Lung lymphocyte elimination by apoptosis in the murine response to intratracheal particulate antigen

Journal of Clinical Investigation

Volumn 99, Issue 5, 1997, Pages 1082-1091

  Milik, Alicja M ^b   Buechner Maxwell, Virginia A ^b   Sonstein, Joanne ^b   Kim, Sucha ^b   Seitzman, Gerami D ^b   Beals, Ted F ^a,b   Curtis, Jeffrey L ^a,b  

^a VA ANN ARBOR HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

cell survival; cyclosporins; disease models, animal; immune tolerance; T lymphocytes

Indexed keywords

CD3 ANTIGEN; CD4 ANTIGEN; CD45 ANTIGEN; CD8 ANTIGEN; CYCLOSPORIN; DNA FRAGMENT; FAS ANTIGEN; PHOSPHATIDYLSERINE; T LYMPHOCYTE ANTIGEN; THY 1 ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CELL DEATH; CELL STRUCTURE; CONTROLLED STUDY; FEMALE; GENE MUTATION; HOMOZYGOSITY; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; LUNG; LUNG ALVEOLUS CELL; LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SHEEP ERYTHROCYTE;

EID: 0030908930     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119236     Document Type: Article

References (60)

1. Pabst, R., R.M. Binns, S.T. Licence, and M. Peter. 1987. Evidence of a selective major vascular marginal pool of lymphocytes in the lung. Am. Rev. Respir. Dis. 136:1213-1218.
2. Nelson, D., D. Strickland, and P.G. Holt. 1990. Selective attrition of nonrecirculating T cells during normal passage through the lung vascular bed. Immunology. 69:476-481.
3. Weissler, J.C., C.R. Lyons, M.F. Lipscomb, and G.B. Toews. 1986. Human pulmonary macrophages. Functional comparison of cells obtained from whole lung and by bronchoalveolar lavage. Am. Rev. Respir. Dis. 133:473-477.
4. Ettensohn, D.B., P.A. Lalor, and N.J. Roberts, Jr. 1988. Human alveolar macrophage suppression of lymphocyte proliferation. Accessory characteristics for the generation and functional expression of con A-induced suppressor cells. Am. Rev. Respir. Dis. 137:765-773.
5. Holt, P.G. 1979. Alveolar macrophages. III. Studies on the mechanisms of inhibition of T-cell proliferation. Immunology. 37:437-445.
6. 1 to suppress lymphocyte activation. J. Leukocyte Biol. 53:366-371.
7. Harmsen, A.C., B. Muggenburg, M. Snipes, and D. Bice. 1985. The role of macrophages in particle translocation from lungs to lymph nodes. Science (Wash. DC). 230:1277-1280.
8. Thepen, T., N. Van Rooijen, and G. Kraal. 1989. Alveolar macrophage elimination in vivo is associated with an increase in pulmonary immune response in mice. J. Exp. Med. 170:499-509.
9. Sitrin, R.G., M.J. Ansfield, and H.B. Kaltreider. 1985. The effect of pulmonary surface-active material on the generation and expression of murine B-and T-lymphocyte effector functions in vitro. Exp. Lung Res. 9:85-97.
10. Paine, R., III, A. Chavis, D. Gaposchkin, P. Christensen, C.H. Mody, L.A. Turka, and G.B. Toews. 1992. A factor secreted by a human pulmonary alveolar epithelial-like cell line blocks T-cell proliferation between G1 and S phase. Am. J. Respir. Cell Mol. Biol. 6:658-666.
11. Cohen, J.J., R.D. Duke, V.A. Fadok, and K.S. Sellins. 1992. Apoptosis and programmed cell death in immunity. Annu. Rev. Immunol. 10:267-293.
