Purification and characterization of cancer stem cells

Cancer Stem Cells

Volumn , Issue , 2009, Pages 1-14

  Hurt, Elaine M ^a   Farrar, William L ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 79955121492     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1017/CBO9780511605536.002     Document Type: Chapter

References (78)

1. Bignold, L.P., Coghlan, B.L., and Jersmann, H.P. Hansemann, Boveri, chromosomes and the gametogenesis-related theories of tumours, Cell Biol. Int., 30: 640-644, 2006.
2. Sell, S. Stem cell origin of cancer and differentiation therapy, Crit. Rev. Oncol. Hema-tol., 51: 1-28, 2004.
3. Knudson, A.G., Jr., Strong, L.C., and Anderson, D.E. Heredity and cancer in man, Prog. Med. Genet., 9: 113-158, 1973.
4. Wang, J.C., and Dick, J.E. Cancer stem cells: lessons from leukemia, Trends Cell Biol., 15: 494-501, 2005.
5. Reya, T., Morrison, S.J., Clarke, M.F., and Weissman, I.L. Stem cells, cancer, and cancer stem cells, Nature, 414: 105-111, 2001.
6. Huntly, B.J., and Gilliland, D.G. Leukaemia stem cells and the evolution of cancer- stem-cell research, Nat. Rev. Cancer, 5: 311-321, 2005.
7. Southam, C.M., and Brunschwig, A. Quantitative studies of autotransplantation of human cancer, Cancer, 14: 971-978, 1961.
8. Bruce, W.R., and Van Der Gaag, H. ADE quantitative assay for the number of murine lymphoma cells capable of proliferation in vivo, Nature, 199: 79-80, 1963.
9. Hamburger, A.W., and Salmon, S.E. Primary bioassay of human tumor stem cells, Science, 197: 461-463, 1977.
10. Lapidot, T., Sirard, C., Vormoor, J., Murdoch, B., Hoang, T., Caceres-Cortes, J., Minden, M., Paterson, B., Caligiuri, M.A., and Dick, J.E. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice, Nature, 367: 645-648, 1994.
11. Al-Hajj, M., Wicha, M.S., ito-Hernandez, A., Morrison, S.J., and Clarke, M.F. Prospective identification of tumorigenic breast cancer cells, Proc. Natl. Acad. Sci. U. S. A., 100: 3983-3988, 2003.
12. Goodell, M.A., Brose, K., Paradis, G., Conner, A.S., and Mulligan, R.C. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo, J. Exp. Med., 183: 1797-1806, 1996.
13. Wulf, G.G., Wang, R.Y., Kuehnle, I., Weidner, D., Marini, F., Brenner, M.K., Andreeff, M., and Goodell, M.A. A leukemic stem cell with intrinsic drug efflux capacity in acute myeloid leukemia, Blood, 98: 1166-1173, 2001.
14. Feuring-Buske, M., and Hogge, D.E. Hoechst 33342 efflux identifies a subpopulation of cytogenetically normal CD34+CD38- progenitor cells from patients with acute myeloid leukemia, Blood, 97: 3882-3889, 2001.
15. Szotek, P.P., Pieretti-Vanmarcke, R., Masiakos, P.T., Dinulescu, D.M., Connolly, D., Foster, R., Dombkowski, D., Preffer, F., Maclaughlin, D.T., and Donahoe, P.K. Ovarian cancer side population defines cells with stem cell-like characteristics and Mullerian Inhibiting Substance responsiveness, Proc. Natl. Acad. Sci. U. S. A., 103: 11154-11159, 2006.
16. Chiba, T., Kita, K., Zheng, Y.W., Yokosuka, O., Saisho, H., Iwama, A., Nakauchi, H., and Taniguchi, H. Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties, Hepatology, 44: 240-251, 2006.
17. Hirschmann-Jax, C., Foster, A.E., Wulf, G.G., Nuchtern, J.G., Jax, T.W., Gobel, U., Goodell, M.A., and Brenner, M.K. A distinct –side population— of cells with high drug efflux capacity in human tumor cells, Proc. Natl. Acad. Sci. U. S. A., 101:14228-14233, 2004.
