Expression in Aneuploid Drosophila S2 Cells
Extensive departures from balanced gene dose in aneuploids are highly deleterious. However, we know very little about the relationship between gene copy number and expression in aneuploid cells. We determined copy number and transcript abundance (expression) genome-wide in Drosophila S2 cells by DNA...
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| Published in | PLoS biology Vol. 8; no. 2; p. e1000320 |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.02.2010
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1545-7885 1544-9173 1545-7885 |
| DOI | 10.1371/journal.pbio.1000320 |
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| Abstract | Extensive departures from balanced gene dose in aneuploids are highly deleterious. However, we know very little about the relationship between gene copy number and expression in aneuploid cells. We determined copy number and transcript abundance (expression) genome-wide in Drosophila S2 cells by DNA-Seq and RNA-Seq. We found that S2 cells are aneuploid for >43 Mb of the genome, primarily in the range of one to five copies, and show a male genotype ( approximately two X chromosomes and four sets of autosomes, or 2X;4A). Both X chromosomes and autosomes showed expression dosage compensation. X chromosome expression was elevated in a fixed-fold manner regardless of actual gene dose. In engineering terms, the system "anticipates" the perturbation caused by X dose, rather than responding to an error caused by the perturbation. This feed-forward regulation resulted in precise dosage compensation only when X dose was half of the autosome dose. Insufficient compensation occurred at lower X chromosome dose and excessive expression occurred at higher doses. RNAi knockdown of the Male Specific Lethal complex abolished feed-forward regulation. Both autosome and X chromosome genes show Male Specific Lethal-independent compensation that fits a first order dose-response curve. Our data indicate that expression dosage compensation dampens the effect of altered DNA copy number genome-wide. For the X chromosome, compensation includes fixed and dose-dependent components. |
|---|---|
| AbstractList |
Extensive departures from balanced gene dose in aneuploids are highly deleterious. However, we know very little about the relationship between gene copy number and expression in aneuploid cells. We determined copy number and transcript abundance (expression) genome-wide in Drosophila S2 cells by DNA-Seq and RNA-Seq. We found that S2 cells are aneuploid for >43 Mb of the genome, primarily in the range of one to five copies, and show a male genotype (~ two X chromosomes and four sets of autosomes, or 2X;4A). Both X chromosomes and autosomes showed expression dosage compensation. X chromosome expression was elevated in a fixed-fold manner regardless of actual gene dose. In engineering terms, the system "anticipates" the perturbation caused by X dose, rather than responding to an error caused by the perturbation. This feed-forward regulation resulted in precise dosage compensation only when X dose was half of the autosome dose. Insufficient compensation occurred at lower X chromosome dose and excessive expression occurred at higher doses. RNAi knockdown of the Male Specific Lethal complex abolished feed-forward regulation. Both autosome and X chromosome genes show Male Specific Lethal-independent compensation that fits a first order dose-response curve. Our data indicate that expression dosage compensation dampens the effect of altered DNA copy number genome-wide. For the X chromosome, compensation includes fixed and dose-dependent components. Analysis of the relationship between gene copy number and gene expression in aneuploid male Drosophila cells reveals a global compensation mechanism in addition to X chromosome-specific dosage compensation. Extensive departures from balanced gene dose in aneuploids are highly deleterious. However, we know very little about the relationship between gene copy number and expression in aneuploid cells. We determined copy number and transcript abundance (expression) genome-wide in Drosophila S2 cells by DNA-Seq and RNA-Seq. We found that S2 cells are aneuploid for >43 Mb of the genome, primarily in the range of one to five copies, and show a male genotype (∼ two X chromosomes and four sets of autosomes, or 2X;4A). Both X chromosomes and autosomes showed expression dosage compensation. X chromosome expression was elevated in a fixed-fold manner regardless of actual gene dose. In engineering terms, the system “anticipates” the perturbation caused by X dose, rather than responding to an error caused by the perturbation. This feed-forward regulation resulted in precise dosage compensation only when X dose was half of the autosome dose. Insufficient compensation occurred at lower X chromosome dose and excessive expression occurred at higher doses. RNAi knockdown of the Male Specific Lethal complex abolished feed-forward regulation. Both autosome and X chromosome genes show Male Specific Lethal–independent compensation that fits a first order dose-response curve. Our data indicate that expression dosage compensation dampens the effect of altered DNA copy number genome-wide. For the X chromosome, compensation includes fixed and dose-dependent components. While it is widely recognized that mutations in protein coding genes can have harmful consequences, one can also have too much or too little of a good thing. Except for the sex chromosomes, genes come in sets of two in diploid organisms. Extra or missing copies of genes or chromosomes result in an imbalance that can lead to cancers, miscarriages, and disease