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Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Review Article

Cancer Stem Cell Niche in Colorectal Cancer and Targeted Therapies

Author(s): Hao Wang, Guihua Cui, Bo Yu, Meiyan Sun and Hong Yang*

Volume 26, Issue 17, 2020

Page: [1979 - 1993] Pages: 15

DOI: 10.2174/1381612826666200408102305

Price: $65

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Abstract

Cancer stem cells (CSCs), also known as tumor-initiating cells, are a sub-population of tumor cells found in many human cancers that are endowed with self-renewal and pluripotency. CSCs may be more resistant to conventional anticancer therapies than average cancer cells, as they can easily escape the cytotoxic effects of standard chemotherapy, thereby resulting in tumor relapse. Despite significant progress in related research, effective elimination of CSCs remains an unmet clinical need. CSCs are localized in a specialized microenvironment termed the niche, which plays a pivotal role in cancer multidrug resistance. The niche components of CSCs, such as the extracellular matrix, also physically shelter CSCs from therapeutic agents. Colorectal cancer is the most common malignancy worldwide and presents a relatively transparent process of cancer initiation and development, making it an ideal model for CSC niche research. Here, we review recent advances in the field of CSCs using colorectal cancer as an example to illustrate the potential therapeutic value of targeting the CSC niche. These findings not only provide a novel theoretical basis for in-depth discussions on tumor occurrence, development, and prognosis evaluation, but also offer new strategies for the targeted treatment of cancer.

Keywords: Cancer stem cells, multidrug resistance, cancer niche, targeted therapy, chemotherapy, tumor-initiating cells.

[1]
Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin 2018; 68(1): 7-30.
[http://dx.doi.org/10.3322/caac.21442] [PMID: 29313949]
[2]
Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013; 63(1): 11-30.
[http://dx.doi.org/10.3322/caac.21166] [PMID: 23335087]
[3]
Furth J, Kahn MC, Breedis C. The transmission of leukemia of mice with a single cell. Am J Cancer 1937; 31: 276-82.
[http://dx.doi.org/10.1158/ajc.1937.276]
[4]
Bruce WR, Van Der Gaag H. A quantitative assay for the number of murine lymphoma cells capable of proliferation in vivo. Nature 1963; 199(4888): 79-80.
[http://dx.doi.org/10.1038/199079a0] [PMID: 14047954]
[5]
Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3(7): 730-7.
[http://dx.doi.org/10.1038/nm0797-730] [PMID: 9212098]
[6]
Lapidot T, Sirard C, Vormoor J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994; 367(6464): 645-8.
[http://dx.doi.org/10.1038/367645a0] [PMID: 7509044]
[7]
Dietrich F, Pietrobon Martins J, Kaiser S, Silva RBM, Rockenbach L, Edelweiss MIA. Corrections: prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100(11): 6890-0.
[http://dx.doi.org/10.1073/pnas.1131491100]
[8]
Singh SK, Clarke ID, Terasaki M, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63(18): 5821-8.
[PMID: 14522905]
[9]
O’Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007; 445(7123): 106-10.
[http://dx.doi.org/10.1038/nature05372] [PMID: 17122772]
[10]
Hermann PC, Huber SL, Herrler T, et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007; 1(3): 313-23.
[http://dx.doi.org/10.1016/j.stem.2007.06.002] [PMID: 18371365]
[11]
Fang D, Nguyen TK, Leishear K, et al. A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res 2005; 65(20): 9328-37.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-1343] [PMID: 16230395]
[12]
Ma S, Chan KW, Hu L, et al. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology 2007; 132(7): 2542-56.
[http://dx.doi.org/10.1053/j.gastro.2007.04.025] [PMID: 17570225]
[13]
Ho MM, Ng AV, Lam S, Hung JY. Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res 2007; 67(10): 4827-33.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-3557] [PMID: 17510412]
[14]
Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 2005; 65(23): 10946-51.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-2018] [PMID: 16322242]
[15]
Bapat SA, Mali AM, Koppikar CB, Kurrey NK. Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Res 2005; 65(8): 3025-9.
[http://dx.doi.org/10.1158/0008-5472.CAN-04-3931] [PMID: 15833827]
[16]
Takaishi S, Okumura T, Tu S, et al. Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells 2009; 27(5): 1006-20.
[http://dx.doi.org/10.1002/stem.30] [PMID: 19415765]
[17]
Clarke MF, Dick JE, Dirks PB, et al. Cancer stem cells--perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 2006; 66(19): 9339-44.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-3126] [PMID: 16990346]
[18]
Calabrese C, Poppleton H, Kocak M, et al. A perivascular niche for brain tumor stem cells. Cancer Cell 2007; 11(1): 69-82.
[http://dx.doi.org/10.1016/j.ccr.2006.11.020] [PMID: 17222791]
[19]
Beck B, Driessens G, Goossens S, et al. A vascular niche and a VEGF-Nrp1 loop regulate the initiation and stemness of skin tumours. Nature 2011; 478(7369): 399-403.
[http://dx.doi.org/10.1038/nature10525] [PMID: 22012397]
[20]
Platet N, Liu SY, Atifi ME, et al. Influence of oxygen tension on CD133 phenotype in human glioma cell cultures. Cancer Lett 2007; 258(2): 286-90.
[http://dx.doi.org/10.1016/j.canlet.2007.09.012] [PMID: 17977646]
[21]
Iida H, Suzuki M, Goitsuka R, Ueno H. Hypoxia induces CD133 expression in human lung cancer cells by up-regulation of OCT3/4 and SOX2. Int J Oncol 2012; 40(1): 71-9.
[PMID: 21947321]
[22]
Ginestier C, Hur MH, Charafe-Jauffret E, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007; 1(5): 555-67.
[http://dx.doi.org/10.1016/j.stem.2007.08.014] [PMID: 18371393]
[23]
Lin WM, Karsten U, Goletz S, Cheng RC, Cao Y. Expression of CD176 (Thomsen-Friedenreich antigen) on lung, breast and liver cancer-initiating cells. Int J Exp Pathol 2011; 92(2): 97-105.
[http://dx.doi.org/10.1111/j.1365-2613.2010.00747.x] [PMID: 21070402]
[24]
Wright MH, Calcagno AM, Salcido CD, Carlson MD, Ambudkar SV, Varticovski L. Brca1 breast tumors contain distinct CD44+/CD24- and CD133+ cells with cancer stem cell characteristics. Breast Cancer Res 2008; 10(1): R10.