18. Setoguchi, T., Taga, T., and Kondo, T. Cancer stem cells persist in many cancer cell lines, Cell Cycle, 3: 414-415, 2004.
19. Shen, G., Shen, F., Shi, Z., Liu, W., Hu, W., Zheng, X., Wen, L., and Yang, X. Identification of cancer stem-like cells in the C6 glioma cell line and the limitation of current identification methods, In Vitro Cell Dev. Biol. Anim., 44: 280-289, 2008.
20. Ho, M.M., Ng, A.V., Lam, S., and Hung, J.Y. Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells, Cancer Res., 67: 4827-4833, 2007.
21. Mitsutake, N., Iwao, A., Nagai, K., Namba, H., Ohtsuru, A., Saenko, V., and Yamashita, S. Characterization of side population in thyroid cancer cell lines: cancer stem-like cells are enriched partly but not exclusively, Endocrinology, 148: 1797-1803, 2007.
22. Wang, J., Guo, L.P., Chen, L.Z., Zeng, Y.X., and Lu, S.H. Identification of cancer stem cell-like side population cells in human nasopharyngeal carcinoma cell line, Cancer Res., 67: 3716-3724, 2007.
23. Patrawala, L., Calhoun, T., Schneider-Broussard, R., Zhou, J., Claypool, K., and Tang, D.G. Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2- cancer cells are similarly tumorigenic, Cancer Res., 65: 6207-6219, 2005.
24. Goodell, M.A., Kinney-Freeman, S., and Camargo, F.D. Isolation and characterization of side population cells, Methods Mol. Biol., 290: 343-352, 2005.
25. Zhou, S., Morris, J.J., Barnes, Y., Lan, L., Schuetz, J.D., and Sorrentino, B.P. Bcrp1 gene expression is required for normal numbers of side population stem cells in mice, and confers relative protection to mitoxantrone in hematopoietic cells in vivo, Proc. Natl. Acad. Sci. U. S. A., 99: 12339-12344, 2002.
26. Yin, L., Castagnino, P., and Assoian, R.K. ABCG2 expression and side population abundance regulated by a transforming growth factor beta-directed epithelial-mesenchymal transition, Cancer Res., 68: 800-807, 2008.
27. Bhatt, R.I., Brown, M.D., Hart, C.A., Gilmore, P., Ramani, V.A., George, N.J., and Clarke, N.W. Novel method for the isolation and characterisation of the putative prostatic stem cell, Cytometry A, 54: 89-99, 2003.
28. Smalley, M.J., and Clarke, R.B. The mammary gland –side population—: a putative stem/progenitor cell marker?, J. Mammary Gland Biol. Neoplasia, 10: 37-47, 2005.
29. Iwatani, H., Ito, T., Imai, E., Matsuzaki, Y., Suzuki, A., Yamato, M., Okabe, M., and Hori, M. Hematopoietic and nonhematopoietic potentials of Hoechst(low)/side population cells isolated from adult rat kidney, Kidney Int., 65: 1604-1614, 2004.
30. Terunuma, A., Jackson, K.L., Kapoor, V., Telford, W.G., and Vogel, J.C. Side population keratinocytes resembling bone marrow side population stem cells are distinct from label-retaining keratinocyte stem cells, J. Invest. Dermatol., 121: 1095-1103, 2003.
31. Triel, C., Vestergaard, M.E., Bolund, L., Jensen, T.G., and Jensen, U.B. Side population cells in human and mouse epidermis lack stem cell characteristics, Exp. Cell Res., 295: 79-90, 2004.
32. Weigmann, A., Corbeil, D., Hellwig, A., and Huttner, W.B. Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells, Proc. Natl. Acad. Sci. U. S. A., 94: 12425-12430, 1997.
33. Yin, A.H., Miraglia, S., Zanjani, E.D., Almeida-Porada, G., Ogawa, M., Leary, A.G., Olweus, J., Kearney, J., and Buck, D.W. AC133, a novel marker for human hematopoietic stem and progenitor cells, Blood, 90: 5002-5012, 1997.
