Skip to main content

Advertisement

SpringerLink
Log in

The emerging role of lncRNAs in the regulation of cancer stem cells

  • Review
  • Published:
Cellular Oncology Aims and scope Submit manuscript

Abstract

Background

Tumors contain a functional subpopulation of cells that exhibit stem cell properties. These cells, named cancer stem cells (CSCs), play significant roles in the initiation and progression of cancer. Long non-coding RNAs (lncRNAs) can act at the transcriptional, posttranscriptional and translational level. As such, they may be involved in various biological processes such as DNA damage repair, inflammation, metabolism, cell survival, cell signaling, cell growth and differentiation. Accumulating evidence indicates that lncRNAs are key regulators of the CSC subpopulation, thereby contributing to cancer progression. The aim of this review is to overview current knowledge about the functional role and the mechanisms of action of lncRNAs in the initiation, maintenance and regulation of CSCs derived from different neoplasms. These lncRNAs include CTCF7, ROR, DILC, HOTAIR, H19, HOTTIP, ATB, HIF2PUT, SOX2OT, MALAT-1, CUDR, Lnc34a, Linc00617, DYNC2H1–4, PVT1, SOX4 and ARSR Uc.283-plus. Furthermore, we will illustrate how lncRNAs may regulate asymmetric CSC division and contribute to self-renewal, drug resistance and EMT, thus affecting the metastasis and recurrence of different cancers. In addition, we will highlight the implications of targeting lncRNAs to improve the efficacy of conventional drug therapies and to hamper CSC survival and proliferation.

Conclusions

lncRNAs are valuable tools in the search for new targets to selectively eliminate CSCs and improve clinical outcomes. LncRNAs may serve as excellent therapeutic targets because they are stable, easily detectable and expressed in tissue-specific contexts.

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. S. Djebali, C.A. Davis, A. Merkel, A. Dobin, T. Lassmann, A. Mortazavi, A. Tanzer, J. Lagarde, W. Lin, F. Schlesinger, C. Xue, G.K. Marinov, J. Khatun, B.A. Williams, C. Zaleski, J. Rozowsky, M. Roder, F. Kokocinski, R.F. Abdelhamid, T. Alioto, I. Antoshechkin, M.T. Baer, N.S. Bar, P. Batut, K. Bell, I. Bell, S. Chakrabortty, X. Chen, J. Chrast, J. Curado, T. Derrien, J. Drenkow, E. Dumais, J. Dumais, R. Duttagupta, E. Falconnet, M. Fastuca, K. Fejes-Toth, P. Ferreira, S. Foissac, M.J. Fullwood, H. Gao, D. Gonzalez, A. Gordon, H. Gunawardena, C. Howald, S. Jha, R. Johnson, P. Kapranov, B. King, C. Kingswood, O.J. Luo, E. Park, K. Persaud, J.B. Preall, P. Ribeca, B. Risk, D. Robyr, M. Sammeth, L. Schaffer, L.H. See, A. Shahab, J. Skancke, A.M. Suzuki, H. Takahashi, H. Tilgner, D. Trout, N. Walters, H. Wang, J. Wrobel, Y. Yu, X. Ruan, Y. Hayashizaki, J. Harrow, M. Gerstein, T. Hubbard, A. Reymond, S.E. Antonarakis, G. Hannon, M.C. Giddings, Y. Ruan, B. Wold, P. Carninci, R. Guigo, T.R. Gingeras, Landscape of transcription in human cells. Nature 489, 101–108 (2012)

    CAS  PubMed  PubMed Central  Google Scholar 

  2. V. Taucher, H. Mangge, J. Haybaeck, Non-coding RNAs in pancreatic cancer: Challenges and opportunities for clinical application. Cell Oncol 39, 295–318 (2016)

    CAS  Google Scholar 

  3. S. Jalali, S. Gandhi, V. Scaria, Navigating the dynamic landscape of long noncoding RNA and protein-coding gene annotations in GENCODE. Hum Genomics 10, 35 (2016)

    PubMed  PubMed Central  Google Scholar 

  4. J.L. Rinn, H.Y. Chang, Genome regulation by long noncoding RNAs. Annu Rev Biochem 81, 145–166 (2012)

    CAS  PubMed  Google Scholar 

  5. G. Bohmdorfer, S. Sethuraman, M.J. Rowley, M. Krzyszton, M.H. Rothi, L. Bouzit, A.T. Wierzbicki, Long non-coding RNA produced by RNA polymerase V determines boundaries of heterochromatin. elife 5, e19092 (2016)

    PubMed  PubMed Central  Google Scholar 

  6. A. Barski, I. Chepelev, D. Liko, S. Cuddapah, A.B. Fleming, J. Birch, K. Cui, R.J. White, K. Zhao, Pol II and its associated epigenetic marks are present at pol III-transcribed noncoding RNA genes. Nat Struct Mol Biol 17, 629–634 (2010)

    CAS  PubMed  PubMed Central  Google Scholar 

  7. K.W. Vance, C.P. Ponting, Transcriptional regulatory functions of nuclear long noncoding RNAs. Trends Genet 30, 348–355 (2014)

    CAS  PubMed  PubMed Central  Google Scholar 

  8. L.L. Chen, Linking long noncoding RNA localization and function. Trends Biochem Sci 41, 761–772 (2016)

    CAS  PubMed  Google Scholar 

  9. J. Cao, The functional role of long non-coding RNAs and epigenetics. Biol Proced Online 16, 11 (2014)

    PubMed  PubMed Central  Google Scholar 

  10. T.R. Mercer, J.S. Mattick, Structure and function of long noncoding RNAs in epigenetic regulation. Nat Struct Mol Biol 20, 300–307 (2013)

    CAS  PubMed  Google Scholar 

  11. M. Guttman, J.L. Rinn, Modular regulatory principles of large non-coding RNAs. Nature 482, 339–346 (2012)

    CAS  PubMed  PubMed Central  Google Scholar 

  12. X. Wang, S. Arai, X. Song, D. Reichart, K. Du, G. Pascual, P. Tempst, M.G. Rosenfeld, C.K. Glass, R. Kurokawa, Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature 454, 126–130 (2008)

    CAS  PubMed  PubMed Central  Google Scholar 

  13. K.C. Wang, H.Y. Chang, Molecular mechanisms of long noncoding RNAs. Mol Cell 43, 904–914 (2011)

    CAS  PubMed  PubMed Central  Google Scholar 

  14. P.O. Angrand, C. Vennin, X. Le Bourhis, E. Adriaenssens, The role of long non-coding RNAs in genome formatting and expression. Front Genet 6, 165 (2015)

