Neuronal per arnt sim (PAS) domain protein 4 (NPAS4) regulates neurite outgrowth and phosphorylation of synapsin i

Journal of Biological Chemistry

Volumn 288, Issue 4, 2013, Pages 2655-2664

  Yun, Jaesuk ^a   Nagai, Taku ^a   Furukawa Hibi, Yoko ^a   Kuroda, Keisuke ^a   Kaibuchi, Kozo ^a   Greenberg, Michael E ^b   Yamada, Kiyofumi ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC HELIX LOOP HELIXES; CHROMATIN IMMUNOPRECIPITATION ASSAY; CYCLIN-DEPENDENT KINASE; EMOTIONAL BEHAVIOR; GABAERGIC; HIPPOCAMPAL NEURONS; IN-VITRO; IN-VIVO; INHIBITORY SYNAPSIS; KNOCK OUTS; MEMORY FORMATION; MRNA LEVEL; NEURITE OUTGROWTH; NEURONAL FUNCTION; OVER-EXPRESSION; PREFRONTAL CORTEX; ROSCOVITINE; SOCIAL ISOLATION; SYNAPSIN I; WILD TYPES;

CELLS; CYTOLOGY; MAMMALS; PHOSPHORYLATION; TRANSCRIPTION; TRANSCRIPTION FACTORS;

NEURONS;

CELL PROTEIN; CYCLIN DEPENDENT KINASE 5; NEURON SPECIFIC NUCLEAR PROTEIN; NEURONAL PER ARNT SIM DOMAIN PROTEIN 4; SYNAPSIN I; TUJ1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYCLIN DEPENDENT KINASE 5 GENE; EPILEPSY; GENE; GROWTH REGULATION; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NEUN GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; UPREGULATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CHROMATIN IMMUNOPRECIPITATION; CYCLIN-DEPENDENT KINASE 5; GENE EXPRESSION REGULATION; HIPPOCAMPUS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NEURITES; NEURONS; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; RNA, MESSENGER; SYNAPSINS;

EID: 84873821803     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.413310     Document Type: Article

References (47)

