Drosophila p53 controls Notch expression and balances apoptosis and proliferation

Apoptosis

Volumn 19, Issue 10, 2014, Pages 1430-1443

  Simón, Rocío ^a   Aparicio, Ricardo ^a   Housden, Ben E ^b   Bray, Sarah ^b   Busturia, Ana ^a  

^a CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Apoptosis; Dp53; Drosophila; Notch transcription; Proliferation; Wing

Indexed keywords

MESSENGER RNA; NOTCH RECEPTOR; PROTEIN P53; DROSOPHILA PROTEIN; NOTCH PROTEIN, DROSOPHILA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; DROSOPHILA; FORELIMB; GAIN OF FUNCTION MUTATION; GENE INTERACTION; LOSS OF FUNCTION MUTATION; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; UPREGULATION; VERTEBRATE; ANIMAL; CYTOLOGY; DROSOPHILA MELANOGASTER; FEMALE; GENETICS; MALE; METABOLISM;

VERTEBRATA;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; MALE; RECEPTORS, NOTCH; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84919843164     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-014-1000-5     Document Type: Article

References (65)

1. Hollstein M, Sidransky D, Vogelstein B, Harris CC (1991) p53 mutations in human cancers. Science 253(5015):49-53
2. El-Deiry WS, Kern SE, Pietenpol JA, Kinzler KW, Vogelstein B (1992) Definition of a consensus binding site for p53. Nat Genet 1(1):45-49
3. Funk WD, Pak DT, Karas RH, Wright WE, Shay JW (1992) A transcriptionally active DNA-binding site for human p53 protein complexes. Mol Cell Biol 12(6):2866-2871
4. Haupt Y, Maya R, Kazaz A, Oren M (1997) Mdm2 promotes the rapid degradation of p53. Nature 387(6630):296-299
5. Kubbutat MH, Jones SN, Vousden KH (1997) Regulation of p53 stability by Mdm2. Nature 387(6630):299-303
6. Riley T, Sontag E, Chen P, Levine A (2008) Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 9(5):402-412
7. Vousden KH, Lane DP (2007) p53 in health and disease. Nat Rev Mol Cell Biol 8(4):275-283
8. Gonzalez C (2013) Drosophila melanogaster: a model and a tool to investigate malignancy and identify new therapeutics. Nat Rev Cancer 13(3):172-183
9. Fuchs Y, Steller H (2011) Programmed cell death in animal development and disease. Cell 147(4):742-758
10. Wing JP, Schwartz LM, Nambu JR (2001) The RHG motifs of Drosophila Reaper and Grim are important for their distinct cell death-inducing abilities. Mech Dev 102(1-2):193-203
11. Ollmann M, Young LM, Di Como CJ, Karim F, Belvin M, Robertson S, Whittaker K, Demsky M, Fisher WW, Buchman A, Duyk G, Friedman L, Prives C, Kopczynski C (2000) Drosophila p53 is a structural and functional homolog of the tumor suppressor p53. Cell 101(1):91-101
12. Jin S, Martinek S, Joo WS, Wortman JR, Mirkovic N, Sali A, Yandell MD, Pavletich NP, Young MW, Levine AJ (2000) Identification and characterization of a p53 homologue in Drosophila melanogaster. Proc Natl Acad Sci USA 97(13):7301-7306
13. Marcel V, Dichtel-Danjoy ML, Sagne C, Hafsi H, Ma D, Ortiz- Cuaran S, Olivier M, Hall J, Mollereau B, Hainaut P, Bourdon JC (2011) Biological functions of p53 isoforms through evolution: lessons from animal and cellular models. Cell Death Differ 18(12):1815-1824
14. Dichtel-Danjoy ML, Ma D, Dourlen P, Chatelain G, Napoletano F, Robin M, Corbet M, Levet C, Hafsi H, Hainaut P, Ryoo HD, Bourdon JC, Mollereau B (2013) Drosophila p53 isoforms differentially regulate apoptosis and apoptosis-induced proliferation. Cell Death Differ 20(1):108-116. doi:10.1038/cdd.2012.100
15. Sogame N, Kim M, Abrams JM (2003) Drosophila p53 preserves genomic stability by regulating cell death. Proc Natl Acad Sci USA 100(8):4696-4701
16. Brodsky MH, Nordstrom W, Tsang G, Kwan E, Rubin GM, Abrams JM (2000) Drosophila p53 binds a damage response element at the reaper locus. Cell 101(1):103-113
17. Ryoo HD, Gorenc T, Steller H (2004) Apoptotic cells can induce compensatory cell proliferation through the JNK and the Wingless signaling pathways. Dev Cell 7(4):491-501
18. Brodsky MH, Weinert BT, Tsang G, Rong YS, McGinnis NM, Golic KG, Rio DC, Rubin GM (2004) Drosophila melanogaster MNK/Chk2 and p53 regulate multiple DNA repair and apoptotic pathways following DNA damage. Mol Cell Biol 24(3):1219-1231
