Early treatment with chloroquine inhibits the immune response against Plasmodium yoelii infection in mice

Tohoku Journal of Experimental Medicine

Volumn 234, Issue 4, 2014, Pages 271-280

  Qin, Xiaosong ^a   Chen, Guang ^b   Feng, Yonghui ^a   Zhu, Xiaotong ^a   Du, Yunting ^a   Pang, Wei ^a   Qi, Zanmei ^a   Cao, Yaming ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b Jamusi University   (China)

Author keywords

Chloroquine; Early infection; Immune response; Immune suppression; Plasmodium yoelii 17XL

Indexed keywords

CHLOROQUINE; GAMMA INTERFERON; INTERLEUKIN 4; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA; ANTIMALARIAL AGENT; TLR9 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL VIABILITY; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG EFFICACY; FEMALE; FLOW CYTOMETRY; HELPER CELL; IMMUNE RESPONSE; IMMUNOMODULATION; INTERNALIZATION; MOUSE; NONHUMAN; PLASMODIUM YOELII INFECTION; PROTEIN EXPRESSION; SINGLE DRUG DOSE; SPLEEN CELL; ANIMAL; DBA MOUSE; DISEASE COURSE; DISEASE MODEL; DRUG EFFECTS; HUMORAL IMMUNITY; IMMUNOLOGY; MALARIA; METABOLISM; PARASITOLOGY; PLASMODIUM YOELII; TH2 CELL;

ANIMALS; ANTIMALARIALS; CHLOROQUINE; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; MALARIA; MICE, INBRED DBA; PLASMODIUM YOELII; TH2 CELLS; TOLL-LIKE RECEPTOR 9;

EID: 84919389225     PISSN: 00408727     EISSN: 13493329     Source Type: Journal    
DOI: 10.1620/tjem.234.271     Document Type: Article

References (47)

