RBFOX3/NeuN is Required for Hippocampal Circuit Balance and Function

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Wang, Han Ying ^a   Hsieh, Pei Fen ^a   Huang, De Fong ^a   Chin, Pey Shyuan ^a   Chou, Chih Hsuan ^a   Tung, Chun Che ^a   Chen, Shin Yuan ^a   Lee, Li Jen ^a   Gau, Susan Shur Fen ^a,b,c   Huang, Hsien Sung ^a,b,c  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVITY REGULATED CYTOSKELETAL-ASSOCIATED PROTEIN; CYTOSKELETON PROTEIN; EARLY GROWTH RESPONSE FACTOR; EGR4 PROTEIN, MOUSE; NERVE PROTEIN; NEUN PROTEIN, MOUSE; NUCLEAR PROTEIN;

ANIMAL; ANXIETY; BIOSYNTHESIS; COGNITIVE DEFECT; DISEASE MODEL; EPILEPSY; GENETICS; HIPPOCAMPUS; HUMAN; KNOCKOUT MOUSE; METABOLISM; MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; SYNAPTIC TRANSMISSION;

ANIMALS; ANXIETY; COGNITION DISORDERS; CYTOSKELETAL PROTEINS; DISEASE MODELS, ANIMAL; EARLY GROWTH RESPONSE TRANSCRIPTION FACTORS; EPILEPSY; HIPPOCAMPUS; HUMANS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; SYNAPTIC TRANSMISSION;

EID: 84948953340     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep17383     Document Type: Article

References (46)