[http://dx.doi.org/10.1186/bcr1855] [PMID: 18241344]
[25]
Gulaia V, Kumeiko V, Shved N, et al. Molecular mechanisms governing the stem cell’s fate in brain cancer: factors of stemness and quiescence. Front Cell Neurosci 2018; 12: 388.
[http://dx.doi.org/10.3389/fncel.2018.00388] [PMID: 30510501]
[26]
Paranjape AN, Soundararajan R, Werden SJ, et al. Inhibition of FOXC2 restores epithelial phenotype and drug sensitivity in prostate cancer cells with stem-cell properties. Oncogene 2016; 35(46): 5963-76.
[http://dx.doi.org/10.1038/onc.2015.498] [PMID: 26804168]
[27]
Jaworska D, Król W, Szliszka E. Król Wojciech; Ewelina, S. Prostate cancer stem cells: research advances. Int J Mol Sci 2015; 16(11): 27433-49.
[http://dx.doi.org/10.3390/ijms161126036] [PMID: 26593898]
[28]
Dalerba P, Dylla SJ, Park IK, et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 2007; 104(24): 10158-63.
[http://dx.doi.org/10.1073/pnas.0703478104] [PMID: 17548814]
[29]
Ricci-Vitiani L, Lombardi DG, Pilozzi E, et al. Identification and expansion of human colon-cancer-initiating cells. Nature 2007; 445(7123): 111-5.
[http://dx.doi.org/10.1038/nature05384] [PMID: 17122771]
[30]
Ke J, Wu X, Wu X, et al. A subpopulation of CD24+ cells in colon cancer cell lines possess stem cell characteristics. Neoplasma 2012; 59(3): 282-8.
[http://dx.doi.org/10.4149/neo_2012_036] [PMID: 22329848]
[31]
Barker N, Ridgway RA, van Es JH, et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 2009; 457(7229): 608-11.
[http://dx.doi.org/10.1038/nature07602] [PMID: 19092804]
[32]
Pelosi E, Castelli G, Testa U. Pancreatic cancer: molecular characterization, clonal evolution and cancer stem cells. Biomedicines 2017; 5(4): 65.
[http://dx.doi.org/10.3390/biomedicines5040065] [PMID: 29156578]
[33]
Testa U, Castelli G, Pelosi E. Lung cancers: molecular characterization, clonal heterogeneity and evolution, and cancer stem cells. Cancers (Basel) 2018; 10(8): 248.
[http://dx.doi.org/10.3390/cancers10080248] [PMID: 30060526]
[34]
Salcido CD, Larochelle A, Taylor BJ, Dunbar CE, Varticovski L. Molecular characterisation of side population cells with cancer stem cell-like characteristics in small-cell lung cancer. Br J Cancer 2010; 102(11): 1636-44.
[http://dx.doi.org/10.1038/sj.bjc.6605668] [PMID: 20424609]
[35]
Yang ZF, Ho DW, Ng MN, et al. Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 2008; 13(2): 153-66.
[http://dx.doi.org/10.1016/j.ccr.2008.01.013] [PMID: 18242515]
[36]
Terris B, Cavard C, Perret C. EpCAM, a new marker for cancer stem cells in hepatocellular carcinoma. J Hepatol 2010; 52(2): 280-1.
[http://dx.doi.org/10.1016/j.jhep.2009.10.026] [PMID: 20006402]
[37]
Testa U, Petrucci E, Pasquini L, Castelli G, Pelosi E. Ovarian cancers: genetic abnormalities, tumor heterogeneity and progression, clonal evolution and cancer stem cells. Medicines (Basel) 2018; 5(1): 16.
[http://dx.doi.org/10.3390/medicines5010016] [PMID: 29389895]
[38]
Singh SR. Gastric cancer stem cells: a novel therapeutic target. Cancer Lett 2013; 338(1): 110-9.
[http://dx.doi.org/10.1016/j.canlet.2013.03.035] [PMID: 23583679]
[39]
Li C, Wu JJ, Hynes M, et al. c-Met is a marker of pancreatic cancer stem cells and therapeutic target. Gastroenterology 2011; 141(6): 2218-2227.e5.
[http://dx.doi.org/10.1053/j.gastro.2011.08.009] [PMID: 21864475]
[40]
Silva IA, Bai S, McLean K, et al. Aldehyde dehydrogenase in combination with CD133 defines angiogenic ovarian cancer stem cells that portend poor patient survival. Cancer Res 2011; 71(11): 3991-4001.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-3175] [PMID: 21498635]
[41]
Lathia JD, Gallagher J, Myers JT, et al. Direct in vivo evidence for tumor propagation by glioblastoma cancer stem cells. PLoS One 2011; 6(9) e24807
[http://dx.doi.org/10.1371/journal.pone.0024807] [PMID: 21961046]
[42]
Son MJ, Woolard K, Nam DH, Lee J, Fine HA. SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma. Cell Stem Cell 2009; 4(5): 440-52.
[http://dx.doi.org/10.1016/j.stem.2009.03.003] [PMID: 19427293]
[43]
Lathia JD, Gallagher J, Heddleston JM, et al. Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell 2010; 6(5): 421-32.
[http://dx.doi.org/10.1016/j.stem.2010.02.018] [PMID: 20452317]
[44]
Meyer MJ, Fleming JM, Lin AF, Hussnain SA, Ginsburg E, Vonderhaar BK. CD44posCD49fhiCD133/2hi defines xenograft-initiating cells in estrogen receptor-negative breast cancer. Cancer Res 2010; 70(11): 4624-33.
[http://dx.doi.org/10.1158/0008-5472.CAN-09-3619] [PMID: 20484027]
[45]
Ishizawa K, Rasheed ZA, Karisch R, et al. Tumor-initiating cells are rare in many human tumors. Cell Stem Cell 2010; 7(3): 279-82.
[http://dx.doi.org/10.1016/j.stem.2010.08.009] [PMID: 20804964]
[46]
Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008; 8(10): 755-68.
[http://dx.doi.org/10.1038/nrc2499] [PMID: 18784658]
[47]
Goardon N, Marchi E, Atzberger A, et al. Coexistence of LMPP-like and GMP-like leukemia stem cells in acute myeloid leukemia. Cancer Cell 2011; 19(1): 138-52.
