Elongation factor P mediates a novel post-transcriptional regulatory pathway critical for bacterial virulence

Virulence

Volumn 2, Issue 2, 2011, Pages

  Betty Zou, S ^a   Roy, Hervé ^b   Ibba, Michael ^b   Navarre, William Wiley ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Antibiotic resistance; Betalysine; Elongation factor P; Lysyl tRNA synthetase; Salmonella

Indexed keywords

BACTERIAL PROTEIN; ELONGATION FACTOR; ELONGATION FACTOR P; INITIATION FACTOR 5A; PROTEIN POXA; PROTEIN YJEK; TRANSFER RNA; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL SURVIVAL; BACTERIAL VIABILITY; BACTERIAL VIRULENCE; CELL CYCLE REGULATION; EFP GENE; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; REGULATORY MECHANISM; SALMONELLA; STRESS; UPREGULATION;

BACTERIA (MICROORGANISMS); EUKARYOTA; SALMONELLA;

EID: 85011940605     PISSN: 21505594     EISSN: 21505608     Source Type: Journal    
DOI: None     Document Type: Article

References (49)

1. Sharma UK, Chatterji D. Transcriptional switching in Escherichia coli during stress and starvation by modulation of sigma activity. FEMS Microbiol Rev 2010; 34:646-57.
2. Raghavan V, Groisman EA. Orphan and hybrid twocomponent system proteins in health and disease. Curr Opin Microbiol 2010; 13:226-31.
3. Gooderham WJ, Hancock REW. Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa. FEMS Microbiol Rev 2009; 33:279-94.
4. Vogel J. A rough guide to the non-coding RNA world of Salmonella. Mol Microbiol 2009; 71:1-11.
5. Block KF, Hammond MC, Breaker RR. Evidence for widespread gene control function by the ydaO riboswitch candidate. J Bacteriol 2010; 192:3983-9.
6. Park S, Cromie MJ, Lee E, Groisman EA. A bacterial mRNA leader that employs different mechanisms to sense disparate intracellular signals. Cell 2010; 142:737-48.
7. Dalebroux ZD, Svensson SL, Gaynor EC, Swanson MS. ppGpp conjures bacterial virulence. Microbiol Mol Biol Rev 2010; 74:171-99.
8. Pesavento C, Hengge R. Bacterial nucleotide-based second messengers. Curr Opin Microbiol 2009; 12:170-6.
9. Gerdes K, Christensen SK, Løbner-Olesen A. Prokaryotic toxin-antitoxin stress response loci. Nat Rev Microbiol 2005; 3:371-82.
10. Milon P, Tischenko E, Tomšic J, Caserta E, Folkers G, La Teana A, et al. The nucleotide-binding site of bacterial translation initiation factor 2 (IF2) as a metabolic sensor. Proc Nat Acad Sci USA 2006; 103:13962-7.
11. Giuliodori AM, Brandi A, Giangrossi M, Gualerzi CO, Pon CL. Cold-stress-induced de novo expression of infC and role of IF3 in cold-shock translational bias. RNA 2007; 13:1355-65.
12. Spriggs KA, Bushell M, Willis AE. Translational regulation of gene expression during conditions of cell stress. Mol Cell 2010; 40:228-37.
13. Navarre WW, Zou SB, Roy H, Xie JL, Savchenko A, Singer A, et al. PoxA, YjeK and elongation factor P coordinately modulate virulence and drug resistance in Salmonella enterica. Mol Cell 2010; 39:209-21.
14. Yanagisawa T, Sumida T, Ishii R, Takemoto C, Yokoyama S. A paralog of lysyl-tRNA synthetase aminoacylates a conserved lysine residue in translation elongation factor P. Nat Struct Mol Biol 2010; 17:1136-43.
15. Kaniga K, Compton M, Curtiss R, Sundaram P. Molecular and functional characterization of Salmonella enterica serovar typhimurium poxA gene: effect on attenuation of virulence and protection. Infect Immun 1998; 66:5599-606.
16. Chang Y, Cronan J. Mapping nonselectable genes of Escherichia coli by using transposon Tn10: location of a gene affecting pyruvate oxidase. J Bacteriol 1982; 151:1279-89.
17. Chang Y, Cronan J. Genetic and biochemical analyses of Escherichia coli strains having a mutation in the structural gene (poxB) for pyruvate oxidase. J Bacteriol 1983; 154:756-62.
18. Behshad E, Ruzicka F, Mansoorabadi S, Chen D, Reed GH, Frey PA. Enantiomeric free radicals and enzymatic control of stereochemistry in a radical mechanism: the case of lysine 2,3-aminomutases. Biochem 2006; 45:12639-46.
19. Bochner B, Gadzinski P, Panomitros E. Phenotype microarrays for high-throughput phenotypic testing and assay of gene function. Genome Res 2001; 11:1246-55.
20. Van Dyk T, Smulski D, Chang Y. Pleiotropic effects of poxA regulatory mutations of Escherichia coli and Salmonella typhimurium, mutations conferring sulfometuron methyl and alpha-ketobutyrate hypersensitivity. J Bacteriol 1987; 169:4540-6.
21. Bailly M, de Crécy-Lagard V. Predicting the pathway involved in post-translational modification of elongation factor P in a subset of bacterial species. Biol Direct 2010; 5:3.
22. Glick B, Ganoza M. Identification of a soluble protein that stimulates peptide bond synthesis. Proc Natl Acad Sci USA 1975; 72:4257-60.
