Clinics in Dermatology
Volume 25, Issue 3 , Pages 250-258 , May 2007

Immunopathogenesis of sarcoidosis

References 

  1. Rybicki BA, Walewski JL, Maliarik MJ, Kian H, Iannuzzi MC. The BTNL2 gene and sarcoidosis susceptibility in African Americans and whites. Am J Hum Genet. 2005;77:491–499
  2. Valentonyte R, Hampe J, Huse K, et al. Sarcoidosis is associated with a truncating splice site mutation in BTNL2. Nat Genet. 2005;37:357–364
  3. Song Z, Marzilli L, Greenlee BM, et al. Mycobacterial catalase-peroxidase is a tissue antigen and target of the adaptive immune response in systemic sarcoidosis. J Exp Med. 2005;201:755–767
  4. Grunewald J, Berlin M, Olerup O, Eklund A. Lung T-helper cells expressing T-cell receptor AV2S3 associate with clinical features of pulmonary sarcoidosis. Am J Respir Crit Care Med. 2000;161(3 Pt 1):814–818
  5. Grunewald J, Janson CH, Eklund A, et al. Restricted V alpha 2.3 gene usage by CD4+ T lymphocytes in bronchoalveolar lavage fluid from sarcoidosis patients correlates with HLA-DR3. Eur J Immunol. 1992;22:129–135
  6. Grunewald J, Olerup O, Persson U, Ohrn MB, Wigzell H, Eklund A. T-cell receptor variable region gene usage by CD4+ and CD8+ T cells in bronchoalveolar lavage fluid and peripheral blood of sarcoidosis patients. Proc Natl Acad Sci U S A. 1994;91:4965–4969
  7. Daniele RP, Rowlans DT. Lymphocyte subpopulations in sarcoidosis: correlation with disease activity and duration. Ann Intern Med. 1976;85:593–600
  8. Hunninghake GW, Fulmer JD, Young RC, Gadek JE, Crystal RG. Localization of the immune response in sarcoidosis. Am Rev Respir Dis. 1979;120:49–57
  9. Siltzbach LE, James DG, Neville E, et al. Course and prognosis of sarcoidosis around the world. Am J Med. 1974;57:847–852
  10. James DG. Immunology of sarcoidosis. Lancet. 1966;2:633–635
  11. Bronchoalveolar lavage constituents in healthy individuals, idiopathic pulmonary fibrosis, and selected comparison groups. The BAL Cooperative Group Steering Committee. Am Rev Respir Dis. 1990;141(5 Pt 2):S169–S202
  12. Hunninghake GW, Crystal RG. Pulmonary sarcoidosis: a disorder mediated by excess helper T-lymphocyte activity at sites of disease activity. N Engl J Med. 1981;305:429–434
  13. Winterbauer RH, Lammert J, Selland M, Wu R, Corley D, Springmeyer SC. Bronchoalveolar lavage cell populations in the diagnosis of sarcoidosis. Chest. 1993;104:352–361
  14. Yeager H, Williams MC, Beekman JF, Bayly TC, Beaman BL. Sarcoidosis: analysis of cells obtained by bronchial lavage. Am Rev Respir Dis. 1977;116:951–954
  15. Semenzato G, Agostini C, Trentin L, et al. Evidence of cells bearing interleukin-2 receptor at sites of disease activity in sarcoid patients. Clin Exp Immunol. 1984;57:331–337
  16. Ziegenhagen MW, Benner UK, Zissel G, Zabel P, Schlaak M, Muller-Quernheim J. Sarcoidosis: TNF-alpha release from alveolar macrophages and serum level of sIL-2R are prognostic markers. Am J Respir Crit Care Med. 1997;156:1586–1592
  17. Wahlstrom J, Berlin M, Skold CM, Wigzell H, Eklund A, Grunewald J. Phenotypic analysis of lymphocytes and monocytes/macrophages in peripheral blood and bronchoalveolar lavage fluid from patients with pulmonary sarcoidosis. Thorax. 1999;54:339–346
