Hemoglobinopathies: Slicing the Gordian Knot of Plasmodium falciparum Malaria Pathogenesis

PLoS Pathogens

Volumn 9, Issue 5, 2013, Pages

  Taylor, Steve M ^a,b   Cerami, Carla ^b   Fairhurst, Rick M ^c  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b IL   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROCYTE MEMBRANE PROTEIN 1; HEME OXYGENASE 1; HEMOGLOBIN C; HEMOGLOBIN E; HEMOGLOBIN F; HEMOGLOBIN S; NITRIC OXIDE;

ADAPTIVE IMMUNITY; ARTICLE; CELL ADHESION; ERYTHROCYTE; GENOTYPE; HEMOGLOBINOPATHY; HOST PARASITE INTERACTION; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; MALARIA FALCIPARUM; NONHUMAN; OXYGEN TENSION; PATHOGENESIS; PHAGOCYTOSIS; PLASMODIUM FALCIPARUM; PROTEIN EXPRESSION; THALASSEMIA;

AFRICA; ANIMALS; CHILD, PRESCHOOL; GENOME, HUMAN; HEMOGLOBINOPATHIES; HUMANS; INFANT; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM;

GORDIA; MURINAE; PLASMODIUM FALCIPARUM;

EID: 84878481415     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003327     Document Type: Article

References (115)

1. Yenne B (2010) Alexander the Great: lessons from history's undefeated general. New York: Palgrave Macmillan.
2. World Health Organization (2012) World malaria report: 2012. Available: http://www.who.int/malaria/publications/world_malaria_report_2012/en/index.html. Accessed 19 March 2013.
3. Bejon P, Lusingu J, Olotu A, Leach A, Lievens M, et al. (2008) Efficacy of RTS,S/AS01E vaccine against malaria in children 5 to 17 months of age. N Engl J Med 359: 2521-2532.
4. The RTS,S Clinical Trials Partnership (2011) First results of phase 3 trial of RTS,S/AS01 malaria vaccine in African children. N Engl J Med 365: 1863-1875.
5. O'Meara WP, Bejon P, Mwangi TW, Okiro EA, Peshu N, et al. (2008) Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet 372: 1555-1562.
6. Miller LH, Baruch DI, Marsh K, Doumbo OK, (2002) The pathogenic basis of malaria. Nature 415: 673-679.
7. Amaratunga C, Lopera-Mesa TM, Tse JG, Mita-Mendoza NK, Fairhurst RM (2010) In:Kaufmann S, Rouse B, Sacks D, editor. Immunology of infectious diseases. Washington, DC: American Society of Microbiology Press.
8. Taylor SM, Parobek CM, Fairhurst RM, (2012) Haemoglobinopathies and the clinical epidemiology of malaria: a systematic review and meta-analysis. Lancet Infect Dis 12: 457-468.
9. Haldane JB, (1949) The rate of mutation of human genes. Hereditas 35: 267-273.
10. Weatherall DJ, Provan AB, (2000) Red cells I: inherited anaemias. Lancet 355: 1169-1175.
11. Trager W, Jensen JB, (1976) Human malaria parasites in continuous culture. Science 193: 673-675.
12. Haynes JD, Diggs CL, Hines FA, Desjardins RE, (1976) Culture of human malaria parasites Plasmodium falciparum. Nature 263: 767-769.
13. Bunyaratvej A, Butthep P, Sae-Ung N, Fucharoen S, Yuthavong Y, (1992) Reduced deformability of thalassemic erythrocytes and erythrocytes with abnormal hemoglobins and relation with susceptibility to Plasmodium falciparum invasion. Blood 79: 2460-2463.
14. Ifediba TC, Stern A, Ibrahim A, Rieder RF, (1985) Plasmodium falciparum in vitro: diminished growth in hemoglobin H disease erythrocytes. Blood 65: 452-455.
15. Chotivanich K, Udomsangpetch R, Pattanapanyasat K, Chierakul W, Simpson J, et al. (2002) Hemoglobin E: a balanced polymorphism protective against high parasitemias and thus severe P falciparum malaria. Blood 100: 1172-1176.
16. Brockelman CR, Wongsattayanont B, Tan-ariya P, Fucharoen S, (1987) Thalassemic erythrocytes inhibit in vitro growth of Plasmodium falciparum. J Clin Microbiol 25: 56-60.
