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Biochemistry, Cell and Molecular Biology

Controlling drug resistance by targeting Plasmodium falciparum heat shock protein 70-1, a chaperone at the centre of protein quality control mechanism: a review

ORCID Icon, ORCID Icon, ORCID Icon, & ORCID Icon
Article: 2202301 | Received 04 Mar 2022, Accepted 07 Mar 2023, Published online: 21 Apr 2023

References

  • Acharya P, Kumar R, Tatu U. 2007. Chaperoning a cellular upheaval in malaria: heat shock proteins in Plasmodium falciparum. Mol Biochem Parasitol. 153(2):85–94.
  • Amusengeri A, Astl L, Lobb K, Verkhivker GM, Bishop ÖT. 2019. Establishing computational approaches towards identifying malarial allosteric modulators: a case study of plasmodium falciparum hsp70s. Int J Mol Sci. 20(22):5574.
  • 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(5):1–10.
  • Bonifazi EL, Ríos-Luci C, León LG, Burton G, Padrón JM, Misico RI. 2010. Antiproliferative activity of synthetic naphthoquinones related to lapachol. First synthesis of 5-hydroxylapachol. Bioorganic Med Chem. 18(7):2621–2630. http://doi.org/10.1016/j.bmc.2010.02.032.
  • Bornschlögl T, Woehlke G, Rief M. 2009. Single molecule mechanics of the kinesin neck. Proc Natl Acad Sci U S A. 106(17):6992–6997.
  • Botha M, Chiang AN, Needham PB, Stephens LL, Hoppe HC, Külzer S, Przyborski JM, Lingelbach K, Wipf P, Brodsky JL, et al. 2010. Plasmodium falciparum encodes a single cytosolic type i Hsp40 that functionally interacts with Hsp70 and is upregulated by heat shock. Cell Stress Chaperones. 16(4):389–401.
  • Botha M, Pesce ER, 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(10):1781–1803.
  • Bourzac K. 2014. Infectious disease: beating the big three. Nature. 507:S4–S7.
  • Cajo GC, Horne BE, Kelley WL, Schwager F, Georgopoulos C, Genevaux P. 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(18):12436–12444.
  • Cerqueira GC, Cheeseman IH, Schaffner SF, Nair S, McDew-White M, Phyo AP, Ashley EA, Melnikov A, Rogov P, Birren BW, et al. 2017. Longitudinal genomic surveillance of Plasmodium falciparum malaria parasites reveals complex genomic architecture of emerging artemisinin resistance. Genome Biol. 18(1):1–13.
  • Chakafana G, Zininga T, Shonhai A. 2019a. Comparative structure-function features of Hsp70s of Plasmodium falciparum and human origins. Biophys Rev. 11(4):591–602.
  • Chakafana G, Zininga T, Shonhai A. 2019b. The link that binds: the linker of Hsp70 as a helm of the protein’s function. Biomolecules. 9(10):543.
  • Charnaud SC, Dixon MWA, Nie CQ, Chappell L, Sanders PR, Nebl T, Hanssen E, Berriman M, Chan J-A, Blanch AJ, et al. 2017. The exported chaperone Hsp70-x supports virulence functions for Plasmodium falciparum blood stage parasites. PLoS One. 12(7):e0181656.
  • Cheetham ME, Caplan AJ. 1998. Structure, function and evolution of DnaJ: conservation and adaptation of chaperone function. Cell Stress and Chaperones. 3:28–36.
  • Chen Y, Murillo-Solano C, Kirkpatrick MG, Antoshchenko T, Park HW, Pizarro JC. 2018. Repurposing drugs to target the malaria parasite unfolding protein response. Sci Rep. 8(1):1–12. http://doi.org/10.1038/s41598-018-28608-2.
  • Chiang AN, Valderramos J-C, Balachandran R, Chovatiya RJ, Mead BP, Schneider C, Bell SL, Klein MG, Huryn DM, Chen XS, et al. 2009 Feb 15. Select pyrimidinones inhibit the propagation of the malarial parasite Plasmodium Falciparum. Bioorg Med Chem. 17(4):1527–1533. http://www.ncbi.nlm.nih.gov/pubmed/19195901.
  • Chua C-SS, Low H, Sim T-SS. 2014 Aug. Co-chaperones of Hsp90 in plasmodium falciparum and their concerted roles in cellular regulation. Parasitology. 141(9):1177–1191.
