A requirement for ERK-dependent Dicer phosphorylation in coordinating oocyte-to-embryo transition in C. elegans
Signaling pathways and small RNAs direct diverse cellular events, but few examples are known of defined signaling pathways directly regulating small RNA biogenesis. We show that ERK phosphorylates Dicer on two conserved residues in its RNase IIIb and double-stranded RNA (dsRNA)-binding domains and t...
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| Published in | Developmental cell Vol. 31; no. 5; pp. 614 - 628 |
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| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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United States
08.12.2014
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| Abstract | Signaling pathways and small RNAs direct diverse cellular events, but few examples are known of defined signaling pathways directly regulating small RNA biogenesis. We show that ERK phosphorylates Dicer on two conserved residues in its RNase IIIb and double-stranded RNA (dsRNA)-binding domains and that phosphorylation of these residues is necessary and sufficient to trigger Dicer's nuclear translocation in worms, mice, and human cells. Phosphorylation of Dicer on either site inhibits Dicer function in the female germline and dampens small RNA repertoire. Our data demonstrate that ERK phosphorylates and inhibits Dicer during meiosis I for oogenesis to proceed normally in Caenorhabditis elegans and that this inhibition is released before fertilization for embryogenesis to proceed normally. The conserved Dicer residues, their phosphorylation by ERK, and the consequences of the resulting modifications implicate an ERK-Dicer nexus as a fundamental component of the oocyte-to-embryo transition and an underlying mechanism coupling extracellular cues to small RNA production. |
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| AbstractList | Signaling pathways and small RNAs direct diverse cellular events, but few examples are known of defined signaling pathways directly regulating small RNA biogenesis. We show that ERK phosphorylates Dicer on two conserved residues in its RNase IIIb and double-stranded RNA (dsRNA)-binding domains and that phosphorylation of these residues is necessary and sufficient to trigger Dicer's nuclear translocation in worms, mice, and human cells. Phosphorylation of Dicer on either site inhibits Dicer function in the female germline and dampens small RNA repertoire. Our data demonstrate that ERK phosphorylates and inhibits Dicer during meiosis I for oogenesis to proceed normally in Caenorhabditis elegans and that this inhibition is released before fertilization for embryogenesis to proceed normally. The conserved Dicer residues, their phosphorylation by ERK, and the consequences of the resulting modifications implicate an ERK-Dicer nexus as a fundamental component of the oocyte-to-embryo transition and an underlying mechanism coupling extracellular cues to small RNA production. |
| Author | Suen, Kin Man Skeath, James B Liu, Bin Ladbury, John E Gonzalez, Gabriel Drake, Melanie Fire, Andrew Z Kalia, Awdhesh Furuta, Tokiko Arur, Swathi |
| Author_xml | – sequence: 1 givenname: Melanie surname: Drake fullname: Drake, Melanie organization: Department of Genetics, UT MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 2 givenname: Tokiko surname: Furuta fullname: Furuta, Tokiko organization: Department of Genetics, UT MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 3 givenname: Kin Man surname: Suen fullname: Suen, Kin Man organization: Department of Biochemistry and Molecular Biology, UT MD Anderson Cancer Center, Houston, TX 77030, USA; Graduate School of Biomedical Sciences, Houston, TX 77030, USA – sequence: 4 givenname: Gabriel surname: Gonzalez fullname: Gonzalez, Gabriel organization: Department of Genetics, UT MD Anderson Cancer Center, Houston, TX 77030, USA; Graduate School of Biomedical Sciences, Houston, TX 77030, USA – sequence: 5 givenname: Bin surname: Liu fullname: Liu, Bin organization: Center for Genetics and Genomics, UT MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 6 givenname: Awdhesh surname: Kalia fullname: Kalia, Awdhesh organization: Graduate Program in Diagnostic Genetics, School of Health Professions, UT MD Anderson Cancer Center, Houston, TX 77030, USA – sequence: 7 givenname: John E surname: Ladbury fullname: Ladbury, John E organization: Department of Biochemistry and Molecular Biology, UT MD Anderson Cancer Center, Houston, TX 77030, USA; Graduate School of Biomedical Sciences, Houston, TX 77030, USA – sequence: 8 givenname: Andrew Z surname: Fire fullname: Fire, Andrew Z organization: Department of Pathology and Genetics, Stanford University, Stanford, CA 94305, USA – sequence: 9 givenname: James B surname: Skeath fullname: Skeath, James B organization: Department of Genetics, Washington University School of Medicine, Scott Avenue, St. Louis, MO 63110, USA – sequence: 10 givenname: Swathi surname: Arur fullname: Arur, Swathi email: sarur@mdanderson.org organization: Department of Genetics, UT MD Anderson Cancer Center, Houston, TX 77030, USA; Graduate School of Biomedical Sciences, Houston, TX 77030, USA; Center for Genetics and Genomics, UT MD Anderson Cancer Center, Houston, TX 77030, USA. Electronic address: sarur@mdanderson.org |
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| Title | A requirement for ERK-dependent Dicer phosphorylation in coordinating oocyte-to-embryo transition in C. elegans |
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