Molecular Oncology
Volume 4, Issue 5 , Pages 404-419 , October 2010

Targeting breast cancer stem cells

Received 8 March 2010 ,Revised 9 June 2010 ,Accepted 9 June 2010.

References 

  1. Abratt RP, Brune D, Dimopoulos MA, Kliment J, Breza J, Selvaggi FP, et al. Randomised phase III study of intravenous vinorelbine plus hormone therapy versus hormone therapy alone in hormone-refractory prostate cancer. Ann. Oncol. 2004;15:1613–1621
  2. Agis H, Jaeger E, Doninger B, Sillaber C, Marosi C, Drach J, et al. In vivo effects of imatinib mesylate on human haematopoietic progenitor cells. Eur. J. Clin. Invest. 2006;36:402–408
  3. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA. 2003;100:3983–3988
  4. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756–760
  5. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136:215–233
  6. Bonner WA, Hulett HR, Sweet RG, Herzenberg LA. Fluorescence activated cell sorting. Rev. Sci. Instrum. 1972;43:404–409
  7. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 1997;3:730–737
  8. Booth B, Zemmel R. Prospects for productivity. Nat. Rev. Drug Discov. 2004;3:451–456
  9. Bouras T, Pal B, Vaillant F, Harburg G, Asselin-Labat ML, Oakes SR, et al. Notch signaling regulates mammary stem cell function and luminal cell-fate commitment. Cell Stem Cell. 2008;3:429–441
  10. Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Opinion: migrating cancer stem cells – an integrated concept of malignant tumour progression. Nat. Rev. Cancer. 2005;5:744–749
  11. Bracken CP, Gregory PA, Kolesnikoff N, Bert AG, Wang J, Shannon MF, et al. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial–mesenchymal transition. Cancer Res. 2008;68:7846–7854
  12. Bray SJ. Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 2006;7:678–689
  13. Campillos M, Kuhn M, Gavin AC, Jensen LJ, Bork P. Drug target identification using side-effect similarity. Science. 2008;321:263–266
  14. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, et al. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res. 2009;69:1302–1313
  15. Chen ST, Dou J, Temple R, Agarwal R, Wu KM, Walker S. New therapies from old medicines. Nat. Biotechnol. 2008;26:1077–1083
  16. Cho RW, Wang X, Diehn M, Shedden K, Chen GY, Sherlock G, et al. Isolation and molecular characterization of cancer stem cells in MMTV-Wnt-1 murine breast tumors. Stem Cells. 2008;26:364–371
  17. Chong CR, Sullivan DJ. New uses for old drugs. Nature. 2007;448:645–646
  18. Chung N, Zhang XD, Kreamer A, Locco L, Kuan PF, Bartz S, et al. Median absolute deviation to improve hit selection for genome-scale RNAi screens. J. Biomol. Screen. 2008;13:149–158
  19. Cicalese A, Bonizzi G, Pasi CE, Faretta M, Ronzoni S, Giulini B, et al. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell. 2009;138:1083–1095
  20. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, et al. Cancer stem cells–perspectives on current status and future directions: AACR workshop on cancer stem cells. Cancer Res. 2006;66:9339–9344
  21. Clarke RB, Anderson E, Howell A, Potten CS. Regulation of human breast epithelial stem cells. Cell Prolif. 2003;36(Suppl. 1):45–58
  22. Clarke RB, Spence K, Anderson E, Howell A, Okano H, Potten CS. A putative human breast stem cell population is enriched for steroid receptor-positive cells. Dev. Biol. 2005;277:443–456
  23. Clarkson B, Fried J, Strife A, Sakai Y, Ota K, Okita T. Studies of cellular proliferation in human leukemia. 3. Behavior of leukemic cells in three adults with acute leukemia given continuous infusions of 3H-thymidine for 8 or 10 days. Cancer. 1970;25:1237–1260
  24. Clarkson BD. Review of recent studies of cellular proliferation in acute leukemia. Natl. Cancer Inst. Monogr. 1969;30:81–120
