Chloroquine is therapeutic in murine experimental model of paracoccidioidomycosis

FEMS Immunology and Medical Microbiology

Volumn 50, Issue 1, 2007, Pages 133-143

  Dias Melicio, Luciane Alarcão ^a   Calvi, Sueli Aparecida ^b   Bordon, Ana Paula ^a   Golim, Marjorie A ^a   Peraçoli, Maria Terezinha Serrão ^a   Soares, Angela Maria Victoriano Campos ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b Ponce School of Medicine   (Brazil)

Author keywords

Chloroquine; Cytokines; Hydrogen peroxide; Iron; Nitric oxide; Paracoccidioides brasiliensis

Indexed keywords

CHLOROQUINE; HYDROGEN PEROXIDE; INTERLEUKIN 10; INTERLEUKIN 6; NITRIC OXIDE; TRANSFERRIN RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DRUG EFFECT; LIVER; LUNG; MALE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOUTH AMERICAN BLASTOMYCOSIS; SPLEEN;

ANIMALS; CHLOROQUINE; DISEASE MODELS, ANIMAL; HYDROGEN PEROXIDE; INTERLEUKIN-6; IRON; MACROPHAGES, PERITONEAL; MALE; MICE; MICE, INBRED BALB C; NITRIC OXIDE; PARACOCCIDIOIDES; PARACOCCIDIOIDOMYCOSIS; RECEPTORS, TRANSFERRIN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 34248512354     PISSN: 09288244     EISSN: 1574695X     Source Type: Journal    
DOI: 10.1111/j.1574-695X.2007.00243.x     Document Type: Article

References (77)