  15. A. Ferraro, Altered primary chromatin structures and their implications in cancer development. Cell Oncol 39, 195–210 (2016)

    Google Scholar 

  16. J.R. Prensner, A.M. Chinnaiyan, The emergence of lncRNAs in cancer biology. Cancer Discov 1, 391–407 (2011)

    CAS  PubMed  PubMed Central  Google Scholar 

  17. R.B. Perry, I. Ulitsky, The functions of long noncoding RNAs in development and stem cells. Development 143, 3882–3894 (2016)

    PubMed  Google Scholar 

  18. G. Eades, Y.S. Zhang, Q.L. Li, J.X. Xia, Y. Yao, Q. Zhou, Long non-coding RNAs in stem cells and cancer. World J Clin Oncol 5, 134–141 (2014)

    PubMed  PubMed Central  Google Scholar 

  19. D. Hanahan, R.A. Weinberg, Hallmarks of cancer: The next generation. Cell 144, 646–674 (2011)

    CAS  Google Scholar 

  20. S.L. Floor, J.E. Dumont, C. Maenhaut, E. Raspe, Hallmarks of cancer: Of all cancer cells, all the time? Trends Mol Med 18, 509–515 (2012)

    CAS  PubMed  Google Scholar 

  21. D. Hanahan, L.M. Coussens, Accessories to the crime: Functions of cells recruited to the tumor microenvironment. Cancer Cell 21, 309–322 (2012)

    CAS  PubMed  Google Scholar 

  22. A. Cicalese, G. Bonizzi, C.E. Pasi, M. Faretta, S. Ronzoni, B. Giulini, C. Brisken, S. Minucci, P.P. Di Fiore, P.G. Pelicci, The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 138, 1083–1095 (2009)

    CAS  PubMed  Google Scholar 

  23. M.F. Clarke, M. Fuller, Stem cells and cancer: Two faces of eve. Cell 124, 1111–1115 (2006)

    CAS  PubMed  Google Scholar 

  24. Y. Welte, J. Adjaye, H.R. Lehrach, C.R. Regenbrecht, Cancer stem cells in solid tumors: Elusive or illusive? Cell Commun Signal 8, 6 (2010)

    PubMed  PubMed Central  Google Scholar 

  25. S. Bugide, V.K. Gonugunta, V. Penugurti, V.L. Malisetty, R.K. Vadlamudi, B. Manavathi, HPIP promotes epithelial-mesenchymal transition and cisplatin resistance in ovarian cancer cells through PI3K/AKT pathway activation. Cell Oncol 40, 133–144 (2017)

    CAS  Google Scholar 

  26. M.R. Sam, P. Ahangar, V. Nejati, R. Habibian, Treatment of LS174T colorectal cancer stem-like cells with n-3 PUFAs induces growth suppression through inhibition of survivin expression and induction of caspase-3 activation. Cell Oncol 39, 69–77 (2016)

    CAS  Google Scholar 

  27. M. Munz, P.A. Baeuerle, O. Gires, The emerging role of EpCAM in cancer and stem cell signaling. Cancer Res 69, 5627–5629 (2009)

    CAS  PubMed  Google Scholar 

  28. K. Vazquez-Santillan, J. Melendez-Zajgla, L. Jimenez-Hernandez, G. Martinez-Ruiz, V. Maldonado, NF-kappaB signaling in cancer stem cells: A promising therapeutic target? Cell Oncol 38, 327–339 (2015)

    CAS  Google Scholar 

  29. A. Sathyanarayanan, K.S. Chandrasekaran, D. Karunagaran, microRNA-145 modulates epithelial-mesenchymal transition and suppresses proliferation, migration and invasion by targeting SIP1 in human cervical cancer cells. Cell Oncol 40, 119–131 (2017)

    CAS  Google Scholar 

  30. Q. Zhang, K. Matsuura, D.E. Kleiner, F. Zamboni, H.J. Alter, P. Farci, Analysis of long noncoding RNA expression in hepatocellular carcinoma of different viral etiology. J Transl Med 14, 328 (2016)

    PubMed  PubMed Central  Google Scholar 

  31. F. Wang, J.H. Yuan, S.B. Wang, F. Yang, S.X. Yuan, C. Ye, N. Yang, W.P. Zhou, W.L. Li, W. Li, S.H. Sun, Oncofetal long noncoding RNA PVT1 promotes proliferation and stem cell-like property of hepatocellular carcinoma cells by stabilizing NOP2. Hepatology 60, 1278–1290 (2014)

    CAS  PubMed  Google Scholar 

  32. M.A. Parasramka, T. Patel, Long non-coding RNA regulation of liver cancer stem cell self-renewal offers new therapeutic targeting opportunities. Stem Cell Investig 3, 1 (2016)

    PubMed  PubMed Central  Google Scholar 

  33. H. Li, L. Zhu, L. Xu, K. Qin, C. Liu, Y. Yu, D. Su, K. Wu, Y. Sheng, Long noncoding RNA linc00617 exhibits oncogenic activity in breast cancer. Mol Carcinog 56, 3–17 (2017)

    CAS  PubMed  Google Scholar 

  34. J. Yao, J. Li, P. Geng, Y. Li, H. Chen, Y. Zhu, Knockdown of a HIF-2alpha promoter upstream long noncoding RNA impairs colorectal cancer stem cell properties in vitro through HIF-2alpha downregulation. Onco Targets Ther 8, 3467–3474 (2015)

    PubMed  PubMed Central  Google Scholar 

  35. W. Li, X. He, R. Xue, Y. Zhang, X. Zhang, J. Lu, Z. Zhang, L. Xue, Combined over-expression of the hypoxia-inducible factor 2alpha gene and its long non-coding RNA predicts unfavorable prognosis of patients with osteosarcoma. Pathol Res Pract 212, 861–866 (2016)

    CAS  PubMed  Google Scholar 

  36. Y. Wang, J. Yao, H. Meng, Z. Yu, Z. Wang, X. Yuan, H. Chen, A. Wang, A novel long non-coding RNA, hypoxia-inducible factor-2alpha promoter upstream transcript, functions as an inhibitor of osteosarcoma stem cells in vitro. Mol Med Rep 11, 2534–2540 (2015)

