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The Role of Maternal-Effect Genes in Mammalian Development: Are Mammalian Embryos Really an Exception?

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Abstract

The essential contribution of multiple maternal factors to early mammalian development is rapidly altering the view that mammals have a unique pattern of development compared to other species. Currently, over 60 maternal-effect mutations have been described in mammalian systems, including critical determinants of pluripotency. This data, combined with the evidence for lineage bias and differential gene expression in early blastomeres, strongly suggests that mammalian development is to some extent mosaic from the four-cell stage onward.

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References

  1. Wennekamp, S., Mesecke, S., Nedelec, F., & Hiiragi, T. (2013). A self-organization framework for symmetry breaking in the mammalian embryo. Nature Reviews Molecular Cell Biology, 14, 452–459.

    Article  PubMed  CAS  Google Scholar 

  2. Lecuyer, E., Yoshida, H., Parthasarathy, N., et al. (2007). Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell, 131, 174–187.

    Article  CAS  PubMed  Google Scholar 

  3. Sulston, J. E., Schierenberg, E., White, J. G., & Thomson, J. N. (1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Developmental Biology, 100, 64–119.

    Article  CAS  PubMed  Google Scholar 

  4. Sulston, J. E., & White, J. G. (1980). Regulation and cell autonomy during postembryonic development of Caenorhabditis elegans. Developmental Biology, 78, 577–597.

    Article  CAS  PubMed  Google Scholar 

  5. Bischoff, M., Parfitt, D. E., & Zernicka-Goetz, M. (2008). Formation of the embryonic-abembryonic axis of the mouse blastocyst: relationships between orientation of early cleavage divisions and pattern of symmetric/asymmetric divisions. Development, 135, 953–962.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Fujimori, T., Kurotaki, Y., Miyazaki, J., & Nabeshima, Y. (2003). Analysis of cell lineage in two- and four-cell mouse embryos. Development, 130, 5113–5122.

    Article  CAS  PubMed  Google Scholar 

  7. Gardner, R. L. (2001). Specification of embryonic axes begins before cleavage in normal mouse development. Development, 128, 839–847.

    CAS  PubMed  Google Scholar 

  8. Gardner, R. L., & Davies, T. J. (2003). The basis and significance of pre-patterning in mammals. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 358, 1331–1338. discussion 8–9.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Gardner, R. L., & Davies, T. J. (2006). An investigation of the origin and significance of bilateral symmetry of the pronuclear zygote in the mouse. Human Reproduction, 21, 492–502.

    Article  CAS  PubMed  Google Scholar 

  10. Piotrowska, K., & Zernicka-Goetz, M. (2001). Role for sperm in spatial patterning of the early mouse embryo. Nature, 409, 517–521.

    Article  CAS  PubMed  Google Scholar 

  11. Plusa, B., Grabarek, J. B., Piotrowska, K., Glover, D. M., & Zernicka-Goetz, M. (2002). Site of the previous meiotic division defines cleavage orientation in the mouse embryo. Nature Cell Biology, 4, 811–815.

    Article  CAS  PubMed  Google Scholar 

  12. Plusa, B., Hadjantonakis, A. K., Gray, D., et al. (2005). The first cleavage of the mouse zygote predicts the blastocyst axis. Nature, 434, 391–395.

    Article  CAS  PubMed  Google Scholar 

  13. Piotrowska, K., Wianny, F., Pedersen, R. A., & Zernicka-Goetz, M. (2001). Blastomeres arising from the first cleavage division have distinguishable fates in normal mouse development. Development, 128, 3739–3748.

    CAS  PubMed  Google Scholar 

  14. Piotrowska-Nitsche, K., Perea-Gomez, A., Haraguchi, S., & Zernicka-Goetz, M. (2005). Four-cell stage mouse blastomeres have different developmental properties. Development, 132, 479–490.

    Article  CAS  PubMed  Google Scholar 

  15. Tabansky, I., Lenarcic, A., Draft, R. W., et al. (2013). Developmental bias in cleavage-stage mouse blastomeres. Current Biology, 23, 21–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Torres-Padilla, M. E., Parfitt, D. E., Kouzarides, T., & Zernicka-Goetz, M. (2007). Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature, 445, 214–218.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Bell, C. E., & Watson, A. J. (2009). SNAI1 and SNAI2 are asymmetrically expressed at the 2-cell stage and become segregated to the TE in the mouse blastocyst. PLoS ONE, 4, e8530.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Hansis, C., Grifo, J. A., & Krey, L. C. (2004). Candidate lineage marker genes in human preimplantation embryos. Reproductive Biomedicine Online, 8, 577–583.

    Article  CAS  PubMed  Google Scholar 

  19. Held, E., Salilew-Wondim, D., Linke, M., et al. (2012). Transcriptome fingerprint of bovine 2-cell stage blastomeres is directly correlated with the individual developmental competence of the corresponding sister blastomere. Biology of Reproduction, 87, 154.

