Clinicopathologic and molecular characteristics of gastric cancer showing gastric and intestinal mucin phenotype

Cancer Science

Volumn 106, Issue 8, 2015, Pages 951-958

  Oue, Naohide ^a   Sentani, Kazuhiro ^a   Sakamoto, Naoya ^a   Yasui, Wataru ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Escherichia coli ampicillin secretion trap; Gastric cancer; Mucin; Phenotype; Serial Analysis of Gene Expression

Indexed keywords

APC PROTEIN; BETA CATENIN; CATENIN; CLAUDIN 18; CYTOKERATIN; DNA; EPIDERMAL GROWTH FACTOR RECEPTOR; MEMBRANE PROTEIN; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; MUCIN; MULTIDRUG RESISTANCE PROTEIN 1; PROTEIN MLH1; PROTEIN P53; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HOXA10;

CANCER CELL; DNA METHYLATION; ESCHERICHIA COLI AMPICILLIN SECRETION TRAP ANALYSIS; GENE EXPRESSION; GENE MUTATION; HUMAN; INTESTINE; MICROSATELLITE INSTABILITY; NUCLEIC ACID ANALYSIS; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SERIAL ANALYSIS OF GENE EXPRESSION; STOMACH; STOMACH CANCER; TUMOR MICROENVIRONMENT; TUMOR SUPPRESSOR GENE; CLASSIFICATION; GENETICS; METABOLISM; PATHOLOGY; STOMACH TUMOR;

HUMANS; INTESTINES; MUCINS; PHENOTYPE; STOMACH NEOPLASMS;

EID: 84939257478     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/cas.12706     Document Type: Review

References (87)

