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Journal of Biomedicine and Biotechnology
Volume 2012 (2012), Article ID 420364, 13 pages
http://dx.doi.org/10.1155/2012/420364
Review Article

Molecular Imaging in Tracking Tumor Stem-Like Cells

Tian Xia,1 Han Jiang,1,2,3,4 Chenrui Li,5 Mei Tian,1,2,3,4 and Hong Zhang1,2,3,4

1Department of Nuclear Medicine, Second Affiliated Hospital of Zhejiang University, School of Medicine, 88 Jiefang Road, Hangzhou, Zhejiang 310009, China
2Zhejiang University Medical PET Center, Zhejiang University, Hangzhou 310009, China
3Institute of Nuclear Medicine and Molecular Imaging, Zhejiang University, Hangzhou 310009, China
4Key Laboratory of Medical Molecular Imaging of Zhejiang Province, Hangzhou 310009, China
5The School of Pharmacy, The Chinese University of Hong Kong, Hong Kong

Received 27 December 2011; Accepted 10 February 2012

Academic Editor: Enzhong Li

Copyright © 2012 Tian Xia et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Siegel, E. Ward, O. Brawley, and A. Jemal, “Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths,” CA Cancer Journal for Clinicians, vol. 61, no. 4, pp. 212–236, 2011. View at Publisher · View at Google Scholar
  2. J. R. Benson, I. Jatoi, M. Keisch, F. J. Esteva, A. Makris, and V. C. Jordan, “Early breast cancer,” The Lancet, vol. 373, no. 9673, pp. 1463–1479, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. K. Kai, Y. Arima, T. Kamiya, and H. Saya, “Breast cancer stem cells,” Breast Cancer, vol. 17, no. 2, pp. 80–85, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Kabashima, H. Higuchi, H. Takaishi et al., “Side population of pancreatic cancer cells predominates in TGF-β-mediated epithelial to mesenchymal transition and invasion,” International Journal of Cancer, vol. 124, no. 12, pp. 2771–2779, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. C. Hirschmann-Jax, A. E. Foster, G. G. Wulf et al., “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, vol. 101, no. 39, pp. 14228–14233, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Hirschmann-Jax, A. E. Foster, G. G. Wulf, M. A. Goodell, and M. K. Brenner, “A distinct “side population” of cells in human tumor cells: implications for tumor biology and therapy,” Cell Cycle, vol. 4, no. 2, pp. 203–205, 2005. View at Scopus
  7. C. T. Jordan, M. L. Guzman, and M. Noble, “Cancer stem cells,” New England Journal of Medicine, vol. 355, no. 12, pp. 1253–1261, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. J. E. Visvader and G. J. Lindeman, “Cancer stem cells in solid tumours: accumulating evidence and unresolved questions,” Nature Reviews Cancer, vol. 8, no. 10, pp. 755–768, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. L. Ricci-Vitiani, D. G. Lombardi, E. Pilozzi et al., “Identification and expansion of human colon-cancer-initiating cells,” Nature, vol. 445, no. 7123, pp. 111–115, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. C. A. O'Brien, A. Pollett, S. Gallinger, and J. E. Dick, “A human colon cancer cell capable of initiating tumour growth in immunodeficient mice,” Nature, vol. 445, no. 7123, pp. 106–110, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Lapidot, C. Sirard, J. Vormoor et al., “A cell initiating human acute myeloid leukaemia after transplantation into SCID mice,” Nature, vol. 367, no. 6464, pp. 645–648, 1994. View at Publisher · View at Google Scholar · View at Scopus
  12. D. Bonnet and J. E. Dick, “Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell,” Nature Medicine, vol. 3, no. 7, pp. 730–737, 1997. View at Publisher · View at Google Scholar · View at Scopus
  13. S. K. Singh, C. Hawkins, I. D. Clarke et al., “Identification of human brain tumour initiating cells,” Nature, vol. 432, no. 7015, pp. 396–401, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. M. T. Chiao, Y. C. Yang, W. Y. Cheng, C. C. Shen, and J. L. Ko, “CD133+ glioblastoma stem-like cells induce vascular mimicry in vivo,” Current Neurovascular Research, vol. 8, no. 3, pp. 210–219, 2011. View at Publisher · View at Google Scholar
  15. M. Tabuse, S. Ohta, Y. Ohashi et al., “Functional analysis of HOXD9 in human gliomas and glioma cancer stem cells,” Molecular Cancer, vol. 10, article 60, 2011. View at Publisher · View at Google Scholar
