Induction of interferon-α production in plasmacytoid dendritic cells by immune complexes containing nucleic acid released by necrotic or late apoptotic cells and lupus IgG

Arthritis and Rheumatism

Volumn 50, Issue 6, 2004, Pages 1861-1872

  Lövgren, Tanja ^a,c   Eloranta, Maija Leena ^b   Båve, Ullvi ^a   Alm, Gunnar V ^b   Rönnblom, Lars ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; AUTOANTIBODY; DEOXYRIBONUCLEASE; DNA; DNA ANTIBODY; IMMUNOGLOBULIN G; NUCLEIC ACID; RIBONUCLEASE; RNA; RNA BINDING PROTEIN; RNA BINDING PROTEIN ANTIBODY; UNCLASSIFIED DRUG;

ADOLESCENT; AGED; ANTIGEN ANTIBODY COMPLEX; APOPTOSIS; ARTICLE; CASE REPORT; CELL DEATH; CELL STRAIN U937; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; FREEZING; HUMAN; HUMAN CELL; IMMUNOASSAY; INTERFERON PRODUCTION; MALE; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; SUPERNATANT; SYSTEMIC LUPUS ERYTHEMATOSUS; THAWING; ULTRAVIOLET RADIATION;

ANTIGEN-ANTIBODY COMPLEX; APOPTOSIS; DENDRITIC CELLS; DEOXYRIBONUCLEASES; DNA; FREEZING; HUMANS; IMMUNOGLOBULIN G; INTERFERON-ALPHA; LEUKOCYTES, MONONUCLEAR; LUPUS ERYTHEMATOSUS, SYSTEMIC; NECROSIS; RIBONUCLEASES; RNA; U937 CELLS; ULTRAVIOLET RAYS;

EID: 2642528779     PISSN: 00043591     EISSN: None     Source Type: Journal    
DOI: 10.1002/art.20254     Document Type: Article

References (76)

