Masking of phosphatidylserine inhibits apoptotic cell engulfment and induces autoantibody production in mice

Journal of Experimental Medicine

Volumn 200, Issue 4, 2004, Pages 459-467

  Asano, Kenichi ^a,c   Miwa, Miyu ^c   Miwa, Keiko ^d   Hanayama, Rikinari ^a   Nagase, Hiroko ^a   Nagata, Shigekazu ^a,b,d   Tanaka, Masato ^a,c  

^a OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c RIKEN YOKOHAMA INSTITUTE   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Apoptosis; Autoimmunity; MFG E8; Phagocytosis; Phosphatidylserine

Indexed keywords

ANTINUCLEAR ANTIBODY; AUTOANTIBODY; CELL PROTEIN; INTERLEUKIN 10; LACTADHERIN; PHOSPHATIDYLSERINE; PHOSPHOLIPID ANTIBODY; THIOGLYCOLIC ACID; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; APOPTOSIS; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; GLOMERULUS; IMMUNOGLOBULIN DEPOSITION; IMMUNOHISTOCHEMISTRY; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PHAGOCYTOSIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, SURFACE; APOPTOSIS; AUTOANTIBODIES; BONE MARROW; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INTERLEUKIN-10; MACROPHAGES; MICE; MICE, INBRED C57BL; MILK PROTEINS; PHAGOCYTOSIS; PHOSPHATIDYLSERINES; POINT MUTATION;

EID: 4344715014     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20040342     Document Type: Article

References (40)

