3'UTRs Regulate Mouse Ntrk2 mRNA Distribution in Cortical Neurons.
3′UTR
NTRK2
Neuron
mRNA
Journal
Journal of molecular neuroscience : MN
ISSN: 1559-1166
Titre abrégé: J Mol Neurosci
Pays: United States
ID NLM: 9002991
Informations de publication
Date de publication:
Nov 2020
Nov 2020
Historique:
received:
10
03
2020
accepted:
01
05
2020
pubmed:
21
5
2020
medline:
30
7
2021
entrez:
21
5
2020
Statut:
ppublish
Résumé
There are two major isoforms of NTRK2 (neurotrophic receptor tyrosine kinase 2, or TrkB), full-length isoform with tyrosine kinase (TK) domain intact (+) and spliced isoform without tyrosine kinase domain (TK(-)). Within each isoform, there exist subtypes with minor modifications of the protein sequences. In human, the NTRK2 mRNA transcripts encoding TK(+) have same 3'UTRs, while the transcripts encoding subtypes of NTRK2 TK(-) have two completely different 3'UTRs. In mouse, the mRNA transcripts encoding same NTRK2 protein sequence for either TK(+) or TK(-) have long or short 3'UTRs, respectively. The physiological functions of these different 3'UTRs are still unknown. Pilocarpine stimulation increased Ntrk2 mRNA levels in soma, while the increase in synaptosome was smaller. FISH results further showed that mouse Ntrk2 transcripts with different 3'UTRs were distributed differently in cultured cortical neurons. The transcripts with long 3'UTR were distributed more in apical dendrites compared with transcripts with short 3'UTR. Our results provide evidence of non-coding 3'UTR function in regulating mRNA distribution in neurons.
Identifiants
pubmed: 32430868
doi: 10.1007/s12031-020-01579-8
pii: 10.1007/s12031-020-01579-8
pmc: PMC7561570
doi:
Substances chimiques
3' Untranslated Regions
0
Membrane Glycoproteins
0
RNA, Messenger
0
Ntrk2 protein, mouse
EC 2.7.10.1
Protein-Tyrosine Kinases
EC 2.7.10.1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1858-1870Subventions
Organisme : National Natural Science Foundation of China
ID : 81971425
Organisme : NINDS NIH HHS
ID : R01 NS073930
Pays : United States
Organisme : Natural Science Foundation of Zhejiang Province
ID : LZ09H090001
Organisme : Natural Science Foundation of Zhejiang Province
ID : LY20H040002
Organisme : National Natural Science Foundation of China
ID : 81871035
Références
Alexander RP, Fang G, Rozowsky J, Snyder M, Gerstein MB (2010) Annotating non-coding regions of the genome. Nat Rev Genet 11(8):559–571
pubmed: 20628352
Altar CA, Vawter MP, Ginsberg SD (2009) Target identification for CNS diseases by transcriptional profiling. Neuropsychopharmacology 34(1):18–54
pubmed: 18923405
An JJ, Gharami K, Liao GY, Woo NH, Lau AG, Vanevski F, Torre ER, Jones KR, Feng Y, Lu B, Xu B (2008) Distinct role of long 3′UTR BDNF mRNA in spine morphology and synaptic plasticity in hippocampal neurons. Cell 134(1):175–187
pubmed: 18614020
pmcid: 2527207
Andreassi C, Crerar H, Riccio A (2018) Post-transcriptional processing of mRNA in neurons: the vestiges of the RNA world drive transcriptome diversity. Front Mol Neurosci 11:304
pubmed: 30210293
pmcid: 6121099
Baj G, Leone E, Chao MV, Tongiorgi E (2011) Spatial segregation of BDNF transcripts enables BDNF to differentially shape distinct dendritic compartments. Proc Natl Acad Sci U S A 108(40):16813–16818
pubmed: 21933955
pmcid: 3189043
Bartoszewski R, Sikorski AF (2018) Editorial focus: entering into the non-coding RNA era. Cell Mol Biol Lett 23:45
pubmed: 30250489
pmcid: 6145373
Binder DK, Scharfman HE (2004) Brain-derived neurotrophic factor. Growth Factors 22(3):123–131
pubmed: 15518235
pmcid: 2504526
Bramham CR, Wells DG (2007) Dendritic mRNA: transport, translation and function. Nat Rev Neurosci 8(10):776–789
pubmed: 17848965
Chao Y, Vogel J (2016) A 3′UTR-derived small RNA provides the regulatory noncoding arm of the inner membrane stress response. Mol Cell 61(3):352–363
pubmed: 26805574
