Bovine paratuberculosis: Recent advances in vaccine development

Veterinary Quarterly

Volumn 31, Issue 4, 2011, Pages 183-191

  Santema, Wiebren ^a   Rutten, Victor ^a,b   Koets, Ad ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

Bovine; Cattle; Johne's disease; Mycobacterium; Paratuberculosis; Subunit; Vaccine

Indexed keywords

BACTERIAL VACCINE; PARATUBERCULOSIS VACCINE; UNCLASSIFIED DRUG;

BACTERIAL SHEDDING; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BACTERIUM CULTURE; BOVINE TUBERCULOSIS; CATTLE; CD4+ T LYMPHOCYTE; CROSS REACTION; DRUG EFFICACY; GAMMA DELTA T LYMPHOCYTE; GENETIC VARIABILITY; IMMUNE RESPONSE; IMMUNOASSAY; INFECTION SENSITIVITY; INTERFERON GAMMA RELEASE ASSAY; MACROPHAGE; MYCOBACTERIUM PARATUBERCULOSIS; NONHUMAN; PARATUBERCULOSIS; PEYER PATCH; POLYMERASE CHAIN REACTION; PROTEIN LOSING GASTROENTEROPATHY; REMISSION; REVIEW; SENSITIVITY AND SPECIFICITY; T LYMPHOCYTE ACTIVATION;

ANIMALS; BACTERIAL VACCINES; CATTLE; CATTLE DISEASES; EUROPEAN UNION; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS; PARATUBERCULOSIS;

BOS; BOVINAE; MYCOBACTERIUM; MYCOBACTERIUM AVIUM;

EID: 84856058827     PISSN: 01652176     EISSN: 18755941     Source Type: Journal    
DOI: 10.1080/01652176.2011.633766     Document Type: Review

References (88)

