Enrichment of HP1a on Drosophila Chromosome 4 Genes Creates an Alternate Chromatin Structure Critical for Regulation in this Heterochromatic Domain
Abstract
Chromatin environments differ greatly within a eukaryotic genome, depending on expression state, chromosomal location, and nuclear position. In genomic regions characterized by high repeat content and high gene density, chromatin structure must silence transposable elements but permit expression of embedded genes. We have investigated one such region, chromosome 4 of Drosophila melanogaster. Using chromatin-immunoprecipitation followed by microarray (ChIP–chip) analysis, we examined enrichment patterns of 20 histone modifications and 25 chromosomal proteins in S2 and BG3 cells, as well as the changes in several marks resulting from mutations in key proteins. Active genes on chromosome 4 are distinct from those in euchromatin or pericentric heterochromatin: while there is a depletion of silencing marks at the transcription start sites (TSSs), HP1a and H3K9me3, but not H3K9me2, are enriched strongly over gene bodies. Intriguingly, genes on chromosome 4 are less frequently associated with paused polymerase. However, when the chromatin is altered by depleting HP1a or POF, the RNA pol II enrichment patterns of many chromosome 4 genes shift, showing a significant decrease over gene bodies but not at TSSs, accompanied by lower expression of those genes. Chromosome 4 genes have a low incidence of TRL/GAGA factor binding sites and a low Tm downstreammore »
- Authors:
-
- Washington Univ., St. Louis, MO (United States). Dept. of Biology
- Harvard Medical School, Boston, MA (United States). Center for Biomedical Informatics
- Harvard Medical School, Boston, MA (United States). Brigham and Women's Hospital. Dept. of Genetics. Dept. of Medicine. Division of Genetics
- Rutgers Univ., Piscataway, NJ (United States). Dept. of Molecular Biology and Biochemistry; Alexandria Univ., Ibrahimia, Alexandria (Egypt). Faculty of Agriculture. Food Science and Technology Dept.
- Rutgers Univ., Piscataway, NJ (United States). Dept. of Molecular Biology and Biochemistry
- Univ. of California, Berkeley, CA (United States). Dept. of Molecular and Cell Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Dept. of Genome Dynamics
- Rutgers Univ., Piscataway, NJ (United States). Dept. of Molecular Biology and Biochemistry; Umea Univ. (Sweden). Dept. of Molecular Biology
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Institutes of Health (NIH)
- OSTI Identifier:
- 1627297
- Grant/Contract Number:
- AC02-05CH11231; R01 GM068388; U01 HG004258; P30 CA91842; UL1RR024992
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Genetics
- Additional Journal Information:
- Journal Volume: 8; Journal Issue: 9; Journal ID: ISSN 1553-7404
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Genetics & Heredity
Citation Formats
Riddle, Nicole C., Jung, Youngsook L., Gu, Tingting, Alekseyenko, Artyom A., Asker, Dalal, Gui, Hongxing, Kharchenko, Peter V., Minoda, Aki, Plachetka, Annette, Schwartz, Yuri B., Tolstorukov, Michael Y., Kuroda, Mitzi I., Pirrotta, Vincenzo, Karpen, Gary H., Park, Peter J., and Elgin, Sarah C. R. Enrichment of HP1a on Drosophila Chromosome 4 Genes Creates an Alternate Chromatin Structure Critical for Regulation in this Heterochromatic Domain. United States: N. p., 2012.
Web. doi:10.1371/journal.pgen.1002954.
Riddle, Nicole C., Jung, Youngsook L., Gu, Tingting, Alekseyenko, Artyom A., Asker, Dalal, Gui, Hongxing, Kharchenko, Peter V., Minoda, Aki, Plachetka, Annette, Schwartz, Yuri B., Tolstorukov, Michael Y., Kuroda, Mitzi I., Pirrotta, Vincenzo, Karpen, Gary H., Park, Peter J., & Elgin, Sarah C. R. Enrichment of HP1a on Drosophila Chromosome 4 Genes Creates an Alternate Chromatin Structure Critical for Regulation in this Heterochromatic Domain. United States. https://doi.org/10.1371/journal.pgen.1002954
Riddle, Nicole C., Jung, Youngsook L., Gu, Tingting, Alekseyenko, Artyom A., Asker, Dalal, Gui, Hongxing, Kharchenko, Peter V., Minoda, Aki, Plachetka, Annette, Schwartz, Yuri B., Tolstorukov, Michael Y., Kuroda, Mitzi I., Pirrotta, Vincenzo, Karpen, Gary H., Park, Peter J., and Elgin, Sarah C. R. Thu .
