Components of the Legionella pneumophila flagellar regulon contribute to multiple virulence traits, including lysosome avoidance and macrophage death

Infection and Immunity

Volumn 73, Issue 9, 2005, Pages 5720-5734

  Molofsky, A B ^a   Shetron Rama, L M ^a   Swanson, Michele S ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; CRYSTAL VIOLET; FLAGELLIN; MELANIN; SIGMA FACTOR; SIGMA FACTOR FLIAA; UNCLASSIFIED DRUG;

AMOEBA; ANIMAL CELL; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BONE MARROW CELL; CELL DEATH; CELL MATURATION; CENTRIFUGATION; CONTROLLED STUDY; DEGRADATION; FEMALE; FLIA GENE; GENE; HOST CELL; LEGIONELLA PNEUMOPHILA; LYSOSOME; MACROPHAGE; MOUSE; MUTANT; NONHUMAN; NUTRIENT; PHAGOSOME; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REGULON; SECRETION; WILD TYPE;

ANIMALS; BACTERIAL PROTEINS; CELL DEATH; CELLS, CULTURED; FEMALE; FLAGELLA; FLAGELLIN; HEAT; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; MACROPHAGES; MICE; MICE, INBRED A; MURAMIDASE; REGULON; SIGMA FACTOR; SODIUM; VIRULENCE;

EID: 23944485009     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.9.5720-5734.2005     Document Type: Article

References (103)

1. Adamo, R., S. Sokol, G. Soong, M. I. Gomez, and A. Prince. 2004. Pseudomonas aeruginosa flagella activate airway epithelial cells through asia-loGM1 and toll-like receptor 2 as well as toll-like receptor 5. Am. J. Respir. Cell Mol. Biol. 30:627-634.
2. Aldridge, P., and K. T. Hughes. 2002. Regulation of flagellar assembly. Curr. Opin. Microbiol. 5:160-165.
3. Allen-Vercoe, E., and M. J. Woodward. 1999. The role of flagella, but not fimbriae, in the adherence of Salmonella enterica serotype Enteritidis to chick gut explant. J. Med. Microbiol. 48:771-780.
4. Alli, O. A. T., L.-Y. Gao, L. L. Pedersen, S. Zink, M. Radulic, M. Doric, and Y. Abu Kwaik. 2000. Temporal pore formation-mediated egress from macrophages and alveolar epithelial cells by Legionella pneumophila. Infect. Immun. 68:6431-6440.
5. +-driven flagellar motors of alkalophilic Bacillus strains by the amiloride analog phenamil. J. Bacteriol. 172:1634-1639.
6. Bachman, M. A., and M. S. Swanson. 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.
7. Bachman, M. A., and M. S. Swanson. 2004. The LetE protein enhances expression of multiple LetA/LetS-dependent transmission traits by Legionella pneumophila. Infect. Immun. 72:3284-3293.
8. Bachman, M. A., and M. S. Swanson. 2001. RpoS co-operates with other factors to induce Legionella pneumophila virulence in the stationary phase. Mol. Microbiol. 40:1201-1214.
9. Bardill, J. P., J. L. Miller, and J. P. Vogel. 2005. IcmS-dependent translocation of SdeA into macrophages by the Legionella pneumophila type IV secretion system. Mol. Microbiol. 56:90-103.
10. Berger, K. H., and R. R. Isberg. 1993. Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol. Microbiol. 7:7-19.
11. Berger, K. H., J. J. Merriam, and R. I. Isberg. 1994. Altered intracellular targeting properties associated with mutations in the Legionella pneumophila dotA gene. Mol. Microbiol. 14:809-822.
12. Blackmon, J. A., M. D. Hicklin, and F. W. Chandler. 1978. Legionnaires' disease. Pathological and historical aspects of a 'new' disease. Arch. Pathol. Lab. Med. 102:337-343.
13. Blocker, A., K. Komoriya, and S. Aizawa. 2003. Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc. Natl. Acad. Sci. USA 100:3027-3030.
