Requirement for a Drosophila E3-Ubiquitin Ligase in Phagocytosis of Apoptotic Cells

Immunity

Volumn 27, Issue 4, 2007, Pages 585-596

  Silva, Elizabeth ^a   Au Yeung, Hiu Wan ^a   Van Goethem, Emeline ^a   Burden, Jemima ^a   Franc, Nathalie C ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

MOLIMMUNO

Indexed keywords

F BOX PROTEIN; PROTEASOME; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; ENZYME SPECIFICITY; GENETIC SCREENING; IN VIVO STUDY; INNATE IMMUNITY; MACROPHAGE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; UBIQUITINATION;

ANIMALS; APOPTOSIS; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; MACROPHAGES; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; PHAGOCYTOSIS; PROTEASOME ENDOPEPTIDASE COMPLEX; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SKP CULLIN F-BOX PROTEIN LIGASES; TRANSFECTION; UBIQUITIN-PROTEIN LIGASES;

EID: 35349021411     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2007.08.016     Document Type: Article

References (50)

1. Abrams J.M., White K., Fessler L.I., and Steller H. Programmed cell death during Drosophila embryogenesis. Development 117 (1993) 29-43
2. Awasaki T., Tatsumi R., Takahashi K., Arai K., Nakanishi Y., Ueda R., and Ito K. Essential role of the apoptotic cell engulfment genes draper and ced-6 in programmed axon pruning during Drosophila metamorphosis. Neuron 50 (2006) 855-867
3. Belote J.M., and Fortier E. Targeted expression of dominant negative proteasome mutants in Drosophila melanogaster. Genesis 34 (2002) 80-82
4. Bocca S.N., Muzzopappa M., Silberstein S., and Wappner P. Occurrence of a putative SCF ubiquitin ligase complex in Drosophila. Biochem. Biophys. Res. Commun. 286 (2001) 357-364
5. Bose J., Gruber A.D., Helming L., Schiebe S., Wegener I., Hafner M., Beales M., Kontgen F., and Lengeling A. The phosphatidylserine receptor has essential functions during embryogenesis but not in apoptotic cell removal. J. Biol. 3 (2004) 15
6. Cohen P.L., Caricchio R., Abraham V., Camenisch T.D., Jennette J.C., Roubey R.A., Earp H.S., Matsushima G., and Reap E.A. Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J. Exp. Med. 196 (2002) 135-140
7. deBakker C.D., Haney L.B., Kinchen J.M., Grimsley C., Lu M., Klingele D., Hsu P.K., Chou B.K., Cheng L.C., Blangy A., et al. Phagocytosis of apoptotic cells is regulated by a UNC-73/TRIO-MIG-2/RhoG signaling module and armadillo repeats of CED-12/ELMO. Curr. Biol. 14 (2004) 2208-2216
8. deCathelineau A.M., and Henson P.M. The final step in programmed cell death: Phagocytes carry apoptotic cells to the grave. Essays Biochem. 39 (2003) 105-117
9. Fadok V.A., Bratton D.L., Rose D.M., Pearson A., Ezekewitz R.A., and Henson P.M. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405 (2000) 85-90
10. Fernandez-Funez P., Nino-Rosales M.L., de Gouyon B., She W.C., Luchak J.M., Martinez P., Turiegano E., Benito J., Capovilla M., Skinner P.J., et al. Identification of genes that modify ataxin-1-induced neurodegeneration. Nature 408 (2000) 101-106
11. Franc N.C. Phagocytosis of apoptotic cells in mammals, caenorhabditis elegans and Drosophila melanogaster: Molecular mechanisms and physiological consequences. Front. Biosci. 7 (2002) d1298-d1313
