The Role of Autophagy and lncRNAs in the Maintenance of Cancer Stem Cells
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, přehledy
PubMed
33799834
PubMed Central
PMC7998932
DOI
10.3390/cancers13061239
PII: cancers13061239
Knihovny.cz E-zdroje
- Klíčová slova
- LncRNAs, autophagy, cancer stem cells (CSCs), haematological malignancies, solid cancers, tumour microenvironment,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Cancer stem cells (CSCs) possess properties such as self-renewal, resistance to apoptotic cues, quiescence, and DNA-damage repair capacity. Moreover, CSCs strongly influence the tumour microenvironment (TME) and may account for cancer progression, recurrence, and relapse. CSCs represent a distinct subpopulation in tumours and the detection, characterisation, and understanding of the regulatory landscape and cellular processes that govern their maintenance may pave the way to improving prognosis, selective targeted therapy, and therapy outcomes. In this review, we have discussed the characteristics of CSCs identified in various cancer types and the role of autophagy and long noncoding RNAs (lncRNAs) in maintaining the homeostasis of CSCs. Further, we have discussed methods to detect CSCs and strategies for treatment and relapse, taking into account the requirement to inhibit CSC growth and survival within the complex backdrop of cellular processes, microenvironmental interactions, and regulatory networks associated with cancer. Finally, we critique the computationally reinforced triangle of factors inclusive of CSC properties, the process of autophagy, and lncRNA and their associated networks with respect to hypoxia, epithelial-to-mesenchymal transition (EMT), and signalling pathways.
Central European Institute of Technology Masaryk University 625 00 Brno Czech Republic
Department of Functional Genomics GlaxoSmithKline Stevenage SG1 2NY UK
Department of Life Sciences Birmingham City University Birmingham B15 3TN UK
Department of Neurology Massachusetts General Hospital Harvard Medical School Boston MA 02114 USA
Mammalian Genetics Unit Medical Research Council Harwell Institute Oxfordshire OX110RD UK
MRC Health Data Research Midlands University of Birmingham Birmingham B15 2TT UK
NIHR Biomedical Research Centre Birmingham B15 2TT UK
NIHR Experimental Cancer Medicine Centre Birmingham B15 2TT UK
NIHR Surgical Reconstruction and Microbiology Research Centre Birmingham B15 2TT UK
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Yap T.A., Futreal P.A., Pusztai L., Swanton C., Gerlinger M. Intratumor heterogeneity: Seeing the wood for the trees. Sci. Transl. Med. 2012;4:127ps10. doi: 10.1126/scitranslmed.3003854. PubMed DOI
Greaves M., Maley C.C. Clonal evolution in Cancer. Nature. 2012;481:306–313. doi: 10.1038/nature10762. PubMed DOI PMC
Gupta P.B., Fillmore C.M., Jiang G., Shapira S.D., Tao K., Kuperwasser C., Lander E.S. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell. 2011;146:633–644. doi: 10.1016/j.cell.2011.07.026. PubMed DOI
Nguyen L.V., Vanner R., Dirks P., Eaves C.J. Cancer stem cells: An evolving concept. Nat. Rev. Cancer. 2012;12:133–143. doi: 10.1038/nrc3184. PubMed DOI
Beck B., Blanpain C. Unravelling cancer stem cell potential. Nat. Rev. Cancer. 2013;13:727–738. doi: 10.1038/nrc3597. PubMed DOI
Allan A.L., Vantyghem S.A., Tuck A.B., Chambers A.F. Tumor dormancy and cancer stem cells: Implications for the biology and treatment of breast cancer metastasis. Breast Dis. 2006;26:87–98. doi: 10.3233/BD-2007-26108. PubMed DOI
Cho R.W., Clarke M.F. Recent advances in cancer stem cells. Curr. Opin. Genet. Dev. 2008;18:48–53. doi: 10.1016/j.gde.2008.01.017. PubMed DOI
Shiozawa Y., Berry J.E., Eber M.R., Jung Y., Yumoto K., Cackowski F.C., Yoon H.J., Parsana P., Mehra R., Wang J., et al. The marrow niche controls the cancer stem cell phenotype of disseminated prostate. Cancer Oncotarget. 2016;7:41217–41232. doi: 10.18632/oncotarget.9251. PubMed DOI PMC
Diehn M., Cho R.W., Lobo N.A., Kalisky T., Dorie M.J., Kulp A.N., Qian D., Lam J.S., Ailles L.E., Wong M., et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature. 2009;458:780–783. doi: 10.1038/nature07733. PubMed DOI PMC
Huntly B.J., Gilliland D.G. Leukaemia stem cells and the evolution of cancer-stem-cell research. Nat. Rev. Cancer. 2005;4:311–321. doi: 10.1038/nrc1592. PubMed DOI
Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., Dewhirst M.W., Bigner D.D., Rich J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756–760. doi: 10.1038/nature05236. PubMed DOI
Barker N., Ridgway R.A., van Es J.H., van de Wetering M., Begthel H., van den Born M., Danenberg E., Clarke A.R., Sansom O.J., Clevers H. Crypt stem cells as the cells-of-origin of intestinal Cancer. Nature. 2009;457:608–611. doi: 10.1038/nature07602. PubMed DOI
Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. PNAS. 2003;100:3983–3988. doi: 10.1073/pnas.0530291100. PubMed DOI PMC
Clarke M.F., Dick J.E., Dirks P.B., Eaves C.J., Jamieson C.H., Jones D.L., Visvader J., Weissman I.L., Wahl G.M. Cancer stem cells–perspectives on current status and future directions: AACR workshop on cancer stem cells. Cancer Res. 2006;66:9339–9344. doi: 10.1158/0008-5472.CAN-06-3126. PubMed DOI
Dean M., Fojo T., Bates S. Tumour stem cells and drug resistance. Nat. Rev. Cancer. 2005;5:275–284. doi: 10.1038/nrc1590. PubMed DOI
Visvader J.E., Lindeman G.J. Cancer stem cells in solid tumours: Accumulating evidence and unresolved questions. Nat. Rev. Cancer. 2008;8:755–768. doi: 10.1038/nrc2499. PubMed DOI
Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 1997;3:730–737. doi: 10.1038/nm0797-730. PubMed DOI
Bruttel V.S., Wischhusen J. Cancer stem cell immunology: Key to understanding tumorigenesis and tumor immune escape? Front. Immunol. 2014;5:360. doi: 10.3389/fimmu.2014.00360. PubMed DOI PMC
Vallette F.M., Olivier C., Lézot F., Oliver L., Cochonneau D., Lalier L., Cartron P.F., Heymann D. Dormant, quiescent, tolerant and persister cells: Four synonyms for the same target in Cancer. Biochem. Pharmacol. 2019;162:169–176. doi: 10.1016/j.bcp.2018.11.004. PubMed DOI
