Dynamics of immune effector mechanisms during infection with mycobacterium avium in C57BL/6 mice

Immunology

Volumn 140, Issue 2, 2013, Pages 232-243

  Haug, Markus ^a,b   Awuh, Jane A ^a   Steigedal, Magnus ^a,b   Frengen Kojen, June ^a   Marstad, Anne ^a   Nordrum, Ivar S ^a,b   Halaas, Øyvind ^a   Flo, Trude H ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b TRONDHEIM UNIVERSITY HOSPITAL   (Norway)

Author keywords

Adaptive immune response; CD4+ T cell subsets; Inflammation; Mouse infection model; Mycobacterium avium

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN M ANTIBODY; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; AVIAN TUBERCULOSIS; BACTERIAL LOAD; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CYTOKINE PRODUCTION; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LIVER CELL; LYMPHOCYTE SUBPOPULATION; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SPLEEN CELL; T LYMPHOCYTE;

ADAPTIVE IMMUNE RESPONSE; CD4+ T CELL SUBSETS; INFLAMMATION; MOUSE INFECTION MODEL; MYCOBACTERIUM AVIUM;

ANIMALS; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MYCOBACTERIUM AVIUM; REAL-TIME POLYMERASE CHAIN REACTION; TUBERCULOSIS;

EID: 84883785458     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12131     Document Type: Article

References (77)

