Growing an embryo from a single cell: A hurdle in animal life

Cold Spring Harbor Perspectives in Biology

Volumn 7, Issue 11, 2015, Pages

  O’Farrell, Patrick H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; CELL COMMUNICATION; CELL ENLARGEMENT; CELL PROLIFERATION; EMBRYO DEVELOPMENT; EMBRYOLOGY; EVOLUTION; MAMMAL; MAMMALIAN EMBRYO; MORPHOGENESIS; NONMAMMALIAN EMBRYO; OOCYTE DEVELOPMENT;

ANIMALS; BIOLOGICAL EVOLUTION; BODY PATTERNING; CELL COMMUNICATION; CELL ENLARGEMENT; CELL PROLIFERATION; EMBRYO, MAMMALIAN; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; MAMMALS; OOGENESIS;

EID: 84946434637     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a019042     Document Type: Article

References (97)

1. Bedford L. 1966. The electron microscopy and cytochemistry of oogenesis and the cytochemistry of embryonic development of the prosobranch gastropod Bembicium nanum L. J Embryol Exp Morphol 15: 15–37
2. Blobel G, Potter VR. 1967. Studies on free and membranebound ribosomes in rat liver. I: Distribution as related to total cellular RNA. J Mol Biol 26: 279–292
3. Bratic I, Hench J, Henriksson J, Antebi A, Bürglin TR, Trifunovic A. 2009. MitochondrialDNA level, but not active replicase, is essential for Caenorhabditis elegans development. Nucleic Acids Res 37: 1817–1828
4. Brown DD, Dawid IB. 1968. Specific gene amplification in oocytes. Oocyte nuclei contain extrachromosomal replicas of the genes for ribosomal RNA. Science 160: 272–280
5. Butcher AR, Brealey JK, Grove DI, Dymock RB. 2002. Brachylaima cribbi (Digenea: Brachylaimidae): Scanning electron microscopical observations of the life-cycle stages. J Helminthol 76: 207–215
6. Cañon S, Fernandez-Tresguerres B, Manzanares M. 2011. Pluripotency and lineages in the mammalian blastocyst: An evolutionary view. Cell Cycle 10: 1731–1738
7. Chase JW, Dawid IB. 1972. Biogenesis of mitochondria during Xenopus laevis development. Dev Biol 27: 504–518
8. Coronado D, Godet M, Bourillot PY, Tapponnier Y, Bernat A, Petit M, Afanassieff M, Markossian S, Malashicheva A, Iacone R, et al. 2013. A short G1 phase is an intrinsic determinant of naïve embryonic stem cell pluripotency. Stem Cell Res 10: 118–131
9. Cox RT, Spradling AC. 2003. A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development 130: 1579–1590
10. Del Pino EM, Humphries AA. 1978.Multiple nuclei during early oogenesis in Flectonotus pygmaeus and other marsupial frogs. Biol Bull 154: 198–212
11. Dobzhansky T. 1973.Nothing in biology makes sense except in the light of evolution. J Hered 68: 3–10
12. Domazet-Lošo T, Tautz D. 2010. A phylogenetically based transcriptome age index mirrors ontogenetic divergence patterns. Nature 468: 815–818
13. Eckelbarger KJ, Larson R. 1992. Ultrastructure of the ovary and oogenesis in the jellyfish Linuche unguiculata and Stomolophus meleagris, with a review of ovarian structure in the Scyphozoa. Marine Biol 114: 633–643
14. Eckelbarger KJ, Young CM. 1997. Ultrastructure of the ovary and oogenesis in the methane-seep mollusc Bathynerita naticoidea (Gastropoda: Neritidae) from the Louisiana slope. Invertebr Biol 116: 299–312
15. Edgar BA, O’Farrell PH. 1990. The three postblastoderm cell cycles of Drosophila embryogenesis are regulated in G2 by string. Cell 62: 469–480
16. Edgar BA, Schubiger G. 1986. Parameters controlling transcriptional activation during early Drosophila development. Cell 44: 871–877
17. Edgar BA, Kiehle CP, Schubiger G. 1986. Cell cycle control by the nucleo-cytoplasmic ratio in early Drosophila development. Cell 44: 365–372
18. Edgar BA, Sprenger F, Duronio RJ, Leopold P, O’Farrell PH. 1994. Distinct molecular mechanism regulate cell cycle timing at successive stages of Drosophila embryogenesis. Genes Dev 8: 440–452
19. Evans MJ, Kaufman MH. 1981. Establishment in culture of pluripotential cells from mouse embryos. Nature 292: 154–156
20. Evans T, Rosenthal ET, Youngblom J, Distel D, Hunt T. 1983. Cyclin: A protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell 33: 389–396
