Therapeutical targeting of nucleic acid-sensing Toll-like receptors prevents experimental cerebral malaria

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 9, 2011, Pages 3689-3694

  Franklin, Bernardo S ^a,b   Ishizaka, Sally T ^c   Lamphier, Marc ^c   Gusovsky, Fabian ^c   Hansen, Hans ^c   Rose, Jeffrey ^c   Zheng, Wanjun ^c   Ataíde, Marco Antônio ^a,b   De Oliveira, Rosane B ^b   Golenbock, Douglas T ^a,b   Gazzinelli, Ricardo T ^a,b,d  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c EISAI RESEARCH INSTITUTE   (United States)

^d FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Immunotherapy; Inflammation; Innate immunity; Nucleic acid recognition

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; ANTIINFLAMMATORY AGENT; E 6446; HYDROXYCHLOROQUINE; SINGLE STRANDED RNA; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BRAIN MALARIA; CEREBROVASCULAR DISEASE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFICACY; DRUG POTENCY; HUMAN; HUMAN CELL; MOUSE; NEUROPATHOLOGY; NONHUMAN; PARALYSIS; PLASMODIUM BERGHEI; PLASMODIUM MALARIAE; PRIORITY JOURNAL; PROTEIN TARGETING; SEPTIC SHOCK; SYMPTOM;

ANIMALS; BLOOD-BRAIN BARRIER; HUMANS; HYDROCARBONS, AROMATIC; INFLAMMATION; LIPOPOLYSACCHARIDES; MALARIA, CEREBRAL; MICE; MICE, INBRED C57BL; NUCLEIC ACIDS; PLASMODIUM CHABAUDI; SHOCK, SEPTIC; TOLL-LIKE RECEPTORS;

PLASMODIUM BERGHEI;

EID: 79952753327     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1015406108     Document Type: Article

References (47)

