Comparative proteomic analysis of the PhoP regulon in Salmonella enterica Serovar Typhi versus Typhimurium

PLoS ONE

Volumn 4, Issue 9, 2009, Pages

  Charles, Richelle C ^a,b   Harris, Jason B ^a,b   Chase, Michael R ^c,d   Lebrun, Lauren M ^a   Sheikh, Alaullah ^a,e   LaRocque, Regina C ^a,b   Logvinenko, Tanya ^f   Rollins, Sean M ^a   Tarique, Abdullah ^e   Hohmann, Elizabeth L ^a,b   Rosenberg, Ian ^c   Krastins, Bryan ^c   Sarracino, David A ^c   Qadri, Firdausi ^e   Calderwood, Stephen B ^a,b   Ryan, Edward T ^a,b,d  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c LABORATORY FOR MOLECULAR MEDICINE   (United States)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^e INTERNATIONAL CENTRE FOR DIARRHOEAL DISEASE RESEARCH   (Bangladesh)

^f TUFTS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CYTOLETHAL DISTENDING TOXIN; CYTOLETHAL DISTENDING TOXIN B; HEMOLYSIN; HEMOLYSIN E; MESSENGER RNA; MICROORGANISM PROTEIN; PERTUSSIS LIKE TOXIN A; PERTUSSIS LIKE TOXIN B; PERTUSSIS TOXIN; PHOP PROTEIN; PHOQ PROTEIN; PROTEIN SLYA; PROTEIN STY1499; UNCLASSIFIED DRUG; BACTERIAL VACCINE; PEPTIDE; PHOP PROTEIN, BACTERIA;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; FUNCTIONAL PROTEOMICS; GENE EXPRESSION; GENE REGULATORY NETWORK; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; MASS SPECTROMETRY; NONHUMAN; OPERON; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULON; SALMONELLA TYPHI; SALMONELLA TYPHIMURIUM; SPECIES COMPARISON; SPECIES DIFFERENCE; UPREGULATION; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; COMPARATIVE STUDY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; METHODOLOGY; MOUSE; MUTATION; PROTEOMICS; VIRULENCE;

BACTERIA (MICROORGANISMS); MUS; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHI; SALMONELLA TYPHI; SALMONELLA TYPHIMURIUM;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL VACCINES; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MICE; MODELS, BIOLOGICAL; MUTATION; PEPTIDES; PROTEOMICS; SALMONELLA TYPHI; SALMONELLA TYPHIMURIUM; SPECIES SPECIFICITY; VIRULENCE;

EID: 70349191583     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006994     Document Type: Article

References (60)

