Open Access Review Article
Cell
Science & Therapy
Mulu et al., J Cell Sci Ther 2012, S5
http://dx.doi.org/10.4172/2157-7013.S5-005
J Cell Sci Ther Cytokines ISSN: 2157-7013 JCEST, an open access journal
Introduction
Contrary to unicellular organisms, cells in multicellular metazoa
must divide under strict control. Intercellular communication is crucial
in the regulation of cell growth, as well as differentiation and migration,
and it oſten occurs indirectly through the release of diffusible growth
factors by certain cells that initiate the signal through receptors on
target cells. Communication between cells can also be achieved
directly, through the gap junctions, i.e., channels running through
the membrane which allow the passage of ions and other molecules
between the interiors of adjacent cells. Gap junctions consist of the
transmembrane proteins, termed connexins, a family of at least 20
members described in mammals. ey are oſten designated with a suffix
referring to their molecular weight. Gap junctions are formed by the
aggregation of two hemi-channels of six connexons each, contributed
by the two neighboring cells. is structure forms an aqueous channel
through the two plasma membranes, that permits the passage of small
molecules such as ions, nucleotides, aminoacids, short peptides or RNA
[1,2] between adjacent cells [3].
Results from a number of labs indicated that an increase in cell
proliferation correlates with a reduction in gap junctional, intercellular
communication (GJIC). In fact, a number of tumor promotors such
as the 12-O-Tetradecanoylphorbol-13-acetate and oncogene products
such as the transforming protein of the Rous Sarcoma virus, vSrc [4],
the polyoma virus middle Tumor antigen (mT [5,6]), the activated
chaperone Hsp90N [7], vRas [8,9] and others have been shown to
interrupt junctional communication.
Src is an oncogene with a high clinical relevance and one of the
best-studied targets for cancer therapy (reviewed in [10]). Src encodes
a potent oncoprotein with high tyrosine kinase activity. Among its
functions, Src can affect the activity of Cx43 by multiple mechanisms,
namely by direct phosphorylation on tyrosine residues, but also
by its direct downstream effector pathways, Ras/Raf/Erk and the
phosphatidylinositol-3 kinase (PI3k)/Akt that phosphorylate Cx43 on
serine residues to disrupt GJIC. In addition, Src may indirectly activate
the ser/thr kinase, protein kinase C that can phosphorylate Cx43 and
block gap junctions, as well as other kinases such as the cell division
cycle-2 (Cdc2) kinase, caseine kinase 1 (Ck1) and protein kinase A
[11-17]. Besides activating kinase pathways, Src can also make use of
the adaptor protein Cas (Crk associated substrate) that binds Cx43 to
suppress gap junctional communication [18], and is a potent activator
of the Signal transducer and activator of transcription-3 (Stat3). In this
communication we review the prevailing evidence on the role of Src
and its effector pathways upon Cx43 and GJIC.
Phosphorylation of Cx43 on Tyrosine by the Src kinase
A reduction in gap junctional communication of Src-transformed
cells was reported for the first time in 1966 [19]. Subsequent cloning of
Cx43 enabled a molecular characterisation of the mechanism whereby
Src affects Cx43 function, and this led to fundamental studies on
Cx43 regulation. A combination of genetic and biochemical evidence
indicated that Src can phosphorylate Cx43 directly: At first the SH3
domain of Src binds a proline-rich area between P274 and P284 of
Cx43. is brings the Src kinase domain in close proximity to Y265,
which is then phosphorylated by Src (Figure 1). e phosphorylated
Y265 offers a docking site for the Src, Src-homology-2 (SH2) domain
and this enhanced interaction causes the phosphorylation of Y247 of
Cx43, which may contribute to GJIC reduction [20-22]. In fact, vSrc co-
expression with a Cx43 mutant where tyr247 and tyr265 were replaced
by phenylalanine in Cx43 knockout cells, was unable to interrupt
communication, indicating that tyr247 and ty265 are important for
GJIC suppression by the Src kinase [21]. However, expression of the
same Cx43 mutants in Xenopus oocytes can result in the formation of
gap junctions, but these gap junctions can be disrupted by Src, indicating
that the sites of direct phosphorylation by Src are not required for GJIC
*Corresponding author: Leda Raptis, Departments of Microbiology, Immunology
and Pathology, Queen’s University, Kingston, Ontario, Canada K7L3N6, Tel: (613)
533 2462 (office/lab)/(613) 533-2450 (secretary); Fax: (613) 533 6796; E-mail:
raptisl@queensu.ca
Received November 25, 2011; Accepted December 16, 2011; Published
December 19, 2011
Citation: Geletu M, Trotman-Grant A, Raptis L (2012) Regulation of Gap Junctional,
Intercellular Communication by the Src Oncogene Product and its Effectors. J Cell
Sci Ther S5:005. doi:10.4172/2157-7013.S5-005
Copyright: © 2012 Geletu M, et al. This is an open-access article distributed under
the terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author and
source are credited.
Abstract
Gap junctions are channels that connect the interiors of neighboring cells and are formed by the connexin (Cx)
proteins. A reduction in gap junctional, intercellular communication (GJIC) often correlates with increased growth and
neoplastic transformation. Cx43 is a widely expressed connexin which can be phosphorylated by the Src oncoprotein
tyrosine kinase on tyr247 and 265 and this reduces communication. However, Src activates multiple signalling
pathways such as the Ras/Raf/Erk and PLCγ/protein kinase C, which can also phosphorylate Cx43 and interrupt
communication. Other Src effectors such as the Crk associated substrate which has an adaptor function, binds Cx43
to suppress gap junctional communication. In sharp contrast, activation of another Src effector, the Signal transducer
and activator of transcription-3 (Stat3) is not required for the Src-mediated, GJIC suppression. Interestingly, Stat3 is
actually required for the maintenance of gap junctional communication in normal cells with high GJIC.
Regulation of Gap Junctional, Intercellular Communication by the Src
Oncogene Product and its Effectors
Mulu Geletu, Aaron Trotman-Grant and Leda Raptis*
Departments of Microbiology, Immunology and Pathology, Queen’s University, Kingston, Ontario, Canada K7L3N6