  • Cockburn IL, Boshoff A, Pesce ER, Blatch GL. 2014. Selective modulation of plasmodial Hsp70s by small molecules with antimalarial activity. Biol Chem. 395(11):1353–1362.
  • Cockburn IL, Pesce ER, Pryzborski JM, Davies-Coleman MT, Clark PGK, Keyzers RA, Stephens LL, Blatch GL. 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(5):431–438.
  • Corbett KD, Berger JM. 2010. Structure of the ATP-binding domain of Plasmodium falciparum Hsp90. Proteins Struct Funct Bioinforma. 78(13):2738–2744.
  • Daniyan MO, Przyborski JM, Shonhai A. 2019. Partners in mischief: functional networks of heat shock proteins of Plasmodium falciparum and their influence on parasite virulence. Biomolecules. MDPI AG. 9:295.
  • 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(7249):945–949.
  • Deu E. 2017. Proteases as antimalarial targets: strategies for genetic, chemical, and therapeutic validation. FEBS J. 284(16):2604–2628.
  • Dobson S, Kar B, Kumar R, Adams B, Barik S. 2001. A novel tetratricopeptide repeat (TPR) containing PP5 serine/threonine protein phosphatase in the malaria parasite, Plasmodium falciparum. BMC Microbiol. 1:1–10.
  • Emerson PM, Ngondi J, Biru E, Graves PM, Ejigsemahu Y, Gebre T, Endeshaw T, Genet A, Mosher AW, Zerihun M, et al. 2008. Integrating an NTD with one of ‘the big three’ combined malaria and trachoma survery in Amhara region of Ethiopia. PLoS Negl Trop Dis. 2(3):e197.
  • Evans LE, Cheeseman MD, Yahya N, Jones K. 2015. Investigating apoptozole as a chemical probe for HSP70 inhibition. PLoS One. 10(10):1–13.
  • Feder ME, Hofmann GE. 1999. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol. 61:243–282.
  • Fewell SW, Smith CM, Lyon MA, Dumitrescu TP, Wipf P, Day BW, Brodsky JL. 2004. Small molecule modulators of endogenous and co-chaperone-stimulated Hsp70 ATPase activity. J Biol Chem. 279(49):51131–51140. http://doi.org/10.1074/jbc.M404857200.
  • Freeman BC, Myers MP, Schumacher R, Morimoto RI. 1995. Identification of a regulatory motif in Hsp70 that affects ATPase activity, substrate binding and interaction with HDJ-1. EMBO J. 14(10):2281–2292.
  • Gisselberg JE, Zhang L, Elias JE, Yeh E. 2017. The prenylated proteome of Plasmodium falciparum reveals pathogen-specific prenylation activity and drug mechanism-of-action. Mol Cell Proteomics. 16(4):S54–S64. http://doi.org/10.1074/mcp.M116.064550.
  • Gitau GW. 2014. Characterisation of the plasmodium falciparum Hsp70- A Thesis submitted in fulfillment of the requirements for the degree. University of Zululand.
  • Gitau GW, Mandal P, Blatch GL, Przyborski J, Shonhai A. 2012. Characterisation of the Plasmodium falciparum Hsp70-Hsp90 organising protein (PfHop). Cell Stress Chaperones. 17(2):191–202.
  • Gong W, Hu W, Xu L, Wu H, Wu S, Zhang H, Wang J, Jones GW, Perrett S. 2018. The C-terminal GGAP motif of Hsp70 mediates substrate recognition and stress response in yeast. J Biol Chem. 293(46):17663–17675.
  • 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(11):1766–1779. http://doi.org/10.1080/07391102.2013.834849.
  • Hatherley R, Brown DK, Glenister M, Bishop ÖT. 2016. PRIMO: An interactive homology modeling pipeline. PLoS One. 11(11):1–20.
  • Hygon M. 2016. Characterization of PFF1010c, a type IV Plasmodium falciparum heat shock protein 40. Thohoyandou: University of Venda.
  • 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. http://doi.org/10.1016/j.molbiopara.2017.03.003.
  • Kayamba F, Malimabe T, Ademola IK, Pooe OJ, Kushwaha ND, Mahlalela M, van Zyl RL, Gordon M, Mudau PT, Zininga T, et al. 2021. Design and synthesis of quinoline-pyrimidine inspired hybrids as potential plasmodial inhibitors. Eur J Med Chem. 217:113330. https://doi.org/10.1016/j.ejmech.2021.113330.
