Cited by 1,048RNA Research and SplicingRNA and protein synthesis mechanismsBiotin and Related Studies

mRNA localization: Gene expression in the spatial dimension

Open access
Martin, Kelsey C., Ephrussi, Anne·2009·Cell

Abstract

The localization of mRNAs to subcellular compartments provides a mechanism for regulating gene expression with exquisite temporal and spatial control. Recent studies suggest that a large fraction of mRNAs localize to distinct cytoplasmic domains. In this Review, we focus on cis-acting RNA localization elements, RNA-binding proteins, and the assembly of mRNAs into granules that are transported by molecular motors along cytoskeletal elements to their final destination in the cell.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.cell.2009.01.044

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • A 3′UTR participates in alternative cleavage and polyadenylation, translation, and localization of mRNA, affecting mRNA stability.

    “A 3′UTR participates in such processes as alternative cleavage and polyadenylation, translation, and localization of mRNA [19], affecting mRNA stability [20].”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 92

  1. Ainger K Avossa D Diana AS Barry C Barbarese E Carson JH 1997 Transport and localization elements in myelin basic protein mRNA J Cell Bio 138 1077 1087 9281585 PMC2136761
  2. Anderson P Kedersha N 2006 RNA granules J Cell Bio 172 803 808 16520386 PMC2063724
  3. Arn EA Cha BJ Theurkauf WE Macdonald PM 2003 Recognition of a bicoid mRNA localization signal by a protein complex containing Swallow, Nod, and RNA binding proteins Dev Cell 4 41 51 12530962
  4. Aronov S Gelin-Licht R Zipor G Haim L Safran E Gerst JE 2007 mRNAs encoding polarity and exocytosis factors are cotransported with the cortical endoplasmic reticulum to the incipient bud in Saccharomyces cerevisiae Mol Cell Bio 27 3441 3455 17339339 PMC1899969
  5. Bashirullah A Cooperstock RL Lipshitz HD 2001 Spatial and temporal control of RNA stability Proc Natl Acad Sci USA 98 7025 7028 11416182 PMC34617
  6. Bassell GJ Warren ST 2008 Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function Neuron 60 201 214 18957214 PMC3691995
  7. Beach DL Salmon ED Bloom K 1999 Localization and anchoring of mRNA in budding yeast Curr Biol 9 569 578 10359695
  8. Bergsten SE Gavis ER 1999 Role for mRNA localization in translational activation but not spatial restriction of nanos RNA Development 126 659 669 9895314
  9. Besse F Ephrussi A 2008 Translational control of localized mRNAs: restricting protein synthesis in space and time Nature Rev 9 971 980 19023284
  10. Besse F Lopez de Quinto S Marchand V Trucco A Ephrussi A 2009 Drosophila PTB promotes formation of high-order RNP particles and represses oskar translation Genes Dev Jan 8 epub PMC2648539 19131435
  11. Betley JN Frith MC Graber JH Choo S Deshler JO 2002 A ubiquitous and conserved signal for RNA localization in chordates Curr Biol 12 1756 1761 12401170
  12. Blichenberg A Rehbein M Muller R Garner CC Richter D Kindler S 2001 Identification of a cis-acting dendritic targeting element in the mRNA encoding the alpha subunit of Ca2+/calmodulin-dependent protein kinase II Eur J Neurosci 13 1881 1888 11403681
  13. Bullock SL Ish-Horowicz D 2001 Conserved signals and machinery for RNA transport in Drosophila oogenesis and embryogenesis Nature 414 611 616 11740552
  14. Bullock SL Nicol A Gross SP Zicha D 2006 Guidance of bidirectional motor complexes by mRNA cargoes through control of dynein number and activity Curr Biol 16 1447 1452 16860745
  15. Chartrand P Meng XH Huttelmaier S Donato D Singer RH 2002 Asymmetric sorting of ash1p in yeast results from inhibition of translation by localization elements in the mRNA Mol Cell 10 1319 1330 12504008
  16. Chartrand P Meng XH Singer RH Long RM 1999 Structural elements required for the localization of ASH1 mRNA and of a green fluorescent protein reporter particle in vivo Curr Biol 9 333 336 10209102
  17. Chekulaeva M Hentze MW Ephrussi A 2006 Bruno acts as a dual repressor of oskar translation, promoting mRNA oligomerization and formation of silencing particles Cell 124 521 533 16469699
  18. Condeelis J Singer RH 2005 How and why does beta-actin mRNA target? Biol Cell 97 97 110 15601261
  19. Davidovic L Jaglin XH Lepagnol-Bestel AM Tremblay S Simonneau M Bardoni B Khandjian EW 2007 The fragile X mental retardation protein is a molecular adaptor between the neurospecific KIF3C kinesin and dendritic RNA granules Human Mol Gen 16 3047 3058 17881655
