The Role of Autophagy and lncRNAs in the Maintenance of Cancer Stem Cells

. 2021 Mar 11 ; 13 (6) : . [epub] 20210311

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid33799834

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.

Zobrazit více v PubMed

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

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...