The distribution of polycomb-group proteins during cell division and development in Drosophila embryos: Impact on models for silencing

Journal of Cell Biology

Volumn 141, Issue 2, 1998, Pages 469-481

  Buchenau, Peter ^a,e   Hodgson, Jacob ^b   Strutt, Helen ^c,d   Arndt Jovin, Donna J ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d UNIVERSITY OF SHEFFIELD   (United Kingdom)

^e UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; POLYCOMB GROUP PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE; CELL DIVISION; CELL MATURATION; DROSOPHILA; EMBRYO; GENE REPRESSION; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING;

ANIMALS; BLASTODERM; CELL CYCLE; CELL DIVISION; CELL NUCLEUS; DNA; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; INSECT PROTEINS; INTERPHASE; MICROSCOPY, CONFOCAL; NUCLEOPROTEINS; TRANSCRIPTION, GENETIC;

HEXAPODA;

EID: 0032550226     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.141.2.469     Document Type: Article

References (83)

1. Agard, D., Y. Hiraoka, P. Shaw, and J. Sedat. 1989. Fluorescence microscopy in three dimensions. Methods Cell Biol. 30:353-377.
2. Alkema, M., M. Bronk, E. Verhoeven, A. Otte, L. van't Verr, A. Berns, and M. von Lohuizen. 1997. Identification of Bmi1-interacting proteins as constituents of a multimeric mammalian Polycomb complex. Genes Dev. 11:226-240.
3. Allis, C.D., G.L. Waring, and A.P. Mahowald. 1977. Mass isolation of pole cells from Drosophila melanogaster. Dev. Biol. 56:372-381.
4. Aparicio. O.M., B.I. Billington, and D.E. Gottschling. 1991. Modifiers of position effect are shared between telomeric and silent mating-type loci in S. cerevisiae. Cell. 66:1279-1287.
5. Belmont, A.S., M.B. Braunfeld, J.W. Sedat, and D.A. Agard. 1989. Large-scale chromatin structural domains within mitotic and interphase chromosomes in vivo and in vitro. Chromosoma. 98:129-143.
6. Bienz, M. 1992. Molecular mechanisms of determination in Drosophila. Curr. Opin. Cell Biol. 4:955-961.
7. Bienz, M., and J. Müller. 1995. Transcriptional silencing of homeotic genes in Drosophila. Bio Essays. 17:775-784.
8. Brunk, B.P., E.C. Martin, and P.N. Adler. 1991. Drosophila genes posterior sex combs and suppressor two of zeste encode proteins with homology to the murine bmi-1 oncogene. Nature. 353:351-353.
9. Buchenau, P. 1996. Verteilung, funktion und in vivo-dynamik chromosomaler proteine in Drosophila melanogaster. Ph.D. thesis. Humboldt University of Berlin, Berlin, Germany. pp. 105.
10. Buchenau, P., D.J. Arndt-Jovin, and H. Saumweber. 1993. In vivo observation of the puff-specific protein no-on transient A (NONA) in nuclei of Drosophila embryos J. Cell Sci. 106:189-199.
11. Buchenau, P., H. Saumweber, and D.J. Arndt-Jovin. 1997. The dynamic nuclear redistribution of an hnRNP-K homologous protein during Drosophila embryo development and heat shock. Flexibility of transcription sites in vivo. J. Cell Biol. 137:291-303.
12. Campbell, R.B., D.A. Sinclair, M. Couling, and H.W. Brock. 1995. Genetic interactions and dosage effects of Polycomb group genes of Drosophila. Mol. Gen. Genet. 246:291-300.
13. Carrington, E.A., and R.S. Jones. 1996. The Drosophila enhancer of zeste gene encodes a chromosomal protein: examination of wild-type and mutant protein distribution. Development. 122:4073-4083.
14. Cheng, N.N., D.A. Sinclair, R.B. Campbell, and H.W. Brock. 1994. Interactions of polyhomeotic with Polycomb group genes of Drosophila melanogaster. Genetics. 138:1151-1162.
15. Chinwalla, V., E.P. Jane, and P.J. Harte. 1995. The Drosophila trithorax protein binds to specific chromosomal sites and is co-localized with Polycomb at many sites. EMBO J. 14:2056-2065.
16. Csink, A.K., and S. Henikoff. 1996. Genetic modification of heterochromatic association and nuclear organization in Drosophila. Nature. 381:529-531.
