Abstract
The incidence of infection with the pathogenic fungi continues to escalate, especially in the era of the acquired immune deficiency syndrome. To the clinician, this heterogeneous group of organisms poses both a diagnostic and a therapeutic challenge. Consequently, growing numbers of investigators are seeking to elucidate the pathogenetic mechanisms involved in disease caused by medically important fungi. In this review, many of the recent scientific advances that have been made in the immunological aspects of the pathogenesis of fungal infections are presented. The topics covered include 1) the receptors for fungi on the surface of professional phagocytes; 2) the mechanisms for killing and growth inhibition of fungi by phagocytes; 3) the means by which fungi evade host defenses; 4) the role of humoral immunity in fungal infection; 5) immunoregulation in fungal infections; and 6) the influence of cytokines on host defenses against pathogenic fungi.
Similar content being viewed by others
References
Reingold AL, Lu XD, Plikaytis BD, Ajello L: Systemic mycoses in the United States, 1980–1982. Journal of Medical and Veterinary Mycology 1986, 24: 433–436.
Whimbey E, Gold JWM, Polsky B, Dryjanski J, Hawkins C, Blevins A, Brannon P, Kiehn TE, Armstrong D: Bacteremia and fungemia in patients with the acquired immune deficiency syndrome. Annals of Internal Medicine 1986, 104: 511–514.
Kovacs JA, Kovacs AA, Polis M, Wright C, Gill VJ, Tuazon CU, Gelmann EP, Lane HC, Longfield R, Overturf G, Macher AM, Fauci AS, Parrillo JE, Bennett JE: Cryptococcosis in the acquired immune deficiency syndrome. Annals of Internal Medicine 1985, 103: 533–538.
Zuger A, Louie E, Holzman RS, Simberkoff MS, Rahal JJ: Cryptococcal disease in patients with acquired immunodeficiency syndrome. Annals of Internal Medicine 1986, 104: 234–240.
Bonner JR, Alexander J, Dismukes WE, App W, Griffin FM, Little R, Shin MS: Disseminated histoplasmosis in patients with the acquired immune deficiency syndrome. Archives of Internal Medicine 1984, 144: 2178–2181.
Wheat LJ, Slama TG, Zeckel ML: Histoplasmosis in the acquired immune deficiency syndrome. American Journal of Medicine 1985, 78: 203–210.
Bronninmann DA, Adam RD, Galgiani JN, Habib MP, Petersen EA, Porter B, Bloom JW: Coccidioidomycosis in the acquired immunodeficiency syndrome. Annals of Internal Medicine 1987, 106: 372–379.
Wileman TE, Lennartz MR, Stahl PD: Identification of the macrophage mannose receptor as a 175-kDa membrane protein. Proceedings of the National Academy of Sciences of the USA 1986, 83: 2501–2505.
Shepherd VL, Lee YC, Schlesinger PH, Stahl PD: L-fucose-terminated glycoconjugates are recognized by pinocytosis receptors on macrophages. Proceedings of the National Academy of Sciences of the USA 1981, 78: 1010–1022.
Warr GA: A macrophage receptor for (mannosamine-glucosamine)-glycoproteins of potential importance in phagocytic activity. Biochemical and Biophysical Research Communications 1980, 93: 737–745.
Kan VL, Bennett JE: Lectin-like attachment sites on murine pulmonary alveolar macrophages bindAspergillus fumigatus conidia. Journal of Infectious Diseases 1988, 158: 407–414.
Oda LM, Kubelka CF, Alviano CS, Travassos LR: Ingestion of yeast forms ofSporothrix schenkii by mouse peritoneal macrophages. Infection and Immunity 1983, 39: 497–504.
Bullock WE, Wright SD: Role of adherence-promoting receptors, CR3, LFA-1, and p150,95, in binding ofHistoplasma capsulatum by human macrophages. Journal of Experimental Medicine 1987, 165: 195–210.
Griffin FM: Roles of macrophages Fc and C3b receptors in phagocytosis of immunologically coatedCryptococcus neoformans. Proceedings of the National Academy of Sciences of the USA 1981, 78: 3853–3857.
Kozel TR, Pfrommer GST: Activation of the complement system byCryptococcus neoformans leads to binding of iC3b to the yeast. Infection and Immunity 1986, 52: 1–5.
