Cover

Microbial Pathogenomics

Editor(s): de Reuse H. (Paris) 
Bereswill S. (Berlin) 
Table of Contents
Vol. 6, No. , 2009
Section title: Paper
de Reuse H, Bereswill S (eds): Microbial Pathogenomics. Genome Dyn. Basel, Karger, 2009, vol 6, pp 170–186
(DOI:10.1159/000235770)

Legionella pneumophila – Host Interactions: Insights Gained from Comparative Genomics and Cell Biology

Lomma M. · Gomez Valero L. · Rusniok C. · Buchrieser C.
Institut Pasteur, Unité Biologie des Bactéries Intracellulaires and CNRS URA 2171, Paris, France

Individual Users: Register with Karger Login Information

Please create your User ID & Password





Contact Information











I have read the Karger Terms and Conditions and agree.

To view the fulltext, please log in

To view the pdf, please log in

Abstract

Legionella pneumophila is the etiological agent of Legionnaires’ disease and of the less acute disease Pontiac fever. It is a Gram-negative bacterium present in fresh and artificial water environments that replicates in protozoan hosts and is also found in biofilms. Replication within protozoa is essential for the survival of the bacterium. The last years have seen a giant step forward in the genomics of L. pneumophila. The establishment and publication of the complete genome sequences of three clinical L. pneumophila isolates in 2004 and a fourth in 2007 has paved the way for major breakthroughs in understanding the biology of L. pneumophila in particular and Legionella in general. Sequence analysis identified several specific features of Legionella: (i) an extraordinary genetic diversity among the different isolates and (ii) the presence of an unexpected high number and variety of eukaryotic-like proteins, predicted to be involved in the exploitation of the host cellular processes by mimicking specific eukaryotic functions. In this chapter, we will first discuss the insights gained from genomics by highlighting the characteristic features and common traits of the four L. pneumophila genomes obtained through genome analysis and comparison and then we will focus on the newest results obtained by functional analysis of different eukaryotic-like proteins and describe their involvementin the pathogenicity of L. pneumophila.



Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  1. Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, et al: Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 1995;269:496-512
  2. Fields BS, Benson RF, Besser RE: Legionella and Legionnaires’ disease: 25 years of investigation. Clin Microbiol Rev 2002;15:506-526
  3. Steinert M, Hentschel U, Hacker J: Legionella pneumophila: an aquatic microbe goes astray. FEMS Microbiol Rev 2002;26:149-162
  4. Diederen BM: Legionella spp. and Legionnaires’ disease. J Infect 2008;56:1-12
  5. Berger KH, Isberg RR: Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol Microbiol 1993;7:7-19
  6. Marra A, Blander SJ, Horwitz MA, Shuman HA: Identification of a Legionella pneumophila locus required for intracellular multiplication in human macrophages. Proc Natl Acad Sci USA 1992;89:9607-9611
  7. Shin S, Roy CR: Host cell processes that influence the intracellular survival of Legionella pneumophila. Cell Microbiol 2008;10:1209-1220
  8. Cazalet C, Rusniok C, Bruggemann H, Zidane N, Magnier A, et al: Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat Genet 2004;36:1165-1173
  9. Chien M, Morozova I, Shi S, Sheng H, Chen J, et al: The genomic sequence of the accidental pathogen Legionella pneumophila. Science 2004;305:1966-1968
  10. Steinert M, Heuner K, Buchrieser C, Albert-Weissenberger C, Glöckner G: Legionella pathogenicity: genome structure, regulatory networks and the host cell response. Int J Med Microbiol 2007;297:577-587
  11. Cazalet C, Jarraud S, Ghavi-Helm Y, Kunst F, Glaser P, et al: Multigenome analysis identifies a worldwide distributed epidemic Legionella pneumophila clone that emerged within a highly diverse species. Genome Res 2008;18:431-441
  12. Brüggemann H, Cazalet C, Buchrieser C: Adaptation of Legionella pneumophila to the host environment: role of protein secretion, effectors and eukaryotic-like proteins. Curr Opin Microbiol 2006;9:86-94
  13. de Felipe KS, Pampou S, Jovanovic OS, Pericone CD, Ye SF, et al: Evidence for acquisition of Legionella type IV secretion substrates via interdo-main horizontal gene transfer. J Bacteriol 2005;187:7716-7726
  14. Albert-Weissenberger C, Cazalet C, Buchrieser C: Legionella pneumophila - a human pathogen that co-evolved with fresh water protozoa. Cell Mol Life Sci 2007;64:432-448
  15. Nichols FC: Novel ceramides recovered from Porphyromonas gingivalis: relationship to adult periodontitis. J Lipid Res 1998;39:2360-2372
  16. Bandhuvula P, Saba JD: Sphingosine-1 -phosphate lyase in immunity and cancer: silencing the siren. Trends Mol Med 2007;13:210-217
  17. Zhang K, Pompey JM, Hsu FF, Key P, Bandhuvula P, et al: Redirection of sphingolipid metabolism toward de novo synthesis of ethanolamine in Leishmania. EMBO J 2007;26:1094-1104
  18. Li G, Foote C, Alexander S, Alexander H: Sphingosine-1-phosphate lyase has a central role in the development of Dictyostelium discoideum. Development 2001;128:3473-3483
  19. Oggioni MR, Memmi G, Maggi T, Chiavolini D, Iannelli F, Pozzi G: Pneumococcal zinc metalloproteinase ZmpC cleaves human matrix metalloproteinase 9 and is a virulence factor in experimental pneumonia. Mol Microbiol 2003;49:795-805
  20. Seshadri R, Paulsen IT, Eisen JA, Read TD, Nelson KE, et al: Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proc Natl Acad Sci USA 2003;100:5455-5460
  21. Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R, et al: Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: A streamlined genome overrun by mobile genetic elements. PLoS Biol 2004;2:E69
  22. Ogata H, La Scola B, Audic S, Renesto P, Blanc G, et al: Genome sequence of Rickettsia bellii illuminates the role of amoebae in gene exchanges between intracellular pathogens. PLoS Genet 2006;2:e:76
  23. Walburger A, Koul A, Ferrari G, Nguyen L, Prescianotto-Baschong C, et al: Protein kinase G from pathogenic mycobacteria promotes survival within macrophages. Science 2004;304:1800-1804
  24. Fernandez P, Saint-Joanis B, Barilone N, Jackson M, Gicquel B, et al: The Ser/Thr protein kinase PknB is essential for sustaining mycobacterial growth. J Bacteriol 2006;188:7778-7784
  25. Greenstein AE, MacGurn JA, Baer CE, Falick AM, Cox JS, Alber T: M. tuberculosis Ser/Thr protein kinase D phosphorylates an anti-anti-sigma factor homolog. PLoS Pathog 2007;3:e49
  26. Rose A, Schraegle SJ, Stahlberg EA, Meier I: Coiled-coil protein composition of 22 proteomes - differences and common themes in subcellular infrastructure and traffic control. BMC Evol Biol 2005;16:66
  27. Chen J, Reyes M, Clarke M, Shuman HA: Host cell-dependent secretion and translocation of the LepA and LepB effectors of Legionella pneumophila. Cell Microbiol 2007;9:1660-1671
  28. Luo ZQ, Isberg RR: Multiple substrates of the Legionella pneumophila Dot/Icm system identified by interbacterial protein transfer. Proc Natl Acad Sci USA 2004;101:841-846
  29. Burkhard P, Stetefeld J, Strelkov SV: Coiled coils: a highly versatile protein folding motif. Trends Cell Biol 2001;11:82-88
  30. de Felipe KS, Glover RT, Charpentier X, Anderson OR, Reyes M, et al: Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog 2008;4:e1000117
  31. Kagan JC, Roy CR: Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat Cell Biol 2002;4:945-954
  32. Tilney LG, Harb OS, Connelly PS, Robinson CG, Roy CR: How the parasitic bacterium Legionella pneumophila modifies its phagosome and transforms it into rough ER: implications for conversion of plasma membrane to the ER membrane. J Cell Sci 2001;114:4637-4650
