Mechanism of suppression of cell-mediated immunity by measles virus

Science

Volumn 273, Issue 5272, 1996, Pages 228-231

  Karp, Christopher L ^a   Wysocka, Maria ^b   Wahl, Larry M ^c   Ahearn, Joseph M ^a   Cuomo, Peter J ^a   Sherry, Barbara ^d   Trinchieri, Giorgio ^b   Griffin, Diane E ^e  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WISTAR INSTITUTE   (United States)

^c NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^d PICOWER INST FOR MEDICAL RESEARCH   (United States)

^e JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; INTERLEUKIN 12;

ARTICLE; CELLULAR IMMUNITY; COMPLEMENT SYSTEM; IMMUNOPATHOGENESIS; IMMUNOSUPPRESSIVE TREATMENT; MEASLES; PRIORITY JOURNAL; VIRUS INFECTIVITY;

EID: 0029818545     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.273.5272.228     Document Type: Article

References (64)

1. F. Assaad,Rev. Infect. Dis. 5, 452 (1983); J. P. Grant, The State of the World's Children 1990 (United Nations Children's Fund, Oxford Univ. Press, Oxford, 1990); B. R. Bloom, Nature 342, 115 (1989).
2. F. Assaad,Rev. Infect. Dis. 5, 452 (1983); J. P. Grant, The State of the World's Children 1990 (United Nations Children's Fund, Oxford Univ. Press, Oxford, 1990); B. R. Bloom, Nature 342, 115 (1989).
3. F. Assaad,Rev. Infect. Dis. 5, 452 (1983); J. P. Grant, The State of the World's Children 1990 (United Nations Children's Fund, Oxford Univ. Press, Oxford, 1990); B. R. Bloom, Nature 342, 115 (1989).
4. C. von Pirquet, Dtsch. Med. Wochenschr. 30, 1297 (1908); V. G. Tamashiro, H. H. Perez, D. E. Griffin, Pediatr. Infect. Dis. J. 6, 451 (1987).
5. C. von Pirquet, Dtsch. Med. Wochenschr. 30, 1297 (1908); V. G. Tamashiro, H. H. Perez, D. E. Griffin, Pediatr. Infect. Dis. J. 6, 451 (1987).
6. H. C. Whittle, J. Dossetor, A. Oduloju, A. D. M. Bryceson, B. M. Greenwood, J. Clin. Invest. 62, 678 (1978); P. Arneborn and G. Biberfeld, Infect. Immun. 39, 29 (1983); R. L. Hirsch et al., Clin. Immunol. Immunopathol. 31, 1 (1984); D. E. Griffin, B. J. Ward, E. Jauregui, R. T. Johnson, A. Vaisberg, Clin. Exp. Immunol. 81, 218 (1990).
7. H. C. Whittle, J. Dossetor, A. Oduloju, A. D. M. Bryceson, B. M. Greenwood, J. Clin. Invest. 62, 678 (1978); P. Arneborn and G. Biberfeld, Infect. Immun. 39, 29 (1983); R. L. Hirsch et al., Clin. Immunol. Immunopathol. 31, 1 (1984); D. E. Griffin, B. J. Ward, E. Jauregui, R. T. Johnson, A. Vaisberg, Clin. Exp. Immunol. 81, 218 (1990).
8. H. C. Whittle, J. Dossetor, A. Oduloju, A. D. M. Bryceson, B. M. Greenwood, J. Clin. Invest. 62, 678 (1978); P. Arneborn and G. Biberfeld, Infect. Immun. 39, 29 (1983); R. L. Hirsch et al., Clin. Immunol. Immunopathol. 31, 1 (1984); D. E. Griffin, B. J. Ward, E. Jauregui, R. T. Johnson, A. Vaisberg, Clin. Exp. Immunol. 81, 218 (1990).
