BMI‑1, a promising therapeutic target for human cancer (Review)
- Authors:
- Min‑Cong Wang
- Chun‑Li Li
- Jie Cui
- Min Jiao
- Tao Wu
- Li Jing
- Ke‑Jun Nan
-
Affiliations: Department of Oncology, The First Affiliated Hospital, College of Medicine of Xi'an Jiaotong University, Xi'an, Shaanxi 710061, P.R. China - Published online on: June 11, 2015 https://doi.org/10.3892/ol.2015.3361
- Pages: 583-588
This article is mentioned in:
Abstract
Sayed SI, Dwivedi RC, Katna R, et al: Implications of understanding cancer stem cell (CSC) biology in head and neck squamous cell cancer. Oral Oncol. 47:237–243. 2011. View Article : Google Scholar : PubMed/NCBI | |
Sinha N, Mukhopadhyay S, Das DN, Panda PK and Bhutia SK: Relevance of cancer initiating/stem cells in carcinogenesis and therapy resistance in oral cancer. Oral Oncol. 49:854–862. 2013. View Article : Google Scholar : PubMed/NCBI | |
Biehs B, Hu JK, Strauli NB, et al: BMI1 represses Ink4a/Arf and Hox genes to regulate stem cells in the rodent incisor. Nat Cell Biol. 15:846–852. 2013. View Article : Google Scholar : PubMed/NCBI | |
Lukacs RU, Memarzadeh S, Wu H and Witte ON: Bmi-1 is a crucial regulator of prostate stem cell self-renewal and malignant transformation. Cell Stem Cell. 7:682–693. 2010. View Article : Google Scholar : PubMed/NCBI | |
Abdouh M, Facchino S, Chatoo W, Balasingam V, Ferreira J and Bernier G: BMI1 sustains human glioblastoma multiforme stem cell renewal. J Neurosci. 29:8884–8896. 2009. View Article : Google Scholar : PubMed/NCBI | |
Gavrilescu MM, Todosi AM, Aniţei MG, Filip B and Scripcariu V: Expression of bmi-1 protein in cervical, breast and ovarian cancer. Rev Med Chir Soc Med Nat Iasi. 116:1112–1117. 2012.PubMed/NCBI | |
Alkema MJ, Wiegant J, Raap AK, Berns A and van Lohuizen M: Characterization and chromosomal localization of the human proto-oncogene BMI-1. Hum Mol Genet. 2:1597–1603. 1993. View Article : Google Scholar : PubMed/NCBI | |
Yang DD, Cui BB, Sun LY, et al: The co-expression of USP22 and BMI-1 may promote cancer progression and predict therapy failure in gastric carcinoma. Cell Biochem Biophys. 61:703–710. 2011. View Article : Google Scholar : PubMed/NCBI | |
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. 10:1332010. View Article : Google Scholar : PubMed/NCBI | |
Guo BH, Feng Y, Zhang R, et al: Bmi-1 promotes invasion and metastasis and its elevated expression is correlated with an advanced stage of breast cancer. Mol Cancer. 10:102011. View Article : Google Scholar : PubMed/NCBI | |
Häyry V, Mäkinen LK, Atula T, et al: Bmi-1 expression predicts prognosis in squamous cell carcinoma of the tongue. Br J Cancer. 102:892–897. 2010. View Article : Google Scholar : PubMed/NCBI | |
Song LB, Zeng MS, Liao WT, et al: Bmi-1 is a novel molecular marker of nasopharyngeal carcinoma progression and immortalizes primary human nasopharyngeal epithelial cells. Cancer Res. 66:6225–6232. 2006. View Article : Google Scholar : PubMed/NCBI | |
Chang Z, Li Z, Wang X, et al: Deciphering the mechanisms of tumorigenesis in human pancreatic ductal epithelial cells. Clin Cancer Res. 19:549–559. 2013. View Article : Google Scholar : PubMed/NCBI | |
Zhang X, Sun J, Wang H, et al: IGF-1R and Bmi-1 expressions in lung adenocarcinoma and their clinicopathologic and prognostic significance. Tumour Biol. 35:739–745. 2014. View Article : Google Scholar : PubMed/NCBI | |