  20. Delanoue R Davis I 2005 Dynein anchors its mRNA cargo after apical transport in the Drosophila blastoderm embryo Cell 122 97 106 16009136
  21. Delanoue R Herpers B Soetaert J Davis I Rabouille C 2007 Drosophila Squid/hnRNP helps Dynein switch from a gurken mRNA transport motor to an ultrastructural static anchor in sponge bodies Dev Cell 13 523 538 17925228
  22. Deshler JO Highett MI Schnapp BJ 1997 Localization of Xenopus Vg1 mRNA by Vera protein and the endoplasmic reticulum Science 276 1128 1131 9148809
  23. Dictenberg JB Swanger SA Antar LN Singer RH Bassell GJ 2008 A direct role for FMRP in activity-dependent dendritic mRNA transport links filopodial-spine morphogenesis to fragile X syndrome Dev Cell 14 926 939 18539120 PMC2453222
  24. Doyle F Zaleski C George AD Stenson EK Ricciardi A Tenenbaum SA 2008 Bioinformatic tools for studying post-transcriptional gene regulation: The UAlbany 3′UTR collection and other informatic resources Methods Mol Bio 419 39 52 18369974
  25. Duncan JE Warrior R 2002 The cytoplasmic dynein and kinesin motors have interdependent roles in patterning the Drosophila oocyte Curr Biol 12 1982 1991 12477386
  26. Eberwine J Belt B Kacharmina JE Miyashiro K 2002 Analysis of subcellularly localized mRNAs using in situ hybridization, mRNA amplification, and expression profiling Neurochem Res 27 1065 1077 12462405
  27. Elvira G Wasiak S Blandford V Tong XK Serrano A Fan X del Rayo Sanchez-Carbente M Servant F Bell AW Boismenu D 2006 Characterization of an RNA granule from developing brain Mol Cell Proteomics 5 635 651 16352523
  28. Farina KL Huttelmaier S Musunuru K Darnell R Singer RH 2003 Two ZBP1 KH domains facilitate beta-actin mRNA localization, granule formation, and cytoskeletal attachment J Cell Biol 160 77 87 12507992 PMC2172732
  29. Ferrandon D Elphick L Nusslein-Volhard C St Johnston D 1994 Staufen protein associates with the 3′UTR of bicoid mRNA to form particles that move in a microtubule-dependent manner Cell 79 1221 1232 8001156
  30. Ferrandon D Koch I Westhof E Nusslein-Volhard C 1997 RNA-RNA interaction is required for the formation of specific bicoid mRNA 3′ UTR-STAUFEN ribonucleoprotein particles EMBO J 16 1751 1758 9130719 PMC1169778
  31. Forrest KM Gavis ER 2003 Live imaging of endogenous RNA reveals a diffusion and entrapment mechanism for nanos mRNA localization in Drosophila Curr Biol 13 1159 1168 12867026
  32. Giorgi C Moore MJ 2007 The nuclear nurture and cytoplasmic nature of localized mRNPs Semin Cell Dev Biol 18 186 193 17459736
  33. Giorgi C Yeo GW Stone ME Katz DB Burge C Turrigiano G Moore MJ 2007 The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression Cell 130 179 191 17632064
  34. Glanzer J Miyashiro KY Sul JY Barrett L Belt B Haydon P Eberwine J 2005 RNA splicing capability of live neuronal dendrites Proc Natl Acad Sci USA 102 16859 16864 16275927 PMC1277967
  35. Gonzalez I Buonomo SB Nasmyth K von Ahsen U 1999 ASH1 mRNA localization in yeast involves multiple secondary structural elements and Ash1 protein translation Curr Biol 9 337 340 10209099
  36. Gu W Pan F Zhang H Bassell GJ Singer RH 2002 A predominantly nuclear protein affecting cytoplasmic localization of beta-actin mRNA in fibroblasts and neurons J Cell Biol 156 41 51 11781334 PMC2173579
  37. Hachet O Ephrussi A 2004 Splicing of oskar RNA in the nucleus is coupled to its cytoplasmic localization Nature 428 959 963 15118729
  38. Hoek KS Kidd GJ Carson JH Smith R 1998 hnRNP A2 selectively binds the cytoplasmic transport sequence of myelin basic protein mRNA Biochemistry 37 7021 7029 9578590
  39. Huang F Chotiner JK Steward O 2007 Actin polymerization and ERK phosphorylation are required for Arc/Arg3.1 mRNA targeting to activated synaptic sites on dendrites J Neurosci 27 9054 9067 17715342 PMC6672203
  40. Januschke J Gervais L Dass S Kaltschmidt JA Lopez-Schier H St Johnston D Brand AH Roth S Guichet A 2002 Polar transport in the Drosophila oocyte requires Dynein and Kinesin I cooperation Curr Biol 12 1971 1981 12477385
  41. Jenny A Hachet O Zavorszky P Cyrklaff A Weston MD Johnston DS Erdelyi M Ephrussi A 2006 A translation-independent role of oskar RNA in early Drosophila oogenesis Development 133 2827 2833 16835436