19. Mandal S, Freije WA, Guptan P, Banerjee U (2010)Metabolic control of G1-S transition: cyclin E degradation by p53-induced activation of the ubiquitin-proteasome system. J Cell Biol 188(4):473-479
20. Biteau B, Jasper H (2009) It's all about balance: p53 and aging. Aging (Albany NY) 1(11):884-886
21. Wells BS, Johnston LA (2012) Maintenance of imaginal disc plasticity and regenerative potential in Drosophila by p53. Dev Biol 361(2):263-276
22. Mollereau B, Perez-Garijo A, Bergmann A, Miura M, Gerlitz O, Ryoo HD, Steller H, Morata G (2012) Compensatory proliferation and apoptosis-induced proliferation: a need for clarification. Cell Death Differ 20(1):181
23. Ryoo HD, Bergmann A (2012) The role of apoptosis-induced proliferation for regeneration and cancer. Cold Spring Harb Perspect Biol 4(8):a008797
24. Perez-Garijo A, Shlevkov E, 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(7):1169-1177
25. Chera S, Ghila L, Dobretz K, Wenger Y, Bauer C, Buzgariu W, Martinou JC, Galliot B (2009) Apoptotic cells provide an unexpected source of Wnt3 signaling to drive hydra head regeneration. Dev Cell 17(2):279-289
26. Fan Y, Bergmann A (2008) Distinct mechanisms of apoptosis-induced compensatory proliferation in proliferating and differentiating tissues in the Drosophila eye. Dev Cell 14(3):399-410
27. Huang Q, Li F, Liu X, Li W, Shi W, Liu FF, O'Sullivan B, He Z, Peng Y, Tan AC, Zhou L, Shen J, Han G, Wang XJ, Thorburn J, Thorburn A, Jimeno A, Raben D, Bedford JS, Li CY (2011) Caspase 3-mediated stimulation of tumor cell repopulation during cancer radiotherapy. Nat Med 17(7):860-866
28. Bray SJ (2006) Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7(9):678-689
29. Ranganathan P, Weaver KL, Capobianco AJ (2011) Notch signalling in solid tumours: a little bit of everything but not all the time. Nat Rev Cancer 11(5):338-351
30. Mohr OL (1919) Character changes caused by mutation of an entire region of a chromosome in Drosophila. Genetics 4(3): 275-282
31. Herranz H, Milan M (2008) Signalling molecules, growth regulators and cell cycle control in Drosophila. Cell Cycle 7(21):3335-3337
32. Go MJ, Eastman DS, Artavanis-Tsakonas S (1998) Cell proliferation control by Notch signaling in Drosophila development. Development 125(11):2031-2040
33. Baonza A, Garcia-Bellido A (2000) Notch signaling directly controls cell proliferation in the Drosophila wing disc. Proc Natl Acad Sci USA 97(6):2609-2614
34. Guruharsha KG, Kankel MW, Artavanis-Tsakonas S (2012) The Notch signalling system: recent insights into the complexity of a conserved pathway. Nat Rev Genet 13(9):654-666. doi:10.1038/nrg3272
35. Alimirah F, Panchanathan R, Davis FJ, Chen J, Choubey D (2007) Restoration of p53 expression in human cancer cell lines upregulates the expression of Notch1: implications for cancer cell fate determination after genotoxic stress. Neoplasia 9(5):427-434
36. Yugawa T, Handa K, Narisawa-Saito M, Ohno S, Fujita M, Kiyono T (2007) Regulation of Notch1 gene expression by p53 in epithelial cells. Mol Cell Biol 27(10):3732-3742
37. Ungerback J, Elander N, Grunberg J, Sigvardsson M, Soderkvist P (2011) The Notch-2 gene is regulated by Wnt signaling in cultured colorectal cancer cells. PLoS One 6(3):e17957
38. Wu J, Iwata F, Grass JA, Osborne CS, Elnitski L, Fraser P, Ohneda O, Yamamoto M, Bresnick EH (2005) Molecular determinants of NOTCH4 transcription in vascular endothelium. Mol Cell Biol 25(4):1458-1474
39. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118(2):401-415
40. Hay BA, Wassarman DA, Rubin GM (1995) Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83(7):1253-1262
41. Bourdon JC, Fernandes K, Murray-Zmijewski F, Liu G, Diot A, Xirodimas DP, Saville MK, Lane DP (2005) p53 isoforms can regulate p53 transcriptional activity. Genes Dev 19(18): 2122-2137
42. Cohen B, McGuffin ME, Pfeifle C, Segal D, Cohen SM (1992) Apterous, a gene required for imaginal disc development in Drosophila encodes a member of the LIM family of developmental regulatory proteins. Genes Dev 6(5):715-729
