Original Article
Activated hepatic stellate cells mediate the differentiation
of macrophages
Jonathan Chang, Tadakazu Hisamatsu, Katsuyoshi Shimamura, Kazuaki Yoneno,
Masayuki Adachi, Hiroshi Naruse, Toru Igarashi, Hajime Higuchi, Katsuyoshi Matsuoka,
Mina T. Kitazume, Setsu Ando, Nobuhiko Kamada, Takanori Kanai and Toshifumi Hibi
Division of Gastroenterology and Hepatology, Department of Internal Medicine, Keio University School of
Medicine, Tokyo, Japan
Aim: Liver macrophages play integral roles in both the pro-
gression and resolution of hepatic inflammation and fibrosis,
comprising opposing functions that largely coincide with the
activation state of nearby hepatic stellate cells (HSC). While
cross-talk between HSC and macrophages may be essential at
various stages of inflammation and fibrogenesis, many facets
of this interaction have yet to be thoroughly explored. Here,
we examine the potential roles of HSC-derived signaling mol-
ecules as mediators of liver macrophage differentiation.
Methods: Human peripheral blood mononuclear cells
(PBMC) were differentiated to macrophages in the presence
or absence of cultured HSC-derived conditioned media. The
phenotype of resulting macrophages was characterized by
examination of cell surface marker expression, antigen-
presenting capabilities and cytokine secretion.
Results: Conditioned media from activated human HSC pro-
moted the differentiation of a unique set of macrophages that
differed in morphology and function from both classical (M1)
and alternative (M2) macrophages, expressing increased
levels of CD14 and CD16, as well as a distinct interleukin
(IL)-6
high
/IL-10
low
/transforming growth factor (TGF)-b
high
expres-
sion profile. These macrophages expressed high levels of
CD206, CD209, CD80 and human leukocyte antigen DR,
though no significant increases in antigen presentation were
apparent. HSC-derived macrophages exhibited specific acti-
vation of p38 mitogen-activated protein kinase, and inhibition
of this activation by p38 inhibitors during differentiation effec-
tively reversed increases in IL-6 and TGF-b.
Conclusion: The present results suggest that HSC-derived
signaling molecules promote differentiation of liver macroph-
ages with both pro-inflammatory and profibrotic functions.
Furthermore, these effects appear to be mediated, at least
partially, in a p38-dependent manner.
Key words: fibrosis, hepatic stellate cell, interleukin-6,
macrophage, p38 mitogen-activated protein kinase,
transforming growth factor-b
INTRODUCTION
T
HE PIVOTAL ROLE of hepatic stellate cells (HSC) in
the progression of chronic liver disease has been
well established in recent years.
1
Though normally
found in a quiescent state, HSC undergo a process of
differentiation in response to liver injury whereby they
assume a more contractile, myofibroblast-like pheno-
type. This latter state is characterized by excessive
production of a-smooth muscle actin and various extra-
cellular matrix (ECM) proteins including collagen types
I and III.
2–4
While numerous resident fibroblast popula-
tions are also known to produce ECM components, acti-
vated HSC are likely to be the principal contributor of
such fibrotic components in most forms of fibrosis.
5–11
Consequently, HSC are widely regarded as critical
mediators of hepatic fibrogenesis.
Not surprisingly, elucidation of the conditions
whereby HSC activation may be triggered, controlled or
reversed has become an area of particular interest.
Because HSC are located in the space of Disse, and
consequently have close proximities to both hepatocytes
and immune cells of the hepatic sinusoid, there are
numerous potential avenues of cellular cross-talk to
be explored. Indeed, research to date has revealed a
complex network of cellular activities and interactions,
Correspondence: Dr Toshifumi Hibi and Dr Tadakazu Hisamatsu,
Division of Gastroenterology and Hepatology, Department of Internal
Medicine, School of Medicine, Keio University, 35 Shinano-machi,
Shinjuku-ku, Tokyo 160-8582, Japan. Email: thibi@sc.itc.keio.ac.jp;
hisamachi@a7.keio.jp
Received 14 April 2012; revision 23 August 2012; accepted 24
September 2012.
Hepatology Research 2013; 43: 658–669 doi: 10.1111/j.1872-034X.2012.01111.x
© 2012 The Japan Society of Hepatology 658