Advertisement

Isolation and Characterization of Cancer Stem Cells (CSCs)

  • Namasivayam Nalini
  • Bichandarkoil Jayaram Pratima
Chapter
  • 60 Downloads

Abstract

The tumour-initiating cancer stem cells (CSCs) are neoplastic cells which produce self-renewable and heterogeneous population of pluripotent stem cells. The exploration on stationary and coursing CSCs because of protection from regular treatments and powerlessness in complete annihilation of malignant growth is basic for creating novel helpful systems for a progressively successful decrease in the danger of tumour metastasis and disease repeat. This chapter incorporates data about various strategies for discovery and separation, side population, cell markers and establishment of CSC culture, as well as attributes of CSCs, for example, tumorigenicity, and pathways related with self-restoration and the ability of the histological tumour recovery in different malignant growths.

Keywords

Cancer stem cells Cellular markers Self-renewal Side population Tumorigenicity 

References

  1. 1.
    Abbaszadegan MR, Bagheri V, Razavi MS, Momtazi AA, Sahebkar A, Gholamin M (2017) Isolation, identification, and characterization of cancer stem cells: a review. J Cell Physiol 232(8):2008–2018PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Akbarzadeh M, Movassaghpour AA, Ghanbari H, Kheirandish M, Fathi Maroufi N, Rahbarghazi R, Samadi N (2017) The potential therapeutic effect of melatonin on human ovarian cancer by inhibition of invasion and migration of cancer stem cells. Sci Rep 7(1):17062PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Akbarzadeh M, Rahbarghazi R, Nabat E, Movassaghpour AA, Shanehbandi D, Maragheh BFA, Matluobi D, Barazvan B, Kazemi M, Samadi N, Nouri M (2017) The impact of different extracellular matrices on melatonin effect in proliferation and stemness properties of ovarian cancer cells. Biomed Pharmacother 87:288–295PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100(7):3983–3988PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Almanaa TN, Geusz ME, Jamasbi RJ (2013) A new method for identifying stem-like cells in esophageal cancer cell lines. J Cancer 4(7):536–548PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Ferrero E, Malavasi F (1999) The metamorphosis of a molecule: from soluble enzyme to the leukocyte receptor CD38. J Leuk Biol 65(2):151–161; Friedrich J, Ebner R, Kunz‐Schughart LA (2007) Experimental anti‐tumor therapy in 3‐D: spheroids—old hat or new challenge? Int J Radiat Biol 83(11–12):849–871Google Scholar
  7. 7.
    Ames E, Canter RJ, Grossenbacher SK, Mac S, Chen M, Smith RC, Murphy WJ (2015) NK cells preferentially target tumor cells with a cancer stem cell phenotype. J Immunol 195:1500447–1504019CrossRefGoogle Scholar
  8. 8.
    Balzano F, Cruciani S, Basoli V, Santaniello S, Facchin F, Ventura C, Maioli M (2018) MiR200 and MiR302: two big families influencing stem cell behavior. Molecules 23(2):282PubMedCentralCrossRefGoogle Scholar
  9. 9.
    Batlle E, Clevers H (2017) Cancer stem cells revisited. Nat Med 23(10):1124–1134PubMedCrossRefGoogle Scholar
  10. 10.
    Bourguignon LYW, Wong G, Earle C, Chen L (2012) Hyaluronan- CD44v3 interaction with Oct4/Sox2/Nanog promotes miR-302 expression leading to self-renewal, clonal formation and cisplatin resistance in cancer stem cells from head and neck squamous cell carcinoma. J Biol Chem M111:308528–332824Google Scholar
  11. 11.
    Bowen MA, Patel DD, Li X, Modrell B, Malacko AR, Wang W-C, Francke U (1995) Cloning, mapping, and characterization of activated leukocyte-cell adhesion molecule (ALCAM), a CD6 ligand. J Exp Med 181(6):2213–2220PubMedCrossRefGoogle Scholar
  12. 12.
