Analysis of the Actinobacillus pleuropneumoniae ArcA regulon identifies fumarate reductase as a determinant of virulence

Infection and Immunity

Volumn 76, Issue 6, 2008, Pages 2284-2295

  Buettner, Falk F R ^a   Bendallah, Ibrahim M ^a   Bosse, Janine T ^b   Dreckmann, Karla ^a   Nash, John H E ^c   Langford, Paul R ^b   Gerlach, Gerald F ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AEROBIC RESPIRATION CONTROL PROTEIN A; FUMARATE REDUCTASE; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; PROTEOME; SUCCINIC ACID; TRANSCRIPTOME; VIRULENCE FACTOR; BACTERIAL PROTEIN; SUCCINATE DEHYDROGENASE;

ACTINOBACILLUS PLEUROPNEUMONIAE; AEROSOL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL INFECTION; BREATHING; CITRIC ACID CYCLE; COMPUTER MODEL; CONTROLLED STUDY; DELETION MUTANT; ENZYME SYNTHESIS; GENE EXPRESSION; IMMUNE RESPONSE; MASS SPECTROMETRY; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULON; SWINE; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION; ANIMAL; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GERMFREE ANIMAL; IMMUNOLOGY; MALE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; RANDOMIZATION; VIRULENCE;

ACTINOBACILLUS INFECTIONS; ACTINOBACILLUS PLEUROPNEUMONIAE; ANIMALS; BACTERIAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; MALE; RANDOM ALLOCATION; REGULON; SPECIFIC PATHOGEN-FREE ORGANISMS; SUCCINATE DEHYDROGENASE; SWINE; VIRULENCE;

EID: 46249098261     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01540-07     Document Type: Article

References (59)

