Virulence properties of the Legionella pneumophila cell envelope

Frontiers in Microbiology

Volumn 2, Issue APR, 2011, Pages

  Shevchuk, Olga ^a   Jäger, Jens ^a   Steinert, Michael ^a  

^a TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

Bacterial envelope; Legionella pneumophila; LPS; Membrane proteins; Outer membrane vesicles; Phospholipids

Indexed keywords

EID: 84866009995     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2011.00074     Document Type: Article

References (109)

1. Akira, S., Takeda, K., and Kaisho, T. (2001). Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2, 675-680.
2. Albers, U., Tiaden, A., Spirig, T., Al Alam, D., Goyert, S. M., Gangloff, S. C., and Hilbi, H. (2007). Expression of Legionella pneumophila paralogous lipid A biosynthesis genes under different growth conditions. Microbiology 153, 3817-3829.
3. Albert-Weissenberger, C., Sahr, T., Sismeiro, O., Hacker, J., Heuner, K., and Buchrieser, C. (2010). Control of flagellar gene regulation in Legionella pneumophila and its relation to growth phase. J. Bacteriol. 192, 446-455.
4. Al-Khodor, S., Kalachikov, S., Morozova, I., Price, C. T., and Abu Kwaik, Y. (2009). The PmrA/PmrB two-component system of Legionella pneumophila is a global regulator required for intracellular replication within macrophages and protozoa. Infect. Immun. 77, 374-386.
5. Amano, K., and Williams, J. C. (1983). Peptidoglycan of Legionella pneumophila: apparent resistance to lysozyme hydrolysis correlates with a high degree of peptide cross-linking. J. Bacteriol. 153, 520-526.
6. Aragon, V., Kurtz, S., Flieger, A., Neumeister, B., and Cianciotto, N. P. (2000). Secreted enzymatic activities of wild-type and pilD-deficient Legionella pneumophila. Infect. Immun. 68, 1855-1863.
7. Bandyopadhyay, P., Byrne, B., Chan, Y., Swanson, M. S., and Steinman, H. M. (2003). Legionella pneumophila catalase-peroxidases are required for proper trafficking and growth in primary macrophages. Infect. Immun. 71, 4526-4535.
8. Banerji, S., Aurass, P., and Flieger, A. (2008). The manifold phospholipases A of Legionella pneumophila - identification, export, regulation, and their link to bacterial virulence. Int. J. Med. Microbiol. 298, 169-181.
9. Barker, J., Lambert, P. A., and Brown, M. R. (1993). Influence of intra-amoebic and other growth conditions on the surface properties of Legionella pneumophila. Infect. Immun. 61, 3503-3510.
10. Bellinger-Kawahara, C., and Horwitz, M. A. (1990). Complement component C3 fixes selectively to the major outer membrane protein (MOMP) of Legionella pneumophila and mediates phagocytosis of liposome-MOMP complexes by human monocytes. J. Exp. Med. 172, 1201-1210.
11. Bishop, R. E., Gibbons, H. S., Guina, T., Trent, M. S., Miller, S. I., and Raetz, C. R. (2000). Transfer of palmitate from phospholipids to lipid A in outer membranes of Gram-negative bacteria. EMBO J. 19, 5071-5080.
12. Bruggemann, H., Hagman, A., Jules, M., Sismeiro, O., Dillies, M. A., Gouyette, C., Kunst, F., Steinert, M., Heuner, K., Coppee, J. Y., and Buchrieser, C. (2006). Virulence strategies for infecting phagocytes deduced from the in vivo transcriptional program of Legionella pneumophila. Cell. Microbiol. 8, 1228-1240.
13. Byrne, B., and Swanson, M. S. (1998). Expression of Legionella pneu-mophila virulence traits in response to growth conditions. Infect. Immun. 66, 3029-3034.
14. Cazalet, C., Jarraud, S., Ghavi-Helm, Y., Kunst, F., Glaser, P., Etienne, J., and Buchrieser, C. (2008). Multigenome analysis identifies a worldwide distributed epidemic Legionella pneumophila clone that emerged within a highly diverse species. Genome Res. 18, 431-441.
