NPAS3 regulates transcription and expression of VGF: Implications for neurogenesis and psychiatric disorders

Frontiers in Molecular Neuroscience

Volumn 9, Issue NOV2016, 2016, Pages

  Yang, Dongxue ^a   Zhang, Wenbo ^a   Padhiar, Arshad ^a   Yue, Yao ^a   Shi, Yonghui ^a   Zheng, Tiezheng ^a   Davis, Kaspar ^b   Zhang, Yu ^b   Huang, Min ^a   Li, Yuyuan ^a   Sha, Li ^a  

^a DALIAN MEDICAL UNIVERSITY   (China)

^b DALIAN UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

Cell proliferation; Glutamatergic signaling pathways; Neurogenesis; NPAS3; Psychiatric disorders; Transcription regulation; VGF

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BETA ACTIN; NEURONAL PAS DOMAIN PROTEIN 3; NEUROPEPTIDE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VGF NERVE GROWTH FACTOR;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DENSITOMETRY; GENE CONTROL; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; LUCIFERASE ASSAY; MENTAL DISEASE; MOLECULAR CLONING; NERVE CELL NETWORK; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; STRUCTURAL PROTEOMICS; TRANSCRIPTION REGULATION; TRANSIENT TRANSFECTION; WESTERN BLOTTING;

EID: 84995640128     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2016.00109     Document Type: Article

References (81)

1. Alder, J., Thakker-Varia, S., Bangasser, D. A., Kuroiwa, M., Plummer, M. R., Shors, T. J., et al. (2003). Brain-derived neurotrophic factor-induced gene expression reveals novel actions of VGF in hippocampal synaptic plasticity. J. Neurosci. 23, 10800-10808.
2. Aloor, R., Zhang, C., Bandyopadhyay, M., and Dasgupta, S. (2015). Impact of nuclear factor-κB on restoration of neuron growth and differentiation in hippocampus of degenerative brain. J. Neurosci. Res. 93, 1471-1475. doi: 10.1002/jnr.23547
3. Altar, C. A., Vawter, M. P., and Ginsberg, S. D. (2009). Target identification for CNS diseases by transcriptional profiling. Neuropsychopharmacology 34, 18-54. doi: 10.1038/npp.2008.172
4. Altshuler, D., and Hirschhorn, J. N. (1999). Upsetting the balance: VGF and the regulation of body weight. Neuron 23, 415-417. doi: 10.1016/S0896-6273(00)80793-X
5. Banasr, M., Soumier, A., Hery, M., Mocaër, E., and Daszuta, A. (2006). Agomelatine, a new antidepressant, induces regional changes in hippocampal neurogenesis. Biol. Psychiatry 59, 1087-1096. doi: 10.1016/j.biopsych.2005.11.025
6. Bayer, K. U., De Koninck, P., Leonard, A. S., Hell, J. W., and Schulman, H. (2001). Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature 411, 801-805. doi: 10.1038/35081080
7. Bortolotto, V., Cuccurazzu, B., Canonico, P. L., and Grilli, M. (2014). NF-κB mediated regulation of adult hippocampal neurogenesis: relevance to mood disorders and antidepressant activity. Biomed Res. Int. 2014: 612798. doi: 10.1155/2014/612798
8. Bozdagi, O., Rich, E., Tronel, S., Sadahiro, M., Patterson, K., Shapiro, M. L., et al. (2008). The neurotrophin-inducible gene Vgf regulates hippocampal function and behavior through a brain-derived neurotrophic factor-dependent mechanism. J. Neurosci. 28, 9857-9869. doi: 10.1523/JNEUROSCI.3145-08.2008
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. doi: 10.1016/s0925-4773(99)00182-3
10. Busse, S., Bernstein, H. G., Busse, M., Bielau, H., Brisch, R., Mawrin, C., et al. (2012). Reduced density of hypothalamic VGF-immunoreactive neurons in schizophrenia: a potential link to impaired growth factor signaling and energy homeostasis. Eur. Arch. Psychiatry Clin. Neurosci. 262, 365-374. doi: 10.1007/s00406-011-0282-7
