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Biophysics Reports 2018, 4(4): 178-188 https://doi.org/10.1007/s41048-018-0062-2
Review | Open Access | Issue | Published: 29 August 2018

Cancer stem cells and tumorigenesis

Show Author's Information Pingping Zhu1,  Zusen Fan1,2( )
CAS Key Laboratory of Infection and Immunity, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China
University of Chinese Academy of Sciences, Beijing 100049, China
Keywords:
Intervention, Cancer stem cells, Signaling pathway, Self-renewal, Tumorigenesis
Cite this article:
Zhu P, Fan Z. Cancer stem cells and tumorigenesis. Biophysics Reports, 2018, 4(4): 178-188. https://doi.org/10.1007/s41048-018-0062-2
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Abstract Full text About this article

Cancer is one of the most serious diseases all over the world, and the cancer stem cell (CSC) model accounts for tumor initiation, metastasis, drug resistance, and relapse. The CSCs within tumor bulk have the capacity to self-renew, differentiate, and give rise to a new tumor. The self-renewal of CSCs is precisely regulated by various modulators, including Wnt/β-catenin signaling, Notch signaling, Hedgehog signaling, transcription factors, chromatin remodeling complexes, and non-coding RNAs. CSCs reside in their niches that are also involved in the self-renewal maintenance of CSCs and protection of CSCs from chemotherapy, radiotherapy, and even endogenous damages. Moreover, CSCs can also remodel their niches to initiate tumorigenesis. The mutual interactions between CSCs and their niches play a critical role in the regulation of CSC self-renewal and tumorigenesis as well. Many surface markers of CSCs have been identified, and these markers become first choices for CSC targeting. Due to heterogeneity and plasticity, targeting CSCs is still a big challenge for tumor elimination. In this review, we summarize recent progresses on the biological features of CSCs and targeting strategies against CSCs.


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About this article

Cancer stem cells and tumorigenesis

Show Author's information Pingping Zhu1, Zusen Fan1,2( )
CAS Key Laboratory of Infection and Immunity, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China
University of Chinese Academy of Sciences, Beijing 100049, China

Abstract

Cancer is one of the most serious diseases all over the world, and the cancer stem cell (CSC) model accounts for tumor initiation, metastasis, drug resistance, and relapse. The CSCs within tumor bulk have the capacity to self-renew, differentiate, and give rise to a new tumor. The self-renewal of CSCs is precisely regulated by various modulators, including Wnt/β-catenin signaling, Notch signaling, Hedgehog signaling, transcription factors, chromatin remodeling complexes, and non-coding RNAs. CSCs reside in their niches that are also involved in the self-renewal maintenance of CSCs and protection of CSCs from chemotherapy, radiotherapy, and even endogenous damages. Moreover, CSCs can also remodel their niches to initiate tumorigenesis. The mutual interactions between CSCs and their niches play a critical role in the regulation of CSC self-renewal and tumorigenesis as well. Many surface markers of CSCs have been identified, and these markers become first choices for CSC targeting. Due to heterogeneity and plasticity, targeting CSCs is still a big challenge for tumor elimination. In this review, we summarize recent progresses on the biological features of CSCs and targeting strategies against CSCs.

Keywords: Intervention, Cancer stem cells, Signaling pathway, Self-renewal, Tumorigenesis

References(111)

Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ, Clevers H, (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5.Nature 449:1003-1007
DOI Google Scholar

Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M, Danenberg E, Clarke AR, Sansom OJ, Clevers H, (2009) Crypt stem cells as the cells-of-origin of intestinal cancer.Nature 457:608-611
DOI Google Scholar

Barry ER, Morikawa T, Butler BL, Shrestha K, de la Rosa R, Yan KS, Fuchs CS, Magness ST, Smits R, Ogino S, Kuo CJ, Camargo FD, (2013) Restriction of intestinal stem cell expansion and the regenerative response by YAP.Nature 493:106-110
DOI Google Scholar

Beck B, Driessens G, Goossens S, Youssef KK, Kuchnio A, Caauwe A, Sotiropoulou PA, Loges S, Lapouge G, Candi A, Mascre G, Drogat B, Dekoninck S, Haigh JJ, Carmeliet P, Blanpain C, (2011) A vascular niche and a VEGF-Nrp1 loop regulate the initiation and stemness of skin tumours.Nature 478:399-403
DOI Google Scholar

Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, Oh EY, Gaber MW, Finklestein D, Allen M, Frank A, Bayazitov IT, Zakharenko SS, Gajjar A, Davidoff A, Gilbertson RJ, (2007) A perivascular niche for brain tumor stem cells.Cancer Cell 11:69-82
DOI Google Scholar

Cao L, Zhou Y, Zhai B, Liao J, Xu W, Zhang R, Li J, Zhang Y, Chen L, Qian H, Wu M, Yin Z, (2011) Sphere-forming cell subpopulations with cancer stem cell properties in human hepatoma cell lines.BMC Gastroenterol 11:71
DOI Google Scholar

Chaffer CL, Weinberg RA, (2015) How does multistep tumorigenesis really proceed?.Cancer Discov 5:22-24
DOI Google Scholar

Charles N, Ozawa T, Squatrito M, Bleau AM, Brennan CW, Hambardzumyan D, Holland EC, (2010) Perivascular nitric oxide activates notch signaling and promotes stem-like character in PDGF-induced glioma cells.Cell Stem Cell 6:141-152
DOI Google Scholar

Chiba T, Kita K, Zheng YW, Yokosuka O, Saisho H, Iwama A, Nakauchi H, Taniguchi H, (2006) Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties.Hepatology 44:240-251
DOI Google Scholar

Clevers H, (2006) Wnt/beta-catenin signaling in development and disease.Cell 127:469-480
DOI Google Scholar

Codd AS, Kanaseki T, Torigo T, Tabi Z, (2018) Cancer stem cells as targets for immunotherapy.Immunology 153:304-314
DOI Google Scholar

Cuiffo BG, Campagne A, Bell GW, Lembo A, Orso F, Lien EC, Bhasin MK, Raimo M, Hanson SE, Marusyk A, El-Ashry D, Hematti P, Polyak K, Mechta-Grigoriou F, Mariani O, Volinia S, Vincent-Salomon A, Taverna D, Karnoub AE, (2014) MSC-regulated microRNAs converge on the transcription factor FOXP2 and promote breast cancer metastasis.Cell Stem Cell 15:762-774
DOI Google Scholar

Davis H, Irshad S, Bansal M, Rafferty H, Boitsova T, Bardella C, Jaeger E, Lewis A, Freeman-Mills L, Giner FC, Rodenas-Cuadrado P, Mallappa S, Clark S, Thomas H, Jeffery R, Poulsom R, Rodriguez-Justo M, Novelli M, Chetty R, Silver A, Sansom OJ, Greten FR, Wang LM, East JE, Tomlinson I, Leedham SJ, (2015) Aberrant epithelial GREM1 expression initiates colonic tumorigenesis from cells outside the stem cell niche.Nat Med 21:62-70
DOI Google Scholar

Dean M, Fojo T, Bates S, (2005) Tumour stem cells and drug resistance.Nat Rev Cancer 5:275-284
DOI Google Scholar

Elsheikh SE, Green AR, Rakha EA, Powe DG, Ahmed RA, Collins HM, Soria D, Garibaldi JM, Paish CE, Ammar AA, Grainge MJ, Ball GR, Abdelghany MK, Martinez-Pomares L, Heery DM, Ellis IO, (2009) Global histone modifications in breast cancer correlate with tumor phenotypes, prognostic factors, and patient outcome.Cancer Res 69:3802-3809
DOI Google Scholar

Fujimoto A, Totoki Y, Abe T, Boroevich KA, Hosoda F, Nguyen HH, Aoki M, Hosono N, Kubo M, Miya F, Arai Y, Takahashi H, Shirakihara T, Nagasaki M, Shibuya T, Nakano K, Watanabe-Makino K, Tanaka H, Nakamura H, Kusuda J, Ojima H, Shimada K, Okusaka T, Ueno M, Shigekawa Y, Kawakami Y, Arihiro K, Ohdan H, Gotoh K, Ishikawa O, Ariizumi S, Yamamoto M, Yamada T, Chayama K, Kosuge T, Yamaue H, Kamatani N, Miyano S, Nakagama H, Nakamura Y, Tsunoda T, Shibata T, Nakagawa H, (2012) Whole-genome sequencing of liver cancers identifies etiological influences on mutation patterns and recurrent mutations in chromatin regulators.Nat Genet 44:760-764
DOI Google Scholar

Gao X, Cui Y, Levenson RM, Chung LW, Nie S, (2004) In vivo cancer targeting and imaging with semiconductor quantum dots.Nat Biotechnol 22:969-976
DOI Google Scholar

