Skip to main content

Advertisement

SpringerLink
Log in

Functions of tumorigenic and migrating cancer progenitor cells in cancer progression and metastasis and their therapeutic implications

  • NON-THEMATIC REVIEW
  • Published:
Cancer and Metastasis Reviews Aims and scope Submit manuscript

Abstract

The in vitro and in vivo characterization of adult stem cells has allowed researchers to identify certain specific functional features to each tissue-specific stem cell. Moreover, recent studies revealed that their malignant counterparts, the cancer progenitor cells with stem cell-like properties, may assume a crucial role for the initiation and progression of locally invasive cancers into disseminated and incurable disease states. Therefore, a new direction in cancer research appears necessary in considering the critical functions of cancer progenitor cells. In this review, we discuss recent concepts on the critical roles of tumorigenic and migrating cancer progenitor cells in carcinogenesis. Particularly, we describe the tumorigenic cascades that are frequently activated through the interplay of diverse hormones, growth factors, cytokines and integrins in cancer progenitor cells versus their further differentiated progeny. The emphasis is on the oncogenic signaling pathways activated during the localized cancer progression and micrometastatic events involved in tumor formation at distant sites such as bone marrow. Of therapeutic interest, important information for the selective molecular targeting of cancer progenitor cells, which must now be considered in developing new effective diagnostic and prognostic methods and curative treatments against the most locally advanced and metastatic cancers, is also described.

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

Similar content being viewed by others

References

  1. Al-Hajj, M., & Clarke, M. F. (2004). Self-renewal and solid tumor stem cells. Oncogene, 23, 7274–7282.

    Article  PubMed  CAS  Google Scholar 

  2. Woodward, W. A., Chen, M. S., Behbod, F., & Rosen, J. M. (2005). On mammary stem cells. Journal of Cell Science, 118, 3585–3594.

    Article  PubMed  CAS  Google Scholar 

  3. Reya, T., & Clevers, H. (2005). Wnt signalling in stem cells and cancer. Nature, 434, 843–850.

    Article  PubMed  CAS  Google Scholar 

  4. Mimeault, M., & Batra, S. K. (2006). Recent advances on multiple tumorigenic cascades involved in prostatic cancer progression and targeting therapies. Carcinogenesis, 27, 1–22.

    Article  PubMed  CAS  Google Scholar 

  5. Mimeault, M., & Batra, S. K. (2006). Recent advances on the significance of stem cells in tissue regeneration and cancer Therapies. Stem Cells, 24, 2319–2345.

    Article  PubMed  CAS  Google Scholar 

  6. Moore, K. A., & Lemischka, I. R. (2006). Stem cells and their niches. Science, 311, 1880–1885.

    Article  PubMed  CAS  Google Scholar 

  7. Li, L., & Neaves, W. B. (2006). Normal stem cells and cancer stem cells: The niche matters. Cancer Research, 66, 4553–4557.

    Article  PubMed  CAS  Google Scholar 

  8. Fuchs, E., Tumbar, T., & Guasch, G. (2004). Socializing with the neighbors: Stem cells and their niche. Cell, 116, 769–778.

    Article  PubMed  CAS  Google Scholar 

  9. Trosko, J. E., & Tai, M. H. (2006). Adult stem cell theory of the multi-stage, multi-mechanism theory of carcinogenesis: Role of inflammation on the promotion of initiated stem cells. Contributions to Microbiology, 13, 45–65.

    PubMed  Google Scholar 

  10. Beachy, P. A., Karhadkar, S. S., & Berman, D. M. (2004). Tissue repair and stem cell renewal in carcinogenesis. Nature, 432, 324–331.

    Article  PubMed  CAS  Google Scholar 

  11. Fang, D., Nguyen, T. K., Leishear, K., Finko, R., Kulp, A. N., Hotz, S., et al. (2005). A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Research, 65, 9328–9337.

    Article  PubMed  CAS  Google Scholar 

  12. Sell, S. (2004). Stem cell origin of cancer and differentiation therapy. Critical Reviews in Oncology/Hematology, 51, 1–28.