  42. Johnstone O Lasko P 2001 Translational regulation and RNA localization in Drosophila oocytes and embryos Ann Rev Genetics 35 365 406 11700288
  43. Kanai Y Dohmae N Hirokawa N 2004 Kinesin transports RNA: isolation and characterization of an RNA-transporting granule Neuron 43 513 525 15312650
  44. Kiebler MA Bassell GJ 2006 Neuronal RNA granules: movers and makers Neuron 51 685 690 16982415
  45. Kiebler MA Hemraj I Verkade P Kohrmann M Fortes P Marion RM Ortin J Dotti CG 1999 The mammalian staufen protein localizes to the somatodendritic domain of cultured hippocampal neurons: implications for its involvement in mRNA transport J Neurosci 19 288 297 9870958 PMC6782358
  46. King ML Messitt TJ Mowry KL 2005 Putting RNAs in the right place at the right time: RNA localization in the frog oocyte Biol Cell 97 19 33 15601255
  47. Kislauskis EH Zhu X Singer RH 1994 Sequences responsible for intracellular localization of beta-actin messenger RNA also affect cell phenotype J Cell Biol 127 441 451 7929587 PMC2120214
  48. Krichevsky AM Kosik KS 2001 Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation Neuron 32 683 696 11719208
  49. Kroll TT Zhao WM Jiang C Huber PW 2002 A homolog of FBP2/KSRP binds to localized mRNAs in Xenopus oocytes Development 129 5609 5619 12421702
  50. Lange S Katayama Y Schmid M Burkacky O Brauchle C Lamb DC Jansen RP 2008 Simultaneous transport of different localized mRNA species revealed by live-cell imaging Traffic 9 1256 1267 18485054
  51. Lawrence JB Singer RH 1986 Intracellular localization of messenger RNAs for cytoskeletal proteins Cell 45 407 415 3698103
  52. Lecuyer E Yoshida H Parthasarathy N Alm C Babak T Cerovina T Hughes TR Tomancak P Krause HM 2007 Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function Cell 131 174 187 17923096
  53. Lewis RA Kress TL Cote CA Gautreau D Rokop ME Mowry KL 2004 Conserved and clustered RNA recognition sequences are a critical feature of signals directing RNA localization in Xenopus oocytes Mech Dev 121 101 109 14706704
  54. Lin AC Holt CE 2007 Local translation and directional steering in axons EMBO J 26 3729 3736 17660744 PMC1952223
  55. Long RM Gu W Meng X Gonsalvez G Singer RH Chartrand P 2001 An exclusively nuclear RNA-binding protein affects asymmetric localization of ASH1 mRNA and Ash1p in yeast J Cell Biol 153 307 318 11309412 PMC2169461
  56. Long RM Singer RH Meng X Gonzalez I Nasmyth K Jansen RP 1997 Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA Science 277 383 387 9219698
  57. Macchi P Kroening S Palacios IM Baldassa S Grunewald B Ambrosino C Goetze B Lupas A St Johnston D Kiebler M 2003 Barentsz, a new component of the Staufen-containing ribonucleoprotein particles in mammalian cells, interacts with Staufen in an RNA-dependent manner J Neurosci 23 5778 5788 12843282 PMC6741274
  58. Macdonald PM Kerr K 1997 Redundant RNA recognition events in bicoid mRNA localization RNA 3 1413 1420 9404892 PMC1369582
  59. Macdonald PM Kerr K Smith JL Leask A 1993 RNA regulatory element BLE1 directs the early steps of bicoid mRNA localization Development 118 1233 1243 8269850
  60. Macdonald PM Struhl G 1988 cis-acting sequences responsible for anterior localization of bicoid mRNA in Drosophila embryos Nature 336 595 598 3143913
  61. MacDougall N Clark A MacDougall E Davis I 2003 Drosophila gurken (TGFalpha) mRNA localizes as particles that move within the oocyte in two dynein-dependent steps Dev Cell 4 307 319 12636913
  62. Martin KC Zukin RS 2006 RNA trafficking and local protein synthesis in dendrites: an overview J Neurosci 26 7131 7134 16822966 PMC6673931
  63. Melton DA 1987 Translocation of a localized maternal mRNA to the vegetal pole of Xenopus oocytes Nature 328 80 82 3600777
  64. Messitt TJ Gagnon JA Kreiling JA Pratt CA Yoon YJ Mowry KL 2008 Multiple kinesin motors coordinate cytoplasmic RNA transport on a subpopulation of microtubules in Xenopus oocytes Dev Cell 15 426 436 18771961 PMC2581415
  65. Miller S Yasuda M Coats JK Jones Y Martone ME Mayford M 2002 Disruption of dendritic translation of CaMKIIalpha impairs stabilization of synaptic plasticity and memory consolidation Neuron 36 507 519 12408852
  66. Mori Y Imaizumi K Katayama T Yoneda T Tohyama M 2000 Two cis-acting elements in the 3′ untranslated region of alpha-CaMKII regulate its dendritic targeting Nature Neurosci 3 1079 1084 11036263
  67. Mowry KL Melton DA 1992 Vegetal messenger RNA localization directed by a 340-nt RNA sequence element in Xenopus oocytes Science 255 991 994 1546297
