Histone titration against the genome sets the DNA-to-cytoplasm threshold for the Xenopus midblastula transition

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 10, 2015, Pages E1086-E1095

  Amodeo, Amanda A ^a   Jukam, David ^a   Straight, Aaron F ^a   Skotheim, Jan M ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Cell size control; Early vertebrate development; Maternal zygotic transition; Systems biology; Transcription activation

Indexed keywords

DNA; HISTONE H3; HISTONE H4; HISTONE;

ANIMAL CELL; ARTICLE; CELL CYCLE CHECKPOINT; CELL FREE SYSTEM; CONTROLLED STUDY; CYTOPLASM; DNA BINDING; DNA SEQUENCE; DNA TO CYTOPLASM RATIO; EMBRYO; EMBRYO DEVELOPMENT; FRACTIONATION; GENETIC PARAMETERS; HISTONE UBIQUITINATION; MIDBLASTULA TRANSITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION; WESTERN BLOTTING; XENOPUS LAEVIS; ANIMAL; BLASTULA; EMBRYOLOGY; GENETIC TRANSCRIPTION; GENOME; METABOLISM; XENOPUS;

ANIMALIA; ANURA; VERTEBRATA; XENOPUS LAEVIS;

ANIMALS; BLASTULA; CYTOPLASM; DNA; GENOME; HISTONES; TRANSCRIPTION, GENETIC; XENOPUS;

EID: 84924322573     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1413990112     Document Type: Article

References (68)

