Single-molecule insights into mRNA dynamics in neurons

Trends in Cell Biology

Volumn 25, Issue 8, 2015, Pages 468-475

  Buxbaum, Adina R ^a,b   Yoon, Young J ^a   Singer, Robert H ^a,b   Park, Hye Yoon ^b,c  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c Seoul National University   (South Korea)

Author keywords

Local translation; mRNA tracking; RNA localization; smFISH

Indexed keywords

MESSENGER RNA;

MOLECULAR DYNAMICS; NERVE CELL; NEURITE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; REVIEW; RNA TRANSPORT; TRANSLATION REGULATION; ANIMAL; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; INTRACELLULAR MEMBRANE; NERVE CELL PLASTICITY; PHYSIOLOGY; PROCEDURES; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

ANIMALS; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; INTRACELLULAR MEMBRANES; NEURONAL PLASTICITY; NEURONS; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84937724664     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2015.05.005     Document Type: Review

References (98)

1. Hanus C., Schuman E.M. Proteostasis in complex dendrites. Nat. Rev. Neurosci. 2013, 14:638-648.
2. Holt C.E., Schuman E.M. The central dogma decentralized: new perspectives on RNA function and local translation in neurons. Neuron 2013, 80:648-657.
3. Buffington S.A., et al. Translational control in synaptic plasticity and cognitive dysfunction. Annu. Rev. Neurosci. 2014, 37:17-38.
4. Costa-Mattioli M., et al. Translational control of long-lasting synaptic plasticity and memory. Neuron 2009, 61:10-26.
5. Liu-Yesucevitz L., et al. Local RNA translation at the synapse and in disease. J. Neurosci. 2011, 31:16086-16093.
6. Casadio A., et al. A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 1999, 99:221-237.
7. Huber K.M., et al. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 2000, 288:1254-1257.
8. Kang H., Schuman E.M. A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 1996, 273:1402-1406.
9. Martin K.C., et al. Synapse-specific, long-term facilitation of Aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 1997, 91:927-938.
10. Martin K.C., et al. Local protein synthesis and its role in synapse-specific plasticity. Curr. Opin. Neurobiol. 2000, 10:587-592.
11. Hutten S., et al. Unmasking the messenger. RNA Biol. 2014, 11:992-997.
12. Buxbaum A.R., et al. In the right place at the right time: visualizing and understanding mRNA localization. Nat. Rev. Mol. Cell Biol. 2015, 16:95-109.
13. Dynes J.L., Steward O. Dynamics of bidirectional transport of Arc mRNA in neuronal dendrites. J. Comp. Neurol. 2007, 500:433-447.
14. Park H.Y., et al. Visualization of dynamics of single endogenous mRNA labeled in live mouse. Science 2014, 343:422-424.
15. Batish M., et al. Neuronal mRNAs travel singly into dendrites. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:4645-4650.
16. Farris S., et al. Selective localization of arc mRNA in dendrites involves activity- and translation-dependent mRNA degradation. J. Neurosci. 2014, 34:4481-4493.
17. Ho V.M., et al. GluA2 mRNA distribution and regulation by miR-124 in hippocampal neurons. Mol. Cell. Neurosci. 2014, 61:1-12.
18. Garner C.C., et al. Selective localization of messenger-RNA for cytoskeletal protein Map2 in dendrites. Nature 1988, 336:674-677.
19. 2+/calmodulin-dependent protein kinase in developing rat brain. J. Neurosci. 1990, 10:1788-1798.
20. Kleiman R., et al. Differential subcellular localization of particular mRNAs in hippocampal neurons in culture. Neuron 1990, 5:821-830.
21. Watson J.B., et al. G-protein gamma-7 subunit is selectively expressed in medium-sized neurons and dendrites of the rat neostriatum. J. Neurosci. Res. 1994, 39:108-116.
22. Paradies M.A., Steward O. Multiple subcellular mRNA distribution patterns in neurons: a nonisotopic in situ hybridization analysis. J. Neurobiol. 1997, 33:473-493.
