Chloroquine mediates specific proteome oxidative damage across the erythrocytic cycle of resistant Plasmodium falciparum

Free Radical Biology and Medicine

Volumn 44, Issue 12, 2008, Pages 2034-2042

  Radfar, Azar ^a   Diez, Amalia ^a   Bautista, José M ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Chloroquine; Drug resistance; Plasmodium falciparum; Redox proteomics

Indexed keywords

CHLOROQUINE; PROTEOME;

ARTICLE; CONTROLLED STUDY; ERYTHROCYTE; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; ANTIGENS, PROTOZOAN; ANTIMALARIALS; CHLOROQUINE; ERYTHROCYTES; HUMANS; OXIDATION-REDUCTION; PHENYLHYDRAZINES; PLASMODIUM FALCIPARUM; PROTEOME; PROTOZOAN PROTEINS;

EUKARYOTA; PLASMODIUM FALCIPARUM;

EID: 43849112193     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2008.03.010     Document Type: Article

References (77)

1. Breman J.G. The ears of the hippopotamus: manifestations, determinants, and estimates of the malaria burden. Am. J. Trop. Med. Hyg. 64 (2001) 1-11
2. Bozdech Z., Llinas M., Pulliam B.L., Wong E.D., Zhu J., and DeRisi J.L. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 1 (2003) E5
3. Becker K., Tilley L., Vennerstrom J.L., Roberts D., Rogerson S., and Ginsburg H. Oxidative stress in malaria parasite-infected erythrocytes: host-parasite interactions. Int. J. Parasitol. 34 (2004) 163-189
4. Muller S. Redox and antioxidant systems of the malaria parasite Plasmodium falciparum. Mol. Microbiol. 53 (2004) 1291-1305
5. Egan T.J., Combrinck J.M., Egan J., Hearne G.R., Marques H.M., Ntenteni S., Sewell B.T., Smith P.J., Taylor D., van Schalkwyk D.A., and Walden J.C. Fate of haem iron in the malaria parasite Plasmodium falciparum. Biochem. J. 365 (2002) 343-347
6. Zhang J.M., Krugliak M., and Ginsburg H. The fate of ferriprotorphyrin IX in malaria infected erythrocytes in conjunction with the mode of action of antimalarial drugs. Mol. Biochem. Parasitol. 99 (1999) 129-141
7. Ginsburg H., Famin O., Zhang J.M., and Krugliak M. Inhibition of glutathione-dependent degradation of heme by chloroquine and amodiaquine as a possible basis for their antimalarial mode of action. Biochem. Pharmacol. 56 (1998) 1305-1313
8. Harwaldt P., Rahlfs S., and Becker K. Glutathione S-transferase of the malarial parasite Plasmodium falciparum: characterization of a potential drug target. Biol. Chem. 383 (2002) 821-830
9. Campanale N., Nickel C., Daubenberger C.A., Wehlan D.A., Gorman J.J., Klonis N., Becker K., and Tilley L. Identification and characterization of heme-interacting proteins in the malaria parasite, Plasmodium falciparum. J. Biol. Chem. 278 (2003) 27354-27361
10. Loria P., Miller S., Foley M., and Tilley L. Inhibition of the peroxidative degradation of haem as the basis of action of chloroquine and other quinoline antimalarials. Biochem. J. 339 (1999) 363-370
11. Famin O., and Ginsburg H. The treatment of Plasmodium falciparum-infected erythrocytes with chloroquine leads to accumulation of ferriprotoporphyrin IX bound to particular parasite proteins and to the inhibition of the parasite's 6-phosphogluconate dehydrogenase. Parasite 10 (2003) 39-50
12. Koncarevic S., Bogumil R., and Becker K. SELDI-TOF-MS analysis of chloroquine resistant and sensitive Plasmodium falciparum strains. Proteomics 7 (2007) 711-721
13. Butterfield D.A., Reed T., Newman S.F., and Sultana R. Roles of amyloid beta-peptide-associated oxidative stress and brain protein modifications in the pathogenesis of Alzheimer's disease and mild cognitive impairment. Free Radic. Biol. Med. 43 (2007) 658-677
14. Stadtman E.R., and Levine R.L. Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 25 (2003) 207-218
15. Oliver C.N., Ahn B.W., Moerman E.J., Goldstein S., and Stadtman E.R. Age-Related-Changes in Oxidized Proteins. J. Biol. Chem. 262 (1987) 5488-5491
16. Stadtman E.R. Protein oxidation and aging. Science 257 (1992) 1220-1224
17. Beckman K.B., and Ames B.N. The free radical theory of aging matures. Physiol. Rev. 78 (1998) 547-581