1. Erbel-Sieler, C., Dudley, C., Zhou, Y., Wu, X., Estill, S. J., Han, T., Diaz- Arrastia, R., Brunskill, E. W., Potter, S. S., and McKnight, S. L. (2004) Behavioral and regulatory abnormalities in mice deficient in the NPAS1 and NPAS3 transcription factors. Proc. Natl. Acad. Sci. U.S.A. 101, 13648-13653
2. Havrda, M. C., Harris, B. T., Mantani, A., Ward, N. M., Paolella, B. R., Cuzon, V. C., Yeh, H. H., and Israel, M. A. (2008) Id2 is required for specification of dopaminergic neurons during adult olfactory neurogenesis. J. Neurosci. 28, 14074-14086
3. Ide, M., Yamada, K., Toyota, T., Iwayama, Y., Ishitsuka, Y., Minabe, Y., Nakamura, K., Hattori, N., Asada, T., Mizuno, Y., Mori, N., and Yoshikawa, T. (2005) Genetic association analyses of PHOX2B and ASCL1 in neuropsychiatric disorders. Evidence for association of ASCL1 with Parkinson's disease. Hum. Genet. 117, 520-527
4. Lee, S., Lee, B., Lee, J. W., and Lee, S. K. (2009) Retinoid signaling and neurogenin2 function are coupled for the specification of spinal motor neurons through a chromatin modifier CBP. Neuron 62, 641-654
5. Pickard, B. S., Pieper, A. A., Porteous, D. J., Blackwood, D. H., and Muir, W. J. (2006) The NPAS3 gene-emerging evidence for a role in psychiatric illness. Ann. Med. 38, 439-448
6. Shimizu, N., Watanabe, H., Kubota, J., Wu, J., Saito, R., Yokoi, T., Era, T., Iwatsubo, T., Watanabe, T., Nishina, S., Azuma, N., Katada, T., and Nishina, H. (2009) Pax6-5a promotes neuronal differentiation of murine embryonic stem cells. Biol. Pharm. Bull. 32, 999-1003
7. Ooe, N., Saito, K., Mikami, N., Nakatuka, I., and Kaneko, H. (2004) Identification of a novel basic helix-loop-helix-PAS factor, NXF, reveals a Sim2 competitive, positive regulatory role in dendritic-cytoskeleton modulator drebrin gene expression. Mol. Cell. Biol. 24, 608-616
8. Zhou, Y. D., Barnard, M., Tian, H., Li, X., Ring, H. Z., Francke, U., Shelton, J., Richardson, J., Russell, D. W., and McKnight, S. L. (1997) Molecular characterization of two mammalian bHLH-PAS domain proteins selectively expressed in the central nervous system. Proc. Natl. Acad. Sci. U.S.A. 94, 713-718
9. Brunskill, E. W., Witte, D. P., Shreiner, A. B., and Potter, S. S. (1999) Characterization of npas3, a novel basic helix-loop-helix PAS gene expressed in the developing mouse nervous system. Mech. Dev. 88, 237-241
10. Pickard, B. S., Christoforou, A., Thomson, P. A., Fawkes, A., Evans, K. L., Morris, S. W., Porteous, D. J., Blackwood, D. H., and Muir, W. J. (2009) Interacting haplotypes at the NPAS3 locus alter risk of schizophrenia and bipolar disorder. Mol. Psychiatry 14, 874-884
11. Pieper, A. A., Wu, X., Han, T. W., Estill, S. J., Dang, Q., Wu, L. C., Reece- Fincanon, S., Dudley, C. A., Richardson, J. A., Brat, D. J., and McKnight, S. L. (2005) The neuronal PAS domain protein 3 transcription factor controls FGF-mediated adult hippocampal neurogenesis in mice. Proc. Natl. Acad. Sci. U.S.A. 102, 14052-14057
12. Moser, M., Knoth, R., Bode, C., and Patterson, C. (2004) LE-PAS, a novel Arnt-dependent HLH-PAS protein, is expressed in limbic tissues and transactivates the CNS midline enhancer element. Brain Res. Mol. Brain Res. 128, 141-149
13. Lin, Y., Bloodgood, B. L., Hauser, J. L., Lapan, A. D., Koon, A. C., Kim, T. K., Hu, L. S., Malik, A. N., and Greenberg, M. E. (2008) Activity-dependent regulation of inhibitory synapse development by NPAS4. Nature 455, 1198-1204
14. Ooe, N., Motonaga, K., Kobayashi, K., Saito, K., and Kaneko, H. (2009) Functional characterization of basic helix-loop-helix-PAS type transcription factor NXF in vivo. Putative involvement in an "on demand" neuroprotection system. J. Biol. Chem. 284, 1057-1063
15. Shamloo, M., Soriano, L., von Schack, D., Rickhag, M., Chin, D. J., Gonzalez- Zulueta, M., Gido, G., Urfer, R., Wieloch, T., and Nikolich, K. (2006) NPAS4, a novel helix-loop-helix PAS domain protein, is regulated in response to cerebral ischemia. Eur. J. Neurosci. 24, 2705-2720
16. Ibi, D., Takuma, K., Koike, H., Mizoguchi, H., Tsuritani, K., Kuwahara, Y., Kamei, H., Nagai, T., Yoneda, Y., Nabeshima, T., and Yamada, K. (2008) Social isolation rearing-induced impairment of the hippocampal neurogenesis is associated with deficits in spatial memory and emotion-related behaviors in juvenile mice. J. Neurochem. 105, 921-932
17. Yun, J., Koike, H., Ibi, D., Toth, E., Mizoguchi, H., Nitta, A., Yoneyama, M., Ogita, K., Yoneda, Y., Nabeshima, T., Nagai, T., and Yamada, K. (2010) Chronic restraint stress impairs neurogenesis and hippocampus-dependent fear memory in mice: possible involvement of a brain-specific transcription factor NPAS4. J. Neurochem. 114, 1840-1851
18. Ramamoorthi, K., Fropf, R., Belfort, G. M., Fitzmaurice, H. L., McKinney, R. M., Neve, R. L., Otto, T., and Lin, Y. (2011) NPAS4 regulates a transcriptional program in CA3 required for contextual memory formation. Science 334, 1669-1675
19. Ploski, J. E., Monsey, M. S., Nguyen, T., DiLeone, R. J., and Schafe, G. E. (2011) The neuronal PAS domain protein 4 (NPAS4) is required for new and reactivated fear memories. PLoS ONE 6, e23760
20. Russo, S. J., Mazei-Robison, M. S., Ables, J. L., and Nestler, E. J. (2009) Neurotrophic factors and structural plasticity in addiction. Neuropharmacology 56, 73-82