    Article  PubMed  CAS  Google Scholar 

  20. Plachta, N., Bollenbach, T., Pease, S., Fraser, S. E., & Pantazis, P. (2011). Oct4 kinetics predict cell lineage patterning in the early mammalian embryo. Nature Cell Biology, 13, 117–123.

    Article  CAS  PubMed  Google Scholar 

  21. Roberts, R. M., Katayama, M., Magnuson, S. R., Falduto, M. T., & Torres, K. E. (2011). Transcript profiling of individual twin blastomeres derived by splitting two-cell stage murine embryos. Biology of Reproduction, 84, 487–494.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Sun, J. H., Zhang, Y., Yin, B. Y., et al. (2012). Differential expression of Axin1, Cdc25c and Cdkn2d mRNA in 2-cell stage mouse blastomeres. Zygote, 20, 305–310.

    Article  CAS  PubMed  Google Scholar 

  23. Galan, A., Montaner, D., Poo, M. E., et al. (2010). Functional genomics of 5- to 8-cell stage human embryos by blastomere single-cell cDNA analysis. PLoS ONE, 5, e13615.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Hartshorn, C., Eckert, J. J., Hartung, O., & Wangh, L. J. (2007). Single-cell duplex RT-LATE-PCR reveals Oct4 and Xist RNA gradients in 8-cell embryos. BMC Biotechnology, 7, 87.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Jedrusik, A., Parfitt, D. E., Guo, G., et al. (2008). Role of Cdx2 and cell polarity in cell allocation and specification of trophectoderm and inner cell mass in the mouse embryo. Genes & Development, 22, 2692–2706.

    Article  CAS  Google Scholar 

  26. May, A., Kirchner, R., Muller, H., et al. (2009). Multiplex rt-PCR expression analysis of developmentally important genes in individual mouse preimplantation embryos and blastomeres. Biology of Reproduction, 80, 194–202.

    Article  CAS  PubMed  Google Scholar 

  27. Niwa, H., Toyooka, Y., Shimosato, D., et al. (2005). Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell, 123, 917–929.

    Article  CAS  PubMed  Google Scholar 

  28. Skamagki, M., Wicher, K. B., Jedrusik, A., Ganguly, S., & Zernicka-Goetz, M. (2013). Asymmetric localization of Cdx2 mRNA during the first cell-fate decision in early mouse development. Cell Reports, 3, 442–457.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Wang, C. W., Yao, D. S., Horng, S. G., et al. (2004). Feasibility of human telomerase reverse transcriptase mRNA expression in individual blastomeres as an indicator of early embryo development. Journal of Assisted Reproduction and Genetics, 21, 163–168.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Dosch, R. (2015). Next generation mothers: maternal control of germline development in zebrafish. Critical Reviews in Biochemistry and Molecular Biology, 50, 54–68.

    Article  CAS  PubMed  Google Scholar 

  31. Langdon, Y. G., & Mullins, M. C. (2011). Maternal and zygotic control of zebrafish dorsoventral axial patterning. Annual Review of Genetics, 45, 357–377.

    Article  CAS  PubMed  Google Scholar 

  32. Luschnig, S., Moussian, B., Krauss, J., Desjeux, I., Perkovic, J., & Nusslein-Volhard, C. (2004). An F1 genetic screen for maternal-effect mutations affecting embryonic pattern formation in Drosophila melanogaster. Genetics, 167, 325–342.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Bowerman, B. (1998). Maternal control of pattern formation in early Caenorhabditis elegans embryos. Current Topics in Developmental Biology, 39, 73–117.

    Article  CAS  PubMed  Google Scholar 

  34. Hu, M.W., Wang, Z.B., Schatten, H., & Sun, Q.Y. (2012). New understandings on folliculogenesis/oogenesis regulation in mouse as revealed by conditional knockout. Journal of Genetics and Genomics = Yi chuan xue bao, 39,61–8.

  35. Kim, K. H., & Lee, K. A. (2014). Maternal effect genes: findings and effects on mouse embryo development. Clinical and Experimental Reproductive Medicine, 41, 47–61.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Li, L., Zheng, P., & Dean, J. (2010). Maternal control of early mouse development. Development, 137, 859–870.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Matzuk, M. M., & Burns, K. H. (2012). Genetics of mammalian reproduction: modeling the end of the germline. Annual Review of Physiology, 74, 503–528.

    Article  CAS  PubMed  Google Scholar 

  38. Zhang, K., & Smith, G.W. (2015). Maternal control of early embryogenesis in mammals. Reproduction, Fertility and Development.

  39. Christians, E., Davis, A. A., Thomas, S. D., & Benjamin, I. J. (2000). Maternal effect of Hsf1 on reproductive success. Nature, 407, 693–694.