Chekulaeva M, Filipowicz W (2009) Mechanisms of miRNA-mediated post-transcriptional regulation in animal cells. Curr Opin Cell Biol 21(3):452–460
pubmed: 19450959
Cheng A, Coksaygan T, Tang H, Khatri R, Balice-Gordon RJ, Rao MS, Mattson MP (2007) Truncated tyrosine kinase B brain-derived neurotrophic factor receptor directs cortical neural stem cells to a glial cell fate by a novel signaling mechanism. J Neurochem 100(6):1515–1530
pubmed: 17286628
Ciolli Mattioli C, Rom A, Franke V, Imami K, Arrey G, Terne M, Woehler A, Akalin A, Ulitsky I, Chekulaeva M (2019) Alternative 3′UTRs direct localization of functionally diverse protein isoforms in neuronal compartments. Nucleic Acids Res 47(5):2560–2573
pubmed: 30590745
Conover JC, Erickson JT, Katz DM, Bianchi LM, Poueymirou WT, McClain J, Pan L, Helgren M, Ip NY, Boland P, Friedman B, Wiegand S, Vejsada R, Kato AC, DeChiara TM, Yancopoulos GD (1995) Neuronal deficits, not involving motor neurons, in mice lacking BDNF and/or NT4. Nature 375(6528):235–238
pubmed: 7746324
Desmet CJ, Peeper DS (2006) The neurotrophic receptor TrkB: a drug target in anti-cancer therapy? Cell Mol Life Sci 63(7–8):755–759
pubmed: 16568244
Djuranovic S, Nahvi A, Green R (2012) miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 336(6078):237–240
pubmed: 22499947
pmcid: 3971879
Dominguez D, Freese P, Alexis MS, Su A, Hochman M, Palden T, Bazile C, Lambert NJ, van Nostrand EL, Pratt GA, Yeo GW, Graveley BR, Burge CB (2018) Sequence, structure, and context preferences of human RNA binding proteins. Mol Cell 70(5):854–867 e859
pubmed: 29883606
pmcid: 6062212
Eide FF, Vining ER, Eide BL, Zang K, Wang XY, Reichardt LF (1996) Naturally occurring truncated trkB receptors have dominant inhibitory effects on brain-derived neurotrophic factor signaling. J Neurosci 16(10):3123–3129
pubmed: 8627351
pmcid: 2710135
Farooqi S, O’Rahilly S (2006) Genetics of obesity in humans. Endocr Rev 27(7):710–718
pubmed: 17122358
Fenner BM (2012) Truncated TrkB: beyond a dominant negative receptor. Cytokine Growth Factor Rev 23(1–2):15–24
pubmed: 22341689
Foltran RB, Diaz SL (2016) BDNF isoforms: a round trip ticket between neurogenesis and serotonin? J Neurochem 138(2):204–221
pubmed: 27167299
Geissler R, Grimson A (2016) A position-specific 3′UTR sequence that accelerates mRNA decay. RNA Biol 13(11):1075–1077
pubmed: 27565004
pmcid: 5100352
Haapasalo A, Koponen E, Hoppe E, Wong G, Castren E (2001) Truncated trkB.T1 is dominant negative inhibitor of trkB.TK+-mediated cell survival. Biochem Biophys Res Commun 280(5):1352–1358
pubmed: 11162678
Hogg DR, Harries LW (2014) Human genetic variation and its effect on miRNA biogenesis, activity and function. Biochem Soc Trans 42(4):1184–1189
pubmed: 25110023
Holt CE, Schuman EM (2013) The central dogma decentralized: new perspectives on RNA function and local translation in neurons. Neuron 80(3):648–657
pubmed: 24183017
pmcid: 3820025
Huang EJ, Reichardt LF (2001) Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24:677–736
pubmed: 11520916
pmcid: 2758233
Jia J, Yao P, Arif A, Fox PL (2013) Regulation and dysregulation of 3′UTR-mediated translational control. Curr Opin Genet Dev 23(1):29–34
pubmed: 23312843
pmcid: 3644486
Kang H, Welcher AA, Shelton D, Schuman EM (1997) Neurotrophins and time: different roles for TrkB signaling in hippocampal long-term potentiation. Neuron 19(3):653–664
pubmed: 9331355
Kawano M, Reynolds AA, Miranda-Rios J, Storz G (2005) Detection of 5′- and 3′-UTR-derived small RNAs and cis-encoded antisense RNAs in Escherichia coli. Nucleic Acids Res 33(3):1040–1050
pubmed: 15718303
pmcid: 549416
Klein R, Parada LF, Coulier F, Barbacid M (1989) trkB, a novel tyrosine protein kinase receptor expressed during mouse neural development. EMBO J 8(12):3701–3709
pubmed: 2555172
pmcid: 402053
