Genome-wide chromosomal association of Upf1 is linked to Pol II transcription in Schizosaccharomyces pombe

Sandip De; David M Edwards; Vibha Dwivedi; Jianming Wang; Wazeer Varsally; Hannah L Dixon; Anand K Singh; Precious O Owuamalam; Matthew T Wright; Reece P Summers; Md Nazmul Hossain; Emily M Price; Marcin W Wojewodzic; Francesco Falciani; Nikolas J Hodges; Marco Saponaro; Kayoko Tanaka; Claus M Azzalin; Peter Baumann; Daniel Hebenstreit; Saverio Brogna

doi:10.1093/nar/gkab1249

Genome-wide chromosomal association of Upf1 is linked to Pol II transcription in Schizosaccharomyces pombe

Sandip De, David M Edwards, Vibha Dwivedi, Jianming Wang, Wazeer Varsally, Hannah L Dixon, Anand K Singh, Precious O Owuamalam, Matthew T Wright, Reece P Summers, Md Nazmul Hossain, Emily M Price, Marcin W Wojewodzic, Francesco Falciani, Nikolas J Hodges, Marco Saponaro, Kayoko Tanaka, Claus M Azzalin, Peter Baumann, Daniel HebenstreitSaverio Brogna

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Abstract

Although the RNA helicase Upf1 has hitherto been examined mostly in relation to its cytoplasmic role in nonsense mediated mRNA decay (NMD), here we report high-throughput ChIP data indicating genome-wide association of Upf1 with active genes in Schizosaccharomyces pombe. This association is RNase sensitive, correlates with Pol II transcription and mRNA expression levels. Changes in Pol II occupancy were detected in a Upf1 deficient (upf1Δ) strain, prevalently at genes showing a high Upf1 relative to Pol II association in wild-type. Additionally, an increased Ser2 Pol II signal was detected at all highly transcribed genes examined by ChIP-qPCR. Furthermore, upf1Δ cells are hypersensitive to the transcription elongation inhibitor 6-azauracil. A significant proportion of the genes associated with Upf1 in wild-type conditions are also mis-regulated in upf1Δ. These data envisage that by operating on the nascent transcript, Upf1 might influence Pol II phosphorylation and transcription.

Original language	English
Pages (from-to)	350-367
Number of pages	18
Journal	Nucleic Acids Research
Volume	50
Issue number	1
Early online date	20 Dec 2021
DOIs	https://doi.org/10.1093/nar/gkab1249
Publication status	Published - 11 Jan 2022

Bibliographical note

ASJC Scopus subject areas

Genetics

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10.1093/nar/gkab1249Licence: Creative Commons: Attribution (CC BY)

gkab1249Final published version, 3.49 MBLicence: Creative Commons: Attribution (CC BY)

Understanding the role that the RNA helicase UPF1 plays in nuclear processes of gene expression
Brogna, S. (Principal Investigator)
Biotechnology & Biological Sciences Research Council
2/09/19 → 28/02/25
Project: Research Councils
Investigation of nonsense mediated mRNA decay (NMD) mechanisms
Brogna, S. (Principal Investigator), Cooper, H. (Co-Investigator) & Kanhere, A. (Co-Investigator)
Biotechnology & Biological Sciences Research Council
4/01/16 → 3/09/19
Project: Research Councils

Cite this

De, S., Edwards, D. M., Dwivedi, V., Wang, J., Varsally, W., Dixon, H. L., Singh, A. K., Owuamalam, P. O., Wright, M. T., Summers, R. P., Hossain, M. N., Price, E. M., Wojewodzic, M. W., Falciani, F., Hodges, N. J., Saponaro, M., Tanaka, K., Azzalin, C. M., Baumann, P., ... Brogna, S. (2022). Genome-wide chromosomal association of Upf1 is linked to Pol II transcription in Schizosaccharomyces pombe. Nucleic Acids Research, 50(1), 350-367. https://doi.org/10.1093/nar/gkab1249

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title = "Genome-wide chromosomal association of Upf1 is linked to Pol II transcription in Schizosaccharomyces pombe",

abstract = "Although the RNA helicase Upf1 has hitherto been examined mostly in relation to its cytoplasmic role in nonsense mediated mRNA decay (NMD), here we report high-throughput ChIP data indicating genome-wide association of Upf1 with active genes in Schizosaccharomyces pombe. This association is RNase sensitive, correlates with Pol II transcription and mRNA expression levels. Changes in Pol II occupancy were detected in a Upf1 deficient (upf1Δ) strain, prevalently at genes showing a high Upf1 relative to Pol II association in wild-type. Additionally, an increased Ser2 Pol II signal was detected at all highly transcribed genes examined by ChIP-qPCR. Furthermore, upf1Δ cells are hypersensitive to the transcription elongation inhibitor 6-azauracil. A significant proportion of the genes associated with Upf1 in wild-type conditions are also mis-regulated in upf1Δ. These data envisage that by operating on the nascent transcript, Upf1 might influence Pol II phosphorylation and transcription.",

