Complement receptor 1 and malaria

Cellular Microbiology

Volumn 13, Issue 10, 2011, Pages 1441-1450

  Stoute, José A ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT RECEPTOR;

ANEMIA; ANOPHELES; ANTIGEN ANTIBODY COMPLEX; BRAIN MALARIA; CAPILLARY; CELL SURFACE; COMPLEMENT ACTIVATION; DISEASE SEVERITY; ERYTHROCYTE; HOST PARASITE INTERACTION; IMMUNOSTIMULATION; LEUKOCYTE; MALARIA FALCIPARUM; NONHUMAN; PATHOGENESIS; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; REVIEW; ROSETTE FORMATION; SURFACE PROPERTY;

CELL ADHESION; ERYTHROCYTES; HOST-PATHOGEN INTERACTIONS; HUMANS; LEUKOCYTES; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; RECEPTORS, COMPLEMENT;

ANOPHELES (GENUS); PLASMODIUM FALCIPARUM;

EID: 80052798357     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2011.01648.x     Document Type: Review

References (94)

1. Al Yaman, F., Genton, B., Mokela, D., Raiko, A., Kati, S., Rogerson, S., etal. (1995) Human cerebral malaria: lack of significant association between erythrocyte rosetting and disease severity. Trans R Soc Trop Med Hyg 89: 55-58.
2. Ansar, W., Habib, S.K., Roy, S., Mandal, C., and Mandal, C. (2009) Unraveling the C-reactive protein complement-cascade in destruction of red blood cells: potential pathological implications in Plasmodium falciparum malaria. Cell Physiol Biochem 23: 175-190.
3. Awandare, G.A., Spadafora, C., Moch, J.K., Dutta, S., Haynes, J.D., and Stoute, J.A. (2011) Plasmodium falciparum field isolates use complement receptor 1 (CR1) as a receptor for invasion of erythrocytes. Mol Biochem Parasitol 117: 57-60.
4. Baum, J., Maier, A.G., Good, R.T., Simpson, K.M., and Cowman, A.F. (2005) Invasion by P. falciparum merozoites suggests a hierarchy of molecular interactions. PLoS Pathog 1: e37.
5. Bellamy, R., Kwiatkowski, D., and Hill, A.V. (1998) Absence of an association between intercellular adhesion molecule 1, complement receptor 1 and interleukin 1 receptor antagonist gene polymorphisms and severe malaria in a West African population. Trans R Soc Trop Med Hyg 92: 312-316.
6. Bickmore, W.A., Longbottom, D., Oghene, K., Fletcher, J.M., and Van Heyningen, V. (1993) Colocalization of the human CD59 gene to 11p13 with the MIC11 cell surface antigen. Genomics 17: 129-135.
7. Birmingham, D.J., Chen, W., Liang, G., Schmitt, H.C., Gavit, K., and Nagaraja, H.N. (2003) A CR1 polymorphism associated with constitutive erythrocyte CR1 levels affects binding to C4b but not C3b. Immunology 108: 531-538.
8. Birmingham, D.J., Irshaid, F., Gavit, K.F., Nagaraja, H.N., Yu, C.Y., Rovin, B.H., and Hebert, L.A. (2007) A polymorphism in the type one complement receptor (CR1) involves an additional cysteine within the C3b/C4b binding domain that inhibits ligand binding. Mol Immunol 44: 3510-3516.
9. Bratosin, D., Mazurier, J., Tissier, J.P., Estaquier, J., Huart, J.J., Ameisen, J.C., etal. (1998) Cellular and molecular mechanisms of senescent erythrocyte phagocytosis by macrophages. A review. Biochimie 80: 173-195.
10. Camacho, L.H., Gordeuk, V.R., Wilairatana, P., Pootrakul, P., Brittenham, G.M., and Looareesuwan, S. (1998) The course of anaemia after the treatment of acute, falciparum malaria. Ann Trop Med Parasitol 92: 525-537.
11. Carlson, J., Helmby, H., Hill, A.V., Brewster, D., Greenwood, B.M., and Wahlgren, M. (1990) Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet 336: 1457-1460.
