Identification and gene expression profiling of tumor-initiating cells isolated from human osteosarcoma cell lines in an orthotopic mouse model

References

• Heppner GH, Miller BE. Tumor heterogeneity: biological implications and therapeutic consequences. Cancer Metastasis Rev 1983; 2:5 - 23; http://dx.doi.org/10.1007/BF00046903
   PubMed Web of Science ®Google Scholar
• Pardal R, Clarke MF, Morrison SJ. Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 2003; 3:895 - 902; http://dx.doi.org/10.1038/nrc1232
   PubMed Web of Science ®Google Scholar
• Dalerba P, Cho RW, Clarke MF. Cancer stem cells: models and concepts. Annu Rev Med 2007; 58:267 - 284; http://dx.doi.org/10.1146/annurev.med.58.062105.204854
   PubMed Web of Science ®Google Scholar
• 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; http://dx.doi.org/10.1073/pnas.0530291100
   PubMed Web of Science ®Google Scholar
• 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; http://dx.doi.org/10.1158/0008-5472.CAN08-2741
   PubMed Web of Science ®Google Scholar
• Kondo T, Setoguchi T, Taga T. Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc Natl Acad Sci USA 2004; 101:781 - 786; http://dx.doi.org/10.1073/pnas.0307618100
   PubMed Web of Science ®Google Scholar
• Dontu G, Wicha MS. Survival of mammary stem cells in suspension culture: implications for stem cell biology and neoplasia. J Mammary Gland Biol Neoplasia 2005; 10:75 - 86; http://dx.doi.org/10.1007/s10911-005-2542-5
   PubMed Web of Science ®Google Scholar
• Dirks PB. Brain tumor stem cells: bringing order to the chaos of brain cancer. J Clin Oncol 2008; 26:2916 - 2924; http://dx.doi.org/10.1200/JCO.2008.17.6792
   PubMed Web of Science ®Google Scholar
• Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008; 8:755 - 768; http://dx.doi.org/10.1038/nrc2499
   PubMed Web of Science ®Google Scholar
• Jones C, Mackay A, Grigoriadis A, Cossu A, Reis-Filho JS, Fulford L, et al. Expression profiling of purified normal human luminal and myoepithelial breast cells: identification of novel prognostic markers for breast cancer. Cancer Res 2004; 64:3037 - 3045; http://dx.doi.org/10.1158/0008-5472.CAN-03-2028
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Kusumbe AP, Bapat SA. Cancer stem cells and aneuploid populations within developing tumors are the major determinants of tumor dormancy. Cancer Res 2009; 69:9245 - 9253; http://dx.doi.org/10.1158/0008-5472.CAN09-2802
   PubMed Web of Science ®Google Scholar
• Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 2010; 140:62 - 73; http://dx.doi.org/10.1016/j.cell.2009.12.007
   PubMed Web of Science ®Google Scholar
• Horan PK, Melnicoff MJ, Jensen BD, Slezak SE. Fluorescent cell labeling for in vivo and in vitro cell tracking. Methods Cell Biol 1990; 33:469 - 490; http://dx.doi.org/10.1016/S0091-679X(08)60547-6
   PubMedGoogle Scholar
• Boutonnat J, Barbier M, Muirhead K, Mousseau M, Grunwald D, Ronot X, et al. Response of chemosensitive and chemoresistant leukemic cell lines to drug therapy: simultaneous assessment of proliferation, apoptosis and necrosis. Cytometry 2000; 42:50 - 60; http://dx.doi.org/10.1002/(SICI)1097-0320(20000215)42:1<50::AIDCYTO8>3.0.CO;2-C
   PubMedGoogle Scholar
• Marina N, Gebhardt M, Teot L, Gorlick R. Biology and therapeutic advances for pediatric osteosarcoma. Oncologist 2004; 9:422 - 441; http://dx.doi.org/10.1634/theoncologist.9-4-422
   PubMed Web of Science ®Google Scholar
• Gibbs CP, Kukekov VG, Reith JD, Tchigrinova O, Suslov ON, Scott EW, et al. Stem-like cells in bone sarcomas: implications for tumorigenesis. Neoplasia 2005; 7:967 - 976; http://dx.doi.org/10.1593/neo.05394
   PubMed Web of Science ®Google Scholar
• Tirino V, Desiderio V, d'Aquino R, De Francesco F, Pirozzi G, Graziano A, et al. Detection and characterization of CD133+ cancer stem cells in human solid tumours. PLoS ONE 2008; 3:3469; http://dx.doi.org/10.1371/journal.pone.0003469
