A novel F-box protein is required for caspase activation during cellular remodeling in Drosophila

Development

Volumn 137, Issue 10, 2010, Pages 1679-1688

  Bader, Maya ^a   Arama, Eli ^b   Steller, Hermann ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Caspase; Drosophila; IAP; Proteasome; SCF; Spermatogenesis; Ubiquitin

Indexed keywords

CASPASE; CULLIN; CULLIN 1; F BOX PROTEIN; PROTEASOME; S PHASE KINASE ASSOCIATED PROTEIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DROSOPHILA; ELECTRON MICROSCOPY; ENZYME ACTIVATION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SPERMATOGENESIS;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CASPASES; CELL DIFFERENTIATION; DROSOPHILA; DROSOPHILA PROTEINS; ENZYME ACTIVATION; F-BOX PROTEINS; INFERTILITY, MALE; MALE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; SEQUENCE HOMOLOGY, AMINO ACID; SPERMATOZOA; TESTIS;

MAMMALIA;

EID: 77952192458     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.050088     Document Type: Article

References (68)

1. Abraham, M. C. and Shaham, S. (2004). Death without caspases, caspases without death. Trends Cell Biol. 14, 184-193.
2. 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. (Pubitemid 36564899)
3. Arama, E., Bader, M., Srivastava, M., Bergmann, A. and Steller, H. (2006). The two Drosophila cytochrome C proteins can function in both respiration and caspase activation. EMBO J. 25, 232-243. (Pubitemid 43077311)
4. Arama, E., Bader, M., Rieckhof, G. E. and Steller, H. (2007). A ubiquitin ligase complex regulates caspase activation during sperm differentiation in Drosophila. PLoS Biol. 5, e251.
5. Bader, M. and Steller, H. (2009). Regulation of cell death by the ubiquitin-proteasome system. Curr. Opin. Cell Biol. 21, 878-884.
6. Bartke, T., Pohl, C., Pyrowolakis, G. and Jentsch, S. (2004). Dual role of BRUCE as an antiapoptotic IAP and a chimeric E2/E3 ubiquitin ligase. Mol. Cell 14, 801-811.
7. Bergmann, A. (2010). The role of ubiquitylation for the control of cell death in Drosophila. Cell Death Differ. 17, 61-67.
8. Bre, M. H., Redeker, V., Quibell, M., Darmanaden-Delorme, J., Bressac, C., Cosson, J., Huitorel, P., Schmitter, J. M., Rossler, J., Johnson, T. et al. (1996). Axonemal tubulin polyglycylation probed with two monoclonal antibodies: widespread evolutionary distribution, appearance during spermatozoan maturation and possible function in motility. J. Cell Sci. 109, 727-738.
9. Bre, M. H., Redeker, V., Vinh, J., Rossier, J. and Levilliers, N. (1998). Tubulin polyglycylation: differential posttranslational modification of dynamic cytoplasmic and stable axonemal microtubules in paramecium. Mol. Biol. Cell 9, 2655-2665. (Pubitemid 28425900)
10. Broemer, M. and Meier, P. (2009). Ubiquitin-mediated regulation of apoptosis. Trends Cell Biol. 19, 130-140.
11. Cardozo, T. and Pagano, M. (2004). The SCF ubiquitin ligase: insights into a molecular machine. Nat. Rev. Mol. Cell Biol. 5, 739-751. (Pubitemid 39208183)
12. Chang, Y. F., Cheng, C. M., Chang, L. K., Jong, Y. J. and Yoo, C. Y. (2006). The F-box protein Fbxo7 interacts with human inhibitor of apoptosis protein cIAP1 and promotes cIAP1 ubiquitination. Biochem. Biophys. Res. Commun. 342, 1022-1026.
