Adenosine triphosphate depletion of erythrocytes simulates the phenotype associated with pyruvate kinase deficiency and confers protection against plasmodium falciparum in vitro

Journal of Infectious Diseases

Volumn 200, Issue 8, 2009, Pages 1289-1299

  Ayi, Kodjo ^a   Liles, W Conrad ^a,b   Gros, Philippe ^c   Kain, Kevin C ^a,b  

^a TORONTO GENERAL HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; FLUORIDE SODIUM; PYRUVATE KINASE;

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME DEFICIENCY; ERYTHROCYTE; FEMALE; GENE EXPRESSION; GLUCOSE 6 PHOSPHATE DEHYDROGENASE DEFICIENCY; HETEROZYGOSITY; HOMOZYGOSITY; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; PHAGOCYTOSIS; PHENOTYPE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PYRUVATE KINASE DEFICIENCY; THALASSEMIA;

EID: 70349416600     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1086/605843     Document Type: Article

References (51)

1. Williams T.N. Human red blood cell polymorphisms and malaria Current Opinion in Microbiology 2006 9 4 388-394 DOI 10.1016/j.mib.2006.06.009, PII S1369527406000920 1. Williams TN. Human red blood cell polymorphisms and malaria. Curr Opin Microbiol 2006; 9:388-394 (Pubitemid 44108720)
2. Arese P, Ayi K, Skorokhod A, Turrini E Removal or early parasite forms from circulation as a mechanism of resistance against malaria in widespread red blood cell mutation. In: Dronamraju KR, Arese P, eds. Malaria: genetic and evolutionary aspects. New York: Springer, 2006: 25-53.
3. Aidoo M. Terlouw D.J. Kolczak M.S. McElroy P.D. Ter Kuile F.O. Kariuki S. Nahlen B.L. Lal A.A. Udhayakumar V. Protective effects of the sickle cell gene against malaria morbidity and mortality Lancet 2002 359 9314 1311-1312 DOI 10.1016/S0140-6736(02)08273-9 3. Aidoo M, Terlouw DJ, Kolczak MS, et al. Protective effects of sickle cell gene against malaria morbidity and mortality. Lancet 2002; 359: 1311-1312 (Pubitemid 34310639)
4. Hill AV. Molecular epidemiology of the thalassaemias (including haemoglobin E). Baillieres Clin Haematol 1992;5:209-238
5. Ruwende C, Khoo SC, Snow RW, et al. Natural selection of hemi- and heterozygotes for G6PD deficiency in Africa by resistance to severe malaria. Nature 1995; 376:246-249
6. Agarwal A. Guindo A. Cissoko Y. Taylor J.G. Coulibaly D. Kone A. Kayentao K. Djimde A. Plowe C.V. Doumbo O. Wellems T.E. Diallo D. Hemoglobin C associated with protection from severe malaria in the Dogon of Mali, a West African population with a low prevalence of hemoglobin S Blood 2000 96 7 2358-2363 6. Agarwal A, Guindo A, Cissoko Y, et al. Hemoglobin C associated with protection from severe malaria in the Dogon of Mali, a West African population with a low prevalence of hemoglobin S. Blood 2000; 96: 2358-2363 (Pubitemid 30745254)
7. Ayi K. Turrini F. Piga A. Arese P. 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 2004 104 10 3364-3371 DOI 10.1182/blood-2003-11-3820 7. Ayi K, Turrini F, Piga A, Arese P. Enhanced phagocytosis of ringparasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and beta-thalassemia trait. Blood 2004; 104:3364-3371 (Pubitemid 39507160)
8. Fairhurst RM, Baruch DI, Brittain NJ, et al. Abnormal display of PfEMP-1 on erythrocytes carrying haemoglobin C may protect against malaria. Nature 2005;435:1117-1121
9. Cappadoro M, Giribaldi G, O'Brien E, et al. Early phagocytosis of glucose-6-phosphate dehydrogenase (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency. Blood 1998;92:2527-2534
