Abstract
Helicobacter pylori plays a causative role in the development of chronic atrophic gastritis, intestinal metaplasia (IM), and stomach cancer. Although IM has long attracted attention as a putative preneoplastic lesion for stomach cancers, its clinicopathologic significance has yet to be clarified in detail. Using gastric and intestinal epithelial cell markers, IM was here divided into two major types: a gastric-and-intestinal (GI) mixed type and a solely intestinal (I) type. In the former, gastric and intestinal phenotypic markers appeared not only at the glandular but also at the cellular level. Furthermore, neuroendocrine cells also showed intestinalization along with their exocrine counterparts. In animal models, GI-type IM was found to appear first, followed by the solely I type. Summarizing these data, it was suggested that IM might be caused by the gradual intestinalization of stem cells from the GI to the I type. The molecular mechanisms of IM include the ectopic expression of CDX1, CDX2, OCT-1, and members of the Erk pathway. Suppression of the expression of gastric transcription factors such as SOX2, genes that are involved in the Sonic hedgehog pathway, and RUNX3, a tumor suppressor gene, could be additional relevant alterations. The expression of PDX1 may also be associated with pseudopyloric gland metaplasia and IM. Detailed analysis of gene regulation may shed light on the molecular bases of gastric lesions, leading to strategies for chemoprevention.
Article PDF
Similar content being viewed by others
References
JR Warren BJ Marshall (1983) ArticleTitleUnidentified curved bacilli on gastric epithelium in active chronic gastritis Lancet 1 1273–5
D Forman DG Newell F Fullerton JW Yarnell AR Stacey N Wald et al. (1991) ArticleTitleAssociation between infection with Helicobacter pylori and risk of gastric cancer: evidence from a prospective investigation BMJ 302 1302–5 Occurrence Handle2059685 Occurrence Handle1:STN:280:DyaK3M3otlKnug%3D%3D Occurrence Handle10.1136/bmj.302.6788.1302
A Nomura GN Stemmermann PH Chyou I Kato GI Perez-Perez MJ Blaser (1991) ArticleTitle Helicobacter pylori infection and gastric carcinoma among Japanese Americans in Hawaii N Engl J Med 325 1132–6 Occurrence Handle1891021 Occurrence Handle1:STN:280:DyaK3Mzmslagsg%3D%3D Occurrence Handle10.1056/NEJM199110173251604
J Parsonnet GD Friedman DP Vandersteen Y Chang JH Vogelman N Orentreich et al. (1991) ArticleTitle Helicobacter pylori infection and the risk of gastric carcinoma N Engl J Med 325 1127–31 Occurrence Handle1891020 Occurrence Handle1:STN:280:DyaK3Mzmslahuw%3D%3D Occurrence Handle10.1056/NEJM199110173251603
N Uemura S Okamoto S Yamamoto N Matsumura S Yamaguchi M Yamakido et al. (2001) ArticleTitle Helicobacter pylori infection and the development of gastric cancer N Engl J Med 345 784–9 Occurrence Handle11556297 Occurrence Handle1:STN:280:DC%2BD3MrgslCqtA%3D%3D Occurrence Handle10.1056/NEJMoa001999
AR Sepulveda LG Coelho (2002) ArticleTitle Helicobacter pylori and gastric malignancies Helicobacter 7 IssueIDSuppl 1 37–42 Occurrence Handle12197908 Occurrence Handle10.1046/j.1523-5378.7.s1.6.x
MM Walker (2003) ArticleTitleIs intestinal metaplasia of the stomach reversible? Gut 52 1–4 Occurrence Handle12477745 Occurrence Handle1:STN:280:DC%2BD38jhsFOktQ%3D%3D Occurrence Handle10.1136/gut.52.1.1