Rycaj K., Tang D.G. Cell-of-Origin of Cancer versus Cancer Stem Cells: Assays and Interpretations. Cancer Res. 2015;75:4003–4011. doi: 10.1158/0008-5472.CAN-15-0798. PubMed DOI PMC
Quintana E., Shackleton M., Sabel M.S., Fullen D.R., Johnson T.M., Morrison S.J. Efficient tumour formation by single human melanoma cells. Nature. 2008;456:593–598. doi: 10.1038/nature07567. PubMed DOI PMC
Tang D.G. Understanding cancer stem cell heterogeneity and plasticity. Cell. 2012;22:457–472. doi: 10.1038/cr.2012.13. PubMed DOI PMC
Eades G., Zhang Y.S., Li Q.L., Xia J.X., Yao Y., Zhou Q. Long non-coding RNAs in stem cells and Cancer. World J. Clin. Oncol. 2014;5:134–141. doi: 10.5306/wjco.v5.i2.134. PubMed DOI PMC
Wang Y., He L., Du Y., Zhu P., Huang G., Luo J., Yan X., Ye B., Li C., Xia P., et al. The long noncoding RNA lncTCF7 promotes self-renewal of human liver cancer stem cells through activation of Wnt signaling. Cell Stem Cell. 2015;16:413–425. doi: 10.1016/j.stem.2015.03.003. PubMed DOI
Castro-Oropeza R., Melendez-Zajgla J., Maldonado V., Vazquez-Santillan K. The emerging role of lncRNAs in the regulation of cancer stem cells. Cell Oncol. 2018;41:585–603. doi: 10.1007/s13402-018-0406-4. PubMed DOI
Lecerf C., Le Bourhis X., Adriaenssens E. The long non-coding RNA H19: An active player with multiple facets to sustain the hallmarks of Cancer. Cell Mol. Life Sci. 2019;76:4673–4687. doi: 10.1007/s00018-019-03240-z. PubMed DOI PMC
Zaarour R.F., Azakir B., Hajam E.Y., Nawafleh H., Zeinelabdin N.A., Engelsen A.S.T., Thiery J., Jamora C., Chouaib S. Role of Hypoxia-Mediated Autophagy in Tumor Cell Death and Survival. Cancers. 2021;13:503. doi: 10.3390/cancers13030533. PubMed DOI PMC
Hanekamp D., Cloos J., Schuurhuis G.J. Leukemic stem cells: Identification and clinical application. Int. J. Hematol. 2017;105:549–557. doi: 10.1007/s12185-017-2221-5. PubMed DOI
Dick J.E. Acute myeloid leukemia stem cells. Ann. N. Y. Acad. Sci. 2005;1044:1–5. doi: 10.1196/annals.1349.001. PubMed DOI
Terpstra W., Prins A., Ploemacher R.E., Wognum B.W., Wagemaker G., Löwenberg B., Wielenga J.J. Long-term leukemia-initiating capacity of a CD34− subpopulation of acute myeloid leukemia. Blood. 1996;87:2187–2194. doi: 10.1182/blood.V87.6.2187.bloodjournal8762187. PubMed DOI
Piao L., Yang Z., Jin J., Ni W., Qi W., Xuan Y. B7H4 is associated with stemness and cancer progression in esophageal squamous cell carcinoma. Hum. Pathol. 2018;80:152–162. doi: 10.1016/j.humpath.2018.05.021. PubMed DOI
Yang Z., Ni W., Cui C., Qi W., Piao L., Xuan Y. Identification of LETM1 as a marker of cancer stem-like cells and predictor of poor prognosis in esophageal squamous cell carcinoma. Hum. Pathol. 2018;81:148–156. doi: 10.1016/j.humpath.2018.07.001. PubMed DOI
Ogawa T., Hirohashi Y., Murai A., Nishidate T., Okita K., Wang L., Ikehara Y., Satoyoshi T., Usui A., Kubo T., et al. ST6GALNAC1 plays important roles in enhancing cancer stem phenotypes of colorectal cancer via the Akt pathway. Oncotarget. 2017;8:112550–112564. doi: 10.18632/oncotarget.22545. PubMed DOI PMC
Xue Z., Yan H., Li J., Liang S., Cai X., Chen X., Wu Q., Gao L., Wu K., Nie Y., et al. Identification of cancer stem cells in vincristine preconditioned SGC7901 gastric cancer cell line. J. Cell Biochem. 2012;113:302–312. doi: 10.1002/jcb.23356. PubMed DOI
Zhu Z., Xu J., Li L., Ye W., Xu G., Chen B., Zeng J., Li J., Huang Z. Effect of gastric cancer stem cell on gastric cancer invasion, migration and angiogenesis. Int. J. Med. Sci. 2020;17:2040–2051. doi: 10.7150/ijms.46774. PubMed DOI PMC
Li C., Heidt D.G., Dalerba P., Burant C.F., Zhang L., Adsay V., Wicha M., Clarke M.F., Simeone D.M. Identification of pancreatic cancer stem cells. Cancer Res. 2007;67:1030–1037. doi: 10.1158/0008-5472.CAN-06-2030. PubMed DOI
Hermann P.C., Huber S.L., Herrler T., Aicher A., Ellwart J.W., Guba M., Bruns C.J., Heeschen C. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic Cancer. Cell Stem Cell. 2007;1:313–323. doi: 10.1016/j.stem.2007.06.002. PubMed DOI
Yamashita T., Wang X.W. Cancer stem cells in the development of liver Cancer. J. Clin. Invest. 2013;123:1911–1918. doi: 10.1172/JCI66024. PubMed DOI PMC
Masciale V., Grisendi G., Banchelli F., D’Amico R., Maiorana A., Sighinolfi P., Stefani A., Morandi U., Dominici M., Aramini B. Isolation and Identification of Cancer Stem-Like Cells in Adenocarcinoma and Squamous Cell Carcinoma of the Lung: A Pilot Study. Bd. 9. Front. Oncol. 2019;s:1394. doi: 10.3389/fonc.2019.01394. PubMed DOI PMC
Herreros-Pomares A., De-Maya-Girones J.D., Calabuig-Fariñas S., Lucas R., Martínez A., Pardo-Sánchez J.M., Alonso S., Blasco A., Guijarro R., Martorell M., et al. Lung tumorspheres reveal cancer stem cell-like properties and a score with prognostic impact in resected non-small-cell lung. Cancer Cell Death Dis. 2019;10:660. doi: 10.1038/s41419-019-1898-1. PubMed DOI PMC
Wang J., Sakariassen P.Ø., Tsinkalovsky O., Immervoll H., Bøe S.O., Svendsen A., Prestegarden L., Røsland G., Thorsen F., Stuhr L., et al. CD133 negative glioma cells form tumors in nude rats and give rise to CD133 positive cells. Int. J. Cancer. 2008;122:761–768. doi: 10.1002/ijc.23130. PubMed DOI
Bradshaw A., Wickremesekera A., Brasch H.D., Chibnall A.M., Davis P.F., Tan S.T., Itinteang T. Cancer Stem Cells in Glioblastoma Multiforme. Front. Surg. 2016;348:48. doi: 10.3389/fsurg.2016.00048. PubMed DOI PMC
Basu-Roy U., Seo E., Ramanathapuram L., Rapp T.B., Perry J.A., Orkin S.H., Mansukhani A., Basilico C. Sox2 maintains self renewal of tumor-initiating cells in osteosarcomas. Oncogene. 2012;31:2270–2282. doi: 10.1038/onc.2011.405. PubMed DOI PMC
Moreira M.P., da Conceição Braga L., Silva L.M. STAT3 as a promising chemoresistance biomarker associated with the CD44+/high/CD24-/low/ALDH+ BCSCs-like subset of the triple-negative breast cancer (TNBC) cell line. Exp. Cell Res. 2018;363:283–290. doi: 10.1016/j.yexcr.2018.01.018. PubMed DOI
