New hope for cancer treatment: Exploring the distinction between normal adult stem cells and cancer stem cells

Pharmacology and Therapeutics

Volumn 119, Issue 1, 2008, Pages 74-82

  Zhao, Robert Chunhua ^a   Zhu, Ya Shu ^a   Shi, Yufang ^b  

^a Center of Excellence in Tissue Engineering   (China)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Cancer stem cell; Cancer treatment; Stem cell

Indexed keywords

ANTINEOPLASTIC AGENT; NOTCH RECEPTOR; SONIC HEDGEHOG PROTEIN; WNT PROTEIN;

ADULT STEM CELL; CANCER CELL; CANCER CHEMOTHERAPY; CANCER PREVENTION; CANCER RADIOTHERAPY; CANCER RECURRENCE; CANCER STEM CELL; CANCER THERAPY; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL RENEWAL; CELL SURVIVAL; HUMAN; METASTASIS; NEOPLASM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TUMOR GROWTH;

ADULT STEM CELLS; ANIMALS; CELL DIFFERENTIATION; HEDGEHOG PROTEINS; HUMANS; NEOPLASMS; NEOPLASTIC STEM CELLS; PHENOTYPE; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 46349087802     PISSN: 01637258     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2008.04.008     Document Type: Review

References (122)

1. Aabo K. Cellular heterogeneity in malignant tumors. The importance of clonal interaction on tumor evolution, response to chemotherapy and metastatic ability evaluated in experimental systems. Dan Med Bull 43 4 (1996) 336-349
2. Abbosh P.H., Montgomery J.S., Starkey J.A., Novotny M., Zuhowski E.G., Egorin M.J., Moseman A.P., Golas A., Brannon K.M., Balch C., Huang T.H., and Nephew K.P. Dominant-negative histone H3 lysine 27 mutant derepresses silenced tumor suppressor genes and reverses the drug-resistant phenotype in cancer cells. Cancer Res 66 11 (2006) 5582-5591
3. Akashi K., He X., Chen J., et al. Transcriptional accessibility for genes of multiple tissues and hematopoietic lineages is hierarchically controlled during early hematopoiesis. Blood 101 (2003) 383-389
4. Al-Hajj M., and Clarke M.F. Self-renewal and solid tumor stem cells. Oncogene 23 43 (2004) 7274-7282
5. Al-Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., and Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100 7 (2003) 3983-3988
6. Androutsellis-Theotokis A., Leker R.R., Soldner F., Hoeppner D.J., Ravin R., Poser S.W., Rueger M.A., Bae S.K., Kittappa R., and McKay R.D. Notch signaling regulates stem cell numbers in vitro and in vivo. Nature 442 7104 (2006) 823-826
7. Arisan S., Buyuktuncer E.D., Palavan-Unsal N., Caşkurlu T., Cakir O.O., and Ergenekon E. Increased expression of EZH2, a polycomb group protein, in bladder carcinoma. Urol Int 75 3 (2005) 252-257
8. Ayton P.M., and Cleary M.L. Molecular mechanisms of leukemogenesis mediated by MLL fusion proteins. Oncogene 20 (2001) 5695-5707
9. Baglole C.J., Ray D.M., Bernstein S.H., et al. More than structural cells, fibroblasts create and orchestrate the tumor microenvironment. Immunol Invest 35 (2006) 297-325
10. Barnhart B.C., and Simon M.C. Metastasis and stem cell pathways. Cancer Metastasis Rev 26 (2007) 261-271
11. Baron M. An overview of the Notch signaling pathway. Semin Cell Dev Biol 14 (2003) 113-119
12. Baum C.M., Weissman I.L., Tsukamoto A.S., Buckle A.M., and Peault B. Isolation of a candidate human hematopoietic stem-cell population. Proc Natl Acad Sci USA 89 (1992) 2804-2808
13. Berman D.M., Karhadkar S.S., Hallahan A.R., Pritchard J.I., Eberhart C.G., Watkins D.N., Chen J.K., Cooper M.K., Taipale J., Olson J.M., and Beachy P.A. Medulloblastoma growth inhibition by hedgehog pathway blockade. Science 297 5586 (2002) 1559-1561