1. Nakamura K, Sugano H, Takagi K. Carcinoma of the stomach in incipient phase: its histogenesis and histological appearances. Gann 1968; 59: 251-8.
2. Lauren P. The two histological main types of gastric carcinoma. Diffuse and so-called intestinal type carcinoma: an attempt at histological classification. Acta Pathol Microbiol Scand 1965; 64: 31-49.
3. Vauhkonen M, Vauhkonen H, Sipponen P. Pathology and molecular biology of gastric cancer. Best Pract Res Clin Gastroenterol 2006; 20: 651-74.
4. Oue N, Oshimo Y, Nakayama H et al. DNA methylation of multiple genes in gastric carcinoma: association with histological type and CpG island methylator phenotype. Cancer Sci 2003; 94: 901-5.
5. Yasui W, Oue N, Ito R, Kuraoka K, Nakayama H. Search for new biomarkers of gastric cancer through serial analysis of gene expression and its clinical implications. Cancer Sci 2004; 95: 385-92.
6. Yasui W, Sentani K, Sakamoto N, Anami K, Naito Y, Oue N. Molecular pathology of gastric cancer: research and practice. Pathol Res Pract 2011; 207: 608-12.
7. Tatematsu M, Tsukamoto T, Inada K. Stem cells and gastric cancer: role of gastric and intestinal mixed intestinal metaplasia. Cancer Sci 2003; 94: 135-41.
8. Endoh Y, Sakata K, Tamura G et al. Cellular phenotypes of differentiated-type adenocarcinomas and precancerous lesions of the stomach are dependent on the genetic pathways. J Pathol 2000; 191: 257-63.
9. Egashira Y, Shimoda T, Ikegami M. Mucin histochemical analysis of minute gastric differentiated adenocarcinoma. Pathol Int 1999; 49: 55-61.
10. Mizoshita T, Tsukamoto T, Nakanishi H et al. Expression of Cdx2 and the phenotype of advanced gastric cancers: relationship with prognosis. J Cancer Res Clin Oncol 2003; 129: 727-34.
11. Oue N, Mitani Y, Aung PP et al. Expression and localization of Reg IV in human neoplastic and non-neoplastic tissues: Reg IV expression is associated with intestinal and neuroendocrine differentiation in gastric adenocarcinoma. J Pathol 2005; 207: 185-98.
12. Kabashima A, Yao T, Sugimachi K, Tsuneyoshi M. Gastric or intestinal phenotypic expression in the carcinomas and background mucosa of multiple early gastric carcinomas. Histopathology 2000; 37: 513-22.
13. Takami H, Sentani K, Matsuda M, Oue N, Sakamoto N, Yasui W. Cytokeratin expression profiling in gastric carcinoma: clinicopathologic significance and comparison with tumor-associated molecules. Pathobiology 2012; 79: 154-61.
14. Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma: 3rd English edition. Gastric Cancer 2011; 14: 101-12.
15. Nakamura T, Yao T, Kabashima A, Nishiyama K, Maehara Y, Tsuneyoshi M. Loss of phenotypic expression is related to tumour progression in early gastric differentiated adenocarcinoma. Histopathology 2005; 47: 357-67.
16. Wu LB, Kushima R, Borchard F, Molsberger G, Hattori T. Intramucosal carcinomas of the stomach: phenotypic expression and loss of heterozygosity at microsatellites linked to the APC gene. Pathol Res Pract 1998; 194: 405-11.
17. Endoh Y, Tamura G, Watanabe H, Ajioka Y, Motoyama T. The common 18-base pair deletion at codons 418-423 of the E-cadherin gene in differentiated-type adenocarcinomas and intramucosal precancerous lesions of the stomach with the features of gastric foveolar epithelium. J Pathol 1999; 189: 201-6.
18. Shibata N, Watari J, Fujiya M, Tanno S, Saitoh Y, Kohgo Y. Cell kinetics and genetic instabilities in differentiated type early gastric cancers with different mucin phenotype. Hum Pathol 2003; 34: 32-40.
19. Yokozaki H, Shitara Y, Fujimoto J, Hiyama T, Yasui W, Tahara E. Alterations of p73 preferentially occur in gastric adenocarcinomas with foveolar epithelial phenotype. Int J Cancer 1999; 83: 192-6.
20. Endoh Y, Tamura G, Ajioka Y, Watanabe H, Motoyama T. Frequent hypermethylation of the hMLH1 gene promoter in differentiated-type tumors of the stomach with the gastric foveolar phenotype. Am J Pathol 2000; 157: 717-22.
21. Motoshita J, Oue N, Nakayama H et al. DNA methylation profiles of differentiated-type gastric carcinomas with distinct mucin phenotypes. Cancer Sci 2005; 96: 474-9.