9. H. C. Whittle, J. Dossetor, A. Oduloju, A. D. M. Bryceson, B. M. Greenwood, J. Clin. Invest. 62, 678 (1978); P. Arneborn and G. Biberfeld, Infect. Immun. 39, 29 (1983); R. L. Hirsch et al., Clin. Immunol. Immunopathol. 31, 1 (1984); D. E. Griffin, B. J. Ward, E. Jauregui, R. T. Johnson, A. Vaisberg, Clin. Exp. Immunol. 81, 218 (1990).
10. D. E. Griffin and B. J. Ward, J. Infect. Dis. 168, 275 (1993).
11. R. L. Hirsch et al., Clin. Immunol. Immunopathol. 21, 341 (1981); B. Zweiman, D. Pappagianis, H. Maibach, E. A. Hildreth, Int. Arch. Allergy Appl. Immunol. 40, 834 (1971); B. J. Ward and D. E. Griffin, Clin. Immunol. Immunopathol. 67, 171 (1993).
12. R. L. Hirsch et al., Clin. Immunol. Immunopathol. 21, 341 (1981); B. Zweiman, D. Pappagianis, H. Maibach, E. A. Hildreth, Int. Arch. Allergy Appl. Immunol. 40, 834 (1971); B. J. Ward and D. E. Griffin, Clin. Immunol. Immunopathol. 67, 171 (1993).
13. R. L. Hirsch et al., Clin. Immunol. Immunopathol. 21, 341 (1981); B. Zweiman, D. Pappagianis, H. Maibach, E. A. Hildreth, Int. Arch. Allergy Appl. Immunol. 40, 834 (1971); B. J. Ward and D. E. Griffin, Clin. Immunol. Immunopathol. 67, 171 (1993).
14. G. Trinchieri, Annu. Rev. Immunol. 13, 251 (1995).
15. _, Blood 84, 4008 (1994); G. Muller et al., J. Immunol. 155, 4661 (1995).
16. _, Blood 84, 4008 (1994); G. Muller et al., J. Immunol. 155, 4661 (1995).
17. R. T. Gazzinelli, S. H. Hieny, T. A. Wynn, S. Wolf, A. Sher, Proc. Natl. Acad. Sci. U.S.A. 90, 6115 (1993).
18. L. M. Esolen, B. J. Ward, T. R. Moench, D. E. Griffin, J. Infect. Dis. 169, 47 (1993); T. R. Moench, D. E. Griffin, C. R. Obriecht, A. J. Vaisberg, R. T. Johnson, ibid. 158, 433 (1988).
19. L. M. Esolen, B. J. Ward, T. R. Moench, D. E. Griffin, J. Infect. Dis. 169, 47 (1993); T. R. Moench, D. E. Griffin, C. R. Obriecht, A. J. Vaisberg, R. T. Johnson, ibid. 158, 433 (1988).
20. L. M. Wahl et al., Cell. Immunol. 85, 373 (1984); P. M. Mertz, D. L. DeWitt, W. G. Stetler-Stevenson, L. M. Wahl, J. Biol. Chem. 269, 21322 (1994).
21. L. M. Wahl et al., Cell. Immunol. 85, 373 (1984); P. M. Mertz, D. L. DeWitt, W. G. Stetler-Stevenson, L. M. Wahl, J. Biol. Chem. 269, 21322 (1994).
22. 6 cells/ml (1 ml per data point) in 24-well plates (Costar). Isolation and culture were performed under LPS-free conditions (12). After 48 to 60 hours in culture, monocytes were stimulated with LPS (1 μg/ml) (Escherichia coli serotype O127:B8; Sigma) or SAC (0.0075%) (Calbiochem), with or without 18 hours of prestimulation with IFN-γ (300 U/ml) (Pharmingen). Twenty-four hours later, cell-free culture supernatants were harvested for measurement of cytokines. IL-12 p40 and p70 levels were measured by specific radioimmunoassays (RIAs) as previously described [A. D'Andrea et al., J. Exp. Med. 176, 1387 (1992)]. p40 was measured with the use of mAb pair C11.79 and C8.6, and p70 was measured with mAb pair 20C2 and C8.6. Both RIAs have a sensitivity of 10 pg/ml. In the absence of stimulation, there was no detectable secretion of IL-12.
