IL-10 Enhances the Growth of Legionella pneumophila in Human Mononuclear Phagocytes and Reverses the Protective Effect of IFN-y: Differential Responses of Blood Monocytes and Alveolar Macrophages

Journal of Immunology

Volumn 157, Issue 6, 1996, Pages 2528-2538

  Park, David R ^a   Skerrett, Shawn J ^b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ANTISERUM; GAMMA INTERFERON; INTERLEUKIN 10; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BINDING COMPETITION; BLOOD; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; LEGIONELLA PNEUMOPHILA; LEGIONNAIRE DISEASE; LUNG ALVEOLUS MACROPHAGE; MICROBIOLOGY; MONOCYTE; SECRETION;

BINDING, COMPETITIVE; CELLS, CULTURED; HUMANS; IMMUNE SERA; INTERFERON TYPE II; INTERLEUKIN-10; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; MACROPHAGES, ALVEOLAR; MONOCYTES; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0030587126     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (72)

1. Nash, T. W., D. M. Libby, and M. A. Horwitz. 1984. Interaction between Legionnaires' disease bacterium (Legionella pneumophila) and human alveolar macrophages: influence of antibody, lymphokines, and hydrocortisone. J. Clin. Invest. 74:771.
2. Davis, G. S., W. C. Winn, Jr., D. W. Gump, and H. N. Beaty. 1983. The kinetics of the early inflammatory events during experimental pneumonia due to Legionella pneumophila. J. Infect. Dis. 148:823.
3. Skerrett, S. J., and T. R. Martin. 1991. Alveolar macrophage activation in experimental legionellosis. J. Immunol. 147:337.
4. Murray, H. W. 1988. Interferon-gamma, the activated macrophage, and host defense against microbial challenge. Ann. Intern Med. 108:595.
5. Nathan, C. R., H. W. Murray, M. E. Wiebe, and B. Y. Rubin. 1983. Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J. Exp. Med. 158:670.
6. Nash, T. W., D. M. Libby, and M. A. Horwitz. 1988. IFN-γ-activated human alveolar macrophages inhibit the intracellular multiplication of Legionella pneumophila. J. Immunol. 140:3978.
7. Jensen, W. A., R. M. Rose, R. H. J. Burke, K. Anton, and H. G. Remold. 1988. Cytokine activation of antibacterial activity in human pulmonary macrophages: comparison of recombinant interferon-gamma and granulocyte-macrophage colony-stimulating factor. Cell. Immunol. 117:369.
8. Bhardwaj, N., T. W. Nash, and M. A. Horwitz. 1986. Interferon-γ-activated human monocytes inhibit the intracellular multiplication of Legionella pneumophila. J. Immunol. 137:2662.
9. Matsiota-Bernard, P., C. Lefebre, M. Sedqui, P. Cornillet, and M. Guenounou. 1993. Involvement of tumor necrosis factor alpha in intracellular multiplication of Legionella pneumophila in human monocytes. Infect. Immun. 61:4980.
10. Skerrett, S. J., and T. R. Martin. 1993. Tumor necrosis factor and lipopolysaccharide potentiate gamma interferon-induced resistance of alveolar macrophages to Legionella pneumophila. In Legionella: current status and emerging perspectives. J. M. Barbaree, R. F. Breiman, and A. P. Dufour, eds. American Society for Microbiology, Washington, p. 105.
11. Bogdan, C., and C. Nathan. 1991. Modulation of macrophage function by transforming growth factor beta, interleukin-4, and interleukin-10. Ann. New York Acad Sci. 685:713.
12. Barral-Netto, M., A. Barral, C. E. Brownwell, Y. A. W. Skeiky, L. R. Ellingsworth, D. R. Twardzik, and S. G. Reed. 1992. Transforming growth factor-beta in leishmanial infection: a parasite escape mechanism. Science 257:545.
13. Silva, J. S., D. R. Twardzik, and S. G. Reed. 1991. Regulation of Trypanosoma cruzi infections in vitro and in vivo by transforming growth factor beta (TGF-beta). J. Exp. Med. 174:539.
14. Gazzinelli, R. T., I. P. Oswald, S. L. James, and A. Sher. 1992. IL-10 inhibits parasite killing and nitrogen oxide production by IFN-γ-activated macrophages. J. Immunol. 148:1792.
15. Tripp, C. S., S. F. Wolf, and E. R. Unanue. 1993. Interleukin 12 and tumor necrosis factor alpha are costimulators of interferon gamma production by natural killer cells in severe combined immunodeficiency mice with listeriosis, and interleukin 10 is a physiologic antagonist. Proc. Natl. Acad. Sci. USA 90:3725.