[http://dx.doi.org/10.1016/j.ccr.2010.12.012] [PMID: 21251617]
[48]
Aparicio S, Caldas C. The implications of clonal genome evolution for cancer medicine. N Engl J Med 2013; 368(9): 842-51.
[http://dx.doi.org/10.1056/NEJMra1204892] [PMID: 23445095]
[49]
Stewart JM, Shaw PA, Gedye C, Bernardini MQ, Neel BG, Ailles LE. Phenotypic heterogeneity and instability of human ovarian tumor-initiating cells. Proc Natl Acad Sci USA 2011; 108(16): 6468-73.
[http://dx.doi.org/10.1073/pnas.1005529108] [PMID: 21451132]
[50]
Eppert K, Takenaka K, Lechman ER, et al. Stem cell gene expression programs influence clinical outcome in human leukemia. Nat Med 2011; 17(9): 1086-93.
[http://dx.doi.org/10.1038/nm.2415] [PMID: 21873988]
[51]
Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ. Efficient tumour formation by single human melanoma cells. Nature 2008; 456(7222): 593-8.
[http://dx.doi.org/10.1038/nature07567] [PMID: 19052619]
[52]
Boiko AD, Razorenova OV, van de Rijn M, et al. Human melanoma-initiating cells express neural crest nerve growth factor receptor CD271. Nature 2010; 466(7302): 133-7.
[http://dx.doi.org/10.1038/nature09161] [PMID: 20596026]
[53]
Vermeulen L, De Sousa E Melo F, van der Heijden M, et al. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol 2010; 12(5): 468-76.
[http://dx.doi.org/10.1038/ncb2048] [PMID: 20418870]
[54]
Heddleston JM, Li Z, McLendon RE, Hjelmeland AB, Rich JN. The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype. Cell Cycle 2009; 8(20): 3274-84.
[http://dx.doi.org/10.4161/cc.8.20.9701] [PMID: 19770585]
[55]
Gupta PB, Chaffer CL, Weinberg RA. Cancer stem cells: mirage or reality? Nat Med 2009; 15(9): 1010-2.
[http://dx.doi.org/10.1038/nm0909-1010] [PMID: 19734877]
[56]
Mani SA, Guo W, Liao MJ, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133(4): 1-715.
[http://dx.doi.org/10.1016/j.cell.2008.03.027]
[57]
Noman MZ, Van Moer K, Marani V, et al. CD47 is a direct target of SNAI1 and ZEB1 and its blockade activates the phagocytosis of breast cancer cells undergoing EMT. OncoImmunology 2018; 7(4) e1345415
[http://dx.doi.org/10.1080/2162402X.2017.1345415] [PMID: 29632713]
[58]
Kotiyal S, Bhattacharya S. Breast cancer stem cells, EMT and therapeutic targets. Biochem Biophys Res Commun 2014; 453(1): 112-6.
[http://dx.doi.org/10.1016/j.bbrc.2014.09.069] [PMID: 25261721]
[59]
Batlle E, Clevers H. Cancer stem cells revisited. Nat Med 2017; 23(10): 1124-34.
[http://dx.doi.org/10.1038/nm.4409] [PMID: 28985214]
[60]
Santamaria PG, Moreno-Bueno G, Portillo F, Cano A. EMT: Present and future in clinical oncology. Mol Oncol 2017; 11(7): 718-38.
[http://dx.doi.org/10.1002/1878-0261.12091] [PMID: 28590039]
[61]
Lv ZD, Kong B, Liu XP, et al. miR-655 suppresses epithelial-to-mesenchymal transition by targeting Prrx1 in triple-negative breast cancer. J Cell Mol Med 2016; 20(5): 864-73.
[http://dx.doi.org/10.1111/jcmm.12770] [PMID: 26820102]
[62]
Beerling E, Seinstra D, de Wit E, et al. Plasticity between epithelial and mesenchymal states unlinks EMT from metastasis-enhancing stem cell capacity. Cell Rep 2016; 14(10): 2281-8.
[http://dx.doi.org/10.1016/j.celrep.2016.02.034] [PMID: 26947068]
[63]
Beck B, Lapouge G, Rorive S, et al. Different levels of Twist1 regulate skin tumor initiation, stemness, and progression. Cell Stem Cell 2015; 16(1): 67-79.
[http://dx.doi.org/10.1016/j.stem.2014.12.002] [PMID: 25575080]
[64]
Wu HT, Zhong HT, Li GW, et al. Oncogenic functions of the EMT-related transcription factor ZEB1 in breast cancer. J Transl Med 2020; 18(1): 51.
[http://dx.doi.org/10.1186/s12967-020-02240-z] [PMID: 32014049]
[65]
Schmidt JM, Panzilius E, Bartsch HS, et al. Stem-cell-like properties and epithelial plasticity arise as stable traits after transient Twist1 activation. Cell Rep 2015; 10(2): 131-9.
[http://dx.doi.org/10.1016/j.celrep.2014.12.032] [PMID: 25578726]
[66]
Yang M, Brackenbury WJ. Membrane potential and cancer progression. Front Physiol 2013; 4(2): 185.
[PMID: 23882223]
[67]
Gao R, Shen Y, Cai J, Lei M, Wang Z. Expression of voltage-gated sodium channel α subunit in human ovarian cancer. Oncol Rep 2010; 23(5): 1293-9.
[PMID: 20372843]
[68]
Yang M, Kozminski DJ, Wold LA, et al. Therapeutic potential for phenytoin: targeting Na(v)1.5 sodium channels to reduce migration and invasion in metastatic breast cancer. Breast Cancer Res Treat 2012; 134(2): 603-15.
[http://dx.doi.org/10.1007/s10549-012-2102-9] [PMID: 22678159]
[69]
Hwang DG, Qian X, Hornick JL. DOG1 antibody is a highly sensitive and specific marker for gastrointestinal stromal tumors in cytology cell blocks. Am J Clin Pathol 2011; 135(3): 448-53.
[http://dx.doi.org/10.1309/AJCP0PPKOBNDT9LB] [PMID: 21350101]
[70]
Gritti M, Würth R, Angelini M, et al. Metformin repositioning as antitumoral agent: selective antiproliferative effects in human glioblastoma stem cells, via inhibition of CLIC1-mediated ion current. Oncotarget 2014; 5(22): 11252-68.
[http://dx.doi.org/10.18632/oncotarget.2617] [PMID: 25361004]
[71]
Setti M, Savalli N, Osti D, et al. Functional role of CLIC1 ion channel in glioblastoma-derived stem/progenitor cells. J Natl Cancer Inst 2013; 105(21): 1644-55.
