Radiotherapy & Oncology
Volume 94, Issue 3 , Pages 375-383 , March 2010

CD133 expression is not selective for tumor-initiating or radioresistant cell populations in the CRC cell line HCT-116

  • Claudia Dittfeld

      Affiliations

    • Tumor Pathophysiology, OncoRay – Center for Radiation Research in Oncology, Dresden University of Technology, Germany
    • Contributed equally.
    • ,
  • Antje Dietrich

      Affiliations

    • Tumor Pathophysiology, OncoRay – Center for Radiation Research in Oncology, Dresden University of Technology, Germany
    • Contributed equally.
    • ,
  • Susann Peickert

      Affiliations

    • Tumor Pathophysiology, OncoRay – Center for Radiation Research in Oncology, Dresden University of Technology, Germany
    • ,
  • Sandra Hering

      Affiliations

    • Institute of Legal Medicine, Dresden University of Technology, Germany
    • ,
  • Michael Baumann

      Affiliations

    • OncoRay – Center for Radiation Research in Oncology, Dresden University of Technology, Germany
    • Department of Radiation Oncology, University Hospital Dresden, Germany
    • ,
  • Marian Grade

      Affiliations

    • Department of General and Visceral Surgery, University Medicine Goettingen, Germany
    • ,
  • Thomas Ried

      Affiliations

    • National Cancer Institute, National Institutes of Health, Bethesda, MD, USA
    • ,
  • Leoni A. Kunz-Schughart

      Affiliations

    • Tumor Pathophysiology, OncoRay – Center for Radiation Research in Oncology, Dresden University of Technology, Germany
    • Corresponding Author InformationCorresponding author. Address: OncoRay – Center for Radiation Research in Oncology, Faculty of Medicine Carl Gustav Carus, Dresden University of Technology, Fetscherstraße 74, PF 86, 01307 Dresden, Germany.

