Eur. J. Entomol. 102 (4): 625-632, 2005
Conservation of HP1 and methylated H3 histones as heterochromatic epigenetic markers in the holocentric chromosomes of the cabbage moth, Mamestra brassicae (Lepidoptera)
- Dipartimento di Biologia Animale, UniversitL di Modena e Reggio Emilia, Via Campi 213/d, 41100 Modena, Italy;
The methylated H3 histone and heterochromatin protein 1 (HP1) are markers of heterochromatin in several eukaryotes possessing monocentric chromosomes. In order to confirm that these epigenetic markers of heterochromatin are evolutionary conserved, the distribution of methylated H3 histones and HP1 homologues on the holocentric chromosomes of the cabbage moth Mamestra brassicae (Lepidoptera) were studied. In particular, PCR experiments with degenerated primers identified a HP1 homologue (called MbHP1) in the M. brassicae genome. Sequencing showed that the MbHP1 gene is 737 bp long including a 102 bp 5'UTR and a 635 bp coding portion (comprising an 80 bp intron). The MbHP1 peptide consisted of 184 amino acids, had a 20 kDa molecular mass and a net negative charge. At the structural level, it showed an N terminal chromo-domain and a chromo-shadow-domain at the C terminus linked by a short hinge region. At the cytogenetic level, MbHP1 was located exclusively in the heterochromatic regions of the chromosomes. The same heterochromatic regions became labelled after immuno-staining with antibodies against H3 histone methylated at lysine 9, reinforcing the hypothesis that this modified histone is essential for HP1 binding. Our data, as a whole, confirm that heterochromatic components and markers are evolutionary conserved both in mono- and holocentric chromosomes despite the difference in the distribution of heterochromatin on chromosomes.
Keywords: Holocentric chromosomes, heterochromatin, HP1, histone H3 methylation, cabbage moth, Lepidoptera, Mamestra brassicae
Received: January 11, 2005; Revised: March 17, 2005; Accepted: March 17, 2005; Published: November 3, 2005 Show citation
| ACS | AIP | APA | ASA | Harvard | Chicago | Chicago Notes | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
References
- BLOM N., GAMMELTOFT S. & BRUNAK S. 1999: Sequence- and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294: 1351-1362
Go to original source... - BONGIORNI S., MAZZUOLI M., MASCI S. & PRANTERA G. 2001: Facultative heterochromatization in parahaploid male mealybugs: involvement of a heterochromatin-associated protein. Development 128: 3809-3817
Go to original source... - BORSATTI F., AZZONI P. & MANDRIOLI M. 2004: Identification of a new hobo element in the cabbage moth, Mamestra brassicae (Lepidoptera). Hereditas 139: 151-155
Go to original source... - COWELL I.G., AUCOTT R., MAHADEVAIAH S.K., BURGOYNE P.S., HUSKISSON N., BONGIORNI S., PRANTERA G., FANTI L., PIMPINELLI S., WU R., GILBERT D.M., SHI W., FUNDELE R., MORRISON H., JEPPESEN P. & SINGH P.B. 2002: Heterochromatin, HP1 and methylation at lysine 9 of histone H3 in animals. Chromosoma 111: 22-36
Go to original source... - DONLON T.A. & MAGENIS R.E. 1983: Methyl-green is a substitute for distamycin A in the formation of distamycin A/DAPI C-bands. Hum. Genet. 65: 144-146
Go to original source... - EISSENBERG J.C. & ELGIN S.C.R. 2000: The HP1 protein family: getting a grip on chromatin. Curr. Opin. Genet. Dev. 10: 204-210
Go to original source... - EISSENBERG J.C., GE Y.W. & HARTNETT T. 1994: Increased phosphorylation of HP1, a heterochromatin-associated protein of Drosophila, is correlated with heterochromatin assembly. J. Biol. Chem. 269: 21315-21321
Go to original source... - EPSTEIN H., JAMES T.C. & SINGH P.B. 1992: Cloning and expression of Drosophila HP1 homologues form a mealybug, Planococcus citri. J. Cell Sci. 101: 463-474
Go to original source... - FROHMAN M.A. 1990: RACE: Rapid amplification of cDNA ends. In Innis D.A., Gelfand D.H. & Snisky J.J. (eds): PCR Protocols. Academic Press, San Diego, pp. 28-38