    Article  PubMed  Google Scholar 

  13. Kastan, M. B., & Bartek, J. (2004). Cell-cycle checkpoints and cancer. Nature, 432, 316–323.

    Article  PubMed  CAS  Google Scholar 

  14. Li, L. C., Carroll, P. R., & Dahiya, R. (2005). Epigenetic changes in prostate cancer: Implication for diagnosis and treatment. Journal of the National Cancer Institute, 97, 103–115.

    Article  PubMed  CAS  Google Scholar 

  15. Bapat, S. A., Mali, A. M., Koppikar, C. B., & Kurrey, N. K. (2005). Stem and progenitor-like cells contribute to the aggressive behavior of human epithelial ovarian cancer. Cancer Research, 65, 3025–3029.

    PubMed  CAS  Google Scholar 

  16. Brabletz, T., Jung, A., Spaderna, S., Hlubek, F., & Kirchner, T. (2005). Opinion: Migrating cancer stem cells––An integrated concept of malignant tumour progression. Nature Reviews. Cancer, 5, 744–749.

    Article  PubMed  CAS  Google Scholar 

  17. Vescovi, A. L., Galli, R., & Reynolds, B. A. (2006). Brain tumour stem cells. Nature Reviews. Cancer, 6, 425–436.

    Article  PubMed  CAS  Google Scholar 

  18. Mimeault, M., Brand, R. E., Sasson, A. A., & Batra, S. K. (2005). Recent advances on the molecular mechanisms involved in pancreatic cancer progression and therapies. Pancreas, 31, 301–316.

    Article  PubMed  CAS  Google Scholar 

  19. Singh, S. K., Clarke, I. D., Terasaki, M., Bonn, V. E., Hawkins, C., Squire, J., et al. (2003). Identification of a cancer stem cell in human brain tumors. Cancer Research, 63, 5821–5828.

    PubMed  CAS  Google Scholar 

  20. Al-Hajj, M., Wicha, M. S., ito-Hernandez, A., Morrison, S. J., & Clarke, M. F. (2003). Prospective identification of tumorigenic breast cancer cells. Proceedings of the National Academy of Sciences of the United States of America, 100, 3983–3988.

    Article  PubMed  CAS  Google Scholar 

  21. Hope, K. J., Jin, L., & Dick, J. E. (2004). Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity. Nature Immunology, 5, 738–743.

    Article  PubMed  CAS  Google Scholar 

  22. Collins, A. T., Berry, P. A., Hyde, C., Stower, M. J., & Maitland, N. J. (2005). Prospective identification of tumorigenic prostate cancer stem cells. Cancer Research, 65, 10946–10951.

    Article  PubMed  CAS  Google Scholar 

  23. Wicha, M. S., Liu, S., & Dontu, G. (2006). Cancer stem cells: An old idea––A paradigm shift. Cancer Research, 66, 1883–1890.

    Article  PubMed  CAS  Google Scholar 

  24. Tai, M. H., Chang, C. C., Kiupel, M., Webster, J. D., Olson, L. K., & Trosko, J. E. (2005). Oct4 expression in adult human stem cells: Evidence in support of the stem cell theory of carcinogenesis. Carcinogenesis, 26, 495–502.

    Article  PubMed  CAS  Google Scholar 

  25. Yu, H. M., Frank, D. E., Zhang, J., You, X., Carter, W. G., & Knudsen, B. S. (2004). Basal prostate epithelial cells stimulate the migration of prostate cancer cells. Molecular Carcinogenesis, 41, 85–97.

    Article  PubMed  CAS  Google Scholar 

  26. Bissell, M. J., & Radisky, D. (2001). Putting tumours in context. Nature Reviews. Cancer, 1, 46–54.

    Article  PubMed  CAS  Google Scholar 

  27. Rak, J. (2006). Is cancer stem cell a cell, or a multicellular unit capable of inducing angiogenesis? Medical Hypotheses, 66, 601–604.

    Article  PubMed  CAS  Google Scholar 

  28. Kalluri, R., & Zeisberg, M. (2006). Fibroblasts in cancer. Nature Reviews. Cancer, 6, 392–401.

    Article  PubMed  CAS  Google Scholar 

  29. Balkwill, F. (2004). Cancer and the chemokine network. Nature Reviews. Cancer, 4, 540–550.

    Article  PubMed  CAS  Google Scholar 

  30. Pollard, J. W. (2004). Tumour-educated macrophages promote tumour progression and metastasis. Nature Reviews. Cancer, 4, 71–78.

