Type IV fimbrial subunit protein ApfA contributes to protection against porcine pleuropneumonia
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, randomizované kontrolované studie, práce podpořená grantem
PubMed
22240397
PubMed Central
PMC3276438
DOI
10.1186/1297-9716-43-2
PII: 1297-9716-43-2
Knihovny.cz E-zdroje
- MeSH
- Actinobacillus pleuropneumoniae genetika imunologie patogenita MeSH
- bakteriální adheziny genetika imunologie MeSH
- bakteriální fimbrie genetika imunologie MeSH
- bakteriální vakcíny genetika imunologie MeSH
- Escherichia coli genetika MeSH
- exotoxiny genetika metabolismus MeSH
- faktory virulence genetika imunologie MeSH
- infekce bakteriemi rodu Actinobacillus imunologie prevence a kontrola veterinární MeSH
- molekulární sekvence - údaje MeSH
- nemoci prasat imunologie prevence a kontrola MeSH
- pleuropneumonie imunologie prevence a kontrola veterinární MeSH
- polymerázová řetězová reakce veterinární MeSH
- prasata MeSH
- rekombinantní proteiny genetika imunologie MeSH
- sekvenční analýza DNA veterinární MeSH
- vakcinace veterinární MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- randomizované kontrolované studie MeSH
- Názvy látek
- bakteriální adheziny MeSH
- bakteriální vakcíny MeSH
- exotoxiny MeSH
- faktory virulence MeSH
- rekombinantní proteiny MeSH
Porcine pleuropneumonia caused by Actinobacillus pleuropneumoniae accounts for serious economic losses in the pig farming industry worldwide. We examined here the immunogenicity and protective efficacy of the recombinant type IV fimbrial subunit protein ApfA as a single antigen vaccine against pleuropneumonia, or as a component of a multi-antigen preparation comprising five other recombinant antigens derived from key virulence factors of A. pleuropneumoniae (ApxIA, ApxIIA, ApxIIIA, ApxIVA and TbpB). Immunization of pigs with recombinant ApfA alone induced high levels of specific serum antibodies and provided partial protection against challenge with the heterologous A. pleuropneumoniae serotype 9 strain. This protection was higher than that engendered by vaccination with rApxIVA or rTbpB alone and similar to that observed after immunization with the tri-antigen combination of rApxIA, rApxIIA and rApxIIIA. In addition, rApfA improved the vaccination potential of the penta-antigen mixture of rApxIA, rApxIIA, rApxIIIA, rApxIVA and rTbpB proteins, where the hexa-antigen vaccine containing rApfA conferred a high level of protection on pigs against the disease. Moreover, when rApfA was used for vaccination alone or in combination with other antigens, such immunization reduced the number of pigs colonized with the challenge strain. These results indicate that ApfA could be a valuable component of an efficient subunit vaccine for the prevention of porcine pleuropneumonia.
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Gottschalk M, Taylor DJ. In: Diseases of Swine. 9. Straw BE, Zimmerman JJ, D'Allaire S, Taylor DJ, editor. Ames, Iowa: Blackwell Publishing; 2006. Actinobacillus pleuropneumoniae; pp. 563–576.
Sebunya TN, Saunders JR. Haemophilus pleuropneumoniae infection in swine: a review. J Am Vet Med Assoc. 1983;182:1331–1337. PubMed
Chiers K, De Waele T, Pasmans F, Ducatelle R, Haesebrouck F. Virulence factors of Actinobacillus pleuropneumoniae involved in colonization, persistence and induction of lesions in its porcine host. Vet Res. 2010;41:65. doi: 10.1051/vetres/2010037. PubMed DOI PMC
Bosse JT, Janson H, Sheehan BJ, Beddek AJ, Rycroft AN, Kroll JS, Langford PR. Actinobacillus pleuropneumoniae : pathobiology and pathogenesis of infection. Microbes Infect. 2002;4:225–235. doi: 10.1016/S1286-4579(01)01534-9. PubMed DOI
Rosendal S, Boyd DA, Gilbride KA. Comparative virulence of porcine Haemophilus bacteria. Can J Comp Med. 1985;49:68–74. PubMed PMC
Shope RE, White DC, Leidy G. Porcine contagious Pleuropneumonia. II. Studies of the pathogenicity of the etiological agent, Hemophilus pleuropneumoniae . J Exp Med. 1964;119:369–375. doi: 10.1084/jem.119.3.369. PubMed DOI PMC
Liggett AD, Harrison LR, Farrell RL. Sequential study of lesion development in experimental haemophilus pleuropneumonia. Res Vet Sci. 1987;42:204–212. PubMed
Sanford SE, Josephson GK. Porcine Haemophilus pleuropneumonia epizootic in southwestern Ontario: clinical, microbiological, pathological and some epidemiological findings. Can J Comp Med. 1981;45:2–7. PubMed PMC
Jones MA. In: The veterinary annual. 24. Grunsell CSG, Hill FWG, editor. Bristol, England: John Wright and Sons Ltd; 1984. Haemophilus pleuropneumoniae infection in pigs; pp. 148–154.
