Branched-chain amino acids are required for the survival and virulence of Actinobacillus pleuropneumoniae in swine

Infection and Immunity

Volumn 77, Issue 11, 2009, Pages 4925-4933

  Subashchandrabose, Sargurunathan ^a   LeVeque, Rhiannon M ^a,b   Wagner, Trevor K ^a,b,c   Kirkwood, Roy N ^a   Kiupel, Matti ^a   Mulks, Martha H ^a,b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b OpGen Inc ^*  (United States)

^c OpGen Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (4 ISOPROPYL 4 METHYL 5 OXO 2 IMIDAZOLIN 2 YL)NICOTINATE ISOPROPYLAMMONIUM; ACETOLACTATE SYNTHASE; BACTERIAL PROTEIN; BRANCHED CHAIN AMINO ACID; CHLORIMURON ETHYL; CHLORSULFURON; IMAZAQUIN; IMIDAZOLINE DERIVATIVE; METSULFURON METHYL; PRIMISULFURON; PROTEIN ILVI; PROTEIN LRP; SULFONYLUREA DERIVATIVE; UNCLASSIFIED DRUG;

ACTINOBACILLUS PLEUROPNEUMONIAE; AMINO ACID SYNTHESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CONTROLLED STUDY; GENE EXPRESSION; LUNG ALVEOLUS EPITHELIUM; LUNG LAVAGE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SWINE;

ACETOLACTATE SYNTHASE; ACTINOBACILLUS INFECTIONS; ACTINOBACILLUS PLEUROPNEUMONIAE; AMINO ACIDS, BRANCHED-CHAIN; ANIMALS; BACTERIAL PROTEINS; BRONCHOALVEOLAR LAVAGE FLUID; GENE EXPRESSION REGULATION, BACTERIAL; LEUCINE-RESPONSIVE REGULATORY PROTEIN; MUTATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SWINE; UP-REGULATION; VIRULENCE;

EID: 70350463582     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00671-09     Document Type: Article

References (63)

