Advertisement

Zygotic genome activation in the chicken: a comparative review

  • Deivendran Rengaraj
  • Young Sun Hwang
  • Hyung Chul Lee
  • Jae Yong HanEmail author
Review

Abstract

Maternal RNAs and proteins in the oocyte contribute to early embryonic development. After fertilization, these maternal factors are cleared and embryonic development is determined by an individual’s own RNAs and proteins, in a process called the maternal-to-zygotic transition. Zygotic transcription is initially inactive, but is eventually activated by maternal transcription factors. The timing and molecular mechanisms involved in zygotic genome activation (ZGA) have been well-described in many species. Among birds, a transcriptome-based understanding of ZGA has only been explored in chickens by RNA sequencing of intrauterine embryos. RNA sequencing of chicken intrauterine embryos, including oocytes, zygotes, and Eyal-Giladi and Kochav (EGK) stages I–X has enabled the identification of differentially expressed genes between consecutive stages. These studies have revealed that there are two waves of ZGA: a minor wave at the one-cell stage (shortly after fertilization) and a major wave between EGK.III and EGK.VI (during cellularization). In the chicken, the maternal genome is activated during minor ZGA and the paternal genome is quiescent until major ZGA to avoid transcription from supernumerary sperm nuclei. In this review, we provide a detailed overview of events in intrauterine embryonic development in birds (and particularly in chickens), as well as a transcriptome-based analysis of ZGA.

Keywords

Avian species Genome activation Intrauterine embryos Maternal-to-zygotic transition 

Notes

Acknowledgements

This work was supported by the National Research Foundation of Korea (NRF) Grant 2015 R1A3A2033826 (Ministry of Science, Information and Communication Technology, and Future Planning; MSIP) and the Cooperative Research Program for Agriculture Science and Technology Development (Project PJ0144612019) from the Korean Rural Development Administration.

Author contributions

The study was designed by DR and JYH. The manuscript was drafted by DR and YSH. The content in the manuscript was critically checked by HCL and JYH. All the authors checked and gave their approval of this version to be published.

Compliance with ethical standards

Conflict of interest

All the authors declare that they have no competing interests.

