Abstract
Intravenous (i.v.) administration of phagocytosable chitin particles (1 to 10 microm) in C57BL/6 mice and SCID mice primed alveolar macrophages (Mphi) within 3 days to yield up to a 50-fold increase in their oxidative burst when elicited in vitro with phorbol myristate acetate (PMA). C57BL/6 mice pretreated with monoclonal antibodies (MAbs) against mouse gamma interferon (IFN-gamma) or NK1.1 showed a markedly decreased level of alveolar Mphi priming following injection of chitin particles. To confirm IFN-gamma production in vitro, spleen cells isolated from normal C57BL/6 mice and SCID mice were cultured with chitin particles. Significant IFN-gamma production was observed following stimulation with chitin but not with chitosan or latex beads. When spleen cells were treated with anti-NK1.1 MAb, IFN-gamma production was significantly inhibited. Another set of experiments showed that when C57BL/6 mice were pretreated i.v. with a small dose IFN-gamma, a higher level of priming was induced with not only phagocytosable chitin particles but also phagocytosable chitosan and even latex beads. Likewise, the spleen cell cultures preconditioned with IFN-gamma provided an up-regulation of IFN-gamma production by these phagocytosable particles. Taken together, the in vivo and in vitro results suggest that (i) the alveolar Mphi priming mechanism is due, at least in part, to direct activation of Mphi by IFN-gamma, which is produced by NK1.1+ CD4- cells; (ii) IFN-gamma would have an autocrine-like effect on Mphi and make them more responsive to particle priming; and (iii) phagocytosis of particulates, probably by a postmembrane event such as interiorization, appears to be important for the up-regulation of alveolar Mphi priming and IFN-gamma production.
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- Allen L. H., Aderem A. A role for MARCKS, the alpha isozyme of protein kinase C and myosin I in zymosan phagocytosis by macrophages. J Exp Med. 1995 Sep 1;182(3):829–840. doi: 10.1084/jem.182.3.829. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Azuma I. Synthetic immunoadjuvants: application to non-specific host stimulation and potentiation of vaccine immunogenicity. Vaccine. 1992;10(14):1000–1006. doi: 10.1016/0264-410x(92)90108-v. [DOI] [PubMed] [Google Scholar]
- Bautista A. P., Schuler A., Spolarics Z., Spitzer J. J. In vivo latex phagocytosis primes the Kupffer cells and hepatic neutrophils to generate superoxide anion. J Leukoc Biol. 1992 Jan;51(1):39–45. doi: 10.1002/jlb.51.1.39. [DOI] [PubMed] [Google Scholar]
- Betz M., Fox B. S. Prostaglandin E2 inhibits production of Th1 lymphokines but not of Th2 lymphokines. J Immunol. 1991 Jan 1;146(1):108–113. [PubMed] [Google Scholar]
- Black C. M., Catterall J. R., Remington J. S. In vivo and in vitro activation of alveolar macrophages by recombinant interferon-gamma. J Immunol. 1987 Jan 15;138(2):491–495. [PubMed] [Google Scholar]
- Bourbouze R., Raffi F., Dameron G., Hali-Miraftab H., Loko F., Vilde J. L. N-acetyl-beta-D-glucosaminidase (NAG) isoenzymes release from human monocyte-derived macrophages in response to zymosan and human recombinant interferon-gamma. Clin Chim Acta. 1991 Jun 14;199(2):185–194. doi: 10.1016/0009-8981(91)90110-x. [DOI] [PubMed] [Google Scholar]
- Buchmeier N. A., Schreiber R. D. Requirement of endogenous interferon-gamma production for resolution of Listeria monocytogenes infection. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7404–7408. doi: 10.1073/pnas.82.21.7404. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chida K., Myrvik Q. N., Leake E. S., Gordon M. R., Wood P. H., Ricardo M. J., Jr Chemiluminescent responses of alveolar macrophages from normal and Mycobacterium bovis BCG-vaccinated rabbits as a function of age. Infect Immun. 1987 Jun;55(6):1476–1483. doi: 10.1128/iai.55.6.1476-1483.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cooper A. M., Dalton D. K., Stewart T. A., Griffin J. P., Russell D. G., Orme I. M. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med. 1993 Dec 1;178(6):2243–2247. doi: 10.1084/jem.178.6.2243. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Corradin S. B., Mauël J. Phagocytosis of Leishmania enhances macrophage activation by IFN-gamma and lipopolysaccharide. J Immunol. 1991 Jan 1;146(1):279–285. [PubMed] [Google Scholar]
