Cell sorting in cancer research-Diminishing degree of cell heterogeneity

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1836, Issue 1, 2013, Pages 105-122

  Barteneva, Natasha S ^a,b   Ketman, Kenneth ^a   Fasler Kan, Elizaveta ^c   Potashnikova, Daria ^d   Vorobjev, Ivan A ^d  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF APPLIED SCIENCES AND ARTS NORTHWESTERN SWITZERLAND   (Switzerland)

^d MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Cancer; Cancer heterogeneity; Cell heterogeneity; Flow cytometry; High speed cell sorting; Microarray

Indexed keywords

GRANULOCYTE COLONY STIMULATING FACTOR;

APOPTOSIS; CANCER GRADING; CANCER RESEARCH; CELL HETEROGENEITY; CELL LINEAGE; CELL MEMBRANE PERMEABILITY; CELL POPULATION; CELL SELECTION; CELL VIABILITY; CLONOGENESIS; DNA DEGRADATION; EARLY DIAGNOSIS; FLOW CYTOMETRY; GENE AMPLIFICATION; GENE EXPRESSION PROFILING; HUMAN; LASER CAPTURE MICRODISSECTION; MICROCHIP ANALYSIS; MICROFLUIDICS; MORPHOLOGY; MUTATIONAL ANALYSIS; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; REVIEW; RNA DEGRADATION; SHORT TANDEM REPEAT; SINGLE NUCLEOTIDE POLYMORPHISM; TUMOR MICROENVIRONMENT;

ANIMALS; BIOMEDICAL RESEARCH; CELL SEPARATION; FLOW CYTOMETRY; GENETIC HETEROGENEITY; HUMANS; MICROARRAY ANALYSIS; NEOPLASMS; TUMOR MARKERS, BIOLOGICAL;

EID: 84877828458     PISSN: 0304419X     EISSN: 18792561     Source Type: Journal    
DOI: 10.1016/j.bbcan.2013.02.004     Document Type: Review

References (266)

1. Almendro V., Marusyk A., Polyak K. Cellular heterogeneity and molecular evolution of cancer. Annu. Rev. Pathol. 2013, 8:277-302.
2. Swanton C. Intratumor heterogeneity: evolution through space and time. Cancer Res. 2012, 72:4875-4882.
3. Gerlinger M., Rowan A.J., Horswell S., Larkin J., Endesfelder D., Gronroos E., Martinez P., Matthews N., Stewart A., Tarpey P., Varela I., Phillimore B., Begum S., McDonald N.Q., Butler A., Jones D., Raine K., Latimer C., Santos C.R., Nohadani M., Eklund A.C., Spencer-Dene B., Clark G., Pickering L., Stamp G., Gore M., Szallasi Z., Downward J., Futreal P.A., Swanton C. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 2012, 366:883-892.
4. Hirsch F.R., Ottesen G., Poedenphant J., Olsen J. Tumor heterogeneity in lung cancer based on light microscopic features. A retrospective study of a consecutive series of 200 patients, treated surgically. Virchows Arch. A Pathol. Anat. Histopathol. 1983, 402:147-153.
5. Mora J., Cheung N.K., Gerald W.L. Genetic heterogeneity and clonal evolution in neuroblastoma. Br. J. Cancer 2001, 85:182-189.
6. Baisse B., Bouzourene H., Saraga E.P., Bosman F.T., Benhattar J. Intratumor genetic heterogeneity in advanced human colorectal adenocarcinoma. Int. J. Cancer 2001, 93:346-352.
7. Heng H.H., Bremer S.W., Stevens J.B., Ye K.J., Liu G., Ye C.J. Genetic and epigenetic heterogeneity in cancer: a genome-centric perspective. J. Cell. Physiol. 2009, 220:538-547.
8. Yachida S., Jones S., Bozic I., Antal T., Leary R., Fu B., Kamiyama M., Hruban R.H., Eshleman J.R., Nowak M.A., Velculescu V.E., Kinzler K.W., Vogelstein B., Iacobuzio-Donahue C.A. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 2010, 467:1114-1117.
9. Hicks J., Krasnitz A., Lakshmi B., Navin N.E., Riggs M., Leibu E., Esposito D., Alexander J., Troge J., Grubor V., Yoon S., Wigler M., Ye K., Boerresen-Dale A.L., Naume B., Schlicting E., Norton L., Haegerstroem T., Skoog L., Auer G., Maener S., Lundin P., Zetterberg A. Novel patterns of genome rearrangement and their association with survival in breast cancer. Genome Res. 2006, 16:1465-1479.
10. Chin S.F., Teschendorff A.E., Marioni J.C., Wang Y., Barbosa-Morais N.L., Thorne N.P., Costa J.L., Pinder S.E., van de Wiel M.A., Green A.R., Ellis I.O., Porter P.L., Tavare S., Brenton J.D., Ylstra B., Caldas C. High-resolution aCGH and expression profiling identifies a novel genomic subtype of ER negative breast cancer. Genome Biol. 2007, 8:R215.
11. Palani S., Sarkar C.A. Transient noise amplification and gene expression synchronization in a bistable mammalian cell-fate switch. Cell Rep. 2012, 1:215-224.
12. Saunders N.A., Simpson F., Thompson E.W., Hill M.M., Endo-Munoz L., Leggatt G., Minchin R.F., Guminski A. Role of intratumoural heterogeneity in cancer drug resistance: molecular and clinical perspectives. EMBO Mol. Med. 2012, 4:675-684.
13. Cottu P.H., Asselah J., Lae M., Pierga J.Y., Dieras V., Mignot L., Sigal-Zafrani B., Vincent-Salomon A. Intratumoral heterogeneity of HER2/neu expression and its consequences for the management of advanced breast cancer. Ann. Oncol. 2008, 19:595-597.
14. Vance G.H., Barry T.S., Bloom K.J., Fitzgibbons P.L., Hicks D.G., Jenkins R.B., Persons D.L., Tubbs R.R., Hammond M.E. Genetic heterogeneity in HER2 testing in breast cancer: panel summary and guidelines. Arch. Pathol. Lab. Med. 2009, 133:611-612.
15. Herzenberg L.A., Parks D., Sahaf B., Perez O., Roederer M., Herzenberg L.A. The history and future of the fluorescence activated cell sorter and flow cytometry: a view from Stanford. Clin. Chem. 2002, 48:1819-1827.
16. Gyllensten U.B. PCR and DNA sequencing. Biotechniques 1989, 7:700-708.
17. Rooney P.H. Multiplex quantitative real-time PCR of laser microdissected tissue. Methods Mol. Biol. 2005, 293:27-37.
18. De Spiegelaere W., Erkens T., De Craene J., Burvenich C., Peelman L., Van den Broeck W. Elimination of amplification artifacts in real-time reverse transcripton PCR using laser capture microdissected samples. Anal. Biochem. 2008, 382:72-74.
19. Liu E.T. Stromal effects in breast cancer. N. Engl. J. Med. 2007, 357:2537-2538.
20. Michel C., Desdouets C., Sacre-Salem B., Gautier J.C., Roberts R., Botier E. Liver gene expression profiles of rats treated with clofibric acid: comparison of whole liver and laser capture microdissected liver. Am. J. Pathol. 2003, 163:2191-2199.
21. Khoudoleeva O., Gretsov E., Barteneva N., Vorobjev I. Proliferative index and expression of CD38, Zap-70 and CD25 in different lymphoid compartments of chronic lymphocytic leukemia patients. Pathol. Lab. Med. 2011, 3:7-16.
22. hi prostate cancer-associated fibroblasts. Prostate 2009, 69:991-1000.
23. Silva A.K., Yi H., Hayes S.H., Seigel G.M., Hackam A.S. Lithium chloride regulates the proliferation of stem-like cells in retinoblastoma cell lines: a potential role for the canonical Wnt signaling pathway. Mol. Vis. 2010, 16:36-45.
24. Wang B., Yang H., Huang Y.Z., Yan R.H., Liu F.J., Zhang J.N. Biologic characteristics of the side population of human small cell lung cancer cell line H446. Chin. J. Cancer 2010, 29:254-260.
25. Primo D., Flores J., Quijano S., Sanchez M.L., Sarasquete M.E., del Pino-Montes J., Gaarder P.I., Gonzalez M., Orfao A. Impact of BCR/ABL gene expression on the proliferative rate of different subpopulations of haematopoietic cells in chronic myeloid leukaemia. Br. J. Haematol. 2006, 135:43-51.
26. Hess C.J., Denkers F., Ossenkoppele G.J., Waisfisz Q., McElgunn C.J., Eldering E., Schouten J.P., Schuurhuis G.J. Gene expression profiling of minimal residual disease in acute myeloid leukaemia by novel multiplex-PCR-based method. Leukemia 2004, 18:1981-1988.