11. Cattaneo, A., Sesta, A., Calabrese, F., Nielsen, G., Riva, M. A., and Gennarelli, M. (2010). The expression of VGF is reduced in leukocytes of depressed patients and it is restored by effective antidepressant treatment. Neuropsychopharmacology 35, 1423-1428. doi: 10.1038/npp.2010.11
12. Chaudhary, J., and Skinner, M. K. (1999). Basic helix-loop-helix proteins can act at the E-box within the serum response element of the c-fos promoter to influence hormone-induced promoter activation in sertoli cells. Mol. Endocrinol. 13, 774-786. doi: 10.1210/me.13.5.774
13. Cirelli, C., and Tononi, G. (2000). Gene expression in the brain across the sleep-waking cycle. Brain Res. 885, 303-321. doi: 10.1016/s0006-8993(00)03008-0
14. Conboy, L., Tanrikut, C., Zoladz, P. R., Campbell, A. M., Park, C. R., Gabriel, C., et al. (2009). The antidepressant agomelatine blocks the adverse effects of stress on memory and enables spatial learning to rapidly increase neural cell adhesion molecule (NCAM) expression in the hippocampus of rats. Int. J. Neuropsychopharmacol. 12, 329-341. doi: 10.1017/s1461145708009255
15. Crampton, S. J., and O’Keeffe, G. W. (2013). NF-κB: emerging roles in hippocampal development and function. Int. J. Biochem. Cell Biol. 45, 1821-1824. doi: 10.1016/j.biocel.2013.05.037
16. Crews, S. T., Thomas, J. B., and Goodman, C. S. (1988). The Drosophila single-minded gene encodes a nuclear protein with sequence similarity to the per gene product. Cell 52, 143-151. doi: 10.1016/0092-8674(88)90538-7
17. Czeh, B., Michaelis, T., Watanabe, T., Frahm, J., de Biurrun, G., van Kampen, M., et al. (2001). Stress-induced changes in cerebral metabolites, hippocampal volume and cell proliferation are prevented by antidepressant treatment with tianeptine. Proc. Natl. Acad. Sci. U S A 98, 12796-12801. doi: 10.1073/pnas.211427898
18. D’Arcangelo, G., Habas, R., Wang, S., Halegoua, S., and Salton, S. R. (1996). Activation of codependent transcription factors is required for transcriptional induction of the vgf gene by nerve growth factor and Ras. Mol. Cell. Biol. 16, 4621-4631. doi: 10.1128/mcb.16.9.4621
19. Duman, R. S., Heninger, G. R., and Nestler, E. J. (1997). A molecular and cellular theory of depression. Arch. Gen. Psychiatry 54, 597-606. doi: 10.1001/archpsyc.1997.01830190015002
20. Duman, R. S., Malberg, J., and Thome, J. (1999). Neural plasticity to stress and antidepressant treatment. Biol. Psychiatry 46, 1181-1191. doi: 10.1097/00008877-199908001-00070
21. Ferri, G. L., Noli, B., Brancia, C., D’Amato, F., and Cocco, C. (2011). VGF: an inducible gene product, precursor of a diverse array of neuro-endocrine peptides and tissue-specific disease biomarkers. J. Chem. Neuroanat. 42, 249-261. doi: 10.1016/j.jchemneu.2011.05.007
22. Gasparini, F., Lingenhöhl, K., Stoehr, N., Flor, P. J., Heinrich, M., Vranesic, I., et al. (1999). 2-Methyl-6-(phenylethynyl)-pyridine (MPEP), a potent, selective and systemically active mGlu5 receptor antagonist. Neuropharmacology 38, 1493-1503. doi: 10.1016/s0028-3908(99)00082-9
23. Gilles-Gonzalez, M. A., and Gonzalez, G. (2004). Signal transduction by heme-containing PAS-domain proteins. J. Appl. Physiol. 96, 774-783. doi: 10.1152/japplphysiol.00941.2003
24. Hill, A. S., Sahay, A., and Hen, R. (2015). Increasing adult hippocampal neurogenesis is sufficient to reduce anxiety and depression-like behaviors. Neuropsychopharmacology 40, 2368-2378. doi: 10.1038/npp.2015.85