12. Perandones, C.E., V.A. Illera, D. Peckham, L.L. Stunz, and R.F. Ashman. 1993. Regulation of apoptosis in vitro in mature murine spleen T cells. J. Immunol. 151:3521-3529.
13. Wesselborg, S., U. Prüfer, M. Wild, B. Schraven, S.C. Meuer, and D. Kabelitz. 1993. Triggering via the alternative CD2 pathway induces apoptosis in activated human T lymphocytes. Eur. J. Immunol. 23:2707-2710.
14. Schmied, M., H. Breitschopf, R. Gold, H. Zischler, G. Rothe, H. Wekerle, and H. Lassmann. 1993. Apoptosis of T lymphocytes in experimental autoimmune encephalomyelitis: inflammation in the brain. Am. J. Pathol. 143: 446-452.
15. Marrack, P., P. Hugo, J. MeCormack, and J.W. Kappler. 1993. Death and T cells. Immunol. Rev. 133:119-129.
16. Newell, M.K., L.J. Haughn, C.R. Maroun, and M.H. Julius. 1990. Death of mature T cells by separate ligation of CD4 and the T-cell receptor for antigen. Nature (Lond.). 347:286-289.
17. Groux, H., G. Torpier, D. Monte, Y. Mouton, A. Capron, and J.C. Ameisen. 1992. Activation-induced death by apoptosis in CD4+ T cells from human immunodeficiency virus-infected asymptomatic individuals. J. Exp. Med. 175:331-340.
18. Bice, D.E., and G.M. Shopp. 1988. Antibody responses after lung immunization. Exp. Lung Res. 14:133-156.
19. Kaltreider, H.B., J.L. Curtis, and S.M. Arraj. 1987. The mechanism of appearance of specific antibody-forming cells in lungs of inbred mice after intratracheal immunization with sheep erythrocytes. II. Dose-dependence & kinetics. Am. Rev. Respir. Dis. 135:87-92.
20. Curtis, J.L., and H.B. Kaltreider. 1989. Characterization of bronchoalveolar lymphocytes during a specific antibody-forming cell response in the lungs of mice. Am. Rev. Respir. Dis. 139:393-400.
21. Curtis, J.L., M.L. Warnock, S.M. Arraj, and H.B. Kaltreider. 1990. Histologic analysis of an immune response in the lung parenchyma of mice: angiopathy accompanies inflammatory cell influx. Am. J. Pathol. 137:689-699.
22. + T cells during a pulmonary immune response to sheep erythrocytes. Am. J. Respir. Cell Mol. Biol. 12:520-530.
23. Kaltreider, H.B., J.L. Caldwell, and P.K. Byrd. 1986. The capacity of normal murine alveolar macrophages to function as antigen-presenting cells for the initiation of primary antibody-forming cell responses to sheep erythrocytes in vitro. Am. Rev. Respir. Dis. 133:1097-1104.
24. McLeod, E., J. Caldwell, and H.B. Kaltreider. 1978. Pulmonary immune responses of inbred mice: appearance of antibody-forming cells in C57BL/6 mice after intrapulmonary or systemic immunization with sheep erythrocytes. Am. Rev. Respir. Dis. 118:561-571.
25. Urdahl, K.B., D.M. Pardoll, and M.K. Jenkins. 1994. Cyclosporin A inhibits positive selection and delays negative selection in αβ transgenic mice. J. Immunol. 152:2853-2859.
26. Nicoletti, I., G. Migliorati, M. Pagliacci, F. Grignani, and C. Riccardi. 1991. A rapid and simple method for measuring thymocyte apoptosis by propidium iodine staining and flow cytometry. J. Immunol. Method. 139:271-279.
27. Julius, M.H., E. Simpson, and L. A. Herzenberg. 1973. A rapid method for the isolation of functional thymus-derived murine lymphocytes. Eur. J. Immunol. 3:645-649.
28. Gavrieli, Y., Y. Sherman, and S.A. Ben-Sasson. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:493-501.
