Nicotinic acid modulates Legionella pneumophila gene expression and induces virulence traits

Infection and Immunity

Volumn 81, Issue 3, 2013, Pages 945-955

  Edwards, Rachel L ^a   Bryan, Andrew ^a   Jules, Matthieu ^b   Harada, Kaoru ^a   Buchrieser, Carmen ^b   Swansona, Michele S ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINIC ACID;

ANIMAL CELL; ARTICLE; BACTERIAL VIRULENCE; BORDETELLA PERTUSSIS; CANDIDA GLABRATA; CELL MOTILITY; CYTOTOXICITY; ESCHERICHIA COLI; FEMALE; FLUOROMETRY; GENE EXPRESSION; LEGIONELLA PNEUMOPHILA; MACROPHAGE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RNA ISOLATION;

ANIMALS; BACTERIAL PROTEINS; BINDING SITES; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; LEGIONELLA PNEUMOPHILA; LYSOSOMES; MACROPHAGES; MICE; MODELS, MOLECULAR; NIACIN; PROTEIN CONFORMATION; TIME FACTORS; TRANSCRIPTOME; VIRULENCE;

EID: 84874735218     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00999-12     Document Type: Article

References (78)

1. Carratala J, Garcia-Vidal C. 2010. An update on Legionella. Curr. Opin. Infect. Dis. 23:152-157.
2. Declerck P. 2010. Biofilms: the environmental playground of Legionella pneumophila. Environ. Microbiol. 12:557-566.
3. Molofsky AB, Swanson MS. 2004. Differentiate to thrive: lessons from the Legionella pneumophila life cycle. Mol. Microbiol. 53:29-40.
4. Fettes PS, Forsbach-Birk V, Lynch D, Marre R. 2001. Overexpresssion of a Legionella pneumophila homologue of the E. coli regulator csrA affects cell size, flagellation and pigmentation. Int. J. Med. Microbiol. 291:353-360.
5. Molofsky AB, Swanson MS. 2003. Legionella pneumophila CsrA is a pivotal repressor of transmission traits and activator of replication. Mol. Microbiol. 50:445-461.
6. Dalebroux ZD, Edwards RL, Swanson MS. 2009. SpoT governs Legionella pneumophila differentiation in host macrophages. Mol. Microbiol. 71:640-658.
7. Edwards RL, Dalebroux ZD, Swanson MS. 2009. Legionella pneumophila couples fatty acid flux to microbial differentiation and virulence. Mol. Microbiol. 71:1190-1204.
8. Hammer BK, Swanson MS. 1999. Co-ordination of Legionella pneumophila virulence with entry into stationary phase by ppGpp. Mol. Microbiol. 33:721-731.
9. Zusman T, Gal-Mor O, Segal G. 2002. Characterization of a Legionella pneumophila relA insertion mutant and roles of RelA and RpoS in virulence gene expression. J. Bacteriol. 184:67-75.
10. 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.
11. 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.
12. Sahr T, Brüggemann H, Jules M, Lomma M, Albert-Weissenberger C, Cazalet C, Buchrieser C. 2009. Two small ncRNAs jointly govern virulence and transmission in Legionella pneumophila. Mol. Microbiol. 72: 741-762.
13. 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.
14. 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.
15. 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.
16. Jacobi S, Schade R, Heuner K. 2004. Characterization of the alternative sigma factor sigma54 and the transcriptional regulator FleQ of Legionella pneumophila, which are both involved in the regulation cascade of flagellar gene expression. J. Bacteriol. 186:2540-2547.
17. Lynch D, Fieser N, Gloggler K, Forsbach-Birk V, Marre R. 2003. The response regulator LetA regulates the stationary-phase stress response in Legionella pneumophila and is required for efficient infection of Acanthamoeba castellanii. FEMS Microbiol. Lett. 219:241-248.
18. Battesti A, Bouveret E. 2006. Acyl carrier protein/SpoT interaction, the switch linking SpoT-dependent stress response to fatty acid metabolism. Mol. Microbiol. 62:1048-1063.