14. Bohach, G. A., and I. S. Snyder. 1983. Characterization of surfaces involved in adherence of Legionella pneumophila to Fischerella species. Infect. Immun. 42:318-325.
15. Bosshardt, S. C., R. F. Benson, and B. S. Fields. 1997. Flagella are a positive predictor for virulence in Legionella. Microb. Pathog. 23:107-112.
16. Brieland, J., P. Freeman, R. Kunkel, C. Chrisp, M. Hurley, J. Fantone, and C. Engleberg. 1994. Replicative Legionella pneumophila lung infection in intratracheally inoculated A/J mice. Am. J. Pathol. 145:1537-1546.
17. Byrne, B., and M. S. Swanson. 1998. Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect. Immun. 66:3029-3034.
18. Chandler, F. W., B. M. Thomason, and G. A. Hebert. 1980. Flagella on Legionnaires' disease bacteria in the human lung. Ann. Intern. Med. 93:715-716.
19. Chen, J., K. S. de Felipe, M. Clarke, H. Lu, O. R. Anderson, G. Segal, and H. A. Shuman. 2004. Legionella effectors that promote nonlytic release from protozoa. Science 303:1358-1361.
20. Chien, M., I. Morozova, S. Shi, H. Sheng, J. Chen, S. M. Gomez, G. Asamani, K. Hill, J. Nuara, M. Feder, J. Rineer, J. J. Greenberg, V. Steshenko, S. H. Park, B. Zhao, E. Teplitskaya, J. R. Edwards, S. Pampou, A. Georghiou, I. C. Chou, W. Iannuccilli, M. E. Ulz, D. H. Kim, A. Geringer-Sameth, C. Goldsberry, P. Morozov, S. G. Fischer, G. Segal, X. Qu, A. Rzhetsky, P. Zhang, E. Cayanis, P. J. De Jong, J. Ju, S. Kalachikov, H. A. Shuman, and J. J. Russo. 2004. The genomic sequence of the accidental pathogen Legionella pneumophila. Science 305:1966-1968.
21. Christie, P. J., and J. P. Vogel. 2000. Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol. 8:354-360.
22. Cirillo, S. L., L. E. Bermudez, S. H. El-Etr, G. E. Duhamel, and J. D. Cirillo. 2001. Legionella pneumophila entry gene rtxA is involved in virulence. Infect. Immun. 69:508-517.
23. Dasgupta, N., M. C. Wolfgang, A. L. Goodman, S. K. Arora, J. Jyot, S. Lory, and R. Ramphal. 2003. A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol. Microbiol. 50:809-824.
24. Dietrich, C., K. Heuner, B. C. Brand, J. Hacker, and M. Steinert. 2001. Flagellum of Legionella pneumophila positively affects the early phase of infection of eukaryotic host cells. Infect. Immun. 69:2116-2122.
25. Doyle, T. B., A. C. Hawkins, and L. L. McCarter. 2004. The complex flagellar torque generator of Pseudomonas aeruginosa. J. Bacteriol. 186:6341-6350.
26. Fettes, P. S., V. Forsbach-Birk, D. Lynch, and R. Marre. 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.
27. Fields, B. S. 1996. The molecular ecology of legionellae. Trends Microbiol. 4:286-290.
28. Flieger, A., K. Rydzewski, S. Banerji, M. Broich, and K. Heuner. 2004. Cloning and characterization of the gene encoding the major cell-associated phospholipase A of Legionella pneumophila, plaB, exhibiting hemolytic activity. Infect. Immun. 72:2648-2658.
29. Gal-Mor, O., and G. Segal. 2003. The Legionella pneumophila GacA homolog (LetA) is involved in the regulation of icm virulence genes and is required for intracellular multiplication in Acanthamoeba castellanii. Microb. Pathog. 34:187-194.
30. Gao, L. Y., and Y. A. Kwaik. 2000. The mechanism of killing and exiting the protozoan host Acanthamoeba polyphaga by Legionella pneumophila, Environ. Microbiol. 2:79-90.
