Dlx-2 homeobox gene controls neuronal differentiation in primary cultures of developing basal ganglia

Journal of Molecular Neuroscience

Volumn 8, Issue 2, 1997, Pages 93-113

  Ding, Min ^a   Robel, Laurence ^a,c   James, Alaina J ^a,d   Eisenstat, David D ^b   Leckman, James F ^a   Rubenstein, John L R ^b   Vaccarino, Flora M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HÔPITAL ROBERT DEBRÉ   (France)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Cell culture; Differentiation; Dlx 2; Homeobox; Microtubule associated proteins; Neurite outgrowth

Indexed keywords

DISTAL LESS HOMEOBOX PROTEINS; DISTAL-LESS HOMEOBOX PROTEINS; DNA BINDING PROTEIN; HOMEODOMAIN PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; TES PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL; ANTIBODY SPECIFICITY; ARTICLE; BASAL GANGLION; CELL CULTURE; CELL DIFFERENTIATION; CELL DIVISION; CHEMISTRY; CYTOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HOMEOBOX; IMMUNOLOGY; IN SITU HYBRIDIZATION; NERVE CELL; NEURITE; NUCLEIC ACID PROBE; PHENOTYPE; PHYSIOLOGY; PREGNANCY; RAT; RHOMBENCEPHALON; TELENCEPHALON; ULTRASTRUCTURE;

ANIMALS; ANTIBODY SPECIFICITY; ANTISENSE ELEMENTS (GENETICS); BASAL GANGLIA; CELL DIFFERENTIATION; CELL DIVISION; CELLS, CULTURED; DNA-BINDING PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HOMEOBOX; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MICROTUBULE-ASSOCIATED PROTEINS; NEURITES; NEURONS; PHENOTYPE; PREGNANCY; RATS; RHOMBENCEPHALON; TELENCEPHALON; TRANSCRIPTION FACTORS;

EID: 0031110363     PISSN: 08958696     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF02736776     Document Type: Article

References (67)