14. Bissell M.J., and Labarge M.A. Context, tissue plasticity, and cancer: are tumor stem cells also regulated by the microenvironment?. Cancer Cell 7 (2005) 17-23
15. Butler L.M., Zhou X., Xu W.S., Scher H.I., Rifkind R.A., Marks P.A., and Richon V.M. The histone deacetylase inhibitor SAHA arrests cancer cell growth, up-regulates thioredoxin-binding protein-2, and down-regulates thioredoxin. Proc Natl Acad Sci U S A 99 18 (2002) 11700-11705
16. Calabrese C., Poppleton H., Kocak M., Hogg T.L., Fuller C., Hamner B., et al. A perivascular niche for brain tumor stem cells. Cancer Cell 11 (2007) 69-82
17. Chen J.K., Taipale J., Cooper M.K., and Beachy P.A. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev 16 21 (2002) 2743-2748
18. Chiba S. Notch signaling in stem cell systems. Stem Cells 24 11 (2006) 2437-2447
19. 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 23 (2005) 10946-10951
20. Cotsarelis G., Kaur P., Dhouailly D., Hengge U., and Bickenbach J. Epithelial stem cells in the skin: definition, markers, localization and functions. Exp Dermatol 8 1 (1999) 80-88
21. Cozzio A., et al. Similar MLL-associated leukemia arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev 17 (2003) 3029-3035
22. Crossen P.E., Broderick R.D., Durie B.G., and Trent J.M. Proliferative characteristics and sister chromatid exchange (SCE) of colony-forming cells (CFU-S) in acute myelogenous leukemia. Cancer Genet Cytogenet 14 3-4 (1985) 267-273
23. 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 24 (2007) 10158-10163
24. Demeter J., Paloczi K., Bibok G., and Lehoczky D. Differentiation and activation antigens on blood mononuclear cells in lymphocytic leukemia before and during IFN-alpha 2B therapy. Leukemia 6 Suppl 3 (1992) 41S-45S
25. Evin G., Sernee M.F., and Masters C.L. Inhibition of gamma-secretase as a therapeutic intervention for Alzheimer's disease: prospects, limitations and strategies. CNS Drugs 20 5 (2006) 351-372
26. 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 (2007) Nov 30
27. Fang B., Zheng C., Liao L., Han Q., Sun Z., Jiang X., and Zhao R.C. Identification of human chronic myelogenous leukemia progenitor cells with hemangioblastic characteristics. Blood 105 7 (2005) 2733-2740
28. 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 20 (2005) 9328-9337
29. Felix C.A., Hosler M.R., Winick N.J., Masterson M., Wilson A.E., and Lange B.J. ALL-1 gene rearrangements in DNA topoisomerase II inhibitor-related leukemia in children. Blood 85 (1995) 3250-3256
30. Fisher P.B., Hermo Jr. H., Prignoli D.R., Weinstein I.B., and Pestka S. Hybrid recombinant human leukocyte interferon inhibits differentiation in murine B-16 melanoma cells. Biochem Biophys Res Commun 119 1 (1984) 108-115
31. Frigola J., Song J., Stizaker C., Hinshelwood R.A., Peinado M.A., and Clark S.J. Epigenetic remodeling in colorectal cancer results in coordinate gene suppression across an entire chromosome band. Nat Genet 38 (2006) 540-549
32. Fukuchi T., Sakamoto M., Tsuda H., Maruyama K., Nozawa S., and Hirohashi S. Beta-catenin mutation in carcinoma of the uterine endometrium. Cancer Res 58 (1998) 3526-3528
33. 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 (1996) 1797-1806
34. Grabher C., von Boehmer H., and Look A.T. Notch 1 activation in the molecular pathogenesis of T-cell acute lymphoblastic leukaemia. Nat Rev Cancer 6 5 (2006) 347-359
35. Grant S., Bhalla K., Weinstein I.B., Pestka S., and Fisher P.B. Differential effect of recombinant human leukocyte interferon on human leukemic and normal myeloid progenitor cells. Biochem Biophys Res Commun 108 3 (1982) 1048-1055
