Comparison of interferon-γ-, interleukin (IL)-17- and IL-22-expressing CD4 T cells, IL-22-expressing granulocytes and proinflammatory cytokines during latent and active tuberculosis infection

Clinical and Experimental Immunology

Volumn 167, Issue 2, 2012, Pages 317-329

  Cowan, J ^a   Pandey, S ^b   Filion, L G ^b   Angel, J B ^a,b   Kumar, A ^b,c   Cameron, D W ^a,b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c CHILDREN S HOSPITAL OF EASTERN ONTARIO   (Canada)

Author keywords

Active tuberculosis; Human; Interleukin 17; Interleukin 22; Latent tuberculosis

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 22; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; GRANULOCYTE; HUMAN; IMMUNOSTIMULATION; MALE; PRIORITY JOURNAL; TH17 CELL; TUBERCULOSIS;

ADULT; CD4-POSITIVE T-LYMPHOCYTES; CYTOKINES; ETHNIC GROUPS; FEMALE; GRANULOCYTES; HUMANS; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKINS; LATENT TUBERCULOSIS; MALE; MIDDLE AGED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TH17 CELLS; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA; YOUNG ADULT;

EID: 84862946782     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2011.04520.x     Document Type: Article

References (65)

1. Dye C, Scheele S, Dolin P, Pathania V, Raviglione MC. Consensus statement. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project. JAMA 1999; 282:677-86.
2. Cooper AM, Kipnis A, Turner J, Magram J, Ferrante J, Orme IM. Mice lacking bioactive IL-12 can generate protective, antigen-specific cellular responses to mycobacterial infection only if the IL-12 p40 subunit is present. J Immunol 2002; 168:1322-7.
3. Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, Orme IM. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med 1993; 178:2243-7.
4. Lyakh L, Trinchieri G, Provezza L, Carra G, Gerosa F. Regulation of interleukin-12/interleukin-23 production and the T-helper 17 response in humans. Immunol Rev 2008; 226:112-31.
5. Curtis MM, Way SS. Interleukin-17 in host defence against bacterial, mycobacterial and fungal pathogens. Immunology 2009; 126:177-85.
6. Bettelli E, Korn T, Oukka M, Kuchroo VK. Induction and effector functions of T(H)17 cells. Nature 2008; 453:1051-7.
7. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 Cells. Annu Rev Immunol 2009; 27:485-517.
8. Acosta-Rodriguez EV, Napolitani G, Lanzavecchia A, Sallusto F. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol 2007; 8:942-9.
9. Bettelli E, Carrier Y, Gao W etal. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006; 441:235-8.
10. Yang L, Anderson DE, Baecher-Allan C etal. IL-21 and TGF-beta are required for differentiation of human T(H)17 cells. Nature 2008; 454:350-2.
11. Stritesky GL, Yeh N, Kaplan MH. IL-23 promotes maintenance but not commitment to the Th17 lineage. J Immunol 2008; 181:5948-55.
12. Furuzawa-Carballeda J, Vargas-Rojas MI, Cabral AR. Autoimmune inflammation from the Th17 perspective. Autoimmun Rev 2007; 6:169-75.
13. Fouser LA, Wright JF, Dunussi-Joannopoulos K, Collins M. Th17 cytokines and their emerging roles in inflammation and autoimmunity. Immunol Rev 2008; 226:87-102.
14. Doe C, Bafadhel M, Siddiqui S etal. Expression of the T helper 17-associated cytokines IL-17A and IL-17F in asthma and COPD. Chest 2010; 138:1140-7.
15. Khader SA, Bell GK, Pearl JE etal. IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat Immunol 2007; 8:369-77.
16. Umemura M, Yahagi A, Hamada S etal. IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guérin infection. J Immunol 2007; 178:3786-96.
17. Khader SA, Pearl JE, Sakamoto K etal. IL-23 compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-gamma responses if IL-12p70 is available. J Immunol 2005; 175:788-95.
18. Liang SC, Tan XY, Luxenberg DP etal. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med 2006; 203:2271-9.
19. Aggarwal S, Xie MH, Maruoka M, Foster J, Gurney AL. Acinar cells of the pancreas are a target of interleukin-22. J Interferon Cytokine Res 2001; 21:1047-53.
