Skip to main content

Role of the J Domain Protein Family in the Survival and Pathogenesis of Plasmodium falciparum

  • Chapter
  • First Online:
Heat Shock Proteins of Malaria

Abstract

Plasmodium falciparum has dedicated an unusually large proportion of its genome to molecular chaperones (2% of all genes), with the heat shock protein 40 (Hsp40) family (now called J domain proteins, JDPs) exhibiting evolutionary radiation into 49 members. A large number of the P. falciparum JDPs (PfJDPs) are predicted to be exported, with certain members shown experimentally to be present in the erythrocyte cytosol (PFA0660w and PFE0055c) or erythrocyte membrane (ring-infected erythrocyte surface antigen, RESA). PFA0660w and PFE0055c are associated with an exported plasmodial Hsp70 (PfHsp70-x) within novel mobile structures called J-dots, which have been proposed to be dedicated to the trafficking of key membrane proteins such as erythrocyte membrane protein 1 (PfEMP1). Well over half of the PfJDPs appear to be essential, including the J-dot PfJDP, PFE0055c, while others have been found to be required for growth under febrile conditions (e.g. PFA0110w, the ring-infected erythrocyte surface antigen protein [RESA]) or involved in pathogenesis (e.g. PF10_0381 has been shown to be important for protrusions of the infected red blood cell membrane, the so-called knobs). Here we review what is known about those PfJDPs that have been well characterised, and may be directly or indirectly involved in the survival and pathogenesis of the malaria parasite.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Acharya P, Pallavi R, Chandran S et al (2009) A glimpse into the clinical proteome of human malaria parasites Plasmodium falciparum and Plasmodium vivax. Proteomics Clin Appl 3:1314–1325

    Article  CAS  PubMed  Google Scholar 

  • Acharya P, Chaubey S, Grover M et al (2012) An exported heat shock protein 40 associates with pathogenesis-related knobs in Plasmodium falciparum infected erythrocytes. PLoS One 7:e44605

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agrawal S, van Dooren GG, Beatty WL et al (2009) Genetic evidence that an endosymbiont-derived endoplasmic reticulum-associated protein degradation (ERAD) system functions in import of apicoplast proteins. J Biol Chem 284:33683–33691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anas M, Shukla A, Tripathi A et al (2020) Structural–functional diversity of malaria parasite’s PfHSP70-1 and PfHSP40 chaperone pair gives an edge over human orthologs in chaperone-assisted protein folding. Biochem J 477:3625–3643

    Article  CAS  PubMed  Google Scholar 

  • Aurrecoechea C, Brestelli J, Brunk BP et al (2009) PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res 37:D539–D543

    Article  CAS  PubMed  Google Scholar 

  • Badaut C, Guyonnet L, Milet J et al (2015) Immunoglobulin response to Plasmodium falciparum RESA proteins in uncomplicated and severe malaria. Malar J 14:278

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Behl A, Mishra PC (2019) Structural insights into the binding mechanism of Plasmodium falciparum exported Hsp40-Hsp70 chaperone pair. Comput Biol Chem 83:107099

    Article  CAS  PubMed  Google Scholar 

  • Behl A, Kumar V, Bisht A, Panda JJ, Hora R, Mishra PC (2019) Cholesterol bound Plasmodium falciparum co-chaperone ‘PFA0660w’ complexes with major virulence factor ‘PfEMP1’ via chaperone ‘PfHsp70-x’. Sci Rep 9:1–7

    Article  CAS  Google Scholar 

  • Bell SL, Chiang AN, Brodsky JL (2011) Expression of a malarial Hsp70 improves defects in chaperone-dependent activities in ssa1 mutant yeast. PLoS One 6:e20047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bennett BJ, Mohandas N, Coppel RL (1997) Defining the minimal domain of the Plasmodium falciparum protein MESA involved in the interaction with the red cell membrane skeletal protein 4.1. J Biol Chem 272:15299–15306

