Killing of targets by CD8+ T cells in the mouse Spleen follows the law of mass action

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Ganusov, Vitaly V ^a   Barber, Daniel L ^b   de Boer, Rob J ^c  

^a UNIVERSITY OF TENNESSEE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD8+ T LYMPHOCYTE; CELL DEATH; CELL DENSITY; CELL DIFFERENTIATION; CELL KILLING; CELL LOSS; CELL SPECIFICITY; CONTROLLED STUDY; EFFECTOR CELL; GROWTH INHIBITION; IMMUNE RESPONSE; LYMPHOCYTE COUNT; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MATHEMATICAL MODEL; MEMORY CELL; MOUSE; NONHUMAN; SPLEEN; TARGET CELL; VIROGENESIS; VIRUS INFECTION; VIRUS REPLICATION; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; CYTOTOXICITY; IMMUNOLOGICAL MEMORY; IMMUNOLOGY;

LYMPHOCYTIC CHORIOMENINGITIS VIRUS;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CYTOTOXICITY, IMMUNOLOGIC; IMMUNOLOGIC MEMORY; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MODELS, IMMUNOLOGICAL; SPLEEN; T-CELL ANTIGEN RECEPTOR SPECIFICITY;

EID: 79551573816     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015959     Document Type: Article

References (51)

