Skip to main content
Top
Published in: BMC Cancer 1/2021

01-12-2021 | Gallbladder Cancer | Research article

Prognostic value of low microRNA-34a expression in human gastrointestinal cancer: a systematic review and meta-analysis

Authors: Yan-Ling Chen, Xiao-Lin Liu, Ling Li

Published in: BMC Cancer | Issue 1/2021

Login to get access

Abstract

Background

Mounting evidence shows that microRNA-34a (miR-34a) is involved in cancer prognosis. Therefore, we summarize the predictive role of miR-34a for survival in patients with gastrointestinal cancers (GICs).

Methods

All eligible studies were found by searching PubMed, Web of Science and EMBASE, and survival results were extracted. Then, the hazard ratio (HR) with the corresponding 95% confidence interval (CI) was calculated to evaluate the prognostic role of miR-34a in GICs. The association between miR-34a expression and clinicopathological characteristics was estimated by odds ratios (ORs) and 95% CIs.

Results

A total of 20 studies were included in this meta-analysis. For overall survival (OS), lower miR-34a expression could probably predict poorer outcome in GICs, with a pooled HR of 1.86 (95% CI: 1.52–2.28, P < 0.01). For disease-free survival (DFS), progression-free survival (PFS), and recurrence-free survival (RFS), lower miR-34a expression was related to worse DFS/PFS/RFS with a pooled HR of 1.86 (95% CI: 1.31–2.63, P  <  0.01). A significant relation of differentiation/TNM stage/lymphatic metastasis and the expression level of miR-34a was identified.

