HP1: a functionally multifaceted protein

Current Opinion in Genetics and Development

Volumn 18, Issue 2, 2008, Pages 169-174

  Fanti, Laura ^a   Pimpinelli, Sergio ^a  

^a Pasteur Institute   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROCHROMATIN PROTEIN 1;

CYTOGENETICS; DROSOPHILA; GENE EXPRESSION; GENE MUTATION; GENE SILENCING; GENETIC TRANSCRIPTION; HETEROCHROMATIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; TELOMERE;

ANIMALS; CHROMOSOMAL PROTEINS, NON-HISTONE; GENE EXPRESSION REGULATION; HETEROCHROMATIN; HUMANS; TELOMERE;

ANIMALIA; DROSOPHILA MELANOGASTER; FUNGI;

EID: 44349122537     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2008.01.009     Document Type: Review

References (42)

1. James T.C., and Elgin S.C.R. Identification of nonhistone chromosomal protein associated with heterochromatin in Drosophila and its gene. Mol Cell Biol 6 (1986) 3862-3872. This paper describes the discovery of HP1 and its gene and represents the starting point of the HP1 saga.
2. James T.C., Eissenberg J.C., Craig C., Dietrich V., Hobson A., and Elgin S.C.R. Distribution patterns of HP1, a heterochromatin-associated nonhistone chromosomal protein of Drosophila. Eur J Cell Biol 50 (1989) 170-180
3. Eissenberg J.C., James T.C., Foster-Hartnett D.M., Hartnett T., Ngan V., and Elgin S.C.R. Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. Proc Natl Acad Sci U S A 87 (1990) 9923-9927
4. Wang G., Ma A., Chow C.M., Horsley D., Brown N.R., Cowell I.G., and Singh P.B. Conservation of heterochromatin protein 1 function. Mol Cell Biol 20 (2000) 6970-6983
5. Lomberk G., Wallrath L., and Urrutia R. The heterochromatin protein 1 family. Genome Biol 7 (2006) 228
6. Paro R., and Hogness D.S. The polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila. Proc Natl Acad Sci U S A 88 (1991) 263-267
7. Aasland R., and Stewart A.F. The chromo shadow domain, a second chromo domain in heterochromatin binding protein 1, HP1. Nucleic Acids Res 23 (1995) 3168-3173
8. Fanti L., Berloco M., Piacentini L., and Pimpinelli S. Chromosomal distribution of heterochromatin protein 1 (HP1) in Drosophila: a cytological map of euchromatic HP1 binding sites. Genetica 117 (2003) 135-147. This paper reports a detailed analysis of HP1 distribution along the euchromatin of a wild-type laboratory strain and four different natural populations of Drosophila melanogaster and other Drosophila species. The results clearly show that the association with multiple specific euchromatic regions, heterochromatin and telomeres is a conserved characteristic of HP1. Intriguingly, the euchromatic HP1 binding sites do not appear to be enriched for known repetitive DNAs.
9. Hiragami K., and Festenstein R. Heterochromatin protein 1: a pervasive controlling influence. Cell Mol Life Sci 62 (2005) 2711-2726
10. Lomberk G., Bensi D., Fernandez-Zapico M.E., and Urrutia R. Evidence for the existence of an HP1-mediated subcode within the histone code. Nat Cell Biol 8 (2006) 407-415. This paper shows that mammalian HP1 isoforms can be extensively modified, similar to histones, suggesting that the silencing of gene expression may be further regulated beyond the histone code by an HP1-mediated 'silencing subcode'.
11. Huisinga K.L., Brower-Toland B., and Elgin S.C. The contradictory definitions of heterochromatin: transcription and silencing. Chromosoma 115 (2006) 110-122
12. Grewal S.I., and Jia S. Heterochromatin revisited. Nat Rev Genet 8 (2007) 35-46
