Opsonization of malaria-infected erythrocytes activates the inflammasome and enhances inflammatory cytokine secretion by human macrophages

Malaria Journal

Volumn 11, Issue , 2012, Pages

  Zhou, Jingling ^a   Ludlow, Louise E ^c,d   Hasang, Wina ^c,d   Rogerson, Stephen J ^c,d   Jaworowski, Anthony ^a,b  

^a BURNET INSTITUTE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d ROYAL MELBOURNE HOSPITAL   (Australia)

Author keywords

Antibody; Fc gamma receptor; Human; Monocyte derived macrophages; Phagocytosis; Plasmodium falciparum; Pro inflammatory cytokines

Indexed keywords

FC RECEPTOR; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 6; MESSENGER RNA; PROTEIN P50; SYNAPTOTAGMIN I; TUMOR NECROSIS FACTOR;

ARTICLE; CONTROLLED STUDY; CROSS LINKING; CYTOKINE RELEASE; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ERYTHROCYTE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOREACTIVITY; INTRACELLULAR SIGNALING; MACROPHAGE; MALARIA FALCIPARUM; MONOCYTE; MONOCYTE DERIVED MACROPHAGE; OPSONIZATION; PHAGOCYTOSIS; PLASMODIUM FALCIPARUM INFECTED ERYTHROCYTE; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; WILCOXON SIGNED RANKS TEST;

BLOTTING, WESTERN; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; ERYTHROCYTES; HUMANS; INFLAMMASOMES; MACROPHAGES; MALARIA, FALCIPARUM; OPSONIN PROTEINS; PLASMODIUM FALCIPARUM; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84867128779     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-11-343     Document Type: Article

References (55)