17. DeCamillis, M., and H.W. Brock. 1994. Expression of the polyhomeotic locus in development of Drosophila melanogaster. Roux's Arch. Dev. Biol. 203:429-438.
18. DeCamillis, M., N.S. Cheng, D. Pierre, and H.W. Brock. 1992. The polyhomeotic gene of Drosophila encodes a chromatin protein that shares polytene chromosome-binding sites with Polycomb. Genes Dev. 6:223-232.
19. Demandolx, D., and J. Davoust. 1997a. Multicolour analysis and local image correlation in confocal microscopy. J. Microsc. 185:21-36.
20. Demandolx, D., and J. Davoust. 1997b. Multiparameter image cytometry: from confocal micrographs to subcellular fluorograms. Bioimaging. 5:159-169.
21. Dernburg, A.F., K.W. Broman, J.C. Fung, W.F. Marshall, J. Philips, D.A. Agard, and J.W. Sedat. 1996. Perturbation of nuclear architecture by long-distance chromosome interactions. Cell. 85:745-759.
22. Eissenberg, J.C., S.C.R. Elgin, and R. Paro. 1995. Epigenetic regulation in Drosophila: a conspiracy of silence. In Chromatin Structure and Gene Expression. S.C.R. Egin, editor. IRL Press, Oxford, United Kingdom. 147-171.
23. Eissenberg, J.C., T.C. James, D.M. Foster-Hartnett, T. Hartnett, V. Ngan, and S.C.R. Elgin. 1990. Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA. 87:9923-9927.
24. Fauvarque, M.O., V. Zuber, and J.M. Dura. 1995. Regulation of polyhomeotic transcription may involve local changes in chromatin activity in Drosophila. Mech. Dev. 52:343-355.
25. Felsenfeld, G. 1996. Chromatin unfolds. Cell. 86:13-19.
26. Foe, V.E. 1989. Mitotic domains reveal commitment of cells in Drosophila embryos. Development. 107:1-22.
27. Franke, A., M. DeCamillis, D. Zink, N. Cheng, H.W. Brock, and R. Paro. 1992. Polycomb and polyhomeotic are constituents of a multimeric protein complex in chromatin of Drosophila melanogaster. EMBO J. 11:2941-2950.
28. Franke, A., S. Messmer, and R. Paro. 1995. Mapping functional domains of the Polycomb protein of Drosophila melanogaster. Chromosome Res. 3:351-360.
29. Frasch, M., and H. Saumweber. 1989. Two proteins from Drosophila nuclei are bound to chromatin and are detected in a series of puffs on polytene chromosomes. Chromosoma. 97:272-281.
30. Gecz, J., S.J. Gaunt, E. Passage, R.D. Burton, C. Cudrey, J.J. Pearce, and M. Fontes. 1995. Assignment of a Polycomb-like chromobox gene (CBX2) to human chromosome 17q25. Genomics. 26:130-133.
31. Hecht, A., T. Laroche, S. Strahl-Bolsinger, S.M. Gasser, and M. Grunstein. 1995. Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast. Cell. 80: 583-592.
32. Heimer, G.V., and C.E.D. Taylor. 1974. Improved mountant for immunofluorescence preparations. J. Clin. Pathol. 27:254-256.
33. Hirons, G.T., J.J. Fawcett, and H.A. Crissman. 1994. TOTO and YOYO: new very bright fluorochromes for DNA content analyses by flow cytometry. Cytometry. 15:129-140.
34. Jackson, D.A., and P.R. Cook. 1995. The structural basis of nuclear function. Int. Rev. Cytol. 162A:125-149.
35. James, T.C., and S.C.R. Elgin. 1986. Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Mol. Cell. Biol. 6:3862-3872.
36. Johnson, L.M., P.S. Kayne, E.S. Kahn, and M. Grunstein. 1990. Genetic evidence for an interaction between SIR3 and histone H4 in the repression of silent mating loci in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 87:6286-6290.
37. Jones, R.S., and W.M. Gelbart. 1990. Genetic analysis of the enhancer of zeste locus and its role in gene regulation in Drosophila melanogaster. Genetics. 126:185-199.
38. Kanno, M., M. Hasegawa, A. Ishida, K. Isono, and M. Taniguchi. 1995. Mel-18, A polycomb group related mammalian gene, encodes a transcriptional negative regulator with tumor suppressive activity. EMBO J. 14:5672-5678.
