Home LiteratureArticle Details
PMID: 9278539 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Cell coupling and uncoupling in the ventricular zone of developing neocortex.

Bittman K, Owens DF, Kriegstein AR, LoTurco JJ

Abstract

Cells within the ventricular zone (VZ) of developing neocortex are coupled together into clusters by gap junction channels. The specific role of clustering in cortical neurogenesis is unknown; however, clustering provides a means for spatially restricted local interactions between subsets of precursors and other cells within the VZ. In the present study, we have used a combination of 5-bromo-2'-deoxyuridine (BrDU) pulse labeling, intracellular biocytin labeling, and immunocytochemistry to determine when in the cell cycle VZ cells couple and uncouple from clusters and to determine what cell types within the VZ are coupled to clusters. Our results indicate that clusters contain radial glia and neural precursors but do not contain differentiating or migrating neurons. In early neurogenesis, all precursors in S and G2 phases of the cell cycle are coupled, and approximately half of the cells in G1 are coupled. In late neurogenesis, however, over half of the cells in both G1 and S phases are not coupled to VZ clusters, whereas all cells in G2 are coupled to clusters. Increased uncoupling in S phase during late neurogenesis may contribute to the greater percentage of VZ cells exiting the cell cycle at this time. Consistent with this hypothesis, we found that pharmacologically uncoupling VZ cells with octanol decreases the percentage of VZ cells that enter S phase. These results demonstrate that cell clustering in the VZ is restricted to neural precursors and radial glia, is dynamic through the cell cycle, and may play a role in regulating neurogenesis.

MeSH Terms
Animals Bromodeoxyuridine/metabolism Cell Communication/physiology Cell Cycle Cerebral Cortex/cytology,embryology Cerebral Ventricles/cytology,embryology Epithelial Cells Female G1 Phase G2 Phase Gap Junctions/metabolism Lysine/analogs & derivatives,metabolism Mice Pregnancy S Phase Tubulin/analysis
Chemicals
Tubulin Bromodeoxyuridine biocytin Lysine
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Bittman K
Department of Physiology and Neurobiology, University of Connecticut, Storrs, Connecticut 06269-4156, USA.
Owens D F
Kriegstein A R
LoTurco J J
References (32)
32 references, click to expand
  1. Dye coupling and possible electrotonic coupling in the guinea pig neocortical slice.
    Science. 1981 Jan 2;211(4477):67-70 PMID: 7444449
  2. Activation of the GABAA receptor inhibits the proliferative effects of bFGF in cortical progenitor cells.
    Eur J Neurosci. 1997 Feb;9(2):291-8 PMID: 9058049
  3. Regeneration of rat tracheal epithelium: changes in gap junctions during specific phases of the cell cycle.
    Exp Lung Res. 1982 Feb;3(1):47-56 PMID: 7060542
  4. Differential expression of three gap junction proteins in developing and mature brain tissues.
    Proc Natl Acad Sci U S A. 1989 Dec;86(24):10148-52 PMID: 2557621
  5. Involvement of gap junctions in tumorigenesis: transfection of tumor cells with connexin 32 cDNA retards growth in vivo.
    Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10701-5 PMID: 1660148
  6. Monoclonal antibody reveals radial glia in adult avian brain.
    J Comp Neurol. 1987 Oct 8;264(2):159-70 PMID: 2445794
  7. Dispersion of neural progenitors within the germinal zones of the forebrain.
    Nature. 1993 Apr 15;362(6421):636-8 PMID: 8464514
  8. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall.
    J Neurosci. 1995 Sep;15(9):6046-57 PMID: 7666188
  9. Gap junctional communication and development.
    Trends Neurosci. 1989 Jan;12(1):12-6 PMID: 2471332
  10. Specification of cerebral cortical areas.
    Science. 1988 Jul 8;241(4862):170-6 PMID: 3291116
  11. Transcriptional downregulation of gap-junction proteins blocks junctional communication in human mammary tumor cell lines.
    J Cell Biol. 1992 Sep;118(5):1213-21 PMID: 1324944
  12. Differential expression of connexins during neocortical development and neuronal circuit formation.
    J Neurosci. 1997 May 1;17(9):3096-111 PMID: 9096144
  13. Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse.
    J Neurosci. 1993 Feb;13(2):820-33 PMID: 8426239
  14. Embryonic vertebrate central nervous system: revised terminology. The Boulder Committee.
    Anat Rec. 1970 Feb;166(2):257-61 PMID: 5414696
  15. Central nervous system neurons migrate on astroglial fibers from heterotypic brain regions in vitro.
    Proc Natl Acad Sci U S A. 1990 Jun;87(12):4543-7 PMID: 2352935
  16. The developmental onset of NMDA receptor-channel activity during neuronal migration.
    Neuropharmacology. 1993 Nov;32(11):1239-48 PMID: 7509049
  17. Reciprocal expression of cell-cell coupling and voltage-dependent Na current during embryogenesis of rat telencephalon.
    Brain Res Dev Brain Res. 1994 Jan 14;77(1):89-95 PMID: 8131265
  18. Distinct roles for bFGF and NT-3 in the regulation of cortical neurogenesis.
    Neuron. 1995 Jul;15(1):89-103 PMID: 7619533
  19. Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex.
    J Neurosci Methods. 1989 Dec;30(3):203-10 PMID: 2607782
  20. Systematic widespread clonal organization in cerebral cortex.
    Neuron. 1995 Aug;15(2):299-310 PMID: 7646887
  21. Transfection of C6 glioma cells with connexin 43 cDNA: analysis of expression, intercellular coupling, and cell proliferation.
    Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1883-7 PMID: 1848013
  22. Neuronal domains in developing neocortex: mechanisms of coactivation.
    Neuron. 1995 Jan;14(1):7-17 PMID: 7826643
  23. The organization of radial glial fibers in spontaneous neocortical ectopias of newborn New Zealand black mice.
    Brain Res Dev Brain Res. 1992 Jun 19;67(2):279-83 PMID: 1511521
  24. Neuronal coupling in the developing mammalian retina.
    J Neurosci. 1994 Jun;14(6):3805-15 PMID: 8207489
  25. Synchrony of clonal cell proliferation and contiguity of clonally related cells: production of mosaicism in the ventricular zone of developing mouse neocortex.
    J Neurosci. 1997 Mar 15;17(6):2088-100 PMID: 9045736
  26. Riding the glial monorail: a common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain.
    Trends Neurosci. 1990 May;13(5):179-84 PMID: 1693236
  27. Neuronal domains in developing neocortex.
    Science. 1992 Jul 31;257(5070):665-9 PMID: 1496379
  28. Separate progenitor cells give rise to pyramidal and nonpyramidal neurons in the rat telencephalon.
    Cereb Cortex. 1991 Nov-Dec;1(6):463-8 PMID: 1822752
  29. Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon.
    J Neurosci. 1994 Sep;14(9):5399-416 PMID: 8083744
  30. Incorporation of the gene for a cell-cell channel protein into transformed cells leads to normalization of growth.
    J Membr Biol. 1991 Dec;124(3):207-25 PMID: 1664859
  31. Clusters of coupled neuroblasts in embryonic neocortex.
    Science. 1991 Apr 26;252(5005):563-6 PMID: 1850552
  32. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis.
    Neuron. 1995 Dec;15(6):1287-98 PMID: 8845153
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1997-09-15
Pages
7037-44
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6573271
Subset
IM
Grants
NIMH NIH HHS · MH56524 · United States
NINDS NIH HHS · NS21223 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com