27. Hoefig K.P., Heissmeyer V. Measuring microRNA expression in size-limited FACS-sorted and microdissected samples. Methods Mol. Biol. 2010, 667:47-63.
28. Edvardsson L., Olofsson T. Real-time PCR analysis for blood cell lineage specific markers. Methods Mol. Biol. 2009, 496:313-322.
29. Zhang H., Li W., Nan F., Ren F., Wang H., Xu Y., Zhang F. MicroRNA expression profile of colon cancer stem-like cells in HT29 adenocarcinoma cell line. Biochem. Biophys. Res. Commun. 2011, 404:273-278.
30. Lamb L.S., Robbins N.F., Abhyankar S., Joyce M., Stetler-Stevenson M., Henslee-Downey P.J., Gee A.P. Flow cytometric cell sorting combined with molecular chimerism analysis to detect minimal recurrent leukemia: good news and bad news. Bone Marrow Transplant. 1997, 19:1157-1161.
31. Bertram S., Hufert F.T., Neumann-Haefelin D., von Laer D. Detection of DNA in single cells using an automated cell deposition unit and PCR. Biotechniques 1995, 19:616-620.
32. Gaynor E.M., Mirsky M.L., Lewin H.A. Use of flow cytometry and RT-PCR for detecting gene expression by single cells. Biotechniques 1996, 21:286-291.
33. Smith M.J., Culhane A.C., Donovan M., Coffey J.C., Barry B.D., Kelly M.A., Higgins D.G., Wang J.H., Kirwan W.O., Cotter T.G., Redmond H.P. Analysis of differential gene expression in colorectal cancer and stroma using fluorescence-activated cell sorting purification. Br. J. Cancer 2009, 100:1452-1464.
34. Hayashi T., Shibata N., Okumura R., Kudome T., Nishimura O., Tarui H., Agata K. Single-cell profiling of planarian stem cells using fluorescent activated cell sorting and its "index sorting" function for stem cell research. Dev. Growth Differ. 2010, 52:131-144.
35. Navin N., Hicks J. Future medical applications of single-cell sequencing in cancer. Genome Med. 2011, 3:31.
36. Nardone A., Corvigno S., Brescia A., D'Andrea D., Limite G., Veneziani B.M. Long-term cultures of stem/progenitor cells from lobular and ductal breast carcinomas under non-adherent conditions. Cytotechnology 2011, 63:67-80.
37. Birkenkamp-Demtroder K., Christensen L.L., Olesen S.H., Frederiksen C.M., Laiho P., Aaltonen L.A., Laurberg S., Sorensen F.B., Hagemann R., Orntoft T.F. Gene expression in colorectal cancer. Cancer Res. 2002, 62:4352-4363.
38. Ramaswamy S., Ross K.N., Lander E.S., Golub T.R. A molecular signature of metastasis in primary solid tumors. Nat. Genet. 2003, 33:49-54.
39. Hofmann W.K., de Vos S., Elashoff D., Gschaidmeier H., Hoelzer D., Koeffler H.P., Ottmann O.G. Relation between resistance of Philadelphia-chromosome-positive acute lymphoblastic leukaemia to the tyrosine-kinase inhibitor STI571 and gene-expression profiles: a gene-expression study. Lancet 2002, 359:481-486.
40. Marton M.J., DeRisi J.L., Bennett H.A., Iyer V.R., Meyer M.R., Roberts C.J., Stoughton R., Burchard J., Slade D., Dai H., Bassett D.E., Hartwell L.H., Brown P.O., Friend S.H. Drug target validation and identification of secondary drug target effects using DNA microarrays. Nat. Med. 1998, 4:1293-1301.
41. Huang E., Cheng S.H., Dressman H., Pittman J., Tsou M.H., Horng C.F., Bild A., Iversen E.S., Liao M., Chen C.M., West M., Nevins J.R., Huang A.T. Gene expression predictors of breast cancer outcomes. Lancet 2003, 361:1590-1596.
42. Iizuka N., Oka M., Yamada-Okabe H., Nishida M., Maeda Y., Mori N., Takao T., Tamesa T., Tangoku A., Tabuchi H., Hamada K., Nakayama H., Ishitsuka H., Miyamoto T., Hirabayashi A., Uchimura S., Hamamoto Y. Oligonucleotide microarray for prediction of early intrahepatic recurrence of hepatocellular carcinoma after curative resection. Lancet 2003, 361:923-929.
43. Navin N., Kendall J., Troge J., Andrews P., Rodgers L., McIndoo J., Cook K., Stepansky A., Levy D., Esposito D., Muthuswamy L., Krasnitz A., McCombie W.R., Hicks J., Wigler M. Tumor evolution inferred by single-cell sequencing. Nature 2011, 472:90-94.
44. Sugiyama Y., Sugiyama K., Hirai Y., Akiyama F., Hasumi K. Microdissection is essential for gene expression profiling of clinically resected cancer tissues. Am. J. Clin. Pathol. 2002, 117:109-116.
45. Kwong K.Y., Bloom G.C., Yang I., Boulware D., Coppola D., Haseman J., Chen E., McGrath A., Makusky A.J., Taylor J., Steiner S., Zhou J., Yeatman T.J., Quackenbush J. Synchronous global assessment of gene and protein expression in colorectal cancer progression. Genomics 2005, 86:142-158.
46. Sun J.G., Liao R.X., Qiu J., Jin J.Y., Wang X.X., Duan Y.Z., Chen F.L., Hao P., Xie Q.C., Wang Z.X., Li D.Z., Chen Z.T., Zhang S.X. Microarray-based analysis of microRNA expression in breast cancer stem cells. J. Exp. Clin. Cancer Res. 2010, 29:174.
47. Andreasson U., Eden P., Peterson C., Hoegekorp C.M., Jerkeman M., Andersen N., Berglund M., Sundstroem C., Rosenquist R., Borrebaeck C.A., Ek S. Identification of uniquely expressed transcription factors in highly purified B-cell lymphoma samples. Am. J. Hematol. 2010, 85:418-425.
48. Tighe S., Held M.A. Isolation of total RNA from transgenic mouse melanoma subsets using fluorescence-activated cell sorting. Methods Mol. Biol. 2010, 632:27-44.
49. Diez C., Bertsch G., Simm A. Isolation of full-size mRNA from cells sorted by flow cytometry. J. Biochem. Biophys. Methods 1999, 40:69-80.
50. Barrett M.T., Glogovac J., Prevo L.J., Reid B.J., Porter P., Rabinovitch P.S. High-quality RNA and DNA from flow cytometrically sorted human epithelial cells and tissues. Biotechniques 2002, 32:888-896.
51. Zaitoun I., Erickson C.S., Schell K., Epstein M.L. Use of RNAlater in fluorescence-activated cell sorting (FACS) reduces the fluorescence from GFP but not from DsRed. BMC Res. Notes 2010, 3:328.
52. + prostate tumor-associated stromal cells involves potential organ-specific genes. BMC Cancer 2009, 9:317.
53. Leers M.P., Schutte B., Theunissen P.H., Ramaekers F.C., Nap M. Heat pretreatment increases resolution in DNA flow cytometry of paraffin-embedded tumor tissue. Cytometry 1999, 35:260-266.
54. Corver W.E., ter Haar N.T. High-resolution multiparameter DNA flow cytometry for the detection and sorting of tumor and stromal subpopulations from paraffin-embedded tissues. Curr. Protoc. Cytom. 2011, 1. (Suppl. 55, Chapter 6:Unit 6.27, 1-6.27.16).
55. Huang W.Y., Sheehy T.M., Moore L.E., Hsing A.W., Purdue M.P. Simultaneous recovery of DNA and RNA from formalin-fixed paraffin-embedded tissue and application in epidemiologic studies. Cancer Epidemiol. Biomarkers Rev. 2010, 19:973-977.
56. Rupp G.M., Locker J. Purification and analysis of RNA from paraffin-embedded tissues. Biotechniques 1988, 6:56-60.
57. Stanta G., Schneider C. RNA extracted from paraffin-embedded human tissues is amenable to analysis by PCR amplification. Biotechniques 1991, 11:304-308.
58. Lee J., Hever A., Willhite D., Zlotnik A., Hevezi P. Effects of RNA degradation on gene expression analysis of human postmortem tissues. FASEB J. 2005, 19:1356-1358.
59. Baloglu G., Haholu A., Kucukodaci Z., Yilmaz I., Yildirim S., Baloglu H. The effects of tissue fixation alternatives on DNA content: a study of normal colon tissue. Appl. Immunohistochem. Mol. Morphol. 2008, 16:485-492.
