Mycoplasma hyopneumoniae: From disease to vaccine development

Veterinary Microbiology

Volumn 165, Issue 3-4, 2013, Pages 234-242

  Simionatto, Simone ^a,b   Marchioro, Silvana Beutinger ^a,c   Maes, Dominiek ^c   Dellagostin, Odir AntÔnio ^a  

^a FEDERAL UNIVERSITY OF PELOTAS   (Brazil)

^b UNIVERSIDADE FEDERAL DA GRANDE DOURADOS   (Brazil)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

Enzootic pneumonia; Reverse vaccinology; Swine

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; BACTERIAL VACCINE; P102 PROTEIN; PROTEIN P97; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

BACTERIAL GENOME; BACTERIAL METABOLISM; INFECTION CONTROL; MYCOPLASMA HYOPNEUMONIAE; MYCOPLASMAL PNEUMONIA OF SWINE; NONHUMAN; PATHOGENESIS; REVIEW; VACCINATION;

MYCOPLASMA HYOPNEUMONIAE; SUIDAE;

ANIMALS; BACTERIAL VACCINES; MYCOPLASMA HYOPNEUMONIAE; PNEUMONIA OF SWINE, MYCOPLASMAL; SWINE; VACCINATION;

EID: 84892975052     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2013.04.019     Document Type: Review

References (71)

