Skip to main content
Top
Published in: Seminars in Immunopathology 2/2006

01-10-2006 | Review

Apoptotic cell death and lupus

Author: Philip L. Cohen

Published in: Seminars in Immunopathology | Issue 2/2006

Login to get access

Abstract

Programmed cell death and the disposal of cell corpses by phagocytic cells are highly regulated ongoing processes essential for the survival and well-being of higher organisms. Abnormalities in the susceptibility of certain cells to receptor-induced death are known to lead to certain human diseases (e.g., autoimmune lymphoproliferative syndrome) and may contribute to the pathogenesis of systemic lupus erythematosus. Impaired clearance of apoptotic cells is also likely to be an important factor in lupus pathogenesis, though the biological basis of such a defect remains elusive. Finally, the process of apoptosis has been shown to contribute to lupus disease effector mechanisms. A better understanding of the role of apoptosis in lupus very likely will lead to improved diagnosis and therapy.
Literature
1.
go back to reference Cohen PL, Eisenberg RA (1991) Lpr and gld: single gene models of systemic autoimmunity and lymphoproliferative disease. Annu Rev Immunol 9:243–269PubMedCrossRef Cohen PL, Eisenberg RA (1991) Lpr and gld: single gene models of systemic autoimmunity and lymphoproliferative disease. Annu Rev Immunol 9:243–269PubMedCrossRef
2.
go back to reference Bouillet P, Metcalf D, Huang DC, Tarlinton DM, Kay TW, Kontgen F, Adams JM, Strasser A (1999) Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286:1735–1738PubMedCrossRef Bouillet P, Metcalf D, Huang DC, Tarlinton DM, Kay TW, Kontgen F, Adams JM, Strasser A (1999) Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286:1735–1738PubMedCrossRef
3.
go back to reference Strasser A, Whittingham S, Vaux DL, Bath ML, Adams JM, Cory S, Harris AW (1991) Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc Natl Acad Sci USA 88:8661–8665PubMedCrossRef Strasser A, Whittingham S, Vaux DL, Bath ML, Adams JM, Cory S, Harris AW (1991) Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc Natl Acad Sci USA 88:8661–8665PubMedCrossRef
4.
go back to reference Mohan C, Yu Y, Morel L, Yang P, Wakeland EK (1999) Genetic dissection of Sle pathogenesis: Sle3 on murine chromosome 7 impacts T cell activation, differentiation, and cell death. J Immunol 162:6492–6502PubMed Mohan C, Yu Y, Morel L, Yang P, Wakeland EK (1999) Genetic dissection of Sle pathogenesis: Sle3 on murine chromosome 7 impacts T cell activation, differentiation, and cell death. J Immunol 162:6492–6502PubMed
5.
go back to reference Zhu J, Liu X, Xie C, Yan M, Yu Y, Sobel ES, Wakeland EK, Mohan C (2005) T cell hyperactivity in lupus as a consequence of hyperstimulatory antigen-presenting cells. J Clin Invest 115:1869–1878PubMedCrossRef Zhu J, Liu X, Xie C, Yan M, Yu Y, Sobel ES, Wakeland EK, Mohan C (2005) T cell hyperactivity in lupus as a consequence of hyperstimulatory antigen-presenting cells. J Clin Invest 115:1869–1878PubMedCrossRef
6.
go back to reference Mehrad B, Park SJ, Akangire G, Standiford TJ, Wu T, Zhu J, Mohan C (2006) The lupus-susceptibility locus, Sle3, mediates enhanced resistance to bacterial infections. J Immunol 176:3233–3239PubMed Mehrad B, Park SJ, Akangire G, Standiford TJ, Wu T, Zhu J, Mohan C (2006) The lupus-susceptibility locus, Sle3, mediates enhanced resistance to bacterial infections. J Immunol 176:3233–3239PubMed
7.
go back to reference Roy V, Chang NH, Cai Y, Bonventi G, Wither J (2005) Aberrant IgM signaling promotes survival of transitional T1 B cells and prevents tolerance induction in lupus-prone New Zealand black mice. J Immunol 175:7363–7371PubMed Roy V, Chang NH, Cai Y, Bonventi G, Wither J (2005) Aberrant IgM signaling promotes survival of transitional T1 B cells and prevents tolerance induction in lupus-prone New Zealand black mice. J Immunol 175:7363–7371PubMed
8.