25. Huang, J. T., Leweke, F. M., Oxley, D., Wang, L., Harris, N., Koethe, D., et al. (2006). Disease biomarkers in cerebrospinal fluid of patients with first-onset psychosis. PLoS Med. 3: e428. doi: 10.1371/journal.pmed.0030428
26. Huang, J., Perlis, R. H., Lee, P. H., Rush, A. J., Fava, M., Sachs, G. S., et al. (2010). Cross-disorder genomewide analysis of schizophrenia, bipolar disorder and depression. Am. J. Psychiatry 167, 1254-1263. doi: 10.1176/appi.ajp.2010.09091335
27. Hunsberger, J. G., Newton, S. S., Bennett, A. H., Duman, C. H., Russell, D. S., Salton, S. R., et al. (2007). Antidepressant actions of the exercise-regulated gene VGF. Nat. Med. 13, 1476-1482. doi: 10.1038/nm1669
28. Jethwa, P. H., Warner, A., Nilaweera, K. N., Brameld, J. M., Keyte, J. W., Carter, W. G., et al. (2007). VGF-derived peptide, TLQP-21, regulates food intake and body weight in Siberian hamsters. Endocrinology 148, 4044-4055. doi: 10.1210/en.2007-0038
29. Kalev-Zylinska, M. L., Symes, W., Young, D., and During, M. J. (2009). Knockdown and overexpression of NR1 modulates NMDA receptor function. Mol. Cell. Neurosci. 41, 383-396. doi: 10.1016/j.mcn.2009.04.003
30. Kamnasaran, D., Muir, W. J., Ferguson-Smith, M. A., and Cox, D. W. (2003). Disruption of the neuronal PAS3 gene in a family affected with schizophrenia. J. Med. Genet. 40, 325-332. doi: 10.1136/jmg.40.5.325
31. Kempermann, G., Krebs, J., and Fabel, K. (2008). The contribution of failing adult hippocampal neurogenesis to psychiatric disorders. Curr. Opin. Psychiatry 21, 290-295. doi: 10.1097/YCO.0b013e3282fad375
32. Kheirbek, M. A., Tannenholz, L., and Hen, R. (2012). NR2B-dependent plasticity of adult-born granule cells is necessary for context discrimination. J. Neurosci. 32, 8696-8702. doi: 10.1523/JNEUROSCI.1692-12.2012
33. Krock, E., Currie, J. B., Weber, M. H., Ouellet, J. A., Stone, L. S., Rosenzweig, D. H., et al. (2016). Nerve growth factor is regulated by toll-like receptor 2 in human intervertebral discs. J. Biol. Chem. 291, 3541-3551. doi: 10.1074/jbc.M115.675900
34. Krueger, D. D., Osterweil, E. K., and Bear, M. F. (2010). Activation of mGluR5 induces rapid and long-lasting protein kinase D phosphorylation in hippocampal neurons. J. Mol. Neurosci. 42, 1-8. doi: 10.1007/s12031-010-9338-9
35. Levi, A., Ferri, G. L., Watson, E., Possenti, R., and Salton, S. R. (2004). Processing, distribution and function of VGF, a neuronal and endocrine peptide precursor. Cell. Mol. Neurobiol. 24, 517-533. doi: 10.1023/b: cemn.0000023627.79947.22
36. Li, N., Lee, B., Liu, R. J., Banasr, M., Dwyer, J. M., Iwata, M., et al. (2010). mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science 329, 959-964. doi: 10.1126/science.1190287
37. Lu, Y., Wang, C., Xue, Z., Li, C., Zhang, J., Zhao, X., et al. (2014). PI3K/AKT/mTOR signaling-mediated neuropeptide VGF in the hippocampus of mice is involved in the rapid onset antidepressant-like effects of GLYX-13. Int. J. Neuropsychopharmacol. 18: pyu110. doi: 10.1093/ijnp/pyu110
38. Madsen, T. M., Newton, S. S., Eaton, M. E., Russell, D. S., and Duman, R. S. (2003). Chronic electroconvulsive seizure up-regulates β-catenin expression in rat hippocampus: role in adult neurogenesis. Biol. Psychiatry 54, 1006-1014. doi: 10.1016/s0006-3223(03)00700-5
39. Malberg, J. E., and Monteggia, L. M. (2008). VGF, a new player in antidepressant action? Sci. Signal. 1: pe19. doi: 10.1126/stke.118pe19
40. Malki, K., Pain, O., Tosto, M. G., Du Rietz, E., Carboni, L., and Schalkwyk, L. C. (2015). Identification of genes and gene pathways associated with major depressive disorder by integrative brain analysis of rat and human prefrontal cortex transcriptomes. Transl. Psychiatry 5: e519. doi: 10.1038/tp.2015.15