1. Anderson, C., A. A. Potter, and G.-F. Gerlach. 1991. Isolation and molecular characterization of spontaneously occurring cytolysin-negative mutants of Actinobacillus pleuropneumoniae serotype 7. Infect. Immun. 59:4110-4116.
2. Ashworth, J. M., and H. L. Kornberg. 1966. The anaplerotic fixation of carbon dioxide by Escherichia coli. Proc. R. Soc. Lond. B 165:179-188.
3. Baltes, N., I. Hennig-Pauka, I. Jacobsen, A. D. Gruber, and G.-F. Gerlach. 2003. Identification of dimethyl sulfoxide reductase in Actinobacillus pleuropneumoniae and its role in infection. Infect. Immun. 71:6784-6792.
4. Baltes, N., M. N'diaye, I. D. Jacobsen, A. Maas, F. F. Buettner, and G.-F. Gerlach. 2005. Deletion of the anaerobic regulator HlyX causes reduced colonization and persistence of Actinobacillus pleuropneumoniae in the porcine respiratory tract. Infect. Immun. 73:4614-4619.
5. Boonstra, J., J. A. Downie, and W. N. Konings. 1978. Energy supply for active transport in anaerobically grown Escherichia coli. J. Bacteriol. 136:844-853.
6. Bosse, J. T., H. Janson, B. J. Sheehan, A. J. Beddek, A. N. Rycroft, K. J. Simon, and P. R. Langford. 2002. Actinobacillus pleuropneumoniae: pathobiology and pathogenesis of infection. Microbes Infect. 4:225-235.
7. Boulette, M. L., and S. M. Payne. 2007. Anaerobic regulation of Shigella flexneri virulence: ArcA regulates fur and iron acquisition genes. J. Bacteriol. 189:6957-6967.
8. Buettner, F. F., A. Maas, and G.-F. Gerlach. 2008. An Actinobacillus pleuropneumoniae arcA deletion mutant is attenuated and deficient in biofilm formation. Vet. Microbiol. 127:106-115.
9. Clark, D. P. 1989. The fermentation pathways of Escherichia coli. FEMS Microbiol. Rev. 5:223-234.
10. Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
11. Dehio, C., and M. Meyer. 1997. Maintenance of broad-host-range incompatibility group P and group Q plasmids and transposition of Tn5 in Bartonella henselae following conjugal plasmid transfer from Escherichia coli. J. Bacteriol. 179:538-540.
12. Deslandes, V., J. H. Nash, J. Harel, J. W. Coulton, and M. Jacques. 2007. Transcriptional profiling of Actinobacillus pleuropneumoniae under iron-restricted conditions. BMC Genomics 8:72.
13. De Souza-Hart, J. A., W. Blackstock, V. Di Modugno, I. B. Holland, and M. Kok. 2003. Two-component systems in Haemophilus influenzae: a regulatory role for ArcA in serum resistance. Infect. Immun. 71:163-172.
14. Dom, P., F. Haesebrouck, R. Ducatelle, and G. Charlier. 1994. In vivo association of Actinobacillus pleuropneumoniae serotype 2 with the respiratory epithelium of pigs. Infect. Immun. 62:1262-1267.
15. Dorrell, N., M. C. Martino, R. A. Stabler, S. J. Ward, Z. W. Zhang, A. A. McColm, M. J. Farthing, and B. W. Wren. 1999. Characterization of Helicobacter pylori PldA, a phospholipase with a role in colonization of the gastric mucosa. Gastroenterology 117:1098-1104.
16. Fenwick, B., and S. Henry. 1994. Porcine pleuropneumonia. J. Am. Vet. Med. Assoc. 204:1334-1340.
17. Ge, Z. 2002. Potential of fumarate reductase as a novel therapeutic target in Helicobacter pylori infection. Expert Opin. Ther. Targets 6:135-146.
18. Ge, Z., Y. Feng, C. A. Dangler, S. Xu, N. S. Taylor, and J. G. Fox. 2000. Fumarate reductase is essential for Helicobacter pylori colonization of the mouse stomach. Microb. Pathog. 29:279-287.
19. Gerard, H. C., J. Freise, Z. Wang, G. Roberts, D. Rudy, B. Krauss-Opatz, L. Kohler, H. Zeidler, H. R. Schumacher, J. A. Whittum-Hudson, and A. P. Hudson. 2002. Chlamydia trachomatis genes whose products are related to energy metabolism are expressed differentially in active vs. persistent infection. Microbes Infect. 4:13-22.
20. Goethe, R., O. F. Gonzales, T. Lindner, and G. F. Gerlach. 2000. A novel strategy for protective Actinobacillus pleuropneumoniae subunit vaccines: detergent extraction of cultures induced by iron restriction. Vaccine 19:966-975.
