A highly conserved enhancer in the Dlx5/Dlx6 intergenic region is the site of cross-regulatory interactions between Dlx genes in the embryonic forebrain

Journal of Neuroscience

Volumn 20, Issue 2, 2000, Pages 709-721

  Zerucha, Ted ^a,b,e   Stühmer, Thorsten ^c   Hatch, Gary ^a   Park, Byung K ^a   Long, Qiaoming ^a   Yu, Guoying ^c,f   Gambarotta, Adrianna ^a   Schultz, Joshua R ^d   Rubenstein, John L R ^c   Ekker, Marc ^a,b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d AMGEN INC   (United States)

^e UNIVERSITY OF CHICAGO   (United States)

^f GENENTECH INC   (United States)

Author keywords

Diencephalon; Evolution; Homeobox; Mouse; Striatum; Telencephalon; Zebrafish

Indexed keywords

HOMEODOMAIN PROTEIN;

ANIMAL TISSUE; ARTICLE; BASE PAIRING; ENHANCER REGION; FEMALE; FOREBRAIN; GENE INSERTION SEQUENCE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REPORTER GENE; TRANSCRIPTION REGULATION; TRANSGENIC MOUSE; ZEBRA FISH;

EID: 0342635450     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-02-00709.2000     Document Type: Article

References (45)

