Use of Human Embryonic Stem Cell-based Models for Male Reproductive Toxicity Screening

REFERENCES

• Aflatoonian, B. and Moore, H. (2006) Germ cells from mouse and human embryonic stem cells. Reproduction 132:699–707.
   PubMed Web of Science ®Google Scholar
• Aflatoonian, B., Ruban, L., Jones, M., Aflatoonian, R., Fazeli, A. and Moore, H. D. (2009). In vitro post-meiotic germ cell development from human embryonic stem cells. Hum Reprod 24:3150–3159.
   PubMed Web of Science ®Google Scholar
• Anway, M. D., Cupp, A. S., Uzumcu, M. and Skinner, M. K. (2005). Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308:1466–1469.
   PubMed Web of Science ®Google Scholar
• Arnold, S. J., Maretto, S., Islam, A., Bikoff, E. K. and Robertson, E. J. (2006) Dose-dependent Smad1, Smad5 and Smad8 signaling in the early mouse embryo. Dev Biol 296:104–118.
   PubMed Web of Science ®Google Scholar
• Brandenberger, R., Wei, H., Zhang, S., Lei, S., Murage, J., Fisk, G. J., et al. (2004). Transcriptome characterization elucidates signaling networks that control human ES cell growth and differentiation. Nat Biotechnol 22:707–716.
   PubMed Web of Science ®Google Scholar
• Bucay, N., Yebra, M., Cirulli, V., Afrikanova, I., Kaido, T., Hayek, A., et al. (2009). A novel approach for the derivation of putative primordial germ cells and sertoli cells from human embryonic stem cells. Stem Cells 27:68–77.
   PubMed Web of Science ®Google Scholar
• Chen, C., Ridzon, D., Lee, C. T., Blake, J., Sun, Y. and Strauss, W. M. (2007). Defining embryonic stem cell identity using differentiation-related microRNAs and their potential targets. Mamm Genome 18:316–327.
   PubMed Web of Science ®Google Scholar
• Chung, Y., Klimanskaya, I., Becker, S., Li, T., Maserati, M., Lu, S. J., et al. (2008). Human embryonic stem cell lines generated without embryo destruction. Cell Stem Cell 2:113–117.
   PubMed Web of Science ®Google Scholar
• Clark, A. T., Bodnar, M. S., Fox, M., Rodriquez, R. T., Abeyta, M. J., Firpo, M. T., et al. (2004). Spontaneous differentiation of germ cells from human embryonic stem cells in vitro. Hum Mol Genet 13:727–739.
   PubMed Web of Science ®Google Scholar
• Clementi, M., Tiboni, G. M., Causin, R., La Rocca, C., Maranghi, F., Raffagnato, F., et al. (2008). Pesticides and fertility: an epidemiological study in Northeast Italy and review of the literature. Reprod Toxicol 26:13–18.
   PubMed Web of Science ®Google Scholar
• Fox, N., Damjanov, I., Martinez-Hernandez, A., Knowles, B. B. and Solter, D. (1981). Immunohistochemical localization of the early embryonic antigen (SSEA-1) in postimplantation mouse embryos and fetal and adult tissues. Dev Biol 83:391–398.
   PubMed Web of Science ®Google Scholar
• Geijsen, N., Horoschak, M., Kim, K., Gribnau, J., Eggan, K. and Daley, G. Q. (2004). Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature 427:148–154.
   PubMed Web of Science ®Google Scholar
• Genschow, E., Scholz, G., Brown, N., Piersma, A., Brady, M., Clemann, N., et al. (2000). Development of prediction models for three in vitro embryotoxicity tests in an ECVAM validation study. In Vitr Mol Toxicol 13:51–66.
   PubMedGoogle Scholar
• Ginis, I., Luo, Y., Miura, T., Thies, S., Brandenberger, R., Gerecht-Nir, S., et al. (2004). Differences between human and mouse embryonic stem cells. Dev Biol 269:360–380.
   PubMed Web of Science ®Google Scholar
• Habert, R., Muczynski, V., Lehraiki, A., Lambrot, R., Lecureuil, C., Levacher, C., et al. (2009). Adverse effects of endocrine disruptors on the foetal testis development: focus on the phthalates. Folia Histochem Cytobiol 47:S67-74.
   PubMed Web of Science ®Google Scholar
• Hauser, R. and Sokol, R. (2008) Science linking environmental contaminant exposures with fertility and reproductive health impacts in the adult male. Fertil Steril 89:e59-65.
   PubMed Web of Science ®Google Scholar
• Houbaviy, H. B., Murray, M. F. and Sharp, P. A. (2003) Embryonic stem cell-specific MicroRNAs. Dev Cell 5:351–358.
