Mycobacterial antigen-induced T helper type 1 (Th1) and Th2 reactivity of peripheral blood mononuclear cells from diabetic and non-diabetic tuberculosis patients and Mycobacterium bovis bacilli Calmette-Guérin (BCG)-vaccinated healthy subjects

Clinical and Experimental Immunology

Volumn 158, Issue 1, 2009, Pages 64-73

  Al Attiyah, R J ^a   Mustafa, A S ^a  

^a KUWAIT UNIVERSITY   (Kuwait)

Author keywords

Diabetes; Peripheral blood mononuclear cells; Th1 and Th2 cytokines; Tuberculosis

Indexed keywords

BCG VACCINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; LYMPHOTOXIN; MYCOBACTERIUM ANTIGEN;

ADULT; ARTICLE; CELL PROLIFERATION; CELL SECRETION; CELLULAR IMMUNITY; CLINICAL ARTICLE; CLINICAL ASSESSMENT; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE PREDISPOSITION; FEMALE; HUMAN; HUMAN CELL; LUNG TUBERCULOSIS; MALE; MYCOBACTERIUM TUBERCULOSIS; NON INSULIN DEPENDENT DIABETES MELLITUS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; RESPIRATORY DISTRESS SYNDROME; TH1 CELL; TH2 CELL;

ADULT; ANTIGENS, BACTERIAL; BCG VACCINE; BIOLOGICAL MARKERS; CELL PROLIFERATION; CELLS, CULTURED; DIABETES MELLITUS; DISEASE SUSCEPTIBILITY; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNIZATION; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-2; LYMPHOTOXIN-ALPHA; MALE; MIDDLE AGED; MYCOBACTERIUM BOVIS; T-LYMPHOCYTES; TH1 CELLS; TH2 CELLS; TUBERCULOSIS, PULMONARY; YOUNG ADULT;

EID: 69949122830     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2009.04000.x     Document Type: Article

References (55)

