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PMID: 15314179 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Cross-regulation among the polycomb group genes in Drosophila melanogaster.

Molecular and cellular biology ·Vol. 24 ·No. 17 ·2004-09-00 ·Pages 7737-47

Ali JY, Bender W

Abstract

Genes of the Polycomb group in Drosophila melanogaster function as long-term transcriptional repressors. A few members of the group encode proteins found in two evolutionarily conserved chromatin complexes, Polycomb repressive complex 1 (PRC1) and the ESC-E(Z) complex. The majority of the group, lacking clear biochemical functions, might be indirect regulators. The transcript levels of seven Polycomb group genes were assayed in embryos mutant for various other genes in the family. Three Polycomb group genes were identified as upstream positive regulators of the core components of PRC1. There is also negative feedback regulation of some PRC1 core components by other PRC1 genes. Finally, there is positive regulation of PRC1 components by the ESC-E(Z) complex. These multiple pathways of cross-regulation help to explain the large size of the Polycomb group family of genes, but they complicate the genetic analysis of any single member.

MeSH Terms
Animals Drosophila Proteins/genetics,metabolism Drosophila melanogaster/genetics,physiology Embryo, Nonmammalian Gene Expression Regulation Histone-Lysine N-Methyltransferase In Situ Hybridization Multigene Family Mutation Polycomb Repressive Complex 1 Polycomb Repressive Complex 2 Repressor Proteins/genetics,metabolism
Chemicals
Drosophila Proteins Pc protein, Drosophila Repressor Proteins Histone-Lysine N-Methyltransferase Polycomb Repressive Complex 2 esc protein, Drosophila Polycomb Repressive Complex 1
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Ali Janann Y
Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 02115, USA.
Bender Welcome
References (75)
75 references, click to expand
  1. One-to-one correspondence between the two genetic units and the tandemly duplicated transcriptional units of the polyhomeotic locus of Drosophila.
    Mol Gen Genet. 1999 Feb;261(1):196-200 PMID: 10071226
  2. A gene complex controlling segmentation in Drosophila.
    Nature. 1978 Dec 7;276(5688):565-70 PMID: 103000
  3. The Additional sex combs gene of Drosophila is required for activation and repression of homeotic loci, and interacts specifically with Polycomb and super sex combs.
    Mol Gen Genet. 1999 Jun;261(4-5):753-61 PMID: 10394912
  4. Stabilization of chromatin structure by PRC1, a Polycomb complex.
    Cell. 1999 Jul 9;98(1):37-46 PMID: 10412979
  5. GFP-tagged balancer chromosomes for Drosophila melanogaster.
    Mech Dev. 2000 Mar 1;91(1-2):451-4 PMID: 10704882
  6. The domino gene of Drosophila encodes novel members of the SWI2/SNF2 family of DNA-dependent ATPases, which contribute to the silencing of homeotic genes.
    Development. 2001 Apr;128(8):1429-41 PMID: 11262242
  7. Mutations in Drosophila heat shock cognate 4 are enhancers of Polycomb.
    Proc Natl Acad Sci U S A. 2001 Mar 27;98(7):3958-63 PMID: 11274417
  8. Advantages of a P-element construct containing MtnA sequences for the identification of patterning and cell determination genes in Drosophila melanogaster.
    Mol Genet Genomics. 2001 Mar;265(1):14-22 PMID: 11370860
  9. Mechanisms of transcriptional memory.
    Nat Rev Mol Cell Biol. 2001 Jun;2(6):409-21 PMID: 11389465
  10. A Drosophila Polycomb group complex includes Zeste and dTAFII proteins.
    Nature. 2001 Aug 9;412(6847):655-60 PMID: 11493925
  11. Su(z)12, a novel Drosophila Polycomb group gene that is conserved in vertebrates and plants.
    Development. 2001 Sep;128(17):3371-9 PMID: 11546753
  12. Reconstitution of a functional core polycomb repressive complex.
    Mol Cell. 2001 Sep;8(3):545-56 PMID: 11583617
  13. Structure of the HP1 chromodomain bound to histone H3 methylated at lysine 9.
    Nature. 2002 Mar 7;416(6876):103-7 PMID: 11882902
  14. The SAM domain of polyhomeotic forms a helical polymer.
    Nat Struct Biol. 2002 Jun;9(6):453-7 PMID: 11992127
  15. Role of histone H3 lysine 27 methylation in Polycomb-group silencing.
    Science. 2002 Nov 1;298(5595):1039-43 PMID: 12351676
  16. Native and recombinant polycomb group complexes establish a selective block to template accessibility to repress transcription in vitro.
    Mol Cell Biol. 2002 Nov;22(22):7919-28 PMID: 12391159
  17. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites.
    Cell. 2002 Oct 18;111(2):185-96 PMID: 12408863
  18. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex.
    Cell. 2002 Oct 18;111(2):197-208 PMID: 12408864
