Rna chaperones buffer deleterious mutations in E. Coli

eLife

Volumn 2015, Issue 4, 2015, Pages

  Rudan, Marina ^a   Schneider, Dominique ^b,c   Warnecke, Tobias ^d   Krisko, Anita ^a  

^a Mediterranean Institute for Life Sciences   (Croatia)

^b UNIV GRENOBLE ALPES   (France)

^c CNRS   (France)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; COLD SHOCK PROTEIN; DEAD BOX PROTEIN; LYSINE; MUTANT PROTEIN; RNA CHAPERONE; RNA HELICASE; UNCLASSIFIED DRUG; BACTERIAL RNA; ESCHERICHIA COLI PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL STRAIN; DBRH GENE; DELETERIOUS MUTATION; ESCHERICHIA COLI; GENE; GENE OVEREXPRESSION; GENE SEQUENCE; GENETIC VARIABILITY; GENOTYPE; MUTATION; NONHUMAN; PLASMID; POINT MUTATION; PROTEIN FOLDING; RNA FOLDING; RNA STRUCTURE; WESTERN BLOTTING; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; REPRODUCTIVE FITNESS;

DEAD-BOX RNA HELICASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENETIC FITNESS; MOLECULAR CHAPERONES; MUTATION; RNA, BACTERIAL;

EID: 85003055733     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.04745     Document Type: Article

References (40)

