Activation of bone marrow-resident memory T cells by circulating, antigen-bearing dendritic cells

Nature Immunology

Volumn 6, Issue 10, 2005, Pages 1029-1037

  Cavanagh, Lois L ^a,d   Bonasio, Roberto ^a,d   Mazo, Irina B ^a   Halin, Cornelia ^a   Cheng, Guiying ^a   van der Velden, Adrianus W M ^a   Cariappa, Annaiah ^b   Chase, Catherine ^b   Russell, Paul ^b   Starnbach, Michael N ^a   Koni, Pandelakis A ^c   Pillai, Shiv ^b   Weninger, Wolfgang ^a,d   von Andrian, Ulrich H ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

^d WISTAR INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; SELECTIN; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW; CELL ACTIVATION; CELL ACTIVITY; CELL DIFFERENTIATION; CELL INTERACTION; CELL MIGRATION; CELL TRANSPORT; CONTROLLED STUDY; DENDRITIC CELL; GENE EXPRESSION; LIVER; LUNG; LYMPH NODE; LYMPHOCYTE HOMING; MEMORY CELL; MICROSCOPY; MICROVASCULATURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN; TISSUE DISTRIBUTION;

ANIMALS; BLOOD VESSELS; BONE MARROW; CELL MOVEMENT; DENDRITIC CELLS; ENDOTHELIUM, VASCULAR; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; MICE; MICE, CONGENIC; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; SELECTINS; T-LYMPHOCYTES; VASCULAR CELL ADHESION MOLECULE-1;

EID: 27144535376     PISSN: 15292908     EISSN: None     Source Type: Journal    
DOI: 10.1038/ni1249     Document Type: Article

References (50)

