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T Lymphocyte Migration to Lymph Nodes Is Maintained during Homeostatic Proliferation

Published online by Cambridge University Press:  03 March 2008

Masanari Kodera ,
Jamison J. Grailer ,
Andrew P-A. Karalewitz ,
Hariharan Subramanian  and
Douglas A. Steeber
Masanari Kodera
Affiliation:
Department of Biological Sciences, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin 53211, USA
Jamison J. Grailer
Affiliation:
Department of Biological Sciences, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin 53211, USA
Andrew P-A. Karalewitz
Affiliation:
Department of Biological Sciences, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin 53211, USA
Hariharan Subramanian
Affiliation:
Department of Biological Sciences, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin 53211, USA
Douglas A. Steeber*
Affiliation:
Department of Biological Sciences, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin 53211, USA
*
Corresponding author. E-mail: Steeber@uwm.edu
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Abstract

The immune system maintains appropriate cell numbers through regulation of cell proliferation and death. Normal tissue distribution of lymphocytes is maintained through expression of specific adhesion molecules and chemokine receptors such as L-selectin and CCR7, respectively. Lymphocyte insufficiency or lymphopenia induces homeostatic proliferation of existing lymphocytes to increase cell numbers. Interestingly, homeostatic proliferation of T lymphocytes induces a phenotypic change from naïve- to memory-type cell. Naïve T cells recirculate between blood and lymphoid tissues whereas memory T cells migrate to nonlymphoid sites such as skin and gut. To assess effects of homeostatic proliferation on migratory ability of T cells, a murine model of lymphopenia-induced homeostatic proliferation was used. Carboxyfluorescein diacetate, succinimidyl ester-labeled wild-type splenocytes were adoptively transferred into recombination activation gene-1-deficient mice and analyzed by flow cytometry, in vitro chemotactic and in vivo migration assays, and immunofluorescence microscopy. Homeostatically proliferated T cells acquired a mixed memory-type CD44high L-selectinhigh CCR7low phenotype. Consistent with this, chemotaxis to secondary lymphoid tissue chemokine in vitro was reduced by 22%–34%. By contrast, no differences were found for migration or entry into lymph nodes during in vivo migration assays. Therefore, T lymphocytes that have undergone homeostatic proliferation recirculate using mechanisms similar to naïve T cells.

Keywords

T lymphocytesrecirculationadhesion moleculesmigrationcell traffickinghomeostatic proliferationflow cytometrychemotaxisimmunofluorescence microscopy
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 14 , Issue 3 , June 2008 , pp. 211 - 224
Copyright
Copyright © Microscopy Society of America 2008

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References

REFERENCES

Abernethy, N.J., Hay, J.B., Kimpton, W.G., Washington, E. & Cahill, R.N.P. (1991). Lymphocyte subset-specific and tissue-specific lymphocyte-endothelial cell recognition mechanisms independently direct the recirculation of lymphocyes from the blood to lymph in sheep. Immunology 72, 239–245.Google Scholar
Arbones, M.L., Ord, D.C., Ley, K., Radich, H., Maynard-Curry, C., Capon, D.J. & Tedder, T.F. (1994). Lymphocyte homing and leukocyte rolling and migration are impaired in L-selectin-deficient mice. Immunity 1, 247–260.CrossRefGoogle ScholarPubMed
Au, B., McCulloch, C.A. & Hay, J.B. (2002). Quantitative studies on the movement of fluid and lymphocytes through periodontal tissue and into the draining lymph. Microsc Res Technol 56, 66–71.Google Scholar
