Skip to main content

Type II Secretion and Legionella Virulence

  • Chapter
  • First Online:
Molecular Mechanisms in Legionella Pathogenesis

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 376))

Abstract

Type II secretion (T2S) is one of six systems that can occur in Gram-negative bacteria for the purpose of secreting proteins into the extracellular milieu and/or into host cells. This chapter will describe the T2S system of Legionella pneumophila. Topics to be covered include the genetic basis of T2S in L. pneumophila, the numbers (>25), types, and novelties of Legionella proteins that are secreted via T2S, and the many ways in which T2S and its substrates promote L. pneumophila physiology, ecology, and virulence. Within the aquatic environment, T2S plays a major role in L. pneumophila intracellular infection of multiple types of (Acanthamoeba, Hartmannella, and Naegleria) amoebae. Within the mammalian host, T2S promotes bacterial persistence in lungs, intracellular infection of both macrophages and epithelial cells, and a dampening of the host innate immune response. In this context, T2S may represent a potential target for both industrial and biomedical application.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Amaro F, Gilbert JA, Owens S, Trimble W, Shuman HA (2012) Whole-genome sequence of the human pathogen Legionella pneumophila serogroup 12 strain 570-CO-H. J Bacteriol 194:1613–1614

    PubMed  CAS  Google Scholar 

  • Anand CM, Skinner AR, Malic A, Kurtz JB (1983) Interaction of L. pneumophila and a free living amoeba (Acanthamoeba palestinensis). J Hyg 91:167–178

    PubMed  CAS  Google Scholar 

  • Aragon V, Kurtz S, Flieger A, Neumeister B, Cianciotto NP (2000) Secreted enzymatic activities of wild-type and pilD-deficient Legionella pneumophila. Infect Immun 68:1855–1863

    PubMed  CAS  Google Scholar 

  • Aragon V, Kurtz S, Cianciotto NP (2001) Legionella pneumophila major acid phosphatase and its role in intracellular infection. Infect Immun 69:177–185

    PubMed  CAS  Google Scholar 

  • Aragon V, Rossier O, Cianciotto NP (2002) Legionella pneumophila genes that encode lipase and phospholipase C activities. Microbiology 148:2223–2231

    PubMed  CAS  Google Scholar 

  • Banerji S, Bewersdorff M, Hermes B, Cianciotto NP, Flieger A (2005) Characterization of the major secreted zinc metalloprotease- dependent glycerophospholipid:cholesterol acyltransferase, PlaC, of Legionella pneumophila. Infect Immun 73:2899–2909

    PubMed  CAS  Google Scholar 

  • Barbaree JM, Fields BS, Feeley JC, Gorman GW, Martin WT (1986) Isolation of protozoa from water associated with a legionellosis outbreak and demonstration of intracellular multiplication of Legionella pneumophila. Appl Environ Microbiol 51:422–424

    PubMed  CAS  Google Scholar 

  • Baskerville A, Conlan JW, Ashworth LA, Dowsett AB (1986) Pulmonary damage caused by a protease from Legionella pneumophila. Br J Exp Pathol 67:527–536

    PubMed  CAS  Google Scholar 

  • Blanchard DK, Friedman H, Klein TW, Djeu JY (1989) Induction of interferon-gamma and tumor necrosis factor by Legionella pneumophila: augmentation of human neutrophil bactericidal activity. J Leukoc Biol 45:538–545

    PubMed  CAS  Google Scholar 

  • Blander SJ, Szeto L, Shuman HA, Horwitz MA (1990) An immunoprotective molecule, the major secretory protein of Legionella pneumophila, is not a virulence factor in a guinea pig model of Legionnaires’ disease. J Clin Invest 86:817–824

    PubMed  CAS  Google Scholar 

  • Brieland J, McClain M, Heath L, Chrisp C, Huffnagle G, LeGendre M, Hurley M, Fantone J, Engleberg C (1996) Coinoculation with Hartmannella vermiformis enhances replicative Legionella pneumophila lung infection in a murine model of Legionnaires’ disease. Infect Immun 64:2449–2456