- Debono M., Gordee R. S. Antibiotics that inhibit fungal cell wall development. Annu Rev Microbiol. 1994;48:471–497. doi: 10.1146/annurev.mi.48.100194.002351. [DOI] [PubMed] [Google Scholar]
- Dunn P. L., North R. J. Early gamma interferon production by natural killer cells is important in defense against murine listeriosis. Infect Immun. 1991 Sep;59(9):2892–2900. doi: 10.1128/iai.59.9.2892-2900.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Flynn J. L., Chan J., Triebold K. J., Dalton D. K., Stewart T. A., Bloom B. R. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med. 1993 Dec 1;178(6):2249–2254. doi: 10.1084/jem.178.6.2249. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Georgopapadakou N. H., Tkacz J. S. The fungal cell wall as a drug target. Trends Microbiol. 1995 Mar;3(3):98–104. doi: 10.1016/s0966-842x(00)88890-3. [DOI] [PubMed] [Google Scholar]
- Hayakawa H., Umehara K., Myrvik Q. N. Oxidative responses of rabbit alveolar macrophages: comparative priming activities of MIF/MAF, sera, and serum components. J Leukoc Biol. 1989 Mar;45(3):231–238. doi: 10.1002/jlb.45.3.231. [DOI] [PubMed] [Google Scholar]
- Hsieh C. S., Heimberger A. B., Gold J. S., O'Garra A., Murphy K. M. Differential regulation of T helper phenotype development by interleukins 4 and 10 in an alpha beta T-cell-receptor transgenic system. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):6065–6069. doi: 10.1073/pnas.89.13.6065. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hsieh C. S., Macatonia S. E., Tripp C. S., Wolf S. F., O'Garra A., Murphy K. M. Development of TH1 CD4+ T cells through IL-12 produced by Listeria-induced macrophages. Science. 1993 Apr 23;260(5107):547–549. doi: 10.1126/science.8097338. [DOI] [PubMed] [Google Scholar]
- Johnston R. B., Jr, Godzik C. A., Cohn Z. A. Increased superoxide anion production by immunologically activated and chemically elicited macrophages. J Exp Med. 1978 Jul 1;148(1):115–127. doi: 10.1084/jem.148.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maródi L., Schreiber S., Anderson D. C., MacDermott R. P., Korchak H. M., Johnston R. B., Jr Enhancement of macrophage candidacidal activity by interferon-gamma. Increased phagocytosis, killing, and calcium signal mediated by a decreased number of mannose receptors. J Clin Invest. 1993 Jun;91(6):2596–2601. doi: 10.1172/JCI116498. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Murray H. W. Interferon-gamma, the activated macrophage, and host defense against microbial challenge. Ann Intern Med. 1988 Apr;108(4):595–608. doi: 10.7326/0003-4819-108-4-595. [DOI] [PubMed] [Google Scholar]
- Myrvik Q. N., Gristina A. G., Giridhar G., Hayakawa H. Particle-induced in vivo priming of alveolar macrophages for enhanced oxidative responses: a novel system of cellular immune augmentation. J Leukoc Biol. 1993 Nov;54(5):439–443. doi: 10.1002/jlb.54.5.439. [DOI] [PubMed] [Google Scholar]
- Nathan C. F., Murray H. W., Wiebe M. E., Rubin B. Y. Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J Exp Med. 1983 Sep 1;158(3):670–689. doi: 10.1084/jem.158.3.670. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nishimura K., Ishihara C., Ukei S., Tokura S., Azuma I. Stimulation of cytokine production in mice using deacetylated chitin. Vaccine. 1986 Sep;4(3):151–156. doi: 10.1016/0264-410x(86)90002-2. [DOI] [PubMed] [Google Scholar]
- Nishimura K., Nishimura S., Seo H., Nishi N., Tokura S., Azuma I. Effect of multiporous microspheres derived from chitin and partially deacetylated chitin on the activation of mouse peritoneal macrophages. Vaccine. 1987 Jun;5(2):136–140. doi: 10.1016/0264-410x(87)90061-2. [DOI] [PubMed] [Google Scholar]
- Nishimura K., Nishimura S., Seo H., Nishi N., Tokura S., Azuma I. Macrophage activation with multi-porous beads prepared from partially deacetylated chitin. J Biomed Mater Res. 1986 Nov-Dec;20(9):1359–1372. doi: 10.1002/jbm.820200910. [DOI] [PubMed] [Google Scholar]