Conclusion

This meta-analysis revealed that lower miR-34a expression is significantly connected with worse OS and DFS/PFS/RFS in GIC patients. In addition, the miR-34a expression level is relatively lower in patients with lymph node metastasis than in patients without lymph node metastasis, and decreased miR-34a expression levels are linked to poor tumour differentiation and late TNM stage. MiR-34a may become a new factor for the prognosis prediction and progression of GICs.
Appendix
Available only for authorised users
Literature
1.
2.
go back to reference Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, Jemal A, Yu XQ, He J. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66(2):115–32.PubMedCrossRef Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, Jemal A, Yu XQ, He J. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66(2):115–32.PubMedCrossRef
4.
5.
go back to reference Iorio MV, Croce CM. MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol Med. 2012;4(3):143–59.PubMedPubMedCentralCrossRef Iorio MV, Croce CM. MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol Med. 2012;4(3):143–59.PubMedPubMedCentralCrossRef
6.
go back to reference Yang L, Song X, Zhu J, Li M, Ji Y, Wu F, Chen Y, Cui X, Hu J, Wang L, et al. Tumor suppressor microRNA-34a inhibits cell migration and invasion by targeting MMP-2/MMP-9/FNDC3B in esophageal squamous cell carcinoma. Int J Oncol. 2017;51(1):378–88.PubMedCrossRef Yang L, Song X, Zhu J, Li M, Ji Y, Wu F, Chen Y, Cui X, Hu J, Wang L, et al. Tumor suppressor microRNA-34a inhibits cell migration and invasion by targeting MMP-2/MMP-9/FNDC3B in esophageal squamous cell carcinoma. Int J Oncol. 2017;51(1):378–88.PubMedCrossRef
7.
go back to reference Wu H, Huang M, Liu Y, Shu Y, Liu P. Luteolin induces apoptosis by up-regulating miR-34a in human gastric Cancer cells. Technol Cancer Res Treat. 2015;14(6):747–55.PubMedCrossRef Wu H, Huang M, Liu Y, Shu Y, Liu P. Luteolin induces apoptosis by up-regulating miR-34a in human gastric Cancer cells. Technol Cancer Res Treat. 2015;14(6):747–55.PubMedCrossRef
8.
go back to reference Hiyoshi Y, Schetter AJ, Okayama H, Inamura K, Anami K, Nguyen GH, Horikawa I, Hawkes JE, Bowman ED, Leung SY, et al. Increased microRNA-34b and -34c predominantly expressed in stromal tissues is associated with poor prognosis in human colon cancer. PLoS One. 2015;10(4):e0124899.PubMedPubMedCentralCrossRef Hiyoshi Y, Schetter AJ, Okayama H, Inamura K, Anami K, Nguyen GH, Horikawa I, Hawkes JE, Bowman ED, Leung SY, et al. Increased microRNA-34b and -34c predominantly expressed in stromal tissues is associated with poor prognosis in human colon cancer. PLoS One. 2015;10(4):e0124899.PubMedPubMedCentralCrossRef
9.
go back to reference Sun TY, Xie HJ, Li Z, Kong LF, Gou XN, Li DJ, Shi YJ. Ding YZ: miR-34a regulates HDAC1 expression to affect the proliferation and apoptosis of hepatocellular carcinoma. Am J Transl Res. 2017;9(1):103–14.PubMedPubMedCentral Sun TY, Xie HJ, Li Z, Kong LF, Gou XN, Li DJ, Shi YJ. Ding YZ: miR-34a regulates HDAC1 expression to affect the proliferation and apoptosis of hepatocellular carcinoma. Am J Transl Res. 2017;9(1):103–14.PubMedPubMedCentral
10.
go back to reference Long LM, Zhan JK, Wang HQ, Li S, Chen YY, Liu YS. The clinical significance of miR-34a in pancreatic ductal carcinoma and associated molecular and cellular mechanisms. Pathobiology. 2017;84(1):38–48.PubMedCrossRef Long LM, Zhan JK, Wang HQ, Li S, Chen YY, Liu YS. The clinical significance of miR-34a in pancreatic ductal carcinoma and associated molecular and cellular mechanisms. Pathobiology. 2017;84(1):38–48.PubMedCrossRef
11.