    Article  PubMed  CAS  Google Scholar 

  31. Li, H. C., Stoicov, C., Rogers, A. B., & Houghton, J. (2006). Stem cells and cancer: Evidence for bone marrow stem cells in epithelial cancers. World Journal of Gastroenterology, 12, 363–371.

    PubMed  Google Scholar 

  32. Kuwana, M., Okazaki, Y., Kodama, H., Satoh, T., Kawakami, Y., & Ikeda, Y. (2006). Endothelial differentiation potential of human monocyte-derived multipotential cells. Stem Cells.

  33. Santarelli, J. G., Udani, V., Yung, Y. C., Cheshier, S., Wagers, A., Brekken, R. A., et al. (2006). Incorporation of bone marrow-derived Flk-1-expressing CD34+ cells in the endothelium of tumor vessels in the mouse brain. Neurosurgery, 59, 374–382.

    Article  PubMed  Google Scholar 

  34. Radisky, D. C., & Bissell, M. J. (2006). Matrix metalloproteinase-induced genomic instability. Current Opinion in Genetics & Development, 16, 45–50.

    Article  CAS  Google Scholar 

  35. Reiss, K., Ludwig, A., & Saftig, P. (2006). Breaking up the tie: Disintegrin-like metalloproteinases as regulators of cell migration in inflammation and invasion. Pharmacology & Therapeutics, 111, 85–1006.

    Article  CAS  Google Scholar 

  36. Munshi, H. G., & Stack, M. S. (2006). Reciprocal interactions between adhesion receptor signaling and MMP regulation. Cancer Metastasis Reviews, 25, 45–56.

    Article  PubMed  CAS  Google Scholar 

  37. Deryugina, E. I., & Quigley, J. P. (2006). Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Reviews, 25, 9–34.

    Article  PubMed  CAS  Google Scholar 

  38. Thiery, J. P. (2002). Epithelial-mesenchymal transitions in tumour progression. Nature Reviews. Cancer, 2 , 442–454.

    Article  PubMed  CAS  Google Scholar 

  39. Gotzmann, J., Mikula, M., Eger, A., Schulte-Hermann, R., Foisner, R., Beug, H., et al. (2004). Molecular aspects of epithelial cell plasticity: Implications for local tumor invasion and metastasis. Mutation Research, 566, 9–20.

    Article  PubMed  CAS  Google Scholar 

  40. Yang, J., Mani, S. A., & Weinberg, R. A. (2006). Exploring a new twist on tumor metastasis. Cancer Research, 66, 4549–4552.

    Article  PubMed  CAS  Google Scholar 

  41. Zavadil, J., Cermak, L., Soto-Nieves, N., & Bottinger, E. P. (2004). Integration of TGF-beta/Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition. EMBO Journal, 23, 1155–1165.

    Article  PubMed  CAS  Google Scholar 

  42. Timmerman, L. A., Grego-Bessa, J., Raya, A., Bertran, E., Perez-Pomares, J. M., Diez, J., et al. (2004). Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes & Development, 18, 99–115.

    Article  CAS  Google Scholar 

  43. Larue, L., & Bellacosa, A. (2005). Epithelial-mesenchymal transition in development and cancer: Role of phosphatidylinositol 3′ kinase/AKT pathways. Oncogene, 24, 7443–7454.

    Article  PubMed  CAS  Google Scholar 

  44. Huber, M. A., Kraut, N., & Beug, H. (2005). Molecular requirements for epithelial-mesenchymal transition during tumor progression. Current Opinion in Cell Biology, 17, 548–558.

    Article  PubMed  CAS  Google Scholar 

  45. Lee, J. M., Dedhar, S., Kalluri, R., & Thompson, E. W. (2006). The epithelial-mesenchymal transition: New insights in signaling, development, and disease. Journal of Cell Biology, 172, 973–981.

    Article  PubMed  CAS  Google Scholar 

  46. Vega, S., Morales, A. V., Ocana, O. H., Valdes, F., Fabregat, I., & Nieto, M. A. (2004). Snail blocks the cell cycle and confers resistance to cell death. Genes & Development, 18, 1131–1143.