1. Abul-Milh, M., S. E. Paradis, J. D. Dubreuil, and M. Jacques. 1999. Binding of Actinobacillus pleuropneumoniae lipopolysaccharides to glycosphingolipids evaluated by thin-layer chromatography. Infect. Immun. 67:4983-4987.
2. Baek, C.-H., S. Wang, K. L. Roland, and R. Curtiss III. 2009. Leucine-responsive regulatory protein (Lrp) acts as a virulence repressor in Salmonella enterica serovar Typhimurium. J. Bacteriol. 191:1278-1292.
3. Baughman, R. P., C. H. Bosken, R. G. Loudon, P. Hurtubise, and T. Wesseler. 1983. Quantitation of bronchoalveolar lavage with methylene blue. Am. Rev. Respir. Dis. 128:266-270.
4. Beuzon, C. R., and D. W. Holden. 2001. Use of mixed infections with Salmonella strains to study virulence genes and their interactions in vivo. Microbes Infect. 3:1345-1352.
5. Boigegrain, R.-A., J.-P. Liautard, and S. Kohler. 2005. Targeting of the virulence factor acetohydroxyacid synthase by sulfonylureas results in inhibition of intramacrophagic multiplication of Brucella suis. Antimicrob. Agents Chemother. 49:3922-3925.
6. Bosse, J. T., H. Janson, B. J. Sheehan, A. J. Beddek, A. N. Rycroft, J. S. Kroll, and P. R. Langford. 2002. Actinobacillus pleuropneumoniae: pathobiology and pathogenesis of infection. Microbes Infect. 4:225-235.
7. Boyce, J. D., I. Wilkie, M. Harper, M. L. Paustian, V. Kapur, and B. Adler. 2004. Genomic-scale analysis of Pasteurella multocida gene expression during growth within liver tissue of chickens with fowl cholera. Microbes Infect. 6:290-298.
8. Boyce, J. D., I. Wilkie, M. Harper, M. L. Paustian, V. Kapur, and B. Adler. 2002. Genomic scale analysis of Pasteurella multocida gene expression during growth within the natural chicken host. Infect. Immun. 70:6871-6879.
9. Brennan, R. G., and T. M. Link. 2007. Hfq structure, function, and ligand binding. Curr. Opin. Microbiol. 10:125-133.
10. Brinkman, A. B., T. J. Ettema, W. M. de Vos, and J. van der Oost. 2003. The Lrp family of transcriptional regulators. Mol. Microbiol. 48:287-294.
11. Cai, X., H. Chen, P. J. Blackall, Z. Yin, L. Wang, Z. Liu, and M. Jin. 2005. Serological characterization of Haemophilus parasuis isolates from China. Vet. Microbiol. 111:231-236.
12. Calvo, J. M., and R. G. Matthews. 1994. The leucine-responsive regulatory protein, a global regulator of metabolism in Escherichia coli. Microbiol. Rev. 58:466-490. (Pubitemid 24279100)
13. Chin, N., J. Frey, C. F. Chang, and Y. F. Chang. 1996. Identification of a locus involved in the utilization of iron by Actinobacillus pleuropneumoniae. FEMS Microbiol. Lett. 143:1-6.
14. Cho, B.-K., C. L. Barrett, E. M. Knight, Y. S. Park, and B. O. Palsson. 2008. Genome-scale reconstruction of the Lrp regulatory network in Escherichia coli. Proc. Natl. Acad. Sci. USA 105:19462-19467.
15. Cowles, K. N., C. E. Cowles, G. R. Richards, E. C. Martens, and H. Goodrich-Blair. 2007. The global regulator Lrp contributes to mutualism, pathogenesis and phenotypic variation in the bacterium Xenorhabdus nematophila. Cell Microbiol. 9:1311-1323.
16. Duggleby, R. G., and S. S. Pang. 2000. Acetohydroxyacid synthase. J. Biochem. Mol. Biol. 33:1-36.
17. Fenwick, B. W., B. I. Osburn, and H. J. Olander. 1986. Isolation and biological characterization of two lipopolysaccharides and a capsular-enriched polysaccharide preparation from Haemophilus pleuropneumoniae. Am. J. Vet. Res. 47:1433-1441.
18. Foote, S. J., J. T. Bosse, A. B. Bouevitch, P. R. Langford, N. M. Young, and J. H. Nash. 2008. The complete genome sequence of Actinobacillus pleuropneumoniae L20 (serotype 5b). J. Bacteriol. 190:1495-1496.
19. Fraser, G. M., L. Claret, R. Furness, S. Gupta, and C. Hughes. 2002. Swarming-coupled expression of the Proteus mirabilis hpmBA haemolysin operon. Microbiology 148:2191-2201.
20. Frey, J. 1995. Virulence in Actinobacillus pleuropneumoniae and RTX toxins. Trends Microbiol. 3:257-261.
21. Fuller, T. E., M. J. Kennedy, and D. E. Lowery. 2000. Identification of Pasteurella multocida virulence genes in a septicemic mouse model using signature-tagged mutagenesis. Microb. Pathog. 29:25-38.
22. Fuller, T. E., R. J. Shea, B. J. Thacker, and M. H. Mulks. 1999. Identification of in vivo induced genes in Actinobacillus pleuropneumoniae. Microb. Pathog. 27:311-327.
23. Fuller, T. E., B. J. Thacker, and M. H. Mulks. 1996. A riboflavin auxotroph of Actinobacillus pleuropneumoniae is attenuated in swine. Infect. Immun. 64:4659-4664.