Griffin JA, Griffin FM: Augmentation of macrophage complement receptor function in vitro. I: Characterization of the cellular interactions required for the generation of a T-lymphocyte product that enhances macrophage complement receptor function. Journal of Experimental Medicine 1979, 150: 653–675.
Griffin FM, Griffin JA: Augmentation of macrophage complement receptor function in vitro. II: Characterization of the effects of a unique lymphokine upon the phagocytic capabilities of macrophages. Journal of Immunology 1980, 125: 844–849.
Griffin JA, Griffin FM: Augmentation of macrophage complement receptor function in vitro. IV: The lymphokine that activates macrophage C3 receptors for phagocytosis binds to a fucose-bearing glycoprotein on the macrophage plasma membrane. Journal of Experimental Medicine 1984, 160: 1206–1218.
Newman SL, Bucher C, Rhodes JC, Bullock WE: Phagocytosis ofHistoplasma capsulatum yeasts and microconidia by human cultured macrophages and alveolar macrophages. Cellular cytoskeleton requirement for attachment and ingestion. Journal of Clinical Investigation 1990, 85: 223–230.
Myones BL, Dalzell JG, Hogg N, Ross GD: Neutrophil and monocyte cell surface p150,95 has iC3b-receptor (CR4) activity resembling CR3. Journal of Clinical Investigation 1988, 82: 640–651.
Kimberlin CL, Hariri AR, Hempel HO, Goodman NL: Interactions betweenHistoplasma capsulatum and macrophages from normal and treated mice: comparison of the mycelial and yeast phases in alveolar and peritoneal macrophages. Infection and Immunity 1981, 34: 6–10.
Diamond RD, Krzesicki R, Jao W: Damage to pseudohyphal forms ofCandida albicans by neutrophils in the absence of serum in vitro. Journal of Clinical Investigation 1978, 61: 349–359.
Drutz DJ, Frey CL: Intracellular and extracellular defenses of human phagocytes againstBlastomyces dermatitidis conidia and yeasts. Journal of Laboratory and Clinical Medicine 1985, 105: 737–750.
Frey CL, Drutz DJ: Influence of fungal surface components on the interaction ofCoccidioides immitis with polymorphonuclear neutrophils. Journal of Infectious Diseases 1986, 153: 933–942.
Klotz SA, Drutz DJ, Harrison JL, Huppert M: Adherence and penetration of vascular endothelium byCandida yeasts. Infection and Immunity 1983, 42: 374–384.
Rotrosen D, Edwards JE, Gibson TR, Moore JC, Cohen AC, Green I: Adherence ofCandida to cultured vascular endothelial cells: mechanisms of attachment and endothelial cell penetration. Journal of Infectious Diseases 1985, 152: 1264–1274.
Bouchara JP, Tronchin G, Annaix V, Robert R, Senet JM: Laminin receptors onCandida albicans germ tubes. Infection and Immunity 1990, 58: 48–54.
Kozel TR, Pfrommer GST, Redelman D: Activated neutrophils exhibit enhanced phagocytosis ofCryptococcus neoformans opsonized with normal human serum. Clinical and Experimental Immunology 1978, 70: 238–246.
Wright SD, Meyer BC: Phorbol esters cause sequential activation and deactivation of complement receptors on polymorphonuclear leukocytes. Journal of Immunology 1986, 136: 1759–1764.
Karbassi A, Becker JM, Foster JS, Moore RN: Enhanced killing ofCandida albicans by murine macrophages treated with macrophage colony-stimulating factor: evidence for augmented expression of mannose receptors. Journal of Immunology 1987, 139: 417–421.
Levitz SM, Diamond RD: Mechanisms of resistance ofAspergillus fumigatus conidia to killing by neutrophils in vitro. Journal of Infectious Diseases 1985, 152: 33–42.
Sixbey JW, Fields BT, Sun CN, Clark RA, Nolan CM: Interactions between human granulocytes andBlastomyces dermatitidis. Infection and Immunity 1979, 23: 41–44.
Danley DL, Hilger AE: Stimulation of oxidative metabolism in murine polymorphonuclear leukocytes by unopsonized fungal cells: evidence for a mannose-specific mechanism. Journal of Immunology 1981, 127: 551–556.
