Indoleamine 2,3-dioxygenase, tryptophan catabolism, and Mycobacterium avium subsp. paratuberculosis: A model for chronic mycobacterial infections

Infection and Immunity

Volumn 79, Issue 9, 2011, Pages 3821-3832

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

^a UNIVERSITY OF SYDNEY   (Australia)

^b CHILDREN S HOSPITAL AT WESTMEAD   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

INDOLEAMINE 2,3 DIOXYGENASE; TRYPTOPHAN;

AMINO ACID BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATYPICAL MYCOBACTERIOSIS; BACTERIAL VIRULENCE; BIOSYNTHESIS; CATABOLISM; CATTLE; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; ILEUM; IMMUNE RESPONSE; MONOCYTE; MYCOBACTERIUM PARATUBERCULOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SHEEP; TH1 CELL; UPREGULATION;

ANIMALS; CATTLE; CELL LINE; DISEASE PROGRESSION; HUMANS; ILEUM; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS; PARATUBERCULOSIS; RNA, MESSENGER; SHEEP; TH1 CELLS; TRYPTOPHAN;

EID: 80052320930     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05204-11     Document Type: Article

References (54)

1. Almeida, A. S., et al. 2009. Tuberculosis is associated with a down-modulatory lung immune response that impairs Th1-type immunity. J. Immunol. 183:718-731.
2. Barceló-Batllori, S., et al. 2002. Proteomic analysis of cytokine induced proteins in human intestinal epithelial cells: implications for inflammatory bowel diseases. Proteomics 2:551-560.
3. Begg, D. J., et al. 2011. Does a Th1 over Th2 dominancy really exist in the early stages of Mycobacterium avium subspecies paratuberculosis infections? Immunobiology 216:840-846.
4. Begg, D. J., et al. 2010. Experimental infection model for Johne's disease using a lyophilised, pure culture, seedstock of Mycobacterium avium subspecies paratuberculosis. Vet. Microbiol. 141:301-311.
5. Belkaid, Y. 2007. Regulatory T cells and infection: a dangerous necessity. Nat. Rev. Immunol. 7:875-888.
6. Bold, T. D., and J. D. Ernst. 2009. Who benefits from granulomas, mycobacteria or host? Cell 136:17-19.
7. Bower, K. L., D. J. Begg, and R. J. Whittington. 2011. Culture of Mycobacterium avium subspecies paratuberculosis (MAP) from blood and extra-intestinal tissues in experimentally infected sheep. Vet. Microbiol. 147:127-132.
8. Bozza, S., et al. 2005. A crucial role for tryptophan catabolism at the host/ Candida albicans interface. J. Immunol. 174:2910-2918.
9. Brown, J., S. E. Howie, and G. Entrican. 2001. A role for tryptophan in immune control of chlamydial abortion in sheep. Vet. Immunol. Immunopathol. 82:107-119.
10. Bush, R. D., P. A. Windsor, and J. A. Toribio. 2006. Losses of adult sheep due to ovine Johne's disease in 12 infected flocks over a 3-year period. Aust. Vet. J. 84:246-253.
11. Carlin, J. M., E. C. Borden, P. M. Sondel, and G. I. Byrne. 1989. Interferoninduced indoleamine 2,3-dioxygenase activity in human mononuclear phagocytes. J. Leukoc. Biol. 45:29-34.
12. Chung, D. J., et al. 2009. Indoleamine 2,3-dioxygenase-expressing mature human monocyte-derived dendritic cells expand potent autologous regulatory T cells. Blood 114:555-563.
13. Clarke, C. J. 1997. The pathology and pathogenesis of paratuberculosis in ruminants and other species. J. Comp. Pathol. 116:217-261.
14. Dennis, M. M., et al. 2008. Association of severity of enteric granulomatous inflammation with disseminated Mycobacterium avium subspecies paratuberculosis infection and antemortem test results for paratuberculosis in dairy cows. Vet. Microbiol. 131:154-163.
15. Dennis, M. M., L. A. Reddacliff, and R. J. Whittington. 2010. Longitudinal study of clinicopathological features of Johne's disease in sheep naturally exposed to Mycobacterium avium subspecies paratuberculosis. Vet. Pathol. 48:565-575.
