Activity-dependent expression of neuronal PAS domain-containing protein 4 (npas4a) in the developing zebrafish brain

Frontiers in Neuroanatomy

Volumn 8, Issue DEC, 2014, Pages

  Klarić, Thomas ^a   Lardelli, Michael ^a   Key, Brian ^b   Koblar, Simon ^a   Lewis, Martin ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Dlxl; Neurodevelopment; Npas4a; PTZ; Shh; Zebrafish

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; EMBRYO; EMBRYO DEVELOPMENT; EVOLUTIONARY ADAPTATION; GENE; GENE EXPRESSION; GENE TARGETING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MITOSIS; NERVE CELL PLASTICITY; NERVE CONDUCTION; NEURONAL PAS DOMAIN CONTAINING PROTEIN 4 GENE; NONHUMAN; PHYLOGENY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; ZEBRA FISH;

EID: 84937698952     PISSN: None     EISSN: 16625129     Source Type: Journal    
DOI: 10.3389/fnana.2014.00148     Document Type: Article

References (71)

1. Andoniadou, C. L., andMartinez-Barbera, J. P. (2013). Developmental mechanisms directing early anterior forebrain specification in vertebrates. Cell. Mol. Life Sci. 70, 3739-3752. doi: 10.1007/s00018-013-1269-5
2. Baraban, S. C., Taylor, M. R., Castro, P. A., and Baier, H. (2005). Pentylenete- trazole induced changes in zebrafish behavior, neural activity and c­fos expression. Neuroscience 131, 759-768. doi: 10.1016/j.neuroscience.2004.11.031
3. Barth, K. A., and Wilson, S. W. (1995). Expression of zebrafish nk2.2 is influenced by sonic hedgehog/vertebrate hedgehog-1 and demarcates a zone of neuronal differentiation in the embryonic forebrain. Development 121, 1755-1768.
4. Baxendale, S., Holdsworth, C. J., Meza Santoscoy, P. L., Harrison, M. R. M., Fox, J., Parkin, C. A., et al. (2012). Identification of compounds with anti-convulsant properties in a zebrafish model of epileptic seizures. Dis. Model. Mech. 5, 773­784. doi: 10.1242/dmm.010090
5. Bepari, A. K., Sano, H., Tamamaki, N., Nambu, A., Tanaka, K. F., and Takebayashi, H. (2012a). Identification of optogenetically activated striatal medium spiny neurons by npas4 expression. PLoS One 7:e52783. doi: 10.1371/journal.pone.0052783
6. Bepari, A. K., Watanabe, K., Yamaguchi, M., Tamamaki, N., and Takebayashi, H. (2012b). Visualization of odor-induced neuronal activity by immediate early gene expression. BMC Neurosci. 13:140. doi: 10.1186/1471-2202­13-140
7. Bloodgood, B. L., Sharma, N., Browne, H. A., Trepman, A. Z., and Greenberg, M. E. (2013). The activity-dependent transcription factor NPAS4 regulates domain- specific inhibition. Nature 503, 121-125. doi: 10.1038/nature12743
8. Bradford, Y., Conlin, T., Dunn, N., Fashena, D., Frazer, K., Howe, D. G., et al. (2011). ZFIN: enhancements and updates to the zebrafish model organism database. Nucleic AcidsRes. 39,D822-D829. doi: 10.1093/nar/gkQ977
9. Cavanna, A. E., and Monaco, F. (2009). Brain mechanisms of altered con­scious states during epileptic seizures. Nat. Rev. Neurol. 5, 267-276. doi: 10.1038/nrneurol.2009.38
10. Cobos, I., Calcagnotto, M. E., Vilaythong, A. J., Thwin, M. T., Noebels, J. L., Baraban, S. C., et al. (2005). Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat. Neurosci. 8, 1059-1068. doi: 10.1038/nn1499
11. Cole, L. K., and Ross, L. S. (2001). Apoptosis in the developing zebrafish embryo.Dev. Biol. 240, 123-142. doi: 10.1006/dbio.2001.0432
12. Cooke, J. E., and Moens, C. B. (2002). Boundary formation in the hindbrain: Eph only it were simple... Trends Neurosci. 25, 260-267. doi: 10.1016/s0166-2236(02)02134-3
13. Corey, D. R., and Abrams, J. M. (2001). Morpholino antisense oligonucleotides: tools for investigating vertebrate development. Genome Biol. 2, 1015.1-1015.3. doi: 10.1186/gb-2001-2-5-reviews1015
14. Coutellier, L., Beraki, S., Ardestani, P. M., Saw, N. L., and Shamloo, M. (2012). Npas4: a neuronal transcription factor with a key role in social and cognitive functions relevant to developmental disorders. PLoS One 7:e46604. doi: 10.1371/journal.pone.0046604
15. Crews, S. E. (2003). PAS Proteins: Regulators and Sensors of Development and Physiology. Boston: Kluwer Academic Publishers.
16. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., et al. (2008). Phylogeny.fr: rubust phylogenetic analysys for the non-specialist. Nucleic Acids Res. 36, W465-W469. doi: 10.1093/nar/gkn180
17. Eisen, J. S., and Smith, J. C. (2008). Controlling morpholino experiments: don’t stop making antisense. Development 135, 1735-1743. doi: 10.1242/dev.001115
18. Eisenstat, D. D., Liu, J. K., Mione, M., Zhong, W., Yu, G., Anderson, S. A., et al. (1999). DLX-1, DLX-2 and DLX-5 expression define distinct stages ofbasal fore­brain differentiation. J. Comp. Neurol. 414, 217-237. doi: 10.1002/(sici)1096-9861(19991115)414:2<217::aid-cne6>3.0.co;2-i
19. Ellies, D. L., Stock, D.W., Hatch, G., Giroux, G., Weiss, K. M., andEkker, M. (1997). Relationship between the genomic organization and the overlapping embryonic expression patterns of the zebrafish dlx genes. Genomics 45, 580-590. doi: 10.1006/geno.1997.4978
20. 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. doi: 10.1111/j.1460-9568.2004.03646.x
21. Fürthauer, M., Thisse, C., and Thisse, B. (1997). A role for FGF-8 in the dorsoven- tral patterning of the zebrafish gastrula. Development 124, 4253-4264.
22. Hagemann, A. I. H., and Scholpp, S. (2012). The tale of the three brothers - Shh, Wnt and Fgf during development of the thalamus. Front. Neurosci. 6:76. doi: 10.3389/fnins.2012.00076
23. Hans, F., and Dimitrov, S. (2001). Histone H3 phosphorylation and cell division.Oncogene 20, 3021-3027. doi: 10.1038/sj.onc.1204326
24. Hao, N., Whitelaw, M. L., Shearwin, K. E., Dodd, I. B., and Chapman-Smith, A. (2011). Identification of residues in the N-terminal PAS domains important for dimerization of Arnt and AhR. Nucleic Acids Res. 39, 3695-3709. doi: 10.1093/nar/gkq1336
25. Hauptmann, G., and Gerster, T. (2000). Regulatorygene expression patterns reveal transverse and longitudinal subdivisions of the embryonic zebrafish forebrain. Mech. Dev. 91, 105-118. doi: 10.1016/s0925-4773(99)00277-4
26. Heffer, A., and Pick, L. (2013). Conservationandvariation in Hoxgenes: howinsect models pioneered the evo-devo field. Annu. Rev. Entomol. 58, 161-179. doi: 10.1146/annurev-ento-120811-153601
27. Hester, I., McKee, S., Pelletier, P., Thompson, C., Storbeck, C., Mears, A., et al. (2007). Transient expression of Nxf, a bHLH-PAS transactivator induced by neuronal preconditioning, confers neuroprotection in cultured cells. Brain Res. 1135, 1-11. doi: 10.1016/j.brainres.2006.11.083
28. Hjorth, J. T., and Key, B. (2001). Are pioneer axons guided by regulatory gene expression domains in the zebrafish forebrain? High-resolution analysis of the patterning of the zebrafish brain during axon tract formation. Dev. Biol. 229, 271-286. doi: 10.1006/dbio.2000.9980
29. Huang, R. Q., Bell-Horner, C. L., Dibas, M. I., Covey, D. F., Drewe, J. A., and Dillon, G. H. (2001). Pentylenetetrazole-induced inhibition of recombinant gamma- aminobutyric acid type A (GABA(A)) receptors: mechanism and site of action. J. Pharmacol. Exp. Ther. 298, 986-995.