IARC Working Group on the Evaluation of Carcinogenic Risks to Humans: Infection with Helicobacter pylori. In: Schistosomes, Liver Flukes and Helicobacter pylori, IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, Vol. 61. World Health Organization/International Agency for Research on Cancer, Lyon, 1994, pp. 177–241
T Kawachi M Kurisu N Numanyu K Sasajima T Sano (1976) ArticleTitlePrecancerous changes in the stomach Cancer Res 36 2673–7 Occurrence Handle58722 Occurrence Handle1:CAS:528:DyaE28XkslKju7w%3D
N Matsukura K Suzuki T Kawachi M Aoyagi T Sugimura H Kitaoka et al. (1980) ArticleTitleDistribution of marker enzymes and mucin in intestinal metaplasia in human stomach and relation to complete and incomplete types of intestinal metaplasia to minute gastric carcinomas J Natl Cancer Inst 65 231–40 Occurrence Handle6931245 Occurrence Handle1:STN:280:DyaL3c3lt1entA%3D%3D
BC Morson (1955) ArticleTitleCarcinoma arising from areas of intestinal metaplasia in the gastric mucosa Br J Cancer 9 377–85 Occurrence Handle13269635 Occurrence Handle1:STN:280:DyaG28%2FitFKmsw%3D%3D
MI Filipe S Ramachandra (1995) The histochemistry of intestinal mucins: changes in disease R Whitehead (Eds) Gastrointestinal and oesophageal pathology Churchill Livingstone Edinburgh 73–95
MI Filipe F Potet WV Bogomoletz PA Dawson B Fabiani P Chauveinc et al. (1985) ArticleTitleIncomplete sulphomucin-secreting intestinal metaplasia for gastric cancer. Preliminary data from a prospective study from three centres Gut 26 1319–26 Occurrence Handle4085908 Occurrence Handle1:STN:280:DyaL287gvFKksA%3D%3D
MI Filipe N Munoz I Matko I Kato V Pompe-Kirn A Jutersek et al. (1994) ArticleTitleIntestinal metaplasia types and the risk of gastric cancer: a cohort study in Slovenia Int J Cancer 57 324–9 Occurrence Handle8168991 Occurrence Handle1:STN:280:DyaK2c3it1Kjtw%3D%3D
A Matsukuma M Mori M Enjoji (1990) ArticleTitleSulphomucin-secreting intestinal metaplasia in the human gastric mucosa. An association with intestinal-type gastric carcinoma Cancer 66 689–94 Occurrence Handle2386900 Occurrence Handle1:STN:280:DyaK3czlt1Cqug%3D%3D Occurrence Handle10.1002/1097-0142(19900815)66:4<689::AID-CNCR2820660417>3.0.CO;2-F
T Rokkas MI Filipe GE Sladen (1991) ArticleTitleDetection of an increased incidence of early gastric cancer in patients with intestinal metaplasia type III who are closely followed up Gut 32 1110–3 Occurrence Handle1955163 Occurrence Handle1:STN:280:DyaK38%2FmsVantw%3D%3D
S Silva MI Filipe (1986) ArticleTitleIntestinal metaplasia and its variants in the gastric mucosa of Portuguese subjects: a comparative analysis of biopsy and gastrectomy material Hum Pathol 17 988–95 Occurrence Handle3759069 Occurrence Handle1:STN:280:DyaL2s%2Fgs1Kqtg%3D%3D
WC You WJ Blot JY Li YS Chang ML Jin R Kneller et al. (1993) ArticleTitlePrecancerous gastric lesions in a population at high risk of stomach cancer Cancer Res 53 1317–21 Occurrence Handle8443811 Occurrence Handle1:STN:280:DyaK3s7osFSksw%3D%3D
GN Stemmermann (1994) ArticleTitleIntestinal metaplasia of the stomach. A status report Cancer 74 556–64 Occurrence Handle8033033 Occurrence Handle1:STN:280:DyaK2czgs1eisQ%3D%3D Occurrence Handle10.1002/1097-0142(19940715)74:2<556::AID-CNCR2820740205>3.0.CO;2-J