60. Hedley D.W., Friedlander M.L., Taylor I.W. Application of DNA flow cytometry to paraffin-embedded archival material for the study of aneuploidy and its clinical significance. Cytometry 1985, 6:327-333.
61. Cunningham R.E. Deparaffinization and processing of pathological material. Methods Mol. Biol. 2010, 588:345-349.
62. Schultz D.S., Zarbo R.J. Comparison of eight modifications of Hedley's method for flow cytometric DNA ploidy analysis of paraffin-embedded tissue. Am. J. Clin. Pathol. 1992, 98:291-295.
63. Cattoretti G., Pileri S., Parravicini C., Becker M.H., Poggi S., Bifulco C., Key G., D'Amato L., Sabatini E., Feudale E., et al. Antigen unmasking on formalin-fixed, paraffin embedded tissue sections. J. Pathol. 1993, 171:83-98.
64. Shi S.R., Key M.F., Kalra K.I. Antigen retrieval in formalin fixed, paraffin embedded tissues: an enhancement method for immunohistochemical staining based on microwave oven heating of tissue sections. J. Histochem. Cytochem. 1991, 39:741-748.
65. Morgan J.M., Navabi H., Schmid K.W., Jasani B. Possible role of tissue-bound calcium ions in citrate-mediated high-temperature antigen retrieval. J. Pathol. 1994, 174:301-307.
66. Schutte B., Reynders M.M., Bosman F.T., Blijham G.H. Flow cytometric determination of DNA ploidy level in nuclei isolated from paraffin-embedded tissue. Cytometry 1985, 6:26-30.
67. Arber D.A., Cook P.D., Moser L.K., Speights V.O. Variation in reference cells for DNA analysis of paraffin-embedded tissue. Am. J. Clin. Pathol. 1992, 97:387-392.
68. Esser C., Goettlinger C., Kremer J., Hundeiker J.C., Radbruch A. Isolation of full-size mRNA from ethanol fixed cells after cellular immunofluorescence staining and fluorescence-activated cell sorting. Cytometry 1995, 21:382-386.
69. Yamada H., Maruo R., Watanabe M., Hidaka Y., Iwatani Y., Takano T. Messenger RNA quantification after fluorescence-activated cell sorting using in situ hybridization. Cytometry 2010, 77:1032-1037.
70. Foss R.D., Guha-Thakurta N., Conran R.M., Gutman P. Effects of fixative and fixation time on the extraction and polymerase chain reaction amplification of RNA from paraffin-embedded tissue: comparison of two housekeeping gene mRNA controls. Diagn. Mol. Pathol. 1994, 3:148-155.
71. Srinivasan M., Sedmak D., Jewell S. Effect of fixatives and tissue processing on the content and integrity of nucleic acids. Am. J. Pathol. 2002, 161:1961-1971.
72. von Smolinski D., Leverkoehne I., von Samson-Himmelstjerna G., Gruber A.D. Impact of formalin-fixation and paraffin-embedding on the ratio between mRNA copy numbers of differently expressed genes. Histochem. Cell Biol. 2005, 124:177-188.
73. Koch I., Slotta-Huspenina J., Hollweck R., Anastasov N., Hofler H., Quintanilla-Martinez L., Fend F. Real-time quantitative RT-PCR shows variable, assay-dependent sensitivity to formalin fixation: implications for direct comparison of transcript levels in paraffin-embedded tissues. Diagn. Mol. Pathol. 2006, 15:149-156.
74. Jordanova E.S., Corver W.E., Vonk M.J., Leers M.P., Riemersma S.A., Schuuring E., Kluin P.M. Flow cytometric sorting of paraffin-embedded tumor tissues considerably improves molecular genetic analysis. Am. J. Clin. Pathol. 2003, 120:327-334.
75. Mehta A.M., Jordanova E.S., Corver W.E., van Wezel T., Uh H.W., Kenter G.G., Fleuren G.J. Single nucleotide polymorphisms in antigen processing machinery component ERAP I significantly associate with clinical outcome in cervical carcinoma. Genes Chromosomes Cancer 2009, 48:410-418.
76. Corver W.E., Middeldorp A., ter Haar N.T., Jordanova E.S., van Puijenbroek M., van Eijk R., Cornelisse C.J., Fleuren G.J., Morreau H., Oosting J., van Wezel T. Genome-wide allelic state analysis on flow-sorted tumor fractions provides an accurate measure of chromosomal aberrations. Cancer Res. 2008, 68:10333-10340.
77. Middeldorp A., van Puijenbroek M., Nielsen M., Corver W.E., Jordanova E.S., ter Haar N., Tops C.M., Vasen H.F., Lips E.H., van Eijk R., Hes F.J., Oosting J., Wijnen J., van Wezel T., Morreau H. High frequency of copy-neutral LOH in MUTYH-associated polyposis carcinomas. J. Pathol. 2008, 216:25-31.
78. Kloth J.N., Gorter A., ter Haar N., Corver W.E., Jordanova E.S., Kenter G.G., Fleuren G.J. Lack of TNFalpha mRNA expression in cervical cancer is not associated with loss of heterozygocity at 6p21.3, inactivating mutations or promoter methylation. Mol. Immunol. 2008, 45:152-159.
79. Boyd Z.S., Raja R., Johnson S., Eberhard D.A., Lackner M.R. A tumor sorting protocol that enables enrichment of pancreatic adenocarcinoma cells and facilitation of genetic analyses. J. Mol. Diagn. 2009, 11:290-297.
80. Schubert E.L., Hsu L., Cousens L.A., Glogovac J., Self S., Reid B.J., Rabinovitch P.S., Porter P.L. Single nucleotide polymorphism array analysis of flow-sorted epithelial cells from frozen versus fixed tissues for whole genome analysis of allelic loss in breast cancer. Am. J. Pathol. 2002, 160:73-79.
81. Sotiriou C., Piccart M.J. Taking gene-expression profiling to the clinic: when will molecular signatures become relevant to patient care?. Nat. Rev. Cancer 2007, 7:545-553.
82. Perlmutter M.A., Best C.J., Gillespie J.W., Gathright Y., Gonzalez S., Velasco A., Linehan W.M., Emmert-Buck M.R., Chuaqui R.F. Comparison of snap freezing versus ethanol fixation for gene expression profiling of tissue specimens. J. Mol. Diagn. 2004, 6:371-377.
83. Wang S.S., Sherman M.E., Rader J.S., Carreon J., Schiffman M., Baker C.C. Cervical tissue collection methods for RNA preservation: comparison of snap-frozen, ethanol-fixed, and RNAlater fixation. Diagn. Mol. Pathol. 2006, 15:144-148.
84. Grotzer M.A., Patti R., Geoerger B., Eggert A., Chou T.T., Phillips P.C. Biological stability of RNA isolated from RNAlater-treated brain tumor and neuroblastoma xenografts. Med. Pediatr. Oncol. 2000, 34:438-442.
85. Mutter G.L., Zahrieh D., Liu C., Neuberg D., Finkelstein D., Baker H.E., Warrington J.A. Comparison of frozen and RNAlater solid tissue storage methods for use in RNA expression microarrays. BMC Genomics 2004, 5:88.
86. Chung J.Y., Braunschweig T., Hewitt S.M. Optimization of recovery of RNA from formalin-fixed, paraffin-embedded tissue. Diagn. Mol. Pathol. 2006, 15:229-236.
87. Hong S.H., Baek H.A., Jang K.Y., Chung M.J., Moon W.S., Kang M.J., Lee D.G., Park H.S. Effects of delay in the snap freezing of colorectal cancer tissues on the quality of DNA and RNA. J. Korean Soc. Coloproctol. 2010, 26:316-323.
88. Almeida A., Paul Thiery J., Magdelenat H., Radvanyi F. Gene expression analysis by real-time reverse transcription polymerase chain reaction: influence of tissue handling. Anal. Biochem. 2004, 328:101-108.
89. Mager S.R., Oomen M.H., Morente M.M., Ratcliffe C., Knox K., Kerr D.J., Pezzella F., Riegman P.H. Standard operating procedure for the collection of fresh frozen tissue samples. Eur. J. Cancer 2007, 43:828-834.
90. Little S.E., Vuononvirta R., Reis-Filho J.S., Natrajan R., Iravani M., Fenwick K., Mackay A., Ashworth A., Pritchard-Jones K., Jones C. Array CGH using whole genome amplification of fresh-frozen and formalin-fixed, paraffin-embedded tumor DNA. Genomics 2006, 87:298-306.
