Subcellular mRNA Localization in Animal Cells and Why It Matters

Subcellular localization of messenger RNAs (mRNAs) can give precise control over where protein products are synthesized and operate. However, just 10 years ago many in the broader cell biology community would have considered this a specialized mechanism restricted to a very small fraction of transcripts. Since then, it has become clear that subcellular targeting of mRNAs is prevalent, and there is mounting evidence for central roles for this process in many cellular events. Here, we review current knowledge of the mechanisms and functions of mRNA localization in animal cells.

[1]  R. Delanoue,et al.  Dynein Anchors Its mRNA Cargo after Apical Transport in the Drosophila Blastoderm Embryo , 2005, Cell.

[2]  W. Chia,et al.  Roles of Bifocal, Homer, and F-actin in anchoring Oskar to the posterior cortex of Drosophila oocytes. , 2004, Genes & development.

[3]  Konstantin A Lukyanov,et al.  Intra-axonal translation and retrograde trafficking of CREB promotes neuronal survival , 2008, Nature Cell Biology.

[4]  S. Schacher,et al.  Target Interaction Regulates Distribution and Stability of Specific mRNAs , 2002, The Journal of Neuroscience.

[5]  R. Singer,et al.  Assembling an intermediate filament network by dynamic cotranslation , 2006, The Journal of cell biology.

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

[7]  James A. Gagnon,et al.  PTB/hnRNP I Is Required for RNP Remodeling during RNA Localization in Xenopus Oocytes , 2007, Molecular and Cellular Biology.

[8]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[9]  J. Carson,et al.  The balance of power in RNA trafficking , 2001, Current Opinion in Neurobiology.

[10]  D. Melton,et al.  A two-step model for the localization of maternal mRNA in Xenopus oocytes: involvement of microtubules and microfilaments in the translocation and anchoring of Vg1 mRNA. , 1990, Development.

[11]  L. Nagy,et al.  Asymmetric inheritance of centrosomally localized mRNAs during embryonic cleavages , 2002, Nature.

[12]  Jiaqi Yao,et al.  An essential role for β-actin mRNA localization and translation in Ca2+-dependent growth cone guidance , 2006, Nature Neuroscience.

[13]  R. Rosenfeld.  Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[14]  S. Bullock,et al.  Guidance of Bidirectional Motor Complexes by mRNA Cargoes through Control of Dynein Number and Activity , 2006, Current Biology.

[15]  C. Sardet,et al.  Maternal determinants and mRNAs in the cortex of ascidian oocytes, zygotes and embryos , 2005, Biology of the cell.

[16]  S. Bullock,et al.  Egalitarian is a selective RNA-binding protein linking mRNA localization signals to the dynein motor. , 2009, Genes & development.

[17]  S. Bullock.  Translocation of mRNAs by molecular motors: think complex? , 2007, Seminars in cell & developmental biology.

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

[19]  J. Mitchison.  Cell Biology , 1964, Nature.

[20]  Robert H. Singer,et al.  Single mRNA Molecules Demonstrate Probabilistic Movement in Living Mammalian Cells , 2003, Current Biology.

[21]  W. Jeffery,et al.  Localization of actin messenger RNA during early ascidian development. , 1983, Developmental biology.

[22]  E. Raz,et al.  Multiple Levels of Posttranscriptional Control Lead to Germ Line-Specific Gene Expression in the Zebrafish , 2002, Current Biology.

[23]  M. Moore,et al.  The nuclear nurture and cytoplasmic nature of localized mRNPs. , 2007, Seminars in cell & developmental biology.

[24]  W. Gu,et al.  ZBP2 Facilitates Binding of ZBP1 to β-Actin mRNA during Transcription , 2007, Molecular and Cellular Biology.

[25]  J. Ashby.  References and Notes , 1999 .

[26]  Robert H Singer,et al.  Asymmetric sorting of ash1p in yeast results from inhibition of translation by localization elements in the mRNA. , 2002, Molecular cell.

[27]  Guoji Guo,et al.  Role of Cdx2 and cell polarity in cell allocation and specification of trophectoderm and inner cell mass in the mouse embryo. , 2008, Genes & development.

[28]  Kelsey C. Martin,et al.  Synapse Formation and mRNA Localization in Cultured Aplysia Neurons , 2006, Neuron.

