Tracking antigen-driven responses by flow cytometry: Monitoring proliferation by dye dilution

Cytometry Part A

Volumn 73, Issue 11, 2008, Pages 1019-1034

  Wallace, Paul K ^a   Tario Jr , Joseph D ^a   Fisher, Jan L ^b   Wallace, Stephen S ^a   Ernstoff, Marc S ^b   Muirhead, Katharine A ^c  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c SciGro Inc   (United States)

Author keywords

Cell tracking; CellVue dyes; CFSE; Dye dilution proliferation assay; Flow cytometry; PKH dyes; Precursor frequency; Proliferation analysis

Indexed keywords

GAMMA INTERFERON; GREEN FLUORESCENT PROTEIN; RED FLUORESCENT PROTEIN;

ANTIGEN BINDING; ANTIGEN SPECIFICITY; ARTICLE; CELL LABELING; DAUGHTER CELL; DYE DILUTION CURVE; EFFECTOR CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; LYMPHOCYTE PROLIFERATION; NEAR INFRARED SPECTROSCOPY; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

ANTIGENS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; DYE DILUTION TECHNIQUE; FLOW CYTOMETRY; FLUORESCEINS; HUMANS; ORGANIC CHEMICALS; REPRODUCIBILITY OF RESULTS; STAINING AND LABELING; SUCCINIMIDES;

EID: 55949113634     PISSN: 15524922     EISSN: 15524930     Source Type: Journal    
DOI: 10.1002/cyto.a.20619     Document Type: Article

References (72)

