Antagonistic regulation of apoptosis and differentiation by the cut transcription factor represents a tumor-suppressing mechanism in drosophila

PLoS Genetics

Volumn 8, Issue 3, 2012, Pages

  Zhai, Zongzhao ^a   Ha, Nati ^a   Papagiannouli, Fani ^a   Hamacher Brady, Anne ^b   Brady, Nathan ^b   Sorge, Sebastian ^a   Bezdan, Daniela ^c   Lohmann, Ingrid ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CUX1 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CUT; UNCLASSIFIED DRUG; CUT PROTEIN, DROSOPHILA; CUX1 PROTEIN, HUMAN; DROSOPHILA PROTEIN; HOMEODOMAIN PROTEIN; NUCLEAR PROTEIN; REAPER PROTEIN, DROSOPHILA; REPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL; CARCINOGENESIS; CELL DEATH; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; NONHUMAN; PROTEIN FUNCTION; REAPER GENE; STEM CELL; VERTEBRATE; ANIMAL; CELL STRAIN HEK293; CELL TRANSFORMATION; DISEASE MODEL; DROSOPHILA MELANOGASTER; GENETICS; METABOLISM; TUMOR SUPPRESSOR GENE;

VERTEBRATA;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CELL LINEAGE; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, TUMOR SUPPRESSOR; HEK293 CELLS; HOMEODOMAIN PROTEINS; HUMANS; NUCLEAR PROTEINS; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS;

EID: 84859226498     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002582     Document Type: Article

References (67)

