Skip to main content

Advertisement

SpringerLink
Log in

MiR-613: a novel diagnostic and prognostic biomarker for patients with esophageal squamous cell carcinoma

  • Original Article
  • Published:
Tumor Biology

Abstract

MicroRNA-613 (miR-613) plays important roles in tumorigenesis and cancer progression. We aimed to evaluate its expression level and potential for diagnosis and prognosis in esophageal squamous cell cancer (ESCC). We examined miR-613 expression in 60 pairs of ESCC cancerous and matched paracancerous tissues, serum samples from 75 ESCC patients and 75 healthy volunteers, and 105 formalin-fixed paraffin-embedded (FFPE) tissue samples using quantitative reverse transcription polymerase chain reaction. Receiver-operating characteristic (ROC) curve analysis, Kaplan-Meier method, and Cox regression were applied to analyze its diagnostic and prognostic value. MiR-613 was significantly decreased in ESCC tissue compared with paracancerous tissue (P < 0.001). Moreover, the expression level of miR-613 was significantly reduced with increased T stage of ESCC. Statistically significant difference between ESCC patients and healthy controls in expression level of miR-613 (0.89 ± 0.73 vs. 1.71 ± 1.03, P < 0.001) was found. The area under the ROC curve (AUC) based on serum miR-613 was 0.767 ± 0.040. We also performed analysis on early-stage patients and revealed that the AUC value was 0.728 ± 0.052 (P < 0.001). The Kaplan-Meier curve revealed that the downregulation of miR-613 was related to worse overall survival (OS) and progression-free survival (PFS) of ESCC patients (P = 0.018 and P = 0.035, respectively). Furthermore, the multivariate analysis identified miR-613 to be an independent prognostic factor for OS and PFS (P = 0.031 and P = 0.006, respectively) In conclusion, miR-613 is significantly reduced in cancerous tissue and serum samples of ESCC patients. It can serve as an ideal indicator for the diagnosis and prognosis of ESCC.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Napier KJ, Scheerer M, Misra S. Esophageal cancer: a review of epidemiology, pathogenesis, staging workup and treatment modalities. World J Gastrointest Oncol. 2014;6(5):112–20. doi:10.4251/wjgo.v6.i5.112.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Pennathur A, Gibson MK, Jobe BA, Luketich JD. Oesophageal carcinoma. Lancet. 2013;381(9864):400–12. doi:10.1016/S0140-6736(12)60643-6.

    Article  PubMed  Google Scholar 

  3. Feng JF, Huang Y, Lu WS, Chen QX. Preoperative platelet count in esophageal squamous cell carcinoma: is it a prognostic factor? Langenbecks Arch Surg. 2013;398(8):1115–22. doi:10.1007/s00423-013-1111-4.

    Article  PubMed  Google Scholar 

  4. Feng JF, Huang Y, Zhao Q. Tumor length in elderly patients with esophageal squamous cell carcinoma: is it a prognostic factor? Ups J Med Sci. 2013;118(3):145–52. doi:10.3109/03009734.2013.792887.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Yu G, Chen G, Huang B, Shao W, Zeng G. Effect of early enteral nutrition on postoperative nutritional status and immune function in elderly patients with esophageal cancer or cardiac cancer. Chin J Cancer Res. 2013;25(3):299–305. doi:10.3978/j.issn.1000-9604.2013.06.01.

    PubMed  PubMed Central  Google Scholar 

  6. Ren P, Yu ZT, Xiu L, Wang M, Liu HM. Elevated serum levels of human relaxin-2 in patients with esophageal squamous cell carcinoma. World J Gastroenterol. 2013;19(15):2412–8. doi:10.3748/wjg.v19.i15.2412.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Wang Q, Ma C, Kemmner W. Wdr66 is a novel marker for risk stratification and involved in epithelial-mesenchymal transition of esophageal squamous cell carcinoma. BMC Cancer. 2013;13:137. doi:10.1186/1471-2407-13-137.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Ren P, Zhang JG, Xiu L, Yu ZT. Clinical significance of phospholipase A2 group IIA (PLA2G2A) expression in primary resected esophageal squamous cell carcinoma. Eur Rev Med Pharmacol Sci. 2013;17(6):752–7.

