Both JNK and apoptosis pathways regulate growth and terminalia rotation during Drosophila genital disc development

International Journal of Developmental Biology

Volumn 54, Issue 4, 2010, Pages 643-653

  Benitez, Sergio ^a   Sosa, Claudia ^a   Tomasini, Nicolás ^a   Macías, Ana ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

Apoptosis; Drosophila; Genital disc; Jnk; Reaper

Indexed keywords

CASPASE; DROSOPHILA PROTEIN; ENGRAILED PROTEIN; HEAD INVOLUTION DEFECTIVE PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN 1; REAPER PROTEIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; GENE CONTROL; GROWTH REGULATION; IMAGINAL DISC; INSECT CELL; INSECT DEVELOPMENT; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; APOPTOSIS; CASPASES; CELL DEATH; CELL PROLIFERATION; DROSOPHILA; FEMALE; GENITALIA, FEMALE; GENITALIA, MALE; GROWTH; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE;

TERMINALIA;

EID: 77950545476     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.082724sb     Document Type: Article

References (51)

1. ABRAMS, J.M. (1999). An emerging blueprint for apoptosis in Drosophila. Trends Cell Biol. 9: 435-440.
2. ABBOTT, M.K. and LENGYEL, J.A. (1991). Embryonic head involution and rotation of male terminalia require the Drosophila locus head involution defective. Genetics 129: 783-789.
3. ADACHI-YAMADA, T., FUJIMURA-KAMADA, K., NISHIDA, Y. and MATSUMOTO, K. (1999). Distortion of proximo-distal information causes JNK-dependent apoptosis in Drosophila wing. Nature 400: 166-169.
4. AHMAD, S.M. and BAKER, B.S. (2002). Sex-Specific Deployment of FGF Signaling innDrosophila recruits mesodermal cells into the male genital imaginal disc. Cell 109: 651-661.
5. BRAND, A.H. and PERRIMON, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
6. BERGMANN, A., AGAPITE, J., MCCALL, K. and STELLER, H. (1998). The Drosophila Gene hid is a direct molecular target of Ras-dependent survival signaling. Cell 95: 331-341.
7. CALLEJA, M., MORENO, E., PELAZ, S. and MORATA, G. (1996). Visualization of gene expression in living adult Drosophila. Science 274: 252-255.
8. CASARES, F., SÁNCHEZ L., GUERRERO, I. and SÁNCHEZ-HERRERO, E. (1997) The genital disc of Drosophila melanogaster. I. Segmental and compartmental organization. Dev Genes Evol 207: 216-228.
9. CHAN, H.Y. and YANG, X. (2000). Proteases for Cell Suicide: Functions and Regulation of Caspases. Microbiol. Mol. Biol. Rev. 64:821-846.
10. CHEN, E.H., CHRISTIANSEN, A.E. and BAKER, B.S. (2005). Allocation and specification of the genital disc precursor cells in Drosophila. Dev. Biol. 281: 270-285.
11. CHEN, P., NORDSTROM, W., GISH, B. and ABRAMS, J.M. (1996). grim, a novel cell death gene in Drosophila. Genes Dev. 10: 1773-1782.
12. de la COVA, C., ABRIL, M., BELLOSTA, P., GALLANT, P. and JOHNSTON, L.A. (2004). Drosophila myc regulates organ size by inducing cell competition. Cell 117: 107-116.
13. de NAVAS, L., FORONDA, D., SUZANNE, M. and SÁNCHEZ-HERRERO, E. (2006). A Simple and efficient method to identify replacements of P-lacZ by P- Gal4 lines allows obtaining Gal4 insertions in the Bithorax complex of Drosophila. Mech. Dev. 123: 860-867.
14. ESTRADA, B., CASARES, F. and SANCHEZ-HERRERO, E. (2003). Development of the genitalia in Drosophila melanogaster. Differentiation 71: 299-310.