   PubMed Web of Science ®Google Scholar
• http://microrna.sanger.ac.uk.
   Google Scholar
• Hubner, K., Fuhrmann, G., Christenson, L. K., Kehler, J., Reinbold, R., De La Fuente, R., et al. (2003). Derivation of oocytes from mouse embryonic stem cells. Science 300:1251–1256.
   PubMed Web of Science ®Google Scholar
• Ilic, D., Giritharan, G., Zdravkovic, T., Caceres, E., Genbacev, O., Fisher, S. J., et al. (2009). Derivation of human embryonic stem cell lines from biopsied blastomeres on human feeders with minimal exposure to xenomaterials. Stem Cells Dev 18:1343–1350.
   PubMed Web of Science ®Google Scholar
• Kee, K., Angeles, V. T., Flores, M., Nguyen, H. N. and Reijo Pera, R. A. (2009) Human DAZL, DAZ and BOULE genes modulate primordial germ-cell and haploid gamete formation. Nature 462:222–225.
   PubMed Web of Science ®Google Scholar
• Kee, K., Gonsalves, J. M., Clark, A. T. and Pera, R. A. (2006) Bone morphogenetic proteins induce germ cell differentiation from human embryonic stem cells. Stem Cells Dev 15:831–837.
   PubMed Web of Science ®Google Scholar
• Kehler, J., Tolkunova, E., Koschorz, B., Pesce, M., Gentile, L., Boiani, M., et al. (2004). Oct4 is required for primordial germ cell survival. EMBO Rep 5:1078–1083.
   PubMed Web of Science ®Google Scholar
• Koshimizu, U., Watanabe, M. and Nakatsuji, N. (1995) Retinoic acid is a potent growth activator of mouse primordial germ cells in vitro. Dev Biol 168:683–685.
   PubMed Web of Science ®Google Scholar
• Landgraf, P., Rusu, M., Sheridan, R., Sewer, A., Iovino, N., Aravin, A., et al. (2007). A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129:1401–1414.
   PubMed Web of Science ®Google Scholar
• Laurent, L. C., Chen, J., Ulitsky, I., Mueller, F. J., Lu, C., Shamir, R., et al. (2008). Comprehensive microRNA profiling reveals a unique human embryonic stem cell signature dominated by a single seed sequence. Stem Cells 26:1506–1516.
   PubMed Web of Science ®Google Scholar
• Matsui, Y., Zsebo, K. and Hogan, B. L. (1992). Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell 70:841–847.
   PubMed Web of Science ®Google Scholar
• McCarroll, S. A., Murphy, C. T., Zou, S., Pletcher, S. D., Chin, C. S., Jan, Y. N., et al. (2004). Comparing genomic expression patterns across species identifies shared transcriptional profile in aging. Nat Genet 36:197–204.
   PubMed Web of Science ®Google Scholar
• McLaren, A. (2003) Primordial germ cells in the mouse. Dev Biol 262:1–15.
   PubMed Web of Science ®Google Scholar
• Mikkola, M., Olsson, C., Palgi, J., Ustinov, J., Palomaki, T., Horelli-Kuitunen, N., et al. (2006). Distinct differentiation characteristics of individual human embryonic stem cell lines. BMC Dev Biol 6:40.
   PubMed Web of Science ®Google Scholar
• Miller, R. K., Peters, P. W. and Schaefer, C. E. (2007) General commentary on drug therapy and drug risks in pregnancy. In: Schaefer, C. E., Peters, P. W. and Miller, R. K. (Eds.) Drugs During Pregnancy and Lactation, 2nd edition. New York: Academic Press.
   Google Scholar
• Miller R. K., P. P. and Schaefer CE. (2007) General commentary on drug therapy and drug risks in pregnancy. Drugs During Pregnancy and Lactation.
   Google Scholar
• Mineno, J., Okamoto, S., Ando, T., Sato, M., Chono, H., Izu, H., et al. (2006). The expression profile of microRNAs in mouse embryos. Nucleic Acids Res 34:1765–1771.
   PubMed Web of Science ®Google Scholar
• Mise, N., Fuchikami, T., Sugimoto, M., Kobayakawa, S., Ike, F., Ogawa, T., et al. (2008). Differences and similarities in the developmental status of embryo-derived stem cells and primordial germ cells revealed by global expression profiling. Genes Cells 13:863–877.
   PubMed Web of Science ®Google Scholar
• Morin, R. D., O'Connor, M. D., Griffith, M., Kuchenbauer, F., Delaney, A., Prabhu, A. L., et al. (2008). Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res 18:610–621.
