Unique features of transcription termination and initiation at closely spaced tandem human genes
The synthesis of RNA polymerase II (Pol2) products, which include messenger RNAs or long noncoding RNAs, culminates in transcription termination. How the transcriptional termination of a gene impacts the activity of promoters found immediately downstream of it, and which can be subject to potential...
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| Published in | Molecular systems biology Vol. 18; no. 4; pp. e10682 - n/a |
|---|---|
| Main Authors | , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.04.2022
EMBO Press John Wiley and Sons Inc Springer Nature |
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| Online Access | Get full text |
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| Abstract | The synthesis of RNA polymerase II (Pol2) products, which include messenger RNAs or long noncoding RNAs, culminates in transcription termination. How the transcriptional termination of a gene impacts the activity of promoters found immediately downstream of it, and which can be subject to potential transcriptional interference, remains largely unknown. We examined in an unbiased manner the features of the intergenic regions between pairs of ‘tandem genes’—closely spaced (< 2 kb) human genes found on the same strand. Intergenic regions separating tandem genes are enriched with guanines and are characterized by binding of several proteins, including AGO1 and AGO2 of the RNA interference pathway. Additionally, we found that Pol2 is particularly enriched in this region, and it is lost upon perturbations affecting splicing or transcriptional elongation. Perturbations of genes involved in Pol2 pausing and R loop biology preferentially affect expression of downstream genes in tandem gene pairs. Overall, we find that features associated with Pol2 pausing and accumulation rather than those associated with avoidance of transcriptional interference are the predominant driving force shaping short tandem intergenic regions.
Synopsis
Hundreds of human genes are transcribed in close proximity to each other and on the same strand. A systematic computational analysis reveals unique genomic features associated with intergenic regions separating these tandem genes.
Co‐expression of closely spaced tandem human genes is common.
Short tandem intergenic regions (STIRs) are particularly G‐rich.
Several proteins, including AGO1 and AGO2, preferentially bind STIRs.
Pol2 accumulates in STIRs, and perturbations related to Pol2 pausing preferentially regulate tandem gene expression.
Graphical Abstract
Hundreds of human genes are transcribed in close proximity to each other and on the same strand. A systematic computational analysis reveals unique genomic features associated with intergenic regions separating these tandem genes. |
|---|---|
| AbstractList | Abstract The synthesis of RNA polymerase II (Pol2) products, which include messenger RNAs or long noncoding RNAs, culminates in transcription termination. How the transcriptional termination of a gene impacts the activity of promoters found immediately downstream of it, and which can be subject to potential transcriptional interference, remains largely unknown. We examined in an unbiased manner the features of the intergenic regions between pairs of ‘tandem genes’—closely spaced (< 2 kb) human genes found on the same strand. Intergenic regions separating tandem genes are enriched with guanines and are characterized by binding of several proteins, including AGO1 and AGO2 of the RNA interference pathway. Additionally, we found that Pol2 is particularly enriched in this region, and it is lost upon perturbations affecting splicing or transcriptional elongation. Perturbations of genes involved in Pol2 pausing and R loop biology preferentially affect expression of downstream genes in tandem gene pairs. Overall, we find that features associated with Pol2 pausing and accumulation rather than those associated with avoidance of transcriptional interference are the predominant driving force shaping short tandem intergenic regions. The synthesis of RNA polymerase II (Pol2) products, which include messenger RNAs or long noncoding RNAs, culminates in transcription termination. How the transcriptional termination of a gene impacts the activity of promoters found immediately downstream of it, and which can be subject to potential transcriptional interference, remains largely unknown. We examined in an unbiased manner the features of the intergenic regions between pairs of ‘tandem genes’—closely spaced (< 2 kb) human genes found on the same strand. Intergenic regions separating tandem genes are enriched with guanines and are characterized by binding of several proteins, including AGO1 and AGO2 of the RNA interference pathway. Additionally, we found that Pol2 is particularly enriched in this region, and it is lost upon perturbations affecting splicing or transcriptional elongation. Perturbations of genes involved in Pol2 pausing and R loop biology preferentially affect expression of downstream genes in tandem gene pairs. Overall, we find that features associated with Pol2 pausing and accumulation rather than those associated with avoidance of transcriptional interference are the predominant driving force shaping short tandem intergenic regions. image Hundreds of human genes are transcribed in close proximity to each other and on the same strand. A systematic computational analysis reveals unique genomic features associated with intergenic regions separating these tandem genes. Co‐expression of closely spaced tandem human genes is common. Short tandem intergenic regions (STIRs) are particularly G‐rich. Several proteins, including AGO1 and AGO2, preferentially bind STIRs. Pol2 