  19. Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein.
    Genes Dev. 2002 Nov 15;16(22):2893-905 PMID: 12435631
  20. A 1-megadalton ESC/E(Z) complex from Drosophila that contains polycomblike and RPD3.
    Mol Cell Biol. 2003 May;23(9):3352-62 PMID: 12697833
  21. Yeast enhancer of polycomb defines global Esa1-dependent acetylation of chromatin.
    Genes Dev. 2003 Jun 1;17(11):1415-28 PMID: 12782659
  22. The polyhomeotic gene of Drosophila encodes a chromatin protein that shares polytene chromosome-binding sites with Polycomb.
    Genes Dev. 1992 Feb;6(2):223-32 PMID: 1346609
  23. Genetic analysis of the additional sex combs locus of Drosophila melanogaster.
    Genetics. 1992 Apr;130(4):817-25 PMID: 1349871
  24. Identification and characterization of polyhomeotic PREs and TREs.
    Dev Biol. 2003 Sep 15;261(2):426-42 PMID: 14499651
  25. The products of the SPT10 and SPT21 genes of Saccharomyces cerevisiae increase the amplitude of transcriptional regulation at a large number of unlinked loci.
    New Biol. 1991 Dec;3(12):1249-59 PMID: 1667480
  26. Homoeosis in Drosophila: a new enhancer of polycomb and related homoeotic mutations.
    Genetics. 1983 Oct;105(2):357-70 PMID: 17246164
  27. 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):351-3 PMID: 1833647
  28. 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):263-7 PMID: 1898775
  29. Molecular genetics of the Posterior sex combs/Suppressor 2 of zeste region of Drosophila: aberrant expression of the Suppressor 2 of zeste gene results in abnormal bristle development.
    Genetics. 1991 May;128(1):119-32 PMID: 1905661
  30. The complex genetic locus polyhomeotic in Drosophila melanogaster potentially encodes two homologous zinc-finger proteins.
    Gene. 1991 Sep 15;105(2):185-95 PMID: 1937015
  31. Genetic analysis of the enhancer of zeste locus and its role in gene regulation in Drosophila melanogaster.
    Genetics. 1990 Sep;126(1):185-99 PMID: 1977656
  32. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  33. In vivo binding pattern of a trans-regulator of homoeotic genes in Drosophila melanogaster.
    Nature. 1989 Feb 2;337(6206):468-71 PMID: 2563569
  34. Mutations affecting the pattern of the larval cuticle inDrosophila melanogaster : I. Zygotic loci on the second chromosome.
    Wilehm Roux Arch Dev Biol. 1984 Sep;193(5):267-282 PMID: 28305337
  35. A complex genetic locus, polyhomeotic, is required for segmental specification and epidermal development in D. melanogaster.
    Cell. 1987 Dec 4;51(5):829-39 PMID: 2890438
  36. Tissue- and stage-specific control of homeotic and segmentation gene expression in Drosophila embryos by the polyhomeotic gene.
    Development. 1988 Aug;103(4):733-41 PMID: 2907878
  37. Isolation and structural analysis of the extra sex combs gene of Drosophila.
    Cold Spring Harb Symp Quant Biol. 1985;50:127-34 PMID: 3006985
  38. Maternal expression of genes that regulate the bithorax complex of Drosophila melanogaster.
    Dev Biol. 1986 Dec;118(2):442-56 PMID: 3098596
  39. Dosage-dependent modifiers of polycomb and antennapedia mutations in Drosophila.
    Proc Natl Acad Sci U S A. 1988 Nov;85(21):8136-40 PMID: 3141923
  40. Polyhomeotic: a gene of Drosophila melanogaster required for correct expression of segmental identity.
    Mol Gen Genet. 1985;198(2):213-20 PMID: 3920476
  41. Genetic limits of the xanthine dehydrogenase structural element within the rosy locus in Drosophila melanogaster.
    Genetics. 1974 Nov;78(3):869-86 PMID: 4217748
  42. The maternal and zygotic roles of the gene Polycomb in embryonic determination in Drosophila melanogaster.
    Dev Biol. 1983 Dec;100(2):399-411 PMID: 6418587
  43. A gene that regulates the bithorax complex differentially in larval and adult cells of Drosophila.
    Cell. 1984 Jul;37(3):815-23 PMID: 6430566
  44. Different requirements for homeotic genes in the soma and germ line of Drosophila.
    Cell. 1983 Nov;35(1):27-34 PMID: 6627397
  45. Role of the esc+ gene product in ensuring the selective expression of segment-specific homeotic genes in Drosophila.
    J Embryol Exp Morphol. 1983 Aug;76:297-331 PMID: 6631324
  46. Polycomblike: a gene that appears to be required for the normal expression of the bithorax and antennapedia gene complexes of Drosophila melanogaster.
    Genetics. 1982 Sep;102(1):49-70 PMID: 6813190
  47. Early role of the esc+ gene product in the determination of segments in Drosophila.
    Cell. 1982 Nov;31(1):285-92 PMID: 7159925
  48. A gene product required for correct initiation of segmental determination in Drosophila.
    Nature. 1981 Sep 3;293(5827):36-41 PMID: 7266657
  49. Mapping functional domains of the polycomb protein of Drosophila melanogaster.