    Article  CAS  PubMed  Google Scholar 

  • Black CG, Proellocks NI, Kats LM et al (2008) In vivo studies support the role of trafficking and cytoskeletal-binding motifs in the interaction of MESA with the membrane skeleton of Plasmodium falciparum-infected red blood cells. Mol Biochem Parasitol 160:143–147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boddey JA, Hodder AN, Günther S et al (2010) An aspartyl protease directs malaria effector proteins to the host cell. Nature 463:627–631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boddey JA, Carvalho TG, Hodder AN et al (2013) Role of Plasmepsin V in export of diverse protein families from the Plasmodium falciparum exportome. Traffic 14:532–550

    Article  CAS  PubMed  Google Scholar 

  • Botha M (2009) Characterisation of the Plasmodium falciparum Hsp40 chaperones and their partnerships with Hsp70. PhD Thesis, Rhodes University. http://hdl.handle.net/10962/d1003997

  • Botha M, Pesce E-R, Blatch GL (2007) The Hsp40 proteins of Plasmodium falciparum and other apicomplexa: regulating chaperone power in the parasite and the host. Int J Biochem Cell Biol 39:1781–1803

    Article  CAS  PubMed  Google Scholar 

  • Botha M, Chiang AN, Needham PG et al (2011) Plasmodium falciparum encodes a single cytosolic type I Hsp40 that functionally interacts with Hsp70 and is upregulated by heat shock. Cell Stress Chaperones 16:389–401

    Article  CAS  PubMed  Google Scholar 

  • Bozdech Z, VanWye J, Haldar K et al (1998) The human malaria parasite Plasmodium falciparum exports the ATP-binding cassette protein PFGCN20 to membrane structures in the host red blood cell. Mol Biochem Parasitol 97:81–95

    Article  CAS  PubMed  Google Scholar 

  • Bozdech Z, Llinás M, Pulliam BL et al (2003) The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol 1:E5

    Article  PubMed  PubMed Central  Google Scholar 

  • Cajo GC, Horne BE, Kelley WL et al (2006) The role of the DIF motif of the DnaJ (Hsp40) co-chaperone in the regulation of the DnaK (Hsp70) chaperone cycle. J Biol Chem 281:12436–12444

    Article  CAS  PubMed  Google Scholar 

  • Charnaud SC, Dixon MW, Nie CQ et al (2017) The exported chaperone Hsp70-x supports virulence functions for Plasmodium falciparum blood stage parasites. PloS One 12:e0181656

    Article  PubMed  PubMed Central  Google Scholar 

  • Chiang AN, Valderramos JC, Balachandran R et al (2009) Select pyrimidinones inhibit the propagation of the malarial parasite, Plasmodium falciparum. Bioorg Med Chem 17:1527–1533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cobb DW, Florentin A, Fierro MA et al (2017) The exported chaperone PfHsp70x is dispensable for the Plasmodium falciparum intraerythrocytic life cycle. MSphere 2:e00363–e00317

    Article  PubMed  PubMed Central  Google Scholar 

  • Cockburn IL, Pesce E-R, Przyborski JM et al (2011) Screening for small molecule modulators of Hsp70 chaperone activity using protein aggregation suppression assays: inhibition of the plasmodial chaperone PfHsp70-1. Biol Chem 392:431–438

    Article  CAS  PubMed  Google Scholar 

  • Cockburn IL, Boshoff A, Pesce ER, Blatch GL (2014) Selective modulation of plasmodial Hsp70s by small molecules with antimalarial activity. Biol Chem 395:1353–1362

    Article  CAS  PubMed  Google Scholar 

  • Cooke BM, Glenister FK, Mohandas N et al (2002) Assignment of functional roles to parasite proteins in malaria-infected red blood cells by competitive flow-based adhesion assay. Br J Haematol 117:203–211

    Article  CAS  PubMed  Google Scholar 

  • Coppel RL (1992) Repeat structures in a Plasmodium falciparum protein (MESA) that binds human erythrocyte protein 4.1. Mol Biochem Parasitol 50:335–347

