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Nematode Hsp90: highly conserved but functionally diverse


Nematodes are amongst the most successful and abundant organisms on the planet with approximately 30 000 species described, although the actual number of species is estimated to be one million or more. Despite sharing a relatively simple and invariant body plan, there is considerable diversity within the phylum. Nematodes have evolved to colonize most ecological niches, and can be free-living or can parasitize plants or animals to the detriment of the host organism. In this review we consider the role of heat shock protein 90 (Hsp90) in the nematode life cycle. We describe studies on Hsp90 in the free-living nematode Caenorhabditis elegans and comparative work on the parasitic species Brugia pahangi, and consider whether a dependence upon Hsp90 can be exploited for the control of parasitic species.

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* Corresponding author: Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Garscube Estate, Bearsden Road, Glasgow, G61 1QH, UK. E-mail:
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P. Abad , J. Gouzy , J. M. Aury , P. Castagnone-Sereno , E. G. Danchin , E. Deleury , L. Perfus-Barbeoch , V. Anthouard , F. Artiguenave , V. C. Blok , M. C. Caillaud and P. M. Coutinho (2008). Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nature Biotechnology 26, 909915.

J. M. Barral , C. C. Bauer , I. Ortiz and H. F. Epstein (1998). Unc-45 mutations in Caenorhabditis elegans implicate a CRO1/She4p-like domain in myosin assembly. Journal of Cell Biology 143, 12151225.

J. M. Barral , A. H. Hutagalung , A. Brinker , F. U. Hartl and H. F. Epstein (2002). Role of the myosin assembly protein UNC-45 as a molecular chaperone for myosin. Science 295, 669671. doi: 10.1126/science.1066648.

M. L. Blaxter , P. De Ley , J. R. Garey , L. X. Liu , P. Scheldeman , A. Vierstraete , J. R. Vanfleteren , L. Y. Mackey , M. Dorris , L. M. Frisse , J. T. Vida and W. K. Thomas (1998). A molecular evolutionary framework for the phylum Nematoda. Nature 392, 7175. doi: 10.1038/32160.

C. Britton and L. Murray (2002). A cathepsin L protease essential for Caenorhabditis elegans embryogenesis is functionally conserved in parasitic nematodes. Molecular and Biochemical Parasitology 122, 2133.

A. R. Burns , I. M. Wallace , J. Wildenhain , M. Tyers , G. Giaever , G. D. Bader , C. Nislow , S. R. Cutler and P. J. Roy (2010). A predictive model for drug bioaccumulation and bioactivity in Caenorhabditis elegans. Nature Chemical Biology 6, 549557. doi: 10.1038/nchembio.380.

E. P. Candido , D. Jones , D. K. Dixon , R. W. Graham , R. H. Russnak and R. J. Kay (1989). Structure, organization, and expression of the 16-kDa heat shock gene family of Caenorhabditis elegans. Genome 31, 690697.

P. Coumailleau , B. Billoud , P. Sourrouille , N. Moreau and N. Angelier (1995). Evidence for a 90 kDa heat-shock protein gene expression in the amphibian oocyte. Developmental Biology 168, 247258. doi: 10.1006/dbio.1995.1077.

A. Couthier , J. Smith , P. Mcgarr , B. Craig and J. S. Gilleard (2004). Ectopic expression of a Haemonchus contortus GATA transcription factor in Caenorhabditis elegans reveals conserved function in spite of extensive sequence divergence. Molecular and Biochemical Parasitology 133, 241253.

B. K. Dalley and M. Golomb (1992). Gene expression in the Caenorhabditis elegans dauer larva: developmental regulation of Hsp90 and other genes. Developmental Biology 151, 8090.

C. L. David , H. E. Smith , D. A. Raynes , E. J. Pulcini and L. Whitesell (2003). Expression of a unique drug-resistant Hsp90 ortholog by the nematode Caenorhabditis elegans. Cell Stress and Chaperones 8, 93104.

