Preferential accumulation of antigen-specific effector CD4 T cells at an antigen injection site involves CD62E-dependent migration but not local proliferation

Journal of Experimental Medicine

Volumn 197, Issue 6, 2003, Pages 751-762

  Reinhardt, R Lee ^a   Bullard, Daniel C ^b   Weaver, Casey T ^c   Jenkins, Marc K ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

Antigen specific; CD4; Migration; Selectin; T cell

Indexed keywords

CD4 ANTIGEN; CD62E ANTIGEN; CHICKEN OVALBUMIN; PADGEM PROTEIN; PEPTIDE DERIVATIVE; SELECTIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIBODY COMBINING SITE; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ARTICLE; BLOOD VESSEL; CELL DIVISION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EFFECTOR CELL; INJECTION SITE; INTERFERON PRODUCTION; LYMPH NODE; LYMPHATIC DRAINAGE; LYMPHOCYTE COUNT; LYMPHOID TISSUE; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; T LYMPHOCYTE ACTIVATION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS; ANTIMETABOLITES; BROMODEOXYURIDINE; CD4-POSITIVE T-LYMPHOCYTES; CELL DIVISION; CELL MOVEMENT; E-SELECTIN; IMMUNIZATION; IMMUNOHISTOCHEMISTRY; INTERFERON TYPE II; INTERLEUKIN-2; MICE; MICE, INBRED STRAINS; OVALBUMIN; PROTEIN BINDING;

EID: 0345268754     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20021690     Document Type: Article

References (62)