17. Pasvol G, Weatherall DJ, Wilson RJ, (1978) Cellular mechanism for the protective effect of haemoglobin S against P. falciparum malaria. Nature 274: 701-703.
18. Pasvol G, (1980) The interaction between sickle haemoglobin and the malarial parasite Plasmodium falciparum. Trans R Soc Trop Med Hyg 74: 701-705.
19. Friedman MJ, Roth EF, Nagel RL, Trager W, (1979) The role of hemoglobins C, S, and Nbalt in the inhibition of malaria parasite development in vitro. Am J Trop Med Hyg 28: 777-780.
20. Olson JA, Nagel RL, (1986) Synchronized cultures of P falciparum in abnormal red cells: the mechanism of the inhibition of growth in HbCC cells. Blood 67: 997-1001.
21. Fairhurst RM, Fujioka H, Hayton K, Collins KF, Wellems TE, (2003) Aberrant development of Plasmodium falciparum in hemoglobin CC red cells: implications for the malaria protective effect of the homozygous state. Blood 101: 3309-3315.
22. Nagel RL, Raventos-Suarez C, Fabry ME, Tanowitz H, Sicard D, et al. (1981) Impairment of the growth of Plasmodium falciparum in HbEE erythrocytes. J Clin Invest 68: 303-305.
23. Pasvol G, Weatherall DJ, Wilson RJ, Smith DH, Gilles HM, (1976) Fetal haemoglobin and malaria. Lancet 1: 1269-1272.
24. Friedman MJ, (1979) Oxidant damage mediates variant red cell resistance to malaria. Nature 280: 245-247.
25. Pasvol G, Weatherall DJ, Wilson RJ, (1977) Effects of foetal haemoglobin on susceptibility of red cells to Plasmodium falciparum. Nature 270: 171-173.
26. Wilson RJ, Pasvol G, Weatherall DJ, (1977) Invasion and growth of Plasmodium falciparum in different types of human erythrocyte. Bull World Health Organ 55: 179-186.
27. Luzzatto L, Nwachuku-Jarrett ES, Reddy S, (1970) Increased sickling of parasitised erythrocytes as mechanism of resistance against malaria in the sickle-cell trait. Lancet 1: 319-321.
28. Roth EF Jr, Friedman M, Ueda Y, Tellez I, Trager W, et al. (1978) Sickling rates of human AS red cells infected in vitro with Plasmodium falciparum malaria. Science 202: 650-652.
29. Friedman MJ, (1978) Erythrocytic mechanism of sickle cell resistance to malaria. Proc Natl Acad Sci U S A 75: 1994-1997.
30. Chen SY, Wang Y, Telen MJ, Chi JT, (2008) The genomic analysis of erythrocyte microRNA expression in sickle cell diseases. PLoS One 3: e2360 doi:10.1371/journal.pone.0002360.
31. Sangokoya C, Telen MJ, Chi JT, (2010) microRNA miR-144 modulates oxidative stress tolerance and associates with anemia severity in sickle cell disease. Blood 116: 4338-4348.
32. Lamonte G, Philip N, Reardon J, Lacsina JR, Majoros W, et al. (2012) Translocation of sickle cell erythrocyte microRNAs into Plasmodium falciparum inhibits parasite translation and contributes to malaria resistance. Cell Host Microbe 12: 187-199.
33. Baruch DI, Gormely JA, Ma C, Howard RJ, Pasloske BL, (1996) Plasmodium falciparum erythrocyte membrane protein 1 is a parasitized erythrocyte receptor for adherence to CD36, thrombospondin, and intercellular adhesion molecule 1. Proc Natl Acad Sci U S A 93: 3497-3502.
34. Carlson J, Helmby H, Hill AV, Brewster D, Greenwood BM, et al. (1990) Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet 336: 1457-1460.
35. Kaul DK, Roth EF Jr, Nagel RL, Howard RJ, Handunnetti SM, (1991) Rosetting of Plasmodium falciparum-infected red blood cells with uninfected red blood cells enhances microvascular obstruction under flow conditions. Blood 78: 812-819.
36. Su XZ, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JA, et al. (1995) The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 82: 89-100.
37. Smith JD, Chitnis CE, Craig AG, Roberts DJ, Hudson-Taylor DE, et al. (1995) Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82: 101-110.
38. Baruch DI, Pasloske BL, Singh HB, Bi X, Ma XC, et al. (1995) Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 82: 77-87.
