DLX-1, DLX-2, and DLX-5 expression define distinct stages of basal forebrain differentiation

Journal of Comparative Neurology

Volumn 414, Issue 2, 1999, Pages 217-237

  Eisenstat, David D ^a   Liu, Jen Kuei ^a   Mione, Marina ^a   Zhong, Weimin ^b   Yu, Guoying ^a   Anderson, Stewart A ^a   Ghattas, Ingrid ^a   Puelles, Luis ^c   Rubenstein, John L R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF MURCIA   (Spain)

Author keywords

Basal ganglia; Dlx; Embryo; Forebrain

Indexed keywords

CELL PROTEIN; RNA;

ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL MIGRATION; CORPUS STRIATUM; EMBRYO; FOREBRAIN; GENE EXPRESSION; GLOBUS PALLIDUS; HOMEOBOX; MITOSIS; MOUSE; NERVE CELL DIFFERENTIATION; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TELENCEPHALON;

3T3 CELLS; ANIMALS; ANTIBODY SPECIFICITY; BASAL GANGLIA; CELL DIFFERENTIATION; CELL NUCLEUS; CEREBRAL VENTRICLES; CYTOPLASM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; ISOMERISM; MICE; MITOSIS; MUTAGENESIS; NEURONS; PROSENCEPHALON; RECOMBINANT PROTEINS; RNA, MESSENGER; S PHASE; TRANSCRIPTION FACTORS;

EID: 0345192350     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19991115)414:2<217::AID-CNE6>3.0.CO;2-I     Document Type: Article

References (85)

