Modeling of influenza-specific CD8 + T cells during the primary response indicates that the spleen is a major source of effectors

Journal of Immunology

Volumn 187, Issue 9, 2011, Pages 4474-4482

  Wu, Hulin ^a   Kumar, Arun ^a   Miao, Hongyu ^a   Holden Wiltse, Jeanne ^a   Mosmann, Timothy R ^a   Livingstone, Alexandra M ^a   Belz, Gabrielle T ^b   Perelson, Alan S ^c   Zand, Martin S ^c   Topham, David J ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c LOS ALAMOS NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; ARTICLE; BIOMECHANICS; CD8+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELL COUNT; CELL EXPANSION; CELL KINETICS; CONTROLLED STUDY; EFFECTOR CELL; EXPERIMENTAL STUDY; FEMALE; IMMUNE RESPONSE; INFLUENZA A; LUNG; LYMPH NODE; LYMPHOCYTE MIGRATION; MATHEMATICAL MODEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROCESS DEVELOPMENT; SPLEEN; STATISTICAL ANALYSIS; TISSUE SPECIFICITY; VIRUS LOAD;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; DISEASE MODELS, ANIMAL; FEMALE; INFLUENZA A VIRUS, H3N2 SUBTYPE; LUNG; LYMPH NODES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MODELS, IMMUNOLOGICAL; ORTHOMYXOVIRIDAE INFECTIONS; SPLEEN;

EID: 80555154911     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101443     Document Type: Article

References (63)

1. Doherty, P. C., D. J. Topham, R. A. Tripp, R. D. Cardin, J. W. Brooks, and P. G. Stevenson. 1997. Effector CD4+ and CD8+ T-cell mechanisms in the control of respiratory virus infections. Immunol. Rev. 159: 105-117. (Pubitemid 27499863)
2. Topham, D. J., R. A. Tripp, and P. C. Doherty. 1997. CD8+ T cells clear influenza virus by perforin or Fas-dependent processes. J. Immunol. 159: 5197-5200. (Pubitemid 127470043)
3. Topham, D. J., and P. C. Doherty. 1998. Clearance of an influenza A virus by CD4+ T cells is inefficient in the absence of B cells. J. Virol. 72: 882-885. (Pubitemid 28048918)
4. Castrucci, M. R., and Y. Kawaoka. 1993. Biologic importance of neuraminidase stalk length in influenza A virus. J. Virol. 67: 759-764. (Pubitemid 23032053)
5. Gao, P., S. Watanabe, T. Ito, H. Goto, K. Wells, M. McGregor, A. J. Cooley, and Y. Kawaoka. 1999. Biological heterogeneity, including systemic replication in mice, of H5N1 influenza A virus isolates from humans in Hong Kong. J. Virol. 73: 3184-3189. (Pubitemid 29135710)
6. Tumpey, T. M., C. F. Basler, P. V. Aguilar, H. Zeng, A. Solórzano, D. E. Swayne, N. J. Cox, J. M. Katz, J. K. Taubenberger, P. Palese, and A. García-Sastre. 2005. Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science 310: 77-80. (Pubitemid 41434537)
7. Lazarowitz, S. G., and P. W. Choppin. 1975. Enhancement of the infectivity of influenza A and B viruses by proteolytic cleavage of the hemagglutinin polypeptide. Virology 68: 440-454.
8. Sun, X., L. V. Tse, A. D. Ferguson, and G. R. Whittaker. 2010. Modifications to the hemagglutinin cleavage site control the virulence of a neurotropic H1N1 influenza virus. J. Virol. 84: 8683-8690.
9. Belz, G. T., C. M. Smith, L. Kleinert, P. Reading, A. Brooks, K. Shortman, F. R. Carbone, and W. R. Heath. 2004. Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc. Natl. Acad. Sci. USA 101: 8670-8675. (Pubitemid 38745829)
10. Belz, G. T., C.M. Smith, D. Eichner, K. Shortman, G. Karupiah, F. R. Carbone, and W. R. Heath. 2004. Cutting edge: conventional CD8 alpha+ dendritic cells are generally involved in priming CTL immunity to viruses. J. Immunol. 172: 1996-2000. (Pubitemid 38182342)
11. Bocharov, G. A., and A. A. Romanyukha. 1994. Mathematical model of antiviral immune response. III. Influenza A virus infection. J. Theor. Biol. 167: 323-360. (Pubitemid 24187094)
12. Smith, A. M., and A. S. Perelson. 2011. Influenza A virus infection kinetics: quantitative data and models. Wiley Interdiscip. Rev. Syst. Biol. Med. 3: 429-445.