23. 21) (XOMA) had an LPS-neutralizing capacity of >10 ng/ml [K. Meszaros et al., J. Leukocyte Biol. 54, 558 (1993); C. L. Karp, unpublished data]. At experimental dilutions, all reagents contained LPS amounts considerably less than 10 ng/ml.
24. 21) (XOMA) had an LPS-neutralizing capacity of >10 ng/ml [K. Meszaros et al., J. Leukocyte Biol. 54, 558 (1993); C. L. Karp, unpublished data]. At experimental dilutions, all reagents contained LPS amounts considerably less than 10 ng/ml.
25. 21) (XOMA) had an LPS-neutralizing capacity of >10 ng/ml [K. Meszaros et al., J. Leukocyte Biol. 54, 558 (1993); C. L. Karp, unpublished data]. At experimental dilutions, all reagents contained LPS amounts considerably less than 10 ng/ml.
26. 21) (XOMA) had an LPS-neutralizing capacity of >10 ng/ml [K. Meszaros et al., J. Leukocyte Biol. 54, 558 (1993); C. L. Karp, unpublished data]. At experimental dilutions, all reagents contained LPS amounts considerably less than 10 ng/ml.
27. 21) (XOMA) had an LPS-neutralizing capacity of >10 ng/ml [K. Meszaros et al., J. Leukocyte Biol. 54, 558 (1993); C. L. Karp, unpublished data]. At experimental dilutions, all reagents contained LPS amounts considerably less than 10 ng/ml.
28. Unlike peripheral blood mononuclear cells or adherence-purified monocytes (6), the production of p70 (as opposed to p40) by elutriated human monocytes is dependent on preincubation with IFN-γ (C. L. Karp, unpublished data).
29. MV strains tested in addition to wild-type Edmonston included a Finnish wild-type isolate (courtesy of A. Salmi) [R. Vainionpaa, B. Ziola, A. A. Salmi, Acta Pathol. Microbiol. Immunol. Scand. B 86, 379 (1978)], as well as JM and Chicago-1 (courtesy of P. Rota).
30. MV preparations (and uninfected Vero cell lysates) were inactivated by short-wave UV irradiation for 55 min in the cold. After irradiation, stocks were kept at 4°C for at least 3 hours and were subsequently frozen before use. Such stocks were used to treat monocytes (11) at a (preirradiation) MOI of 5.
31. TNF-α and IL-6 were measured by ELISA (Pharmingen); ELISA measurement of MIP-1α and MIP-1β was done as previously described [H. Schmidtmayerova et al., Proc. Natl. Acad. Sci. U.S.A. 93, 700 (1996)].
32. D. G. Mayernik, A. Haq, J. J. Rinehart, J. Leukocyte Biol. 36, 551 (1984).
33. G. Zurawski and J. E. de Vries, Immunol. Today 15, 19 (1994); S. K. Durum and J. J. Oppenheim, in Fundamental Immunology, W. E. Paul, Ed. (Raven, New York, ed. 3, 1993), pp. 801-833.
34. G. Zurawski and J. E. de Vries, Immunol. Today 15, 19 (1994); S. K. Durum and J. J. Oppenheim, in Fundamental Immunology, W. E. Paul, Ed. (Raven, New York, ed. 3, 1993), pp. 801-833.
35. IL-10 was measured by ELISA (Pharmingen).
36. MV- or mock-infected monocytes were stimulated with IFN-γ-LPS or IFN-γ-SAC in the presence of a neutralizing mAb to IL-10 or of an isotype control (both from Pharmingen).
37. Neutralizing rabbit polyclonal (R & D Systems) and monoclonal (Genzyme) antibodies to TGF-β were used with appropriate isotype control antibodies from the same manufacturers.
