The Collagen Binding α1β1 Integrin VLA-1 Regulates CD8 T Cell-Mediated Immune Protection against Heterologous Influenza Infection

Immunity

Volumn 20, Issue 2, 2004, Pages 167-179

  Ray, Steven J ^a   Franki, Suzanne N ^a   Pierce, Robert H ^a   Dimitrova, Snezhana ^a   Koteliansky, Victor ^b,d   Sprague, Andrew G ^b,d   Doherty, Peter C ^c   De Fougerolles, Antonin R ^b,d   Topham, David J ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b BIOGEN   (United States)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^d ALNYLAM PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; COLLAGEN; VERY LATE ACTIVATION ANTIGEN 1;

ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INFLUENZA; LUNG; LYMPHOID TISSUE; MEMORY CELL; PASSIVE IMMUNIZATION; PRIORITY JOURNAL; PROTEIN BINDING; SPLEEN; T LYMPHOCYTE; TISSUE DISTRIBUTION; ANIMAL; APOPTOSIS; CD8+ T LYMPHOCYTE; CELL ADHESION; FEMALE; FLOW CYTOMETRY; IMMUNOCOMPETENCE; IMMUNOHISTOCHEMISTRY; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE; NICK END LABELING; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; VIROLOGY;

ANIMALS; APOPTOSIS; CD8-POSITIVE T-LYMPHOCYTES; CELL ADHESION; COLLAGEN; FEMALE; FLOW CYTOMETRY; IMMUNOCOMPETENCE; IMMUNOHISTOCHEMISTRY; IMMUNOLOGIC MEMORY; IN SITU NICK-END LABELING; INTEGRIN ALPHA1BETA1; LUNG; LYMPHOCYTE ACTIVATION; MICE; ORTHOMYXOVIRIDAE INFECTIONS; SPLEEN;

EID: 1342308326     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-7613(04)00021-4     Document Type: Article

References (72)