15. GLEICHAUF, R. (1936). Anatomie und Variabilitat des Geschlechtapparates von Drosophila melanogaster (Meigen). Z. Wiss. Zool 148: 1-66
16. GRETHER, M.E., ABRAMS, J.M., AGAPITE, J., WHITE, K. and STELLER, H. (1995). The head involution defective gene of Drosophila melanogaster func- tions in programmed cell death. Genes Dev. 9: 1694-1708.
17. HAY, B.A., WOLFF, T. and RUBIN, G.M. (1994). Expression of baculovirus P35 prevents cell death in Drosophila. Development 120: 2121-2129.
18. HAY, B.A. (2000). Understanding IAP function and regulation: a view from Drosophila. Cell Death Differ 7: 1045-1056.
19. HUH, J.R., GUO, M. and HAY, B.A. (2004). Compensatory proliferation induce by cell death in the Drosophila wing disc requires activity of the apical cell death caspase Dronc in a non-apoptotic role. Curr. Biol. 14: 1262-1266.
20. ITO, K., AWANO, W., SUZUKI, K., HIROMI, Y. and YAMAMOTO, D. (1997). The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurons and glial cells. Development 124: 761-771.
21. JIANG, C., BAEHRECKE, E.H. and THUMMEL, C.S. (1997). Steroid regulated programmed cell death during Drosophila metamorphosis. Development 124: 4673-4683.
22. KEISMAN, E.L., CHRISTIANSEN, A.E. and BAKER, B.S. (2001). The sex determi- nation gene doublesex regulates the A/P organizer to direct sex-specific patterns of growth in the Drosophila genital Imaginal Disc. Cell 1: 215-22.
23. KRIESER, R.J., MOORE, F.E., DRESNEK, D., PELLOCK, B.J., PATEL, R., HUANG, A., BRACHMANN, C. and WHITE, K. (2007). The Drosophila homolog of the putative phosphatidylserine receptor functions to inhibit apoptosis. Development 134: 2407-2414.
24. KURADA, P. and WHITE K. (1998). Ras promotes cell survival in Drosophila by downregulating hid expression. Cell 95: 319-329.
25. KURANAGA, E., KANUKA, H., IGAKI, T., SAWAMOTO, K., ICHIJO, H., OKANO, H. and MIURA, M. (2002). Reaper-mediated inhibition of DIAP1-induced DTRAF1 degradation results in activation of JNK in Drosophila. Nat. Cell Biol. 4: 705-710
26. MACIAS, A., ROMERO, N.M., MARTIN, F.A., SUAREZ, L., ROSA, A.L. and MORATA, G. (2004). PVF1/PVR signaling and apoptosis promotes the rotation and dorsal closure of the Drosophila male terminalia. Int. J. Dev. Biol. 48: 1087- 1094.
27. MARTÍN, F.A., PERÉZ-GARIJO, A. and MORATA, G. (2009). Apoptosis in Droso- phila: compensatory proliferation and undead cells. Int. J. Dev. Biol. 53: 1341- 1347
28. MARTIN-BLANCO, E., GAMPEL, A., RING, J., VIRDEE, K., KIROV, N., TOLKOVSKY, A.M. and 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.
29. McCARTHY, J.V. (2003). Apoptosis and development. Essays Biochem. 39: 11-24.
30. McEWEN, D.G. and PEIFER, M. (2005). Puckered, a Drosophila MAPK phos- phatase, ensures cell viability by antagonizing JNK-induced apoptosis. Development 132: 3935-3946.
31. McGUIRE, S.E., LE, P.T., OSBORN, A.J., MATSUMOTO, K. and DAVIS, R.L. (2003). Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302: 1765-1768.
32. MORATA, G. and RIPOLL, P. (1975). Minutes: mutants of Drosophila autono- mously affecting cell division rate. Dev. Biol. 42: 211-221.
