DNA copy number evolution in Drosophila cell lines
Background Structural rearrangements of the genome resulting in genic imbalance due to copy number change are often deleterious at the organismal level, but are common in immortalized cell lines and tumors, where they may be an advantage to cells. In order to explore the biological consequences of c...
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| Published in | Genome biology Vol. 15; no. 8; p. R70 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
BioMed Central
28.08.2014
|
| Subjects | |
| Online Access | Get full text |
| ISSN | 1474-760X 1465-6906 1474-760X 1465-6914 |
| DOI | 10.1186/gb-2014-15-8-r70 |
Cover
| Abstract | Background
Structural rearrangements of the genome resulting in genic imbalance due to copy number change are often deleterious at the organismal level, but are common in immortalized cell lines and tumors, where they may be an advantage to cells. In order to explore the biological consequences of copy number changes in the
Drosophila
genome, we resequenced the genomes of 19 tissue-culture cell lines and generated RNA-Seq profiles.
Results
Our work revealed dramatic duplications and deletions in all cell lines. We found three lines of evidence indicating that copy number changes were due to selection during tissue culture. First, we found that copy numbers correlated to maintain stoichiometric balance in protein complexes and biochemical pathways, consistent with the gene balance hypothesis. Second, while most copy number changes were cell line-specific, we identified some copy number changes shared by many of the independent cell lines. These included dramatic recurrence of increased copy number of the PDGF/VEGF receptor, which is also over-expressed in many cancer cells, and of
bantam
, an anti-apoptosis miRNA. Third, even when copy number changes seemed distinct between lines, there was strong evidence that they supported a common phenotypic outcome. For example, we found that proto-oncogenes were over-represented in one cell line (
S2-DRSC
), whereas tumor suppressor genes were under-represented in another (
Kc167
).
Conclusion
Our study illustrates how genome structure changes may contribute to selection of cell lines
in vitro
. This has implications for other cell-level natural selection progressions, including tumorigenesis. |
|---|---|
| AbstractList | Background
Structural rearrangements of the genome resulting in genic imbalance due to copy number change are often deleterious at the organismal level, but are common in immortalized cell lines and tumors, where they may be an advantage to cells. In order to explore the biological consequences of copy number changes in the
Drosophila
genome, we resequenced the genomes of 19 tissue-culture cell lines and generated RNA-Seq profiles.
Results
Our work revealed dramatic duplications and deletions in all cell lines. We found three lines of evidence indicating that copy number changes were due to selection during tissue culture. First, we found that copy numbers correlated to maintain stoichiometric balance in protein complexes and biochemical pathways, consistent with the gene balance hypothesis. Second, while most copy number changes were cell line-specific, we identified some copy number changes shared by many of the independent cell lines. These included dramatic recurrence of increased copy number of the PDGF/VEGF receptor, which is also over-expressed in many cancer cells, and of
bantam
, an anti-apoptosis miRNA. Third, even when copy number changes seemed distinct between lines, there was strong evidence that they supported a common phenotypic outcome. For example, we found that proto-oncogenes were over-represented in one cell line (
S2-DRSC
), whereas tumor suppressor genes were under-represented in another (
Kc167
).