91. Killian J.K., Bilke S., Davis S., Walker R.L., Kilian M.S., Jaeger E.B., Chen Y., Hipp J., Pittaluga S., Raffeld M., Cornelison R., Smith W.I., Bibikova M., Fan J.B., Emmert-Buck M.R., Jaffe E.S., Meltzer P.S. Large-scale profiling of archival lymph nodes reveals pervasive remodeling of the follicular lymphoma methylome. Cancer Res. 2009, 69:758-764.
92. Dietmaier W., Hartmannh A., Wallinger S., Heinmoeller E., Kerner T., Endl E., Juch K.-W., Hofstaedter F., Rueschoff J. Multiple mutation analyses in single tumor cells with improved whole genome amplification. Am. J. Pathol. 1999, 154:83-95.
93. Clevers H. The cancer stem cell: premises, promises and challenges. Nat. Med. 2011, 17:313-319.
94. Clarke M.F., Dick J.E., Dirks P.B., Eaves C.J., Jamieson C.H., Jones D.L., Visvader J., Weissman I.L., Wahl G.M. Cancer stem cells-perspectives on current status and future directions: AACR workshop on cancer stem cells. Cancer Res. 2006, 66:9339-9344.
95. Hermann P.C., Bhaskar S., Cioffi M., Heeschen C. Cancer stem cells in solid tumors. Semin. Cancer Biol. 2010, 20:77-84.
96. Liu S.V., Lenkiewicz E., Evers L., Holley T., Kiefer J., Ruiz C., Glatz K., Bubendorf L., Demeure M.J., Eng C., Ramanathan R.K., Hoff D.D., Barrett M.T. Genomic analysis and selected molecular pathways in rare cancers. Phys. Biol. 2012, 9:065004.
97. - breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Res. 2006, 8:R59.
98. Dalerba P., Kalisky T., Sahoo D., Rajendran P.S., Rothenberg M.E., Leyrat A.A., Sim S., Okamoto J., Johnston D.M., Qian D., Zabala M., Bueno J., Neff N.F., Wang J., Shelton A.A., Visser B., Hisamori S., Shimono Y., van de Wetering M., Clevers H., Clarke M.F., Quake S.R. Single-cell dissection of transcriptional heterogeneity in human colon tumors. Nat. Biotechnol. 2011, 29:1120-1127.
99. + ovarian cancer cells. Oncogene 2009, 28:209-218.
100. Joo K.M., Nam D.H. Prospective identification of cancer stem cells with the surface antigen CD133. Methods Mol. Biol. 2009, 568:57-71.
101. Meyer M.J., Fleming J.M., Ali M.A., Pesesky M.W., Ginsburg E., Vonderhaar B.K. Dynamic regulation of CD24 and the invasive, CD44posCD24neg phenotype in breast cancer cell lines. Breast Cancer Res. 2009, 11:R82.
102. Lapidot T., Sirard C., Vormoor J., Murdoch B., Hoang T., Caceres-Cortes J., Minden M., Paterson B., Caligiuri M.A., Dick J.E. A cell initiating human acute myeloid leukemia after transplantation into SCID mice. Nature 1994, 367:645-648.
103. Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 1997, 3:730-737.
104. Donnenberg V.S., Landrenau R.J., Donnenberg A.D. Tumorogenic stem and progenitor cells: implications for the therapeutic index of anti-cancer agents. J. Control Release 2007, 122:385-391.
105. Zhang M., Behbod F., Atkinson R.L., Landis M.D., Kittrell F., Edwards D., Medina D., Tsimelzon A., Hilsenbeck S., Green J.E., Michalowska A.M., Rosen J.M. Identification of tumor-initiating cells in a p53-null mouse model of breast cancer. Cancer Res. 2008, 68:4674-4682.
106. Yang Z.F., Ngai P., Ho D.W., Yu W.C., Ng M.N., Lau C.K., Li M.L., Tam K.H., Lam C.T., Poon R.T., Fan S.T. Identification of local and circulating cancer stem cells in human liver cancer. Hepatology 2008, 47:919-928.
107. Goodell M.A., Brose K., Paradis G., Conner A.S., Mulligan R.C. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J. Exp. Med. 1996, 183:1797-1806.
108. Liu W.-H., Qian N.-S., Li R., Dou K.-F. Replacing Hoechst33342 with Rhodamine 123 in isolation of cancer stem-like cells from the MHCC97 cell line. Toxicol. Vitr. 2010, 24:538-545.
109. Telford W.G. Stem cell side population analysis and sorting using DyeCycle violet. Curr. Protoc. Cytom. 2010, 1. (Suppl. 51, Chapter 9: Unit 9:30.1-9.30.9).
110. Bunting K.D. ABC transporters as phenotypic markers and functional regulators of stem cells. Stem Cells 2002, 20:11-20.
111. Wu C., Wei Q., Utomo V., Nadesan P., Whetstone H., Kandel R., Wunder J.S., Altman B.A. Side population cells isolated from mesenchymal neoplasms have tumor initiating potential. Cancer Res. 2007, 67:8216-8222.
112. Santamaria-Martinez A., Barquinero J., Barbosa-Desongles A., Hurtado A., Pinos T., Seoane J., Poupon M.F., Morote J., Reventos J., Munell F. Identification of multipotent mesenchymal stromal cells in the reactive stroma of a prostate cancer xenograft by side population analysis. Exp. Cell Res. 2009, 315:3004-3013.
113. Boesch M., Reimer D., Rumpold H., Zeimet A.G., Sopper S., Wolf D. DyeCycle Violet used for side population detection is a substrate of P-glycoprotein. Cytometry A 2012, 81:517-522.
114. Litman T., Brangi M., Hudson E., Fetsch P., Abati A., Ross D.D., Miyake K., Resau J.H., Bates S.E. The multidrug-resistant phenotype associated with overexpression of the new ABC half-transporter, MXR (ABCG2). J. Cell Sci. 2000, 113:2011-2021.
115. Zhou S., Schuetz J.D., Bunting K.D., Colapietro A.M., Sampath J., Morris J.J., Lagutina I., Grosveld G.C., Osawa M., Nakauchi H., Sorrentino B.P. 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.
116. Monzani E., Facchetti F., Galmozzi E., Corsini E., Benetti A., Cavazzin C., Gritti A., Piccinini A., Porro D., Santinami M., Invernici G., Parati E., Alessandri G., La Porta C.A. Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourogenic potential. Eur. J. Cancer 2007, 43:935-946.
117. Deichmann M., Thome M., Egner U., Hartschuh W., Kurzen H. The chemoresistance gene ABCG2 (MXR/BCRP1/ABCP1) is not expressed in melanomas but in single neuroendocrine carcinomas of the skin. J. Cutan. Pathol. 2005, 32:467-473.
118. Yamamoto K., Suzu S., Yoshidomi Y., Hiyoshi M., Harada H., Okada S. Erythroblasts highly express the ABC transporter Bcrp1/ABCG2 but do not show the side population (SP) phenotype. Immunol. Lett. 2007, 114:52-58.
119. Broadley K.W., Hunn M.K., Farrand K.J., Price K.M., Grasso C., Miller R.J., Hermans I.F., McConnell M.J. Side population is not necessary or sufficient for a cancer stem cell phenotype in glioblastoma multiforme. Stem Cells 2011, 29:452-461.
120. Bleau A.M., Hambardzumyan D., Ozawa T., Fomchenko E.I., Huse J.T., Brennan C.W., Holland E.C. PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 2009, 4:226-235.
121. Harris M.A., Yang H., Low B.E., Mukherjee J., Guha A., Bronson R.T., Shultz L.D., Israel M.A., Yun K. Cancer stem cells are enriched in the side population cells in a mouse model of glioma. Cancer Res. 2008, 68:10051-10059.
122. Mitsutake N., Iwao A., Nagai K., Namba H., Ohtsuru A., Saenko V., Yamashita S. Characterization of side population in thyroid cancer cell lines: cancer stem-like cells are enriched partly but not exclusively. Endocrinology 2007, 148:1797-1803.
123. Burkert J., Otto W.R., Wright N.A. Side populations of gastrointestinal cancers are not enriched in stem cells. J. Pathol. 2008, 214:564-573.
124. Lichtenauer U.D., Shapiro I., Geiger K., Quinkler M., Fassnacht M., Nitschke R., Rueckauer K.D., Beuschlein F. Side population does not define stem cell-like cancer cells in the adrenocortical carcinoma cell line NCI h295R. Endocrinology 2008, 149:1314-1322.
125. Ho M.M., Ng A.V., Lam S., Hung J.Y. Side population in human lung cancer cell lines and tumors in enriched with stem-like cancer cells. Cancer Res. 2007, 67:4827-4833.
