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Abstract

Colorectal cancer (CRC) is the third most common cancer and the second leading cause of cancer deaths in the United States with over 50,000 deaths per year. The sporadic colorectal cancer, which occurs in ~80 % of the patients, is an age-related disease, the incidence of which rises dramatically after 50 years of age. According to stochastic model of sporadic cancer, it was thought that all cancer cells that possess driver mutation(s) will lead to the process of carcinogenesis. However, in recent years, numerous studies have appeared to challenge the stochastic model. It is becoming increasingly accepted that not all, but only a small sub-population of pluripotent self-renewing tumor cells that are termed as cancer stem cells (CSC) play a determinant role in the development and progression of many malignancies, including colorectal cancer. The focus of this book chapter is to briefly describe the role of cancer stem cells in recurrence of colorectal cancer, which leads to metastasis and remains a major clinical challenge. Although the underlying biochemical and molecular events leading to recurrence of various malignancies are not fully understood, CSCs that have been shown to be resistant to conventional chemotherapy play pivotal role in these processes. While the origin of CSCs is not fully known they are thought to be derived from mutations in normal stem, progenitor or differentiated cells. Despite recent advances in medicine, nearly 50 % of the patients develop recurrence of colon tumor that is highly enriched in CSCs. Unfortunately the conventional chemotherapy has shown limited success in treating recurrent cancer. This underscores the need for development of novel treatment strategies for recurrent colon cancer by targeting CSCs. Attempts are being made to target CSCs utilizing combination of chemotherapy and specific inhibitors of growth factor receptors or signal transduction. In addition, efforts have also been made to utilize non-toxic natural agent(s), either alone or in combination with conventional chemotherapy.

Author contributed equally with all other contributors

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References

  • Aoki K, Taketo MM (2007) Adenomatous polyposis coli (APC): a multi-functional tumor suppressor gene. J Cell Sci 120(Pt 19):3327–3335

    CAS  PubMed  Google Scholar 

  • Babashah S, Soleimani M (2011) The oncogenic and tumuor suppressive roles of miRNAs in cancer and apoptosis. Eur. J. Cancer 47(8):1127–1137. doi:10.1016/j.ejca

  • Babashah S (ed) (2014) MicroRNAs: key regulators of oncogenesis. Springer International Publishing, Switzerland, pp 3–28

    Google Scholar 

  • Baker SJ, Preisinger AC, Jessup JM, Paraskeva C, Markowitz S, Willson JK et al (1990) p53 gene mutations occur in combination with 17p allelic deletions as late events in colorectal tumorigenesis. Cancer Res 50(23):7717–7722

    CAS  PubMed  Google Scholar 

  • Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M et al (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449(7165):1003–1007

    CAS  PubMed  Google Scholar 

  • Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M et al (2009) Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457(7229):608–611

    CAS  PubMed  Google Scholar 

  • Battelli C, Nikopoulos GN, Mitchell JG, Verdi JM (2006) The RNA-binding protein Musashi-1 regulates neural development through the translational repression of p21WAF-1. Mol Cell Neurosci 31(1):85–96

    CAS  PubMed  Google Scholar 

  • Bissell MJ, Labarge MA (2005) Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment? Cancer Cell 7(1):17–23

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bozza PT, Viola JP (2010) Lipid droplets in inflammation and cancer. Prostaglandins Leukot Essent Fatty Acids 82(4–6):243–250

    CAS  PubMed  Google Scholar 

  • Brocardo M, Henderson BR (2008) APC shuttling to the membrane, nucleus and beyond. Trends Cell Biol 18(12):587–596

    CAS  PubMed  Google Scholar 

  • Buczacki SJ, Zecchini HI, Nicholson AM, Russell R, Vermeulen L, Kemp R et al (2013) Intestinal label-retaining cells are secretory precursors expressing Lgr5. Nature 495(7439):65–69