1. Alford CE, King TE Jr. Campbell PA (1991) Role of transferrin, transferrin receptors, and iron in macrophage listericidal activity. J Exp Med 174 : 459 466.
2. Antoni F, Hrabák A Csuka I (1986) Effect of emetine and chloroquine on phagocytic processes of rat macrophages. Biochem Pharmacol 35 : 2869 2874.
3. Arango R Restrepo A (1988) Growth and production of iron chelants by Paracoccidioides brasiliensis mycelial and yeast forms. J Med Vet Mycol 26 : 113 118.
4. Baynes R, Bukofzer G, Bothwell T, Bezwoda W Macfarlane B (1987) Transferrin receptors and transferrin iron uptake by cultured human blood monocytes. Eur J Cell Biol 43 : 372 376.
5. Bermudez LE, Wu M, Petrofsky M Young LS (1992) Interleukin-6 antagonizes tumor necrosis factor-mediated mycobacteriostatic and mycobactericidal activities in macrophages. Infect Immun 60 : 4245 4252.
6. Blanchard DK, Michelini-Norris MB, Pearson CA, Freitag CS Djeu JY (1991) Mycobacterium avium-intracellulare induces interleukin-6 from human monocytes and large granular lymphocytes. Blood 77 : 2218 2224.
7. Bocca AL, Hayashi EE, Pinheiro AG, Furlanetto AB, Campanelli AP, Cunha FQ Figueiredo F (1998) Treatment of Paracoccidioides brasiliensis-infected mice with a nitric oxide inhibitor prevents the failure of cell-mediated immune response. J Immunol 161 : 3056 3063.
8. Boelaert JR, Appelberg R, Gomes MS et al 2001) Experimental results on chloroquine and AIDS-related opportunistic infections. J Acquir Immune Defic Syndr 26 : 300 301.
9. Brummer E, Hanson LH, Restrepo A Stevens DA (1989) Intracellular multiplication of Paracoccidioides brasiliensis in macrophages: killing and restriction of multiplication by activated macrophages. Infect Immun 57 : 2289 2294.
10. Byrd TF Horwitz MA (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 1465.
11. Byrd TF Horwitz MA (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.
12. Byrd TF Horwitz MA (1993) Regulation of transferrin receptor expression and ferritin content in human mononuclear phagocytes. Coordinate upregulation by iron transferrin and downregulation by interferon gamma. J Clin Invest 91 : 969 976.
13. Calvi SA, Peraçoli MTS, Mendes RP, Marcondes-Machado J, Fecchio D, Marques SA Soares AMVC (2003) Effect of cytokines on the in vitro fungicidal activity of monocytes from paracoccidioidomycosis patients. Microbes Infect 5 : 107 113.
14. Cano LE, Arango R, Salazar ME, Brummer E, Stevens DA Restrepo A (1992) Killing of P. brasiliensis conidia by pulmonary macrophages and the effect of cytokines. J Med Vet Mycol 30 : 161 168.
15. Cano LE, Brummer E, Restrepo A Stevens DA (1994) Inhibitory effect of deferoxamine or macrophage activation on transformation of Paracoccidioides brasiliensis conidia ingested by macrophages: reversal by holotransferrin. Infect Immun 62 : 1494 1496.
16. Cano LE, Singer-Vermes LM, Vaz CAC, Russo M Calich VLG (1995) Pulmonary paracoccidioidomycosis in resistant and susceptible mice: relationship among progression of infection, bronchoalveolar cell activation, cellular immune response, and specific isotype patterns. Infect Immun 63 : 1777 1783.
17. Carmo JPM, Dias-Melicio LA, Calvi SA, Peraçoli MTS Soares AMVC (2006) TNF-α activates human monocytes for Paracoccidioides brasiliensis killing by an H2O2-dependent mechanism. Med Mycol 44 : 363 368.
18. Conrad ME, Umbreit JN Moore EG (1999) Iron absorption and transport. Am J Med Sci 318 : 213 229.
19. Crowle AJ May MH (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.
20. Dautry-Varsat A, Ciechanover A Lodish HF (1983) pH and the recycling of transferrin during receptor-mediated endocytosis. Proc Natl Acad Sci USA 80 : 2258 2262.
21. Dias-Melicio LA, Calvi SA, Peraçoli MTS Soares AMVC (2005) Inhibitory effect of deferoxamine on human monocytes Paracoccidioides brasiliensis survival: reversal by holotransferrin not by apotransferrin. Rev Inst Med Trop S Paulo 47 : 263 266.
22. Dias-Melicio LA, Moreira AP, Calvi SA Soares AMVC (2006) Chloroquine inhibits Paracoccidioides brasiliensis survival within human monocytes by limiting the availability of intracellular iron. Microbiol Immunol 50 : 307 314.
23. Fornari MC, Bava AJ, Guereno VE, Berarde MR, Silaf MR, Negroni R Diez RA (2001) High serum interleukin-10 and tumor necrosis factor alpha levels in chronic paracoccidioidomycosis. Clin Diagn Lab Immunol 8 : 1036 1038.
24. Forsbeck K Nilsson N (1983) Iron metabolism of established human hematopoietic cell lines in vitro. Exp Cell Res 14 : 323 332.
25. Fox RI (1993) Mechanism of action of hydroxychloroquine as an antirheumatic drug. Semin Arthritis Rheum 23 : 82 91.
26. Franco M, Mendes RP, Moscardi-Bacchi M, Rezkallah-Iwasso MT Montenegro MR (1989) Paracoccidioidomycosis. Bailliere's Clin Trop Med Commun Dis 4 : 185 220.
27. Godfrey K (1985) Statistics in practice. Comparing the means of several groups. N Engl J Med 313 : 1450 1456.
28. Gonzalez A, Gregori W, Velez D, Restrepo A Cano LE (2000) Nitric oxide participation in the fungicidal mechanism of gamma-interferon-activated murine macrophages against Paracoccidioides brasiliensis conidia. Infect Immun 68 : 2546 2552.
29. Green LC (1981) Nitrite biosynthesis in man. Proc Natl Acad Sci 15 : 106 122.
30. Hentze MW Kuhn LC (1996) Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc Natl Acad Sci USA 93 : 8175 8182.
31. Hong Z, Jiang Z, Liangxi W, Guofu D, Ping L, Yongling L, Wendong P Wang M (2004) Chloroquine protects mice from challenge with CpG ODN and lipopolysaccharide by decreasing proinflammatory cytokine release. Intern Immunopharm 4 : 223 234.
32. Hrabák A, Sefrioui H, Vercruysse V, Temesi A, Bajor T Vray B (1998) Action of chloroquine on nitric oxide production and parasite killing by macrophages. Eur J Pharm 354 : 83 90.
33. Jacobs A (1977) Low molecular weight intracellular iron transport compounds. Blood 50 : 433 439.
34. Karhawi AS, Colombo AL Salomão R (2000) Production of IFN-gamma is impaired in patients with paracoccidioidomycosis during active disease and is restored after clinical remission. Med Mycol 38 : 225 229.
35. Kim S Ponka P (1999) Control of transferrin receptor expression via nitric oxide-mediated modulation of iron-regulatory protein 2. J Biol Chem 274 : 33035 33042.
36. Kim S Ponka P (2000) Effects of interferon-γ and lipopolysaccharide on macrophage iron metabolism are mediated by nitric oxide-induced degradation of iron-regulatory protein 2. J Biol Chem 275 : 6220 6226.
37. Kim S Ponka P (2002) Nitric oxide-mediated modulation of iron regulatory proteins: implication for cellular iron homeostasis. Blood Cells Mol Dis 29 : 400 410.
38. Krogstad DJ Schlesinger PH (1987) Acid-vesicle function, intracellular pathogens, and the action of choroquine against Plasmodium falciparum. N Engl J Med 317 : 542 549.
39. Lane TE, Wu-Hsieh BA Howard DH (1991) Iron limitation and the gamma interferon-mediated antihistoplasma state of murine macrophages. Infect Immun 59 : 2274 2278.
40. Lang T Kaye PM (1991) Presentation of Leishmania donovani promastigotes occurs via a brefeldin A-sensitive pathway. Eur J Immunol 21 : 2407 2413.
41. Legssyer R, Ward RJ, Crichton RR Boelaert J (1999) Effect of chronic chloroquine administration on iron loading in the liver and reticuloendothelial system and on oxidative responses by the alveolar macrophages. Biochem Pharmacol 57 : 907 911.
42. Legssyer R, Josse C, Piette J, Ward RJ Crichton RR (2003) Changes in function of iron-loaded alveolar macrophages after in vivo administration of desferrioxamine and/or chloroquine. J Inorg Biochem 94 : 36 42.
43. Lestas AN (1976) The effect of pH upon human transferrin: selective labeling of the two iron-binding sites. Br J Haematol 32 : 341 350.
44. Levitz MS, Harrison TS, Tabuni A Liu X (1997) Chloroquine induces human mononuclear phagocytes to inhibit and kill Cryptococcus neoformans by a mechanism independent of iron deprivation. J Clin Invest 100 : 1640 1646.
45. Lewin R (1984) How microorganisms transport iron. Science 225 : 401 402.
46. Moreira AP, Dias LA, Peraçoli MTS, Martins M, Calvi SA Soares AMVC (2001) Killing of Paracoccidioides brasiliensis by peritoneal macrophages activated by IFN-gamma or TNF-alpha is mediated by H2O2 and NO. Rev Soc Bras Med Trop 34 : 145.
47. Moscardi-Bacchi M, Brummer E Stevens DA (1994) Support of Paracoccidioides brasiliensis multiplication by human monocytes or macrophages: inhibition by activated phagocytes. J Med Microbiol 40 : 159 164.
48. Musial A Eissa NT (2001) Inducible nitric-oxide synthase is regulated by the proteasome degradation pathway. J Biol Chem 276 : 24268 24273.
49. Nascimento FRF, Calich VLG, Rodríguez D Russo M (2002) Dual role for nitric oxide in paracoccidioidomycosis: essential for resistance, but overproduction associated with susceptibility. J Immunol 168 : 4593 4600.
50. Newman SL, Gootee L, Brunner G Deepe GS 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.
51. Nunez MT, Gaete V, Watkins JA Glass J (1990) Mobilization of iron from endocytic vesicles - the effects of acidification and reduction. J Biol Chem 265 : 6688 6692.
52. Octave JN, Scheneider YJ, Hoffman P, Troluet A Crichton RR (1979) Transferrin protein and iron uptake by culture rat fibroblasts. FEBS Lett 108 : 127 130.
53. Park YC, Ho P, Yoo JC, Choi BM, Jue DM Chung HT (1999) Chloroquine inhibits inducible nitric oxide synthase expression in murine peritoneal macrophages. Pharmacol Toxicol 85 : 188 191.
54. Peraçoli MTS, Sugizaki MF, Mendes RP, Naiff R Montenegro MR (1999) Paracoccidioides brasiliensis isolated from armadillos is virulent to syrian hamsters. Mycopathol 148 : 123 130.
55. Pick A Keisari A (1980) A simple colorimetric method for measurement of hydrogen peroxidase produced by cells in culture. J Immunol Meth 38 : 161 172.
56. Pick E Mizel D (1981) Rapid microassay for the measurement of superoxide and hydrogen peroxide production by macrophage in culture using an automatic enzyme immunoassay reader. J Immunol Meth 46 : 211 226.
57. Princiotto JV Zapolski EJ (1975) Difference between the two iron-bindings sites of transferrin. Nature 255 : 87 88.
58. Rayne F, Vendeville A, Bonhoure A Beaumelle B (2004) The ability of chloroquine to prevent Tat-induced cytokine secretion by monocytes is implicated in its in vivo anti-human immunodeficiency virus type 1 activity. J Virol 78 : 12054 12057.
59. Restrepo A (1985) The ecology of Paracoccidioides brasiliensis: a puzzle still unsolved. J Med Vet Mycol 23 : 323 334.
60. Richardson DR Ponka P (1997) The molecular mechanisms of the metabolism and transport of iron in normal and neoplastic cells. Biochim Biophys Acta 1331 : 1 40.
61. Roberts S Bomford A (1988) Chelation of transferrin iron by desferioxamine in K562 cells - the partition of iron between ferrioxamine and ferritin. Biochem J 254 : 869 875.
62. Sibille J, Kondo H Aisen P (1989) Uptake of ferritin and iron bound to ferritin by rat hepatocytes: modulation by apotransferrin, iron chelators and chloroquine. Biochem Biophys Acta 1010 : 204 208.
63. Silva CL Figueiredo F (1995) Tumor necrosis factor in paracoccidioidomycosis patients. J Infect Dis 164 : 1033 1034.
64. Silva CL, Silva MF, Faccioli LH, Pietro CL, Cortez SA Foss NT (1995) Differential correlation between interleukin patterns in disseminated and chronic human paracoccidioidomycosis. Clin Exp Immunol 101 : 314 320.
65. Singer-Vermes LM, Ciavaglia MC, Kashino SS, Burger E Calich VLG (1992) The source of growth-promoting factor(s) affects the plating efficiency of Paracoccidioides brasiliensis. J Med Vet Mycol 30 : 261 264.
66. Siqueira KZ, Soares AMVC, Calvi SA Peraçoli MTS (2007) Interleukin-6 modulates cytokine production and increases growth of a virulent strain of Paracoccidioides brasiliensis in human monocytes. Cytokine, in press.
67. Slater AF (1993) Chloroquine: mechanism of drug action and resistance in Plasmodium falciparum. Pharmacol Ther 57 : 203 235.
68. Soares AMVC, Calvi SA, Peraçoli MTS, Fernandez AC, Dias LA Anjos AR (2001) Modulatory effect of prostaglandins on human monocyte activation for killing of high- and low-virulence strains of Paracoccidioides brasiliensis. Immunol 102 : 480 485.
69. Soler P Bernaudin JF (1993) Physiology of granulomas. Rev Pneumol Clin 49 : 257 261.
70. Souto JF, Figueiredo F, Furlanetto A, Pfeffer K, Rossi MA Silva JS (2000) Interferon-γ and tumor necrosis factor-α determine resistance to Paracoccidioides brasiliensis infection in mice. Am J Pathol 156 : 1811 1820.
71. Swaiman KF Machen VL (1986) Chloroquine reduces neuronal and glial iron uptake. J Neurochem 46 : 652 654.
72. Utaisincharoen P, Anuntagool N, Chaisuriya P, Pichyangkul S Sirisinha S (2002) CpG ODN activates NO and iNOS production in mouse macrophage cell line (RAW 264-7). Clin Exp Immunol 128 : 467 473.
73. Wallace DJ (1994) Antimalarial agents and lupus. Rheum Dis Clin North Am 20 : 243 263.
74. Wellems TE (1992) Malaria. How chloroquine works. Nature 335 : 108 109.
75. Zar JH (1984) Biostatistical Analysis, 2nd edn. Englewood Cliffs, Prentice-Hall.
76. Zhu X, Ertel W, Ayala A, Morrison MH, Perrin MM Chaudry IH (1993) Chloroquine inhibits macrophage tumor necrosis factor-alpha mRNA transcription. Immunol 80 : 122 126.
77. Ziegler HK Unanue ER (1982) Decrease in macrophage antigen catabolism caused by ammonia and chloroquine is associated with inhibition of arginine presentation to T cells. Proc Natl Acad Sci USA 79 : 175 178.