Plasmodium falciparum malaria and the immunogenetics of ABO, HLA, and CD36 (platelet glycoprotein IV)

Vox Sanguinis

Volumn 100, Issue 1, 2011, Pages 99-111

  Cserti Gazdewich, C M ^a   Mayr, W R ^b   Dzik, W H ^c  

^a TORONTO GENERAL HOSPITAL   (Canada)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

ABO; Blood group; CD36; Human leukocyte antigen; Malaria; Plasmodium falciparum; Platelet glycoprotein IV

Indexed keywords

CD36 ANTIGEN; HLA ANTIGEN; HLA DR ANTIGEN;

ANTIGEN EXPRESSION; BLOOD GROUP ABO SYSTEM; BRAIN MALARIA; CELL ADHESION; GENE DOSAGE; GENE MUTATION; GENETIC POLYMORPHISM; GENOTYPE PHENOTYPE CORRELATION; HUMAN; IMMUNOGENETICS; LETHALITY; MALARIA FALCIPARUM; PLASMODIUM FALCIPARUM; PREVALENCE; PRIORITY JOURNAL; REVIEW; SURVIVAL RATE; THROMBOCYTE; TISSUE SPECIFICITY; VASCULAR ENDOTHELIUM; ZYGOSITY;

ABO BLOOD-GROUP SYSTEM; ANIMALS; ANTIGENS, CD36; BIOLOGICAL EVOLUTION; GENETIC PREDISPOSITION TO DISEASE; HLA ANTIGENS; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNOGENETIC PHENOMENA; MALARIA, FALCIPARUM; MODELS, GENETIC; MUTATION; PLASMODIUM FALCIPARUM;

EID: 78650335593     PISSN: 00429007     EISSN: 14230410     Source Type: Journal    
DOI: 10.1111/j.1423-0410.2010.01429.x     Document Type: Review

References (117)