24. Gally, D. L., T. J. Rucker, and I. C. Blomfield. 1994. The leucine-responsive regulatory protein binds to the fim switch to control phase variation of type 1 fimbrial expression in Escherichia coli K-12. J. Bacteriol. 176:5665-5672.
25. Grandoni, J. A., P. T. Marta, and J. V. Schloss. 1998. Inhibitors of branched-chain amino acid biosynthesis as potential antituberculosis agents. J. Antimicrob. Chemother. 42:475-482.
26. Haesebrouck, F., K. Chiers, I. Van Overbeke, and R. Ducatelle. 1997. Actinobacillus pleuropneumoniae infections in pigs: the role of virulence factors in pathogenesis and protection. Vet. Microbiol. 58:239-249.
27. Jansen, R., J. Briaire, H. E. Smith, P. Dom, F. Haesebrouck, E. M. Kamp, A. L. Gielkens, and M. A. Smits. 1995. Knockout mutants of Actinobacillus pleuropneumoniae serotype 1 that are devoid of RTX toxins do not activate or kill porcine neutrophils. Infect. Immun. 63:27-37.
28. Jolie, R. A., M. H. Mulks, and B. J. Thacker. 1995. Cross-protection experiments in pigs vaccinated with Actinobacillus pleuropneumoniae subtypes 1A and 1B. Vet. Microbiol. 45:383-391.
29. Lin, W., G. Kovacikova, and K. Skorupski. 2007. The quorum sensing regulator HapR downregulates the expression of the virulence gene transcription factor AphA in Vibrio cholerae by antagonizing Lrp- and VpsR-mediated activation. Mol. Microbiol. 64:953-967.
30. Lintner, R., P. Mishra, P. Srivastava, B. Martinez-Vaz, A. Khodursky, and R. Blumenthal. 2008. Limited functional conservation of a global regulator among related bacterial genera: Lrp in Escherichia coli, Proteus, and Vibrio. BMC Microbiol. 8:60-86. (Pubitemid 351667508)
31. McCourt, J. A., and R. G. Duggleby. 2006. Acetohydroxyacid synthase and its role in the biosynthetic pathway for branched-chain amino acids. Amino Acids 31:173-210.
32. McFarland, K. A., S. Lucchini, J. C. Hinton, and C. J. Dorman. 2008. The leucine-responsive regulatory protein, Lrp, activates transcription of the fim operon in Salmonella enterica serovar Typhimurium via the fimZ regulatory gene. J. Bacteriol. 190:602-612.
33. Mei, J. M., F. Nourbakhsh, C. W. Ford, and D. W. Holden. 1997. Identification of Staphylococcus aureus virulence genes in a murine model of bacteraemia using signature-tagged mutagenesis. Mol. Microbiol. 26:399-407.
34. Miller, V. L., and J. J. Mekalanos. 1988. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170:2575-2583.
35. Mulks, M. H., and J. M. Buysse. 1995. A targeted mutagenesis system for Actinobacillus pleuropneumoniae. Gene 165:61-66.
36. Negrete-Abascal, E., R. M. Garcia, M. E. Reyes, D. Godinez, and M. de la Garza. 2000. Membrane vesicles released by Actinobacillus pleuropneumoniae contain proteases and Apx toxins. FEMS Microbiol. Lett. 191:109-113.
37. Negrete Abascal, E., V. R. Tenorio, J. J. Serrano, C. Garcia, and M. de la Garza. 1994. Secreted proteases from Actinobacillus pleuropneumoniae serotype 1 degrade porcine gelatin, hemoglobin, and immunoglobulin A. Can. J. Vet. Res. 58:83-86.
38. Newman, E. B., and R. Lin. 1995. Leucine-responsive regulatory protein: a global regulator of gene expression in Escherichia coli. Annu. Rev. Microbiol. 49:747-775.
39. Rennard, S. I., G. Basset, D. Lecossier, K. M. O'Donnell, P. Pinkston, P. G. Martin, and R. G. Crystal. 1986. Estimation of volume of epithelial lining fluid recovered by lavage using urea as marker of dilution. J. Appl. Physiol. 60:532-538.
40. Ried, J. L., and A. Collmer. 1987. An nptI-sacB-sacR cartridge for constructing directed, unmarked mutations in gram-negative bacteria by marker exchange- eviction mutagenesis. Gene 57:239-246.
41. Rioux, S., C. Begin, D. Dubreuil, and M. Jacques. 1997. Isolation and characterization of LPS mutants of Actinobacillus pleuropneumoniae serotype 1. Curr. Microbiol. 35:139-144.
42. Rosey, E. L., M. J. Kennedy, and R. J. Yancey. 1996. Dual flaA1 flaB1 mutant of Serpulina hyodysenteriae expressing periplasmic flagella is severely attenuated in a murine model of swine dysentery. Infect. Immun. 64:4154-4162.
43. Simon, R., U. Priefer, and A. Puhler. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gramnegative bacteria. Bio/Technology 1:784-791. (Pubitemid 14239484)
