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Clearance deficiency and systemic lupus erythematosus (SLE)
Abstract
Systemic lupus erythematosus (SLE) is a fairly heterogeneous autoimmune disease. Impaired clearance functions for dying cells may explain accumulation of nuclear autoantigens in various tissues of SLE patients. Our data show that in a subgroup of patients with SLE, apoptotic cells accumulated in the germinal centres of the lymph nodes. Apoptotic material was attached to the surfaces of follicular dendritic cells. Furthermore, we found an accumulation of apoptotic cells in the skin of patients with cutaneous lupus after UV exposure. Granulocytes and monocytes in whole blood of SLE patients showed a reduced uptake of albumin- and polyglobin-coated beads. Furthermore, we analysed sera from SLE patients in migration assays and observed that the attraction signals for macrophages were reduced by sera of approximately 25% of the SLE patients. Analyses of high-affinity DNA binding IgG autoantibodies of SLE patients revealed that those antibodies had gained their DNA reactivity in a germinal centre reaction. We suggest a stepwise maturation from a non-anti-DNA reactive B cell to an anti-dsDNA autoreactive B cell. We conclude that impaired clearance in early phases of apoptosis leads to a secondary necrotic status of the cells. Danger signals are released; modified autoantigens are accessible, favouring an autoimmune reaction.
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“DAMPs are released from dying cells and induce immune responses to cellular antigens whether the cell is a tumor cell, autologous tissue or infected with a pathogen.”
From Immunogenic and tolerogenic cell death (2009) · cites this paper as [4]
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“Similar considerations pertain to the role played by other proteins such as C-reactive protein and IgM, where deficiency may lead to impaired clearance and enhanced autoreactivty [ 15 ].”
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BackgroundMoonlighting osteoclasts as undertakers of apoptotic cells
Steffen, U., Keppeler, H., Ipseiz, N., Derer, A., Poller, K., Aigner, M., Schett, G. A., i, M. H., & Lauber, K. (2012) · Autoimmunity · doi:10.3109/08916934.2012.719950 · Cited by 68
“As a consequence, deficiencies in the clearance of apoptotic cells and the concomitant accumulation of secondary necrotic material are known to be associated with systemic lupus erythematosus (SLE), a severe systemic autoimmune disease [1-3].”
BackgroundSelf-citationRecarte-Pelz, P., Tàssies, D., Espinosa, G., Hurtado, B., Sala, N., Cervera, R., Reverter, J. C., & de Frutos, P. G. (2013) · Arthritis Research & Therapy · doi:10.1186/ar4199 · Cited by 69
“Presence of apoptotic cells in lymphatic tissue and decreased engulfment of apoptotic cells by macrophages and dendritic cells have been reported in SLE patients [42,43].”
BackgroundInteraction between glutathione and apoptosis in systemic lupus erythematosus
Shah, D., Sah, S., & Nath, S. K. (2012) · Autoimmunity Reviews · doi:10.1016/j.autrev.2012.12.007 · Cited by 67
“This is based on observations of excessive apoptosis of T and B lymphocytes and on defective clearance of apoptotic cells in patients with SLE [4,101].”
Apoptotic cell fragments locally activate tingible body macrophages in the germinal center
Grootveld, A. K., Kyaw, W., Panova, V., Lau, A. W. Y., Ashwin, E., Seuzaret, G., Dhenni, R., Bhattacharyya, N. D., Khoo, W. H., Biro, M., et al. (2023) · Cell · doi:10.1016/j.cell.2023.02.004 · Cited by 74
Xia, C., Campbell, K. A., & Clare-Salzler, M. J. (2009) · Current Opinion in Organ Transplantation · doi:10.1097/mot.0b013e32832ce943 · Cited by 66
Microvesicles in Autoimmune Diseases
Liu, M., Williams, K. J., & Werth, V. P. (2016) · Advances in clinical chemistry · doi:10.1016/bs.acc.2016.06.005 · Cited by 68
Wittmann, M., Macdonald, A., & Renne, J. (2009) · Autoimmunity Reviews · doi:10.1016/j.autrev.2009.03.003 · Cited by 62
Seredkina, N., Zykova, S. N., & Rekvig, O. P. (2009) · American Journal Of Pathology · doi:10.2353/ajpath.2009.080943 · Cited by 61
Tsai, P., Ka, S., Chang, J., Lai, J., Dai, M., Jheng, H.-L., Kuo, M.-T., Chen, P., & Chen, A. (2011) · Arthritis & Rheumatism · doi:10.1002/art.33328 · Cited by 61
Infection and apoptosis as a combined inflammatory trigger
Torchinsky, M. B., Garaude, J., & Blander, J. M. (2010) · Current Opinion in Immunology · doi:10.1016/j.coi.2010.01.003 · Cited by 60
“Defects in clearance of apoptotic cells can lead to their accumulation and progression into secondary necrosis, a type of death that is inflammatory in nature with dire consequences to the host manifested by autoimmune disease such as systemic lupus erythematosus (SLE) [2 ,3].”
