Plasmodium falciparum encodes a single cytosolic type i Hsp40 that functionally interacts with Hsp70 and is upregulated by heat shock

Cell Stress and Chaperones

Volumn 16, Issue 4, 2011, Pages 389-401

  Botha, Melissa ^a   Chiang, Annette N ^b   Needham, Patrick B ^b   Stephens, Linda L ^a   Hoppe, Heinrich C ^c   Külzer, Simone ^d   Przyborski, Jude M ^d   Lingelbach, Klaus ^d   Wipf, Peter ^b   Brodsky, Jeffrey L ^b   Shonhai, Addmore ^e   Blatch, Gregory L ^a  

^a RHODES UNIVERSITY   (South Africa)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c DSI CSIR Nanotechnology Innovation Centre   (South Africa)

^d PHILIPPS UNIVERSITY MARBURG   (Germany)

^e UNIVERSITY OF ZULULAND   (South Africa)

Author keywords

Aggregation; ATPase; Codon harmonization; Heat shock protein; Malaria; Molecular chaperone

Indexed keywords

ADENOSINE TRIPHOSPHATE; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 70; RECOMBINANT PROTEIN;

ARTICLE; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVITY; ERYTHROCYTE; HEAT SHOCK; HYDROLYSIS; IMMUNOFLUORESCENCE MICROSCOPY; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; UPREGULATION;

ADENOSINE TRIPHOSPHATASES; CYTOSOL; GENE EXPRESSION; HEAT-SHOCK RESPONSE; HSP40 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HYDROLYSIS; MOLECULAR CHAPERONES; PLASMODIUM FALCIPARUM; UP-REGULATION;

PLASMODIUM FALCIPARUM;

EID: 79956289943     PISSN: 13558145     EISSN: 14661268     Source Type: Journal    
DOI: 10.1007/s12192-010-0250-6     Document Type: Article

References (56)