44. Sohn, H., K.-S. Lee, Y.-K. Ko, J.-W. Ryu, J.-C. Woo, D.-W. Koo, S.-J. Shin, S.-J. Ahn, A.-R. Shin, C.-H. Song, E.-K. Jo, J.-K. Park, and H.-J. Kim. 2008. In vitro and ex vivo activity of new derivatives of acetohydroxyacid synthase inhibitors against Mycobacterium tuberculosis and non-tuberculous mycobacteria. Int. J. Antimicrob. Agents 31:567-571.
45. Spackman, D. H., W. H. Stein, and S. Moore. 1958. Automatic recording apparatus for use in chromatography of amino acids. Anal. Chem. 30:1190-1206.
46. Sun, Y.-H., S. Bakshi, R. Chalmers, and C. M. Tang. 2000. Functional genomics of Neisseria meningitidis pathogenesis. Nat. Med. 6:1269-1273.
47. Tascon, R. I., J. A. Vazquez-Boland, C. B. Gutierrez-Martin, I. Rodriguez-Barbosa, and E. F. Rodriguez-Ferri. 1994. The RTX haemolysins ApxI and ApxII are major virulence factors of the swine pathogen Actinobacillus pleuropneumoniae: evidence from mutational analysis. Mol. Microbiol. 14: 207-216.
48. Taylor, D. J. 1999. Actinobacillus pleuropneumoniae, p. 343-354. In B. E. Straw, S. D'Allaire, W. L. Mengeling, and D. J. Taylor (ed.), Diseases of swine, 8th ed. Iowa State University Press, Ames, IA.
49. Toledo-Arana, A., F. Repoila, and P. Cossart. 2007. Small non-coding RNAs controlling pathogenesis. Curr. Opin. Microbiol. 10:182-188.
50. Tonpitak, W., S. Thiede, W. Oswald, N. Baltes, and G. F. Gerlach. 2000. Actinobacillus pleuropneumoniae iron transport: a set of exbBD genes is transcriptionally linked to the tbpB gene and required for utilization of transferrin-bound iron. Infect. Immun. 68:1164-1170.
51. van de Kerkhof, A., F. Haesebrouck, K. Chiers, R. Ducatelle, E. M. Kamp, and M. A. Smits. 1996. Influence of Actinobacillus pleuropneumoniae and its metabolites on porcine alveolar epithelial cells. Infect. Immun. 64:3905-3907.
52. van Leengoed, L. A. M. G., and E. B. Kamp. 1989. A method for bronchoalveolar lavage in live pigs. Vet. Q. 11:65-72.
53. Vieira, J., and J. Messing. 1982. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 19:259-268. (Pubitemid 13201666)
54. Wagner, T. K., and M. H. Mulks. 2007. Identification of the Actinobacillus pleuropneumoniae leucine-responsive regulatory protein and its involvement in the regulation of in vivo-induced genes. Infect. Immun. 75:91-103.
55. Wagner, T. K., and M. H. Mulks. 2006. A subset of Actinobacillus pleuropneumoniae in vivo induced promoters respond to branched-chain amino acid limitation. FEMS Immunol. Med. Microbiol. 48:192-204.
56. Wang, J., A. Mushegian, S. Lory, and S. Jin. 1996. Large-scale isolation of candidate virulence genes of Pseudomonas aeruginosa by in vivo selection. Proc. Natl. Acad. Sci. USA 93:10434-10439.
57. Ward, C. K., and T. J. Inzana. 1994. Resistance of Actinobacillus pleuropneumoniae to bactericidal antibody and complement is mediated by capsular polysaccharide and blocking antibody specific for lipopolysaccharide. J. Immunol. 153:2110-2121.
58. Ward, C. K., M. L. Lawrence, H. P. Veit, and T. J. Inzana. 1998. Cloning and mutagenesis of a serotype-specific DNA region involved in encapsulation and virulence of Actinobacillus pleuropneumoniae serotype 5a: concomitant expression of serotype 5a and 1 capsular polysaccharides in recombinant A. pleuropneumoniae serotype 1. Infect. Immun. 66:3326-3336.
59. West, S. E., M. J. Romero, L. B. Regassa, N. A. Zielinski, and R. A. Welch. 1995. Construction of Actinobacillus pleuropneumoniae-Escherichia coli shuttle vectors: expression of antibiotic-resistance genes. Gene 160:81-86.
60. Weyand, N. J., and D. A. Low. 2000. Regulation of Pap phase variation. Lrp is sufficient for the establishment of the phase off pap DNA methylation pattern and repression of pap transcription in vitro. J. Biol. Chem. 275:3192-3200.
61. Xu, Z., Y. Zhou, L. Li, R. Zhou, S. Xiao, Y. Wan, S. Zhang, K. Wang, W. Li, H. Jin, M. Kang, B. Dalai, T. Li, L. Liu, Y. Cheng, L. Zhang, T. Xu, H. Zheng, S. Pu, B. Wang, W. Gu, X. L. Zhang, G. F. Zhu, S. Wang, G. P. Zhao, and H. Chen. 2008. Genome biology of Actinobacillus pleuropneumoniae JL03, an isolate of serotype 3 prevalent in China. PLoS ONE. 3:e1450.
62. Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119. (Pubitemid 15122816)
63. Zhang, Y., J. M. Tennent, A. Ingham, G. Beddome, C. Prideaux, and W. P. Michalski. 2000. Identification of type 4 fimbriae in Actinobacillus pleuropneumoniae. FEMS Microbiol. Lett. 189:15-18.