Phosphatidylserine recognition and induction of apoptotic cell clearance by Drosophila engulfment receptor Draper

Journal of Biochemistry

Volumn 153, Issue 5, 2013, Pages 483-491

  Tung, Tran Thanh ^a,b   Nagaosa, Kaz ^a   Fujita, Yu ^a   Kita, Asana ^a   Mori, Hiroki ^a   Okada, Ryo ^a,c   Nonaka, Saori ^a   Nakanishi, Yoshinobu ^a  

^a KANAZAWA UNIVERSITY   (Japan)

^b HANOI MEDICAL UNIVERSITY   (Viet Nam)

^c KYUSHU UNIVERSITY   (Japan)

Author keywords

apoptosis; Drosophila; membrane receptor; phagocytosis; phospholipid

Indexed keywords

LACTADHERIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; BINDING AFFINITY; CELL PHAGOCYTOSIS; CELL SURFACE; CLEARANCE; DROSOPHILA; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECEPTOR BINDING;

ACYLTRANSFERASES; ANIMALS; APOPTOSIS; DROSOPHILA; DROSOPHILA PROTEINS; MEMBRANE PROTEINS; PHAGOCYTOSIS; PHOSPHATIDYLSERINES;

EID: 84877273148     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvt014     Document Type: Article

References (56)

