Modulation of dendritic AMPA receptor mRNA trafficking by RNA splicing and editing

Nucleic Acids Research

Volumn 41, Issue 1, 2013, Pages 617-631

  La Via, Luca ^a   Bonini, Daniela ^a   Russo, Isabella ^a   Orlandi, Cesare ^a,b   Barlati, Sergio ^a   Barbon, Alessandro ^a  

^a UNIVERSITY OF BRESCIA   (Italy)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR 3; GLUTAMATE RECEPTOR 4; MESSENGER RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; EMBRYO; GENETIC TRANSCRIPTION; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; RAT; RNA EDITING; RNA SPLICING; RNA TRANSPORT;

ALTERNATIVE SPLICING; ANIMALS; CELLS, CULTURED; DENDRITES; PROTEIN ISOFORMS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RNA EDITING; RNA TRANSPORT; RNA, MESSENGER; RNA-BINDING PROTEINS;

RATTUS;

EID: 84871818894     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1223     Document Type: Article

References (60)

1. Dingledine, R., Borges, K., Bowie, D. and Traynelis, S.F. (1999) The glutamate receptor ion channels. Pharmacol. Rev., 51, 7-61.
2. Wenthold, R.J., Petralia, R.S., Blahos, J. II and Niedzielski, A.S. (1996) Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J. Neurosci., 16, 1982-1989.
3. Seeburg, P.H. and Hartner, J. (2003) Regulation of ion channel/neurotransmitter receptor function by RNA editing. Curr. Opin. Neurobiol., 13, 279-283.
4. 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.
5. 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.
6. Grosskreutz, J., Zoerner, A., Schlesinger, F., Krampfl, K., Dengler, R. and Bufler, J. (2003) Kinetic properties of human AMPA-type glutamate receptors expressed in HEK293 cells. Eur. J. Neurosci., 17, 1173-1178.
7. Koike, M., Tsukada, S., Tsuzuki, K., Kijima, H. and Ozawa, S. (2000) Regulation of kinetic properties of GluR2 AMPA receptor channels by alternative splicing. J. Neurosci., 20, 2166-2174.
8. Mosbacher, J., Schoepfer, R., Monyer, H., Burnashev, N., Seeburg, P.H. and Ruppersberg, J.P. (1994) A molecular determinant for submillisecond desensitization in glutamate receptors. Science, 266, 1059-1062.
9. Hollmann, M. and Heinemann, S. (1994) Cloned glutamate receptors. Ann. Rev. Neurosci., 17, 31-108.
10. Monyer, H., Seeburg, P.H. and Wisden, W. (1991) Glutamate-operated channels: developmentally early and mature forms arise by alternative splicing. Neuron, 6, 799-810.
11. Barbon, A. and Barlati, S. (2011) Glutamate receptor RNA editing in health and disease. Biochemistry, 76, 882-889.
12. Seeburg, P.H., Higuchi, M. and Sprengel, R. (1998) RNA editing of brain glutamate receptor channels: mechanism and physiology. Brain Res. Brain Res. Rev., 26, 217-229.
13. Orlandi, C., Barbon, A. and Barlati, S. (2012) Activity regulation of adenosine deaminases acting on RNA (ADARs). Mol. Neurobiol., 45, 61-75.
14. Boulter, J., Hollmann, M., O'Shea-Greenfield, A., Hartley, M., Deneris, E., Maron, C. and Heinemann, S. (1990) Molecular cloning and functional expression of glutamate receptor subunit genes. Science, 249, 1033-1037.
15. Krampfl, K., Schlesinger, F., Zorner, A., Kappler, M., Dengler, R. and Bufler, J. (2002) Control of kinetic properties of GluR2 flop AMPA-type channels: impact of R/G nuclear editing. Eur. J. Neurosci., 15, 51-62.
16. 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.
17. 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.
18. Penn, A.C. and Greger, I.H. (2009) Sculpting AMPA receptor formation and function by alternative RNA processing. RNA Biol., 6, 517-521.
19. Grooms, S.Y., Noh, K.M., Regis, R., Bassell, G.J., Bryan, M.K., Carroll, R.C. and Zukin, R.S. (2006) Activity bidirectionally regulates AMPA receptor mRNA abundance in dendrites of hippocampal neurons. J. Neurosci., 26, 8339-8351.
20. Doyle, M. and Kiebler, M.A. (2011) Mechanisms of dendritic mRNA transport and its role in synaptic tagging. EMBO J., 30, 3540-3552.
21. Bramham, C.R. and Wells, D.G. (2007) Dendritic mRNA: transport, translation and function. Nat. Rev. Neurosci., 8, 776-789.