go back to reference Xin H, D’Souza S, Jorgensen TN, Vaughan AT, Lengyel P, Kotzin BL, Choubey D (2006) Increased expression of Ifi202, an IFN-activatable gene, in B6.Nba2 lupus susceptible mice inhibits p53-mediated apoptosis. J Immunol 176:5863–5870PubMed Xin H, D’Souza S, Jorgensen TN, Vaughan AT, Lengyel P, Kotzin BL, Choubey D (2006) Increased expression of Ifi202, an IFN-activatable gene, in B6.Nba2 lupus susceptible mice inhibits p53-mediated apoptosis. J Immunol 176:5863–5870PubMed
9.
go back to reference Chen M, Wang YH, Wang Y, Huang L, Sandoval H, Liu YJ, Wang J (2006) Dendritic cell apoptosis in the maintenance of immune tolerance. Science 311:1160–1164PubMedCrossRef Chen M, Wang YH, Wang Y, Huang L, Sandoval H, Liu YJ, Wang J (2006) Dendritic cell apoptosis in the maintenance of immune tolerance. Science 311:1160–1164PubMedCrossRef
10.
go back to reference Emlen W, Niebur J, Kadera R (1994) Accelerated in vitro apoptosis of lymphocytes form patients with systemic lupus erythematosus. J Immunol 152:3685–3692PubMed Emlen W, Niebur J, Kadera R (1994) Accelerated in vitro apoptosis of lymphocytes form patients with systemic lupus erythematosus. J Immunol 152:3685–3692PubMed
11.
go back to reference Armstrong DJ, Whitehead EM, Crockard AD, Bell AL (2005) Distinctive effects of G-CSF, GM-CSF and TNFalpha on neutrophil apoptosis in systemic lupus erythematosus. Clin Exp Rheumatol 23:152–158PubMed Armstrong DJ, Whitehead EM, Crockard AD, Bell AL (2005) Distinctive effects of G-CSF, GM-CSF and TNFalpha on neutrophil apoptosis in systemic lupus erythematosus. Clin Exp Rheumatol 23:152–158PubMed
12.
go back to reference Perl A, Gergely P Jr, Banki K (2004) Mitochondrial dysfunction in T cells of patients with systemic lupus erythematosus. Int Rev Immunol 23:293–313PubMedCrossRef Perl A, Gergely P Jr, Banki K (2004) Mitochondrial dysfunction in T cells of patients with systemic lupus erythematosus. Int Rev Immunol 23:293–313PubMedCrossRef
13.
go back to reference Seki M, Ushiyama C, Seta N, Abe K, Fukazawa T, Asakawa J, Takasaki Y, Hashimoto H (1998) Apoptosis of lymphocytes induced by glucocorticoids and relationship to therapeutic efficacy in patients with systemic lupus erythematosus. Arthritis Rheum 41:823–830PubMedCrossRef Seki M, Ushiyama C, Seta N, Abe K, Fukazawa T, Asakawa J, Takasaki Y, Hashimoto H (1998) Apoptosis of lymphocytes induced by glucocorticoids and relationship to therapeutic efficacy in patients with systemic lupus erythematosus. Arthritis Rheum 41:823–830PubMedCrossRef
14.
go back to reference Wu J, Wilson J, He J, Xiang L, Schur PH, Mountz JD (1996) Fas ligand mutation in a patient with systemic lupus erythematosus and lymphoproliferative disease. J Clin Invest 98:1107–1113PubMed Wu J, Wilson J, He J, Xiang L, Schur PH, Mountz JD (1996) Fas ligand mutation in a patient with systemic lupus erythematosus and lymphoproliferative disease. J Clin Invest 98:1107–1113PubMed
15.
go back to reference McNally J, Yoo DH, Drappa J, Chu JL, Yagita H, Friedman SM, Elkon KB (1997) Fas ligand expression and function in systemic lupus erythematosus. J Immunol 159:4628–4636PubMed McNally J, Yoo DH, Drappa J, Chu JL, Yagita H, Friedman SM, Elkon KB (1997) Fas ligand expression and function in systemic lupus erythematosus. J Immunol 159:4628–4636PubMed
16.
go back to reference Mysler E, Bini P, Drappa J, Ramos P, Friedman SM, Krammer PH, Elkon KB (1994) The apoptosis-1/Fas protein in human systemic lupus erythematosus. J Clin Invest 93:1029–1034PubMedCrossRef Mysler E, Bini P, Drappa J, Ramos P, Friedman SM, Krammer PH, Elkon KB (1994) The apoptosis-1/Fas protein in human systemic lupus erythematosus. J Clin Invest 93:1029–1034PubMedCrossRef
17.