Baccala, R. & Theofilopoulos, A.N. (2005). The new paradigm of T-cell homeostatic proliferation-induced autoimmunity. Trends Immunol 26, 5–8.CrossRefGoogle ScholarPubMed
Bajenoff, M., Granjeaud, S. & Guerder, S. (2003). The strategy of T cell antigen-presenting cell encounter in antigen-draining lymph nodes revealed by imaging of initial T cell activation. J Exp Med 198, 715–724.Google Scholar
Bender, J., Mitchell, T., Kappler, J. & Marrack, P. (1999). CD4+ T cell division in irradiated mice requires peptides distinct from those responsible for thymic selection. J Exp Med 190, 367–374.CrossRefGoogle ScholarPubMed
Berg, E.L., Robinson, M.K., Warnock, R.A. & Butcher, E.C. (1991). The human peripheral lymph node vascular addressin is a ligand for LECAM-1, the peripheral lymph node homing receptor. J Cell Biol 114, 343–349.CrossRefGoogle ScholarPubMed
Bradley, L.M., Atkins, G.G. & Swain, S.S. (1992). Long-term memory CD4+ T cells from spleen lack MEL-14, the lymph node homing receptor. J Immunol 148, 324–331.CrossRefGoogle ScholarPubMed
Bromley, S.K., Thomas, S.Y. & Luster, A.D. (2005). Chemokine receptor CCR7 guides T cell exit from peripheral tissues and entry into afferent lymphatics. Nat Immunol 6, 895–901.Google Scholar
Cahalan, M.D., Parker, I., Wei, S.H. & Miller, M.J. (2002). Two-photon tissue imaging: Seeing the immune system in a fresh light. Nat Rev Immunol 2, 872–880.CrossRefGoogle Scholar
Campbell, D.J. & Butcher, E.C. (2002). Rapid acquisition of tissue-specific homing phenotypes by CD4+ T cells activated in cutaneous or mucosal lymphoid tissues. J Exp Med 195, 135–141.CrossRefGoogle ScholarPubMed
Campbell, D.J., Kim, C.H. & Butcher, E.C. (2003). Chemokines in the systemic organization of immunity. Immunol Rev 195, 58–71.Google Scholar
Chao, C.C., Jensen, R. & Dailey, M.O. (1997). Mechanisms of L-selectin regulation by activated T cells. J Immunol 159, 1686–1694.Google Scholar
Chen, A., Engel, P. & Tedder, T.F. (1995). Structural requirements regulate endoproteolytic release of the L-selectin (CD62L) adhesion receptor from the cell surface of leukocytes. J Exp Med 182, 519–530.CrossRefGoogle ScholarPubMed
Cho, B.K., Rao, V.P., Ge, Q., Eisen, H.N. & Chen, J. (2000). Homeostasis-stimulated proliferation drives naive T cells to differentiate directly into memory T cells. J Exp Med 192, 549–556.CrossRefGoogle ScholarPubMed
Cho, Y. & De Bruyn, P.P.H. (1986). Internal structure of the postcapillary high-endothelial venules of rodent lymph nodes and Peyer's patches and the transendothelial lymphocyte passage. Am J Anat 177, 481–490.CrossRefGoogle ScholarPubMed
Cinalli, R.M., Herman, C.E., Lew, B.O., Wieman, H.L., Thompson, C.B. & Rathmell, J.C. (2005). T cell homeostasis requires G protein-coupled receptor-mediated access to trophic signals that promote growth and inhibit chemotaxis. Eur J Immunol 35, 786–795.CrossRefGoogle ScholarPubMed
Cose, S., Brammer, C., Khanna, K.M., Masopust, D. & Lefrancois, L. (2006). Evidence that a significant number of naive T cells enter non-lymphoid organs as part of a normal migratory pathway. Eur J Immunol 36, 1423–1433.Google Scholar
Dai, Z. & Lakkis, F.G. (2001). Cutting edge: Secondary lymphoid organs are essential for maintaining the CD4, but not CD8, naive T cell pool. J Immunol 167, 6711–6715.Google Scholar
D'Apuzzo, M., Rolink, A., Loetscher, M., Hoxie, J.A., Clark-Lewis, I., Melchers, F., Baggiolini, M. & Moser, B. (1997). The chemokine SDF-1, stromal cell derieved factor 1, attracts early stage B cells precusors via chemokine receptor CXCR4. Eur J Immunol 27, 1788–1793.CrossRefGoogle Scholar
DeGrendele, H.C., Estess, P. & Siegelman, M.H. (1997). Requirement for CD44 in activated T cell extravasation into an inflammatory site. Science 278, 672–675.Google Scholar