[http://dx.doi.org/10.1093/jnci/djt278] [PMID: 24115360]
[72]
Brackenbury WJ. Voltage-gated sodium channels and metastatic disease. Channels (Austin) 2012; 6(5): 352-61.
[http://dx.doi.org/10.4161/chan.21910] [PMID: 22992466]
[73]
Pang R, Law WL, Chu AC, et al. A subpopulation of CD26+ cancer stem cells with metastatic capacity in human colorectal cancer. Cell Stem Cell 2010; 6(6): 603-15.
[http://dx.doi.org/10.1016/j.stem.2010.04.001] [PMID: 20569697]
[74]
Campbell PJ, Yachida S, Mudie LJ, et al. The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 2010; 467(7319): 1109-13.
[http://dx.doi.org/10.1038/nature09460] [PMID: 20981101]
[75]
Wu X, Northcott PA, Dubuc A, et al. Clonal selection drives genetic divergence of metastatic medulloblastoma. Nature 2012; 482(7386): 529-33.
[http://dx.doi.org/10.1038/nature10825] [PMID: 22343890]
[76]
Borst P. Cancer drug pan-resistance: pumps, cancer stem cells, quiescence, epithelial to mesenchymal transition, blocked cell death pathways, persisters or what? Open Biol 2012; 2(5): 120066-6.
[http://dx.doi.org/10.1098/rsob.120066] [PMID: 22724067]
[77]
Holohan C, Van Schaeybroeck S, Longley DB, Johnston PG. Cancer drug resistance: an evolving paradigm. Nat Rev Cancer 2013; 13(10): 714-26.
[http://dx.doi.org/10.1038/nrc3599] [PMID: 24060863]
[78]
Gialmanidis IP, Bravou V, Amanetopoulou SG, Varakis J, Kourea H, Papadaki H. Overexpression of hedgehog pathway molecules and FOXM1 in non-small cell lung carcinomas. Lung Cancer 2009; 66(1): 64-74.
[http://dx.doi.org/10.1016/j.lungcan.2009.01.007] [PMID: 19200615]
[79]
Kreso A, O’Brien CA, van Galen P, et al. Variable clonal repopulation dynamics influence chemotherapy response in colorectal cancer. Science 2013; 339(6119): 543-8.
[http://dx.doi.org/10.1126/science.1227670] [PMID: 23239622]
[80]
Chen J, Li Y, Yu TS, et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012; 488(7412): 522-6.
[http://dx.doi.org/10.1038/nature11287] [PMID: 22854781]
[81]
Oshimori N, Oristian D, Fuchs E. TGF-β promotes heterogeneity and drug resistance in squamous cell carcinoma. Cell 2015; 160(5): 963-76.
[http://dx.doi.org/10.1016/j.cell.2015.01.043] [PMID: 25723170]
[82]
Liau BB, Sievers C, Donohue LK, et al. Adaptive chromatin remodeling drives glioblastoma stem cell plasticity and drug tolerance. Cell Stem Cell 2017; 20(2): 233-246.e7.
[http://dx.doi.org/10.1016/j.stem.2016.11.003] [PMID: 27989769]
[83]
Kurtova AV, Xiao J, Mo Q, et al. Blocking PGE2-induced tumour repopulation abrogates bladder cancer chemoresistance. Nature 2015; 517(7533): 209-13.
[http://dx.doi.org/10.1038/nature14034] [PMID: 25470039]
[84]
Creighton CJ, Li X, Landis M, et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci USA 2009; 106(33): 13820-5.
[http://dx.doi.org/10.1073/pnas.0905718106] [PMID: 19666588]
[85]
Buczacki SJ, Zecchini HI, Nicholson AM, et al. Intestinal label-retaining cells are secretory precursors expressing Lgr5. Nature 2013; 495(7439): 65-9.
[http://dx.doi.org/10.1038/nature11965] [PMID: 23446353]
[86]
Wei L, Leibowitz BJ, Wang X, et al. Inhibition of CDK4/6 protects against radiation-induced intestinal injury in mice. J Clin Invest 2016; 126(11): 4076-87.
[http://dx.doi.org/10.1172/JCI88410] [PMID: 27701148]
[87]
Zhou S, Morris JJ, Barnes Y, Lan L, Schuetz JD, Sorrentino BP. Bcrp1 gene expression is required for normal numbers of side population stem cells in mice, and confers relative protection to mitoxantrone in hematopoietic cells in vivo. Proc Natl Acad Sci USA 2002; 99(19): 12339-44.
[http://dx.doi.org/10.1073/pnas.192276999] [PMID: 12218177]
[88]
Besançon R, Valsesia-Wittmann S, Puisieux A, Caron de Fromentel C, Maguer-Satta V. Cancer stem cells: the emerging challenge of drug targeting. Curr Med Chem 2009; 16(4): 394-416.
[http://dx.doi.org/10.2174/092986709787315531] [PMID: 19199913]
[89]
Nakanishi T, Ross DD. Breast cancer resistance protein (BCRP/ABCG2): its role in multidrug resistance and regulation of its gene expression. Chin J Cancer 2012; 31(2): 73-99.
[http://dx.doi.org/10.5732/cjc.011.10320] [PMID: 22098950]
[90]
Torquato HFV, Goettert MI, Justo GZ, Paredes-Gamero EJ. Anti-Cancer Phytometabolites Targeting Cancer Stem Cells. Curr Genomics 2017; 18(2): 156-74.
[http://dx.doi.org/10.2174/1389202917666160803162309] [PMID: 28367074]
[91]
Sung JM, Cho HJ, Yi H, et al. Characterization of a stem cell population in lung cancer A549 cells. Biochem Biophys Res Commun 2008; 371(1): 163-7.
[http://dx.doi.org/10.1016/j.bbrc.2008.04.038] [PMID: 18423378]
[92]
Hirschmann-Jax C, Foster AE, Wulf GG, et al. A distinct “side population” of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci USA 2004; 101(39): 14228-33.
[http://dx.doi.org/10.1073/pnas.0400067101] [PMID: 15381773]
[93]
Johannessen TC, Bjerkvig R, Tysnes BB. DNA repair and cancer stem-like cells--potential partners in glioma drug resistance? Cancer Treat Rev 2008; 34(6): 558-67.