Davies SR, Clifford DP, Hoidal JR, Repine, JE: Opsonic requirements for the uptake ofCryptococcus neoformans by human polymorphonuclear leukocytes and monocytes. Journal of Infectious Diseases 1982, 145: 870–874.
Seligmann BE, Gallin JI: Comparison of indirect probes of membrane potential utilized in studies of human neutrophils. Journal of Cellular Physiology 1983, 115: 105–115.
Sbarra JJ, Paul BB, Jacobs AA, Strauss RR, Mitchell GW: Role of the phagocyte in host-parasite interactions. XXXVIII: Metabolic activities of the phagocyte as related to antimicrobial action. Journal of the Reticuloendothelial Society 1972, 12: 109–126.
Korchak HM, Rutherford LE, Weissmann G: Stimulus response coupling in the human neutrophil. I: Kinetic analysis of changes in calcium permeability. Journal of Biological Chemistry 1984, 259: 4070–4075.
Baldridge CW, Gerard RW: The extra respiration of phagocytosis. American Journal of Physiology 1933, 103: 235–236.
Lyman CA, Simons ER, Melnick DA, Diamond RD: UnopsonizedCandida albicans hyphae stimulate a neutrophil respiratory burst and cystolic calcium flux without membrane depolarization. Journal of Infectious Diseases 1987, 156: 770–776.
Levitz SM, Lyman CA, Murata T, Sullivan JA;Mandell GL, Diamond RD: Cystolic calcium changes in individual neutrophils stimulated by opsonized and unopsonizedCandida albicans hyphae. Infection and Immunity 1987, 55: 2783–2788.
Schaffner A, Davis CE, Schaffner T, Markert M, Douglas H, Braude AI: In vitro susceptibility of fungi to killing by neutrophil granulocytes discriminates between primary pathogenicity and opportunism. Journal of Clinical Investigation 1986, 78: 511–524.
Diamond RD, Clark RA, Haudenschild CC: Damage toCandida albicans hyphae and pseudohyphae by the myeloperoxidase system and oxidative products of neutrophil metabolism in vitro. Journal of Clinical Investigation 1980, 66: 908–917.
Washburn RG, Gallin JI, Bennett JE: Oxidative killing ofAspergillus fumigatus proceeds by parallel myeloperoxidase-dependent and -independent pathways. Infection and Immunity 1987, 55: 2088–2092.
Sugar AM, Chahal RS, Brummer E, Stevens DA: Susceptibility ofBlastomyces dermatitidis strains to products of oxidative metabolism. Infection and Immunity 1983, 41: 908–912.
Levitz SM, Diamond RD: Killing ofAspergillus fumigatus spores andCandida albicans yeast phase by the iron-hydrogen peroxide-iodide cytotoxic system: comparison with the myeloperoxidase-hydrogen peroxide-halide system. Infection and Immunity 1984, 43: 1100–1102.
Sugar AM, Chahal RS, Brummer E, Stevens DA: The iron-hydrogen peroxide-iodide system is fungicidal: activity against the yeast phase ofBlastomyces dermatitidis. Journal of Leukocyte Biology 1984, 36: 545–548.
Goodill JJ, Abuelo JG: Murcomycosis — a new risk of deferoxamine therapy in dialysis patients with albumin or iron overload? New England Journal of Medicine 1987, 317: 54.
Morrison CJ, Brummer E, Isenberg RA, Stevens DA: Activation of murine polymorphonuclear neutrophils for fungicidal activity by recombinant gamma interferon. Journal of Leukocyte Biology 1987, 41: 434–440.
Diamond RD, Haudenschild CC: Monocyte-mediated serum-independent damage to hyphal and pseudohyphal forms ofCandida albicans in vitro. Journal of Clinical Investigation 1981, 67: 173–182.
Diamond RD, Huber E, Haudenschild CC: Mechanisms of destruction ofAspergillus fumigatus hyphae mediated by human monocytes. Journal of Infectious Diseases 1983, 147: 474–483.
Diamond RD, Haudenschild CC, Erickson NF: Monocyte-mediated damage toRhizopus oryzae hyphae in vitro. Infection and Immunity 1982, 38: 292–297.
Wu-Hsieh B, Howard DH: Inhibition of growth ofHistoplasma capsulatum by lymphokine-stimulated macrophages. Journal of Immunology 1984, 132: 2593–2597.
