Skip to main content
NCBI home page
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1997 Dec;17(12):6773–6783. doi: 10.1128/mcb.17.12.6773

The polycomb group protein complex of Drosophila melanogaster has different compositions at different target genes.

H Strutt 1, R Paro 1
PMCID: PMC232533  PMID: 9372908

Abstract

In Drosophila the Polycomb group genes are required for the long-term maintenance of the repressed state of many developmental regulatory genes. Their gene products are thought to function in a common multimeric complex that associates with Polycomb group response elements (PREs) in target genes and regulates higher-order chromatin structure. We show that the chromodomain of Polycomb is necessary for protein-protein interactions within a Polycomb-Polyhomeotic complex. In addition, Posterior Sex Combs protein coimmunoprecipitates Polycomb and Polyhomeotic, indicating that they are members of a common multimeric protein complex. Immunoprecipitation experiments using in vivo cross-linked chromatin indicate that these three Polycomb group proteins are associated with identical regulatory elements of the selector gene engrailed in tissue culture cells. Polycomb, Polyhomeotic, and Posterior Sex Combs are, however, differentially distributed on regulatory sequences of the engrailed-related gene invected. This suggests that there may be multiple different Polycomb group protein complexes which function at different target sites. Furthermore, Polyhomeotic and Posterior Sex Combs are also associated with expressed genes. Polyhomeotic and Posterior Sex Combs may participate in a more general transcriptional mechanism that causes modulated gene repression, whereas the inclusion of Polycomb protein in the complex at PREs leads to stable silencing.

Full Text

The Full Text of this article is available as a PDF (2.2 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alkema M. J., Bronk M., Verhoeven E., Otte A., van 't Veer L. J., Berns A., van Lohuizen M. Identification of Bmi1-interacting proteins as constituents of a multimeric mammalian polycomb complex. Genes Dev. 1997 Jan 15;11(2):226–240. doi: 10.1101/gad.11.2.226. [DOI] [PubMed] [Google Scholar]
  2. Brunk B. P., Martin E. C., Adler P. N. Drosophila genes Posterior Sex Combs and Suppressor two of zeste encode proteins with homology to the murine bmi-1 oncogene. Nature. 1991 Sep 26;353(6342):351–353. doi: 10.1038/353351a0. [DOI] [PubMed] [Google Scholar]
  3. Bunker C. A., Kingston R. E. Transcriptional repression by Drosophila and mammalian Polycomb group proteins in transfected mammalian cells. Mol Cell Biol. 1994 Mar;14(3):1721–1732. doi: 10.1128/mcb.14.3.1721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Busturia A., Morata G. Ectopic expression of homeotic genes caused by the elimination of the Polycomb gene in Drosophila imaginal epidermis. Development. 1988 Dec;104(4):713–720. doi: 10.1242/dev.104.4.713. [DOI] [PubMed] [Google Scholar]
  5. Carrington E. A., Jones R. S. The Drosophila Enhancer of zeste gene encodes a chromosomal protein: examination of wild-type and mutant protein distribution. Development. 1996 Dec;122(12):4073–4083. doi: 10.1242/dev.122.12.4073. [DOI] [PubMed] [Google Scholar]
  6. Chan C. S., Rastelli L., Pirrotta V. A Polycomb response element in the Ubx gene that determines an epigenetically inherited state of repression. EMBO J. 1994 Jun 1;13(11):2553–2564. doi: 10.1002/j.1460-2075.1994.tb06545.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chang Y. L., King B. O., O'Connor M., Mazo A., Huang D. H. Functional reconstruction of trans regulation of the Ultrabithorax promoter by the products of two antagonistic genes, trithorax and Polycomb. Mol Cell Biol. 1995 Dec;15(12):6601–6612. doi: 10.1128/mcb.15.12.6601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cheng N. N., Sinclair D. A., Campbell R. B., Brock H. W. Interactions of polyhomeotic with Polycomb group genes of Drosophila melanogaster. Genetics. 1994 Dec;138(4):1151–1162. doi: 10.1093/genetics/138.4.1151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chiang A., O'Connor M. B., Paro R., Simon J., Bender W. Discrete Polycomb-binding sites in each parasegmental domain of the bithorax complex. Development. 1995 Jun;121(6):1681–1689. doi: 10.1242/dev.121.6.1681. [DOI] [PubMed] [Google Scholar]