13. Perelson, A. S. 2002. Modelling viral and immune system dynamics. Nat. Rev. Immunol. 2: 28-36. (Pubitemid 37328773)
14. Handel, A., and R. Antia. 2008. A simple mathematical model helps to explain the immunodominance of CD8 T cells in influenza A virus infections. J. Virol. 82: 7768-7772.
15. Beauchemin, C., J. Samuel, and J. Tuszynski. 2005. A simple cellular automaton model for influenza A viral infections. J. Theor. Biol. 232: 223-234. (Pubitemid 39458050)
16. Möhler, L., D. Flockerzi, H. Sann, and U. Reichl. 2005. Mathematical model of influenza A virus production in large-scale microcarrier culture. Biotechnol. Bioeng. 90: 46-58. (Pubitemid 40547038)
17. Baccam, P., C. Beauchemin, C. A. Macken, F. G. Hayden, and A. S. Perelson. Kinetics of influenza A virus infection in humans. J. Virol. 80: 7590-7599.
18. Hancioglu, B., D. Swigon, and G. Clermont. 2007. A dynamical model of human immune response to influenza A virus infection. J. Theor. Biol. 246: 70-86. (Pubitemid 46566369)
19. Lee, H. Y., D. J. Topham, S. Y. Park, J. Hollenbaugh, J. Treanor, T. R. Mosmann, X. Jin, B. M. Ward, H. Miao, J. Holden-Wiltse, et al. 2009. Simulation and prediction of the adaptive immune response to influenza A virus infection. J. Virol. 83: 7151-7165.
20. Miao, H., J. A. Hollenbaugh, M. S. Zand, J. Holden-Wiltse, T. R. Mosmann, A. S. Perelson, H. Wu, and D. J. Topham. 2010. Quantifying the early immune response and adaptive immune response kinetics in mice infected with influenza A virus. J. Virol. 84: 6687-6698.
21. Belz, G. T., G. M. Behrens, C. M. Smith, J. F. Miller, C. Jones, K. Lejon, C. G. Fathman, S. N. Mueller, K. Shortman, F. R. Carbone, and W. R. Heath. The CD8alpha(+) dendritic cell is responsible for inducing peripheral selftolerance to tissue-associated antigens. J. Exp. Med. 196: 1099-1104.
22. Belz, G. T., F. R. Carbone, and W. R. Heath. 2002. Cross-presentation of antigens by dendritic cells. Crit. Rev. Immunol. 22: 439-448. (Pubitemid 36548953)
23. Belz, G. T. 2010. Direct ex vivo activation of T cells for analysis of dendritic cells antigen presentation. Methods Mol. Biol. 595: 351-369.
24. Polakos, N. K., I. Klein, M. V. Richter, D. M. Zaiss, M. Giannandrea, I. N. Crispe, and D. J. Topham. 2007. Early intrahepatic accumulation of CD8+ T cells provides a source of effectors for nonhepatic immune responses. J. Immunol. 179: 201-210. (Pubitemid 46986535)
25. Miao, H., X. Xia, A. S. Perelson, and H. Wu. 2011. On identifiability of nonlinear ODE models with applications in viral dynamics. SIAM Rev. 53: 3-39.
26. Xia, X., and C. H. Moog. 2003. Identifiability of nonlinear systems with application to HIV/AIDS models. Automatic Control. IEEE Trans. Automatic Control 48: 330-336.
27. Miao, H., C. Dykes, L. M. Demeter, J. Cavenaugh, S. Y. Park, A. S. Perelson, and H. Wu. 2008. Modeling and estimation of kinetic parameters and replicative fitness of HIV-1 from flow-cytometry-based growth competition experiments. Bull. Math. Biol. 70: 1749-1771.
28. Miao, H., C. Dykes, L. M. Demeter, and H. Wu. 2009. Differential equation modeling of HIV viral fitness experiments: model identification, model selection, and multimodel inference. Biometrics 65: 292-300.