1. Fritzler MJ, Andrade L. Antibodies to nonhistone antigens in systemic lupus erythematosus. In: Lahita RG, editor. Systemic lupus erythematosus. 3rd ed. San Diego: Academic Press; 1999. p. 247-67.
2. Ronnblom L, Alm GV. An etiopathogenic role for the type I IFN system in SLE. Trends Immunol 2001;22:427-31.
3. Ronnblom L, Alm GV. The natural interferon-α producing cells in systemic lupus erythematosus. Hum Immunol 2002;63:1181-93.
4. Preble OT, Black RJ, Friedman RM, Klippel JH, Vilcek J. Systemic lupus erythematosus: presence in human serum of an unusual acid-labile leukocyte interferon. Science 1982;216:429-31.
5. Ytterberg SR, Schnitzer TJ. Serum interferon levels in patients with systemic lupus erythematosus. Arthritis Rheum 1982;25:401-6.
6. Strannegard O, Hermodsson S, Westberg G. Interferon and natural killer cells in systemic lupus erythematosus. Clin Exp Immunol 1982;50:246-52.
7. Bengtsson AA, Sturfelt G, Truedsson L, Blomberg J, Alm G, Vallin H, et al. Activation of type I interferon system in systemic lupus erythematosus correlates with disease activity but not with antiretroviral antibodies. Lupus 2000;9:664-71.
8. Baechler EC, Batliwalla FM, Karypis G, Gaffney PM, Ortmann WA, Espe KJ, et al. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci U S A 2003;100:2610-5.
9. Ioannou Y, Isenberg DA. Current evidence for the induction of autoimmune rheumatic manifestations by cytokine therapy. Arthritis Rheum 2000;43:1431-42.
10. Raanani P, Ben-Bassat I. Immune-mediated complications during interferon therapy in hematological patients. Acta Haematol 2002;107:133-44.
11. Ronnblom LE, Alm GV, Oberg KE. Possible induction of systemic lupus erythematosus by interferon-α treatment in a patient with a malignant carcinoid tumour. J Intern Med 1990;227:207-10.
12. Ehrenstein MR, McSweeney E, Swane M, Worman CP, Goldstone AH, Isenberg DA. Appearance of anti-DNA antibodies in patients treated with interferon-α. Arthritis Rheum 1993;36:279-80.
13. Kalkner KM, Ronnblom L, Karlsson Parra AK, Bengtsson M, Olsson Y, Oberg K. Antibodies against double-stranded DNA and development of polymyositis during treatment with interferon. QJM 1998;91:393-9.
14. Bogdan C. The function of type I interferons in antimicrobial immunity. Curr Opin Immunol 2000;12:419-24.
15. Biron CA. Interferons α and β as immune regulators - a new look. Immunity 2001;14:661-4.
16. Belardelli F, Ferrantini M. Cytokines as a link between innate and adaptive antitumor immunity. Trends Immunol 2002;23:201-8.
17. Luft T, Pang KC, Thomas E, Hertzog P, Hart DN, Trapani J, et al. Type I IFNs enhance the terminal differentiation of dendritic cells. J Immunol 1998;161:1947-53.
18. Paquette RL, Hsu NC, Kiertscher SM, Park AN, Tran L, Roth MD, et al. Interferon-α and granulocyte-macrophage colony-stimulating factor differentiate peripheral blood monocytes into potent antigen-presenting cells. J Leukoc Biol 1998;64:358-67.
19. Le Bon A, Schiavoni G, D'Agostino G, Gresser I, Belardelli F, Tough DF. Type I interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in vivo. Immunity 2001;14:461-70.
20. Marrack P, Kappler J, Mitchell T. Type I interferons keep activated T cells alive. J Exp Med 1999;189:521-30.
21. Ruuth K, Carlsson L, Hallberg B, Lundgren E. Interferon-α promotes survival of human primary B-lymphocytes via phosphatidylinositol 3-kinase. Biochem Biophys Res Commun 2001;284:583-6.
22. Braun D, Caramalho I, Demengeot J. IFN-α/β enhances BCR-dependent B cell responses. Int Immunol 2002;14:411-9.
23. Vallin H, Blomberg S, Alm GV, Cederblad B, Ronnblom L. Patients with systemic lupus erythematosus (SLE) have a circulating inducer of interferon-α (IFN-α) production acting on leucocytes resembling immature dendritic cells. Clin Exp Immunol 1999;115:196-202.
24. Vallin H, Perers A, Alm GV, Ronnblom L. Anti-double-stranded DNA antibodies and immunostimulatory plasmid DNA in combination mimic the endogenous IFN-α inducer in systemic lupus erythematosus. J Immunol 1999;163:6306-13.
25. Amoura Z, Piette JC, Chabre H, Cacoub P, Papo T, Wechsler B, et al. Circulating plasma levels of nucleosomes in patients with systemic lupus erythematosus: correlation with serum antinucleosome antibody titers and absence of clear association with disease activity. Arthritis Rheum 1997;40:2217-25.
26. Perniok A, Wedekind F, Herrmann M, Specker C, Schneider M. High levels of circulating early apoptic peripheral blood mononuclear cells in systemic lupus erythematosus. Lupus 1998;7:113-8.
