Improved identification of enriched peptide-RNA cross-links from ribonucleoprotein particles (RNPs) by mass spectrometry

Nucleic Acids Research

Volumn 35, Issue 15, 2007, Pages

  Kühn Hölsken, Eva ^a   Dybkov, Olexandr ^a   Sander, Björn ^a   Lührmann, Reinhard ^a   Urlaub, Henning ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; PROTEIN P14; RIBONUCLEOPROTEIN; RNA; PEPTIDE; SMALL NUCLEAR RIBONUCLEOPROTEIN; SMALL NUCLEAR RNA;

ARTICLE; BINDING SITE; CONTROLLED STUDY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NUCLEIC ACID ANALYSIS; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN RNA BINDING; ULTRAVIOLET IRRADIATION; AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; BIOLOGY; CHEMISTRY; ISOLATION AND PURIFICATION; LIQUID CHROMATOGRAPHY; METHODOLOGY; MOLECULAR GENETICS; RADIATION EXPOSURE; ULTRAVIOLET RADIATION; VALIDATION STUDY;

ALKALINE PHOSPHATASE; AMINO ACID SEQUENCE; BINDING SITES; CHROMATOGRAPHY, AFFINITY; CHROMATOGRAPHY, LIQUID; COMPUTATIONAL BIOLOGY; MOLECULAR SEQUENCE DATA; PEPTIDES; RIBONUCLEOPROTEIN, U1 SMALL NUCLEAR; RIBONUCLEOPROTEIN, U2 SMALL NUCLEAR; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA, SMALL NUCLEAR; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; ULTRAVIOLET RAYS;

EID: 34548650202     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm540     Document Type: Article

References (47)