1. Hanahan D, Weinberg RA, (2000) The hallmarks of cancer. Cell 100: 57-70.
2. Harris H, (2005) A long view of fashions in cancer research. Bioessays 27: 833-838.
3. Shah N, Sukumar S, (2010) The Hox genes and their roles in oncogenesis. Nat Rev Cancer 10: 361-370.
4. Bossuyt W, De Geest N, Aerts S, Leenaerts I, Marynen P, et al. (2009) The Atonal proneural transcription factor links differentiation and tumor formation in Drosophila. PLoS Biol 7: e40 doi:10.1371/journal.pbio.1000040.
5. Vidal M, Cagan RL, (2006) Drosophila models for cancer research. Curr Opin Genet Dev 16: 10-16.
6. Portt L, Norman G, Clapp C, Greenwood M, Greenwood MT, (2011) Anti-apoptosis and cell survival: A review. Biochim Biophys Acta.
7. Pitsouli C, Perrimon N, (2010) Embryonic multipotent progenitors remodel the Drosophila airways during metamorphosis. Development 137: 3615-3624.
8. Werz C, Lee TV, Lee PL, Lackey M, Bolduc C, et al. (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.
9. Hu N, Castelli-Gair J, (1999) Study of the posterior spiracles of Drosophila as a model to understand the genetic and cellular mechanisms controlling morphogenesis. Dev Biol 214: 197-210.
10. Goyal L, McCall K, Agapite J, Hartwieg E, Steller H, (2000) Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. EMBO J 19: 589-597.
11. Bardet PL, Kolahgar G, Mynett A, Miguel-Aliaga I, Briscoe J, et al. (2008) A fluorescent reporter of caspase activity for live imaging. Proc Natl Acad Sci U S A 105: 13901-13905.
12. Hay BA, Wolff T, Rubin GM, (1994) Expression of baculovirus P35 prevents cell death in Drosophila. Development 120: 2121-2129.
13. Merabet S, Catala F, Pradel J, Graba Y, (2002) A green fluorescent protein reporter genetic screen that identifies modifiers of Hox gene function in the Drosophila embryo. Genetics 162: 189-202.
14. Nepveu A, (2001) Role of the multifunctional CDP/Cut/Cux homeodomain transcription factor in regulating differentiation, cell growth and development. Gene 270: 1-15.
15. Hilgers V, Bushati N, Cohen SM, Drosophila microRNAs 263a/b confer robustness during development by protecting nascent sense organs from apoptosis. PLoS Biol 8: e1000396 doi:10.1371/journal.pbio.1000396.
16. Ferres-Marco D, Gutierrez-Garcia I, Vallejo DM, Bolivar J, Gutierrez-Avino FJ, et al. (2006) Epigenetic silencers and Notch collaborate to promote malignant tumours by Rb silencing. Nature 439: 430-436.
17. Palomero T, Sulis ML, Cortina M, Real PJ, Barnes K, et al. (2007) Mutational loss of PTEN induces resistance to NOTCH1 inhibition in T-cell leukemia. Nat Med 13: 1203-1210.
18. Willecke M, Toggweiler J, Basler K, Loss of PI3K blocks cell-cycle progression in a Drosophila tumor model. Oncogene 30: 4067-4074.
19. Pagliarini RA, Xu T, (2003) A genetic screen in Drosophila for metastatic behavior. Science 302: 1227-1231.
20. Mohamet L, Hawkins K, Ward CM, (2011) Loss of function of E-cadherin in embryonic stem cells and the relevance to models of tumorigenesis. J Oncol 2011: 352616.
21. Bokel C, Brown NH, (2002) Integrins in development: moving on, responding to, and sticking to the extracellular matrix. Dev Cell 3: 311-321.
22. Chaffer CL, Weinberg RA, (2011) A perspective on cancer cell metastasis. Science 331: 1559-1564.
23. Sansregret L, Nepveu A, (2008) The multiple roles of CUX1: insights from mouse models and cell-based assays. Gene 412: 84-94.
24. Quaggin SE, Yeger H, Igarashi P, (1997) Antisense oligonucleotides to Cux-1, a Cut-related homeobox gene, cause increased apoptosis in mouse embryonic kidney cultures. J Clin Invest 99: 718-724.
25. Ripka S, Neesse A, Riedel J, Bug E, Aigner A, et al. (2010) CUX1: target of Akt signalling and mediator of resistance to apoptosis in pancreatic cancer. Gut 59: 1101-1110.
26. Sinclair AM, Lee JA, Goldstein A, Xing D, Liu S, et al. (2001) Lymphoid apoptosis and myeloid hyperplasia in CCAAT displacement protein mutant mice. Blood 98: 3658-3667.
27. Woodhouse EC, Liotta LA, (2004) Drosophila invasive tumors: a model for understanding metastasis. Cell Cycle 3: 38-40.
28. Yu J, Wang P, Ming L, Wood MA, Zhang L, (2007) SMAC/Diablo mediates the proapoptotic function of PUMA by regulating PUMA-induced mitochondrial events. Oncogene 26: 4189-4198.
29. Zhou L, Schnitzler A, Agapite J, Schwartz LM, Steller H, et al. (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 U S A 94: 5131-5136.
30. Portales-Casamar E, Thongjuea S, Kwon AT, Arenillas D, Zhao X, et al. (2010) JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res 38: D105-110.
31. Certel K, Anderson MG, Shrigley RJ, Johnson WA, (1996) Distinct variant DNA-binding sites determine cell-specific autoregulated expression of the Drosophila POU domain transcription factor Drifter in midline glia or trachea. Mol Cell Biol 16: 1813-1823.
32. Inbal A, Levanon D, Salzberg A, (2003) Multiple roles for u-turn/ventral veinless in the development of Drosophila PNS. Development 130: 2467-2478.
33. Conradt B, (2009) Genetic control of programmed cell death during animal development. Annu Rev Genet 43: 493-523.
34. Baehrecke EH, (2002) How death shapes life during development. Nat Rev Mol Cell Biol 3: 779-787.
35. Igaki T, (2009) Correcting developmental errors by apoptosis: lessons from Drosophila JNK signaling. Apoptosis 14: 1021-1028.