    CAS  PubMed  Google Scholar 

  37. A. Shahryari, M.R. Rafiee, Y. Fouani, N.A. Oliae, N.M. Samaei, M. Shafiee, S. Semnani, M. Vasei, S.J. Mowla, Two novel splice variants of SOX2OT, SOX2OT-S1, and SOX2OT-S2 are coupregulated with SOX2 and OCT4 in esophageal squamous cell carcinoma. Stem Cells 32, 126–134 (2014)

    CAS  PubMed  Google Scholar 

  38. M.E. Askarian-Amiri, V. Seyfoddin, C.E. Smart, J. Wang, J.E. Kim, H. Hansji, B.C. Baguley, G.J. Finlay, E.Y. Leung, Emerging role of long non-coding RNA SOX2OT in SOX2 regulation in breast cancer. PLoS One 9, e102140 (2014)

    PubMed  PubMed Central  Google Scholar 

  39. Z. Hou, W. Zhao, J. Zhou, L. Shen, P. Zhan, C. Xu, C. Chang, H. Bi, J. Zou, X. Yao, R. Huang, L. Yu, J. Yan, A long noncoding RNA Sox2ot regulates lung cancer cell proliferation and is a prognostic indicator of poor survival. Int J Biochem Cell Biol 53, 380–388 (2014)

    CAS  PubMed  Google Scholar 

  40. P.P. Amaral, C. Neyt, S.J. Wilkins, M.E. Askarian-Amiri, S.M. Sunkin, A.C. Perkins, J.S. Mattick, Complex architecture and regulated expression of the Sox2ot locus during vertebrate development. RNA 15, 2013–2027 (2009)

    CAS  PubMed  PubMed Central  Google Scholar 

  41. M. Saghaeian Jazi, N.M. Samaei, M. Ghanei, M.B. Shadmehr, S.J. Mowla, Identification of new SOX2OT transcript variants highly expressed in human cancer cell lines and down regulated in stem cell differentiation. Mol Biol Rep 43, 65–72 (2016)

    CAS  PubMed  Google Scholar 

  42. S.S. Saha, R. Roy Chowdhury, N.R. Mondal, B. Chakravarty, T. Chatterjee, S. Roy, S. Sengupta., Identification of genetic variation in the lncRNA HOTAIR associated with HPV16-related cervical cancer pathogenesis. Cell Oncol 39, 559–572 (2016)

    Google Scholar 

  43. S. Sharma Saha, R. Roy Chowdhury, N.R. Mondal, B. Chakravarty, T. Chatterjee, S. Roy, S. Sengupta, Identification of genetic variation in the lncRNA HOTAIR associated with HPV16-related cervical cancer pathogenesis. Cell Oncol 39, 559–572 (2016)

    CAS  Google Scholar 

  44. Y.N. Jun Dou, X. He, M.L. Di Wu, S. Wu, R. Zhang, M. Guo, Fengsu, l. Zhao, Decreasing lncRNA HOTAIR expression inhibits human colorectal cancer stem cells. Am J Transl Res 8, 98–108 (2016)

    PubMed  PubMed Central  Google Scholar 

  45. C. Padua Alves, A.S. Fonseca, B.R. Muys, E.L.B.R. de Barros, M.C. Burger, J.E. de Souza, V. Valente, M.A. Zago, W.A. Silva Jr., Brief report: The lincRNA Hotair is required for epithelial-to-mesenchymal transition and stemness maintenance of cancer cell lines. Stem Cells 31, 2827–2832 (2013)

    PubMed  Google Scholar 

  46. J. Deng, M. Yang, R. Jiang, N. An, X. Wang, B. Liu, Long non-coding RNA HOTAIR regulates the proliferation, self-renewal capacity, tumor formation and migration of the Cancer stem-like cell (CSC) subpopulation enriched from breast Cancer cells. PLoS One 12, e0170860 (2017)

    PubMed  PubMed Central  Google Scholar 

  47. J.A. Haiyan Li, M. Wu, Q. Zheng, X. Gui, T. Li, P. Hu, D. Lu, LncRNA HOTAIR promotes human liver cancer stem cell malignant growth through downregulation of SETD2. Oncotarget 6, 27847–27864 (2015)

    PubMed  PubMed Central  Google Scholar 

  48. K. Fang, P. Liu, S. Dong, Y. Guo, X. Cui, X. Zhu, X. Li, L. Jiang, T. Liu, Y. Wu, Magnetofection based on superparamagnetic iron oxide nanoparticle-mediated low lncRNA HOTAIR expression decreases the proliferation and invasion of glioma stem cells. Int J Oncol 49, 509–518 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  49. S.N. Min, T. Wei, X.T. Wang, L.L. Wu, G.Y. Yu, Clinicopathological and prognostic significance of homeobox transcript antisense RNA expression in various cancers: A meta-analysis. Medicine 96, e7084 (2017)

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Y.-W.L. Ming-Yi Lu, P.-Y. Chen, P.-L. Hsieh, C.-Y. Fang, C.-Y. Wu, M.-L. Yen, B.-Y. Peng, D.P. Wang, H.-C. Cheng, C.-Z. Wu, Y.-H. Shih, D.-J. Wang, C.-c. Yu, L.-L. Tsai, Targeting LncRNA HOTAIR suppresses cancer stemness and metastasis in oral carcinomas stem cells through modulation of EMT. Oncotarget 8, 98542–98552 (2017)

    PubMed  PubMed Central  Google Scholar 

  51. P.D. Marco Galasso, M. Previati, S. Sandhu, J. Palatini, V. Coppola, S. Warner, M.E. Sana, R. Zanella, R. Abujarour, C. Desponts, M.A. Teitell, R. Garzon, G. Calin, C.M. Croce, S. Volinia, A large scale expression study associates uc.283-plus lncRNA with pluripotent stem cells and human glioma. Genome Medicine 6, 76 (2014)

  52. G.S. Markopoulos, E. Roupakia, M. Tokamani, E. Chavdoula, M. Hatziapostolou, C. Polytarchou, K.B. Marcu, A.G. Papavassiliou, R. Sandaltzopoulos, E. Kolettas, A step-by-step microRNA guide to cancer development and metastasis. Cell Oncol 40, 303–339 (2017)