    Article  CAS  PubMed  Google Scholar 

  40. Lee, J. T. (2000). Disruption of imprinted X inactivation by parent-of-origin effects at Tsix. Cell, 103, 17–27.

    Article  CAS  PubMed  Google Scholar 

  41. Tong, Z. B., Gold, L., Pfeifer, K. E., et al. (2000). Mater, a maternal effect gene required for early embryonic development in mice. Nature Genetics, 26, 267–268.

    Article  CAS  PubMed  Google Scholar 

  42. Tong, Z. B., Nelson, L. M., & Dean, J. (2000). Mater encodes a maternal protein in mice with a leucine-rich repeat domain homologous to porcine ribonuclease inhibitor. Mammalian Genome, 11, 281–287.

    Article  CAS  PubMed  Google Scholar 

  43. Leader, B., Lim, H., Carabatsos, M. J., et al. (2002). Formin-2, polyploidy, hypofertility and positioning of the meiotic spindle in mouse oocytes. Nature Cell Biology, 4, 921–928.

    Article  CAS  PubMed  Google Scholar 

  44. Rother, F., Shmidt, T., Popova, E., et al. (2011). Importin alpha7 is essential for zygotic genome activation and early mouse development. PLoS ONE, 6, e18310.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Lingenfelter, B. M., Tripurani, S. K., Tejomurtula, J., Smith, G. W., & Yao, J. (2011). Molecular cloning and expression of bovine nucleoplasmin 2 (NPM2): a maternal effect gene regulated by miR-181a. Reproductive Biology and Endocrinology, 9, 40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Burns, K. H., Viveiros, M. M., Ren, Y., et al. (2003). Roles of NPM2 in chromatin and nucleolar organization in oocytes and embryos. Science, 300, 633–636.

    Article  CAS  PubMed  Google Scholar 

  47. Narducci, M. G., Fiorenza, M. T., Kang, S. M., et al. (2002). TCL1 participates in early embryonic development and is overexpressed in human seminomas. Proceedings of the National Academy of Sciences of the United States of America, 99, 11712–11717.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Guglielmino, M. R., Santonocito, M., Vento, M., et al. (2011). TAp73 is downregulated in oocytes from women of advanced reproductive age. Cell Cycle, 10, 3253–3256.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Tomasini, R., Tsuchihara, K., Tsuda, C., et al. (2009). TAp73 regulates the spindle assembly checkpoint by modulating BubR1 activity. Proceedings of the National Academy of Sciences of the United States of America, 106, 797–802.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Tomasini, R., Tsuchihara, K., Wilhelm, M., et al. (2008). TAp73 knockout shows genomic instability with infertility and tumor suppressor functions. Genes & Development, 22, 2677–2691.

    Article  CAS  Google Scholar 

  51. Hu, J., Wang, F., Zhu, X., Yuan, Y., Ding, M., & Gao, S. (2010). Mouse ZAR1-like (XM_359149) colocalizes with mRNA processing components and its dominant-negative mutant caused two-cell-stage embryonic arrest. Developmental Dynamics, 239, 407–424.

    Article  CAS  PubMed  Google Scholar 

  52. Wu, X., Viveiros, M. M., Eppig, J. J., Bai, Y., Fitzpatrick, S. L., & Matzuk, M. M. (2003). Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nature Genetics, 33, 187–191.

    Article  CAS  PubMed  Google Scholar 

  53. Lykke-Andersen, K., Gilchrist, M. J., Grabarek, J. B., Das, P., Miska, E., & Zernicka-Goetz, M. (2008). Maternal Argonaute 2 is essential for early mouse development at the maternal-zygotic transition. Molecular Biology of the Cell, 19, 4383–4392.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Tsukamoto, S., Kuma, A., & Mizushima, N. (2008). The role of autophagy during the oocyte-to-embryo transition. Autophagy, 4, 1076–1078.

    Article  PubMed  Google Scholar 

  55. Tsukamoto, S., Kuma, A., Murakami, M., Kishi, C., Yamamoto, A., & Mizushima, N. (2008). Autophagy is essential for preimplantation development of mouse embryos. Science, 321, 117–120.

    Article  CAS  PubMed  Google Scholar 

  56. Murchison, E. P., Stein, P., Xuan, Z., et al. (2007). Critical roles for Dicer in the female germline. Genes & Development, 21, 682–693.

    Article  CAS  Google Scholar 

  57. Mohan, K. N., Ding, F., & Chaillet, J. R. (2011). Distinct roles of DMAP1 in mouse development. Molecular and Cellular Biology, 31, 1861–1869.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Cirio, M. C., Martel, J., Mann, M., et al. (2008). DNA methyltransferase 1o functions during preimplantation development to preclude a profound level of epigenetic variation. Developmental Biology, 324, 139–150.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Hirasawa, R., Chiba, H., Kaneda, M., et al. (2008). Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes & Development, 22, 1607–1616.

    Article  CAS  Google Scholar 

  60. Howell, C. Y., Bestor, T. H., Ding, F., et al. (2001). Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell, 104, 829–838.