Gargiulo G, Cesaroni M, Serresi M, de Vries N, Hulsman D, Bruggeman SW, Lancini C, van Lohuizen M, (2013) In vivo RNAi screen for BMI1 targets identifies TGF-beta/BMP-ER stress pathways as key regulators of neural- and malignant glioma-stem cell homeostasis.Cancer Cell 23:660-676
DOI Google Scholar

Gopalan V, Islam F, Lam AK, (2018) Surface markers for the identification of cancer stem cells.Methods Mol Biol 1692:17-29
DOI Google Scholar

Greaves M, (2013) Cancer stem cells as ‘units of selection’.Evol Appl 6:102-108
DOI Google Scholar

Guarnerio J, Bezzi M, Jeong JC, Paffenholz SV, Berry K, Naldini MM, Lo-Coco F, Tay Y, Beck AH, Pandolfi PP, (2016) Oncogenic role of fusion-circRNAs derived from cancer-associated chromosomal translocations.Cell 166:1055-1056
DOI Google Scholar

Haraguchi N, Ishii H, Mimori K, Tanaka F, Ohkuma M, Kim HM, Akita H, Takiuchi D, Hatano H, Nagano H, Barnard GF, Doki Y, Mori M, (2010) CD13 is a therapeutic target in human liver cancer stem cells.J Clin Invest 120:3326-3339
DOI Google Scholar

Henderson T, Chen M, Darrow MA, Li CS, Chiu CL, Monjazeb AM, Murphy WJ, Canter RJ, (2018) Alterations in cancer stem-cell marker CD44 expression predict oncologic outcome in soft-tissue sarcomas.J Surg Res 223:207-214
DOI Google Scholar

Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, Bruns CJ, Heeschen C, (2007) Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer.Cell Stem Cell 1:313-323
DOI Google Scholar

Ji JF, Yamashita T, Budhu A, Forgues M, Jia HL, Li CL, Deng CX, Wauthier E, Reid LM, Ye QH, Qin LX, Yang W, Wang HY, Tang ZY, Croce CM, Wang XW, (2009) Identification of microRNA-181 by genome-wide screening as a critical player in EpCAM-positive hepatic cancer stem cells.Hepatology 50:472-480
DOI Google Scholar

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

Jones PA, Baylin SB, (2007) The epigenomics of cancer.Cell 128:683-692
DOI Google Scholar

Kalluri R, Zeisberg M, (2006) Fibroblasts in cancer.Nat Rev Cancer 6:392-401
DOI Google Scholar

Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, MacDonald DD, Jin DK, Shido K, Kerns SA, Zhu Z, Hicklin D, Wu Y, Port JL, Altorki N, Port ER, Ruggero D, Shmelkov SV, Jensen KK, Rafii S, Lyden D, (2005) VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche.Nature 438:820-827
DOI Google Scholar

Katoh Y, Katoh M, (2006) Hedgehog signaling pathway and gastrointestinal stem cell signaling network (Review).Int J Mol Med 18:1019-1023
DOI Google Scholar

Kim E, Kim M, Woo DH, Shin Y, Shin J, Chang N, Oh YT, Kim H, Rheey J, Nakano I, Lee C, Joo KM, Rich JN, Nam DH, Lee J, (2013) Phosphorylation of EZH2 activates STAT3 signaling via STAT3 methylation and promotes tumorigenicity of glioblastoma stem-like cells.Cancer Cell 23:839-852
DOI Google Scholar

Kitamura T, Qian BZ, Pollard JW, (2015) Immune cell promotion of metastasis.Nat Rev Immunol 15:73-86
DOI Google Scholar

Kleer CG, Cao Q, Varambally S, Shen RL, Ota L, Tomlins SA, Ghosh D, Sewalt RGAB, Otte AP, Hayes DF, Sabel MS, Livant D, Weiss SJ, Rubin MA, Chinnaiyan AM, (2003) EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells.Proc Natl Acad Sci USA 100:11606-11611
DOI Google Scholar

Klochendler-Yeivin A, Muchardt C, Yaniv M, (2002) SWI/SNF chromatin remodeling and cancer.Curr Opin Genet Dev 12:73-79
DOI Google Scholar

Kopan R, Ilagan MXG, (2009) The canonical notch signaling pathway: unfolding the activation mechanism.Cell 137:216-233
DOI Google Scholar