    CAS  Google Scholar 

  53. Y. Li, T. Mine, C.G. Ioannides, Short GC-rich RNA similar to miR 1909 and 1915 folds in silico with the 5'-UTR and ORF of notch and responders: Potential for the elimination of cancer stem cells. Oncol Rep 24, 1443–1453 (2010)

  54. A. Lujambio, A. Portela, J. Liz, S.A. Melo, S. Rossi, R. Spizzo, C.M. Croce, G.A. Calin, M. Esteller, CpG island hypermethylation-associated silencing of non-coding RNAs transcribed from ultraconserved regions in human cancer. Oncogene 29, 6390–6401 (2010)

    CAS  PubMed  PubMed Central  Google Scholar 

  55. S.-Y.L. Wei-Yu Chen, Y.-S. Chang, J.J. Yin, Hsiu-lien, T.H. Yeh, O.H. Mouhieddine, W. Abou-Kheir, Y.-N. Liu, MicroRNA-34a regulates WNT/TCF7 signaling and inhibits bone metastasis in Ras activated prostate cancer. Oncotarget 6, 441–457 (2014)

    PubMed Central  Google Scholar 

  56. P. Bu, K.Y. Chen, J.H. Chen, L. Wang, J. Walters, Y.J. Shin, J.P. Goerger, J. Sun, M. Witherspoon, N. Rakhilin, J. Li, H. Yang, J. Milsom, S. Lee, W. Zipfel, M.M. Jin, Z.H. Gumus, S.M. Lipkin, X. Shen, A microRNA miR-34a-regulated bimodal switch targets notch in colon cancer stem cells. Cell Stem Cell 12, 602–615 (2013)

    CAS  PubMed  PubMed Central  Google Scholar 

  57. U.S.B. Sumithra, A.B. Das, Alternative splicing within the Wnt signaling pathway: Role in cancer development. Cell Oncol 39, 1–13 (2016)

    CAS  Google Scholar 

  58. L. Wang, P. Bu, Y. Ai, T. Srinivasan, H.J. Chen, K. Xiang, S.M. Lipkin, X. Shen, A long non-coding RNA targets microRNA miR-34a to regulate colon cancer stem cell asymmetric division. elife 5, e14620 (2016)

    PubMed  PubMed Central  Google Scholar 

  59. J. Wu, J. Zhang, B. Shen, K. Yin, J. Xu, W. Gao, L. Zhang, Long noncoding RNA lncTCF7, induced by IL-6/STAT3 transactivation, promotes hepatocellular carcinoma aggressiveness through epithelial-mesenchymal transition. J Exp Clin Cancer Res 34, 116 (2015)

    PubMed  PubMed Central  Google Scholar 

  60. S. Wan, E. Zhao, I. Kryczek, L. Vatan, A. Sadovskaya, G. Ludema, D.M. Simeone, W. Zou, T.H. Welling, Tumor-associated macrophages produce interleukin 6 and signal via STAT3 to promote expansion of human hepatocellular carcinoma stem cells. Gastroenterology 147, 1393–1404 (2014)

    CAS  PubMed  PubMed Central  Google Scholar 

  61. R. Bharti, G. Dey, M. Mandal, Cancer development, chemoresistance, epithelial to mesenchymal transition and stem cells: A snapshot of IL-6 mediated involvement. Cancer Lett 375, 51–61 (2016)

    CAS  PubMed  Google Scholar 

  62. Y. Wang, L. He, Y. Du, P. Zhu, G. Huang, J. Luo, X. Yan, B. Ye, C. Li, P. Xia, G. Zhang, Y. Tian, R. Chen, Z. Fan, The long noncoding RNA lncTCF7 promotes self-renewal of human liver cancer stem cells through activation of Wnt signaling. Cell Stem Cell 16, 413–425 (2015)

    CAS  PubMed  Google Scholar 

  63. J. Wu, D. Wang, Long noncoding RNA TCF7 promotes invasiveness and self-renewal of human non-small cell lung cancer cells. Hum Cell 30, 23–29 (2017)

    CAS  PubMed  Google Scholar 

  64. P. Massoner, T. Thomm, B. Mack, G. Untergasser, A. Martowicz, K. Bobowski, H. Klocker, O. Gires, M. Puhr, EpCAM is overexpressed in local and metastatic prostate cancer, suppressed by chemotherapy and modulated by MET-associated miRNA-200c/205. Br J Cancer 111, 955–964 (2014)

    CAS  PubMed  PubMed Central  Google Scholar 

  65. C.C. Poirier F, P.M. Timmons, E.J. Robertson, M.J. Evans, P.W. Rigby, The murine H19 gene is activated during embryonic stem cell differentiation in vitro and at the time of implantation in the developing embryo. Development 113, 1105–1114 (1991)

  66. F. Peng, T.T. Li, K.L. Wang, G.Q. Xiao, J.H. Wang, H.D. Zhao, Z.J. Kang, W.J. Fan, L.L. Zhu, M. Li, B. Cui, F.M. Zheng, H.J. Wang, E.W. Lam, B. Wang, J. Xu, Q. Liu, H19/let-7/LIN28 reciprocal negative regulatory circuit promotes breast cancer stem cell maintenance. Cell Death Dis 8, e2569 (2017)

    CAS  PubMed  PubMed Central  Google Scholar 

  67. H. Bauderlique-Le Roy, C. Vennin, G. Brocqueville, N. Spruyt, E. Adriaenssens, R.P. Bourette, Enrichment of human stem-like prostate cells with s-SHIP promoter activity uncovers a role in Stemness for the long noncoding RNA H19. Stem Cells Dev 24, 1252–1262 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  68. X. Jiang, Y. Yan, M. Hu, X. Chen, Y. Wang, Y. Dai, D. Wu, Y. Wang, Z. Zhuang, H. Xia, Increased level of H19 long noncoding RNA promotes invasion, angiogenesis, and stemness of glioblastoma cells. J Neurosurg 124, 129–136 (2016)

    CAS  PubMed  Google Scholar 

  69. S.R. Viswanathan, G.Q. Daley, Lin28: A microRNA regulator with a macro role. Cell 140, 445–449 (2010)

    CAS  PubMed  Google Scholar 

  70. X. Cai, B.R. Cullen, The imprinted H19 noncoding RNA is a primary microRNA precursor. RNA 13, 313–316 (2007)

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Y. Zheng, X. Lu, L. Xu, Z. Chen, Q. Li, J. Yuan, MicroRNA-675 promotes glioma cell proliferation and motility by negatively regulating retinoblastoma 1. Hum Pathol 69, 63–71 (2017)

