Kinetic analysis of intracellular Hoechst 33342-DNA interactions by flow cytometry: Misinterpretation of side population status?

Cytometry Part A

Volumn 83 A, Issue 1, 2013, Pages 161-169

  Smith, Paul J ^a   Wiltshire, Marie ^a   Chappell, Sally C ^a   Cosentino, Laura ^b   Burns, Philip A ^c   Pors, Klaus ^b   Errington, Rachel J ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF BRADFORD   (United Kingdom)

^c ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

Author keywords

ABCB1; ABCG2; ALDH1A1; Cell viability; DRAQ7; Flow cytometry; Hoechst 33342; Side population

Indexed keywords

ABC TRANSPORTER; ABCG2 PROTEIN, HUMAN; ALDEHYDE DEHYDROGENASE; BENZIMIDAZOLE DERIVATIVE; DNA; FLUORESCENT DYE; HOE 33342; TUMOR PROTEIN;

ARTICLE; CELL SURVIVAL; FLOW CYTOMETRY; HUMAN; KINETICS; LUNG ALVEOLUS CELL CARCINOMA; LUNG TUMOR; METABOLISM; METHODOLOGY; PATHOLOGY; PHENOTYPE; TUMOR CELL LINE;

ADENOCARCINOMA, BRONCHIOLO-ALVEOLAR; ALDEHYDE DEHYDROGENASE; ATP-BINDING CASSETTE TRANSPORTERS; BENZIMIDAZOLES; CELL LINE, TUMOR; CELL SURVIVAL; DNA, NEOPLASM; FLOW CYTOMETRY; FLUORESCENT DYES; HUMANS; KINETICS; LUNG NEOPLASMS; NEOPLASM PROTEINS; PHENOTYPE;

EID: 84871641353     PISSN: 15524922     EISSN: 15524930     Source Type: Journal    
DOI: 10.1002/cyto.a.22224     Document Type: Article

References (57)