Y Kato T Kitagawa A Yanagisawa K Kubo T Utsude H Hiratsuka et al. (1992) ArticleTitleSite-dependent development of complete and incomplete intestinal metaplasia types in the human stomach Jpn J Cancer Res 83 178–83 Occurrence Handle1372886 Occurrence Handle1:STN:280:DyaK383htVCjtw%3D%3D
P Lauren (1965) ArticleTitleThe two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma: an attempt at a histo-clinical classification Acta Pathol Microbiol Scand 64 31–49 Occurrence Handle14320675 Occurrence Handle1:STN:280:DyaF2M7isFenug%3D%3D
Y Yuasa (2003) ArticleTitleControl of gut differentiation and intestinal-type gastric carcinogenesis Nat Rev Cancer 3 592–600 Occurrence Handle12894247 Occurrence Handle1:CAS:528:DC%2BD3sXlvV2iu74%3D Occurrence Handle10.1038/nrc1141
M Kusakabe M Yokoyama T Sakakura T Nomura HL Hosick Y Nishizuka (1988) ArticleTitleA novel methodology for analysis of cell distribution in chimeric mouse organs using a strain specific antibody J Cell Biol 107 257–65 Occurrence Handle3292542 Occurrence Handle1:STN:280:DyaL1c3ntlejug%3D%3D Occurrence Handle10.1083/jcb.107.1.257
M Tatematsu H Fukami M Yamamoto H Nakanishi T Masui N Kusakabe et al. (1994) ArticleTitleClonal analysis of glandular stomach carcinogenesis in C3H/HeNk<->lBALB/c chimeric mice treated with N-methyl-N-nitrosourea Cancer Lett 83 37–42 Occurrence Handle8062232 Occurrence Handle1:CAS:528:DyaK2cXlvFyht7Y%3D Occurrence Handle10.1016/0304-3835(94)90296-8
M Tatematsu T Masui H Fukami M Yamamoto H Nakanishi K Inada et al. (1996) ArticleTitlePrimary monoclonal and secondary polyclonal growth of colon neoplastic lesions in C3H/HeNk<->lBALB/c chimeric mice treated with 1,2-dimethylhydrazine: immunohistochemical detection of C3H strain-specific antigen and simple sequence length polymorphism analysis of DNA Int J Cancer 66 234–8 Occurrence Handle8603817 Occurrence Handle1:CAS:528:DyaK28XisFyqur8%3D Occurrence Handle10.1002/(SICI)1097-0215(19960410)66:2<234::AID-IJC16>3.0.CO;2-C
Tsukamoto T, Yamamoto M, Fukami H, Yoshikawa A, Sakai H, Hirata A, et al. Susceptibility to colon carcinogenesis in C3Hk-lC57BL/6 chimeric mice reflects both tissue microenvironment and genotype. Cancer Lett 2006 (in press)
PJ Fialkow (1976) ArticleTitleClonal origin of human tumors Biochim Biophys Acta 458 283–321 Occurrence Handle1067873 Occurrence Handle1:CAS:528:DyaE28XlsFOnsL0%3D
T Kakizoe H Tanooka K Tanaka T Sugimura (1983) ArticleTitleSingle-cell origin of bladder cancer induced by N-butyl-N-(4-hydroxybutyl) nitrosamine in mice with cellular mosaicism Gann 74 462–5 Occurrence Handle6628898 Occurrence Handle1:CAS:528:DyaL3sXltlGgsrw%3D
S Nomura M Kaminishi K Sugiyama T Oohara H Esumi (1998) ArticleTitleClonal analysis of isolated intestinal metaplastic glands of stomach using X-linked polymorphism Gut 42 663–8 Occurrence Handle9659161 Occurrence Handle1:STN:280:DyaK1czitlaqtQ%3D%3D Occurrence Handle10.1136/gut.42.5.663
DJ Winton MA Blount BA Ponder (1988) ArticleTitleA clonal marker induced by mutation in mouse intestinal epithelium Nature 333 463–6 Occurrence Handle3163778 Occurrence Handle1:STN:280:DyaL1c3jt12jug%3D%3D Occurrence Handle10.1038/333463a0
HS Park RA Goodlad NA Wright (1995) ArticleTitleCrypt fission in the small intestine and colon. A mechanism for the emergence of G6PD locus-mutated crypts after treatment with mutagens Am J Pathol 147 1416–27 Occurrence Handle7485404 Occurrence Handle1:CAS:528:DyaK28XktVylsA%3D%3D