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.
2. Anderson SA, Qiu M, Bulfone A, Eisenstat DD, Meneses J, Pederson R, Rubenstein JLR. 1997a. 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.
3. Anderson SA, Eisenstat DD, Shi L, Rubenstein JLR. 1997b. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474-476.
4. Anderson SA, Mione M, Yun K, Rubenstein JLR. 1999. Differential origins of neocortical projection and local circuit neurons; role of Dlx genes in neocortical interneuronogenesis. Cerebral Cortex (in press).
5. Asano M, Emori Y, Saigo K, Shiokawa K. 1992. Isolation and characterization of a Xenopus cDNA which encodes a homeodomain highly homologous to Drosophila Distal-less. J Biol Chem 267:5044-5047.
6. Beauchemin M, Savard P. 1992. Two distal-less related homeobox-containing genes expressed in regeneration blastemas of the newt. Dev Biol 154:55-65.
7. Bhide PG. 1996. Cell cycle kinetics in the embryonic mouse corpus striatum. J Comp Neurol 374:506-522.
8. Bittman K, Owens DF, Kriegstein AR, LoTurco JJ. 1997. Cell coupling and uncoupling in the ventricular zone of developing neocortex. J Neurosci 17:7037-7044.
9. Broadus J, Doe CQ. 1997. Extrinsic cues, intrinsic cues and microfilaments regulate asymmetric protein localization in Drosophila neuroblasts. Curr Biol 7:827-835.
10. Bulfone A, Kim H-J, 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.
11. Bulfone A, Puelles L, Porteus MH, Frohman MA, Martin GR, Rubenstein JLR. 1993b. 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.
12. Bulfone A, Smiga SM, Shimamura K, Peterson A, Puelles L, Rubenstein JLR. 1995. T-Brain-1: a homolog of Brachyury whose expression defines molecularly distinct domains within the cerebral cortex. Neuron 15:63-78.
13. Bulfone A, Wang F, Hevner R, Anderson S, Cutforth T, Chen S, Meneses J, Pedersen R, Axel R, Rubenstein JLR. 1998. An olfactory sensory map develops in the absence of normal projection neurons or GABAergic interneurons. Neuron 21:1273-1282.
14. Casares F, Mann RS. 1998. Control of antennal versus leg development in Drosophila. Nature 392:723-726.
15. Casarosa S, Fode C, Guillemot F. 1999. Mash1 regulates neurogenesis in the ventral telencephalon. Development 126:525-534.
16. Chen C, Okayama H. 1987. High efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 7:2745-2752.
17. Chenn A, McConnell SK. 1995. Cleavage orientation and the asymmetric inheritance of Notch-1 immunoreactivity in mammalian, neurogenesis. Cell 82:631-641.
18. Chenn A, Zhang YA, Chang BT, McConnell SK. 1998. Intrinsic polarity of mammalian neuroepithelial cells. Mol Cell Neurosci 11:183-193.
19. Cohen SM. 1990. Specification of limb development in the Drosophila embryo by positional cues from segmentation genes. Nature 343:173-177.
20. Cohen SM, Jürgens G. 1989. Proximal-distal pattern formation in Drosophila: cell autonomous requirement for Distal-less gene activity in limb development. EMBO J 8:2045-2055.
21. 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.
22. Di Gregorio A, Spagnuolo A, Ristoratore F, Pischetola M, Aniello F, Branno, Cariello L, Di Lauro R. 1995. Cloning of ascidian homeobox genes provides evidence for a primordial chordate cluster. Gene 156:253-257.
23. Dirkson ML, Mathers P, Jamrich M. 1993. Expression of a Xenopus Distal-less homeobox gene involved in forebrain and cranio-facial development. Mech Dev 41:121-128.
24. Dollè P, Price M, Duboule D. 1992. Expression of the murine Dlx-1 homeobox gene during facial, ocular and limb development. Differentiation 49:93-99.
25. Dong H, O'Brien RJ, Fung ET, Lanahan AA, Worley PF, Huganir RL. 1997. GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature 386:279-84.
26. Eisenstat D, Shimamura K, Bulfone A, Liu J-K, Martinez S, Puelles L, Fan CM, Tessier-Lavigne M, Schachner M, Rubenstein J. 1994. The prosomeric model of the embryonic forebrain. Soc Neurosci Abstr 20:253.
27. Ellies DL, Langille RM, Martin CC, Akimenko MA, Ekker M. 1997. Specific craniofacial cartilage dysmorphogenesis coincides with a loss of dlx gene expression in retinoic acid-treated zebrafish embryos. Mech Dev 61:23-36.
28. Fan CM, Kuwana E, Bulfone A, Fletcher CF, Copeland NG, Jenkins NA, Crews S, Martinez S, Puelles L, Rubenstein JL, Tessier-Lavigne M. 1996. Expression patterns of two murine homologs of Drosophila single-minded suggest possible roles in embryonic patterning and in the pathogenesis of Down syndrome. Mol Cell Neurosci 7:1-16.