15. Cianciotto, N. P. (2007). Iron acquisition by Legionella pneumophila. Biometals 20, 323-331.
16. Cianciotto, N. P. (2009). Many substrates and functions of type II secretion: lessons learned from Legionella pneumophila. Future Microbiol. 4, 797-805.
17. Ciesielski, C. A., Blaser, M. J., and Wang, W. L. (1986). Serogroup specificity of Legionella pneumophila is related to lipopolysaccharide characteristics. Infect Immun. 51, 397-404.
18. Cirillo, S. L., Lum, J., and Cirillo, J. D. (2000). Identification of novel loci involved in entry by Legionella pneumophila. Microbiology 146(Pt 6), 1345-1359.
19. Conover, G. M., Martinez-Morales, F., Heidtman, M. I., Luo, Z. Q., Tang, M., Chen, C., Geiger, O., and Isberg, R. R. (2008). Phosphatidylcholine synthesis is required for optimal function of Legionella pneumophila virulence determinants. Cell. Microbiol. 10, 514-528.
20. Debroy, S., Aragon, V., Kurtz, S., and Cianciotto, N. P. (2006). Legionella pneumophila Mip, a surface-exposed peptidylproline cis-trans-isomerase, promotes the presence of phospholipase C-like activity in culture supernatants. Infect. Immun. 74, 5152-5160.
21. Doerrler, W. T., Gibbons, H. S., and Raetz, C. R. (2004). MsbA-dependent translocation of lipids across the inner membrane of Escherichia coli. J. Biol. Chem. 279, 45102-45109.
22. Doleans, A., Aurell, H., Reyrolle, M., Lina, G., Freney, J., Vandenesch, F., Etienne, J., and Jarraud, S. (2004). Clinical and environmental distributions of Legionella strains in France are different. J. Clin. Microbiol. 42, 458-460.
23. Ellis, T. N., and Kuehn, M. J. (2010). Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol. Mol. Biol. Rev. 74, 81-94.
24. Faulkner, G., and Garduño, R. A. (2002). Ultrastructural analysis of differentiation in Legionella pneumophila. J. Bacteriol. 184, 7025-7041.
25. Fernandez-Moreira, E., Helbig, J. H., and Swanson, M. S. (2006). Membrane vesicles shed by Legionella pneumophila inhibit fusion of phagosomes with lysosomes. Infect. Immun. 74, 3285-3295.
26. Finnerty, W. R., Makula, R. A., and Feeley, J. C. (1979). Cellular lipids of the Legionnaires' disease bacterium. Ann. Intern. Med. 90, 631-634.
27. Gabay, J. E., Blake, M., Niles, W. D., and Horwitz, M. A. (1985). Purification of Legionella pneumophila major outer membrane protein and demonstration that it is a porin. J. Bacteriol. 162, 85-91.
28. Gabay, J. E., and Horwitz, M. A. (1985). Isolation and characterization of the cytoplasmic and outer membranes of the Legionnaires' disease bacterium (Legionella pneumophila). J. Exp. Med. 161, 409-422.
29. Gabay, J. E., Horwitz, M. A., and Cohn, Z. A. (1986). Phagosome-lysosome fusion. Biochem. Soc. Trans. 14, 256-257.
30. Galka, F., Wai, S. N., Kusch, H., Engelmann, S., Hecker, M., Schmeck, B., Hippenstiel, S., Uhlin, B. E., and Steinert, M. (2008). Proteomic characterization of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles. Infect. Immun. 76, 1825-1836.
31. Garduño, R. A., Garduño, E., and Hoffman, P. S. (1998). Surface-associated hsp60 chaperonin of Legionella pneumophila mediates invasion in a HeLa cell model. Infect. Immun. 66, 4602-4610.
32. Gibbons, H. S., Kalb, S. R., Cotter, R. J., and Raetz, C. R. (2005). Role of Mg2 + and pH in the modification of Salmonella lipid A after endocytosis by macrophage tumour cells. Mol. Microbiol. 55, 425-440.
33. Girard, R., Pedron, T., Uematsu, S., Balloy, V., Chignard, M., Akira, S., and Chaby, R. (2003). Lipopolysaccharides from Legionella and Rhizobium stimulate mouse bone marrow granulocytes via Toll-like receptor 2. J. Cell. Sci. 116, 293-302.