Beaman L, Benjamini E, Pappagianis D: Role of lymphocytes in macrophage-induced killing ofCoccidioides immitis in vitro. Infection and Immunity 1981, 34: 347–353.
Diamond RD, Root RK, Bennet JE: Factors influencing killing ofCryptococcus neoformans by human leukocytes in vitro. Journal of Infectious Diseases 1972, 125: 367–375.
Levitz SM, Selsted ME, Ganz T, Lehrer RI, Diamond RD: In vitro killing of spores and hyphae ofAspergillus fumigatus andRhizopus oryzae by rabbit neutrophil cationic peptides and bronchoalveolar macrophages. Journal of Infectious Diseases 1986, 154: 483–489.
Schaffner A, Douglas H, Braude AI, Davis CE: Killing ofAspergillus spores depend on the anatomical sources of the macrophage. Infection and Immunity 1983, 42: 1109–1115.
van Oud Alblas AB, van Furth R: Origin, kinetics, and characteristics of pulmonary macrophages in the normal steady state. Journal of Experimental Medicine 1979, 149: 1504–1518.
Hearst JE, Warr GA, Jakab GJ: Characterization of murine lung and peritoneal macrophages. Journal of the Reticuloendothelial Society 1980, 27: 443–454.
Granger DL, Hibbs JB, Perfect JR, Durack DT: Specific amino acid (L-arginine) requirement for the microbiostatic activity of murine macrophages. Journal of Clinical Investigation 1988, 81: 1129–1136.
Granger DL, Hibbs JB, Perfect JR, Durack DT: Metabolic fate of L-arginine in relation to microbiostatic capability of murine macrophages. Journal of Clinical Investigation 1990, 85: 264–270.
Selsted ME, Brown DM, Delange RJ, Lehrer RI: Primary structures of MCP-1 and MCP-2, natural peptide antibiotics of rabbit lung macrophages. Journal of Biological Chemistry 1983, 258: 14485–14489.
Selsted ME, Brown DM, De Lange RJ, Harwig SSL, Lehrer RI: Primary structure of six antimicrobial peptides of rabbit peritoneal neutrophils. Journal of Biological Chemistry 1985, 260: 4579–4584.
Ganz T, Selsted ME, Szklarek D, Harwig SSL, Daher K, Bainton DF, Lehrer RI: Defensins. Natural peptide antibiotic of human neutrophils. Journal of Clinical Investigation 1985, 76: 1427–1435.
Lehrer RI, Daher K, Ganz T, Selsted ME: Direct inactivation of viruses by MCP-1 and MCP-2, natural peptide antibiotics from rabbit leukocytes. Journal of Virology 1985, 54: 467–472.
Selsted ME, Szklarek D, Ganz T, Lehrer RI: Activity of rabbit leukocyte peptides againstCandida albicans. Infection and Immunity 1985, 49: 202–206.
Segal G, Lehrer RI, Selsted ME: In vitro effect of phagocyte cationic peptides onCoccidioides immitis. Journal of Infectious Diseases 1985, 151: 890–894.
Lehrer RI, Szklarek D, Ganz T, Selsted ME: Synergistic activity of rabbit granulocyte peptides againstCandida albicans. Infection and Immunity 1986, 52: 902–904.
Selsted ME, Szkarek D, Lehrer RI: Purification and antimicrobial activity of antimicrobial peptides of rabbit granulocytes. Infection and Immunity 1984, 45: 150–154.
Heberman RB, Holden HT: Natural cell-mediated immunity. Advances in Cancer Research 1978, 27: 305–372.
Cauley LK, Murphy JW: Response of congenitally athymic (nude) and phenotypically normal mice to aCryptococcus neoformans infection. Infection and Immunity 1979, 23: 644–651.
Murphy JW, McDaniel DO: In vitro reactivity of natural killer (NK) cells againstCryptococcus neoformans. Journal of Immunology 1982, 128: 1577–1583.
Jimenez BE, Murphy JW: In vitro effects of natural killer cells againstParacoccidioides brasiliensis yeast phase. Infection and Immunity 1984, 46: 552–558.
Petkus AF, Baum LL: Natural killer cell inhibition of young spherules and endospores ofCoccidioides immitis. Journal of Immunology 1987, 139: 3107–3111.