accumulates in STIRs, and perturbations related to Pol2 pausing preferentially regulate tandem gene expression. The synthesis of RNA polymerase II (Pol2) products, which include messenger RNAs or long noncoding RNAs, culminates in transcription termination. How the transcriptional termination of a gene impacts the activity of promoters found immediately downstream of it, and which can be subject to potential transcriptional interference, remains largely unknown. We examined in an unbiased manner the features of the intergenic regions between pairs of ‘tandem genes’—closely spaced (< 2 kb) human genes found on the same strand. Intergenic regions separating tandem genes are enriched with guanines and are characterized by binding of several proteins, including AGO1 and AGO2 of the RNA interference pathway. Additionally, we found that Pol2 is particularly enriched in this region, and it is lost upon perturbations affecting splicing or transcriptional elongation. Perturbations of genes involved in Pol2 pausing and R loop biology preferentially affect expression of downstream genes in tandem gene pairs. Overall, we find that features associated with Pol2 pausing and accumulation rather than those associated with avoidance of transcriptional interference are the predominant driving force shaping short tandem intergenic regions. The synthesis of RNA polymerase II (Pol2) products, which include messenger RNAs or long noncoding RNAs, culminates in transcription termination. How the transcriptional termination of a gene impacts the activity of promoters found immediately downstream of it, and which can be subject to potential transcriptional interference, remains largely unknown. We examined in an unbiased manner the features of the intergenic regions between pairs of 'tandem genes'-closely spaced (< 2 kb) human genes found on the same strand. Intergenic regions separating tandem genes are enriched with guanines and are characterized by binding of several proteins, including AGO1 and AGO2 of the RNA interference pathway. Additionally, we found that Pol2 is particularly enriched in this region, and it is lost upon perturbations affecting splicing or transcriptional elongation. Perturbations of genes involved in Pol2 pausing and R loop biology preferentially affect expression of downstream genes in tandem gene pairs. Overall, we find that features associated with Pol2 pausing and accumulation rather than those associated with avoidance of transcriptional interference are the predominant driving force shaping short tandem intergenic regions.The synthesis of RNA polymerase II (Pol2) products, which include messenger RNAs or long noncoding RNAs, culminates in transcription termination. How the transcriptional termination of a gene impacts the activity of promoters found immediately downstream of it, and which can be subject to potential transcriptional interference, remains largely unknown. We examined in an unbiased manner the features of the intergenic regions between pairs of 'tandem genes'-closely spaced (< 2 kb) human genes found on the same strand. Intergenic regions separating tandem genes are enriched with guanines and are characterized by binding of several proteins, including AGO1 and AGO2 of the RNA interference pathway. Additionally, we found that Pol2 is particularly enriched in this region, and it is lost upon perturbations affecting splicing or transcriptional elongation. Perturbations of genes involved in Pol2 pausing and R loop biology preferentially affect expression of downstream genes in tandem gene pairs. Overall, we find that features associated with Pol2 pausing and accumulation rather than those associated with avoidance of transcriptional interference are the predominant driving force shaping short tandem intergenic regions. The synthesis of RNA polymerase II (Pol2) products, which include messenger RNAs or long noncoding RNAs, culminates in transcription termination. How the transcriptional termination of a gene impacts the activity of promoters found immediately downstream of it, and which can be subject to potential transcriptional interference, remains largely unknown. We examined in an unbiased manner the features of the intergenic regions between pairs of ‘tandem genes’—closely spaced (< 2 kb) human genes found on the same strand. Intergenic regions separating tandem genes are enriched with guanines and are characterized by binding of several proteins, including AGO1 and AGO2 of the RNA interference pathway. Additionally, we found that Pol2 is particularly enriched in this region, and it is lost upon perturbations affecting splicing or transcriptional elongation. Perturbations of genes involved in Pol2 pausing and R loop biology preferentially affect expression of downstream genes in tandem gene pairs. Overall, we find that features associated with Pol2 pausing and accumulation rather than those associated with avoidance of transcriptional interference are the predominant driving force shaping short tandem intergenic regions. Hundreds of human genes are transcribed in close proximity to each other and on the same strand. A systematic computational analysis reveals unique genomic features associated with intergenic regions separating these tandem genes. The synthesis of RNA polymerase II (Pol2) products, which include messenger RNAs or long noncoding RNAs, culminates in transcription termination. How the transcriptional termination of a gene impacts the activity of promoters found immediately downstream of it, and which can be subject to potential transcriptional interference, remains largely unknown. We examined in an unbiased manner the features of the intergenic regions between pairs of ‘tandem genes’—closely spaced (< 2 kb) human genes found on the same strand. Intergenic regions