    CAS  PubMed  Google Scholar 

  • Burness ML, Sipkins DA (2010) The stem cell niche in health and malignancy. Semin Cancer Biol 20(2):107–115

    PubMed  Google Scholar 

  • Chaffer CL, Weinberg RA (2011) A perspective on cancer cell metastasis. Science 331(6024):1559–1564

    CAS  PubMed  Google Scholar 

  • Chu P, Clanton DJ, Snipas TS, Lee J, Mitchell E, Nguyen ML et al (2009) Characterization of a subpopulation of colon cancer cells with stem cell-like properties. Int J Cancer 124(6):1312–1321

    CAS  PubMed  Google Scholar 

  • Clevers H (2011) The cancer stem cell: premises, promises and challenges. Nat Med 17(3):313–319

    CAS  PubMed  Google Scholar 

  • Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW et al (2007) Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 104(24):10158–10163

    PubMed Central  CAS  PubMed  Google Scholar 

  • Das G, La Rocca R, Lakshmikanth T, Gentile F, Tallerico R, Zambetti LP et al (2010) Monitoring human leukocyte antigen class I molecules by micro-Raman spectroscopy at single-cell level. J Biomed Opt 15(2):027007

    PubMed  Google Scholar 

  • Dean M, Fojo T, Bates S (2005) Tumour stem cells and drug resistance. Nat Rev Cancer 5(4):275–284

    CAS  PubMed  Google Scholar 

  • Deonarain MP, Kousparou CA, Epenetos AA (2009) Antibodies targeting cancer stem cells: a new paradigm in immunotherapy? MAbs 1(1):12–25

    PubMed Central  PubMed  Google Scholar 

  • Dick JE (2008) Stem cell concepts renew cancer research. Blood 112(13):4793–4807

    CAS  PubMed  Google Scholar 

  • Eilers M, Eisenman RN (2008) Myc’s broad reach. Genes Dev 22(20):2755–2766

    PubMed Central  CAS  PubMed  Google Scholar 

  • Farese RV Jr, Walther TC (2009) Lipid droplets finally get a little R-E-S-P-E-C-T. Cell 139(5):855–860

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fearon ER (2011) Molecular genetics of colorectal cancer. Annu Rev Pathol 6:479–507

    CAS  PubMed  Google Scholar 

  • Fearon ER, Vogelstein B (1990) A genetic model for colorectal tumorigenesis. Cell 61(5):759–767

    CAS  PubMed  Google Scholar 

  • Feng HL, Liu YQ, Yang LJ, Bian XC, Yang ZL, Gu B et al (2010) Expression of CD133 correlates with differentiation of human colon cancer cells. Cancer Biol Ther 9(3):216–223

    CAS  PubMed  Google Scholar 

  • Fitzgerald TL, Rangan S, Dobbs L, Starr S, Sigounas G (2014) The impact of Aldehyde dehydrogenase 1 expression on prognosis for metastatic colon cancer. J Surg Res 192(1):82–89

    CAS  PubMed  Google Scholar 

  • Fletcher JI, Haber M, Henderson MJ, Norris MD (2010) ABC transporters in cancer: more than just drug efflux pumps. Nat Rev Cancer 10(2):147–156

    CAS  PubMed  Google Scholar 

  • Frank NY, Schatton T, Frank MH (2010) The therapeutic promise of the cancer stem cell concept. J Clin Invest 120(1):41–50

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fujimoto K, Beauchamp RD, Whitehead RH (2002) Identification and isolation of candidate human colonic clonogenic cells based on cell surface integrin expression. Gastroenterology 123(6):1941–1948

    CAS  PubMed  Google Scholar 

  • Gazzaniga P, Gradilone A, Petracca A, Nicolazzo C, Raimondi C, Iacovelli R et al (2010) Molecular markers in circulating tumour cells from metastatic colorectal cancer patients. J Cell Mol Med 14(8):2073–2077

