Home LiteratureArticle Details
PMID: 12040035 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Connexin 43 enhances the adhesivity and mediates the invasion of malignant glioma cells.

Lin JH, Takano T, Cotrina ML, Arcuino G, Kang J, Liu S, Gao Q, Jiang L, Li F, Lichtenberg-Frate H, Haubrich S, Willecke K, Goldman SA, Nedergaard M

Abstract

A hallmark of astrocytic tumors is their infiltrative nature. Although their aggressive and typically widespread dispersal in the adult brain differs fundamentally from that of other brain tumors, little is known about their cellular basis. Astrocytic tumors express the gap junction protein connexin 43 (Cx43), and we show here that Cx43 expression induced the morphological transformation of glioma cells into an epithelial phenotype. In a short-term aggregation assay, Cx43 expression was associated with a several-fold increase in the competence of glioma cells to aggregate. Antibodies directed against the extracellular domain of Cx43 restored the connexin-deficient phenotype, as manifested by a dose-dependent reduction in aggregation. Apart from their role in gap junction formation, connexins may therefore be considered a distinct class of membrane proteins with adhesive properties. Moreover, implanted Cx43-expressing glioma cells established functional gap junction channels with host astrocytes and dispersed through a substantially greater volume of brain parenchyma than mock- and mutant Cx43-transfected sister cells. Cx43 expression therefore may modulate not only the adhesion of astrocytes to one another, but the spread of glial tumor cells throughout astrocytic syncytia. These observations widen our concept of the potential interactions between tumor cells and their surroundings and suggest that both connexin proteins and their derived gap junctions are critical determinants of the invasiveness of central gliomas.

MeSH Terms
Animals Antibodies/pharmacology Astrocytes/cytology Brain Neoplasms/genetics,metabolism,pathology Cell Adhesion/genetics Cell Aggregation/drug effects Cells, Cultured Connexin 43/antagonists & inhibitors,biosynthesis,genetics Connexins/biosynthesis,genetics Dose-Response Relationship, Drug Fluorescent Dyes Gap Junctions/metabolism,pathology Glioma/genetics,metabolism,pathology Immunohistochemistry Male Mutagenesis, Site-Directed Neoplasm Invasiveness Neoplasm Transplantation Neoplasms, Experimental/genetics,metabolism,pathology Patch-Clamp Techniques Permeability Rats Rats, Wistar Structure-Activity Relationship Transfection Tumor Cells, Cultured
Chemicals
Antibodies Connexin 43 Connexins Fluorescent Dyes connexin 32
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Lin Jane H C
Departments of Pathology and Anatomy and Cell Biology, New York Medical College, Valhalla, New York 10595, USA. [email protected].
Takano Takahiro
Cotrina Maria Luisa
Arcuino Gregory
Kang Jian
Liu Shujun
Gao Qun
Jiang Li
Li Fanshu
Lichtenberg-Frate Hella
Haubrich Sandra
Willecke Klaus
Goldman Steven A
Nedergaard Maiken
References (63)
63 references, click to expand
  1. Astrocytic gap junctions remain open during ischemic conditions.
    J Neurosci. 1998 Apr 1;18(7):2520-37 PMID: 9502812
  2. Detergent sensitivity and splitting of isolated liver gap junctions.
    J Membr Biol. 1984;78(2):147-55 PMID: 6425504
  3. Gap junction-mediated cell-cell communication modulates mouse neural crest migration.
    J Cell Biol. 1998 Dec 14;143(6):1725-34 PMID: 9852163
  4. A population-based study on the incidence and survival rates of 3857 glioma patients diagnosed from 1953 to 1984.
    Cancer. 1991 Sep 15;68(6):1394-400 PMID: 1873791
  5. Astrocyte-mediated potentiation of inhibitory synaptic transmission.
    Nat Neurosci. 1998 Dec;1(8):683-92 PMID: 10196584
  6. Endothelial trophic support of neuronal production and recruitment from the adult mammalian subependyma.
    Mol Cell Neurosci. 1999 Jun;13(6):450-64 PMID: 10383830
  7. Mutated connexin43 proteins inhibit rat glioma cell growth suppression mediated by wild-type connexin43 in a dominant-negative manner.
