Integrin αpS3/β-mediated Phagocytosis of Apoptotic Cells and Bacteria in Drosophila

Journal of Biological Chemistry

Volumn 288, Issue 15, 2013, Pages 10374-10380

  Nonaka, Saori ^a   Nagaosa, Kaz ^a,b   Mori, Toshinobu ^a   Shiratsuchi, Akiko ^a,b   Nakanishi, Yoshinobu ^a,b  

^a Graduate School of Natural Science and Technology   (Japan)

^b KANAZAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC CELLS; CELLULAR FUNCTION; COIMMUNOPRECIPITATION ANALYSIS; DROSOPHILA CELLS; DROSOPHILA EMBRYOS; NUCLEOTIDE SEQUENCES; STAPHYLOCOCCUS AUREUS; TRANSMEMBRANES;

BACTERIA; CELL CULTURE; CELLS; CHEMICAL ANALYSIS;

ANTIGEN-ANTIBODY REACTIONS;

ALPHA INTEGRIN; BETA INTEGRIN; DROSOPHILA PROTEIN; INTEGRIN ALPHAPS3; INTEGRIN BETAV; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BACTERIUM; BLOOD CELL; CONTROLLED STUDY; CROSS LINKING; DROSOPHILA; EMBRYO CELL; GENE; GENE EXPRESSION REGULATION; GENE INSERTION; LARVA; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTOSIS; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RNA INTERFERENCE; SCB GENE; STAPHYLOCOCCUS AUREUS;

ANIMALS; APOPTOSIS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; HEMOCYTES; INTEGRIN ALPHA CHAINS; INTEGRIN BETA CHAINS; MUTATION; PHAGOCYTOSIS; STAPHYLOCOCCUS AUREUS;

ANIMALIA; STAPHYLOCOCCUS AUREUS;

EID: 84876224820     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.451427     Document Type: Article

References (46)

