Mass spectrometric analysis of the human 40S ribosomal subunit: Native and HCV IRES-bound complexes

Protein Science

Volumn 14, Issue 6, 2005, Pages 1438-1446

  Yu, Yonghao ^a,b   Ji, Hong ^a   Doudna, Jennifer A ^a   Leary, Julie A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Mass spectrometry; Protein mapping; Ribosome

Indexed keywords

INITIATION FACTOR 3; METHIONINE; NUCLEOLIN; PROTEIN SUBUNIT; RIBOSOME PROTEIN; VIRUS RNA;

ARTICLE; COMPLEX FORMATION; DISULFIDE BOND; EUKARYOTE; HEPATITIS C VIRUS; MASS SPECTROMETRY; METHODOLOGY; METHYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; RIBOSOME; TRANSLATION INITIATION;

HEPACIVIRUS; HUMANS; MASS SPECTROMETRY; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RIBOSOMES; RNA, VIRAL;

EUKARYOTA; HEPATITIS C VIRUS;

EID: 22444444478     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.041293005     Document Type: Article

References (41)

1. Angenstein, F., Evans, A.M., Settlage, R.E., Moran, S.T., Ling, S., Klintsova, A.Y., Shabanowitz, J., Hunt, D.F., and Greenough, W.T. 2002. A receptor for activated C kinase is part of messenger ribonucleoprotein complexes associated with polyA-mRNAs in neurons. J. Neurosci. 22: 8827-8837.
2. Arnold, R.J., Polevoda, B., Reilly, J.P., and Sherman, F. 1999. The action of N-terminal acetyltransferases on yeast ribosomal proteins. J. Biol. Chem. 274: 37035-37040.
3. Chantrel, Y., Gaisne, M., Lions, C., and Verdiere, J. 1998. The transcriptional regulator Hap1p (Cyp1p) is essential for anaerobic or hemedeficient growth of Saccharomyces cerevisiae: Genetic and molecular characterization of an extragenic suppressor that encodes a WD repeat protein. Genetics 148: 559-569.
4. Chong, B.E., Hamler, R.L., Lubman, D.M., Ethier, S.P., Rosenspire, A.J., and Miller, F.R. 2001. Differential screening and mass mapping of proteins from premalignant and cancer cell lines using nonporous reversed-phase HPLC coupled with mass spectrometric analysis. Anal. Chem. 73: 1219-1227.
5. Du, Y., Meng, F., Patrie, S.M., Miller, L.M., and Kelleher, N.L. 2004. Improved molecular weight-based processing of intact proteins for interrogation by quadrupole-enhanced FT MS/MS. J. Proteome Res. 3: 801-806.
6. Forbes, A.J., Patrie, S.M., Tylor, G.K., Kim, Y., Jiang, L., and Kelleher, N.L. 2004. Targeted analysis and discovery of posttranslational modifications in proteins from Methanogenic archaea by top-down MS. Proc. Natl. Acad. Sci. 101: 2678-2683.
7. Ge, Y., ElNaggar, M., Sze, S.K., Oh, H.B., Begley, T.P., McLafferty, F.W., Boshoff, H., and Barry III, C.E. 2003. Top down characterization of secreted proteins from Mycobacterium tuberculosis by electron capture dissociation mass spectrometry. J. Am. Soc. Mass Spectrom. 14: 253-261.
8. Ginistry, H., Sicard, H., and Bouvet, P. 1999. Structure and functions of nucleolin. J. Cell Sci. 112: 761-772.
9. Hanash, S.M. 2000. Biomedical applications of two-dimensional electrophoresis using immobilized pH gradients: Current status. Electrophoresis 21: 1202-1209.
10. Hardy, S.J.S., Kurland, C.G., Voynow, P., and Mora, G. 1969. Ribosomal proteins of Escherichia coli. I. Purification of the 30 S ribosomal proteins. Biochemistry 8: 2897-2905.