References 

  1. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100:57–70
  2. Clarke MF, et al. Cancer stem cells – perspectives on current status and future directions: AACR workshop on cancer stem cells. Cancer Res. 2006;66:9339–9344
  3. Neuzil J, et al. Tumour-initiating cells vs. cancer ’stem’ cells and CD133: what’s in the name?. Biochem Biophys Res Commun. 2007;355:855–859
  4. Shipitsin M, Polyak K. The cancer stem cell hypothesis: in search of definitions, markers, and relevance. Lab Invest. 2008;88:459–463
  5. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer. 2008;8:755–768
  6. Wicha MS, Liu S, Dontu G. Cancer stem cells: an old idea – a paradigm shift. Cancer Res. 2006;66:1883–1890[discussion 1895–6]
  7. Woodward WA, Sulman EP. Cancer stem cells: markers or biomarkers?. Cancer Metastasis Rev. 2008;27:459–470
  8. Ricci-Vitiani L, et al. Colon cancer stem cells. Gut. 2008;57:538–548
  9. Fabian A, et al. Die hard: are cancer stem cells the Bruce Willises of tumor biology?. Cytometry A. 2009;75:67–74
  10. Corbeil D, et al. Prominin: a story of cholesterol, plasma membrane protrusions and human pathology. Traffic. 2001;2:82–91
  11. Miraglia S, et al. A novel five-transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning. Blood. 1997;90:5013–5021
  12. Shmelkov SV, et al. Alternative promoters regulate transcription of the gene that encodes stem cell surface protein AC133. Blood. 2004;103:2055–2061
  13. Jaszai J, et al. Focus on molecules: prominin-1 (CD133). Exp Eye Res. 2007;85:585–586
  14. Maw MA, et al. A frameshift mutation in prominin (mouse)-like 1 causes human retinal degeneration. Hum Mol Genet. 2000;9:27–34
  15. Roper K, Corbeil D, Huttner WB. Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nat Cell Biol. 2000;2:582–592
  16. Mizrak D, Brittan M, Alison MR. CD133: molecule of the moment. J Pathol. 2008;214:3–9
  17. Bidlingmaier S, Zhu X, Liu B. The utility and limitations of glycosylated human CD133 epitopes in defining cancer stem cells. J Mol Med. 2008;86:1025–1032
  18. Bao S, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756–760
  19. Liu G, et al. Analysis of gene expression, chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer. 2006;5:67
  20. Pfenninger CV, et al. CD133 is not present on neurogenic astrocytes in the adult subventricular zone, but on embryonic neural stem cells, ependymal cells, and glioblastoma cells. Cancer Res. 2007;67:5727–5736
  21. Singh SK, et al. Identification of human brain tumour initiating cells. Nature. 2004;432:396–401
  22. Singh SK, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63:5821–5828
  23. Yi L, et al. Isolation and characterization of stem cell-like precursor cells from primary human anaplastic oligoastrocytoma. Mod Pathol. 2007;20:1061–1068
  24. Pallini R, et al. Cancer stem cell analysis and clinical outcome in patients with glioblastoma multiforme. Clin Cancer Res. 2008;14:8205–8212
  25. Shu Q, et al. Direct orthotopic transplantation of fresh surgical specimen preserves CD133+ tumor cells in clinically relevant mouse models of medulloblastoma and glioma. Stem Cells. 2008;26:1414–1424
  26. Monzani E, et al. Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur J Cancer. 2007;43:935–946
  27. Eramo A, et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ. 2008;15:504–514
  28. Bruno S, et al. CD133+ renal progenitor cells contribute to tumor angiogenesis. Am J Pathol. 2006;169:2223–2235
  29. Ferrandina G, et al. Expression of CD133-1 and CD133-2 in ovarian cancer. Int J Gynecol Cancer. 2008;18:506–514
  30. Baba T, et al. Epigenetic regulation of CD133 and tumorigenicity of CD133+ ovarian cancer cells. Oncogene. 2009;28:209–218
  31. Richardson GD, et al. CD133, a novel marker for human prostatic epithelial stem cells. J Cell Sci. 2004;117:3539–3545
  32. Collins AT, et al. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 2005;65:10946–10951
  33. Ma S, et al. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology. 2007;132:2542–2556
  34. Suetsugu A, et al. Characterization of CD133+ hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem Biophys Res Commun. 2006;351:820–824
  35. Yin S, et al. CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Int J Cancer. 2007;120:1444–1450
  36. Hermann PC, et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell. 2007;1:313–323
  37. O’Brien CA, et al. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007;445:106–110
  38. Ricci-Vitiani L, et al. Identification and expansion of human colon-cancer-initiating cells. Nature. 2007;445:111–115
