The multifunctional Staufen proteins: conserved roles from neurogenesis to synaptic plasticity

Highlights • Staufen (Stau) proteins have evolutionarily conserved functions in the brain.• Stau proteins asymmetrically segregate mRNAs during mouse and fly neurogenesis.• Stau proteins regulate synaptic plasticity and memory formation in flies and mammals.• Stau proteins have roles in translation, localisation, and ribonucleoprotein formation.• New data indicate that mammalian Stau1 and Stau2 can both stabilise and destabilise target mRNAs.

[1]  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.

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

[3]  Martin A. M. Reijns,et al.  A role for Q/N-rich aggregation-prone regions in P-body localization , 2008, Journal of Cell Science.

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

[5]  Q. Morris,et al.  Staufen2 regulates neuronal target RNAs. , 2013, Cell reports.

[6]  P. Macdonald,et al.  Translational regulation of oskar mRNA by Bruno, an ovarian RNA-binding protein, is essential , 1995, Cell.

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

[8]  R. Parker,et al.  Edc3p and a glutamine/asparagine-rich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae , 2007, The Journal of cell biology.

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

[10]  C. Nüsslein-Volhard,et al.  Multiple steps in the localization of bicoid RNA to the anterior pole of the Drosophila oocyte. , 1989, Development.

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

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

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

[14]  P. Madan,et al.  Bovine oocytes and early embryos express Staufen and ELAVL RNA-binding proteins , 2008, Zygote.

[15]  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.

[16]  Stephen M. Fitzjohn,et al.  Metabotropic Glutamate Receptor-Mediated Long-Term Depression: Molecular Mechanisms , 2009, Pharmacological Reviews.

[17]  G. Bassell,et al.  Binding proteins for mRNA localization and local translation, and their dysfunction in genetic neurological disease , 2004, Current Opinion in Neurobiology.

[18]  J. Knoblich,et al.  Mechanisms of Asymmetric Stem Cell Division , 2008, Cell.

[19]  C. Doe,et al.  Staufen-dependent localization of prospero mRNA contributes to neuroblast daughter-cell fate , 1998, Nature.

[20]  M. A. Desbats,et al.  Mammalian Staufen 1 is recruited to stress granules and impairs their assembly , 2009, Journal of Cell Science.

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

[22]  Bin Wu,et al.  Single β-Actin mRNA Detection in Neurons Reveals a Mechanism for Regulating Its Translatability , 2014, Science.

[23]  M. Kiebler,et al.  RNA‐binding proteins involved in RNA localization and their implications in neuronal diseases , 2012, The European journal of neuroscience.

[24]  L. DesGroseillers,et al.  Molecular Composition of Staufen2-Containing Ribonucleoproteins in Embryonic Rat Brain , 2010, PloS one.

[25]  L. DesGroseillers,et al.  Genome wide identification of Staufen2-bound mRNAs in embryonic rat brains. , 2010, BMB reports.

[26]  Peng Li,et al.  Inscuteable and Staufen Mediate Asymmetric Localization and Segregation of prospero RNA during Drosophila Neuroblast Cell Divisions , 1997, Cell.

[27]  M. Chagoyen,et al.  Functional signature for the recognition of specific target mRNAs by human Staufen1 protein , 2014, Nucleic acids research.

[28]  B. Alberts The Cell as a Collection of Protein Machines: Preparing the Next Generation of Molecular Biologists , 1998, Cell.

[29]  K. Mowry,et al.  Xenopus Staufen is a component of a ribonucleoprotein complex containing Vg1 RNA and kinesin , 2004, Development.

[30]  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.

[31]  Eugene Berezikov,et al.  The TRIM-NHL Protein TRIM32 Activates MicroRNAs and Prevents Self-Renewal in Mouse Neural Progenitors , 2009, Cell.

[32]  T. Duchaine,et al.  Molecular mapping of the determinants involved in human Staufen-ribosome association. , 2002, The Biochemical journal.

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

[34]  L. Maquat,et al.  mRNA–mRNA duplexes that auto-elicit Staufen1-mediated mRNA decay , 2013, Nature Structural &Molecular Biology.

[35]  C. Holt,et al.  The Central Dogma Decentralized: New Perspectives on RNA Function and Local Translation in Neurons , 2013, Neuron.

[36]  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.

[37]  Hye Yoon Park,et al.  Visualization of Dynamics of Single Endogenous mRNA Labeled in Live Mouse , 2014, Science.

[38]  P. Anderson,et al.  Stress granule assembly is mediated by prion-like aggregation of TIA-1. , 2004, Molecular biology of the cell.

[39]  L. Maquat,et al.  Staufen‐mediated mRNA decay , 2013, Wiley interdisciplinary reviews. RNA.

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

[41]  Nobutaka Hirokawa,et al.  Kinesin Transports RNA Isolation and Characterization of an RNA-Transporting Granule , 2004, Neuron.

[42]  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.

[43]  G. Superti-Furga,et al.  Interactome of two diverse RNA granules links mRNA localization to translational repression in neurons. , 2013, Cell reports.

[44]  R. Lehmann,et al.  Localization of oskar RNA regulates oskar translation and requires Oskar protein. , 1995, Development.

[45]  Arnold Kriegstein,et al.  The glial nature of embryonic and adult neural stem cells. , 2009, Annual review of neuroscience.

[46]  Daniel St Johnston,et al.  staufen, a gene required to localize maternal RNAs in the Drosophila egg , 1991, Cell.

[47]  L. Maquat,et al.  Control of myogenesis by rodent SINE-containing lncRNAs. , 2013, Genes & development.