1. Dye C. Global epidemiology of tuberculosis. Lancet 2006 36 : 938 940.
2. Boutayeb A. The double burden of communicable and non-communicable diseases in developing countries. Trans R Soc Trop Med Hyg 2006 100 : 191 199.
3. Broxmeyer L. Diabetes mellitus, tuberculosis and the mycobacteria: two millennia of enigma. Med Hypotheses 2005 65 : 433 439.
4. Tsukaguchi K,Okamura H,Matsuzawa K et al. Longitudinal assessment of IFN-gamma production in patients with pulmonary tuberculosis complicated with diabetes mellitus. Kekkaku 2002; 77:409-13 [in Japanese].
5. Alisjahbana B, van Crevel R, Sahiratmadja E et al. Diabetes mellitus is strongly associated with tuberculosis in Indonesia. Int J Tuberc Lung Dis 2006; 10:696-700.
6. Dyck RF, Klomp H, Marciniuk DD et al. The relationship between diabetes and tuberculosis in Saskatchewan: comparison of registered Indians and other Saskatchewan people. Can J Public Health 2007 98 : 55 9.
7. Swai AB, McLarty DG, Mugusi F. Tuberculosis in diabetic patients in Tanzania. Trop Doct 1990 20 : 147 150.
8. Mustafa AS. Recombinant and synthetic peptides to identify Mycobacterium tuberculosis antigens and epitopes of diagnostic and vaccine relevance. Tuberculosis (Edinb) 2005 85 : 367 376.
9. Karachunskii MA, Gerget Via, Iakovleva OB. Specific features of cellular immunity of pulmonary tuberculosis in patients with diabetes mellitus. Probl Tuberk 1997; 6:59-60 [in Russian].
10. Saiki O, Negoro S, Tsuyuguchi I, Yamamura Y. Depressed immunological defence mechanisms in mice with experimentally induced diabetes. Infect Immun 1980; 28:127-31.
11. Al-Attiyah R, Madi N, El-Shamy AS, Wiker H, Andersen P, Mustafa AS. Cytokine profiles in tuberculosis patients and healthy subjects in response to complex and single antigens of Mycobacterium tuberculosis. FEMS Immunol Med Microbiol 2006 47 : 254 261.
12. Bai X, Wilson SE, Chmura K, Feldman NE, Chan ED. Morphometric analysis of Th(1) and Th(2) cytokine expression in human pulmonary tuberculosis. Tuberculosis 2004 84 : 375 385.
13. Flynn J. Immunology of tuberculosis and implications in vaccine development. Tuberculosis 2004 4 : 93 101.
14. Turner J, Gonzalez-Juarrero M, Ellis DL et al. In vivo IL-10 production reactivates chronic pulmonary tuberculosis in C57BL/6 mice. J Immunol 2002 169 : 6343 6351.
15. Ottenhoff TH, Verreck FA, Hoeve MA, van de Vosse E. Control of human host immunity to mycobacteria. Tuberculosis (Edinb) 2005 85 : 53 64.
16. Grahmann PR, Braun RK. A new protocol for multiple inhalation of IFN-gamma successfully treats MDR-TB: a case study. Int J Tuberc Lung Dis 2008 12 : 636 644.
17. Arend SM, Andersen P, van Meijgaarden KE et al. Detection of active tuberculosis infection by T cell responses to early-secreted antigenic target 6-kDa protein and culture filtrate protein 10. J Infect Dis 2001 181 : 1850 1854.
18. Ferrara G, Losi M, D'Amico R et al. Use in routine clinical practice of two commercial blood tests for diagnosis of infection with Mycobacterium tuberculosis: a prospective study. Lancet 2006 367 : 1328 1334.
19. Liebeschuetz S, Bamber S, Ewer K, Deeks J, Pathan AA, Lalvani A. Diagnosis of tuberculosis in South African children with a T-cell-based assay: a prospective cohort study. Lancet 2004 364 : 2196 2203.
20. Roach DR, Briscoe H, Saunders B et al. Secreted lymphotoxin-alpha is essential for the control of an intracellular bacterial infection. J Exp Med 2001 193 : 239 246.
21. Weir RE, Black GF, Dockrell HM et al. Mycobacterial purified protein derivatives stimulate innate immunity: Malawians show enhanced tumor necrosis factor alpha, interleukin-1beta (IL-1beta), and IL-10 responses compared to those of adolescents in the United Kingdom. Infect Immun 2004 72 : 1807 1811.
22. Rook GAW. Th2 cytokines in susceptibility to tuberculosis. Curr Mol Med 2007 7 : 327 337.
23. Yamashiro S, Kawakami K, Uezu K et al. Lower expression of Th1-related cytokines and inducible nitric oxide synthase in mice with streptozotocin- induced diabetes mellitus infected with Mycobacterium tuberculosis. Clin Exp Immunol 2005 139 : 57 64.
24. Stalenhoef JE, Alisjahbana B, Nelwan EJ et al. The role of interferon-gamma in the increased tuberculosis risk in type 2 diabetes mellitus. Eur J Clin Microbiol Infect Dis 2008 27 : 97 103.
25. Restrepo BI, Fisher-Hoch SP, Pino PA et al. Tuberculosis in poorly controlled type 2 diabetes: altered cytokine expression in peripheral white blood cells. Clin Infect Dis 2008 47 : 634 641.
26. Amoudy HA, Al-Turab MB, Mustafa AS. Identification of transcriptionally active open reading frames within the RD1 genomic segment of Mycobacterium tuberculosis. Med Princ Pract 2006 15 : 137 144.
27. Behr MA, Wilson MA, Gill WP et al. Comparative genomics of BCG vaccines by whole-genome DNA microarray. Science 1999 284 : 1520 1523.
28. Al-Attiyah R, Shaban FA, Wiker HG, Oftung F, Mustafa AS. Synthetic peptides identify promiscuous human Th1 cell epitopes of the secreted mycobacterial antigen MPB70. Infect Immun 2003 71 : 1953 1960.
29. Mustafa AS, Shaban FA. ProPred analysis and experimental evaluation of promiscuous T-cell epitopes of three major secreted antigens of Mycobacterium tuberculosis. Tuberculosis (Edinb) 2006 86 : 115 124.