1. Alexander DC, Turenne CY, Behr MA. 2009. Insertion and deletion events that define the pathogen Mycobacterium avium subsp. paratuberculosis. J Bacteriol. 191:1018-1025
2. Balu S, Reljic R, Lewis MJ, Pleass RJ, McIntosh R, van Kooten C, van Egmond M, Challacombe S, Woof JM, Ivanyi J. 2011. A Novel Human IgA Monoclonal Antibody Protects against tuberculosis. J Immunol. 186:3113-3119.
3. Bannantine JP, Bayles DO, Waters WR, Palmer MV, Stabel JR, Paustian ML. 2008. Early antibody response against Mycobacterium avium subspecies paratuberculosis antigens in subclinical cattle. Proteome Sci. 6:5.
4. Bassey EO, Collins MT. 1997. Study of T-lymphocyte subsets of healthy and Mycobacterium avium subsp. paratuberculosis-infected cattle. Infect Immunol. 65:4869-4872.
5. Bech-Nielsen S, Jorgensen JB, Ahrens P, Feld NC. 1992. Diagnostic accuracy of a Mycobacterium phlei-absorbed serum enzyme-linked immunosorbent assay for diagnosis of bovine paratuberculosis in dairy cows. J Clin Microbiol. 30:613-618.
6. Behr MA, Kapur V. 2008. The evidence for Mycobacterium paratuberculosis in Crohn's disease. Curr Opin Gastroenterol. 24:17-21.
7. Benedictus A, Mitchell RM, Linde-Widmann M, Sweeney R, Fyock T, Schukken YH, Whitlock RH. 2008. Transmission parameters of Mycobacterium avium subspecies paratuberculosis infections in a dairy herd going through a control program. Prev Vet Med. 83:215-227.
8. Boysen P, Storset AK. 2009. Bovine natural killer cells. Vet Immunol Immunopathol. 130:163-177.
9. Buergelt CD, Hall C, McEntee K, Duncan JR. 1978. Pathological evaluation of paratuberculosis in naturally infected cattle. Vet Pathol. 15:196-207.
10. Clarke CJ. 1997. The pathology and pathogenesis of paratuberculosis in ruminants and other species. J Comp Pathol. 116:217-261.
11. Coussens PM. 2004. Model for immune responses to Mycobacterium avium subspecies paratuberculosis in cattle. Infect Immunol. 72:3089-3096.
12. de Almeida DE, Colvin CJ, Coussens PM. 2008. Antigen-specific regulatory T cells in bovine paratuberculosis. Vet Immunol Immunopathol. 125:234-245.
13. Diekmann O, Heesterbeek JAP. 2000. Mathematical epidemiology of infectious diseases: model building, analysis, and interpretation. Chichester (UK): Wiley and Sons.
14. Eisenberg SW, Nielen M, Santema W, Houwers DJ, Heederik D, Koets AP. 2010. Detection of spatial and temporal spread of Mycobacterium avium subsp. Para-tuberculosis in the environment of a cattle farm through bio-aerosols. Vet Microbiol. 143:284-292.
15. Ferwerda G, Kullberg BJ, de Jong DJ, Girardin SE, Langenberg DM, van Crevel R, Ottenhoff TH, van der Meer JW, Netea MG. 2007. Mycobacterium paratuberculosis is recognized by Toll-like receptors and NOD2. J Leukoc Biol. 82:1011-1018.
16. Flynn JL, Chan J. 2001. Immunology of tuberculosis. Annu Rev Immunol. 19:93-129.
17. Glatman-Freedman A. 2006. The role of antibody-mediated immunity in defense against Mycobacterium tuberculosis: advances toward a novel vaccine strategy. Tuberculosis (Edinb). 86:191-197.
18. Hines II ME, Stabel 2nd JR, Sweeney RW, Griffin F, Talaat AM, Bakker D, Benedictus G, Davis WC, de Lisle GW, Gardner IA, et al. 2007. Experimental challenge models for Johne's disease: a review and proposed international guidelines. Vet Microbiol. 122:197-222.
19. Hoek A, Rutten VP, Kool J, Arkesteijn GJ, Bouwstra RJ, van Rhijn I, Koets AP. 2009. Subpopulations of bovine WC1({thorn}) gammadelta T cells rather than CD4({thorn})CD25(high) Foxp3({thorn}) T cells act as immune regulatory cells ex vivo. Vet Res. 40:6.
20. Hoek A, Rutten VP, van der Zee R, Davies CJ, Koets AP. 2010. Epitopes of Mycobacterium avium ssp. paratuber-culosis 70kDa heat-shock protein activate bovine helper T cells in outbred cattle. Vaccine. 28:5910-5919.