1. Reichenbach J, Rosenzweig S, Doffinger R, Dupuis S, Holland SM, Casanova JL. Mycobacterial diseases in primary immunodeficiencies. Curr Opin Allergy Clin Immunol 2001; 1:503-11.
2. Wagner D, Young LS. Nontuberculous mycobacterial infections: a clinical review. Infection 2004; 32:257-70.
3. Griffith DE. Nontuberculous mycobacterial lung disease. Curr Opin Infect Dis 2010; 23:185-90.
4. Ehlers S. Why does tumor necrosis factor targeted therapy reactivate tuberculosis? J Rheumatol Suppl 2005; 74:35-9.
5. Winthrop KL, Chang E, Yamashita S, Iademarco MF, LoBue PA. Nontuberculous mycobacteria infections and anti-tumor necrosis factor-α therapy. Emerg Infect Dis 2009; 15:1556-61.
6. Jacobson MA, Hopewell PC, Yajko DM et al. Natural history of disseminated Mycobacterium avium complex infection in AIDS. J Infect Dis 1991; 164:994-8.
7. Horsburgh CR Jr. Mycobacterium avium complex infection in the acquired immunodeficiency syndrome. N Engl J Med 1991; 324:1332-8.
8. Horsburgh CR Jr, Gettings J, Alexander LN, Lennox JL. Disseminated Mycobacterium avium complex disease among patients infected with human immunodeficiency virus, 1985-2000. Clin Infect Dis 2001; 33:1938-43.
9. Hazra R, Robson CD, Perez-Atayde AR, Husson RN. Lymphadenitis due to nontuberculous mycobacteria in children: presentation and response to therapy. Clin Infect Dis 1999; 28:123-9.
10. Thegerstrom J, Romanus V, Friman V, Brudin L, Haemig PD, Olsen B. Mycobacterium avium lymphadenopathy among children, Sweden. Emerg Infect Dis 2008; 14:661-3.
11. van Ingen J, Egelund EF, Levin A et al. The pharmacokinetics and pharmacodynamics of pulmonary Mycobacterium avium complex disease treatment. Am J Respir Crit Care Med 2012; 186:559-65.
12. Griffith DE, Aksamit TR. Therapy of refractory nontuberculous mycobacterial lung disease. Curr Opin Infect Dis 2012; 25:218-27.
13. + T cells. Int Immunol 1996; 8:1299-310.
14. Cooper AM, Pearl JE, Brooks JV, Ehlers S, Orme IM. Expression of the nitric oxide synthase 2 gene is not essential for early control of Mycobacterium tuberculosis in the murine lung. Infect Immun 2000; 68:6879-82.
15. Gomes MS, Florido M, Pais TF, Appelberg R. Improved clearance of Mycobacterium avium upon disruption of the inducible nitric oxide synthase gene. J Immunol 1999; 162:6734-9.
16. Cooper AM, Appelberg R, Orme IM. Immunopathogenesis of Mycobacterium avium infection. Front Biosci 1998; 3:e141-8.
17. Appelberg R. Pathogenesis of Mycobacterium avium infection: typical responses to an atypical mycobacterium? Immunol Res 2006; 35:179-90.
18. Appelberg R, Castro AG, Pedrosa J, Silva RA, Orme IM, Minoprio P. Role of γ interferon and tumor necrosis factor α during T-cell-independent and -dependent phases of Mycobacterium avium infection. Infect Immun 1994; 62:3962-71.
19. Altare F, Durandy A, Lammas D et al. Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science 1998; 280:1432-5.
20. Dorman SE, Picard C, Lammas D et al. Clinical features of dominant and recessive interferon γ receptor 1 deficiencies. Lancet 2004; 364:2113-21.
21. Hambleton S, Salem S, Bustamante J et al. IRF8 mutations and human dendritic-cell immunodeficiency. N Engl J Med 2011; 365:127-38.
22. Berrington WR, Hawn TR. Mycobacterium tuberculosis, macrophages, and the innate immune response: does common variation matter? Immunol Rev 2007; 219:167-86.
23. Cooper AM, Mayer-Barber KD, Sher A. Role of innate cytokines in mycobacterial infection. Mucosal Immunol 2011; 4:252-60.
24. + recycling endocytic pathway and avoid lipocalin 2 trafficking to the lysosomal pathway. J Infect Dis 2010; 201:783-92.
25. Saiga H, Nishimura J, Kuwata H et al. Lipocalin 2-dependent inhibition of mycobacterial growth in alveolar epithelium. J Immunol 2008; 181:8521-7.
26. Nishimura J, Saiga H, Sato S et al. Potent antimycobacterial activity of mouse secretory leukocyte protease inhibitor. J Immunol 2008; 180:4032-9.
27. Yuk JM, Shin DM, Lee HM et al. Vitamin D3 induces autophagy in human monocytes/macrophages via cathelicidin. Cell Host Microbe 2009; 6:231-43.
28. + T cells and protective memory against tuberculosis. Tuberculosis (Edinb) 2007; 87:465-73.
