A Sequence in the Drosophila H3-H4 Promoter Triggers Histone Locus Body Assembly and Biosynthesis of Replication-Coupled Histone mRNAs

Developmental Cell

Volumn 24, Issue 6, 2013, Pages 623-634

  Salzler, Harmony R ^a   Tatomer, Deirdre C ^a   Malek, Pamela Y ^a   McDaniel, Stephen L ^a   Orlando, Anna N ^a   Marzluff, William F ^a,b   Duronio, Robert J ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; HISTONE H4; MESSENGER RNA;

ARTICLE; DROSOPHILA; GENE CLUSTER; GENE LOCUS; GENETIC VARIABILITY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RNA REPLICATION; TRANSGENE;

ANIMALS; DNA REPLICATION; DROSOPHILA; GENE EXPRESSION; HISTONES; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EUKARYOTA;

EID: 84875599991     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2013.02.014     Document Type: Article

References (61)

1. Azzouz T.N., Schumperli D. Evolutionary conservation of the U7 small nuclear ribonucleoprotein in Drosophila melanogaster. RNA 2003, 9:1532-1541.
2. Bateman J.R., Lee A.M., Wu C.T. Site-specific transformation of Drosophila via phiC31 integrase-mediated cassette exchange. Genetics 2006, 173:769-777.
3. Bischof J., Maeda R.K., Hediger M., Karch F., Basler K. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 2007, 104:3312-3317.
4. Boisvert F.M., van Koningsbruggen S., Navascués J., Lamond A.I. The multifunctional nucleolus. Nat. Rev. Mol. Cell Biol. 2007, 8:574-585.
5. Bongiorno-Borbone L., De Cola A., Vernole P., Finos L., Barcaroli D., Knight R.A., Melino G., De Laurenzi V. FLASH and NPAT positive but not Coilin positive Cajal Bodies correlate with cell ploidy. Cell Cycle 2008, 7:2357-2367.
6. Bongiorno-Borbone L., De Cola A., Barcaroli D., Knight R.A., Di Ilio C., Melino G., De Laurenzi V. FLASH degradation in response to UV-C results in histone locus bodies disruption and cell-cycle arrest. Oncogene 2010, 29:802-810.
7. Bulchand S., Menon S.D., George S.E., Chia W. Muscle wasted: a novel component of the Drosophila histone locus body required for muscle integrity. J. Cell Sci. 2010, 123:2697-2707.
8. Burch B.D., Godfrey A.C., Gasdaska P.Y., Salzler H.R., Duronio R.J., Marzluff W.F., Dominski Z. Interaction between FLASH and Lsm11 is essential for histone pre-mRNA processing in vivo in Drosophila. RNA 2011, 17:1132-1147.
9. Burch B.D., Godfrey A.C., Gasdaska P.Y., Salzler H.R., Duronio R.J., Marzluff W.F., Dominski Z. Interaction between FLASH and Lsm11 is essential for histone pre-mRNA processing in vivo in Drosophila. RNA 2011, 17:1132-1147.
10. Carmo-Fonseca M., Rino J. RNA seeds nuclear bodies. Nat. Cell Biol. 2011, 13:110-112.
11. Chen M., Galvão R.M., Li M., Burger B., Bugea J., Bolado J., Chory J. Arabidopsis HEMERA/pTAC12 initiates photomorphogenesis by phytochromes. Cell 2010, 141:1230-1240.
12. Denissov S., Lessard F., Mayer C., Stefanovsky V., van Driel M., Grummt I., Moss T., Stunnenberg H.G. A model for the topology of active ribosomal RNA genes. EMBO Rep. 2011, 12:231-237.
13. Deryusheva S., Gall J.G. Small Cajal body-specific RNAs of Drosophila function in the absence of Cajal bodies. Mol. Biol. Cell 2009, 20:5250-5259.
14. Dundr M. Seed and grow: a two-step model for nuclear body biogenesis. J. Cell Biol. 2011, 193:605-606.
15. Frey M.R., Matera A.G. Coiled bodies contain U7 small nuclear RNA and associate with specific DNA sequences in interphase human cells. Proc. Natl. Acad. Sci. USA 1995, 92:5915-5919.
16. Fung J.C., Marshall W.F., Dernburg A., Agard D.A., Sedat J.W. Homologous chromosome pairing in Drosophila melanogaster proceeds through multiple independent initiations. J. Cell Biol. 1998, 141:5-20.
17. Ghule P.N., Dominski Z., Yang X.C., Marzluff W.F., Becker K.A., Harper J.W., Lian J.B., Stein J.L., van Wijnen A.J., Stein G.S. Staged assembly of histone gene expression machinery at subnuclear foci in the abbreviated cell cycle of human embryonic stem cells. Proc. Natl. Acad. Sci. USA 2008, 105:16964-16969.
