Characterization of the AtsR hybrid sensor kinase phosphorelay pathway and identification of its response regulator in burkholderia cenocepacia

Journal of Biological Chemistry

Volumn 288, Issue 42, 2013, Pages 30473-30484

  Khodai Kalaki, Maryam ^a   Aubert, Daniel F ^a   Valvano, Miguel A ^a,b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BURKHOLDERIA; GLOBAL REGULATORS; PHOSPHORELAY; QUORUM-SENSING; RESPONSE REGULATORS;

ENZYMES; HYBRID SENSORS;

PLANTS (BOTANY);

ASPARTIC ACID; ASPARTIC ACID 536; HISTIDINE; HISTIDINE 245; MEMBRANE PROTEIN; PROTEIN KINASE; PROTEINASE; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BIOFILM; BURKHOLDERIA CENOCEPACIA; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; QUORUM SENSING; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS;

BACTERIAL PROTEIN KINASES; CYSTIC FIBROSIS; HISTIDINE KINASES; MACROPHAGES; PHOSPHORYLATION; PROTEASE; TRANSCRIPTION REGULATION; VIRULENCE FACTORS;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA INFECTIONS; CELL LINE; MICE; PHOSPHORYLATION; PROTEIN KINASES; QUORUM SENSING; SIGNAL TRANSDUCTION;

EID: 84886935416     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.489914     Document Type: Article

References (46)