  • Keyzers RA, Gray CA, Schleyer MH, Whibley CE, Hendricks DT, Davies-Coleman MT. 2006. Malonganenones A-C, novel tetraprenylated alkaloids from the Mozambique gorgonian Leptogorgia gilchristi. Tetrahedron. 62(10):2200–2206.
  • Kityk R, Kopp J, Mayer MP. 2018. Molecular mechanism of J-domain-triggered ATP hydrolysis by Hsp70 chaperones. Mol Cell. 69(2):227–237.e4.
  • Kravats AN, Hoskins JR, Reidy M, Johnson JL, Doyle SM, Genest O, Masison DC, Wickner S. 2018. Functional and physical interaction between yeast Hsp90 and Hsp70. Proc Natl Acad Sci U S A. 115(10):E2210–9.
  • Külzer S, Charnaud S, Dagan T, Riedel J, Mandal P, Pesce ER, Blatch GL, Crabb BS, Gilson PR, Przyborski JM. 2012 Nov. Plasmodium falciparum-encoded exported hsp70/hsp40 chaperone/co-chaperone complexes within the host erythrocyte. Cell Microbiol. 14(11):1784–1795.
  • Kumar R, Musiyenko A, Barik S. 2003. The heat shock protein 90 of Plasmodium falciparum and antimalarial activity of its inhibitor, geldanamycin. Malar J. 2:1–11.
  • Lilburn TG, Cai H, Gu J, Zhou Z, Wang Y. 2014. Exploring systems affected by the heat shock response in Plasmodium falciparum via protein association networks. Int J Comput Biol Drug Des. 7(4):369–383.
  • Lindquist S, Craig EA. 1988. The heat-shock proteins. Annu Rev Genet. 22(1):631–677. https://doi.org/10.1146/annurev.ge.22.120188.003215.
  • Liu K, Houry WA. 2014. Heat shock proteins of malaria. In: Shonhai A, Blatch GL, editor. Heat shock proteins of malaria. London: Springer; p. 1–223.
  • Liu Q, Liang C, Zhou L. 2019. Structural and functional analysis of the Hsp70/Hsp40 chaperone system. Protein Science. 29:378–390.
  • Mabate B. 2017. Exploration of interaction between Plasmodium falciparum Hsp70-x (PfHsp70-x) and human Hsp70-Hsp90 organizing protein (hHop) by, A thesis submitted in fulfillment of the requirements for the degree of Master of Science in the subject of Biochemistry at.
  • Mabate B, Zininga T, Ramatsui L, Makumire S, Achilonu I, Dirr HW, Shonhai A. 2018. Structural and biochemical characterization of Plasmodium falciparum Hsp70-x reveals functional versatility of its C-terminal EEVN motif. Proteins Struct Funct Bioinforma. 86(11):1189–1201. https://doi.org/10.1016/j.compbiolchem.2019.107099.
  • Machin JM, Kantsadi AL, Vakonakis I. 2019. The complex of Plasmodium falciparum falcipain-2 protease with an (E)-chalcone-based inhibitor highlights a novel, small, molecule-binding site. Malar J. 18(1):1–9. https://doi.org/10.1186/s12936-019-3043-0.
  • Makumire S. 2019. Investigation of the role of the GGMP motif of Plasmodium falciparum Hsp70-1 on the chaperone function of the protein and its interaction with a co-chaperone, PfHop by Stanley Makumire submitted in fulfilment of the requirements for the degree of Doctor. University of Venda.
  • Mathews ES, Jezewski AJ, Odom John AR. 2021 Jun 29. Protein prenylation and Hsp40 in thermotolerance of Plasmodium falciparum malaria parasites. MBio. 12(3):e0076021.
  • Misra G, Ramachandran R. 2009. Hsp70-1 from Plasmodium falciparum: protein stability, domain analysis and chaperone activity. Biophys Chem. 142(1–3):55–64. http://doi.org/10.1016/j.bpc.2009.03.006.
  • 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. 3:1310–1310. http://www.nature.com/.
  • Njunge J, Ludewig MH, Boshoff A, Pesce E-R, Blatch GL. 2013. Hsp70s and J proteins of plasmodium parasites infecting rodents and primates: structure, function, clinical relevance, and drug targets. Curr Pharm Des. 19(3):387–403.
  • Njunge JM, Mandal P, Przyborski JM, Boshoff A, Pesce ER, Blatch GL. 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.
  • Pavithra SR, Kumar R, Tatu U. 2007. Systems analysis of chaperone networks in the malarial parasite Plasmodium falciparum. PLoS Comput Biol. 3(9):1701–1715.
  • Pesce ER, 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(12):2914–2926.