11. Hellen, C.T. and Sarnow, P. 2001. Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev. 15: 1593-1612.
12. Hunt, F.D., Yates III, J.R., Shabanowitz, J., Winston, S., and Hauer, C.R. 1986. Protein sequencing by tandem mass spectrometry. Proc. Natl. Acad. Sci. 83: 6233-6237.
13. Izumi, R.E., Valdez, B., Banerjee, R., Srivastava, M., and Dasgupta, A. 2001. Nucleolin stimulates viral internal ribosome entry site-mediated translation. Virus Res. 76: 17-29.
14. Ji, H., Fraser, C.S., Yu, Y., Leary, J.A., and Doudna, J.A. 2004. Coordinated assembly of human ribosomes by the hepatitis C virus IRES RNA. Proc. Natl. Acad. Sci. 101: 16990-16995.
15. Kelleher, N.L. 2004. Top-down proteomics. Anal. Chem. 76: 196A-203A.
16. Kieft, J.S., Zhou, K., Jubin, R., and Doudna, J.A. 2001. Mechanism of ribosome recruitment by hepatitis C IRES RNA. RNA 7: 194-206.
17. Lee, S., Berger, S.J., Martinovica, S., Paša-Tolicá, L., Anderson, G.A., Shen, Y., Zhao, R., and Smith, R.D. 2002. Direct mass spectrometric analysis of intact proteins of the yeast large ribosomal subunit using capillary LC/FTICR. Proc. Natl. Acad. Sci. 99: 5942-5947.
18. Lhoest, J., Lobet, Y., Costers, E., and Colson, C. 1984. Methylated proteins and amino-acids in the ribosomes of Saccharomyces-cerevisiae. Eur. J. Biochem. 141: 585-590.
19. Link, A.J., Eng, J., Schieltz, D.M., Carmack, E., Mize, G.J., Morris, D.R., Garvik, B.M., and Yates III, J.R. 1999. Direct analysis of protein complexes using mass spectrometry. Nat. Biotechnol. 17: 676-682.
20. Lopez, M.F.,Kristal,B.S.,Chernokalskaya,E.,Lazarev,A.,Shestopalov,A.I., Bogdanova, A., and Robinson, M. 2000. High-throughput profiling of the mitochondrial proteome using affinity fractionation and automation. Electrophoresis 21: 3427-3440.
21. Lu, H., Li, W., Noble, W.S., Payan, D., and Anderson, D.C. 2004. Riboproteomics of the hepatitis C virus internal ribosomal entry site. J. Proteome Res. 3: 949-957.
22. Lubman, D.M., Kachman, M.T., Wang, H., Gong, S., Yan, F., Hamler, R.L., O'Neil, K.A., Zhu, K., Buchanan, N.S., and Barder, T.J. 2002. Two-dimensional liquid separations-mass mapping of proteins from human cancer cell lysates. J. Chromatogr. B 782: 183-196.
23. MacCoss, M.J., McDonald, W.H., Saraf, A., Sadygov, R., Clark, J.M., Tasto, J.J., Gould, K.L., Wolters, D., Washburn, M., Weiss, A., et al. 2002. Shotgun identification of protein modifications from protein complexes and lens tissue. Proc. Natl. Acad. Sci. 99: 7900-7905.
24. Madison-Antenucci, S., Grams, J., and Hajduk, S.L. 2002. Editing machines: The complexities of trypanosome RNA editing. Cell 108: 435-438.
25. McCahill, A., Warwicker, J., Bolger, G.B., Houslay, M.D., and Yarwood, S.J. 2002. The RACK1 scaffold protein: A dynamic cog in cell response mechanisms. Mol. Pharmocol. 62: 1261-1273.
26. Morris-Desbois, C., Réty, S., Ferro, M., Garin, J., and Jalinot, P. 2001. The human protein HSPC021 interacts with Int-6 and is associated with eukaryotic translation initiation factor 3. J. Biol. Chem. 276: 45988-45995.