Conclusion
Our study illustrates how genome structure changes may contribute to selection of cell lines
in vitro
. This has implications for other cell-level natural selection progressions, including tumorigenesis. Background: Structural rearrangements of the genome resulting in genic imbalance due to copy number change are often deleterious at the organismal level, but are common in immortalized cell lines and tumors, where they may be an advantage to cells. In order to explore the biological consequences of copy number changes in the Drosophila genome, we resequenced the genomes of 19 tissue-culture cell lines and generated RNA-Seq profiles. Results: Our work revealed dramatic duplications and deletions in all cell lines. We found three lines of evidence indicating that copy number changes were due to selection during tissue culture. First, we found that copy numbers correlated to maintain stoichiometric balance in protein complexes and biochemical pathways, consistent with the gene balance hypothesis. Second, while most copy number changes were cell line-specific, we identified some copy number changes shared by many of the independent cell lines. These included dramatic recurrence of increased copy number of the PDGF/VEGF receptor, which is also over-expressed in many cancer cells, and of bantam, an anti-apoptosis miRNA. Third, even when copy number changes seemed distinct between lines, there was strong evidence that they supported a common phenotypic outcome. For example, we found that proto-oncogenes were over-represented in one cell line (S2-DRSC), whereas tumor suppressor genes were under-represented in another (Kc167). Conclusion: Our study illustrates how genome structure changes may contribute to selection of cell lines in vitro. This has implications for other cell-level natural selection progressions, including tumorigenesis. Structural rearrangements of the genome resulting in genic imbalance due to copy number change are often deleterious at the organismal level, but are common in immortalized cell lines and tumors, where they may be an advantage to cells. In order to explore the biological consequences of copy number changes in the Drosophila genome, we resequenced the genomes of 19 tissue-culture cell lines and generated RNA-Seq profiles. Our work revealed dramatic duplications and deletions in all cell lines. We found three lines of evidence indicating that copy number changes were due to selection during tissue culture. First, we found that copy numbers correlated to maintain stoichiometric balance in protein complexes and biochemical pathways, consistent with the gene balance hypothesis. Second, while most copy number changes were cell line-specific, we identified some copy number changes shared by many of the independent cell lines. These included dramatic recurrence of increased copy number of the PDGF/VEGF receptor, which is also over-expressed in many cancer cells, and of bantam, an anti-apoptosis miRNA. Third, even when copy number changes seemed distinct between lines, there was strong evidence that they supported a common phenotypic outcome. For example, we found that proto-oncogenes were over-represented in one cell line (S2-DRSC), whereas tumor suppressor genes were under-represented in another (Kc167). Our study illustrates how genome structure changes may contribute to selection of cell lines in vitro. This has implications for other cell-level natural selection progressions, including tumorigenesis. Structural rearrangements of the genome resulting in genic imbalance due to copy number change are often deleterious at the organismal level, but are common in immortalized cell lines and tumors, where they may be an advantage to cells. In order to explore the biological consequences of copy number changes in the Drosophila genome, we resequenced the genomes of 19 tissue-culture cell lines and generated RNA-Seq profiles. Our work revealed dramatic duplications and deletions in all cell lines. We found three lines of evidence indicating that copy number changes were due to selection during tissue culture. First, we found that copy numbers correlated to maintain stoichiometric balance in protein complexes and biochemical pathways, consistent with the gene balance hypothesis. Second, while most copy number changes were cell line-specific, we identified some copy number changes shared by many of the independent cell lines. These included dramatic recurrence of increased copy number of the PDGF/VEGF receptor, which is also over-expressed in many cancer cells, and of bantam, an anti-apoptosis miRNA. Third, even when copy number changes seemed distinct between lines, there was strong evidence that they supported a common phenotypic outcome. For example, we found that proto-oncogenes were over-represented in one cell line (S2-DRSC), whereas tumor suppressor genes were under-represented in another (Kc167). Our study illustrates how genome structure changes may contribute to selection of cell lines in vitro. This has implications for other cell-level natural selection progressions, including tumorigenesis. Structural rearrangements of the genome