and Hanke, W. (2011). Exposure to phthalates: reproductive outcome and children health. A review of epidemiological studies. Int. J. Occup. Med. Environ. Health 24, 115–141.
| Exposure to phthalates: reproductive outcome and children health. A review of epidemiological studies.Crossref | GoogleScholarGoogle Scholar | 21594692PubMed |
Kang, S. C., and Lee, B. M. (2005). DNA methylation of estrogen receptor alpha gene by phthalates. J. Toxicol. Environ. Health A 68, 1995–2003.
| DNA methylation of estrogen receptor alpha gene by phthalates.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1KgtrzM&md5=a1d4367a38420a75b90d037261c0b94eCAS | 16326419PubMed |
Kasahara, E., Sato, E. F., Miyoshi, M., Konaka, R., Hiramoto, K., Sasaki, J., Tokuda, M., Nakano, Y., and Inoue, M. (2002). Role of oxidative stress in germ cell apoptosis induced by di (2-ethylhexyl)phthalate. Biochem. J. 365, 849–856.
| 1:CAS:528:DC%2BD3sXptFOgsro%3D&md5=7d30e2f3174bbd52f827cafc4754caecCAS | 11982482PubMed |
Kim, T. S., Jung, K. K., Kim, S. S., Kang, I. H., Baek, J. H., Nam, H. S., Hong, S. K., Lee, B. M., Hong, J. T., Oh, K. W., Kim, H. S., Han, S. Y., and Kang, T. S. (2010). Effects of in utero exposure to di (n-butyl) phthalate on development of male reproductive tracts in Sprague-Dawley rats. J. Toxicol. Environ. Health A 73, 1544–1559.
| Effects of in utero exposure to di (n-butyl) phthalate on development of male reproductive tracts in Sprague-Dawley rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht12ltL3I&md5=629c24049b63f8b47c08044bd1e7667fCAS | 20954080PubMed |
Kleymenova, E., Swanson, C., Boekelheide, K., and Gaido, K. W. (2005). Exposure in utero to di (n-butyl) phthalate alters the vimentin cytoskeleton of fetal rat Sertoli cells and disrupts Sertoli cell–gonocyte contact. Biol. Reprod. 73, 482–490.
| Exposure in utero to di (n-butyl) phthalate alters the vimentin cytoskeleton of fetal rat Sertoli cells and disrupts Sertoli cell–gonocyte contact.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXovV2qt7Y%3D&md5=98a15df58efa531678ca73ff7f8bec54CAS | 15901642PubMed |
Koch, H. M., Preuss, R., and Angerer, J. (2006). Di (2-ethylhexyl)phthalate (DEHP): human metabolism and internal exposure. An update and latest results. Int. J. Androl. 29, 155–165.
| Di (2-ethylhexyl)phthalate (DEHP): human metabolism and internal exposure. An update and latest results.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjslWitrY%3D&md5=a65a65ae5b5eeedf25d6ddefdc6b6b1cCAS | 16466535PubMed |
Kondo, T., Shono, T., and Suita, S. (2006). Age-specific effect of phthalate ester on testicular development in rats. J. Pediatr. Surg. 41, 1290–1293.
| Age-specific effect of phthalate ester on testicular development in rats.Crossref | GoogleScholarGoogle Scholar | 16818065PubMed |
Kroemer, G., and Reed, J. C. (2000). Mitochondrial control of cell death. Nat. Med. 6, 513–519.
| Mitochondrial control of cell death.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtFyhsL4%3D&md5=89a44e5d519c6ff058af8586cbce5949CAS | 10802706PubMed |
Lee, S. K., Owens, G. A., and Veeramachaneni, D. N. (2005). Exposure to low concentrations of di-n-butyl phthalate during embryogenesis reduces survivability and impairs development of Xenopus laevis frogs. J. Toxicol. Environ. Health A 68, 763–772.
| Exposure to low concentrations of di-n-butyl phthalate during embryogenesis reduces survivability and impairs development of Xenopus laevis frogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1OntLw%3D&md5=9fb96733f6085775f44b44e34318a332CAS | 16020175PubMed |
Li, G., Khateeb, K., Schaeffer, E., Zhang, B., and Khatib, H. (2012). Genes of the transforming growth factor-beta signalling pathway are associated with pre-implantation embryonic development in cattle. J. Dairy Res. 79, 310–317.
