Differential localization and processing of apoptotic proteins in Malpighian tubules of Drosophila during metamorphosis

European Journal of Cell Biology

Volumn 90, Issue 1, 2011, Pages 72-80

  Shukla, Anukampa ^a   Tapadia, Madhu G ^a  

^a BANARAS HINDU UNIVERSITY   (India)

Author keywords

Apoptosis; Caspases; Drosophila; Malpighian tubules; Metamorphosis

Indexed keywords

APOPTOSIS REGULATORY PROTEIN; DRICE PROTEIN; DRONC PROTEIN; GRIM PROTEIN; HEAD INVOLUTION DEFECTIVE PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; DROSOPHILA; LARVA; LETHALITY; MALPIGHIAN TUBULE; METAMORPHOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PUPA (LIFE CYCLE STAGE);

ANIMALS; APOPTOSIS; CASPASES; CELL NUCLEUS; DROSOPHILA; DROSOPHILA PROTEINS; ECDYSONE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; INHIBITOR OF APOPTOSIS PROTEINS; LARVA; MALPIGHIAN TUBULES; METAMORPHOSIS, BIOLOGICAL; MICROSCOPY, CONFOCAL; NEUROPEPTIDES; PROTEIN TRANSPORT; PUPA;

EID: 78649480734     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejcb.2010.08.010     Document Type: Article

References (54)