13. Derry, W. B., Putzke, A. P. and Rothman, J. H. (2001). Caenorhabditis elegans p53: role in apoptosis, meiosis, and stress resistance. Science 294, 591-595. (Pubitemid 32999555)
14. Deveraux, Q. L. and Reed, J. C. (1999). IAP family proteins-suppressors of apoptosis. Genes Dev. 13, 239-252.
15. Ditzel, M., Broemer, M., Tenev, T., Bolduc, C., Lee, T. V., Rigbolt, K. T., Elliott, R., Zvelebil, M., Blagoev, B., Bergmann, A. et al. (2008). Inactivation of effector caspases through nondegradative polyubiquitylation. Mol. Cell 32, 540-553.
16. Fan, Y. and Bergmann, A. (2009). The cleaved-Caspase-3 antibody is a marker of Caspase-9-like DRONC activity in Drosophila. Cell Death Differ. 17, 534-539.
17. Feinstein-Rotkopf, Y. and Arama, E. (2009). Can't live without them, can live with them: roles of caspases during vital cellular processes. Apoptosis 14, 980-995.
18. Fuller, M. T. (1993). The Development of Drosophila melanogaster: Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
19. Glickman, M. H. and Raveh, D. (2005). Proteasome plasticity. FEBS Lett. 579, 3214-3223.
20. 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. (Pubitemid 30093732)
21. Haglund, K. and Dikic, I. (2005). Ubiquitylation and cell signaling. EMBO J. 24, 3353-3359.
22. Hanahan, D. and Weinberg, R. A. (2000). The hallmarks of cancer. Cell 100, 57-70.
23. Hao, Y., Sekine, K., Kawabata, A., Nakamura, H., Ishioka, T., Ohata, H., Katayama, R., Hashimoto, C., Zhang, X., Noda, T. et al. (2004). Apollon ubiquitinates SMAC and caspase-9, and has an essential cytoprotection function. Nat. Cell Biol. 6, 849-860.
24. 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.
25. Hays, R., Wickline, L. and Cagan, R. (2002). Morgue mediates apoptosis in the Drosophila melanogaster retina by promoting degradation of DIAP1. Nat. Cell Biol. 4, 425-431. (Pubitemid 34746160)
26. Hime, G. R., Brill, J. A. and Fuller, M. T. (1996). Assembly of ring canals in the male germ line from structural components of the contractile ring. J. Cell Sci. 109, 2779-2788.
27. Hinds, M. G., Norton, R. S., Vaux, D. L. and Day, C. L. (1999). Solution structure of a baculoviral inhibitor of apoptosis (IAP) repeat. Nat. Struct. Biol. 6, 648-651.
28. Huh, J. R., Vernooy, S. Y., Yu, H., Yan, N., Shi, Y., Guo, M. and Hay, B. A. (2004). Multiple apoptotic caspase cascades are required in nonapoptotic roles for Drosophila spermatid individualization. PLoS Biol. 2, E15.
29. Jiang, J. (2006). Regulation of Hh/Gli signaling by dual ubiquitin pathways. Cell Cycle 5, 2457-2463. (Pubitemid 44785822)
30. Jin, Z., Li, Y., Pitti, R., Lawrence, D., Pham, V. C., Lill, J. R. and Ashkenazi, A. (2009). Cullin3-based polyubiquitination and p62-dependent aggregation of caspase-8 mediate extrinsic apoptosis signaling. Cell 137, 721-735.
31. Kipreos, E. T. and Pagano, M. (2000). The F-box protein family. Genome Biol. 1, REVIEWS3002.
32. Kirk, R., Laman, H., Knowles, P. P., Murray-Rust, J., Lomonosov, M., Meziane, xEl K. and McDonald, N. Q. (2008). Structure of a conserved dimerization domain within the F-box protein Fbxo7 and the PI31 proteasome inhibitor. J. Biol. Chem. 283, 22325-22335.
33. Kleino, A., Valanne, S., Ulvila, J., Kallio, J., Myllymäki, H., Enwald, H., Stöven, S., Poidevin, M., Ueda, R., Hultmark, D. et al. (2005). Inhibitor of apoptosis 2 and TAK1-binding protein are components of the Drosophila Imd pathway. EMBO J. 24, 3423-3434.