10. Zanella A. Fermo E. Bianchi P. Valentini G. Red cell pyruvate kinase deficiency: Molecular and clinical aspects British Journal of Haematology 2005 130 1 11-25 DOI 10.1111/j.1365-2141.2005.05527.x 10. Zanella A, Fermo E, Bianchi P, Valentini G. Red cell pyruvate kinase deficiency: molecular and clinical aspects. Br J Haematol 2005; 130: 11-25. (Pubitemid 40979128)
11. Hay SI, Guerra CA, Tatem AJ, Noor AM, Snow RW The global distribution and population at risk of malaria: past, present and future. Lancet Infect Dis 2004; 4:327-336
12. Mohrenweiser HW Functional hemizygosity in the human genome: direct estimate from twelve erythrocyte enzyme loci. Hum Genet 1987;77:241-245
13. Warburg O, Christian W. Isolierung und Kristillisation des Garungsferments Enolase. Biochem Z 1941; 310:384.
14. Keitt AS. Pyruvate kinase deficiency and related disorders of red cell glycolysis. Am J Med 1966;41:762-785
15. Ayi K, Min-Oo G, Serghides L et al. Pyruvate kinase deficiency and malaria. N Engl J Med 2008;358:1805-1810
16. Durand P.M. Coetzer T.L. Pyruvate kinase deficiency protects against malaria in humans Haematologica 2008 93 6 939-940 http://www.haematologica.org/ cgi/reprint/93/6/939 DOI 10.3324/haematol.12450 16. Durand PM, Coetzer TL. Pyruvate kinase deficiency protects against malaria in human. Haematologica 2008; 93:939-940 (Pubitemid 351821735)
17. Oka H, Tabara A, Fujisawa K, et al. Babesia rodhaini: the protective effect of pyruvate kinase in mice. Exp Parasitol 2008; 120:290-294
18. Morse EF, Jilani F, Brassel J. Acquired pyruvate kinase deficiency. Ann Clin Lab Sci 1977;7:399-404
19. Smilkstein M. Sriwilaijaroen N. Kelly J.X. Wilairat P. Riscoe M. Simple and Inexpensive Fluorescence-Based Technique for High-Throughput Antimalarial Drug Screening Antimicrobial Agents and Chemotherapy 2004 48 5 1803-1806 DOI 10.1128/AAC.48.5.1803-1806.2004 19. Smilkstein M, Sriwilaijaroen N, Kelly JX, Wilairat P, Riscoe M. Simple and inexpensive fluorescence-based technique for high-throughput antimalarial drug screening. Antimicrob Agents Chemother 2004; 48: 1803-1806 (Pubitemid 38544392)
20. Makler MT, Ries JM, Williams JA, et al. Parasite lactate dehydrogenase as an assay for Plasmodium falciparum drug sensitivity. Am J Trop Med Hyg 1993;48:739-741
21. Makler MT, Hinrichs DJ. Measurement of the lactate dehydrogenase activity of Plasmodium falciparum as an assessment of parasitemia. Am J Trop Med Hyg 1993;48:205-210
22. Trager W, Jensen JB. Human malaria parasites in continuous culture. Science 1976; 193:673-675
23. Rivadeniera EM, Wasserman M, Espinal CT. Separation and concentration of schizonts of Plasmodium falciparum by Percoll gradients. J Protozool 1983;30:367-370
24. Schwarzer E, Turrini F, Ulliers D, Giribaldi G, Ginsburg H, Arese P. Impairment of macrophage functions after ingestion of Plasmodium falciparum-infected erythrocytes or isolated malarial pigment. J Exp Med 1992; 176:1033-1041 (erratum: J Exp Med 1993; 177:following 873).
25. Ayi K, Patel SN, Serghides L, Smith TG, Kain KC. Nonopsonic phagocytosis of erythrocytes infected with ring-stage Plasmodium falciparum. Infect Immun 2005; 73:2559-2569