34. Gosselin, F., Duval, J. F., Simonet, J., Ginevra, C., Gaboriaud, F., Jarraud, S., and Mathieu, L. (2010). Impact of the virulence-associated MAb3/1 epitope on the physicochemical surface properties of Legionella pneumophila sg1: an issue to explain infection potential? Colloids Surf. B Biointerfaces 82, 283-290.
35. Gunn, J. S., Lim, K. B., Krueger, J., Kim, K., Guo, L., Hackett, M., and Miller, S. I. (1998). PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol. Microbiol. 27, 1171-1182.
36. Guo, L., Lim, K. B., Gunn, J. S., Bainbridge, B., Darveau, R. P., Hackett, M., and Miller, S. I. (1997). Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ. Science 276, 250-253.
37. Guo, L., Lim, K. B., Poduje, C. M., Daniel, M., Gunn, J. S., Hackett, M., and Miller, S. I. (1998). Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 95, 189-198.
38. Hasegawa, M., Yang, K., Hashimoto, M., Park, J. H., Kim, Y. G., Fujimoto, Y., Nunez, G., Fukase, K., and Inohara, N. (2006). Differential release and distribution of Nod1 and Nod2 immunostimulatory molecules among bacterial species and environments. J. Biol. Chem. 281, 29054-29063.
39. Hawn, T. R., Verbon, A., Janer, M., Zhao, L. P., Beutler, B., and Aderem, A. (2005). Toll-like receptor 4 polymorphisms are associated with resistance to Legionnaires' disease. Proc. Natl. Acad. Sci. U.S.A. 102, 2487-2489.
40. Helbig, J. H., and Amemura-Maekawa, J. (2009). Serotyping of Legionella pneumophila and epidemiological investigations. Nowa Medycyna 16, 69-75.
41. Helbig, J. H., Bernander, S., Castellani Pastoris, M., Etienne, J., Gaia, V., Lauwers, S., Lindsay, D., Lück, P. C., Marques, T., Mentula, S., Peeters, M. F., Pelaz, C., Struelens, M., Uldum, S. A., Wewalka, G., and Harrison, T. G. (2002). Pan-European study on culture-proven Legionnaires' disease: distribution of Legionella pneumophila serogroups and monoclonal subgroups. Eur. J. Clin. Microbiol. Infect. Dis. 21, 710-716.
42. Helbig, J. H., Lück, P. C., Knirel, Y. A., Witzleb, W., and Zähringer, U. (1995). Molecular characterization of a virulence-associated epitope on the lipopolysaccharide of Legionella pneumophila serogroup 1. Epidemiol. Infect. 115, 71-78.
43. Heuner, K., and Albert-Weissenberger, C. (2008). Legionella Molecular Biology. Norfolk: Caister Academic Press. Heuner, K., and 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.
44. Hindahl, M. S., and Iglewski, B. H. (1984). Isolation and characterization of the Legionella pneumophila outer membrane. J. Bacteriol. 159, 107-113.
45. Hoffman, P. S., and Garduño, R. A. (1999). Surface-associated heat shock proteins of Legionella pneumophila and Helicobacter pylori: roles in pathogenesis and immunity. Infect. Dis. Obstet. Gynecol. 7, 58-63.
46. Hovel-Miner, G., Pampou, S., Faucher, S. P., Clarke, M., Morozova, I., Morozov, P., Russo, J. J., Shuman, H. A., and Kalachikov, S. (2009). SigmaS controls multiple pathways associated with intracellular multiplication of Legionella pneumophila. J. Bacteriol. 191, 2461-2473.
47. Hubber, A., and Roy, C. R. (2010). Modulation of host cell function by Legionella pneumophila type IV effectors. Annu. Rev. Cell Dev. Biol. 26, 261-283.
48. Huston, W. M., Naylor, J., Cianciotto, N. P., Jennings, M. P., and McEwan, A. G. (2008). Functional analysis of the multi-copper oxidase from Legionella pneumophila. Microbes Infect. 10, 497-503.
