Interleukin 15 is produced by endothelial cells and increases the transendothelial migration of T cells in vitro and in the SCID mouse-human rheumatoid arthritis model in vivo

Journal of Clinical Investigation

Volumn 101, Issue 6, 1998, Pages 1261-1272

  Oppenheimer Marks, Nancy ^a   Brezinschek, Ruth I ^a   Mohamadzadeh, Mansour ^a   Vita, Randi ^a   Lipsky, Peter E ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Adhesion; CD69; Cytokine; LFA 1; Motility

Indexed keywords

CD69 ANTIGEN; INTERLEUKIN 15; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COMBINED IMMUNODEFICIENCY; CONTROLLED STUDY; HUMAN; HUMAN CELL; LYMPHOCYTE MIGRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; SYNOVIUM; T LYMPHOCYTE; UMBILICAL VEIN; VASCULAR ENDOTHELIUM;

EID: 0032521147     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI1986     Document Type: Article

References (48)

1. Kavanaugh, A., and N. Oppenheimer-Marks. 1992. The role of the vascular endothelium in the pathogenesis of vasculitis. In Systemic Vasculitis: The Biological Basis. E. Carwile LeRoy, editor. Marcel Dekker, Inc.
2. Oppenheimer-Marks, N., and P.E. Lipsky. 1994. Transendotholial migration of T cells in chronic inflammation. Immunologist. 2:58-64.
3. Oppenheimer-Marks. N., L.S. Davis, D. Tompkins Bogue, J. Ramberg, and P.E. Lipsky. 1991. Differential utilization of ICAM-1 and VCAM-1 during the adhesion and transendothelial migration of human T lymphocytes. J. Immunol. 147:2913-2921.
4. Oppenheimer-Marks, N., L.S. Davis, and P.E. Lipsky. 1990 Human T lymphocyte adhesion to endothelial cells and trans-endothelial migration: alteration of receptor utilization relates to the activation status of both the T cell and the endothelial cell. J. Immunol. 145:140-148.
5. Brezinschek, R., P.E. Lipsky, P. Galea, R. Vita, and N. Oppenheimer-Marks. 1995. Phenotypic characterization of CD4(+) T cells that exhibit a transendothelial migratory capacity. J. Immunol. 154:3062-3077.
6. Woldemar Carr, M., S.J. Roth, E. Luther, S.S. Rose, and T.S. Springer. 1994. Monocyte chemoattractant protein 1 acts as a T-lymphocyte chemoattractant. Proc. Natl. Acad. Med. 91:3652-3656.
7. Roth, S.J., M. Woldemar Carr, and T.S. Springer. 1995. C-C chemokines. but not the C-X-C chemokines interleukin-8 and interferon-γ inducible protein-10. stimulate the transendothelial chemotaxis of T lymphocytes. Eur. J. Immunol. 25:3482-3488.
8. del Pozo, M.A., P. Sánchez-Mateos, M. Nieto, and F. Sánchez-Madrid. 1995. Chemokines regulate cellular polarization and adhesion receptor redistribution during lymphocyte interaction with endothelium and extracellular matrix. Involvement of cAMP signaling pathway. J. Cell Biol. 131:495-508.
9. Woldemar Carr, M., R. Alon, and T.S. Springer. 1996. The C-C chemokine MCP-1 differentially modulates the avidity of β1 and β2 integrins on T lymphocytes. Immunity. 4:179-187.
10. Gimbrone, M.A., Jr., M.S. Obin, A.F. Brock, E.A. Luis, P.E. Hass, C.A. Hébert, Y.K. Yip, D.W. Leung, D.G. Lowe, W.J. Kohr, et al. 1989. Endothelial interleukin-8: a novel inhibitor of leukocyte-endothelial interactions. Science. 246:1601-1603.
11. Li, Y.-S., Y.-J. Shyy, J.G. Wright, A.J. Valente, J.F. Cornhill, and P.E. Kolattukudy. 1993. The expression of monocyte chemotactic protein (MCP-1) in human vascular endothelium in vitro and in vivo. Mol. Cell. Biochem. 126: 61-68.
12. Grabstein, K.H., J. Eisenman, K. Shanebeck, C. Rauch, S. Srinivasan, V. Fung, C. Beers, J. Richardson, M.A. Schoenborn, M. Ahdieh, et al. 1994. Cloning of a T cell growth factor that interacts with the β chain of the interleukin-2 receptor. Science. 264:965-968.