23. Berry F.B., Brown I.R. CaM I mRNA is localized to apical dendrites during postnatal development of neurons in the rat brain. J. Neurosci. Res. 1996, 43:565-575.
24. Cox D.J., Racca C. Differential dendritic targeting of AMPA receptor subunit mRNAs in adult rat hippocampal principal neurons and interneurons. J. Comp. Neurol. 2013, 521:1954-2007.
25. Cajigas I.J., et al. The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. Neuron 2012, 74:453-466.
26. Lionnet T., et al. A transgenic mouse for in vivo detection of endogenous labeled mRNA. Nat. Methods 2011, 8:165-170.
27. You X., et al. Neural circular RNAs are derived from synaptic genes and regulated by development and plasticity. Nat. Neurosci. 2015, 18:603-610.
28. Ghamari-Langroudi M., et al. G-protein-independent coupling of MC4R to Kir7.1 in hypothalamic neurons. Nature 2015, 520:94-98.
29. Zhang H.Y., et al. Species differences in cannabinoid receptor 2 and receptor responses to cocaine self-administration in mice and rats. Neuropsychopharmacology 2015, 40:1037-1051.
30. Czaplinski K. Understanding mRNA trafficking: are we there yet?. Semin. Cell Dev. Biol. 2014, 32:63-70.
31. Tubing F., et al. Dendritically localized transcripts are sorted into distinct ribonucleoprotein particles that display fast directional motility along dendrites of hippocampal neurons. J. Neurosci. 2010, 30:4160-4170.
32. Doyle M., Kiebler M.A. Mechanisms of dendritic mRNA transport and its role in synaptic tagging. EMBO J. 2011, 30:3540-3552.
33. Kobayashi H., et al. Identification of a cis-acting element required for dendritic targeting of activity-regulated cytoskeleton-associated protein mRNA. Eur. J. Neurosci. 2005, 22:2977-2984.
34. Subramanian M., et al. G-quadruplex RNA structure as a signal for neurite mRNA targeting. EMBO Rep. 2011, 12:697-704.
35. Meer E.J., et al. Identification of a cis-acting element that localizes mRNA to synapses. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:4639-4644.
36. Andreassi C., Riccio A. To localize or not to localize: mRNA fate is in 3'UTR ends. Trends Cell Biol. 2009, 19:465-474.
37. Xing L., Bassell G.J. mRNA localization: an orchestration of assembly, traffic and synthesis. Traffic 2013, 14:2-14.
38. Patel V.L., et al. Spatial arrangement of an RNA zipcode identifies mRNAs under post-transcriptional control. Genes Dev. 2012, 26:43-53.
39. Kohrmann M., et al. Microtubule-dependent recruitment of Staufen-green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons. Mol. Biol. Cell 1999, 10:2945-2953.
40. Zhang H.L., et al. Neurotrophin-induced transport of a β-actin mRNP complex increases β-actin levels and stimulates growth cone motility. Neuron 2001, 31:261-275.
41. Tiruchinapalli D.M., et al. Activity-dependent trafficking and dynamic localization of zipcode binding protein 1 and β-actin mRNA in dendrites and spines of hippocampal neurons. J. Neurosci. 2003, 23:3251-3261.
42. Alami N.H., et al. Axonal transport of TDP-43 mRNA granules is impaired by ALS-causing mutations. Neuron 2014, 81:536-543.
43. Estes P.S., et al. Fragile X protein controls the efficacy of mRNA transport in Drosophila neurons. Mol. Cell. Neurosci. 2008, 39:170-179.
44. Donnelly C.J., et al. Limited availability of ZBP1 restricts axonal mRNA localization and nerve regeneration capacity. EMBO J. 2011, 30:4665-4677.
45. Bullock S.L. Translocation of mRNAs by molecular motors: think complex?. Semin. Cell Dev. Biol. 2007, 18:194-201.
46. Park H.Y., et al. Single mRNA tracking in live cells. Methods Enzymol. 2010, 472:387-406.
47. Gao Y., et al. Multiplexed dendritic targeting of alpha calcium calmodulin-dependent protein kinase II, neurogranin, and activity-regulated cytoskeleton-associated protein RNAs by the A2 pathway. Mol. Biol. Cell 2008, 19:2311-2327.