12. Clark, I.A., and Alleva, L.M. (2009) Is human malarial coma caused, or merely deepened, by sequestration? Trends Parasitol 25: 314-318.
13. Cockburn, I.A., Mackinnon, M.J., O'Donnell, A., Allen, S.J., Moulds, J.M., Baisor, M., etal. (2004) A human complement receptor 1 polymorphism that reduces Plasmodium falciparum rosetting confers protection against severe malaria. Proc Natl Acad Sci USA 101: 272-277.
14. Davies, K.A., Hird, V., Stewart, S., Sivolapenko, G.B., Jose, P., Epenetos, A.A., and Walport, M.J. (1990) A study of in vivo immune complex formation and clearance in man. J Immunol 144: 4613-4620.
15. Deas, J.E., and Lee, L.T. (1981) Competitive inhibition by soluble erythrocyte glycoproteins of penetration by Plasmodium falciparum. Am J Trop Med Hyg 30: 1164-1167.
16. Dolan, S.A., Proctor, J.L., Alling, D.W., Okubo, Y., Wellems, T.E., and Miller, L.H. (1994) Glycophorin B as an EBA-175 independent Plasmodium falciparum receptor of human erythrocytes. Mol Biochem Parasitol 64: 55-63.
17. Dorovini-Zis, K., Schmidt, K., Huynh, H., Fu, W., Whitten, R.O., Milner, D., etal. (2011) The neuropathology of fatal cerebral malaria in malawian children. Am J Pathol 178: 2146-2158.
18. Doumbo, O.K., Thera, M.A., Kone, A.K., Raza, A., Tempest, L.J., Lyke, K.E., etal. (2009) High levels of Plasmodium falciparum rosetting in all clinical forms of severe malaria in African children. Am J Trop Med Hyg 81: 987-993.
19. Facer, C.A. (1980a) Direct antiglobulin reactions in Gambian children with P. falciparum malaria. III. Expression of IgG subclass determinants and genetic markers and association with anaemia. Clin Exp Immunol 41: 81-90.
20. Facer, C.A. (1980b) Direct Coombs antiglobulin reactions in Gambian children with Plasmodium falciparum malaria. II. Specificity of erythrocyte-bound IgG. Clin Exp Immunol 39: 279-288.
21. Facer, C.A., Bray, R.S., and Brown, J. (1979) Direct Coombs antiglobulin reactions in Gambian children with Plasmodium falciparum malaria. I. Incidence and class specificity. Clin Exp Immunol 35: 119-127.
22. Fearon, D.T. (1980) Identification of the membrane glycoprotein that is the C3b receptor of the human erythrocyte, polymorphonuclear leukocyte, B lymphocyte, and monocyte. J Exp Med 152: 20-30.
23. Fearon, D.T. (1985) Human complement receptors for C3b (CR1) and C3d (CR2). J Invest Dermatol 85: 53s-57s.
24. Friedman, M.J., Blankenberg, T., Sensabaugh, G., and Tenforde, T.S. (1984) Recognition and invasion of human erythrocytes by malarial parasites: contribution of sialoglycoproteins to attachment and host specificity. J Cell Biol 98: 1672-1677.
25. Gaur, D., Furuya, T., Mu, J., Jiang, L.B., Su, X.Z., and Miller, L.H. (2006) Upregulation of expression of the reticulocyte homology gene 4 in the Plasmodium falciparum clone Dd2 is associated with a switch in the erythrocyte invasion pathway. Mol Biochem Parasitol 145: 205-215.
26. Gelfand, M.C., Frank, M.M., and Green, I. (1975) A receptor for the third component of complement in the human renal glomerulus. J Exp Med 142: 1029-1034.
27. Ghiran, I., Barbashov, S.F., Klickstein, L.B., Tas, S.W., Jensenius, J.C., and Nicholson-Weller, A. (2000) Complement receptor 1/CD35 is a receptor for mannan-binding lectin. J Exp Med 192: 1797-1808.
28. Goka, B.Q., Kwarko, H., Kurtzhals, J.A., Gyan, B., Ofori-Adjei, E., Ohene, S.A., etal. (2001) Complement binding to erythrocytes is associated with macrophage activation and reduced haemoglobin in Plasmodium falciparum malaria. Trans R Soc Trop Med Hyg 95: 545-549.