126. Wu A., Oh S., Wiesner S.M., Ericson K., Chen L., Hall W.A., Champoux P.E., Low W.C., Ohlfest J.R. Persistence of CD133+ cells in human and mouse glioma cell lines: detailed characterization of GL261 glioma cells with cancer stem cell-like properties. Stem Cells Dev. 2008, 17:173-184.
127. Sales-Pardo I., Avendano A., Martinez-Munoz V., Garcia-Escarp M., Celis R., Whittle P., Barquinero J., Domingo J.C., Marin P., Petriz J. Flow cytometry of the side population: tips & tricks. Cell. Oncol. 2006, 28:37-53.
128. Challen G.A., Boles N., Lin K.K., Goodell M.A. Mouse hematopoietic stem cell identification and analysis. Cytometry A 2009, 75:14-24.
129. Ma S., Chan K.W., Lee T.K., Tang K.H., Wo J.Y., Zheng B.J., Guan X.Y. Aldehyde dehydrogenase discriminates the CD133 liver cancer stem cell populations. Mol. Cancer Res. 2008, 6:1146-1153.
130. Ginestier C., Hur M.H., Charafe-Jauffret E., Monville F., Dutcher J., Brown M., Jacquemier J., Viens P., Kleer C.G., Liu S., Schott A., Hayes D., Birnbaum D., Wicha M.S., Dontu G. 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.
131. Armstrong L., Stojkovic M., Dimmick I., Ahmad S., Stojkovic P., Hole N., Lako M. Phenotypic characterization of murine primitive hematopoietic progenitor cells isolated on basis of aldehyde dehydrogenase activity. Stem Cells 2004, 22:1142-1151.
132. Hess D.A., Meyerrose T.E., Wirthlin L., Craft T.P., Herrbrich P.E., Creer M.H., Nolta J.A. Functional characterization of highly purified human hematopoietic repopulating cells isolated according to aldehyde dehydrogenase activity. Blood 2004, 104:1648-1655.
133. Gerber J.M., Smith B.D., Ngwang B., Zhang H., Vala M.S., Morsberger L., Galkin S., Collector M.I., Perkins B., Levis M.J., Griffin C.A., Sharkis S.J., Borowitz M.J., Karp J.E., Jones R.J. A clinically relevant population of leukemic CD34(+)CD38(-) cells in acute myeloid leukemia. Blood 2012, 119:3571-3577.
134. Stuelten C.H., Mertins S.D., Busch J.I., Gowens M., Scudiero D.A., Burkett M.W., Hite K.M., Alley M., Hollingshead M., Shoemaker R.H., Niederhuber J.E. Compex display of putative tumor stem cell markers in the NCI60 tumor cell line panel. Stem Cells 2010, 28:649-660.
135. Al Hajj M., Wicha M.S., Benito-Hernandez A., Morrison S.J., Clarke M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:3983-3988.
136. Beier D., Hau P., Proescholdt M., Lohmeier A., Wischhusen J., Oefner P.J., Aigner L., Brawanski A., Bogdahn U., Beier C.P. CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res. 2007, 67:4010-4015.
137. Zheng X., Shen G., Yang X., Liu W. Most C6 cells are cancer stem cells: evidence from clonal and population analyses. Cancer Res. 2007, 67:3691-3697.
138. Shmelkov S.V., Butler J.M., Hooper A.T., Hormigo A., Kushner J., Milde T., St Clair R., Baljevic M., White I., Jin D.K., Chadburn A., Murphy A.J., Valenzuela D.M., Gale N.W., Thurston G., Yancopoulos G.D., D'Angelica M., Kemeny N., Lyden D., Rafii S. CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J. Clin. Invest. 2008, 118:2111-2120.
139. Singh S.K., Clarke I.D., Terasaki M., Bonn V.E., Hawkins C., Squire J.A., Dirks P.B. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003, 63:5821-5828.
140. Zuba-Surma E.K., Kucia M., Ratajczak J., Ratajczak M.Z. "Small stem cells" in adult tissues: very small embryonic-like stem cells stand up!. Cytometry A 2009, 75:4-13.
141. Ratajczak M.Z., Kucia M., Ratajczak J., Zuba-Surma E.K. A multi-instrumental approach to identify and purify very small embryonic like stem cells (VSELs) from adult tissues. Micron 2009, 40:386-393.
142. Cammareri P., Lombardo Y., Francipane M.G., Bonventre S., Todaro M., Stassi G. Isolation and culture of colon cancer stem cells. Methods Cell Biol. 2008, 86:311-324.
143. Clement V., Marino D., Cudalbu C., Hamou M., Mlynarik V., de Tribolet N., Dietrich P., Gruetter R., Hegi M.E., Radovanovic I. Marker-independent identification of glioma-initiating cells. Nat. Methods 2010, 7:224-228.
144. Bidlingmaier S., Zhu X., Liu B. The utility and limitations of glycosylated human CD133 epitopes in defining cancer stem cells. J. Mol. Med. 2008, 86:1025-1032.
145. Tabu K., Sasai K., Kimura T., Wang L., Aoyanagi E., Kohsaka S., Tanino M., Nishihara H., Tanaka S. Promoter hypomethylation regulates CD133 expression in human gliomas. Cell Res. 2008, 18:1037-1046.
146. Fabian A., Barok M., Vereb G., Szollosi J. Die hard: are cancer cells the Bruce Willises of tumor biology?. Cytometry 2009, 75:67-74.
147. Visvader J.E., Lindeman G.J. Cancer stem cells in solid tumors: accumulating evidence and unresolved questions. Nat. Rev. Cancer 2008, 8:755-768.
148. Pollard S.M., Yoshikawa K., Clarke I.D., Danovi D., Stricker S., Russell R., Bayani J., Head R., Lee M., Bernstein M., Squire J.A., Smith A., Dirks P. 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.
149. Woolard K., Fine H.A. Glioma stem cells: better flat than round. Cell Stem Cell 2009, 4:466-467.
150. Holtz M.S., Forman S.J., Bhatia R. Nonproliferating CML CD34+ progenitors are resistant to apoptosis induced by a wide range of proapoptotic stimuli. Leukemia 2005, 19:1034-1041.
151. Moshaver B., van Rhenen A., Kelder A., van der Pol M., Terwijn M., Bachas C., Westra A.H., Ossenkoppele G.J., Zweegman S., Schuurhuis G.J. Identification of a small subpopulation of candidate leukemia-initiating cells in the side population of patients with acute myeloid leukemia. Stem Cells 2008, 26:3059-3067.
152. Carter B.Z., Qiu Y., Huang X., Diao L., Coombes K.R., Mak D.H., Konopleva M., Cortes J., Kantarjian H.M., Mills G.B., Andreeff M., Kornblau S.M. Survivin is highly expressed in CD34(+)38(-) leukemic stem/progenitor cells and predicts poor clinical outcomes in AML. Blood 2012, 120:173-180.
153. Baum C.M., Weissman I.L., Tsukamoto A.S., Buckle A.M., Peault B. Isolation of a candidate human hematopoietic stem-cell population. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:2804-2808.
154. Majeti R., Park C.Y., Weissman I.L. Identification of a hierarchy of multipotent hematopoietic progenitors in human cord blood. Cell Stem Cell 2007, 1:635-645.
155. van Rhenen A., van Dongen G.A., Kelder A., Rombouts E.J., Feller N., Moshaver B., Stigter-van Walsum M., Zweegman S., Ossenkoppele G.J., Jan Schuurhius G. The novel AML stem cell associated antigen CLL-1 aids in discrimination between normal and leukemic stem cell. Blood 2007, 110:2659-2666.
156. van Rhenen A., Moshaver B., Ossenkoppele G.J., Schuurhuis G.J. New approaches for the detection of minimal residual disease in acute myeloid leukemia. Curr. Hematol. Malig. Rep. 2007, 2:111-118.
157. Jordan C.T. The leukemic stem cell. Best Pract. Res. Clin. Haematol. 2007, 20:13-18.
158. Jan M., Chao M.P., Cha A.C., Alizadeh A.A., Gentles A.J., Weissman I.L., Majeti R. Prospective separation of normal and leukemic stem cells based on differential expression of TIM3, a human acute myeloid leukemia stem cell marker. Proc. Natl. Acad. Sci. 2011, 108:5009-5014.
159. Taussig D.C., Vargaftig J., Miraki-Moud F., Griessinger E., Sharrock K., Luke T., Lillington D., Oakervee H., Cavenagh J., Agrawal S.G., Lister T.A., Gribben J.G., Bonnet D. Leukemia-initiating cells from some acute myeloid leukemia patients with mutated nucleophosmin reside in the CD34--fraction. Blood 2010, 115:1976-1984.