49. Kawasaki, K., Ernst, R. K., and Miller, S. I. (2004). 3-O-deacylation of lipid A by PagL, a PhoP/PhoQ-regulated deacylase of Salmonella typhimurium, modulates signaling through Toll-like receptor 4. J. Biol. Chem. 279, 20044-20048.
50. Khemiri, A., Galland, A., Vaudry, D., Chan Tchi Song, P., Vaudry, H., Jouenne, T., and Cosette, P. (2008). Outer-membrane proteomic maps and surface-exposed proteins of Legionella pneumophila using cellular fractionation and fluorescent labelling. Anal. Bioanal. Chem. 390, 1861-1871.
51. Kim, M. J., Sohn, J. W., Park, D. W., Park, S. C., and Chun, B. C. (2003). Characterization of a lipoprotein common to Legionella species as a urinary broad-spectrum antigen for diagnosis of Legionnaires' disease. J. Clin. Microbiol. 41, 2974-2979.
52. Knirel, Y. A., Moll, H., Helbig, J. H., and Zähringer, U. (1997). Chemical characterization of a new 5,7-diamino-3,5,7,9-tetradeoxynonulosonic acid released by mild acid hydrolysis of the Legionella pneumophila serogroup 1 lipopolysaccharide. Carbohydr. Res. 304, 77-79.
53. Knirel, Y. A., Moll, H., and Zähringer, U. (1996). Structural study of a highly O-acetylated core of Legionella pneumophila serogroup 1 lipopolysaccharide. Carbohydr. Res. 293, 223-234.
54. Knirel, Y. A., Rietschel, E. T., Marre, R., and Zähringer, U. (1994). The structure of the O-specific chain of Legionella pneumophila serogroup 1 lipopolysaccharide. Eur. J. Biochem. 221, 239-245.
55. Kooistra, O., Herfurth, L., Lüneberg, E., Frosch, M., Peters, T., and Zähringer, U. (2002a). Epitope mapping of the O-chain polysaccharide of Legionella pneumophila serogroup 1 lipopolysaccharide by saturation-transfer-difference NMR spectroscopy. Eur. J. Biochem. 269, 573-582.
56. Kooistra, O., Lüneberg, E., Knirel, Y. A., Frosch, M., and Zähringer, U. (2002b). N-methylation in polylegionaminic acid is associated with the phase-variable epitope of Legionella pneumophila serogroup 1 lipopolysaccharide. Identification of 5-(N,N-dimethylacetimidoyl)amino and 5-acetimidoyl(N-methyl)amino-7-acetamido-3,5,7,9-tetradeoxynon-2-ulosonic acid in the O-chain polysaccharide. Eur. J. Biochem. 269, 560-572.
57. Krinos, C., High, A. S., and Rodgers, F. G. (1999). Role of the 25 kDa major outer membrane protein of Legionella pneumophila in attachment to U-937 cells and its potential as a virulence factor for chick embryos. J. Appl. Microbiol. 86, 237-244.
58. Lammertyn, E., and Anne, J. (2004). Protein secretion in Legionella pneumophila and its relation to virulence. FEMS Microbiol. Lett. 238, 273-279.
59. Liles, M. R., Viswanathan, V. K., and Cianciotto, N. P. (1998). Identification and temperature regulation of Legionella pneumophila genes involved in type IV pilus biogenesis and type II protein secretion. Infect. Immun. 66, 1776-1782.
60. Lucas, C. E., Brown, E., and Fields, B. S. (2006). Type IV pili and type II secretion play a limited role in Legionella pneumophila biofilm colonization and retention. Microbiology 152, 3569-3573.
61. Lüneberg, E., Mayer, B., Daryab, N., Kooistra, O., Zähringer, U., Rohde, M., Swanson, J., and Frosch, M. (2001). Chromosomal insertion and excision of a 30 kb unstable genetic element is responsible for phase variation of lipopolysaccharide and other virulence determinants in Legionella pneumophila. Mol. Microbiol. 39, 1259-1271.
62. Lüneberg, E., Zähringer, U., Knirel, Y. A., Steinmann, D., Hartmann, M., Steinmetz, I., Rohde, M., Köhl, J., and Frosch, M. (1998). Phase-variable expression of lipopolysaccharide contributes to the virulence of Legionella pneumophila. J. Exp. Med. 188, 49-60.