29. Gros, P., Milder, F.J., and Janssen, B.J. (2008) Complement driven by conformational changes. Nat Rev Immunol 8: 48-58.
30. Hadley, T.J., Klotz, F.W., Pasvol, G., Haynes, J.D., McGinniss, M.H., Okubo, Y., and Miller, L.H. (1987) Falciparum malaria parasites invade erythrocytes that lack glycophorin A and B (MkMk). Strain differences indicate receptor heterogeneity and two pathways for invasion. J Clin Invest 80: 1190-1193.
31. Helegbe, G.K., Goka, B.Q., Kurtzhals, J.A., Addae, M.M., Ollaga, E., Tetteh, J.K., etal. (2007) Complement activation in Ghanaian children with severe Plasmodium falciparum malaria. Malar J 6: 165.
32. Herrera, A.H., Xiang, L., Martin, S.G., Lewis, J., and Wilson, J.G. (1998) Analysis of complement receptor type 1 (CR1) expression on erythrocytes and of CR1 allelic markers in Caucasian and African American populations. Clin Immunol Immunopathol 87: 176-183.
33. Holers, V.M., Chaplin, D.D., Leykam, J.F., Gruner, B.A., Kumar, V., and Atkinson, J.P. (1987) Human complement C3b/C4b receptor (CR1) mRNA polymorphism that correlates with the CR1 allelic molecular weight polymorphism. Proc Natl Acad Sci USA 84: 2459-2463.
34. Iida, K., and Nussenzweig, V. (1981) Complement receptor is an inhibitor of the complement cascade. J Exp Med 153: 1138-1150.
35. Jakeman, G.N., Saul, A., Hogarth, W.L., and Collins, W.E. (1999) Anaemia of acute malaria infections in non-immune patients primarily results from destruction of uninfected erythrocytes. Parasitology 119: 127-133.
36. Jhaveri, K.N., Ghosh, K., Mohanty, D., Parmar, B.D., Surati, R.R., Camoens, H.M., etal. (1997) Autoantibodies, immunoglobulins, complement and circulating immune complexes in acute malaria. Natl Med J India 10: 5-7.
37. Klickstein, L.B., Barbashov, S.F., Liu, T., Jack, R.M., and Nicholson-Weller, A. (1997) Complement receptor type 1 (CR1, CD35) is a receptor for C1q. Immunity 7: 345-355.
38. Krych-Goldberg, M., and Atkinson, J.P. (2001) Structure-function relationships of complement receptor type 1. Immunol Rev 180: 112-122.
39. Lin, E., Tavul, L., Michon, P., Richards, J.S., Dabod, E., Beeson, J.G., etal. (2010) Minimal association of common red blood cell polymorphisms with Plasmodium falciparum infection and uncomplicated malaria in Papua New Guinean school children. Am J Trop Med Hyg 83: 828-833.
40. Lutz, H.U., Stammler, P., and Fasler, S. (1990) How naturally occurring anti-band 3 antibodies stimulate C3b deposition to senescent and oxidatively stressed red blood cells. Biomed Biochim Acta 49: S224-S229.
41. Luxemburger, C., Ricci, F., Nosten, F., Raimond, D., Bathet, S., and White, N.J. (1997) The epidemiology of severe malaria in an area of low transmission in Thailand. Trans R Soc Trop Med Hyg 91: 256-262.
42. Marsh, K., and Snow, R.W. (1999) Malaria transmission and morbidity. Parassitologia 41: 241-246.
43. Medof, M.E., and Nussenzweig, V. (1984) Control of the function of substrate-bound C4b-C3b by the complement receptor Cr1. J Exp Med 159: 1669-1685.
44. Medof, M.E., Iida, K., Mold, C., and Nussenzweig, V. (1982) Unique role of the complement receptor CR1 in the degradation of C3b associated with immune complexes. J Exp Med 156: 1739-1754.
45. Mibei, E.K., Orago, A.S., and Stoute, J.A. (2005) Immune complex levels in children with severe Plasmodium falciparum malaria. Am J Trop Med Hyg 72: 593-599.