1. Acampora D, Merlo GR, Palcari L, Zeraga B, Postiglione MP, Mantero S, Bober E, Barbieri O, Simeone A, Levi G (1999) Craniofacial, vestibular and bone defects in mice lacking the Distal-less-related gene Dlx5. Development 126:3795-3809.
2. Akimenko M-A, 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.
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. Andrews NC, Faller DV (1991) A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res 19:2499.
6. Becker D, Jiang Z, Knodler P, Deinard AS, Eid R, Kidd KK, Shashikant CS, Ruddle FH, Schughart K (1996) Conserved regulatory element involved in the early onset of Hoxb6 gene expression. Dev Dyn 205:73-81.
7. Beckers J, Gérard M, Duboule D (1996) Transgenic analysis of a potential Hoxd-11 limb regulatory element present in tetrapods and fish. Dev Biol 180:543-553.
8. Bulfone A, Kim HJ, Puelles L, Porteus MH, Grippo JF, Rubenstein JLR (1993a) The mouse Dlx-2 (Tes-1) gene is expressed in spatially restricted domains of the forebrain, face and limbs in midgestation mouse embryos. Mech Dev 40:129-140.
9. Bulfone A, Puelles L, Porteus MH, Frohman MA, Martin GR, Rubenstein JLR (1993b) Spatially restricted expression of Dlx-1, Dlx-2 (Tes1), 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.
10. Cormack BP, Valdivia RH, Falkow S (1996) FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173:33-38.
11. Depew MJ, Liu JK, Long JE, Presley R, Meneses JJ, Pedersen RA, Rubenstein JLR (1999) Dlx5 regulates regional development of the branchial arches and sensory capsules. Development 126:3831-3846.
12. Di Gregorio A, Spagnuolo A, Ristoratore F, Pischetola M, Aniello F, Branno M, Cariello L, Di Lauro R (1995) Cloning of ascidian homeobox genes provides evidence for a primordial chordate cluster. Gene 156:253-257.
13. Dollé P, Price M, Duboule D (1992) Expression of the murine Dlx-1 homeobox gene during facial, ocular and limb development. Differentiation 49:93-99.
14. 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.
15. Feledy JA, Morasso MI, Jang S-I, Sargent TD (1999) Transcriptional activation by the homeodomain protein Distal-less 3. Nucleic Acids Res 27:764-770.
16. Gerard M, Zakany J, Duboule D (1997) Interspecies exchange of a Hoxd enhancer in vivo induces premature transcription and anterior shift of the sacrum. Dev Biol 190:32-40.
17. Gould A, Morrison A, Sproat G, White RAH, Krumlauf R (1997) Positive cross-regulation and enhancer sharing: two mechanisms for specifying overlapping Hox expression patterns. Genes Dev 11:900-913.
18. Hogan B, Constantini F, Lacy E (1986) Manipulating the mouse embryo: a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
19. Kimura C, Takeda N, Suzuki M, Oshimura M, Aizawa S, Matsuo I (1997) Cis-acting elements conserved between mouse and pufferfish Otx2 genes govern the expression in mesencephalic neural crest cells. Development 124:3929-3941.
20. 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.
21. Long Q, Meng A, Wang H, Jessen JR, Farrell MJ, Lin S (1997) GATA-1 expression pattern can be recapitulated in living transgenic zebrafish using GFP reporter gene. Development 124:4105-4111.
22. Luckow B, Schütz G (1987) CAT constructions with multiple unique restriction sites for the functional analysis of eukaryotic promoters and regulatory elements. Nucleic Acids Res 15:5490.
23. Marshall H, Studer M, Pöpperl H, Aparicio S, Kuroiwa A, Brenner S, Krumlauf R (1994) A conserved retinoic acid response element required for early expression of the homeobox gene Hoxb-1. Nature 370:567-571.
24. McGuinness T, Portcus MH, Smiga S, Bulfone A, Kingsley C, Qiu M, Liu JK, Long JE, Xu D, Rubenstein JLR (1996) Sequence, organization, and transcription of the Dlx-1 and Dlx-2 locus. Genomics 35:473-485.
25. Morrison A, Chaudhuri C, Ariza-McNaughton L, Muchamore I, Kuroiwa A, Krumlauf R (1995) Comparative analysis of chicken Hoxb-4 regulation in transgenic mice. Mech Dev 53:47-59.
26. Nonchev S, Maconocie M, Gould A, Morrison A, Krumlauf R (1997) Cross-regulatory interactions between Hox genes and the control of segmental expression in the vertebrate central nervous system. Cold Spring Harb Symp Quant Biol 62:313-323.
27. O'Hara E, Cohen B, Cohen SM, McGinnis W (1993) Distal-less is a downstream gene of Deformed required for ventral maxillary identity. Development 117:847-856.
28. Porteus MH, Bulfone A, Ciaranello RD, Rubenstein JLR (1991) Isolation and characterization of a novel cDNA clone encoding a homeodomain that is developmentally regulated in the ventral forebrain. Neuron 7:221-229.
29. Prefontaine GG, Lemieux ME, Giffin W, Schild-Poulter C, Pope L, LaCasse E, Walker P, Hache RJG (1998) Recruitment of octamer transcription factors to DNA by glucocorticoid receptor. Mol Cell Biol 18:3416-3430.
30. Price M, Lemaistre M, Pischetola M, Di Lauro R, Duboule D (1991) A mouse gene related to distal-less shows a restricted expression in the developing forebrain, Nature 351:748-751.
31. Qiu M, Bulfone A, Ghattas I, Meneses JJ, Christensen L, Sharpe PT, Presley R, Pedersen RA, Rubenstein JLR (1997) Role of the DIlx homeobox genes in proximodistal patterning of the branchial arches: mutations of Dlx-1, Dlx-2, and Dlx-1 and -2 alter morphogenesis of proximal skeletal and soft tissue structures derived from the first and second arches. Dev Biol 185:165-184.
32. Robinson GW, Wray S, Mahon KA (1991) Spatially restricted expression of a member of a new family of murine distal-less homeobox genes in the developing forebrain. New Biol 3:1183-1194.
33. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, a laboratory manual, Ed 2. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
34. Sharpe J, Nonchev S, Gould A, Whiting J, Krumlauf R (1998) Selectivity, sharing and competitive interactions in the regulation of Hoxb genes. EMBO J 17:1788-1798.
35. Shimamura K, Martinez S, Puelles L, Rubenstein JLR (1997) Patterns of gene expression in the neural plate and neural tube subdivide the embryonic forebrain into transverse and longitudinal domains. Dev Neurosci 19:88-96.
36. Simeone A, Acampora D, Pannese M, Desposito M, Stornaiuolo A, Gulisano M, Mallamaci A, Kastury K, Druck T, Huebner K, Boncinelli E (1994) Cloning and characterization of two members of the vertebrate Dlx gene family. Proc Natl Acad Sci USA 91:2250-2254.
37. Stock DW, Ellies DL, Zhao Z, Ekker M, Ruddle FH, Weiss KM (1996) The evolution of the vertebrate Dlx gene family. Proc Natl Acad Sci USA 93:10858-10863.
38. Studer M, Gavalas A, Marshall H, Ariza-McNaughton L, Rijli FM, Chambon P, Krumlauf R (1998) Genetic interactions between Hoxa1 and Horb1 reveal new roles in regulation of early hindbrain patterning. Development 125:1025-1036.
39. Thompson EA (1984) Information gain in joint linkage analysis. IMA J Math Appl Med Biol 1:31-49.
40. Vachon G, Cohen B, Pfeifle C, McGuffin ME, Botas J, Cohen SM (1992) Homeotic genes of the Bithorax complex repress limb development in the abdomen of the Drosophila embryo through the target gene distalless. Cell 71:437-450.
41. van der Hoeven F, Zakany J, Duboule D (1996) Gene transposition in the HoxD complex reveal a hierarchy of regulatory controls. Cell 85:1025-1035.
42. Williams SC, Altmann CR, Chow RL, Hemmati-Brivanlou A, Lang RA (1998) A highly conserved lens transcriptional control element from the Pax-6 gene. Mech Dev 73:225-229.
43. Yee S-P, Rigby PWJ (1993) The regulation of myogenin gene expression during the embryonic development of the mouse. Genes Dev 7:1277-1289.
44. Zerucha T, Muller J-P, Chartrand N, Ekker M (1997) Cross-interactions between two members of the Dlx family of homeobox-containing genes during zebrafish development. Biochem Cell Biol 75:613-622.
45. Zhang H, Hu G, Wang H, Sciavolino P, Iler N, Shen MM, Abate-Shen C (1997) Heterodimerization of Msx and Dlx homeoproteins results in functional antagonism. Mol Cell Biol 17:2920-2932.