Geminin is required for zygotic gene expression at the xenopus mid-blastula transition

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Kerns, Sarah L ^a   Schultz, Kathryn M ^a   Barry, Kelly A ^a   Thorne, Tina M ^a   McGarry, Thomas J ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 1; GEMININ; HYDROXYUREA; REPLICATION LICENSING FACTOR CDT1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLASTOMERE; BLASTULA; CELL CYCLE ARREST; CELL CYCLE CHECKPOINT; CELL CYCLE REGULATION; CONTROLLED STUDY; DNA CLEAVAGE; DOUBLE STRANDED DNA BREAK; EMBRYO; FEMALE; GENE DELETION; GENE EXPRESSION; GENETIC TRANSCRIPTION; MALE; MID BLASTULA TRANSITION; NONHUMAN; PROTEIN DEPLETION; XENOPUS; ZYGOTE;

ANIMALS; BLASTULA; CELL CYCLE CHECKPOINTS; CELL CYCLE PROTEINS; DNA DAMAGE; DNA-BINDING PROTEINS; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HYDROXYUREA; MALE; MUTATION; PROTEIN BINDING; T-BOX DOMAIN PROTEINS; TRANSCRIPTION, GENETIC; XENOPUS; XENOPUS PROTEINS; ZYGOTE;

EID: 84861471202     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038009     Document Type: Article

References (69)

