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Co-chaperones of Hsp90 in Plasmodium falciparum and their concerted roles in cellular regulation

  • CHUN-SONG CHUA (a1), HUIYU LOW (a1) and TIOW-SUAN SIM (a1)

Co-chaperones are well-known regulators of heat shock protein 90 (Hsp90). Hsp90 is a molecular chaperone that is essential in the eukaryotes for the folding and activation of numerous proteins involved in important cellular processes such as signal transduction, growth and developmental regulation. Co-chaperones assist Hsp90 in the protein folding process by modulating conformational changes to promote client protein interaction and functional maturation. With the recognition of Plasmodium falciparum Hsp90 (PfHsp90) as a potential antimalarial drug target, there is obvious interest in the study of its co-chaperones in their partnership in regulating cellular processes in malaria parasite. Previous studies on PfHsp90 have identified more than 10 co-chaperones in P. falciparum genome. However, many of them remained annotated as putative proteins as their functionality has not been validated experimentally. So far, only five co-chaperones, PfHop, Pfp23, PfAha1, PfPP5 and PfFKBP35 have been characterized and shown to interact with PfHsp90. This review will summarize current knowledge on the co-chaperones in P. falciparum and discuss their regulatory roles on PfHsp90. As certain eukaryotic co-chaperones have also been implicated in altering the affinity of Hsp90 for its inhibitor, this review will also examine plasmodial co-chaperones’ potential influence on approaches towards designing antimalarials targeting PfHsp90.

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* Corresponding author: Department of Microbiology, Yong Loo Lin School of Medicine, National University of Singapore, 5 Science Drive 2, Singapore 117597, Singapore. E-mail:
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R. Alag , N. Bharatham , A. Dong , T. Hills , A. Harikishore , A. A. Widjaja , S. G. Shochat , R. Hui and H. S. Yoon (2009). Crystallographic structure of the tetratricopeptide repeat domain of Plasmodium falciparum FKBP35 and its molecular interaction with Hsp90 C-terminal pentapeptide. Protein Science 18, 21152124.

P. Acharya , R. Kumar and U. Tatu (2007). Chaperoning a cellular upheaval in malaria: heat shock proteins in Plasmodium falciparum. Molecular and Biochemical Parasitology 153, 8594.

S. O. Angel , M. Matrajt and P. C. Echeverria (2012). A review of recent patents on the protozoan parasite HSP90 as a drug target. Recent Patents on Biotechnology 7, 28.

C. A. Ballinger , P. Connell , Y. Wu , Z. Hu , L. J. Thompson , L. Y. Yin and C. Patterson (1999). Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Molecular and Cellular Biology 19, 45354545.

S. Bandhakavi , R. O. McCann , D. E. Hanna and C. V. Glover (2003). A positive feedback loop between protein kinase CKII and Cdc37 promotes the activity of multiple protein kinases. Journal of Biological Chemistry 278, 28292836.

G. Banumathy , V. Singh , S. R. Pavithra and U. Tatu (2003). Heat shock protein 90 function is essential for Plasmodium falciparum growth in human erythrocytes. Journal of Biological Chemistry 278, 1833618345.

R. L. Barent , S. C. Nair , D. C. Carr , Y. Ruan , R. A. Rimerman , J. Fulton , Y. Zhang and D. F. Smith (1998). Analysis of FKBP51/FKBP52 chimeras and mutants for Hsp90 binding and association with progesterone receptor complexes. Molecular Endocrinology 12, 342354.

S. Barik (2006). Immunophilins: for the love of proteins. Cellular and Molecular Life Sciences 63, 28892900.

A. D. Basso , D. B. Solit , G. Chiosis , B. Giri , P. Tsichlis and N. Rosen (2002). Akt forms an intracellular complex with heat shock protein 90 (Hsp90) and Cdc37 and is destabilized by inhibitors of Hsp90 function. Journal of Biological Chemistry 277, 3985839866.

A. Bell , B. Wernli and R. M. Franklin (1994). Roles of peptidyl-prolyl cis-trans isomerase and calcineurin in the mechanisms of antimalarial action of cyclosporin A, FK506, and rapamycin. Biochemical Pharmacology 48, 495503.