1. Malaria in pregnancy: linking immunity and pathogenesis to prevention. Rogerson SJ, Mwapasa V, Meshnick SR, Am J Trop Med Hyg 2007 77 14 22 18165470
2. Gamma-globulin and acquired immunity to human malaria. Cohen S, McGregor IA, Carrington S, Nature 1961 192 733 737 10.1038/192733a0 13880318
3. Parasitologic and clinical human response to immunoglobulin administration in falciparum malaria. Sabchareon A, Burnouf T, Ouattara D, Attanath P, Bouharoun-Tayoun H, Chantavanich P, Foucault C, Chongsuphajaisiddhi T, Druilhe P, Am J Trop Med Hyg 1991 45 297 308 1928564
4. IVIG-Mechanisms of action. Simon HU, Spath PJ, Allergy 2003 58 543 552 10.1034/j.1398-9995.2003.00239.x 12823109 (Pubitemid 36831306)
5. Do maternally acquired antibodies protect infants from malaria infection? Riley EM, Wagner GE, Akanmori BD, Koram KA, Parasite Immunol 2001 23 51 59 10.1046/j.1365-3024.2001.00364.x 11240896 (Pubitemid 32231907)
6. Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Marsh K, Otoo L, Hayes RJ, Carson DC, Greenwood BM, Trans R Soc Trop Med Hyg 1989 83 293 303 10.1016/0035-9203(89)90478-1 2694458 (Pubitemid 19163208)
7. The role of antibodies to Plasmodium falciparum-infected-erythrocyte surface antigens in naturally acquired immunity to malaria. Bull PC, Marsh K, Trends Microbiol 2002 10 55 58 10.1016/S0966-842X(01)02278-8 11827798 (Pubitemid 34119334)
8. The immunological challenge to developing a vaccine to the blood stages of malaria parasites. Good MF, Stanisic D, Xu H, Elliott S, Wykes M, Immunol Rev 2004 201 254 267 10.1111/j.0105-2896.2004.00178.x 15361246 (Pubitemid 39318457)
9. Target antigens of purified human immunoglobulins which inhibit growth of Plasmodium falciparum in vitro. Brown GV, Anders RF, Mitchell GF, Heywood PF, Nature 1982 297 591 593 10.1038/297591a0 7045680 (Pubitemid 12027626)
10. Merozoite surface protein-3: a malaria protein inducing antibodies that promote Plasmodium falciparum killing by cooperation with blood monocytes. Oeuvray C, Bouharoun-Tayoun H, Gras-Masse H, Bottius E, Kaidoh T, Aikawa M, Filgueira MC, Tartar A, Druilhe P, Blood 1994 84 1594 1602 8068948 (Pubitemid 24273030)
11. The glutamate-rich protein (GLURP) of Plasmodium falciparum is a target for antibody-dependent monocyte-mediated inhibition of parasite growth in vitro. Theisen M, Soe S, Oeuvray C, Thomas AW, Vuust J, Danielsen S, Jepsen S, Druilhe P, Infect Immun 1998 66 11 17 9423833 (Pubitemid 28018795)
12. Specificity of the protective antibody response to apical membrane antigen 1. Hodder AN, Crewther PE, Anders RF, Infect Immun 2001 69 3286 3294 10.1128/IAI.69.5.3286-3294.2001 11292751 (Pubitemid 32332227)
13. Antibodies against merozoite surface protein (MSP)-1(19) are a major component of the invasion-inhibitory response in individuals immune to malaria. O'Donnell RA, de Koning-Ward TF, Burt RA, Bockarie M, Reeder JC, Cowman AF, Crabb BS, J Exp Med 2001 193 1403 1412 10.1084/jem.193.12.1403 11413195 (Pubitemid 32565969)
14. Variation in use of erythrocyte invasion pathways by Plasmodium falciparum mediates evasion of human inhibitory antibodies. Persson KEM, McCallum FJ, Reiling L, Lister NA, Stubbs J, Cowman AF, Marsh K, Beeson JG, J Clin Invest 2008 118 342 351 10.1172/JCI32138 18064303
15. Maternal antibodies block malaria. Fried M, Nosten F, Brockman A, Brabin BJ, Duffy PE, Nature 1998 395 851 852 10.1038/27570 9804416 (Pubitemid 28503415)
16. Strain-transcending Fc-dependent killing of Plasmodium falciparum by merozoite surface protein 2 allele-specific human antibodies. Stubbs J, Olugbile S, Saidou B, Simpore J, Corradin G, Lanzavecchia A, Infect Immun 2011 79 1143 1152 10.1128/IAI.01034-10 21189324
17. Relationship between human immunodeficiency virus type 1 coinfection, anemia, and levels and function of antibodies to variant surface antigens in pregnancy-associated malaria. Jaworowski A, Fernandes LA, Yosaatmadja F, Feng G, Mwapasa V, Molyneux ME, Meshnick SR, Lewis J, Rogerson SJ, Clin Vaccine Immunol 2009 16 312 319 10.1128/CVI.00356-08 19129467
18. Antigenic diversity of Plasmodium falciparum and antibody-mediated parasite neutralization. Bolad A, Berzins K, Scand J Immunol 2000 52 233 239 10.1046/j.1365-3083.2000.00787.x 10972898
19. IgG3 antibodies to Plasmodium falciparum merozoite surface protein 2 (MSP2): increasing prevalence with age and association with clinical immunity to malaria. Taylor RR, Allen SJ, Greenwood BM, Riley EM, Am J Trop Med Hyg 1998 58 406 413 9574783 (Pubitemid 28183248)