21. Huda A, Jungersen G, Lind P. 2004. Longitudinal study of interferon-gamma, serum antibody and milk antibody responses in cattle infected with Mycobacterium avium subsp. paratuberculosis. Vet Microbiol. 104:43-53.
22. Joller N, Weber SS, Muller AJ, Sporri R, Selchow P, Sander P, Hilbi H, Oxenius A. 2010. Antibodies protect against intracellular bacteria by Fc receptor-mediated lysosomal targeting. Proc Natl Acad Sci. USA. 107:20441-20446.
23. Kalis CH, Hesselink JW, Barkema HW, Collins MT. 2001. Use of long-term vaccination with a killed vaccine to prevent fecal shedding of Mycobacterium avium subsp paratuberculosis in dairy herds. Am J Vet Res. 62:270-274.
24. Kathaperumal K, Park SU, McDonough S, Stehman S, Akey B, Huntley J, Wong S, Chang CF, Chang YF. 2008. Vaccination with recombinant Mycobacterium avium subsp. paratuberculosis proteins induces differential immune responses and protects calves against infection by oral challenge. Vaccine. 26: 1652-1663.
25. Kaufmann SH. 2007. The contribution of immunology to the rational design of novel antibacterial vaccines. Nat Rev Microbiol. 5:491-504.
26. Kaufmann SH. 2010. Future vaccination strategies against tuberculosis: thinking outside the box. Immunity. 33:567-577.
27. Kirkpatrick BW, Shi X, Shook GE, Collins MT. 2010. Whole-Genome association analysis of susceptibility to paratuberculosis in holstein cattle. Anim Genet. 42:149-160.
28. Koets AP, Adugna G, Janss LL, van Weering HJ, Kalis CH, Wentink GH, Rutten VP, Schukken YH. 2000. Genetic variation of susceptibility to Mycobacterium avium subsp. paratuberculosis infection in dairy cattle. J Dairy Sci. 83:2702-2708.
29. Koets AP, Hoek A, Langelaar M, Overdijk M, Santema W, Franken P, Eden W, Rutten V. 2006. Mycobacterial 70 kD heat-shock protein is an effective subunit vaccine against bovine paratuberculosis. Vaccine. 24:2550-2559.
30. Koets AP, Rutten V, Hoek A, van Mil F, Muller K, Bakker D, Gruys E, van Eden W. 2002. Progressive bovine paratuberculosis is associated with local loss of CD4({thorn}) T cells, increased frequency of gamma delta T cells, and related changes in T-cell function. Infect Immunol. 70:3856-3864.
31. Koets AP, Rutten VP, Hoek A, Bakker D, van Zijderveld F, Muller KE, van Eden W. 1999. Heat-shock protein-specific T-cell responses in various stages of bovine paratuberculosis. Vet Immunol Immunopathol. 70:105-115.
32. Koets AP, Santema W, Mertens H, Oostenrijk D, Keestra M, Overdijk M, Labouriau R, Franken P, Frijters A, Nielen M, et al. 2010. Susceptibility to paratuberculosis infection in cattle is associated with single nucleotide polymorphisms in Toll-like receptor 2 which modulate immune responses against Mycobacterium avium subspecies paratuberculosis. Prev Vet Med. 93:305-315.
33. Kohler H, Gyra H, Zimmer K, Drager KG, Burkert B, Lemser B, Hausleithner D, Cubler K, Klawonn W, Hess RG. 2001. Immune reactions in cattle after immunization with a Mycobacterium paratuberculosis vaccine and implications for the diagnosis of M. paratuberculosis and M. bovis infections. J Vet Med B Infect Dis Vet Public Health. 48:185-195.
34. Koo HC, Park YH, Hamilton MJ, Barrington GM, Davies CJ, Kim JB, Dahl JL, Waters WR, Davis WC. 2004. Analysis of the immune response to Mycobacterium avium subsp. paratuberculosis in experimentally infected calves. Infect Immunol. 72:6870-6883.
35. Kuehnel MP, Goethe R, Habermann A, Mueller E, Rohde M, Griffiths G, Valentin-Weigand P. 2001. Characterization of the intracellular survival of Mycobacterium avium ssp. paratuberculosis: phagosomal pH and fusogenicity in J774 macrophages compared with other mycobacteria. Cell Microbiol. 3:551-566.
