Elsevier

Differentiation

Volume 74, Issues 9–10, December 2006, Pages 562-572
Differentiation

ORIGINAL ARTICLE
Interactive properties of human glioblastoma cells with brain neurons in culture and neuronal modulation of glial laminin organization

https://doi.org/10.1111/j.1432-0436.2006.00090.xGet rights and content

Abstract

The harmonious development of the central nervous system depends on the interactions of the neuronal and glial cells. Extracellular matrix elements play important roles in these interactions, especially laminin produced by astrocytes, which has been shown to be a good substrate for neuron growth and axonal guidance. Glioblastomas are the most common subtypes of primary brain tumors and may be astrocytes in origin. As normal laminin-producing glial cells are the preferential substrate for neurons, and glial tumors have been shown to produce laminin, we questioned whether glioblastoma retained the same normal glial–neuron interactive properties with respect to neuronal growth and differentiation. Then, rat neurons were co-cultured onto rat normal astrocytes or onto three human glioblastoma cell lines obtained from neurosurgery. The co-culture confirmed that human glioblastoma cells as well as astrocytes maintained the ability to support neuritogenesis, but non-neural normal or tumoral cells failed to do so. However, glioblastoma cells did not distinguish embryonic from post-natal neurons in relation to neurite pattern in the co-cultures, as normal astrocytes did. Further, the laminin organization on both normal and tumoral glial cells was altered from a filamentous arrangement to a mixed punctuate/filamentous pattern when in co-culture with neurons. Together, these results suggest that glioblastoma cells could identify neuronal cells as partners, to support their growth and induce complex neurites, but they lost the normal glia property to distinguish neuronal age. In addition, our results show for the first time that neurons modulate the organization of astrocytes and glioblastoma laminin on the extracellular matrix.

References (67)

  • M. Mallat et al.

    Two simian virus 40 (SV40)-transformed cells lines from the mouse striatum and mesencephalon presenting astrocytic characters. II. Interactions with mesencephalic neurons

    Brain Res

    (1986)
  • V. Moura Neto et al.

    Two simian virus 40 (SV40)-transformed cell lines from the mouse striatum and mesencephalon presenting astrocytic characters. I. Immunological and pharmacological properties

    Brain Res

    (1986)
  • T. Nakayama et al.

    Astrocytic-derived factors instruct differentiation of embryonic stem cells into neurons

    Neurosci Res

    (2003)
  • R.R. Pindzola et al.

    Putative inhibitory extracellular matrix molecules at the dorsal root entry zone of the spinal cord during development and after root and sciatic nerve lesions

    Dev Biol

    (1993)
  • S.K. Powell et al.

    Neuronal laminins and their cellular receptors

    Int J Biochem Cell Biol

    (1997)
  • P. Rakic

    Neuronal–glial interaction during brain development

    TINS

    (1981)
  • J.T. Rutka et al.

    Co-expression of nestin and vimentin intermediate filaments in invasive human astrocytoma cells

    Int J Dev Neurosci

    (1999)
  • D.M. Snow et al.

    Molecular and cellular characterization of the glial roof plate of the spinal cord and optic tectum: a possible role for a proteoglycan in development of an axon barrier

    Dev Biol

    (1990)
  • F.C. Zhou

    Four patterns of laminin-immunoreactive structure in developing rat brain

    Brain Res Dev Brain Res

    (1990)
  • L.A. Cavalcante et al.

    Modulators of axonal growth and guidance at the brain midline with special reference to glial heparan sulfate proteoglycans

    An Acad Bras Cienc

    (2002)
  • B. Chamak et al.

    Influence of extracellular matrix proteins on the expression of neuronal polarity

    Development

    (1989)
  • H. Colognato et al.

    Form and function: the laminin family of heterotrimers

    Dev Dynam

    (2000)
  • JH. Deck et al.

    The role of glial fibrillary acidic protein in the diagnosis of central nervous system tumors

    Acta Neuropathol

    (1978)
  • S. Denis-Donini et al.

    Glial heterogeneity might define the three-dimensional shape of mouse mesencephalic dopaminergic neurons

    Nature

    (1984)
  • T.C. De Sampaio e Spohr et al.

    Neuro-glia interaction effects on GFAP gene: a novel role for transforming growth factor-β1

    Eur J Neurosci

    (2002)
  • M.A. Ferrari de Outeiro-Berstein et al.

    A recombinant NH(2)-terminal heparin-binding domain of the adhesive glycoprotein, thrombospondin-1, promotes endothelial tube formation and cell survival: a possible role for syndecan-4 proteoglycan

    Matrix Biol

    (2002)
  • E. Förster et al.

    Reelin, Disabled 1, and β1 integrins are required for the formation of the radial glial scaffold in the hippocampus

    Proc Natl Acad Sci USA

    (2002)
  • E. Freire et al.

    Structure of laminin substrate modulates cellular signaling for neuritogeneses

    J Cell Sci

    (2002)
  • E. Freire et al.

    Sialic acid residues on astrocytes regulate neuritogenesis by controlling the assembly of laminin matrices

    J Cell Sci

    (2004)
  • P.S. Frisa et al.

    Immortalization of immature and mature mouse astrocytes with SV40T antigen

    J Neurosci Res

    (1994)
  • M.M. Fróes et al.

    Gap-junctional coupling between neurons and astrocytes in primary central neurvous system cultures

    Proc Natl Acad Sci USA

    (1999)
  • J. Garcia-Abreu et al.

    Differential patterns of laminin expression in lateral and medial midbrain glia

    NeuroReport

    (1995)
  • J. Garcia-Abreu et al.

    Contribution of heparan sulfate to the non-permissive role of the midline glia to the growth of midbrain neurites

    Glia

    (2000)
  • Cited by (0)

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    These authors contributed equally to this work.

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