separating tandem genes are enriched with guanines and are characterized by binding of several proteins, including AGO1 and AGO2 of the RNA interference pathway. Additionally, we found that Pol2 is particularly enriched in this region, and it is lost upon perturbations affecting splicing or transcriptional elongation. Perturbations of genes involved in Pol2 pausing and R loop biology preferentially affect expression of downstream genes in tandem gene pairs. Overall, we find that features associated with Pol2 pausing and accumulation rather than those associated with avoidance of transcriptional interference are the predominant driving force shaping short tandem intergenic regions. Synopsis Hundreds of human genes are transcribed in close proximity to each other and on the same strand. A systematic computational analysis reveals unique genomic features associated with intergenic regions separating these tandem genes. Co‐expression of closely spaced tandem human genes is common. Short tandem intergenic regions (STIRs) are particularly G‐rich. Several proteins, including AGO1 and AGO2, preferentially bind STIRs. Pol2 accumulates in STIRs, and perturbations related to Pol2 pausing preferentially regulate tandem gene expression. Hundreds of human genes are transcribed in close proximity to each other and on the same strand. A systematic computational analysis reveals unique genomic features associated with intergenic regions separating these tandem genes. The synthesis of RNA polymerase II (Pol2) products, which include messenger RNAs or long noncoding RNAs, culminates in transcription termination. How the transcriptional termination of a gene impacts the activity of promoters found immediately downstream of it, and which can be subject to potential transcriptional interference, remains largely unknown. We examined in an unbiased manner the features of the intergenic regions between pairs of ‘tandem genes’—closely spaced (< 2 kb) human genes found on the same strand. Intergenic regions separating tandem genes are enriched with guanines and are characterized by binding of several proteins, including AGO1 and AGO2 of the RNA interference pathway. Additionally, we found that Pol2 is particularly enriched in this region, and it is lost upon perturbations affecting splicing or transcriptional elongation. Perturbations of genes involved in Pol2 pausing and R loop biology preferentially affect expression of downstream genes in tandem gene pairs. Overall, we find that features associated with Pol2 pausing and accumulation rather than those associated with avoidance of transcriptional interference are the predominant driving force shaping short tandem intergenic regions. Synopsis Hundreds of human genes are transcribed in close proximity to each other and on the same strand. A systematic computational analysis reveals unique genomic features associated with intergenic regions separating these tandem genes. Co‐expression of closely spaced tandem human genes is common. Short tandem intergenic regions (STIRs) are particularly G‐rich. Several proteins, including AGO1 and AGO2, preferentially bind STIRs. Pol2 accumulates in STIRs, and perturbations related to Pol2 pausing preferentially regulate tandem gene expression. Graphical Abstract Hundreds of human genes are transcribed in close proximity to each other and on the same strand. A systematic computational analysis reveals unique genomic features associated with intergenic regions separating these tandem genes. |
| Author | Ulitsky, Igor Nissani, Noa |
| AuthorAffiliation | 1 Departments of Biological Regulation and Molecular Neuroscience Weizmann Institute of Science Rehovot Israel |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35362230$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1016_j_isci_2022_105543 crossref_primary_10_15252_embj_2022112443 |
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| Keywords | Argonaute proteins Pol2 transcription transcriptional interference tandem genes genome organization |
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| Snippet | The synthesis of RNA polymerase II (Pol2) products, which include messenger RNAs or long noncoding RNAs, culminates in transcription termination. How the... Abstract The synthesis of RNA polymerase II (Pol2) products, which include messenger RNAs or long noncoding RNAs, culminates in transcription termination. How... |
| SourceID | doaj pubmedcentral proquest pubmed crossref wiley springer |
| SourceType | Open Website Open Access Repository Aggregation Database Index Database Enrichment Source Publisher |
| StartPage | e10682 |
| SubjectTerms | Argonaute 2 protein Argonaute proteins Binding sites Chemical synthesis DNA-directed RNA polymerase Elongation EMBO09 Gene expression Genes genome organization Genomes Guanines Humans Interference Mammals Perturbation Pol2 transcription Promoter Regions, Genetic Ribonucleic acid RNA RNA polymerase RNA polymerase II RNA Polymerase II - genetics RNA Polymerase II - metabolism RNA, Messenger RNA-mediated interference Splicing tandem genes Transcription elongation Transcription initiation Transcription termination Transcription, Genetic transcriptional interference |
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| Title | Unique features of transcription termination and initiation at closely spaced tandem human genes |
| URI | https://link.springer.com/article/10.15252/msb.202110682 https://onlinelibrary.wiley.com/doi/abs/10.15252%2Fmsb.202110682 https://www.ncbi.nlm.nih.gov/pubmed/35362230 https://www.proquest.com/docview/2655977627 https://www.proquest.com/docview/2646720692 https://pubmed.ncbi.nlm.nih.gov/PMC8972054 https://doaj.org/article/ea2475733bd44f929871c9a00bc47e4d |
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