30. Jiang, L., and Crews, S. T. (2003). The Drosophila dysfusion basic helix-loop-helix (bHLH)-PAS gene controls tracheal fusion and levels of the trachealess bHLH- PAS protein. Mol. Cell. Biol. 23, 5625-5637. doi: 10.1128/mcb.23.16.5625-5637.2003
31. Jiang, L., and Crews, S. T. (2006). Dysfusion transcriptional control of Drosophila tracheal migration, adhesion and fusion. Mol. Cell. Biol. 26, 6547-6556. doi: 10.1128/mcb.00284-06
32. Jiang, L., and Crews, S. T. (2007). Transcriptional specificity of Drosophila dysfusion and the control oftracheal fusion cell gene expression. J. Biol. Chem. 282, 28659­28668. doi: 10.1074/jbc.m703803200
33. Jowett, T. (1997). Tissue in Situ Hybridization: Methods in Animal Development. Chichester: Wiley.
34. Kim, C. H., Ueshima, E., Muraoka, O., Tanaka, H., Yeo, S. Y., Huh, T. L., et al. (1996). Zebrafish elav/HuC homologue as a very early neuronal marker. Neu- rosci. Lett. 216, 109-112. doi: 10.1016/s0304-3940(96)13021-4
35. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253­310. doi: 10.1002/aja.1002030302
36. Klaric, T. S., Thomas, P. Q., Dottori, M., Leong, W. K., Koblar, S. A., and Lewis, M. D. (2014). A reduction in Npas4 expression results in delayed neural differentiation of mouse embryonic stem cells. Stem Cell Res. Ther. 5:64. doi: 10.1186/scrt453
37. Kleinjan, D. A., Bancewicz, R. M., Gautier, P., Dahm, R., Schonthaler, H. B., Damante, G., et al. (2008). Subfunctionalization of duplicated zebrafish pax6 genes by cis-regulatory divergence. PLoS Genet. 4:e29. doi: 10.1371/journal.pgen.0040029
38. Krauss, S., Concordet, J. P., and Ingham, P. W. (1993). A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75, 1431-1444. doi: 10.1016/0092-8674(93)90628-4
39. Krauss, S., Johansen, T., Korzh, V., Moens, U., Ericson, J. U., and Fjose, A. (1991). Zebrafish pax[zf-a]: a paired box-containing gene expressed in the neural tube. EMBOJ. 10,3609-3619.
