Cell death-induced regeneration in wing imaginal discs requires JNK signalling

Development

Volumn 137, Issue 7, 2010, Pages 1169-1179

  Bergantiños, Cora ^a   Corominas, Montserrat ^a   Serras, Florenci ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Apoptosis; Drosophila; Growth; Regeneration; Wing disc

Indexed keywords

PROTEIN PATCHED; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR GAL4; DROSOPHILA PROTEIN; REAPER PROTEIN, DROSOPHILA;

APOPTOSIS; ARTICLE; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; CYTOSKELETON; DROSOPHILA; ENZYME ACTIVITY; FORELIMB; MICROSURGERY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TISSUE REGENERATION; ANIMAL; ANIMAL EMBRYO; CELL LINEAGE; DROSOPHILA MELANOGASTER; GENETICS; HISTOLOGY; METABOLISM; MITOSIS; PHYSIOLOGY; PRENATAL DEVELOPMENT; REGENERATION; ULTRASTRUCTURE;

ANIMALS; CELL DEATH; CELL LINEAGE; CELL PROLIFERATION; CYTOSKELETON; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MITOSIS; REGENERATION; SIGNAL TRANSDUCTION; WING;

EID: 77950492682     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.045559     Document Type: Article

References (85)

1. Abbott, L. C., Karpen, G. H. and Schubiger, G. (1981). Compartmental restrictions and blastema formation during pattern regulation in Drosophila imaginal leg discs. Dev. Biol. 87, 64-75.
2. Adler, P. N. (1981). Growth during pattern regulation in imaginal discs. Dev. Biol. 87, 356-373.
3. Aegerter-Wilmsen, T., Aegerter, C. M., Hafen, E. and Basler, K. (2007). Model for the regulation of size in the wing imaginal disc of Drosophila. Mech. Dev. 124, 318-326. (Pubitemid 46400393)
4. Agata, K., Saito, Y. and Nakajima, E. (2007). Unifying principles of regeneration I: Epimorphosis versus morphallaxis. Dev. Growth Differ. 49, 73-78. (Pubitemid 46310578)
5. Agnes, F., Suzanne, M. and Noselli, S. (1999). The Drosophila JNK pathway controls the morphogenesis of imaginal discs during metamorphosis. Development 126, 5453-5462. (Pubitemid 30015937)
6. Ashburner, M., Golic, K. and Hawley, R. (2005). Drosophila: A Laboratory Handbook. New York: Cold Spring Harbor Laboratory Press.
7. Barrio, R. and de Celis, J. F. (2004). Regulation of spalt expression in the Drosophila wing blade in response to the Decapentaplegic signaling pathway. Proc. Natl. Acad. Sci. USA 101, 6021-6026. (Pubitemid 38520521)
8. Basler, K. and Struhl, G. (1994). Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368, 208-214. (Pubitemid 24108836)
9. Bodenstein, D. (1943). Hormones and tissue competence in the development of Drosophila. Biol. Bull. 84, 34-58.
10. Bosch, M., Serras, F., Martin-Blanco, E. and Baguna, J. (2005). JNK signaling pathway required for wound healing in regenerating Drosophila wing imaginal discs. Dev. Biol. 280, 73-86. (Pubitemid 40342743)
11. Bosch, M., Baguna, J. and Serras, F. (2008). Origin and proliferation of blastema cells during regeneration of Drosophila wing imaginal discs. Int. J. Dev. Biol. 52, 1043-1050.
12. 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.
13. Brockes, J. P. and Kumar, A. (2008). Comparative aspects of animal regeneration. Annu. Rev. Cell Dev. Biol. 24, 525-549.
14. Brook, W. J., Ostafichuk, L. M., Piorecky, J., Wilkinson, M. D., Hodgetts, D. J. and Russell, M. A. (1993). Gene expression during imaginal disc regeneration detected using enhancer-sensitive P-elements. Development 117, 1287-1297. (Pubitemid 23154494)
15. Bryant, P. J. (1971). Regeneration and duplication following operations in situ on the imaginal discs of Drosophila melanogaster. Dev. Biol. 26, 637-651.
16. Bryant, P. J. and Fraser, S. E. (1988). Wound healing, cell communication, and DNA synthesis during imaginal disc regeneration in Drosophila. Dev. Biol. 127, 197-208.
