Expression of genes associated with the antigen presentation and processing pathway are consistently regulated in early Mycobacterium avium subsp. paratuberculosis infection

Comparative Immunology, Microbiology and Infectious Diseases

Volumn 35, Issue 2, 2012, Pages 151-162

  Purdie, Auriol C ^a   Plain, Karren M ^a   Begg, Douglas J ^a   de Silva, Kumudika ^a   Whittington, Richard J ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Affymetrix; Antigen presentation and processing; Cattle; Genomics; Johne's disease; Microarray; Mycobacterium avium subsp. paratuberculosis; Paratuberculosis

Indexed keywords

CD8 ANTIGEN; GAMMA INTERFERON; RNA;

ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; ATYPICAL MYCOBACTERIOSIS; BACTERIAL GENE; BLOOD SAMPLING; CATTLE; COHORT ANALYSIS; CONTROLLED STUDY; GENE EXPRESSION PROFILING; GENE NUMBER; GENETIC ASSOCIATION; GENETIC VARIABILITY; IMMUNE RESPONSE; MHC GENE; MYCOBACTERIUM AVIUM; MYCOBACTERIUM PARATUBERCULOSIS; NONHUMAN; PARATUBERCULOSIS; PATHOGENESIS; RNA PROCESSING; TRANSCRIPTOMICS;

ANIMALS; ANTIGEN PRESENTATION; CATTLE; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; MOLECULAR SEQUENCE ANNOTATION; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS; PARATUBERCULOSIS; REPRODUCIBILITY OF RESULTS;

ANIMALIA; BOS; BOVINAE; MYCOBACTERIUM AVIUM; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS;

EID: 84857038209     PISSN: 01479571     EISSN: 18781667     Source Type: Journal    
DOI: 10.1016/j.cimid.2011.12.007     Document Type: Article

References (73)