36. Grimaud C., Negre N., and Cavalli G. From genetics to epigenetics: the tale of Polycomb group and trithorax group genes. Chromosome Res 14 (2006) 363-375
37. Grinstein E., and Wernet P. Cellular signaling in normal and cancerous stem cells. Cell Signal 19 12 (2007) 2428-2433
38. Hall B., Dembinski J., Sasser A.K., Studeny M., Andreeff M., and Marini F. Mesenchymal stem cells in cancer: tumor-associated fibroblasts and cell-based delivery vehicles. Int J Hematol 86 1 (2007) 8-16
39. Hatsell S., and Frost A.R. Hedgehog signaling in mammary gland development and breast cancer. J Mammary Gland Biol Neoplasia 12 2-3 (2007) 163-173 Sep
40. He X.C., Yin T., Grindley J.C., Tian Q., Sato T., Tao W.A., et al. PTEN-deficient intestinal stem cells initiate intestinal polyposis. Nat Gen 39 (2007) 189-198
41. Hemmati H.D., Nakano I., Lazareff J.A., Masterman-Smith M., Geschwind D.H., Bronner-Fraser M., and Kornblum H.I. Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A 100 25 (2003) 15178-15183
42. Hu M., Yao J., Cai L., et al. Distinct epigenetic changes in the stromal cells of breast cancers. Nat Genet 37 (2005) 899-905
43. Huang D., Desbois A., and Hou S.T. A novel adenoviral vector which mediates hypoxia-inducible gene expression selectively in neurons. Gene Therapy 12 (2005) 1369-1376
44. Huff C.A., Matsui W.H., Douglas Smith B., and Jones R.J. Strategies to eliminate cancer stem cells: clinical implications. Eur J Cancer 42 9 (2006) 1293-1297
45. Huret J.L., Dessen P., and Bernheim A. An atlas of chromosomes in hematological malignancies. Example: 11q23 and MLL partners. Leukemia 15 (2001) 987-989
46. Jackson A.L., and Loeb L.A. On the origin of multiple mutations in human cancers. Semin Cancer Biol 8 6 (1998) 421-429
47. Jaiswal S., Traver D., Miyamoto T., Akashi K., Lagasse E., and Weissman I.L. Expression of BCR/ABL and BCL-2 in myeloid progenitors leads to myeloid leukemia. Proc Natl Acad Sci U S A 100 17 (2003) 10002-10007
48. Jamieson C.H., Ailles L.E., Dylla S.J., Muijtjens M., Jones C., Zehnder J.L., Gotlib J., Li K., Manz M.G., Keating A., Sawyers C.L., and Weissman I.L. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med 351 7 (2004) 657-667
49. Jiang X., Zhao Y., Smith C., Gasparetto M., Turhan A., Eaves A., and Eaves C. Chronic myeloid leukemia stem cells possess multiple unique features of resistance to BCR-ABL targeted therapies. Leukemia 21 5 (2007) 926-935
50. Kameyama K., Tanaka S., Ishida Y., and Hearing V.J. Interferons modulate the expression of hormone receptors on the surface of murine melanoma cells. J Clin Invest 83 1 (1989) 213-221
51. Karhadkar S.S., Bova G.S., Abdallah N., Dhara S., Gardner D., Maitra A., Isaacs J.T., Berman D.M., and Beachy P.A. Hedgehog signalling in prostate regeneration, neoplasia and metastasis. Nature 431 (2004) 707-712
52. Kléber M., and Sommer L. Wnt signaling and the regulation of stem cell function. Curr Opin Cell Biol 16 6 (2004) 681-687
53. Kobayashi K., Sagae S., Nishioka Y., Tokino T., and Kudo R. Mutations of the beta-catenin gene in endometrial carcinomas. Jpn J Cancer Res 90 (1999) 55-59
54. Koblas T., Zacharovová K., Berková Z., Mindlová M., Girman P., Dovolilová E., Karasová L., and Saudek F. Isolation and characterization of human CXCR4-positive pancreatic cells. Folia Biol (Praha) 53 1 (2007) 13-22
55. Koch A., Denkhaus D., Albrecht S., Leuschner I., von Schweinitz D., and Pietsch T. Childhood hepatoblastomas frequently carry a mutated degradation targeting box of the beta-catenin gene. Cancer Res 59 (1999) 69-273