1. Weatherall DJ: Genetic variation and susceptibility to infection: the red cell and malaria. Br J Haematol 2008; 141:276-286
2. Carvalho BO, Lopes SC, Nogueira PA, et al. On the cytoadhesion of Plasmodium vivax-infected erythrocytes. J Infect Dis 2010; 202:639-647
3. Hasler T, Handunnetti SM, Aguiar JC, et al. In vitro rosetting, cytoadherence, and microagglutination properties of Plasmodium falciparum-infected erythrocytes from Gambian and Tanzanian patients. Blood 1990; 76:1845-1852
4. Ho M, White NJ: Molecular mechanisms of cytoadherence in malaria. Am J Physiol 1999; 276:C1231-C1242
5. Yipp BG, Anand S, Schollaardt T, et al. Synergism of multiple adhesion molecules in mediating cytoadherence of Plasmodium falciparum-infected erythrocytes to microvascular endothelial cells under flow. Blood 2000; 96:2292-2298
6. Rowe JA, Claessens A, Corrigan RA, et al. Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications. Expert Rev Mol Med 2009; 11:e16
7. Gruenberg J, Allred DR, Sherman IW: Scanning electron microscope-analysis of the protrusions (knobs) present on the surface of Plasmodium falciparum-infected erythrocytes. J Cell Biol 1983; 97:795-802
8. Maier AG, Cooke BM, Cowman AF, et al. Malaria parasite proteins that remodel the host erythrocyte. Nat Rev Microbiol 2009; 7:341-354
9. Nagao E, Kaneko O, Dvorak JA: Plasmodium falciparum-infected erythrocytes: qualitative and quantitative analyses of parasite-induced knobs by atomic force microscopy. J Struct Biol 2000; 130:34-44
10. Smith JD, Subramanian G, Gamain B, et al. Classification of adhesive domains in the Plasmodium falciparum erythrocyte membrane protein 1 family. Mol Biochem Parasitol 2000; 110:293-310
11. Carlson J, Wahlgren M: Plasmodium falciparum erythrocyte rosetting is mediated by promiscuous lectin-like interactions. J Exp Med 1992; 176:1311-1317
12. Rowe JA, Handel IG, Thera MA, et al. Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting. Proc Natl Acad Sci U S A 2007; 104:17471-17476
13. Heddini A, Pettersson F, Kai O, et al. Fresh isolates from children with severe Plasmodium falciparum malaria bind to multiple receptors. Infect Immun 2001; 69:5849-5856
14. Barragan A, Kremsner PG, Wahlgren M, et al. Blood group A antigen is a coreceptor in Plasmodium falciparum rosetting. Infect Immun 2000; 68:2971-2975
15. Athreya BH, Coriell LL: Relation of blood groups to infection. I. A survey and review of data suggesting possible relationship between malaria and blood groups. Am J Epidemiol 1967; 86:292-304
16. Oliver-Gonzalez J, Torregrosa MV: A substance in animal parasites related to the human isoagglutinogens. J Infect Dis 1944; 74:173-177
17. Harrison J, Ridley DS: Heterologous reactions involving parasites, blood group antibodies and tissue components. Trans R Soc Trop Med Hyg 1975; 69:312-317
18. Loscertales MP, Owens S, O'Donnell J, et al. ABO blood group phenotypes and Plasmodium falciparum malaria: unlocking a pivotal mechanism. Adv Parasitol 2007; 65:1-50
19. Rowe JA, Opi DH, Williams TN: Blood groups and malaria: fresh insights into pathogenesis and identification of targets for intervention. Curr Opin Hematol 2009; 16:480-487
20. Cserti-Gazdewich CM: Plasmodium falciparum malaria and carbohydrate blood group evolution. ISBT Sci Series 2010; 5:256-266
21. Cserti CM, Dzik WH: The ABO blood group system and Plasmodium falciparum malaria. Blood 2007; 110:2250-2258
22. Bowen DJ: An influence of ABO blood group on the rate of proteolysis of von Willebrand factor by ADAMTS13. J Thromb Haemost 2003; 1:33-40
23. Jenkins PV, O'Donnell JS: ABO blood group determines plasma von Willebrand factor levels: a biologic function after all? Transfusion 2006; 46:1836-1844
24. Bridges DJ, Bunn J, van Mourik JA, et al. Rapid activation of endothelial cells enables Plasmodium falciparum adhesion to platelet-decorated von Willebrand factor strings. Blood 2010; 115:1472-1474