1. Bush R.D., Windsor P.A., Toribio J.A. Losses of adult sheep due to ovine Johne's disease in 12 infected flocks over a 3-year period. Aust Vet J 2006, 84:246-253.
2. Harris N.B., Barletta R.G. Mycobacterium avium subsp. paratuberculosis in veterinary medicine. Clin Microbiol Rev 2001, 14:489-512.
3. Sewell G.W., Marks D.J., Segal A.W. The immunopathogenesis of Crohn's disease: a three-stage model. Curr Opin Immunol 2009, 21:506-513.
4. Behr M.A., Kapur V. The evidence for Mycobacterium paratuberculosis in Crohn's disease. Curr Opin Gastroenterol 2008, 24:17-21.
5. Chiodini R.J., Van Kruiningen H.J., Merkal R.S. Ruminant paratuberculosis (Johne's disease): the current status and future prospects. Cornell Vet 1984, 74:218-262.
6. Windsor P.A., Whittington R.J. Evidence for age susceptibility of cattle to Johne's disease. Vet J 2010, 184:37-44.
7. Bower K.L., Begg D.J., Whittington R.J. Culture of Mycobacterium avium subspecies paratuberculosis (MAP) from blood and extra-intestinal tissues in experimentally infected sheep. Vet Microbiol 2011, 147:127-132.
8. Hostetter J., Steadham E., Haynes J., Bailey T., Cheville N. Phagosomal maturation and intracellular survival of Mycobacterium avium subspecies paratuberculosis in J774 cells. Comp Immunol Microbiol Infect Dis 2003, 26:269-283.
9. Weiss D.J., Evanson O.A., McClenahan D.J., Abrahamsen M.S., Walcheck B.K. Regulation of expression of major histocompatibility antigens by bovine macrophages infected with Mycobacterium avium subsp. paratuberculosis or Mycobacterium avium subsp. avium. Infect Immun 2001, 69:1002-1008.
10. Begg D., Whittington R.J. Paratuberculosis in sheep. Paratuberculosis: organism, disease, control 2010, 157-168. CABI, Wallingford. M.A. Behr, D.M. Collins (Eds.).
11. Clarke C.J. The pathology and pathogenesis of paratuberculosis in ruminants and other species. J Comp Pathol 1997, 116:217-261.
12. Sohal J.S., Singh S.V., Tyagi P., Subhodh S., Singh P.K., Singh A.V., et al. Immunology of mycobacterial infections: with special reference to Mycobacterium avium subspecies paratuberculosis. Immunobiology 2008, 213:585-598.
13. Begg D.J., de Silva K., Carter N., Plain K.M., Purdie A., Whittington R.J. Does a th1 over th2 dominancy really exist in the early stages of mycobacterium avium subspecies paratuberculosis infections?. Immunobiology 2011, 216:840-846.
14. De Silva K., Begg D., Whittington R. The interleukin 10 response in ovine Johne's disease. Vet Immunol Immunopathol 2011, 139:10-16.
15. de Silva K., Begg D., Carter N., Taylor D., Di Fiore L., Whittington R. The early lymphocyte proliferation response in sheep exposed to Mycobacterium avium subsp. paratuberculosis compared to infection status. Immunobiology 2010, 215:12-25.
16. Tiwari A., VanLeeuwen J.A., McKenna S.L., Keefe G.P., Barkema H.W. Johne's disease in Canada Part I: clinical symptoms, pathophysiology, diagnosis, and prevalence in dairy herds. Can Vet J 2006, 47:874-882.
17. Begg D.J., de Silva K., Di Fiore L., Taylor D.L., Bower K., Zhong L., et al. Experimental infection model for Johne's disease using a lyophilised, pure culture, seedstock of Mycobacterium avium subspecies paratuberculosis. Vet Microbiol 2010, 141:301-311.
18. Marsh I.B., Bannantine J.P., Paustian M.L., Tizard M.L., Kapur V., Whittington R.J. Genomic comparison of Mycobacterium avium subsp. paratuberculosis sheep and cattle strains by microarray hybridization. J Bacteriol 2006, 188:2290-2293.
19. Huda A., Jungersen G., Christoffersen A.B., Lind P. Diagnosis of bovine paratuberculosis by interferon-gamma (IFN-γ) test. Acta Vet Scand 2003, 44:281.
20. Huda A., Lind P., Christoffersen A.B., Jungersen G. Analysis of repeated tests for interferon-gamma (IFN-γ) response and faecal excretion for diagnosis of subclinical paratuberculosis in Danish cattle. Vet Immunol Immunopathol 2003, 94:95-103.
21. Irizarry R.A., Hobbs B., Collin F., Beazer-Barclay Y.D., Antonellis K.J., Scherf U., et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264.
22. Hochberg Y., Benjamini Y. More powerful procedures for multiple significance testing. Stat Med 1990, 9:811-818.
23. Huang da W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
24. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., et al. Gene ontology: tool for the unification of biology. Nat Genet 2000, 25:25-29.
25. Kanehisa M. A database for post-genome analysis. Trends Genet 1997, 13:375-376.
26. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3.