1. Adams C., Pitzer J., Minion F.C. In vivo expression analysis of the P97 and P102 paralog families of Mycoplasma hyopneumoniae. Infect. Immun. 2005, 73:7784-7787.
2. Bogema D.R., Deutscher A.T., Woolley L.K., Seymour L.M., Raymond B.B.A., Tacchi J.L., Padula M.P., Dixon N.E., Minion F.C., Jenkins C., Walker M.J., Djordjevic S.P. Characterization of cleavage events in the multifunctional cilium adhesin Mhp684 (P146) reveals a mechanism by which Mycoplasma hyopneumoniae regulates surface topography. Mol. Biol. 2012, 3:1-11.
3. Bogema D.R., Scott N.E., Padula M.P., Tacchi J.L., Raymond B.B.A., Jenkins C., Cordwell S.J., Minion F.C., Walker M.J., Djordjevic S.P. Sequence TTKF QE defines the site of proteolytic cleavage in Mhp683 protein, a novel glycosaminoglycan and cilium adhesin of Mycoplasma hyopneumoniae. J. Biol. Chem. 2011, 286:41217-41229.
4. Browning G.F., Marenda M.S., Noormohammadi A.H., Markham P.F. The central role of lipoproteins in the pathogenesis of mycoplasmoses. Vet. Microbiol. 2011, 153:44-50.
5. Calsamiglia M., Pijoan C., Trigo A. Application of a nested polymerase chain reaction assay to detect Mycoplasma hyopneumoniae from nasal swabs. J. Vet. Diagn. Invest. 1999, 11:246-251.
6. Calus D., Baele M., Meyns T., de K.A., Butaye P., Decostere A., Haesebrouck F., Maes D. Protein variability among Mycoplasma hyopneumoniae isolates. Vet. Microbiol. 2007, 120:284-291.
7. Chen A.Y., Fry S.R., Daggard G.E., Mukkur T.K. Evaluation of immune response to recombinant potential protective antigens of Mycoplasma hyopneumoniae delivered as cocktail DNA and/or recombinant protein vaccines in mice. Vaccine 2008, 26:4372-4378.
8. Chen A.Y., Fry S.R., Forbes-Faulkner J., Daggard G., Mukkur T.K. Evaluation of the immunogenicity of the P97R1 adhesin of Mycoplasma hyopneumoniae as a mucosal vaccine in mice. J. Med. Microbiol. 2006, 55:923-929.
9. Chen A.Y., Fry S.R., Forbes-Faulkner J., Daggard G.E., Mukkur T.K. Comparative immunogenicity of M. hyopneumoniae NrdF encoded in different expression systems delivered orally via attenuated S. typhimurium aroA in mice. Vet. Microbiol. 2006, 114:252-259.
10. Chen J.R., Liao C.W., Mao S.J., Weng C.N. A recombinant chimera composed of repeat region RR1 of Mycoplasma hyopneumoniae adhesin with Pseudomonas exotoxin: in vivo evaluation of specific IgG response in mice and pigs. Vet. Microbiol. 2001, 80:347-357.
11. Chen Y.L., Wang S.N., Yang W.J., Chen Y.J., Lin H.H., Shiuan D. Expression and immunogenicity of Mycoplasma hyopneumoniae heat shock protein antigen p42 by DNA vaccination. Infect. Immun. 2003, 71:1155-1160.
12. Ciprian A., Palacios J.M., Quintanar D., Batista L., Colmenares G., Cruz T., Romero A., Schnitzlein W., Mendoza S. Florfenicol feed supplemented decrease the clinical effects of Mycoplasma hyopneumoniae experimental infection in swine in Mexico. Res. Vet. Sci. 2012, 92:191-196.
13. Conceicao F.R., Moreira A.N., Dellagostin O.A. A recombinant chimera composed of R1 repeat region of Mycoplasma hyopneumoniae P97 adhesin with Escherichia coli heat-labile enterotoxin B subunit elicits immune response in mice. Vaccine 2006, 24:5734-5743.
14. Debey M.C., Ross R.F. Ciliostasis and loss of cilia induced by Mycoplasma hyopneumoniae in porcine tracheal organ-cultures. Infect. Immun. 1994, 62:5312-5318.