16. Frei, K., D. Nadal, H. W. Pfister, and A. Fontana. 1993. Listeria meningitis: identification of a cerebrospinal fluid inhibitor of macrophage listericidal function as interleukin 10. J. Exp. Med. 178:1255.
17. Denis, M., and E. Ghadirian. 1991. Transforming growth factor beta (TGF-β1) plays a detrimental role in the progression of experimental Mycobacterium avium infection; in vivo and in vitro evidence. Microb. Pathog. 11:367.
18. Denis, M., and E. Ghadirian. 1993. IL-10 neutralization augments mouse resistance to systemic Mycobacterium avium infections. J. Immunol. 151:5425.
19. Bermudez, L. E. 1993. Production of transforming growth factor-β by Mycobacterium avium-infected human macrophages is associated with unresponsiveness to IFN-γ. J. Immunol. 150:1838.
20. Bermudez, L. E., and J. Champsi. 1993. Infection with Mycobacterium avium induces production of interleukin-10 (IL-10), and administration of anti-IL-10 antibody is associated with enhanced resistance to infection in mice. Infect. Immun. 61:3093.
21. Flesch, I., J. Hess, I. Oswald, and S. Kaufman. 1994. Growth inhibition of Mycobacterium bovis by IFN-gamma-stimulated macrophages: regulation by endogenous tumor necrosis factor-alpha and by IL-10. Int. Immunol. 6:693.
22. Summersgill, J. T., L. A. Powell, B. L. Buster, R. D. Miller, and J. A. Ramirez. 1992. Killing of Legionella pneumophila by nitric oxide in gamma-interferon-activated macrophages. J. Leukocyte Biol. 52:625.
23. Schneemann, M., G. Schoedon, S. Hofer, N. Blau, L. Guerrero, and A. Schaffner. 1993. Nitric oxide synthase is not a constituent of the antimicrobial armature of human mononuclear phagocytes (see Comments). J. Infect. Dis. 167:1358.
24. Denis, M. 1994. Human monocytes/macrophages: NO or no NO? J. Leukocyte Biol. 55:682.
25. Hirsch, C., T. Yoneda, L. Averill, J. Ellner, and Z. Toossi. 1994. Enhancement of intracellular growth of Mycobacterium tuberculosis in human monocytes by transforming growth factor-beta 1. J. Infect. Dis. 170:1229.
26. Shiratsuchi, H., B. Hamilton, Z. Toossi, and J. Ellner. 1996. Evidence against a role for Interleukin-10 in the regulation of growth of Mycobacterium avium in human monocytes. J. Infect. Dis. 173:410.
27. Nakagawara, A., and C. F. Nathan. 1983. A simple method for counting adherent cells: application to cultured human monocytes, macrophages, and multinucleated giant cells. J. Immunol. Methods 56:261.
28. Kaplow, L. S. 1981. Cytochemical identification of mononuclear macrophages. In Manual of Macrophage Methodology: Collection, Characterization, and Function. H. B. Herscowitz, H. T. Hoblen, J. A. Bellanti, and A. Ghaffar, eds. Marcel Dekker, New York, p. 199.
29. Skerrett, S. J., R. A. Schmidt, and T. R. Martin. 1989. Impaired clearance of aerosolized Legionella pneumophila in corticosteroid-treated rats: a model of Legionnaires' disease in the compromised host. J. Infect. Dis. 160:261.
30. Denis, M. 1991. Growth of Mycobacterium avium in human monocytes: identification of cytokines which reduce and enhance intracellular microbial growth. Eur. J. Immunol. 21:391.
31. Portal, R., B. Clark, S. Wolff, and C. Dinarello. 1991. Enhancement of growth of virulent strains of Escherichia coli by interleukin-1. Science 254:430.
32. Shiratsuchi, H., J. L. Johnson, and J. J. Ellner. 1991. Bidirectional effects of cytokines on the growth of Mycobacterium avium within human monocytes. J. Immunol. 146:3165.
33. Warwick-Davies, J., J. Dhillon, L. O'Brien, P. Andrew, and D. Lowrie. 1994. Apparent killing of Mycobacterium tuberculosis can be an artefact of a cytotoxic effect on the monocytes. Clin. Exp. Immunol. 96:214.
34. Esparza, I., R. Fox, and R. Schreriber. 1986. Interferon-γ-dependem modulation of C3b receptor (CR1) on human peripheral blood monocytes. J. Immunol. 136:1360.