Klein R, Conway D, Parada LF, Barbacid M (1990) The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell 61(4):647–656
pubmed: 2160854
Klein R, Nanduri V, Jing SA, Lamballe F, Tapley P, Bryant S et al (1991) The trkB tyrosine protein kinase is a receptor for brain-derived neurotrophic factor and neurotrophin-3. Cell 66(2):395–403
pubmed: 1649702
pmcid: 2710095
Kobayashi H, Yamamoto S, Maruo T, Murakami F (2005) Identification of a cis-acting element required for dendritic targeting of activity-regulated cytoskeleton-associated protein mRNA. Eur J Neurosci 22(12):2977–2984
pubmed: 16367764
Kocabas A, Duarte T, Kumar S, Hynes MA (2015) Widespread differential expression of coding region and 3′UTR sequences in neurons and other tissues. Neuron 88(6):1149–1156
pubmed: 26687222
Leppek K, Das R, Barna M (2018) Functional 5′UTR mRNA structures in eukaryotic translation regulation and how to find them. Nat Rev Mol Cell Biol 19(3):158–174
pubmed: 29165424
Li YX, Xu Y, Ju D, Lester HA, Davidson N, Schuman EM (1998) Expression of a dominant negative TrkB receptor, T1, reveals a requirement for presynaptic signaling in BDNF-induced synaptic potentiation in cultured hippocampal neurons. Proc Natl Acad Sci U S A 95(18):10884–10889
pubmed: 9724799
pmcid: 27990
Luberg K, Wong J, Weickert CS, Timmusk T (2010) Human TrkB gene: novel alternative transcripts, protein isoforms and expression pattern in the prefrontal cerebral cortex during postnatal development. J Neurochem 113(4):952–964
pubmed: 20193039
Marz P, Cheng JG, Gadient RA, Patterson PH, Stoyan T, Otten U, Rose-John S (1998) Sympathetic neurons can produce and respond to interleukin 6. Proc Natl Acad Sci U S A 95(6):3251–3256
pubmed: 9501249
pmcid: 19728
Medioni C, Mowry K, Besse F (2012) Principles and roles of mRNA localization in animal development. Development 139(18):3263–3276
pubmed: 22912410
pmcid: 3424039
Middleton SA, Eberwine J, Kim J (2019) Comprehensive catalog of dendritically localized mRNA isoforms from sub-cellular sequencing of single mouse neurons. BMC Biol 17(1):5
pubmed: 30678683
pmcid: 6344992
Minichiello L (2009) TrkB signalling pathways in LTP and learning. Nat Rev Neurosci 10(12):850–860
pubmed: 19927149
Miura P, Shenker S, Andreu-Agullo C, Westholm JO, Lai EC (2013) Widespread and extensive lengthening of 3′UTRs in the mammalian brain. Genome Res 23(5):812–825
pubmed: 23520388
pmcid: 3638137
Muddashetty RS, Kelic S, Gross C, Xu M, Bassell GJ (2007) Dysregulated metabotropic glutamate receptor-dependent translation of AMPA receptor and postsynaptic density-95 mRNAs at synapses in a mouse model of fragile X syndrome. J Neurosci 27(20):5338–5348
pubmed: 17507556
pmcid: 6672337
Murer MG, Yan Q, Raisman-Vozari R (2001) Brain-derived neurotrophic factor in the control human brain, and in Alzheimer’s disease and Parkinson’s disease. Prog Neurobiol 63(1):71–124
pubmed: 11040419
Numakawa T, Suzuki S, Kumamaru E, Adachi N, Richards M, Kunugi H (2010) BDNF function and intracellular signaling in neurons. Histol Histopathol 25(2):237–258
pubmed: 20017110
Oe S, Yoneda Y (2010) Cytoplasmic polyadenylation element-like sequences are involved in dendritic targeting of BDNF mRNA in hippocampal neurons. FEBS Lett 584(15):3424–3430
pubmed: 20603120
Ohira K, Kumanogoh H, Sahara Y, Homma KJ, Hirai H, Nakamura S, Hayashi M (2005) A truncated tropomyosin-related kinase B receptor, T1, regulates glial cell morphology via Rho GDP dissociation inhibitor 1. J Neurosci 25(6):1343–1353
pubmed: 15703388
pmcid: 6725989
Ohira K, Homma KJ, Hirai H, Nakamura S, Hayashi M (2006) TrkB-T1 regulates the RhoA signaling and actin cytoskeleton in glioma cells. Biochem Biophys Res Commun 342(3):867–874
pubmed: 16500620
Oktaba K, Zhang W, Lotz TS, Jun DJ, Lemke SB, Ng SP, Esposito E, Levine M, Hilgers V (2015) ELAV links paused Pol II to alternative polyadenylation in the Drosophila nervous system. Mol Cell 57(2):341–348
