Staufen‐mediated mRNA decay

Staufen1 (STAU1)‐mediated mRNA decay (SMD) is an mRNA degradation process in mammalian cells that is mediated by the binding of STAU1 to a STAU1‐binding site (SBS) within the 3′‐untranslated region (3′‐UTR) of target mRNAs. During SMD, STAU1, a double‐stranded (ds) RNA‐binding protein, recognizes dsRNA structures formed either by intramolecular base pairing of 3′‐UTR sequences or by intermolecular base pairing of 3′‐UTR sequences with a long‐noncoding RNA (lncRNA) via partially complementary Alu elements. Recently, STAU2, a paralog of STAU1, has also been reported to mediate SMD. Both STAU1 and STAU2 interact directly with the ATP‐dependent RNA helicase UPF1, a key SMD factor, enhancing its helicase activity to promote effective SMD. Moreover, STAU1 and STAU2 form homodimeric and heterodimeric interactions via domain‐swapping. Because both SMD and the mechanistically related nonsense‐mediated mRNA decay (NMD) employ UPF1; SMD and NMD are competitive pathways. Competition contributes to cellular differentiation processes, such as myogenesis and adipogenesis, placing SMD at the heart of various physiologically important mechanisms. WIREs RNA 2013, 4:423–435. doi: 10.1002/wrna.1168

[1]  R. Kesterson,et al.  Deletion of PPARγ in adipose tissues of mice protects against high fat diet-induced obesity and insulin resistance , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[2]  T. Miki,et al.  Cell type-dependent gene regulation by Staufen2 in conjunction with Upf1 , 2011, BMC Molecular Biology.

[3]  T. Jensen,et al.  Nuclear quality control of RNA polymerase II transcripts , 2010, Wiley interdisciplinary reviews. RNA.

[4]  L. Maquat,et al.  Staufen1 dimerizes via a conserved motif and a degenerate dsRNA-binding domain to promote mRNA decay , 2013, Nature Structural &Molecular Biology.

[5]  Y. Nam,et al.  The transport of Staufen2‐containing ribonucleoprotein complexes involves kinesin motor protein and is modulated by mitogen‐activated protein kinase pathway , 2007, Journal of neurochemistry.

[6]  T. Kerppola,et al.  Close encounters of many kinds: Fos-Jun interactions that mediate transcription regulatory specificity , 2001, Oncogene.

[7]  Louise Wickham,et al.  Mammalian Staufen Is a Double-Stranded-RNA- and Tubulin-Binding Protein Which Localizes to the Rough Endoplasmic Reticulum , 1999, Molecular and Cellular Biology.

[8]  R. Parker,et al.  Structural basis of the PNRC2-mediated link between mrna surveillance and decapping. , 2012, Structure.

[9]  J. Lacaille,et al.  Staufen 2 regulates mGluR long-term depression and Map1b mRNA distribution in hippocampal neurons. , 2011, Learning & memory.

[10]  Craig E. Higgins,et al.  SERPINE1 (PAI-1) is deposited into keratinocyte migration “trails” and required for optimal monolayer wound repair , 2008, Archives of Dermatological Research.

[11]  G. Kusek,et al.  Asymmetric segregation of the double-stranded RNA binding protein Staufen2 during mammalian neural stem cell divisions promotes lineage progression. , 2012, Cell stem cell.

[12]  L. Maquat,et al.  “Alu”strious long ncRNAs and their roles in shortening mRNA half-lives , 2011, Cell cycle.

[13]  Craig E. Higgins,et al.  SERPINE1 (PAI-1) is a prominent member of the early G0 --> G1 transition "wound repair" transcriptome in p53 mutant human keratinocytes. , 2008, The Journal of investigative dermatology.

[14]  Christopher W. Wong,et al.  RCP is a human breast cancer-promoting gene with Ras-activating function. , 2009, The Journal of clinical investigation.

[15]  J. Lacaille,et al.  mRNA binding protein staufen 1-dependent regulation of pyramidal cell spine morphology via NMDA receptor-mediated synaptic plasticity , 2011, Molecular Brain.

[16]  Silvia Domcke,et al.  Molecular mechanisms for the RNA-dependent ATPase activity of Upf1 and its regulation by Upf2. , 2011, Molecular cell.

[17]  G. Steinberg,et al.  Adipose tissue as an endocrine organ , 2010, Molecular and Cellular Endocrinology.