Haesebrouck F, Pasmans F, Chiers K, Maes D, Ducatelle R, Decostere A. Efficacy of vaccines against bacterial diseases in swine: what can we expect? Vet Microbiol. 2004;100:255–268. doi: 10.1016/j.vetmic.2004.03.002. PubMed DOI
Ramjeet M, Deslandes V, Goure J, Jacques M. Actinobacillus pleuropneumoniae vaccines: from bacterins to new insights into vaccination strategies. Anim Health Res Rev. 2008;9:25–45. doi: 10.1017/S1466252307001338. PubMed DOI
Blackall PJ, Klaasen HL, van den Bosch H, Kuhnert P, Frey J. Proposal of a new serovar of Actinobacillus pleuropneumoniae : serovar 15. Vet Microbiol. 2002;84:47–52. doi: 10.1016/S0378-1135(01)00428-X. PubMed DOI
Dubreuil JD, Jacques M, Mittal KR, Gottschalk M. Actinobacillus pleuropneumoniae surface polysaccharides: their role in diagnosis and immunogenicity. Anim Health Res Rev. 2000;1:73–93. doi: 10.1017/S1466252300000074. PubMed DOI
Jacques M. Surface polysaccharides and iron-uptake systems of Actinobacillus pleuropneumoniae . Can J Vet Res. 2004;68:81–85. PubMed PMC
Higgins R, Lariviere S, Mittal KR, Martineau GP, Rousseau P, Cameron J. Evaluation of a killed vaccine against porcine pleuropneumonia due to Haemophilus pleuropneumoniae . Can Vet J. 1985;26:86–89. PubMed PMC
Nielsen R. Haemophilus pleuropneumoniae serotypes--cross protection experiments. Nord Vet Med. 1984;36:221–234. PubMed
Nielsen R. Haemophilus pleuropneumoniae (Actinobacillus pleuropneumoniae ). Serotypes 8, 3 and 6. Serological response and cross immunity in pigs. Nord Vet Med. 1985;37:217–227. PubMed
Boekema BK, Van Putten JP, Stockhofe-Zurwieden N, Smith HE. Host cell contact-induced transcription of the type IV fimbria gene cluster of Actinobacillus pleuropneumoniae . Infect Immun. 2004;72:691–700. doi: 10.1128/IAI.72.2.691-700.2004. PubMed DOI PMC
Cho WS, Chae C. Expression of the apxIV gene in pigs naturally infected with Actinobacillus pleuropneumoniae . J Comp Pathol. 2001;125:34–40. doi: 10.1053/jcpa.2001.0474. PubMed DOI
Haesebrouck F, Chiers K, Van Overbeke I, Ducatelle R. Actinobacillus pleuropneumoniae infections in pigs: the role of virulence factors in pathogenesis and protection. Vet Microbiol. 1997;58:239–249. doi: 10.1016/S0378-1135(97)00162-4. PubMed DOI
Haga Y, Ogino S, Ohashi S, Ajito T, Hashimoto K, Sawada T. Protective efficacy of an affinity-purified hemolysin vaccine against experimental swine pleuropneumonia. J Vet Med Sci. 1997;59:115–120. doi: 10.1292/jvms.59.115. PubMed DOI
Seah JN, Frey J, Kwang J. The N-terminal domain of RTX toxin ApxI of Actinobacillus pleuropneumoniae elicits protective immunity in mice. Infect Immun. 2002;70:6464–6467. doi: 10.1128/IAI.70.11.6464-6467.2002. PubMed DOI PMC
Cruijsen T, van Leengoed LA, Ham-Hoffies M, Verheijden JH. Convalescent pigs are protected completely against infection with a homologous Actinobacillus pleuropneumoniae strain but incompletely against a heterologous-serotype strain. Infect Immun. 1995;63:2341–2343. PubMed PMC
Haesebrouk F, Van de Kerkhof A, Dom P, Chiers K, Ducatelle R. Cross-protection between Actinobacillus pleuropneumoniae biotypes-serotypes in pigs. Vet Microbiol. 1996;52:277–284. doi: 10.1016/S0378-1135(96)00075-2. PubMed DOI
Baltes N, Tonpitak W, Gerlach GF, Hennig-Pauka I, Hoffmann-Moujahid A, Ganter M, Rothkotter HJ. Actinobacillus pleuropneumoniae iron transport and urease activity: effects on bacterial virulence and host immune response. Infect Immun. 2001;69:472–478. doi: 10.1128/IAI.69.1.472-478.2001. PubMed DOI PMC
Byrd W, Hooke AM. Immunization with temperature-sensitive mutants of Actinobacillus pleuropneumoniae induces protective hemolysin-neutralizing antibodies in mice. Curr Microbiol. 1997;34:149–154. doi: 10.1007/s002849900160. PubMed DOI
Fuller TE, Thacker BJ, Mulks MH. A riboflavin auxotroph of Actinobacillus pleuropneumoniae is attenuated in swine. Infect Immun. 1996;64:4659–4664. PubMed PMC
Garside LH, Collins M, Langford PR, Rycroft AN. Actinobacillus pleuropneumoniae serotype 1 carrying the defined aroA mutation is fully avirulent in the pig. Res Vet Sci. 2002;72:163–167. doi: 10.1053/rvsc.2002.0554. PubMed DOI
Ingham A, Zhang Y, Prideaux C. Attenuation of Actinobacillus pleuropneumoniae by inactivation of aroQ. Vet Microbiol. 2002;84:263–273. doi: 10.1016/S0378-1135(01)00465-5. PubMed DOI
Maas A, Jacobsen ID, Meens J, Gerlach GF. Use of an Actinobacillus pleuropneumoniae multiple mutant as a vaccine that allows differentiation of vaccinated and infected animals. Infect Immun. 2006;74:4124–4132. doi: 10.1128/IAI.00133-06. PubMed DOI PMC
Prideaux CT, Lenghaus C, Krywult J, Hodgson AL. Vaccination and protection of pigs against pleuropneumonia with a vaccine strain of Actinobacillus pleuropneumoniae produced by site-specific mutagenesis of the ApxII operon. Infect Immun. 1999;67:1962–1966. PubMed PMC
Prideaux CT, Pierce L, Krywult J, Hodgson AL. Protection of mice against challenge with homologous and heterologous serovars of Actinobacillus pleuropneumoniae after live vaccination. Curr Microbiol. 1998;37:324–332. doi: 10.1007/s002849900386. PubMed DOI
Tumamao JQ, Bowles RE, van den Bosch H, Klaasen HL, Fenwick BW, Storie GJ, Blackall PJ. Comparison of the efficacy of a subunit and a live streptomycin-dependent porcine pleuropneumonia vaccine. Aust Vet J. 2004;82:370–374. doi: 10.1111/j.1751-0813.2004.tb11108.x. PubMed DOI
Xu F, Chen X, Shi A, Yang B, Wang J, Li Y, Guo X, Blackall PJ, Yang H. Characterization and immunogenicity of an apxIA mutant of Actinobacillus pleuropneumoniae . Vet Microbiol. 2006;118:230–239. doi: 10.1016/j.vetmic.2006.07.013. PubMed DOI
Bei W, He Q, Zhou R, Yan L, Huang H, Chen H. Evaluation of immunogenicity and protective efficacy of Actinobacillus pleuropneumoniae HB04C(-) mutant lacking a drug resistance marker in the pigs. Vet Microbiol. 2007;125:120–127. doi: 10.1016/j.vetmic.2007.05.013. PubMed DOI
Lin L, Bei W, Sha Y, Liu J, Guo Y, Liu W, Tu S, He Q, Chen H. Construction and immunogencity of a DeltaapxIC/DeltaapxIIC double mutant of Actinobacillus pleuropneumoniae serovar 1. FEMS Microbiol Lett. 2007;274:55–62. doi: 10.1111/j.1574-6968.2007.00813.x. PubMed DOI
Frey J, Meier R, Gygi D, Nicolet J. Nucleotide sequence of the hemolysin I gene from Actinobacillus pleuropneumoniae . Infect Immun. 1991;59:3026–3032. PubMed PMC
Frey J. Virulence in Actinobacillus pleuropneumoniae and RTX toxins. Trends Microbiol. 1995;3:257–261. doi: 10.1016/S0966-842X(00)88939-8. PubMed DOI