34. Bauer, N., Fonseca, A.V., Florek, M., Freund, D., Jaszai, J., Bornhauser, M., Fargeas, C.A., and Corbeil, D. New insights into the cell biology of hematopoietic progenitors by studying prominin-1 (CD133), Cells Tissues Organs, 188: 127-138, 2008.
35. Maw, M.A., Corbeil, D., Koch, J., Hellwig, A., Wilson-Wheeler, J.C., Bridges, R.J., Kumaramanickavel, G., John, S., Nancarrow, D., Roper, K., Weigmann, A., Huttner, W.B., and Denton, M.J. A frameshift mutation in prominin (mouse)-like 1 causes human retinal degeneration, Hum. Mol. Genet., 9: 27-34, 2000.
36. Singh, S.K., Clarke, I.D., Terasaki, M., Bonn, V.E., Hawkins, C., Squire, J., and Dirks, P.B. Identification of a cancer stem cell in human brain tumors, Cancer Res., 63: 5821-5828, 2003.
37. Singh, S.K., Hawkins, C., Clarke, I.D., Squire, J.A., Bayani, J., Hide, T., Henkelman, R.M., Cusimano, M.D., and Dirks, P.B. Identification of human brain tumour initiating cells, Nature, 432: 396-401, 2004.
38. O’Brien, C.A., Pollett, A., Gallinger, S., and Dick, J.E. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice, Nature, 445: 106-110, 2007.
39. Ricci-Vitiani, L., Lombardi, D.G., Pilozzi, E., Biffoni, M., Todaro, M., Peschle, C., and De, Maria, R. Identification and expansion of human colon-cancer-initiating cells, Nature, 445: 111-115, 2007.
40. Eramo, A., Lotti, F., Sette, G., Pilozzi, E., Biffoni, M., Di, Virgilio, A., Conticello, C., Ruco, L., Peschle, C., and De, Maria, R. Identification and expansion of the tumorigenic lung cancer stem cell population, Cell Death Differ., 15: 504-514, 2008.
41. Ma, S., Chan, K.W., Hu, L., Lee, T.K., Wo, J.Y., Ng, I.O., Zheng, B.J., and Guan, X.Y. Identification and characterization of tumorigenic liver cancer stem/progenitor cells, Gastroenterology, 132: 2542-2556, 2007.
42. Collins, A.T., Berry, P.A., Hyde, C., Stower, M.J., and Maitland, N.J. Prospective identification of tumorigenic prostate cancer stem cells, Cancer Res., 65: 10946-10951, 2005.
43. Du, L., Wang, H., He, L., Zhang, J., Ni, B., Wang, X., Jin, H., Cahuzac, N., Mehrpour, M., Lu, Y., and Chen, Q. CD44 is of functional importance for colorectal cancer stem cells, Clin. Cancer Res., 14: 6751-6760, 2008.
44. Misra, S., Hascall, V.C., Berger, F.G., Markwald, R.R., and Ghatak, S. Hyaluronan, CD44, and cyclooxygenase-2 in colon cancer, Connect. Tissue Res., 49: 219-224, 2008.
45. Ghatak, S., Misra, S., and Toole, B.P. Hyaluronan constitutively regulates ErbB2 phosphorylation and signaling complex formation in carcinoma cells, J. Biol. Chem., 280:8875-8883, 2005.
46. Misra, S., Toole, B.P., and Ghatak, S. Hyaluronan constitutively regulates activation of multiple receptor tyrosine kinases in epithelial and carcinoma cells, J. Biol. Chem., 281: 34936-34941, 2006.
47. Sheridan, C., Kishimoto, H., Fuchs, R.K., Mehrotra, S., Bhat-Nakshatri, P., Turner, C.H., Goulet, R., Jr., Badve, S., and Nakshatri, H. CD44+/CD24- breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis, Breast Cancer Res., 8: R59, 2006.