56. Krivtsov A.V., Twomey D., Feng Z., Stubbs M.C., Wang Y., Faber J., Levine J.E., Wang J., Hahn W.C., Gilliland D.G., Golub T.R., and Armstrong S.A. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature 442 7104 (2006) 818-822
57. Kuzmichev A., Margueron R., Vaquero A., et al. Composition and histone substrates of polycomb repressive group complexes change during cellular differentiation. Proc Natl Acad Sci U S A 102 (2005) 1859-1864
58. La Porta C.A. Drug resistance in melanoma: new perspectives. Curr Med Chem 14 4 (2007) 387-391
59. 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 6464 (1994) 645-648
60. Leszczyniecka M., Roberts T., Dent P., Grant S., and Fisher P.B. Differentiation therapy of human cancer: basic science and clinical applications. Pharmacol Ther 90 2-3 (2001) 105-156
61. Levine S.S., King I.F., and Kingston R.E. Division of labor in polycomb group repression. Trends Biochem Sci 29 (2004) 478-485
62. Li C., Heidt D.G., Dalerba P., Burant C.F., Zhang L., Adsay V., Wicha M., and Clarke M.F. Identification of pancreatic cancer stem cells. Cancer Res 67 3 (2007) 1030-1037
63. Li L., and Neaves W.B. Normal stem cells and cancer stem cells: the niche matters. Cancer Res 66 12 (2006) 6458
64. Li L., and Xie T. Stem cell niche: structure and function. Annu Rev Cell Dev Biol 21 (2005) 605-631
65. Li J., Shi M., Cao Y., Yuan W., Pang T., Li B., Sun Z., Chen L., and Zhao R.C. Knockdown of hypoxia-inducible factor-1alpha in breast carcinoma MCF-7 cells results in reduced tumor growth and increased sensitivity to methotrexate. Biochem Biophys Res Commun 342 4 (2006) 1341-1351
66. Lo Coco F., Nervi C., Avvisati G., and Mandelli F. Acute promyelocytic leukemia: a curable disease. Leukemia 12 (1998) 1866-1880
67. Lobo N.A., Shimono Y., Qian D., and Clarke M.F. The biology of cancer stem cells. Annu Rev Cell Dev Biol 23 (2007) 675-699
68. Luu H.H., Zhang R., Haydon R.C., Rayburn E., Kang Q., Si W., Park J.K., Wang H., Peng Y., Jiang W., and He T.C. Wnt/beta-catenin signaling pathway as a novel cancer drug target. Curr Cancer Drug Targets 4 8 (2004) 653-671
69. 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 7 (2007) 2542-2556
70. Margueron R., Trojer P., and Reinberg D. The key to development: interpreting the histone code?. Curr Opin Genet 15 (2005) 163-176
71. Martinez Arias A., Zecchini V., and Brennan K. CSL-independent Notch signaling: a checkpoint in cell fate decisions during development?. Curr Opin Genet Dev 12 (2002) 524-533
72. Migliore L., and Coppedè F. Genetic and environmental factors in cancer and neurodegenerative diseases. Mutat Res 512 2-3 (2002) 135-153
73. Miletti-Gonzalez K.E., Chen S., Muthukumaran N., et al. The CD44 receptor interacts with P-glycoprotein to promote cell migration and invasion in cancer. Cancer Res 65 (2005) 6660-6667
74. Mintz B., and Illmensee K. Normal genetically mosaic mice produced from malignant teratocarcinoma cells. Proc Natl Acad Sci 72 (1975) 3583-3589
75. Moore K.A., and Lemischka I.R. Stem cells and their niches. Science 11 (2006) 1880-1885
76. Morin P.J., Sparks A.B., Korinek V., Barker N., Clevers H., Vogelstein B., and Kinzler K.W. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275 (1997) 1787-1790
77. Mrózek K., Heinonen K., Lawrence D., Carroll A.J., Koduru P.R., Rao K.W., Strout M.P., Hutchison R.E., Moore J.O., Mayer R.J., Schiffer C.A., and Bloomfield C.D. Adult patients with de novo acute myeloid leukemia and t(9;11)(p22; q23) have a superior outcome to patients with other translocations involving band 11q23: a cancer and leukemia group B study. Blood 90 (1997) 4532-4538