Korinek V, Barker N, Morin PJ, van Wichen D, de Weger R, Kinzler KW, Vogelstein B, Clevers H, (1997) Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC−/− colon carcinoma.Science 275:1784-1787
DOI Google Scholar

Krebs ET, (1947) Cancer and the embryonal hypothesis.Calif Med 66:270-271
Google Scholar

Kreso A, Dick JE, (2014) Evolution of the cancer stem cell model.Cell Stem Cell 14:275-291
DOI Google Scholar

Kurtova AV, Xiao J, Mo Q, Pazhanisamy S, Krasnow R, Lerner SP, Chen F, Roh TT, Lay E, Ho PL, Chan KS, (2015) Blocking PGE2-induced tumour repopulation abrogates bladder cancer chemoresistance.Nature 517:209-213
DOI Google Scholar

Lai AY, Wade PA, (2011) Cancer biology and NuRD: a multifaceted chromatin remodelling complex.Nat Rev Cancer 11:588-596
DOI Google Scholar

Laugesen A, Helin K, (2014) Chromatin repressive complexes in stem cells, development, and cancer.Cell Stem Cell 14:735-751
DOI Google Scholar

Lee TKW, Castilho A, Cheung VCH, Tang KH, Ma S, Irene OLN, (2011) CD24(+) liver tumor-initiating cells drive self-renewal and tumor initiation through STAT3-mediated NANOG regulation.Cell Stem Cell 9:50-63
DOI Google Scholar

Levina VV, Marrangoni A, Wang TT, Parikh S, Su YY, Herberman R, Lokshin A, Gorelik E, (2010) Elimination of human lung cancer stem cells through targeting of the SCF-c-kit autocrine signaling loop.Cancer Res 70:4272
DOI Google Scholar

Li HX, Gao QL, Guo LP, Lu SH, (2011) The PTEN/PI3K/Akt pathway regulates stem-like cells in primary esophageal carcinoma cells.Cancer Biol Ther 11:950-958
DOI Google Scholar

Li C, Yang Z, Du Y, Tang H, Chen J, Hu D, Fan Z, (2014) BCMab1, a monoclonal antibody against aberrantly glycosylated integrin α3β1, has potent antitumor activity of bladder cancer in vivo.Clin Cancer Res 20:4001-4013
DOI Google Scholar

Li C, Du Y, Yang Z, He L, Wang Y, Hao L, Ding M, Yan R, Wang J, Fan Z, (2016) GALNT1-mediated glycosylation and activation of sonic Hedgehog signaling maintains the self-renewal and tumor-initiating capacity of bladder cancer stem cells.Cancer Res 76:1273-1283
DOI Google Scholar

Li WZ, Ma HL, Zhang J, Zhu L, Wang C, Yang YL, (2017) Unraveling the roles of CD44/CD24 and ALDH1 as cancer stem cell markers in tumorigenesis and metastasis.Sci Rep

DOI Google Scholar

Liu Y, Cao X, (2016) Characteristics and significance of the pre-metastatic niche.Cancer Cell 30:668-681
DOI Google Scholar

Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H, Patrawala L, Yan H, Jeter C, Honorio S, Wiggins JF, Bader AG, Fagin R, Brown D, Tang DG, (2011) The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44.Nat Med 17:211-215
DOI Google Scholar

Liu SJ, Horlbeck MA, Cho SW, Birk HS, Malatesta M, He D, Attenello FJ, Villalta JE, Cho MY, Chen Y, Mandegar MA, Olvera MP, Gilbert LA, Conklin BR, Chang HY, Weissman JS, Lim DA, (2017) CRISPRi-based genome-scale identification of functional long noncoding RNA loci in human cells.Science

DOI Google Scholar

MacDonald BT, Tamai K, He X, (2009) Wnt/beta-catenin signaling: components, mechanisms, and diseases.Dev Cell 17:9-26
DOI Google Scholar

Marotta LLC, Almendro V, Marusyk A, Shipitsin M, Schemme J, Walker SR, Bloushtain-Qimron N, Kim JJ, Choudhury SA, Maruyama R, Wu Z, Gönen M, Mulvey LA, Bessarabova MO, Huh SJ, Silver SJ, Kim SY, Park SY, Lee HE, Anderson KS, Richardson AL, Nikolskaya T, Nikolsky Y, Liu XS, Root DE, Hahn WC, Frank DA, Polyak K, (2011) The JAK2/STAT3 signaling pathway is required for growth of CD44(+)CD24(−) stem cell-like breast cancer cells in human tumors.J Clin Invest 121:2723-2735
DOI Google Scholar