Golebiewska A., Brons N.H., Bjerkvig R., Niclou S.P. Critical appraisal of the side population assay in stem cell and cancer stem cell research. Cell Stem Cell. 2011;8:136–147. doi: 10.1016/j.stem.2011.01.007. PubMed DOI
Murase M., Kano M., Tsukahara T., Takahashi A., Torigoe T., Kawaguchi S., Kimura S., Wada T., Uchihashi Y., Kondo T., et al. Side population cells have the characteristics of cancer stem-like cells/cancer-initiating cells in bone sarcomas. Br. J. Cancer. 2009;101:1425–1432. doi: 10.1038/sj.bjc.6605330. PubMed DOI PMC
Tomita H., Tanaka K., Tanaka T., Hara A. Aldehyde dehydrogenase 1A1 in stem cells and Cancer. Oncotarget. 2016;7:11018–11032. doi: 10.18632/oncotarget.6920. PubMed DOI PMC
Xu X., Chai S., Wang P., Zhang C., Yang Y., Yang Y., Wang K. Aldehyde dehydrogenases and cancer stem cells. Cancer Lett. 2015;369:50–57. doi: 10.1016/j.canlet.2015.08.018. PubMed DOI
Somervaille T.C., Cleary M.L. Identification and characterization of leukemia stem cells in murine MLL-AF9 acute myeloid leukemia. Cancer Cell. 2006;10:257–268. doi: 10.1016/j.ccr.2006.08.020. PubMed DOI
Liu L., Cheung T.H., Charville G.W., Hurgo B.M., Leavitt T., Shih J., Brunet A., Rando T.A. Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging. Cell Rep. 2013;4:189–204. doi: 10.1016/j.celrep.2013.05.043. PubMed DOI PMC
Sreepadmanabh M., Toley B.J. Investigations into the cancer stem cell niche using in-vitro 3-D tumor models and microfluidics. Biotechnol. Adv. 2018;36:1094–1110. doi: 10.1016/j.biotechadv.2018.03.009. PubMed DOI
LaBarbera D.V., Reid B.G., Yoo B.H. The multicellular tumor spheroid model for high-throughput cancer drug discovery. Expert Opin. Drug. Discov. 2012;7:819–883. doi: 10.1517/17460441.2012.708334. PubMed DOI
Forde S., Matthews J.D., Jahangiri L., Lee L.C., Prokoph N., Malcolm T.I., Giger O.T., Bell N., Blair H., O’Marcaigh A., et al. Paediatric Burkitt lymphoma patient-derived xenografts capture disease characteristics over time and are a model for therapy. Br. J. Haematol. 2021;192:354–365. doi: 10.1111/bjh.17043. PubMed DOI
Dalerba P., Cho R.W., Clarke M.F. Cancer stem cells: Models and concepts. Annu. Rev. Med. 2007;58:267–284. doi: 10.1146/annurev.med.58.062105.204854. PubMed DOI
Islam F., Gopalan V., Wahab R., Smith R.A., Lam A.K. Cancer stem cells in oesophageal squamous cell carcinoma: Identification, prognostic and treatment perspectives. Crit. Rev. Oncol. Hematol. 2015;96:9–19. doi: 10.1016/j.critrevonc.2015.04.007. PubMed DOI
Tang K.H., Dai Y.D., Tong M., Chan Y.P., Kwanm P.S., Fu L., Qin Y.R., Tsao S.W., Lung H.L., Lung M.L., et al. A CD90(+) tumor-initiating cell population with an aggressive signature and metastatic capacity in esophageal Cancer. Cancer Res. 2013;73:2322–2332. doi: 10.1158/0008-5472.CAN-12-2991. PubMed DOI
Liu C.C., Chou K.T., Hsu J.W., Lin J.H., Hsu T.W., Yen D.H., Hung S.C., Hsu H.S. High metabolic rate and stem cell characteristics of esophageal cancer stem-like cells depend on the Hsp27-AKT-HK2 pathway. Int. J. Cancer. 2019;145:2144–2156. doi: 10.1002/ijc.32301. PubMed DOI
Taniguchi H., Moriya C., Igarashi H., Saitoh A., Yamamoto H., Adachi Y., Imai K. Cancer stem cells in human gastrointestinal Cancer. Cancer Sci. 2016;107:1556–1562. doi: 10.1111/cas.13069. PubMed DOI PMC
Munro M.J., Wickremesekera S.K., Peng L., Tan S.T., Itinteang T. Cancer stem cells in colorectal cancer: A review. J. Clin. Pathol. 2018;71:110–116. doi: 10.1136/jclinpath-2017-204739. PubMed DOI
Ricci-Vitiani L., Lombardi D.G., Pilozzi E., Biffoni M., Todaro M., Peschle C., De Maria R. Identification and expansion of human colon-cancer-initiating cells. Nature. 2007;445:111–115. doi: 10.1038/nature05384. PubMed DOI
Clark P.A., Iida M., Treisman D.M., Kalluri H., Ezhilan S., Zorniak M., Wheeler D.L., Kuo J.S. Activation of multiple ERBB family receptors mediates glioblastoma cancer stem-like cell resistance to EGFR-targeted inhibition. Neoplasia. 2012;14:420–428. doi: 10.1596/neo.12432. PubMed DOI PMC
Kang T.W., Choi S.W., Yang S.R., Shin T.H., Kim H.S., Yu K.R., Hong I.S., Ro S., Cho J.M., Kang K.S. Growth arrest and forced differentiation of human primary glioblastoma multiforme by a novel small molecule. Sci. Rep. 2014;4:5546. doi: 10.1038/srep05546. PubMed DOI PMC
Cheray M., Bessette B., Lacroix A., Mélin C., Jawhari S., Pinet S., Deluche E., Clavère P., Durand K., Sanchez-Prieto R., et al. KLRC3, a Natural Killer receptor gene, is a key factor involved in glioblastoma tumourigenesis and aggressiveness. J. Cell Mol. Med. 2017;21:244–253. doi: 10.1111/jcmm.12960. PubMed DOI PMC
Wang H.H., Liao C.C., Chow N.H., Huang L.L., Chuang J.I., Wei K.C., Shin J.W. Whether CD44 is an applicable marker for glioma stem cells. Am. J. Transl. Res. 2017;9:4785–4806. PubMed PMC
Yang M., Yan M., Zhang R., Li J., Luo Z. Side population cells isolated from human osteosarcoma are enriched with tumor-initiating cells. Cancer Sci. 2011;102:1774. doi: 10.1111/j.1349-7006.2011.02028.x. PubMed DOI PMC
Maurizi G., Verma N., Gadi A., Mansukhani A., Basilico C. Sox2 is required for tumor development and cancer cell proliferation in osteosarcoma. Oncogene August. 2018;37:4626–4632. doi: 10.1038/s41388-018-0292-2. PubMed DOI PMC
Deter R.L., De Duve C. Influence of glucagon, an inducer of cellular autophagy, on some physical properties of rat liver lysosomes. J. Cell Biol. 1967;33:437–449. doi: 10.1083/jcb.33.2.437. PubMed DOI PMC
Wang C., Wang X. The interplay between autophagy and the ubiquitin-proteasome system in cardiac proteotoxicity. Biochim. Biophys. Acta. 2015;1852:188–194. doi: 10.1016/j.bbadis.2014.07.028. PubMed DOI PMC
Lilienbaum A. Relationship between the proteasomal system and autophagy. Int. J. Biochem. Mol. Biol. 2013;4:1–26. PubMed PMC
Russell R.C., Yuan H.X., Guan K.L. Autophagy regulation by nutrient signaling. Cell Res. 2014;24:42–57. doi: 10.1038/cr.2013.166. PubMed DOI PMC
Fulda S., Gorman A.M., Hori O., Samali A. Cellular stress responses: Cell survival and cell death. Int. J. Cell Biol. 2010;2010:214074. doi: 10.1155/2010/214074. PubMed DOI PMC