"Enrichment of HP1a on Drosophila Chromosome 4 Genes Creates an Alternate Chromatin Structure Critical for Regulation in this Heterochromatic Domain". United States. https://doi.org/10.1371/journal.pgen.1002954. https://www.osti.gov/servlets/purl/1627297.
@article{osti_1627297,
title = {Enrichment of HP1a on Drosophila Chromosome 4 Genes Creates an Alternate Chromatin Structure Critical for Regulation in this Heterochromatic Domain},
author = {Riddle, Nicole C. and Jung, Youngsook L. and Gu, Tingting and Alekseyenko, Artyom A. and Asker, Dalal and Gui, Hongxing and Kharchenko, Peter V. and Minoda, Aki and Plachetka, Annette and Schwartz, Yuri B. and Tolstorukov, Michael Y. and Kuroda, Mitzi I. and Pirrotta, Vincenzo and Karpen, Gary H. and Park, Peter J. and Elgin, Sarah C. R.},
abstractNote = {Chromatin environments differ greatly within a eukaryotic genome, depending on expression state, chromosomal location, and nuclear position. In genomic regions characterized by high repeat content and high gene density, chromatin structure must silence transposable elements but permit expression of embedded genes. We have investigated one such region, chromosome 4 of Drosophila melanogaster. Using chromatin-immunoprecipitation followed by microarray (ChIP–chip) analysis, we examined enrichment patterns of 20 histone modifications and 25 chromosomal proteins in S2 and BG3 cells, as well as the changes in several marks resulting from mutations in key proteins. Active genes on chromosome 4 are distinct from those in euchromatin or pericentric heterochromatin: while there is a depletion of silencing marks at the transcription start sites (TSSs), HP1a and H3K9me3, but not H3K9me2, are enriched strongly over gene bodies. Intriguingly, genes on chromosome 4 are less frequently associated with paused polymerase. However, when the chromatin is altered by depleting HP1a or POF, the RNA pol II enrichment patterns of many chromosome 4 genes shift, showing a significant decrease over gene bodies but not at TSSs, accompanied by lower expression of those genes. Chromosome 4 genes have a low incidence of TRL/GAGA factor binding sites and a low Tm downstream of the TSS, characteristics that could contribute to a low incidence of RNA polymerase pausing. Our data also indicate that EGG and POF jointly regulate H3K9 methylation and promote HP1a binding over gene bodies, while HP1a targeting and H3K9 methylation are maintained at the repeats by an independent mechanism. The HP1a-enriched, POF-associated chromatin structure over the gene bodies may represent one type of adaptation for genes embedded in repetitive DNA.},
doi = {10.1371/journal.pgen.1002954},
journal = {PLoS Genetics},
number = 9,
volume = 8,
place = {United States},
year = {Thu Sep 20 00:00:00 EDT 2012},
month = {Thu Sep 20 00:00:00 EDT 2012}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Role of Drosophila HP1 in euchromatic gene expression
journal, March 2005
- Cryderman, Diane E.; Grade, Stephanie K.; Li, Yuhong
- Developmental Dynamics, Vol. 232, Issue 3
In vitro study of the DNA replication patterns of somatic chromosomes of Drosophila melanogaster
journal, August 1966
- Barigozzi, C.; Dolfini, Silvana; Fraccaro, M.
- Experimental Cell Research, Vol. 43, Issue 1
Pol II waiting in the starting gates: Regulating the transition from transcription initiation into productive elongation
journal, January 2011
- Nechaev, Sergei; Adelman, Karen
- Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1809, Issue 1
Stimulating Conversations between HP1a and Histone Demethylase dKDM4A
journal, December 2008
- Wallrath, Lori L.; Elgin, Sarah C. R.
- Molecular Cell, Vol. 32, Issue 5
Regulation of chromatin by histone modifications
journal, February 2011
- Bannister, Andrew J.; Kouzarides, Tony
- Cell Research, Vol. 21, Issue 3
RNA polymerase is poised for activation across the genome
journal, November 2007
- Muse, Ginger W.; Gilchrist, Daniel A.; Nechaev, Sergei
- Nature Genetics, Vol. 39, Issue 12
Lack of evidence for DNA methylation of Invader4 retroelements in Drosophila and implications for Dnmt2-mediated epigenetic regulation
journal, October 2010
- Schaefer, Matthias; Lyko, Frank
- Nature Genetics, Vol. 42, Issue 11
Painting of fourth in genus
Drosophila
suggests autosome-specific gene regulation
journal, June 2004
- Larsson, Jan; Svensson, Malin J.; Stenberg, Per
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 26
Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing
journal, March 2002
- Schotta, G.
- The EMBO Journal, Vol. 21, Issue 5
Heterochromatic silencing of Drosophila heat shock genes acts at the level of promoter potentiation
journal, August 1999
- Cryderman, D. E.; Tang, H.; Bell, C.