| Genes of the transforming growth factor-beta signalling pathway are associated with pre-implantation embryonic development in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFWns7bE&md5=a70ef70ce5913f8ac712e6c697f63ec5CAS | 22687279PubMed |
Meeker, J. D., Sathyanarayana, S., and Swan, S. H. (2009). Phthalates and other additives in plastics: human exposure and associated health outcomes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 2097–2113.
| Phthalates and other additives in plastics: human exposure and associated health outcomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpt1Skt7Y%3D&md5=7dedb0c736aa225a3d44aa06ef0e29f6CAS | 19528058PubMed |
Montag, M., Koll, B., Holmes, P., and van der Ven, H. (2000). Significance of the number of embryonic cells and the state of the zona pellucida for hatching of mouse blastocysts in vitro versus in vivo. Biol. Reprod. 62, 1738–1744.
| Significance of the number of embryonic cells and the state of the zona pellucida for hatching of mouse blastocysts in vitro versus in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsF2hsbs%3D&md5=c0a0947e3e1d37510192262f31c39c13CAS | 10819778PubMed |
Oliver, V. F., Miles, H. L., Cutfield, W. S., Hofman, P. L., Ludgate, J. L., and Morison, I. M. (2012). Defects in imprinting and genome-wide DNA methylation are not common in the in vitro fertilization population. Fertil. Steril. 97, 147–153.e7.
| Defects in imprinting and genome-wide DNA methylation are not common in the in vitro fertilization population.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht12rtg%3D%3D&md5=7f3da3f22e1cf2c499e7e6d9306351d6CAS | 22112648PubMed |
Pant, N., Shukla, M., Kumar Patel, D., Shukla, Y., Mathur, N., Kumar Gupta, Y., and Saxena, D. K. (2008). Correlation of phthalate exposures with semen quality. Toxicol. Appl. Pharmacol. 231, 112–116.
| Correlation of phthalate exposures with semen quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXps1Gnurc%3D&md5=87d40b10bbfdee4ef886f03588ba94d1CAS | 18513777PubMed |
Prasanth, G. K., Divya, L. M., and Sadasivan, C. (2009). Effects of mono and di (n-butyl) phthalate on superoxide dismutase. Toxicology 262, 38–42.
| Effects of mono and di (n-butyl) phthalate on superoxide dismutase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotF2jtrY%3D&md5=5dceb014b2ff556dbe6c2f40cc4c8ee1CAS | 19386278PubMed |
Reik, W., Dean, W., and Walter, J. (2001). Epigenetic reprogramming in mammalian development. Science 293, 1089–1093.
| Epigenetic reprogramming in mammalian development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtVWltL8%3D&md5=b7db7079b851794188bbc5fce7d600adCAS | 11498579PubMed |
Rideout, W. M., Eggan, K., and Jaenisch, R. (2001). Nuclear cloning and epigenetic reprogramming of the genome. Science 293, 1093–1098.
| Nuclear cloning and epigenetic reprogramming of the genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtVWltLw%3D&md5=ac798502188592c44ea8f4dab3893e9cCAS | 11498580PubMed |
Saillenfait, A. M., Payan, J. P., Fabry, J. P., Beydon, D., Langonne, I., Gallissot, F., and Sabate, J. P. (1998). Assessment of the developmental toxicity, metabolism, and placental transfer of di-n-butyl phthalate administered to pregnant rats. Toxicol. Sci. 45, 212–224.
| 1:CAS:528:DyaK1cXntlKmsb4%3D&md5=06b9430067245fc87a81a191d6b206baCAS | 9848128PubMed |
Shelby, M. D. (2006). NTP-CERHR monograph on the potential human reproductive and developmental effects of di (2-ethylhexyl) phthalate (DEHP). NTP CERHR MON. 18, v.
| 19407857PubMed |
Simon, H. U., Haj-Yehia, A., and Levi-Schaffer, F. (2000). Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5, 415–418.
| Role of reactive oxygen species (ROS) in apoptosis induction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXitV2ru7k%3D&md5=7dc358473ecd534e09cc217dce5d0280CAS | 11256882PubMed |
Struve, M. F., Gaido, K. W., Hensley, J. B., Lehmann, K. P., Ross, S. M., Sochaski, M. A., Willson, G. A., and Dorman, D. C. (2009). Reproductive toxicity and pharmacokinetics of di-n-butyl phthalate (DBP) following dietary exposure of pregnant rats. Birth Defects Res. B Dev. Reprod. Toxicol. 86, 345–354.