C. A. Desjardins , G. C. Cerqueira , J. M. Goldberg , J. C. Dunning Hotopp , B. J. Haas , J. Zucker , J. M. Ribeiro , S. Saif , J. Z. Levin , L. Fan , Q. Zeng , C. Russ , J. R. Wortman , D. L. Fink , B. W. Birren and T. B. Nutman (2013). Genomics of Loa loa, a Wolbachia-free filarial parasite of humans. Nature Genetics 45, 495500. doi: 10.1038/ng.2585.

E. Devaney , V. Gillan , I. Wheatley , J. Jenson , R. O'connor and P. Balmer (2002). Interleukin-4 influences the production of microfilariae in a mouse model of Brugia infection. Parasite Immunology 24, 2937.

E. Devaney , K. O'Neill , W. Harnett , L. Whitesell and J. H. Kinnaird (2005). Hsp90 is essential in the filarial nematode Brugia pahangi. International Journal for Parasitology 35, 627636.

C. Dieterich , S. W. Clifton , L. N. Schuster , A. Chinwalla , K. Delehaunty , I. Dinkelacker , L. Fulton , R. Fulton , J. Godfrey , P. Minx , M. Mitreva , W. Roeseler , H. Tian , H. Witte , S. P. Yang , R. K. Wilson and R. J. Sommer (2008). The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nature Genetics 40, 11931198.

D. Dupuy , N. Bertin , C. A. Hidalgo , K. Venkatesan , D. Tu , D. Lee , J. Rosenberg , N. Svrzikapa , A. Blanc , A. Carnec , A. R. Carvunis , R. Pulak , J. Shingles , J. Reece-Hoyes , R. Hunt-Newbury , R. Viveiros , W. A. Mohler , M. Tasan , F. P. Roth , C. Le Peuch , I. A. Hope , R. Johnsen , D. G. Moerman , A. L. Barabasi , D. Baillie and M. Vidal (2007). Genome-scale analysis of in vivo spatiotemporal promoter activity in Caenorhabditis elegans . Nature Biotechnology 25, 663668. doi: 10.1038/nbt1305.

S. A. Eccles , A. Massey , F. I. Raynaud , S. Y. Sharp , G. Box , M. Valenti , L. Patterson , A. De Haven Brandon , S. Gowan , F. Boxall , W. Aherne , M. Rowlands , A. Hayes , V. Martins , F. Urban , K. Boxall , C. Prodromou , L. Pearl , K. James , T. P. Matthews , K. M. Cheung , A. Kalusa , K. Jones , E. McDonald , X. Barril , P. A. Brough , J. E. Cansfield , B. Dymock , M. J. Drysdale , H. Finch , R. Howes , R. E. Hubbard , A. Surgenor , P. Webb , M. Wood , L. Wright and P. Workman (2008). NVP-AUY922: a novel heat shock protein 90 inhibitor active against xenograft tumor growth, angiogenesis, and metastasis. Cancer Research 68, 28502860. doi: 10.1158/0008-5472.can-07-5256.

B. K. Eustace and D. G. Jay (2004). Extracellular roles for the molecular chaperone, hsp90. Cell Cycle 3, 10981100.

B. K. Eustace , T. Sakurai , J. K. Stewart , D. Yimlamai , C. Unger , C. Zehetmeier , B. Lain , C. Torella , S. W. Henning , G. Beste , B. T. Scroggins , L. Neckers , L. L. Ilag and D. G. Jay (2004). Functional proteomic screens reveal an essential extracellular role for hsp90 alpha in cancer cell invasiveness. Nature Cell Biology 6, 507514. doi: 10.1038/ncb1131.

S. J. Felts , L. M. Karnitz and D. O. Toft (2007). Functioning of the Hsp90 machine in chaperoning checkpoint kinase I (Chk1) and the progesterone receptor (PR). Cell Stress and Chaperones 12, 353363.

A. M. Gaiser , F. Brandt and K. Richter (2009). The non-canonical Hop protein from Caenorhabditis elegans exerts essential functions and forms binary complexes with either Hsc70 or Hsp90. Journal of Molecular Biology 391, 621634. doi: 10.1016/j.jmb.2009.06.051.

