Proteomic analysis of growth phase-dependent expression of Legionella pneumophila proteins which involves regulation of bacterial virulence traits

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Hayashi, Tsuyoshi ^a,b   Nakamichi, Masahiro ^a   Naitou, Hirotaka ^a   Ohashi, Norio ^a   Imai, Yasuyuki ^a   Miyake, Masaki ^a  

^a UNIVERSITY OF SHIZUOKA   (Japan)

^b NATIONAL INSTITUTE OF ANIMAL HEALTH   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; AMINO ACID; BACTERIAL ENZYME; BACTERIAL PROTEIN; KETONE BODY; LIPID; POLY(3 HYDROXYBUTYRIC ACID); SUGAR;

ACANTHAMOEBA; ACANTHAMOEBA POLYPHAGA; ARTICLE; BACTERIAL GROWTH; BACTERIAL TRANSLOCATION; BACTERIAL VIRULENCE; BORDETELLA PERTUSSIS; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; ENZYME GLYCOSYLATION; FATTY ACID SYNTHESIS; FLAGELLUM; GENE EXPRESSION REGULATION; HEMOLYSIS; HOST CELL; IN VITRO STUDY; LEGIONELLA PNEUMOPHILA; MACROPHAGE FUNCTION; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; METABOLIC BALANCE; MORPHOLOGICAL TRAIT; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANISMS BY ENERGY SOURCE; PHYSIOLOGICAL PROCESS; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEOMICS; SEQUENCE HOMOLOGY; SHEEP ERYTHROCYTE; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION; CELL LINE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; SOUTHERN BLOTTING; VIRULENCE;

BACTERIA (MICROORGANISMS); BORDETELLA PERTUSSIS; LEGIONELLA PNEUMOPHILA; OVIS ARIES;

BACTERIAL PROTEINS; BLOTTING, SOUTHERN; CELL LINE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; LEGIONELLA PNEUMOPHILA; PROTEOMICS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; VIRULENCE;

EID: 77955392504     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011718     Document Type: Article

References (78)