36. Larsen AB, Merkal RS, Moon HW. 1974. Evaluation of a paratuberculosis vaccine given to calves before infection. Am J Vet Res. 35:367-369.
37. Larsen AB, Moyle AI, Himes EM. 1978. Experimental vaccination of cattle against paratuberculosis (Johne's disease) with killed bacterial vaccines: a controlled field study. Am J Vet Res. 39:65-69.
38. Li L, Bannantine JP, Zhang Q, Amonsin A, May BJ, Alt D, Banerji N, Kanjilal S, Kapur V. 2005. The complete genome sequence of Mycobacterium avium subspecies paratuberculosis. Proc Natl Acad Sci. USA. 102:12344-12349.
39. Lin MY, Ottenhoff TH. 2008. Not to wake a sleeping giant: new insights into host-pathogen interactions identify new targets for vaccination against latent Mycobacterium tuberculosis infection. Biol Chem. 389:497-511.
40. Lu Z, Schukken YH, Smith RL, Grohn YT. 2010. Stochastic simulations of a multi-group compartmental model for Johne's disease on US dairy herds with test-based culling intervention. J Theor Biol. 264: 1190-1201.
41. Maglione PJ, Chan J. 2009. How B cells shape the immune response against Mycobacterium tuberculosis. Eur J Immunol. 39:676-686.
42. Marce C, Ezanno P, Seegers H, Pfeiffer DU, Fourichon C. 2011. Within-herd contact structure and transmission of Mycobacterium avium subspecies paratuberculosis in a persistently infected dairy cattle herd. Prev Vet Med. 100:116-125.
43. Momotani E, Whipple DL, Thiermann AB, Cheville NF. 1988. Role of M cells and macrophages in the entrance of Mycobacterium paratuberculosis into domes of ileal Peyer's patches in calves. Vet Pathol. 25:131-137.
44. Muskens J, van Zijderveld F, Eger A, Bakker D. 2002. Evaluation of the long-term immune response in cattle after vaccination against paratuberculosis in two Dutch dairy herds. Vet Microbiol. 86:269-278.
45. Nagata R, Muneta Y, Yoshihara K, Yokomizo Y, Mori Y. 2005. Expression cloning of gamma interferon-inducing antigens of Mycobacterium avium subsp. paratuberculosis. Infect Immunol. 73:3778-3782.
46. Nielsen SS, Toft N. 2008. Ante mortem diagnosis of paratuberculosis: a review of accuracies of ELISA, interferon-gamma assay and faecal culture techniques. Vet Microbiol. 129:217-235.
47. Nielsen SS, Toft N. 2009. A review of prevalences of paratuberculosis in farmed animals in Europe. Prev Vet Med. 88:1-14.
48. Olsen I, Boysen P, Kulberg S, Hope JC, Jungersen G, Storset AK. 2005. Bovine NK cells can produce gamma interferon in response to the secreted mycobacterial proteins ESAT-6 and MPP14 but not in response to MPB70. Infect Immunol. 73:5628-5635.
49. Park KT, Allen AJ, Bannantine JP, Seo KS, Hamilton MJ, Abdellrazeq GS, Rihan HM, Grimm A, Davis WC. 2011. Evaluation of two mutants of Mycobacterium avium subsp. paratuberculosis as candidates for a live attenuated vaccine for Johne's disease. Vaccine. 29:4709-4719.
50. Patterson CJ, LaVenture M, Hurley SS, Davis JP. 1988. Accidental self-inoculation with Mycobacterium paratuberculosis bacterin (Johne's bacterin) by veterinarians in Wisconsin. J Am Vet Med Assoc. 192: 1197-1199.
51. Pethe K, Alonso S, Biet F, Delogu G, Brennan MJ, Locht C, Menozzi FD. 2001. The heparin-binding haemagglutinin of M. tuberculosis is required for extrapulmonary dissemination. Nature. 412:190-194.
52. Pinedo PJ, Buergelt CD, Donovan GA, Melendez P, Morel L, Wu R, Langaee TY, Rae DO. 2009. Association between CARD15/NOD2 gene polymorphisms and paratuberculosis infection in cattle. Vet Microbiol. 134:346-352.
53. Plotkin SA. 2008. Vaccines: correlates of vaccine-induced immunity. Clin Infect Dis. 47:401-409.
54. Rigden RC, Jandhyala DM, Dupont C, Crosbie-Caird D, Lopez-Villalobos N, Maeda N, Gicquel B, Murray A. 2006. Humoral and cellular immune responses in sheep immunized with a 22 kilodalton exported protein of Mycobacterium avium subspecies paratuberculosis. J Med Microbiol. 55:1735-1740.