39. Raventos-Suarez C, Kaul DK, Macaluso F, Nagel RL, (1985) Membrane knobs are required for the microcirculatory obstruction induced by Plasmodium falciparum-infected erythrocytes. Proc Natl Acad Sci U S A 82: 3829-3833.
40. Fried M, Duffy PE, (1996) Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 272: 1502-1504.
41. Salanti A, Staalsoe T, Lavstsen T, Jensen AT, Sowa MP, et al. (2003) Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol Microbiol 49: 179-191.
42. Rowe JA, Moulds JM, Newbold CI, Miller LH, (1997) P. falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature 388: 292-295.
43. Carlson J, Wahlgren M, (1992) Plasmodium falciparum erythrocyte rosetting is mediated by promiscuous lectin-like interactions. J Exp Med 176: 1311-1317.
44. Chen Q, Barragan A, Fernandez V, Sundstrom A, Schlichtherle M, et al. (1998) Identification of Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) as the rosetting ligand of the malaria parasite P. falciparum. J Exp Med 187: 15-23.
45. Schofield L, Hackett F, (1993) Signal transduction in host cells by a glycosylphosphatidylinositol toxin of malaria parasites. J Exp Med 177: 145-153.
46. Lopera-Mesa TM, Mita-Mendoza NK, van de Hoef DL, Doumbia S, Konate D, et al. (2012) Plasma Uric Acid Levels Correlate with Inflammation and Disease Severity in Malian Children with Plasmodium falciparum Malaria. PLoS One 7: e46424 doi:10.1371/journal.pone.0046424.
47. D'Ombrain MC, Voss TS, Maier AG, Pearce JA, Hansen DS, et al. (2007) Plasmodium falciparum erythrocyte membrane protein-1 specifically suppresses early production of host interferon-gamma. Cell Host Microbe 2: 130-138.
48. Udomsangpetch R, Sueblinvong T, Pattanapanyasat K, Dharmkrong-at A, Kittikalayawong A, et al. (1993) Alteration in cytoadherence and rosetting of Plasmodium falciparum-infected thalassemic red blood cells. Blood 82: 3752-3759.
49. Fairhurst RM, Baruch DI, Brittain NJ, Ostera GR, Wallach JS, et al. (2005) Abnormal display of PfEMP-1 on erythrocytes carrying haemoglobin C may protect against malaria. Nature 435: 1117-1121.
50. Cholera R, Brittain NJ, Gillrie MR, Lopera-Mesa TM, Diakite SA, et al. (2008) Impaired cytoadherence of Plasmodium falciparum-infected erythrocytes containing sickle hemoglobin. Proc Natl Acad Sci U S A 105: 991-996.
51. Amaratunga C, Lopera-Mesa TM, Brittain NJ, Cholera R, Arie T, et al. (2011) A role for fetal hemoglobin and maternal immune IgG in infant resistance to Plasmodium falciparum malaria. PLoS One 6: e14798 doi:10.1371/journal.pone.0014798.
52. Krause MA, Diakite SA, Lopera-Mesa TM, Amaratunga C, Arie T, et al. (2012) alpha-Thalassemia impairs the cytoadherence of Plasmodium falciparum-infected erythrocytes. PLoS One 7: e37214 doi:10.1371/journal.pone.0037214.
53. Fairhurst RM, Bess CD, Krause MA, (2012) Abnormal PfEMP1/knob display on Plasmodium falciparum-infected erythrocytes containing hemoglobin variants: fresh insights into malaria pathogenesis and protection. Microbes Infect 14: 851-862.
54. Cyrklaff M, Sanchez CP, Kilian N, Bisseye C, Simpore J, et al. (2011) Hemoglobins S and C interfere with actin remodeling in Plasmodium falciparum-infected erythrocytes. Science 334: 1283-1286.
55. Schofield L, Grau GE, (2005) Immunological processes in malaria pathogenesis. Nat Rev Immunol 5: 722-735.
56. Clark IA, Alleva LM, Mills AC, Cowden WB, (2004) Pathogenesis of malaria and clinically similar conditions. Clin Microbiol Rev 17: 509-539 table of contents.
57. Hunt NH, Grau GE, (2003) Cytokines: accelerators and brakes in the pathogenesis of cerebral malaria. Trends Immunol 24: 491-499.
58. John CC, Kutamba E, Mugarura K, Opoka RO, (2010) Adjunctive therapy for cerebral malaria and other severe forms of Plasmodium falciparum malaria. Expert Rev Anti Infect Ther 8: 997-1008.