1. Horwitz MA, Silverstein SC (1980) Legionnaires' disease bacterium (Legionella pneumophila) multiples intracellularly in human monocytes. J Clin Invest 66: 441-450.
2. Harb OS, Gao LY, Abu Kwaik, Y (2000) From protozoa to mammalian cells: a new paradigm in the life cycle of intracellular bacterial pathogens. Environ Microbiol 2: 251-265.
3. Horwitz MA (1983) Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J Exp Med 158: 1319-1331.
4. Swanson MS, Isberg RR (1995) Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect Immun 63: 3609-3620.
5. Horwitz MA (1983) The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J Exp Med 158: 2108-2126.
6. Berger KH, Isberg RR (1993) Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol Microbiol 7: 7-19.
7. Sadosky AB, Wiater LA, Shuman HA (1993) Identification of Legionella pneumophila genes required for growth within and killing of human macrophages. Infect Immun 61: 5361-5373.
8. Ninio S, Roy CR (2007) Effector proteins translocated by Legionella pneumophila: strength in numbers. Trends Microbiol 15: 372-380.
9. Chen J, de Felipe KS, Clarke M, Lu H, Anderson OR, et al. (2004) Legionella effectors that promote nonlytic release from protozoa. Science 303: 1358-1361.
10. Bardill JP, Miller JL, Vogel JP (2005) IcmS-dependent translocation of SdeA into macrophages by the Legionella pneumophila type IV secretion system. Mol Microbiol 56: 90-103.
11. Shohdy N, Efe JA, Emr SD, Shuman HA (2005) Pathogen effector protein screening in yeast identifies Legionella factors that interfere with membrane trafficking. Proc Natl Acad Sci USA 102: 4866-4871.
12. de Felipe KS, Pampou S, Jovanovic OS, Pericone CD, Ye SF, et al. (2005) Evidence for acquisition of Legionella type IV secretion substrates via interdomain horizontal gene transfer. J Bacteriol 187: 7716-7726.
13. Murata T, Delprato A, Ingmundson A, Toomre DK, Lambright DG, et al. (2006) Legionella pneumophila effector protein DrrA is a Rab1 guanine nucleotideexchange factor. Nat Cell Biol 8: 971-977.
14. Franco IS, Shuman HA, Charpentier X (2009) The perplexing functions and surprising origins of Legionella pneumophila type IV secretion effectors. Cell Microbiol 11: 1435-1443.
15. Burstein D, Zusman T, Degtyar E, Viner R, Segal G, et al. (2009) Genome-scale identification of Legionella pneumophila effectors using a machine learning approach. PLoS Pathog 5: e1000508.
16. Ensminger AW, Isberg RR (2009) Legionella pneumophila Dot/Icm translocated substrates: a sum of parts. Curr Opin Microbiol 12: 67-73.
17. Laguna RK, Creasey EA, Li Z, Valtz N, Isberg RR (2006) A Legionella pneumophila-translocated substrate that is required for growth within macrophages and protection from host cell death. Proc Natl Acad Sci U S A 103: 18745-18750.
18. Liu Y, Luo ZQ (2007) The Legionella pneumophila effector SidJ is required for efficient recruitment of endoplasmic reticulum proteins to the bacterial phagosome. Infect Immun 75: 592-603.
19. Al-Khodor S, Price CT, Habyarimana F, Kalia A, Abu Kwaik YA (2008) Dot/Icm-translocated ankyrin protein of Legionella pneumophila is required for intracellular proliferation within human macrophages and protozoa. Mol Microbiol 70: 908-923.
20. Price CT, Al-Khodor S, Al-Quadan T, Santic M, Habyarimana F, et al. (2009) Molecular mimicry by an F-box effector of Legionella pneumophila hijacks a conserved polyubiquitination machinery within macrophages and protozoa. PLoS Pathog 5: e1000704.
21. Molofsky AB, Swanson MS (2004) Differentiate to thrive: lessons from the Legionella pneumophila life cycle. Mol Microbiol 53: 29-40.
22. Byrne B, Swanson MS (1998) Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect Immun 66: 3029-3034.
23. Hammer BK, Swanson MS (1999) Co-ordination of Legionella pneumophila virulence with entry into stationary phase by ppGpp. Mol Microbiol 33: 721-731.
24. Dalebroux ZD, Edwards RL, Swanson MS (2009) SpoT governs Legionella pneumophila differentiation in host macrophages. Mol Microbiol 71: 640-658.
25. Edwards RL, Dalebroux ZD, Swanson MS (2009) Legionella pneumophila couples fatty acid flux to microbial differentiation and virulence. Mol Microbiol 71: 1190-1204.
26. Bachman MA, Swanson MS (2001) RpoS co-operates with other factors to induce Legionella pneumophila virulence in the stationary phase. Mol Microbiol 40: 1201-1214.
27. Hammer BK, Tateda ES, Swanson MS (2002) A two-component regulator induces the transmission phenotype of stationary-phase Legionella pneumophila. Mol Microbiol 44: 107-118.
28. Molofsky AB, Swanson MS (2003) Legionella pneumophila CsrA is a pivotal repressor of transmission traits and activator of replication. Mol Microbiol 50: 445-461.