33. MORENO, E; BASLER, K. and MORATA G. (2002a). Cells compete for Decapen- taplegic survival factor to prevent apoptosis in Drosophila. Nature 416:755-759.
34. MORENO, E., YAN, M. and BASLER, K. (2002b). Evolution of TNF signaling mechanisms: JNK-dependent apoptosis triggered by Eiger, the Drosophila homolog of the TNF superfamily. Curr. Biol. 12: 1263-1268.
35. MORENO, E. and BASLER, K. (2004). dMyc transforms cells into super-competitors. Cell 117: 117-129.
36. 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 non-apoptotic process. Development 133: 3305-3315.
37. NORDSTROM, W., CHEN, P., STELLER, H. and ABRAMS, J.M. (1996). Activation of reaper Gene during Ectopic Cell Killing in Drosophila. Dev. Biol. 180: 213- 226.
38. PASTORP-AREJA, J.C., GRAWE, F., MARTIN-BLANCO, E. and GARCIABELLIDO, A. (2004). Invasive cell behaviour during Drosophila imaginal disc eversion is mediated by the JNK signaling cascade. Dev. Cell 7: 387-399.
39. PEREZ-GARIJO, A., MARTIN, F.A. and MORATA, G. (2004). Caspase inhibition during apoptosis causes abnormal signaling and developmental aberrations in Drosophila. Development 131: 5591-5598.
40. PEREZ-GARIJO, A., MARTIN, F. A., STRUHL, G. and MORATA, G (2005). Dpp signaling and the induction of neoplastic tumours by caspase-inhibited apop- totic cells in Drosophila. Proc. Natl. Acad. Sci. USA 1002: 17664-17669.
41. POLASKI, S., WHITNEY, L., BARKER, B.W. and STRONACH, B. (2006). Genetic Analysis of Slipper/Mixed Lineage Kinase Reveals Requirements in Multiple Jun-N-Terminal Kinase-Dependent Morphogenetic Events During Drosophila Development. Genetics174: 719-733.
42. 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.
43. RYOO, H.D., GORENC, T. and STELLER, H. (2004). Apoptotic cells can induce compensatory cell proliferation through the JNK and the Wingless signaling pathways. Dev. Cell 7: 491-501.
44. SANCHEZ, L. and GUERRERO, I. (2001). The development of the Drosophila genital disc. Bioessays 23: 698-707.
45. SPEDER, P. ADAM, G. and NOSELLI, S. (2006). Type ID unconventional myosin controls left-right asymmetry in Drosophila. Nature 440: 803-807.
46. SU, T.T., SPRENGER, F., DiGREGORIO, P.J., SHELAGH, D CAMPBELL S.D.and O'FARELL P.H. (1998). Exit from mitosis in Drosophila syncytial embryos requires proteolysis and cyclin degradation, and is associated with localized dephosphorylation. Genes Dev. 12: 1495-1503.
47. TABATA, T., SCHWARTZ, C., GUSTAVSON, E., ALI, Z. and KORNBERG, T.B. (1995). Creating a Drosophila wing de novo, the role of engrailed and the compartment border hypothesis. Development 121: 3359-3369.
48. TSUJIMURA, H., YONEDA, T., AONUMA, H., ARAI, H. and HIRAI, S. (2008). Reaperand Grim-induced cell death is suppressed by Ras/MAPK signaling in Drosophila developing indirect flight muscles. A. Dros. Res. Conf. 49: 764B.
49. WHITE, K.; TAHAOGLU, E. and STELLER, H. (1998). Cell Killing by the Drosophila Gene reaper. Science 271: 805-807.
50. XIA, Y. and KARIN, M. (2004). The control of cell motility and epithelial morphogen- esis by Jun kinases. Trends Cell Biol. 14: 94-101.
51. YOO, J.S., HUH, J.R., MURO, I., YU, H., WANG, L., WANG, S.L., FELDMAN, R.M.R., CLEM, R.J., MÜLLER, H.A.J. and HAY, B.A. (2002). Hid, Rpr and Grim negatively regulate DIAP1 levels through distinct mechanisms. Nat. Cell Biol. 4:416-424.