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Nematode Hsp90: highly conserved but functionally diverse

Published online by Cambridge University Press:  10 April 2014

VICTORIA GILLAN  and
EILEEN DEVANEY
VICTORIA GILLAN*
Affiliation:
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
EILEEN DEVANEY
Affiliation:
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
*
* 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: victoria.gillan@glasgow.ac.uk
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Summary

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.

Keywords

NematodesCaenorhabditis elegansBrugia pahangiHsp90heat shock proteinco-chaperone
Type
Special Issue Article
Information
Parasitology , Volume 141 , Special Issue 9: Heat shock proteins as drug targets in infectious diseases , August 2014 , pp. 1203 - 1215
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Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Abad, P., Gouzy, J., Aury, J. M., Castagnone-Sereno, P., Danchin, E. G., Deleury, E., Perfus-Barbeoch, L., Anthouard, V., Artiguenave, F., Blok, V. C., Caillaud, M. C. and Coutinho, P. M. (2008). Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita . Nature Biotechnology 26, 909–915.CrossRefGoogle ScholarPubMed
Barral, J. M., Bauer, C. C., Ortiz, I. and Epstein, H. F. (1998). Unc-45 mutations in Caenorhabditis elegans implicate a CRO1/She4p-like domain in myosin assembly. Journal of Cell Biology 143, 1215–1225.CrossRefGoogle ScholarPubMed
Barral, J. M., Hutagalung, A. H., Brinker, A., Hartl, F. U. and Epstein, H. F. (2002). Role of the myosin assembly protein UNC-45 as a molecular chaperone for myosin. Science 295, 669–671. doi: 10.1126/science.1066648.CrossRefGoogle ScholarPubMed
Birnby, D. A., Link, E. M., Vowels, J. J., Tian, H., Colacurcio, P. L. and Thomas, J. H. (2000). A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in Caenorhabditis elegans . Genetics 155, 85–104.CrossRefGoogle ScholarPubMed
Blaxter, M. L., De Ley, P., Garey, J. R., Liu, L. X., Scheldeman, P., Vierstraete, A., Vanfleteren, J. R., Mackey, L. Y., Dorris, M., Frisse, L. M., Vida, J. T. and Thomas, W. K. (1998). A molecular evolutionary framework for the phylum Nematoda. Nature 392, 71–75. doi: 10.1038/32160.CrossRefGoogle ScholarPubMed
Britton, C. and Murray, L. (2002). A cathepsin L protease essential for Caenorhabditis elegans embryogenesis is functionally conserved in parasitic nematodes. Molecular and Biochemical Parasitology 122, 21–33.CrossRefGoogle ScholarPubMed
Burns, A. R., Wallace, I. M., Wildenhain, J., Tyers, M., Giaever, G., Bader, G. D., Nislow, C., Cutler, S. R. and Roy, P. J. (2010). A predictive model for drug bioaccumulation and bioactivity in Caenorhabditis elegans . Nature Chemical Biology 6, 549–557. doi: 10.1038/nchembio.380.CrossRefGoogle ScholarPubMed
Candido, E. P., Jones, D., Dixon, D. K., Graham, R. W., Russnak, R. H. and Kay, R. J. (1989). Structure, organization, and expression of the 16-kDa heat shock gene family of Caenorhabditis elegans . Genome 31, 690–697.CrossRefGoogle ScholarPubMed
Chiosis, G. and Tao, H. (2006). Purine-scaffold Hsp90 inhibitors. IDrugs 9, 778–782.Google ScholarPubMed
Coumailleau, P., Billoud, B., Sourrouille, P., Moreau, N. and Angelier, N. (1995). Evidence for a 90 kDa heat-shock protein gene expression in the amphibian oocyte. Developmental Biology 168, 247–258. doi: 10.1006/dbio.1995.1077.CrossRefGoogle ScholarPubMed
Couthier, A., Smith, J., Mcgarr, P., Craig, B. and Gilleard, J. S. (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, 241–253.CrossRefGoogle ScholarPubMed
