The relationship between dlx and gad1 expression indicates highly conserved genetic pathways in the zebrafish forebrain

Developmental Dynamics

Volumn 239, Issue 8, 2010, Pages 2298-2306

  MacDonald, Ryan B ^a   Debiais Thibaud, Mélanie ^a   Talbot, Jared Coffin ^b   Ekker, Marc ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF OREGON   (United States)

Author keywords

Dlx; Fluorescent in situ hybridization; Forebrain; Regulatory elements; Transgenesis; Zebrafish

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DLX GENE; ENHANCER REGION; FLUORESCENCE IN SITU HYBRIDIZATION; FOREBRAIN; GABAERGIC SYSTEM; GAD1 GENE; GENE EXPRESSION; GENE LOCUS; GENETIC TRANSCRIPTION; GENETICS; GENOTYPE; INTERNEURON; MOUSE; NONHUMAN; PRIORITY JOURNAL; REPORTER GENE; TELENCEPHALON; TRANSGENICS; VERTEBRATE; ZEBRA FISH;

ANIMALS; DIENCEPHALON; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION, FLUORESCENCE; INTERNEURONS; ORGANISMS, GENETICALLY MODIFIED; PROSENCEPHALON; TELENCEPHALON; TRANSCRIPTION FACTORS; ZEBRAFISH;

DANIO RERIO; MUS; VERTEBRATA;

EID: 77954999717     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22365     Document Type: Article

References (36)

