Regulation of cellular plasticity in Drosophila imaginal disc cells by the Polycomb group, trithorax group and lama genes

Development

Volumn 132, Issue 16, 2005, Pages 3753-3765

  Klebes, Ansgar ^a,c   Sustar, Anne ^b   Kechris, Katherina ^a   Li, Hao ^a   Schubiger, Gerold ^b   Kornberg, Thomas B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Cellular plasticity; Expression profiling; Imaginal disc; Polycomb group; Transdetermination; Trithorax group

Indexed keywords

DNA; NOTCH RECEPTOR; REGULATOR PROTEIN; RNA; TRANSCRIPTION FACTOR; WNT PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL HYBRIDIZATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA MICROARRAY; DROSOPHILA; FEMALE; FORELIMB; GENE AMPLIFICATION; GENE EXPRESSION PROFILING; GENE NUMBER; GENETIC DIFFERENCE; IMAGINAL DISC; LEG; LIVER REGENERATION; MUTANT; NONHUMAN; ORTHOLOGY; PLASTICITY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REGULATORY MECHANISM; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYONIC STRUCTURES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; MORPHOGENESIS; MULTIGENE FAMILY; NERVE TISSUE PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TRANSCRIPTION FACTORS;

EID: 24944520037     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01927     Document Type: Article

References (77)

