The divergent homeobox gene PBX1 is expressed in the postnatal subventricular zone and interneurons of the olfactory bulb

Journal of Neuroscience

Volumn 16, Issue 9, 1996, Pages 2972-2982

  Redmond, Lori ^a   Hockfield, Susan ^a   Morabito, Maria A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

development; differentiation; forebrain; homeobox gene; neurogenesis; olfactory bulb; PBX1; precursor cell; subventricular zone; transcription factor

Indexed keywords

BETA TUBULIN; CYCLINE; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; HOMEOBOX; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERNEURON; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; NORTHERN BLOTTING; OLFACTORY BULB; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RAT; STEM CELL; TELENCEPHALON;

EID: 0029876691     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-09-02972.1996     Document Type: Article

References (58)

1. Acklin SE, van der Kooy D (1993) Clonal heterogeneity in the germinal zone of the developing rat telencephalon. Development 118:175-192.
2. Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 137:433-457.
3. Alvarez-Bolado G, Rosenfeld MG, Swanson LW (1995) Model of forebrain regionalization based on spatiotemporal patterns of POU-III homeobox gene expression, birthdates, and morphological features. J Comp Neurol 355.237-295.
4. 3H-thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp Brain Res 50:329-340.
5. Bignami A, Eng LF, Dahl D, Uyeda CT (1972) Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res 43:429-435.
6. Boncinelli E (1994) Early CNS development: distal-less related genes and forebrain development. Curr Opin Neurobiol 4:29-36.
7. Bravo R, Frank R, Blundell PA, Macdonald-Bravo H (1987) Cyclin/ PCNA is the auxiliary protein of DNA polymerase. Nature 326:515-517.
8. Chang C-P, Shen W-F, Rozenfeld S, Lawrence HJ, Largman C, Cleary ML (1995) Pbx proteins display hexapeptide-dependent cooperative DNA binding with a subset of Hox proteins. Genes Dev 9:663-674.
9. Chen A, Reyes A, Akeson R (1990) Transcription initiation sites and structural organization of the extreme 5′ region of the rat neural cell adhesion molecule gene. Mol Cell Biol 10:3314-3324.
10. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
11. Collarini EJ, Kuhn R, Marshall CJ, Monuki ES, Lemke G, Richardson WD (1992) Down-regulation of the POU transcription factor SCIP is an early event in oligodendrocyte differentiation in vitro. Development 116:193-200.
12. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, Brown R, Baldwin S, Kraemer P, Scheff S, Barthels D, Rajewsky K, Wille W (1994) Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367:455-459.
13. Danielson PE, Forss-Petter S, Brow MA, Calavetta L, Douglass J, Milner RJ, Sutcliffe JG (1988) pIB15: a cDNA clone of the rat mRNA encoding cyclophilin. DNA 7:261-267.
14. Dedera DA, Waller EK, LeBrun DP, Sen-Majumdar A, Stevens ME, Barsh GS, Cleary ML (1993) Chimeric homeobox gene E2A-PBX1 induces proliferation, apoptosis, and malignant lymphomas in transgenic mice. Cell 74:833-843.
15. Easter Jr SS, Ross LS, Frankfurter A (1993) Initial tract formation in the mouse brain. J Neurosci 13:285-299.
16. Eng LF, Vanderhaeghen JJ, Bignami A, Gerstl B (1971) An acidic protein isolated from fibrous astrocytes. Brain Res 28:351-354.
17. Hegel WA, Singson AW, Margolis JS, Bang AG, Posakony JW, Murre C (1993) Dpbx, a new homeobox gene closely related to the human proto-oncogene pbx1. Molecular structure and developmental expression. Mech Dev 41:155-161.
18. Frantz GD, Bohner AP, Akers RM, McConnell SK (1994) Regulation of the POU domain gene SCIP during cerebral cortical development. J Neurosci 14:472-485.
19. Gruss P, Walther C (1992) Pax in development. Cell 69:719-722.
20. Hicks SP, D'Amato CJ (1968) Cell migrations to the isocortex in the rat. Anat Rec 160:619-634.
21. Jaworski DM, Kelly GM, Hockfield S (1994) BEHAB, a new member of the proteoglycan tandem repeat family of hyaluronan-binding proteins that is restricted to the brain. J Cell Biol 125:495-509.
22. Kamps MP, Murre C, Sun X, Baltimore D (1990) A new homeobox gene contributes the DNA binding domain of the t(1;19) translocation protein in the pre-B ALL. Cell 60:547-555.
23. Kishi K (1987) Golgi studies on the development of granule cells of the rat olfactory bulb with reference to migration in the subependymal layer. J Comp Neurol 258:112-124.
24. LeBrun DP, Cleary ML (1994) Fusion with E2A alters the transcriptional properties of the homeodomain protein PBX1 in t(1;19) leukemias. Oncogene 9:1641-1647.
25. Lee MK, Rebhun LI, Frankfurter A (1990a) Posttranslational modification of class III β-tubulin. Proc Natl Acad Sci USA 87:7195-7199.
26. Lee MK, Tuttle JB, Rebhun LI, Cleveland DW, Frankfurter A (1990b) The expression and posttranslational modification of a neuron-specific B-tubulin isotype during chick embryogenesis. Cell Motil Cytoskeleton 17:118-132.
