Protein disulfide isomerase assisted protein folding in malaria parasites

International Journal for Parasitology

Volumn 36, Issue 9, 2006, Pages 1037-1048

  Mahajan, B ^a   Noiva, R ^b   Yadava, A ^c   Zheng, H ^a   Majam, V ^a   Mohan, K V Krishna ^a   Moch, J K ^c   Haynes, J D ^c   Nakhasi, H ^a   Kumar, S ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^b UNIVERSITY OF SOUTH DAKOTA   (United States)

^c WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

Author keywords

EBA 175; Folding; Plasmodium falciparum; Protein disulfide isomerase

Indexed keywords

AMINO ACID; DISULFIDE; ISOMERASE; MALARIA VACCINE; PROTEIN PFPDI11; PROTEIN PFPDI14; PROTEIN PFPDI8; PROTEIN PFPDI9; PROTOZOAL PROTEIN; RECOMBINANT VACCINE; THIOREDOXIN; UNCLASSIFIED DRUG;

ENZYME; EUKARYOTE; GENETIC ANALYSIS; LIFE CYCLE; MALARIA; PARASITE; PHYLOGENETICS; PROTOZOAN;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; CHEMICAL ANALYSIS; CHROMOSOME; CONFORMATION; CONTROLLED STUDY; DRUG TARGETING; ENDOPLASMIC RETICULUM; FEMALE; GENE ISOLATION; GENE SEQUENCE; LIFE CYCLE; MOLECULE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLASMODIUM; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PLASMODIUM KNOWLESI; PLASMODIUM VIVAX; PLASMODIUM YOELII; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTOZOAL GENETICS; SIGNAL TRANSDUCTION; SPECIES DIFFERENTIATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, PROTOZOAN; CLONING, MOLECULAR; GENES, PROTOZOAN; GENOME; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLASMODIUM; PLASMODIUM FALCIPARUM; PROTEIN DISULFIDE-ISOMERASE; PROTEIN DISULFIDE-ISOMERASES; PROTEIN FOLDING; PROTOZOAN PROTEINS; RECOMBINANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT;

EUKARYOTA; MURINAE; PLASMODIUM (APICOMPLEXA); PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PLASMODIUM KNOWLESI; PLASMODIUM VIVAX; PLASMODIUM YOELII; SIMIAE;

EID: 33746315951     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2006.04.012     Document Type: Article

References (52)