46. Mibei, E.K., Otieno, W.O., Orago, A.S., and Stoute, J.A. (2008) Distinct pattern of class and subclass antibodies in immune complexes of children with cerebral malaria and severe malarial anaemia. Parasite Immunol 31: 61-63.
47. Mitchell, G.H., Hadley, T.J., McGinniss, M.H., Klotz, F.W., and Miller, L.H. (1986) Invasion of erythrocytes by Plasmodium falciparum malaria parasites: evidence for receptor heterogeneity and two receptors. Blood 67: 1519-1521.
48. Moulds, J.M. (2005) KAM: A new allele in the Knops blood group system. Transfusion 45: ii-226A.
49. Moulds, J.M., Nickells, M.W., Moulds, J.J., Brown, M.C., and Atkinson, J.P. (1991) The C3b/C4b receptor is recognized by the Knops, McCoy, Swain-langley, and York blood group antisera. J Exp Med 173: 1159-1163.
50. Moulds, J.M., Brai, M., Cohen, J., Cortelazzo, A., Cuccia, M., Lin, M., etal. (1998) Reference typing report for complement receptor 1 (CR1). Exp Clin Immunogenet 15: 291-294.
51. Moulds, J.M., Kassambara, L., Middleton, J.J., Baby, M., Sagara, I., Guindo, A., etal. (2000) Identification of complement receptor one (CR1) polymorphisms in west Africa. Genes Immun 1: 325-329.
52. Moulds, J.M., Zimmerman, P.A., Doumbo, O.K., Kassambara, L., Sagara, I., Diallo, D.A., etal. (2001) Molecular identification of Knops blood group polymorphisms found in long homologous region D of complement receptor 1. Blood 97: 2879-2885.
53. Moulds, J.M., Zimmerman, P.A., Doumbo, O.K., Diallo, D.A., Atkinson, J.P., Krych-Goldberg, M., etal. (2002) Expansion of the Knops blood group system and subdivision of Sl(a). Transfusion 42: 251-256.
54. Moulds, J.M., Thomas, B.J., Doumbo, O., Diallo, D.A., Lyke, K.E., Plowe, C.V., etal. (2004) Identification of the Kna/Knb polymorphism and a method for Knops genotyping. Transfusion 44: 164-169.
55. Nagayasu, E., Ito, M., Akaki, M., Nakano, Y., Kimura, M., Looareesuwan, S., and Aikawa, M. (2001) CR1 density polymorphism on erythrocytes of falciparum malaria patients in Thailand. Am J Trop Med Hyg 64: 1-5.
56. Nickells, M.W., Seya, T., Holers, V.M., and Atkinson, J.P. (1986) Analysis of C3b/C4b receptor (CR1) polymorphic variants by tryptic peptide mapping. Mol Immunol 23: 661-668.
57. Odhiambo, C.O., Otieno, W., Adhiambo, C., Odera, M.M., and Stoute, J.A. (2008) 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 6: 23.
58. Owuor, B.O., Odhiambo, C.O., Otieno, W.O., Adhiambo, C., Makawiti, D.W., and Stoute, J.A. (2007) Reduced immune complex binding capacity and increased complement susceptibility of red cells from children with severe malaria-associated anemia. Mol Med 14: 89-97.
59. Pasvol, G., and Jungery, M. (1983) Glycophorins and red cell invasion by Plasmodium falciparum. Ciba Found Symp 94: 174-195.
60. Perkins, M.E. (1984) Binding of glycophorins to Plasmodium falciparum merozoites. Mol Biochem Parasitol 10: 67-78.
61. Persson, K.E., McCallum, F.J., Reiling, L., Lister, N.A., Stubbs, J., Cowman, A.F., etal. (2008) Variation in use of erythrocyte invasion pathways by Plasmodium falciparum mediates evasion of human inhibitory antibodies. J Clin Invest 118: 342-351.
62. Price, R.N., Simpson, J.A., Nosten, F., Luxemburger, C., Hkirjaroen, L., ter Kuile, F., etal. (2001) Factors contributing to anemia after uncomplicated falciparum malaria. Am J Trop Med Hyg 65: 614-622.
63. Rao, N., Ferguson, D.J., Lee, S.F., and Telen, M.J. (1991) Identification of human erythrocyte blood group antigens on the C3b/C4b receptor. J Immunol 146: 3502-3507.