78. Nakamizo A., Marini F., Amano T., Khan A., Studeny M., Gumin J., Chen J., Hentschel S., Vecil G., Dembinski J., Andreeff M., and Lang F.F. Human bone marrow-derived mesenchymal stem cells in the treatment of gliomas. Cancer Res 65 8 (2005) 3307-3318
79. Olsen C.L., Hsu P.P., Glienke J., Rubanyi G.M., and Brooks A.R. Hedgehog-interacting protein is highly expressed in endothelial cells but down-regulated during angiogenesis and in several human tumors. BMC Cancer 4 (2004) 43
80. Pardal R., Clarke M.F., and Morrison S.J. Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 3 (2003) 895-902
81. Pasca di Magliano M., and Hebrok M. Hedgehog signaling in cancer formation and maintenance. Nat Rev Cancer 3 (2003) 903-911
82. Pearce D.J., Taussig D., Zibara K., Smith L.L., Ridler C.M., Preudhomme C., Young B.D., Rohatiner A.Z., Lister T.A., and Bonnet D. AML engraftment in the NOD/SCID assay reflects the outcome of AML: implications for our understanding of the heterogeneity of AML. Blood 107 3 (2006) 1166-1173
83. Perez-Plasencia C., and Duenas-Gonzalez A. Can the state of cancer chemotherapy resistance be reverted by epigenetic therapy?. Mol Cancer 5 (2006) 27
84. Peter A.J., and Stephen B.B. The epigenomics of cancer. Cell 128 (2007) 683-692
85. Pfenninger C.V., Roschupkina T., Hertwig F., Kottwitz D., Englund E., Bengzon J., Jacobsen S.E., and Nuber U.A. 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 67 12 (2007) 5727-5736
86. 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 3 (2007) 973-978
87. Raaphorst F.M., Meijer C.J., Fieret E., Blokzijl T., Mommers E., Buerger H., Packeisen J., Sewalt R.A., Otte A.P., and van Diest P.J. Poorly differentiated breast carcinoma is associated with increased expression of the human polycomb group EZH2 gene. Neoplasia 5 6 (2003) 481-488
88. Rajasekhar V.K., and Vemuri M.C. Molecular insights into the function, fate, and prospects of stem cells. STEM CELLS 23 (2005) 1212-1220
89. Recamier J. Recherche sur le Traitement du Cancer (1829) Paris
90. Reya T., and Clevers H. Wnt signaling in stem cells and cancer. Nature 434 7035 (2005) 843-850
91. 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 7123 (2007) 111-115
92. Richardson G.D., Robson C.N., Lang S.H., et al. CD133, a novel marker for human prostatic epithelial stem cells. J Cell Sci 117 (2004) 3539-3545
93. Ringrose L., and Paro R. Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins. Annu Rev Genet 38 (2004) 413-443
94. Ruizi Altaba A., Sánchez P., and Dahmane N. Gli and hedgehog in cancer: tumors, embryos and stem cells. Nat Rev Cancer 2 5 (2002) 361-372
95. Schlesinger Y., Straussman R., Keshet I., Farkash S., Hecht M., Zimmerman J., Eden E., Yakhini Z., Ben-Shushan E., Reubinoff B.E., Bergman Y., Simon I., and Cedar H. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 39 2 (2007) 232-236
96. Schmelzer E., Zhang L., Bruce A., Wauthier E., Ludlow J., Yao H.L., Moss N., Melhem A., McClelland R., Turner W., Kulik M., Sherwood S., Tallheden T., Cheng N., Furth M.E., and Reid L.M. Human hepatic stem cells from fetal and postnatal donors. J Exp Med 204 8 (2007) 1973-1987
97. Schuettengruber B., Chourrout D., Vervoort M., et al. Genome regulation by polycomb and trithorax proteins. Cell 128 (2007) 735-745
98. Schwartz Y.B., and Pirrotta V. Polycomb silencing mechanisms and the management of genomic programmes. Nat Rev Genet 8 (2007) 9-22