Dalley, B. K. and Golomb, M. (1992). Gene expression in the Caenorhabditis elegans dauer larva: developmental regulation of Hsp90 and other genes. Developmental Biology 151, 80–90.CrossRefGoogle ScholarPubMed
David, C. L., Smith, H. E., Raynes, D. A., Pulcini, E. J. and Whitesell, L. (2003). Expression of a unique drug-resistant Hsp90 ortholog by the nematode Caenorhabditis elegans . Cell Stress and Chaperones 8, 93–104.2.0.CO;2>CrossRefGoogle ScholarPubMed
Desjardins, C. A., Cerqueira, G. C., Goldberg, J. M., Dunning Hotopp, J. C., Haas, B. J., Zucker, J., Ribeiro, J. M., Saif, S., Levin, J. Z., Fan, L., Zeng, Q., Russ, C., Wortman, J. R., Fink, D. L., Birren, B. W. and Nutman, T. B. (2013). Genomics of Loa loa, a Wolbachia-free filarial parasite of humans. Nature Genetics 45, 495–500. doi: 10.1038/ng.2585.CrossRefGoogle ScholarPubMed
Devaney, E., Gillan, V., Wheatley, I., Jenson, J., O'connor, R. and Balmer, P. (2002). Interleukin-4 influences the production of microfilariae in a mouse model of Brugia infection. Parasite Immunology 24, 29–37.CrossRefGoogle Scholar
Devaney, E., O'Neill, K., Harnett, W., Whitesell, L. and Kinnaird, J. H. (2005). Hsp90 is essential in the filarial nematode Brugia pahangi . International Journal for Parasitology 35, 627–636.CrossRefGoogle ScholarPubMed
Dieterich, C., Clifton, S. W., Schuster, L. N., Chinwalla, A., Delehaunty, K., Dinkelacker, I., Fulton, L., Fulton, R., Godfrey, J., Minx, P., Mitreva, M., Roeseler, W., Tian, H., Witte, H., Yang, S. P., Wilson, R. K. and Sommer, R. J. (2008). The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nature Genetics 40, 1193–1198.CrossRefGoogle ScholarPubMed
Dupuy, D., Bertin, N., Hidalgo, C. A., Venkatesan, K., Tu, D., Lee, D., Rosenberg, J., Svrzikapa, N., Blanc, A., Carnec, A., Carvunis, A. R., Pulak, R., Shingles, J., Reece-Hoyes, J., Hunt-Newbury, R., Viveiros, R., Mohler, W. A., Tasan, M., Roth, F. P., Le Peuch, C., Hope, I. A., Johnsen, R., Moerman, D. G., Barabasi, A. L., Baillie, D. and Vidal, M. (2007). Genome-scale analysis of in vivo spatiotemporal promoter activity in Caenorhabditis elegans . Nature Biotechnology 25, 663–668. doi: 10.1038/nbt1305.CrossRefGoogle ScholarPubMed
Eccles, S. A., Massey, A., Raynaud, F. I., Sharp, S. Y., Box, G., Valenti, M., Patterson, L., De Haven Brandon, A., Gowan, S., Boxall, F., Aherne, W., Rowlands, M., Hayes, A., Martins, V., Urban, F., Boxall, K., Prodromou, C., Pearl, L., James, K., Matthews, T. P., Cheung, K. M., Kalusa, A., Jones, K., McDonald, E., Barril, X., Brough, P. A., Cansfield, J. E., Dymock, B., Drysdale, M. J., Finch, H., Howes, R., Hubbard, R. E., Surgenor, A., Webb, P., Wood, M., Wright, L. and Workman, P. (2008). NVP-AUY922: a novel heat shock protein 90 inhibitor active against xenograft tumor growth, angiogenesis, and metastasis. Cancer Research 68, 2850–2860. doi: 10.1158/0008-5472.can-07-5256.CrossRefGoogle ScholarPubMed
Eustace, B. K. and Jay, D. G. (2004). Extracellular roles for the molecular chaperone, hsp90. Cell Cycle 3, 1098–1100.CrossRefGoogle ScholarPubMed
Eustace, B. K., Sakurai, T., Stewart, J. K., Yimlamai, D., Unger, C., Zehetmeier, C., Lain, B., Torella, C., Henning, S. W., Beste, G., Scroggins, B. T., Neckers, L., Ilag, L. L. and Jay, D. G. (2004). Functional proteomic screens reveal an essential extracellular role for hsp90 alpha in cancer cell invasiveness. Nature Cell Biology 6, 507–514. doi: 10.1038/ncb1131.CrossRefGoogle ScholarPubMed
Felts, S. J., Karnitz, L. M. and Toft, D. O. (2007). Functioning of the Hsp90 machine in chaperoning checkpoint kinase I (Chk1) and the progesterone receptor (PR). Cell Stress and Chaperones 12, 353–363.CrossRefGoogle ScholarPubMed