22. Goto A, Hirahashi M, Osada M et al. Aberrant activation-induced cytidine deaminase expression is associated with mucosal intestinalization in the early stage of gastric cancer. Virchows Arch 2011; 458: 717-24.
23. Park SY, Kim HS, Hong EK, Kim WH. Expression of cytokeratins 7 and 20 in primary carcinomas of the stomach and colorectum and their value in the differential diagnosis of metastatic carcinomas to the ovary. Hum Pathol 2002; 33: 1078-85.
24. Sentani K, Matsuda M, Oue N et al. Clinicopathological significance of MMP-7, laminin gamma2 and EGFR expression at the invasive front of gastric carcinoma. Gastric Cancer 2014; 17: 412-22.
25. Velculescu VE, Zhang L, Vogelstein B, Kinzler KW. Serial analysis of gene expression. Science 1995; 270: 484-7.
26. Ferguson DA, Muenster MR, Zang Q et al. Selective identification of secreted and transmembrane breast cancer markers using Escherichia coli ampicillin secretion trap. Cancer Res 2005; 65: 8209-17.
27. Oue N, Hamai Y, Mitani Y et al. Gene expression profile of gastric carcinoma: identification of genes and tags potentially involved in invasion, metastasis, and carcinogenesis by serial analysis of gene expression. Cancer Res 2004; 64: 2397-405.
28. Berndorff D, Gessner R, Kreft B et al. Liver-intestine cadherin: molecular cloning and characterization of a novel Ca(2+)-dependent cell adhesion molecule expressed in liver and intestine. J Cell Biol 1994; 125: 1353-69.
29. Kreft B, Berndorff D, Bottinger A et al. LI-cadherin-mediated cell-cell adhesion does not require cytoplasmic interactions. J Cell Biol 1997; 136: 1109-21.
30. Ito R, Oue N, Yoshida K et al. Clinicopathological significant and prognostic influence of cadherin-17 expression in gastric cancer. Virchows Arch 2005; 447: 717-22.
31. Grotzinger C, Kneifel J, Patschan D et al. LI-cadherin: a marker of gastric metaplasia and neoplasia. Gut 2001; 49: 73-81.
32. Sakamoto N, Oue N, Sentani K et al. Liver-intestine cadherin induction by epidermal growth factor receptor is associated with intestinal differentiation of gastric cancer. Cancer Sci 2012; 103: 1744-50.
33. Hartupee JC, Zhang H, Bonaldo MF, Soares MB, Dieckgraefe BK. Isolation and characterization of a cDNA encoding a novel member of the human regenerating protein family: Reg IV. Biochim Biophys Acta 2001; 1518: 287-93.
34. Bishnupuri KS, Luo Q, Murmu N, Houchen CW, Anant S, Dieckgraefe BK. Reg IV activates the epidermal growth factor receptor/Akt/AP-1 signaling pathway in colon adenocarcinomas. Gastroenterology 2006; 130: 137-49.
35. Mitani Y, Oue N, Matsumura S et al. Reg IV is a serum biomarker for gastric cancer patients and predicts response to 5-fluorouracil-based chemotherapy. Oncogene 2007; 26: 4383-93.
36. Katsuno Y, Ehata S, Yashiro M, Yanagihara K, Hirakawa K, Miyazono K. Coordinated expression of REG4 and aldehyde dehydrogenase 1 regulating tumourigenic capacity of diffuse-type gastric carcinoma-initiating cells is inhibited by TGF-β. J Pathol 2012; 228: 391-404.
37. Takehara A, Eguchi H, Ohigashi H et al. Novel tumor marker REG4 detected in serum of patients with resectable pancreatic cancer and feasibility for antibody therapy targeting REG4. Cancer Sci 2006; 97: 1191-7.
38. Nakata K, Nagai E, Ohuchida K et al. REG4 is associated with carcinogenesis in the 'intestinal' pathway of intraductal papillary mucinous neoplasms. Mod Pathol 2009; 22: 460-8.
39. Oue N, Kuniyasu H, Noguchi T et al. Serum concentration of Reg IV in patients with colorectal cancer: overexpression and high serum levels of Reg IV are associated with liver metastasis. Oncology 2007; 72: 371-80.
40. Ohara S, Oue N, Matsubara A et al. Reg IV is an independent prognostic factor for relapse in patients with clinically localized prostate cancer. Cancer Sci 2008; 99: 1570-7.
41. Sasahira T, Oue N, Kirita T et al. Reg IV expression is associated with cell growth and prognosis of adenoid cystic carcinoma in the salivary gland. Histopathology 2008; 53: 667-75.
