Dynamic single-cellmeasurements of gene expression in primary lymphocytes: Challenges, tools and prospects

Briefings in Functional Genomics

Volumn 12, Issue 2, 2013, Pages 99-108

  Polonsky, Michal ^a,b   Zaretsky, Irina ^b,c   Friedman, Nir ^b  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Live cell imaging; Lymphocytes; Microfluidics; Microwell arrays; T cells

Indexed keywords

ARTICLE; CELL ACTIVATION; CELL CULTURE; CELL DEATH; CELL FUNCTION; CELL MOTION; CELL PROLIFERATION; CELL SCREENING; CELL SELECTION; CELL VIABILITY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOLYSIS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; HUMAN; IMAGE ANALYSIS; IMMUNE RESPONSE; LYMPHOCYTE; MICROFLUIDICS; MICROTECHNOLOGY; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE CELL ANALYSIS; T LYMPHOCYTE ACTIVATION; CULTURE TECHNIQUE; CYTOLOGY; GENE EXPRESSION REGULATION; METABOLISM; METHODOLOGY; REVIEW;

CELL CULTURE TECHNIQUES; CELL PROLIFERATION; CELLS, CULTURED; GENE EXPRESSION REGULATION; HUMANS; LYMPHOCYTES; SINGLE-CELL ANALYSIS;

EID: 84875780166     PISSN: 20412649     EISSN: 20412657     Source Type: Journal    
DOI: 10.1093/bfgp/els061     Document Type: Article

References (59)