Mari M., Tooze S.A., Reggiori F. The puzzling origin of the autophagosomal membrane. F1000 Biol. Rep. 2011;3:25. doi: 10.3410/B3-25. PubMed DOI PMC
Klionsky D.J., Cuervo A.M., Seglen P.O. Methods for monitoring autophagy from yeast to human. Autophagy. 2007;3:181–206. doi: 10.4161/auto.3678. PubMed DOI
Tooze S.A., Yoshimori T. The origin of the autophagosomal membrane. Nat. Cell Biol. 2010;12:831–835. doi: 10.1038/ncb0910-831. PubMed DOI
Roberts R., Ktistakis N.T. Omegasomes: PI3P platforms that manufacture autophagosomes. Essays Biochem. 2013;55:17–27. PubMed
Esclatine A., Chaumorcel M., Codogno P. Macroautophagy signaling and regulation. Curr. Top. Microbiol. Immunol. 2009;335:33–70. PubMed
Eskelinen E.L., Saftig P. Autophagy: A lysosomal degradation pathway with a central role in health and disease. Biochim. Biophys. Acta. 2009;1793:664–673. doi: 10.1016/j.bbamcr.2008.07.014. PubMed DOI
Mizushima N. Autophagy: Process and function. Genes Dev. 2007;21:2861–2873. doi: 10.1101/gad.1599207. PubMed DOI
Monastyrska I., Rieter E., Klionsky D.J., Reggiori F. Multiple roles of the cytoskeleton in autophagy. Biol. Rev. Camb. Philos. Soc. 2009;84:431–448. doi: 10.1111/j.1469-185X.2009.00082.x. PubMed DOI PMC
Smith A.G., Macleod K.F. Autophagy, cancer stem cells and drug resistance. J. Pathol. 2019;247:708–718. doi: 10.1002/path.5222. PubMed DOI PMC
Praharaj P.P., Panigrahi D.P., Bhol C.S., Patra S., Mishra S.R., Mahapatra K.K., Behera B.P., Singh A., Patil S., Bhutia S.K. Mitochondrial rewiring through mitophagy and mitochondrial biogenesis in cancer stem cells: A potential target for anti-CSC cancer therapy. Cancer Lett. 2021;498:217–228. doi: 10.1016/j.canlet.2020.10.036. PubMed DOI
Van Doeselaar S., Burgering B.M.T. FOXOs Maintaining the Equilibrium for Better or for Worse. Curr. Top. Dev. Biol. 2018;127:49–103. PubMed
Barzilay R., Melamed E., Offen D. Introducing Transcription Factors to Multipotent Mesenchymal Stem Cells: Making Transdifferentiation Possible. Stem Cells. 2009;27:2509–2515. doi: 10.1002/stem.172. PubMed DOI
Peng Q., Qin J., Zhang Y., Cheng X., Wang X., Lu W., Xie X., Zhang S. Autophagy maintains the stemness of ovarian cancer stem cells by FOXA2. J. Exp. Clin. Cancer Res. 2017;36:171. doi: 10.1186/s13046-017-0644-8. PubMed DOI PMC
Cufí S., Vazquez-Martin A., Oliveras-Ferraros C., Martin-Castillo B., Vellon L., Menendez J.A. Autophagy positively regulates the CD44(+) CD24(-/low) breast cancer stem-like phenotype. Cell Cycle. 2011;10:3871–3885. doi: 10.4161/cc.10.22.17976. PubMed DOI
Galavotti S., Bartesaghi S., Faccenda D., Shaked-Rabi M., Sanzone S., McEvoy A., Dinsdale D., Condorelli F., Brandner S., Campanella M., et al. The autophagy-associated factors DRAM1 and p62 regulate cell migration and invasion in glioblastoma stem cells. Oncogene. 2013;32:699–712. doi: 10.1038/onc.2012.111. PubMed DOI
Kiyono K., Suzuki H.I., Matsuyama H., Morishita Y., Komuro A., Kano M.R., Sugimoto K., Miyazono K. Autophagy is activated by TGF-beta and potentiates TGF-beta-mediated growth inhibition in human hepatocellular carcinoma cells. Cancer Res. 2009;69:8844–8852. doi: 10.1158/0008-5472.CAN-08-4401. PubMed DOI
Morel A.P., Lièvre M., Thomas C., Hinkal G., Ansieau S., Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS ONE. 2008;3:e2888. doi: 10.1371/journal.pone.0002888. PubMed DOI PMC
Courtois S., Haykal M., Bodineau C., Sifré E., Azzi-Martin L., Ménard A., Mégraud F., Lehours P., Durán R.V., Varon C., et al. Autophagy induced by Helicobacter pylori infection is necessary for gastric cancer stem cell emergence. Gastric. Cancer. 2021;24:133–144. doi: 10.1007/s10120-020-01118-9. PubMed DOI
Flynn A.B., Schiemann W.P. Autophagy in breast cancer metastatic dormancy: Tumor suppressing or tumor promoting functions? J. Cancer Metastasis Treat. 2019;5:43. PubMed PMC
Chaterjee M., van Golen K.L. Breast cancer stem cells survive periods of farnesyl-transferase inhibitor-induced dormancy by undergoing autophagy. Bone Marrow Res. 2011;2011:362938. doi: 10.1155/2011/362938. PubMed DOI PMC
Gong C., Bauvy C., Tonelli G., Yue W., Deloménie C., Nicolas V., Zhu Y., Domergue V., Marin-Esteban V., Tharinger H., et al. Beclin 1 and autophagy are required for the tumorigenicity of breast cancer stem-like/progenitor cells. Oncogene. 2013;32:2261–2272. doi: 10.1038/onc.2012.252. PubMed DOI PMC
Maycotte P., Jones K.L., Goodall M.L., Thorburn J., Thorburn A. Autophagy Supports Breast Cancer Stem Cell Maintenance by Regulating IL6 Secretion. Mol. Cancer Res. 2015;13:651–658. doi: 10.1158/1541-7786.MCR-14-0487. PubMed DOI PMC
Ojha R., Bhattacharyya S., Singh S.K. Autophagy in Cancer Stem Cells: A Potential Link Between Chemoresistance, Recurrence, and Metastasis. Biores. Open Access. 2015;4:97–108. doi: 10.1089/biores.2014.0035. PubMed DOI PMC
Mele L., del Vecchio V., Liccardo D., Prisco C., Schwerdtfeger M., Robinson N., Desiderio V., Tirino V., Papaccio G., La Noce M. The role of autophagy in resistance to targeted therapies. Cancer Treat Rev. 2020;88:102043. doi: 10.1016/j.ctrv.2020.102043. PubMed DOI
Golden E.B., Cho H.Y., Jahanian A., Hofman F.M., Louie S.G., Schönthal A.H., Chen T.C. Chloroquine enhances temozolomide cytotoxicity in malignant gliomas by blocking autophagy. Neurosurg. Focus. 2014;37:E12. doi: 10.3171/2014.9.FOCUS14504. PubMed DOI
Li L.-Q., Pan D., Zhang S.-W., Xie D.-Y., Zheng X.-L., Chen H. Autophagy regulates chemoresistance of gastric cancer stem cells via the Notch signaling pathway. Eur. Rev. Med. Pharmacol. Sci. 2018;22:3402–3407. PubMed
Fu Y., Chang H., Peng X., Bai Q., Yi L., Zhou Y., Zhu J., Mi M. Resveratrol inhibits breast cancer stem-like cells and induces autophagy via suppressing Wnt/β-catenin signaling pathway. PLoS ONE. 2014;9:e102535. doi: 10.1371/journal.pone.0102535. PubMed DOI PMC
Rahman M.A., Saha S.K., Rahman M.S., Uddin M.J., Uddin M.S., Pang M.-G., Rhim H., Cho S.G. Molecular Insights Into Therapeutic Potential of Autophagy Modulation by Natural Products for Cancer Stem Cells. Front. Cell Dev. Biol. 2020;8:283. doi: 10.3389/fcell.2020.00283. PubMed DOI PMC