susceptibility. We have examined what happens to gene expression in Drosophila cells with the types of gross copy number changes that are typical of cancers. We have compared the response of autosomes and sex chromosomes and show that there is some compensation for copy number change in both cases. One response is universal and acts to correct copy number changes by changing transcript abundance. The other is specific to the X chromosome and acts to increase expression regardless of gene dose. Our data highlight how important gene expression balance is for cell function. Extensive departures from balanced gene dose in aneuploids are highly deleterious. However, we know very little about the relationship between gene copy number and expression in aneuploid cells. We determined copy number and transcript abundance (expression) genome-wide in Drosophila S2 cells by DNA-Seq and RNA-Seq. We found that S2 cells are aneuploid for >43 Mb of the genome, primarily in the range of one to five copies, and show a male genotype ( approximately two X chromosomes and four sets of autosomes, or 2X;4A). Both X chromosomes and autosomes showed expression dosage compensation. X chromosome expression was elevated in a fixed-fold manner regardless of actual gene dose. In engineering terms, the system "anticipates" the perturbation caused by X dose, rather than responding to an error caused by the perturbation. This feed-forward regulation resulted in precise dosage compensation only when X dose was half of the autosome dose. Insufficient compensation occurred at lower X chromosome dose and excessive expression occurred at higher doses. RNAi knockdown of the Male Specific Lethal complex abolished feed-forward regulation. Both autosome and X chromosome genes show Male Specific Lethal-independent compensation that fits a first order dose-response curve. Our data indicate that expression dosage compensation dampens the effect of altered DNA copy number genome-wide. For the X chromosome, compensation includes fixed and dose-dependent components.Extensive departures from balanced gene dose in aneuploids are highly deleterious. However, we know very little about the relationship between gene copy number and expression in aneuploid cells. We determined copy number and transcript abundance (expression) genome-wide in Drosophila S2 cells by DNA-Seq and RNA-Seq. We found that S2 cells are aneuploid for >43 Mb of the genome, primarily in the range of one to five copies, and show a male genotype ( approximately two X chromosomes and four sets of autosomes, or 2X;4A). Both X chromosomes and autosomes showed expression dosage compensation. X chromosome expression was elevated in a fixed-fold manner regardless of actual gene dose. In engineering terms, the system "anticipates" the perturbation caused by X dose, rather than responding to an error caused by the perturbation. This feed-forward regulation resulted in precise dosage compensation only when X dose was half of the autosome dose. Insufficient compensation occurred at lower X chromosome dose and excessive expression occurred at higher doses. RNAi knockdown of the Male Specific Lethal complex abolished feed-forward regulation. Both autosome and X chromosome genes show Male Specific Lethal-independent compensation that fits a first order dose-response curve. Our data indicate that expression dosage compensation dampens the effect of altered DNA copy number genome-wide. For the X chromosome, compensation includes fixed and dose-dependent components. Extensive departures from balanced gene dose in aneuploids are highly deleterious. However, we know very little about the relationship between gene copy number and expression in aneuploid cells. We determined copy number and transcript abundance (expression) genome-wide in Drosophila S2 cells by DNA-Seq and RNA-Seq. We found that S2 cells are aneuploid for >43 Mb of the genome, primarily in the range of one to five copies, and show a male genotype (~ two X chromosomes and four sets of autosomes, or 2X;4A). Both X chromosomes and autosomes showed expression dosage compensation. X chromosome expression was elevated in a fixed-fold manner regardless of actual gene dose. In engineering terms, the system "anticipates" the perturbation caused by X dose, rather than responding to an error caused by the perturbation. This feed-forward regulation resulted in precise dosage compensation only when X dose was half of the autosome dose. Insufficient compensation occurred at lower X chromosome dose and excessive expression occurred at higher doses. RNAi knockdown of the Male Specific Lethal complex abolished feed-forward regulation. Both autosome and X chromosome genes show Male Specific Lethal-independent compensation that fits a first order dose-response curve. Our data indicate that expression dosage compensation dampens the effect of altered DNA copy number genome-wide. For the X chromosome, compensation includes fixed and dose-dependent components. Extensive departures from balanced gene dose in aneuploids are highly deleterious. However, we know very little about the relationship between gene copy number and expression in aneuploid cells. We determined copy number and transcript abundance (expression) genome-wide in Drosophila S2 cells by DNA-Seq and RNA-Seq. We found that S2 cells are aneuploid for >43 Mb of the genome, primarily in the range of one to five copies, and show a male genotype ( approximately two X chromosomes and four sets of autosomes, or 2X;4A). Both X chromosomes and autosomes showed expression dosage compensation. X chromosome expression was elevated in a fixed-fold manner regardless of actual gene dose. In engineering terms, the system "anticipates" the perturbation caused by X dose, rather than responding to an error caused by the perturbation. This feed-forward regulation resulted in precise dosage compensation only when X dose was half of the autosome dose. Insufficient compensation occurred at lower X chromosome dose and excessive expression occurred at higher doses. RNAi knockdown of the Male Specific Lethal complex abolished feed-forward regulation. Both autosome and X chromosome genes show Male Specific Lethal-independent compensation that fits a first order dose-response curve. Our data indicate that expression dosage compensation dampens the effect of altered DNA copy number genome-wide. For the X chromosome, compensation includes fixed and dose-dependent components. |
