Updates in colorectal cancer stem cell research

Journal of Cancer Research and Therapeutics

Volumn 10, Issue 8, 2014, Pages C233-C239

  Li, Chun Jie ^a,b   Zhang, Xueqian ^c   Fan, Guan Wei ^a  

^a TIANJIN UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^b Department of Breast Cancer   (China)

^c TIANJIN HUANHU HOSPITAL   (China)

Author keywords

Biomarker; cancer stem cell; colorectal cancer; target therapy

Indexed keywords

CELL SURFACE MARKER;

CANCER RESISTANCE; CANCER STEM CELL; CELL PROLIFERATION; CELL SUBPOPULATION; CLINICAL TRIAL (TOPIC); COLORECTAL CANCER; HUMAN; MOLECULARLY TARGETED THERAPY; NONHUMAN; REVIEW; STEM CELL RESEARCH; TARGET CELL; COLORECTAL TUMOR; PATHOLOGY;

COLORECTAL NEOPLASMS; HUMANS; NEOPLASTIC STEM CELLS;

EID: 84924058970     PISSN: 09731482     EISSN: 19984138     Source Type: Journal    
DOI: 10.4103/0973-1482.151449     Document Type: Review

References (92)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin 2014;64:9-29.
2. Markowitz SD, Bertagnolli MM. Molecular origins of cancer: Molecular basis of colorectal cancer. N Engl J Med 2009;361:2449-60.
3. Zhou BB, Zhang H, Damelin M, Geles KG, Grindley JC, Dirks PB. Tumour-initiating cells: Challenges and opportunities for anticancer drug discovery. Nat Rev Drug Discov 2009;8:806-23.
4. Siegel D. Changes in colonoscopy: New tricks for an old dog. J Interv Gastroenterol 2013;3:57-58.
5. Frank NY, Schatton T, Frank MH. The therapeutic promise of the cancer stem cell concept. J Clin Invest 2010;120:41-50.
6. Zoratto F, Rossi L, Verrico M, Papa A, Basso E, Zullo A, et al. Focus on genetic and epigenetic events of colorectal cancer pathogenesis: Implications for molecular diagnosis. Tumour Biol 2014;35:6195-206.
7. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990;61:759-67.
8. Kinzler KW, Nilbert MC, Vogelstein B, Bryan TM, Levy DB, Smith KJ, et al. Identification of a gene located at chromosome 5q21 that is mutated in colorectal cancers. Science 1991;251:1366-70.
9. Nishisho I, Nakamura Y, Miyoshi Y, Miki Y, Ando H, Horii A, et al. Mutations of chromosome 5q21 genes in FAP and colorectal cancer patients. Science 1991;253:665-9.
10. Farkas SA, Vymetalkova V, Vodickova L, Vodicka P, Nilsson TK. DNA methylation changes in genes frequently mutated in sporadic colorectal cancer and in the DNA repair and Wnt/ß-catenin signaling pathway genes. Epigenomics 2014;6:179-91.
11. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B, et al. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 1997;275:1787-90.
12. Deming DA, Leystra AA, Nettekoven L, Sievers C, Miller D, Middlebrooks M, et al. PIK3CA and APC mutations are synergistic in the development of intestinal cancers. Oncogene 2014;33:2245-54.
13. Howe JR, Bair JL, Sayed MG, Anderson ME, Mitros FA, Petersen GM, et al. Germline mutations of the gene encoding bone morphogenetic protein receptor 1A in juvenile polyposis. Nat Genet 2001;28:184-7.
14. Howe JR, Roth S, Ringold JC, Summers RW, Järvinen HJ, Sistonen P, et al. Mutations in the SMAD4/DPC4 gene in juvenile polyposis. Science 1998;280:1086-8.
15. Cheah PY, Wong YH, Chau YP, Loi C, Lim KH, Lim JF, et al. Germline bone morphogenesis protein receptor 1A mutation causes colorectal tumorigenesis in hereditary mixed polyposis syndrome. Am J Gastroenterol 2009;104:3027-33.
