Anterior gradient 2 downregulation in a subset of pancreatic ductal adenocarcinoma is a prognostic factor indicative of epithelial-mesenchymal transition

Laboratory Investigation

Volumn 95, Issue 2, 2015, Pages 193-206

  Mizuuchi, Yusuke ^a,b   Aishima, Shinichi ^a   Ohuchida, Kenoki ^a   Shindo, Koji ^a,b   Fujino, Minoru ^a   Hattori, Masami ^a   Miyazaki, Tetsuyuki ^a   Mizumoto, Kazuhiro ^c   Tanaka, Masao ^a   Oda, Yoshinao ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^c KYUSHU UNIVERSITY HOSPITAL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTERIOR GRADIENT 2; BIOLOGICAL MARKER; NEUTRALIZING ANTIBODY; PROTEIN DISULFIDE ISOMERASE; RECOMBINANT RECEPTOR; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; AGR2 PROTEIN, HUMAN; CADHERIN; PRIMER DNA; PROTEIN; TUMOR MARKER;

ADULT; ADVANCED CANCER; ADVERSE OUTCOME; AGED; ARTICLE; CANCER GRADING; CANCER PATIENT; CANCER PROGNOSIS; CANCER STAGING; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; COCULTURE; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; EARLY CANCER; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MAJOR CLINICAL STUDY; MALE; MONOCULTURE; PANCREAS ADENOCARCINOMA; PANCREAS ADENOMA; PANCREATIC CANCER CELL LINE; PANCREATIC STELLATE CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; CELL MOTION; CFU COUNTING; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; GENETICS; INFECTIOUS PANCREATIC NECROSIS VIRUS; KAPLAN MEIER METHOD; METABOLISM; PANCREAS CARCINOMA; PATHOPHYSIOLOGY; PHYSIOLOGY; PROGNOSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TUMOR INVASION; WESTERN BLOTTING;

BLOTTING, WESTERN; CADHERINS; CARCINOMA, PANCREATIC DUCTAL; CELL MOVEMENT; CELL PROLIFERATION; COLONY-FORMING UNITS ASSAY; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; INFECTIOUS PANCREATIC NECROSIS VIRUS; KAPLAN-MEIER ESTIMATE; NEOPLASM INVASIVENESS; PROGNOSIS; PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSFORMING GROWTH FACTOR BETA; TUMOR MARKERS, BIOLOGICAL; VIMENTIN;

EID: 84921851371     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2014.138     Document Type: Article