41. Marx, C. E., Bradford, D. W., Hamer, R. M., Naylor, J. C., Allen, T. B., Lieberman, J. A., et al. (2011). Pregnenolone as a novel therapeutic candidate in schizophrenia: emerging preclinical and clinical evidence. Neuroscience 191, 78-90. doi: 10.1016/j.neuroscience.2011.06.076
42. Meffert, M. K., Chang, J. M., Wiltgen, B. J., Fanselow, M. S., and Baltimore, D. (2003). NF-κB functions in synaptic signaling and behavior. Nat. Neurosci. 6, 1072-1078. doi: 10.1038/nn1110
43. Millan, M. J., Gobert, A., Lejeune, F., Dekeyne, A., Newman-Tancredi, A., Pasteau, V., et al. (2003). The novel melatonin agonist agomelatine (S20098) is an antagonist at 5-hydroxytryptamine2C receptors, blockade of which enhances the activity of frontocortical dopaminergic and adrenergic pathways. J. Pharmacol. Exp. Ther. 306, 954-964. doi: 10.1124/jpet.103.051797
44. Molteni, R., Calabrese, F., Pisoni, S., Gabriel, C., Mocaer, E., Racagni, G., et al. (2010). Synergistic mechanisms in the modulation of the neurotrophin BDNF in the rat prefrontal cortex following acute agomelatine administration. World J. Biol. Psychiatry 11, 148-153. doi: 10.3109/15622970903447659
45. Moriguchi, S., Shinoda, Y., Yamamoto, Y., Sasaki, Y., Miyajima, K., Tagashira, H., et al. (2013). Stimulation of the sigma-1 receptor by DHEA enhances synaptic efficacy and neurogenesis in the hippocampal dentate gyrus of olfactory bulbectomized mice. PLoS One 8: e60863. doi: 10.1371/journal.pone.0060863
46. Mostany, R., Valdizan, E. M., and Pazos, A. (2008). A role for nuclear β-catenin in SNRI antidepressant-induced hippocampal cell proliferation. Neuropharmacology 55, 18-26. doi: 10.1016/j.neuropharm.2008.04.012
47. Natarajan, K., Singh, S., Burke, T. R. Jr., Grunberger, D., and Aggarwal, B. B. (1996). Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-κB. Proc. Natl. Acad. Sci. U S A 93, 9090-9095. doi: 10.1073/pnas.93.17.9090
48. Pasinetti, G. M., Ungar, L. H., Lange, D. J., Yemul, S., Deng, H., Yuan, X., et al. (2006). Identification of potential CSF biomarkers in ALS. Neurology 66, 1218-1222. doi: 10.1212/01.WNL.0000203129.82104.07
49. Pickard, B. S., Christoforou, A., Thomson, P. A., Fawkes, A., Evans, K. L., Morris, S. W., et al. (2009). Interacting haplotypes at the NPAS3 locus alter risk of schizophrenia and bipolar disorder. Mol. Psychiatry 14, 874-884. doi: 10.1038/mp.2008.24
50. Pieper, A. A., Wu, X., Han, T. W., Estill, S. J., Dang, Q., Wu, L. C., et al. (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. doi: 10.1073/pnas.0506713102
51. Pieper, A. A., Xie, S., Capota, E., Estill, S. J., Zhong, J., Long, J. M., et al. (2010). Discovery of a proneurogenic, neuroprotective chemical. Cell 142, 39-51. doi: 10.1016/j.cell.2010.06.018
52. Pompili, M., Serafini, G., Innamorati, M., Venturini, P., Fusar-Poli, P., Sher, L., et al. (2013). Agomelatine, a novel intriguing antidepressant option enhancing neuroplasticity: a critical review. World J. Biol. Psychiatry 14, 412-431. doi: 10.3109/15622975.2013.765593
53. Possenti, R., Di Rocco, G., Nasi, S., and Levi, A. (1992). Regulatory elements in the promoter region of vgf, a nerve growth factor-inducible gene. Proc. Natl. Acad. Sci. U S A 89, 3815-3819. doi: 10.1073/pnas.89.9.3815