16. Thiagalingam S, Lengauer C, Leach FS, Schutte M, Hahn SA, Overhauser J, et al. Evaluation of candidate tumour suppressor genes on chromosome 18 in colorectal cancers. Nat Genet 1996;13:343-6.
17. Fleming NI, Jorissen RN, Mouradov D, Chri s t ie M, Sakthianandeswaren A, Palmieri M, et al. SMAD2, SMAD3 and SMAD4 mutations in colorectal cancer. Cancer Res 2013;73:725-35.
18. Schwenter F, Faughnan ME, Gradinger AB, Berk T, Gryfe R, Pollett A, et al. Juvenile polyposis, hereditary hemorrhagic telangiectasia, and early onset colorectal cancer in patients with SMAD4 mutation. J Gastroenterol 2012;47:795-804.
19. Bellacosa A, Genuardi M, Anti M, Viel A, Ponz de Leon M. Hereditary nonpolyposis colorectal cancer: Review of clinical, molecular genetics, and counseling aspects. Am J Med Genet 1996;62:353-64.
20. Müller A, Korabiowska M, Brinck U. Review. DNA-mismatch repair and hereditary nonpolyposis colorectal cancer syndrome. In Vivo 2003;17:55-9.
21. Bruce WR, van der Gaag H. A quantitative assay for the number of murine lymphoma cells capable of proliferation in vivo. Nature 1963;199:79-80.
22. Hamburger AW, Salmon SE. Primary bioassay of human tumor stem cells. Science 1977;197:461-3.
23. Brunschwig A, Southam CM, Levin AG. Host resistance to cancer. Clinical experiments by homotransplants, autotransplants and admixture of autologous leucocytes. Ann Surg 1965;162:416-25.
24. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001;414:105-11.
25. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003;100:3983-8.
26. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, et al. Identification of human brain tumour initiating cells. Nature 2004;432:396-401.
27. O'Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007;445:106-10.
28. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, et al. Identification and expansion of human colon-cancer-initiating cells. Nature 2007;445:111-5.
29. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci U S A 2007;104:10158-63.
30. Papailiou J, Bramis KJ, Gazouli M, Theodoropoulos G. Stem cells in colon cancer. A new era in cancer theory begins. Int J Colorectal Dis 2011;26:1-11.
31. Lu J, Ye X, Fan F, Xia L, Bhattacharya R, Bellister S, et al. Endothelial cells promote the colorectal cancer stem cell phenotype through a soluble form of Jagged-1. Cancer Cell 2013;23:171-85.
32. Zhu L, Gibson P, Currle DS, Tong Y, Richardson RJ, Bayazitov IT, et al. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature 2009;457:603-7.
33. Vermeulen L, Todaro M, de Sousa Mello F, Sprick MR, Kemper K, Perez Alea M, et al. Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc Natl Acad Sci U S A 2008;105:13427-32.
34. Yeung TM, Gandhi SC, Wilding JL, Muschel R, Bodmer WF. Cancer stem cells from colorectal cancer-derived cell lines. Proc Natl Acad Sci U S A 2010;107:3722-7.
35. Takahashi H, Ishii H, Nishida N, Takemasa I, Mizushima T, Ikeda M, et al. Significance of Lgr5(+ve) cancer stem cells in the colon and rectum. Ann Surg Oncol 2011;18:1166-74.
36. Pang R, Law WL, Chu AC, Poon JT, Lam CS, Chow AK, et al. A subpopulation of CD26+cancer stem cells with metastatic capacity in human colorectal cancer. Cell Stem Cell 2010;6:603-15.
37. Ong CW, Kim LG, Kong HH, Low LY, Iacopetta B, Soong R, et al. CD133 expression predicts for non-response to chemotherapy in colorectal cancer. Mod Pathol 2010;23:450-7.