Gaiser, A. M., Brandt, F. and Richter, K. (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, 621–634. doi: 10.1016/j.jmb.2009.06.051.CrossRefGoogle ScholarPubMed
Garon, E. B., Finn, R. S., Hamidi, H., Dering, J., Pitts, S., Kamranpour, N., Desai, A. J., Hosmer, W., Ide, S., Avsar, E., Jensen, M. R., Quadt, C., Liu, M., Dubinett, S. M. and Slamon, D. J. (2013). The HSP90 inhibitor NVP-AUY922 potently inhibits non-small cell lung cancer growth. Molecular Cancer Therapy 12, 890–900. doi: 10.1158/1535-7163.mct-12-0998.CrossRefGoogle ScholarPubMed
Gangaraju, V. K., Yin, H., Weiner, M. M., Wang, J., Huang, X. A. and Lin, H. (2011). Drosophila Piwi functions in Hsp90-mediated suppression of phenotypic variation. Nature Genetics 43, 153–158. doi: 10.1038/ng.743.CrossRefGoogle ScholarPubMed
Geary, T. G., Woo, K., McCarthy, J. S., Mackenzie, C. D., Horton, J., Prichard, R. K., De Silva, N. R., Olliaro, P. L., Lazdins-Helds, J. K., Engels, D. A. and Bundy, D. A. (2010). Unresolved issues in anthelmintic pharmacology for helminthiases of humans. International Journal for Parasitology 40, 1–13. doi: 10.1016/j.ijpara.2009.11.001.CrossRefGoogle ScholarPubMed
Ghedin, E., Wang, S., Spiro, D., Caler, E., Zhao, Q., Crabtree, J., Allen, J. E., Delcher, A. L., Guiliano, D. B., Miranda-Saavedra, D., Angiuoli, S. V. and Creasy, T. (2007). Draft genome of the filarial nematode parasite Brugia malayi . Science 317, 1756–1760.CrossRefGoogle ScholarPubMed
Gillan, V., Maitland, K., McCormack, G., Nik Him, N. A. and Devaney, E. (2009). Functional genomics of hsp-90 in parasitic and free-living nematodes. International Journal for Parasitology 39, 1071–1081. doi: S0020-7519(09)00167-2 [pii]10.1016/j.ijpara.2009.02.024.CrossRefGoogle ScholarPubMed
Gillan, V., O'Neill, K., Maitland, K., Sverdrup, F. M. and Devaney, E. (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.CrossRefGoogle ScholarPubMed
Gilleard, J. S. (2006). Understanding anthelmintic resistance: the need for genomics and genetics. International Journal for Parasitology 36, 1227–1239. doi: 10.1016/j.ijpara.2006.06.010.CrossRefGoogle ScholarPubMed
Godel, C., Kumar, S., Koutsovoulos, G., Ludin, P., Nilsson, D., Comandatore, F., Wrobel, N., Thompson, M., Schmid, C. D., Goto, S., Bringaud, F., Wolstenholme, A., Bandi, C., Epe, C., Kaminsky, R., Blaxter, M. and Maser, P. (2012). The genome of the heartworm, Dirofilaria immitis, reveals drug and vaccine targets. Journal of the Federation of American Societies for Experimental Biology 26, 4650–4661. doi: 10.1096/fj.12-205096.CrossRefGoogle ScholarPubMed
Golden, J. W. and Riddle, D. L. (1982). A pheromone influences larval development in the nematode Caenorhabditis elegans . Science 218, 578–580.CrossRefGoogle ScholarPubMed
Harst, A., Lin, H. and Obermann, W. M. (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, 789–796. doi: 10.1042/BJ20041283.CrossRefGoogle Scholar
Hashmi, S., Wang, Y., Parhar, R. S., Collison, K. S., Conca, W., Al-Mohanna, F. and Gaugler, R. (2013). A C. elegans model to study human metabolic regulation. Nutrition and Metabolism 10, 31. doi: 10.1186/1743-7075-10-31.CrossRefGoogle Scholar
Haslbeck, V., Eckl, J. M., Kaiser, C. J., Papsdorf, K., Hessling, M. and Richter, K. (2013). Chaperone-interacting TPR proteins in Caenorhabditis elegans . Journal of Molecular Biology 425, 2922–2939. doi: 10.1016/j.jmb.2013.05.019.CrossRefGoogle ScholarPubMed
Him, N. A., Gillan, V., Emes, R. D., Maitland, K. and Devaney, E. (2009). Hsp-90 and the biology of nematodes. BMC Evolutionary Biology 9, 254. doi: 10.1186/1471-2148-9-254.CrossRefGoogle ScholarPubMed