1. von Andrian, U.H., and C.R. Mackay. 2000. T-cell function and migration. N. Engl. J. Med. 343:1020-1034.
2. Banchereau, J., and R.M. Steinman. 1998. Dendritic cells and the control of immunity. Nature. 392:245-252.
3. Jenkins, M.K., A. Khoruts, E. Ingulli, D.L. Mueller, S.J. McSorley, R.L. Reinhardt, A. Itano, and K.A. Pape. 2001. In vivo activation of antigen-specific CD4 T cells. Annu. Rev. Immunol. 19:23-45.
4. Reinhardt, R.L., A. Khoruts, R. Merica, T. Zell, and M.K. Jenkins. 2001. Visualizing the generation of memory CD4 T cells in the whole body. Nature. 410:101-105.
5. Mohrs, M., K. Shinkai, K. Mohrs, and R.M. Locksley. 2001. Analysis of type 2 immunity in vivo with a bicistronic IL-4 reporter. Immunity. 15:303-311.
6. Harris, N.L., V. Watt, F. Ronchese, and G. Le Gros. 2002. Differential T cell function and fate in lymph node and nonlymphoid tissues. J. Exp. Med. 195:317-326.
7. Roman, E., E. Miller, A. Harmsen, J. Wiley, U.H. Von Andrian, G. Huston, and S.L. Swain. 2002. CD4 effector T cell subsets in the response to influenza: heterogeneity, migration, and function. J. Exp. Med. 196:957-968.
8. Campbell, J.J., and E.C. Butcher. 2000. Chemokines in tissue-specific and microenvironment-specific lymphocyte homing. Curr. Opin. Immunol. 12:336-341.
9. Fuhlbrigge, R.C., J.D. Kieffer, D. Armerding, and T.S. Kupper. 1997. Cutaneous lymphocyte antigen is a specialized form of PSGL-1 expressed on skin-homing T cells. Nature. 389:978-981.
10. Steegmaier, M., A. Levinovitz, S. Isenmann, E. Borges, M. Lenter, H.P. Kocher, B. Kleuser, and D. Vestweber. 1995. The E-selectin-ligand ESL-1 is a variant of a receptor for fibroblast growth factor. Nature. 373:615-620.
11. Lim, Y.C., L. Henault, AJ. Wagers, G.S. Kansas, F.W. Luscinskas, and A.H. Lichtman. 1999. Expression of functional selectin ligands on Th cells is differentially regulated by IL-12 and IL-4. J. Immunol. 162:3193-3201.
12. Maly, P., A. Thall, B. Petryniak, C.E. Rogers, P.L. Smith, R.M. Marks, R.J. Kelly, K.M. Gersten, G. Cheng, T.L. Saunders, et al. 1996. The alpha(1,3) fucosyltransferase Fuc-TVII controls leukocyte trafficking through an essential role in L-, E-, and P-selectin ligand biosynthesis. Cell. 86:643-653.
13. Blander, J.M., I. Visintin, C.A. Janeway, Jr., and R. Medzhitov. 1999. Alpha (1,3)-fucosyltransferase VII and alpha(2,3)-sialyltransferase IV are up-regulated in activated CD4 T cells and maintained after their differentiation into Th1 and migration into inflammatory sites. J. Immunol. 163:3746-3752.
14. Lim, Y.C., H. Xie, C.E. Come, S.I. Alexander, M.J. Grusby, A.H. Lichtman, and F.W. Luscinskas. 2001. IL-12, STAT4-dependent up-regulation of CD4(+) T cell core 2 beta-1,6-n-acetylglucosaminyltransferase, an enzyme essential for biosynthesis of P-selectin ligands. J. Immunol. 167:4476-4484.
15. White, S.J., G.H. Underhill, M.H. Kaplan, and G.S. Kansas. 2001. Differential requirements for Stat4 in expression of glycosyltransferases responsible for selectin ligand formation in Th1 cells. J. Immunol. 167:628-631.
16. Tietz, W., Y. Allemand, E. Borges, D. von Laer, R. Hallmann, D. Vestweber, and A. Hamann. 1998. CD4+ T cells migrate into inflamed skin only if they express ligands for E- and P-selectin. J. Immunol. 161:963-970.
17. Austrup, F., D. Vestweber, E. Borges, M. Lohning, R. Brauer, U. Herz, H. Renz, R. Hallmann, A. Scheffold, A. Radbruch, and A. Hamann. 1997. P- and E-selectin mediate recruitment of T-helper-1 but not T-helper-2 cells into inflamed tissues. Nature. 385:81-83.
18. Hirata, T., G. Merrill-Skoloff, M. Aab, J. Yang, B.C. Furie, and B. Furie. 2000. P-Selectin glycoprotein ligand 1 (PSGL-1) is a physiological ligand for E-selectin in mediating T helper 1 lymphocyte migration. J. Exp. Med. 192:1669-1676.
19. Subramaniam, M., S. Saffaripour, S.R. Watson, T.N. Mayadas, R.O. Hynes, and D.D. Wagner. 1995. Reduced recruitment of inflammatory cells in a contact hypersensitivity response in P-selectin-deficient mice. J. Exp. Med. 181: 2277-2282.
20. Labow, M.A., C.R. Norton, J.M. Rumberger, K.M. Lombard-Gillooly, D.J. Shuster, J. Hubbard, R. Bertko, P.A. Knaack, R.W. Terry, and M.L. Harbison. 1994. Characterization of E-selectin-deficient mice: demonstration of overlapping function of the endothelial selectins. Immunity. 1:709-720.