del Hoyo, G.M., Martin, P., Arias, C.F., Marin, A.R. & Ardavin, C. (2002). CD8a+ dendritic cells originate from the CD8a− dendritic cell subset by a maturation process involving CD8a, DEC-205, and CD24 up-regulation. Blood 99, 999–1004.CrossRefGoogle Scholar
Dustin, M.L., Rothlein, R., Bhan, A.K., Dinarello, C.A. & Springer, T.A. (1986). Induction by IL 1 and interferon-γ: Tissue distribution, biochemistry, and function of a natural adherence molecule (ICAM-1). J Immunol 137, 245–253.CrossRefGoogle ScholarPubMed
Elices, M.J., Osborn, L., Takada, Y., Crouse, C., Luhowskyj, S., Hemler, M.E. & Lobb, R.R. (1990). VCAM-1 on activated endothelium interacts with the leukocyte integrin VLA-4 at a site distinct from the VLA-4/fibronectin binding site. Cell 60, 577–584.CrossRefGoogle Scholar
Ernst, B., Lee, D.S., Chang, J.M., Sprent, J. & Surh, C.D. (1999). The peptide ligands mediating positive selection in the thymus control T cell survival and homeostatic proliferation in the periphery. Immunity 11, 173–181.Google Scholar
Forster, R., Mattis, A.E., Kremmer, E., Wolf, E., Brem, G. & Lipp, M. (1996). A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen. Cell 87, 1037–1047.Google Scholar
Forster, R., Schubel, A., Breitfeld, D., Kremmer, E., Renner-Muller, I., Wolf, E. & Lipp, M. (1999). CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99, 23–33.Google Scholar
Galkina, E., Tanousis, K., Preece, G., Tolaini, M., Kioussis, D., Florey, O., Haskard, D.O., Tedder, T.F. & Ager, A. (2003). L-selectin shedding does not regulate constitutive T cell trafficking but controls the migration pathways of antigen-activated T lymphocytes. J Exp Med 198, 1323–1335.Google Scholar
Gallatin, W.M., Weissman, I.L. & Butcher, E.C. (1983). A cell-surface molecule involved in organ-specific homing of lymphocytes. Nature 304, 30–34.CrossRefGoogle ScholarPubMed
Goldrath, A.W., Bogatzki, L.Y. & Bevan, M.J. (2000). Naive T cells transiently acquire a memory-like phenotype during homeostasis-driven proliferation. J Exp Med 192, 557–564.Google Scholar
Goldschneider, I. & McGregor, D.D. (1968). Migration of lymphocytes and thymocytes in the rat I. The route of migration from blood to spleen and lymph nodes. J Exp Med 127, 155–168.Google Scholar
Gowans, J.L. (1959). The recirculation of lymphocytes from blood to lymph in the rat. J Physiol 146, 54–69.Google Scholar
Gowans, J.L. & Knight, E.J. (1964). The route of recirculation of lymphocytes in the rat. Proc Roy Soc Lond B 159, 257–282.Google Scholar
Gretz, J.E., Anderson, A.O. & Shaw, S. (1997). Cords, channels, corridors and conduits: Critical architectural elements facilitating cell interactions in the lymph node cortex. Immunol Rev 156, 11–24.CrossRefGoogle ScholarPubMed
Gunn, M.D., Tangemann, K., Tam, C., Cyster, J.G., Rosen, S.D. & Williams, L.T. (1998). A chemokine expressed in lymphoid high endothelial venules promotes the adhesion and chemotaxis of naive T lymphocytes. Proc Natl Acad Sci USA 95, 258–263.Google Scholar
Hall, J.G. & Morris, B. (1965). The origin of the cells in the efferent lymph from a single lymph node. J Exp Med 121, 901–910.Google Scholar
Hazelrigg, M.R., Hirsch, J.I. & Merchant, R.E. (2002). Distribution of adoptively transferred, tumor-sensitized lymphocytes in the glioma-bearing rat. J Neurooncol 60, 143–150.Google Scholar
Huang, A.Y.C., Qi, H. & Germain, R.N. (2004). Illuminating the landscape of in vivo immunity: Insights from dynamic in situ imaging of secondary lymphoid tissues. Immunity 21, 331–339.Google ScholarPubMed
Jameson, S.C. (2002). Maintaining the norm: T-cell homeostasis. Nat Rev Immunol 2, 547–556.Google Scholar
Jung, T.M., Gallatin, W.M., Weissman, I.L. & Dailey, M.O. (1988). Down-regulation of homing receptors after T cell activation. J Immunol 141, 4110–4117.Google Scholar