    PubMed  CAS  Google Scholar 

  • Cazalet C, Rusniok C, Bruggemann 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

    PubMed  CAS  Google Scholar 

  • Chaudhuri S, Bruno JC, Alonzo F 3rd, Xayarath B, Cianciotto NP, Freitag NE (2010) Contribution of chitinases to Listeria monocytogenes pathogenesis. Appl Environ Microbiol 76:7302–7305

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Cianciotto NP (2005) Type II secretion: a protein secretion system for all seasons. Trends Microbiol 13:581–588

    PubMed  CAS  Google Scholar 

  • Cianciotto NP (2009) Many substrates and functions of type II protein secretion: Lessons learned from Legionella pneumophila. Future Microbiol 4:797–805

    PubMed  Google Scholar 

  • Cianciotto NP, Kim Stamos J, Kamp DW (1995) Infectivity of Legionella pneumophila mip mutant for alveolar epithelial cells. Curr Microbiol 30:247–250

    PubMed  CAS  Google Scholar 

  • Cirillo JD, Cirillo SLG, Yan L, Bermudez LE, Falkow S, Tompkins LS (1999) Intracellular growth in Acanthamoeba castellani affects monocyte entry mechanism and enhances virulence of Legionella pneumophila. Infect Immun 67:4427–4434

    PubMed  CAS  Google Scholar 

  • Conlan JW, Baskerville A, Ashworth LAE (1986) Separation of Legionella pneumophila proteases and purification of a protease which produces lesions like those of Legionnaires’ disease in guinea pig lung. J Gen Microbiol 132:1565–1574

    PubMed  CAS  Google Scholar 

  • Conlan JW, Williams A, Ashworth LA (1988) In vivo production of a tissue-destructive protease by Legionella pneumophila in the lungs of experimentally infected guinea-pigs. J Gen Microbiol 134:143–149

    PubMed  CAS  Google Scholar 

  • Costa J, d’Avo AF, da Costa MS, Verissimo A (2011) Molecular evolution of key genes for type II secretion in Legionella pneumophila. Environ Microbiol 14:2017–2033

    PubMed  Google Scholar 

  • D’Auria G, Jimenez-Hernandez N, Peris-Bondia F, Moya A, Latorre A (2010) Legionella pneumophila pangenome reveals strain-specific virulence factors. BMC Genomics 11:181

    PubMed  Google Scholar 

  • De Buck E, Lebeau I, Maes L, Geukens N, Meyen E, Van Mellaert L, Anne J, Lammertyn E (2004) A putative twin-arginine translocation pathway in Legionella pneumophila. Biochem Biophys Res Commun 317:654–661

    PubMed  Google Scholar 

  • De Buck E, Maes L, Meyen E, Van Mellaert L, Geukens N, Anne J, Lammertyn E (2005) Legionella pneumophila Philadelphia-1 tatB and tatC affect intracellular replication and biofilm formation. Biochem Biophys Res Commun 331:1413–1420

    PubMed  Google Scholar 

  • de Felipe KS, Glover RT, Charpentier X, Anderson OR, Reyes M, Pericone CD, Shuman HA (2008) Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog 4:e1000117

    PubMed  Google Scholar 

  • DebRoy S, Dao J, Soderberg M, Rossier O, Cianciotto NP (2006a) Legionella pneumophila type II secretome reveals unique exoproteins and a chitinase that promotes bacterial persistence in the lung. PNAS 103:19146–19151

    PubMed  CAS  Google Scholar 

  • DebRoy S, Aragon V, Kurtz S, Cianciotto NP (2006b) 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

    PubMed  CAS  Google Scholar 

  • Desvaux M, Hebraud M, Talon R, Henderson IR (2009) Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue. Trends Microbiol 17:139–145

    PubMed  CAS  Google Scholar 

  • Dey R, Bodennec J, Mameri MO, Pernin P (2009) Free-living freshwater amoebae differ in their susceptibility to the pathogenic bacterium Legionella pneumophila. FEMS Microbiol Lett 290:10–17

