Spatial Heterogeneity and Peptide Availability Determine CTL Killing Efficiency In Vivo

PLoS Computational Biology

Volumn 10, Issue 9, 2014, Pages

  Hogan, Thea ^a   Kadolsky, Ulrich ^b   Tung, Sim ^a   Seddon, Benedict ^c   Yates, Andrew ^b,d  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ASSAYS; CELL CULTURE; CELL MEMBRANES; CELL PROLIFERATION; CYTOTOXICITY; EPITOPES; IMMUNE SYSTEM; T-CELLS; VIRUSES;

B CELLS; CELL-BE; CELL/B.E; CYTOTOXIC T LYMPHOCYTES; IMMUNE RESPONSE; IN-VITRO; IN-VIVO; INFECTED CELLS; SPATIAL HETEROGENEITY; SPLENOCYTES;

PEPTIDES;

MAJOR HISTOCOMPATIBILITY ANTIGEN; PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CALCULATION; CELL DENSITY; CELL DIFFERENTIATION; CELL KILLING; CELL MIGRATION; CELL POPULATION; CELL SURFACE; CELL TYPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY TEST; IN VITRO STUDY; IN VIVO STUDY; MATHEMATICAL ANALYSIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SPLEEN; T LYMPHOCYTE; TARGET CELL; ANIMAL; BIOLOGICAL MODEL; CELL DEATH; CYTOLOGY; DISEASE MODEL; HUMAN; IMMUNOLOGY; INFLUENZA; TRANSGENIC MOUSE;

ANIMALS; B-LYMPHOCYTES; CELL DEATH; DISEASE MODELS, ANIMAL; HUMANS; INFLUENZA, HUMAN; MICE; MICE, TRANSGENIC; MODELS, IMMUNOLOGICAL; PEPTIDES; SPLEEN; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84907587263     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003805     Document Type: Article

References (45)