    Article  CAS  Google Scholar 

  47. Davies, M., Robinson, M., Smith, E., Huntley, S., Prime, S., & Paterson, I. (2005). Induction of an epithelial to mesenchymal transition in human immortal and malignant keratinocytes by TGF-beta1 involves MAPK, Smad and AP-1 signalling pathways. Journal of Cellular Biochemistry, 95, 918–931.

    Article  PubMed  CAS  Google Scholar 

  48. Kasper, M., Schnidar, H., Neill, G. W., Hanneder, M., Klingler, S., Blaas, L., et al. (2006) Selective modulation of hedgehog/GLI target gene expression by epidermal growth factor signaling in human keratinocytes. Molecular and Cellular Biology, 26, 6283–6298.

    Article  PubMed  CAS  Google Scholar 

  49. Bierie, B., & Moses, H. L. (2006). Tumour microenvironment: TGFbeta: The molecular Jekyll and Hyde of cancer. Nature Reviews Cancer, 6, 506–520.

    Article  PubMed  CAS  Google Scholar 

  50. Menke, A., Philippi, C., Vogelmann, R., Seidel, B., Lutz, M. P., Adler, G., et al. (2001). Down-regulation of E-cadherin gene expression by collagen type I and type III in pancreatic cancer cell lines. Cancer Research, 61, 3508–3517.

    PubMed  CAS  Google Scholar 

  51. Savagner, P. (2001). Leaving the neighborhood: Molecular mechanisms involved during epithelial-mesenchymal transition. BioEssays, 23, 912–923.

    Article  PubMed  CAS  Google Scholar 

  52. Bergers, G., & Coussens, L. M. (2000). Extrinsic regulators of epithelial tumor progression: Metalloproteinases. Current Opinion in Genetics & Development, 10, 120–127.

    Article  CAS  Google Scholar 

  53. Ii, M., Yamamoto, H., Adachi, Y., Maruyama, Y., & Shinomura, Y. (2006). Role of matrix metalloproteinase-7 (matrilysin) in human cancer invasion, apoptosis, growth, and angiogenesis. Experimental Biology and Medicine (Maywood), 231, 20–27.

    CAS  Google Scholar 

  54. van de Vijver, M. J., He, Y. D., van’t Veer, L. J., Dai, H., Hart, A. A., Voskuil, D. W., et al. (2002). A gene-expression signature as a predictor of survival in breast cancer. New England Journal of Medicine, 347, 1999–2009.

    Article  PubMed  Google Scholar 

  55. Buyse, M., Loi, S., van’t V. L., Viale, G., Delorenzi, M., Glas, A. M., et al. (2006). Validation and clinical utility of a 70-gene prognostic signature for women with node-negative breast cancer. Journal of the National Cancer Institute, 98, 1183–1192.

    Article  PubMed  CAS  Google Scholar 

  56. Simon, R. (2006). Development and evaluation of therapeutically relevant predictive classifiers using gene expression profiling. Journal of the National Cancer Institute, 98, 1169–1171.

    Article  PubMed  CAS  Google Scholar 

  57. Pantel, K., & Woelfle, U. (2004). Micrometastasis in breast cancer and other solid tumors. Journal of Biological Regulators and Homeostatic Agents, 18, 120–125.

    PubMed  CAS  Google Scholar 

  58. van Leenders, G. J., Aalders, T. W., Hulsbergen-van de Kaa, C. A., Ruiter, D. J., & Schalken, J. A. (2001). Expression of basal cell keratins in human prostate cancer metastases and cell lines. Journal of Pathology, 195, 563–570.

    Article  PubMed  Google Scholar 

  59. Yang, X. J., Lecksell, K., Gaudin, P., & Epstein, J. I. (1999). Rare expression of high-molecular-weight cytokeratin in adenocarcinoma of the prostate gland: A study of 100 cases of metastatic and locally advanced prostate cancer. American Journal of Surgical Pathology, 23, 147–152.

    Article  PubMed  CAS  Google Scholar 

  60. Kaplan, R. N., Riba, R. D., Zacharoulis, S., Bramley, A. H., Vincent, L., Costa, C., et al. (2005). VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature, 438, 820–827.