13. Giri, J.G., D.M. Anderson, S. Kumaki, L.S. Park, K.H. Grabstein, and D. Cosman. 1995. IL-15, a novel T cell growth factor that shares activities and receptor components with IL-2. J. Leukoctye Biol. 57:763-766.
14. Kennedy, M.K., and L.S. Park. 1996. Characterization of interleukin-15 (IL-15) and the IL-15 receptor complex. J. Clin. Immunol. 16:134-143.
15. Wilkinson, P.C., and F.Y. Liew. 1995. Chemoattraction of human blood T lymphocytes by interleukin-15. J. Exp. Med. 181:1255-1259.
16. Nieto, M., M.A. del Pozo, and F. Sánchez-Madrid. 1996. Interleukin-15 induces adhesion receptor redistribution in T lymphocytes. Eur. J. Immunol. 26:1302-1307.
17. McInnes, I.B., J. Al-Mughales, M. Feld, B.P. Leung, F.-P. Huang, R. Dixon, R.D. Sturrock, P.C. Wilkinson, and F.Y. Liew. 1996. The role of interleukin-15 in T-cell migration and activation in rheumatoid arthritis. Nat. Med. 2: 175-182.
18. Allevana, P., G. Giardina, G. Bianchi, and A. Montovani. 1997. IL-15 is chemotactic for natural killer cells and stimulates their adhesion to vascular endothelium. J. Leukocyte Biol. 61:729-735.
19. Carson, W.E., J.G. Giri, M.J. Lindemann, M.L. Linett, M. Ahdieh, R. Paxton, D. Anderson, J. Eisenmann, K. Grabstein, and M.A. Caligiuri. 1994. Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor. J. Exp. Med. 180:1395-1403.
20. Giri, J.G., M. Ahdieh, J. Eisenman, K. Shanebeck, K. Grabstein, S. Kumaki, A. Namen, L.S. Park, D. Cosman, and D. Anderson. 1994. Utilization of the β and γ chains of the IL-2 receptor by the novel cytokine IL-15. EMBO (Eur. Mol. Biol. Organ.) J. 13:2822-2830.
21. Giri, J.G., S. Kumaki, M. Ahdieh, D.J. Friend, A. Loomis, K. Shanebeck, R. DuBose, D. Cosman, L.S. Park, and D.M. Anderson. 1995. Identification and cloning of a novel IL-15 binding protein that is structurally related to the α chain of the IL-2 receptor. EMBO (Eur. Mol. Biol. Organ.) J. 14: 3654-3663.
22. Tagaya, Y., J.D. Burton. Y. Miyamoto, and T.A. Waldmann. 1996. Identification of a novel receptor/signal transduction pathway for IL-15/T in mast cells. EMBO (Eur. Mol. Biol. Organ.) J. 15:4428-4939.
23. Tagaya, Y., R.N. Bamford, A.P. DeFilippis, and T.A. Waldmann. 1996. IL-15: a pleiotropic cytokine with diverse receptor/signaling pathways whose expression is controlled at multiple levels. Immunity. 4:329-336.
24. Oppenheimer-Marks, N., and M. Ziff. 1988. Lymphocyte migration through endothelial cell monolayers: augmentation by gamma interferon. Cell. Immunol. 114:307-323.
25. Rothlein, R., E.A. Mainolfi, M. Czajkowski, and S.D. Marlin. 1991. A form of circulating ICAM-1 in human serum. J. Immunol. 147:3788-3793.
26. Brezinschek, R.I., H.-P. Brezinschek, A. Lazarovits, P.E. Lipsky, and N. Oppenheimer-Marks. 1996. Expression of the beta7 integrin by human endothelial cells. Am. J. Pathol. 149:1651-1660.
27. Dustin, M.L., and T.A. Springer. 1989. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature. 341:619-624.
28. Oppenheimer-Marks, N., and P.E. Lipsky. 1995. Leukocyte adhesion and leukocyte traffic in rheumatoid arthritis. In Mechanisms and Models in Rheumatoid Arthritis. B. Henderson, J.C.W. Edwards, and E.R. Pettipher, editors. Academic Press Ltd., San Diego, CA. 221-239.
29. Sharar, S.R., R.K. Winn, and J.M. Harlan. 1995. The adhesion cascade and anti-adhesion therapy: an overview. Springer Semin. Immunopathol. 16: 359-378.
30. Geppert, T.D., and P.E. Lipsky. 1989. Antigen presentation by cells that are not of bone marrow origin. Regional Immunol. 2:60-71.
31. van Seventer, G.A., Y. Shimizu, K.J. Horgan, and S. Shaw. 1990. The LFA-1 ligand ICAM-1 provides an important costimulatory signal for T cell receptor-mediated activation of resting T cells. J. Immunol. 144:4579-4586.