  10. Chinwalla V., Jane E. P., Harte P. J. The Drosophila trithorax protein binds to specific chromosomal sites and is co-localized with Polycomb at many sites. EMBO J. 1995 May 1;14(9):2056–2065. doi: 10.1002/j.1460-2075.1995.tb07197.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Coleman K. G., Poole S. J., Weir M. P., Soeller W. C., Kornberg T. The invected gene of Drosophila: sequence analysis and expression studies reveal a close kinship to the engrailed gene. Genes Dev. 1987 Mar;1(1):19–28. doi: 10.1101/gad.1.1.19. [DOI] [PubMed] [Google Scholar]
  12. DeCamillis M., Cheng N. S., Pierre D., Brock H. W. The polyhomeotic gene of Drosophila encodes a chromatin protein that shares polytene chromosome-binding sites with Polycomb. Genes Dev. 1992 Feb;6(2):223–232. doi: 10.1101/gad.6.2.223. [DOI] [PubMed] [Google Scholar]
  13. Drees B., Ali Z., Soeller W. C., Coleman K. G., Poole S. J., Kornberg T. The transcription unit of the Drosophila engrailed locus: an unusually small portion of a 70,000 bp gene. EMBO J. 1987 Sep;6(9):2803–2809. doi: 10.1002/j.1460-2075.1987.tb02576.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dura J. M., Randsholt N. B., Deatrick J., Erk I., Santamaria P., Freeman J. D., Freeman S. J., Weddell D., Brock H. W. A complex genetic locus, polyhomeotic, is required for segmental specification and epidermal development in D. melanogaster. Cell. 1987 Dec 4;51(5):829–839. doi: 10.1016/0092-8674(87)90106-1. [DOI] [PubMed] [Google Scholar]
  15. Fauvarque M. O., Zuber V., Dura J. M. Regulation of polyhomeotic transcription may involve local changes in chromatin activity in Drosophila. Mech Dev. 1995 Aug;52(2-3):343–355. doi: 10.1016/0925-4773(95)00412-t. [DOI] [PubMed] [Google Scholar]
  16. Franke A., DeCamillis M., Zink D., Cheng N., Brock H. W., Paro R. Polycomb and polyhomeotic are constituents of a multimeric protein complex in chromatin of Drosophila melanogaster. EMBO J. 1992 Aug;11(8):2941–2950. doi: 10.1002/j.1460-2075.1992.tb05364.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Franke A., Messmer S., Paro R. Mapping functional domains of the polycomb protein of Drosophila melanogaster. Chromosome Res. 1995 Sep;3(6):351–360. doi: 10.1007/BF00710016. [DOI] [PubMed] [Google Scholar]
  18. Gunster M. J., Satijn D. P., Hamer K. M., den Blaauwen J. L., de Bruijn D., Alkema M. J., van Lohuizen M., van Driel R., Otte A. P. Identification and characterization of interactions between the vertebrate polycomb-group protein BMI1 and human homologs of polyhomeotic. Mol Cell Biol. 1997 Apr;17(4):2326–2335. doi: 10.1128/mcb.17.4.2326. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gustavson E., Goldsborough A. S., Ali Z., Kornberg T. B. The Drosophila engrailed and invected genes: partners in regulation, expression and function. Genetics. 1996 Mar;142(3):893–906. doi: 10.1093/genetics/142.3.893. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hama C., Ali Z., Kornberg T. B. Region-specific recombination and expression are directed by portions of the Drosophila engrailed promoter. Genes Dev. 1990 Jul;4(7):1079–1093. doi: 10.1101/gad.4.7.1079. [DOI] [PubMed] [Google Scholar]
  21. Hidalgo A. The roles of engrailed. Trends Genet. 1996 Jan;12(1):1–4. doi: 10.1016/0168-9525(96)81373-4. [DOI] [PubMed] [Google Scholar]
  22. Jones B., McGinnis W. The regulation of empty spiracles by Abdominal-B mediates an abdominal segment identity function. Genes Dev. 1993 Feb;7(2):229–240. doi: 10.1101/gad.7.2.229. [DOI] [PubMed] [Google Scholar]
  23. Karch F., Weiffenbach B., Peifer M., Bender W., Duncan I., Celniker S., Crosby M., Lewis E. B. The abdominal region of the bithorax complex. Cell. 1985 Nov;43(1):81–96. doi: 10.1016/0092-8674(85)90014-5. [DOI] [PubMed] [Google Scholar]