McGuire S, (2016) World cancer report 2014. Geneva, Switzerland: World Health Organization, international agency for research on cancer, WHO Press, 2015.Adv Nutr 7:418-419
DOI Google Scholar

Meacham CE, Morrison SJ, (2013) Tumour heterogeneity and cancer cell plasticity.Nature 501:328-337
DOI Google Scholar

Melo FS, Kurtova AV, Harnoss JM, Kljavin N, Hoeck JD, Hung J, Anderson JE, Storm EE, Modrusan Z, Koeppen H, Dijkgraaf GJ, Piskol R, de Sauvage FJ, (2017) A distinct role for Lgr5+ stem cells in primary and metastatic colon cancer.Nature 543:676-680
DOI Google Scholar

Merlos-Suarez A, Barriga FM, Jung P, Iglesias M, Cespedes MV, Rossell D, Sevillano M, Hernando-Momblona X, da Silva-Diz V, Munoz P, Clevers H, Sancho E, Mangues R, Batlle E, (2011) The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse.Cell Stem Cell 8:511-524
DOI Google Scholar

Mitchem JB, Brennan DJ, Knolhoff BL, Belt BA, Zhu Y, Sanford DE, Belaygorod L, Carpenter D, Collins L, Piwnica-Worms D, Hewitt S, Udupi GM, Gallagher WM, Wegner C, West BL, Wang-Gillam A, Goedegebuure P, Linehan DC, DeNardo DG, (2013) Targeting tumor-infiltrating macrophages decreases tumor-initiating cells, relieves immunosuppression, and improves chemotherapeutic responses.Cancer Res 73:1128-1141
DOI Google Scholar

Mumm JS, Kopan R, (2000) Notch signaling: from the outside in.Dev Biol 228:151-165
DOI Google Scholar

Ntziachristos P, Tsirigos A, Welstead GG, Trimarchi T, Bakogianni S, Xu L, Loizou E, Holmfeldt L, Strikoudis A, King B, Mullenders J, Becksfort J, Nedjic J, Paietta E, Tallman MS, Rowe JM, Tonon G, Satoh T, Kruidenier L, Prinjha R, Akira S, Van Vlierberghe P, Ferrando AA, Jaenisch R, Mullighan CG, Aifantis I, (2014) Contrasting roles of histone 3 lysine 27 demethylases in acute lymphoblastic leukaemia.Nature 514:513-517
DOI Google Scholar

O’Brien CA, Pollett A, Gallinger S, Dick JE, (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice.Nature 445:106-110
DOI Google Scholar

Organista-Nava J, Gomez-Gomez Y, Gariglio P, (2014) Embryonic stem cell-specific signature in cervical cancer.Tumour Biol 35:1727-1738
DOI Google Scholar

Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D, Pilotti S, Pierotti MA, Daidone MG, (2005) Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties.Cancer Res 65:5506-5511
DOI Google Scholar

Quail DF, Taylor MJ, Postovit LM, (2012) Microenvironmental regulation of cancer stem cell phenotypes.Curr Stem Cell Res T 7:197-216
DOI Google Scholar

Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, De Maria R, (2007) Identification and expansion of human colon-cancer-initiating cells.Nature 445:111-115
DOI Google Scholar

Santoro F, Botrugno OA, Dal Zuffo R, Pallavicini I, Matthews GM, Cluse L, Barozzi I, Senese S, Fornasari L, Moretti S, Altucci L, Pelicci PG, Chiocca S, Johnstone RW, Minucci S, (2013) A dual role for Hdac1: oncosuppressor in tumorigenesis, oncogene in tumor maintenance.Blood 121:3459-3468
DOI Google Scholar

Scheel C, Eaton EN, Li SH, Chaffer CL, Reinhardt F, Kah KJ, Bell G, Guo W, Rubin J, Richardson AL, Weinberg RA, (2011) Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast.Cell 145:926-940
DOI Google Scholar

Schepers AG, Snippert HJ, Stange DE, van den Born M, van Es JH, van de Wetering M, Clevers H, (2012) Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas.Science 337:730-735
DOI Google Scholar

Schroeder A, Heller DA, Winslow MM, Dahlman JE, Pratt GW, Langer R, Jacks T, Anderson DG, (2012) Treating metastatic cancer with nanotechnology.Nat Rev Cancer 12:39-50
DOI Google Scholar