Go to original source... - HUANG D.W., FANTI L., PAK D.T.S., BOTCHAN M.R., PIMPINELLI S. & KELLUM R. 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
Go to original source... - JAMES T.C. & ELGIN S.C.R. 1986: Identification of non-histone chromosomal protein associated with heterochromatin in Drosophila and its gene. Mol. Cell. Biol. 6: 3862-3872
Go to original source... - JONES D.O., COWELL I.G. & SINGH P.B. 2000: Mammalian chromo domain proteins: their role in genome organization and expression. Bioessays 22: 124-137
Go to original source... - JENUWEIN T. & ALLIS C.D. 2001: Translating the histone code. Science 293: 1074-1080
Go to original source... - KELLUM R. 2003: HP1 complexes and heterochromatin assembly. Curr. Top. Microbiol. Immunol. 274: 53-77
Go to original source... - KOIKE N., MAITA H., TAIRA T., ARIGA H. & IGUCHI-ARIGA S.M. 2000: Identification of heterochromatin protein 1 (HP1) as a phosphorylation target by Pim-1 kinase and the effect of phosphorylation on the transcriptional repression function of HP1. FEBS Lett. 467: 17-21
Go to original source... - LACHNER M., O'CARROLL D., REA S., MECHTLER K. & JENUWEIN T. 2001: Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410: 116-120
Go to original source... - MANDRIOLI M. 2002: Cytogenetic characterization of telomeres in the holocentric chromosomes of the lepidopteran Mamestra brassicae. Chromosome Res. 9: 279-286
Go to original source... - MANDRIOLI M. 2003a: Identification and chromosomal localization of mariner-like elements in the cabbage moth Mamestra brassicae (Lepidoptera). Chromosome Res. 11: 319-322
Go to original source... - MANDRIOLI M. 2003b: Identification and molecular characterization of R1 transposable elements in the cabbage moth Mamestra brassicae. Caryologia 56: 155-160
Go to original source... - MANDRIOLI M., BIZZARO D., GIUSTI M., GIONGHI D., MANICARDI G.C. & BIANCHI U. 1999: Cytogenetic and molecular characterization of a highly repeated DNA sequence in the peach potato aphid Myzus persicae. Chromosoma 108: 436-442
Go to original source... - MANDRIOLI M., MANICARDI G.C. & MAREC F. 2003: Cytogenetic and molecular characterization of the MBSAT1 satellite DNA in holokinetic chromosomes of the cabbage moth, Mamestra brassicae (Lepidoptera). Chromosome Res. 11: 51-56
Go to original source... - NAKAYAMA J., RICE J.C., STRAHL B.D., ALLIS C.D. & GREWAL S.I. 2001: Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 292: 110-113
Go to original source... - OHBAYASHI F., SHIMADA T., SUGASAKI T., KAWAI S., MITA K., OSHIKI T. & ABE H. 1998: Molecular structure of the copialike retrotransposable element Yokozuna on the W chromosome of the silkworm, Bombyx mori. Genes Genet. Syst. 73: 345-352
Go to original source... - REA S., EISENHABER F., O'CARROLL D., STRAHL B.D., SUN Z.W., SCHMID M., OPRAVIL S., MECHTLER K., PONTING C.P., ALLIS C.D. & JENUWEIN T. 2000: Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406: 593-599
Go to original source... - SAMBROOK J., FRITSCH E.F. & MANIATIS T. 1989: Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA
- STRAHL B.D. & ALLIS C.D. 2000: The language of covalent histone modifications. Nature 403: 41-45
Go to original source... - SUMNER A.T. 1972: A simple technique for demonstrating centromeric heterochromatin. Exp. Cell. Res. 75: 304-306
Go to original source... - TURNER B.M. 2000: Histone acetylation and an epigenetic code. Bioessays 22: 836-845
Go to original source... - WANG G., MA A., CHOW C.M., HORSLEY D., BROWN N.R., COWELL I.G. & SINGH P.B. 2000: Conservation of heterochromatin protein 1 function. Mol. Cell. Biol. 20: 6970-6983
Go to original source... - ZHANG Y. & REINBERG D. 2001: Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev. 15: 2343-2360
Go to original source... - ZHAO T., HEYDUK T. & EISSENBERG J.C. 2000: Phosphorylation site mutations in heterochromatin protein 1 (HP1) reduce or eliminate silencing activity. J. Biol. Chem. 276: 9512-9518
Go to original source...
This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.