CS Potten (1998) ArticleTitleStem cells in gastrointestinal epithelium: numbers, characteristics and death Philos Trans R Soc Lond B Biol Sci 353 821–30 Occurrence Handle9684279 Occurrence Handle1:CAS:528:DyaK1cXkslSnt70%3D Occurrence Handle10.1098/rstb.1998.0246
T Katsuyama SS Spicer (1978) ArticleTitleHistochemical differentiation of complex carbohydrates with variants of the concanavalin A-horseradish peroxidase method J Histochem Cytochem 26 233–50 Occurrence Handle351046 Occurrence Handle1:CAS:528:DyaE1cXhs1Kgs7o%3D
M Tatematsu T Katsuyama S Fukushima M Takahashi T Shirai N Ito et al. (1980) ArticleTitleMucin histochemistry by paradoxical concanavalin A staining in experimental gastric cancers induced in Wistar rats by N-methyl-N-nitro-N-nitrosoguanidine or 4-nitroquinoline 1-oxide J Natl Cancer Inst 64 835–43 Occurrence Handle6154163 Occurrence Handle1:CAS:528:DyaL3cXktl2isr4%3D
C Furihata M Tatematsu K Miki T Katsuyama K Sudo N Miyagi et al. (1984) ArticleTitleGastric- and intestinal-type properties of human gastric cancers transplanted into nude mice Cancer Res 44 727–33 Occurrence Handle6692375 Occurrence Handle1:STN:280:DyaL2c7gs1Ghsw%3D%3D
M Tatematsu C Furihata T Katsuyama Y Mera T Inoue T Matsushima et al. (1987) ArticleTitleImmunohistochemical demonstration of pyloric gland-type cells with low-pepsinogen isozyme 1 in preneoplastic and neoplastic tissues of rat stomachs treated with N-methyl-N′-nitro-N-nitrosoguanidine J Natl Cancer Inst 78 771–7 Occurrence Handle3470552 Occurrence Handle1:CAS:528:DyaL2sXitV2hs74%3D
M Tatematsu T Katsuyama C Furihata S Fukushima T Shirai T Kato et al. (1990) ArticleTitleCellular differentiation and histogenesis of rat glandular stomach cancers Jpn J Cancer Res 81 760–7 Occurrence Handle1697850 Occurrence Handle1:STN:280:DyaK3cznsFeluw%3D%3D
H Iwata SH Itzkowitz JL Werther K Hayashi H Nakamura M Ichinose et al. (1993) ArticleTitleExpression of sialosyl-Tn in intestinal type cancer cells of human gastric cancers Acta Pathol Jpn 43 646–53 Occurrence Handle8310825 Occurrence Handle1:CAS:528:DyaK2cXhs1SitL0%3D
K Inada H Nakanishi Y Fujimitsu N Shimizu M Ichinose K Miki et al. (1997) ArticleTitleGastric and intestinal mixed and solely intestinal types of intestinal metaplasia in the human stomach Pathol Int 47 831–41 Occurrence Handle9503464 Occurrence Handle1:STN:280:DyaK1c7msVajtw%3D%3D Occurrence Handle10.1111/j.1440-1827.1997.tb03714.x
K Inada H Tanaka H Nakanishi T Tsukamoto Y Ikehara K Tatematsu et al. (2001) ArticleTitleIdentification of Paneth cells in pyloric glands associated with gastric and intestinal mixed-type intestinal metaplasia of the human stomach Virchows Arch 439 14–20 Occurrence Handle11499835 Occurrence Handle1:CAS:528:DC%2BD3MXks1Oru7w%3D Occurrence Handle10.1007/s004280000291
Y Tajima T Shimoda Y Nakanishi N Yokoyama T Tanaka K Shimizu et al. (2001) ArticleTitleGastric and intestinal phenotypic marker expression in gastric carcinomas and its prognostic significance: immunohistochemical analysis of 136 lesions Oncology 61 212–20 Occurrence Handle11574777 Occurrence Handle1:STN:280:DC%2BD3MrivVKntg%3D%3D Occurrence Handle10.1159/000055377