1. Liao, D.J. (2005) The scavenger cell hypothesis of apoptosis. Apoptosis redefined as a process by which a cell in living tissue is destroyed by phagocytosis. Med. Hypotheses 65, 23-28 (Pubitemid 40704523)
2. Nakanishi, Y., Nagaosa, K., and Shiratsuchi, A. (2011 Phagocytic removal of cells that have become unwanted. Implications for animal development and tissue homeostasis. Dev. Growth Differ. 53, 149-160
3. Savill, J. and Fadok, V. (2000) Corpse clearance defines the meaning of cell death. Nature 407, 784-788
4. Lauber, K., Blumenthal, S.G., Waibel, M., and Wesselborg, S. (2004) Clearance of apoptotic cells. Getting rid of the corpses. Mol. Cell 14, 277-287 (Pubitemid 38607340)
5. Ravichandran, K.S. and Lorenz, U. (2007) Engulfment of apoptotic cells: Signals for a good meal. Nat. Rev. Immunol. 7, 964-974 (Pubitemid 350166061)
6. Ravichandran, K.S. (2011) Beginning of a good apoptotic meal. The find-me and eat-me signaling pathways. Immunity 35, 445-455
7. Reddien, P.W. and Horvitz, H.R. (2004) The engulfment process of programmed cell death in Caenorhabditis elegans. Annu. Rev. Cell Dev. Biol. 20, 193-221 (Pubitemid 39488637)
8. Kinchen, J.M. and Hengartner, M.O. (2004) Tales of cannibalism, suicide, and murder. Programmed cell death in C. elegans. Curr. Top. Dev. Biol. 65, 1-45
9. Mangahas, P.M. and Zhou, Z. (2005) Clearance of apoptotic cells in Caenorhabditis elegans. Semin. Cell Dev. Biol. 16, 295-306 (Pubitemid 40432130)
10. Lettre, G. and Hengartner, M.O. (2006) Developmental apoptosis in C. elegans: A complex CEDnario. Nat. Rev. Mol. Cell Biol. 7, 97-108 (Pubitemid 43278293)
11. Zhou, Z., Hartwieg, E., and Horvitz, H.R. (2001) CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 104, 43-56 (Pubitemid 32144971)
12. Hsu, T.-Y. and Wu, Y.-C. (2010) Engulfment of apoptotic cells in C. elegans is mediated by integrin a/SRC signaling. Curr. Biol. 20, 477-486
13. Callebaut, I., Mignotte, V., Souchet, M., and Mornon, J.-P. (2003) EMI domains are widespread and reveal the probable orthologs of the Caenorhabditis elegans CED-1 protein. Biochem. Biophys. Res. Commun. 300, 619-623 (Pubitemid 36268880)
14. Brown, N.H. (2000) Cell-cell adhesion via the ECM: Integrin genetics in fly and worm. Matrix Biol. 19, 191-201 (Pubitemid 30601752)
15. Kinchen, J.M. and Ravichandran, K.S. (2007) Journey to the grave: Signaling events regulating removal of apoptotic cells. J. Cell Sci. 120, 2143-2149 (Pubitemid 47074120)
16. Schlegel, R.A. and Williamson, P. (2001) Phosphatidylserine, a death knell. Cell Death Differ. 8, 551-563 (Pubitemid 32586592)
17. Wu, Y., Tibrewal, N., and Birge, R.B. (2006 Phosphatidylserine recognition by phagocytes: A view to a kill. Trends Cell Biol. 16, 189-197
18. Ravichandran, K.S. (2011) Beginning of a good apoptotic meal. The find-me and eat-me signaling pathways. Immunity 35, 445-455
19. Wang, X., Li, W., Zhao, D., Liu, B., Shi, Y., Chen, B., Yang, H., Guo, P., Geng, X., Shang, Z., Peden, E., Kage-Nakadai, E., Mitani, S., and Xue, D. (2010 Caenorhabditis elegans transthyretin-like protein TTR-52 mediates recognition of apoptotic cells by the CED-1 phagocyte receptor. Nat. Cell Biol. 12, 655-664
20. Kang, Y., Zhao, D., Liang, H., Liu, B., Zhang, Y., Liu, Q., Wang, X., and Liu, Y. (2012) Structural study of TTR-52 reveals the mechanism by which a bridging molecule mediates apoptotic cell engulfment. Genes Dev. 26, 1339-1350
21. Freeman, M.R., Delrow, J., Kim, J., Johnson, E., and Doe, C.Q. (2003) Unwrapping glial biology: Gcm target genes regulating glial development, diversification, and function. Neuron 38, 567-580 (Pubitemid 36645032)
22. Manaka, J., Kuraishi, T., Shiratsuchi, A., Nakai, Y., Higashida, H., Henson, P., and Nakanishi, Y. (2004 Draper-mediated and phosphatidylserine- independent phagocytosis of apoptotic cells by Drosophila hemocytes macrophages. J. Biol. Chem. 279, 48466-48476 (Pubitemid 39541005)
