Activity-regulated RNA editing in select neuronal subfields in hippocampus

Nucleic Acids Research

Volumn 41, Issue 2, 2013, Pages 1124-1134

  Balik, Ales ^a,b   Penn, Andrew C ^a   Nemoda, Zsofia ^a   Greger, Ingo H ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b INSTITUTE OF PHYSIOLOGY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DEAMINASE; AMPA RECEPTOR; CALCIUM ION; RNA;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; DOWN REGULATION; EXON; GENE ACTIVITY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RNA EDITING; RNA PROCESSING;

ADENOSINE DEAMINASE; ALTERNATIVE SPLICING; ANIMALS; CA1 REGION, HIPPOCAMPAL; CELLS, CULTURED; HIPPOCAMPUS; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RNA EDITING;

METAZOA;

EID: 84875413542     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1045     Document Type: Article

References (70)

1. Bass, B.L. (2002) RNA editing by adenosine deaminases that act on RNA. Annu. Rev. Biochem., 71, 817-846. (Pubitemid 34800236)
2. Jepson, J.E. and Reenan, R.A. (2008) RNA editing in regulating gene expression in the brain. Biochim. Biophys. Acta, 1779, 459-470.
3. Hundley, H.A. and Bass, B.L. (2012) ADAR editing in double-stranded UTRs and other noncoding RNA sequences. Trends Biochem. Sci., 35, 377-383.
4. Peng, Z., Cheng, Y., Tan, B.C., Kang, L., Tian, Z., Zhu, Y., Zhang, W., Liang, Y., Hu, X., Tan, X. et al. (2012) Comprehensive analysis of RNA-Seq data reveals extensive RNA editing in a human transcriptome. Nat. Biotechnol., 30, 253-260.
5. Paul, M.S. and Bass, B.L. (1998) Inosine exists in mRNA at tissue-specific levels and is most abundant in brain mRNA. EMBO J., 17, 1120-1127. (Pubitemid 28077665)
6. Hoopengardner, B., Bhalla, T., Staber, C. and Reenan, R. (2003) Nervous system targets of RNA editing identified by comparative genomics. Science, 301, 832-836. (Pubitemid 36962624)
7. Tariq, A. and Jantsch, M.F. (2012) Transcript diversification in the nervous system: A to I RNA editing in CNS function and disease development. Front. Neurosci., 6, 99.
8. Palladino, M.J., Keegan, L.P., O'Connell, M.A. and Reenan, R.A. (2000) A-to-I pre-mRNA editing in Drosophila is primarily involved in adult nervous system function and integrity. Cell, 102, 437-449.
9. Seeburg, P.H. and Hartner, J. (2003) Regulation of ion channel/neurotransmitter receptor function by RNA editing. Curr. Opin. Neurobiol., 13, 279-283. (Pubitemid 36792239)
10. Maas, S., Kawahara, Y., Tamburro, K.M. and Nishikura, K. (2006) A-to-I RNA editing and human disease. RNA Biol., 3, 1-9.
11. Rosenthal, J.J. and Seeburg, P.H. (2012) A-to-I RNA editing: effects on proteins key to neural excitability. Neuron, 74, 432-439.
12. Traynelis, S.F., Wollmuth, L.P., McBain, C.J., Menniti, F.S., Vance, K.M., Ogden, K.K., Hansen, K.B., Yuan, H., Myers, S.J., Dingledine, R. et al. (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev., 62, 405-496.
13. Seeburg, P.H. (1996) The role of RNA editing in controlling glutamate receptor channel properties. J. Neurochem., 66, 1-5. (Pubitemid 26010757)
14. Greger, I.H., Khatri, L., Kong, X. and Ziff, E.B. (2003) AMPA receptor tetramerization is mediated by Q/R editing. Neuron, 40, 763-774. (Pubitemid 37431036)
15. Sommer, B., Kohler, M., Sprengel, R. and Seeburg, P.H. (1991) RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell, 67, 11-19. (Pubitemid 121001421)