1. Adams, G. A., Maestri, M., Squiers, E. C., Alfrey, E. J., Starzl, T. E. and Dafoe, D. C. (1998). Augmenter of liver regeneration enhances the success rate of fetal pancreas transplantation in rodents. Transplantation 65, 32-36.
2. Adams, M. D., Celniker, S. E., Holt, R. A., Evans, C. A., Gocayne, J. D., Amanatides, P. G., Scherer, S. E., Li, P. W., Hoskins, R. A., Galle, R. F. et al. (2000). The genome sequence of Drosophila melanogaster. Science 287, 2185-2195.
3. Adler, P. N., Charlton, J. and Brunk, B. (1989). Genetic interactions of the suppressor 2 of zeste region genes. Dev. Genet. 10, 249-260.
4. Bach, E. A., Vincent, S., Zeidler, M. P. and Perrimon, N. (2003). A sensitized genetic screen to identify novel regulators and components of the Drosophila jams kinase/signal transducer and activator of transcription pathway. Genetics 165, 1149-1166.
5. Baker, N. E. (1988). Transcription of the segment-polarity gene wingless in the imaginal discs of Drosophila, and the phenotype of a pupal-lethal wg mutation. Development 102, 489-497.
6. Barker, N., Hurlstone, A., Musisi, H., Miles, A., Bienz, M. and Clevers, H. (2001). The chromatin remodelling factor Brg-1 interacts with beta-catenin to promote target gene activation. EMBO J 20, 4935-4943.
7. Benjamini, Y., Drai, D., Elmer, G., Kafkafi, N. and Golani, I. (2001). Controlling the false discovery rate in behavior genetics research. Behav. Brain Res. 125, 279-284.
8. Berman, B. P., Nibu, Y., Pfeiffer, B. D., Tomancak, P., Celniker, S. E., Levine, M., Rubin, G. M. and Eisen, M. B. (2002). Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. Proc. Natl. Acad. Sci. USA 99, 757-762.
9. Bierie, B., Nozawa, M., Renou, J. P., Shillingford, J. M., Morgan, F., Oka, T., Taketo, M. M., Cardiff, R. D., Miyoshi, K., Wagner, K. U. et al. (2003). Activation of beta-catenin in prostate epithelium induces hyperplasias and squamous transdifferentiation. Oncogene 22, 3875-3887.
10. Bornemann, D., Miller, E. and Simon, J. (1998). Expression and properties of wild-type and mutant forms of the Drosophila sex comb on midleg (SCM) repressor protein. Genetics 150, 675-686.
11. Brumby, A. M., Zraly, C. B., Horsfield, J. A., Secombe, J., Saint, R., Dingwall, A. K. and Richardson, H. (2002). Drosophila cyclin E interacts with components of the Brahma complex. EMBO J. 21, 3377-3389.
12. Bussemaker, H. J., Li, H. and Siggia, E. D. (2001). Regulatory element detection using correlation with expression. Nat. Genet. 27, 167-171.
13. Cohen, B., McGuffin, M. E., Pfeifle, C., Segal, D. and Cohen, S. M. (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, 715-729.
14. Collins, R. T. and Treisman, J. E. (2000). Osa-containing Brahma chromatin remodeling complexes are required for the repression of wingless target genes. Genes Dev. 14, 3140-3152.
15. Corpet, F. (1988). Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16, 10881-10890.
16. Couso, J. P., Knust, E. and Martinez Arias, A. (1995). Serrate and wingless cooperate to induce vestigial gene expression and wing formation in Drosophila. Curr. Biol. 5, 1437-1448.
17. Diaz-Benjumea, F. J. and Cohen, S. M. (1993). Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila. Cell 75, 741-752.
18. Eisen, M. B., Spellman, P. T., Brown, P. O. and Botstein, D. (1998). Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95, 14863-14868.
19. Frith, M. C., Hansen, U. and Weng, Z. (2001). Detection of cis-element clusters in higher eukaryotic DNA. Bioinformatics 10, 878-889.
20. Gildea, J. J., Lopez, R. and Shearn, A. (2000). A screen for new trithorax group genes identified little imaginal discs, the Drosophila melanogaster homologue of human retinoblastoma binding protein 2. Genetics 156, 645-663.
21. Gindhart, J. G., Jr and Kaufman, T. C. (1995). Identification of Polycomb and trithorax group responsive elements in the regulatory region of the Drosophila homeotic gene Sex combs reduced. Genetics 139, 797-814.
22. Gonzalez-Reyes, A. (2003). Stem cells, niches and cadherins: a view from Drosophila. J. Cell Sci. 116, 949-954.
23. Hadorn, E. (1963). Differenzierungsleistungen wiederholt fragmentierter Teilstücke männlicher Genitalscheiben von Drosophila melanogaster nach Dauerkultur in vivo. Dev. Biol. 7, 617-629.
24. Hadorn, E. (1965). Problems of determination and transdetermination. Brookhaven Symp. Biol. 18, 148-161.
25. Hagiya, M., Francavilla, A., Polimeno, L., Ihara, I., Sakai, H., Seki, T., Shimonishi, M., Porter, K. A. and Starzl, T. E. (1994). Cloning and sequence analysis of the rat augmenter of liver regeneration (ALR) gene: expression of biologically active recombinant ALR and demonstration of tissue distribution. Proc. Natl. Acad. Sci. USA 91, 8142-8146.
26. Halder, G., Polaczyk, P., Kraus, M. E., Hudson, A., Kim, J., Laughon, A. and Carroll, S. (1998). The Vestigial and Scalloped proteins act together to directly regulate wing-specific gene expression in Drosophila. Genes Dev. 12, 3900-3909.