1. Akimenko MA, Ekker M, Wegner J, Lin W, Westerfield M. 1994. Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J Neurosci 14:3475-3486. (Pubitemid 24174099)
2. Amores A, Force A, Yan YL, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang YL, Westerfield M, Ekker M, Postlethwait JH. 1998. Zebra-fish hox clusters and vertebrate genome evolution. Science 282:1711-1714. (Pubitemid 28549287)
3. Anderson SA, Eisenstat DD, Shi L, Rubenstein JLR. 1997a. Interneuron migration from basal forebrain to neocortex: dependence on dlx genes. Science 278:474-476.
4. Anderson SA, Qiu M, Bulfone A, Eisenstat DD, Meneses J, Pedersen R, Rubenstein JLR. 1997b. Mutations of the homeobox genes dlx-1 and dlx-2 disrupt the striatal subventricular zone and differentiation of late-born striatal neurons. Neuron 19:27-37.
5. Anderson S, Mione M, Yun K, Rubenstein JL. 1999. Differential origins of neocortical projection and local circuit neurons: role of dlx genes in neocortical interneuronogenesis. Cereb Cortex 9:646-654. (Pubitemid 29441506)
6. Eisenstat DD, Liu JK, Mione M, Zhong W, Yu G, Anderson SA, Ghattas I, Puelles L, Rubenstein JLR. 1999. DLX-1, DLX-2 and DLX-5 expression define distinct stages of basal forebrain differentiation. J Comp Neurol 414:217-237.
7. Ellies DL, Stock DW, Hatch G, Giroux G, Weiss KM, Ekker M. 1997. Relationship between the genomic organization and the overlapping embryonic expression patterns of the zebrafish dlx genes. Genomics 45:580-590.
8. Fisher S, Grice EA, Vinton RM, Bessling SL, Urasaki A, Kawakami K, McCallion AS. 2006. Evaluating the biological relevance of putative enhancers using Tol2 transposon-mediated transgenesis in zebrafish. Nat Protoc 1:1297-1305.
9. Ghanem N, Jarinova O, Amores A, Hatch G, Park BK, Rubenstein JLR, Ekker M. 2003. Regulatory roles of conserved intergenic domains in vertebrate dlx bigene clusters. Genome Res 13:533-543.
10. Ghanem N, Yu M, Long J, Hatch G, Rubenstein JL, Ekker M. 2007. Distinct cis-regulatory elements from the Dlx1/Dlx2 locus mark different progenitor cell populations in the ganglionic eminences and different subtypes of adult cortical interneurons. J Neurosci 27:5012-5022.
11. Jowett T, Yan YL. 1996. Double fluorescent in situ hybridization to zebrafish embryos. Trends Genet 12:387-389. (Pubitemid 26336473)
12. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. 1995. Stages of embryonic development of the zebra-fish. Dev Dyn 203:253-310.
13. Liu JK, Ghattas I, Liu S, Chen S, Rubenstein JLR. 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. (Pubitemid 27516674)
14. Marin O, Anderson SA, Rubenstein JL. 2000. Origin and molecular specification of striatal interneurons. J Neurosci 20:6063-6076. (Pubitemid 30658400)
15. Martin SC, Heinrich G, Sandell JH. 1998. Sequence and expression of glutamic acid decarboxylase isoforms in the developing zebrafish. J Comp Neurol 396:253-266.
16. Mione M, Baldessari D, Deflorian G, Nappo G, Santoriello C. 2008. How neuronal migration contributes to the morphogenesis of the CNS: insights from the zebrafish. Dev Neurosci 30:65-81.
17. Mueller T, Wullimann MF. 2002. BrdU-, neuroD (nrd)- and Hu-studies reveal unusual non-ventricular neurogenesis in the postembryonic zebrafish forebrain. Mech Dev 117:123-135.
18. Mueller T, Wullimann MF. 2003. Anatomy of neurogenesis in the early zebrafish brain. Brain Res Dev Brain Res 140:137-155.
19. Mueller T, Wullimann MF. 2009. An evolutionary interpretation of teleostean forebrain anatomy. Brain Behav Evol 74:30-42.
20. Mueller T, Vernier P, Wullimann MF. 2006. A phylotypic stage in vertebrate brain development: GABA cell patterns in zebrafish compared with mouse. J Comp Neurol 494:620-634.
21. Mueller T, Wullimann MF, Guo S. 2008. Early teleostean basal ganglia development visualized by zebrafish Dlx2a, Lhx6, Lhx7, Tbr2 (eomesa), and GAD67 gene expression. J Comp Neurol 507:1245-1257.
22. Pleasure SJ, Anderson S, Hevner R, Bagri A, Marin O, Lowenstein DH, Rubenstein JLR. 2000. Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 28:727-740.
23. Potter GB, Petryniak MA, Shevchenko E, McKinsey GL, Ekker M, Rubenstein JLR. 2009. Generation of Cre-transgenic mice using Dlx1/Dlx2 enhancers and their characterization in GABAergic interneurons. Mol Cell Neurosci 40:167-186.
24. Quint E, Zerucha T, Ekker M. 2000. Differential expression of orthologous dlx genes in zebrafish and mice: implications for the evolution of the dlx homeobox gene family. J Exp Zool 288:235-241.
25. Stühmer T, Anderson SA, Ekker M, Rubenstein JLR. 2002a. Ectopic expression of the dlx genes induces glutamic acid decarboxylase and dlx expression. Development 129:245-252. (Pubitemid 34863792)
26. Stühmer T, Puelles L, Ekker M, Rubenstein JL. 2002b. Expression from a dlx gene enhancer marks adult mouse cortical GABAergic neurons. Cereb Cortex 12:75-85. (Pubitemid 33152019)
27. Sumiyama K, Irvine SQ, Stock DW, Weiss KM, Kawasaki K, Shimuzu N, Shashikant CS, Miller W, Ruddle FH. 2002. Genomic structure and functional control of the Dlx3-7 bigene cluster. Proc Natl Acad Sci U S A 99:780-785.
28. Thisse C, Thisse B. 1998. High resolution whole-mount in situ hybridization. Zebrafish Sci Monit 5:8-9.
29. Welten MC, de Haan SB, van den Boogert N, Noordermeer JN, Lamers GE, Spaink HP, Meijer AH, Verbeek FJ. 2006. ZebraFISH: fluorescent in situ hybridization protocol and three-dimensional imaging of gene expression patterns. Zebrafish 3:465-476.
30. Westerfield M. 2000. The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio). 4th ed. Eugene, OR: University of Oregon Press.
31. Wullimann M. 2009. Secondary neurogenesis and telencephalic organization in zebrafish and mice: a brief review. Integr Zool 4:123-133.
32. Wullimann MF, Mueller T. 2002. Expression of zash-1a in the postembryonic zebrafish brain allows comparison to mouse Mash1 domains. Brain Res Gene Expr Patterns 1:187-192.
33. Wullimann MF, Mueller T. 2004. Teleostean and mammalian forebrains contrasted: evidence from genes to behavior. J Comp Neurol 475:143-162.
34. Yun K, Fischman S, Johnson J, Hrabe de Angelis M, Weinmaster G, Rubenstein JL. 2002. Modulation of the notch signaling by Mash1 and Dlx1/2 regulates sequential specification and differentiation of progenitor cell types in the subcortical telencephalon. Development 129:5029-5040.
35. Zerucha T, Stühmer T, Hatch G, Park BK, Long Q, Yu G, Gambarotta A, Schultz JR, Rubenstein JLR, Ekker M. 2000. A highly conserved enhancer in the Dlx5/Dlx6 intergenic region is the site of cross-regulatory interactions between Dlx genes in the embryonic forebrain. J Neurosci 20:709-721.
36. Zhou QP, Le TN, Qiu X, Spencer V, de Melo J, Du G, Plews M, Fonseca M, Sun JM, Davie JR, Eisenstat DD. 2004. Identification of a direct Dlx homeodomain target in the developing mouse forebrain and retina by optimization of chromatin immunoprecipitation. Nucleic Acids Res 32:884-892.