27. Rozen S., Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 2000, 132:365-386.
28. -ΔΔCT method. Methods 2001, 25:402-408.
29. Weiss D.J., Evanson O.A., Deng M., Abrahamsen M.S. Gene expression and antimicrobial activity of bovine macrophages in response to Mycobacterium avium subsp. paratuberculosis. Vet Pathol 2004, 41:326-337.
30. Murphy J.T., Sommer S., Kabara E.A., Verman N., Kuelbs M.A., Saama P., et al. Gene expression profiling of monocyte-derived macrophages following infection with Mycobacterium avium subspecies avium and Mycobacterium avium subspecies paratuberculosis. Physiol Genomics 2006, 28:67-75.
31. Bannantine J.P., Talaat A.M. Genomic and transcriptomic studies in Mycobacterium avium subspecies paratuberculosis. Vet Immunol Immunopathol 2010, 138:303-311.
32. Kabara E., Kloss C.C., Wilson M., Tempelman R.J., Sreevatsan S., Janagama H., et al. A large-scale study of differential gene expression in monocyte-derived macrophages infected with several strains of Mycobacterium avium subspecies paratuberculosis. Brief Funct Genomics 2010, 9:220-237.
33. Verschoor C.P., Pant S.D., You Q., Kelton D.F., Karrow N.A. Gene expression profiling of PBMCs from Holstein and Jersey cows sub-clinically infected with Mycobacterium avium ssp. paratuberculosis. Vet Immunol Immunopathol 2010, 137:1-11.
34. Koets A.P., Rutten V.P., de Boer M., Bakker D., Valentin-Weigand P., van Eden W. Differential changes in heat shock protein-, lipoarabinomannan-, and purified protein derivative-specific immunoglobulin G1 and G2 isotype responses during bovine Mycobacterium avium subsp. paratuberculosis infection. Infect Immun 2001, 69:1492-1498.
35. Trombetta E.S., Mellman I. Cell biology of antigen processing in vitro and in vivo. Annu Rev Immunol 2005, 23:975-1028.
36. Pieters J. MHC class II-restricted antigen processing and presentation. Adv Immunol 2000, 75:159-208.
37. O'Rourke A.M., Rogers J., Mescher M.F. Activated CD8 binding to class I protein mediated by the T-cell receptor results in signalling. Nature 1990, 346:187-189.
38. Exley M., Wileman T., Mueller B., Terhorst C. Evidence for multivalent structure of T-cell antigen receptor complex. Mol Immunol 1995, 32:829-839.
39. Iezzi G., Karjalainen K., Lanzavecchia A. The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity 1998, 8:89-95.
40. Tessema M.Z., Koets A.P., Rutten V.P.M.G., Gruys E. How does Mycobacterium avium subsp. paratuberculosis resist intracellular degradation?. Vet Q 2001, 23:153-162.
41. Holling T.M., Schooten E., van Den Elsen P.J. Function and regulation of MHC class II molecules in T-lymphocytes: of mice and men. Hum Immunol 2004, 65:282-290.
42. van den Elsen P.J., Holling T.M., Kuipers H.F., van der Stoep N. Transcriptional regulation of antigen presentation. Curr Opin Immunol 2004, 16:67-75.
43. Pennini M.E., Pai R.K., Schultz D.C., Boom W.H., Harding C.V. Mycobacterium tuberculosis 19-kDa lipoprotein inhibits IFN-gamma-induced chromatin remodeling of MHC2TA by TLR2 and MAPK signaling. J Immunol 2006, 176:4323-4330.
44. Radosevich M., Ono S.J. Novel mechanisms of class II major histocompatibility complex gene regulation. Immunol Res 2003, 27:85-106.
45. Pamer E., Cresswell P. Mechanisms of MHC class I-restricted antigen processing. Annu Rev Immunol 1998, 16:323-358.
46. Van Hateren A., James E., Bailey A., Phillips A., Dalchau N., Elliott T. The cell biology of major histocompatibility complex class I assembly: towards a molecular understanding. Tissue Antigens 2010, 76:259-275.
47. Tufariello J.M., Chan J., Flynn J.L. Latent tuberculosis: mechanisms of host and bacillus that contribute to persistent infection. Lancet Infect Dis 2003, 3:578-590.
48. Wadee A.A., Kuschke R.H., Dooms T.G. The inhibitory effects of Mycobacterium tuberculosis on MHC class II expression by monocytes activated with riminophenazines and phagocyte stimulants. Clin Exp Immunol 1995, 100:434-439.
49. Pai R.K., Convery M., Hamilton T.A., Boom W.H., Harding C.V. Inhibition of IFN-gamma-induced class II transactivator expression by a 19-kDa lipoprotein from Mycobacterium tuberculosis: a potential mechanism for immune evasion. J Immunol 2003, 171:175-184.
50. Noss E.H., Pai R.K., Sellati T.J., Radolf J.D., Belisle J., Golenbock D.T., et al. Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis. J Immunol 2001, 167:910-918.
51. Pecora N.D., Gehring A.J., Canaday D.H., Boom W.H., Harding C.V. Mycobacterium tuberculosis LprA is a lipoprotein agonist of TLR2 that regulates innate immunity and APC function. J Immunol 2006, 177:422-429.