23. Kuraishi, T., Nakagawa, Y., Nagaosa, K., Hashimoto, Y., Ishimoto, T., Moki, T., Fujita, Y., Nakayama, H., Dohmae, N., Shiratsuchi, A., Yamamoto, N., Ueda, K., Yamaguchi, M., Awasaki, T., and Nakanishi, Y. (2009 Pretaporter, a Drosophila protein serving as a ligand for Draper in the phagocytosis of apoptotic cells. EMBO J. 28, 3868-3878
24. Kurant, E., Axelrod, S., Leaman, D., and Gaul, U. (2008) Six-microns-under acts upstream of Draper in the glial phagocytosis of apoptotic neurons. Cell 133, 498-509 (Pubitemid 351608695)
25. Brückner, K., Kockel, L., Duchek, P., Luque, C.M., Rørth, P., and Perrimon, N. (2004) The PDGF/VEGF receptor controls blood cell survival in Drosophila. Dev. Cell 7, 73-84 (Pubitemid 39172689)
26. Hanayama, R., Tanaka, M., Miwa, K., Shinohara, A., Iwamatsu, A., and Nagata, S. (2002) Identification of a factor that links apoptotic cells to phagocytes. Nature 417, 182-187 (Pubitemid 34506799)
27. Venegas, V. and Zhou, Z. (2007) Two alternative mechanisms that regulate the presentation of apoptotic cell engulfment signal in Caenorhabditis elegans. Mol. Biol. Cell 18, 3180-3192 (Pubitemid 47235321)
28. Brand, A.H. and Perrimon, N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415 (Pubitemid 23214028)
29. Fujita, Y., Nagaosa, K., Shiratsuchi, A., and Nakanishi, Y. (2012) Role of NPxY motif in Draper-mediated apoptotic cell clearance in Drosophila. Drug Discov. Ther. 6, 291-297
30. Bischof, J., Maeda, R.K., Hediger, M., Karch, F., and Basler, K. (2007) An optimized transgenesis system for Drosophila using germ-line-specific fC31 integrases. Proc. Natl Acad. Sci. U S A 104, 3312-3317
31. Kawasaki, Y., Nakagawa, A., Nagaosa, K., Shiratsuchi, A., and Nakanishi, Y. (2002) Phosphatidylserine binding of class B scavenger receptor type I, a phagocytosis receptor of testicular Sertoli cells. J. Biol. Chem. 277, 27559-27566 (Pubitemid 34951777)
32. Shiratsuchi, A., Umeda, M., Ohba, Y., and Nakanishi, Y. (1997) Recognition of phosphatidylserine on the surface of apoptotic spermatogenic cells and subsequent phagocytosis by Sertoli cells of the rat. J. Biol. Chem. 272, 2354-2358 (Pubitemid 27058522)
33. Nagaosa, K., Okada, R., Nonaka, S., Takeuchi, K., Fujita, Y., Miyasaka, T., Manaka, J., Ando, I., and Nakanishi, Y. (2011) Integrin bn-mediated phagocytosis of apoptotic cells in Drosophila embryos. J. Biol. Chem. 286, 25770-25777
34. Züllig, S., Neukomm, L.J., Jovanovic, M., Charette, S.J., Lyssenko, N.N., Halleck, M.S., Reutelingsperger, C.P.M., Schlegel, R.A., and Hengartner, M.O. (2007 Aminophospholipid translocase TAT-1 promotesphosphatidylserine exposure during C. elegans apoptosis. Curr. Biol. 17, 994-999 (Pubitemid 46829845)
35. Wang, X., Wang, J., Gengyo-Ando, K., Gu, L., Sun, C.-L., Yang, C., Shi, Y., Kobayashi, T., Shi, Y., Mitani, S., Xie, X.-S., and Xue, D. (2007) C. elegans mitochondrial factor WAH-1 promotes phosphatidylserine externalization in apoptotic cells through phospholipid scramblase SCRM-1. Nat. Cell Biol. 9, 541-549 (Pubitemid 46696535)
36. Darland-Ransom, M., Wang, X., Sun, C.-L., Mapes, J., Gengyo-Ando, K., Mitani, S., and Xue, D. (2008) Role of C. elegans TAT-1 protein in maintaining plasma membrane phosphatidylserine asymmetry. Science 320, 528-531 (Pubitemid 351590665)
37. Park, S.-Y., Jung, M.-Y., Kim, H.-J., Lee, S.-J., Kim, S.-Y., Lee, B.-H., Kwon, T.-H., Park, R.-W., and Kim, I.-S. (2008) Rapid cell corpse clearance by stabilin-2, a membrane phosphatidylserine receptor. Cell Death Differ. 15, 192-201 (Pubitemid 350286187)
38. Kurucz, É ., Má rkus, R., Zsámboki, J., Folkl-Medzihradszky, K., Darula, Z., Vilmos, P., Udvardy, A., Krausz, I., Lukacsovich, T., Gateff, E., Zettervall, C.-J., Hultmark, D., and Andó, I. (2007) Nimrod, a putative phagocytosis receptor with EGF repeats in Drosophila plasmatocytes. Curr. Biol. 17, 649-654 (Pubitemid 46509583)
39. Doliana, R., Bot, S., Bonaldo, P., and Colombatti, A. (2000) EMI, a novel cysteine-rich domain of EMILINs and other extracellular proteins, interacts with the gC1q domains and participates in multimerization. FEBS Lett. 484, 164-168