1. Newport J, Kirschner M (1982) A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell 30(3):687-696.
2. Newport J, Kirschner M (1982) A major developmental transition in early Xenopus embryos: I. Characterization and timing of cellular changes at the midblastula stage. Cell 30(3):675-686.
3. Di Talia S, et al. (2013) Posttranslational control of Cdc25 degradation terminates Drosophila's early cell-cycle program. Curr Biol 23(2):127-132.
4. Farrell JA, O'Farrell PH (2013) Mechanism and regulation of Cdc25/Twine protein destruction in embryonic cell-cycle remodeling. Curr Biol 23(2):118-126.
5. Farrell JA, Shermoen AW, Yuan K, O'Farrell PH (2012) Embryonic onset of late replication requires Cdc25 down-regulation. Genes Dev 26(7):714-725.
6. Lu X, Li JM, Elemento O, Tavazoie S, Wieschaus EF (2009) Coupling of zygotic transcription to mitotic control at the Drosophila mid-blastula transition. Development 136(12):2101-2110.
7. Sung HW, Spangenberg S, Vogt N, Großhans J (2013) Number of nuclear divisions in the Drosophila blastoderm controlled by onset of zygotic transcription. Curr Biol 23(2):133-138.
8. Clute P, Masui Y (1995) Regulation of the appearance of division asynchrony and microtubule-dependent chromosome cycles in Xenopus laevis embryos. Dev Biol 171(2):273-285.
9. Howe JA, Newport JW (1996) A developmental timer regulates degradation of cyclin E1 at the midblastula transition during Xenopus embryogenesis. Proc Natl Acad Sci USA 93(5):2060-2064.
10. Almouzni G, Wolffe AP (1995) Constraints on transcriptional activator function contribute to transcriptional quiescence during early Xenopus embryogenesis. EMBO J 14(8):1752-1765.
11. Prioleau MN, Huet J, Sentenac A, Méchali M (1994) Competition between chromatin and transcription complex assembly regulates gene expression during early development. Cell 77(3):439-449.
12. Almouzni G, Méchali M, Wolffe AP (1990) Competition between transcription complex assembly and chromatin assembly on replicating DNA. EMBO J 9(2):573-582.
13. Almouzni G, Méchali M, Wolffe AP (1991) Transcription complex disruption caused by a transition in chromatin structure. Mol Cell Biol 11(2):655-665.
14. Dunican DS, Ruzov A, Hackett JA, Meehan RR (2008) xDnmt1 regulates transcriptional silencing in pre-MBT Xenopus embryos independently of its catalytic function. Development 135(7):1295-1302.
15. Stancheva I, El-Maarri O, Walter J, Niveleau A, Meehan RR (2002) DNA methylation at promoter regions regulates the timing of gene activation in Xenopus laevis embryos. Dev Biol 243(1):155-165.
16. Stancheva I, Meehan RR (2000) Transient depletion of xDnmt1 leads to premature gene activation in Xenopus embryos. Genes Dev 14(3):313-327.
17. Murphy CM, Michael WM (2013) Control of DNA replication by the nucleus/cytoplasm ratio in Xenopus. J Biol Chem 288(41):29382-29393.
18. Collart C, Allen GE, Bradshaw CR, Smith JC, Zegerman P (2013) Titration of four replication factors is essential for the Xenopus laevis midblastula transition. Science 341(6148):893-896.
19. Vastag L, et al. (2011) Remodeling of the metabolome during early frog development. PLoS ONE 6(2):e16881.
20. De Renzis S, Elemento O, Tavazoie S, Wieschaus EF (2007) Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo. PLoS Biol 5(5):e117.
21. Harrison MM, Botchan MR, Cline TW (2010) Grainyhead and Zelda compete for binding to the promoters of the earliest-expressed Drosophila genes. Dev Biol 345(2):248-255.
22. Liang HL, et al. (2008) The zinc-finger protein Zelda is a key activator of the early zygotic genome in Drosophila. Nature 456(7220):400-403.
23. Kanodia JS, et al. (2012) Pattern formation by graded and uniform signals in the early Drosophila embryo. Biophys J 102(3):427-433.
24. Pearson JC, Watson JD, Crews ST (2012) Drosophila melanogaster Zelda and Single-minded collaborate to regulate an evolutionarily dynamic CNS midline cell enhancer. Dev Biol 366(2):420-432.
25. Lee MT, et al. (2013) Nanog, Pou5f1 and SoxB1 activate zygotic gene expression during the maternal-to-zygotic transition. Nature 503(7476):360-364.
26. Leichsenring M, Maes J, Mössner R, Driever W, Onichtchouk D (2013) Pou5f1 transcription factor controls zygotic gene activation in vertebrates. Science 341(6149):1005-1009.
27. Philpott A, Leno GH, Laskey RA (1991) Sperm decondensation in Xenopus egg cytoplasm is mediated by nucleoplasmin. Cell 65(4):569-578.
28. Collart C, et al. (2014) High-resolution analysis of gene activity during the Xenopus mid-blastula transition. Development 141(9):1927-1939.
29. Skirkanich J, Luxardi G, Yang J, Kodjabachian L, Klein PS (2011) An essential role for transcription before the MBT in Xenopus laevis. Dev Biol 357(2):478-491.
30. Tan MH, et al. (2013) RNA sequencing reveals a diverse and dynamic repertoire of the Xenopus tropicalis transcriptome over development. Genome Res 23(1):201-216.
31. Yang J, Tan C, Darken RS, Wilson PA, Klein PS (2002) Beta-catenin/Tcf-regulated transcription prior to the midblastula transition. Development 129(24):5743-5752.
32. Wolffe AP (1989) Transcriptional activation of Xenopus class III genes in chromatin isolated from sperm and somatic nuclei. Nucleic Acids Res 17(2):767-780.
33. Sun L, et al. (2014) Quantitative proteomics of Xenopus laevis embryos: Expression kinetics of nearly 4000 proteins during early development. Sci Rep 4:4365.