    Article  PubMed  CAS  Google Scholar 

  61. Kucia, M., Reca, R., Miekus, K., Wanzeck, J., Wojakowski, W., Janowska-Wieczorek, A., et al. (2005). Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: Pivotal role of the SDF-1-CXCR4 axis. Stem Cells, 23, 879–894.

    Article  PubMed  CAS  Google Scholar 

  62. Neiva, K., Sun, Y. X., & Taichman, R. S. (2005). The role of osteoblasts in regulating hematopoietic stem cell activity and tumor metastasis. Brazilian Journal of Medical and Biological Research, 38, 1449–1454.

    Article  PubMed  CAS  Google Scholar 

  63. Engl, T., Relja, B., Marian, D., Blumenberg, C., Muller, I., Beecken, W. D., et al. (2006). CXCR4 chemokine receptor mediates prostate tumor cell adhesion through alpha5 and beta3 integrins. Neoplasia, 8, 290–301.

    Article  PubMed  CAS  Google Scholar 

  64. Hideshima, T., Chauhan, D., Richardson, P., & Anderson, K. C. (2005). Identification and validation of novel therapeutic targets for multiple myeloma. Journal of Clinical Oncology, 23, 6345–6350.

    Article  PubMed  CAS  Google Scholar 

  65. Hart, C. A., Brown, M., Bagley, S., Sharrard, M., & Clarke, N. W. (2005). Invasive characteristics of human prostatic epithelial cells: Understanding the metastatic process. British Journal of Cancer, 92, 503–512.

    PubMed  CAS  Google Scholar 

  66. Loberg, R. D., Day, L. L., Harwood, J., Ying, C., St John, L. N., Giles, R., et al. (2006). CCL2 is a potent regulator of prostate cancer cell migration and proliferation. Neoplasia, 8, 578–586.

    Article  PubMed  CAS  Google Scholar 

  67. Dimitroff, C. J., Descheny, L., Trujillo, N., Kim, R., Nguyen, V., Huang, W., et al. (2005). Identification of leukocyte E-selectin ligands, P-selectin glycoprotein ligand-1 and E-selectin ligand-1, on human metastatic prostate tumor cells. Cancer Research, 65, 5750–5760.

    Article  PubMed  CAS  Google Scholar 

  68. Tremblay, P. L., Auger, F. A., & Huot, J. (2006). Regulation of transendothelial migration of colon cancer cells by E-selectin-mediated activation of p38 and ERK MAP kinases. Oncogene, 25, 6563–6573.

    Article  PubMed  CAS  Google Scholar 

  69. Witz, I. P. (2006). Tumor-microenvironment interactions: The selectin-selectin ligand axis in tumor-endothelium cross talk. Cancer Treatment and Research, 130, 125–140.

    PubMed  CAS  Google Scholar 

  70. Bukholm, I. K., Nesland, J. M., & Borresen-Dale, A. L. (2000). Re-expression of E-cadherin, alpha-catenin and beta-catenin, but not of gamma-catenin, in metastatic tissue from breast cancer patients. Journal of Pathology, 190, 15–19.

    Article  PubMed  CAS  Google Scholar 

  71. Thiery, J. P. (2003). Epithelial-mesenchymal transitions in development and pathologies. Current Opinion in Cell Biology, 15, 740–746.

    Article  PubMed  CAS  Google Scholar 

  72. Fizazi, K., Yang, J., Peleg, S., Sikes, C. R., Kreimann, E. L., Daliani, D., et al. (2003). Prostate cancer cells-osteoblast interaction shifts expression of growth/survival-related genes in prostate cancer and reduces expression of osteoprotegerin in osteoblasts. Clinical Cancer Research, 9, 2587–2597.

    PubMed  CAS  Google Scholar 

  73. Nuciforo, P., & Fraggetta, F. (2004). Cancer stem cell theory: Pathologists’ considerations and ruminations about wasting time and wrong evaluations. Journal of Clinical Pathology, 57, 782.

    PubMed  CAS  Google Scholar 

  74. Fehm, T., Sagalowsky, A., Clifford, E., Beitsch, P., Saboorian, H., Euhus, D., et al. (2002). Cytogenetic evidence that circulating epithelial cells in patients with carcinoma are malignant. Clinical Cancer Research, 8, 2073–2084.