1. Acharya P, Kumar R, Tatu U (2007) Chaperoning a cellular upheaval in malaria: heat shock proteins in Plasmodium falciparum. Mol Biochem Parasitol 153:85-94 (Pubitemid 46654240)
2. Akide-Ndunge OB, Tambini E, Giribaldi G, McMillan PJ, Müller S, Arese P, Turrini F (2009) Co-ordinated stage-dependent enhancement of Plasmodium falciparum antioxidant enzymes and heat shock protein expression in parasites growing in oxidatively stressed or G6PD-deficient red blood cells. Malar J 8:113
3. Angov E, Hiller CJ, Kincad R, Lyon JA (2008) Heterologous protein expression is enhanced by harmonizing the codon usage frequencies of the target gene with those of the expression host. PLoS ONE 3:e2189
4. Botha M, Pesce E-R, Blatch GL (2007) The Hsp40 proteins of Plasmodium falciparum: regulating chaperone power in the parasite and the host. Int J Biochem Cell Biol 39:1781-1803 (Pubitemid 47321340)
5. Brodsky JL, Bracher A (2007) Nucleotide exchange factors for Hsp70 molecular chaperones. In: Blatch GL (ed) Networking of chaperones by co-chaperones. Austin: Landes Bioscience; New York: Springer Science+Business Media; 26-37
6. Cheetham ME, Caplan AJ (1998) Structure, function and evolution of DnaJ: conservation and adaptation of chaperone function. Cell Stress Chaperones 3:28-36 (Pubitemid 28159676)
7. Cheetham ME, Jackson AP, Anderton BH (1994) Regulation of 70- kDa heat-shock-protein ATPase activity and substrate binding by human DnaJ-like proteins, HSJ1a and HSJ1b. Eur J Biochem 226:99-107 (Pubitemid 24348673)
8. Chiang AN, Valderramos JC, Balachandran R, Chovatiya RJ, Mead BP, Schneider C, Bell SL, Klein MG, Huryn DM, Chen XS, Day BW, Fidock DA, Wipf P, Brodsky JL (2009) Select pyrimidinones inhibit the propagation of the malarial parasite, Plasmodium falciparum. Bioorg Med Chem 17:1527-1533
9. Crabb BS, Cooke BM, Reeder JC, Waller RF, Caruana SR, Davern KM, Wickham ME, Brown GV, Coppel RL, Cowman AF (1997), Targeted gene disruption shows that knobs enable malariainfected red cells to cytoadhere under physiological shear stress. Cell 89:287-296 (Pubitemid 27199900)
10. de Koning-Ward TF, Gilson PR, Boddey JA, Rug M, Smith BJ, Papenfuss AT, Sanders PR, Lundie RJ, Maier AG, Cowman AF, Crabb BS (2009) A newly discovered protein export machine in malaria parasites. Nature 459:945-949
11. Famin O, Ginsburg H (2003) 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 10:39-50 (Pubitemid 37363201)
12. Fewell SW, Smith CM, Lyon MA, Dumitrescu TP, Wipf P, Day B, Brodsky JL (2004) Small molecule modulators of endogenous and co-chaperone-stimulated Hsp70 ATPase activity. J Biol Chem 279:51131-51140 (Pubitemid 40017855)
13. Flaherty KM, DeLuca-Flaherty C, McKay DB (1990) Threedimensional structure of the ATPase fragment of a 70-K heat shock cognate protein. Nature 346:623-628
14. Guiguemde WA, Anang A, Shelat AA et al (2010) Chemical genetics of Plasmodium facliparum. Nature 465:311-315
15. Hennessy F, Nicoll WS, Zimmermann R, Cheetham ME, Blatch GL (2005) Not all J domains are created equal: implications for the specificity of Hsp40-Hsp70 interactions. Protein Sci 14:1697-1709 (Pubitemid 41001413)
16. Hiller NL, Bhattacharjee S, van Ooij C, Liolios K, Harrison T, Lopez- Estrano C, Haldar K (2004) A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306:1934-1937 (Pubitemid 39627857)
17. Jiang J, Maes EG, Taylor AB, Wang L, Hinck AP, Lafer EM, Sousa R (2007) Structural basis of the J cochaperone binding and regulation of Hsp70. Mol Cell 28:1-12
18. Kabani M, Martineau CN (2008) Multiple Hsp70 isoforms in the eukaryotic cytosol: mere redundancy or functional specificity? Curr Genomics 9:338-348
19. Kappes B, Suetterlin BW, Hofer-Warbinek R, Humar R, Franklin RM (1993) Two major phosphoproteins of Plasmodium falciparum are heat shock proteins. Mol Biochem Parasitol 59:83-94