E. B. Garon , R. S. Finn , H. Hamidi , J. Dering , S. Pitts , N. Kamranpour , A. J. Desai , W. Hosmer , S. Ide , E. Avsar , M. R. Jensen , C. Quadt , M. Liu , S. M. Dubinett and D. J. Slamon (2013). The HSP90 inhibitor NVP-AUY922 potently inhibits non-small cell lung cancer growth. Molecular Cancer Therapy 12, 890900. doi: 10.1158/1535-7163.mct-12-0998.

V. K. Gangaraju , H. Yin , M. M. Weiner , J. Wang , X. A. Huang and H. Lin (2011). Drosophila Piwi functions in Hsp90-mediated suppression of phenotypic variation. Nature Genetics 43, 153158. doi: 10.1038/ng.743.

T. G. Geary , K. Woo , J. S. McCarthy , C. D. Mackenzie , J. Horton , R. K. Prichard , N. R. De Silva , P. L. Olliaro , J. K. Lazdins-Helds , D. A. Engels and D. A. Bundy (2010). Unresolved issues in anthelmintic pharmacology for helminthiases of humans. International Journal for Parasitology 40, 113. doi: 10.1016/j.ijpara.2009.11.001.

E. Ghedin , S. Wang , D. Spiro , E. Caler , Q. Zhao , J. Crabtree , J. E. Allen , A. L. Delcher , D. B. Guiliano , D. Miranda-Saavedra , S. V. Angiuoli and T. Creasy (2007). Draft genome of the filarial nematode parasite Brugia malayi. Science 317, 17561760.

V. Gillan , K. Maitland , G. McCormack , N. A. Nik Him and E. Devaney (2009). Functional genomics of hsp-90 in parasitic and free-living nematodes. International Journal for Parasitology 39, 10711081. doi: S0020-7519(09)00167-2 [pii]10.1016/j.ijpara.2009.02.024.

V. Gillan , K. O'Neill , K. Maitland , F. M. Sverdrup and E. Devaney (2014). A repurposing strategy for Hsp90 inhibitors demonstrates their potency against filarial nematodes. PLoS Neglected Tropical Disease 8, e2699. doi: 10.1371/journal.pntd.0002699.

J. S. Gilleard (2006). Understanding anthelmintic resistance: the need for genomics and genetics. International Journal for Parasitology 36, 12271239. doi: 10.1016/j.ijpara.2006.06.010.

C. Godel , S. Kumar , G. Koutsovoulos , P. Ludin , D. Nilsson , F. Comandatore , N. Wrobel , M. Thompson , C. D. Schmid , S. Goto , F. Bringaud , A. Wolstenholme , C. Bandi , C. Epe , R. Kaminsky , M. Blaxter and P. Maser (2012). The genome of the heartworm, Dirofilaria immitis, reveals drug and vaccine targets. Journal of the Federation of American Societies for Experimental Biology 26, 46504661. doi: 10.1096/fj.12-205096.

J. W. Golden and D. L. Riddle (1982). A pheromone influences larval development in the nematode Caenorhabditis elegans. Science 218, 578580.

A. Harst , H. Lin and W. M. Obermann (2005). Aha1 competes with Hop, p50 and p23 for binding to the molecular chaperone Hsp90 and contributes to kinase and hormone receptor activation. Biochemical Journal 387, 789796. doi: 10.1042/BJ20041283.

S. Hashmi , Y. Wang , R. S. Parhar , K. S. Collison , W. Conca , F. Al-Mohanna and R. Gaugler (2013). A C. elegans model to study human metabolic regulation. Nutrition and Metabolism 10, 31. doi: 10.1186/1743-7075-10-31.

V. Haslbeck , J. M. Eckl , C. J. Kaiser , K. Papsdorf , M. Hessling and K. Richter (2013). Chaperone-interacting TPR proteins in Caenorhabditis elegans. Journal of Molecular Biology 425, 29222939. doi: 10.1016/j.jmb.2013.05.019.