  24. Kassis J. A. Spatial and temporal control elements of the Drosophila engrailed gene. Genes Dev. 1990 Mar;4(3):433–443. doi: 10.1101/gad.4.3.433. [DOI] [PubMed] [Google Scholar]
  25. Kassis J. A. Unusual properties of regulatory DNA from the Drosophila engrailed gene: three "pairing-sensitive" sites within a 1.6-kb region. Genetics. 1994 Mar;136(3):1025–1038. doi: 10.1093/genetics/136.3.1025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kassis J. A., VanSickle E. P., Sensabaugh S. M. A fragment of engrailed regulatory DNA can mediate transvection of the white gene in Drosophila. Genetics. 1991 Aug;128(4):751–761. doi: 10.1093/genetics/128.4.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kuner J. M., Nakanishi M., Ali Z., Drees B., Gustavson E., Theis J., Kauvar L., Kornberg T., O'Farrell P. H. Molecular cloning of engrailed: a gene involved in the development of pattern in Drosophila melanogaster. Cell. 1985 Aug;42(1):309–316. doi: 10.1016/s0092-8674(85)80126-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. LaJeunesse D., Shearn A. E(z): a polycomb group gene or a trithorax group gene? Development. 1996 Jul;122(7):2189–2197. doi: 10.1242/dev.122.7.2189. [DOI] [PubMed] [Google Scholar]
  29. Lewis E. B. A gene complex controlling segmentation in Drosophila. Nature. 1978 Dec 7;276(5688):565–570. doi: 10.1038/276565a0. [DOI] [PubMed] [Google Scholar]
  30. Lonie A., D'Andrea R., Paro R., Saint R. Molecular characterisation of the Polycomblike gene of Drosophila melanogaster, a trans-acting negative regulator of homeotic gene expression. Development. 1994 Sep;120(9):2629–2636. doi: 10.1242/dev.120.9.2629. [DOI] [PubMed] [Google Scholar]
  31. Martin C. H., Mayeda C. A., Davis C. A., Ericsson C. L., Knafels J. D., Mathog D. R., Celniker S. E., Lewis E. B., Palazzolo M. J. Complete sequence of the bithorax complex of Drosophila. Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8398–8402. doi: 10.1073/pnas.92.18.8398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Martin E. C., Adler P. N. The Polycomb group gene Posterior Sex Combs encodes a chromosomal protein. Development. 1993 Feb;117(2):641–655. doi: 10.1242/dev.117.2.641. [DOI] [PubMed] [Google Scholar]
  33. Messmer S., Franke A., Paro R. Analysis of the functional role of the Polycomb chromo domain in Drosophila melanogaster. Genes Dev. 1992 Jul;6(7):1241–1254. doi: 10.1101/gad.6.7.1241. [DOI] [PubMed] [Google Scholar]
  34. Moazed D., O'Farrell P. H. Maintenance of the engrailed expression pattern by Polycomb group genes in Drosophila. Development. 1992 Nov;116(3):805–810. doi: 10.1242/dev.116.3.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Müller J. Transcriptional silencing by the Polycomb protein in Drosophila embryos. EMBO J. 1995 Mar 15;14(6):1209–1220. doi: 10.1002/j.1460-2075.1995.tb07104.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Orlando V., Paro R. Mapping Polycomb-repressed domains in the bithorax complex using in vivo formaldehyde cross-linked chromatin. Cell. 1993 Dec 17;75(6):1187–1198. doi: 10.1016/0092-8674(93)90328-n. [DOI] [PubMed] [Google Scholar]
  37. Paro R., Hogness D. S. The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):263–267. doi: 10.1073/pnas.88.1.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Paro R. Imprinting a determined state into the chromatin of Drosophila. Trends Genet. 1990 Dec;6(12):416–421. doi: 10.1016/0168-9525(90)90303-n. [DOI] [PubMed] [Google Scholar]
  39. Paro R. Mechanisms of heritable gene repression during development of Drosophila. Curr Opin Cell Biol. 1993 Dec;5(6):999–1005. doi: 10.1016/0955-0674(93)90084-4. [DOI] [PubMed] [Google Scholar]
  40. Pearce J. J., Singh P. B., Gaunt S. J. The mouse has a Polycomb-like chromobox gene. Development. 1992 Apr;114(4):921–929. doi: 10.1242/dev.114.4.921. [DOI] [PubMed] [Google Scholar]
