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Cited by 470MicroRNA in disease regulationRetinal Development and DisordersRNA Research and Splicing

Characterizing Light-Regulated Retinal MicroRNAs Reveals Rapid Turnover as a Common Property of Neuronal MicroRNAs

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Krol, Jacek, Busskamp, Volker, Markiewicz, Ilona, Stadler, Michael B., Ribi, Sebastian, Richter, Jens, Duebel, Jens, Bicker, Silvia +7 more·2010·Cell
DOI 10.1016/j.cell.2010.03.039
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Abstract

Adaptation to different levels of illumination is central to the function of the retina. Here, we demonstrate that levels of the miR-183/96/182 cluster, miR-204, and miR-211 are regulated by different light levels in the mouse retina. Concentrations of these microRNAs were downregulated during dark adaptation and upregulated in light-adapted retinas, with rapid decay and increased transcription being responsible for the respective changes. We identified the voltage-dependent glutamate transporter Slc1a1 as one of the miR-183/96/182 targets in photoreceptor cells. We found that microRNAs in retinal neurons decay much faster than microRNAs in nonneuronal cells. The high turnover is also characteristic of microRNAs in hippocampal and cortical neurons, and neurons differentiated from ES cells in vitro. Blocking activity reduced turnover of microRNAs in neuronal cells while stimulation with glutamate accelerated it. Our results demonstrate that microRNA metabolism in neurons is higher than in most other cells types and linked to neuronal activity.

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  • MIR204 belongs to the group of recently characterised retinal-specific miRNAs regulating important processes in the retina including phototransduction cascade and development of RPE, neural retina, ciliary body, and lens.

    “The MIR204 belongs to the group of recently characterised retinal-specific miRNAs 20,21 regulating important processes in the retina including phototransduction cascade and development of RPE, neural retina, ciliary body, and lens.”

    From Confirmation of the <i>MIR204</i> n.37C&gt;T heterozygous variant as a cause of chorioretinal dystrophy variably associated with iris coloboma, early-onset cataracts and congenital glaucoma (2023) · cites this paper as [21]

    The Results report miR-204 expression in mouse retina, enrichment in the inner nuclear layer, and increased levels in response to light. The cited paper does not establish that miR-204 is retina-specific or that it regulates phototransduction or development of the RPE, neural retina, ciliary body, or lens. Its identified photoreceptor-cell target is attributed to the different miR-183/96/182 cluster (Discussion). (LLM, conf=0.87)