34. Adamson ED, Woodland HR (1974) Histone synthesis in early amphibian development: Histone and DNA syntheses are not co-ordinated. J Mol Biol 88(2):263-285.
35. Wang WL, et al. (2014) Phosphorylation and arginine methylation mark histone H2A prior to deposition during Xenopus laevis development. Epigenetics Chromatin 7:22.
36. Burton DR, et al. (1978) The interaction of core histones with DNA: Equilibrium binding studies. Nucleic Acids Res 5(10):3643-3663.
37. Oohara I, Wada A (1987) Spectroscopic studies on histone-DNA interactions. II. Three transitions in nucleosomes resolved by salt-titration. J Mol Biol 196(2):399-411.
38. Kimura H, Cook PR (2001) Kinetics of core histones in living human cells: Little exchange of H3 and H4 and some rapid exchange of H2B. J Cell Biol 153(7):1341-1353.
39. Zhang Y (2003) Transcriptional regulation by histone ubiquitination and deubiquitination. Genes Dev 17(22):2733-2740.
40. Szenker E, Lacoste N, Almouzni G (2012) A developmental requirement for HIRA-dependent H3.3 deposition revealed at gastrulation in Xenopus. Cell Reports 1(6):730-740.
41. Adamson ED, Woodland HR (1977) Changes in the rate of histone synthesis during oocyte maturation and very early development of Xenopus laevis. Dev Biol 57(1):136-149.
42. Johnson KE (1976) Circus movements and blebbing locomotion in dissociated embryonic cells of an amphibian, Xenopus laevis. J Cell Sci 22(3):575-583.
43. Minoura I, Nakamura H, Tashiro K, Shiokawa K (1995) Stimulation of circus movement by activin, bFGF and TGF-beta 2 in isolated animal cap cells of Xenopus laevis. Mech Dev 49(1-2):65-69.
44. Kimelman D, Kirschner M, Scherson T (1987) The events of the midblastula transition in Xenopus are regulated by changes in the cell cycle. Cell 48(3):399-407.
45. Dasso M, Newport JW (1990) Completion of DNA replication is monitored by a feedback system that controls the initiation of mitosis in vitro: Studies in Xenopus. Cell 61(5):811-823.
46. Zamir E, Kam Z, Yarden A (1997) Transcription-dependent induction of G1 phase during the zebra fish midblastula transition. Mol Cell Biol 17(2):529-536.
47. Akkers RC, et al. (2009) A hierarchy of H3K4me3 and H3K27me3 acquisition in spatial gene regulation in Xenopus embryos. Dev Cell 17(3):425-434.
48. Vastenhouw NL, et al. (2010) Chromatin signature of embryonic pluripotency is established during genome activation. Nature 464(7290):922-926.
49. Pérez-Montero S, Carbonell A, Morán T, Vaquero A, Azorín F (2013) The embryonic linker histone H1 variant of Drosophila, dBigH1, regulates zygotic genome activation. Dev Cell 26(6):578-590.
50. Yue HM, et al. (2013) Oocyte-specific H2A variant H2af1o is required for cell synchrony before midblastula transition in early zebrafish embryos. Biol Reprod 89(4):82.
51. Donachie WD (1968) Relationship between cell size and time of initiation of DNA replication. Nature 219(5158):1077-1079.
52. Hill NS, Kadoya R, Chattoraj DK, Levin PA (2012) Cell size and the initiation of DNA replication in bacteria. PLoS Genet 8(3):e1002549.
53. Turner JJ, Ewald JC, Skotheim JM (2012) Cell size control in yeast. Curr Biol 22(9):R350-R359.
54. Wang H, Carey LB, Cai Y, Wijnen H, Futcher B (2009) Recruitment of Cln3 cyclin to promoters controls cell cycle entry via histone deacetylase and other targets. PLoS Biol 7(9):e1000189.
55. Masui Y, Wang P (1998) Cell cycle transition in early embryonic development of Xenopus laevis. Biol Cell 90(8):537-548.
56. Gregory TR (2001) Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biol Rev Camb Philos Soc 76(1):65-101.
57. Newman JR, et al. (2006) Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441(7095):840-846.
58. Oliva A, et al. (2005) The cell cycle-regulated genes of Schizosaccharomyces pombe. PLoS Biol 3(7):e225.
59. Spellman PT, et al. (1998) Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell 9(12):3273-3297.
60. Whitfield ML, et al. (2002) Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol Biol Cell 13(6):1977-2000.
61. Desai A, Murray A, Mitchison TJ, Walczak CE (1999) The use of Xenopus egg extracts to study mitotic spindle assembly and function in vitro. Methods Cell Biol 61:385-412.
62. Desai A, Deacon HW, Walczak CE, Mitchison TJ (1997) A method that allows the assembly of kinetochore components onto chromosomes condensed in clarified Xenopus egg extracts. Proc Natl Acad Sci USA 94(23):12378-12383.
63. Hannak E, Heald R (2006) Investigating mitotic spindle assembly and function in vitro using Xenopus laevis egg extracts. Nat Protoc 1(5):2305-2314.
64. Guse A, Fuller CJ, Straight AF (2012) A cell-free system for functional centromere and kinetochore assembly. Nat Protoc 7(10):1847-1869.
65. Luger K, Rechsteiner TJ, Flaus AJ, Waye MM, Richmond TJ (1997) Characterization of nucleosome core particles containing histone proteins made in bacteria. J Mol Biol 272(3):301-311.
66. Satoh N, Kageyama T, Sirakami K (1976) Motility of dissociated embryonic cells in xenopus laevis: Its significance to morphogenetic movements. Dev Growth Differ 18(1):55-67.
67. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2(-Delta C(T)) Method. Methods 25(4):402-408.
68. Krol A, Carbon P, Ebel JP, Appel B (1987) Xenopus tropicalis U6 snRNA genes transcribed by Pol III contain the upstream promoter elements used by Pol II dependent U snRNA genes. Nucleic Acids Res 15(6):2463-2478.