12. Franc N.C., Dimarcq J.L., Lagueux M., Hoffmann J., and Ezekowitz R.A. Croquemort, a novel Drosophila hemocyte/macrophage receptor that recognizes apoptotic cells. Immunity 4 (1996) 431-443
13. Franc N.C., Heitzler P., Ezekowitz R.A., and White K. Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila. Science 284 (1999) 1991-1994
14. Friedman J., and Xue D. To live or die by the sword: The regulation of apoptosis by the proteasome. Dev. Cell 6 (2004) 460-461
15. Gaipl U.S., Sheriff A., Franz S., Munoz L.E., Voll R.E., Kalden J.R., and Herrmann M. Inefficient clearance of dying cells and autoreactivity. Curr. Top. Microbiol. Immunol. 305 (2006) 161-176
16. Glickman M.H., and Ciechanover A. The ubiquitin-proteasome proteolytic pathway: Destruction for the sake of construction. Physiol. Rev. 82 (2002) 373-428
17. Gumienny T.L., Brugnera E., Tosello-Trampont A.C., Kinchen J.M., Haney L.B., Nishiwaki K., Walk S.F., Nemergut M.E., Macara I.G., Francis R., et al. CED-12/ELMO, a novel member of the CrkII/Dock180/Rac pathway, is required for phagocytosis and cell migration. Cell 107 (2001) 27-41
18. Ho M.S., Tsai P.I., and Chien C.T. F-box proteins: The key to protein degradation. J. Biomed. Sci. 13 (2006) 181-191
19. Khush R.S., Cornwell W.D., Uram J.N., and Lemaitre B. A ubiquitin-proteasome pathway represses the Drosophila immune deficiency signaling cascade. Curr. Biol. 12 (2002) 1728-1737
20. Kinchen J.M., Cabello J., Klingele D., Wong K., Feichtinger R., Schnabel H., Schnabel R., and Hengartner M.O. Two pathways converge at CED-10 to mediate actin rearrangement and corpse removal in C. elegans. Nature 434 (2005) 93-99
21. Kloetzel P.M., and Ossendorp F. Proteasome and peptidase function in MHC-class-I-mediated antigen presentation. Curr. Opin. Immunol. 16 (2004) 76-81
22. Koh K., Zheng X., and Sehgal A. JETLAG resets the Drosophila circadian clock by promoting light-induced degradation of TIMELESS. Science 312 (2006) 1809-1812
23. Kostova Z., and Wolf D.H. For whom the bell tolls: Protein quality control of the endoplasmic reticulum and the ubiquitin-proteasome connection. EMBO J. 22 (2003) 2309-2317
24. Lee W.L., Kim M.K., Schreiber A.D., and Grinstein S. Role of ubiquitin and proteasomes in phagosome maturation. Mol. Biol. Cell 16 (2005) 2077-2090
25. Liu Q.A., and Hengartner M.O. Candidate adaptor protein CED-6 promotes the engulfment of apoptotic cells in C. elegans. Cell 93 (1998) 961-972
26. MacDonald J.M., Beach M.G., Porpiglia E., Sheehan A.E., Watts R.J., and Freeman M.R. The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 50 (2006) 869-881
27. Manaka J., Kuraishi T., Shiratsuchi A., Nakai Y., Higashida H., Henson P., and Nakanishi Y. Draper-mediated and phosphatidylserine-independent phagocytosis of apoptotic cells by Drosophila hemocytes/macrophages. J. Biol. Chem. 279 (2004) 48466-48476
28. Mangahas P.M., and Zhou Z. Clearance of apoptotic cells in Caenorhabditis elegans. Semin. Cell Dev. Biol. 16 (2005) 295-306
29. Murphy T.D. Drosophila skpA, a component of SCF ubiquitin ligases, regulates centrosome duplication independently of cyclin E accumulation. J. Cell Sci. 116 (2003) 2321-2332
30. Pazdera T.M., Janardhan P., and Minden J.S. Patterned epidermal cell death in wild-type and segment polarity mutant Drosophila embryos. Development 125 (1998) 3427-3436
