Analysis of the Actinobacillus pleuropneumoniae HlyX (FNR) regulon and identification of iron-regulated protein B as an essential virulence factor

Proteomics

Volumn 9, Issue 9, 2009, Pages 2383-2398

  Buettner, Falk F R ^a   Bendalla, Ibrahim M ^a   Bossé, Janine T ^b   Meens, Jochen ^a   Nash, John H E ^c   Härtig, Elisabeth ^d   Langford, Paul R ^b   Gerlachh, Gerald F ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^d TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

Bacteria; cDNA microarray; Electrospray ionization quadrupole time of flight tandem mass spectrometry; Fluorescence two dimensional difference gel electrophoresis; Ionization time of flight mass spectrometry; Matrix assisted laser desorption

Indexed keywords

HYDROGENASE; IRON BINDING PROTEIN; IRON REGULATED PROTEIN B; OXIDOREDUCTASE; PROTEIN HLYX; REGULATOR PROTEIN; SERINE PROTEINASE; UNCLASSIFIED DRUG;

ACTINOBACILLUS PLEUROPNEUMONIAE; ANAEROBIC GROWTH; ANAEROBIC METABOLISM; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; DOWN REGULATION; FUNCTIONAL PROTEOMICS; GENE EXPRESSION; GENE MUTATION; IRON TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REAL TIME POLYMERASE CHAIN REACTION; REGULON; TRANSCRIPTOMICS; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION; VIRULENCE;

ACTINOBACILLUS PLEUROPNEUMONIAE; ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; DNA-BINDING PROTEINS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION, BACTERIAL; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REGULON; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE DELETION; SWINE; TRANSCRIPTION FACTORS; VIRULENCE FACTORS;

ACTINOBACILLUS PLEUROPNEUMONIAE; NEGIBACTERIA; SUIDAE; SUS;

EID: 66249093160     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200800439     Document Type: Article

References (59)