29. Ferrari D, Sumoy L, Gannon J, Sun H, Brown AM, Upholt WB, Kosher RA. 1995. The expression pattern of the Distal-less homeobox-containing gene Dlx-5 in the developing chick limb bud suggests its involvement in apical ectodermal ridge activity, pattern formation, and cartilage differentiation. Mech Dev 52:257-264.
30. Ghattas IR, Sanes JR, Majors JE. 1991. The encephalomyocarditis virus internal ribosome entry site allows efficient coexpression of two genes from a recombinant proviris in cultured cells and in embryos. Mol Cell Biol 11:5848-5859.
31. Harlow E, Lane D. 1988. Antibodies: a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
32. Holland ND, Panganiban G, Henyey EL, Holland LZ. 1996. Sequence and developmental expression of AmphiDll, an amphioxus Distal-less gene transcribed in the ectoderm, epidermis and nervous system: insights into the evolution of craniate forebrain and neural crest. Development 122:2911-2920.
33. Jiang YJ, Smithers L, Lewis J. 1998. Vertebrate segmentation: the clock is linked to Notch signalling. Curr Biol 8:R868-R871.
34. Knoblich JA, Jan LY, Jan YN. 1995. Asymmetric segregation of Numb and Prospero during cell division. Nature 377:624-627.
35. Kohtz JD, Baker DP, Corte G, Fishell G. 1998. Regionalization within the mammalian telencephalon is mediated by changes in responsiveness to sonic hedgehog. Development 125:5079-5089.
36. Liu J-K, 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.
37. Lois C, Alvarez-Buylla A. 1994. Long-distance neuronal migration in the adult mammalian brain. Science 264:1145-1148.
38. Lois C, Garcia-Verdugo JM, Alvarez-Buylla A. 1996. Chain migration of neuronal precursors. Science 271:978-981.
39. Luskin MB. 1993. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173-189.
40. McConnell SK, Kaznowski CE. 1991. Cell cycle dependence of laminar determination in developing cerebral cortex. Science 254:282-285.
41. McGuinness T, Porteus MH, Smiga S, Bulfone A, Kingsley C, Qiu M, Liu J-K, Long JE, Xu D, Rubenstein JLR. 1996. Sequence, organization, and transcription of the Dlx-1 and Dlx-2 locus. Genomics 35:473-485.
42. Mione MC, Cavanagh JFR, Harris B, Parnavelas JG. 1997. Cell fate specification and symmetrical/asymmetrical divisions in the developing cerebral cortex. J Neurosci 17:2018-2029.
43. Miyama S, Takahashi T, Nowakowski RS, Caviness VS Jr. 1997. A gradient in the duration of the G1 phase in the murine neocortical proliferative epithelium. Cerebral Cortex 7:678-689.
44. Morasso MI, Yonescu R, Griffin CA, Sargent TD. 1997. Localization of human DLX8 to chromosome 17q21.3-q22 by fluorescence in situ hybridization. Mamm Genome 8:302-303.
45. Nakamura S, Stock DW, Wydner KL, Bollekens JA, Takeshita K, Nagai BM, Chiba S, Kitamura T, Freeland TM, Zhao Z, Minowada J, Lawrence JB, Weiss KM, Ruddle FH. 1996. Genomic analysis of a new mammalian distal-less gene: Dlx7. Genomics 38:314-324.
46. Özcelik T, Porteus MH, Rubenstein JL, Francke U. 1992. DLX2 (TES1), a homeobox gene of the Distal-less family, assigned to conserved regions on human and mouse chromosomes 2. Genomics 13:1157-1161.
47. Page M, Baines MG, Thorpe R. 1994. Preparation of purified immunoglobulin G (IgG). In: Walker JM, editor. Methods in molecular biology, vol 32. Basic protein and peptide protocols. Totowa, NJ: Humana Press Inc. p 407-432.
48. Panganiban G, Nagy L, Carroll SB. 1994. The role of the Distal-less gene in the development and evolution of insect limbs. Curr Biol 4:671-675.
49. Panganiban G, Sebring A, Nagy L, Carroll S. 1995. The development of crustacean limbs and the evolution of arthropods. Science 270:1363-1366.
50. Papalopulu N, Kintner C. 1993. Xenopus Distal-less related homeobox genes are expressed in the developing forebrain and are induced by planar signals. Development 117:961-975.
51. 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.
52. Porteus MH, Bulfone A, Lui J-K, Puelles L, Lo L-C, Rubenstein JLR. 1994. DLX-2, MASH-1, and MAP-2 expression and bromodeoxyuridine incorporation define molecularly distinct cell populations in the embryonic mouse forebrain. J. Neuroscience 14:6370-6383.
53. 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.
54. Puelles L, Rubenstein JLR. 1993. Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization. Trends Neurosci 16:472-479.
55. Qiu M, Bulfone A, Martinez S, Meneses JJ, Shimamura K, Pedersen RA, Rubenstein JLR. 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.