    PubMed Central  CAS  PubMed  Google Scholar 

  • Glazer RI, Vo DT, Penalva LO (2012) Musashi1: an RBP with versatile functions in normal and cancer stem cells. Front Biosci 17:54–64

    CAS  Google Scholar 

  • Goossens-Beumer IJ, Zeestraten EC, Benard A, Christen T, Reimers MS, Keijzer R et al (2014) Clinical prognostic value of combined analysis of Aldh1, Survivin, and EpCAM expression in colorectal cancer. Br J Cancer 110(12):2935–2944

    PubMed Central  CAS  PubMed  Google Scholar 

  • Grosse-Gehling P, Fargeas CA, Dittfeld C, Garbe Y, Alison MR, Corbeil D et al (2013) CD133 as a biomarker for putative cancer stem cells in solid tumours: limitations, problems and challenges. J Pathol 229(3):355–378

    CAS  PubMed  Google Scholar 

  • Han Y, Xue X, Jiang M, Guo X, Li P, Liu F et al (2015) LGR5, a relevant marker of cancer stem cells, indicates a poor prognosis in colorectal cancer patients: a meta-analysis. Clin Res Hepatol Gastroenterol 39:267–273, pii:S2210-7401(14)00171-5

    Google Scholar 

  • Harradine KA, Akhurst RJ (2006) Mutations of TGFbeta signaling molecules in human disease. Ann Med 38(6):403–414

    CAS  PubMed  Google Scholar 

  • Horst D, Kriegl L, Engel J, Kirchner T, Jung A (2009) Prognostic significance of the cancer stem cell markers CD133, CD44, and CD166 in colorectal cancer. Cancer Invest 27(8):844–850

    PubMed  Google Scholar 

  • Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, Appelman H et al (2009) Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 69(8):3382–3389

    PubMed Central  CAS  PubMed  Google Scholar 

  • Iinuma H, Watanabe T, Mimori K, Adachi M, Hayashi N, Tamura J et al (2011) Clinical significance of circulating tumor cells, including cancer stem-like cells, in peripheral blood for recurrence and prognosis in patients with Dukes’ stage B and C colorectal cancer. J Clin Oncol 29(12):1547–1555

    PubMed  Google Scholar 

  • Imai T, Tokunaga A, Yoshida T, Hashimoto M, Mikoshiba K, Weinmaster G et al (2001) The neural RNA-binding protein Musashi1 translationally regulates mammalian numb gene expression by interacting with its mRNA. Mol Cell Biol 21(12):3888–3900

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kanwar SS, Yu Y, Nautiyal J, Patel BB, Majumdar AP (2010) The Wnt/beta-catenin pathway regulates growth and maintenance of colonospheres. Mol Cancer 9:212

    PubMed Central  PubMed  Google Scholar 

  • Kanwar SS, Yu Y, Nautiyal J, Patel BB, Padhye S, Sarkar FH et al (2011) Difluorinated-curcumin (CDF): a novel curcumin analog is a potent inhibitor of colon cancer stem-like cells. Pharm Res 28(4):827–838

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kemper K, Grandela C, Medema JP (2010) Molecular identification and targeting of colorectal cancer stem cells. Oncotarget 1(6):387–395

    PubMed Central  PubMed  Google Scholar 

  • Kinzler KW, Vogelstein B (1996) Lessons from hereditary colorectal cancer. Cell 87(2):159–170

    CAS  PubMed  Google Scholar 

  • Krahmer N, Guo Y, Farese RV Jr, Walther TC (2009) SnapShot: lipid droplets. Cell 139(5):1024.e1021

    Google Scholar 

  • Kreso A, van Galen P, Pedley NM, Lima-Fernandes E, Frelin C, Davis T et al (2014) Self-renewal as a therapeutic target in human colorectal cancer. Nat Med 20(1):29–36