1. Crump JA, Luby SP, Mintz ED (2004) The global burden of typhoid fever. Bull World Health Organ 82: 346-353.
2. Parry CM, Hien TT, Dougan G, White NJ, Farrar JJ (2002) Typhoid fever. N Engl J Med 347: 1770-1782.
3. Parkhill J, Dougan G, James KD, Thomson NR, Pickard D, et al. (2001) Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413: 848-852.
4. Groisman EA (2001) The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 183: 1835-1842.
5. Miller SI, Loomis WP, Alpuche-Aranda C, Behlau I, Hohmann E (1993) The PhoP virulence regulon and live oral Salmonella vaccines. Vaccine 11: 122-125.
6. Fields PI, Groisman EA, Heffron F (1989) A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 243: 1059-1062.
7. 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 U S A 83: 5189-5193.
8. Zwir I, Shin D, Kato A, Nishino K, Latifi T, et al. (2005) Dissecting the PhoP regulatory network of Escherichia coli and Salmonella enterica. Proc Natl Acad Sci U S A 102: 2862-2867.
9. Monsieurs P, De Keersmaecker S, Navarre WW, Bader MW, De Smet F, et al. (2005) Comparison of the PhoPQ regulon in Escherichia coli and Salmonella typhimurium. J Mol Evol 60: 462-474.
10. +-responsive PhoP-PhoQ regulon in Salmonella enterica. J Bacteriol 185: 6287-6294.
11. Kato A, Groisman EA, Howard Hughes Medical Institute (2008) The PhoQ/ PhoP regulatory network of Salmonella enterica. Adv Exp Med Biol 631: 7-21.
12. Soncini FC, Garcia Vescovi E, Solomon F, Groisman EA (1996) Molecular basis of the magnesium deprivation response in Salmonella typhimurium: identification of PhoP-regulated genes. J Bacteriol 178: 5092-5099.
13. Garcia Vescovi E, Soncini FC, Groisman EA (1994) The role of the PhoP/ PhoQ regulon in Salmonella virulence. Res Microbiol 145: 473-480.
14. + as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84: 165-174.
15. Groisman EA, Mouslim C (2006) Sensing by bacterial regulatory systems in host and non-host environments. Nat Rev Microbiol 4: 705-709.
16. Bijlsma JJ, Groisman EA (2005) The PhoP/PhoQ system controls the intramacrophage type three secretion system of Salmonella enterica. Mol Microbiol 57: 85-96.
17. Kox LF, Wosten MM, Groisman EA (2000) A small protein that mediates the activation of a two-component system by another two-component system. EMBO J 19: 1861-1872.
18. Norte VA, Stapleton MR, Green J (2003) PhoP-responsive expression of the Salmonella enterica serovar Typhimurium slyA gene. J Bacteriol 185: 3508-3514.
19. Tu X, Latifi T, Bougdour A, Gottesman S, Groisman EA (2006) The PhoP/ PhoQ two-component system stabilizes the alternative sigma factor RpoS in Salmonella enterica. Proc Natl Acad Sci U S A 103: 13503-13508.
20. Ansong C, Yoon H, Norbeck AD, Gustin JK, McDermott JE, et al. (2008) Proteomics analysis of the causative agent of typhoid fever. J Proteome Res 7: 546-557.
21. Adkins JN, Mottaz HM, Norbeck AD, Gustin JK, Rue J, et al. (2006) Analysis of the Salmonella typhimurium proteome through environmental response toward infectious conditions. Mol Cell Proteomics 5: 1450-1461.
22. Shi L, Adkins JN, Coleman JR, Schepmoes AA, Dohnkova A, et al. (2006) Proteomic analysis of Salmonella enterica serovar Typhimurium isolated from RAW 264.7 macrophages: identification of a novel protein that contributes to the replication of serovar Typhimurium inside macrophages. J Biol Chem 281: 29131-29140.
23. Eriksson S, Lucchini S, Thompson A, Rhen M, Hinton JC (2003) Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 47: 103-118.
24. Faucher SP, Curtiss R 3rd, Daigle F (2005) Selective capture of Salmonella enterica serovar Typhi genes expressed in macrophages that are absent from the Salmonella enterica serovar Typhimurium genome. Infect Immun 73: 5217-5221.
25. Faucher SP, Porwollik S, Dozois CM, McClelland M, Daigle F (2006) Transcriptome of Salmonella enterica serovar Typhi within macrophages revealed through the selective capture of transcribed sequences. Proc Natl Acad Sci U S A 103: 1906-1911.
26. Daigle F, Graham JE, Curtiss R, 3rd (2001) Identification of Salmonella typhi genes expressed within macrophages by selective capture of transcribed sequences (SCOTS). Mol Microbiol 41: 1211-1222.
27. Hautefort I, Thompson A, Eriksson-Ygberg S, Parker ML, Lucchini S, et al. (2008) During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell Microbiol 10: 958-984.
28. Hohmann EL, Oletta CA, Killeen KP, Miller SI (1996) phoP/phoQ-deleted Salmonella typhi (Ty800) is a safe and immunogenic single-dose typhoid fever vaccine in volunteers. J Infect Dis 173: 1408-1414.
29. Kotton CN, Lankowski AJ, Scott N, Sisul D, Chen LM, et al. (2006) Safety and immunogenicity of attenuated Salmonella enterica serovar Typhimurium delivering an HIV-1 Gag antigen via the Salmonella Type III secretion system. Vaccine 24: 6216-6224.
30. Miller SI, Kukral AM, Mekalanos JJ (1989) A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. Proc Natl Acad Sci U S A 86: 5054-5058.
31. Behlau I, Miller SI (1993) A PhoP-repressed gene promotes Salmonella typhimurium invasion of epithelial cells. J Bacteriol 175: 4475-4484.
32. Kier LD, Weppelman RM, Ames BN (1979) Regulation of nonspecific acid phosphatase in Salmonella: phoN and phoP genes. J Bacteriol 138: 155-161.