29. Maglione PJ, Chan J. How B cells shape the immune response against Mycobacterium tuberculosis. Eur J Immunol 2009; 39:676-86.
30. Abebe F, Bjune G. The protective role of antibody responses during Mycobacterium tuberculosis infection. Clin Exp Immunol 2009; 157:235-43.
31. Fattorini L, Mattei M, Placido R et al. Mycobacterium avium infection in BALB/c and SCID mice. J Med Microbiol 1999; 48:577-83.
32. Chen ZW. Immune regulation of γδ T cell responses in mycobacterial infections. Clin Immunol 2005; 116:202-7.
33. + T-cell responses in HIV-positive patients with mycobacterial immune restoration disease. Eur J Immunol 2009; 39:391-403.
34. Jonsson B, Ridell M, Wold AE. Non-tuberculous mycobacteria and their surface lipids efficiently induced IL-17 production in human T cells. Microbes Infect 2012; 14:1186-95.
35. Kolls JK, Linden A. Interleukin-17 family members and inflammation. Immunity 2004; 21:467-76.
36. + regulatory T cells in the human immune system. Nat Rev Immunol 2010; 10:490-500.
37. Horan KL, Freeman R, Weigel K et al. Isolation of the genome sequence strain Mycobacterium avium 104 from multiple patients over a 17-year period. J Clin Microbiol 2006; 44:783-9.
38. Semret M, Zhai G, Mostowy S et al. Extensive genomic polymorphism within Mycobacterium avium. J Bacteriol 2004; 186:6332-4.
39. Saunders BM, Dane A, Briscoe H, Britton WJ. Characterization of immune responses during infection with Mycobacterium avium strains 100, 101 and the recently sequenced 104. Immunol Cell Biol 2002; 80:544-9.
40. Flo TH, Smith KD, Sato S et al. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 2004; 432:917-21.
41. Doherty TM, Sher A. Defects in cell-mediated immunity affect chronic, but not innate, resistance of mice to Mycobacterium avium infection. J Immunol 1997; 158:4822-31.
42. Baldridge MT, King KY, Boles NC, Weksberg DC, Goodell MA. Quiescent haematopoietic stem cells are activated by IFN-γ in response to chronic infection. Nature 2010; 465:793-7.
43. O'Reilly RA. Splenomegaly in 2, 505 patients at a large university medical center from 1913 to 1995. 1963 to 1995: 449 patients. West J Med 1998; 169:88-97.
44. Russell DG, Barry CE III, Flynn JL. Tuberculosis: what we don't know can, and does, hurt us. Science 2010; 328:852-6.
45. Kondratieva E, Logunova N, Majorov K, Averbakh M, Apt A. Host genetics in granuloma formation: human-like lung pathology in mice with reciprocal genetic susceptibility to M. tuberculosis and M. avium. PLoS One 2010; 5:e10515.
46. Berger T, Togawa A, Duncan GS et al. Lipocalin 2-deficient mice exhibit increased sensitivity to Escherichia coli infection but not to ischemia-reperfusion injury. Proc Natl Acad Sci U S A 2006; 103:1834-9.
47. Kjeldsen L, Cowland JB, Borregaard N. Human neutrophil gelatinase-associated lipocalin and homologous proteins in rat and mouse. Biochim Biophys Acta 2000; 1482:272-83.
48. Khader SA, Gopal R. IL-17 in protective immunity to intracellular pathogens. Virulence 2010; 1:423-7.
49. Cruz A, Fraga AG, Fountain JJ et al. Pathological role of interleukin 17 in mice subjected to repeated BCG vaccination after infection with Mycobacterium tuberculosis. J Exp Med 2010; 207:1609-16.
50. Urdahl KB, Shafiani S, Ernst JD. Initiation and regulation of T-cell responses in tuberculosis. Mucosal Immunol 2011; 4:288-93.
51. Pedrosa J, Florido M, Kunze ZM et al. Characterization of the virulence of Mycobacterium avium complex (MAC) isolates in mice. Clin Exp Immunol 1994; 98:210-6.
52. Benini J, Ehlers EM, Ehlers S. Different types of pulmonary granuloma necrosis in immunocompetent vs. TNFRp55-gene-deficient mice aerogenically infected with highly virulent Mycobacterium avium. J Pathol 1999; 189:127-37.
53. Florido M, Cooper AM, Appelberg R. Immunological basis of the development of necrotic lesions following Mycobacterium avium infection. Immunology 2002; 106:590-601.
54. Florido M, Goncalves AS, Silva RA, Ehlers S, Cooper AM, Appelberg R. Resistance of virulent Mycobacterium avium to γ interferon-mediated antimicrobial activity suggests additional signals for induction of mycobacteriostasis. Infect Immun 1999; 67:3610-8.
55. Rodrigues PN, Gomes SS, Neves JV et al. Mycobacteria-induced anaemia revisited: a molecular approach reveals the involvement of NRAMP1 and lipocalin-2, but not of hepcidin. Immunobiology 2011; 216:1127-34.