25. Tregouet DA, Heath S, Saut N, et al. Common susceptibility alleles are unlikely to contribute as strongly as the FV and ABO loci to VTE risk: results from a GWAS approach. Blood 2009; 113:5298-5303
26. Anstee DJ: The relationship between blood groups and disease. Blood 2010; 115:4635-4643
27. Haldane JBS: The rate of mutation of human genes. Proceedings of the Eighth International Congress on Genetics Sweden. Hereditas 1949; 35:267-273
28. Williams TN: Red blood cell defects and malaria. Mol Biochem Parasitol 2006; 149:121-127
29. Calafell F, Roubinet F, Ramirez-Soriano A, et al. Evolutionary dynamics of the human ABO gene. Hum Genet 2008; 124:123-135
30. D'Adamo P, Whitney C: Eat Right 4 (for) Your Type: The Individualized Diet Solution to Staying Healthy, Living Longer & Achieving Your Ideal Weight: 4 Blood Types, 4 Diets. New York, G.P. Putnam's Sons, 1996
31. Pathirana SL, Alles HK, Bandara S, et al. ABO-blood-group types and protection against severe, Plasmodium falciparum malaria. Ann Trop Med Parasitol 2005; 99:119-124
32. Sharon R, Fibach E: Quantitative flow cytometric analysis of ABO red cell antigens. Cytometry 1991; 12:545-549
33. Fry AE, Griffiths MJ, Auburn S, et al. Common variation in the ABO glycosyltransferase is associated with susceptibility to severe Plasmodium falciparum malaria. Hum Mol Genet 2008; 17:567-576
34. Blumenfeld OO, Patnaik SK: Allelic genes of blood group antigens: a source of human mutations and cSNPs documented in the blood group antigen gene mutation database. Hum Mutat 2004; 23:8-16
35. Storry JR, Olsson ML: The ABO blood group system revisited: a review and update. Immunohematology 2009; 25:48-59
36. Tilley CA, Crookston MC, Brown BL, et al. A and B and A1Leb substances in glycosphingolipid fractions of human serum. Vox Sang 1975; 28:25-33
37. Bongfen SE, Laroque A, Berghout J, et al. Genetic and genomic analyses of host-pathogen interactions in malaria. Trends Parasitol 2009; 25:417-422
38. Kwiatkowski DP: How malaria has affected the human genome and what human genetics can teach us about malaria. Am J Hum Genet 2005; 77:171-192
39. Piazza A, Belvedere MC, Bernoco D, et al. HL-A variation in four Sardinian villages under differential selective pressure by malaria; in Dausset J, Colombani J (eds): Histocompatibility Testing 1972: Report of an International Workshop & Conference (5th: 1972: Evian-les-Bains, France). Copenhagen, Munksgaard; Baltimore, Williams & Wilkins, 1973:73-83.
40. Piazza A, Mayr WR, Contu L, et al. Genetic and population structure of four Sardinian villages. Ann Hum Genet 1985; 49:47-63
41. Contu L, Carcassi C, Orru S, et al. HLA-B35 frequency variations correlate with malaria infection in Sardinia. Tissue Antigens 1998; 52:452-461
42. Bennett S, Allen SJ, Olerup O, et al. Human leucocyte antigen (HLA) and malaria morbidity in a Gambian community. Trans R Soc Trop Med Hyg 1993; 87:286-287
43. Carpenter D, Rooth I, Farnert A, et al. Genetics of susceptibility to malaria related phenotypes. Infect Genet Evol 2009; 9:97-103
44. Hananantachai H, Patarapotikul J, Ohashi J, et al. Polymorphisms of the HLA-B and HLA-DRB1 genes in Thai malaria patients. Jpn J Infect Dis 2005; 58:25-28
45. Hill AV, Allsopp CE, Kwiatkowski D, et al. Common west African HLA antigens are associated with protection from severe malaria. Nature 1991; 352:595-600
46. May J, Meyer CG, Kun JF, et al. HLA class II factors associated with Plasmodium falciparum merozoite surface antigen allele families. J Infect Dis 1999; 179:1042-1045
47. Modiano D, Luoni G, Sirima BS, et al. The lower susceptibility to Plasmodium falciparum malaria of Fulani of Burkina Faso (west Africa) is associated with low frequencies of classic malaria-resistance genes. Trans R Soc Trop Med Hyg 2001; 95:149-152
48. Ndiaye M, Thiam A, Ndiaye R, et al. Susceptibility to neuro-malaria and HLA-DR alleles in Senegal. Dakar Med 1998; 43:25-28