[http://dx.doi.org/10.1016/j.ctrv.2008.03.125] [PMID: 18501520]
[94]
Sato A, Sunayama J, Matsuda K, et al. MEK-ERK signaling dictates DNA-repair gene MGMT expression and temozolomide resistance of stem-like glioblastoma cells via the MDM2-p53 axis. Stem Cells 2011; 29(12): 1942-51.
[http://dx.doi.org/10.1002/stem.753] [PMID: 21957016]
[95]
Todaro M, Perez Alea M, Scopelliti A, Medema JP, Stassi G. IL-4-mediated drug resistance in colon cancer stem cells. Cell Cycle 2008; 7(3): 309-13.
[http://dx.doi.org/10.4161/cc.7.3.5389] [PMID: 18235245]
[96]
Hsu HS, Lin JH, Huang WC, et al. Chemoresistance of lung cancer stemlike cells depends on activation of Hsp27. Cancer 2011; 117(7): 1516-28.
[http://dx.doi.org/10.1002/cncr.25599] [PMID: 21425153]
[97]
Ma S, Lee TK, Zheng BJ, Chan KW, Guan XY. CD133+ HCC cancer stem cells confer chemoresistance by preferential expression of the Akt/PKB survival pathway. Oncogene 2008; 27(12): 1749-58.
[http://dx.doi.org/10.1038/sj.onc.1210811] [PMID: 17891174]
[98]
Touho H, Karasawa J, Shishido H, Morisako T, Yamada K, Shibamoto K. Hemodynamic evaluation in patients with superficial temporal artery-middle cerebral artery anastomosis--stable xenon CT-CBF study and acetazolamide. Neurol Med Chir (Tokyo) 1990; 30(13): 1003-10.
[http://dx.doi.org/10.2176/nmc.30.1003] [PMID: 1714045]
[99]
Shih IeM, Wang TL. Notch signaling, gamma-secretase inhibitors, and cancer therapy. Cancer Res 2007; 67(5): 1879-82.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-3958] [PMID: 17332312]
[100]
Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 1978; 4(1-2): 7-25.
[PMID: 747780]
[101]
Testa U, Pelosi E, Castelli G. Colorectal cancer: genetic abnormalities, tumor progression, tumor heterogeneity, clonal evolution and tumor-initiating cells. Med Sci (Basel) 2018; 6(2): 31.
[http://dx.doi.org/10.3390/medsci6020031] [PMID: 29652830]
[102]
Choi S, Yoo YJ, Kim H, et al. Clinical and biochemical relevance of monounsaturated fatty acid metabolism targeting strategy for cancer stem cell elimination in colon cancer. Biochem Biophys Res Commun 2019; 519(1): 100-5.
[http://dx.doi.org/10.1016/j.bbrc.2019.08.137] [PMID: 31481234]
[103]
Mohamed SY, Kaf RM, Ahmed MM, Elwan A, Ashour HR, Ibrahim A. The prognostic value of cancer stem cell markers (notch1, aldh1, and cd44) in primary colorectal carcinoma. J Gastrointest Cancer 2018; 1-14.
[PMID: 30136202]
[104]
Kahlert UD, Mooney SM, Natsumeda M, Steiger HJ, Maciaczyk J. Targeting cancer stem-like cells in glioblastoma and colorectal cancer through metabolic pathways. Int J Cancer 2017; 140(1): 10-22.
[http://dx.doi.org/10.1002/ijc.30259] [PMID: 27389307]
[105]
Todaro M, Gaggianesi M, Catalano V, et al. CD44v6 is a marker of constitutive and reprogrammed cancer stem cells driving colon cancer metastasis. Cell Stem Cell 2014; 14(3): 342-56.
[http://dx.doi.org/10.1016/j.stem.2014.01.009] [PMID: 24607406]
[106]
Ricci-Vitiani L, Pallini R, Biffoni M, et al. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 2010; 468(7325): 824-8.
[http://dx.doi.org/10.1038/nature09557] [PMID: 21102434]
[107]
Alvero AB, Chen R, Fu HH, et al. Molecular phenotyping of human ovarian cancer stem cells unravels the mechanisms for repair and chemoresistance. Cell Cycle 2009; 8(1): 158-66.
[http://dx.doi.org/10.4161/cc.8.1.7533] [PMID: 19158483]
[108]
Momeny M, Moghaddaskho F, Gortany NK, et al. Blockade of vascular endothelial growth factor receptors by tivozanib has potential anti-tumour effects on human glioblastoma cells. Sci Rep 2017; 7: 44075.
[http://dx.doi.org/10.1038/srep44075]
[109]
Filatova A, Acker T, Garvalov BK. The cancer stem cell niche(s): the crosstalk between glioma stem cells and their microenvironment. Biochim Biophys Acta 2013; 1830(2): 2496-508.
[http://dx.doi.org/10.1016/j.bbagen.2012.10.008] [PMID: 23079585]
[110]
Ginestier C, Liu S, Diebel ME, et al. CXCR1 blockade selectively targets human breast cancer stem cells in vitro and in xenografts. J Clin Invest 2010; 120(2): 485-97.
[http://dx.doi.org/10.1172/JCI39397] [PMID: 20051626]
[111]
Rehn M, Olsson A, Reckzeh K, et al. Hypoxic induction of vascular endothelial growth factor regulates murine hematopoietic stem cell function in the low-oxygenic niche. Blood 2011; 118(6): 1534-43.
[http://dx.doi.org/10.1182/blood-2011-01-332890] [PMID: 21670467]
[112]
Collet G, El Hafny-Rahbi B, Nadim M, Tejchman A, Klimkiewicz K, Kieda C. Hypoxia-shaped vascular niche for cancer stem cells. Contemp Oncol (Pozn) 2015; 19(1A): A39-43.
[http://dx.doi.org/10.5114/wo.2014.47130] [PMID: 25691820]
[113]
Sceneay J, Chow MT, Chen A, et al. Primary tumor hypoxia recruits CD11b+/Ly6Cmed/Ly6G+ immune suppressor cells and compromises NK cell cytotoxicity in the premetastatic niche. Cancer Res 2012; 72(16): 3906-11.
[http://dx.doi.org/10.1158/0008-5472.CAN-11-3873] [PMID: 22751463]
[114]
Mao Q, Zhang Y, Fu X, et al. A tumor hypoxic niche protects human colon cancer stem cells from chemotherapy. J Cancer Res Clin Oncol 2013; 139(2): 211-22.