54. Ramos, A., Rodriguez-Seoane, C., Rosa, I., Trossbach, S. V., Ortega-Alonso, A., Tomppo, L., et al. (2014). Neuropeptide precursor VGF is genetically associated with social anhedonia and underrepresented in the brain of major mental illness: its downregulation by DISC1. Hum. Mol. Genet. 23, 5859-5865. doi: 10.1093/hmg/ddu303
55. Reif, A., Fritzen, S., Finger, M., Strobel, A., Lauer, M., Schmitt, A., et al. (2006). Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol. Psychiatry 11, 514-522. doi: 10.1038/sj.mp.4001791
56. Ren, J., Li, X., Zhang, X., Li, M., Wang, Y., and Ma, Y. (2013). The effects of intra-hippocampal microinfusion of D-cycloserine on fear extinction and the expression of NMDA receptor subunit NR2B and neurogenesis in the hippocampus in rats. Prog. Neuropsychopharmacol. Biol. Psychiatry 44, 257-264. doi: 10.1016/j.pnpbp.2013.02.017
57. Ruetschi, U., Zetterberg, H., Podust, V. N., Gottfries, J., Li, S., Hviid Simonsen, A., et al. (2005). Identification of CSF biomarkers for frontotemporal dementia using SELDI-TOF. Exp. Neurol. 196, 273-281. doi: 10.1016/j.expneurol.2005.08.002
58. Sadahiro, M., Erickson, C., Lin, W. J., Shin, A. C., Razzoli, M., Jiang, C., et al. (2015). Role of VGF-derived carboxy-terminal peptides in energy balance and reproduction: analysis of '‘humanized’' knockin mice expressing full-length or truncated VGF. Endocrinology 156, 1724-1738. doi: 10.1210/en.2014-1826
59. Sahay, A., and Hen, R. (2007). Adult hippocampal neurogenesis in depression. Nat. Neurosci. 10, 1110-1115. doi: 10.1038/nn1969
60. Salton, S. R., Ferri, G. L., Hahm, S., Snyder, S. E., Wilson, A. J., Possenti, R., et al. (2000). VGF: a novel role for this neuronal and neuroendocrine polypeptide in the regulation of energy balance. Front. Neuroendocrinol. 21, 199-219. doi: 10.1006/frne.2000.0199
61. Selle, H., Lamerz, J., Buerger, K., Dessauer, A., Hager, K., Hampel, H., et al. (2005). Identification of novel biomarker candidates by differential peptidomics analysis of cerebrospinal fluid in Alzheimer’s disease. Comb. Chem. High Throughput Screen. 8, 801-806. doi: 10.2174/138620705774962391
62. Sha, L., MacIntyre, L., Machell, J. A., Kelly, M. P., Porteous, D. J., Brandon, N. J., et al. (2012). Transcriptional regulation of neurodevelopmental and metabolic pathways by NPAS3. Mol. Psychiatry 17, 267-279. doi: 10.1038/mp.2011.73
63. Sha, S., Qu, W. J., Li, L., Lu, Z. H., Chen, L., Yu, W. F., et al. (2013). Sigma-1 receptor knockout impairs neurogenesis in dentate gyrus of adult hippocampus via down-regulation of NMDA receptors. CNS Neurosci. Ther. 19, 705-713. doi: 10.1111/cns.12129
64. Sharma, S., Darland, D., Lei, S., Rakoczy, S., and Brown-Borg, H. M. (2012). NMDA and kainate receptor expression, long-term potentiation and neurogenesis in the hippocampus of long-lived Ames dwarf mice. Age (Dordr.) 34, 609-620. doi: 10.1007/s11357-011-9253-1
65. Soumier, A., Banasr, M., Lortet, S., Masmejean, F., Bernard, N., Kerkerian-Le-Goff, L., et al. (2009). Mechanisms contributing to the phase-dependent regulation of neurogenesis by the novel antidepressant, agomelatine, in the adult rat hippocampus. Neuropsychopharmacology 34, 2390-2403. doi: 10.1038/npp.2009.72
66. Spellman, D. S., Wildsmith, K. R., Honigberg, L. A., Tuefferd, M., Baker, D., Raghavan, N., et al. (2015). Development and evaluation of a multiplexed mass spectrometry based assay for measuring candidate peptide biomarkers in Alzheimer’s Disease Neuroimaging Initiative (ADNI) CSF. Proteomics Clin. Appl. 9, 715-731. doi: 10.1002/prca.201400178
67. Thakker-Varia, S., and Alder, J. (2009). Neuropeptides in depression: role of VGF. Behav. Brain Res. 197, 262-278. doi: 10.1016/j.bbr.2008.10.006