go back to reference Jin K, Xiang Y, Tang J, Wu G, Li J, Xiao H, Li C, Chen Y. Zhao J: miR-34 is associated with poor prognosis of patients with gallbladder cancer through regulating telomere length in tumor stem cells. Tumour Biol. 2014;35(2):1503–10.PubMedCrossRef Jin K, Xiang Y, Tang J, Wu G, Li J, Xiao H, Li C, Chen Y. Zhao J: miR-34 is associated with poor prognosis of patients with gallbladder cancer through regulating telomere length in tumor stem cells. Tumour Biol. 2014;35(2):1503–10.PubMedCrossRef
12.
go back to reference Gao H, Zhao H, Xiang W. Expression level of human miR-34a correlates with glioma grade and prognosis. J Neuro-Oncol. 2013;113(2):221–8.CrossRef Gao H, Zhao H, Xiang W. Expression level of human miR-34a correlates with glioma grade and prognosis. J Neuro-Oncol. 2013;113(2):221–8.CrossRef
13.
go back to reference Shi H, Zhou S, Liu J, Zhu J, Xue J, Gu L. Chen Y: miR-34a inhibits the in vitro cell proliferation and migration in human esophageal cancer. Pathol Res Pract. 2016;212(5):444–9.PubMedCrossRef Shi H, Zhou S, Liu J, Zhu J, Xue J, Gu L. Chen Y: miR-34a inhibits the in vitro cell proliferation and migration in human esophageal cancer. Pathol Res Pract. 2016;212(5):444–9.PubMedCrossRef
14.
go back to reference Chu J, Li H, Xing Y, Jia J, Sheng J, Yang L, Sun K, Qu Y, Zhang Y, Yin H, et al. LncRNA MNX1-AS1 promotes progression of esophageal squamous cell carcinoma by regulating miR-34a/SIRT1 axis. Biomed Pharmacother. 2019;116:109029.PubMedCrossRef Chu J, Li H, Xing Y, Jia J, Sheng J, Yang L, Sun K, Qu Y, Zhang Y, Yin H, et al. LncRNA MNX1-AS1 promotes progression of esophageal squamous cell carcinoma by regulating miR-34a/SIRT1 axis. Biomed Pharmacother. 2019;116:109029.PubMedCrossRef
15.
go back to reference Yoon JH, Choi WS, Kim O, Choi BJ, Nam SW, Lee JY, Park WS. Gastrokine 1 inhibits gastric cancer cell migration and invasion by downregulating RhoA expression. Gastric Cancer. 2017;20(2):274–85.PubMedCrossRef Yoon JH, Choi WS, Kim O, Choi BJ, Nam SW, Lee JY, Park WS. Gastrokine 1 inhibits gastric cancer cell migration and invasion by downregulating RhoA expression. Gastric Cancer. 2017;20(2):274–85.PubMedCrossRef
16.
go back to reference Li N, Fu H, Tie Y, Hu Z, Kong W, Wu Y. Zheng X: miR-34a inhibits migration and invasion by down-regulation of c-met expression in human hepatocellular carcinoma cells. Cancer Lett. 2009;275(1):44–53.PubMedCrossRef Li N, Fu H, Tie Y, Hu Z, Kong W, Wu Y. Zheng X: miR-34a inhibits migration and invasion by down-regulation of c-met expression in human hepatocellular carcinoma cells. Cancer Lett. 2009;275(1):44–53.PubMedCrossRef
17.
go back to reference Cheng C, Qin Y, Zhi Q, Wang J, Qin C. Knockdown of long non-coding RNA HOTAIR inhibits cisplatin resistance of gastric cancer cells through inhibiting the PI3K/Akt and Wnt/β-catenin signaling pathways by up-regulating miR-34a. Int J Biol Macromol. 2018;107(Pt B):2620–9.PubMedCrossRef Cheng C, Qin Y, Zhi Q, Wang J, Qin C. Knockdown of long non-coding RNA HOTAIR inhibits cisplatin resistance of gastric cancer cells through inhibiting the PI3K/Akt and Wnt/β-catenin signaling pathways by up-regulating miR-34a. Int J Biol Macromol. 2018;107(Pt B):2620–9.PubMedCrossRef
18.
go back to reference Peng Y, Guo JJ, Liu YM, Wu XL. MicroRNA-34A inhibits the growth, invasion and metastasis of gastric cancer by targeting PDGFR and MET expression. Biosci Rep. 2014;34(3):e00112.PubMedPubMedCentralCrossRef Peng Y, Guo JJ, Liu YM, Wu XL. MicroRNA-34A inhibits the growth, invasion and metastasis of gastric cancer by targeting PDGFR and MET expression. Biosci Rep. 2014;34(3):e00112.PubMedPubMedCentralCrossRef
19.