  16. J. Ferlay, H. R. Shin, F. Bray, D. Forman, C. Mathers, and D. M. Parkin, “Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008,” International Journal of Cancer, vol. 127, no. 12, pp. 2893–2917, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Ginestier, M. H. Hur, E. Charafe-Jauffret et al., “ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome,” Cell Stem Cell, vol. 1, no. 5, pp. 555–567, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Al-Hajj, M. S. Wicha, A. Benito-Hernandez, S. J. Morrison, and M. F. Clarke, “Prospective identification of tumorigenic breast cancer cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 7, pp. 3983–3988, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Cordenonsi, F. Zanconato, L. Azzolin et al., “The hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells,” Cell, vol. 147, no. 4, pp. 759–772, 2011. View at Publisher · View at Google Scholar
  20. A. Eramo, F. Lotti, G. Sette et al., “Identification and expansion of the tumorigenic lung cancer stem cell population,” Cell Death and Differentiation, vol. 15, no. 3, pp. 504–514, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. V. Levina, A. M. Marrangoni, R. DeMarco, E. Gorelik, and A. E. Lokshin, “Drug-selected human lung cancer stem cells: cytokine network, tumorigenic and metastatic properties,” PLoS One, vol. 3, no. 8, Article ID e3077, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. M. M. Ho, A. V. Ng, S. Lam, and J. Y. Hung, “Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells,” Cancer Research, vol. 67, no. 10, pp. 4827–4833, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. H. Iinuma, T. Watanabe, K. Mimori et al., “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,” Journal of Clinical Oncology, vol. 29, no. 12, pp. 1547–1555, 2011. View at Publisher · View at Google Scholar
  24. L. Vermeulen, M. Todaro, F. de Sousa Mello et al., “Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 36, pp. 13427–13432, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. P. Dalerba, S. J. Dylla, I. K. Park et al., “Phenotypic characterization of human colorectal cancer stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 24, pp. 10158–10163, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. L. Vermeulen, F. de Sousa E Melo, M. van der Heijden et al., “Wnt activity defines colon cancer stem cells and is regulated by the microenvironment,” Nature Cell Biology, vol. 12, no. 5, pp. 468–476, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Beck, X. Jin, J. Yin et al., “Identification of a peptide that interacts with Nestin protein expressed in brain cancer stem cells,” Biomaterials, vol. 32, no. 33, pp. 8518–8528, 2011. View at Publisher · View at Google Scholar
  28. C. Yu, Z. Yao, J. Dai et al., “ALDH activity indicates increased tumorigenic cells, but not cancer stem cells, in prostate cancer cell lines,” In Vivo, vol. 25, no. 1, pp. 69–76, 2011.
  29. V. K. Rajasekhar, L. Studer, W. Gerald, N. D. Socci, and H. I. Scher, “Tumour-initiating stem-like cells in human prostate cancer exhibit increased NF-κB signalling,” Nature Communications, vol. 2, article 162, 2011. View at Publisher · View at Google Scholar
  30. P. A. Philip, M. Mooney, D. Jaffe et al., “Consensus report of the national cancer institute clinical trials planning meeting on pancreas cancer treatment,” Journal of Clinical Oncology, vol. 27, no. 33, pp. 5660–5669, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. M. J. Moore, D. Goldstein, J. Hamm et al., “Erlotinib plus gemcitabine compared with gemcitabine alone in patients with advanced pancreatic cancer: a phase III trial of the National Cancer Institute of Canada Clinical Trials Group,” Journal of Clinical Oncology, vol. 25, no. 15, pp. 1960–1966, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. T. Reya, S. J. Morrison, M. F. Clarke, and I. L. Weissman, “Stem cells, cancer, and cancer stem cells,” Nature, vol. 414, no. 6859, pp. 105–111, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Dorado, E. Lonardo, I. Miranda-Lorenzo, and C. Heeschen, “Pancreatic cancer stem cells: new insights and perspectives,” Journal of Gastroenterology, vol. 46, no. 8, pp. 966–973, 2011. View at Publisher · View at Google Scholar