T Kawachi K Kogure N Tanaka A Tokunaga T Sugimura (1974) ArticleTitleStudies of intestinal metaplasia in the gastric mucosa by detection of disaccharidases with “Tes-Tape” J Natl Cancer Inst 53 19–30 Occurrence Handle4835098 Occurrence Handle1:STN:280:DyaE2c3mt1yltA%3D%3D
PS Teglbjaerg HO Nielsen (1978) ArticleTitle“Small intestinal type” and “colonic type” intestinal metaplasia of the human stomach, and their relationship to the histogenetic types of gastric adenocarcinoma Acta Pathol Microbiol Scand [A] 86A 351–5 Occurrence Handle1:STN:280:DyaE1M%2FlvVOnsw%3D%3D
DI Segura C Montero (1983) ArticleTitleHistochemical characterization of different types of intestinal metaplasia in gastric mucosa Cancer 52 498–503 Occurrence Handle6190549 Occurrence Handle1:STN:280:DyaL3s3jt1Khsg%3D%3D Occurrence Handle10.1002/1097-0142(19830801)52:3<498::AID-CNCR2820520320>3.0.CO;2-8
JR Jass MI Filipe (1979) ArticleTitleA variant of intestinal metaplasia associated with gastric carcinoma: a histochemical study Histopathology 3 191–9 Occurrence Handle468122 Occurrence Handle1:STN:280:DyaE1M3jsl2gtA%3D%3D
SM Karam CP Leblond (1993) ArticleTitleDynamics of epithelial cells in the corpus of the mouse stomach. I. Identification of proliferative cell types and pinpointing of the stem cell Anat Rec 236 259–79 Occurrence Handle8338232 Occurrence Handle1:STN:280:DyaK3szjt1antQ%3D%3D Occurrence Handle10.1002/ar.1092360202
BA Ponder GH Schmidt MM Wilkinson MJ Wood M Monk A Reid (1985) ArticleTitleDerivation of mouse intestinal crypts from single progenitor cells Nature 313 689–91 Occurrence Handle3974703 Occurrence Handle1:STN:280:DyaL2M7jslyltQ%3D%3D Occurrence Handle10.1038/313689a0
T Hattori S Fujita (1976) ArticleTitleTritiated thymidine autoradiographic study of cell migration and renewal in the pyloric mucosa of golden hamsters Cell Tissue Res 175 49–57 Occurrence Handle1000597 Occurrence Handle1:STN:280:DyaE2s%2Fms12qtQ%3D%3D Occurrence Handle10.1007/BF00220822
H Yuasa K Inada H Watanabe M Tatematsu (2002) ArticleTitleA phenotypic shift from gastric-intestinal to solely intestinal cell types in intestinal metaplasia in rat stomach following treatment with X-rays J Toxicol Pathol 15 85–93 Occurrence Handle10.1293/tox.15.85
K Nozaki N Shimizu T Tsukamoto K Inada X Cao Y Ikehara et al. (2002) ArticleTitleReversibility of heterotopic proliferative glands in glandular stomach of Helicobacter pylori-infected Mongolian gerbils on eradication Jpn J Cancer Res 93 374–81 Occurrence Handle11985786 Occurrence Handle1:CAS:528:DC%2BD38Xks1Ojt7w%3D
M Yamamoto C Furihata T Ogiu T Tsukamoto K Inada K Hirano et al. (2002) ArticleTitleIndependent variation in susceptibilities of six different mouse strains to induction of pepsinogen-altered pyloric glands and gastric tumor intestinalization by N-methyl-N-nitrosourea Cancer Lett 179 121–32 Occurrence Handle11888666 Occurrence Handle1:CAS:528:DC%2BD38XhvVWmur4%3D Occurrence Handle10.1016/S0304-3835(02)00013-7
GV Mallo H Rechreche JM Frigerio D Rocha A Zweibaum M Lacasa et al. (1997) ArticleTitleMolecular cloning, sequencing and expression of the mRNA encoding human Cdx1 and Cdx2 homeobox. Down-regulation of Cdx1 and Cdx2 mRNA expression during colorectal carcinogenesis Int J Cancer 74 35–44 Occurrence Handle9036867 Occurrence Handle1:CAS:528:DyaK2sXhvFCgu74%3D Occurrence Handle10.1002/(SICI)1097-0215(19970220)74:1<35::AID-IJC7>3.0.CO;2-1