References

  1. 1.
    Memili E, First NL (2000) Zygotic and embryonic gene expression in cow: a review of timing and mechanisms of early gene expression as compared with other species. Zygote 8(1):87–96PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Edgar LG, Wolf N, Wood WB (1994) Early transcription in Caenorhabditis elegans embryos. Development 120(2):443–451PubMedPubMedCentralGoogle Scholar
  3. 3.
    Aoki F, Worrad DM, Schultz RM (1997) Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev Biol 181(2):296–307PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Mathavan S, Lee SG, Mak A, Miller LD, Murthy KR, Govindarajan KR, Tong Y, Wu YL, Lam SH, Yang H, Ruan Y, Korzh V, Gong Z, Liu ET, Lufkin T (2005) Transcriptome analysis of zebrafish embryogenesis using microarrays. PLoS Genet 1(2):260–276PubMedCrossRefPubMedCentralGoogle Scholar
  5. 5.
    Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, Van Dongen S, Inoue K, Enright AJ, Schier AF (2006) Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312(5770):75–79PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Aanes H, Winata CL, Lin CH, Chen JP, Srinivasan KG, Lee SG, Lim AY, Hajan HS, Collas P, Bourque G, Gong Z, Korzh V, Alestrom P, Mathavan S (2011) Zebrafish mRNA sequencing deciphers novelties in transcriptome dynamics during maternal to zygotic transition. Genome Res 21(8):1328–1338PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Xue Z, Huang K, Cai C, Cai L, Jiang CY, Feng Y, Liu Z, Zeng Q, Cheng L, Sun YE, Liu JY, Horvath S, Fan G (2013) Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature 500(7464):593–597PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Yan L, Yang M, Guo H, Yang L, Wu J, Li R, Liu P, Lian Y, Zheng X, Yan J, Huang J, Li M, Wu X, Wen L, Lao K, Li R, Qiao J, Tang F (2013) Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat Struct Mol Biol 20(9):1131–1139PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Harrison MM, Eisen MB (2015) Transcriptional activation of the zygotic genome in Drosophila. Curr Top Dev Biol 113:85–112PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    Oda-Ishii I, Satou Y (2018) Initiation of the zygotic genetic program in the ascidian embryo. Semin Cell Dev Biol 84:111–117PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Sheng G (2014) Day-1 chick development. Dev Dyn 243(3):357–367PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Nagai H, Sezaki M, Kakiguchi K, Nakaya Y, Lee HC, Ladher R, Sasanami T, Han JY, Yonemura S, Sheng G (2015) Cellular analysis of cleavage-stage chick embryos reveals hidden conservation in vertebrate early development. Development 142(7):1279–1286PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Hwang YS, Seo M, Choi HJ, Kim SK, Kim H, Han JY (2018) The first whole transcriptomic exploration of pre-oviposited early chicken embryos using single and bulked embryonic RNA-sequencing. Gigascience 7(4):1–9PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Hwang YS, Seo M, Lee BR, Lee HJ, Park YH, Kim SK, Lee HC, Choi HJ, Yoon J, Kim H, Han JY (2018) The transcriptome of early chicken embryos reveals signaling pathways governing rapid asymmetric cellularization and lineage segregation. Development 145(6):157453CrossRefGoogle Scholar
  15. 15.
    Hwang YS, Seo M, Bang S, Kim H, Han JY (2018) Transcriptional and translational dynamics during maternal-to-zygotic transition in early chicken development. FASEB J 32(4):2004–2011PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Hwang YS, Seo M, Kim SK, Bang S, Kim H, Han JY (2018) Zygotic gene activation in the chicken occurs in two waves, the first involving only maternally derived genes. Elife 7:e39381PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Villegas J, Kehr K, Soto L, Henkel R, Miska W, Sanchez R (2003) Reactive oxygen species induce reversible capacitation in human spermatozoa. Andrologia 35(4):227–232PubMedCrossRefGoogle Scholar
  18. 18.
    Younglai EV, Holloway AC, Foster WG (2005) Environmental and occupational factors affecting fertility and IVF success. Hum Reprod Update 11(1):43–57PubMedCrossRefGoogle Scholar
  19. 19.
    Rengaraj D, Kwon WS, Pang MG (2015) Effects of motor vehicle exhaust on male reproductive function and associated proteins. J Proteome Res 14(1):22–37PubMedCrossRefGoogle Scholar
  20. 20.
    Rengaraj D, Hong YH (2015) Effects of dietary vitamin E on fertility functions in poultry species. Int J Mol Sci 16(5):9910–9921PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Aitken RJ (2018) Not every sperm is sacred; a perspective on male infertility. Mol Hum Reprod 24(6):287–298PubMedPubMedCentralGoogle Scholar
  22. 22.
    Kumar S, Mishra V, Thaker R, Gor M, Perumal S, Joshi P, Sheth H, Shaikh I, Gautam AK, Verma Y (2018) Role of environmental factors & oxidative stress with respect to in vitro fertilization outcome. Indian J Med Res 148(Suppl):S125–S133PubMedPubMedCentralGoogle Scholar
  23. 23.