    CAS  PubMed  Google Scholar 

  72. A. Farzi-Molan, S. Babashah, B. Bakhshinejad, A. Atashi, M. Fakhr Taha, Down-regulation of the non-coding RNA H19 and its derived miR-675 is concomitant with up-regulation of insulin-like growth factor receptor type 1 during neural-like differentiation of human bone marrow mesenchymal stem cells. Cell Biol Int 42, 940–448 (2018)

    CAS  PubMed  Google Scholar 

  73. B.K. Dey, K. Pfeifer, A. Dutta, The H19 long noncoding RNA gives rise to microRNAs miR-675-3p and miR-675-5p to promote skeletal muscle differentiation and regeneration. Genes Dev 28, 491–501 (2014)

    PubMed  PubMed Central  Google Scholar 

  74. A. Keniry, D. Oxley, P. Monnier, M. Kyba, L. Dandolo, G. Smits, W. Reik, The H19 lincRNA is a developmental reservoir of miR-675 that suppresses growth and Igf1r. Nat Cell Biol 14, 659–665 (2012)

    CAS  PubMed  PubMed Central  Google Scholar 

  75. N. Liu, L. Zhong, J. Zeng, X. Zhang, Q. Yang, D. Liao, Y. Wang, G. Chen, Y. Wang, Upregulation of microRNA-200a associates with tumor proliferation, CSCs phenotype and chemosensitivity in ovarian cancer. Neoplasma 62, 550–559 (2015)

    CAS  PubMed  Google Scholar 

  76. C. Liu, R. Liu, D. Zhang, Q. Deng, B. Liu, H.P. Chao, K. Rycaj, Y. Takata, K. Lin, Y. Lu, Y. Zhong, J. Krolewski, J. Shen, D.G. Tang, MicroRNA-141 suppresses prostate cancer stem cells and metastasis by targeting a cohort of pro-metastasis genes. Nat Commun 8, 14270 (2017)

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Q. Yang, X. Wang, C. Tang, X. Chen, J. He, H19 promotes the migration and invasion of colon cancer by sponging miR-138 to upregulate the expression of HMGA1. Int J Oncol 50, 1801–1809 (2017)

    CAS  PubMed  Google Scholar 

  78. W.-M.F. Wei-Cheng Liang, C.-W. Wong, Y. Wang, G.-X.H.W. Wei-Mao, L. Zhang, L.-J. Xiao, D.C.-C. Wan, Jin-Fang, M.M.-Y.W. Zhang, The lncRNA H19 promotes epithelial to mesenchymal transition by functioning as miRNA sponges in colorectal cancer. Oncotarget 6, 22513–22525 (2015)

    PubMed  PubMed Central  Google Scholar 

  79. S. Cufi, A. Vazquez-Martin, C. Oliveras-Ferraros, B. Martin-Castillo, J. Joven, J.A. Menendez, Metformin against TGFbeta-induced epithelial-to-mesenchymal transition (EMT): From cancer stem cells to aging-associated fibrosis. Cell Cycle 9, 4461–4468 (2010)

    CAS  PubMed  Google Scholar 

  80. J.H. Yuan, F. Yang, F. Wang, J.Z. Ma, Y.J. Guo, Q.F. Tao, F. Liu, W. Pan, T.T. Wang, C.C. Zhou, S.B. Wang, Y.Z. Wang, Y. Yang, N. Yang, W.P. Zhou, G.S. Yang, S.H. Sun, A long noncoding RNA activated by TGF-beta promotes the invasion-metastasis cascade in hepatocellular carcinoma. Cancer Cell 25, 666–681 (2014)

    CAS  PubMed  Google Scholar 

  81. W. Li, Y. Kang, A new Lnc in metastasis: Long noncoding RNA mediates the prometastatic functions of TGF-beta. Cancer Cell 25, 557–559 (2014)

    CAS  PubMed  PubMed Central  Google Scholar 

  82. E. Karamitopoulou, Tumor budding cells, cancer stem cells and epithelial-mesenchymal transition-type cells in pancreatic cancer. Front Oncol 2, 209 (2012)

    PubMed  Google Scholar 

  83. U. Wellner, J. Schubert, U.C. Burk, O. Schmalhofer, F. Zhu, A. Sonntag, B. Waldvogel, C. Vannier, D. Darling, A. zur Hausen, V.G. Brunton, J. Morton, O. Sansom, J. Schuler, M.P. Stemmler, C. Herzberger, U. Hopt, T. Keck, S. Brabletz, T. Brabletz, The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 11, 1487–1495 (2009)

    CAS  PubMed  Google Scholar 

  84. L.-J.W. Sheng-Jia Shi, B. Yu, Y.-H. Li, Y. Jin, X.-Z. Bai, LncRNA-ATB promotes trastuzumab resistance and invasion metastasis cascade in breast cancer. Oncotarget 6, 11652–11663 (2015)

    PubMed  PubMed Central  Google Scholar 

  85. C. Mehner, E. Miller, D. Khauv, A. Nassar, A.L. Oberg, W.R. Bamlet, L. Zhang, J. Waldmann, E.S. Radisky, H.C. Crawford, D.C. Radisky, Tumor cell-derived MMP3 orchestrates Rac1b and tissue alterations that promote pancreatic adenocarcinoma. Mol Cancer Res 12, 1430–1439 (2014)

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Y. Gao, Z. Zhang, K. Li, L. Gong, Q. Yang, X. Huang, C. Hong, M. Ding, H. Yang, Linc-DYNC2H1-4 promotes EMT and CSC phenotypes by acting as a sponge of miR-145 in pancreatic cancer cells. Cell Death Dis 8, e2924 (2017)

    CAS  PubMed  PubMed Central  Google Scholar 

  87. T. Han, X.P. Yi, B. Liu, M.J. Ke, Y.X. Li, MicroRNA-145 suppresses cell proliferation, invasion and migration in pancreatic cancer cells by targeting NEDD9. Mol Med Rep 11, 4115–4120 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Z. Li, X. Zhao, Y. Zhou, Y. Liu, Q. Zhou, H. Ye, Y. Wang, J. Zeng, Y. Song, W. Gao, S. Zheng, B. Zhuang, H. Chen, W. Li, H. Li, H. Li, Z. Fu, R. Chen, The long non-coding RNA HOTTIP promotes progression and gemcitabine resistance by regulating HOXA13 in pancreatic cancer. J Transl Med 13, 84 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Z. Fu, C. Chen, Q. Zhou, Y. Wang, Y. Zhao, X. Zhao, W. Li, S. Zheng, H. Ye, L. Wang, Z. He, Q. Lin, Z. Li, R. Chen, LncRNA HOTTIP modulates cancer stem cell properties in human pancreatic cancer by regulating HOXA9. Cancer Lett 410, 68–81 (2017)