26. Saliba K.J. Horner H.A. Kirk K. Transport and metabolism of the essential vitamin pantothenic acid in human erythrocytes infected with the malaria parasite Plasmodium falciparum Journal of Biological Chemistry 1998 273 17 10190-10195 DOI 10.1074/jbc.273.17.10190 26. Saliba KJ, Horner HA, Kirk K. Transport and metabolism of the essential vitamin pantothenic acid in human erythrocytes infected with the malaria parasite Plasmodium falciparum. J Biol Chem 1998; 273: 10190-10195 (Pubitemid 28227619)
27. Kanaani J. Ginsburg H. Compartment analysis of ATP in malaria-infected erythrocytes Biochemistry International 1988 17 3 451-459 27. Kanaani J, Ginsburg H. Compartment analysis of ATP in malariainfected erythrocytes. Biochem Int 1988; 17:451-459 (Pubitemid 18236540)
28. Chan M, Sim TS. Functional analysis, overexpression, and kinetic characterization of pyruvate kinase from Plasmodium falciparum. Biochem Biophys Res Commun 2005;326:188-196
29. Ferreira ID, Rosário VE, Cravo PV. Real-time quantitative PCR with SYBR Green I detection for estimating copy numbers of nine drug resistance candidate genes in Plasmodium falciparum. Malar J 2006; 5: 1-6.
30. Zanella A, Bianchi P, Baronciani L, et al. Molecular characterization of PK-LR gene in pyruvate kinase-deficient Italian patients. Blood 1997; 89: 3847-3852
31. Zerez CR, Wong MD, Lachant NA, Tanaka KR. Impaired erythrocyte phosphoribosylpyrophosphate formation in hemolytic anemia due to pyruvate kinase deficiency. Blood 1988; 72:500-506
32. Senok AC, Li K, Nelson EA, Yu LM, Tian LP, Oppenheimer SJ. Invasion and growth of Plasmodium falciparum is inhibited in fractionated thalassaemic erythrocytes. Trans R Soc Trop Med Hyg 1997;91:138-143
33. Kanaani J, Ginsburg H. Metabolic interconnection between the human malarial parasite Plasmodium falciparum and its host erythrocyte: regulation of ATP levels by means of an adenylate translocator and adenylate kinase. J Biol Chem 1989;264:3194-3199
34. Zerez CR, Lachant NA, Tanaka KR. Decreased erythrocyte phosphoribosylpyrophosphate synthetase activity and impaired formation in thalassemia minor: a mechanism for decreased adenine nucleotide content. J Lab Clin Med 1989; 114:43-50.
35. Rangachari K. Beaven G.H. Nash G.B. Clough B. Dluzewski A.R. Myint-Oo Wilson R.J.M. Gratzer W.B. A study of red cell membrane properties in relation to malarial invasion Molecular and Biochemical Parasitology 1989 34 1 63-74 DOI 10.1016/0166-6851(89)90020-0 35. Rangachari K, Beaven GH, Nash GB, et al. A study of red cell membrane properties in relation to malarial invasion. Mol Biochem Parasitol 1989;34:63-74. (Pubitemid 19090338)
36. Min-Oo G. Gros P. Erythrocyte variants and the nature of their malaria protective effect Cellular Microbiology 2005 7 6 753-763 DOI 10.1111/j.1462-5822.2005.00524.x 36. Min-Oo G, Gros P. Erythrocyte variants and the nature of their malaria protective effect. Cell Microbiol 2005; 7:753-763 (Pubitemid 40740372)
37. Valentini G. Chiarelli L.R. Fortin R. Dolzan M. Galizzi A. Abraham D.J. Wang C. Bianchi P. Zanella A. Mattevi A. Structure and function of human erythrocyte pyruvate kinase: Molecular basis of nonspherocytic hemolytic anemia Journal of Biological Chemistry 2002 277 26 23807-23814 DOI 10.1074/jbc. M202107200 37. Valentini G, Chiarelli LR, Fortin R, et al. Structure and function of human erythrocyte pyruvate kinase: molecular basis of nonspherocytic hemolytic anemia. J Biol Chem 2002; 277:23807-23814 (Pubitemid 34952224)