    Chromosome Res. 1995 Sep;3(6):351-60 PMID: 7551550
  50. The Drosophila extra sex combs protein contains WD motifs essential for its function as a repressor of homeotic genes.
    Mech Dev. 1995 Jul;52(1):77-87 PMID: 7577677
  51. A genetic analysis of the Suppressor 2 of zeste complex of Drosophila melanogaster.
    Genetics. 1995 May;140(1):139-81 PMID: 7635282
  52. Comparison of germline mosaics of genes in the Polycomb group of Drosophila melanogaster.
    Genetics. 1995 May;140(1):231-43 PMID: 7635288
  53. Locking in stable states of gene expression: transcriptional control during Drosophila development.
    Curr Opin Cell Biol. 1995 Jun;7(3):376-85 PMID: 7662368
  54. The Polycomb group gene Posterior Sex Combs encodes a chromosomal protein.
    Development. 1993 Feb;117(2):641-55 PMID: 7687213
  55. Characterization of a region of the X chromosome of Drosophila including multi sex combs (mxc), a Polycomb group gene which also functions as a tumour suppressor.
    Mol Gen Genet. 1995 Feb 6;246(3):282-90 PMID: 7854313
  56. Genetic interactions and dosage effects of Polycomb group genes of Drosophila.
    Mol Gen Genet. 1995 Feb 6;246(3):291-300 PMID: 7854314
  57. Interactions of polyhomeotic with Polycomb group genes of Drosophila melanogaster.
    Genetics. 1994 Dec;138(4):1151-62 PMID: 7896097
  58. Molecular characterisation of the Polycomblike gene of Drosophila melanogaster, a trans-acting negative regulator of homeotic gene expression.
    Development. 1994 Sep;120(9):2629-36 PMID: 7956837
  59. SPT10 and SPT21 are required for transcription of particular histone genes in Saccharomyces cerevisiae.
    Mol Cell Biol. 1994 Aug;14(8):5223-8 PMID: 8035801
  60. polyhomeotic regulatory sequences induce developmental regulator-dependent variegation and targeted P-element insertions in Drosophila.
    Genes Dev. 1993 Aug;7(8):1508-20 PMID: 8101825
  61. Silent domains are assembled continuously from the telomere and are defined by promoter distance and strength, and by SIR3 dosage.
    Genes Dev. 1993 Jul;7(7A):1133-45 PMID: 8319906
  62. 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):1513-22 PMID: 8467801
  63. Regulating the HO endonuclease in yeast.
    Curr Opin Genet Dev. 1993 Apr;3(2):286-94 PMID: 8504254
  64. Regulation of polyhomeotic transcription may involve local changes in chromatin activity in Drosophila.
    Mech Dev. 1995 Aug;52(2-3):343-55 PMID: 8541220
  65. The extra sex combs product contains WD40 repeats and its time of action implies a role distinct from other Polycomb group products.
    Mech Dev. 1995 Oct;53(2):197-208 PMID: 8562422
  66. Vive la différence: males vs females in flies vs worms.
    Annu Rev Genet. 1996;30:637-702 PMID: 8982468
  67. The Drosophila Enhancer of zeste gene encodes a chromosomal protein: examination of wild-type and mutant protein distribution.
    Development. 1996 Dec;122(12):4073-83 PMID: 9012527
  68. The cramped gene of Drosophila is a member of the Polycomb-group, and interacts with mus209, the gene encoding Proliferating Cell Nuclear Antigen.
    Development. 1997 Sep;124(17):3385-94 PMID: 9310333
  69. The polyhomeotic locus of Drosophila melanogaster is transcriptionally and post-transcriptionally regulated during embryogenesis.
    Mech Dev. 1997 Aug;66(1-2):69-81 PMID: 9376325
  70. The Additional sex combs gene of Drosophila encodes a chromatin protein that binds to shared and unique Polycomb group sites on polytene chromosomes.
    Development. 1998 Apr;125(7):1207-16 PMID: 9477319
  71. Polycombing the genome: PcG, trxG, and chromatin silencing.
    Cell. 1998 May 1;93(3):333-6 PMID: 9590168
  72. The Drosophila Polycomb Group proteins ESC and E(Z) bind directly to each other and co-localize at multiple chromosomal sites.
    Development. 1998 Sep;125(17):3483-96 PMID: 9693151
  73. The enhancer of polycomb gene of Drosophila encodes a chromatin protein conserved in yeast and mammals.
    Development. 1998 Oct;125(20):4055-66 PMID: 9735366
  74. Expression and properties of wild-type and mutant forms of the Drosophila sex comb on midleg (SCM) repressor protein.
    Genetics. 1998 Oct;150(2):675-86 PMID: 9755199
  75. dMi-2, a hunchback-interacting protein that functions in polycomb repression.
    Science. 1998 Dec 4;282(5395):1897-900 PMID: 9836641
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
DOI
10.1128/MCB.24.17.7737-7747.2004
Published
2004-09-00
Pages
7737-47
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC507012
Subset
IM
External Links
PubMed source DOI: 10.1128/MCB.24.17.7737-7747.2004 PMC Full Text View journal details
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