    PubMed  CAS  Google Scholar 

  • Duncan C, Prashar A, So J, Tang P, Low DE, Terebiznik M, Guyard C (2011) Lcl of Legionella pneumophila is an immunogenic GAG binding adhesin that promotes interactions with lung epithelial cells and plays a crucial role in biofilm formation. Infect Immun 79:2168–2181

    PubMed  CAS  Google Scholar 

  • Edelstein PH, Hu B, Higa F, Edelstein MA (2003) lvgA, a novel Legionella pneumophila virulence factor. Infect Immun 71:2394–2403

    PubMed  CAS  Google Scholar 

  • Fields BS (1996) The molecular ecology of legionellae. Trends Microbiol 4:286–290

    PubMed  CAS  Google Scholar 

  • Fields BS, Shotts EB Jr, Feeley JC, Gorman GW, Martin WT (1984) Proliferation of Legionella pneumophila as an intracellular parasite of the ciliated protozoan Tetrahymena pyriformis. Appl Environ Microbiol 47:467–471

    PubMed  CAS  Google Scholar 

  • Fields BS, Barbaree JM, Shotts EB Jr, Feeley JC, Morrill WE, Sanden GN, Dykstra MJ (1986) Comparison of guinea pig and protozoan models for determining virulence of Legionella species. Infect Immun 53:553–559

    PubMed  CAS  Google Scholar 

  • Fields BS, Sanden GN, Barbaree JM, Morrill WE, Wadowsky RM, White EH, Feeley JC (1989) Intracellular multiplication of Legionella pneumophila in amoebae isolated from hospital hot water tanks. Curr Microbiol 18:131–137

    Google Scholar 

  • Flieger A, Gong S, Faigle M, Stevanovic S, Cianciotto NP, Neumeister B (2001) Novel lysophospholipase A secreted by Legionella pneumophila. J Bacteriol 183:2121–2124

    PubMed  CAS  Google Scholar 

  • Flieger A, Neumeister B, Cianciotto NP (2002) Characterization of the gene encoding the major secreted lysophospholipase A of Legionella pneumophila and its role in detoxification of lysophosphatidylcholine. Infect Immun 70:6094–6106

    PubMed  CAS  Google Scholar 

  • Galka F, Wai SN, Kusch H, Engelmann S, Hecker M, Schmeck B, Hippenstiel S, Uhlin BE, Steinert M (2008) Proteomic characterization of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles. Infect Immun 76:1825–1836

    PubMed  CAS  Google Scholar 

  • George JR, Pine L, Reeves MW, Harrell WK (1980) Amino acid requirements of Legionella pneumophila. J Clin Microbiol 11:286–291

    PubMed  CAS  Google Scholar 

  • Geukens N, De Buck E, Meyen E, Maes L, Vranckx L, Van Mellaert L, Anne J, Lammertyn E (2006) The type II signal peptidase of Legionella pneumophila. Res Microbiol 157:836–841

    PubMed  CAS  Google Scholar 

  • Glockner G, Albert-Weissenberger C, Weinmann E, Jacobi S, Schunder E, Steinert M, Hacker J, Heuner K (2008) Identification and characterization of a new conjugation/type IVA secretion system (trb/tra) of Legionella pneumophila Corby localized on two mobile genomic islands. Int J Med Microbiol 298:411–428

    PubMed  Google Scholar 

  • Hagele S, Kohler R, Merkert H, Schleicher M, Hacker J, Steinert M (2000) Dictyostelium discoideum: a new host model system for intracellular pathogens of the genus Legionella. Cell Microbiol 2:165–171

    PubMed  CAS  Google Scholar 

  • Hales LM, Shuman HA (1999) Legionella pneumophila contains a type II general secretion pathway required for growth in amoebae as well as for secretion of the Msp protease. Infect Immun 67:3662–3666

    PubMed  CAS  Google Scholar 

  • Harada E, Iida K, Shiota S, Nakayama H, Yoshida S (2010) Glucose metabolism in Legionella pneumophila: dependence on the Entner-Doudoroff pathway and connection with intracellular bacterial growth. J Bacteriol 192:2892–2899

    PubMed  CAS  Google Scholar 

  • Harf C, Monteil H (1988) Interactions between free-living amoebae and Legionella in the environment. Water Sci Tech 20:235–239

    Google Scholar 

  • Henke M, Seidel KM (1986) Association between Legionella pneumophila and amoebae in water. Isr J Med Sci 22:690–695

    PubMed  CAS  Google Scholar 

  • Herrmann V, Eidner A, Rydzewski K, Bladel I, Jules M, Buchrieser C, Eisenreich W, Heuner K (2011) GamA is a eukaryotic-like glucoamylase responsible for glycogen- and starch-degrading activity of Legionella pneumophila. Int J Med Microbiol 301:133–139

    PubMed  CAS  Google Scholar 

  • Hindre T, Bruggemann H, Buchrieser C, Hechard Y (2008) Transcriptional profiling of Legionella pneumophila biofilm cells and the influence of iron on biofilm formation. Microbiology 154:30–41

    PubMed  CAS  Google Scholar 

  • Holden EP, Winkler HH, Wood DO, Leinbach ED (1984) Intracellular growth of Legionella pneumophila within Acanthamoeba castellanii Neff. Infect Immun 45:18–24

    PubMed  CAS  Google Scholar 

  • Huang B, Yuan Z, Heron BA, Gray BR, Eglezos S, Bates JR, Savill J (2006) Distribution of 19 major virulence genes in Legionella pneumophila serogroup 1 isolates from patients and water in Queensland, Australia. J Med Microbiol 55:993–997

    PubMed  CAS  Google Scholar 

  • James BW, Mauchline WS, Dennis PJ, Keevil CW (1997) A study of iron acquisition mechanisms of Legionella pneumophila grown in chemostat culture. Curr Microbiol 34:238–243

    PubMed  CAS  Google Scholar 

  • Kikuhara H, Ogawa M, Miyamoto H, Nikaido Y, Yoshida S (1994) Intracellular multiplication of Legionella pneumophila in Tetrahymena thermophila. Sangyo Ika Daigaku Zasshi 16:263–275

    PubMed  CAS  Google Scholar 

  • Korotkov KV, Sandkvist M, Hol WG (2012) The type II secretion system: biogenesis, molecular architecture and mechanism. Nat Rev Microbiol 10:336–351

    PubMed  CAS  Google Scholar 

  • Lammertyn E, Anne J (2004) Protein secretion in Legionella pneumophila and its relation to virulence. FEMS Microbiol Lett 238:273–279

    PubMed  CAS  Google Scholar 

  • Lammertyn E, Van Mellaert L, Meyen E, Lebeau I, De Buck E, Anne J, Geukens N (2004) Molecular and functional characterization of type I signal peptidase from Legionella pneumophila. Microbiology 150:1475–1483

    PubMed  CAS  Google Scholar 

  • Lang C, Rastew E, Hermes B, Siegbrecht E, Ahrends R, Banerji S, Flieger A (2012) Zinc metalloproteinase ProA directly activates Legionella pneumophila PlaC glycerophospholipid:cholesterol acyltransferase. J Biol Chem 287:23464–23478

    PubMed  CAS  Google Scholar 

  • Lee VT, Schneewind O (2001) Protein secretion and the pathogenesis of bacterial infections. Genes Dev 15:1725–1752

    PubMed  CAS  Google Scholar 

  • Liles MR, Viswanathan VK, Cianciotto NP (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

    PubMed  CAS  Google Scholar 

  • Liles MR, Edelstein PH, Cianciotto NP (1999) The prepilin peptidase is required for protein secretion by and the virulence of the intracellular pathogen Legionella pneumophila. Mol Microbiol 31:959–970

    PubMed  CAS  Google Scholar 

  • McCoy-Simandle K, Stewart CR, Dao J, Debroy S, Rossier O, Bryce PJ, Cianciotto NP (2011) Legionella pneumophila type II secretion dampens the cytokine response of infected macrophages and epithelia. Infect Immun 79:1984–1997