27. Harrison, D. A., McCoon, P. E., Binari, R., Gilman, M. and Perrimon, N. (1998). Drosophila unpaired encodes a secreted protein that activates the JAK signaling pathway. Genes Dev. 12, 3252-3263.
28. Hirose, F., Yamaguchi, M., Kuroda, K., Omori, A., Hachiya, T., Ikeda, M., Nishimoto, Y. and Matsukage, A. (1996). Isolation and characterization of cDNA for DREF, a promoter-activating factor for Drosophila DNA replication-related genes. J. Biol. Chem. 271, 3930-3937.
29. Hombria, J. C. and Brown, S. (2002). The fertile field of Drosophila Jak/STAT signalling. Curr. Biol. 12, R569-R575.
30. Ihaka, R. and Gentleman, R. R. (1996). A language for data analysis and graphics. J. Comp. Graphic. Stat. 5, 2344-2999.
31. Jankowski, J. A., Wright, N. A., Meltzer, S. J., Triadafilopoulos, G., Geboes, K., Casson, A. G., Kerr, D. and Young, L. S. (1999). Molecular evolution of the metaplasia-dysplasia-adenocarcinoma sequence in the esophagus. Am. J. Pathol. 154, 965-973.
32. Janson, K., Cohen, E. D. and Wilder, E. L. (2001). Expression of DWnt6, DWnt10, and DFz4 during Drosophila development. Mech. Dev. 103, 117-120.
33. Johnston, L. A. and Schubiger, G. (1996). Ectopic expression of wingless in imaginal discs interferes with decapentaplegic expression and alters cell determination. Development 122, 3519-3529.
34. Jones, R. S. and Gelbart, W. M. (1990). Genetic analysis of the enhancer of zeste locus and its role in gene regulation in Drosophila melanogaster. Genetics 126, 185-199.
35. Kim, J., Sebring, A., Esch, J. J., Kraus, M. E., Vorwerk, K., Magee, J. and Carroll, S. B. (1996). Integration of positional signals and regulation of wing formation and identity by Drosophila vestigial gene. Nature 382, 133-138.
36. Klebes, A., Biehs, B., Cifuentes, F. and Kornberg, T. B. (2002). Expression profiling of Drosophila imaginal discs. Genome Biol. 3, R0038.
37. Klein, T. and Arias, A. M. (1999). The vestigial gene product provides a molecular context for the interpretation of signals during the development of the wing in Drosophila. Development 126, 913-925.
38. Kurata, S., Go, M. J., Artavanis-Tsakonas, S. and Gehring, W. J. (2000). Notch signaling and the determination of appendage identity. Proc. Natl. Acad. Sci. USA 97, 2117-2122.
39. Lindsley, D. L. and Zimm, G. G. (1992). The Genome of Drosophila melanogaster. San Diego, CA: Academic Press.
40. Lisowsky, T., Weinstat-Saslow, D. L., Barton, N., Reeders, S. T. and Schneider, M. C. (1995). A new human gene located in the PKD1 region of chromosome 16 is a functional homologue to ERV1 of yeast. Genomics 29, 690-697.
41. Lund, A. H. and van Lohuizen, M. (2004). Polycomb complexes and silencing mechanisms. Curr. Opin. Cell Biol. 16, 239-246.
42. Maves, L. and Schubiger, G. (1995). Wingless induces transdetermination in developing Drosophila imaginal discs. Development 121, 1263-1272.
43. Maves, L. and Schubiger, G. (1998). A molecular basis for transdetermination in Drosophila imaginal discs: interactions between wingless and decapentaplegic signaling. Development 125, 115-124.
44. Maves, L. and Schubiger, G. (2003). Transdetermination in Drosophila imaginal discs: a model for understanding pluripotency and selector gene maintenance. Curr. Opin. Genet. Dev. 13, 472-479.
45. Merrill, B. J., Gat, U., DasGupta, R. and Fuchs, E. (2001). Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin. Genes Dev. 15, 1688-1705.
46. Miyoshi, K., Shillingford, J. M., Le Provost, F., Gounari, F., Bronson, R., von Boehmer, H., Taketo, M. M., Cardiff, R. D., Hennighausen, L. and Khazaie, K. (2002). Activation of beta-catenin signaling in differentiated mammary secretory cells induces transdifferentiation into epidermis and squamous metaplasias. Proc. Natl. Acad. Sci. USA 99, 219-224.
47. Niemann, C., Owens, D. M., Hulsken, J., Birchmeier, W. and Watt, F. M. (2002). Expression of DeltaNLef1 in mouse epidermis results in differentiation of hair follicles into squamous epidermal cysts and formation of skin tumours. Development 129, 95-109.
48. O'Neill, J. W. and Bier, E. (1994). Double-label in situ hybridization using biotin and digoxigenin-tagged RNA probes. Biotechniques 17, 870, 874-875.
49. Okubo, T. and Hogan, B. L. (2004). Hyperactive Wnt signaling changes the developmental potential of embryonic lung endoderm. J. Biol. 3, 11.
50. Paro, R., Strutt, H. and Cavalli, G. (1998). Heritable chromatin states induced by the Polycomb and trithorax group genes. Novartis Found. Symp. 214, 51-61; discussion 61-66, 104-113.
51. Paumard-Rigal, S., Zider, A., Vaudin, P. and Silber, J. (1998). Specific interactions between vestigial and scalloped are required to promote wing tissue proliferation in Drosophila melanogaster. Dev. Genes Evol. 208, 440-446.
52. Perez, S. E. and Steller, H. (1996). Molecular and genetic analyses of lama, an evolutionarily conserved gene expressed in the precursors of the Drosophila first optic ganglion. Mech. Dev. 59, 11-27.