    CAS  PubMed  Google Scholar 

  9. Reddy KB. MicroRNA (miRNA) in cancer. Cancer Cell Int. 2015;15:38. doi:10.1186/s12935-015-0185-1.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Garzon R, Calin GA, Croce CM. MicroRNAs in cancer. Annu Rev Med. 2009;60:167–79. doi:10.1146/annurev.med.59.053006.104707.

    Article  CAS  PubMed  Google Scholar 

  11. Komatsu S, Ichikawa D, Hirajima S, Kawaguchi T, Miyamae M, Okajima W, et al. Plasma microRNA profiles: identification of miR-25 as a novel diagnostic and monitoring biomarker in oesophageal squamous cell carcinoma. Br J Cancer. 2014;111(8):1614–24. doi:10.1038/bjc.2014.451.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Wu C, Li M, Hu C, Duan H. Clinical significance of serum miR-223, miR-25 and miR-375 in patients with esophageal squamous cell carcinoma. Mol Biol Rep. 2014;41(3):1257–66. doi:10.1007/s11033-013-2970-z.

    Article  CAS  PubMed  Google Scholar 

  13. Tanaka K, Miyata H, Yamasaki M, Sugimura K, Takahashi T, Kurokawa Y, 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:S607–15. doi:10.1245/s10434-013-3093-4.

    Article  PubMed  Google Scholar 

  14. Dong W, Li B, Wang Z, Zhang Z, Wang J. Clinical significance of microRNA-24 expression in esophageal squamous cell carcinoma. Neoplasma. 2015;62(2):250–8. doi:10.4149/neo_2015_030.

    Article  CAS  PubMed  Google Scholar 

  15. Yang Z, Yuan Z, Fan Y, Deng X, Zheng Q. Integrated analyses of microRNA and mRNA expression profiles in aggressive papillary thyroid carcinoma. Mol Med Rep. 2013;8(5):1353–8. doi:10.3892/mmr.2013.1699.

    CAS  PubMed  Google Scholar 

  16. Shah AA, Leidinger P, Backes C, Keller A, Karpinski P, Sasiadek MM, et al. A set of specific miRNAs is connected with murine and human gastric cancer. Genes Chromosomes Cancer. 2013;52(3):237–49. doi:10.1002/gcc.22024.

    Article  CAS  PubMed  Google Scholar 

  17. Cho WC. OncomiRs: the discovery and progress of microRNAs in cancers. Mol Cancer. 2007;6:60. doi:10.1186/1476-4598-6-60.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Meng H, Wang K, Chen X, Guan X, Hu L, Xiong G, et al. MicroRNA-330-3p functions as an oncogene in human esophageal cancer by targeting programmed cell death 4. Am J Cancer Res. 2015;5(3):1062–75.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Ide S, Toiyama Y, Shimura T, Kawamura M, Yasuda H, Saigusa S, et al. MicroRNA-503 promotes tumor progression and acts as a novel biomarker for prognosis in oesophageal cancer. Anticancer Res. 2015;35(3):1447–51.

    PubMed  Google Scholar 

  20. Jiang L, Wang Y, Rong Y, Xu L, Chu Y, Zhang Y, et al. miR-1179 promotes cell invasion through SLIT2/ROBO1 axis in esophageal squamous cell carcinoma. Int J Clin Exp Pathol. 2015;8(1):319–27.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Li M, He XY, Zhang ZM, Li S, Ren LH, Cao RS, et al. MicroRNA-1290 promotes esophageal squamous cell carcinoma cell proliferation and metastasis. World J Gastroenterol. 2015;21(11):3245–55. doi:10.3748/wjg.v21.i11.3245.

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Qi Y, Li X, Zhao S. miR-29b inhibits the progression of esophageal squamous cell carcinoma by targeting MMP-2. Neoplasma. 2015;62(3):384–90. doi:10.4149/neo_2015_046.

    Article  CAS  PubMed  Google Scholar 

  23. Nie J, Ge X, Geng Y, Cao H, Zhu W, Jiao Y, et al. miR-34a inhibits the migration and invasion of esophageal squamous cell carcinoma by targeting Yin Yang-1. Oncol Rep. 2015. doi:10.3892/or.2015.3962.

    Google Scholar 

  24. Yang JS, Li BJ, Lu HW, Chen Y, Lu C, Zhu RX, et al. Serum miR-152, miR-148a, miR-148b, and miR-21 as novel biomarkers in non-small cell lung cancer screening. Tumour Biol. 2015;36(4):3035–42. doi:10.1007/s13277-014-2938-1.