- Nucleic Acids Research, Vol. 27, Issue 16
Position effect variegation in Drosophila is associated with an altered chromatin structure.
journal, May 1995
- Wallrath, L. L.; Elgin, S. C.
- Genes & Development, Vol. 9, Issue 10
POF Regulates the Expression of Genes on the Fourth Chromosome in Drosophila melanogaster by Binding to Nascent RNA
journal, June 2012
- Johansson, Anna-Mia; Stenberg, Per; Allgardsson, Anders
- Molecular and Cellular Biology, Vol. 32, Issue 11
cis-Acting Determinants of Heterochromatin Formation on Drosophila melanogaster Chromosome Four
journal, September 2004
- Sun, Fang-Lin; Haynes, Karmella; Simpson, Cory L.
- Molecular and Cellular Biology, Vol. 24, Issue 18
baySeq: Empirical Bayesian methods for identifying differential expression in sequence count data
journal, August 2010
- Hardcastle, Thomas J.; Kelly, Krystyna A.
- BMC Bioinformatics, Vol. 11, Issue 1
Normalization and experimental design for ChIP-chip data
journal, June 2007
- Peng, Shouyong; Alekseyenko, Artyom A.; Larschan, Erica
- BMC Bioinformatics, Vol. 8, Issue 1
Comparison of dot chromosome sequences from D. melanogaster and D. virilisreveals an enrichment of DNA transposon sequences in heterochromatic domains
journal, February 2006
- Slawson, Elizabeth E.; Shaffer, Christopher D.; Malone, Colin D.
- Genome Biology, Vol. 7, Issue 2
Vreteno, a gonad-specific protein, is essential for germline development and primary piRNA biogenesis inDrosophila
journal, September 2011
- Zamparini, Andrea L.; Davis, Marie Y.; Malone, Colin D.
- Development, Vol. 138, Issue 18
POF and HP1 Bind Expressed Exons, Suggesting a Balancing Mechanism for Gene Regulation
journal, January 2005
- Johansson, Anna-Mia; Stenberg, Per; Pettersson, Fredrik
- PLoS Genetics, Vol. preprint, Issue 2007
Buffering of Segmental and Chromosomal Aneuploidies in Drosophila melanogaster
journal, May 2009
- Stenberg, Per; Lundberg, Lina E.; Johansson, Anna-Mia
- PLoS Genetics, Vol. 5, Issue 5
Heterochromatin Protein 1 (HP1a) Positively Regulates Euchromatic Gene Expression through RNA Transcript Association and Interaction with hnRNPs in Drosophila
journal, October 2009
- Piacentini, Lucia; Fanti, Laura; Negri, Rodolfo
- PLoS Genetics, Vol. 5, Issue 10
Global Analysis of the Relationship between JIL-1 Kinase and Transcription
journal, March 2011
- Regnard, Catherine; Straub, Tobias; Mitterweger, Angelika
- PLoS Genetics, Vol. 7, Issue 3
Loss-Of-Function Alleles of the JIL-1 Kinase Are Strong Suppressors of Position Effect Variegation of the wm4 Allele in Drosophila
journal, August 2006
- Lerach, Stephanie; Zhang, Weiguo; Bao, Xiaomin
- Genetics, Vol. 173, Issue 4
Reduced Levels of Su(var)3-9 But Not Su(var)2-5 (HP1) Counteract the Effects on Chromatin Structure and Viability in Loss-of-Function Mutants of the JIL-1 Histone H3S10 Kinase
journal, September 2007
- Deng, Huai; Bao, Xiaomin; Zhang, Weiguo
- Genetics, Vol. 177, Issue 1
Multiple SET Methyltransferases Are Required to Maintain Normal Heterochromatin Domains in the Genome of Drosophila melanogaster
journal, April 2009
- Brower-Toland, Brent; Riddle, Nicole C.; Jiang, Hongmei
- Genetics, Vol. 181, Issue 4
Works referencing / citing this record:
Rapid embryonic cell cycles defer the establishment of heterochromatin by Eggless/SetDB1 in Drosophila
journal, February 2019
- Seller, Charles A.; Cho, Chun-Yi; O'Farrell, Patrick H.
- Genes & Development, Vol. 33, Issue 7-8
A Course-Based Research Experience: How Benefits Change with Increased Investment in Instructional Time
journal, March 2014
- Shaffer, Christopher D.; Alvarez, Consuelo J.; Bednarski, April E.
- CBE—Life Sciences Education, Vol. 13, Issue 1
Dynamic turnover of centromeres drives karyotype evolution in Drosophila
journal, September 2019
- Bracewell, Ryan; Chatla, Kamalakar; Nalley, Matthew J.