  68. Munro TP Magee RJ Kidd GJ Carson JH Barbarese E Smith LM Smith R 1999 Mutational analysis of a heterogeneous nuclear ribonucleoprotein A2 response element for RNA trafficking J Biol Chem 274 34389 34395 10567417
  69. Pan F Huttelmaier S Singer RH Gu W 2007 ZBP2 facilitates binding of ZBP1 to beta-actin mRNA during transcription Mol Cell Biol 27 8340 8351 17893325 PMC2169170
  70. Paquin N Chartrand P 2008 Local regulation of mRNA translation: new insights from the bud Trends Cell Biol 18 105 111 18262421
  71. Puthanveettil SV Monje FJ Miniaci MC Choi YB Karl KA Khandros E Gawinowicz MA Sheetz MP Kandel ER 2008 A new component in synaptic plasticity: upregulation of kinesin in the neurons of the gill-withdrawal reflex Cell 135 960 973 19041756 PMC2635114
  72. Rabani M Kertesz M Segal E 2008 Computational prediction of RNA structural motifs involved in posttranscriptional regulatory processes Proc Natl Acad Sci USA 105 14885 14890 18815376 PMC2567462
  73. Reck-Peterson SL Tyska MJ Novick PJ Mooseker MS 2001 The yeast class V myosins, Myo2p and Myo4p, are nonprocessive actin-based motors J Cell Biol 153 1121 1126 11381095 PMC2174330
  74. Rehbein M Kindler S Horke S Richter D 2000 Two trans-acting rat-brain proteins, MARTA1 and MARTA2, interact specifically with the dendritic targeting element in MAP2 mRNAs Brain Res 79 192 201 10925159
  75. Roegiers F Jan YN 2000 Staufen: a common component of mRNA transport in oocytes and neurons? Trends Cell Biol 10 220 224 10802537
  76. Ross AF Oleynikov Y Kislauskis EH Taneja KL Singer RH 1997 Characterization of a beta-actin mRNA zipcode-binding protein Mol Cell Biol 17 2158 2165 9121465 PMC232064
  77. Rusten TE Stenmark H 2007 Developmental biology: moonlighting at the pole Nature 445 497 499 17268460
  78. Schmid M Jaedicke A Du TG Jansen RP 2006 Coordination of endoplasmic reticulum and mRNA localization to the yeast bud Curr Biol 16 1538 1543 16890529
  79. Shan J Munro TP Barbarese E Carson JH Smith R 2003 A molecular mechanism for mRNA trafficking in neuronal dendrites J Neurosci 23 8859 8866 14523087 PMC6740403
  80. Smith R 2004 Moving molecules: mRNA trafficking in Mammalian oligodendrocytes and neurons Neuroscientist 10 495 500 15534035
  81. Sossin WS DesGroseillers L 2006 Intracellular trafficking of RNA in neurons Traffic 7 1581 1589 17054760
  82. St Johnston D Beuchle D Nusslein-Volhard C 1991 Staufen, a gene required to localize maternal RNAs in the Drosophila egg Cell 66 51 63 1712672
  83. St Johnston D Brown NH Gall JG Jantsch M 1992 A conserved double-stranded RNA-binding domain Proc Natl Acad Sci USA 89 10979 10983 1438302 PMC50466
  84. Takizawa PA Sil A Swedlow JR Herskowitz I Vale RD 1997 Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast Nature 389 90 93 9288973
  85. Tang SJ Meulemans D Vazquez L Colaco N Schuman E 2001 A role for a rat homolog of staufen in the transport of RNA to neuronal dendrites Neuron 32 463 475 11709157
  86. Tiruchinapalli DM Oleynikov Y Kelic S Shenoy SM Hartley A Stanton PK Singer RH Bassell GJ 2003 Activity-dependent trafficking and dynamic localization of zipcode binding protein 1 and beta-actin mRNA in dendrites and spines of hippocampal neurons J Neurosci 23 3251 3261 12716932 PMC6742306
  87. Weil TT Forrest KM Gavis ER 2006 Localization of bicoid mRNA in late oocytes is maintained by continual active transport Dev Cell 11 251 262 16890164
  88. Weil TT Parton R Davis I Gavis ER 2008 Changes in bicoid mRNA anchoring highlight conserved mechanisms during the oocyte-to-embryo transition Curr Biol 18 1055 1061 18639459 PMC2581475
  89. Yisraeli JK Sokol S Melton DA 1990 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 Development 108 289 298 2351071
  90. Zaessinger S Busseau I Simonelig M 2006 Oskar allows nanos mRNA translation in Drosophila embryos by preventing its deadenylation by Smaug/CCR4 Development 133 4573 4583 17050620
  91. Zhang HL Eom T Oleynikov Y Shenoy SM Liebelt DA Dictenberg JB Singer RH Bassell GJ 2001 Neurotrophin-induced transport of a beta-actin mRNP complex increases beta-actin levels and stimulates growth cone motility Neuron 31 261 275 11502257
  92. Zimyanin VL Belaya K Pecreaux J Gilchrist MJ Clark A Davis I St Johnston D 2008 In vivo imaging of oskar mRNA transport reveals the mechanism of posterior localization Cell 134 843 853 18775316 PMC2585615

