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Originally published as JHC exPRESS on November 13, 2006.
doi:10.1369/jhc.6A7097.2006
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Journal of Histochemistry and Cytochemistry
Volume 55 (3): 263-274, 2007
Copyright ©The Histochemical Society, Inc.

A Distinctive Set of Genes Is Upregulated During the Inflammation–Carcinoma Sequence in Mouse Stomach Infected by Helicobacter felis

Motohiro Kobayashi, Heeseob Lee, Lana Schaffer, Tim J. Gilmartin, Steven R. Head, Shigeo Takaishi, Timothy C. Wang, Jun Nakayama and Minoru Fukuda

Glycobiology Program, Cancer Research Center, Burnham Institute for Medical Research, La Jolla, California (MK,HL,MF); DNA Array Core Facility, The Scripps Research Institute, La Jolla, California (LS,TJG,SRH); Department of Medicine, College of Physicians and Surgeons, Columbia University, New York, New York (ST,TCW); and Department of Pathology, Shinshu University School of Medicine, Matsumoto, Japan (JN)

Correspondence to: Minoru Fukuda, Burnham Institute for Medical Research, 10901 North Torrey Pines Road, La Jolla, CA 92037. E-mail: minoru{at}burnham.org

Helicobacter pylori infects over half the population worldwide and is a leading cause of chronic gastritis and gastric cancer. However, the mechanism by which this organism induces inflammation and carcinogenesis is not fully understood. In the present study we used insulin–gastrin (INS-GAS) transgenic mice that fully develop gastric adenocarcinoma after infection of H. pylori-related Helicobacter felis. Histological examination revealed that more than half of those mice developed invasive adenocarcinoma after 8 months of infection. These carcinomas were stained by NCC-ST-439 and HECA-452 that recognize 6-sulfated and non-sulfated sialyl Lewis X. Lymphocytic infiltration predominantly to submucosa was observed in most H. felis-infected mice, and this was associated with the formation of peripheral lymph node addressin (PNAd) on high endothelial venule (HEV)-like vessels detected by MECA-79. Time-course analysis of gene expression by using gene microarray revealed upregulation of several inflammation-associated genes including chemokines, adhesion molecules, surfactant protein D (SP-D), and CD74 in the infected stomach. Immunohistochemical analysis demonstrated that SP-D is expressed in hyperplasia and adenocarcinoma whereas CD74 is expressed in adenocarcinoma in situ and invasive carcinoma. These results as a whole indicate that H. felis induces HEV-like vessels and inflammation-associated chemokines and chemokine receptors, followed by adenocarcinoma formation. (J Histochem Cytochem 55:263–274, 2007)

Key Words: Helicobacter felis • insulin–gastrin transgenic mouse • high endothelial venule-like vessel • peripheral lymph node addressin • inflammation–carcinoma sequence • carcinogenesis • surfactant protein D • CD74


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