1. Huang S.Non-genetic heterogeneity of cells in development: More than just noise.Development 2009;136:3853-3862.
2. Reya T, Morrison SJ, Clarke MF, Weissman IL.Stem cells, cancer, and cancer stem cells.Nature 2001;414:105-111.
3. Hart LS, El-Deiry WS.Invincible, but not invisible: Imaging approaches toward in vivo detection of cancer stem cells.J Clin Oncol 2008;26:2901-2910.
4. Pajonk F, Vlashi E, McBride WH.Radiation resistance of cancer stem cells: The 4 R's of radiobiology revisited.Stem Cells 2010;28:639-648.
5. Bunting KD.ABC transporters as phenotypic markers and functional regulators of stem cells.Stem Cells 2002;20:11-20.
6. Szakacs G, Annereau JP, Lababidi S, Shankavaram U, Arciello A, Bussey KJ, Reinhold W, Guo Y, Kruh GD, Reimers M, et al.Predicting drug sensitivity and resistance: Profiling ABC transporter genes in cancer cells.Cancer Cell 2004;6:129-137.
7. Donnenberg VS, Donnenberg AD.Multiple drug resistance in cancer revisited: The cancer stem cell hypothesis.J Clin Pharmacol 2005;45:872-877.
8. Doyle LA, Ross DD.Multidrug resistance mediated by the breast cancer resistance protein BCRP (ABCG2).Oncogene 2003;22:7340-7358.
9. Ee PL, He X, Ross DD, Beck WT.Modulation of breast cancer resistance protein (BCRP/ABCG2) gene expression using RNA interference.Mol Cancer Ther 2004;3:1577-1583.
10. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC.Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo.J Exp Med 1996;183:1797-1806.
11. Nakano A, Tsuji D, Miki H, Cui Q, El Sayed SM, Ikegame A, Oda A, Amou H, Nakamura S, Harada T, et al.Glycolysis inhibition inactivates ABC transporters to restore drug sensitivity in malignant cells.PLoS One 2011;6:e27222.
12. Goodell MA.Multipotential stem cells and 'side population' cells.Cytotherapy 2002;4:507-508.
13. Goodell MA, McKinney-Freeman S, Camargo FD.Isolation and characterization of side population cells.Methods Mol Biol 2005;290:343-352.
14. Hirschmann-Jax C, Foster AE, Wulf GG, Nuchtern JG, Jax TW, Gobel U, Goodell MA, Brenner MK.A distinct side population of cells with high drug efflux capacity in human tumor cells.Proc Natl Acad Sci USA 2004;101:14228-14233.
15. Storms RW, Goodell MA, Fisher A, Mulligan RC, Smith C.Hoechst dye efflux reveals a novel CD7(+)CD34(-) lymphoid progenitor in human umbilical cord blood.Blood 2000;96:2125-2133.
16. Storms RW, Trujillo AP, Springer JB, Shah L, Colvin OM, Ludeman SM, Smith C.Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity.Proc Natl Acad Sci USA 1999;96:9118-9123.
17. Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, Morris JJ, Lagutina I, Grosveld GC, Osawa M, Nakauchi H, 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 2001;7:1028-1034.
18. Mo W, Zhang JT.Human ABCG2: Structure, function, and its role in multidrug resistance.Int J Biochem Mol Biol 2012;3:1-27.
19. Smith PJ, Furon E, Wiltshire M, Campbell L, Feeney GP, Snyder RD, Errington RJ.ABCG2-associated resistance to Hoechst 33342 and topotecan in a murine cell model with constitutive expression of side population characteristics.Cytometry A 2009;75A:924-933.
20. Ho MM, Ng AV, Lam S, Hung JY.Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells.Cancer Res 2007;67:4827-4833.
21. Sung JM, Cho HJ, Yi H, Lee CH, Kim HS, Kim DK, Abd El-Aty AM, Kim JS, Landowski CP, Hediger MA, et al.Characterization of a stem cell population in lung cancer A549 cells.Biochem Biophys Res Commun 2008;371:163-167.
22. Blazek ER, Foutch JL, Maki G.Daoy medulloblastoma cells that express CD133 are radioresistant relative to CD133- cells, and the CD133+ sector is enlarged by hypoxia.Int J Radiat Oncol Biol Phys 2007;67:1-5.
23. Fan X, Matsui W, Khaki L, Stearns D, Chun J, Li YM, Eberhart CG.Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors.Cancer Res 2006;66:7445-7452.
24. Fukuda S, Kondo T, Takebayashi H, Taga T.Negative regulatory effect of an oligodendrocytic bHLH factor OLIG2 on the astrocytic differentiation pathway.Cell Death Differ 2004;11:196-202.
25. 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.
26. Setoguchi T, Taga T, Kondo T.Cancer stem cells persist in many cancer cell lines.Cell Cycle 2004;3:414-415.
27. Engelmann K, Shen H, Finn OJ.MCF7 side population cells with characteristics of cancer stem/progenitor cells express the tumor antigen MUC1.Cancer Res 2008;68:2419-2426.
28. Orina JN, Calcagno AM, Wu CP, Varma S, Shih J, Lin M, Eichler G, Weinstein JN, Pommier Y, Ambudkar SV, et al.Evaluation of current methods used to analyze the expression profiles of ATP-binding cassette transporters yields an improved drug-discovery database.Mol Cancer Ther 2009;8:2057-2066.
29. Lebedeva IV, Pande P, Patton WF.Sensitive and specific fluorescent probes for functional analysis of the three major types of mammalian ABC transporters.PLoS One 2012;6:e22429.
30. Donnenberg VS, Meyer EM, Donnenberg AD.Measurement of multiple drug resistance transporter activity in putative cancer stem/progenitor cells.Methods Mol Biol 2009;568:261-279.