1. Akimenko M. A., Ekker M., Wegner J., Lin W., and 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. Alho H., Ferrarese C., Vicini S., and Vaccarino F. M. (1988) Subsets of GABAergic neurons in dissociated cell cultures of neonatal rat cerebral cortex show co-localization with specific modulator peptides. Dev. Brain Res. 39, 193-204.
3. Anderson S. A., Qiu M.-S., Bulfone A., Meneses J., Pederson R., and Rubenstein J. L. R. (1995) Functional analysis of Dlx-1 and Dlx-2 using gene replacement. Soc. Neurosci. Abstracts 21, 793.
4. Bennett C. F., Chiang M. Y., Chan H., Shoemaker J. E., and Mirabelli C. K. (1992) Cationic lipids enhance cellular uptake and activity of phosphorothioate antisense oligonucleotides. Mol. Pharmacol. 41, 23-33.
5. Bielinska A., Shivdasani R. A., Zhang L., and Nabel G. J. (1990) Regulation of gene expression with double-stranded phosphorothioate oligonucleotides. Science 250, 997-1000.
6. Binder L. I., Frankfurter A., Kim H., Caceres A., Payne M. R., and Rebhun L. I. (1986a) Heterogeneity of microtubule-associated protein 2 during brain development. Proc. Natl. Acad. Sci. USA 81, 5613-5617.
7. Binder L. I., Frankfurter A., and Rebhun L. I. (1986b) Differential localization of MAP-2 and tau in mammalian neurons in situ. Ann. NY Acad. Sci. 466, 145-166.
8. Bloch-Gallego E., Le Roux I., Joliot A. H., Volovitch M., Henderson C. E., and Prochiantz A. (1993) Antennapedia homeobox peptide enhances growth and branching of embryonic chicken motoneurons in vitro. J. Cell Biol. 120,485-492.
9. Bradley R. S., Cowin P., and Brown A. M. C. (1993) Expression of Wnt-1 in PC12 cells results in modulation of Plakoglobin and E-cadherin and increased cellular adhesion. J. Cell Biol. 123, 1857-1865.
10. Bulfone A., Puelles L., Porteus M. H., Frohman M. A., Martin G. R., and Rubenstein J. L. R. (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.
11. Caceres A., Banker G., and Binder L. (1986) Immunocytochemical localization of tubulin and microtubule-associated protein 2 during the development of hippocampal neurons in culture. J. Neurosci. 6, 714-722.
12. Caceres A. and Kosik K. S. (1990) Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343, 461-463.
13. Caceres A., Mautino J., and Kosik K. S. (1992) Suppression of MAP2 in cultured cerebellar macroneurons inhibits minor neurite extension. Neuron 9, 607-618.
14. Castrillo J.-L., Theill L. E., and Karin M. (1991) Function of the homeodomain protein GHF1 in pituitary proliferation. Science 253, 197-199.
15. Chamak B. and Prochiantz A. (1989) Influence of extracellular matrix proteins on the expression of neuronal polarity. Development 106, 483-491.
16. Chatelin L., Volovitch M., Joliot A. H., Perez F., and Prochiantz A. (1996) Transcription factor Hoxa-5 is taken up by cells in culture and conveyed to their nuclei. Mech. Dev. 55, 111-117.
17. Chiang M.-Y., Chan H., Zounes M. A., Freier S. M., Lima W. F., and Bennett C. F. (1991) Antisense oligonucleotides inhibit intercellular adhesion molecule 1 expression by two distinct mechanisms. J. Biol. Chem. 266, 18,162-18,171.
18. Cohen S. M., Bronner G., Kuttner F., Jurgens G., and Jackle H. (1989) Distal-less encodes a homeodomain protein required for limb development in Drosophila. Nature 338, 432-434.
19. Cohen S. M. (1990) Specification of limb development in the Drosophila embryo by positional cues from segmentation genes. Nature 343, 173-177.
20. Craig A. M. and Banker G. (1994) Neuronal polarity. Ann. Rev. Neurosci. 17, 267-310.
21. De Camilli P., Navone F., Miller P., Theurkauf W. E., and Vallee R. B. (1984) Distribution of microtubule-associated protein 2 (MAP2) in the nervous system of the rat studied by immunofluorescence. Neuroscience 11, 819-846.
22. Dinsmore J. H. and Solomon F. (1991) Inhibition of MAP2 expression affects both morphological and cell division phenotypes of neuronal differentiation. Cell 64, 817-826.
23. Dotti C. G., Banker G. A., and Binder L. I. (1987) The expression and distribution of the microtubule-associated proteins tau and microtubule-associated protein 2 in hippocampal neurons in the rat in situ and in cell culture. Neuroscience 23, 121-130.