Hoerauf, A. (2008). Filariasis: new drugs and new opportunities for lymphatic filariasis and onchocerciasis. Current Opinion in Infectious Disease 21, 673–681. doi: 10.1097/QCO.0b013e328315cde7.CrossRefGoogle ScholarPubMed
Inoue, T., Takamura, K., Yamae, H., Ise, N., Kawakami, M., Tabuse, Y., Miwa, J. and Yamaguchi, Y. (2003). Caenorhabditis elegans DAF-21 (Hsp90) is characteristically and predominantly expressed in germline cells: spatial and temporal analysis. Development Growth and Differentiation 45, 369–376.CrossRefGoogle ScholarPubMed
Inoue, T., Hirata, K., Kuwana, Y., Fujita, M., Miwa, J., Roy, R. and Yamaguchi, Y. (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, 25–32. doi: 10.1111/j.1440-169X.2006.00841.x.CrossRefGoogle ScholarPubMed
Iwasaki, S., Kobayashi, M., Yoda, M., Sakaguchi, Y., Katsuma, S., Suzuki, T. and Tomari, Y. (2010). Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes. Molecular Cell 39, 292–299. doi: 10.1016/j.molcel.2010.05.015.CrossRefGoogle ScholarPubMed
Izumi, N., Kawaoka, S., Yasuhara, S., Suzuki, Y., Sugano, S., Katsuma, S. and Tomari, Y. (2013). Hsp90 facilitates accurate loading of precursor piRNAs into Piwi proteins. RNA 19, 896–901. doi: 10.1261/rna.037200.112.CrossRefGoogle ScholarPubMed
Jecock, R. M. and Devaney, E. (1992). Expression of small heat shock proteins by the third-stage larva of Brugia pahangi . Molecular and Biochemical Parasitology 56, 219–226.CrossRefGoogle ScholarPubMed
Jeong, P. Y., Na, K., Jeong, M. J., Chitwood, D., Shim, Y. H. and Paik, Y. K. (2009). Proteomic analysis of Caenorhabditis elegans . Methods in Molecular Biology 519, 145–169. doi: 10.1007/978-1-59745-281-6_10.CrossRefGoogle ScholarPubMed
Jex, A. R., Liu, S., Li, B., Young, N. D., Hall, R. S., Li, Y., Yang, L., Zeng, N., Xu, X., Xiong, Z., Chen, F., Wu, X., Zhang, G., Fang, X., Kang, Y., Anderson, G. A., Harris, T. W., Campbell, B. E., Vlaminck, J., Wang, T., Cantacessi, C., Schwarz, E. M., Ranganathan, S., Geldhof, P., Nejsum, P., Sternberg, P. W., Yang, H., Wang, J., Wang, J. and Gasser, R. B. (2011). Ascaris suum draft genome. Nature 479, 529–533. doi: 10.1038/nature10553.CrossRefGoogle ScholarPubMed
Johnson, J. L. and Brown, C. (2009). Plasticity of the Hsp90 chaperone machine in divergent eukaryotic organisms. Cell Stress and Chaperones 14, 83–94. doi: 10.1007/s12192-008-0058-9.CrossRefGoogle ScholarPubMed
Jones, D., Dixon, D. K., Graham, R. W. and Candido, E. P. (1989). Differential regulation of closely related members of the hsp16 gene family in Caenorhabditis elegans . DNA 8, 481–490.CrossRefGoogle ScholarPubMed
Jones, S. J., Riddle, D. L., Pouzyrev, A. T., Velculescu, V. E., Hillier, L., Eddy, S. R., Stricklin, S. L., Baillie, D. L., Waterston, R. and Marra, M. A. (2001). Changes in gene expression associated with developmental arrest and longevity in Caenorhabditis elegans . Genome Research 11, 1346–1352. doi: 10.1101/gr.184401.CrossRefGoogle ScholarPubMed
Kamal, A., Thao, L., Sensintaffar, J., Zhang, L., Boehm, M. F., Fritz, L. C. and Burrows, F. J. (2003). A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 425, 407–410. doi: 10.1038/nature01913.CrossRefGoogle ScholarPubMed
Kirienko, N. V., Mani, K. and Fay, D. S. (2010). Cancer models in Caenorhabditis elegans . Development Dynamics 239, 1413–1448. doi: 10.1002/dvdy.22247.CrossRefGoogle ScholarPubMed
Kumar, R., Musiyenko, A. and Barik, S. (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.CrossRefGoogle ScholarPubMed
