Apoptotic DNA binds to HLA class II molecules inhibiting antigen presentation and participating in the development of anti-inflammatory functional behavior of phagocytic macrophages

Human Immunology

Volumn 64, Issue 1, 2003, Pages 9-20

  Filaci, Gilberto ^a   Contini, Paola ^a   Fravega, Marco ^a   Fenoglio, Daniela ^a   Azzarone, Bruno ^b   Julien Giron, Michel ^b   Fiocca, Roberto ^c   Boggio, Maurizio ^c   Necchi, Vittorio ^d   De Lerma Barbaro, Andrea ^e   Merlo, Andrea ^c   Rizzi, Marta ^a   Ghio, Massimo ^a   Setti, Maurizio ^a   Puppo, Francesco ^a   Zanetti, Maurizio ^f   Indiveri, Francesco ^c  

^a UNIVERSITY OF GENOA   (Italy)

^b HÔPITAL PAUL BROUSSE   (France)

^c UNIVERSITY OF GENOA   (Italy)

^d UNIVERSITY OF PAVIA   (Italy)

^e UNIVERSITY OF INSUBRIA   (Italy)

^f UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Dendritic cells; DNA; HLA class II molecules; Immunoregulation; Tolerance

Indexed keywords

AUTOANTIGEN; CANCER GROWTH FACTOR; HLA ANTIGEN CLASS 2; TUMOR NECROSIS FACTOR ALPHA;

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; CELL FUNCTION; DENDRITIC CELL; DNA BINDING; HUMAN; HUMAN CELL; IMMUNOPATHOLOGY; IMMUNOREGULATION; INFLAMMATION; NECROSIS; PHAGOCYTOSIS; PRIORITY JOURNAL;

ANTIGEN PRESENTATION; APOPTOSIS; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; JURKAT CELLS; MACROPHAGES; PHAGOCYTES; PHAGOCYTOSIS;

EID: 12244250755     PISSN: 01988859     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0198-8859(02)00778-4     Document Type: Article

References (49)

