Heat shock protein 90 from neglected protozoan parasites

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1823, Issue 3, 2012, Pages 707-711

  Roy, Nainita ^a   Nageshan, Rishi Kumar ^a   Ranade, Shatakshi ^a   Tatu, Utpal ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

Chaperone; Giardia; Hsp90; Plasmodium; Protozoan; Trans splicing

Indexed keywords

HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR;

GIARDIA LAMBLIA; HOST CELL; HUMAN; LEISHMANIASIS; MALARIA; MICROENVIRONMENT; NONHUMAN; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTOZOON; REVIEW; TRYPANOSOMIASIS;

ANIMALS; CELLULAR MICROENVIRONMENT; HSP90 HEAT-SHOCK PROTEINS; HUMANS; PARASITES; PROTOZOAN INFECTIONS;

GIARDIA; GIARDIA INTESTINALIS; MAMMALIA; PROTOZOA;

EID: 84857058509     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2011.12.003     Document Type: Review

References (41)

1. Frydman J. Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu. Rev. Biochem. 2001, 70:603-647.
2. Denis M., Poellinger L., Wikstöm A.C., Gustafsson J.A. Requirement of hormone for thermal conversion of the glucocorticoid receptor to a DNA-binding state. Nature 1988, 333:686-688.
3. Catelli M.G., Devin-Leclerc J., Bouhouche I., Cadepond F. Functional interaction of HSP90 with steroid receptors. J. Soc. Biol. 1999, 193:361-367.
4. Ananthan J., Goldberg A.L., Voellmy R. Abnormal proteins serve as eukaryotic stress signals and trigger the activation of heat shock genes. Science 1986, 1232:522-524.
5. Ali A., Bharadwaj S., O'Carroll R., Ovsenek N. HSP90 interacts with and regulates the activity of heat shock factor 1 in Xenopus oocytes. Mol. Cell. Biol. 1998, 18:4949-4960.
6. Zou J., Guo Y., Guettouche T., Smith D.F., Voellmy R. Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1. Cell 1998, 94:471-480.
7. Hainzl O., Lapina M.C., Buchner J., Richter K. The charged linker region is an important regulator of Hsp90 function. J. Biol. Chem. 2009, 284:22559-22567.
8. Tsutsumi S., Mollapour M., Graf C., Lee C.T., Scroggins B.T., Xu W., Haslerova L., Hessling M., Konstantinova A.A., Trepel J.B., Panaretou B., Buchner J., Mayer M.P., Prodromou C., Neckers L. Hsp90 charged-linker truncation reverses the functional consequences of weakened hydrophobic contacts in the N domain. Nat. Struct. Mol. Biol. 2009, 16:1141-1147.
9. Sreeramulu S., Jonker H.R., Langer T., Richter C., Lancaster C.R., Schwalbe H. The human Cdc37.Hsp90 complex studied by heteronuclear NMR spectroscopy. J. Biol. Chem. 2009, 284:3885-3896.
10. Mollapour M., Tsutsumi S., Neckers L. Hsp90 phosphorylation, Wee1 and the cell cycle. Cell Cycle 2010, 9:2310-2316.
11. Hameed S., Dhamgaye S., Singh A., Goswami S.K., Prasad R. Calcineurin signaling and membrane lipid homeostasis regulates iron mediated multidrug resistance mechanisms in Candida albicans. PLoS One 2011, 6:e18684.
12. Cowen L.E., Lindquist S. Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 2005, 309:2185-2189.
13. Sangster T.A., Salathia N., Lee H.N., Watanabe E., Schellenberg K., Morneau K., Wang H., Undurraga S., Queitsch C., Lindquist S. HSP90-buffered genetic variation is common in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:2969-2974.
14. Jarosz D.F., Lindquist S. Hsp90 and environmental stress transform the adaptive value of natural genetic variation. Science 2010, 330:1820-1824.
15. Taldone T., Gozman A., Maharaj R., Chiosis G. Targeting Hsp90: small-molecule inhibitors and their clinical development. Curr. Opin. Pharmacol. 2008, 8:370-374.
16. Taldone T., Zatorska D., Patel P.D., Zong H., Rodina A., Ahn J.H., Moulick K., Guzman M.L., Chiosis G. Design, synthesis, and evaluation of small molecule Hsp90 probes. Bioorg. Med. Chem. 2011, 19:2603-2614.
17. Banumathy G., Singh V., Pavithra S.R., Tatu U. Heat shock protein 90 function is essential for Plasmodium falciparum growth in human erythrocytes. J. Biol. Chem. 2003, 278:18336-18345.
18. Kwiatkowski D. Febrile temperatures can synchronize the growth of Plasmodium falciparum in vitro. J. Exp. Med. 1989, 169:357-361.
19. Pavithra S.R., Banumathy G., Joy O., Singh V., Tatu U. Recurrent fever promotes Plasmodium falciparum development in human erythrocytes. J. Biol. Chem. 2004, 279:46692-46699.
