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

Volumn 313, Issue 1, 2008, Pages 347-358

  Arnold, Daniel R ^a   Françon, Patricia ^a   Zhang, James ^a   Martin, Kyle ^a   Clarke, Hugh J ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Early embryogenesis; Histones; Maternal control; Oogenesis; SLBP

Indexed keywords

BINDING PROTEIN; GAMMA HISTONE H2A; HISTONE H2A; HISTONE H3; HISTONE H4; MESSENGER RNA; UNCLASSIFIED DRUG;

ARTICLE; CELL GROWTH; EMBRYO DEVELOPMENT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENIC MOUSE;

MUS MUSCULUS;

EID: 37349100253     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2007.10.032     Document Type: Article

References (64)

1. Allard P., Champigny M.J., Skoggard S., Erkmann J.A., Whitfield M.L., Marzluff W.F., and Clarke H.J. Stem-loop binding protein accumulates during oocyte maturation and is not cell-cycle-regulated in the early mouse embryo. J. Cell. Sci. 115 (2002) 4577-4586
2. Allard P., Yang Q., Marzluff W.F., and Clarke H.J. The stem-loop binding protein regulates translation of histone mRNA during mammalian oogenesis. Dev. Biol. 286 (2005) 195-206
3. Ambrosio L., and Schedl P. Two discrete modes of histone gene expression during oogenesis in Drosophila melanogaster. Dev. Biol. 111 (1985) 220-231
4. Anderson K.V., and Lengyel J.A. Changing rates of histone mRNA synthesis and turnover in Drosophila embryos. Cell 21 (1980) 717-727
5. Belyaev N.D., Keohane A.M., and Turner B.M. Histone H4 acetylation and replication timing in Chinese hamster chromosomes. Exp. Cell Res. 225 (1996) 277-285
6. Crest J., Oxnard N., Ji J.-Y., and Schubiger G. Onset of the DNA replication checkpoint in the early Drosophila embryo. Genetics 175 (2007) 567-584
7. Dominski Z., Zheng L.X., Sanchez R., and Marzluff W.F. Stem-loop binding protein facilitates 3′-end formation by stabilizing U7 snRNP binding to histone pre-mRNA. Mol. Cell. Biol. 19 (1999) 3561-3570
8. Dominski Z., Erkmann J.A., Greenland J.A., and Marzluff W.F. Mutations in the RNA binding domain of stem-loop binding protein define separable requirements for RNA binding and for histone pre-mRNA processing. Mol. Cell. Biol. 21 (2001) 2008-2017
9. Dominski Z., Yang X.-C., and Marzluff W.F. The polyadenylation factor CPSF-73 is involved in histone-pre-mRNA processing. Cell 123 (2005) 37-48
10. Eppig J.J., and Telfer E.E. Isolation and culture of oocytes. Methods Enzymol. 225 (1993) 77-84
11. Fedoriw A.M., Stein P., Svoboda P., Schultz R.M., and Bartolomei M.S. Transgenic RNAi reveals essential function for CTCF in H19 gene imprinting. Science 303 (2004) 238-240
12. Ferreira J., and Carmo-Fonseca M. Genome replication in early mouse embryos follows a defined temporal and spatial order. J. Cell. Sci. 110 (1997) 889-897
13. Fu G., Ghadam P., Sirotkin A., Khochbin S., Skoultchi A.I., and Clarke H.J. Mouse oocytes and early embryos express multiple histone H1 subtypes. Biol. Reprod. 68 (2003) 1569-1576
14. Gilbert D.M. Replication timing and transcriptional control: beyond cause and effect. Curr. Opin. Cell Biol. 14 (2002) 377-383
15. Gorgoni B., Andrews S., Schaller A., Schumperli D., Gray N.K., and Muller B. The stem-loop binding protein stimulates histone translation at an early step in the initiation pathway. RNA 11 (2005) 1030-1042
16. Graves R.A., Marzluff W.F., Giebelhaus D.H., and Schultz G.A. Quantitative and qualitative changes in histone gene expression during early mouse embryo development. Proc. Natl. Acad. Sci. U. S. A. 82 (1985) 5685-5689
17. Han S.J., Chen R., Paronetto M.P., and Conti M. Wee1B is an oocyte-specific kinase involved in the control of meiotic arrest in the mouse. Curr. Biol. 15 (2005) 1670-1676
18. Henikoff S., and Ahmad K. Assembly of variant histones into chromatin. Annu. Rev. Cell Dev. Biol. 21 (2005) 133-153
19. Jaeger S., Barends S., Giege R., Eriani G., and Martin F. Expression of metazoan replication-dependent histone genes. Biochimie 87 (2005) 827-834
20. Kanka J. Gene expression and chromatin structure in the pre-implantation embryo. Theriogenology 59 (2003) 3-19
21. Kodama Y., Rothman J.H., Sugimoto A., and Yamamoto M. The stem-loop binding protein CDL-1 is required for chromosome condensation, progression of cell death and morphogenesis in Caenorhabditis elegans. Development 129 (2002) 187-196