1. Allan W., Tabi Z., Cleary A., Doherty P.C. Cellular events in the lymph node and lung of mice with influenza. Consequences of depleting CD4+ T cells. J. Immunol. 144:1990;3980-3986.
2. Andreasen S.O., Thomsen A.R., Koteliansky V.E., Novobrantseva T.I., Sprague A.G., de Fougerolles A.R., Christensen J.P. Expression and functional importance of collagen-binding integrins, alpha1beta1 and alpha2beta1, on virus-activated T cells. J. Immunol. 171:2003;2804-2811.
3. Aoudjit F., Vuori K. Engagement of the alpha2beta1 integrin inhibits Fas ligand expression and activation-induced cell death in T cells in a focal adhesion kinase-dependent manner. Blood. 95:2000;2044-2051.
4. Arase H., Saito T., Phillips J.H., Lanier L.L. Cutting edge. the mouse NK cell-associated antigen recognized by DX5 monoclonal antibody is CD49b (alpha 2 integrin, very late antigen-2) J. Immunol. 167:2001;1141-1144.
5. Bachmann M.F., Kundig T.M., Hengartner H., Zinkernagel R.M. Protection against immunopathological consequences of a viral infection by activated but not resting cytotoxic T cells. T cell memory without "memory T cells"? Proc. Natl. Acad. Sci. USA. 94:1997;640-645.
6. Bank I., Roth D., Book M., Guterman A., Shnirrer I., Block R., Ehrenfeld M., Langevitz P., Brenner H., Pras M. Expression and functions of very late antigen 1 in inflammatory joint diseases. J. Clin. Immunol. 11:1991;29-38.
7. Belkin V.M., Belkin A.M., Koteliansky V.E. Human smooth muscle VLA-1 integrin. purification, substrate specificity, localization in aorta, and expression during development J. Cell Biol. 111:1990;2159-2170.
8. Belz G.T., Altman J.D., Doherty P.C. Characteristics of virus-specific CD8(+) T cells in the liver during the control and resolution phases of influenza pneumonia. Proc. Natl. Acad. Sci. USA. 95:1998;13812-13817.
9. Belz G.T., Xie W., Altman J.D., Doherty P.C. A previously unrecognized H-2D(b)-restricted peptide prominent in the primary influenza A virus-specific CD8(+) T-cell response is much less apparent following secondary challenge. J. Virol. 74:2000;3486-3493.
10. Bennink J., Effros R.B., Doherty P.C. Influenzal pneumonia. early appearance of cross-reactive T cells in lungs of mice primed with heterologous type A viruses Immunology. 35:1978;503-509.
11. Blankenship J.W., McKinney B.C., Roos P.J., Sandberg L.B. Quantitation of lung elastin and collagen in protein and essential fatty acid malnourished rats. Connect. Tissue Res. 29:1993;311-318.
12. Butcher E.C., Picker L.J. Lymphocyte homing and homeostasis. Science. 272:1996;60-66.
13. Darzynkiewicz Z., Bruno S., Del Bino G., Gorczyca W., Hotz M.A., Lassota P., Traganos F. Features of apoptotic cells measured by flow cytometry. Cytometry. 13:1992;795-808.
14. de Fougerolles A.R., Sprague A.G., Nickerson-Nutter C.L., Chi-Rosso G., Rennert P.D., Gardner H., Gotwals P.J., Lobb R.R., Koteliansky V.E. Regulation of inflammation by collagen-binding integrins alpha1beta1 and alpha2beta1 in models of hypersensitivity and arthritis. J. Clin. Invest. 105:2000;721-729.
15. Doherty P.C., Topham D.J., Tripp R.A. Establishment and persistence of virus-specific CD4+ and CD8+ T cell memory. Immunol. Rev. 150:1996;23-44.
16. Doherty P.C., Hamilton-Easton A.M., Topham D.J., Riberdy J., Brooks J.W., Cardin R.D. Consequences of viral infections for lymphocyte compartmentalization and homeostasis. Semin. Immunol. 9:1997;365-373.
17. Doherty P.C., Riberdy J.M., Belz G.T. Quantitative analysis of the CD8+ T-cell response to readily eliminated and persistent viruses. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355:2000;1093-1101.
18. Dustin M.L., de Fougerolles A.R. Reprogramming T cells. the role of extracellular matrix in coordination of T cell activation and migration Curr. Opin. Immunol. 13:2001;286-290.
19. Effros R.B., Doherty P.C., Gerhard W., Bennink J. Generation of both cross-reactive and virus-specific T-cell populations after immunization with serologically distinct influenza A viruses. J. Exp. Med. 145:1977;557-568.
20. Effros R.B., Bennink J., Doherty P.C. Characteristics of secondary cytotoxic T-cell responses in mice infected with influenza A viruses. Cell. Immunol. 36:1978;345-353.
21. Ennis F.A., Verbonitz M., Reichelderfer P., Daniel S. Recombination of influenza A virus strains. effect on pathogenicity Dev. Biol. Stand. 33:1976;220-225.
22. Flynn K.J., Belz G.T., Altman J.D., Ahmed R., Woodland D.L., Doherty P.C. Virus-specific CD8+ T cells in primary and secondary influenza pneumonia. Immunity. 8:1998;683-691.
23. Frisch S.M., Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 124:1994;619-626.
24. Gardner H., Kreidberg J., Koteliansky V., Jaenisch R. Deletion of integrin alpha 1 by homologous recombination permits normal murine development but gives rise to a specific deficit in cell adhesion. Dev. Biol. (Orlando). 175:1996;301-313.