go back to reference Caricchio R, Cohen PL (1999) Spontaneous and induced apoptosis in systemic lupus erythematosus: multiple assays fail to reveal consistent abnormalities. Cell Immunol 198:54–60PubMedCrossRef Caricchio R, Cohen PL (1999) Spontaneous and induced apoptosis in systemic lupus erythematosus: multiple assays fail to reveal consistent abnormalities. Cell Immunol 198:54–60PubMedCrossRef
18.
go back to reference Rieux-Laucat F, LeDiest F, Hivrox C, Roberts IAG, Debatin KM, Fischer A, deVillartay JP (1995) Mutations in Fas associated with human lymphoproliferative syndrome and autoimmunity. Science 268:1347PubMed Rieux-Laucat F, LeDiest F, Hivrox C, Roberts IAG, Debatin KM, Fischer A, deVillartay JP (1995) Mutations in Fas associated with human lymphoproliferative syndrome and autoimmunity. Science 268:1347PubMed
19.
go back to reference Pitidhammabhorn D, Kantachuvesiri S, Totemchokchyakarn K, Kitiyanant Y, Ubol S (2006) Partial construction of apoptotic pathway in PBMC obtained from active SLE patients and the significance of plasma TNF-alpha on this pathway. Clin Rheumatol 25(5):705–714PubMedCrossRef Pitidhammabhorn D, Kantachuvesiri S, Totemchokchyakarn K, Kitiyanant Y, Ubol S (2006) Partial construction of apoptotic pathway in PBMC obtained from active SLE patients and the significance of plasma TNF-alpha on this pathway. Clin Rheumatol 25(5):705–714PubMedCrossRef
20.
go back to reference Napirei M, Gultekin A, Kloeckl T, Moroy T, Frostegard J, Mannherz HG (2006) Systemic lupus-erythematosus: deoxyribonuclease 1 in necrotic chromatin disposal. Int J Biochem Cell Biol 38:297–306PubMedCrossRef Napirei M, Gultekin A, Kloeckl T, Moroy T, Frostegard J, Mannherz HG (2006) Systemic lupus-erythematosus: deoxyribonuclease 1 in necrotic chromatin disposal. Int J Biochem Cell Biol 38:297–306PubMedCrossRef
21.
go back to reference Okabe Y, Kawane K, Akira S, Taniguchi T, Nagata S (2005) Toll-like receptor-independent gene induction program activated by mammalian DNA escaped from apoptotic DNA degradation. J Exp Med 202:1333–1339PubMedCrossRef Okabe Y, Kawane K, Akira S, Taniguchi T, Nagata S (2005) Toll-like receptor-independent gene induction program activated by mammalian DNA escaped from apoptotic DNA degradation. J Exp Med 202:1333–1339PubMedCrossRef
22.
go back to reference Lauber K, Blumenthal SG, Waibel M, Wesselborg S (2004) Clearance of apoptotic cells: getting rid of the corpses. Mol Cell 14:277–287PubMedCrossRef Lauber K, Blumenthal SG, Waibel M, Wesselborg S (2004) Clearance of apoptotic cells: getting rid of the corpses. Mol Cell 14:277–287PubMedCrossRef
23.
go back to reference Fadok VA, Bratton DL, Henson PM (2001) Phagocyte receptors for apoptotic cells: recognition, uptake, and consequences. J Clin Invest 108:957–962PubMedCrossRef Fadok VA, Bratton DL, Henson PM (2001) Phagocyte receptors for apoptotic cells: recognition, uptake, and consequences. J Clin Invest 108:957–962PubMedCrossRef
24.
go back to reference Caricchio R, McPhie L, Cohen PL (2003) Ultraviolet B radiation-induced cell death: critical role of ultraviolet dose in inflammation and lupus autoantigen redistribution. J Immunol 171:5778–5786PubMed Caricchio R, McPhie L, Cohen PL (2003) Ultraviolet B radiation-induced cell death: critical role of ultraviolet dose in inflammation and lupus autoantigen redistribution. J Immunol 171:5778–5786PubMed
25.
go back to reference Weston KM, Yeh ET, Sy MS (1987) Autoreactivity accelerates the development of autoimmunity and lymphoproliferation in MRL/Mp-lpr/lpr mice. J Clin Invest 139:734–742 Weston KM, Yeh ET, Sy MS (1987) Autoreactivity accelerates the development of autoimmunity and lymphoproliferation in MRL/Mp-lpr/lpr mice. J Clin Invest 139:734–742
26.