References (44)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012;62:10-29.
2. Hruban RH, Wilentz RE, Kern SE. Genetic progression in the pancreatic ducts. Am J Pathol 2000;156:1821-1825.
3. van Heek T, Rader AE, Offerhaus GJ, et al. K-ras, p53, and DPC4 (MAD4) alterations in fine-needle aspirates of the pancreas: a molecular panel correlates with and supplements cytologic diagnosis. Am J Clin Pathol 2002;117:755-765.
4. Hansel DE, Kern SE, Hruban RH. Molecular pathogenesis of pancreatic cancer. Annu Rev Genomics Hum Genet 2003;4:237-256.
5. Sive HL, Hattori K, Weintraub H. Progressive determination during formation of the anteroposterior axis in Xenopus laevis. Cell 1989; 58:171-180.
6. Thompson DA, Weigel RJ. HAG-2, the human homologue of the Xenopus laevis cement gland gene XAG-2, is coexpressed with estrogen receptor in breast cancer cell lines. Biochem Biophys Res Commun 1998;251:111-116.
7. Aberger F, Weidinger G, Grunz H, et al. Anterior specification of embryonic ectoderm: the role of the Xenopus cement gland-specific gene XAG-2. Mech Dev 1998;72:115-130.
8. Kumar A, Godwin JW, Gates PB, et al. Molecular basis for the nerve dependence of limb regeneration in an adult vertebrate. Science 2007;318:772-777.
9. Brychtova V, Vojtesek B, Hrstka R. Anterior gradient 2: a novel player in tumor cell biology. Cancer Lett 2011;304:1-7.
10. Darb-Esfahani S, Fritzsche F, Kristiansen G, et al. Anterior gradient protein 2 (AGR2) is an independent prognostic factor in ovarian highgrade serous carcinoma. Virchows Arch 2012;461:109-116.
11. Innes HE, Liu D, Barraclough R, et al. Significance of the metastasisinducing protein AGR2 for outcome in hormonally treated breast cancer patients. Br J Cancer 2006;94:1057-1065.
12. Wang Z, Hao Y, Lowe AW. The adenocarcinoma-associated antigen, AGR2, promotes tumor growth, cell migration, and cellular transformation. Cancer Res 2008;68:492-497.
13. Zhang Y, Forootan SS, Liu D, et al. Increased expression of anterior gradient-2 is significantly associated with poor survival of prostate cancer patients. Prostate Cancer Prostatic Dis 2007;10:293-300.
14. Ramachandran V, Arumugam T, Wang H, et al. Anterior gradient 2 is expressed and secreted during the development of pancreatic cancer and promotes cancer cell survival. Cancer Res 2008;68:7811-7818.
15. Riener MO, Pilarsky C, Gerhardt J, et al. Prognostic significance of AGR2 in pancreatic ductal adenocarcinoma. Histol Histopathol 2009;24: 1121-1128.
16. Dumartin L, Whiteman HJ, Weeks ME, et al. AGR2 is a novel surface antigen that promotes the dissemination of pancreatic cancer cells through regulation of cathepsins B and D. Cancer Res 2011;71:7091-7102.
17. Hugo H, Ackland ML, Blick T, et al. Epithelial-mesenchymal and mesenchymal-epithelial transitions in carcinoma progression. J cell Physiol 2007;213:374-383.
18. Prudkin L, Liu DD, Ozburn NC, et al. Epithelial-to-mesenchymal transition in the development and progression of adenocarcinoma and squamous cell carcinoma of the lung. Mod Pathol 2009;22: 668-678.
19. Morali OG, Delmas V, Moore R, et al. IGF-II induces rapid beta-catenin relocation to the nucleus during epithelium to mesenchyme transition. Oncogene 2001;20:4942-4950.
20. Jeong H, Ryu YJ, An J, et al. Epithelial-mesenchymal transition in breast cancer correlates with high histological grade and triplenegative phenotype. Histopathology 2012;60:E87-E95.
21. Bachem MG, Schneider E, Gross H, et al. Identification, culture, and characterization of pancreatic stellate cells in rats and humans. Gastroenterology 1998;115:421-432.
22. Erkan M, Adler G, Apte MV, et al. StellaTUM: current consensus and discussion on pancreatic stellate cell research. Gut 2012;61:172-178.
23. Hwang RF, Moore T, Arumugam T, et al. Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res 2008;68:918-926.
24. Miettinen PJ, Ebner R, Lopez AR, et al. TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J Cell Biol 1994;127:2021-2036.
25. Sakuma K, Aoki M, Kannagi R. Transcription factors c-Myc and CDX2 mediate E-selectin ligand expression in colon cancer cells undergoing EGF/bFGF-induced epithelial-mesenchymal transition. Proc Natl Acad Sci USA 2012;109:7776-7781.
26. El-Hariry I, Pignatelli M, Lemoine NR. FGF-1 and FGF-2 regulate the expression of E-cadherin and catenins in pancreatic adenocarcinoma. Int J Cancer 2001;94:652-661.
27. Kikuta K, Masamune A, Watanabe T, et al. Pancreatic stellate cells promote epithelial-mesenchymal transition in pancreatic cancer cells. Biochem Biophys Res Commun 2010;403:380-384.
28. Al-Aynati MM, Radulovich N, Riddell RH, et al. Epithelial-cadherin and b-catenin expression changes in pancreatic intraepithelial neoplasia. Clin Cancer Res 2004;10:1235-1240.
29. Ohuchida K, Mizumoto K, Ishikawa N, et al. The role of S100A6 in pancreatic cancer development and its clinical implication as a diagnostic marker and therapeutic target. Clin Cancer Res 2005;11: 7785-7793.
30. Ikenaga N, Ohuchida K, Mizumoto K, et al. CD10+ pancreatic stellate cells enhance the progression of pancreatic cancer. Gastroenterology 2010;139:1041-1051.
31. Odate S, Nakamura K, Onishi H, et al. TrkB/BDNF signaling pathway is a potential therapeutic target for pulmonary large cell neuroendocrine carcinoma. Lung Cancer 2013;79:205-214.
32. Tsang ML, Zhou L, Zheng BL, et al. Characterization of recombinant soluble human transforming growth factor-beta receptor type II (rhTGF-beta sRII). Cytokine 1995;7:389-397.
33. Ellenrieder V, Hendler SF, Boeck W, et al. Transforming growth factor beta1 treatment leads to an epithelial-mesenchymal transdifferentiation of pancreatic cancer cells requiring extracellular signalregulated kinase 2 activation. Cancer Res 2001;61:4222-4228.
34. Norris AM, Gore A, Balboni A, et al. AGR2 is a SMAD4-suppressible gene that modulates MUC1 levels and promotes the initiation and progression of pancreatic intraepithelial neoplasia. Oncogene 2013;32:3867-3876.
35. Maresh EL, Mah V, Alavi M, et al. Differential expression of anterior gradient gene AGR2 in prostate cancer. BMC Cancer 2010;10:680.
36. Ho ME, Quek SI, True LD, et al. Prostate cancer cell phenotypes based on AGR2 and CD10 expression. Mod Pathol 2013;26:849-859.
37. Fritzsche FR, Dahl E, Pahl S, et al. Prognostic relevance of AGR2 expression in breast cancer. Clin Cancer Res 2006;12:1728-1734.
38. Chen R, Pan S, Duan X, et al. Elevated level of anterior gradient-2 in pancreatic juice from patients with pre-malignant pancreatic neoplasia. Mol Cancer 2010;9:149.
39. Riener MO, Thiesler T, Hellerbrand C, et al. Loss of Anterior gradient-2 expression is an independent prognostic factor in colorectal carcinomas. Eur J Cancer 2014;50:1722-1730.
40. Yang G, Truong LD, Wheeler TM, et al. Caveolin-1 expression in clinically confined human prostate cancer: a novel prognostic marker. Cancer Res 1999;59:5719-5723.
41. Bender FC, Reymond MA, Bron C, et al. Caveolin-1 levels are downregulated in human colon tumors, and ectopic expression of caveolin-1 in colon carcinoma cell lines reduces cell tumorigenicity. Cancer Res 2000;60:5870-5878.
42. Shi C, Washington MK, Chaturvedi R, et al. Fibrogenesis in pancreatic cancer is a dynamic process regulated by macrophage-stellate cell interaction. Lab Invest 2014;94:409-421.
43. Schutte M, Hruban RH, Hedrick L, et al. DPC4 gene in various tumor types. Cancer Res 1996;56:2527-2530.
44. Zavadil J, Bitzer M, Liang D, et al. Genetic programs of epithelial cell plasticity directed by transforming growth factor-beta. Proc Natl Acad Sci USA 2001;98:6686-6691.