Deficient and dysfunctional regulatory T cells in the lungs of chronic beryllium disease subjects

American Journal of Respiratory and Critical Care Medicine

Volumn 181, Issue 11, 2010, Pages 1241-1249

  Mack, Douglas G ^a   Lanham, Allison M ^a   Falta, Michael T ^a   Palmer, Brent E ^a   Maier, Lisa A ^a,b   Fontenot, Andrew P ^a,c  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b DEPARTMENT OF MEDICINE   (United States)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

Fibrosis; Granuloma; Human; Inflammation

Indexed keywords

BERYLLIUM; CD27 ANTIGEN; CD4 ANTIGEN; INTERLEUKIN 2 RECEPTOR ALPHA; TRANSCRIPTION FACTOR FOXP3; CD3 ANTIGEN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; IL2RA PROTEIN, HUMAN; MONOCLONAL ANTIBODY;

ADAPTIVE IMMUNITY; ADULT; AGED; ARTICLE; BERYLLIOSIS; CD4+ T LYMPHOCYTE; CHRONIC DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; EFFECTOR CELL; FEMALE; HUMAN; HUMAN CELL; IMMUNOMODULATION; INFLAMMATION; LUNG LAVAGE; LYMPHOCYTE PROLIFERATION; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; CASE CONTROL STUDY; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECT; HOSPITALIZATION; IMMUNOLOGY; LUNG; METABOLISM; MIDDLE AGED;

ADULT; AGED; ANTIBODIES, MONOCLONAL; ANTIGENS, CD3; BERYLLIOSIS; BRONCHOALVEOLAR LAVAGE FLUID; CASE-CONTROL STUDIES; CELL PROLIFERATION; CHRONIC DISEASE; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LUNG; MALE; MIDDLE AGED; SEVERITY OF ILLNESS INDEX; T-LYMPHOCYTES, REGULATORY;

EID: 77954693829     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201001-0025OC     Document Type: Article

References (53)