19. Seyfzadeh M, Keener J, Nomura M. 1993. spoT-dependent accumulation of guanosine tetraphosphate in response to fatty acid starvation in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 90:11004-11008. 20. Calva E, Oropeza R. 2006. Two-component signal transduction systems, environmental signals, and virulence. Microb. Ecol. 51:166-176.
20. Calva E, Oropeza R. 2006. Two-component signal transduction systems, environmental signals, and virulence. Microb. Ecol. 51:166-176.
21. Broich M, Rydzewski K, McNealy TL, Marre R, Flieger A. 2006. The global regulatory proteins LetA and RpoS control phospholipase A, lysophospholipase A, acyltransferase, and other hydrolytic activities of Legionella pneumophila JR32. J. Bacteriol. 188:1218-1226.
22. Edwards RL, Jules M, Sahr T, Buchrieser C, Swanson MS. 2010. The Legionella pneumophila LetA/LetS two-component system exhibits rheostat- like behavior. Infect. Immun. 78:2571-2583.
23. Shi C, Forsbach-Birk V, Marre R, McNealy TL. 2006. The Legionella pneumophila global regulatory protein LetA affects DotA and Mip. Int. J. Med. Microbiol. 296:15-24.
24. Cotter PA, DiRita VJ. 2000. Bacterial virulence gene regulation: an evolutionary perspective. Annu. Rev. Microbiol. 54:519-565.
25. Cummings CA, Bootsma HJ, Relman DA, Miller JF. 2006. Species- and strain-specific control of a complex, flexible regulon by Bordetella BvgAS. J. Bacteriol. 188:1775-1785.
26. McPheat WL, Wardlaw AC, Novotny P. 1983. Modulation of Bordetella pertussis by nicotinic acid. Infect. Immun. 41:516-522.
27. Schneider DR, Parker CD. 1982. Effect of pyridines on phenotypic properties of Bordetella pertussis. Infect. Immun. 38:548-553.
28. Miller JF, Roy CR, Falkow S. 1989. Analysis of Bordetella pertussis virulence gene regulation by use of transcriptional fusions in Escherichia coli. J. Bacteriol. 171:6345-6348.
29. Eguchi Y, Oshima T, Mori H, Aono R, Yamamoto K, Ishihama A, Utsumi R. 2003. Transcriptional regulation of drug efflux genes by EvgAS, a two-component system in Escherichia coli. Microbiology 149:2819-2828.
30. Masuda N, Church GM. 2002. Escherichia coli gene expression responsive to levels of the response regulator EvgA. J. Bacteriol. 184:6225-6234.
31. Masuda N, Church GM. 2003. Regulatory network of acid resistance genes in Escherichia coli. Mol. Microbiol. 48:699-712.
32. Nishino K, Inazumi Y, Yamaguchi A. 2003. Global analysis of genes regulated by EvgA of the two-component regulatory system in Escherichia coli. J. Bacteriol. 185:2667-2672.
33. Nishino K, Yamaguchi A. 2001. Overexpression of the response regulator evgA of the two-component signal transduction system modulates multidrug resistance conferred by multidrug resistance transporters. J. Bacteriol. 183:1455-1458.
34. Utsumi R, Katayama S, Taniguchi M, Horie T, Ikeda M, Igaki S, Nakagawa H, Miwa A, Tanabe H, Noda M. 1994. Newly identified genes involved in the signal transduction of Escherichia coli K-12. Gene 140:73-77.
35. 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.
36. Bryan A, Harada K, Swanson MS. 2011. Efficient generation of unmarked deletions in Legionella pneumophila. Appl. Environ. Microbiol. 77:2545-2548.
37. Bryan A, Swanson MS. 2011. Oligonucleotides stimulate genomic alterations of Legionella pneumophila. Mol. Microbiol. 80:231-247.
38. Sexton JA, Vogel JP. 2004. Regulation of hypercompetence in Legionella pneumophila. J. Bacteriol. 186:3814-3825.
39. Swanson MS, Isberg RR. 1995. Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect. Immun. 63:3609-3620.