48. Tatavarty V., et al. Single-molecule imaging of translational output from individual RNA granules in neurons. Mol. Biol. Cell 2012, 23:918-929.
49. Rook M.S., et al. CaMKIIα 3' untranslated region-directed mRNA translocation in living neurons: visualization by GFP linkage. J. Neurosci. 2000, 20:6385-6393.
50. Dictenberg J.B., et al. A direct role for FMRP in activity-dependent dendritic mRNA transport links filopodial-spine morphogenesis to fragile X syndrome. Dev. Cell 2008, 14:926-939.
51. Dynes J.L., Steward O. Arc mRNA docks precisely at the base of individual dendritic spines indicating the existence of a specialized microdomain for synapse-specific mRNA translation. J. Comp. Neurol. 2012, 520:3105-3119.
52. Kao D.I., et al. Altered mRNA transport, docking, and protein translation in neurons lacking fragile X mental retardation protein. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:15601-15606.
53. Jo A., Kim H.K. Up-regulation of dendritic Kv4.2 mRNA by activation of the NMDA receptor. Neurosci. Lett. 2011, 496:129-134.
54. Oh J.Y., et al. Apolipoprotein E mRNA is transported to dendrites and may have a role in synaptic structural plasticity. J. Neurochem. 2010, 114:685-696.
55. Bi J., et al. Axonal mRNA transport and localized translational regulation of kappa-opioid receptor in primary neurons of dorsal root ganglia. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:19919-19924.
56. Bi J., et al. Copb1-facilitated axonal transport and translation of kappa opioid-receptor mRNA. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:13810-13815.
57. Ma B., et al. Huntingtin mediates dendritic transport of β-actin mRNA in rat neurons. Sci. Rep. 2011, 1:140.
58. Matsuzaki M., et al. Structural basis of long-term potentiation in single dendritic spines. Nature 2004, 429:761-766.
59. Steward O., et al. Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 1998, 21:741-751.
60. Frey S., Frey J.U. 'Synaptic tagging' and 'cross-tagging' and related associative reinforcement processes of functional plasticity as the cellular basis for memory formation. Prog. Brain Res. 2008, 169:117-143.
61. Buxbaum A.R., et al. Single β-actin mRNA detection in neurons reveals a mechanism for regulating its translatability. Science 2014, 343:419-422.
62. Newby J.M., Bressloff P.C. Quasi-steady state reduction of molecular motor-based models of directed intermittent search. Bull. Math. Biol. 2010, 72:1840-1866.
63. Newby J., Bressloff P.C. Local synaptic signaling enhances the stochastic transport of motor-driven cargo in neurons. Phys. Biol. 2010, 7:036004.
64. Ferrari F., et al. The fragile X mental retardation protein-RNP granules show an mGluR-dependent localization in the post-synaptic spines. Mol. Cell. Neurosci. 2007, 34:343-354.
65. Fujii R., et al. The RNA binding protein TLS is translocated to dendritic spines by mGluR5 activation and regulates spine morphology. Curr. Biol. 2005, 15:587-593.
66. Yoshimura A., et al. Myosin-Va facilitates the accumulation of mRNA/protein complex in dendritic spines. Curr. Biol. 2006, 16:2345-2351.
67. Nalavadi V.C., et al. Regulation of zipcode binding protein 1 transport dynamics in axons by myosin Va. J. Neurosci. 2012, 32:15133-15141.
68. Mikl M., et al. Independent localization of MAP2, CaMKIIα and β-actin RNAs in low copy numbers. EMBO Rep. 2011, 12:1077-1084.
69. An J.J., et al. Distinct role of long 3' UTR BDNF mRNA in spine morphology and synaptic plasticity in hippocampal neurons. Cell 2008, 134:175-187.
70. Will T.J., et al. Deep sequencing and high-resolution imaging reveal compartment-specific localization of Bdnf mRNA in hippocampal neurons. Sci. Signal. 2013, 6:rs16.
71. Miyashiro K., et al. On the nature and differential distribution of mRNAs in hippocampal neurites: implications for neuronal functioning. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:10800-10804.
