POSH misexpression induces caspase-dependent cell death in Drosophila

Developmental Dynamics

Volumn 239, Issue 2, 2010, Pages 665-671

  Lennox, Ashley L ^a   Stronach, Beth ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Caspase; JNk pathway; Scaffold

Indexed keywords

CASPASE 9; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; MIXED LINEAGE KINASE; PLENTY OF SH3 DOMAIN PROTEIN; PROTEIN SH3; SCAFFOLD PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; UNCLASSIFIED DRUG;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL SURVIVAL; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; IMAGINAL DISC; IN SITU HYBRIDIZATION; INNATE IMMUNITY; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

EID: 75149144454     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22188     Document Type: Article

References (84)

1. Abrams JM, White K, Fessler LI, Steller H. 1993. Programmed cell death during Drosophila embryogenesis. Development 117:29-43.
2. Adachi-Yamada T, Nakamura M, Irie K, Tomoyasu Y, Sano Y, Mori E, Goto S, Ueno N, Nishida Y, Matsumoto K. 1999. p38 mitogen-activated protein kinase can be involved in transforming growth factor beta superfamily signal transduction in Drosophila wing morphogenesis. Mol Cell Biol 19:2322-2329.
3. Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
4. Brown S, Hu N, Hombria JC. 2003. Novel level of signalling control in the JAK/ STAT pathway revealed by in situ visualisation of protein-protein interaction during Drosophila development. Development 130:3077-3084.
5. Bruckner K, Kockel L, Duchek P, Luque CM, Rorth P, Perrimon N. 2004. The PDGF/VEGF receptor controls blood cell survival in Drosophila. Dev Cell 7: 73-84.
6. Brun S, Vidal S, Spellman P, Takahashi K, Tricoire H, Lemaitre B. 2006. The MAPKKK Mekk1 regulates the expression of Turandot stress genes in response to septic injury in Drosophila. Genes Cells 11:397-407.
7. Calleja M, Moreno E, Pelaz S, Morata G. 1996. Visualization of gene expression in living adult Drosophila. Science 274: 252-255.
8. Chen P, Nordstrom W, Gish B, Abrams JM. 1996. grim, a novel cell death gene in Drosophila. Genes Dev 10:1773-1782.
9. Chen W, White MA, Cobb MH. 2002. Stimulus-specific requirements for MAP3 kinases in activating the JNK pathway. J Biol Chem 277:49105-49110.
10. Chew SK, Akdemir F, Chen P, Lu WJ, Mills K, Daish T, Kumar S, Rodriguez A, Abrams JM. 2004. The apical caspase dronc governs programmed and unprogrammed cell death in Drosophila. Dev Cell 7:897-907.
11. Collins CA, Wairkar YP, Johnson SL, DiAntonio A. 2006. Highwire restrains synaptic growth by attenuating a MAP kinase signal. Neuron 51:57-69.
12. Delaney JR, Stoven S, Uvell H, Anderson KV, Engstrom Y, Mlodzik M. 2006. Cooperative control of Drosophila immune responses by the JNK and NF-kappaB signaling pathways. EMBO J 25: 3068-3077.
13. Dhanasekaran DN, Kashef K, Lee CM, Xu H, Reddy EP. 2007. Scaffold proteins of MAP-kinase modules. Oncogene 26: 3185-3202.
14. Elion EA. 2001. The Ste5p scaffold. J Cell Sci 114:3967-3978.
15. Fernandez BG, Arias AM, Jacinto A. 2007. Dpp signalling orchestrates dorsal closure by regulating cell shape changes both in the amnioserosa and in the epidermis. Mech Dev 124:884-897.
16. Figueroa C, Tarras S, Taylor J, Vojtek AB. 2003. Akt2 negatively regulates assembly of the POSH-MLK-JNK signaling complex. J Biol Chem 278: 47922-47927.
17. Frank LH, Rushlow C. 1996. A group of genes required for maintenance of the amnioserosa tissue in Drosophila. Development 122:1343-1352.
18. Glise B, Bourbon H, Noselli S. 1995. hemipterous encodes a novel Drosophila MAP kinase kinase, required for epithelial cell sheet movement. Cell 83: 451-461.
19. Gorfinkiel N, Blanchard GB, Adams RJ, Martinez Arias A. 2009. Mechanical control of global cell behaviour during dorsal closure in Drosophila. Development 136:1889-1898.