1. Wolanin, P. M., Thomason, P. A., and Stock, J. B. (2002) Histidine protein kinases. Key signal transducers outside the animal kingdom. Genome Biol. 3, REVIEWS3013
2. Krell, T., Lacal, J., Busch, A., Silva-Jiménez, H., Guazzaroni, M. E., and Ramos, J. L. (2010) Bacterial sensor kinases. Diversity in the recognition of environmental signals. Annu. Rev. Microbiol. 64, 539-559
3. Georgellis, D., Lynch, A. S., and Lin, E. C. (1997) In vitro phosphorylation study of the arc two-component signal transduction system of Escherichia coli. J. Bacteriol. 179, 5429-5435
4. Uhl, M. A., and Miller, J. F. (1994) Autophosphorylation and phosphotransfer in the Bordetella pertussis BvgAS signal transduction cascade. Proc. Natl. Acad. Sci. U.S.A. 91, 1163-1167
5. Mahenthiralingam, E., Baldwin, A., and Dowson, C. G. (2008) Burkholderia cepacia complex bacteria. Opportunistic pathogens with important natural biology. J. Appl. Microbiol. 104, 1539-1551
6. Vandamme, P., and Dawyndt, P. (2011) Classification and identification of the Burkholderia cepacia complex. Past, present, and future. Syst. Appl. Microbiol. 34, 87-95
7. Bevivino, A., Costa, B., Cantale, C., Cesarini, S., Chiarini, L., Tabacchioni, S., Caballero-Mellado, J., and Dalmastri, C. (2011) Genetic relationships among Italian and Mexican maize-rhizosphere Burkholderia cepacia complex (BCC) populations belonging to Burkholderia cenocepacia IIIB and BCC6 group. BMC Microbiol. 11, 228
8. McNeely, D., Moore, J. E., Elborn, J. S., Millar, B. C., Rendall, J., and Dooley, J. S. (2009) Isolation of Burkholderia cenocepacia and Burkholderia vietnamiensis from human sewage. Int. J. Environ. Health Res. 19, 157-162
9. Lee, Y. A., and Chan, C. W. (2007) Molecular typing and presence of genetic markers among strains of banana finger-tip rot pathogen, Burkholderia cenocepacia, in Taiwan. Phytopathology 97, 195-201
10. Burkholder, W. H. (1950) Sour skin, a bacterial rot of onion bulbs. Phytopathol. 40, 115-117
11. Vergunst, A. C., Meijer, A. H., Renshaw, S. A., and O'Callaghan, D. (2010) Burkholderia cenocepacia creates an intramacrophage replication niche in zebrafish embryos, followed by bacterial dissemination and establishment of systemic infection. Infect. Immun. 78, 1495-1508
12. Uehlinger, S., Schwager, S., Bernier, S. P., Riedel, K., Nguyen, D. T., Sokol, P. A., and Eberl, L. (2009) Identification of specific and universal virulence factors in Burkholderia cenocepacia strains by using multiple infection hosts. Infect. Immun. 77, 4102-4110
13. Lamothe, J., Huynh, K. K., Grinstein, S., and Valvano, M. A. (2007) Intracellular survival of Burkholderia cenocepacia in macrophages is associated with a delay in the maturation of bacteria-containing vacuoles. Cell. Microbiol. 9, 40-53
14. Lamothe, J., Thyssen, S., and Valvano, M. A. (2004) Burkholderia cepacia complex isolates survive intracellularly without replication within acidic vacuoles of Acanthamoeba polyphaga. Cell. Microbiol. 6, 1127-1138
15. Aubert, D. F., Flannagan, R. S., and Valvano, M. A. (2008) A novel sensor kinase-response regulator hybrid controls biofilm formation and type VI secretion system activity in Burkholderia cenocepacia. Infect. Immun. 76, 1979-1991
16. Aubert, D. F., O'Grady, E. P., Hamad, M. A., Sokol, P. A., and Valvano, M. A. (2013) The Burkholderia cenocepacia sensor kinase hybrid AtsR is a global regulator modulating quorum-sensing signalling. Environ. Microbiol. 15, 372-385
17. Baldwin, A., Sokol, P. A., Parkhill, J., and Mahenthiralingam, E. (2004) The Burkholderia cepacia epidemic strain marker is part of a novel genomic island encoding both virulence and metabolism-associated genes in Burkholderia cenocepacia. Infect. Immun. 72, 1537-1547
18. Kooi, C., Subsin, B., Chen, R., Pohorelic, B., and Sokol, P. A. (2006) Burkholderia cenocepacia ZmpB is a broad-specificity zinc metalloprotease involved in virulence. Infect. Immun. 74, 4083-4093
19. Malott, R. J., Baldwin, A., Mahenthiralingam, E., and Sokol, P. A. (2005) Characterization of the cciIR quorum-sensing system in Burkholderia cenocepacia. Infect. Immun. 73, 4982-4992
20. Malott, R. J., O'Grady, E. P., Toller, J., Inhülsen, S., Eberl, L., and Sokol, P. A. (2009) A Burkholderia cenocepacia orphan LuxR homolog is involved in quorum-sensing regulation. J. Bacteriol. 191, 2447-2460
21. Sokol, P. A., Sajjan, U., Visser, M. B., Gingues, S., Forstner, J., and Kooi, C. (2003) The CepIR quorum-sensing system contributes to the virulence of Burkholderia cenocepacia respiratory infections. Microbiology 149, 3649 -3658
22. Rosales-Reyes, R., Skeldon, A. M., Aubert, D. F., and Valvano, M. A. (2012) The type VI secretion system of Burkholderia cenocepacia affects multiple Rho family GTPases disrupting the actin cytoskeleton and the assembly of NADPH oxidase complex in macrophages. Cell. Microbiol. 14, 255-273
