Complement activation in malaria: Friend or foe?

Trends in Molecular Medicine

Volumn 20, Issue 5, 2014, Pages 293-301

  Biryukov, Sergei ^a   Stoute, José A ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Cerebral malaria; Complement; Malaria; Placental malaria; Plasmodium falciparum; Severe malarial anemia

Indexed keywords

CELL SURFACE PROTEIN; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C3B; COMPLEMENT COMPONENT C4A; COMPLEMENT COMPONENT C5A; COMPLEMENT INHIBITOR; COMPLEMENT MEMBRANE ATTACK COMPLEX; ECULIZUMAB; MANNOSE BINDING LECTIN; COMPLEMENT;

ANOPHELES; BRAIN MALARIA; COMPLEMENT ACTIVATION; HEMOLYSIS; HUMAN; INFLAMMATION; INNATE IMMUNITY; MALARIA; MALARIA FALCIPARUM; MATERNAL MORTALITY; NONHUMAN; PATHOGENESIS; PLACENTA MALARIA; PLASMODIUM FALCIPARUM; PLASMODIUM KNOWLESI; PLASMODIUM MALARIAE; PLASMODIUM OVALE; PLASMODIUM VIVAX; REVIEW; ANIMAL; IMMUNOLOGY;

ANIMALS; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; HUMANS; MALARIA;

EID: 84899623435     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2014.01.001     Document Type: Review

References (84)

