Protein kinase LegK2 is a type IV secretion system effector involved in endoplasmic reticulum recruitment and intracellular replication of Legionella pneumophila

Infection and Immunity

Volumn 79, Issue 5, 2011, Pages 1936-1950

  Hervet, Eva ^a   Charpentier, Xavier ^b,c   Vianney, Anne ^a   Lazzaroni, Jean Claude ^a   Gilbert, Christophe ^a   Atlan, Danièle ^a   Doublet, Patricia ^a  

^a UNIVERSITÉ DE LYON   (France)

^b NewYork Presbyterian Hospital   (United States)

^c UNIV GRENOBLE ALPES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN KINASE LEGK2; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL VIRULENCE; CELL DIVISION; ENDOPLASMIC RETICULUM; GENE INACTIVATION; LEGIONELLA PNEUMOPHILA; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 79955585865     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00805-10     Document Type: Article

References (75)

1. Alber, T. 2009. Signaling mechanisms of the Mycobacterium tuberculosis receptor Ser/Thr protein kinases. Curr. Opin. Struct. Biol. 19:650-657.
2. Amrein, K., et al. 1995. Purification and characterization of recombinant human p50csk protein-tyrosine kinase from an Escherichia coli expression system overproducing the bacterial chaperones GroES and GroEL. Proc. Natl. Acad. Sci. U. S. A. 92:1048-1052.
3. Andrews, H. L., J. P. Vogel, and R. R. Isberg. 1998. Identification of linked Legionella pneumophila genes essential for intracellular growth and evasion of the endocytic pathway. Infect. Immun. 66:950-958.
4. Barz, C., T. N. Abahji, K. Trulzsch, and J. Heesemann. 2000. The Yersinia Ser/Thr protein kinase YpkA/YopO directly interacts with the small GTPases RhoA and Rac-1. FEBS Lett. 482:139-143.
5. Berger, K., and R. Isberg. 1993. Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol. Microbiol. 7:7-19.
6. Brenner, S. 1987. Phosphotransferase sequence homology. Nature 329:21.
7. Brombacher, E., et al. 2009. Rab1 guanine nucleotide exchange factor SidM is a major phosphatidylinositol 4-phosphate-binding effector protein of Le-gionella pneumophila. J. Biol. Chem. 284:4846-4856.
8. Cazalet, C., et al. 2004. Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat. Genet. 36:1165-1173.
9. Chao, J., et al. 2010. Protein kinase and phosphatase signaling in Mycobacterium tuberculosis physiology and pathogenesis. Biochim. Biophys. Acta 1804:620-627.
10. Charpentier, X., et al. 2009. Chemical genetics reveals bacterial and host cell functions critical for type IV effector translocation by Legionella pneumophila. PLoS Pathog. 5:e1000501.
11. Coers, J., C. Monahan, and C. Roy. 1999. Modulation of phagosome biogenesis by Legionella pneumophila creates an organelle permissive for intracellular growth. Nat. Cell Biol. 1:451-453.
12. Cornillon, S., et al. 2000. Phg1p is a nine-transmembrane protein superfamily member involved in Dictyostelium adhesion and phagocytosis. J. Biol. Chem. 275:34287-34292.
13. Cozzone, A. J. 2005. Role of protein phosphorylation on serine/threonine and tyrosine in the virulence of bacterial pathogens. J. Mol. Microbiol. Biotechnol. 9:198-213.
14. Datsenko, K., and B. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
15. D'Auria, G., N. Jiménez-Hernández, F. Peris-Bondia, A. Moya, and A. Latorre. 2010. Legionella pneumophila pangenome reveals strain-specific virulence factors. BMC Genomics 11:181.
16. de Felipe, K., et al. 2005. Evidence for acquisition of Legionella type IV secretion substrates via interdomain horizontal gene transfer. J. Bacteriol. 187:7716-7726.
17. de Felipe, K. S., et al. 2008. Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog. 4:e1000117.
18. Degtyar, E., T. Zusman, M. Ehrlich, and G. Segal. 2009. A Legionella effector acquired from protozoa is involved in sphingolipids metabolism and is targeted to the host cell mitochondria. Cell Microbiol. 11:1219-1235.
19. Deutscher, J., and M. H. Saier. 2005. Ser/Thr/Tyr protein phosphorylation in bacteria: for long time neglected, now well established. J. Mol. Microbiol. Biotechnol. 9:125-131.
20. Echenique, J., A. Kadioglu, S. Romao, P. W. Andrew, and M. C. Trombe. 2004. Protein serine/threonine kinase StkP positively controls virulence and competence in Streptococcus pneumoniae. Infect. Immun. 72:2434-2437.
21. Ensminger, A., and R. Isberg. 2010. E3 ubiquitin ligase activity and targeting of BAT3 by multiple Legionella pneumophila translocated substrates. Infect. Immun. 78:3905-3919.
