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Digestive Diseases and Sciences
Published in: Digestive Diseases and Sciences 6/2010

01-06-2010 | Original Article

Helicobacter pylori in a Korean Isolate Expressed Proteins Differentially in Human Gastric Epithelial Cells

Authors: Soon Ok Cho, Joo Weon Lim, Jong-Ho Jun, Kyung Hwan Kim, Hyeyoung Kim

Published in: Digestive Diseases and Sciences | Issue 6/2010

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Abstract

Purpose

The proteins expressed in gastric epithelial cells infected with Helicobacter pylori (H. pylori) may determine the clinical outcome such as chronic gastritis, peptic ulcer, and gastric carcinoma. The present study aims to determine the differentially expressed proteins in human gastric epithelial AGS cells that were infected with H. pylori in a Korean isolate, a cagA+, vacA s1b m2 iceA1 H. pylori by proteomic analysis. The differentially expressed proteins, whose expression levels were more or less than twofold in H. pylori-infected cells, were analyzed.

Results

Ten proteins (chromatin assembly factor-1, proliferating cell nuclear antigen, 14-3-3 protein τ, eukaryotic translation initiation factor 6, heat-shock protein 90β, dimethylarginine dimethylaminohydrolase-1, l-lactate dehydrogenase B chain, prohibitin, triosephosphate isomerase, protein disulfide isomerase) were up-regulated while eight proteins (heat-shock gp96 precursor, nucleophosmin, ornithine aminotransferase, Ku70, l-arginine-glycine amidinotransferase, Smad anchor for receptor activation, ADP-ribosylation factor, WD repeat-containing protein isoform 1) were down-regulated by H. pylori infection in AGS cells. These proteins are related to cell proliferation, cell adhesion, carcinogenesis, cell-defense mechanisms against oxidative stress, membrane trafficking, and energy metabolism.