1. Murray C.J., et al. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 2012, 379:413-431.
2. Pierce S.K., Miller L.H. World Malaria Day 2009: what malaria knows about the immune system that immunologists still do not. J. Immunol. 2009, 182:5171-5177.
3. Silver K.L., et al. Complement driven innate immune response to malaria: fuelling severe malarial diseases. Cell. Microbiol. 2010, 12:1036-1045.
4. Ricklin D., et al. Complement: a key system for immune surveillance and homeostasis. Nat. Immunol. 2010, 11:785-797.
5. Neva F.A., et al. Relationship of serum complement levels to events of the malarial paroxysm. J. Clin. Invest. 1974, 54:451-460.
6. Dulaney A.D. Complement activity of human serum with especial reference to malaria. Fed. Proc. 1947, 6:425.
7. Ade-Serrano M.A., et al. Correlation of Plasmodium falciparum gametocytemia with complement component titers in rural Nigerian school children. J. Clin. Microbiol. 1981, 13:195-198.
8. Srichaikul T., et al. Complement changes and disseminated intravascular coagulation in Plasmodium falciparum malaria. Lancet 1975, 1:770-772.
9. Greenwood B.M., Brueton M.J. Complement activation in children with acute malaria. Clin. Exp. Immunol. 1974, 18:267-272.
10. Phanuphak P., et al. Complement changes in Falciparum malaria infection. Clin. Exp. Immunol. 1985, 59:571-576.
11. Glew R.H., et al. Serum complement and immunity in experimental simian malaria. I. Cyclical alterations in C4 related to schizont rupture. J. Infect. Dis. 1975, 131:17-25.
12. Roestenberg M., et al. Complement activation in experimental human malaria infection. Trans. R. Soc. Trop. Med. Hyg. 2007, 101:643-649.
13. Dasari P., et al. Digestive vacuole of Plasmodium falciparum released during erythrocyte rupture dually activates complement and coagulation. Blood 2012, 119:4301-4310.
14. Dasari P., et al. Digestive vacuoles of Plasmodium falciparum are selectively phagocytosed by and impair killing function of polymorphonuclear leukocytes. Blood 2011, 118:4946-4956.
15. Hill D.L., et al. Opsonising antibodies to P. falciparum merozoites associated with immunity to clinical malaria. PLoS ONE 2013, 8:e74627.
16. Stoute J.A., et al. Loss of red blood cell-complement regulatory proteins and increased levels of circulating immune complexes are associated with severe malarial anemia. J. Infect. Dis. 2003, 187:522-525.
17. Jhaveri K.N., et al. Autoantibodies, immunoglobulins, complement and circulating immune complexes in acute malaria. Natl. Med. J. India 1997, 10:5-7.
18. Adam C., et al. Cryoglobulins, circulating immune complexes, and complement activation in cerebral malaria. Infect. Immun. 1981, 31:530-535.
19. Klabunde J., et al. Recognition of Plasmodium falciparum proteins by mannan-binding lectin, a component of the human innate immune system. Parasitol. Res. 2002, 88:113-117.
20. Garred P., et al. Mannose-binding lectin is a disease modifier in clinical malaria and may function as opsonin for Plasmodium falciparum-infected erythrocytes. Infect. Immun. 2003, 71:5245-5253.
21. Lipscombe R.J., et al. Distinct physicochemical characteristics of human mannose binding protein expressed by individuals of differing genotype. Immunology 1995, 85:660-667.
22. Lipscombe R.J., et al. High frequencies in African and non-African populations of independent mutations in the mannose binding protein gene. Hum. Mol. Genet. 1992, 1:709-715.
23. Madsen H.O., et al. Different molecular events result in low protein levels of mannan-binding lectin in populations from southeast Africa and South America. J. Immunol. 1998, 161:3169-3175.
24. Holmberg V., et al. Mutations of complement lectin pathway genes MBL2 and MASP2 associated with placental malaria. Malar. J. 2012, 11:61.
25. Holmberg V., et al. Mannose-binding lectin variant associated with severe malaria in young African children. Microbes Infect. 2008, 10:342-348.
26. Boldt A.B., et al. Haplotype specific-sequencing reveals MBL2 association with asymptomatic Plasmodium falciparum infection. Malar. J. 2009, 8:97.
27. Luty A.J., et al. Mannose-binding lectin plasma levels and gene polymorphisms in Plasmodium falciparum malaria. J. Infect. Dis. 1998, 178:1221-1224.
28. Thevenon A.D., et al. Genetic polymorphisms of mannose-binding lectin do not influence placental malaria but are associated with preterm deliveries. Infect. Immun. 2009, 77:1483-1491.
29. Mombo L.E., et al. Human genetic polymorphisms and asymptomatic Plasmodium falciparum malaria in Gabonese schoolchildren. Am. J. Trop. Med. Hyg. 2003, 68:186-190.
