Control of a Salmonella virulence operon by proline-charged tRNA Pro

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 8, 2014, Pages 3140-3145

  Lee, Eun Jin ^a,b,c,d   Choi, Jeongjoon ^a,b   Groisman, Eduardo A ^a,b,c  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c YALE UNIVERSITY   (United States)

^d Kyung Hee University   (South Korea)

Author keywords

Leader mRNA; Transcription attenuation

Indexed keywords

PROLINE TRANSFER RNA; SIGNAL PEPTIDE; THREONINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUXOTROPHY; BACTERIAL GENE; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CELL SURVIVAL; CODON; CONTROLLED STUDY; GENE EXPRESSION; HYPEROSMOTIC STRESS; MACROPHAGE; MGTC GENE; MICROBIAL ATTENUATION; MOUSE; NONHUMAN; OPERON; PHAGOCYTE; PRIORITY JOURNAL; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION;

LEADER MRNA; TRANSCRIPTION ATTENUATION;

5' UNTRANSLATED REGIONS; AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BASE PAIRING; BASE SEQUENCE; CATION TRANSPORT PROTEINS; CODON; GENE EXPRESSION REGULATION, BACTERIAL; HOST-PATHOGEN INTERACTIONS; MICE; MOLECULAR SEQUENCE DATA; OLIGODEOXYRIBONUCLEOTIDES; OPEN READING FRAMES; PROLINE; REAL-TIME POLYMERASE CHAIN REACTION; RNA, TRANSFER, PRO; SALMONELLA TYPHIMURIUM; VIRULENCE;

EID: 84896836077     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1316209111     Document Type: Article

References (39)