Li X, Yang Z, Song W, et al: Overexpression of Bmi-1 contributes to the invasion and metastasis of hepatocellular carcinoma by increasing the expression of matrix metalloproteinase (MMP) 2, MMP-9 and vascular endothelial growth factor via the PTEN/PI3K/Akt pathway. Int J Oncol. 43:793–802. 2013.PubMed/NCBI | |
Engelsen IB, Mannelqvist M, Stefansson IM, et al: Low BMI-1 expression is associated with an activated BMI-1-driven signature, vascular invasion and hormone receptor loss in endometrial carcinoma. Br J Cancer. 98:1662–1669. 2008. View Article : Google Scholar : PubMed/NCBI | |
Molofsky AV, He S, Bydon M, Morrison SJ and Pardal R: Bmi-1 promotes neural stem cell self-renewal and neural development but not mouse growth and survival by repressing the p16Ink4a and p19Arf senescence pathways. Genes Dev. 19:1432–1437. 2005. View Article : Google Scholar : PubMed/NCBI | |
Mihara K, Chowdhury M, Nakaju N, et al: Bmi-1 is useful as a novel molecular marker for predicting progression of myelodysplastic syndrome and patient prognosis. Blood. 107:305–308. 2006. View Article : Google Scholar : PubMed/NCBI | |
Mohty M, Yong AS, Szydlo RM, Apperley JF and Melo JV: The polycomb group BMI1 gene is a molecular marker for predicting prognosis of chronic myeloid leukemia. Blood. 110:380–383. 2007. View Article : Google Scholar : PubMed/NCBI | |
Abd Al Kader L, Oka T, Takata K, et al: In aggressive variants of non-Hodgkin lymphomas, Ezh2 is strongly expressed and polycomb repressive complex PRC1.4 dominates over PRC1.2. Virchows Arch. 463:697–711. 2013. View Article : Google Scholar : PubMed/NCBI | |
Chen Y, Lian G, Zhang Q, et al: Overexpression of Bmi-1 induces the malignant transformation of gastric epithelial cells in vitro. Oncol Res. 21:33–41. 2013. View Article : Google Scholar : PubMed/NCBI | |
Gao FL, Li WS, Liu CL and Zhao GQ: Silencing Bmi-1 enhances the senescence and decreases the metastasis of human gastric cancer cells. World J Gastroenterol. 19:8764–8769. 2013. View Article : Google Scholar : PubMed/NCBI | |
Yin T, Wei H, Leng Z, et al: Bmi-1 promotes the chemoresistance, invasion and tumorigenesis of pancreatic cancer cells. Chemotherapy. 57:488–496. 2011. View Article : Google Scholar : PubMed/NCBI | |
Song W, Tao K, Li H, et al: Bmi-1 is related to proliferation, survival and poor prognosis in pancreatic cancer. Cancer Sci. 101:1754–1760. 2010. View Article : Google Scholar : PubMed/NCBI | |
Guo S, Xu X, Tang Y, et al: miR-15a inhibits cell proliferation and epithelial to mesenchymal transition in pancreatic ductal adenocarcinoma by down-regulating Bmi-1 expression. Cancer Lett. 344:40–46. 2014. View Article : Google Scholar : PubMed/NCBI | |
Kuang BH, Zhang MQ, Xu LH, et al: Proline-rich tyrosine kinase 2 and its phosphorylated form pY881 are novel prognostic markers for non-small-cell lung cancer progression and patients' overall survival. Br J Cancer. 109:1252–1263. 2013. View Article : Google Scholar : PubMed/NCBI | |
Song LB, Li J, Liao WT, et al: The polycomb group protein Bmi-1 represses the tumor suppressor PTEN and induces epithelial-mesenchymal transition in human nasopharyngeal epithelial cells. J Clin Invest. 119:3626–3636. 2009. View Article : Google Scholar : PubMed/NCBI | |
Dong P, Kaneuchi M, Watari H, et al: MicroRNA-194 inhibits epithelial to mesenchymal transition of endometrial cancer cells by targeting oncogene BMI-1. Mol Cancer. 10:992011. View Article : Google Scholar : PubMed/NCBI | |
Liu PW, Lin Y and Chen XY: Expression of B-cell-specific Moloney murine leukemia virus integration site 1 mRNA and protein in gastric cancer. J Dig Dis. 15:166–173. 2014. View Article : Google Scholar : PubMed/NCBI | |