13. Elgin S.C.R., and Reuter G. In: Allis C.D., Jenuwein T., and Reinberg R. (Eds). Epigenetics (2007), Cold Spring Harbor Laboratory Press, Woodbury 81-100
14. Bannister A.J., Zegerman P., Partridge J.F., Miska E.A., Thomas J.O., Allshire R.C., and Kouzarides T. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410 (2001) 120-124
15. Lachner M., O'Carroll D., Rea S., Mechtler K., and Jenuwein T. Methylation histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410 (2001) 116-120
16. Nakayama J., Rice J.C., Strahl B.D., Allis C.D., and Grewal S.I. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292 (2001) 110-113
17. Nielsen A.L., Oulad-Abdelghani M., Ortiz J.A., Remboutsika E., Chambon P., and Losson R. Heterochromatin formation in mammalian cells: interaction between histones and HP1 proteins. Mol Cell 7 (2001) 729-739
18. Schotta G., Ebert A., Krauss V., Fischer A., Hoffmann J., Rea S., et al. Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J 21 (2002) 1121-1131
19. Horn P.J., and Peterson C.L. Heterochromatin assembly: a new twist on an old model. Chromosome Res 14 (2006) 83-94
20. Smallwood A., Estève P.O., Pradhan S., and Carey M. Functional cooperation between HP1 and DNMT1 mediates gene silencing. Genes Dev 21 (2007) 1169-1178. This paper shows that mammalian HP1 family members, by a direct interaction with DNMT1, mediate communication between histone and DNA methyltransferases to repress euchromatic genes.
21. Haynes K.A., Caudy A., Collins L., and Elgin S.C. Element 1360 and RNAi components contribute to HP1-dependent silencing of a pericentric reporter. Curr Biol 16 (2006) 2222-2227
22. Grewal S.I., and Elgin S.C. Transcription and RNA interference in the formation of heterochromatin. Nature 447 (2007) 399-406
23. Bühler M., and Moazed D. Transcription and RNAi in heterochromatic gene silencing. Nat Struct Mol Biol 14 (2007) 1041-1048
24. Fanti L., Giovinazzo G., Berloco M., and Pimpinelli S. The heterochromatin protein 1 prevents telomere fusions in Drosophila. Mol Cell 2 (1998) 527-538. This paper shows, for the first time, that HP1 is necessary for telomere capping in Drosophila.
25. Cowell I.G., Aucott R., Mahadevaiah S.K., Burgoyne P.S., Huskisson N., Bongiorni S., Prantera G., Fanti L., Pimpinelli S., Wu R., et al. Heterochromatin, HP1 and methylation at lysine 9 of histone H3 in animals. Chromosoma 111 (2002) 22-36
26. Perrini B., Piacentini L., Fanti L., Altieri F., Chichiarelli S., Berloco M., Turano C., Ferraro A., and Pimpinelli S. HP1 controls telomere capping, telomere elongation, and telomere silencing by two different mechanisms in Drosophila. Mol Cell 15 (2004) 467-476
27. Savitsky M., Kravchuk O., Melnikova L., and Georgiev P. Heterochromatin protein 1 is involved in control of telomere elongation in Drosophila melanogaster. Mol Cell Biol 22 (2002) 3204-3218
28. Aagaard L., Schmid M., Warburton P., and Jenuwein T. Mitotic phosphorylation of SUV39H1, a novel component of active centromeres, coincides with transient accumulation at mammalian centromeres. J Cell Sci 113 (2000) 817-829
29. Minc E., Allory Y., Worman H.J., Courvalin J.C., and Buendia B. Localization and phosphorylation of HP1 proteins during the cell cycle in mammalian cells. Chromosoma 108 (1999) 220-234
30. Koering C.E., Pollice A., Zibella M.P., Bauwens S., Puisieux A., Brunori M., Brun C., Martins L., Sabatier L., Pulitzer J.F., and Gilson E. Human telomeric position effect is determined by chromosomal context and telomeric chromatin integrity. EMBO Rep 3 (2002) 1055-1061