16. Feldmeyer, D., Kask, K., Brusa, R., Kornau, H.C., Kolhekar, R., Rozov, A., Burnashev, N., Jensen, V., Hvalby, O., Sprengel, R. et al. (1999) Neurological dysfunctions in mice expressing different levels of the Q/R site-unedited AMPAR subunit GluR-B. Nat. Neurosci., 2, 57-64. (Pubitemid 30488941)
17. Lomeli, H., Mosbacher, J., Melcher, T., Hoger, T., Geiger, J.R., Kuner, T., Monyer, H., Higuchi, M., Bach, A. and Seeburg, P.H. (1994) Control of kinetic properties of AMPA receptor channels by nuclear RNA editing. Science, 266, 1709-1713.
18. Greger, I.H., Akamine, P., Khatri, L. and Ziff, E.B. (2006) Developmentally regulated, combinatorial RNA processing modulates AMPA receptor biogenesis. Neuron, 51, 85-97. (Pubitemid 43963334)
19. Li, Q., Lee, J.A. and Black, D.L. (2007) Neuronal regulation of alternative pre-mRNA splicing. Nat. Rev. Neurosci., 8, 819-831. (Pubitemid 350006218)
20. Xie, J. and Black, D.L. (2001) A CaMK IV responsive RNA element mediates depolarization-induced alternative splicing of ion channels. Nature, 410, 936-939. (Pubitemid 32335839)
21. Penn, A.C., Balik, A., Wozny, C., Cais, O. and Greger, I.H. (2012) Activity-mediated AMPA receptor remodeling, driven by alternative splicing in the ligand-binding domain. Neuron, 76, 503-510.
22. Coleman, S.K., Mö ykkynen, T., Cai, C., von Ossowski, L., Kuismanen, E., Korpi, E.R. and Keinä nen, K. (2006) Isoform-specific early trafficking of AMPA receptor flip and flop variants. J. Neurosci., 26, 11220-11229. (Pubitemid 44772209)
23. Coleman, S.K., Mö ykkynen, T., Hinkkuri, S., Vaahtera, L., Korpi, E.R., Pentikä inen, O.T. and Keinä nen, K. (2010) Ligandbinding domain determines endoplasmic reticulum exit of AMPA receptors. J. Biol Chem., 285, 36032-36039.
24. Greger, I.H., Ziff, E.B. and Penn, A.C. (2007) Molecular determinants of AMPA receptor subunit assembly. Trends Neurosci., 30, 407-416. (Pubitemid 47088718)
25. Penn, A.C., Williams, S.R. and Greger, I.H. (2008) Gating motions underlie AMPA receptor secretion from the endoplasmic reticulum. EMBO J., 27, 3056-3068.
26. Liu, Y. and Samuel, C.E. (1999) Editing of glutamate receptor subunit B pre-mRNA by splice-site variants of interferon-inducible double-stranded RNA-specific adenosine deaminase ADAR1. J. Biol. Chem., 274, 5070-5077.
27. Gahwiler, B.H. (1981) Organotypic monolayer cultures of nervous tissue. J. Neurosci. Methods, 4, 329-342. (Pubitemid 12084147)
28. Ge, B., Gurd, S., Gaudin, T., Dore, C., Lepage, P., Harmsen, E., Hudson, T.J. and Pastinen, T. (2005) Survey of allelic expression using EST mining. Genome Res., 15, 1584-1591. (Pubitemid 41545012)
29. Goodman, L.A. (1965) On simultaneous confidence intervals for multinomial proportions. Technometrics, 7, 247-254.
30. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402. (Pubitemid 27359211)
31. Birney, E., Andrews, T.D., Bevan, P., Caccamo, M., Chen, Y., Clarke, L., Coates, G., Cuff, J., Curwen, V., Cutts, T. et al. (2004) An overview of Ensembl. Genome Res., 14, 925-928. (Pubitemid 38660511)
32. Kent, W.J. (2002) BLAT-the BLAST-like alignment tool. Genome Res., 12, 656-664.
33. Venkatesh, B., Kirkness, E.F., Loh, Y.H., Halpern, A.L., Lee, A.P., Johnson, J., Dandona, N., Viswanathan, L.D., Tay, A., Venter, J.C. et al. (2007) Survey sequencing and comparative analysis of the elephant shark (Callorhinchus milii) genome. PLoS Biol., 5, e101.
34. Katoh, K., Kuma, K., Miyata, T. and Toh, H. (2005) Improvement in the accuracy of multiple sequence alignment program MAFFT. Genome Inform., 16, 22-33.
