Genetica

, Volume 117, Issue 2–3, pp 135–147

Chromosomal Distribution of Heterochromatin Protein 1 (HP1) in Drosophila: a Cytological Map of Euchromatic HP1 Binding Sites

  • Laura Fanti
  • Maria Berloco
  • Lucia Piacentini
  • Sergio Pimpinelli
Article

Abstract

The Heterochromatin Protein 1 (HP1) is a conserved protein which is best known for its strong association with the heterochromatin of Drosophila melanogaster. We previously demonstrated that another important property of HP1 is its localization to the telomeres of Drosophila, a feature that reflects its critical function as a telomere capping protein. Here we report our analysis of the euchromatic sites to which HP1 localizes. Using an anti-HP1 antibody, we compared immunostaining patterns on polytene chromosomes of the Ore-R wild type laboratory strain and four different natural populations. HP1 was found to accumulate at specific euchromatic sites, with a subset of the sites conserved among strains. These sites do not appear to be defined by an enrichment of known repetitive DNAs. Comparisons of HP1 patterns among several Drosophila species revealed that association with specific euchromatic regions, heterochromatin and telomeres is a conserved characteristic of HP1. Based on these results, we argue that HP1 serves a broader function than typically postulated. In addition to its role in heterochromatin assembly and telomere stability, we propose that HP1 plays an important role in regulating the expression of many different euchromatic regions.