Frey J, Beck M, Stucki U, Nicolet J. Analysis of hemolysin operons in Actinobacillus pleuropneumoniae . Gene. 1993;123:51–58. doi: 10.1016/0378-1119(93)90538-E. PubMed DOI
Frey J, Beck M, van den Bosch JF, Segers RP, Nicolet J. Development of an efficient PCR method for toxin typing of Actinobacillus pleuropneumoniae strains. Mol Cell Probes. 1995;9:277–282. doi: 10.1016/S0890-8508(95)90158-2. PubMed DOI
Frey J, Bosse JT, Chang YF, Cullen JM, Fenwick B, Gerlach GF, Gygi D, Haesebrouck F, Inzana TJ, Jansen R, Kamp M, Macdonald J, MacInnes JI, Mittal KR, Nicolet J, Rycroft AN, Segers RP, Smits MA, Stenbaek E, Struck DK, van den Bosch, Willson PJ, Young R. Actinobacillus pleuropneumoniae RTX-toxins: uniform designation of haemolysins, cytolysins, pleurotoxin and their genes. J Gen Microbiol. 1993;139:1723–1728. PubMed
Linhartova I, Bumba L, Masin J, Basler M, Osicka R, Kamanova J, Prochazkova K, Adkins I, Hejnova-Holubova J, Sadilkova L, Morová J, Sebo P. RTX proteins: a highly diverse family secreted by a common mechanism. FEMS Microbiol Rev. 2010;34:1076–1112. PubMed PMC
Frey J, Nicolet J. Hemolysin patterns of Actinobacillus pleuropneumoniae . J Clin Microbiol. 1990;28:232–236. PubMed PMC
Kamp EM, Popma JK, Anakotta J, Smits MA. Identification of hemolytic and cytotoxic proteins of Actinobacillus pleuropneumoniae by use of monoclonal antibodies. Infect Immun. 1991;59:3079–3085. PubMed PMC
Rosendal S, Devenish J, MacInnes JI, Lumsden JH, Watson S, Xun H. Evaluation of heat-sensitive, neutrophil-toxic, and hemolytic activity of Haemophilus (Actinobacillus ) pleuropneumoniae . Am J Vet Res. 1988;49:1053–1058. PubMed
Rycroft AN, Williams D, Cullen JM, Macdonald J. The cytotoxin of Actinobacillus pleuropneumoniae (pleurotoxin) is distinct from the haemolysin and is associated with a 120 kDa polypeptide. J Gen Microbiol. 1991;137:561–568. PubMed
Chiers K, van Overbeke I, De Laender P, Ducatelle R, Carel S, Haesebrouck F. Effects of endobronchial challenge with Actinobacillus pleuropneumoniae serotype 9 of pigs vaccinated with inactivated vaccines containing the Apx toxins. Vet Q. 1998;20:65–69. doi: 10.1080/01652176.1998.9694841. PubMed DOI
Van Overbeke I, Chiers K, Ducatelle R, Haesebrouck F. Effect of endobronchial challenge with Actinobacillus pleuropneumoniae serotype 9 of pigs vaccinated with a vaccine containing Apx toxins and transferrin-binding proteins. J Vet Med B Infect Dis Vet Public Health. 2001;48:15–20. doi: 10.1046/j.1439-0450.2001.00419.x. PubMed DOI
Wang C, Wang Y, Shao M, Si W, Liu H, Chang Y, Peng W, Kong X, Liu S. Positive role for rApxIVN in the immune protection of pigs against infection by Actinobacillus pleuropneumoniae . Vaccine. 2009;27:5816–5821. doi: 10.1016/j.vaccine.2009.07.065. PubMed DOI
Schaller A, Kuhn R, Kuhnert P, Nicolet J, Anderson TJ, MacInnes JI, Segers RP, Frey J. Characterization of apxIVA, a new RTX determinant of Actinobacillus pleuropneumoniae . Microbiology. 1999;145:2105–2116. doi: 10.1099/13500872-145-8-2105. PubMed DOI