38. Shmelkov SV, Butler JM, Hooper AT, Hormigo A, Kushner J, Milde T, et al. CD133 expression is not restricted to stem cells, and both CD133+and CD133- metastatic colon cancer cells initiate tumors. J Clin Invest 2008;118:2111-20.
39. Li G, Liu C, Yuan J, Xiao X, Tang N, Hao J, et al. CD133(+) single cell-derived progenies of colorectal cancer cell line SW480 with different invasive and metastatic potential. Clin Exp Metastasis 2010;27:517-27.
40. Weichert W, Knösel T, Bellach J, Dietel M, Kristiansen G. ALCAM/CD166 is overexpressed in colorectal carcinoma and correlates with shortened patient survival. J Clin Pathol 2004;57:1160-4.
41. Frank NY, Margaryan A, Huang Y, Schatton T, Waaga-Gasser AM, Gasser M, et al. ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma. Cancer Res 2005;65:4320-33.
42. Haraguchi N, Ohkuma M, Sakashita H, Matsuzaki S, Tanaka F, Mimori K, et al. CD133+CD44+population efficiently enriches colon cancer initiating cells. Ann Surg Oncol 2008;15:2927-33.
43. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, Appelman H, et al. Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 2009;69:3382-9.
44. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007;449:1003-7.
45. Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M, et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 2009;457:608-11.
46. Du L, Wang H, He L, Zhang J, Ni B, Wang X, et al. CD44 is of functional importance for colorectal cancer stem cells. Clin Cancer Res 2008;14:6751-60.
47. Zeilstra J, Joosten SP, Dokter M, Verwiel E, Spaargaren M, Pals ST. Deletion of the WNT target and cancer stem cell marker CD44 in Apc(Min/+) mice attenuates intestinal tumorigenesis. Cancer Res 2008;68:3655-61.
48. Ponta H, Sherman L, Herrlich PA. CD44: From adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 2003;4:33-45.
49. Ishimoto T, Oshima H, Oshima M, Kai K, Torii R, Masuko T, et al. CD44+slow-cycling tumor cell expansion is triggered by cooperative actions of Wnt and prostaglandin E2 in gastric tumorigenesis. Cancer Sci 2010;101:673-8.
50. Dissanayake SK, Wade M, Johnson CE, O'Connell MP, Leotlela PD, French AD, et al. The Wnt5A/protein kinase C pathway mediates motility in melanoma cells via the inhibition of metastasis suppressors and initiation of an epithelial to mesenchymal transition. J Biol Chem 2007;282:17259-71.
51. Vermeulen L, De Sousa E Melo F, van der Heijden M, Cameron K, de Jong JH, Borovski T, et al. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol 2010;12:468-76.
52. Long H, Zhang S, Liu C, Shi J, Tao L, Situ D, et al. Characterization of a stem cell population in lung cancer cell line Glc-82. Thorac Cancer 2012;3:8-18.
53. Kahi CJ. Chromocolonoscopy for colorectal cancer screening: Dive into the Big Blue. J Interv Gastroenterol 2012;2:112-13.
54. nd, et al. Chemoresistant colorectal cancer cells, the cancer stem cell phenotype, and increased sensitivity to insulin-like growth factor-I receptor inhibition. Cancer Res 2009;69:1951-7.
55. Todaro M, Alea MP, Di Stefano AB, Cammareri P, Vermeulen L, Iovino F, et al. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell 2007;1:389-402.
56. Cammareri P, Scopelliti A, Todaro M, Eterno V, Francescangeli F, Moyer MP, et al. Aurora - A is essential for the tumorigenic capacity and chemoresistance of colorectal cancer stem cells. Cancer Res 2010;70:4655-65.
57. Song B, Wang Y, Xi Y, Kudo K, Bruheim S, Botchkina GI, et al. Mechanism of chemoresistance mediated by miR-140 in human osteosarcoma and colon cancer cells. Oncogene 2009;28:4065-74.