[18]  J. Epstein,et al.  Pax3 Inhibits Myogenic Differentiation of Cultured Myoblast Cells (*) , 1995, The Journal of Biological Chemistry.

[19]  J. Lykke-Andersen,et al.  Upf1 ATPase-Dependent mRNP Disassembly Is Required for Completion of Nonsense- Mediated mRNA Decay , 2010, Cell.

[20]  R. Bravo,et al.  c-JUN, JUN B, and JUN D differ in their binding affinities to AP-1 and CRE consensus sequences: effect of FOS proteins. , 1991, Oncogene.

[21]  L. Maquat,et al.  Nonsense-mediated mRNA decay (NMD) in animal embryogenesis: to die or not to die, that is the question. , 2011, Current opinion in genetics & development.

[22]  K. Mowry,et al.  Principles and roles of mRNA localization in animal development , 2012, Development.

[23]  Yoon Ki Kim,et al.  Human proline-rich nuclear receptor coregulatory protein 2 mediates an interaction between mRNA surveillance machinery and decapping complex. , 2009, Molecular cell.

[24]  L. Maquat,et al.  The Pioneer Round of Translation: Features and Functions , 2010, Cell.

[25]  A. Jacobson,et al.  RNA decay modulates gene expression and controls its fidelity , 2010, Wiley interdisciplinary reviews. RNA.

[26]  L. Maquat,et al.  Upf1 Phosphorylation Triggers Translational Repression during Nonsense-Mediated mRNA Decay , 2008, Cell.

[27]  M. Kiebler,et al.  Staufen2 isoforms localize to the somatodendritic domain of neurons and interact with different organelles. , 2002, Journal of cell science.

[28]  Sanjay Tyagi,et al.  Neuronal mRNAs travel singly into dendrites , 2012, Proceedings of the National Academy of Sciences.

[29]  L. Maquat,et al.  Staufen2 functions in Staufen1-mediated mRNA decay by binding to itself and its paralog and promoting UPF1 helicase but not ATPase activity , 2012, Proceedings of the National Academy of Sciences.

[30]  R. Parker,et al.  Structural and functional insights into the human Upf 1 helicase core , 2013 .

[31]  R. Steinman.  mRNA stability control: a clandestine force in normal and malignant hematopoiesis , 2007, Leukemia.

[32]  Roy Parker,et al.  No‐go decay: a quality control mechanism for RNA in translation , 2010, Wiley interdisciplinary reviews. RNA.

[33]  L. Maquat,et al.  Rules that govern UPF1 binding to mRNA 3′ UTRs , 2013, Proceedings of the National Academy of Sciences.

[34]  E. Lai.  miRNAs: Whys and Wherefores of miRNA-Mediated Regulation , 2005, Current Biology.

[35]  K. Nishikura,et al.  RNA Binding-independent Dimerization of Adenosine Deaminases Acting on RNA and Dominant Negative Effects of Nonfunctional Subunits on Dimer Functions* , 2007, Journal of Biological Chemistry.

[36]  G. Peters,et al.  Modular Structure of PACT: Distinct Domains for Binding and Activating PKR , 2001, Molecular and Cellular Biology.

[37]  M. Karin,et al.  AP-1 as a regulator of cell life and death , 2002, Nature Cell Biology.

[38]  O. Mühlemann,et al.  Cutting the nonsense: the degradation of PTC-containing mRNAs. , 2010, Biochemical Society transactions.

[39]  A. Ballabio,et al.  Identification of a novel homolog of the Drosophila staufen protein in the chromosome 8q13-q21.1 region. , 1999, Genomics.

[40]  E. Wieschaus,et al.  Germline autonomy of maternal-effect mutations altering the embryonic body pattern of Drosophila. , 1986, Developmental biology.

[41]  S. Hoshino.  Mechanism of the initiation of mRNA decay: role of eRF3 family G proteins , 2012, Wiley interdisciplinary reviews. RNA.

[42]  J. Lacaille,et al.  Staufen1 Regulation of Protein Synthesis-Dependent Long-Term Potentiation and Synaptic Function in Hippocampal Pyramidal Cells , 2008, Molecular and Cellular Biology.

[43]  R. Jansen,et al.  Assembly of mRNA-Protein Complexes for Directional mRNA Transport in Eukaryotes - An Overview , 2012, Current protein & peptide science.

