Host responses to persistent Mycobacterium avium subspecies paratuberculosis infection in surgically isolated bovine ileal segments

Clinical and Vaccine Immunology

Volumn 20, Issue 2, 2013, Pages 156-165

  Charavaryamath, Chandrashekhar ^a,d   Gonzalez Cano, Patricia ^a   Fries, Patrick ^a,e   Gomis, Susantha ^b   Doig, Kimberley ^a   Scruten, Erin ^a   Potter, Andrew ^a   Napper, Scott ^a,c   Griebel, Philip J ^a,c  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

^d WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

^e Centre for Food Borne and Animal Parasitology   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; T LYMPHOCYTE RECEPTOR; TOLL LIKE RECEPTOR 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIUM DETECTION; BIOACCUMULATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL SUBPOPULATION; CELLULAR IMMUNITY; CONTROLLED STUDY; COW; CYTOKINE RELEASE; DENDRITIC CELL; GAMMA DELTA T LYMPHOCYTE; HOST PATHOGEN INTERACTION; ILEUM DISEASE; IMMUNE RESPONSE; INTESTINE INFECTION; INTESTINE SURGERY; LAMINA PROPRIA; LEUKOCYTE; LYMPHATIC DRAINAGE; LYMPHOCYTE PROLIFERATION; MACROPHAGE; MALE; MESENTERY LYMPH NODE; MYCOBACTERIUM PARATUBERCULOSIS; NEWBORN; NONHUMAN; PARATUBERCULOSIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANIMALS, NEWBORN; CATTLE; CATTLE DISEASES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; ILEUM; INTERFERON-GAMMA; LYMPH NODES; LYMPHOCYTE ACTIVATION; MACROPHAGES; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS; PARATUBERCULOSIS; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; TOLL-LIKE RECEPTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84874925662     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00496-12     Document Type: Article

References (67)