20. Serum IgG3 to the Plasmodium falciparum merozoite surface protein 2 is strongly associated with a reduced prospective risk of malaria. Metzger WG, Okenu DMN, Cavanagh DR, Robinson JV, Bojang KA, Weiss HA, McBride JS, Greenwood BM, Conway DJ, Parasite Immunol 2003 25 307 312 10.1046/j.1365-3024.2003.00636.x 14507328 (Pubitemid 38019285)
21. Cytophilic antibodies to Plasmodium falciparum glutamate rich protein are associated with malaria protection in an area of holoendemic transmission. Lusingu JP, Vestergaard LS, Alifrangis M, Mmbando BP, Theisen M, Kitua AY, Lemnge MM, Theander TG, Malar J 2005 4 48 10.1186/1475-2875-4-48 16194274 (Pubitemid 41548317)
22. Naturally acquired immunoglobulin (Ig)G subclass antibodies to crude asexual Plasmodium falciparum lysates: evidence for association with protection for IgG1 and disease for IgG2. Ndungu FM, Bull PC, Ross A, Lowe BS, Kabiru E, Marsh K, Parasite Immunol 2002 24 77 82 10.1046/j.0141-9838.2001.00440.x 11874562 (Pubitemid 34225276)
23. Long-term clinical protection from falciparum malaria is strongly associated with IgG3 antibodies to merozoite surface protein 3. Roussilhon C, Oeuvray C, Müller-Graf C, Tall A, Rogier C, Trape J-F, Theisen M, Balde A, Pérignon J-L, Druilhe P, PLoS Med 2007 4 320 10.1371/journal.pmed.0040320 18001147 (Pubitemid 350220532)
24. Immunoglobulin G subclass-specific responses against Plasmodium falciparum merozoite antigens are associated with control of parasitemia and protection from symptomatic illness. Stanisic DI, Richards JS, McCallum FJ, Michon P, King CL, Schoepflin S, Gilson PR, Murphy VJ, Anders RF, Mueller I, Beeson JG, Infect Immun 2009 77 1165 1174 10.1128/IAI.01129-08 19139189
25. Effects of pregnancy and intensity of Plasmodium falciparum transmission on immunoglobulin G subclass responses to variant surface antigens. Megnekou R, Staalsoe T, Taylor DW, Leke R, Hviid L, Infect Immun 2005 73 4112 4118 10.1128/IAI.73.7.4112-4118.2005 15972500 (Pubitemid 40923152)
26. Placental malaria induces variant-specific antibodies of the cytophilic subtypes immunoglobulin G1 (IgG1) and IgG3 that correlate with adhesion inhibitory activity. Elliott SR, Brennan AK, Beeson JG, Tadesse E, Molyneux ME, Brown GV, Rogerson SJ, Infect Immun 2005 73 5903 5907 10.1128/IAI.73.9.5903- 5907.2005 16113309 (Pubitemid 41193027)
27. Association of Fcgamma receptor IIa (CD32) polymorphism with severe malaria in West Africa. Cooke GS, Aucan C, Walley AJ, Segal S, Greenwood BM, Kwiatkowski DP, Hill AVS, Am J Trop Med Hyg 2003 69 565 568 14740869 (Pubitemid 38248224)
28. Fcgamma receptor IIA and IIIB polymorphisms are associated with susceptibility to cerebral malaria. Omi K, Ohashi J, Patarapotikul J, Hananantachai H, Naka I, Looareesuwan S, Tokunaga K, Parasitol Int 2002 51 361 366 10.1016/S1383-5769(02)00040-5 12421634 (Pubitemid 35287508)
29. Fcgamma receptor IIa (CD32) polymorphism is associated with protection of infants against high-density Plasmodium falciparum infection. VII. Asembo Bay Cohort Project. Shi YP, Nahlen BL, Kariuki S, Urdahl KB, McElroy PD, Roberts JM, J Infect Dis 2001 184 107 111 10.1086/320999 11398118 (Pubitemid 32568509)
30. Association of FCgamma receptor IIA (CD32) polymorphism with malarial anemia and high-density parasitemia in infants and young children. Ouma C, Keller CC, Opondo DA, Were T, Otieno RO, Otieno MF, Orago ASS, Ong'Echa JM, Vulule JM, Ferrell RE, Perkins DJ, Am J Trop Med Hyg 2006 74 573 577 16606986 (Pubitemid 46774435)
31. Cutting edge: biasing immune responses by directing antigen to macrophage Fc gamma receptors. Anderson CF, Mosser DM, J Immunol 2002 168 3697 3701 11937518 (Pubitemid 34298366)
32. A novel phenotype for an activated macrophage: the type 2 activated macrophage. Anderson CF, Mosser DM, J Leukoc Biol 2002 72 101 106 12101268
33. Possible importance of macrophage -derived mediators in acute malaria. Clark IA, Virelizier J-L, Carswell EA, Wood PR, Infect Immun 1981 32 1058 1066 6166564 (Pubitemid 11109808)
34. Divergent roles of IRAK4-mediated innate immune responses in two experimental models of severe malaria. Finney CAM, Lu Z, Hawkes M, Yeh W-C, Liles WC, Kain KC, Am J Trop Med Hyg 2010 83 69 74 10.4269/ajtmh.2010.09-0753 20595480
35. HIV-1 Inhibits phagocytosis and inflammatory cytokine responses of human monocyte-derived macrophages to P. falciparum infected erythrocytes. Ludlow LE, Zhou J, Tippett E, Cheng W-J, Hasang W, Rogerson SJ, Jaworowski A, PLoS One 2012 7 32102 10.1371/journal.pone.0032102 22363802