    Brown HK, Tellez-Gabriel M, Heymann D (2017) Cancer stem cells in osteosarcoma. Cancer Lett 386:189–195PubMedCrossRefGoogle Scholar
  13. 13.
    Duxbury MS, Ito H, Zinner MJ, Ashley SW, Whang EE (2003) CEACAM6 gene silencing impairs anoikis resistance and suppresses metastasis of pancreatic adenocarcinoma. J Surg Res 114(2):241CrossRefGoogle Scholar
  14. 14.
    Fan Z, Xue W, Dou M, Li L, Lu J, Ma B, Zhao J (2018) Bushenshugan formula attenuates the development of lung cancer by inhibiting epithelial-mesenchymal transition. Cell Physiol Biochem 47(5):1977–1988PubMedCrossRefGoogle Scholar
  15. 15.
    Friedrich J, Seidel C, Ebner R, Kunz-Schughart LA (2009) Spheroid-based drug screen: considerations and practical approach. Nat Protoc 4(3):309–324PubMedCrossRefGoogle Scholar
  16. 16.
    Gemei M, Mirabelli P, Di Noto R, Corbo C, Iaccarino A, Zamboli A, Salvatore F (2013) CD66c is a novel marker for colorectal cancer stem cell isolation, and its silencing halts tumor growth in vivo. Cancer 119(4):729–738PubMedCrossRefGoogle Scholar
  17. 17.
    Gilbert CA, Ross AH (2009) Cancer stem cells: cell culture, markers, and targets for new therapies. J Cell Biochem 108(5):1031–1038PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Golebiewska A, Brons NHC, Bjerkvig R, Niclou SP (2011) Critical appraisal of the side population assay in stem cell and cancer stem cell research. Cell Stem Cell 8(2):136–147PubMedCrossRefGoogle Scholar
  19. 19.
    Guo W, Lasky JL, Wu H (2006) Cancer stem cells. Pediatr Res 59(S4):59R–64RPubMedCrossRefGoogle Scholar
  20. 20.
    Haji-Karim M, Carisson J (1978) Proliferation and viability in cellular spheroids of human origin. Cancer Res 38(5):1457–1464PubMedPubMedCentralGoogle Scholar
  21. 21.
    Haraguchi N, Ishii H, Mimori K, Tanaka F, Ohkuma M, Kim HM, Akita H, Takiuchi D, Hatano H, Nagano H, Barnard GF, Doki Y, Mori M (2010) CD13 is a therapeutic target in human liver cancer stem cells. J Clin Invest 120(9):3326–3339PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    He J, Liu Y, Zhu T, Zhu J, DiMeco F, Vescovi AL, Heth JA, Muraszko KM, Fan X, Lubman DM (2012) CD90 is identified as a candidate marker for cancer stem cells in primary high-grade gliomas using tissue microarrays. Mol Cell Proteomics 11(6):M111.010744PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Hirschhaeuser F, Menne H, Dittfeld C, West J, Mueller-Klieser W, Kunz-Schughart LA (2010) Multicellular tumor spheroids: an under-estimated tool is catching up again. J Biotechnol 148(1):3–15; Horst D, Kriegl L, Engel J, Kirchner T, Jung A (2009) Prognostic significance of the cancer stem cell markers CD133, CD44, and CD166 in colorectal cancer. Cancer Investig 27(8):844–850Google Scholar
  24. 24.
    Hu P, Zhang W, Xin H, Deng G (2016) Single cell isolation and analysis. Front Cell Dev Biol 4:116PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Hu Y, Smyth GK (2009) ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods 347(1–2):70–78PubMedPubMedCentralGoogle Scholar
  26. 26.
    Gangavarpu KJ, Huss WJ (2011) Isolation and applications of prostate side population cells based on dye cycle violet efflux. Curr Protoc Toxicol 47(1):22.22.21–22.22.14Google Scholar
  27. 27.