  34. C. Li, D. G. Heidt, P. Dalerba et al., “Identification of pancreatic cancer stem cells,” Cancer Research, vol. 67, no. 3, pp. 1030–1037, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Rovira, S. G. Scott, A. S. Liss, J. Jensen, S. P. Thayer, and S. D. Leach, “Isolation and characterization of centroacinar/terminal ductal progenitor cells in adult mouse pancreas,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 1, pp. 75–80, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. M. P. Kim, J. B. Fleming, H. Wang et al., “ALDH activity selectively defines an enhanced tumor-initiating cell population relative to CD133 expression in human pancreatic adenocarcinoma,” PLoS One, vol. 6, no. 6, Article ID e20636, 2011. View at Publisher · View at Google Scholar
  37. B. I. Carr, “Hepatocellular carcinoma: current management and future trends,” Gastroenterology, vol. 127, supplement 1, no. 5, pp. S218–S224, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. W. T. Kassahun, J. Fangmann, J. Harms, J. Hauss, and M. Bartels, “Liver resection and transplantation in the management of hepatocellular carcinoma: a review,” Experimental and Clinical Transplantation, vol. 4, no. 2, pp. 549–558, 2006. View at Scopus
  39. T. K. W. Lee, A. Castilho, V. C. H. Cheung, K. H. Tang, S. Ma, and I. O. L. Ng, “CD24+ liver tumor-initiating cells drive self-renewal and tumor initiation through STAT3-mediated NANOG regulation,” Cell Stem Cell, vol. 9, no. 1, pp. 50–63, 2011. View at Publisher · View at Google Scholar
  40. A. Hadnagy, L. Gaboury, R. Beaulieu, and D. Balicki, “SP analysis may be used to identify cancer stem cell populations,” Experimental Cell Research, vol. 312, no. 19, pp. 3701–3710, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. H. Liu, M. R. Patel, J. A. Prescher et al., “Cancer stem cells from human breast tumors are involved in spontaneous metastases in orthotopic mouse models,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 42, pp. 18115–18120, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. J. V. Leyton, T. Olafsen, E. J. Lepin et al., “Humanized radioiodinated minibody for imaging of prostate stem cell antigen-expressing tumors,” Clinical Cancer Research, vol. 14, no. 22, pp. 7488–7496, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. R. McClelland, E. Wauthier, T. Tallheden, L. M. Reid, and E. Hsu, “In Situ labeling and magnetic resonance imaging of transplanted human hepatic stem cells,” Molecular Imaging and Biology, vol. 13, no. 5, pp. 911–922, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Tsurumi, N. Esser, E. Firat et al., “Non-invasive in vivo imaging of tumor-associated cd133/prominin,” PLoS One, vol. 5, no. 12, Article ID e15605, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Hubank and D. G. Schatz, “Identifying differences in mRNA expression by representational difference analysis of cDNA,” Nucleic Acids Research, vol. 22, no. 25, pp. 5640–5648, 1994. View at Scopus
  46. R. E. Reiter, Z. Gu, T. Watabe et al., “Prostate stem cell antigen: a cell surface marker overexpressed in prostate cancer,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 4, pp. 1735–1740, 1998. View at Publisher · View at Google Scholar · View at Scopus
  47. Z. Gu, G. Thomas, J. Yamashiro et al., “Prostate stem cell antigen (PSCA) expression increases with high gleason score, advanced stage and bone metastasis in prostate cancer,” Oncogene, vol. 19, no. 10, pp. 1288–1296, 2000. View at Scopus
  48. J. V. Leyton, T. Olafsen, M. A. Sherman et al., “Engineered humanized diabodies for microPET imaging of prostate stem cell antigen-expressing tumors,” Protein Engineering, Design and Selection, vol. 22, no. 3, pp. 209–216, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. E. J. Lepin, J. V. Leyton, Y. Zhou et al., “An affinity matured minibody for PET imaging of prostate stem cell antigen (PSCA)-expressing tumors,” European Journal of Nuclear Medicine and Molecular Imaging, vol. 37, no. 8, pp. 1529–1538, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. C. A. Foss, J. J. Fox, G. Feldmann et al., “Radiolabeled anti-claudin 4 and anti-prostate stem cell antigen: initial imaging in experimental models of pancreatic cancer,” Molecular Imaging, vol. 6, no. 2, pp. 