    CAS  PubMed  Google Scholar 

  • Kuhnle M, Egger M, Muller C, Mahringer A, Bernhardt G, Fricker G et al (2009) Potent and selective inhibitors of breast cancer resistance protein (ABCG2) derived from the p-glycoprotein (ABCB1) modulator tariquidar. J Med Chem 52(4):1190–1197

    PubMed  Google Scholar 

  • Lampropoulos P, Zizi-Sermpetzoglou A, Rizos S, Kostakis A, Nikiteas N, Papavassiliou AG (2012) TGF-beta signalling in colon carcinogenesis. Cancer Lett 314(1):1–7

    CAS  PubMed  Google Scholar 

  • Langan RC, Mullinax JE, Raiji MT, Upham T, Summers T, Stojadinovic A et al (2013) Colorectal cancer biomarkers and the potential role of cancer stem cells. J Cancer 4(3):241–250

    PubMed Central  PubMed  Google Scholar 

  • Leary RJ, Lin JC, Cummins J, Boca S, Wood LD, Parsons DW et al (2008) Integrated analysis of homozygous deletions, focal amplifications, and sequence alterations in breast and colorectal cancers. Proc Natl Acad Sci USA 105(42):16224–16229

    PubMed Central  CAS  PubMed  Google Scholar 

  • Levin TG, Powell AE, Davies PS, Silk AD, Dismuke AD, Anderson EC et al (2010) Characterization of the intestinal cancer stem cell marker CD166 in the human and mouse gastrointestinal tract. Gastroenterology 139(6):2072.e2075–2082.e2075

    Google Scholar 

  • Lugli A, Iezzi G, Hostettler I, Muraro MG, Mele V, Tornillo L et al (2010) Prognostic impact of the expression of putative cancer stem cell markers CD133, CD166, CD44s, EpCAM, and ALDH1 in colorectal cancer. Br J Cancer 103(3):382–390

    PubMed Central  CAS  PubMed  Google Scholar 

  • Malumbres M, Barbacid M (2003) RAS oncogenes: the first 30 years. Nat Rev Cancer 3(6):459–465

    CAS  PubMed  Google Scholar 

  • Markowitz SD, Bertagnolli MM (2009) Molecular origins of cancer: molecular basis of colorectal cancer. N Engl J Med 361(25):2449–2460

    PubMed Central  CAS  PubMed  Google Scholar 

  • Medema JP, Vermeulen L (2011) Microenvironmental regulation of stem cells in intestinal homeostasis and cancer. Nature 474(7351):318–326

    CAS  PubMed  Google Scholar 

  • Muraro MG, Mele V, Daster S, Han J, Heberer M, Cesare Spagnoli G et al (2012) CD133+, CD166 + CD44+, and CD24 + CD44+ phenotypes fail to reliably identify cell populations with cancer stem cell functional features in established human colorectal cancer cell lines. Stem Cells Transl Med 1(8):592–603

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nakamura M, Okano H, Blendy JA, Montell C (1994) Musashi, a neural RNA-binding protein required for Drosophila adult external sensory organ development. Neuron 13(1):67–81

    CAS  PubMed  Google Scholar 

  • Nishimura S, Wakabayashi N, Toyoda K, Kashima K, Mitsufuji S (2003) Expression of Musashi-1 in human normal colon crypt cells: a possible stem cell marker of human colon epithelium. Dig Dis Sci 48(8):1523–1529

    CAS  PubMed  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(7123):106–110

    PubMed  Google Scholar 

  • Ozawa M, Ichikawa Y, Zheng YW, Oshima T, Miyata H, Nakazawa K et al (2014) Prognostic significance of CD44 variant 2 upregulation in colorectal cancer. Br J Cancer 111(2):365–374

    PubMed Central  CAS  PubMed  Google Scholar 

  • Paldino E, Tesori V, Casalbore P, Gasbarrini A, Puglisi MA (2014) Tumor initiating cells and chemoresistance: which is the best strategy to target colon cancer stem cells? BioMed Res Int 2014:859871

