Computational modeling and experimental validation of the Legionella and Coxiella virulence-related type-IVB secretion signal

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 8, 2013, Pages

  Lifshitz, Ziv ^a   Burstein, David ^a   Peeri, Michael ^a   Zusman, Tal ^a   Schwartz, Kierstyn ^b   Shuman, Howard A ^b   Pupko, Tal ^a   Segal, Gil ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Legionnaire disease; Pathogenomics; Q fever; Translocated substrates; Type IV secretion

Indexed keywords

GLUTAMIC ACID;

AMINO ACID COMPOSITION; AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENOME; BACTERIAL MUTATION; BACTERIAL TRANSLOCATION; BACTERIAL VIRULENCE; COMPUTATIONAL MODEL; COMPUTER MODEL; CONTROLLED STUDY; COXIELLA BURNETII; DELETION MUTANT; ENTOMOPATHOGENIC BACTERIUM; HIDDEN MARKOV MODEL; HOST CELL; LEGIONELLA LONGBEACHAE; LEGIONELLA PNEUMOPHILA; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; TYPE IV SECRETION SYSTEM; WESTERN BLOTTING;

AMINO ACID SEQUENCE; COMPUTER SIMULATION; COXIELLA BURNETII; GENOME, BACTERIAL; LEGIONELLA PNEUMOPHILA; MARKOV CHAINS; MOLECULAR SEQUENCE DATA; PROTEIN TRANSPORT; VIRULENCE;

EID: 84874280135     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1215278110     Document Type: Article

References (56)