N. A. Him , V. Gillan , R. D. Emes , K. Maitland and E. Devaney (2009). Hsp-90 and the biology of nematodes. BMC Evolutionary Biology 9, 254. doi: 10.1186/1471-2148-9-254.

A. Hoerauf (2008). Filariasis: new drugs and new opportunities for lymphatic filariasis and onchocerciasis. Current Opinion in Infectious Disease 21, 673681. doi: 10.1097/QCO.0b013e328315cde7.

T. Inoue , K. Takamura , H. Yamae , N. Ise , M. Kawakami , Y. Tabuse , J. Miwa and Y. Yamaguchi (2003). Caenorhabditis elegans DAF-21 (Hsp90) is characteristically and predominantly expressed in germline cells: spatial and temporal analysis. Development Growth and Differentiation 45, 369376.

T. Inoue , K. Hirata , Y. Kuwana , M. Fujita , J. Miwa , R. Roy and Y. Yamaguchi (2006). Cell cycle control by daf-21/Hsp90 at the first meiotic prophase/metaphase boundary during oogenesis in Caenorhabditis elegans. Development Growth and Differentiation 48, 2532. doi: 10.1111/j.1440-169X.2006.00841.x.

S. Iwasaki , M. Kobayashi , M. Yoda , Y. Sakaguchi , S. Katsuma , T. Suzuki and Y. Tomari (2010). Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes. Molecular Cell 39, 292299. doi: 10.1016/j.molcel.2010.05.015.

N. Izumi , S. Kawaoka , S. Yasuhara , Y. Suzuki , S. Sugano , S. Katsuma and Y. Tomari (2013). Hsp90 facilitates accurate loading of precursor piRNAs into Piwi proteins. RNA 19, 896901. doi: 10.1261/rna.037200.112.

R. M. Jecock and E. Devaney (1992). Expression of small heat shock proteins by the third-stage larva of Brugia pahangi. Molecular and Biochemical Parasitology 56, 219226.

P. Y. Jeong , K. Na , M. J. Jeong , D. Chitwood , Y. H. Shim and Y. K. Paik (2009). Proteomic analysis of Caenorhabditis elegans. Methods in Molecular Biology 519, 145169. doi: 10.1007/978-1-59745-281-6_10.

A. R. Jex , S. Liu , B. Li , N. D. Young , R. S. Hall , Y. Li , L. Yang , N. Zeng , X. Xu , Z. Xiong , F. Chen , X. Wu , G. Zhang , X. Fang , Y. Kang , G. A. Anderson , T. W. Harris , B. E. Campbell , J. Vlaminck , T. Wang , C. Cantacessi , E. M. Schwarz , S. Ranganathan , P. Geldhof , P. Nejsum , P. W. Sternberg , H. Yang , J. Wang , J. Wang and R. B. Gasser (2011). Ascaris suum draft genome. Nature 479, 529533. doi: 10.1038/nature10553.

J. L. Johnson and C. Brown (2009). Plasticity of the Hsp90 chaperone machine in divergent eukaryotic organisms. Cell Stress and Chaperones 14, 8394. doi: 10.1007/s12192-008-0058-9.

D. Jones , D. K. Dixon , R. W. Graham and E. P. Candido (1989). Differential regulation of closely related members of the hsp16 gene family in Caenorhabditis elegans . DNA 8, 481490.

S. J. Jones , D. L. Riddle , A. T. Pouzyrev , V. E. Velculescu , L. Hillier , S. R. Eddy , S. L. Stricklin , D. L. Baillie , R. Waterston and M. A. Marra (2001). Changes in gene expression associated with developmental arrest and longevity in Caenorhabditis elegans. Genome Research 11, 13461352. doi: 10.1101/gr.184401.

A. Kamal , L. Thao , J. Sensintaffar , L. Zhang , M. F. Boehm , L. C. Fritz and F. J. Burrows (2003). A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 425, 407410. doi: 10.1038/nature01913.

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. doi: 10.1186/1475-2875-2-30.