Mandhair H.K., Arambasic M., Novak U., Radpour R. Molecular modulation of autophagy: New venture to target resistant cancer stem cells. World J. Stem Cells. 2020;12:303–322. doi: 10.4252/wjsc.v12.i5.303. PubMed DOI PMC
Baquero P., Dawson A., Mukhopadhyay A., Kuntz E.M., Mitchell R., Olivares O., Ianniciello A., Scott M.T., Dunn K., Nicastri M.C., et al. Targeting quiescent leukemic stem cells using second generation autophagy inhibitors. Leukemia. 2019;33:981–994. doi: 10.1038/s41375-018-0252-4. PubMed DOI PMC
Terry S., Faouzi Zaarour R., Hassan Venkatesh G., Francis A., El-Sayed W., Buart S., Bravo P., Thiery J., Chouaib S. Role of Hypoxic Stress in Regulating Tumor Immunogenicity, Resistance and Plasticity. Int. J. Mol. Sci. 2018;19:3044. doi: 10.3390/ijms19103044. PubMed DOI PMC
Tong W., Tong G., Liu Y. Cancer stem cells and hypoxia-inducible factors (Review) Int. J. Oncol. 2018;53:469–476. doi: 10.3892/ijo.2018.4417. PubMed DOI
Semenza G.L. Dynamic regulation of stem cell specification and maintenance by hypoxia-inducible factors. Mol. Aspects Med. 2016;47:15–23. doi: 10.1016/j.mam.2015.09.004. PubMed DOI
Yang M., Wu M., Chiou S., Chen P., Chang S., Liu C., Teng S., Wu K. Direct regulation of TWIST by HIF-1α promotes metastasis. Nat. Cell Biol. 2008;10:295–305. doi: 10.1038/ncb1691. PubMed DOI
Nakuluri K., Mukhi D., Nishad R., Saleem M.A., Mungamuri S.K., Menon R.K., Pasupulati A.K. Hypoxia induces ZEB2 in podocytes: Implications in the pathogenesis of proteinuria. J. Cell Physiol. 2019;234:6503–6518. doi: 10.1002/jcp.27387. PubMed DOI
Xu X., Tan X., Tampe B., Sanchez E., Zeisberg M., Zeisberg E.M. ducible Factor 1α (HIF1α) in Hypoxia-induced Endothelial to Mesenchymal Transition of Human Coronary Endothelial Cells. J. Biol. Chem. 2015;290:16653–16664. doi: 10.1074/jbc.M115.636944. PubMed DOI PMC
Bellot G., Garcia-Medina R., Gounon P., Chiche J., Roux D., Pouysségur J., Mazure N.M. Hypoxia-Induced Autophagy Is Mediated through Hypoxia-Inducible Factor Induction of BNIP3 and BNIP3L via Their BH3 Domains. Mol. Cell Biol. 2009;29:2570–2581. doi: 10.1128/MCB.00166-09. PubMed DOI PMC
Hasmim M., Janji B., Khaled M., Noman M.Z., Louache F., Bordereaux D., Abderamane A., Baud V., Mami-Chouaib F., Chouaib S. Cutting Edge: NANOG Activates Autophagy under Hypoxic Stress by Binding to BNIP3L Promoter. J. Immunol. 2017;198:1423–1428. doi: 10.4049/jimmunol.1600981. PubMed DOI
Zhu H., Wang D., Liu Y., Su Z., Zhang L., Chen F., Zhou Y., Wu Y., Yu M., Zhang Z., et al. Role of the Hypoxia-inducible factor-1 alpha induced autophagy in the conversion of non-stem pancreatic cancer cells into CD133+ pancreatic cancer stem-like cells. Cancer Cell Int. 2013;13:119. doi: 10.1186/1475-2867-13-119. PubMed DOI PMC
Qureshi-Baig K., Kuhn D., Viry E., Pozdeev V.I., Schmitz M., Rodriguez F., Ullmann P., Koncina E., Nurmik M., Frasquilho S., et al. Hypoxia-induced autophagy drives colorectal cancer initiation and progression by activating the PRKC/PKC-EZR (ezrin) pathway. Autophagy. 2020;16:1436–1452. doi: 10.1080/15548627.2019.1687213. PubMed DOI PMC
Yuan N., Song L., Zhang S., Lin W., Cao Y., Xu F., Fang Y., Wang Z., Zhang H., Li X., et al. Bafilomycin A1 targets both autophagy and apoptosis pathways in pediatric B-cell acute lymphoblastic leukemia. Haematologica. 2015;100:345–356. doi: 10.3324/haematol.2014.113324. PubMed DOI PMC
Wouters B., Koritzinsky M. Hypoxia signalling through mTOR and the unfolded protein response in Cancer. Nat. Rev. Cancer. 2008;8:851–864. doi: 10.1038/nrc2501. PubMed DOI
Land S.C., Tee A.R. Hypoxia-inducible Factor 1α Is Regulated by the Mammalian Target of Rapamycin (mTOR) via an mTOR Signaling Motif. J. Biol. Chem. 2007;282:20534–20543. doi: 10.1074/jbc.M611782200. PubMed DOI
Agani F., Jiang B.H. Oxygen-independent Regulation of HIF-1: Novel Involvement of PI3K/ AKT/mTOR Pathway in Cancer Bd. 13. Curr. Cancer Drug Targets. 2013;3:245–251. doi: 10.2174/1568009611313030003. PubMed DOI
Losuwannarak N., Maiuthed A., Kitkumthorn N., Leelahavanichkul A., Roytrakul S., Chanvorachote P. Gigantol Targets Cancer Stem Cells and Destabilizes Tumors via the Suppression of the PI3K/AKT and JAK/STAT Pathways in Ectopic Lung Cancer Xenografts. Cancers. 2019;11:2032. doi: 10.3390/cancers11122032. PubMed DOI PMC
Li X., Liu X., Xu Y., Liu J., Xie M., Ni W., Chen S. KLF5 promotes hypoxia-induced survival and inhibits apoptosis in non-small cell lung cancer cells via HIF-1α. Int. J. Oncol. 2014;45:1507–1514. doi: 10.3892/ijo.2014.2544. PubMed DOI
Gong T., Cui L., Wang H., Wang H., Han N. Knockdown of KLF5 suppresses hypoxia-induced resistance to cisplatin in NSCLC cells by regulating HIF-1α-dependent glycolysis through inactivation of the PI3K/Akt/mTOR pathway. J. Transl. Med. 2018;16:164. doi: 10.1186/s12967-018-1543-2. PubMed DOI PMC
Nazio F., Bordi M., Cianfanelli F., Cecconi F. Autophagy and cancer stem cells: Molecular mechanisms and therapeutic applications. Cell Death Differ. 2019;26:690–702. doi: 10.1038/s41418-019-0292-y. PubMed DOI PMC
Ding W.X., Yin X.M. Mitophagy: Mechanisms, pathophysiological roles, and analysis. Biol. Chem. 2012;393:547–564. doi: 10.1515/hsz-2012-0119. PubMed DOI PMC
Pickles S., Vigié P., Youle R.J. Mitophagy and Quality Control Mechanisms in Mitochondrial Maintenance. Curr. Biol. 2018;28:R170–R185. doi: 10.1016/j.cub.2018.01.004. PubMed DOI PMC
Jin S.M., Youle R.J. PINK1- and Parkin-mediated mitophagy at a glance. J. Cell Sci. 2012;125:795–799. doi: 10.1242/jcs.093849. PubMed DOI PMC
Peiris-Pagès M., Martinez-Outschoorn U.E., Pestell R.G., Sotgia F., Lisanti M.P. Cancer stem cell metabolism. Breast Cancer Res. 2016;18:55. doi: 10.1186/s13058-016-0712-6. PubMed DOI PMC
Peixoto J., Lima J. Metabolic traits of cancer stem cells. Dis. Model. Mech. 2018;11:dmm033464. doi: 10.1242/dmm.033464. PubMed DOI PMC
Lleonart M.E., Abad E., Graifer D., Lyakhovich A. Reactive Oxygen Species-Mediated Autophagy Defines the Fate of Cancer Stem Cells. Antioxid. Redox Signal. 2018;28:1066–1079. doi: 10.1089/ars.2017.7223. PubMed DOI