58. Song B, Wang Y, Titmus MA, Botchkina G, Formentini A, Kornmann M, et al. Molecular mechanism of chemoresistance by miR-215 in osteosarcoma and colon cancer cells. Mol Cancer 2010;9:96.
59. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: Role of ATP-dependent transporters. Nat Rev Cancer 2002;2:48-58.
60. Ejendal KF, Hrycyna CA. Multidrug resistance and cancer: The role of the human ABC transporter ABCG2. Curr Protein Pept Sci 2002;3:503-11.
61. Riordan JR, Deuchars K, Kartner N, Alon N, Trent J, Ling V. Amplification of P-glycoprotein genes in multidrug-resistant mammalian cell lines. Nature 1985;316:817-9.
62. Frank NY, Pendse SS, Lapchak PH, Margaryan A, Shlain D, Doeing C, et al. Regulation of progenitor cell fusion by ABCB5 P-glycoprotein, a novel human ATP-binding cassette transporter. J Biol Chem 2003;278:47156-65.
63. Huang Y, Anderle P, Bussey KJ, Barbacioru C, Shankavaram U, Dai Z, et al. Membrane transporters and channels: Role of the transportome in cancer chemosensitivity and chemoresistance. Cancer Res 2004;64:4294-301.
64. Elliott AM, Al-Hajj MA. ABCB8 mediates doxorubicin resistance in melanoma cells by protecting the mitochondrial genome. Mol Cancer Res 2009;7:79-87.
65. Cheung ST, Cheung PF, Cheng CK, Wong NC, Fan ST. Granulin-epithelin precursor and ATP-dependent binding cassette (ABC) B5 regulate liver cancer cell chemoresistance. Gastroenterology 2011;140:344-55.
66. Fukunaga-Kalabis M, Martinez G, Nguyen TK, Kim D, Santiago-Walker A, Roesch A, et al. Tenascin-C promotes melanoma progression by maintaining the ABCB5-positive side population. Oncogene 2010;29:6115-24.
67. Wilson BJ, Saab KR, Ma J, Schatton T, Pütz P, Zhan Q, et al. ABCB5 maintains melanoma-initiating cells through a proinflammatory cytokine signaling circuit. Cancer Res 2014;74:4196-207.
68. Farawela HM, Khorshied MM, Kassem NM, Kassem HA, Zawam HM. The clinical relevance and prognostic significance of adenosine triphosphate ATP-binding cassette (ABCB5) and multidrug resistance (MDR1) genes expression in acute leukemia: An Egyptian study. J Cancer Res Clin Oncol 2014;140:1323-30.
69. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006;444:756-60.
70. Saigusa S, Tanaka K, Toiyama Y, Yokoe T, Okugawa Y, Koike Y, et al. Clinical significance of CD133 and hypoxia inducible factor-1a gene expression in rectal cancer after preoperative chemoradiotherapy. Clin Oncol (R Coll Radiol) 2011;23:323-32.
71. Saigusa S, Tanaka K, Toiyama Y, Yokoe T, Okugawa Y, Kawamoto A, et al. Immunohistochemical features of CD133 expression: Association with resistance to chemoradiotherapy in rectal cancer. Oncol Rep 2010;24:345-50.
72. Seal BS, Sullivan SD, Ramsey SD, Shermock KM, Ren J, Kreilick C, et al. Systemic therapy for colorectal cancer: Patterns of chemotherapy and biologic therapy use in nationally representative US claims database. BioDrugs 2014;28:229-36.
73. Meyerhardt JA, Mayer RJ. Systemic therapy for colorectal cancer. N Engl J Med 2005;352:476-87.
74. Chen X, Liu Y, Yang HW, Zhou S, Cheng C, Zheng MW, et al. SKLB-287, a?novel oral multikinase inhibitor of EGFR and VEGFR2, exhibits potent antitumor activity in LoVo colorectal tumor model. Neoplasma 2014;61:514-22.
75. Takahashi Y, Kitadai Y, Bucana CD, Cleary KR, Ellis LM. Expression of vascular endothelial growth factor and its receptor, KDR, correlates with vascularity, metastasis, and proliferation of human colon cancer. Cancer Res 1995;55:3964-8.