20. Chang H, Hanawa H, Liu H etal. Hydrodynamic-based delivery of an interleukin-22-Ig fusion gene ameliorates experimental autoimmune myocarditis in rats. J Immunol 2006; 177:3635-43.
21. Sugimoto K, Ogawa A, Mizoguchi E etal. IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis. J Clin Invest 2008; 118:534-44.
22. Zenewicz LA, Yancopoulos GD, Valenzuela DM, Murphy AJ, Karow M, Flavell RA. Interleukin-22 but not interleukin-17 provides protection to hepatocytes during acute liver inflammation. Immunity 2007; 27:647-59.
23. Scriba TJ, Kalsdorf B, Abrahams DA etal. Distinct, specific IL-17- and IL-22-producing CD4+ T cell subsets contribute to the human anti-mycobacterial immune response. J Immunol 2008; 180:1962-70.
24. Weaver CT, Hatton RD, Mangan PR, Harrington LE. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol 2007; 25:821-52.
25. Antony VB, Sahn SA, Antony AC, Repine JE. Bacillus Calmette-Guérin-stimulated neutrophils release chemotaxins for monocytes in rabbit pleural spaces and in vitro. J Clin Invest 1985; 76:1514-21.
26. Seiler P, Aichele P, Bandermann S etal. Early granuloma formation after aerosol Mycobacterium tuberculosis infection is regulated by neutrophils via CXCR3-signaling chemokines. Eur J Immunol 2003; 33:2676-86.
27. Petrofsky M, Bermudez LE. Neutrophils from Mycobacterium avium-infected mice produce TNF-alpha, IL-12, and IL-1 beta and have a putative role in early host response. Clin Immunol 1999; 91:354-8.
28. Martineau AR, Newton SM, Wilkinson KA etal. Neutrophil-mediated innate immune resistance to mycobacteria. J Clin Invest 2007; 117:1988-94.
29. Rhoades ER, Frank AA, Orme IM. Progression of chronic pulmonary tuberculosis in mice aerogenically infected with virulent Mycobacterium tuberculosis. Tuber Lung Dis 1997; 78:57-66.
30. Larousserie F, Pflanz S, Coulomb-L'Hermine A, Brousse N, Kastelein R, Devergne O. Expression of IL-27 in human Th1-associated granulomatous diseases. J Pathol 2004; 202:164-71.
31. Kreymborg K, Etzensperger R, Dumoutier L etal. IL-22 is expressed by Th17 cells in an IL-23-dependent fashion, but not required for the development of autoimmune encephalomyelitis. J Immunol 2007; 179:8098-104.
32. Dlugovitzky D, Torres-Morales A, Rateni L etal. Circulating profile of Th1 and Th2 cytokines in tuberculosis patients with different degrees of pulmonary involvement. FEMS Immunol Med Microbiol 1997; 18:203-7.
33. Verbon A, Juffermans N, Van Deventer SJ, Speelman P, Van Deutekom H, Van Der Poll T. Serum concentrations of cytokines in patients with active tuberculosis (TB) and after treatment. Clin Exp Immunol 1999; 115:110-13.
34. Qiu L, Huang D, Chen CY etal. Severe tuberculosis induces unbalanced up-regulation of gene networks and overexpression of IL-22, MIP-1alpha, CCL27, IP-10, CCR4, CCR5, CXCR3, PD1, PDL2, IL-3, IFN-beta, TIM1, and TLR2 but low antigen-specific cellular responses. J Infect Dis 2008; 198:1514-19.
35. Khader SA, Cooper AM. IL-23 and IL-17 in tuberculosis. Cytokine 2008; 41:79-83.
36. Stern JN, Keskin DB, Romero V etal. Molecular signatures distinguishing active from latent tuberculosis in peripheral blood mononuclear cells, after in vitro antigenic stimulation with purified protein derivative of tuberculin (PPD) or Candida: a preliminary report. Immunol Res 2009; 45:1-12.
37. Dokter WH, Esselink MT, Sierdsema SJ, Halie MR, Vellenga E. Transcriptional and posttranscriptional regulation of the interleukin-4 and interleukin-3 genes in human T cells. Blood 1993; 81:35-40.
38. Schroder AK, Uciechowski P, Fleischer D, Rink L. Crosslinking of CD66B on peripheral blood neutrophils mediates the release of interleukin-8 from intracellular storage. Hum Immunol 2006; 67:676-82.
39. Matzer SP, Baumann T, Lukacs NW, Rollinghoff M, Beuscher HU. Constitutive expression of macrophage-inflammatory protein 2 (MIP-2) mRNA in bone marrow gives rise to peripheral neutrophils with preformed MIP-2 protein. J Immunol 2001; 167:4635-43.
40. Spencer LA, Szela CT, Perez SA etal. Human eosinophils constitutively express multiple Th1, Th2, and immunoregulatory cytokines that are secreted rapidly and differentially. J Leukoc Biol 2009; 85:117-23.