20. Külzer S, Rug M, Brinkman K, Cannon P, Cowman A, Lingelbach K, Blatch GL, Maier AG, Przyborski JM (2010) Parasite encoded Hsp40 proteins define novel mobile structures in the cytosol of the P. falciparum infected erythrocyte. Cell Microbiol 12:1398-1420
21. Kumar N, Koski G, Harada M, Aikawa M, Zheng H (1991) Induction and localization of Plasmodium falciparum stress proteins related to the heat shock protein 70 family. Mol Biochem Parasitol 48:47-58
22. Kumar A, Tanveer A, Biswas S, Ram EVSR, Gupta A, Kumar B, Habib S (2010) Nuclear-encoded DnaJ homologue of Plasmodium falciparum interacts with replication ori of the apicoplast genome. Mol Microbiol 75:942-956
23. Lambros C, Vandeberg JP1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65:418-420 (Pubitemid 10222999)
24. Landry SJ (2003) Structure and energetics of an allele-specific genetic interaction between dnaJ and dnaK: correlation of nuclear magnetic resonance chemical shift perturbations in the J-domain of Hsp40/DnaJ with binding affinity for the ATPase domain of Hsp70/DnaK. Biochemistry 42:4926-4936 (Pubitemid 36532045)
25. Le Roch KG, Zhou Y, Blair PL, Grainger M, Moch JK, Haynes JD, De La Vega P, Holder AA, Batalov S, Carucci DJ, Winzeler EA (2003) Discovery of gene function by expression profiling of the malaria parasite lifecycle. Science 301:1487-1488
26. Li J, Qian X, Sha B (2009) Heat shock protein 40: structural studies and their functional implications. Protein Pept Lett 16:606-612
27. Lu Z, Cyr DM (1998) Protein folding activity of Hsp70 is modified differentially by the Hsp40 co-chaperones Sis1 and Ydj1. J Biol Chem 273:27824-27830 (Pubitemid 28496069)
28. Maier AG, Rug M, O'Neill MT, Brown M, Chakravorty S, Szestak T, Chesson J, Wu Y, Hughes K, Coppel RL, Newbold C, Beeson JG, Craig A, Crabb BS, Cowman AF (2008) Exported proteins required for virulence and rigidity of Plasmodium falciparuminfected human erythrocytes. Cell 134:48-61 (Pubitemid 351905737)
29. Marti M, Good RT, Rug M, Knuepfer E, Cowman AF (2004) Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 306:1930-1933 (Pubitemid 39627856)
30. Matambo TS, Odunuga OO, Boshoff A, Blatch GL (2004) Overproduction, purification, and characterization of the Plasmodium falciparum heat shock protein 70. Protein Expr Purif 33:214-222 (Pubitemid 38161987)
31. McNamara C (2006) Rhodes University MSc thesis
32. Miller LH, Baruch DI, Marsh K, Doumbo OK (2002) The pathogenic basis of malaria. Nature 415:673-679 (Pubitemid 34136400)
33. Misra G, Ramachandran R (2009) Hsp70-1 from Plasmodium falciparum: protein stability, domain analysis and chaperone activity. Biophys Chem 142:55-64
34. Nicoll WS, Botha M, Mcnamara C, Schlange M, Pesce ER, Boshoff A, Ludewig MH, Zimmermann R, Cheetham ME, Chapple JP, Blatch GL (2007) Cytosolic and ER J-domains of mammalian and parasitic origin can functionally interact with DnaK. Int J Biochem Cell Biol 39:736-751 (Pubitemid 46366803)
35. Pavithra SR, Banumathy G, Joy O, Singh V, Tatu U (2004) Recurrent fever promotes Plasmodium falciparum development in human erythrocytes. J Biol Chem 279:46692-46699 (Pubitemid 39518317)
36. Pavithra SR, Kumar R, Tatu U (2007) Systems analysis of chaperone networks in the malarial parasite Plasmodium falciparum. PLoS Comput Biol 3:1701-1715 (Pubitemid 47502975)
37. Pesce E-R, Acharya P, Tatu U, Nicoll WS, Shonhai A, Hoppe HC, Blatch GL (2008) The Plasmodium falciparum heat shock protein 40, Pfj4, associates with heat shock protein 70 and shows similar heat induction and localisation patterns. Int J Biochem Cell Biol 40:2914-2926
38. Pesce E-R, Cockburn IL, Goble JL, Stephens LL, Blatch GL (2010) Malaria heat shock proteins: drug targets that chaperone other drug targets. Infect Disord Drug Targets 10:147-157