- eLife, Vol. 8
Rapid embryonic cell cycles defer the establishment of heterochromatin by Eggless/SetDB1 in Drosophila
posted_content, January 2018
- Seller, Charles A.; Cho, Chun-Yi; O’Farrell, Patrick H.
- Genes & Development
The SUMO ligase Su(var)2-10 controls eu- and heterochromatic gene expression via establishment of H3K9 trimethylation and negative feedback regulation
posted_content, January 2019
- Ninova, Maria; Godneeva, Baira; Ariel Chen, Yung-Chia
- Molecular Cell
Insulator proteins contribute to expression of gene loci repositioned into heterochromatin in the course of Drosophila evolution
posted_content, January 2019
- Funikov, Sergei Yu.; Rezvykh, Alexander P.; Kulikova, Dina A.
- Semantic Scholar
Retrotransposons Are the Major Contributors to the Expansion of the Drosophila ananassae Muller F Element
journal, August 2017
- Leung, Wilson; Shaffer, Christopher D.; Chen, Elizabeth J.
- G3 Genes|Genomes|Genetics, Vol. 7, Issue 8
Islands of retroelements are the major components of Drosophila centromeres
journal, February 2019
- Chang, Ching-Ho; Chavan, Ankita; Palladino, Jason
- PLOS Biology
Establishment and evolution of heterochromatin
journal, February 2020
- Liu, Jing; Ali, Mujahid; Zhou, Qi
- Annals of the New York Academy of Sciences, Vol. 1476, Issue 1
Distinct polymer physics principles govern chromatin dynamics in mouse and Drosophila topological domains
journal, August 2015
- Ea, Vuthy; Sexton, Tom; Gostan, Thierry
- BMC Genomics, Vol. 16, Issue 1
Islands of retroelements are major components of Drosophila centromeres
journal, May 2019
- Chang, Ching-Ho; Chavan, Ankita; Palladino, Jason
- PLOS Biology, Vol. 17, Issue 5
HP1B is a euchromatic Drosophila HP1 homolog with links to metabolism
posted_content, January 2018
- Mills, Benjamin B.; Thomas, Andrew D.; Riddle, Nicole C.
- PLOS ONE
HP1B is a euchromatic Drosophila HP1 homolog with links to metabolism
journal, October 2018
- Mills, Benjamin B.; Thomas, Andrew D.; Riddle, Nicole C.
- PLOS ONE, Vol. 13, Issue 10
HP1a, Su(var)3-9, SETDB1 and POF stimulate or repress gene expression depending on genomic position, gene length and expression pattern in Drosophila melanogaster
journal, March 2013
- Lundberg, Lina E.; Stenberg, Per; Larsson, Jan
- Nucleic Acids Research, Vol. 41, Issue 8
Differentiating Drosophila female germ cells initiate Polycomb silencing by altering PRC2 sampling
posted_content, January 2020
- DeLuca, Steven Z.; Ghildiyal, Megha; Niu, Wanbao
- eLife
Dosage Compensation of X-Linked Muller Element F Genes but Not X-Linked Transgenes in the Australian Sheep Blowfly
journal, October 2015
- Linger, Rebecca J.; Belikoff, Esther J.; Scott, Maxwell J.
- PLOS ONE, Vol. 10, Issue 10
Molecular and genetic organization of bands and interbands in the dot chromosome of Drosophila melanogaster
journal, April 2019
- Sidorenko, Darya S.; Sidorenko, Ivan A.; Zykova, Tatyana Yu.
- Chromosoma, Vol. 128, Issue 2
Differential effect of aneuploidy on the X chromosome and genes with sex-biased expression in Drosophila
journal, September 2013
- Sun, L.; Johnson, A. F.; Li, J.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 41
Molecular and genetic organization of bands and interbands in the dot chromosome of Drosophila melanogaster
journal, April 2019
- Sidorenko, Darya S.; Sidorenko, Ivan A.; Zykova, Tatyana Yu.
- Chromosoma, Vol. 128, Issue 2
Comparative Genomic Analyses Provide New Insights into the Evolutionary Dynamics of Heterochromatin in Drosophila
journal, August 2016
- Caizzi, Ruggiero; Moschetti, Roberta; Piacentini, Lucia
- PLOS Genetics, Vol. 12, Issue 8
Dosage Compensation of X-Linked Muller Element F Genes but Not X-Linked Transgenes in the Australian Sheep Blowfly
journal, October 2015
- Linger, Rebecca J.; Belikoff, Esther J.; Scott, Maxwell J.
- PLOS ONE, Vol. 10, Issue 10
The Drosophila Dot Chromosome: Where Genes Flourish Amidst Repeats
journal, October 2018
- Riddle, Nicole C.; Elgin, Sarah C. R.
- Genetics, Vol. 210, Issue 3