    Article  CAS  PubMed  Google Scholar 

  • Coppel RL, Lustigman S, Murray L et al (1988) MESA is a Plasmodium falciparum phosphoprotein associated with the erythrocyte membrane skeleton. Mol Biochem Parasitol 31:223–231

    Article  CAS  PubMed  Google Scholar 

  • Crabb BS, Cooke BM, Reeder JC et al (1997) Targeted gene disruption shows that knobs enable malaria-infected red cells to cytoadhere under physiological shear stress. Cell 89:287–296

    Article  CAS  PubMed  Google Scholar 

  • Daniyan MO, Blatch GL (2017) Plasmodial Hsp40s: new avenues for antimalarial drug discovery. Curr Pharm Des 23:4555–4570

    Article  CAS  PubMed  Google Scholar 

  • Daniyan MO, Boshoff A, Prinsloo E, Pesce ER, Blatch GL (2016) The malarial exported PFA0660w is an Hsp40 co-chaperone of PfHsp70-x. PLoS One 11:e0148517

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Day J, Passecker A, Beck HP, Vakonakis I (2019) The Plasmodium falciparum Hsp70-x chaperone assists the heat stress response of the malaria parasite. FASEB J 33:14611–14624

    Article  PubMed  PubMed Central  Google Scholar 

  • De Koning-Ward TF, Gilson PR, Boddey JA et al (2009) A newly discovered protein export machine in malaria parasites. Nature 459:945–949

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deponte M, Hoppe HC, Lee MCS et al (2012) Wherever I may roam: protein and membrane trafficking in P. falciparum-infected red blood cells. Mol Biochem Parasitol 186:95–116

    Article  CAS  PubMed  Google Scholar 

  • Diez-Silva M, Park Y, Huang S et al (2012) Pf155/RESA protein influences the dynamic microcirculatory behavior of ring-stage Plasmodium falciparum infected red blood cells. Sci Rep 2:614

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Durand R, Migot-Nabias F, Andriantsoanirina V et al (2012) Possible association of the Plasmodium falciparum T1526C resa2 gene mutation with severe malaria. Malar J 11:128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dutta T, Singh H, Gestwicki JE et al (2021) Exported plasmodial J domain protein, PFE0055c, and PfHsp70-x form a specific co-chaperone-chaperone partnership. Cell Stress Chaperones. 26:355-366

    Google Scholar 

  • Elsworth B, Matthews K, Nie CQ et al (2014) PTEX is an essential nexus for protein export in malaria parasites. Nature 511:587–591

    Article  CAS  PubMed  Google Scholar 

  • Elsworth B, Sanders PR, Nebl T et al (2016) Proteomic analysis reveals novel proteins associated with the Plasmodium protein exporter PTEX and a loss of complex stability upon truncation of the core PTEX component, PTEX150. Cell Microbiol 18:1551–1569

    Article  CAS  PubMed  Google Scholar 

  • Farh L, Mitchell DA, Deschenes RJ (1995) Farnesylation and proteolysis are sequential, but distinct steps in the CaaX box modification pathway. Arch Biochem Biophys 318:113–121

    Article  CAS  PubMed  Google Scholar 

  • Fewell SW, Smith CM, Lyon MA et al (2004) Small molecule modulators of endogenous and co-chaperone-stimulated Hsp70 ATPase activity. J Biol Chem 279:51131–51140

    Article  CAS  PubMed  Google Scholar 

  • Flom GA, Lemieszek M, Fortunato EA et al (2008) Farnesylation of Ydj1 is required for in Vivo interaction with Hsp90 client proteins. Mol Biol Cell 19:5249–5258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Florens L, Washburn MP, Raine JD et al (2002) A proteomic view of the Plasmodium falciparum life cycle. Nature 419:520–526