  25. Clarkson BD, Fried J. Changing concepts of treatment in acute leukemia. Med. Clin. North Am. 1971;55:561–600
  26. Cozzio A, Passegue E, Ayton PM, Karsunky H, Cleary ML, Weissman IL. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev. 2003;17:3029–3035
  27. Creighton CJ, Li X, Landis M, Dixon JM, Neumeister VM, Sjolund A, et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc. Natl. Acad. Sci. USA. 2009;106:13820–13825
  28. Daniel CW, De Ome KB, Young JT, Blair PB, Faulkin LJ. The in vivo life span of normal and preneoplastic mouse mammary glands: a serial transplantation study. Proc. Natl. Acad. Sci. USA. 1968;61:53–60
  29. Daniel CW, Young LJ. Influence of cell division on an aging process. Life span of mouse mammary epithelium during serial propagation in vivo. Exp. Cell Res. 1971;65:27–32
  30. Daniel D, Crawford J. Myelotoxicity from chemotherapy. Semin. Oncol. 2006;33:74–85
  31. Dekaney CM, Gulati AS, Garrison AP, Helmrath MA, Henning SJ. Regeneration of intestinal stem/progenitor cells following doxorubicin treatment of mice. Am. J. Physiol. Gastrointest. Liver Physiol. 2009;297:G461–G470
  32. Deng G, Lu Y, Zlotnikov G, Thor AD, Smith HS. Loss of heterozygosity in normal tissue adjacent to breast carcinomas. Science. 1996;274:2057–2059
  33. DeOme KB, Fauklin LJ, Bern HA, Blair PB. Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H. J. Natl. Cancer Inst. 1959;78:751–757
  34. Diamandis P, Wildenhain J, Clarke ID, Sacher AG, Graham J, Bellows DS, et al. Chemical genetics reveals a complex functional ground state of neural stem cells. Nat. Chem. Biol. 2007;3:268–273
  35. Dick JE. Stem cells: self-renewal writ in blood. Nature. 2003;423:231–233
  36. Dick JE. Stem cell concepts renew cancer research. Blood. 2008;112:4793–4807
  37. Dierks C, Beigi R, Guo GR, Zirlik K, Stegert MR, Manley P, et al. Expansion of Bcr-Abl-positive leukemic stem cells is dependent on Hedgehog pathway activation. Cancer Cell. 2008;14:238–249
  38. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 2003;17:1253–1270
  39. Dontu G, Jackson KW, McNicholas E, Kawamura MJ, Abdallah WM, Wicha MS. Role of notch signaling in cell-fate determination of human mammary stem/progenitor cells. Breast Cancer Res. 2004;6:R605–R615
  40. Eberhard Y, McDermott SP, Wang X, Gronda M, Venugopal A, Wood TE, et al. Chelation of intracellular iron with the antifungal agent ciclopirox olamine induces cell death in leukemia and myeloma cells. Blood. 2009;114:3064–3073
  41. Eirew P, Stingl J, Raouf A, Turashvili G, Aparicio S, Emerman JT, et al. A method for quantifying normal human mammary epithelial stem cells with in vivo regenerative ability. Nat. Med. 2008;14:1384–1389
  42. Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur. J. Cancer. 2009;45:228–247
  43. Eng C. PTEN: one gene, many syndromes. Hum. Mutat. 2003;22:183–198
  44. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998;391:806–811
  45. Fuchs D, Heinold A, Opelz G, Daniel V, Naujokat C. Salinomycin induces apoptosis and overcomes apoptosis resistance in human cancer cells. Biochem. Biophys. Res. Commun. 2009;390:743–749
  46. Furth J, Kahn M. The transmission of leukemia of mice with a single cell. Am. J. Cancer. 1937;31:276–282
  47. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell. 2007;1:555–567
  48. Ginestier C, Liu S, Diebel ME, Korkaya H, Luo M, Brown M, et al. CXCR1 blockade selectively targets human breast cancer stem cells in vitro and in xenografts. J. Clin. Invest. 2010;
  49. Ginestier C, Liu S, Wicha MS. Getting to the root of BRCA1-deficient breast cancer. Cell Stem Cell. 2009;5:229–230
  50. Gonzalez C. Spindle orientation, asymmetric division and tumour suppression in Drosophila stem cells. Nat. Rev. Genet. 2007;8:462–472