   PubMed Web of Science ®Google Scholar
• Levings PP, McGarry SV, Currie TP, Nickerson DM, McClellan S, Ghivizzani SC, et al. Expression of an exogenous human Oct-4 promoter identifies tumor-initiating cells in osteosarcoma. Cancer Res 2009; 69:5648 - 5655; http://dx.doi.org/10.1158/0008-5472.CAN-08-3580
   PubMed Web of Science ®Google Scholar
• Adhikari AS, Agarwal N, Wood BM, Porretta C, Ruiz B, Pochampally RR, et al. CD117 and Stro-1 identify osteosarcoma tumor-initiating cells associated with metastasis and drug resistance. Cancer Res 2010; 70:4602 - 4612; http://dx.doi.org/10.1158/0008-5472.CAN-09-3463
   PubMed Web of Science ®Google Scholar
• Luu HH, Kang Q, Park JK, Si W, Luo Q, Jiang W, et al. An orthotopic model of human osteosarcoma growth and spontaneous pulmonary metastasis. Clin Exp Metastasis 2005; 22:319 - 329; http://dx.doi.org/10.1007/s10585-005-0365-9
   PubMed Web of Science ®Google Scholar
• Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007; 1:313 - 323; http://dx.doi.org/10.1016/j.stem.2007.06.002
   PubMed Web of Science ®Google Scholar
• 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; http://dx.doi.org/10.1038/nrc1694
   PubMed Web of Science ®Google Scholar
• Man TK, Chintagumpala M, Visvanathan J, Shen J, Perlaky L, Hicks J, et al. Expression profiles of osteosarcoma that can predict response to chemotherapy. Cancer Res 2005; 65:8142 - 8150; http://dx.doi.org/10.1158/00085472.CAN-05-0985
   PubMed Web of Science ®Google Scholar
• Cleton-Jansen AM, Anninga JK, Briaire-de Bruijn IH, Romeo S, Oosting J, Egeler RM, et al. Profiling of high-grade central osteosarcoma and its putative progenitor cells identifies tumourigenic pathways. Br J Cancer 2009; 101:1909 - 1918; http://dx.doi.org/10.1038/sj.bjc.6605405
   PubMed Web of Science ®Google Scholar
• Kubista B, Klinglmueller F, Bilban M, Pfeiffer M, Lass R, Giurea A, et al. Microarray analysis identifies distinct gene expression profiles associated with histological subtype in human osteosarcoma. Int Orthop 2011; 35:401 - 411; http://dx.doi.org/10.1007/s00264-010-0996-6
   PubMed Web of Science ®Google Scholar
• Di Cosimo S, Baselga J. Management of breast cancer with targeted agents: importance of heterogeneity. [corrected]. Nat Rev Clin Oncol 7:139 - 147; http://dx.doi.org/10.1038/nrclinonc.2009.234
   PubMed Web of Science ®Google Scholar
• Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, et al. DAVID: Database for annotation, visualization and integrated Discovery. Genome Biol 2003; 4:3; http://dx.doi.org/10.1186/gb-2003-4-5-p3
   PubMed Web of Science ®Google Scholar
• Wang L, Park P, Lin CY. Characterization of stem cell attributes in human osteosarcoma cell lines. Cancer Biol Ther 2009; 8:543 - 552; http://dx.doi.org/10.4161/cbt.8.6.7695
   PubMed Web of Science ®Google Scholar
• Klein MJ, Siegal GP. Osteosarcoma: anatomic and histologic variants. Am J Clin Pathol 2006; 125:555 - 581; http://dx.doi.org/10.1309/UC6KQHLD9LV2KENN
   PubMed Web of Science ®Google Scholar
• Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63:5821 - 5828
   PubMed Web of Science ®Google Scholar
• Clarke MF, Fuller M. Stem cells and cancer: two faces of eve. Cell 2006; 124:1111 - 1115; http://dx.doi.org/10.1016/j.cell.2006.03.011
   PubMed Web of Science ®Google Scholar
• Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, et al. 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 2006; 9:391 - 403; http://dx.doi.org/10.1016/j.ccr.2006.03.030
   PubMed Web of Science ®Google Scholar
• Rikhof B, de Jong S, Suurmeijer AJ, Meijer C, van der Graaf WT. The insulin-like growth factor system and sarcomas. J Pathol 2009; 217:469 - 482; http://dx.doi.org/10.1002/path.2499
   PubMed Web of Science ®Google Scholar