1. Jacobson, M.D., M. Weil, and M.C. Raff. 1997. Programmed cell death in animal development. Cell. 88:347-354.
2. Vaux, D.L., and S.J. Korsmeyer. 1999. Cell death in development. Cell. 96:245-254.
3. Stroh, C., and K. Schulze-Osthoff. 1998. Death by a thousand cuts: an ever increasing list of caspase substrates. Cell Death Differ. 5:997-1000.
4. Nagata, S. 1997. Apoptosis by death factor. Cell. 88:355-365.
5. McIlroy, D., M. Tanaka, H. Sakahira, H. Fukuyama, M. Suzuki, K. Yamamura, Y. Ohsawa, Y. Uchiyama, and S. Nagata. 2000. An auxiliary mode of apoptotic DNA fragmentation provided by phagocytes. Genes Dev. 14:549-558.
6. Kawane, K., H. Fukuyama, H. Yoshida, H. Nagase, Y. Ohsawa, Y. Uchiyama, K. Okada, T. Iida, and S. Nagata. 2003. Impaired thymic development in mouse embryos deficient in apoptotic DNA degradation. Nat. Immunol. 4:138-144.
7. Ren, Y., and J. Savill. 1998. Apoptosis: the importance of being eaten. Cell Death Differ. 5:563-568.
8. Aderem, A., and D.M. Underhill. 1999. Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol. 17:593-423.
9. Hengartner, M.O. 2001. Apoptosis: corralling the corpses. Cell. 104:325-328.
10. Savill, J., and V. Fadok. 2000. Corpse clearance defines the meaning of cell death. Nature. 407:784-788.
11. Savill, J., I. Dransfield, C. Gregory, and C. Haslett. 2002. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2:965-975.
12. Platt, N., R.P. da Silva, and S. Gordon. 1998. Recognizing death: the phagocytosis of apoptotic cells. Trends Cell Biol. 8:365-372.
13. Hoffmann, P.R., A.M. deCathelineau, C.A. Ogden, Y. Leverrier, D.L. Bratton, D.L. Daleke, A.J. Ridley, V.A. Fadok, and P.M. Henson. 2001. Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptotic cells. J. Cell Biol. 155:649-659.
14. Fadok, V.A., D.L. Bratton, D.M. Rose, A. Pearson, R.A. Ezekewitz, and P.M. Henson. 2000. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature. 405:85-90.
15. Oka, K., T. Sawamura, K. Kikuta, S. Itokawa, N. Kume, T. Kita, and T. Masaki. 1998. Lectin-like oxidized low-density lipoprotein receptor 1 mediates phagocytosis of aged/apoptotic cells in endothelial cells. Proc. Natl. Acad. Sci. USA. 95: 9535-9540.
16. Kawasaki, Y., A. Nakagawa, K. Nagaosa, A. Shiratsuchi, and Y. Nakanishi. 2002. Phosphatidylserine binding of class B scavenger receptor type I, a phagocytosis receptor of testicular sertoli cells. J. Biol. Chem. 277:27559-27566.
17. Anderson, H.A., C.A. Maylock, J.A. Williams, C.P. Paweletz, H. Shu, and E. Shacter. 2003. Serum-derived protein S binds to phosphatidylserine and stimulates the phagocytosis of apoptotic cells. Nat. Immunol. 4:87-91.
18. Hanayama, R., M. Tanaka, K. Miwa, A. Shinohara, A. Iwamatsu, and S. Nagata. 2002. Identification of a factor that links apoptotic cells to phagocytes. Nature. 417:182-187.
19. Aoki, N., M. Kishi, Y. Taniguchi, T. Adachi, R. Nakamura, and T. Matsuda. 1995. Molecular cloning of glycoprotein antigens MGP57/53 recognized by monoclonal antibodies raised against bovine milk fat globule membrane. Biochim. Biophys. Acta. 1245:385-391.
20. Aoki, N., M. Ujita, H. Kuroda, M. Urabe, A. Noda, T. Adachil, R. Nakamura, and T. Matsuda. 1994. Immunologically cross-reactive 57 kDa and 53 kDa glycoprotein antigens of bovine milk fat globule membrane: isoforms with different N-linked sugar chains and differential glycosylation at early stages of lactation. Biochim. Biophys. Acta. 1200:227-234.
21. Stubbs, J.D., C. Lekutis, K.L. Singer, A. Bui, D. Yuzuki, U. Srinivasan, and G. Parry. 1990. 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. Proc. Natl. Acad. Sci. USA. 87:8417-8421.
22. Tada, K., M. Tanaka, R. Hanayama, K. Miwa, A. Shinohara, A. Iwamatsu, and S. Nagata. 2003. Tethering of apoptotic cells to phagocytes through binding of CD47 to Src homology 2 domain-bearing protein tyrosine phosphatase substrate-1. J. Immunol. 171:5718-5726.
23. Hanayama, R., M. Tanaka, K. Miwa, and S. Nagata. 2004. Expression of Del-1 in a subset of macrophages for engulfment of apoptotic cells. J. Immunol. 172:3876-3882.
24. Voll, R.E., M. Herrmann, E.A. Roth, C. Stach, J.R. Kalden, and I. Girkontaite. 1997. Immunosuppressive effects of apoptotic cells. Nature. 390:350-351.
25. Byrne, A., and D.J. Reen. 2002. Lipopolysaccharide induces rapid production of IL-10 by monocytes in the presence of apoptotic neutrophils. J. Immunol. 168:1968-1977.
26. Scott, R.S., E.J. McMahon, S.M. Pop, E.A. Reap, R. Caricchio, P.L. Cohen, H.S. Earp, and G.K. Matsushima. 2001. Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature. 411:207-211.
27. Cohen, P.L., R. Caricchio, V. Abraham, T.D. Camenisch, J.C. Jennette, R.A. Roubey, H.S. Earp, G. Matsushima, and E.A. Reap. 2002. Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J. Exp. Med. 196:135-140.
28. Mevorach, D., J.L. Zhou, X. Song, and K.B. Elkon. 1998. Systemic exposure to irradiated apoptotic cells induces autoantibody production. J. Exp. Med. 188:387-392.
29. Gharavi, A.E., L.R. Sammaritano, J. Wen, and K.B. Elkon. 1992. Induction of antiphospholipid autoantibodies by immunization with beta 2 glycoprotein I (apolipoprotein H). J. Clin. Invest. 90:1105-1109.
30. Levine, J.S., R. Subang, J.S. Koh, and J. Rauch. 1998. Induction of anti-phospholipid autoantibodies by beta2-glycoprotein I bound to apoptotic thymocytes. J. Autoimmun. 11:413-424.
31. Fadok, V.A., D.L. Bratton, S.C. Frasch, M.L. Warner, and P.M. Henson. 1998. The role of phosphatidylserine in recognition of apoptotic cells by phagocytes. Cell Death Differ. 5:551-562.
32. Taylor, P.R., A. Carugati, V.A. Fadok, H.T. Cook, M. Andrews, M.C. Carroll, J.S. Savill, P.M. Henson, M. Botto, and M.J. Walport. 2000. A hierarchical role for classical pathway complement proteins in the clearance of apoptotic cells in vivo. J. Exp. Med. 192:359-366.
33. Botto, M., C. Dell'Agnola, A.E. Bygrave, E.M. Thompson, H.T. Cook, F. Petry, M. Loos, P.P. Pandolfi, and M.J. Walport. 1998. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19:56-59.
34. Hanayama, R., M. Tanaka, K. Miyasaka, K. Aozasa, M. Koike, Y. Uchiyama, and S. Nagata. 2004. Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science. 304:1147-1150.
35. Liu, K., T. Iyoda, M. Saternus, Y. Kimura, K. Inaba, and R.M. Steinman. 2002. Immune tolerance after delivery of dying cells to dendritic cells in situ. J. Exp. Med. 196:1091-1097.
36. Shi, Y., J.E. Evans, and K.L. Rock. 2003. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature. 425:516-521.
37. Millar, D.G., K.M. Garza, B. Odermatt, A.R. Elford, N. Ono, Z. Li, and P.S. Ohashi. 2003. Hsp70 promotes antigen-presenting cell function and converts T-cell tolerance to autoimmunity in vivo. Nat. Med. 9:1469-1476.
38. Aoki, N., T. Ishii, S. Ohira, Y. Yamaguchi, M. Negi, T. Adachi, R. Nakamura, and T. Matsuda. 1997. Stage specific expression of milk fat globule membrane glycoproteins in mouse mammary gland: comparison of MFG-E8, butyrophilin, and CD36 with a major milk protein, beta-casein. Biochim. Biophys. Acta. 1334:182-190.
39. Oshima, K., N. Aoki, M. Negi, M. Kishi, K. Kitajima, and T. Matsuda. 1999. Lactation-dependent expression of an mRNA splice variant with an exon for a multiply O-glycosylated domain of mouse milk fat globule glycoprotein MFG-E8. Biochem. Biophys. Res. Commun. 254:522-528.
40. Shi, J., and G.E. Gilbert. 2003. Lactadherin inhibits enzyme complexes of blood coagulation by competing for phospholipid-binding sites. Blood. 101:2628-2636.