Skip to main content
Top
Published in: Digestive Diseases and Sciences 9/2018

01-09-2018 | Original Article

Circulating microRNA-22-3p Predicts the Malignant Progression of Precancerous Gastric Lesions from Intestinal Metaplasia to Early Adenocarcinoma

Authors: Tsung-Hsing Chen, Cheng-Tang Chiu, Chieh Lee, Yin-Yi Chu, Hao-Tsai Cheng, Jun-Te Hsu, Ren-Chin Wu, Ta-Sen Yeh, Kwang-Huei Lin

Published in: Digestive Diseases and Sciences | Issue 9/2018

Login to get access

Abstract

Background

Gastric cancer has a poor outcome and identifying useful biomarkers from peripheral blood or tissue could allow its early detection, or potentially precancerous changes, thus improving the curative rates. MicroRNAs (miRNAs) have been shown to offer great potential in cancer diagnosis and prediction.

Aim

Here, we investigated the role of plasma miRNAs in the natural course of gastric cancer, from intestinal metaplasia to early cancer. The findings were used to understand whether patients at a high risk of malignancy could be given appropriate interventions in the early disease process, such as using endoscopic submucosal dissection to treat gastric dysplasia or early gastric cancer.

Methods

Participants were divided into healthy control, intestinal metaplasia (IM), and dysplasia/early cancer (pT1a/b) groups. Microarray was used to select potential markers in tissue.

Results

Quantitative real-time polymerase chain reaction data showed circulating miRNA-22-3p had significantly different expression in patients with precancerous lesions or gastric adenocarcinoma. The areas under the curve of incomplete IM versus healthy control, low-grade/high-grade dysplasia, early gastric cancer, and GED were 0.8080, 0.8040, 0.8494, and 0.8095, respectively (all P values < 0.05).