76. Fan F, Wey JS, McCarty MF, Belcheva A, Liu W, Bauer TW, et al. Expression and function of vascular endothelial growth factor receptor-1 on human colorectal cancer cells. Oncogene 2005;24:2647-53.
77. Feng QY, Wei Y, Chen JW, Chang WJ, Ye LC, Zhu DX, et al. Anti-EGFR and anti-VEGF agents: Important targeted therapies of colorectal liver metastases. World J Gastroenterol 2014;20:4263-75.
78. Wu WK, Wang XJ, Cheng AS, Luo MX, Ng SS, To KF, et al. Dysregulation and crosstalk of cellular signaling pathways in colon carcinogenesis. Crit Rev Oncol Hematol 2013;86:251-77.
79. Zhang K, Civan J, Mukherjee S, Patel F, Yang H. Genetic variations in colorectal cancer risk and clinical outcome. World J Gastroenterol 2014;20:4167-77.
80. Hsu HC, Liu YS, Tseng KC, Tan BC, Chen SJ, Chen HC. LGR5 regulates survival through mitochondria-mediated apoptosis and by targeting the Wnt/ß-catenin signaling pathway in colorectal cancer cells. Cell Signal 2014;26:2333-42.
81. He S, Zhou H, Zhu X, Hu S, Fei M, Wan D, et al. Expression of Lgr5, a marker of intestinal stem cells, in colorectal cancer and its clinicopathological significance. Biomed Pharmacother 2014;68:507-13.
82. Todaro M, Gaggianesi M, Catalano V, Benfante A, Iovino F, Biffoni M, et al. CD44v6 is a marker of constitutive and reprogrammed cancer stem cells driving colon cancer metastasis. Cell Stem Cell 2014;14:342-56.
83. Sikandar SS, Pate KT, Anderson S, Dizon D, Edwards RA, Waterman ML, et al. NOTCH signaling is required for formation and self-renewal of tumor-initiating cells and for repression of secretory cell differentiation in colon cancer. Cancer Res 2010;70:1469-78.
84. van Es JH, van Gijn ME, Riccio O, van den Born M, Vooijs M, Begthel H, et al. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 2005;435:959-63.
85. Whissell G, Montagni E, Martinelli P, Hernando-Momblona X, Sevillano M, Jung P, et al. The transcription factor GATA6 enables self-renewal of colon adenoma stem cells by repressing BMP gene expression. Nat Cell Biol 2014;16:695-707.
86. Haramis AP, Begthel H, van den Born M, van Es J, Jonkheer S, Offerhaus GJ, et al. De novo crypt formation and juvenile polyposis on BMP inhibition in mouse intestine. Science 2004;303:1684-6.
87. Kodach LL, Bleuming SA, Musler AR, Peppelenbosch MP, Hommes DW, van den Brink GR, et al. The bone morphogenetic protein pathway is active in human colon adenomas and inactivated in colorectal cancer. Cancer 2008;112:300-6.
88. Lombardo Y, Scopelliti A, Cammareri P, Todaro M, Iovino F, Ricci-Vitiani L, et al. Bone morphogenetic protein 4 induces differentiation of colorectal cancer stem cells and increases their response to chemotherapy in mice. Gastroenterology 2011;140:297-309.
89. Ricci-Vitiani L, Mollinari C, di Martino S, Biffoni M, Pilozzi E, Pagliuca A, et al. Thymosin beta4 targeting impairs tumorigenic activity of colon cancer stem cells. FASEB J 2010;24:4291-301.
90. Kim JW, Dang CV. Cancer's molecular sweet tooth and the Warburg effect. Cancer Res 2006;66:8927-30.
91. Bui T, Thompson CB. Cancer's sweet tooth. Cancer Cell 2006;9:419-20.
92. Akao Y, Noguchi S, Iio A, Kojima K, Takagi T, Naoe T. Dysregulation of microRNA-34a expression causes drug-resistance to 5-FU in human colon cancer DLD-1 cells. Cancer Lett 2011;300:197-204.