nach oben

Cellular Oncology

Erschienen in:

14.09.2018 | Review

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

verfasst von: Rosario Castro-Oropeza, Jorge Melendez-Zajgla, Vilma Maldonado, Karla Vazquez-Santillan

Erschienen in: Cellular Oncology | Ausgabe 6/2018

Einloggen, um Zugang zu erhalten

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.

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)PubMedPubMedCentral

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

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)PubMedPubMedCentral

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

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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

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

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

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)PubMed

11.

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

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)PubMedPubMedCentral

13.

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

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)

16.

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

17.

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

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)PubMedPubMedCentral

19.

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

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)PubMed

21.

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

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)PubMed

23.

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

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)PubMedPubMedCentral

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)

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)

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)PubMed

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)

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)

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)PubMedPubMedCentral

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)PubMed

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)PubMedPubMedCentral

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)PubMed

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)PubMedPubMedCentral

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)PubMed

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)PubMed

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)PubMed

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)PubMedPubMedCentral

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)PubMed

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)PubMedPubMedCentral

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)PubMed

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)

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)

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)PubMedPubMedCentral

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

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)

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)PubMedPubMedCentral

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)PubMedCentral

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)PubMedPubMedCentral

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)

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMed

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)PubMed

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)PubMed

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMed

69.

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

70.

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

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)PubMed

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)PubMed

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMed

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)PubMedPubMedCentral

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)PubMed

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)PubMedPubMedCentral

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)PubMed

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)PubMed

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)PubMedPubMedCentral

82.

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

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)PubMed

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMed

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)PubMedPubMedCentral

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)

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)PubMed

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)PubMed

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)PubMed

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMed

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMed

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)PubMed

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)

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMed

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)PubMedPubMedCentral

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)PubMed

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)PubMed

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)PubMed

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMed

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)PubMedPubMedCentral

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

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)

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)

124.

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

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)PubMedPubMedCentral

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

127.

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

128.

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

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)PubMedPubMedCentral

130.

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

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)PubMedPubMedCentral

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)PubMed

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)PubMed

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)

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)PubMedPubMedCentral

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)

Titel: The emerging role of lncRNAs in the regulation of cancer stem cells
verfasst von: Rosario Castro-Oropeza
Jorge Melendez-Zajgla
Vilma Maldonado
Karla Vazquez-Santillan
Publikationsdatum: 14.09.2018
Verlag: Springer Netherlands
Erschienen in: Cellular Oncology / Ausgabe 6/2018
Print ISSN: 2211-3428
Elektronische ISSN: 2211-3436
DOI: https://doi.org/10.1007/s13402-018-0406-4

Neu im Fachgebiet Pathologie

01.04.2024 | Forensische Traumatologie | CME

Live-Webinar: Aktuelle Leitlinien bei Herz-Kreislauf-Erkrankungen

Springer Medizin

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

Abstract

Background

Conclusions

Neu im Fachgebiet Pathologie

Theoretische Grundlagen von Explosionen und Explosionsverletzungen

Auswirkungen vorgeschalteter Laborprozesse auf die Digitalisierung histologischer Schnittpräparate

Knochenmarkhistologie bei Zytopenien

Herausforderungen der Automation bei der quantitativen Auswertung von Leberbiopsien

Live-Webinar: Aktuelle Leitlinien bei Herz-Kreislauf-Erkrankungen

Springer Medizin

Abstract

Background

Conclusions

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 6/2018

Induction of apoptosis via proteasome inhibition in leukemia/lymphoma cells by two potent piperidones

Emerging ways to treat breast cancer: will promises be met?

Drug-induced expression of EpCAM contributes to therapy resistance in esophageal adenocarcinoma

Epigenetic markers in basal cell carcinoma: universal themes in oncogenesis and tumor stratification? - a short report

In silico screening for ERα down modulators identifies thioridazine as an anti-proliferative agent in primary, 4OH-tamoxifen-resistant and Y537S ERα-expressing breast cancer cells

Anti-tumor effect of CDK inhibitors on CDKN2A-defective squamous cell lung cancer cells

Neu im Fachgebiet Pathologie

Theoretische Grundlagen von Explosionen und Explosionsverletzungen

Auswirkungen vorgeschalteter Laborprozesse auf die Digitalisierung histologischer Schnittpräparate

Knochenmarkhistologie bei Zytopenien

Herausforderungen der Automation bei der quantitativen Auswertung von Leberbiopsien