- Okamura H., Tsutsi H., Komatsu T., Yutsudo M., Hakura A., Tanimoto T., Torigoe K., Okura T., Nukada Y., Hattori K. Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature. 1995 Nov 2;378(6552):88–91. doi: 10.1038/378088a0. [DOI] [PubMed] [Google Scholar]
- Pontow S. E., Kery V., Stahl P. D. Mannose receptor. Int Rev Cytol. 1992;137B:221–244. doi: 10.1016/s0074-7696(08)62606-6. [DOI] [PubMed] [Google Scholar]
- Powrie F., Menon S., Coffman R. L. Interleukin-4 and interleukin-10 synergize to inhibit cell-mediated immunity in vivo. Eur J Immunol. 1993 Nov;23(11):3043–3049. doi: 10.1002/eji.1830231147. [DOI] [PubMed] [Google Scholar]
- Schafer R., Eisenstein T. K. Natural killer cells mediate protection induced by a Salmonella aroA mutant. Infect Immun. 1992 Mar;60(3):791–797. doi: 10.1128/iai.60.3.791-797.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Scott P. IFN-gamma modulates the early development of Th1 and Th2 responses in a murine model of cutaneous leishmaniasis. J Immunol. 1991 Nov 1;147(9):3149–3155. [PubMed] [Google Scholar]
- Scott P. IL-12: initiation cytokine for cell-mediated immunity. Science. 1993 Apr 23;260(5107):496–497. doi: 10.1126/science.8097337. [DOI] [PubMed] [Google Scholar]
- Shepherd V. L., Lee Y. C., Schlesinger P. H., Stahl P. D. L-Fucose-terminated glycoconjugates are recognized by pinocytosis receptors on macrophages. Proc Natl Acad Sci U S A. 1981 Feb;78(2):1019–1022. doi: 10.1073/pnas.78.2.1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shibata Y., Bjorkman D. R., Schmidt M., Oghiso Y., Volkman A. Macrophage colony-stimulating factor-induced bone marrow macrophages do not synthesize or release prostaglandin E2. Blood. 1994 Jun 1;83(11):3316–3323. [PubMed] [Google Scholar]
- Shibata Y. Prostaglandin E2 release triggered by phagocytosis of latex particles. A distinct association with prostaglandin synthase isozymes in bone marrow macrophages. J Immunol. 1995 Mar 15;154(6):2878–2887. [PubMed] [Google Scholar]
- Shibata Y., Volkman A. The effect of bone marrow depletion on prostaglandin E-producing suppressor macrophages in mouse spleen. J Immunol. 1985 Dec;135(6):3897–3904. [PubMed] [Google Scholar]
- Skeen M. J., Miller M. A., Shinnick T. M., Ziegler H. K. Regulation of murine macrophage IL-12 production. Activation of macrophages in vivo, restimulation in vitro, and modulation by other cytokines. J Immunol. 1996 Feb 1;156(3):1196–1206. [PubMed] [Google Scholar]
- Snijders A., Hilkens C. M., van der Pouw Kraan T. C., Engel M., Aarden L. A., Kapsenberg M. L. Regulation of bioactive IL-12 production in lipopolysaccharide-stimulated human monocytes is determined by the expression of the p35 subunit. J Immunol. 1996 Feb 1;156(3):1207–1212. [PubMed] [Google Scholar]
- Tripp C. S., Gately M. K., Hakimi J., Ling P., Unanue E. R. Neutralization of IL-12 decreases resistance to Listeria in SCID and C.B-17 mice. Reversal by IFN-gamma. J Immunol. 1994 Feb 15;152(4):1883–1887. [PubMed] [Google Scholar]
- Tripp C. S., Wolf S. F., Unanue E. R. 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 U S A. 1993 Apr 15;90(8):3725–3729. doi: 10.1073/pnas.90.8.3725. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Warr G. A. A macrophage receptor for (mannose/glucosamine)-glycoproteins of potential importance in phagocytic activity. Biochem Biophys Res Commun. 1980 Apr 14;93(3):737–745. doi: 10.1016/0006-291x(80)91139-0. [DOI] [PubMed] [Google Scholar]
- Wong H. L., Lotze M. T., Wahl L. M., Wahl S. M. Administration of recombinant IL-4 to humans regulates gene expression, phenotype, and function in circulating monocytes. J Immunol. 1992 Apr 1;148(7):2118–2125. [PubMed] [Google Scholar]
- Yamamoto N., Zou J. P., Li X. F., Takenaka H., Noda S., Fujii T., Ono S., Kobayashi Y., Mukaida N., Matsushima K. Regulatory mechanisms for production of IFN-gamma and TNF by antitumor T cells or macrophages in the tumor-bearing state. J Immunol. 1995 Mar 1;154(5):2281–2290. [PubMed] [Google Scholar]
- Yoshihara R., Shiozawa S., Fujita T., Chihara K. Gamma interferon is produced by human natural killer cells but not T cells during Staphylococcus aureus stimulation. Infect Immun. 1993 Aug;61(8):3117–3122. doi: 10.1128/iai.61.8.3117-3122.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]