40. 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.
41. Byrne B, Swanson MS. 1998. Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect. Immun. 66:3029-3034.
42. Milohanic E, Glaser P, Coppee JY, Frangeul L, Vega Y, Vazquez-Boland JA, Kunst F, Cossart P, Buchrieser C. 2003. Transcriptome analysis of Listeria monocytogenes identifies three groups of genes differently regulated by PrfA. Mol. Microbiol. 47:1613-1625.
43. Brüggemann H, Hagman A, Jules M, Sismeiro O, Dillies MA, Gouyette C, Kunst F, Steinert M, Heuner K, Coppee JY, Buchrieser C. 2006. Virulence strategies for infecting phagocytes deduced from the in vivo transcriptional program of Legionella pneumophila. Cell. Microbiol. 8:1228-1240.
44. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP. 2002. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30:e15. doi:10.1093/nar/30.4.e15.
45. Delmar P, Robin S, Daudin JJ. 2005. VarMixt: efficient variance modelling for the differential analysis of replicated gene expression data. Bioinformatics 21:502-508.
46. Reiner A, Yekutieli D, Benjamini Y. 2003. Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19:368-375.
47. Cazalet C, Rusniok C, Brüggemann H, Zidane N, Magnier A, Ma L, Tichit M, Jarraud S, Bouchier C, Vandenesch F, Kunst F, Etienne J, Glaser P, Buchrieser C. 2004. Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat. Genet. 36:1165-1173.
48. Chien M, Morozova I, Shi S, Sheng H, Chen J, Gomez SM, Asamani G, Hill K, Nuara J, Feder M, Rineer J, Greenberg JJ, Steshenko V, Park SH, Zhao B, Teplitskaya E, Edwards JR, Pampou S, Georghiou A, Chou IC, Iannuccilli W, Ulz ME, Kim DH, Geringer-Sameth A, Goldsberry C, Morozov P, Fischer SG, Segal G, Qu X, Rzhetsky A, Zhang P, Cayanis E, De Jong PJ, Ju J, Kalachikov S, Shuman HA, Russo JJ. 2004. The genomic sequence of the accidental pathogen Legionella pneumophila. Science 305:1966-1968.
49. Edwards RL, Swanson MS. 2006. Regulation of the L. pneumophila life cycle, p 95-111. In Hoffman P, Klein T, FriedmanH(ed), Legionella pneumophila: pathogenesis and Immunity. Springer Publishing Corp., New York, NY.
50. Heuner K, Steinert M. 2003. The flagellum of Legionella pneumophila and its link to the expression of the virulent phenotype. Int. J. Med. Microbiol. 293:133-143.
51. Hales LM, Shuman HA. 1999. The Legionella pneumophila rpoS gene is required for growth within Acanthamoeba castellanii. J. Bacteriol. 181: 4879-4889.
52. Segal G, Feldman M, Zusman T. 2005. The Icm/Dot type-IV secretion systems of Legionella pneumophila and Coxiella burnetii. FEMS Microbiol. Rev. 29:65-81.
53. Weissenmayer BA, Prendergast JG, Lohan AJ, Loftus BJ. 2011. Sequencing illustrates the transcriptional response of Legionella pneumophila during infection and identifies seventy novel small non-coding RNAs. PLoS One 6:e17570. doi:10.1371/journal.pone.0017570.
54. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
55. Weisburg WG, Dobson ME, Samuel JE, Dasch GA, Mallavia LP, Baca O, Mandelco L, Sechrest JE, Weiss E, Woese CR. 1989. Phylogenetic diversity of the Rickettsiae. J. Bacteriol. 171:4202-4206.
56. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4:363-371.
57. Yin Y, He X, Szewczyk P, Nguyen T, Chang G. 2006. Structure of the multidrug transporter EmrD from Escherichia coli. Science 312:741-744.
58. Han YW, Uhl MA, Han SJ, Shi W. 1999. Expression of bvgAS of Bordetella pertussis represses flagellar biosynthesis of Escherichia coli. Arch. Microbiol. 171:127-130.