34. Kornbluth, S. and White, K. (2005). Apoptosis in Drosophila: neither fish nor fowl (nor man, nor worm). J. Cell Sci. 118, 1779-1787.
35. Kuo, C. T., Zhu, S., Younger, S., Jan, L. Y. and Jan, Y. N. (2006). Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron 51, 283-290. (Pubitemid 44118716)
36. Kuranaga, E. and Miura, M. (2007). Nonapoptotic functions of caspases: caspases as regulatory molecules for immunity and cell-fate determination. Trends Cell Biol. 17, 135-144. (Pubitemid 46341825)
37. Lee, T. V., Ding, T., Chen, Z., Rajendran, V., Scherr, H., Lackey, M., Bolduc, C. and Bergmann, A. (2008). The E1 ubiquitin-activating enzyme Uba1 in Drosophila controls apoptosis autonomously and tissue growth non-autonomously. Development 135, 43-52. (Pubitemid 351201480)
38. Lehmann, R. and Nusslein-Volhard, C. (1986). Abdominal segmentation, pole cell formation, and embryonic polarity require the localized activity of oskar, a maternal gene in Drosophila. Cell 47, 141-152.
39. Lisi, S., Mazzon, I. and White, K. (2000). Diverse domains of THREAD/DIAP1 are required to inhibit apoptosis induced by REAPER and HID in Drosophila. Genetics 154, 669-678. (Pubitemid 30096589)
40. Lotz, K., Pyrowolakis, G. and Jentsch, S. (2004). BRUCE, a giant E2/E3 ubiquitin ligase and inhibitor of apoptosis protein of the trans-Golgi network, is required for normal placenta development and mouse survival. Mol. Cell. Biol. 24, 9339-9350. (Pubitemid 39391672)
41. Muro, I., Berry, D. L., Huh, J. R., Chen, C. H., Huang, H., Yoo, S. J., Guo, M., Baehrecke, E. H. and Hay, B. A. (2006). The Drosophila caspase Ice is important for many apoptotic cell deaths and for spermatid individualization, a nonapoptotic process. Development 133, 3305-3315. (Pubitemid 44501833)
42. Nikolaev, A., McLaughlin, T., O'Leary, D. D. and Tessier-Lavigne, M. (2009). APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 457, 981-989.
43. Noguchi, T. and Miller, K. G. (2003). A role for actin dynamics in individualization during spermatogenesis in Drosophila melanogaster. Development 130, 1805-1816.
44. Ou, C. Y., Lin, Y. F., Chen, Y. J. and Chien, C. T. (2002). Distinct protein degradation mechanisms mediated by Cul1 and Cul3 controlling Ci stability in Drosophila eye development. Genes Dev. 16, 2403-2414.
45. Reed, J. C. (2003). Apoptosis-targeted therapies for cancer. Cancer Cell 3, 17-22.
46. Ribeiro, P. S., Kuranaga, E., Tenev, T., Leulier, F., Miura, M. and Meier, P. (2007). DIAP2 functions as a mechanism-based regulator of drICE that contributes to the caspase activity threshold in living cells. J. Cell Biol. 179, 1467-1480.
47. Rogowski, K., Juge, F., van Dijk, J., Wloga, D., Strub, J. M., Levilliers, N., Thomas, D., Bre, M. H., Van Dorsselaer, A., Gaertig, J. et al. (2009). Evolutionary divergence of enzymatic mechanisms for posttranslational polyglycylation. Cell 137, 1076-1087.
48. Ryoo, H. D., Bergmann, A., Gonen, H., Ciechanover, A. and Steller, H. (2002). Regulation of Drosophila IAP1 degradation and apoptosis by reaper and ubcD1. Nat. Cell Biol. 4, 432-438.
49. Salvesen, G. S. and Duckett, C. S. (2002). IAP proteins: blocking the road to death's door. Nat. Rev. Mol. Cell Biol. 3, 401-410.