1. Abrams J.M. An emerging blueprint for apoptosis in Drosophila. Trends Cell Biol. 1999, 9:435-440.
2. Baliga B.C., Colussi P.A., Read S.H., Dias M.M., Jans D.A., Kumar S. Role of prodomain in importin-mediated nuclear localization and activation of caspase-2. J. Biol. Chem. 2003, 278:4899-4905.
3. Berendes H.D., Willart E. Ecdysone-related changes at the nuclear and cytoplasmic level of Malpighian tubule cells in Drosophila. Insect Physiol. 1971, 17:2337-2350.
4. Bergmann A., Agapite J., McCall K., Steller H. The Drosophila gene hid is a direct molecular target of Ras-dependent survival signaling. Cell 1998, 95:331-341.
5. Bodenstein D. The postembryonic development of Drosophila. Biology of Drosophila 1965, 275-367. Hafner Publishing, New York. M. Demerc (Ed.).
6. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
7. Cakouros D., Daish T.J., Kumar S. Ecdysone receptor directly binds the promotor of Drosophila caspase DRONC regulating its expression in specific tissue. J. Cell Biol. 2004, 165:631-640.
8. Chen P., Nordstrom W., Gish B., Abrams J.M. Grim, a novel cell death gene in Drosophila. Genes Dev. 1996, 10:1773-1782.
9. Christich A., Kauppila S., Chen P., Sogame N., Ho S.I., Abrams J.M. The damage-responsive Drosophila gene sickle encodes a novel IAP binding protein similar to but distinct from reaper, grim, and hid. Curr. Biol. 2002, 12:137-140.
10. Claveria C., Albar J.P., Serrano A., Buesa J.M., Barbero J.L., Martínez-A C., Torres M. Drosophila grim induces apoptosis in mammalian cells. EMBO J. 1998, 17:7199-7208.
11. Cryns V., Yuan J. Proteases to die for. Genes Dev. 1998, 12:1551-1570.
12. Daish T.J., Mills K., Kumar S. Drosophila caspase DRONC is required for specific developmental cell death pathways and stress-induced apoptosis. Dev. Cell 2004, 7:909-915.
13. Deveraux Q.L., Reed J.L. IAP family proteins - suppressors of apoptosis. Genes Dev. 1999, 13:239-252.
14. Ditzel M., Wilson R., Tenev T., Zacharious A., Deas E., Meir P. Degradation of DIAP1 by the N-end rule pathway is essential for regulating apoptosis. Nat. Cell Biol. 2003, 5:467-473.
15. Dorstyn L., Kumar S. A biochemical analysis of the activation of the Drosophila caspase DRONC. Cell Death Differ. 2008, 15:461-470.
16. Dorstyn L., Colussi P.A., Quinn L.M., Richardson H., Kumar S. DRONC, an ecdysone-inducible Drosophila caspase. Proc. Natl. Acad. Sci. 1999, 96:4307-4312.
17. Dow J.A., Davies S.A., Guo Y., Graham S., Finbow M.E., Kaiser K. Molecular genetic analysis of V-ATPase function in Drosophila melanogaster. J. Exp. Biol. 1997, 200:237-245.
18. Fraser A.G., McCarthy N.J., Evan G.I. DRICE is an essential caspase required for apoptotic activity in Drosophila cells. EMBO J. 1997, 16:6192-6199.
19. Goyal L., McCall K., Agapite J., Hartwieg E., Steller H. Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. EMBO J. 2000, 19:589-597.
20. Grether M.E., Abrams J.M., Agapite J., White K., Steller H. The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev. 1995, 9:1694-1708.
21. Harvey A.J., Bidwai A.P., Miller L.K. ch-IAP, a member of the inhibitor of apoptosis protein family is a mediator of the antiapoptotic activity of the v-rel oncoprotein. Mol. Cell Biol. 1997, 17:7328-7431.
22. Hawkins C.J., Yoo S.J., Peterson E.P., Wang S.L., Vernooy S.Y., Hay B.A. The Drosophila caspase DRONC cleaves following glutamate or aspartate and is regulated by DIAP1, HID, and GRIM. J. Biol. Chem. 2000, 275:27084-27093.
23. Hay B.A., Guo M. Caspase dependent cell death in Drosophila. Annu. Rev. Cell Dev. Biol. 2006, 22:623-650.
24. Hay B.A., Wassarman D.A., Rubin G.M. Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 1995, 83:1253-1262.
25. Hay B., Huh J.R., Guo M. The genetics of cell death: approaches insight and opportunities in Drosophila. Nat. Gene. Rev. 2004, 5:911-922.
26. Horner M.A., Chen T., Thummel C.S. Ecdysteroid regulation and DNA binding properties of Drosophila nuclear hormone receptor superfamily members. Dev. Biol. 1995, 168:490-502.
27. Hu X., Cherbas L., Cherbas P. Transcription activation by the ecdysone receptor (EcR/USP): identification of activated functions. Mol. Endocrinol. 2003, 17:716-731.
28. Huh J.R., Vernooy S.Y., Yu H., Yan N., Shi Y., Guo M., Hay B.A. Multiple apoptotic caspase cascades are required in nonapoptotic roles for Drosophila spermatid individualization. PLoS Biol. 2004, 2:43-53.