Conclusions

Oxidative stress, cell proliferation, cell adhesion, and membrane trafficking may be involved in the pathogenesis of gastric diseases including cancer associated with H. pylori in a Korean isolate.
Literature
1.
Grisham DY. Pathogenic mechanisms loading to Helicobacter pylori-induced inflammation. Eur J Gastroenterol Hepatol. 1992;4:S9–S16.
2.
Marshall BJ. Helicobacter pylori. Am J Gastroenterol. 1994;89:S116–S128.PubMed
3.
Sung JW, Yook EJ, Im EH. Prevalence of Helicobacter pylori infection in peptic ulcer and gastric cancer. Korean J Med. 1993;45:77–83.
4.
Jang MK, Kim HY, Cho BD; Prospective study for the prevalence of Helicobacter infection in patients with gastric ulcer and duodenal ulcer among Korean population. Korean J Med. 1997;52:457–464.
5.
Jung H-K, Na YJ, Moon I-H. Changes of Helicobacter pylori-positive peptic ulcer diseases: based on data from a general hospital. Kor J Gastrointest Endoscop. 2006;32:1–8.
6.
Sobala GM, Crabtree JE, Dixon MF, et al. Acute Helicobacter pylori infection: clinical features, local and systemic immune response, gastric mucosal histology, and gastric juice ascorbic acid concentrations. Gut. 1991;32:1415–1418.CrossRefPubMed
7.
Isaacson PG. Extranodal lumphomas: the MALT concept. Verh Dtsch Ges Pathol. 1992;76:14–23.PubMed
8.
Meyer-ter-Vehn T, Covacci A, Kist M, Pahl HL. Helicobacter pylori activates mitogen-activated protein kinase cascades and induces expression of the proto-oncogenes c-fos and c-jun. J Biol Chem. 2000;275:16064–16072.CrossRefPubMed
9.
Kim H, Lim JW, Kim KH. Helicobacter pylori-induced expression of interleukin-8 and cyclooxygenase-2 in AGS gastric epithelial cells: mediation by nuclear factor-kappaB. Scand J Gastroenterol. 2001;36:706–716.CrossRefPubMed
10.
Kim H, Seo JY, Kim KH. Inhibition of lipid peroxidation, NF-kappaB activation and IL-8 production by rebamipide in Helicobacter pylori-stimulated gastric epithelial cells. Dig Dis Sci. 2000;44:621–628.CrossRef
11.
Lim JW, Kim H, Kim KH. NF-κB, inducible nitric oxide synthase and apoptosis by Helicobacter pylori infection. Free Rad Biol Med. 2001;31:355–366.CrossRefPubMed
12.
Seo JY, Kim H, Kim KH. Transcriptional regulation by thiol compounds in Helicobacter pylori-induced interleukin-8 production in human gastric epithelial cells. Ann NY Acad Sci. 2002;973:541–545.CrossRefPubMed
13.
Chu SH, Kim H, Seo JY, Lim JW, Mukaida N, Kim KH. Role of NF-κB and AP-1 on Helicobacter pylori-induced IL-8 expression in AGS cells. Dig Dis Sci. 2003;48:257–265.CrossRefPubMed
14.
Peek Jr RM, Moss SF, Tham KT, Perez-Perez GI, Wang S, Miller GG, et al. Helicobacter pylori cagA+ strains and dissociation of gastric epithelial cell proliferation from apoptosis. J Nat Cancer Inst. 1997;89: 863–868.
15.
Lim JW, Kim H, Kim KH. Cell adhesion-related gene expression by Helicobacter pylori in gastric epithelial AGS cells. Int J Biochem Cell Biol. 2003;35:1284–1296.CrossRefPubMed
16.
Baek HY, Lim JW, Kim H, et al. Oxidative stress-related proteome changes in Helicobacter pylori-infected human gastric mucosa. Biochem J. 2004;379:291–299.CrossRefPubMed
17.
Mobley HL. Defining Helicobacter pylori as a pathogen: strain heterogenicity and virulence. Am J Med. 1997;100:2S–11S.
18.
Graham DY, Yamaoka Y. Disease-specific Helicobacter pylori virulence factors: the unfulfilled promise. Helicobacter Suppl. 2000;1:S3–S9.CrossRef
19.
Bach S, Markristathis A, Rooter M, Hirschl MA. Gene expression profiling in AGS cells stimulated with Helicobacter pylori isogenic strains (cagA positive or cagA negative). Infect Immun. 2003;701:988–992.
20.
Seo JH, Lim JW, Kim H, Kim KH. Helicobacter pylori in a Korean isolate activates mitogen-activated protein kinases, AP-1 and NF-κB and induces chemokine expression in gastric epithelial AGS cells. Lab Invest. 2004;84:49–62.CrossRefPubMed