DG Silberg EE Furth JK Taylor T Schuck T Chiou PG Traber (1997) ArticleTitleCDX1 protein expression in normal, metaplastic, and neoplastic human alimentary tract epithelium Gastroenterology 113 478–86 Occurrence Handle9247467 Occurrence Handle1:CAS:528:DyaK2sXls1Wnsr8%3D Occurrence Handle10.1053/gast.1997.v113.pm9247467
T Mizoshita K Inada T Tsukamoto Y Kodera Y Yamamura T Hirai et al. (2001) ArticleTitleExpression of Cdx1 and Cdx2 mRNAs and relevance of this expression to differentiation in human gastrointestinal mucosa — with special emphasis on participation in intestinal metaplasia of the human stomach Gastric Cancer 4 185–91 Occurrence Handle11846061 Occurrence Handle1:CAS:528:DC%2BD38XislCksbg%3D Occurrence Handle10.1007/PL00011741
A Eda H Osawa I Yanaka K Satoh H Mutoh K Kihira et al. (2002) ArticleTitleExpression of homeobox gene CDX2 precedes that of CDX1 during the progression of intestinal metaplasia J Gastroenterol 37 94–100 Occurrence Handle11871772 Occurrence Handle1:CAS:528:DC%2BD38XitVWrt7w%3D Occurrence Handle10.1007/s005350200002
K Satoh H Mutoh A Eda I Yanaka H Osawa S Honda et al. (2002) ArticleTitleAberrant expression of CDX2 in the gastric mucosa with and without intestinal metaplasia: effect of eradication of Helicobacter pylori Helicobacter 7 192–8 Occurrence Handle12047325 Occurrence Handle1:CAS:528:DC%2BD38Xmt1Wqurk%3D Occurrence Handle10.1046/j.1523-5378.2002.00080.x
F Drummond J Sowden K Morrison YH Edwards (1996) ArticleTitleThe caudal-type homeobox protein Cdx-2 binds to the colon promoter of the carbonic anhydrase 1 gene Eur J Biochem 236 670–81 Occurrence Handle8612644 Occurrence Handle1:CAS:528:DyaK28XhslWmtbc%3D Occurrence Handle10.1111/j.1432-1033.1996.t01-1-00670.x
E Suh L Chen J Taylor PG Traber (1994) ArticleTitleA homeodomain protein related to caudal regulates intestine-specific gene transcription Mol Cell Biol 14 7340–51 Occurrence Handle7935448 Occurrence Handle1:CAS:528:DyaK2MXhsVWlsbY%3D
JT Troelsen C Mitchelmore N Spodsberg AM Jensen O Noren H Sjostrom (1997) ArticleTitleRegulation of lactase-phlorizin hydrolase gene expression by the caudal-related homoeodomain protein Cdx-2 Biochem J 322 IssueIDPt 3 833–8 Occurrence Handle9148757 Occurrence Handle1:CAS:528:DyaK2sXit1OntLg%3D
J Park S Schulz SA Waldman (2000) ArticleTitleIntestine-specific activity of the human guanylyl cyclase C promoter is regulated by Cdx2 Gastroenterology 119 89–96 Occurrence Handle10889158 Occurrence Handle1:CAS:528:DC%2BD3cXlsFGlt7k%3D Occurrence Handle10.1053/gast.2000.8520
H Yamamoto YQ Bai Y Yuasa (2003) ArticleTitleHomeodomain protein CDX2 regulates goblet-specific MUC2 gene expression Biochem Biophys Res Commun 300 813–8 Occurrence Handle12559945 Occurrence Handle1:CAS:528:DC%2BD3sXmsVCgsg%3D%3D Occurrence Handle10.1016/S0006-291X(02)02935-2
V Subramanian B Meyer GS Evans (1998) ArticleTitleThe murine Cdx1 gene product localises to the proliferative compartment in the developing and regenerating intestinal epithelium Differentiation 64 11–8 Occurrence Handle9921649 Occurrence Handle1:CAS:528:DyaK1MXhs1CrsQ%3D%3D Occurrence Handle10.1046/j.1432-0436.1998.6410011.x
H Lickert C Domon G Huls C Wehrle I Duluc H Clevers et al. (2000) ArticleTitleWnt/beta-catenin signaling regulates the expression of the homeobox gene Cdx1 in embryonic intestine Development 127 3805–13 Occurrence Handle10934025 Occurrence Handle1:CAS:528:DC%2BD3cXmvFSmtL0%3D