49. Osafo-Addo AD, Koram KA, Oduro AR, et al. HLA-DRB1*04 allele is associated with severe malaria in northern Ghana. Am J Trop Med Hyg 2008; 78:251-255
50. Restrepo M, Rojas W, Montoya F, et al. HLA and malaria in four Colombian ethnic groups. Rev Inst Med Trop Sao Paulo 1988; 30:323-331
51. Shankarkumar U, Devaraj JP, Ghosh K, et al. HLA associations in P. falciparum malaria patients from Mumbai, western India. Indian J Malariol 2002; 39:76-82
52. Sy NE, Long GW, Alcantara AK, et al. HLA antigens and malaria at San Lazaro Hospital Manila, Philippines. Southeast Asian J Trop Med Public Health 1984; 15:1-6
53. Ghosh K: Evolution and selection of human leukocyte antigen alleles by Plasmodium falciparum infection. Hum Immunol 2008; 69:856-860
54. Jallow M, Teo YY, Small KS, et al. Genome-wide and fine-resolution association analysis of malaria in West Africa. Nat Genet 2009; 41:657-665
55. Diakite M, Clark TG, Auburn S, et al. A genetic association study in the Gambia using tagging polymorphisms in the major histocompatibility complex class III region implicates a HLA-B associated transcript 2 polymorphism in severe malaria susceptibility. Hum Genet 2009; 125:105-109
56. Hill AV, Elvin J, Willis AC, et al. Molecular analysis of the association of HLA-B53 and resistance to severe malaria. Nature 1992; 360:434-439
57. Gupta S, Hill AV: Dynamic interactions in malaria: host heterogeneity meets parasite polymorphism. Proc Biol Sci 1995; 261:271-277
58. Hill AV, Jepson A, Plebanski M, et al. Genetic analysis of host-parasite coevolution in human malaria. Philos Trans R Soc Lond B Biol Sci 1997; 352:1317-1325
59. Villartay JP, Rouger P, Muller JY, et al. HLA antigens on peripheral red blood cells: analysis by flow cytofluorometry using monoclonal antibodies. Tissue Antigens 1985; 26:12-19
60. Birkeland S: A method for quantitative evaluation of red cell turnover in humans. II. Clinical application. Scand J Clin Lab Invest 1958; 10:81-90
61. Craig A, Scherf A: Molecules on the surface of the Plasmodium falciparum infected erythrocyte and their role in malaria pathogenesis and immune evasion. Mol Biochem Parasitol 2001; 115:129-143
62. Kraemer SM, Smith JD: A family affair: var genes, PfEMP1 binding, and malaria disease. Curr Opin Microbiol 2006; 9:374-380
63. Graves P, Gelband H: Vaccines for preventing malaria. Cochrane Database Syst Rev 2000; CD000129
64. Graves P, Gelband H: Vaccines for preventing malaria (pre-erythrocytic). Cochrane Database Syst Rev 2006; CD006198
65. Graves P, Gelband H: Vaccines for preventing malaria (SPf66). Cochrane Database Syst Rev 2006; CD005966
66. Graves P, Gelband H: Vaccines for preventing malaria (blood-stage). Cochrane Database Syst Rev 2006; CD006199
67. Ghani AC, Sutherland CJ, Riley EM, et al. Loss of population levels of immunity to malaria as a result of exposure-reducing interventions: consequences for interpretation of disease trends. PLoS ONE 2009; 4:e4383
68. Miller LH, Baruch DI, Marsh K, et al. The pathogenic basis of malaria. Nature 2002; 415:673-679
69. Sherman IW, Eda S, Winograd E: Cytoadherence and sequestration in Plasmodium falciparum: defining the ties that bind. Microbes Infect 2003; 5:897-909
70. Ockenhouse CF, Ho M, Tandon NN, et al. Molecular basis of sequestration in severe and uncomplicated Plasmodium falciparum malaria: differential adhesion of infected erythrocytes to CD36 and ICAM-1. J Infect Dis 1991; 164:163-169
71. Klein MM, Gittis AG, Su HP, et al. The cysteine-rich interdomain region from the highly variable Plasmodium falciparum erythrocyte membrane protein-1 exhibits a conserved structure. PLoS Pathog 2008; 4:e1000147
72. Armesilla AL, Vega MA: Structural organization of the gene for human CD36 glycoprotein. J Biol Chem 1994; 269:18985-18991