go back to reference Lai M, Du G, Shi R, Yao J, Yang G, Wei Y, Zhang D, Xu Z, Zhang R, Li Y, et al. MiR-34a inhibits migration and invasion by regulating the SIRT1/p53 pathway in human SW480 cells. Mol Med Rep. 2015;11(5):3301–7.PubMedPubMedCentralCrossRef Lai M, Du G, Shi R, Yao J, Yang G, Wei Y, Zhang D, Xu Z, Zhang R, Li Y, et al. MiR-34a inhibits migration and invasion by regulating the SIRT1/p53 pathway in human SW480 cells. Mol Med Rep. 2015;11(5):3301–7.PubMedPubMedCentralCrossRef
20.
go back to reference Xu X, Chen W, Miao R, Zhou Y, Wang Z, Zhang L, Wan Y, Dong Y, Qu K, Liu C. miR-34a induces cellular senescence via modulation of telomerase activity in human hepatocellular carcinoma by targeting FoxM1/c-Myc pathway. Oncotarget. 2015;6(6):3988–4004.PubMedPubMedCentralCrossRef Xu X, Chen W, Miao R, Zhou Y, Wang Z, Zhang L, Wan Y, Dong Y, Qu K, Liu C. miR-34a induces cellular senescence via modulation of telomerase activity in human hepatocellular carcinoma by targeting FoxM1/c-Myc pathway. Oncotarget. 2015;6(6):3988–4004.PubMedPubMedCentralCrossRef
21.
go back to reference Hu Y, Correa AM, Hoque A, Guan B, Ye F, Huang J, Swisher SG, Wu TT, Ajani JA, Xu X-C. Prognostic significance of differentially expressed miRNAs in esophageal cancer. Int J Cancer. 2011;128(1):132–43.PubMedPubMedCentralCrossRef Hu Y, Correa AM, Hoque A, Guan B, Ye F, Huang J, Swisher SG, Wu TT, Ajani JA, Xu X-C. Prognostic significance of differentially expressed miRNAs in esophageal cancer. Int J Cancer. 2011;128(1):132–43.PubMedPubMedCentralCrossRef
22.
go back to reference Hui W-T, Ma X-B, Zan Y, Wang X-J, Dong L. Prognostic significance of MiR-34a expression in patients with gastric Cancer after radical Gastrectomy. Chin Med J. 2015;128(19):2632–7.PubMedPubMedCentralCrossRef Hui W-T, Ma X-B, Zan Y, Wang X-J, Dong L. Prognostic significance of MiR-34a expression in patients with gastric Cancer after radical Gastrectomy. Chin Med J. 2015;128(19):2632–7.PubMedPubMedCentralCrossRef
23.
go back to reference Yang B, Huang J, Liu H, Guo W. Li G: miR-335 directly, while miR-34a indirectly modulate survivin expression and regulate growth, apoptosis, and invasion of gastric cancer cells. Tumour Biol. 2016;37(2):1771–9.PubMedCrossRef Yang B, Huang J, Liu H, Guo W. Li G: miR-335 directly, while miR-34a indirectly modulate survivin expression and regulate growth, apoptosis, and invasion of gastric cancer cells. Tumour Biol. 2016;37(2):1771–9.PubMedCrossRef
24.
go back to reference Osawa S, Shimada Y, Sekine S, Okumura T, Nagata T, Fukuoka J, Tsukada K. MicroRNA profiling of gastric cancer patients from formalin-fixed paraffin-embedded samples. Oncol Lett. 2011;2(4):613–9.PubMedPubMedCentralCrossRef Osawa S, Shimada Y, Sekine S, Okumura T, Nagata T, Fukuoka J, Tsukada K. MicroRNA profiling of gastric cancer patients from formalin-fixed paraffin-embedded samples. Oncol Lett. 2011;2(4):613–9.PubMedPubMedCentralCrossRef
25.
go back to reference Zhang X, Ai F, Li X, Tian L, Wang X, Shen S, Liu F. MicroRNA-34a suppresses colorectal cancer metastasis by regulating notch signaling. Oncol Lett. 2017;14(2):2325–33.PubMedPubMedCentralCrossRef Zhang X, Ai F, Li X, Tian L, Wang X, Shen S, Liu F. MicroRNA-34a suppresses colorectal cancer metastasis by regulating notch signaling. Oncol Lett. 2017;14(2):2325–33.PubMedPubMedCentralCrossRef
26.
go back to reference Wang M, Zhang P, Li Y, Liu G, Zhou B, Zhan L, Zhou Z, Sun X. The quantitative analysis by stem-loop real-time PCR revealed the microRNA-34a, microRNA-155 and microRNA-200c overexpression in human colorectal cancer. Med Oncol. 2012;29(5):3113–8.PubMedCrossRef Wang M, Zhang P, Li Y, Liu G, Zhou B, Zhan L, Zhou Z, Sun X. The quantitative analysis by stem-loop real-time PCR revealed the microRNA-34a, microRNA-155 and microRNA-200c overexpression in human colorectal cancer. Med Oncol. 2012;29(5):3113–8.PubMedCrossRef
27.