30. Atkinson J.P., et al. Serum complement and immunity in experimental simian malaria. II. Preferential activation of early components and failure of depletion of late components to inhibit protective immunity. J. Infect. Dis. 1975, 131:26-33.
31. Ramos T.N., et al. The C5 convertase is not required for activation of the terminal complement pathway in murine experimental cerebral malaria. J. Biol. Chem. 2012, 287:24734-24738.
32. Taylor P.R., et al. Complement contributes to protective immunity against reinfection by Plasmodium chabaudi chabaudi parasites. Infect. Immun. 2001, 69:3853-3859.
33. Ward P.A., et al. Complement does not facilitate plasmodial infections. J. Immunol. 1981, 126:1826-1828.
34. Ramos T.N., et al. Deletion of the complement phagocytic receptors CR3 and CR4 does not alter susceptibility to experimental cerebral malaria. Parasite Immunol. 2012, 34:547-550.
35. Shikani H.J., et al. Cerebral malaria: we have come a long way. Am. J. Pathol. 2012, 181:1484-1492.
36. Idro R., et al. Cerebral malaria: mechanisms of brain injury and strategies for improved neurocognitive outcome. Pediatr. Res. 2010, 68:267-274.
37. Dorovini-Zis K., et al. The neuropathology of fatal cerebral malaria in Malawian children. Am. J. Pathol. 2011, 178:2146-2158.
38. Vannaphan S., et al. The epidemiology of patients with severe malaria who died at the Hospital for Tropical Diseases, 1991-2004. Southeast Asian J. Trop. Med. Public Health 2005, 36:385-389.
39. Lackner P., et al. Complement factors C1q, C3 and C5 in brain and serum of mice with cerebral malaria. Malar. J. 2008, 7:207.
40. Patel S.N., et al. C5 deficiency and C5a or C5aR blockade protects against cerebral malaria. J. Exp. Med. 2008, 205:1133-1143.
41. Kim H., et al. Functional roles for C5a and C5aR but not C5L2 in the pathogenesis of human and experimental cerebral malaria. Infect. Immun. 2014, 82:371-379.
42. Ramos T.N., et al. Cutting edge: the membrane attack complex of complement is required for the development of murine experimental cerebral malaria. J. Immunol. 2011, 186:6657-6660.
43. Huber-Lang M., et al. Generation of C5a in the absence of C3: a new complement activation pathway. Nat. Med. 2006, 12:682-687.
44. Huber-Lang M., et al. Generation of C5a by phagocytic cells. Am. J. Pathol. 2002, 161:1849-1859.
45. Hunt N.H., et al. Immunopathogenesis of cerebral malaria. Int. J. Parasitol. 2006, 36:569-582.
46. Kilgore K.S., et al. Enhancement by the complement membrane attack complex of tumor necrosis factor-alpha-induced endothelial cell expression of E-selectin and ICAM-1. J. Immunol. 1995, 155:1434-1441.
47. Turner G.D., et al. An immunohistochemical study of the pathology of fatal malaria. Evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration. Am. J. Pathol. 1994, 145:1057-1069.
48. Duffy P.E. Plasmodium in the placenta: parasites, parity, protection, prevention and possibly preeclampsia. Parasitology 2007, 134:1877-1881.
49. Beeson J.G., Duffy P.E. The immunology and pathogenesis of malaria during pregnancy. Curr. Top. Microbiol. Immunol. 2005, 297:187-227.
50. Galbraith R.M., et al. The human materno-foetal relationship in malaria. II. Histological, ultrastructural and immunopathological studies of the placenta. Trans. R. Soc. Trop. Med. Hyg. 1980, 74:61-72.
51. Yamada M., et al. Plasmodium falciparum associated placental pathology: a light and electron microscopic and immunohistologic study. Am. J. Trop. Med. Hyg. 1989, 41:161-168.
52. Muehlenbachs A., et al. Genome-wide expression analysis of placental malaria reveals features of lymphoid neogenesis during chronic infection. J. Immunol. 2007, 179:557-565.
53. Puga I., Cerutti A. Protection by natural IgG: a sweet partnership with soluble lectins does the trick!. EMBO J. 2013, 32:2897-2899.
54. Shiratsuchi A., et al. Bridging effect of recombinant human mannose-binding lectin in macrophage phagocytosis of Escherichia coli. Immunology 2008, 124:575-583.
55. Girardi G., et al. Complement activation induces dysregulation of angiogenic factors and causes fetal rejection and growth restriction. J. Exp. Med. 2006, 203:2165-2175.
56. Conroy A.L., et al. Complement activation and the resulting placental vascular insufficiency drives fetal growth restriction associated with placental malaria. Cell Host Microbe 2013, 13:215-226.
57. Muehlenbachs A., et al. Hypertension and maternal-fetal conflict during placental malaria. PLoS Med. 2006, 3:e446.
58. Muehlenbachs A., et al. Natural selection of FLT1 alleles and their association with malaria resistance in utero. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:14488-14491.
