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Apoptosis

, Volume 14, Issue 8, pp 943–949 | Cite as

Regulation of Drosophila melanogaster pro-apoptotic gene hid

  • Amber Bilak
  • Tin Tin Su
Apoptosis in Drosophila

Abstract

Key decisions one makes in a lifetime include whether and how often to reproduce, what role to play in the community and, under certain conditions, whether to live or die. Similar decisions are also made at the level of cells: whether to divide, what fate to assume in the multicellular context of metazoan development and, under certain conditions, whether to live or to die. The pro-apoptotic gene hid plays an important role in the execution of cell death in Drosophila. Here, we review the various levels of control that exist to regulate Hid according to the life-or-death choice of a cell.

Keywords

Drosophila Apoptosis hid 

References

  1. 1.
    Bergmann A, Yang AY, Srivastava M (2003) Regulators of IAP function: coming to grips with the grim reaper. Curr Opin Cell Biol 15:717–724PubMedCrossRefGoogle Scholar
  2. 2.
    Hay BA, Guo M (2006) Caspase-dependent cell death in Drosophila. Annu Rev Cell Dev Biol 22:623–650PubMedCrossRefGoogle Scholar
  3. 3.
    Steller H (2008) Regulation of apoptosis in Drosophila. Cell Death Differ 15:1132–1138PubMedCrossRefGoogle Scholar
  4. 4.
    Claveria C, Caminero E, Martinez AC, Campuzano S, Torres M (2002) GH3, a novel proapoptotic domain in Drosophila grim, promotes a mitochondrial death pathway. EMBO J 21:3327–3336PubMedCrossRefGoogle Scholar
  5. 5.
    Wing JP, Schwartz LM, Nambu JR (2001) The RHG motifs of Drosophila reaper and grim are important for their distinct cell death-inducing abilities. Mech Dev 102:193–203PubMedCrossRefGoogle Scholar
  6. 6.
    Zhou L (2005) The ‘unique key’ feature of the Iap-binding motifs in RHG proteins. Cell Death Differ 12:1148–1151PubMedCrossRefGoogle Scholar
  7. 7.
    Freel CD, Richardson DA, Thomenius MJ et al (2008) Mitochondrial localization of reaper to promote inhibitors of apoptosis protein degradation conferred by GH3 domain-lipid interactions. J Biol Chem 283:367–379PubMedCrossRefGoogle Scholar
  8. 8.
    Olson MR, Holley CL, Gan EC, Colon-Ramos DA, Kaplan B, Kornbluth S (2003) A GH3-like domain in reaper is required for mitochondrial localization and induction of IAP degradation. J Biol Chem 278:44758–44768PubMedCrossRefGoogle Scholar
  9. 9.
    Abdelwahid E, Yokokura T, Krieser RJ, Balasundaram S, Fowle WH, White K (2007) Mitochondrial disruption in Drosophila apoptosis. Dev Cell 12:793–806PubMedCrossRefGoogle Scholar
  10. 10.
    White K, Grether ME, Abrams JM, Young L, Farrell K, Steller H (1994) Genetic control of programmed cell death in Drosophila. Science 264:677–683PubMedCrossRefGoogle Scholar
  11. 11.
    Grether ME, Abrams JM, Agapite J, White K, Steller H (1995) The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev 9:1694–1708PubMedCrossRefGoogle Scholar
  12. 12.
    Sen A, Kuruvilla D, Pinto L, Sarin A, Rodrigues V (2004) Programmed cell death and context dependent activation of the EGF pathway regulate gliogenesis in the Drosophila olfactory system. Mech Dev 121:65–78PubMedCrossRefGoogle Scholar
  13. 13.
    Miller DT, Cagan RL (1998) Local induction of patterning and programmed cell death in the developing Drosophila retina. Development 125:2327–2335PubMedGoogle Scholar
  14. 14.