131–139, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. Y. Yoshii, T. Furukawa, Y. Kiyono et al., “Internal radiotherapy with copper-64-diacetyl-bis (N4-methylthiosemicarbazone) reduces CD133+ highly tumorigenic cells and metastatic ability of mouse colon carcinoma,” Nuclear Medicine and Biology, vol. 38, no. 2, pp. 151–157, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. O. K. Okamoto and J. F. Perez, “Targeting cancer stem cells with monoclonal antibodies: a new perspective in cancer therapy and diagnosis,” Expert Review of Molecular Diagnostics, vol. 8, no. 4, pp. 387–393, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. E. K. Lim, H. O. Kim, E. Jang et al., “Hyaluronan-modified magnetic nanoclusters for detection of CD44-overexpressing breast cancer by MR imaging,” Biomaterials, vol. 32, no. 31, pp. 7941–7950, 2011. View at Publisher · View at Google Scholar
  54. A. Z. Wang, V. Bagalkot, C. C. Vasilliou et al., “Superparamagnetic iron oxide nanoparticle-aptamer bioconjugates for combined prostate cancer imaging and therapy,” ChemMedChem, vol. 3, no. 9, pp. 1311–1315, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. E. Vlashi, K. Kim, C. Lagadec et al., “In vivo imaging, tracking, and targeting of cancer stem cells,” Journal of the National Cancer Institute, vol. 101, no. 5, pp. 350–359, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. H. Y. Ko, K. J. Choi, C. H. Lee, and S. Kim, “A multimodal nanoparticle-based cancer imaging probe simultaneously targeting nucleolin, integrin αvβ3 and tenascin-C proteins,” Biomaterials, vol. 32, no. 4, pp. 1130–1138, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. L. Garzia, I. Andolfo, E. Cusanelli et al., “MicroRNA-199b-5p impairs cancer stem cells through negative regulation of HES1 in medulloblastoma,” PLoS One, vol. 4, no. 3, Article ID e4998, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. V. Ponomarev, M. Doubrovin, I. Serganova et al., “A novel triple-modality reporter gene for whole-body fluorescent, bioluminescent, and nuclear noninvasive imaging,” European Journal of Nuclear Medicine and Molecular Imaging, vol. 31, no. 5, pp. 740–751, 2004. View at Scopus
  59. M. F. Clarke and M. Fuller, “Stem cells and cancer: two faces of eve,” Cell, vol. 124, no. 6, pp. 1111–1115, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. A. V. Molofsky, R. Pardal, T. Iwashita, I. K. Park, M. F. Clarke, and S. J. Morrison, “Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation,” Nature, vol. 425, no. 6961, pp. 962–967, 2003. View at Publisher · View at Google Scholar · View at Scopus
  61. I. K. Park, D. Qian, M. Kiel et al., “Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells,” Nature, vol. 423, no. 6937, pp. 302–305, 2003. View at Publisher · View at Google Scholar · View at Scopus
  62. J. Lessard and G. Sauvageau, “Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells,” Nature, vol. 423, no. 6937, pp. 255–260, 2003. View at Publisher · View at Google Scholar · View at Scopus
  63. T. J. Sweeney, V. Mailander, A. A. Tucker et al., “Visualizing the kinetics of tumor-cell clearance in living animals,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 21, pp. 12044–12049, 1999. View at Publisher · View at Google Scholar · View at Scopus
  64. H. Niwa, J. I. Miyazaki, and A. G. Smith, “Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells,” Nature Genetics, vol. 24, no. 4, pp. 372–376, 2000. View at Publisher · View at Google Scholar · View at Scopus
  65. J. A. Thomson, “Embryonic stem cell lines derived from human blastocysts,” Science, vol. 282, no. 5391, pp. 1145–1147, 1998.
  66. C. Calabrese, H. Poppleton, M. Kocak et al., “A perivascular niche for brain tumor stem cells,” Cancer Cell, vol. 11, no. 1, pp. 69–82, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. S. Pece, D. Tosoni, S. Confalonieri et al., “Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content,” Cell, vol. 140, no. 1, pp. 62–73, 2010. View at Publisher · View at Google Scholar · View at Scopus
  68. P. Eirew, J. Stingl, A. Raouf et al., “A method for quantifying normal human mammary epithelial stem cells with in vivo regenerative ability,” Nature Medicine, vol. 14, no. 12, pp. 1384–1389, 2008. View at Publisher · View at Google Scholar · View at Scopus