Prognostic significance of microRNA-21 expression in esophageal cancer: a systematic review and meta-analysis_West China Medical Journal

Authors：

WANG Chaokun ^1,2 ,  WANG Xinshuai ² , CHEN Jing ² , LIU Zhiwei ² , GAO Shegan ²

1. Department of Oncology, Shangqiu Municipal Hospital, Shangqiu, Henan 476000, P. R. China;
2. Department of Oncology, the First Affiliated Hospital of Henan University of Science and Technology, Luoyang, Henan 471003, P. R. China;

Corresponding?author：

WANG Xinshuai, Email: xshuaiw@haust.edu.cn

Keywords：

MicroRNA-21; esophageal cancer; prognosis; meta-analysis

DOI：

10.7507/1002-0179.202004240

Video：

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Objective To systematically evaluate the correlation between the expression of microRNA (miRNA)-21 and the prognosis of esophageal cancer. Methods PubMed, Cochrane Library, Embase, Wanfang Data, China National Knowledge Infrastructure and VIP Databases were searched by for the literature on the correlation between miRNA-21 and the prognosis of esophageal cancer till July 10, 2022. Two researchers independently performed literature screening, quality evaluation, and data extraction. Statistical analysis was conducted with Stata 14.0. Results A total of 13 articles were included, including 1 204 patients. The results of meta-analysis showed that: the overall survival (OS) of patients with high expression of miRNA-21 was lower than that of patients with low expression of miRNA-21 [hazard ratio (HR)=2.11, 95% confidence interval (CI) (1.56, 2.84), P<0.001]. miRNA-21 expression was not associated with disease free survival [HR=2.53, 95%CI (0.67, 8.22), P=0.182]. The OS of Asian patients with high expression of miRNA-21 was significantly lower [HR=2.44, 95%CI (1.71, 3.49), P=0.005], while the OS of non-Asian patients was not related to miRNA-21 expression [HR=1.34, 95%CI (0.94, 1.91), P=0.363]. The high expression of miRNA-21 was correlated with the decreased OS in patients with esophageal squamous cell carcinoma [HR=2.22, 95%CI (1.52, 3.26), P=0.001], while the OS in patients with esophageal adenocarcinoma was not correlated with the expression of miRNA-21 [HR=1.39, 95%CI (0.63, 3.06), P=0.409]. Conclusion The overexpression of miRNA-21 is associated with poor prognosis and might be regarded as a potential prognostic biomarker for patients with esophageal cancer.

Citation： WANG Chaokun, WANG Xinshuai, CHEN Jing, LIU Zhiwei, GAO Shegan. Prognostic significance of microRNA-21 expression in esophageal cancer: a systematic review and meta-analysis. West China Medical Journal, 2022, 37(8): 1213-1220. doi: 10.7507/1002-0179.202004240 Copy