[48]  Ann-Shyn Chiang,et al.  Drosophila ORB protein in two mushroom body output neurons is necessary for long-term memory formation , 2013, Proceedings of the National Academy of Sciences.

[49]  H. Rohrer,et al.  Prox1 Regulates the Notch1-Mediated Inhibition of Neurogenesis , 2010, PLoS biology.

[50]  Dietmar Kuhl,et al.  Two rat brain Staufen isoforms differentially bind RNA , 2001, Journal of neurochemistry.

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

[52]  Can Cenik,et al.  Staufen1 senses overall transcript secondary structure to regulate translation , 2013, Nature Structural &Molecular Biology.

[53]  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.

[54]  T. Miyashita,et al.  Mg2+ Block of Drosophila NMDA Receptors Is Required for Long-Term Memory Formation and CREB-Dependent Gene Expression , 2012, Neuron.

[55]  D. Sandstrom,et al.  The Drosophila Transcription Factor Adf-1 (nalyot) Regulates Dendrite Growth by Controlling FasII and Staufen Expression Downstream of CaMKII and Neural Activity , 2013, The Journal of Neuroscience.

[56]  Jean-Christophe Olivo-Marin,et al.  In Vivo Colocalisation of oskar mRNA and Trans-Acting Proteins Revealed by Quantitative Imaging of the Drosophila Oocyte , 2009, PloS one.

[57]  Tim Tully,et al.  Excess protein synthesis in Drosophila Fragile X mutants impairs long-term memory , 2008, Nature Neuroscience.

[58]  M. Kiebler,et al.  Isolation and characterization of Staufen-containing ribonucleoprotein particles from rat brain , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Jimin Pei,et al.  Cell-free Formation of RNA Granules: Low Complexity Sequence Domains Form Dynamic Fibers within Hydrogels , 2012, Cell.

[60]  K. Martin,et al.  mRNA Localization: Gene Expression in the Spatial Dimension , 2009, Cell.

[61]  Q. Morris,et al.  Genome-wide analysis of Staufen-associated mRNAs identifies secondary structures that confer target specificity , 2013, Nucleic acids research.

[62]  Ann-Shyn Chiang,et al.  The staufen/pumilio Pathway Is Involved in Drosophila Long-Term Memory , 2003, Current Biology.

[63]  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.

[64]  K. Irie,et al.  Stau1 regulates Dvl2 expression during myoblast differentiation. , 2012, Biochemical and biophysical research communications.

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

[66]  F. Allain,et al.  RNA recognition by double-stranded RNA binding domains: a matter of shape and sequence , 2012, Cellular and Molecular Life Sciences.

[67]  Erin M. Schuman,et al.  The Local Transcriptome in the Synaptic Neuropil Revealed by Deep Sequencing and High-Resolution Imaging , 2012, Neuron.

[68]  Howard Y. Chang,et al.  Control of somatic tissue differentiation by the long non-coding RNA TINCR , 2012, Nature.

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

[70]  K. Sampath,et al.  Zebrafish Staufen1 and Staufen2 are required for the survival and migration of primordial germ cells. , 2006, Developmental biology.

[71]  S. Antonini,et al.  Cytoplasmic remodelling and the acquisition of developmental competence in pig oocytes. , 2007, Animal reproduction science.

[72]  Christian Lüscher,et al.  Group 1 mGluR-Dependent Synaptic Long-Term Depression: Mechanisms and Implications for Circuitry and Disease , 2010, Neuron.

[73]  J. Knoblich,et al.  Drosophila neuroblasts: a model for stem cell biology , 2012, Development.

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

[75]  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.

[76]  R. M. Marión,et al.  A Human Sequence Homologue of Staufen Is an RNA-Binding Protein That Is Associated with Polysomes and Localizes to the Rough Endoplasmic Reticulum , 1999, Molecular and Cellular Biology.

[77]  T. Miyashita,et al.  Mg2+ Block of Drosophila NMDA Receptors Is Required for Long-Term Memory Formation and CREB-Dependent Gene Expression , 2012, Neuron.

[78]  Bin Tian,et al.  STAU1 binding 3' UTR IRAlus complements nuclear retention to protect cells from PKR-mediated translational shutdown. , 2013, Genes & development.

[79]  I. Dobbie,et al.  Distinguishing direct from indirect roles for bicoid mRNA localization factors , 2010, Development.

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

[81]  S. Schacher,et al.  Two mRNA-Binding Proteins Regulate the Distribution of Syntaxin mRNA in Aplysia Sensory Neurons , 2006, The Journal of Neuroscience.

[82]  Jimin Pei,et al.  Cell-free Formation of RNA Granules: Bound RNAs Identify Features and Components of Cellular Assemblies , 2012, Cell.

[83]  L. Maquat,et al.  Evidence for a Pioneer Round of mRNA Translation mRNAs Subject to Nonsense-Mediated Decay in Mammalian Cells Are Bound by CBP80 and CBP20 , 2001, Cell.

[84]  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.

[85]  Q. Wang,et al.  Neurodegeneration-associated TDP-43 Interacts with Fragile X Mental Retardation Protein (FMRP)/Staufen (STAU1) and Regulates SIRT1 Expression in Neuronal Cells* , 2012, The Journal of Biological Chemistry.

[86]  D. St Johnston,et al.  Distinct roles of two conserved Staufen domains in oskar mRNA localization and translation , 2000, The EMBO journal.

[87]  D. St Johnston,et al.  In Vivo Imaging of oskar mRNA Transport Reveals the Mechanism of Posterior Localization , 2008, Cell.

[88]  K. Mechtler,et al.  Asymmetric Segregation of the Tumor Suppressor Brat Regulates Self-Renewal in Drosophila Neural Stem Cells , 2006, Cell.

[89]  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.