20. Goyal L, McCall K, Agapite J, Hartwieg E, Steller H. 2000. Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. EMBO J 19:589-597.
21. 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: 1694-1708.
22. Harden N, Ricos M, Ong YM, Chia W, Lim L. 1999. Participation of small GTPases in dorsal closure of the Drosophila embryo: distinct roles for Rho subfamily proteins in epithelial morphogenesis. J Cell Sci 112:273-284.
23. Harden N, Ricos M, Yee K, Sanny J, Langmann C, Yu H, Chia W, Lim L. 2002. Drac1 and Crumbs participate in amnioserosa morphogenesis during dorsal closure in Drosophila. J Cell Sci 115:2119-2129.
24. Hay BA, Wolff T, Rubin GM. 1994. Expression of baculovirus P35 prevents cell death in Drosophila. Development 120:2121-2129.
25. Homsy JG, Jasper H, Peralta XG, Wu H, Kiehart DP, Bohmann D. 2006. JNK signaling coordinates integrin and actin functions during Drosophila embryogenesis. Dev Dyn 235:427-434.
26. Igaki T, Kanda H, Yamamoto-Goto Y, Kanuka H, Kuranaga E, Aigaki T, Miura M. 2002. Eiger, a TNF superfamily ligand that triggers the Drosophila JNK pathway. EMBO J 21:3009-3018.
27. Inoue H, Tateno M, Fujimura-Kamada K, Takaesu G, Adachi-Yamada T, Ninomiya-Tsuji J, Irie K, Nishida Y, Matsumoto K. 2001. A Drosophila MAPKKK, D-MEKK1, mediates stress responses through activation of p38 MAPK. EMBO J 20:5421-5430.
28. Kanda H, Igaki T, Kanuka H, Yagi T, Miura M. 2002. Wengen, a member of the Drosophila tumor necrosis factor receptor superfamily, is required for Eiger signaling. J Biol Chem 277: 28372-28375.
29. Kiehart DP, Galbraith CG, Edwards KA, Rickoll WL, Montague RA. 2000. Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J Cell Biol 149:471-490.
30. Kim GH, Park E, Kong YY, Han JK. 2006. Novel function of POSH, a JNK scaffold, as an E3 ubiquitin ligase for the Hrs stability on early endosomes. Cell Signal 18:553-563.
31. Kosman D, Small S, Reinitz J. 1998. Rapid preparation of a panel of polyclonal antibodies to Drosophila segmentation proteins. Dev Genes Evol 208: 290-294.
32. Kukekov NV, Xu Z, Greene LA. 2006. Direct interaction of the molecular scaffolds POSH and JIP is required for apoptotic activation of JNKs. J Biol Chem 281:15517-15524.
33. Kuranaga E, Kanuka H, Igaki T, Sawamoto K, Ichijo H, Okano H, Miura M. 2002. Reaper-mediated inhibition of DIAP1-induced DTRAF1 degradation results in activation of JNK in Drosophila. Nat Cell Biol 4:705-710.
34. Leulier F, Rodriguez A, Khush RS, Abrams JM, Lemaitre B. 2000. The Drosophila caspase Dredd is required to resist gram-negative bacterial infection. EMBO Rep 1:353-358.
35. Lyons TR, Thorburn J, Ryan PW, Thorburn A, Anderson SM, Kassenbrock CK. 2007. Regulation of the pro-apoptotic scaffolding protein POSH by Akt. J Biol Chem 282:21987-21997.
36. Manseau L, Baradaran A, Brower D, Budhu A, Elefant F, Phan H, Philp AV, Yang M, Glover D, Kaiser K, Palter K, Selleck S. 1997. GAL4 enhancer traps expressed in the embryo, larval brain, imaginal discs, and ovary of Drosophila. Dev Dyn 209:310-322.
37. Maroney AC, Finn JP, Bozyczko-Coyne D, O'Kane TM, Neff NT, Tolkovsky AM, Park DS, Yan CY, Troy CM, Greene LA. 1999. CEP-1347 (KT7515), an inhibitor 662 LENNOX AND STRONACH of JNK activation, rescues sympathetic neurons and neuronally differentiated PC12 cells from death evoked by three distinct insults. J Neurochem 73: 1901-1912.
38. Martin-Blanco E, Gampel A, Ring J, Virdee K, Kirov N, Tolkovsky AM, Martinez-Arias A. 1998. puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev 12:557-570.
39. Meier P, Silke J, Leevers SJ, Evan GI. 2000. The Drosophila caspase DRONC is regulated by DIAP1. EMBO J 19: 598-611.
40. Mihaly J, Kockel L, Gaengel K, Weber U, Bohmann D, Mlodzik M. 2001. The role of the Drosophila TAK homologue dTAK during development. Mech Dev 102:67-79.
41. Mohseni N, McMillan SC, Chaudhary R, Mok J, Reed BH. 2009. Autophagy promotes caspase-dependent cell death during Drosophila development. Autophagy 5;329-338.