Meng X, Wang Y, Zheng X, et al: shRNA-mediated knockdown of Bmi-1 inhibit lung adenocarcinoma cell migration and metastasis. Lung Cancer. 77:24–30. 2012. View Article : Google Scholar : PubMed/NCBI | |
Huang J, Qiu Y, Chen G, Huang L and He J: The relationship between Bmi-1 and the epithelial-mesenchymal transition in lung squamous cell carcinoma. Med Oncol. 29:1606–1613. 2012. View Article : Google Scholar : PubMed/NCBI | |
Colas E, Pedrola N, Devis L, et al: The EMT signaling pathways in endometrial carcinoma. Clin Transl Oncol. 14:715–720. 2012. View Article : Google Scholar : PubMed/NCBI | |
Huber GF, Albinger-Hegyi A, Soltermann A, et al: Expression patterns of Bmi-1 and p16 significantly correlate with overall, disease-specific and recurrence-free survival in oropharyngeal squamous cell carcinoma. Cancer. 117:4659–4670. 2011. View Article : Google Scholar : PubMed/NCBI | |
Dimri GP, Martinez JL, Jacobs JJ, et al: The Bmi-1 oncogene induces telomerase activity and immortalizes human mammary epithelial cells. Cancer Res. 62:4736–4745. 2002.PubMed/NCBI | |
Wang Y, Zhe H, Ding Z, Gao P, Zhang N and Li G: Cancer stem cell marker Bmi-1 expression is associated with basal-like phenotype and poor survival in breast cancer. World J Surg. 36:1189–1194. 2012. View Article : Google Scholar : PubMed/NCBI | |
Joensuu K, Hagstrom J, Leidenius M, et al: Bmi-1, c-myc and Snail expression in primary breast cancers and their metastases - elevated Bmi-1 expression in late breast cancer relapses. Virchows Arch. 459:31–39. 2011. View Article : Google Scholar : PubMed/NCBI | |
Wu J, Hu D and Zhang R: Depletion of Bmi-1 enhances 5-fluorouracil-induced apoptosis and autophagy in hepatocellular carcinoma cells. Oncol Lett. 4:723–726. 2012.PubMed/NCBI | |
Wang E, Bhattacharyya S, Szabolcs A, et al: Enhancing chemotherapy response with Bmi-1 silencing in ovarian cancer. PLoS One. 6:e179182011. View Article : Google Scholar : PubMed/NCBI | |
Xin T, Zhang FB, Sui GJ and Jin XM: Bmi-1 siRNA inhibited ovarian cancer cell line growth and decreased telomerase activity. Br J Biomed Sci. 69:62–66. 2012.PubMed/NCBI | |
Bhattacharyya J, Mihara K, Ohtsubo M, et al: Overexpression of BMI-1 correlates with drug resistance in B-cell lymphoma cells through the stabilization of survivin expression. Cancer Sci. 103:34–41. 2012. View Article : Google Scholar : PubMed/NCBI | |
Zhu Y, Yu F, Jiao Y, et al: Reduced miR-128 in breast tumor-initiating cells induces chemotherapeutic resistance via Bmi-1 and ABCC5. Clin Cancer Res. 17:7105–7115. 2011. View Article : Google Scholar : PubMed/NCBI | |
Liu ZG, Liu L, Xu LH, et al: Bmi-1 induces radioresistance in MCF-7 mammary carcinoma cells. Oncol Rep. 27:1116–1122. 2012.PubMed/NCBI | |
Vrzalikova K, Skarda J, Ehrmann J, et al: Prognostic value of Bmi-1 oncoprotein expression in NSCLC patients: a tissue microarray study. J Cancer Res Clin Oncol. 134:1037–1042. 2008. View Article : Google Scholar : PubMed/NCBI | |
Balasubramanian S, Kanade S, Han B and Eckert RL: A proteasome inhibitor-stimulated Nrf1 protein-dependent compensatory increase in proteasome subunit gene expression reduces polycomb group protein level. J Biol Chem. 287:36179–36189. 2012. View Article : Google Scholar : PubMed/NCBI | |
Liu S, Tetzlaff MT, Cui R and Xu X: miR-200c inhibits melanoma progression and drug resistance through down-regulation of BMI-1. Am J Pathol. 181:1823–1835. 2012. View Article : Google Scholar : PubMed/NCBI | |