| Audience | Academic |
| Author | Zhang, Yu Malone, John H. Oliver, Brian MacAlpine, David M. Powell, Sara K. Periwal, Vipul Spana, Eric |
| AuthorAffiliation | 2 Department of Pharmacology and Cancer Biology, Duke University Medical Center, Durham, North Carolina, United States of America Adolf Butenandt Institute, Germany 4 Department of Biology, Duke University, Durham, North Carolina, United States of America 3 Laboratory of Biological Modeling, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland, United States of America 1 Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland, United States of America |
| AuthorAffiliation_xml | – name: 3 Laboratory of Biological Modeling, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland, United States of America – name: 4 Department of Biology, Duke University, Durham, North Carolina, United States of America – name: Adolf Butenandt Institute, Germany – name: 2 Department of Pharmacology and Cancer Biology, Duke University Medical Center, Durham, North Carolina, United States of America – name: 1 Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland, United States of America |
| Author_xml | – sequence: 1 givenname: Yu surname: Zhang fullname: Zhang, Yu – sequence: 2 givenname: John H. surname: Malone fullname: Malone, John H. – sequence: 3 givenname: Sara K. surname: Powell fullname: Powell, Sara K. – sequence: 4 givenname: Vipul surname: Periwal fullname: Periwal, Vipul – sequence: 5 givenname: Eric surname: Spana fullname: Spana, Eric – sequence: 6 givenname: David M. surname: MacAlpine fullname: MacAlpine, David M. – sequence: 7 givenname: Brian surname: Oliver fullname: Oliver, Brian |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/20186269$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2010 Public Library of Science This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. 2010 2010 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Citation: Zhang Y, Malone JH, Powell SK, Periwal V, Spana E, et al. (2010) Expression in Aneuploid Drosophila S2 Cells. PLoS Biol 8(2): e1000320. doi:10.1371/journal.pbio.1000320 |
| Copyright_xml | – notice: COPYRIGHT 2010 Public Library of Science – notice: This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. 2010 – notice: 2010 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Citation: Zhang Y, Malone JH, Powell SK, Periwal V, Spana E, et al. (2010) Expression in Aneuploid Drosophila S2 Cells. PLoS Biol 8(2): e1000320. doi:10.1371/journal.pbio.1000320 |
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| Keywords | Cell Line Drosophila Proteins Oligonucleotide Array Sequence Analysis Drosophila Gene Expression Regulation Aneuploidy Male Sequence Analysis, DNA Blotting, Western Dosage Compensation, Genetic Animals Chromatin Immunoprecipitation Comparative Genomic Hybridization RNA Interference X Chromosome |
| Language | English |
| License | This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration, which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. Creative Commons Attribution License |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 The author(s) have made the following declarations about their contributions: Conceived and designed the experiments: YZ SKP ES DMM BO. Performed the experiments: YZ SKP. Analyzed the data: YZ JHM SKP VP DMM BO. Contributed reagents/materials/analysis tools: JHM ES. Wrote the paper: YZ BO. |
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| Snippet | Extensive departures from balanced gene dose in aneuploids are highly deleterious. However, we know very little about the relationship between gene copy number... Analysis of the relationship between gene copy number and gene expression in aneuploid male Drosophila cells reveals a global compensation mechanism in... Extensive departures from balanced gene dose in aneuploids are highly deleterious. However, we know very little about the relationship between gene copy... |
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| SubjectTerms | Aneuploidy Animals Blotting, Western Cell culture Cell Line Chromatin Immunoprecipitation Chromosomes Comparative Genomic Hybridization Compensation Dosage Compensation, Genetic - genetics Drosophila Drosophila - genetics Drosophila - metabolism Drosophila Proteins - genetics Drosophila Proteins - metabolism Dynamic programming Experiments Gene expression Gene Expression Regulation Genetic aspects Genetics Genetics and Genomics/Cancer Genetics Genetics and Genomics/Chromosome Biology Genetics and Genomics/Epigenetics Genetics and Genomics/Functional Genomics Genomes Hypotheses Insects Male Mutation Oligonucleotide Array Sequence Analysis Organisms Risk factors RNA Interference Sequence Analysis, DNA Tumors X Chromosome - genetics |
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| Title | Expression in Aneuploid Drosophila S2 Cells |
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