42. Moreno E, Yan M, Basler K. 2002. Evolution of TNF signaling mechanisms: JNK-dependent apoptosis triggered by Eiger, the Drosophila homolog of the TNF superfamily. Curr Biol 12:1263-1268.
43. Morrison DK, Davis RJ. 2003. Regulation of MAP kinase signaling modules by scaffold proteins in mammals. Annu Rev Cell Dev Biol 19:91-118.
44. Narasimha M, Brown NH. 2004. Novel functions for integrins in epithelial morphogenesis. Curr Biol 14:381-385.
45. Oda H, Tsukita S. 1999. Dynamic features of adherens junctions during Drosophila embryonic epithelial morphogenesis revealed by a Dalpha-catenin-GFP fusion protein. Dev Genes Evol 209:218-225.
46. Patel NH. 1994. Imaging neuronal subsets and other cell types in wholemount Drosophila embryos and larvae using antibody probes. In: Goldstein LSB, Fyrberg EA, editors. Drosophila melanogaster: practical uses in cell and molecular biology. San Diego: Academic Press. p446-487.
47. Polaski S, Whitney L, Barker BW, Stronach B. 2006. Genetic analysis of slipper/ mixed lineage kinase reveals requirements in multiple Jun-N-terminal kinase-dependent morphogenetic events during Drosophila development. Genetics 174:719-733.
48. Quinn LM, Dorstyn L, Mills K, Colussi PA, Chen P, Coombe M, Abrams J, Kumar S, Richardson H. 2000. An essential role for the caspase dronc in developmentally programmed cell death in Drosophila. J Biol Chem 275: 40416-40424.
49. Reed BH, Wilk R, Lipshitz HD. 2001. Downregulation of Jun kinase signaling in the amnioserosa is essential for dorsal closure of the Drosophila embryo. Curr Biol 11:1098-1108.
50. Reed BH, Wilk R, Schock F, Lipshitz HD. 2004. Integrin-dependent apposition of Drosophila extraembryonic membranes promotes morphogenesis and prevents anoikis. Curr Biol 14:372-380.
51. Reim I, Lee HH, Frasch M. 2003. The Tbox-encoding Dorsocross genes function in amnioserosa development and the patterning of the dorsolateral germ band downstream of Dpp. Development 130:3187-3204.
52. Riesgo-Escovar JR, Hafen E. 1997. Drosophila Jun kinase regulates expression of decapentaplegic via the ETS-domain protein Aop and the AP-1 transcription factor DJun during dorsal closure. Genes Dev 11:1717-1727.
53. Riesgo-Escovar JR, Jenni M, Fritz A, Hafen E. 1996. The Drosophila Jun-Nterminal kinase is required for cell morphogenesis but not for DJun-dependent cell fate specification in the eye. Genes Dev 10:2759-2768.
54. Salvesen GS, Abrams JM. 2004. Caspase activation - stepping on the gas or releasing the brakes? Lessons from humans and flies. Oncogene 23:2774-2784.
55. Schnorr JD, Holdcraft R, Chevalier B, Berg CA. 2001. Ras1 interacts with multiple new signaling and cytoskeletal loci in Drosophila eggshell patterning and morphogenesis. Genetics 159: 609-622.
56. Schock F, Perrimon N. 2003. Retraction of the Drosophila germ band requires cellmatrix interaction. Genes Dev 17: 597-602.
57. Scuderi A, Letsou A. 2005. Amnioserosa is required for dorsal closure in Drosophila. Dev Dyn 232:791-800.
58. Seong KH, Matsuo T, Fuyama Y, Aigaki T. 2001a. Neural-specific overexpression of drosophila plenty of SH3s (DPOSH) extends the longevity of adult flies. Biogerontology 2:271-281.
59. Seong KH, Ogashiwa T, Matsuo T, Fuyama Y, Aigaki T. 2001b. Application of the gene search system to screen for longevity genes in Drosophila. Biogerontology 2:209-217.
60. Silverman N, Zhou R, Erlich RL, Hunter M, Bernstein E, Schneider D, Maniatis T. 2003. Immune activation of NF-kappaB and JNK requires Drosophila TAK1. J Biol Chem 278:48928-48934.
61. Sluss HK, Han Z, Barrett T, Goberdhan DC, Wilson C, Davis RJ, Ip YT. 1996. A JNK signal transduction pathway that mediates morphogenesis and an immune response in Drosophila. Genes Dev 10:2745-2758.
62. Stronach B. 2005. Dissecting JNK signaling, one KKKinase at a time. Dev Dyn 232:575-584.