C Domon-Dell JN Freund (2002) ArticleTitleStimulation of Cdx1 by oncogenic beta-catenin/Tcf4 in colon cancer cells; opposite effect of the CDX2 homeoprotein FEBS Lett 518 83–7 Occurrence Handle11997022 Occurrence Handle1:CAS:528:DC%2BD38XjsVSrsrY%3D Occurrence Handle10.1016/S0014-5793(02)02650-9
Y Yuasa H Nagasaki Y Akiyama H Sakai T Nakajima Y Ohkura et al. (2005) ArticleTitleRelationship between CDX2 gene methylation and dietary factors in gastric cancer patients Carcinogenesis 26 193–200 Occurrence Handle15498792 Occurrence Handle1:CAS:528:DC%2BD2MXisVSlsA%3D%3D Occurrence Handle10.1093/carcin/bgh304
J Bowles G Schepers P Koopman (2000) ArticleTitlePhylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators Dev Biol 227 239–55 Occurrence Handle11071752 Occurrence Handle1:CAS:528:DC%2BD3cXnvVelu7g%3D Occurrence Handle10.1006/dbio.2000.9883
HB Wood V Episkopou (1999) ArticleTitleComparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages Mech Dev 86 197–201 Occurrence Handle10446282 Occurrence Handle1:CAS:528:DyaK1MXlt1Sgs7s%3D Occurrence Handle10.1016/S0925-4773(99)00116-1
Y Ishii M Rex PJ Scotting S Yasugi (1998) ArticleTitleRegion-specific expression of chicken Sox2 in the developing gut and lung epithelium: regulation by epithelial-mesenchymal interactions Dev Dyn 213 464–75 Occurrence Handle9853967 Occurrence Handle1:CAS:528:DyaK1cXotVGnsLk%3D Occurrence Handle10.1002/(SICI)1097-0177(199812)213:4<464::AID-AJA11>3.0.CO;2-Z
N Sakamoto K Fukuda K Watanuki D Sakai T Komano PJ Scotting et al. (2000) ArticleTitleRole for cGATA-5 in transcriptional regulation of the embryonic chicken pepsinogen gene by epithelial-mesenchymal interactions in the developing chicken stomach Dev Biol 223 103–13 Occurrence Handle10864464 Occurrence Handle1:CAS:528:DC%2BD3cXktFeht7k%3D Occurrence Handle10.1006/dbio.2000.9731
T Tsukamoto K Inada H Tanaka T Mizoshita M Mihara T Ushijima et al. (2004) ArticleTitleDown regulation of a gastric transcription factor, Sox2, and ectopic expression of intestinal homeobox genes, Cdx1 and Cdx2: inverse correlation during progression from gastric/intestinal-mixed to complete intestinal metaplasia J Cancer Res Clin Oncol 130 135–45 Occurrence Handle14655050 Occurrence Handle1:CAS:528:DC%2BD2cXjslylt7o%3D Occurrence Handle10.1007/s00432-003-0519-6
XL Li Y Eishi YQ Bai H Sakai Y Akiyama M Tani et al. (2004) ArticleTitleExpression of the SRY-related HMG box protein SOX2 in human gastric carcinoma Int J Oncol 24 257–63 Occurrence Handle14719100 Occurrence Handle1:CAS:528:DC%2BD2cXht1Ojsrk%3D
T Tsukamoto T Mizoshita M Mihara H Tanaka Y Takenaka Y Yamamura et al. (2005) ArticleTitleSox2 expression in human stomach adenocarcinomas with gastric and gastric-and-intestinal-mixed phenotypes Histopathology 46 649–58 Occurrence Handle15910596 Occurrence Handle1:STN:280:DC%2BD2M3mvV2itA%3D%3D Occurrence Handle10.1111/j.1365-2559.2005.02170.x
H Sakai Y Eishi XL Li Y Akiyama S Miyake T Takizawa et al. (2004) ArticleTitlePDX1 homeobox protein expression in pseudopyloric glands and gastric carcinomas Gut 53 323–30 Occurrence Handle14960508 Occurrence Handle1:CAS:528:DC%2BD2cXitlersL8%3D Occurrence Handle10.1136/gut.2003.026609