15. Deutscher A.T., Tacchi J.L., Minion F.C., Padula M.P., Crossett B., Bogema D.R., Jenkins C., Kuit T.A., Walker M.J., Djordjevic S.P. Mycoplasma hyopneumoniae surface proteins Mhp385 and Mhp384 bind host cilia and glycosaminoglycans and are endoproteolytically processed by proteases that recognize different cleavage motifs. J. Prot. Res. 2012, 11:1924-1936.
16. Fagan P.K., Djordjevic S.P., Chin J., Eamens G.J., Walker M.J. Oral immunization of mice with attenuated Salmonella typhimurium aroA expressing a recombinant Mycoplasma hyopneumoniae antigen (NrdF). Infect. Immun. 1997, 65:2502-2507.
17. Fagan P.K., Walker M.J., Chin J., Eamens G.J., Djordjevic S.P. Oral immunization of swine with attenuated Salmonella typhimurium aroA SL3261 expressing a recombinant antigen of Mycoplasma hyopneumoniae (NrdF) primes the immune system for a NrdF specific secretory IgA response in the lungs. Microb. Pathog. 2001, 30:101-110.
18. Friis N.F. Some recommendations concerning primary isolation of Mycoplasma suipneumoniae and Mycoplasma flocculare a survey. Nord. Vet. Med. 1975, 27:337-339.
19. Galli V., Simionatto S., Marchioro S.B., Fisch A., Gomes C.K., Conceicao F.R., Dellagostin O.A. Immunisation of mice with Mycoplasma hyopneumoniae antigens P37, P42, P46 and P95 delivered as recombinant subunit or DNA vaccines. Vaccine 2012, 31:135-140.
20. Haesebrouck F., Pasmans F., Chiers K., Maes D., Ducatelle R., Decostere A. Efficacy of vaccines against bacterial diseases in swine: what can we expectα. Vet. Microbiol. 2004, 100:255-268.
21. King K.W., Faulds D.H., Rosey E.L., Yancey R.J. Characterization of the gene encoding Mhp1 from Mycoplasma hyopneumoniae and examination of Mhp1's vaccine potential. Vaccine 1997, 15:25-35.
22. Kobisch M., Friis N.F. Swine mycoplasmoses. Revue Scientifique et Technique de l Office International des Epizooties 1996, 15:1569-1605.
23. Liu W., Feng Z., Fang L., Zhou Z., Li Q., Li S., Luo R., Wang L., Chen H., Shao G., Xiao S. Complete genome sequence of Mycoplasma hyopneumoniae strain 168. J. Bacteriol. 2011, 193:1016-1017.
24. Maes D., Deluyker H., Verdonck M., Castryck F., Miry C., Vrijens B., Verbeke W., Viaene J., de K.A. Effect of vaccination against Mycoplasma hyopneumoniae in pig herds with an all-in/all-out production system. Vaccine 1999, 17:1024-1034.
25. Maes D., Segales J., Meyns T., Sibila M., Pieters M., Haesebrouck F. Control of Mycoplasma hyopneumoniae infections in pigs. Vet. Microbiol. 2008, 126:297-309.
26. Marchioro S.B., Simionatto S., Galli V., Conceição F.R., Brum C.B., Fisch A., Gomes C.K., Dellagostin O.A. Production and characterization of recombinant transmembrane proteins from Mycoplasma hyopneumoniae. Vet. Microbiol. 2012, 155:44-52.
27. Marois C., Le C.J., Kobisch M., Gautier-Bouchardon A.V. Isolation of Mycoplasma hyopneumoniae from different sampling sites in experimentally infected and contact SPF piglets. Vet. Microbiol. 2007, 120:96-104.
28. Mateusen B., Maes D., Van G.M., Verdonck M., de K.A. Effectiveness of treatment with lincomycin hydrochloride and/or vaccination against Mycoplasma hyopneumoniae for controlling chronic respiratory disease in a herd of pigs. Vet. Rec. 2002, 151:135-140.
29. Meyns T., Dewulf J., de K.A., Calus D., Haesebrouck F., Maes D. Comparison of transmission of Mycoplasma hyopneumoniae in vaccinated and non-vaccinated populations. Vaccine 2006, 24:7081-7086.
30. Meyns T., Maes D., Dewulf J., Vicca J., Haesebrouck F., de K.A. Quantification of the spread of Mycoplasma hyopneumoniae in nursery pigs using transmission experiments. Prev. Vet. Med. 2004, 66:265-275.
