A microRNA expression signature characterizing the properties of tumor-initiating cells for breast cancer

Wang,Lixin; Zhang,Daoqiang; Zhang,Changwen; Zhang,Shuping; Wang,Zhe; Qu,Chen; Liu,Sijin

doi:10.3892/ol.2011.431

A microRNA expression signature characterizing the properties of tumor-initiating cells for breast cancer

Authors:
- Lixin Wang
- Daoqiang Zhang
- Changwen Zhang
- Shuping Zhang
- Zhe Wang
- Chen Qu
- Sijin Liu
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Affiliations: State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, P.R. China
Published online on: September 28, 2011 https://doi.org/10.3892/ol.2011.431
Pages: 119-124

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Abstract

microRNAs (miRNAs) are involved in controlling tumor behaviors either as oncogenes or tumor suppressors. To elucidate the role of miRNAs in the regulation of tumor initiation, we delineated the microRNA expression signature characterizing the properties of tumor-initiating cells for breast cancer. A group of miRNAs were differentially expressed in MDA-MB‑231 and SUM1315 cells (with a high proportion of breast cancer tumor‑initiating cells, CD44+CD24-/low subpopulation) compared to MCF-7 cells (only a small proportion of CD44+CD24-/low cells). Among the differentially expressed miRNAs common to MDA-MB‑231 and SUM1315, approximately 46% of them are suggested to regulate the 'stemness' of stem cells or progenitor cells. Taken together, these findings suggested that miRNAs contribute to the maintenance of tumor‑initiating properties and indicate the potential value of the miRNA expression signature in characterizing or predicting the features (including metastasis) of breast cancer.

