No stress - Hsp90 and signal transduction in Leishmania

Parasitology

Volumn 141, Issue 9, 2014, Pages 1156-1166

  Hombach, A ^a   Clos, J ^a  

^a BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

Author keywords

heat shock; Hsp90; Leishmania; radicicol; signal transduction

Indexed keywords

HEAT SHOCK PROTEIN 90; PROTEIN KINASE; ANTIGEN; PROTOZOAL PROTEIN;

AMASTIGOTE; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; INSECT; LEISHMANIA; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROMASTIGOTE; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STRESS; ANTIBIOTIC RESISTANCE; DRUG TARGETING; KINETOPLASTID LIFE CYCLE STAGE; LEISHMANIA DONOVANI; LEISHMANIA MEXICANA; PROTEIN DEPLETION; PROTEIN FUNCTION; REVERSE GENETICS; REVIEW; SKIN LEISHMANIASIS; VISCERAL LEISHMANIASIS; DRUG RESISTANCE; GENETICS; HUMAN; LEISHMANIASIS; METABOLISM; PARASITOLOGY; PATHOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

HEXAPODA; LEISHMANIA DONOVANI; MAMMALIA; PROTOZOA;

DRUG RESISTANCE; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LEISHMANIA; LEISHMANIASIS; PROTOZOAN PROTEINS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84904251225     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182013002151     Document Type: Article

References (94)