• Zhang M, Xuan S, Bouxsein ML, von Stechow D, Akeno N, Faugere MC, et al. Osteoblast-specific knockout of the insulin-like growth factor (IGF) receptor gene reveals an essential role of IGF signaling in bone matrix mineralization. J Biol Chem 2002; 277:44005 - 44012; http://dx.doi.org/10.1074/jbc.M208265200
   PubMed Web of Science ®Google Scholar
• Kappel CC, Velez-Yanguas MC, Hirschfeld S, Helman LJ. Human osteosarcoma cell lines are dependent on insulin-like growth factor I for in vitro growth. Cancer Res 1994; 54:2803 - 2807
   PubMed Web of Science ®Google Scholar
• Pollak M, Sem AW, Richard M, Tetenes E, Bell R. Inhibition of metastatic behavior of murine osteosarcoma by hypophysectomy. J Natl Cancer Inst 1992; 84:966 - 971; http://dx.doi.org/10.1093/jnci/84.12.966
   PubMed Web of Science ®Google Scholar
• Kolb EA, Kamara D, Zhang W, Lin J, Hingorani P, Baker L, et al. R1507, a fully human monoclonal antibody targeting IGF-1R, is effective alone and in combination with rapamycin in inhibiting growth of osteosarcoma xenografts. Pediatr Blood Cancer 2010; 55:67 - 75
   PubMed Web of Science ®Google Scholar
• Ehlen HW, Buelens LA, Vortkamp A. Hedgehog signaling in skeletal development. Birth Defects Res C Embryo Today 2006; 78:267 - 279; http://dx.doi.org/10.1002/bdrc.20076
   PubMedGoogle Scholar
• Jiang J, Hui CC. Hedgehog signaling in development and cancer. Dev Cell 2008; 15:801 - 812; http://dx.doi.org/10.1016/j.devcel.2008.11.010
   PubMed Web of Science ®Google Scholar
• Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010; 141:52 - 67; http://dx.doi.org/10.1016/j.cell.2010.03.015
   PubMed Web of Science ®Google Scholar
• Jones PA, Baylin SB. The epigenomics of cancer. Cell 2007; 128:683 - 692; http://dx.doi.org/10.1016/j.cell.2007.01.029
   PubMed Web of Science ®Google Scholar
• 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; http://dx.doi.org/10.1158/00085472.CAN-07-6353
   PubMed Web of Science ®Google Scholar
• Liang CC, Park AY, Guan JL. In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc 2007; 2:329 - 333; http://dx.doi.org/10.1038/nprot.2007.30
   PubMed Web of Science ®Google Scholar
• Saito Y, Kitamura H, Hijikata A, Tomizawa-Murasawa M, Tanaka S, Takagi S, et al. Identification of therapeutic targets for quiescent, chemotherapy-resistant human leukemia stem cells. Sci Transl Med 2:17
   Google Scholar
• Shachaf CM, Kopelman AM, Arvanitis C, Karlsson A, Beer S, Mandl S, et al. MYC inactivation uncovers pluripotent differentiation and tumour dormancy in hepatocellular cancer. Nature 2004; 431:1112 - 1117; http://dx.doi.org/10.1038/nature03043
   PubMed Web of Science ®Google Scholar
• Lanzkron SM, Collector MI, Sharkis SJ. Hematopoietic stem cell tracking in vivo: a comparison of short-term and long-term repopulating cells. Blood 1999; 93:1916 - 1921
   PubMed Web of Science ®Google Scholar
• R Development Core Team. R: A language and environment for statistical computing 2011; Vienna, Austria R Foundation for Statistical Computing Available at: http://www.R-project.org/
   Google Scholar
• Smyth G, Hu Y, Dunn P, Phipson B. statmod: Statistical Modeling. R package version 1.4.8 2010; Available at: http://CRAN.R-project.org/package=statmod
   Google Scholar
• Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004; 5:80; http://dx.doi.org/10.1186/gb-2004-5-10-r80
   PubMed Web of Science ®Google Scholar
• Simon R, Lam A, Li MC, Ngan M, Menenzes S, Zhao Y. Analysis of gene expression data using BRB-array tools. Cancer Inform 2007; 3:11 - 17
   PubMedGoogle Scholar
• Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I. Controlling the false discovery rate in behavior genetics research. Behav Brain Res 2001; 125:279 - 284; http://dx.doi.org/10.1016/S0166-4328(01)00297-2
   PubMed Web of Science ®Google Scholar
• Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, et al. TM4 microarray software suite. Methods Enzymol 2006; 411:134 - 193; http://dx.doi.org/10.1016/S0076-6879(06)11009-5
   PubMed Web of Science ®Google Scholar