A Dynamic Scaffold of Pre-snoRNP Factors Facilitates Human Box C/D SnoRNP Assembly

Overview

Journal Mol Cell Biol

Specialty Cell Biology

Date 2007 Jul 20

PMID 17636026

Citations 58

Authors

Kenneth Scott McKeegan

Charles Maurice Debieux

Severine Boulon

Edouard Bertrand

Nicholas James Watkins

Affiliations

Soon will be listed here.

Abstract

The box C/D small nucleolar RNPs (snoRNPs) are essential for the processing and modification of rRNA. The core box C/D proteins are restructured during human U3 box C/D snoRNP biogenesis; however, the molecular basis of this is unclear. Here we show that the U8 snoRNP is also restructured, suggesting that this may occur with all box C/D snoRNPs. We have characterized four novel human biogenesis factors (BCD1, NOP17, NUFIP, and TAF9) which, along with the ATPases TIP48 and TIP49, are likely to be involved in the formation of the pre-snoRNP. We have analyzed the in vitro protein-protein interactions between the assembly factors and core box C/D proteins. Surprisingly, this revealed few interactions between the individual core box C/D proteins. However, the novel biogenesis factors and TIP48 and TIP49 interacted with one or more of the core box C/D proteins, implying that they mediate the assembly of the pre-snoRNP. Consistent with this, we show that NUFIP bridges interactions between the core box C/D proteins in a partially reconstituted pre-snoRNP. Restructuring of the core complex probably reflects the conversion of the pre-snoRNP, where core protein-protein interactions are maintained by the bridging biogenesis factors, to the mature snoRNP.

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References

Nottrott S, Hartmuth K, Fabrizio P, Urlaub H, Vidovic I, Ficner R . Functional interaction of a novel 15.5kD [U4/U6.U5] tri-snRNP protein with the 5' stem-loop of U4 snRNA. EMBO J. 1999; 18(21):6119-33. PMC: 1171676. DOI: 10.1093/emboj/18.21.6119. View

Frank S, Parisi T, Taubert S, Fernandez P, Fuchs M, Chan H . MYC recruits the TIP60 histone acetyltransferase complex to chromatin. EMBO Rep. 2003; 4(6):575-80. PMC: 1319201. DOI: 10.1038/sj.embor.embor861. View

Sauer R, Bolon D, Burton B, Burton R, Flynn J, Grant R . Sculpting the proteome with AAA(+) proteases and disassembly machines. Cell. 2004; 119(1):9-18. PMC: 2717008. DOI: 10.1016/j.cell.2004.09.020. View

Dignam J, Lebovitz R, Roeder R . Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983; 11(5):1475-89. PMC: 325809. DOI: 10.1093/nar/11.5.1475. View

Klemm R, Goodrich J, Zhou S, Tjian R . Molecular cloning and expression of the 32-kDa subunit of human TFIID reveals interactions with VP16 and TFIIB that mediate transcriptional activation. Proc Natl Acad Sci U S A. 1995; 92(13):5788-92. PMC: 41586. DOI: 10.1073/pnas.92.13.5788. View

MAXWELL E, Fournier M . The small nucleolar RNAs. Annu Rev Biochem. 1995; 64:897-934. DOI: 10.1146/annurev.bi.64.070195.004341. View

Gautier T, Berges T, Tollervey D, Hurt E . Nucleolar KKE/D repeat proteins Nop56p and Nop58p interact with Nop1p and are required for ribosome biogenesis. Mol Cell Biol. 1997; 17(12):7088-98. PMC: 232565. DOI: 10.1128/MCB.17.12.7088. View

Weinstein L, Steitz J . Guided tours: from precursor snoRNA to functional snoRNP. Curr Opin Cell Biol. 1999; 11(3):378-84. DOI: 10.1016/S0955-0674(99)80053-2. View

Jonsson Z, Jha S, Wohlschlegel J, Dutta A . Rvb1p/Rvb2p recruit Arp5p and assemble a functional Ino80 chromatin remodeling complex. Mol Cell. 2004; 16(3):465-77. DOI: 10.1016/j.molcel.2004.09.033. View

10.

Peng W, Robinson M, Mnaimneh S, Krogan N, Cagney G, Morris Q . A panoramic view of yeast noncoding RNA processing. Cell. 2003; 113(7):919-33. DOI: 10.1016/s0092-8674(03)00466-5. View

11.

Tran E, Zhang X, Maxwell E . Efficient RNA 2'-O-methylation requires juxtaposed and symmetrically assembled archaeal box C/D and C'/D' RNPs. EMBO J. 2003; 22(15):3930-40. PMC: 169041. DOI: 10.1093/emboj/cdg368. View

12.

Hirose T, Shu M, Steitz J . Splicing-dependent and -independent modes of assembly for intron-encoded box C/D snoRNPs in mammalian cells. Mol Cell. 2003; 12(1):113-23. DOI: 10.1016/s1097-2765(03)00267-3. View

13.

Rashid R, Aittaleb M, Chen Q, Spiegel K, Demeler B, Li H . Functional requirement for symmetric assembly of archaeal box C/D small ribonucleoprotein particles. J Mol Biol. 2003; 333(2):295-306. DOI: 10.1016/j.jmb.2003.08.012. View

14.

Granneman S, Baserga S . Ribosome biogenesis: of knobs and RNA processing. Exp Cell Res. 2004; 296(1):43-50. DOI: 10.1016/j.yexcr.2004.03.016. View

15.

Yong J, Wan L, Dreyfuss G . Why do cells need an assembly machine for RNA-protein complexes?. Trends Cell Biol. 2004; 14(5):226-32. DOI: 10.1016/j.tcb.2004.03.010. View

16.

cabart P, Chew H, Murphy S . BRCA1 cooperates with NUFIP and P-TEFb to activate transcription by RNA polymerase II. Oncogene. 2004; 23(31):5316-29. DOI: 10.1038/sj.onc.1207684. View

17.

Schaffert N, Hossbach M, Heintzmann R, Achsel T, Luhrmann R . RNAi knockdown of hPrp31 leads to an accumulation of U4/U6 di-snRNPs in Cajal bodies. EMBO J. 2004; 23(15):3000-9. PMC: 514917. DOI: 10.1038/sj.emboj.7600296. View

18.

Nazar R . Ribosomal RNA processing and ribosome biogenesis in eukaryotes. IUBMB Life. 2004; 56(8):457-65. DOI: 10.1080/15216540400010867. View

19.

Kiss T . Biogenesis of small nuclear RNPs. J Cell Sci. 2004; 117(Pt 25):5949-51. DOI: 10.1242/jcs.01487. View

20.

Boulon S, Verheggen C, Jady B, Girard C, Pescia C, Paul C . PHAX and CRM1 are required sequentially to transport U3 snoRNA to nucleoli. Mol Cell. 2004; 16(5):777-87. DOI: 10.1016/j.molcel.2004.11.013. View