    Bakst MR (1998) Structure of the avian oviduct with emphasis on sperm storage in poultry. J Exp Zool 282(4–5):618–626PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Brillard JP (1993) Sperm storage and transport following natural mating and artificial insemination. Poult Sci 72(5):923–928PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Sasanami T, Matsuzaki M, Mizushima S, Hiyama G (2013) Sperm storage in the female reproductive tract in birds. J Reprod Dev 59(4):334–338PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Lovell TM, Gladwell RT, Groome NP, Knight PG (2003) Ovarian follicle development in the laying hen is accompanied by divergent changes in inhibin A, inhibin B, activin A and follistatin production in granulosa and theca layers. J Endocrinol 177(1):45–55PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Johnson AL (2015) Reproduction in the female. In: Scanes CG (ed) Sturkie’s avian physiology, 6th edn. Elsevier, London, pp 635–665CrossRefGoogle Scholar
  28. 28.
    Yoshimura Y, Barua A (2017) Female reproductive system and immunology. Adv Exp Med Biol 1001:33–57PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Wyburn GM, Aitken RN, Johnston HS (1965) The ultrastructure of the zona radiata of the ovarian follicle of the domestic fowl. J Anat 99(Pt 3):469–484PubMedPubMedCentralGoogle Scholar
  30. 30.
    Nishio S, Kohno Y, Iwata Y, Arai M, Okumura H, Oshima K, Nadano D, Matsuda T (2014) Glycosylated chicken ZP2 accumulates in the egg coat of immature oocytes and remains localized to the germinal disc region of mature eggs. Biol Reprod 91(5):107PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Perry MM (1987) Nuclear events from fertilisation to the early cleavage stages in the domestic fowl (Gallus domesticus). J Anat 150:99–109PubMedPubMedCentralGoogle Scholar
  32. 32.
    Okumura H (2017) Avian egg and egg coat. Adv Exp Med Biol 1001:75–90PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    Santos TC, Murakami AE, Oliveira CA, Giraldelli N (2013) Sperm–egg interaction and fertility of Japanese breeder quails from 10 to 61 weeks. Poultry Sci 92(1):205–210CrossRefGoogle Scholar
  34. 34.
    Nishio S, Matsuda T (2017) Fertilization 1: sperm–egg interaction. Adv Exp Med Biol 1001:91–103PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Snook RR, Hosken DJ, Karr TL (2011) The biology and evolution of polyspermy: insights from cellular and functional studies of sperm and centrosomal behavior in the fertilized egg. Reproduction 142(6):779–792PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    Iwao Y (2012) Egg activation in physiological polyspermy. Reproduction 144(1):11–22PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Lee HC, Choi HJ, Park TS, Lee SI, Kim YM, Rengaraj D, Nagai H, Sheng G, Lim JM, Han JY (2013) Cleavage events and sperm dynamics in chick intrauterine embryos. PLoS One 8(11):e80631PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Mizushima S (2017) Fertilization 2: polyspermic fertilization. Adv Exp Med Biol 1001:105–123PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Hemmings N, Birkhead TR (2015) Polyspermy in birds: sperm numbers and embryo survival. Proc Biol Sci 282(1818):20151682PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Bellairs R, Osmond M (2014) The Hen’s egg and its formation. The atlas of chick Development, 3rd edn. Academic Press, Oxford, pp 1–6Google Scholar
  41. 41.
    Eyal-Giladi H, Kochav S (1976) From cleavage to primitive streak formation: a complementary normal table and a new look at the first stages of the development of the chick. I. General morphology. Dev Biol 49(2):321–337PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Kochav S, Ginsburg M, Eyal-Giladi H (1980) From cleavage to primitive streak formation: a complementary normal table and a new look at the first stages of the development of the chick. II. Microscopic anatomy and cell population dynamics. Dev Biol 79(2):296–308PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Hamburger V, Hamilton HL (1992) A series of normal stages in the development of the chick embryo. Dev Dyn 195(4):231–272PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Park HJ, Park TS, Kim TM, Kim JN, Shin SS, Lim JM, Han JY (2006) Establishment of an in vitro culture system for chicken preblastodermal cells. Mol Reprod Dev 73(4):452–461PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Fabian B, Eyal-Giladi H (1981) A SEM study of cell shedding during the formation of the area pellucida in the chick embryo. J Embryol Exp Morph 64:11–22PubMedPubMedCentralGoogle Scholar
  46. 46.
    Han JY, Lee HG, Hwang YS, Lee HC, Kim SK, Rengaraj D (2018) Expression of transcription factors during area pellucida formation in intrauterine chicken embryos. Int J Dev Biol 62(4–5):341–345PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Sellier N, Brillard JP, Dupuy V, Bakst MR (2006) Comparative staging of embryo development in chicken, turkey, duck, goose, guinea fowl, and Japanese quail assessed from five hours after fertilization through seventy-two hours of incubation. J Appl Poult Res 15(2):219–228CrossRefGoogle Scholar
  48. 48.