    Article  CAS  PubMed  Google Scholar 

  61. McGraw, S., Oakes, C. C., Martel, J., et al. (2013). Loss of DNMT1o disrupts imprinted X chromosome inactivation and accentuates placental defects in females. PLoS Genetics, 9, e1003873.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Shinagawa, T., Takagi, T., Tsukamoto, D., et al. (2014). Histone variants enriched in oocytes enhance reprogramming to induced pluripotent stem cells. Cell Stem Cell, 14, 217–227.

    Article  CAS  PubMed  Google Scholar 

  63. Arnold, D. R., Francon, P., Zhang, J., Martin, K., & Clarke, H. J. (2008). Stem-loop binding protein expressed in growing oocytes is required for accumulation of mRNAs encoding histones H3 and H4 and for early embryonic development in the mouse. Developmental Biology, 313, 347–358.

    Article  CAS  PubMed  Google Scholar 

  64. Ciccone, D. N., Su, H., Hevi, S., et al. (2009). KDM1B is a histone H3K4 demethylase required to establish maternal genomic imprints. Nature, 461, 415–418.

    Article  CAS  PubMed  Google Scholar 

  65. Foygel, K., Choi, B., Jun, S., et al. (2008). A novel and critical role for Oct4 as a regulator of the maternal-embryonic transition. PLoS ONE, 3, e4109.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Zimmerman, D. L., Boddy, C. S., & Schoenherr, C. S. (2013). Oct4/Sox2 binding sites contribute to maintaining hypomethylation of the maternal igf2/h19 imprinting control region. PLoS ONE, 8, e81962.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Zuccotti, M., Merico, V., Sacchi, L., et al. (2008). Maternal Oct-4 is a potential key regulator of the developmental competence of mouse oocytes. BMC Developmental Biology, 8, 97.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Posfai, E., Kunzmann, R., Brochard, V., et al. (2012). Polycomb function during oogenesis is required for mouse embryonic development. Genes & Development, 26, 920–932.

    Article  CAS  Google Scholar 

  69. Zhang, W., Poirier, L., Diaz, M. M., Bordignon, V., & Clarke, H. J. (2009). Maternally encoded stem-loop-binding protein is degraded in 2-cell mouse embryos by the co-ordinated activity of two separately regulated pathways. Developmental Biology, 328, 140–147.

    Article  CAS  PubMed  Google Scholar 

  70. Avilion, A. A., Nicolis, S. K., Pevny, L. H., Perez, L., Vivian, N., & Lovell-Badge, R. (2003). Multipotent cell lineages in early mouse development depend on SOX2 function. Genes & Development, 17, 126–140.

    Article  CAS  Google Scholar 

  71. Gu, T. P., Guo, F., Yang, H., et al. (2011). The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature, 477, 606–610.

    Article  CAS  PubMed  Google Scholar 

  72. Torres-Padilla, M. E., & Zernicka-Goetz, M. (2006). Role of TIF1alpha as a modulator of embryonic transcription in the mouse zygote. The Journal of Cell Biology, 174, 329–338.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Messerschmidt, D. M. (2012). Should I, stay or should I go: protection and maintenance of DNA methylation at imprinted genes. Epigenetics, 7, 969–975.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Messerschmidt, D. M., de Vries, W., Ito, M., Solter, D., Ferguson-Smith, A., & Knowles, B. B. (2012). Trim28 is required for epigenetic stability during mouse oocyte to embryo transition. Science, 335, 1499–1502.

    Article  CAS  PubMed  Google Scholar 

  75. Strogantsev, R., & Ferguson-Smith, A. C. (2012). Proteins involved in establishment and maintenance of imprinted methylation marks. Briefings in Functional Genomics, 11, 227–239.

    Article  CAS  PubMed  Google Scholar 

  76. Kaneda, M., Hirasawa, R., Chiba, H., Okano, M., Li, E., & Sasaki, H. (2010). Genetic evidence for Dnmt3a-dependent imprinting during oocyte growth obtained by conditional knockout with Zp3-Cre and complete exclusion of Dnmt3b by chimera formation. Genes Cells.

  77. Kaneda, M., Okano, M., Hata, K., et al. (2004). Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature, 429, 900–903.

    Article  CAS  PubMed  Google Scholar 

  78. Bourc’his, D., Xu, G. L., Lin, C. S., Bollman, B., & Bestor, T. H. (2001). Dnmt3L and the establishment of maternal genomic imprints. Science, 294, 2536–2539.

    Article  PubMed  Google Scholar 

  79. Hata, K., Okano, M., Lei, H., & Li, E. (2002). Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development, 129, 1983–1993.

    CAS  PubMed  Google Scholar 

  80. Bortvin, A., Goodheart, M., Liao, M., & Page, D. C. (2004). Dppa3 / Pgc7 / stella is a maternal factor and is not required for germ cell specification in mice. BMC Developmental Biology, 4, 2.