25. Goldman R., Harvey J., Hogg N. VLA-2 is the integrin used as a collagen receptor by leukocytes. Eur. J. Immunol. 22:1992;1109-1114.
26. Gomori G. A rapid one-step trichrome stain. Am. J. Clin. Pathol. 20:1950;661-664.
27. Gretz J.E., Kaldjian E.P., Anderson A.O., Shaw S. Sophisticated strategies for information encounter in the lymph node. the reticular network as a conduit of soluble information and a highway for cell traffic J. Immunol. 157:1996;495-499.
28. Gretz J.E., Norbury C.C., Anderson A.O., Proudfoot A.E., Shaw S. Lymph-borne chemokines and other low molecular weight molecules reach high endothelial venules via specialized conduits while a functional barrier limits access to the lymphocyte microenvironments in lymph node cortex. J. Exp. Med. 192:2000;1425-1440.
29. Gunzer M., Schafer A., Borgmann S., Grabbe S., Zanker K.S., Brocker E.B., Kampgen E., Friedl P. Antigen presentation in extracellular matrix. interactions of T cells with dendritic cells are dynamic, short lived, and sequential Immunity. 13:2000;323-332.
30. Hemler M.E. VLA proteins in the integrin family. structures, functions, and their role on leukocytes Annu. Rev. Immunol. 8:1990;365-400.
31. Hemler M.E., Jacobson J.G. Cell matrix adhesion-related proteins VLA-1 and VLA-2. regulation of expression on T cells J. Immunol. 138:1987;2941-2948.
32. Hemler M.E., Jacobson J.G., Brenner M.B., Mann D., Strominger J.L. VLA-1. a t cell surface antigen which defines a novel late stage of human t cell activation Eur. J. Immunol. 15:1985;502-508.
33. Hemler M.E., Glass D., Coblyn J.S., Jacobson J.G. Very late activation antigens on rheumatoid synovial fluid T lymphocytes. Association with stages of T cell activation. J. Clin. Invest. 78:1986;696-702.
34. Hernandez-Pando R., Rook G.A. The role of TNF-alpha in T-cell-mediated inflammation depends on the Th1/Th2 cytokine balance. Immunology. 82:1994;591-595.
35. Hogan R.J., Usherwood E.J., Zhong W., Roberts A.A., Dutton R.W., Harmsen A.G., Woodland D.L. Activated antigen-specific CD8+ T cells persist in the lungs following recovery from respiratory virus infections. J. Immunol. 166:2001;1813-1822. a.
36. Hogan R.J., Zhong W., Usherwood E.J., Cookenham T., Roberts A.D., Woodland D.L. Protection from respiratory virus infections can be mediated by antigen-specific CD4(+) T cells that persist in the lungs. J. Exp. Med. 193:2001;981-986. b.
37. Ianaro A., Cicala C., Calignano A., Koteliansky V., Gotwals P., Bucci M., Gerli R., Santucci L., Fiorucci S., Cirino G. Anti-very late antigen-1 monoclonal antibody modulates the development of secondary lesion and T-cell response in experimental arthritis. Lab. Invest. 80:2000;73-80.
38. Kambayashi T., Assarsson E., Chambers B.J., Ljunggren H.G. Expression of the DX5 antigen on CD8+ T cells is associated with activation and subsequent cell death or memory during influenza virus infection. Eur. J. Immunol. 31:2001;1523-1530.
39. Kunkel E.J., Butcher E.C. Chemokines and the tissue-specific migration of lymphocytes. Immunity. 16:2002;1-4.
40. Laver W.G., Bischofberger N., Webster R.G. The origin and control of pandemic influenza. Perspect. Biol. Med. 43:2000;173-192.
41. Liang S., Mozdzanowska K., Palladino G., Gerhard W. Heterosubtypic immunity to influenza type A virus in mice. Effector mechanisms and their longevity. J. Immunol. 152:1994;1653-1661.
42. Lohman B.L., Razvi E.S., Welsh R.M. T-lymphocyte downregulation after acute viral infection is not dependent on CD95 (Fas) receptor-ligand interactions. J. Virol. 70:1996;8199-8203.
43. Mackay C.R., Marston W.L., Dudler L., Spertini O., Tedder T.F., Hein W.R. Tissue-specific migration pathways by phenotypically distinct subpopulations of memory T cells. Eur. J. Immunol. 22:1992;887-895.
44. Marshall D.R., Turner S.J., Belz G.T., Wingo S., Andreansky S., Sangster M.Y., Riberdy J.M., Liu T., Tan M., Doherty P.C. Measuring the diaspora for virus-specific CD8+ T cells. Proc. Natl. Acad. Sci. USA. 98:2001;6313-6318.
45. Masopust D., Vezys V., Marzo A.L., Lefrancois L. Preferential localization of effector memory cells in nonlymphoid tissue. Science. 291:2001;2413-2417.
46. Mendrick D.L., Kelly D.M., duMont S.S., Sandstrom D.J. Glomerular epithelial and mesangial cells differentially modulate the binding specificities of VLA-1 and VLA-2. Lab. Invest. 72:1995;367-375.
47. Miner J.H., Sanes J.R. Collagen IV alpha 3, alpha 4, and alpha 5 chains in rodent basal laminae. sequence, distribution, association with laminins, and developmental switches J. Cell Biol. 127:1994;879-891.