1. Lyons AB, Parish CR. Determination of lymphocyte division by flow cytometry. J Immunol Methods 1994;171:131-137.
2. Hawkins ED, Hommel M, Turner ML, Battye FL, Markham JF, Hodgkin PD. Measuring lymphocyte proliferation, survival and differentiation using CFSE time-series data. Nat Protoc 2007;2:2057-2067.
3. Wallace PK, Muirhead KA. Cell tracking 2007: A proliferation of probes and applications. Immunol Invest 2007;36:527-561.
4. Bercovici N, Givan AL, Waugh MG, Fisher JL, Vernel-Pauillac F, Ernstoff MS, Abastado JP, Wallace PK. Multiparameter precursor analysis of T-cell responses to antigen. J Immunol Methods 2003;276:5-17.
5. Fazekas de St Groth B, Smith AL, Koh WP, Girgis L, Cook MC, Bertolino P. Carboxyfluorescein diacetate succinimidyl ester and the virgin lymphocyte: A marriage made in heaven. Immunol Cell Biol 1999;77:530-538.
6. Tanaka Y, Ohdan H, Onoe T, Asahara T. Multiparameter flow cytometric approach for simultaneous evaluation of proliferation and cytokine-secreting activity in T cells responding to allo-stimulation. Immunol Invest 2004;33:309-324.
7. Weston SA, Parish CR. New fluorescent dyes for lymphocyte migration studies. Analysis by flow cytometry and fluorescence microscopy. J Immunol Methods 1990;133:87-97.
8. Wells AD, Gudmundsdottir H, Turka LA. Following the fate of individual T cells throughout activation and clonal expansion. Signals from T cell receptor and CD28 differentially regulate the induction and duration of a proliferative response. J Clin Invest 1997;100:3173-3183.
9. Bird JJ, Brown DR, Mullen AC, Moskowitz NH, Mahowald MA, Sider JR, Gajewski TF, Wang C-R, Reiner SL. Helper T cell differentiation is controlled by the cell cycle. Immunity 1998;9:229-237.
10. Li Y, Li XC, Zheng XX, Wells AD, Turka LA, Strom TB. Blocking both signal 1 and signal 2 of T-cell activation prevents apoptosis of alloreactive T cells and induction of peripheral allograft tolerance. Nat Med 1999;5:1298-1302.
11. Gett AV, Hodgkin PD. A cellular calculus for signal integration by T cells. Nat Immun 2000;1:239-244.
12. Popma SH, Krasinskas AM, McLean AD, Szeto WY, Kreisel D, Moore JS, Rosengard BR. Immune monitoring in xenotransplantation: The multiparameter flow cytometric mixed lymphocyte culture assay. Cytometry 2000;42:277-283.
13. Champagne P, Ogg GS, King AS, Knabenhans C, Ellefsen K, Nobile M, Appay V, Rizzardi GP, Fleury S, Lipp M, Förster R, Rowland-Jones S, Sékaly RP, McMichael AJ, Pantaleo G. Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature 2001;410:106-111.
14. Brusko TM, Hulme MA, Myhr CB, Haller MJ, Atkinson MA. Assessing the in vitro suppressive capacity of regulatory T cells. Immunol Invest 2007;36:607-628.
15. Song HK, Noorchashm H, Lieu YK, Rostami S, Greeley SA, Barker CF, Naji A. Tracking alloreactive cell division in vivo. Transplantation 1999;68:297-299.
16. Ku CC, Murakami M, Sakamoto A, Kappler J, Marrack P. Control of homeostasis of CD8+ memory T cells by opposing cytokines. Science 2000;288:675-678.
17. Veiga-Fernandes H, Walter U, Bourgeois C, McLean A, Rocha B. Response of naive and memory CD8+ T cells to antigen stimulation in vivo. Nat Immun 2000;1:47-53.
18. Quah BJ, Warren HS, Parish CR. Monitoring lymphocyte proliferation in vitro and in vivo with the intracellular fluorescent dye carboxyfluorescein diacetate succinimidyl ester. Nat Protoc 2007;2:2049-2056.
19. Nordon RE, Nakamura M, Ramirez C, Odell R. Analysis of growth kinetics by division tracking. Immunol Cell Biol 1999;77:523-529.
20. Matera G, Lupi M, Ubezio P. Heterogeneous cell response to topotecan in a CFSE-based proliferation test. Cytometry Part A 2004;62A:118-128.
21. Ko KH, Odell R, Nordon RE. Analysis of cell differentiation by division tracking cytometry. Cytometry Part A 2007;71A:773-782.
22. Luzyanina T, Mrusek S, Edwards JT, Roose D, Ehl S, Bocharov G. Computational analysis of CFSE proliferation assay. J Math Biol 2007;54:57-89.
23. Luzyanina T, Roose D, Schenkel T, Sester M, Ehl S, Meyerhans A, Bocharov G. Numerical modelling of label-structured cell population growth using CFSE distribution data. Theor Biol Med Model 2007; http://www.tbiomed.com/content/4/ 1/26.
24. Kimura K, Vincent AL, Lager KM, Roth JA, Kehrli J, M.E. Assay for proliferation of porcine PBMC with Oregon Green 488 and its application for evaluation of T cell responsiveness to swine influenza virus [abstract]. J Immunol 2006;176:S118.
25. Magg T, Albert MH. Tracking cell proliferation using the far red fluorescent dye SNARF-1. Cytometry Part B Clin Cytom 2007;72B:458-464.
26. Quong MW, Harris DP, Swain SL, Murre C. E2A activity is induced during B-cell activation to promote immunoglobulin class switch recombination. EMBO J 1999;18:6307-6318.