18. Godfrey A.C., Kupsco J.M., Burch B.D., Zimmerman R.M., Dominski Z., Marzluff W.F., Duronio R.J. U7 snRNA mutations in Drosophila block histone pre-mRNA processing and disrupt oogenesis. RNA 2006, 12:396-409.
19. Godfrey A.C., White A.E., Tatomer D.C., Marzluff W.F., Duronio R.J. The Drosophila U7 snRNP proteins Lsm10 and Lsm11 are required for histone pre-mRNA processing and play an essential role in development. RNA 2009, 15:1661-1672.
20. Günesdogan U., Jäckle H., Herzig A. A genetic system to assess in vivo the functions of histones and histone modifications in higher eukaryotes. EMBO Rep. 2010, 11:772-776.
21. Gunjan A., Verreault A. A Rad53 kinase-dependent surveillance mechanism that regulates histone protein levels in S. cerevisiae. Cell 2003, 115:537-549.
22. Hammond M.P., Laird C.D. Control of DNA replication and spatial distribution of defined DNA sequences in salivary gland cells of Drosophila melanogaster. Chromosoma 1985, 91:279-286.
23. Handwerger K.E., Gall J.G. Subnuclear organelles: new insights into form and function. Trends Cell Biol. 2006, 16:19-26.
24. Hernandez-Verdun D. The nucleolus: a model for the organization of nuclear functions. Histochem. Cell Biol. 2006, 126:135-148.
25. Hernandez-Verdun D., Robert-Nicoud M., Geraud G., Masson C. Behaviour of nucleolar proteins in nuclei lacking ribosomal genes. A study by confocal laser scanning microscopy. J. Cell Sci. 1991, 98:99-105.
26. Kaiser T.E., Intine R.V., Dundr M. De novo formation of a subnuclear body. Science 2008, 322:1713-1717.
27. Karpen G.H., Schaefer J.E., Laird C.D. A Drosophila rRNA gene located in euchromatin is active in transcription and nucleolus formation. Genes Dev. 1988, 2(12B):1745-1763.
28. Lanzotti D.J., Kaygun H., Yang X., Duronio R.J., 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. 2002, 22:2267-2282.
29. Liu J.L., Murphy C., Buszczak M., Clatterbuck S., Goodman R., Gall J.G. The Drosophila melanogaster Cajal body. J. Cell Biol. 2006, 172:875-884.
30. Liu J.L., Wu Z., Nizami Z., Deryusheva S., Rajendra T.K., Beumer K.J., Gao H., Matera A.G., Carroll D., Gall J.G. Coilin is essential for Cajal body organization in Drosophila melanogaster. Mol. Biol. Cell 2009, 20:1661-1670.
31. Ma T., Van Tine B.A., Wei Y., Garrett M.D., Nelson D., Adams P.D., Wang J., Qin J., Chow L.T., Harper J.W. Cell cycle-regulated phosphorylation of p220(NPAT) by cyclin E/Cdk2 in Cajal bodies promotes histone gene transcription. Genes Dev. 2000, 14:2298-2313.
32. Mao Y.S., Sunwoo H., Zhang B., Spector D.L. Direct visualization of the co-transcriptional assembly of a nuclear body by noncoding RNAs. Nat. Cell Biol. 2011, 13:95-101.
33. Marzluff W.F. Terminating histone synthesis to preserve centromere integrity. Dev. Cell 2010, 18:335-336.
34. Marzluff W.F., Duronio R.J. Histone mRNA expression: multiple levels of cell cycle regulation and important developmental consequences. Curr. Opin. Cell Biol. 2002, 14:692-699.
35. Marzluff W.F., Wagner E.J., Duronio R.J. Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat. Rev. Genet. 2008, 9:843-854.
36. Matera A.G., Izaguire-Sierra M., Praveen K., Rajendra T.K. Nuclear bodies: random aggregates of sticky proteins or crucibles of macromolecular assembly?. Dev. Cell 2009, 17:639-647.
37. Meeks-Wagner D., Hartwell L.H. Normal stoichiometry of histone dimer sets is necessary for high fidelity of mitotic chromosome transmission. Cell 1986, 44:43-52.
38. Miele A., Braastad C.D., Holmes W.F., Mitra P., Medina R., Xie R., Zaidi S.K., Ye X., Wei Y., Harper J.W., et al. HiNF-P directly links the cyclin E/CDK2/p220NPAT pathway to histone H4 gene regulation at the G1/S phase cell cycle transition. Mol. Cell. Biol. 2005, 25:6140-6153.
39. Misteli T. The concept of self-organization in cellular architecture. J. Cell Biol. 2001, 155:181-185.
40. Misteli T. Concepts in nuclear architecture. Bioessays 2005, 27:477-487.