36. McNeill H, Downward J, (1999) Apoptosis: Ras to the rescue in the fly eye. Curr Biol 9: R176-179.
37. Richardson H, Kumar S, (2002) Death to flies: Drosophila as a model system to study programmed cell death. J Immunol Methods 265: 21-38.
38. Molchadsky A, Rivlin N, Brosh R, Rotter V, Sarig R, (2010) p53 is balancing development, differentiation and de-differentiation to assure cancer prevention. Carcinogenesis 31: 1501-1508.
39. Schmeichel KL, (2004) A fly's eye view of tumor progression and metastasis. Breast Cancer Res 6: 82-83.
40. Balzer EM, Konstantopoulos K, (2011) Intercellular adhesion: mechanisms for growth and metastasis of epithelial cancers. Wiley Interdiscip Rev Syst Biol Med.
41. Wirtz D, Konstantopoulos K, Searson PC, (2011) The physics of cancer: the role of physical interactions and mechanical forces in metastasis. Nat Rev Cancer 11: 512-522.
42. Michl P, Downward J, (2006) CUTL1: a key mediator of TGFbeta-induced tumor invasion. Cell Cycle 5: 132-134.
43. Harada R, Berube G, Tamplin OJ, Denis-Larose C, Nepveu A, (1995) DNA-binding specificity of the cut repeats from the human Cut-like protein. Mol Cell Biol 15: 129-140.
44. Iulianella A, Sharma M, Vanden Heuvel GB, Trainor PA, (2009) Cux2 functions downstream of Notch signaling to regulate dorsal interneuron formation in the spinal cord. Development 136: 2329-2334.
45. Sharma M, Fopma A, Brantley JG, Vanden Heuvel GB, (2004) Coexpression of Cux-1 and Notch signaling pathway components during kidney development. Dev Dyn 231: 828-838.
46. Verhagen AM, Vaux DL, (2002) Cell death regulation by the mammalian IAP antagonist Diablo/Smac. Apoptosis 7: 163-166.
47. Chipuk JE, Green DR, (2009) PUMA cooperates with direct activator proteins to promote mitochondrial outer membrane permeabilization and apoptosis. Cell Cycle 8: 2692-2696.
48. Wasserman WW, Sandelin A, (2004) Applied bioinformatics for the identification of regulatory elements. Nat Rev Genet 5: 276-287.
49. Noyes MB, Christensen RG, Wakabayashi A, Stormo GD, Brodsky MH, et al. (2008) Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell 133: 1277-1289.
50. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034-1050.
51. Lovegrove B, Somoes S, Rivas ML, Sotillos S, Johnson K, et al. (2006) Co-ordinated control of cell adhesion, cell polarity and cytoskeleton underlies Hox induced organogenesis in Drosophila. Curr Biol 16: 2206-2216.
52. Pi H, Wu HJ, Chien CT, (2001) A dual function of phyllopod in Drosophila external sensory organ development: cell fate specification of sensory organ precursor and its progeny. Development 128: 2699-2710.
53. Grueber WB, Jan LY, Jan YN, (2003) Different levels of the homeodomain protein Cut regulate distinct dendrite branching patterns of Drosophila multidendritic neurons. Cell 112: 805-818.
54. Hueber SD, Bezdan D, Henz SR, Blank M, Wu H, et al. (2007) Comparative analysis of Hox downstream genes in Drosophila. Development 134: 381-392.
55. Lohmann I, McGinnis N, Bodmer M, McGinnis W, (2002) The Drosophila Hox gene Deformed sculpts head morphology via direct regulation of the apoptosis activator reaper. Cell 110: 457-466.
56. Stobe P, Stein SM, Habring-Muller A, Bezdan D, Fuchs AL, et al. (2009) Multifactorial regulation of a Hox target gene. PLoS Genet 5: e1000412 doi:10.1371/journal.pgen.1000412.
57. Zhai Z, Stein MA, Lohmann I, (2009) Expression of the apoptosis gene reaper in homeotic, segmentation and other mutants in Drosophila. Gene Expr Patterns 9: 357-363.
58. Barolo S, Carver LA, Posakony JW, (2000) GFP and β-galactosidase transformation vectors for promoter/enhancer analysis in Drosophila. Biotechniques 29: 726-732.
59. Boy AL, Zhai Z, Habring-Muller A, Kussler-Schneider Y, Kaspar P, et al. (2010) Vectors for efficient and high-throughput construction of fluorescent Drosophila reporters using the PhiC31 site-specific integration system. Genesis 48: 452-456.
60. Kosman D, Mizutani CM, Lemons D, Cox WG, McGinnis W, et al. (2004) Multiplex detection of RNA expression in Drosophila embryos. Science 305: 846.
61. Zhai Z, Fuchs AL, Lohmann I, (2010) Cellular analysis of newly identified Hox downstream genes in Drosophila. Eur J Cell Biol 89: 273-278.
62. Stratigopoulos G, LeDuc CA, Cremona ML, Chung WK, Leibel RL, (2011) Cut-like homeobox 1 (CUX1) regulates expression of the fat mass and obesity-associated and retinitis pigmentosa GTPase regulator-interacting protein-1-like (RPGRIP1L) genes and coordinates leptin receptor signaling. J Biol Chem 286: 2155-2170.
63. Blochlinger K, Jan LY, Jan YN, (1993) Postembryonic patterns of expression of cut, a locus regulating sensory organ identity in Drosophila. Development 117: 441-450.
64. Jack J, DeLotto Y, (1995) Structure and regulation of a complex locus: the cut gene of Drosophila. Genetics 139: 1689-1700.
65. Krupp JJ, Yaich LE, Wessells RJ, Bodmer R, (2005) Identification of genetic loci that interact with cut during Drosophila wing-margin development. Genetics 170: 1775-1795.
66. 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: 1485-1495.
67. Ludlow C, Choy R, Blochlinger K, (1996) Functional analysis of Drosophila and mammalian Cut proteins in flies. Dev Biol 178: 149-159.