41. Tapper H. The secretion of preformed granules by macrophages and neutrophils. J Leukoc Biol 1996; 59:613-22.
42. Aujla SJ, Chan YR, Zheng M etal. IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat Med 2008; 14:275-81.
43. Munoz M, Heimesaat MM, Danker K etal. Interleukin (IL)-23 mediates Toxoplasma gondii-induced immunopathology in the gut via matrix metalloproteinase-2 and IL-22 but independent of IL-17. J Exp Med 2009; 206:3047-59.
44. Zheng Y, Valdez PA, Danilenko DM etal. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med 2008; 14:282-9.
45. Zheng Y, Danilenko DM, Valdez P etal. Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 2007; 445:648-51.
46. Aspinall R. Age-related changes in the function of T cells. Microsc Res Tech 2003; 62:508-13.
47. Friedland JS, Remick DG, Shattock R, Griffin GE. Secretion of interleukin-8 following phagocytosis of Mycobacterium tuberculosis by human monocyte cell lines. Eur J Immunol 1992; 22:1373-8.
48. Wickremasinghe MI, Thomas LH, Friedland JS. Pulmonary epithelial cells are a source of IL-8 in the response to Mycobacterium tuberculosis: essential role of IL-1 from infected monocytes in a NF-kappa B-dependent network. J Immunol 1999; 163:3936-47.
49. Baggiolini M, Loetscher P, Moser B. Interleukin-8 and the chemokine family. Int J Immunopharmacol 1995; 17:103-8.
50. Mills KH. Induction, function and regulation of IL-17-producing T cells. Eur J Immunol 2008; 38:2636-49.
51. Lotze MT, Matory YL, Ettinghausen SE etal. In vivo administration of purified human interleukin 2. II. Half life, immunologic effects, and expansion of peripheral lymphoid cells in vivo with recombinant IL 2. J Immunol 1985; 135:2865-75.
52. Marchant A, Deviere J, Byl B, De GD, Vincent JL, Goldman M. Interleukin-10 production during septicaemia. Lancet 1994; 343:707-8.
53. Park HD, Guinn KM, Harrell MI etal. Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis. Mol Microbiol 2003; 48:833-43.
54. Schnappinger D, Ehrt S, Voskuil MI etal. Transcriptional adaptation of mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 2003; 198:693-704.
55. Sherman DR, Voskuil M, Schnappinger D, Liao R, Harrell MI, Schoolnik GK. Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding alpha-crystallin. Proc Natl Acad Sci USA 2001; 98:7534-9.
56. Voskuil MI, Schnappinger D, Visconti KC etal. Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J Exp Med 2003; 198:705-13.
57. Wayne LG, Hayes LG. An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect Immun 1996; 64:2062-9.
58. Wayne LG, Sohaskey CD. Nonreplicating persistence of Mycobacterium tuberculosis. Annu Rev Microbiol 2001; 55:139-63.
59. Rustad TR, Harrell MI, Liao R, Sherman DR. The enduring hypoxic response of Mycobacterium tuberculosis. PLoS ONE 2008; 3:e1502.
60. Launois P, DeLeys R, Niang MN etal. T-cell-epitope mapping of the major secreted mycobacterial antigen Ag85A in tuberculosis and leprosy. Infect Immun 1994; 62:3679-87.
61. Ordway DJ, Costa L, Martins M etal. Increased interleukin-4 production by CD8 and gammadelta T cells in health-care workers is associated with the subsequent development of active tuberculosis. J Infect Dis 2004; 190:756-66.
62. Wassie L, Demissie A, Aseffa A etal. Ex vivo cytokine mRNA levels correlate with changing clinical status of ethiopian TB patients and their contacts over time. PLoS ONE 2008; 3:e1522.
63. Shabaana AK, Kulangara K, Semac I etal. Mycobacterial lipoarabinomannans modulate cytokine production in human T helper cells by interfering with raft/microdomain signalling. Cell Mol Life Sci 2005; 62:179-87.
64. Morris KR, Lutz RD, Bai X etal. Suppression of IFNgamma+mycobacterial lipoarabinomannan-induced NO by IL-4 is due to decreased IRF-1 expression. Tuberculosis (Edinb) 2009; 89:294-303.
65. Sinsimer D, Huet G, Manca C etal. The phenolic glycolipid of Mycobacterium tuberculosis differentially modulates the early host cytokine response but does not in itself confer hypervirulence. Infect Immun 2008; 76:3027-36.