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  1. [1]1. Arora, A. ∙ McKay, G.J. ∙ Simpson, D.A.C. Prediction and verification of miRNA expression in human and rat retinas Invest. Ophthalmol. Vis. Sci. 2007; 48:3962-3967 Crossref Scopus (81) PubMed Google Scholar
  2. [2]2. Bartel, D.P. MicroRNAs: targets recognition and regulatory functions Cell. 2009; 136:215-233 Full Text Full Text (PDF) Scopus (17074) PubMed Google Scholar
  3. [3]3. Bhattacharyya, S.N. ∙ Habermacher, R. ∙ Martine, U. ... Relief of microRNA-mediated translational repression in human cells subjected to stress Cell. 2006; 125:1111-1124 Full Text Full Text (PDF) Scopus (1104) PubMed Google Scholar
  4. [5]5. Bushati, N. ∙ Cohen, S.M. MicroRNA functions Annu. Rev. Cell Dev. Biol. 2007; 23:175-205 Crossref Scopus (2558) PubMed Google Scholar
  5. [6]6. Chatterjee, S. ∙ Grosshans, H. Active turnover modulates mature microRNA activity in Caenorhabditis elegans Nature. 2009; 461:546-549 Crossref Scopus (295) PubMed Google Scholar
  6. [7]7. Cheng, H.Y. ∙ Papp, J.W. ∙ Varlamova, O. ... microRNA modulation of circadian-clock period and entrainment Neuron. 2007; 54:813-829 Full Text Full Text (PDF) Scopus (492) PubMed Google Scholar
  7. [8]8. Copenhagen, D.R. ∙ Jahr, C.E. Release of endogenous excitatory amino acids from turtle photoreceptors Nature. 1989; 341:536-539 Crossref Scopus (224) PubMed Google Scholar
  8. [9]9. Demb, J.B. Functional circuitry of visual adaptation in the retina J. Physiol. 2008; 586:4377-4384 Crossref Scopus (120) PubMed Google Scholar
  9. [10]10. Ding, X.C. ∙ Weiler, J. ∙ Grosshans, H. Regulating the regulators: mechanisms controlling the maturation of microRNAs Trends Biotechnol. 2009; 27:27-36 Full Text Full Text (PDF) Scopus (75) PubMed Google Scholar
  10. [11]11. Ebert, M.S. ∙ Neilson, J.R. ∙ Sharp, P.A. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells Nat. Methods. 2007; 4:721-726 Crossref Scopus (1818) PubMed Google Scholar
  11. [12]12. Filipowicz, W. ∙ Bhattacharyya, S.N. ∙ Sonenberg, N. Mechanism of post-transcriptional regulation by microRNAs: are the answers in sight? Nat. Rev. Genet. 2008; 9:102-114 Crossref Scopus (4420) PubMed Google Scholar
  12. [13]13. Flavell, S.W. ∙ Greenberg, M.E. Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system Annu. Rev. Neurosci. 2008; 31:563-590 Crossref Scopus (660) PubMed Google Scholar
  13. [14]14. Fu, Y. ∙ Yau, K.W. Phototransduction in mouse rods and cones Pflugers Arch. 2007; 454:805-819 Crossref Scopus (224) PubMed Google Scholar
  14. [15]15. Gaal, L. ∙ Roska, B. ∙ Picaud, S.A. ... Postsynaptic response kinetics are controlled by a glutamate transporter at cone photoreceptors J. Neurophysiol. 1998; 79:190-196 Crossref Scopus (53) PubMed Google Scholar
  15. [16]16. Gatfield, D. ∙ Le Martelot, G. ∙ Vejnar, C.E. ... Integration of microRNA miR-122 in hepatic circadian gene expression Genes Dev. 2009; 23:1313-1326 Crossref Scopus (326) PubMed Google Scholar
  16. [17]17. Hasegawa, J. ∙ Obara, T. ∙ Tanaka, K. ... High-density presynaptic transporters are required for glutamate removal from the first visual synapse Neuron. 2006; 50:63-74 Full Text Full Text (PDF) Scopus (86) PubMed Google Scholar
  17. [18]18. Hwang, H.-W. ∙ Wentzel, E.A. ∙ Mendell, J.T. A hexanucleotide element directs microRNA nuclear import Science. 2007; 315:97-100 Crossref Scopus (593) PubMed Google Scholar
  18. [19]19. Impey, S. ∙ Davare, M. ∙ Lasiek, A. ... An activity-induced microRNA controls dendritic spine formation by regulating Rac1-PAK signalling Mol. Cell. Neurosci. 2010; 43:146-156 Crossref Scopus (248) PubMed Google Scholar
  19. [20]20. Karali, M. ∙ Peluso, I. ∙ Marigo, V. ... Identification and characterization of microRNAs expressed in the mouse eye Invest. Ophthalmol. Vis. Sci. 2007; 48:509-515 Crossref Scopus (179) PubMed Google Scholar
  20. [21]21. Katoh, T. ∙ Sakaguchi, Y. ∙ Miyauchi, K. ... Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2 Genes Dev. 2009; 23:433-438 Crossref Scopus (368) PubMed Google Scholar
  21. [22]22. Kosik, K.S. The neuronal microRNA system Nat. Rev. Neurosci. 2006; 7:911-920 Crossref Scopus (705) PubMed Google Scholar
  22. [23]23. Kugler, P. ∙ Beyer, A. Expression of glutamate transporters in human and rat retina and rat optic nerve Histochem. Cell Biol. 2003; 120:199-212 Crossref Scopus (52) PubMed Google Scholar
  23. [25]25. Loscher, C.J. ∙ Hokamp, K. ∙ Kenna, P.F. ... Altered retinal microRNA expression profile in a mouse model of retinitis pigmentosa Genome Biol. 2007; 8:R248 Crossref Scopus (132) PubMed Google Scholar
  24. [26]26. Matsuda, T. ∙ Cepko, C.L. Electroporation and RNA interference in the rodent retina in vivo and in vitro Proc. Natl. Acad. Sci. USA. 2004; 101:16-22 Crossref Scopus (820) PubMed Google Scholar