1. Alexandratos, A., Clos, J., Samiotaki, M., Efstathiou, A., Panayotou, G., Soteriadou, K. and Smirlis, D. (2013). Restoration of heat shock protein 83 expression in histone H1 over-expressing Leishmania donovani attenuated parasites identifies HSP83 as a virulence factor. Molecular Microbiology 88, 1015-1031. doi: 10.1111/mmi.12240.
2. Alvar, J., Velez, I. D., Bern, C., Herrero, M., Desjeux, P., Cano, J., Jannin, J. and den Boer, M. (2012). Leishmaniasis worldwide and global estimates of its incidence. PloS One 7, e35671. doi: 10.1371/journal.pone.0035671.
3. Argaman, M., Aly, R. and Shapira, M. (1994). Expression of heat shock protein 83 in Leishmania is regulated post-Transcriptionally. Molecular and Biochemical Parasitology 64, 95-110. (Pubitemid 24126845)
4. Banumathy, G., Singh, V., Pavithra, S. R. and Tatu, U. (2003). Heat shock protein 90 function is essential for Plasmodium falciparum growth in human erythrocytes. Journal of Biological Chemistry 278, 18336-18345. doi: 10.1074/jbc.M211309200. (Pubitemid 36799454)
5. Barak, E., Amin-Spector, S., Gerliak, E., Goyard, S., Holland, N. and Zilberstein, D. (2005). Differentiation of Leishmania donovani in host-free system: Analysis of signal perception and response. Molecular and Biochemical Parasitology 141, 99-108. (Pubitemid 40461901)
6. Bates, P. A. (1993). Axenic amastigote culture of Leishmania amastigotes. Parasitology Today 9, 143-146.
7. Bates, P. A. (1994). Complete developmental cycle of Leishmania mexicana in axenic culture. Parasitology 108, 1-9.
8. Bates, P. A., Cobertson, C. D., Tetley, L. and Coombs, G. H. (1992). Axenic cultivation and characterization of Leishmania mexicana amastigotelike forms. Parasitology 105, 193-202.
9. Bente, M., Harder, S., Wiesgigl, M., Heukeshoven, J., Gelhaus, C., Krause, E., Clos, J. and Bruchhaus, I. (2003). Developmentally induced changes of the proteome in the protozoan parasite Leishmania donovani. Proteomics 3, 1811-1829. (Pubitemid 37129827)
10. Brandau, S., Dresel, A. and Clos, J. (1995). High constitutive levels of heat-shock proteins in human-pathogenic parasites of the genus Leishmania. Biochemical Journal 310, 225-232.
11. Brochu, C., Haimeur, A. and Ouellette, M. (2004). The heat shock protein HSP70 and heat shock cognate protein HSC70 contribute to antimony tolerance in the protozoan parasite leishmania. Cell Stress and Chaperones 9, 294-303. (Pubitemid 39457433)
12. Buchner, J. (1999). Hsp90 & Co.-A holding for folding. Trends in Biochemical Sciences 24, 136-141.
13. Catelli, M. G., Binart, N., Jung-Testas, I., Renoir, J. M., Baulieu, E. E., Feramisco, J. R. and Welch, W. J. (1985). The common 90-kd protein component of non-Transformed '8S' steroid receptors is a heat-shock protein. EMBO Journal 4, 3131-3135.
14. Charest, H. and Matlashewski, G. (1994). Developmental gene expression in Leishmania donovani: Differential cloning and analysis of an amastigote-stage-specific gene. Molecular and Cellular Biology 14, 2975-2984. (Pubitemid 24132711)
15. Charest, H., Zhang, W.-W. and Matlashewski, G. (1996). The developmental expression of Leishmania donovani A2 amastigote-specific genes is post-Transcriptionally mediated and involves elements located in the 3′-untranslated region. Journal of Biological Chemistry 271, 17081-17090. (Pubitemid 26244256)
16. Chen, B., Zhong, D. and Monteiro, A. (2006). Comparative genomics and evolution of the HSP90 family of genes across all kingdoms of organisms. BioMed Central Genomics 7, 156. doi: 10.1186/1471-2164-7-156. (Pubitemid 44151610)
17. Chrobak, M., Forster, S., Meisel, S., Pfefferkorn, R., Forster, F. and Clos, J. (2012). Leishmania donovani HslV does not interact stably with HslU proteins. International Journal for Parasitology 42, 329-339. doi: 10.1016/j.ijpara.2012.01.008.
18. Clayton, C. E. (2002). Life without transcriptional control? From fly to man and back again. EMBO Journal 21, 1881-1888.