    Article  CAS  PubMed  Google Scholar 

  • Florentin A, Cobb DW, Kudyba HM, Muralidharan V (2020) Directing traffic: chaperone-mediated protein transport in malaria parasites. Cell Microbiol 22:e13215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grover M, Chaubey S, Ranade S, Tatu U (2013) Identification of an exported heat shock protein 70 in Plasmodium falciparum. Parasite 20:2

    Article  PubMed  PubMed Central  Google Scholar 

  • Hagiwara M, Maegawa K, Suzuki M et al (2011) Structural basis on an ERAD pathway mediated by the ER-resident protein disulfide reductase Erdj5. Mol Cell 41:432–444

    Article  CAS  PubMed  Google Scholar 

  • Hatherley R, Blatch GL, Bishop ÖT (2014) Plasmodium falciparum Hsp70-x: a heat shock protein at the host–parasite interface. J Biomol Struct Dyn 32:1766–1779

    Article  CAS  PubMed  Google Scholar 

  • Hennessy F, Nicoll WS, Zimmermann R et al (2005) Not all J domains are created equal: implications for the specificity of Hsp40-Hsp70 interactions. Protein Sci 14:1697–1709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hiller NL, Bhattacharjee S, van Ooij C et al (2004) A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 306:1934–1937

    Article  CAS  PubMed  Google Scholar 

  • Jha P, Laskar S, Dubey S, Bhattacharyya MK, Bhattacharyya S (2017) Plasmodium Hsp40 and human Hsp70: a potential cochaperone-chaperone complex. Mol Biochem Parasitol 214:10–13

    Article  CAS  PubMed  Google Scholar 

  • Kalanon M, Tonkin CJ, McFadden GI et al (2009) Characterization of two putative protein translocation components in the apicoplast of Plasmodium falciparum. Eukaryot Cell 8:1146–1154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kampinga HH, Andreasson C, Barducci A et al (2019) Function, evolution, and structure of J-domain proteins. Cell Stress Chaperones 24:7–15

    Article  PubMed  Google Scholar 

  • Khosh-Naucke M, Becker J, Mesén-Ramírez P et al (2018) Identification of novel parasitophorous vacuole proteins in P. falciparum parasites using BioID. Int J Med Microbiol 308:13–24

    Article  CAS  PubMed  Google Scholar 

  • Kilili GK, LaCount DJ (2011) An erythrocyte cytoskeleton-binding motif in exported Plasmodium falciparum proteins. Eukaryot Cell 10:1439–1447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Külzer S, Rug M, Brinkmann K et al (2010) Parasite-encoded Hsp40 proteins define novel mobile structures in the cytosol of the P. falciparum-infected erythrocyte. Cell Microbiol 12:1398–1420

    Article  PubMed  CAS  Google Scholar 

  • Külzer S, Charnaud S, Dagan T et al (2012) Plasmodium falciparum-encoded exported Hsp70/Hsp40 chaperone/co-chaperone complexes within the host erythrocyte. Cell Microbiol 14:1784–1795

    Article  PubMed  CAS  Google Scholar 

  • Kumar N, Koski G, Harada M et al (1991) Induction and localization of Plasmodium falciparum stress proteins related to the heat shock protein 70 family. Mol Biochem Parasitol 48:47–58

    Article  CAS  PubMed  Google Scholar 

  • Kumar A, Tanveer A, Biswas S et al (2010) Nuclear-encoded DnaJ homologue of Plasmodium falciparum interacts with replication ori of the apicoplast genome. Mol Microbiol 75:942–956

    Article  CAS  PubMed  Google Scholar 

  • LaCount DJ, Vignali M, Chettier R et al (2005) A protein interaction network of the malaria parasite Plasmodium falciparum. Nature 438:103–107

    Article  CAS  PubMed  Google Scholar 

  • Le Roch KG, Zhou Y, Blair PL et al (2003) Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301:1503–1508

    Article  PubMed  Google Scholar 

  • Li J, Sha B (2005) Structure-based mutagenesis studies of the peptide substrate binding fragment of type I heat-shock protein 40. Biochem J 386:453–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mabate B, Zininga T, Ramatsui L et al (2018) Structural and biochemical characterization of Plasmodium falciparum Hsp70- x reveals functional versatility of its C-terminal EEVN motif. Proteins 86:1189–1201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maier AG, Rug M, O’Neill MT et al (2008) Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell 134:48–61

