Supraspliceosomes at defined functional states portray the pre-assembled nature of the pre-mRNA processing machine in the cell nucleus

International Journal of Molecular Sciences

Volumn 15, Issue 7, 2014, Pages 11637-11664

  Kotzer Nevo, Hani ^a   de Lima Alves, Flavia ^b   Rappsilber, Juri ^b,c   Sperling, Joseph ^d   Sperling, Ruth ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^d WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

PP7 tagged supraspliceosomes; pre mRNA splicing; Specific supraspliceosomes; U snRNPs

Indexed keywords

MESSENGER RNA PRECURSOR; SMALL NUCLEAR RIBONUCLEOPROTEIN; MESSENGER RNA; RNA PRECURSOR; VIRUS PROTEIN; VIRUS RNA;

ADENOVIRUS; ARTICLE; BACTERIOPHAGE; BASE PAIRING; CELL NUCLEUS; CONTROLLED STUDY; HUMAN CELL; MASS SPECTROMETRY; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PLASMID; PROTEIN ANALYSIS; PROTEIN PURIFICATION; PSEUDOMONAS AERUGINOSA PHAGE 7; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA BINDING; RNA ISOLATION; RNA PROCESSING; RNA PURIFICATION; RNA SPLICING; SPLICEOSOME; SUPRASPLICEOSOME; WESTERN BLOTTING; ADENOVIRIDAE; GENETICS; HELA CELL LINE; HUMAN; LEVIVIRUS; METABOLISM; PSEUDOMONAS AERUGINOSA; VIROLOGY;

ADENOVIRIDAE; CELL NUCLEUS; HELA CELLS; HUMANS; LEVIVIRUS; PSEUDOMONAS AERUGINOSA; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA PRECURSORS; RNA, MESSENGER; RNA, VIRAL; SPLICEOSOMES; VIRAL PROTEINS;

EID: 84903698579     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms150711637     Document Type: Article

References (58)