31. Pittoni V., and Valesini G. The clearance of apoptotic cells: Implications for autoimmunity. Autoimmun. Rev. 1 (2002) 154-161
32. Raff M.C., Barres B.A., Burne J.F., Coles H.S., Ishizaki Y., and Jacobson M.D. Programmed cell death and the control of cell survival. Philos. Trans. R. Soc. Lond. B Biol. Sci. 345 (1994) 265-268
33. Reddien P.W., and Horvitz H.R. CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat. Cell Biol. 2 (2000) 131-136
34. Ren Y., Silverstein R.L., Allen J., and Savill J. CD36 gene transfer confers capacity for phagocytosis of cells undergoing apoptosis. J. Exp. Med. 181 (1995) 1857-1862
35. Savill J., Dransfield I., Gregory C., and Haslett C. A blast from the past: Clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2 (2002) 965-975
36. Savill J., Hogg N., Ren Y., and Haslett C. Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J. Clin. Invest. 90 (1992) 1513-1522
37. Skowyra D., Craig K.L., Tyers M., Elledge S.J., and Harper J.W. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91 (1997) 209-219
38. Sonnenfeld M.J., and Jacobs J.R. Macrophages and glia participate in the removal of apoptotic neurons from the Drosophila embryonic nervous system. J. Comp. Neurol. 359 (1995) 644-652
39. Studer D., Graber W., Al-Amoudi A., and Eggli P. A new approach for cryofixation by high-pressure freezing. J. Microsc. 203 (2001) 285-294
40. Tepass U., Fessler L.I., Aziz A., and Hartenstein V. Embryonic origin of hemocytes and their relationship to cell death in Drosophila. Development 120 (1994) 1829-1837
41. Tosello-Trampont A.C., Brugnera E., and Ravichandran K.S. Evidence for a conserved role for CRKII and Rac in engulfment of apoptotic cells. J. Biol. Chem. 276 (2001) 13797-13802
42. White K., Lisi S., Kurada P., Franc N., and Bangs P. Methods for studying apoptosis and phagocytosis of apoptotic cells in Drosophila tissues and cell lines. Methods Cell Biol. 66 (2001) 321-338
43. Wing J.P., Schreader B.A., Yokokura T., Wang Y., Andrews P.S., Huseinovic N., Dong C.K., Ogdahl J.L., Schwartz L.M., White K., and Nambu J.R. Drosophila Morgue is an F box/ubiquitin conjugase domain protein important for grim-reaper mediated apoptosis. Nat. Cell Biol. 4 (2002) 451-456
44. Wu Y.C., and Horvitz H.R. C. elegans phagocytosis and cell-migration protein CED-5 is similar to human DOCK180. Nature 392 (1998) 501-504
45. Wu Y.C., and Horvitz H.R. The C. elegans cell corpse engulfment gene ced-7 encodes a protein similar to ABC transporters. Cell 93 (1998) 951-960
46. Wu Y.C., Tsai M.C., Cheng L.C., Chou C.J., and Weng N.Y. C. elegans CED-12 acts in the conserved crkII/DOCK180/Rac pathway to control cell migration and cell corpse engulfment. Dev. Cell 1 (2001) 491-502
47. Wyllie A.H., Kerr J.F., and Currie A.R. Cell death: The significance of apoptosis. Int. Rev. Cytol. 68 (1980) 251-306
48. Yu X., Odera S., Chuang C.H., Lu N., and Zhou Z. C. elegans Dynamin mediates the signaling of phagocytic receptor CED-1 for the engulfment and degradation of apoptotic cells. Dev. Cell 10 (2006) 743-757
49. Zhou Z., Hartwieg E., and Horvitz H.R. CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 104 (2001) 43-56
50. Zhou Z., Mangahas P.M., and Yu X. The genetics of hiding the corpse: Engulfment and degradation of apoptotic cells in C. elegans and D. melanogaster. Curr. Top. Dev. Biol. 63 (2004) 91-143