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mansouri R, Ali-Hassanzadeh M, Shafiei R et al (2020) The use of proteomics for the identification of promising vaccine and diagnostic biomarkers in Plasmodium falciparum. Parasitology 147:1255–1262

    Article  CAS  PubMed  Google Scholar 

  • Marti M, Good RT, Rug M et al (2004) Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 306:1930–1933

    Article  CAS  PubMed  Google Scholar 

  • Matambo TS, Odunuga OO, Boshoff A et al (2004) Overproduction, purification, and characterization of the Plasmodium falciparum heat shock protein 70. Protein Expr Purif 33:214–222

    Article  CAS  PubMed  Google Scholar 

  • Matthews KM, Kalanon M, de Koning-Ward TF (2019) Uncoupling the threading and unfoldase actions of Plasmodium HSP101 reveals differences in export between soluble and insoluble proteins. MBio 10(3):e01106-19

    Article  PubMed  PubMed Central  Google Scholar 

  • Misra G, Ramachandran R (2009) Hsp70-1 from Plasmodium falciparum: protein stability, domain analysis and chaperone activity. Biophys Chem 142:55–64

    Article  CAS  PubMed  Google Scholar 

  • Morahan BJ, Strobel C, Hasan U et al (2011) Functional analysis of the exported type IV HSP40 protein PfGECO in Plasmodium falciparum gametocytes. Eukaryot Cell 10:1492–1503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moses MA, Kim YS, Rivera-Marquez GM et al (2018) Targeting the Hsp40/Hsp70 chaperone axis as a novel strategy to treat castration-resistant prostate cancer. Cancer Res 78:4022–4035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muralidharan V, Oksman A, Pal P, Lindquist S, Goldberg DE (2012) Plasmodium falciparum heat shock protein 110 stabilizes the asparagine repeat-rich parasite proteome during malarial fevers. Nat Commun 3:1310

    Article  PubMed  CAS  Google Scholar 

  • Nicoll WS, Botha M, McNamara C et al (2007) Cytosolic and ER J-domains of mammalian and parasitic origin can functionally interact with DnaK. Int J Biochem Cell Biol 39:736–751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Njunge JM, Ludewig MH, Boshoff A et al (2013) Hsp70s and J proteins of Plasmodium parasites infecting rodents and primates: structure, function, clinical relevance, and drug targets. Curr Pharm Design 19:387–403

    Article  CAS  Google Scholar 

  • Njunge JM, Mandal P, Przyborski JM et al (2015) PFB0595w is a Plasmodium falciparum J protein that co-localizes with PfHsp70-1 and can stimulate its in vitro ATP hydrolysis activity. Int J Biochem Cell Biol 62:47–53

    Article  CAS  PubMed  Google Scholar 

  • Nyalwidhe J, Lingelbach K (2006) Proteases and chaperones are the most abundant proteins in the parasitophorous vacuole of Plasmodium falciparum-infected erythrocytes. Proteomics 6:1563–1573

    Article  CAS  PubMed  Google Scholar 

  • Oakley MSM, Kumar S, Anantharaman V et al (2007) Molecular factors and biochemical pathways induced by febrile temperature in intraerythrocytic Plasmodium falciparum parasites. Infect Immun 75:2012–2025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oakley MSM, Gerald N, McCutchan TF et al (2011) Clinical and molecular aspects of malaria fever. Trends Parasitol 27:442–449