63. Lüneberg, E., Zetzmann, N., Alber, D., Knirel, Y. A., Kooistra, O., Zähringer, U., and Frosch, M. (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.
64. Ma, B., Reynolds, C. M., and Raetz, C. R. (2008). Periplasmic orientation of nascent lipid A in the inner membrane of an Escherichia coli LptA mutant. Proc. Natl. Acad. Sci. U.S.A. 105, 13823-13828.
65. Matthews, M., and Roy, C. R. (2000). Identification and subcellular localization of the Legionella pneumophila IcmX protein: a factor essential for establishment of a replicative organelle in eukaryotic host cells. Infect. Immun. 68, 3971-3982.
66. Merault, N., Rusniok, C., Jarraud, S., Gomez-Valero, L., Cazalet, C., Marin, M., Brachet, E., Aegerter, P., Gaillard, J. L., Etienne, J., Herrmann, J. L., DELPH-I Study Group, Lawrence, C., and Buchrieser, C. (2010). A specific real-time PCR for simultaneous detection and identification of Legionella pneumophila serogroup 1 in water and clinical samples. Appl. Environ. Microbiol. 77, 1708-1717.
67. Miller, S. I., Kukral, A. M., and Mekalanos, J. J. (1989). A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. Proc. Natl. Acad. Sci. U.S.A. 86, 5054-5058.
68. Mintz, C. S., Arnold, P. I., Johnson, W., and Schultz, D. R. (1995). Antibody-independent binding of complement component C1q by Legionella pneumophila. Infect. Immun. 63, 4939-4943.
69. Mintz, C. S., Schultz, D. R., Arnold, P. I., and Johnson, W. (1992). Legionella pneumophila lipopolysaccharide activates the classical complement pathway. Infect. Immun. 60, 2769-2776.
70. Moll, H., Knirel, Y. A., Helbig, J. H., and Zähringer, U. (1997). Identification of an alpha-D-Manp-(1 → 8)-Kdo disaccharide in the inner core region and the structure of the complete core region of the Legionella pneumophila serogroup 1 lipopolysaccharide. Carbohydr. Res. 304, 91-95.
71. Moll, H., Sonesson, A., Jantzen, E., Marre, R., and Zähringer, U. (1992). Identification of 27-oxo-octacosanoic acid and heptacosane-1,27-dioic acid in Legionella pneumophila. FEMS Microbiol. Lett. 76, 1-6.
72. Molofsky, A. B., Byrne, B. G., Whitfield, N. N., Madigan, C. A., Fuse, E. T., Tateda, K., and Swanson, M. S. (2006). Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J. Exp. Med. 203, 1093-1104.
73. Molofsky, A. B., Shetron-Rama, L. M., and Swanson, M. S. (2005). Components of the Legionella pneumophila flagellar regulon contribute to multiple virulence traits, including lysosome avoidance and macrophage death. Infect. Immun. 73, 5720-5734.
74. Nakano, N., Kubori, T., Kinoshita, M., Imada, K., and Nagai, H. (2010). Crystal structure of Legionella DotD: insights into the relationship between type IVB and type II/III secretion systems. PLoS Pathog. 6, e1001129. doi: 10.1371/journal.ppat.1001129
75. Napoli, C., Fasano, F., Iatta, R., Barbuti, G., Cuna, T., and Montagna, M. T. (2010). Legionella spp. and legionellosis in southeastern Italy: disease epidemiology and environmental surveillance in community and health care facilities. BMC Public Health 10, 660. doi: 10.1186/1471-2458-10-660
76. Neumeister, B., Faigle, M., Sommer, M., Zähringer, U., Stelter, F., Menzel, R., Schütt, C., and Northoff, H. (1998). Low endotoxic potential of Legionella pneumophila lipopolysaccharide due to failure of interaction with the monocyte lipopolysaccharide receptor CD14. Infect. Immun. 66, 4151-4157.