40. Somogyi, K., Sipos, B., Pénzes, Z., Kurucz, É ., Zsámboki, J., Hultmark, D., and Andó, I. (2008 Evolution of genes and repeats in the Nimrod superfamily. Mol. Biol. Evol. 25, 2337-2347
41. Franc, N.C., Dimarcq, J.-L., Lagueux, M., Hoffmann, J., and Ezekowitz, R.A.B. (1996) Croquemort, a novel Drosophila hemocyte/macrophage receptor that recognizes apoptotic cells. Immunity 4, 431-443 (Pubitemid 26354653)
42. Franc, N.C., Heitzler, P., Ezekowitz, R.A.B., and White, K. (1999) Requirement for Croquemort in phagocytosis of apoptotic cells in Drosophila. Science 284, 1991-1994 (Pubitemid 29309447)
43. Hashimoto, Y., Tabuchi, Y., Sakurai, K., Kutsuna, M., Kurokawa, K., Awasaki, T., Sekimizu, K., Nakanishi, Y., and Shiratsuchi, A. (2009) Identification of lipoteichoic acid as a ligand for Draper in the phagocytosis of Staphylococcus aureus by Drosophila hemocytes. J. Immunol. 183, 7451-7460
44. Okada, R., Nagaosa, K., Kuraishi, T., Nakayama, H., Yamamoto, N., Nakagawa, Y., Dohmae, N., Shiratsuchi, A., and Nakanishi, Y. (2012) Apoptosisdependent externalization and involvement in apoptotic cell clearance of DmCaBP1, an endoplasmic reticulum protein of Drosophila. J. Biol. Chem. 287, 3138-3146
45. Ishimoto, Y., Ohashi, K., Mizuno, K., and Nakano, T. (2000) Promotion of the uptake of PS liposomes and apoptotic cells by a product of growth arrest-specific gene, gas6. J. Biochem. 127, 411-417 (Pubitemid 30185245)
46. Oka, K., Sawamura, T., Kikuta, K., Itokawa, S., Kume, N., Kita, T., and Masaki, T. (1998) Lectin-like oxidized low-density lipoprotein receptor 1 mediates phagocytosis of aged/apoptotic cells in endothelial cells. Proc. Natl Acad. Sci. U S A 95, 9535-9540 (Pubitemid 28506266)
47. Park, D., Tosello-Trampont, A.-C., Elliott, M.R., Lu, M., Haney, L.B., Ma, Z., Klibanov, A.L., Mandell, J.W., and Ravichandran, K.S. (2007) BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module. Nature 450, 430-434 (Pubitemid 350126756)
48. Miyanishi, M., Tada, K., Koike, M., Uchiyama, Y., Kitamura, T., and Nagata, S. (2007) Identification of Tim4 as a phosphatidylserine receptor. Nature 450, 435-439 (Pubitemid 350126753)
49. Ichimura, T., Asseldonk, E.J., Humphreys, B.D., Gunaratnam, L., Duffield, J.S., and Bonventre, J.V. (2008) Kidney injury molecule-1 is a phosphatidylserine receptor that confers a phagocytic phenotype on epithelial cells. J. Clin. Invest. 118, 1657-1668 (Pubitemid 351632370)
50. He, M., Kubo, H., Morimoto, K., Fujino, N., Suzuki, T., Takahashi, T., Yamada, M., Yamaya, M., Maekawa, T., Yamamoto, Y., and Yamamoto, H. (2011) Receptor for advanced glycation end products binds to phosphatidylserine and assists in the clearance of apoptotic cells. EMBO Rep. 12, 358-364
51. Friggeri, A., Banerjee, S., Biswas, S., de Freitas, A., Liu, G., Bierhaus, A., and Abraham, E. (2011) Participation of the receptor for advanced glycation end products in efferocytosis. J. Immunol. 186, 6191-6198
52. Choi, S.-C., Simhadri, V.R., Tian, L., Gil-Krzewska, A., Krzewski, K., Borrego, F., and Coligan, J.E. (2011 Cutting Edge: Mouse CD300f (CMRF-35-like molecule-1) recognizes outer membrane-exposed phosphatidylserine and can promote phagocytosis. J. Immunol. 187, 3483-3487
53. de Freitas, A., Banerjee, S., Xie, N., Cui, H., Davis, K.I., Friggeri, A., Fu, M., Abraham, E., and Liu, G. (2012 Identification of TLT2 as an engulfment receptor for apoptotic cells. J. Immunol. 188, 6381-6388
54. Emoto, K., Toyama-Sorimachi, N., Karasuyama, H., Inoue, K., and Umeda, M. (1997) Exposure of phosphatidylethanolamine on the surface of apoptotic cells. Exp. Cell Res. 232, 430-434 (Pubitemid 27194059)
55. Verhoven, B., Schlegel, R.A., and Williamson, R. (1995 Mechanisms of phosphatidylserine exposure, a phagocyte recognition signal, on apoptotic T lymphocytes. J. Exp. Med. 182, 1597-1601
56. Shiratsuchi, A., Osada, S., Kanazawa, S., and Nakanishi, Y. (1998) Essential role of phosphatidylserine externalization in apoptosing cell phagocytosis by macrophages. Biochem. Biophys. Res. Commun. 246, 549-555 (Pubitemid 28412640)