Nucleosomes inhibit phagocytosis of apoptotic thymocytes by peritoneal macrophages from MRL+/+ lupus-prone mice

Journal of Leukocyte Biology

Volumn 64, Issue 6, 1998, Pages 774-780

  Laderach, Diego ^a   Bach, Jean François ^a   Koutouzov, Sophie ^a  

^a HÔPITAL NECKER ENFANTS MALADES   (France)

Author keywords

Apoptosis; Chromatin; Phagocytosis; SLE

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; FEMALE; MOUSE; MOUSE STRAIN; NONHUMAN; NUCLEOSOME; PERITONEUM MACROPHAGE; PHAGOCYTOSIS; PRIORITY JOURNAL; SYSTEMIC LUPUS ERYTHEMATOSUS; THYMOCYTE;

ANIMALIA; MURINAE;

EID: 0031788414     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1002/jlb.64.6.774     Document Type: Article

References (40)

1. Tan, E. M. (1989) Antinuclear antibodies: diagnostic markers for autoimmune diseases and probes for cell biology. Adv. Immunol. 44, 93-151.
2. Burlingame, R. W., Rubin, R. L., Balderas, R. S., Theofilopoulos, A. N. (1993) Genesis and evolution of antichromatin autoantibodies in murine lupus implicates T-dependent immunization with self antigen. J. Clin. Invest. 91, 1687-1696.
3. Amoura, Z., Chabre, H., Koutouzov, S., Lotton, C., Cabrespines, A., Bach, J. F., Jacob, L. (1994) Nucleosome-restricted antibodies are detected before anti-dsDNA and/or antihistone antibodies in serum of MRL-Mp lpr/lpr and +/+ mice, and are present in kidney eluates of lupus mice with proteinuria. Arthritis Rheum. 37, 1684-1688.
4. Mohan, C., Adams, S., Stanik, V., Datta, S. K. (1993) Nucleosome: a major immunogen for pathogenic autoantibody-inducing T cells of lupus. J. Exp. Med. 177, 1367-1381.
5. Burlingame, R. W., Boey, M. L., Starkebaum, G., Rubin, R. L. (1994) The central role of chromatin in autoimmune responses to histones and DNA in systemic lupus erythematosus. J. Clin. Invest. 94, 184-192.
6. Chabre, H., Amoura, Z., Piette, J. C., Godeau, P., Bach, J. F., Koutouzov, S. (1995) Presence of nucleosome-restricted antibodies in patients with systemic lupus erythematosus. Arthritis Rheum. 38, 1485-1491.
7. Cohen, J. J. (1993) Apoptosis. Immunol. Today 14, 126-130.
8. Casciola-Rosen, L. A., Anhalt, G., Rosen, A. (1994) Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinoeytes. J. Exp. Med. 179, 1317-1330.
9. Savill, J., Fadok, V., Henson, P., Haslett, C. (1993) Phagocyte recognition of cells undergoing apoptosis. Immunol. Today 14, 131-136.
10. Duvall, E., Wyllie, A. H., Morris, R. G. (1985) Macrophage recognition of cells undergoing programmed cell death (apoptosis). Immunol. 56, 351-358.
11. Savill, J., Dransfield, I., Hogg, N., Haslett, C. (1990) Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 343, 170-173.
12. Fadok, V. A., Voelker, D. R., Campbell, P. A., Cohen, J. J., Bratton, D. L., Henson, P. M. (1992) Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immurtol. 148, 2207-2216.
13. Platt, N., Suzuki, H., Kurihara, Y., Kodama, T., Gordon. S. (1996) Role for the class A macrophage scavenger receptor in the phagocytosis of apoptotic thymocytes in vitro. Proc. Natl. Acad. Sci. USA 93, 12456-12460.
14. Luciani, M.-F., Chimini, G. (1996) The ATP binding cassette transporter ABC1, is required for the engulfment of corpses generated by apoptotic cell death. EMBO J. 15, 226-235.
15. Devitt, A., Moffatt, O. D., Raykundalia, C., Capra, J. D., Simmons, D. L., Gregory, C. D. (1998) Human CD14 mediates recognition and phagocytosis of apoptotic cells. Nature 392, 505-509.
16. Fadok, V. A., Savill, J. S., Haslett, C., Bratton, D. L., Doherty, D. E., Campbell, P. A., Henson, P. M. (1992) Different populations of macrophages use either the vitronectin receptor or the phosphatidylserine receptor to recognize and remove apoptotic cells. J. Immunol. 149, 4029-4035.
17. Pradhan, D., Krahling, S., Williamson, P., Schlegel, R. A. (1997) Multiple systems for recognition of apoptotic lymphocytes by macrophages. Mol. Biol. Cell 8, 767-778.
18. Emlen, W., Niebur, J., Kadera, R. (1994) Accelerated in vitro apoptosis of lymphocytes from patients with systemic lupus erythematosus. J. Immunol. 152, 3685-3692.
19. Van Houten, N., Budd, R. C. (1992) Accelerated programmed cell death of MRL-lpr/lpr T lymphocytes. J. Immunol. 149, 2513-2517.
20. Lorenz, H. M., Grunke, M., Hieronymus, T., Herrmann, M., Kuhnel, A., Manger, B., Kalden, J. R. (1997) In vitro apoptosis and expression of apoptosis-related molecules in lymphocytes from patients with systemic lupus erythematosus and other autoimmune diseases. Arthritis Rheum. 40, 306-317.