32. Damle, N.K., and A. Aruffo. 1991. Vascular cell adhesion molecule 1 induces T-cell antigen receptor-dependent activation of CD4+ T lymphocytes. Proc. Natl. Acad. Sci. USA. 88:6403-6407.
33. Karmann, K., C.C. Hughes, J. Schechner, W.C. Fanslow, and J.S. Pober. 1995. CD40 on human endothelial cells: inducibility by cytokines and functional regulation of adhesion molecule expression. Proc. Natl. Acad. Sci. USA. 92: 4342-4346.
34. Mach, F., U. Schönbeck, G.K. Sukhova, T. Bourcier, J.-Y. Bonnefoy, J.S. Pober, and P. Libby. 1997. Functional CD40 ligand is expressed on human vascular endothelial cells, smooth muscle cells, and macrophages: implications for CD40-CD40 ligand signaling in atherosclerosis. Proc. Natl. Acad. Sci. USA. 94:1931-1936.
35. de Jong, J.L.O., N.L. Farner, M.B. Widmer, J.G. Giri, and P.M. Sondel. 1996. Interaction of IL-15 with the shared IL-2 receptor β and γc subunits. J. Immunol. 156:1339-1348.
36. Onu, A., T. Pohl, H. Krause, and S. Bulfone-Paus. 1997. Regulation of IL-15 secretion via the leader peptide of two IL-15 isoforms. J. Immunol 158: 255-262.
37. Kaplan, D.R., C.A., Bergmann, D. Gould, and B. Landmeier. 1988. Membrane-associated interleukin 2 epitopes on the surface of human T lymphocytes. J. Immunol. 140:819-826.
38. Assenmacher, M., A. Schefoold, J, Schmitz, J.A.S. Checa, S. Miltenyi, and A. Radbruch. 1996. Specific expression of surface interferon-γ on interferon-γ producing T cells from mouse and man. Eur. J. Immunol. 26:263-267.
39. Rendt, K.E., T.S. Barry, D.M. Jones, C.B. Richter, S.S. McCachren, and B.F. Haynes. 1993. Engraftment of human synovium into severe combined immune deficient mice. J. Immunol. 151:7324-7336.
40. Sack, U., H. Kuhn, J. Ermann, R.W. Kinne, S. Vogt. D. Jungmichl, and F. Emmrich. 1993. Synovial tissue implants from patients with rheumatoid arthritis cause cartilage destruction in knee joints of SCID.bg mice. J. Rheumatol. 19:10-16.
41. Geiler, T., J. Kriegsmann, G.M. Keyszer, R.E. Gay, and S. Gay. 1994. A new model for rheumatoid synovial tissue and normal human cartilage into SCID mice. Arthritis Rheum. 37:1664-1671.
42. Jorgensen, C., I. Couret, I. Hellier, C. Bologna, F. Canovas, J. Brochier, T. Reme, and J. Sany. 1996. In vivo migration of radiolabeled lymphocytes in rheumatoid synovial tissue engrafted in SCID mice: implication of β2 and β7-integrin. J. Rheumatol. 23:32-35.
43. Muller-Ladner, U., J. Kriegsmann, B.N. Franklin, S. Matsumoto, T. Geiler, R.E. Gay, and S. Gay. 1996. Synovial fibroblasts of patients with rheumatoid arthritis attach to and invade normal human cartilage when engrafted into SCID mice. Am. J. Pathol. 140:1607-1615.
44. Lipsky, P.E., L.S. Davis, J.J. Cush, and N. Oppenheimer-Marks. 1989. The role of cytokines in the pathogenesis of rheumatoid arthritis. Springer Semin. Immunopathol. 11:123-162.
45. Cush, J.J., and P.E. Lipsky. 1988. Phenotypic analysis of synovial tissue and peripheral blood lymphocytes isolated from patients with rheumatoid arthritis. Arthritis Rheum. 31:1230-1238.
46. Kohem, C.L., R.I. Brezinschek, P.E. Lipsky, and N. Oppenheimer-Marks. 1996. Enrichment of differentiated CD27-memory T cells in rheumatoid arthritis blood, synovial fluid and tissue. Arthritis Rheum. 39:844-834.
47. Jorgensen, C., J. Courets, F. Canova, C. Bologna, J. Brochier, T. Reme, P. Lipsky, and J. Sany. 1996. Mononuclear cell retention in rheumatoid synovial tissue engrafted in SCID mice is up-regulated by TNF-α mediated through ICAM-1. Clin. Exp. Immunol. 106:20-25.
48. McInnes, I.B., B.P. Leung, R.D. Sturrock, M. Field, and F.Y. Liew. 1997. Interleukin-15 mediates T cell-dependent regulation of tumor necrosis factor-α production in rheumatoid arthritis. Nat. Med. 3:189-195.