42. Tamura H, Ohtsuka M, Washiro M et al. Reg IV expression and clinicopathologic features of gallbladder carcinoma. Hum Pathol 2009; 40: 1686-92.
43. Heiskala K, Arola J, Heiskala M, Andersson LC. Expression of Reg IV and Hath1 in neuroendocrine neoplasms. Histol Histopathol 2010; 25: 63-72.
44. Zhang J, Liu WL, Tang DC et al. Identification and characterization of a novel member of olfactomedin-related protein family, hGC-1, expressed during myeloid lineage development. Gene 2002; 283: 83-93.
45. van der Flier LG, Haegebarth A, Stange DE, van de Wetering M, Clevers H. OLFM4 is a robust marker for stem cells in human intestine and marks a subset of colorectal cancer cells. Gastroenterology 2009; 137: 15-7.
46. Oue N, Sentani K, Noguchi T et al. Serum olfactomedin 4 (GW112, hGC-1) in combination with Reg IV is a highly sensitive biomarker for gastric cancer patients. Int J Cancer 2009; 125: 2383-92.
47. Qiu W, Wang X, Leibowitz B et al. Chemoprevention by nonsteroidal anti-inflammatory drugs eliminates oncogenic intestinal stem cells via SMAC-dependent apoptosis. Proc Natl Acad Sci U S A 2010; 107: 20027-32.
48. Reynolds A, Wharton N, Parris A et al. Canonical Wnt signals combined with suppressed TGFbeta/BMP pathways promote renewal of the native human colonic epithelium. Gut 2014; 63: 610-21.
49. Liu W, Yan M, Liu Y et al. Olfactomedin 4 down-regulates innate immunity against Helicobacter pylori infection. Proc Natl Acad Sci U S A 2010; 107: 11056-61.
50. Schuijers J, van der Flier LG, van Es J, Clevers H. Robust cre-mediated recombination in small intestinal stem cells utilizing the olfm4 locus. Stem Cell Reports 2014; 3: 234-41.
51. Liu W, Liu Y, Zhu J, Wright E, Ding I, Rodgers GP. Reduced hGC-1 protein expression is associated with malignant progression of colon carcinoma. Clin Cancer Res 2008; 14: 1041-9.
52. Seko N, Oue N, Noguchi T et al. Olfactomedin 4 (GW112, hGC-1) is an independent prognostic marker for survival in patients with colorectal cancer. Exp Ther Med 2010; 1: 73-8.
53. Duan C, Liu X, Liang S et al. Oestrogen receptor-mediated expression of Olfactomedin 4 regulates the progression of endometrial adenocarcinoma. J Cell Mol Med 2014; 18: 863-74.
54. Sentani K, Oue N, Naito Y et al. Upregulation of HOXA10 in gastric cancer with the intestinal mucin phenotype: reduction during tumor progression and favorable prognosis. Carcinogenesis 2012; 33: 1081-8.
55. McGinnis W, Krumlauf R. Homeobox genes and axial patterning. Cell 1992; 68: 283-302.
56. Li B, Cao X, Weng C et al. HoxA10 induces proliferation in human prostate carcinoma PC-3 cell line. Cell Biochem Biophys 2014; 70: 1363-8.
57. Calvo R, West J, Franklin W et al. Altered HOX and WNT7A expression in human lung cancer. Proc Natl Acad Sci U S A 2000; 97: 12776-81.
58. Jiang Y, Chu Y, Tang W, Wan Y, Zhang L, Cheng W. Transcription factor WT1 and promoter CpG hypomethylation coactivate HOXA10 expression in ovarian cancer. Curr Pharm Des 2014; 20: 1647-54.
59. Bromleigh VC, Freedman LP. p21 is a transcriptional target of HOXA10 in differentiating myelomonocytic cells. Genes Dev 2000; 14: 2581-6.
60. Yoshida H, Broaddus R, Cheng W, Xie S, Naora H. Deregulation of the HOXA10 homeobox gene in endometrial carcinoma: role in epithelial-mesenchymal transition. Cancer Res 2006; 66: 889-97.
61. Anami K, Oue N, Noguchi T et al. Search for transmembrane protein in gastric cancer by the Escherichia coli ampicillin secretion trap: expression of DSC2 in gastric cancer with intestinal phenotype. J Pathol 2010; 221: 275-84.
62. Stokes DL. Desmosomes from a structural perspective. Curr Opin Cell Biol 2007; 19: 565-71.
63. Yin T, Green KJ. Regulation of desmosome assembly and adhesion. Semin Cell Dev Biol 2004; 15: 665-77.
64. Anami K, Oue N, Noguchi T et al. TSPAN8, identified by Escherichia coli ampicillin secretion trap, is associated with cell growth and invasion in gastric cancer. Gastric Cancer. [Epub ahead of print].
65. Zoller M. Tetraspanins: push and pull in suppressing and promoting metastasis. Nat Rev Cancer 2009; 9: 40-55.