31. Greve B, Kelsch R, Spaniol K, Eich HT, Gotte M.Flow cytometry in cancer stem cell analysis and separation.Cytometry A 2012;81A:284-293.
32. Golebiewska A, Brons NH, Bjerkvig R, Niclou SP.Critical appraisal of the side population assay in stem cell and cancer stem cell research.Cell Stem Cell 2011;8:136-147.
33. Smith PJ, Nakeff A, Watson JV.Flow-cytometric detection of changes in the fluorescence emission spectrum of a vital DNA-specific dye in human tumour cells.Exp Cell Res 1985;159:37-46.
34. Watson JV, Nakeff A, Chambers SH, Smith PJ.Flow cytometric fluorescence emission spectrum analysis of Hoechst-33342-stained DNA in chicken thymocytes.Cytometry 1985;6:310-315.
35. Petersen TW, Ibrahim SF, Diercks AH, van den Engh G.Chromatic shifts in the fluorescence emitted by murine thymocytes stained with Hoechst 33342.Cytometry A 2004;60A:173-181.
36. Edward R.Red/far-red fluorescing DNA-specific anthraquinones for nucl:cyto segmentation and viability reporting in cell-based assays.Methods Enzymol 2012;505:23-45.
37. Deeken JF, Robey RW, Shukla S, Steadman K, Chakraborty AR, Poonkuzhali B, Schuetz EG, Holbeck S, Ambudkar SV, Bates SE.Identification of compounds that correlate with ABCG2 transporter function in the National Cancer Institute Anticancer Drug Screen.Mol Pharmacol 2009;76:946-956.
38. Robey RW, Polgar O, Deeken J, To KW, Bates SE.ABCG2: Determining its relevance in clinical drug resistance.Cancer Metastasis Rev 2007;26:39-57.
39. Ross DD, Doyle LA.Mining our ABCs: Pharmacogenomic approach for evaluating transporter function in cancer drug resistance.Cancer Cell 2004;6:105-107.
40. Rabindran SK, Ross DD, Doyle LA, Yang W, Greenberger LM.Fumitremorgin C reverses multidrug resistance in cells transfected with the breast cancer resistance protein.Cancer Res 2000;60:47-50.
41. Nakanishi T, Doyle LA, Hassel B, Wei Y, Bauer KS, Wu S, Pumplin DW, Fang HB, Ross DD.Functional characterization of human breast cancer resistance protein (BCRP, ABCG2) expressed in the oocytes of Xenopus laevis.Mol Pharmacol 2003;64:1452-1462.
42. Moreb JS, Zucali JR, Ostmark B, Benson NA.Heterogeneity of aldehyde dehydrogenase expression in lung cancer cell lines is revealed by Aldefluor flow cytometry-based assay.Cytometry B Clin Cytom 2007;72B:281-289.
43. Pesta D, Gnaiger E.High-resolution respirometry: OXPHOS protocols for human cells and permeabilized fibers from small biopsies of human muscle.Methods Mol Biol 2012;810:25-58.
44. Lieber M, Smith B, Szakal A, Nelson-Rees W, Todaro G.A continuous tumor-cell line from a human lung carcinoma with properties of type II alveolar epithelial cells.Int J Cancer 1976;17:62-70.
45. Livak K, Schmittgen, T.Analysis of relative gene expression data using real-time quantitative PCR and the 22DDCT method.Methods 2001;25:402-408.
46. Mo SL, Li J, Loh YS, Brown RD, Smith AL, Chen Y, Joshua D, Roufogalis BD, Li GQ, Fan K, et al.Factors influencing the abundance of the side population in a human myeloma cell line.Bone Marrow Res 2011;2011:524845.
47. Visvader JE, Lindeman GJ.Cancer stem cells in solid tumours: Accumulating evidence and unresolved questions.Nat Rev Cancer 2008;8:755-768.
48. Douville J, Beaulieu R, Balicki D.ALDH1 as a functional marker of cancer stem and progenitor cells.Stem Cells Dev 2009;18:17-25.
49. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S, 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.
50. Patrawala L, Calhoun T, Schneider-Broussard R, Zhou J, Claypool K, Tang DG.Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2- cancer cells are similarly tumorigenic.Cancer Res 2005;65:6207-6219.
51. Robey RW, To KK, Polgar O, Dohse M, Fetsch P, Dean M, Bates SE.ABCG2: A perspective.Adv Drug Deliv Rev 2009;61:3-13.
52. Tassi E, Zanon M, Vegetti C, Molla A, Bersani I, Perotti V, Pennati M, Zaffaroni N, Milella M, Ferrone S, et al.Role of apollon in human melanoma resistance to antitumor agents that activate the intrinsic or the extrinsic apoptosis pathways.Clin Cancer Res 2012;18:3316-3327.
53. Vossenkamper A, Marches O, Fairclough PD, Warnes G, Stagg AJ, Lindsay JO, Evans PC, Luong le A, Croft NM, Naik S, et al.Inhibition of NF-kappaB signaling in human dendritic cells by the enteropathogenic Escherichia coli effector protein NleE.J Immunol 2010;185:4118-4127.
54. Smith PJ, Lacy M, Debenham PG, Watson JV.A mammalian cell mutant with enhanced capacity to dissociate a bis-benzimidazole dye-DNA complex.Carcinogenesis 1988;9:485-490.
55. Ellwart JW, Dormer P.Vitality measurement using spectrum shift in Hoechst 33342 stained cells.Cytometry 1990;11:239-243.
56. Ibrahim SF, Diercks AH, Petersen TW, van den Engh G.Kinetic analyses as a critical parameter in defining the side population (SP) phenotype.Exp Cell Res 2007;313:1921-1926.
57. Smith PJ, Morgan SA, Watson JV.Detection of multidrug resistance and quantification of responses of human tumour cells to cytotoxic agents using flow cytometric spectral shift analysis of Hoechst 33342-DNA fluorescence.Cancer Chemother Pharmacol 1991;27:445-450.