1. Newman LS, Maier LA. Beryllium disease. In: Schwarz MI, King TE Jr, editors. Interstitial lung disease, 3rd ed. Hamilton, Ontario: B.C. Decker; 2003. pp. 435-451.
2. Kreiss K, Wasserman S, Mroz MM, Newman LS. Beryllium disease screening in the ceramics industry: blood test performance and exposure-disease relations. J Occup Med 1993;35:267-274.
3. Kreiss K, Mroz MM, Zhen B, Martyny JW, Newman LS. Epidemiology of beryllium sensitization and disease in nuclear workers. Am Rev Respir Dis 1993;148:985-991.
4. 3. Am J Ind Med 1996;30:16-25.
5. Richeldi L, Sorrentino R, Saltini C. HLA-DPB1 glutamate 69: a genetic marker of beryllium disease. Science 1993;262:242-244.
6. Richeldi L, Kreiss K, Mroz MM, Zhen B, Tartoni P, Saltini C. Interaction of genetic and exposure factors in the prevalence of berylliosis. Am J Ind Med 1997;32:337-340.
7. Wang Z, White PS, Petrovic M, Tatum OL, Newman LS, Maier LA, Marrone BL. Differential susceptibilities to chronic beryllium disease contributed by different Glu69 HLA-DPB1 and -DPA1 alleles. J Immunol 1999;163:1647-1653.
8. Rossman MD, Stubbs J, Lee CW, Argyris E, Magira E, Monos D. Human leukocyte antigen Class II amino acid epitopes: susceptibility and progression markers for beryllium hypersensitivity. Am J Respir Crit Care Med 2002;165:788-794. (Pubitemid 34229648)
9. Maier LA, McGrath DS, Sato H, Lympany P, Welsh K, Du Bois R, Silveira L, Fontenot AP, Sawyer RT, Wilcox E, et al. Influence of MHC class II in susceptibility to beryllium sensitization and chronic beryllium disease. J Immunol 2003;171:6910-6918.
10. Fontenot AP, Maier LA. Genetic susceptibility and immune-mediated destruction in beryllium-induced disease. Trends Immunol 2005;26:543-549.
11. Newman LS, Bobka C, Schumacher B, Daniloff E, Zhen B, Mroz M, King TE Jr. Compartmentalized immune response reflects clinical severity of beryllium disease. Am J Respir Crit Care Med 1994;150:135-142.
12. Rossman MD, Kern JA, Elias JA, Cullen MR, Epstein PE, Preuss OP, Markham TN, Daniele RP. Proliferative response of bronchoalveolar lymphocytes to beryllium. Ann Intern Med 1988;108:687-693.
13. Saltini C, Winestock K, Kirby M, Pinkston P, Crystal RG. Maintenance of alveolitis in patients with chronic beryllium disease by beryllium-specific helper T cells. N Engl J Med 1989;320:1103-1109.
14. Fontenot AP, Falta MT, Freed BM, Newman LS, Kotzin BL. Identification of pathogenic T cells in patients with beryllium-induced lung disease. J Immunol 1999;163:1019-1026.
15. + T cells in patients with chronic beryllium disease. J Clin Invest 2002;110:1473-1482.
16. Tinkle SS, Kittle LA, Schumacher BA, Newman LS. Beryllium induces IL-2 and IFN-g in berylliosis. J Immunol 1997;158:518-526.
17. Fontenot AP, Kotzin BL, Comment CE, Newman LS. Expansions of T-cell subsets expressing particular T cell receptor variable regions in chronic beryllium disease. Am J Respir Cell Mol Biol 1998;18:581-589.
18. Mroz MM, Maier LA, Strand M, Silviera L, Newman LS. Beryllium lymphocyte proliferation test surveillance identifies clinically significant beryllium disease. Am J Ind Med 2009;52:762-773.
19. Williams WL. UK beryllium registry: mortality and autopsy study. Environ Health Perspect 1996;104:949S-951S.
20. Sakaguchi S. Regulatory T cells: key controllers of immunologic self-tolerance. Cell 2000;101:455-458.
21. Shevach EM. Regulatory T cells in autoimmmunity. Annu Rev Immunol 2000;18:423-449.
22. Sakaguchi S, Fukuma K, Kuribayashi K, Masuda T. Organ-specific autoimmune diseases induced in mice by elimination of T cell subset. I. Evidence for the active participation of T cells in natural self-tolerance; deficit of a T cell subset as a possible cause of autoimmune disease. J Exp Med 1985;161:72-87.
23. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alphachains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995;155:1151-1164.
24. Thornton AM, Shevach EM. CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med 1998;188:287-296.
25. Baecher-Allan C, Brown JA, Freeman GJ, Hafler DA. CD4+CD25 high regulatory cells in human peripheral blood. J Immunol 2001;167:1245-1253.
26. Brunkow ME, Jeffery EW, Hjerrild KA, Paeper B, Clark LB, Yasayko SA, Wilkinson JE, Galas D, Ziegler SF, Ramsdell F. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat Genet 2001;27:68-73.
27. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 2003;4:330-336.
28. Marie JC, Letterio JJ, Gavin M, Rudensky AY. TGF-beta1 maintains suppressor function and Foxp3 expression in CD4+CD25+ regulatory T cells. J Exp Med 2005;201:1061-1067.