1. Will, C.L.; Luhrmann, R. Spliceosome structure and function. Cold Spring Harb. Perspect. Biol. 2011, 3, a003707.
2. Burge, C.B.; Tuschl, T.H.; Sharp, P.A. The RNA World, 2nd ed.; Gesteland, R.F., Cech, T.R., Atkins, J.F., Eds.; Cold Spring Harbor Laboratory Press: New York, NY, USA, 1999; pp. 525-560.
3. Brow, D.A. Allosteric cascade of spliceosome activation. Annu. Rev. Genet. 2002, 36, 333-360.
4. Will, C.L.; Lührmann, R. Spliceosomal UsnRNP biogenesis, structure and function. Curr. Opin. Cell Biol. 2001, 13, 290-301.
5. Staley, J.P.; Guthrie, C. Mechanical devices of the spliceosome: Motors, clocks, springs, and things. Cell 1998, 92, 315-326.
6. Lin, S.; Fu, X.D. SR proteins and related factors in alternative splicing. Adv. Exp. Med. Biol. 2007, 623, 107-122.
7. Shepard, P.J.; Hertel, K.J. The SR protein family. Genome Biol. 2009, 10, 242.
8. Long, J.C.; Caceres, J.F. The SR protein family of splicing factors: Master regulators of gene expression. Biochem. J. 2009, 417, 15-27.
9. Han, S.P.; Tang, Y.H.; Smith, R. Functional diversity of the hnRNPs: Past, present and perspectives. Biochem. J. 2010, 430, 379-392.
10. Rappsilber, J.; Ryder, U.; Lamond, A.I.; Mann, M. Large-scale proteomic analysis of the human spliceosome. Genome Res. 2002, 12, 1231-1245.
11. Hegele, A.; Kamburov, A.; Grossmann, A.; Sourlis, C.; Wowro, S.; Weimann, M.; Will, C.L.; Pena, V.; Luhrmann, R.; Stelzl, U. Dynamic protein-protein interaction wiring of the human spliceosome. Mol. Cell 2012, 45, 567-580.
12. Chen, Y.I.; Moore, R.E.; Ge, H.Y.; Young, M.K.; Lee, T.D.; Stevens, S.W. Proteomic analysis of in vivo-assembled pre-mRNA splicing complexes expands the catalog of participating factors. Nucleic Acids Res. 2007, 35, 3928-3944.
13. Sperling, J.; Azubel, M.; Sperling, R. Structure and function of the pre-mRNA splicing machine. Structure 2008, 16, 1605-1615.
14. Miriami, E.; Angenitzki, M.; Sperling, R.; Sperling, J. Magnesium cations are required for the association of U small nuclear ribonucleoproteins and SR proteins with pre-mRNA in 200S large nuclear ribonucleoprotein particles. J. Mol. Biol. 1995, 246, 254-263.
15. Azubel, M.; Habib, N.; Sperling, J.; Sperling, R. Native spliceosomes assemble with pre-mRNA to form supraspliceosomes. J. Mol. Biol. 2006, 356, 955-966.
16. Yitzhaki, S.; Miriami, E.; Sperling, J.; Sperling, R. Phosphorylated Ser/Arg-rich proteins: Limiting factors in the assembly of 200S large nuclear ribonucleoprotein particles. Proc. Natl. Acad. Sci. USA 1996, 93, 8830-8835.
17. Heinrich, B.; Zhang, Z.; Raitskin, O.; Hiller, M.; Benderska, N.; Hartmann, A.M.; Bracco, L.; Elliott, D.; Ben-Ari, S.; Soreq, H.; et al. Heterogeneous nuclear ribonucleoprotein G regulates splice site selection by binding to CC(A/C)-rich regions in pre-mRNA. J. Biol. Chem. 2009, 284, 14303-14315.
18. Markus, M.A.; Heinrich, B.; Raitskin, O.; Adams, D.J.; Mangs, H.; Goy, C.; Ladomery, M.; Sperling, R.; Stamm, S.; Morris, B.J. WT1 interacts with the splicing protein RBM4 and regulates its ability to modulate alternative splicing in vivo. Exp. Cell Res. 2006, 312, 3379-3388.
19. Yang, Y.-H.J.; Markus, A.M.; Mangs, H.A.; Raitskin, O.; Sperling, R.; Morris, B.J. ZRANB2 localizes to supraspliceosomes and influences the alternative splicing of multiple genes in the transcriptome. Mol. Biol. Rep. 2013, 40, 5381-5395.
20. Raitskin, O.; Angenitzki, M.; Sperling, J.; Sperling, R. Large nuclear RNP particles-The nuclear pre-mRNA processing machine. J. Struct. Biol. 2002, 140, 123-130.
