PMID- 29339519 OWN - NLM STAT- MEDLINE DCOM- 20180716 LR - 20211204 IS - 1091-6490 (Electronic) IS - 0027-8424 (Print) IS - 0027-8424 (Linking) VI - 115 IP - 5 DP - 2018 Jan 30 TI - Evidence for convergent evolution of SINE-directed Staufen-mediated mRNA decay. PG - 968-973 LID - 10.1073/pnas.1715531115 [doi] AB - Primate-specific Alu short interspersed elements (SINEs) as well as rodent-specific B and ID (B/ID) SINEs can promote Staufen-mediated decay (SMD) when present in mRNA 3'-untranslated regions (3'-UTRs). The transposable nature of SINEs, their presence in long noncoding RNAs, their interactions with Staufen, and their rapid divergence in different evolutionary lineages suggest they could have generated substantial modification of posttranscriptional gene-control networks during mammalian evolution. Some of the variation in SMD regulation produced by SINE insertion might have had a similar regulatory effect in separate mammalian lineages, leading to parallel evolution of the Staufen network by independent expansion of lineage-specific SINEs. To explore this possibility, we searched for orthologous gene pairs, each carrying a species-specific 3'-UTR SINE and each regulated by SMD, by measuring changes in mRNA abundance after individual depletion of two SMD factors, Staufen1 (STAU1) and UPF1, in both human and mouse myoblasts. We identified and confirmed orthologous gene pairs with 3'-UTR SINEs that independently function in SMD control of myoblast metabolism. Expanding to other species, we demonstrated that SINE-directed SMD likely emerged in both primate and rodent lineages >20-25 million years ago. Our work reveals a mechanism for the convergent evolution of posttranscriptional gene regulatory networks in mammals by species-specific SINE transposition and SMD. FAU - Lucas, Bronwyn A AU - Lucas BA AD - Department of Biochemistry and Biophysics, School of Medicine and Dentistry, University of Rochester Medical Center, Rochester, NY 14642. AD - Center for RNA Biology, University of Rochester, Rochester, NY 14642. FAU - Lavi, Eitan AU - Lavi E AD - Department of Genetics, Alexander Silberman Institute of Life Sciences, Faculty of Science, Hebrew University of Jerusalem, Jerusalem 91904, Israel. FAU - Shiue, Lily AU - Shiue L AD - Center for Molecular Biology of RNA, Department of Molecular, Cell and Developmental Biology, University of California, Santa Cruz, CA 95064. FAU - Cho, Hana AU - Cho H AD - Department of Biochemistry and Biophysics, School of Medicine and Dentistry, University of Rochester Medical Center, Rochester, NY 14642. AD - Center for RNA Biology, University of Rochester, Rochester, NY 14642. FAU - Katzman, Sol AU - Katzman S AD - Center for Biomolecular Science and Engineering, University of California, Santa Cruz, CA 95064. FAU - Miyoshi, Keita AU - Miyoshi K AD - Department of Biochemistry and Biophysics, School of Medicine and Dentistry, University of Rochester Medical Center, Rochester, NY 14642. AD - Center for RNA Biology, University of Rochester, Rochester, NY 14642. FAU - Siomi, Mikiko C AU - Siomi MC AD - Graduate School of Science, University of Tokyo, Tokyo 113-0032, Japan. FAU - Carmel, Liran AU - Carmel L AD - Department of Genetics, Alexander Silberman Institute of Life Sciences, Faculty of Science, Hebrew University of Jerusalem, Jerusalem 91904, Israel. FAU - Ares, Manuel Jr AU - Ares M Jr AD - Center for Molecular Biology of RNA, Department of Molecular, Cell and Developmental Biology, University of California, Santa Cruz, CA 95064; ares@ucsc.edu lynne_maquat@urmc.rochester.edu. FAU - Maquat, Lynne E AU - Maquat LE AD - Department of Biochemistry and Biophysics, School of Medicine and Dentistry, University of Rochester Medical Center, Rochester, NY 14642; ares@ucsc.edu lynne_maquat@urmc.rochester.edu. AD - Center for RNA Biology, University of Rochester, Rochester, NY 14642. LA - eng SI - figshare/10.6084/m9.figshare.4765015 GR - R01 GM040478/GM/NIGMS NIH HHS/United States GR - R37 GM074593/GM/NIGMS NIH HHS/United States PT - Journal Article DEP - 20180116 PL - United States TA - Proc Natl Acad Sci U S A JT - Proceedings of the National Academy of Sciences of the United States of America JID - 7505876 RN - 0 (3' Untranslated Regions) RN - 0 (Pyruvate Dehydrogenase Acetyl-Transferring Kinase) RN - 0 (RNA, Messenger) RN - 0 (RNA-Binding Proteins) RN - 0 (staufen protein, mammalian) RN - EC 2.7.11.1 (Protein Serine-Threonine Kinases) SB - IM MH - 3' Untranslated Regions MH - AT Rich Sequence MH - Animals MH - *Evolution, Molecular MH - Humans MH - Mice MH - Protein Serine-Threonine Kinases/genetics/metabolism MH - Pyruvate Dehydrogenase Acetyl-Transferring Kinase MH - RNA Stability/*genetics MH - RNA, Messenger/genetics/metabolism MH - RNA-Binding Proteins/genetics/*metabolism MH - *Short Interspersed Nucleotide Elements PMC - PMC5798355 OTO - NOTNLM OT - SINEs OT - Staufen-mediated mRNA decay OT - Staufen1 OT - UPF1 OT - convergent evolution COIS- The authors declare no conflict of interest. EDAT- 2018/01/18 06:00 MHDA- 2018/07/17 06:00 PMCR- 2018/07/30 CRDT- 2018/01/18 06:00 PHST- 2018/01/18 06:00 [pubmed] PHST- 2018/07/17 06:00 [medline] PHST- 2018/01/18 06:00 [entrez] PHST- 2018/07/30 00:00 [pmc-release] AID - 1715531115 [pii] AID - 201715531 [pii] AID - 10.1073/pnas.1715531115 [doi] PST - ppublish SO - Proc Natl Acad Sci U S A. 2018 Jan 30;115(5):968-973. doi: 10.1073/pnas.1715531115. Epub 2018 Jan 16.