21.
Seo JH, Lim JW, Yoon JH, Kim H. Proteinase-activated receptor 2 mediates the expression of integrin α5 and β1 in Helicobacter pylori-infected gastric epithelial AGS cells. Digestion. 2009;80:49.CrossRef
22.
Baek HY, Lim JW, Kim H. Interaction between the Helicobacter pylori CagA and α-pix in gastric epithelial AGS cells. Ann N Y Acad Sci. 2007;1096:18–23.CrossRefPubMed
23.
Rudi J, Rudy A, Maiwald M, Kuck D, Sieg A, Stremmel W. Direct determination of Helicobacter pylori vacA genotypes and cagA gene in gastric biopsies and relationship to gastrointestinal diseases. Am J Gastroenterol. 1999;94:1525–1531.CrossRefPubMed
24.
Gunn MC, Stephens JC, Stewart JA, Rathbone BJ, West KP. The significance of cagA and vacA subtypes of Helicobacter pylori in the pathogenesis of inflammation and peptic ulceration. J Clin Pathol. 1998;51:761–764.CrossRefPubMed
25.
Kim JM, Kim JS, Jung HC, Song IS, Kim CY. Virulence factors of Helicobacter pylori in Korean isolates do not influence proinflammatory cytokine gene expression and apoptosis in human gastric epithelial cells, nor do these factors influence the clinical outcome. J Gastroenterol. 2000;35:898–906.CrossRefPubMed
26.
Chen XJ, Yan J, Shen YF. Dominant cagA/vacA genotypes and coinfection frequency of H. pylori in peptic ulcer or chronic gastritis patients in Zhejiang Province and correlations among different genotypes, coinfection and severity of the diseases. Chin Med J. 2005;118:460–467.
27.
Ko JS, Kim KM, Oh YL, Seo JK. cagA, vacA, and iceA genotypes of Helicobacter pylori in Korean children. Pediatr Int. 2008;50:628–631.CrossRefPubMed
28.
Yamaoka Y, Kodama T, Gutierrez O, Kim JG, Kashima K, Graham DY. Relationship between Helicobacter pylori iceA, cagA, and vacA status and clinical outcome: studies in four different countries. J Clin Microbiol. 1999;37:2274–2279.PubMed
29.
Cover TL, Tummuru MK, Cao P, Thompson SA, Blaser MJ. Divergence of genetic sequences for the vacuolating cytotoxin among Helicobacter pylori strains. J Biol Chem. 1994;269:10566–10573.PubMed
30.
Kim JM, Kim JS, Jung HC, Song IS, Kim CY. Upregulated cyclooxygenase-2 inhibits apoptosis of human gastric epithelial cells uninfected with Helicobacter pylori. Dig Dis Sci. 2000;45:2436–2443.CrossRefPubMed
31.
Kim JM, Kim JS, Jung HC, et al. Helicobacter pylori infection activates NF-kB signaling pathway to induce iNOS and protect human gastric epithelial cells from apoptosis. Am J Physiol Gastrointest Liver Physiol. 2003;285:G1171–G1180.PubMed
32.
Woods AL, Hall PA, Shepherd VA, et al. The assessment of proliferating cell nuclear antigen (PCNA) immunostaining in primary gastrointestinal lymphomas and its relationship to histological grade, S + G2 + M phase fraction (flow cytometric analysis) and prognosis. Histopathology. 1991;19:21–27.CrossRefPubMed
33.
Yonemura Y, Kimura H, Fushida S, et al. Analysis of proliferative activity using antiproliferating cell nuclear antigen antibody in gastric cancer tissue specimens obtained by endoscopic biopsy. Cancer. 1993;71:2448–2453.CrossRefPubMed
34.
Morrison DK. The 14-3-3 proteins: integrators of diverse signaling cues that impact cell fate and cancer development. Trans Cell Biol. 2009;19(1):16–23l.CrossRef
35.
Guo G, Yan-Sanders Y, Lyn-Cook BD, et al. Manganese superoxide dismutase-mediated gene expression in radiation-induced adaptive responses. Mol Cell Biol. 2003;23:2362–2378.CrossRefPubMed
36.
Yu JH, Yun SY, Lim JW, Kim H, Kim KH. Proteome analysis of rat pancreatic acinar cells: implication for cerulein-induced acute pancreatitis. Proteomics. 2003;3:2446–2453.CrossRefPubMed
37.
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analyt Biochem. 1976;72:248–254.CrossRefPubMed
38.