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1	Shipitsin M, Campbell LL, Argani P, et al: Molecular definition of breast tumor heterogeneity. Cancer Cell. 11:259–273. 2007. View Article : Google Scholar : PubMed/NCBI
2	Ponti D, Costa A, Zaffaroni N, et al: Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res. 65:5506–5511. 2005.PubMed/NCBI
3	Deng SCG, Croce CM, Coukos G and Zhang L: Mechanisms of microRNA deregulation in human cancer. Cell Cycle. 7:2643–2646. 2008. View Article : Google Scholar : PubMed/NCBI
4	Garzon R, Marcucci G and Croce CM: Targeting microRNAs in cancer: rationale, strategies and challenges. Nat Rev Drug Discov. 9:775–789. 2010. View Article : Google Scholar : PubMed/NCBI
5	Suh M-R, Lee Y, Kim JY, et al: Human embryonic stem cells express a unique set of microRNAs. Dev Biol. 270:488–498. 2004. View Article : Google Scholar : PubMed/NCBI
6	Croce CM and Calin GA: miRNAs, cancer, and stem cell division. Cell. 122:6–7. 2005. View Article : Google Scholar : PubMed/NCBI
7	Bernstein EKS, Carmell MA, Murchison EP, Alcorn H, Li MZ, Mills AA, Elledge SJ, Anderson KV and Hannon GJ: Dicer is essential for mouse development. Nat Genet. 35:215–217. 2003. View Article : Google Scholar
8	Kanellopoulou C, Muljo SA, Kung AL, et al: Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 19:489–501. 2005. View Article : Google Scholar : PubMed/NCBI
9	Liu S, Goldstein RH, Scepansky EM and Rosenblatt M: Inhibition of rho-associated kinase signaling prevents breast cancer metastasis to human bone. Cancer Res. 69:8742–8751. 2009. View Article : Google Scholar : PubMed/NCBI
10	Yu F, Yao H, Zhu P, et al: let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell. 131:1109–1123. 2007. View Article : Google Scholar : PubMed/NCBI
11	Liu S, Suragani RN, Wang F, Han A, Zhao W, Andrews NC and Chen JJ: The function of heme-regulated eIF2alpha kinase in murine iron homeostasis and macrophage maturation. J Clin Invest. 117:3296–3305. 2007. View Article : Google Scholar : PubMed/NCBI
12	Fillmore CM and Kuperwasser C: Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res. 10:R252008. View Article : Google Scholar : PubMed/NCBI
13	Kuperwasser C, Dessain S, Bierbaum BE, et al: A mouse model of human breast cancer metastasis to human bone. Cancer Res. 65:6130–6138. 2005. View Article : Google Scholar : PubMed/NCBI
14	Kang Y, Siegel PM, Shu W, et al: A multigenic program mediating breast cancer metastasis to bone. Cancer Cell. 3:537–549. 2003. View Article : Google Scholar : PubMed/NCBI
15	Hinton A, Afrikanova I, Wilson M, et al: A distinct microRNA signature for definitive endoderm derived from human embryonic stem cells. Stem Cells and Dev. 19:797–807. 2010. View Article : Google Scholar : PubMed/NCBI
16	Lena AM, Shalom-Feuerstein R, Di Val Cervo PR, et al: miR-203 represses 'stemness' by repressing [Delta]Np63. Cell Death Differ. 15:1187–1195. 2008.
17	Bueno MJ, Pérez de Castro I, Gómez de Cedrón M, et al: Genetic and epigenetic silencing of microRNA-203 enhances ABL1 and BCR-ABL1 oncogene expression. Cancer Cell. 13:496–506. 2008. View Article : Google Scholar : PubMed/NCBI
18	Shimono Y, Zabala M, Cho RW, et al: Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell. 138:592–603. 2009. View Article : Google Scholar : PubMed/NCBI
19	Pek JW, Lim AK and Kai T: Drosophila maelstrom ensures proper germline stem cell lineage differentiation by repressing microRNA-7. Dev Cell. 17:417–424. 2009. View Article : Google Scholar
20	Mallick B, Ghosh Z and Chakrabarti J: MicroRNome analysis unravels the molecular basis of SARS infection in bronchoalveolar stem cells. PLoS ONE. 4:e78372009. View Article : Google Scholar : PubMed/NCBI
21	Wellner U, Schubert J, Burk UC, et al: The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol. 11:1487–1495. 2009. View Article : Google Scholar : PubMed/NCBI
22	Ma Y-L, Zhang P, Wang F, et al: Human embryonic stem cells and metastatic colorectal cancer cells shared the common endogenous human microRNA-26b. J Cell Mol Med. View Article : Google Scholar : (E-pub ahead of print). Accessed September 10, 2010
23	Singh SK, Kagalwala MN, Parker-Thornburg J, Adams H and Majumder S: REST maintains self-renewal and pluripotency of embryonic stem cells. Nature. 453:223–227. 2008. View Article : Google Scholar : PubMed/NCBI
24	Schoolmeesters A, Eklund T, Leake D, et al: Functional profiling reveals critical role for miRNA in differentiation of human mesenchymal stem cells. PLoS ONE. 4:e56052009. View Article : Google Scholar : PubMed/NCBI
25	Ibarra I, Erlich Y, Muthuswamy SK, Sachidanandam R and Hannon GJ: A role for microRNAs in maintenance of mouse mammary epithelial progenitor cells. Genes Dev. 21:3238–3243. 2007. View Article : Google Scholar : PubMed/NCBI