Conclusions

Circulating miRNA-22-3p could be a potential biomarker for gastric precancerous dysplasia and early cancer detection.
Appendix
Available only for authorised users
Literature
1.
go back to reference Brenner H, Rothenbacher D, Arndt V. Epidemiology of stomach cancer. Methods Mol Biol. 2009;472:467–477.CrossRefPubMed Brenner H, Rothenbacher D, Arndt V. Epidemiology of stomach cancer. Methods Mol Biol. 2009;472:467–477.CrossRefPubMed
2.
go back to reference Karpeh M, Kelsen D, Tepper J. Cancer of the stomach. In: DeVita V, Hellman S, Rosenberg S, eds. Cancer Principles & Practice of Oncology. Philadelphia: Lippincot, Williams & Wilkins; 2001:1092–1126. Karpeh M, Kelsen D, Tepper J. Cancer of the stomach. In: DeVita V, Hellman S, Rosenberg S, eds. Cancer Principles & Practice of Oncology. Philadelphia: Lippincot, Williams & Wilkins; 2001:1092–1126.
3.
go back to reference Sugano K. Detection and management of early gastric cancer. Curr Treat Options Gastroenterol. 2015;13:398–408.CrossRefPubMed Sugano K. Detection and management of early gastric cancer. Curr Treat Options Gastroenterol. 2015;13:398–408.CrossRefPubMed
4.
go back to reference Kanzaki H, Takenaka R, Kawahara Y, et al. Linked color imaging (LCI), a novel image-enhanced endoscopy technology, emphasizes the color of early gastric cancer. Endosc Int Open. 2017;5:E1005–E1013.CrossRefPubMedPubMedCentral Kanzaki H, Takenaka R, Kawahara Y, et al. Linked color imaging (LCI), a novel image-enhanced endoscopy technology, emphasizes the color of early gastric cancer. Endosc Int Open. 2017;5:E1005–E1013.CrossRefPubMedPubMedCentral
5.
go back to reference Rugge M, Pennelli G, Pilozzi E, et al. Gastritis: the histology report. Dig Liver Dis. 2011;43:S373–S384.CrossRefPubMed Rugge M, Pennelli G, Pilozzi E, et al. Gastritis: the histology report. Dig Liver Dis. 2011;43:S373–S384.CrossRefPubMed
6.
go back to reference Leung WK, Wu MS, Kakugawa Y, et al. Screening for gastric cancer in Asia: current evidence and practice. Lancet Oncol. 2008;9:279–287.CrossRefPubMed Leung WK, Wu MS, Kakugawa Y, et al. Screening for gastric cancer in Asia: current evidence and practice. Lancet Oncol. 2008;9:279–287.CrossRefPubMed
7.
go back to reference Marrelli D, Roviello F, De Stefano A, et al. Prognostic significance of CEA, CA 19-9 and CA 72-4 preoperative serum levels in gastric carcinoma. Oncology. 1999;57:55e62.CrossRef Marrelli D, Roviello F, De Stefano A, et al. Prognostic significance of CEA, CA 19-9 and CA 72-4 preoperative serum levels in gastric carcinoma. Oncology. 1999;57:55e62.CrossRef
8.
go back to reference Esquela-Kerscher A, Slack FJ. Oncomirs—microRNAs with a role in cancer. Nat Rev Cancer. 2006;6:259–269.CrossRefPubMed Esquela-Kerscher A, Slack FJ. Oncomirs—microRNAs with a role in cancer. Nat Rev Cancer. 2006;6:259–269.CrossRefPubMed
9.
10.
go back to reference Kosaka N, Iguchi H, Ochiya T. Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci. 2010;101:2087–2092.CrossRefPubMed Kosaka N, Iguchi H, Ochiya T. Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci. 2010;101:2087–2092.CrossRefPubMed
11.
go back to reference Mitchell PS, Parkin RK, Kroh EM, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA. 2008;105:10513–10518.CrossRefPubMed Mitchell PS, Parkin RK, Kroh EM, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA. 2008;105:10513–10518.CrossRefPubMed
12.
13.
go back to reference Tsai MM, Wang CS, Tsai CY, et al. Circulating microRNA-196a/b are novel biomarkers associated with metastatic gastric cancer. Eur J Cancer. 2016;64:137e148.CrossRef Tsai MM, Wang CS, Tsai CY, et al. Circulating microRNA-196a/b are novel biomarkers associated with metastatic gastric cancer. Eur J Cancer. 2016;64:137e148.CrossRef
14.
go back to reference Correa P. Human gastric carcinogenesis: a multistep and multifactorial process—first American Cancer Society award lecture on cancer epidemiology and prevention. Cancer Res. 1992;52:6735–6740.PubMed Correa P. Human gastric carcinogenesis: a multistep and multifactorial process—first American Cancer Society award lecture on cancer epidemiology and prevention. Cancer Res. 1992;52:6735–6740.PubMed
15.
go back to reference Busuttil RA, Boussioutas A. Intestinal metaplasia: a premalignant lesion involved in gastric carcinogenesis. J Gastroenterol Hepatol. 2009;24:193–201.CrossRefPubMed Busuttil RA, Boussioutas A. Intestinal metaplasia: a premalignant lesion involved in gastric carcinogenesis. J Gastroenterol Hepatol. 2009;24:193–201.CrossRefPubMed
16.
17.
go back to reference González CA, Pardo ML, Liso JM, et al. Gastric cancer occurrence in preneoplastic lesions: a long-term follow-up in a high-risk area in Spain. Int J Cancer. 2010;127:2654–2660.CrossRefPubMed González CA, Pardo ML, Liso JM, et al. Gastric cancer occurrence in preneoplastic lesions: a long-term follow-up in a high-risk area in Spain. Int J Cancer. 2010;127:2654–2660.CrossRefPubMed
18.
go back to reference Oka S, Tanaka S, Kaneko I, et al. Advantage of endoscopic submucosal dissection compared with EMR for early gastric cancer. Gastrointest Endosc. 2006;64:877–883.CrossRefPubMed Oka S, Tanaka S, Kaneko I, et al. Advantage of endoscopic submucosal dissection compared with EMR for early gastric cancer. Gastrointest Endosc. 2006;64:877–883.CrossRefPubMed
19.
go back to reference Gotoda T. Endoscopic submucosal dissection of early gastric cancer. Curr Opin Gastroenterol. 2006;22:561–569.CrossRefPubMed Gotoda T. Endoscopic submucosal dissection of early gastric cancer. Curr Opin Gastroenterol. 2006;22:561–569.CrossRefPubMed
20.