21. Farrell JA, O’Farrell PH. 2013.Mechanism and regulation of Cdc25/twine protein destruction in embryonic cell-cycle remodeling. Curr Biol 23: 118–126
22. Farrell JA, O’Farrell PH. 2014. Fromegg to gastrula:How the cell cycle is remodeled during the Drosophila mid-blastula transition. Annu Rev Genet 48: 269–294
23. Follette PJ, O’Farrell PH. 1997. Connecting cell behavior to patterning: Lessons from the cell cycle. Cell 88: 309–314
24. Follette PJ, Duronio RJ, O’Farrell PH. 1998. Fluctuations in cyclin E levels are required for multiple rounds of endocycle S phase in Drosophila. Curr Biol 8: 235–238
25. Fujii-Yamamoto H, Kim JM, Arai KI, Masai H. 2005. Cell cycle and developmental regulations of replication factors in mouse embryonic stem cells. J Biol Chem 280: 12976–12987
26. Gall JG. 1968. Differential synthesis of the genes for ribosomal RNA during amphibian oögenesis. Proc Natl Acad Sci 60: 553–560
27. Gall JG. 2012. Are lampbrush chromosomes unique to meiotic cells? Chromosome Res 20: 905–909
28. Gall JG, Wu Z, Murphy C, Gao H. 2004. Structure in the amphibian germinal vesicle. Exp Cell Res 296: 28–34
29. Ganot P, Bouquet JM, Kallesøe T, Thompson EM. 2007. The Oikopleura coenocyst, a unique chordate germ cell permitting rapid, extensive modulation of oocyte production. Dev Biol 302: 591–600
30. Ganot P, Moosmann-Schulmeister A, Thompson EM. 2008. Oocyte selection is concurrent with meiosis resumption in the coenocystic oogenesis of Oikopleura. Dev Biol 324: 266–276
31. Gardner EJ, Nizami ZF, Talbot CC, Gall JG. 2012. Stable intronic sequence RNA (sisRNA), a new class of noncoding RNA from the oocyte nucleus of Xenopus tropicalis. Genes Dev 26: 2550–2559
32. Gersh ES. 1968. Mutants at the bobbed locus in Drosophila melanogaster: Relation to ribosomal RNA synthesis? Science 162: 1139
33. Graham A, Richardson J. 2012. Developmental and evolutionary origins of the pharyngeal apparatus. Evodevo 3: 24
34. Grbic´ M. 2000. “Alien” wasps and evolution of development. Bioessays 22: 920–932
35. Grbić M, Nagy LM, Strand MR. 1998. Development of polyembryonic insects: A major departure from typical insect embryogenesis. Dev Genes Evol 208: 69–81
36. Gruzova MN, Batalova FM. 1979. Nuclear structures in the telotrophic ovarioles of nocturnal ground beetles (Tenebrionidae, Polyphaga). II: The oocyte nucleus of Blaps lethifera and Gnaptor spinimanus. Light optical data. Ontogenez 10: 323–331
37. Gurdon JB, Elsdale TR, Fischberg M. 1958. Sexually mature individuals of Xenopus laevis from the transplantation of single somatic nuclei. Nature 182: 64–65
38. Harvey EB. 1935. Cleavage without nuclei. Science 82: 277
39. Hayashi S, Yamaguchi M. 1999.Kinase-independent activity of Cdc2/cyclin A prevents the S phase in the Drosophila cell cycle. Genes Cells 4: 111–122
40. Howe JA, Howell M, Hunt T, Newport JW. 1995. Identification of a developmental timer regulating the stability of embryonic cyclin A and a new somatic A-type cyclin at gastrulation. Genes Dev 9: 1164–1176
41. Jourdane J, Theron A. 1980. Schistosoma mansoni: Cloning by microsurgical transplantation of sporocysts. Exp Parasitol 50: 349–357
42. Kalinka AT, Varga KM, Gerrard DT, Preibisch S, Corcoran DL, Jarrells J, Ohler U, Bergman CM, Tomancak P. 2010. Gene expression divergence recapitulates the developmental hourglass model. Nature 468: 811–814
43. Kloc M, Jedrzejowska I, Tworzydlo W, Bilinski SM. 2014. Balbiani body, nuage and sponge bodies—The germ plasm pathway players. Arthropod Struct Dev 43: 341–348
44. Landström U, Løvtrup-Rein H, Løvtrup S. 1975. Control of cell division and cell differentiation by deoxynucleotides in the early embryo of Xenopus laevis. Cell Differ 4: 313–325
45. Laskey RA, Honda BM, Mills AD, Finch JT. 1978. Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA. Nature 275: 416–420
46. Le Bin GC, Muñoz-Descalzo S, Kurowski A, Leitch H, Lou X, Mansfield W, Etienne-Dumeau C, Grabole N, Mulas C, Niwa H, et al. 2014. Oct4 is required for lineage priming in the developing inner cell mass of the mouse blastocyst. Development 141: 1001–1010