59. Achtman AH, Pilat S, Law CW, Lynn DJ, Janot L, et al. (2012) Effective adjunctive therapy by an innate defense regulatory peptide in a preclinical model of severe malaria. Sci Transl Med 4: 135ra164.
60. Casals-Pascual C, Idro R, Picot S, Roberts DJ, Newton CR, (2009) Can erythropoietin be used to prevent brain damage in cerebral malaria? Trends Parasitol 25: 30-36.
61. Weinberg JB, Lopansri BK, Mwaikambo E, Granger DL, (2008) Arginine, nitric oxide, carbon monoxide, and endothelial function in severe malaria. Curr Opin Infect Dis 21: 468-475.
62. Takeuchi O, Akira S, (2010) Pattern recognition receptors and inflammation. Cell 140: 805-820.
63. Villa P, Bigini P, Mennini T, Agnello D, Laragione T, et al. (2003) Erythropoietin selectively attenuates cytokine production and inflammation in cerebral ischemia by targeting neuronal apoptosis. J Exp Med 198: 971-975.
64. Siren AL, Fratelli M, Brines M, Goemans C, Casagrande S, et al. (2001) Erythropoietin prevents neuronal apoptosis after cerebral ischemia and metabolic stress. Proc Natl Acad Sci U S A 98: 4044-4049.
65. Wagener FA, Eggert A, Boerman OC, Oyen WJ, Verhofstad A, et al. (2001) Heme is a potent inducer of inflammation in mice and is counteracted by heme oxygenase. Blood 98: 1802-1811.
66. Kapturczak MH, Wasserfall C, Brusko T, Campbell-Thompson M, Ellis TM, et al. (2004) Heme oxygenase-1 modulates early inflammatory responses: evidence from the heme oxygenase-1-deficient mouse. Am J Pathol 165: 1045-1053.
67. Kim H, Higgins S, Liles WC, Kain KC, (2011) Endothelial activation and dysregulation in malaria: a potential target for novel therapeutics. Curr Opin Hematol 18: 177-185.
68. Koh SH, Noh MY, Cho GW, Kim KS, Kim SH, (2009) Erythropoietin increases the motility of human bone marrow-multipotent stromal cells (hBM-MSCs) and enhances the production of neurotrophic factors from hBM-MSCs. Stem Cells Dev 18: 411-421.
69. Erbayraktar Z, Erbayraktar S, Yilmaz O, Cerami A, Coleman T, et al. (2009) Nonerythropoietic tissue protective compounds are highly effective facilitators of wound healing. Mol Med 15: 235-241.
70. Krishnegowda G, Hajjar AM, Zhu J, Douglass EJ, Uematsu S, 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.
71. Parroche P, Lauw FN, Goutagny N, Latz E, Monks BG, 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 U S A 104: 1919-1924.
72. Jaramillo M, Plante I, Ouellet N, Vandal K, Tessier PA, et al. (2004) Hemozoin-inducible proinflammatory events in vivo: potential role in malaria infection. J Immunol 172: 3101-3110.
73. 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.
74. Clark IA, Hunt NH, Butcher GA, Cowden WB, (1987) Inhibition of murine malaria (Plasmodium chabaudi) in vivo by recombinant interferon-gamma or tumor necrosis factor, and its enhancement by butylated hydroxyanisole. J Immunol 139: 3493-3496.
75. Kaiser K, Texier A, Ferrandiz J, Buguet A, Meiller A, et al. (2006) Recombinant human erythropoietin prevents the death of mice during cerebral malaria. J Infect Dis 193: 987-995.
76. Yeo TW, Lampah DA, Gitawati R, Tjitra E, Kenangalem E, et al. (2008) Angiopoietin-2 is associated with decreased endothelial nitric oxide and poor clinical outcome in severe falciparum malaria. Proc Natl Acad Sci U S A 105: 17097-17102.
77. Conroy AL, Phiri H, Hawkes M, Glover S, Mallewa M, et al. (2010) Endothelium-based biomarkers are associated with cerebral malaria in Malawian children: a retrospective case-control study. PLoS One 5: e15291 doi:10.1371/journal.pone.0015291.
78. Lovegrove FE, Tangpukdee N, Opoka RO, Lafferty EI, Rajwans N, et al. (2009) Serum angiopoietin-1 and-2 levels discriminate cerebral malaria from uncomplicated malaria and predict clinical outcome in African children. PLoS One 4: e4912 doi:10.1371/journal.pone.0004912.