Lock RA, Cordwell SJ, Coombs GW, Walsh BJ, Forbes GM. Proteome analysis of Helicobacter pylori: major proteins of type strain NCTC 11637. Pathology. 2001;33:365–374.CrossRefPubMed
39.
Takami Y, Ono T, Fukagawa T, Shibahara K, Nakayama T. Essential role of chromatin assembly factor-1-mediated rapid nucleosome assembly for DNA replication and cell division in vertebrate cells. Mol Biol Cell. 2007;18:129–141.
40.
41.
Gaillard PH, Martini EM, Kaufman PD, Stillman B, Moustacchi E, Almouzni G. Chromatin assembly coupled to DNA repair: a new role for chromatin assembly factor I. Cell. 1996;86:887–896.CrossRefPubMed
42.
Polo SE, Theocharis SE, Klijanienko J, Savignoni A, Asselain B, Vielh P, et al. Chromatin assembly factor-1, a marker of clinical value to distinguish quiescent from proliferating cells. Cancer Res. 2004;64:2371–2381.
43.
Naryzhny SN. Proliferating cell nuclear antigen: a proteomics view. Cell Mol Life Sci. 2008;65:3789–3808.
44.
Stoimenov I. Helleday T.PCNA on the crossroad of cancer. Biochem Soc Trans. 2009;37(Pt 3):605–613.CrossRefPubMed
45.
Saadat I, Higashi H, Obuse C, et al. Helicobacter pylori CagA targets PAR1/MAPK kinase to disrupt epithelial cell polarity. Nature. 2008;447:330–334.CrossRef
46.
Kwok T, Zabler D, Urman S, et al. Helicobacter exploits integrin for type IV secretion and kinase activation. Nature. 2007;449:862–866.CrossRefPubMed
47.
Snider JL, Allison C, Bellaire BH, Ferrero RL, Cardelli JA. The beta1 integrin activates JNK independent of CgA, and JNK activation is required for Helicobacter pylori CagA+-induced motility of gastric cancer cells. J Biol Chem. 2008;283:13952–13963.CrossRefPubMed
48.
Lim JW, Kim H, Kim JM, Kim JS, Jung HC, Kim KH. Cellular stress-related protein expression in Helicobacter pylori-infected gastric epithelial AGS cells. Int J Biochem Cell Biol. 2004;36:1624–1634.CrossRefPubMed
49.
Pillinger MH, Marjanovic N, Kim SY, et al. Helicobacter pylori stimulates gastric epithelial cell MMP-1 secretion via CagA-dependent and–independent ERK activation. J Biol Chem. 2007;282:18722–18731.CrossRefPubMed
50.
Ji Y, Shah S, Soanes K, et al. Eukaryotic initiation factor 6 selectively regulates Wnt signaling and β-catenin protein synthesis. Oncogene. 2007;27(6):755–762.CrossRefPubMed
51.
Snoeckx LH, Cornelussen RN, Van Nieuwenhoven FA, Reneman RS, Van Der Vusse GJ. Heat shock proteins and cardiovascular pathophysiology. Physiol Rev. 2001;81:1461–1497.PubMed
52.
Huang QQ, Sobkoviak R, Jockheck-Clark AR, et al. Heat shock protein 96 is elevated in rheumatoid arthritis and activates macrophages primarily via TLR2 signaling. J Immunol. 2009;182(8):4965–4973.CrossRefPubMed
53.
Cappello F, de Macario EC, Marasà L, Zummo G, Macario AJ. Hsp60 expression, new locations, functions and perspectives for cancer diagnosis and therapy. Cancer Biol Ther. 2008;7(6):801–809.CrossRefPubMed
54.
Tran CT, Fox MF, Vallance P, Leiper JM. Chromosomal localization, gene structure, and expression pattern of DDAH1: comparison with DDAH2 and implications for evolutionary origins. Genomics. 2002;68:101–105.CrossRef
55.
Zeng X, Liao AJ, Tang HL, Yi L, Xie N, Su Q. Screening human gastric carcinoma-associated antigens by serologic proteome analysis. Ai Zheng. 2007;26:1080–1084.PubMed
56.
Xin HY, Jiang DJ, Jia SJ, et al. Regulation by DDAH/ADMA pathway of lipopolysaccharide-induced tissue factor expression in endothelial cells. Thromb Haemost. 2007;97:830–838.PubMed
57.
Jacobi J, Sydow K, von Degenfeld G, et al. Overexpression of DDAH enhances angiogenesis, determined by postnatal neovascularization using the disk angiogenesis system and a murine model of hindlimb ischemia. Circulation. 2005;111:1431–1438.CrossRefPubMed
58.
Bunn HF, Poyton RO. Oxygen sensing and molecular adaptation to hypoxia. Physiol Rev. 1996;76:839–885.PubMed
59.
