Biotechnology and Bioprocess Engineering 20: 358-365 (2015)
DOI 10.1007/s12257-014-0595-2
Role of Gap Junction Communication in Hepatocyte/Fibroblast
Co-cultures: Implications for Hepatic Tissue Engineering
Dongjoo Kim, Yoonjae Seo, and Soonjo Kwon
Received: 3 September 2014 / Revised: 6 November 2014 / Accepted: 13 November 2014
© The Korean Society for Biotechnology and Bioengineering and Springer 2015
Abstract The success of cell-based therapies for treatment
of liver disease hinges on the phenotypic stability of
isolated hepatocytes; however, primary hepatocytes rapidly
lose many liver-specific functions following enzymatic
isolation from the liver. Previous studies have demonstrated
that liver-specific functions can be stabilized by co-
cultivation with non-parenchymal cells. Although the
precise mechanisms underlying these effects have not yet
been elucidated, it is believed that gap junctional intercellular
communication plays an important role in cell-cell
communication. In this study, indirect immunofluorescence
was used to identify connexin 32 and 26 as homotypic gap
junction proteins that were present between hepatocytes
during co-culture with 3T3 fibroblasts, but not in pure
hepatocyte cultures. Additionally, dye transfer of Lucifer
yellow revealed that these gap junctions were functionally
coupled. Although previous studies reported abundant
connexin 43 expression in 3T3 fibroblasts and functional
coupling by dye transfer, we did not observe heterotypic
gap junction (connexin 43) expression or its functional
coupling by either immunofluorescence or dye transfer.
Incubation with a gap junction inhibitor, 18β-glycyrrhetinic
acid, in hepatocyte co-culture diminished the level of liver-
specific markers such as albumin production and P450
activity relative to control co-cultures. Overall, these findings
suggest that homotypic gap junctions are present in
hepatocytes co-cultured with fibroblasts and might play a
functional role in homotypic hepatocyte communication. In
conclusion, homotypic gap junctional communication may
be important to phenotypic stability of isolated hepatocytes
in co-culture and crucial to the design of tissue-engineered
therapies for treatment of liver failure.
Keywords: gap junction, cell-cell communication, homotypic
interaction, co-culture, gap junction inhibition
1. Introduction
Cell-cell interaction is important in the function of many
organ systems. The interaction of parenchymal cells with
stromal neighbors often results in modulation of cell
growth, migration, and/or differentiation of either cell type
[1,2]. These interactions are of fundamental importance to
embryonic development, adult liver, skin, vasculature,
muscle, and hematopoietic physiology [3]. Gap junctions
form intercellular channels through which cells communicate
directly, and changes in gap junction expression have been
shown to be closely related to chronic liver disease and liver
carcinogenesis [4-7]. Therefore, fundamental understanding
of the mechanisms by which liver-specific functions are
stabilized may reveal approaches that enable the manipulation
of tissue function in vitro for therapeutic application.
The coordinated function of the liver depends on long-
and short-range signaling among hepatocytes, fibroblasts,
Ito cells, cholangiocytes, and endothelial cells. Such signaling
is accompanied by hormones and transmitters moving through
the extracellular space, as well as direct intercellular
diffusion of ion and messenger molecules. Gap junctional
intercellular communication (GJIC) allows the exchange of
low molecular weight (<1 kDa) ions, metabolites, and
secondary messengers between cells through gap junction
channels. Adjacent cells in tissues and organs communicate
through signaling and regulatory molecules via gap junction
channels. In hepatic acinus, bile flow in hepatocyte canaliculi
Dongjoo Kim, Yoonjae Seo, Soonjo Kwon
*
Department of Biological Engineering, Inha University, Incheon 402-751,
Korea
Tel: +82-32-860-9176; Fax: +82-32-872-4046
E-mail: soonjo.kwon@inha.ac.kr
RESEARCH PAPER