   PubMed Web of Science ®Google Scholar
• Nayernia, K., Nolte, J., Michelmann, H. W., Lee, J. H., Rathsack, K., Drusenheimer, N., et al. (2006). In vitro-differentiated embryonic stem cells give rise to male gametes that can generate offspring mice. Dev Cell 11:125–132.
   PubMed Web of Science ®Google Scholar
• Ohinata, Y., Payer, B., O'Carroll, D., Ancelin, K., Ono, Y., Sano, M., et al. (2005). Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436:207–213.
   PubMed Web of Science ®Google Scholar
• Park, T. S., Galic, Z., Conway, A. E., Lindgren, A., van Handel, B. J., Magnusson, M., et al. (2009). Derivation of primordial germ cells from human embryonic and induced pluripotent stem cells is significantly improved by coculture with human fetal gonadal cells. Stem Cells 27:783–795.
   PubMed Web of Science ®Google Scholar
• Payer, B., Chuva de Sousa Lopes, S. M., Barton, S. C., Lee, C., Saitou, M. and Surani, M. A. (2006). Generation of stella-GFP transgenic mice: a novel tool to study germ cell development. Genesis 44:75–83.
   PubMed Web of Science ®Google Scholar
• Pesce, M., Gross, M. K. and Scholer, H. R. (1998) In line with our ancestors: Oct-4 and the mammalian germ. Bioessays 20:722–732.
   PubMed Web of Science ®Google Scholar
• Rajpert-De Meyts, E., Bartkova, J., Samson, M., Hoei-Hansen, C. E., Frydelund-Larsen, L., Bartek, J., et al. (2003a) The emerging phenotype of the testicular carcinoma in situ germ cell. Apmis 111:267-278; discussion 278-269.
   PubMed Web of Science ®Google Scholar
• Rajpert-De Meyts, E., Jacobsen, G. K., Bartkova, J., Aubry, F., Samson, M., Bartek, J., et al. (2003b) The immunohistochemical expression pattern of Chk2, p53, p19INK4d, MAGE-A4 and other selected antigens provides new evidence for the premeiotic origin of spermatocytic seminoma. Histopathology 42:217–226.
   PubMed Web of Science ®Google Scholar
• Rao, M. (2004) Conserved and divergent paths that regulate self-renewal in mouse and human embryonic stem cells. Dev Biol 275:269–286.
   PubMed Web of Science ®Google Scholar
• Rohwedel, J., Guan, K., Hegert, C. and Wobus, A. M. (2001). Embryonic stem cells as an in vitro model for mutagenicity, cytotoxicity and embryotoxicity studies: present state and future prospects. Toxicol In Vitro 15:741–753.
   PubMed Web of Science ®Google Scholar
• Ruggiu, M., Speed, R., Taggart, M., McKay, S. J., Kilanowski, F., Saunders, P., et al. (1997). The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature 389:73–77.
   PubMed Web of Science ®Google Scholar
• Saitou, M., Barton, S. C. and Surani, M. A. (2002) A molecular programme for the specification of germ cell fate in mice. Nature 418:293–300.
   PubMed Web of Science ®Google Scholar
• Sandlow, J. I., Feng, H. L., Zheng, L. J. and Sandra, A. (1999). Migration and ultrastructural localization of the c-kit receptor protein in spermatogenic cells and spermatozoa of the mouse. J Urol 161:1676–1680.
   PubMed Web of Science ®Google Scholar
• Scholz, G., Pohl, I., Genschow, E., Klemm, M. and Spielmann, H. (1999) Embryotoxicity screening using embryonic stem cells in vitro: correlation to in vivo teratogenicity. Cells Tissues Organs 165:203–211.
   PubMed Web of Science ®Google Scholar
• Seiler, A., Visan, A., Buesen, R., Genschow, E. and Spielmann, H. (2004) Improvement of an in vitro stem cell assay for developmental toxicity: the use of molecular endpoints in the embryonic stem cell test. Reprod Toxicol 18:231–240.
   PubMed Web of Science ®Google Scholar
• Silva, C., Wood, J. R., Salvador, L., Zhang, Z., Kostetskii, I., Williams, C. J., et al. (2009). Expression profile of male germ cell-associated genes in mouse embryonic stem cell cultures treated with all-trans retinoic acid and testosterone. Mol Reprod Dev 76:11–21.
   PubMed Web of Science ®Google Scholar
• Skakkebaek, N. E., Rajpert-De Meyts, E. and Main, K. M. (2001) Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod 16:972–978.
   PubMed Web of Science ®Google Scholar
• Smith, A. (2006) A glossary for stem-cell biology. Nature 441:1060.