22. Orlandi, C., La Via, L., Bonini, D., Mora, C., Russo, I., Barbon, A. and Barlati, S. (2011) AMPA receptor regulation at the mRNA and protein level in rat primary cortical cultures. PLoS One, 6, e25350.
23. Muddashetty, R.S., Kelic, S., Gross, C., Xu, M. and Bassell, G.J. (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, 5338-5348.
24. Larsson, C., Grundberg, I., Soderberg, O. and Nilsson, M. (2010) In situ detection and genotyping of individual mRNA molecules. Nat. Methods, 7, 395-397.
25. Bagni, C., Mannucci, L., Dotti, C.G. and Amaldi, F. (2000) Chemical stimulation of synaptosomes modulates alpha-Ca2+/calmodulin-dependent protein kinase II mRNA association to polysomes. J. Neurosci., 20, RC76.
26. Dunkley, P.R., Jarvie, P.E. and Robinson, P.J. (2008) A rapid Percoll gradient procedure for preparation of synaptosomes. Nat. Protoc., 3, 1718-1728.
27. Kiebler, M.A., Lopez-Garcia, J.C. and Leopold, P.L. (1999) Purification and characterization of rat hippocampal CA3-dendritic spines associated with mossy fiber terminals. FEBS Lett., 445, 80-86.
28. Barbon, A., Vallini, I., La Via, L., Marchina, E. and Barlati, S. (2003) Glutamate receptor RNA editing: a molecular analysis of GluR2, GluR5 and GluR6 in human brain tissues and in NT2 cells following in vitro neural differentiation. Brain Res., 117, 168-178.
29. Barbon, A., Fumagalli, F., La Via, L., Caracciolo, L., Racagni, G., Riva, M.A. and Barlati, S. (2007) Chronic phencyclidine administration reduces the expression and editing of specific glutamate receptors in rat prefrontal cortex. Exp. Neurol., 208, 54-62.
30. Barbon, A., Fumagalli, F., Caracciolo, L., Madaschi, L., Lesma, E., Mora, C., Carelli, S., Slotkin, T.A., Racagni, G., Di Giulio, A.M. et al. (2010) Acute spinal cord injury persistently reduces R/G RNA editing of AMPA receptors. J. Neurochem., 114, 397-407.
31. Barbon, A., Caracciolo, L., Orlandi, C., Musazzi, L., Mallei, A., La Via, L., Bonini, D., Mora, C., Tardito, D., Gennarelli, M. et al. (2011) Chronic antidepressant treatments induce a time-dependent up-regulation of AMPA receptor subunit protein levels. Neurochem. Int., 59, 896-905.
32. Blichenberg, A., Schwanke, B., Rehbein, M., Garner, C.C., Richter, D. and Kindler, S. (1999) Identification of a cis-acting dendritic targeting element in MAP2 mRNAs. J. Neurosci., 19, 8818-8829.
33. Wheeler, D.G. and Cooper, E. (2001) Depolarization strongly induces human cytomegalovirus major immediate-early promoter/enhancer activity in neurons. J. Biol. Chem., 276, 31978-31985.
34. Huang, Y.S., Kan, M.C., Lin, C.L. and Richter, J.D. (2006) CPEB3 and CPEB4 in neurons: analysis of RNA-binding specificity and translational control of AMPA receptor GluR2 mRNA. EMBO J., 25, 4865-4876.
35. Pavlopoulos, E., Trifilieff, P., Chevaleyre, V., Fioriti, L., Zairis, S., Pagano, A., Malleret, G. and Kandel, E.R. (2011) Neuralized1 activates CPEB3: a function for nonproteolytic ubiquitin in synaptic plasticity and memory storage. Cell, 147, 1369-1383.
36. Trotter, J., Karram, K. and Nishiyama, A. (2010) NG2 cells: properties, progeny and origin. Brain Res. Rev., 63, 72-82.
37. Bergles, D.E., Jabs, R. and Steinhauser, C. (2010) Neuron-glia synapses in the brain. Brain Res. Rev., 63, 130-137.
38. Stegmuller, J., Werner, H., Nave, K.A. and Trotter, J. (2003) The proteoglycan NG2 is complexed with alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid (AMPA) receptors by the PDZ glutamate receptor interaction protein (GRIP) in glial progenitor cells. Implications for glial-neuronal signaling. J. Biol. Chem., 278, 3590-3598.
39. Poon, M.M., Choi, S.H., Jamieson, C.A., Geschwind, D.H. and Martin, K.C. (2006) Identification of process-localized mRNAs from cultured rodent hippocampal neurons. J. Neurosci., 26, 13390-13399.
40. 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. and Dingledine, R. (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev., 62, 405-496.
41. Miyashiro, K., Dichter, M. and Eberwine, J. (1994) On the nature and differential distribution of mRNAs in hippocampal neurites: implications for neuronal functioning. Proc. Natl Acad. Sci. USA, 91, 10800-10804.