[44]  L. Maquat,et al.  Regulation of cytoplasmic mRNA decay , 2012, Nature Reviews Genetics.

[45]  Anne Gatignol,et al.  TRBP, a regulator of cellular PKR and HIV‐1 virus expression, interacts with Dicer and functions in RNA silencing , 2005, EMBO reports.

[46]  Paul Martin,et al.  Wound Healing--Aiming for Perfect Skin Regeneration , 1997, Science.

[47]  P. Higgins,et al.  PAI‐1 expression is required for epithelial cell migration in two distinct phases of in vitro wound repair , 2004, Journal of cellular physiology.

[48]  M. Kiebler,et al.  An asymmetrically localized Staufen2-dependent RNA complex regulates maintenance of mammalian neural stem cells. , 2012, Cell stem cell.

[49]  M. Wilkinson,et al.  Regulation of nonsense‐mediated mRNA decay , 2012, Wiley interdisciplinary reviews. RNA.

[50]  R. Balsara,et al.  Enhanced in Vitro Proliferation of Aortic Endothelial Cells from Plasminogen Activator Inhibitor-1-deficient Mice* , 2004, Journal of Biological Chemistry.

[51]  R. Parker,et al.  Structural and functional insights into the human Upf1 helicase core , 2007, The EMBO journal.

[52]  L. Maquat,et al.  Gene expression networks: competing mRNA decay pathways in mammalian cells. , 2009, Biochemical Society transactions.

[53]  Florence Besse,et al.  Translational control of localized mRNAs: restricting protein synthesis in space and time , 2008, Nature Reviews Molecular Cell Biology.

[54]  Victor K. Lin,et al.  Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD , 1989, Cell.

[55]  L. Furic,et al.  A genome-wide approach identifies distinct but overlapping subsets of cellular mRNAs associated with Staufen1- and Staufen2-containing ribonucleoprotein complexes. , 2007, RNA.

[56]  Luc DesGroseillers,et al.  Mammalian Staufen1 Recruits Upf1 to Specific mRNA 3′UTRs so as to Elicit mRNA Decay , 2005, Cell.

[57]  F. Bonneau,et al.  NMD factors UPF2 and UPF3 bridge UPF1 to the exon junction complex and stimulate its RNA helicase activity , 2008, Nature Structural &Molecular Biology.

[58]  I. Gallouzi,et al.  Decoding ARE-mediated decay: is microRNA part of the equation? , 2008, The Journal of cell biology.

[59]  Gene W. Yeo,et al.  The EJC Factor eIF4AIII Modulates Synaptic Strength and Neuronal Protein Expression , 2007, Cell.

[60]  H. Lodish,et al.  Induction of caveolin during adipogenesis and association of GLUT4 with caveolin-rich vesicles , 1994, The Journal of cell biology.

[61]  Bin Tian,et al.  A large-scale analysis of mRNA polyadenylation of human and mouse genes , 2005, Nucleic acids research.

[62]  T. Gondo,et al.  Promotion of skin epithelial cell migration and wound healing by a 2-benzazepine derivative. , 2007, European journal of pharmacology.

[63]  O. MacDougald,et al.  Adipocyte differentiation from the inside out , 2006, Nature Reviews Molecular Cell Biology.

[64]  R. Shiekhattar,et al.  TRBP recruits the Dicer complex to Ago2 for microRNA processing and gene silencing , 2005, Nature.

[65]  Béatrice Conne,et al.  The 3′ untranslated region of messenger RNA: A molecular ‘hotspot’ for pathology? , 2000, Nature Medicine.

[66]  G. Dreyfuss,et al.  Binding of a novel SMG-1-Upf1-eRF1-eRF3 complex (SURF) to the exon junction complex triggers Upf1 phosphorylation and nonsense-mediated mRNA decay. , 2006, Genes & development.

[67]  M. Batzer,et al.  Alu repeats and human genomic diversity , 2002, Nature Reviews Genetics.

[68]  M. Kiebler,et al.  The Mammalian Staufen Protein Localizes to the Somatodendritic Domain of Cultured Hippocampal Neurons: Implications for Its Involvement in mRNA Transport , 1999, The Journal of Neuroscience.

[69]  J. Lykke-Andersen,et al.  Regulated and quality-control mRNA turnover pathways in eukaryotes. , 2010, Biochemical Society transactions.