56. Appelberg R, Castro AG, Gomes S, Pedrosa J, Silva MT. Susceptibility of beige mice to Mycobacterium avium: role of neutrophils. Infect Immun 1995; 63:3381-7.
57. Petrofsky M, Bermudez LE. Neutrophils from Mycobacterium avium-infected mice produce TNF-α, IL-12, and IL-1β and have a putative role in early host response. Clin Immunol 1999; 91:354-8.
58. Maglione PJ, Xu J, Chan J. B cells moderate inflammatory progression and enhance bacterial containment upon pulmonary challenge with Mycobacterium tuberculosis. J Immunol 2007; 178:7222-34.
59. Phuah JY, Mattila JT, Lin PL, Flynn JL. Activated B cells in the granulomas of nonhuman primates infected with Mycobacterium tuberculosis. Am J Pathol 2012; 181:508-14.
60. Guirado E, Amat I, Gil O et al. Passive serum therapy with polyclonal antibodies against Mycobacterium tuberculosis protects against post-chemotherapy relapse of tuberculosis infection in SCID mice. Microbes Infect 2006; 8:1252-9.
61. Smith D, Hansch H, Bancroft G, Ehlers S. T-cell-independent granuloma formation in response to Mycobacterium avium: role of tumour necrosis factor-α and interferon-γ. Immunology 1997; 92:413-21.
62. Ehlers S, Benini J, Kutsch S, Endres R, Rietschel ET, Pfeffer K. Fatal granuloma necrosis without exacerbated mycobacterial growth in tumor necrosis factor receptor p55 gene-deficient mice intravenously infected with Mycobacterium avium. Infect Immun 1999; 67:3571-9.
63. Bermudez LE, Young LS. Tumor necrosis factor, alone or in combination with IL-2, but not IFN-γ, is associated with macrophage killing of Mycobacterium avium complex. J Immunol 1988; 140:3006-13.
64. Champsi JH, Bermudez LE, Young LS. The role of cytokines in mycobacterial infection. Biotherapy 1994; 7:187-93.
65. Flynn JL, Goldstein MM, Chan J et al. Tumor necrosis factor-α is required in the protective immune response against Mycobacterium tuberculosis in mice. Immunity 1995; 2:561-72.
66. Silva RA, Gomes MS, Appelberg R. Minor role played by type I tumour necrosis factor receptor in the control of Mycobacterium avium proliferation in infected mice. Immunology 2000; 99:203-7.
67. Lindenstrom T, Agger EM, Korsholm KS et al. Tuberculosis subunit vaccination provides long-term protective immunity characterized by multifunctional CD4 memory T cells. J Immunol 2009; 182:8047-55.
68. Darrah PA, Patel DT, De Luca PM et al. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med 2007; 13:843-50.
69. Kagina BM, Abel B, Scriba TJ et al. Specific T cell frequency and cytokine expression profile do not correlate with protection against tuberculosis after bacillus Calmette-Guérin vaccination of newborns. Am J Respir Crit Care Med 2010; 182:1073-9.
70. Tameris MD, Hatherill M, Landry BS et al. Safety and efficacy of MVA85A, a new tuberculosis vaccine, in infants previously vaccinated with BCG: a randomised, placebo-controlled phase 2b trial. Lancet 2013; 381:1021-8.
71. Sarmento AM, Appelberg R. Relationship between virulence of Mycobacterium avium strains and induction of tumor necrosis factor α production in infected mice and in in vitro-cultured mouse macrophages. Infect Immun 1995; 63:3759-64.
72. + T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat Immunol 2007; 8:369-77.
73. Torrado E, Cooper AM. IL-17 and Th17 cells in tuberculosis. Cytokine Growth Factor Rev 2010; 21:455-62.
74. Phyu S, Sornes S, Mustafa T, Tadesse A, Jonsson R, Bjune G. Changes in T-lymphocyte subsets in lungs and spleens of mice with slowly progressive primary Mycobacterium tuberculosis infection: involvement of unconventional T-cell subsets. Scand J Immunol 1999; 50:137-44.
75. Lockhart E, Green AM, Flynn JL. IL-17 production is dominated by γδ T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J Immunol 2006; 177:4662-9.
76. Cruz A, Khader SA, Torrado E et al. Cutting edge: IFN-γ regulates the induction and expansion of IL-17-producing CD4 T cells during mycobacterial infection. J Immunol 2006; 177:1416-20.
77. Scott-Browne JP, Shafiani S, Tucker-Heard G et al. Expansion and function of Foxp3-expressing T regulatory cells during tuberculosis. J Exp Med 2007; 204:2159-69.