S. Kumari , C. D. Lillibridge , M. Bakeer , R. C. Lowrie Jr., K. Jayaraman and M. T. Philipp (1994). Brugia malayi: the diagnostic potential of recombinant excretory/secretory antigens. Experimental Parasitology 79, 489505. doi: 10.1006/expr.1994.1110.

M. S. Kwa , J. G. Veenstra , M. Van Dijk and M. H. Roos (1995). Beta-tubulin genes from the parasitic nematode Haemonchus contortus modulate drug resistance in Caenorhabditis elegans. Journal of Molecular Biology 246, 500510. doi: 10.1006/jmbi.1994.0102.

R. Laing , T. Kikuchi , A. Martinelli , I. J. Tsai , R. N. Beech , E. Redman , N. Holroyd , D. J. Bartley , H. Beasley , C. Britton , D. Curran , E. Devaney , A. Gilabert , M. Hunt , F. Jackson , S. L. Johnston , I. Kryukov , K. Li , A. A. Morrison , A. J. Reid , N. Sargison , G. I. Saunders , J. D. Wasmuth , A. Wolstenholme , M. Berriman , J. S. Gilleard and J. A. Cotton (2013). The genome and transcriptome of Haemonchus contortus, a key model parasite for drug and vaccine discovery. Genome Biology 14, R88. doi: 10.1186/gb-2013-14-8-r88.

M. L. Landsverk , S. Li , A. H. Hutagalung , A. Najafov , T. Hoppe , J. M. Barral and H. F. Epstein (2007). The UNC-45 chaperone mediates sarcomere assembly through myosin degradation in Caenorhabditis elegans. Journal of Cell Biology 177, 205210. doi: 10.1083/jcb.200607084.

N. J. Martinez and R. I. Gregory (2013). Argonaute2 expression is post-transcriptionally coupled to microRNA abundance. RNA 19, 605612. doi: 10.1261/rna.036434.112.

H. C. Massey Jr., M. K. Bhopale , X. Li , M. Castelletto and J. B. Lok (2006). The fork head transcription factor FKTF-1b from Strongyloides stercoralis restores DAF-16 developmental function to mutant Caenorhabditis elegans. International Journal for Parasitology 36, 347352. doi: 10.1016/j.ijpara.2005.11.007.

S. H. Millson , C. S. Chua , S. M. Roe , S. Polier , S. Solovieva , L. H. Pearl , T. S. Sim , C. Prodromou and P. W. Piper (2011). Features of the Streptomyces hygroscopicus HtpG reveal how partial geldanamycin resistance can arise with mutation to the ATP binding pocket of a eukaryotic Hsp90. Journal of the Federation of American Societies for Experimental Biology 25, 38283837. doi: 10.1096/fj.11-188821.

M. Mitreva , D. P. Jasmer , D. S. Zarlenga , Z. Wang , S. Abubucker , J. Martin , C. M. Taylor , Y. Yin , L. Fulton , P. Minx , S. P. Yang , W. C. Warren , R. S. Fulton , V. Bhonagiri , X. Zhang , K. Hallsworth-Pepin , S. W. Clifton , J. P. McCarter , J. Appleton , E. R. Mardis and R. K. Wilson (2011). The draft genome of the parasitic nematode Trichinella spiralis. Nature Genetics 43, 228235. doi: 10.1038/ng.769.

T. Miyoshi , A. Takeuchi , H. Siomi and M. C. Siomi (2010). A direct role for Hsp90 in pre-RISC formation in Drosophila . Nature Structural and Molecular Biology 17, 10241026. doi: 10.1038/nsmb.1875.

D. H. Molyneux , M. Bradley , A. Hoerauf , D. Kyelem and M. J. Taylor (2003). Mass drug treatment for lymphatic filariasis and onchocerciasis. Trends in Parasitology 19, 516522.