39. Kurz, A., S. Lampel, H. Nickolenko, J. Bradl, A. Benner, R. Zierbel, T. Cremer, and P. Lichter. 1996. Active and inactive genes localize preferentially in the periphery of chromosome territories. J. Cell Biol. 135:1195-1205.
40. Lewis, E.B. 1978. A gene complex controlling segmentation in Drosophila. Nature. 276:565-570.
41. Lonie, A., R. D'Andrea, R. Paro, and R. Saint. 1994. Molecular characterisation of the Polycomb like gene of Drosophila melanogaster, a trans-acting negative regulator of homeotic gene expression. Development. 120:2629-2636
42. Martin, E.C., and P.N. Adler. 1993. The polycomb group gene posterior sex combs encodes a chromosomal protein. Development. 117:641-655.
43. Martinez-Balbas, M.A., A. Dey, S.K. Rabindran, K. Ozato, and C. Wu. 1995. Displacement of sequence-specific transcription factors from mitotic chromatin. Cell. 83:29-38.
44. Mathog, D., M. Hochstrasser, Y. Gruenbaum, H. Saumweber, and J. Sedat. 1984. Characteristic folding pattern of polytene chromosomes in Drosophila salivary gland nuclei. Nature. 308:414-421.
45. McCall, K., and W. Bender. 1996. Probes for chromatin accessibility in the Drosophila bithorax complex respond differently to Polycomb-mediated repression. EMBO J. 15:569-580.
46. Messmer, S., A. Franke, and R. Paro. 1992. Analysis of the functional role of the Polycomb chromo domain in Drosophila melanogaster. Genes Dev. 6:1241-1254.
47. Michelotti, E.F., S. Sanford, and D. Levens. 1997. Marking of active genes on mitotic chromosomes. Nature. 388:895-899.
48. Mitchison, T.J., and J.W. Sedat. 1983. Localization of antigenic determinants in whole Drosophila embryos. Dev. Biol. 99:261-264.
49. Moretti, P., K. Freeman, L. Coodly, and D. Shore. 1994. Evidence that a complex of SIR proteins interacts with the silencer and telomere-binding protein RAP1. Genes Dev. 8:2257-2269.
50. Mueller, J., S. Gaunt, and P.A. Lawrence. 1995. Function of the Polycomb protein is conserved in mice and flies. Development. 121:2847-2852.
51. Müller, J. 1995. Transcriptional silencing by the Polycomb protein in Drosophila embryos. EMBO J. 14:1209-1220.
52. O'Brien, T., R.C. Wilkins, C. Giardina, and J.T. Lis. 1995. Distribution of GAGA protein on Drosophila genes in vivo. Genes Dev. 9:1098-1110.
53. Orlando, V., and R. Paro. 1993. Mapping Polycomb-repressed domains in the bithorax complex using in vivo formaldehyde cross-linked chromatin. Cell 75:1187-1198.
54. Orlando, V., and R. Paro. 1995. Chromatin multiprotein complexes involved in the maintenance of transcription patterns. Curr. Opin. Genet. Dev. 5:174-179.
55. Paro, R. 1990. Imprinting a determined state into the chromatin of Drosophila. Trends Genet. 6:416-421.
56. Paro, R. 1993. Mechanisms of heritable gene repression during development of Drosophila. Curr. Opin. Cell Biol. 5:999-1005.
57. Paro, R., and D.S. Hogness. 1991. The polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. Proc. Natl. Acad. Sci. USA. 88:263-267.
58. Paro, R., and B. Zink. 1992. The polycomb gene is differentially regulated during oogenesis and embryogenesis of Drosophila melanogaster. Mech. Dev. 40:37-46.
59. Pearce, J.J., P.B. Singh, and S.J. Gaunt. 1992. The mouse has a polycomb-like chromobox gene. Development. 114:921-929.
60. Petty, K.J. 1987. Metal chelate affinity chromatography. In Current Protocols in Molecular Biology. K. Janssen, editor. John Wiley & Sons, Inc. New York. 10.11.8-10.11.22.
61. Pirrotta, V. 1995. Chromatin complexes regulating gene expression in Drosophila. Curr. Opin. Genet. Dev. 5:466-472.
62. Pirrotta, V., and L. Rastelli. 1994. White gene expression, repressive chromatin domains and homeotic gene regulation in Drosophila. BioEssays. 16:549-556.
63. Rastelli, L., C.S. Chan, and V. Pirrotta. 1993. Related chromosome binding sites for zeste, suppressors of zeste and polycomb group proteins in Drosophila and their dependence on enhancer of zeste function. EMBO J. 12: 1513-1522.