22. Kolev N.G., and Steitz J.A. Symplekin and multiple other polyadenylation factors participate in 3′-end maturation of histone mRNAs. Genes Dev. 19 (2005) 2583-2592
23. Lanzotti D.J., Kaygun H., Yang X., Duronio R.J., and Marzluff W.F. Developmental control of histone mRNA and dSLBP synthesis during Drosophila embryogenesis and the role of dSLBP in histone mRNA 3′ end processing in vivo. Mol. Cell. Biol. 22 (2002) 2267-2282
24. Levine B.J., Chodchoy N., Marzluff W.F., and Skoultchi A.I. Coupling of replication type histone mRNA levels to DNA synthesis requires the stem-loop sequence at the 3′ end of the mRNA. Proc. Natl. Acad. Sci. 84 (1987) 6189-6193
25. Lilly M.A., and Duronio R.J. New insights into cell cycle control from the Drosophila endocycle. Oncogene 24 (2005) 2765-2775
26. Ling J., Morley S.J., Pain V.M., Marzluff W.F., and Gallie D.R. The histone 3′-terminal stern-loop-binding protein enhances translation through a functional and physical interaction with eukaryotic initiation factor 4G (eIF4G) and eIF3. Mol. Cell. Biol. 22 (2002) 7853-7867
27. Ma J., Zeng F., Schultz R.M., and Tseng H. Basonuclin: a novel mammalian maternal-effect gene. Development 133 (2006) 2053-2062
28. Martin F., Schaller A., Eglite S., Schumperli D., and Muller B. The gene for histone RNA hairpin binding protein is located on human chromosome 4 and encodes a novel type of RNA binding protein. EMBO J. 16 (1997) 769-778
29. Marzluff W.F. Metazoan replication-dependent histone mRNAs: a distinct set of RNA polymerase II transcripts. Curr. Opin. Cell Biol. 17 (2005) 274-280
30. Marzluff W.F., and Duronio R.J. Histone mRNA expression: multiple levels of cell cycle regulation and important developmental consequences. Curr. Opin. Cell Biol. 14 (2002) 692-699
31. Marzluff W.F., Gongidi P., Woods K.R., Jin J.P., and Maltais L.J. The human and mouse replication-dependent histone genes. Genomics 80 (2002) 487-498
32. Mcnairn A.J., and Gilbert D.M. Epigenomic replication: linking epigenetics to DNA replication. BioEssays 25 (2003) 647-656
33. Mohamed O.A., Bustin M., and Clarke H.J. High-mobility group proteins 14 and 17 maintain the timing of early embryonic development in the mouse. Dev. Biol. 229 (2001) 237-249
34. Moss S.B., Challoner P.B., and Groudine M. Expression of a novel histone 2B during mouse spermiogenesis. Dev. Biol. 133 (1989) 83-92
35. Moss S.B., Ferry R.A., and Groudine M. An alternative pathway of histone mRNA 3′ end formation in mouse round spermatids. Nucleic Acids Res. 22 (1994) 3160-3166
36. Narita T., Yung T.M., Yamamoto J., Tsuboi Y., Tanabe H., Tanaka K., Yamaguchi Y., and Handa H. NELF interacts with CBC and participates in 3′ end processing of replication-dependent histone mRNAs. Mol. Cell 26 (2007) 349-365
37. Nelson D.M., Ye X., Hall C., Santos H., Ma T., Kao G.D., Yen T.J., Harper J.W., and Adams P.D. Coupling of DNA synthesis and histone synthesis in S phase independent of cyclin/cdk2 activity. Mol. Cell. Biol. 22 (2002) 7459-7472
38. Nightingale K.P., O'Neill L.P., and Turner B.M. Histone modifications: signalling receptors and potential elements of a heritable epigenetic code. Curr. Opin. Genet. Dev. 16 (2006) 125-136
39. Osley M.A. The regulation of histone synthesis in the cell cycle. Annu. Rev. Biochem. 60 (1991) 827-861
40. Pettitt J., Crombie C., Schumperli D., and Muller B. The Caenorhabditis elegans histone hairpin-binding protein is required for core histone gene expression and is essential for embryonic and postembryonic cell division. J. Cell. Sci. 115 (2002) 857-866
41. Philpott C.C., Ringuette M.J., and Dean J. Oocyte-specific expression and developmental regulation of ZP3, the sperm receptor of the mouse zona pellucida. Dev. Biol. 121 (1987) 568-575
42. Robertson A.J., Howard J.T., Dominski Z., Schnackenberg B.J., Sumerel J.L., McCarthy J.J., Coffman J.A., and Marzluff W.F. The sea urchin stem-loop-binding protein: a maternally expressed protein that probably functions in expression of multiple classes of histone mRNA. Nucleic Acids Res. 32 (2004) 811-818
43. Ruddell A., and Jacobs-Lorena M. Biphasic pattern of histone gene expression during Drosophila oogenesis. Proc. Natl. Acad. Sci. 82 (1985) 3316-3319