22. Ensminger, A. W., and R. R. Isberg. 2009. Legionella pneumophila Dot/Icm translocated substrates: a sum of parts. Curr. Opin. Microbiol. 12:67-73.
23. Ferhat, M., et al. 2009. The TolC protein of Legionella pneumophila plays a major role in multidrug resistance and the early steps of host invasion. PLoS One 4:e7732.
24. Gao, L. Y., O. S. Harb, and Y. AbuKwaik. 1997. Utilization of similar mechanisms by Legionella pneumophila to parasitize two evolutionarily distant host cells, mammalian macrophages and protozoa. Infect. Immun. 65: 4738-4746.
25. Ge, J., et al. 2009. A Legionella type IV effector activates the NF-κB pathway by phosphorylating the IκB family of inhibitors. Proc. Natl. Acad. Sci. U. S. A. 106:13725-13730.
26. Glockner, G., et al. 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.
27. Han, G., and C. Zhang. 2001. On the origin of Ser/Thr kinases in a pro-karyote. FEMS Microbiol. Lett. 200:79-84.
28. Hanks, S. 2003. Genomic analysis of the eukaryotic protein kinase super-family: a perspective. Genome Biol. 4:111.
29. Harb, O., L. Gao, and Y. Abu Kwaik. 2000. From protozoa to mammalian cells: a new paradigm in the life cycle of intracellular bacterial pathogens. Environ. Microbiol. 2:251-265.
30. Ingmundson, A., A. Delprato, D. Lambright, and C. Roy. 2007. Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature 450: 365-369.
31. Ish-Horowicz, D., and J. Burke. 1981. Rapid and efficient cosmid cloning. Nucleic Acids Res. 9:2989-2998.
32. Jin, H., and V. Pancholi. 2006. Identification and biochemical characterization of a eukaryotic-type serine/threonine kinase and its cognate phosphatase in Streptococcus pyogenes: their biological functions and substrate identification. J. Mol. Biol. 357:1351-1372.
33. Juris, S., A. Rudolph, D. Huddler, K. Orth, and J. Dixon. 2000. A distinctive role for the Yersinia protein kinase: actin binding, kinase activation, and cytoskeleton disruption. Proc. Natl. Acad. Sci. U. S. A. 97:9431-9436.
34. Kagan, J., and C. Roy. 2002. Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat. Cell Biol. 4:945-954.
35. Kawachi, H., A. Fujikawa, N. Maeda, and M. Noda. 2001. Identification of GIT1/Cat-1 as a substrate molecule of protein tyrosine phosphatase zeta/beta by the yeast substrate-trapping system. Proc. Natl. Acad. Sci. U. S. A. 98:6593-6598.
36. Kim, E., X. Charpentier, O. Torres-Urquidy, M. McEvoy, and C. Rensing. 2009. The metal efflux island of Legionella pneumophila is not required for survival in macrophages and amoebas. FEMS Microbiol. Lett. 301:164-170.
37. Kristich, C. J., C. L. Wells, and G. M. Dunny. 2007. A eukaryotic-type Ser/Thr kinase in Enterococcus faecalis mediates antimicrobial resistance and intestinal persistence. Proc. Natl. Acad. Sci. U. S. A. 104:3508-3513.
38. Krupa, A., K. Abhinandan, and N. Srinivasan. 2004. KinG: a database of protein kinases in genomes. Nucleic Acids Res. 32:D153-D155.
39. Krupa, A., and N. Srinivasan. 2005. Diversity in domain architectures of Ser/Thr kinases and their homologues in prokaryotes. BMC Genomics 6:129.
40. Kubori, T., A. Hyakutake, and H. Nagai. 2008. Legionella translocates an E3 ubiquitin ligase that has multiple U-boxes with distinct functions. Mol. Microbiol. 67:1307-1319.
41. Laemmli, U. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
42. La Scola, B., et al. 2004. Legionella drancourtii sp. nov., a strictly intracellular amoebal pathogen. Int. J. Syst. Evol. Microbiol. 54:699-703.
43. Liu, Y., and Z. Luo. 2007. The Legionella pneumophila effector SidJ is required for efficient recruitment of endoplasmic reticulum proteins to the bacterial phagosome. Infect. Immun. 75:592-603.
44. Lomma, M., et al. 2010. The Legionella pneumophila F-box protein Lpp2082 (AnkB) modulates ubiquitination of the host protein parvin B and promotes intracellular replication. Cell Microbiol. 12:1272-1291.
45. Losick, V., E. Haenssler, M. Moy, and R. Isberg. 2010. LnaB: a Legionella pneumophila activator of NF-κB. Cell Microbiol. 12:1083-1097.
46. Lurie-Weinberger, M., et al. 2010. The origins of eukaryotic-like proteins in Legionella pneumophila. Int. J. Med. Microbiol. 300:470-481.
47. Lux, R., and W. Shi. 2005. A novel bacterial signaling system with a combination of a Ser/Thr kinase cascade and a His/Asp two-component system. Mol. Microbiol. 58:345-348.