Young JDE, Hengartner H, Podack ER, Cohn ZA: Purification and characterization of a cytolytic poreforming protein from granules of cloned lymphocytes with natural killer activity. Cell 1986, 44: 849–859.
Kozel TR, Mastroianni RP: Inhibition of phagocytosis by cryptococcal polysaccharide: dissociation of the attachment and ingestion phases of phagocytosis. Infection and Immunity 1976, 14: 62–67.
Gilmore BJ, Retsinas EM, Lorenz JS, Hostetter MK: An iC3b receptor onCandida albicans: structure, function, and correlates for pathogenicity. Journal of Infectious Diseases 1988, 157: 38–46.
Edwards JE, Gaither TA, O'Shea J, Rotrosen D, Lawley TJ, Wright SA, Frank MM, Green I: Expression of specific binding sites onCandida with functional and antigen characteristics of human complement receptors. Journal of Immunology 1986, 137: 3577–3583.
Saxena A, Calderone R: Purification and characterization of the extracellular C3d-binding protein ofCandida albicans. Infection and Immunity 1990, 58: 309–314.
Eissenberg LG, Goldman WE:Histoplasma capsulatum fails to trigger release of superoxide from macrophages. Infection and Immunity 1987, 55: 29–34.
Wolf JE, Herchberger V, Kobayashi GS, Little JR: Modulation of the macrophage oxidative burst byHistoplasma capsulatum. Journal of Immunology 1987, 138: 582–586.
Mullbacher LA, Eichner RD: Immunosuppression in vitro by a metabolite of a human pathogenic fungus. Proceedings of the National Academy of Sciences of the USA 1984, 81: 3835–3837.
Washburn RG, Hammer CH, Bennet JE: Inhibition of complement by culture supernatants ofAspergillus fumigatus. Journal of Infectious Diseases 1986, 154: 944–950.
Carrow E, Domer JE: Immunoregulation in experimental candidiasis: specific suppression induced byCandida albicans cell wall glycoprotein. Infection and Immunity 1985, 49: 172–181.
Domer JE, Stashak PW, Elkins K, Prescott B, Caldes G, Baker PJ: Separation of immunomodulatory effects of mannan fromCandida albicans into stimulatory and suppressive components. Cellular Immunology 1986, 101: 403–414.
Khardori N, Chardhary S, McConnachie P, Tewari RP: Characterization of lymphocytes responsible for protective immunity to histoplasmosis in mice. Mykosen 1983, 26: 523–532.
Brummer E, Morozumi PA, Vo PT, Stevens DA: Protection against pulmonary blastomycosis: adoptive transfer with T lymphocytes, but not serum, from resistant mice. Cellular Immunology 1982, 73: 349–359.
Lehrer RI, Cline MJ: Interaction ofCandida albicans with human leukocytes and serum. Journal of Bacteriology 1969, 98: 996–1004.
Tacker JR, Farhi F, Bulmer GS: Intracellular fate ofCryptococcus neoformans. Infection and Immunity 1972, 6: 162–167.
Morelli R, Rosenberg LT: Role of complement during experimentalCandida infection in mice. Infection and Immunity 1971, 3: 521–523.
Rhodes JC: Contribution of complement component C5 to the pathogenesis of experimental murine cryptococcosis. Journal of Medical and Veterinary Mycology 1985, 23: 225–234.
Gelfand JA, Hurley DL, Fauci AS, Frank MM: Role of complement in host defense against experimental disseminated candidiasis. Journal of Infectious Diseases 1978, 138: 9–16.
Yoshinoya S, Cox RA, Pope RM: Circulating immune complexes in coccidiodomycosis: detection and characterization. Journal of Clinical Investigation 1980, 66: 655–683.
Burges G, Holley HP, Virella G: Circulating immune complexes in patients withCandida albicans infections. Clinical and Experimental Immunology 1983, 53: 165–174.
Cox RA, Pope RM, Stevens DA: Immune complexes in coccidioidomycosis. Correlation with disease involvement. American Review of Respiratory Diseases 1982, 126: 439–443.
Bullock WE, Artz RP, Bhathena D, Tung KS: Histoplasmosis. Association with circulating immune complexes, eosinophilia, and mesangopathic glomerulonephritis. Archives of Internal Medicine 1979, 139: 700–702.