50. Santel, A., Winhauer, T., Blümer, N. and Renkawitz-Pohl, R. (1997). The Drosophila don juan (dj) gene encodes a novel sperm specific protein component characterized by an unusual domain of a repetitive amino acid motif. Mech. Dev. 64, 19-30. (Pubitemid 27351513)
51. Santel, A., Blumer, N., Kampfer, M. and Renkawitz-Pohl, R. (1998). Flagellar mitochondrial association of the male-specific Don Juan protein in Drosophila spermatozoa. J. Cell Sci. 111, 3299-3309. (Pubitemid 28563033)
52. Schile, A. J., Garcia-Fernandez, M. and Steller, H. (2008). Regulation of apoptosis by XIAP ubiquitin-ligase activity. Genes Dev. 22, 2256-2266.
53. Schreader, B. A., Wang, Y. and Nambu, J. R. (2003). Drosophila morgue and the intersection between protein ubiquitination and programmed cell death. Apoptosis 8, 129-139. (Pubitemid 36547100)
54. Schumacher, B., Hofmann, K., Boulton, S. and Gartner, A. (2001). The C. elegans homolog of the p53 tumor suppressor is required for DNA damage-induced apoptosis. Curr. Biol. 11, 1722-1727. (Pubitemid 33037787)
55. Steller, H. (1995). Mechanisms and genes of cellular suicide. Science 267, 1445-1449.
56. Steller, H. (2008). Regulation of apoptosis in Drosophila. Cell Death Differ. 15, 1132-1138.
57. Thompson, C. B. (1995). Apoptosis in the pathogenesis and treatment of disease. Science 267, 1456-1462.
58. Tokuyasu, K. T., Peacock, W. J. and Hardy, R. W. (1972). Dynamics of spermiogenesis in Drosophila melanogaster. I. Individualization process. Z. Zellforsch. Mikrosk. Anat. 124, 479-506.
59. Vaux, D. L. and Silke, J. (2005). IAPs, RINGs and ubiquitylation. Nat. Rev. Mol. Cell Biol. 6, 287-297.
60. Vernooy, S. Y., Chow, V., Su, J., Verbrugghe, K., Yang, J., Cole, S., Olson, M. R. and Hay, B. A. (2002). Drosophila Bruce can potently suppress Rpr- and Grim-dependent but not Hid-dependent cell death. Curr. Biol. 12, 1164-1168. (Pubitemid 34766942)
61. Vucic, D. (2008). Targeting IAP (inhibitor of apoptosis) proteins for therapeutic intervention in tumors. Curr. Cancer Drug Targets 8, 110-117.
62. Wakimoto, B. T., Lindsley, D. L. and Herrera, C. (2004). Toward a comprehensive genetic analysis of male fertility in Drosophila melanogaster. Genetics 167, 207-216.
63. Williams, D. W., Kondo, S., Krzyzanowska, A., Hiromi, Y. and Truman, J. W. (2006). Local caspase activity directs engulfment of dendrites during pruning. Nat. Neurosci. 9, 1234-1236.
64. Wilson, R., Goyal, L., Ditzel, M., Zachariou, A., Baker, D. A., Agapite, J., Steller, H. and Meier, P. (2002). The DIAP1 RING finger mediates ubiquitination of Dronc and is indispensable for regulating apoptosis. Nat. Cell Biol. 4, 445-450.
65. 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. et al. (2002). Drosophila Morgue is an F box/ubiquitin conjugase domain protein important for grim-reaper mediated apoptosis. Nat. Cell Biol. 4, 451-456.
66. Yang, Y., Fang, S., Jensen, J. P., Weissman, A. M. and Ashwell, J. D. (2000). Ubiquitin protein ligase activity of IAPs and their degradation in proteasomes in response to apoptotic stimuli. Science 288, 874-877.
67. Yi, C. H. and Yuan, J. (2009). The Jekyll and Hyde functions of caspases. Dev. Cell 16, 21-34.
68. Zhong, L. and Belote, J. M. (2007). The testis-specific proteasome subunit Prosalpha6T of D. melanogaster is required for individualization and nuclear maturation during spermatogenesis. Development 134, 3517-3525.