author = "Sandip De and Edwards, {David M} and Vibha Dwivedi and Jianming Wang and Wazeer Varsally and Dixon, {Hannah L} and Singh, {Anand K} and Owuamalam, {Precious O} and Wright, {Matthew T} and Summers, {Reece P} and Hossain, {Md Nazmul} and Price, {Emily M} and Wojewodzic, {Marcin W} and Francesco Falciani and Hodges, {Nikolas J} and Marco Saponaro and Kayoko Tanaka and Azzalin, {Claus M} and Peter Baumann and Daniel Hebenstreit and Saverio Brogna",

note = "{\textcopyright} The Author(s) 2021. Published by Oxford University Press on behalf of Nucleic Acids Research.",

year = "2022",

month = jan,

day = "11",

doi = "10.1093/nar/gkab1249",

language = "English",

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De, S, Edwards, DM, Dwivedi, V, Wang, J, Varsally, W, Dixon, HL, Singh, AK, Owuamalam, PO, Wright, MT, Summers, RP, Hossain, MN, Price, EM, Wojewodzic, MW, Falciani, F, Hodges, NJ , Saponaro, M, Tanaka, K, Azzalin, CM, Baumann, P, Hebenstreit, D & Brogna, S 2022, 'Genome-wide chromosomal association of Upf1 is linked to Pol II transcription in Schizosaccharomyces pombe', Nucleic Acids Research, vol. 50, no. 1, pp. 350-367. https://doi.org/10.1093/nar/gkab1249

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T1 - Genome-wide chromosomal association of Upf1 is linked to Pol II transcription in Schizosaccharomyces pombe

AU - De, Sandip

AU - Edwards, David M

AU - Dwivedi, Vibha

AU - Wang, Jianming

AU - Varsally, Wazeer

AU - Dixon, Hannah L

AU - Singh, Anand K

AU - Owuamalam, Precious O

AU - Wright, Matthew T

AU - Summers, Reece P

AU - Hossain, Md Nazmul

AU - Price, Emily M

AU - Wojewodzic, Marcin W

AU - Falciani, Francesco

AU - Hodges, Nikolas J

AU - Saponaro, Marco

AU - Tanaka, Kayoko

AU - Azzalin, Claus M

AU - Baumann, Peter

AU - Hebenstreit, Daniel

AU - Brogna, Saverio

PY - 2022/1/11

Y1 - 2022/1/11

N2 - Although the RNA helicase Upf1 has hitherto been examined mostly in relation to its cytoplasmic role in nonsense mediated mRNA decay (NMD), here we report high-throughput ChIP data indicating genome-wide association of Upf1 with active genes in Schizosaccharomyces pombe. This association is RNase sensitive, correlates with Pol II transcription and mRNA expression levels. Changes in Pol II occupancy were detected in a Upf1 deficient (upf1Δ) strain, prevalently at genes showing a high Upf1 relative to Pol II association in wild-type. Additionally, an increased Ser2 Pol II signal was detected at all highly transcribed genes examined by ChIP-qPCR. Furthermore, upf1Δ cells are hypersensitive to the transcription elongation inhibitor 6-azauracil. A significant proportion of the genes associated with Upf1 in wild-type conditions are also mis-regulated in upf1Δ. These data envisage that by operating on the nascent transcript, Upf1 might influence Pol II phosphorylation and transcription.

AB - Although the RNA helicase Upf1 has hitherto been examined mostly in relation to its cytoplasmic role in nonsense mediated mRNA decay (NMD), here we report high-throughput ChIP data indicating genome-wide association of Upf1 with active genes in Schizosaccharomyces pombe. This association is RNase sensitive, correlates with Pol II transcription and mRNA expression levels. Changes in Pol II occupancy were detected in a Upf1 deficient (upf1Δ) strain, prevalently at genes showing a high Upf1 relative to Pol II association in wild-type. Additionally, an increased Ser2 Pol II signal was detected at all highly transcribed genes examined by ChIP-qPCR. Furthermore, upf1Δ cells are hypersensitive to the transcription elongation inhibitor 6-azauracil. A significant proportion of the genes associated with Upf1 in wild-type conditions are also mis-regulated in upf1Δ. These data envisage that by operating on the nascent transcript, Upf1 might influence Pol II phosphorylation and transcription.

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DO - 10.1093/nar/gkab1249

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SN - 0305-1048

VL - 50

SP - 350

EP - 367

JO - Nucleic Acids Research

JF - Nucleic Acids Research

IS - 1

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Genome-wide chromosomal association of Upf1 is linked to Pol II transcription in Schizosaccharomyces pombe

Abstract

Bibliographical note

ASJC Scopus subject areas

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Projects

Understanding the role that the RNA helicase UPF1 plays in nuclear processes of gene expression

Investigation of nonsense mediated mRNA decay (NMD) mechanisms

Cite this