GABAergic interneuron differentiation in the basal forebrain is mediated through direct regulation of glutamic acid decarboxylase isoforms by Dlx homeobox transcription factors

Journal of Neuroscience

Volumn 37, Issue 36, 2017, Pages 8816-8829

  Le, Trung N ^a,b   Zhou, Qing Ping ^a   Cobos, Inma ^c   Zhang, Shunzhen ^a   Zagozewski, Jamie ^d   Japoni, Sara ^d   Vriend, Jerry ^a   Parkinson, Tracie ^a   Du, Guoyan ^a   Rubenstein, John L ^c   Eisenstat, David D ^a,d  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Forebrain development; GABA; Glutamic acid decarboxylase; Homeobox; Interneuron

Indexed keywords

4 AMINOBUTYRIC ACID; DLX1 HOMEODOMAIN PROTEIN; DLX2 HOMEODOMAIN PROTEIN; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; HOMEODOMAIN PROTEIN; ISOPROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; DISTAL-LESS HOMEOBOX PROTEINS;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASAL FOREBRAIN; BRAIN DEVELOPMENT; CELL COUNTING; CELL MIGRATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DLX GENE; GABAERGIC SYSTEM; GEL MOBILITY SHIFT ASSAY; GENE; GENE EXPRESSION; GENE FUNCTION; GENETIC TRANSFECTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HOMEOBOX; IMMUNOFLUORESCENCE TEST; IN SITU HYBRIDIZATION; MOUSE; NERVE CELL DIFFERENTIATION; NEUROTRANSMITTER RELEASE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; REAL TIME POLYMERASE CHAIN REACTION; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TELENCEPHALON; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; FEMALE; GENE EXPRESSION REGULATION; INTERNEURON; KNOCKOUT MOUSE; MALE; METABOLISM; PHYSIOLOGY;

ANIMALS; BASAL FOREBRAIN; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; FEMALE; GABAERGIC NEURONS; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUTAMATE DECARBOXYLASE; HOMEODOMAIN PROTEINS; INTERNEURONS; MALE; MICE; MICE, KNOCKOUT; TRANSCRIPTION FACTORS;

EID: 85029152680     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2125-16.2017     Document Type: Article

References (55)