    Huang T-H, Hsu H-M, Huang CYF (2018) Abstract LB-051: an Astragalus-based Chinese herbal medicine extraction inhibits cancer stem cell growth and sensitizes of drug-resistant human non-small cell lung cancer cells for targeted therapy. AACR 78:LB-051Google Scholar
  28. 28.
    Ishiguro T, Ohata H, Sato A, Yamawaki K, Enomoto T, Okamoto K (2017) Tumor-derived spheroids: relevance to cancer stem cells and clinical applications. Cancer Sci 108(3):283–289PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Islam F, Qiao B, Smith RA, Gopalan V, Lam AK-Y (2015) Cancer stem cell: fundamental experimental pathological concepts and updates. Exp Mol Pathol 98(2):184–191PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Jaggupilli A, Elkord E (2012) Significance of CD44 and CD24 as cancer stem cell markers: an enduring ambiguity. Clin Dev Immunol 2012:708036PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Jeon Y-K, Kim S-H, Choi S-H, Kim K-H, Yoo B-C, Ku J-L, Park J-G (2010) Promoter hypermethylation and loss of CD133 gene expression in colorectal cancers. World J Gastroenterol 16(25):3153PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Keysar SB, Jimeno A (2010) More than markers: biological significance of cancer stem cell-defining molecules. Mol Cancer Ther 9:2450–2457PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Klonisch T, Wiechec E, Hombach-Klonisch S, Ande SR, Wesselborg S, Schulze-Osthoff K, Los M (2008) Cancer stem cell markers in common cancers–therapeutic implications. Trends Mol Med 14(10):450–460PubMedCrossRefGoogle Scholar
  34. 34.
    Kohara H, Watanabe K, Shintou T, Nomoto T, Okano M, Shirai T, Miyazaki T, Tabata Y (2013) The use of fluorescent indoline dyes for side population analysis. Biomaterials 34(4):1024–1032PubMedCrossRefGoogle Scholar
  35. 35.
    Kosovsky M (2012) Cancer stem cell research. Bioscience 3:1–8Google Scholar
  36. 36.
    Kreso A, O’Brien CA (2008) Colon cancer stem cells. Curr Protoc Stem Cell Biol 7(1):3.1.1–3.1.12CrossRefGoogle Scholar
  37. 37.
    Kristiansen G, Pilarsky C, Wissmann C, Stephan C, Weissbach L, Loy V, Loening S, Dietel M, Rosenthal A (2003) ALCAM/CD166 is up-regulated in low- grade prostate cancer and progressively lost in high-grade lesions. Prostate 54(1):34–43PubMedCrossRefGoogle Scholar
  38. 38.
    Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, Minden M, Paterson B, Caligiuri MA, Dick JE (1994) A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367(6464):645–648PubMedCrossRefGoogle Scholar
  39. 39.
    Lawrenson K, Grun B, Gayther SA (2012) Heterotypic three- dimensional in vitro modeling of stromal-epithelial interactions during ovarian cancer initiation and progression. J Vis Exp 66:e4206Google Scholar
  40. 40.
    Lee TKW, Castilho A, Cheung VCH, Tang KH, Ma S, Ng IOL (2011) CD24+ liver tumor-initiating cells drive self-renewal and tumor initiation through STAT3-mediated NANOG regulation. Cell Stem Cell 9(1):50–63PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, Simeone DM (2007) Identification of pancreatic cancer stem cells. Cancer Res 67(3):1030–1037PubMedCrossRefGoogle Scholar
  42. 42.