go back to reference Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. EurJ Epidemiol. 2010;25(9):603–5.CrossRef Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. EurJ Epidemiol. 2010;25(9):603–5.CrossRef
28.
go back to reference Tierney JF, Stewart LA, Ghersi D, Burdett S, Sydes MR. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials. 2007;8:16.PubMedPubMedCentralCrossRef Tierney JF, Stewart LA, Ghersi D, Burdett S, Sydes MR. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials. 2007;8:16.PubMedPubMedCentralCrossRef
29.
go back to reference Lin X, Xu XY, Chen QS, Huang C. Clinical significance of microRNA-34a in esophageal squamous cell carcinoma. Genet Mol Res. 2015;14(4):17684–91.PubMedCrossRef Lin X, Xu XY, Chen QS, Huang C. Clinical significance of microRNA-34a in esophageal squamous cell carcinoma. Genet Mol Res. 2015;14(4):17684–91.PubMedCrossRef
30.
go back to reference Wei B, Huang QY, Huang SR, Mai W, Zhong XG. MicroRNA-34a attenuates the proliferation, invasion and metastasis of gastric cancer cells via downregulation of MET. Mol Med Rep. 2015;12(4):5255–61.PubMedCrossRef Wei B, Huang QY, Huang SR, Mai W, Zhong XG. MicroRNA-34a attenuates the proliferation, invasion and metastasis of gastric cancer cells via downregulation of MET. Mol Med Rep. 2015;12(4):5255–61.PubMedCrossRef
31.
go back to reference Zhang H, Li S, Yang J, Liu S, Gong X, Yu X. The prognostic value of miR-34a expression in completely resected gastric cancer: tumor recurrence and overall survival. Int J Clin Exp Med. 2015;8(2):2635–41.PubMedPubMedCentral Zhang H, Li S, Yang J, Liu S, Gong X, Yu X. The prognostic value of miR-34a expression in completely resected gastric cancer: tumor recurrence and overall survival. Int J Clin Exp Med. 2015;8(2):2635–41.PubMedPubMedCentral
32.
go back to reference Li X-Y, Wen J-Y, Jia C-C, Wang T-T, Li X, Dong M, Lin QU, Chen Z-H, Ma X-K, Wei LI, et al. MicroRNA-34a-5p enhances sensitivity to chemotherapy by targeting AXL in hepatocellular carcinoma MHCC-97L cells. Oncol Lett. 2015;10(5):2691–8.PubMedPubMedCentralCrossRef Li X-Y, Wen J-Y, Jia C-C, Wang T-T, Li X, Dong M, Lin QU, Chen Z-H, Ma X-K, Wei LI, et al. MicroRNA-34a-5p enhances sensitivity to chemotherapy by targeting AXL in hepatocellular carcinoma MHCC-97L cells. Oncol Lett. 2015;10(5):2691–8.PubMedPubMedCentralCrossRef
33.
go back to reference Yang F, Li Q-J, Gong Z-B, Zhou L, You N, Wang S, Li X-L, Li J-J, An J-Z, Wang D-S, et al. MicroRNA-34a targets Bcl-2 and sensitizes human hepatocellular carcinoma cells to sorafenib treatment. Technol Cancer Res Treat. 2014;13(1):77–86.PubMedCrossRef Yang F, Li Q-J, Gong Z-B, Zhou L, You N, Wang S, Li X-L, Li J-J, An J-Z, Wang D-S, et al. MicroRNA-34a targets Bcl-2 and sensitizes human hepatocellular carcinoma cells to sorafenib treatment. Technol Cancer Res Treat. 2014;13(1):77–86.PubMedCrossRef
34.
go back to reference Cui X, Wu Y, Wang Z, Liu X, Wang S, Qin C. MicroRNA-34a expression is predictive of recurrence after radiofrequency ablation in early hepatocellular carcinoma. Tumour Biol. 2015;36(5):3887–93.PubMedCrossRef Cui X, Wu Y, Wang Z, Liu X, Wang S, Qin C. MicroRNA-34a expression is predictive of recurrence after radiofrequency ablation in early hepatocellular carcinoma. Tumour Biol. 2015;36(5):3887–93.PubMedCrossRef
35.
go back to reference Ohuchida K, Mizumoto K, Kayashima T, Fujita H, Moriyama T, Ohtsuka T, Ueda J, Nagai E, Hashizume M, Tanaka M. MicroRNA expression as a predictive marker for gemcitabine response after surgical resection of pancreatic cancer. Ann Surg Oncol. 2011;18(8):2381–7.PubMedPubMedCentralCrossRef Ohuchida K, Mizumoto K, Kayashima T, Fujita H, Moriyama T, Ohtsuka T, Ueda J, Nagai E, Hashizume M, Tanaka M. MicroRNA expression as a predictive marker for gemcitabine response after surgical resection of pancreatic cancer. Ann Surg Oncol. 2011;18(8):2381–7.PubMedPubMedCentralCrossRef
