Caspases function in autophagic programmed cell death in Drosophila

Development

Volumn 131, Issue 2, 2004, Pages 275-284

  Martin, Damali N ^a,b   Baehrecke, Eric H ^a  

^a UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

Author keywords

Apoptosis; Autophagic cell death; Caspases; Drosophila; Salivary glands

Indexed keywords

ACTIN; ALPHA TUBULIN; CASPASE; CASPASE INHIBITOR; FODRIN; LAMIN; MONOCLONAL ANTIBODY E74; NUCLEAR PROTEIN; SALIVA PROTEIN; STEROID;

ACTIN FILAMENT; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL DEATH; CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; DROSOPHILA; ENZYME ACTIVATION; ENZYME INHIBITION; FEMALE; FRAGMENTATION REACTION; GENE MUTATION; MALE; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SALIVARY GLAND;

ACTINS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; AUTOPHAGY; CASPASES; DROSOPHILA; DROSOPHILA PROTEINS; GENES, INSECT; MUTATION; SALIVARY GLANDS; STEROIDS;

EID: 0842279780     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00933     Document Type: Article

References (65)

1. Arama, E., Agapite, J. and Steller, H. (2003). Caspase activity and a specific cytochrome c are required for sperm differentiation in Drosophila. Dev. Cell 4, 687-697.
2. Aravind, L., Dixit, V. M. and Koonin, E. V. (2001). Apoptotic molecular machinery: vastly increased complexity in vertebrates revealed by genome comparisons. Science 291, 1279-1284.
3. Baehrecke, E. H. (2000). Steroid regulation of programmed cell death during Drosophila development. Cell Death Differ. 7, 1057-1062.
4. Baehrecke, E. H. (2002). How death shapes life during development. Nat. Rev. Mol. Cell. Biol. 3, 779-787.
5. Baehrecke, E. H. (2003). Autophagic programmed cell death in Drosophila. Cell Death Differ. 10, 940-945.
6. Broadus, J., McCabe, J. R., Endrizzi, B., Thummel, C. S. and Woodard, C. T. (1999). The Drosophila βFTZ-F1 orphan nuclear receptor provides competence for stage-specific responses to the steroid hormone ecdysone. Mol. Cell 3, 143-149.
7. Bursch, W., Hochegger, K., Torok, L., Marian, B., Ellinger, A. and Hermann, R. S. (2000). Autophagic and apoptotic types of programmed cell death exhibit different fates of cytoskeletal filaments. J. Cell Sci. 113, 1189-1198.
8. Chen, P., Nordstrom, W., Gish, B. and Abrams, J. M. (1996). grim, a novel cell death gene in Drosophila. Genes Dev. 10, 1773-1782.
9. Chen, P., Rodriguez, A., Erskine, R., Thach, T. and Abrams, J. M. (1998). Dredd, a novel effector of the apoptosis activators Reaper, Grim, and Hid in Drosophila. Dev. Biol. 201, 202-216.
10. Christich, A., Kauppila, S., Chen, P., Sogame, N., Ho, S. I. and Abrams, J. M. (2002). Damage-responsive Drosophila gene sickle encodes a novel IAP binding protein similar to but distinct from reaper, grim, and hid. Curr. Biol. 12, 137-140.
11. Clarke, P. G. H. (1990). Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. 181, 195-213.
12. Coleman, M. L. and Olson, M. F. (2002). Rho GTPase signalling pathways in the morphological changes associated with apoptosis. Cell Death Deffer 9, 493-504.
13. Cryns, V. and Yuan, J. (1998). Proteases to die for. Genes Dev. 12, 1551-1570.
14. Distelhorst, C. W. (2002). Recent insights into the mechanism of glucocorticosteroid-induced apoptosis. Cell Death Differ. 9, 6-19.
15. Dorstyn, L., Colussi, P. A., Quinn, L. M., Richardson, H. and Kumar, S. (1999a). DRONC, an ecdysone-inducible Drosophila caspase. Proc. Natl. Acad. Sci. USA 96, 4307-4312.
16. Dorstyn, L., Read, S. H., Quinn, L. M., Richardson, H. and Kumar, S. (1999b). DECAY, a novel Drosophila caspase related to mammalian caspase-3 and caspase-7. J. Biol. Chem. 274, 30778-30783.
17. Doumanis, J., Quinn, L., Richardson, H. and Kumar, S. (2001). STRICA, a novel Drosophila melanogaster caspase with an unusual serine/threonine-rich prodomain, interacts with DIAP1 and DIAP2. Cell Death Differ. 8, 387-394.
18. Dubreuil, R., Byers, T. J., Branton, D., Goldstein, L. S. and Kiehart, D. P. (1987). Drosophilia spectrin. I. Characterization of the purified protein. J. Cell Biol. 105, 2095-2102.
19. Evans-Storm, R. B. and Cidlowski, J. A. (1995). Regulation of apoptosis by steroid hormones. J. Steroid Biochem. Molec. Biol. 53, 1-6.