K. Moulick , J. H. Ahn , H. Zong , A. Rodina , L. Cerchietti , E. M. Gomes Dagama , E. Caldas-Lopes , K. Beebe , F. Perna , K. Hatzi , L. P. Vu , X. Zhao , D. Zatorska , T. Taldone , P. Smith-Jones , M. Alpaugh , S. S. Gross , N. Pillarsetty , T. Ku , J. S. Lewis , S. M. Larson , R. Levine , H. Erdjument-Bromage , M. L. Guzman , S. D. Nimer , A. Melnick , L. Neckers and G. Chiosis (2011). Affinity-based proteomics reveal cancer-specific networks coordinated by Hsp90. Nature Chemical Biology 7, 818826. doi: 10.1038/nchembio.670.

L. Neckers , E. Mimnaugh and T. W. Schulte (1999). Hsp90 as an anti-cancer target. Drug Resistance Update 2, 165172. doi: 10.1054/drup.1999.0082.

W. Ni , A. H. Hutagalung , S. Li and H. F. Epstein (2011). The myosin-binding UCS domain but not the Hsp90-binding TPR domain of the UNC-45 chaperone is essential for function in Caenorhabditis elegans. Journal of Cell Science 124, 31643173. doi: 10.1242/jcs.087320.

J. M. Nicol , S. J. Turner , D. L. Coyne , L. Den Nijs , S. Hockland and Z. T. Maafi (2011). Current nematode threats to world agriculture. In Genomics and Molecular Genetics of Plant-Nematode Interactions (ed. J. Jones , G. Gheysen and C. Fenoll ), pp. 2143. Springer, Dordrecht, the Netherlands.

C. H. Opperman , D. M. Bird , V. M. Williamson , D. S. Rokhsar , M. Burke , J. Cohn , J. Cromer , S. Diener , J. Gajan , S. Graham , T. D. Houfek , Q. Liu , T. Mitros , J. Schaff , R. Schaffer , E. Scholl , B. R. Sosinski , V. P. Thomas and E. Windham (2008). Sequence and genetic map of Meloidogyne hapla: a compact nematode genome for plant parasitism. Proceedings of the National Academy of Sciences USA 105, 1480214807.

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). 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. doi: 10.1074/jbc.M110.155317.

G. Palmer , J. F. Louvion , R. S. Tibbetts , D. M. Engman and D. Picard (1995). Trypanosoma cruzi heat-shock protein 90 can functionally complement yeast. Molecular and Biochemical Parasitology 70, 199202.

L. H. Pearl and C. Prodromou (2006). Structure and mechanism of the Hsp90 molecular chaperone machinery. Annual Review of Biochemistry 75, 271294. doi: 10.1146/annurev.biochem.75.103004.142738.

A. L. Petersen , C. E. Guedes , C. L. Versoza , J. G. Lima , L. A. De Freitas , V. M. Borges and P. S. Veras (2012). 17-AAG kills intracellular Leishmania amazonensis while reducing inflammatory responses in infected macrophages. PLoS One 7, e49496. doi: 10.1371/journal.pone.0049496.

F. Piano , A. J. Schetter , M. Mangone , L. Stein and K. J. Kemphues (2000). RNAi analysis of genes expressed in the ovary of Caenorhabditis elegans. Current Biology 10, 16191622.

P. W. Piper , B. Panaretou , S. H. Millson , A. Trumana , M. Mollapour , L. H. Pearl and C. Prodromou (2003). Yeast is selectively hypersensitised to heat shock protein 90 (Hsp90)-targeting drugs with heterologous expression of the human Hsp90beta, a property that can be exploited in screens for new Hsp90 chaperone inhibitors. Gene 302, 165170.

W. B. Pratt , M. D. Galigniana , J. M. Harrell and D. B. Defranco (2004). Role of Hsp90 and the Hsp90-binding immunophilins in signalling protein movement. Cell Signalling 16, 857872. doi: 10.1016/j.cellsig.2004.02.004.

R. K. Prichard , M. G. Basanez , B. A. Boatin , J. S. McCarthy , H. H. Garcia , G. J. Yang , B. Sripa and S. Lustigman (2012). A research agenda for helminth diseases of humans: intervention for control and elimination. PLoS Neglected Tropical Diseases 6, e1549. doi: 10.1371/journal.pntd.0001549.