1. Coussens PM. 2001. Mycobacterium paratuberculosis and the bovine immune system. Anim. Health Res. Rev. 2:141-161.
2. Stabel JR. 2006. Host responses to Mycobacterium avium subsp. paratuberculosis: a complex arsenal. Anim. Health Res. Rev. 7:61-70.
3. Ott SL, Wells SJ, Wagner BA. 1999. Herd-level economic losses associated with Johne's disease on US dairy operations. Prev. Vet. Med. 40:179-192.
4. Pradhan AK, Mitchell RM, Kramer AJ, Zurakowski MJ, Fyock TL, Whitlock RH, Smith JM, Hovingh E, Van Kessel JA, Karns JS, Schukken YH. 2011. Molecular epidemiology of Mycobacterium avium subsp. paratuberculosis in a longitudinal study of three dairy herds. J. Clin. Microbiol. 49:893-901.
5. Pierce ES. 2009. Where are all the Mycobacterium avium subspecies paratuberculosis in patients with Crohn's disease? PLoS Pathog. 5:e1000234. doi:10.1371/journal.ppat.1000234.
6. Van Kruiningen HJ. 2011. Where are the weapons of mass destruction - the Mycobacterium paratuberculosis in Crohn's disease? J. Crohns Colitis 5:638-644.
7. Whittington RJ, Windsor PA. 2009. In utero infection of cattle with Mycobacterium avium subsp. paratuberculosis: a critical review and metaanalysis. Vet. J. 179:60-69.
8. Khare S, Nunes J, Figueiredo J, Lawhon S, Rossetti C, Gull T, Rice-Ficht A, Garry AL. 2009. Early phase morphological lesions and transcriptional responses of bovine ileum infected with Mycobacterium avium subsp. paratuberculosis. Vet. Pathol. 46:717-728.
9. Pott J, Basler T, Duerr CU, Rohde M, Goethe R, Hornef MW. 2009. Internalization-dependent recognition of Mycobacterium avium ssp. paratuberculosis by intestinal epithelial cells. Cell. Microbiol. 11:1802-1815.
10. Sigurethardottir OG, Valheim M, Press CM. 2004. Establishment of Mycobacterium avium subsp. paratuberculosis infection in the intestine of ruminants. Adv. Drug Deliv. Rev. 56:819-834.
11. Sohal JS, Singh SV, Tyagi P, Subhodh S, Singh PK, Singh AV, Narayanasamy K, Sheoran N, Singh Sandhu K. 2008. Immunology of mycobacterial infections: with special reference to Mycobacterium avium subspecies paratuberculosis. Immunobiology 213:585-598.
12. Sigur-Dardottir OG, Press CM, Evensen O. 2001. Uptake of Mycobacterium avium subsp. paratuberculosis through the distal small intestinal mucosa in goats: an ultrastructural study. Vet. Pathol. 38:184-189.
13. Weiss DJ, Souza CD. 2008. Modulation of mononuclear phagocyte function by Mycobacterium avium subsp. paratuberculosis. Vet. Pathol. 45: 829-841.
14. DE Almeida DE, Colvin CJ, Coussens PM. 2008. Antigen-specific regulatory T cells in bovine paratuberculosis. Vet. Immunol. Immunopathol. 125:234-245.
15. Bassey EO, Collins MT. 1997. Study of T-lymphocyte subsets of healthy and Mycobacterium avium subsp. paratuberculosis-infected cattle. Infect. Immun. 65:4869-4872.
16. 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.
17. Coussens PM. 2004. Model for immune responses to Mycobacterium avium subspecies paratuberculosis in cattle. Infect. Immun. 72:3089-3096.
18. Rosseels V, Huygen K. 2008. Vaccination against paratuberculosis. Expert Rev. Vaccines 7:817-832.
19. Bull TJ, Gilbert SC, Sridhar S, Linedale R, Dierkes N, Sidi-Boumedine K, Hermon-Taylor J. 2007. A novel multi-antigen virally vectored vaccine against Mycobacterium avium subspecies paratuberculosis. PLoS One 2:e1229. doi:10.1371/journal.pone.0001229.
20. Huntley JF, Stabel JR, Paustian ML, Reinhardt TA, Bannantine JP. 2005. Expression library immunization confers protection against Mycobacterium avium subsp. paratuberculosis infection. Infect. Immun. 73: 6877-6884.
21. Roupie V, Leroy B, Rosseels V, Piersoel V, Noel-Georis I, Romano M, Govaerts M, Letesson JJ, Wattiez R, Huygen K. 2008. Immunogenicity and protective efficacy of DNA vaccines encoding MAP0586c and MAP4308c of Mycobacterium avium subsp. paratuberculosis secretome. Vaccine 26:4783-4794.
22. Roupie V, Rosseels V, Piersoel V, Zinniel DK, Barletta RG, Huygen K. 2008. Genetic resistance of mice to Mycobacterium paratuberculosis is influenced by Slc11a1 at the early but not at the late stage of infection. Infect. Immun. 76:2099-2105.
23. Momotani E, Whipple DL, Thiermann AB, Cheville NF. 1988. Role ofM cells and macrophages in the entrance of Mycobacterium paratuberculosis into domes of ileal Peyer's patches in calves. Vet. Pathol. 25:131-137.
24. Wu CW, Livesey M, Schmoller SK, Manning EJB, Steinberg H, Davis WC, Hamilton MJ, Talaat AM. 2007. Invasion and persistence of Mycobacterium avium subsp. paratuberculosis during early stages of Johne's disease in calves. Infect. Immun. 75:2110-2119.