31. Ghelardi, E., F. Celandroni, S. Salvetti, D. J. Beecher, M. Gominet, D. Lereclus, A. C. Wong, and S. Senesi. 2002. Requirement of flhA for swarming differentiation, flagellin export, and secretion of virulence-associated proteins in Bacillus thuringiensis. J. Bacteriol. 184:6424-6433.
32. Girard, R., T. Pedron, S. Uematsu, V. Balloy, M. Chignard, S. Akira, and R. Chaby. 2003. Lipopolysaccharides from Legionella and Rhizobium stimulate mouse bone marrow granulocytes via Toll-like receptor 2. J. Cell Sci. 116:293-302.
33. Giron, J. A., A. G. Torres, E. Freer, and J. B. Kaper. 2002. The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol. Microbiol. 44:361-379.
34. +-driven motor of Escherichia coli. J. Bacteriol. 182:4234-4240.
35. Hammer, B. K., and M. S. Swanson. 1999. Co-ordination of Legionella pneumophila virulence with entry into stationary phase by ppGpp. Mol. Microbiol. 33:721-731.
36. Hammer, B. K., E. S. Tateda, and M. S. Swanson. 2002. A two-component regulator induces the transmission phenotype of stationary-phase Legionella pneumophila. Mol. Microbiol. 44:107-118.
37. Heuner, K., L. Bender-Beck, B. C. Brand, P. C. Luck, K. H. Mann, R. Marre, M. Ott, and J. Hacker. 1995. Cloning and genetic characterization of the flagellum subunit gene (flaA) of Legionella pneumophila serogroup 1. Infect. Immun. 63:2499-2507.
38. 28 factor on virulence and flagellum expression of Legionella pneumophila. Infect. Immun. 70:1604-1608.
39. 28 of Legionella pneumophila restores flagellation and motility to an Escherichia coli fliA mutant. J. Bacteriol. 179:17-23.
40. Heuner, K., and M. Steinert. 2003. The flagellum of Legionella pneumophila and its link to the expression of the virulent phenotype. Int. J. Med. Microbiol. 293:133-143.
41. Heytler, P. G., and W. W. Prichard. 1962. A new class of uncoupling agents-carbonyl cyanide phenylhydrazones. Biochem. Biophys. Res. Commun. 7:272-275.
42. Horwitz, M. A. 1983. The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J. Exp. Med. 158:2108-2126.
43. Horwitz, M. A., and S. C. Silverstein. 1980. Legionnaires' disease bacterium (Legionella pneumophila) multiplies intracellularly in human monocytes. J. Clin. Investig. 66:441-450.
44. Husmann, L. K., and W. Johnson. 1994. Cytotoxicity of extracellular Legionella pneumophila. Infect. Immun. 62:2111-2114.
45. Ikeda, T., K. Oosawa, and H. Hotani. 1996. Self-assembly of the filament capping protein, FliD, of bacterial flagella into an annular structure. J. Mol Biol. 259:679-686.
46. Ikeda, T., S. Yamaguchi, and H. Hotani. 1993. Flagellar growth in a filament-less Salmonella fliD mutant supplemented with purified hook-associated protein 2. J. Biochem. (Tokyo) 114:39-44.
47. Inglis, T. J., T. Robertson, D. E. Woods, N. Dutton, and B. J. Chang. 2003. Flagellum-mediated adhesion by Burkholderia pseudomallei precedes invasion of Acanthamoeba astronyxis. Infect. Immun. 71:2280-2282.
48. 54 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.
49. Joshi, A. D., S. Sturgill-Koszycki, and M. S. Swanson. 2001. Evidence that Dot-dependent and -independent factors isolate the Legionella pneumophila phagosome from the endocytic network in mouse macrophages. Cell Microbiol. 3:99-114.
50. Katz, S. M., and S. Hahemi. 1982. Electron microscopic examination of the inflammatory response to Legionella pneumophila in guinea pigs. Lab. Investig. 46:24-32.
51. Kirby, J. E., J. P. Vogel, H. L. Andrews, and R. R. Isberg. 1998. Evidence of pore-forming ability by Legionella pneumophila. Mol. Microbiol. 27:323-336.