68. Thakker-Varia, S., Behnke, J., Doobin, D., Dalal, V., Thakkar, K., Khadim, F., et al. (2014). VGF (TLQP-62)-induced neurogenesis targets early phase neural progenitor cells in the adult hippocampus and requires glutamate and BDNF signaling. Stem Cell Res. 12, 762-777. doi: 10.1016/j.scr.2014.03.005
69. Thakker-Varia, S., Jean, Y. Y., Parikh, P., Sizer, C. F., Jernstedt Ayer, J., Parikh, A., et al. (2010). The neuropeptide VGF is reduced in human bipolar postmortem brain and contributes to some of the behavioral and molecular effects of lithium. J. Neurosci. 30, 9368-9380. doi: 10.1523/jneurosci.5987-09.2010
70. Thakker-Varia, S., Krol, J. J., Nettleton, J., Bilimoria, P. M., Bangasser, D. A., Shors, T. J., et al. (2007). The neuropeptide VGF produces antidepressant-like behavioral effects and enhances proliferation in the hippocampus. J. Neurosci. 27, 12156-12167. doi: 10.1523/jneurosci.1898-07.2007
71. Thomas, P., and Smart, T. G. (2005). HEK293 cell line: a vehicle for the expression of recombinant proteins. J. Pharmacol. Toxicol. Methods 51, 187-200. doi: 10.1016/j.vascn.2004.08.014
72. Trauzold, A., Schmiedel, S., Sipos, B., Wermann, H., Westphal, S., Röder, C., et al. (2003). PKCµ prevents CD95-mediated apoptosis and enhances proliferation in pancreatic tumour cells. Oncogene 22, 8939-8947. doi: 10.1038/sj.onc.1207001
73. Walker, A. K., Rivera, P. D., Wang, Q., Chuang, J. C., Tran, S., Osborne-Lawrence, S., et al. (2015). The P7C3 class of neuroprotective compounds exerts antidepressant efficacy in mice by increasing hippocampal neurogenesis. Mol. Psychiatry 20, 500-508. doi: 10.1038/mp.2014.34
74. Warner-Schmidt, J. L., and Duman, R. S. (2006). Hippocampal neurogenesis: opposing effects of stress and antidepressant treatment. Hippocampus 16, 239-249. doi: 10.1002/hipo.20156
75. Wong, C., and Jin, Z. G. (2005). Protein kinase C-dependent protein kinase D activation modulates ERK signal pathway and endothelial cell proliferation by vascular endothelial growth factor. J. Biol. Chem. 280, 33262-33269. doi: 10.1074/jbc.m503198200
76. Wong, E. H., Kemp, J. A., Priestley, T., Knight, A. R., Woodruff, G. N., and Iversen, L. L. (1986). The anticonvulsant MK-801 is a potent N-methyl-D-aspartate antagonist. Proc. Natl. Acad. Sci. U S A 83, 7104-7108. doi: 10.1073/pnas.83.18.7104
77. Xiao, X. L., Ma, D. L., Wu, J., and Tang, F. R. (2013). Metabotropic glutamate receptor 5 (mGluR5) regulates proliferation and differentiation of neuronal progenitors in the developmental hippocampus. Brain Res. 1493, 1-12. doi: 10.1016/j.brainres.2012.11.015
78. Yamasaki, N., Maekawa, M., Kobayashi, K., Kajii, Y., Maeda, J., Soma, M., et al. (2008). Alpha-CaMKII deficiency causes immature dentate gyrus, a novel candidate endophenotype of psychiatric disorders. Mol. Brain 1: 6. doi: 10.1186/1756-6606-1-6
79. Yu, L., Arbez, N., Nucifora, L. G., Sell, G. L., Delisi, L. E., Ross, C. A., et al. (2014). A mutation in NPAS3 segregates with mental illness in a small family. Mol. Psychiatry 19, 7-8. doi: 10.1038/mp.2012.192
80. Yuan, X., and Desiderio, D. M. (2005). Human cerebrospinal fluid peptidomics. J. Mass Spectrom. 40, 176-181. doi: 10.1002/jms.737
81. Zaheer, A., Yorek, M. A., and Lim, R. (2001). Effects of glia maturation factor overexpression in primary astrocytes on MAP kinase activation, transcription factor activation and neurotrophin secretion. Neurochem. Res. 26, 1293-1299. doi: 10.1023/A: 1014241300179