Skip to main content

Advertisement

SpringerLink
Log in

Enrichment of Cancer Stem Cells Based on Heterogeneity of Invasiveness

  • Published:
Stem Cell Reviews and Reports Aims and scope Submit manuscript

Abstract

Cancer stem cells (CSCs) have multiple potentials in carcinogenesis and tumor progression. However, it is rather difficult to enrich and amplify CSCs either from tumor cell lines or even primary tumor tissues. Therefore, establishing new methodologies for isolation and enrichment based on the functional properties of CSCs is of great importance for studies on CSCs. According to the findings that CSCs possess more infiltrative capability as compared with their differentiated descendants, we propose a novel strategy based on heterogeneity of cancer cell invasiveness for isolation and enrichment of CSCs from committed cancer cell population. In addition, we hypothesize that existence of CSCs might be the real root of tumor invasion and metastasis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Reya, T., Morrison, S. J., Clarke, M. F., & Weissman, I. L. (2001). Stem cells, cancer, and cancer stem cells. Nature, 414, 105–111. doi:10.1038/35102167.

    Article  PubMed  CAS  Google Scholar 

  2. Polyak, K., & Hahn, W. C. (2006). Roots and stems: stem cells in cancer. Natural Medicines, 12, 296–300. doi:10.1038/nm1379.

    Article  CAS  Google Scholar 

  3. Bao, S., Wu, Q., McLendon, R. E., et al. (2006). Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature, 444, 756–760. doi:10.1038/nature05236.

    Article  PubMed  CAS  Google Scholar 

  4. Liu, G., Yuan, X., Zeng, Z., et al. (2006). Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Molecular Cancer, 5, 67. doi:10.1186/1476-4598-5-67.

    Article  PubMed  Google Scholar 

  5. Eramo, A., Lotti, F., Sette, G., et al. (2008). Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death & Differentiation, 15, 504–514. doi:10.1038/sj.cdd.4402283.

    Article  CAS  Google Scholar 

  6. Van, S. A., Van der Pol, M. A., Kok, A., et al. (2003). Differences between the CD34+ and CD34− blast compartments in apoptosis resistance in acute myeloid leukemia. Haematologica, 88, 497–508.

    Google Scholar 

  7. Sheridan, C., Kishimoto, H., Fuchs, R. K., et al. (2006). CD44+/CD24− breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Research, 8, R59. doi:10.1186/bcr1610.

    Article  PubMed  Google Scholar 

  8. Bonnet, D., & Dick, J. E. (1997). Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nature Medicine, 3, 730–737. doi:10.1038/nm0797-730.

    Article  PubMed  CAS  Google Scholar 

  9. Tirino, V., Desiderio, V., d, , ’Aquino, R., et al. (2008). Detection and characterization of CD133+ cancer stem cells in human solid tumours. PLoS One, 3, e3469. doi:10.1371/journal.pone.0003469.

    Article  PubMed  Google Scholar 

  10. Baba, T., Convery, P. A., Matsumura, N., et al. (2008). Epigenetic regulation of CD133 and tumorigenicity of CD133+ ovarian cancer cells. Oncogene. doi:10.1038/onc.2008.374.

  11. Beier, D., Hau, P., Proescholdt, M., et al. (2007). CD133(+) and CD133(−) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Research, 67, 4010–4015. doi:10.1158/0008-5472.CAN-06-4180.

    Article  PubMed  CAS  Google Scholar 

  12. Ogden, A. T., Waziri, A. E., Lochhead, R. A., et al. (2008). Identification of A2B5+CD133− tumor-initiating cells in adult human gliomas. Neurosurgery, 62, 505–514. doi:10.1227/01.neu.0000316019.28421.95.

    Article  PubMed  Google Scholar 

  13. Shmelkov, S. V., Butler, J. M., Hooper, A. T., et al. (2008). CD133 expression is not restricted to stem cells, and both CD133+ and CD133− metastatic colon cancer cells initiate tumors. The Journal of Clinical Investigation, 118, 2111–2120.