35. Hamada, M., Sato, K. and Asai, K. (2011) Improving the accuracy of predicting secondary structure for aligned RNA sequences. Nucleic Acids Res., 39, 393-402.
36. Darty, K., Denise, A. and Ponty, Y. (2009) VARNA: Interactive drawing and editing of the RNA secondary structure. Bioinformatics, 25, 1974-1975.
37. Sommer, B., Keinanen, K., Verdoorn, T.A., Wisden, W., Burnashev, N., Herb, A., Kohler, M., Takagi, T., Sakmann, B. and Seeburg, P.H. (1990) Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science, 249, 1580-1585.
38. Witter, M.P., Wouterlood, F.G., Naber, P.A. and Van Haeften, T. (2000) Anatomical organization of the parahippocampalhippocampal network. Ann. NY Acad. Sci., 911, 1-24.
39. Turrigiano, G.G. (2008) The self-tuning neuron: synaptic scaling of excitatory synapses. Cell, 135, 422-435.
40. Turrigiano, G.G., Leslie, K.R., Desai, N.S., Rutherford, L.C. and Nelson, S.B. (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature, 391, 892-896. (Pubitemid 28157666)
41. Fisahn, A., Pike, F.G., Buhl, E.H. and Paulsen, O. (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature, 394, 186-189. (Pubitemid 28325972)
42. Schoft, V.K., Schopoff, S. and Jantsch, M.F. (2007) Regulation of glutamate receptor B pre-mRNA splicing by RNA editing. Nucleic Acids Res., 35, 3723-3732. (Pubitemid 47244665)
43. Gallo, A., Keegan, L.P., Ring, G.M. and O'Connell, M.A. (2003) An ADAR that edits transcripts encoding ion channel subunits functions as a dimer. EMBO J., 22, 3421-3430. (Pubitemid 36834872)
44. Valente, L. and Nishikura, K. (2007) RNA binding-independent dimerization of adenosine deaminases acting on RNA and dominant negative effects of nonfunctional subunits on dimer functions. J. Biol. Chem., 282, 16054-16061. (Pubitemid 47100344)
45. Higuchi, M., Maas, S., Single, F.N., Hartner, J., Rozov, A., Burnashev, N., Feldmeyer, D., Sprengel, R. and Seeburg, P.H. (2000) Point mutation in an AMPA receptor gene rescues lethality in mice deficient in the RNA-editing enzyme ADAR2. Nature, 406, 78-81. (Pubitemid 30460214)
46. Wang, Q., Khillan, J., Gadue, P. and Nishikura, K. (2000) Requirement of the RNA editing deaminase ADAR1 gene for embryonic erythropoiesis. Science, 290, 1765-1768. (Pubitemid 32004807)
47. Lein, E.S., Hawrylycz, M.J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A.F., Boguski, M.S., Brockway, K.S., Byrnes, E.J. et al. (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature, 445, 168-176. (Pubitemid 46095716)
48. Feng, Y., Sansam, C.L., Singh, M. and Emeson, R.B. (2006) Altered RNA editing in mice lacking ADAR2 autoregulation. Mol. Cell. Biol., 26, 480-488. (Pubitemid 43089761)
49. Rueter, S.M., Dawson, T.R. and Emeson, R.B. (1999) Regulation of alternative splicing by RNA editing. Nature, 399, 75-80.
50. Gurevich, I., Englander, M.T., Adlersberg, M., Siegal, N.B. and Schmauss, C. (2002) Modulation of serotonin 2C receptor editing by sustained changes in serotonergic neurotransmission. J. Neurosci., 22, 10529-10532. (Pubitemid 36005126)
51. Hideyama, T., Yamashita, T., Aizawa, H., Tsuji, S., Kakita, A., Takahashi, H. and Kwak, S. (2012) Profound downregulation of the RNA editing enzyme ADAR2 in ALS spinal motor neurons. Neurobiol. Dis., 45, 1121-1128.
52. Hideyama, T., Yamashita, T., Suzuki, T., Tsuji, S., Higuchi, M., Seeburg, P.H., Takahashi, R., Misawa, H. and Kwak, S. (2010) Induced loss of ADAR2 engenders slow death of motor neurons from Q/R site-unedited GluR2. J. Neurosci., 30, 11917-11925.