  51. Greene SB, Gunaratne PH, Hammond SM, Rosen JM. A putative role for microRNA-205 in mammary epithelial cell progenitors. J. Cell Sci. 2010;
  52. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 2008;10:593–601
  53. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. miRBase: tools for microRNA genomics. Nucleic Acids Res. 2008;36:D154–D158
  54. Gunther S, Kuhn M, Dunkel M, Campillos M, Senger C, Petsalaki E, et al. Super target and matador: resources for exploring drug–target relationships. Nucleic Acids Res. 2008;36:D919–D922
  55. Guo W, Lasky JL, Chang CJ, Mosessian S, Lewis X, Xiao Y, et al. Multi-genetic events collaboratively contribute to Pten-null leukaemia stem-cell formation. Nature. 2008;453:529–533
  56. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA, et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell. 2009;138:645–659
  57. Guzman ML, Neering SJ, Upchurch D, Grimes B, Howard DS, Rizzieri DA, et al. Nuclear factor-kappaB is constitutively activated in primitive human acute myelogenous leukemia cells. Blood. 2001;98:2301–2307
  58. Guzman ML, Rossi RM, Karnischky L, Li X, Peterson DR, Howard DS, et al. The sesquiterpene lactone parthenolide induces apoptosis of human acute myelogenous leukemia stem and progenitor cells. Blood. 2005;105:4163–4169
  59. Guzman ML, Rossi RM, Neelakantan S, Li X, Corbett CA, Hassane DC, et al. An orally bioavailable parthenolide analog selectively eradicates acute myelogenous leukemia stem and progenitor cells. Blood. 2007;110:4427–4435
  60. Harrison H, Farnie G, Howell SJ, Rock RE, Stylianou S, Brennan KR, et al. Regulation of breast cancer stem cell activity by signaling through the Notch4 receptor. Cancer Res. 2010;70:709–718
  61. Hassane DC, Guzman ML, Corbett C, Li X, Abboud R, Young F, et al. Discovery of agents that eradicate leukemia stem cells using an in silico screen of public gene expression data. Blood. 2008;111:5654–5662
  62. Herschkowitz JI, He X, Fan C, Perou CM. The functional loss of the retinoblastoma tumour suppressor is a common event in basal-like and luminal B breast carcinomas. Breast Cancer Res. 2008;10:R75
  63. Herschkowitz JI, Simin K, Weigman VJ, Mikaelian I, Usary J, Hu Z, et al. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol. 2007;8:R76
  64. Hill R, Wu H. PTEN, stem cells, and cancer stem cells. J. Biol. Chem. 2009;284:11755–11759
  65. Hollstein M, Sidransky D, Vogelstein B, Harris CC. p53 mutations in human cancers. Science. 1991;253:49–53
  66. Hope KJ, Jin L, Dick JE. Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity. Nat. Immunol. 2004;5:738–743
  67. Huff CA, Matsui W, Smith BD, Jones RJ. The paradox of response and survival in cancer therapeutics. Blood. 2006;107:431–434
  68. Huntly BJP, Shigematsu H, Deguchi K, Lee BH, Mizuno S, Duclos N, et al. MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell. 2004;6:587–596
  69. Ijiri K, Potten CS. Response of intestinal cells of differing topographical and hierarchical status to ten cytotoxic drugs and five sources of radiation. Br. J. Cancer. 1983;47:175–185
  70. Ijiri K, Potten CS. Further studies on the response of intestinal crypt cells of different hierarchical status to eighteen different cytotoxic agents. Br. J. Cancer. 1987;55:113–123
  71. Iorns E, Lord CJ, Turner N, Ashworth A. Utilizing RNA interference to enhance cancer drug discovery. Nat. Rev. Drug Discov. 2007;6:556–568
  72. Jackson AL, Linsley PS. Recognizing and avoiding siRNA off-target effects for target identification and therapeutic application. Nat. Rev. Drug Discov. 2010;9:57–67
  73. Jeselsohn, R., Brown, N.E., Arendt, L., Klebba, I., Hu, M.G., Kuperwasser, C., Hinds, P.W., 2010. Cyclin D1 kinase activity is required for the self-renewal of mammary stem and progenitor cells that are targets of MMTV-ErbB2 tumorigenesis 17, 65–76.