53. Petruk, S., Sedkov, Y., Smith, S., Tillib, S., Kraevski, V., Nakamura, T., Canaani, E., Croce, C. M. and Mazo, A. (2001). Trithorax and dCBP acting in a complex to maintain expression of a homeotic gene. Science 294, 1331-1334.
54. Pueyo, J. I., Galindo, M. I., Bishop, S. A. and Couso, J. P. (2000). Proximal-distal leg development in Drosophila requires the apterous gene and the Lim1 homologue dlim1. Development 127, 5391-5402.
55. Raftery, L. A., Sanicola, M., Blackman, R. K. and Gelbart, W. M. (1991). The relationship of decapentaplegic and engrailed expression in Drosophila imaginal disks: do these genes mark the anterior-posterior compartment boundary? Development 113, 27-33.
56. Ramalho-Santos, M., Yoon, S., Matsuzaki, Y., Mulligan, R. C. and Melton, D. A. (2002). 'Stemness': transcriptional profiling of embryonic and adult stem cells. Science 298, 597-600.
57. Reya, T., Duncan, A. W., Ailles, L., Domen, J., Scherer, D. C., Willert, K., Hintz, L., Nusse, R. and Weissman, I. L. (2003). A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 423, 409-414.
58. Ringrose, L., Rehmsmeier, M., Dura, J. M. and Paro, R. (2003). Genome-wide prediction of Polycomb/Trithorax response elements in Drosophila melanogaster. Dev. Cell 5, 759-771.
59. Schubiger, G. (1973). Regeneration of Drosophila melanogaster male leg disc fragments in sugar fed female hosts. Experientia 29, 631-632.
60. Schweizer, P. and Bodenstein, D. (1975). Aging and its relation to cell growth and differentiation in Drosophila imaginal discs: developmental response to growth restricting conditions. Proc. Natl. Acad. Sci. USA 72, 4674-4678.
61. Simmonds, A. J., Liu, X., Soanes, K. H., Krause, H. M., Irvine, K. D. and Bell, J. B. (1998). Molecular interactions between Vestigial and Scalloped promote wing formation in Drosophila. Genes Dev. 12, 3815-3820.
62. Sivasankaran, R., Calleja, M., Morata, G. and Basler, K. (2000). The Wingless target gene Dfz3 encodes a new member of the Drosophila Frizzled family. Mech. Dev. 91, 427-431.
63. Smyth, G. K. (2004). Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Statistical Applications in Genetics and Molecular Biology http://www.bepress.com/sagmb/vol3/iss1/art3
64. Soto, M. C., Chou, T. B. and Bender, W. (1995). Comparison of germline mosaics of genes in the Polycomb group of Drosophila melanogaster. Genetics 140, 231-243.
65. Strub, S. (1977). Localization of the cells capable of transdetermiantion in a specific region of the male foreleg disc of Drosophila. Wilhelm Roux's Arch. Dev. Biol. 182, 69-74.
66. Sustar, A. and Schubiger, G. (2005). A transient cell cycle shift in Drosophila imaginal disc cells precedes multipotency. Cell 120, 383-393.
67. Tobler, H. (1966). Zellspezifische Determination and Beziehung zwischen Proliferation and Transdetermination in Bein- und Flu-gelprimordien von Drosophila melanogaster. J. Embryol. Exp. Morphol. 16, 609-633.
68. Trimarchi, J. M., Fairchild, B., Wen, J. and Lees, J. A. (2001). The E2F6 transcription factor is a component of the mammalian Bmi1-containing polycomb complex. Proc. Natl. Acad. Sci. USA 98, 1519-1524.
69. Tusher, V. G., Tibshirani, R. and Chu, G. (2001). Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98, 5116-5121.
70. Valk-Lingbeek, M. E., Bruggeman, S. W. and van Lohuizen, M. (2004). Stem cells and cancer; the polycomb connection. Cell 118, 409-418.
71. van de Wetering, M., Cavallo, R., Dooijes, D., van Beest, M., van, Es, J., Loureiro, J., Ypma, A., Hursh, D., Jones, T., Bejsovec, A. et al. (1997). Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88, 789-799.
72. Vervoort, M., Crozatier, M., Valle, D. and Vincent, A. (1999). The COE transcription factor Collier is a mediator of short-range Hedgehog-induced patterning of the Drosophila wing. Curr. Biol. 9, 632-639.
73. Vierstraete, E., Verleyen, P., Baggerman, G., D'Hertog, W., Van den Bergh, G., Arckens, L., De Loof, A. and Schools, L. (2004). A proteomic approach for the analysis of instantly released wound and immune proteins in Drosophila melanogaster hemolymph. Proc. Natl. Acad. Sci. USA 101, 470-475.
74. Weaver, T. A. and White, R. A. (1995). headcase, an imaginal specific gene required for adult morphogenesis in Drosophila melanogaster. Development 121, 4149-4160.
75. Williams, J. A., Bell, J. B. and Carroll, S. B. (1991). Control of Drosophila wing and haltere development by the nuclear vestigial gene product. Genes Dev. 5, 2481-2495.
76. Xu, E. Y., Lee, D. F., Klebes, A., Turek, P. J., Kornberg, T. B. and Reijo Pera, R. A. (2003). Human BOULE gene rescues meiotic defects in infertile flies. Hum. Mol. Genet. 12, 169-175.
77. Yamaguchi, M., Hayashi, Y., Nishimoto, Y., Hirose, F. and Matsukage, A. (1995). A nucleotide sequence essential for the function of DRE, a common promoter element for Drosophila DNa replication-related genes. J. Biol. Chem. 270, 15808-15814.