Drosophila euchromatin HP1 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aasland, R. & A.F. Stewart, 1995. The chromo shadow domain, a second chromo domain in heterochromatin-binding protein 1, HP1. Nucl. Acid. Res. 23: 3168-3173.Google Scholar
  2. Bannister, A.J., P. Zegerman, J.F. Partridge, E.A. Miska, J.O. Thomas, R.C. Allshire & T. Kouzarides, 2001. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromodomain. Nature 410: 120–124.Google Scholar
  3. Delattre, M., A. Spierer, C.H. Tonka & P. Spierer, 2000. The genomic silencing of position-effect variegation in Drosophila melanogaster: interaction between the heterochromatinassociated proteins Su(var)3-7 and HP1. J. Cell Sci. 23: 4253-4261.Google Scholar
  4. Eissenberg, J.C. & T. Hartnett, 1993. A heat shock-activated cDNA rescues the recessive lethality of mutations in the heterochromatin-associated protein HP1 of Drosophila melanogaster. Mol. Gen. Genet. 240: 333–338.Google Scholar
  5. Eissenberg, J.C., T.C. James, D.M. Foster-Hartnett, T. Hartnett, V. Ngan & 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.Google Scholar
  6. Elgin, S.C.R., 1996. Heterochromatin and gene regulation in Drosophila. Curr. Opin. Genet. Dev. 6: 193–202.Google Scholar
  7. Fanti, L., D.R. Dorer, M. Berloco, S. Henikoff & S. Pimpinelli, 1998a. Heterochromatin Protein 1 binds transgene arrays. Chromosoma 107: 286–292.Google Scholar
  8. Fanti, L., G. Giovinazzo, M. Berloco & S. Pimpinelli, 1998b. The Heterochromatin Protein 1 (HP1) prevents telomere fusions in Drosophila melanogaster. Mol. Cell. 2: 1–20.Google Scholar
  9. Furuta, K., E.K.L. Chan, K. Kiyosawa, G. Reimer, C. Luderschmidt & E.M. Tan, 1997. Heterochromatin protein HP1Hsβ (p25β) and its localization with centromeres in mitosis. Chromosoma 106: 11–19.Google Scholar
  10. Horsley, D., A. Hutchings, G.W. Butcher & P.B. Singh, 1996. M32, a murine homologue of Drosophila Heterochromatin Protein 1 (HP1), localises to euchromatin within interphase nuclei and is largely excluded from constitutive heterochromatin. Cytogenet. Cell Genet. 73: 308–311.Google Scholar
  11. Huang, D.W., L. Fanti, D.T. Pak, M.R. Botchan, S. Pimpinelli & R. Kellum, 1998. Distinct cytoplasmic and nuclear fractions of Drosophila Heterochromatin Protein 1: their phosphorylation levels and associations with origin recognition complex proteins. J. Cell Biol. 142: 307–318.Google Scholar
  12. Hwang, K.K., J.C. Eissenberg & H.J. Worman, 2001. Transcriptional repression of euchromatic genes by Drosophila Heterochromatin Protein 1 and histone modifiers. Proc. Natl. Acad. Sci. USA 98: 11423–11427.Google Scholar
  13. James, T.C.& S.C.R. Elgin, 1986. Identification of nonhistone chromosomal protein associated with heterochromatin in Drosophila and its gene. Mol. Cell. Biol. 6: 3862-3872.Google Scholar
  14. James, T.C., J.C. Eissenberg, C. Craig, V. Dietrich, A. Hobson & S.C.R. Elgin, 1989. Distribution patterns of HP1, a hetero-chromatin-associated nonhistone chromosomal protein of Drosophila. Eur. J. Cell Biol. 50: 170–180.Google Scholar
  15. Jones, D.O., I.G. Cowell & P. Singh, 2000. Mammalian chromodomain proteins: their role in genome organisation and expression. Bioessays 22: 124–137.Google Scholar
  16. Kaufmann, B.P., 1939. Distribution of induced breaks along the X chromosome of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 25: 571–577.Google Scholar
  17. Lachner, M., D. O'Carroll, S. Rea, K. Mechtler & T. Jenuwein, 2001. Methylation of histone H3 Lysine9 creates a binding site for HP1 proteins. Nature 410: 116–120.Google Scholar
  18. Miklos, G.L. & J.N. Cotsell, 1990. Chromosome structure at interfaces between major chromatin types: alpha-and betaheterochromatin. Bioessays 12: 1–6.Google Scholar
  19. Miklos, G.L., M. Yamamoto, J. Davis & V. Pirrotta, 1988. Microcloning reveals a high frequency of repetitive sequences characteristic of chromosome 4 and the β-heterochromatin of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 85: 2051-2055.Google Scholar
  20. Minc, E., J.C. Courvalin & B. Buendia, 2000. HP1 gamma associates with euchromatin and heterochromatin in mammalian nuclei and chromosomes. Cytogenet. Cell Genet. 90: 279–284.Google Scholar
  21. Minc, E., Y. Allory, H.J. Worman, J.C. Courvalin & B. Buendia, 1999. Localization and phosphorylation of HP1 proteins during the cell cycle in mammalian cells. Chromosoma 108: 220–234.Google Scholar
  22. Minc, E., Y. Allory, J.C. Courvalin & B. Buendia, 2001. Immunolocalization of HP1 proteins in metaphasic mammalian chromosomes. Meth Cell Sci. 23: 173–176.Google Scholar
  23. Nielsen, S.J., R. Schneider, U.M. Bauer, A.J. Bannister, A. Morrison, D. O'Carroll, R. Firestein, M. Cleary, T. Jenuwein, R.E. Herrera & T. Kouzarides, 2001. Rb targets histone H3 methylation and HP1 to promoters. Nature 412: 561–565.Google Scholar
  24. Pak, D.T.S., M. Pflumm, I. Chesnokov, D.W. Huang, R. Kellum, J. Marr, P. Romanowski & M.R. Botchan, 1997. Association of the origin recognition complex with heterochromatin and HP1 in higher eukaryotes. Cell 91: 311–323.Google Scholar
  25. Paro, R. & 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.Google Scholar
  26. Pimpinelli, S., M. Berloco, L. Fanti, P. Dimitri, S. Bonaccorsi, E. Marchetti, R. Caizzi, C. Caggese & M. Gatti, 1995. Transposable elements are stable structural components of Drosophila melanogaster heterochromatin. Proc. Natl. Acad. Sci. USA 92: 3804-3808.Google Scholar
  27. Pimpinelli, S., S. Bonaccorsi, L. Fanti & M. Gatti, 2000. Preparation and analysis of mitotic chromosomes of Drosophila melanogaster, pp. 1-24 in Drosophila: A Laboratory Manual, edited by W. Sullivan, M. Ashburner & S. Hawley. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.Google Scholar
  28. Scholzen, T., E. Endl, C. Wohlenberg, S. van Der Sar, I.G. Cowell, J. Gerdes & P.B. Singh, 2002. The Ki-67 protein interacts with members of the Heterochromatin Protein 1 (HP1) family: a potential role in the regulation of higher-order chromatin structure. J. Pathol. 196: 135–144.Google Scholar
  29. Singh, P.B., J.R. Miller, J. Pearce, R. Kothary, R.D. Burton, R. Paro, T.C. James & S.J. Gaunt, 1991. A sequence motif found in a Drosophila heterochromatin protein is conserved in animal and plants. Nucl. Acid. Res. 19: 789–794.Google Scholar
  30. Smothers, J.F. & S. Henikoff, 2001. The hinge and chromo shadow domain impart distinct targeting of HP1-like proteins. Mol. Cell Biol. 21: 2555-2569.Google Scholar
  31. Song, K., Y. Jung, D. Jung & I. Lee, 2001. Human Ku70 interacts with Heterochromatin Protein 1 alpha. J. Biol. Chem. 276: 8321-8327.Google Scholar
  32. Vaury, C., A. Bucheton & A. Pelisson, 1989. The beta heterochromatic sequences flanking the I elements are themselves defective transposable elements. Chromosoma 98: 215–224.Google Scholar
  33. Wreggett, K.A., F. Hill, P.S. James, A. Hutchings, G.W. Butcher & P.B. Singh, 1994. A mammalian homologue of Drosophila Heterochromatin Protein 1 (HP1) is a component of constitutive heterochromatin. Cytogenet. Cell Genet. 66: 99–103.Google Scholar
  34. Zhimulev, I.F., V.F. Semeshin, V.A. Kulichkov & E.S. Belyaeva, 1982. Intercalary heterochromatin in Drosophila. I. Localization and general characteristics. Chromosoma 87: 197–228.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Laura Fanti
    • 1
  • Maria Berloco
    • 2
  • Lucia Piacentini
    • 1
  • Sergio Pimpinelli
    • 1
  1. 1.Dipartimento di Genetica e Biologia Molecolare, Istituto Pasteur, Fondazione Cenci BolognettiUniversità 'La Sapienza’RomaItaly
  2. 2.Dipartimento di Anatomia Patologica e di Genetica (DAPEG)Università di BariBariItaly

Personalised recommendations