47. Lee MT, Bonneau AR, Takacs CM, Bazzini AA, DiVito KR, Fleming ES, Giraldez AJ. 2013.Nanog, Pou5f1 and SoxB1 activate zygotic gene expression during the maternal-tozygotic transition. Nature 503: 360–364
48. Leichsenring M, Maes J, Mössner R, Driever W, Onichtchouk D. 2013. Pou5f1 transcription factor controls zygotic gene activation in vertebrates. Science 341: 1005–1009
49. Li XY, Harrison MM, Villalta JE, Kaplan T, Eisen MB. 2014. Establishment of regions of genomic activity during the Drosophila maternal to zygotic transition. eLife doi: 10.7554/eLife.03737
50. Lin CJ, Koh FM, Wong P, Conti M, Ramalho-Santos M. 2014. Hira-mediated H3.3 incorporation is required for DNA replication and ribosomalRNAtranscription in the mouse zygote. Dev Cell 30: 268–279
51. Loppin B, Bonnefoy E, Anselme C, Laurençon A, Karr TL, Couble P. 2005. The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 437: 1386–1390
52. Mac Auley A, Werb Z, Mirkes PE. 1993. Characterization of the unusually rapid cell cycles during rat gastrulation. Development 117: 873–883
53. Macgregor HC, Del Pino EM. 1982. Ribosomal gene ampli- fication in multinucleate oocytes of the egg brooding hylid frog Flectonotus pygmaeus. Chromosoma 85: 475–488
54. Marandel L, Labbe C, Bobe J, Le Bail PY. 2012. nanog 50- upstream sequence, DNA methylation, and expression in gametes and early embryo reveal striking differences between teleosts and mammals. Gene 492: 130–137
55. Marlow FL, Mullins MC. 2008. Bucky ball functions in Balbiani body assembly and animal–vegetal polarity in the oocyte and follicle cell layer in zebrafish. Dev Biol 321: 40–50
56. Martin GR. 1981. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci 78: 7634–7638
57. Newport J, Dasso M. 1989. On the coupling between DNA replication and mitosis. J Cell Sci 12: 149–160
58. Newport J, Kirschner M. 1982a. A major developmental transition in early Xenopus embryos. I: Characterization and timing of cellular changes at the midblastula stage. Cell 30: 675–686
59. Newport J, Kirschner M. 1982b. A major developmental transition in early Xenopus embryos. II: Control of the onset of transcription. Cell 30: 687–696
60. O’Farrell PH. 2004. How metazoans reach their full size: The natural history of bigness. In Cell growth: Control of cell size (ed. Hall M, et al.). Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
61. O’Farrell PH. 2011. Quiescence: Early evolutionary origins and universality do not imply uniformity. Phil Trans R Soc B 366: 3498–3507
62. O’Farrell PH, Stumpff J, Su TT. 2004. Embryonic cleavage cycles: How is a mouse like a fly? Curr Biol 14: R35–R45
63. Orsi GA, Algazeery A, Meyer RE, Capri M, Sapey-Triomphe LM, Horard B, Gruffat H, Couble P, Ahmed O, Loppin B. 2013. Drosophila Yemanuclein and HIRA cooperate for de novo assembly of H3.3-containing nucleosomes in the male pronucleus. PLoS Genet 9: e1003285
64. Patel NH, Martin-Blanco E, Coleman KG, Poole SJ, Ellis MC, Kornberg TB, Goodman CS. 1989. Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58: 955–968
65. Pepling ME, de Cuevas M, Spradling AC. 1999. Germline cysts: A conserved phase of germ cell development? Trends Cell Biol 9: 257–262
66. Philpott A, Leno GH, Laskey RA. 1991. Sperm decondensation in Xenopus egg cytoplasm is mediated by nucleoplasmin. Cell 65: 569–578
67. Philpott A, Krude T, Laskey RA. 2000. Nuclear chaperones. Semin Cell Dev Biol 11: 7–14
68. Podvyaznaya IM, Galaktionov KV. 2014. Trematode reproduction in the molluscan host: An ultrastructural study of the germinal mass in the rediae of Himasthla elongata (Mehlis, 1831) (Digenea: Echinostomatidae). Parasitol Res 113: 1215–1224
69. Pritchard DK, Schubiger G. 1996. Activation of transcription in Drosophila embryos is a gradual process mediated by the nucleocytoplasmic ratio. Genes Dev 10: 1131–1142
70. Prud’homme B, Gompel N. 2010. Evolutionary biology: Genomic hourglass. Nature 468: 768–769