64. Reinagel, M.L., Gezen, M., Ferguson, P.J., Kuhn, S., Martin, E.N., and Taylor, R.P. (1997) The primate erythrocyte complement receptor (CR1) as a privileged site: binding of immunoglobulin G to erythrocyte CR1 does not target erythrocytes for phagocytosis. Blood 89: 1068-1077.
65. Rey-Campos, J., Rubinstein, P., and Rodriguez de Cordoba, S. (1988) A physical map of the human regulator of complement activation gene cluster linking the complement genes CR1, CR2, DAF, and C4 BP. J Exp Med 167: 664-669.
66. Rout, R., Dhangadamajhi, G., Mohapatra, B.N., Kar, S.K., and Ranjit, M. (2011) High CR1 level and related polymorphic variants are associated with cerebral malaria in eastern-India. Infect Genet Evol 11: 139-144.
67. Rowe, A., Obeiro, J., Newbold, C.I., and Marsh, K. (1995) Plasmodium falciparum rosetting is associated with malaria severity in Kenya. Infect Immun 63: 2323-2326.
68. Rowe, J.A., Moulds, J.M., Newbold, C.I., and Miller, L.H. (1997) P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature 388: 292-295.
69. Rowe, J.A., Raza, A., Diallo, D.A., Baby, M., Poudiougo, B., Coulibaly, D., etal. (2002) Erythrocyte CR1 expression level does not correlate with a HindIII restriction fragment length polymorphism in Africans: implications for studies on malaria susceptibility. Genes Immun 3: 497-500.
70. Sherwood, T.A., and Virella, G. (1986) The binding of immune complexes to human red cells: complement requirements and fate of the RBC-bound IC after interaction with human phagocytic cells. Clin Exp Immunol 64: 195-204.
71. Sinha, S., Jha, G.N., Anand, P., Qidwai, T., Pati, S.S., Mohanty, S., etal. (2009) CR1 levels and gene polymorphisms exhibit differential association with falciparum malaria in regions of varying disease endemicity. Hum Immunol 70: 244-250.
72. Snow, R.W., Omumbo, J.A., Lowe, B., Molyneux, C.S., Obiero, J.O., Palmer, A., etal. (1997) Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet 349: 1650-1654.
73. Soares, S.C., be-Sandes, K., Nascimento Filho, V., Nunes, F.M., and Silva, W.A., Jr. (2008) Genetic polymorphisms in TLR4, CR1 and Duffy genes are not associated with malaria resistance in patients from Baixo Amazonas region, Brazil. Genet Mol Res 7: 1011-1019.
74. Spadafora, C., Awandare, G.A., Kopydlowski, K.M., Czege, J., Moch, J.K., Finberg, R.W., etal. (2010) Complement receptor 1 is a sialic acid-independent erythrocyte receptor of Plasmodium falciparum. PLoS Pathog 6: e1000968.
75. Stoute, J.A. (2005) Complement-regulatory proteins in severe malaria: too little or too much of a good thing? Trends Parasitol 21: 218-223.
76. Stoute, J.A., Odindo, A.O., Owuor, B.O., Mibei, E.K., Opollo, M.O., and Waitumbi, J.N. (2003) Loss of red blood cell-complement regulatory proteins and increased levels of circulating immune complexes are associated with severe malarial anemia. J Infect Dis 187: 522-525.
77. Stubbs, J., Simpson, K.M., Triglia, T., Plouffe, D., Tonkin, C.J., Duraisingh, M.T., etal. (2005) Molecular mechanism for switching of P. falciparum invasion pathways into human erythrocytes. Science 309: 1384-1387.
78. Taylor, R.P., Ferguson, P.J., Martin, E.N., Cooke, J., Greene, K.L., Grinspun, K., etal. (1997) Immune complexes bound to the primate erythrocyte complement receptor (CR1) via anti-CR1 mAbs are cleared simultaneously with loss of CR1 in a concerted reaction in a rhesus monkey model. Clin Immunol Immunopathol 82: 49-59.