17. Capdevila, J., Estrada, M. P., Sanchez-Herrero, E. and Guerrero, I. (1994). The Drosophila segment polarity gene patched interacts with decapentaplegic in wing development. EMBO J. 13, 71-82. (Pubitemid 24017176)
18. Chera, S., Ghila, L., Dobretz, K., Wenger, Y., Bauer, C., Buzgariu, W., Martinou, J. C. and Galliot, B. (2009). Apoptotic cells provide an unexpected source of Wnt3 signaling to drive hydra head regeneration. Dev. Cell 17, 279-289.
19. 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. (Pubitemid 38469902)
20. Dunne, J. F. (1981). Growth dynamics in the regeneration of a fragment of the wing imaginal disc of Drosophila melanogaster. Dev. Biol. 87, 379-382.
21. Fain, M. J. and Alvarez, C. (1987). The cell cycle and its relation to growth during pattern regulation in wing discs of Drosophila. J. Insect Physiol. 33, 697-705.
22. Fan, Y. and Bergmann, A. (2008). Distinct mechanisms of apoptosis-induced compensatory proliferation in proliferating and differentiating tissues in the Drosophila eye. Dev. Cell 14, 399-410.
23. Galliot, B., Tanaka, E. and Simon, A. (2008). Regeneration and tissue repair: themes and variations. Cell Mol. Life Sci. 65, 3-7.
24. Garcia-Bellido, A. and Merriam, J. R. (1971). Parameters of the wing imaginal disc development of Drosophila melanogaster. Dev. Biol. 24, 61-87.
25. Garcia-Bellido, A., Cortes, F. and Milan, M. (1994). Cell interactions in the control of size in Drosophila wings. Proc. Natl. Acad. Sci. USA 91, 10222-10226. (Pubitemid 24311981)
26. 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.
27. Hadorn, E. (1963). Differenzierungsleistungen wiederholt fragmentierter Teilstücke männlicher Genitalscheiben von Drosophila melanogaster nach Kultur in vivo. Dev. Biol. 7, 617-629.
28. Hadorn, E., Hürlimann, R., Mindek, G., Schubiger, G. and Staub, M. (1968). Developmental capacity of embryonal blastema in Drosophila following cultivation in an adult host. Rev. Suisse Zool. 75, 557-569.
29. Handberg-Thorsager, M., Fernandez, E. and Salo, E. (2008). Stem cells and regeneration in planarians. Front. Biosci. 13, 6374-6394.
30. Hay, B. A., Wolff, T. and Rubin, G. M. (1994). Expression of baculovirus P35 prevents cell death in Drosophila. Development 120, 2121-2129. (Pubitemid 24232280)
31. Haynie, J. and Bryant, P. J. (1977). The effects of X-rays on the proliferation dynamics of cells in the imaginal wing disc of Drosophila melanogaster Roux's Arch. Dev. Biol. 183, 85-100. (Pubitemid 8205618)
32. Herranz, H., Perez, L., Martin, F. A. and Milan, M. (2008). A Wingless and Notch double-repression mechanism regulates G1-S transition in the Drosophila wing. EMBO J. 27, 1633-1645. (Pubitemid 351794030)
33. Hinz, U., Giebel, B. and Campos-Ortega, J. A. (1994). The basic-helix-loop-helix domain of Drosophila lethal of scute protein is sufficient for proneural function and activates neurogenic genes. Cell 76, 77-87. (Pubitemid 24035283)
34. Hufnagel, L., Teleman, A. A., Rouault, H., Cohen, S. M. and Shraiman, B. I. (2007). On the mechanism of wing size determination in fly development. Proc. Natl. Acad. Sci. USA 104, 3835-3840. (Pubitemid 47181540)
35. 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. (Pubitemid 38991813)
36. Jacinto, A., Wood, W., Woolner, S., Hiley, C., Turner, L., Wilson, C., Martinez-Arias, A. and Martin, P. (2002a). Dynamic analysis of actin cable function during Drosophila dorsal closure. Curr. Biol. 12, 1245-1250. (Pubitemid 34801174)
37. Jacinto, A., Woolner, S. and Martin, P. (2002b). Dynamic analysis of dorsal closure in Drosophila: from genetics to cell biology. Dev. Cell 3, 9-19. (Pubitemid 34778392)
38. James, A. A. and Bryant, P. J. (1981). A quantitative study of cell death and mitotic inhibition in gamma-irradiated imaginal wing discs of Drosophila melanogaster. Radiat. Res. 87, 552-564.
39. Jasper, H., Benes, V., Schwager, C., Sauer, S., Clauder-Munster, S., Ansorge, W. and Bohmann, D. (2001). The genomic response of the Drosophila embryo to JNK signaling. Dev. Cell 1, 579-586. (Pubitemid 33586108)