27. Weber SE, Harbertson J, Godebu E, Mros GA, Padrick RC, Carson BD, Ziegler SF, Bradley LM. Adaptive islet-specific regulatory CD4 T cells control autoimmune diabetes and mediate the disappearance of pathogenic Th1 cells in vivo. J Immunol 2006;176:4730-4739.
28. Horan PK, Melnicoff MJ, Jensen BD, Slezak SE. Fluorescent cell labeling for in vivo and in vitro cell tracking. Methods Cell Biol 1990;33:469-490.
29. Wallace PK, Palmer LD, Perry-Lalley D, Bolton ES, Alexander RB, Horan PK, Yang JC, Muirhead KA. Mechanisms of adoptive immunotherapy: Improved methods for in vivo tracking of tumor-infiltrating lymphocytes and lymphokine-activated killer cells. Cancer Res 1993;53:2358-2367.
30. Givan AL, Fisher JL, Waugh M, Ernstoff MS, Wallace PK. A flow cytometric method to estimate the precursor frequencies of cells proliferating in response to specific antigens. J Immunol Methods 1999;230:99-112.
31. Poon RY, Ohlsson-Wilhelm BM, Bagwell CB, Muirhead KA. Use of PKH membrane intercalating dyes to monitor cell trafficking and function. In: Diamond RA, DeMagio S, editors. In Living Color: Flow Cytometry and Cell Sorting Protocols. New York: Springer-Verlag; 2000. pp 302-352.
32. Rousselle C, Barbier M, Comte VV, Alcouffe C, Clement-Lacroix J, Chancel G, Ronot X. Innocuousness and intracellular distribution of PKH67: A fluorescent probe for cell proliferation assessment. In Vitro Cell Dev Biol Anim 2001;37:646-655.
33. Bantly AD, Gray BD, Breslin E, Weinstein1 EG, Muirhead KA, Ohlsson-Wilhelm BM, Moore JS. Cellvue Claret, a new far-red dye, facilitates polychromatic assessment of immune cell proliferation. Immunol Invest 2007;36:581-605.
34. Tario JD Jr, Gray BD, Wallace SS, Muirhead KA, Ohlsson-Wilhelm BM, Wallace PK. Novel lipophilic tracking dyes for monitoring cell proliferation. Immunol Invest 2007;36:861-885.
35. Ashley DM, Bol SJ, Kannourakis G. Measurement of the growth parameters of precursor B-acute lymphoblastic leukaemic cells in co-culture with bone marrow stromal cells; detection of two cd10 positive populations with different proliferative capacities and survival. Leuk Res 1994;18:37-48.
36. Yamamura Y, Rodriguez N, Schwartz A, Eylar E, Bagwell B, Yano N. A new flow cytometric method for quantitative assessment of lymphocyte mitogenic potentials. Cell Mol Biol (Noisy-le-grand) 1995;41(Suppl 1):S121-S132.
37. Young AJ, Hay JB. Rapid turnover of the recirculating lymphocyte pool in vivo. Int Immunol 1995;7:1607-1615.
38. Allsopp CE, Nicholls SJ, Langhorne J. A flow cytometric method to assess antigen-specific proliferative responses of different subpopulations of fresh and cryopreserved human peripheral blood mononuclear cells. J Immunol Methods 1998;214:175-186.
39. Ohneda O, Fennie C, Zheng Z, Donahue C, La H, Villacorta R, Cairns B, Lasky LA. Hematopoietic stem cell maintenance and differentiation are supported by embryonic aorta-gonad-mesonephros region-derived endothelium. Blood 1998;92:908-919.
40. Batard P, Monier MN, Fortunel N, Ducos K, Sansilvestri-Morel P, Phan T, Hatzfeld A, Hatzfeld JA TGF-(beta)1 maintains hematopoietic immaturity by a reversible negative control of cell cycle and induces CD34 antigen up-modulation. J Cell Sci 2000;113(Part 3):383-390.
41. Bhatia R, Munthe HA, Williams AD, Zhang F, Forman SJ, Slovak ML. Chronic myelogenous leukemia primitive hematopoietic progenitors demonstrate increased sensitivity to growth factor-induced proliferation and maturation. Exp Hematol 2000;28:1401-1412.
42. Boutonnat J, Barbier M, Muirhead K, Mousseau M, Grunwald D, Ronot X, Seigneurin D. Response of chemosensitive and chemoresistant leukemic cell lines to drug therapy: Simultaneous assessment of proliferation, apoptosis, and necrosis. Cytometry 2000;42:50-60.
43. Rimaniol AC, Garcia G, Till SJ, Capel F, Gras G, Balabanian K, Emilie D, Humbert M. Evaluation of CD4+ T cells proliferating to grass pollen in seasonal allergic subjects by flow cytometry. Clin Exp Immunol 2003;132:76-80.
44. Askenasy N, Stein J, Farkas DL. Imaging approaches to hematopoietic stem and progenitor cell function and engraftment Immunol Invest 2007;36:713-738.
45. Waters WR, Sacco RE. Veterinary applications for monitoring mononuclear cell proliferation using cell tracking dyes. Immunol Invest 2007;36:887-908.
46. Bergmann C, Strauss L, Zeidler R, Lang S, Whiteside TL. Expansion and characteristics of human T regulatory type 1 cells in co-cultures simulating tumor microenvironment. Cancer Immunol Immunother 2007;56:1429-1442.
47. Suchin EJ, Langmuir PB, Palmer E, Sayegh MH, Wells AD, Turka LA. Quantifying the frequency of alloreactive T cells in vivo: New answers to an old question. J Immunol 2001;166:973-981.