Wang GL, Semenza GL. Characterization of hypoxia-inducible factor 1 and regulation of DNA binding activity by hypoxia. J Biol Chem. 1993;268:21513–21518.PubMed
60.
Semenza GL, Roth PH, Fang HM, Wang GL. Transcriptional regulation of genes encoding glcolytic enzymes by hypoxia-inducible factor. J Biol Chem. 1994;269:23757–23763.PubMed
61.
Gina F, Piyali D, Shipra R, Bharat J, Srikumar C. Prohibitin induces the transcriptional activity of p53 and is exported from the nucleus upon apoptotic signaling. J Biol Chem. 2003;278:47853–47861.CrossRef
62.
Kang X, Zhang L, Sun J, et al. Prohibitin: a potential biomarker for tissue-based detection of gastric cancer. J Gastroenterol. 2008;43:618–625.CrossRefPubMed
63.
Qi YJ, He QY, Ma YF, et al. Proteomic identification of malignant transformation-related proteins in esophageal squamous cell carcinoma. J Cell Biochem. 2008;104:1625–1635.CrossRefPubMed
64.
Scatena R, Bottoni P, Pontoglio A, Mastrototaro L, Giardina B. Glycolytic enzyme inhibitors in cancer treatment. Expert Opinion Investig Drugs. 2008;17(10):1533–1545.CrossRef
65.
Wilkinson B, Gilbert HF. Protein disulfide isomerase. Biochim Biophys Acta. 2004;1699:35–44.PubMed
66.
Falini B, Nicoletti I, Bolli N, et al. Translocations and mutations involving the nucleophosmin (NPM1) gene in lymphomas and leukemias. Haematologica. 2007;92:519–532.CrossRefPubMed
67.
Ventura G, De Bandt JP, Segaud F, et al. Overexpression of ornithine aminotransferase: consequences on amino acid homeostasis. Br J Nutr. 2009;101:843–851.CrossRefPubMed
68.
Luk GD, Marton LJ, Baylin SB. Ornithine decarboxylase is important in intestinal mucosal maturation and recovery from injury in rats. Science. 1980;210:195–198.CrossRef
69.
Um JH, Kang CD, Lee BG, Kim DW, Chung BS, Kim SH. Increased and correlated nuclear factor-kappa B and Ku autoantigen activities are associated with development of multidrug resistance. Oncogene. 2001;20:6048–6056.CrossRefPubMed
70.
Lim JW, Kim H, Kim KH. Expression of Ku70 and Ku80 mediated by NF-κB and cyclooxygenase-2 is related to proliferation of human gastric cancer cells. J Biol Chem. 2002;277:46093–46100.CrossRefPubMed
71.
Zhao H, Cao Y, Grunz H. Expression of Xenopus l-arginine:glycine amidinotransferase (XAT) during early embryonic development. Develop genes Evol. 2006;211:358–360.CrossRef
72.
Tsukazaki T, Chiang TA, Davison AF, Attisano L, Wrana JL. SARA, a FYVE domain protein that recruits Smad2 to the TGFbeta receptor. Cell. 1998;95:779–791.
73.
Panopoulou E, Gillooly DJ, Wrana JL, et al. Early endosomal regulation of Smad dependent signaling in endothelial cells. J Biol Chem. 2002;277:18046–18052.CrossRefPubMed
74.
Hiroi T. Regulation of epithelial junctions by proteins of the ADP-ribosylation factor family. Front Biosci. 2009;14:717–730.CrossRefPubMed
75.
Myers KR, Casanova JE. Regulation of actin cytoskeleton dynamics by Arf-family GTPases. Trends Cell Biol. 2008;18(4):184–192.CrossRefPubMed
76.
77.
Ahmad A, Takami Y, Nakayama T. WD repeats of the p48 subunit of chicken chromatin assembly factor-1 required for in vitro interaction with chicken histone deacetylase-2. J Biol Chem. 1999;274:16646–16653.CrossRefPubMed
78.
Mitsuzawa H, Seino H, Yamao F, Ishihama A. Two WD repeat-containing TATA-binding protein-associated factors in fission yeast that suppress defects in the anaphase-promoting complex. J Biol Chem. 2001;276:17117–17124.CrossRefPubMed
Metadata
Title
Helicobacter pylori in a Korean Isolate Expressed Proteins Differentially in Human Gastric Epithelial Cells
Authors
Soon Ok Cho
Joo Weon Lim
Jong-Ho Jun
Kyung Hwan Kim
Hyeyoung Kim
Publication date
01-06-2010
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 6/2010
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-009-0908-z

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