[http://dx.doi.org/10.1007/s00432-012-1310-3] [PMID: 23052691]
[115]
Miao ZF, Wang ZN, Zhao TT, et al. Peritoneal milky spots serve as a hypoxic niche and favor gastric cancer stem/progenitor cell peritoneal dissemination through hypoxia-inducible factor 1α. Stem Cells 2014; 32(12): 3062-74.
[http://dx.doi.org/10.1002/stem.1816] [PMID: 25142304]
[116]
Yan KS, Chia LA, Li X, et al. The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations. Proc Natl Acad Sci USA 2012; 109(2): 466-71.
[http://dx.doi.org/10.1073/pnas.1118857109] [PMID: 22190486]
[117]
van Es JH, Clevers H. Paneth cells. Curr Biol 2014; 24(12): R547-8.
[http://dx.doi.org/10.1016/j.cub.2014.04.049] [PMID: 24937274]
[118]
Setiawan J, Kotani T, Konno T, et al. Regulation of small intestinal epithelial homeostasis by Tsc2-mTORC1 signaling. Kobe J Med Sci 2019; 64(6): E200-9.
[PMID: 31327863]
[119]
Sato T, van Es JH, Snippert HJ, et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 2011; 469(7330): 415-8.
[http://dx.doi.org/10.1038/nature09637] [PMID: 21113151]
[120]
Pentinmikko N, Iqbal S, Mana M, et al. Notum produced by Paneth cells attenuates regeneration of aged intestinal epithelium. Nature 2019; 571(7765): 398-402.
[http://dx.doi.org/10.1038/s41586-019-1383-0] [PMID: 31292548]
[121]
Pai RK, Rybicki LA, Goldblum JR, Shen B, Xiao SY, Liu X. Paneth cells in colonic adenomas: association with male sex and adenoma burden. Am J Surg Pathol 2013; 37(1): 98-103.
[http://dx.doi.org/10.1097/PAS.0b013e318267b02e] [PMID: 23232853]
[122]
Wada R, Kuwabara N, Suda K. Incidence of Paneth cells in colorectal adenomas of Japanese descendants in Hawaii. J Gastroenterol Hepatol 1994; 9(3): 286-8.
[http://dx.doi.org/10.1111/j.1440-1746.1994.tb01727.x] [PMID: 8054530]
[123]
Mantani Y, Nishida M, Yuasa H, et al. Ultrastructural and histochemical study on the Paneth cells in the rat ascending colon. Anat Rec (Hoboken) 2014; 297(8): 1462-71.
[http://dx.doi.org/10.1002/ar.22937] [PMID: 24788798]
[124]
Joo M, Shahsafaei A, Odze RD. Paneth cell differentiation in colonic epithelial neoplasms: evidence for the role of the Apc/beta-catenin/Tcf pathway. Hum Pathol 2009; 40(6): 872-80.
[http://dx.doi.org/10.1016/j.humpath.2008.12.003] [PMID: 19269007]
[125]
Langlands AJ, Almet AA, Appleton PL, Newton IP, Osborne JM, Näthke IS. Paneth Cell-rich regions separated by a cluster of Lgr5+ cells initiate crypt fission in the intestinal stem cell niche. PLoS Biol 2016; 14(6) e1002491
[http://dx.doi.org/10.1371/journal.pbio.1002491] [PMID: 27348469]
[126]
Rothenberg ME, Nusse Y, Kalisky T, et al. Identification of a cKit(+) colonic crypt base secretory cell that supports Lgr5(+) stem cells in mice. Gastroenterology 2012; 142(5): 1195-1205.e6.
[http://dx.doi.org/10.1053/j.gastro.2012.02.006] [PMID: 22333952]
[127]
Emmink BL, Van Houdt WJ, Vries RG, et al. Differentiated human colorectal cancer cells protect tumor-initiating cells from irinotecan. Gastroenterology 2011; 141(1): 269-78.
[http://dx.doi.org/10.1053/j.gastro.2011.03.052] [PMID: 21459094]
[128]
Bellone G, Carbone A, Sibona N, et al. Aberrant activation of c-kit protects colon carcinoma cells against apoptosis and enhances their invasive potential. Cancer Res 2001; 61(5): 2200-6.
[PMID: 11280787]
[129]
Fatrai S, van Schelven SJ, Ubink I, et al. cells. tumor differentiated by factor cell stem of secretion requires cells tumor colon human KIT+ clonogenic of Maintenance Gastroenterology 2015; 149(3): 692-704.
[http://dx.doi.org/10.1053/j.gastro.2015.05.003] [PMID: 25962936]
[130]
Saito Y, Uchida N, Tanaka S, et al. Induction of cell cycle entry eliminates human leukemia stem cells in a mouse model of AML. Nat Biotechnol 2010; 28(3): 275-80.
[http://dx.doi.org/10.1038/nbt.1607] [PMID: 20160717]
[131]
Chen Y, Zhang F, Tsai Y, et al. IL-6 signaling promotes DNA repair and prevents apoptosis in CD133+ stem-like cells of lung cancer after radiation. Radiat Oncol 2015; 10(1): 227.
[http://dx.doi.org/10.1186/s13014-015-0534-1] [PMID: 26572130]
[132]
Somasagara RR, Spencer SM, Tripathi K, et al. RAD6 promotes DNA repair and stem cell signaling in ovarian cancer and is a promising therapeutic target to prevent and treat acquired chemoresistance. Oncogene 2017; 36(48): 6680-90.
[http://dx.doi.org/10.1038/onc.2017.279] [PMID: 28806395]
[133]
Jin L, Hope KJ, Zhai Q, Smadja-Joffe F, Dick JE. Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat Med 2006; 12(10): 1167-74.
[http://dx.doi.org/10.1038/nm1483] [PMID: 16998484]
[134]
Jin L, Lee EM, Ramshaw HS, et al. Monoclonal antibody-mediated targeting of CD123, IL-3 receptor alpha chain, eliminates human acute myeloid leukemic stem cells. Cell Stem Cell 2009; 5(1): 31-42.
[http://dx.doi.org/10.1016/j.stem.2009.04.018] [PMID: 19570512]
[135]
Gupta PB, Onder TT, Jiang G, et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 2009; 138(4): 645-59.