29. Newman LS, Kreiss K, King TE Jr, Seay S, Campbell PA. Pathologic and immunologic alterations in early stages of beryllium disease: reexamination of disease definition and natural history. Am Rev Respir Dis 1989;139:1479-1486. (Pubitemid 19155510)
30. Newman LS. Significance of the blood beryllium lymphocyte proliferation test. Environ Health Perspect 1996;104:953-956.
31. Mroz MM, Kreiss K, Lezotte DC, Campbell PA, Newman LS. Reexamination of the blood lymphocyte transformation test in the diagnosis of chronic beryllium disease. J Allergy Clin Immunol 1991;88:54-60.
32. + T cells in chronic beryllium disease. J Immunol 2008;180:2704-2712.
33. Mack DG, Lanham AM, Palmer BE, Maier LA, Fontenot AP. CD27 expression on CD4+ T cells differentiates effector from regulatory T cell subsets in the lung. J Immunol 2009;182:7317-7324.
34. Balandina A, Lecart S, Dartevelle P, Saoudi A, Berrih-Aknin S. Functional defect of regulatory CD4+CD25+ T cells in the thymus of patients with autoimmune myasthenia gravis. Blood 2005;105:735-741. (Pubitemid 40070760)
35. Huan J, Culbertson N, Spencer L, Bartholomew R, Burrows GG, Chou YK, Bourdette D, Ziegler SF, Offner H, Vandenbark AA. Decreased FOXP3 levels in multiple sclerosis patients. J Neurosci Res 2005;81:45-52. (Pubitemid 41139109)
36. Miura Y, Thoburn CJ, Bright EC, Phelps ML, Shin T, Matsui EC, Matsui WH, Arai S, Fuchs EJ, Vogelsang GB, et al. Association of Foxp3 regulatory gene expression with graft-versus-host disease. Blood 2004;104:2187-2193.
37. Wan YY, Flavell RA. Regulatory T-cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature 2007;445:766-770.
38. Jones-Williams W, Kelland D. New aid for diagnosing chronic beryllium disease (CBD): laser ion mass analysis (LIMA). J Clin Pathol 1986;39:900-901.
39. Jones-Williams W, Wallach ER. Laser microprobe mass spectrometry (LAMMS) analysis of beryllium, sarcoidosis, and other granulomatous diseases. Sarcoidosis 1989;6:111-117.
40. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003;299:1057-1061.
41. Lal G, Bromberg JS. Epigenetic mechanisms of regulation of Foxp3 expression. Blood 2009;114:3727-3735.
42. Idali F, Wahlstrom J, Muller-Suur C, Eklund A, Grunewald J. Analysis of regulatory T cell associated forkhead box P3 expression in the lungs of patients with sarcoidosis. Clin Exp Immunol 2008;152:127-137.
43. Miyara M, Amoura Z, Parizot C, Badoual C, Dorgham K, Trad S, Kambouchner M, Valeyre D, Chapelon-Abric C, Debre P, et al. The immune paradox of sarcoidosis and regulatory T cells. J Exp Med 2006;203:359-370.
44. Planck A, Katchar K, Eklund A, Gripenback S, Grunewald J. T-lymphocyte activity in HLA-DR17 positive patients with active and clinically recovered sarcoidosis. Sarcoidosis Vasc Diffuse Lung Dis 2003;20:110-117. (Pubitemid 36841691)
45. Taflin C, Miyara M, Nochy D, Valeyre D, Naccache JM, Altare F, Salek-Peyron P, Badoual C, Bruneval P, Haroche J, et al. FoxP3+ regulatory T cells suppress early stages of granuloma formation but have little impact on sarcoidosis lesions. Am J Pathol 2009;174:497-508.
46. Kotsianidis I, Nakou E, Bouchliou I, Tzouvelekis A, Spanoudakis E, Steiropoulos P, Sotiriou I, Aidinis V, Margaritis D, Tsatalas C, et al. Global impairment of CD4+CD25+FOXP3+ regulatory T cells in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2009;179:1121-1130.
47. O'Garra A. Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity 1998;8:275-283.
48. Salez F, Gosset P, Copin MC, Lamblin Degros C, Tonnel AB, Wallaert B. Transforming growth factor-beta1 in sarcoidosis. Eur Respir J 1998;12:913-919.
49. Cambien F, Ricard S, Troesch A, Mallet C, Generenaz L, Evans A, Arveiler D, Luc G, Ruidavets JB, Poirier O. Polymorphisms of the transforming growth factor-beta 1 gene in relation to myocardial infarction and blood pressure. The Etude Cas-Temoin de l'Infarctus du Myocarde (ECTIM) Study. Hypertension 1996;28:881-887.
50. Jonth AC, Silveira L, Fingerlin TE, Sato H, Luby JC, Welsh KI, Rose CS, Newman LS, du Bois RM, Maier LA. TGF-beta 1 variants in chronic beryllium disease and sarcoidosis. J Immunol 2007;179:4255-4262.
51. Grainger DJ, Heathcote K, Chiano M, Snieder H, Kemp PR, Metcalfe JC, Carter ND, Spector TD. Genetic control of the circulating concentration of transforming growth factor type beta1. Hum Mol Genet 1999;8:93-97.
52. Silverman ES, Palmer LJ, Subramaniam V, Hallock A, Mathew S, Vallone J, Faffe DS, Shikanai T, Raby BA, Weiss ST, et al. Transforming growth factor-beta1 promoter polymorphism C-509T is associated with asthma. Am J Respir Crit Care Med 2004;169:214-219.
53. Kruit A, Grutters JC, Ruven HJ, van Moorsel CH, Weiskirchen R, Mengsteab S, van den Bosch JM. Transforming growth factor-beta gene polymorphisms in sarcoidosis patients with and without fibrosis. Chest 2006;129:1584-1591.