29. Noguchi, P. 1991. Use of flow cytometry for DNA analysis. In Current Protocols in Immunology. J. Coligan, A. Kruisbeek, D. Margulies, E. Shevach, and W. Strober, editors. John Wiley & Sons, Inc., New York. 5.7.1-5.7.6.
30. Fadok, V.A., D.R. Voelker, P.A. Campbell, J.J. Cohen, D.L. Braton, and P.M. Henson. 1992. Exposure of phophatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148:2207-2216.
31. Vermes, I., C. Haanen, H. Steffens-Nakken, and C. Reutelingsperger. 1995. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labeled Annexin V. J. Immunol. Methods. 184:39-51.
32. Zar, J.H. 1974. Biostatistical Analysis. Prentice-Hall, Englewood Cliffs, NJ. 718 pp.
33. Reimann, J. 1991. Double-negative (CD4-CD8-), TCR αβ-expressing, peripheral T cells. Scand. J. Immunol. 34:679-688.
34. Shi, Y., B.M. Sahai, and D.R. Green. 1989. Cyclosporin A inhibits activation-induced cell death in T-cell hybridomas and thymocytes. Nature (Lond.). 339:625-626.
35. Watanabe-Fukunaga, R., C.I. Brannan, N.G. Copeland, N.A. Jenkins, and S. Nagala. 1992. Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature (Lond.). 356:314-317.
36. Chu, J.L., J. Drappa, A. Parnassa, and K.B. Elkon. 1993. The defect in Fas mRNA expression in MRL/lpr mice is associated with insertion of the retrotransposon, ETn. J. Exp. Med. 178:723-730.
37. Sunderrajan, E.V., W.N. McKenzie, T.R. Lieske, J.L. Kavanaugh, S.R. Braun, and S.E. Walker. 1986. Pulmonary inflammation in autoimmune MRL/ Mp-lpr/lpr mice. Histopathology and bronchoalveolar lavage evaluation. Am. J. Pathol. 124:353-362.
38. Dhein, J., H. Walczk, C. Bäumier, K.-M. Debain, and P.H. Krammer. 1995. Autocrine T-cell suicide mediated by APO-1/(Fas/CD95). Nature (Lond.). 373:438-441.
39. Cohen, P.L., and R.A. Eisenberg. 1991. Lpr and gld: single gene models of systemic autoimmunity and lymphoproliferative disease. Annu. Rev. Immunol. 9:243-269.
40. Okuyama, H., K. Yamamoto, T. Matsunaga, S. Kobayashi, and A. Tashiro. 1986. Analysis of defective delayed-type hypersensitivity in autoimmune mice bearing lpr gene. Clin. Exp. Immunol. 63:87-94.
41. Katagiri, T., T. Mori, T. Nakano, K. Ueno, and K. Kano. 1984. Aberrant expression of Forssman and Paul-Bunnell antigens on lymph node cells of MRL/MP-lpr/lpr mice. J. Immunol. 133:3143-3148.
42. Cohen, D.A., E.A. Fitzpatrick, S.S. Barve, J.M. Guthridge, R.J. Jacob. L. Simmerman, and A.M. Kaplan. 1993. Activation-dependent apoptosis in CD4+ T cells during murine AIDS. Cell. Immunol. 151:392-403.
43. Terai, C., R.S. Kornbluth, C.D. Pauza, D.D. Richman, and D.A. Carson. 1991. Apoptosis as a mechanism of cell death in cultured T lymphoblasts acutely infected with HIV-1. J. Clin. Invest. 87:1710-1715.
44. Curtis, J.L., P.K. Byrd, M.L. Warnock, J.M. Beck, and H.B. Kaltreider. 1993. Pulmonary lymphocyte recruitment: depletion of CD8+ T cells does not impair the pulmonary immune response to intratracheal antigen. Am. J. Respir. Cell Mol. Biol. 9:90-98.
45. Berke, G. 1994. The binding and lysis of target cells by cytotoxic lymphocytes: molecular and cellular aspects. Annu. Rev. Immunol. 12:735-773.