  18. Pinkston P, Bitterman PB, Crystal RG. Spontaneous release of interleukin-2 by lung T lymphocytes in active pulmonary sarcoidosis. N Engl J Med. 1983;308:793–800
  19. Robinson BW, McLemore TL, Crystal RG. Gamma interferon is spontaneously released by alveolar macrophages and lung T lymphocytes in patients with pulmonary sarcoidosis. J Clin Invest. 1985;75:1488–1495
  20. Wahlstrom J, Katchar K, Wigzell H, Olerup O, Eklund A, Grunewald J. Analysis of intracellular cytokines in CD4+ and CD8+ lung and blood T cells in sarcoidosis. Am J Respir Crit Care Med. 2001;163:115–121
  21. Moller DR. Involvement of T cells and alterations in T cell receptors in sarcoidosis. Semin Respir Infect. 1998;13:174–183
  22. Du R, Bois M, Kirby M, Balbi B, Saltini C, Crystal RG. T-lymphocytes that accumulate in the lung in sarcoidosis have evidence of recent stimulation of the T-cell antigen receptor. Am Rev Respir Dis. 1992;145:1205–1211
  23. Moller DR, Konishi K, Kirby M, Balbi B, Crystal RG. Bias toward use of a specific T cell receptor beta-chain variable region in a subgroup of individuals with sarcoidosis. J Clin Invest. 1988;82:1183–1191
  24. Grunewald J, Wahlstrom J, Berlin M, Wigzell H, Eklund A, Olerup O. Lung restricted T cell receptor AV2S3+ CD4+ T cell expansions in sarcoidosis patients with a shared HLA-DRbeta chain conformation. Thorax. 2002;57:348–352
  25. Idali F, Wiken M, Wahlstrom J, et al. Reduced Th1 response in the lungs of HLA-DRB1*0301 patients with pulmonary sarcoidosis. Eur Respir J. 2006;27:451–459
  26. Zissel G, Baumer I, Fleischer B, Schlaak M, Muller-Quernheim J. TCR V beta families in T cell clones from sarcoid lung parenchyma, BAL, and blood. Am J Respir Crit Care Med. 1997;156:1593–1600
  27. Klein JT, Horn TD, Forman JD, Silver RF, Teirstein AS, Moller DR. Selection of oligoclonal V beta-specific T cells in the intradermal response to Kveim-Siltzbach reagent in individuals with sarcoidosis. J Immunol. 1995;154:1450–1460
  28. Bour-Jordan H, Blueston JA. CD28 function: a balance of costimulatory and regulatory signals. J Clin Immunol. 2002;22:1–7
  29. Pawlik A, Ostanek L, Brzosko I, et al. The expansion of CD4+CD28− T cells in patients with rheumatoid arthritis. Arthritis Res Ther. 2003;5:R210–R213
  30. Lamprecht P, Moosig F, Csernok E, et al. CD28 negative T cells are enriched in granulomatous lesions of the respiratory tract in Wegener's granulomatosis. Thorax. 2001;56:751–757
  31. Tang Q, Henriksen KJ, Boden EK, et al. Cutting edge: CD28 controls peripheral homeostasis of CD4+CD25+ regulatory T cells. J Immunol. 2003;171:3348–3352
  32. Roberts SD, Kohli LL, Wood KL, Wilkes DS, Knox KS. CD4+CD28− T cells are expanded in sarcoidosis. Sarcoidosis Vasc Diffuse Lung Dis. 2005;22:13–19
  33. Godfrey DI, Kronenberg M. Going both ways: immune regulation via CD1d-dependent NKT cells. J Clin Invest. 2004;114:1379–1388
  34. Ho LP, Urban BC, Thickett DR, Davies RJ, McMichael AJ. Deficiency of a subset of T-cells with immunoregulatory properties in sarcoidosis. Lancet. 2005;365:1062–1072
  35. Kobayashi S, Kaneko Y, Seino K, et al. Impaired IFN-gamma production of Valpha24 NKT cells in non-remitting sarcoidosis. Int Immunol. 2004;16:215–222