1. Ghigo E, et al. (2009) Intracellular life of Coxiella burnetii in macrophages. Ann N Y Acad Sci 1166:55-66.
2. Diederen BM (2008) Legionella spp. and Legionnaires' disease. J Infect 56 (1):1-12.
3. Cutler SJ, Bouzid M, Cutler RR (2007) Q fever. J Infect 54 (4):313-318.
4. Fields BS (1996) The molecular ecology of legionellae. Trends Microbiol 4 (7):286-290.
5. Newton HJ, Roy CR (2011) The Coxiella burnetii Dot/Icm system creates a comfortable home through lysosomal renovation. MBio 2 (5):e00226-e00211.
6. Isberg RR, O'Connor TJ, Heidtman M (2009) The Legionella pneumophila replication vacuole: Making a cosy niche inside host cells. Nat Rev Microbiol 7 (1):13-24.
7. Voth DE, Heinzen RA (2007) Lounging in a lysosome: The intracellular lifestyle of Coxiella burnetii. Cell Microbiol 9 (4):829-840.
8. Fields BS, Benson RF, Besser RE (2002) Legionella and Legionnaires' disease: 25 years of investigation. Clin Microbiol Rev 15 (3):506-526.
9. Segal G, Feldman M, Zusman T (2005) The Icm/Dot type-IV secretion systems of Legionella pneumophila and Coxiella burnetii. FEMS Microbiol Rev 29 (1):65-81.
10. Carey KL, Newton HJ, Lührmann A, Roy CR (2011) The Coxiella burnetii Dot/Icm system delivers a unique repertoire of type IV effectors into host cells and is required for intracellular replication. PLoS Pathog 7 (5):e1002056.
11. Voth DE, Heinzen RA (2009) Coxiella type IV secretion and cellular microbiology. Curr Opin Microbiol 12 (1):74-80.
12. Shin S, Roy CR (2008) Host cell processes that influence the intracellular survival of Legionella pneumophila. Cell Microbiol 10 (6):1209-1220.
13. Pan X, Lührmann A, Satoh A, Laskowski-Arce MA, Roy CR (2008) Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors. Science 320 (5883):1651-1654.
14. Voth DE, et al. (2009) The Coxiella burnetii ankyrin repeat domain-containing protein family is heterogeneous, with C-terminal truncations that influence Dot/Icm-mediated secretion. J Bacteriol 191 (13):4232-4242.
15. Nagai H, Kagan JC, Zhu X, Kahn RA, Roy CR (2002) A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 295 (5555):679-682.
16. Nagai H, et al. (2005) A C-terminal translocation signal required for Dot/Icm-dependent delivery of the Legionella RalF protein to host cells. Proc Natl Acad Sci USA 102 (3):826-831.
17. Kubori T, Hyakutake A, Nagai H (2008) Legionella translocates an E3 ubiquitin ligase that has multiple U-boxes with distinct functions. Mol Microbiol 67 (6):1307-1319.
18. Burstein D, et al. (2009) Genome-scale identification of Legionella pneumophila effectors using a machine learning approach. PLoS Pathog 5 (7):e1000508.
19. Huang L, et al. (2011) The E Block motif is associated with Legionella pneumophila translocated substrates. Cell Microbiol 13 (2):227-245.
20. Ninio S, Zuckman-Cholon DM, Cambronne ED, Roy CR (2005) The Legionella IcmS-IcmW protein complex is important for Dot/Icm-mediated protein translocation. Mol Microbiol 55 (3):912-926.
21. Cambronne ED, Roy CR (2007) The Legionella pneumophila IcmSW complex interacts with multiple Dot/Icm effectors to facilitate type IV translocation. PLoS Pathog 3 (12): e188.
22. Degtyar E, Zusman T, Ehrlich M, Segal G (2009) A Legionella effector acquired from protozoa is involved in sphingolipids metabolism and is targeted to the host cell mitochondria. Cell Microbiol 11 (8):1219-1235.
23. Durbin R, Eddy S, Krogh A, Mitchison G (1998) Biological Sequence Analysis: Probabilistic Models of Proteins and Nucleic Acids (Cambridge Univ Press, Cambridge, UK).
24. Levinson SE (1986) Continuously variable duration hidden Markov models for automatic speech recognition. Comput Speech Lang 1 (1):29-45.
25. Rabiner LR (1989) A tutorial on hidden Markov models and selected applications in speech recognition. Proc IEEE 77 (2):257-286.
26. de Felipe KS, et al. (2008) Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog 4 (8):e1000117.
27. Zhu W, et al. (2011) Comprehensive identification of protein substrates of the Dot/Icm type IV transporter of Legionella pneumophila. PLoS ONE 6 (3):e17638.
28. Feldman M, Zusman T, Hagag S, Segal G (2005) Coevolution between nonhomologous but functionally similar proteins and their conserved partners in the Legionella patho-genesis system. Proc Natl Acad Sci USA 102 (34):12206-12211.
29. Asare R, Abu Kwaik Y (2007) Early trafficking and intracellular replication of Legionella longbeachae within an ER-derived late endosome-like phagosome. Cell Microbiol 9 (6):1571-1587.
30. Cazalet C, et al. (2004) Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat Genet 36 (11):1165-1173.
31. de Felipe KS, et al. (2005) Evidence for acquisition of Legionella type IV secretion substrates via interdomain horizontal gene transfer. J Bacteriol 187 (22):7716-7726.
32. Beare PA, et al. (2011) Dot/Icm type IVB secretion system requirements for Coxiella burnetii growth in human macrophages. MBio 2 (4):e00175-e11.
33. Voth DE, et al. (2011) The Coxiella burnetii cryptic plasmid is enriched in genes encoding type IV secretion system substrates. J Bacteriol 193 (7):1493-1503.
34. Chen C, et al. (2010) Large-scale identification and translocation of type IV secretion substrates by Coxiella burnetii. Proc Natl Acad Sci USA 107 (50):21755-21760.
35. Leclerque A, Kleespies RG (2008) Type IV secretion system components as phylogenetic markers of entomopathogenic bacteria of the genus Rickettsiella. FEMS Microbiol Lett 279 (2):167-173.
36. Lloyd SA, Norman M, Rosqvist R, Wolf-Watz H (2001) Yersinia YopE is targeted for type III secretion by N-terminal, not mRNA, signals. Mol Microbiol 39 (2):520-531.
37. Lloyd SA, Sjöström M, Andersson S, Wolf-Watz H (2002) Molecular characterization of type III secretion signals via analysis of synthetic N-terminal amino acid sequences. Mol Microbiol 43 (1):51-59.
38. Hueck CJ (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62 (2):379-433.
39. Galán JE, Wolf-Watz H (2006) Protein delivery into eukaryotic cells by type III secretion machines. Nature 444 (7119):567-573.
40. Schulein R, et al. (2005) A bipartite signal mediates the transfer of type IV secretion substrates of Bartonella henselae into human cells. Proc Natl Acad Sci USA 102 (3):856-861.
41. Hurtado-Guerrero R, et al. (2010) Molecular mechanism of elongation factor 1A inhibition by a Legionella pneumophila glycosyltransferase. Biochem J 426 (3):281-292.
42. Kozak NA, et al. (2010) Virulence factors encoded by Legionella longbeachae identified on the basis of the genome sequence analysis of clinical isolate D-4968. J Bacteriol 192 (4):1030-1044.
43. Cazalet C, et al. (2010) Analysis of the Legionella longbeachae genome and transcriptome uncovers unique strategies to cause Legionnaires' disease. PLoS Genet 6 (2):e1000851.
44. Pearce MM, et al. (2012) Legionella cardiaca sp. nov., isolated from a case of native valve endocarditis in a human heart. Int J Syst Evol Microbiol 62 (Pt 12):2946-2954.
45. Campocasso A, Boughalmi M, Fournous G, Raoult D, La Scola B (2012) Legionella tunisiensis sp. nov. and Legionella massiliensis sp. nov., isolated from environmental water samples. Int J Syst Evol Microbiol. 62 (12):3003-3006.
46. Witten IH, Frank E (2005) Data Mining: Practical Machine Learning Tools and Techniques (Morgan Kaufmann, San Francisco).
47. Finn RD, et al. (2010) The Pfam protein families database. Nucleic Acids Res 38 (Database issue):D211-D222.
48. Chien M, et al. (2004) The genomic sequence of the accidental pathogen Legionella pneumophila. Science 305 (5692):1966-1968.
49. Moliner C, Raoult D, Fournier PE (2009) Evidence that the intra-amoebal Legionella drancourtii acquired a sterol reductase gene from eukaryotes. BMC Res Notes 2:51.
50. Seshadri R, et al. (2003) Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proc Natl Acad Sci USA 100 (9):5455-5460.
51. Blattner FR, et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277 (5331):1453-1462.
52. Sadosky AB, Wiater LA, Shuman HA (1993) Identification of Legionella pneumophila genes required for growth within and killing of human macrophages. Infect Immun 61 (12):5361-5373.
53. Zusman T, Yerushalmi G, Segal G (2003) Functional similarities between the icm/dot pathogenesis systems of Coxiella burnetii and Legionella pneumophila. Infect Immun 71 (7):3714-3723.
54. Omsland A, et al. (2011) Isolation from animal tissue and genetic transformation of Coxiella burnetii are facilitated by an improved axenic growth medium. Appl Environ Microbiol 77 (11):3720-3725.
55. Howe D, Shannon JG, Winfree S, Dorward DW, Heinzen RA (2010) Coxiella burnetii phase I and II variants replicate with similar kinetics in degradative phagolysosome-like compartments of human macrophages. Infect Immun 78 (8):3465-3474.
56. Saldanha AJ (2004) Java Treeview-Extensible visualization of microarray data. Bioinformatics 20 (17):3246-3248.