36. Adhesion of malaria-infected red blood cells to chondroitin sulfate A under flow conditions. Cooke BM, Rogerson SJ, Brown GV, Coppel RL, Blood 1996 88 4040 4044 8916971 (Pubitemid 26383129)
37. The mechanism underlying defective Fc gamma receptor-mediated phagocytosis by HIV-1-infected human monocyte-derived macrophages. Leeansyah E, Wines B, Crowe S, Jaworowski A, J Immunol 2007 178 1096 17202373
38. Quantifying complement-mediated phagocytosis by human monocyte-derived macrophages. Chan HT, Kedzierska K, O'Mullane J, Crowe SM, Jaworowski A, Immunol Cell Biol 2001 79 429 435 10.1046/j.1440-1711.2001.01027.x 11564150 (Pubitemid 34225137)
39. CyProQuant-PCR: a real time RT-PCR technique for profiling human cytokines, based on external RNA standards, readily automatable for clinical use. Boeuf P, Vigan-Womas I, Jublot D, Loizon S, Barale J-C, Akanmori BD, Mercereau-Puijalon O, Behr C, BMC Immunol 2005 6 5 18 10.1186/1471-2172-6-5 15748278 (Pubitemid 41418119)
40. Carbon Monoxide blocks lipopolysaccharide-induced gene expression by interfering with proximal TLR4 to NF-κB signal transduction in human monocytes. Chhikara M, Wang S, Kern SJ, Ferreyra GA, Barb JJ, Munson PJ, Danner RL, PLoS One 2009 4 8139 10.1371/journal.pone.0008139 19956541
41. Innate immune recognition. Janeway CA Jr, Medzhitov R, Annu Rev Immunol 2002 20 197 216 10.1146/annurev.immunol.20.083001.084359 11861602 (Pubitemid 34293424)
42. Emerging inflammasome effector mechanisms. Lamkanfi M, Nat Rev Immunol 2011 11 213 220 10.1038/nri2936 21350580
43. Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. Krishnegowda G, Hajjar AM, Zhu J, Douglass EJ, Uematsu S, Akira S, Woods AS, Gowda DC, J Biol Chem 2005 280 8606 8616 15623512 (Pubitemid 40349765)
44. Mast cell-mediated immune responses through IgE antibody and Toll-like receptor 4 by malarial peroxiredoxin. Furuta T, Imajo-Ohmi S, Fukuda H, Kano S, Miyake K, Watanabe N, Eur J Immunol 2008 38 1341 1350 10.1002/eji.200738059 18398934
45. Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. Coban C, Ishii KJ, Kawai T, Hemmi H, Sato S, Uematsu S, Yamamoto M, Takeuchi O, Itagaki S, Kumar N, Horii T, Akira S, J Exp Med 2005 201 19 25 10.1084/jem.20041836 15630134 (Pubitemid 40130079)
46. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Parroche P, Lauw FN, Goutagny N, Latz E, Monks BG, Visintin A, Halmen KA, Lamphier M, Olivier M, Bartholomeu DC, Gazzinelli RT, Golenbock DT, Proc Natl Acad Sci USA 2007 104 1919 1924 10.1073/pnas.0608745104 17261807 (Pubitemid 46239879)
47. Pure hemozoin is inflammatory in vivo and activates the NALP3 inflammasome via release of uric acid. Griffith JW, Sun T, McIntosh MT, Bucala R, J Immunol 2009 183 5208 5220 10.4049/jimmunol.0713552 19783673
48. Protein-DNA complex is the exclusive malaria parasite component that activates dendritic cells and triggers innate immune responses. Wu X, Gowda NM, Kumar S, Gowda DC, J Immunol 2010 184 4338 4348 10.4049/jimmunol.0903824 20231693
49. The nucleosome (Histone-DNA complex) is the TLR9-specific immunostimulatory component of Plasmodium falciparum that activates DCs. Gowda NM, Wu X, Gowda DC, PLoS One 2011 6 20398 10.1371/journal.pone.0020398 21687712
50. TLR9 and MyD88 are crucial for the development of protective immunity to malaria. Gowda NM, Wu X, Gowda DC, J Immunol 2012 188 5073 5085 10.4049/jimmunol.1102143 22516959
51. Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. Tiemi Shio M, Tiemi Shio M, Eisenbarth SC, Savaria M, Vinet AF, Bellemare M-J, Harder KW, Sutterwala FS, Bohle DS, Descoteaux A, Flavell RA, Olivier M, PLoS Pathog 2009 5 1000559 10.1371/journal.ppat.1000559 19696895
52. The interaction between DC and Plasmodium berghei/chabaudi-infected erythrocytes in mice involves direct cell-to-cell contact, internalization and TLR. Seixas E, Nunes J, Matos I, Coutinho A, Eur J Immunol 2009 39 1850 1863 10.1002/eji.200838403 19585512
53. CD36 and TLR interactions in inflammation and phagocytosis: implications for malaria. Erdman LK, Cosio G, Helmers AJ, Gowda DC, Grinstein S, Kain KC, J Immunol 2009 183 6452 6459 10.4049/jimmunol.0901374 19864601
54. Interferon-γ-central mediator of protective immune responses against the pre-erythrocytic and blood stage of malaria. McCall MBB, Sauerwein RW, J Leukoc Biol 2010 88 1131 1143 10.1189/jlb.0310137 20610802
55. Blocking IL-1 in systemic inflammation. Dinarello CA, J Exp Med 2005 201 1355 1359 10.1084/jem.20050640 15867089 (Pubitemid 40664079)