160. Sarry J.-E., Murphy K., Perry R., Sanchez P.V., Secreto A., Keefer C., Swider C.R., Strzelecki A.-C., Cavelier C., Recher C., Mansat-De Mas V., Delabesse E., Danet-Desnoyers G., Carroll M. Human acute myelogenous leukemia stem cells are rare and heterogeneous when assayed in NOD/SCID/IL2Rγc-deficient mice. J. Clin. Invest. 2011, 121:384-395.
161. + cells from AML with mutated NPM1 harbor cytoplasmic mutated nucleophosmin and generate leukemia in immunocompromised mice. Blood 2010, 116:3907-3922.
162. Giambra V., Jenkins C.R., Wang H., Lam S.H., Shevchuk O.O., Nemirovsky O., Wai C., Gusscott S., Chiang M.Y., Aster J.C., Humphries R.K., Eaves C., Weng A.P. NOTCH1 promotes T cell leukemia-initiating activity by RUNX-mediated regulation of PKC-θ and reactive oxygen species. Nat. Med. 2012, 18:1693-1698.
163. Takahashi N., Miura I., Saitoh K., Miura A.B. Lineage involvement of stem cells bearing the Philadelphia chromosome in chronic myeloid leukemia in the chronic phase as shown by a combination of fluorescence-activated cell sorting and fluorescence in situ hybridization. Blood 1998, 92:4758-4763.
164. + human hemopoietic cells from normal and chronic myeloid leukemia sources. Stem Cells 2007, 25:3111-3120.
165. Abe A., Minami Y., Hayakawa F., Kitamura K., Nomura Y., Murata M., Katsumi A., Kiyoi H., Jamieson C.H., Wang J.Y.J., Naoe T. Retention but significant reduction of BCR-ABK transcript in hematopoietic stem cells in chronic myelogenous leukemia after imatinib therapy. Int. J. Hematol. 2008, 88:471-475.
166. McWeeney S.K., Pemberton L.C., Loriaux M.M., Vartanian K., Willis S.G., Yochum G., Wilmot B., Turpaz Y., Pillai R., Druker B.J., Snead J.L., MacPartlin M., O'Brien S.G., Melo J.V., Lange T., Harrington C.A., Deininger M.W. A gene expression signature of CD34+ cells to predict major cytogenetic response in chronic-phase chronic myeloid leukemia patients treated with imatinib. Blood 2010, 115:315-325.
167. + cells identifies a molecular signature of chronic myeloid leukemia blast crysis. Leukemia 2006, 20:1028-1034.
168. Moshaver B., van Rhenen A., Kelder A., van der Pol M., Terwijn M., Bachas C., Westra A.H., Ossenkoppele G.J., Zweegman S., Schuurhuis G.J. Identification of a small subpopulation of candidate leukemia-initiating cells in the side population of patients with acute myeloid leukemia. Stem Cells 2008, 26:3059-3067.
169. Zehentner B.K., Fritschle W., Stelzer T., Ghirardelli K.M., Hunter K., Wentzel C., Bennington R., Hansen C.L., Myerson D., Kalnoski M., Wells D.A., Loken M.R. Minimal disease detection and confirmation in hematologic malignancies: combining cell sorting with clonality profiling. Clin. Chem. 2006, 52:430-437.
170. Engel H., Goodacre A., Keyhani A., Jiang S., Van N.T., Kimmel M., Sanchez-Williams G., Andreeff M. Minimal residual disease in acute myelogenous leaukemia and myelodysplastic syndromes: a follow-up of patients in clinical remission. Br. J. Haematol. 1997, 99:64-75.
171. Cotteret S., Belloc F., Boiron J.M., Bilhou-Nabera C., Dumain P., Boyer C., Lacombe F., Reiffers J., Bernard P. Fluorescent in situ hybridization on flow-sorted cells as a tool for evaluating minimal residual disease or chimerism after allogeneic bone marrow transplantation. Cytometry 1998, 34:216-222.
172. Godder K.T., Abhyankar S.H., Lamb L.S., Best R.G., Geier S.S., Pati A.R., Gee A.P., Henslee-Downey P.J. Donor leukocyte infusion for treatment of graft rejection post partially mismatched related donor bone marrow transplant. Bone Marrow Transplant. 1998, 22:111-113.
173. Zaliova M., Fronkova E., Krejcikova K., Muzikova K., Mejstrikova E., Stary J., Trka J., Zuna J. Quantification of fusion transcript reveals a subgroup with distinct biological properties and predicts relapse in BCR/ABL- positive ALL: implications for residual disease monitoring. Leukemia 2009, 23:944-951.
174. + cell sorting. Leukemia 2001, 15:1408-1414.
175. Shaffer D.R., Leversha M.A., Danila D.C., Lin O., Gonzalez-Espinoza R., Gu B., Anand A., Smith K., Maslak P., Doyle G.V., Terstappen L.W., Lilja H., Heller G., Fleisher M., Scher H.I. Circulating tumor cell analysis in patients with progressive castration-resistant prostate cancer. Clin. Cancer Res. 2007, 13:2023-2029.
176. Logan A.C., Weissman I.L., Shizuru J.A. The road to purified hematopoietic stem cell transplants is paved with antibodies. Curr. Opin. Immunol. 2012, 24:640-648.
177. Chiang A.C., Massague J. Molecular basis of metastasis. N. Engl. J. Med. 2008, 359:2814-2823.
178. Ross A.A., Cooper B.W., Lazarus H.M., Mackay W., Moss T.J., Ciobanu N., Tallman M.S., Kennedy M.J., Davidson N.E., Sweet D., et al. Detection and viability of tumor cells in peripheral blood stem cell collections from breast cancer patients using immunocytochemical and clonogenic assay techniques. Blood 1993, 82:2605-2610.
179. Sleijifer S., Gratama J.-W., Sieuwerts A.M., Kraan J., Martens J.W.M., Foekens J.A. Circulating tumour cell detection on its way to routine diagnostic implementation?. Eur. J. Cancer 2007, 43:2645-2650.
180. Tibbe A.G.J., Miller M.C., Terstappen L.W. Statistical considerations for enumeration of circulating tumor cells. Cytometry A 2007, 71:154-162.
181. Allan A.L., Keeney M. Circulating tumor analysis: technical and statistical considerations for application to the clinic. J. Oncol. 2010, 426218.
182. Xi L., Nicastri D.G., El-Hefnawy T., Hughes S.J., Luketich J.D., Godfrey T.E. Optimal markers for real-time quantitative reverse transcription PCR detection of circulating tumor cells from melanoma, breast, colon, esophageal, head and neck, and lung cancers. Clin. Chem. 2007, 53:1206-1215.
183. Pantel K., Brakenhoff R.H., Brandt B. Detection, clinical relevance and specific biological properties of disseminating tumour cells. Nat. Rev. Cancer 2008, 8:329-340.
184. Hristozova T., Konschak R., Budach V., Tinhofer I. A simple multicolor flow cytometry protocol for detection and molecular characterization of circulating tumor cells in epithelial cancers. Cytometry A 2012, 81:489-495.
185. Jung R., Krueger W., Hosch S., Holweg M., Kroeger N., Gutensohn K., Wagener C., Neumaier M., Zander A.R. Specificity of reverse transcriptase polymerase chain reaction assays designed for the detection of circulating cancer cells is influenced by cytokines in vivo and in vitro. Br. J. Cancer 1998, 78:1194-1198.
186. Thiery J.P., Sleeman J.P. Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 2006, 7:131-142.
187. Polyak K., Weinberg R.A. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat. Rev. Cancer 2009, 9:265-273.
188. Sieuwerts A.M., Kraan J., Bolt J., van der Spoel P., Elstrodt F., Schutte M., Martens J.W., Gratama J.W., Sleijfer S., Foekens J.A. Anti-epithelial cell adhesion molecule antibodies and the detection of circulating normal-like breast tumor cells. J. Natl. Cancer Inst. 2009, 101:61-66.
189. Cristofanilli M., Budd G.T., Ellis M.J., Stopeck A., Matera J., Miller M.C., Reuben J.M., Doyle G.V., Allard W.J., Terstappen L.W., Hayes D.F. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N. Engl. J. Med. 2004, 351:781-791.
190. Pierga J., Bidard F., Denis M.G., de Cremoux P. Prognostic value of peripheral blood double detection of CK19 and MUC1 mRNA positive cells detected by RT-quantitative PCR in 94 breast cancer patients with follow-up of 9years. Mol. Oncol. 2007, 1:267-268.
191. Smerage J.B., Hayes D.F. The prognostic implications of circulating tumor cells in patients with breast cancer. Cancer Invest. 2008, 26:109-114.