27. Emlen W, Niebur J, Kadera R. Accelerated in vitro apoptosis of lymphocytes from patients with systemic lupus erythematosus. J Immunol 1994;152:3685-92.
28. Shoshan Y, Shapira I, Toubi E, Frolkis I, Yaron M, Mevorach D. Accelerated Fas-mediated apoptosis of monocytes and maturing macrophages from patients with systemic lupus erythematosus: relevance to in vitro impairment of interaction with iC3b-opsonized apoptotic cells. J Immunol 2001;167:5963-9.
29. Grondal G, Traustadottir KH, Kristjansdottir H, Lundberg I, Klareskog L, Erlendsson K, et al. Increased T-lymphocyte apoptosis/necrosis and IL-10 producing cells in patients and their spouses in Icelandic systemic lupus erythematosus multicase families. Lupus 2002;11:435-42.
30. Herrmann M, Voll RE, Zoller OM, Hagenhofer M, Ponner BB, Kalden JR. Impaired phagocytosis of apoptotic cell material by monocyte-derived macrophages from patients with systemic lupus erythematosus. Arthritis Rheum 1998;41:1241-50.
31. Bave U, Alm GV, Ronnblom L. The combination of apoptotic U937 cells and lupus IgG is a potent IFN-α inducer. J Immunol 2000;165:3519-26.
32. Bave U, Vallin H, Alm GV, Ronnblom L. Activation of natural interferon-α producing cells by apoptotic U937 cells combined with lupus IgG and its regulation by cytokines. J Autoimmun 2001;17:71-80.
33. Svensson H, Johannisson A, Nikkila T, Alm GV, Cederblad B. The cell surface phenotype of human natural interferon-α producing cells as determined by flow cytometry. Scand J Immunol 1996;44:164-72.
34. Siegal FP, Kadowaki N, Shodell M, Fitzgerald-Bocarsly PA, Shah K, Ho S, et al. The nature of the principal type 1 interferon-producing cells in human blood. Science 1999;284:1835-7.
35. Cella M, Jarrossay D, Facchetti F, Alebardi O, Nakajima H, Lanzavecchia A, et al. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat Med 1999;5:919-23.
36. Fitzgerald-Bocarsly P. Natural interferon-α producing cells: the plasmacytoid dendritic cells. Biotechniques 2002;33 Suppl:16-29.
37. Cederblad B, Blomberg S, Vallin H, Perers A, Alm GV, Ronnblom L. Patients with systemic lupus erythematosus have reduced numbers of circulating natural interferon-α-producing cells. J Autoimmun 1998;11:465-70.
38. Blomberg S, Eloranta ML, Magnusson M, Alm GV, Ronnblom L. Expression of the markers BDCA-2 and BDCA-4 and production of interferon-α by plasmacytoid dendritic cells in systemic lupus erythematosus. Arthritis Rheum 2003;48:2524-32.
39. Farkas L, Beiske K, Lund-Johansen F, Brandtzaeg P, Jahnsen FL. Plasmacytoid dendritic cells (natural interferon-α/β-producing cells) accumulate in cutaneous lupus erythematosus lesions. Am J Pathol 2001;159:237-43.
40. Blomberg S, Eloranta ML, Cederblad B, Nordlin K, Alm GV, Ronnblom L. Presence of cutaneous interferon-α producing cells in patients with systemic lupus erythematosus. Lupus 2001;10:484-90.
41. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982;25:1271-7.
42. Hylkema MN, Huygen H, Kramers C, van de Wal TJ, de Jong J, van Bruggen MC, et al. Clinical evaluation of a modified ELISA, using photobiotinylated DNA, for the detection of anti-DNA antibodies. J Immunol Methods 1994;170:93-102.
43. Feltkamp TE, Kirkwood TB, Maini RN, Aarden LA. The first international standard for antibodies to double stranded DNA. Ann Rheum Dis 1988;47:740-6.
44. Dzionek A, Fuchs A, Schmidt P, Cremer S, Zysk M, Miltenyi S, et al. BDCA-2, BDCA-3, and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood. J Immunol 2000;165:6037-46.
45. Sauter B, Albert ML, Francisco L, Larsson M, Somersan S, Bhardwaj N. Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J Exp Med 2000;191:423-34.
46. Gallucci S, Lolkema M, Matzinger P. Natural adjuvants: endogenous activators of dendritic cells. Nat Med 1999;5:1249-55.
47. Gershov D, Kim S, Brot N, Elkon KB. C-reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an antiinflammatory innate immune response: implications for systemic autoimmunity [published erratum appears in J Exp Med 2001;193:1439]. J Exp Med 2000;192:1353-64.
48. Gershov D, Kim S, Brot N, Elkon KB. C-reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an antiinflammatory innate immune response: implications for systemic autoimmunity [published erratum appears in J Exp Med 2001;193:1439]. J Exp Med 2000;192:1353-64.
49. Li M, Carpio DF, Zheng Y, Bruzzo P, Singh V, Ouaaz F, et al. An essential role of the NF-κB/Toll-like receptor pathway in induction of inflammatory and tissue-repair gene expression by necrotic cells. J Immunol 2001;166:7128-35.