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

[30]  James A. Gagnon,et al.  Multiple kinesin motors coordinate cytoplasmic RNA transport on a subpopulation of microtubules in Xenopus oocytes. , 2008, Developmental cell.

[31]  C. Holt,et al.  Asymmetrical β-actin mRNA translation in growth cones mediates attractive turning to netrin-1 , 2006, Nature Neuroscience.

[32]  J. Derisi,et al.  Cis-acting determinants of asymmetric, cytoplasmic RNA transport. , 2007, RNA.

[33]  M. Feldbrügge,et al.  mRNA trafficking in fungi , 2007, Molecular Genetics and Genomics.

[34]  E. R. Gavis,et al.  Live Imaging of Endogenous RNA Reveals a Diffusion and Entrapment Mechanism for nanos mRNA Localization in Drosophila , 2003, Current Biology.

[35]  K. Martin,et al.  Synapse- and Stimulus-Specific Local Translation During Long-Term Neuronal Plasticity , 2009, Science.

[36]  Oswald Steward,et al.  Synaptic Activation Causes the mRNA for the IEG Arc to Localize Selectively near Activated Postsynaptic Sites on Dendrites , 1998, Neuron.

[37]  Oswald Steward,et al.  Dynamics of bidirectional transport of Arc mRNA in neuronal dendrites , 2007, The Journal of comparative neurology.

[38]  A. Mccarthy.  Development , 1996, Current Opinion in Neurobiology.

[39]  P. Tomançak,et al.  Global Analysis of mRNA Localization Reveals a Prominent Role in Organizing Cellular Architecture and Function , 2007, Cell.

[40]  H. Lipshitz,et al.  Spatial and temporal control of RNA stability , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[41]  P. Worley,et al.  The Immediate Early Gene Arc/Arg3.1: Regulation, Mechanisms, and Function , 2008, The Journal of Neuroscience.

[42]  C. Nüsslein-Volhard,et al.  The γTuRC components Grip75 and Grip128 have an essential microtubule-anchoring function in the Drosophila germline , 2006, Development.

[43]  D. Finnegan,et al.  gurken and the I factor retrotransposon RNAs share common localization signals and machinery. , 2005, Developmental cell.

[44]  J. Lawrence,et al.  Intracellular localization of messenger RNAs for cytoskeletal proteins , 1986, Cell.

[45]  J. Condeelis,et al.  Spatial regulation of β-actin translation by Src-dependent phosphorylation of ZBP1 , 2005, Nature.

[46]  S. Mili,et al.  Genome-wide screen reveals APC-associated RNAs enriched in cell protrusions , 2008, Nature.

[47]  T. Okita,et al.  mRNA localization in plants: targeting to the cell's cortical region and beyond. , 2002, Current opinion in plant biology.

[48]  R. Singer,et al.  β-Actin Messenger RNA Localization and Protein Synthesis Augment Cell Motility , 1997, The Journal of cell biology.

[49]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]／Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[50]  C. Nüsslein-Volhard,et al.  Myosin-V Regulates oskar mRNA Localization in the Drosophila Oocyte , 2009, Current Biology.

[51]  F. Young.  Biochemistry , 1955, The Indian Medical Gazette.

[52]  Aldine R. Amiel,et al.  Three distinct RNA localization mechanisms contribute to oocyte polarity establishment in the cnidarian Clytia hemisphaerica. , 2009, Developmental biology.

[53]  E. R. Gavis,et al.  Localization of bicoid mRNA in late oocytes is maintained by continual active transport. , 2006, Developmental cell.

[54]  Tyson A. Clark,et al.  HITS-CLIP yields genome-wide insights into brain alternative RNA processing , 2008, Nature.

[55]  G. G. Stokes.  "J." , 1890, The New Yale Book of Quotations.

[56]  M. Mayford,et al.  Disruption of Dendritic Translation of CaMKIIα Impairs Stabilization of Synaptic Plasticity and Memory Consolidation , 2002, Neuron.

[57]  M. L. King,et al.  Putting RNAs in the right place at the right time: RNA localization in the frog oocyte , 2005, Biology of the cell.

[58]  J. Condeelis,et al.  Localization of all seven messenger RNAs for the actin-polymerization nucleator Arp2/3 complex in the protrusions of fibroblasts , 2005, Journal of Cell Science.