73. van Schravendijk MR, Handunnetti SM, Barnwell JW, et al. Normal human erythrocytes express CD36, an adhesion molecule of monocytes, platelets, and endothelial cells. Blood 1992; 80:2105-2114
74. Swerlick RA, Lee KH, Wick TM, et al. Human dermal microvascular endothelial but not human umbilical vein endothelial cells express CD36 in vivo and in vitro. J Immunol 1992; 148:78-83
75. Serghides L, Smith TG, Patel SN, et al. CD36 and malaria: friends or foes? Trends Parasitol 2003; 19:461-469
76. Davis AK, Makar RS, Stowell CP, et al. ADAMTS13 binds to CD36: a potential mechanism for platelet and endothelial localization of ADAMTS13. Transfusion 2009; 49:206-213
77. Febbraio M, Hajjar DP, Silverstein RL: CD36: a class B scavenger receptor involved in angiogenesis, atherosclerosis, inflammation, and lipid metabolism. J Clin Invest 2001; 108:785-791
78. Ho M, Singh B, Looareesuwan S, et al. Clinical correlates of in vitro Plasmodium falciparum cytoadherence. Infect Immun 1991; 59:873-878
79. Patel SN, Lu Z, Ayi K, et al. Disruption of CD36 impairs cytokine response to Plasmodium falciparum glycosylphosphatidylinositol and confers susceptibility to severe and fatal malaria in vivo. J Immunol 2007; 178:3954-3961
80. Ockenhouse CF, Tandon NN, Magowan C, et al. Identification of a platelet membrane glycoprotein as a falciparum malaria sequestration receptor. Science 1989; 243:1469-1471
81. Udomsangpetch R, Webster HK, Pattanapanyasat K, et al. Cytoadherence characteristics of rosette-forming Plasmodium falciparum. Infect Immun 1992; 60:4483-4490
82. Pain A, Ferguson DJ, Kai O, et al. Platelet-mediated clumping of Plasmodium falciparum-infected erythrocytes is a common adhesive phenotype and is associated with severe malaria. Proc Natl Acad Sci U S A 2001; 98:1805-1810
83. Cserti-Gazdewich CM, Dzik WH, Dorn ME, et al. Quantitation of CD36 (platelet glycoprotein IV) expression on platelets and monocytes by flow cytometry: application to the study of Plasmodium falciparum malaria. Cytometry B Clin Cytom 2009; 76:127-134
84. Grau GE, Mackenzie CD, Carr RA, et al. Platelet accumulation in brain microvessels in fatal pediatric cerebral malaria. J Infect Dis 2003; 187:461-466
85. Ladhani S, Lowe B, Cole AO, et al. Changes in white blood cells and platelets in children with falciparum malaria: relationship to disease outcome. Br J Haematol 2002; 119:839-847
86. Silamut K, Phu NH, Whitty C, et al. A quantitative analysis of the microvascular sequestration of malaria parasites in the human brain. Am J Pathol 1999; 155:395-410
87. de Mast Q, Groot E, Lenting PJ, et al. Thrombocytopenia and release of activated von Willebrand Factor during early Plasmodium falciparum malaria. J Infect Dis 2007; 196:622-628
88. Hollestelle MJ, Donkor C, Mantey EA, et al. von Willebrand factor propeptide in malaria: evidence of acute endothelial cell activation. Br J Haematol 2006; 133:562-569
89. de Mast Q, Groot E, Asih PB, et al. ADAMTS13 deficiency with elevated levels of ultra-large and active von Willebrand factor in P. falciparum and P. vivax malaria. Am J Trop Med Hyg 2009; 80:492-498
90. Larkin D, de Laat B, Jenkins PV, et al. Severe Plasmodium falciparum malaria is associated with circulating ultra-large von Willebrand multimers and ADAMTS13 inhibition. PLoS Pathog 2009; 5:e1000349
91. Cox D, McConkey S: The role of platelets in the pathogenesis of cerebral malaria. Cell Mol Life Sci 2010; 67:557-568
92. Wassmer SC, Lepolard C, Traore B, et al. Platelets reorient Plasmodium falciparum-infected erythrocyte cytoadhesion to activated endothelial cells. J Infect Dis 2004; 189:180-189
93. Combes V, Coltel N, Faille D, et al. Cerebral malaria: role of microparticles and platelets in alterations of the blood-brain barrier. Int J Parasitol 2006; 36:541-546
94. Faille D, Combes V, Mitchell AJ, et al. Platelet microparticles: a new player in malaria parasite cytoadherence to human brain endothelium. FASEB J 2009; 23:3449-3458