50. Van Cruchten S, van den Broeck W. Morphological and biochemical aspects of apoptosis, oncosis and necrosis. Anat Histol Embryol 2002;31:214-23.
51. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-β, PGE2, and PAF. J Clin Invest 1998;101:890-8.
52. Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, Girkontaite I. Immunosuppressive effects of apoptotic cells. Nature 1997;390:350-1.
53. Payvandi F, Amrute S, Fitzgerald-Bocarsly P. Exogenous and endogenous IL-10 regulate IFN-α production by peripheral blood mononuclear cells in response to viral stimulation. J Immunol 1998;160:5861-8.
54. Bave U, Magnusson M, Eloranta ML, Perers A, Alm GV, Ronnblom L. FcγRIIa is expressed on natural IFN-α-producing cells (plasmacytoid dendritic cells) and is required for the IFN-α production induced by apoptotic cells combined with lupus IgG. J Immunol 2003;171:3296-302.
55. Majde JA. Viral double-stranded RNA, cytokines, and the flu. J Interferon Cytokine Res 2000;20:259-72.
56. Reichlin M, Harley JB. Antibodies to Ro/SSA and La/SSB. In: Wallace DJ, Hahn BH, editors. Dubois' lupus erythematosus. 6th ed. Philadelphia: Lippincott Williams & Wilkins; 2002. p. 467-80.
57. Craft JE. Anti-snRNP antibodies. In: Wallace DJ, Hahn BH, editors. Dubois' lupus erythematosus. 6th ed. Philadelphia: Lippincott Williams & Wilkins; 2002. p. 481-94.
58. Krug A, Rothenfusser S, Hornung V, Jahrsdorfer B, Blackwell S, Ballas ZK, et al. Identification of CpG oligonucleotide sequences with high induction of IFN-α/β in plasmacytoid dendritic cells. Eur J Immunol 2001;31:2154-63.
59. Magnusson M, Magnusson S, Vallin H, Ronnblom L, Alm GV. Importance of CpG dinucleotides in activation of natural IFN-α-producing cells by a lupus-related oligodeoxynucleotide. Scand J Immunol 2001;54:543-50.
60. Richardson BC. Role of DNA methylation in the regulation of cell function: autoimmunity, aging and cancer. J Nutr 2002;132(8 Suppl):2401S-5S.
61. Huck S, Deveaud E, Namane A, Zouali M. Abnormal DNA methylation and deoxycytosine-deoxyguanine content in nucleosomes from lymphocytes undergoing apoptosis. FASEB J 1999;13:1415-22.
62. Rush LJ, Plass C. Alterations of DNA methylation in hematologic malignancies. Cancer Lett 2002;185:1-12.
63. Batteux F, Palmer P, Daeron M, Weill B, Lebon P. FcγRII (CD32)-dependent induction of interferon-α by serum from patients with lupus erythematosus. Eur Cytokine Netw 1999;10:509-14.
64. Ahmad-Nejad P, Hacker H, Rutz M, Bauer S, Vabulas RM, Wagner H. Bacterial CpG-DNA and lipopolysaccharides activate Toll-like receptors at distinct cellular compartments. Eur J Immunol 2002;32:1958-68.
65. Hornung V, Rothenfusser S, Britsch S, Krug A, Jahrsdorfer B, Giese T, et al. Quantitative expression of Toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J Immunol 2002;168:4531-7.
66. Akira S, Hemmi H. Recognition of pathogen-associated molecular patterns by TLR family. Immunol Lett 2003;85:85-95.
67. Leadbetter EA, Rifkin IR, Hohlbaum AM, Beaudette BC, Shlomchik MJ, Marshak-Rothstein A. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 2002;416:603-7.
68. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 2001;413:732-8.
69. Ito T, Amakawa R, Kaisho T, Hemmi H, Tajima K, Uehira K, et al. Interferon-α and interleukin-12 are induced differentially by Toll-like receptor 7 ligands in human blood dendritic cell subsets. J Exp Med 2002;195:1507-12.
70. Sanders CJ, van Weelden H, Kazzaz GA, Sigurdsson V, Toonstra J, Bruijnzeel-Koomen CA. Photosensitivity in patients with lupus erythematosus: a clinical and photobiological study of 100 patients using a prolonged phototest protocol. Br J Dermatol 2003;149:131-7.
71. Kulms D, Schwarz T. Molecular mechanisms of UV-induced apoptosis. Photodermatol Photoimmunol Photomed 2000;16:195-201.
72. Newkirk MM, van Venrooij WJ, Marshall GS. Autoimmune response to U1 small nuclear ribonucleoprotein (U1 snRNP) associated with cytomegalovirus infection. Arthritis Res 2001;3:253-8.
73. Pisetsky DS. Immune responses to DNA in normal and aberrant immunity. Immunol Res 2000;22:119-26.
74. Chernysheva AD, Kirou KA, Crow MK. T cell proliferation induced by autologous non-T cells is a response to apoptotic cells processed by dendritic cells. J Immunol 2002;169:1241-50.
75. Matzinger P. The danger model: a renewed sense of self. Science 2002;296:301-5.
76. Fujinami RS. Viruses and autoimmune disease-two sides of the same coin? Trends Microbiol 2001;9:377-81.