25. Allen AJ, Park KT, Barrington GM, Lahmers KK, Hamilton MJ, Davis WC. 2009. Development of a bovine ileal cannulation model to study the immune response and mechanisms of pathogenesis of paratuberculosis. Clin. Vaccine Immunol. 16:453-463.
26. Charavaryamath C, Fries P, Gomis S, Bell C, Doig K, Guan LL, Potter A, Napper S, Griebel PJ. 2011. Mucosal changes in a long-term bovine intestinal segment model following removal of ingesta and microflora. Gut Microbes 2:134-144.
27. Fries P, Popowych YI, Guan LL, Beskorwayne T, Potter A, Babiuk L, Griebel PJ. 2011. Mucosal dendritic cell subpopulations in the small intestine of newborn calves. Dev. Comp. Immunol. 35:1040-1051.
28. Mookherjee N, Wilson HL, Doria S, Popowych Y, Falsafi R, Yu JJ, Li Y, Veatch S, Roche FM, Brown KL, Brinkman FS, Hokamp K, Potter A, Babiuk LA, Griebel PJ, Hancock RE. 2006. Bovine and human cathelicidin cationic host defense peptides similarly suppress transcriptional responses to bacterial lipopolysaccharide. J. Leukoc. Biol. 80:1563-1574.
29. Raggo C, Habermehl M, Babiuk LA, Griebel P. 2000. The in vivo effects of recombinant bovine herpesvirus-1 expressing bovine interferongamma. J. Gen. Virol. 81:2665-2673.
30. Buchanan RM, Popowych Y, Arsic N, Townsend HG, Mutwiri GK, Potter AA, Babiuk LA, Griebel PJ, Wilson HL. 2011. B-cell activating factor (BAFF) promotes CpG ODN-induced B cell activation and proliferation. Cell. Immunol. 271:16-28.
31. Fries PN, Griebel PJ. 2011. Mucosal dendritic cell diversity in the gastrointestinal tract. Cell Tissue Res. 343:33-41.
32. Davis WC, MacHugh ND, Park YH, Hamilton MJ, Wyatt CR. 1993. Identification of a monoclonal antibody reactive with the bovine orthologue of CD3 (BoCD3). Vet. Immunol. Immunopathol. 39:85-91.
33. Howard CJ, Morrison WI, Bensaid A, Davis W, Eskra L, Gerdes J, Hadam M, Hurley D, Leibold W, Letesson JJ. 1991. Summary of workshop findings for leukocyte antigens of cattle. Vet. Immunol. Immunopathol. 27:21-27.
34. Larsen RA, Monaghan ML, Park YH, Hamilton MJ, Ellis JA, Davis WC. 1990. Identification and characterization of monoclonal antibodies reactive with bovine, caprine and ovine T-lymphocyte determinants by flow microfluorimetry. Vet. Immunol. Immunopathol. 25:195-208.
35. Davis WC, Brown WC, Hamilton MJ, Wyatt CR, Orden JA, Khalid AM, Naessens J. 1996. Analysis of monoclonal antibodies specific for the gamma delta TcR. Vet. Immunol. Immunopathol. 52:275-283.
36. Harbo SJ, Barrington GM, Allen AJ, Sample GL, Parish SM, Hamilton MJ, Davis WC. 2004. Characterization of lymphocyte populations by flow cytometry in a calf with sporadic juvenile lymphoma. Vet. Clin. Pathol. 33:163-167.
37. Buergelt CD, Hall C, McEntee K, Duncan JR. 1978. Pathological evaluation of paratuberculosis in naturally infected cattle. Vet. Pathol. 15: 196-207.
38. Clarke CJ. 1997. The pathology and pathogenesis of paratuberculosis in ruminants and other species. J. Comp. Pathol. 116:217-261.
39. Balseiro A, Prieto JM, Espi A, Perez V, Garcia Marin JF. 2003. Presence of focal and multifocal paratuberculosis lesions in mesenteric lymph nodes and the ileocaecal valve of cattle positive to the tuberculin skin test. Vet. J. 166:210-212.
40. Hunnam JC, Wilson PR, Heuer C, Mackintosh CG, West DM, Clark RG. 2011. Histopathology of grossly normal mesenteric lymph nodes of New Zealand farmed red deer (Cervus elaphus) including identification of lipopigment. Vet. Pathol. 48:525-529.
41. Subharat S, Shu D, Wedlock DN, Price-Carter M, de Lisle GW, Luo D, Collins DM, Buddle BM. 2012. Immune responses associated with progression and control of infection in calves experimentally challenged with Mycobacterium avium subsp. paratuberculosis. Vet. Immunol. Immunopathol. 149:225-236.
42. Plattner BL, Chiang YW, Roth JA, Platt R, Huffman E, Zylstra J, Hostetter JM. 2011. Direct inoculation of Mycobacterium avium subspecies paratuberculosis into ileocecal Peyer's patches results in colonization of the intestine in a calf model. Vet. Pathol. 48:584-592.
43. Perez V, Garcia Marin JF, Badiola JJ. 1996. Description and classification of different types of lesion associated with natural paratuberculosis infection in sheep. J. Comp. Pathol. 114:107-122.
44. Gonzalez J, Geijo MV, Garcia-Pariente C, Verna A, Corpa JM, Reyes LE, Ferreras MC, Juste RA, Garcia Marin JF, Perez V. 2005. Histopathological classification of lesions associated with natural paratuberculosis infection in cattle. J. Comp. Pathol. 133:184-196.