resulting in genic imbalance due to copy number change are often deleterious at the organismal level, but are common in immortalized cell lines and tumors, where they may be an advantage to cells. In order to explore the biological consequences of copy number changes in the Drosophila genome, we resequenced the genomes of 19 tissue-culture cell lines and generated RNA-Seq profiles.BACKGROUNDStructural rearrangements of the genome resulting in genic imbalance due to copy number change are often deleterious at the organismal level, but are common in immortalized cell lines and tumors, where they may be an advantage to cells. In order to explore the biological consequences of copy number changes in the Drosophila genome, we resequenced the genomes of 19 tissue-culture cell lines and generated RNA-Seq profiles.Our work revealed dramatic duplications and deletions in all cell lines. We found three lines of evidence indicating that copy number changes were due to selection during tissue culture. First, we found that copy numbers correlated to maintain stoichiometric balance in protein complexes and biochemical pathways, consistent with the gene balance hypothesis. Second, while most copy number changes were cell line-specific, we identified some copy number changes shared by many of the independent cell lines. These included dramatic recurrence of increased copy number of the PDGF/VEGF receptor, which is also over-expressed in many cancer cells, and of bantam, an anti-apoptosis miRNA. Third, even when copy number changes seemed distinct between lines, there was strong evidence that they supported a common phenotypic outcome. For example, we found that proto-oncogenes were over-represented in one cell line (S2-DRSC), whereas tumor suppressor genes were under-represented in another (Kc167).RESULTSOur work revealed dramatic duplications and deletions in all cell lines. We found three lines of evidence indicating that copy number changes were due to selection during tissue culture. First, we found that copy numbers correlated to maintain stoichiometric balance in protein complexes and biochemical pathways, consistent with the gene balance hypothesis. Second, while most copy number changes were cell line-specific, we identified some copy number changes shared by many of the independent cell lines. These included dramatic recurrence of increased copy number of the PDGF/VEGF receptor, which is also over-expressed in many cancer cells, and of bantam, an anti-apoptosis miRNA. Third, even when copy number changes seemed distinct between lines, there was strong evidence that they supported a common phenotypic outcome. For example, we found that proto-oncogenes were over-represented in one cell line (S2-DRSC), whereas tumor suppressor genes were under-represented in another (Kc167).Our study illustrates how genome structure changes may contribute to selection of cell lines in vitro. This has implications for other cell-level natural selection progressions, including tumorigenesis.CONCLUSIONOur study illustrates how genome structure changes may contribute to selection of cell lines in vitro. This has implications for other cell-level natural selection progressions, including tumorigenesis. |
| ArticleNumber | R70 |
| Author | Cherbas, Lucy Przytycka, Teresa M Somma, Maria Patrizia Oliver, Brian Lee, Hangnoh Zhan, Lijun Eaton, Matthew Powell, Sara May, Gemma MacAlpine, David Cho, Dong-Yeon Graveley, Brenton Gatti, Maurizio McManus, C Joel Resch, Alissa Cherbas, Peter Andrews, Justen Celniker, Susan E Renda, Fioranna Zhang, Dayu |
| Author_xml | – sequence: 1 givenname: Hangnoh surname: Lee fullname: Lee, Hangnoh organization: National Institute of Diabetes, Digestive, and Kidney Diseases, National Institutes of Health – sequence: 2 givenname: C Joel surname: McManus fullname: McManus, C Joel organization: Department of Genetics and Developmental Biology, Institute for Systems Genomics, University of Connecticut Health Center, Department of Biological Sciences, Carnegie Mellon University – sequence: 3 givenname: Dong-Yeon surname: Cho fullname: Cho, Dong-Yeon organization: Computational Biology Branch, National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health – sequence: 4 givenname: Matthew surname: Eaton fullname: Eaton, Matthew organization: Department of Pharmacology and Cancer Biology, Duke University Medical Center, Levine Science Research Center – sequence: 5 givenname: Fioranna surname: Renda fullname: Renda, Fioranna organization: Istituto di Biologia e Patologia Molecolari (IBPM) del CNR and Dipartimento di Biologia e Biotecnologie, Sapienza, Università di Roma – sequence: 6 givenname: Maria Patrizia surname: Somma fullname: Somma, Maria Patrizia organization: Istituto di Biologia e Patologia Molecolari (IBPM) del CNR and Dipartimento di Biologia e Biotecnologie, Sapienza, Università di Roma – sequence: 7 givenname: Lucy surname: Cherbas fullname: Cherbas, Lucy organization: Department of Biology, Indiana University – sequence: 8 givenname: Gemma surname: May fullname: May, Gemma organization: Department of Genetics and Developmental Biology, Institute for Systems