20. Fadok, V. A., Voelker, D. R., Campbell, P. A., Cohen, J. J., Bratton, D. L. and Henson, P. M. (1992). Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148, 2207-2216.
21. Franc, N. C., Dimarcq, J.-L., Lagueux, M., Hoffmann, J. and Ezekowitz, A. B. (1996). Croquemort, a novel Drosophila hemocyte/macrophage receptor that recognizes apoptotic cells. Immunity 4, 431-443.
22. Fraser, A. G. and Evan, G. I. (1997). Identification of a Drosophila melanogaster ICE/CED-3-relatedprotease, drICE. EMBO J 16, 2805-2813.
23. Frydman, H. M. and Spradling, A. C. (2001). The receptor-like tyrosine phosphatase lar is required for epithelial planar polarity and for axis determination within Drosophila ovarian follicles. Development 128, 3209-3220.
24. Goyal, L., McCall, K., Agapite, J., Hartwieg, E. and Steller, H. (2000). Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. EMBO J. 19, 589-597.
25. Grether, M. E., Abrams, J. M., Agapite, J., White, K. and Steller, H. (1995). The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev. 9, 1694-1708.
26. Harvey, N. L., Daish, T., Mills, K., Dorstyn, L., Quinn, L. M., Read, S. H., Richardson, H. and Kumar, S. (2001). Characterization of the Drosophila caspase, DAMM. J. Biol. Chem. 276, 25342-25350.
27. Hay, B. A., Wassarman, D. A. and Rubin, G. M. (1995). Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83, 1253-1262.
28. Jacobson, M. D., Weil, M. and Raff, M. C. (1997). Programmed cell death in animal development. Cell 88, 347-354.
29. Jiang, C., Baehrecke, E. H. and Thummel, C. S. (1997). Steroid regulated programmed cell death during Drosophila metamorphosis. Development 124, 4673-4683.
30. Jiang, C., Lamblin, A.-E, J., Steller, H. and Thummel, C. S. (2000). A steroid-triggered transcriptional hierarchy controls salivary gland cell death during Drosophila metamorphosis. Mol. Cell 5, 445-455.
31. Jochova, J., Zakeri, Z. and Lockshin, R. A. ( 1997). Rearrangement of the tubulin and actin cytoskeleton during programmed cell death in Drosophila salivary glands. Cell Death Differ. 4, 140-149.
32. Kanuka, H., Sawamoto, K., Inohara, N., Matsuno, K., Okano, H. and Miura, M. (1999). Control of the cell death pathway by Dapaf-1, a Drosophila Apaf-1/CED-4-related caspase activator. Mol. Cell 4, 757-769.
33. Kerr, J. F., Wyllie, A. H. and Currie, A. R. (1972). Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26, 239-257.
34. Klionsky, D. J. and Emr, S. D. (2000). Autophagy as a regulated pathway of cellular degradation. Science 290, 1717-1721.
35. Lee, C.-Y. and Baehrecke, E. H. (2001). Steroid regulation of autophagic programmed cell death during development. Development 128, 1443-1455.
36. Lee, C.-Y., Wendel, D. P., Reid, P., Lam, G., Thummel, C. S. and Baehrecke, E. H. (2000). E93 directs steroid-triggered programmed cell death in Drosophila. Mol. Cell 6, 433-443.
37. Lee, C.-Y., Cooksey, B. A. K. and Baehrecke, E. H. (2002a). Steroid regulation of midgut cell death during Drosophila development. Dev. Biol. 250, 101-111.
38. Lee, C.-Y., Simon, C. R., Woodard, C. T. and Baehrecke, E. H. (2002b). Genetic mechanism for the stage- and tissue-specific regulation of steroid-triggered programmed cell death in Drosophila. Dev. Biol. 252, 138-148.
39. Lee, C.-Y., Clough, E. A., Yellon, P., Teslovich, T. M., Stephan, D. A. and Baehrecke, E. H. (2003). Genome-wide analyses of steroid- and radiation-triggered programmed cell death in Drosophila. Curr. Biol. 13, 350-357.
40. McCall, K. and Steller, H. (1998). Requirement for DCP-1 Caspase During Drosophila Oogenesis. Science 279, 230-234.
41. Meier, P., Silke, J., Leevers, S. J. and Evan, G. I. (2000). The Drosophila caspase DRONC is regulated by DIAP1. EMBO J. 19, 598-611.
42. Ohsumi, Y. (2001). Molecular dissection of autophagy: two ubiquitin-like systems. Nat. Rev. Mol. Cell. Biol. 2, 211-216.
43. Piperno, G. and Fuller, M. T. (1985). Monoclonal antibodies specific for an acetylated form of alpha-tubulin recognize the antigen in cilia and flagella from a variety of organisms. J. Cell Biol. 101, 2085-2094.
44. Puthalakath, H., Huang, D. C., O'Reilly, L. A., King, S. M. and Strasser, A. (1999). The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol. Cell 3, 287-296.
