Cited by 992Phagocytosis and Immune RegulationSystemic Lupus Erythematosus ResearchLiver Diseases and Immunity

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Autoimmune Disease and Impaired Uptake of Apoptotic Cells in MFG-E8-Deficient Mice

Hanayama, Rikinari, Tanaka, Masato, Miyasaka, Kay, Aozasa, Katsuyuki, Koike, Masato, Uchiyama, Yasuo, Nagata, Shigekazu·2004·Science

DOI 10.1126/science.1094359

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Abstract

Apoptotic cells expose phosphatidylserine and are swiftly engulfed by macrophages. Milk fat globule epidermal growth factor (EGF) factor 8 (MFG-E8) is a protein that binds to apoptotic cells by recognizing phosphatidylserine and that enhances the engulfment of apoptotic cells by macrophages. We report that tingible body macrophages in the germinal centers of the spleen and lymph nodes strongly express MFG-E8. Many apoptotic lymphocytes were found on the MFG-E8 –/– tingible body macrophages, but they were not efficiently engulfed. The MFG-E8 –/– mice developed splenomegaly, with the formation of numerous germinal centers, and suffered from glomerulonephritis as a result of autoantibody production. These data demonstrate that MFG-E8 has a critical role in removing apoptotic B cells in the germinal centers and that its failure can lead to autoimmune diseases.

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Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages
Fadok, V. A., Voelker, D. R., Campbell, P. A., Cohen, J., Bratton, D. L., & Henson, P. M. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.148.7.2207 · Cited by 3,321
Programmed Cell Death in Animal Development
Jacobson, M. D., Weil, M., & RAFF, M. C. (1997) · Cell · doi:10.1016/s0092-8674(00)81873-5 · Cited by 2,685
A blast from the past: clearance of apoptotic cells regulates immune responses
Savill, J., Dransfield, I., Gregory, C. D., & Haslett, C. (2002) · Nature reviews. Immunology · doi:10.1038/nri957 · Cited by 1,574
Corpse clearance defines the meaning of cell death
Savill, J., & Fadok, V. A. (2000) · Nature · doi:10.1038/35037722 · Cited by 1,572
Identification of a factor that links apoptotic cells to phagocytes
Hanayama, R., Tanaka, M., Miwa, K., Shinohara, A., Iwamatsu, A., & Nagata, S. (2002) · Nature · doi:10.1038/417182a · Cited by 1,401
Self-citation
Phagocytosis and clearance of apoptotic cells is mediated by MER
Scott, R. S., McMahon, E. J., Pop, S. M., Reap, E. A., Caricchio, R., Cohen, P. L., Earp, H. S., & Matsushima, G. K. (2001) · Nature · doi:10.1038/35075603 · Cited by 1,215
T-cell apoptosis detected in situ during positive and negative selection in the thymus
Surh, C. D., & Sprent, J. (1994) · Nature · doi:10.1038/372100a0 · Cited by 1,082
Systemic Exposure to Irradiated Apoptotic Cells Induces Autoantibody Production
Mevorach, D., Zhou, J. L., Song, X., & Elkon, K. B. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.188.2.387 · Cited by 567
Phosphatidylserine (PS) induces PS receptor–mediated macropinocytosis and promotes clearance of apoptotic cells
Hoffmann, P. R., deCathelineau, A. M., Ogden, C. A., Leverrier, Y., Bratton, D. L., Daleke, D. L., Ridley, A. J., Fadok, V. A., & Henson, P. M. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200108080 · Cited by 541
cDNA cloning of a mouse mammary epithelial cell surface protein reveals the existence of epidermal growth factor-like domains linked to factor VIII-like sequences.
Stubbs, J. D., Lekutis, C., Singer, K. L., Bui, A., Yuzuki, D., Srinivasan, U., & Parry, G. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.21.8417 · Cited by 313

Show all 24 references

Research works printed but not linked: 3

G. Kraal, M. Janse, Immunology58, 665 (1986).
V. J. Gauthier, C. K. Abrass, Semin. Nephrol.12, 379 (1992).
G. Kelsoe, Immunity4, 107 (1996).