41. Misteli T. Beyond the sequence: cellular organization of genome function. Cell 2007, 128:787-800.
42. Moore G.D., Sinclair D.A., Grigliatti T.A. Histone gene multiplicity and position effect variegation in Drosophila melanogaster. Genetics 1983, 105:327-344.
43. Nechaev S., Fargo D.C., dos Santos G., Liu L., Gao Y., Adelman K. Global analysis of short RNAs reveals widespread promoter-proximal stalling and arrest of Pol II in Drosophila. Science 2010, 327:335-338.
44. Nizami Z., Deryusheva S., Gall J.G. The Cajal body and histone locus body. Cold Spring Harb. Perspect. Biol. 2010, 2:a000653.
45. Paro R. Mapping protein distribution on polytene chromosomes by immunostaining. Drosophila Protocols 2000, 131-140. Cold Spring Harbor Press, New York. W. Sullivan, M. Ashburner, R.S. Hawley (Eds.).
46. Pillai R.S., Grimmler M., Meister G., Will C.L., Lührmann R., Fischer U., Schümperli D. Unique Sm core structure of U7 snRNPs: assembly by a specialized SMN complex and the role of a new component, Lsm11, in histone RNA processing. Genes Dev. 2003, 17:2321-2333.
47. Prieto J.L., McStay B. Pseudo-NORs: a novel model for studying nucleoli. Biochim. Biophys. Acta 2008, 1783:2116-2123.
48. Rajendra T.K., Praveen K., Matera A.G. Genetic Analysis of Nuclear Bodies: From Nondeterministic Chaos to Deterministic Order. Cold Spring Harb. Symp. Quant. Biol. 2010, 75:365-374.
49. Saget O., Forquignon F., Santamaria P., Randsholt N.B. Needs and targets for the multi sex combs gene product in Drosophila melanogaster. Genetics 1998, 149:1823-1838.
50. Shevtsov S.P., Dundr M. Nucleation of nuclear bodies by RNA. Nat. Cell Biol. 2011, 13:167-173.
51. Strzelecka M., Trowitzsch S., Weber G., Lührmann R., Oates A.C., Neugebauer K.M. Coilin-dependent snRNP assembly is essential for zebrafish embryogenesis. Nat. Struct. Mol. Biol. 2010, 17:403-409.
52. Tucker K.E., Berciano M.T., Jacobs E.Y., LePage D.F., Shpargel K.B., Rossire J.J., Chan E.K., Lafarga M., Conlon R.A., Matera A.G. Residual Cajal bodies in coilin knockout mice fail to recruit Sm snRNPs and SMN, the spinal muscular atrophy gene product. J. Cell Biol. 2001, 154:293-307.
53. Wagner E.J., Burch B.D., Godfrey A.C., Salzler H.R., Duronio R.J., Marzluff W.F. A genome-wide RNA interference screen reveals that variant histones are necessary for replication-dependent histone pre-mRNA processing. Mol. Cell 2007, 28:692-699.
54. Walker M.P., Tian L., Matera A.G. Reduced viability, fertility and fecundity in mice lacking the cajal body marker protein, coilin. PLoS ONE 2009, 4:e6171.
55. Wei Y., Jin J., Harper J.W. The cyclin E/Cdk2 substrate and Cajal body component p220(NPAT) activates histone transcription through a novel LisH-like domain. Mol. Cell. Biol. 2003, 23:3669-3680.
56. White A.E., Leslie M.E., Calvi B.R., Marzluff W.F., Duronio R.J. Developmental and cell cycle regulation of the Drosophila histone locus body. Mol. Biol. Cell 2007, 18:2491-2502.
57. White A.E., Burch B.D., Yang X.C., Gasdaska P.Y., Dominski Z., Marzluff W.F., Duronio R.J. Drosophila histone locus bodies form by hierarchical recruitment of components. J. Cell Biol. 2011, 193:677-694.
58. Yang X.C., Burch B.D., Yan Y., Marzluff W.F., Dominski Z. FLASH, a proapoptotic protein involved in activation of caspase-8, is essential for 3' end processing of histone pre-mRNAs. Mol. Cell 2009, 36:267-278.
59. Ye X., Wei Y., Nalepa G., Harper J.W. The cyclin E/Cdk2 substrate p220(NPAT) is required for S-phase entry, histone gene expression, and Cajal body maintenance in human somatic cells. Mol. Cell. Biol. 2003, 23:8586-8600.
60. Zeitlinger J., Stark A., Kellis M., Hong J.W., Nechaev S., Adelman K., Levine M., Young R.A. RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nat. Genet. 2007, 39:1512-1516.
61. Zhao J., Kennedy B.K., Lawrence B.D., Barbie D.A., Matera A.G., Fletcher J.A., Harlow E. NPAT links cyclin E-Cdk2 to the regulation of replication-dependent histone gene transcription. Genes Dev. 2000, 14:2283-2297.