Review

Clinicopathological significance of Bmi-1 overexpression in esophageal cancer: a meta-analysis

Department of Pathology & Key Laboratory for Xinjiang Endemic & Ethnic Diseases, Shihezi University School of Medicine, Xinjiang 832002, PR China

^‡Co-first authors.

Search for more papers by this author

Kai Liu^‡

Department of Pathology & Key Laboratory for Xinjiang Endemic & Ethnic Diseases, Shihezi University School of Medicine, Xinjiang 832002, PR China

^‡Co-first authors.

Search for more papers by this author

Xianli Jiang^‡

Department of Pathology & Key Laboratory for Xinjiang Endemic & Ethnic Diseases, Shihezi University School of Medicine, Xinjiang 832002, PR China

^‡Co-first authors.

Search for more papers by this author

Xueli Wang

Department of Pathology & Key Laboratory for Xinjiang Endemic & Ethnic Diseases, Shihezi University School of Medicine, Xinjiang 832002, PR China

Search for more papers by this author

Yunzhao Chen

Department of Pathology & Key Laboratory for Xinjiang Endemic & Ethnic Diseases, Shihezi University School of Medicine, Xinjiang 832002, PR China

Search for more papers by this author

Xiaobin Cui

Department of Pathology & Key Laboratory for Xinjiang Endemic & Ethnic Diseases, Shihezi University School of Medicine, Xinjiang 832002, PR China

Search for more papers by this author

Lijuan Pang

Department of Pathology & Key Laboratory for Xinjiang Endemic & Ethnic Diseases, Shihezi University School of Medicine, Xinjiang 832002, PR China

Search for more papers by this author

Shugang Li

Department of Preventive Medicine, Shihezi University School of Medicine, Xinjiang 832002, PR China

Search for more papers by this author

Chunxia Liu

Department of Pathology & Key Laboratory for Xinjiang Endemic & Ethnic Diseases, Shihezi University School of Medicine, Xinjiang 832002, PR China

Search for more papers by this author

Hong Zou

Department of Pathology & Key Laboratory for Xinjiang Endemic & Ethnic Diseases, Shihezi University School of Medicine, Xinjiang 832002, PR China

Search for more papers by this author

Lan Yang

Department of Pathology & Key Laboratory for Xinjiang Endemic & Ethnic Diseases, Shihezi University School of Medicine, Xinjiang 832002, PR China

Search for more papers by this author

Jin Zhao

Department of Pathology & Key Laboratory for Xinjiang Endemic & Ethnic Diseases, Shihezi University School of Medicine, Xinjiang 832002, PR China

Search for more papers by this author

Yan Qi

Department of Pathology & Key Laboratory for Xinjiang Endemic & Ethnic Diseases, Shihezi University School of Medicine, Xinjiang 832002, PR China

Search for more papers by this author

Jian Ming Hu

*Author for correspondence:

E-mail Address: jianming.120@163.com

Department of Pathology & Key Laboratory for Xinjiang Endemic & Ethnic Diseases, Shihezi University School of Medicine, Xinjiang 832002, PR China

Search for more papers by this author

Feng Li

**Author for correspondence:

E-mail Address: lifeng7855@126.com

Department of Pathology & Key Laboratory for Xinjiang Endemic & Ethnic Diseases, Shihezi University School of Medicine, Xinjiang 832002, PR China

Department of Pathology, Beijing ChaoYang Hospital, Capital Medical University, Beijing 100020, PR China

Search for more papers by this author

Published Online:14 Dec 2017https://doi.org/10.2217/bmm-2017-0092

View article

Abstract

Aim: The clinicopathological effects of Bmi-1 expression in esophageal cancer remain widely disputed. Our aim was to clarify this relationship. Methods: Available studies were retrieved from diverse databases. Review Manager 5.3 and Stata 12.0 software were used to identify correlations between Bmi-1 expression and the clinicopathological features of esophageal cancer. Results: From 16 studies, 1523 esophageal cancer patients were analyzed. Meta-analysis demonstrated that Bmi-1 overexpression was associated with differentiation (p = 0.03), tumor/node/metastasis stage (p = 0.02), depth of invasion (p = 0.0006) and lymph node metastasis (p = 0.008). Conclusion: The expression of Bmi-1 is associated with the progression and invasion of esophageal cancer.