[70]  L. Maquat,et al.  SMD and NMD are competitive pathways that contribute to myogenesis: effects on PAX3 and myogenin mRNAs. , 2009, Genes & development.

[71]  K. Kosik,et al.  The mammalian RNA-binding protein staufen2 links nuclear and cytoplasmic RNA processing pathways in neurons , 2007, NeuroMolecular Medicine.

[72]  George A. Calin,et al.  Mammalian microRNAs: a small world for fine-tuning gene expression , 2006, Mammalian Genome.

[73]  Yoon Ki Kim,et al.  Staufen1-mediated mRNA decay functions in adipogenesis. , 2012, Molecular cell.

[74]  J. Bishop,et al.  A 3' truncation of MYC caused by chromosomal translocation in a human T-cell leukemia increases mRNA stability. , 1990, Oncogene.

[75]  L. Maquat,et al.  Biochemical analysis of long non-coding RNA-containing ribonucleoprotein complexes. , 2012, Methods.

[76]  P. Higgins,et al.  PAI‐1 gene expression is regionally induced in wounded epithelial cell monolayers and required for injury repair , 2000, Journal of cellular physiology.

[77]  M. Santoro,et al.  Cellular and molecular facets of keratinocyte reepithelization during wound healing. , 2005, Experimental cell research.

[78]  T. Curran,et al.  Removal of a 67-base-pair sequence in the noncoding region of protooncogene fos converts it to a transforming gene. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[79]  T. Duchaine,et al.  Multimerization of Staufen1 in live cells. , 2010, RNA.

[80]  L. Maquat,et al.  Staufen1 regulates diverse classes of mammalian transcripts , 2007, The EMBO journal.

[81]  Y. Taya,et al.  Human SMG-1, a novel phosphatidylinositol 3-kinase-related protein kinase, associates with components of the mRNA surveillance complex and is involved in the regulation of nonsense-mediated mRNA decay. , 2001, Genes & development.

[82]  D. Benjamin,et al.  mRNA stability and cancer: an emerging link? , 2007, Expert opinion on biological therapy.

[83]  M. Kiebler,et al.  The brain-specific double-stranded RNA-binding protein Staufen2 is required for dendritic spine morphogenesis , 2006, The Journal of cell biology.

[84]  M. Kiebler,et al.  Microtubule-dependent recruitment of Staufen-green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons. , 1999, Molecular biology of the cell.

[85]  P. V. John,et al.  ネズミのスタウフェン1に対する機能消失対立遺伝子は,樹状突起のStaufen1‐RNP配送や樹状突起棘の形態形成の障害を誘導する , 2008 .

[86]  B. Spiegelman,et al.  Molecular regulation of adipogenesis. , 2000, Annual review of cell and developmental biology.

[87]  Nahum Sonenberg,et al.  The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC , 2012, Nature Structural &Molecular Biology.

[88]  T. Abel,et al.  A loss of function allele for murine Staufen1 leads to impairment of dendritic Staufen1-RNP delivery and dendritic spine morphogenesis , 2008, Proceedings of the National Academy of Sciences.

[89]  L. Maquat,et al.  lncRNAs transactivate Staufen1-mediated mRNA decay by duplexing with 3'UTRs via Alu elements , 2010, Nature.

[90]  S. Peltz,et al.  Characterization of the biochemical properties of the human Upf1 gene product that is involved in nonsense-mediated mRNA decay. , 2000, RNA.

[91]  R. Kesterson,et al.  Deletion of PPARgamma in adipose tissues of mice protects against high fat diet-induced obesity and insulin resistance. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[92]  E. Schuman,et al.  A Role for a Rat Homolog of Staufen in the Transport of RNA to Neuronal Dendrites , 2001, Neuron.

[93]  Shiuan Chen,et al.  Nuclear Receptor Coactivator PNRC2 Regulates Energy Expenditure and Adiposity* , 2008, Journal of Biological Chemistry.

[94]  A. Git,et al.  Two distinct Staufen isoforms in Xenopus are vegetally localized during oogenesis. , 2004, RNA.

[95]  A. Mouland,et al.  Interaction of Staufen1 with the 5′ end of mRNA facilitates translation of these RNAs , 2005, Nucleic acids research.

[96]  M. Kiebler,et al.  Mechanisms of dendritic mRNA transport and its role in synaptic tagging , 2011, The EMBO journal.