39. Ramya TNC, Surolia NN, Surolia A (2006) 15-Deoxyspergualin modulates Plasmodium falciparum heat shock protein function. Biochem Biophys Res Commun 348:585-592 (Pubitemid 44188604)
40. Rosser MFN, Cyr DM (2007) Do Hsp40s act as chaperones or cochaperones? In: Blatch GLed) Networking of Chaperones by Co-Chaperones. Austin: Landes Bioscience; New York: Springer Science+Business Media, 38-51
41. Rüdiger S, Schneider-Mergener J, Bukau B (2001) Its substrate specificity characterizes the DnaJ co-chaperone as a scanning factor for the DnaK chaperone. EMBO J 20:1042-1050 (Pubitemid 32186795)
42. Schnaider T, Soti C, Cheetham ME, Miyata Y, Yahara I, Csermely P (2000) Interaction of the human DnaJ homologue, HSJ1b with the 90 kDa heat shock protein, Hsp90. Life Sci 67:1455-1465 (Pubitemid 30658703)
43. Shonhai A (2010) Plasmodial heat shock proteins: targets for chemotherapy. FEMS Immunol Med Microbiol 58:61-74
44. Shonhai A, Boshoff A, Blatch GL (2005) Plasmodium falciparum heat shock protein 70 is able to suppress the thermosensitivity of an Escherichia coli DnaK mutant strain. Mol Genet Genomics 274:70-78 (Pubitemid 41396985)
45. Shonhai A, Boshoff A, Blatch GL (2007) The structural and functional diversity of Hsp70 proteins from Plasmodium falciparum. Protein Sci 16:1803-1818 (Pubitemid 47367104)
46. Shonhai A, Botha M, de Beer TAP, Boshoff A, Blatch GL (2008) Structure-function study of Plasmodium falciparum heat shock protein 70 using three dimensional modeling and in vitro analysis. Protein Pept Lett 15:1117-1125
47. Silva MD, Cooke BM, Guillotte M, Buckingham DW, Sauzet JP, Le Scanf C, Contamin H, David P, Mercereau-Puijalon O, Bonnefoy S (2005) A role for the Plasmodium falciparum RESA protein in resistance against heat shock demonstrated using gene disruption. Mol Microbiol 56:990-1003 (Pubitemid 40646770)
48. Snow RW, Guerra CA, Noor AM, Myint H, Hay SI (2005) The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434:214-217 (Pubitemid 40388051)
49. Stolinski LA, Eisenmann DM, Arndt KM (1997) Identification of RTF1, a novel gene important for TATA site selection by TATA box-binding protein in Saccharomyces cerevisiae. Mol Cell Biol 17:4490-4500 (Pubitemid 27318125)
50. Walsh P, Bursac D, Law YC, Cry D, Lithgow T (2004) The J-protein family: modulating protein assembly, disassembly and translocation. EMBO Rep 5:567-571 (Pubitemid 39136416)
51. Wang T-F, Chang J, Wang C (1993) Identification of the peptide binding domain of hsc70. 18-kilodalton fragment located immediately after ATPase domain is sufficient for high affinity binding. J Biol Chem 268:26049-26051 (Pubitemid 23361661)
52. Watanabe J (1997) Cloning and characterization of heat shock protein DnaJ homologues from Plasmodium falciparum and comparison with ring infected erythrocyte surface antigen. Mol Biochem Parasitol 88:253-258 (Pubitemid 27346836)
53. Westhoff B, Chapple JP, van der Spuy J, Höhfeld J, Cheetham ME (2005) HSJI is a neuronal shuttling factor for the sorting of chaperone clients to the proteasome. Curr Biol 15:1058-1064 (Pubitemid 40772155)
54. Wisén S, Bertelsen EB, Thompson AD, Patury S, Ung PM-U, Chang L, Evans CG, Walter GM, Wipf P, Carlson HA, Brodsky JL, Zuiderweg ER, Gestwicki J (2010) Binding of a small molecule at a protein-protein interface regulates the chaperone activity of Hsp70-Hsp40. ACS Chem Biol 5:611-622
55. Wittung-Stafshede P, Guidry J, Horne BE, Landry SJ (2003) The J domain of Hsp40 couples ATP hydrolysis to substrate capture in Hsp70. Biochemistry 42:4937-4944 (Pubitemid 36532046)
56. Wright CM, Chovatiya RJ, Jameson NE, Turner DM, Zhu G, Werner S, Huryn DM, Pipas JM, Day BW, Wipf P, Brodsky JL (2008) Pyrimidinone-peptoid hybrid molecules with distinct effects on molecular chaperone function and cell proliferation. Bioorg Med Chem 16:3291-3301 (Pubitemid 351418180)