21. Raitskin, O.; Cho, D.S.; Sperling, J.; Nishikura, K.; Sperling, R. RNA editing activity is associated with splicing factors in lnRNP particles: The nuclear pre-mRNA processing machinery. Proc. Natl. Acad. Sci. USA 2001, 98, 6571-6576.
22. Sperling, R.; Koster, A.J.; Melamed-Bessudo, C.; Rubinstein, A.; Angenitzki, M.; Berkovitch-Yellin, Z.; Sperling, J. Three-dimensional image reconstruction of large nuclear RNP (lnRNP) particles by automated electron tomography. J. Mol. Biol. 1997, 267, 570-583.
23. Medalia, O.; Typke, D.; Hegerl, R.; Angenitzki, M.; Sperling, J.; Sperling, R. Cryoelectron microscopy and cryoelectron tomography of the nuclear pre-mRNA processing machine. J. Struct. Biol. 2002, 138, 74-84.
24. Müller, S.; Wolpensinger, B.; Angenitzki, M.; Engel, A.; Sperling, J.; Sperling, R. A supraspliceosome model for large nuclear ribonucleoprotein particles based on mass determinations by scanning transmission electron microscopy. J. Mol. Biol. 1998, 283, 383-394.
25. Azubel, M.; Wolf, S.G.; Sperling, J.; Sperling, R. Three-dimensional structure of the native spliceosome by cryo-electron microscopy. Mol. Cell 2004, 15, 833-839.
26. Cohen-Krausz, S.; Sperling, R.; Sperling, J. Exploring the architecture of the intact supraspliceosome using electron microscopy. J. Mol. Biol. 2007, 368, 319-327.
27. Spann, P.; Feinerman, M.; Sperling, J.; Sperling, R. Isolation and visualization of large compact ribonucleoprotein particles of specific nuclear RNAs. Proc. Natl. Acad. Sci. USA 1989, 86, 466-470.
28. Nilsen, T.W. RNA Structure and Function; Simons, R.W., Grunberg-Manago, M., Eds.; Cold Spring Harbor Laboratory Press: New York, NY, USA, 1998; pp. 279-307.
29. Hogg, J.R.; Collins, K. RNA-based affinity purification reveals 7SK RNPs with distinct composition and regulation. RNA 2007, 13, 868-880.
30. Carey, J.; Uhlenbeck, O.C. Kinetic and thermodynamic characterization of the R17 coat protein-ribonucleic acid interaction. Biochemistry 1983, 22, 2610-2615.
31. Lim, F.; Downey, T.P.; Peabody, D.S. Translational repression and specific RNA binding by the coat protein of the Pseudomonas phage PP7. J. Biol. Chem. 2001, 276, 22507-22513.
32. Sebbag-Sznajder, N.; Raitskin, O.; Angenitzki, M.; Sato, T.A.; Sperling, J.; Sperling, R. Regulation of alternative splicing within the supraspliceosome. J. Struct. Biol. 2012, 177, 152-159.
33. Baserga, S.J.; Steitz, J.A. The RNA World; Gesteland, R.F., Atkins, J.F., Eds.; Cold Spring Harbor Laboratory Press: New York, NY, USA, 2001; pp. 359-381.
34. Stevens, S.W.; Ryan, D.E.; Ge, H.Y.; Moore, R.E.; Young, M.K.; Lee, T.D.; Abelson, J. Composition and functional characterization of the yeast spliceosomal penta-snRNP. Mol. Cell 2002, 9, 31-44.
35. Iborra, F.J.; Jackson, D.A.; Cook, P.R. The path of transcripts from extra-nucleolar synthetic sites to nuclear pores: Transcripts in transit are concentrated in discrete structures containing SR proteins. J. Cell Sci. 1998, 111, 2269-2282.
36. Schmidt, C.; Gronborg, M.; Deckert, J.; Bessonov, S.; Conrad, T.; Luhrmann, R.; Urlaub, H. Mass spectrometry-based relative quantification of proteins in precatalytic and catalytically active spliceosomes by metabolic labeling (SILAC), chemical labeling (iTRAQ), and label-free spectral count. RNA 2014, 20, 406-420.
37. Nilsen, T.W. The spliceosome: No assembly required? Mol. Cell 2002, 9, 8-9.
38. Deckert, J.; Hartmuth, M.; Boehringer, D.; Behzadnia, N.; Will, C.L.; Kastner, B.; Stark, H.; Urlaub, H.; Luhrmann, R. Protein composition and electron microscopy structure of affinity-purified human spliceosomal B complexes isolated under physiological conditions. Mol. Cell. Biol. 2006, 26, 5528-5543.