    PubMed  CAS  Google Scholar 

  • McHugh SL, Newton CA, Yamamoto Y, Klein TW, Friedman H (2000) Tumor necrosis factor induces resistance of macrophages to Legionella pneumophila infection. Proc Soc Exp Biol Med 224:191–196

    PubMed  CAS  Google Scholar 

  • Michel R, Muller KD, Amann R, Schmid EN (1998) Legionella-like slender rods multiplying within a strain of Acanthamoeba sp. isolated from drinking water. Parasitol Res 84:84–88

    PubMed  CAS  Google Scholar 

  • Miyamoto H, Taniguchi H, Yoshida S (2003) A simple qualitative assay for intracellular growth of Legionella pneumophila within Acanthamoeba culbertsoni. Kansenshogaku Zasshi 77:343–345

    PubMed  Google Scholar 

  • Moffat JF, Edelstein PH, Regula DP Jr, Cirillo JD, Tompkins LS (1994) Effects of an isogenic Zn-metalloprotease-deficient mutant of Legionella pneumophila in a guinea-pig pneumonia model. Mol Microbiol 12:693–705

    PubMed  CAS  Google Scholar 

  • Molmeret M, Jarraud S, Mori JP, Pernin P, Forey F, Reyrolle M, Vandenesch F, Etienne J, Farge P (2001) Different growth rates in amoeba of genotypically related environmental and clinical Legionella pneumophila strains isolated from a thermal spa. Epidemiol Infect 126:231–239

    PubMed  CAS  Google Scholar 

  • Molmeret M, Alli OA, Zink S, Flieger A, Cianciotto NP, Kwaik YA (2002) icmT is essential for pore formation-mediated egress of Legionella pneumophila from mammalian and protozoan cells. Infect Immun 70:69–78

    PubMed  CAS  Google Scholar 

  • Molmeret M, Santic M, Asare R, Carabeo RA, Abu Kwaik Y (2007) Rapid escape of the dot/icm mutants of Legionella pneumophila into the cytosol of mammalian and protozoan cells. Infect Immun 75:3290–3304

    PubMed  CAS  Google Scholar 

  • Newsome AL, Baker RL, Miller RD, Arnold RR (1985) Interactions between Naegleria fowleri and Legionella pneumophila. Infect Immun 50:449–452

    PubMed  CAS  Google Scholar 

  • Newton HJ, Sansom FM, Bennett-Wood V, Hartland EL (2006) Identification of Legionella pneumophila-specific genes by genomic subtractive hybridization with Legionella micdadei and identification of lpnE, a gene required for efficient host cell entry. Infect Immun 74:1683–1691

    PubMed  CAS  Google Scholar 

  • Newton HJ, Ang DK, van Driel IR, Hartland EL (2010) Molecular pathogenesis of infections caused by Legionella pneumophila. Clin Microbiol Rev 23:274–298

    PubMed  CAS  Google Scholar 

  • N’Guessan PD, Etouem MO, Schmeck B, Hocke AC, Scharf S, Vardarova K, Opitz B, Flieger A, Suttorp N, Hippenstiel S (2007) Legionella pneumophila-induced PKCa-, MAPK-, and NF-kB-dependent COX-2 expression in human lung epithelium. Am J Physiol Lung Cell Mol Physiol 292:L267–L277

    PubMed  Google Scholar 

  • O’Connor TJ, Boyd D, Dorer MS, Isberg RR (2012) Aggravating genetic interactions allow a solution to redundancy in a bacterial pathogen. Science 338:1440–1444

    PubMed  Google Scholar 

  • Opitz B, Vinzing M, van Laak V, Schmeck B, Heine G, Gunther S, Preissner R, Slevogt H, N’Guessan PD, Eitel J, Goldmann T, Flieger A, Suttorp N, Hippenstiel S (2006) Legionella pneumophila induced IFN-b in lung epithelial cells via IPS-1 and IRF3, which also control bacterial replication. J Biol Chem 281:36173–36179

    PubMed  CAS  Google Scholar 

  • Pearce MM, Cianciotto NP (2009) Legionella pneumophila secretes an endoglucanase that belongs to the family-5 of glycosyl hydrolases and is dependent upon type II secretion. FEMS Microbiol Lett 300:256–264