    PubMed  CAS  Google Scholar 

  75. Kurbel, S. (2005). Selective reduction of estrogen receptor (ER) positive breast cancer occurrence by estrogen receptor modulators supports etiological distinction between ER positive and ER negative breast cancers. Medical Hypotheses, 64, 1182–1187.

    Article  PubMed  CAS  Google Scholar 

  76. Liu, S., Dontu, G., & Wicha, M. S. (2005). Mammary stem cells, self-renewal pathways, and carcinogenesis. Breast Cancer Research, 7, 86–95.

    Article  PubMed  CAS  Google Scholar 

  77. Romer, J., & Curran, T. (2005). Targeting medulloblastoma: Small-molecule inhibitors of the Sonic Hedgehog pathway as potential cancer therapeutics. Cancer Research, 65, 4975–4978.

    Article  PubMed  CAS  Google Scholar 

  78. Sun, S. Y., Hail, N. Jr., & Lotan, R. (2004). Apoptosis as a novel target for cancer chemoprevention. Journal of the National Cancer Institute, 96, 662–672.

    Article  PubMed  CAS  Google Scholar 

  79. Sarkar, F. H., & Li, Y. (2006). Using chemopreventive agents to enhance the efficacy of cancer therapy. Cancer Research, 66, 3347–3350.

    Article  PubMed  CAS  Google Scholar 

  80. Shay, J. W., & Wright, W. E. (2002). Telomerase: A target for cancer therapeutics. Cancer Cell, 2, 257–265.

    Article  PubMed  CAS  Google Scholar 

  81. Sano, T., Kagawa, M., Okuno, M., Ishibashi, N., Hashimoto, M., Yamamoto, M., et al. (2005). Prevention of rat hepatocarcinogenesis by acyclic retinoid is accompanied by reduction in emergence of both TGF-alpha-expressing oval-like cells and activated hepatic stellate cells. Nutrition and Cancer, 51, 197–206.

    Article  PubMed  CAS  Google Scholar 

  82. Hope, K. J., Jin, L., & Dick, J. E. (2003). Human acute myeloid leukemia stem cells. Archives of Medical Research, 34, 507–514.

    Article  PubMed  CAS  Google Scholar 

  83. Kajita, M., McClinic, K. N., & Wade, P. A. (2004). Aberrant expression of the transcription factors snail and slug alters the response to genotoxic stress. Molecular and Cellular Biology, 24, 7559–7566.

    Article  PubMed  CAS  Google Scholar 

  84. Oloumi, A., McPhee, T., & Dedhar, S. (2004). Regulation of E-cadherin expression and beta-catenin/Tcf transcriptional activity by the integrin-linked kinase. Biochimica et Biophysica Acta, 1691, 1–15.

    Article  PubMed  CAS  Google Scholar 

  85. Jechlinger, M., Sommer, A., Moriggl, R., Seither, P., Kraut, N., Capodiecci, P., et al. (2006). Autocrine PDGFR signaling promotes mammary cancer metastasis. Journal of Clinical Investigation, 116, 1561–1570.

    Article  PubMed  CAS  Google Scholar 

  86. Biswas, S., Criswell, T. L., Wang, S. E., & Arteaga, C. L. (2006). Inhibition of transforming growth factor-beta signaling in human cancer: Targeting a tumor suppressor network as a therapeutic strategy. Clinical Cancer Research, 12, 4142–4146.

    Article  PubMed  CAS  Google Scholar 

  87. Park, C. C., Zhang, H., Pallavicini, M., Gray, J. W., Baehner, F., Park, C. J., et al. (2006). Beta1 integrin inhibitory antibody induces apoptosis of breast cancer cells, inhibits growth, and distinguishes malignant from normal phenotype in three dimensional cultures and in vivo. Cancer Research, 66, 1526–1535.

    Article  PubMed  CAS  Google Scholar 

  88. Hu, X. F., & Xing, P. X. (2005). Cripto as a target for cancer immunotherapy. Expert Opinion on Therapeutic Targets, 9, 383–394.