Seligson DB, Horvath S, Shi T, Yu H, Tze S, Grunstein M, Kurdistani SK, (2005) Global histone modification patterns predict risk of prostate cancer recurrence.Nature 435:1262-1266
DOI Google Scholar

Shabbir A, Esfandyari T, Farassati F, (2018) Cancer stem cells, the ultimate targets in cancer therapy.OncoTargets Therapy 11:183-184
DOI Google Scholar

Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA, Mikkelson T, Heckl D, Ebert BL, Root DE, Doench JG, Zhang F, (2014) Genome-scale CRISPR-Cas9 knockout screening in human cells.Science 343:84-87
DOI Google Scholar

Shigdar S, Lin J, Li Y, Yang CJ, Wei M, Zhus Y, Liu H, Duan W, (2012) Cancer stem cell targeting: the next generation of cancer therapy and molecular imaging.Ther Deliv 3:227-244
DOI Google Scholar

Shimokawa M, Ohta Y, Nishikori S, Matano M, Takano A, Fujii M, Date S, Sugimoto S, Kanai T, Sato T, (2017) Visualization and targeting of LGR5+ human colon cancer stem cells.Nature 545:187-192
DOI Google Scholar

Shimono Y, Zabala M, Cho RW, Lobo N, Dalerba P, Qian D, Diehn M, Liu H, Panula SP, Chiao E, Dirbas FM, Somlo G, Pera RA, Lao K, Clarke MF, (2009) Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells.Cell 138:592-603
DOI Google Scholar

Soeda A, Park M, Lee D, Mintz A, Androutsellis-Theotokis A, McKay RD, Engh J, Iwama T, Kunisada T, Kassam AB, Pollack IF, Park DM, (2009) Hypoxia promotes expansion of the CD133-positive glioma stem cells through activation of HIF-1 alpha.Oncogene 28:3949-3959
DOI Google Scholar

Storm EE, e Melo FDS, Tremayne J, Kljavin N, Tan C, Ye X, Chiu C, Pham T, Hongo JA, Bainbridge T, Firestein R, Blackwood E, Metcalfe C, Stawiski EW, Yauch RL, Wu Y, de Sauvage FJ, (2016) Targeting PTPRK-RSPO3 colon tumours promotes differentiation and loss of stem-cell function.Nature 529:97-100
DOI Google Scholar

Su SC, Chen JN, Yao HR, Liu J, Yu SB, Lao LY, Wang MH, Luo ML, Xing Y, Chen F, Huang D, Zhao J, Yang L, Liao D, Su F, Li M, Liu Q, Song E, (2018) CD10(+)GPR77(+) cancer-associated fibroblasts promote cancer formation and chemoresistance by sustaining cancer stemness.Cell 172:841-856
DOI Google Scholar

Sun TM, Wang YC, Wang F, Du JZ, Mao CQ, Sun CY, Tang RZ, Liu Y, Zhu J, Zhu YH, Yang XZ, Wang J, (2014) Cancer stem cell therapy using doxorubicin conjugated to gold nanoparticles via hydrazone bonds.Biomaterials 35:836-845
DOI Google Scholar

Takahashi K, Yamanaka S, (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors.Cell 126:663-676
DOI Google Scholar

Takawa M, Masuda K, Kunizaki M, Daigo Y, Takagi K, Iwai Y, Cho HS, Toyokawa G, Yamane Y, Maejima K, Field HI, Kobayashi T, Akasu T, Sugiyama M, Tsuchiya E, Atomi Y, Ponder BA, Nakamura Y, Hamamoto R, (2011) Validation of the histone methyltransferase EZH2 as a therapeutic target for various types of human cancer and as a prognostic marker.Cancer Sci 102:1298-1305
DOI Google Scholar

Takebe N, Harris PJ, Warren RQ, Ivy SP, (2011) Targeting cancer stem cells by inhibiting Wnt, Notch, and Hedgehog pathways.Nat Rev Clin Oncol 8:97-106
DOI Google Scholar

Takebe N, Miele L, Harris PJ, Jeong W, Bando H, Kahn M, Yang SX, Ivy SP, (2015) Targeting Notch, Hedgehog, and Wnt pathways in cancer stem cells: clinical update.Nat Rev Clin Oncol 12:445-464
DOI Google Scholar

Terstappen LW, Huang S, Safford M, Lansdorp PM, Loken MR, (1991) Sequential generations of hematopoietic colonies derived from single nonlineage-committed CD34+CD38− progenitor cells.Blood 77:1218-1227
DOI Google Scholar