1. Steller H: Mechanisms and genes of cellular suicide. Science 267:1445, 1995.
2. Surh CD, Sprent J: T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 372:100, 1994.
3. Rajewsky K: Early and late B-cell development in the mouse. Curr Opin Immunol 4:171, 1992.
4. Rathmell JC, Goodnow CC: Effects of the lpr mutation on elimination and inactivation of self-reactive B cells. J Immunol 153:2831, 1994.
5. Webb SR, Hutchinson J, Hayden K, Sprent J: Expansion/deletion of mature T cells exposed to endogenous superantigens in vivo. J Immunol 152:586, 1994.
6. Kabelitz D, Pohl T, Pechhold K: Activation-induced cell death (apoptosis) of mature peripheral T lymphocytes. Immunol Today 14:338, 1993.
7. Savill JS, Wyllie AH, Henson JE, Walport MJ, Henson PM, Haslett C: Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J Clin Invest 83:865, 1989.
8. Haslett C: Resolution of acute inflammation and the role of apoptosis in the tissue fate of granulocytes. Clin Sci 83:639, 1992.
9. Nagata S, Golstein P: The Fas death factor. Science 267: 1449, 1995.
10. Metchnikoff E: Lectures on the Comparative Pathology of Inflammation. London: Kegan, Paul, Trench, and Trubner, 1893.
11. Savill J, Fadok V, Henson P, Haslett C: Phagocyte recognition of cells undergoing apoptosis. Immunol Today 14:131, 1993.
12. Norbury CC, Hewlett JL, Prescott AR, Shastri N, Watts C: Class I MHC presentation of exogenous soluble antigen via macropinocytosis in bone marrow macrophages. Immunity 3:783, 1995.
13. Gordon S: Macrophages and the immune response. In Paul WE (ed): Fundamental Immunology, Fourth Edition. Philadelphia: Lippincott-Raven Publishers, 1999.
14. Ren Y, Silverstein RL, Allen J, Savill J: CD36 gene transfer confers capacity for phagocytosis of cells undergoing apoptosis. J Exp Med 181:1857, 1995.
15. Aderem A, Undrehill DM: Mechanisms of phagocytosis in macrophages. Ann Rev Immunol 17:593, 1999.
16. Fadok VA, Bratton DL, Rose DM, Pearson A, Ezekewitz RA, Henson PM: A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405:85, 2000.
17. Cohen JJ: Apoptosis. Immunol Today 14:126, 1993.
18. Voll RE, Herrmann M, Roth E, Stach C, Kalder JR, Girkontaite I: Immunosuppressive effects of apoptotic cells. Nature 390:350, 1997.
19. 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-beta, PGE2, and PAF. J Clin Invest 101:890, 1998.
20. Ronchetti A, Rovere P, Iezzi G, Galati G, Heltai S, Protti MP, Garancini MP, Manfredi AA, Rugarli C, Bellone M: Immunogenicity of apoptotic cells in vivo: role of antigen load, antigen-presenting cells, and cytokines. J Immunol 163:130, 1999.
21. Nouri-Shirazi M, Banchereau J, Bell D, Burkeholder S, Kraus ET, Davoust J, Palucka KA: Dendritic cells capture killed tumor cells and present their antigens to elicit tumor-specific immune responses. J Immunol 165:3797, 2000.
22. Castedo M, Hirsch T, Susin SA, Zamzami N, Marchetti P, Macho A, Kroemer G: Sequential acquisition of mitochondrial and plasma membrane alterations during early lymphocyte apoptosis. J Immunol 157:512, 1996.
23. Temponi M, Kekish U, Hamby CV, Nielsen H, Marboe CC, Ferrone S: Characterization of anti-HLA class II monoclonal antibody LGII-612.14 reacting with formalin fixed tissues. J Immunol Methods 161:239, 1993.
24. Fiocca R, Necchi V, Sommi P, Ricci V, Telford J, Cover TL, Solcia E: Release of Helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles. Uptake of released toxin and vesicles by gastric epithelium. J Pathol 188:220, 1999.
25. Russo C, Nepo A, Lanza E, Igarashi M, Ferrone S: Antibody-induced association between discrete regions of HLA class I and II antigens. J Immunol 138:3152, 1987.
26. Parham P, Barnstable CJ, Bodmer WF: Use of a monoclonal antibody (W6/32) in structural studies of HLA-A, -B, -C antigens. J Immunol 123:342, 1979.
27. Natali P, Nicotra MR, Cavaliere R, Bigotti A, Romano G, Temponi M, Ferrone S: Differential expression of intercellular adhesion molecule 1 in primary and metastatic melanoma lesions. Cancer Res 50:1271, 1990.
28. Molinaro GA, Quaranta V, Ferrone S: Characterization of the specificity of DR monoclonal antibodies. Transplant Proc 11:1748, 1979.
29. Current Protocols in Immunology. New York: Greene Publ. Assoc. & Wiley Interscience, 1994.
30. Filaci G, Contini P, Grasso I, Bignardi D, Ghio M, Lanza L, Scudeletti M, Puppo F, Bolognesi M, Accolla RS, Indiveri F: dsDNA binds to HLA class II molecules and inhibits HLA class II mediated antigen presentation. Eur J Immunol 28:3968, 1998.
31. Weiss A: T-lymphocyte activation. In Paul WE (ed): Fundamental Immunology, Fourth Edition. Philadelphia: Lippincott-Raven Publishers, 1999.
32. Kehrl JH, Taylor A, Kim SJ, Fauci AS: Transforming growth factor-beta is a potent negative regulator of human lymphocytes. Ann NY Acad Sci 628:345, 1991.
33. Steinman RM: Dendritic cells. In Paul WE (ed): Fundamental Immunology, Fourth Edition. Philadelphia: Lippincott-Raven Publishers, 1999.
34. Magnus T, Chan A, Grauer O, Toyka KV, Gold R: Microglial phagocytosis of apoptotic inflammatory T cells leads to down-regulation of microglial immune activation. J Immunol 167:5004, 2001.
35. Albrechtsen D, Solheim B, Thorsey E: Antiserum inhibition of the mixed lymphocyte culture (MLC) interaction. Inhibitory effect of antibodies reactive with HLA-D-associated determinants. Cell Immunol 28:258, 1977.
36. Accolla RS, Moretta A, Cerottini J-C: Allogeneic mixed lymphocyte reactions in humans: pretreatment of either the stimulator or the responder cell population with monoclonal anti-Ia antibodies leads to an inhibition of cell proliferation. J Immunol 127:2438, 1981.
37. Thomas DW, Yamashita U, Shevac EM: Nature of the antigenic complex recognized by T lymphocytes. IV. Inhibition of antigen-specific T cell proliferation by antibodies to stimulator macrophage Ia antigens. J Immunol 119:223, 1977.
38. Triebel F, Missenard-Leblond V, Couty MC, Charron DJ, Debre P: Differential inhibition of human antigen-specific T cell clone proliferative responses by distinct monoclonal anti-HLA-DR antibodies. J Immunol 132:1773, 1984.
39. Romain PL, Schlossman SF, Reinherz EL: Surface molecules involved in self-recognition and T cell activation in the autologous mixed lymphocyte reaction. J Immunol 133:1093, 1984.
40. Yamamoto K, Watanabe T, Otsubo O, Nakauchi H, Okumura K: Prolonged survival of dog kidney allografts induced by a monoclonal anti-Ia antibody. Transplantation 37:419, 1984.
41. Davies DA, Staines NA: A cardinal role for I-region antigens (Ia) in immunological enhancement, and the clinical implications. Transplant Rev 30:18, 1976.
42. Barker RN, Erwig LP, Hill KS, Devine A, Pearce WP, Rees AJ: Antigen presentation by macrophages is enhanced by the uptake of necrotic, but not apoptotic, cells. Clin Exp Immunol 127:220, 2002.
43. Kehrl JH, Thevenin C, Rieckmann P, Fauci AS: Transforming growth factor-beta suppresses human B lymphocyte Ig production by inhibiting synthesis and the switch from the membrane form to the secreted form of Ig mRNA. J Immunol 146:4016, 1991.
44. Strobl H, Knapp W: TGF-beta1 regulation of dendritic cells. Microbes Infect 1:1283, 1999.
45. Dieckmann D, Plottner H, Berchtold S, Berger T, Schuler G: Ex vivo isolation and characterization of CD4(+)CD25(+) T cells with regulatory properties from human blood. J Exp Med 193:1303, 2001.
46. Jonuleit H, Schmitt E, Stassen M, Tuettenberg A, Knop J, Enk AK: Identification and functional characterization of human CD4(+)CD25(+) T cells with regulatory properties isolated from peripheral blood. J Exp Med 193: 1285, 2001.
47. Ciubotariu R, Colovai AI, Pennesi G, Liu Z, Smith D, Berlocco P, Cortesini R, Suciu-Foca N: Specific suppression of human CD4+ Th cell responses to pig MHC antigens by CD8+CD28- regulatory T cells. J Immunol 161:5193, 1998.
48. Filaci G, Bacilieri S, Fravega M, Monetti M, Contini P, Ghio M, Setti M, Puppo F, Indiveri F: Impairment of CD8+ T suppressor cell function in patients with active systemic lupus erythematosus. J Immunol 166:6452, 2001.
49. 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 41:1241, 1998.