38. PGE2 measurement was by RIA as previously described [L. M. Wahl, in Manual of Macrophage Methodology, H. B. Herscowitz, H. T. Holden, J. A. Bellanti, A Ghaffar, Eds. (Dekker, New York, 1981), pp. 423-429].
39. IL-4 measurement was by means of an ELISA with a sensitivity of 10 to 20 pg/ml (Pharmingen). IL-13 was measured by RT-PCR at 40 cycles [C. L. Karp et al., J. Clin. Invest. 91, 1644 (1993)].
40. D. Naniche et al., J. Virol. 67, 6025 (1993); R. E. Dorig, A. Marcil, A. Chopra, C. D. Richardson, Cell 75, 295 (1993).
41. D. Naniche et al., J. Virol. 67, 6025 (1993); R. E. Dorig, A. Marcil, A. Chopra, C. D. Richardson, Cell 75, 295 (1993).
42. M. K. Liszewski, T. W. Post, J. P. Atkinson, Annu. Rev. Immunol. 9, 431 (1991).
43. D. Gerlier et al., J. Gen. Virol. 75, 2163 (1994); O. Nussbaum et al., J. Virol. 69, 3341 (1995); M. Manchester et al., Proc. Natl. Acad. Sci. U.S.A. 92, 2303 (1995); E. M. Adams, M. C. Brown, M. Nunge, M. Krych, J. P. Atkinson, J. Immunol. 147, 3005 (1991).
44. D. Gerlier et al., J. Gen. Virol. 75, 2163 (1994); O. Nussbaum et al., J. Virol. 69, 3341 (1995); M. Manchester et al., Proc. Natl. Acad. Sci. U.S.A. 92, 2303 (1995); E. M. Adams, M. C. Brown, M. Nunge, M. Krych, J. P. Atkinson, J. Immunol. 147, 3005 (1991).
45. D. Gerlier et al., J. Gen. Virol. 75, 2163 (1994); O. Nussbaum et al., J. Virol. 69, 3341 (1995); M. Manchester et al., Proc. Natl. Acad. Sci. U.S.A. 92, 2303 (1995); E. M. Adams, M. C. Brown, M. Nunge, M. Krych, J. P. Atkinson, J. Immunol. 147, 3005 (1991).
46. D. Gerlier et al., J. Gen. Virol. 75, 2163 (1994); O. Nussbaum et al., J. Virol. 69, 3341 (1995); M. Manchester et al., Proc. Natl. Acad. Sci. U.S.A. 92, 2303 (1995); E. M. Adams, M. C. Brown, M. Nunge, M. Krych, J. P. Atkinson, J. Immunol. 147, 3005 (1991).
47. M. Manchester et al., Proc. Natl. Acad. Sci. U.S.A. 92, 2303 (1995); R. E. Dorig, A. Marcil, A. Chopra, C. D. Richardson, Cell 75, 295 (1993); S. W. Cho, T. J. Oglesby, B. L. Hsi, E. M. Adams, J. P. Atkinson, Clin. Exp. Immunol. 83, 257 (1991).
48. M. Manchester et al., Proc. Natl. Acad. Sci. U.S.A. 92, 2303 (1995); R. E. Dorig, A. Marcil, A. Chopra, C. D. Richardson, Cell 75, 295 (1993); S. W. Cho, T. J. Oglesby, B. L. Hsi, E. M. Adams, J. P. Atkinson, Clin. Exp. Immunol. 83, 257 (1991).
49. M. Manchester et al., Proc. Natl. Acad. Sci. U.S.A. 92, 2303 (1995); R. E. Dorig, A. Marcil, A. Chopra, C. D. Richardson, Cell 75, 295 (1993); S. W. Cho, T. J. Oglesby, B. L. Hsi, E. M. Adams, J. P. Atkinson, Clin. Exp. Immunol. 83, 257 (1991).
50. 1&.
51. K. R. Kalli et al., J. Exp. Med. 174, 1451 (1991).
52. D. T. Fearon and R. H. Carter, Annu. Rev. Immunol. 13, 127 (1995).
53. S. J. James, Microbiol. Rev. 59, 533 (1995).
54. M. S. Hirsch and J. Curran, in Virology, B. N. Fields et al., Eds. (Lippincott-Raven, Philadelphia, PA, ed. 3, 1996), pp. 1953-1973.