48. Munoz F.M., Galasso G.J., Gwaltney J.M. Jr., Hayden F.G., Murphy B., Webster R., Wright P., Couch R.B. Current research on influenza and other respiratory viruses. II international symposium Antiviral Res. 46:2000;91-124.
49. Razvi E.S., Jiang Z., Woda B.A., Welsh R.M. Lymphocyte apoptosis during the silencing of the immune response to acute viral infections in normal, lpr, and Bcl-2-transgenic mice. Am. J. Pathol. 147:1995;79-91.
50. Reinhardt R.L., Khoruts A., Merica R., Zell T., Jenkins M.K. Visualizing the generation of memory CD4 T cells in the whole body. Nature. 410:2001;101-105.
51. Sad S., Mosmann T.R. Single IL-2-secreting precursor CD4 T cell can develop into either Th1 or Th2 cytokine secretion phenotype. J. Immunol. 153:1994;3514-3522.
52. Sado Y., Kagawa M., Naito I., Ueki Y., Seki T., Momota R., Oohashi T., Ninomiya Y. Organization and expression of basement membrane collagen IV genes and their roles in human disorders. J. Biochem. (Tokyo). 123:1998;767-776.
53. Sallusto F., Lenig D., Forster R., Lipp M., Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature. 401:1999;708-712.
54. Saltini C., Hemler M.E., Crystal R.G. T lymphocytes compartmentalized on the epithelial surface of the lower respiratory tract express the very late activation antigen complex VLA-1. Clin. Immunol. Immunopathol. 46:1988;221-233.
55. Seki N., Sudo Y., Yamane A., Sugihara S., Takai Y., Ishihara K., Ono S., Hamaoka T., Senoh H., Fujiwara H. Type II collagen-induced murine arthritis. II. Genetic control of arthritis induction is expressed on L3T4+ T cells required for humoral as well as cell-mediated immune responses to type II collagen. Reg. Immunol. 2:1989;203-212.
56. Shields J.M., Haston W., Wilkinson P.C. Invasion of collagen gels by mouse lymphoid cells. Immunology. 51:1984;259-268.
57. Stemme S., Holm J., Hansson G.K. T lymphocytes in human atherosclerotic plaques are memory cells expressing CD45RO and the integrin VLA-1. Arterioscler. Thromb. 12:1992;206-211.
58. Takahashi H., Soderstrom K., Nilsson E., Kiessling R., Patarroyo M. Integrins and other adhesion molecules on lymphocytes from synovial fluid and peripheral blood of rheumatoid arthritis patients. Eur. J. Immunol. 22:1992;2879-2885.
59. Tite J.P., Hughes-Jenkins C., O'Callaghan D., Dougan G., Russell S.M., Gao X.M., Liew F.Y. Anti-viral immunity induced by recombinant nucleoprotein of influenza A virus. II. Protection from influenza infection and mechanism of protection. Immunology. 71:1990;202-207.
60. Topham D.J., Doherty P.C. Clearance of an influenza A virus by CD4+ T cells is inefficient in the absence of B cells. J. Virol. 72:1998;882-885.
61. Topham D.J., Castrucci M.R., Wingo F.S., Belz G.T., Doherty P.C. The role of antigen in the localization of naive, acutely activated, and memory CD8(+) T cells to the lung during influenza pneumonia. J. Immunol. 167:2001;6983-6990.
62. Tripp R.A., Hou S., McMickle A., Houston J., Doherty P.C. Recruitment and proliferation of CD8+ T cells in respiratory virus infections. J. Immunol. 154:1995;6013-6021. a.
63. Tripp R.A., Sarawar S.R., Doherty P.C. Characteristics of the influenza virus-specific CD8+ T cell response in mice homozygous for disruption of the H-2lAb gene. J. Immunol. 155:1995;2955-2959. b.
64. van Kuppevelt T.H., Veerkamp J.H., Timmermans J.A. Immunoquantification of type I, III, IV and V collagen in small samples of human lung parenchyma. Int. J. Biochem. Cell Biol. 27:1995;775-782.
65. Van Parijs L., Abbas A.K. Homeostasis and self-tolerance in the immune system. turning lymphocytes off Science. 280:1998;243-248.
66. Wang X., Mosmann T. In vivo priming of CD4 T cells that produce interleukin (IL)-2 but not IL-4 or interferon (IFN)-gamma, and can subsequently differentiate into IL-4- or IFN-gamma-secreting Cells. J. Exp. Med. 194:2001;1069-1080.
67. Wang X.Z., Stepp S.E., Brehm M.A., Chen H.D., Selin L.K., Welsh R.M. Virus-specific CD8 T cells in peripheral tissues are more resistant to apoptosis than those in lymphoid organs. Immunity. 18:2003;631-642.
68. Webster R.G. Influenza. an emerging disease Emerg. Infect. Dis. 4:1998;436-441.
69. Wherry E.J., Teichgraber V., Becker T.C., Masopust D., Kaech S.M., Antia R., von Andrian U.H., Ahmed R. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat. Immunol. 4:2003;225-234.
70. Wiley J.A., Hogan R.J., Woodland D.L., Harmsen A.G. Antigen-specific CD8(+) T cells persist in the upper respiratory tract following influenza virus infection. J. Immunol. 167:2001;3293-3299.
71. Yewdell J.W., Bennink J.R., Smith G.L., Moss B. Influenza A virus nucleoprotein is a major target antigen for cross-reactive anti-influenza A virus cytotoxic T lymphocytes. Proc. Natl. Acad. Sci. USA. 82:1985;1785-1789.
72. Young A.J. The physiology of lymphocyte migration through the single lymph node in vivo. Semin. Immunol. 11:1999;73-83.