    Article  PubMed  PubMed Central  Google Scholar 

  81. Liu, Y. J., Nakamura, T., & Nakano, T. (2012). Essential role of DPPA3 for chromatin condensation in mouse oocytogenesis. Biology of Reproduction, 86, 40.

    Article  PubMed  CAS  Google Scholar 

  82. Nakamura, T., Liu, Y. J., Nakashima, H., et al. (2012). PGC7 binds histone H3K9me2 to protect against conversion of 5mC to 5hmC in early embryos. Nature, 486, 415–419.

    CAS  PubMed  Google Scholar 

  83. Payer, B., Saitou, M., Barton, S. C., et al. (2003). Stella is a maternal effect gene required for normal early development in mice. Current Biology, 13, 2110–2117.

    Article  CAS  PubMed  Google Scholar 

  84. Denomme, M. M., White, C. R., Gillio-Meina, C., et al. (2012). Compromised fertility disrupts Peg1 but not Snrpn and Peg3 imprinted methylation acquisition in mouse oocytes. Frontiers in Genetics, 3, 129.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Fallahian, M., Sebire, N. J., Savage, P. M., Seckl, M. J., & Fisher, R. A. (2013). Mutations in NLRP7 and KHDC3L confer a complete hydatidiform mole phenotype on digynic triploid conceptions. Human Mutation, 34, 301–308.

    Article  CAS  PubMed  Google Scholar 

  86. Mahadevan, S., Wen, S., Wan, Y. W., et al. (2014). NLRP7 affects trophoblast lineage differentiation, binds to overexpressed YY1 and alters CpG methylation. Human Molecular Genetics, 23, 706–716.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Reddy, R., Akoury, E., Phuong Nguyen, N. M., et al. (2013). Report of four new patients with protein-truncating mutations in C6orf221/KHDC3L and colocalization with NLRP7. European Journal of Human Genetics, 21, 957–964.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Court, F., Martin-Trujillo, A., Romanelli, V., et al. (2013). Genome-wide allelic methylation analysis reveals disease-specific susceptibility to multiple methylation defects in imprinting syndromes. Human Mutation, 34, 595–602.

    CAS  PubMed  Google Scholar 

  89. Peng, H., Chang, B., Lu, C., et al. (2012). Nlrp2, a maternal effect gene required for early embryonic development in the mouse. PLoS ONE, 7, e30344.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Mahadevan, S., Wen, S., Balasa, A., et al. (2013). No evidence for mutations in NLRP7 and KHDC3L in women with androgenetic hydatidiform moles. Prenatal Diagnosis, 33, 1242–1247.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Mahadevan, S., Wen, S., Wan, Y.W., et al. (2013). NLRP7 affects trophoblast lineage differentiation, binds to overexpressed YY1 and alters CpG methylation. Human Molecular Genetics.

  92. Andreasen, L., Christiansen, O. B., Niemann, I., Bolund, L., & Sunde, L. (2013). NLRP7 or KHDC3L genes and the etiology of molar pregnancies and recurrent miscarriage. Molecular Human Reproduction, 19, 773–781.

    Article  CAS  PubMed  Google Scholar 

  93. Parry, D. A., Logan, C. V., Hayward, B. E., et al. (2011). Mutations causing familial biparental hydatidiform mole implicate c6orf221 as a possible regulator of genomic imprinting in the human oocyte. American Journal of Human Genetics, 89, 451–458.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Ulker, V., Gurkan, H., Tozkir, H., et al. (2013). Novel NLRP7 mutations in familial recurrent hydatidiform mole: are NLRP7 mutations a risk for recurrent reproductive wastage? European Journal of Obstetrics, Gynecology, and Reproductive Biology, 170, 188–192.

    Article  CAS  PubMed  Google Scholar 

  95. Ohsugi, M., Zheng, P., Baibakov, B., Li, L., & Dean, J. (2008). Maternally derived FILIA-MATER complex localizes asymmetrically in cleavage-stage mouse embryos. Development, 135, 259–269.

    Article  CAS  PubMed  Google Scholar 

  96. Wang, J., Xu, M., Zhu, K., Li, L., & Liu, X. (2012). The N-terminus of FILIA forms an atypical KH domain with a unique extension involved in interaction with RNA. PLoS ONE, 7, e30209.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Zheng, P., & Dean, J. (2009). Role of Filia, a maternal effect gene, in maintaining euploidy during cleavage-stage mouse embryogenesis. Proceedings of the National Academy of Sciences of the United States of America, 106, 7473–7478.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Fernandes, R., Tsuda, C., Perumalsamy, A. L., et al. (2012). NLRP5 mediates mitochondrial function in mouse oocytes and embryos. Biology of Reproduction, 86(138), 1–10.