79. Clark IA, Awburn MM, Harper CG, Liomba NG, Molyneux ME, (2003) Induction of HO-1 in tissue macrophages and monocytes in fatal falciparum malaria and sepsis. Malar J 2: 41.
80. Casals-Pascual C, Idro R, Gicheru N, Gwer S, Kitsao B, et al. (2008) High levels of erythropoietin are associated with protection against neurological sequelae in African children with cerebral malaria. Proc Natl Acad Sci U S A 105: 2634-2639.
81. Larsen R, Gozzelino R, Jeney V, Tokaji L, Bozza FA, et al. (2010) A central role for free heme in the pathogenesis of severe sepsis. Sci Transl Med 2: 51ra71.
82. Pamplona A, Ferreira A, Balla J, Jeney V, Balla G, et al. (2007) Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat Med 13: 703-710.
83. Seixas E, Gozzelino R, Chora A, Ferreira A, Silva G, et al. (2009) Heme oxygenase-1 affords protection against noncerebral forms of severe malaria. Proc Natl Acad Sci U S A 106: 15837-15842.
84. Cunnington AJ, de Souza JB, Walther M, Riley EM, (2012) Malaria impairs resistance to Salmonella through heme- and heme oxygenase-dependent dysfunctional granulocyte mobilization. Nat Med 18: 120-127.
85. Ferreira A, Marguti I, Bechmann I, Jeney V, Chora A, et al. (2011) Sickle hemoglobin confers tolerance to Plasmodium infection. Cell 145: 398-409.
86. Walther M, De Caul A, Aka P, Njie M, Amambua-Ngwa A, et al. (2012) HMOX1 gene promoter alleles and high HO-1 levels are associated with severe malaria in Gambian children. PLoS Pathog 8: e1002579 doi:10.1371/journal.ppat.1002579.
87. Lopansri BK, Anstey NM, Weinberg JB, Stoddard GJ, Hobbs MR, et al. (2003) Low plasma arginine concentrations in children with cerebral malaria and decreased nitric oxide production. Lancet 361: 676-678.
88. Yeo TW, Lampah DA, Gitawati R, Tjitra E, Kenangalem E, et al. (2007) Impaired nitric oxide bioavailability and L-arginine reversible endothelial dysfunction in adults with falciparum malaria. J Exp Med 204: 2693-2704.
89. Hobbs MR, Udhayakumar V, Levesque MC, Booth J, Roberts JM, et al. (2002) A new NOS2 promoter polymorphism associated with increased nitric oxide production and protection from severe malaria in Tanzanian and Kenyan children. Lancet 360: 1468-1475.
90. Rockett KA, Awburn MM, Cowden WB, Clark IA, (1991) Killing of Plasmodium falciparum in vitro by nitric oxide derivatives. Infect Immun 59: 3280-3283.
91. Rockett KA, Awburn MM, Rockett EJ, Cowden WB, Clark IA, (1994) Possible role of nitric oxide in malarial immunosuppression. Parasite Immunol 16: 243-249.
92. De Caterina R, Libby P, Peng HB, Thannickal VJ, Rajavashisth TB, et al. (1995) Nitric oxide decreases cytokine-induced endothelial activation. Nitric oxide selectively reduces endothelial expression of adhesion molecules and proinflammatory cytokines. J Clin Invest 96: 60-68.
93. Serirom S, Raharjo WH, Chotivanich K, Loareesuwan S, Kubes P, et al. (2003) Anti-adhesive effect of nitric oxide on Plasmodium falciparum cytoadherence under flow. Am J Pathol 162: 1651-1660.
94. Williams TN, Mwangi TW, Roberts DJ, Alexander ND, Weatherall DJ, et al. (2005) An immune basis for malaria protection by the sickle cell trait. PLoS Med 2: e128 doi:10.1371/journal.pmed.0020128.
95. Gong L, Maiteki-Sebuguzi C, Rosenthal PJ, Hubbard AE, Drakeley CJ, et al. (2012) Evidence for both innate and acquired mechanisms of protection from Plasmodium falciparum in children with sickle cell trait. Blood 119: 3808-3814.