  36. Mempel M, Flageul B, Suarez F, et al. Comparison of the T cell patterns in leprous and cutaneous sarcoid granulomas. Presence of Valpha24-invariant natural killer T cells in T-cell-reactive leprosy together with a highly biased T cell receptor Valpha repertoire. Am J Pathol. 2000;157:509–523
  37. Miyara M, Amoura Z, Parizot C, et al. The immune paradox of sarcoidosis and regulatory T cells. J Exp Med. 2006;203:359–370
  38. Handa T, Nagai S, Ito I, et al. Cytotoxic T-lymphocyte antigen-4 (CTLA-4) exon 1 polymorphism affects lymphocyte profiles in bronchoalveolar lavage of patients with sarcoidosis. Sarcoidosis Vasc Diffuse Lung Dis. 2003;20:190–196
  39. Hattori N, Niimi T, Sato S, et al. Cytotoxic T-lymphocyte antigen 4 gene polymorphisms in sarcoidosis patients. Sarcoidosis Vasc Diffuse Lung Dis. 2005;22:27–32
  40. Girardi M. Immunosurveillance and immunoregulation by gammadelta T cells. J Invest Dermatol. 2006;126:25–31
  41. Balbi B, Moller DR, Kirby M, Holroyd KJ, Crystal RG. Increased numbers of T lymphocytes with gamma delta-positive antigen receptors in a subgroup of individuals with pulmonary sarcoidosis. J Clin Invest. 1990;85:1353–1361
  42. Wilsher ML, Hallowes M, Birchall NM. Gamma/delta T lymphocytes in the blood of patients with sarcoidosis. Thorax. 1995;50:858–862
  43. Forrester JM, Newman LS, Wang Y, King TE, Kotzin BL. Clonal expansion of lung V delta 1+ T cells in pulmonary sarcoidosis. J Clin Invest. 1993;91:292–300
  44. Tazi A, Fajac I, Soler P, Valeyre D, Battesti JP, Hance AJ. Gamma/delta T-lymphocytes are not increased in number in granulomatous lesions of patients with tuberculosis or sarcoidosis. Am Rev Respir Dis. 1991;144:1373–1375
  45. Wilsher ML, Hallowes M, Birchall NM. Gamma/delta cells in tissue from patients with sarcoidosis. Thorax. 1996;51:1123–1126
  46. Agostini C, Zambello R, Sancetta R, et al. Expression of tumor necrosis factor-receptor superfamily members by lung T lymphocytes in interstitial lung disease. Am J Respir Crit Care Med. 1996;153(4 Pt 1):1359–1367
  47. Herry I, Bonay M, Bouchonnet F, et al. Extensive apoptosis of lung T-lymphocytes maintained in vitro. Am J Respir Cell Mol Biol. 1996;15:339–347
  48. Soler P, Basset F. Morphology and distribution of the cells of a sarcoid granuloma: ultrastructural study of serial section. Ann N Y Acad Sci. 1976;278:147–160
  49. Gee JB, Bodel PT, Zorn SK, Hinman LM, Stevens CA, Matthay RA. Sarcoidosis and mononuclear phagocytes. Lung. 1978;155:243–253
  50. Prior C, Barbee RA, Evans PM, et al. Lavage versus serum measurements of lysozyme, angiotensin converting enzyme and other inflammatory markers in pulmonary sarcoidosis. Eur Respir J. 1990;3:1146–1154
  51. Agostini C, Trentin L, Facco M, et al. Role of IL-15, IL-2, and their receptors in the development of T cell alveolitis in pulmonary sarcoidosis. J Immunol. 1996;157:910–918
  52. Muller-Quernheim J, Pfeifer S, Mannel D, Strausz J, Ferlinz R. Lung-restricted activation of the alveolar macrophage/monocyte system in pulmonary sarcoidosis. Am Rev Respir Dis. 1992;145:187–192
  53. Hunninghake GW. Release of interleukin-1 by alveolar macrophages of patients with active pulmonary sarcoidosis. Am Rev Respir Dis. 1984;129:569–572