23. Glick B, Chládek S, Ganoza M. Peptide bond formation stimulated by protein synthesis factor EF-P depends on the aminoacyl moiety of the acceptor. Eur J Biochem 1979; 97:23-8.
24. Hanawa-Suetsugu K, Sekine S, Sakai H, Hori-Takemoto C, Terada T, Unzai S, et al. Crystal structure of elongation factor P from Thermus thermophilus HB8. Proc Natl Acad Sci USA 2004; 101:9595-600.
25. Blaha G, Stanley R, Steitz T. Formation of the first peptide bond: the structure of EF-P bound to the 70S ribosome. Science 2009; 325:966-70.
26. Aoki H, Xu J, Emili A, Chosay JG, Golshani A, Ganoza MC. Interactions of elongation factor EF-P with the Escherichia coli ribosome. FEBS J 2008; 275:671-81.
27. Aoki H, Dekany K, Adams S, Ganoza M. The gene encoding the elongation factor P protein is essential for viability and is required for protein synthesis. J Biol Chem 1997; 272:32254-9.
28. Gerdes SY, Scholle MD, Campbell JW, et al. Experimental determination and system level analysis of essential genes in Escherichia coli MG1655. J Bacteriol 2003; 185:5673-84.
29. Yamamoto N, Nakahigashi K, Nakamichi T, Yoshino M, Takai Y, Touda Y, et al. Update on the Keio collection of Escherichia coli single-gene deletion mutants. Mol Syst Biol 2009; 5:335.
30. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2006; 2:2006-8.
31. Langridge GC, Phan M, Turner DJ, Perkins TT, Parts L, Haase J, et al. Simultaneous assay of every Salmonella typhi gene using one million transposon mutants. Genome Res 2009; 19:2308-16.
32. Peng W, Banta L, Charles T, Nester E. The chvH locus of Agrobacterium encodes a homologue of an elongation factor involved in protein synthesis. J Bacteriol 2001; 183:36-45.
33. Charles TC, Nester EW. A chromosomally encoded two-component sensory transduction system is required for virulence of Agrobacterium tumefaciens. J Bacteriol 1993; 175:6614-25.
34. Park M, Nishimura K, Zanelli C, Valentini S. Functional significance of eIF5A and its hypusine modification in eukaryotes. Amino Acids 2010; 38:491-500.
35. Clement P, Johansson H, Wolff E, Park M. Differential expression of eIF5A-1 and eIF5A-2 in human cancer cells. FEBS J 2006; 273:1102-14.
36. Frigieri M, Thompson G, Pandolfi J, Zanelli C, Valentini S. Use of a synthetic lethal screen to identify genes related to TIF51A in Saccharomyces cerevisiae. Genet Mol Res 2007; 6:152-65.
37. Liu Z, Duguay J, Ma F, Wang TW, Tshin R, Hopkins MT, et al. Modulation of eIF5A1 expression alters xylem abundance in Arabidopsis thaliana. J Exp Bot 2008; 59:939-50.
38. Li A, Li H, Jin B, Ye QN, Zhou T, Yu XD, et al. A novel eIF5A complex functions as a regulator of p53 and p53-dependent apoptosis. J Biol Chem 2004; 279:49251-8.
39. Sun Z, Cheng Z, Taylor C, Mcconkey B, Thompson J. Apoptosis induction by eIF5A1 involves activation of the intrinsic mitochondrial pathway. J Cell Physiol 2010; 223:798-809.
40. Rahman-Roblick R, Roblick UJ, Hellman U, Conrotto P, Liu T, Becker S, et al. p53 targets identified by protein expression profiling. Proc Natl Acad Sci USA 2007; 104:5401-6.
41. Li C, Ohn T, Ivanov P, Tisdale S, Anderson P. eIF5A promotes translation elongation, polysome disassembly and stress granule assembly. PLoS ONE 2010; 5:9942.
42. Ma F, Liu Z, Wang T, Hopkins MT, Peterson CA, Thompson JE. Arabidopsis eIF5A3 influences growth and the response to osmotic and nutrient stress. Plant Cell Environ 2010; 33:1682-96.
43. Xu J, Zhang B, Jiang C, Ming F. RceIF5A, encoding an eukaryotic translation initiation factor 5A in Rosa chinensis, can enhance thermotolerance, oxidative and osmotic stress resistance of Arabidopsis thaliana. Plant Mol Biol 2010; 75:167-78.
44. Xu A, Jao DL, Chen KY. Identification of mRNA that binds to eukaryotic initiation factor 5A by affinity co-purification and differential display. Biochem J 2004; 384:585-90.
45. Saini P, Eyler D, Green R, Dever T. Hypusinecontaining protein eIF5A promotes translation elongation. Nature 2009; 459:118-21.
46. Gregio A, Cano V, Avaca J, Valentini S, Zanelli C. eIF5A has a function in the elongation step of translation in yeast. Biochem Biophys Res Commun 2009; 380:785-90.
47. Bustamante V, Martínez L, Santana F, Knodler LA, Steele-Mortimer O, Puente JL. HilD-mediated transcriptional cross-talk between SPI-1 and SPI-2. Proc Natl Acad Sci USA 2008; 105:14591-6.
48. Clement PMJ, Henderson CA, Jenkins ZA, Smit-McBride Z, Wolff EC, Hershey JW, et al. Identification and characterization of eukaryotic initiation factor 5A-2. Eur J Bioche 2003; 270:4254-63.
49. Shi H, Moore PB. The crystal structure of yeast phenylalanine tRNA at 1.93 Å resolution: a classic structure revisited. RNA 2000; 6:1091-105.