66. Nazarenko I, Rana S, Baumann A et al. Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation. Cancer Res 2010; 70: 1668-78.
67. Oo HZ, Sentani K, Sakamoto N et al. Identification of novel transmembrane proteins in scirrhous-type gastric cancer by the Escherichia coli ampicillin secretion trap (CAST) method: TM9SF3 participates in tumor invasion and serves as a prognostic factor. Pathobiology 2014; 81: 138-48.
68. Pruvot B, Laurens V, Salvadori F, Solary E, Pichon L, Chluba J. Comparative analysis of nonaspanin protein sequences and expression studies in zebrafish. Immunogenetics 2010; 62: 681-99.
69. Cornillon S, Pech E, Benghezal M et al. Phg1p is a nine-transmembrane protein superfamily member involved in dictyostelium adhesion and phagocytosis. J Biol Chem 2000; 275: 34287-92.
70. Sanada Y, Oue N, Mitani Y, Yoshida K, Nakayama H, Yasui W. Down-regulation of the claudin-18 gene, identified through serial analysis of gene expression data analysis, in gastric cancer with an intestinal phenotype. J Pathol 2006; 208: 633-42.
71. Tsukita S, Furuse M, Itoh M. Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2001; 2: 285-93.
72. Niimi T, Nagashima K, Ward JM et al. claudin-18, a novel downstream target gene for the T/EBP/NKX2.1 homeodomain transcription factor, encodes lung- and stomach-specific isoforms through alternative splicing. Mol Cell Biol 2001; 21: 7380-90.
73. Hayashi D, Tamura A, Tanaka H et al. Deficiency of claudin-18 causes paracellular H+ leakage, up-regulation of interleukin-1beta, and atrophic gastritis in mice. Gastroenterology 2012; 142: 292-304.
74. Cancer Genome Atlas Research Network. Comprehensive molecular characterization of gastric adenocarcinoma. Nature 2014; 513: 202-9.
75. Woll S, Schlitter AM, Dhaene K et al. Claudin 18.2 is a target for IMAB362 antibody in pancreatic neoplasms. Int J Cancer 2014; 134: 731-9.
76. Silberg DG, Swain GP, Suh ER, Traber PG. Cdx1 and cdx2 expression during intestinal development. Gastroenterology 2000; 119: 961-71.
77. Silberg DG, Sullivan J, Kang E et al. Cdx2 ectopic expression induces gastric intestinal metaplasia in transgenic mice. Gastroenterology 2002; 122: 689-96.
78. Park ET, Gum JR, Kakar S, Kwon SW, Deng G, Kim YS. Aberrant expression of SOX2 upregulates MUC5AC gastric foveolar mucin in mucinous cancers of the colorectum and related lesions. Int J Cancer 2008; 122: 1253-60.
79. Tani Y, Akiyama Y, Fukamachi H, Yanagihara K, Yuasa Y. Transcription factor SOX2 up-regulates stomach-specific pepsinogen A gene expression. J Cancer Res Clin Oncol 2007; 133: 263-9.
80. Benahmed F, Gross I, Gaunt SJ et al. Multiple regulatory regions control the complex expression pattern of the mouse Cdx2 homeobox gene. Gastroenterology 2008; 135: 1238-47, 47.e1-3.
81. Hinoi T, Lucas PC, Kuick R, Hanash S, Cho KR, Fearon ER. CDX2 regulates liver intestine-cadherin expression in normal and malignant colon epithelium and intestinal metaplasia. Gastroenterology 2002; 123: 1565-77.
82. Naito Y, Oue N, Hinoi T et al. Reg IV is a direct target of intestinal transcriptional factor CDX2 in gastric cancer. PLoS ONE 2012; 7: e47545.
83. Takakura Y, Hinoi T, Oue N et al. CDX2 regulates multidrug resistance 1 gene expression in malignant intestinal epithelium. Cancer Res 2010; 70: 6767-78.
84. Kakiuchi M, Nishizawa T, Ueda H et al. Recurrent gain-of-function mutations of RHOA in diffuse-type gastric carcinoma. Nat Genet 2014; 46: 583-7.
85. Forbes SA, Beare D, Gunasekaran P et al. COSMIC: exploring the world's knowledge of somatic mutations in human cancer. Nucleic Acids Res 2015; 43: D805-11.
86. Wang K, Yuen ST, Xu J et al. Whole-genome sequencing and comprehensive molecular profiling identify new driver mutations in gastric cancer. Nat Genet 2014; 46: 573-82.
87. Uozaki H, Barua RR, Minhua S et al. Transcriptional factor typing with SOX2, HNF4aP1, and CDX2 closely relates to tumor invasion and Epstein-Barr virus status in gastric cancer. Int J Clin Exp Pathol 2011; 4: 230-40.