   Web of Science ®Google Scholar
• Spielmann, H., Bochkov, N. P., Costa, L., Gribaldo, L., Guillouzo, A., Heindel, J. J., et al. (1998). 13th Meeting of the Scientific Group on Methodologies for the Safety Evaluation of Chemicals (SGOMSEC): alternative testing methodologies for organ toxicity. Environ Health Perspect 106(Suppl 2):427-439.
   PubMedGoogle Scholar
• Stuart, J. M., Segal, E., Koller, D. and Kim, S. K. (2003). A gene-coexpression network for global discovery of conserved genetic modules. Science 302:249–255.
   PubMed Web of Science ®Google Scholar
• Suh, M. R., Lee, Y., Kim, J. Y., Kim, S. K., Moon, S. H., Lee, J. Y., et al. (2004). Human embryonic stem cells express a unique set of microRNAs. Dev Biol 270:488–498.
   PubMed Web of Science ®Google Scholar
• Sun, Y., Li, H., Liu, Y., Shin, S., Mattson, M. P., Rao, M. S., et al. (2007). Cross-species transcriptional profiles establish a functional portrait of embryonic stem cells. Genomics 89:22–35.
   PubMed Web of Science ®Google Scholar
• Swan, S. H. (2006) Does our environment affect our fertility? Some examples to help reframe the question. Semin Reprod Med 24:142–146.
   PubMed Web of Science ®Google Scholar
• The Teratology Society (2005). Teratology Primer. Reston, VA: The Teratology Society.
   Google Scholar
• Telisman, S., Cvitkovic, P., Jurasovic, J., Pizent, A., Gavella, M. and Rocic, B. (2000) Semen quality and reproductive endocrine function in relation to biomarkers of lead, cadmium, zinc, and copper in men. Environ Health Perspect 108:45–53.
   PubMed Web of Science ®Google Scholar
• Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S., et al. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282:1145–1147.
   PubMed Web of Science ®Google Scholar
• Tilgner, K., Atkinson, S. P., Golebiewska, A., Stojkovic, M., Lako, M. and Armstrong, L. (2008) Isolation of primordial germ cells from differentiating human embryonic stem cells. Stem Cells 26:3075–3085.
   PubMed Web of Science ®Google Scholar
• Toovey, S., Hudson, E., Hendry, W. F. and Levi, A. J. (1981) Sulphasalazine and male infertility: reversibility and possible mechanism. Gut 22:445–451.
   PubMed Web of Science ®Google Scholar
• Toyooka, Y., Tsunekawa, N., Akasu, R. and Noce, T. (2003) Embryonic stem cells can form germ cells in vitro. Proc Natl Acad Sci USA 100:11457–11462.
   PubMed Web of Science ®Google Scholar
• Toyooka, Y., Tsunekawa, N., Takahashi, Y., Matsui, Y., Satoh, M. and Noce, T. (2000) Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech Dev 93:139–149.
   PubMed Web of Science ®Google Scholar
• Ungrin, M. D., Joshi, C., Nica, A., Bauwens, C. and Zandstra, P. W. (2008). Reproducible, ultra high-throughput formation of multicellular organization from single cell suspension-derived human embryonic stem cell aggregates. PLoS ONE 3:e1565.
   PubMed Web of Science ®Google Scholar
• Vogel, R. (1993) In vitro approach to fertility research: genotoxicity tests on primordial germ cells and embryonic stem cells. Reprod Toxicol 7(Suppl 1):69-73.
   PubMed Web of Science ®Google Scholar
• Wang, Y., Keys, D. N., Au-Young, J. K. and Chen, C. (2009) MicroRNAs in embryonic stem cells. J Cell Physiol 218:251–255.
   PubMed Web of Science ®Google Scholar
• West, F. D., Machacek, D. W., Boyd, N. L., Pandiyan, K., Robbins, K. R. and Stice, S. L. (2008) Enrichment and differentiation of human germ-like cells mediated by feeder cells and basic fibroblast growth factor signaling. Stem Cells 26:2768–2776.
   PubMed Web of Science ®Google Scholar
• Ying, Y., Liu, X. M., Marble, A., Lawson, K. A. and Zhao, G. Q. (2000) Requirement of Bmp8b for the generation of primordial germ cells in the mouse. Mol Endocrinol 14:1053–1063.
   PubMed Web of Science ®Google Scholar
• Ying, Y., Qi, X. and Zhao, G. Q. (2001). Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signaling pathways. Proc Natl Acad Sci USA 98:7858–7862.
   PubMed Web of Science ®Google Scholar
• zur Nieden, N. I., Kempka, G. and Ahr, H. J. (2004). Molecular multiple endpoint embryonic stem cell test–a possible approach to test for the teratogenic potential of compounds. Toxicol Appl Pharmacol 194:257–269.
   PubMed Web of Science ®Google Scholar