    PubMed Central  PubMed  Google Scholar 

  • Patel BB, Yu Y, Du J, Levi E, Phillip PA, Majumdar AP (2009) Age-related increase in colorectal cancer stem cells in macroscopically normal mucosa of patients with adenomas: a risk factor for colon cancer. Biochem Biophys Res Commun 378(3):344–347

    PubMed Central  CAS  PubMed  Google Scholar 

  • Peters GJ, Backus HH, Freemantle S, van Triest B, Codacci-Pisanelli G, van der Wilt CL et al (2002) Induction of thymidylate synthase as a 5-fluorouracil resistance mechanism. Biochim Biophys Acta 1587(2–3):194–205

    CAS  PubMed  Google Scholar 

  • Pirozzi G, Tirino V, Camerlingo R, La Rocca A, Martucci N, Scognamiglio G et al (2013) Prognostic value of cancer stem cells, epithelial-mesenchymal transition and circulating tumor cells in lung cancer. Oncol Rep 29(5):1763–1768

    CAS  PubMed  Google Scholar 

  • Polakis P (2007) The many ways of Wnt in cancer. Curr Opin Genet Dev 17(1):45–51

    CAS  PubMed  Google Scholar 

  • Ponz de Leon M, Di Gregorio C (2001) Pathology of colorectal cancer. Dig Liver Dis 33(4):372–388

    CAS  PubMed  Google Scholar 

  • Puglisi MA, Sgambato A, Saulnier N, Rafanelli F, Barba M, Boninsegna A et al (2009) Isolation and characterization of CD133+ cell population within human primary and metastatic colon cancer. Eur Rev Med Pharmacol Sci 13(Suppl 1):55–62

    PubMed  Google Scholar 

  • Puglisi MA, Barba M, Corbi M, Errico MF, Giorda E, Saulnier N et al (2011) Identification of Endothelin-1 and NR4A2 as CD133-regulated genes in colon cancer cells. J Pathol 225(2):305–314

    CAS  PubMed  Google Scholar 

  • Rattan R, Ali Fehmi R, Munkarah A (2012) Metformin: an emerging new therapeutic option for targeting cancer stem cells and metastasis. J Oncol 2012:928127

    PubMed Central  PubMed  Google Scholar 

  • Ren F, Sheng WQ, Du X (2013) CD133: a cancer stem cells marker, is used in colorectal cancers. World J Gastroenterol 19(17):2603–2611

    PubMed Central  CAS  PubMed  Google Scholar 

  • Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414(6859):105–111

    CAS  PubMed  Google Scholar 

  • Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C et al (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445(7123):111–115

    CAS  PubMed  Google Scholar 

  • Robey RW, Polgar O, Deeken J, To KW, Bates SE (2007) ABCG2: determining its relevance in clinical drug resistance. Cancer Metastasis Rev 26(1):39–57

    CAS  PubMed  Google Scholar 

  • Ruggero D (2009) The role of Myc-induced protein synthesis in cancer. Cancer Res 69(23):8839–8843

    PubMed Central  CAS  PubMed  Google Scholar 

  • Samuels Y, Wang Z, Bardelli A, Silliman N, Ptak J, Szabo S et al (2004) High frequency of mutations of the PIK3CA gene in human cancers. Science 304(5670):554

    CAS  PubMed  Google Scholar 

  • Sangiorgi E, Capecchi MR (2008) Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet 40(7):915–920

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE et al (2009) Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459(7244):262–265

    CAS  PubMed  Google Scholar 

  • Schepers AG, Snippert HJ, Stange DE, van den Born M, van Es JH, van de Wetering M et al (2012) Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas. Science 337(6095):730–735

    CAS  PubMed  Google Scholar 

  • Shmelkov SV, Butler JM, Hooper AT, Hormigo A, Kushner J, Milde T et al (2008) CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J Clin Invest 118(6):2111–2120

    PubMed Central  CAS  PubMed  Google Scholar 

  • Singh A, Settleman J (2010) EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 29(34):4741–4751