1. Banchereau, J. et al. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18, 767-811 (2000).
2. Cavanagh, L.L. & von Andrian, U.H. Travellers in many guises: The origins and destinations of dendritic cells. Immunol. Cell Biol. 80, 448-462 (2002).
3. Sallusto, F. et al. Rapid and coordinated switch in chemokine receptor expression during dendritic cell maturation. Eur. J. Immunol. 28, 2760-2769 (1998).
4. Balazs, M., Martin, F., Zhou, T. & Kearney, J. Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity 17, 341-352 (2002).
5. Randolph, G.J., Inaba, K., Robbiani, D.F., Steinman, R.M. & Muller, W.A. Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity 11, 753-761 (1999).
6. Legge, K.L. & Braciale, T.J. Accelerated migration of respiratory dendritic cells to the regional lymph nodes is limited to the early phase of pulmonary infection. Immunity 18, 265-277 (2003).
7. Mullins, D.W. et al. Route of immunization with peptide-pulsed dendritic cells controls the distribution of memory and effector T cells in lymphoid tissues and determines the pattern of regional tumor control. J. Exp. Med. 198, 1023-1034 (2003).
8. Schuler, G., Schuler-Thurner, B. & Steinman, R.M. The use of dendritic cells in cancer immunotherapy. Curr. Opin. Immunol. 15, 138-147, (2003).
9. Sallusto, F., Geginat, J. & Lanzavecchia, A. Central memory and effector memory T cell subsets: Function, generation, and maintenance. Annu. Rev. Immunol. 22, 745-763 (2004).
10. Di Rosa, F. & Santoni, A. Bone marrow CD8 T cells are in a different activation state than those in lymphoid periphery. Eur. J. Immunol. 32, 1873-1880 (2002).
11. Becker, T.C., Coley, S.M., Wherry, E.J. & Ahmed, R. Bone marrow is a preferred site for homeostatic proliferation of memory CD8 T cells. J. Immunol. 174, 1269-1273 (2005).
12. + T cells. Immunity 22, 259-270 (2005).
13. Feuerer, M. et al. Therapy of human tumors in NOD/SCID mice with patient-derived reactivated memory T cells from bone marrow. Nat. Med. 7, 452-458 (2001).
14. Maraskovsky, E. et al. Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell subpopulations identified. J. Exp. Med. 184, 1953-1962 (1996).
15. Mora, J.R. et al. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 424, 88-93 (2003).
16. von Andrian, U.H. & Mackay, C.R. T-cell function and migration. Two sides of the same coin. N. Engl. J. Med. 343, 1020-1034 (2000).
17. Shortman, K. & Liu, Y.J. Mouse and human dendritic cell subtypes. Nat. Rev. Immunol. 2, 151-161 (2002).
18. Donnenberg, V.S. et al. Rare-event analysis of circulating human dendritic cell subsets and their presumptive mouse counterparts. Transplantation 72, 1946-1951 (2001).
19. Wright, D.E., Wagers, A.J., Gulati, A.P., Johnson, F.L. & Weissman, I.L. Physiological migration of hematopoietic stem and progenitor cells. Science 294, 1933-1936 (2001).
20. Kamath, A.T. et al. The development, maturation, and turnover rate of mouse spleen dendritic cell populations. J. Immunol. 165, 6762-6770 (2000).
21. Mazo, I.B. et al. Hematopoietic progenitor cell rolling in bone marrow microvessels: Parallel contributions by endothelial selectins and VCAM-1. J. Exp. Med. 188, 465-474 (1998).
22. Manjunath, N. et al. Effector differentiation is not prerequisite for generation of memory cytotoxic T lymphocytes. J. Clin. Invest. 108, 871-878 (2001).
23. + T cells. J. Exp. Med. 194, 953-966 (2001).
24. Robert, C. et al. Gene therapy to target dendritic cells from blood to lymph nodes. Gene Ther. 10, 1479-1486 (2003).
25. Sumen, C., Mempel, T.R., Mazo, I.B. & von Andrian, U.H. Intravital microscopy; visualizing immunity in context. Immunity 21, 315-329 (2004).
26. del Hoyo, G.M. et al. Characterization of a common precursor population for dendritic cells. Nature 415, 1043-1047 (2002).
27. + DC1 precursors. Blood 101, 1453-1459 (2003).
28. Robert, C. et al. Interaction of dendritic cells with skin endothelium: A new perspective on immunosurveillance. J. Exp. Med. 189, 627-636 (1999).
29. Fossum, S. Lymph-borne dendritic leucocytes do not recirculate, but enter the lymph node paracortex to become interdigitating cells. Scand. J. Immunol. 27, 97-105 (1988).
30. Kupiec-Weglinski, J.W., Austyn, J.M. & Morris, P.J. Migration patterns of dendritic cells in the mouse. Traffic from the blood, and T cell-dependent and -independent entry to lymphoid tissues. J. Exp. Med. 167, 632-645 (1988).
31. Lappin, M.B. et al. Analysis of mouse dendritic cell migration in vivo upon subcutaneous and intravenous injection. Immunology 98 181-188 (1999).
32. Frenette, P.S., Subbarao, S., Mazo, I.B., von Andrian, U.H. & Wagner, D.D. Endothelial selectins and vascular cell adhesion molecule-1 promote hematopoietic progenitor homing to bone marrow. Proc. Natl. Acad. Sci. USA 95, 14423-14428 (1998).
33. Di Rosa, F. & Pabst, R. The bone marrow: A nest for migratory memory T cells. Trends Immunol. 26, 360-366 (2005).
34. Wherry, E.J. et al. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat. Immunol. 4, 225-234 (2003).
35. Zammit, D.J., Cauley, L.S., Pham, Q.M. & Lefrancois, L. Dendritic cells maximize the memory CD8 T cell response to infection. Immunity 22, 561-570 (2005).
36. 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).
37. Gesner, B.M. & Gowans, J.L. The output of lymphocytes from the thoracic duct of unanaesthetized mice. Br. J. Exp. Path. 43, 424-430 (1962).
38. von Andrian, U.H. & Mempel, T.R. Homing and cellular traffic in lymph nodes. Nat. Rev. Immunol. 3, 867-878 (2003).
39. Randolph, G.J., Beaulieu, S., Lebecque, S., Steinman, R.M. & Muller, W.A. Differentiation of monocytes into dendritic cells in a model of transendothelial trafficking. Science 282, 480-483 (1998).
40. Enioutina, E.Y., Visic, D. & Daynes, R.A. The induction of systemic and mucosal immune responses to antigen-adjuvant compositions administered into the skin: Alterations in the migratory properties of dendritic cells appears to be important for stimulating mucosal immunity. Vaccine 18, 2753-2767 (2000).
41. + T cells and antiviral immunity. Immunity 20, 47-58 (2004).
42. Larsen, C.P., Morris, P.J. & Austyn, J.M. Migration of dendritic leukocytes from cardiac allografts into host spleens. A novel pathway for initiation of rejection. J. Exp. Med. 171, 307-314 (1990).
43. Saiki, T., Ezaki, T., Ogawa, M. & Matsuno, K. Trafficking of host- and donor-derived dendritic cells in rat cardiac transplantation: allosensitization in the spleen and hepatic nodes. Transplantation 71, 1806-1815 (2001).
44. Vazquez-Torres, A. et al. Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 401, 804-808 (1999).
45. Pircher, H., Burki, K., Lang, R., Hengartner, H. & Zinkernagel, R.M. Tolerance induction in double specific T-cell receptor transgenic mice varies with antigen. Nature 342, 559-561 (1989).
46. Koni, P.A. et al. Conditional vascular cell adhesion molecule 1 deletion in mice. Impaired lymphocyte migration to bone marrow. J. Exp. Med. 193, 741-754 (2001).
47. Boggs, D.R. The total marrow mass of the mouse: A simplified method of measurement. Am. J. Hematol. 16, 277-286 (1984).
48. Boak, J.L. & Woodruff, M.F.A. Modified technique for collecting mouse thoracic duct lymph. Nature 205, 396-397 (1965).
49. Lyons, A.B. Analysing cell division in vivo and in vitro using flow cytometric measurement of CFSE dye dilution. J. Immunol. Methods 243, 147-154 (2000).
50. Mempel, T.R., Scimone, M.L., Mora, J.R. & von Andrian, U.H. In vivo imaging of leukocyte trafficking in blood vessels and tissues. Curr. Opin. lmmunol. 16, 406-417 (2004).