31. García-Cao M., O'Sullivan R., Peters A.H., Jenuwein T., and Blasco M.A. Epigenetic regulation of telomere length in mammalian cells by the Suv39h1 and Suv39h2 histone methyltransferases. Nat Genet 36 (2004) 94-99
32. Song K., Jung Y., Jung D., and Lee I. Human Ku70 interacts with heterochromatin protein 1alpha. J Biol Chem 276 (2001) 8321-8327
33. Sharma G.G., Hwang K.K., Pandita R.K., Gupta A., Dhar S., Parenteau J., Agarwal M., Worman H.J., Wellinger R.J., and Pandita T.K. Human heterochromatin protein 1 isoforms HP1(Hsalpha) and HP1(Hsbeta) interfere with hTERT-telomere interactions and correlate with changes in cell growth and response to ionizing radiation. Mol Cell Biol 23 (2003) 8363-8376
34. Hwang K.K., Eissenberg J.C., and Worman H.J. Transcriptional repression of euchromatic genes by Drosophila heterochromatin protein 1 and histone modifiers. Proc Natl Acad Sci U S A 98 (2001) 11423-11427
35. Piacentini L., Fanti L., Berloco M., Perrini B., and Pimpinelli S. Heterochromatin protein 1 (HP1) is associated with induced gene expression in Drosophila euchromatin. J Cell Biol 161 (2003) 707-714. This paper shows that HP1 is associated with developmental and heat-shock-induced puffs on Drosophila polytene chromosomes and is positively involved in their activity.
36. Michael A., and Bonner J.J. The induction of gene activity in Drosophila by heat shock. Cell 17 (1979) 241-254
37. Cryderman D.E., Grade S.K., Li Y., Fanti L., Pimpinelli S., and Wallrath L.L. Role of Drosophila HP1 in euchromatic gene expression. Dev Dyn 232 (2005) 767-774. This paper reports a comparation between mRNAs from wild type and Su(var)2-5 mutants lacking HP1. The results show that HP1 regulates several hundred genes throughout the genome and many of them colocalize with HP1 along the chromosomes. A detailed analysis of some HP1-associated genes strongly suggests a positive role for HP1 in euchromatic gene expression.
38. De Lucia F., Ni J.Q., Vaillant C., and Sun F.L. HP1 modulates the transcription of cell-cycle regulators in Drosophila melanogaster. Nucleic Acids Res 33 (2005) 2852-2858
39. de Wit E., Greil F., and van Steensel B. High-resolution mapping reveals links of HP1 with active and inactive chromatin components. PLoS Genet 3 (2007) 0346-0357. This paper reports a high-resolution map of HP1 binding sites on chromosomes 2 and 4 in Drosophila Kc cells. The results show that HP1 forms large domains in pericentric regions but is targeted to single euchromatic genes that are actively transcribed.
40. Johansson A.M., Stenberg P., Pettersson F., and Larsson J. POF and HP1 bind expressed exons, suggesting a balancing mechanism for gene regulation. PLoS Genet 3 (2007) 2235-2246
41. Vakoc C.R., Mandat S.A., Olenchock B.A., and Blobel G.A. Histone H3 lysine 9 methylation and HP1gamma are associated with transcription elongation through mammalian chromatin. Mol Cell 19 (2005) 381-391
42. Brower-Toland B., Findley S.D., Jiang L., Liu L., Yin H., Dus M., Zhou P., Elgin S.C., and Lin H. Drosophila PIWI associates with chromatin and interacts directly with HP1a. Genes Dev 21 (2007) 2300-2311. This paper shows that PIWI, an ARGONAUTE/PIWI protein family member, strongly and specifically interacts with heterochromatin protein 1a (HP1a) and shows an association with polytene chromosomes with a pattern that overlaps with HP1a and appears to be RNA dependent. These findings implicate a direct interaction between the PIWI-mediated small RNA mechanism and heterochromatin-forming pathways in determining the epigenetic state of the fly genome.