1. Zhang,B., Pan,X., Cobb,G.P. and Anderson,T.A. (2007) microRNAs as oncogenes and tumor suppressors. Dev. Biol., 302, 1-12.
2. Blencowe,B.J. (2006) Alternative splicing: New insights from global analyses. Cell, 126, 37-47.
3. Jones-Rhoades,M.W., Bartel,D.P. and Bartel,B. (2006) MicroRNAs and their regulatory roles in plants. Annu. Rev. Plant Biol., 57, 19-53.
4. Kloosterman,W.P. and Plasterk,R.H. (2006) The diverse functions of microRNAs in animal development and disease. Dev. Cell, 11, 441-450.
5. Mallory,A.C. and Vaucheret,H. (2006) Functions of microRNAs and related small RNAs in plants. Nat. Genet., 38, S31-S36 Erratum in: Nat. Genet., 38, 850.
6. Karas,M. and Hillenkamp,F. (1988) Laser desorption ionization of proteins with molecular masses exceeding 10,000 daltons. Anal. Chem. 60, 2299-2301.
7. Fenn,J.B., Mann,M., Meng,C.K., Wong,S.F. and Whitehouse,C.M. (1989) Electrospray ionisation for mass spectrometry of large biomolecules. Science, 246, 64-71.
8. Garcia-Blanco,M.A. (2006) Alternative splicing: Therapeutic target and tool. Prog. Mol. Subcell. Biol., 44, 47-64.
9. Horiuchi,T. and Aigaki,T. (2006) Alternative trans-splicing: A novel mode of pre-mRNA processing. Biol. Cell, 98, 135-140.
10. Hui,J. and Bindereif,A. (2005) Alternative pre-mRNA splicing in the human system: Unexpected role of repetitive sequences as regulatory elements. Biol. Chem., 386, 1265-1271.
11. Nilsen,T.W. (2007) Mechanisms of microRNA-mediated gene regulation in animal cells. Trends Genet., 23, 243-249.
12. Scherr,M. and Eder,M. (2007) Gene silencing by small regulatory RNAs in mammalian cells. Cell Cycle, 6, 444-449.
13. Filipowicz,W., Jaskiewicz,L., Kolb,F.A. and Pillai,R.S. (2005) Post-transcriptional gene silencing by siRNAs and miRNAs. Curr. Opin. Struct. Biol., 15, 331-341.
14. Tang,G. (2005) siRNA and miRNA: An insight into RISCs. Trends Biochem. Sci., 30, 106-114.
15. Kühn-Hölsken,E., Lenz,C., Sander,B., Lührmann,R. and Urlaub,H. (2005) Complete MALDI-ToF MS analysis of cross-linked peptide-RNA oligonucleotides derived from non-labelled UV-irradiated ribonucleoprotein particles. RNA, 11, 1915-1930.
16. Hernandez,H. and Robinson,C.V. (2007) Determining the stoichiometry and interactions of macromolecular assemblies from mass spectrometry. Nat. Protoc., 2, 715-726.
17. Sharon,M. and Robinson,C.V. (2007) The role of mass spectrometry in structure elucidation of dynamic protein complexes. Annu. Rev. Biochem., 76, 8.1-8.27.
18. Görner,H. (1994) Photochemistry of DNA and related biomolecules: quantum yields and consequences of photoionization. J. Photochem. Photobiol. B, 26, 117-139.
19. Konarska,M.M. (1999) Site-specific derivatization of RNA with photocrosslinkable groups. Methods, 18, 22-28.
20. Rhode,B.M., Hartmuth,K., Urlaub,H. and Lührmann,R. (2003) Analysis of site-specific protein-RNA cross-links in isolated RNP complexes, combining affinity selection and mass spectrometry. RNA, 9, 1542-1551.
21. Zhang,Q., Yu,E.T., Kellersberger,K.A., Crosland,E. and Fabris,D. (2006) Toward building a database of bifunctional probes for the MS3D investigation of nucleic acids structures. J. Am. Soc. Mass Spectrom. 17, 1570-1581.
22. Yu,E.T., Zhang,Q. and Fabris,D. (2005) Untying the FIV frameshifting pseudoknot structure by MS3D. J. Mol. Biol., 345, 69-80.
23. Urlaub,H., Raker,V.A., Kostka,S. and Lührmann,R. (2001) Sm protein-Sm site RNA interactions within the inner ring of the spliceosomal snRNP core structure. EMBO J., 20, 187-196.
24. Liu,S., Li,P., Dybkov,O., Nottrott,S., Hartmuth,K., Lührmann,R., Carlomagno,T. and Wahl,M.C. (2007) Binding of the human Prp31 Nop domain to a composite RNA-protein platform in U4 snRNP. Science, 316 115-120.
25. Nottrott,S., Urlaub,H. and Lührmann,R. (2002) Hierarchical, clustered protein interactions with U4/U6 snRNA: A biochemical role for U4/U6 proteins. EMBO J., 21, 5527-5538.
26. Will,C.L. and Lührmann,R. (2005) Splicing of a rare class of introns by the U12-dependent spliceosome. Biol. Chem., 386, 713-724.
27. Kastner,B. and Lührmann,R. (1999) Purification of U small nuclear ribonucleoprotein particles. In Haynes,S.R. (ed.), RNA-Protein Interaction Protocols, Methods in Molecular Biology, Vol. 118, Humana Press, Totowa, NY, pp. 289-298.
28. Will,C.L. and Lührmann,R. (2006) Spliceosome structure and function. In Gesteland,R.F., Gesteland,T.R., and Atkins,J.F. (eds), The RNA World III, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 369-400.
29. Urlaub,H., Hartmuth,K., Kostka,S., Grelle,G. and Lührmann,R. (2000) A general approach for identification of RNA-protein cross-linking sites within native human spliceosomal small nuclear ribonucleoproteins (snRNPs). Analysis of RNA-protein contacts in native U1 and U4/U6.U5 snRNPs. J. Biol. Chem., 275, 41458-41468.
30. Lenz,C., Kühn-Hölsken,E. and Urlaub,H. (2007) Detection of protein-RNA cross-links by nanoLC-ESI-MS/MS using precursor ion scanning and multiple reaction monitoring (MRM) experiments. J. Am. Soc. Mass Spectrom., 18, 869-881.
31. Spadaccini,R., Reidt,U., Dybkov,O., Will,C.L., Frank,R., Stier,G., Corsini,L., Wahl,M.C., Lührmann,R. and Sattler,M. (2006) Biochemical and NMR analyses of an SF3b155-p14-U2AF-RNA interaction network involved in branch point definition during pre-mRNA splicing. RNA, 12 410-425.
32. Stensballe,A., Andersen,S. and Jensen,O.N. (2001) Characterization of phosphoproteins from electrophoretic gels by nanoscale Fe(III) affinity chromatography with off-line mass spectrometry analysis. Proteomics 1, 207-222.
33. 3+) affinity chromatography. Anal. Biochem. 154, 250-254.
34. Li,S. and Dass,C. (1999) Iron(III)-immobilized metal ion affinity chromatography and mass spectrometry for the purification and characterization of synthetic phosphopeptides. Anal. Biochem., 270, 9-14.
35. Steen,H., Petersen,J., Mann,M. and Jensen,O.N. (2001) Mass spectrometry analysis of a UV-cross-linked protein-DNA complex: Tryptophans 54 and 88 of E. coli SSB cross-link to DNA. Protein Sci., 10, 1989-2001.
36. Pingoud,V., Geyer,H., Geyer,R., Kubareva,E., Bujnicki,J.M. and Pingoud,A. (2005) Identification of base-specific contacts in protein-DNA complexes by photocrosslinking and mass spectrometry: A case study using the restriction endonuclease SsoII. Mol. Biosyst., 1, 135-141.
37. Geyer,H., Geyer,R. and Pingoud,V. (2004) A novel strategy for the identification of protein-DNA contacts by photocrosslinking and mass spectrometry. Nucleic Acids Res., 32, e132.
38. Query,C.C., Strobel,S.A. and Sharp,P.A. (1996) Three recognition events at the branch-site adenine. EMBO J., 15, 1392-1402.
39. Schellenberg,M.J., Edwards,R.A., Ritchie,D.B., Kent,O.A., Golas,M.M., Stark,H., Lührmann,R., Glover,J.N. and MacMillan,A.M. (2006) Crystal structure of a core spliceosomal protein interface. Proc. Natl Acad. Sci. USA, 103, 1266-1271.
40. Gozani,O., Potashkin,J. and Reed,R. (1998) A potential role for U2AF-SAP 155 interactions in recruiting U2 snRNP to the branch site. Mol. Cell. Biol., 18, 4752-4760.
41. Query,C.C., McCaw,P.S. and Sharp,P.A. (1997) A minimal spliceosomal complex A recognizes the branch site and polypyrimidine tract. Mol. Cell. Biol., 17, 2944-2953.
42. Will,C.L., Schneider,C., MacMillan,A.M., Katopodis,N.F., Neubauer,G., Wilm,M., Lührmann,R. and Query,C.C. (2001) A novel U2 and U11/U12 snRNP protein that associates with the pre-mRNA branch site. EMBO J. 20, 4536-4546.
43. Dybkov,O., Will,C.L., Deckert,J., Behzadnia,N., Hartmuth,K. and Lührmann,R. (2006) U2 snRNA-protein contacts in purified human 17S U2 snRNPs and in spliceosomal A and B complexes. Mol. Cell. Biol., 26, 2803-2816.
44. Urlaub,H., Kruft,V., Bischof,O., Müller,E.C. and Wittmann-Liebold,B. (1995) Protein-rRNA binding features and their structural and functional implications in ribosomes as determined by cross-linking studies. EMBO J., 14, 4578-4588.
45. Janek,K., Wenschuh,H., Bienert,M. and Krause,E. (2001) Phosphopeptide analysis by positive and negative ion matrix-assisted laser desorption/ ionization mass spectrometry. Rapid Commun. Mass Spectrom., 15 1593-1599.
46. Deckert,J., Hartmuth,K., Boehringer,D., Behzadnia,N., Will,C.L., Kastner,B., Stark,H., Urlaub,H. and Lührmann,R. (2006) Protein composition and electron microscopy structure of affinity-purified human spliceosomal B complexes isolated under physiological conditions. Mol. Cell. Biol., 26, 5528-5543.
47. Jurica,M.S., Sousa,D., Moore,M.J. and Grigorieff,N. (2004) Three-dimensional structure of C complex spliceosomes by electron microscopy. Nat. Struct. Mol. Biol., 11, 265-269.