59. Leonardo MR, Dailly Y, Clark DP. 1996. Role of NAD in regulating the adhE gene of Escherichia coli. J. Bacteriol. 178:6013-6018.
60. Domergue R, Castano I, De Las Penas A, Zupancic M, Lockatell V, Hebel JR, Johnson D, Cormack BP. 2005. Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Science 308:866-870. 61. Blander G, Guarente L. 2004. The Sir2 family of protein deacetylases. Annu. Rev. Biochem. 73:417-435.
61. Blander G, Guarente L. 2004. The Sir2 family of protein deacetylases. Annu. Rev. Biochem. 73:417-435.
62. Starai VJ, Takahashi H, Boeke JD, Escalante-Semerena JC. 2004. A link between transcription and intermediary metabolism: a role for Sir2 in the control of acetyl-coenzyme A synthetase. Curr. Opin. Microbiol. 7:115-119.
63. Canto C, Auwerx J. 2011. NAD+ as a signaling molecule modulating metabolism. Cold Spring Harb. Symp. Quant. Biol. 76:291-298.
64. Brachmann CB, Sherman JM, Devine SE, Cameron EE, Pillus L, Boeke JD. 1995. The SIR2 gene family, conserved from bacteria to humans, functions in silencing, cell cycle progression, and chromosome stability. Genes Dev. 9:2888-2902.
65. Starai VJ, Celic I, Cole RN, Boeke JD, Escalante-Semerena JC. 2002. Sir2-dependent activation of acetyl-CoA synthetase by deacetylation of active lysine. Science 298:2390-2392.
66. Wolfe AJ. 2005. The acetate switch. Microbiol. Mol. Biol. Rev. 69:12-50. 67. Cotter PA, Miller JF. 1997. A mutation in the Bordetella bronchiseptica bvgS gene results in reduced virulence and increased resistance to starvation, and identifies a new class of Bvg-regulated antigens. Mol. Microbiol. 24:671-685.
67. Cotter PA, Miller JF. 1997. A mutation in the Bordetella bronchiseptica bvgS gene results in reduced virulence and increased resistance to starvation, and identifies a new class of Bvg-regulated antigens. Mol. Microbiol. 24:671-685.
68. Heeb S, Haas D. 2001. Regulatory roles of the GacS/GacA twocomponent system in plant-associated and other gram-negative bacteria. Mol. Plant Microbe Interact. 14:1351-1363.
69. Lapouge K, Schubert M, Allain Haas FH-TD. 2008. Gac/Rsm signal transduction pathway of γ-proteobacteria: from RNA recognition to regulation of social behavior. Mol. Microbiol. 67:241-253.
70. Perraud A, Weiss V, Gross R. 1999. Signalling pathways in twocomponent phosphorelay systems. Trends Microbiol. 7:115-120.
71. Wass MN, Kelley LA, Sternberg MJ. 2010. 3DLigandSite: predicting ligand-binding sites using similar structures. Nucleic Acids Res. 38: W469-W473.
72. Belenky P, Stebbins R, Bogan KL, Evans CR, Brenner C. 2011. Nrt1 and Tna1-independent export ofNAD+precursor vitamins promotesNAD+ homeostasis and allows engineering of vitamin production. PLoS One 6:e19710. doi:10.1371/journal.pone.0019710.
73. Lu SP, Kato M, Lin SJ. 2009. Assimilation of endogenous nicotinamide riboside is essential for calorie restriction-mediated life span extension in Saccharomyces cerevisiae. J. Biol. Chem. 284:17110-17119.
74. Belenky P, Bogan KL, Brenner C. 2007. NAD+metabolism in health and disease. Trends Biochem. Sci. 32:12-19.
75. 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.
76. Vogel JP, Roy C, Isberg RR. 1996. Use of salt to isolate Legionella pneumophila mutants unable to replicate in macrophages. Ann. N. Y. Acad. Sci. 797:271-272.
77. Yu D, Ellis HM, Lee EC, Jenkins NA, Copeland NG, Court DL. 2000. An efficient recombination system for chromosome engineering in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 97:5978-5983.
78. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645. Nicotinic Acid Induces Legionella Virulence Expression March.