27. Levison SW, Chuang C, Abramson BJ, Goldman JE (1993) The migrational patterns and developmental fates of glial precursors in the rat subventricular zone are temporally regulated. Development 119:611-622.
28. Levison SW, Goldman JE (1993) Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 10:201-212.
29. Lois C, Alvarez-Buylla A (1993) Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci USA 90:2074-2077.
30. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145-1148.
31. Lu Q, Wright DD, Kamps MP (1994) Fusion with E2A converts the Pbx1 homeodomain protein into a constitutive transcriptional activator in human leukemias carrying the t(1;19) translocation. Mol Cell Biol 14:3938-3948.
32. Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173-189.
33. Luskin MB, McDermott K (1994) Divergent lineages for oligodendrocytes and astrocytes originating in the neonatal forebrain subventricular zone. Glia 11:211-226.
34. Maniatis T, Fritsch EF, Sambrook J (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
35. Mathews MB, Bernstein RM, Franza Jr BR, Garrels JI (1984) Identity of the proliferating cell nuclear antigen and cyclin. Nature 309:374-376.
36. Menezes JRL, Luskin MB (1994) Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. J Neurosci 14:5399-5416.
37. Miyachi K, Fritzler MJ, Tan EM (1978) Autoantibody to a nuclear antigen in proliferating cells. J Immunol 121:2228-2234.
38. Monica K, Galili N, Nourse J, Saltman D, Cleary ML (1991) PBX2 and PBX3, new homeobox genes with extensive homology to the human proto-oncogene PBX1. Mol Cell Biol 11:6149-6157.
39. Moody SA, Quigg MS, Frankfurter A (1989) Development of the peripheral trigeminal system in the chick revealed by an isotype-specific anti-beta-tubulin monoclonal antibody. J Comp Neurol 279:567-580.
40. Morshead CM, van der Kooy D (1992) Postmitotic death is the fate of constitutively proliferating cells in the subependymal layer of the adult mouse brain. J Neurosci 12:249-256.
41. Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, Morassutti D, Weiss S, van der Kooy D (1994) Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13:1071-1082.
42. Neuteboom ST, Peltenburg LT, van Dijk MA, Murre C (1995) The hexapeptide LFPWMR in Hoxb-8 is required for cooperative DNA binding with Pbx1 and Pbx2 proteins. Proc Natl Acad Sci USA 92:9166-9170.
43. Nourse J, Mellentin JD, Galili N, Wilkinson J, Stanbridge E, Smith SD, Cleary ML (1990) Chromosomal translocation t(1;19) results in synthesis of a homeobox fusion mRNA that codes for a potential chimeric transcription factor. Cell 60:535-545.
44. Ono K, Tomasiewicz H, Magnuson T, Rutishauser U (1994) N-CAM mutation inhibits tangential neuronal migration and is phenocopied by enzymatic removal of polysialic acid. Neuron 13:595-609.
45. Popperl H, Bienz M, Studer M, Chan SK, Aparicio S, Brenner S, Mann RS, Krumlauf R (1995) Segmental expression of Hoxb-1 is controlled by a highly conserved autoregulatorv loop dependent upon exd/pbx. Cell 81.1031-1042.
46. Porteus MH, Bulfone A, Liu 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 Neurosci 14:6370-6383.
47. Rauskolb C, Peifer M, Wieschaus E (1993) Extradenticle, a regulator of homeotic gene activity, is a homolog of the homeobox-containing human proto-oncogene pbx1. Cell 74:1101-1112.
48. Reynolds BA, Weiss S (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710.
49. Roberts VJ, van Dijk MA, Murre C (1995) Localization of Pbx1 transcripts in developing rat embryos. Mech Dev 51:193-198.
50. Rousselot P, Lois C, Alvarez-Buylla A (1995) Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateral ventricle and the olfactory bulb of aduit mice. J Comp Neurol 351:51-61.
51. Rubenstein JLR, Puelles L (1994) Homeobox gene expression during development of the vertebrate brain. Curr Top Dev Biol 29:1-63.
52. Sullivan KF (1988) Structure and utilization of tubulin isotypes. Annu Rev Cell Biol 4:687-716.
53. Tomasiewicz H, Ono K, Yee D, Thompson C, Goridis C, Rutishauser U, Magnuson T (1993) Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron 11:1163-1174.
54. Treacy MN, Rosenfeld MG (1992) Expression of a family of POU-domain protein regulatory genes during development of the central nervous system. Annu Rev Neurosci 15:139-165.
55. Valverde F, Facal-Valverde MV, Santacana M, Heredia M (1989) Development and differentiation of early generated cells of sublayer VIb in the somatosensory cortex of the rat: a correlated Golgi and autoradiographic study. J Comp Neurol 290:118-140.
56. van Dijk MA, Voorhoeve PM, Murre C (1993) Pbx1 is converted into a transcriptional activator upon acquiring the N-terminal region of E2A in pre-B-cell acute lymphoblastoid leukemia. Proc Natl Acad Sci USA 90:6061-6065.
57. van Dijk MA, Peltenburg LTC, Murre C (1995) Hox gene products modulate the DNA binding activity of Pbx1 and Pbx2. Mech Dev 52:99-108.
58. Wilson DS, Desplan C (1995) Cooperating to be different. Curr Biol 5:32-34.