48. Omara-Opyene, A.L., Qiu, J., Shah, G.V., and Iczkowski, K.A. Prostate cancer invasion is influenced more by expression of a CD44 isoform including variant 9 than by Muc18, Lab. Invest., 84: 894-907, 2004.
49. Li, Y., and Heldin, P. Hyaluronan production increases the malignant properties of mesothelioma cells, Br. J. Cancer, 85: 600-607, 2001.
50. Avigdor, A., Goichberg, P., Shivtiel, S., Dar, A., Peled, A., Samira, S., Kollet, O., Her- shkoviz, R., Alon, R., Hardan, I., Ben-Hur, H., Naor, D., Nagler, A., and Lapidot, T. CD44 and hyaluronic acid cooperate with SDF-1 in the trafficking of human CD34+ stem/progenitor cells to bone marrow, Blood, 103: 2981-2989, 2004.
51. Paradis, V., Eschwege, P., Loric, S., Dumas, F., Ba, N., Benoit, G., Jardin, A., and Bedossa, P. De novo expression of CD44 in prostate carcinoma is correlated with systemic dissemination of prostate cancer, J. Clin. Pathol., 51: 798-802, 1998.
52. Dontu, G., Abdallah, W.M., Foley, J.M., Jackson, K.W., Clarke, M.F., Kawamura, M.J., and Wicha, M.S. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells, Genes Dev., 17: 1253-1270, 2003.
53. Patrawala, L., Calhoun, T., Schneider-Broussard, R., Li, H., Bhatia, B., Tang, S., Reilly, J.G., Chandra, D., Zhou, J., Claypool, K., Coghlan, L., and Tang, D.G. Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumori- genic and metastatic progenitor cells, Oncogene, 25: 1696-1708, 2006.
54. Hurt, E.M., Kawasaki, B.T., Klarmann, G.J., Thomas, S.B., and Farrar, W.L. CD44(+)CD24(-) prostate cells are early cancer progenitor/stem cells that provide a model for patients with poor prognosis, Br. J. Cancer, 98: 756-765, 2008.
55. Dalerba, P., Dylla, S.J., Park, I.K., Liu, R., Wang, X., Cho, R.W., Hoey, T., Gurney, A., Huang, E.H., Simeone, D.M., Shelton, A.A., Parmiani, G., Castelli, C., and Clarke, M.F. Phenotypic characterization of human colorectal cancer stem cells, Proc. Natl. Acad. Sci. U. S. A., 104: 10158-10163, 2007.
56. Li, C., Heidt, D.G., Dalerba, P., Burant, C.F., Zhang, L., Adsay, V., Wicha, M., Clarke, M.F., and Simeone, D.M. Identification of pancreatic cancer stem cells, Cancer Res., 67: 1030-1037, 2007.
57. Prince, M.E., Sivanandan, R., Kaczorowski, A., Wolf, G.T., Kaplan, M.J., Dalerba, P., Weissman, I.L., Clarke, M.F., and Ailles, L.E. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma Proc. Natl. Acad. Sci. U. S. A, 104: 973-978, 2007.
58. Matsui, W., Huff, C.A., Wang, Q., Malehorn, M.T., Barber, J., Tanhehco, Y., Smith, D., Civin, C.I., and Jones, R.J. Characterization of clonogenic multiple myeloma cells, Blood, 103: 2332-2336, 2004.
59. Bonnet, D., and Dick, J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell, Nat. Med., 3: 730-737, 1997.
60. Masters, J.R., Foley, C.L., Bisson, I., and Ahmed, A. Cancer stem cells, BJU Int., 92: 661-662, 2003.
61. Reynolds, B.A., and Weiss, S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system, Science, 255: 1707-1710, 1992.
62. Todaro, M., Alea, M.P., Di Stefano, A.B., Cammareri, P., Vermeulen, L., Iovino, F., Tripodo, C., Russo, A., Gulotta, G., Medema, J.P., and Stassi, G. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4, Cell Stem Cell, 1: 389-402, 2007.