1. Blanc-Potard AB, Groisman EA (1997) The Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J 16(17):5376-5385.
2. Buchmeier N, et al. (2000) A parallel intraphagosomal survival strategy shared by mycobacterium tuberculosis and Salmonella enterica. Mol Microbiol 35(6):1375-1382. (Pubitemid 30175513)
3. Grabenstein JP, Fukuto HS, Palmer LE, Bliska JB (2006) Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infect Immun 74(7):3727-3741. (Pubitemid 43993304)
4. Lavigne JP, O'callaghan D, Blanc-Potard AB (2005) Requirement of MgtC for Brucella suis intramacrophage growth: A potential mechanism shared by Salmonella enterica and Mycobacterium tuberculosis for adaptation to a low-Mg2+ environment. Infect Immun 73(5):3160-3163.
5. Maloney KE, Valvano MA (2006) The mgtC gene of Burkholderia cenocepacia is required for growth under magnesium limitation conditions and intracellular survival in macrophages. Infect Immun 74(10):5477-5486. (Pubitemid 44484530)
6. Lee EJ, Pontes MH, Groisman EA (2013) A bacterial virulence protein promotes pathogenicity by inhibiting the bacterium's own F1Fo ATP synthase. Cell 154(1):146-156.
7. Turner AK, et al. (2003) Contribution of proton-translocating proteins to the virulence of Salmonella enterica serovars Typhimurium, Gallinarum, and Dublin in chickens and mice. Infect Immun 71(6):3392-3401. (Pubitemid 36637567)
8. Soncini FC, García Véscovi E, Solomon F, Groisman EA (1996) Molecular basis of the magnesium deprivation response in Salmonella typhimurium: Identification of PhoP-regulated genes. J Bacteriol 178(17):5092-5099. (Pubitemid 26293065)
9. Groisman EA (2001) The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 183(6):1835-1842.
10. Lee EJ, Groisman EA (2012) Control of a Salmonella virulence locus by an ATP-sensing leader messenger RNA. Nature 486(7402):271-275.
11. Lee EJ, Groisman EA (2012) Tandem attenuators control expression of the Salmonella mgtCBR virulence operon. Mol Microbiol 86(1):212-224.
12. Snavely MD, Miller CG, Maguire ME (1991) The mgtB Mg2+ transport locus of Salmonella typhimurium encodes a P-type ATPase. J Biol Chem 266(2):815-823. (Pubitemid 21907189)
13. Alix E, Blanc-Potard AB (2008) Peptide-assisted degradation of the Salmonella MgtC virulence factor. EMBO J 27(3):546-557. (Pubitemid 351225683)
14. Park SY, Cromie MJ, Lee EJ, Groisman EA (2010) A bacterial mRNA leader that employs different mechanisms to sense disparate intracellular signals. Cell 142(5):737-748.
15. Henkin TM, Yanofsky C (2002) Regulation by transcription attenuation in bacteria: How RNA provides instructions for transcription termination/ antitermination decisions. Bioessays 24(8):700-707. (Pubitemid 34850326)
16. Merino E, Yanofsky C (2005) Transcription attenuation: A highly conserved regulatory strategy used by bacteria. Trends Genet 21(5):260-264. (Pubitemid 40558929)
17. Csonka LN, Leisinger T (2007) Biosynthesis of proline. Escherichia coli and Salmonella. Cellular and Molecular Biology, ed Kaper J (ASM Press, Washinton, DC).
18. Baich A (1969) Proline synthesis in Escherichia coli. A proline-inhibitable glutamic acid kinase. Biochim Biophys Acta 192(3):462-467.
19. Strecker HJ (1957) The interconversion of glutamic acid and proline. I. The formation of delta1-pyrroline-5-carboxylic acid from glutamic acid in Escherichia coli. J Biol Chem 225(2):825-834.
20. Balaji B, O'Connor K, Lucas JR, Anderson JM, Csonka LN (2005) Timing of induction of osmotically controlled genes in Salmonella enterica Serovar Typhimurium, determined with quantitative real-time reverse transcription-PCR. Appl Environ Microbiol 71(12):8273-8283. (Pubitemid 41803954)
21. Doerfel LK, et al. (2013) EF-P is essential for rapid synthesis of proteins containing consecutive proline residues. Science 339(6115):85-88.
22. Tanner DR, Cariello DA, Woolstenhulme CJ, Broadbent MA, Buskirk AR (2009) Genetic identification of nascent peptides that induce ribosome stalling. J Biol Chem 284(50): 34809-34818.
23. Ude S, et al. (2013) Translation elongation factor EF-P alleviates ribosome stalling at polyproline stretches. Science 339(6115):82-85.
24. Woolstenhulme CJ, et al. (2013) Nascent peptides that block protein synthesis in bacteria. Proc Natl Acad Sci USA 110(10):E878-E887.
25. Navarre WW, et al. (2010) PoxA, yjeK, and elongation factor P coordinately modulate virulence and drug resistance in Salmonella enterica. Mol Cell 39(2):209-221.
26. Spinelli SV, Pontel LB, García Véscovi E, Soncini FC (2008) Regulation of magnesium homeostasis in Salmonella: Mg(2 +) targets the mgtA transcript for degradation by RNase E. FEMS Microbiol Lett 280(2):226-234. (Pubitemid 351287520)
27. García-del Portillo F (2001) Salmonella intracellular proliferation: Where, when and how? Microbes Infect 3(14-15):1305-1311.
28. Fields PI, Swanson RV, Haidaris CG, Heffron F (1986) Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci USA 83(14):5189-5193. (Pubitemid 16051340)
29. Steeb B, et al. (2013) Parallel exploitation of diverse host nutrients enhances Salmonella virulence. PLoS Pathog 9(4):e1003301.
30. Faucher SP, Mueller CA, Shuman HA (2011) Legionella Pneumophila transcriptome during intracellular multiplication in human macrophages. Front Microbiol 2:60.
31. Crawford JM, Kontnik R, Clardy J (2010) Regulating alternative lifestyles in entomopathogenic bacteria. Curr Biol 20(1):69-74.
32. García Véscovi E, Soncini FC, Groisman EA (1996) Mg2+ as an extracellular signal: Environmental regulation of Salmonella virulence. Cell 84(1):165-174.
33. Véscovi EG, Ayala YM, Di Cera E, Groisman EA (1997) Characterization of the bacterial sensor protein PhoQ. Evidence for distinct binding sites for Mg2+ and Ca2+. J Biol Chem 272(3):1440-1443. (Pubitemid 27043217)
34. Prost LR, et al. (2007) Activation of the bacterial sensor kinase PhoQ by acidic pH. Mol Cell 26(2):165-174. (Pubitemid 46617335)
35. Bader MW, et al. (2005) Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122(3):461-472. (Pubitemid 41127146)
36. Heithoff DM, et al. (1999) Coordinate intracellular expression of Salmonella genes induced during infection. J Bacteriol 181(3):799-807. (Pubitemid 29061561)
37. Cromie MJ, Shi Y, Latifi T, Groisman EA (2006) An RNA sensor for intracellular Mg(2+). Cell 125(1):71-84.
38. Davis RW, Bolstein D, Roth JR (1980) Advanced Bacterial Genetics (Cold Spring Harbor Lab Press, Cold Spring Harbor, NY).
39. Varshney U, Lee CP, RajBhandary UL (1991) Direct analysis of aminoacylation levels of tRNAs in vivo. Application to studying recognition of Escherichia coli initiator tRNA mutants by glutaminyl-tRNA synthetase. J Biol Chem 266(36):24712-24718. (Pubitemid 21909000)