21. Staite, N.D., J.M. Justen, L.M. Sly, A.L. Beaudet, and D.C. Bullard. 1996. Inhibition of delayed-type contact hypersensitivity in mice deficient in both E-selectin and P-selectin. Blood. 88:2973-2979.
22. Erdmann, I., E.P. Scheidegger, F.K. Koch, L. Heinzerling, B. Odermatt, G. Burg, J.B. Lowe, and T.M. Kundig. 2002. Fucosyltransferase VII-deficient mice with defective E-, P-, and L-selectin ligands show impaired CD4+ and CD8+ T cell migration into the skin, but normal extravasation into visceral organs. J. Immunol. 168:2139-2146.
23. Binns, R.M., A. Whyte, S.T. Licence, A.A. Harrison, Y.T. Tsang, D.O. Haskard, and M.K. Robinson. 1996. The role of E-selectin in lymphocyte and polymorphonuclear cell recruitment into cutaneous delayed hypersensitivity reactions in sensitized pigs. J. Immunol. 157:4094-4099.
24. Silber, A., W. Newman, V.G. Sasseville, D. Pauley, D. Beall, D.G. Walsh, and D.J. Ringler. 1994. Recruitment of lymphocytes during cutaneous delayed hypersensitivity in nonhuman primates is dependent on E-selectin and vascular cell adhesion molecule 1. J. Clin. Invest. 93:1554-1563.
25. Campbell, D.J., C.H. Kim, and E.C. Butcher. 2001. Separable effector T cell populations specialized for B cell help or tissue inflammation. Nat. Immunol. 2:876-881.
26. Picker, L.J., L.W. Terstappen, L.S. Rott, P.R. Streeter, H. Stein, and E.C. Butcher. 1990. Differential expression of homing-associated adhesion molecules by T cell subsets in man. J. Immunol. 145:3247-3255.
27. Topham, D.J., M.R. Castrucci, F.S. Wingo, G.T. Belz, and P.C. Doherty. 2001. The role of antigen in the localization of naive, acutely activated, and memory CD8(+) T cells to the lung during influenza pneumonia. J. Immunol. 167:6983-6990.
28. Cross, A.H., T. O'Mara, and C.S. Raine. 1993. Chronologic localization of myelin-reactive cells in the lesions of relapsing EAE: implications for the study of multiple sclerosis. Neurology. 43:1028-1033.
29. Liu, C.P., K. Jiang, C.H. Wu, W.H. Lee, and W.J. Lin. 2000. Detection of glutamic acid decarboxylase-activated T cells with I-Ag7 tetramers. Proc. Natl. Acad. Sci. USA. 97: 14596-14601.
30. Masopust, D., V. Vezys, A.L. Marzo, and L. Lefrancois. 2001. Preferential localization of effector memory cells in nonlymphoid tissue. Science. 291:2413-2417.
31. lo thymocytes in vivo. Science. 250: 1720-1723.
32. Barnden, M.J., J. Allison, W.R. Heath, and F.R. Carbone. 1998. Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and beta-chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 76:34-40.
33. Bullard, D.C., E.J. Kunkel, H. Kubo, M.J. Hicks, I. Lorenzo, N.A. Doyle, C.M. Doerschuk, K. Ley, and A.L. Beaudet. 1996. Infectious susceptibility and severe deficiency of leukocyte rolling and recruitment in E-selectin and P-selectin double mutant mice. J. Exp. Med. 183:2329-2336.
34. Haskins, K., R. Kubo, J. White, M. Pigeon, J. Kappler, and P. Marrack. 1983. The major histocompatibility complex-restricted antigen receptor on T cells. I. Isolation with a monoclonal antibody. J. Exp. Med. 157:1149-1169.
35. Southern, P.J., P. Blount, and M.B. Oldstone. 1984. Analysis of persistent virus infections by in situ hybridization to whole-mouse sections. Nature. 312:555-558.
36. Khoruts, A., A. Mondino, K.A. Pape, S.L. Reiner, and M.K. Jenkins. 1998. A natural immunological adjuvant enhances T cell clonal expansion through a CD28-dependent, interleukin (IL)-2-independent mechanism. J. Exp. Med. 187:225-236.
37. Penit, C., and F. Vasseur. 1997. Expansion of mature thymocyte subsets before emigration to the periphery. J. Immunol. 159:4848-4856.
38. Warren, H.S., F.R. Vogel, and L.A. Chedid. 1986. Current status of immunological adjuvants. Annu. Rev. Immunol. 4:369-388.
39. Kearney, E.R., K.A. Pape, D.Y. Loh, and M.K. Jenkins. 1994. Visualization of peptide-specific T cell immunity and peripheral tolerance induction in vivo. Immunity. 1:327-339.
40. Mackay, C.R., D.P. Andrew, M. Briskin, D.J. Ringler, and E.C. Butcher. 1996. Phenotype, and migration properties of three major subsets of tissue homing T cells in sheep. Eur. J. Immunol. 26:2433-2439.