21. Amoura, Z., Piette, J. C., Chabre, H., Cacoub, P., Papo, T., Wechsler, B., Bach, J. F., Koutouzov, S. (1997) 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. 40, 2217-2225.
22. Rumore, P. M., Steinman, C. R. (1990) Endogenous circulating DNA in systemic lupus erythematosus. Occurrence as multimeric complexes bound to histone. J. Clin. Invest. 86, 69-74.
23. Kramers, C., Hylkema, M. N., Van Bruggen, M. C., Van de Lagemaat, R., Dijkman, H. B., Assmann, K. J., Smeenk, R. J., Berden, J. H. (1994) Anti-nucleosome antibodies complexed to nucleosomal antigens show anti-DNA reactivity and bind to rat glomerular basement membrane in vivo. J. Clin. Invest. 94, 568-577.
24. Van Bruggen, M. C., Walgreen, B., Rijke, T. P., Tamboer, W., Kramers, K., Smeenk, R. J., Monestier, M., Fournie, G. J., Berden, J. H. (1997) Antigen specificity of anti-nuclear antibodies complexed to nucleosomes determines glomerular basement membrane binding in vivo. Eur. J. Immunol. 27, 1564-1569.
25. Bernstein, K. A., Valerio, R. D., Lefkowith, J. B. (1995) Glomerular binding activity in MRL lpr serum consists of antibodies that bind to a DNA/histone/type IV collagen complex. J. Immunol. 154, 2424-2433.
26. Lefkowith, J. B., Di Valerio, R., Norris, J., Glick, G. D., Alexander, A. L., Jackson, L., Gilkeson, G. S. (1996) Murine glomerulotropic monoclonal antibodies are highly oligoclonal and exhibit distinctive molecular features. J. Immunol. 157, 1297-1305.
27. Emlen, W., Holers, V. M., Arend, W. P., Kotzin, B. (1992) Regulation of nuclear antigen expression on the cell surface of human monocytes. J. Immunol. 148, 3042-3048.
28. Coritsidis, G. N., Beers, P. C., Rumore, P. M. (1995) Glomerular uptake of nucleosomes: evidence for receptor-mediated mesangial cell binding. Kidney Int. 47, 1258-1265.
29. Koutouzov, S., Cabrespines, A., Amoura, Z., Chabre, H., Lotton, C., Bach, J. F. (1996) Binding of nucleosomes to a cell surface receptor: redistribution and endocytosis in the presence of lupus antibodies. Eur. J. Immunol. 26, 472-486.
30. Bell, D. A., Morrison, B., Vandenbygaart, P. (1990) Immunogenic DNA-related factors. Nucleosomes spontaneously released from normal murine lymphoid cells stimulate proliferation and immunoglobulin synthesis of normal mouse lymphocytes. J. Clin. Invest. 85, 1487-1496.
31. Bell, D. A., Morrison, B. (1991) The spontaneous apoptotic death of normal human lymphocytes in vitro: the release of, and immunoproliferative response to, nucleosomes in vitro. Clin. Immunol. Immunopathol. 60, 13-26.
32. Hefeneider, S. H., Cornell, K. A., Brown, L. E., Bakke, A. C., McCoy, S. L., Bennett, R. M. (1992) Nucleosomes and DNA bind to specific cell-surface molecules on murine cells and induce cytokine production. Clin. Immunol. Immunopathol. 63, 245-251.
33. Le Lann, A. D., Fournié, G. J., Boissier, L., Toutain, P.-.L., Benoist, H. (1994) In vitro inhibition of natural-killer-mediated lysis by chromatin fragments. Cancer Immunol. Immunother. 39, 185-192.
34. Theofilopoulos, A. N., Dixon, F. J. (1985) Murine models of systemic lupus erythematosus. Adv. Immunol. 37, 269-390.
35. Datta, S. K., Patel, H., Berry, D. (1987) Induction of a cationic shift in IgG anti-DNA autoantibodies. Role of T helper cells with classical and novel phenotypes in three murine models of lupus nephritis. J. Exp. Med. 165, 1252-1268.
36. Lutter, L. C. (1978) Kinetic analysis of deoxyribonuclease I cleavages in the nucleosome core: evidence for a DNA superhelix. J. Mol. Biol. 124, 391-420.
37. Mevorach, D., Gershov, D., Ng, S., Salmon, J., Elkon, K. B. (1997) Decrease in uptake of apoptotic cells in patients with systemic lupus erythematosus (SLE). Arthritis Rheum. 40, S306 (abstract).
38. Herrmann, M., Voll, R. E., Zoller, O. M., Hagenhofer, M., Ponner, B. B., Kalden, J. R. (1998) Impaired phagocytosis of apoptotic cell material by monocyte-derived macrophages from patients with systemic lupus erythematosus. Arthritis Rheum. 41, 1241-1250.
39. Savill, J., Hogg, N., Ren, Y., Haslett, C. (1992) Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J. Clin. Invest. 90, 1513-1522.
40. Bennett, R. M., Gabor, G. T., Merritt, M. M. (1985) DNA binding to human leukocytes. Evidence for a receptor-mediated association, internalization, and degradation of DNA. J. Clin. Invest. 76, 2182-2190.