1. Pantaleo G, Koup R (2004) Correlates of immune protection in HIV-1 infection: what we know, what we don't know, what we should know. NatMed 10: 806-10.
2. Plotkin SA (2008) Vaccines: correlates of vaccine-induced immunity. Clin Infect Dis 47: 401-9.
3. Precopio ML, Betts MR, Parrino J, Price DA, Gostick E, et al. (2007) Immunization with vaccinia virus induces polyfunctional and phenotypically distinctive CD8(+) T cell responses. J Exp Med 204: 1405-16.
4. Darrah PA, Patel DT, De Luca PM, Lindsay RW, Davey DF, et al. (2007) Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med 13: 843-50.
5. Liu J, O'Brien KL, Lynch DM, Simmons NL, La Porte A, et al. (2009) Immune control of an SIV challenge by a T-cell-based vaccine in rhesus monkeys. Nature 457: 87-91.
6. Rehr M, Cahenzli J, Haas A, Price DA, Gostick E, et al. (2008) Emergence of polyfunctional CD8+ T cells after prolonged suppression of human immunodeficiency virus replication by antiretroviral therapy. J Virol 82: 3391-404.
7. Streeck H, Brumme ZL, Anastario M, Cohen KW, Jolin JS, et al. (2008) Antigen load and viral sequence diversification determine the functional profile of HIV-1-specific CD8+ T cells. PLoS Med 5: e100.
8. 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.
9. Blancou P, Chenciner N, Cumont MC, Wain-Hobson S, Hurtrel B, et al. (2001) The infiltration kinetics of simian immunodeficiency virus-specific T cells drawn to sites of high antigenic stimulation determines local in vivo viral escape. Proc Natl Acad Sci U S A 98: 13237-42.
10. Aichele P, Brduscha-Riem K, Oehen S, Odermatt B, Zinkernagel RM, et al. (1997) Peptide antigen treatment of naive and virus-immune mice: antigenspecific tolerance versus immunopathology. Immunity 6: 519-529.
11. Oehen S, Brduscha-Riem K (1998) Differentiation of naive CTL to effector and memory CTL: correlation of effector function with phenotype and cell division. J Immunol 161: 5338-5346.
12. 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: 1356-1363.
13. Mueller S, Jones C, Smith C, Heath W, Carbone F (2002) Rapid cytotoxic T lymphocyte activation occurs in the draining lymph nodes after cutaneous herpes simplex virus infection as a result of early antigen presentation and not the presence of virus. J Exp Med 195: 651-6.
14. Coles R, Mueller S, Heath W, Carbone F, Brooks A (2002) Progression of armed CTL from draining lymph node to spleen shortly after localized infection with herpes simplex virus 1. J Immunol 168: 834-8.
15. Byers A, Kemball C, Moser J, Lukacher A (2003) Cutting edge: rapid in vivo CTL activity by polyoma virus-specific effector and memory CD8+ T cells. J Immunol 171: 17-21.
16. Barber D, Wherry E, Ahmed R (2003) Cutting edge: rapid in vivo killing by memory CD8 T cells. J Immunol 171: 27-31.
17. Curtsinger J, Lins D, Mescher M (2003) Signal 3 determines tolerance versus full activation of naive CD8 T cells: dissociating proliferation and development of effector function. J Exp Med 197: 1141-51.
18. Hermans IF, Silk JD, Yang J, Palmowski MJ, Gileadi U, et al. (2004) The VITAL assay: a versatile fluorometric technique for assessing CTL- and NKTmediated cytotoxicity against multiple targets in vitro and in vivo. J Immunol Methods 285: 25-40.
19. Ingulli E (2007) Tracing Tolerance and Immunity In Vivo by CFSE-Labeling of Administered Cells. Methods Mol Biol 380: 365-376.
20. Regoes R, Barber D, Ahmed R, Antia R (2007) Estimation of the rate of killing by cytotoxic T lymphocytes in vivo. Proc Natl Acad Sci USA 104: 1599-1603.
21. 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.
22. Ganusov VV, De Boer RJ (2008) Estimating in vivo death rates of targets due to CD8 T-cell-mediated killing. J Virol 82: 11749-11757.
23. 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.
24. Schmidt NW, Podyminogin RL, Butler NS, Badovinac VP, Tucker BJ, et al. (2008) Memory CD8 T cell responses exceeding a large but definable threshold provide long-term immunity to malaria. Proc Natl Acad Sci U S A 105: 14017-22.
25. Hansen SG, Vieville C, Whizin N, Coyne-Johnson L, Siess DC, et al. (2009) Effector memory T cell responses are associated with protection of rhesus monkeys from mucosal simian immunodeficiency virus challenge. Nat Med 15: 293-9.
26. Kaech SM, Ahmed R (2001) Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat Immunol 2: 415-422.
27. Bates DM, Watts DG (1988) Nonlinear regression analysis and its applications. (John Wiles & Sons, Inc.).
28. De Boer RJ, Oprea M, Antia R, Murali-Krishna K, Ahmed R, et al. (2001) Recruitment times, proliferation, and apoptosis rates during the CD8(+) T-cell response to lymphocytic choriomeningitis virus. Journal of Virology 75: 10663-10669.
29. De Boer R, Homann D, Perelson A (2003) Different dynamics of CD4(+) and CD8(+) T cell responses during and after acute lymphocytic choriomeningitis virus infection. J Immunol 171: 3928-3935.
30. Ganusov V (2007) Discriminating between Different Pathways of Memory CD8+ T Cell Differentiation. J Immunol 179: 5006-5013.
31. Murali-Krishna K, Altman JD, Suresh M, Sourdive DJD, Zajac AJ, et al. (1998) Counting antigen-specific CD8+ T cells: A re-evaluation of bystander actiation during viral infection. Immunity 8: 177-187.
32. Homann D, Teyton L, Oldstone M (2001) Differential regulation of antiviral Tcell immunity results in stable CD8+ but declining CD4+ T-cell memory. Nat Med 7: 913-919.
33. Sykulev Y, Cohen RJ, Eisen HN (1995) The law of mass action governs antigenstimulated cytolytic activity of CD8+ cytotoxic T lymphocytes. Proc Natl Acad Sci U S A 92: 11990-2.
34. Ehl S, Klenerman P, Aichele P, Hengartner H, Zinkernagel R (1997) A functional and kinetic comparison of antiviral effector and memory cytotoxic T lymphocyte populations in vivo and in vitro. Eur J Immunol 27: 3404-13.
35. Bocharov G, Ludewig B, Bertoletti A, Klenerman P, Junt T, et al. (2004) Underwhelming the immune response: effect of slow virus growth on CD8+-Tlymphocyte responses. J Virol 78: 2247-54.
36. Althaus C, Ganusov V, De Boer R (2007) Dynamics of CD8+ T cell responses during acute and chronic lymphocytic choriomeningitis virus infection. J Immunol 179: 2944-2951.
37. Berger D, Homann D, Oldstone M (2000) Defining parameters for successful immunocytotherapy of persistent viral infection. Virology 266: 257-63.
38. Sekaly R (2008) The failed HIV Merck vaccine study: a step back or a launching point for future vaccine development? J Exp Med 205: 7-12.
39. De Boer R (2007) Understanding the failure of CD8+ T-cell vaccination against simian/human immunodeficiency virus. J Virol 81: 2838-48.
40. Chandrasekhar S (1943) Stochastic problems in physics and astronomy. Rev Mod Phys 15: 1-89.
41. Merrill SJ (1982) Foundations of the use of an enzyme-kinetic analogy in cellmediated cytotoxicity. Math Bio 62: 219-35.
42. Perelson A, Macken C, Grimm E, Roos L, 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.
43. Borghans J, de Boer R, Segel L (1996) Extending the quasi-steady state approximation by changing variables. Bull Math Biol 58: 43-63.
44. Graw F, Regoes RR (2009) Investigating CTL mediated killing with a 3D cellular automaton. PLoS Comput Biol 5: e1000466.
45. Bachmann MF, Barner M, Viola A, Kopf M (1999) Distinct kinetics of cytokine production and cytolysis in effector and memory T cells after viral infection. Eur J Immunol 29: 291-9.
46. Mempel T, Junt T, von Andrian U (2006) Rulers over randomness: stroma cells guide lymphocyte migration in lymph nodes. Immunity 25: 867-869.
47. Jenkins MR, La Gruta NL, Doherty PC, Trapani JA, Turner SJ, et al. (2009) Visualizing CTL activity for different CD8+ effector T cells supports the idea that lower TCR/epitope avidity may be advantageous for target cell killing. Cell Death Differ 16: 537-42.
48. Regner M, Pavlinovic L, Koskinen A, Young N, Trapani JA, et al. (2009) Cutting edge: Rapid and efficient in vivo cytotoxicity by cytotoxic T cells is independent of granzymes A and B. J Immunol 183: 37-40.
49. Kim S, Welsh R (2004) Comprehensive early and lasting loss of memory CD8 T cells and functional memory during acute and persistent viral infections. J Immunol 172: 3139-50.
50. Vezys V, Yates A, Casey KA, Lanier G, Ahmed R, et al. (2009) Memory CD8 Tcell compartment grows in size with immunological experience. Nature 457: 196-9.
51. Efron B, Tibshirani R (1993) An introduction to the bootstrap (Chapman & Hall, New York).