G Faller T Kirchner (2005) ArticleTitleImmunological and morphogenic basis of gastric mucosa atrophy and metaplasia Virchows Arch 446 1–9 Occurrence Handle15583929 Occurrence Handle1:CAS:528:DC%2BD2MXltVWltw%3D%3D Occurrence Handle10.1007/s00428-004-1157-3
CP Verrijzer PC Van der Vliet (1993) ArticleTitlePOU domain transcription factors Biochim Biophys Acta 1173 1–21 Occurrence Handle8485147 Occurrence Handle1:CAS:528:DyaK3sXisV2rt7Y%3D
T Jin H Li (2001) ArticleTitlePou homeodomain protein OCT1 is implicated in the expression of the caudal-related homeobox gene Cdx-2 J Biol Chem 276 14752–8 Occurrence Handle11278400 Occurrence Handle1:CAS:528:DC%2BD3MXjs1Okurs%3D Occurrence Handle10.1074/jbc.M008277200
GR van den Brink JC Hardwick C Nielsen C Xu FJ ten Kate J Glickman et al. (2002) ArticleTitleSonic hedgehog expression correlates with fundic gland differentiation in the adult gastrointestinal tract Gut 51 628–33 Occurrence Handle12377798 Occurrence Handle1:CAS:528:DC%2BD38Xoslensrw%3D Occurrence Handle10.1136/gut.51.5.628
JH Kim Z Huang R Mo (2005) ArticleTitleGli3 null mice display glandular overgrowth of the developing stomach Dev Dyn 234 984–91 Occurrence Handle16247775 Occurrence Handle1:CAS:528:DC%2BD2MXhtlCisrjF Occurrence Handle10.1002/dvdy.20542
AH Lund M van Lohuizen (2002) ArticleTitleRUNX: a trilogy of cancer genes Cancer Cell 1 213–5 Occurrence Handle12086855 Occurrence Handle1:CAS:528:DC%2BD38XjsFGltr0%3D Occurrence Handle10.1016/S1535-6108(02)00049-1
QL Li K Ito C Sakakura H Fukamachi K Inoue XZ Chi et al. (2002) ArticleTitleCausal relationship between the loss of RUNX3 expression and gastric cancer Cell 109 113–24 Occurrence Handle11955451 Occurrence Handle1:CAS:528:DC%2BD38XjtVOntLs%3D Occurrence Handle10.1016/S0092-8674(02)00690-6
TY Kim HJ Lee KS Hwang M Lee JW Kim YJ Bang et al. (2004) ArticleTitleMethylation of RUNX3 in various types of human cancers and premalignant stages of gastric carcinoma Lab Invest 84 479–84 Occurrence Handle14968123 Occurrence Handle1:CAS:528:DC%2BD2cXmtF2itrk%3D Occurrence Handle10.1038/labinvest.3700060
M Osaki M Moriyama K Adachi C Nakada A Takeda Y Inoue et al. (2004) ArticleTitleExpression of RUNX3 protein in human gastric mucosa, intestinal metaplasia and carcinoma Eur J Clin Invest 34 605–12 Occurrence Handle15379759 Occurrence Handle1:CAS:528:DC%2BD2cXpt1GmtL8%3D Occurrence Handle10.1111/j.1365-2362.2004.01401.x
H Fukamachi K Ito Y Ito (2004) ArticleTitleRunx3-/- gastric epithelial cells differentiate into intestinal type cells Biochem Biophys Res Commun 321 58–64 Occurrence Handle15358215 Occurrence Handle1:CAS:528:DC%2BD2cXlvVWis78%3D Occurrence Handle10.1016/j.bbrc.2004.06.099
H Tanaka T Tsukamoto T Mizoshita K Inada N Ogasawara X Cao et al. (2005) ArticleTitleExpression of small intestinal and colonic phenotypes in complete intestinal metaplasia of the human stomach Virchows Arch 447 806–15 Occurrence Handle16088401 Occurrence Handle1:CAS:528:DC%2BD2MXht1KnsLfM Occurrence Handle10.1007/s00428-005-0040-1
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Tsukamoto, T., Mizoshita, T. & Tatematsu, M. Gastric-and-intestinal mixed-type intestinal metaplasia: aberrant expression of transcription factors and stem cell intestinalization. Gastric Cancer 9, 156–166 (2006). https://doi.org/10.1007/s10120-006-0375-6
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10120-006-0375-6