48. Machner, M., and R. Isberg. 2007. A bifunctional bacterial protein links GDI displacement to Rab1 activation. Science 318:974-977.
49. Machner, M., and R. Isberg. 2006. Targeting of host Rab GTPase function by the intravacuolar pathogen Legionella pneumophila. Dev. Cell 11:47-56.
50. Moliner, C, P. Fournier, and D. Raoult. 2010. Genome analysis of microorganisms living in amoebae reveals a melting pot of evolution. FEMS Microbiol. Rev. 34:281-294.
51. Molle, V., and L. Kremer. 2010. Division and cell envelope regulation by Ser/Thr phosphorylation: Mycobacterium shows the way. Mol. Microbiol. 75:1064-1077.
52. Molofsky, A., and M. Swanson. 2004. Differentiate to thrive: lessons from the Legionella pneumophila life cycle. Mol. Microbiol. 53:29-40.
53. Moncrief, N., R. Kretsinger, and M. Goodman. 1990. Evolution of EF-hand calcium-modulated proteins. I. Relationships based on amino acid sequences. J. Mol. Evol. 30:522-562.
54. Murata, T., et al. 2006. The Legionella pneumophila effector protein DrrA is a Rab1 guanine nucleotide-exchange factor. Nat. Cell Biol. 8:971-977.
55. Muller-Taubenberger, A., et al. 2001. Calreticulin and calnexin in the endoplasmic reticulum are important for phagocytosis. EMBO J. 20:6772-6782.
56. Nagai, H., J. Kagan, X. Zhu, R. Kahn, and C. Roy. 2002. A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 295:679-682.
57. Nariya, H., and S. Inouye. 2006. A protein Ser/Thr kinase cascade negatively regulates the DNA-binding activity of MrpC, a smaller form of which may be necessary for the Myxococcus xanthus development. Mol. Microbiol. 60: 1205-1217.
58. Patel, R., et al. 1999. DRBP76, a double-stranded RNA-binding nuclear protein, is phosphorylated by the interferon-induced protein kinase, PKR. J. Biol. Chem. 274:20432-20437.
59. Poh, J., et al. 2008. SteC is a Salmonella kinase required for SPI-2-dependent F-actin remodeling. Cell. Microbiol. 10:20-30.
60. Pope, C, L. Dhand, and N. Cianciotto. 1994. Random mutagenesis of Legionella pneumophila with mini-Tn10. FEMS Microbiol. Lett. 124:107-111.
61. Price, C, et al. 2009. Molecular mimicry by an F-box effector of Legionella pneumophila hijacks a conserved polyubiquitination machinery within macrophages and protozoa. PLoS Pathog. 5:e1000704.
62. Ragaz, C, et al. 2008. The Legionella pneumophila phosphatidylinositol-4 phosphate-binding type IV substrate SidC recruits endoplasmic reticulum vesicles to a replication-permissive vacuole. Cell Microbiol. 10:2416-2433.
63. Rowbotham, T. 1980. Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J. Clin. Pathol. 33: 1179-1183.
64. Roy, C. R., K. H. Berger, and R. R. Isberg. 1998. Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol. Microbiol. 28:663-674.
65. Sahr, T., et al. 2009. Two small ncRNAs jointly govern virulence and transmission in Legionella pneumophila. Mol. Microbiol. 72:741-762.
66. Saskova, L., L. Novakova, M. Basler, and P. Branny. 2007. Eukaryotic-type serine/threonine protein kinase StkP is a global regulator of gene expression in Streptococcus pneumoniae. J. Bacteriol. 189:4168-4179.
67. Segal, G., M. Purcell, 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. U. S. A. 95:1669-1674.
68. Shin, S., and C. R. Roy. 2008. Host cell processes that influence the intracellular survival of Legionella pneumophila. Cell. Microbiol. 10:1209-1220.
69. Smith, D., and K. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67:31-40.
70. Tiwari, D., et al. 2009. Key residues in Mycobacterium tuberculosis protein kinase G play a role in regulating kinase activity and survival in the host. J. Biol. Chem. 284:27467-27479.
71. Walburger, A., et al. 2004. Protein kinase G from pathogenic mycobacteria promotes survival within macrophages. Science 304:1800-1804.
72. Weber, S., C. Ragaz, K. Reus, Y. Nyfeler, and H. Hilbi. 2006. Legionella pneumophila exploits PI(4)P to anchor secreted effector proteins to the replicative vacuole. PLoS Pathog. 2:e46.
73. Xu, L., et al. 2010. Inhibition of host vacuolar H+-ATPase activity by a Legionella pneumophila effector. PLoS Pathog. 6:e1000822.
74. Zhang, C, J. Jang, S. Sakr, and L. Wang. 2005. Protein phosphorylation on Ser, Thr, and Tyr residues in cyanobacteria. J. Mol. Microbiol. Bio-technol. 9:154-166.
75. Zheng, J., C. He, V. Singh, N. Martin, and Z. Jia. 2007. Crystal structure of a novel prokaryotic Ser/Thr kinase and its implication in the Cpx stress response pathway. Mol. Microbiol. 63:1360-1371.