Cited by

Sorted by citations

Authors
Martin, K. C., & Ephrussi, A.
Affiliations
  • University of California, Los Angeles (US)
  • European Molecular Biology Laboratory (DE)
Corresponding author
  • Martin, Kelsey C.
  • Ephrussi, Anne
Venue
Cell
Publisher
Elsevier BV
Published
2009-02
Volume
136
Issue
4
Pages
719-730
ISSN
0092-8674 (ISSN-L)
OpenAlex
W1970827552
Cited by
1,048
References
0
Citations by year
2026: 36 · 2025: 39 · 2024: 55 · 2023: 66 · 2022: 40 · 2021: 83 · 2020: 56 · 2019: 63 · 2018: 67 · 2017: 73 · 2016: 62 · 2015: 37 · 2014: 77 · 2013: 67 · 2012: 62
FWCI
5.86
Type
journal article
Language
en
Open access
Locations
  • Cell (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of Neurological Disorders and Stroke (R01NS045324)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Biotin and Related Studies
Keywords
mRNA localization, RNA-binding proteins, RNA granules, molecular motors, cytoskeleton, subcellular compartmentalization, spatial regulation of gene expression, mRNA transport
MeSH terms
Animals, Cytoplasm, Humans, RNA, Messenger, RNA-Binding Proteins, RNA Transport, Regulatory Sequences, Ribonucleic Acid

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review