Qin ZK, Yang JA, Ye YL, et al: Expression of Bmi-1 is a prognostic marker in bladder cancer. BMC Cancer. 9:612009. View Article : Google Scholar : PubMed/NCBI | |
Farivar S, Zati Keikha R, Shiari R and Jadali F: Expression of bmi-1 in pediatric brain tumors as a new independent prognostic marker of patient survival. Biomed Res Int. 2013:1925482013. View Article : Google Scholar : PubMed/NCBI | |
Mimeault M and Batra SK: Frequent gene products and molecular pathways altered in prostate cancer- and metastasis-initiating cells and their progenies and novel promising multitargeted therapies. Mol Med. 17:949–964. 2011. View Article : Google Scholar : PubMed/NCBI | |
Park CH, Bergsagel DE and McCulloch EA: Mouse myeloma tumor stem cells: A primary cell culture assay. J Natl Cancer Inst. 46:411–422. 1971.PubMed/NCBI | |
Oishi N and Wang XW: Novel therapeutic strategies for targeting liver cancer stem cells. Int J Biol Sci. 7:517–535. 2011. View Article : Google Scholar : PubMed/NCBI | |
Raaphorst FM: Self-renewal of hematopoietic and leukemic stem cells: a central role for the Polycomb-group gene Bmi-1. Trends Immunol. 24:522–524. 2003. View Article : Google Scholar : PubMed/NCBI | |
Iwama A, Oguro H, Negishi M, Kato Y and Nakauchia H: Epigenetic regulation of hematopoietic stem cell self-renewal by polycomb group genes. Int J Hematol. 81:294–300. 2005. View Article : Google Scholar : PubMed/NCBI | |
Gong H, Zhang YC and Liu WL: Regulatory effects of Bmi-1 gene on self-renewal of hematopoietic stem cells - review. Zhongguo Shi Yan Xue Ye Xue Za Zhi. 14:413–415. 2006.(In Chinese). PubMed/NCBI | |
Park IK, Qian D, Kiel M, et al: Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature. 423:302–305. 2003. View Article : Google Scholar : PubMed/NCBI | |
Lessard J and Sauvageau G: Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature. 423:255–260. 2003. View Article : Google Scholar : PubMed/NCBI | |
Lee CJ, Dosch J and Simeone DM: Pancreatic cancer stem cells. J Clin Oncol. 26:2806–2812. 2008. View Article : Google Scholar : PubMed/NCBI | |
Molofsky AV, Pardal R, Iwashita T, Park IK, Clarke MF and Morrison SJ: Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature. 425:962–967. 2003. View Article : Google Scholar : PubMed/NCBI | |
Yu X, Jiang X, Li H, Guo L, Jiang W and Lu SH: miR-203 inhibits the proliferation and self-renewal of esophageal cancer stem-like cells by suppressing stem renewal factor Bmi-1. Stem Cells Dev. 23:576–585. 2014. View Article : Google Scholar : PubMed/NCBI | |
Ma J, Lanza DG, Guest I, et al: Characterization of mammary cancer stem cells in the MMTV-PyMT mouse model. Tumour Biol. 33:1983–1996. 2012. View Article : Google Scholar : PubMed/NCBI | |
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. 12:1462012. View Article : Google Scholar : PubMed/NCBI | |
Liu W, Feng JQ, Shen XM, Wang HY, Liu Y and 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. 118:1693–1700. 2012. View Article : Google Scholar : PubMed/NCBI | |
Gonzalez S, Klatt P, Delgado S, et al: Oncogenic activity of Cdc6 through repression of the INK4/ARF locus. Nature. 440:702–706. 2006. View Article : Google Scholar : PubMed/NCBI | |
Koh CM, Iwata T, Zheng Q, Bethel C, Yegnasubramanian S and De Marzo AM: Myc enforces overexpression of EZH2 in early prostatic neoplasia via transcriptional and post-transcriptional mechanisms. Oncotarget. 2:669–683. 2011.PubMed/NCBI | |
Sander S, Bullinger L, Klapproth K, et al: MYC stimulates EZH2 expression by repression of its negative regulator miR-26a. Blood. 112:4202–4212. 2008. View Article : Google Scholar : PubMed/NCBI | |