1. Al-Jaberi N, Lindsay S, Sarma S, Bayatti N, Clowry GJ (2015) The early fetal development of human neocortical GABAergic interneurons. Cereb Cortex 25:631–645. CrossRef Medline
2. Anderson SA, Eisenstat DD, Shi L, Rubenstein JL (1997a) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474–476. CrossRef Medline
3. Anderson SA, Qiu M, Bulfone A, Eisenstat DD, Meneses J, Pedersen R, Rubenstein JL (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. CrossRef Medline
4. Anderson SA, Kaznowski CE, Horn C, Rubenstein JL, McConnell SK (2002) Distinct origins of neocortical projection neurons and interneurons in vivo. Cereb Cortex 12:702–709. CrossRef Medline
5. Anderson SA, Marín O, Horn C, Jennings K, Rubenstein JL (2001) Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128:353–363. Medline
6. 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. CrossRef Medline
7. Barker JL, Behar T, Li YX, Liu QY, Ma W, Maric D, Maric I, Schaffner AE, Serafini R, Smith SV, Somogyi R, Vautrin JY, Wen XL, Xian H (1998) GABAergic cells and signals in CNS development. Perspect Dev Neurobiol 5:305–322. Medline
8. Bickford ME, Ramcharan E, Godwin DW, Erişir A, Gnadt J, Sherman SM (2000) Neurotransmitters contained in the subcortical extraretinal inputs to the monkey lateral geniculate nucleus. J Comp Neurol 424:701– 717. CrossRef Medline
9. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. CrossRef Medline
10. Bulfone A, Puelles L, Porteus MH, Frohman MA, Martin GR, Rubenstein JL (1993) Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries. J Neurosci 13:3155–3172. Medline
11. Cejas P, Li L, O’Neill NK, Duarte M, Rao P, Bowden M, Zhou CW, Mendiola M, Burgos E, Feliu J, Moreno-Rubio J, Guadalajara H, Moreno V, García-Olmo D, Bellmunt J, Mullane S, Hirsch M, Sweeney CJ, Richardson A, Liu XS, et al. (2016) Chromatin immunoprecipitation from fixed clinical tissues reveals tumor-specific enhancer profiles. Nat Med 22:685–691. CrossRef Medline
12. Chang YC, Gottlieb DI (1988) Characterization of the proteins purified with monoclonal antibodies to glutamic acid decarboxylase. J Neurosci 8:2123–2130. Medline
13. Cobos I, Calcagnotto ME, Vilaythong AJ, Thwin MT, Noebels JL, Baraban SC, Rubenstein JL (2005) Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat Neurosci 8:1059– 1068. CrossRef Medline
14. Cobos I, Borello U, Rubenstein JL (2007) Dlx transcription factors promote migration through repression of axon and dendrite growth. Neuron 54: 873–888. CrossRef Medline
15. de Melo J, Qiu X, Du G, Cristante L, Eisenstat DD (2003) Dlx1, Dlx2, Pax6, Brn3b, and Chx10 homeobox gene expression defines the retinal ganglion and inner nuclear layers of the developing and adult mouse retina. J Comp Neurol 461:187–204. CrossRef Medline
16. Donzanti BA, Yamamoto BK (1988) An improved and rapid HPLC-EC method for the isocratic separation of amino acid neurotransmitters from brain tissue and microdialysis perfusates. Life Sci 43:913–922. CrossRef Medline
17. Eisenstat DD, Liu JK, Mione M, Zhong W, Yu G, Anderson SA, Ghattas I, Puelles L, Rubenstein JL (1999) DLX-1, DLX-2, and DLX-5 expression define distinct stages of basal forebrain differentiation. J Comp Neurol 414:217–237. CrossRef Medline
18. Erlander MG, Tillakaratne NJ, Feldblum S, Patel N, Tobin AJ (1991) Two genes encode distinct glutamate decarboxylases. Neuron 7:91–100. CrossRef Medline
19. Feledy JA, Morasso MI, Jang SI, Sargent TD (1999) Transcriptional activation by the homeodomain protein distal-less 3. Nucleic Acids Res 27:764– 770. CrossRef Medline
20. Fode C, Ma Q, Casarosa S, Ang SL, Anderson DJ, Guillemot F (2000) A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev 14:67–80. CrossRef Medline
21. Ghanem N, Yu M, Poitras L, Rubenstein JL, Ekker M (2008) Characterization of a distinct subpopulation of striatal projection neurons expressing the Dlx genes in the basal ganglia through the activity of the I56ii enhancer. Dev Biol 322:415–424. CrossRef Medline
22. Givens ML, Rave-Harel N, Goonewardena VD, Kurotani R, Berdy SE, Swan CH, Rubenstein JL, Robert B, Mellon PL (2005) Developmental regulation of gonadotropin-releasing hormone gene expression by the MSX and DLX homeodomain protein families. J Biol Chem 280:19156–19165. CrossRef Medline
23. Göbel U, Reimer J, Turck F (2010) Genome-wide mapping of protein-DNA interaction by chromatin immunoprecipitation and DNA microarray hybridization (ChIP-chip): Part B. ChIP-chip data analysis. Methods Mol Biol 631:161–184. CrossRef Medline
24. Gould AP, Brookman JJ, Strutt DI, White RA (1990) Targets of homeotic gene control in Drosophila. Nature 348:308–312. CrossRef Medline
25. Graba Y, Aragnol D, Pradel J (1997) Drosophila Hox complex downstream targets and the function of homeotic genes. Bioessays 19:379–388. CrossRef Medline
26. Harwell CC, Fuentealba LC, Gonzalez-Cerrillo A, Parker PR, Gertz CC, Mazzola E, Garcia MT, Alvarez-Buylla A, Cepko CL, Kriegstein AR (2015) Wide dispersion and diversity of clonally related inhibitory interneurons. Neuron 87:999–1007. CrossRef Medline
27. Kito-Shingaki A, Seta Y, Toyono T, Kataoka S, Kakinoki Y, Yanagawa Y, Toyoshima K (2014) Expression of GAD67 and Dlx5 in the taste buds of mice genetically lacking Mash1. Chem Senses 39:403–414. CrossRef Medline