Cox RA, Pope RM: Serum-mediated suppression of lymphocyte transformation responses in coccidioidomycosis. Infection and Immunity 1987, 55: 1058–1062.
Williams DM, Graybill JR, Drutz DJ:Histoplasma capsulatum infection in nude mice. Infection and Immunity 1978, 21: 973–981.
Clemons KV, Leathers CR, Lee KW: SystemicCoccidioides immitis infection in nude and beige mice. Infection and Immunity 1985, 47: 814–821.
Cox RA: Cross-reactivity between antigens ofCoccidioides immitis, Histoplasma capsulatum andBlastomyces dermatitidis in lymphocyte transformation assays. Infection and Immunity 1979, 25: 932–938.
Deepe GS, Smith JG, Sonnenfeld G, Derman D, Bullock WE: Development and characterization ofHistoplasma capsulatum-reactive murine T-cell lines and clones. Infection and Immunity 1986, 54: 714–721.
Gomez AM, Bullock WE, Taylor CL, Deepe GS: The role of L3T4+ T cells in host defense againstHistoplasma capsulatum. Infection and Immunity 1988, 56: 1685–1691.
Mathew RC, Boros DL: Anti-L3T4 antibody treatment suppresses hepatic granuloma formation and abrogates antigen-induced interleukin-2 production inSchistosoma mansoni infection. Infection and Immunity 1986, 54: 820–826.
Deepe GS: Protective immunity in murine histoplasmosis: functional comparison of adoptively transferred T-cell clones and splenic T cells. Infection and Immunity 1988, 56: 2350–2355.
Cenci E, Romani L, Veccharelli A, Pucetti P, Bistoni F: Role of L3T4+ lymphocytes in protective immunity to systemicCandida albicans infection in mice. Infection and Immunity 1989, 57: 3581–3587.
Mody CH, Lipscomb MF, Street NE, Toews GB: Depletion of CD4+ (L3T4+) lymphocytes in vivo impairs murine host defense toCryptococcus neoformans. Journal of Immunology 1990, 144: 1472–1477.
Artz RP, Bullock WE: Immunoregulatory responses in experimental disseminated histoplasmosis: depression of T-cell-dependent and T-effector responses by activation of splenic suppressor cells. Infection and Immunity 1979, 23: 893–902.
Nickerson DA, Havens RA, Bullock WE: Immunoregulation in disseminated histoplasmosis: characterization of splenic suppressor cells. Cellular Immunology 1981, 60: 287–297.
Watson SR, Bullock WE: Immunoregulation in disseminated histoplasmosis: characterization of the surface phenotype of splenic suppressor T lymphocytes. Infection and Immunity 1982, 37: 940–945.
Deepe GS, Kravitz GR, Bullock WE: Pharmacological modulation of suppressor cell activity in mice with disseminated histoplasmosis. Infection and Immunity 1983, 41: 114–120.
Deepe GS, Watson SR, Bullock WE: Generation of disparate immunoregulatory factors in two inbred strains of mice with disseminated histoplasmosis. Journal of Immunology 1982, 129: 2186–2191.
Deepe GS, Watson SR, Bullock WE: Cellular origins and target cells of immunoregulatory factors in mice with disseminated histoplasmosis. Journal of Immunology 1984, 132: 2064–2071.
Murphy JW, Moorhead JW: Regulation of cell-mediated immunity in cryptococcosis. I: Induction of specific afferent T suppressor cell by cryptococcal antigen. Journal of Immunology 1982, 128: 276–283.
Murphy JW, Mosley RL, Moorhead JW: Regulation of cell-mediated immunity in cryptococcosis. II: Characterization of first-order T suppressor cells (Ts1) and induction of second-order suppressor cells. Journal of Immunology 1983, 130: 2876–2881.
Murphy JW, Mosley RL: Regulation of cell-mediated immunity in cryptococcosis. III: Characterization of second-order T suppressor cells (Ts2). Journal of Immunology 1985, 134: 577–584.
Khakpour FR, Murphy JW: Characterization of a third-order suppressor T cell (Ts3) induced by cryptococcal antigen(s). Infection and Immunity 1987, 55: 1657–1662.