  • Pesce ER, Blatch GL.. 2014. Plasmodial Hsp40 and Hsp70 chaperones: current and future perspectives. Parasitology. 141(9):1167–1176.
  • 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(3):147–157. https://www.eurekaselect.com/86120/article.
  • Posfai D, Eubanks AL, Keim AI, Lu KY, Wang GZ, Hughes PF, Kato N, Haystead TA, Derbyshire ER. 2018. Identification of Hsp90 inhibitors with anti-plasmodium activity. Antimicrob Agents Chemother. 62(4):e01799-17.
  • Priya PP, Grover M, Tatu US, Natarajan V, Langsley G. 2015. Characterization of precursor PfHsp60 in Plasmodium falciparum cytosol during its asexual development in human erythrocytes. PLoS One. 10(8):e0136401.
  • Przyborski JM, Diehl M, Blatch GL. 2015. Plasmodial HSP70s are functionally adapted to the malaria parasite life cycle. Front Mol Biosci. 2(JUN):1–7. http://doi.org/10.3389/fmolb.2015.00034/abstract.
  • Qiu XB, Shao YM, Miao S, Wang L. 2006. The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cell Mol Life Sci. 63(22):2560–2570.
  • Ramya TNC, Surolia N, Surolia A. 2006. 15-Deoxyspergualin modulates Plasmodium falciparum heat shock protein function. Biochem Biophys Res Commun. 348(2):585–592.
  • Ramya TNC, Surolia N, Surolia A. 2007. 15-Deoxyspergualin inhibits eukaryotic protein synthesis through eIF2α phosphorylation. Biochem J. 401(2):411–420.
  • Reiter K, Mukhopadhyay D, Zhang H, Boucher LE, Kumar N, Bosch J, Matunis MJ. 2013. Identification of biochemically distinct properties of the small ubiquitin-related modifier (SUMO) conjugation pathway in Plasmodium falciparum. J Biol Chem. 288(39):27724–27736.
  • Reiter KH, Matunis MJ. 2016. Detection of SUMOylation in Plasmodium falciparum. Methods in Molecular Biology. 1475:283–290.
  • Richter K, Buchner J. 2001. Hsp90: chaperoning signal transduction. J Cell Physiol. 188(3):281–290.
  • Rodina A, Vilenchik M, Moulick K, Aguirre J, Kim J, Chiang A, Litz J, Clement CC, Kang Y, She Y, et al. 2007. Selective compounds define Hsp90 as a major inhibitor of apoptosis in small-cell lung cancer. Nat Chem Biol. 3(8):498–507.
  • Rug M, Maier AG. 2011. The heat shock protein 40 family of the malaria parasite Plasmodium falciparum. IUBMB Life. 63(12):1081–1086.
  • Salomane N, Pooe OJ, Simelane MBC. 2021. Iso-mukaadial acetate and ursolic acid acetate inhibit the chaperone activity of Plasmodium falciparum heat shock protein 70-1. Cell Stress Chaperones. 26(4):685–693.
  • Sannella AR, Messori L, Casini A, Francesco Vincieri F, Bilia AR, Majori G, Severini C. 2007. Antimalarial properties of green tea. Biochem Biophys Res Commun. 353(1):177–181.
  • Schulze J, Kwiatkowski M, Borner J, Schlüter H, Bruchhaus I, Burmester T, Spielmann T, Pick C. 2015. The Plasmodium falciparum exportome contains non-canonical PEXEL/HT proteins. Mol Microbiol. 97(2):301–314.
  • Seraphim T V, Chakafana G, Shonhai A, Houry WA. 2019. Plasmodium falciparum R2TP complex: driver of parasite Hsp90 function. Biophys Rev. 11(6):1007–1015.
  • Shahinas D, Folefoc A, Pillai DR. 2013a. Targeting plasmodium falciparum Hsp90: towards reversing antimalarial resistance. Pathogens. 2(1):33–54.
  • Shahinas D, Folefoc A, Taldone T, Chiosis G, Crandall I, Pillai DR. 2013b. A purine analog synergizes with chloroquine (CQ) by targeting Plasmodium falciparum Hsp90 (PfHsp90). PLoS One. 8(9):e75446.
  • Shonhai A. 2010. Plasmodial heat shock proteins: targets for chemotherapy. FEMS immunology & medical microbiology. 58(1):61–74. https://doi.org/10.1111/j.1574-695X.2009.00639.x
  • 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(1):70–78.