Genomics, University of Connecticut Health Center, Department of Biological Sciences, Carnegie Mellon University – sequence: 9 givenname: Sara surname: Powell fullname: Powell, Sara organization: Department of Pharmacology and Cancer Biology, Duke University Medical Center, Levine Science Research Center – sequence: 10 givenname: Dayu surname: Zhang fullname: Zhang, Dayu organization: Department of Biology, Indiana University, School of Agricultural and Food Science, Zhejiang A&F University – sequence: 11 givenname: Lijun surname: Zhan fullname: Zhan, Lijun organization: Department of Genetics and Developmental Biology, Institute for Systems Genomics, University of Connecticut Health Center – sequence: 12 givenname: Alissa surname: Resch fullname: Resch, Alissa organization: Department of Genetics and Developmental Biology, Institute for Systems Genomics, University of Connecticut Health Center – sequence: 13 givenname: Justen surname: Andrews fullname: Andrews, Justen organization: Department of Biology, Indiana University – sequence: 14 givenname: Susan E surname: Celniker fullname: Celniker, Susan E organization: Department of Genome Dynamics, Lawrence Berkeley National Laboratory – sequence: 15 givenname: Peter surname: Cherbas fullname: Cherbas, Peter organization: Department of Biology, Indiana University – sequence: 16 givenname: Teresa M surname: Przytycka fullname: Przytycka, Teresa M organization: Computational Biology Branch, National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health – sequence: 17 givenname: Maurizio surname: Gatti fullname: Gatti, Maurizio organization: Istituto di Biologia e Patologia Molecolari (IBPM) del CNR and Dipartimento di Biologia e Biotecnologie, Sapienza, Università di Roma – sequence: 18 givenname: Brian surname: Oliver fullname: Oliver, Brian email: briano@helix.nih.gov organization: National Institute of Diabetes, Digestive, and Kidney Diseases, National Institutes of Health – sequence: 19 givenname: Brenton surname: Graveley fullname: Graveley, Brenton email: graveley@uchc.edu organization: Department of Genetics and Developmental Biology, Institute for Systems Genomics, University of Connecticut Health Center – sequence: 20 givenname: David surname: MacAlpine fullname: MacAlpine, David email: david.macalpine@duke.edu organization: Department of Pharmacology and Cancer Biology, Duke University Medical Center, Levine Science Research Center |
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| Keywords | Fourth Chromosome Kc167 Cell Copy Number Change Data Coordination Center Dosage Compensation |
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| PublicationPlace | London |
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| PublicationTitle | Genome biology |
| PublicationTitleAbbrev | Genome Biol |
| PublicationTitleAlternate | Genome Biol |
| PublicationYear | 2014 |
| Publisher | BioMed Central |
| Publisher_xml | – sequence: 0 name: BioMed Central – name: BioMed Central |
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Structural rearrangements of the genome resulting in genic imbalance due to copy number change are often deleterious at the organismal level, but... Structural rearrangements of the genome resulting in genic imbalance due to copy number change are often deleterious at the organismal level, but are common in... Background: Structural rearrangements of the genome resulting in genic imbalance due to copy number change are often deleterious at the organismal level, but... BACKGROUND: Structural rearrangements of the genome resulting in genic imbalance due to copy number change are often deleterious at the organismal level, but... |
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| SubjectTerms | Animal Genetics and Genomics Animals Bantam BASIC BIOLOGICAL SCIENCES biochemical pathways Bioinformatics Biomedical and Life Sciences carcinogenesis Cell Line Cell Survival copy number change data coordination center DNA DNA - analysis dosage compensation Drosophila Drosophila melanogaster - cytology Drosophila melanogaster - genetics Drosophila Proteins - genetics Evolution, Molecular Evolutionary Biology Female fourth chromosome Gene Dosage Genetic Fitness Genetic Variation Human Genetics Kc167 cell Life Sciences Male Microbial Genetics and Genomics microRNA MicroRNAs - genetics natural selection neoplasm cells neoplasms phenotype Plant Genetics and Genomics proto-oncogenes Receptor Protein-Tyrosine Kinases - genetics Selection, Genetic sequence analysis Sequence Analysis, DNA Sex Chromosomes - genetics tissue culture Tissue Culture Techniques tumor suppressor genes vascular endothelial growth factor receptors vascular endothelial growth factors |
| Title | DNA copy number evolution in Drosophila cell lines |
| URI | https://link.springer.com/article/10.1186/gb-2014-15-8-r70 https://www.ncbi.nlm.nih.gov/pubmed/25262759 https://www.proquest.com/docview/1566831174 https://www.proquest.com/docview/1634269683 https://www.proquest.com/docview/2000280407 https://www.osti.gov/servlets/purl/1626745 https://pubmed.ncbi.nlm.nih.gov/PMC4289277 |
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