    Liang S, Furuhashi M, Nakane R, Nakazawa S, Goudarzi H, Hamada J, Iizasa H (2013) Isolation and characterization of human breast cancer cells with SOX2 promoter activity. Biochem Biophys Res Commun 437(2):205–211PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Lianidou ES, Markou A (2011) Circulating tumor cells in breast cancer: detection systems, molecular characterization, and future challenges. Clin Chem 57(9):1242–1255PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Lin WM, Karsten U, Goletz S, Cheng RC, Cao Y (2011) Expression of CD176 (Thomsen-Friedenreich antigen) on lung, breast and liver cancer-initiating cells. Int J Exp Pathol 92(2):97–105PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Longati P, Jia X, Eimer J, Wagman A, Witt M-R, Rehnmark S, Verbeke C, Toftgård R, Löhr M, Heuchel RL (2013) 3D pancreatic carcinoma spheroids induce a matrix-rich, chemoresistant phenotype offering a better model for drug testing. BMC Cancer 13(1):95PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Lovitt C, Shelper T, Avery V (2014) Advanced cell culture techniques for cancer drug discovery. Biology 3(2):345–367PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Jiang F, Qiu Q, Khanna A, Todd NW, Deepak J, Xing L, Wang H, Liu Z, Su Y, Stass SA, Katz RL (2009) Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Res 7(3):330–338PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Kemper K, Sprick MR, de Bree M, Scopelliti A, Vermeulen L, Hoek M, Stassi G (2010) The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation. Cancer Res 70:719–729PubMedCrossRefGoogle Scholar
  49. 49.
    Kern SE, Shibata D (2007) The fuzzy math of solid tumor stem cells: a perspective. Cancer Res 67(19):8985–8988PubMedCrossRefGoogle Scholar
  50. 50.
    Ma S, Chan KW, Hu L, Lee TKW, Wo JYH, Ng IOL, Zheng BJ, Guan XY (2007) Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology 132(7):2542–2556PubMedCrossRefGoogle Scholar
  51. 51.
    Maeda S, Shinchi H, Kurahara H, Mataki Y, Maemura K, Sato M, Takao S (2008) CD133 expression is correlated with lymph node metastasis and vascular endothelial growth factor-C expression in pancreatic cancer. Br J Cancer 98(8):1389–1397PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Masters JR, Foley CL, Bisson I, Ahmed A (2003) Cancer stem cells. BJU Int 92(7):661–662PubMedCrossRefGoogle Scholar
  53. 53.
    Mather JP (2012) In vitro models. Stem Cells 30(2):95–99PubMedCrossRefGoogle Scholar
  54. 54.
    Mauri FA, Pinato DJ, Trivedi P, Sharma R, Shiner RJ (2012) Isogeneic comparison of primary and metastatic lung cancer identifies CX3CR1 as a molecular determinant of site-specific metastatic diffusion. Oncol Rep 28(2):647–653PubMedCrossRefGoogle Scholar
  55. 55.
    Mayer B, Klement G, Kaneko M, Man S, Jothy S, Rak J, Kerbel RS (2001) Multicellular gastric cancer spheroids recapitulate growth pattern and differentiation phenotype of human gastric carcinomas. Gastroenterology 121(4):839–852PubMedCrossRefGoogle Scholar
  56. 56.
    Mehta G, Hsiao AY, Ingram M, Luker GD, Takayama S (2012) Opportunities and challenges for use of tumor spheroids as models to test drug delivery and efficacy. J Control Release 164(2):192–204PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Miltenyi S, Müller W, Weichel W, Radbruch A (1990) High gradient magnetic cell separation with MACS. Cytometry 11(2):231–238PubMedCrossRefGoogle Scholar
  58. 58.
    Mima K, Okabe H, Ishimoto T, Hayashi H, Nakagawa S, Kuroki H, Baba H (2012) CD44s regulates the TGF-β-mediated mesenchymal phenotype and is associated with poor prognosis in patients with hepatocellular carcinoma. Cancer Res 72:3414–3423. 0299.2012PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    Moghbeli M, Moghbeli F, Forghanifard MM, Abbaszadegan MR (2014) Cancer stem cell detection and isolation. Med Oncol 31(9):69PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Most C (1992) Molecular features of CD34: a hemopoietic progenitor cell-associated molecule. Leukemia 6(1):31–36Google Scholar
  61. 61.