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Larsson, A., Peng, S., Persson, H., Rosenbloom, J., Abrams, W. R., Wassberg, E., Thelin, S., Sletten, K., Gerwins, P., & Westermark, P. (2006) · Amyloid · doi:10.1080/13506120600722530 · Cited by 50
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Hinterseher, I., Erdman, R., Elmore, J. R., Stahl, E. C., Pahl, M. C., Derr, K., Golden, A. M., Lillvis, J. H., Cindric, M. C., Jackson, K., et al. (2012) · Pathobiology · doi:10.1159/000339303 · Cited by 55
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Atkin‐Smith, G. K., Miles, M. A., Tixeira, R., Lay, F. T., Duan, M., Hawkins, C. J., Phan, T. K., Paone, S., Mathivanan, S., Hulett, M. D., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.10.014 · Cited by 55
GRK6 deficiency in mice causes autoimmune disease due to impaired apoptotic cell clearance
Nakaya, M., Tajima, M., Kosako, H., Nakaya, T., Hashimoto, A. S., Watari, K., Nishihara, H., Ohba, M., Komiya, S., Tani, N., et al. (2013) · Nature Communications · doi:10.1038/ncomms2540 · Cited by 54
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Qiu, P., Zhou, J., Zhang, J., Dong, Y., & Liu, Y. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.671164 · Cited by 54
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Identification of MFG-E8 as a novel therapeutic target for diseases
Li, B., Zhang, H.-Y., Pan, H., & Ye, D. (2013) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2013.829455 · Cited by 53
Recombinant Milk Fat Globule–EGF Factor-8 Reduces Oxidative Stress via Integrin β3/Nuclear Factor Erythroid 2–Related Factor 2/Heme Oxygenase Pathway in Subarachnoid Hemorrhage Rats
Liu, F., Hu, Q., Li, B., Manaenko, A., Chen, Y., Tang, J., Guo, Z., Tang, J., & Zhang, J. H. (2014) · Stroke · doi:10.1161/strokeaha.114.006635 · Cited by 53
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Schaller, M. M., Bigler, C., Danner, D., Ditzel, H. J., & Trendelenburg, M. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0902642 · Cited by 53
Milk fat globule-EGF factor 8 suppresses the aberrant immune response of systemic lupus erythematosus-derived neutrophils and associated tissue damage
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Levine, J. S., Subang, R., Nasr, S. H., Fournier, S., Lajoie, G., Wither, J., & Rauch, J. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.9.6504 · Cited by 51
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Liu, F., Chen, Y., Hu, Q., Li, B., Tang, J., He, Y., Guo, Z., Feng, H., Tang, J., & Zhang, J. H. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.04.016 · Cited by 51
Retracted
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Li, E., Noda, M., Doi, Y., Parajuli, B., Kawanokuchi, J., Sonobe, Y., Takeuchi, H., Mizuno, T., & Suzumura, A. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-148 · Cited by 54
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Janssen, W. J., & Henson, P. M. (2011) · Toxicologic Pathology · doi:10.1177/0192623311428477 · Cited by 53
Pneumococcal Extracellular Vesicles Modulate Host Immunity
Yerneni, S. S., Werner, S., Azambuja, J. H., Ludwig, N., Eutsey, R. A., Aggarwal, S. D., Lucas, P. C., Bailey, N. G., Whiteside, T. L., Campbell, P. G., et al. (2021) · mBio · doi:10.1128/mbio.01657-21 · Cited by 50
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Xie, R., Gao, C., Li, W., Zhu, J., Novakovic, V. A., Wang, J., Ma, R., Zhou, J., Gilbert, G. E., & Shi, J. (2011) · Blood · doi:10.1182/blood-2011-06-362186 · Cited by 50
Mechanisms of fertilization elucidated by gene-manipulated animals
Okabe, M. (2015) · Asian Journal of Andrology · doi:10.4103/1008-682x.153299 · Cited by 50
Cell surface-expressed phosphatidylserine as therapeutic target to enhance phagocytosis of apoptotic cells
Schutters, K., Kusters, D. H. M., Chatrou, M. L. L., Montero‐Melendez, T., Donners, M. M. P. C., Deckers, N. M., Krysko, D. V., Vandenabeele, P., Perretti, M., Schurgers, L. J., et al. (2012) · Cell Death and Differentiation · doi:10.1038/cdd.2012.107 · Cited by 53
Alteration of N‐glycosylation in the kidney in a mouse model of systemic lupus erythematosus: relative quantification of N‐glycans using an isotope‐tagging method
Hashii, N., Kawasaki, N., Itoh, S., Nakajima, Y., Kawanishi, T., & Yamaguchi, T. (2008) · Immunology · doi:10.1111/j.1365-2567.2008.02898.x · Cited by 50
Regulation of cancer stem cell activities by tumor-associated macrophages.
Jinushi, M., Baghdadi, M., Chiba, S., & Yoshiyama, H. (2012) · Europe PMC (PubMed Central) · Cited by 49
Milk Fat Globule Epidermal Growth Factor VIII Signaling in Arterial Wall Remodeling
Wang, M., Wang, H. H., & Lakatta, E. G. (2013) · Current Vascular Pharmacology · doi:10.2174/1570161111311050014 · Cited by 49
Autophagy in C. elegans development
Palmisano, N. J., & Meléndez, A. (2018) · Developmental Biology · doi:10.1016/j.ydbio.2018.04.009 · Cited by 53
Phagocytic clearance of apoptotic, necrotic, necroptotic and pyroptotic cells
Atkin‐Smith, G. K. (2021) · Biochemical Society Transactions · doi:10.1042/bst20200696 · Cited by 50