43. Housden BE, Millen K, Bray SJ (2012) Drosophila reporter vectors compatible with PhiC31 integrase transgenesis techniques and their use to generate new notch reporter fly lines. G3 (Bethesda) 2(1):79-82
44. Gonzalez I, Busturia A (2009) High levels of dRYBP induce apoptosis in Drosophila imaginal cells through the activation of reaper and the requirement of trithorax, dredd and dFADD. Cell Res 19(6):747-757
45. Aparicio R, Neyen C, Lemaitre B, Busturia A (2013) dRYBP contributes to the negative regulation of the Drosophila Imd pathway. PLoS One 8(4):e62052
46. Classen AK, Bunker BD, Harvey KF, Vaccari T, Bilder D (2009) A tumor suppressor activity of Drosophila Polycomb genes mediated by JAK-STAT signaling. Nat Genet 41(10):1150-1155
47. Gonzalez I, Aparicio R, Busturia A (2008) Functional characterization of the dRYBP gene in Drosophila. Genetics 179(3):1373-1388
48. Ryoo HD, Bergmann A, Gonen H, Ciechanover A, Steller H (2002) Regulation of Drosophila IAP1 degradation and apoptosis by reaper and ubcD1. Nat Cell Biol 4(6):432-438
49. Lee JH, Lee E, Park J, Kim E, Kim J, Chung J (2003) In vivo p53 function is indispensable for DNA damage-induced apoptotic signaling in Drosophila. FEBS Lett 550(1-3):5-10
50. Blochlinger K, Bodmer R, Jack J, Jan LY, Jan YN (1988) Primary structure and expression of a product from cut, a locus involved in specifying sensory organ identity in Drosophila. Nature 333(6174):629-635
51. Micchelli CA, Rulifson EJ, Blair SS (1997) The function and regulation of cut expression on the wing margin of Drosophila: Notch, Wingless and a dominant negative role for Delta and Serrate. Development 124(8):1485-1495
52. Mesquita D, Dekanty A, Milan M (2010) A dp53-dependent mechanism involved in coordinating tissue growth in Drosophila. PLoS Biol 8(12):e1000566
53. Johansen KM, Fehon RG, Artavanis-Tsakonas S (1989) The notch gene product is a glycoprotein expressed on the cell surface of both epidermal and neuronal precursor cells during Drosophila development. J Cell Biol 109(5):2427-2440
54. Giraldez AJ, Cohen SM (2003) Wingless and Notch signaling provide cell survival cues and control cell proliferation during wing development. Development 130(26):6533-6543
55. Neumann CJ, Cohen SM (1996) A hierarchy of cross-regulation involving Notch, wingless, vestigial and cut organizes the dorsal/ ventral axis of the Drosophila wing. Development 122(11):3477-3485
56. Rafel N, Milan M (2008) Notch signalling coordinates tissue growth and wing fate specification in Drosophila. Development 135(24):3995-4001
57. Beckerman R, Prives C (2010) Transcriptional regulation by p53. Cold Spring Harb Perspect Biol 2(8):a000935
58. Lozano G (2010) Mouse models of p53 functions. Cold Spring Harb Perspect Biol 2(4):a001115
59. Green DR, Kroemer G (2009) Cytoplasmic functions of the tumour suppressor p53. Nature 458(7242):1127-1130
60. Espinosa JM, Verdun RE, Emerson BM (2003) p53 functions through stress- and promoter-specific recruitment of transcription initiation components before and after DNA damage. Mol Cell 12(4):1015-1027
61. Shaked H, Shiff I, Kott-Gutkowski M, Siegfried Z, Haupt Y, Simon I (2008) Chromatin immunoprecipitation-on-chip reveals stress-dependent p53 occupancy in primary normal cells but not in established cell lines. Cancer Res 68(23):9671-9677
62. Lefort K, Mandinova A, Ostano P, Kolev V, Calpini V, Kolfschoten I, Devgan V, Lieb J, Raffoul W, Hohl D, Neel V, Garlick J, Chiorino G, Dotto GP (2007) Notch1 is a p53 target gene involved in human keratinocyte tumor suppression through negative regulation of ROCK1/2 and MRCKalpha kinases. Genes Dev 21(5):562-577
63. Dotto GP (2009) Crosstalk of Notch with p53 and p63 in cancer growth control. Nat Rev Cancer 9(8):587-595
64. Perez-Garijo A, Martin FA, Morata G (2004) Caspase inhibition during apoptosis causes abnormal signalling and developmental aberrations in Drosophila. Development 131(22):5591-5598
65. Kondo S, Senoo-Matsuda N, Hiromi Y, Miura M (2006) DRONC coordinates cell death and compensatory proliferation. Mol Cell Biol 26(19):7258-7268