    Munshi A, Hobbs M, Meyn RE (2005) Clonogenic cell survival assay. Chemosensitivity 110:21–28CrossRefGoogle Scholar
  62. 62.
    Nastaly P, Filipska M, Morrissey C, Eltze E, Semjonow A, Brandt B, Pantel K, Bednarz-Knoll N (2018) ALDH1-positive intratumoral stromal cells indicate epithelial differentiation and good prognosis in prostate cancer. Transl Res 203:49–56PubMedCrossRefGoogle Scholar
  63. 63.
    Nerada Z, Hegyi Z, Szepesi Á, Tóth S, Hegedüs C, Várady G, Telbisz Á (2016) Application of fluorescent dye substrates for functional characterization of ABC multidrug transporters at a single cell level. Cytometry 89(9):826–834PubMedCrossRefGoogle Scholar
  64. 64.
    Nguyen LV, Vanner R, Dirks P, Eaves CJ (2012) Cancer stem cells: an evolving concept. Nat Rev Cancer 12(2):133–143PubMedCrossRefGoogle Scholar
  65. 65.
    Niess H, Camaj P, Renner A, Ischenko I, Zhao Y, Krebs S, Bruns CJ (2015) Side population cells of pancreatic cancer show characteristics of cancer stem cells responsible for resistance and metastasis. Target Oncol 10(2):215–227PubMedCrossRefGoogle Scholar
  66. 66.
    Ning N, Pan Q, Zheng F, Teitz-Tennenbaum S, Egenti M, Yet J, Li M, Ginestier C, Wicha MS, Moyer JS, Prince ME, Xu Y, Zhang XL, Huang S, Chang AE, Li Q (2012) Cancer stem cell vaccination confers significant antitumor immunity. Cancer Res 72(7):1853–1864PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    O’Brien CA, Kreso A, Jamieson CH (2010) Cancer stem cells and self-renewal. Clin Cancer Res 16:3113–3120PubMedCrossRefGoogle Scholar
  68. 68.
    O’Conor CJ, Chen T, González I, Cao D, Peng Y (2018) Cancer stem cells in triple-negative breast cancer: a potential target and prognostic marker. Biomark Med 12:813–820PubMedCrossRefGoogle Scholar
  69. 69.
    Orecchioni S, Bertolini F (2016) Characterization of cancer stem cells. Methods Mol Biol 1464:49–62PubMedCrossRefGoogle Scholar
  70. 70.
    Panaccione A, Zhang Y, Ryan M, Moskaluk CA, Anderson KS, Yarbrough WG, Ivanov SV (2017) MYB fusions and CD markers as tools for authentication and purification of cancer stem cells from salivary adenoid cystic carcinoma. Stem Cell Res 21:160–166PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, Bernard L, Viale G, Pelicci PG, Di Fiore PP (2010) Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 140(1):62–73PubMedCrossRefGoogle Scholar
  72. 72.
    Pietra G, Manzini C, Vitale M, Balsamo M, Ognio E, Boitano M, Queirolo P, Moretta L, Mingari MC (2009) Natural killer cells kill human melanoma cells with characteristics of cancer stem cells. Int Immunol 21(7):793–801PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Rahimi K, Fuchtbauer AC, Fathi F, Mowla SJ, Fuchtbauer E-M (2019) Isolation of cancer stem cells by selection for miR-302 expressing cells. PeerJ 7:e6635PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Rege TA, Hagood JS (2006) Thy-1, a versatile modulator of signaling affecting cellular adhesion, proliferation, survival, and cytokine/growth factor responses. Biochim Biophys Acta 1763(10):991–999PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Reim F, Dombrowski Y, Ritter C, Buttmann M, Hausler S, Ossadnik M, Krockenberger M, Beier D, Beier CP, Dietl J, Becker JC, Hönig A, Wischhusen J (2009) Immunoselection of breast and ovarian cancer cells with trastuzumab and natural killer cells: selective escape of CD44high/CD24low/HER2low breast cancer stem cells. Cancer Res 69:8058–8066PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Resnicoff M, Medrano EE, Podhajcer OL, Bravo AI, Bover L, Mordoh J (1987) Subpopulations of MCF7 cells separated by Percoll gradient centrifugation: a model to analyze the heterogeneity of human breast cancer. Proc Natl Acad Sci U S A 84(20):7295–7299PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Rezaie P, Khoei S, Khoee S, Shirvalilou S, Mahdavi SR (2018) Evaluation of combined effect of hyperthermia and ionizing radiation on cytotoxic damages induced by IUdR-loaded PCL-PEG-coated magnetic nanoparticles in spheroid culture of U87MG glioblastoma cell line. Int J Radiat Biol 94:1–36CrossRefGoogle Scholar
  78. 78.