[http://dx.doi.org/10.1016/j.cell.2009.06.034] [PMID: 19682730]
[136]
Li J, Lam M. Registered report: the microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. eLife 2015; 4(4) e06434
[http://dx.doi.org/10.7554/eLife.06434] [PMID: 26231042]
[137]
Wang Y, Krivtsov AV, Sinha AU, et al. The Wnt/β-catenin pathway is required for the development of leukemia stem cells in AML. Science 2010; 327(5973): 1650-3.
[http://dx.doi.org/10.1126/science.1186624] [PMID: 20339075]
[138]
Pannuti A, Foreman K, Rizzo P, et al. Targeting Notch to target cancer stem cells. Clin Cancer Res 2010; 16(12): 3141-52.
[http://dx.doi.org/10.1158/1078-0432.CCR-09-2823] [PMID: 20530696]
[139]
Zhao C, Chen A, Jamieson CH, et al. Hedgehog signalling is essential for maintenance of cancer stem cells in myeloid leukaemia. Nature 2009; 458(7239): 776-9.
[http://dx.doi.org/10.1038/nature07737] [PMID: 19169242]
[140]
Foster BM, Zaidi D, Young TR, Mobley ME, Kerr BA. CD117/c-kit in cancer stem cell-Mediated Progression and Therapeutic Resistance. Biomedicines 2018; 6(1): 31.
[http://dx.doi.org/10.3390/biomedicines6010031] [PMID: 29518044]
[141]
Holland JD, Klaus A, Garratt AN, Birchmeier W. Wnt signaling in stem and cancer stem cells. Curr Opin Cell Biol 2013; 25(2): 254-64.
[http://dx.doi.org/10.1016/j.ceb.2013.01.004] [PMID: 23347562]
[142]
Malanchi I, Peinado H, Kassen D, et al. Cutaneous cancer stem cell maintenance is dependent on beta-catenin signalling. Nature 2008; 452(7187): 650-3.
[http://dx.doi.org/10.1038/nature06835] [PMID: 18385740]
[143]
Cai C, Zhu X. The Wnt/β-catenin pathway regulates self-renewal of cancer stem-like cells in human gastric cancer. Mol Med Rep 2012; 5(5): 1191-6.
[PMID: 22367735]
[144]
Xu W, Lin H, Zhang Y, et al. Compound Kushen Injection suppresses human breast cancer stem-like cells by down-regulating the canonical Wnt/β-catenin pathway. J Exp Clin Cancer Res 2011; 30(1): 103.
[http://dx.doi.org/10.1186/1756-9966-30-103] [PMID: 22032476]
[145]
Jang GB, Hong IS, Kim RJ, et al. Wnt/β-catenin small molecule inhibitor CWP232228 preferentially inhibits the growth of breast cancer stem-like cells. Cancer Res 2015; 75(8): 1691-702.
[http://dx.doi.org/10.1158/0008-5472.CAN-14-2041] [PMID: 25660951]
[146]
Qi L, Song W, Liu Z, Zhao X, Cao W, Sun B. Wnt3a promotes the vasculogenic mimicry formation of colon cancer via wnt/β-catenin signaling. Int J Mol Sci 2015; 16(8): 18564-79.
[http://dx.doi.org/10.3390/ijms160818564] [PMID: 26266404]
[147]
Qi L, Sun B, Liu Z, Cheng R, Li Y, Zhao X. Wnt3a expression is associated with epithelial-mesenchymal transition and promotes colon cancer progression. J Exp Clin Cancer Res 2014; 33: 107.
[http://dx.doi.org/10.1186/s13046-014-0107-4] [PMID: 25499541]
[148]
Koo BK, Spit M, Jordens I, et al. Tumour suppressor RNF43 is a stem-cell E3 ligase that induces endocytosis of Wnt receptors. Nature 2012; 488(7413): 665-9.
[http://dx.doi.org/10.1038/nature11308] [PMID: 22895187]
[149]
Gregorieff A, Pinto D, Begthel H, Destrée O, Kielman M, Clevers H. Expression pattern of Wnt signaling components in the adult intestine. Gastroenterology 2005; 129(2): 626-38.
[http://dx.doi.org/10.1016/j.gastro.2005.06.007] [PMID: 16083717]
[150]
van Es JH, Jay P, Gregorieff A, et al. Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat Cell Biol 2005; 7(4): 381-6.
[http://dx.doi.org/10.1038/ncb1240] [PMID: 15778706]
[151]
Jamieson CH, Weissman IL, Passegué E. Chronic versus acute myelogenous leukemia: a question of self-renewal. Cancer Cell 2004; 6(6): 531-3.
[PMID: 15607956]
[152]
Takahashi-Yanaga F, Kahn M. Targeting Wnt signaling: can we safely eradicate cancer stem cells? Clin Cancer Res 2010; 16(12): 3153-62.
[http://dx.doi.org/10.1158/1078-0432.CCR-09-2943] [PMID: 20530697]
[153]
Teng Y, Wang X, Wang Y, Ma D. Wnt/beta-catenin signaling regulates cancer stem cells in lung cancer A549 cells. Biochem Biophys Res Commun 2010; 392(3): 1-379.
[154]
Kim HY, Park JH, Won HY, Lee JY, Kong G. CBX7 inhibits breast tumorigenicity through DKK-1-mediated suppression of the Wnt/β-catenin pathway. FASEB J 2015; 29(1): 300-13.
[http://dx.doi.org/10.1096/fj.14-253997] [PMID: 25351982]
[155]
D’Angelo RC, Ouzounova M, Davis A, et al. Notch reporter activity in breast cancer cell lines identifies a subset of cells with stem cell activity. Mol Cancer Ther 2015; 14(3): 779-87.
[http://dx.doi.org/10.1158/1535-7163.MCT-14-0228] [PMID: 25673823]
[156]
Sansone P, Storci G, Giovannini C, et al. p66Shc/Notch-3 interplay controls self-renewal and hypoxia survival in human stem/progenitor cells of the mammary gland expanded in vitro as mammospheres. Stem Cells 2007; 25(3): 807-15.
[http://dx.doi.org/10.1634/stemcells.2006-0442] [PMID: 17158237]
[157]
Nishina S, Shiraha H, Nakanishi Y, et al. Restored expression of the tumor suppressor gene RUNX3 reduces cancer stem cells in hepatocellular carcinoma by suppressing Jagged1-Notch signaling. Oncol Rep 2011; 26(3): 523-31.