16. de Silva, K., et al. 2010. The early lymphocyte proliferation response in sheep exposed to Mycobacterium avium subsp. paratuberculosis compared to infection status. Immunobiology 215:12-25.
17. Desvignes, L., and J. D. Ernst. 2009. Gamma interferon-responsive nonhematopoietic cells regulate the immune response to Mycobacterium tuberculosis. Immunity 31:974-985.
18. Fenhalls, G., et al. 2002. Distribution of IFN-gamma, IL-4 and TNF-alpha protein and CD8 T cells producing IL-12p40 mRNA in human lung tuberculous granulomas. Immunology 105:325-335.
19. Ferdinande, L., et al. 2008. Inflamed intestinal mucosa features a specific epithelial expression pattern of indoleamine 2,3-dioxygenase. Int. J. Immunopathol. Pharmacol. 21:289-295.
20. Fitzgerald, P., et al. 2008. Tryptophan catabolism in females with irritable bowel syndrome: relationship to gamma interferon, severity of symptoms and psychiatric co-morbidity. Neurogastroenterol. Motil. 20:1291-1297.
21. Flynn, J. L., et al. 1993. An essential role for gamma interferon in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 178:2249-2254.
22. Gumber, S., D. L. Taylor, I. B. Marsh, and R. J. Whittington. 2009. Growth pattern and partial proteome of Mycobacterium avium subsp. paratuberculosis during the stress response to hypoxia and nutrient starvation. Vet. Microbiol. 133:344-357.
23. Harris, N. B., and R. G. Barletta. 2001. Mycobacterium avium subsp. paratuberculosis in veterinary medicine. Clin. Microbiol. Rev. 14:489-512.
24. Hayashi, T., et al. 2001. Enhancement of innate immunity against Mycobacterium avium infection by immunostimulatory DNA is mediated by indoleamine 2,3-dioxygenase. Infect. Immun. 69:6156-6164.
25. Hostetter, J., E. Steadham, J. Haynes, T. Bailey, and N. Cheville. 2003. Phagosomal maturation and intracellular survival of Mycobacterium avium subspecies paratuberculosis in J774 cells. Comp. Immunol. Microbiol. Infect. Dis. 26:269-283
26. Jungersen, G., A. Huda, J. J. Hansen, and P. Lind. 2002. Interpretation of the gamma interferon test for diagnosis of subclinical paratuberculosis in cattle. Clin. Diagn. Lab. Immunol. 9:453-460.
27. Kabara, E., et al. 2010. A large-scale study of differential gene expression in monocyte-derived macrophages infected with several strains of Mycobacterium avium subspecies paratuberculosis. Brief Funct. Genomics 9:220-237.
28. Katz, J. B., A. J. Muller, and G. C. Prendergast. 2008. Indoleamine 2,3-dioxygenase in T-cell tolerance and tumoral immune escape. Immunol. Rev. 222:206-221.
29. Kawaji, S., D. L. Taylor, Y. Mori, and R. J. Whittington. 2007. Detection of Mycobacterium avium subsp. paratuberculosis in ovine faeces by direct quantitative PCR has similar or greater sensitivity compared to radiometric culture. Vet. Microbiol. 125:36-48.
30. Kim, C. J., et al. 2010. L-Tryptophan exhibits therapeutic function in a porcine model of dextran sodium sulfate (DSS)-induced colitis. J. Nutr. Biochem. 21:468-475.
31. Kincaid, E. Z., and J. D. Ernst. 2003. Mycobacterium tuberculosis exerts gene-selective inhibition of transcriptional responses to IFN-gamma without inhibiting STAT1 function. J. Immunol. 171:2042-2049.
32. Le Floc'h, N., D. Melchior, and B. Sève. 2008. Dietary tryptophan helps to preserve tryptophan homeostasis in pigs suffering from lung inflammation. J. Anim. Sci. 86:3473-3479.
33. -ΔΔCT method. Methods 25:402-408.
34. Logan, G. J., et al. 2002. HeLa cells cocultured with peripheral blood lymphocytes acquire an immuno-inhibitory phenotype through up-regulation of indoleamine 2,3-dioxygenase activity. Immunology 105:478-487.
35. MacKenzie, C. R., U. Hadding, and W. Daubener. 1998. Gamma interferoninduced activation of indoleamine 2,3-dioxygenase in cord blood monocytederived macrophages inhibits the growth of group B streptococci. J. Infect. Dis. 178:875-878.