55. J. Chehimi et al., J. Exp. Med. 179, 1361 (1994).
56. C. F. Ebenbichler et al., ibid 174, 1417 (1991); N. M. Thielens, I. M. Bally, C. F. Ebenbichler, M. P. Dierich, G. J. Arlaud, J. Immunol. 151, 6583 (1993); N. Thieblemont, N. Haeffner-Cavaillon, L. Weiss, F. Maillet, M. D. Kazatchkine, AIDS Res. Hum. Retrovir. 9, 229 (1993); H. Stoiber, R. Schneider, J. Janatova, M. P. Dierich, Immunobiology 193, 98 (1995). B. M. Solder, Immunol. Lett 22, 135 (1989); G. T. Spear, A. L. Landay, B. L. Sullivan, B. Dittel, T. F. Lint, J. Immunol. 144, 1490 (1990); P. Marschang et al., AIDS 7, 903 (1993); M. P. Dierich et al., Immunol. Today 14, 435 (1993).
57. C. F. Ebenbichler et al., ibid 174, 1417 (1991); N. M. Thielens, I. M. Bally, C. F. Ebenbichler, M. P. Dierich, G. J. Arlaud, J. Immunol. 151, 6583 (1993); N. Thieblemont, N. Haeffner-Cavaillon, L. Weiss, F. Maillet, M. D. Kazatchkine, AIDS Res. Hum. Retrovir. 9, 229 (1993); H. Stoiber, R. Schneider, J. Janatova, M. P. Dierich, Immunobiology 193, 98 (1995). B. M. Solder, Immunol. Lett 22, 135 (1989); G. T. Spear, A. L. Landay, B. L. Sullivan, B. Dittel, T. F. Lint, J. Immunol. 144, 1490 (1990); P. Marschang et al., AIDS 7, 903 (1993); M. P. Dierich et al., Immunol. Today 14, 435 (1993).
58. C. F. Ebenbichler et al., ibid 174, 1417 (1991); N. M. Thielens, I. M. Bally, C. F. Ebenbichler, M. P. Dierich, G. J. Arlaud, J. Immunol. 151, 6583 (1993); N. Thieblemont, N. Haeffner-Cavaillon, L. Weiss, F. Maillet, M. D. Kazatchkine, AIDS Res. Hum. Retrovir. 9, 229 (1993); H. Stoiber, R. Schneider, J. Janatova, M. P. Dierich, Immunobiology 193, 98 (1995). B. M. Solder, Immunol. Lett 22, 135 (1989); G. T. Spear, A. L. Landay, B. L. Sullivan, B. Dittel, T. F. Lint, J. Immunol. 144, 1490 (1990); P. Marschang et al., AIDS 7, 903 (1993); M. P. Dierich et al., Immunol. Today 14, 435 (1993).
59. C. F. Ebenbichler et al., ibid 174, 1417 (1991); N. M. Thielens, I. M. Bally, C. F. Ebenbichler, M. P. Dierich, G. J. Arlaud, J. Immunol. 151, 6583 (1993); N. Thieblemont, N. Haeffner-Cavaillon, L. Weiss, F. Maillet, M. D. Kazatchkine, AIDS Res. Hum. Retrovir. 9, 229 (1993); H. Stoiber, R. Schneider, J. Janatova, M. P. Dierich, Immunobiology 193, 98 (1995). B. M. Solder, Immunol. Lett 22, 135 (1989); G. T. Spear, A. L. Landay, B. L. Sullivan, B. Dittel, T. F. Lint, J. Immunol. 144, 1490 (1990); P. Marschang et al., AIDS 7, 903 (1993); M. P. Dierich et al., Immunol. Today 14, 435 (1993).