Katakai, T., Hara, T., Lee, J.-H., Gonda, H., Sugai, M. & Shimizu, A. (2004). A novel reticular stromal structure in lymph node cortex: An immuno-platform for interactions among dendritic cells, T cells and B cells. Int Immunol 16, 1133–1142.CrossRefGoogle ScholarPubMed
Keramidaris, E., Merson, T.D., Steeber, D.A., Tedder, T.F. & Tang, M.L.K. (2001). L-selectin and intercellular adhesion molecule 1 mediate lymphocyte migration to the inflamed airway/lung during an allergic inflammatory response in an animal model of asthma. J Allergy Clin Immunol 107, 734–738.CrossRefGoogle Scholar
Kieper, W.C., Troy, A., Burghardt, J.T., Ramsey, C., Lee, J.Y., Jiang, H.-Q., Dummer, W., Shen, H., Cebra, J.J. & Surh, C.D. (2005). Cutting edge: Recent immune status determines the source of antigens that drive homeostatic T cell expansion. J Immunol 174, 3158–3163.Google Scholar
Kim, C.H. & Broxmeyer, H.E. (1999). Chemokines: Signal lamps for trafficking of T and B cells for development and effector function. J Leukoc Biol 65, 6–15.CrossRefGoogle Scholar
Kodera, M., Conway, R.M., Subramanian, H., Venturi, G.M. & Steeber, D.A. (2006). L-selectin- and β7 integrin-mediated recirculation is required for homeostatic proliferation of CD4+ and CD8+ T cells. J Immunol 176, S295.Google Scholar
Lefrancois, L. (2006). Development, trafficking, and function of memory T-cell subsets. Immunol Rev 211, 93–103.Google Scholar
Lefrancois, L. & Masopust, D. (2002). T cell immunity in lymphoid and non-lymphoid tissues. Curr Opin Immunol 14, 503–508.CrossRefGoogle ScholarPubMed
Lesley, J., Hyman, R. & Kincade, P.W. (1993). CD44 and its interaction with extracellular matrix. Adv Immunol 54, 271–335.Google Scholar
Ley, K. & Kansas, G.S. (2004). Selectins in T-cell recruitment to non-lymphoid tissues and sites of inflammation. Nat Rev Immunol 4, 325–335.Google Scholar
Luettig, B., Pape, L., Bode, U., Bell, E.B., Sparshott, S.M., Wagner, S. & Westermann, J. (1999). Naive and memory T lymphocytes migrate in comparable numbers through normal rat liver: Activated T cells accumulate in the periportal field. J Immunol 163, 4300–4307.Google Scholar
Lyons, A.B. (1999). Divided we stand: Tracking cell proliferation with carboxyfluorescein diacetate succinimidyl ester. Immunol Cell Biol 77, 509–515.Google Scholar
Lyons, A.B. & Parish, C.R. (1994). Determination of lymphocyte division by flow cytometry. J Immunol Meth 171, 131–137.Google Scholar
MacDonald, H.R., Budd, R.C. & Cerottini, J.-C. (1989). Pgp-1 (Ly 24) as a marker of murine memory T lymphocytes. Curr Top Microbiol Immunol 159, 97–109.Google Scholar
Mackay, C.R. (1991). T-cell memory: The connection between function, phenotype and migration pathways. Immunol Today 12, 189–192.CrossRefGoogle ScholarPubMed
Mackay, C.R., Marston, W. & Dudler, L. (1992a). Altered patterns of T cell migration through lymph nodes and skin following antigen challenge. Eur J Immunol 22, 2205–2210.Google Scholar
Mackay, C.R., Marston, W.L. & Dudler, L. (1990). Naive and memory T cells show distinct pathways of lymphocyte recirculation. J Exp Med 171, 801–817.Google Scholar
Mackay, C.R., Marston, W.L., Dudler, L., Spertini, O., Tedder, T.F. & Hein, W.R. (1992b). Tissue-specific migration pathways by phenotypically distinct subpopulations of memory T cells. Eur J Immunol 22, 887–895.CrossRefGoogle ScholarPubMed
Makgoba, M.M., Sanders, M.E., Ginther Luce, G.E., Dustin, M.L., Springer, T.A., Clark, E.A., Mannoni, P. & Shaw, S. (1988). ICAM-1: A ligand for LFA-1 dependent adhesion of B, T, and myeloid cells. Nature 331, 86–88.Google Scholar
Marchesi, V.T. & Gowans, J.L. (1964). The migration of lymphocytes through the endothelium of venules in lymph nodes: An electron microscopic study. Proc Roy Soc Ser B 159, 283–290.Google Scholar