    Ricardo S, Vieira AF, Gerhard R, Leitao D, Pinto R, Cameselle-Teijeiro JF, Milanezi F, Schmitt F, Paredes J (2011) Breast cancer stem cell markers CD44, CD24 and ALDH1: expression distribution within intrinsic molecular subtype. J Clin Pathol 64(11):937–946PubMedCrossRefGoogle Scholar
  79. 79.
    Rosca AM, Burlacu A (2010) Isolation of a mouse bone marrow population enriched in stem and progenitor cells by centrifugation on a Percoll gradient. Biotechnol Appl Biochem 55(4):199–208PubMedCrossRefGoogle Scholar
  80. 80.
    Santini MT, Rainaldi G (1999) Three-dimensional spheroid model in tumor biology. Pathobiology 67(3):148–157PubMedCrossRefGoogle Scholar
  81. 81.
    Sarry J-E, Murphy K, Perry R, Sanchez PV, Secreto A, Keefer C, Swider CR, Strzelecki AC, Cavelier C, Récher C, Mansat-De Mas V, Delabesse E, Danet-Desnoyers G, Carroll M (2011) Human acute myelogenous leukemia stem cells are rare and heterogeneous when assayed in NOD/SCID/IL2Rγc-deficient mice. J Clin Invest 121(1):384–395PubMedCrossRefGoogle Scholar
  82. 82.
    Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, Gasser M, Frank MH (2008) Identification of cells initiating human melanomas. Nature 451(7176):345–349PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Scheel C, Weinberg RA (2012) Cancer stem cells and epithelial–mesenchymal transition. In: Concepts and molecular links. Elsevier, Amsterdam, pp 396–403Google Scholar
  84. 84.
    Pastrana E, Silva-Vargas V, Doetsch F (2011) Eyes wide open: a critical review of sphere-formation as an assay for stem cells. Cell Stem Cell 8(5):486–498PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Kalisky T, Quake SR (2011) Single-cell genomics. Nat Methods 8(4):311–314; Katt ME, Placone AL, Wong AD, Xu ZS, Searson PC (2016) In vitro tumor models: advantages, disadvantages, variables, and selecting the right platform. Front Bioeng Biotechnol 4:12Google Scholar
  86. 86.
    Schmidt P, Kopecky C, Hombach A, Zigrino P, Mauch C, Abken H (2011) Eradication of melanomas by targeted elimination of a minor subset of tumor cells. Proc Natl Acad Sci U S A 108(6):2474–2479PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat M-L, Wu L, Lindeman GJ, Visvader JE (2006) Generation of a functional mammary gland from a single stem cell. Nature 439(7072):84–88PubMedCrossRefGoogle Scholar
  88. 88.
    Shaheen S, Ahmed M, Lorenzi F, Nateri AS (2016) Spheroid- formation (colonosphere) assay for in vitro assessment and expansion of stem cells in colon cancer. Stem Cell Rev Rep 12(4):492–499PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Stein AM, Bottino D, Modur V, Branford S, Kaeda J, Goldman JM, Hochhaus A (2011) BCR-ABL transcript dynamics support the hypothesis that leukemic stem cells are reduced during imatinib treatment. Clin Cancer Res 17:6812–6821PubMedCrossRefPubMedCentralGoogle Scholar
  90. 90.