1. Fenwick, B., Henry, S., Porcine pleuropneumonia. J. Am. Vet. Med. Assoc. 1994, 204, 1334-1340.
2. Nicolet, J., in: Leman, A. D., Straw, B. (Eds.), Diseases of Swine, 7th ed., Iowa State University Press, Ames, Iowa, USA 1992, pp. 215-225.
3. Bosse, J. T., Janson, H., Sheehan, B. J., Beddek, A. J. et al., Actinobacillus pleuropneumoniae: pathobiology and pathogenesis of infection. Microbes Infect. 2002, 4, 225-235.
4. Rycroft, A. N., Garside, L. H., Actinobacillus species and their role in animal disease. Vet. J. 2000, 159, 18-36.
5. Worlitzsch, D., Tarran, R., Ulrich, M., Schwab, U. et al., Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J. Clin. Invest. 2002, 109, 317-325.
6. Jacobsen, I., Hennig-Pauka, I., Baltes, N., Trost, M., Gerlach, G.-F., Enzymes involved in anaerobic respiration appear to play a role in Actinobacillus pleuropneumoniae virulence. Infect. Immun. 2005, 73, 226-234.
7. Baltes, N., Hennig-Pauka, I., Jacobsen, I., Gruber, A. D., Ger- lach, G.-F., Identification of dimethyl sulfoxide reductase in Actinobacillus pleuropneumoniae and its role in infection. Infect. Immun. 2003, 71, 6784-6792.
8. Buettner, F. F., Maas, A., Gerlach, G.-F., An Actinobacillus pleuropneumoniae arcA deletion mutant is attenuated and deficient in biofilm formation. Vet. Microbiol. 2008, 127,106-115.
9. Baltes, N., N'Diaye, M., Jacobsen, I. D., Maas, A. etal., Deletion of the anaerobic regulator HlyX causes reduced colonization and persistence of Actinobacillus pleuropneumoniae in the porcine respiratory tract. Infect. Immun. 2005, 73, 4614-4619.
10. Green, J., Baldwin, M. L., HlyX, the FNR homologue of Acti- nobacillus pleuropneumoniae, is a [4Fe-4S]-containing oxygen-responsive transcription regulator that anaerobically activates FNR-dependent class I promoters via an enhanced AR1 contact. Mol. Microbiol. 1997, 24, 593-605.
11. Constantinidou, C., Hobman, J. L., Griffiths, L., Patel, M. D. et al., A reassessment of the FNR regulon and transcriptomic analysis of the effects of nitrate, nitrite, NarXL, and NarQP as Escherichia coli K12 adapts from aerobic to anaerobic growth. J. Biol. Chem. 2006, 281, 4802-4815.
12. Salmon, K., Hung, S. P., Mekjian, K., Baldi, P. et al., Global gene expression profiling in Escherichia coliK12. The effects of oxygen availability and FNR. J. Biol. Chem. 2003, 278, 29837-29855.
13. Kang, Y., Weber, K. D., Qiu, Y., Kiley, P. J., Blattner, F. R., Genome-wide expression analysis indicates that FNR of Escherichia coli K-12 regulates a large number of genes of unknown function. J. Bacteriol. 2005, 187, 1135-1160.
14. Whitehead, R. N., Overton, T. W., Snyder, L. A., McGowan, S. J. et al., The small FNR regulon of Neisseria gonorrhoeae. comparison with the larger Escherichia coli FNR regulon and interaction with the NarQ-NarP regulon. BMC Genomics 2007, 8,35.
15. Fink, R. C., Evans, M. R., Porwollik, S., Vazquez-Torres, A. et al., FNR is a global regulator of virulence and anaerobic metabolism in Salmonella enterica serovar Typhimurium (ATCC 14028s). J. Bacteriol. 2007, 189, 2262-2273.
16. Candiano, G., Bruschi, M., Musante, L., Santucci, L. et al., Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 2004, 25, 1327-1333.
17. Shevchenko, A., Wilm, M., Vorm, O., Mann, M., Mass spec- trometric sequencing of proteins silver-stained polyacryl- amide gels. Anal. Chem. 1996, 68, 850-858.
18. Deslandes, V., Nash, J. H., Harel, J., Coulton, J. W., Jacques, M., Transcriptional profiling of Actinobacillus pleur- opneumoniae under iron-restricted conditions. BMC Geno- mics 2007, 8,72.
19. Buettner, F. F., Bendallah, I. M., Bosse, J. T., Dreckmann, K. et al., Analysis of the Actinobacillus pleuropneumoniae ArcA regulon identifies fumarate reductase as a determinant of virulence. Infect. Immun. 2008, 76, 2284-2295.