59. Conroy A., et al. C5a enhances dysregulated inflammatory and angiogenic responses to malaria in vitro: potential implications for placental malaria. PLoS ONE 2009, 4:e4953.
60. Khattab A., et al. Complement activation in primiparous women from a malaria endemic area is associated with reduced birthweight. Placenta 2013, 34:162-167.
61. Conroy A.L., et al. Complement activation: a critical mediator of adverse fetal outcomes in placental malaria?. Trends Parasitol. 2011, 27:294-299.
62. Reyburn H., et al. Association of transmission intensity and age with clinical manifestations and case fatality of severe Plasmodium falciparum malaria. JAMA 2005, 293:1461-1470.
63. Anonymous Severe falciparum malaria. World Health Organization, Communicable Diseases Cluster. Trans. R. Soc. Trop. Med. Hyg. 2000, 94(Suppl. 1):S1-S90.
64. Looareesuwan S., et al. Reduced erythrocyte survival following clearance of malarial parasitaemia in Thai patients. Br. J. Haematol. 1987, 67:473-478.
65. Jakeman G.N., et al. Anaemia of acute malaria infections in non-immune patients primarily results from destruction of uninfected erythrocytes. Parasitology 1999, 119:127-133.
66. Price R.N., et al. Factors contributing to anemia after uncomplicated falciparum malaria. Am. J. Trop. Med. Hyg. 2001, 65:614-622.
67. Nyakoe N.K., et al. Complement consumption in children with Plasmodium falciparum malaria. Malar. J. 2009, 8:7.
68. Pawluczkowycz A.W., et al. Hematin promotes complement alternative pathway-mediated deposition of C3 activation fragments on human erythrocytes: potential implications for the pathogenesis of anemia in malaria. J. Immunol. 2007, 179:5543-5552.
69. Boldt A.B., et al. Association of a new mannose-binding lectin variant with severe malaria in Gabonese children. Genes Immun. 2006, 7:393-400.
70. Waitumbi J.N., et al. Red cell surface changes and erythrophagocytosis in children with severe Plasmodium falciparum anemia. Blood 2000, 95:1481-1486.
71. Owuor B.O., et al. Reduced immune complex binding capacity and increased complement susceptibility of red cells from children with severe malaria-associated anemia. Mol. Med. 2008, 14:89-97.
72. Odhiambo C.O., et al. Increased deposition of C3b on red cells with low CR1 and CD55 in a malaria-endemic region of western Kenya: implications for the development of severe anemia. BMC Med. 2008, 6:23.
73. Gwamaka M., et al. Early and extensive CD55 loss from red blood cells supports a causal role in malarial anaemia. Malar. J. 2011, 10:386.
74. Mahajan R.C., et al. Anaemia and expression levels of CD35, CD55 and CD59 on red blood cells in Plasmodium falciparum malaria patients from India. Indian J. Med. Res. 2011, 133:662-664.
75. Thomas B.N., et al. Circulating immune complex levels are associated with disease severity and seasonality in children with malaria from Mali. Biomark. Insights 2012, 7:81-86.
76. Fernandez-Arias C., et al. Malaria inhibits surface expression of complement receptor 1 in monocytes/macrophages, causing decreased immune complex internalization. J. Immunol. 2013, 190:3363-3372.
77. Helegbe G.K., et al. Complement activation in Ghanaian children with severe Plasmodium falciparum malaria. Malar. J. 2007, 6:165.
78. Waitumbi J.N., et al. Age-related changes in red blood cell complement regulatory proteins and susceptibility to severe malaria. J. Infect. Dis. 2004, 190:1183-1191.
79. Evans K.J., et al. Severe malarial anemia of low parasite burden in rodent models results from accelerated clearance of uninfected erythrocytes. Blood 2006, 107:1192-1199.
80. Harris J.V., et al. Sequential Plasmodium chabaudi and Plasmodium berghei infections provide a novel model of severe malarial anemia. Infect. Immun. 2012, 80:2997-3007.
81. Pappas M.G., et al. Complement-mediated defect in clearance and sequestration of sensitized, autologous erythrocytes in rodent malaria. J. Clin. Invest. 1981, 67:183-192.
82. Reinagel M.L., et al. The primate erythrocyte complement receptor (CR1) as a privileged site: binding of immunoglobulin G to erythrocyte CR1 does not target erythrocytes for phagocytosis. Blood 1997, 89:1068-1077.
83. Qu H., et al. Novel analogues of the therapeutic complement inhibitor compstatin with significantly improved affinity and potency. Mol. Immunol. 2011, 48:481-489.
84. Hillmen P., et al. Effect of eculizumab on hemolysis and transfusion requirements in patients with paroxysmal nocturnal hemoglobinuria. N. Engl. J. Med. 2004, 350:552-559.