  74. Jhappan C, Gallahan D, Stahle C, Chu E, Smith GH, Merlino G, et al. Expression of an activated Notch-related int-3 transgene interferes with cell differentiation and induces neoplastic transformation in mammary and salivary glands. Genes Dev. 1992;6:345–355
  75. Jiang J, Hui CC. Hedgehog signaling in development and cancer. Dev. Cell. 2008;15:801–812
  76. Jin L, Hope KJ, Zhai Q, Smadja-Joffe F, Dick JE. Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat. Med. 2006;12:1167–1174
  77. Jin L, Lee EM, Ramshaw HS, Busfield SJ, Peoppl AG, Wilkinson L, et al. Monoclonal antibody-mediated targeting of CD123, IL-3 receptor alpha chain, eliminates human acute myeloid leukemic stem cells. Cell Stem Cell. 2009;5:31–42
  78. Keiser MJ, Setola V, Irwin JJ, Laggner C, Abbas AI, Hufeisen SJ, et al. Predicting new molecular targets for known drugs. Nature. 2009;462:175–181
  79. Kelly PN, Dakic A, Adams JM, Nutt SL, Strasser A. Tumor growth need not be driven by rare cancer stem cells. Science. 2007;317:337
  80. Keniry M, Parsons R. The role of PTEN signaling perturbations in cancer and in targeted therapy. Oncogene. 2008;27:5477–5485
  81. Kennedy JA, Barabe F, Poeppl AG, Wang JC, Dick JE. Comment on “Tumor growth need not be driven by rare cancer stem cells”. Science. 2007;318:1722;author reply 1722
  82. Kordon E, Smith G. An entire functional mammary gland may comprise the progeny from a single cell. Development. 1998;125:1921–1930
  83. Korkaya H, Paulson A, Charafe-Jauffret E, Ginestier C, Brown M, Dutcher J, et al. Regulation of mammary stem/progenitor cells by PTEN/Akt/beta-catenin signaling. PLoS Biol. 2009;7:e1000121
  84. Krivtsov AV, Twomey D, Feng Z, Stubbs MC, Wang Y, Faber J, et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature. 2006;442:818–822
  85. Krutzik PO, Nolan GP. Fluorescent cell barcoding in flow cytometry allows high-throughput drug screening and signaling profiling. Nat. Methods. 2006;3:361–368
  86. Kuperwasser C, Chavarria T, Wu M, Magrane G, Gray JW, Carey L, et al. Reconstruction of functionally normal and malignant human breast tissues in mice. Proc. Natl. Acad. Sci. USA. 2004;101:4966–4971Epub 2004 Mar 4929
  87. Lamb J, Crawford ED, Peck D, Modell JW, Blat IC, Wrobel MJ, et al. The connectivity map: using gene-expression signatures to connect small molecules, genes, and disease. Science. 2006;313:1929–1935
  88. Land CE, McGregor DH. Breast cancer incidence among atomic bomb survivors: implications for radiobiologic risk at low doses. J. Natl. Cancer Inst. 1979;62:17–21
  89. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature. 1994;367:645–648
  90. Lessard J, Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature. 2003;423:255–260
  91. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, et al. Identification of pancreatic cancer stem cells. Cancer Res. 2007;67:1030–1037
  92. Li G, Robinson GW, Lesche R, Martinez-Diaz H, Jiang Z, Rozengurt N, et al. Conditional loss of PTEN leads to precocious development and neoplasia in the mammary gland. Development. 2002;129:4159–4170
  93. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J. Natl. Cancer Inst. 2008;100:672–679
  94. Li Y, Welm B, Podsypanina K, Huang S, Chamorro M, Zhang X, et al. Evidence that transgenes encoding components of the Wnt signaling pathway preferentially induce mammary cancers from progenitor cells. Proc. Natl. Acad. Sci. USA. 2003;100:15853–15858
  95. Lim E, Vaillant F, Wu D, Forrest NC, Pal B, Hart AH, et al. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat. Med. 2009;15:907–913
  96. Liu BY, McDermott SP, Khwaja SS, Alexander CM. The transforming activity of Wnt effectors correlates with their ability to induce the accumulation of mammary progenitor cells. Proc. Natl. Acad. Sci. USA. 2004;101:4158–4163
  97. Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, Jackson KW, et al. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 2006;66:6063–6071
  98. Liu S, Ginestier C, Charafe-Jauffret E, Foco H, Kleer CG, Merajver SD, et al. BRCA1 regulates human mammary stem/progenitor cell fate. Proc. Natl. Acad. Sci. USA. 2008;105:1680–1685
  99. Majeti R, Chao MP, Alizadeh AA, Pang WW, Jaiswal S, Gibbs KD, et al. CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell. 2009;138:286–299
  100. Majeti R, Park CY, Weissman IL. Identification of a hierarchy of multipotent hematopoietic progenitors in human cord blood. Cell Stem Cell. 2007;1:635–645