46. Zacharchuk, C.M., M. Mercep, P.K. Chakraborti, S.S. Simons, Jr., and J.D. Ashwell. 1990. Programmed T lymphocyte death. Cell activation-and steroid-induced pathways are mutually antagonistic. J. Immunol. 145:4037-4045.
47. Kennedy, J.D., C.A. Hatfield, S.F. Fidler, G.E. Winterrowd, J.V. Haas, J.E. Cin, and I.M. Richards. 1995. Phenotypic characterization of T lymphocyte emigrating into lung tissue and the airway lumen after antigen inhalation in sensitized mice. Am. J. Respir. Cell Mol. Biol. 12:613-623.
48. Marathias, K.P., F.I. Preffer, C. Pinto, and R.L. Kradin. 1991. Most human pulmonary infiltrating lymphocytes display the surface immune phenotype and functional responses of sensitized T cells. Am. J. Respir. Cell Mol. Biol. 5: 470-476.
49. Holt, P.G., A. Degerbrodt, T. Venaille, C. O'Leary, K. Krska, J. Flexman, H. Farrell, G.R. Shellam, P. Young, J. Penhale, T. Robertson, and J.M. Papadimitriou. 1985. Preparation of interstitial lung cells by enzymatic digestion of tissue slices: preliminary characterization by morphology and performance in functional assays. Immunology. 54:139-147.
50. Chang, J.C.C., L. Zhang, S.G. Distler, G. Ziang, and A.M. Kaplan. 1992. Characterization and function of CD3+ CD4-CD8-TcR-αβ bearing cells infiltrating the lung during the immune response. Reg. Immunol. 4:25-33.
51. Bender, A., and D. Kabelitz. 1990. CD4-CD8-human T cells: phenotypic heterogeneity and activation requirements of freshly isolated "double-negative" T cells. Cell. Immunol. 128:542-554.
52. Shivakumar, S., G. Tsokos, and S. Datta. 1989. T cell receptor αβ expressing double negative (CD4-/CDS-) and CD4+ T helper T cells in humans augment the production of pathogenic anti-DNA autoantibodies associated with lupus nephritis. J. Immunol. 143:103-112.
53. Matsumoto, M., M. Yasukawa, A. Inatsuki, and Y. Kobayashi. 1991. Human double-negative (CD4-CD8-) T cells bearing αβ T cell receptor possess both helper and cytotoxic activities. Clin. Exp. Immunol. 85:525-530.
54. Wang, Z., A. Dudhane, T. Orlikowsky, K. Clarke, X. Li, Z. Darzynkiewicz, and M.K. Hoffmann. 1994. CD4 engagement induces Fas antigen-dependenl apoptosis of Tcells in vivo. Eur. J. Immunol. 24:1549-1552.
55. Malorni, W., R. Rivabene, M.T. Santini, S. Paradisi, F. Iosi, and G. Donelli. 1993. Down-modulation of CD4 antigen during programmed cell death in U937 cells. FEBS Lett. 336:335-339.
56. Pabst, R., and R.M. Binns. 1995. Lymphocytes migrate from the bronchoalveolar space to regional bronchial lymph nodes. Am. J. Respir. Crit. Care Med. 151:495-199.
57. Surh, C.D., and J. Sprent. 1994. T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature (Lond.). 372:100-103.
58. Diamond, B., and M.D. Scharff. 1984. Somatic mutation of the T15 heavy chain gives rise to an antibody with autoantihody specificity. Proc. Natl. Acad. Sci. USA. 81:5841-5844.
59. Savill, J., I. Dransfield, N. Hogg, and C. Haslett. 1990. Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature (Lond.). 143:170-173.
60. Herry, I., M. Bonay, F. Bouchonnet, M.P. Schuller, D. Lecossier, A. Tazi, D.H. Lynch, A.J. Hance. 1996. Extensive apoptosis of lung F-lymphocytes maintained in vitro. Am. J. Respir. Cell Mol. Biol. 15:339-347.