36.
go back to reference Jamieson NB, Morran DC, Morton JP, Ali A, Dickson EJ, Carter CR, Sansom OJ, Evans TRJ, McKay CJ, Oien KA. MicroRNA molecular profiles associated with diagnosis, clinicopathologic criteria, and overall survival in patients with resectable pancreatic ductal adenocarcinoma. Clin Cancer Res. 2012;18(2):534–45.PubMedCrossRef Jamieson NB, Morran DC, Morton JP, Ali A, Dickson EJ, Carter CR, Sansom OJ, Evans TRJ, McKay CJ, Oien KA. MicroRNA molecular profiles associated with diagnosis, clinicopathologic criteria, and overall survival in patients with resectable pancreatic ductal adenocarcinoma. Clin Cancer Res. 2012;18(2):534–45.PubMedCrossRef
37.
go back to reference Sun Z, Zhang B, Cui T. Long non-coding RNA XIST exerts oncogenic functions in pancreatic cancer via miR-34a-5p. Oncol Rep. 2018;39(4):1591–600.PubMedPubMedCentral Sun Z, Zhang B, Cui T. Long non-coding RNA XIST exerts oncogenic functions in pancreatic cancer via miR-34a-5p. Oncol Rep. 2018;39(4):1591–600.PubMedPubMedCentral
38.
go back to reference Hasakova K, Reis R, Vician M, Zeman M, Herichova I. Expression of miR-34a-5p is up-regulated in human colorectal cancer and correlates with survival and clock gene PER2 expression. PLoS One. 2019;14(10):e0224396.PubMedPubMedCentralCrossRef Hasakova K, Reis R, Vician M, Zeman M, Herichova I. Expression of miR-34a-5p is up-regulated in human colorectal cancer and correlates with survival and clock gene PER2 expression. PLoS One. 2019;14(10):e0224396.PubMedPubMedCentralCrossRef
39.
go back to reference Gao J, Li N, Dong Y, Li S, Xu L, Li X, Li Y, Li Z, Ng SS, Sung JJ, et al. miR-34a-5p suppresses colorectal cancer metastasis and predicts recurrence in patients with stage II/III colorectal cancer. Oncogene. 2015;34(31):4142–52.PubMedCrossRef Gao J, Li N, Dong Y, Li S, Xu L, Li X, Li Y, Li Z, Ng SS, Sung JJ, et al. miR-34a-5p suppresses colorectal cancer metastasis and predicts recurrence in patients with stage II/III colorectal cancer. Oncogene. 2015;34(31):4142–52.PubMedCrossRef
40.
go back to reference Cho WC. MicroRNAs: potential biomarkers for cancer diagnosis, prognosis and targets for therapy. Int J Biochem Cell Biol. 2010;42(8):1273–81.PubMedCrossRef Cho WC. MicroRNAs: potential biomarkers for cancer diagnosis, prognosis and targets for therapy. Int J Biochem Cell Biol. 2010;42(8):1273–81.PubMedCrossRef
41.
go back to reference Hayes J, Peruzzi PP, Lawler S. MicroRNAs in cancer: biomarkers, functions and therapy. Trends Mol Med. 2014;20(8):460–9.PubMedCrossRef Hayes J, Peruzzi PP, Lawler S. MicroRNAs in cancer: biomarkers, functions and therapy. Trends Mol Med. 2014;20(8):460–9.PubMedCrossRef
42.
go back to reference Sun F, Fu H, Liu Q, Tie Y, Zhu J, Xing R, Sun Z, Zheng X. Downregulation of CCND1 and CDK6 by miR-34a induces cell cycle arrest. FEBS Lett. 2008;582(10):1564–8.PubMedCrossRef Sun F, Fu H, Liu Q, Tie Y, Zhu J, Xing R, Sun Z, Zheng X. Downregulation of CCND1 and CDK6 by miR-34a induces cell cycle arrest. FEBS Lett. 2008;582(10):1564–8.PubMedCrossRef
43.
go back to reference Chandrasekaran KS, Sathyanarayanan A, Karunagaran D. Downregulation of HMGB1 by miR-34a is sufficient to suppress proliferation, migration and invasion of human cervical and colorectal cancer cells. Tumour Biol. 2016;37(10):13155–66.PubMedCrossRef Chandrasekaran KS, Sathyanarayanan A, Karunagaran D. Downregulation of HMGB1 by miR-34a is sufficient to suppress proliferation, migration and invasion of human cervical and colorectal cancer cells. Tumour Biol. 2016;37(10):13155–66.PubMedCrossRef
44.