64. Reuter, G., and P. Spierer. 1992. Position effect variegation and chromatin proteins. BioEssays. 14:605-612.
65. Saumweber, H., P. Symmons, R. Kabisch, H. Will, and F. Bonhoeffer. 1980. Monoclonal antibodies against chromosomal proteins of Drosophila melanogaster. Chromosoma. 80:253-275.
66. Schloßherr, J., H. Eggert, R. Paro, S. Cremer, and R.S. Jack. 1994. Gene inactivation in Drosophila mediated by the polycomb gene product or by position-effect variegation does not involve major changes in the accessibility of the chromatin fibre. Mol. Gen. Genet. 243:453-462.
67. Segil, N., M. Guermah, A. Hoffmann, R. Roeder, and N. Heintz. 1996. Mitotic regulation of TFIID: inhibition of activator-dependent transcription and changes in subcellular localization. Genes Dev. 10:2389-2400.
68. Simon, J. 1995. Locking in stable states of gene expression: transcriptional control during Drosophila development. Curr. Opin. Cell Biol. 7:376-385.
69. Simon, J., A. Chiang, and W. Bender. 1992. Ten different Polycomb group genes are required for spatial control of the abdA and AbdB homeotic products. Development. 114:493-505.
70. Strouboulis, J., and A. Wolffe. 1996. Functional compartmentalization of the nucleus, J. Cell Sci. 109:1991-2000.
71. Strutt, H., G. Cavalli, and R. Paro. 1997. Co-localisation of Polycomb protein and GAGA factor on regulatory elements responsible for the maintenance of homeotic gene expression. EMBO J. 16:3621-3632.
72. Studier, F.W., and B.A. Moffatt. 1986. Use of bacteriophage T7 RNA polymerase to direct selective high level expression of cloned genes. J. Mol. Biol. 189:113-130.
73. Tamkun, J. 1995. The role of brahma and related proteins in transcription and development. Curr. Opin. Genet. Dev. 5:473-477.
74. Thompson, J.S., X. Ling, and M. Grunstein. 1994. Histone H3 amino terminus is required for telomeric and silent mating locus repression in yeast. Nature. 369:245-247.
75. van der Lugt, N.M.T., J. Domen, K. Linders, M. van Roon, E. Robanus-Maandag, H. Te Riele, M. van der Valk, J. Deschamps, M. Sofroniew, M. van Lohuizen, and A. Berns. 1994. Posterior transformation, neurological abnormalities, and severe hematopoietic defects in mice with a targeted deletion of the bmi-1 proto-oncogene. Genes Dev. 8:757-769.
76. van der Voort, H., and K. Straster. 1995. Restoration of confocal images for quantitative image analysis. J. Microsc. 178:165-181.
77. van Kempen, G.M.P., L.J. van Vliet, P.J. Verveer, and H.T.M. van der Voort. 1997. A quantitative comparison of image restoration methods for confocal microscopy. J. Microsc. 185:354-365.
78. van Lohuizen, M., M. Frasch, E. Wientjens, and A. Berns. 1991. Sequence similarity between the mammalian bmi-1 proto-oncogene and the Drosophila regulatory genes Psc and Su(z)2. Nature. 353:353-355.
79. Wakimoto, B.T., and M.G. Hearn. 1990. The effects of chromosome rearrangements on the expression of heterochromatic genes in chromosome 2L of Drosophila melanogaster. Genetics. 125:141-154.
80. Wu, C.T., and M. Howe. 1995. A genetic analysis of the suppressor 2 of zeste complex of Drosophila melanogaster. Genetics. 140:139-181.
81. Xing, Y., C. Johnson, P. Moen. J. McNeil, and J.L. Lawrence. 1995. Nonrandom gene organization: structural arrangements of specific pre-mRNA transcription and splicing with SC-35 domains. J. Cell Biol. 131:1635-1647.
82. Zink, B., Y. Engstrom, W.J. Gehring, and R. Paro. 1991. Direct interaction of the polycomb protein with antennapedia regulatory sequences in polytene chromosomes of Drosophila melanogaster. EMBO J. 10:153-162.
83. Zink, B., and R. Paro. 1989. In vivo binding pattern of a trans-regulator of homeotic genes in Drosophila melanogaster. Nature. 337:468-471.