  25. [27]27. Morgans, C.W. ∙ Zhang, J. ∙ Jeffrey, B.G. ... TRPM1 is required for the depolarizing light response in retinal ON-bipolar cells Proc. Natl. Acad. Sci. USA. 2009; 106:19174-19178 Crossref Scopus (251) PubMed Google Scholar
  26. [28]28. Nieoullon, A. ∙ Canolle, B. ∙ Masmejean, F. ... The neuronal excitatory amino acid transporter EAAC1/EAAT3: does it represent a major actor at the brain excitatory synapse? J. Neurochem. 2006; 98:1007-1018 Crossref Scopus (119) PubMed Google Scholar
  27. [29]29. Nudelman, A.S. ∙ DiRocco, D.P. ∙ Lambert, T.J. ... Neuronal activity rapidly induces transcription of the CREB-regulated microRNA-132, in vivo Hippocampus. 2009; 20:492-498 Google Scholar
  28. [30]30. Pugh, Jr., E.N. ∙ Nikonov, S. ∙ Lamb, T.D. Molecular mechanisms of vertebrate photoreceptor light adaptation Curr. Opin. Neurobiol. 1999; 9:410-418 Crossref Scopus (278) PubMed Google Scholar
  29. [31]31. Rajasethupathy, P. ∙ Fiumara, F. ∙ Sheridan, R. ... Characterization of small RNAs in aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB Neuron. 2009; 63:803-817 Full Text Full Text (PDF) Scopus (359) PubMed Google Scholar
  30. [32]32. Ramachandran, V. ∙ Chen, X. Degradation of microRNAs by a family of exoribonucleases in Arabidopsis Science. 2008; 321:1490-1492 Crossref Scopus (346) PubMed Google Scholar
  31. [33]33. Ryan, D.G. ∙ Oliveira-Fernandes, M. ∙ Lavker, R.M. MicroRNAs of the mammalian eye display distinct and overlapping tissue specificity Mol. Vis. 2006; 12:1175-1184 PubMed Google Scholar
  32. [34]34. Schratt, G.M. ∙ Nigh, E.A. ∙ Chen, W.G. ... BDNF regulates the translation of a selected group of mRNAs by a mammalian target of rapamycin-phosphatidylinositol 3-kinase-dependent pathway during neuronal development J. Neurosci. 2004; 24:7366-7377 Crossref Scopus (348) PubMed Google Scholar
  33. [35]35. Schratt, G. microRNAs at the synapse Nat. Rev. Neurosci. 2009; 10:842-849 Crossref Scopus (424) PubMed Google Scholar
  34. [36]36. Sethi, P. ∙ Lukiw, W.J. Micro-RNA abundance and stability in human brain: Specific alteration in Alzheimer's disease temporal lobe neocortex Neurosci. Lett. 2009; 459:100-104 Crossref Scopus (355) PubMed Google Scholar
  35. [37]37. Shen, Y. ∙ Heimel, J.A. ∙ Kamerans, M. ... A transient receptor potential-like channel mediates synaptic transmission in red bipolar cells J. Neurosci. 2009; 29:6088-6093 Crossref Scopus (179) PubMed Google Scholar
  36. [38]38. Stoppini, L. ∙ Buchs, P.A. ∙ Muller, D. A simple method for organotypic cultures of nervous tissue J. Neurosci. Methods. 1991; 37:173-182 Crossref Scopus (2624) PubMed Google Scholar
  37. [39]39. Tzingounis, A.V. ∙ Wadiche, J.I. Glutamate transporters: confining runaway excitation by shaping synaptic transmission Nat. Rev. Neurosci. 2007; 8:935-947 Crossref Scopus (426) PubMed Google Scholar
  38. [40]40. Wässle, H. Parallel processing in the mammalian retina Nat. Rev. Neurosci. 2004; 5:747-757 Crossref Scopus (903) PubMed Google Scholar
  39. [41]41. Wayman, G.A. ∙ Davare, M. ∙ Ando, H. ... An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP Proc. Natl. Acad. Sci. USA. 2008; 105:9093-9098 Crossref Scopus (489) PubMed Google Scholar
  40. [42]42. Weiler, R. ∙ Schultz, K. ∙ Pottek, M. ... Retinoic acid has light-adaptative effects on horizontal cells in the retina Proc. Natl. Acad. Sci. USA. 1998; 95:7139-7144 Crossref Scopus (51) PubMed Google Scholar
  41. [43]43. Xu, S. ∙ Witmer, P.D. ∙ Lumayag, S. ... microRNA (miRNA) transcriptome of mouse retina and identification of a sensory organ-specific miRNA cluster J. Biol. Chem. 2007; 282:25053-25066 Full Text Full Text (PDF) Scopus (429) PubMed Google Scholar Supplemental References
  42. [8]8. Billy, E., Brondani, V., Zhang, H., Müller, U., and Filipowicz, W. (2001). Specific interference with gene expression induced by long, double-stranded RNA in mouse embryonal teratocarcinoma cell lines. Proc. Natl. Acad. Sci. USA 98, 14428–14433. Google Scholar
  43. [10]10. Corbo, J.C., Myers, C.A., Lawrence, K.A., Jadhav, A.P., and Cepko, C.L. (2007). A typology of photoreceptor gene expression patterns in the mouse. Proc. Natl. Acad. Sci. USA 104, 12069–12074. Google Scholar
  44. [12]12. Holbro, N., Grunditz, A., and Oertner, T.G. (2009). Differential distribution of endoplasmic reticulum controls metabotropic signaling and plasticity at hippocampal synapses. Proc. Natl. Acad. Sci. USA 106, 15055–15060. Google Scholar
  45. [17]17. Matsuda, T., and Cepko, C.L. (2007). Controlled expression of transgenes introduced by in vivo electroporation. Proc. Natl. Acad. Sci. USA 104, 1027–1032. Google Scholar