36. Makala, L. H., et al. 2011. Leishmania major attenuates host immunity by stimulating local indoleamine 2,3-dioxygenase expression. J. Infect. Dis. 203: 715-725.
37. Mellor, A. 2005. Indoleamine 2,3 dioxygenase and regulation of T cell immunity. Biochem. Biophys. Res. Commun. 338:20-24.
38. Mellor, A. L., and D. H. Munn. 2004. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat. Rev. Immunol. 4:762-774.
39. Nacy, C., and M. Buckley. 2008. Mycobacterium avium paratuberculosis: infrequent human pathogen or public health threat? American Academy of Microbiology, Washington, DC. http://academy.asm.org/images/stories/documents/mycobacteriumaviumparatuberculosis.pdf.
40. Pardridge, W. M., and G. Fierer. 1990. Transport of tryptophan into brain from the circulating, albumin-bound pool in rats and in rabbits. J. Neurochem. 54:971-976.
41. Pérez, V., J. F. Garcia Marin, and J. J. Badiola. 1996. Description and classification of different types of lesion associated with natural paratuberculosis infection in sheep. J. Comp. Pathol. 114:107-122.
42. Reddacliff, L. A., P. J. Nicholls, A. Vadali, and R. J. Whittington. 2003. Use of growth indices from radiometric culture for quantification of sheep strains of Mycobacterium avium subsp. paratuberculosis. Appl. Environ. Microbiol. 69:3510-3516.
43. Sakurai, K., J. P. Zou, J. R. Tschetter, J. M. Ward, and G. M. Shearer. 2002. Effect of indoleamine 2,3-dioxygenase on induction of experimental autoimmune encephalomyelitis. J. Neuroimmunol. 129:186-196.
44. Sewell, G. W., D. J. Marks, and A. W. Segal. 2009. The immunopathogenesis of Crohn's disease: a three-stage model. Curr. Opin. Immunol. 21:506-513.
45. Sźantó, S., et al. 2007. Inhibition of indoleamine 2,3-dioxygenase-mediated tryptophan catabolism accelerates collagen-induced arthritis in mice. Arthritis Res. Ther. 9:R50.
46. Tattevin, P., et al. 2010. Enhanced indoleamine 2,3-dioxygenase activity in patients with severe sepsis and septic shock. J. Infect. Dis. 201:956-966.
47. Taylor, D. L., P. C. Thomson, K. de Silva, and R. J. Whittington. 2007. Validation of endogenous reference genes for expression profiling of RAW264.7 cells infected with Mycobacterium avium subsp. paratuberculosis by quantitative PCR. Vet. Immunol. Immunopathol. 115:43-55.
48. Taylor, D. L., L. Zhong, D. J. Begg, K. de Silva, and R. J. Whittington. 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.
49. Thomas, S. M., et al. 1993. IFN-gamma-mediated antimicrobial response. Indoleamine 2,3-dioxygenase-deficient mutant host cells no longer inhibit intracellular Chlamydia spp. or Toxoplasma growth. J. Immunol. 150:5529-5534.
50. Weiss, D. J., O. A. Evanson, D. J. McClenahan, M. S. Abrahamsen, and B. K. Walcheck. 2001. Regulation of expression of major histocompatibility antigens by bovine macrophages infected with Mycobacterium avium subsp. paratuberculosis or Mycobacterium avium subsp. avium. Infect. Immun. 69:1002-1008.
51. Whittington, R. J., D. J. Begg, K. de Silva, K. M. Plain, and A. C. Purdie. 2011. Comparative immunological and microbiological aspects of paratuber-culosis as a model mycobacterial infection. Vet. Immunol. Immunopathol. doi:10.1016/j.vetimm.2011.03.003.
52. Wirleitner, B., G. Neurauter, K. Schrocksnadel, B. Frick, and D. Fuchs. 2003. Gamma interferon-induced conversion of tryptophan: immunologic and neuropsychiatric aspects. Curr. Med. Chem. 10:1581-1591.
53. Zelante, T., F. Fallarino, F. Bistoni, P. Puccetti, and L. Romani. 2009.Indoleamine 2,3-dioxygenase in infection: the paradox of an evasive strategy that benefits the host. Microbes Infect. 11:133-141.
54. Zhong, L., et al. 2009. Identification of differentially expressed genes in ileum, intestinal lymph node and peripheral blood mononuclear cells of sheep infected with Mycobacterium avium subsp. paratuberculosis using differential display PCR. Vet. Immunol. Immunopathol. 131:177-189.