31. Minion F.C., Adams C., Hsu T. R1 region of P97 mediates adherence of Mycoplasma hyopneumoniae to swine cilia. Infect. Immun. 2000, 68:3056-3060.
32. Minion F.C., Lefkowitz E.J., Madsen M.L., Cleary B.J., Swartzell S.M., Mahairas G.G. The genome sequence of Mycoplasma hyopneumoniae strain 232, the agent of swine mycoplasmosis. J. Bacteriol. 2004, 186:7123-7133.
33. Muneta Y., Minagawa Y., Shimoji Y., Ogawa Y., Hikono H., Mori Y. Immune response of gnotobiotic piglets against Mycoplasma hyopneumoniae. J. Vet. Med. Sci. 2008, 70:1065-1070.
34. Nuc P., Nuc K. Recombinant protein production in Escherichia coli. Postepy Biochem. 2006, 52:448-456.
35. Ogawa Y., Oishi E., Muneta Y., Sano A., Hikono H., Shibahara T., Yagi Y., Shimoji Y. Oral vaccination against mycoplasmal pneumonia of swine using a live Erysipelothrix rhusiopathiae vaccine strain as a vector. Vaccine 2009, 27:4543-4550.
36. Okamba F.R., Arella M., Music N., Jia J.J., Gottschalk M., Gagnon C.A. Potential use of a recombinant replication-defective adenovirus vector carrying the C-terminal portion of the P97 adhesin protein as a vaccine against Mycoplasma hyopneumoniae in swine. Vaccine 2010, 28:4802-4809.
37. Okamba F.R., Moreau E., Cheikh Saad B.K., Gagnon C.A., Massie B., Arella M. Immune responses induced by replication-defective adenovirus expressing the C-terminal portion of the Mycoplasma hyopneumoniae P97 adhesin. Clin. Vaccine Immunol. 2007, 14:767-774.
38. Pinto P.M., Chemale G., de Castro L.A., Costa A.P., Kich J.D., Vainstein M.H., Zaha A., Ferreira H.B. Proteomic survey of the pathogenic Mycoplasma hyopneumoniae strain 7448 and identification of novel post-translationally modified and antigenic proteins. Vet. Microbiol. 2007, 121:83-93.
39. Pinto P.M., de Carvalho M.O., ves-Junior L., Brocchi M., Schrank I.S. Molecular analysis of an Integrative Conjugative Element, ICEH, present in the chromosome of different strains of Mycoplasma hyopneumoniae. Genet. Mol. Biol. 2007, 30:256-263.
40. Rappuoli R. Reverse vaccinology, a genome-based approach to vaccine development. Vaccine 2001, 19:2688-2691.
41. Razin S., Yogev D., Naot Y. Molecular biology and pathogenicity of mycoplasmas. Microbiol. Mol. Biol. Rev. 1998, 62:1094-1156.
42. Reynolds S.C., St Aubin L.B., Sabbadini L.G., Kula J., Vogelaar J., Runnels P., Peters A.R. Reduced lung lesions in pigs challenged 25 weeks after the administration of a single dose of Mycoplasma hyopneumoniae vaccine at approximately 1 week of age. Vet. J. 2009, 181:312-320.
43. Rodriguez F., Ramirez G.A., Sarradell J., Andrada M., Lorenzo H. Immunohistochemical labelling of cytokines in lung lesions of pigs naturally infected with Mycoplasma hyopneumoniae. J. Comp. Pathol. 2004, 130:306-312.
44. Seymour L.M., Deutscher A.T., Jenkins C., Kuit T.A., Falconer L., Minion F.C., Crossett B., Padula M., Dixon N.E., Djordjevic S.P., Walker M.J. A processed multidomain Mycoplasma hyopneumoniae adhesin binds fibronectin, plasminogen, and swine respiratory cilia. J. Biol. Chem. 2010, 285:33971-33978.
45. Seymour L.M., Falconer L., Deutscher A.T., Minion F.C., Padula M.P., Dixon N.E., Djordjevic S.P., Walker M.J. Mhp107 is a member of the multifunctional adhesin family of Mycoplasma hyopneumoniae. J. Biol. Chem. 2011, 286:10097-10104.