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Authors
Krol, J., Busskamp, V., Markiewicz, I., Stadler, M. B., Ribi, S., Richter, J., Duebel, J., Bicker, S., Fehling, H. J., Schübeler, D., Oertner, T. G., Schratt, G., Bibel, M., Roska, B., & Filipowicz, W.
Affiliations
  • Friedrich Miescher Institute (CH)
  • Novartis Institutes for BioMedical Research (CH)
  • Heidelberg University (DE)
  • University Hospital Ulm (DE)
Corresponding author
  • Roska, Botond
  • Filipowicz, Witold
ORCID
Venue
Cell
Publisher
Elsevier BV
Published
2010-05
Volume
141
Issue
4
Pages
618-631
ISSN
0092-8674 (ISSN-L)
DOI
10.1016/j.cell.2010.03.039
OpenAlex
W2109505983
Cited by
470
References
6
Citations by year
2026: 5 · 2025: 13 · 2024: 18 · 2023: 22 · 2022: 16 · 2021: 30 · 2020: 28 · 2019: 30 · 2018: 23 · 2017: 29 · 2016: 34 · 2015: 40 · 2014: 48 · 2013: 43 · 2012: 44
FWCI
13.28
Type
journal article
Language
en
Open access
Licence
Locations
  • Cell (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
Keywords
light adaptation, miR-183/96/182 cluster, miR-204, miR-211, dark adaptation, photoreceptors, SLC1A1, glutamate transporters, neuronal activity, hippocampal neurons, cortical neurons, iPSC-derived neurons
MeSH terms
Animals, Dark Adaptation, Neurons, Down-Regulation, Up-Regulation, Photoreceptor Cells, Vertebrate, MicroRNAs, Excitatory Amino Acid Transporter 3, Mice, Embryonic Stem Cells, Retinal Neurons

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