Original Article
Expression of Sonic hedgehog signaling molecules in normal,
hyperplastic and carcinomatous endometrium
Kyung Hee Kim,
1
Jin Man Kim,
2
Yoon-La Choi,
3
Young Kee Shin,
4
Ho-chang Lee,
5
In Ock Seong,
1
Bum Kyung Kim,
6
Seoung Wan Chae,
7
Yun-Shin Chung
8
and Seok-Hyung Kim
3
1
Department of Pathology, Eulji University College of Medicine,
2
Cancer Research Institute and Infection Signaling
Network Research Center, Chungnam National University, School of Medicine,
6
Department of Pathology, Konyang
University College of Medicine, Daejeon,
3
Department of Pathology, Samsung Medical Center, Sungkyunkwan
University School of Medicine,
4
Research Institute of Pharmaceutical Science, Department of Pharmacy, Seoul
National University College of Pharmacy,
7
Department of Pathology, Kangbuk Samsung Hospital Sungkyunkwan
University College of Medicine,
8
Transplantation Research Center, Clinical Research Institute, Samsung Medical
Center, Seoul and
5
Department of Pathology, Chungbuk National University College of Medicine, Cheongju, Korea
The aim of the present study was to determine the expres-
sion profile of the hedgehog (Hh) signaling molecules
in normal, hyperplastic, and carcinomatous uterine
endometrium. For this purpose, 271 endometrial tissue
samples, (62 of normal endometrium, 127 of endometrial
hyperplasias, and 82 endometrial adenocarcinomas) were
studied using antibodies recognizing Hh-related signaling
proteins, such as, sonic hedgehog (Shh), Patched (PTCH),
Smoothened (Smo), Suppressor of fused [Su(Fu)], Gli-1,
Gli-2, and Gli-3 by immunohistochemistry. The mRNA
expression of these molecules was also assessed on
reverse transcription–polymerase chain reaction. In the
normal endometrium, the expression of Hh signaling mol-
ecules was generally downregulated except for Su(Fu),
Gli-2, and Shh. In particular, the expression of both PTCH
and Smo was very low or almost absent. Overall expression
of Hh signaling molecules increased in hyperplastic
endometrium; in particular, PTCH and Smo were signifi-
cantly highly expressed in complex and atypical hyper-
plasia. In carcinoma samples extensive alterations were
observed in the expression pattern of the signaling mol-
ecules. Nuclear Gli-2, cytoplasmic Gli-3, and Su(Fu) were
overexpressed, whereas Shh, PTCH, and Smo expression
were significantly reduced compared with the hyperplastic
endometrium. The results suggest that the alteration of Hh
signaling may be implicated in tumorigenesis of the
endometrium.
Key words: adenocarcinoma, endometrium, Gli protein, hedge-
hog proteins, hyperplasia, patched receptors, sonic hedgehog
protein, Smoothened protein
The hedgehog (Hh) signaling pathway is central to embryonic
pattern formation during development and regulates stem
cell renewal in adult tissues.
1
In mammals, three Hh homo-
logues have been identified: Sonic (Shh), Indian, and Desert.
The Hh proteins activate a membrane-receptor complex
formed by Patched (PTCH) and Smoothened (Smo), where
PTCH normally inhibits Smo. When Hh binds to PTCH, the
repression of Smo by PTCH is released, allowing Smo to
activate the Gli proteins,
2
which are large, multifunctional
transcription factors. There are three Gli proteins that behave
differently, with partially redundant functions: Gli-1 and Gli-2
can mediate Hh signals and have been implicated in tumori-
genesis. Gli-1 functions primarily as an oncogene; in con-
trast, Gli-2 and Gli-3 either function as an oncogene or a
tumor suppressor, depending on the type of mutation and
cellular context.
3
Suppressor of fused [Su(Fu)] negatively
regulates the Hh-signaling network by repressing Gli-
mediated transcription.
4,5
The deregulation of the Hh signaling pathway has been
implicated in several types of cancer.
6–8
The mutational
activation of the Hh signaling pathway is associated with
tumorigenesis in a small subset of tissues, predominantly
skin, the cerebellum, and skeletal muscle.
9,10
Extensive acti-
vation of the Shh signaling pathway has been reported in
Correspondence: Seok-Hyung Kim, MD, PhD, Department of Path-
ology, Samsung Medical Center, Sungkyunkwan University, School
of Medicine, 50 Ilwon-dong, Gangnam-Gu, Seoul 135-710, South
Korea. Email: platoshkim@daum.net
Received 8 September 2008. Accepted for publication 5 January
2009.
© 2009 The Authors
Journal compilation © 2009 Japanese Society of Pathology
Pathology International 2009; 59: 279–287 doi:10.1111/j.1440-1827.2009.02366.x