52. Kirov, S. M., M. Castrisios, and J. G. Shaw. 2004. Aeromonas flagella (polar and lateral) are enterocyte adhesins that contribute to biofilm formation on surfaces. Infect. Immun. 72:1939-1945.
53. Komoriya, K., N. Shibano, T. Higano, N. Azuma, S. Yamaguchi, and S. I. Aizawa. 1999. Flagellar proteins and type III-exported virulence factors are the predominant proteins secreted into the culture media of Salmonella typhimurium. Mol. Microbiol. 34:767-779.
54. Konkel, M. E., J. D. Klena, V. Rivera-Amill, M. R. Monteville, D. Biswas, B. Raphael, and J. Mickelson. 2004. Secretion of virulence proteins from Campylobacter jejuni is dependent on a functional fiagellar export apparatus. J. Bacteriol. 186:3296-3303.
55. Kutsukake, K., Y. Ohya, and T. Iino. 1990. Transcriptional analysis of the flagellar regulon of Salmonella typhimurium. J. Bacteriol. 172:741-747.
56. Landini, P., and A. J. Zehnder. 2002. The global regulatory hns gene negatively affects adhesion to solid surfaces by anaerobically grown Escherichia coli by modulating expression of flagellar genes and lipopolysaccharide production. J. Bacteriol. 184:1522-1529.
57. Luneberg, E., N. Zetzmann, D. Alber, Y. A. Knirel, O. Kooistra, U. Zahringer, and M. Frosch. 2000. Cloning and functional characterization of a 30 kb gene locus required for lipopolysaccharide biosynthesis in Legionella pneumophila. Int. J. Med. Microbiol. 290:37-49.
58. Lynch, D., N. Fieser, K. Gloggler, V. Forsbach-Birk, and R. Marre. 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.
59. Macnab, R. M. 2003. How bacteria assemble flagella. Annu. Rev. Microbiol. 57:77-100.
60. McDade, J. E., C. C. Shepard, D. W. Fraser, T. R. Tsai, M. A. Redus, and W. R. Dowdle. 1977. Legionnaires' disease: isolation of a bacterium and demonstration of its role in other respiratory diseases. N. Engl. J. Med. 297:1197-1203.
61. Merriam, J. J., R. Mathur, R. Maxfield-Boumil, and R. R. Isberg. 1997. Analysis of the Legionella pneumophila fliI gene: intracellular growth of a denned mutant defective for flagellum biosynthesis. Infect. Immun. 65:2497-2501.
62. Minamino, T., T. Iino, and K. Kutuskake. 1994. Molecular characterization of the Salmonella typhimurium flhB operon and its protein products. J. Bacteriol. 176:7630-7637.
63. Minamino, T., and R. M. Macnab. 1999. Components of the Salmonella flagellar export apparatus and classification of export substrates. J. Bacteriol. 181:1388-1394.
64. Molmeret, M., O. A. Alli, M. Radulic, M. Susa, M. Doric, and Y. A. Kwaik. 2002. The C-terminus of IcmT is essential for pore formation and for intracellular trafficking of Legionella pneumophila within Acanthamoeba polyphaga. Mol. Microbiol. 43:1139-1150.
65. Molofsky, A. B., and M. S. Swanson. 2004. Differentiate to thrive: lessons from the Legionella pneumophila life cycle. Mol. Microbiol. 53:29-40.
66. Molofsky, A. B., and M. S. Swanson. 2003. Legionella pneumophila CsrA is a pivotal repressor of transmission traits and activator of replication. Mol. Microbiol. 50:445-461.
67. Nishihara, T., and E. Freese. 1975. Motility of Bacillus subtilis during growth and sporulation. J. Bacteriol. 123:366-371.
68. Okuda, S., R. Igarashi, Y. Kusui, Y. Kasahara, and H. Morisaki. 2003. Electrophoretic mobility of Bacillus subtilis knockout mutants with and without flagella. J. Bacteriol. 185:3711-3717.