    CAS  PubMed  Google Scholar 

  90. L. Quagliata, M.S. Matter, S. Piscuoglio, L. Arabi, C. Ruiz, A. Procino, M. Kovac, F. Moretti, Z. Makowska, T. Boldanova, J.B. Andersen, M. Hammerle, L. Tornillo, M.H. Heim, S. Diederichs, C. Cillo, L.M. Terracciano, Long noncoding RNA HOTTIP/HOXA13 expression is associated with disease progression and predicts outcome in hepatocellular carcinoma patients. Hepatology 59, 911–923 (2014)

    CAS  PubMed  PubMed Central  Google Scholar 

  91. C.R. Cochrane, A. Szczepny, D.N. Watkins, J.E. Cain, Hedgehog signaling in the maintenance of Cancer stem cells. Cancers (Basel) 7, 1554–1585 (2015)

    CAS  Google Scholar 

  92. M. Zhou, Y. Hou, G. Yang, H. Zhang, G. Tu, Y.E. Du, S. Wen, L. Xu, X. Tang, S. Tang, L. Yang, X. Cui, M. Liu, LncRNA-Hh strengthen Cancer stem cells generation in Twist-positive breast Cancer via activation of hedgehog signaling pathway. Stem Cells 34, 55–66 (2016)

    CAS  PubMed  Google Scholar 

  93. L. Qu, J. Ding, C. Chen, Z. J. Wu, B. Liu, Y. Gao, W. Chen, F. Liu, W. Sun, X.F. Li, X. Wang, Y. Wang, Z.Y. Xu, L. Gao, Q. Yang, B. Xu, Y.M. Li, Z.Y. Fang, Z.P. Xu, Y. Bao, D.S. Wu, X. Miao, H.Y. Sun, Y.H. Sun, H.Y. Wang and L.H. Wang, Exosome-transmitted lncARSR promotes Sunitinib resistance in renal Cancer by acting as a competing endogenous RNA. Cancer Cell 29, 653–668 (2016)

    CAS  PubMed  Google Scholar 

  94. Y. Li, Y. Ye, B. Feng, Y. Qi, Long Noncoding RNA lncARSR promotes doxorubicin resistance in hepatocellular carcinoma via modulating PTEN-PI3K/Akt pathway. J Cell Biochem 118, 4498–4507 (2017)

    CAS  PubMed  Google Scholar 

  95. L. Qu, Z. Wu, Y. Li, Z. Xu, B. Liu, F. Liu, Y. Bao, D. Wu, J. Liu, A. Wang, X. Chu, Y. Sun, C. Chen, Z. Zhang, L. Wang, A feed-forward loop between lncARSR and YAP activity promotes expansion of renal tumour-initiating cells. Nat Commun 7, 12692 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  96. C.M. Loewer, M. Guttman, Y.H. Loh, K. Thomas, I.H. Park, M. Garber, M. Curran, T. Onder, S. Agarwal, P.D. Manos, S. Datta, E.S. Lander, T.M. Schlaeger, G.Q. Daley, J.L. Rinn, Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nat Genet 42, 1113–1117 (2010)

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Y. Pan, C. Li, J. Chen, K. Zhang, X. Chu, R. Wang, L. Chen, The emerging roles of long noncoding RNA ROR (lincRNA-ROR) and its possible mechanisms in human cancers. Cell Physiol Biochem 40, 219–229 (2016)

    CAS  PubMed  Google Scholar 

  98. P. Hou, Y. Zhao, Z. Li, R. Yao, M. Ma, Y. Gao, L. Zhao, Y. Zhang, B. Huang, J. Lu, LincRNA-ROR induces epithelial-to-mesenchymal transition and contributes to breast cancer tumorigenesis and metastasis. Cell Death Dis 5, e1287 (2014)

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Y. Pan, et al., Long noncoding RNA ROR regulates chemoresistance in docetaxelresistant lung adenocarcinoma cells via epithelial mesenchymal transition pathway. Oncotarget 20, 33144–33158 (2017)

  100. Y. Lou, H. Jiang, Z. Cui, L. Wang, X. Wang, T. Tian, Linc-ROR induces epithelial-to-mesenchymal transition in ovarian cancer by increasing Wnt/β-catenin signaling. Oncotarget 8, 69983–69994 (2017)

    PubMed  PubMed Central  Google Scholar 

  101. F. Xia, Y. Xiong, Q. Li, Interaction of lincRNA ROR and p53/miR-145 correlates with lung cancer stem cell signatures. J Cell Biochem 1 (2017)

  102. Z. Fu, G. Li, Z. Li, Y. Wang, Y. Zhao, S. Zheng, H. Ye, Y. Luo, X. Zhao, L. Wei, Y. Liu, Q. Lin, Q. Zhou, R. Chen, Endogenous miRNA sponge LincRNA-ROR promotes proliferation, invasion and stem cell-like phenotype of pancreatic cancer cells. Cell Death Discov 3, 17004 (2017)

    CAS  PubMed  PubMed Central  Google Scholar 

  103. S. Wang, F. Liu, J. Deng, X. Cai, J. Han, Q. Liu, Long noncoding RNA ROR regulates proliferation, invasion, and Stemness of gastric Cancer stem cell. Cell Reprogram 18, 319–326 (2016)

    CAS  PubMed  Google Scholar 

  104. X. Zhou, Q. Gao, J. Wang, X. Zhang, K. Liu, Z. Duan, Linc-RNA-RoR acts as "sponge" against mediation of the differentiation of endometrial cancer stem cells by microRNA-145. Gynecol Oncol 133, 333–339 (2014)

    CAS  PubMed  Google Scholar 

  105. S. Chen, S. Nagel, B. Schneider, H. Dai, R. Geffers, M. Kaufmann, C. Meyer, C. Pommerenke, K.S. Thress, J. Li, H. Quentmeier, H.G. Drexler, R.A.F. MacLeod, A new ETV6-NTRK3 cell line model reveals MALAT1 as a novel therapeutic target - a short report. Cell Oncol 41, 93–101 (2018)