40. Lakowski, J., Majumder, A., and Lauderdale, J. D. (2007). Mechanisms controlling Pax6 isoform expression in the retina have been conserved between teleosts and mammals. Dev. Biol. 307, 498-520. doi: 10.1016/j.ydbio.2007.04.015
41. Leger, S., and Brand, M. (2002). Fgf8 and Fgf3 are required for zebrafish ear placode induction, maintenance and inner ear patterning. Mech. Dev. 119, 91­108. doi: 10.1016/s0925-4773(02)00343-x
42. Lin, Y., Bloodgood, B. L., Hauser, J. L., Lapan, A. D., Koon, A. C., Kim, T. K., et al. (2008). Activity-dependent regulation of inhibitory synapse development by Npas4. Nature 455, 1198-1204. doi: 10.1038/nature07319
43. Liu, J. K., Ghattas, I., Liu, S., Chen, S., and Rubenstein, J. L. R. (1997). Dlx genes encode DNA-binding proteins that are expressed in an overlapping and sequential pattern during basal ganglia differentiation. Dev. Dyn. 210, 498-512. doi: 10.1002/(sici)1097-0177(199712)210:4<498::aid-aja12>3.0.co;2-3
44. MacDonald, R. B., Debiais-Thibaud, M., Talbot, J. C., and Ekker, M. (2010). The relationship between dlx and gad1 expression indicates highly conserved genetic pathways in the zebrafish forebrain. Dev. Dyn. 239, 2298-2306. doi: 10.1002/dvdy.22365
45. MacDonald, R. B., Pollack, J. N., Debiais-Thibaud, M., Heude, E., Coffin Talbot, J., and Ekker, M. (2013). The ascl1a and dlx genes have a regulatory role in the development of GABAergic interneurons in the zebrafish diencephalon. Dev. Biol. 381, 276-285. doi: 10.1016/j.ydbio.2013.05.025
46. Mao, R., Page, D. T., Merzlyak, I., Kim, C., Tecott, L. H., Janak, P. H., et al. (2009). Reduced conditioned fear response in mice that lack Dlx1 and show subtype-specific loss of interneurons. J. Neurodev. Disord. 1, 224-236. doi: 10.1007/s11689-009-9025-8
47. Mattes, B., Weber, S., Peres, J., Chen, Q., Davidson, G., Houart, C., et al. (2012). Wnt3 and Wnt3a are required for induction of the mid-diencephalic organizer in the caudal forebrain. Neural Dev. 7:12. doi: 10.1186/1749-8104-7-12
48. Meyer, A., and Van De Peer, Y. (2005). From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27, 937-945. doi: 10.1002/bies.20293
49. 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. doi: 10.1016/j.molbrainres.2004.06.023
50. Nornes, S., Clarkson, M., Mikkola, I., Pedersen, M., Bardsley, A., Martinez, J. P., et al. (1998). Zebrafish contains two Pax6 genes involved in eye development. Mech. Dev. 77, 185-196. doi: 10.1016/s0925-4773(98)00156-7
51. Ooe, N., Motonaga, K., Kobayashi, K., Saito, K., and Kaneko, H. (2009). Functional characterization ofbasic helix-loop-helix-PAS type transcription factor NXF in vivo: putative involvement in an “on demand” neuroprotection system. J. Biol. Chem. 284, 1057-1063. doi: 10.1074/jbc.m805196200
52. 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. doi: 10.1128/mcb.24.2.608-616.2004
53. Ooe, N., Saito, K., Oeda, K., Nakatuka, I., and Kaneko, H. (2007). Character­ization of Drosophila and Caenorhabditis elegans NXF-like-factors, putative homologs of mammalian NXF. Gene 400, 122-130. doi: 10.1016/j.gene.2007.06.005
54. Park, H. C., Hong, S. K., Kim, H. S., Kim, S. H., Yoon, E. J., Kim, C. H., et al. (2000). Structural comparison of zebrafish Elav/Hu and their differential expressions duringneurogenesis. Neurosci. Lett. 279, 81-84. doi: 10.1016/s0304-3940(99)00940-4
55. Petryniak, M. A., Potter, G. B., Rowitch, D. H., and Rubenstein, J. L. R. (2007). Dlx1 and Dlx2 control neuronal versus oligodendroglial cell fate acquisition in the developing forebrain. Neuron 55, 417-433. doi: 10.1016/j.neuron.2007.06.036
56. 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. doi: 10.1371/journal.pone.0023760
57. Pruunsild, P., Sepp, M., Orav, E., Koppel, I., and Timmusk, T. (2011). Identifi­cation of cis-Elements and transcription factors regulating neuronal activity- dependent transcription of human BDNF gene. J. Neurosci. 31, 3295-3308. doi: 10.1523/jneurosci.4540-10.2011
58. Ramamoorthi, K., Fropf, R., Belfort, G. M., Fitzmaurice, H. L., McKinney, R. M., Neve, R. L., et al. (2011). Npas4 regulates a transcriptional program in CA3 required for contextual memory formation. Science 334, 1669-1675. doi: 10.1126/science.1208049
59. Reifers, F., Böhli, H., Walsh, E. C., Crossley, P. H., Stainier, D. Y., and Brand, M. (1998). Fgf8 is mutated in zebrafish acerebellar (ace) mutants and is required for maintenance of midbrain-hindbrainboundary development and somitogenesis. Development 125, 2381-2395.