    PubMed  CAS  Google Scholar 

  • Pearce MM, Theodoropoulos N, Mandel MJ, Brown E, Reed KD, Cianciotto NP (2012) Legionella cardiaca sp. nov., isolated from a case of native valve endocarditis in a human heart. Int J Syst Evol Microbiol 62:2946–2954

    PubMed  CAS  Google Scholar 

  • Polesky AH, Ross JT, Falkow S, Tompkins LS (2001) Identification of Legionella pneumophila genes important for infection of amoebas by signature-tagged mutagenesis. Infect Immun 69:977–987

    PubMed  CAS  Google Scholar 

  • Rechnitzer C, Williams A, Wright JB, Dowsett AB, Milman N, Fitzgeorge RB (1992) Demonstration of the intracellular production of tissue-destructive protease by Legionella pneumophila multiplying within guinea-pig and human alveolar macrophages. J Gen Microbiol 138:1671–1677

    PubMed  CAS  Google Scholar 

  • Robson A, Collinson I (2006) The structure of the Sec complex and the problem of protein translocation. EMBO Rep 7:1099–1103

    PubMed  CAS  Google Scholar 

  • Rossier O, Cianciotto NP (2001) Type II protein secretion is a subset of the PilD-dependent processes that facilitate intracellular infection by Legionella pneumophila. Infect Immun 69:2092–2098

    PubMed  CAS  Google Scholar 

  • Rossier O, Cianciotto NP (2005) The Legionella pneumophila tatB gene facilitates secretion of phospholipase C, growth under iron-limiting conditions, and intracellular infection. Infect Immun 73:2020–2032

    PubMed  CAS  Google Scholar 

  • Rossier O, Starkenburg S, Cianciotto NP (2004) Legionella pneumophila type II protein secretion promotes virulence in the A/J mouse model of Legionnaires’ disease pneumonia. Infect Immun 72:310–321

    PubMed  CAS  Google Scholar 

  • Rossier O, Dao J, Cianciotto NP (2008) The type II secretion system of Legionella pneumophila elaborates two aminopeptidases as well as a metalloprotease that contributes to differential infection among protozoan hosts. Appl Environ Microbiol 74:753–761

    PubMed  CAS  Google Scholar 

  • Rossier O, Dao J, Cianciotto NP (2009) A type II-secreted ribonuclease of Legionella pneumophila facilitates optimal intracellular infection of Hartmannella vermiformis. Microbiology 155:882–890

    PubMed  CAS  Google Scholar 

  • Rowbotham TJ (1980) Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J Clin Pathol 33:1179–1183

    PubMed  CAS  Google Scholar 

  • Rowbotham TJ (1986) Current views on the relationships between amoebae, legionellae and man. Isr J Med Sci 22:678–689

    PubMed  CAS  Google Scholar 

  • Sargent F, Berks BC, Palmer T (2006) Pathfinders and trailblazers: a prokaryotic targeting system for transport of folded proteins. FEMS Microbiol Lett 254:198–207

    PubMed  CAS  Google Scholar 

  • Schmeck B, N’Guessan PD, Ollomang M, Lorenz J, Zahlten J, Opitz B, Flieger A, Suttorp N, Hippenstiel S (2007) Legionella pneumophila-induced NF-kB- and MAPK-dependent cytokine release by lung epithelial cells. Eur Respir J 29:25–33

    PubMed  CAS  Google Scholar 

  • Schroeder GN, Petty NK, Mousnier A, Harding CR, Vogrin AJ, Wee B, Fry NK, Harrison TG, Newton HJ, Thomson NR, Beatson SA, Dougan G, Hartland E, Frankel G (2010) The genome of Legionella pneumophila strain 130b contains a unique combination of type IV secretion systems and encodes novel Dot/Icm secretion system effector proteins. J Bacteriol 192:6001–6016

    PubMed  CAS  Google Scholar 

  • Shadrach WS, Rydzewski K, Laube U, Holland G, Ozel M, Kiderlen AF, Flieger A (2005) Balamuthia mandrillaris, free-living ameba and opportunistic agent of encephalitis, is a potential host for Legionella pneumophila bacteria. Appl Environ Microbiol 71:2244–2249