    Mak SS, Alev C, Nagai H, Wrabel A, Matsuoka Y, Honda A, Sheng G, Ladher RK (2015) Characterization of the finch embryo supports evolutionary conservation of the naive stage of development in amniotes. Elife 4:e07178PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Lee MT, Bonneau AR, Giraldez AJ (2014) Zygotic genome activation during the maternal-to-zygotic transition. Annu Rev Cell Dev Biol 30:581–613PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Jukam D, Shariati SAM, Skotheim JM (2017) Zygotic genome activation in vertebrates. Dev Cell 42(4):316–332PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Liu C, Ma Y, Shang Y, Huo R, Li W (2018) Post-translational regulation of the maternal-to-zygotic transition. Cell Mol Life Sci 75(10):1707–1722PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    Schulz KN, Harrison MM (2019) Mechanisms regulating zygotic genome activation. Nat Rev Genet 20(4):221–234PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Robertson S, Lin R (2015) The maternal-to-zygotic transition in C. elegans. Curr Top Dev Biol 113:1–42PubMedCrossRefPubMedCentralGoogle Scholar
  54. 54.
    Lee HC, Choi HJ, Lee HG, Lim JM, Ono T, Han JY (2016) DAZL expression explains origin and central formation of primordial germ cells in chickens. Stem Cells Dev 25(1):68–79PubMedCrossRefPubMedCentralGoogle Scholar
  55. 55.
    Elinson RP (2009) Nutritional endoderm: a way to breach the holoblastic–meroblastic barrier in tetrapods. J Exp Zool B Mol Dev Evol 312(6):526–532PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Hasley A, Chavez S, Danilchik M, Wuhr M, Pelegri F (2017) Vertebrate embryonic cleavage pattern determination. Adv Exp Med Biol 953:117–171PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Del Pino EM (2018) The extraordinary biology and development of marsupial frogs (Hemiphractidae) in comparison with fish, mammals, birds, amphibians and other animals. Mech Dev 154:2–11PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Siefert JC, Clowdus EA, Sansam CL (2015) Cell cycle control in the early embryonic development of aquatic animal species. Comp Biochem Physiol C Toxicol Pharmacol 178:8–15PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Bouniol C, Nguyen E, Debey P (1995) Endogenous transcription occurs at the 1-cell stage in the mouse embryo. Exp Cell Res 218(1):57–62PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Longo FJ, Kunkle M (1977) Synthesis of RNA by male pronuclei of fertilized sea-urchin eggs. J Exp Zool 201(3):431–437PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Poccia D, Wolff R, Kragh S, Williamson P (1985) RNA Synthesis in male pronuclei of the sea-urchin. Biochim Biophys Acta 824(4):349–356PubMedCrossRefPubMedCentralGoogle Scholar
  62. 62.
    Wu J, Huang B, Chen H, Yin Q, Liu Y, Xiang Y, Zhang B, Liu B, Wang Q, Xia W, Li W, Li Y, Ma J, Peng X, Zheng H, Ming J, Zhang W, Zhang J, Tian G, Xu F, Chang Z, Na J, Yang X, Xie W (2016) The landscape of accessible chromatin in mammalian preimplantation embryos. Nature 534(7609):652–657PubMedCrossRefPubMedCentralGoogle Scholar
  63. 63.
    Aoshima K, Inoue E, Sawa H, Okada Y (2015) Paternal H3K4 methylation is required for minor zygotic gene activation and early mouse embryonic development. EMBO Rep 16(7):803–812PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Zhang B, Zheng H, Huang B, Li W, Xiang Y, Peng X, Ming J, Wu X, Zhang Y, Xu Q, Liu W, Kou X, Zhao Y, He W, Li C, Chen B, Li Y, Wang Q, Ma J, Yin Q, Kee K, Meng A, Gao S, Xu F, Na J, Xie W (2016) Allelic reprogramming of the histone modification H3K4me3 in early mammalian development. Nature 537(7621):553–557PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Abe K, Yamamoto R, Franke V, Cao M, Suzuki Y, Suzuki MG, Vlahovicek K, Svoboda P, Schultz RM, Aoki F (2015) The first murine zygotic transcription is promiscuous and uncoupled from splicing and 3′processing. EMBO J 34(11):1523–1537PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Heyn P, Kircher M, Dahl A, Kelso J, Tomancak P, Kalinka AT, Neugebauer KM (2014) The earliest transcribed zygotic genes are short, newly evolved, and different across species. Cell Rep 6(2):285–292PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Fresard L, Leroux S, Servin B, Gourichon D, Dehais P, Cristobal MS, Marsaud N, Vignoles F, Bedhom B, Coville JL, Hormozdiari F, Beaumont C, Zerjal T, Vignal A, Morisson M, Lagarrigue S, Pitel F (2014) Transcriptome-wide investigation of genomic imprinting in chicken. Nucleic Acids Res 42(6):3768–3782PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Braude P, Bolton V, Moore S (1988) Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature 332(6163):459–461PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Zhang C, Basta T, Jensen ED, Klymkowsky MW (2003) The beta-catenin/VegT-regulated early zygotic gene Xnr5 is a direct target of SOX3 regulation. Development 130(23):5609–5624PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Okuda Y, Yoda H, Uchikawa M, Furutani-Seiki M, Takeda H, Kondoh H, Kamachi Y (2006) Comparative genomic and expression analysis of group B1 sox genes in zebrafish indicates their diversification during vertebrate evolution. Dev Dyn 