Apical deficiency triggers JNK-dependent apoptosis in the embryonic epidermis of Drosophila

Development

Volumn 138, Issue 14, 2011, Pages 3021-3031

  Kolahgar, Golnar ^a,b   Bardet, Pierre Luc ^a,c   Langton, Paul F ^a   Alexandre, Cyrille ^a   Vincent, Jean Paul ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c INSTITUT CURIE   (France)

Author keywords

Apical basal polarity; Apoptosis; Drosophila; Epithelial integrity; JNK (Basket); Reaper

Indexed keywords

STRESS ACTIVATED PROTEIN KINASE;

APICAL MEMBRANE; APOPTOSIS; ARTICLE; BASOLATERAL MEMBRANE; CELL JUNCTION; CELL SURVIVAL; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EPIDERMIS CELL; EPITHELIUM CELL; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE; GENE EXPRESSION; GENE OVEREXPRESSION; MALE; MUTANT; NONHUMAN; PRIORITY JOURNAL; REAPER GENE; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; UPREGULATION;

ADHERENS JUNCTIONS; ANIMALS; APOPTOSIS; DROSOPHILA; DROSOPHILA PROTEINS; EPIDERMIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICROARRAY ANALYSIS; PHOSPHOPROTEIN PHOSPHATASES; SIGNAL TRANSDUCTION;

EID: 79959416200     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.059980     Document Type: Article

References (81)