44. Sanchez R., and Marzluff W.F. The stem-loop binding protein is required for efficient translation of histone mRNA in vivo and in vitro. Mol. Cell. Biol. 22 (2002) 7093-7104
45. Sanchez R., and Marzluff W.F. The oligo(A) tail on histone mRNA plays an active role in translational silencing of histone mRNA during Xenopus oogenesis. Mol. Cell. Biol. 24 (2004) 2513-2525
46. Schultz R.M. The molecular foundations of the maternal to zygotic transition in the preimplantation mouse embryo. Hum. Reprod. Updat. 8 (2002) 323-331
47. Sobel R., Cook R., Perry C., Annunziato A., and Allis C. Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc. Natl. Acad. Sci. 92 (1995) 1237-1241
48. Stein P., Svoboda P., and Schultz R.M. Transgenic RNAi in mouse oocytes: a simple and fast approach to study gene function. Dev. Biol. 256 (2003) 188-194
49. Sullivan E., Santiago C., Parker E.D., Dominski Z., Yang X.C., Lanzotti D.J., Ingledue T.C., Marzluff W.F., and Duronio R.J. Drosophila stem loop binding protein coordinates accumulation of mature histone mRNA with cell cycle progression. Genes Dev. 15 (2001) 173-187
50. Svoboda P., Stein P., and Schultz R.M. RNAi in mouse oocytes and preimplantation embryos: Effectiveness of hairpin dsRNA. Biochem. Biophys. Res. Commun. 287 (2001) 1099-1104
51. Torres-Padilla M.-E., Bannister A.J., Hurd P.J., Kouzarides T., and Zernicka-Goetz M. Dynamic distribution of the replacement histone variant H3.3 in the mouse oocyte and preimplantation embryos. Int. J. Dev. Biol. 50 (2006) 455-461
52. Townley-Tilson W.H.D., Pendergrass S.A., Marzluff W.F., and Whitfield M.L. Genome-wide analysis of mRNAs bound to the histone stem-loop binding protein. RNA 12 (2006) 1853-1867
53. Van Der Heijden G.W., Dieker J.W., Derijck A.A.H.A., Muller S., Berden J.H.M., Braat D.D.M., Van Der Vlag J., and De Boer P. Asymmetry in Histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote. Mech. Dev. 122 (2005) 1008-1022
54. Wallace J.A., and Orr-Weaver T.L. Replication of heterochromatin: insights into mechanisms of epigenetic inheritance. Chromosoma 114 (2005) 389-402
55. Wang Z.F., Whitfield M.L., Ingledue T.C., Dominski Z., and Marzluff W.F. The protein that binds the 3′ end of histone mRNA: A novel RNA- binding protein required for histone pre-mRNA processing. Genes Dev. 10 (1996) 3028-3040
56. Wang Z.F., Ingledue T.C., Dominski Z., Sanchez R., and Marzluff W.F. Two Xenopus proteins that bind the 3′ end of histone mRNA: implications for translational control of histone synthesis during oogenesis. Mol. Cell. Biol. 19 (1999) 835-845
57. Wassarman P.M. The mammalian ovum. In: Knobil E. (Ed). The Physiology of Reproduction (1988), Raven Press, New York 69-101
58. Whitfield M.L., Zheng L.X., Baldwin A., Ohta T., Hurt M.M., and Marzluff W.F. Stem-loop binding protein, the protein that binds the 3′ end of histone mRNA, is cell cycle regulated by both translational and posttranslational mechanisms. Mol. Cell. Biol. 20 (2000) 4188-4198
59. Whitfield M.L., Kaygun H., Erkmann J.A., Townley-Tilson W.H.D., Dominski Z., and Marzluff W.F. SLBP is associated with histone mRNA on polyribosomes as a component of the histone mRNP. Nucleic Acids Res. 32 (2004) 4833-4842
60. Woodland H.R. Histone synthesis during the development of Xenopus. FEBS Lett. 121 (1980) 1-7
61. Wurtele H., and Verreault A. Histone post-translational modifications and the response to DNA double-strand breaks. Curr. Opin. Cell Biol. 18 (2006) 137-144
62. Ye X., Franco A.A., Santos H., Nelson D.M., Kaufman P.D., and Adams P.D. Defective S phase chromatin assembly causes DNA damage, activation of the S phase checkpoint, and S phase arrest. Mol. Cell 11 (2003) 341-351
63. Zhao X., McKillop-Smith S., and Muller B. The human histone gene expression regulator HBP/SLBP is required for histone and DNA synthesis, cell cycle progression and cell proliferation in mitotic cells. J. Cell. Sci. 117 (2004) 6043-6051
64. Zheng L.X., Dominski Z., Yang X.C., Elms P., Raska C.S., Borchers C.H., and Marzluff W.F. Phosphorylation of stem-loop binding protein (SLBP) on two threonines triggers degradation of SLBP, the sole cell cycle-regulated factor required for regulation of histone mRNA processing, at the end of S phase. Mol. Cell. Biol. 23 (2003) 1590-1601