46. Seymour L.M., Jenkins C., Deutscher A.T., Raymond B.B.A., Padula M.P., Tacchi J.L., Bogema D.R., Eamens G.J., Woolley L.K., Dixon N.E., Walker M.J., Djordjevic S.P. Mhp182 (P102) binds fibronectin and contributes to the recruitment of plasmin(ogen) to the Mycoplasma hyopneumoniae cell surface. Cell. Microbiol. 2012, 14:81-94.
47. Shimoji Y., Oishi E., Muneta Y., Nosaka H., Mori Y. Vaccine efficacy of the attenuated Erysipelothrix rhusiopathiae YS-19 expressing a recombinant protein of Mycoplasma hyopneumoniae P97 adhesin against mycoplasmal pneumonia of swine. Vaccine 2003, 21:532-537.
48. Sibila M., Calsamiglia M., Vidal D., Badiella L., Aldaz A., Jensen J.C. Dynamics of Mycoplasma hyopneumoniae infection in 12 farms with different production systems. Can. J. Vet. Res. 2004, 68:12-18.
49. Sibila M., Nofrarias M., Lopez-Soria S., Segales J., Valero O., Espinal A., Calsamiglia M. Chronological study of Mycoplasma hyopneumoniae infection, seroconversion and associated lung lesions in vaccinated and non-vaccinated pigs. Vet. Microbiol. 2007, 122:97-107.
50. Sibila M., Pieters M., Molitor T., Maes D., Haesebrouck F., Segales J. Current perspectives on the diagnosis and epidemiology of Mycoplasma hyopneumoniae infection. Vet. J. 2009, 181:221-231.
51. Simionatto S., Marchioro S.B., Hartwig D., Galli V., Carlessi R.M., Munari F.M. Cloning and purification of recombinant proteins of Mycoplasma hyopneumoniae expressed in E. coli systems. Protein Expr. Purif. 2010, 69:132-136.
52. Simionatto S., Marchioro S.B., Galli V., Brum C.B., Klein C.S., Rebelatto R., Silva E.F., Borsuk S., Conceicao F.R., Dellagostin O.A. Immunological characterization of Mycoplasma hyopneumoniae recombinant proteins. Comp. Immunol. Microb. 2012, 35:209-216.
53. Simionatto S., Marchioro S.B., Galli V., Luerce T.D., Hartwig D.D., Moreira A.N., Dellagostin O.A. Efficient site-directed mutagenesis using an overlap extension-PCR method for expressing Mycoplasma hyopneumoniae genes in Escherichia coli. J. Microbiol. Methods 2009, 79:101-105.
54. Siqueira F.M., Schrank A., Schrank I.S. Mycoplasma hyopneumoniae transcription unit organization: genome survey and prediction. DNA Res. 2011, 18:413-422.
55. Sorensen V., Ahrens P., Barfod K., Feenstra A.A., Feld N.C., Friis N.F., Bille-Hansen V., Jensen N.E., Pedersen M.W. Mycoplasma hyopneumoniae infection in pigs: duration of the disease and evaluation of four diagnostic assays. Vet. Microbiol. 1997, 54:23-34.
56. Strait E.L., Madsen M.L., Minion F.C., Christopher-Hennings J., Dammen M., Jones K.R., Thacker E.L. Real-time PCR assays to address genetic diversity among strains of Mycoplasma hyopneumoniae. J. Clin. Microbiol. 2008, 46:2491-2498.
57. Stakenborg T., Vicca J., Butaye P., Maes D., Peeters J., de K.A., Haesebrouck F. The diversity of Mycoplasma hyopneumoniae within and between herds using pulsed-field gel electrophoresis. Vet. Microbiol. 2005, 109:29-36.
58. Thacker E.L. Diagnosis of Mycoplasma hyopneumoniae. Anim. Health Res. Rev. 2004, 5:317-320.
59. Thacker E.L., Minion F.C. Mycoplasmosis. Diseases of Swine 2010, 779-797. Iowa State University Press, Ames, Iowa, USA. J. Zimmerman (Ed.).
60. Thacker E.L., Thacker B.J., Boettcher T.B., Jayappa H. Comparison of antibody production, lymphocyte stimulation, and protection induced by four commercial Mycoplasma hyopneumoniae bacterins. J. Swine Health Prod. 1998, 6:107-112.
61. Thacker E.L., Thacker B.J., Kuhn M., Hawkins P.A., Waters W.R. Evaluation of local and systemic immune responses induced by intramuscular injection of a Mycoplasma hyopneumoniae bacterin to pigs. Am. J. Vet. Res. 2000, 61:1384-1389.