69. Ott, M., P. Messner, J. Heesemann, R. Marre, and J. Hacker. 1991. Temperature-dependent expression of flagella in Legionella. J. Gen. Microbiol. 137:1955-1961.
70. Ottemann, K. M., and J. F. Miller. 1997. Roles for motility in bacterial-host interactions. Mol. Microbiol. 24:1109-1117.
71. 28-dependent flagellar gene transcription hierarchy of Vibrio cholerae. Mol. Microbiol. 39:1595-1609.
72. Pruckler, J. M., R. F. Benson, M. Moyenuddin, W. T. Martin, and B. S. Fields. 1995. Association of flagellum expression and intracellular growth of Legionella pneumophila. Infect. Immun. 63:4928-4932.
73. Quinn, F. D., and L. S. Tompkins. 1989. Analysis of a cloned sequence of Legionella pneumophila encoding a 38 kD metalloprotease possessing haemolytic and cytotoxic activities. Mol. Microbiol. 3:797-805.
74. Ristroph, J. D., K. W. Hedlund, and S. Gowda. 1981. Chemically defined medium for Legionella pneumophila growth. J. Clin. Microbiol. 13:115-119.
75. Rohde, M., J. Puls, R. Buhrdorf, W. Fischer, and R. Haas. 2003. A novel sheathed surface organelle of the Helicobacterpylori cag type IV secretion system. Mol. Microbiol. 49:219-234.
76. Rowbotham, T. J. 1986. Current views on the relationships between amoebae, legionellae and man. Isr. J. Med. Sci. 22:678-689.
77. Rowbotham, T. J. 1980. Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J. Clin. Pathol. 33:1179-1183.
78. Roy, C. R., and R. R. Isberg. 1997. Topology of Legionella pneumophila DotA: an inner membrane protein required for replication in macrophages. Infect. Immun. 65:571-578.
79. Sadosky, A. B., L. A. Water, and H. A. Shuman. 1993. Identification of Legionella pneumophila genes required for growth within and killing of human macrophages. Infect. Immun. 61:5361-5373.
80. Scharfman, A., S. K. Arora, P. Delmotte, E. Van Brussel, J. Mazurier, R. Ramphal, and P. Roussel. 2001. Recognition of Lewis x derivatives present on mucins by flagellat components of Pseudomonas aeruginosa. Infect. Immun. 69:5243-5248.
81. Scherer, D. C., I. DeBuron-Connors, and M. F. Minnick. 1993. Characterization of Bartonella bacilliformis flagella and effect of antiflagellin antibodies on invasion of human erythrocytes. Infect. Immun. 61:4962-4971.
82. Segal, G., M. Purchell, and H. A. Shuman. 1998. Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc. Natl. Acad. Sci. USA 95:1669-1674.
83. Shimizu, R., F. Taguchi, M. Marutani, T. Mukaihara, Y. Inagaki, K. Toyoda, T. Shiraishi, and Y. Ichinose. 2003. The ΔfliD mutant of Pseudomonas syringae pv. tabaci, which secretes flagellin monomers, induces a strong hypersensitive reaction (HR) in non-host tomato cells. Mol. Genet. Genomics 269:21-30.
84. Song, Y. C., S. Jin, H. Louie, D. Ng, R. Lau, Y. Zhang, R. Weerasekera, S. Al Rashid, L. A. Ward, S. D. Der, and V. L. Chan. 2004. FlaC, a protein of Campylobacter jejuni TGH9011 (ATCC 43431) secreted through the flagellar apparatus, binds epithelial cells and influences cell invasion. Mol. Microbiol. 53:541-553.
85. Steinert, M., M. Flugel, M. Schuppler, J. H. Helbig, A. Supriyono, P. Proksch, and P. C. Luck. 2001. The Lly protein is essential for p-hydroxyphenylpyruvate dioxygenase activity in Legionella pneumophila. FEMS Microbiol. Lett. 203:41-47.
86. Steinert, M., U. Hentschel, and J. Hacker. 2002. Legionella pneumophila: an aquatic microbe goes astray. FEMS Microbiol. Rev. 26:149-162.
