Initial T cell receptor transgenic cell precursor frequency dictates critical aspects of the CD8(+) T cell response to infection.

Adoptive-transfer experiments with relatively large input numbers ( approximately 10(6)) of T cell receptor-transgenic (TCR-tg) T cells are widely used to model endogenous T cell responses to infection or immunization. We show that input numbers of naive TCR-tg T cells sufficient to squelch the endogenous response to the same epitope substantially alter the kinetics, proliferative expansion, phenotype, and efficiency of memory generation by the TCR-tg T cells in response to infection. Thus, responses from nonphysiologic input numbers of TCR-tg T cells fail to accurately mimic the endogenous T cell response. Importantly, seeding as few as approximately 10-50 TCR-tg T cells, which constitute a fraction of the endogenous repertoire, allowed vigorous proliferation and analysis of TCR-tg cells after infection in a scenario representing normal physiology for any individual TCR. These data strongly suggest that modeling the endogenous T cell response with TCR-tg cells will require every effort to approximate the endogenous precursor frequency.

[1]  Antonio Lanzavecchia,et al.  Central memory and effector memory T cell subsets: function, generation, and maintenance. , 2004, Annual review of immunology.

[2]  Rustom Antia,et al.  Estimating the Precursor Frequency of Naive Antigen-specific CD8 T Cells , 2002, The Journal of experimental medicine.

[3]  S. Tonegawa,et al.  Evidence for a differential avidity model of T cell selection in the thymus , 1994, Cell.

[4]  L. Lefrançois,et al.  Preferential Localization of Effector Memory Cells in Nonlymphoid Tissue , 2001, Science.

[5]  Alan D. Roberts,et al.  Differential contributions of central and effector memory T cells to recall responses , 2005, The Journal of experimental medicine.

[6]  E. Wherry,et al.  Vaccines: Effector and memory T-cell differentiation: implications for vaccine development , 2002, Nature Reviews Immunology.

[7]  J. Altman,et al.  Individual variations in the murine T cell response to a specific peptide reflect variability in naive repertoires. , 1998, Immunity.

[8]  J. Harty,et al.  Programming, demarcating, and manipulating CD8+ T‐cell memory , 2006, Immunological reviews.

[9]  Peter Jensen,et al.  CD8αα-Mediated Survival and Differentiation of CD8 Memory T Cell Precursors , 2004, Science.

[10]  Kristin A. Hogquist,et al.  T cell receptor antagonist peptides induce positive selection , 1994, Cell.

[11]  J. Altman,et al.  Differentiating between Memory and Effector Cd8 T Cells by Altered Expression of Cell Surface O-Glycans , 2000, The Journal of experimental medicine.

[12]  D. Busch,et al.  Coordinate regulation of complex T cell populations responding to bacterial infection. , 1998, Immunity.

[13]  A. Khoruts,et al.  Naïve and Memory CD4+ T Cell Survival Controlled by Clonal Abundance , 2006, Science.

[14]  J. Harty,et al.  Programmed contraction of CD8+ T cells after infection , 2002, Nature Immunology.

[15]  R. Ahmed,et al.  Similarities and differences in CD4+ and CD8+ effector and memory T cell generation , 2003, Nature Immunology.

[16]  Susan M. Kaech,et al.  Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naïve cells , 2001, Nature Immunology.

[17]  Susan M. Kaech,et al.  Molecular and Functional Profiling of Memory CD8 T Cell Differentiation , 2002, Cell.

[18]  Rustom Antia,et al.  Lineage relationship and protective immunity of memory CD8 T cell subsets , 2003, Nature Immunology.

[19]  Philippa Marrack,et al.  T cells down-modulate peptide-MHC complexes on APCs in vivo , 2002, Nature Immunology.

[20]  E. Wherry,et al.  Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells , 2003, Nature Immunology.

[21]  J. Harty,et al.  CD8+ T cell contraction is controlled by early inflammation , 2004, Nature Immunology.

[22]  P. Doherty,et al.  Quantification of Repertoire Diversity of Influenza-Specific Epitopes with Predominant Public or Private TCR Usage1 , 2006, The Journal of Immunology.

[23]  Marie-Pierre Hardy,et al.  IL-7 Receptor Expression Levels Do Not Identify CD8+ Memory T Lymphocyte Precursors following Peptide Immunization1 , 2005, The Journal of Immunology.

[24]  E. Wherry,et al.  Memory CD8 T-Cell Differentiation during Viral Infection , 2004, Journal of Virology.

[25]  Emmanuel Beaudoing,et al.  Size Estimate of the αβ TCR Repertoire of Naive Mouse Splenocytes1 , 2000, The Journal of Immunology.

[26]  Hermann Wagner,et al.  Selective expression of IL-7 receptor on memory T cells identifies early CD40L-dependent generation of distinct CD8+ memory T cell subsets. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[27]  J. Harty,et al.  Regulation of CD8+ T Cells Undergoing Primary and Secondary Responses to Infection in the Same Host1 , 2003, The Journal of Immunology.

[28]  S. Perlman,et al.  Very Diverse CD8 T Cell Clonotypic Responses after Virus Infections1 , 2004, The Journal of Immunology.

[29]  Leo Lefrançois,et al.  Initial T cell frequency dictates memory CD8+ T cell lineage commitment , 2005, Nature Immunology.

[30]  R. Dutton,et al.  Cutting Edge: Regulation of CD8+ T Cell Effector Population Size1 , 2004, The Journal of Immunology.

[31]  S. Jameson,et al.  Interleukin-7 mediates the homeostasis of naïve and memory CD8 T cells in vivo , 2000, Nature Immunology.

[32]  D. Loh,et al.  Visualization of peptide-specific T cell immunity and peripheral tolerance induction in vivo. , 1994, Immunity.

[33]  Hao Shen,et al.  Cutting Edge: CD4 and CD8 T Cells Are Intrinsically Different in Their Proliferative Responses1 , 2002, The Journal of Immunology.

[34]  J. Altman,et al.  Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. , 1998, Immunity.

[35]  J. Rose,et al.  Generation of mucosal cytotoxic T cells against soluble protein by tissue-specific environmental and costimulatory signals. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[36]  J. Harty,et al.  CD8+ T cell effector mechanisms in resistance to infection. , 2000, Annual review of immunology.

[37]  J. Harty,et al.  Accelerated CD8+ T-cell memory and prime-boost response after dendritic-cell vaccination , 2005, Nature Medicine.

[38]  M. Bevan,et al.  Massive expansion of antigen-specific CD8+ T cells during an acute virus infection. , 1998, Immunity.

[39]  E. Pamer,et al.  Rapid Development of T Cell Memory1 , 2004, The Journal of Immunology.

[40]  W. Heath,et al.  Cross-presentation, dendritic cells, tolerance and immunity. , 2001, Annual review of immunology.