Held N.M., Houtkooper R.H. Mitochondrial quality control pathways as determinants of metabolic health. Bioessays. 2015;37:867–876. doi: 10.1002/bies.201500013. PubMed DOI PMC
Tanaka A., Cleland M.M., Xu S., Narendra D.P., Suen D.F., Karbowski M., Youle R.J. Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J. Cell Biol. 2010;191:1367–1380. doi: 10.1083/jcb.201007013. PubMed DOI PMC
Rambold A.S., Kostelecky B., Elia N., Lippincott-Schwartz J. Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. PNAS. 2011;108:10190–10195. doi: 10.1073/pnas.1107402108. PubMed DOI PMC
Xie Q., Wu Q., Horbinski C.M., Flavahan W.A., Yang K., Zhou W., Dombrowski S.M., Huang Z., Fang X., Shi Y., et al. Mitochondrial control by DRP1 in brain tumor initiating cells. Nat. Neurosci. 2015;18:501–510. doi: 10.1038/nn.3960. PubMed DOI PMC
Liu K., Lee J., Kim J.Y., Wang L., Tian Y., Chan S.T., Cho C., Machida K., Chen D., Ou J.J. Mitophagy Controls the Activities of Tumor Suppressor p53 to Regulate Hepatic Cancer Stem Cells. Mol. Cell. 2017;68:281–292. doi: 10.1016/j.molcel.2017.09.022. PubMed DOI PMC
Yan C., Luo L., Guo C.-Y., Goto S., Urata Y., Shao J.-H., Li T.-S. Doxorubicin-induced mitophagy contributes to drug resistance in cancer stem cells from HCT8 human colorectal cancer cells. Cancer Lett. 2017;388:34–42. doi: 10.1016/j.canlet.2016.11.018. PubMed DOI
Yan C., Li T.S. Dual Role of Mitophagy in Cancer Drug Resistance. Anticancer Res. 2018;38:617–621. PubMed
Zhou J., Li G., Zheng Y., Shen H.M., Hu X., Ming Q.L., Huang C., Li P., Gao N. A novel autophagy/mitophagy inhibitor liensinine sensitizes breast cancer cells to chemotherapy through DNM1L-mediated mitochondrial fission. Autophagy. 2015;11:1259–1279. doi: 10.1080/15548627.2015.1056970. PubMed DOI PMC
Pennisi E. Genomics. ENCODE project writes eulogy for junk DNA. Science. 2012;337:1159–1161. doi: 10.1126/science.337.6099.1159. PubMed DOI
Ponjavic J., Ponting C.P., Lunter G. Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs. Genome Res. 2007;17:556–565. doi: 10.1101/gr.6036807. PubMed DOI PMC
Xu Z., Liu C., Zhao Q., Lü J., Ding X., Luo A., He J., Wang G., Li Y., Cai Z., et al. Long non-coding RNA CCAT2 promotes oncogenesis in triple-negative breast cancer by regulating stemness of cancer cells. Pharmacol. Res. 2020;152:104628. doi: 10.1016/j.phrs.2020.104628. PubMed DOI
Wu J., Zhu P., Lu T., Du Y., Wang Y., He L., Ye B., Liu B., Yang L., Wang J., et al. The long non-coding RNA LncHDAC2 drives the self-renewal of liver cancer stem cells via activation of Hedgehog signaling. J. Hepatol. 2019;70:918–929. doi: 10.1016/j.jhep.2018.12.015. PubMed DOI
Crea F., Clermont P.L., Parolia A., Wang Y., Helgason C.D. The non-coding transcriptome as a dynamic regulator of cancer metastasis. Cancer Metastasis Rev. 2014;33:1–16. doi: 10.1007/s10555-013-9455-3. PubMed DOI PMC
Crea F., Venalainen E., Ci X., Cheng H., Pikor L., Parolia A., Xue H., Nur Saidy N.R., Lin D., Lam W., et al. The role of epigenetics and long noncoding RNA MIAT in neuroendocrine prostate. Cancer Epigenomics. 2016;8:721–731. doi: 10.2217/epi.16.6. PubMed DOI
Jiao F., Hu H., Han T., Yuan C., Wang L., Jin Z., Guo Z., Wang L. Long noncoding RNA MALAT-1 enhances stem cell-like phenotypes in pancreatic cancer cells. Int. J. Mol. Sci. 2015;16:6677–6693. doi: 10.3390/ijms16046677. PubMed DOI PMC
Peperstraete E., Lecerf C., Collette J., Vennin C., Raby L., Völkel P., Angrand P.O., Winter M., Bertucci F., Finetti P., et al. Enhancement of Breast Cancer Cell Aggressiveness by lncRNA H19 and its Mir-675 Derivative: Insight into Shared and Different Actions. Cancers. 2020;29:1730. doi: 10.3390/cancers12071730. PubMed DOI PMC
Dai D., Wang H., Zhu L., Jin H., Wang X. N6-methyladenosine links RNA metabolism to cancer progression. Cell Death Dis. 2018;9:124. doi: 10.1038/s41419-017-0129-x. PubMed DOI PMC
Siebenthall K.T., Miller C.P., Vierstra J.D., Mathieu J., Tretiakova M., Reynolds A., Sandstrom R., Rynes E., Haugen E., Johnson A., et al. Integrated epigenomic profiling reveals endogenous retrovirus reactivation in renal cell carcinoma. EBioMedicine. 2019;41:427–442. doi: 10.1016/j.ebiom.2019.01.063. PubMed DOI PMC
Yan H., Bu P. Non-coding RNAs in cancer stem cells. Cancer Lett. 2018;421:121–126. doi: 10.1016/j.canlet.2018.01.027. PubMed DOI
Huang R., Zhu L., Zhang Y. XIST lost induces ovarian cancer stem cells to acquire taxol resistance via a KMT2C-dependent way. Cancer Cell Int. 2020;20:436. doi: 10.1186/s12935-020-01500-8. PubMed DOI PMC
Zheng Q., Xu J., Lin Z., Lu Y., Xin X., Li X., Yang Y., Meng Q., Wang C., Xiong W., et al. Inflammatory factor receptor Toll-like receptor 4 controls telomeres through heterochromatin protein 1 isoforms in liver cancer stem cell. J. Cell Mol. Med. 2018;22:3246–3258. doi: 10.1111/jcmm.13606. PubMed DOI PMC
Li H., An J., Wu M., Zheng Q., Gui X., Li T., Pu H., Lu D. LncRNA HOTAIR promotes human liver cancer stem cell malignant growth through downregulation of SETD2. Oncotarget. 2015;6:27847–27864. doi: 10.18632/oncotarget.4443. PubMed DOI PMC
Li L., Dang Q., Xie H., Yang Z., He D., Liang L., Song W., Yeh S., Chang C. Correction: Infiltrating mast cells enhance prostate cancer invasion via altering LncRNA-HOTAIR/PRC2-androgen receptor (AR)-MMP9 signals and increased stem/progenitor cell population. Oncotarget. 2016;7:83828. doi: 10.18632/oncotarget.13912. PubMed DOI PMC
Sasaki N., Toyoda M., Yoshimura H., Matsuda Y., Arai T., Takubo K., Aida J., Ishiwata T. H19 long non-coding RNA contributes to sphere formation and invasion through regulation of CD24 and integrin expression in pancreatic cancer cells. Oncotarget. 2018;9:34719–34734. doi: 10.18632/oncotarget.26176. PubMed DOI PMC
Shima H., Kida K., Adachi S., Yamada A., Sugae S., Narui K., Miyagi Y., Nishi M., Ryo A., Murata S., et al. Lnc RNA H19 is associated with poor prognosis in breast cancer patients and promotes cancer stemness. Breast Cancer Res. Treat. 2018;170:507–516. doi: 10.1007/s10549-018-4793-z. PubMed DOI