20. Oswald, W., Tonpitak, W., Ohrt, Gerlach, G.-F., A single-step transconjugation system for the introduction of unmarked deletions into Actinobacillus pleuropneumoniae serotype 7 using a sucrose sensitivity marker. FEMS Microbiol. Lett. 1999, 179, 153-160.
21. Sambrook, J., Fritsch, E. F., Maniatis, T., Molecular Cloning: A Laboratory Manual. 1999, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
22. Deneer, H. G., Potter, A. A., Effect of iron restriction on the outer membrane poteins of Actinobacillus (Haemophilus) pleuropneumoniae. Infect. Immun. 1989, 57, 798-804.
23. Maas, A., Jacobsen, I. D., Meens, J., Gerlach, G-F., Use of an Actinobacillus pleuropneumoniae multiple mutant as a vaccine that allows differentiation of vaccinated and infected animals. Infect. Immun. 2006, 74, 4124-4132.
24. Jacobsen, M. J., Nielsen, J. P., Development and evaluation of a selective and indicative medium for isolation of Actinobacillus pleuropneumoniae from tonsils. Vet. Microbiol. 1995, 47, 191-197.
25. Tatusov, R. L., Koonin, E. V., Lipman, D. J., A genomic perspective on protein families. Science 1997, 278, 631-637.
26. Reents, H., Munch, R., Dammeyer, T., Jahn, D., Hartig, E., The Fnr regulon of Bacillus subtilis. J. Bacteriol. 2006, 188, 1103-1112.
27. MacInnes, J. I., Kim, J. E., Lian, C. J., Soltes, G. A., Actino- bacillus pleuropneumoniae hlyX gene homology with the fnr gene of Escherichia coli. J. Bacteriol. 1990, 172, 4587-4592.
28. Fritz, C., Maass, S., Kreft, A., Bange, F. C., Dependence of Mycobacterium bovis BCG on anaerobic nitrate reductase for persistence is tissue specific. Infect. Immun. 2002, 70, 286-291.
29. Van Alst, N. E., Picardo, K. F., Iglewski, B. H., Haidaris, C. G., Nitrate sensing and metabolism modulate motility, biofilm formation, and virulence in Pseudomonas aeruginosa. Infect. Immun. 2007, 75, 3780-3790.
30. Mellies, J., Jose, J., Meyer, T. F., The Neisseria gonorrhoeae gene aniA encodes an inducible nitrite reductase. Mol. Gen. Genet. 1997, 256, 525-532.
31. Philippot, L., Denitrification in pathogenic bacteria: for better or worst? Trends Microbiol. 2005, 13, 191-192.
32. Wang, H., Tseng, C. P., Gunsalus, R. P., The napF and narG nitrate reductase operons in Escherichia coli are differentially expressed in response to submicromolar oncentrations of nitrate but not nitrite. J. Bacteriol. 1999, 181, 5303-5308.
33. Jungst, A., Wakabayashi, S., Matsubara, H., Zumft, W. G., The nirSTBM region coding for cytochrome cd1-dependent nitrite respiration of Pseudomonas stutzeri consists of a cluster of mono-, di-, and tetraheme proteins. FEBS Lett. 1991, 279,205-209.
34. Anjum, M. F., Stevanin, T. M., Read, R. C., Moir, J. W., Nitric oxide metabolism in Neisseria meningitidis. J. Bacteriol. 2002, 184, 2987-2993.
35. Viebrock, A., Zumft, W. G., Molecular cloning, heterologous expression, and primary structure of the structural gene for the copper enzyme nitrous oxide reductase from denitrifying Pseudomonas stutzeri. J. Bacteriol. 1988, 170, 4658-4668.
36. Berks, B. C., Ferguson, S. J., Moir, J. W., Richardson, D. J., Enzymes and associated electron transport systems that catalyse the respiratory reduction of nitrogen oxides and oxyanions. Biochim. Biophys. Acta 1995, 1232, 97-173.
37. Sheehan, B. J., Bosse, J. T., Beddek, A. J., Rycroft, A. N. etal., Identification of Actinobacillus pleuropneumoniae genes important for survival during infection in its natural host. Infect. Immun. 2003, 71, 3960-3970.
38. Bodini, A., D'Orazio, C., Peroni, D. G., Corradi, M. etal., IL-8 and pH values in exhaled condensate after antibiotics in cystic fibrosis children. Int. J. Immunopathol. Pharmacol. 2007, 20, 467-472.
39. Tonpitak, W., Baltes, N., Hennig-Pauka, I., Gerlach, G.-F., Construction of an Actinobacillus pleuropneumoniae sero- type 2 prototype live negative-marker vaccine. Infect. Immun. 2002, 70, 7120-7125.
40. Richard, D. J., Sawers, G., Sargent, F., McWalter, L. et al., Transcriptional regulation in response to oxygen and nitrate ofthe operons encoding the [NiFe] hydrogenases 1 and 2 of Escherichia coli. Microbiology 1999, 145, 2903-2912.