23. Galperin, M. Y. (2006) Structural classification of bacterial response regulators. Diversity of output domains and domain combinations. J. Bacteriol. 188, 4169-4182
24. Finn, R. D., Mistry, J., Tate, J., Coggill, P., Heger, A., Pollington, J. E., Gavin, O. L., Gunasekaran, P., Ceric, G., Forslund, K., Holm, L., Sonnhammer, E. L., Eddy, S. R., and Bateman, A. (2010) The Pfam protein families database. Nucleic Acids Res. 38, D211-D222
25. Sambrook, J., and Russell, D. W. (2006) The condensed protocols from molecular cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
26. Cohen, S. N., Chang, A. C., and Hsu, L. (1972) Nonchromosomal antibiotic resistance in bacteria. Genetic transformation of Escherichia coli by R-factor DNA. Proc. Natl. Acad. Sci. U.S.A. 69, 2110-2114
27. Craig, F. F., Coote, J. G., Parton, R., Freer, J. H., and Gilmour, N. J. (1989) A plasmid which can be transferred between Escherichia coli and Pasteurella haemolytica by electroporation and conjugation. J. Gen. Microbiol. 135, 2885-2890
28. Figurski, D. H., and Helinski, D. R. (1979) Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. U.S.A. 76, 1648-1652
29. Flannagan, R. S., Linn, T., and Valvano, M. A. (2008) A system for the construction of targeted unmarked gene deletions in the genus Burkholderia. Environ. Microbiol. 10, 1652-1660
30. Hamad, M. A., Di Lorenzo, F., Molinaro, A., and Valvano, M. A. (2012) Aminoarabinose is essential for lipopolysaccharide export and intrinsic antimicrobial peptide resistance in Burkholderia cenocepacia. Mol. Microbiol. 85, 962-974
31. Hamad, M. A., Skeldon, A. M., and Valvano, M. A. (2010) Construction of aminoglycoside-sensitive Burkholderia cenocepacia strains for use in studies of intracellular bacteria with the gentamicin protection assay. Appl. Environ Microbiol. 76, 3170-3176
32. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
33. Pérez, J. M., McGarry, M. A., Marolda, C. L., and Valvano, M. A. (2008) Functional analysis of the large periplasmic loop of the Escherichia coli K-12 WaaL O-antigen ligase. Mol. Microbiol. 70, 1424-1440
34. Aubert, D., MacDonald, D. K., and Valvano, M. A. (2010) BcsK(C) is an essential protein for the type VI secretion system activity in Burkholderia cenocepacia that forms an outer membrane complex with BcsL(B). J. Biol. Chem. 285, 35988-35998
35. Goodman, A. L., Kulasekara, B., Rietsch, A., Boyd, D., Smith, R. S., and Lory, S. (2004)Asignaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev. Cell 7, 745-754
36. Laskowski, M. A., Osborn, E., and Kazmierczak, B. I. (2004)Anovel sensor kinase-response regulator hybrid regulates type III secretion and is required for virulence in Pseudomonas aeruginosa. Mol. Microbiol. 54, 1090-1103
37. Ventre, I., Goodman, A. L., Vallet-Gely, I., Vasseur, P., Soscia, C., Molin, S., Bleves, S., Lazdunski, A., Lory, S., and Filloux, A. (2006) Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatoryRNA and virulence genes. Proc. Natl. Acad. Sci. U.S.A. 103, 171-176
38. Stock, J. B., Ninfa, A. J., and Stock, A. M. (1989) Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol. Rev. 53, 450-490
39. Jourlin, C., Ansaldi, M., and Méjean, V. (1997) Transphosphorylation of the TorR response regulator requires the three phosphorylation sites of the TorS unorthodox sensor in Escherichia coli. J. Mol. Biol. 267, 770-777
40. Kwon, O., Georgellis, D., and Lin, E. C. (2000) Phosphorelay as the sole physiological route of signal transmission by the arc two-component system of Escherichia coli. J. Bacteriol. 182, 3858-3862
41. Perraud, A. L., Kimmel, B., Weiss, V., and Gross, R. (1998) Specificity of the BvgAS and EvgAS phosphorelay is mediated by the C-terminal HPt domains of the sensor proteins. Mol. Microbiol. 27, 875-887
42. Chang, C. H., Zhu, J., and Winans, S. C. (1996) Pleiotropic phenotypes caused by genetic ablation of the receiver module of the Agrobacterium tumefaciens VirA protein. J. Bacteriol. 178, 4710-4716
43. Yamamoto, K., Hirao, K., Oshima, T., Aiba, H., Utsumi, R., and Ishihama, A. (2005) Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J. Biol. Chem. 280, 1448-1456
44. Castelli, M. E., García Véscovi, E., and Soncini, F. C. (2000) The phosphatase activity is the target forMg2 regulation of the sensor protein PhoQ in Salmonella. J. Biol. Chem. 275, 22948-22954
45. Hsing, W., and Silhavy, T. J. (1997) Function of conserved histidine 243 in phosphatase activity of EnvZ, the sensor for porin osmoregulation in Escherichia coli. J. Bacteriol. 179, 3729-3735
46. Mahenthiralingam, E., Coenye, T., Chung, J. W., Speert, D. P., Govan, J. R., Taylor, P., and Vandamme, P. (2000) Diagnostically and experimentally useful panel of strains from the Burkholderia cepacia complex. J. Clin. Microbiol. 38, 910-913