42. Ju, W., Morishita, W., Tsui, J., Gaietta, G., Deerinck, T.J., Adams, S.R., Garner, C.C., Tsien, R.Y., Ellisman, M.H. and Malenka, R.C. (2004) Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors. Nat. Neurosci., 7, 244-253.
43. Aoto, J., Nam, C.I., Poon, M.M., Ting, P. and Chen, L. (2008) Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity. Neuron, 60, 308-320.
44. Maghsoodi, B., Poon, M.M., Nam, C.I., Aoto, J., Ting, P. and Chen, L. (2008) Retinoic acid regulates RARalpha-mediated control of translation in dendritic RNA granules during homeostatic synaptic plasticity. Proc. Natl Acad. Sci. USA, 105, 16015-16020.
45. Smith, W.B., Starck, S.R., Roberts, R.W. and Schuman, E.M. (2005) Dopaminergic stimulation of local protein synthesis enhances surface expression of GluR1 and synaptic transmission in hippocampal neurons. Neuron, 45, 765-779.
46. Cajigas, I.J., Tushev, G., Will, T.J., tom Dieck, S., Fuerst, N. and Schuman, E.M. (2012) The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. Neuron, 74, 453-466.
47. Soden, M.E. and Chen, L. (2010) Fragile X protein FMRP is required for homeostatic plasticity and regulation of synaptic strength by retinoic acid. J. Neurosci., 30, 16910-16921.
48. Schutt, J., Falley, K., Richter, D., Kreienkamp, H.J. and Kindler, S. (2009) Fragile X mental retardation protein regulates the levels of scaffold proteins and glutamate receptors in postsynaptic densities. J. Biol. Chem., 284, 25479-25487.
49. Mori, Y., Imaizumi, K., Katayama, T., Yoneda, T. and Tohyama, M. (2000) Two cis-acting elements in the 3′ untranslated region of alpha-CaMKII regulate its dendritic targeting. Nat. Neurosci., 3, 1079-1084.
50. Blichenberg, A., Rehbein, M., Muller, R., Garner, C.C., Richter, D. and 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.
51. Steward, O., Wallace, C.S., Lyford, G.L. and Worley, P.F. (1998) Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron, 21, 741-751.
52. Andreassi, C. and Riccio, A. (2009) To localize or not to localize: mRNA fate is in 3'UTR ends. Trends Cell Biol., 19, 465-474.
53. Prakash, N., Fehr, S., Mohr, E. and Richter, D. (1997) Dendritic localization of rat vasopressin mRNA: ultrastructural analysis and mapping of targeting elements. Eur. J. Neurosci., 9, 523-532.
54. Chiaruttini, C., Vicario, A., Li, Z., Baj, G., Braiuca, P., Wu, Y., Lee, F.S., Gardossi, L., Baraban, J.M. and Tongiorgi, E. (2009) Dendritic trafficking of BDNF mRNA is mediated by translin and blocked by the G196A (Val66Met) mutation. Proc. Natl Acad. Sci. USA, 106, 16481-16486.
55. Baj, G., Leone, E., Chao, M.V. and Tongiorgi, E. (2011) Spatial segregation of BDNF transcripts enables BDNF to differentially shape distinct dendritic compartments. Proc. Natl Acad. Sci. USA, 108, 16813-16818.
56. Bhogal, B., Jepson, J.E., Savva, Y.A., Pepper, A.S., Reenan, R.A. and Jongens, T.A. (2011) Modulation of dADAR-dependent RNA editing by the Drosophila fragile X mental retardation protein. Nat. Neurosci., 14, 1517-1524.
57. Bassell, G.J. (2011) Fragile balance: RNA editing tunes the synapse. Nat. Neurosci., 14, 1492-1494.
58. Mueller, O., Hahnenberger, K., Dittmann, M., Yee, H., Dubrow, R., Nagle, R. and Ilsley, D. (2000) A microfluidic system for high-speed reproducible DNA sizing and quantitation. Electrophoresis, 21, 128-134.
59. Barbon, A., Popoli, M., La Via, L., Moraschi, S., Vallini, I., Tardito, D., Tiraboschi, E., Musazzi, L., Giambelli, R., Gennarelli, M. et al. (2006) Regulation of editing and expression of glutamate alpha-amino-propionic-acid (AMPA)/kainate receptors by antidepressant drugs. Biol. Psychiatry, 59, 713-720.
60. Barbon, A., Orlandi, C., La Via, L., Caracciolo, L., Tardito, D., Musazzi, L., Mallei, A., Gennarelli, M., Racagni, G., Popoli, M. et al. (2011) Antidepressant treatments change 5-HT2C receptor mRNA expression in rat prefrontal/frontal cortex and hippocampus. Neuropsychobiology, 63, 160-168.