35. Firestein, G., and N. Zvaifler. 1987. Downregulation of human monocyte differentiation antigens by interferon-gamma. Cell. Immunol. 104:343.
36. Limb, G., A. Hamblin, R. Wolstencroft, and D. Dumonde. 1992. Rapid cytokine upregulation of integrins, complement receptor 1, and HLA-DR on monocytes but not on lymphocytes. Immunology 77:88.
37. Capsoni, F., F. Minonzio, A. Ongari, V. Carbonelli, A. Galli, and C. Zanussi. 1995. IL-10 up-regulates human monocyte phagocytosis in the presence of IL-4 and IFN-gamma. J. Leukocyte Biol. 58:351.
38. Jacobs, R., R. Locksley, C. Wilson, J. Haas, and S. Klebanoff. 1984. Interaction of primate alveolar macrophages and Legionella pneumophila. J. Clin. Invest. 73:1515.
39. Martin, T., J. Ruzinski, C. Wilson, and S. Skerrett. 1995. Effects of endotoxin in the lungs of neonatal rats: age-dependent impairment of the inflammatory response. J. Infect. Dis. 171:134.
40. Skerrett, S. J., and T. R. Martin. 1992. Recombinant murine interferon-gamma reversibly activates rat alveolar macrophages to kill Legionella pneumophila. J. Infect. Dis. 166:1354.
41. Blanchard, D. K., J. Y. Djeu, T. W. Klein, H. Friedman, and W. E. Stewart II. 1987. Induction of tumor necrosis factor by Legionella pneumophila. Infect. Immun. 55:433.
42. de Waal Malefyt, R., J. Abrams, B. Bennett, C. G. Figdor, and J. E. de Vries. 1991. Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 174:1209.
43. Oswald, I. P., T. A. Wynn, A. Sher, and S. L. James. 1992. Interleukin 10 inhibits macrophage microbicidal activity by blocking endogenous production of tumor necrosis factor-alpha required as a costimulatory factor for interferon-gamma-induced activation. Proc. Natl. Acad. Sci. USA 89:8676.
44. Marrack, P., and J. Kappler. 1994. Subversion of the immune system by pathogens. Cell 76:323.
45. Hall, B., and K. Joiner. 1991. Strategies of obligate intracellular parasites for evading host defences. Immunol. Today. 12:A22.
46. Silva, J. S., P. J. Morrissey, K. H. Grabstein, K. M. Mohler, D. Anderson, and S. G. Reed. 1992. Interleukin 10 and Interferon gamma regulation of experimental Trypanosoma cruzi infection. J. Exp. Med. 175:169.
47. Yamamura, M., K. Uyemura, R. J. Deans, K. Weinberg, T. H. Rea, B. R. Bloom, and R. L. Modlin. 1991. Defining protective responses to infectious pathogens: cytokine profiles in leprosy lesions. Science 254:277.
48. Sieling, P., and R. Modlin. 1994. Cytokine patterns at the site of mycobacterial infection. Immunobiology 191:378.
49. Pirmez, C., M. Yamamura, K. Uyemura, M. Paes-Oliveira, F. Conceicao-Silva, and R. L. Modlin. 1993. Cytokine patterns in the pathogenesis of human leishmaniasis. J. Clin. Invest. 91:1390.
50. Karp, C. L., S. H. El-Safi, T. A. Wynn, M. M. H. Satti, A. M. Kordofani, F. A. Hashim, M. Hag-Ali, F. A. Neva, T. B. Nutman, and D. L. Sacks. 1993. In vivo cytokine profiles in patients with kala-azar: marked elevation of both interleukin-10 and interferon-gamma. J. Clin. Invest. 91:1644
51. Ghalib, H. W., M. R. Piuvezam, Y. A. W. Skeiky, M. Siddig, F. A. Hashim, A. M. El-Hassan, D. M. Russo, and S. G. Reed. 1993. Interleukin 10 production correlates with pathology in human Leishmania donovani infections. J. Clin. Invest. 92:324.
52. Melby, P., F. Andrade-Navaez, B. Darnell, G. Valencia-Pacheco, V. Tyron, and A. Palomo-Cetina. 1994. Increased expression of proinflammatory cytokines in chronic lesions of human cutaneous leishmaniasis. Infect. Immun. 62:837.
53. Wang, P., P. Wu, M. Siegel, R. Egan, and M. Billah. 1994. IL-10 inhibits transcription of cytokine genes in human peripheral blood mononuclear cells. J. Immunol. 153:811.