Keywords:

Papers of special note have been highlighted as: • of interest; •• of considerable interest

References

1 Ferlay J, Soerjomataram I, Dikshit R et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer. 136(5), E359–E386 (2015).Crossref, Medline, CAS, Google Scholar
2 Hiyama T, Yoshihara M, Tanaka S, Chayama K. Genetic polymorphisms and esophageal cancer risk. Int. J. Cancer 121(8), 1643–1658 (2007).Crossref, Medline, CAS, Google Scholar
3 Meves V, Behrens A, Pohl J. Diagnostics and early diagnosis of esophageal cancer. Viszeralmedizin 31(5), 315–318 (2015).Medline, Google Scholar
4 Tomochika S, Iizuka N, Watanabe Y et al. Increased serum cell-free DNA levels in relation to inflammation are predictive of distant metastasis of esophageal squamous cell carcinoma. Exp. Ther. Med. 1(1), 89–92 (2010).Crossref, Medline, Google Scholar
5 Jain S, Dhingra S. Pathology of esophageal cancer and Barrett's esophagus. Ann. Cardiothorac. Surg. 6(2), 99–109 (2017).Crossref, Medline, Google Scholar
6 Alkema MJ, Wiegant J, Raap AK, Berns A, Van Lohuizen M. Characterization and chromosomal localization of the human proto-oncogene BMI-1. Hum. Mol. Genet. 2(10), 1597–1603 (1993).Crossref, Medline, CAS, Google Scholar
7 Jacobs JJ, Scheijen B, Voncken JW, Kieboom K, Berns A, Van Lohuizen M. Bmi-1 collaborates with c-Myc in tumorigenesis by inhibiting c-Myc-induced apoptosis via INK4a/ARF. Genes Dev. 13(20), 2678–2690 (1999).Crossref, Medline, CAS, Google Scholar
8 Li Z, Cao R, Wang M, Myers MP, Zhang Y, Xu RM. Structure of a Bmi-1-Ring1B polycomb group ubiquitin ligase complex. J. Biol. Chem. 281(29), 20643–20649 (2006).Crossref, Medline, CAS, Google Scholar
9 Jacobs JJ, Kieboom K, Marino S, Depinho RA, Van Lohuizen M. The oncogene and polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 397(6715), 164–168 (1999).Crossref, Medline, CAS, Google Scholar
10 Park IK, Qian D, Kiel M et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 423(6937), 302–305 (2003).Crossref, Medline, CAS, Google Scholar
11 Molofsky AV, Pardal R, Iwashita T, Park IK, Clarke MF, Morrison SJ. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 425(6961), 962–967 (2003).Crossref, Medline, CAS, Google Scholar
12 Wang JF, Liu Y, Liu WJ, He SY. Expression of Bmi-1 gene in esophageal carcinoma cell EC9706 and its effect on cell cycle, apoptosis and migration. Chin. J. Cancer 29(7), 689–696 (2010). •• Discusses the crucial role of Bmi-1 in cancer progression, which supports our findings greatly.Crossref, Medline, CAS, Google Scholar
13 He XT, Cao XF, Ji L et al. Association between Bmi1 and clinicopathological status of esophageal squamous cell carcinoma. World J. Gastroenterol. 15(19), 2389–2394 (2009).Crossref, Medline, CAS, Google Scholar
14 Choy B, Bandla S, Xia Y et al. Clinicopathologic characteristics of high expression of Bmi-1 in esophageal adenocarcinoma and squamous cell carcinoma. BMC Gastroenterol. 12, 146 (2012).Crossref, Medline, Google Scholar
15 Liu WL, Guo XZ, Zhang LJ et al. Prognostic relevance of Bmi-1 expression and autoantibodies in esophageal squamous cell carcinoma. BMC Cancer 10, 467 (2010).Crossref, Medline, Google Scholar
16 Ha SY, Kim SH. Co-expression of Bmi1 and EZH2 as an independent poor prognostic factor in esophageal squamous cell carcinoma. Pathol. Res. Pract. 208(8), 462–469 (2012). •• This outcome of this study was that elevated Bmi-1 expression correlated negatively with the aggressive clinicopathological parameters of esophageal cancer. This result conflicted with several other published findings, rendering the relationship between the expression Bmi-1 expression and the esophageal cancer clinicopathological features is still inconclusive. This formed the basis of our study.Crossref, Medline, CAS, Google Scholar