1. Abrams, J. M., White, K., Fessler, L. I. and Steller, H. (1993). Programmed cell death during Drosophila embryogenesis. Development 117, 29-43.
2. Adachi-Yamada, T. and O'Connor, M. B. (2002). Morphogenetic apoptosis: a mechanism for correcting discontinuities in morphogen gradients. Dev. Biol. 251, 74-90.
3. Affolter, M., Nellen, D., Nussbaumer, U. and Basler, K. (1994). Multiple requirements for the receptor serine/threonine kinase thick veins reveal novel functions of TGF beta homologs during Drosophila embryogenesis. Development 120, 3105-3117.
4. Agrawal, N., Kango, M., Mishra, A. and Sinha, P. (1995). Neoplastic transformation and aberrant cell-cell interactions in genetic mosaics of lethal(2)giant larvae (lgl), a tumor suppressor gene of Drosophila. Dev. Biol. 172, 218-229.
5. Baehrecke, E. H. (2002). How death shapes life during development. Nat. Rev. Mol. Cell Biol. 3, 779-787.
6. Bardet, P. L., Kolahgar, G., Mynett, A., Miguel-Aliaga, I., Briscoe, J., Meier, P. and Vincent, J. P. (2008). A fluorescent reporter of caspase activity for live imaging. Proc. Natl. Acad. Sci. USA 105, 13901-13905.
7. Bilder, D. (2004). Epithelial polarity and proliferation control: links from the Drosophila neoplastic tumor suppressors. Genes Dev. 18, 1909-1925.
8. Bilder, D. and Perrimon, N. (2000). Localization of apical epithelial determinants by the basolateral PDZ protein Scribble. Nature 403, 676-680.
9. Bilder, D., Schober, M. and Perrimon, N. (2003). Integrated activity of PDZ protein complexes regulates epithelial polarity. Nat. Cell Biol. 5, 53-58.
10. Blankenship, J. T., Fuller, M. T. and Zallen, J. A. (2007). The Drosophila homolog of the Exo84 exocyst subunit promotes apical epithelial identity. J. Cell Sci. 120, 3099-3110.
11. Bökel, C. and Brown, N. H. (2002). Integrins in development: moving on, responding to, and sticking to the extracellular matrix. Dev. Cell 3, 311-321.
12. Brumby, A., Secombe, J., Horsfield, J., Coombe, M., Amin, N., Coates, D., Saint, R. and Richardson, H. (2004). A genetic screen for dominant modifiers of a cyclin E hypomorphic mutation identifies novel regulators of S-phase entry in Drosophila. Genetics 168, 227-251.
13. Brumby, A. M. and Richardson, H. E. (2003). scribble mutants cooperate with oncogenic Ras or Notch to cause neoplastic overgrowth in Drosophila. EMBO J. 22, 5769-5779.
14. Bulgakova, N. A. and Knust, E. (2009). The Crumbs complex: from epithelial-cell polarity to retinal degeneration. J. Cell Sci. 122, 2587-2596.
15. Campbell, K., Knust, E. and Skaer, H. (2009). Crumbs stabilises epithelial polarity during tissue remodelling. J. Cell Sci. 122, 2604-2612.
16. Devenport, D. and Brown, N. H. (2004). Morphogenesis in the absence of integrins: mutation of both Drosophila beta subunits prevents midgut migration. Development 131, 5405-5415.
17. Dickinson, W. J. and Thatcher, J. W. (1997). Morphogenesis of denticles and hairs in Drosophila embryos: involvement of actin-associated proteins that also affect adult structures. Cell Motil. Cytoskeleton 38, 9-21.
18. Ditzel, M., Wilson, R., Tenev, T., Zachariou, A., Paul, A., Deas, E. and Meier, P. (2003). Degradation of DIAP1 by the N-end rule pathway is essential for regulating apoptosis. Nat. Cell Biol. 5, 467-473.
19. Foe, V. E., Odell, G. M. and Edgar, B. A. (1993). Mitosis and morphogenesis in the Drosophila embryo: point and counterpoint. In The Development of Drosophila melanogaster (ed. M. Bate and A. Martinez Arias), pp. 149-300. New York: Cold Spring Harbor Laboratory Press.
20. Frisch, S. M. and Screaton, R. A. (2001). Anoikis mechanisms. Curr. Opin. Cell Biol. 13, 555-562.
21. Gentleman, R., Carey, V., Dudoit, S., Irizarry, R. and Huber, W. (2005). Bioinformatics and Computational Biology Solutions Using R and Bioconductor. New York: Springer.
22. Gibson, M. C. and Perrimon, N. (2005). Extrusion and death of DPP/BMPcompromised epithelial cells in the developing Drosophila wing. Science 307, 1785-1789.
23. Grawe, F., Wodarz, A., Lee, B., Knust, E. and Skaer, H. (1996). The Drosophila genes crumbs and stardust are involved in the biogenesis of adherens junctions. Development 122, 951-959.
24. Gumbiner, B. M. (1996). Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84, 345-357.
25. Harden, N. (2002). Signaling pathways directing the movement and fusion of epithelial sheets: lessons from dorsal closure in Drosophila. Differentiation 70, 181-203.
26. Hariharan, I. K. (2006). Growth regulation: a beginning for the hippo pathway. Curr. Biol. 16, R1037-R1039.