  54. Fehrenbach H, Zissel G, Goldmann T, et al. Alveolar macrophages are the main source for tumour necrosis factor-alpha in patients with sarcoidosis. Eur Respir J. 2003;21:421–428
  55. Doty JD, Mazur JE, Judson MA. Treatment of sarcoidosis with infliximab. Chest. 2005;127:1064–1071
  56. Roberts SD, Wilkes DS, Burgett RA, Knox KS. Refractory sarcoidosis responding to infliximab. Chest. 2003;124:2028–2031
  57. Pandey JP, Frederick M. TNF-alpha, IL1-beta, and immunoglobulin (GM and KM) gene polymorphisms in sarcoidosis. Hum Immunol. 2002;63:485–491
  58. Ziegenhagen MW, Muller-Quernheim J. The cytokine network in sarcoidosis and its clinical relevance. J Intern Med. 2003;253:18–30
  59. Moller DR, Forman JD, Liu MC, et al. Enhanced expression of IL-12 associated with Th1 cytokine profiles in active pulmonary sarcoidosis. J Immunol. 1996;156:4952–4960
  60. Shigehara K, Shijubo N, Ohmichi M, et al. IL-12 and IL-18 are increased and stimulate IFN-gamma production in sarcoid lungs. J Immunol. 2001;166:642–649
  61. Capelli A, Di Stefano A, Lusuardi M, Gnemmi I, Donner CF. Increased macrophage inflammatory protein-1alpha and macrophage inflammatory protein-1beta levels in bronchoalveolar lavage fluid of patients affected by different stages of pulmonary sarcoidosis. Am J Respir Crit Care Med. 2002;165:236–241
  62. Gibejova A, Mrazek F, Subrtova D, et al. Expression of macrophage inflammatory protein-3 beta/CCL19 in pulmonary sarcoidosis. Am J Respir Crit Care Med. 2003;167:1695–1703
  63. Xaus J, Besalduch N, Comalada M, et al. High expression of p21 Waf1 in sarcoid granulomas: a putative role for long-lasting inflammation. J Leukoc Biol. 2003;74:295–301
  64. Agostini C, Facco M, Chilosi M, Semenzato G. Alveolar macrophage-T cell interactions during Th1-type sarcoid inflammation. Microsc Res Tech. 2001;53:278–287
  65. Havenith CE, van Haarst JM, Breedijk AJ, et al. Enrichment and characterization of dendritic cells from human bronchoalveolar lavages. Clin Exp Immunol. 1994;96:339–343
  66. Munro CS, Campbell DA, Du Bois RM, Mitchell DN, Cole PJ, Poulter LW. Dendritic cells in cutaneous, lymph node and pulmonary lesions of sarcoidosis. Scand J Immunol. 1987;25:461–467
  67. Ota M, Amakawa R, Uehira K, et al. Involvement of dendritic cells in sarcoidosis. Thorax. 2004;59:408–413
  68. Oliver SJ, Kikuchi T, Krueger JG, Kaplan G. Thalidomide induces granuloma differentiation in sarcoid skin lesions associated with disease improvement. Clin Immunol. 2002;102:225–236
  69. Mentzer SJ. Dendritic cells in the pathophysiology of sarcoidal reactions. In Vivo. 2000;14:209–212
  70. Macaron NC, Cohen C, Chen SC, Arbiser JL. gli-1 oncogene is highly expressed in granulomatous skin disorders, including sarcoidosis, granuloma annulare, and necrobiosis lipoidica diabeticorum. Arch Dermatol. 2005;141:259–262
  71. Richter E, Kataria YP, Zissel G, Homolka J, Schlaak M, Muller-Quernheim J. Analysis of the Kveim-Siltzbach test reagent for bacterial DNA. Am J Respir Crit Care Med. 1999;159:1981–1984