60. C. F. Ebenbichler et al., ibid 174, 1417 (1991); N. M. Thielens, I. M. Bally, C. F. Ebenbichler, M. P. Dierich, G. J. Arlaud, J. Immunol. 151, 6583 (1993); N. Thieblemont, N. Haeffner-Cavaillon, L. Weiss, F. Maillet, M. D. Kazatchkine, AIDS Res. Hum. Retrovir. 9, 229 (1993); H. Stoiber, R. Schneider, J. Janatova, M. P. Dierich, Immunobiology 193, 98 (1995). B. M. Solder, Immunol. Lett 22, 135 (1989); G. T. Spear, A. L. Landay, B. L. Sullivan, B. Dittel, T. F. Lint, J. Immunol. 144, 1490 (1990); P. Marschang et al., AIDS 7, 903 (1993); M. P. Dierich et al., Immunol. Today 14, 435 (1993).
61. C. F. Ebenbichler et al., ibid 174, 1417 (1991); N. M. Thielens, I. M. Bally, C. F. Ebenbichler, M. P. Dierich, G. J. Arlaud, J. Immunol. 151, 6583 (1993); N. Thieblemont, N. Haeffner-Cavaillon, L. Weiss, F. Maillet, M. D. Kazatchkine, AIDS Res. Hum. Retrovir. 9, 229 (1993); H. Stoiber, R. Schneider, J. Janatova, M. P. Dierich, Immunobiology 193, 98 (1995). B. M. Solder, Immunol. Lett 22, 135 (1989); G. T. Spear, A. L. Landay, B. L. Sullivan, B. Dittel, T. F. Lint, J. Immunol. 144, 1490 (1990); P. Marschang et al., AIDS 7, 903 (1993); M. P. Dierich et al., Immunol. Today 14, 435 (1993).
62. C. F. Ebenbichler et al., ibid 174, 1417 (1991); N. M. Thielens, I. M. Bally, C. F. Ebenbichler, M. P. Dierich, G. J. Arlaud, J. Immunol. 151, 6583 (1993); N. Thieblemont, N. Haeffner-Cavaillon, L. Weiss, F. Maillet, M. D. Kazatchkine, AIDS Res. Hum. Retrovir. 9, 229 (1993); H. Stoiber, R. Schneider, J. Janatova, M. P. Dierich, Immunobiology 193, 98 (1995). B. M. Solder, Immunol. Lett 22, 135 (1989); G. T. Spear, A. L. Landay, B. L. Sullivan, B. Dittel, T. F. Lint, J. Immunol. 144, 1490 (1990); P. Marschang et al., AIDS 7, 903 (1993); M. P. Dierich et al., Immunol. Today 14, 435 (1993).
63. C. F. Ebenbichler et al., ibid 174, 1417 (1991); N. M. Thielens, I. M. Bally, C. F. Ebenbichler, M. P. Dierich, G. J. Arlaud, J. Immunol. 151, 6583 (1993); N. Thieblemont, N. Haeffner-Cavaillon, L. Weiss, F. Maillet, M. D. Kazatchkine, AIDS Res. Hum. Retrovir. 9, 229 (1993); H. Stoiber, R. Schneider, J. Janatova, M. P. Dierich, Immunobiology 193, 98 (1995). B. M. Solder, Immunol. Lett 22, 135 (1989); G. T. Spear, A. L. Landay, B. L. Sullivan, B. Dittel, T. F. Lint, J. Immunol. 144, 1490 (1990); P. Marschang et al., AIDS 7, 903 (1993); M. P. Dierich et al., Immunol. Today 14, 435 (1993).
64. We thank J. Atkinson and J. Hildreth for mAbs and M. Wills-Karp, D. R. Moller, and A. Valsamakis for useful discussions. Supported in part by NIH grants AI01223 (C.L.K.); AI35149 and AI23047 (D.E.G.); and AI34412, CA20833, CA10815, and CA32898 (G.T., M.W.); the Peggy Meyerhoff Pearlstone Foundation (J.M.A.); and World Health Organization grant V21/181/67 (D.E.G.).