  101. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial–mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133:704–715
  102. McCulloch EA, Till JE. The radiation sensitivity of normal mouse bone marrow cells, determined by quantitative marrow transplantation into irradiated mice. Radiat. Res. 1960;13:115
  103. McKenzie JL, Gan OI, Doedens M, Wang JC, Dick JE. Individual stem cells with highly variable proliferation and self-renewal properties comprise the human hematopoietic stem cell compartment. Nat. Immunol. 2006;7:1225–1233
  104. Molofsky AV, Pardal R, Iwashita T, Park IK, Clarke MF, Morrison SJ. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature. 2003;425:962–967
  105. Morin RD, O’Connor MD, Griffith M, Kuchenbauer F, Delaney A, Prabhu AL, et al. Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res. 2008;18:610–621
  106. Morrison SJ, Kimble J. Asymmetric and symmetric stem-cell divisions in development and cancer. Nature. 2006;441:1068–1074
  107. Munos B. Lessons from 60 years of pharmaceutical innovation. Nat. Rev. Drug Discov. 2009;8:959–968
  108. Murchison EP, Partridge JF, Tam OH, Cheloufi S, Hannon GJ. Characterization of Dicer-deficient murine embryonic stem cells. Proc. Natl. Acad. Sci. USA. 2005;102:12135–12140
  109. Neumuller RA, Knoblich JA. Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev. 2009;23:2675–2699
  110. Nirenberg A. Managing hematologic toxicities: novel therapies. Cancer Nurs. 2003;26:32S–37S
  111. Nowak D, Stewart D, Koeffler HP. Differentiation therapy of leukemia: 3 decades of development. Blood. 2009;113:3655–3665
  112. O’Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007;445:106–110
  113. Overington JP, Al-Lazikani B, Hopkins AL. How many drug targets are there?. Nat. Rev. Drug Discov. 2006;5:993
  114. Park IK, Qian D, Kiel M, Becker MW, Pihalja M, Weissman IL, et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature. 2003;423:302–305
  115. Park SM, Gaur AB, Lengyel E, Peter ME. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 2008;22:894–907
  116. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, et al. Molecular portraits of human breast tumours. Nature. 2000;406:747–752
  117. Perrimon N, Friedman A, Mathey-Prevot B, Eggert US. Drug-target identification in Drosophila cells: combining high-throughout RNAi and small-molecule screens. Drug Discov. Today. 2007;12:28–33
  118. Peter ME. Regulating cancer stem cells the miR way. Cell Stem Cell. 2010;6:4–6
  119. Phillips TM, McBride WH, Pajonk F. The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J. Natl. Cancer Inst. 2006;98:1777–1785
  120. Pierce GB, Dixon FJ, Verney EL. Teratocarcinogenic and tissue-forming potentials of the cell types comprising neoplastic embryoid bodies. Lab. Invest. 1960;9:583–602
  121. Pierce GB, Speers WC. Tumors as caricatures of the process of tissue renewal: prospects for therapy by directing differentiation. Cancer Res. 1988;48:1996–2004
  122. Pollard SM, Yoshikawa K, Clarke ID, Danovi D, Stricker S, Russell R, et al. Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell. 2009;4:568–580
  123. Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, Dalerba P, et al. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc. Natl. Acad. Sci. USA. 2007;
  124. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ. Efficient tumour formation by single human melanoma cells. Nature. 2008;456:593–598
  125. Rachidi W, Harfourche G, Lemaitre G, Amiot F, Vaigot P, Martin MT. Sensing radiosensitivity of human epidermal stem cells. Radiother. Oncol. 2007;83:267–276
  126. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature. 2001;414:105–111
  127. Rix U, Superti-Furga G. Target profiling of small molecules by chemical proteomics. Nat. Chem. Biol. 2009;5:616–624
  128. Rocha Lima CM, Green MR, Rotche R, Miller WH, Jeffrey GM, Cisar LA, et al. Irinotecan plus gemcitabine results in no survival advantage compared with gemcitabine monotherapy in patients with locally advanced or metastatic pancreatic cancer despite increased tumor response rate. J. Clin. Oncol. 2004;22:3776–3783
  129. Roesch, A., Fukunaga-Kalabis, M., Schmidt, E.C., Zabierowski, S.E., Brafford, P.A., Vultur, A., Basu, D., Gimotty, P., Vogt, T., Herlyn, M., 2010. A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. 141, 583–594.