17 Peters JL, Sutton AJ, Jones DR, Abrams KR, Rushton L. Comparison of two methods to detect publication bias in meta-analysis. JAMA 295(6), 676–680 (2006).Crossref, Medline, CAS, Google Scholar
18 Zintzaras E, Ioannidis JP. HEGESMA: genome search meta-analysis and heterogeneity testing. Bioinformatics 21(18), 3672–3673 (2005).Crossref, Medline, CAS, Google Scholar
19 Yamada A, Fujii S, Daiko H, Nishimura M, Chiba T, Ochiai A. Aberrant expression of EZH2 is associated with a poor outcome and P53 alteration in squamous cell carcinoma of the esophagus. Int. J. Oncol. 38(2), 345–353 (2011).Medline, CAS, Google Scholar
20 Zhang Y, Zhang YL, Chen HM et al. Expression of Bmi-1 and PAI-1 in esophageal squamous cell carcinoma. World J. Gastroenterol. 20(18), 5533–5539 (2014).Crossref, Medline, Google Scholar
21 Hwang CC, Nieh S, Lai CH et al. A retrospective review of the prognostic value of ALDH-1, Bmi-1 and Nanog stem cell markers in esophageal squamous cell carcinoma. PLoS ONE 9(8), e105676 (2014).Crossref, Medline, Google Scholar
22 Zhou GYW, Mo C. Expression and correlation analysis of Bmi-1 and HTERT in esophageal squamous cell carcinoma. China Clin. Res. 27(08), 904–906 (2014).CAS, Google Scholar
23 Zhang XGY, Xing R, Guo X, Wang X. The expression and the related clinical significance of SALL4, Bmi-1 and β-catenin in esophageal squamous cell carcinoma. Acad. J. Second Mil. Med. Univ. 35(04), 406–412 (2014).Crossref, CAS, Google Scholar
24 Wu JZX, Zhu Y. Expression and clinical significance of Bmi-1 protein in esophageal squamous cell carcinoma. Chin. J. Clin. Oncol. (13), 911–913 (2012).Google Scholar
25 Sun YTX, Yang X, Du X et al. The clinical significance of bmi-1 expresssion in esophageal squamous cell carcinoma tissues. PLA Medical College (1), 88–90 (2013).Google Scholar
26 Liu JKC, Wang Y. Clinical significance and expression of Bmi1 and EZH2 in esophageal squamous cell carcinoma. Ningxia Medical University. (3), 305–307 (2014).Google Scholar
27 Li JYX, Ding B, Gong R, Ni Z, Wu F. Bmi-1 and p27 expression and their correlation in esophageal squamous cell carcinoma. Chin. J. Clin. Pharmacol. Ther. (12), 1388–1391 + 1396 (2015).Google Scholar
28 Jiang QCY, Liu X, Li Y. Bmi-1 expression and invasion and metastasis in esophageal carcinoma. Medical Forum (10), 29–31 (2010).Google Scholar
29 Fu ZZL, Li Y, Zhang T, Zhang Y, Wen H. Clinicopathological significance of Bmi-1 and S100A4 expression in esophageal squamous cell carcinoma. World Chin. J. Digestol. (13), 1344–1349 (2010).Crossref, Google Scholar
30 Fei ZCS, Chen L. Expression and significance of Bmi-1 and CD133 in esophageal squamous cell carcinoma. Modern Practical Medicine (3), 337–339 (2011).Google Scholar
31 Van Lohuizen M, Verbeek S, Scheijen B, Wientjens E, Van Der Gulden H, Berns A. Identification of cooperating oncogenes in E mu-myc transgenic mice by provirus tagging. Cell 65(5), 737–752 (1991).Crossref, Medline, CAS, Google Scholar
32 Song W, Tao K, Li H et al. Bmi-1 is related to proliferation, survival and poor prognosis in pancreatic cancer. Cancer Sci. 101(7), 1754–1760 (2010).Crossref, Medline, CAS, Google Scholar
33 Yang GF, He WP, Cai MY et al. Intensive expression of Bmi-1 is a new independent predictor of poor outcome in patients with ovarian carcinoma. BMC Cancer 10, 133 (2010). •• Highlights the involvement of Bmi-1 in cancer; specifically, in cellular proliferation and cell invasion, resulting in poor prognosis.Crossref, Medline, CAS, Google Scholar