18. Ehrhardt S., Eggelte T.A., Kaiser S., Adjei L., Burchard G.D., Anemana S.D., Bienzle U., and Mockenhaupt F.P. Large-scale surveillance of Plasmodium falciparum crt(K76T) in northern Ghana. Antimicrob. Agents Chemother. 51 (2007) 3407-3409
19. Rosario V.E. Genetics of chloroquine resistance in malaria parasites. Nature 261 (1976) 585-586
20. Quashie N.B., de Koning H.P., and Ranford-Cartwright L.C. An improved and highly sensitive microfluorimetric method for assessing susceptibility of Plasmodium falciparum to antimalarial drugs in vitro. Malar. J. 5 (2006) 95
21. Akoachere M., Buchholz K., Fischer E., Burhenne J., Haefeli W.E., Schirmer R.H., and Becker K. In vitro assessment of methylene blue on chloroquine-sensitive and -resistant Plasmodium falciparum strains reveals synergistic action with artemisinins. Antimicrob. Agents Chemother. 49 (2005) 4592-4597
22. Levine R.L., Williams J.A., Stadtman E.R., and Shacter E. Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol. 233 (1994) 346-357
23. Shacter E., Williams J.A., Lim M., and Levine R.L. Differential susceptibility of plasma-proteins to oxidative modification - examination by Western-blot immunoassay. Free Radic. Biol. Med. 17 (1994) 429-437
24. Trager W., and Jensen J.B. Human malaria parasites in continuous culture. Science 193 (1976) 673-675
25. Lambros C., and Vanderberg J.P. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 65 (1979) 418-420
26. Peck S.C., Nuhse T.S., Hess D., Iglesias A., Meins F., and Boller T. Directed proteomics identifies a plant-specific protein rapidly phosphorylated in response to bacterial and fungal elicitors. Plant Cell 13 (2001) 1467-1475
27. Neuhoff V., Stamm R., and Eibl H. Clear background and highly sensitive protein staining with Coomassie blue dyes in polyacrylamide gels-a systematic analysis. Electrophoresis 6 (1985) 427-448
28. Shevchenko A., Wilm M., Vorm O., and Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68 (1996) 850-858
29. Cabiscol E., Piulats E., Echave P., Herrero E., and Ros J. Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae. J. Biol. Chem. 275 (2000) 27393-27398
30. Castegna A., Aksenov M., Aksenova M., Thongboonkerd V., Klein J.B., Pierce W.M., Booze R., Markesbery W.R., and Butterfield D.A. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part 1: creatine kinase bb, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1. Free Radic. Biol. Med. 33 (2002) 562-571
31. Butterfield D.A. Proteomics: a new approach to investigate oxidative stress in Alzheimer's disease brain. Brain Res. 1000 (2004) 1-7
32. Poon H.F., Castegna A., Farr S.A., Thongboonkerd V., Lynn B.C., Banks W.A., Morley J.E., Klein J.B., and Butterfield D.A. Quantitative proteomics analysis of specific protein expression and oxidative modification in aged senescence-accelerated-prone 8 mice brain. Neuroscience 126 (2004) 915-926
33. Reverter-Branchat G., Cabiscol E., Tamarit J., and Ros J. Oxidative damage to specific proteins in replicative and chronological-aged Saccharomyces cerevisiae-common targets and prevention by calorie restriction. J. Biol. Chem. 279 (2004) 31983-31989
34. Ruepp A., Zollner A., Maier D., Albermann K., Hani J., Mokrejs M., Tetko I., Guldener U., Mannhaupt G., Munsterkotter M., and Mewes H.W. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res. 32 (2004) 5539-5545
35. Florens L., Washburn M.P., Raine J.D., Anthony R.M., Grainger M., Haynes J.D., Moch J.K., Muster N., Sacci J.B., Tabb D.L., Witney A.A., Wolters D., Wu Y.M., Gardner M.J., Holder A.A., Sinden R.E., Yates J.R., and Carucci D.J. A proteomic view of the Plasmodium falciparum life cycle. Nature 419 (2002) 520-526
36. Crooke A., Diez A., Mason P.J., and Bautista J.M. Transient silencing of Plasmodium falciparum bifunctional glucose-6-phosphate dehydrogenase-6-phosphogluconolactonase. FEBS J. 273 (2006) 1537-1546
37. Poon H.F., Hensley K., Thongboonkerd V., Merchant M.L., Lynn B.C., Pierce W.M., Klein J.B., Calabrese V., and Butterfield D.A. Redox proteomics analysis of oxidatively modified proteins in G93A-SOD1 transgenic mice-a model of familial amyotrophic lateral sclerosis. Free Radic. Biol. Med. 39 (2005) 453-462