C. Prodromou , J. M. Nuttall , S. H. Millson , S. M. Roe , T. S. Sim , D. Tan , P. Workman , L. H. Pearl and P. W. Piper (2009). Structural basis of the radicicol resistance displayed by a fungal Hsp90. ACS Chemical Biology 4, 289297. doi: 10.1021/cb9000316.

R. Rae , M. Riebesell , I. Dinkelacker , Q. Wang , M. Herrmann , A. M. Weller , C. Dieterich and R. J. Sommer (2008). Isolation of naturally associated bacteria of necromenic Pristionchus nematodes and fitness consequences. Journal of Experimental Biology 211, 19271936. doi: 10.1242/jeb.014944.

D. L. Riggs , M. B. Cox , J. Cheung-Flynn , V. Prapapanich , P. E. Carrigan and D. F. Smith (2004). Functional specificity of co-chaperone interactions with Hsp90 client proteins. Critical Reviews in Biochemistry and Molecular Biology 39, 279295. doi: 10.1080/10409230490892513.

D. M. Ruden and X. Y. Lu (2008). Hsp90 affecting chromatin remodeling might explain transgenerational epigenetic inheritance in Drosophila. Current Genomics 9, 500508. doi: 10.2174/138920208786241207.

L. C. Russell , S. R. Whitt , M. S. Chen and M. Chinkers (1999). Identification of conserved residues required for the binding of a tetratricopeptide repeat domain to heat shock protein 90. Journal of Biological Chemistry 274, 2006020063.

S. L. Rutherford and S. Lindquist (1998). Hsp90 as a capacitor for morphological evolution. Nature 396, 336342. doi: 10.1038/24550.

R. Sawarkar , C. Sievers and R. Paro (2012). Hsp90 globally targets paused RNA polymerase to regulate gene expression in response to environmental stimuli. Cell 149, 807818.

C. Scheufler , A. Brinker , G. Bourenkov , S. Pegoraro , L. Moroder , H. Bartunik , F. U. Hartl and I. Moarefi (2000). Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101, 199210. doi: 10.1016/S0092-8674(00)80830-2.

E. M. Schwarz , P. K. Korhonen , B. E. Campbell , N. D. Young , A. R. Jex , A. Jabbar , R. S. Hall , A. Mondal , A. C. Howe , J. Pell , A. Hofmann , P. R. Boag , X. Q. Zhu , T. R. Gregory , A. Loukas , B. A. Williams , I. Antoshechkin , C. T. Brown , P. W. Sternberg and R. B. Gasser (2013). The genome and developmental transcriptome of the strongylid nematode Haemonchus contortus. Genome Biology 14, R89. doi: 10.1186/gb-2013-14-8-r89.

D. Shahinas , M. Liang , A. Datti and D. R. Pillai (2010). A repurposing strategy identifies novel synergistic inhibitors of Plasmodium falciparum heat shock protein 90. Journal of Medicinal Chemistry 53, 35523557. doi: 10.1021/jm901796s.

D. Shahinas , A. Folefoc , T. Taldone , G. Chiosis , I. Crandall and D. R. Pillai (2013). A purine analog synergizes with chloroquine (CQ) by targeting Plasmodium falciparum Hsp90 (PfHsp90). PLoS One 8, e75446. doi: 10.1371/journal.pone.0075446.

D. F. Smith and D. O. Toft (2008). Minireview: the intersection of steroid receptors with molecular chaperones: observations and questions. Molecular Endocrinology 22, 22292240. doi: 10.1210/me.2008-0089.

V. Specchia , L. Piacentini , P. Tritto , L. Fanti , R. D'Alessandro , G. Palumbo , S. Pimpinelli and M. P. Bozzetti (2010). Hsp90 prevents phenotypic variation by suppressing the mutagenic activity of transposons. Nature 463, 662665. doi: 10.1038/nature08739.

