Akt-Mediated Phosphorylation of Argonaute 2 Downregulates Cleavage and Upregulates Translational Repression of MicroRNA Targets

A high-throughput RNA interference (RNAi) screen targeting 542 genes of the human kinome was used to discover regulators of RNAi. Here we report that the proto-oncogene Akt-3/PKBγ (Akt3) phosphorylates Argonaute 2 (Ago2) at S387, which downregulates cleavage and upregulates translational repression...

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Published inMolecular cell Vol. 50; no. 3; pp. 356 - 367
Main Authors Horman, Shane R., Janas, Maja M., Litterst, Claudia, Wang, Bingbing, MacRae, Ian J., Sever, Mary J., Morrissey, David V., Graves, Paul, Luo, Biao, Umesalma, Shaikamjad, Qi, Hank H., Miraglia, Loren J., Novina, Carl D., Orth, Anthony P.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 09.05.2013
Subjects
Argonaute Proteins - genetics
Argonaute Proteins - metabolism
Cell Line
Cell Line, Tumor
Down-Regulation
HEK293 Cells
HeLa Cells
Humans
messenger RNA
microRNA
MicroRNAs - genetics
Phosphorylation
Proto-Oncogene Proteins c-akt - genetics
Proto-Oncogene Proteins c-akt - metabolism
proto-oncogenes
RNA interference
translation (genetics)
Up-Regulation
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Abstract A high-throughput RNA interference (RNAi) screen targeting 542 genes of the human kinome was used to discover regulators of RNAi. Here we report that the proto-oncogene Akt-3/PKBγ (Akt3) phosphorylates Argonaute 2 (Ago2) at S387, which downregulates cleavage and upregulates translational repression of endogenous microRNA (miRNA)-targeted messenger RNAs (mRNAs). We further demonstrate that Akt3 coimmunoprecipitates with Ago2 and phosphorylation of Ago2 at S387 facilitates its interaction with GW182 and localization to cytoplasmic processing bodies (P bodies), where miRNA-targeted mRNAs are thought to be stored and degraded. Therefore, Akt3-mediated phosphorylation of Ago2 is a molecular switch between target mRNA cleavage and translational repression activities of Ago2. ► Akt3 interacts with and phosphorylates Ago2 at S387 ► Phosphorylation of Ago2 increases translational repression of pten and pdcd4 ► Phosphorylation of Ago2 decreases mRNA cleavage of the hoxb8 oncogene ► Akt3-mediated phosphorylation of Ago2 is an RNAi molecular switch
AbstractList A high-throughput RNA interference (RNAi) screen targeting 542 genes of the human kinome was used to discover regulators of RNAi. Here we report that the proto-oncogene Akt-3/PKBγ (Akt3) phosphorylates Argonaute 2 (Ago2) at S387, which downregulates cleavage and upregulates translational repression of endogenous microRNA (miRNA)-targeted messenger RNAs (mRNAs). We further demonstrate that Akt3 coimmunoprecipitates with Ago2 and phosphorylation of Ago2 at S387 facilitates its interaction with GW182 and localization to cytoplasmic processing bodies (P bodies), where miRNA-targeted mRNAs are thought to be stored and degraded. Therefore, Akt3-mediated phosphorylation of Ago2 is a molecular switch between target mRNA cleavage and translational repression activities of Ago2.
A high-throughput RNA interference (RNAi) screen targeting 542 genes of the human kinome was used to discover regulators of RNAi. Here we report that the proto-oncogene Akt-3/PKBγ (Akt3) phosphorylates Argonaute 2 (Ago2) at S387, which downregulates cleavage and upregulates translational repression of endogenous microRNA (miRNA)-targeted messenger RNAs (mRNAs). We further demonstrate that Akt3 coimmunoprecipitates with Ago2 and phosphorylation of Ago2 at S387 facilitates its interaction with GW182 and localization to cytoplasmic processing bodies (P bodies), where miRNA-targeted mRNAs are thought to be stored and degraded. Therefore, Akt3-mediated phosphorylation of Ago2 is a molecular switch between target mRNA cleavage and translational repression activities of Ago2. ► Akt3 interacts with and phosphorylates Ago2 at S387 ► Phosphorylation of Ago2 increases translational repression of pten and pdcd4 ► Phosphorylation of Ago2 decreases mRNA cleavage of the hoxb8 oncogene ► Akt3-mediated phosphorylation of Ago2 is an RNAi molecular switch
Author Litterst, Claudia
Wang, Bingbing
Morrissey, David V.