    PubMed Central  CAS  PubMed  Google Scholar 

  • Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T et al (2004) Identification of human brain tumour initiating cells. Nature 432(7015):396–401

    CAS  PubMed  Google Scholar 

  • Stenvang J, Petri A, Lindow M, Obad S, Kauppinen S (2012) Inhibition of microRNA function by antimiR oligonucleotides. Silence 3(1):1

    PubMed Central  CAS  PubMed  Google Scholar 

  • Stewart DJ, Chiritescu G, Dahrouge S, Banerjee S, Tomiak EM (2007) Chemotherapy dose–response relationships in non-small cell lung cancer and implied resistance mechanisms. Cancer Treat Rev 33(2):101–137

    CAS  PubMed  Google Scholar 

  • Suzuki HI, Yamagata K, Sugimoto K, Iwamoto T, Kato S, Miyazono K (2009) Modulation of microRNA processing by p53. Nature 460(7254):529–533

    CAS  PubMed  Google Scholar 

  • Takubo K, Ohmura M, Azuma M, Nagamatsu G, Yamada W, Arai F et al (2008) Stem cell defects in ATM-deficient undifferentiated spermatogonia through DNA damage-induced cell-cycle arrest. Cell Stem Cell 2(2):170–182

    CAS  PubMed  Google Scholar 

  • ten Dijke P, Hill CS (2004) New insights into TGF-beta-Smad signalling. Trends Biochem Sci 29(5):265–273

    PubMed  Google Scholar 

  • Tian H, Biehs B, Warming S, Leong KG, Rangell L, Klein OD et al (2011) A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 478(7368):255–259

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tirinato L, Liberale C, Di Franco S, Candeloro P, Benfante A, La Rocca R et al (2014) Lipid droplets: a new player in colorectal cancer stem cells unveiled by spectroscopic imaging. Stem Cells 33(1):35–44

    PubMed Central  Google Scholar 

  • Todaro M, Perez Alea M, Scopelliti A, Medema JP, Stassi G (2008) IL-4-mediated drug resistance in colon cancer stem cells. Cell Cycle 7(3):309–313

    CAS  PubMed  Google Scholar 

  • Todaro M, Francipane MG, Medema JP, Stassi G (2010) Colon cancer stem cells: promise of targeted therapy. Gastroenterology 138(6):2151–2162

    CAS  PubMed  Google Scholar 

  • Touil Y, Igoudjil W, Corvaisier M, Dessein AF, Vandomme J, Monte D et al (2014) Colon cancer cells escape 5FU chemotherapy-induced cell death by entering stemness and quiescence associated with the c-Yes/YAP axis. Clin Cancer Res 20(4):837–846

    PubMed Central  CAS  PubMed  Google Scholar 

  • Vaiopoulos AG, Kostakis ID, Koutsilieris M, Papavassiliou AG (2012) Colorectal cancer stem cells. Stem Cells 30(3):363–371

    CAS  PubMed  Google Scholar 

  • Vasudevan A, Yu Y, Banerjee S, Woods J, Farhana L, Rajendra SG et al (2014) Omega-3 fatty acid is a potential preventive agent for recurrent colon cancer. Cancer Prev Res 7(11):1138–1148

    CAS  Google Scholar 

  • Vermeulen L, De Sousa EMF, van der Heijden M, Cameron K, de Jong JH, Borovski T et al (2010) Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol 12(5):468–476

    CAS  PubMed  Google Scholar 

  • Visvader JE, Lindeman GJ (2008) Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 8(10):755–768

    CAS  PubMed  Google Scholar 

  • Vries RG, Huch M, Clevers H (2010) Stem cells and cancer of the stomach and intestine. Mol Oncol 4(5):373–384