Tseng YY, Moriarity BS, Gong W, Akiyama R, Tiwari A, Kawakami H, Ronning P, Reuland B, Guenther K, Beadnell TC, Essig J, Otto GM, O’Sullivan MG, Largaespada DA, Schwertfeger KL, Marahrens Y, Kawakami Y, Bagchi A, (2014) PVT1 dependence in cancer with MYC copy-number increase.Nature 512:82-86
DOI Google Scholar

Valdes-Mora F, Song JZ, Statham AL, Strbenac D, Robinson MD, Nair SS, Patterson KI, Tremethick DJ, Stirzaker C, Clark SJ, (2012) Acetylation of H2A.Z is a key epigenetic modification associated with gene deregulation and epigenetic remodeling in cancer.Genome Res 22:307-321
DOI Google Scholar

Van der Flier LG, Haegebarth A, Stange DE, Van de Wetering M, Clevers H, (2009) OLFM4 is a robust marker for stem cells in human intestine and marks a subset of colorectal cancer cells.Gastroenterology 137:15-17
DOI Google Scholar

Visvader JE, Lindeman GJ, (2012) Cancer stem cells: current status and evolving complexities.Cell Stem Cell 10:717-728
DOI Google Scholar

Wang GG, Allis CD, Chi P, (2007) Chromatin remodeling and cancer, part I: covalent histone modifications.Trends Mol Med 13:363-372
DOI Google Scholar

Wang Y, Zhang H, Chen YP, Sun YM, Yang F, Yu WH, Liang J, Sun LY, Yang XH, Shi L, Li R, Li Y, Zhang Y, Li Q, Yi X, Shang Y, (2009) LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer.Cell 138:660-672
DOI Google Scholar

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

West AC, Johnstone RW, (2014) New and emerging HDAC inhibitors for cancer treatment.J Clin Invest 124:30-39
DOI Google Scholar

Wu G, Xu GZ, Schulman BA, Jeffrey PD, Harper JW, Pavletich NP, (2003) Structure of a beta-TrCP1-Skp1-beta-catenin complex: destruction motif binding and lysine specificity of the SCF beta-TrCP1 ubiquitin ligase.Mol Cell 11:1445-1456
DOI Google Scholar

Xing YH, Yao RW, Zhang Y, Guo CJ, Jiang S, Xu G, Dong R, Yang L, Chen LL, (2017) SLERT regulates DDX21 rings associated with pol I transcription.Cell 169(664–678):e616
DOI Google Scholar

Xu K, Wu ZJ, Groner AC, He HH, Cai C, Lis RT, Wu X, Stack EC, Loda M, Liu T, Xu H, Cato L, Thornton JE, Gregory RI, Morrissey C, Vessella RL, Montironi R, Magi-Galluzzi C, Kantoff PW, Balk SP, Liu XS, Brown M, (2012) EZH2 oncogenic activity in castration-resistant prostate cancer cells is polycomb-independent.Science 338:1465-1469
DOI Google Scholar

Yachida S, Jones S, Bozic I, Antal T, Leary R, Fu B, Kamiyama M, Hruban RH, Eshleman JR, Nowak MA, Velculescu VE, Kinzler KW, Vogelstein B, Iacobuzio-Donahue CA, (2010) Distant metastasis occurs late during the genetic evolution of pancreatic cancer.Nature 467:1114-1117
DOI Google Scholar

Yamazaki J, Estecio MR, Lu Y, Long H, Malouf GG, Graber D, Huo Y, Ramagli L, Liang S, Kornblau SM, Jelinek J, Issa JP, (2013) The epigenome of AML stem and progenitor cells.Epigenetics 8:92-104
DOI Google Scholar

Yang XJ, Ullah M, (2007) MOZ and MORF, two large MYSTic HATs in normal and cancer stem cells.Oncogene 26:5408-5419
DOI Google Scholar

Yang W, Yan HX, Chen L, Liu Q, He YQ, Yu LX, Zhang SH, Huang DD, Tang L, Kong XN, Chen C, Liu SQ, Wu MC, Wang HY, (2008) Wnt/beta-catenin signaling contributes to activation of normal and tumorigenic liver progenitor cells.Cancer Res 68:4287-4295
DOI Google Scholar