63. Gou, S., Liu, T., Wang, C., Yin, T., Li, K., Yang, M., and Zhou, J. Establishment of clonal colony-forming assay for propagation of pancreatic cancer cells with stem cell properties, Pancreas, 34: 429-435, 2007.
64. Fang, D., Nguyen, T.K., Leishear, K., Finko, R., Kulp, A.N., Hotz, S., Van Belle, P.A., Xu, X., Elder, D.E., and Herlyn, M. A tumorigenic subpopulation with stem cell properties in melanomas, Cancer Res., 65: 9328-9337, 2005.
65. Ponti, D., Costa, A., Zaffaroni, N., Pratesi, G., Petrangolini, G., Coradini, D., Pilotti, S., Pierotti, M.A., and Daidone, M.G. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties, Cancer Res., 65: 5506-5511, 2005.
66. Yuan, X., Curtin, J., Xiong, Y., Liu, G., Waschsmann-Hogiu, S., Farkas, D.L., Black, K.L., and Yu, J.S. Isolation of cancer stem cells from adult glioblastoma multiforme, Oncogene, 23: 9392-9400, 2004.
67. Galli, R., Binda, E., Orfanelli, U., Cipelletti, B., Gritti, A., De Vitis, S., Fiocco, R., Foroni, C., Dimeco, F., and Vescovi, A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma, Cancer Res., 64: 7011-7021, 2004.
68. Gibbs, C.P., Kukekov, V.G., Reith, J.D., Tchigrinova, O., Suslov, O.N., Scott, E.W., Ghivizzani, S.C., Ignatova, T.N., and Steindler, D.A. Stem-like cells in bone sarcomas: implications for tumorigenesis, Neoplasia, 7: 967-976, 2005.
69. Suslov, O.N., Kukekov, V.G., Ignatova, T.N., and Steindler, D.A. Neural stem cell heterogeneity demonstrated by molecular phenotyping of clonal neurospheres, Proc. Natl. Acad. Sci. U. S. A, 99: 14506-14511, 2002.
70. Jensen, J.B., and Parmar, M. Strengths and limitations of the neurosphere culture system, Mol. Neurobiol., 34: 153-161, 2006.
71. Clarke, M.F., Dick, J.E., Dirks, P.B., Eaves, C.J., Jamieson, C.H., Jones, D.L., Visvader, J., Weissman, I.L., and Wahl, G.M. Cancer stem cells - perspectives on current status and future directions: AACR Workshop on Cancer Stem Cells, Cancer Res., 66: 9339-9344, Quote from p. 9340.
72. Flanagan, S.P. –Nude,— a new hairless gene with pleiotropic effects in the mouse, Genet. Res., 8: 295-309, 1966.
73. Shultz, L.D., Schweitzer, P.A., Christianson, S.W., Gott, B., Schweitzer, I.B., Tennent, B., McKenna, S., Mobraaten, L., Rajan, T.V., and Greiner, D.L. Multiple defects in innate and adaptive immunologic function in NOD/LtSz-SCID mice, J. Immunol., 154: 180-191, 1995.
74. Bosma, G.C., Custer, R.P., and Bosma, M.J. A severe combined immunodeficiency mutation in the mouse, Nature, 301: 527-530, 1983.
75. Collins, A.T., Habib, F.K., Maitland, N.J., and Neal, D.E. Identification and isolation of human prostate epithelial stem cells based on alpha(2)beta(1)-integrin expression, J. Cell Sci., 114: 3865-3872, 2001.
76. Al-Hajj, M., and Clarke, M.F. Self-renewal and solid tumor stem cells, Oncogene, 23: 7274-7282, 2004.
77. Lee, J., Kotliarova, S., Kotliarov, Y., Li, A., Su, Q., Donin, N.M., Pastorino, S., Purow, B.W., Christopher, N., Zhang, W., Park, J.K., and Fine, H.A. 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, 2006.
78. Tang, D.G., Patrawala, L., Calhoun, T., Bhatia, B., Choy, G., Schneider-Broussard, R., and Jeter, C. Prostate cancer stem/progenitor cells: identification, characterization, and implications, Mol. Carcinog., 46: 1-14, 2007.