Authors: Hanayama, R., Tanaka, M., Miyasaka, K., Aozasa, K., Koike, M., Uchiyama, Y., & Nagata, S.
Affiliations: RIKEN (JP)
Corresponding author: Nagata, Shigekazu
ORCID: Hanayama, Rikinari
Tanaka, Masato
Koike, Masato
Uchiyama, Yasuo
Nagata, Shigekazu
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2004-05-21
Volume: 304
Issue: 5674
Pages: 1147-1150
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.1094359
OpenAlex: W2037393136
Cited by: 992
References: 24
Citations by year: 2026: 10 · 2025: 22 · 2024: 32 · 2023: 37 · 2022: 34 · 2021: 48 · 2020: 36 · 2019: 36 · 2018: 41 · 2017: 46 · 2016: 32 · 2015: 42 · 2014: 51 · 2013: 64 · 2012: 59
FWCI: 21.82
Type: journal article
Language: en
Open access: closed
Locations: Science (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
Health Sciences › Medicine › Rheumatology › Systemic Lupus Erythematosus Research
Health Sciences › Medicine › Hepatology › Liver Diseases and Immunity
Keywords: MFG-E8, efferocytosis, phosphatidylserine, macrophages, tingible body macrophages, germinal center, splenomegaly, glomerulonephritis, autoantibodies, autoimmune disease, B cell apoptosis
MeSH terms: CD68 Molecule, Animals, Antigens, Surface, Antibodies, Antinuclear, Autoantibodies, Autoimmune Diseases, B-Lymphocytes, Female, Glomerulonephritis, Macrophage Activation, Macrophages, Membrane Glycoproteins, Milk Proteins, Phagocytosis, Phosphatidylserines, Protein Binding, Spleen, Splenomegaly, T-Lymphocytes, Blotting, Northern, Antigens, Differentiation, Myelomonocytic, Antigens, CD, Apoptosis, Macrophages, Peritoneal, Gene Targeting, Germinal Center, In Situ Nick-End Labeling, Mice

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Autoimmune Disease and Impaired Uptake of Apoptotic Cells in MFG-E8-Deficient Mice

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