  72. Kataria YP, Park HK. Dynamics and mechanism of the sarcoidal granuloma. Detecting T cell subsets, non-T cells, and immunoglobulins in biopsies at varying intervals of Kveim-Siltzbach test sites. Ann N Y Acad Sci. 1986;465:221–232
  73. Shaw PA, Fletcher A. Counts of S-100 positive epidermal dendritic cells in Kveim test skin biopsies. Histopathology. 1991;18:149–153
  74. Munro CS, Mitchell DN, Poulter LW, Cole PJ. Early cellular responses to intradermal injection of Kveim suspension in normal subjects and those with sarcoidosis. J Clin Pathol. 1986;39:176–182
  75. Kataria YP, Holter JF. Immunology of sarcoidosis. Clin Chest Med. 1997;18:719–739
  76. Teirstein AS. Kveim antigen: what does it tell us about causation of sarcoidosis?. Semin Respir Infect. 1998;13:206–211
  77. O'Regan AW, Chupp GL, Lowry JA, Goetschkes M, Mulligan N, Berman JS. Osteopontin is associated with T cells in sarcoid granulomas and has T cell adhesive and cytokine-like properties in vitro. J Immunol. 1999;162:1024–1031
  78. Nau GJ, Liaw L, Chupp GL, Berman JS, Hogan BL, Young RA. Attenuated host resistance against Mycobacterium bovis BCG infection in mice lacking osteopontin. Infect Immun. 1999;67:4223–4230
  79. O'Regan AW, Hayden JM, Body S, et al. Abnormal pulmonary granuloma formation in osteopontin-deficient mice. Am J Respir Crit Care Med. 2001;164:2243–2247
  80. Yamagami H, Matsumoto T, Fujiwara N, et al. Trehalose 6,6′-dimycolate (cord factor) of Mycobacterium tuberculosis induces foreign-body- and hypersensitivity-type granulomas in mice. Infect Immun. 2001;69:810–815
  81. Co DO, Hogan LH, Il-Kim S, Sandor M. T cell contributions to the different phases of granuloma formation. Immunol Lett. 2004;92:135–142
  82. Kunkel SL, Lukacs NW, Strieter RM, Chensue SW. Animal models of granulomatous inflammation. Semin Respir Infect. 1998;13:221–228
  83. Nishiwaki T, Yoneyama H, Eishi Y, et al. Indigenous pulmonary Propionibacterium acnes primes the host in the development of sarcoid-like pulmonary granulomatosis in mice. Am J Pathol. 2004;165:631–639
  84. Perez RL, Rivera-Marrero CA, Roman J. Pulmonary granulomatous inflammation: from sarcoidosis to tuberculosis. Semin Respir Infect. 2003;18:23–32
  85. Minami J, Eishi Y, Ishige Y, et al. Pulmonary granulomas caused experimentally in mice by a recombinant trigger-factor protein of Propionibacterium acnes. J Med Dent Sci. 2003;50:265–274
  86. Seiler P, Aichele P, Bandermann S, et al. Early granuloma formation after aerosol Mycobacterium tuberculosis infection is regulated by neutrophils via CXCR3-signaling chemokines. Eur J Immunol. 2003;33:2676–2686
  87. Belcher RW, Reid JD. Sarcoid granulomas in CBA/J mice. Histologic response after inoculation with sarcoid and nonsarcoid tissue homogenates. Arch Pathol. 1975;99:283–285
  88. Mitchell DN, Rees RJ, Goswami KK. Transmissible agents from human sarcoid and Crohn's disease tissues. Lancet. 1976;2:761–765
  89. French MA, Price P, Stone SF. Immune restoration disease after antiretroviral therapy. Aids. 2004;18:1615–1627
  90. Blanche P, Passeron A, Gombert B, Ginsburg C, Salmon D, Sicard D. Sarcoidosis and HIV infection: influence of highly active antiretroviral therapy. Br J Dermatol. 1999;140:1185