1. Tadros W, Lipshitz HD, (2009) The maternal-to-zygotic transition: a play in two acts. Development 136: 3033-3042.
2. O'Farrell PH, Stumpff J, Su TT, (2004) Embryonic cleavage cycles: how is a mouse like a fly? Curr Biol 14: R35-45.
3. Foe VE, Odell GM, Edgar BA, (1993) Mitosis and Morphogenesis in the Drosophila Embryo: Point and Counterpoint. In: Bate M, Martinez-Arias A, editors. The Development of Drosophila melanogaster Cold Spring Harbor, NY Cold Spring Harbor Press.
4. 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: 675-686.
5. Edgar BA, Kiehle CP, Schubiger G, (1986) Cell cycle control by the nucleo-cytoplasmic ratio in early Drosophila development. Cell 44: 365-372.
6. Kane DA, Kimmel CB, (1993) The zebrafish midblastula transition. Development 119: 447-456.
7. Newport J, Kirschner M, (1982) A major developmental transition in early Xenopus embryos: II. Control of the onset of transcription. Cell 30: 687-696.
8. 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: 2101-2110.
9. Benoit B, He CH, Zhang F, Votruba SM, Tadros W, et al. (2009) An essential role for the RNA-binding protein Smaug during the Drosophila maternal-to-zygotic transition. Development 136: 923-932.
10. Tadros W, Goldman AL, Babak T, Menzies F, Vardy L, et al. (2007) SMAUG is a major regulator of maternal mRNA destabilization in Drosophila and its translation is activated by the PAN GU kinase. Dev Cell 12: 143-155.
11. Semotok JL, Cooperstock RL, Pinder BD, Vari HK, Lipshitz HD, et al. (2005) Smaug recruits the CCR4/POP2/NOT deadenylase complex to trigger maternal transcript localization in the early Drosophila embryo. Curr Biol 15: 284-294.
12. 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.
13. Edgar BA, Schubiger G, (1986) Parameters controlling transcriptional activation during early Drosophila development. Cell 44: 871-877.
14. 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: 399-407.
15. Shermoen AW, O'Farrell PH, (1991) Progression of the cell cycle through mitosis leads to abortion of nascent transcripts. Cell 67: 303-310.
16. Sibon OC, Laurencon A, Hawley R, Theurkauf WE, (1999) The Drosophila ATM homologue Mei-41 has an essential checkpoint function at the midblastula transition. Curr Biol 9: 302-312.
17. Sibon OC, Stevenson VA, Theurkauf WE, (1997) DNA-replication checkpoint control at the Drosophila midblastula transition. Nature 388: 93-97.
18. Fogarty P, Campbell SD, Abu-Shumays R, Phalle BS, Yu KR, et al. (1997) The Drosophila grapes gene is related to checkpoint gene chk1/rad27 and is required for late syncytial division fidelity. Curr Biol 7: 418-426.
19. Takada S, Kwak S, Koppetsch BS, Theurkauf WE, (2007) grp (chk1) replication-checkpoint mutations and DNA damage trigger a Chk2-dependent block at the Drosophila midblastula transition. Development 134: 1737-1744.
20. Luo L, Kessel M, (2004) Geminin coordinates cell cycle and developmental control. Cell Cycle 3: 711-714.
21. Seo S, Kroll KL, (2006) Geminin's double life: chromatin connections that regulate transcription at the transition from proliferation to differentiation. Cell Cycle 5: 374-379.
22. McGarry TJ, Kirschner MW, (1998) Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 93: 1043-1053.
23. Tada S, Li A, Maiorano D, Mechali M, Blow JJ, (2001) Repression of origin assembly in metaphase depends on inhibition of RLF-B/Cdt1 by geminin. Nature Cell Biology 3: 107-113.
24. Wohlschlegel JA, Dwyer BT, Dhar SK, Cvetic C, Walter JC, et al. (2000) Inhibition of eukaryotic DNA replication by geminin binding to cdt1. Science 290: 2309-2312.
25. Del Bene F, Tessmar-Raible K, Wittbrodt J, (2004) Direct interaction of geminin and Six3 in eye development. Nature 427: 745-749.
26. Luo L, Yang X, Takihara Y, Knoetgen H, Kessel M, (2004) The cell-cycle regulator geminin inhibits Hox function through direct and polycomb-mediated interactions. Nature 427: 749-753.
27. Seo S, Herr A, Lim JW, Richardson GA, Richardson H, et al. (2005) Geminin regulates neuronal differentiation by antagonizing Brg1 activity. Genes Dev 19: 1723-1734.
28. McGarry TJ, (2002) Geminin deficiency causes a Chk1-dependent G2 arrest in Xenopus. Mol Biol Cell 13: 3662-3671.
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.
30. Wilson R, Mohun T, (1995) XIdx, a dominant negative regulator of bHLH function in early Xenopus embryos. Mech Dev 49: 211-222.
31. Cho KW, Blumberg B, Steinbeisser H, De Robertis EM, (1991) Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid. Cell 67: 1111-1120.
32. Wilkinson DG, Bhatt S, Herrmann BG, (1990) Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 343: 657-659.
33. De Robertis EM, Kuroda H, (2004) Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu Rev Cell Dev Biol 20: 285-308.
34. Kroll KL, Salic AN, Evans LM, Kirschner MW, (1998) Geminin, a neuralizing molecule that demarcates the future neural plate at the onset of gastrulation. Development 125: 3247-3258.
35. Lim JW, Hummert P, Mills JC, Kroll KL, (2011) Geminin cooperates with Polycomb to restrain multi-lineage commitment in the early embryo. Development 138: 33-44.
36. Benjamin JM, Torke SJ, Demeler B, McGarry TJ, (2004) Geminin Has Dimerization, Cdt1-binding, and Destruction Domains That Are Required for Biological Activity. J Biol Chem 279: 45957-45968.