N. Bharatham , M. W. Chang and H. S. Yoon (2011). Targeting FK506 binding proteins to fight malarial and bacterial infections: current advances and future perspectives. Current Medicinal Chemistry 18, 18741889.

A. J. Caplan , A. K. Mandal and M. A. Theodoraki (2007). Molecular chaperones and protein kinase quality control. Trends in Cell Biology 17, 8792.

M. S. Chen , A. M. Silverstein , W. B. Pratt and M. Chinkers (1996). The tetratricopeptide repeat domain of protein phosphatase 5 mediates binding to glucocorticoid receptor heterocomplexes and acts as a dominant negative mutant. Journal of Biological Chemistry 271, 3231532320.

S. Chen and D. F. Smith (1998). Hop as an adaptor in the heat shock protein 70 (Hsp70) and hsp90 chaperone machinery. Journal of Biological Chemistry 273, 3519435200.

C. S. Chua , H. Low , K. S. Goo and T. S. Sim (2010). Characterization of Plasmodium falciparum co-chaperone p23: its intrinsic chaperone activity and interaction with Hsp90. Cellular and Molecular Life Sciences 67, 16751686.

C. S. Chua , H. Low , N. Lehming and T. S. Sim (2012). Molecular analysis of Plasmodium falciparum co-chaperone Aha1 supports its interaction with and regulation of Hsp90 in the malaria parasite. International Journal of Biochemistry and Cell Biology 44, 233245.

L. D. D'Andrea and L. Regan (2003). TPR proteins: the versatile helix. Trends in Biochemical Sciences 28, 655662.

C. A. Dickey , A. Kamal , K. Lundgren , N. Klosak , R. M. Bailey , J. Dunmore , P. Ash , S. Shoraka , J. Zlatkovic , C. B. Eckman , C. Patterson , D. W. Dickson , N. S. Nahman Jr., M. Hutton , F. Burrows and L. Petrucelli (2007). The high-affinity HSP90-CHIP complex recognizes and selectively degrades phosphorylated tau client proteins. Journal of Clinical Investigation 117, 648658.

S. Dobson , B. Kar , R. Kumar , B. Adams and S. Barik (2001). A novel tetratricopeptide repeat (TPR) containing PP5 serine/threonine protein phosphatase in the malaria parasite, Plasmodium falciparum. BMC Microbiology 1, 31.

K. J. Dolinski , M. E. Cardenas and J. Heitman (1998). CNS1 encodes an essential p60/Sti1 homolog in Saccharomyces cerevisiae that suppresses cyclophilin 40 mutations and interacts with Hsp90. Molecular and Cellular Biology 18, 73447352.

A. A. Duina , J. A. Marsh and R. F. Gaber (1996). Identification of two CyP-40-like cyclophilins in Saccharomyces cerevisiae, one of which is required for normal growth. Yeast 12, 943952.

K. Eckert , J. M. Saliou , L. Monlezun , A. Vigouroux , N. Atmane , C. Caillat , S. Quevillon-Cheruel , K. Madiona , M. Nicaise , S. Lazereg , A. Van Dorsselaer , S. Sanglier-Cianferani , P. Meyer and S. Morera (2010). The Pih1-Tah1 cochaperone complex inhibits Hsp90 molecular chaperone ATPase activity. Journal of Biological Chemistry 285, 3130431312.

O. Famin and H. Ginsburg (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, 3950.

Y. Fang , A. E. Fliss , J. Rao and A. J. Caplan (1998). SBA1 encodes a yeast hsp90 cochaperone that is homologous to vertebrate p23 proteins. Molecular and Cellular Biology 18, 37273734.

J. Fanghanel and G. Fischer (2004). Insights into the catalytic mechanism of peptidyl prolyl cis/trans isomerases. Frontiers in Bioscience 9, 34533478.

S. Fletcher and A. D. Hamilton (2006). Targeting protein-protein interactions by rational design: mimicry of protein surfaces. Journal of the Royal Society, Interface 3, 215233.

F. Forafonov , O. A. Toogun , I. Grad , E. Suslova , B. C. Freeman and D. Picard (2008). p23/Sba1p protects against Hsp90 inhibitors independently of its intrinsic chaperone activity. Molecular and Cellular Biology 28, 34463456.