53. Peng, P.L., Zhong, X., Tu, W., Soundarapandian, M.M., Molner, P., Zhu, D., Lau, L., Liu, S., Liu, F. and Lu, Y. (2006) ADAR2-dependent RNA editing of AMPA receptor subunit GluR2 determines vulnerability of neurons in forebrain ischemia. Neuron, 49, 719-733. (Pubitemid 43290131)
54. Penn, A.C., Balik, A. and Greger, I.H. (2012) Steric antisense inhibition of AMPA receptor Q/R editing reveals tight coupling to intronic editing sites and splicing. Nucleic Acids Res., 41, 1113-1123.
55. Dawson, T.R., Sansam, C.L. and Emeson, R.B. (2004) Structure and sequence determinants required for the RNA editing of ADAR2 substrates. J. Biol. Chem., 279, 4941-4951. (Pubitemid 38199090)
56. Stefl, R., Oberstrass, F.C., Hood, J.L., Jourdan, M., Zimmermann, M., Skrisovska, L., Maris, C., Peng, L., Hofr, C., Emeson, R.B. et al. (2010) The solution structure of the ADAR2 dsRBM-RNA complex reveals a sequence-specific readout of the minor groove. Cell, 143, 225-237.
57. Aruscavage, P.J. and Bass, B.L. (2000) A phylogenetic analysis reveals an unusual sequence conservation within introns involved in RNA editing. RNA, 6, 257-269. (Pubitemid 30091596)
58. Daniel, C., Veno, M.T., Ekdahl, Y., Kjems, J. and Ohman, M. (2012) A distant cis acting intronic element induces site-selective RNA editing. Nucleic Acids Res., 40, 9876-9886.
59. Stefl, R. and Allain, F.H. (2005) A novel RNA pentaloop fold involved in targeting ADAR2. RNA, 11, 592-597. (Pubitemid 40594327)
60. Lee, J.A., Xing, Y., Nguyen, D., Xie, J., Lee, C.J. and Black, D.L. (2007) Depolarization and CaM kinase IV modulate NMDA receptor splicing through two essential RNA elements. PLoS Biol., 5, e40.
61. Gainey, M.A., Hurvitz-Wolff, J.R., Lambo, M.E. and Turrigiano, G.G. (2009) Synaptic scaling requires the GluR2 subunit of the AMPA receptor. J. Neurosci., 29, 6479-6489.
62. Pozo, K. and Goda, Y. (2010) Unraveling mechanisms of homeostatic synaptic plasticity. Neuron, 66, 337-351.
63. Brorson, J.R., Li, D. and Suzuki, T. (2004) Selective expression of heteromeric AMPA receptors driven by flip-flop differences. J. Neurosci., 24, 3461-3470. (Pubitemid 38481102)
64. Toth, K. and McBain, C.J. (1998) Afferent-specific innervation of two distinct AMPA receptor subtypes on single hippocampal interneurons. Nat. Neurosci., 1, 572-578.
65. Bratt, E. and Ohman, M. (2003) Coordination of editing and splicing of glutamate receptor pre-mRNA. RNA, 9, 309-318. (Pubitemid 36246170)
66. Ryman, K., Fong, N., Bratt, E., Bentley, D.L. and Ohman, M. (2007) The C-terminal domain of RNA Pol II helps ensure that editing precedes splicing of the GluR-B transcript. RNA, 13, 1071-1078. (Pubitemid 46984897)
67. de la Mata, M., Munoz, M.J., Allo, M., Fededa, J.P., Schor, I.E. and Kornblihtt, A.R. (2011) RNA polymerase II elongation at the crossroads of transcription and alternative splicing. Genet. Res. Int., 2011, 309865.
68. Marcucci, R., Brindle, J., Paro, S., Casadio, A., Hempel, S., Morrice, N., Bisso, A., Keegan, L.P., Del Sal, G. and O'Connell, M.A. (2011) Pin1 and WWP2 regulate GluR2 Q/R site RNA editing by ADAR2 with opposing effects. EMBO J., 30, 4211-4222.
69. Sanjana, N.E., Levanon, E.Y., Hueske, E.A., Ambrose, J.M. and Li, J.B. (2012) Activity-dependent A-to-I RNA editing in rat cortical neurons. Genetics, 192, 281-287.
70. Higuchi, M., Single, F.N., Kohler, M., Sommer, B., Sprengel, R. and Seeburg, P.H. (1993) RNA editing of AMPA receptor subunit GluR-B: a base-paired intron-exon structure determines position and efficiency. Cell, 75, 1361-1370. (Pubitemid 24021910)