21. Gralnick, J. A., C. T. Brown, and D. K. Newman. 2005. Anaerobic regulation by an atypical Arc system in Shewanella oneidensis. Mol. Microbiol. 56:1347-1357.
22. Hannan, P. C., B. S. Bhogal, and J. P. Fish. 1982. Tylosin tartrate and tiamutilin effects on experimental piglet pneumonia induced with pneumonic pig lung homogenate containing mycoplasmas, bacteria and viruses. Res. Vet. Sci. 33:76-88.
23. Ingledew, W. J., and R. K. Poole. 1984. The respiratory chains of Escherichia coli. Microbiol. Rev. 48:222-271.
24. Iuchi, S., and E. C. Lin. 1988. arcA (dye), a global regulatory gene in Escherichia coli mediating repression of enzymes in aerobic pathways. Proc. Natl. Acad. Sci. USA 85:1888-1892.
25. Jacobs, N. J., and P. J. VanDemark. 1960. Comparison of the mechanism of glycerol oxidation in aerobically and anaerobically grown Streptococcus faecalis. J. Bacteriol. 79:532-538.
26. Jacobsen, I., I. Hennig-Pauka, N. Baltes, M. Trost, and G. F. Gerlach. 2005. Enzymes involved in anaerobic respiration appear to play a role in Actinobacillus pleuropneumoniae virulence. Infect. Immun. 73:226-234.
27. Jacobsen, M. J., and J. P. Nielsen. 1995. Development and evaluation of a selective and indicative medium for isolation of Actinobacillus pleuropneumoniae from tonsils. Vet. Microbiol. 47:191-197.
28. Kather, B., K. Stingl, M. E. van der Rest, K. Altendorf, and D. Molenaar. 2000. Another unusual type of citric acid cycle enzyme in Helicobacter pylori: the malate:quinone oxidoreductase. J. Bacteriol. 182:3204-3209.
29. Kramer, A., I. Schwebke, and G. Kampf. 2006. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect. Dis. 6:130.
30. Leiner, G., B. Franz, K. Strutzberg, and G. F. Gerlach. 1999. A novel enzyme-linked immunosorbent assay using the recombinant Actinobacillus pleuropneumoniae ApxII antigen for diagnosis of pleuropneumonia in pig herds. Clin. Diagn. Lab. Immunol. 6:630-632.
31. Liu, X., and P. De Wulf. 2004. Probing the ArcA-P modulon of Escherichia coli by whole genome transcriptional analysis and sequence recognition profiling. J. Biol. Chem. 279:12588-12597.
32. Lorenz, M. C., and G. R. Fink. 2001. The glyoxylate cycle is required for fungal virulence. Nature 412:83-86.
33. Maas, A., I. D. Jacobsen, J. Meens, and G. F. Gerlach. 2006. Use of an Actinobacillus pleuropneumoniae multiple mutant as a vaccine that allows differentiation of vaccinated and infected animals. Infect. Immun. 74:4124-4132.
34. McKinney, J. D., K. Honer zu Bentrup, E. J. Muñoz-Elías, A. Miczak, B. Chen, W.-T. Chan, D. Swenson, J. C. Sacchettini, W. R. Jacobs, Jr., and D. G. Russell. 2000. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406:735-738.
35. Mendz, G. L., and S. L. Hazell. 1993. Fumarate catabolism in Helicobacter pylori. Biochem. Mol. Biol. Int. 31:325-332.
36. Mendz, G. L., S. L. Hazell, and S. Srinivasan. 1995. Fumarate reductase: a target for therapeutic intervention against Helicobacter pylori. Arch. Biochem. Biophys. 321:153-159.
37. Miki, K., and E. C. Lin. 1975. Anaerobic energy-yielding reaction associated with transhydrogenation from glycerol 3-phosphate to fumarate by an Escherichia coli system. J. Bacteriol. 124:1282-1287.
38. Miki, K., and T. H. Wilson. 1978. Proton translocation associated with anaerobic transhydrogenation from glycerol 3-phosphate to fumarate in Escherichia coli. Biochem. Biophys. Res. Commun. 83:1570-1575.
39. Molenaar, D., M. E. van der Rest, A. Drysch, and R. Yucel. 2000. Functions of the membrane-associated and cytoplasmic malate dehydrogenases in the citric acid cycle of Corynebacterium glutamicum. J. Bacteriol. 182:6884-6891.