1. Hay SI, et al. (2009) A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med 6:e1000048.
2. Maher B (2008) Malaria: The end of the beginning. Nature 451:1042-1046.
3. Gatton ML, Cheng Q (2002) Evaluation of the pyrogenic threshold for Plasmodium falciparum malaria in naive individuals. Am J Trop Med Hyg 66:467-473.
4. Boutlis CS, Yeo TW, Anstey NM (2006) Malaria tolerance-For whom the cell tolls? Trends Parasitol 22:371-377.
5. Eyles DE, Young MD (1951) The duration of untreated or inadequately treated Plasmodium falciparum infections in the human host. J Natl Malar Soc 10:327-336.
6. O'Neill LA, Bryant CE, Doyle SL (2009) Therapeutic targeting of Toll-like receptors for infectious and inflammatory diseases and cancer. Pharmacol Rev 61:177-197.
7. Sun S, Rao NL, Venable J, Thurmond R, Karlsson L (2007) TLR7/9 antagonists as therapeutics for immune-mediated inflammatory disorders. Inflamm Allergy Drug Targets 6:223-235.
8. Kalia S, Dutz JP (2007) New concepts in antimalarial use and mode of action in dermatology. Dermatol Ther 20:160-174. (Pubitemid 350029307)
9. Togbe D, et al. (2007) Murine cerebral malaria development is independent of toll-like receptor signaling. Am J Pathol 170:1640-1648. (Pubitemid 47339308)
10. Adachi K, et al. (2001) Plasmodium berghei infection in mice induces liver injury by an IL-12- and toll-like receptor/myeloid differentiation factor 88-dependent mechanism. J Immunol 167:5928-5934. (Pubitemid 33062788)
11. Krishnegowda G, et al. (2005) Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: Cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J Biol Chem 280:8606-8616. (Pubitemid 40349765)
12. Coban C, et al. (2005) Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. J Exp Med 201:19-25. (Pubitemid 40130079)
13. Coban C, et al. (2007) Pathological role of Toll-like receptor signaling in cerebral malaria. Int Immunol 19:67-79. (Pubitemid 46017889)
14. Ockenhouse CF, et al. (2006) Common and divergent immune response signaling pathways discovered in peripheral blood mononuclear cell gene expression patterns in presymptomatic and clinically apparent malaria. Infect Immun 74:5561-5573. (Pubitemid 44484539)
15. Tripathi AK, Sha W, Shulaev V, Stins MF, Sullivan DJ, Jr. (2009) Plasmodium falciparum-infected erythrocytes induce NF-kappaB regulated inflammatory pathways in human cerebral endothelium. Blood 114:4243-4252.
16. McCall MB, et al. (2007) Plasmodium falciparum infection causes proinflammatory priming of human TLR responses. J Immunol 179:162-171. (Pubitemid 46986530)
17. Sam-Agudu NA, et al. (2010) TLR9 polymorphisms are associated with altered IFN-gamma levels in children with cerebral malaria. Am J Trop Med Hyg 82:548-555.
18. Franklin BS, et al. (2007) MyD88-dependent activation of dendritic cells and CD4(+) T lymphocytes mediates symptoms, but is not required for the immunological control of parasites during rodent malaria. Microbes Infect 9:881-890. (Pubitemid 46891856)
19. Franklin BS, et al. (2009) Malaria primes the innate immune response due to interferon-gamma induced enhancement of toll-like receptor expression and function. Proc Natl Acad Sci USA 106:5789-5794.
20. Parroche P, et al. (2007) Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc Natl Acad Sci USA 104:1919-1924. (Pubitemid 46239879)
21. Clark IA (1978) Does endotoxin cause both the disease and parasite death in acute malaria and babesiosis? Lancet 2:75-77.
22. Hartgers FC, et al. (2008) Enhanced Toll-like receptor responsiveness associated with mitogen-activated protein kinase activation in Plasmodium falciparum-infected children. Infect Immun 76:5149-5157.
23. Chow JC, Young DW, Golenbock DT, Christ WJ, Gusovsky F (1999) Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J Biol Chem 274:10689-10692.
24. Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa C (2004) Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303:1529-1531. (Pubitemid 38314425)
25. Jurk M, et al. (2002) Human TLR7 or TLR8 independently confer responsiveness to the antiviral compound R-848. Nat Immunol 3:499. (Pubitemid 34669818)
26. Fox RI (1993) Mechanism of action of hydroxychloroquine as an antirheumatic drug. Semin Arthritis Rheum 23 (Suppl 1):82-91.
27. Savarino A, Boelaert JR, Cassone A, Majori G, Cauda R (2003) Effects of chloroquine on viral infections: An old drug against today's diseases? Lancet Infect Dis 3:722-727.
28. Wallace DJ, Linker-Israeli M, Hyun S, Klinenberg JR, Stecher V (1994) The effect of hydroxychloroquine therapy on serum levels of immunoregulatory molecules in patients with systemic lupus erythematosus. J Rheumatol 21:375-376. (Pubitemid 24078865)
29. Griffith JW, et al. (2007) Toll-like receptor modulation of murine cerebral malaria is dependent on the genetic background of the host. J Infect Dis 196:1553-1564. (Pubitemid 351411993)
30. Langhorne J, et al. (2004) Dendritic cells, pro-inflammatory responses, and antigen presentation in a rodent malaria infection. Immunol Rev 201:35-47. (Pubitemid 39318442)
31. Ing R, Segura M, Thawani N, Tam M, Stevenson MM (2006) Interaction of mouse dendritic cells and malaria-infected erythrocytes: Uptake, maturation, and antigen presentation. J Immunol 176:441-450. (Pubitemid 43023290)
32. Brinkmann MM, et al. (2007) The interaction between the ER membrane protein UNC93B and TLR3, 7, and 9 is crucial for TLR signaling. J Cell Biol 177:265-275. (Pubitemid 46658638)
33. Hunt NH, et al. (2006) Immunopathogenesis of cerebral malaria. Int J Parasitol 36:569-582. (Pubitemid 43674512)
34. Clark IA, Budd AC, Alleva LM, Cowden WB (2006) Human malarial disease: A consequence of inflammatory cytokine release. Malar J 5:85.
35. Hunt NH, Grau GE (2003) Cytokines: Accelerators and brakes in the pathogenesis of cerebral malaria. Trends Immunol 24:491-499. (Pubitemid 37088152)
36. Haldar K, Murphy SC, Milner DA, Taylor TE (2007) Malaria: Mechanisms of erythrocytic infection and pathological correlates of severe disease. Annu Rev Pathol 2:217-249. (Pubitemid 46448065)
37. Garcia I, et al. (1995) Transgenic mice expressing high levels of soluble TNF-R1 fusion protein are protected from lethal septic shock and cerebral malaria, and are highly sensitive to Listeria monocytogenes and Leishmania major infections. Eur J Immunol 25:2401-2407.
38. Campanella GS, et al. (2008) Chemokine receptor CXCR3 and its ligands CXCL9 and CXCL10 are required for the development of murine cerebral malaria. Proc Natl Acad Sci USA 105:4814-4819. (Pubitemid 351753829)
39. Collins WE, Jeffery GM, Roberts JM (2003) A retrospective examination of anemia during infection of humans with Plasmodium vivax. Am J Trop Med Hyg 68:410-412. (Pubitemid 38230639)
40. Young NS (1995) Aplastic anaemia. Lancet 346:228-232.
41. Thawani N, Tam M, Stevenson MM (2009) STAT6-mediated suppression of erythropoiesis in an experimental model of malarial anemia. Haematologica 94:195-204.
42. Lamikanra AA, Theron M, Kooij TW, Roberts DJ (2009) Hemozoin (malarial pigment) directly promotes apoptosis of erythroid precursors. PLoS ONE 4:e8446.
43. McDevitt MA, Xie J, Gordeuk V, Bucala R (2004) The anemia of malaria infection: Role of inflammatory cytokines. Curr Hematol Rep 3:97-106.
44. van Hensbroek MB, et al. (1996) The effect of a monoclonal antibody to tumor necrosis factor on survival from childhood cerebral malaria. J Infect Dis 174:1091-1097.
45. Hermsen C, van de Wiel T, Mommers E, Sauerwein R, Eling W (1997) Depletion of CD4+ or CD8+ T-cells prevents Plasmodium berghei induced cerebral malaria in end-stage disease. Parasitology 114:7-12. (Pubitemid 27022698)
46. Noedl H, et al.; (2008) Artemisinin Resistance in Cambodia 1 (ARC1) Study Consortium (2008) Evidence of artemisinin-resistant malaria in western Cambodia. N Engl J Med 359:2619-2620.
47. Dondorp AM, et al. (2009) Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 361:455-467.