go back to reference Casciola-Rosen L, Rosen A (1997) Ultraviolet light-induced keratinocyte apoptosis: a potential mechanism for the induction of skin lesions and autoantibody production in LE. Lupus 6:175–180PubMed Casciola-Rosen L, Rosen A (1997) Ultraviolet light-induced keratinocyte apoptosis: a potential mechanism for the induction of skin lesions and autoantibody production in LE. Lupus 6:175–180PubMed
27.
go back to reference Casciola-Rosen L, Andrade F, Ulanet D, Wong WB, Rosen A (1999) Cleavage by granzyme B is strongly predictive of autoantigen status: implications for initiation of autoimmunity. J Exp Med 190:815–826PubMedCrossRef Casciola-Rosen L, Andrade F, Ulanet D, Wong WB, Rosen A (1999) Cleavage by granzyme B is strongly predictive of autoantigen status: implications for initiation of autoimmunity. J Exp Med 190:815–826PubMedCrossRef
28.
go back to reference Cline AM, Radic MZ (2004) Apoptosis, subcellular particles, and autoimmunity. Clin Immunol 112:175–182PubMedCrossRef Cline AM, Radic MZ (2004) Apoptosis, subcellular particles, and autoimmunity. Clin Immunol 112:175–182PubMedCrossRef
29.
go back to reference Hof D, Raats JM, Pruijn GJ (2005) Apoptotic modifications affect the autoreactivity of the U1 snRNP autoantigen. Autoimmun Rev 4:380–388PubMedCrossRef Hof D, Raats JM, Pruijn GJ (2005) Apoptotic modifications affect the autoreactivity of the U1 snRNP autoantigen. Autoimmun Rev 4:380–388PubMedCrossRef
30.
go back to reference Andrade F, Casciola-Rosen LA, Rosen A (2005) Generation of novel covalent RNA-protein complexes in cells by ultraviolet B irradiation: implications for autoimmunity. Arthritis Rheum 52:1160–1170PubMedCrossRef Andrade F, Casciola-Rosen LA, Rosen A (2005) Generation of novel covalent RNA-protein complexes in cells by ultraviolet B irradiation: implications for autoimmunity. Arthritis Rheum 52:1160–1170PubMedCrossRef
31.
32.
go back to reference Georgiev M, Agle LM, Chu JL, Elkon KB, Ashany D (2005) Mature dendritic cells readily break tolerance in normal mice but do not lead to disease expression. Arthritis Rheum 52:225–238PubMedCrossRef Georgiev M, Agle LM, Chu JL, Elkon KB, Ashany D (2005) Mature dendritic cells readily break tolerance in normal mice but do not lead to disease expression. Arthritis Rheum 52:225–238PubMedCrossRef
33.
go back to reference Ma L, Chan KW, Trendell-Smith NJ, Wu A, Tian L, Lam AC, Chan AK, Lo CK, Chik S, Ko KH, To CK, Kam SK, Li XS, Yang CH, Leung SY, Ng MH, Stott DI, MacPherson GG, Huang FP (2005) Systemic autoimmune disease induced by dendritic cells that have captured necrotic but not apoptotic cells in susceptible mouse strains. Eur J Immunol 35:3364–3375PubMedCrossRef Ma L, Chan KW, Trendell-Smith NJ, Wu A, Tian L, Lam AC, Chan AK, Lo CK, Chik S, Ko KH, To CK, Kam SK, Li XS, Yang CH, Leung SY, Ng MH, Stott DI, MacPherson GG, Huang FP (2005) Systemic autoimmune disease induced by dendritic cells that have captured necrotic but not apoptotic cells in susceptible mouse strains. Eur J Immunol 35:3364–3375PubMedCrossRef
34.
go back to reference Denny MF, Chandaroy P, Killen PD, Caricchio R, Lewis EE, Richardson BC, Lee KD, Gavalchin J, Kaplan MJ (2006) Accelerated macrophage apoptosis induces autoantibody formation and organ damage in systemic lupus erythematosus. J Immunol 176:2095–2104PubMed Denny MF, Chandaroy P, Killen PD, Caricchio R, Lewis EE, Richardson BC, Lee KD, Gavalchin J, Kaplan MJ (2006) Accelerated macrophage apoptosis induces autoantibody formation and organ damage in systemic lupus erythematosus. J Immunol 176:2095–2104PubMed
35.
go back to reference Rovere P, Sabbadini MG, Vallinoto C, Fascio U, Recigno M, Crosti M, Ricciardi-Castagnoli P, Balestrieri G, Tincani A, Manfredi AA (1999) Dendritic cell presentation of antigens from apoptotic cells in a proinflammatory context: role of opsonizing anti-beta2-glycoprotein I antibodies. Arthritis Rheum 42:1412–1420PubMedCrossRef Rovere P, Sabbadini MG, Vallinoto C, Fascio U, Recigno M, Crosti M, Ricciardi-Castagnoli P, Balestrieri G, Tincani A, Manfredi AA (1999) Dendritic cell presentation of antigens from apoptotic cells in a proinflammatory context: role of opsonizing anti-beta2-glycoprotein I antibodies. Arthritis Rheum 42:1412–1420PubMedCrossRef
36.
go back to reference Nauta AJ, Castellano G, Xu W, Woltman AM, Borrias MC, Daha MR, van Kooten C, Roos A (2004) Opsonization with C1q and mannose-binding lectin targets apoptotic cells to dendritic cells. J Immunol 173:3044–3050PubMed Nauta AJ, Castellano G, Xu W, Woltman AM, Borrias MC, Daha MR, van Kooten C, Roos A (2004) Opsonization with C1q and mannose-binding lectin targets apoptotic cells to dendritic cells. J Immunol 173:3044–3050PubMed
37.
go back to reference Williams JM, Colman R, Brookes CJ, Savage CO, Harper L (2005) Anti-endothelial cell antibodies from lupus patients bind to apoptotic endothelial cells promoting macrophage phagocytosis but do not induce apoptosis. Rheumatology (Oxford) 44:879–884CrossRef Williams JM, Colman R, Brookes CJ, Savage CO, Harper L (2005) Anti-endothelial cell antibodies from lupus patients bind to apoptotic endothelial cells promoting macrophage phagocytosis but do not induce apoptosis. Rheumatology (Oxford) 44:879–884CrossRef
38.
go back to reference Frisoni L, McPhie L, Colonna L, Sriram U, Monestier M, Gallucci S, Caricchio R (2005) Nuclear autoantigen translocation and autoantibody opsonization lead to increased dendritic cell phagocytosis and presentation of nuclear antigens: a novel pathogenic pathway for autoimmunity? J Immunol 175:2692–2701PubMed Frisoni L, McPhie L, Colonna L, Sriram U, Monestier M, Gallucci S, Caricchio R (2005) Nuclear autoantigen translocation and autoantibody opsonization lead to increased dendritic cell phagocytosis and presentation of nuclear antigens: a novel pathogenic pathway for autoimmunity? J Immunol 175:2692–2701PubMed
39.
go back to reference Shaw PX, Goodyear CS, Chang MK, Witztum JL, Silverman GJ (2003) The autoreactivity of anti-phosphorylcholine antibodies for atherosclerosis-associated neo-antigens and apoptotic cells. J Immunol 170:6151–6157PubMed Shaw PX, Goodyear CS, Chang MK, Witztum JL, Silverman GJ (2003) The autoreactivity of anti-phosphorylcholine antibodies for atherosclerosis-associated neo-antigens and apoptotic cells. J Immunol 170:6151–6157PubMed
40.
go back to reference Chang MK, Binder CJ, Miller YI, Subbanagounder G, Silverman GJ, Berliner JA, Witztum JL (2004) Apoptotic cells with oxidation-specific epitopes are immunogenic and proinflammatory. J Exp Med 200:1359–1370PubMedCrossRef Chang MK, Binder CJ, Miller YI, Subbanagounder G, Silverman GJ, Berliner JA, Witztum JL (2004) Apoptotic cells with oxidation-specific epitopes are immunogenic and proinflammatory. J Exp Med 200:1359–1370PubMedCrossRef
41.
go back to reference Shaw PX, Horkko S, Tsimikas S, Chang MK, Palinski W, Silverman GJ, Chen PP, Witztum JL (2001) Human-derived anti-oxidized LDL autoantibody blocks uptake of oxidized LDL by macrophages and localizes to atherosclerotic lesions in vivo. Arterioscler Thromb Vasc Biol 21:1333–1339PubMed Shaw PX, Horkko S, Tsimikas S, Chang MK, Palinski W, Silverman GJ, Chen PP, Witztum JL (2001) Human-derived anti-oxidized LDL autoantibody blocks uptake of oxidized LDL by macrophages and localizes to atherosclerotic lesions in vivo. Arterioscler Thromb Vasc Biol 21:1333–1339PubMed
42.
go back to reference Paul E, Carroll MC (1999) SAP-less chromatin triggers systemic lupus erythematosus. Nat Med 5:607–608PubMedCrossRef Paul E, Carroll MC (1999) SAP-less chromatin triggers systemic lupus erythematosus. Nat Med 5:607–608PubMedCrossRef
43.