BackgroundDendritic Cell-Mediated Phagocytosis but Not Immune Activation Is Enhanced by Plasmin
Borg, R. J., Samson, A. L., Au, A. E., Scholzen, A., Fuchsberger, M., Kong, Y., Freeman, R., Mifsud, N. A., Plebanski, M., & Medcalf, R. L. (2015) · PLoS ONE · doi:10.1371/journal.pone.0131216 · Cited by 58
Requirements for innate immune pathways in environmentally induced autoimmunity
Pollard, K. M., & Kono, D. H. (2013) · BMC Medicine · doi:10.1186/1741-7015-11-100 · Cited by 57
“tions suggest that scavenger receptor-mediated uptake of silica and subsequent macrophage cell death may adversely affect clearance of dead and dying cells, which, in turn, could impact self-tolerance [158,159] and promote autoimmunity.”
BackgroundGerl, V., Lischka, A., Panne, D., Großmann, P., Berthold, R., Hoyer, B. F., Biesen, R., Bruns, A., Alexander, T., Jacobi, A. M., et al. (2009) · Annals of the Rheumatic Diseases · doi:10.1136/ard.2009.111021 · Cited by 55
“The low overall migratory capacity of SLE monocytes could result in lower numbers of monocyte-derived DCs and macrophages at inflammatory sites, promoting the accumulation of apoptotic material, as observed in germinal centres of lymph nodes of patients with SLE.”
BackgroundBacteria-induced phagocyte secondary necrosis as a pathogenicity mechanism
Silva, M. T. (2010) · Journal of Leukocyte Biology · doi:10.1189/jlb.0410205 · Cited by 55
The Exonuclease Trex1 Restrains Macrophage Proinflammatory Activation
Pereira‐Lopes, S., Celhar, T., Sans-Fons, G., Serra, M., Fairhurst, A., Lloberas, J., & Celada, A. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1301603 · Cited by 57
Yoo, E. J., Oh, K., Piao, H., Kang, H. J., Jeong, G. W., Park, H., Lee, C. J., Ryu, H., Yang, S. H., Kim, M.-G., et al. (2023) · Kidney International · doi:10.1016/j.kint.2023.03.030 · Cited by 51
Influence of Atg5 Mutation in SLE Depends on Functional IL-10 Genotype
López, P., Alonso‐Perez, E., Rodríguez‐Carrio, J., & Suárez, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078756 · Cited by 52
“Among them, the increased apoptosis rate and the impaired clearance of apoptotic bodies [4,5] may cause harmful effects, since they provide a source of autoantigens to elicit the autoimmune response [6].”
Cellular Regulation of the Inflammatory Response
Janssen, W. J., & Henson, P. M. (2011) · Toxicologic Pathology · doi:10.1177/0192623311428477 · Cited by 53
“…in apoptotic clearance mechanisms have been widely demonstrated in autoimmune diseases, such as systemic lupus erythematosus (Ren et al. 2003; Gaipl et al. 2005, 2007; Baumann et al. 2002; Herrmann et al. 1998) where increased numbers of apoptotic cells can be detected in the circulation…”
BackgroundSilica-Triggered Autoimmunity in Lupus-Prone Mice Blocked by Docosahexaenoic Acid Consumption
Bates, M. A., Brandenberger, C., Langohr, I. M., Kumagai, K., Lock, A. L., Harkema, J. R., Holian, A., & Pestka, J. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0160622 · Cited by 53
Majai, G. E., Kiss, E. V., Tarr, T., Zahuczky, G., Hartman, Z. C., Szegedi, G. Y., & Fésüs, L. (2013) · Lupus · doi:10.1177/0961203313511557 · Cited by 49
Systemic Lupus Erythematosus and DNA Degradation and Elimination Defects
Arneth, B. M. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01697 · Cited by 49
“The impaired clearance of apoptotic cells in SLE is due to their failed recognition by phagocytes because (a) the phagocytes are smaller (4), (b) the phagocytes have diminished and delayed phagocytic activity (46), (c) the phagocytes have reduced adherence (47), or (d) the differentiation of phagocytes from CD34-posit…”