1. Chu G, (1978) The kinetics of target cell lysis by cytotoxic T lymphocytes: a description by Poisson statistics. Journal of Immunology 120: 1261–7.
2. Grimm EA, Thoma JA, Bonavida B, (1979) Mechanism of cell-mediated cytotoxicity at the single cell level. II. Evidence for first-order kinetics of T cell-mediated cytolysis and for heterogeneity of lytic rate. Journal of Immunology 123: 2870–7.
3. Zagury D, Bernard J, Jeannesson P, Thiernesse N, Cerottini JC, (1979) Studies on the Mechanism of T Cell-Mediated Lysis at the Single Effector Cell Level: I. Kinetic Analysis of Lethal Hits and Target Cell Lysis in Multicellular Conjugates. Journal of Immunology 123: 1604–1609.
4. Perelson AS, Bell GI, (1982) Delivery of lethal hits by cytotoxic T lymphocytes in multicellular conjugates occurs sequentially but at random times. J Immunol 129: 2796–801.
5. Macken CA, Perelson AS, (1984) A multistage model for the action of cytotoxic T lymphocytes in multicellular conjugates. J Immunol 132: 1614–24.
6. Perelson AS, Macken CA, Grimm EA, Roos LS, Bonavida B, (1984) Mechanism of cell-mediated cytotoxicity at the single cell level. VIII. Kinetics of lysis of target cells bound by more than one cytotoxic T lymphocyte. J Immunol 132: 2190–8.
7. Perelson AS, Macken CA, (1985) Quantitative models for the kinetics of cell-mediated cytotoxicity at the single cell level. Adv Exp Med Biol 184: 551–61.
8. Perez P, Bluestone JA, Stephany DA, Segal DM, (1985) Quantitative measurements of the specificity and kinetics of conjugate formation between cloned cytotoxic T lymphocytes and splenic target cells by dual parameter flow cytometry. Journal of immunology (Baltimore, Md: 1950) 134: 478–85.
9. Poe M, Wu JK, Talento A, Koo GC, (1996) CTL lysis: there is a hyperbolic relation of killing rate to exocytosable granzyme A for highly cytotoxic murine cytotoxic T lymphocytes. Journal of immunological methods 192: 37–41.
10. Wiedemann A, Depoil D, Faroudi M, Valitutti S, (2006) Cytotoxic T lymphocytes kill multiple targets simultaneously via spatiotemporal uncoupling of lytic and stimulatory synapses. Proceedings of the National Academy of Sciences of the United States of America 103: 10985–90.
11. Regoes RR, Barber DL, Ahmed R, Antia R, (2007) Estimation of the rate of killing by cytotoxic T lymphocytes in vivo. Proc Natl Acad Sci U S A 104: 1599–603.
12. Yates A, Graw F, Barber DL, Ahmed R, Regoes RR, et al. (2007) Revisiting estimates of CTL killing rates in vivo. PLoS One 2: e1301.
13. Ganusov VV, De Boer RJ, (2008) Estimating in vivo death rates of targets due to CD8 T-cell-mediated killing. J Virol 82: 11749–57.
14. Graw F, Regoes RR, (2009) Investigating CTL mediated killing with a 3D cellular automaton. PLoS Comput Biol 5: e1000466.
15. Beal AM, Anikeeva N, Varma R, Cameron TO, Vasiliver-Shamis G, et al. (2009) Kinetics of early T cell receptor signaling regulate the pathway of lytic granule delivery to the secretory domain. Immunity 31: 632–42.
16. Ganusov VV, Lukacher AE, Byers AM, (2010) Persistence of viral infection despite similar killing efficacy of antiviral CD8(+) T cells during acute and chronic phases of infection. Virology 405: 193–200.
17. Budhu S, Loike JD, Pandolfi A, Han S, Catalano G, et al. (2010) CD8+ T cell concentration determines their efficiency in killing cognate antigen-expressing syngeneic mammalian cells in vitro and in mouse tissues. J Exp Med 207: 223–35.
18. Graw F, Richter K, Oxenius A, Regoes RR, (2011) Comparison of cytotoxic T lymphocyte efficacy in acute and persistent lymphocytic choriomeningitis virus infection. Proc Biol Sci 278: 3395–402.
19. Ganusov VV, Barber DL, De Boer RJ, (2011) Killing of targets by CD8 T cells in the mouse spleen follows the law of mass action. PLoS One 6: e15959.
20. Regoes RR, Yates A, Antia R, (2007) Mathematical models of cytotoxic T-lymphocyte killing. Immunol Cell Biol 85: 274–9.
21. Barchet W, Oehen S, Klenerman P, Wodarz D, Bocharov G, et al. (2000) Direct quantitation of rapid elimination of viral antigen-positive lymphocytes by antiviral CD8(+) T cells in vivo. Eur J Immunol 30: 1356–63.
22. Yates AJ, Van Baalen M, Antia R, (2011) Virus replication strategies and the critical CTL numbers required for the control of infection. PLoS Comput Biol 7: e1002274.
23. Valitutti S, Müller S, Cella M, Padovan E, Lanzavecchia A, (1995) Serial triggering of many T-cell receptors by a few peptide-MHC complexes. Nature 375: 148–51.
24. Purbhoo MA, Irvine DJ, Huppa JB, Davis MM, (2004) T cell killing does not require the formation of a stable mature immunological synapse. Nat Immunol 5: 524–30.
25. Burnham KP, Anderson DR (2002) Model Selection and Multimodel Inference. Springer, second edition.
26. Foley MH, Forcier T, McAndrew E, Gonzalez M, Chen H, et al. (2014) High avidity CD8+ T cells efficiently eliminate motile hiv-infected targets and execute a locally focused program of anti-viral function. PLoS One 9: e87873.
27. Mempel TR, Pittet MJ, Khazaie K, Weninger W, Weissleder R, et al. (2006) Regulatory T cells reversibly suppress cytotoxic T cell function independent of effector differentiation. Immunity 25: 129–41.
28. Ganusov VV, Auerbach J, (2014) Mathematical modeling reveals kinetics of lymphocyte recirculation in the whole organism. PLoS Comput Biol 10: e1003586.
29. Steiniger B (2001) Spleen, John Wiley & Sons, Ltd. doi:10.1038/npg.els.0000900.
30. Bajénoff M, Glaichenhaus N, Germain RN, (2008) Fibroblastic reticular cells guide T lymphocyte entry into and migration within the splenic T cell zone. J Immunol 181: 3947–54.
31. van der Burg SH, Visseren MJ, Brandt RM, Kast WM, Melief CJ, (1996) Immunogenicity of peptides bound to MHC class I molecules depends on the MHC-peptide complex stability. J Immunol 156: 3308–14.
32. Busch DH, Pamer EG, (1998) MHC class I/peptide stability: implications for immunodominance, in vitro proliferation, and diversity of responding CTL. J Immunol 160: 4441–8.
33. Henrickson SE, Mempel TR, Mazo IB, Liu B, Artyomov MN, et al. (2008) T cell sensing of antigen dose governs interactive behavior with dendritic cells and sets a threshold for T cell activation. Nat Immunol 9: 282–91.
34. Jenkins MR, Tsun A, Stinchcombe JC, Griffiths GM, (2009) The strength of T cell receptor signal controls the polarization of cytotoxic machinery to the immunological synapse. Immunity 31: 621–31.
35. Barber DL, Wherry EJ, Ahmed R, (2003) Cutting edge: rapid in vivo killing by memory CD8 T cells. J Immunol 171: 27–31.
36. Byers AM, Kemball CC, Moser JM, Lukacher AE, (2003) Cutting edge: rapid in vivo CTL activity by polyoma virus-specigic effector and memory CD8+ T cells. J Immunol 171: 17–21.
37. Breart B, Lemaître F, Celli S, Bousso P, (2008) Two-photon imaging of intratumoral CD8+ T cell cytotoxic activity during adoptive T cell therapy in mice. J Clin Invest 118: 1390–7.
38. Jung YW, Rutishauser RL, Joshi NS, Haberman AM, Kaech SM, (2010) Differential localization of effector and memory CD8 T cell subsets in lymphoid organs during acute viral infection. J Immunol 185: 5315–25.
39. Christinck ER, Luscher MA, Barber BH, Williams DB, (1991) Peptide binding to class I MHC on living cells and quantitation of complexes required for CTL lysis. Nature 352: 67–70.
40. Sykulev Y, Joo M, Vturina I, Tsomides TJ, Eisen HN, (1996) Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T cell response. Immunity 4: 565–71.
41. Guidotti LG, Chisari FV, (2001) Noncytolytic control of viral infections by the innate and adaptive immune response. Annu Rev Immunol 19: 65–91.
42. DeVico AL, Gallo RC, (2004) Control of HIV-1 infection by soluble factors of the immune response. Nat Rev Microbiol 2: 401–13.
43. Perelson AS, (2002) Modelling viral and immune system dynamics. Nat Rev Immunol 2: 28–36.
44. Wolfram Research, Inc (2012) Mathematica 9.0. Champaign, Illinois.
45. R Development Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org.