go back to reference Kong J, Wang W. A systemic review on the regulatory roles of miR-34a in gastrointestinal Cancer. OncoTargets Ther. 2020;13:2855–72.CrossRef Kong J, Wang W. A systemic review on the regulatory roles of miR-34a in gastrointestinal Cancer. OncoTargets Ther. 2020;13:2855–72.CrossRef
45.
go back to reference Asadi M, Shanehbandi D, Mohammadpour H, Hashemzadeh S, Sepehri B. Expression level of miR-34a in tumor tissue from patients with esophageal squamous cell carcinoma. J Gastrointest Cancer. 2019;50(2):304–7.PubMedCrossRef Asadi M, Shanehbandi D, Mohammadpour H, Hashemzadeh S, Sepehri B. Expression level of miR-34a in tumor tissue from patients with esophageal squamous cell carcinoma. J Gastrointest Cancer. 2019;50(2):304–7.PubMedCrossRef
46.
go back to reference Zhou Y, Ding BZ, Lin YP, Wang HB. MiR-34a, as a suppressor, enhance the susceptibility of gastric cancer cell to luteolin by directly targeting HK1. Gene. 2018;644:56–65.PubMedCrossRef Zhou Y, Ding BZ, Lin YP, Wang HB. MiR-34a, as a suppressor, enhance the susceptibility of gastric cancer cell to luteolin by directly targeting HK1. Gene. 2018;644:56–65.PubMedCrossRef
47.
go back to reference Lu G, Sun Y, An S, Xin S, Ren X, Zhang D, Wu P, Liao W, Ding Y, Liang L. MicroRNA-34a targets FMNL2 and E2F5 and suppresses the progression of colorectal cancer. Exp Mol Pathol. 2015;99(1):173–9.PubMedCrossRef Lu G, Sun Y, An S, Xin S, Ren X, Zhang D, Wu P, Liao W, Ding Y, Liang L. MicroRNA-34a targets FMNL2 and E2F5 and suppresses the progression of colorectal cancer. Exp Mol Pathol. 2015;99(1):173–9.PubMedCrossRef
48.
go back to reference Tazawa H, Tsuchiya N, Izumiya M, Nakagama H. Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc Natl Acad Sci U S A. 2007;104(39):15472–7.PubMedPubMedCentralCrossRef Tazawa H, Tsuchiya N, Izumiya M, Nakagama H. Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc Natl Acad Sci U S A. 2007;104(39):15472–7.PubMedPubMedCentralCrossRef
49.
go back to reference Jiang L. Hermeking H: miR-34a and miR-34b/c suppress intestinal tumorigenesis. Cancer Res. 2017;77(10):2746–58.PubMedCrossRef Jiang L. Hermeking H: miR-34a and miR-34b/c suppress intestinal tumorigenesis. Cancer Res. 2017;77(10):2746–58.PubMedCrossRef
50.
go back to reference Hayes DF, Isaacs C, Stearns V. Prognostic factors in breast cancer: current and new predictors of metastasis. J Mammary Gland Biol Neoplasia. 2001;6(4):375–92.PubMedCrossRef Hayes DF, Isaacs C, Stearns V. Prognostic factors in breast cancer: current and new predictors of metastasis. J Mammary Gland Biol Neoplasia. 2001;6(4):375–92.PubMedCrossRef
51.
go back to reference Tang Y, Tang Y, Cheng YS. miR-34a inhibits pancreatic cancer progression through Snail1-mediated epithelial-mesenchymal transition and the notch signaling pathway. Sci Rep. 2017;7:38232.PubMedPubMedCentralCrossRef Tang Y, Tang Y, Cheng YS. miR-34a inhibits pancreatic cancer progression through Snail1-mediated epithelial-mesenchymal transition and the notch signaling pathway. Sci Rep. 2017;7:38232.PubMedPubMedCentralCrossRef
52.
go back to reference Nalls D, Tang SN, Rodova M, Srivastava RK, Shankar S. Targeting epigenetic regulation of miR-34a for treatment of pancreatic cancer by inhibition of pancreatic cancer stem cells. PLoS One. 2011;6(8):e24099.PubMedPubMedCentralCrossRef Nalls D, Tang SN, Rodova M, Srivastava RK, Shankar S. Targeting epigenetic regulation of miR-34a for treatment of pancreatic cancer by inhibition of pancreatic cancer stem cells. PLoS One. 2011;6(8):e24099.PubMedPubMedCentralCrossRef
Metadata
Title
Prognostic value of low microRNA-34a expression in human gastrointestinal cancer: a systematic review and meta-analysis
Authors
Yan-Ling Chen
Xiao-Lin Liu
Ling Li
Publication date
01-12-2021

Other articles of this Issue 1/2021

BMC Cancer 1/2021 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine