Chloroquine induces human mononuclear phagocytes to inhibit and kill Cryptococcus neoformans by a mechanism independent of iron deprivation

Journal of Clinical Investigation

Volumn 100, Issue 6, 1997, Pages 1640-1646

  Levitz, Stuart M ^a   Harrison, Thomas S ^a   Tabuni, Abdulmoneim ^a   Liu, Xiuping ^a  

^a BOSTON MEDICAL CENTER   (United States)

Author keywords

Chloroquine; Cryptococcus; HIV; Iron; Macrophage

Indexed keywords

CHLOROQUINE; IRON;

ANTIFUNGAL ACTIVITY; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CRYPTOCOCCUS NEOFORMANS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOSTIMULATION; IRON METABOLISM; LEUKOCYTE ACTIVATION; MONONUCLEAR CELL; NORMAL HUMAN; PHAGOCYTOSIS; PHAGOSOME; PRIORITY JOURNAL;

EID: 0030824696     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119688     Document Type: Article

References (49)

1. Diamond, R.D. 1995. Cryptococcus neoformans. In Mandell, Douglas and Bennett's Principles and Practice of Infectious Diseases. G.L. Mandell, J.E. Bennett, and R. Dolin, editors. Churchill-Livingstone Inc., New York. 2331-2340.
2. Powderly, W.G. 1993. Cryptococcal meningitis and AIDS. Clin. Infect. Dis. 17:837-842.
3. Levitz, S.M. 1991. The ecology of Cryptococcus neoformans and the epidemiology of cryptococcosis. Rev. Infect. Dis. 13:1163-1169.
4. Byrd, T.F., and M.A. Horwitz. 1991. Chloroquine inhibits the intracellular multiplication of Legionella pneumophila by limiting the availability of iron. A potential new mechanism for the therapeutic effect of chloroquine against intracellular pathogens. J. Clin. Invest. 88:351-357.
5. Newman, S.L., L. Gootee, G. Brunner, and G.S. Deepe, Jr. 1994. Chloroquine induces human macrophage killing of Histoplasma capsulatum by limiting the availability of intracellular iron and is therapeutic in a murine model of histoplasmosis. J. Clin. Invest. 93:1422-1429.
6. Fortier, A.H., D.A. Leiby, R.B. Narayanan, E. Asafoadjei, R.M. Crawford, C.A. Nancy, and M.S. Mitzer. 1995. Growth of Francisella tularensis LVS in macrophages: the acidic intracellular compartment provides essential iron required for growth. Infect. Immun. 63:1478-1483.
7. Dautry-Varsat, A., A. Ciechanover, and H.F. Lodish. 1983. pH and the recycling of transferrin during receptor-mediated endocytosis. Proc. Natl. Acad. Sci. USA. 80:2258-2262.
8. Starke, P.E., J.D. Gilbertson, and J.L. Farber. 1985. Lysosomal origin of the ferric iron required for cell killing by hydrogen peroxide. Biochem. Biophys. Res. Commun. 133:371-379.
9. Sibille, J.C., H. Kondo, and P. Aisen. 1989. Uptake of ferritin and iron bound to ferritin by rat hepatocytes: modulation by apotransferrin, iron chelators and chloroquine. Biochim. Biophys. Acta. 1010:204-209.
10. Sibille, J.C., M. Ciriolo, H. Kondo, R.R. Crichton, and P. Aisen. 1989. Subcellular localization of ferritin and iron taken up by rat hepatocytes. Biochem. J. 262:685-688.
11. Bates, G.W., and J. Wernicke. 1971. The kinetics and mechanism of iron(3) exchange between chelates and transferrin. IV. The reaction of transferrin with iron(3) nitrilotriacetate. J. Biol. Chem. 246:3679-3685.
12. Olakanmi, O., J.B. Stokes, and B.E. Britigan. 1994. Acquisition of iron bound to low molecular weight chelates by human monocyte-derived macrophages. J. Immunol. 153:2691-2703.
13. Levitz, S.M., A. Tabuni, H. Kornfeld, C.C. Reardon, and D.T. Golenbock. 1994. Production of tumor necrosis factor-alpha in human leukocytes stimulated by Cryptococcus neoformans. Infect. Immun. 62:1975-1981.
14. Miller, M.F., and T.G. Mitchell. 1991. Killing of Cryptococcus neoformans strains by human neutrophils and monocytes. Infect. Immun. 59:24-28.
15. Levitz, S.M., E.A. North, Y. Jiang, S. Nong, H. Kornfeld, and T.S. Harrison. 1997. Variables affecting production of monocyte chemotactic factor 1 from human leukocytes stimulated with Cryptococcus neoformans. Infect. Immun. 65:903-908.
16. Harrison, T.S., and S.M. Levitz. 1996. Role of IL-12 in PBMC responses to fungi in persons with and without HIV infection. J. Immunol. 156:4492-4497.
17. Harrison, T.S., H. Kornfeld, and S.M. Levitz. 1995. The effect of infection with human immunodeficiency virus on the anticryptococcal activity of lymphocytes and monocytes. J. Infect. Dis. 172:665-671.
18. Levitz, S.M. 1991. Activation of human peripheral blood mononuclear cells by interleukin-2 and granulocyte-macrophage colony-stimulating factor to inhibit Cryptococcus neoformans. Infect. Immun. 59:3393-3397.
19. Levitz, S.M., and A. Tabuni. 1991. Binding of Cryptococcus neoformans by human cultured macrophages. Requirements for multiple complement receptors and actin. J. Clin. Invest. 87:528-535.
20. Levitz, S.M., A. Tabuni, T.R. Kozel, R.S. MacGill, R.R. Ingalls, and D.T. Golenbock. 1997. Binding of Cryptococcus neoformans to heterologously expressed human complement receptors. Infect. Immun. 65:931-935.
21. Clemons, K.V., R. Azzi, and D.A. Stevens. 1996. Experimental systemic cryptococcosis in SCID mice. J Med. Vet. Mycol. 34:331-335.
22. Levitz, S.M., and T.P. Farrell. 1990. Growth inhibition of Cryptococcus neoformans by cultured monocytes: role of the capsule, opsonins, the culture surface, and cytokines. Infect. Immun. 58:1201-1209.
23. Diamond, R.D., and J.E. Bennett. 1973. Growth of Cryptococcus neoformans within human macrophages in vitro. Infect. Immun. 7:231-236.
24. Wang, Y., and A. Casadevall. 1994. Susceptibility of melanized and non-melanized Crvptococcus neoformans to nitrogen- and oxygen-derived oxidants. Infect. Immun. 62:3004-3007.
25. Krogstad, D.J., and P.H. Schlesinger. 1987. Acid-vesicle function, intracellular pathogens, and the action of chloroquine against Plasmodium falciparum. N. Engl. J. Med. 317:542-549.
26. Kozel, T.R., G.S. Pfrommer, A.S. Guerlain, B.A. Highison, and G.J. Highison. 1988. Strain variation in phagocytosis of Cryptococcus neoformans: dissociation of susceptibility to phagocytosis from activation and binding of opsonic fragments of C3. Infect. Immun. 56:2794-2800.
27. Small, J.M., T.G. Mitchell, and R.W. Wheat. 1986. Strain variation in composition and molecular size of the capsular polysaccharide of Cryptococcus neoformans serotype A. Infect. Immun. 54:735-741.
28. Levitz, S.M. 1994. Macrophage Cryptococcus interactions. In Macrophage Pathogen Interactions. B.S. Zwilling and T.K. Eisenstein, editors. Marcell Dekker, Inc., New York. 533-543.
29. Jacobson, E.S., and M.J. Petro. 1987. Extracellular iron chelation in Crvptococcus neoformans. J. Med. Vet. Mycol. 25:415-418.
30. Vartivarian, S.E., R.E. Cowart, E.J. Anaissie, T. Tashiro, and H.A. Sprigg. 1995. Iron acquisition by Cryptococcus neoformans. J. Med. Vet. Mycol. 33:151-156.
31. Johnson, W., L. Varner, and M. Poch. 1991. Acquisition of iron by Legionella Pneumophila: role of iron reductase. Infect. Immun. 59:2376-2381.
32. Tesfa-Selase, F., and R.J. Hay. 1996. Partial characterization and identification of a transferrin-like molecule of pathogenic yeast Cryptococcus neoformans. J. Gen. Appl. Microbiol. 42:61-70.
33. Howard, D.H. 1961. Some factors which affect the initiation of growth for Cryptococctis neoformans. J. Bacteriol. 82:430-435.
34. Nathan, C.F. 1987. Secretory products of macrophages. J. Clin. Invest. 79:319-326.
35. Campbell, E.J., J.D. Cury, S.D. Shapiro, G.I. Goldberg, and H.G. Welgus. 1991. Neutral proteinases of human mononuclear phagocytes. Cellular differentiation markedly alters cell phenotype for serine proteinases, metalloproteinases, and tissue inhibitor of metalloproteinases. J. Immunol. 146:1286-1293.
36. Eissenberg, L.G., W.E. Goldman, and P.H. Schlesinger. 1993. Histoplasma capsulatum modulates the acidification of phagolysosomes. J. Exp. Med. 177:1605-1611.
37. Zhu, X., W. Ertel, A. Ayala, M.H. Morrison. M.M. Perrin. and I.H. Chaudry. 1993. Chloroquine inhibits macrophage tumour necrosis factor-alpha mRNA transcription. Immunology. 80:122-126.
38. Ertel, W., M.H. Morrison, A. Ayala, and I.H. Chaudry. 1992. Chloroquine attenuates hemorrhagic shock-induced immunosuppression and decreases susceptibility to sepsis. Arch. Surg. 127:70-75.
39. Misra, U.K., G. Gawdi, and S.V. Pizzo. 1997. Chloroquine, quinine and quinidine inhibit calcium release from macrophage intracellular stores by blocking inositol 1,4,5-trisphosphate binding to its receptor. J. Cell. Biochem. 64:225-232.
40. Hart, P.D., and M.R. Young. 1991. Ammonium chloride, an inhibitor of phagosome-lysosome fusion in macrophages, concurrently induces phagosome-endosome fusion, and opens a novel pathway: studies of a pathogenic mycobacterium and a nonpathogenic yeast. J. Exp. Med. 174:881-889.
41. Baker, R.D., and R.K. Haugen. 1955. Tissue changes and tissue diagnosis in cryptococcosis. A study of 26 cases. Am. J. Clin. Path. 25:14-24.
42. Zebedee, S.L., R.K. Koduri, J. Mukherjee, S. Mukherjee, S. Lee, D.F. Sauer, M.D. Scharff, and A. Casadevall. 1994. Mouse-human immunoglobulin G1 chimeric antibodies with activities against Cryptococcus neoformans. Antimicrob. Agents Chemother. 38:1507-1514.
43. Mazzolla, R., R. Barluzzi, A. Brozzetti, J.R. Boelaert, T. Luna, S. Saleppico, F. Bistoni, and E. Blasi. 1997. Enhanced resistance to Cryptococcus neoformans infection induced by chloroquine in a murine model of meningoencephalitis. Antimicrob. Agents Chemother. 41:802-807.
44. Mackenzie, A.H. 1983. Pharmacologic actions of 4-aminoquinoline compounds. Am. J. Med. 75:5-10.
45. French, J.K., N.P. Hurst, M.L. O'Donnell, and W.H. Betts. 1987. Uptake of chloroquine and hydroxychloroquine by human blood leucocytes in vitro: relation, to cellular concentrations during antirheumatic therapy. Ann. Rheum. Dis. 46:42-45.
46. Crowle, A.J., and M.H. May. 1990. Inhibition of tubercle bacilli in cultured human macrophages by chloroquine used alone and in combination with streptomycin, isoniazid, pyrazinamide, and two metabolites of vitamin D3. Antimicrob. Agents Chemother. 34:2217-2222.
47. Collins, H.L., and G.J. Bancroft. 1991. Encapsulation of Cryptococcus neoformans impairs antigen-specific T-cell responses. Infect. Immun. 59:3883-3888.
48. Sperber, K., T.H. Kalb, V.J. Stecher, R. Banerjee, and L. Mayer. 1993. Inhibition of human immunodeficiency virus type 1 replication by hydroxychloroquine in T cells and monocytes. AIDS Res. Hum. Retroviruses. 9:91-98.
49. Sperber, K., M. Louie, T. Kraus, J. Proner, E. Sapira, S. Lin, V. Stecher, and L. Mayer. 1995. Hydroxychloroquine treatment of patients with human immunodeficiency virus type 1. Clin. Ther. 17:622-636.