60. Schmittgen, T. D., and Livak, K. J. (2008). Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101-1108. doi: 10.1038/nprot.2008.73
61. Scholpp, S., and Lumsden, A. (2010). Building a bridal chamber: development of the thalamus. Trends Neurosci. 33, 373-380. doi: 10.1016/j.tins.2010.05.003
62. Scholpp, S., Wolf, O., Brand, M., and Lumsden, A. (2006). Hedgehog signalling from the zona limitans intrathalamica orchestrates patterning of the zebrafish diencephalon. Development 133, 855-864. doi: 10.1242/dev.02248
63. Shamloo, M., Soriano, L., Von Schack, D., Rickhag, M., Chin, D. J., Gonzalez- Zulueta, M., et al. (2006). Npas4, a novel helix-loop-helix PAS domain protein, is regulated in response to cerebral ischemia. Eur. J. Neurosci. 24, 2705-2720. doi: 10.1111/j.1460-9568.2006.05172.x
64. Sperber, S. M., Saxena, V., Hatch, G., and Ekker, M. (2008). Zebrafish dlx2a contributes to hindbrain neural crest survival, is necessary for differentiation of sensory ganglia and functions with dlx1a in maturation of the arch cartilage elements. Dev. Biol. 314,59-70.doi: 10.1016/j.ydbio.2007.11.005
65. Stühmer, T., Anderson, S. A., Ekker, M., and Rubenstein, J. L. R. (2002a). Ectopic expression of the Dlx genes induces glutamic acid decarboxylase and Dlx expression. Development 129, 245-252.
66. Stühmer, T., Puelles, L., Ekker, M., and Rubenstein, J. L. R. (2002b). Expression from a Dlx gene enhancer marks adult mouse cortical GABAergic neurons. Cereb. Cortex 12, 75-85. doi: 10.1093/cercor/12.1.75
67. Talbot, J. C., Johnson, S. L., and Kimmel, C. B. (2010). hand2 and Dlx genes specify dorsal, intermediate and ventral domains within zebrafish pharyngeal arches. Development 137, 2507-2517. doi: 10.1242/dev.049700
68. Taylor, J. S., Van de Peer, Y., Braasch, I., and Meyer, A. (2001). Comparative genomics provides evidence for an ancient genome duplication event in fish. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356, 1661-1679. doi: 10.1098/rstb.2001.0975
69. Thummel, R., Enright, J. M., Kassen, S. C., Montgomery, J. E., Bailey, T. J., and Hyde, D. R. (2010). Pax6aand Pax6b are required at different points in neuronal progenitor cell proliferation during zebrafish photoreceptor regeneration. Exp. Eye Res. 90, 572-582. doi: 10.1016/j.exer.2010.02.001
70. Verreijdt, L., Debiais-Thibaud, M., Borday-Birraux, V., Van der Heyden, C., Sire, J.-Y., and Huysseune, A. (2006). Expression of the dlx gene family during formation of the cranial bones in the zebrafish (Danio rerio): differential involvement in the visceral skeleton and braincase. Dev. Dyn. 235, 1371-1389. doi: 10.1002/dvdy.20734
71. Xiang, G., Pan, L., Xing, W., Zhang, L., Huang, L., Yu, J., et al. (2007). Identification of activity-dependent gene expression profiles reveals specific subsets of genes induced by different routes of Ca2+ entry in cultured rat cortical neurons. J. Cell. Physiol. 212, 126-136. doi: 10.1002/jcp.21008