    PubMed  CAS  Google Scholar 

  14. Zheng, X., Shen, G., Yang, X., & Liu, W. (2007). Most C6 cells are cancer stem cells: evidence from clonal and population analyses. Cancer Research, 67, 3691–3697. doi:10.1158/0008-5472.CAN-06-3912.

    Article  PubMed  CAS  Google Scholar 

  15. Ho, M. M., Ng, A. V., Lam, S., & Hung, J. Y. (2007). Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Research, 67, 4827–4233. doi:10.1158/0008-5472.CAN-06-3557.

    Article  PubMed  CAS  Google Scholar 

  16. Wang, J., Guo, L. P., & Chen, L. Z. (2007). Identification of cancer stem cell-like side population cells in human nasopharyngeal carcinoma cell line. Cancer Research, 67, 3716–3724. doi:10.1158/0008-5472.CAN-06-4343.

    Article  PubMed  CAS  Google Scholar 

  17. Kondo, T., Setoguchi, T., & Taga, T. (2004). Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proceedings of the National Academy of Sciences of the United States of America, 101, 781–786. doi:10.1073/pnas.0307618100.

    Article  PubMed  CAS  Google Scholar 

  18. Patrawala, L., Calhoun, T., Schneider-Broussard, R., Zhou, J., Claypool, K., & Tang, D. G. (2005). Side population is enriched in tumorigenic, stem-Like cancer cells, whereas ABCG2+ and ABCG2− cancer cells are similarly tumorigenic. Cancer Research, 65, 6207–6219. doi:10.1158/0008-5472.CAN-05-0592.

    Article  PubMed  CAS  Google Scholar 

  19. Hirschmann Jax, C., Foster, A. E., Wulf, G. G., et al. (2004). A distinct “side population” of cells with high drug efflux capacity in human tumor cells. Proceedings of the National Academy of Sciences of the United States of America, 101, 14228–14233. doi:10.1073/pnas.0400067101.

    Article  PubMed  CAS  Google Scholar 

  20. Hadnagy, A., Gaboury, L., Beaulieu, R., & Balicki, D. (2006). SP analysis may be used to identify cancer stem cell populations. Experimental Cell Research, 312, 3701–3710. doi:10.1016/j.yexcr.2006.08.030.

    Article  PubMed  CAS  Google Scholar 

  21. Goodell, M. A., Brose, K., Paradis, G., Conner, A. S., & Mulligan, R. C. (1996). Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. The Journal of Experimental Medicine, 183, 1797–1806. doi:10.1084/jem.183.4.1797.

    Article  PubMed  CAS  Google Scholar 

  22. Burkert, J., Otto, W. R., & Wright, N. A. (2008). Side populations of gastrointestinal cancers are not enriched in stem cells. The Journal of Pathology, 214, 564–573. doi:10.1002/path.2307.

    Article  PubMed  CAS  Google Scholar 

  23. Yuan, X., Curtin, J., Xiong, Y., et al. (2004). Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene, 23, 9392–9400. doi:10.1038/sj.onc.1208311.

    Article  PubMed  CAS  Google Scholar 

  24. Salmaggi, A., Boiardi, A., Gelati, M., et al. (2006). Glioblastoma-derived tumorospheres identify a population of tumor stem-like cells with angiogenic potential and enhanced multidrug resistance phenotype. Glia, 54, 850–860. doi:10.1002/glia.20414.

    Article  PubMed  Google Scholar 

  25. Reynolds, B. A., & Weiss, S. (1996). Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Developments of Biological, 175, 1–13. doi:10.1006/dbio.1996.0090.

    Article  CAS  Google Scholar 

  26. Yu, F., Yao, H., Zhu, P., et al. (2007). let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell, 131, 1109–1123. doi:10.1016/j.cell.2007.10.054.

    Article  PubMed  CAS  Google Scholar 

  27. Li, H. Z., Yi, T. B., & Wu, Z. Y. (2008). Suspension culture combined with chemotherapeutic agents for sorting of breast cancer stem cells. BioMed Central Cancer, 8, 135. doi:10.1186/1471-2407-8-135.