A. M. Gaiser , A. Kretzschmar and K. Richter (2010). Cdc37-Hsp90 complexes are responsive to nucleotide-induced conformational changes and binding of further cofactors. Journal of Biological Chemistry 285, 4092140932.

G. Giaever , A. M. Chu , L. Ni , C. Connelly , L. Riles , S. Veronneau , S. Dow , A. Lucau-Danila , K. Anderson , B. Andre , A. P. Arkin , A. Astromoff , M. El-Bakkoury , R. Bangham , R. Benito , S. Brachat , S. Campanaro , M. Curtiss , K. Davis , A. Deutschbauer , K. D. Entian , P. Flaherty , F. Foury , D. J. Garfinkel , M. Gerstein , D. Gotte , U. Guldener , J. H. Hegemann , S. Hempel , Z. Herman , D. F. Jaramillo , D. E. Kelly , S. L. Kelly , P. Kotter , D. LaBonte , D. C. Lamb , N. Lan , H. Liang , H. Liao , L. Liu , C. Luo , M. Lussier , R. Mao , P. Menard , S. L. Ooi , J. L. Revuelta , C. J. Roberts , M. Rose , P. Ross-Macdonald , B. Scherens , G. Schimmack , B. Shafer , D. D. Shoemaker , S. Sookhai-Mahadeo , R. K. Storms , J. N. Strathern , G. Valle , M. Voet , G. Volckaert , C. Y. Wang , T. R. Ward , J. Wilhelmy , E. A. Winzeler , Y. Yang , G. Yen , E. Youngman , K. Yu , H. Bussey , J. D. Boeke , M. Snyder , P. Philippsen , R. W. Davis and M. Johnston (2002). Functional profiling of the Saccharomyces cerevisiae genome. Nature 418, 387391.

G. W. Gitau , P. Mandal , G. L. Blatch , J. Przyborski and A. Shonhai (2012). Characterisation of the Plasmodium falciparum Hsp70-Hsp90 organising protein (PfHop). Cell Stress and Chaperones 17, 191202.

A. Harikishore , M. Niang , S. Rajan , P. R. Preiser and H. S. Yoon (2013). Small molecule Plasmodium FKBP35 inhibitor as a potential antimalaria agent. Scientific Reports 3, 2501.

H. Hieronymus , J. Lamb , K. N. Ross , X. P. Peng , C. Clement , A. Rodina , M. Nieto , J. Du , K. Stegmaier , S. M. Raj , K. N. Maloney , J. Clardy , W. C. Hahn , G. Chiosis and T. R. Golub (2006). Gene expression signature-based chemical genomic prediction identifies a novel class of HSP90 pathway modulators. Cancer Cell 10, 321330.

A. Hombach , G. Ommen , M. Chrobak and J. Clos (2012). The Hsp90-Sti1 interaction is critical for Leishmania donovani proliferation in both life cycle stages. Cellular Microbiology 15, 585600.

J. L. Johnson and C. Brown (2009). Plasticity of the Hsp90 chaperone machine in divergent eukaryotic organisms. Cell Stress and Chaperones 14, 8394.

J. L. Johnson and D. O. Toft (1995). Binding of p23 and hsp90 during assembly with the progesterone receptor. Molecular Endocrinology 9, 670678.

Y. Kadota , B. Amigues , L. Ducassou , H. Madaoui , F. Ochsenbein , R. Guerois and K. Shirasu (2008). Structural and functional analysis of SGT1-HSP90 core complex required for innate immunity in plants. EMBO Reports 9, 12091215.

Y. Kadota , K. Shirasu and R. Guerois (2010). NLR sensors meet at the SGT1-HSP90 crossroad. Trends in Biochemical Sciences 35, 199207.

Y. Kimura , S. L. Rutherford , Y. Miyata , I. Yahara , B. C. Freeman , L. Yue , R. I. Morimoto and S. Lindquist (1997). Cdc37 is a molecular chaperone with specific functions in signal transduction. Genes and Development 11, 17751785.

H. S. Ko , R. Bailey , W. W. Smith , Z. Liu , J. H. Shin , Y. I. Lee , Y. J. Zhang , H. Jiang , C. A. Ross , D. J. Moore , C. Patterson , L. Petrucelli , T. M. Dawson and V. L. Dawson (2009). CHIP regulates leucine-rich repeat kinase-2 ubiquitination, degradation, and toxicity. Proceedings of the National Academy of Sciences USA 106, 28972902.