    Strickland LA, Ross J, Williams S, Ross S, Romero M, Spencer S, Erickson R, Sutcliffe J, Verbeke C, Polakis P, van Bruggen N, Koeppen H (2009) Preclinical evaluation of carcinoembryonic cell adhesion molecule (CEACAM) 6 as potential therapy target for pancreatic adenocarcinoma. J Pathol 218(3):380–390PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Sun Q, Lesperance J, Wettersten H, Luterstein E, DeRose YS, Welm A, Desgrosellier JS (2018) Proapoptotic PUMA targets stem-like breast cancer cells to suppress metastasis. J Clin Invest 128(1):531–544PubMedCrossRefPubMedCentralGoogle Scholar
  92. 92.
    Greve B, Kelsch R, Spaniol K, Eich HT, Götte M (2012) Flow cytometry in cancer stem cell analysis and separation. Cytometry A 81(4):284–293PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    Suvà M-L, Riggi N, Stehle J-C, Baumer K, Tercier S, Joseph J-M, Stamenkovic I (2009) Identification of cancer stem cells in Ewing’s sarcoma. Cancer Res 69(5):1776–1781PubMedCrossRefPubMedCentralGoogle Scholar
  94. 94.
    Sundlisaeter E, Wang J, Sakariassen PO, Marie M, Mathisen JR, Karlsen BO, Prestegarden L, Skaftnesmo KO, Bjerkvig R, Enger PØ (2006) Primary glioma spheroids maintain tumourogenicity and essential phenotypic traits after cryopreservation. Neuropathol Appl Neurobiol 32(4):419–427PubMedCrossRefGoogle Scholar
  95. 95.
    Takaishi S, Okumura T, Tu S, Wang SSW, Shibata W, Vigneshwaran R, Wang TC (2009) Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells 27(5):1006–1020PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Terry J, Nielsen T (2010) Expression of CD133 in synovial sarcoma. Appl Immunohistochem Mol Morphol 18(2):159–165; Tirino V, Camerlingo R, Franco R, Malanga D, La Rocca A, Viglietto G, Rocco G, Pirozzi G (2009) The role of CD133 in the identification and characterisation of tumour‐initiating cells in non‐small‐cell lung cancer. Eur J Cardiothorac Surg 36(3):446–453Google Scholar
  97. 97.
    Tirino V, Desiderio V, Paino F, De Rosa A, Papaccio F, Fazioli F, Papaccio G (2011) Human primary bone sarcomas contain CD133+ cancer stem cells displaying high tumorigenicity in vivo. FASEB J 25(6):2022–2030PubMedCrossRefGoogle Scholar
  98. 98.
    Tirino V, Desiderio V, Paino F, De Rosa A, Papaccio F, La Noce M, Papaccio G (2013) Cancer stem cells in solid tumors: an overview and new approaches for their isolation and characterization. FASEB J 27(1):13–24PubMedCrossRefGoogle Scholar
  99. 99.
    Tseng H-C, Arasteh A, Paranjpe A, Teruel A, Yang W, Behel A, Jewett A (2010) Increased lysis of stem cells but not their differentiated cells by natural killer cells; de-differentiation or reprogramming activates NK cells. PLoS One 5(7):e11590PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Valent P, Bonnet D, De Maria R, Lapidot T, Copland M, Melo JV, Chomienne C, Ishikawa F, Schuringa JJ, Stassi G, Huntly B, Herrmann H, Soulier J, Roesch A, Schuurhuis GJ, Wöhrer S, Arock M, Zuber J, Cerny-Reiterer S, Johnsen HE, Andreeff M, Eaves C (2012) Cancer stem cell definitions and terminology: the devil is in the details. Nat Rev Cancer 12(11):767–775PubMedCrossRefPubMedCentralGoogle Scholar
  101. 101.