40. Omura, S., H. Miyadera, H. Ui, K. Shiomi, Y. Yamaguchi, R. Masuma, T. Nagamitsu, D. Takano, T. Sunazuka, A. Harder, H. Kolbl, M. Namikoshi, H. Miyoshi, K. Sakamoto, and K. Kita. 2001. An anthelmintic compound, nafuredin, shows selective inhibition of complex I in helminth mitochondria. Proc. Natl. Acad. Sci. USA 98:60-62.
41. Oswald, W., W. Tonpitak, G. Ohrt, and G.-F. Gerlach. 1999. A single-step transconjugation system for the introduction of unmarked deletions into Actinobacillus pleuropneumoniae serotype 7 using a sucrose sensitivity marker. FEMS Microbiol. Lett. 179:153-160.
42. Parish, T., D. A. Smith, G. Roberts, J. Betts, and N. G. Stoker. 2003. The senX3-regX3 two-component regulatory system of Mycobacterium tuberculosis is required for virulence. Microbiology 149:1423-1435.
43. Pitson, S. M., G. L. Mendz, S. Srinivasan, and S. L. Hazell. 1999. The tricarboxylic acid cycle of Helicobacter pylori. Eur. J. Biochem. 260:258-267.
44. Raleigh, F. A., K. Lech, and R. Brent. 1989. Selected topics from classical bacterial genetics, p.1.4.1-1.4.14. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, et al. (ed.), Current protocols in molecular biology. Wiley Interscience, New York, NY.
45. Rickman, L., J. W. Saldanha, D. M. Hunt, D. N. Hoar, M. J. Colston, J. B. Millar, and R. S. Buxton. 2004. A two-component signal transduction system with a PAS domain-containing sensor is required for virulence of Mycobacterium tuberculosis in mice. Biochem. Biophys. Res. Commun. 314:259-267.
46. Salmon, K. A., S. P. Hung, N. R. Steffen, R. Krupp, P. Baldi, G. W. Hatfield, and R. P. Gunsalus. 2005. Global gene expression profiling in Escherichia coli K12: effects of oxygen availability and ArcA. J. Biol. Chem. 280:15084-15096.
47. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. Sawers, G., and B. Suppmann. 1992. Anaerobic induction of pyruvate formate-lyase gene expression is mediated by the ArcA and FNR proteins. J. Bacteriol. 174:3474-3478.
49. Schryvers, A., and J. H. Weiner. 1981. The anaerobic sn-glycerol-3-phosphate dehydrogenase of Escherichia coli: purification and characterization. J. Biol. Chem. 256:9959-9965.
50. Sengupta, N., K. Paul, and R. Chowdhury. 2003. The global regulator ArcA modulates expression of virulence factors in Vibrio cholerae. Infect. Immun. 71:5583-5589.
51. Shevchenko, A., M. Wilm, O. Vorm, and M. Mann. 1996. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68: 850-858.
52. Shuman, S. 1994. Novel approach to molecular cloning and polynucleotide synthesis using vaccinia DNA topoisomerase. J. Biol. Chem. 269:32678-32684.
53. Tatusov, R. L., E. V. Koonin, and D. J. Lipman. 1997. A genomic perspective on protein families. Science 278:631-637.
54. Tchawa Yimga, M., M. P. Leatham, J. H. Allen, D. C. Laux, T. Conway, and P. S. Cohen. 2006. Role of gluconeogenesis and the tricarboxylic acid cycle in the virulence of Salmonella enterica serovar Typhimurium in BALB/c mice. Infect. Immun. 74:1130-1140.
55. Ui, H., K. Shiomi, Y. Yamaguchi, R. Masuma, T. Nagamitsu, D. Takano, T. Sunazuka, M. Namikoshi, and S. Omura. 2001. Nafuredin, a novel inhibitor of NADH-fumarate reductase, produced by Aspergillus niger FT-0554. J. Antibiot. (Tokyo) 54:234-238.
56. +/ATP coupling ratio of the ATP synthase from thiol-modulated chloroplasts and two cyanobacterial strains is four. FEBS Lett. 379:309-313.
57. Weitzman, P. D. 1987. Patterns of diversity of citric acid cycle enzymes. Biochem. Soc. Symp. 54:33-43.
58. Willson, P. J., W. L. Albritton, L. Slaney, and J. K. Setlow. 1989. Characterization of a multiple antibiotic resistance plasmid from Haemophilus ducreyi. Antimicrob. Agents Chemother. 33:1627-1630.
59. Wong, S. M., K. R. Alugupalli, S. Ram, and B. J. Akerley. 2007. The ArcA regulon and oxidative stress resistance in Haemophilus influenzae. Mol. Microbiol. 64:1375-1390.