Jimenez-Finkel BE, Murphy JW: Induction of antigen-specific T suppressor cells by solubleParacoccidioides brasiliensis antigen. Infection and Immunity 1988, 56: 734–743.
Jimenez-Finkel BE, Murphy JW: Characterization of efferent T suppressor cells induced byParacoccidioides brasiliensis-specific afferent T suppressor cells. Infection and Immunity 1988, 56: 744–750.
Blackstock R, McCormack JM, Hall NK: Induction of a macrophage-suppressive lymphokine by soluble cryptococcal antigens and its association with models of immunologic tolerance. Infection and Immunity 1987, 55: 233–239.
Blackstock R, Hernandez NC: Characterization of the macrophage subset affected and its response to a T suppressor factor (TsFmp) found in cryptococcosis. Infection and Immunity 1989, 57: 2931–2937.
Murphy JW: Clearance ofCryptococcus neoformans from immunologically suppressed mice. Infection and Immunity 1989, 57: 1946–1952.
Watson SR, Schmitt SK, Hendricks DE, Bulfock WE: Immunoregulation in disseminated murine histoplasmosis: disturbances in the production of interleukins 1 and 2. Journal of Immunology 1985, 135: 3487–3493.
Deepe GS, Taylor CL, Harris JE, Bullock WE: Modulation of cellular immune responses in mice with disseminated histoplasmosis by recombinant interleukin-2. Infection and Immunity 1986, 53: 6–12.
Sharma SD, Hofflin JM, Remington JS: In vivo recombinant interleukin-2 administration enhances survival against a lethal challenge withToxoplasma gondii. Journal of Immunology 1985, 135: 4160–4163.
Choromanski L, Kuhn RE: Interleukin 2 enhances specific and nonspecific immune responses in experimental Chagas' disease. Infection and Immunity 1985, 50: 354–357.
Cheever MA, Thompson JA, Dern DE, Greenberg PD: Interleukin 2 (IL-2) administered in vivo: influence of IL-2 route and timing on T cell growth. Journal of Immunology 1985, 134: 3895–3990.
Hardt C, Rollinghoff M, Pfizenmaier M, Mosmann M, Wagner H: Lyt-23+ cyclophosphamide-sensitive T cells regulate the activity of an interleukin 2 inhibitor in vivo. Journal of Experimental Medicine 1981, 154: 262–274.
Wu-Hsieh BA, Howard DH: Inhibition of intracellular growth ofHistoplasma capsulatum by recombinant murine gamma interferon. Infection and Immunity 1987, 55: 1014–1016.
Beaman L: Fungicidal activation of murine macrophages by recombinant gamma interferon. Infection and Immunity 1987, 55: 2951–2955.
Brummer E, Morrison CJ, Stevens DA: Recombinant and natural gamma-interferon activation of macrophages in vitro: different dose requirement for induction of killing activity against phagocytizable and nonphagocytizable fungi. Infection and Immunity 1985, 49: 724–730.
Brummer E, Hanson LH, Restrepo A, Stevens DA: In vivo and in vitro activation of pulmonary macrophages by gamma-IFN for enhanced killing ofParacoccidioides brasiliensis orBlastomyces dermatitidis. Journal of Immunology 1988, 140: 2786–2789.
Fleischman J, Wu-Hsieh B, Howard DH: The intracellular fate ofHistoplasma capsulatum in human macrophages is unaffected by recombinant human interferon. Journal of Infectious Diseases 1990, 161: 143–145.
Beutler B, Cerami A: Cachectin: more than a tumor necrosis factor. New England Journal of Medicine 1987, 316: 379–385.
Djeu JY, Blanchard DK, Halkias D, Friedman H: Growth inhibition ofCandida albicans by human polymorphonuclear neutrophils: activation by interferon-gamma and tumor necrosis factor. Journal of Immunology 1986, 137: 2980–2984.
Slagle DC, Cox RA, Kuruganti U: Induction of tumor necrosis factor alpha by spherules ofCoccidioides immitis. Infection and Immunity 1989, 57: 1916–1921.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Deepe, G.S., Bullock, W.E. Immunological aspects of fungal pathogenesis. Eur. J. Clin. Microbiol. Infect. Dis. 9, 567–579 (1990). https://doi.org/10.1007/BF01967211
Issue Date:
DOI: https://doi.org/10.1007/BF01967211