71. Prud’homme B, de Rosa R, Arendt D, Julien JF, Pajaziti R, Dorresteijn AWC, Adoutte A, Wittbrodt J, Balavoine G. 2003. Arthropod-like expression patterns of engrailed and wingless in the annelid Platynereis dumerilii suggest a role in segment formation. Curr Biol 13: 1876–1881
72. Raff RA. 1996. The shape of life. University of Chicago Press, Chicago
73. Rahn H, Paganelli CV, Ar A. 1974. The avian egg: Air-cell gas tension, metabolism and incubation time. Respir Physiol 22: 297–309
74. Sánchez-Sánchez AV, Camp E, Mullor JL. 2011. Fishing pluripotency mechanisms in vivo. Int J Biol Sci 7: 410–417
75. Savatier P, Lapillonne H, van Grunsven LA, Rudkin BB, Samarut J. 1996.Withdrawal of differentiation inhibitory activity/leukemia inhibitory factor up-regulates D-type cyclins and cyclin-dependent kinase inhibitors in mouse embryonic stem cells. Oncogene 12: 309–322
76. Shen MM. 2007. Nodal signaling: Developmental roles and regulation. Development 134: 1023–1034
77. Shermoen AW, O’Farrell PH. 1991. Progression of the cell cycle through mitosis leads to abortion of nascent transcripts. Cell 67: 303–310
78. Shermoen AW, McCleland ML, O’Farrell PH. 2010. Developmental control of late replication and S phase length. Curr Biol 20: 2067–2077
79. Skála V, Bulantová J, Walker AJ, Horák P. 2014. Insights into the development of Notocotylus attenuatus (Digenea:Notocotylidae) in Lymnaea stagnalis: From mother sporocyst to cercariae. Parasitol Int 63: 94–99
80. Smiley S. 1990. A reviewof echinoderm oogenesis. J Electron Microsc Tech 16: 93–114
81. Snow MHL. 1977. Gastrulation in the mouse: Growth and regionalization of the epiblast. J Embryol Exp Morphol 42: 293–303
82. Snow MH. 1981. Growth and its control in early mammalian development. Br Med Bull 37: 221–226
83. Sun LT, Yamaguchi S, Hirano K, Ichisaka T, Kuroda T, Tada T. 2014. Nanog co-regulated by Nodal/Smad2 and Oct4 is required for pluripotency in developing mouse epiblast. Dev Biol 392: 182–192
84. Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663–676
85. Tsang WY, Lemire BD. 2002. Mitochondrial genome content is regulated during nematode development. Biochem Biophys Res Commun 291: 8–16
86. Tworzydlo W, Kloc M, Bilinski SM. 2009. The Balbiani body in the female germline cells of an earwig, Opisthocosmia silvestris. Zool Sci 26: 754–757
87. van der Laan S, Tsanov N, Crozet C, Maiorano D. 2013. High Dub3 expression in mouse ESCs couples the G1/S checkpoint to pluripotency. Mol Cell 52: 366–379
88. Webb AC, Smith LD. 1977. Accumulation of mitochondrial DNA during oogenesis in Xenopus laevis. Dev Biol 56: 219–225
89. White J, Stead E, Faast R, Conn S, Cartwright P, Dalton S. 2005. Developmental activation of the Rb-E2F pathway and establishment of cell cycle-regulated cyclin-depen- dent kinase activity during embryonic stem cell differentiation. Mol Biol Cell 16: 2018–2027
90. Wiegmann BM, Trautwein MD, Winkler IS, Barr NB, Kim JW, Lambkin C, Bertone MA, Cassel BK, Bayless KM, Heimberg AM, et al. 2011. Episodic radiations in the fly tree of life. Proc Natl Acad Sci 108: 5690–5695
91. Wieschaus E. 1996. Embryonic transcription and the control of developmental pathways. Genetics 142: 5–10
92. Wolf SF, Schlessinger D. 1977. Nuclear metabolism of ribosomal RNA in growing, methionine-limited, and ethionine-treated HeLa cells. Biochemistry 16: 2783–2791
93. Woodland H. 1982. The translational control phase of early development. Biosci Rep 2: 471–491
94. Woodland HR, Pestell RQ. 1972. Determination of the nucleoside triphosphate contents of eggs and oocytes of Xenopus laevis. Biochem J 127: 597–605
95. Yang VS, Carter SA, Hyland SJ, Tachibana-Konwalski K, Laskey RA, Gonzalez MA. 2011. Geminin escapes degradation in G1 of mouse pluripotent cells and mediates the expression of Oct4, Sox2, and Nanog. Curr Biol 21: 692–699
96. Yuan K, Shermoen AW, O’Farrell PH. 2014. Illuminating DNA replication during Drosophila development using TALE-lights. Curr Biol 24: R144–R145
97. Zhao ZK, Li W, Wang MY, Zhou L, Wang JL, Wang YF. 2011. The role of HIRA andmaternal histones in sperm nucleus decondensation in the gibel carp and color crucian carp. Mol Reprod Dev 78: 139–147.