38. Sultana R., Perluigi M., and Butterfield D.A. Redox proteomics identification of oxidatively modified proteins in Alzheimer's disease brain and in vivo and in vitro models of AD centered around Abeta(1-42). J. Chromatogr., B, Analyt. Technol. Biomed. Life Sci. 833 (2006) 3-11
39. Singh N.R., Rondeau P., Hoareau L., and Bourdon E. Identification of preferential protein targets for carbonylation in human mature adipocytes treated with native or glycated albumin. Free Radic. Res. 41 (2007) 1078-1088
40. Egan T.J., Hunter R., Kaschula C.H., Marques H.M., Misplon A., and Walden J. Structure-function relationships in aminoquinolines: effect of amino and chloro groups on quinoline-hematin complex formation, inhibition of beta-hematin formation, and antiplasmodial activity. J. Med. Chem. 43 (2000) 283-291
41. Egan T.J., and Ncokazi K.K. Quinoline antimalarials decrease the rate of beta-hematin formation. J. Inorg. Biochem. 99 (2005) 1532-1539
42. Arese P., and Schwarzer E. Malarial pigment (haemozoin): a very active 'inert' substance. Ann. Trop. Med. Parasitol. 91 (1997) 501-516
43. Skorokhod A., Schwarzer E., Gremo G., and Arese P. HNE produced by the malaria parasite Plasmodium falciparum generates HNE-protein adducts and decreases erythrocyte deformability. Redox Rep. 12 (2007) 73-75
44. England K., O'Driscoll C., and Cotter T.G. Carbonylation of glycolytic proteins is a key response to drug-induced oxidative stress and apoptosis. Cell Death Differ. 11 (2004) 252-260
45. Ishii T., Sakurai T., Usami H., and Uchida K. Oxidative modification of proteasome: Identification of an oxidation-sensitive subunit in 26 S proteasome. Biochemistry 44 (2005) 13893-13901
46. Dalle-Donne I., Aldini G., Carini M., Colombo R., Rossi R., and Milzani A. Protein carbonylation, cellular dysfunction, and disease progression. J. Cell. Mol. Med. 10 (2006) 389-406
47. Nirmalan N., Sims P.F., and Hyde J.E. Quantitative proteomics of the human malaria parasite Plasmodium falciparum and its application to studies of development and inhibition. Mol. Microbiol. 52 (2004) 1187-1199
48. Uchida K., Hasui Y., and Osawa T. Covalent attachment of 4-hydroxy-2-nonenal to erythrocyte proteins. J. Biochem. (Tokyo) 122 (1997) 1246-1251
49. Ozensoy O., Arslan O., and Sinan S.O. A new method for purification of carbonic anhydrase isozymes by affinity chromatography. Biochemistry (Moscow) 69 (2004) 216-219
50. Raisanen S.R., Lehenkari P., Tasanen M., Rahkila P., Harkonen P.L., and Vaananen H.K. Carbonic anhydrase III protects cells from hydrogen peroxide-induced apoptosis. FASEB J. 13 (1999) 513-522
51. Barreiro E., Gea J., Matar G., and Hussain S.N. Expression and carbonylation of creatine kinase in the quadriceps femoris muscles of patients with chronic obstructive pulmonary disease. Am. J. Respir. Cell Mol. Biol. 33 (2005) 636-642
52. Cappadoro M., Giribaldi G., O'Brien E., Turrini F., Mannu F., Ulliers D., Simula G., Luzzatto L., and Arese P. Early phagocytosis of glucose-6-phosphate dehydrogenase (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency. Blood 92 (1998) 2527-2534
53. Nickel C., Rahlfs S., Deponte M., Koncarevic S., and Becker K. Thioredoxin networks in the malarial parasite Plasmodium falciparum. Antioxid. Redox Signal. 8 (2006) 1227-1239
54. Atamna H., Pascarmona G., and Ginsburg H. Hexose-monophosphate shunt activity in intact Plasmodium falciparum-infected erythrocytes and in free parasites. Mol. Biochem. Parasitol. 67 (1994) 79-89
55. Fairfield A.S., Abosch A., Ranz A., Eaton J.W., and Meshnick S.R. Oxidant defense enzymes of Plasmodium falciparum. Mol. Biochem. Parasitol. 30 (1988) 77-82
56. Tilley L., Loria P., and Foley M. Chloroquine and other quinoline antimalarials. In: Rosenthal P.J. (Ed). Antimalarial chemotherapy: mechanisms of action, resistance and new directions in drug discovery (2001), Humana Press, Totowa, NJ 87-122