    Int J Cancer. 1998 Nov 9;78(4):446-53 PMID: 9797133
  8. Vascular niche for adult hippocampal neurogenesis.
    J Comp Neurol. 2000 Oct 2;425(4):479-94 PMID: 10975875
  9. Direct signaling from astrocytes to neurons in cultures of mammalian brain cells.
    Science. 1994 Mar 25;263(5154):1768-71 PMID: 8134839
  10. Preparation, characterization, and structure of half gap junctional layers split with urea and EGTA.
    J Membr Biol. 1995 Jul;146(1):15-28 PMID: 7563034
  11. Selective adhesion of embryonal carcinoma cells and differentiated cells by Ca2+-dependent sites.
    Dev Biol. 1981 Oct 30;87(2):340-50 PMID: 6793433
  12. Neural differentiation, NCAM-mediated adhesion, and gap junctional communication in neuroectoderm. A study in vitro.
    J Cell Biol. 1988 Apr;106(4):1307-19 PMID: 2834404
  13. Reduced connexin43 expression in high-grade human brain glioma cells.
    J Surg Oncol. 1999 Jan;70(1):21-4 PMID: 9989416
  14. Adhesion-mediated gap junctional communication between lung-metastatatic cancer cells and endothelium.
    Invasion Metastasis. 1994-1995;14(1-6):164-76 PMID: 7657509
  15. Direct isolation and analysis of endogenous transjunctional ADP from Cx43 transfected C6 glioma cells.
    Exp Cell Res. 1998 Feb 25;239(1):82-92 PMID: 9511727
  16. Inhibition of gap junction and adherens junction assembly by connexin and A-CAM antibodies.
    J Cell Biol. 1992 Oct;119(1):179-89 PMID: 1326565
  17. Biochemical and immunochemical analysis of the arrangement of connexin43 in rat heart gap junction membranes.
    J Cell Sci. 1990 Sep;97 ( Pt 1):109-17 PMID: 2175311
  18. High resolution quantitation of microvascular plasma perfusion in non-ischemic and ischemic rat brain by laser-scanning confocal microscopy.
    Brain Res Brain Res Protoc. 1999 Jul;4(2):185-91 PMID: 10446413
  19. The origin of annular junctions: a mechanism of gap junction internalization.
    J Cell Sci. 2001 Feb;114(Pt 4):763-73 PMID: 11171382
  20. Expressed recombinant cadherins mediate cell sorting in model systems.
    Cell. 1988 Sep 23;54(7):993-1001 PMID: 3416359
  21. Direct gap junction communication between malignant glioma cells and astrocytes.
    Cancer Res. 1999 Apr 15;59(8):1994-2003 PMID: 10213512
  22. Direct association of the gap junction protein connexin-43 with ZO-1 in cardiac myocytes.
    J Biol Chem. 1998 May 22;273(21):12725-31 PMID: 9582296
  23. Bystander killing of cancer cells by herpes simplex virus thymidine kinase gene is mediated by connexins.
    Proc Natl Acad Sci U S A. 1996 Mar 5;93(5):1831-5 PMID: 8700844
  24. Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling.
    Science. 1990 Jan 26;247(4941):470-3 PMID: 1967852
  25. Immunohistochemical localization of cell adhesion molecules and cell-cell contact proteins during regeneration of the rat optic nerve induced by sciatic nerve autotransplantation.
    Anat Rec. 1996 Sep;246(1):114-26 PMID: 8876830
  26. Fate of intercellular junctions in isolated adult rat cardiac cells.
    Circ Res. 1985 Feb;56(2):195-204 PMID: 3971501
  27. Measurement of cerebral microvessel diameters after embolic stroke in rat using quantitative laser scanning confocal microscopy.
    Brain Res. 2000 Sep 8;876(1-2):31-6 PMID: 10973590
  28. Mutational analysis of gap junction formation.
    Biophys J. 1992 Apr;62(1):172-80; discussion 180-2 PMID: 1376165
  29. Reduced expression of connexin-43 and functional gap junction coupling in human gliomas.
    Glia. 2001 Feb;33(2):107-17 PMID: 11180508
  30. Formation and maintenance of the myelin sheath in the peripheral nerve: roles of cell adhesion molecules and the gap junction protein connexin 32.
    Microsc Res Tech. 1998 Jun 1;41(5):403-15 PMID: 9672423
  31. Selective adhesion of cells from different telencephalic regions.
    Neuron. 1996 Mar;16(3):551-64 PMID: 8785052
  32. Functional correlation between cell adhesive properties and some cell surface proteins.
    J Cell Biol. 1977 Nov;75(2 Pt 1):464-74 PMID: 264120
  33. Specific permeability and selective formation of gap junction channels in connexin-transfected HeLa cells.
    J Cell Biol. 1995 May;129(3):805-17 PMID: 7537274
  34. Connexin 43-enhanced suicide gene therapy using herpesviral vectors.
    Mol Ther. 2000 Jan;1(1):71-81 PMID: 10933914
  35. Growth retardation in glioma cells cocultured with cells overexpressing a gap junction protein.
    Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10218-21 PMID: 1332037
  36. Evidence for the participation of actin microfilaments and bristle coats in the internalization of gap junction membrane.
    J Cell Biol. 1979 Dec;83(3):576-87 PMID: 574870
  37. Analysis of distribution patterns of gap junctions during development of embryonic chick facial primordia and brain.
    Development. 1991 Feb;111(2):509-22 PMID: 1654251
  38. N-cadherin influences migration of oligodendrocytes on astrocyte monolayers.
    Mol Cell Neurosci. 2000 Mar;15(3):288-302 PMID: 10736205
  39. Regulation of connexin 43-mediated gap junctional intercellular communication by Ca2+ in mouse epidermal cells is controlled by E-cadherin.
    J Cell Biol. 1991 Aug;114(3):545-55 PMID: 1650371
  40. Leukocytes express connexin 43 after activation with lipopolysaccharide and appear to form gap junctions with endothelial cells after ischemia-reperfusion.