Kumari, S., Lillibridge, C. D., Bakeer, M., Lowrie, R. C. Jr., Jayaraman, K. and Philipp, M. T. (1994). Brugia malayi: the diagnostic potential of recombinant excretory/secretory antigens. Experimental Parasitology 79, 489–505. doi: 10.1006/expr.1994.1110.CrossRefGoogle ScholarPubMed
Kwa, M. S., Veenstra, J. G., Van Dijk, M. and Roos, M. H. (1995). Beta-tubulin genes from the parasitic nematode Haemonchus contortus modulate drug resistance in Caenorhabditis elegans . Journal of Molecular Biology 246, 500–510. doi: 10.1006/jmbi.1994.0102.CrossRefGoogle ScholarPubMed
Laing, R., Kikuchi, T., Martinelli, A., Tsai, I. J., Beech, R. N., Redman, E., Holroyd, N., Bartley, D. J., Beasley, H., Britton, C., Curran, D., Devaney, E., Gilabert, A., Hunt, M., Jackson, F., Johnston, S. L., Kryukov, I., Li, K., Morrison, A. A., Reid, A. J., Sargison, N., Saunders, G. I., Wasmuth, J. D., Wolstenholme, A., Berriman, M., Gilleard, J. S. and Cotton, J. A. (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.CrossRefGoogle ScholarPubMed
Landsverk, M. L., Li, S., Hutagalung, A. H., Najafov, A., Hoppe, T., Barral, J. M. and Epstein, H. F. (2007). The UNC-45 chaperone mediates sarcomere assembly through myosin degradation in Caenorhabditis elegans . Journal of Cell Biology 177, 205–210. doi: 10.1083/jcb.200607084.CrossRefGoogle ScholarPubMed
Li, J. and Le, W. (2013). Modeling neurodegenerative diseases in Caenorhabditis elegans . Experimental Neurology 250C, 94–103. doi: 10.1016/j.expneurol.2013.09.024.CrossRefGoogle Scholar
Martinez, N. J. and Gregory, R. I. (2013). Argonaute2 expression is post-transcriptionally coupled to microRNA abundance. RNA 19, 605–612. doi: 10.1261/rna.036434.112.CrossRefGoogle ScholarPubMed
Massey, H. C. Jr., Bhopale, M. K., Li, X., Castelletto, M. and Lok, J. B. (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, 347–352. doi: 10.1016/j.ijpara.2005.11.007.CrossRefGoogle ScholarPubMed
Millson, S. H., Chua, C. S., Roe, S. M., Polier, S., Solovieva, S., Pearl, L. H., Sim, T. S., Prodromou, C. and Piper, P. W. (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, 3828–3837. doi: 10.1096/fj.11-188821.CrossRefGoogle Scholar
Mitreva, M., Jasmer, D. P., Zarlenga, D. S., Wang, Z., Abubucker, S., Martin, J., Taylor, C. M., Yin, Y., Fulton, L., Minx, P., Yang, S. P., Warren, W. C., Fulton, R. S., Bhonagiri, V., Zhang, X., Hallsworth-Pepin, K., Clifton, S. W., McCarter, J. P., Appleton, J., Mardis, E. R. and Wilson, R. K. (2011). The draft genome of the parasitic nematode Trichinella spiralis . Nature Genetics 43, 228–235. doi: 10.1038/ng.769.CrossRefGoogle ScholarPubMed
Miyoshi, T., Takeuchi, A., Siomi, H. and Siomi, M. C. (2010). A direct role for Hsp90 in pre-RISC formation in Drosophila . Nature Structural and Molecular Biology 17, 1024–1026. doi: 10.1038/nsmb.1875.CrossRefGoogle ScholarPubMed
Molyneux, D. H., Bradley, M., Hoerauf, A., Kyelem, D. and Taylor, M. J. (2003). Mass drug treatment for lymphatic filariasis and onchocerciasis. Trends in Parasitology 19, 516–522.CrossRefGoogle ScholarPubMed
Moulick, K., Ahn, J. H., Zong, H., Rodina, A., Cerchietti, L., Gomes Dagama, E. M., Caldas-Lopes, E., Beebe, K., Perna, F., Hatzi, K., Vu, L. P., Zhao, X., Zatorska, D., Taldone, T., Smith-Jones, P., Alpaugh, M., Gross, S. S., Pillarsetty, N., Ku, T., Lewis, J. S., Larson, S. M., Levine, R., Erdjument-Bromage, H., Guzman, M. L., Nimer, S. D., Melnick, A., Neckers, L. and Chiosis, G. (2011). Affinity-based proteomics reveal cancer-specific networks coordinated by Hsp90. Nature Chemical Biology 7, 818–826. doi: 10.1038/nchembio.670.CrossRefGoogle ScholarPubMed