57. Parsell D.A., and Lindquist S. Heat shock proteins and stress tolerance. In: Morimoto R.I., Tissieres A., and Georgeopoulus C. (Eds). The biology of heat shock proteins and molecular chaperones (1994), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 457-494
58. Banumathy G., Singh V., Pavithra S.R., and Tatu U. Heat shock protein 90 function is essential for Plasmodium falciparum growth in human erythrocytes. J. Biol. Chem. 278 (2003) 18336-18345
59. Kumar R., Musiyenko A., and Barik S. The heat shock protein 90 of Plasmodium falciparum and antimalarial activity of its inhibitor, geldanamycin. Malar. J. 2 (2003) 1-11
60. Yayon A., Vande Waa J.A., Yayon M., Geary T.G., and Jensen J.B. Stage-dependent effects of chloroquine on Plasmodium falciparum in vitro. J. Protozool. 30 (1983) 642-647
61. Berke S.J., and Paulson H.L. Protein aggregation and the ubiquitin proteasome pathway: gaining the UPPer hand on neurodegeneration. Curr. Opin. Genet. Dev. 13 (2003) 253-261
62. Ponnappan S., Ovaa H., and Ponnappan U. Lower expression of catalytic and structural subunits of the proteasome contributes to decreased proteolysis in peripheral blood T lymphocytes during aging. Int. J. Biochem. Cell Biol. 39 (2007) 799-809
63. Bulteau A.L., Moreau M., Nizard C., and Friguet B. Impairment of proteasome function upon UVA- and UVB-irradiation of human keratinocytes. Free Radic. Biol. Med. 32 (2002) 1157-1170
64. Hunt P., Afonso A., Creasey A., Culleton R., Sidhu A.B., Logan J., Valderramos S.G., McNae I., Cheesman S., do Rosario V., Carter R., Fidock D.A., and Cravo P. Gene encoding a deubiquitinating enzyme is mutated in artesunate- and chloroquine-resistant rodent malaria parasites. Mol. Microbiol. 65 (2007) 27-40
65. Certad G., Abrahem A., and Georges E. Cloning and partial characterization of the proteasome S4 ATPase from Plasmodium falciparum. Exp. Parasitol. 93 (1999) 123-131
66. Allary M., Schrevel J., and Florent I. Properties, stage-dependent expression and localization of Plasmodium falciparum M1 family zinc-aminopeptidase. Parasitology 125 (2002) 1-10
67. Flipo M., Florent I., Grellier P., Sergheraert C., and Deprez-Poulain R. Design, synthesis and antimalarial activity of novel, quinoline-based, zinc metallo-aminopeptidase inhibitors. Bioorg. Med. Chem. Lett. 13 (2003) 2659-2662
68. Orjih A.U., Ryerse J.S., and Fitch C.D. Hemoglobin catabolism and the killing of intraerythrocytic Plasmodium falciparum by chloroquine. Experientia 50 (1994) 34-39
69. Vander Jagt D.L., Baack B.R., and Hunsaker L.A. Purification and characterization of an aminopeptidase from Plasmodium falciparum. Mol. Biochem. Parasitol. 10 (1984) 45-54
70. Lang-Unnasch N., and Murphy A.D. Metabolic changes of the malaria parasite during the transition from the human to the mosquito host. Annu. Rev. Microbiol. 52 (1998) 561-590
71. Mehta M., Sonawat H.M., and Sharma S. Malaria parasite-infected erythrocytes inhibit glucose utilization in uninfected red cells. FEBS Lett. 579 (2005) 6151-6158
72. Roth E.F., Calvin M.C., Maxaudit I., Rosa J., and Rosa R. The enzymes of the glycolytic pathway in erythrocytes infected with plasmodium-falciparum malaria parasites. Blood 72 (1988) 1922-1925
73. Fried M., and Duffy P.E. Two DBLgamma subtypes are commonly expressed by placental isolates of Plasmodium falciparum. Mol. Biochem. Parasitol. 122 (2002) 201-210
74. Rowe J.A., Kyes S.A., Rogerson S.J., Babiker H.A., and Raza A. Identification of a conserved Plasmodium falciparum var gene implicated in malaria in pregnancy. J. Infect. Dis. 185 (2002) 1207-1211
75. Howard R.J., and Gilladoga A.D. Molecular studies related to the pathogenesis of cerebral malaria. Blood 74 (1989) 2603-2618
76. Kirchgatter K., and Del Portillo H.A. Clinical and molecular aspects of severe malaria. An. Acad. Bras. Cienc. 77 (2005) 455-475
77. McDermott J.M., Heymann D.L., Wirima J.J., Macheso A.P., Wahl R.D., Steketee R.W., and Campbell C.C. Efficacy of chemoprophylaxis in preventing Plasmodium falciparum parasitemia and placental infection in pregnant women in Malawi. Trans. R. Soc. Trop. Med. Hyg. 82 (1988) 520-523