1. Ahvazi, B.C., Jacobs, P. & Stevenson, M.M. (1995) Role of macrophage-derived nitric oxide in suppression of lymphocyte proliferation during blood-stage malaria. J. Leukoc. Biol., 58, 23-31.
2. Amet, S., Zimner-Rapuch, S., Launay-Vacher, V., Janus, N. & Deray, G. (2013) Malaria prophylaxis in patients with renal impairment: a review. Drug Saf., 36, 83-91.
3. Awab, G.R., Pukrittayakamee, S., Imwong, M., Dondorp, A.M., Woodrow, C.J., Lee, S.J., Day, N.P., Singhasivanon, P., White, N.J. & Kaker, F. (2010) Dihydroartemisinin-piperaquine versus chloroquine to treat vivax malaria in Afghanistan: an open randomized, non-inferiority, trial. Malar. J., 9, 105.
4. Baird, J.K. (2004) Chloroquine resistance in Plasmodium vivax. Antimicrob. Agents Chemother., 48, 4075-4083.
5. Baird, J.K. (2009) Resistance to therapies for infection by Plasmo-dium vivax. Clin. Microbiol. Rev., 22, 508-534.
6. Bauer, S., Kirschning, C.J., Hacker, H., Redecke, V., Hausmann, S., Akira, S., Wagner, H. & Lipford, G.B. (2001) Human TLR9 confers responsiveness to bacterial DNA via species-specifc CpG motif recognition. Proc. Natl. Acad. Sci. USA, 98, 9237-9242.
7. Coban, C., Ishii, K.J., Kawai, T., Hemmi, H., Sato, S., Uematsu, S., Yamamoto, M., Takeuchi, O., Itagaki, S., Kumar, N., Horii, T. & Akira, S. (2005) Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J. Exp. Med., 201, 19-25.
8. Fidock, D.A., Rosenthal, P.J., Croft, S.L., Brun, R. & Nwaka, S. (2004) Antimalarial drug discovery: efficacy models for compound screening. Nat. Rev. Drug Discov., 3, 509-520.
9. Harinasuta, T., Suntharasamai, P. & Viravan, C. (1965) Chloro-quine-resistant falciparum malaria in Thailand. Lancet, 2, 657-660.
10. He, B., Qiao, X. & Cerutti, A. (2004) CpG DNA induces IgG class switch DNA recombination by activating human B cells through an innate pathway that requires TLR9 and cooperates with IL-10. J. Immunol., 173, 4479-4491.
11. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M., Hoshino, K., Wagner, H., Takeda, K. & Akira, S. (2000) A Toll-like receptor recognizes bacterial DNA. Nature, 408, 740-745.
12. Hong, Z., Jiang, Z., Liangxi, W., Guofu, D., Ping, L., Yongling, L., Wendong, P. & Minghai, W. (2004) Chloroquine protects mice from challenge with CpG ODN and LPS by decreasing proin-flammatory cytokine release. Int. Immunopharmacol., 4, 223-234.
13. Huang, L.Y., Ishii, K.J., Akira, S., Aliberti, J. & Golding, B. (2005) Th1-like cytokine induction by heat-killed Brucella abortus is dependent on triggering of TLR9. J. Immunol., 175, 3964-3970.
14. Iwasaki, A. & Medzhitov, R. (2004) Toll-like receptor control of the adaptive immune responses. Nat. Immunol., 5, 987-995.
15. Kadowaki, N., Ho, S., Antonenko, S., Malefyt, R.W., Kastelein, R.A., Bazan, F. & Liu, Y.J. (2001) Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J. Exp. Med., 194, 863-869.
16. Kamugisha, E., Bujila, I., Lahdo, M., Pello-Esso, S., Minde, M., Kongola, G., Naiwumbwe, H., Kiwuwa, S., Kaddumukasa, M., Kironde, F. & Swedberg, G. (2012) Large differences in prevalence of Pfcrt and Pfmdr1 mutations between Mwanza, Tanzania and Iganga, Uganda-a reflection of differences in policies regarding withdrawal of chloroquine? Acta Trop., 121, 148-151.
17. Kapsenberg, M.L. (2003) Dendritic-cell control of pathogen-driven T-cell polarization. Nat. Rev. Immunol., 3, 984-993.
18. Katze, M.G., He, Y. & Gale, M. Jr. (2002) Viruses and interferon: a fght for supremacy. Nat. Rev. Immunol., 2, 675-687.
19. Krishnegowda, G., Hajjar, A.M., Zhu, J., Douglass, E.J., Uematsu, S., Akira, S., Woods, A.S. & Gowda, D.C. (2005) Induction of proinfammatory responses in macrophages by the glyco-sylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J. Biol. Chem., 280, 8606-8616.
20. Kublin, J.G., Cortese, J.F., Njunju, E.M., Mukadam, R.A., Wirima, J.J., Kazembe, P.N., Djimde, A.A., Kouriba, B., Taylor, T.E. & Plowe, C.V. (2003) Reemergence of chloroquine-sensitive Plasmodium falciparum malaria after cessation of chloroquine use in Malawi. J. Infect. Dis., 187, 1870-1875.
21. Litinskiy, M.B., Nardelli, B., Hilbert, D.M., He, B., Schaffer, A., Casali, P. & Cerutti, A. (2002) DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat. Immunol., 3, 822-829.
22. Liu, N., Ohnishi, N., Ni, L., Akira, S. & Bacon, K.B. (2003) CpG directly induces T-bet expression and inhibits IgG1 and IgE switching in B cells. Nat. Immunol., 4, 687-693.
23. Manicassamy, S. & Pulendran, B. (2009) Modulation of adaptive immunity with Toll-like receptors. Semin. Immunol., 21, 185-193.
24. Meier, F.M., Frerix, M., Hermann, W. & Muller-Ladner, U. (2013) Current immunotherapy in rheumatoid arthritis. Immuno-therapy, 5, 955-974.
25. Mita, T., Kaneko, A., Lum, J.K., Bwijo, B., Takechi, M., Zungu, I.L., Tsukahara, T., Tanabe, K., Kobayakawa, T. & Bjorkman, A. (2003) Recovery of chloroquine sensitivity and low prevalence of the Plasmodium falciparum chloroquine resistance transporter gene mutation K76T following the discontinuance of chloroquine use in Malawi. Am. J. Trop. Med. Hyg., 68, 413-415.