62. Vasconcelos A.T., Ferreira H.B., Bizarro C.V., Bonatto S.L., Carvalho M.O., Pinto P.M., Almeida D.F., Almeida L.G., Almeida R., ves-Filho L., Assuncao E.N., Azevedo V.A., Bogo M.R., Brigido M.M., Brocchi M., Burity H.A., Camargo A.A., Camargo S.S., Carepo M.S., Carraro D.M., de Mattos Cascardo J.C., Castro L.A., Cavalcanti G., Chemale G., Collevatti R.G., Cunha C.W., Dallagiovanna B., Dambros B.P., Dellagostin O.A., Falcao C., Fantinatti-Garboggini F., Felipe M.S., Fiorentin L., Franco G.R., Freitas N.S., Frias D., Grangeiro T.B., Grisard E.C., Guimaraes C.T., Hungria M., Jardim S.N., Krieger M.A., Laurino J.P., Lima L.F., Lopes M.I., Loreto E.L., Madeira H.M., Manfio G.P., Maranhao A.Q., Martinkovics C.T., Medeiros S.R., Moreira M.A., Neiva M., Ramalho-Neto C.E., Nicolas M.F., Oliveira S.C., Paixao R.F., Pedrosa F.O., Pena S.D., Pereira M., Pereira-Ferrari L., Piffer I., Pinto L.S., Potrich D.P., Salim A.C., Santos F.R., Schmitt R., Schneider M.P., Schrank A., Schrank I.S., Schuck A.F., Seuanez H.N., Silva D.W., Silva R., Silva S.C., Soares C.M., Souza K.R., Souza R.C., Staats C.C., Steffens M.B., Teixeira S.M., Urmenyi T.P., Vainstein M.H., Zuccherato L.W., Simpson A.J., Zaha A. Swine and poultry pathogens: the complete genome sequences of two strains of Mycoplasma hyopneumoniae and a strain of Mycoplasma synoviae. J. Bacteriol. 2005, 187:5568-5577.
63. Vicca J., Stakenborg T., Maes D., Butaye P., Peeters J., de K.A., Haesebrouck F. Evaluation of virulence of Mycoplasma hyopneumoniae field isolates. Vet. Microbiol. 2003, 97:177-190.
64. Vicca J., Stakenborg T., Maes D., Butaye P., Peeters J., de K.A., Haesebrouck F. In vitro susceptibilities of Mycoplasma hyopneumoniae field isolates. Antimicrob. Agents Chemother. 2004, 48:4470-4472.
65. Villarreal I., Maes D., Vranckx K., Calus D., Pasmans F., Haesebrouck F. Effect of vaccination of pigs against experimental infection with high and low virulence Mycoplasma hyopneumoniae strains. Vaccine 2011, 29:1731-1735.
66. Vranckx K., Maes D., Calus D., Villarreal I., Pasmans F., Haesebrouck F. Multiple locus variable number of tandem repeats analysis is a suitable tool for the differentiation of M. hyopneumoniae strains without cultivation. J. Clin. Microbiol. 2011, 49:2020-2023.
67. Wilton J., Jenkins C., Cordwell S.J., Falconer L., Minion F.C., Oneal D.C., Djordjevic M.A., Connolly A., Barchia I., Walker M.J., Djordjevic S.P. Mhp493 (P216) is a proteolytically processed, cilium and heparin binding protein of Mycoplasma hyopneumoniae. Mol. Microbiol. 2009, 71:566-582.
68. Woolley L.K., Fell S., Gonsalves J.R., Walker M.J., Djordjevic S.P., Jenkins C., Eamens G.J. Evaluation of clinical, histological and immunological changes and qPCR detection of Mycoplasma hyopneumoniae in tissues during the early stages of mycoplasmal pneumonia in pigs after experimental challenge with two field isolates. Vet. Microbiol. 2012, 161:186-195.
69. Yuki Y., Kiyono H. New generation of mucosal adjuvants for the induction of protective immunity. Rev. Med. Virol. 2003, 13:293-310.
70. Zhang Q., Young T.F., Ross R.F. Identification and characterization of a Mycoplasma hyopneumoniae adhesin. Infect. Immun. 1995, 63:1013-1019.
71. Zou H.Y., Liu X.J., Ma F.Y., Chen P., Zhou R., He Q.G. Attenuated Actinobacillus pleuropneumoniae as a bacterial vector for expression of Mycoplasma hyopneumoniae P36 gene. J. Gene Med. 2011, 13:221-229.