99. Shen Z.X., Shi Z.Z., Fang J., Gu B.W., Li J.M., Zhu Y.M., Shi J.Y., Zheng P.Z., Yan H., Liu Y.F., Chen Y., Shen Y., Wu W., Tang W., Waxman S., De Thé H., Wang Z.Y., Chen S.J., and Chen Z. All-trans retinoic acid/As2O3 combination yields a high quality remission and survival in newly diagnosed acute promyelocytic leukemia. Proc Natl Acad Sci U S A 101 15 (2004) 5328-5335
100. Shih I., and Wang T.L. Notch signaling, gamma-secretase inhibitors, and cancer therapy. Cancer Res 67 5 (2007) 1879-1882
101. Shiras A., Chettiar S.T., Shepal V., Rajendran G., Prasad G.R., and Shastry P. Spontaneous transformation of human adult nontumorigenic stem cells to cancer stem cells is driven by genomic instability in a human model of glioblastoma. Stem Cells 25 6 (2007) 1478-1489
102. 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 18 (2003) 5821-5828
103. Spandidos D.A. Oncogenes and tumor suppressor genes as paradigms in oncogenesis. J BUON 12 Suppl 1 (2007) S9-12
104. Sparmann A., and van Lohuizen M. Polycomb silencers control cell fate, development and cancer. Nature Rev Cancer 6 (2006) 846-856
105. Spira A.I., and Carducci M.A. Differentiation therapy. Curr Opin Pharmacol (2003) 338-343
106. Squazzo S.L., O'Geen H., Komashko V.M., et al. Suz12 binds to silenced regions of the genome in a cell-type-specific manner. Genome Res 16 (2006) 890-900
107. Studeny M., Marini F.C., Dembinski J.L., Zompetta C., Cabreira-Hansen M., Bekele B.N., Champlin R.E., and Andreeff M. Mesenchymal stem cells: potential precursors for tumor stroma and targeted-delivery vehicles for anticancer agents. J Natl Cancer Inst 96 21 (2004) 1593-1603
108. 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 30 (2006) 11154-11159
109. Taipale J., and Beachy P.A. The Hedgehog and Wnt signaling pathways in cancer. Nature 411 6835 (2001) 349-354
110. Tan J., Yang X., Zhuang L., et al. Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes Dev 21 (2007) 1050-1063
111. Tkachuk D.C., Kohler S., and Cleary M.L. Involvement of a homolog of Drosophila trithorax by 11q23 chromosomal translocations in acute leukemia. Cell 71 (1992) 691-700
112. Trosko J.E., and Chang C.C. Role of tumor promotion in affecting the multi-hit nature of carcinogenesis. Basic Life Sci 33 (1985) 261-284
113. Tu S.M., Lin S.H., and Logothetis C.J. Stem-cell origin of metastasis and heterogeneity in solid tumors. Lancet Oncol 3 8 (2002) 508-513
114. Uchida N., Buck D.W., He D., et al. Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA 97 (2000) 14720-14725
115. Valk-Lingbeek M.E., Bruggeman S.W., and van Lohuizen M. Stem cells and cancer; the polycomb connection. Cell 118 (2004) 409-418
116. Virchow R. Editorial. Archiv fuer Pathologische Anatomie und Physiologie und fuer Klinische Medizin 8 (1855) 23
117. Watkins D.N., and Peacock C.D. Hedgehog signalling in foregut malignancy. Biochem Pharmacol 68 6 (2004) 1055-1060
118. Weng A.P., and Aster J.C. Multiple niches for Notch in cancer: context is everything. Curr Opin Genet Dev 14 (2004) 48-54
119. Widschwendter M., Fiegl H., Egle D., Mueller-Holzner E., Spizzo G., Marth C., Weisenberger D.J., Campan M., Young J., Jacobs I., and Laird P.W. Epigenetic stem cell signature in cancer. Nat Genet 39 2 (2007) 157-158
120. Yilmaz O.H., Valdez R., Theisen B.K., Guo W., Ferguson D.O., et al. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 441 (2006) 475-482
121. Zhou S., Schuetz J.D., Bunting K.D., et al. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med 7 (2001) 1028-1034
122. Zhu Y., Ghosh P., Charnay P., Burns D.K., and Prada L.F. Nuerofibromas in NF1. Schwann cell origin and role of tumor environment. Science 296 (2002) 920-922