| Reproductive toxicity and pharmacokinetics of di-n-butyl phthalate (DBP) following dietary exposure of pregnant rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtV2isL3M&md5=b7d70c20efe2081783734d2cc3b93f0dCAS | 19585553PubMed |
Susin, S. A., Lorenzo, H. K., Zamzami, N., Marzo, I., Snow, B. E., Brothers, G. M., Mangion, J., Jacotot, E., Costantini, P., Loeffler, M., Larochette, N., Goodlett, D. R., Aebersold, R., Siderovski, D. P., Penninger, J. M., and Kroemer, G. (1999). Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397, 441–446.
| Molecular characterization of mitochondrial apoptosis-inducing factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtFOhu78%3D&md5=3c95ee401714ce4327f5d2bbba645e1bCAS | 9989411PubMed |
Swan, S. H., Main, K. M., Liu, F., Stewart, S. L., Kruse, R. L., Calafat, A. M., Mao, C. S., Redmon, J. B., Ternand, C. L., Sullivan, S., and Teague, J. L. (2005). Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ. Health Perspect. 113, 1056–1061.
| Decrease in anogenital distance among male infants with prenatal phthalate exposure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpslSku74%3D&md5=870befdfe9afa83121dc445aa74f7e3eCAS | 16079079PubMed |
Tranfo, G., Caporossi, L., Paci, E., Aragona, C., Romanzi, D., De Carolis, C., De Rosa, M., Capanna, S., Papaleo, B., and Pera, A. (2012). Urinary phthalate monoesters concentration in couples with infertility problems. Toxicol. Lett. 213, 15–20.
| Urinary phthalate monoesters concentration in couples with infertility problems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVymtrnK&md5=715685d756d8773d9aef82369fe0e3beCAS | 22197707PubMed |
Wang, J. Z., Sui, H. S., Miao, D. Q., Liu, N., Zhou, P., Ge, L., and Tan, J. H. (2009). Effects of heat stress during in vitro maturation on cytoplasmic versus nuclear components of mouse oocytes. Reproduction 137, 181–189.
| Effects of heat stress during in vitro maturation on cytoplasmic versus nuclear components of mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovV2ks7s%3D&md5=daffa31b48884713a76158ee336cc04cCAS | 19029342PubMed |
Wright, K., Brown, L., Brown, G., Casson, P., and Brown, S. (2011). Microarray assessment of methylation in individual mouse blastocyst stage embryos shows that in vitro culture may have widespread genomic effects. Hum. Reprod. 26, 2576–2585.
| Microarray assessment of methylation in individual mouse blastocyst stage embryos shows that in vitro culture may have widespread genomic effects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVynsr3K&md5=e7b6fdc1bde6f18aea462ee17fe449bdCAS | 21685140PubMed |
Xia, H. F., Chi, Y., Qi, X., Su, M. M., Cao, Y., Song, P. P., Li, X., Chen, T., Zhao, A., Zhang, Y., Cao, Y., Ma, X., and Jia, W. (2011). Metabolomicevaluation of di-n-butyl phthalate (DBP)-induced teratogenesis in mice. Metabolomics 7, 559–571.
| Metabolomicevaluation of di-n-butyl phthalate (DBP)-induced teratogenesis in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlWrsbfO&md5=98bd122145edcdff889df93cc57c6578CAS |
Zhang, C., Liu, C., Li, D., Yao, N., Yuan, X., Yu, A., Lu, C., and Ma, X. (2010). Intracellular redox imbalance and extracellular amino acid metabolic abnormality contribute to arsenic-induced developmental retardation in mouse preimplantation embryos. J. Cell. Physiol. 222, 444–455.
| Intracellular redox imbalance and extracellular amino acid metabolic abnormality contribute to arsenic-induced developmental retardation in mouse preimplantation embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFSgsrvL&md5=2abecb687aeae539e70b0f304496ce0eCAS | 19918794PubMed |
Zhou, Y., Fukuoka, M., and Tanaka, A. (1990). Mechanisms of testicular atrophy induced by di-n-butyl phthalate in rats. Part 3. Changes in the activity of some enzymes in the Sertoli and germ cells, and in the levels of metal ions. J. Appl. Toxicol. 10, 447–453.
| Mechanisms of testicular atrophy induced by di-n-butyl phthalate in rats. Part 3. Changes in the activity of some enzymes in the Sertoli and germ cells, and in the levels of metal ions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXitF2jsA%3D%3D&md5=075fd574118d5258f9caab9e047c9c3aCAS | 2128091PubMed |