29. Sahr T, Brüggemann H, Jules M, Lomma M, Albert-Weissenberger C, et al. (2009) Two small ncRNAs jointly govern virulence and transmission in Legionella pneumophila. Mol Microbiol 72: 741-762.
30. Rasis M, Segal G (2009) The LetA-RsmYZ-CsrA regulatory cascade, together with RpoS and PmrA, post-transcriptionally regulates stationary phase activation of Legionella pneumophila Icm/Dot effectors. Mol Microbiol 72: 995-1010.
31. Miyake M, Watanabe T, Koike H, Molmeret M, Imai Y, et al. (2005) Characterization of Legionella pneumophila pmiA, a gene essential for infectivity of protozoa and macrophages. Infect Immun 73: 6272-6282.
32. Bozue JA, Johnson W (1996) Interaction of Legionella pneumophila with Acanthamoeba castellanii: uptake by coiling phagocytosis and inhibition of phagosome-lysosome fusion. Infect Immun 64: 668-673.
33. Sadosky AB, Wiater LA, Shuman HA (1993) Identification of Legionella pneumophila genes required for growth within and killing of human macrophages. Infect Immun 61: 5361-5373.
34. Ibuki Y, Naitou H, Ohashi N, Goto R (2005) Proteome analysis of UV-Binduced anti-apoptotic regulatory factors. Photochem Photobiol 81: 823-829.
35. Katanasaka Y, Asai T, Naitou H, Ohashi N, Oku N (2007) Proteomic characterization of angiogenic endothelial cells stimulated with cancer cellconditioned medium. Biol Pharm Bull 30: 2300-2307.
36. Wiater LA, Sadosky AB, Shuman HA (1994) Mutagenesis of Legionella pneumophila using Tn903 dlllacZ: identification of a growth-phase-regulated pigmentation gene. Mol Microbiol 11: 641-653.
37. Yerushalmi G, Zusman T, Segal G (2005) Additive effect on intracellular growth by Legionella pneumophila Icm/Dot proteins containing a lipobox motif. Infect Immun 73: 7578-7587.
38. Nagai H, Cambronne ED, Kagan JC, Amor JC, Kahn RA, et al. (2005) A Cterminal translocation signal required for Dot/Icm-dependent delivery of the Legionella RalF protein to host cells. Proc Natl Acad Sci USA 102: 826-831.
39. Kubori T, Matsushima Y, Nakamura D, Uralil J, Lara-Tejero M, et al. (1998) Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280: 602-605.
40. Cambronne ED, Roy CR (2007) The Legionella pneumophila IcmSW complex interacts with multiple Dot/Icm effectors to facilitate type IV translocation. PLoS Pathog 3: e188.
41. Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, et al. (2006) From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34: 354-357.
42. George JR, Pine L, Reeves MW, Harrell WK (1980) Amino acid requirements of Legionella pneumophila. J Clin Microbiol 11: 286-291.
43. Chien M, Morozova I, Shi S, Sheng H, Chen J, et al. (2004) The genomic sequence of the accidental pathogen Legionella pneumophila. Science 305: 1966-1968.
44. Cazalet C, Rusniok C, Brüggemann H, Zidane N, Magnier A, et al. (2004) Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat Genet 36: 1165-1173.
45. James BW, Mauchline WS, Dennis PJ, Keevil CW, Wait R (1999) Poly-3- hydroxybutyrate in Legionella pneumophila, an energy source for survival in lownutrient environments. Appl Environ Microbiol 65: 822-827.
46. Irikura VM, Kihara M, Yamaguchi S, Sockett H, Macnab RM (1993) Salmonella typhimurium fliG and fliN mutations causing defects in assembly, rotation, and switching of the flagellar motor. J Bacteriol 175: 802-810.
47. Ren T, Zamboni DS, Roy CR, Dietrich WF, Vance RE (2006) Flagellin deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog 2: e18.
48. Whitfield NN, Byrne BG, Swanson MS (2010) Mouse macrophages are permissive to motile Legionella species that fail to trigger pyroptosis. Infect Immun 78: 423-432.
49. Merz AJ, So M, Sheetz MP (2000) Pilus retraction powers bacterial twitching motility. Nature 407: 98-102.
50. Coil DA, Anné J (2009) Twitching motility in Legionella pneumophila FEMS Microbiol Lett 293: 271-277.
51. Stone BJ, Abu Kwaik Y (1998) Expression of multiple pili by Legionella pneumophila: identification and characterization of a type IV pilin gene and its role in adherence to mammalian and protozoan cells. Infect Immun 66: 1768-1775.
52. Stone BJ, Kwaik YA (1999) Natural competence for DNA transformation by Legionella pneumophila and its association with expression of type IV pili. J Bacteriol 181: 1395-1402.
53. Molofsky AB, Shetron-Rama LM, Swanson MS (2005) Components of the Legionella pneumophila flagellar regulon contribute to multiple virulence traits, including lysosome avoidance and macrophage death. Infect Immun 73: 5720-5734.
54. Luo ZQ, Isberg RR (2004) Multiple substrates of the Legionella pneumophila Dot/Icm system identified by interbacterial protein transfer. Proc Natl Acad Sci USA 101: 841-846.
55. Nagai H, Kagan JC, Zhu X, Kahn RA, Roy CR (2002) A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 295: 679-682.