72. Kacharmina J.E., et al. Stimulation of glutamate receptor protein synthesis and membrane insertion within isolated neuronal dendrites. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:11545-11550.
73. Ju W., et al. Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors. Nat. Neurosci. 2004, 7:244-253.
74. Grooms S.Y., et al. Activity bidirectionally regulates AMPA receptor mRNA abundance in dendrites of hippocampal neurons. J. Neurosci. 2006, 26:8339-8351.
75. Kim T.K., et al. Dendritic glutamate receptor mRNAs show contingent local hotspot-dependent translational dynamics. Cell Rep. 2013, 5:114-125.
76. Aakalu G., et al. Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 2001, 30:489-502.
77. Raab-Graham K.F., et al. Activity- and mTOR-dependent suppression of Kv1.1 channel mRNA translation in dendrites. Science 2006, 314:144-148.
78. Sutton M.A., et al. Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 2006, 125:785-799.
79. Swanger S.A., et al. Dendritic GluN2A synthesis mediates activity-induced NMDA receptor insertion. J. Neurosci. 2013, 33:8898-8908.
80. Wang D.O., et al. Synapse- and stimulus-specific local translation during long-term neuronal plasticity. Science 2009, 324:1536-1540.
81. Graber T.E., et al. Reactivation of stalled polyribosomes in synaptic plasticity. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:16205-16210.
82. Valluy J., et al. A coding-independent function of an alternative Ube3a transcript during neuronal development. Nat. Neurosci. 2015, 18:666-673.
83. Ifrim M.F., et al. Single-molecule imaging of PSD-95 mRNA translation in dendrites and its dysregulation in a mouse model of fragile X syndrome. J. Neurosci. 2015, 35:7116-7130.
84. Smith W.B., et al. Dopaminergic stimulation of local protein synthesis enhances surface expression of GluR1 and synaptic transmission in hippocampal neurons. Neuron 2005, 45:765-779.
85. Dieterich D.C., et al. In situ visualization and dynamics of newly synthesized proteins in rat hippocampal neurons. Nat. Neurosci. 2010, 13:897-905.
86. Femino A.M., et al. Visualization of single RNA transcripts in situ. Science 1998, 280:585-590.
87. Kwon S. Single-molecule fluorescence in situ hybridization: quantitative imaging of single RNA molecules. BMB Rep. 2013, 46:65-72.
88. Raj A., et al. Imaging individual mRNA molecules using multiple singly labeled probes. Nat. Methods 2008, 5:877-879.
89. Sinnamon J.R., Czaplinski K. RNA detection in situ with FISH-STICs. RNA 2014, 20:260-266.
90. Bertrand E., et al. Localization of ASH1 mRNA particles in living yeast. Mol. Cell 1998, 2:437-445.
91. Chao J.A., et al. Structural basis for the coevolution of a viral RNA-protein complex. Nat. Struct. Mol. Biol. 2008, 15:103-105.
92. Larson D.R., et al. Real-time observation of transcription initiation and elongation on an endogenous yeast gene. Science 2011, 332:475-478.
93. Hocine S., et al. Single-molecule analysis of gene expression using two-color RNA labeling in live yeast. Nat. Methods 2013, 10:119-121.
94. Zenklusen D., et al. Single-RNA counting reveals alternative modes of gene expression in yeast. Nat. Struct. Mol. Biol. 2008, 15:1263-1271.
95. Darzacq X., et al. Imaging transcription in living cells. Annu. Rev. Biophys. 2009, 38:173-196.
96. Guzowski J.F., et al. Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat. Neurosci. 1999, 2:1120-1124.
97. Guzowski J.F., et al. Recent behavioral history modifies coupling between cell activity and Arc gene transcription in hippocampal CA1 neurons. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:1077-1082.
98. Perry R.B., Fainzilber M. Local translation in neuronal processes - in vivo tests of a "heretical hypothesis". Dev. Neurobiol. 2014, 74:210-217.