    Sawamoto K, Taguchi A, Hirota Y, Yamada C, Jin M, Okano H (1998) Argos induces programmed cell death in the developing Drosophila eye by inhibition of the Ras pathway. Cell Death Differ 5:548PubMedCrossRefGoogle Scholar
  15. 15.
    Baker NE, Yu SY (2001) The EGF receptor defines domains of cell cycle progression and survival to regulate cell number in the developing Drosophila eye. Cell 104:699–708PubMedCrossRefGoogle Scholar
  16. 16.
    Yu SY, Yoo SJ, Yang L et al (2002) A pathway of signals regulating effector and initiator caspases in the developing Drosophila eye. Development 129:3269–3278PubMedGoogle Scholar
  17. 17.
    Bergmann A, Tugentman M, Shilo BZ, Steller H (2002) Regulation of cell number by MAPK-dependent control of apoptosis: a mechanism for trophic survival signaling. Dev Cell 2:159–170PubMedCrossRefGoogle Scholar
  18. 18.
    Kurada P, White K (1998) Ras promotes cell survival in Drosophila by downregulating hid expression. Cell 95:319–329PubMedCrossRefGoogle Scholar
  19. 19.
    Bergmann A, Agapite J, McCall K, Steller H (1998) The Drosophila gene hid is a direct molecular target of Ras-dependent survival signaling. Cell 95:331–341PubMedCrossRefGoogle Scholar
  20. 20.
    Luo X, Puig O, Hyun J, Bohmann D, Jasper H (2007) Foxo and Fos regulate the decision between cell death and survival in response to UV irradiation. EMBO J 26:380–390PubMedCrossRefGoogle Scholar
  21. 21.
    Udan RS, Kango-Singh M, Nolo R, Tao C, Halder G (2003) Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway. Nat Cell Biol 5:914–920PubMedCrossRefGoogle Scholar
  22. 22.
    Thompson BJ, Cohen SM (2006) The Hippo pathway regulates the bantam microRNA to control cell proliferation and apoptosis in Drosophila. Cell 126:767–774PubMedCrossRefGoogle Scholar
  23. 23.
    Nolo R, Morrison CM, Tao C, Zhang X, Halder G (2006) The bantam microRNA is a target of the hippo tumor-suppressor pathway. Curr Biol 16:1895–1904PubMedCrossRefGoogle Scholar
  24. 24.
    de la Cova C, Abril M, Bellosta P, Gallant P, Johnston LA (2004) Drosophila myc regulates organ size by inducing cell competition. Cell 117:107–116PubMedCrossRefGoogle Scholar
  25. 25.
    Dimova DK, Dyson NJ (2005) The E2F transcriptional network: old acquaintances with new faces. Oncogene 24:2810–2826PubMedCrossRefGoogle Scholar
  26. 26.
    DeGregori J, Johnson DG (2006) Distinct and overlapping roles for E2F family members in transcription, proliferation and apoptosis. Curr Mol Med 6:739–748PubMedGoogle Scholar
  27. 27.
    Moon NS, Frolov MV, Kwon EJ et al (2005) Drosophila E2F1 has context-specific pro- and antiapoptotic properties during development. Dev Cell 9:463–475PubMedCrossRefGoogle Scholar
  28. 28.
    Moon NS, Di Stefano L, Morris EJ, Patel R, White K, Dyson NJ (2008) E2F and p53 induce apoptosis independently during Drosophila development but intersect in the context of DNA damage. PLoS Genet 4:e1000153PubMedCrossRefGoogle Scholar
  29. 29.
    Tanaka-Matakatsu M, Xu J, Cheng L, Du W (2009) Regulation of apoptosis of rbf mutant cells during Drosophila development. Dev Biol 326:347–356PubMedCrossRefGoogle Scholar
  30. 30.
    Du W, Vidal M, Xie JE, Dyson N (1996) RBF, a novel RB-related gene that regulates E2F activity and interacts with cyclin E in Drosophila. Genes Dev 10:1206–1218PubMedCrossRefGoogle Scholar
  31. 31.
    Stevaux O, Dimova D, Frolov MV, Taylor-Harding B, Morris E, Dyson N (2002) Distinct mechanisms of E2F regulation by Drosophila RBF1 and RBF2. EMBO J 21:4927–4937PubMedCrossRefGoogle Scholar