H. Kosano , B. Stensgard , M. C. Charlesworth , N. McMahon and D. Toft (1998). The assembly of progesterone receptor-hsp90 complexes using purified proteins. Journal of Biological Chemistry 273, 3297332979.

M. Kotaka , H. Ye , R. Alag , G. Hu , Z. Bozdech , P. R. Preiser , H. S. Yoon and J. Lescar (2008). Crystal structure of the FK506 binding domain of Plasmodium falciparum FKBP35 in complex with FK506. Biochemistry 47, 59515961.

R. Kumar , A. Musiyenko and S. Barik (2003). The heat shock protein 90 of Plasmodium falciparum and antimalarial activity of its inhibitor, geldanamycin. Malaria Journal 2, 30.

R. Kumar , B. Adams , A. Musiyenko , O. Shulyayeva and S. Barik (2005). The FK506-binding protein of the malaria parasite, Plasmodium falciparum, is a FK506-sensitive chaperone with FK506-independent calcineurin-inhibitory activity. Molecular and Biochemical Parasitology 141, 163173.

R. Kumar , S. R. Pavithra and U. Tatu (2007). Three-dimensional structure of heat shock protein 90 from Plasmodium falciparum: molecular modelling approach to rational drug design against malaria. Journal of Biosciences 32, 531536.

L. Kundrat and L. Regan (2010). Balance between folding and degradation for Hsp90-dependent client proteins: a key role for CHIP. Biochemistry 49, 74287438.

D. J. LaCount , M. Vignali , R. Chettier , A. Phansalkar , R. Bell , J. R. Hesselberth , L. W. Schoenfeld , I. Ota , S. Sahasrabudhe , C. Kurschner , S. Fields and R. E. Hughes (2005). A protein interaction network of the malaria parasite Plasmodium falciparum. Nature 438, 103107.

L. Lamphere , F. Fiore , X. Xu , L. Brizuela , S. Keezer , C. Sardet , G. F. Draetta and J. Gyuris (1997). Interaction between Cdc37 and Cdk4 in human cells. Oncogene 14, 19992004.

T. Laufen , M. P. Mayer , C. Beisel , D. Klostermeier , A. Mogk , J. Reinstein and B. Bukau (1999). Mechanism of regulation of hsp70 chaperones by DnaJ cochaperones. Proceedings of the National Academy of Sciences USA 96, 54525457.

Y. T. Lee , J. Jacob , W. Michowski , M. Nowotny , J. Kuznicki and W. J. Chazin (2004). Human Sgt1 binds HSP90 through the CHORD-Sgt1 domain and not the tetratricopeptide repeat domain. Journal of Biological Chemistry 279, 1651116517.

J. Li , K. Richter and J. Buchner (2011). Mixed Hsp90-cochaperone complexes are important for the progression of the reaction cycle. Nature Structural and Molecular Biology 18, 6166.

J. Li , J. Soroka and J. Buchner (2012). The Hsp90 chaperone machinery: conformational dynamics and regulation by co-chaperones. Biochimica et Biophysica Acta 1823, 624635.

J. Liu , E. S. Istvan , I. Y. Gluzman , J. Gross and D. E. Goldberg (2006). Plasmodium falciparum ensures its amino acid supply with multiple acquisition pathways and redundant proteolytic enzyme systems. Proceedings of the National Academy of Sciences USA 103, 88408845.

S. MacKinnon , T. Durst , J. T. Arnason , C. Angerhofer , J. Pezzuto , P. E. Sanchez-Vindas , L. J. Poveda and M. Gbeassor (1997). Antimalarial activity of tropical Meliaceae extracts and gedunin derivatives. Journal of Natural Products 60, 336341.

A. K. Mandal , P. Lee , J. A. Chen , N. Nillegoda , A. Heller , S. DiStasio , H. Oen , J. Victor , D. M. Nair , J. L. Brodsky and A. J. Caplan (2007). Cdc37 has distinct roles in protein kinase quality control that protect nascent chains from degradation and promote posttranslational maturation. Journal of Cell Biology 176, 319328.