go back to reference Botto M, Dell’Agnola C, Bygrave AE, Thompson EM, Cook HT, Petry F, Loos M, Pandolfi PP, Walport MJ (1998) Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet 19:56–59PubMedCrossRef Botto M, Dell’Agnola C, Bygrave AE, Thompson EM, Cook HT, Petry F, Loos M, Pandolfi PP, Walport MJ (1998) Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet 19:56–59PubMedCrossRef
44.
go back to reference Prodeus AP, Goerg S, Shen LM, Pozdnyakova OO, Chu L, Alicot EM, Goodnow CC, Carroll MC (1998) A critical role for complement in maintenance of self-tolerance. Immunity 9:721–731PubMedCrossRef Prodeus AP, Goerg S, Shen LM, Pozdnyakova OO, Chu L, Alicot EM, Goodnow CC, Carroll MC (1998) A critical role for complement in maintenance of self-tolerance. Immunity 9:721–731PubMedCrossRef
45.
go back to reference Kim SJ, Gershov D, Ma X, Brot N, Elkon KB (2003) Opsonization of apoptotic cells and its effect on macrophage and T cell immune responses. Ann N Y Acad Sci 987:68–78PubMedCrossRef Kim SJ, Gershov D, Ma X, Brot N, Elkon KB (2003) Opsonization of apoptotic cells and its effect on macrophage and T cell immune responses. Ann N Y Acad Sci 987:68–78PubMedCrossRef
46.
go back to reference Limburg PC, Bijl M (2005) Autoantibodies to opsonins of apoptotic cells in systemic lupus erythematosus. Ann Rheum Dis 64:1669–1670PubMedCrossRef Limburg PC, Bijl M (2005) Autoantibodies to opsonins of apoptotic cells in systemic lupus erythematosus. Ann Rheum Dis 64:1669–1670PubMedCrossRef
47.
go back to reference Leadbetter EA, Rifkin IR, Hohlbaum AM, Beaudette BC, Shlomchik MJ, Marshak-Rothstein A (2002) Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416:603–607PubMedCrossRef Leadbetter EA, Rifkin IR, Hohlbaum AM, Beaudette BC, Shlomchik MJ, Marshak-Rothstein A (2002) Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416:603–607PubMedCrossRef
48.
go back to reference Boule MW, Broughton C, Mackay F, Akira S, Marshak-Rothstein A, Rifkin IR (2004) Toll-like receptor 9-dependent and -independent dendritic cell activation by chromatin-immunoglobulin G complexes. J Exp Med 199:1631–1640PubMedCrossRef Boule MW, Broughton C, Mackay F, Akira S, Marshak-Rothstein A, Rifkin IR (2004) Toll-like receptor 9-dependent and -independent dendritic cell activation by chromatin-immunoglobulin G complexes. J Exp Med 199:1631–1640PubMedCrossRef
49.
go back to reference Blander JM, Medzhitov R (2006) Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature 440:808–812PubMedCrossRef Blander JM, Medzhitov R (2006) Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature 440:808–812PubMedCrossRef
50.
go back to reference Hanayama R, Tanaka M, Miyasaka K, Aozasa K, Koike M, Uchiyama Y, Nagata S (2004) Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science 304:1147–1150PubMedCrossRef Hanayama R, Tanaka M, Miyasaka K, Aozasa K, Koike M, Uchiyama Y, Nagata S (2004) Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science 304:1147–1150PubMedCrossRef
51.
go back to reference Asano K, Miwa M, Miwa K, Hanayama R, Nagase H, Nagata S, Tanaka M (2004) Masking of phosphatidylserine inhibits apoptotic cell engulfment and induces autoantibody production in mice. J Exp Med 200:459–467PubMedCrossRef Asano K, Miwa M, Miwa K, Hanayama R, Nagase H, Nagata S, Tanaka M (2004) Masking of phosphatidylserine inhibits apoptotic cell engulfment and induces autoantibody production in mice. J Exp Med 200:459–467PubMedCrossRef
52.
go back to reference Cohen PL, Caricchio R, Abraham V, Camenisch T, Jennette JC, Roubey RAS, Earp HS, Matsushima G, Reap EA (2002) Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J Exp Med 196:1CrossRef Cohen PL, Caricchio R, Abraham V, Camenisch T, Jennette JC, Roubey RAS, Earp HS, Matsushima G, Reap EA (2002) Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J Exp Med 196:1CrossRef
53.
go back to reference Lu Q, Lemke G (2001) Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family. Science 293:306–311PubMedCrossRef Lu Q, Lemke G (2001) Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family. Science 293:306–311PubMedCrossRef
54.