24. Edelman G. M. and Jones F. S. (1993) Outside and downstream of the homeobox. J. Biol. Chem. 268, 20,683-20,686.
25. Eisenberg L. M., Ingham P. W., and Brown A. M. C. (1992) Cloning and characterization of a novel Drosophila Wnf gene, Dwnt-5, a putative downstream target of the homeobox gene Distal-less. Dev. Biol. 154, 73-83.
26. Ekker M., Akimenko M.-A., Bremiller R., and Westerfield M. (1992) Regional expression of three homeobox transcripts in the inner ear of zebrafish embryos. Neuron 9, 27-35.
27. Fletcher T. L., Cameron P., De Camilli P., and Banker G. (1991) The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture. J. Neurosci. 11, 1617-1626.
28. Greenstein D., Hird S., Plasterk R. H., Andachi Y., Kohara Y., Finney M., Wang B., Finney M., and Ruvkun G. (1994) Targeted mutations in the Caenorhabditis elegans POU homeo box gene ceh-18 cause defects in oocyte cell cycle arrest, gonad migration, and epidermal differentiation. Genes Dev. 8, 1935-1948.
29. Guvakova M. A., Yakubov L. A., Vlodavsky I., Tokinson J. L., and Stein C. A. (1995) Phosphorothioate oligodeoxynudeotides bind to basic fibroblast growth factor, inhibit its binding to cell surface receptors, and remove it from low affinity binding sites on extracellular matrix. J. Biol. Chem. 270, 2620-2627.
30. Holt C. E., Garlick N., and Cornel E. (1990) Lipofection of cDNAs in the embryonic vertebrate central nervous system. Neuron 4, 203-214.
31. Immergluck K., Lawrence P. A., and Bienz M. (1990) Induction across germ layers in Drosophila mediated by a genetic cascade. Cell 62, 261-268.
32. Joliot A., Le Roux I., Bloch-Gallego E., and Prochiantz A. (1994) Neurotrophic activity of a homeobox peptide. Prog. Neurobiol. 42, 309-311.
33. Jones K. H. and Senft J. A. (1985) An improved method to determine cell viability by simultaneous staining with fluorescein diacetate-propidium iodide. J. Histochem. Cytochem. 33, 77-79.
34. Kalcheva N., Albala J., O'Guin K., Rubino H., Garner C., and Shafit-Zagardo B. (1995) Genomic structure of human microtubular-associated protein 2 (MAP-2) and characterization of newly identified isoforms. Proc. Natl. Acad. Sci. USA 92, 10,894-10,898.
35. Lallier T. and Bronner-Fraser M. (1993) Inhibition of neural crest cell attachment by integrin antisense oligonucleotides. Science 259, 692-695.
36. Lewis S. A., Ivanov I. E., Lee G.-H., and Cowan N. J. (1989) Organization of microtubules in dendrites and axons is determined by a short hydrophobic zipper in microtubule-associated proteins MAP2 and tau. Nature 342, 498-505.
37. Loke S. L., Stein C. A., Zhang X. H., Mori K., Nakanishi N., Subasinghe C., Cohen S. J., and Neckers L. M. (1989) Characterization of oligonucleotide transport into livinge cells. Proc. Natl. Acad. Sci. USA 86, 3474-3478.
38. Malone R. W., Feigner P. L., and Verma I. M. (1989) Cationic liposome-mediated RNA transfection. Proc. Natl. Acad. Sci. USA 86, 6077-6081.
39. Marshall W. S. and Caruthers M. H. (1993) Phosphorothioate DNA as a potential therapeutic drug. Science 259, 1564-1570.
40. Matus A. (1994) Stiff microtubules and neuronal morphology. Trends Neurosci. 17, 19-23.
41. McCarthy M. M., Masters D. B., Rimvall K., Schwartz-Giblin S., and Pfaff D. W. (1994) Intracerebral administration of antisense oligodeoxynucleotides to GAD65 and GAD67 modulate reproductive behavior in the female rat. Brain Res. 636, 209-220.
42. Miller D. M., Shen M. M., Shamu C. E., Burglin T. R., Ruvkun G., Dubois M. L., Ghee M., and Wilson L. (1992) C. elegans unc-4 gene encodes a homeodomain protein that determines the pattern of synaptic input to specific motor neurons. Nature 355, 841-845.
43. Papalopulu N. and 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.
44. Porteus M. H., Bulfone A., Ciaranello R. D., and Rubenstein J. L. R. (1991) A partial cDNA sequence of the Dlx-2 cDNA. Neuron 9, 187.
45. Porteus M. H., Bulfone A., Liu J. K., Puelles L., Lo L. C., and Rubenstein J. L. R. (1994) DLX-2, MASH-1, and MAP2 expression and bromodeoxyuridine incorporation define molecularly distinct cell populations in the embryonic mouse forebrain. J. Neurosci. 14, 6370-6383.