J. A. Marsh , H. M. Kalton and R. F. Gaber (1998). Cns1 is an essential protein associated with the hsp90 chaperone complex in Saccharomyces cerevisiae that can restore cyclophilin 40-dependent functions in cpr7Delta cells. Molecular and Cellular Biology 18, 73537359.

R. L. Matts , G. E. Brandt , Y. Lu , A. Dixit , M. Mollapour , S. Wang , A. C. Donnelly , L. Neckers , G. Verkhivker and B. S. Blagg (2011). A systematic protocol for the characterization of Hsp90 modulators. Bioorganic and Medicinal Chemistry 19, 684692.

A. Mayor , F. Martinon , T. De Smedt , V. Petrilli and J. Tschopp (2007). A crucial function of SGT1 and HSP90 in inflammasome activity links mammalian and plant innate immune responses. Nature Immunology 8, 497503.

H. McDonough and C. Patterson (2003). CHIP: a link between the chaperone and proteasome systems. Cell Stress and Chaperones 8, 303308.

S. H. McLaughlin , F. Sobott , Z. P. Yao , W. Zhang , P. R. Nielsen , J. G. Grossmann , E. D. Laue , C. V. Robinson and S. E. Jackson (2006). The co-chaperone p23 arrests the Hsp90 ATPase cycle to trap client proteins. Journal of Molecular Biology 356, 746758.

P. Monaghan and A. Bell (2005). A Plasmodium falciparum FK506-binding protein (FKBP) with peptidyl-prolyl cis-trans isomerase and chaperone activities. Molecular and Biochemical Parasitology 139, 185195.

M. A. Morales , R. Watanabe , M. Dacher , P. Chafey , J. Osorio y Fortea , D. A. Scott , S. M. Beverley , G. Ommen , J. Clos , S. Hem , P. Lenormand , J. C. Rousselle , A. Namane and G. F. Spath (2010). Phosphoproteome dynamics reveal heat-shock protein complexes specific to the Leishmania donovani infectious stage. Proceedings of the National Academy of Sciences USA 107, 83818386.

P. Muller , E. Ruckova , P. Halada , P. J. Coates , R. Hrstka , D. P. Lane and B. Vojtesek (2013). C-terminal phosphorylation of Hsp70 and Hsp90 regulates alternate binding to co-chaperones CHIP and HOP to determine cellular protein folding/degradation balances. Oncogene 32, 31013110.

S. Murata , Y. Minami , M. Minami , T. Chiba and K. Tanaka (2001). CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein. EMBO Reports 2, 11331138.

P. Muskett and J. Parker (2003). Role of SGT1 in the regulation of plant R gene signalling. Microbes and Infection 5, 969976.

R. Pallavi , P. Acharya , S. Chandran , J. P. Daily and U. Tatu (2010 a). Chaperone expression profiles correlate with distinct physiological states of Plasmodium falciparum in malaria patients. Malaria Journal 9, 236.

R. Pallavi , N. Roy , R. K. Nageshan , P. Talukdar , S. R. Pavithra , R. Reddy , S. Venketesh , R. Kumar , A. K. Gupta , R. K. Singh , S. C. Yadav and U. Tatu (2010 b). Heat shock protein 90 as a drug target against protozoan infections: biochemical characterization of HSP90 from Plasmodium falciparum and Trypanosoma evansi and evaluation of its inhibitor as a candidate drug. Journal of Biological Chemistry 285, 3796437975.

S. R. Pavithra , G. Banumathy , O. Joy , V. Singh and U. Tatu (2004). Recurrent fever promotes Plasmodium falciparum development in human erythrocytes. Journal of Biological Chemistry 279, 4669246699.

C. A. Patwardhan , A. Fauq , L. B. Peterson , C. Miller , B. S. Blagg and A. Chadli (2013). Gedunin inactivates the co-chaperone p23 protein causing cancer cell death by apoptosis. Journal of Biological Chemistry 288, 73137325.

S. R. Pavithra , R. Kumar and U. Tatu (2007). Systems analysis of chaperone networks in the malarial parasite Plasmodium falciparum. PLoS Comput Biol 3, 17011715.