54. Levitz, S., A. Tabuni, S.-H. Nong, and D. Golenbock. 1996. Effects of interleukin-10 on human peripheral blood mononuclear cell responses to Cryptococcus neoformans, Candida albicans, and lipopolysaccharide. Infect. Immun. 64:945.
55. Armstrong, L., N. Jordan, and A. Millar. 1996. Interleukin 10 (IL-10) regulation of tumour necrosis factor α (TNF-α) from human alveolar macrophages and peripheral blood monocytes. Thorax 51:143.
56. Bogdan, C., Y. Vodovotz, and C. Nathan. 1991. Macrophage deactivation by interleukin 10. J. Exp. Med. 174:1549.
57. Niiro, H., T. Otsuka, M. Abe, H. Satoh, T. Ogo, T. Nakano, Y. Furukawa, and Y. Niho. 1992. Epstein-Barr virus BCRF1 gene product (viral interleukin-10) inhibits superoxide anion production by human monocytes. Lymphokine Cytokine Res. 11:209.
58. Seitz, M., P. Loetscher, B. Dewald, H. Towbin, H. Gallati, and M. Baggiolini. 1995. Interleukin-10 differentially regulates cytokine inhibitor and chemokine release from blood mononuclear cells and fibroblasts. Eur. J. Immunol. 25:1129.
59. Byrd, T. F., and M. A. Horwitz. 1989. Interferon gamma-activated human monocytes downregulate transferrin receptors and inhibit the intracellular multiplication of Legionella pneumophila by limiting the availability of iron. J. Clin. Invest. 83:1457.
60. Liu, Y., S. Wei, A. Ho, R. de Waal Malefyt, and K. Moore. 1994. Expression cloning and characterization of human IL-10 receptor. J. Immunol. 152:1821.
61. Ho, A., Y. Liu, T. Khan, D. Hsu, J. Bazan, and K. Moore. 1993. A receptor for interleukin 10 is related to interferon receptors. Proc. Natl. Acad. Sci. USA 90:11267.
62. Barral-Netto, M., and A. Barral. 1994. Transforming growth factor-beta in tegumentary leishmaniasis. Braz. J. Med. Biol. Res. 27:1.
63. Sadick, M. D., F. P. Heinzel, B. J. Holaday, R. T. Pu, R. S. Dawkins, and R. M. Locksley. 1990. Cure of murine leishmaniasis with anti-interleukin 4 monoclonal antibody: evidence for a T cell-dependent, interferon gamma-independent mechanism. J. Exp. Med. 171:115.
64. Flesch, I. E. A. and S. H. E. Kaufmann. 1990. Activation of tuberculostatic macrophage functions by gamma interferon, interleukin-4, and tumor necrosis factor. Infect. Immun. 58:2675.
65. Fleming, S., and P. Campbell. 1996. Macrophages have cell surface IL-10 that regulates macrophage bactericidal activity. J. Immunol. 156:1143.
66. Moslen, M. 1994. Reactive oxygen species in formal physiology, cell injury, and phagocytosis. Adv. Exp. Med. Biol. 366:17.
67. Hirata, T., P. Bitterman, J.-F. Mornex, and R. Crystal. 1986. Expression of the transferrin receptor gene during the process of mononuclear phagocyte maturation. J. Immunol. 136:1339.
68. Corhay, J., G. Weber, T. Bury, S. Mariz, I. Roelandts, and M. Radermecker. 1992. Iron content in human alveolar macrophages. Eur. Resp. J. 5:804.
69. Wesselius, L., C. Flowers, and B. Skikne. 1992. Alveolar macrophage content of isoferritins and transferrin. Am. Rev. Respir. Dis. 145:311.
70. Hirsch, C. S., J. J. Ellner, D. G. Russell, and E. A. Rich. 1994. Complement receptor mediated uptake and tumor necrosis factor-alpha-mediated growth inhibition of Mycobacterium tuberculosis by human alveolar macrophages. J. Immunol. 152:743.
71. Rich, E. A., J. R. Panuska, R. S. Wallis, C. B. Wolf, M. L. Leonard, and J. J. Ellner. 1989. Dyscoordinate expression of tumor necrosis factor-alpha by human blood monocytes and alveolar macrophages. Am. Rev. Respir. Dis. 139:1010.
72. Greenberger, M., R. Strieter, S. Kunkel, J. Danforth, R. Goodman, and T. Standiford. 1995. Neutralization of IL-10 increases survival in a murine model of Klebsiella pneumonia. J. Immunol. 155:722.