    PubMed  Google Scholar 

  • Walker F, Zhang HH, Odorizzi A, Burgess AW (2011) LGR5 is a negative regulator of tumourigenicity, antagonizes Wnt signalling and regulates cell adhesion in colorectal cancer cell lines. PLoS One 6(7), e22733

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wang JC, Dick JE (2005) Cancer stem cells: lessons from leukemia. Trends Cell Biol 15(9):494–501

    CAS  PubMed  Google Scholar 

  • Weichert W, Knosel T, Bellach J, Dietel M, Kristiansen G (2004) ALCAM/CD166 is overexpressed in colorectal carcinoma and correlates with shortened patient survival. J Clin Pathol 57(11):1160–1164

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wood LD, Parsons DW, Jones S, Lin J, Sjoblom T, Leary RJ et al (2007) The genomic landscapes of human breast and colorectal cancers. Science 318(5853):1108–1113

    CAS  PubMed  Google Scholar 

  • Woodhouse EC, Chuaqui RF, Liotta LA (1997) General mechanisms of metastasis. Cancer 80(8 Suppl):1529–1537

    CAS  PubMed  Google Scholar 

  • Xiong B, Ma L, Hu X, Zhang C, Cheng Y (2014) Characterization of side population cells isolated from the colon cancer cell line SW480. Int J Oncol 45(3):1175–1183

    CAS  PubMed  Google Scholar 

  • Yamamoto S, Tanaka K, Takeda K, Akiyama H, Ichikawa Y, Nagashima Y et al (2014) Patients with CD133-negative colorectal liver metastasis have a poor prognosis after hepatectomy. Ann Surg Oncol 21(6):1853–1861

    PubMed  Google Scholar 

  • Yan KS, Chia LA, Li X, Ootani A, Su J, Lee JY et al (2012) The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations. Proc Natl Acad Sci USA 109(2):466–471

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yang K, Chen XZ, Zhang B, Yang C, Chen HN, Chen ZX et al (2011) Is CD133 a biomarker for cancer stem cells of colorectal cancer and brain tumors? A meta-analysis. Int J Biol Markers 26(3):173–180

    CAS  PubMed  Google Scholar 

  • Yu Y, Kanwar SS, Patel BB, Nautiyal J, Sarkar FH, Majumdar AP (2009) Elimination of colon cancer stem-like cells by the combination of curcumin and FOLFOX. Transl Oncol 2(4):321–328

    PubMed Central  PubMed  Google Scholar 

  • Yu Y, Kanwar SS, Patel BB, Oh PS, Nautiyal J, Sarkar FH et al (2012) MicroRNA-21 induces stemness by downregulating transforming growth factor beta receptor 2 (TGFbetaR2) in colon cancer cells. Carcinogenesis 33(1):68–76

    PubMed Central  PubMed  Google Scholar 

  • Yu Y, Sarkar FH, Majumdar AP (2013) Down-regulation of miR-21 induces differentiation of chemoresistant colon cancer cells and enhances susceptibility to therapeutic regimens. Transl Oncol 6(2):180–186

    PubMed Central  PubMed  Google Scholar 

  • Yu Y, Nangia-Makker P, Majumdar AP (2014) Overcoming drug resistance in colorectal cancer by microRNAs. In: Sarkar FH (ed) microRNA targeted cancer therapy. Springer, Switzerland, pp 139–155

    Google Scholar 

  • Zhou BB, Zhang H, Damelin M, Geles KG, Grindley JC, Dirks PB (2009) Tumour-initiating cells: challenges and opportunities for anticancer drug discovery. Nat Rev Drug Discov 8(10):806–823

    CAS  PubMed  Google Scholar 

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Nangia-Makker, P., Yu, Y., Farhana, L., Ahmed, K., Majumdar, A.P.N. (2015). Colorectal Cancer Stem Cells. In: Babashah, S. (eds) Cancer Stem Cells: Emerging Concepts and Future Perspectives in Translational Oncology. Springer, Cham. https://doi.org/10.1007/978-3-319-21030-8_9

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