27. Odintsova, T.I., Mueller, E., Ivanov, A.V., Egorov, T.A., Bienert, R., Vladimirov, S.N., Kostka, S., Otto, A., Wittmann-Liebold, B., and Karpova, G.G. 2003. Characterization and analysis of posttranslational modifications of the human large cytoplasmic ribosomal subunit proteins by mass spectrometry and edman sequencing. J. Protein Chem. 22: 249-258.
28. Pestova, T.V., Hellen, C.U., and Shatsky, I.N. 1996. Canonical eukaryotic initiation factors determine initiation of translation by internal ribosomal entry. Mol. Cell Biol. 16: 6859-6869.
29. Pestova, T.V., Kolupaeva, V.G., Lomakin, I.B., Pilipenko, E.V., Shatsky, I.N., Agol, V.I., and Hellen, C.U.T. 2001. Molecular mechanisms of translation initiation in eukaryotes. Proc. Natl. Acad. Sci. 98: 7029-7036.
30. Phizicky, E.M. and Fields, S. 1995. Protein-protein interactions: Methods for detection and analysis. Microbiol. Rev. 59: 94-123.
31. Pugh, B.F. 1996. Mechanisms of transcription complex assembly. Curr. Opin. Cell. Biol. 8: 303-311.
32. Ranish, J.A., Yi, E.C., Leslie, D.M., Purvine, S.O., Goodlett, D.R., Eng, J., and Aebersold, R. 2003. The study of macromolecular complexes by quantitative proteomics. Nat. Genet. 33: 349-355.
33. Sengupta, J., Nilsson, J., Gursky, R., Spahn, C.M.T., Nissen, P., and Frank, J. 2004. Identification of the versatile scaffold protein RACK1 on the eukaryotic ribosome by cryo-EM. Nat. Struct. Mol. Biol. 11: 957-962.
34. Shevchenko, A., Jensen, O.N., Podtelejnikov, A.V., Sagliocco, F., Wilm, M., Vorm, O., Mortensen, P., Boucherie, H., and Mann, M. 1996. Linking genome and proteome by mass spectrometry: Large-scale identification of yeast proteins from two dimensional gels. Proc. Natl. Acad. Sci. 90: 14440-14445.
35. Shor, B., Calaycay, J., Rushbrook, J., and McLeod, M. 2003. Cpc2/RACK1 is a ribosome-associated protein that promotes efficient translation in Schizosaccharomyces pombe. J. Biol. Chem. 278: 49119-49128.
36. Sizova, D.V., Kolupaeva, V.G., Pestova, T.V., Shatsky, I.N., and Hellen, C.U.T. 1998. Specific interaction of eukaryotic translation initiation factor 3 with the 5′ nontranslated regions of hepatitis C virus and classical swine fever virus RNAs. J. Virol. 72: 4775-4782.
37. Strader, M.B., VerBerkmoes, N.C., Tabb, D.L., Connelly, H.M., Barton, J.W., Bruce, B.D., Pelletier, D.A., Davison, B.H., Hettich, R.L., Larimer, F.W., et al. 2004. Characterization of the 70S ribosome from Rhodopseudomonas palustris using an integrated "top-down" and "bottom-up" mass spectrometric approach. J. Proteome Res. 3: 965-978.
38. VerBerkmoes,N.C.,Bundy, J.L.,Hauser, L.,Asano,K.G.,Razumovskaya, J., Larimer, F., Hettich, R.L., and Stephenson Jr., J.L. 2002. Integrating "top-down" and "bottom-up" mass spectrometric approaches for proteomic analysis of Shewanella oneidensis. J. Proteome Res. 1: 239-252.
39. Waggoner, S. and Sarnow, P. 1998. Viral ribonucleoprotein complex formation and nucleolar-cytoplasmic relocalization of nucleolin in poliovirus-infected cells. J. Virol. 72: 6699-6709.
40. Will, C.L. and Luhrmann, R. 2001. Spliceosomal UsnRNP biogenesis, structure and function. Curr. Opin. Cell. Biol. 13: 290-301.
41. Zhou, Z., Licklider, L.L., Gygi, S.P., and Reed, R. 2002. Comprehensive proteomic analysis of the human spliceosome. Nature 419: 182-185.