1. Ross IL, Browne CM, Hume DA. Transcription of individual genes in eukaryotic cells occurs randomly and infrequently. Immunol Cell Biol 1994;72:177-85.
2. Munsky B, Neuert G, van Oudenaarden A. Using gene expression noise to understand gene regulation. Science 2012;336:183-7.
3. Cai L, Friedman N, Xie XS. Stochastic protein expression in individual cells at the single molecule level. Nature 2006; 440:358-62.
4. Cohen AA, Kalisky T, Mayo A, et al. Protein dynamics in individual human cells: experiment and theory. PLoS One 2009;4:e4901.
5. Choi PJ, Cai L, Frieda K, et al. A stochastic single-molecule event triggers phenotype switching of a bacterial cell. Science 2008;322:442-6.
6. Raser JM, O'Shea EK. Noise in gene expression: origins, consequences, and control. Science 2005;309:2010-3.
7. Elowitz MB, Levine AJ, Siggia ED, et al. Stochastic gene expression in a single cell. Science 2002;297:1183-6.
8. Issaeva I, Cohen AA, Eden E, et al. Generation of double-labeled reporter cell lines for studying co-dynamics of endogenous proteins in individual human cells. PLoSOne 2010;5:e13524.
9. Zhu J, Paul WE. CD4 T cells: fates, functions, and faults. Blood 2008;112:1557-69.
10. Zhu J, Yamane H, Paul WE. Differentiation of effector CD4 T cell populations. Annual Rev Immunol 2010;28: 445-89.
11. Itoh Y, Germain RN. Single cell analysis reveals regulated hierarchical T cell antigen receptor signaling thresholds and intraclonal heterogeneity for individual cytokine responses of CD4+ T cells. J ExpMed 1997;186:757-66.
12. Germain RN. The art of the probable: system control in the adaptive immune system. Science 2001;293:240-5.
13. Bucy RP, Panoskaltsis-Mortari A, Huang GQ, et al. Heterogeneity of single cell cytokine gene expression in clonal T cell populations. J ExpMed 1994;180:1251-62.
14. Kelso A, Groves P, Troutt AB, et al. Evidence for the stochastic acquisition of cytokine profile by CD4+ T cells activated in a T helper type 2-like response in vivo. Eur J Immunol 1995;25:1168-75.
15. Hume DA. Probability in transcriptional regulation and its implications for leukocyte differentiation and inducible gene expression. Blood 2000;96:2323-8.
16. Callard RE. Decision-making by the immune response. Immunol Cell Biol 2007;85:300-5.
17. O'Shea JJ, Paul WE. Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells. Science 2010;327:1098-102.
18. London CA, Abbas AK, Kelso A. Helper T cell subsets: heterogeneity, functions and development. Vet Immunol Immunopathol 1998;63:37-44.
19. Miller MJ, Wei SH, Parker I, et al. Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 2002;296:1869-73.
20. Doh J, Krummel MF. Immunological synapses within context: patterns of cell-cell communication and their application in T-T interactions. Communication 2010;340: 25-50.
21. Sabatos C, Doh J, Chakravarti S, et al. A synaptic basis for paracrine interleukin-2 signaling during homotypic T cell interaction. Immunity 2008;29:238-48.
22. El-Ali J, Sorger PK, Jensen KF. Cells on chips. Nature 2006; 442:403-11.
23. McDonald JC, Whitesides GM. Poly(dimethylsiloxane) as a material for fabricating microfluidic devices. Acc Chem Res 2002;35:491-9.
24. Selimović S, Piraino F, Bae H, et al. Microfabricated polyester conical microwells for cell culture applications. Lab Chip 2011;11:2325-32.
25. Yamamura S, Kishi H, Tokimitsu Y, etal. Single-cell microarray for analyzing cellular response. Anal Chem 2005;77: 8050-6.
26. Love JC, Ronan JL, Grotenbreg GM, et al. A microengraving method for rapid selection of single cells producing antigen-specific antibodies. Nat Biotechnol 2006;24:703-7.
27. Zurgil N, Afrimzon E, Deutsch A, et al. Polymer live-cell array for real-time kinetic imaging of immune cells. Biomaterials 2010;31:5022-9.
28. Rettig JR, Folch A. Large-scale single-cell trapping and imaging using microwell arrays. Anal Chem 2005;77: 5628-34.
29. Zaretsky I, Polonsky M, Shifrut E, et al. Monitoring the dynamics of primary T cell activation and differentiation using long term live cell imaging in microwell arrays. Lab Chip 2012;12:5007-15.
30. Rosenthal A, Macdonald A, Voldman J. Cell patterning chip for controlling the stem cell microenvironment. Biomaterials 2007;28:3208-16.
31. Rottmar M, Ha°kanson M, Smith M, et al. Stem cell plasticity, osteogenic differentiation and the third dimension. J Mater SciMaterMed 2010;21:999-1004.
32. Han Q, Bradshaw EM, Nilsson B, et al. Multidimensional analysis of the frequencies and rates of cytokine secretion from single cells by quantitative microengraving. Lab Chip 2010;10:1391-400.
33. Ogunniyi AO, Story CM, Papa E, etal. Screening individual hybridomas by microengraving to discover monoclonal antibodies. Nat Protoc 2009;4:767-82.
34. Bradshaw EM, Kent SC, Tripuraneni V, et al. Concurrent detection of secreted products from human lymphocytes by microengraving: cytokines and antigen-reactive antibodies. Clin Immunol 2008;129:10-8.
35. Han Q, Bagheri N, Bradshaw EM, et al. Polyfunctional responses by human T cells result from sequential release of cytokines. Proc Natl Acad SciUSA 2012;109:1607-12.
36. Gong Y, Ogunniyi AO, Love JC. Massively parallel detection of gene expression in single cells using subnanolitre wells. Lab Chip 2010;10:2334-7.
37. Carroll S, Al-Rubeai M. The selection of high-producing cell lines using flow cytometry and cell sorting. Exp Opin BiolTher 2004;4:1821-9.
38. Varadarajan N, Julg B, Yamanaka YJ, et al. A highthroughput single-cell analysis of human CD8+ T cell functions reveals discordance for cytokine secretion and cytolysis. JClin Investig 2011;121:4322-31.
39. Duffy KR, Wellard CJ, Markham JF, et al. Activationinduced B cell fates are selected by intracellular stochastic competition. Science 2012;335:338-41.
40. Yui MA, Hernández-Hoyos G, Rothenberg EV. A new regulatory region of the IL-2 locus that confers positionindependent transgene expression. J Immunol 2001;166: 1730-9.
41. Holländer GA, Zuklys S, Morel C, et al. Monoallelic expression of the interleukin-2 locus. Science 1998;279: 2118-21.
42. Holländer GA. On the stochastic regulation of interleukin-2 transcription. Semin Immunol 1999;11:357-67.
43. Mohrs M, Shinkai K, Mohrs K, et al. Analysis of type 2 immunity in vivo with a bicistronic IL-4 reporter. Immunity 2001;15:303-11.
44. Bix M, Locksley RM. Independent and epigenetic regulation of the interleukin-4 alleles in CD4+ T cells. Science 1998;281:1352-4.
45. Rivière I, Sunshine MJ, Littman DR. Regulation of IL-4 expression by activation of individual alleles. Immunity 1998; 9:217-28.
46. Hu-Li J, Pannetier C, Guo L, et al. Regulation of expression of IL-4 alleles analysis using a chimeric GFP/IL-4 gene. Immunity 2001;14:1-11.
47. Mariani L, Schulz EG, Lexberg MH, et al. Short-term memory in gene induction reveals the regulatory principle behind stochastic IL-4 expression. Mol Syst Biol 2010;6: 359.
48. Yurkovsky E, Nachman I. Event timing at the single-cell level. Brief Funct Genomics 2012;12:90-8.
49. Hawkins ED, Markham JF, McGuinness LP, et al. A singlecell pedigree analysis of alternative stochastic lymphocyte fates. ProcNatl Acad SciUSA 2009;106:13457-62.
50. Schiffenbauer YS, Kalma Y, Trubniykov E, et al. A cell chip for sequential imaging of individual non-adherent live cells reveals transients and oscillations. Lab Chip 2009; 9:2965-72.
51. Guldevall K, Vanherberghen B, Frisk T, et al. Imaging immune surveillance of individual natural killer cells confined in microwell arrays. PLoS One 2010;5:e15453.
52. Day D, Pham K, Ludford-Menting MJ, et al. A method for prolonged imaging of motile lymphocytes. ImmunolCellBiol 2009;87:154-8.
53. Razooky BS, Gutierrez E, Terry VH, et al. Microwell devices with finger-like channels for long-term imaging of HIV-1 expression kinetics in primary human lymphocytes. Lab Chip 2012;12:4305-12.
54. Ozbudak EM, Thattai M, Kurtser I, et al. Regulation of noise in the expression of a single gene. Nature Genet 2002;31:69-73.
55. Luche H, Weber O, Nageswara Rao T, et al. Faithful activation of an extra-bright red fluorescent protein in "knock-in" Cre-reporter mice ideally suited for lineage tracing studies. EuropeanJ Immunol 2007;37:43-53.
56. Burroughs NJ, van der Merwe PA. Stochasticity and spatial heterogeneity in T-cell activation. Immunol Rev 2007;216: 69-80.
57. Garrity PA, Chen D, Rothenberg EV, et al. Interleukin-2 transcription is regulated in vivo at the level of coordinated binding of both constitutive and regulated factors. Mol Cell Biol 1994;14:2159-69.
58. Guo L, Hu-Li J, Paul WE. Probabilistic regulation in TH2 cells accounts for monoallelic expression of IL-4 and IL-13. Immunity 2005;23:89-99.
59. Calado DP, Paixão T, Holmberg D, et al. Stochastic monoallelic expression of IL-10 in T cells. J Immunol 2006;177: 5358-64.