  • Shonhai A, Boshoff A, Blatch GL. 2007. The structural and functional diversity of Hsp70 proteins from Plasmodium falciparum. Protein Sci. 16(9):1803–1818.
  • Stephens LL, Shonhai A, Blatch GL. 2011. Co-expression of the Plasmodium falciparum molecular chaperone, PfHsp70, improves the heterologous production of the antimalarial drug target GTP cyclohydrolase I, PfGCHI. Protein Expr Purif. 77(2):159–165. http://doi.org/10.1016/j.pep.2011.01.005.
  • Tavella TA, Da Silva NSM, Spillman N, Kayano ACAV, Cassiano GC, Vasconcelos AA, Camargo AP, da Silva DCB, Fontinha D, Salazar Alvarez LC, et al. 2021. Violacein-Induced chaperone system collapse underlies multistage antiplasmodial activity. ACS Infect Dis. 7(4):759–776.
  • Tsai J, Douglas MG. 1996. A conserved HPD sequence of the J-domain is necessary for YDJ1 stimulation of Hsp70 ATPase activity at a site distinct from substrate binding. J Biol Chem. 271(16):9347–9354.
  • USAID. 2018. President’s Malaria Initiative – Zimbabwe Country Profile.
  • Utpal T, Soundara Raghavan P, Gowrishankar B. 2004. A Novel Assay to Screen for Anti-Malarials.
  • Wayne N, Mishra P, Bolon DN. 2011. Hsp90 and client protein maturation. Methods Mol Biol. 787:33–44.
  • World Health Organization. 2021. World malaria report 2021 [Internet]. [cited 2022 Feb 12]. https://apps.who.int/iris/rest/bitstreams/1398397/retrieve.
  • Yeo SJ, Liu DX, Park H. 2015. Potential interaction of Plasmodium falciparum Hsp60 and calpain. Korean J Parasitol. 53(6):665–673.
  • Yuan X, Yin P, Hao Q, Yan C, Wang J, Yan N. 2010. Single amino acid alteration between valine and isoleucine determines the distinct pyrabactin selectivity by PYL1 and PYL2. J Biol Chem. 285(37):28953–8.
  • Zhang M, Wang C, Oberstaller J, Thomas P, Otto TD, Casandra D, Boyapalle S, Adapa SR, Xu S, Button-Simons K, Mayho M. 2021. The apicoplast link to fever-survival and artemisinin-resistance in the malaria parasite. Nat Commun. 12(1):1–15. http://doi.org/10.1038/s41467-021-24814-1.
  • Zininga T. 2015. Characterization of heat shock protein 70-z (PfHsp70-z) from Plasmodium falciparium; (November). http://univendspace.univen.ac.za/handle/11602/619.
  • Zininga T, Achilonu I, Hoppe H, Prinsloo E, Dirr HW, Shonhai A. 2015. Overexpression, purification and characterisation of the Plasmodium falciparum Hsp70-z (PfHsp70-z) protein. PLoS One. 10(6):1–13.
  • Zininga T, Anokwuru CP, Sigidi MT, Tshisikhawe MP, Ramaite IID, Traoré AN, Hoppe H, Shonhai A, Potgieter N. 2017a. Extracts obtained from pterocarpus angolensis dc and ziziphus mucronata exhibit antiplasmodial activity and inhibit heat shock protein 70 (Hsp70) function. Molecules. 22(8):1224.
  • Zininga T, Pooe OJ, Makhado PB, Ramatsui L, Prinsloo E, Achilonu I, Dirr H, Shonhai A. 2017b. Polymyxin B inhibits the chaperone activity of Plasmodium falciparum Hsp70. Cell Stress Chaperones. 22(5):707–715.
  • Zininga T, Ramatsui L, Makhado PB, Makumire S, Achilinou I, Hoppe H, Dirr H, Shonhai A. 2017c. (−)-Epigallocatechin-3-gallate inhibits the chaperone activity of Plasmodium falciparum Hsp70 chaperones and abrogates their association with functional partners. Molecules. 22(12):2139.
  • Zininga T, Ramatsui L, Shonhai A. 2018. Heat shock proteins as immunomodulants. Molecules. 23(11):2846.
  • Zininga T, Shonhai A. 2014. Are heat shock proteins druggable candidates? Am J Biochem Biotechnol Sci Publ. 10(2014):208–210.
  • Zininga T, Shonhai A. 2019. Small molecule inhibitors targeting the heat shock protein system of human obligate protozoan parasites. Int J Mol Sci. 20(23):1–29.