40. Karpen, G. H. and Schubiger, G. (1981). Extensive regulatory capabilities of a Drosophila imaginal disk blastema. Nature 294, 744-747.
41. Kondo, S., Senoo-Matsuda, N., Hiromi, Y. and Miura, M. (2006). DRONC coordinates cell death and compensatory proliferation. Mol. Cell. Biol. 26, 7258-7268. (Pubitemid 44477701)
42. Kragl, M., Knapp, D., Nacu, E., Khattak, S., Maden, M., Epperlein, H. H. and Tanaka, E. M. (2009). Cells keep a memory of their tissue origin during axolotl limb regeneration. Nature 460, 60-65.
43. Lee, N., Maurange, C., Ringrose, L. and Paro, R. (2005). Suppression of Polycomb group proteins by JNK signalling induces transdetermination in Drosophila imaginal discs. Nature 438, 234-237. (Pubitemid 41599876)
44. Lepilina, A., Coon, A. N., Kikuchi, K., Holdway, J. E., Roberts, R. W., Burns, C. G. and Poss, K. D. (2006). A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 127, 607-619. (Pubitemid 44647426)
45. Li, W. and Baker, N. E. (2007). Engulfment is required for cell competition. Cell 129, 1215-1225.
46. Ma, C., Zhou, Y., Beachy, P. A. and Moses, K. (1993). The segment polarity gene hedgehog is required for progression of the morphogenetic furrow in the developing Drosophila eye. Cell 75, 927-938. (Pubitemid 24014549)
47. Martin, P. and Wood, W. (2002). Epithelial fusions in the embryo. Curr. Opin. Cell Biol. 14, 569-574.
48. Martin, P. and Parkhurst, S. M. (2004). Parallels between tissue repair and embryo morphogenesis. Development 131, 3021-3034. (Pubitemid 39077428)
49. 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. (Pubitemid 28101018)
50. Mattila, J., Omelyanchuk, L., Kyttala, S., Turunen, H. and Nokkala, S. (2005). Role of Jun N-terminal Kinase (JNK) signaling in the wound healing and regeneration of a Drosophila melanogaster wing imaginal disc. Int. J. Dev. Biol. 49, 391-399. (Pubitemid 41076267)
51. 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. (Pubitemid 37505740)
52. Milan, M., Campuzano, S. and Garcia-Bellido, A. (1996). Cell cycling and patterned cell proliferation in the wing primordium of Drosophila. Proc. Natl. Acad. Sci. USA 93, 640-645. (Pubitemid 26041141)
53. Millard, T. H. and Martin, P. (2008). Dynamic analysis of filopodial interactions during the zippering phase of Drosophila dorsal closure. Development 135, 621-626.
54. Moreno, E. and Basler, K. (2004). dMyc transforms cells into super-competitors. Cell 117, 117-129.
55. Moreno, E., Basler, K. and Morata, G. (2002). Cells compete for decapentaplegic survival factor to prevent apoptosis in Drosophila wing development. Nature 416, 755-759. (Pubitemid 34429153)
56. Morgan, T. H. (1901). Regeneration and Liability to Injury. Science 14, 235-248.
57. Motzny, C. K. and Holmgren, R. (1995). The Drosophila cubitus interruptus protein and its role in the wingless and hedgehog signal transduction pathways. Mech. Dev. 52, 137-150.
58. Ninov, N., Chiarelli, D. A. and Martin-Blanco, E. (2007). Extrinsic and intrinsic mechanisms directing epithelial cell sheet replacement during Drosophila metamorphosis. Development 134, 367-379. (Pubitemid 46252423)
59. O'Brochta, D. A. and Bryant, P. J. (1987). Distribution of S-phase cells during the regeneration of Drosophila imaginal wing discs. Dev. Biol. 119, 137-142.
60. 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. (Pubitemid 39625203)
61. 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. (Pubitemid 41803554)
62. Perez-Garijo, A., Shlevkov, E. and Morata, G. (2009). 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 136, 1169-1177.
63. Poss, K. D. (2007). Getting to the heart of regeneration in zebrafish. Semin. Cell Dev. Biol. 18, 36-45.