  41. Pelegri F., Lehmann R. A role of polycomb group genes in the regulation of gap gene expression in Drosophila. Genetics. 1994 Apr;136(4):1341–1353. doi: 10.1093/genetics/136.4.1341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Pirrotta V., Rastelli L. White gene expression, repressive chromatin domains and homeotic gene regulation in Drosophila. Bioessays. 1994 Aug;16(8):549–556. doi: 10.1002/bies.950160808. [DOI] [PubMed] [Google Scholar]
  43. Platero J. S., Hartnett T., Eissenberg J. C. Functional analysis of the chromo domain of HP1. EMBO J. 1995 Aug 15;14(16):3977–3986. doi: 10.1002/j.1460-2075.1995.tb00069.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Platero J. S., Sharp E. J., Adler P. N., Eissenberg J. C. In vivo assay for protein-protein interactions using Drosophila chromosomes. Chromosoma. 1996 Mar;104(6):393–404. doi: 10.1007/BF00352263. [DOI] [PubMed] [Google Scholar]
  45. Poole S. J., Kauvar L. M., Drees B., Kornberg T. The engrailed locus of Drosophila: structural analysis of an embryonic transcript. Cell. 1985 Jan;40(1):37–43. doi: 10.1016/0092-8674(85)90306-x. [DOI] [PubMed] [Google Scholar]
  46. Rastelli L., Chan C. S., Pirrotta V. 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. 1993 Apr;12(4):1513–1522. doi: 10.1002/j.1460-2075.1993.tb05795.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Reijnen M. J., Hamer K. M., den Blaauwen J. L., Lambrechts C., Schoneveld I., van Driel R., Otte A. P. Polycomb and bmi-1 homologs are expressed in overlapping patterns in Xenopus embryos and are able to interact with each other. Mech Dev. 1995 Sep;53(1):35–46. doi: 10.1016/0925-4773(95)00422-x. [DOI] [PubMed] [Google Scholar]
  48. Reuter G., Spierer P. Position effect variegation and chromatin proteins. Bioessays. 1992 Sep;14(9):605–612. doi: 10.1002/bies.950140907. [DOI] [PubMed] [Google Scholar]
  49. Simon J., Chiang A., Bender W., Shimell M. J., O'Connor M. Elements of the Drosophila bithorax complex that mediate repression by Polycomb group products. Dev Biol. 1993 Jul;158(1):131–144. doi: 10.1006/dbio.1993.1174. [DOI] [PubMed] [Google Scholar]
  50. Smouse D., Goodman C., Mahowald A., Perrimon N. polyhomeotic: a gene required for the embryonic development of axon pathways in the central nervous system of Drosophila. Genes Dev. 1988 Jul;2(7):830–842. doi: 10.1101/gad.2.7.830. [DOI] [PubMed] [Google Scholar]
  51. Strutt H., Cavalli G., Paro R. Co-localization of Polycomb protein and GAGA factor on regulatory elements responsible for the maintenance of homeotic gene expression. EMBO J. 1997 Jun 16;16(12):3621–3632. doi: 10.1093/emboj/16.12.3621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Studier F. W., Moffatt B. A. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol. 1986 May 5;189(1):113–130. doi: 10.1016/0022-2836(86)90385-2. [DOI] [PubMed] [Google Scholar]
  53. Tabata T., Schwartz C., Gustavson E., Ali Z., Kornberg T. B. Creating a Drosophila wing de novo, the role of engrailed, and the compartment border hypothesis. Development. 1995 Oct;121(10):3359–3369. doi: 10.1242/dev.121.10.3359. [DOI] [PubMed] [Google Scholar]
  54. Wedeen C., Harding K., Levine M. Spatial regulation of Antennapedia and bithorax gene expression by the Polycomb locus in Drosophila. Cell. 1986 Mar 14;44(5):739–748. doi: 10.1016/0092-8674(86)90840-8. [DOI] [PubMed] [Google Scholar]
  55. Zavortink M., Sakonju S. The morphogenetic and regulatory functions of the Drosophila Abdominal-B gene are encoded in overlapping RNAs transcribed from separate promoters. Genes Dev. 1989 Dec;3(12A):1969–1981. doi: 10.1101/gad.3.12a.1969. [DOI] [PubMed] [Google Scholar]
  56. Zink B., Paro R. In vivo binding pattern of a trans-regulator of homoeotic genes in Drosophila melanogaster. Nature. 1989 Feb 2;337(6206):468–471. doi: 10.1038/337468a0. [DOI] [PubMed] [Google Scholar]
  57. van Lohuizen M., Frasch M., Wientjens E., Berns A. Sequence similarity between the mammalian bmi-1 proto-oncogene and the Drosophila regulatory genes Psc and Su(z)2. Nature. 1991 Sep 26;353(6342):353–355. doi: 10.1038/353353a0. [DOI] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES