Selective ribosome profiling as a tool for studying the interaction of chaperones and targeting factors with nascent polypeptide chains and ribosomes

Nature Protocols

Volumn 8, Issue 11, 2013, Pages 2212-2239

  Becker, Annemarie H ^a   Oh, Eugene ^b,c,d   Weissman, Jonathan S ^b,c   Kramer, Günter ^a   Bukau, Bernd ^a  

^a GERMAN CANCER RESEARCH CENTER   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; MEMBRANE PROTEIN; MESSENGER RNA; NUCLEASE; POLYPEPTIDE; RIBOSOME NASCENT CHAIN COMPLEX; TARGETING FACTOR; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ARTICLE; BACTERIUM; CHEMICAL INTERACTION; CONTROLLED STUDY; CROSS LINKING; DNA LIBRARY; NONHUMAN; PRIORITY JOURNAL; RIBOSOME; RNA SEQUENCE; SELECTIVE RIBOSOME PROFILING;

BACTERIA; BACTERIAL PROTEINS; GENE LIBRARY; MOLECULAR CHAPERONES; PROTEIN INTERACTION MAPS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RIBOSOMES;

EID: 84887009051     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2013.133     Document Type: Article

References (42)

1. Pechmann, S., Willmund, F. & Frydman, J. The ribosome as a hub for protein quality control. Mol. Cell 49, 411-421 (2013).
2. Kramer, G., Boehringer, D., Ban, N. & Bukau, B. The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 16, 589-597 (2009).
3. Giglione, C., Boularot, A. & Meinnel, T. Protein N-terminal methionine excision. Cell Mol. Life Sci. 61, 1455-1474 (2004). (Pubitemid 38858352)
4. Starheim, K.K., Gevaert, K. & Arnesen, T. Protein N-terminal acetyltransferases: when the start matters. Trends Biochem. Sci. 37, 152-161 (2012).
5. Jones, J.D. & O?Connor, C.D. Protein acetylation in prokaryotes. Proteomics 11, 3012-3022 (2011).
6. Hartl, F.U. & Hayer-Hartl, M. Converging concepts of protein folding in vitro and in vivo. Nat. Struct. Mol. Biol. 16, 574-581 (2009).
7. Hartl, F.U., Bracher, A. & Hayer-Hartl, M. Molecular chaperones in protein folding and proteostasis. Nature 475, 324-332 (2011).
8. Preissler, S. & Deuerling, E. Ribosome-associated chaperones as key players in proteostasis. Trends Biochem. Sci. 37, 274-283 (2012).
9. Egea, P.F., Stroud, R.M. & Walter, P. Targeting proteins to membranes: structure of the signal recognition particle. Curr. Opin. Struct. Biol. 15, 213-220 (2005).
10. Ingolia, N.T., Brar, G.A., Rouskin, S., McGeachy, A.M. & Weissman, J.S. The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments. Nat. Protoc. 7, 1534-1550 (2012).
11. Oh, E. et al. Selective ribosome profiling reveals the cotranslational chaperone action of trigger factor in vivo. Cell 147, 1295-1308 (2011).
12. Ingolia, N.T., Ghaemmaghami, S., Newman, J.R. & Weissman, J.S. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324, 218-223 (2009).
13. Brar, G.A. et al. High-resolution view of the yeast meiotic program revealed by ribosome profiling. Science 335, 552-557 (2012).
14. Ingolia, N.T., Lareau, L.F. & Weissman, J.S. Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147, 789-802 (2011).
15. Li, G.W., Oh, E. & Weissman, J.S. The anti-Shine-Dalgarno sequence drives translational pausing and codon choice in bacteria. Nature 484, 538-541 (2012).
16. Han, Y. et al. Monitoring cotranslational protein folding in mammalian cells at codon resolution. Proc. Natl. Acad. Sci. USA 109, 12467-12472 (2012).
17. Patzelt, H. et al. Three-state equilibrium of Escherichia coli trigger factor. Biol. Chem. 383, 1611-1619 (2002). (Pubitemid 35282981)
18. Kramer, G. et al. L23 protein functions as a chaperone docking site on the ribosome. Nature 419, 171-174 (2002). (Pubitemid 35025445)
19. Mitkevich, V.A. et al. Thermodynamic characterization of ppGpp binding to EF-G or IF2 and of initiator tRNA binding to free IF2 in the presence of GDP, GTP, or ppGpp. J. Mol. Biol. 402, 838-846 (2010).
20. Nakatogawa, H. & Ito, K. The ribosomal exit tunnel functions as a discriminating gate. Cell 108, 629-636 (2002). (Pubitemid 34241424)
21. Gong, F. & Yanofsky, C. Instruction of translating ribosome by nascent peptide. Science 297, 1864-1867 (2002). (Pubitemid 35024344)
22. Wilson, D.N. On the specificity of antibiotics targeting the large ribosomal subunit. Ann. NY Acad. Sci. 1241, 1-16 (2011).
23. Kerner, M.J. et al. Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122, 209-220 (2005). (Pubitemid 41032985)
24. Calloni, G. et al. DnaK functions as a central hub in the E. coli chaperone network. Cell Rep. 1, 251-264 (2012).
25. Datta, A.K. & Burma, D.P. Association of ribonuclease I with ribosomes and their subunits. J. Biol. Chem. 247, 6795-6801 (1972).
26. Dingwall, C., Lomonossoff, G.P. & Laskey, R.A. High sequence specificity of micrococcal nuclease. Nucleic Acids Res. 9, 2659-2673 (1981).
27. Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 10-12 (2011).
28. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
29. Langmead, B. & Salzberg, S.L. Fast gapped-read alignment with Bowtie Nat. Methods 9, 357-359 (2012).
30. Merz, F. et al. Molecular mechanism and structure of Trigger Factor bound to the translating ribosome. EMBO J. 27, 1622-1632 (2008). (Pubitemid 351794035)
31. Buskiewicz, I. et al. Trigger factor binds to ribosome-signal-recognition particle (SRP) complexes and is excluded by binding of the SRP receptor. Proc. Natl. Acad. Sci. USA 101, 7902-7906 (2004). (Pubitemid 38698026)
32. Raine, A., Lovmar, M., Wikberg, J. & Ehrenberg, M. Trigger factor binding to ribosomes with nascent peptide chains of varying lengths and sequences. J. Biol. Chem. 281, 28033-28038 (2006). (Pubitemid 44414516)
33. Bornemann, T., Jockel, J., Rodnina, M.V. & Wintermeyer, W. Signal sequence-independent membrane targeting of ribosomes containing short nascent peptides within the exit tunnel. Nat. Struct. Mol. Biol. 15, 494-499 (2008). (Pubitemid 351653581)
34. Vorderwulbecke, S. et al. Low temperature or GroEL/ES overproduction permits growth of Escherichia coli cells lacking trigger factor and DnaK. FEBS Lett. 559, 181-187 (2004). (Pubitemid 38186725)
35. Martinez-Hackert, E. & Hendrickson, W.A. Promiscuous substrate recognition in folding and assembly activities of the trigger factor chaperone. Cell 138, 923-934 (2009).
36. Deuerling, E., Schulze-Specking, A., Tomoyasu, T., Mogk, A. & Bukau, B. Trigger factor and DnaK cooperate in folding of newly synthesized proteins. Nature 400, 693-696 (1999).
37. Deuerling, E. et al. Trigger Factor and DnaK possess overlapping substrate pools and binding specificities. Mol. Microbiol. 47, 1317-1328 (2003). (Pubitemid 36307854)
38. del Alamo, M. et al. Defining the specificity of cotranslationally acting chaperones by systematic analysis of mRNAs associated with ribosome-nascent chain complexes. PLoS Biol. 9, e1001100 (2011).
39. Willmund, F. et al. The cotranslational function of ribosome-associated Hsp70 in eukaryotic protein homeostasis. Cell 152, 196-209 (2013).
40. Guo, H., Ingolia, N.T., Weissman, J.S. & Bartel, D.P. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466, 835-840 (2010).
41. Homann, O.R. & Johnson, A.D. MochiView: versatile software for genome browsing and DNA motif analysis. BMC Biol. 8, 49 (2010).
42. van den Berg, S., Lofdahl, P.A., Hard, T. & Berglund, H. Improved solubility of TEV protease by directed evolution. J. Biotechnol. 121, 291-298 (2006). (Pubitemid 43113101)