26	Rybak A, Fuchs H, Smirnova L, et al: A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat Cell Biol. 10:987–993. 2008. View Article : Google Scholar : PubMed/NCBI
27	Qian S, Ding JY, Xie R, et al: MicroRNA expression profile of bronchioalveolar stem cells from mouse lung. Biochem Biophys Res Commun. 377:668–673. 2008. View Article : Google Scholar : PubMed/NCBI
28	Lakshmipathy U and Hart RP: Concise review: microRNA expression in multipotent mesenchymal stromal cells. Stem Cells. 26:356–363. 2008. View Article : Google Scholar : PubMed/NCBI
29	Godlewski J, Nowicki MO, Bronisz A, et al: Targeting of the Bmi-1 oncogene/stem cell renewal factor by microRNA-128 inhibits glioma proliferation and self-renewal. Cancer Res. 68:9125–9130. 2008. View Article : Google Scholar : PubMed/NCBI
30	Luzi E, Marini F, Sala SC, Tognarini I, Galli G and Brandi ML: Osteogenic differentiation of human adipose tissue-derived stem cells is modulated by the miR-26a targeting of the SMAD1 transcription factor. J Bone Miner Res. 23:287–295. 2008. View Article : Google Scholar : PubMed/NCBI
31	Foshay KM and Gallicano GI: miR-17 family miRNAs are expressed during early mammalian development and regulate stem cell differentiation. Dev Biol. 326:431–443. 2009. View Article : Google Scholar : PubMed/NCBI
32	Rogler CE, LeVoci L, Ader T, et al: MicroRNA-23b cluster microRNAs regulate transforming growth factor-beta/bone morphogenetic protein signaling and liver stem cell differentiation by targeting Smads. Hepatology. 50:575–584. 2009. View Article : Google Scholar : PubMed/NCBI
33	Lee S, Jung J-W, Park S-B, et al: Histone deacetylase regulates high mobility group A2-targeting microRNAs in human cord blood-derived multipotent stem cell aging. Cell Mol Life Sci. 68:325–336. 2011. View Article : Google Scholar : PubMed/NCBI
34	Sengupta S, Nie J, Wagner RJ, Yang C, Stewart R and Thomson JA: MicroRNA 92b controls the G1/S checkpoint gene p57 in human embryonic stem cells. Stem Cells. 27:1524–1528. 2009. View Article : Google Scholar : PubMed/NCBI
35	Tzur G, Levy A, Meiri E, et al: MicroRNA expression patterns and function in endodermal differentiation of human embryonic stem cells. PLoS ONE. 3:e37262008. View Article : Google Scholar : PubMed/NCBI
36	Tsai Z-Y, Singh S, Yu S-L, et al: Identification of microRNAs regulated by activin A in human embryonic stem cells. J Cell Biochem. 109:93–102. 2010.PubMed/NCBI
37	Wagner W, Horn P, Castoldi M, et al: Replicative senescence of mesenchymal stem cells: A continuous and organized process. PLoS ONE. 3:e22132008. View Article : Google Scholar : PubMed/NCBI
38	Wang K-H, Kao A-P, Singh S, et al: Comparative expression profiles of mRNAs and microRNAs among human mesenchymal stem cells derived from breast, face, and abdominal adipose tissues. Kaohsiung J Med Sci. 26:113–122. 2010. View Article : Google Scholar : PubMed/NCBI
39	Han Y-C, Park CY, Bhagat G, et al: microRNA-29a induces aberrant self-renewal capacity in hematopoietic progenitors, biased myeloid development, and acute myeloid leukemia. J Exp Med. 207:475–489. 2010. View Article : Google Scholar : PubMed/NCBI
40	Shi L, Zhang J, Pan T, et al: MiR-125b is critical for the suppression of human U251 glioma stem cell proliferation. Brain Res. 1312:120–126. 2010. View Article : Google Scholar : PubMed/NCBI
41	Tarantino C, Paolella G, Cozzuto L, et al: miRNA 34a, 100, and 137 modulate differentiation of mouse embryonic stem cells. FASEB J. 24:3255–3263. 2010. View Article : Google Scholar : PubMed/NCBI
42	Decembrini S, Bressan D, Vignali R, et al: MicroRNAs couple cell fate and developmental timing in retina. Proc Natl Acad Sci USA. 106:21179–21184
43	Poliseno L, Tuccoli A, Mariani L, et al: MicroRNAs modulate the angiogenic properties of HUVECs. Blood. 108:3068–3071. 2006. View Article : Google Scholar : PubMed/NCBI
44	Wu L and Belasco JG: Micro-RNA regulation of the mammalian lin-28 gene during neuronal differentiation of embryonal carcinoma cells. Mol Cell Biol. 25:9198–9208. 2005. View Article : Google Scholar : PubMed/NCBI
45	McPherson JP, Tamblyn L, Elia A, et al: Lats2/Kpm is required for embryonic development, proliferation control and genomic integrity. Embo J. 23:3677–3688. 2004. View Article : Google Scholar : PubMed/NCBI
46	Savarese F, Dávila A, Nechanitzky R, et al: Satb1 and Satb2 regulate embryonic stem cell differentiation and Nanog expression. Genes Dev. 23:2625–2638. 2009. View Article : Google Scholar : PubMed/NCBI
47	Zheng H, Ying H, Wiedemeyer R, et al: PLAGL2 regulates Wnt signaling to impede differentiation in neural stem cells and gliomas. Cancer Cell. 17:497–509. 2010. View Article : Google Scholar : PubMed/NCBI
48	Reinhart BJ, Slack FJ, Basson M, et al: The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature. 403:901–906. 2000. View Article : Google Scholar : PubMed/NCBI