52. Cho S., Mehra V., Thoma-Uszynski S., Stenger S., Serbina N., Mazzaccaro R.J., et al. Antimicrobial activity of MHC class I-restricted CD8+ T cells in human tuberculosis. Proc Natl Acad Sci USA 2000, 97:12210-12215.
53. Flynn J.L., Chan J. Immune evasion by Mycobacterium tuberculosis: living with the enemy. Curr Opin Immunol 2003, 15:450-455.
54. Bonecini-Almeida M.G., Chitale S., Boutsikakis I., Geng J., Doo H., He S., et al. Induction of in vitro human macrophage anti-mycobacterium tuberculosis activity: requirement for IFN-γ and primed lymphocytes. J Immunol 1998, 160:4490-4499.
55. Waters W.R., Stabel J.R., Sacco R.E., Harp J.A., Pesch B.A., Wannemuehler M.J. Antigen-specific B-cell unresponsiveness induced by chronic Mycobacterium avium subsp. paratuberculosis infection of cattle. Infect Immun 1999, 67:1593-1598.
56. Liébana E., Girvin R.M., Welsh M., Neill S.D., Pollock J.M. Generation of CD8+ T-cell responses to Mycobacterium bovis and mycobacterial antigen in experimental bovine tuberculosis. Infect Immun 1999, 67:1034-1044.
57. de Almeida D.E., Colvin C.J., Coussens P.M. Antigen-specific regulatory T cells in bovine paratuberculosis. Vet Immunol Immunopathol 2008, 125:234-245.
58. Jun S.L., Sung J.S., Collins M.T., In D.J., Jeong Y.I., Lee C.M., et al. Mycobacterium avium subsp. paratuberculosis fibronectin attachment protein activates dendritic cells and induces a Th1 polarization. Infect Immun 2009, 77:2979-2988.
59. Robinson M.W., O'Brien R., Mackintosh C.G., Clark R.G., Griffin J.F.T. Immunoregulatory cytokines are associated with protection from immunopathology following Mycobacterium avium subspecies paratuberculosis infection in red deer. Infect Immun 2011, 79:2089-2097.
60. Germain R.N., Stefanova I. The dynamics of T cell receptor signaling: complex orchestration and the key roles of tempo and cooperation. Annu Rev Immunol 1999, 17:467-522.
61. Weiss A., Littman D.R. Signal transduction by lymphocyte antigen receptors. Cell 1994, 76:263-274.
62. Geisler C. Failure to synthesize the CD3-γ chain: consequences for T cell antigen receptor assembly, processing, and expression. J Immunol 1992, 148:2437-2445.
63. Au-Yeung B.B., Deindl S., Hsu L.Y., Palacios E.H., Levin S.E., Kuriyan J., et al. The structure, regulation, and function of ZAP-70. Immunol Rev 2009, 228:41-57.
64. Deindl S., Kadlecek T.A., Brdicka T., Cao X., Weiss A., Kuriyan J. Structural basis for the inhibition of tyrosine kinase activity of ZAP-70. Cell 2007, 129:735-746.
65. Kumar A., Humphreys T.D., Kremer K.N., Bramati P.S., Bradfield L., Edgar C.E., et al. CXCR4 physically associates with the T cell receptor to signal in T cells. Immunity 2006, 25:213-224.
66. Morra M., Zubiaur M., Terhorst C., Sancho J., Malavasi F. CD38 is functionally dependent on the TCR/CD3 complex in human T cells. FASEB J 1998, 12:581-592.
67. Viola A., Contento R.L., Molon B. T cells and their partners: the chemokine dating agency. Trends Immunol 2006, 27:421-427.
68. Juliarena M.A., Poli M., Sala L., Ceriani C., Gutierrez S., Dolcini G., et al. Association of BLV infection profiles with alleles of the BoLA-DRB3.2 gene. Anim Genet 2008, 39:432-438.
69. Kulberg S., Heringstad B., Guttersrud O.A., Olsaker I. Study on the association of BoLA-DRB3.2 alleles with clinical mastitis in Norwegian Red cows. J Anim Breed Genet 2007, 124:201-207.
70. Takeshima S., Matsumoto Y., Chen J., Yoshida T., Mukoyama H., Aida Y. Evidence for cattle major histocompatibility complex (BoLA) class II DQA1 gene heterozygote advantage against clinical mastitis caused by Streptococci and Escherichia species. Tissue Antigens 2008, 72:525-531.
71. Schwab A.E., Geary T.G., Baillargeon P., Schwab A.J., Fecteau G. Association of BoLA DRB3 and DQA1 alleles with susceptibility to Neospora caninum and reproductive outcome in Quebec Holstein cattle. Vet Parasitol 2009, 165:136-140.
72. Maillard J.C., Martinez D., Bensaid A. An amino acid sequence coded by the exon 2 of the BoLA DRB3 gene associated with a BoLA class I specificity constitutes a likely genetic marker of resistance to dermatophilosis in Brahman zebu cattle of Martinique (FWI). Ann N Y Acad Sci 1996, 791:185-197.
73. Reddacliff L.A., Beh K., McGregor H., Whittington R.J. A preliminary study of possible genetic influences on the susceptibility of sheep to Johne's disease. Aust Vet J 2005, 83:435-441.