    PubMed  Google Scholar 

  28. Dean, M., Fojo, T., & Bates, S. (2005). Tumour stem cells and drug resistance. Nature Reviews Cancer, 5, 275–284. doi:10.1038/nrc1590.

    Article  PubMed  CAS  Google Scholar 

  29. Eramo, A., Ricci-Vitiani, L., Zeuner, A., et al. (2006). Chemotherapy resistance of glioblastoma stem cells. Cell Death & Differentiation, 13, 1238–1241. doi:10.1038/sj.cdd.4401872.

    Article  CAS  Google Scholar 

  30. Ghods, A. J., Irvin, D., Liu, G., et al. (2007). Spheres isolated from 9L gliosarcoma rat cell line possess chemoresistant and aggressive cancer stem-like cells. Stem Cells, 25, 1645–1653. doi:10.1634/stemcells.2006-0624.

    Article  PubMed  CAS  Google Scholar 

  31. Pellegatta, S., Poliani, P. L., Corno, D., et al. (2006). Neurospheres enriched in cancer stem-like cells are highly effective in eliciting a dendritic cell-mediated immune response against malignant gliomas. Cancer Research, 66, 10247–10252. doi:10.1158/0008-5472.CAN-06-2048.

    Article  PubMed  CAS  Google Scholar 

  32. Rak, J. (2006). Is cancer stem cell a cell, or a multicellular unit capable of inducing angiogenesis? Medical Hypotheses, 66, 601–604. doi:10.1016/j.mehy.2005.09.004.

    Article  PubMed  CAS  Google Scholar 

  33. Shen, R., Ye, Y., Chen, L., Yan, Q., Barsky, S. H., & Gao, J. X. (2008). Precancerous stem cells can serve as tumor vasculogenic progenitors. PLoS One, 3, e1652. doi:10.1371/journal.pone.0001652.

    Article  PubMed  Google Scholar 

  34. Locke, M., Heywood, M., Fawell, S., & Mackenzie, I. C. (2005). Retention of intrinsic stem cell hierarchies in carcinoma-derived cell lines. Cancer Research, 65, 8944–8950. doi:10.1158/0008-5472.CAN-05-0931.

    Article  PubMed  CAS  Google Scholar 

  35. Yu, S. C., Ping, Y. F., Yi, L., et al. (2008). Isolation and characterization of cancer stem cells from a human glioblastoma cell line U87. Cancer Letters, 265, 124–134. doi:10.1016/j.canlet.2008.02.010.

    Article  PubMed  CAS  Google Scholar 

  36. Lee, J., Kotliarova, S., Kotliarov, Y., et al. (2006). Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell, 9, 391–403. doi:10.1016/j.ccr.2006.03.030.

    Article  PubMed  CAS  Google Scholar 

  37. Brabletz, T., Jung, A., Spaderna, S., Hlubek, F., & Kirchner, T. (2005). Opinion: migrating cancer stem cells—an integrated concept of malignant tumour progression. Nature Review Cancer, 5, 744–749. doi:10.1038/nrc1694.

    Article  CAS  Google Scholar 

  38. Li, F., Tiede, B., Massagué, J., & Kang, Y. (2007). Beyond tumorigenesis: cancer stem cells in metastasis. Cell Research, 17, 3–14. doi:10.1038/sj.cr.7310118.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by grants from the National Basic Research Program of China (973 Program, No.2006CB708503) and the National Natural Science Foundation of China (No. 30725035, 30700863).

Author information

Authors and Affiliations

  1. Institute of Pathology and Southwest Cancer Center, Southwest Hospital, Third Military Medical University, Chongqing, 400038, P. R. China

    Shi-cang Yu & Xiu-wu Bian

Authors
  1. Shi-cang Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiu-wu Bian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiu-wu Bian.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yu, Sc., Bian, Xw. Enrichment of Cancer Stem Cells Based on Heterogeneity of Invasiveness. Stem Cell Rev and Rep 5, 66–71 (2009). https://doi.org/10.1007/s12015-008-9047-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12015-008-9047-8

Keywords

Search

Navigation