55. Rogers AN, Vanburen DG, Hedblom EE, Tilahun ME, Telfer JC, Baldwin CL. 2005. Gammadelta T cell function varies with the expressed WC1 coreceptor. J Immunol. 174:3386-3393.
56. Ruiz-Larranaga O, Garrido JM, Iriondo M, Manzano C, Molina E, Koets AP, Rutten VP, Juste RA, Estonba A. 2010. Genetic association between bovine NOD2 polymorphisms and infection by Mycobacterium avium subsp. paratuberculosis in Holstein-Friesian cattle. Anim Genet. 41:652-655.
57. Sallusto F, Lanzavecchia A, Araki K, Ahmed R. 2010. From vaccines to memory and back. Immunity. 33: 451-463.
58. Santema W, Hensen S, Rutten V, Koets A. 2009a. Heat shock protein 70 subunit vaccination against bovine paratuberculosis does not interfere with current immunodiagnostic assays for bovine tuberculosis. Vaccine. 27:2312-2319.
59. Santema W, Overdijk M, Barends J, Krijgsveld J, Rutten V, Koets A. 2009b. Searching for proteins of Mycobacterium avium subspecies paratuberculosis with diagnostic potential by comparative qualitative proteomic analysis of mycobacterial tuberculins. Vet Microbiol. 138:191-196.
60. Santema W, van Kooten P, Hoek A, Leeflang M, Overdijk M, Rutten V, Koets A. 2011. Hsp70 vaccination-induced antibodies recognize B cell epitopes in the cell wall of Mycobacterium avium subspecies paratuberculosis. Vaccine. 29:1364-1373.
61. Shin SJ, Chang CF, Chang CD, McDonough SP, Thompson B, Yoo HS, Chang YF. 2005. In vitro cellular immune responses to recombinant antigens of Mycobacterium avium subsp. paratuberculosis. Infect Immunol. 73:5074-5085.
62. Stabel JR, Palmer MV, Harris B, Plattner B, Hostetter J, Robbe-Austerman S. 2009. Pathogenesis of Mycobacterium avium subsp. paratuberculosis in neonatal calves after oral or intraperitoneal experimental infection. Vet Microbiol. 136:306-313.
63. Stabel JR, Robbe-Austerman S. 2011. Early immune markers associated with Mycobacterium avium subsp. paratuberculosis (MAP) infection in a neonatal calf model. Clin Vaccine Immunol. 18:393-405.
64. Stevenson K, Hughes VM, de Juan L, Inglis NF, Wright F, Sharp JM. 2002. Molecular characterization of pigmented and nonpigmented isolates of Mycobacterium avium subsp. paratuberculosis. J Clin Microbiol. 40:1798-1804.
65. Stewart DJ, Vaughan JA, Stiles PL, Noske PJ, Tizard ML, Prowse SJ, Michalski WP, Butler KL, Jones SL. 2007. A long-term bacteriological and immunological study in Holstein-Friesian cattle experimentally infected with Mycobacterium avium subsp. paratuberculosis and necropsy culture results for Holstein-Friesian cattle, Merino sheep and Angora goats. Vet Microbiol. 122:83-96.
66. Sweeney RW. 1996. Transmission of paratuberculosis. Vet Clin North Am Food Anim Pract. 12:305-312.
67. Sweeney RW, Whitlock RH, Bowersock TL, Cleary DL, Meinert TR, Habecker PL, Pruitt GW. 2009. Effect of subcutaneous administration of a killed Mycobacterium avium subsp paratuberculosis vaccine on colonization of tissues following oral exposure to the organism in calves. Am J Vet Res. 70:493-497.
68. Teitelbaum R, Glatman-Freedman A, Chen B, Robbins JB, Unanue E, Casadevall A, Bloom BR. 1998. A mAb recognizing a surface antigen of Mycobacterium tuberculosis enhances host survival. Proc Natl Acad Sci. USA. 95:15688-15693.
69. Turenne CY, Wallace Jr R, Behr MA. 2007. Mycobacterium avium in the postgenomic era. Clinical microbiology reviews. 20:205-229.
70. Uzonna JE, Chilton P, Whitlock RH, Habecker PL, Scott P, Sweeney RW. 2003. Efficacy of commercial and field-strain Mycobacterium paratuberculosis vaccinations with recombinant IL-12 in a bovine experimental infection model. Vaccine. 21:3101-3109.
