Identification of HuR target circular RNAs uncovers suppression of PABPN1 translation by CircPABPN1

HuR influences gene expression programs and hence cellular phenotypes by binding to hundreds of coding and noncoding linear RNAs. However, whether HuR binds to circular RNAs (circRNAs) and impacts on their function is unknown. Here, we have identified en masse circRNAs binding HuR in human cervical...

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Vydáno v:RNA biology Ročník 14; číslo 3; s. 361 - 369
Hlavní autoři: Abdelmohsen, Kotb, Panda, Amaresh C., Munk, Rachel, Grammatikakis, Ioannis, Dudekula, Dawood B., De, Supriyo, Kim, Jiyoung, Noh, Ji Heon, Kim, Kyoung Mi, Martindale, Jennifer L., Gorospe, Myriam
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States Taylor & Francis 04.03.2017
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ISSN:1547-6286, 1555-8584, 1555-8584
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Abstract HuR influences gene expression programs and hence cellular phenotypes by binding to hundreds of coding and noncoding linear RNAs. However, whether HuR binds to circular RNAs (circRNAs) and impacts on their function is unknown. Here, we have identified en masse circRNAs binding HuR in human cervical carcinoma HeLa cells. One of the most prominent HuR target circRNAs was hsa_circ_0031288, renamed CircPABPN1 as it arises from the PABPN1 pre-mRNA. Further analysis revealed that HuR did not influence CircPABPN1 abundance; interestingly, however, high levels of CircPABPN1 suppressed HuR binding to PABPN1 mRNA. Evaluation of PABPN1 mRNA polysomes indicated that PABPN1 translation was modulated positively by HuR and hence negatively by CircPABPN1. We propose that the extensive binding of CircPABPN1 to HuR prevents HuR binding to PABPN1 mRNA and lowers PABPN1 translation, providing the first example of competition between a circRNA and its cognate mRNA for an RBP that affects translation.
AbstractList HuR influences gene expression programs and hence cellular phenotypes by binding to hundreds of coding and noncoding linear RNAs. However, whether HuR binds to circular RNAs (circRNAs) and impacts on their function is unknown. Here, we have identified en masse circRNAs binding HuR in human cervical carcinoma HeLa cells. One of the most prominent HuR target circRNAs was hsa_circ_0031288, renamed CircPABPN1 as it arises from the PABPN1 pre-mRNA. Further analysis revealed that HuR did not influence CircPABPN1 abundance; interestingly, however, high levels of CircPABPN1 suppressed HuR binding to PABPN1 mRNA. Evaluation of PABPN1 mRNA polysomes indicated that PABPN1 translation was modulated positively by HuR and hence negatively by CircPABPN1. We propose that the extensive binding of CircPABPN1 to HuR prevents HuR binding to PABPN1 mRNA and lowers PABPN1 translation, providing the first example of competition between a circRNA and its cognate mRNA for an RBP that affects translation.
HuR influences gene expression programs and hence cellular phenotypes by binding to hundreds of coding and noncoding linear RNAs. However, whether HuR binds to circular RNAs (circRNAs) and impacts on their function is unknown. Here, we have identified en masse circRNAs binding HuR in human cervical carcinoma HeLa cells. One of the most prominent HuR target circRNAs was hsa_circ_0031288, renamed CircPABPN1 as it arises from the PABPN1 pre-mRNA. Further analysis revealed that HuR did not influence CircPABPN1 abundance; interestingly, however, high levels of CircPABPN1 suppressed HuR binding to PABPN1 mRNA. Evaluation of PABPN1 mRNA polysomes indicated that PABPN1 translation was modulated positively by HuR and hence negatively by CircPABPN1. We propose that the extensive binding of CircPABPN1 to HuR prevents HuR binding to PABPN1 mRNA and lowers PABPN1 translation, providing the first example of competition between a circRNA and its cognate mRNA for an RBP that affects translation.HuR influences gene expression programs and hence cellular phenotypes by binding to hundreds of coding and noncoding linear RNAs. However, whether HuR binds to circular RNAs (circRNAs) and impacts on their function is unknown. Here, we have identified en masse circRNAs binding HuR in human cervical carcinoma HeLa cells. One of the most prominent HuR target circRNAs was hsa_circ_0031288, renamed CircPABPN1 as it arises from the PABPN1 pre-mRNA. Further analysis revealed that HuR did not influence CircPABPN1 abundance; interestingly, however, high levels of CircPABPN1 suppressed HuR binding to PABPN1 mRNA. Evaluation of PABPN1 mRNA polysomes indicated that PABPN1 translation was modulated positively by HuR and hence negatively by CircPABPN1. We propose that the extensive binding of CircPABPN1 to HuR prevents HuR binding to PABPN1 mRNA and lowers PABPN1 translation, providing the first example of competition between a circRNA and its cognate mRNA for an RBP that affects translation.