    PubMed  CAS  Google Scholar 

  • Skerrett SJ, Martin TR (1996) Roles for tumor necrosis factor alpha and nitric oxide in resistance of rat alveolar macrophages to Legionella pneumophila. Infect Immun 64:3236–3243

    PubMed  CAS  Google Scholar 

  • Söderberg MA, Cianciotto NP (2008) A Legionella pneumophila peptidyl-prolyl cis-trans isomerase present in culture supernatants is necessary for optimal growth at low temperatures. Appl Environ Microbiol 74:1634–1638

    PubMed  Google Scholar 

  • Söderberg MA, Rossier O, Cianciotto NP (2004) The type II protein secretion system of Legionella pneumophila promotes growth at low temperatures. J Bacteriol 186:3712–3720

    PubMed  Google Scholar 

  • Söderberg MA, Dao J, Starkenburg S, Cianciotto NP (2008) Importance of type II secretion for Legionella pneumophila survival in tap water and amoebae at low temperature. Appl Environ Microbiol 74:5583–5588

    PubMed  Google Scholar 

  • Solomon JM, Rupper A, Cardelli JA, Isberg RR (2000) Intracellular growth of Legionella pneumophila in Dictyostelium discoideum, a system for genetic analysis of host-pathogen interactions. Infect Immun 68:2939–2947

    PubMed  CAS  Google Scholar 

  • Stewart CR, Rossier O, Cianciotto NP (2009) Surface translocation by Legionella pneumophila: A form of sliding motility that is dependent upon type II protein secretion. J Bacteriol 191:1537–1546

    PubMed  CAS  Google Scholar 

  • Stewart CR, Burnside DM, Cianciotto NP (2011) The surfactant of Legionella pneumophila is secreted in a TolC-dependent manner and is antagonistic toward other Legionella species. J Bacteriol 193:5971–5984

    PubMed  CAS  Google Scholar 

  • Tyndall RL, Domingue EL (1982) Cocultivation of Legionella pneumophila and free-living amoebae. Appl Environ Microbiol 44:954–959

    PubMed  CAS  Google Scholar 

  • Tyson JY, Pearce MM, Vargas P, Bagchi S, Mulhern BJ, Cianciotto NP (2013) Multiple Legionella pneumophila type II secretion substrates, including an entirely novel protein, contribute to differential infection of the amoebae Acanthamoeba castellanii, Hartmannella vermiformis, and Naegleria lovaniensis. Infect Immun 81:1399–1410

    Google Scholar 

  • Vandersmissen L, De Buck E, Saels V, Coil DA, 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

    PubMed  CAS  Google Scholar 

  • Wadowsky RM, Wilson TM, Kapp NJ, West AJ, Kuchta JM, States SJ, Dowling JN, Yee RB (1991) Multiplication of Legionella spp. in tap water containing Hartmannella vermiformis. Appl Environ Microbiol 57:1950–1955

    PubMed  CAS  Google Scholar 

  • Williams A, Baskerville A, Dowsett AB, Conlan JW (1987) Immunocytochemical demonstration of the association between Legionella pneumophila, its tissue-destructive protease, and pulmonary lesions in experimental Legionnaires’ disease. J Pathol 153:257–264

    PubMed  CAS  Google Scholar 

  • Zink SD, Pedersen L, Cianciotto NP, Abu-Kwaik Y (2002) The Dot/Icm type IV secretion system of Legionella pneumophila is essential for the induction of apoptosis in human macrophages. Infect Immun 70:1657–1663

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nicholas P. Cianciotto .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Cianciotto, N.P. (2013). Type II Secretion and Legionella Virulence. In: Hilbi, H. (eds) Molecular Mechanisms in Legionella Pathogenesis. Current Topics in Microbiology and Immunology, vol 376. Springer, Berlin, Heidelberg. https://doi.org/10.1007/82_2013_339

Download citation

Publish with us

Policies and ethics