BackgroundMunoz, L. E., Peter, C., i, M. H., Wesselborg, S., & Lauber, K. (2009) · Autoimmunity Reviews · doi:10.1016/j.autrev.2009.11.016 · Cited by 52
Self-citationPeripheral B cell abnormalities and disease activity in systemic lupus erythematosus
Hostmann, A., Jacobi, A., Mei, H. E., Hiepe, F., & Dörner, T. (2008) · Lupus · doi:10.1177/0961203308095138 · Cited by 48
Marée, A. F. M., Komba, M., Finegood, D. T., & Leah Edelstein-keshet, A. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00514.2007 · Cited by 48
Khan, T. N., Wong, E. B., Soni, C., & Rahman, Z. S. M. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1200824 · Cited by 48
He, X., Ding, Y., Xiang, W., & Dang, X. (2016) · Cellular Physiology and Biochemistry · doi:10.1159/000453135 · Cited by 48
Dörner, T., & Lipsky, P. E. (2013) · Current Opinion in Rheumatology · doi:10.1097/bor.0000000000000000 · Cited by 48
“These results strongly indicate that despite many check-point abnormalities in autoimmune diseases [8], the essential break in B-cell tolerance may occur in the periphery by abnormal selection in the germinal centre [9].”
ResultApoptotic molecular mechanisms implicated in autoimmune diseases.
Cacciapaglia, F., Spadaccio, C., Chello, M., Gigante, A., Coccia, R., Afeltra, A., & Amoroso, A. (2009) · PubMed · Cited by 46
Bone marrow transplantation, refractory autoimmunity and the contributions of Susumu Ikehara
Gershwin, M. E. (2008) · Journal of Autoimmunity · doi:10.1016/j.jaut.2007.12.006 · Cited by 46
Monsiváis-Urenda, A. E., Niño-Moreno, P., Abud‐Mendoza, C., Baranda, L., Layseca‐Espinosa, E., López‐Botet, M., & González‐Amaro, R. (2007) · Journal of Autoimmunity · doi:10.1016/j.jaut.2007.05.003 · Cited by 44
Chen, J., Zhao, Y., & Liu, Y. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00656 · Cited by 45
“For example, deregulated apoptosis and insufficient removal of apoptotic cells leads to the release of modified chromatin into the circulation and activation of antigen-presenting cells, which play an important role in the pathogenesis of systemic lupus erythematosus (61, 63).”
Background
Metadata
- Authors
- Gaipl, U. S., Munoz, L. E., Grossmayer, G., Lauber, K., Franz, S., Sarter, K., Voll, R. E., Winkler, T., Kuhn, A., Kalden, J., Kern, P., & Herrmann, M.
- Affiliations
- Friedrich-Alexander-Universität Erlangen-Nürnberg (DE)
- University of Tübingen (DE)
- Heinrich Heine University Düsseldorf (DE)
- ORCID
- Venue
- Journal of Autoimmunity
- Publisher
- Elsevier BV
- Published
- 2007-03
- Volume
- 28
- Issue
- 2-3
- Pages
- 114-121
- ISSN
- 0896-8411 (ISSN-L)
- OpenAlex
- W2021273693
- Cited by
- 277
- References
- 56
- Citations by year
- 2026: 6 · 2025: 2 · 2024: 6 · 2023: 6 · 2022: 6 · 2021: 8 · 2020: 10 · 2019: 12 · 2018: 11 · 2017: 18 · 2016: 14 · 2015: 18 · 2014: 25 · 2013: 21 · 2012: 19
- FWCI
- 18.12
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Autoimmunity (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Rheumatology › Systemic Lupus Erythematosus Research
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Health Sciences › Medicine › Rheumatology › Systemic Sclerosis and Related Diseases
- Keywords
- systemic lupus erythematosus, efferocytosis, germinal center, follicular dendritic cells, cutaneous lupus erythematosus, UV-induced apoptosis, macrophage migration, anti-dsDNA antibodies, B cell maturation, damage-associated molecular patterns, nuclear autoantigens, secondary necrosis
- MeSH terms
- B-Lymphocytes, Humans, Immunohistochemistry, Lupus Erythematosus, Cutaneous, Lupus Erythematosus, Systemic, Macrophages, Monocytes, Phagocytosis, Apoptosis, Models, Immunological, Germinal Center, In Situ Nick-End Labeling
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