Apoptosis controls the speed of looping morphogenesis in Drosophila male terminalia

Development

Volumn 138, Issue 8, 2011, Pages 1493-1499

  Kuranaga, Erina ^a,b,c   Matsunuma, Takayuki ^a   Kanuka, Hirotaka ^d   Takemoto, Kiwamu ^b,e   Koto, Akiko ^a   Kimura, Ken Ichi ^f   Miura, Masayuki ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c RIKEN Center for Biosystems Dynamics Research   (Japan)

^d OBIHIRO UNIVERSITY OF AGRICULTURE AND VETERINARY MEDICINE   (Japan)

^e YOKOHAMA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^f HOKKAIDO UNIVERSITY OF EDUCATION   (Japan)

Author keywords

Apoptosis; Caspase; Drosophila; In vivo imaging

Indexed keywords

CASPASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4;

ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL TRACKING; CONTROLLED STUDY; DEVELOPMENTAL STAGE; ENZYME ACTIVATION; MALE; MALE GENITAL SYSTEM; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; TIME LAPSE IMAGING;

ANIMALS; APOPTOSIS; CASPASES; DROSOPHILA; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENITALIA, MALE; MALE; MICROSCOPY, ELECTRON, SCANNING; MORPHOGENESIS;

METAZOA; TERMINALIA;

EID: 79955427907     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.058958     Document Type: Article

References (27)

1. 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.
2. Adachi-Yamada, T., Nakamura, M., Irie, K., Tomoyasu, Y., Sano, Y., Mori, E., Goto, S., Ueno, N., Nishida, Y. and Matsumoto, K. (1999). p38 mitogenactivated protein kinase can be involved in transforming growth factor beta superfamily signal transduction in Drosophila wing morphogenesis. Mol. Cell. Biol. 19, 2322-2329.
3. Adam, G., Perrimon, N. and Noselli, S. (2003). The retinoic-like juvenile hormone controls the looping of left-right asymmetric organs in Drosophila. Development 130, 2397-2406.
4. Benitez, S., Sosa, C., Tomasini, N. and Macias, A. (2010). Both JNK and apoptosis pathways regulate growth and terminalia rotation during Drosophila genital disc development. Int. J. Dev. Biol. 54, 643-653.
5. de Navas, L., Foronda, D., Suzanne, M. and Sanchez-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.
6. Degterev, A., Boyce, M. and Yuan, J. (2003). A decade of caspases. Oncogene 22, 8543-8567.
7. Duchek, P., Somogyi, K., Jekely, G., Beccari, S. and Rorth, P. (2001). Guidance of cell migration by the Drosophila PDGF/VEGF receptor. Cell 107, 17-26.
8. Estrada, B., Casares, F. and Sanchez-Herrero, E. (2003). Development of the genitalia in Drosophila melanogaster. Differentiation 71, 299-310.
9. Gleichauf, R. (1936). Anatomie und variabilitat des geschlechtapparates von Drosophila melanogaster. Z. Wiss. Zool. 148, 1-66.
10. Gorfinkiel, N., Sanchez, L. and Guerrero, I. (2003). Development of the Drosophila genital disc requires interactions between its segmental primordia. Development 130, 295-305.
11. Kanuka, H., Kuranaga, E., Takemoto, K., Hiratou, T., Okano, H. and Miura, M. (2005). Drosophila caspase transduces Shaggy/GSK-3beta kinase activity in neural precursor development. EMBO J. 24, 3793-3806.
12. Keisman, E. L., Christiansen, A. E. and Baker, B. S. (2001). The sex determination gene doublesex regulates the A/P organizer to direct sex-specific patterns of growth in the Drosophila genital imaginal disc. Dev. Cell 1, 215-225.
13. Koto, A., Kuranaga, E. and Miura, M. (2009). Temporal regulation of Drosophila IAP1 determines caspase functions in sensory organ development. J. Cell Biol. 187, 219-231.
14. 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.
15. Kuranaga, E., Kanuka, H., Tonoki, A., Takemoto, K., Tomioka, T., Kobayashi, M., Hayashi, S. and Miura, M. (2006). Drosophila IKK-related kinase regulates nonapoptotic function of caspases via degradation of IAPs. Cell 126, 583-596.
16. Macias, A., Romero, N. M., Martin, F., 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.
17. 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.
18. 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.
19. Pandey, R., Heidmann, S. and Lehner, C. F. (2005). Epithelial re-organization and dynamics of progression through mitosis in Drosophila separase complex mutants. J. Cell Sci. 118, 733-742.
20. Rosenblatt, J., Raff, M. C. and Cramer, L. P. (2001). An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin-and myosindependent mechanism. Curr. Biol. 11, 1847-1857.
21. Rousset, R., Bono-Lauriol, S., Gettings, M., Suzanne, M., Speder, P. and Noselli, S. (2010). The Drosophila serine protease homologue Scarface regulates JNK signalling in a negative-feedback loop during epithelial morphogenesis. Development 137, 2177-2186.
22. Stenn, K. S. and Paus, R. (2001). Controls of hair follicle cycling. Physiol. Rev. 81, 449-494.
23. Suzanne, M., Petzoldt, A. G., Speder, P., Coutelis, J. B., Steller, H. and Noselli, S. (2010). Coupling of apoptosis and L/R patterning controls stepwise organ looping. Curr. Biol. 20, 1773-1778.
24. Takemoto, K., Nagai, T., Miyawaki, A. and Miura, M. (2003). Spatio-temporal activation of caspase revealed by indicator that is insensitive to environmental effects. J. Cell Biol. 160, 235-243.
25. Takemoto, K., Kuranaga, E., Tonoki, A., Nagai, T., Miyawaki, A. and Miura, M. (2007). Local initiation of caspase activation in Drosophila salivary gland programmed cell death in vivo. Proc. Natl. Acad. Sci. USA 104, 13367-13372.
26. Toyama, Y., Peralta, X. G., Wells, A. R., Kiehart, D. P. and Edwards, G. S. (2008). Apoptotic force and tissue dynamics during Drosophila embryogenesis. Science 321, 1683-1686.
27. Zhou, L., Schnitzler, A., Agapite, J., Schwartz, L. M., Steller, H. and Nambu, J. R. (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. USA 94, 5131-5136.