Zhan Y., Chen Z., He S., Gong Y., He A., Li Y., Zhang L., Zhang X., Fang D., Li X., et al. Long non-coding RNA SOX2OT promotes the stemness phenotype of bladder cancer cells by modulating SOX2. Mol. Cancer. 2020;19:25. doi: 10.1186/s12943-020-1143-7. PubMed DOI PMC
Zheng A., Song X., Zhang L., Zhao L., Mao X., Wei M., Jin F. Long non-coding RNA LUCAT1/miR-5582-3p/TCF7L2 axis regulates breast cancer stemness via Wnt/β-catenin pathway. J. Exp. Clin. Cancer Res. 2019;38:305. doi: 10.1186/s13046-019-1315-8. PubMed DOI PMC
Pucci P., Rescigno P., Sumanasuriya S., de Bono J., Crea F. Hypoxia and Noncoding RNAs in Taxane Resistance. Trends Pharmacol. Sci. 2018;39:695–709. doi: 10.1016/j.tips.2018.05.002. PubMed DOI
Wang X., Sun W., Shen W., Xia M., Chen C., Xiang D., Ning B., Cui X., Li H., Li X., et al. Long non-coding RNA DILC regulates liver cancer stem cells via IL-6/STAT3 axis. J. Hepatol. 2016;64:1283–1294. doi: 10.1016/j.jhep.2016.01.019. PubMed DOI
Huang R., Nie W., Yao K., Chou J. Depletion of the lncRNA RP11-567G11.1 inhibits pancreatic cancer progression. Biomed. Pharmacother. 2019;112:108685. doi: 10.1016/j.biopha.2019.108685. PubMed DOI
Pucci P., Venalainen E., Alborelli I., Quagliata L., Hawkes C., Mather R., Romero I., Rigas S.H., Wang Y., Crea F. LncRNA HORAS5 promotes taxane resistance in castration-resistant prostate cancer via a BCL2A1-dependent mechanism. Epigenomics. 2020;12:1123–1138. doi: 10.2217/epi-2019-0316. PubMed DOI
Qiu G., Ma D., Li F., Sun D., Zeng Z. lnc-PKD2-2-3, identified by long non-coding RNA expression profiling, is associated with pejorative tumor features and poor prognosis, enhances cancer stemness and may serve as cancer stem-cell marker in cholangiocarcinoma. Int. J. Oncol. 2019;55:45–58. doi: 10.3892/ijo.2019.4798. PubMed DOI PMC
Bellmunt J., Eigl B.J., Senkus E., Loriot Y., Twardowski P., Castellano D., Blais N., Sridhar S.S., Sternberg C.N., Retz M., et al. Borealis-1: A randomized, first-line, placebo-controlled, phase II study evaluating apatorsen and chemotherapy for patients with advanced urothelial Cancer. Ann. Oncol. 2017;28:2481–2488. doi: 10.1093/annonc/mdx400. PubMed DOI
Chi K.N., Higano C.S., Blumenstein B., Ferrero J.M., Reeves J., Feyerabend S., Gravis G., Merseburger A.S., Stenzl A., Bergman A.M., et al. Custirsen in combination with docetaxel and prednisone for patients with metastatic castration-resistant prostate cancer (SYNERGY trial): A phase 3, multicentre, open-label, randomised trial. Lancet Oncol. 2017;18:473–485. doi: 10.1016/S1470-2045(17)30168-7. PubMed DOI
Chery J. RNA therapeutics: RNAi and antisense mechanisms and clinical applications. Postdoc J. 2016;4:35–50. doi: 10.14304/SURYA.JPR.V4N7.5. PubMed DOI PMC
Liang X.H., Sun H., Nichols J.G., Crooke S.T. RNase H1-Dependent Antisense Oligonucleotides Are Robustly Active in Directing RNA Cleavage in Both the Cytoplasm and the Nucleus. Mol. Ther. 2017;25:2075–2092. doi: 10.1016/j.ymthe.2017.06.002. PubMed DOI PMC
Wang W.T., Han C., Sun Y.M., Chen T.Q., Chen Y.Q. Noncoding RNAs in cancer therapy resistance and targeted drug development. J. Hematol. Oncol. 2019;12:55. doi: 10.1186/s13045-019-0748-z. PubMed DOI PMC
Shen X., Corey D.R. Chemistry, mechanism and clinical status of antisense oligonucleotides and duplex RNAs. Nucleic Acids Res. 2018;46:1584–1600. doi: 10.1093/nar/gkx1239. PubMed DOI PMC
Sekhon H.S., London C.A., Sekhon M., Iversen P.L., Devi G.R. c-MYC antisense phosphosphorodiamidate morpholino oligomer inhibits lung metastasis in a murine tumor model. Lung Cancer. 2008;60:347–354. doi: 10.1016/j.lungcan.2007.10.028. PubMed DOI
Iversen P.L., Arora V., Acker A.J., Mason D.H., Devi G.R. Efficacy of antisense morpholino oligomer targeted to c-myc in prostate cancer xenograft murine model and a Phase I safety study in humans. Clin. Cancer Res. 2003;9:2510–2519. PubMed
Vidovic D., Huynh T.T., Konda P., Dean C., Cruickshank B.M., Sultan M., Coyle K.M., Gujar S., Marcato P. ALDH1A3-regulated long non-coding RNA NRAD1 is a potential novel target for triple-negative breast tumors and cancer stem cells. Cell Death Differ. 2020;27:363–378. doi: 10.1038/s41418-019-0362-1. PubMed DOI PMC
Zhang B., Lu H.Y., Xia Y.H., Jiang A.G., Lv Y.X. Long non-coding RNA EPIC1 promotes human lung cancer cell growth. Biochem. Biophys. Res. Commun. 2018;503:1342–1348. doi: 10.1016/j.bbrc.2018.07.046. PubMed DOI
Panda S., Setia M., Kaur N., Shepal V., Arora V., Singh D.K., Mondal A., Teli A., Tathode M., Gajula R., et al. Noncoding RNA Ginir functions as an oncogene by associating with centrosomal proteins. PLoS Biol. 2018;16:e2004204. doi: 10.1371/journal.pbio.2004204. PubMed DOI PMC
Lavalou P., Eckert H., Damy L., Constanty F., Majello S., Bitetti A., Graindorge A., Shkumatava A. Corrigendum: Strategies for genetic inactivation of long noncoding RNAs in zebrafish. RNA. 2020;26:529. doi: 10.1261/rna.074989.120. PubMed DOI PMC
Roobol M.J., Schröder F.H., van Leeuwen P., Wolters T., van den Bergh R.C., van Leenders G.J., Hessels D. Performance of the prostate cancer antigen 3 (PCA3) gene and prostate-specific antigen in prescreened men: Exploring the value of PCA3 for a first-line diagnostic test. Eur. Urol. 2010;58:475–481. doi: 10.1016/j.eururo.2010.06.039. PubMed DOI
Sun L., Su Y., Liu X., Xu M., Chen X., Zhu Y., Guo Z., Bai T., Dong L., Wei C., et al. Serum and exosome long non coding RNAs as potential biomarkers for hepatocellular carcinoma. J. Cancer. 2018;9:2631–2639. doi: 10.7150/jca.24978. PubMed DOI PMC
Conigliaro A., Costa V., Lo Dico A., Saieva L., Buccheri S., Dieli F., Manno M., Raccosta S., Mancone C., Tripodi M., et al. CD90+ liver cancer cells modulate endothelial cell phenotype through the release of exosomes containing H19, l.n.c.R.N.A. Mol. Cancer. 2015;14:155. doi: 10.1186/s12943-015-0426-x. PubMed DOI PMC
Fu Z., Chen C., Zhou Q., Wang Y., Zhao Y., Zhao X., Li W., Zheng S., Ye H., Wang L., et al. LncRNA HOTTIP modulates cancer stem cell properties in human pancreatic cancer by regulating HOXA9. Cancer Lett. 2017;410:68–81. doi: 10.1016/j.canlet.2017.09.019. PubMed DOI