Gonzalez GC, Caamano DL, Schryvers AB. Identification and characterization of a porcine-specific transferrin receptor in Actinobacillus pleuropneumoniae . Mol Microbiol. 1990;4:1173–1179. doi: 10.1111/j.1365-2958.1990.tb00692.x. PubMed DOI
Baltes N, Hennig-Pauka I, Gerlach GF. Both transferrin binding proteins are virulence factors in Actinobacillus pleuropneumoniae serotype 7 infection. FEMS Microbiol Lett. 2002;209:283–287. doi: 10.1111/j.1574-6968.2002.tb11145.x. PubMed DOI
Rossi-Campos A, Anderson C, Gerlach GF, Klashinsky S, Potter AA, Willson PJ. Immunization of pigs against Actinobacillus pleuropneumoniae with two recombinant protein preparations. Vaccine. 1992;10:512–518. doi: 10.1016/0264-410X(92)90349-O. PubMed DOI
Oldfield NJ, Donovan EA, Worrall KE, Wooldridge KG, Langford PR, Rycroft AN, Ala'Aldeen DA. Identification and characterization of novel antigenic vaccine candidates of Actinobacillus pleuropneumoniae . Vaccine. 2008;26:1942–1954. doi: 10.1016/j.vaccine.2008.02.022. PubMed DOI
Zhang Y, Tennent JM, Ingham A, Beddome G, Prideaux C, Michalski WP. Identification of type 4 fimbriae in Actinobacillus pleuropneumoniae . FEMS Microbiol Lett. 2000;189:15–18. doi: 10.1111/j.1574-6968.2000.tb09199.x. PubMed DOI
Bakaletz LO, Baker BD, Jurcisek JA, Harrison A, Novotny LA, Bookwalter JE, Mungur R, Munson RS Jr. Demonstration of Type IV pilus expression and a twitching phenotype by Haemophilus influenzae . Infect Immun. 2005;73:1635–1643. doi: 10.1128/IAI.73.3.1635-1643.2005. PubMed DOI PMC
Luke NR, Howlett AJ, Shao J, Campagnari AA. Expression of type IV pili by Moraxella catarrhalis is essential for natural competence and is affected by iron limitation. Infect Immun. 2004;72:6262–6270. doi: 10.1128/IAI.72.11.6262-6270.2004. PubMed DOI PMC
Bieber D, Ramer SW, Wu CY, Murray WJ, Tobe T, Fernandez R, Schoolnik GK. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli . Science. 1998;280:2114–2118. doi: 10.1126/science.280.5372.2114. PubMed DOI
Carbonnelle E, Helaine S, Nassif X, Pelicic V. A systematic genetic analysis in Neisseria meningitidis defines the Pil proteins required for assembly, functionality, stabilization and export of type IV pili. Mol Microbiol. 2006;61:1510–1522. doi: 10.1111/j.1365-2958.2006.05341.x. PubMed DOI
Koga T, Ishimoto K, Lory S. Genetic and functional characterization of the gene cluster specifying expression of Pseudomonas aeruginosa pili. Infect Immun. 1993;61:1371–1377. PubMed PMC
Wall D, Kaiser D. Type IV pili and cell motility. Mol Microbiol. 1999;32:1–10. doi: 10.1046/j.1365-2958.1999.01339.x. PubMed DOI
Craig L, Pique ME, Tainer JA. Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol. 2004;2:363–378. doi: 10.1038/nrmicro885. PubMed DOI
Hansen JK, Forest KT. Type IV pilin structures: insights on shared architecture, fiber assembly, receptor binding and type II secretion. J Mol Microbiol Biotechnol. 2006;11:192–207. doi: 10.1159/000094054. PubMed DOI
Stevenson A, Macdonald J, Roberts M. Cloning and characterisation of type 4 fimbrial genes from Actinobacillus pleuropneumoniae . Vet Microbiol. 2003;92:121–134. doi: 10.1016/S0378-1135(02)00351-6. PubMed DOI
Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual. 2. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y., USA; 1989.