1.	Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2018, 68(6): 394-424.
2.	Zeng H, Chen W, Zheng R, et al. Changing cancer survival in China during 2003-15: a pooled analysis of 17 population-based cancer registries. Lancet Glob Health, 2018, 6(5): e555-e567.
3.	Winter J, Jung S, Keller S, et al. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol, 2009, 11(3): 228-234.
4.	Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 2004, 116(2): 281-297.
5.	Zhang Q, Gan H, Song W, et al. MicroRNA-145 promotes esophageal cancer cells proliferation and metastasis by targeting SMAD5. Scand J Gastroenterol, 2018, 53(7): 769-776.
6.	Uhlmann S, Mannsperger H, Zhang JD, et al. Global microRNA level regulation of EGFR-driven cell-cycle protein network in breast cancer. Mol Syst Biol, 2012, 8: 570.
7.	Hayes J, Peruzzi PP, Lawler S. MicroRNAs in cancer: biomarkers, functions and therapy. Trends Mol Med, 2014, 20(8): 460-469.
8.	Cao D, Di M, Liang J, et al. MicroRNA-183 in cancer progression. J Cancer, 2020, 11(6): 1315-1324.
9.	Jansson MD, Lund AH. MicroRNA and cancer. Mol Oncol, 2012, 6(6): 590-610.
10.	Mavridis K, Stravodimos K, Scorilas A. Downregulation and prognostic performance of microRNA 224 expression in prostate cancer. Clin Chem, 2013, 59(1): 261-269.
11.	Cui Y, Xu HF, Liu MY, et al. Mechanism of exosomal microRNA-224 in development of hepatocellular carcinoma and its diagnostic and prognostic value. World J Gastroenterol, 2019, 25(15): 1890-1898.
12.	Peng Z, Zhu W, Dai J, et al. MicroRNA-200 as potential diagnostic markers for colorectal cancer: meta-analysis and experimental validation. Cell Mol Biol (Noisy-le-grand), 2018, 64(6): 77-85.
13.	黃聲凱, 王佳, 李燕, 等. 血清 miR-378 和 miR-21 聯合檢測對胃癌的診斷價值. 中華腫瘤雜志, 2018, 40(6): 441-445.
14.	Liao J, Liu R, Shi YJ, et al. Exosome-shuttling microRNA-21 promotes cell migration and invasion-targeting PDCD4 in esophageal cancer. Int J Oncol, 2016, 48(6): 2567-2579.
15.	劉思玉, 李宏衛. 微 RNA 在口腔鱗狀細胞癌中表達的研究進展. 中華口腔醫學雜志, 2013, 48(6): 376-380.
16.	Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
17.	周支瑞, 張天嵩, 李博, 等. 生存曲線中 Meta 分析適宜數據的提取與轉換. 中國循證心血管醫學雜志, 2014, 6(3): 243-247.
18.	Egger M, Davey Smith G, Schneider M, et al. Bias in meta-analysis detected by a simple, graphical test. BMJ, 1997, 315(7109): 629-634.
19.	Hamano R, Miyata H, Yamasaki M, et al. Overexpression of miR-200c induces chemoresistance in esophageal cancers mediated through activation of the Akt signaling pathway. Clin Cancer Res, 2011, 17(9): 3029-3038.
20.	He Y, Jin J, Wang L, et al. Evaluation of miR-21 and miR-375 as prognostic biomarkers in oesophageal cancer in high-risk areas in China. Clin Exp Metastasis, 2017, 34(1): 73-84.
21.	Hu Y, Correa AM, Hoque A, et al. Prognostic significance of differentially expressed miRNAs in esophageal cancer. Int J Cancer, 2011, 128(1): 132-143.