  130. Rubin LL, de Sauvage FJ. Targeting the Hedgehog pathway in cancer. Nat. Rev. Drug Discov. 2006;5:1026
  131. Rudin CM, Hann CL, Laterra J, Yauch RL, Callahan CA, Fu L, et al. Treatment of medulloblastoma with hedgehog pathway inhibitor GDC-0449. N. Engl. J. Med. 2009;361:1173–1178
  132. Sansone P, Storci G, Tavolari S, Guarnieri T, Giovannini C, Taffurelli M, et al. IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland. J. Clin. Invest. 2007;117:3988–4002
  133. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, et al. Generation of a functional mammary gland from a single stem cell. Nature. 2006;439:84–88
  134. Shimono Y, Zabala M, Cho RW, Lobo N, Dalerba P, Qian D, et al. Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell. 2009;138:592–603
  135. Shipitsin M, Polyak K. The cancer stem cell hypothesis: in search of definitions, markers, and relevance. Lab. Invest. 2008;88:459–463
  136. Shultz LD, Ishikawa F, Greiner DL. Humanized mice in translational biomedical research. Nat. Rev. Immunol. 2007;7:118–130
  137. Shultz LD, Schweitzer PA, Christianson SW, Gott B, Schweitzer IB, Tennent B, et al. Multiple defects in innate and adaptive immunologic function in NOD/LtSz-scid mice. J. Immunol. 1995;154:180–191
  138. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, et al. Identification of human brain tumour initiating cells. Nature. 2004;432:396–401
  139. Smith GH, Medina D. A morphologically distinct candidate for an epithelial stem cell in mouse mammary gland. J. Cell Sci. 1988;90:173–183
  140. Somervaille TC, Cleary ML. Identification and characterization of leukemia stem cells in murine MLL-AF9 acute myeloid leukemia. Cancer Cell. 2006;10:257–268
  141. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. USA. 2001;98:10869–10874
  142. Southam C, Brunschwig A, Dizon Q. Autologous and Homologous Transplantation of Human Cancer. Biological Interactions in Normal and Neoplastic Growth: a Contribution to the Tumor-Host Problem. Boston, MA: Little Brown; 1962;pp. 723–738
  143. Spangrude GJ, Heimfeld S, Weissman IL. Purification and characterization of mouse hematopoietic stem cells. Science. 1988;241:58–62(erratum appears in Science 1989 Jun 2. 244(4908), 1030)
  144. Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, et al. Purification and unique properties of mammary epithelial stem cells. Nature. 2006;439:993–997
  145. Thayer SP, di Magliano MP, Heiser PW, Nielsen CM, Roberts DJ, Lauwers GY, et al. Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis. Nature. 2003;425:851–856
  146. Theunissen JW, de Sauvage FJ. Paracrine hedgehog signaling in cancer. Cancer Res. 2009;69:6007–6010
  147. Troester MA, Herschkowitz JI, Oh DS, He X, Hoadley KA, Barbier CS, et al. Gene expression patterns associated with p53 status in breast cancer. BMC Cancer. 2006;6:276
  148. Trotti A, Colevas AD, Setser A, Rusch V, Jaques D, Budach V, et al. CTCAE v3.0: development of a comprehensive grading system for the adverse effects of cancer treatment. Semin. Radiat. Oncol. 2003;13:176–181
  149. Trowbridge JJ, Scott MP, Bhatia M. Hedgehog modulates cell cycle regulators in stem cells to control hematopoietic regeneration. Proc. Natl. Acad. Sci. USA. 2006;103:14134–14139
  150. Tsai YC, Lu Y, Nichols PW, Zlotnikov G, Jones PA, Smith HS. Contiguous patches of normal human mammary epithelium derived from a single stem cell: implications for breast carcinogenesis. Cancer Res. 1996;56:402–404
  151. Vaillant F, Asselin-Labat ML, Shackleton M, Forrest NC, Lindeman GJ, Visvader JE. The mammary progenitor marker CD61/beta3 integrin identifies cancer stem cells in mouse models of mammary tumorigenesis. Cancer Res. 2008;68:7711–7717
  152. Visvader JE. Keeping abreast of the mammary epithelial hierarchy and breast tumorigenesis. Genes Dev. 2009;23:2563–2577