37. Kerns SL, Torke SJ, Benjamin JM, McGarry TJ, (2007) Geminin prevents rereplication during xenopus development. J Biol Chem 282: 5514-5521.
38. Maiorano D, Moreau J, Mechali M, (2000) XCDT1 is required for the assembly of pre-replicative complexes in Xenopus laevis. Nature 404: 622-625.
39. Newport J, Dasso M, (1989) On the coupling between DNA replication and mitosis. J Cell Sci (Suppl 12): 149-160.
40. Mihaylov IS, Kondo T, Jones L, Ryzhikov S, Tanaka J, et al. (2002) Control of DNA replication and chromosome ploidy by geminin and cyclin A. Mol Cell Biol 22: 1868-1880.
41. Kumagai A, Yakowec PS, Dunphy WG, (1998) 14-3-3 proteins act as negative regulators of the mitotic inducer Cdc25 in Xenopus egg extracts. Mol Biol Cell 9: 345-354.
42. Peng CY, Graves PR, Thoma RS, Wu Z, Shaw AS, et al. (1997) Mitotic and G2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216 [see comments]. Science 277: 1501-1505.
43. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM, (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858-5868.
44. Rogakou EP, Boon C, Redon C, Bonner WM, (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146: 905-916.
45. Guo Z, Dunphy WG, (2000) Response of Xenopus Cds1 in cell-free extracts to DNA templates with double-stranded ends. Mol Biol Cell 11: 1535-1546.
46. Lee CH, Chung JH, (2001) The hCds1 (Chk2)-FHA domain is essential for a chain of phosphorylation events on hCds1 that is induced by ionizing radiation. J Biol Chem 276: 30537-30541.
47. Schwarz JK, Lovly CM, Piwnica-Worms H, (2003) Regulation of the Chk2 protein kinase by oligomerization-mediated cis- and trans-phosphorylation. Mol Cancer Res 1: 598-609.
48. Wroble BN, Sible JC, (2005) Chk2/Cds1 protein kinase blocks apoptosis during early development of Xenopus laevis. Dev Dyn 233: 1359-1365.
49. Gonzalez MA, Tachibana KE, Adams DJ, van der Weyden L, Hemberger M, et al. (2006) Geminin is essential to prevent endoreduplication and to form pluripotent cells during mammalian development. Genes Dev 20: 1880-1884.
50. Hara K, Nakayama KI, Nakayama K, (2006) Geminin is essential for the development of preimplantation mouse embryos. Genes Cells 11: 1281-1293.
51. Quinn LM, Herr A, McGarry TJ, Richardson H, (2001) The Drosophila Geminin homolog: roles for Geminin in limiting DNA replication, in anaphase and in neurogenesis. Genes Dev 15: 2741-2754.
52. Melixetian M, Ballabeni A, Masiero L, Gasparini P, Zamponi R, et al. (2004) Loss of Geminin induces rereplication in the presence of functional p53. J Cell Biol 165: 473-482.
53. Mihaylov IS, Kondo T, Jones L, Ryzhikov S, Tanaka J, et al. (2002) Control of DNA replication and chromosome ploidy by geminin and cyclin A. Molecular & Cellular Biology 22: 1868-1880.
54. Vaziri C, Saxena S, Jeon Y, Lee C, Murata K, et al. (2003) A p53-dependent checkpoint pathway prevents rereplication. Mol Cell 11: 997-1008.
55. Zhu W, Chen Y, Dutta A, (2004) Rereplication by depletion of geminin is seen regardless of p53 status and activates a G2/M checkpoint. Mol Cell Biol 24: 7140-7150.
56. Reinhardt HC, Aslanian AS, Lees JA, Yaffe MB, (2007) p53-deficient cells rely on ATM- and ATR-mediated checkpoint signaling through the p38MAPK/MK2 pathway for survival after DNA damage. Cancer Cell 11: 175-189.
57. Keren A, Bengal E, (2010) Studying MAP Kinase pathways during early development of Xenopus laevis. Methods Mol Biol 661: 409-420.
58. Karamitros D, Kotantaki P, Lygerou Z, Veiga-Fernandes H, Pachnis V, et al. (2010) Differential geminin requirement for proliferation of thymocytes and mature T cells. J Immunol 184: 2432-2441.
59. Schultz KM, Banisadr G, Lastra RO, McGuire T, Kessler JA, et al. (2011) Geminin-deficient neural stem cells exhibit normal cell division and normal neurogenesis. PLoS One 6: e17736.
60. Shinnick KM, Eklund EA, McGarry TJ, (2010) Geminin deletion from hematopoietic cells causes anemia and thrombocytosis in mice. J Clin Invest 120: 4303-4315.
61. Spella M, Kyrousi C, Kritikou E, Stathopoulou A, Guillemot F, et al. (2011) Geminin regulates cortical progenitor proliferation and differentiation. Stem Cells 29: 1269-1282.
62. Nakajo N, Oe T, Uto K, Sagata N, (1999) Involvement of Chk1 kinase in prophase I arrest of Xenopus oocytes. Dev Biol 207: 432-444.
63. Matsuoka S, Huang M, Elledge SJ, (1998) Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 282: 1893-1897.
64. Nieuwkoop PD, Faber J, (1967) Normal Table of Xenopus laevis (Daudin). Amsterdam North-Holland Publishing Company.
65. Sive HL, Grainger RM, Harland RM, (2000) Early Development of Xenopus laevis. A Laboratory Manual. Cold Spring Harbor NY Cold SPring Harbor Press.
66. Blumberg B, Wright CV, De Robertis EM, Cho KW, (1991) Organizer-specific homeobox genes in Xenopus laevis embryos. Science 253: 194-196.
67. Smith WC, Harland RM, (1991) Injected Xwnt-8 RNA acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center. Cell 67: 753-765.
68. Hensey C, Gautier J, (1998) Programmed cell death during Xenopus development: a spatio-temporal analysis. Dev Biol 203: 36-48.
69. Sible JC, Anderson JA, Lewellyn AL, Maller JL, (1997) Zygotic transcription is required to block a maternal program of apoptosis in Xenopus embryos. Dev Biol 189: 335-346.