39. Boehringer, D.; Makarov, E.M.; Sander, B.; Makarova, O.V.; Kastner, B.; Luhrmann, R.; Stark, H. Three-dimensional structure of a pre-catalytic human spliceosomal complex B. Nat. Struct. Mol. Biol. 2004, 11, 463-468.
40. Rino, J.; Carmo-Fonseca, M. The spliceosome: A self-organized macromolecular machine in the nucleus? Trends Cell Biol. 2009, 19, 375-384.
41. Will, C.L.; Behrens, S.E.; Lührmann, R. Protein composition of mammalian spliceosomal snRNPs. Mol. Biol. Rep. 1993, 18, 121-126.
42. Wahl, M.C.; Will, C.L.; Lührmann, R. The spliceosome: Design principles of a dynamic RNP machine. Cell 2009, 136, 701-718.
43. Chiu, Y.F.; Liu, Y.C.; Chiang, T.W.; Yeh, T.C.; Tseng, C.K.; Wu, N.Y.; Cheng, S.C. Cwc25 is a novel splicing factor required after Prp2 and Yju2 to facilitate the first catalytic reaction. Mol. Cell. Biol. 2009, 29, 5671-5678.
44. Liu, Y.C.; Chen, H.C.; Wu, N.Y.; Cheng, S.C. A novel splicing factor, Yju2, is associated with NTC and acts after Prp2 in promoting the first catalytic reaction of pre-mRNA splicing. Mol. Cell. Biol. 2007, 27, 5403-5413.
45. Warkocki, Z.; Odenwalder, P.; Schmitzova, J.; Platzmann, F.; Stark, H.; Urlaub, H.; Ficner, R.; Fabrizio, P.; Luhrmann, R. Reconstitution of both steps of Saccharomyces cerevisiae splicing with purified spliceosomal components. Nat. Struct. Mol. Biol. 2009, 16, 1237-1243.
46. Villa, T.; Guthrie, C. The Isy1p component of the NineTeen complex interacts with the ATPase Prp16p to regulate the fidelity of pre-mRNA splicing. Genes Dev. 2005, 19, 1894-1904.
47. Fabrizio, P.; Dannenberg, J.; Dube, P.; Kastner, B.; Stark, H.; Urlaub, H.; Luhrmann, R. The evolutionarily conserved core design of the catalytic activation step of the yeast spliceosome. Mol. Cell 2009, 36, 593-608.
48. Kolev, N.G.; Yario, T.A.; Benson, E.; Steitz, J.A. Conserved motifs in both CPSF73 and CPSF100 are required to assemble the active endonuclease for histone mRNA 3' end maturation. EMBO Rep. 2008, 9, 1013-1018.
49. Mandel, C.R.; Kaneko, S.; Zhang, H.; Gebauer, D.; Vethantham, V.; Manley, J.L.; Tong, L. Polyadenylation factor CPSF-73 is the pre-mRNA 3' end-processing endonuclease. Nature 2006, 444, 953-956.
50. Mandel, C.R.; Bai, Y.; Tong, L. Protein factors in pre-mRNA 3' end processing. Cell. Mol. Life Sci. 2008, 65, 1099-1122.
51. Agranat, L.; Raitskin, O.; Sperling, J.; Sperling, R. The editing enzyme ADAR1 and the mRNA surveillance protein hUpf1 interact in the cell nucleus. Proc. Natl. Acad. Sci. USA 2008, 105, 5028-5033.
52. Taniguchi, I.; Ohno, M. ATP-dependent recruitment of export factor Aly/REF onto intronless mRNAs by RNA helicase UAP56. Mol. Cell. Biol. 2008, 28, 601-608.
53. Sperling, R.; Sperling, J. RNP Particles, Splicing and Autoimmune Diseases; Schenkel, J., Ed.; Springer: Heidelberg, Germany, 1998; pp. 29-47.
54. Lerner, E.A.; Lerner, M.R.; Janeway, L.A.; Steitz, J.A. Monoclonal antibodies to nucleic acid containing cellular constituents: Probes for molecular biology and autoimmune disease. Proc. Natl. Acad. Sci. USA 1981, 78, 2737-2741.
55. Shevchenko, A.; Wilm, M.; Vorm, O.; Mann, M. Mass spectrometric sequencing of proteins from silver stained polyacrylamide gels. Anal. Chem. 1996, 68, 850-858.
56. Rappsilber, J.; Ishihama, Y.; Mann, M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal. Chem. 2003, 75, 663-670.
57. Ishihama, Y.; Rappsilber, J.; Andersen, J.S.; Mann, M. Microcolumns with self-assembled particle frits for proteomics. J. Chromatogr. A 2002, 979, 233-239.
58. Uniprot. Available online: http://www.uniprot.org/ (accessed on 9 January 2013).