29. Chen, J., and H. Wu. 2008. Estimation of time-varying parameters in deterministic dynamic models with application to HIV infections. Statistica Sinica 18: 987-1006.
30. Liang, H., H. Miao, and H. Wu. 2010. Estimation of constant and time-varying dynamic parameters of HIV infection in a nonlinear differential equation model. Ann. Appl. Stat. 4: 460-483.
31. Liang, H., and H. Wu. 2008. Parameter estimation for differential equation models using a framework of measurement error in regression model. J. Am. Stat. Assoc. 103: 1570-1583.
32. Xue, H., H. Miao, and H. Wu. 2010. Sieve estimation of constant and timevarying coefficients in nonlinear ordinary differential equation models by considering both numerical error and measurement error. Ann. Stat. 38: 2351-2387.
33. de Boor, C. 1978. A Practical Guide to Splines. Springer-Verlag, Berlin.
34. Akaike, H. 1973. Information theory and an extension of the maximum likehood principle. In Second International Symposium on Information Theory. B. Petrov, and F. Csáki, eds. Akadémiai Kiadó, Budapest, p. 267-281.
35. Burnham, K. P., and D. R. Anderson. 2004. Multimodel inference: understanding AIC and BIC in model selection. Sociol. Methods Res. 33: 261-304. (Pubitemid 39519124)
36. Flynn, K. J., G. T. Belz, J. D. Altman, R. Ahmed, D. L. Woodland, and P. C. Doherty. 1998. Virus-specific CD8+ T cells in primary and secondary influenza pneumonia. Immunity 8: 683-691. (Pubitemid 28294515)
37. Flynn, K. J., J. M. Riberdy, J. P. Christensen, J. D. Altman, and P. C. Doherty. In vivo proliferation of naïve and memory influenza-specific CD8(+) T cells. Proc. Natl. Acad. Sci. USA 96: 8597-8602.
38. Tripp, R. A., S. Hou, A. McMickle, J. Houston, and P. C. Doherty. 1995. Recruitment and proliferation of CD8+ T cells in respiratory virus infections. J. Immunol. 154: 6013-6021.
39. Tripp, R. A., J. M. Lahti, and P. C. Doherty. 1995. Laser light suicide of proliferating virus-specific CD8+ T cells in an in vivo response. J. Immunol. 155: 3719-3721.
40. Yoon, H., T. S. Kim, and T. J. Braciale. 2010. The cell cycle time of CD8+ T cells responding in vivo is controlled by the type of antigenic stimulus. PLoS ONE 5: e15423.
41. D'Souza,W. N., and L. Lefrançois. 2003. IL-2 is not required for the initiation of CD8 T cell cycling but sustains expansion. J. Immunol. 171: 5727-5735. (Pubitemid 37467187)
42. D'Souza, W. N., K. S. Schluns, D. Masopust, and L. Lefrançois. 2002. Essential role for IL-2 in the regulation of antiviral extralymphoid CD8 T cell responses. J. Immunol. 168: 5566-5572. (Pubitemid 34556136)
43. Whitmire, J. K., N. Benning, and J. L. Whitton. 2006. Precursor frequency, nonlinear proliferation, and functional maturation of virus-specific CD4+ T cells. J. Immunol. 176: 3028-3036.
44. Topham, D. J., M. R. Castrucci, F. S. Wingo, G. T. Belz, and P. C. Doherty. 2001. The role of antigen in the localization of naive, acutely activated, and memory CD8(+) T cells to the lung during influenza pneumonia. J. Immunol. 167: 6983-6990. (Pubitemid 33144193)
45. Chapman, T. J., M. R. Castrucci, R. C. Padrick, L. M. Bradley, and D. J. Topham. Antigen-specific and non-specific CD4+ T cell recruitment and proliferation during influenza infection. Virology 340: 296-306.
