Mishra et al. Journal of Molecular Signaling 2010, 5:9
http://www.jmolecularsignaling.com/content/5/1/9
Open Access RESEARCH ARTICLE
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Research article
Glycogen Synthase Kinase-3beta regulates Snail
and beta-catenin during gastrin-induced
migration of gastric cancer cells
Prajna Mishra
1
, Subramanian Senthivinayagam
1
, Ajay Rana
2,3
and Basabi Rana*
1,2,3
Abstract
Background: The gastrointestinal peptide hormone gastrin is known to regulate various cellular processes including
proliferation, migration and metastasis in gastrointestinal (GI) cells. The studies described here were undertaken to
elucidate in detail the signaling pathways mediating the migratory responses of amidated gastrin (G17) and to
understand the involvement of the serine/threonine kinase Glycogen Synthase Kinase-3 beta (GSK3β) in this.
Results: Our results indicate that incubation of gastric cancer cells overexpressing CCK2 receptor (AGSE cells) with G17
results in a dose and time dependent increase of GSK3β
Ser9
phosphorylation, indicative of an inhibition of the kinase.
Pretreatment with a pharmacological inhibitor of PI3Kinase pathway (Wortmannin) was unable to antagonize G17-
induced GSK3β
Ser9
phosphorylation, suggesting that this might involve PI3Kinase-independent pathways. Treatment
with G17 was also associated with increased Snail expression, and β-catenin nuclear translocation, both of which are
GSK3β downstream targets. Pretreatment with a pharmacological inhibitor of GSK3β (AR-A014418) augmented Snail
expression and β-catenin nuclear translocation in the absence of G17, whereas overexpression of a phosphorylation
deficient mutant of GSK3β (S9A) abrogated Snail promoter induction. These suggested that G17 modulates Snail and
β-catenin pathways via inhibiting GSK3β. In addition, overexpression of GSK3β wild type (WT ) or S9A mutant inhibited
G17-induced migration and MMP7 promoter induction. G17 studies designed following small interference RNA
(siRNA)-mediated knockdown of Snail and β-catenin expression indicated a significant reduction of G-17-induced
migration and MMP7 promoter induction following combined knockdown of both proteins.
Conclusion: Our studies indicate that inhibition of GSK3β is necessary to activate G17-induced migratory pathways in
gastric cancer cells. Inhibition of GSK3β leads to an induction of Snail expression and β-catenin nuclear translocation,
both of which participate to promote G17-induced migration.
Background
Gastric cancer is the second leading cause of cancer-
related deaths worldwide [1], and are often characterized
as highly aggressive and unresponsive to therapy [2]. The
major risk factor contributing to this disease include Heli-
cobacter pylori (H. pylori) infection, diet as well as genetic
background [3,4]. Interestingly, studies during the past
two decades have also demonstrated that the gastrointes-
tinal (GI) peptide hormone gastrin might contribute
towards the pathobiology of gastric cancers. In addition
to regulating gastric acid secretion, mature gastrin (G-17)
and its unprocessed intermediate forms progastrin and
glycine extended gastrin (Gly-G) can regulate growth in a
variety of cancer cells [5,6]. Results from transgenic mice
show that mice overexpressing the amidated form of gas-
trin have increased proliferation of gastric mucosa [7],
which can synergize with Helicobacter infection leading
to the development of invasive gastric cancer [8]. Pro-
longed hypergastrinemia increases the relative risk of
developing colon cancer [9] and might promote adenoma
to carcinoma progression [10]. Recent studies have con-
firmed gastrin to be an essential cofactor for carcinogene-
sis of gastric corpus [11]. In addition, significantly high
levels of plasma gastrin has been reported in patients
with gastric cancer, with high expression of gastrin and
* Correspondence: brana@lumc.edu
1
Department of Medicine, Division of Gastroenterology, Hepatology and
Nutrition, Loyola University Chicago, 2160 South First Avenue, Maywood, IL
60153, USA
Full list of author information is available at the end of the article