26. Moore, B.R., Page-Sharp, M., Stoney, J.R., Ilett, K.F., Jago, J.D. & Batty, K.T. (2011) Pharmacokinetics, pharmacodynamics, and allometric scaling of chloroquine in a murine malaria model. Antimicrob. Agents Chemother., 55, 3899-3907.
27. Mwai, L., Ochong, E., Abdirahman, A., Kiara, S.M., Ward, S., Kokwaro, G., Sasi, P., Marsh, K., Borrmann, S., Mackinnon, M. & Nzila, A. (2009) Chloroquine resistance before and after its withdrawal in Kenya. Malar. J., 8, 106.
28. Parroche, P., Lauw, F.N., Goutagny, N., Latz, E., Monks, B.G., Visintin, A., Halmen, K.A., Lamphier, M., Olivier, M., Bartholomeu, D.C., Gazzinelli, R.T. & Golenbock, D.T. (2007) Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Tolllike receptor 9. Proc. Natl. Acad. Sci. USA, 104, 1919-1924.
29. Poeck, H., Wagner, M., Battiany, J., Rothenfusser, S., Wellisch, D., Hornung, V., Jahrsdorfer, B., Giese, T., Endres, S. & Hartmann, G. (2004) Plasmacytoid dendritic cells, antigen, and CpG-C license human B cells for plasma cell differentiation and immunoglobulin production in the absence of T-cell help. Blood, 103, 3058-3064.
30. Price, R.N., Douglas, N.M. & Anstey, N.M. (2009) New developments in Plasmodium vivax malaria: severe disease and the rise of chloroquine resistance. Curr. Opin. Infect. Dis., 22, 430-435.
31. Reis e Sousa, C. (2006) Dendritic cells in a mature age. Nat. Rev. Immunol., 6, 476-483.
32. Sancho, D., Gomez, M. & Sanchez-Madrid, F. (2005) CD69 is an immunoregulatory molecule induced following activation. Trends Immunol., 26, 136-140.
33. Slater, A.F. (1993) Chloroquine: mechanism of drug action and resistance in Plasmodium falciparum. Pharmacol. Ther., 57, 203-235.
34. Srivastava, H.C., Yadav, R.S., Joshi, H., Valecha, N., Mallick, P.K., Prajapati, S.K. & Dash, A.P. (2008) Therapeutic responses of Plasmodium vivax and P. falciparum to chloroquine, in an area of western India where P. vivax predominates. Ann. Trop. Med. Parasitol., 102, 471-480.
35. Steinman, R.M. & Hemmi, H. (2006) Dendritic cells: translating innate to adaptive immunity. Curr. Top. Microbiol. Immunol., 311, 17-58.
36. Stephens, R., Albano, F.R., Quin, S., Pascal, B.J., Harrison, V., Stockinger, B., Kioussis, D., Weltzien, H.U. & Langhorne, J. (2005) Malaria-specific transgenic CD4(+) T cells protect immunodefcient mice from lethal infection and demonstrate requirement for a protective threshold of antibody production for parasite clearance. Blood, 106, 1676-1684.
37. Su, Z. & Stevenson, M.M. (2002) IL-12 is required for antibody-mediated protective immunity against blood-stage Plasmo-dium chabaudi AS malaria infection in mice. J. Immunol., 168, 1348-1355.
38. Thome, R., Issayama, L.K., DiGangi, R., Bombeiro, A.L., da Costa, T.A., Ferreira, I.T., de Oliveira, A.L. & Verinaud, L. (2014) Dendritic cells treated with chloroquine modulate experimental autoimmune encephalomyelitis. Immunol. Cell Biol., 92, 124-132.
39. Thome, R., Lopes, S.C., Costa, F.T. & Verinaud, L. (2013) Chloroquine: modes of action of an undervalued drug. Immunol. Lett., 153, 50-57.
40. Vijaykadga, S., Rojanawatsirivej, C., Congpoung, K., Wilairatana, P., Satimai, W., Uaekowitchai, C., Pumborplub, B., Sittimongkol, S., Pinyorattanachote, A. & Prigchoo, P. (2004) Assessment of therapeutic efficacy of chloroquine for vivax malaria in Thailand. Southeast Asian J. Trop. Med. Public Health, 35, 566-569.
41. Weber, S.M. & Levitz, S.M. (2000) Chloroquine interferes with lipopolysaccharide-induced TNF-alpha gene expression by a nonlysosomotropic mechanism. J. Immunol., 165, 1534-1540.
42. World Health Organization (2011) World Malaria Report 2011. http://www.who.int/malaria/world_malaria_report_2011/en/ [Accessed: May 8, 2014].
43. Wu, X., Gowda, N.M., Kumar, S. & Gowda, D.C. (2010) Protein-DNA complex is the exclusive malaria parasite component that activates dendritic cells and triggers innate immune responses. J. Immunol., 184, 4338-4348.
44. Wykes, M.N. & Good, M.F. (2008) What really happens to dendritic cells during malaria? Nat. Rev. Microbiol., 6, 864-870.
45. Yayon, A., Timberg, R., Friedman, S. & Ginsburg, H. (1984) Effects of chloroquine on the feeding mechanism of the intraerythrocytic human malarial parasite Plasmodium falci-parum. J. Protozool., 31, 367-372.
46. Yi, A.K., Tuetken, R., Redford, T., Waldschmidt, M., Kirsch, J. & Krieg, A.M. (1998) CpG motifs in bacterial DNA activate leukocytes through the pH-dependent generation of reactive oxygen species. J. Immunol., 160, 4755-4761.
47. Zhu, X., Pan, Y., Li, Y., Jiang, Y., Shang, H., Gowda, D.C., Cui, L. & Cao, Y. (2012) Targeting Toll-like receptors by chloroquine protects mice from experimental cerebral malaria. Int. Immu-nopharmacol., 13, 392-397.