34 Gao F, Huang W, Zhang Y et al. Hes1 promotes cell proliferation and migration by activating Bmi-1 and PTEN/Akt/GSK3beta pathway in human colon cancer. Oncotarget 6(36), 38667–38680 (2015). • Suggests an important role for Bmi-1 in the regulation of cancer-promoting signaling pathways.Crossref, Medline, Google Scholar
35 Ma J, Lanza DG, Guest I et al. Characterization of mammary cancer stem cells in the MMTV-PyMT mouse model. Tumour Biol. 33(6), 1983–1996 (2012).Crossref, Medline, CAS, Google Scholar
36 Liu W, Feng JQ, Shen XM, Wang HY, Liu Y, Zhou ZT. Two stem cell markers, ATP-binding cassette, G2 subfamily (ABCG2) and BMI-1, predict the transformation of oral leukoplakia to cancer: a long-term follow-up study. Cancer 118(6), 1693–1700 (2012). • Describes the involvement of Bmi-1 in the regulation of tumor initiation and differentiation in cancer stem cells.Crossref, Medline, CAS, Google Scholar
37 Wang MC, Jiao M, Wu T et al. Polycomb complex protein BMI-1 promotes invasion and metastasis of pancreatic cancer stem cells by activating PI3K/AKT signaling, an ex vivo, in vitro, and in vivo study. Oncotarget 7(8), 9586–9599 (2016).Crossref, Medline, Google Scholar
38 Tong YQ, Liu B, Zheng HY et al. Overexpression of BMI-1 is associated with poor prognosis in cervical cancer. Asia Pac. J. Clin. Oncol. 8(4), e55–e62 (2012).Crossref, Medline, Google Scholar
39 Wang Y, Zhe H, Ding Z, Gao P, Zhang N, Li G. Cancer stem cell marker Bmi-1 expression is associated with basal-like phenotype and poor survival in breast cancer. World J. Surg. 36(5), 1189–1194 (2012).Crossref, Medline, Google Scholar
40 Hu J, Liu YL, Piao SL, Yang DD, Yang YM, Cai L. Expression patterns of USP22 and potential targets BMI-1, PTEN, p-AKT in non-small-cell lung cancer. Lung Cancer 77(3), 593–599 (2012).Crossref, Medline, Google Scholar
41 Li DW, Tang HM, Fan JW et al. Expression level of Bmi-1 oncoprotein is associated with progression and prognosis in colon cancer. J. Cancer Res. Clin. Oncol. 136(7), 997–1006 (2010).Crossref, Medline, CAS, Google Scholar
42 Liu JH, Song LB, Zhang X et al. Bmi-1 expression predicts prognosis for patients with gastric carcinoma. J. Surg. Oncol. 97(3), 267–272 (2008).Crossref, Medline, CAS, Google Scholar

Vol. 12, No. 1

Metrics

Downloaded 113 times

History

Received 16 March 2017

Accepted 13 September 2017

Published online 14 December 2017

Published in print January 2018

Information

Keywords

Availability of data and materials

Data were obtained from literature publications.

Authors’ contributions

J Liu, K Liu and X Jiang equally contributed to the writing, data collection and delivery of the manuscript. S Li and J Hu helped to design the statistical approaches. J Hu and F Li contributed to the design of tables and figures, and helped to modify the syntactic. All the authors contributed to the preparation of the manuscript and approved the final manuscript.

Financial & competing interest disclosure

This research was supported by grants from the National Natural Science Foundation of China ‘No. 81460363’ and ‘No. 81560399’. The authors have no other relevant affiliations or financial involvement with any organization or entity, with a financial interest in, or financial conflict with, the subject matter or materials discussed in the manuscript, apart from those disclosed.

Professional language editorial assistance was provided for the preparation of this manuscript.

Ethical conduct of research

The authors state that they have obtained appropriate institutional review board approval or have followed the principles outlined in the Declaration of Helsinki for all human or animal experimental investigations. In addition, for investigations involving human subjects, informed consent has been obtained from the participants involved.

PDF download