The role of Dpp and Wg in compensatory proliferation and in the formation of hyperplastic overgrowths caused by apoptotic cells in the Drosophila wing disc

Development

Volumn 136, Issue 7, 2009, Pages 1169-1177

  Pérez Garijo, Ainhoa ^a   Shlevkov, Evgeny ^a   Morata, Ginés ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Apoptosis; Compensatory proliferation; dpp; Hyperplastic overgrowths; JNK; wg

Indexed keywords

CASPASE INHIBITOR; DECAPENTAPLEGIC PROTEIN; PROTEIN P35; WNT1 PROTEIN; DPP PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; STRESS ACTIVATED PROTEIN KINASE; WG PROTEIN, DROSOPHILA;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COMPARTMENTALIZATION; CELL LOSS; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DROSOPHILA; FORELIMB; HYPERPLASTIC OVERGROWTH; LIMB DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; X IRRADIATION; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; GENE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOMEOSTASIS; HYPERPLASIA; METABOLISM; MUTATION; RADIATION EXPOSURE; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; CELL PROLIFERATION; DROSOPHILA; DROSOPHILA PROTEINS; GENES, INSECT; HOMEOSTASIS; HYPERPLASIA; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, BIOLOGICAL; MUTATION; SIGNAL TRANSDUCTION; WING; WNT1 PROTEIN;

EID: 67449113922     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.034017     Document Type: Article

References (53)