235(3):811–825PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Liang HL, Nien CY, Liu HY, Metzstein MM, Kirov N, Rushlow C (2008) The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila. Nature 456(7220):400–403PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Leichsenring M, Maes J, Mossner R, Driever W, Onichtchouk D (2013) Pou5f1 transcription factor controls zygotic gene activation in vertebrates. Science 341(6149):1005–1009PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Lu F, Liu Y, Inoue A, Suzuki T, Zhao K, Zhang Y (2016) Establishing chromatin regulatory landscape during mouse preimplantation development. Cell 165(6):1375–1388PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    De Iaco A, Planet E, Coluccio A, Verp S, Duc J, Trono D (2017) DUX-family transcription factors regulate zygotic genome activation in placental mammals. Nat Genet 49(6):941–945PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Tang F, Kaneda M, O’Carroll D, Hajkova P, Barton SC, Sun YA, Lee C, Tarakhovsky A, Lao K, Surani MA (2007) Maternal microRNAs are essential for mouse zygotic development. Genes Dev 21(6):644–648PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Lund E, Liu M, Hartley RS, Sheets MD, Dahlberg JE (2009) Deadenylation of maternal mRNAs mediated by miR-427 in Xenopus laevis embryos. RNA 15(12):2351–2363PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Fu S, Nien CY, Liang HL, Rushlow C (2014) Co-activation of microRNAs by Zelda is essential for early Drosophila development. Development 141(10):2108–2118PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Han JY, Lee HG, Park YH, Hwang YS, Kim SK, Rengaraj D, Cho BW, Lim JM (2018) Acquisition of pluripotency in the chick embryo occurs during intrauterine embryonic development via a unique transcriptional network. J Anim Sci Biotechnol 9:31PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Hinkley CS, Martin JF, Leibham D, Perry M (1992) Sequential expression of multiple POU proteins during amphibian early development. Mol Cell Biol 12(2):638–649PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Yeo JC, Ng HH (2013) The transcriptional regulation of pluripotency. Cell Res 23(1):20–32PubMedCrossRefGoogle Scholar
  81. 81.
    Yang J, Aguero T, King ML (2015) The Xenopus maternal-to-zygotic transition from the perspective of the germline. Curr Top Dev Biol 113:271–303PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Skromne I, Stern CD (2001) Interactions between Wnt and Vg1 signalling pathways initiate primitive streak formation in the chick embryo. Development 128(15):2915–2927PubMedGoogle Scholar
  83. 83.
    Rengaraj D, Lee BR, Lee SI, Seo HW, Han JY (2011) Expression patterns and miRNA regulation of DNA methyltransferases in chicken primordial germ cells. PLoS ONE 6(5):e19524PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Li C, Guo S, Zhang M, Gao J, Guo Y (2015) DNA methylation and histone modification patterns during the late embryonic and early postnatal development of chickens. Poult Sci 94(4):706–721PubMedCrossRefGoogle Scholar
  85. 85.
    Li S, Zhu Y, Zhi L, Han X, Shen J, Liu Y, Yao J, Yang X (2016) DNA methylation variation trends during the embryonic development of chicken. PLoS ONE 11(7):e0159230PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Jung HG, Hwang YS, Park YH, Cho HY, Rengaraj D, Han JY (2018) Role of epigenetic regulation by the REST/CoREST/HDAC corepressor complex of moderate NANOG expression in chicken primordial germ cells. Stem Cells Dev 27(17):1215–1225PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Liu Z, Han S, Shen X, Wang Y, Cui C, He H, Chen Y, Zhao J, Li D, Zhu Q, Yin H (2019) The landscape of DNA methylation associated with the transcriptomic network in layers and broilers generates insight into embryonic muscle development in chicken. Int J Biol Sci 15(7):1404–1418PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Lee SI, Lee BR, Hwang YS, Lee HC, Rengaraj D, Song G, Park TS, Han JY (2011) MicroRNA-mediated posttranscriptional regulation is required for maintaining undifferentiated properties of blastoderm and primordial germ cells in chickens. Proc Natl Acad Sci USA 108(26):10426–10431PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Rengaraj D, Park TS, Lee SI, Lee BR, Han BK, Song G, Han JY (2013) Regulation of glucose phosphate isomerase by the 3′UTR-specific miRNAs miR-302b and miR-17-5p in chicken primordial germ cells. Biol Reprod 89(2):33PubMedCrossRefPubMedCentralGoogle Scholar
  90. 90.
    Rengaraj D, Lee SI, Park TS, Lee HJ, Kim YM, Sohn YA, Jung M, Noh SJ, Jung H, Han JY (2014) Small non-coding RNA profiling and the role of piRNA pathway genes in the protection of chicken primordial germ cells. BMC Genom 15:757CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Agricultural Biotechnology, and Research Institute of Agriculture and Life SciencesSeoul National UniversitySeoulSouth Korea
  2. 2.Department of Biomedical Sciences, School of Veterinary MedicineUniversity of PennsylvaniaPhiladelphiaUSA
  3. 3.Department of Cell and Developmental BiologyUniversity College LondonLondonUK

Personalised recommendations