Neckers, L., Mimnaugh, E. and Schulte, T. W. (1999). Hsp90 as an anti-cancer target. Drug Resistance Update 2, 165–172. doi: 10.1054/drup.1999.0082.CrossRefGoogle ScholarPubMed
Ni, W., Hutagalung, A. H., Li, S. and Epstein, H. F. (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, 3164–3173. doi: 10.1242/jcs.087320.CrossRefGoogle Scholar
Nicol, J. M., Turner, S. J., Coyne, D. L., Den Nijs, L., Hockland, S. and Maafi, Z. T. (2011). Current nematode threats to world agriculture. In Genomics and Molecular Genetics of Plant-Nematode Interactions (ed. Jones, J., Gheysen, G. and Fenoll, C.), pp. 21–43. Springer, Dordrecht, the Netherlands.CrossRefGoogle Scholar
Opperman, C. H., Bird, D. M., Williamson, V. M., Rokhsar, D. S., Burke, M., Cohn, J., Cromer, J., Diener, S., Gajan, J., Graham, S., Houfek, T. D., Liu, Q., Mitros, T., Schaff, J., Schaffer, R., Scholl, E., Sosinski, B. R., Thomas, V. P. and Windham, E. (2008). Sequence and genetic map of Meloidogyne hapla: a compact nematode genome for plant parasitism. Proceedings of the National Academy of Sciences USA 105, 14802–14807.CrossRefGoogle ScholarPubMed
Pallavi, R., Roy, N., Nageshan, R. K., Talukdar, P., Pavithra, S. R., Reddy, R., Venketesh, S., Kumar, R., Gupta, A. K., Singh, R. K., Yadav, S. C. and Tatu, U. (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, 37964–37975. doi: 10.1074/jbc.M110.155317.CrossRefGoogle ScholarPubMed
Palmer, G., Louvion, J. F., Tibbetts, R. S., Engman, D. M. and Picard, D. (1995). Trypanosoma cruzi heat-shock protein 90 can functionally complement yeast. Molecular and Biochemical Parasitology 70, 199–202.CrossRefGoogle ScholarPubMed
Pearl, L. H. and Prodromou, C. (2006). Structure and mechanism of the Hsp90 molecular chaperone machinery. Annual Review of Biochemistry 75, 271–294. doi: 10.1146/annurev.biochem.75.103004.142738.CrossRefGoogle ScholarPubMed
Petersen, A. L., Guedes, C. E., Versoza, C. L., Lima, J. G., De Freitas, L. A., Borges, V. M. and Veras, P. S. (2012). 17-AAG kills intracellular Leishmania amazonensis while reducing inflammatory responses in infected macrophages. PLoS One 7, e49496. doi: 10.1371/journal.pone.0049496.CrossRefGoogle ScholarPubMed
Piano, F., Schetter, A. J., Mangone, M., Stein, L. and Kemphues, K. J. (2000). RNAi analysis of genes expressed in the ovary of Caenorhabditis elegans . Current Biology 10, 1619–1622.CrossRefGoogle ScholarPubMed
Piper, P. W., Panaretou, B., Millson, S. H., Trumana, A., Mollapour, M., Pearl, L. H. and Prodromou, C. (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, 165–170.CrossRefGoogle Scholar
Pratt, W. B., Galigniana, M. D., Harrell, J. M. and Defranco, D. B. (2004). Role of Hsp90 and the Hsp90-binding immunophilins in signalling protein movement. Cell Signalling 16, 857–872. doi: 10.1016/j.cellsig.2004.02.004.CrossRefGoogle ScholarPubMed
Prichard, R. K., Basanez, M. G., Boatin, B. A., McCarthy, J. S., Garcia, H. H., Yang, G. J., Sripa, B. and Lustigman, S. (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.CrossRefGoogle ScholarPubMed
Prodromou, C., Nuttall, J. M., Millson, S. H., Roe, S. M., Sim, T. S., Tan, D., Workman, P., Pearl, L. H. and Piper, P. W. (2009). Structural basis of the radicicol resistance displayed by a fungal Hsp90. ACS Chemical Biology 4, 289–297. doi: 10.1021/cb9000316.CrossRefGoogle ScholarPubMed
Rae, R., Riebesell, M., Dinkelacker, I., Wang, Q., Herrmann, M., Weller, A. M., Dieterich, C. and Sommer, R. J. (2008). Isolation of naturally associated bacteria of necromenic Pristionchus nematodes and fitness consequences. Journal of Experimental Biology 211, 1927–1936. doi: 10.1242/jeb.014944.CrossRefGoogle ScholarPubMed