45. Clark RG, Griffin JF, Mackintosh CG. 2010. Johne's disease caused by Mycobacterium avium subsp. paratuberculosis infection in red deer (Cervus elaphus): an histopathological grading system, and comparison of paucibacillary and multibacillary disease. N. Z. Vet. J. 58:90-97.
46. Mokresh AH, Czuprynski CJ, Butler DG. 1989. A rabbit model for study of Mycobacterium paratuberculosis infection. Infect. Immun. 57:3798-3807.
47. Lasco TM, Turner OC, Cassone L, Sugawara I, Yamada H, McMurray DN, Orme IM. 2004. Rapid accumulation of eosinophils in lung lesions in guinea pigs infected with Mycobacterium tuberculosis. Infect. Immun. 72: 1147-1149.
48. Vijayan VK, Reetha AM, Jawahar MS, Sankaran K, Prabhakar R. 1992. Pulmonary eosinophilia in pulmonary tuberculosis. Chest 101:1708-1709.
49. Kirman J, Zakaria Z, McCoy K, Delahunt B, Le Gros G. 2000. Role of eosinophils in the pathogenesis of Mycobacterium bovis BCG infection in gamma interferon receptor-deficient mice. Infect. Immun. 68:2976-2978.
50. Co DO, Hogan LH, Kim SI, Sandor M. 2004. Mycobacterial granulomas: keys to a long-lasting host-pathogen relationship. Clin. Immunol. 113: 130-136.
51. Aho AD, McNulty AM, Coussens PM. 2003. Enhanced expression of interleukin-1α and tumor necrosis factor receptor-associated protein 1 in ileal tissues of cattle infected with Mycobacterium avium subsp. paratuberculosis. Infect. Immun. 71:6479-6486.
52. Smeed JA, Watkins CA, Gossner AG, Hopkins J. 2010. Expression profiling reveals differences in immuno-inflammatory gene expression between the two disease forms of sheep paratuberculosis. Vet. Immunol. Immunopathol. 135:218-225.
53. Tanaka S, Sato M, Onitsuka T, Kamata H, Yokomizo Y. 2005. Inflammatory cytokine gene expression in different types of granulomatous lesions during asymptomatic stages of bovine paratuberculosis. Vet. Pathol. 42:579-588.
54. Tsuchiya T, Chida K, Suda T, Schneeberger EE, Nakamura H. 2002. Dendritic cell involvement in pulmonary granuloma formation elicited by bacillus Calmette-Guerin in rats. Am. J. Respir. Crit. Care Med. 165:1640-1646.
55. Schreiber HA, Sandor M. 2010. The role of dendritic cells in mycobacterium-induced granulomas. Immunol. Lett. 130:26-31.
56. Sun CM, Hall JA, Blank RB, Bouladoux N, Oukka M, Mora JR, Belkaid Y. 2007. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204:1775-1785.
57. Stabel JR. 2000. Transitions in immune responses to Mycobacterium paratuberculosis. Vet. Microbiol. 77:465-473.
58. + T-cell population. Vaccine 27:270-279.
59. + T cells, increased frequency of γδ T cells, and related changes in T-cell function. Infect. Immun. 70:3856-3864.
60. Navarro JA, Ramis G, Seva J, Pallares FJ, Sanchez J. 1998. Changes in lymphocyte subsets in the intestine and mesenteric lymph nodes in caprine paratuberculosis. J. Comp. Pathol. 118:109-121.
61. Skyberg JA, Thornburg T, Rollins M, Huarte E, Jutila MA, Pascual DW. 2011. Murine and bovine γδ T cells enhance innate immunity against Brucella abortus infections. PLoS One 6:e21978. doi:10.1371/journal.pone .0021978.
62. Simutis FJ, Jones DE, Hostetter JM. 2007. Failure of antigen-stimulated γδ T cells and CD4+ T cells from sensitized cattle to upregulate nitric oxide and mycobactericidal activity of autologous Mycobacterium avium subsp. paratuberculosis-infected macrophages. Vet. Immunol. Immunopathol. 116:1-12.
63. Werling D, Piercy J, Coffey TJ. 2006. Expression of Toll-like receptors (TLR) by bovine antigen-presenting cells - potential role in pathogen discrimination? Vet. Immunol. Immunopathol. 112:2-11.
64. 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.
65. Plain KM, Purdie AC, Begg DJ, de Silva K, Whittington RJ. 2010. Toll-like receptor (TLR)6 and TLR1 differentiation in gene expression studies of Johne's disease. Vet. Immunol. Immunopathol. 137:142-148.
66. Taylor DL, Zhong L, Begg DJ, de Silva K, Whittington RJ. 2008. Toll-like receptor genes are differentially expressed at the sites of infection during the progression of Johne's disease in outbred sheep. Vet. Immunol. Immunopathol. 124:132-151.
67. Thoma-Uszynski S, Stenger S, Takeuchi O, Ochoa MT, Engele M, Sieling PA, Barnes PF, Rollinghoff M, Bolcskei PL, Wagner M, Akira S, Norgard MV, Belisle JT, Godowski PJ, Bloom BR, Modlin RL. 2001. Induction of direct antimicrobial activity through mammalian toll-like receptors. Science 291:1544-1547.