63. Stronach B, Perrimon N. 2002. Activation of the JNK pathway during dorsal closure in Drosophila requires the mixed lineage kinase, slipper. Genes Dev 16: 377-387.
64. Sykiotis GP, Bohmann D. 2008. Stressactivated protein kinase signaling in Drosophila. In: Posas F, Nebreda AR, editor. Stress activated protein kinases. Berlin: Springer. p 225-241.
65. Tapon N, Nagata K, Lamarche N, Hall A. 1998. A new rac target POSH is an SH3-containing scaffold protein involved in the JNK and NF-kappaB signalling pathways. EMBO J 17:1395-1404.
66. Tournier C, Hess P, Yang DD, Xu J, Turner TK, Nimnual A, Bar-Sagi D, Jones SN, Flavell RA, Davis RJ. 2000. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288:870-874.
67. Toyama Y, Peralta XG, Wells AR, Kiehart DP, Edwards GS. 2008. Apoptotic force and tissue dynamics during Drosophila embryogenesis. Science 321:1683-1686.
68. Tsuda M, Langmann C, Harden N, Aigaki T. 2005. The RING-finger scaffold protein plenty of SH3s targets TAK1 to control immunity signalling in Drosophila. EMBO Rep 6:1082-1087.
69. Tuvia S, Taglicht D, Erez O, Alroy I, Alchanati I, Bicoviski V, Dori-Bachash M, Ben-Avraham D, Reiss Y. 2007. The ubiquitin E3 ligase POSH regulates calcium homeostasis through spatial control of Herp. J Cell Biol 177:51-61.
70. Vidal S, Khush RS, Leulier F, Tzou P, Nakamura M, Lemaitre B. 2001. Mutations in the Drosophila dTAK1 gene reveal a conserved function for MAPKKKs in the control of rel/NF-kappaB-dependent innate immune responses. Genes Dev 15:1900-1912.
71. Wang SL, Hawkins CJ, Yoo SJ, Muller HA, Hay BA. 1999. The Drosophila caspase inhibitor DIAP1 is essential for cell survival and is negatively regulated by HID. Cell 98:453-463.
72. Wang X, Destrument A, Tournier C. 2007. Physiological roles of MKK4 and MKK7: insights from animal models. Biochim Biophys Acta 1773:1349-1357.
73. White K, Grether ME, Abrams JM, Young L, Farrell K, Steller H. 1994. Genetic control of programmed cell death in Drosophila. Science 264:677-683.
74. Whitmarsh AJ, Cavanagh J, Tournier C, Yasuda J, Davis RJ. 1998. A mammalian scaffold complex that selectively mediates MAP kinase activation. Science 281:1671-1674.
75. Wolff T. 2000. Histological Techniques for the Drosophila Eye. Part I: larva and pupa. In: Sullivan W, Ashburner M, Hawley RS, editor. Drosophila protocols. Cold Spring Harbor, NY: CSHL Press. p 728.
76. Woolner S, Jacinto A, Martin P. 2005. The small GTPase Rac plays multiple roles in epithelial sheet fusion-dynamic studies of Drosophila dorsal closure. Dev Biol 282:163-173.
77. Xu Z, Greene LA. 2006. Activation of the apoptotic JNK pathway through the Rac1-binding scaffold protein POSH. Methods Enzymol 406:479-489.
78. Xu Z, Kukekov NV, Greene LA. 2003. POSH acts as a scaffold for a multiprotein complex that mediates JNK activation in apoptosis. EMBO J 22:252-261.
79. Xu Z, Kukekov NV, Greene LA. 2005. Regulation of apoptotic c-Jun N-terminal kinase signaling by a stabilizationbased feed-forward loop. Mol Cell Biol 25:9949-9959.
80. Xu Z, Maroney AC, Dobrzanski P, Kukekov NV, Greene LA. 2001. The MLK family mediates c-Jun N-terminal kinase activation in neuronal apoptosis. Mol Cell Biol 21:4713-4724.
81. Yasuda J, Whitmarsh AJ, Cavanagh J, Sharma M, Davis RJ. 1999. The JIP group of mitogen-activated protein kinase scaffold proteins. Mol Cell Biol 19:7245-7254.
82. Yu X, Wang L, Acehan D, Wang X, Akey CW. 2006. Three-dimensional structure of a double apoptosome formed by the Drosophila Apaf-1 related killer. J Mol Biol 355:577-589.
83. Zhou L, Schnitzler A, Agapite J, Schwartz LM, Steller H, Nambu JR. 1997. Cooperative functions of the reaper and head involution defective genes in the programmed cell death of Drosophila central nervous system midline cells. Proc Natl Acad Sci U S A 94: 5131-5136.
84. Zhuang ZH, Zhou Y, Yu MC, Silverman N, Ge BX. 2006. Regulation of Drosophila p38 activation by specific MAP2 kinase and MAP3 kinase in response to different stimuli. Cell Signal 18:441-448.