L. D. Stein , Z. Bao , D. Blasiar , T. Blumenthal , M. R. Brent , N. Chen , A. Chinwalla , L. Clarke , C. Clee , A. Coghlan , A. Coulson , P. D'Eustachio , D. H. Fitch , L. A. Fulton , R. E. Fulton , S. Griffiths-Jones , T. W. Harris , L. W. Hillier , R. Kamath , P. E. Kuwabara , E. R. Mardis , M. A. Marra , T. L. Miner , P. Minx , J. C. Mullikin , R. W. Plumb , J. Rogers , J. E. Schein , M. Sohrmann , J. Spieth , J. E. Stajich , C. Wei , D. Willey , R. K. Wilson , R. Durbin and R. H. Waterston (2003). The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biology 1, E45. doi: 10.1371/journal.pbio.0000045.

T. Taldone , V. Gillan , W. Sun , A. Rodina , P. Patel , K. Maitland , K. O'Neill , G. Chiosis and E. Devaney (2010). Assay strategies for the discovery and validation of therapeutics targeting Brugia pahangi Hsp90. PLoS Neglected Tropical Diseases 4, e714. doi: 10.1371/journal.pntd.0000714.

T. Taldone , D. Zatorska , P. D. Patel , H. Zong , A. Rodina , J. H. Ahn , K. Moulick , M. L. Guzman and G. Chiosis (2011). Design, synthesis, and evaluation of small molecule Hsp90 probes. Bioorganic and Medicinal Chemistry 19, 26032614. doi: 10.1016/j.bmc.2011.03.013.

Y. T. Tang , X. Gao , B. A. Rosa , S. Abubucker , K. Hallsworth-Pepin , J. Martin , R. Tyagi , E. Heizer , X. Zhang , V. Bhonagiri-Palsikar , P. Minx , W. C. Warren , Q. Wang , B. Zhan , P. J. Hotez , P. W. Sternberg , A. Dougall , S. T. Gaze , J. Mulvenna , J. Sotillo , S. Ranganathan , E. M. Rabelo , R. K. Wilson , P. L. Felgner , J. Bethony , J. M. Hawdon , R. B. Gasser , A. Loukas and M. Mitreva (2014). Genome of the human hookworm Necator americanus. Nature Genetics 46, 261269. doi: 10.1038/ng.2875.

M. Tariq , U. Nussbaumer , Y. Chen , C. Beisel and R. Paro (2009). Trithorax requires Hsp90 for maintenance of active chromatin at sites of gene expression. Proceedings of the National Academy of Sciences USA 106, 11571162. doi: 10.1073/pnas.0809669106.

F. J. Thompson , A. C. Cockroft , I. Wheatley , C. Britton and E. Devaney (2001). Heat shock and developmental expression of hsp83 in the filarial nematode Brugia pahangi. European Journal of Biochemistry 268, 58085815.

J. Vercruysse , B. Levecke and R. Prichard (2012). Human soil-transmitted helminths: implications of mass drug administration. Current Opinion in Infectious Disease 25, 703708. doi: 10.1097/QCO.0b013e328358993a.

D. Wenkert , B. Ramirez , Y. Shen and M. A. Kron (2010). In vitro activity of geldanamycin derivatives against Schistosoma japonicum and Brugia malayi. Journal of Parasitology Research 2010, 716498. doi: 10.1155/2010/716498.

D. Wider , M. P. Peli-Gulli , P. A. Briand , U. Tatu and D. Picard (2009). The complementation of yeast with human or Plasmodium falciparum Hsp90 confers differential inhibitor sensitivities. Molecular and Biochemical Parasitology 164, 147152.

C. Wu (1995). Heat shock transcription factors: structure and regulation. Annual Review of Cell Developmental Biology 11, 441469. doi: 10.1146/annurev.cb.11.110195.002301.

H. Xiao and J. T. Lis (1989). Heat shock and developmental regulation of the Drosophila melanogaster hsp83 gene. Molecular Cell Biology 9, 17461753.

Y. Yang , W. Qin , D. Zarlenga , L. Cao and G. Tian (2013). TsDAF-21/Hsp90 is expressed in all examined stages of Trichinella spiralis. Veterinary Parasitology 194, 171174. doi: 10.1016/j.vetpar.2013.01.048.

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