79. Teeranaipong, P., Ohashi, J., Patarapotikul, J., Kimura, R., Nuchnoi, P., Hananantachai, H., etal. (2008) A functional single-nucleotide polymorphism in the CR1 promoter region contributes to protection against cerebral malaria. J Infect Dis 198: 1880-1891.
80. Tham, W.H., Wilson, D.W., Reiling, L., Chen, L., Beeson, J.G., and Cowman, A.F. (2009) Antibodies to reticulocyte binding like homologue 4 inhibit invasion of P. falciparum into human erythrocytes. Infect Immun 77: 2427-2435.
81. Tham, W.H., Wilson, D.W., Lopaticki, S., Schmidt, C.Q., Tetteh-Quarcoo, P.B., Barlow, P.N., etal. (2010) Complement receptor 1 is the host erythrocyte receptor for Plasmodium falciparum PfRh4 invasion ligand. Proc Natl Acad Sci USA 107: 17327-17332.
82. Tham, W.H., Schmidt, C.Q., Hauhart, R.E., Guariento, M., Tetteh-Quarcoo, P.B., Lopaticki, S., etal. (2011) Plasmodium falciparum uses a key functional site in complement receptor type-1 for invasion of human erythrocytes. Blood (in press).
83. Thathy, V., Moulds, J.M., Guyah, B., Otieno, W., and Stoute, J.A. (2005) Complement receptor 1 polymorphisms associated with resistance to severe malaria in Kenya. Malar J 4: 54.
84. Thomas, B.N., Donvito, B., Cockburn, I., Fandeur, T., Rowe, J.A., Cohen, J.H., and Moulds, J.M. (2005) A complement receptor-1 polymorphism with high frequency in malaria endemic regions of Asia but not Africa. Genes Immun 6: 31-36.
85. Veldhuisen, B., Ligthart, P.C., Vidarsson, G., Roels, I., Folman, C.C., van der Schoot, C.E., and Haas, M. (2011) Molecular analysis of the York antigen of the Knops blood group system. Transfusion 51: 1389-1396.
86. Vik, D.P., and Wong, W.W. (1993) Structure of the gene for the F allele of complement receptor type 1 and sequence of the coding region unique to the S allele. J Immunol 151: 6214-6224.
87. Waitumbi, J.N., Opollo, M.O., Muga, R.O., Misore, A.O., and Stoute, J.A. (2000) Red cell surface changes and erythrophagocytosis in children with severe Plasmodium falciparum anemia. Blood 95: 1481-1486.
88. Waitumbi, J.N., Donvito, B., Kisserli, A., Cohen, J.H., and Stoute, J.A. (2004) Age-related changes in red blood cell complement regulatory proteins and susceptibility to severe malaria. J Infect Dis 190: 1183-1191.
89. Wilson, J.G., Wong, W.W., Schur, P.H., and Fearon, D.T. (1982) Mode of inheritance of decreased C3b receptors on erythrocytes of patients with systemic lupus erythematosus. N Engl J Med 307: 981-986.
90. Wilson, J.G., Murphy, E.E., Wong, W.W., Klickstein, L.B., Weis, J.H., and Fearon, D.T. (1986) Identification of a restriction fragment length polymorphism by a CR1 cDNA that correlates with the number of CR1 on erythrocytes. J Exp Med 164: 50-59.
91. Wong, W.W., Cahill, J.M., Rosen, M.D., Kennedy, C.A., Bonaccio, E.T., Morris, M.J., etal. (1989) Structure of the human CR1 gene. Molecular basis of the structural and quantitative polymorphisms and identification of a new CR1-like allele. J Exp Med 169: 847-863.
92. Xiang, L., Rundles, J.R., Hamilton, D.R., and Wilson, J.G. (1999) Quantitative alleles of CR1: coding sequence analysis and comparison of haplotypes in two ethnic groups. J Immunol 163: 4939-4945.
93. Zimmerman, P.A., Fitness, J., Moulds, J.M., McNamara, D.T., Kasehagen, L.J., Rowe, J.A., and Hill, A.V. (2003) CR1 Knops blood group alleles are not associated with severe malaria in the Gambia. Genes Immun 4: 368-373.
94. Zipfel, P.F., and Skerka, C. (2009) Complement regulators and inhibitory proteins. Nat Rev Immunol 9: 729-740.