29. Igaki T., Yamamoto-Goto Y., Tokushige N., Kanda H., Miura M. Down-regulation of DIAP1 triggers a novel Drosophila cell death pathway mediated by dark and DRONC. J. Biol. Chem. 2002, 277:23103-23106.
30. Jacobson M.D., Weil M., Raff M.C. Programmed cell death in animal development. Cell 1997, 88:347-354.
31. Jiang C., Baehrecke E., Thummel C. Steroid regulated programmed cell death during Drosophila metamorphosis. Development 1997, 124:4673-4683.
32. Kaiser W.J., Vucic D., Miller L.K. The Drosophila inhibitor of apoptosis DIAP1 suppresses cell death induced by the caspase DRICE. FEBS Lett. 1998, 440:243-248.
33. Kilpatrick Z.E., Cakouros D., Kumar S. Ecdysone-mediated up-regulation of the effector caspase DRICE is required for hormone-dependent apoptosis in Drosophila cells. J. Biol. Chem. 2005, 280:1981-11986.
34. Meier P., Silke J., Leevers S.J., Evan G.I. The Drosophila caspase DRONC is regulated by DIAP1. EMBO J. 2000, 19:598-611.
35. Muro I., Hay B.A., Clem R.J. The Drosophila DIAP1 protein is required to prevent accumulation of a continuously generated, processed form of the apical caspase DRONC. J. Biol. Chem. 2002, 277:49644-49650.
36. Muro I., Monser K., Clem R.J. Mechanism of Dronc activation in Drosophila cells. J. Cell Sci. 2004, 117:5035-5041.
37. Muro I., Means J.C., Clem R.J. Cleavage of the apoptosis inhibitor DIAP1 by the apical caspase DRONC in both normal and apoptotic Drosophila cells. J. Biol. Sci. 2005, 280:18683-18688.
38. Riddiford L.M. Hormones and Drosophila development. The Development of Drosophila melanogaster 1993, vol. 2:899-940. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
39. Shi Y. Caspase activation, inhibition, and reactivation: a mechanistic view. Protein Sci. 2004, 13:1979-1987.
40. Silke J.H., Kratina T., Ekert P.G., Pakusch M., Vaux D.L. Unlike Diablo/smac, grim promotes global ubiquitination and specific degradation of XIAP and neither cause apoptosis. J. Biol. Chem. 2004, 279:4313-4321.
41. Singh S.R., Liu W., Hou S.X. The adult Drosophila Malpighian tubules are maintained by multipotent stem cells. Cell Stem Cell 2007, 1:191-203.
42. Snipas S.J., Drag M., Stennicke H.R., Salvesen G.S. Activation mechanism and substrate specificity of the Drosophila initiator caspase DRONC. Cell Death Differ. 2008, 15:938-945.
43. Spradling A.C., Rubin G.M. The effect of chromosomal position on the expression of the Drosophila xanthine dehydrogenase gene. Cell 1983, 34:47-57.
44. Spreij T.E. Cell death during the development of imaginal discs of Calliphora erythrocephala. Neth. J. Zool. 1971, 21:221-264.
45. 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.B., Alnemri E.S. Sickle, a novel Drosophila death gene in the reaper/hid/grim region, encodes an IAP-inhibitory protein. Curr. Biol. 2002, 12:125-130.
46. White K., Grether M.E., Abrams J.M., Young L., Farrell K., Steller H. Genetic control of programmed cell death in Drosophila. Science 1994, 264:677-683.
47. Wilde A., Zheng Y. Ran out of the nucleus for apoptosis. Nat. Cell Biol. 2009, 11:11-12.
48. Wing J.P., Karres J.S., Ogdahl J.L., Zhou L., Schwartz L.M., Nambu J.R. Drosophila sickle is a novel grim-reaper cell death activator. Curr. Biol. 2002, 12:131-135.
49. Wong C.H., Chan H., Ho C.Y., Lai S.K., Chan K.S., Koh C.G., Li H.Y. Apoptotic histone modification inhibits nuclear transport by regulating RCC1. Nat. Cell Biol. 2009, 11:32-45.
50. Xu D., Li Y., Arcaro M., Lackey M., Bergmann A. The CARD-carrying caspase Dronc is essential for most, but not all, developmental cell death in Drosophila. Development 2005, 132:2125-2134.
51. Yan N., Huh J.R., Schirf V., Demeler B., Hay B.A., Shi Y. Structure and activation mechanism of the Drosophila initiator caspase Dronc. J. Biol. Chem. 2006, 281:8667-8674.
52. Yao T.P., Forman B.M., Jiang Z., Cherbas L., Chen J.D., Mckeown M., Cherbas P., Evans R.M. Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature 1993, 366:476-479.
53. Yin V.P., Thummel C.S. A balance between the Diap1 death inhibitor and reaper and hid death inducers control steroid triggered cell death in Drosophila. Proc. Natl. Acad. Sci. 2004, 101:8022-8027.
54. Zhivotovsky B., Samali A., Gahm A., Orrenius S. Caspases: their intracellular localization and translocation during apoptosis. Cell Death Differ. 1999, 6:644-651.