[http://dx.doi.org/10.3892/or.2011.1336] [PMID: 21637926]
[158]
Fan X, Matsui W, Khaki L, et al. Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res 2006; 66(15): 7445-52.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-0858] [PMID: 16885340]
[159]
Abel EV, Kim EJ, Wu J, et al. The Notch pathway is important in maintaining the cancer stem cell population in pancreatic cancer. PLoS One 2014; 9(3) e91983
[http://dx.doi.org/10.1371/journal.pone.0091983] [PMID: 24647545]
[160]
Kim TH, Shivdasani RA. Notch signaling in stomach epithelial stem cell homeostasis. J Exp Med 2011; 208(4): 677-88.
[http://dx.doi.org/10.1084/jem.20101737] [PMID: 21402740]
[161]
Pellegrinet L, Rodilla V, Liu Z, et al. Dll1- and dll4-mediated notch signaling are required for homeostasis of intestinal stem cells. Gastroenterology 2011; 140(4): 1230-40.e1, 7.
[http://dx.doi.org/10.1053/j.gastro.2011.01.005] [PMID: 21238454]
[162]
Bu P, Chen KY, Chen JH, et al. A microRNA miR-34a-regulated bimodal switch targets Notch in colon cancer stem cells. Cell Stem Cell 2013; 12(5): 602-15.
[http://dx.doi.org/10.1016/j.stem.2013.03.002] [PMID: 23642368]
[163]
López-Arribillaga E, Rodilla V, Colomer C, et al. Manic Fringe deficiency imposes Jagged1 addiction to intestinal tumor cells. Nat Commun 2018; 9(1): 2992-3005.
[http://dx.doi.org/10.1038/s41467-018-05385-0] [PMID: 30065304]
[164]
Medina V, Calvo MB, Díaz-Prado S, Espada J. Hedgehog signalling as a target in cancer stem cells. Clin Transl Oncol 2009; 11(4): 199-207.
[http://dx.doi.org/10.1007/s12094-009-0341-y] [PMID: 19380296]
[165]
Merchant AA, Matsui W. Targeting Hedgehog--a cancer stem cell pathway. Clin Cancer Res 2010; 16(12): 3130-40.
[http://dx.doi.org/10.1158/1078-0432.CCR-09-2846] [PMID: 20530699]
[166]
Heiden KB, Williamson AJ, Doscas ME, et al. The sonic hedgehog signaling pathway maintains the cancer stem cell self-renewal of anaplastic thyroid cancer by inducing snail expression. J Clin Endocrinol Metab 2014; 99(11): E2178-87.
[http://dx.doi.org/10.1210/jc.2014-1844] [PMID: 25078145]
[167]
Yang W, Liu X, Choy E, Mankin H, Hornicek FJ, Duan Z. Targeting hedgehog-GLI-2 pathway in osteosarcoma. J Orthop Res 2013; 31(3): 502-9.
[http://dx.doi.org/10.1002/jor.22230] [PMID: 22968906]
[168]
Yoon C, Park DJ, Schmidt B, et al. CD44 expression denotes a subpopulation of gastric cancer cells in which Hedgehog signaling promotes chemotherapy resistance. Clin Cancer Res 2014; 20(15): 3974-88.
[http://dx.doi.org/10.1158/1078-0432.CCR-14-0011] [PMID: 24947926]
[169]
Clement V, Sanchez P, de Tribolet N, Radovanovic I, Ruiz i Altaba A. HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr Biol 2007; 17(2): 165-72.
[http://dx.doi.org/10.1016/j.cub.2006.11.033] [PMID: 17196391]
[170]
Palma V, Lim DA, Dahmane N, et al. Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development 2005; 132(2): 335-44.
[http://dx.doi.org/10.1242/dev.01567] [PMID: 15604099]
[171]
Palma V, Ruiz i Altaba A. Hedgehog-GLI signaling regulates the behavior of cells with stem cell properties in the developing neocortex. Development 2004; 131(2): 337-45.
[http://dx.doi.org/10.1242/dev.00930] [PMID: 14681189]
[172]
Liu S, Dontu G, Mantle ID, et al. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res 2006; 66(12): 6063-71.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-0054] [PMID: 16778178]
[173]
Dierks C, Beigi R, Guo GR, et al. Expansion of Bcr-Abl-positive leukemic stem cells is dependent on Hedgehog pathway activation. Cancer Cell 2008; 14(3): 238-49.
[http://dx.doi.org/10.1016/j.ccr.2008.08.003] [PMID: 18772113]
[174]
Mizuarai S, Kawagishi A, Kotani H. Inhibition of p70S6K2 down-regulates Hedgehog/GLI pathway in non-small cell lung cancer cell lines. Mol Cancer 2009; 8(1): 44.
[http://dx.doi.org/10.1186/1476-4598-8-44] [PMID: 19575820]
[175]
Levina V, Marrangoni A, Wang T, et al. Elimination of human lung cancer stem cells through targeting of the stem cell factor-c-kit autocrine signaling loop. Cancer Res 2010; 70(1): 338-46.
[http://dx.doi.org/10.1158/0008-5472.CAN-09-1102] [PMID: 20028869]
[176]
Funayama K, Murai F, Shimane M, Nomura H, Asano S. Adhesion-induced drug resistance in leukemia stem cells. Pharmacology 2010; 86(2): 79-84.
[http://dx.doi.org/10.1159/000305344] [PMID: 20689339]
[177]
Kaplan RN, Riba RD, Zacharoulis S, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005; 438(7069): 820-7.
[http://dx.doi.org/10.1038/nature04186] [PMID: 16341007]
[178]
Cortina C, Turon G, Stork D, et al. A genome editing approach to study cancer stem cells in human tumors. EMBO Mol Med 2017; 9(7): 869-79.
[http://dx.doi.org/10.15252/emmm.201707550] [PMID: 28468934]
[179]
Virant-Klun I, Kenda-Suster N, Smrkolj S. Small putative NANOG, SOX2, and SSEA-4-positive stem cells resembling very small embryonic-like stem cells in sections of ovarian tissue in patients with ovarian cancer. J Ovarian Res 2016; 9(1): 12.
[http://dx.doi.org/10.1186/s13048-016-0221-3] [PMID: 26940129]
[180]
Li C, Ruan J, Yang M, et al. Human induced pluripotent stem cells labeled with fluorescent magnetic nanoparticles for targeted imaging and hyperthermia therapy for gastric cancer. Cancer Biol Med 2015; 12(3): 163-74.
[PMID: 26487961]

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