27. Harris, K. P. and Tepass, U. (2008). Cdc42 and Par proteins stabilize dynamic adherens junctions in the Drosophila neuroectoderm through regulation of apical endocytosis. J. Cell Biol. 183, 1129-1143.
28. Heitzler, P., Haenlin, M., Ramain, P., Calleja, M. and Simpson, P. (1996). A genetic analysis of pannier, a gene necessary for viability of dorsal tissues and bristle positioning in Drosophila. Genetics 143, 1271-1286.
29. Hermiston, M. L. and Gordon, J. I. (1995). In vivo analysis of cadherin function in the mouse intestinal epithelium: essential roles in adhesion, maintenance of differentiation, and regulation of programmed cell death. J. Cell Biol. 129, 489-506.
30. Herranz, H. and Morata, G. (2001). The functions of pannier during Drosophila embryogenesis. Development 128, 4837-4846.
31. Hughes, S. C. and Krause, H. M. (2001). Establishment and maintenance of parasegmental compartments. Development 128, 1109-1118.
32. Hutterer, A., Betschinger, J., Petronczki, M. and Knoblich, J. A. (2004). Sequential roles of Cdc42, Par-6, aPKC, and Lgl in the establishment of epithelial polarity during Drosophila embryogenesis. Dev. Cell 6, 845-854.
33. Igaki, T., Kanda, H., Yamamoto-Goto, Y., Kanuka, H., Kuranaga, E., Aigaki, T. and Miura, M. (2002). Eiger, a TNF superfamily ligand that triggers the Drosophila JNK pathway. EMBO J. 21, 3009-3018.
34. Igaki, T., Pagliarini, R. A. and Xu, T. (2006). Loss of cell polarity drives tumor growth and invasion through JNK activation in Drosophila. Curr. Biol. 16, 1139-1146.
35. Jacinto, A., Woolner, S. and Martin, P. (2002). Dynamic analysis of dorsal closure in Drosophila: from genetics to cell biology. Dev. Cell 3, 9-19.
36. Kim, M., Datta, A., Brakeman, P., Yu, W. and Mostov, K. E. (2007). Polarity proteins PAR6 and aPKC regulate cell death through GSK-3beta in 3D epithelial morphogenesis. J. Cell Sci. 120, 2309-2317.
37. Knust, E., Tepass, U. and Wodarz, A. (1993). crumbs and stardust, two genes of Drosophila required for the development of epithelial cell polarity. Dev. Suppl. 1993, 261-268.
38. 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.
39. Laprise, P., Beronja, S., Silva-Gagliardi, N. F., Pellikka, M., Jensen, A. M., McGlade, C. J. and Tepass, U. (2006). The FERM protein Yurt is a negative regulatory component of the Crumbs complex that controls epithelial polarity and apical membrane size. Dev. Cell 11, 363-374.
40. Leppa, S. and Bohmann, D. (1999). Diverse functions of JNK signaling and c-Jun in stress response and apoptosis. Oncogene 18, 6158-6162.
41. 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.
42. 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.
43. Martinez Arias, A. (1993). Development and patterning of the larval epidermis of Drosophila. In The Development of Drosophila melanogaster (ed. M. Bate and A. Martinez Arias), pp. 517-608. New York: Cold Spring Harbor Laboratory Press.
44. McEwen, D. G. and Peifer, M. (2005). Puckered, a Drosophila MAPK phosphatase, ensures cell viability by antagonizing JNK-induced apoptosis. Development 132, 3935-3946.
45. Meier, P., Finch, A. and Evan, G. (2000). Apoptosis in development. Nature 407, 796-801.
46. Menéndez, J., Pérez-Garijo, A., Calleja, M. and Morata, G. (2010). A tumorsuppressing mechanism in Drosophila involving cell competition and the Hippo pathway. Proc. Natl. Acad. Sci. USA 107, 14651-14656.
47. 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.
48. Muller, H. A. and Wieschaus, E. (1996). armadillo, bazooka, and stardust are critical for early stages in formation of the zonula adherens and maintenance of the polarized blastoderm epithelium in Drosophila. J. Cell Biol. 134, 149-163.
49. Muller, H. A. and Bossinger, O. (2003). Molecular networks controlling epithelial cell polarity in development. Mech. Dev. 120, 1231-1256.
50. Nordstrom, W., Chen, P., Steller, H. and Abrams, J. M. (1996). Activation of the reaper gene during ectopic cell killing in Drosophila. Dev. Biol. 180, 213-226.
51. Noselli, S. and Agnes, F. (1999). Roles of the JNK signaling pathway in Drosophila morphogenesis. Curr. Opin. Genet. Dev. 9, 466-472.
52. Pan, D. (2007). Hippo signalling in organ size control. Genes Dev. 21, 886-897.
53. Pazdera, T. M., Janardhan, P. and Minden, J. S. (1998). Patterned epidermal cell death in wild-type and segment polarity mutant Drosophila embryos. Development 125, 3427-3436.
54. Peterson, C., Carney, G. E., Taylor, B. J. and White, K. (2002). reaper is required for neuroblast apoptosis during Drosophila development. Development 129, 1467-1476.