20. Zilberstein D., Shapira M. The role of pH and temperature in the development of Leishmania parasites. Annu. Rev. Microbiol. 1994, 48:449-470.
21. Wiesgigl M., Clos J. Heat shock protein 90 homeostasis controls stage differentiation in Leishmania donovani. Mol. Biol. Cell 2001, 12:3307-3316.
22. Hem S., Gherardini P.F., Osorio Fortéa J., Hourdel V., Morales M.A., Watanabe R., Pescher P., Kuzyk M.A., Smith D., Borchers C.H., Zilberstein D., Helmer-Citterich M., Namane A., Späth G.F. Identification of Leishmania-specific protein phosphorylation sites by LC-ESI-MS/MS and comparative genomics analyses. Proteomics 2010, 21:3868-3883.
23. Morales M.A., Watanabe R., Dacher M., Chafey P., Osorio Fortéa J., Scott D.A., Beverley S.M., Ommen G., Clos J., Hem S., Lenormand P., Rousselle J.C., Namane A., Späth G.F. Phosphoproteome dynamics reveal heat-shock protein complexes specific to the Leishmania donovani infectious stage. Proc. Natl. Acad. Sci. U. S. A. 2010, 18:8381-8386.
24. Péroval M., Péry P., Labbé M. The heat shock protein 90 of Eimeria tenella is essential for invasion of host cell and schizont growth. Int. J. Parasitol. 2006, 36:1205-1215.
25. Gerhards J., Ebel T., Dobbelaere D.D., Morzaria S.P., Musoke A.J., Williams R.O., Lipp J. Sequence and expression of a 90-kilodalton heat-shock protein family member of Theileria parva. Mol. Biochem. Parasitol. 1994, 68:235-246.
26. Echeverria P.C., Matrajt M., Harb O.S., Zappia M.P., Costas M.A., Roos D.S., Dubremetz J.F., Angel S.O. Toxoplasma gondii Hsp90 is a potential drug target whose expression and subcellular localization are developmentally regulated. J. Mol. Biol. 2005, 350:723-734.
27. Graefe S.E., Wiesgigl M., Gaworski I., Macdonald A., Clos J. Inhibition of HSP90 in Trypanosoma cruzi induces a stress response but no stage differentiation. Eukaryot. Cell 2002, 1:936-943.
28. Jones C., Anderson S., Singha U.K., Chaudhuri M. Protein phosphatase 5 is required for Hsp90 function during proteotoxic stresses in Trypanosoma brucei. Parasitol. Res. 2008, 102:835-844.
29. Sawarkar R., Roy N., Rao S., Raman S., Venketesh S., Suguna K., Tatu U. Heat shock protein 90 regulates development in Dictyostelium discoideum. J. Mol. Biol. 2008, 383:24-35.
30. Singh S.D., Robbins N., Zaas A.K., Schell W.A., Perfect J.R., Cowen L.E. Hsp90 governs echinocandin resistance in the pathogenic yeast Candida albicans via calcineurin. PLoS Pathog. 2009, 5:e1000532.
31. Shapiro R.S., Cowen L. Coupling temperature sensing and development: Hsp90 regulates morphogenetic signalling in Candida albicans. Virulence 2010, 1:45-48.
32. Nageshan R.K., Roy N., Hehl A.B., Tatu U. Post-transcriptional repair of a split heat shock protein 90 gene by mRNA trans-splicing. J. Biol. Chem. 2011, 286:7116-7122.
33. Kamikawa R., Inagaki Y., Tokoro M., Roger A.J., Hashimoto T. Split introns in the genome of Giardia intestinalis are excised by spliceosome-mediated trans-splicing. Curr. Biol. 2011, 21:311-315.
34. Kim Y.S., Alarcon S.V., Lee S., Lee M.J., Giaccone G., Neckers L., Trepel J.B. Update on Hsp90 inhibitors in clinical trial. Curr. Top. Med. Chem. 2009, 9:1479-1492.
35. 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., Tatu U. 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. J. Biol. Chem. 2010, 285:37964-37975.
36. Shahinas D., Liang M., Datti A., Pillai D.R. A repurposing strategy identifies novel synergistic inhibitors of Plasmodium falciparum heat shock protein 90. J. Med. Chem. 2010, 53:3552-3557.
37. Petersen I., Eastman R., Lanzer M. Drug-resistant malaria: molecular mechanisms and implications for public health. FEBS Lett. 2011, 585:1551-1562.
38. Delespaux V., de Koning H.P. Drugs and drug resistance in African trypanosomiasis. Drug Resist. Updat. 2007, 10:30-50.
39. Cowen L.E., Steinbach W.J. Stress, drugs, and evolution: the role of cellular signaling in fungal drug resistance. Eukaryot. Cell 2008, 7:747-764.
40. Cowen L.E., Lindquist S. Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 2005, 309:2185-2189.
41. Johnson J.L., Brown C. Plasticity of the Hsp90 chaperone machine in divergent eukaryotic organisms. Cell Stress Chaperones 2009, 14:83-94.