56. Qiu M, Bulfone A, Ghattas I, Meneses JJ, Christensen L, Sharpe PT, Presley R, Pedersen RA, Rubenstein JLR. 1997. Role of the Dlx homeobox genes in proximodistal patterning of the branchial arches: mutations of Dlx-1, Dlx-2, and Dlx-1 and Dlx-2 alter morphogenesis of proximal skeletal and soft tissue structures derived from the first and second arches. Dev Biol 185:165-184.
57. Qiu M, Shimamura K, Sussel L, Chen S, Rubenstein JLR. 1998. Control of anteroposterior and dorsoventral domains of Nkx-6.1 gene expression relative to other Nkx genes during vertebrate CNS development. Mech Dev 72:77-88.
58. Quinn LM, Latham SE, Kalionis B. 1998. Adistal-less class homeobox gene, DLX4, is a candidate for regulating epithelial-mesenchymal cell interactions in the human placenta. Placenta 19:87-93.
59. Rieckhof GE, Casares F, Ryoo HD, Abu-Shaar M, Mann RS. 1997. Nuclear translocation of extradenticle requires homothorax, which encodes an extradenticle-related homeodomain protein. Cell 91:171-183.
60. Robinson GW, Mahon KA. 1994. Differential and overlapping expression domains of Dlx-2 and Dlx-3 suggest distinct roles for Distal-less homeobox genes in craniofacial development. Mech Dev 48:199-215.
61. 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.
62. Rubenstein JL, Puelles L. 1994. Homeobox gene expression during development of the vertebrate brain. Curr Top Dev Biol 29:1-63.
63. Rubenstein JLR, Martinez S, Shimamura K, Puelles L. 1994. The embryonic vertebrate forebrain: the prosomeric model. Science 266:578-580.
64. Rubenstein JLR, Shimamura K. 1997. Regulation of patterning and differentiation in the embryonic vertebrate forebrain. In: Cowan SM, Jessel TM, Zipursky SL, editors. Molecular and cellular approaches to neural development. Oxford: Oxford University Press.
65. Rubenstein JLR, Shimamura K, Martinez S, Puelles L. 1998. Regionalization of the prosencephalic neural plate. Annu Rev Neurosci 21:445-477.
66. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning, 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
67. Selski DJ, Thomas NE, Coleman PD, Rogers KE. 1993. The human brain homeogene, DLX-2: cDNA sequence and alignment with the murine homologue. Gene 132:301-303.
68. Shen CP, Jan LY, Jan YN. 1997. Miranda is required for the asymmetric localization of Prospero during mitosis in Drosophila. Cell 90:449-458.
69. Shen CP, Knoblich JA, Chan YM, Jiang MM, Jan LY, Jan YN. 1998. Miranda as a multidomain adapter linking apically localized Inscuteable and basally localized Staufen and Prospero during asymmetric cell division in Drosophila. Genes Dev 12:1837-1846.
70. Shimamura K, Rubenstein JLR. 1997. Inductive interactions direct early regionalization of the mouse forebrain. Development 124:2709-2718.
71. Shimamura K, Hirano S, McMahon AP, Takeichi M. 1994. Wnt-1-dependent regulation of local E-cadherin and αN-catenin expression in the embryonic mouse brain. Development 120:2225-2234.
72. Shimamura K, Hartigan DJ, Martinez S, Puelles L, Rubenstein JLR. 1995. Longitudinal organization of the anterior neural plate and neural tube. Development 121:3923-3933.
73. 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.
74. Simeone A, Acampora D, Pannese M, D'Esposito 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.
75. 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.
76. Sussel L, Kimura S, Rubenstein JLR. 1999. Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126:3359-3370.
77. Takahashi T, Nowakowski RS, Caviness VS Jr. 1993. Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse. J Neurosci 13:820-833.
78. Takahashi T, Nowakowski RS, Caviness VS Jr. 1995. Early ontogeny of the secondary proliferative population of the embryonic murine cerebral wall. J Neurosci 15:6058-6068.
79. Thomas BL, Porteus MH, Rubenstein JLR, Sharpe PT. 1995. The spatial localization of Dlx-2 during tooth development. Connective Tissue Res. 31:1-8.
80. 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 Distal-less. Cell 71:437-450.
81. Weinmaster G. 1997. The ins and outs of notch signaling. Mol Cell Neurosci 9:91-102.
82. Yang L, Zhang H, Hu G, Wang H, Abate-Shen C, Shen MM. 1998. An early phase of embryonic Dlx5 expression defines the rostral boundary of the neural plate. J Neurosci 18:8322-8330.
83. Zerucha T, Muller JP, 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.
84. Zhao GQ, Zhao S, Zhou X, Eberspaecher H, Solursh M, de Crombrugghe B. 1994. rDlx, a novel distal-less-like homeoprotein is expressed in developing cartilages and discrete neuronal tissues. Dev Biol 164:37-51.
85. Zhong W, Feder NJ, Jiang M-M, Jan LY, Jan YN. 1996. Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron 17:43-53.