Han M., Gu Y., Lu P., Li J., Cao H., Li X., Qian X., Yu C., Yang Y., Yang X., et al. Exosome-mediated lncRNA AFAP1-AS1 promotes trastuzumab resistance through binding with AUF1 and activating ERBB2 translation. Mol. Cancer. 2020;19:26. doi: 10.1186/s12943-020-1145-5. PubMed DOI PMC
Zhu Z., Wang H., Pang Y., Hu H., Zhang H., Wang W. Exosomal long non-coding RNA UCA1 functions as growth inhibitor in esophageal Cancer. Aging. 2020;12:20523–20539. doi: 10.18632/aging.103911. PubMed DOI PMC
Wu G., Dawson E., Duong A., Haw R., Stein L. ReactomeFIViz: A Cytoscape app for pathway and network-based data analysis. F1000Research. 2014;3:146. PubMed PMC
Jassal B., Matthews L., Viteri G., Gong C., Lorente P., Fabregat A., Sidiropoulos K., Cook J., Gillespie M., Haw R., et al. The reactome pathway knowledgebase. Nucleic Acids Res. 2020;48:D498–D503. doi: 10.1093/nar/gkz1031. PubMed DOI PMC
Shannon P., Markiel A., Ozier O., Baliga N.S., Wang J.T., Ramage D., Amin N., Schwikowski B., Ideker T. Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498–2504. doi: 10.1101/gr.1239303. PubMed DOI PMC
Szklarczyk D., Gable A.L., Lyon D., Junge A., Wyder S., Huerta-Cepas J., Simonovic M., Doncheva N.T., Morris J.H., Bork P., et al. STRING v11: Protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019;47:D607–D613. doi: 10.1093/nar/gky1131. PubMed DOI PMC
Piñero J., Ramírez-Anguita J.M. Saüch-Pitarch J, Ronzano F, Centeno E, Sanz F, Furlong LI. The DisGeNET knowledge platform for disease genomics: 2019 update. Nucleic Acids Res. 2019;48:D845–D885. PubMed PMC
Yu G., Wang L.-G., Han Y., He Q.-Y. ClusterProfiler: An R package for comparing biological themes among gene clusters. OMI J. Integr. Biol. 2012;16:284–287. doi: 10.1089/omi.2011.0118. PubMed DOI PMC
Montojo J., Zuberi K., Rodriguez H., Kazi F., Wright G., Donaldson S.L., Morris Q., Bader G.D. GeneMANIA Cytoscape plugin: Fast gene function predictions on the desktop. Bioinformatics. 2010;26:2927–2928. doi: 10.1093/bioinformatics/btq562. PubMed DOI PMC
Merico D., Isserlin R., Stueker O., Emili A., Bader G.D. Enrichment Map: A Network-Based Method for Gene-Set Enrichment Visualization and Interpretation. PLoS ONE. 2010;5:e13984. doi: 10.1371/journal.pone.0013984. PubMed DOI PMC
Terry S., Buart S., Tan T.Z., Gros G., Noman M.Z., Lorens J.B., Mami-Chouaib F., Thiery J.P., Chouaib S. Acquisitionoftumor cell phenotypic diversity along the EMT spectrum under hypoxic pressure: Consequences on susceptibility to cell-mediated cytotoxicity. Oncoimmunology. 2017;6:e1271858. doi: 10.1080/2162402X.2016.1271858. PubMed DOI PMC
Shi J., Dong B., Cao J., Mao Y., Guan W., Peng Y., Wang S. Long non-coding RNA in glioma: Signaling pathways. Oncotarget. 2017;8:27582–27592. doi: 10.18632/oncotarget.15175. PubMed DOI PMC
Wang S.S., Jiang J., Liang X.H., Tang Y.L. Links between cancer stem cells and epithelial-mesenchymal transition. Onco. Targets Ther. 2015;8:2973–2980. PubMed PMC
Galoczova M., Coates P., Vojtesek B. STAT3, stem cells, cancer stem cells and p63. Cell Mol. Biol. Lett. 2018;23:12. doi: 10.1186/s11658-018-0078-0. PubMed DOI PMC
Yan C., Zhao J., Qin Y., Zhao F., Ji L., Zhang J. Overexpression of ATG4a promotes autophagy and proliferation, and inhibits apoptosis in lens epithelial cells via the AMPK and Akt pathways. Mol. Med. Rep. 2020;22:1295–1302. doi: 10.3892/mmr.2020.11205. PubMed DOI PMC
Martinez-Outschoorn U.E., Whitaker-Menezes D., Lin Z., Flomenberg N., Howell A., Pestell R.G., Lisanti M.P., Sotgia F. Cytokine production and inflammation drive autophagy in the tumor microenvironment: Role of stromal caveolin-1 as a key regulator. Cell Cycle. 2011;10:1784–1793. doi: 10.4161/cc.10.11.15674. PubMed DOI PMC
Visvader J.E. Cells of origin in Cancer. Nature. 2011;469:314–322. doi: 10.1038/nature09781. PubMed DOI
Taussig D.C., Miraki-Moud F., Anjos-Afonso F., Pearce D.J., Allen K., Ridler C., Lillington D., Oakervee H., Cavenagh J., Agrawal S.G. Anti-CD38 antibody-mediated clearance of human repopulating cells masks the heterogeneity of leukemia-initiating cells. Blood. 2008;112:568–575. doi: 10.1182/blood-2007-10-118331. PubMed DOI
Jang J.E., Eom J.I., Jeung H.K., Cheong J.W., Lee J.Y., Kim J.S., Min Y.H. Targeting AMPK-ULK1-mediated autophagy for combating BET inhibitor resistance in acute myeloid leukemia stem cells. Autophagy. 2017;13:761–762. doi: 10.1080/15548627.2016.1278328. PubMed DOI PMC
Zhang B., Nguyen L.X.T., Li L., Zhao D., Kumar B., Wu H., Lin A., Pellicano F., Hopcroft L., Su Y.-L., et al. Bone marrow niche trafficking of miR-126 controls the self-renewal of leukemia stem cells in chronic myelogenous leukemia. Nat. Med. 2018;24:450–462. doi: 10.1038/nm.4499. PubMed DOI PMC
Silvestri G., Trotta R., Stramucci L., Ellis J.J., Harb J.G., Neviani P., Wang S., Eisfeld A.K., Walker C.J., Zhang B., et al. Persistence of Drug-Resistant Leukemic Stem Cells and Impaired NK Cell Immunity in CML Patients Depend on MIR300 Antiproliferative and PP2A-Activating Functions. Blood. Cancer Discov. 2020;1:48–67. doi: 10.1158/0008-5472.BCD-19-0039. PubMed DOI PMC
Wang L., Bu P., Ai Y., Srinivasan T., Chen H.J., Xiang K., Lipkin S.M., Shen X. A long non-coding RNA targets microRNA miR-34a to regulate colon cancer stem cell asymmetric division. Elife. 2016;5:e14620. doi: 10.7554/eLife.14620. PubMed DOI PMC
Li H., Zhu L., Xu L., Qin K., Liu C., Yu Y., Su D., Wu K., Sheng Y. Long noncoding RNA linc00617 exhibits oncogenic activity in breast Cancer. Mol. Carcinog. 2017;56:3–17. doi: 10.1002/mc.22338. PubMed DOI
Meacham C.E., Morrison S.J. Tumour heterogeneity and cancer cell plasticity. Nature. 2013;501:328–337. doi: 10.1038/nature12624. PubMed DOI PMC
Notta F., Mullighan C.G., Wang J.C., Poeppl A., Doulatov S., Phillips L.A., Ma J., Minden M.D., Downing J.R., Dick J.E. Evolution of human BCR-ABL1 lymphoblastic leukaemia-initiating cells. Nature. 2011;469:362–367. doi: 10.1038/nature09733. PubMed DOI