    Article  PubMed  CAS  Google Scholar 

  89. Orend, G., & Chiquet-Ehrismann, R. (2006). Tenascin-C induced signaling in cancer. Cancer Letters, 244, 143–163.

    Article  PubMed  CAS  Google Scholar 

  90. Wang, X., Ling, M. T., Guan, X. Y., Tsao, S. W., Cheung, H. W., Lee, D. T., et al. (2004). Identification of a novel function of TWIST, a bHLH protein, in the development of acquired taxol resistance in human cancer cells. Oncogene, 23, 474–482.

    Article  PubMed  CAS  Google Scholar 

  91. Kwok, W. K., Ling, M. T., Lee, T. W., Lau, T. C., Zhou, C., Zhang, X., et al. (2005). Up-regulation of TWIST in prostate cancer and its implication as a therapeutic target. Cancer Research, 65, 5153–5162.

    Article  PubMed  CAS  Google Scholar 

  92. Kenny, P. A., & Bissell, M. J. (2003). Tumor reversion: Correction of malignant behavior by microenvironmental cues. International Journal of Cancer, 107, 688–695.

    Article  CAS  Google Scholar 

  93. Miller, J. C., & Sorensen, A. G. (2005). Imaging biomarkers predictive of disease/therapy outcome: Ischemic stroke and drug development. Progress in Drug Research, 62, 319–356.

    Article  PubMed  CAS  Google Scholar 

  94. Arora, A., & Scholar, E. M. (2005). Role of tyrosine kinase inhibitors in cancer therapy. Journal of Pharmacology and Experimental Therapeutics, 315, 971–979.

    Article  PubMed  CAS  Google Scholar 

  95. Zhong, H., & Bowen, J. P. (2006). Antiangiogenesis drug design: Multiple pathways targeting tumor vasculature. Current Medicinal Chemistry, 13, 849–862.

    Article  PubMed  CAS  Google Scholar 

  96. Meric, J. B., Rottey, S., Olaussen, K., Soria, J. C., Khayat, D., Rixe, O., et al. (2006). Cyclooxygenase-2 as a target for anticancer drug development. Critical Reviews in Oncology/Hematology, 59, 51–64.

    Article  PubMed  Google Scholar 

  97. Aggarwal, B. B., Shishodia, S., Sandur, S. K., Pandey, M. K., & Sethi, G. (2006). Inflammation and cancer: How hot is the link? Biochem Pharmacol.

  98. Kobayashi, H., & Lin, P. C. (2006). Antiangiogenic and radiotherapy for cancer treatment. Histology and Histopathology, 21, 1125–1134.

    PubMed  CAS  Google Scholar 

  99. Grosch, S., Maier, T. J., Schiffmann, S., & Geisslinger, G. (2006). Cyclooxygenase-2 (COX-2)-independent anticarcinogenic effects of selective COX-2 inhibitors. Journal of the National Cancer Institute, 98, 736–747.

    Article  PubMed  CAS  Google Scholar 

  100. Lyden, D., Hattori, K., Dias, S., Costa, C., Blaikie, P., Butros, L., et al. (2001). Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nature Medicine, 7, 1194–1201.

    Article  PubMed  CAS  Google Scholar 

  101. Vosseler, S., Mirancea, N., Bohlen, P., Mueller, M. M., & Fusenig, N. E. (2005). Angiogenesis inhibition by vascular endothelial growth factor receptor-2 blockade reduces stromal matrix metalloproteinase expression, normalizes stromal tissue, and reverts epithelial tumor phenotype in surface heterotransplants. Cancer Research, 65, 1294–1305.

    Article  PubMed  CAS  Google Scholar 

  102. Kulbe, H., Levinson, N. R., Balkwill, F., & Wilson, J. L. (2004). The chemokine network in cancer-much more than directing cell movement. International Journal of Developmental Biology, 48, 489–496.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, Eppley Institute of Cancer and Allied Diseases, University of Nebraska Medical Center, Omaha, NE, 68198-5870, USA

    Murielle Mimeault & Surinder K. Batra

Authors
  1. Murielle Mimeault
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Surinder K. Batra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Murielle Mimeault or Surinder K. Batra.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mimeault, M., Batra, S.K. Functions of tumorigenic and migrating cancer progenitor cells in cancer progression and metastasis and their therapeutic implications. Cancer Metastasis Rev 26, 203–214 (2007). https://doi.org/10.1007/s10555-007-9052-4

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10555-007-9052-4

Keywords

Search

Navigation