41. Mackay, C., W. Marston, and L. Dudler. 1990. Naive and memory T cells show distinct pathways of lymphocyte recirculation. J. Exp. Med. 171:801-817.
42. Lyons, A.B., and C.R. Parish. 1994. Determination of lymphocyte division by flow cytometry. J. Immunol. Methods. 171:131-137.
43. Campbell, D.J., and E.C. Butcher. 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.
44. Todderud, G., J. Alford, K.A. Millsap, A. Aruffo, and K.M. Tramposch. 1992. PMN binding to P-selectin is inhibited by sulfatide. J. Leukoc. Biol. 52:85-88.
45. Marshall, D.R., S.J. Turner, G.T. Belz, S. Wingo, S. Andreansky, M.Y. Sangster, J.M. Riberdy, T. Liu, M. Tan, and P.C. Doherty. 2001. Measuring the diaspora for virus-specific CD8+ T cells. Proc. Natl. Acad. Sci. USA. 98:6313-6318.
46. Moser, B., and P. Loetscher. 2001. Lymphocyte traffic control by chemokines. Nat. Immunol. 2:123-128.
47. Geng, J.G., M.P. Bevilacqua, K.L. Moore, T.M. McIntyre, S.M. Prescott, J.M. Kim, G.A. Bliss, G.A. Zimmerman, and R.P. McEver. 1990. Rapid neutrophil adhesion to activated endothelium mediated by GMP-140. Nature. 343:757-760.
48. Groves, R.W., M.H. Allen, J.N. Barker, D.O. Haskard, and D.M. MacDonald. 1991. Endothelial leucocyte adhesion molecule-1 (ELAM-1) expression in cutaneous inflammation. Br. J. Dermatol. 124:117-123.
49. Silber, A., W. Newman, K.A. Reimann, E. Hendricks, D. Walsh, and D.J. Ringler. 1994. Kinetic expression of endothelial adhesion molecules and relationship to leukocyte recruitment in two cutaneous models of inflammation. Lab. Invest. 70:163-175.
50. Streeter, P.R., E.L. Berg, B.T. Rouse, K.F. Bargatze, and E.C. Butcher. 1988. A tissue-specific endothelial cell molecule involved in lymphocyte homing. Nature. 331:41-46.
51. Hirata, T., B.C. Furie, and B. Furie. 2002. P-, E-, and L-selectin mediate migration of activated CD8+ T lymphocytes into inflamed skin. J. Immunol. 169:4307-4313.
52. Kulidjian, A.A., A.C. Issekutz, and T.B. Issekutz. 2002. Differential role of E-selectin and P-selectin in T lymphocyte migration to cutaneous inflammatory reactions induced by cytokines. Int. Immunol. 14:751-760.
53. Bevilacqua, M.P., S. Stengelin, M.A. Gimbrone, Jr., and B. Seed. 1989. Endothelial leukocyte adhesion molecule 1: an inducible receptor for neutrophils related to complement regulatory proteins and lectins. Science. 243:1160-1165.
54. St Louis, J.D., J.A. Lederer, and A.H. Lichtman. 1993. Costimulator deficient antigen presentation by an endothelial cell line induces a nonproliferative T cell activation response without anergy. J. Exp. Med. 178:1597-1605.
55. Girvin, A.M., K.B. Gordon, C.J. Welsh, N.A. Clipstone, and S.D. Miller. 2002. Differential abilities of central nervous system resident endothelial cells and astrocytes to serve as inducible antigen-presenting cells. Blood. 99:3692-3701.
56. Zeine, R., and T. Owens. 1992. Direct demonstration of the infiltration of murine central nervous system by Pgp-1/ CD44high CD45RB(low) CD4+ T cells that induce experimental allergic encephalomyelitis. J. Neuroimmunol. 40:57-69.
57. Masopust, D., J. Jiang, H. Shen, and L. Lefrancois. 2001. Direct analysis of the dynamics of the intestinal mucosa CD8 T cell response to systemic virus infection. J. Immunol. 166: 2348-2356.
58. Hogan, R.J., E.J. Usherwood, W. Zhong, A.A. Roberts, R.W. Dutton, A.G. Harmsen, and D.L. Woodland. 2001. Activated antigen-specific CD8+ T cells persist in the lungs following recovery from respiratory virus infections. J. Immunol. 166:1813-1822.
59. Deeths, M.J., R.M. Kedl, and M.F. Mescher. 1999. CD8+ T cells become nonresponsive (anergic) following activation in the presence of costimulation. J. Immunol. 163:102-110.
60. Shrikant, P., A. Khoruts, and M.F. Mescher. 1999. CTLA-4 blockade reverses CD8+ T cell tolerance to tumor by a CD4+ T cell- and IL-2-dependent mechanism. Immunity. 11:483-493.
61. Bird, J.J., D.R. Brown, A.C. Mullen, N.H. Moskowitz, M.A. Mahowald, J.R. Sider, T.F. Gajewski, C.R. Wang, and S.L. Reiner. 1998. Helper T cell differentiation is controlled by the cell cycle. Immunity. 9:229-237.
62. Laouar, Y., and I.N. Crispe. 2000. Functional flexibility in T cells: independent regulation of CD4+ T cell proliferation and effector function in vivo. Immunity. 13:291-301.