Riggs, D. L., Cox, M. B., Cheung-Flynn, J., Prapapanich, V., Carrigan, P. E. and Smith, D. F. (2004). Functional specificity of co-chaperone interactions with Hsp90 client proteins. Critical Reviews in Biochemistry and Molecular Biology 39, 279–295. doi: 10.1080/10409230490892513.CrossRefGoogle ScholarPubMed
Ruden, D. M. and Lu, X. Y. (2008). Hsp90 affecting chromatin remodeling might explain transgenerational epigenetic inheritance in Drosophila . Current Genomics 9, 500–508. doi: 10.2174/138920208786241207.CrossRefGoogle ScholarPubMed
Russell, L. C., Whitt, S. R., Chen, M. S. and Chinkers, M. (1999). Identification of conserved residues required for the binding of a tetratricopeptide repeat domain to heat shock protein 90. Journal of Biological Chemistry 274, 20060–20063.CrossRefGoogle ScholarPubMed
Rutherford, S. L. and Lindquist, S. (1998). Hsp90 as a capacitor for morphological evolution. Nature 396, 336–342. doi: 10.1038/24550.CrossRefGoogle ScholarPubMed
Sawarkar, R., Sievers, C. and Paro, R. (2012). Hsp90 globally targets paused RNA polymerase to regulate gene expression in response to environmental stimuli. Cell 149, 807–818.CrossRefGoogle ScholarPubMed
Scheufler, C., Brinker, A., Bourenkov, G., Pegoraro, S., Moroder, L., Bartunik, H., Hartl, F. U. and Moarefi, I. (2000). Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101, 199–210. doi: 10.1016/S0092-8674(00)80830-2.CrossRefGoogle ScholarPubMed
Schwarz, E. M., Korhonen, P. K., Campbell, B. E., Young, N. D., Jex, A. R., Jabbar, A., Hall, R. S., Mondal, A., Howe, A. C., Pell, J., Hofmann, A., Boag, P. R., Zhu, X. Q., Gregory, T. R., Loukas, A., Williams, B. A., Antoshechkin, I., Brown, C. T., Sternberg, P. W. and Gasser, R. B. (2013). The genome and developmental transcriptome of the strongylid nematode Haemonchus contortus . Genome Biology 14, R89. doi: 10.1186/gb-2013-14-8-r89.CrossRefGoogle ScholarPubMed
Shahinas, D., Liang, M., Datti, A. and Pillai, D. R. (2010). A repurposing strategy identifies novel synergistic inhibitors of Plasmodium falciparum heat shock protein 90. Journal of Medicinal Chemistry 53, 3552–3557. doi: 10.1021/jm901796s.CrossRefGoogle ScholarPubMed
Shahinas, D., Folefoc, A., Taldone, T., Chiosis, G., Crandall, I. and Pillai, D. R. (2013). A purine analog synergizes with chloroquine (CQ) by targeting Plasmodium falciparum Hsp90 (PfHsp90). PLoS One 8, e75446. doi: 10.1371/journal.pone.0075446.CrossRefGoogle ScholarPubMed
Smith, D. F. and Toft, D. O. (2008). Minireview: the intersection of steroid receptors with molecular chaperones: observations and questions. Molecular Endocrinology 22, 2229–2240. doi: 10.1210/me.2008-0089.CrossRefGoogle ScholarPubMed
Specchia, V., Piacentini, L., Tritto, P., Fanti, L., D'Alessandro, R., Palumbo, G., Pimpinelli, S. and Bozzetti, M. P. (2010). Hsp90 prevents phenotypic variation by suppressing the mutagenic activity of transposons. Nature 463, 662–665. doi: 10.1038/nature08739.CrossRefGoogle ScholarPubMed
Stein, L. D., Bao, Z., Blasiar, D., Blumenthal, T., Brent, M. R., Chen, N., Chinwalla, A., Clarke, L., Clee, C., Coghlan, A., Coulson, A., D'Eustachio, P., Fitch, D. H., Fulton, L. A., Fulton, R. E., Griffiths-Jones, S., Harris, T. W., Hillier, L. W., Kamath, R., Kuwabara, P. E., Mardis, E. R., Marra, M. A., Miner, T. L., Minx, P., Mullikin, J. C., Plumb, R. W., Rogers, J., Schein, J. E., Sohrmann, M., Spieth, J., Stajich, J. E., Wei, C., Willey, D., Wilson, R. K., Durbin, R. and Waterston, R. H. (2003). The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biology 1, E45. doi: 10.1371/journal.pbio.0000045.CrossRefGoogle ScholarPubMed