Ma L, Young J, Prabhala H, et al: miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol. 12:247–256. 2010.PubMed/NCBI | |
Coskun V, Zhao J and Sun YE: Neurons or glia? Can SHP2 know it all? Sci STKE. 2007:pe582007. View Article : Google Scholar : PubMed/NCBI | |
Ke Y, Zhang EE, Hagihara K, et al: Deletion of Shp2 in the brain leads to defective proliferation and differentiation in neural stem cells and early postnatal lethality. Mol Cell Biol. 27:6706–6717. 2007. View Article : Google Scholar : PubMed/NCBI | |
Gao C, Kong NR and Chai L: The role of stem cell factor SALL4 in leukemogenesis. Crit Rev Oncog. 16:117–127. 2011. View Article : Google Scholar : PubMed/NCBI | |
Yang J, Chai L, Liu F, et al: Bmi-1 is a target gene for SALL4 in hematopoietic and leukemic cells. Proc Natl Acad Sci USA. 104:10494–10499. 2007. View Article : Google Scholar : PubMed/NCBI | |
Zhu J, Wang H, Sun Q, et al: Nrf2 is required to maintain the self-renewal of glioma stem cells. BMC Cancer. 13:3802013. View Article : Google Scholar : PubMed/NCBI | |
Won HY, Lee JY, Shin DH, et al: Loss of Mel-18 enhances breast cancer stem cell activity and tumorigenicity through activating Notch signaling mediated by the Wnt/TCF pathway. FASEB J. 26:5002–5013. 2012. View Article : Google Scholar : PubMed/NCBI | |
Jacobs JJ, Kieboom K, Marino S, DePinho RA and van Lohuizen M: The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature. 397:164–168. 1999. View Article : Google Scholar : PubMed/NCBI | |
Lowe SW and Sherr CJ: Tumor suppression by Ink4a-Arf: progress and puzzles. Curr Opin Genet Dev. 13:77–83. 2003. View Article : Google Scholar : PubMed/NCBI | |
Carnero A, Hudson JD, Price CM and Beach DH: p16INK4A and p19ARF act in overlapping pathways in cellular immortalization. Nat Cell Biol. 2:148–155. 2000. View Article : Google Scholar : PubMed/NCBI | |
Chiba T, Seki A, Aoki R, et al: Bmi1 promotes hepatic stem cell expansion and tumorigenicity in both Ink4a/Arf-dependent and -independent manners in mice. Hepatology. 52:1111–1123. 2010. View Article : Google Scholar : PubMed/NCBI | |
Grinstein E and Wernet P: Cellular signaling in normal and cancerous stem cells. Cell Signal. 19:2428–2433. 2007. View Article : Google Scholar : PubMed/NCBI | |
Grinstein E and Mahotka C: Stem cell divisions controlled by the proto-oncogene BMI-1. J Stem Cells. 4:141–146. 2009.PubMed/NCBI | |
Zacharek SJ, Fillmore CM, Lau AN, et al: Lung stem cell self-renewal relies on BMI1-dependent control of expression at imprinted loci. Cell Stem Cell. 9:272–281. 2011. View Article : Google Scholar : PubMed/NCBI | |
Bruggeman SW, Hulsman D and van Lohuizen M: Bmi1 deficient neural stem cells have increased integrin dependent adhesion to self-secreted matrix. Biochim Biophys Acta. 1790:351–360. 2009. View Article : Google Scholar : PubMed/NCBI | |
Fasano CA, Dimos JT, Ivanova NB, Lowry N, Lemischka IR and Temple S: shRNA knockdown of Bmi-1 reveals a critical role for p21-Rb pathway in NSC self-renewal during development. Cell Stem Cell. 1:87–99. 2007. View Article : Google Scholar : PubMed/NCBI | |
Jiang L, Song L, Wu J, et al: Bmi-1 promotes glioma angiogenesis by activating NF-κB signaling. PLoS One. 8:e555272013. View Article : Google Scholar : PubMed/NCBI | |
Vlachostergios PJ and Papandreou CN: The Bmi-1/NF-κB/VEGF story: another hint for proteasome involvement in glioma angiogenesis? J Cell Commun Signal. 7:235–237. 2013. View Article : Google Scholar : PubMed/NCBI |