go back to reference Salvon-Harman JC, Cady B, Nikulasson S, Khettry U, Stone MD, Lavin P. Shifting proportions of gastric adenocarcinomas. Archives of surgery (Chicago, Ill: 1960). 1994;129:381–388. (discussion 388–389).CrossRef Salvon-Harman JC, Cady B, Nikulasson S, Khettry U, Stone MD, Lavin P. Shifting proportions of gastric adenocarcinomas. Archives of surgery (Chicago, Ill: 1960). 1994;129:381–388. (discussion 388–389).CrossRef
21.
go back to reference Park JC, Lee YC, Kim JH, et al. Clinicopathological aspects and prognostic value with respect to age: an analysis of 3,362 consecutive gastric cancer patients. J Surg Oncol. 2009;99:395–401.CrossRefPubMed Park JC, Lee YC, Kim JH, et al. Clinicopathological aspects and prognostic value with respect to age: an analysis of 3,362 consecutive gastric cancer patients. J Surg Oncol. 2009;99:395–401.CrossRefPubMed
22.
go back to reference Petrelli F, Berenato R, Turati L, et al. Prognostic value of diffuse versus intestinal histotype in patients with gastric cancer: a systematic review and meta-analysis. J Gastrointest Oncol. 2017;8:148–163.CrossRefPubMedPubMedCentral Petrelli F, Berenato R, Turati L, et al. Prognostic value of diffuse versus intestinal histotype in patients with gastric cancer: a systematic review and meta-analysis. J Gastrointest Oncol. 2017;8:148–163.CrossRefPubMedPubMedCentral
23.
go back to reference Slattery ML, Herrick JS, Pellatt DF, et al. MicroRNA profiles in colorectal carcinomas, adenomas and normal colonic mucosa: variations in miRNA expression and disease progression. Carcinogenesis. 2016;37:245–261.CrossRefPubMedPubMedCentral Slattery ML, Herrick JS, Pellatt DF, et al. MicroRNA profiles in colorectal carcinomas, adenomas and normal colonic mucosa: variations in miRNA expression and disease progression. Carcinogenesis. 2016;37:245–261.CrossRefPubMedPubMedCentral
24.
go back to reference Bosman FT, Carneiro F, Hruban RH, Theise ND, eds. WHO Classification of Tumours of the Digestive System. 4th ed. Lyon: IARC Press; 2010. Bosman FT, Carneiro F, Hruban RH, Theise ND, eds. WHO Classification of Tumours of the Digestive System. 4th ed. Lyon: IARC Press; 2010.
25.
go back to reference Lin YH, Wu MH, Liao CJ, et al. Repression of microRNA-130b by thyroid hormone enhances cell motility. J Hepatol. 2015;62:1328–1340.CrossRefPubMed Lin YH, Wu MH, Liao CJ, et al. Repression of microRNA-130b by thyroid hormone enhances cell motility. J Hepatol. 2015;62:1328–1340.CrossRefPubMed
26.
go back to reference Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods. 2001;25:402–408.CrossRefPubMed Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods. 2001;25:402–408.CrossRefPubMed
27.
28.
go back to reference Correa P. Clinical implications of recent developments in gastric cancer pathology and epidemiology. Semin Oncol. 1985;12:2–10.PubMed Correa P. Clinical implications of recent developments in gastric cancer pathology and epidemiology. Semin Oncol. 1985;12:2–10.PubMed
30.
go back to reference Wang W, Li F, Zhang Y, et al. Reduced expression of miR-22 in gastric cancer is related to clinicopathologic characteristics or patient prognosis. Diagn Pathol. 2013;8:102.PubMedPubMedCentral Wang W, Li F, Zhang Y, et al. Reduced expression of miR-22 in gastric cancer is related to clinicopathologic characteristics or patient prognosis. Diagn Pathol. 2013;8:102.PubMedPubMedCentral
31.
go back to reference Zuo QF, Cao LY, Yu T, et al. MicroRNA-22 inhibits tumor growth and metastasis in gastric cancer by directly targeting MMP14 and Snail. Cell Death Dis. 2015;6:e2000.CrossRefPubMedPubMedCentral Zuo QF, Cao LY, Yu T, et al. MicroRNA-22 inhibits tumor growth and metastasis in gastric cancer by directly targeting MMP14 and Snail. Cell Death Dis. 2015;6:e2000.CrossRefPubMedPubMedCentral
32.
go back to reference Tang Y, Liu X, Su B, et al. microRNA-22 acts as a metastasis suppressor by targeting metadherin in gastric cancer. Mol Med Rep. 2015;11:454–460.CrossRefPubMed Tang Y, Liu X, Su B, et al. microRNA-22 acts as a metastasis suppressor by targeting metadherin in gastric cancer. Mol Med Rep. 2015;11:454–460.CrossRefPubMed
33.
go back to reference Wang G, Shen N, Cheng L, et al. Downregulation of miR-22 acts as an unfavorable prognostic biomarker in osteosarcoma. Tumor Biol. 2015;36:7891–7895.CrossRef Wang G, Shen N, Cheng L, et al. Downregulation of miR-22 acts as an unfavorable prognostic biomarker in osteosarcoma. Tumor Biol. 2015;36:7891–7895.CrossRef
34.
go back to reference Li B, Song Y, Liu TJ, et al. miRNA-22 suppresses colon cancer cell migration and invasion by inhibiting the expression of T-cell lymphoma invasion and metastasis 1 and matrix metalloproteinases 2 and 9. Oncol Rep. 2013;29:1932–1938.CrossRefPubMed Li B, Song Y, Liu TJ, et al. miRNA-22 suppresses colon cancer cell migration and invasion by inhibiting the expression of T-cell lymphoma invasion and metastasis 1 and matrix metalloproteinases 2 and 9. Oncol Rep. 2013;29:1932–1938.CrossRefPubMed
35.
go back to reference You Y, Tan JX, Dai HS, et al. MiRNA-22 inhibits oncogene galectin-1 in hepatocellular carcinoma. Oncotarget. 2016;7:57099–57116.PubMedPubMedCentral You Y, Tan JX, Dai HS, et al. MiRNA-22 inhibits oncogene galectin-1 in hepatocellular carcinoma. Oncotarget. 2016;7:57099–57116.PubMedPubMedCentral
Metadata
Title
Circulating microRNA-22-3p Predicts the Malignant Progression of Precancerous Gastric Lesions from Intestinal Metaplasia to Early Adenocarcinoma
Authors
Tsung-Hsing Chen
Cheng-Tang Chiu
Chieh Lee
Yin-Yi Chu
Hao-Tsai Cheng
Jun-Te Hsu
Ren-Chin Wu
Ta-Sen Yeh
Kwang-Huei Lin
Publication date
01-09-2018
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 9/2018
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-018-5106-4

Other articles of this Issue 9/2018

Digestive Diseases and Sciences 9/2018 Go to the issue