Yang ZF, Ho DW, Ng MN, Lau CK, Yu WC, Ngai P, Chu PW, Lam CT, Poon RT, Fan ST, (2008) Significance of CD90+ cancer stem cells in human liver cancer.Cancer Cell 13:153-166
DOI Google Scholar

Yang L, Ren Y, Yu X, Qian F, Bian BSJ, Xiao HL, Wang WG, Xu SL, Yang J, Cui W, Liu Q, Wang Z, Guo W, Xiong G, Yang K, Qian C, Zhang X, Zhang P, Cui YH, Bian XW, (2014) ALDH1A1 defines invasive cancer stem-like cells and predicts poor prognosis in patients with esophageal squamous cell carcinoma.Mod Pathol 27:775-783
DOI Google Scholar

Yang Z, Li C, Fan Z, Liu H, Zhang X, Cai Z, Xu L, Luo J, Huang Y, He L, Liu C, Wu S, (2017) Single-cell sequencing reveals variants in ARID1A, GPRC5A and MLL2 driving self-renewal of human bladder cancer stem cells.Eur Urol 71:8-12
DOI Google Scholar

Ye J, Wu D, Wu P, Chen ZG, Huang J, (2014) The cancer stem cell niche: cross talk between cancer stem cells and their microenvironment.Tumor Biol 35:3945-3951
DOI Google Scholar

Yilmaz OH, Valdez R, Theisen BK, Guo W, Ferguson DO, Wu H, Morrison SJ, (2006) Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells.Nature 441:475-482
DOI Google Scholar

Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, Huang Y, Hu X, Su F, Lieberman J, Song E, (2007) Let-7 regulates self renewal and tumorigenicity of breast cancer cells.Cell 131:1109-1123
DOI Google Scholar

Yu CC, Lo WL, Chen YW, Huang PI, Hsu HS, Tseng LM, Hung SC, Kao SY, Chang CJ, Chiou SH, (2011) BMI-1 regulates snail expression and promotes metastasis ability in head and neck squamous cancer-derived ALDH1 positive cells.J Oncol

DOI Google Scholar

Zheng H, Pomyen Y, Hernandez MO, Li C, Livak F, Tang W, Dang H, Greten TF, Davis JL, Zhao Y, Mehta M, Levin Y, Shetty J, Tran B, Budhu A, Wang XW, (2018) Single-cell analysis reveals cancer stem cell heterogeneity in hepatocellular carcinoma.Hepatology 68:127-140
DOI Google Scholar

Zhou JB, Wulfkuhle J, Zhang H, Gu PH, Yang YQ, Deng JH, Margolick JB, Liotta LA, Petricoin E, Zhang Y, (2007) Activation of the PTEN/mTOR/STAT3 pathway in breast cancer stem-like cells is required for viability and maintenance.Proc Natl Acad Sci USA 104:16158-16163
DOI Google Scholar

Zhu P, Wang Y, He L, Huang G, Du Y, Zhang G, Yan X, Xia P, Ye B, Wang S, Hao L, Wu J, Fan Z, (2015) ZIC2-dependent OCT4 activation drives self-renewal of human liver cancer stem cells.J Clin Invest 125:3795-3808
DOI Google Scholar

Zhu PP, Wang YY, Du Y, He L, Huang GL, Zhang G, Yan XL, Fan ZS, (2015) C8orf4 negatively regulates self-renewal of liver cancer stem cells via suppression of NOTCH2 signalling.Nat Commun 6:1722
DOI Google Scholar

Zhu P, Wang Y, Huang G, Ye B, Liu B, Wu J, Du Y, He L, Fan Z, (2016) lnc-beta-Catm elicits EZH2-dependent beta-catenin stabilization and sustains liver CSC self-renewal.Nat Struct Mol Biol 23:631-639
DOI Google Scholar

Zhu P, Wang Y, Wu J, Huang G, Liu B, Ye B, Du Y, Gao G, Tian Y, He L, Fan Z, (2016) LncBRM initiates YAP1 signalling activation to drive self-renewal of liver cancer stem cells.Nat Commun 7:13608
DOI Google Scholar
Publication history
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Acknowledgements
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Publication history

Received: 01 June 2018
Accepted: 16 July 2018
Published: 29 August 2018
Issue date: August 2018

Copyright

© The Author(s) 2018

Acknowledgements

Acknowledgements

This work was supported by the funding provided by the National Natural Science Foundation of China (91640203, 31771638), Beijing Natural Science Foundation (7181006), and Postdoctoral Innovative Talent Support Program to Pingping Zhu.

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Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

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