Marleau, A.M. & Sarvetnick, N. (2005). T cell homeostasis in tolerance and immunity. J Leukoc Biol 78, 575–584.Google Scholar
Masopust, D., Vezys, V., Marzo, A.L. & Lefrancois, L. (2001). Preferential localization of effector memory cells in nonlymphoid tissue. Science 291, 2413–2417.Google Scholar
Masopust, D., Vezys, V., Usherwood, E.J., Cauley, L.S., Olson, S., Marzo, A.L., Ward, R.L., Woodland, D.L. & Lefrancois, L. (2004). Activated primary and memory CD8 T cells migrate to nonlymphoid tissues regardless of site of activation or tissue of origin. J Immunol 172, 4875–4882.Google Scholar
Maury, S., Salomon, B., Klatzmann, D. & Cohen, J.L. (2001). Division rate and phenotypic differences discriminate alloreactive and nonalloreactive T cells transferred in lethally irradiated mice. Blood 98, 3156–3158.Google Scholar
Miller, M.J., Wei, S.H., Parker, I. & Cahalan, M.D. (2002). Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 296, 1869–1873.Google Scholar
Mobley, J.L. & Dailey, M.O. (1992). Regulation of adhesion molecule expression by CD8 T cells in vivo. I. Differential regulation of gp90MEL14 (LECAM-1), Pgp-1, LFA-1, and VLA-4a during the differentiation of CTL induced by allografts. J Immunol 148, 2348–2356.Google Scholar
Mombaerts, P., Iacomini, J., Johnson, R.S., Herrup, K., Tonegawa, S. & Papaioannou, V.E. (1992). RAG-1 deficient mice have no mature B and T lymphocytes. Cell 68, 869–877.Google Scholar
Murali-Krishna, K. & Ahmed, R. (2000). Cutting edge: Naive T cells masquerading as memory cells. J Immunol 165, 1733–1737.Google Scholar
Nolte, M.A., Kraal, G. & Mebius, R.E. (2004). Effects of fluorescent and nonfluorescent tracing methods on lymphocyte migration in vivo. Cytometry 61A, 35–44.CrossRefGoogle Scholar
Okada, T., Ngo, V.N., Ekland, E.H., Forster, R., Lipp, M., Littman, D.R. & Cyster, J.G. (2002). Chemokine requirements for B cell entry to lymph nodes and Peyer's patches. J Exp Med 196, 65–75.CrossRefGoogle ScholarPubMed
Parish, C.R. (1999). Fluorescent dyes for lymphocyte migration and proliferation studies. Immunol Cell Biol 77, 499–508.Google Scholar
Picker, L.J. & Butcher, E.C. (1992). Physiological and molecular mechanisms of lymphocyte homing. Annu Rev Immunol 10, 561–591.Google Scholar
Ploix, C., Lo, D. & Carson, M.J. (2001). A ligand for the chemokine receptor CCR7 can influence the homeostatic proliferation of CD4 T cells and progression of autoimmunity. J Immunol 167, 6724–6730.CrossRefGoogle ScholarPubMed
Pribila, J.T., Quale, A.C., Mueller, K.L. & Shimizu, Y. (2004). Integrins and T cell-mediated immunity. Annu Rev Immunol 22, 157–180.Google Scholar
Sallusto, F., Lenig, D., Forster, R., Lipp, M. & Lanzavecchia, A. (1999). Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401, 708–712.Google Scholar
Salmi, M., Tohka, S. & Jalkanen, S. (2000). Human vascular adhesion protein-1 (VAP-1) plays a critical role in lymphocyte-endothelial cell adhesion cascade under shear. Circ Res 86, 1245–1251.CrossRefGoogle Scholar
Schoefl, G.I. (1972). The migration of lymphocytes across the vascular endothelium in lymphoid tissue. A reexamination. J Exp Med 136, 568–588.CrossRefGoogle ScholarPubMed
Scimone, M.L., Felbinger, T.W., Mazo, I.B., Stein, J.V., Von Andrian, U.H. & Weninger, W. (2004). CXCL12 mediates CCR7-independent homing of central memory cells, but not naive T cells, in peripheral lymph nodes. J Exp Med 199, 1113–1120.Google Scholar
Shimizu, Y., Rose, D.M. & Ginsberg, M.H. (1999). Integrins and the immune response. Adv Immunol 72, 325–380.Google Scholar
Singbartl, K., Thatte, J., Smith, M.L., Wethmar, K., Day, K. & Ley, K. (2001). A CD2-green fluorescence protein-transgenic mouse reveals very late antigen-4-dependent CD8+ lymphocyte rolling in inflamed venules. J Immunol 166, 7520–7526.Google Scholar