1. Anfinsen C.B., Haber E., Sela M., and White Jr. F.H. The kinetics of formation of native ribonuclease during oxidation of the reduced polypeptide chain. Proc. Natl Acad. Sci. USA 47 (1961) 1309-1314
2. Baruch D.I., Gamain B., Barnwell J.W., Sullivan J.S., Stowers A., Galland G.G., Miller L.H., and Collins W.E. Immunization of Aotus monkeys with a functional domain of the Plasmodium falciparum variant antigen induces protection against a lethal parasite line. Proc. Natl Acad. Sci. USA 99 (2002) 3860-3865
3. 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
4. Breman J.G., Egan A., and Keusch G.T. The intolerable burden of malaria: a new look at the numbers. Am. J. Trop. Med. Hyg. 64 (2001) iv-vii
5. Buchner J. Supervising the fold: functional principles of molecular chaperones. Fed. Am. Soc. Exp. Biol. J. 10 (1996) 10-19
6. Carvalho A.P., Fernandes P.A., and Ramos M.J. Similarities and differences in the thioredoxin superfamily. Prog. Biophys. Mol. Biol. (2005) (Epub ahead of print)
7. Creighton T.E., Bagley C.J., Cooper L., Darby N.J., Freedman R.B., Kemmink J., and Sheikh A. On the biosynthesis of bovine pancreatic trypsin inhibitor (BPTI). Structure, processing, folding and disulphide bond formation of the precursor in vitro and in microsomes. J. Mol. Biol. 232 (1993) 1176-1196
8. Debarbieux L., and Beckwith J. Electron avenue: pathways of disulfide bond formation and isomerization. Cell 99 (1999) 117-119
9. Dutta S., Lalitha P.V., Ware L.A., Barbosa A., Moch J.K., Vassell M.A., Fileta B.B., Kitov S., Kolodny N., Heppner D.G., Haynes J.D., and Lanar D.E. Purification, characterization, and immunogenicity of the refolded ectodomain of the Plasmodium falciparum apical membrane antigen 1 expressed in Escherichia coli. Infect. Immun. 70 (2002) 3101-3110
10. Edman J.C., Ellis L., Blacher R.W., Roth R.A., and Rutter W.J. Sequence of protein disulphide isomerase and implications of its relationship to thioredoxin. Nature 317 (1985) 267-270
11. Ellgaard L., and Ruddock L.W. The human protein disulphide isomerase family: substrate interactions and functional properties. Eur. Mol. Biol. Org. Rep. 6 (2005) 28-32
12. Florent I., and Mouray E. Cloning of Plasmodium falciparum protein disulfide isomerase homologue by affinity purification using the antiplasmodial inhibitor 1,4-bis[3-[N-(cyclohexyl methyl)amino]propyl]piperazine. Fed. Eur. Biochem. Soc. Lett. 484 (2000) 246-252
13. Frand A.R., and Kaiser C.A. The Ero1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol. Cell 1 (1998) 161-170
14. Frand A.R., and Kaiser C.A. Ero1p oxidizes protein disulfide isomerase in a pathway for disulfide bond formation in the endoplasmic reticulum. Mol. Cell 4 (1999) 469-477
15. Frand A.R., Cuozzo J.W., and Kaiser C.A. Pathways for protein disulphide bond formation. Trends Cell Biol. 10 (2000) 203-210
16. Freedman R.B., Hirst T.R., and Tuite M.F. Protein disulphide isomerase: building bridges in protein folding. Trends Biochem. Sci. 19 (1994) 331-336
17. Gess B., Hofbauer K.H., Wenger R.H., Lohaus C., Meyer H.E., and Kurtz A. The cellular oxygen tension regulates expression of the endoplasmic oxidoreductase ERO1-Lalpha. Eur. J. Biochem. 270 (2003) 2228-2235
18. Gross E., Kastner D.B., Kaiser C.A., and Fass D. Structure of Ero1p, source of disulfide bonds for oxidative protein folding in the cell. Cell 117 (2004) 601-610
19. Guevara Patino J.A., Holder A.A., McBride J.S., and Blackman M.J. Antibodies that inhibit malaria merozoite surface protein-1 processing and erythrocyte invasion are blocked by naturally acquired human antibodies. J. Exp. Med. 186 (1997) 1689-1699
20. Hartl F.U., and Hayer-Hartl M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295 (2002) 1852-1858
21. Hawkins H.C., Blackburn E.C., and Freedman R.B. Comparison of the activities of protein disulphide-isomerase and thioredoxin in catalysing disulphide isomerization in a protein substrate. Biochem. J. 275 Pt 2 (1991) 349-353
22. Haynes J.D., and Moch J.K. Automated synchronization of Plasmodium falciparum parasites by culture in a temperature-cycling incubator. Methods Mol. Med. 72 (2002) 489-497
23. Hiniker A., and Bardwell J.C. Disulfide relays between and within proteins: the Ero1p structure. Trends Biochem. Sci. 29 (2004) 516-519
24. Hodder A.N., Crewther P.E., Matthew M.L., Reid G.E., Moritz R.L., Simpson R.J., and Anders R.F. The disulfide bond structure of Plasmodium apical membrane antigen-1. J. Biol. Chem. 271 (1996) 29446-29452
25. Kimura T., Hosoda Y., Sato Y., Kitamura Y., Ikeda T., Horibe T., and Kikuchi M. Interactions among yeast protein-disulfide isomerase proteins and endoplasmic reticulum chaperone proteins influence their activities. J. Biol. Chem. 280 (2005) 31438-31441
26. Knodler L.A., Noiva R., Mehta K., McCaffery J.M., Aley S.B., Svard S.G., Nystul T.G., Reiner D.S., Silberman J.D., and Gillin F.D. Novel protein-disulfide isomerases from the early-diverging protist Giardia lamblia. J. Biol. Chem. 274 (1999) 29805-29811