    Google Scholar 

  99. Kim, B., Kan, R., Anguish, L., Nelson, L. M., & Coonrod, S. A. (2010). Potential role for MATER in cytoplasmic lattice formation in murine oocytes. PLoS ONE, 5, e12587.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. Pisani, L. F., Ramelli, P., Lazzari, B., Braglia, S., Ceciliani, F., & Mariani, P. (2010). Characterization of maternal antigen that embryos require (MATER/NLRP5) gene and protein in pig somatic tissues and germ cells. Journal of Reproduction and Development, 56, 41–48.

    Article  CAS  PubMed  Google Scholar 

  101. Wu, X. (2009). Maternal depletion of NLRP5 blocks early embryogenesis in rhesus macaque monkeys (Macaca mulatta). Human Reproduction, 24, 415–424.

    Article  CAS  PubMed  Google Scholar 

  102. Kim, B., Zhang, X., Kan, R., et al. (2014). The role of MATER in endoplasmic reticulum distribution and calcium homeostasis in mouse oocytes. Developmental Biology, 386, 331–339.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Li, L., Baibakov, B., & Dean, J. (2008). A subcortical maternal complex essential for preimplantation mouse embryogenesis. Developmental Cell, 15, 416–425.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Tashiro, F., Kanai-Azuma, M., Miyazaki, S., et al. (2010). Maternal-effect gene Ces5/Ooep/Moep19/Floped is essential for oocyte cytoplasmic lattice formation and embryonic development at the maternal-zygotic stage transition. Genes to Cells, 15, 813–828.

    Article  CAS  PubMed  Google Scholar 

  105. Zhao, B., Cun, Y. X., He, X. C., & Zheng, P. (2013). Maternal-effect Floped gene is essential for the derivation of embryonic stem cells in mice. Dongwuxue Yanjiu, 34, E82–E86.

    CAS  PubMed  Google Scholar 

  106. Esposito, G., Vitale, A. M., Leijten, F. P., et al. (2007). Peptidylarginine deiminase (PAD) 6 is essential for oocyte cytoskeletal sheet formation and female fertility. Molecular and Cellular Endocrinology, 273, 25–31.

    Article  CAS  PubMed  Google Scholar 

  107. Kan, R., Yurttas, P., Kim, B., et al. (2011). Regulation of mouse oocyte microtubule and organelle dynamics by PADI6 and the cytoplasmic lattices. Developmental Biology, 350, 311–322.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Yurttas, P., Vitale, A. M., Fitzhenry, R. J., et al. (2008). Role for PADI6 and the cytoplasmic lattices in ribosomal storage in oocytes and translational control in the early mouse embryo. Development, 135, 2627–2636.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Duncan, F.E., Padilla-Banks, E., Bernhardt, M.L., et al. (2014). Transducin-like enhancer of split-6 (TLE6) is a substrate of protein kinase A activity during mouse oocyte maturation. Biology of Reproduction.

  110. Ma, J., Zeng, F., Schultz, R. M., & Tseng, H. (2006). Basonuclin: a novel mammalian maternal-effect gene. Development, 133, 2053–2062.

    Article  CAS  PubMed  Google Scholar 

  111. Philipps, D. L., Wigglesworth, K., Hartford, S. A., et al. (2008). The dual bromodomain and WD repeat-containing mouse protein BRWD1 is required for normal spermiogenesis and the oocyte-embryo transition. Developmental Biology, 317, 72–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Wan, L. B., Pan, H., Hannenhalli, S., et al. (2008). Maternal depletion of CTCF reveals multiple functions during oocyte and preimplantation embryo development. Development, 135, 2729–2738.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Hu, W., Gauthier, L., Baibakov, B., Jimenez-Movilla, M., & Dean, J. (2010). FIGLA, a basic helix-loop-helix transcription factor, balances sexually dimorphic gene expression in postnatal oocytes. Molecular and Cellular Biology, 30, 3661–3671.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Tripurani, S.K., Wee, G., Lee, K.B., Smith, G.W., Wang, L., & Jianboyao (2013). MicroRNA-212 post-transcriptionally regulates oocyte-specific basic-helix-loop-helix Transcription factor, factor in the germline alpha (FIGLA), during bovine early embryogenesis. PLoS ONE, 8, e76114.

  115. Tosh, D., Rani, H. S., Murty, U. S., Deenadayal, A., & Grover, P. (2015). Mutational analysis of the FIGLA gene in women with idiopathic premature ovarian failure. Menopause, 22, 520–526.

    Article  PubMed  Google Scholar 

  116. Lin, C. J., Koh, F. M., Wong, P., Conti, M., & Ramalho-Santos, M. (2014). Hira-mediated H3.3 incorporation is required for DNA replication and ribosomal RNA transcription in the mouse zygote. Developmental Cell, 30, 268–279.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Andreu-Vieyra, C.V., Chen, R., Agno, J.E., et al. (2010). MLL2 is required in oocytes for bulk histone 3 lysine 4 trimethylation and transcriptional silencing. PLoS Biology, 8.