  39. Ieta K, et al. Biological and genetic characteristics of tumor-initiating cells in colon cancer. Ann Surg Oncol. 2008;15:638–648
  40. Friedrich J, et al. A reliable tool to determine cell viability in complex 3-d culture: the acid phosphatase assay. J Biomol Screen. 2007;12:925–937
  41. Friedrich J, et al. Spheroid-based drug screen: considerations and practical approach. Nat Protoc. 2009;4:309–324
  42. Ghadimi BM, et al. Centrosome amplification and instability occurs exclusively in aneuploid, but not in diploid colorectal cancer cell lines, and correlates with numerical chromosomal aberrations. Genes Chromosomes Cancer. 2000;27:183–190
  43. Carlsson J, Yuhas JM. Liquid-overlay culture of cellular spheroids. Recent Results Cancer Res. 1984;95:1–23
  44. Kunz-Schughart LA, Mueller-Klieser W, Masters JRW. Three-dimensional culture. In: Animal cell culture. Oxford: Oxford University Press; 2000. p. 123–48.
  45. Trzpis M, et al. Epithelial cell adhesion molecule: more than a carcinoma marker and adhesion molecule. Am J Pathol. 2007;171:386–395
  46. Baeuerle PA, Gires O. EpCAM (CD326) finding its role in cancer. Br J Cancer. 2007;96:417–423
  47. Sauer R, et al. Preoperative versus postoperative chemoradiotherapy for rectal cancer. N Engl J Med. 2004;351:1731–1740
  48. Baumann M, Krause M, Hill R. Exploring the role of cancer stem cells in radioresistance. Nat Rev Cancer. 2008;8:545–554
  49. Baumann M, et al. Cancer stem cells and radiotherapy. Int J Radiat Biol. 2009;1–12
  50. Donnenberg VS, Landreneau RJ, Donnenberg AD. Tumorigenic stem and progenitor cells: implications for the therapeutic index of anti-cancer agents. J Control Release. 2007;122:385–391
  51. Giordano A, et al. Carcinogenesis and environment: the cancer stem cell hypothesis and implications for the development of novel therapeutics and diagnostics. Front Biosci. 2007;12:3475–3482
  52. Ishii H, et al. Cancer stem cells and chemoradiation resistance. Cancer Sci. 2008;99:1871–1877
  53. Horst D, et al. CD133 expression is an independent prognostic marker for low survival in colorectal cancer. Br J Cancer. 2008;99:1285–1289
  54. Dallas NA, 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;69:1951–1957
  55. Dalerba P, et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA. 2007;104:10158–10163
  56. Haraguchi N, et al. CD133(+)CD44 (+) population efficiently enriches colon cancer initiating cells. Ann Surg Oncol. 2008;
  57. Quintana E, et al. Efficient tumour formation by single human melanoma cells. Nature. 2008;456:593–598
  58. Eaves CJ. Cancer stem cells: here, there, everywhere?. Nature. 2008;456:581–582
  59. Kleivi K, et al. Genome signatures of colon carcinoma cell lines. Cancer Genet Cytogenet. 2004;155:119–131
  60. Ferrand A, et al. Expression of gastrin precursors by CD133-positive colorectal cancer cells is crucial for tumour growth. Biochim Biophys Acta. 2009;1793:477–488
  61. Dylla SJ, et al. Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS ONE. 2008;3:e2428
  62. Chu P, et al. Characterization of a subpopulation of colon cancer cells with stem cell-like properties. Int J Cancer. 2009;124:1312–1321
  63. Vermeulen L, et al. Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc Natl Acad Sci USA. 2008;105:13427–13432
  64. LaBarge MA, Bissell MJ. Is CD133 a marker of metastatic colon cancer stem cells?. J Clin Invest. 2008;118:2021–2024
  65. Boivin D, et al. The stem cell marker CD133 (prominin-1) is phosphorylated on cytoplasmic tyrosine-828 and tyrosine-852 by Src and Fyn tyrosine kinases. Biochemistry. 2009;
  66. Platet N, et al. Influence of oxygen tension on CD133 phenotype in human glioma cell cultures. Cancer Lett. 2007;258:286–290
  67. Blazek ER, Foutch JL, Maki G. Daoy medulloblastoma cells that express CD133 are radioresistant relative to CD133− cells, and the CD133+ sector is enlarged by hypoxia. Int J Radiat Oncol Biol Phys. 2007;67:1–5
  68. Hambardzumyan D, Squatrito M, Holland EC. Radiation resistance and stem-like cells in brain tumors. Cancer Cell. 2006;10:454–456

☆ The publisher regrets that an incorrect version of the above paper was published in Radiotherapy and Oncology, volume 92, issue 3, pages 353–61. The incorrect version contained grammatical errors, e.g. in title, abstract and the discussion as well as an incomplete Fig. 2.

PII: S0167-8140(09)00590-8

doi: 10.1016/j.radonc.2009.10.010

Radiotherapy & Oncology
Volume 94, Issue 3 , Pages 375-383 , March 2010

Article Tools

* Image Usage & Resolution