go back to reference Radic MZ, Shah K, Zhang W, Lu Q, Lemke G, Hilliard GM (2006) Heterogeneous nuclear ribonucleoprotein P2 is an autoantibody target in mice deficient for Mer, Axl, and Tyro3 receptor tyrosine kinases. J Immunol 176:68–74PubMed Radic MZ, Shah K, Zhang W, Lu Q, Lemke G, Hilliard GM (2006) Heterogeneous nuclear ribonucleoprotein P2 is an autoantibody target in mice deficient for Mer, Axl, and Tyro3 receptor tyrosine kinases. J Immunol 176:68–74PubMed
55.
go back to reference Camenisch TD, Koller BH, Earp HS, Matsushima GK (1999) A novel receptor tyrosine kinase, Mer, inhibits TNF-alpha production and lipopolysaccharide-induced endotoxic shock. J Immunol 162:3498–3503PubMed Camenisch TD, Koller BH, Earp HS, Matsushima GK (1999) A novel receptor tyrosine kinase, Mer, inhibits TNF-alpha production and lipopolysaccharide-induced endotoxic shock. J Immunol 162:3498–3503PubMed
56.
go back to reference Ren Y, Tang J, Mok MY, Chan AW, Wu A, Lau CS (2003) Increased apoptotic neutrophils and macrophages and impaired macrophage phagocytic clearance of apoptotic neutrophils in systemic lupus erythematosus. Arthritis Rheum 48:2888–2897PubMedCrossRef Ren Y, Tang J, Mok MY, Chan AW, Wu A, Lau CS (2003) Increased apoptotic neutrophils and macrophages and impaired macrophage phagocytic clearance of apoptotic neutrophils in systemic lupus erythematosus. Arthritis Rheum 48:2888–2897PubMedCrossRef
57.
go back to reference Kimberly RP (1991) Of mice and men: insights into the complexity of mononuclear phagocyte system blockade provided by autoimmune mouse strains. J Lab Clin Med 117:173–174PubMed Kimberly RP (1991) Of mice and men: insights into the complexity of mononuclear phagocyte system blockade provided by autoimmune mouse strains. J Lab Clin Med 117:173–174PubMed
58.
go back to reference Tas SW, Quartier P, Botto M, Fossati-Jimack L (2006) Macrophages from patients with SLE and rheumatoid arthritis have defective adhesion in vitro, while only SLE macrophages have impaired uptake of apoptotic cells. Ann Rheum Dis 65:216–221PubMedCrossRef Tas SW, Quartier P, Botto M, Fossati-Jimack L (2006) Macrophages from patients with SLE and rheumatoid arthritis have defective adhesion in vitro, while only SLE macrophages have impaired uptake of apoptotic cells. Ann Rheum Dis 65:216–221PubMedCrossRef
59.
go back to reference Baumann I, Kolowos W, Voll RE, Manger B, Gaipl U, Neuhuber WL, Kirchner T, Kalden JR, Herrmann M (2002) Impaired uptake of apoptotic cells into tingible body macrophages in germinal centers of patients with systemic lupus erythematosus. Arthritis Rheum 46:191–201PubMedCrossRef Baumann I, Kolowos W, Voll RE, Manger B, Gaipl U, Neuhuber WL, Kirchner T, Kalden JR, Herrmann M (2002) Impaired uptake of apoptotic cells into tingible body macrophages in germinal centers of patients with systemic lupus erythematosus. Arthritis Rheum 46:191–201PubMedCrossRef
60.
go back to reference Gaipl US, Voll RE, Sheriff A, Franz S, Kalden JR, Herrmann M (2005) Impaired clearance of dying cells in systemic lupus erythematosus. Autoimmun Rev 4:189–194PubMedCrossRef Gaipl US, Voll RE, Sheriff A, Franz S, Kalden JR, Herrmann M (2005) Impaired clearance of dying cells in systemic lupus erythematosus. Autoimmun Rev 4:189–194PubMedCrossRef
61.
go back to reference Kuhn A, Herrmann M, Kleber S, Beckmann-Welle M, Fehsel K, Martin-Villalba A, Lehmann P, Ruzicka T, Krammer PH, Kolb-Bachofen V (2006) Accumulation of apoptotic cells in the epidermis of patients with cutaneous lupus erythematosus after ultraviolet irradiation. Arthritis Rheum 54:939–950PubMedCrossRef Kuhn A, Herrmann M, Kleber S, Beckmann-Welle M, Fehsel K, Martin-Villalba A, Lehmann P, Ruzicka T, Krammer PH, Kolb-Bachofen V (2006) Accumulation of apoptotic cells in the epidermis of patients with cutaneous lupus erythematosus after ultraviolet irradiation. Arthritis Rheum 54:939–950PubMedCrossRef
62.
