Abstract
This series of reviews examines the effect of differing tissue environments on the activity and functional capacity of cells in the immune system. From their origins as hematopoietic stem cells, throughout their development and as mature cells, cells of the immune system find themselves in distinct and highly specialized niches, and contact with antigen or inflammatory signals changes their phenotype, activity and trafficking. Two-photon microscopy has provided the first direct observations of living cells and their activation choreography in the tissue environment and will no doubt continue to provide greater understanding of cellular dynamics and immune function.
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References
Gowans, J.L. The recirculation of lymphocytes from blood to lymph in the rat. J. Physiol. (Lond.) 146, 54–69 (1959).
Gowans, J.L. & Knight, E.J. The route of re-circulation of lymphocytes in the rat. Proc. R. Soc. Lond. B 159, 257–282 (1964).
Howard, J.C., Hunt, S.V. & Gowans, J.L. Identification of marrow-derived and thymus-derived small lymphocytes in the lymphoid tissue and thoracic duct lymph of normal rats. J. Exp. Med. 135, 200–219 (1972).
Gutman, G.A. & Weissman, I.L. Lymphoid tissue architecture. Experimental analysis of the origin and distribution of T-cells and B-cells. Immunology 23, 465–479 (1972).
Weissman, I.L. Thymus cell migration. J. Exp. Med. 126, 291–304 (1967).
Scollay, R., Kochen, M., Butcher, E. & Weissman, I. Lyt markers on thymus cell migrants. Nature 276, 79–80 (1978).
Stamper, H.B., Jr. & Woodruff, J.J. Lymphocyte homing into lymph nodes: in vitro demonstration of the selective affinity of recirculating lymphocytes for high-endothelial venules. J. Exp. Med. 144, 828–833 (1976).
Gallatin, W.M., Weissman, I.L. & Butcher, E.C. A cell-surface molecule involved in organ-specific homing of lymphocytes. Nature 304, 30–34 (1983).
Cahalan, M.D., Parker, I., Wei, S.H. & Miller, M.J. Two-photon tissue imaging: seeing the immune system in a fresh light. Nat. Rev. Immunol. 2, 872–880 (2002).
Miller, M.J., Wei, S.H., Parker, I. & Cahalan, M.D. Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 296, 1869–1873 (2002).
Mempel, T.R., Henrickson, S.E. & Von Andrian, U.H. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427, 154–159 (2004).
Miller, M.J., Wei, S.H., Cahalan, M.D. & Parker, I. Autonomous T cell trafficking examined in vivo with intravital two-photon microscopy. Proc. Natl. Acad. Sci. USA 100, 2604–2609 (2003).
Adams, G.B. & Scadden, D.T. The hematopoietic stem cell in its place. Nat. Immunol. 7, 333–337 (2006).
Cariappa, A. et al. Perisinusoidal B cells in the bone marrow participate in T-independent responses to blood-borne microbes. Immunity 23, 397–407 (2005).
Cavanagh, L.L. et al. Activation of bone marrow-resident memory T cells by circulating, antigen-bearing dendritic cells. Nat. Immunol. 6, 1029–1037 (2005).
Ladi, E., Yin, X., Chtanova, T. & Robey, E.A. Thymic microenvironments for T cell differentiation and selection. Nat. Immunol. 7, 338–343 (2006).
Witt, C.M., Raychaudhuri, S., Schaefer, B., Chakraborty, A.K. & Robey, E.A. Directed migration of positively selected thymocytes visualized in real time. PLoS Biol. 3, 1062–1069 (2005).
Bhakta, N.R., Oh, D.Y. & Lewis, R.S. Calcium oscillations regulate thymocyte motility during positive selection in the three-dimensional thymic environment. Nat. Immunol. 6, 143–151 (2005).
Drayton, D.L., Liao, S., Mounzer, R.H. & Ruddle, N.H. Lymphoid organ development: from ontogeny to neogenesis. Nat. Immunol. 7, 344–353 (2006).
Wei, S.H. et al. Sphingosine 1-phosphate type 1 receptor agonism inhibits transendothelial migration of medullary T cells to lymphatic sinuses. Nat. Immunol. 6, 1228–1235 (2005).
Cyster, J.G. Chemokines, sphingosine-1-phosphate, and cell migration in secondary lymphoid organs. Annu. Rev. Immunol. 23, 127–159 (2005).
Rosen, H. & Goetzl, E.J. Sphingosine 1-phosphate and its receptors: an autocrine and paracrine network. Nat. Rev. Immunol. 5, 560–570 (2005).
Miller, M.J., Hejazi, A.S., Wei, S.H., Cahalan, M.D. & Parker, I. T cell repertoire scanning is promoted by dynamic dendritic cell behavior and random T cell motility in the lymph node. Proc. Natl. Acad. Sci. USA 101, 998–1003 (2004).
Lindquist, R.L. et al. Visualizing dendritic cell networks in vivo. Nat. Immunol. 5, 1243–1250 (2004).
Miller, M.J., Safrina, O., Parker, I. & Cahalan, M.D. Imaging the single cell dynamics of CD4+ T cell activation by dendritic cells in lymph nodes. J. Exp. Med. 200, 847–856 (2004).
Okada, T. et al. Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells. PLoS Biol. 3, 1047–1061 (2005).
Niederkorn, J.Y. See no evil, hear no evil, do no evil: the lessons of immune privilege. Nat. Immunol. 7, 354–359 (2006).
Medawar, P.B. Immunity to homologous grafted skin. III. The fate of skin homografts transplanted to the brain, to subcutaneous tissue, and to the anterior chamber of the eye. Br. J. Exp. Pathol. 29, 58–69 (1948).
Kawakami, N. et al. Live imaging of effector cell trafficking and autoantigen recognition within the unfolding autoimmune encephalomyelitis lesion. J. Exp. Med. 201, 1805–1814 (2005).
Acknowledgements
Supported by the National Institutes of Health (GM41514 to M.D.C.). Supplementary video 1 was reproduced from The Journal of Experimental Medicine (ref. 25) by copyright permission of The Rockefeller University Press (www.jem.org). Supplementary video 2 was reproduced from PLoS Biol. (www.plosbiology.org) with permission from the authors (ref. 26).
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Supplementary information
Supplementary Video 1
CD4+ T cell—dendritic cell interactions within the diffuse cortex of a lymph node ∼10 hours into a priming immune response. Note stable contacts between several T cells (red) with individual dendritic cells (green) during this cluster stage of the interaction. Reproduced from The Journal of Experimental Medicine (ref. 25) by copyright permission of The Rockefeller University Press (www.jem.org).
Supplementary Video 2
Helper T cell—B cell conjugate pairs viewed ‘waltzing’ near the edge of a lymph node follicle ∼30 hr after priming with antigen. Note rapid motility stable pairs, with B cells (red) leading T cells (green). Reproduced from PLoS Biology (ref. 26) with permission from the authors (www.plosbiology.org).
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Cahalan, M., Gutman, G. The sense of place in the immune system. Nat Immunol 7, 329–332 (2006). https://doi.org/10.1038/ni0406-329
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DOI: https://doi.org/10.1038/ni0406-329
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