77. Newton, H. J., Sansom, F. M., Dao, J., Cazalet, C., Bruggemann, H., Albert-Weissenberger, C., Buchrieser, C., Cianciotto, N. P., and Hartland, E. L. (2008). Significant role for ladC in initiation of Legionella pneumophila infection. Infect. Immun. 76, 3075-3085.
78. Ninio, S., and Roy, C. R. (2007). Effector proteins translocated by Legionella pneumophila: strength in numbers. Trends Microbiol. 15, 372-380.
79. Palusinska-Szysz, M., Janczarek, M., Kalitynski, R., Dawidowicz, A. L., and Russa, R. (2011). Legionella bozemanae synthesizes phosphatidylcholine from exogenous choline. Microbiol. Res. 166, 87-98.
80. Palusinska-Szysz, M., and Russa, R. (2009). Chemical structure and biological significance of lipopolysaccharide from Legionella. Recent Pat. Antiinfect. Drug. Discov. 4, 96-107.
81. Petermann, N., Hansen, G., Schmidt, C. L., and Hilgenfeld, R. (2010). Structure of the GTPase and GDI domains of FeoB, the ferrous iron transporter of Legionella pneumophila. FEBS Lett. 584, 733-738.
82. Rasis, M., and 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.
83. Ren, T., Zamboni, D. S., Roy, C. R., Dietrich, W. F., and Vance, R. E. (2006). Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog. 2, e18. doi: 10.1371/journal.ppat.0020018
84. Riboldi-Tunnicliffe, A., Konig, B., Jessen, S., Weiss, M. S., Rahfeld, J., Hacker, J., Fischer, G., and Hilgenfeld, R. (2001). Crystal structure of Mip, a prolylisomerase from Legionella pneumophila. Nat. Struct. Biol. 8, 779-783.
85. Robey, M., and Cianciotto, N. P. (2002). Legionella pneumophila feoAB promotes ferrous iron uptake and intracellular infection. Infect. Immun. 70, 5659-5669.
86. Robey, M., O'Connell, W., and Cianciotto, N. P. (2001). Identification of Legionella pneumophila rcp, a pagP-like gene that confers resistance to cationic antimicrobial peptides and promotes intracellular infection. Infect. Immun. 69, 4276-4286.
87. Rodgers, F. G., and Davey, M. R. (1982). Ultrastructure of the cell envelope layers and surface details of Legionella pneumophila. J. Gen. Microbiol. 128, 1547-1557.
88. Rodgers, F. G, Greaves, P. W., Macrae, A. D., and Lewis, M. J. (1980). Electron microscopic evidence of flagella and pili on Legionella pneumophila. J. Clin. Pathol. 33, 1184-1188.
89. Rogers, J., Hakki, A., Perkins, I., Newton, C., Widen, R., Burdash, N., Klein, T., and Friedman, H. (2007). Legionella pneumophila infection up-regulates dendritic cell Toll-like receptor 2 (TLR2)/TLR4 expression and key maturation markers. Infect. Immun. 75, 3205-3208.
90. Rossier, O., and Cianciotto, N. P. (2005). The Legionella pneumophila tatB gene facilitates secretion of phospholipase C, growth under iron-limiting conditions, and intracellular infection. Infect. Immun. 73, 2020-2032.
91. Sankaran, K., and Wu, H. C. (1994). Lipid modification of bacterial prolipoprotein. Transfer of diacylglyceryl moiety from phosphatidylglycerol. J. Biol. Chem. 269, 19701-19706.
92. Sawada, K., Ariki, S., Kojima, T., Saito, A., Yamazoe, M., Nishitani, C., Shimizu, T., Takahashi, M., Mitsuzawa, H., Yokota, S., Sawada, N., Fujii, N., Takahashi, H., and Kuroki, Y. (2010). Pulmonary collectins protect macrophages against pore-forming activity of Legionella pneumophila and suppress its intracellular growth. J. Biol. Chem. 285, 8434-8443.
93. Schnell, S., and Steinman, H. M. (1995). Function and stationary-phase induction of periplasmic copper-zinc superoxide dismutase and catalase/ peroxidase in Caulobacter crescentus. J. Bacteriol. 177, 5924-5929.