Springer, T.A. (1994). Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm. Cell 76, 301–314.Google Scholar
Stamper, H.B. Jr. & Woodruff, J.J. (1976). 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.Google Scholar
Steeber, D.A., Engel, P., Miller, A.S., Sheetz, M.P. & Tedder, T.F. (1997). Ligation of L-selectin through conserved regions within the lectin domain activates signal transduction pathways and integrin function in human, mouse, and rat leukocytes. J Immunol 159, 952–963.Google Scholar
Steeber, D.A., Green, N.E., Sato, S. & Tedder, T.F. (1996). Lymphocyte migration in L-selectin-deficient mice: Altered subset migration and aging of the immune system. J Immunol 157, 1096–1106.CrossRefGoogle ScholarPubMed
Steeber, D.A. & Tedder, T.F. (2000). Adhesion molecule cascades direct lymphocyte recirculation and leukocyte migration during inflammation. Immunol Res 22, 299–317.Google Scholar
Stein, J.V., Rot, A., Luo, Y., Narasimhaswamy, M., Nakano, H., Gunn, M.D., Matsuzawa, A., Quackenbush, E.J., Dorf, M.E. & von Andrian, U.H. (2000). The CC chemokine thymus-derived chemokine agent 4 (TCA-4, secondary lymphoid tissue chemokine, 6Ckine, exodus-2) triggers lymphocyte function-associated antigen 1-mediated arrest of rolling T lymphocytes in peripheral lymph node high endothelial venules. J Exp Med 191, 61–75.Google Scholar
Stoll, S., Delon, J., Brotz, T.M. & Germain, R.N. (2002). Dynamic imaging of T cell-dendritic cell interactions in lymph nodes. Science 296, 1873–1876.Google Scholar
Streeter, P.R., Rouse, B.T.N. & Butcher, E.C. (1988). Immunohistologic and functional characterization of a vascular addressin involved in lymphocyte homing into peripheral lymph nodes. J Cell Biol 107, 1853–1862.Google Scholar
Sumen, C., Mempel, T.R., Mazo, I.B. & Von Andrian, U.H. (2004). Intravital microscopy: Visualizing immunity in context. Immunity 21, 315–329.Google Scholar
Tan, J.T., Dudl, E., LeRoy, E., Murray, R., Sprent, J., Weinberg, K.I. & Surh, C.D. (2001). IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proc Natl Acad Sci USA 98, 8732–8737.CrossRefGoogle ScholarPubMed
Tang, M.L.K., Steeber, D.A., Zhang, X.-Q. & Tedder, T.F. (1998). Intrinsic differences in L-selectin expression levels affect T and B lymphocyte subset-specific recirculation pathways. J Immunol 160, 5113–5121.Google Scholar
Tedder, T.F., Penta, A.C., Levine, H.B. & Freedman, A.S. (1990). Expression of the human leukocyte adhesion molecule, LAM1. Identity with the TQ1 and Leu-8 differentiation antigens. J Immunol 144, 532–540.Google Scholar
van Montfrans, C., Bennink, R.J., de Bruin, K., de Jonge, W., Verberne, H.J., ten Kate, F.J.W., van Deventer, S.J.H. & te Velde, A.A. (2004). In vivo evaluation of 111In-labeled T-lymphocyte homing in experimental colitis. J Nucl Med 45, 1759–1765.Google ScholarPubMed
Venturi, G.M., Conway, R.M., Steeber, D.A. & Tedder, T.F. (2007). CD25+CD4+ regulatory T cell migration requires L-selectin expression: L-selectin transcriptional regulation balances constitutive receptor turnover. J Immunol 178, 291–300.Google Scholar
Venturi, G.M., Tu, L., Kadono, T., Khan, A.I., Fujimoto, Y., Oshel, P., Bock, C.B., Miller, A.S., Albrecht, R.M., Kubes, P., Steeber, D.A. & Tedder, T.F. (2003). Leukocyte migration is regulated by L-selectin endoproteolytic release. Immunity 19, 713–724.Google Scholar
Westermann, J. & Pabst, R. (1996). How organ-specific is the migration of “naive” and “memory” T lymphocytes? Immunol Today 17, 278–282.Google Scholar
Young, A.J., Marston, W.L. & Dudler, L. (2000). Subset-specific regulation of the lymphatic exit of recirculating lymphocytes in vivo. J Immunol 165, 3168–3174.Google Scholar
Zatz, M.M. & Lance, E.M. (1971). The distribution of 51Cr-labeled lymphocytes into antigen-stimulated mice. Lymphocyte trapping. J Exp Med 134, 224–241.Google Scholar