38. Min-Oo G. Fortin A. Tam M.-F. Nante A. Stevenson M.M. Gros P. Pyruvate kinase deficiency in mice protects against malaria Nature Genetics 2003 35 4 357-362 DOI 10.1038/ng1260 38. Min-Oo G, Fortin A, Tam MF, Nantel A, Stevenson MM, Gros P. Pyruvate kinase deficiency in mice protects against malaria. Nat Genet 2003;35:357-362 (Pubitemid 37486919)
39. Durand PM, Coetzer TL. Pyruvate kinase deficiency in a South African kindred caused by a 1529A mutation in the PK-LR gene. S Afr Med J 2008;98:456-457
40. Tomoda A, Lachant NA, Noble NA, Tanaka KR. Inhibition of the pentose phosphate shunt by 2,3-diphosphoglycerate in erythrocyte pyruvate kinase deficiency. Br J Haematol 1983;54:475-484
41. Hoorn RK, Flickweert JP, Staal GE. Purification and properties of enolase of human erythroctyes. Int J Biochem 1974;5:845-852
42. Saralakumari D, Ramakrishna Rao P. Red blood cell glucose metabolism in human chronic fluoride toxicity. Bull Environ Contam Toxicol 1991;47:834-839
43. Roth E Jr. Plasmodium falciparum carbohydrate metabolism: a connection between host cell and parasite. Blood Cells 1990; 16:453-460
44. Dluzewski A.R. Rangachari K. Wilson R.J.M. Gratzer W.B. A cytoplasmic requirement of red cells for invasion by malarial parasites Molecular and Biochemical Parasitology 1983 9 2 145-160 44. Dluzewski AR, Rangachari K, Wilson RT, Gratzer WB. A cytoplamic requirement of red cells for invasion by malarial parasites. Mol Biochem Parasitol 1983;9:145-160 (Pubitemid 14239434)
45. Rangachari K. Beaven G.H. Nash G.B. Clough B. Dluzewski A.R. Myint-Oo Wilson R.J.M. Gratzer W.B. A study of red cell membrane properties in relation to malarial invasion Molecular and Biochemical Parasitology 1989 34 1 63-74 DOI 10.1016/0166-6851(89)90020-0 45. Rangachari K, Beaven GH, Nash GB, et al. A study of red cell membrane properties in relation to malarial invasion. Mol Biochem Parasitol 1989;34:63-74. (Pubitemid 19090338)
46. Micheli V, Simmonds HA. NAD synthesis by erythrocytes in phosphoribosylpyrophosphate synthetase (PRPPs) superactivity. Adv Exp Med Biol 1989;253A:1-17.
47. Dubey ML, Hegde R, Ganguly NK, Mahajan RC. Decreased level of 2,3-diphosphosglycerate and alteration of structural integrity in erythrocytes infected with Plasmodium falciparum in vivo. Mol Cell Biochem 2003;246:137-141
48. Goel VK, Li X, Chen H, Liu SC, Chishti AH, Oh SS. Band 3 is a host receptor binding merozoite surface protein 1 during the Plasmodium falciparum invasion of erythrocytes. Proc Natl Acad Sei USA 2003; 100:5164-5169
49. Che A. Cherry R.J. Bannister L.H. Dluzewski A.R. Aggregation of band 3 in hereditary ovalocytic red blood cell membranes. Electron microscopy and protein rotational diffusion studies Journal of Cell Science 1993 105 3 655-660 49. Che A, Cherry RJ, Bannister LH, Dluzewski AR. Aggregation of band 3 in hereditary ovalocytic red blood cell membranes. Electron microscopy and protein rotational diffusion studies. J Cell Sci 1993; 105: 655-660 (Pubitemid 23243198)
50. Dluzewski AR, Nash GB, Wilson RJ, Reardon DM, Gratzer WB. Invasion of hereditary ovalocytes by Plasmodium falciparum in vitro and it relation to intracellular ATP concentration. MoI Biochem Parasitol 1992;55:1-7.
51. Turrini F, Ginsburg H, Bussolino F, Pescarmona GP, Serra MV, Arese P. Phagocytosis of Plasmodium falciparum-infected human red blood cells by human monocytes: involvement of immune and nonimmune determinants and dependence on parasite developmental stage. Blood 1992;80:801-808