    CAS  Google Scholar 

  106. F. Jiao, H. Hu, T. Han, C. Yuan, L. Wang, Z. Jin, Z. Guo, L. Wang, Long noncoding RNA MALAT-1 enhances stem cell-like phenotypes in pancreatic cancer cells. Int J Mol Sci 16, 6677–6693 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  107. L. Zeng, Y. Cen, J. Chen, Long non-coding RNA MALAT-1 contributes to maintenance of stem cell-like phenotypes in breast cancer cells. Oncol Lett 15, 2117–2122 (2017)

    PubMed  PubMed Central  Google Scholar 

  108. Y. Han, L. Zhou, T. Wu, Y. Huang, Z. Cheng, X. Li, T. Sun, Y. Zhou, Z. Du, Downregulation of lncRNA-MALAT1 affects proliferation and the expression of Stemness markers in glioma stem cell line SHG139S. Cell Mol Neurobiol 36, 1097–1107 (2016)

    CAS  PubMed  Google Scholar 

  109. M. Wu, Z. Lin, X. Li, X. Xin, J. An, Q. Zheng, Y. Yang, D. Lu, HULC cooperates with MALAT1 to aggravate liver cancer stem cells growth through telomere repeat-binding factor 2. Sci Rep 6, 36045 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  110. F. Jiao, H. Hu, C. Yuan, L. Wang, W. Jiang, Z. Jin, Z. Guo, L. Wang, Elevated expression level of long noncoding RNA MALAT-1 facilitates cell growth, migration and invasion in pancreatic cancer. Oncol Rep 32, 2485–2492 (2014)

    CAS  PubMed  Google Scholar 

  111. Y. Fan, B. Shen, M. Tan, X. Mu, Y. Qin, F. Zhang, Y. Liu, Long non-coding RNA UCA1 increases chemoresistance of bladder cancer cells by regulating Wnt signaling. FEBS J 281, 1750–1758 (2014)

    CAS  PubMed  Google Scholar 

  112. M. Jiang, O. Huang, Z. Xie, S. Wu, X. Zhang, A. Shen, H. Liu, X. Chen, J. Wu, Y. Lou, Y. Mao, K. Sun, S. Hu, M. Geng, K. Shen, A novel long non-coding RNA-ARA: Adriamycin resistance-associated. Biochem Pharmacol 87, 254–283 (2014)

    CAS  PubMed  Google Scholar 

  113. W.P. Tsang, T.W. Wong, A.H. Cheung, C.N. Co, T.T. Kwok, Induction of drug resistance and transformation in human cancer cells by the noncoding RNA CUDR. RNA 13, 890–898 (2007)

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Q. Zheng, Z. Lin, X. Li, X. Xin, M. Wu, J. An, X. Gui, T. Li, H. Pu, H. Li, D. Lu, Inflammatory cytokine IL6 cooperates with CUDR to aggravate hepatocyte-like stem cells malignant transformation through NF-kappaB signaling. Sci Rep 6, 36843 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  115. X. Gui, H. Li, T. Li, H. Pu, D. Lu, Long noncoding RNA CUDR regulates HULC and beta-catenin to govern human liver stem cell malignant differentiation. Mol Ther 23, 1843–1853 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  116. T. Li, Q. Zheng, J. An, M. Wu, H. Li, X. Gui, H. Pu, D. Lu, SET1A cooperates with CUDR to promote liver Cancer growth and hepatocyte-like stem cell malignant transformation epigenetically. Mol Ther 24, 261–275 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  117. F. Wang, H.-Q. Ying, B.-S. He, Y.-Q. Pan, Q.-W. Deng, H.-L. Sun, J. Chen, X. Liu, S.-K. Wang, Upregulated lncRNA-UCA1 contributes to progression of hepatocellular carcinoma through inhibition of miR-216b and activation of FGFR1/ERK signaling pathway. Oncotarget 6, 7899–7917 (2015)

    PubMed  PubMed Central  Google Scholar 

  118. Q.Z.H. Pu, H. Li, M. Wu, J. An, X. Gui, T. Li, D. Lu, CUDR promotes liver cancer stem cell growth through upregulating TERT and C-Myc. Oncotarget 6, 40775–40798 (2015)

    PubMed  PubMed Central  Google Scholar 

  119. X. Wang, W. Sun, W. Shen, M. Xia, C. Chen, D. Xiang, B. Ning, X. Cui, H. Li, X. Li, J. Ding, H. Wang, Long non-coding RNA DILC regulates liver cancer stem cells via IL-6/STAT3 axis. J Hepatol 64, 1283–1294 (2016)

    CAS  PubMed  Google Scholar 

  120. V. Plaks, N. Kong, Z. Werb, The cancer stem cell niche: How essential is the niche in regulating stemness of tumor cells? Cell Stem Cell 16, 225–238 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  121. M. Prieto-Vila, R.U. Takahashi, W. Usuba, I. Kohama, T. Ochiya, Drug resistance driven by Cancer stem cells and their niche. Int J Mol Sci 18, e2574 (2017)

    PubMed  Google Scholar 

  122. L.T.H. Phi, I.N. Sari, Y.G. Yang, S.H. Lee, N. Jun, K.S. Kim, Y.K. Lee, H.Y. Kwon, Cancer stem cells (CSCs) in drug resistance and their therapeutic implications in Cancer treatment. Stem Cells Int 5416923, 2018 (2018)

    Google Scholar 

  123. S. Lee, H.H. Seo, C.Y. Lee, J. Lee, S. Shin, S.W. Kim, S. Lim, K.C. Hwang, Human long noncoding RNA regulation of stem cell potency and differentiation. Stem Cells Int 6374504, 2017 (2017)

    Google Scholar 

  124. A.M. Schmitt, H.Y. Chang, Long noncoding RNAs in Cancer pathways. Cancer Cell 29, 452–463 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  125. A.C.P. Ioannis Grammatikakis, K. Abdelmohsen, M. Gorospe, Long noncoding RNAs (lncRNAs) and the molecular hallmarks of aging. Aging 6, 992–1009 (2014)

    PubMed  PubMed Central  Google Scholar 

  126. Y.T. Liting Yang, F. Xiong, H. Yi, F. Wei, S. Zhang, B.X. Can Guo, M. Zhou, N. Xie, X. Li, Y. Li, G. Li, W.X.Z. Zeng, LncRNAs regulate cancer metastasis via binding to functional proteins. Oncotarget 9, 1426–1443 (2018)