33. Elias JE, Gygi SP (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 4: 207-214.
34. Zhang B, VerBerkmoes NC, Langston MA, Uberbacher E, Hettich RL, et al. (2006) Detecting differential and correlated protein expression in label-free shotgun proteomics. J Proteome Res 5: 2909-2918.
35. Haas BJ, Delcher AL, Wortman JR, Salzberg SL (2004) DAGchainer: a tool for mining segmental genome duplications and synteny. Bioinformatics 20: 3643-3646.
36. Larocque RC, Harris JB, Dziejman M, Li X, Khan AI, et al. (2005) Transcriptional profiling of Vibrio cholerae recovered directly from patient specimens during early and late stages of human infection. Infect Immun 73: 4488-4493.
37. Belden WJ, Miller SI (1994) Further characterization of the PhoP regulon: identification of new PhoP-activated virulence loci. Infect Immun 62: 5095-5101.
38. Faucher SP, Forest C, Beland M, Daigle F (2009) A novel PhoP-regulated locus encoding the cytolysin ClyA and the secreted invasin TaiA of Salmonella enterica serovar Typhi is involved in virulence. Microbiology 155: 477-488.
39. Soncini FC, Vescovi EG, Groisman EA (1995) Transcriptional autoregulation of the Salmonella typhimurium phoPQ operon. J Bacteriol 177: 4364-4371.
40. +responsive promoters. J Bacteriol 181: 5516-5520.
41. Yamamoto K, Ogasawara H, Fujita N, Utsumi R, Ishihama A (2002) Novel mode of transcription regulation of divergently overlapping promoters by PhoP, the regulator of two-component system sensing external magnesium availability. Mol Microbiol 45: 423-438.
42. Spory A, Bosserhoff A, von Rhein C, Goebel W, Ludwig A (2002) Differential regulation of multiple proteins of Escherichia coli and Salmonella enterica serovar Typhimurium by the transcriptional regulator SlyA. J Bacteriol 184: 3549-3559.
43. Aguirre A, Lejona S, Vescovi EG, Soncini FC (2000) Phosphorylated PmrA interacts with the promoter region of ugd in Salmonella enterica serovar Typhimurium. J Bacteriol 182: 3874-3876.
44. Mouslim C, Groisman EA (2003) Control of the Salmonella ugd gene by three two-component regulatory systems. Mol Microbiol 47: 335-344.
45. Wosten MM, Groisman EA (1999) Molecular characterization of the PmrA regulon. J Biol Chem 274: 27185-27190.
46. Carmel-Harel O, Storz G (2000) Roles of the glutathione- and thioredox-independent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu Rev Microbiol 54: 439-461.
47. Bjur E, Eriksson-Ygberg S, Aslund F, Rhen M (2006) Thioredoxin 1 promotes intracellular replication and virulence of Salmonella enterica serovar Typhimurium. Infect Immun 74: 5140-5151.
48. Haghjoo E, Galan JE (2004) Salmonella typhi encodes a functional cytolethal distending toxin that is delivered into host cells by a bacterial-internalization pathway. Proc Natl Acad Sci U S A 101: 4614-4619.
49. Spano S, Ugalde JE, Galan JE (2008) Delivery of a Salmonella typhi exotoxin from a host intracellular compartment. Cell Host Microbe 3: 30-38.
50. Haghjoo E, Galan JE (2007) Identification of a transcriptional regulator that controls intracellular gene expression in Salmonella typhi. Mol Microbiol 64: 1549-1561.
51. Libby SJ, Goebel W, Ludwig A, Buchmeier N, Bowe F, et al. (1994) A cytolysin encoded by Salmonella is required for survival within macrophages. Proc Natl Acad Sci U S A 91: 489-493.
52. Lithgow JK, Haider F, Roberts IS, Green J (2007) Alternate SlyA and H-NS nucleoprotein complexes control hlyE expression in Escherichia coli K-12. Mol Microbiol 66: 685-698.
53. Oscarsson J, Westermark M, Lofdahl S, Olsen B, Palmgren H, et al. (2002) Characterization of a pore-forming cytotoxin expressed by Salmonella enterica serovars Typhi and Paratyphi A. Infect Immun 70: 5759-5769.
54. Westermark M, Oscarsson J, Mizunoe Y, Urbonaviciene J, Uhlin BE (2000) Silencing and activation of ClyA cytotoxin expression in Escherichia coli. J Bacteriol 182: 6347-6357.
55. Wyborn NR, Stapleton MR, Norte VA, Roberts RE, Grafton J, et al. (2004) Regulation of Escherichia coli hemolysin E expression by H-NS and Salmonella SlyA. J Bacteriol 186: 1620-1628.
56. Lai XH, Arencibia I, Johansson A, Wai SN, Oscarsson J, et al. (2000) Cytocidal and apoptotic effects of the ClyA protein from Escherichia coli on primary and cultured monocytes and macrophages. Infect Immun 68: 4363-4367.
57. von Rhein C, Hunfeld KP, Ludwig A (2006) Serologic evidence for effective production of cytolysin A in Salmonella enterica serovars Typhi and Paratyphi A during human infection. Infect Immun 74: 6505-6508.
58. Buchmeier N, Bossie S, Chen CY, Fang FC, Guiney DG, et al. (1997) SlyA, a transcriptional regulator of Salmonella typhimurium, is required for resistance to oxidative stress and is expressed in the intracellular environment of macrophages. Infect Immun 65: 3725-3730.
59. von Rhein C, Bauer S, Lopez Sanjurjo EJ, Benz R, Goebel W, et al. (2008) ClyA cytolysin from Salmonella: Distribution within the genus, regulation of expression by SlyA, and pore-forming characteristics. Int J Med Microbiol.
60. Navarre WW, Halsey TA, Walthers D, Frye J, McClelland M, et al. (2005) Coregulation of Salmonella enterica genes required for virulence and resistance to antimicrobial peptides by SlyA and PhoP/PhoQ. Mol Microbiol 56: 492-508.