pubmed: 25544561
Oliva G, Sahr T, Buchrieser C (2015) Small RNAs, 5′UTR elements and RNA-binding proteins in intracellular bacteria: impact on metabolism and virulence. FEMS Microbiol Rev 39(3):331–349
pubmed: 26009640
Reichardt LF (2006) Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond Ser B Biol Sci 361(1473):1545–1564
Roberts TC, Morris KV, Wood MJ (2014) The role of long non-coding RNAs in neurodevelopment, brain function and neurological disease. Philos Trans R Soc Lond Ser B Biol Sci 369(1652):20130507
Rook MS, Lu M, Kosik KS (2000) CaMKIIalpha 3′ untranslated region-directed mRNA translocation in living neurons: visualization by GFP linkage. J Neurosci 20(17):6385–6393
pubmed: 10964944
pmcid: 6772957
Rose CR, Blum R, Pichler B, Lepier A, Kafitz KW, Konnerth A (2003) Truncated TrkB-T1 mediates neurotrophin-evoked calcium signalling in glia cells. Nature 426(6962):74–78
pubmed: 14603320
Sala C, Rudolph-Correia S, Sheng M (2000) Developmentally regulated NMDA receptor-dependent dephosphorylation of cAMP response element-binding protein (CREB) in hippocampal neurons. J Neurosci 20(10):3529–3536
pubmed: 10804193
pmcid: 6772703
Siegel GJ, Chauhan NB (2000) Neurotrophic factors in Alzheimer’s and Parkinson’s disease brain. Brain Res Brain Res Rev 33(2–3):199–227
pubmed: 11011066
Stoilov P, Castren E, Stamm S (2002) Analysis of the human TrkB gene genomic organization reveals novel TrkB isoforms, unusual gene length, and splicing mechanism. Biochem Biophys Res Commun 290(3):1054–1065
pubmed: 11798182
Taliaferro JM, Lambert NJ, Sudmant PH, Dominguez D, Merkin JJ, Alexis MS, Bazile CA, Burge CB (2016) RNA sequence context effects measured in vitro predict in vivo protein binding and regulation. Mol Cell 64(2):294–306
pubmed: 27720642
pmcid: 5107313
Tomassoni-Ardori F, Fulgenzi G, Becker J, Barrick C, Palko ME, Kuhn S, Koparde V, Cam M, Yanpallewar S, Oberdoerffer S, Tessarollo L (2019) Rbfox1 up-regulation impairs BDNF-dependent hippocampal LTP by dysregulating TrkB isoform expression levels. Elife 8
Tongiorgi E, Armellin M, Giulianini PG, Bregola G, Zucchini S, Paradiso B, Steward O, Cattaneo A, Simonato M (2004) Brain-derived neurotrophic factor mRNA and protein are targeted to discrete dendritic laminas by events that trigger epileptogenesis. J Neurosci 24(30):6842–6852
pubmed: 15282290
pmcid: 6729709
Tushev G, Glock C, Heumuller M, Biever A, Jovanovic M, Schuman EM (2018) Alternative 3′ UTRs modify the localization, regulatory potential, stability, and plasticity of mRNAs in neuronal compartments. Neuron 98(3):495–511 e496
pubmed: 29656876
Vicario A, Colliva A, Ratti A, Davidovic L, Baj G, Gricman L et al (2015) Dendritic targeting of short and long 3′ UTR BDNF mRNA is regulated by BDNF or NT-3 and distinct sets of RNA-binding proteins. Front Mol Neurosci 8:62
pubmed: 26578876
pmcid: 4624863
Yacoubian TA, Lo DC (2000) Truncated and full-length TrkB receptors regulate distinct modes of dendritic growth. Nat Neurosci 3(4):342–349
pubmed: 10725923
Yamada K, Nabeshima T (2003) Brain-derived neurotrophic factor/TrkB signaling in memory processes. J Pharmacol Sci 91(4):267–270
pubmed: 12719654
Zampetaki A, Albrecht A, Steinhofel K (2018) Long non-coding RNA structure and function: is there a link? Front Physiol 9:1201
pubmed: 30197605
pmcid: 6117379
Zhang H, Lee JY, Tian B (2005) Biased alternative polyadenylation in human tissues. Genome Biol 6(12):R100
pubmed: 16356263
pmcid: 1414089
Zhao X, Liu R, Tang H, Osei-Adjei G, Xu S, Zhang Y, Huang X (2018) A 3′ UTR-derived non-coding RNA RibS increases expression of cfa and promotes biofilm formation of Salmonella enterica serovar Typhi. Res Microbiol 169(6):279–288
pubmed: 29751065
Zuccato C, Cattaneo E (2007) Role of brain-derived neurotrophic factor in Huntington’s disease. Prog Neurobiol 81(5–6):294–330
pubmed: 17379385