21. Dickstein, D. L., Kabaso, D., Rocher, A. B., Luebke, J. I., Wearne, S. L., and Hof, P. R. (2007) Changes in the structural complexity of the aged brain. Aging Cell 6, 275-284
22. Le Bé, J. V., and Markram, H. (2006) Spontaneous and evoked synaptic rewiring in the neonatal neocortex. Proc. Natl. Acad. Sci. U.S.A. 103, 13214-13219
23. Majewska, A. K., Newton, J. R., and Sur, M. (2006) Remodeling of synaptic structure in sensory cortical areas in vivo. J. Neurosci. 26, 3021-3029
24. Parrish, J. Z., Emoto, K., Kim, M. D., and Jan, Y. N. (2007) Mechanisms that regulate establishment, maintenance, and remodeling of dendritic fields. Annu. Rev. Neurosci. 30, 399-423
25. Pautot, S., Wyart, C., and Isacoff, E. Y. (2008) Colloid-guided assembly of oriented 3D neuronal networks. Nat. Methods 5, 735-740
26. Fath, T., Ke, Y. D., Gunning, P., Götz, J., and Ittner, L. M. (2009) Primary support cultures of hippocampal and substantia nigra neurons. Nat. Protoc. 4, 78-85
27. Wayman, G. A., Impey, S., Marks, D., Saneyoshi, T., Grant, W. F., Derkach, V., and Soderling, T. R. (2006) Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron 50, 897-909
28. Schröder, H., Becker, A., and Lössner, B. (1993) Glutamate binding to brain membranes is increased in pentylenetetrazole-kindled rats. J. Neurochem. 60, 1007-1011
29. Becker, A., and Grecksch, G. (1995) Flunarizine-its effect on pentylenetetrazole- kindled seizures and on related cognitive disturbances. Pharmacol. Biochem. Behav. 52, 765-769
30. Matsubara, M., Kusubata, M., Ishiguro, K., Uchida, T., Titani, K., and Taniguchi, H. (1996) Site-specific phosphorylation of synapsin I by mitogen- activated protein kinase and CDK5 and its effects on physiological functions. J. Biol. Chem. 271, 21108-21113
31. Levy, M., Faas, G. C., Saggau, P., Craigen, W. J., and Sweatt, J. D. (2003) Mitochondrial regulation of synaptic plasticity in the hippocampus. J. Biol. Chem. 278, 17727-17734
32. Flood, W. D., Moyer, R. W., Tsykin, A., Sutherland, G. R., and Koblar, S. A. (2004) Nxf and Fbxo33. Novel seizure-responsive genes in mice. Eur. J. Neurosci. 20, 1819-1826
33. García-Pérez, J., Avila, J., and Díaz-Nido, J. (1999) Lithium induces morphological differentiation of mouse neuroblastoma cells. J. Neurosci. Res. 57, 261-270
34. Bykhovskaia, M. (2011) Synapsin regulation of vesicle organization and functional pools. Semin. Cell Dev. Biol. 22, 387-392
35. Shupliakov, O., Haucke, V., and Pechstein, A. (2011) How synapsin I may cluster synaptic vesicles. Semin. Cell Dev. Biol. 22, 393-399
36. Fornasiero, E. F., Bonanomi, D., Benfenati, F., and Valtorta, F. (2010) The role of synapsins in neuronal development. Cell. Mol. Life Sci. 67, 1383-1396
37. Bonanomi, D., Menegon, A., Miccio, A., Ferrari, G., Corradi, A., Kao, H. T., Benfenati, F., and Valtorta, F. (2005) Phosphorylation of synapsin I by cAMP-dependent protein kinase controls synaptic vesicle dynamics in developing neurons. J. Neurosci. 25, 7299-7308
38. Kao, H. T., Song, H. J., Porton, B., Ming, G. L., Hoh, J., Abraham, M., Czernik, A. J., Pieribone, V. A., Poo, M. M., and Greengard, P. (2002) A protein kinase A-dependent molecular switch in synapsins regulates neurite outgrowth. Nat. Neurosci. 5, 431-437
39. Nikolic, M., Dudek, H., Kwon, Y. T., Ramos, Y. F., and Tsai, L. H. (1996) The cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation. Genes Dev. 10, 816-825
40. Cheung, Z. H., Chin, W. H., Chen, Y., Ng, Y. P., and Ip, N. Y. (2007) CDK5 is involved in BDNF-stimulated dendritic growth in hippocampal neurons. PLoS Biol. 5, e63
41. Cheung, Z. H., and Ip, N. Y. (2007) The roles of cyclin-dependent kinase 5 in dendrite and synapse development. Biotechnol. J. 2, 949-957
42. Wilczynski, G. M., Konopacki, F. A., Wilczek, E., Lasiecka, Z., Gorlewicz, A., Michaluk, P., Wawrzyniak, M., Malinowska, M., Okulski, P., Kolodziej, L. R., Konopka, W., Duniec, K., Mioduszewska, B., Nikolaev, E., Walczak, A., Owczarek, D., Gorecki, D. C., Zuschratter, W., Ottersen, O. P., and Kaczmarek, L. (2008) Important role of matrix metalloproteinase 9 in epileptogenesis. J. Cell Biol. 180, 1021-1035
43. Evangelopoulos, M. E., Weis, J., and Krüttgen, A. (2005) Signalling pathways leading to neuroblastoma differentiation after serum withdrawal. HDL blocks neuroblastoma differentiation by inhibition of EGFR. Oncogene 24, 3309-3318
44. Evangelopoulos, M. E., Weis, J., and Krüttgen, A. (2009) Mevastatin-induced neurite outgrowth of neuroblastoma cells via activation of EGFR. J. Neurosci. Res. 87, 2138-2144
45. Kim, T. K., Hemberg, M., Gray, J. M., Costa, A. M., Bear, D. M., Wu, J., Harmin, D. A., Laptewicz, M., Barbara-Haley, K., Kuersten, S., Markenscoff- Papadimitriou, E., Kuhl, D., Bito, H., Worley, P. F., Kreiman, G., and Greenberg, M. E. (2010) Widespread transcription at neuronal activityregulated enhancers. Nature 465, 182-187
46. Soylemezoglu, F., Onder, S., Tezel, G. G., and Berker, M. (2003) Neuronal nuclear antigen (NeuN). A new tool in the diagnosis of central neurocytoma. Pathol. Res. Pract. 199, 463-468
47. Kim, K. K., Adelstein, R. S., and Kawamoto, S. (2009) 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