G. H. Perdew , H. Wiegand , J. P. Vanden Heuvel , C. Mitchell and S. S. Singh (1997). A 50 kilodalton protein associated with raf and pp60(v-src) protein kinases is a mammalian homolog of the cell cycle control protein cdc37. Biochemistry 36, 36003607.

E. R. Pesce , I. L. Cockburn , J. L. Goble , L. L. Stephens and G. L. Blatch (2010). Malaria heat shock proteins: drug targets that chaperone other drug targets. Infectious Disorders Drug Targets 10, 147157.

I. Petersen , R. Eastman and M. Lanzer (2011). Drug-resistant malaria: molecular mechanisms and implications for public health. FEBS Letters 585, 15511562.

D. Picard (2006). Intracellular dynamics of the Hsp90 co-chaperone p23 is dictated by Hsp90. Experimental Cell Research 312, 198204.

P. W. Piper , S. H. Millson , M. Mollapour , B. Panaretou , G. Siligardi , L. H. Pearl and C. Prodromou (2003). Sensitivity to Hsp90-targeting drugs can arise with mutation to the Hsp90 chaperone, cochaperones and plasma membrane ATP binding cassette transporters of yeast. European Journal of Biochemistry 270, 46894695.

F. Pirkl and J. Buchner (2001). Functional analysis of the Hsp90-associated human peptidyl prolyl cis/trans isomerases FKBP51, FKBP52 and Cyp40. Journal of Molecular Biology 308, 795806.

W. B. Pratt (1998). The hsp90-based chaperone system: involvement in signal transduction from a variety of hormone and growth factor receptors. Proceedings of the Society for Experimental Biology and Medicine 217, 420434.

W. B. Pratt and D. O. Toft (1997). Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocrine Reviews 18, 306360.

C. Prodromou (2012). The ‘active life’ of Hsp90 complexes. Biochimica et Biophysica Acta 1823, 614623.

C. Prodromou , G. Siligardi , R. O'Brien , D. N. Woolfson , L. Regan , B. Panaretou , J. E. Ladbury , P. W. Piper and L. H. Pearl (1999). Regulation of Hsp90 ATPase activity by tetratricopeptide repeat (TPR)-domain co-chaperones. EMBO Journal 18, 754762.

C. Prodromou , B. Panaretou , S. Chohan , G. Siligardi , R. O'Brien , J. E. Ladbury , S. M. Roe , P. W. Piper and L. H. Pearl (2000). The ATPase cycle of Hsp90 drives a molecular ‘clamp’ via transient dimerization of the N-terminal domains. EMBO Journal 19, 43834392.

T. Ratajczak , B. K. Ward , C. Cluning and R. K. Allan (2009). Cyclophilin 40: an Hsp90-cochaperone associated with apo-steroid receptors. International Journal of Biochemistry and Cell Biology, 41, 16521655.

A. K. Rochani , M. Singh and U. Tatu (2013). Heat shock protein 90 inhibitors as broad spectrum anti-infectives. Current Pharmaceutical Design 19, 377386.

P. J. Rosenthal (2004). Cysteine proteases of malaria parasites. International Journal for Parasitology 34, 14891499.

R. Russell , A. Wali Karzai , A. F. Mehl and R. McMacken (1999). DnaJ dramatically stimulates ATP hydrolysis by DnaK: insight into targeting of Hsp70 proteins to polypeptide substrates. Biochemistry 38, 41654176.

A. Shonhai (2010). Plasmodial heat shock proteins: targets for chemotherapy. FEMS Immunology and Medical Microbiology 58, 6174.

A. M. Silverstein , M. D. Galigniana , M. S. Chen , J. K. Owens-Grillo , M. Chinkers and W. B. Pratt (1997). Protein phosphatase 5 is a major component of glucocorticoid receptor hsp90 complexes with properties of an FK506-binding immunophilin. Journal of Biological Chemistry 272, 1622416230.

D. A. Stavreva , W. G. Muller , G. L. Hager , C. L. Smith and J. G. McNally (2004). Rapid glucocorticoid receptor exchange at a promoter is coupled to transcription and regulated by chaperones and proteasomes. Molecular and Cellular Biology 24, 26822697.

C. L. Storer , C. A. Dickey , M. D. Galigniana , T. Rein and M. B. Cox (2011). FKBP51 and FKBP52 in signaling and disease. Trends in Endocrinology and Metabolism 22, 481490.