    Article  CAS  PubMed  Google Scholar 

  • Otto TD, Wilinski D, Assefa S et al (2010) New insights into the blood-stage transcriptome of Plasmodium falciparum using RNA-Seq. Mol Microbiol 76:12–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pei X, Guo X, Coppel R et al (2007) The ring-infected erythrocyte surface antigen (RESA) of Plasmodium falciparum stabilizes spectrin tetramers and suppresses further invasion. Blood 110:1036–1042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez-Sacau E, Estévez-Braun A, Ravelo ÁG, Gutiérrez Yapu D, GiménezTurba A (2005) Antiplasmodial activity of naphthoquinones related to lapachol and β-lapachone. Chem Bio Divers 2:264–274

    Google Scholar 

  • Pesce ER, Blatch GL (2014) Plasmodial Hsp40 and Hsp70 chaperones: current and future perspectives. Parasitology 141:1167–1176

    Article  CAS  PubMed  Google Scholar 

  • Pesce E-R, Acharya P, Tatu U et al (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

    Article  CAS  PubMed  Google Scholar 

  • Pesce E-R, Cockburn IL, Goble JL et al (2010) Malaria heat shock proteins: drug targets that chaperone other drug targets. Infect Disord Drug Targets 10:147–157

    Article  CAS  PubMed  Google Scholar 

  • Petersen C, Nelson R, Magowan C (1989) The mature erythrocyte surface antigen of Plasmodium falciparum is not required for knobs or cytoadherence. Mol Biochem Parasitol 36:61–65

    Article  CAS  PubMed  Google Scholar 

  • Petersen W, Külzer S, Engels S, Zhang Q, Ingmundson A, Rug M, Maier AG, Przyborski JM (2016) J-dot targeting of an exported HSP40 in Plasmodium falciparum-infected erythrocytes. Int J Parasitol 46:519–525

    Article  CAS  PubMed  Google Scholar 

  • Przyborski JM (2008) The Maurer’s clefts of Plasmodium falciparum: parasite-induced islands within an intracellular ocean. Trends Parasitol 24:285–288

    Article  CAS  PubMed  Google Scholar 

  • Przyborski JM, Diehl M, Blatch GL (2015) Plasmodial HSP70s are functionally adapted to the malaria parasite life cycle. Front Mol Biosc 2:34

    Article  CAS  Google Scholar 

  • Pudhom K, Kasai K, Terauchi H et al (2006) Synthesis of three classes of rhodacyanine dyes and evaluation of their in vitro and in vivo antimalarial activity. Bioorg Med Chem 14:8550–8563

    Article  CAS  PubMed  Google Scholar 

  • Qin HL, Zhang ZW, Lekkala R, Alsulami H, Rakesh KP (2020) Chalcone hybrids as privileged scaffolds in antimalarial drug discovery: a key review. Eur J Med Chem 193:112215

    Article  CAS  PubMed  Google Scholar 

  • Rajapandi T (2020) Chaperoning of asparagine repeat-containing proteins in Plasmodium falciparum. J Parasit Dis 25:1–7

    Google Scholar 

  • Ramya TNC, Surolia NN, Surolia A (2006) 15-Deoxyspergualin modulates Plasmodium falciparum heat shock protein function. Biochem Biophys Res Comm 348:585–592

    Article  CAS  PubMed  Google Scholar 

  • Ramya TN, Karmodiya K, Surolia A, Surolia N (2007) 15-deoxyspergualin primarily targets the trafficking of apicoplast proteins in Plasmodium falciparum. J Biol Chem 282:6388–6397

    Article  CAS  PubMed  Google Scholar 

  • Rhiel M, Bittl V, Tribensky A et al (2016) Trafficking of the exported P. falciparum chaperone PfHsp70x. Sci Reports 6:1–3

    Google Scholar 

  • Rinaldi S, Assimon VA, Young ZT et al (2018) A local allosteric network in heat shock protein 70 (Hsp70) links inhibitor binding to enzyme activity and distal protein–protein interactions. ACS Chem Biol 13:3142–3152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Russo I, Babbitt S, Muralidharan V et al (2010) Plasmepsin V licenses Plasmodium falciparum proteins for export into the host erythrocyte. Nature 463:632–636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sargeant TJ, Marti M, Caler E et al (2006) Lineage-specific expansion of proteins exported to the erythrocyte in malaria parasites. Genome Biol 7:R12