46. Masopust, D., V. Vezys, A. L. Marzo, and L. Lefrançois. 2001. Preferential localization of effector memory cells in nonlymphoid tissue. Science 291: 2413-2417. (Pubitemid 32231804)
47. Reinhardt, R. L., A. Khoruts, R. Merica, T. Zell, and M. K. Jenkins. 2001. Visualizing the generation of memory CD4 T cells in the whole body. Nature 410: 101-105. (Pubitemid 32225844)
48. Allan, W., Z. Tabi, A. Cleary, and P. C. Doherty. 1990. Cellular events in the lymph node and lung of mice with influenza. Consequences of depleting CD4+ T cells. J. Immunol. 144: 3980-3986. (Pubitemid 20171213)
49. Butcher, E. C., and L. J. Picker. 1996. Lymphocyte homing and homeostasis. Science 272: 60-66. (Pubitemid 26110755)
50. Topham, D. J., and P. C. Doherty. 1998. Longitudinal analysis of the acute Sendai virus-specific CD4+ T cell response and memory. J. Immunol. 161: 4530-4535. (Pubitemid 28492023)
51. Lawrence, C. W., R. M. Ream, and T. J. Braciale. 2005. Frequency, specificity, and sites of expansion of CD8+ T cells during primary pulmonary influenza virus infection. J. Immunol. 174: 5332-5340. (Pubitemid 40593171)
52. Lawrence, C. W., and T. J. Braciale. 2004. Activation, differentiation, and migration of naive virus-specific CD8+ T cells during pulmonary influenza virus infection. J. Immunol. 173: 1209-1218. (Pubitemid 38924298)
53. Marshall, D. R., S. J. Turner, G. T. Belz, S. Wingo, S. Andreansky, M. Y. Sangster, J. M. Riberdy, T. Liu, M. Tan, and P. C. Doherty. 2001. Measuring the diaspora for virus-specific CD8+ T cells. Proc. Natl. Acad. Sci. USA 98: 6313-6318. (Pubitemid 32488236)
54. McGill, J., and K. L. Legge. 2009. Cutting edge: contribution of lung-resident T cell proliferation to the overall magnitude of the antigen-specific CD8 T cell response in the lungs following murine influenza virus infection. J. Immunol. 183: 4177-4181.
55. Dolfi, D. V., P. A. Duttagupta, A. C. Boesteanu, Y. M. Mueller, C. H. Oliai, A. B. Borowski, and P. D. Katsikis. 2011. Dendritic cells and CD28 costimulation are required to sustain virus-specific CD8+ T cell responses during the effector phase in vivo. J. Immunol. 186: 4599-4608.
56. Tripp, R. A., D. J. Topham, S. R. Watson, and P. C. Doherty. 1997. Bone marrow can function as a lymphoid organ during a primary immune response under conditions of disrupted lymphocyte trafficking. J. Immunol. 158: 3716-3720. (Pubitemid 127488726)
57. Di Rosa, F., and R. Pabst. 2005. The bone marrow: a nest for migratory memory T cells. Trends Immunol. 26: 360-366. (Pubitemid 40835841)
58. Feuerer, M., P. Beckhove, N. Garbi, Y. Mahnke, A. Limmer, M. Hommel, G. J. Hämmerling, B. Kyewski, A. Hamann, V. Umansky, and V. Schirrmacher. Bone marrow as a priming site for T-cell responses to blood-borne antigen. Nat. Med. 9: 1151-1157.
59. Mercado, R., S. Vijh, S. E. Allen, K. Kerksiek, I. M. Pilip, and E. G. Pamer. Early programming of T cell populations responding to bacterial infection. J. Immunol. 165: 6833-6839.
60. Maxwell, J. R., R. J. Rossi, S. J. McSorley, and A. T. Vella. 2004. T cell clonal conditioning: a phase occurring early after antigen presentation but before clonal expansion is impacted by Toll-like receptor stimulation. J. Immunol. 172: 248-259. (Pubitemid 38020478)
61. Lund, F. E., S. Partida-Sánchez, B. O. Lee, K. L. Kusser, L. Hartson, R. J. Hogan, D. L. Woodland, and T. D. Randall. 2002. Lymphotoxin-alphadeficient mice make delayed, but effective, T and B cell responses to influenza. J. Immunol. 169: 5236-5243. (Pubitemid 35217195)
62. Yap, K. L., and G. L. Ada. 1978. Cytotoxic T cells in the lungs of mice infected with an influenza A virus. Scand. J. Immunol. 7: 73-80. (Pubitemid 8295415)
63. Veiga-Fernandes, H., U. Walter, C. Bourgeois, A. McLean, and B. Rocha. 2000. Response of naïve and memory CD8+ T cells to antigen stimulation in vivo. Nat. Immunol. 1: 47-53.