1. Aderem, A., and Underhill, D. M. (1999) Mechanism of phagocytosis in macrophages. Annu. Rev. Immunol. 17, 593-623
2. Stuart, L. M., and Ezekowitz, R. A. (2005) Phagocytosis: elegant complexity. Immunity 22, 539-550
3. 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
4. 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
5. Savill, J., and Fadok, V. (2000) Corpse clearance defines the meaning of cell death. Nature 407, 784-788
6. 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
7. Ravichandran, K. S., and Lorenz, U. (2007) Engulfment of apoptotic cells: signals for a good meal. Nat. Rev. Immunol. 7, 964-974
8. Ravichandran, K. S. (2011) Beginning of a good apoptotic meal: the find-me and eat-me signaling pathways. Immunity 35, 445-455
9. 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
10. Kinchen, J. M., and Hengartner, M. O. (2005) Tales of cannibalism, suicide, and murder: programmed cell death in C. elegans. Curr. Top. Dev. Biol. 65, 1-45
11. Mangahas, P. M., and Zhou, Z. (2005) Clearance of apoptotic cells in Caenorhabditis elegans. Semin. Cell Dev. Biol. 16, 295-306
12. Lettre, G., and Hengartner, M. O. (2006) Developmental apoptosis in C. elegans: a complex CEDnario. Nat. Rev. Mol. Cell Biol. 7, 97-108
13. 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
14. Hsu, T.-Y., and Wu, Y.-C. (2010) Engulfment of apoptotic cells in C. elegans is mediated by integrin -/SRC signaling. Curr. Biol. 20, 477-486
15. 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
16. Brown, N. H. (2000) Cell-cell adhesion via the ECM: integrin genetics in fly and worm. Matrix Biol. 19, 191-201
17. 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
18. Hynes, R. O. (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687
19. Margadant, C., Monsuur, H. N., Norman, J. C., and Sonnenberg, A. (2011) Mechanisms of integrin activation and trafficking. Curr. Opin. Cell Biol. 23, 607-614
20. Giancotti, F. G., and Ruoslahti, E. (1999) Integrin signaling. Science 285, 1028-1032
21. Wu, Y., Tibrewal, N., and Birge, R. B. (2006) Phosphatidylserine recognition by phagocytes: a view to a kill. Trends Cell Biol. 16, 189-197
22. Dupuy, A. G., and Caron, E. (2008) Integrin-dependent phagocytosis: spreading from microadhesion to new concepts. J. Cell Sci. 121, 1773-1783
23. Nagaosa, K., Okada, R., Nonaka, S., Takeuchi, K., Fujita, Y., Miyasaka, T., Manaka, J., Ando, I., and Nakanishi, Y. (2011) Integrin -mediated phagocytosis of apoptotic cells in Drosophila embryos. J. Biol. Chem. 286, 25770-25777
24. Shiratsuchi, A., Mori, T., Sakurai, K., Nagaosa, K., Sekimizu, K., Lee, B. L., and Nakanishi, Y. (2012) Independent recognition of Staphylococcus aureus by two receptors for phagocytosis in Drosophila. J. Biol. Chem. 287, 21663-21672
25. Brown, N. H., Gregory, S. L., and Martin-Bermudo, M. D. (2000) Integrins as mediators of morphogenesis in Drosophila. Dev. Biol. 223, 1-16
26. Devenport, D., and Brown, N. H. (2004) Morphogenesis in the absence of integrins: mutation of both Drosophila- subunits prevents midgut migration. Development 131, 5405-5415
27. Ju?rgens, G., Wieschaus, E., Nüsslein-Volhard, C., and Kluding, H. (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster II. Zygotic loci on the third chromosome. Roux's Arch. Dev. Biol. 193, 283-295
28. 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
29. 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
30. Manaka, J., Kuraishi, T., Shiratsuchi, A., Nakai, Y., Higashida, H., Henson, P., and Nakanishi, Y. (2004) Draper-mediated and phosphatidylserineindependent phagocytosis of apoptotic cells by Drosophila hemocytes/ macrophages. J. Biol. Chem. 279, 48466-48476
31. Awasaki, T., Tatsumi, R., Takahashi, K., Arai, K., Nakanishi, Y., Ueda, R., and Ito, K. (2006) Essential role of the apoptotic cell engulfment genes draper and ced-6 in programmed axon pruning during Drosophila metamorphosis. Neuron 50, 855-867
32. Wada, A., Kato, K., Uwo, M. F., Yonemura, S., and Hayashi, S. (2007) Specialized extraembryonic cells connect embryonic and extraembryonic epidermis in response to Dpp during dorsal closure in Drosophila. Dev. Biol. 301, 340-349
33. Yee, G. H., and Hynes, R. O. (1993) A novel, tissue-specific integrin subunit, -, expressed in the midgut of Drosophila melanogaster. Development 118, 845-858
34. 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
35. Stark, K. A., Yee, G. H., Roote, C. E., Williams, E. L., Zusman, S., and Hynes, R. O. (1997) A novel - integrin subunit associates with -PS and functions in tissue morphogenesis and movement during Drosophila development. Development 124, 4583-4594
36. Grotewiel, M. S., Beck, C. D. O., Wu, K. H., Zhu, X.-R., and Davis, R. L. (1998) Integrin-mediated short-term memory in Drosophila. Nature 391, 455-460
37. Tsai, P.-I., Kao, H.-H., Grabbe, C., Lee, Y.-T., Ghose, A., Lai, T.-T., Peng, K.-P., Van Vactor, D., Palmer, R. H., Chen, R.-H., Yeh, S.-R., and Chien, C.-T. (2008) Fak56 functions downstream of integrin -PS3- and suppresses MAPK activation in neuromascular junction growth. Neural. Dev. 3, 26
38. Baum, P. D., and Garriga, G. (1997) Neuronal migrations and axon fasciculation are disrupted in ina-1 integrin mutants. Neuron 19, 51-62
39. Hsieh, H.-H., Hsu, T.-Y., Jiang, H.-S., and Wu, Y.-C. (2012) Integrin - PAT-2/CDC42 signaling is required for muscle-mediated clearance of apoptotic cells in Caenorhabditis elegans. PLoS Genet. 8, e1002663
40. 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
41. 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
42. 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
43. 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
44. 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
45. Franc, N. C., Dimarcq, J.-L., Lagueux, M., Hoffmann, J., and Ezekowitz, R. A. (1996) Croquemort, a novel Drosophila hemocyte/macrophage receptor that recognizes apoptotic cells. Immunity 4, 431-443
46. Franc, N. C., Heitzler, P., Ezekowitz, R. A., and White, K. (1999) Requirement for Croquemort in phagocytosis of apoptotic cells in Drosophila. Science 284, 1991-1994