1. Rutherford, S. L. & Lindquist, S. Hsp90 as a capacitor for morphological evolution. Nature 396, 336–342 (1998).
2. Queitsch, C., Sangster, T. A. & Lindquist, S. Hsp90 as a capacitor of phenotypic variation. Nature 417, 618–624 (2002).
3. Rohner, N. et al. Cryptic variation in morphological evolution: HSP90 as a capacitor for loss of eyes in cavefish. Science 342, 1372–1375 (2013).
4. Tokuriki, N. & Tawfik, D. S. Chaperonin overexpression promotes genetic variation and enzyme evolution. Nature 459, 668–673 (2009).
5. Williams, T. A. & Fares, M. A. The Effect of Chaperonin Buffering on Protein Evolution. Genome Biol Evol 2, 609–619 (2010).
6. Bogumil, D. & Dagan, T. Chaperonin-Dependent Accelerated Substitution Rates in Prokaryotes. Genome Biol Evol 2, 602–608 (2010).
7. Warnecke, T. & Hurst, L. D. GroEL dependency affects codon usage—support for a critical role of misfolding in gene evolution. Mol. Syst. Biol. 6, 340 (2010).
8. Burga, A., Casanueva, M. O. & Lehner, B. Predicting mutation outcome from early stochastic variation in genetic interaction partners. Nature 480, 250–253 (2011).
9. Fares, M. A., Ruiz-González, M. X., Moya, A., Elena, S. F. & Barrio, E. Endosymbiotic bacteria: groEL buffers against deleterious mutations. Nature 417, 398–398 (2002).
10. Herschlag, D. RNA chaperones and the RNA folding problem. The Journal of 405 Biological Chemistry 270, 20871–20874 (1995).
11. Downs, W. D. & Cech, T. R. Kinetic pathway for folding of the Tetrahymena ribozyme revealed by three UV-inducible crosslinks. RNA 2, 718–732 (1996).
12. Bhaskaran, H. & Russell, R. Kinetic redistribution of native and misfolded RNAs by a DEAD-box chaperone. Nature 449, 1014–1018 (2007).
13. Mohr, S., Stryker, J. M. & Lambowitz, A. M. A DEAD-Box Protein Functions as an ATP-Dependent RNA Chaperone in Group I Intron Splicing. Cell 109, 769–779 (2002).
14. Russell, R. RNA misfolding and the action of chaperones. Front Biosci 13, 1–20 (2008).
15. Pan, C. & Russell, R. Roles of DEAD-box proteins in RNA and RNP Folding. rnabiology 7, 667–676 (2010).
16. Py, B., Higgins, C. F., Krisch, H. M. & Carpousis, A. J. A DEAD-box RNA 418 helicase in the Escherichia coli RNA degradosome. Nature 381, 169–172 (1996).
17. Lenski, R. E. Quantifying fitness and gene stability in microorganisms. Biotechnology 15, 173–192 (1991).
18. Sniegowski, P. D., Gerrish, P. J. & Lenski, R. E. Evolution of high mutation rates in experimental populations of E. coli. Nature 387, 703–705 (1997).
19. Hartl, F. U., Bracher, A. & Hayer-Hartl, M. Molecular chaperones in protein folding and proteostasis. Nature 475, 324–332 (2011).
20. Jarmoskaite, I., Bhaskaran, H., Seifert, S. & Russell, R. DEAD-box protein427 CYT-19 is activated by exposed helices in a group I intron RNA. Proceedings 428 of the National Academy of Sciences 111, E2928–36 (2014).
21. Death, A., Notley, L. & Ferenci, T. Derepression of LamB protein facilitates outer membrane permeation of carbohydrates into Escherichia coli under conditions of nutrient stress. Journal of Bacteriology 175, 1475–1483 (1993).
22. Lind, P. A., Berg, O. G. & Andersson, D. I. Mutational robustness of ribosomal protein genes. Science 330, 825–827 (2010).
23. Jiang, W., Hou, Y. & inouye, M. CspA, the Major Cold-shock Protein of Escherichia coli, Is an RNA Chaperone. The Journal of Biological Chemistry 272, 196–202 (1997).
24. Hilier, B. J., Rodriguez, H. M. & Gregoret, L. M. Coupling proein stability and protein function in Escherichia coli CspA. Folding & Design 3, 87–93 (1998).
25. Bae, W., Jones, P. G. & Inouye, M. CspA, the major cold shock protein of Escherichia coli, negatively regulates its own gene expression. Journal of Bacteriology 179, 7081–7088 (1997).
26. Hunger, K., Beckering, C. L., Wiegeshoff, F., Graumann, P. L. & Marahiel, M. A. Cold-induced putative DEAD box RNA helicases CshA and CshB are essential for cold adaptation and interact with cold shock protein B in Bacillus subtilis. Journal of Bacteriology 188, 240–248 (2006).
27. Plotkin, J. B. & Kudla, G. Synonymous but not the same: the causes and48 consequences of codon bias. Nat. Rev. Genet. 12, 32–42 (2011).
28. Vanzo, N. F. et al. Ribonuclease E organizes the protein interactions in the 450 Escherichia coli RNA degradosome. Genes & Development 12, 2770–2781 (1998).
29. Elles, L. M. S. & Uhlenbeck, O. C. Mutation of the arginine finger in the active site of Escherichia co 453 li DbpA abolishes ATPase and helicase activity and confers a dominant slow growth phenotype. Nucleic Acids Research 36, 41–50 455 (2008).
30. Turner, A.-M. W., Love, C. F., Alexander, R. W. & Jones, P. G. Mutational 457 Analysis of the Escherichia coli DEAD Box Protein CsdA. Journal of Bacteriology 189, 2769–2776 (2007).
31. Lenski, R. E. Experimental Studies of Pleiotropy and Epistasis in Escherichia coli. I. Variation in Competitive Fitness Among Mutants Resistant to Virus T4. Evolution 42 (1988).
32. Tenaillon, O. et al. The molecular diversity of adaptive convergence. Science 463 335, 457–461 (2012).
33. Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
34. Vallenet, D. et al. MicroScope—an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data. Nucleic Acids Research gks1194 (2012). doi:10.1093/nar/gks1194
35. Barrick, J. E. et al. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461, 1243–1247 (2009).
36. Sawitzke, J. A. et al. Recombineering: highly efficient in vivo genetic engineering using single-strand oligos. Meth. Enzymol. 533, 157–177 (2013).
37. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Anal. Biochem. 72, 248–254 (1976).
38. Collins, T. J. ImageJ for microscopy. BioTechniques 43, 25–30 (2007).
39. Lorenz, R. et al. ViennaRNA Package 2.0. Algorithms Mol Biol 6, 26 (2011).
40. Khemici, V. & Carpousis, A. J. The RNA degradosome and poly(A) polymerase of Escherichia coli are required in vivo for the degradation of small mRNA decay intermediates containing REP‐stabilizers. Molecular Microbiology 51, 777–790 (2004).