    Venkataraman G, Sasisekharan V, Herr AB, Ornitz DM, Waksman G, Cooney CL, Sasisekharan R (1996) Preferential self- association of basic fibroblast growth factor is stabilized by heparin during receptor dimerization and activation. Proc Natl Acad Sci U S A 93(2):845–850PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Walter D, Satheesha S, Albrecht P, Bornhauser BC, D’Alessandro V, Oesch SM, Rehrauer H, Leuschner I, Koscielniak E, Gengler C, Moch H, Bernasconi M, Niggli FK, Schäfer BW, CWS Study Group (2011) CD133 positive embryonal rhabdomyosarcoma stem-like cell population is enriched in rhabdospheres. PLoS One 6(5):e19506PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Wang P, Gao Q, Suo Z, Munthe E, Solberg S, Ma L, Wang M, Westerdaal NA, Kvalheim G, Gaudernack G (2013) Identification and characterization of cells with cancer stem cell properties in human primary lung cancer cell lines. PLoS One 8(3):e57020PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Weiswald L-B, Bellet D, Dangles-Marie V (2015) Spherical cancer models in tumor biology. Neoplasia 17(1):1–15PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Wen L, Chen XZ, Yang K, Chen ZX, Zhang B, Chen JP, Zhou ZG, Mo XM, Hu JK (2013) Prognostic value of cancer stem cell marker CD133 expression in gastric cancer: a systematic review. PLoS One 8(3):e59154PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Wolpert F, Roth P, Lamszus K, Tabatabai G, Weller M, Eisele G (2012) HLA-E contributes to an immune-inhibitory phenotype of glioblastoma stem-like cells. J Neuroimmunol 250(1–2):27–34PubMedCrossRefPubMedCentralGoogle Scholar
  107. 107.
    Yang ZF, Ho DW, Ng MN, Lau CK, Yu WC, Ngai P, Fan ST (2008) Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 13(2):153–166PubMedCrossRefPubMedCentralGoogle Scholar
  108. 108.
    Yang ZF, Ngai P, Ho DW, Yu WC, Ng MNP, Lau CK, Fan ST (2008) Identification of local and circulating cancer stem cells in human liver cancer. Hepatology 47(3):919–928PubMedCrossRefPubMedCentralGoogle Scholar
  109. 109.
    Yeon SE, No DY, Lee SH, Nam SW, Oh IH, Lee J, Kuh HJ (2013) Application of concave microwells to pancreatic tumor spheroids enabling anticancer drug evaluation in a clinically relevant drug resistance model. PLoS One 8(9):e73345PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Yu M, Bardia A, Aceto N, Bersani F, Madden MW, Donaldson MC, Haber DA (2014) Ex vivo culture of circulating breast tumor cells for individualized testing of drug susceptibility. Science 345(6193):216–220PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Zhang C, Li C, He F, Cai Y, Yang H (2011) Identification of CD44+ CD24+ gastric cancer stem cells. J Cancer Res Clin Oncol 137(11):1679–1686PubMedCrossRefPubMedCentralGoogle Scholar
  112. 112.
    Zhang J, Guo X, Chang DY, Rosen DG, Mercado Uribe I, Liu J (2012) CD133 expression associated with poor prognosis in ovarian cancer. Mod Pathol 25(3):456–464PubMedCrossRefPubMedCentralGoogle Scholar
  113. 113.
    Zhao JS, Li WJ, Ge D, Zhang PJ, Li JJ, Lu CL, Xie D (2011) Tumor initiating cells in esophageal squamous cell carcinomas express high levels of CD44. PLoS One 6(6):e21419PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2020

Authors and Affiliations

  • Namasivayam Nalini
    • 1
  • Bichandarkoil Jayaram Pratima
    • 1
  1. 1.Department of Biochemistry and BiotechnologyFaculty of Science Annamalai UniversityAnnamalai NagarIndia

Personalised recommendations