Abstract
Mounting a protective immune response is critically dependent on the orchestrated movement of cells within lymphoid organs. We report here the visualization, using major histocompatability complex class I tetramers, of the CD8-positive (CD8) T cell response in the spleens of mice to Listeria monocytogenes infection. A multistage pathway was revealed that included initial activation at the borders of the B and T cell zones followed by cluster formation with antigenpresenting cells leading to CD8 T cell exit to the red pulp via bridging channels. Strikingly, many memory CD8 T cells localized to the B cell zones and, when challenged, underwent rapid migration to the T cell zones where proliferation occurred, followed by egress via bridging channels in parallel with the primary response. Thus, the ability to track endogenous immune responses has uncovered both distinct and overlapping mechanisms and anatomical locations driving primary and secondary immune responses.
MeSH Terms
Animals
Antigen-Presenting Cells/immunology
Antigens, CD/analysis
B-Lymphocytes/immunology
CD8 Antigens/analysis
CD8-Positive T-Lymphocytes/cytology,immunology,physiology
Cell Movement
Dendritic Cells/immunology,physiology
Fluorescent Dyes
Histocompatibility Antigens Class I
Immunologic Memory
Kinetics
Listeria monocytogenes/immunology
Listeriosis/immunology
Lymphocyte Activation
Mice
Mice, Inbred C57BL
Microscopy, Confocal
Receptors, Antigen, T-Cell/analysis
Spleen/cytology,immunology
Staining and Labeling
T-Lymphocyte Subsets/cytology,immunology,physiology
Chemicals
Antigens, CD
CD8 Antigens
Fluorescent Dyes
Histocompatibility Antigens Class I
Receptors, Antigen, T-Cell
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Khanna Kamal M
Department of Immunology, University of Connecticut, Farmington, CT 06030, U.S.A.
McNamara Jeffery T
Lefrançois Leo
References (20)
20 references, click to expand
-
T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases.
Nature. 2004 Jan 8;427(6970):154-9
PMID: 14712275
-
Distinct migration patterns of naive and effector CD8 T cells in the spleen: correlation with CCR7 receptor expression and chemokine reactivity.
Eur J Immunol. 1999 Nov;29(11):3562-70
PMID: 10556810
-
Competition for antigen determines the stability of T cell-dendritic cell interactions during clonal expansion.
Proc Natl Acad Sci U S A. 2007 Mar 13;104(11):4553-8
PMID: 17360562
-
Constitutive expression of CCR7 directs effector CD8 T cells into the splenic white pulp and impairs functional activity.
J Immunol. 2004 Sep 1;173(5):3013-9
PMID: 15322160
-
Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody.
Immunity. 1997 Jun;6(6):715-26
PMID: 9208844
-
Cutting edge: In situ tetramer staining of antigen-specific T cells in tissues.
J Immunol. 2000 Jul 15;165(2):613-7
PMID: 10878330
-
Lymphocyte circulation in the spleen. Marginal zone bridging channels and their possible role in cell traffic.
Immunology. 1973 Jan;24(1):93-107
PMID: 4539831
-
Molecular anatomy of antigen-specific CD8(+) T cell engagement and synapse formation in vivo.
Nat Immunol. 2002 Oct;3(10):918-25
PMID: 12352968
-
Structure and function of the spleen.
Nat Rev Immunol. 2005 Aug;5(8):606-16
PMID: 16056254
-
CD8 T cell recall responses are regulated by the tissue tropism of the memory cell and pathogen.
J Immunol. 2006 Nov 15;177(10):6738-46
PMID: 17082587
-
Dynamic regulation of IFN-gamma signaling in antigen-specific CD8+ T cells responding to infection.
J Immunol. 2005 Jun 1;174(11):6791-802
PMID: 15905520
-
Naïve CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation.
Nat Immunol. 2001 May;2(5):423-9
PMID: 11323696
-
Organ-specific regulation of the CD8 T cell response to Listeria monocytogenes infection.
J Immunol. 2001 Mar 1;166(5):3402-9
PMID: 11207297
-
Initial T cell frequency dictates memory CD8+ T cell lineage commitment.
Nat Immunol. 2005 Aug;6(8):793-9
PMID: 16025119
-
The clone size of peripheral CD8 T cells is regulated by TCR promiscuity.
J Exp Med. 2006 Jul 10;203(7):1643-9
PMID: 16769997
-
Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naïve cells.
Nat Immunol. 2001 May;2(5):415-22
PMID: 11323695
-
Dynamics of CD8+ T cell priming by dendritic cells in intact lymph nodes.
Nat Immunol. 2003 Jun;4(6):579-85
PMID: 12730692
-
Herpes simplex virus-specific memory CD8+ T cells are selectively activated and retained in latently infected sensory ganglia.
Immunity. 2003 May;18(5):593-603
PMID: 12753737
-
Migration of B lymphocytes in lymphoid organs of lethally irradiated, thymocyte-reconstituted mice.
Cell Tissue Res. 1980;212(3):497-508
PMID: 6970085
-
Two-photon imaging of lymphocyte motility and antigen response in intact lymph node.
Science. 2002 Jun 7;296(5574):1869-73
PMID: 12016203