  118. Tripurani, S. K., Lee, K. B., Wee, G., Smith, G. W., & Yao, J. (2011). MicroRNA-196a regulates bovine newborn ovary homeobox gene (NOBOX) expression during early embryogenesis. BMC Developmental Biology, 11, 25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Tripurani, S. K., Lee, K. B., Wang, L., et al. (2011). A novel functional role for the oocyte-specific transcription factor newborn ovary homeobox (NOBOX) during early embryonic development in cattle. Endocrinology, 152, 1013–1023.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Zheng, W., Gorre, N., Shen, Y., et al. (2010). Maternal phosphatidylinositol 3-kinase signalling is crucial for embryonic genome activation and preimplantation embryogenesis. EMBO Reports, 11, 890–895.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Ma, J. Y., Li, M., Luo, Y. B., et al. (2013). Maternal factors required for oocyte developmental competence in mice: transcriptome analysis of non-surrounded nucleolus (NSN) and surrounded nucleolus (SN) oocytes. Cell Cycle, 12, 1928–1938.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Kim, K. H., Kim, E. Y., & Lee, K. A. (2008). SEBOX is essential for early embryogenesis at the two-cell stage in the mouse. Biology of Reproduction, 79, 1192–1201.

    Article  CAS  PubMed  Google Scholar 

  123. Zheng, Z., Zhao, M. H., Jia, J. L., et al. (2013). Knockdown of maternal homeobox transcription factor SEBOX gene impaired early embryonic development in porcine parthenotes. Journal of Reproduction and Development, 59, 557–562.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Bultman, S. J., Gebuhr, T. C., Pan, H., Svoboda, P., Schultz, R. M., & Magnuson, T. (2006). Maternal BRG1 regulates zygotic genome activation in the mouse. Genes & Development, 20, 1744–1754.

    Article  CAS  Google Scholar 

  125. Ramos, S. B., Stumpo, D. J., Kennington, E. A., et al. (2004). The CCCH tandem zinc-finger protein Zfp36l2 is crucial for female fertility and early embryonic development. Development, 131, 4883–4893.

    Article  CAS  PubMed  Google Scholar 

  126. Li, X., Ito, M., Zhou, F., et al. (2008). A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints. Developmental Cell, 15, 547–557.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Xu, Q., Wang, F., Xiang, Y., et al. (2015). Maternal BCAS2 protects genomic integrity in mouse early embryonic development. Development, 142, 3943–3953.

    Article  CAS  PubMed  Google Scholar 

  128. Gurtu, V. E., Verma, S., Grossmann, A. H., Liskay, R. M., Skarnes, W. C., & Baker, S. M. (2002). Maternal effect for DNA mismatch repair in the mouse. Genetics, 160, 271–277.

    CAS  PubMed  PubMed Central  Google Scholar 

  129. Shin, J., Bossenz, M., Chung, Y., et al. (2010). Maternal Rnf12/RLIM is required for imprinted X-chromosome inactivation in mice. Nature, 467, 977–981.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Roest, H. P., Baarends, W. M., de Wit, J., et al. (2004). The ubiquitin-conjugating DNA repair enzyme HR6A is a maternal factor essential for early embryonic development in mice. Molecular and Cellular Biology, 24, 5485–5495.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Mtango, N. R., Sutovsky, M., Susor, A., Zhong, Z., Latham, K. E., & Sutovsky, P. (2012). Essential role of maternal UCHL1 and UCHL3 in fertilization and preimplantation embryo development. Journal of Cellular Physiology, 227, 1592–1603.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Sekiguchi, S., Kwon, J., Yoshida, E., et al. (2006). Localization of ubiquitin C-terminal hydrolase L1 in mouse ova and its function in the plasma membrane to block polyspermy. American Journal of Pathology, 169, 1722–1729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Angulo, L., Perreau, C., Lakhdari, N., et al. (2013). Breast-cancer anti-estrogen resistance 4 (BCAR4) encodes a novel maternal-effect protein in bovine and is expressed in the oocyte of humans and other non-rodent mammals. Human Reproduction, 28, 430–441.

    Article  CAS  PubMed  Google Scholar 

  134. Kim, K. H., Kim, E. Y., Kim, Y., et al. (2011). Gas6 downregulation impaired cytoplasmic maturation and pronuclear formation independent to the MPF activity. PLoS ONE, 6, e23304.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Nakamura, B. N., Fielder, T. J., Hoang, Y. D., et al. (2011). Lack of maternal glutamate cysteine ligase modifier subunit (Gclm) decreases oocyte glutathione concentrations and disrupts preimplantation development in mice. Endocrinology, 152, 2806–2815.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Kloc, M., Jaglarz, M., Dougherty, M., Stewart, M. D., Nel-Themaat, L., & Bilinski, S. (2008). Mouse early oocytes are transiently polar: three-dimensional and ultrastructural analysis. Experimental Cell Research, 314, 3245–3254.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Elkouby, Y. M., Jamieson-Lucy, A., & Mullins, M. C. (2016). Oocyte polarization is coupled to the chromosomal bouquet, a conserved polarized nuclear configuration in meiosis. PLoS Biology, 14, e1002335.