48. Brooimans RA, Boyce CS, Popma J, Broyles DA, Gratama JW, Southwick PC, Keeney M. Analytical performance of a standardized single-platform MHC tetramer assay for the identification and enumeration of CMV-specific CD8+ T lymphocytes. Cytometry Part A 2008;73A: in press. DOI: 10.1002/cyto.a.20641 (this issue).
49. Nomura L, Maino VC, Maecker HT. Standardization and optimization of multiparameter flow cytometric studies. Cytometry Part A 2008;73A: in press. DOI: 10.1002/cyto.a.20602 (this issue).
50. Olive D, Autran B, Robinet E. The ELISPOT assay - quality issues related to its use in a multicenter setting. 2008; Presented at the thirdMASIR conference, La Plagne, France.
51. Givan AL. A flow cytometric assay for quantitation of rare antigen-specific T-cells: Using cell-tracking dyes to calculate precursor frequencies for proliferation. Immunol Invest 2007;36:563-580.
52. Lyons AB, Doherty KV. Flow cytometric analysis of cell division by dye dilution. In: Robinson JP, Darzynkiewicz Z, Hoffman R, Nolan JP, Orfao A, Rabinovitch PS, Watkins S, editors. Current Protocols in Cytometry. Volume 9.11. New York: John Wiley & Sons, Inc; 2004..
53. Givan AL, Fisher JL, Waugh MG, Bercovici N, Wallace PK. Use of cell-tracking dyes to determine proliferation precursor frequencies of antigen-specific T cells. Methods Mol Biol 2004;263:109-124.
54. Kreisel D, Krupnick AS, Gelman AE, Engels FH, Popma SH, Krasinskas AM, Balsara KR, Szeto WY, Turka LA, Rosengard BR. Non-hematopoietic allograft cells directly activate CD8+ T cells and trigger acute rejection: An alternative mechanism of allorecognition. Nat Med 2002;8:233-239.
55. VanOosten RL, Griffith TS. Activation of tumor-specific CD8+ T Cells after intratumoral Ad5-TRAIL/CpG oligodeoxynucleotide combination therapy. Cancer Res 2007;67:11980-11990.
56. De Clerck LS, Bridts CH, Mertens AM, Moens MM, Stevens WJ. Use of fluorescent dyes in the determination of adherence of human leucocytes to endothelial cells and the effect of fluorochromes on cellular function. J ImmunolMethods 1994;172:115-124.
57. Darling D, Galea-Lauri J, Gaken J, Towner P, Kuiper M, Hollingsworth S, Hirst W, Barnard A, Buggins A, Mufti G, Farzaneh F. In vitro immune modulation by antibodies coupled to tumour cells. Gene Ther 1997;4:1350-1360.
58. Fischer K, Andreesen R, Mackensen A. An improved flow cytometric assay for the determination of cytotoxic T lymphocyte activity. J Immunol Methods 2002;259:159-169.
59. Rieck B, Schlaak S. In vivo tracking of rat preadipocytes after autologous transplantation. Ann Plast Surg 2003;51:294-300.
60. Fulcher D, Wong S. Carboxyfluorescein succinimidyl ester-based proliferative assays for assessment of T cell function in the diagnostic laboratory. Immunol Cell Biol 1999;77:559-564.
61. Schwaab T, Fisher JL, Meehan KR, Fadul CE, Givan AL, Ernstoff MS. Dye dilution proliferation assay: Application of the DDPA to identify tumor-specific T cell precursor frequencies in clinical trials. Immunol Invest 2007;35:649-664.
62. Li Pira G, Ivaldi F, Dentone C, Righi E, Del Bono V, Viscoli C, Manca F. Miniaturization and automation for measuring antigen specific T-cell responses. 2008; Presented at the third MASIR conference, La Plagne, France.
63. Putz T, Ramoner R, Gander H, Rahm A, Bartsch G, Holtl L, Thurnher M. Monitoring of CD4+ and CD8+ T-cell responses after dendritic cell-based immunotherapy using CFSE dye dilution analysis. J Clin Immunol 2004;24:653-663.
64. Yu J, Chen H, Horton H, Bansal A, McElrath JM, Reichman R, Goepfert P, Jin X. Interleukin-2 reconstitutes defective human immunodeficiency virus (HIV), and cytomegalovirus (CMV) specific CD8+ T cell proliferation in HIV infection. J Med Virol 2006;78:1147-1157.
65. Lyons AB. Divided we stand: Tracking cell proliferation with carboxyfluorescein diacetate succinimidyl ester. Immunol Cell Biol 1999;77:509-515.
66. Wang LX, Li R, Yang G, Lim M, O'Hara A, Chu Y, Fox BA, Restifo NP, Urba WJ, Hu HM. Interleukin-7-dependent expansion and persistence of melanoma-specific T cells in lymphodepleted mice lead to tumor regression and editing. Cancer Res 2005;65:10569-10577.
67. Boyd FT. Identification of growth inhibited cells by retention of a lipophilic fluorescent dye. Cell Growth Differ 1993;4:777-784.
68. Stewart CC, Woodring ML, Podniesinski E, Gray B Flow cytometer in the infrared: Inexpensive modifications to a commercial instrument. Cytometry Part A 2005;67A:104-111.
69. Stewart CC, Stewart SJ. Four color compensation. Cytometry 1999;38:161-175.
70. Givan AL. Seeing the light: Lasers, Fluorochromes and Filters. Flow Cytometry: First Principles. New York: Wiley; 2001. pp 59-80.
71. Roederer M. Spectral compensation for flow cytometry: Visualization artifacts, limitations, and caveats. Cytometry 2001;45:194-205.
72. Bagwell CB. Hyperlog-a flexible log-like transform for negative, zero, and positive valued data. Cytometry Part A 2005;64A:34-42.