    Proc Natl Acad Sci U S A. 1995 Jul 18;92(15):7011-5 PMID: 7624360
  41. Connexins and gap junctions of astrocytes and oligodendrocytes in the CNS.
    Brain Res Brain Res Rev. 2000 Apr;32(1):29-44 PMID: 10751655
  42. Microglia at brain stab wounds express connexin 43 and in vitro form functional gap junctions after treatment with interferon-gamma and tumor necrosis factor-alpha.
    Proc Natl Acad Sci U S A. 2001 Mar 27;98(7):4190-5 PMID: 11259646
  43. Integrity of the dissociated adult cardiac myocyte: gap junction tearing and the mechanism of plasma membrane resealing.
    J Muscle Res Cell Motil. 1990 Apr;11(2):154-66 PMID: 2351753
  44. c-Src regulates the interaction between connexin-43 and ZO-1 in cardiac myocytes.
    J Biol Chem. 2001 Jan 19;276(3):1780-8 PMID: 11035005
  45. Extensive dye coupling between rat neocortical neurons during the period of circuit formation.
    Neuron. 1993 Jan;10(1):103-14 PMID: 8427699
  46. Treatment of rat experimental brain tumors by herpes simplex virus thymidine kinase gene-transduced allogeneic tumor cells and ganciclovir.
    Cancer Gene Ther. 2000 Jun;7(6):947-53 PMID: 10880027
  47. 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
  48. Protein and messenger RNA expression of connexin43 in astrocytomas: implications in brain tumor gene therapy.
    J Neurosurg. 1996 May;84(5):839-45; discussion 846 PMID: 8622159
  49. Neuronal domains in developing neocortex: mechanisms of coactivation.
    Neuron. 1995 Jan;14(1):7-17 PMID: 7826643
  50. Gap-junction-mediated propagation and amplification of cell injury.
    Nat Neurosci. 1998 Oct;1(6):494-500 PMID: 10196547
  51. Gene therapy of experimental brain tumors using neural progenitor cells.
    Nat Med. 2000 Apr;6(4):447-50 PMID: 10742153
  52. Connexin45 interacts with zonula occludens-1 and connexin43 in osteoblastic cells.
    J Biol Chem. 2001 Jun 22;276(25):23051-5 PMID: 11313345
  53. cDNAs of cell adhesion molecules of different specificity induce changes in cell shape and border formation in cultured S180 cells.
    J Cell Biol. 1990 Apr;110(4):1239-52 PMID: 2182648
  54. Quantitation of microvascular plasma perfusion and neuronal microtubule-associated protein in ischemic mouse brain by laser-scanning confocal microscopy.
    J Cereb Blood Flow Metab. 1999 Jan;19(1):68-78 PMID: 9886357
  55. The gap junction protein connexin43 interacts with the second PDZ domain of the zona occludens-1 protein.
    Curr Biol. 1998 Jul 30-Aug 13;8(16):931-4 PMID: 9707407
  56. Incompatibility of connexin 40 and 43 Hemichannels in gap junctions between mammalian cells is determined by intracellular domains.
    Mol Biol Cell. 1996 Dec;7(12):1995-2006 PMID: 8970160
  57. Up-regulation of neuropilin-1 in neovasculature after focal cerebral ischemia in the adult rat.
    J Cereb Blood Flow Metab. 2001 May;21(5):541-9 PMID: 11333364
  58. The pattern of disulfide linkages in the extracellular loop regions of connexin 32 suggests a model for the docking interface of gap junctions.
    J Cell Biol. 1998 Mar 9;140(5):1187-97 PMID: 9490731
  59. A pre-loading method of evaluating gap junctional communication by fluorescent dye transfer.
    Biotechniques. 1995 Mar;18(3):490-7 PMID: 7779401
  60. Gene expression of neural cell adhesion molecule L1 in malignant gliomas and biological significance of L1 in glioma invasion.
    Cancer Res. 1996 Mar 15;56(6):1440-4 PMID: 8640837
  61. A role for heterologous gap junctions between melanoma and endothelial cells in metastasis.
    J Clin Invest. 2000 May;105(9):1189-97 PMID: 10791993
  62. Transient coupling of Ng-CAM expression to NgCAM-dependent calcium signaling during migration of new neurons in the adult songbird brain.
    Mol Cell Neurosci. 1996 Jan;7(1):29-45 PMID: 8812057
  63. The gap junction communication channel.
    Cell. 1996 Feb 9;84(3):381-8 PMID: 8608591
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2002-06-01
Pages
4302-11
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6758793
Subset
IM
Grants
NINDS NIH HHS · R01NS29813 · United States
NINDS NIH HHS · R01 NS029813 · United States
NINDS NIH HHS · R01NS38073 · United States
NINDS NIH HHS · R01 NS030007 · United States
NINDS NIH HHS · R01NS30007 · United States
NINDS NIH HHS · R01 NS033106 · United States
NINDS NIH HHS · R01NS33106 · United States
NINDS NIH HHS · R01 NS038073 · 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: [email protected]