45. Puthalakath, H., Villunger, A., O'Reilly, L. A., Beaumont, J. G., Coultas, L., Cheney, R. E., Huang, D. C. and Strasser, A. (2001). Bmf: a proapoptotic BH3-only protein regulated by interaction with the myosin V actin motor complex, activated by anoikis. Science 293, 1829-1832.
46. Quinn, L. M., Dorstyn, L., Mills, K., Colussi, P. A., Chen, P., Coombe, M., Abrams, J., Kumar, S. and Richardson, H. (2000). An essential role for the caspase dronc in developmentally programmed cell death in Drosophila. J. Biol. Chem. 275, 40416-40424.
47. Rao, L., Perez, D. and White, E. (1996). Lamin proteolysis facilitates nuclear events during apoptosis. J. Cell Biol. 135, 1441-1455.
48. Restifo, L. L. and White, K. (1992). Mutations in a steroid hormone-regulated gene disrupt the metamorphosis of internal tissues in Drosophila: salivary glands, muscle, and gut. Wilhelm Roux's Arch. Dev. Biol. 201, 221-234.
49. Rodriguez, A., Oliver, H., Zou, H., Chen, P., Wang, X. and Abrams, J. M. (1999). Dark is a Drosophila homologue of Apaf-1/CED-4 and functions in an evolutionarily conserved death pathway. Nat. Cell Biol. 1, 272-279.
50. Rodriguez, A., Chen, P., Oliver, H. and Abrams, J. M. (2002). Unrestricted caspase-dependent cell death caused by loss of Diap1 function requires the Drosophila Apaf-1 homolog, dark. EMBO J. 21, 2189-2197.
51. Schweichel, J.-U. and Merker, H.-J. (1973). The morphology of various types of cell death in prenatal tissues. Teratology 7, 253-266.
52. Song, Z., McCall, K. and Steller, H. (1997). DCP-1, a Drosophila cell death protease essential for development. Science 275, 536-540.
53. Srinivasula, S. M., Datta, P., Kobayashi, M., Wu, J. W., Fujioka, M., Hegde, R., Zhang, Z., Mukattash, R., Fernandes-Alnemri, T., Shi, Y., Jaynes, J. and Alnemri, E. S. (2002). sickle, a novel Drosophila death gene in the reaper/hid/grim region, encodes an IAP-inhibitory protein. Curr. Biol. 12, 125-130.
54. Stuurman, N., Maus, N. and Fisher, P. A. (1995). Interphase phosphorylation of the Drosophila nuclear lamin: site-mapping using a monoclonal antibody. J. Cell Sci. 108, 3137-3144.
55. Vernooy, S. Y., Copeland, J., Ghaboosi, N., Griffin, E. E., You, S. J. and Hay, B. A. (2000). Cell death regulation in Drosophila: conservation of mechanism and unique insights. J. Cell Biol. 150, F69-F75.
56. Wang, S. L., Hawkins, C. J., Yoo, S. J., Müller, H.-A. J. and Hay, B. A. (1999). The Drosophila caspase inhibitor DIAP1 is essential for cell survival and is negatively regulated by HID. Cell 98, 453-463.
57. White, K., Grether, M. E., Abrams, J. M., Young, L., Farrell, K. and Steller, H. ( 1994). Genetic control of programmed cell death in Drosophila. Science 264, 677-683.
58. Wing, J. P., Karres, J. S., Ogdahl, J. L., Zhou, L., Schwartz, L. M. and Nambu, J. R. (2002). Drosophila sickle is a novel grim-reaper cell death activator. Curr. Biol. 12, 131-135.
59. Woodard, C. T., Baehrecke, E. H. and Thummel, C. S. (1994). A molecular mechanism for the stage-specificity of the Drosophila prepupal genetic response to ecdysone. Cell 79, 607-615.
60. Wu, G., Chai, J., Suber, T. L., Wu, J. W., Do, C., Wang, X. and Shi, Y. (2000). Structural basis of IAP recognition by Smac/DIABLO. Nature 408, 1008-1012.
61. Wu, J. W., Cocina, A. E., Chai, J., Hay, B. A. and Shi, Y. (2001). Structural analysis of a functional DIAP1 fragment bound to grim and hid peptides. Mol. Cell 8, 95-104.
62. Wyllie, A. H. (1980). Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284, 555-556.
63. Yoo, S. J., Huh, J. R., Muro, I., Yu, H., Wang, L., Wang, S. L., Feldman, R. M., Clem, R. J., Muller, H. A. and Hay, B. A. (2002). Hid, Rpr and Grim negatively regulate DIAP1 levels through distinct mechanisms. Nat. Cell Biol. 4, 416-424.
64. Yu, S. Y., Yoo, S. J., Yang, L., Zapata, C., Srinivasan, A., Hay, B. A. and Baker, N. E. (2002). A pathway of signals regulating effector and initiator caspases in the developing Drosophila eye. Development 129, 3269-3278.
65. Zhou, L., Song, Z., Tittel, J. and Steller, H. (1999). HAC-1, a Drosophila homolog of APAF-1 and CED-4, functions in developmental and radiation-induced apoptosis. Mol. Cell 4, 745-755.