Umesalma, Shaikamjad
Qi, Hank H.
Luo, Biao
Orth, Anthony P.
MacRae, Ian J.
Janas, Maja M.
Graves, Paul
Horman, Shane R.
Miraglia, Loren J.
Sever, Mary J.
Novina, Carl D.
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  surname: Janas
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  organization: Department of Cancer Immunology and AIDS, Dana-Farber Cancer Institute, and Department of Microbiology and Immunobiology, Harvard Medical School, 450 Brookline Avenue, Boston, MA 02215, USA
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  givenname: Claudia
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  surname: Wang
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  organization: Department of Cancer Immunology and AIDS, Dana-Farber Cancer Institute, and Department of Microbiology and Immunobiology, Harvard Medical School, 450 Brookline Avenue, Boston, MA 02215, USA
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  givenname: Ian J.
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  organization: Department of Molecular Biology, The Scripps Research Institute, 10550 N. Torrey Pines Road, La Jolla, CA 92037, USA
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  givenname: Mary J.
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  organization: Department of Molecular Biology, The Scripps Research Institute, 10550 N. Torrey Pines Road, La Jolla, CA 92037, USA
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  givenname: David V.
  surname: Morrissey
  fullname: Morrissey, David V.
  organization: Novartis Institutes for Biomedical Research, 250 Massachusetts Avenue, Cambridge, MA 02139, USA
– sequence: 8
  givenname: Paul
  surname: Graves
  fullname: Graves, Paul
  organization: Department of Radiation Oncology, New York Methodist Hospital, 506 6th Street, Brooklyn, NY 11215, USA
– sequence: 9
  givenname: Biao
  surname: Luo
  fullname: Luo, Biao
  organization: Broad Institute of Harvard and MIT, 7 Cambridge Center, Cambridge, MA 02142, USA
– sequence: 10
  givenname: Shaikamjad
  surname: Umesalma
  fullname: Umesalma, Shaikamjad
  organization: Department of Anatomy and Cell Biology, Carver College of Medicine, University of Iowa, 51 Newton Road, Iowa City, IA 52242, USA
– sequence: 11
  givenname: Hank H.
  surname: Qi
  fullname: Qi, Hank H.
  organization: Department of Anatomy and Cell Biology, Carver College of Medicine, University of Iowa, 51 Newton Road, Iowa City, IA 52242, USA
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  givenname: Loren J.
  surname: Miraglia
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  givenname: Carl D.
  surname: Novina
  fullname: Novina, Carl D.
  organization: Department of Cancer Immunology and AIDS, Dana-Farber Cancer Institute, and Department of Microbiology and Immunobiology, Harvard Medical School, 450 Brookline Avenue, Boston, MA 02215, USA
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  givenname: Anthony P.
  surname: Orth
  fullname: Orth, Anthony P.
  email: aorth@gnf.org
  organization: Genomics Institute of the Novartis Research Foundation, 10675 John Jay Hopkins Drive, San Diego, CA 92121, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/23603119$$D View this record in MEDLINE/PubMed
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Snippet A high-throughput RNA interference (RNAi) screen targeting 542 genes of the human kinome was used to discover regulators of RNAi. Here we report that the...
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SubjectTerms Argonaute Proteins - genetics
Argonaute Proteins - metabolism
Cell Line
Cell Line, Tumor
Down-Regulation
HEK293 Cells
HeLa Cells
Humans
messenger RNA
microRNA
MicroRNAs - genetics
Phosphorylation
Proto-Oncogene Proteins c-akt - genetics
Proto-Oncogene Proteins c-akt - metabolism
proto-oncogenes
RNA interference
translation (genetics)
Up-Regulation
Title Akt-Mediated Phosphorylation of Argonaute 2 Downregulates Cleavage and Upregulates Translational Repression of MicroRNA Targets
URI https://dx.doi.org/10.1016/j.molcel.2013.03.015
https://www.ncbi.nlm.nih.gov/pubmed/23603119
https://search.proquest.com/docview/1350892342
Volume 50
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