22.	Komatsu S, Ichikawa D, Takeshita H, et al. Prognostic impact of circulating miR-21 and miR-375 in plasma of patients with esophageal squamous cell carcinoma. Expert Opin Biol Ther, 2012, 12(Suppl 1): S53-S59.
23.	Li P, Mao WM, Zheng ZG, et al. Down-regulation of PTEN expression modulated by dysregulated miR-21 contributes to the progression of esophageal cancer. Dig Dis Sci, 2013, 58(12): 3483-3493.
24.	Li BX, Yu Q, Shi ZL, et al. Circulating microRNAs in esophageal squamous cell carcinoma: association with locoregional staging and survival. Int J Clin Exp Med, 2015, 8(5): 7241-7250.
25.	Lv H, He Z, Wang H, et al. Differential expression of miR-21 and miR-75 in esophageal carcinoma patients and its clinical implication. Am J Transl Res, 2016, 8(7): 3288-3298.
26.	Mathé EA, Nguyen GH, Bowman ED, et al. MicroRNA expression in squamous cell carcinoma and adenocarcinoma of the esophagus: associations with survival. Clin Cancer Res, 2009, 15(19): 6192-6200.
27.	Winther M, Alsner J, Tramm T, et al. Evaluation of miR-21 and miR-375 as prognostic biomarkers in esophageal cancer. Acta Oncol, 2015, 54(9): 1582-1591.
28.	Zhao Y, Schetter AJ, Yang GB, et al. microRNA and inflammatory gene expression as prognostic marker for overall survival in esophageal squamous cell carcinoma. Int J Cancer, 2013, 132(12): 2901-2909.
29.	Tanaka K, Miyata H, Yamasaki M, et al. Circulating miR-200c levels significantly predict response to chemotherapy and prognosis of patients undergoing neoadjuvant chemotherapy for esophageal cancer. Ann Surg Oncol, 2013, 20 (Suppl 3): S607-S615.
30.	向正凱, 嚴寶國. 食管癌組織中 microRNA-21 的表達及其意義. 腫瘤防治研究, 2014, 41(8): 902-905.
31.	Luo D, Huang Z, Lv H, et al. Up-regulation of microRNA-21 indicates poor prognosis and promotes cell proliferation in esophageal squamous cell carcinoma via upregulation of lncRNA SNHG1. Cancer Manag Res, 2020, 12: 1-14.
32.	王斌, 姜雷, 王冰冰, 等. miRNA-21 表達水平與結直腸癌患者預后關系的 Meta 分析. 腫瘤, 2015, 35(1): 84-91.
33.	Yuan Y, Xu XY, Zheng HG, et al. Elevated miR-21 is associated with poor prognosis in non-small cell lung cancer: a systematic review and meta-analysis. Eur Rev Med Pharmacol Sci, 2018, 22(13): 4166-4180.
34.	Wang H, Tan Z, Hu H, et al. microRNA-21 promotes breast cancer proliferation and metastasis by targeting LZTFL1. BMC Cancer, 2019, 19(1): 738.
35.	Wen SW, Zhang YF, Li Y, et al. Association of miR-21 with esophageal cancer prognosis: a meta-analysis. Genet Mol Res, 2015, 14(2): 6578-6582.
36.	Arnold M, Soerjomataram I, Ferlay J, et al. Global incidence of oesophageal cancer by histological subtype in 2012. Gut, 2015, 64(3): 381-387.
37.	Yang Z, Zeng H, Xia R, et al. Annual cost of illness of stomach and esophageal cancer patients in urban and rural areas in China: a multi-center study. Chin J Cancer Res, 2018, 30(4): 439-448.

1. Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2018, 68(6): 394-424.
2. Zeng H, Chen W, Zheng R, et al. Changing cancer survival in China during 2003-15: a pooled analysis of 17 population-based cancer registries. Lancet Glob Health, 2018, 6(5): e555-e567.
3. Winter J, Jung S, Keller S, et al. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol, 2009, 11(3): 228-234.
4. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 2004, 116(2): 281-297.
5. Zhang Q, Gan H, Song W, et al. MicroRNA-145 promotes esophageal cancer cells proliferation and metastasis by targeting SMAD5. Scand J Gastroenterol, 2018, 53(7): 769-776.
6. Uhlmann S, Mannsperger H, Zhang JD, et al. Global microRNA level regulation of EGFR-driven cell-cycle protein network in breast cancer. Mol Syst Biol, 2012, 8: 570.
7. Hayes J, Peruzzi PP, Lawler S. MicroRNAs in cancer: biomarkers, functions and therapy. Trends Mol Med, 2014, 20(8): 460-469.
8. Cao D, Di M, Liang J, et al. MicroRNA-183 in cancer progression. J Cancer, 2020, 11(6): 1315-1324.
9. Jansson MD, Lund AH. MicroRNA and cancer. Mol Oncol, 2012, 6(6): 590-610.
10. Mavridis K, Stravodimos K, Scorilas A. Downregulation and prognostic performance of microRNA 224 expression in prostate cancer. Clin Chem, 2013, 59(1): 261-269.
11. Cui Y, Xu HF, Liu MY, et al. Mechanism of exosomal microRNA-224 in development of hepatocellular carcinoma and its diagnostic and prognostic value. World J Gastroenterol, 2019, 25(15): 1890-1898.
12. Peng Z, Zhu W, Dai J, et al. MicroRNA-200 as potential diagnostic markers for colorectal cancer: meta-analysis and experimental validation. Cell Mol Biol (Noisy-le-grand), 2018, 64(6): 77-85.
13. 黃聲凱, 王佳, 李燕, 等. 血清 miR-378 和 miR-21 聯合檢測對胃癌的診斷價值. 中華腫瘤雜志, 2018, 40(6): 441-445.
14. Liao J, Liu R, Shi YJ, et al. Exosome-shuttling microRNA-21 promotes cell migration and invasion-targeting PDCD4 in esophageal cancer. Int J Oncol, 2016, 48(6): 2567-2579.
15. 劉思玉, 李宏衛. 微 RNA 在口腔鱗狀細胞癌中表達的研究進展. 中華口腔醫學雜志, 2013, 48(6): 376-380.
16. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
17. 周支瑞, 張天嵩, 李博, 等. 生存曲線中 Meta 分析適宜數據的提取與轉換. 中國循證心血管醫學雜志, 2014, 6(3): 243-247.
18. Egger M, Davey Smith G, Schneider M, et al. Bias in meta-analysis detected by a simple, graphical test. BMJ, 1997, 315(7109): 629-634.
19. Hamano R, Miyata H, Yamasaki M, et al. Overexpression of miR-200c induces chemoresistance in esophageal cancers mediated through activation of the Akt signaling pathway. Clin Cancer Res, 2011, 17(9): 3029-3038.
20. He Y, Jin J, Wang L, et al. Evaluation of miR-21 and miR-375 as prognostic biomarkers in oesophageal cancer in high-risk areas in China. Clin Exp Metastasis, 2017, 34(1): 73-84.
21. Hu Y, Correa AM, Hoque A, et al. Prognostic significance of differentially expressed miRNAs in esophageal cancer. Int J Cancer, 2011, 128(1): 132-143.
22. Komatsu S, Ichikawa D, Takeshita H, et al. Prognostic impact of circulating miR-21 and miR-375 in plasma of patients with esophageal squamous cell carcinoma. Expert Opin Biol Ther, 2012, 12(Suppl 1): S53-S59.
23. Li P, Mao WM, Zheng ZG, et al. Down-regulation of PTEN expression modulated by dysregulated miR-21 contributes to the progression of esophageal cancer. Dig Dis Sci, 2013, 58(12): 3483-3493.
24. Li BX, Yu Q, Shi ZL, et al. Circulating microRNAs in esophageal squamous cell carcinoma: association with locoregional staging and survival. Int J Clin Exp Med, 2015, 8(5): 7241-7250.
25. Lv H, He Z, Wang H, et al. Differential expression of miR-21 and miR-75 in esophageal carcinoma patients and its clinical implication. Am J Transl Res, 2016, 8(7): 3288-3298.
26. Mathé EA, Nguyen GH, Bowman ED, et al. MicroRNA expression in squamous cell carcinoma and adenocarcinoma of the esophagus: associations with survival. Clin Cancer Res, 2009, 15(19): 6192-6200.
27. Winther M, Alsner J, Tramm T, et al. Evaluation of miR-21 and miR-375 as prognostic biomarkers in esophageal cancer. Acta Oncol, 2015, 54(9): 1582-1591.
28. Zhao Y, Schetter AJ, Yang GB, et al. microRNA and inflammatory gene expression as prognostic marker for overall survival in esophageal squamous cell carcinoma. Int J Cancer, 2013, 132(12): 2901-2909.
29. Tanaka K, Miyata H, Yamasaki M, et al. Circulating miR-200c levels significantly predict response to chemotherapy and prognosis of patients undergoing neoadjuvant chemotherapy for esophageal cancer. Ann Surg Oncol, 2013, 20 (Suppl 3): S607-S615.
30. 向正凱, 嚴寶國. 食管癌組織中 microRNA-21 的表達及其意義. 腫瘤防治研究, 2014, 41(8): 902-905.
31. Luo D, Huang Z, Lv H, et al. Up-regulation of microRNA-21 indicates poor prognosis and promotes cell proliferation in esophageal squamous cell carcinoma via upregulation of lncRNA SNHG1. Cancer Manag Res, 2020, 12: 1-14.
32. 王斌, 姜雷, 王冰冰, 等. miRNA-21 表達水平與結直腸癌患者預后關系的 Meta 分析. 腫瘤, 2015, 35(1): 84-91.
33. Yuan Y, Xu XY, Zheng HG, et al. Elevated miR-21 is associated with poor prognosis in non-small cell lung cancer: a systematic review and meta-analysis. Eur Rev Med Pharmacol Sci, 2018, 22(13): 4166-4180.
34. Wang H, Tan Z, Hu H, et al. microRNA-21 promotes breast cancer proliferation and metastasis by targeting LZTFL1. BMC Cancer, 2019, 19(1): 738.
35. Wen SW, Zhang YF, Li Y, et al. Association of miR-21 with esophageal cancer prognosis: a meta-analysis. Genet Mol Res, 2015, 14(2): 6578-6582.
36. Arnold M, Soerjomataram I, Ferlay J, et al. Global incidence of oesophageal cancer by histological subtype in 2012. Gut, 2015, 64(3): 381-387.
37. Yang Z, Zeng H, Xia R, et al. Annual cost of illness of stomach and esophageal cancer patients in urban and rural areas in China: a multi-center study. Chin J Cancer Res, 2018, 30(4): 439-448.

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