55. Plant, P. J., Fawcett, J. P., Lin, D. C., Holdorf, A. D., Binns, K., Kulkarni, S. and Pawson, T. (2003). A polarity complex of mPar-6 and atypical PKC binds, phosphorylates and regulates mammalian Lgl. Nat. Cell Biol. 5, 301-308.
56. Ring, J. M. and Martinez Arias, A. (1993). puckered, a gene involved in positionspecific cell differentiation in the dorsal epidermis of the Drosophila larva. Dev. Suppl. 1993, 251-259.
57. Roeth, J. F., Sawyer, J. K., Wilner, D. A. and Peifer, M. (2009). Rab11 helps maintain apical crumbs and adherens junctions in the Drosophila embryonic ectoderm. PLoS ONE 4, e7634.
58. 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.
59. Shen, X. and Kramer, R. H. (2004). Adhesion-mediated squamous cell carcinoma survival through ligand-independent activation of epidermal growth factor receptor. Am. J. Pathol. 165, 1315-1329.
60. Sorrosal, G., Perez, L., Herranz, H. and Milan, M. (2010). Scarface, a secreted serine protease-like protein, regulates polarized localization of laminin A at the basement membrane of the Drosophila embryo. EMBO Rep. 11, 373-379.
61. Srinivasula, S. M., Datta, P., Kobayashi, M., Wu, J. W., Fujioka, M., Hegde, R., Zhang, Z., Mukattash, R., Fernandes-Alnemri, T., Shi, Y. et al. (2002). sickle, a novel Drosophila death gene in the reaper/hid/grim region, encodes an IAP-inhibitory protein. Curr. Biol. 12, 125-130.
62. St Johnston, D. and Ahringer, J. (2010). Cell polarity in eggs and epithelia: parallels and diversity. Cell 141, 757-774.
63. Steller, H. (2008). Regulation of apoptosis in Drosophila. Cell Death Differ. 15, 1132-1138.
64. Suzuki, A. and Ohno, S. (2006). The PAR-aPKC system: lessons in polarity. J. Cell Sci. 119, 979-987.
65. Takeichi, M. (1995). Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7, 619-627.
66. Tanentzapf, G. and Tepass, U. (2003). Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization. Nat. Cell Biol. 5, 46-52.
67. Tenev, T., Zachariou, A., Wilson, R., Paul, A. and Meier, P. (2002). Jafrac2 is an IAP antagonist that promotes cell death by liberating Dronc from DIAP1. EMBO J. 21, 5118-5129.
68. Tepass, U. and Knust, E. (1993). Crumbs and stardust act in a genetic pathway that controls the organization of epithelia in Drosophila melanogaster. Dev. Biol. 159, 311-326.
69. Tepass, U., Theres, C. and Knust, E. (1990). crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell 61, 787-799.
70. Tepass, U., Gruszynski-DeFeo, E., Haag, T. A., Omatyar, L., Torok, T. and Hartenstein, V. (1996). shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes Dev. 10, 672-685.
71. Uemura, T., Oda, H., Kraut, R., Hayashi, S., Kotaoka, Y. and Takeichi, M. (1996). Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Genes Dev. 10, 659-671.
72. Wang, Q. and Margolis, B. (2007). Apical junctional complexes and cell polarity. Kidney Int. 72, 1448-1458.
73. Werz, C., Lee, T. V., Lee, P. L., Lackey, M., Bolduc, C., Stein, D. S. and Bergmann, A. (2005). Mis-specified cells die by an active gene-directed process, and inhibition of this death results in cell fate transformation in Drosophila. Development 132, 5343-5352.
74. Westhoff, M. A. and Fulda, S. (2009). Adhesion-mediated apoptosis resistance in cancer. Drug Resist. Updat. 12, 127-136.
75. Westhoff, M. A., Zhou, S., Bachem, M. G., Debatin, K. M. and Fulda, S. (2008). Identification of a novel switch in the dominant forms of cell adhesionmediated drug resistance in glioblastoma cells. Oncogene 27, 5169-5181.
76. White, K., Grether, M. E., Abrams, J. M., Young, L., Farrell, K. and Steller, H. (1994). Genetic control of programmed cell death in Drosophila. Science 264, 677-683.
77. Wing, J. P., Karres, J. S., Ogdahl, J. L., Zhou, L., Schwartz, L. M. and Nambu, J. R. (2002). Drosophila sickle is a novel grim-reaper cell death activator. Curr. Biol. 12, 131-135.
78. Woods, D. F. and Bryant, P. J. (1991). The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66, 451-464.
79. Yamanaka, T., Horikoshi, Y., Sugiyama, Y., Ishiyama, C., Suzuki, A., Hirose, T., Iwamatsu, A., Shinohara, A. and Ohno, S. (2003). Mammalian Lgl forms a protein complex with PAR-6 and aPKC independently of PAR-3 to regulate epithelial cell polarity. Curr. Biol. 13, 734-743.
80. Zachariou, A., Tenev, T., Goyal, L., Agapite, J., Steller, H. and Meier, P. (2003). IAP-antagonists exhibit non-redundant modes of action through differential DIAP1 binding. EMBO J. 22, 6642-6652.
81. Zhan, L., Rosenberg, A., Bergami, K. C., Yu, M., Xuan, Z., Jaffe, A. B., Allred, C. and Muthuswamy, S. K. (2008). Deregulation of scribble promotes mammary tumorigenesis and reveals a role for cell polarity in carcinoma. Cell 135, 865-878.