W. Sullivan , B. Stensgard , G. Caucutt , B. Bartha , N. McMahon , E. S. Alnemri , G. Litwack and D. Toft (1997). Nucleotides and two functional states of hsp90. Journal of Biological Chemistry 272, 80078012.

W. P. Sullivan , B. A. Owen and D. O. Toft (2002). The influence of ATP and p23 on the conformation of hsp90. Journal of Biological Chemistry 277, 4594245948.

M. Taipale , D. F. Jarosz and S. Lindquist (2010). HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nature Reviews: Molecular Cell Biology 11, 515528.

A. Takahashi , C. Casais , K. Ichimura and K. Shirasu (2003). HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proceedings of the National Academy of Sciences USA 100, 1177711782.

T. Tanioka , Y. Nakatani , N. Semmyo , M. Murakami and I. Kudo (2000). Molecular identification of cytosolic prostaglandin E2 synthase that is functionally coupled with cyclooxygenase-1 in immediate prostaglandin E2 biosynthesis. Journal of Biological Chemistry 275, 3277532782.

H. Tapia and K. A. Morano (2010). Hsp90 nuclear accumulation in quiescence is linked to chaperone function and spore development in yeast. Molecular Biology of the Cell 21, 6372.

A. M. Vaughan and S. H. Kappe (2012). Malaria vaccine development: persistent challenges. Current Opinion in Immunology 24, 324331.

C. K. Vaughan , M. Mollapour , J. R. Smith , A. Truman , B. Hu , V. M. Good , B. Panaretou , L. Neckers , P. A. Clarke , P. Workman , P. W. Piper , C. Prodromou and L. H. Pearl (2008). Hsp90-dependent activation of protein kinases is regulated by chaperone-targeted dephosphorylation of Cdc37. Molecular Cell 31, 886895.

S. K. Wandinger , M. H. Suhre , H. Wegele and J. Buchner (2006). The phosphatase Ppt1 is a dedicated regulator of the molecular chaperone Hsp90. EMBO Journal 25, 367376.

P. Ward , L. Equinet , J. Packer and C. Doerig (2004). Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote. BMC Genomics 5, 79.

M. F. Wiser and B. Plitt (1987). Plasmodium berghei, P. chabaudi, and P. falciparum: similarities in phosphoproteins and protein kinase activities and their stage specific expression. Experimental Parasitology 64, 328335.

C. Wongsrichanalai and S. R. Meshnick (2008). Declining artesunate-mefloquine efficacy against falciparum malaria on the Cambodia–Thailand border. Emerging Infectious Diseases 14, 716719.

M. Zhang , M. Boter , K. Li , Y. Kadota , B. Panaretou , C. Prodromou , K. Shirasu and L. H. Pearl (2008). Structural and functional coupling of Hsp90- and Sgt1-centred multi-protein complexes. EMBO Journal 27, 27892798.

T. Zhang , Y. Li , Y. Yu , P. Zou , Y. Jiang and D. Sun (2009). Characterization of celastrol to inhibit hsp90 and cdc37 interaction. Journal of Biological Chemistry 284, 3538135389.

R. Zhao and W. A. Houry (2005). Hsp90: a chaperone for protein folding and gene regulation. Biochemistry and Cell Biology, 83, 703710.

R. Zhao , Y. Kakihara , A. Gribun , J. Huen , G. Yang , M. Khanna , M. Costanzo , R. L. Brost , C. Boone , T. R. Hughes , C. M. Yip and W. A. Houry (2008). Molecular chaperone Hsp90 stabilizes Pih1/Nop17 to maintain R2TP complex activity that regulates snoRNA accumulation. Journal of Cell Biology 180, 563578.

A. D. Zuehlke and J. L. Johnson (2012). Chaperoning the chaperone: a role for the co-chaperone Cpr7 in modulating Hsp90 function in Saccharomyces cerevisiae. Genetics 191, 805814.

A. Zurawska , J. Urbanski , J. Matuliene , J. Baraniak , M. P. Klejman , S. Filipek , D. Matulis and P. Bieganowski (2010). Mutations that increase both Hsp90 ATPase activity in vitro and Hsp90 drug resistance in vivo. Biochimica et Biophysica Acta 1803, 575583.

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