  91. Foulon G, Wislez M, Naccache JM, et al. Sarcoidosis in HIV-infected patients in the era of highly active antiretroviral therapy. Clin Infect Dis. 2004;38:418–425
  92. Gomez V, Smith PR, Burack J, Daley R, Rosa U. Sarcoidosis after antiretroviral therapy in a patient with acquired immunodeficiency syndrome. Clin Infect Dis. 2000;31:1278–1280
  93. Lenner R, Bregman Z, Teirstein AS, DePalo L. Recurrent pulmonary sarcoidosis in HIV-infected patients receiving highly active antiretroviral therapy. Chest. 2001;119:978–981
  94. Naccache JM, Antoine M, Wislez M, et al. Sarcoid-like pulmonary disorder in human immunodeficiency virus-infected patients receiving antiretroviral therapy. Am J Respir Crit Care Med. 1999;159:2009–2013
  95. Trevenzoli M, Cattelan AM, Marino F, Marchioro U, Cadrobbi P. Sarcoidosis and HIV infection: a case report and a review of the literature. Postgrad Med J. 2003;79:535–538
  96. Blanche P, Gombert B, Rollot F, Salmon D, Sicard D. Sarcoidosis in a patient with acquired immunodeficiency syndrome treated with interleukin-2. Clin Infect Dis. 2000;31:1493–1494
  97. Logan TF, Bensadoun ES. Increased disease activity in a patient with sarcoidosis after high dose interleukin 2 treatment for metastatic renal cancer. Thorax. 2005;60:610–611
  98. Cogrel O, Doutre MS, Marliere V, Beylot-Barry M, Couzigou P, Beylot C. Cutaneous sarcoidosis during interferon alfa and ribavirin treatment of hepatitis C virus infection: two cases. Br J Dermatol. 2002;146:320–324
  99. Ramos-Casals M, Mana J, Nardi N, et al. Sarcoidosis in patients with chronic hepatitis C virus infection: analysis of 68 cases. Medicine (Baltimore). 2005;84:69–80
  100. Weyer P, Cummings OW, Knox KS. A 49-year-old woman with hepatitis, confusion, and abnormal chest radiograph findings. Chest 2005;128(4):3076-7, 3078-9.
  101. Hurst EA, Mauro T. Sarcoidosis associated with pegylated interferon alfa and ribavirin treatment for chronic hepatitis C: a case report and review of the literature. Arch Dermatol. 2005;141:865–868
  102. Mirmirani P, Maurer TA, Herndier B, McGrath M, Weinstein MD, Berger TG. Sarcoidosis in a patient with AIDS: a manifestation of immune restoration syndrome. J Am Acad Dermatol. 1999;41(2 Pt 2):285–286
  103. Ionescu DN, Hunt JL, Lomago D, Yousem SA. Recurrent sarcoidosis in lung transplant allografts: granulomas are of recipient origin. Diagn Mol Pathol. 2005;14:140–145
  104. Milman N, Andersen CB, Burton CM, Iversen M. Recurrent sarcoid granulomas in a transplanted lung derive from recipient immune cells. Eur Respir J. 2005;26:549–552
  105. Heyll A, Meckenstock G, Aul C, et al. Possible transmission of sarcoidosis via allogeneic bone marrow transplantation. Bone Marrow Transplant. 1994;14:161–164
  106. Padilla ML, Schilero GJ, Teirstein AS. Donor-acquired sarcoidosis. Sarcoidosis Vasc Diffuse Lung Dis. 2002;19:18–24
  107. Tauro S, Mahendra P. Resolution of sarcoidosis after allogeneic bone marrow transplantation with donor lymphocyte infusions. Bone Marrow Transplant. 2001;27:757–759

PII: S0738-081X(07)00056-9

doi: 10.1016/j.clindermatol.2007.03.002

Clinics in Dermatology
Volume 25, Issue 3 , Pages 250-258 , May 2007

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