95. Curtis BR, Aster RH: Incidence of the Nak(a)-negative platelet phenotype in African Americans is similar to that of Asians. Transfusion 1996; 36:331-334
96. Lee K, Godeau B, Fromont P, et al. CD36 deficiency is frequent and can cause platelet immunization in Africans. Transfusion 1999; 39:873-879
97. Ikeda H, Mitani T, Ohnuma M, et al. A new platelet-specific antigen, Naka, involved in the refractoriness of HLA-matched platelet transfusion. Vox Sang 1989; 57:213-217
98. Yamamoto N, Ikeda H, Tandon NN, et al. A platelet membrane glycoprotein (GP) deficiency in healthy blood donors: Naka- platelets lack detectable GPIV (CD36). Blood 1990; 76:1698-1703
99. Kashiwagi H, Honda S, Tomiyama Y, et al. A novel polymorphism in glycoprotein IV (replacement of proline-90 by serine) predominates in subjects with platelet GPIV deficiency. Thromb Haemost 1993; 69:481-484
100. Pain A, Urban BC, Kai O, et al. A non-sense mutation in Cd36 gene is associated with protection from severe malaria. Lancet 2001; 357:1502-1503
101. Chilongola J, Balthazary S, Mpina M, et al. CD36 deficiency protects against malarial anaemia in children by reducing Plasmodium falciparum-infected red blood cell adherence to vascular endothelium. Trop Med Int Health 2009; 14:810-816
102. Omi K, Ohashi J, Patarapotikul J, et al. CD36 polymorphism is associated with protection from cerebral malaria. Am J Hum Genet 2003; 72:364-374
103. Sinha S, Qidwai T, Kanchan K, et al. Variations in host genes encoding adhesion molecules and susceptibility to falciparum malaria in India. Malar J 2008; 7:250
104. Das A, Das TK, Sahu U, et al. CD36 T188G gene polymorphism and severe falciparum malaria in India. Trans R Soc Trop Med Hyg 2009; 103:687-690
105. Aitman TJ, Cooper LD, Norsworthy PJ, et al. Malaria susceptibility and CD36 mutation. Nature 2000; 405:1015-1016
106. Omi K, Ohashi J, Naka I, et al. Polymorphisms of CD36 in Thai malaria patients. Southeast Asian J Trop Med Public Health 2002; 33(Suppl. 3):1-4
107. Fry AE, Ghansa A, Small KS, et al. Positive selection of a CD36 nonsense variant in sub-Saharan Africa, but no association with severe malaria phenotypes. Hum Mol Genet 2009; 18:2683-2692
108. Cunha-Rodrigues M, Portugal S, Febbraio M, et al. Bone marrow chimeric mice reveal a dual role for CD36 in Plasmodium berghei ANKA infection. Malar J 2007; 6:32
109. Kashiwagi H, Tomiyama Y, Honda S, et al. Molecular basis of CD36 deficiency. Evidence that a 478C-->T substitution (proline90-->serine) in CD36 cDNA accounts for CD36 deficiency. J Clin Invest 1995; 95:1040-1046
110. Kashiwagi H, Tomiyama Y, Kosugi S, et al. Family studies of type II CD36 deficient subjects: linkage of a CD36 allele to a platelet-specific mRNA expression defect(s) causing type II CD36 deficiency. Thromb Haemost 1995; 74:758-763
111. Imai M, Tanaka T, Kintaka T, et al. Genomic heterogeneity of type II CD36 deficiency. Clin Chim Acta 2002; 321:97-106
112. Yanai H, Chiba H, Fujiwara H, et al. Phenotype-genotype correlation in CD36 deficiency types I and II. Thromb Haemost 2000; 84:436-441
113. Singh Ahuja H, Liu S, Crombie DL, et al. Differential effects of rexinoids and thiazolidinediones on metabolic gene expression in diabetic rodents. Mol Pharmacol 2001; 59:765-773
114. Rac ME, Safranow K, Poncyljusz W: Molecular basis of human CD36 gene mutations. Mol Med 2007; 13:288-296
115. Andersen M, Lenhard B, Whatling C, et al. Alternative promoter usage of the membrane glycoprotein CD36. BMC Mol Biol 2006; 7:8
116. Kern P, Kolowos W, Hagenhofer M, et al. Alternatively spliced mRNA molecules of the thrombospondin receptor (CD36) in human PBMC. Eur J Immunogenet 1999; 26:337-342
117. Tang Y, Taylor KT, Sobieski DA, et al. Identification of a human CD36 isoform produced by exon skipping. Conservation of exon organization and pre-mRNA splicing patterns with a CD36 gene family member, CLA-1. J Biol Chem 1994; 269:6011-6015