64. Ramet, M., Lanot, R., Zachary, D. and Manfruelli, P. (2002). JNK signaling pathway is required for efficient wound healing in Drosophila. Dev. Biol. 241, 145-156. (Pubitemid 34066768)
65. Reinhardt, C. A. and Bryant, P. J. (1981). Wound healing in the imaginal discs of Drosophila. II. Transmission electron microscopy of normal and healing wing discs. J. Exp. Zool. 216, 45-61.
66. Reinhardt, C. A., Hodgkin, N. M. and Bryant, P. J. (1977). Wound healing in the imaginal discs of Drosophila. I. Scanning electron microscopy of normal and healing wing discs. Dev. Biol. 60, 238-257.
67. Rogulja, D. and Irvine, K. D. (2005). Regulation of cell proliferation by a morphogen gradient. Cell 123, 449-461. (Pubitemid 41546675)
68. Russell, M. A., Ostafichuk, L. and Scanga, S. (1998). Lethal P-lacZ insertion lines expressed during pattern respecification in the imaginal discs of Drosophila. Genome 41, 7-13. (Pubitemid 28226452)
69. 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. (Pubitemid 39341835)
70. Salmeron, J. M., Jr, Leuther, K. K. and Johnston, S. A. (1990). GAL4 mutations that separate the transcriptional activation and GAL80-interactive functions of the yeast GAL4 protein. Genetics 125, 21-27.
71. Schubiger, G. (1971). Regeneration, duplication and transdetermination in fragments of the leg disc of Drosophila melanogaster. Dev. Biol. 26, 277-295.
72. Shraiman, B. I. (2005). Mechanical feedback as a possible regulator of tissue growth. Proc. Natl. Acad. Sci. USA 102, 3318-3323.
73. Slack, J. M., Lin, G. and Chen, Y. (2008). The Xenopus tadpole: a new model for regeneration research. Cell Mol. Life Sci. 65, 54-63.
74. Smith-Bolton, R. K., Worley, M. I., Kanda, H. and Hariharan, I. K. (2009). Regenerative growth in Drosophila imaginal discs is regulated by Wingless and Myc. Dev. Cell 16, 797-809.
75. Struhl, G. and Basler, K. (1993). Organizing activity of wingless protein in Drosophila. Cell 72, 527-540. (Pubitemid 23077741)
76. Szabad, J., Simpson, P. and Nothiger, R. (1979). Regeneration and compartments in Drosophila. J. Embryol. Exp. Morphol. 49, 229-241.
77. Weber, U., Paricio, N. and Mlodzik, M. (2000). Jun mediates Frizzled-induced R3/R4 cell fate distinction and planar polarity determination in the Drosophila eye. Development 127, 3619-3629.
78. Wells, B. S., Yoshida, E. and Johnston, L. A. (2006). Compensatory proliferation in Drosophila imaginal discs requires Dronc-dependent p53 activity. Curr. Biol. 16, 1606-1615. (Pubitemid 44233289)
79. Weston, C. R., Wong, A., Hall, J. P., Goad, M. E., Flavell, R. A. and Davis, R. J. (2004). The c-Jun NH2-terminal kinase is essential for epidermal growth factor expression during epidermal morphogenesis. Proc. Natl. Acad. Sci. USA 101, 14114-14119. (Pubitemid 39305039)
80. Wing, J. P., Zhou, L., Schwartz, L. M. and Nambu, J. R. (1998). Distinct cell killing properties of the Drosophila reaper, head involution defective, and grim genes. Cell Death Differ. 5, 930-939. (Pubitemid 28510695)
81. Wood, W., Jacinto, A., Grose, R., Woolner, S., Gale, J., Wilson, C. and Martin, P. (2002). Wound healing recapitulates morphogenesis in Drosophila embryos. Nat. Cell Biol. 4, 907-912. (Pubitemid 35331367)
82. 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. (Pubitemid 34746159)
83. Zeidler, M. P., Tan, C., Bellaiche, Y., Cherry, S., Hader, S., Gayko, U. and Perrimon, N. (2004). Temperature-sensitive control of protein activity by conditionally splicing inteins. Nat. Biotechnol. 22, 871-876. (Pubitemid 38886607)
84. Zeitlinger, J. and Bohmann, D. (1999). Thorax closure in Drosophila: involvement of Fos and the JNK pathway. Development 126, 3947-3956. (Pubitemid 29440491)
85. Zenz, R., Scheuch, H., Martin, P., Frank, C., Eferl, R., Kenner, L., Sibilia, M. and Wagner, E. F. (2003). c-Jun regulates eyelid closure and skin tumor development through EGFR signaling. Dev. Cell 4, 879-889. (Pubitemid 36676039)