Foote SJ, Bosse JT, Bouevitch AB, Langford PR, Young NM, Nash JH. The complete genome sequence of Actinobacillus pleuropneumoniae L20 (serotype 5b) J Bacteriol. 2008;190:1495–1496. doi: 10.1128/JB.01845-07. PubMed DOI PMC
Xu Z, Zhou Y, Li L, Zhou R, Xiao S, Wan Y, Zhang S, Wang K, Li W, Jin H, Kang M, Dalai B, Li T, Liu L, Cheng Y, Zhang L, Xu T, Zheng H, Pu S, Wang B, Gu W, Zhang XL, Zhu GF, Wang S, Zhao GP, Chen H. Genome biology of Actinobacillus pleuropneumoniae JL03, an isolate of serotype 3 prevalent in China. PLoS One. 2008;3:e1450. doi: 10.1371/journal.pone.0001450. PubMed DOI PMC
van den Bosch H, Frey J. Interference of outer membrane protein PalA with protective immunity against Actinobacillus pleuropneumoniae infections in vaccinated pigs. Vaccine. 2003;21:3601–3607. doi: 10.1016/S0264-410X(03)00410-9. PubMed DOI
Kucerova Z, Jaglic Z, Ondriasova R, Nedbalcova K. Serotype distribution of Actinobacillus pleuropneumoniae isolated from porcine pleuropneumonia in the Czech Republic during period 2003-2004. Veterinarni Medicina - UZPI (Czech Republic) 2005;50:355–360.
Mittal KR, Higgins R, Lariviere S. Identification and serotyping of Haemophilus pleuropneumoniae by coagglutination test. J Clin Microbiol. 1983;18:1351–1354. PubMed PMC
Shao M, Wang Y, Wang C, Guo Y, Peng Y, Liu J, Li G, Liu H, Liu S. Evaluation of multicomponent recombinant vaccines against Actinobacillus pleuropneumoniae in mice. Acta Vet Scand. 2010;52:52. doi: 10.1186/1751-0147-52-52. PubMed DOI PMC
Stewart DJ, Clark BL, Peterson JE, Emery DL, Smith EF, Griffiths DA, O'Donnell IJ. The protection given by pilus and whole cell vaccines of Bacteroides nodosus strain 198 against ovine foot-rot induced by strains of different serogroups. Aust Vet J. 1985;62:153–159. doi: 10.1111/j.1751-0813.1985.tb07277.x. PubMed DOI
Lepper AW, Moore LJ, Atwell JL, Tennent JM. The protective efficacy of pili from different strains of Moraxella bovis within the same serogroup against infectious bovine keratoconjunctivitis. Vet Microbiol. 1992;32:177–187. doi: 10.1016/0378-1135(92)90104-2. PubMed DOI
Lepper AW, Atwell JL, Lehrbach PR, Schwartzkoff CL, Egerton JR, Tennent JM. The protective efficacy of cloned Moraxella bovis pili in monovalent and multivalent vaccine formulations against experimentally induced infectious bovine keratoconjunctivitis (IBK) Vet Microbiol. 1995;45:129–138. doi: 10.1016/0378-1135(94)00123-E. PubMed DOI
Boslego JW, Tramont EC, Chung RC, McChesney DG, Ciak J, Sadoff JC, Piziak MV, Brown JD, Brinton CC, Wood SW, Bryan JR. Efficacy trial of a parenteral gonococcal pilus vaccine in men. Vaccine. 1991;9:154–162. doi: 10.1016/0264-410X(91)90147-X. PubMed DOI
Dom P, Haesebrouck F, Ducatelle R, Charlier G. In vivo association of Actinobacillus pleuropneumoniae serotype 2 with the respiratory epithelium of pigs. Infect Immun. 1994;62:1262–1267. PubMed PMC
Jeannotte ME, Abul-Milh M, Dubreuil JD, Jacques M. Binding of Actinobacillus pleuropneumoniae to phosphatidylethanolamine. Infect Immun. 2003;71:4657–4663. doi: 10.1128/IAI.71.8.4657-4663.2003. PubMed DOI PMC
Van Overbeke I, Chiers K, Charlier G, Vandenberghe I, Van Beeumen J, Ducatelle R, Haesebrouck F. Characterization of the in vitro adhesion of Actinobacillus pleuropneumoniae to swine alveolar epithelial cells. Vet Microbiol. 2002;88:59–74. doi: 10.1016/S0378-1135(02)00080-9. PubMed DOI