56. Brüggemann H, Hagman A, Jules M, Sismeiro O, Dillies MA, et al. (2006) Virulence strategies for infecting phagocytes deduced from the in vivo transcriptional program of Legionella pneumophila. Cell Microbiol 8: 1228-1240.
57. Pan X, Lührmann A, Satoh A, Laskowski-Arce MA, Roy CR (2008) Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors. Science 320: 1651-1654.
58. Buckles EL, Wang X, Lockatell CV, Johnson DE, Donnenberg MS (2006) PhoU enhances the ability of extraintestinal pathogenic Escherichia coli strain CFT073 to colonize the murine urinary tract. Microbiology 152: 153-60.
59. Stancik LM, Stancik DM, Schmidt B, Barnhart D M, Yoncheva YN, et al. (2002) PH-dependent expression of periplasmic proteins and amino acid catabolism in Escherichia coli. J Bacteriol 184: 4246-4258.
60. Young IG, McCann LM, Stroobant P, Gibson F (1971) Characterization and genetic analysis of mutant strains of Escherichia coli K-12 accumulating the biquinone precursors 2-octaprenyl-6-methoxy-1,4-benzoquinone and 2-octaprenyl- 3-methyl-6-methoxy-1,4-benzo-quinone. J Bacteriol 105: 769-778.
61. Benin AL, Benson RF, Besser RE (2002) Trends in legionnaires disease, 1980- 1998: declining mortality and new patterns of diagnosis. Clin Infect Dis 35: 1039-1046.
62. Cazalet C, Jarraud S, Ghavi-Helm Y, Kunst F, Glaser P, et al. (2008) Multigenome analysis identifies a worldwide distributed epidemic Legionella pneumophila clone that emerged within a highly diverse species. Genome Res 18: 431-441.
63. Zuckman DM, Hung JB, Roy CR (1999) Pore-forming activity is not sufficient for Legionella pneumophila phagosome trafficking and intracellular growth. Mol Microbiol 32: 990-1001.
64. Alli OA, Gao LY, Pedersen LL, Zink S, Radulic M, et al. (2000) Temporal pore ormation-mediated egress from macrophages and alveolar epithelial cells by Legionella pneumophila. Infect Immun 68: 6431-6440.
65. Molmeret M, Alli OA, Radulic M, Susa M, Doric M, et al. (2002) The Cterminus of IcmT is essential for pore formation and for intracellular trafficking of Legionella pneumophila within Acanthamoeba polyphaga. Mol Microbiol 43: 1139-1150.
66. Molmeret M, Alli OA, Zink S, Flieger A, Cianciotto NP, et al. (2002) IcmT is essential for pore formation-mediated egress of Legionella pneumophila from mammalian and protozoan cells. Infect Immun 70: 69-78.
67. Duménil G, Montminy TP, Tang M, Isberg RR (2004) IcmR-regulated membrane insertion and efflux by the Legionella pneumophila IcmQ protein. J Biol Chem 279: 4686-4695.
68. Sory MP, Boland A, Lambermont I, Cornelis GR (1995) Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc Natl Acad Sci USA 92: 11998-12002.
69. Bachman MA, Swanson MS (2004) Genetic evidence that Legionella pneumophila RpoS modulates expression of the transmission phenotype in both the exponential phase and the stationary phase. Infect Immun 72: 2468-2476.
70. Albers U, Tiaden A, Spirig T, Al Alam D, Goyert SM, et al. (2007) Expression of Legionella pneumophila paralogous lipid A biosynthesis genes under different growth conditions. Microbiology 153: 3817-3829.
71. Bachman MA, Swanson MS (2004) The LetE protein enhances expression of multiple LetA/LetS-dependent transmission traits by Legionella pneumophila. Infect Immun 72: 3284-3293.
72. Kubori T, Hyakutake A, Nagai H (2008) Legionella translocates an E3 ubiquitin ligase that has multiple U-boxes with distinct functions. Mol Microbiol 67: 1307-1319.
73. Machner MP, Isberg RR (2006) Targeting of host Rab GTPase function by the intravacuolar pathogen Legionella pneumophila. Dev Cell 11: 47-56.
74. Banga S, Gao P, Shen X, Fiscus V, Zong WX, et al. (2007) Legionella pneumophila inhibits macrophage apoptosis by targeting pro-death members of the Bcl2 protein family. Proc Natl Acad Sci USA 104: 5121-5126.
75. Lebeau I, Lammertyn E, De Buck E, Maes L, Geukens N, et al. (2005) First proteomic analysis of Legionella pneumophila based on its developing genome sequence. Res Microbiol 156: 119-129.
76. DebRoy S, Dao J, Soderberg M, Rossier O, Cianciotto NP (2006) Legionella pneumophila type II secretome reveals unique exoproteins and a chitinase that promotes bacterial persistence in the lung. Proc Natl Acad Sci USA 103: 19146-19151.
77. Tiaden A, Spirig T, Weber SS, Brüggemann H, Bosshard R, et al. (2007) Legionella pneumophila response regulator LqsR promotes host cell interactions as an element of the virulence regulatory network controlled by RpoS and LetA. Cell Microbiol 9: 2903-2920.
78. De Buck E, Höper D, Lammertyn E, Hecker M, Anné J (2008) Differential 2-D protein gel electrophoresis analysis of Legionella pneumophila wild type and Tat secretion mutants. Int J Med Microbiol 298: 449-461.