  32. 32.
    Sato K, Hayashi Y, Ninomiya Y et al (2007) Maternal Nanos represses hid/skl-dependent apoptosis to maintain the germ line in Drosophila embryos. Proc Natl Acad Sci USA 104:7455–7460PubMedCrossRefGoogle Scholar
  33. 33.
    Leaman D, Chen PY, Fak J et al (2005) Antisense-mediated depletion reveals essential and specific functions of microRNAs in Drosophila development. Cell 121:1097–1108PubMedCrossRefGoogle Scholar
  34. 34.
    Hipfner DR, Weigmann K, Cohen SM (2002) The bantam gene regulates Drosophila growth. Genetics 161:1527–1537PubMedGoogle Scholar
  35. 35.
    Brennecke J, Hipfner DR, Stark A, Russell RB, Cohen SM (2003) Bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 113:25–36PubMedCrossRefGoogle Scholar
  36. 36.
    Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–655PubMedCrossRefGoogle Scholar
  37. 37.
    Vazquez-Pianzola P, Hernandez G, Suter B, Rivera-Pomar R (2007) Different modes of translation for hid, grim and sickle mRNAs in Drosophila. Cell Death Differ 14:286–295PubMedCrossRefGoogle Scholar
  38. 38.
    Haining WN, Carboy-Newcomb C, Wei CL, Steller H (1999) The proapoptotic function of Drosophila Hid is conserved in mammalian cells. Proc Natl Acad Sci USA 96:4936–4941PubMedCrossRefGoogle Scholar
  39. 39.
    Jiang C, Lamblin AF, Steller H, Thummel CS (2000) A steroid-triggered transcriptional hierarchy controls salivary gland cell death during Drosophila metamorphosis. Mol Cell 5:445–455PubMedCrossRefGoogle Scholar
  40. 40.
    Brodsky MH, Weinert BT, Tsang G et al (2004) Drosophila melanogaster MNK/Chk2 and p53 regulate multiple DNA repair and apoptotic pathways following DNA damage. Mol Cell Biol 24:1219–1231PubMedCrossRefGoogle Scholar
  41. 41.
    Wichmann A, Jaklevic B, Su TT (2006) Ionizing radiation induces caspase-dependent but Chk2- and p53-independent cell death in Drosophila melanogaster. Proc Natl Acad Sci USA 103:9952–9957PubMedCrossRefGoogle Scholar
  42. 42.
    Brodsky MH, Nordstrom W, Tsang G, Kwan E, Rubin GM, Abrams JM (2000) Drosophila p53 binds a damage response element at the reaper locus. Cell 101:103–113PubMedCrossRefGoogle Scholar
  43. 43.
    Zhang Y, Lin N, Carroll PM et al (2008) Epigenetic blocking of an enhancer region controls irradiation-induced proapoptotic gene expression in Drosophila embryos. Dev Cell 14:481–493PubMedCrossRefGoogle Scholar
  44. 44.
    Zhu CC, Bornemann DJ, Zhitomirsky D, Miller EL, O’Connor MB, Simon JA (2008) Drosophila histone deacetylase-3 controls imaginal disc size through suppression of apoptosis. PLoS Genet 4:e1000009PubMedCrossRefGoogle Scholar
  45. 45.
    Wells BS, Yoshida E, Johnston LA (2006) Compensatory proliferation in Drosophila imaginal discs requires Dronc-dependent p53 activity. Curr Biol 16:1606–1615PubMedCrossRefGoogle Scholar
  46. 46.
    Jassim OW, Fink JL, Cagan RL (2003) Dmp53 protects the Drosophila retina during a developmentally regulated DNA damage response. EMBO J 22:5622–5632PubMedCrossRefGoogle Scholar
  47. 47.
    Jaklevic B, Uyetake L, Wichmann A, Bilak A, English CN, Su TT (2008) Modulation of ionizing radiation-induced apoptosis by bantam microRNA in Drosophila. Dev Biol 320:122–130PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.MCD BiologyUniversity of ColoradoBoulderUSA

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