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sato S, Wilson RJ (2005) Organelle-specific cochaperonins in apicomplexan parasites. Mol Biochem Parasitol 141:133–143

    Article  CAS  PubMed  Google Scholar 

  • Shao H, Li X, Moses MA et al (2018) Exploration of benzothiazole rhodacyanines as allosteric inhibitors of protein–protein interactions with heat shock protein 70 (Hsp70). J Med Chem 61:6163–6177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 Gen Genomics 274:70–78

    Article  CAS  Google Scholar 

  • Shonhai A, Botha M, de Beer TA et al (2008) Structure-function study of a Plasmodium falciparum Hsp70 using three dimensional modelling and in vitro analyses. Protein Pept Lett 15:1117–1125

    Article  CAS  PubMed  Google Scholar 

  • Silva MD, Cooke BM, Guillotte M et al (2005) A role for the Plasmodium falciparum RESA protein in resistance against heat shock demonstrated using gene disruption. Mol Microbiol 56:990–1003

    Article  CAS  PubMed  Google Scholar 

  • Sinha S, Batovska DI, Medhi B, Radotra BD, Bhalla A, Markova N (2019) In vitro anti-malarial efficacy of chalcones: cytotoxicity profile, mechanism of action and their effect on erythrocytes. Malar J 18:421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sommer MS, Gould SB, Lehmann P et al (2007) Der1-mediated preprotein import into the periplastid compartment of chromalveolates. Mol Biol Evol 24:918–928

    Article  CAS  PubMed  Google Scholar 

  • Spork S, Hiss JA, Mandel K et al (2009) An unusual ERAD-like complex is targeted to the apicoplast of Plasmodium falciparum. Eukaryot Cell 8:1134–1145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suthram S, Sittler T, Ideker T (2005) The Plasmodium protein network diverges from those of other eukaryotes. Nature 438:108–112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuteja R (2007) Unraveling the components of protein translocation pathway in human malaria parasite Plasmodium falciparum. Arch Biochem Biophys 467:249–260

    Article  CAS  PubMed  Google Scholar 

  • Ushioda R, Hoseki J, Araki K et al (2008) Erdj5 is required as a disulfide reductase for degradation of misfolded proteins in the ER. Science 321:569–572

    Article  CAS  PubMed  Google Scholar 

  • Waller KL, Nunomura W, An X et al (2003) Mature parasite-infected erythrocyte surface antigen (MESA) of Plasmodium falciparum binds to the 30-kDa domain of protein 4.1 in malaria-infected red blood cells. Blood 102:1911–1914

    Article  CAS  PubMed  Google Scholar 

  • Walsh P, Bursać D, Law YC et al (2004) The J-protein family: modulating protein assembly, disassembly and translocation. EMBO Rep 5:567–571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Zhang M, Wang C, Otto TD et al (2018) Uncovering the essential genes of the human malaria parasite Plasmodium falciparum by saturation mutagenesis. Science 360:eaap7847

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zimmermann R, Blatch GL (2009) A novel twist to protein secretion in eukaryotes. Trends Parasitol 25:147–150

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

TD and GLB are thankful for financial assistance from The University of Notre Dame Australia. E-RP gratefully acknowledges funding from the Victoria University Research Development Grant Scheme. AGM is kindly supported by the Australian Research Council (DP180103212) and the National Health and Medical Research Council of Australia (APP1182369).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gregory L. Blatch .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Dutta, T., Pesce, ER., Maier, A.G., Blatch, G.L. (2021). Role of the J Domain Protein Family in the Survival and Pathogenesis of Plasmodium falciparum. In: Shonhai, A., Picard, D., Blatch, G.L. (eds) Heat Shock Proteins of Malaria. Advances in Experimental Medicine and Biology, vol 1340. Springer, Cham. https://doi.org/10.1007/978-3-030-78397-6_4

Download citation

Publish with us

Policies and ethics