    Article  PubMed  PubMed Central  Google Scholar 

  138. Zernicka-Goetz, M. (2005). Cleavage pattern and emerging asymmetry of the mouse embryo. Nature Reviews Molecular Cell Biology, 6, 919–928.

    Article  CAS  PubMed  Google Scholar 

  139. Bontems, F., Stein, A., Marlow, F., et al. (2009). Bucky ball organizes germ plasm assembly in zebrafish. Current Biology, 19, 414–422.

    Article  CAS  PubMed  Google Scholar 

  140. Kumano, G. (2012). Polarizing animal cells via mRNA localization in oogenesis and early development. Development, Growth & Differentiation, 54, 1–18.

    Article  CAS  Google Scholar 

  141. Forbes, M. M., Rothhamel, S., Jenny, A., & Marlow, F. L. (2015). Maternal dazap2 regulates germ granules by counteracting dynein in zebrafish primordial germ cells. Cell Reports, 12, 49–57.

    Article  CAS  PubMed  Google Scholar 

  142. Suwinska, A., Czolowska, R., Ozdzenski, W., & Tarkowski, A. K. (2008). Blastomeres of the mouse embryo lose totipotency after the fifth cleavage division: expression of Cdx2 and Oct4 and developmental potential of inner and outer blastomeres of 16- and 32-cell embryos. Developmental Biology, 322, 133–144.

    Article  CAS  PubMed  Google Scholar 

  143. Samarage, C. R., White, M. D., Alvarez, Y. D., et al. (2015). Cortical tension allocates the first inner cells of the mammalian embryo. Developmental Cell, 34, 435–447.

    Article  CAS  PubMed  Google Scholar 

  144. Blij, S., Frum, T., Akyol, A., Fearon, E., & Ralston, A. (2012). Maternal Cdx2 is dispensable for mouse development. Development, 139, 3969–3972.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Jedrusik, A., Cox, A., Wicher, K., Glover, D. M., & Zernicka-Goetz, M. (2015). Maternal-zygotic knockout reveals a critical role of Cdx2 in the morula to blastocyst transition. Developmental Biology, 398, 147–152.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Grobstein, C. (1979). External human fertilization. Scientific American, 240, 57–67.

    Article  CAS  PubMed  Google Scholar 

  147. Ferrer Colomer, M., & Pastor, L. M. (2012). The preembryo’s short lifetime. The history of a word. Cuadernos de Bioética, 23, 677–694.

    PubMed  Google Scholar 

  148. Vivanco, L., Bartolomé, B., Martín, M. S., & Martínez, A. (2011). Bibliometric analysis of the use of the term preembryo in scientific literature. Journal of the American Society for Information Science, 62, 987–991.

    Article  Google Scholar 

  149. Gilbert, S. F., Tyler, A. L., & Zackin, E. J. (2005). Bioethics and the new embryology; Springboards for debate. Sunderland, MA: Sinauer Associates.

    Google Scholar 

  150. Hallgrímsson, B., & Hall, B. K. (Eds.). (2011). Epigenetics linking genotype and phenotype in development and evolution. Berkeley: University of California Press.

    Google Scholar 

  151. Price, F. E. (2011). The law of life and death. Cambridge: Harvard University Press.

    Google Scholar 

  152. Condic, M. L. (2014). Totipotency: what it is and what it is not. Stem Cells and Development, 23, 796–812.

    Article  PubMed  PubMed Central  Google Scholar 

  153. Condic, M. L. (2014). When does human life begin? The scientific evidence and terminology revisited. Journal of Law and Public Policy, 8, 44–81.

    Google Scholar 

  154. Li, L., Lu, X., & Dean, J. (2013). The maternal to zygotic transition in mammals. Molecular Aspects of Medicine, 34, 919–938.

    Article  PubMed  PubMed Central  Google Scholar 

  155. McGinnis, L. K., Luo, J., & Kinsey, W. H. (2013). Protein tyrosine kinase signaling in the mouse oocyte cortex during sperm-egg interactions and anaphase resumption. Molecular Reproduction and Development, 80, 260–272.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

I thank Dr. H.J. Yost for suggestions on the manuscript.

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  1. Department of Neurobiology, School of Medicine, University of Utah, 20 South 2030 East, Bldg. 570 BPRB, Salt Lake City, UT, 84112, USA

    Maureen L. Condic

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Condic, M.L. The Role of Maternal-Effect Genes in Mammalian Development: Are Mammalian Embryos Really an Exception?. Stem Cell Rev and Rep 12, 276–284 (2016). https://doi.org/10.1007/s12015-016-9648-6

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