go back to reference Reefman E, Kuiper H, Jonkman MF, Limburg PC, Kallenberg CG, Bijl M (2006) Skin sensitivity to UVB irradiation in systemic lupus erythematosus is not related to the level of apoptosis induction in keratinocytes. Rheumatology (Oxford) 45:538–544CrossRef Reefman E, Kuiper H, Jonkman MF, Limburg PC, Kallenberg CG, Bijl M (2006) Skin sensitivity to UVB irradiation in systemic lupus erythematosus is not related to the level of apoptosis induction in keratinocytes. Rheumatology (Oxford) 45:538–544CrossRef
63.
go back to reference Bijl M, Reefman E, Horst G, Limburg PC, Kallenberg CG (2006) Reduced uptake of apoptotic cells by macrophages in systemic lupus erythematosus: correlates with decreased serum levels of complement. Ann Rheum Dis 65:57–63PubMedCrossRef Bijl M, Reefman E, Horst G, Limburg PC, Kallenberg CG (2006) Reduced uptake of apoptotic cells by macrophages in systemic lupus erythematosus: correlates with decreased serum levels of complement. Ann Rheum Dis 65:57–63PubMedCrossRef
64.
go back to reference Jin O, Sun LY, Zhou KX, Zhang XS, Feng XB, Mok MY, Lau CS (2005) Lymphocyte apoptosis and macrophage function: correlation with disease activity in systemic lupus erythematosus. Clin Rheumatol 24:107–110PubMedCrossRef Jin O, Sun LY, Zhou KX, Zhang XS, Feng XB, Mok MY, Lau CS (2005) Lymphocyte apoptosis and macrophage function: correlation with disease activity in systemic lupus erythematosus. Clin Rheumatol 24:107–110PubMedCrossRef
65.
go back to reference Ablin J, Verbovetski I, Trahtemberg U, Metzger S, Mevorach D (2005) Quinidine and procainamide inhibit murine macrophage uptake of apoptotic and necrotic cells: a novel contributing mechanism of drug-induced-lupus. Apoptosis 10:1009–1018PubMedCrossRef Ablin J, Verbovetski I, Trahtemberg U, Metzger S, Mevorach D (2005) Quinidine and procainamide inhibit murine macrophage uptake of apoptotic and necrotic cells: a novel contributing mechanism of drug-induced-lupus. Apoptosis 10:1009–1018PubMedCrossRef
66.
go back to reference Buyon JP, Clancy RM (2003) From antibody insult to fibrosis in neonatal lupus—the heart of the matter. Arthritis Res Ther 5:266–270PubMedCrossRef Buyon JP, Clancy RM (2003) From antibody insult to fibrosis in neonatal lupus—the heart of the matter. Arthritis Res Ther 5:266–270PubMedCrossRef
67.
go back to reference Rodriguez W, Mold C, Marnell LL, Hutt J, Silverman GJ, Tran D, Du Clos TW (2006) Prevention and reversal of nephritis in MRL/lpr mice with a single injection of C-reactive protein. Arthritis Rheum 54:325–335PubMedCrossRef Rodriguez W, Mold C, Marnell LL, Hutt J, Silverman GJ, Tran D, Du Clos TW (2006) Prevention and reversal of nephritis in MRL/lpr mice with a single injection of C-reactive protein. Arthritis Rheum 54:325–335PubMedCrossRef
68.
go back to reference Seery JP, Cattell V, Watt FM (2001) Cutting edge: amelioration of kidney disease in a transgenic mouse model of lupus nephritis by administration of the caspase inhibitor carbobenzoxy-valyl-alanyl-aspartyl-(beta-o-methyl)-fluoromethylketone. J Immunol 167:2452–2455PubMed Seery JP, Cattell V, Watt FM (2001) Cutting edge: amelioration of kidney disease in a transgenic mouse model of lupus nephritis by administration of the caspase inhibitor carbobenzoxy-valyl-alanyl-aspartyl-(beta-o-methyl)-fluoromethylketone. J Immunol 167:2452–2455PubMed
Metadata
Title
Apoptotic cell death and lupus
Author
Philip L. Cohen
Publication date
01-10-2006
Publisher
Springer-Verlag
Published in
Seminars in Immunopathology / Issue 2/2006
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-006-0038-z

Other articles of this Issue 2/2006

Seminars in Immunopathology 2/2006 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.