28. Komata M, Katou Y, Tanaka H, Nakato R, Shirahige K, Bando M (2014) Chromatin immunoprecipitation protocol for mammalian cells. Methods Mol Biol 1164:33–38. CrossRef Medline
29. Kuo MH, Allis CD (1999) In vivo cross-linking and immunoprecipitation for studying dynamic protein: DNA associations in a chromatin environment. Methods 19:425–433. CrossRef Medline
30. Kwakowsky A, Schwirtlich M, Zhang Q, Eisenstat DD, Erdélyi F, Baranyi M, Katarova ZD, Szabó G (2007) GAD isoforms exhibit distinct spatiotem-poral expression patterns in the developing mouse lens: correlation with Dlx2 and Dlx5. Dev Dyn 236:3532–3544. CrossRef Medline
31. Le TN, Du G, Fonseca M, Zhou QP, Wigle JT, Eisenstat DD (2007) Dlx homeobox genes promote cortical interneuron migration from the basal forebrain by direct repression of the semaphorin receptor neuropilin-2. J Biol Chem 282:19071–19081. CrossRef Medline
32. Li H, Hader AT, Han YR, Wong JA, Babiarz J, Ricupero CL, Godfrey SB, Corradi JP, Fennell M, Hart RP, Plummer MR, Grumet M (2012) Isolation of a novel rat neural progenitor clone that expresses Dlx family transcription factors and gives rise to functional GABAergic neurons in culture. Dev Neurobiol 72:805–820. CrossRef Medline
33. Liu JK, Ghattas I, Liu S, Chen S, Rubenstein JL (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. CrossRef Medline
34. Luján R, Shigemoto R, López-Bendito G (2005) Glutamate and GABA receptor signalling in the developing brain. Neuroscience 130:567–580. CrossRef Medline
35. MacDonald RB, Debiais-Thibaud M, Talbot JC, Ekker M (2010) The relationship between dlx and gad1 expression indicates highly conserved genetic pathways in the zebrafish forebrain. Dev Dyn 239:2298–2306. CrossRef Medline
36. MacDonald RB, Pollack JN, Debiais-Thibaud M, Heude E, Talbot JC, Ekker M (2013) The ascl1a and dlx genes have a regulatory role in the devel- opment of GABAergic interneurons in the zebrafish diencephalon. Dev Biol 381:276–285. CrossRef Medline
37. Mannervik M (1999) Target genes of homeodomain proteins. Bioessays 21: 267–270. CrossRef Medline
38. Marin O, Anderson SA, Rubenstein JL (2000) Origin and molecular specification of striatal interneurons. J Neurosci 20:6063–6076. Medline
39. Martin DL, Liu H, Martin SB, Wu SJ (2000) Structural features and regulatory properties of the brain glutamate decarboxylases. Neurochem Int 37:111–119. CrossRef Medline
40. Mayer C, Jaglin XH, Cobbs LV, Bandler RC, Streicher C, Cepko CL, Hippen-meyer S, Fishell G (2015) Clonally related forebrain interneurons disperse broadly across both functional areas and structural boundaries. Neuron 87:989–998. CrossRef Medline
41. Mayer C, Bandler RC, Fishell G (2016) Lineage is a poor predictor of interneuron positioning within the forebrain. Neuron 92:45–51. CrossRef Medline
42. Orlando V, Strutt H, Paro R (1997) Analysis of chromatin structure by in vivo formaldehyde cross-linking. Methods 11:205–214. CrossRef Medline
43. Petroff OA (2002) GABA and glutamate in the human brain. Neuroscientist 8:562–573. CrossRef Medline
44. Qiu M, Bulfone A, Martinez S, Meneses JJ, Shimamura K, Pedersen RA, Rubenstein JL (1995) Null mutation of Dlx-2 results in abnormal morphogenesis of proximal first and second branchial arch derivatives and abnormal differentiation in the forebrain. Genes Dev 9:2523–2538. CrossRef Medline
45. Reimer JJ, Turck F (2010) Genome-wide mapping of protein-DNA interaction by chromatin immunoprecipitation and DNA microarray hybridization (ChIP-chip): Part A. ChIP-chip molecular methods. Methods Mol Biol 631:139–160. CrossRef Medline
46. Rubenstein JL, Merzenich MM (2003) Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav 2:255– 267. CrossRef Medline
47. Stühmer T, Anderson SA, Ekker M, Rubenstein JL (2002a) Ectopic expression of the Dlx genes induces glutamic acid decarboxylase and Dlx expression. Development 129:245–252. Medline
48. 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. CrossRef Medline
49. Sultan KT, Han Z, Zhang XJ, Xianyu A, Li Z, Huang K, Shi SH (2016) Clonally related GABAergic interneurons do not randomly disperse but frequently form local clusters in the forebrain. Neuron 92:31–44. CrossRef Medline
50. Turrero García M, Mazzola E, Harwell CC (2016) Lineage relationships do not drive MGE/PoA-derived interneuron clustering in the brain. Neuron 92:52–58. CrossRef Medline
51. Vriend J, Alexiuk NA, Green-Johnson J, Ryan E (1993) Determination of amino acids and monoamine neurotransmitters in caudate nucleus of seizure-resistant and seizure-prone BALB/c mice. J Neurochem 60:1300– 1307. CrossRef Medline
52. Wang B, Lufkin T, Rubenstein JL (2011) Dlx6 regulates molecular properties of the striatum and central nucleus of the amygdala. J Comp Neurol 519:2320–2334. CrossRef Medline
53. Yun K, Garel S, Fischman S, Rubenstein JL (2003) Patterning of the lateral ganglionic eminence by the Gsh1 and Gsh2 homeobox genes regulates striatal and olfactory bulb histogenesis and the growth of axons through the basal ganglia. J Comp Neurol 461:151–165. CrossRef Medline
54. Zerucha T, Stühmer T, Hatch G, Park BK, Long Q, Yu G, Gambarotta A, Schultz JR, Rubenstein JL, 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. Medline
55. 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. CrossRef Medline