94. Schunder, E., Adam, P., Higa, F., Remer, K. A., Lorenz, U., Bender, J., Schulz, T., Flieger, A., Steinert, M., and Heuner, K. (2010). Phospholipase PlaB is a new virulence factor of Legionella pneumophila. Int. J. Med. Microbiol. 300, 313-323.
95. Seeger, E. M., Thuma, M., Fernandez-Moreira, E., Jacobs, E., Schmitz, M., and Helbig, J. H. (2010). Lipopolysaccharide of Legionella pneumophila shed in a liquid culture as a nonvesicular fraction arrests phagosome maturation in amoeba and monocytic host cells. FEMS Microbiol. Lett. 307, 113-119.
96. Shim, H. K., Kim, J. Y., Kim, M. J., Sim, H. S., Park, D. W., Sohn, J. W., and Kim, M. J. (2009). Legionella lipoprotein activates toll-like receptor 2 and induces cytokine production and expression of costimulatory molecules in peri-toneal macrophages. Exp. Mol. Med. 41, 687-694.
97. Silhavy, T. J., Kahne, D., and Walker, S. (2010). The bacterial cell envelope. Cold Spring Harb. Perspect. Biol. 2, a000414.
98. Soderberg, M. A., and Cianciotto, N. P. (2010). Mediators of lipid A modification, RNA degradation, and central intermediary metabolism facilitate the growth of Legionella pneumophila at low temperatures. Curr. Microbiol. 60, 59-65.
99. Sohlenkamp, C., Lopez-Lara, I. M., and Geiger, O. (2003). Biosynthesis of phosphatidylcholine in bacteria. Prog. Lipid Res. 42, 115-162.
100. St John, G., and Steinman, H. M. (1996). Periplasmic copper-zinc superoxide dismutase of Legionella pneumophila: role in stationary-phase survival. J. Bacteriol. 178, 1578-1584.
101. Stone, B. J., and 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 mam-malian and protozoan cells. Infect. Immun. 66, 1768-1775.
102. Stone, B. J., and Kwaik, Y. A. (1999). Natural competence for DNA transformation by Legionella pneumophila and its association with expression of type IV pili. J. Bacteriol. 181, 1395-1402.
103. Vandersmissen, L., De Buck, E., Saels, V., Coil, D. A., and Anne, J. (2010). A Legionella pneumophila collagen-like protein encoded by a gene with a variable number of tandem repeats is involved in the adherence and invasion of host cells. FEMS Microbiol. Lett. 306, 168-176.
104. Verdon, J., Labanowski, J., Sahr, T., Ferreira, T., Lacombe, C., Buchrieser, C., Berjeaud, J. M., and Héchard, Y. (2011). Fatty acid composition modulates sensitivity of Legionella pneumophila to warnericin RK, an antimicrobial peptide. Biochim. Biophys. Acta. 1808, 1146-1153.
105. Viswanathan, V. K., Edelstein, P. H., Pope, C. D., and Cianciotto, N. P. (2000). The Legionella pneumophila iraAB locus is required for iron assimilation, intracellular infection, and virulence. Infect. Immun. 68, 1069-1079.
106. Wagner, C., Khan, A. S., Kamphausen, T., Schmausser, B., Ünal, C., Lorenz, U., Fischer, G., Hacker, J., and Steinert, M. (2007). Collagen binding protein Mip enables Legionella pneumophila to transmigrate through a barrier of NCI-H292 lung epithelial cells and extracellular matrix. Cell. Microbiol. 9, 450-462.
107. Wang, X., and Quinn, P. J. (2010). Lipopolysaccharide: biosynthetic pathway and structure modification. Prog. Lipid Res. 49, 97-107.
108. Yerushalmi, G., Zusman, T., and Segal, G. (2005). Additive effect on intracellular growth by Legionella pneumophila Icm/Dot proteins containing a lipobox motif. Infect. Immun. 73, 7578-7587.
109. Zähringer, U., Knirel, Y. A., Lindner, B., Helbig, J. H., Sonesson, A., Marre, R., and Rietschel, E. T. (1995). The lipopolysaccharide of Legionella pneumophila serogroup 1 (strain Philadelphia 1): chemical structure and biological significance. Prog. Clin. Biol. Res. 392, 113-139.