41. Olson, J. W., Maier, R. J., Molecular hydrogen as an energy source for Helicobacter pylori. Science 2002, 298, 1788-1790.
42. Maier, R. J., Olczak, A., Maier, S., Soni, S., Gunn, J., Respiratory hydrogen use by Salmonella enterica serovar Typhimurium is essential for virulence. Infect. Immun. 2004, 72, 6294-6299.
43. Baltes, N., Kyaw, S., Hennig-Pauka, I., Gerlach, G.-F., Lack of influence of the anaerobic [NiFe] hydrogenase and L-1,2 propanediol oxidoreductase on the outcome of Actinoba- cillus pleuropneumoniae serotype 7 infection. Vet. Micro-biol. 2004, 102, 67-72.
44. Heusipp, G., Falker, S., Schmidt, M. A., DNA adenine methylation and bacterial pathogenesis. Int. J. Med. Micro- biol. 2007, 297, 1-7.
45. Low, D. A., Weyand, N. J., Mahan, M. J., Roles of DNA ade- nine methylation in regulating bacterial gene expression and virulence. Infect. Immun. 2001, 69, 7197-7204.
46. Oshima, T., Wada, C., Kawagoe, Y., Ara, T. et al., Genome- wide analysis of deoxyadenosine methyltransferase-medi- ated control of gene expression in Escherichia coli. Mol. Microbiol. 2002, 45, 673-695.
47. Tonpitak, W., Thiede, S., Oswald, W., Baltes, N., Gerlach, G. F., Actinobacillus pleuropneumoniae iron transport: a set of exbBDgenes istranscriptionally linkedtothe tbpBgene and required for utilization of transferrin-bound iron. Infect. Immun. 2000, 68, 1164-1170.
48. Beddek, A. J., Sheehan, B. J., Bosse, J. T., Rycroft, A. N. etal., Two TonB systems in Actinobacillus pleuropneumoniae: their roles in iron acquisition and virulence. Infect. Immun. 2004, 72, 701-708.
49. Jacobsen, I., Gerstenberger, J., Gruber, A. D., Bosse, J. T. et al., Deletion of the ferric uptake regulator Fur impairs the in vitro growth and virulence of Actinobacillus pleuro- pneumoniae. Infect. Immun. 2005, 73, 3740-3744.
50. Dyer, D. W., West, E. P., McKenna, W., Thompson, S. A. etal., A pleiotropic iron-uptake mutant of Neisseria meningitidis lacks a 70-kilodalton iron-regulated protein. Infect. Immun. 1988, 56, 977-983.
51. Beucher, M., Sparling, P. F., Cloning, sequencing, and characterization of the gene encoding FrpB, a major iron-regulated, outer membrane protein of Neisseria gonorrhoeae. J. Bacteriol. 1995, 177, 2041-2049.
52. Carson, S. D., Klebba, P. E., Newton, S. M., Sparling, P. F., Ferric enterobactin binding and utilization by Neisseria gonorrhoeae. J. Bacteriol. 1999, 181, 2895-2901.
53. Reyes-Ramirez, F., Sawers, R. G., Aerobic activation of transcription of the anaerobically inducible Escherichia coli focA-pfl operon by fumarate nitrate regulator. FEMS Microbiol. Lett. 2006, 255, 262-267.
54. Young, G. M., Postle, K., Repression of tonB transcription during anaerobic growth requires Fur binding at the promoter and a second factor binding upstream. Mol. Micro- biol. 1994, 11, 943-954.
55. Wilke, M., Franz, B., Gerlach, G.-F., Characterization of a large transferrin-binding protein from Actinobacillus pleuropneumoniae serotype 7. Zentralbl. Veterinarmed. 1997, 44, 73-86.
56. Chung, J. W., Ng-Thow-Hing, C., Budman, L. I., Gibbs, B. F. et al., Outer membrane proteome of Actinobacillus pleuro- pneumoniae: LC-MS/MS analyses validate in silico predictions. Proteomics 2007, 7, 1854-1865.
57. Ala'Aldeen, D. A., Davies, H. A., Borriello, S. P., Vaccine potential of meningococcal FrpB: studies on surface exposure and functional attributes of common epitopes. Vaccine 1994, 12, 535-541.
58. Thompson, E. A., Feavers, I. M., Maiden, M. C., Antigenic diversity of meningococcal enterobactin receptor FetA, a vaccine component. Microbiology 2003, 149, 1849-1858.
59. Pettersson, A., Kuipers, B., Pelzer, M., Verhagen, E. et al., Monoclonal antibodies against the 70-kilodalton iron-regulated protein of Neisseria meningitidis are bactericidal and strain specific. Infect. Immun. 1990, 58, 3036-3041.