87. Stone, B. J., and Y. Abu Kwaik. 1999. Natural competence for DNA transformation by Legionella pneumophila and its association with expression of type IV pili. J. Bacteriol. 181:1395-1402.
88. Swanson, M. S., and B. K. Hammer. 2000. Legionella pneumophila pathogenesis: a fateful journey from amoebae to macrophages. Annu. Rev. Microbiol. 54:567-613.
89. Swanson, M. S., and R. R. Isberg. 1995. Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect. Immun. 63:3609-3620.
90. Tasteyre, A., M. C. Bare, A. Collignon, H. Boureau, and T. Karjalainen. 2001. Role of FliC and FliD flagellar proteins of Clostridium difficile in adherence and gut colonization. Infect. Immun. 69:7937-7940.
91. Thomas, J., G. P. Stafford, and C. Hughes. 2004. Docking of cytosolic chaperone-substrate complexes at the membrane ATPase during flagellar type III protein export. Proc. Natl. Acad. Sci. USA 101:3945-3950.
92. Tweten, R. K., M. W. Parker, and A. E. Johnson. 2001. The cholesterol-dependent cytolysins. Curr. Top. Microbiol. Immunol. 257:15-33.
93. Vogel, J. P., H. L. Andrews, S. K. Wong, and R. R. Isberg. 1998. Conjugative transfer by the virulence system of Legionella pneumophila. Science 279:873-876.
94. Vogel, J. P., C. Roy, and R. R. Isberg. 1996. Use of salt to isolate Legionella pneumophila mutants unable to replicate in macrophages. Ann. N. Y. Acad. Sci. 797:271-272.
95. Warren, W. J., and R. D. Miller. 1979. Growth of Legionnaires' disease bacterium (Legionella pneumophila) in chemically defined medium. J. Clin. Microbiol. 10:50-55.
96. Watarai, M., I. Derre, J. Kirby, J. D. Growney, W. F. Dietrich, and R. R. Isberg. 2001. Legionella pneumophila is internalized by a macropinocytotic uptake pathway controlled by the Dot/Icm system and the mouse Lgn1 locus. J. Exp. Med. 194:1081-1096.
97. Wiater, L. A., A. B. Sadosky, and H. A. Shuman. 1994. Mutagenesis of Legionella pneumophila using Tn903 dlllacZ: identification of a growth-phase-regulated pigmentation gene. Mol. Microbiol. 11:641-653.
98. Wintermeyer, E., M. Flugel, M. Ott, M. Steinert, V. Rdest, K. H. Mann, and J. Hacker. 1994. Sequence determination and mutational analysis of the lly locus of Legionella pneumophila. Infect. Immun. 62:1109-1117.
99. Wintermeyer, E., U. Rdest, B. Ludwig, A. Debes, and J. Hacker. 1991. Characterization of legiolysin (lly), responsible for hemolytic activity, colour production, and fluorescence of Legionella pneumophila. Mol. Microbiol. 5:1135-1143.
100. Young, G. M., D. H. Schmiel, and V. L. Miller. 1999. A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc. Natl. Acad. Sci. USA 96:6456-6461.
101. Zahringer, U., Y. A. Knirel, B. Lindner, J. H. Helbig, A. Sonesson, R. Marre, and E. T. Rietschel. 1995. The lipopolysaccharide of Legionella pneumophila serogroup 1 (strain Philadelphia 1): chemical structure and biological significance. Prog. Clin. Biol. Res. 392:113-139.
102. Zuberi, A. R., C. W. Ying, H. M. Parker, and G. W. Ordal. 1990. Transposon Tn917lacZ mutagenesis of Bacillus subtilis: identification of two new loci required for motility and chemotaxis. J. Bacteriol. 172:6841-6848.
103. Zusman, T., O. Gal-Mor, and G. Segal. 2002. Characterization of a Legionella pneumophila relA insertion mutant and roles of RelA and RpoS in virulence gene expression. J. Bacteriol. 184:67-75.