30. Hanif SNM, El-Shammy AM, Al-Attiyah R, Mustafa AS. Whole blood assays to identify Th1 cell antigens and peptides encoded by Mycobacterium tuberculosis-specific RD1 genes. Med Princ Pract 2008 17 : 244 249.
31. Al-Attiyah R, Mustafa AS. Characterization of human cellular immune responses to novel Mycobacterium tuberculosis antigens encoded by genomic regions absent in Mycobacterium bovis BCG. Infect Immun 2008 76 : 4190 4198.
32. Mustafa AS, Al-Attiyah R, Hanif SNM, Shaban FA. Efficient testing of pools of large numbers of peptides covering 12 open reading frames of M. tuberculosis RD1 and identification of major antigens and immunodominant peptides recognized by humanTh1 cells. Clin Vaccine Immunol 2008 15 : 916 924.
33. Mustafa AS, El-Shamy AM, Madi NM, Amoudy HA, Al-Attiyah R. Cell mediated immune responses to complex and single mycobacterial antigens in tuberculosis patients with diabetes. Med Princ Pract 2008 17 : 325 330.
34. Leyten EM, Arend SM, Prins C, Cobelens FG, Ottenhoff TH, van Dissel JT. Discrepancy between Mycobacterium tuberculosis-specific gamma interferon release assays using short and prolonged in vitro incubation. Clin Vaccine Immunol 2007 14 : 880 885.
35. Okkels LM, Brock I, Follmann F et al. PPE protein (Rv3873) from DNA segment RD1 of Mycobacterium tuberculosis: strong recognition of both specific T-cell epitopes and epitopes conserved within the PPE family. Infect Immun 2003 71 : 6116 6123.
36. Lalvani A, Nagvenkar P, Udwadia Z et al. Enumeration of T cells specific for RD1-encoded antigens suggests a high prevalence of latent Mycobacterium tuberculosis infection in healthy urban Indians. J Infect Dis 2001 183 : 469 477.
37. Cardoso FL, Antas PR, Milagres AS et al. T-cell responses to the Mycobacterium tuberculosis-specific antigen ESAT-6 in Brazilian tuberculosis patients. Infect Immun 2002 70 : 6707 6714.
38. Bhattacharyya S, Singla R, Dey AB, Prasad HK. Dichotomy of cytokine profiles in patients and high-risk healthy subjects exposed to tuberculosis. Infect Immun 1999 67 : 5597 5603.
39. Walker D, Jason J, Wallace K et al. Spontaneous cytokine production and its effect on induced production. Clin Diagn Lab Immunol 2002 9 : 1049 1056.
40. Stadler BM, Dougherty SF, Farrar JJ, Oppenheim JJ. Relationship of cell cycle to recovery of IL-2 activity from human mononuclear cells, human and mouse T cell lines. J Immunol 1981 127 : 1936 1940.
41. Morosini M, Meloni F, Uccelli M, Marone Bianco A, Solari N, Fietta AM. Ex vivo evaluation of PPD-specific IFN-gamma or IL-5 secreting cells in the peripheral blood and lungs of patients with tuberculosis. Int J Tuberc Lung Dis 2005 9 : 753 759.
42. van Crevel R, Ottenhoff THM, van der Meer JWM. Innate immunity to Mycobacterium tuberculosis. Clin Microbiol Rev 2002 15 : 294 309.
43. Murray PJ, Wang L, Onufryk C, Tepper RI, Young RA. T cell-derived IL-10 antagonizes macrophage function in mycobacterial infection. J Immunol 1997 158 : 315 321.
44. Katsikis PD, Cohen SB, Londei M, Feldmann M. Are CD4+ Th1 cells pro-inflammatory or anti-inflammatory? The ratio of IL-10 to IFN-gamma or IL-2 determines their function. Int Immunol 1995 7 : 1287 1294.
45. Jamil B, Shahid F, Hasa Z et al. Interferon γ/IL-10 ratio defines the disease severity in pulmonary and extra pulmonary tuberculosis. Tuberculosis 2007 87 : 279 287.
46. Sahiratmadja E, Alisjahbana B, de Boer T et al. Dynamic changes in pro- and anti-inflammatory cytokine profiles and gamma interferon receptor signaling integrity correlate with tuberculosis disease activity and response to curative treatment. Infect Immun 2007 75 : 820 829.
47. Mutis T, Cornelisse YE, Ottenhoff TH. Mycobacteria induce CD4+ T cells that are cytotoxic and display Th1-like cytokine secretion profile: heterogeneity in cytotoxic activity and cytokine secretion levels. Eur J Immunol 1993 23 : 2189 2195.
48. Hussey GD, Watkins ML, Goddard EA et al. Neonatal mycobacterial specific cytotoxic T-lymphocyte and cytokine profiles in response to distinct BCG vaccination strategies. Immunology 2002 105 : 314 324.
49. Seah GT, Scott GM, Rook GA. Type 2 cytokine gene activation and its relationship to extent of disease in patients with tuberculosis. J Infect Dis 2000 181 : 385 389.
50. Lienhardt C, Azzurri A, Amedei A et al. Active tuberculosis in Africa is associated with reduced Th1 and increased Th2 activity in vivo. Eur J Immunol 2002 32 : 1605 1613.
51. Baumann S, Nasser Eddine A, Kaufmann SH. Progress in tuberculosis vaccine development. Curr Opin Immunol 2006 18 : 438 448.
52. Chen X, Zhou B, Li M et al. CD4(+)CD25(+)FoxP3(+) regulatory T cells suppress Mycobacterium tuberculosis immunity in patients with active disease. Clin Immunol 2007 123 : 50 9.
53. Demissie A, Abebe M, Aseffa A et al. Healthy individuals that control a latent infection with Mycobacterium tuberculosis express high levels of Th1 cytokines and the IL-4 antagonist IL-4delta2. J Immunol 2004 172 : 6938 6943.
54. Dheda K, Chang JS, Breen RA et al. In vivo and in vitro studies of a novel cytokine, interleukin 4delta2, in pulmonary tuberculosis. Am J Respir Crit Care Med 2005 172 : 501 508.
55. Wassie L, Demissie A, Aseffa A et al. Ex vivo cytokine mRNA levels correlate with changing clinical status of Ethiopian TB patients and their contacts over time. PLoS ONE 2008 3 : e1522.