71. van Hulzen KJ, Heuven HC, Nielen M, Hoeboer J, Santema WJ, Koets AP. 2010. Different Mycobacterium avium subsp. paratuberculosis MIRU-VNTR patterns coexist within cattle herds. Vet Microbiol. 148:419-424.
72. van Hulzen KJ, Nielen M, Koets AP, de Jong G, van Arendonk JA, Heuven HC. 2011. Effect of herd prevalence on heritability estimates of antibody response to Mycobacterium avium subspecies paratuberculosis. J Dairy Sci. 94:992-997.
73. van Rhijn I, Nguyen TK, Michel A, Cooper D, Govaerts M, Cheng TY, van Eden W, Moody DB, Coetzer JA, Rutten V, et al. 2009. Low cross-reactivity of T-cell responses against lipids from Mycobacterium bovis and M. avium paratuberculosis during natural infection. Eur J Immunol. 39:3031-3041.
74. van Roermund HJ, Bakker D, Willemsen PT, de Jong MC. 2007. Horizontal transmission of Mycobacterium avium subsp. paratuberculosis in cattle in an experimental setting: calves can transmit the infection to other calves. Vet Microbiol. 122:270-279.
75. van Schaik G, Kalis CH, Benedictus G, Dijkhuizen AA, Huirne RB. 1996. Cost-benefit analysis of vaccination against paratuberculosis in dairy cattle. Vet Rec. 139:624-627.
76. Vary PH, Andersen PR, Green E, Hermon-Taylor J, McFadden JJ. 1990. Use of highly specific DNA probes and the polymerase chain reaction to detect Mycobacterium paratuberculosis in Johne's disease. J Clin Microbiol. 28:933-937.
77. Weber MF, Groenendaal H. 2011. Effects of infectious young stock on results of certification, surveillance and control programmes for paratuberculosis in dairy herds. Vet Microbiol. doi:10.1016/j.vetmic.2011.07.004.
78. Weber MF, Kogut J, de Bree J, van Schaik G, Nielen M. 2010. Age at which dairy cattle become Mycobacterium avium subsp. paratuberculosis faecal culture positive. Prev Vet Med. 97:29-36.
79. Weber MF, Nielen M, Velthuis AG, van Roermund HJ. 2008. Milk quality assurance for paratuberculosis: simulation of within-herd infection dynamics and economics. Vet Res. 39:12.
80. Weiss DJ, Evanson OA, de Souza C, Abrahamsen MS. 2005. A critical role of interleukin-10 in the response of bovine macrophages to infection by Mycobacterium avium subsp paratuberculosis. Am J Vet Res. 66:721-726.
81. Weiss DJ, Evanson OA, Moritz A, Deng MQ, Abrahamsen MS. 2002. Differential responses of bovine macrophages to Mycobacterium avium subsp. Para tuberculosis and Mycobacterium avium subsp. avium. Infect Immunol. 70:5556-5561.
82. Weiss DJ, Souza CD. 2008. Review paper: modulation of mononuclear phagocyte function by Mycobacterium avium subsp. paratuberculosis. Vet Pathol. 45:829-841.
83. Wentink GH, Bongers JH, Zeeuwen AA, Jaartsveld FH. 1994. Incidence of paratuberculosis after vaccination against M. paratuberculosis in two infected dairy herds. Zentralbl Veterinarmed. B. 41:517-522.
84. Whitlock RH, Wells SJ, Sweeney RW, van Tiem J. 2000. ELISA and fecal culture for paratuberculosis (Johne's disease): sensitivity and specificity of each method. Vet Microbiol. 77:387-398.
85. Whittington RJ, Marshall DJ, Nicholls PJ, Marsh IB, Reddacliff LA. 2004. Survival and dormancy of Mycobacterium avium subsp. paratuberculosis in the environment. Appl Environ Microbiol. 70:2989-3004.
86. Whittington RJ, Windsor PA. 2009. In utero infection of cattle with Mycobacterium avium subsp. paratuberculosis: a critical review and meta-analysis. Vet J. 179:60-69.
87. Windsor PA, Bush R, Links I, Eppleston J. 2005. Injury caused by self-inoculation with a vaccine of a Freund's complete adjuvant nature (Gudair) used for control of ovine paratuberculosis. Aust Vet J. 83: 216-220.
88. Windsor PA, Whittington RJ. 2009. Evidence for age susceptibility of cattle to Johne's disease. Vet J. 184: 37-44.