96. Cohen S, Mc GI, Carrington S, (1961) Gamma-globulin and acquired immunity to human malaria. Nature 192: 733-737.
97. Cornille-Brogger R, Fleming AF, Kagan I, Matsushima T, Molineaux L, (1979) Abnormal haemoglobins in the Sudan savanna of Nigeria. II. Immunological response to malaria in normals and subjects with sickle cell trait. Ann Trop Med Parasitol 73: 173-183.
98. Allen SJ, Bennett S, Riley EM, Rowe PA, Jakobsen PH, et al. (1992) Morbidity from malaria and immune responses to defined Plasmodium falciparum antigens in children with sickle cell trait in The Gambia. Trans R Soc Trop Med Hyg 86: 494-498.
99. Le Hesran JY, Personne I, Personne P, Fievet N, Dubois B, et al. (1999) Longitudinal study of Plasmodium falciparum infection and immune responses in infants with or without the sickle cell trait. Int J Epidemiol 28: 793-798.
100. Luty AJ, Ulbert S, Lell B, Lehman L, Schmidt-Ott R, et al. (2000) Antibody responses to Plasmodium falciparum: evolution according to the severity of a prior clinical episode and association with subsequent reinfection. Am J Trop Med Hyg 62: 566-572.
101. Cabrera G, Cot M, Migot-Nabias F, Kremsner PG, Deloron P, et al. (2005) The sickle cell trait is associated with enhanced immunoglobulin G antibody responses to Plasmodium falciparum variant surface antigens. J Infect Dis 191: 1631-1638.
102. Verra F, Simpore J, Warimwe GM, Tetteh KK, Howard T, et al. (2007) Haemoglobin C and S role in acquired immunity against Plasmodium falciparum malaria. PLoS One 2: e978 doi: 10.1371/journal.pone.0000978.
103. Tan X, Traore B, Kayentao K, Ongoiba A, Doumbo S, et al. (2011) Hemoglobin S and C heterozygosity enhances neither the magnitude nor breadth of antibody responses to a diverse array of Plasmodium falciparum antigens. J Infect Dis 204: 1750-1761.
104. Celada A, Cruchaud A, Perrin LH, (1982) Opsonic activity of human immune serum on in vitro phagocytosis of Plasmodium falciparum infected red blood cells by monocytes. Clin Exp Immunol 47: 635-644.
105. Luzzi GA, Merry AH, Newbold CI, Marsh K, Pasvol G, et al. (1991) Surface antigen expression on Plasmodium falciparum-infected erythrocytes is modified in alpha- and beta-thalassemia. J Exp Med 173: 785-791.
106. Williams TN, Weatherall DJ, Newbold CI, (2002) The membrane characteristics of Plasmodium falciparum-infected and-uninfected heterozygous alpha(0)thalassaemic erythrocytes. Br J Haematol 118: 663-670.
107. Ayi K, Turrini F, Piga A, Arese P, (2004) Enhanced phagocytosis of ring-parasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and beta-thalassemia trait. Blood 104: 3364-3371.
108. Langhorne J, Ndungu F, Sponaas A-M, Marsh K, (2008) Immunity to malaria: more questions than answers. Nature Immunol 9: 725-732.
109. Urban BC, Mwangi T, Ross A, Kinyanjui S, Mosobo M, et al. (2001) Peripheral blood dendritic cells in children with acute Plasmodium falciparum malaria. Blood 98: 2859-2861.
110. Xu H, Wipasa J, Yan H, Zeng M, Makobongo MO, et al. (2002) The mechanism and significance of deletion of parasite-specific CD4(+) T cells in malaria infection. J Exp Med 195: 881-892.
111. Sun T, Holowka T, Song Y, Zierow S, Leng L, et al. (2012) A Plasmodium-encoded cytokine suppresses T-cell immunity during malaria. Proc Natl Acad Sci U S A 109: E2117-2126.
112. Wykes MN, Zhou YH, Liu XQ, Good MF, (2005) Plasmodium yoelii can ablate vaccine-induced long-term protection in mice. J Immunol 175: 2510-2516.
113. Urban BC, Ferguson DJ, Pain A, Willcox N, Plebanski M, et al. (1999) Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 400: 73-77.
114. Wu Y, Szestak T, Stins M, Craig AG, (2011) Amplification of P. falciparum Cytoadherence through induction of a pro-adhesive state in host endothelium. PLoS One 6: e24784 doi:10.1371/journal.pone.0024784.
115. Santiyanont R, Wilairat P, (1981) Red cells containing hemoglobin E do not inhibit malaria parasite development in vitro. Am J Trop Med Hyg 30: 541-543.