1. Duan, W. et al. Novel Insights into NeuN: from Neuronal Marker to Splicing Regulator. Mol Neurobiol, doi: 10.1007/s12035-015-9122-5 (2015).
2. Maxeiner, S., Glassmann, A., Kao, H. T. & Schilling, K. The molecular basis of the specificity and cross-reactivity of the NeuN epitope of the neuron-specific splicing regulator, Rbfox3. Histochem Cell Biol 141, 43-55, doi: 10.1007/s00418-013-1159-9 (2014).
3. Mullen, R. J., Buck, C. R. & Smith, A. M. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116, 201-211 (1992).
4. Kim, K. K., Adelstein, R. S. & Kawamoto, S. Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors. J Biol Chem 284, 31052-31061, doi: 10.1074/jbc.M109.052969 (2009).
5. Dredge, B. K. & Jensen, K. B. NeuN/Rbfox3 nuclear and cytoplasmic isoforms differentially regulate alternative splicing and nonsense-mediated decay of Rbfox2. PLoS One 6, e21585, doi: 10.1371/journal.pone.0021585 (2011).
6. Gehman, L. T. et al. The splicing regulator Rbfox1 (A2BP1) controls neuronal excitation in the mammalian brain. Nat Genet 43, 706-711, doi: 10.1038/ng.841 (2011).
7. Gehman, L. T. et al. The splicing regulator Rbfox2 is required for both cerebellar development and mature motor function. Genes Dev 26, 445-460, doi: 10.1101/gad.182477.111 (2012).
8. Kim, K. K., Nam, J., Mukouyama, Y. S. & Kawamoto, S. Rbfox3-regulated alternative splicing of Numb promotes neuronal differentiation during development. J Cell Biol 200, 443-458, doi: 10.1083/jcb.201206146 (2013).
9. Utami, K. H. et al. Detection of chromosomal breakpoints in patients with developmental delay and speech disorders. PLoS One 9, e90852, doi: 10.1371/journal.pone.0090852 (2014).
10. Cooper, G. M. et al. A copy number variation morbidity map of developmental delay. Nat Genet 43, 838-846, doi: 10.1038/ng.909 (2011).
11. Lal, D. et al. RBFOX1 and RBFOX3 mutations in rolandic epilepsy. PLoS One 8, e73323, doi: 10.1371/journal.pone.0073323 (2013).
12. Lucas, C. H., Calvez, M., Babu, R. & Brown, A. Altered subcellular localization of the NeuN/Rbfox3 RNA splicing factor in HIVassociated neurocognitive disorders (HAND). Neurosci Lett 558, 97-102, doi: 10.1016/j.neulet.2013.10.037 (2014).
13. Zhao, C., Deng, W. & Gage, F. H. Mechanisms and functional implications of adult neurogenesis. Cell 132, 645-660, doi: 10.1016/j.cell.2008.01.033 (2008).
14. Kheirbek, M. A. et al. Differential control of learning and anxiety along the dorsoventral axis of the dentate gyrus. Neuron 77, 955-968, doi: 10.1016/j.neuron.2012.12.038 (2013).
15. Aimone, J. B. et al. Regulation and function of adult neurogenesis: from genes to cognition. Physiol Rev 94, 991-1026, doi: 10.1152/physrev.00004.2014 (2014).
16. Tannenholz, L., Jimenez, J. C. & Kheirbek, M. A. Local and regional heterogeneity underlying hippocampal modulation of cognition and mood. Front Behav Neurosci 8, 147, doi: 10.3389/fnbeh.2014.00147 (2014).
17. Brenner, R. et al. BK channel beta4 subunit reduces dentate gyrus excitability and protects against temporal lobe seizures. Nat Neurosci 8, 1752-1759, doi: 10.1038/nn1573 (2005).
18. Pallud, J. et al. Dentate gyrus and hilus transection blocks seizure propagation and granule cell dispersion in a mouse model for mesial temporal lobe epilepsy. Hippocampus 21, 334-343, doi: 10.1002/hipo.20795 (2011).
19. Perrot, R., Lonchampt, P., Peterson, A. C. & Eyer, J. Axonal neurofilaments control multiple fiber properties but do not influence structure or spacing of nodes of Ranvier. J Neurosci 27, 9573-9584, doi: 10.1523/JNEUROSCI.1224-07.2007 (2007).
20. Perrot, R., Berges, R., Bocquet, A. & Eyer, J. Review of the multiple aspects of neurofilament functions, and their possible contribution to neurodegeneration. Mol Neurobiol 38, 27-65, doi: 10.1007/s12035-008-8033-0 (2008).
21. Sloviter, R. S., Bumanglag, A. V., Schwarcz, R. & Frotscher, M. In Jasper's Basic Mechanisms of the Epilepsies (eds J. L. Noebels et al.) (2012).
22. Holmes, G. L. & Thompson, J. L. Effects of kainic acid on seizure susceptibility in the developing brain. Brain Res 467, 51-59 (1988).
23. Tang, Y. P. et al. Genetic enhancement of learning and memory in mice. Nature 401, 63-69, doi: 10.1038/43432 (1999).
24. Deacon, R. M. & Rawlins, J. N. Hippocampal lesions, species-typical behaviours and anxiety in mice. Behav Brain Res 156, 241-249, doi: 10.1016/j.bbr.2004.05.027 (2005).
25. Korb, E. & Finkbeiner, S. Arc in synaptic plasticity: from gene to behavior. Trends Neurosci 34, 591-598, doi: 10.1016/j. tins.2011.08.007 (2011).
26. Uvarov, P., Ludwig, A., Markkanen, M., Rivera, C. & Airaksinen, M. S. Upregulation of the neuron-specific K+/Cl-cotransporter expression by transcription factor early growth response 4. J Neurosci 26, 13463-13473, doi: 10.1523/JNEUROSCI.4731-06.2006 (2006).
27. Li, L., Carter, J., Gao, X., Whitehead, J. & Tourtellotte, W. G. The neuroplasticity-associated arc gene is a direct transcriptional target of early growth response (Egr) transcription factors. Mol Cell Biol 25, 10286-10300, doi: 10.1128/MCB.25.23.10286-10300.2005 (2005).
28. Ludwig, A. et al. Neurturin evokes MAPK-dependent upregulation of Egr4 and KCC2 in developing neurons. Neural Plast 2011, 1-8, doi: 10.1155/2011/641248 (2011).
29. Martin, S. J., Grimwood, P. D. & Morris, R. G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23, 649-711, doi: 10.1146/annurev.neuro.23.1.649 (2000).
30. Bliss, T. V. & Collingridge, G. L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39, doi: 10.1038/361031a0 (1993).
31. Nicholls, R. E. et al. Transgenic mice lacking NMDAR-dependent LTD exhibit deficits in behavioral flexibility. Neuron 58, 104-117, doi: 10.1016/j.neuron.2008.01.039 (2008).
32. Dong, Z. et al. Hippocampal long-term depression mediates spatial reversal learning in the Morris water maze. Neuropharmacology 64, 65-73, doi: 10.1016/j.neuropharm.2012.06.027 (2013).
33. Moser, E. I., Krobert, K. A., Moser, M. B. & Morris, R. G. Impaired spatial learning after saturation of long-term potentiation. Science 281, 2038-2042 (1998).
34. Katz, B. & Miledi, R. The role of calcium in neuromuscular facilitation. J Physiol 195, 481-492 (1968).
35. Zucker, R. S. Short-term synaptic plasticity. Annu Rev Neurosci 12, 13-31, doi: 10.1146/annurev.ne.12.030189.000305 (1989).
36. Thomson, A. M. Facilitation, augmentation and potentiation at central synapses. Trends Neurosci 23, 305-312 (2000).
37. Prange, O. & Murphy, T. H. Correlation of miniature synaptic activity and evoked release probability in cultures of cortical neurons. J Neurosci 19, 6427-6438 (1999).
38. Hsia, A. Y., Malenka, R. C. & Nicoll, R. A. Development of excitatory circuitry in the hippocampus. J Neurophysiol 79, 2013-2024 (1998).
39. Carlisle, H. J. & Kennedy, M. B. Spine architecture and synaptic plasticity. Trends Neurosci 28, 182-187, doi: 10.1016/j. tins.2005.01.008 (2005).
40. Grabowski, P. Alternative splicing takes shape during neuronal development. Curr Opin Genet Dev 21, 388-394, doi: 10.1016/j. gde.2011.03.005 (2011).
41. Bang, M. L. & Owczarek, S. A matter of balance: role of neurexin and neuroligin at the synapse. Neurochem Res 38, 1174-1189, doi: 10.1007/s11064-013-1029-9 (2013).
42. Krueger, D. D., Tuffy, L. P., Papadopoulos, T. & Brose, N. The role of neurexins and neuroligins in the formation, maturation, and function of vertebrate synapses. Curr Opin Neurobiol 22, 412-422, doi: 10.1016/j.conb.2012.02.012 (2012).
43. Varoqueaux, F. et al. Neuroligins determine synapse maturation and function. Neuron 51, 741-754, doi: 10.1016/j. neuron.2006.09.003 (2006).
44. Missler, M. et al. Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature 423, 939-948, doi: 10.1038/nature01755 (2003).
45. Racine, R. J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32, 281-294 (1972).
46. Morris, R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11, 47-60 (1984).