  153. Von Hoff DD, LoRusso PM, Rudin CM, Reddy JC, Yauch RL, Tibes R, et al. Inhibition of the hedgehog pathway in advanced basal-cell carcinoma. N. Engl. J. Med. 2009;361:1164–1172
  154. Wang J, Wakeman TP, Lathia JD, Hjelmeland AB, Wang XF, White RR, et al. Notch promotes radioresistance of glioma stem cells. Stem Cells. 2010;28:17–28
  155. Wang JC. Evaluating therapeutic efficacy against cancer stem cells: new challenges posed by a new paradigm. Cell Stem Cell. 2007;1:497–501
  156. Wang S, Garcia AJ, Wu M, Lawson DA, Witte ON, Wu H. Pten deletion leads to the expansion of a prostatic stem/progenitor cell subpopulation and tumor initiation. Proc. Natl. Acad. Sci. USA. 2006;103:1480–1485
  157. Wang Y, Baskerville S, Shenoy A, Babiarz JE, Baehner L, Blelloch R. Embryonic stem cell-specific microRNAs regulate the G1-S transition and promote rapid proliferation. Nat. Genet. 2008;40:1478–1483
  158. Wang Y, Schulte BA, LaRue AC, Ogawa M, Zhou D. Total body irradiation selectively induces murine hematopoietic stem cell senescence. Blood. 2006;107:358–366
  159. Watkins DN, Berman DM, Burkholder SG, Wang B, Beachy PA, Baylin SB. Hedgehog signalling within airway epithelial progenitors and in small-cell lung cancer. Nature. 2003;422:313–317
  160. Wei G, Twomey D, Lamb J, Schlis K, Agarwal J, Stam RW, et al. Gene expression-based chemical genomics identifies rapamycin as a modulator of MCL1 and glucocorticoid resistance. Cancer Cell. 2006;10:331–342
  161. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A, et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat. Cell Biol. 2009;11:1487–1495
  162. Weng AP, Ferrando AA, Lee W, Morris JPt, Silverman LB, Sanchez-Irizarry C, et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science. 2004;306:269–271
  163. Whitehead KA, Langer R, Anderson DG. Knocking down barriers: advances in siRNA delivery. Nat. Rev. Drug Discov. 2009;8:129–138
  164. Whitehurst AW, Bodemann BO, Cardenas J, Ferguson D, Girard L, Peyton M, et al. Synthetic lethal screen identification of chemosensitizer loci in cancer cells. Nature. 2007;446:815–819
  165. Wishart DS, Knox C, Guo AC, Cheng D, Shrivastava S, Tzur D, et al. DrugBank: a knowledgebase for drugs, drug actions and drug targets. Nucleic Acids Res. 2008;36:D901–D906
  166. Woodward WA, Chen MS, Behbod F, Alfaro MP, Buchholz TA, Rosen JM. WNT/beta-catenin mediates radiation resistance of mouse mammary progenitor cells. Proc. Natl. Acad. Sci. USA. 2007;104:618–623
  167. Wurdak H, Zhu S, Romero A, Lorger M, Watson J, Chiang CY, et al. An RNAi screen identifies TRRAP as a regulator of brain tumor-initiating cell differentiation. Cell Stem Cell. 2010;6:37–47
  168. Xu N, Papagiannakopoulos T, Pan G, Thomson JA, Kosik KS. MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell. 2009;137:647–658
  169. Yilmaz OH, Valdez R, Theisen BK, Guo W, Ferguson DO, Wu H, et al. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature. 2006;441:475–482
  170. Young LJ, Medina D, DeOme KB, Daniel CW. The influence of host and tissue age on life span and growth rate of serially transplanted mouse mammary gland. Exp. Gerontol. 1971;6:49–56
  171. Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C, et al. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell. 2007;131:1109–1123
  172. Zhang J, Grindley JC, Yin T, Jayasinghe S, He XC, Ross JT, et al. PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature. 2006;441:518–522
  173. Zhang M, Behbod F, Atkinson RL, Landis MD, Kittrell F, Edwards D, et al. Identification of tumor-initiating cells in a p53-null mouse model of breast cancer. Cancer Res. 2008;68:4674–4682

PII: S1574-7891(10)00051-7

doi: 10.1016/j.molonc.2010.06.005

Molecular Oncology
Volume 4, Issue 5 , Pages 404-419 , October 2010