192. Bidard F.C., Saliba A.E., Saias L., Degeorges A., Cremoux P., Viovy J.L., Vincent-Salomon A., Mathiot C., Pierga J.Y., de Gramont A. Circulating tumor cells and breast cancer: detection techniques and clinical results. Bull. Cancer (French) 2009, 96:73-86.
193. Budd G.T., Cristofanilli M., Ellis M.J., Stopeck A., Borden E., Miller M.C., Repollet M., Doyle G.V., Terstappen L.W., Hayes D.F. Circulating tumor cells versus imaging-predicting overall survival in metastatic breast cancer. Clin. Cancer Res. 2006, 12:6403-6409.
194. Galanzha E.I., Zharov V.P. Photoacoustic flow cytometry. Methods 2012, 57:280-296.
195. Tuchin V.V., Tarnok A., Zharov V.P. In vivo flow cytometry: a horizon of opportunities. Cytometry A 2011, 79:737-745.
196. Fan Z.C., Yan J., Liu G.D., Tan X.Y., Weng X.F., Wu W.Z., Zhou J., Wei X.B. Real-time monitoring of rare circulating hepatocellular carcinoma cells in an orthotopic model by in vivo flow cytometry assesses resection on metastasis. Cancer Res. 2012, 72:2683-2691.
197. Golan L., Yeheskely-Hayon D., Minai L., Dann E.J., Yelin D. Noninvasive imaging of flowing blood cells using label-free spectrally encoded flow cytometry. Biomed. Opt. Express 2012, 3:1455-1464.
198. Nedosekin D.A., Sarimollaoglu M., Galanzha E.I., Sawant R., Torchilin V.P., Verkhusha V.V., Ma J., Frank M.H., Biris A.S., Zharov V.P. Synergy of photoacoustic and fluorescence flow cytometry of circulating cells with negative and positive contrasts. J. Biophotonics 2012, (Epub Aug 20).
199. Stovel R.T. Influence of particles on jet breakoff. J. Hystochem. Cytochem. 1977, 25:813-820.
200. Ibrahim S.F., van den Engh G. High-speed cell sorting: fundamentals and recent advances. Curr. Opin. Biotechnol. 2003, 14:5-12.
201. Shapiro H.M. Practical flow cytometry 2003, John Wiley &Sons Inc., Hoboken, New Jersey. Fourth ed.
202. Bernstein R.L., Hyun W.C., Davis J.H., Fulwyler M.J., Pershadsingh H.A. Flow cytometric analysis of mature adipocytes. Cytometry 1989, 10:469-474.
203. Resina-Pelfort O., Comas-Riu J., Vives-Rego J. Effects of deflected droplet electrostatic cell sorting on the viability and exoproteolytic activity of bacterial cultures and marine bacterioplankton. Syst. Appl. Microbiol. 2001, 24:31-36.
204. Suh T.K., Schenk J.L., Seidel G.E. High pressure flow cytometric sorting damages sperm. Theriogenology 2005, 64:1035-1048.
205. Fromm J.R., Wood B.L. Strategies for immunophenotyping and purifying classical Hodgkin lymphoma cells from lymph nodes by flow cytometry and flow cytometric cell sorting. Methods 2012, 57:368-375.
206. Gross H.J., Verwer B., Houck D., Recktenwald D. Detection of rare cell at frequency of one per million by flow cytometry. Cytometry 1993, 14:519-526.
207. Leary J.F. Strategies for rare cell detection and isolation. Methods Cell Biol. 1994, 42 PtB:331-358.
208. Radbruch A., Rectenwald D. Detection and isolation of rare cells. Curr. Opin. Immunol. 1995, 7:270-273.
209. Daugherty P.S., Iverson B.L., Georgiou G. Flow cytometric screening of cell-based libraries. J. Immunol. Methods 2000, 243:211-227.
210. Vorobjev I.A., Buchholz K., Prabhat P., Ketman K., Egan E., Marti M., Duraisingh M.T., Barteneva N.S. Optimization of flow cytometric detection and cell sorting of transgenic Plasmodium parasites using interchangeable optical filters. Malar. J. 2012, 11:312.
211. Klein A.B., Witonsky S.G., Ahmed S.A., Holladay S.D., Gogal R.M., Link L., Reilly C.M. Impact of different cell isolation techniques on lymphocyte viability and function. J. Immunoass. Immunochem. 2006, 27:61-76.
212. Panchision D.M., Chen H.-L., Pistollato F., Papini D., Ni H.T., Hawley T.S. Optimized flow cytometric analysis of central nervous system tissue reveals novel functional relationships among cells expressing CD133, CD15, and CD24. Stem Cells 2007, 25:1560-1570.
213. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J.A., Hide T., Henkelman R.M., Cusimano M.D., Dirks P.B. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401.
214. Stockinger H., Majdic O., Liszka K., Aberer W., Bettelheim P., Lutz D., Knapp W. Exposure by desialyation of myeloid antigens on acute lymphoblastic leukemia cells. J. Natl. Cancer Inst. 1984, 73:7-11.
215. Corver W.E., Cornelisse C.J., Hermans J., Fleuren G.J. Limited loss of nine tumor-associated surface antigenic determinants after tryptic cell dissociation. Cytometry 1995, 19:267-272.
216. Cunningham R.E. Tissue disaggregation. Methods Mol. Biol. 2010, 588:327-330.
217. Cerra R., Zarbo R.J., Crissman J.D. Dissociation of cells from solid tumors. Methods Cell. Biol. 1990, 33:1-12.
218. Frisch S.M., Screaton R.A. Anoikis mechanisms. Curr. Opin. Cell Biol. 2001, 13:555-562.
219. Watanabe K., Ueno M., Kamiya D., Nishiyama A., Matsumura M., Wataya T., Takahashi J.B., Nishikawa S., Nishikawa S., Muguruma K., Sasai Y. A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat. Biotechnol. 2007, 25:681-686.
220. Emre N., Vidal J.G., Elia J., O'Connor E.D., Paramban R.I., Hefferan M.P., Navarro R., Goldberg D.S., Varki N.M., Marsala M., Carson C.T. The ROCK inhibitor Y-27632 improves recovery of human embryonic stem cells after fluorescence-activated cell sorting with multiple cell surface markers. PLoS One 2010, 5:e12148.
221. Sugiyama T., Kim S.K. Fluorescence-activated cell sorting purification of pancreatic progenitor cells. Diabetes Obes. Metab. 2008, 10(Suppl. 4):179-185.
222. Jett J.H., Alexander R.G. Droplet sorting of large particles. Cytometry 1985, 6:484-486.
223. Osborne G.W. A method of quantifying cell sorting yield in "real time". Cytometry A 2010, 77:983-989.
224. Leahy T., Celi P., Bathgate R., Evans G., Maxwell W.M., Marti J.I. Flow-sorted ram spermatozoa are highly susceptible to hydrogen peroxide damage but are protected by seminal plasma and catalase. Reprod. Fertil. Dev. 2010, 22:1131-1140.
225. Boehmer R.M., Bandala-Sanchez E., Harrison L.C. Forward light scatter is a simple measure of T-cell activation and proliferation but is not universally suited for doublet discrimination. Cytometry A 2011, 79A:646-652.
226. Arnold L.W., Lannigan J. Practical issues in high-speed cell sorting. Curr. Protoc. Cytom. 2010, 1-30. (Chapter 1: Unit 1.24).
227. Boonyaratanakornkit J.B., Yue L., Strachan L.R., Scalapino K.J., LeBoit P.E., Lu Y., Leong S.P., Smith J.E., Ghadially R. Selection of tumorigenic melanoma cells using ALDH. J. Invest. Dermatol. 2010, 130:2799-2808.
228. Bigos M., Bigos M. Separation index: an easy-to-use metric for evaluation of different configurations on the same flow cytometer. Curr. Protoc. Cytom. 2007, (Chapter 1; Unit 1.21).
229. Gross H.J., Verwer B., Houck D., Hoffman R.A., Recktenwald D. Model study detecting breast cancer cells in peripheral blood mononuclear cells at frequencies as low as 10(-7). Proc. Natl. Acad. Sci. U.S.A. 1995, 92:537-541.
230. Perfetto S.P., Chattopadhyay P.K., Roederer M. Seventeen-colour flow cytometry: unravelling the immune system. Nat. Rev. Immunol. 2004, 4:648-655.
231. Preffer F., Dombkowski D. Advances in complex multiparameter flow cytometry technology: applications in stem cell reserch. Cytometry B Clin. Cytom. 2009, 76:295-314.