27. Lambert N., and Freedman R.B. Kinetics and specificity of homogeneous protein disulphide-isomerase in protein disulphide isomerization and in thiol-protein-disulphide oxidoreduction. Biochem. J. 213 (1983) 235-243
28. Le Roch K.G., Zhou Y., Blair P.L., Grainger M., Moch J.K., Haynes J.D., De La Vega P., Holder A.A., Batalov S., Carucci D.J., and Winzeler E.A. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301 (2003) 1503-1508
29. Liang H., Narum D.L., Fuhrmann S.R., Luu T., and Sim B.K. A recombinant baculovirus-expressed Plasmodium falciparum receptor-binding domain of erythrocyte binding protein EBA-175 biologically mimics native protein. Infect. Immun. 68 (2000) 3564-3568
30. Liu Y., Zhao T.J., Yan Y.B., and Zhou H.M. Increase of soluble expression in Escherichia coli cytoplasm by a protein disulfide isomerase gene fusion system. Protein Expr. Purif. 44 (2005) 155-161
31. McArthur A.G., Knodler L.A., Silberman J.D., Davids B.J., Gillin F.D., and Sogin M.L. The evolutionary origins of eukaryotic protein disulfide isomerase domains: new evidence from the Amitochondriate protist Giardia lamblia. Mol. Biol. Evol. 18 (2001) 1455-1463
32. Miller L.H., Baruch D.I., Marsh K., and Doumbo O.K. The pathogenic basis of malaria. Nature 415 (2002) 673-679
33. Missiakas D., and Raina S. Protein folding in the bacterial periplasm. J. Bacteriol. 179 (1997) 2465-2471
34. Norgaard P., and Winther J.R. Mutation of yeast Eug1p CXXS active sites to CXXC results in a dramatic increase in protein disulphide isomerase activity. Biochem. J. 358 (2001) 269-274
35. Norgaard P., Westphal V., Tachibana C., Alsoe L., Holst B., and Winther J.R. Functional differences in yeast protein disulfide isomerases. J. Cell Biol. 152 (2001) 553-562
36. Padilla A., Noiva R., Lee N., Mohan K.V., Nakhasi H.L., and Debrabant A. An atypical protein disulfide isomerase from the protozoan parasite Leishmania containing a single thioredoxin-like domain. J. Biol. Chem. 278 (2003) 1872-1878
37. Pagani M., Fabbri M., Benedetti C., Fassio A., Pilati S., Bulleid N.J., Cabibbo A., and Sitia R. Endoplasmic reticulum oxidoreductin 1-lbeta (ERO1-Lbeta), a human gene induced in the course of the unfolded protein response. J. Biol. Chem. 275 (2000) 23685-23692
38. Pollard M.G., Travers K.J., and Weissman J.S. Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol. Cell 1 (1998) 171-182
39. Rubotham J., Woods K., Garcia-Salcedo J.A., Pays E., and Nolan D.P. Characterization of two protein disulfide isomerases from the endocytic pathway of bloodstream forms of Trypanosoma brucei. J. Biol. Chem. 280 (2005) 10410-10418
40. Sevier C.S., and Kaiser C.A. Formation and transfer of disulphide bonds in living cells. Nat. Rev. Mol. Cell Biol. 3 (2002) 836-847
41. Singh S., Kennedy M.C., Long C.A., Saul A.J., Miller L.H., and Stowers A.W. Biochemical and immunological characterization of bacterially expressed and refolded Plasmodium falciparum 42-kilodalton C-terminal merozoite surface protein 1. Infect. Immun. 71 (2003) 6766-6774
42. Su X.Z., Heatwole V.M., Wertheimer S.P., Guinet F., Herrfeldt J.A., Peterson D.S., Ravetch J.A., and Wellems T.E. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 82 (1995) 89-100
43. Templeton T.J., and Kaslow D.C. Identification of additional members define a Plasmodium falciparum gene superfamily which includes Pfs48/45 and Pfs230. Mol. Biochem. Parasitol. 101 (1999) 223-227
44. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids. Res. 22 (1994) 4673-4680
45. Tian G., Xiang S., Noiva R., Lennarz W.J., and Schindelin H. The crystal structure of yeast protein disulfide isomerase suggests cooperativity between its active sites. Cell 124 (2006) 61-73
46. Tolia N.H., Enemark E.J., Sim B.K., and Joshua-Tor L. Structural basis for the EBA-175 erythrocyte invasion pathway of the malaria parasite Plasmodium falciparum. Cell 122 (2005) 183-193
47. Tsai C.W., Duggan P.F., Shimp Jr. R.L., Miller L.H., and Narum D.L. Overproduction of Pichia pastoris or Plasmodium falciparum protein disulfide isomerase affects expression, folding and O-linked glycosylation of a malaria vaccine candidate expressed in P. pastoris. J. Biotechnol. 121 (2006) 458-470
48. Tu B.P., and Weissman J.S. The FAD- and O(2)-dependent reaction cycle of Ero1-mediated oxidative protein folding in the endoplasmic reticulum. Mol. Cell 10 (2002) 983-994
49. Vad R., Nafstad E., Dahl L.A., and Gabrielsen O.S. Engineering of a Pichia pastoris expression system for secretion of high amounts of intact human parathyroid hormone. J. Biotechnol. 116 (2005) 251-260
50. Wilkinson B., and Gilbert H.F. Protein disulfide isomerase. Biochim. Biophys. Acta 1699 (2004) 35-44
51. Yadava A., and Ockenhouse C.F. Effect of codon optimization on expression levels of a functionally folded malaria vaccine candidate in prokaryotic and eukaryotic expression systems. Infect. Immun. 71 (2003) 4961-4969
52. Zhan X., Schwaller M., Gilbert H.F., and Georgiou G. Facilitating the formation of disulfide bonds in the Escherichia coli periplasm via coexpression of yeast protein disulfide isomerase. Biotechnol. Prog. 15 (1999) 1033-1038