Author Abdelmohsen, Kotb
Panda, Amaresh C.
Noh, Ji Heon
Kim, Kyoung Mi
Gorospe, Myriam
Grammatikakis, Ioannis
Dudekula, Dawood B.
De, Supriyo
Kim, Jiyoung
Martindale, Jennifer L.
Munk, Rachel
Author_xml – sequence: 1
  givenname: Kotb
  surname: Abdelmohsen
  fullname: Abdelmohsen, Kotb
  email: abdelmohsenk@mail.nih.gov, abdelmohsenk@grc.nia.nih.gov
  organization: Laboratory of Genetics and Genomics, National Institute on Aging, National Institutes of Health
– sequence: 2
  givenname: Amaresh C.
  surname: Panda
  fullname: Panda, Amaresh C.
  organization: Laboratory of Genetics and Genomics, National Institute on Aging, National Institutes of Health
– sequence: 3
  givenname: Rachel
  surname: Munk
  fullname: Munk, Rachel
  organization: Laboratory of Genetics and Genomics, National Institute on Aging, National Institutes of Health
– sequence: 4
  givenname: Ioannis
  surname: Grammatikakis
  fullname: Grammatikakis, Ioannis
  organization: Laboratory of Genetics and Genomics, National Institute on Aging, National Institutes of Health
– sequence: 5
  givenname: Dawood B.
  surname: Dudekula
  fullname: Dudekula, Dawood B.
  organization: Laboratory of Genetics and Genomics, National Institute on Aging, National Institutes of Health
– sequence: 6
  givenname: Supriyo
  surname: De
  fullname: De, Supriyo
  organization: Laboratory of Genetics and Genomics, National Institute on Aging, National Institutes of Health
– sequence: 7
  givenname: Jiyoung
  surname: Kim
  fullname: Kim, Jiyoung
  organization: Laboratory of Genetics and Genomics, National Institute on Aging, National Institutes of Health
– sequence: 8
  givenname: Ji Heon
  surname: Noh
  fullname: Noh, Ji Heon
  organization: Laboratory of Genetics and Genomics, National Institute on Aging, National Institutes of Health
– sequence: 9
  givenname: Kyoung Mi
  surname: Kim
  fullname: Kim, Kyoung Mi
  organization: Laboratory of Genetics and Genomics, National Institute on Aging, National Institutes of Health
– sequence: 10
  givenname: Jennifer L.
  surname: Martindale
  fullname: Martindale, Jennifer L.
  organization: Laboratory of Genetics and Genomics, National Institute on Aging, National Institutes of Health
– sequence: 11
  givenname: Myriam
  surname: Gorospe
  fullname: Gorospe, Myriam
  organization: Laboratory of Genetics and Genomics, National Institute on Aging, National Institutes of Health
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28080204$$D View this record in MEDLINE/PubMed
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Snippet HuR influences gene expression programs and hence cellular phenotypes by binding to hundreds of coding and noncoding linear RNAs. However, whether HuR binds to...
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proquest
pubmed
crossref
informaworld
SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 361
SubjectTerms Base Sequence
Binding Sites
Cell Line, Tumor
Cell proliferation
circPABPN1
circular RNA
ELAV-Like Protein 1 - metabolism
endogenous competing RNA
gene expression
Gene Expression Regulation
human cell lines
human diseases
Humans
HuR
messenger RNA
Models, Biological
neoplasm cells
PABPN1
phenotype
Poly(A)-Binding Protein I - genetics
polyribosomes
Protein Binding
Protein Biosynthesis
Research Paper
RNA - genetics
RNA - metabolism
RNA, Messenger - chemistry
RNA, Messenger - genetics
RNA, Messenger - metabolism
RNA-binding Protein
translation
translation (genetics)
uterine cervical neoplasms
Title Identification of HuR target circular RNAs uncovers suppression of PABPN1 translation by CircPABPN1
URI https://www.tandfonline.com/doi/abs/10.1080/15476286.2017.1279788
https://www.ncbi.nlm.nih.gov/pubmed/28080204
https://www.proquest.com/docview/1861424493
https://www.proquest.com/docview/2440693629
https://pubmed.ncbi.nlm.nih.gov/PMC5367248
Volume 14
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