    PubMed  Google Scholar 

  127. A. Bhan, M. Soleimani, S.S. Mandal, Long noncoding RNA and Cancer: A new paradigm. Cancer Res 77, 3965–3981 (2017)

    CAS  PubMed  Google Scholar 

  128. A. Sahu, U. Singhal, A.M. Chinnaiyan, Long noncoding RNAs in cancer: From function to translation. Trends Cancer 1, 93–109 (2015)

    PubMed  PubMed Central  Google Scholar 

  129. T. Shi, G. Gao, Y. Cao, Long noncoding RNAs as novel biomarkers have a promising future in Cancer diagnostics. Dis Markers 2016, 9085195 (2016)

    PubMed  PubMed Central  Google Scholar 

  130. e.a. Qin-nan Chen, Long non-coding RNAs in anti-cancer drug resistance. Oncotarget 8, 1925–1936 (2017)

    Google Scholar 

  131. J.R. Evans, F.Y. Feng, A.M. Chinnaiyan, The bright side of dark matter: lncRNAs in cancer. J Clin Invest 126, 2775–2782 (2016)

    PubMed  PubMed Central  Google Scholar 

  132. L. Cheng, H. Ming, M. Zhu, B. Wen, Long noncoding RNAs as organizers of nuclear architecture. Sci China Life Sci 59, 236–244 (2016)

    CAS  PubMed  Google Scholar 

  133. B.M. Boman, M.S. Wicha, J.Z. Fields, O.A. Runquist, Symmetric division of cancer stem cells--a key mechanism in tumor growth that should be targeted in future therapeutic approaches. Clin Pharmacol Ther 81, 893–898 (2007)

    CAS  PubMed  Google Scholar 

  134. L. Landskron, V. Steinmann, F. Bonnay, T.R. Burkard, J. Steinmann, I. Reichardt, H. Harzer, A.S. Laurenson, H. Reichert, J.A. Knoblich, The asymmetrically segregating lncRNA cherub is required for transforming stem cells into malignant cells. elife 7 (2018)

  135. M.S. Beg, A.J. Brenner, J. Sachdev, M. Borad, Y.K. Kang, J. Stoudemire, S. Smith, A.G. Bader, S. Kim, D.S. Hong, Phase I study of MRX34, a liposomal miR-34a mimic, administered twice weekly in patients with advanced solid tumors. Investig New Drugs 35, 180–188 (2017)

    CAS  Google Scholar 

  136. M. Al-Hajj, M.S. Wicha, A. Benito-Hernandez, S.J. Morrison, M.F. Clarke, Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100, 3983–3988 (2003)

    CAS  PubMed  PubMed Central  Google Scholar 

  137. H. Fan, J.H. Zhu, X.Q. Yao, Knockdown of long noncoding RNA PVT1 reverses multidrug resistance in colorectal cancer cells. Mol Med Rep 17, 8309–8315 (2018)

    CAS  PubMed  PubMed Central  Google Scholar 

  138. Z. Bian, L. Jin, J. Zhang, Y. Yin, C. Quan, Y. Hu, Y. Feng, H. Liu, B. Fei, Y. Mao, L. Zhou, X. Qi, S. Huang, D. Hua, C. Xing, Z. Huang, LncRNA-UCA1 enhances cell proliferation and 5-fluorouracil resistance in colorectal cancer by inhibiting miR-204-5p. Sci Rep 6, 23892 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  139. K. Takahashi, I.K. Yan, T. Kogure, H. Haga, T. Patel, Extracellular vesicle-mediated transfer of long non-coding RNA ROR modulates chemosensitivity in human hepatocellular cancer. FEBS Open Bio 4, 458–467 (2014)

    CAS  PubMed  PubMed Central  Google Scholar 

  140. M. Rasool, A. Malik, S. Zahid, M.A. Basit Ashraf, M.H. Qazi, M. Asif, A. Zaheer, M. Arshad, A. Raza, M.S. Jamal, Non-coding RNAs in cancer diagnosis and therapy. Non-coding RNA Research 1, 69–76 (2016)

    PubMed  PubMed Central  Google Scholar 

  141. M.M. Ali, V.S. Akhade, S.T. Kosalai, S. Subhash, L. Statello, M. Meryet-Figuiere, J. Abrahamsson, T. Mondal, C. Kanduri, PAN-cancer analysis of S-phase enriched lncRNAs identifies oncogenic drivers and biomarkers. Nat Commun 9, 883 (2018)

    PubMed  PubMed Central  Google Scholar 

  142. H.S. Chiu, S. Somvanshi, E. Patel, T.W. Chen, V.P. Singh, B. Zorman, S.L. Patil, Y. Pan, S.S. Chatterjee, N. Cancer Genome Atlas Research, A.K. Sood, P.H. Gunaratne, P. Sumazin, Pan-Cancer analysis of lncRNA regulation supports their targeting of Cancer genes in each tumor context. Cell Rep e212, 297–312 (2018)

    Google Scholar 

Download references

Acknowledgments

We thank graphic designer Cristina Oropeza Ramírez for her excellent contribution.

Author information

Authors and Affiliations

  1. Epigenetics, Instituto Nacional de Medicina Genomica, Periferico Sur No.4809, Col Arenal Tepepan, Tlalpan, 14610, Mexico City, Mexico

    Rosario Castro-Oropeza, Vilma Maldonado & Karla Vazquez-Santillan

  2. Functional Genomics Laboratories, Instituto Nacional de Medicina Genomica, Periferico Sur No.4809, Col Arenal Tepepan, Tlalpan, 14610, Mexico City, Mexico

    Jorge Melendez-Zajgla

  3. National Institute of Genomic Medicine, Mexico City, Mexico

    Karla Vazquez-Santillan

Authors
  1. Rosario Castro-Oropeza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jorge Melendez-Zajgla
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vilma Maldonado
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Karla Vazquez-Santillan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Karla Vazquez-Santillan.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Castro-Oropeza, R., Melendez-Zajgla, J., Maldonado, V. et al. The emerging role of lncRNAs in the regulation of cancer stem cells. Cell Oncol. 41, 585–603 (2018). https://doi.org/10.1007/s13402-018-0406-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13402-018-0406-4

Keywords

Search

Navigation