1. Adachi-Yamada, T., Fujimura-Kamada, K., Nishida, Y. and Matsumoto, K. (1999). Distorsion of proximodistal information causes JNK-dependent apoptosis in Drosophila wing. Nature 400, 166-169.
2. Aldaz, S., Morata, G. and Azpiazu, N. (2003). The Pax-homeobox gene eyegone is involved in the subdivision of the thorax of Drosophila. Development 130, 4473-4482.
3. Brodsky, M. H., Nordstrom, W., Tsang, G., Kwan, E., Rubin, G. M. and Abrams. J. M. (2000). Drosophila p53 binds a damage response element at the reaper locus. Cell 101, 103-113.
4. Burke, R. and Basler, K. (1996). Dpp receptors are autonomously required for cell proliferation in the entire developing Drosophila wing. Development 122, 2261-2269.
5. Chew, S. K., Akdemir, F., Chen, P., Lu, W. J., Mills, K., Daish, T., Kumar, S., Rodriguez, A. and Abrams, J. M. (2004). The apical caspase dronc governs programmed and unprogrammed cell death in Drosophila. Dev. Cell 7, 897-907.
6. Daish, T. J., Mills, K. and Kumar, S. (2004). Drosophila caspase DRONC is required for specific developmental cell death pathways and stress-induced apoptosis. Dev. Cell 7, 909-915.
7. de la Cova, C., Abril, M., Bellosta, P., Gallant, P. and Johnston, L. (2004). Drosophila myc regulates organ size by inducing cell competition. Cell 117, 107-116.
8. Foronda, D., Perez-Garijo, A. and Martin, F. A. (2009). Dpp of posterior origin patterns the proximal region of the wing. Mech. Dev. (in press).
9. Garcia-Bellido, A. and Merriam, J. (1971). Parameters of the wing imaginal disc development of Drosophila melanogaster. Dev. Biol. 24 61-87.
10. Giraldez, A. J. and Cohen, S. M. (2003). Wingless and Notch signaling provide cell survival cues and control cell proliferation during wing development. Development 130, 6533-6543.
11. Glise, B. and Noselli, S. (1997). Coupling of Jun amino-terminal kinase and Decapentaplegic signaling pathways in Drosophila morphogenesis. Genes Dev. 11, 1738-1747.
12. Glise, B., Bourbon, H. and Noselli, S. (1995). hemipterous encodes a novel Drosophila MAP kinase kinase, required for epithelial cell sheet movement. Cell 83, 451-461.
13. Goto, S. and Hayashi, S. (1997). Specification of the embryonic limb primordium by graded activity of Decapentaplegic. Development 124, 125-132.
14. Goyal, L., McCall, K., Agapite, J., Hartwieg, E. and Steller, H. (2000). Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. EMBO J. 19, 589-597.
15. Haley, B., Hendrix, D., Trang, V. and Levine. M. (2008). A simplified miRNA-based gene silencing method for Drosophila melanogaster. Dev. Biol. 15, 482-490.
16. Hariharan, I. K. and Bilder, D. (2006). Regulation of imaginal disc growth by tumor-suppressor genes in Drosophila. Annu. Rev. Genet. 40, 335-361.
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. Haynie, J. L. and Bryant, P. J. (1977). The effects of X-rays on the proliferation dynamics of Cells in the imagina wing disc of Drosophila melanogaster. Roux's Arch. 183, 85-100.
19. Heasley, L. E. and Han, S. Y. (2006). JNK regulation of oncogenesis. Mol. Cells 21, 167-173.
20. Hou, X. S., Goldstein, E. S. and Perrimon, N. (1997). Drosophila Jun relays the Jun amino-terminal kinase signal transduction pathway to the Decapentaplegic signal transduction pathway in regulating epithelial cell sheet movement. Genes Dev. 11, 1728-1737.
21. Huh, J. R., Guo, M. and Hay, B. A. (2004). Compensatory proliferation induced by cell death in the Drosophila wing disc requires activity of the apical cell death caspase Dronc in a nonapoptotic role. Curr. Biol. 14, 1262-1266.
22. Johnston, L. A. and Sanders, A. L. (2003). Wingless promotes cell survival but constrains growth during Drosophila wing development. Nat. Cell Biol. 5, 827-833.
23. Johnston, L. A., Prober, D. A., Edgar, B. A., Eisenmann, R. N. and Gallant, P. (1999). Drosophila myc regulates growth during development. Cell 98 779-790.
24. Katoh, M. (2007). Networking of WNT, FGF, Notch, BMP, and Hedgehog signaling pathways during carcinogenesis. Stem Cell Rev. 3, 30-38.
25. Kennedy, N. J. and Davis, R. J. (2003). Role of JNK in tumor development. Cell Cycle 2, 199-201.
26. Kondo, S., Senoo-Matsuda, N., Hiromi, Y. and Miura, M. (2006). DRONC coordinates cell death and compensatory proliferation. Mol. Cell. Biol. 19, 7258-726
27. Lawrence, P. A. and Struhl, G. (1996). Morphogens, compartments and pattern: lessons from Drosophila. Cell 85, 951-961.
28. Lohmann, I., McGinnis, N., Bodmer, M. and McGinnis, W. (2002). The Drosophila Hox gene deformed sculpts head morphology via direct regulation of the apoptosis activator reaper. Cell 110, 457-466.
29. Luo, X., Puig, O., Hyun, J., Bohmann, D. and Jasper, H. (2007). Foxo and Fos regulate the decision between cell death and survival in response to UV irradiation. EMBO J. 26, 380-390.
30. Manjon, C., Sanchez-Herrero, E. and Suzanne, M. (2007). Sharp boundaries of Dpp signalling trigger local cell death required for Drosophila leg morphogenesis. Nat. Cell Biol. 9, 57-63.
31. Martin, F. A. and Morata, G. (2006). Compartments and the control of growth in the Drosophila wing imaginal disc. Development 133, 4421-4426.
32. Martín, F. A., Pérez-Garijo, A., Moreno, E. and Morata, G. (2004). The brinker gradient controls wing growth in Drosophila. Development 131, 4921-4930.
33. Martin, F. A., Pérez-Garijo, A. and Morata, G. (2009). Apoptosis in Drosophila: compensatory proliferation and undead cells. Int. J. Dev. Biol. (in press).
34. Martín-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.
35. Martin-Blanco, E., Pastor-Pareja, J. C. and Garcia-Bellido, A. (2000). JNK and decapentaplegic signaling control adhesiveness and cytoskeleton dynamics during thorax closure in Drosophila. Proc. Natl. Acad. Sci. USA 97, 7888-7893.
36. Martín-Castellanos, C. and Edgar, B. A. (2002). A characterization of the effects of Dpp signaling on cell growth and proliferation in the Drosophila wing. Development 129, 1003-1013.
37. McEwen, D. G. and Peifer, M. (2005). Puckered, a Drosophila MAPK phosphatase, ensures cell viability by antagonizing JNK-induced apoptosis. Development 132, 3935-3946.
38. Milan, M., Campuzano, S. and Garcia-Bellido, A. (1997). Developmental parameters of cell death in the wing disc of Drosophila. Proc. Natl. Acad. Sci. USA 94, 5691-5696.
39. Morata, G. and Ripoll, P. (1975). Minutes: mutants of Drosophila autonomously affecting cell division rate. Dev. Biol. 42, 211-221.
40. Moreno, E. and Basler, K. (2004). dMyc transforms cells into super-competitors. Cell 117, 117-129.
41. Neufeld, T. P., de la Cruz, A. F., Johnston, L. A. and Edgar, B. A. (1998). Coordination of growth and cell division in the Drosophila wing. Cell 93, 1183-1193.
42. Ollmann, M., Young, L. M., Di Como, C. J., Karim, F., Belvin, M., Robertson, S., Whittaker, K., Demsky, M., Fisher, W. W., Buchman, A. et al. (2000). Drosophila p53 is a structural and functional homolog of the tumor suppressor p53. Cell 101, 91-101.
43. Perez-Garijo, A., Martin, F. A. and Morata, G. (2004). Caspase inhibition during apoptosis causes abnormal signalling and developmental aberrations in Drosophila. Development 131, 5591-5598.
44. Perez-Garijo, A., Martin, F. A., Struhl, G. and Morata, G. (2005). Dpp signaling and the induction of neoplastic tumors by caspase-inhibited apoptotic cells in Drosophila. Proc. Natl. Acad. Sci. USA 102, 17664-17669.
45. Polakis, P. (2007). The many ways of Wnt in cancer. Curr. Opin. Genet. Dev. 17, 45-51.
46. Riesgo-Escovar, J. R. and 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.
47. 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.
48. 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.
49. St Johnston, R., Hoffmann, F., Blackman, R., Segal, D., Grimaila, R., Padgett, R., Irick, H. and Gelbart, W. (1990). Molecular organization of the decapentaplegic gene in Drosophila melanogaster. Genes Dev. 4, 1114-1127.
50. Wang, S. L., Hawkins, C. J., Yoo, S. J., Muller, H. A. and Hay, B. A. (1999). The Drosophila caspase inhibitor DIAP1 is essential for cell survival and is negatively regulated by HID. Cell 98, 453-463.
51. Wells, B. S., Yoshida, E. and Johnston, L. (2006). Compensatory proliferation in Drosophila imaginal discs requires requires Dronc-dependent p53 activity. Curr. Biol. 16, 1606-1615.
52. Xu, D., Li, Y., Arcaro, M., Lackey, M. and Bergmann, A. (2005). The CARD-carrying caspase Dronc is essential for most, but not all, developmental cell death in Drosophila. Development 132, 2125-2134.
53. Yoo, S. J., Huh, J. R., Muro, I., Yu, H., Wang, L., Wang, S. L., Feldman, R. M., Clem, R. J., Muller, H. A. and Hay, B. A. (2002). Hid, Rpr and Grim negatively regulate DIAP1 levels through distinct mechanisms. Nat. Cell Biol. 4, 416-424.