Taldone, T., Gillan, V., Sun, W., Rodina, A., Patel, P., Maitland, K., O'Neill, K., Chiosis, G. and Devaney, E. (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.CrossRefGoogle ScholarPubMed
Taldone, T., Zatorska, D., Patel, P. D., Zong, H., Rodina, A., Ahn, J. H., Moulick, K., Guzman, M. L. and Chiosis, G. (2011). Design, synthesis, and evaluation of small molecule Hsp90 probes. Bioorganic and Medicinal Chemistry 19, 2603–2614. doi: 10.1016/j.bmc.2011.03.013.CrossRefGoogle ScholarPubMed
Tang, Y. T., Gao, X., Rosa, B. A., Abubucker, S., Hallsworth-Pepin, K., Martin, J., Tyagi, R., Heizer, E., Zhang, X., Bhonagiri-Palsikar, V., Minx, P., Warren, W. C., Wang, Q., Zhan, B., Hotez, P. J., Sternberg, P. W., Dougall, A., Gaze, S. T., Mulvenna, J., Sotillo, J., Ranganathan, S., Rabelo, E. M., Wilson, R. K., Felgner, P. L., Bethony, J., Hawdon, J. M., Gasser, R. B., Loukas, A. and Mitreva, M. (2014). Genome of the human hookworm Necator americanus . Nature Genetics 46, 261–269. doi: 10.1038/ng.2875.CrossRefGoogle ScholarPubMed
Tariq, M., Nussbaumer, U., Chen, Y., Beisel, C. and Paro, R. (2009). Trithorax requires Hsp90 for maintenance of active chromatin at sites of gene expression. Proceedings of the National Academy of Sciences USA 106, 1157–1162. doi: 10.1073/pnas.0809669106.CrossRefGoogle ScholarPubMed
Terhell, A. J., Haarbrink, M., Van Den Biggelaar, A., Mangali, A., Sartono, E. and Yazdanbakhsh, M. (2003). Long-term follow-up of treatment with diethylcarbamazine on anti-filarial IgG4: dosage, compliance, and differential patterns in adults and children. American Journal of Tropical Medicine and Hygiene 68, 33–39.CrossRefGoogle ScholarPubMed
Thompson, F. J., Cockroft, A. C., Wheatley, I., Britton, C. and Devaney, E. (2001). Heat shock and developmental expression of hsp83 in the filarial nematode Brugia pahangi . European Journal of Biochemistry 268, 5808–5815.CrossRefGoogle ScholarPubMed
Vercruysse, J., Levecke, B. and Prichard, R. (2012). Human soil-transmitted helminths: implications of mass drug administration. Current Opinion in Infectious Disease 25, 703–708. doi: 10.1097/QCO.0b013e328358993a.CrossRefGoogle ScholarPubMed
Walker, G. A., Thompson, F. J., Brawley, A., Scanlon, T. and Devaney, E. (2003). Heat shock factor functions at the convergence of the stress response and developmental pathways in Caenorhabditis elegans . Journal of the Federation of American Societies for Experimental Biology 17, 1960–1962. doi: 10.1096/fj.03-0164fje.CrossRefGoogle ScholarPubMed
Wenkert, D., Ramirez, B., Shen, Y. and Kron, M. A. (2010). In vitro activity of geldanamycin derivatives against Schistosoma japonicum and Brugia malayi . Journal of Parasitology Research 2010, 716498. doi: 10.1155/2010/716498.CrossRefGoogle ScholarPubMed
Wider, D., Peli-Gulli, M. P., Briand, P. A., Tatu, U. and Picard, D. (2009). The complementation of yeast with human or Plasmodium falciparum Hsp90 confers differential inhibitor sensitivities. Molecular and Biochemical Parasitology 164, 147–152.CrossRefGoogle ScholarPubMed
Wu, C. (1995). Heat shock transcription factors: structure and regulation. Annual Review of Cell Developmental Biology 11, 441–469. doi: 10.1146/annurev.cb.11.110195.002301.CrossRefGoogle ScholarPubMed
Xiao, H. and Lis, J. T. (1989). Heat shock and developmental regulation of the Drosophila melanogaster hsp83 gene. Molecular Cell Biology 9, 1746–1753.Google ScholarPubMed
Yang, Y., Qin, W., Zarlenga, D., Cao, L. and Tian, G. (2013). TsDAF-21/Hsp90 is expressed in all examined stages of Trichinella spiralis . Veterinary Parasitology 194, 171–174. doi: 10.1016/j.vetpar.2013.01.048.CrossRefGoogle ScholarPubMed