232. Kalina T., Flores-Montero J., van der Velden V.H., Martin-Ayuso M., Boettcher S., Ritgen M., Almeida J., Lhermitte L., Asnafi V., Mendonca A., de Tute R., Cullen M., Sedek L., Vidriales M.B., Perez J.J., te Marvelde J.G., Mejstrikova E., Hrusak O., Szczepanski T., Van Dongen J.J., Orfao A. EuroFlow standardization of flow cytometer instrument settings and immunophenotyping protocols. Leukemia 2012, 26:1986-2010.
233. Domingues P.H., Teodosio C., Ortiz J., Sousa P., Otero A., Maillo A., Barcena P., Garcia-Macias M.C., Lopes M.C., de Oliveira C., Orfao A., Tabernero M.D. Immunophenotypic identification and characterization of tumor cells and infiltrating cell populations in meningiomas. Am. J. Pathol. 2012, 181:1749-1761.
234. van Dongen J.J., Orfao A. EuroFlow Consortium, EuroFlow: resetting leukemia and lymphoma immunophenotyping. Basis for companion diagnostics and personalized medicine. Leukemia 2012, 26:1899-1907.
235. Tricot G., Gazitt Y., Leemhius T., Jagannath S., Desikan K.R., Siegel D., Fassas A., Tindle S., Nelson J., Juttner C., Tsukamoto A., Hallagan J., Atkinson K., Reading C., Hoffman R., Barlogie B. Collection, tumor contamination, and engraftment kinetics of highly purified progenitor cells to support high dose therapy in multiple myeloma. Blood 1998, 91:4489-4495.
236. Kim D., Park C.Y., Medeiros B.C., Weissman I.L. CD19(-)CD45(low/-)CD38(high)/CD138(+) plasma cells enrich for human tumorigenic myeloma cells. Leukemia 2012, 26:2530-2537.
237. Fromm J.R., Kussick S.J., Wood B.L. Identification and purification of classical Hodgkin cells from lymph nodes by flow cytometry and flow cytometric cell sorting. Am. J. Pathol. 2006, 126:764-780.
238. Frelinger J., Ottinger J., Gouttefangeas C., Chan C. Modeling flow cytometry data for cancer vaccine immune monitoring. Cancer Immunol. Immunother. 2010, 59:1435-1441.
239. Sarkar D., Le Meur N., Gentleman R. Using flowViz to visualize flow cytometry data. Bioinformatics 2008, 24:878-879.
240. Lo K., Hahne F., Brinkman R.R., Gottardo R. FlowClust: a Bioconductor package for automated gating of flow cytometry data. BMC Bioinforma. 2009, 10:145.
241. Miller D.T., Hunsberger B.C., Bagwell C.B. Automated analysis of GPI-deficient leukocyte flow cytometric data using GemStoneTM. Cytometry B 2012, 82B:319-324.
242. Agelopoulos K., Greve B., Schmidt H., Pospisil H., Kurtz S., Bartkowiak K., Andreas A., Wieczorek M., Korsching E., Buerger H., Brandt B. Selective regain of egfr gene copies in CD44+/CD24-/low breast cancer cellular model MDA-MB-468. BMC Cancer 2010, 10:78.
243. Bae K.M., Parker N.N., Dai Y., Vieweg J., Siemann D.W. E-cadherin plasticity in prostate cancer stem cell invasion. Am. J. Cancer Res. 2011, 1:71-84.
244. Goldstein A.S., Huang J., Guo C., Garraway I.P., Witte O.N. Identification of a cell of origin for human prostate cancer. Science 2010, 329:568-571.
245. + cancer stem cells in glioblastoma. Mol. Cancer 2006, 5:67.
246. Navin N., Krasnitz A., Rodgers L., Cook K., Meth J., Kendall J., Riggs M., Eberling Y., Troge J., Grubor V., Levy D., Lundin P., Maaner S., Zetterberg A., Hicks J., Wigler M. Inferring tumor progression from genomic heterogeneity. Genome Res. 2010, 20:68-80.
247. Ruiz C., Lenkiewicz E., Evers L., Holley T., Robeson A., Kiefer J., Demeure M.J., Hollingsworth M.A., Shen M., Prunkard D., Rabinovitch P.S., Zellweger T., Mousses S., Trent J.M., Carpten J.D., Bubendorf L., Von Hoff D., Barrett M.T. Advancing a clinically relevant perspective of the clonal nature of cancer. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:12054-12059.
248. Baldetorp B., Johansson M., Ingvar C., Lundgren L., Olsson H., Jansson B., Welinder C. Analysis of protein expression in pure cell nuclei populations isolated from human breast cancer tissue by DNA flow cytometric sorting. J. Proteome 2010, 73:1111-1116.
249. Geido E., Sciutto A., Rubagotti A., Oliani C., Monaco R., Risio M., Giaretti W. Combined DNA flow cytometry and sorting with k-ras2 mutation spectrum analysis and the prognosis of human sporadic colorectal cancer. Cytometry (Clin. Cytom.) 2002, 50:216-224.
250. Gribble S.M., Ng B.L., Prigmore E., Fitzgerald T., Carter N.P. Array painting: a protocol for the rapid analysis of aberrant chromosomes using DNA microarrays. Nat. Protoc. 2009, 4:1722-1736.
251. Butler T.P., Gullino P.M. Quantitation of cell shedding into efferent blood of mammary adenocarcinoma. Cancer Res. 1975, 35:512-516.
252. Liotta L.A., Saidel M.G., Kleinerman J. The significance of hematogenous tumor cell clumps in the metastatic process. Cancer Res. 1976, 36:889-894.
253. Liotta L.A., Saidel M.G., Kleinerman J. The significance of hematogenous tumor cell clumps in the metastatic process. Cancer Res. 1976, 36:889-894.
254. Radisic M., Iyer R.K., Murthy S.K. Micro- and nanotechnology in cell separation. Int. J. Nanomedicine 2006, 1:3-14.
255. Whitesides G.M. The origins and the future of microfluidics. Nature 2006, 442:368-373.
256. Cho S.H., Chen C.H., Tsai F.S., Godin J.M., Lo Y.H. Human mammalian cell sorting using a highly integrated micro-fabricated fluorescence-activated cell sorter (microFACS). Lab. Chip 2010, 10:1567-1573.
257. Krueger J., Singh K., O'Neill A., Jackson C., Morrison A., O'Brien P. Development of a microfluidic device for fluorescence activated cell sorting. J. Micromech. Microeng. 2002, 12:486-494.
258. Wolff A., Perch-Nielsen I.R., Larsen U.D., Friis P., Goranovic G., Poulsen C.R., Kutter J.P., Telleman P. Integrating advanced functionality in a microfabricated high-throughput fluorescent-activated cell sorter. Lab. Chip 2003, 3:22-27.
259. Simonnet C., Groisman A. High-throughput and high-resolution flow cytometry in molded microfluidic devices. Anal. Chem. 2006, 78:5653-5663.
260. Xu Y., Phillips J.A., Yan J., Li Q., Fan Z.H., Tan W. Aptamer-based microfluidic device for enrichment, sorting and detection of multiple cancer cells. Anal. Chem. 2009, 81:7436-7442.
261. Sequist L.V., Nagrath S., Toner M., Haber D.A., Lynch T.J. The CTC-chip: an exciting new tool to detect circulating tumor cells in lung cancer patients. J. Thorac. Oncol. 2009, 4:281-283.
262. Lau A.Y., Lee L.P., Chan J.W. An integrated optofluidic platform for Raman-activated cell sorting (RACS). Lab. Chip 2008, 8:1116-1120.
263. Lathia J.D., Venere M., Rao M.S., Rich J.N. Seeing is believing: are cancer stem cells the Loch Ness monster of tumor biology?. Stem Cell Rev. 2011, 7:227-237.
264. Hernandez-Vargas H., Ouzounova M., Le Calvez-Kelm F., Lambert M.P., McKay-Chopin S., Tavtigian S.V., Puisieux A., Matar C., Herceg Z. Methylome analysis reveals Jak-STAT pathway deregulation in putative brest cancer stem cells. Epigenetics 2011, 6:428-439.
265. Kodach L.L., Jacobs R.J., Voorneveld P.W., Wildenberg M.E., Verspaget H.W., van Wezel T., Morreau H., Hommes D.W., Peppelenbosch M.P., van den Brink G.R., Hardwick J.C. Statins augment the chemosensitivity of colorectal cancer cells inducing epigenetic reprogramming and reducing colorectal cancer cell "stemness" via the bone morphogenetic protein pathway. Gut 2011, 60:1544-1553.
266. Furusawa J., Zhang H., Vural E., Stone A., Fukuda S., Oridate N., Fang H., Ye Y., Suen J.Y., Fan C.Y. Distinct epigenetic profiling in head and neck squamous cell carcinoma stem cells. Otolaryngol. Head Neck Surg. 2011, 144:900-909.