46. Price M., Lemaistre M., Pischetola M., Di Lauro R., and Duboule D. (1991) A mouse gene related to Distal-less shows a restricted expression in the developing forebrain. Nature 351, 748-751.
47. Prochiantz A. (1995) Neuronal polarity: giving neurons heads and tails. Neuron 15, 743-746.
48. Qiu M., Bulfone A., Martinez S., Meneses J. J., Shimamura K., Pedersen R. A., and Rubenstein J. L. R. (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.
49. Retaux S., McNeill L., and Harris W. A. (1996) Engrailed, retinotectal targeting, and axonal patterning in the midbrain during Xenopus development: an antisense study. Neuron 16, 63-75.
50. Reuter R., Panganibam G. E. F., Hoffmann F. M., and Scott M. P. (1990) Homeotic genes regulate the spatial expression of putative growth factors in the visceral mesoderm of Drosophila embryos. Development 110, 1031-1040.
51. Robel L., Ding M., James A. J., Lin X., Leckman J. F., and Vaccarino F. M. (1995) Fibroblast growth factor 2 increases Otx2 expression in precursor cells from the mammalian telencephalon. J. Neurosci. 15, 7879-7891.
52. Robinson G. W., Wray S., and Mahon K. A. (1991) Spatially restricted expression of a member of a new family of murine Distal-less homeobox genes in the developing forebrain. New Biologist 3, 1183-1194.
53. Robinson G. W. and Mahon K. A. (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.
54. Rousselet A., Autillo-Touati A., Araud D., and Prochiantz A. (1990) In vitro regulation of neuronal morphogenesis and polarity by astrocyte-derived factors. Dev. Biol. 137, 33-45.
55. Schoenfeld T. A., McKerracher L., Obar R., and Vallee R. B. (1989) MAP1A and MAP1B are structurally related microtubule associated proteins with distinct developmental patterns in the CNS. J. Neurosci. 9, 1712-1730.
56. Selski D. J., Thomas N. E., Coleman P. D., and Rogers K. E. (1993) The human brain homeogene, DLX-2, cDNA sequence and alignment with the murine homologue. Gene 132, 301-303.
57. Simeone A., Gulisano M., Acampora D., Stornaiuolo A., Rambaldi M., and Boncinelli E. (1992) Two vertebrate homeobox genes related to the Drosophila empty spiracles gene are expressed in the embryonic cerebral cortex. EMBO J. 11, 2541-2550.
58. Simeone A., Acampora D., Pannese M., D'Esposito M., Stornaiuolo A., Gulisano M., Mallamaci A., Kastury K., Druck T., Huebner K., et al. (1994) Cloning and characterization of two members of the vertebrate DIx gene family. Proc. Natl. Acad. Sci. USA 91, 2250-2254.
59. Stein C. A. and Cheng Y.-C. (1993) Antisense oligonucleotides as therapeutic agents - is the bullet really magical? Science 261, 1004-1011.
60. Tucker R. P., Binder L. I., and Matus A. I. (1988) Differential localization of the high- and low-molecular weight variants of MAP2 in the developing retina. Brain Res. 466, 313-318.
61. Vaccarino F. M., Schwartz M. L., Hartigan D., and Leckman J. F. (1995) Effect of basic fibroblast growth factor on the genesis of excitatory and inhibitory neurons in primary cultures of cells from the mammalian telencephalon. CerCx 1, 1047-3211.
62. van Leeuwen F., Harryman Samos C., and Nusse R. (1994) Biological activity of soluble wingless protein in cultured Drosophila imaginal disk cells. Nature 368, 342-344.
63. Wahlestedt C., Golanov E., Yamamoto S., Yee F., Ericson H., Yoo H., Inturrisi C. E., and Reis D. J. (1993) Antisense oligodeoxynucleotides to NMDA-R1 receptor channel protect cortical neurons from excitotoxicity and reduce focal ischaemic infarctions. Nature 363, 260-263.
64. Weisshaar B., Doll T., and Matus A. (1992) Reorganization of the microtubular cytoskeleton by embryonic microtubule-associated protein 2 (MAP2c). Development 116, 1151-1161.
65. Weisshaar B. and Matus A. (1993) Microtubule-associated protein 2 and the organization of cellular microtubules. J. Neurocytol. 22, 727-734.
66. White J. G., Southgate E., and Thomson J. N. (1992) Mutations in Caenorhabditis elegans unc-4 gene alter the synaptic input to ventral cord motor neurons. Nature 355, 838-841.
67. Zhao G. Q., Zhao S., Zhou X., Eberspaecher H., Solursh M., and 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.