  33. Horwitz MA: The Legionnaires’ disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J Exp Med 1983;158:2108-2126
  34. Dubuisson JF, Swanson MS: Mouse infection by Legionella, a model to analyze autophagy. Autophagy 2006;2:179-182
  35. Amer AO, Swanson MS: Autophagy is an immediate macrophage response to Legionella pneumophila. Cell Microbiol 2005;7:765-778
  36. Sturgill-Koszycki S, Swanson MS: Legionella pneumophila replication vacuoles mature into acidic, endocytic organelles. J Exp Med 2000;192:1261-1272
  37. Molmeret M, Bitar DM, Han L, Kwaik YA: Disruption of the phagosomal membrane and egress of Legionella pneumophila into the cytoplasm during the last stages of intracellular infection of macrophages and Acanthamoeba polyphaga. Infect Immun 2004;72:4040-4051
  38. Alli OA, Gao LY, Pedersen LL, Zink S, Radulic M, et al: Temporal pore formation-mediated egress from macrophages and alveolar epithelial cells by Legionella pneumophila. Infect Immun 2000;68:6431-6440
  39. Marcus AJ, Broekman MJ, Drosopoulos JH, Olson KE, Islam N, et al: Role of CD39 (NTPDase-1) in thromboregulation, cerebroprotection, and cardio-protection. Semin Thromb Hemost 2005;31:234-246
  40. Sansom FM, Newton HJ, Crikis S, Cianciotto NP, Cowan PJ, et al: A bacterial ecto-triphosphate diphosphohydrolase similar to human CD39 is essential for intracellular multiplication of Legionella pneumophila. Cell Microbiol 2007;9:1922-1935
  41. Sansom FM, Riedmaier P, Newton HJ, Dunstone MA, Müller CE, et al: Enzymatic properties of an ecto-nucleoside triphosphate diphosphohydrolase from Legionella pneumophila: substrate specificity and requirement for virulence. J Biol Chem 2008;283:12909-12918
  42. Shohdy N, Efe JA, Emr SD, Shuman HA: Pathogen effector protein screening in yeast identifies Legionella factors that interfere with membrane trafficking. Proc Natl Acad Sci USA 2005;102:4866-4871
  43. Banerji S, Aurass P, Flieger A: The manifold phospholipases A of Legionella pneumophila - identification, export, regulation, and their link to bacterial virulence. Int J Med Microbiol 2008;298:169-181
  44. Goebl M, Yanagida M: The TPR snap helix: a novel protein repeat motif from mitosis to transcription. Trends Biochem Sci 1991;16:173-177
  45. Liu M, Conover GM, Isberg RR: Legionella pneumophila EnhC is required for efficient replication in tumor necrosis factor alpha-stimulated macrophages. Cell Microbiol 2008;10:1906-1923
  46. Cirillo SL, Lum J, Cirillo JD: Identification of novel loci involved in entry by Legionella pneumophila. Microbiology 2000;146:1345-1359
  47. Newton HJ, Sansom FM, Bennett-Wood V, Hartland EL: 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 2006;74:1683-1691
  48. Newton HJ, Sansom FM, Dao J, McAlister AD, Sloan J, et al: Sel1 repeat protein LpnE is a Legionella pneumophila virulence determinant that influences vacuolar trafficking. Infect Immun 2007;75:5575-5585
  49. Kagan JC, Stein MP, Pypaert M, Roy CR: Legionella subvert the functions of Rab1 and Sec22b to create a replicative organelle. J Exp Med 2004;199:1201-1211
  50. Derré I, Isberg RR: Legionella pneumophila replication vacuole formation involves rapid recruitment of proteins of the early secretory system. Infect Immun 2004;72:3048-3053
  51. Nagai H, Kagan JC, Zhu X, Kahn RA, Roy CR: A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 2002;295:679-682
  52. Machner MP, Isberg RR: Targeting of host Rab GTPase function by the intravacuolar pathogen Legionella pneumophila. Dev Cell 2006;11:47-56
  53. Murata T, Delprato A, Ingmundson A, Toomre DK, Lambright DG, Roy CR: The Legionella pneumophila effector protein DrrA is a Rab1 guanine nucleotide-exchange factor. Nat Cell Biol 2006;8:971-977
  54. Ingmundson A, Delprato A, Lambright DG, Roy CR: Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature 2007;450:365-369
  55. Sedgwick SG, Smerdon SJ: The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem Sci 1999;24:311-316
  56. Mosavi LK, Minor DL, Jr, Peng ZY: Consensus-derived structural determinants of the ankyrin repeat motif. Proc Natl Acad Sci USA 2002;99:16029-16034
  57. Habyarimana F, Al-Khodor S, Kalia A, Graham JE, Price CT, et al: Role for the Ankyrin eukaryotic-like genes of Legionella pneumophila in parasitism of protozoan hosts and human macrophages. Environ Microbiol 2008;10:1460-1474
  58. Pan X, Lührmann A, Satoh A, Laskowski-Arce MA, Roy CR: Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors. Science 2008;320:1651-1654
  59. Dorer MS, Kirton D, Bader JS, Isberg RR: RNA interference analysis of Legionella in Drosophila cells: exploitation of early secretory apparatus dynamics. PLoS Pathog 2006;2:e34
  60. Kubori T, Hyakutake A, Nagai H: Legionella translocates an E3 ubiquitin ligase that has multiple U-boxes with distinct functions. Mol Microbiol 2008;67:1307-1319
  61. Molmeret M, Abu Kwaik Y: How does Legionella pneumophila exit the host cell?. Trends Microbiol 2002;10:258-260
  62. Sutton RB, Fasshauer D, Jahn R, Brunger AT: Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 1998;395:347-353
  63. Amor JC, Swails J, Zhu X, Roy CR, Nagai H, et al: The structure of RalF, an ADP-ribosylation factor guanine nucleotide exchange factor from Legionella pneumophila, reveals the presence of a cap over the active site. J Biol Chem 2005;280:1392-1400


Pay-per-View Options
Direct payment This item at the regular price: USD 38.00
Payment from account With a Karger Pay-per-View account (down payment USD 150) you profit from a special rate for this and other single items.
This item at the discounted price: USD 26.50