    Article  CAS  PubMed  Google Scholar 

  25. Chen J, Wang W, Zhang Y, Chen Y, Hu T. Predicting distant metastasis and chemoresistance using plasma miRNAs. Med Oncol. 2014;31(1):799. doi:10.1007/s12032-013-0799-x.

    Article  PubMed  Google Scholar 

  26. Ouyang M, Li Y, Ye S, Ma J, Lu L, Lv W, et al. MicroRNA profiling implies new markers of chemoresistance of triple-negative breast cancer. PLoS One. 2014;9(5):e96228. doi:10.1371/journal.pone.0096228.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Mar-Aguilar F, Mendoza-Ramirez JA, Malagon-Santiago I, Espino-Silva PK, Santuario-Facio SK, Ruiz-Flores P, et al. Serum circulating microRNA profiling for identification of potential breast cancer biomarkers. Dis Markers. 2013;34(3):163–9. doi:10.3233/DMA-120957.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hezova R, Kovarikova A, Srovnal J, Zemanova M, Harustiak T, Ehrmann J, et al. Diagnostic and prognostic potential of miR-21, miR-29c, miR-148 and miR-203 in adenocarcinoma and squamous cell carcinoma of esophagus. Diagn Pathol. 2015;10(1):42. doi:10.1186/s13000-015-0280-6.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Sun N, Ye L, Chang T, Li X, Li X. microRNA-195-Cdc42 axis acts as a prognostic factor of esophageal squamous cell carcinoma. Int J Clin Exp Pathol. 2014;7(10):6871–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Wang TY, Liu SG, Zhao BS, Qi B, Qin XG, Yao WJ. Implications of microRNA-197 downregulated expression in esophageal cancer with poor prognosis. Genet Mol Res. 2014;13(3):5574–81. doi:10.4238/2014.July.25.12.

    Article  CAS  PubMed  Google Scholar 

  31. Zhang BJ, Gong HY, Zheng F, Liu DJ, Liu HX. Up-regulation of miR-335 predicts a favorable prognosis in esophageal squamous cell carcinoma. Int J Clin Exp Pathol. 2014;7(9):6213–8.

    PubMed  PubMed Central  Google Scholar 

  32. Qi B, Liu SG, Qin XG, Yao WJ, Lu JG, Guo L, et al. Overregulation of microRNA-212 in the poor prognosis of esophageal cancer patients. Genet Mol Res. 2014;13(3):7800–7. doi:10.4238/2014.September.26.18.

    Article  CAS  PubMed  Google Scholar 

  33. Wang C, Guan S, Chen X, Liu B, Liu F, Han L, et al. Clinical potential of miR-3651 as a novel prognostic biomarker for esophageal squamous cell cancer. Biochem Biophys Res Commun. 2015;465(1):30–4. doi:10.1016/j.bbrc.2015.07.109.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Science and Technology Development Planning Project of Shandong Province (2014GSF118058).

Author information

Authors and Affiliations

  1. Department of Radiation Oncology, Qilu Hospital of Shandong University, Jinan, Shandong, 250012, China

    Shanghui Guan, Cong Wang, Xuan Chen, Bowen Liu, Bingxu Tan, Lihui Han, Lu Wang, Xiaochen Huang, Jiangfeng Wang, Bin Yao, Jialei Shi, Pengxiang Chen, Effat Un Nesa, Qingxu Song & Yufeng Cheng

  2. Department of Image, Shandong Medical College, Jinan, Shandong, 250002, China

    Fang Liu

  3. Department of Clinical Laboratory, Qilu Hospital of Shandong University, Jinan, Shandong, 250012, China

    Ding Wang

Authors
  1. Shanghui Guan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xuan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bowen Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bingxu Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ding Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Lihui Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Lu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Xiaochen Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jiangfeng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Bin Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Jialei Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Pengxiang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Effat Un Nesa
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Qingxu Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Yufeng Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yufeng Cheng.

Ethics declarations

Conflicts of interest

None

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guan, S., Wang, C., Chen, X. et al. MiR-613: a novel diagnostic and prognostic biomarker for patients with esophageal squamous cell carcinoma. Tumor Biol. 37, 4383–4391 (2016). https://doi.org/10.1007/s13277-015-4271-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13277-015-4271-8

Keywords

Search

Navigation