19. Clos, J. and Krobitsch, S. (1999). Heat shock as a regular feature of the life cycle of Leishmania parasites. American Zoologist 39, 848-856.
20. Clos, J. and Choudhury, K. (2006). Functional cloning as a means to identify Leishmania genes involved in drug resistance. Mini Reviews in Medicinal Chemistry 6, 123-129.
21. Cruz, A., Coburn, C. M. and Beverley, S.M. (1991). Double targeted gene replacement for creating null mutants. Proceedings of the National Academy of Sciences USA 88, 7170-7174. (Pubitemid 21915111)
22. Dai, B., Wang, Y., Li, D., Xu, Y., Liang, R., Zhao, L., Cao, Y., Jia, J. and Jiang, Y. (2012). Hsp90 is involved in apoptosis of Candida albicans by regulating the calcineurin-caspase apoptotic pathway. PloS One 7, e45109. doi: 10.1371/journal.pone.0045109.
23. de Andrade, C. R., Kirchhoff, L. V., Donelson, J. E. and Otsu, K. (1992). Recombinant Leishmania Hsp90 and Hsp70 are recognized by sera from visceral leishmaniasis patients but not Chagas' disease patients. Journal of Clinical Microbiology 30, 330-335.
24. Echeverria, P. C., Matrajt, M., Harb, O. S., Zappia, M. P., Costas, M. A., Roos, D. S., Dubremetz, J. F. and Angel, S. O. (2005). Toxoplasma gondii Hsp90 is a potential drug target whose expression and subcellular localization are developmentally regulated. Journal of Molecular Biology 350, 723-734. doi: 10.1016/j.jmb.2005.05.031. (Pubitemid 40848670)
25. Folgueira, C. and Requena, J. M. (2007). A postgenomic view of the heat shock proteins in kinetoplastids. FEMS Microbiology Reviews 31, 359-377. doi: 10.1111/j.1574-6976.2007.00069.x. (Pubitemid 46920247)
26. Forafonov, F., Toogun, O. A., Grad, I., Suslova, E., Freeman, B. C. and Picard, D. (2008). p23/Sba1p protects against Hsp90 inhibitors independently of its intrinsic chaperone activity. Molecular and Cellular Biology 28, 3446-3456. doi: 10.1128/MCB.02246-07. (Pubitemid 351657106)
27. Garcia-Ranea, J. A., Mirey, G., Camonis, J. and Valencia, A. (2002). p23 and HSP20/alpha-crystallin proteins define a conserved sequence domain present in other eukaryotic protein families. FEBS Letters 529, 162-167.
28. Gartner, E. M., Silverman, P., Simon, M., Flaherty, L., Abrams, J., Ivy, P. and Lorusso, P. M. (2012). A phase II study of 17-Allylamino-17- demethoxygeldanamycin in metastatic or locally advanced, unresectable breast cancer. Breast Cancer Research and Treatment 131, 933-937. doi: 10.1007/s10549-011-1866-7.
29. Genest, P. A., ter Riet, B., Dumas, C., Papadopoulou, B., van Luenen, H. G. and Borst, P. (2005). Formation of linear inverted repeat amplicons following targeting of an essential gene in Leishmania. Nucleic Acids Research 33, 1699-1709. doi: 10.1093/nar/gki304.
30. Graefe, S. E., Wiesgigl, M., Gaworski, I., Macdonald, A. and Clos, J. (2002). Inhibition of HSP90 in Trypanosoma cruzi induces a stress response but no stage differentiation. Eukaryotic Cell 1, 936-943. (Pubitemid 36557714)
31. Hassani, K., Antoniak, E., Jardim, A. and Olivier, M. (2011). Temperature-induced protein secretion by Leishmania mexicana modulates macrophage signalling and function. PloS One 6, e18724. doi: 10.1371/journal.pone.0018724.
32. Hombach, A (2013). Mutational analysis of heat shock protein 90 from Leishmania donovani. Thesis, Faculty of Mathematics, Informatics and Science, University of Hamburg, Hamburg. http://ediss.sub.uni-hamburg.de/volltexte/2013/ 6492/.
33. Hombach, A., Ommen, G., Chrobak, M. and Clos, J. (2012). The Hsp90-Sti1 interaction is critical for Leishmania donovani proliferation in both life cycle stages. Cellular Microbiology 15, 585-600. doi: 10.1111/cmi.12057.
34. Hübel, A. and Clos, J. (1996). The genomic organization of the HSP83 gene locus is conserved in three Leishmania species. Experimental Parasitology 82, 225-228. (Pubitemid 26161940)
35. Hübel, A., Brandau, S., Dresel, A. and Clos, J. (1995). A member of the ClpB family of stress proteins is expressed during heat shock in Leishmania spp. Molecular and Biochemical Parasitology 70, 107-118.
36. Hübel, A., Krobitsch, S., Horauf, A. and Clos, J. (1997). Leishmania major Hsp100 is required chiefly in the mammalian stage of the parasite. Molecular and Cellular Biology 17, 5987-5995. (Pubitemid 27411106)
37. Hunter, K.W., Cook, C. L. and Hayunga, E. G. (1984). Leishmanial differentiation in vitro: Induction of heat shock proteins. Biochemical and Biophysical Research Communications 125, 755-760.
38. Ivens, A. C., Peacock, C. S., Worthey, E. A., Murphy, L., Aggarwal, G., Berriman, M., Sisk, E., Rajandream, M. A., Adlem, E., Aert, R., Anupama, A., Apostolou, Z., Attipoe, P., Bason, N., Bauser, C., Beck, A., Beverley, S. M., Bianchettin, G., Borzym, K., Bothe, G. and Myler, P. J. (2005). The genome of the kinetoplastid parasite, Leishmania major. Science 309, 436-442. (Pubitemid 40994677)
39. Johnson, J. L. and Brown, C. (2009). Plasticity of the Hsp90 chaperone machine in divergent eukaryotic organisms. Cell Stress and Chaperones 14, 83-94.
40. Kim, Y. E., Hipp, M. S., Bracher, A., Hayer-Hartl, M. and Hartl, F. U. (2013). Molecular chaperone functions in protein folding and proteostasis. Annual Review of Biochemistry 82, 323-355. doi: 10.1146/annurev-biochem-060208- 092442.
41. Kitson, R. R. and Moody, C. J. (2013). Learning from nature: Advances in geldanamycin-And radicicol-based inhibitors of Hsp90. Journal of Organic Chemistry 78, 5117-5141. doi: 10.1021/jo4002849.
42. Krobitsch, S. and Clos, J. (1999). A novel role for 100 kD heat shock proteins in the parasite Leishmania donovani. Cell Stress and Chaperones 4, 191-198. (Pubitemid 29435926)
43. Krobitsch, S., Brandau, S., Hoyer, C., Schmetz, C., Hübel, A. and Clos, J. (1998). Leishmania donovani heat shock protein 100: Characterization and function in amastigote stage differentiation. Journal of Biological Chemistry 273, 6488-6494. (Pubitemid 28144745)
44. Kuhls, K., Alam, M. Z., Cupolillo, E., Ferreira, G. E., Mauricio, I. L., Oddone, R., Feliciangeli, M. D., Wirth, T., Miles, M. A. and Schonian, G. (2011). Comparative microsatellite typing of new world Leishmania infantum reveals low heterogeneity among populations and its recent old world origin. PLoS Neglected Tropical Diseases 5, e1155. doi: 10.1371/journal.pntd.0001155.
45. Lambertz, U., Silverman, J. M., Nandan, D., McMaster, W. R., Clos, J., Foster, L. J. and Reiner, N. E. (2012). Secreted virulence factors and immune evasion in visceral leishmaniasis. Journal of Leukocyte Biology 91, 887-899. doi: 10.1189/jlb.0611326.
46. Lawrence, F. and Robert-Gero, M. (1985). Induction of heat shock and stress proteins in promastigotes of three Leishmania species. Proceedings of the National Academy of Sciences USA 82, 4414-4417. (Pubitemid 15234244)
47. Lee, M G., Atkinson, B. L., Giannini, S. H. and Van der Ploeg, L. H. (1988). Structure and expression of the hsp 70 gene family of Leishmania major [published erratum appears in Nucleic Acids Research 1988;16 (23):11400-11401]. Nucleic Acids Research 16, 9567-9585.
48. Lye, L. F., Owens, K., Shi, H., Murta, S. M., Vieira, A. C., Turco, S. J., Tschudi, C., Ullu, E. and Beverley, S.M. (2010). Retention and loss of RNA interference pathways in trypanosomatid protozoans. PLoS Pathogens 6, e1001161. doi: 10.1371/journal.ppat.1001161.
49. MacFarlane, J., Blaxter, M. L., Bishop, R. P., Miles, M. A. and Kelly, J. M. (1990). Identification and characterisation of a Leishmania donovani antigen belonging to the 70-kDa heat-shock protein family. European Journal of Biochemistry 190, 377-384.
50. Mauricio, I. L., Stothard, J. R. and Miles,M. A. (2000). The strange case of Leishmania chagasi. Parasitology Today 16, 188-189. (Pubitemid 30216562)
51. Miller, J. (1988). Effects of temperature elevation on mRNA and protein synthesis in Leishmania mexicana amazonensis. Molecular and Biochemical Parasitology 30, 175-184.
52. Morales, M., Watanabe, R., Dacher, M., Chafey, P., Osorio y Fortéa, J., Beverley, S., Ommen, G., Clos, J., Hem, S., Lenormand, P., Rousselle, J.-C., Namane, A. and Spath, G. (2010). Phosphoproteome dynamics reveals heat shock protein complexes specific to the Leishmania infectious stage. Proceedings of the National Academy of Sciences USA 107, 8381-8386.
53. Myler, P. J., Sisk, E., McDonagh, P. D., Martinez-Calvillo, S., Schnaufer, A., Sunkin, S. M., Yan, S., Madhubala, R., Ivens, A. and Stuart, K. (2000). Genomic organization and gene function in Leishmania. Biochemical Society Transactions 28, 527-531.
54. Nathan, D. F. and Lindquist, S. (1995). Mutational analysis of Hsp90 function: Interactions with a steroid receptor and a protein kinase. Molecular and Cellular Biology 15, 3917-3925.
55. Ochel, H. J., Eichhorn, K. and Gademann, G. (2001). Geldanamycin: The prototype of a class of antitumor drugs targeting the heat shock protein 90 family of molecular chaperones. Cell Stress and Chaperones 6, 105-112. (Pubitemid 32522216)
56. Oki, Y., Copeland, A., Romaguera, J., Fayad, L., Fanale, M., Faria Sde, C., Medeiros, L. J., Ivy, P. and Younes, A. (2012). Clinical experience with the heat shock protein-90 inhibitor, tanespimycin, in patients with relapsed lymphoma. Leukemia and Lymphoma 53, 990-992. doi: 10.3109/10428194.2011.631236.
57. Ommen, G. (2009). Charakterisierung putativer Co-Chaperonen des Parasiten Leishmania donovani (Ross, 1903). Thesis, Faculty of Mathematics, Informatics and Science, University of Hamburg, Hamburg. http://ediss.sub.uni-hamburg.de/ volltexte/2010/4507/.
58. Ommen, G., Lorenz, S. and Clos, J. (2009). One-step generation of double-Allele gene replacement mutants in Leishmania donovani. International Journal for Parasitology 39, 541-546.
59. Ommen, G., Chrobak, M. and Clos, J. (2010). The co-chaperone SGT of Leishmania donovani is essential for the parasite's viability. Cell Stress and Chaperones 39, 541-546. doi: 10.1007/s12192-009-0160-7.
60. 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. (Pubitemid 44118034)
61. 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.
62. Picard, D. (2002). Heat-shock protein 90, a chaperone for folding and regulation. Cellular and Molecular Life Sciences 59, 1640-1648.
63. Pimenta, P. F. P., Turco, S. J., McConville, M. J., Lawyer, P. G., Perkins, P. V. and Sacks, D. L. (1992). Stage-specific adhesion of Leishmania promastigotes to the sandfly midgut. Science 256, 1812-1815.
64. Pratt, W. B. and Toft, D. O. (2003). Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Experimental Biology and Medicine 228, 111-133.
65. 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.
66. Retzlaff, M., Stahl, M., Eberl, H. C., Lagleder, S., Beck, J., Kessler,H. and Buchner, J. (2009). Hsp90 is regulated by a switch point in the C-Terminal domain. EMBO Reports 10, 1147-1153. doi: Embor2009153 [pii] 10.1038/embor.2009. 153.
67. Rosenzweig, D., Smith, D., Opperdoes, F., Stern, S., Olafson, R.W. and Zilberstein, D. (2008). Retooling Leishmania metabolism: From sand fly gut to human macrophage. FASEB Journal 22, 590-602. doi: Fj.07-9254com [pii] 10.1096/fj.07-9254com.
68. Rutherford, S. L. and Zuker, C. S. (1994). Protein folding and the regulation of signaling pathways. Cell 79, 1129-1132.
69. Sacks, D. L. (1989). Metacyclogenesis in Leishmania promastigotes. Experimental Parasitology 69, 100-103.
70. Sacks, D. L. and Perkins, P. V. (1984). Identification of an infective stage of Leishmania promastigotes. Science 223, 1417-1419.
71. Sanchez, E. R., Meshinchi, S., Tienrungroj, W., Schlesinger, M. J., Toft, D. O. and Pratt,W. B. (1987). Relationship of the 90-kDa murine heat shock protein to the untransformed and transformed states of the L cell glucocorticoid receptor. Journal of Biological Chemistry 262, 6986-6991.
72. Schulte, T.W., Akinaga, S., Soga, S., Sullivan, W., Stensgard, B., Toft, D. and Neckers, L. M. (1998). Antibiotic radicicol binds to the Nterminal domain of Hsp90 and shares important biologic activities with geldanamycin. Cell Stress and Chaperones 3, 100-108.
73. Scroggins, B. T., Robzyk, K., Wang, D., Marcu, M. G., Tsutsumi, S., Beebe, K., Cotter, R. J., Felts, S., Toft, D., Karnitz, L., Rosen, N. and Neckers, L. (2007). An acetylation site in the middle domain of Hsp90 regulates chaperone function. Molecular Cell 25, 151-159. doi: 10.1016/j. molcel.2006.12.008.
74. Shapiro, R. S., Zaas, A. K., Betancourt-Quiroz, M., Perfect, J. R. and Cowen, L. E. (2012). The Hsp90 co-chaperone Sgt1 governs Candida albicans morphogenesis and drug resistance. PloS One 7, e44734. doi: 10.1371/journal. pone.0044734.
75. Sharma, S. V., Agatsuma, T. and Nakano, H. (1998). Targeting of the protein chaperone, HSP90, by the transformation suppressing agent, radicicol. Oncogene 16, 2639-2645. (Pubitemid 28264041)
76. Silverman, J. M., Clos, J., de'Oliveira, C. C., Shirvani, O., Fang, Y., Wang, C., Foster, L. J. and Reiner, N. E. (2010a). An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages. Journal of Cell Science 123, 842-852. doi: Jcs.056465 [pii] 10.1242/jcs.056465.
77. Silverman, J. M., Clos, J., Horakova, E., Wang, A. Y., Wiesgigl, M., Kelly, I., Lynn, M. A., McMaster, W. R., Foster, L. J., Levings, M. K. and Reiner, N. E. (2010b). Leishmania exosomes modulate innate and adaptive immune responses through effects on monocytes and dendritic cells. Journal of Immunology 185, 5011-5022.
78. Skeiky, Y. A., Benson, D. R., Guderian, J. A., Whittle, J. A., Bacelar, O., Carvalho, E. M. and Reed, S. G. (1995). Immune responses of leishmaniasis patients to heat shock proteins of Leishmania species and humans. Infection and Immunity 63, 4105-4114.
79. Skeiky, Y. A., Benson, D. R., Costa, J. L., Badaro, R. and Reed, S. G. (1997). Association of Leishmania heat shock protein 83 antigen and immunoglobulin G4 antibody titers in Brazilian patients with diffuse cutaneous leishmaniasis [In Process Citation]. Infection and Immunity 65, 5368-5370.
80. Smith, D. F., Whitesell, L. and Katsanis, E. (1998). Molecular chaperones: Biology and prospects for pharmacological intervention. Pharmacological Reviews 50, 493-514.
81. The Myeloma Beacon (2010). Bristol-Myers Squibb halts development of Tanespimycin. In The Myeloma Beacon, Vol. 2014. (ed. Simkovich, B.), Light Knowledge Resources LLC, Princeton, NJ, USA
82. van der Ploeg, L.H. T., Giannini, S. H. and Cantor, C. R. (1985). Heat shock genes: Regulatory role for differentiation in parasitic protozoa. Science 228, 1443-1446.
83. Vergnes, B., Gourbal, B., Girard, I., Sundar, S., Drummelsmith, J. and Ouellette, M. (2007). A proteomics screen implicates HSP83 and a small kinetoplastid calpain-related protein in drug resistance in Leishmania donovani clinical field isolates by modulating drug-induced programmed cell death. Molecular and Cellular Proteomics 6, 88-101. doi: 10.1074/mcp. M600319-MCP200. (Pubitemid 46152694)
84. Webb, J. R., Campos-Neto, A., Skeiky, Y. A. and Reed, S. G. (1997). Molecular characterization of the heat-inducible LmSTI1 protein of Leishmania major [In Process Citation]. Molecular and Biochemical Parasitology 89, 179-193.
85. Wenzel, U. A., Bank, E., Florian, C., Forster, S., Zimara, N., Steinacker, J., Klinger, M., Reiling, N., Ritter, U. and van Zandbergen, G. (2012). Leishmania major parasite stage-dependent host cell invasion and immune evasion. FASEB Journal 26, 29-39. doi: 10.1096/fj.11-184895.
86. Whitesell, L. and Cook, P. (1996). Stable and specific binding of heat shock protein 90 by geldanamycin disrupts glucocorticoid receptor function in intact cells. Molecular Endocrinology 10, 705-712. (Pubitemid 26176278)
87. Whitesell, L. and Lindquist, S. L. (2005). Hsp90 and the chaperoning of cancer. Nature Reviews Cancer 5, 761-772.
88. Whitesell, L., Mimnaugh, E. G., De Costa, B., Myers, C. E. and Neckers, L. M. (1994). Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: Essential role for stress proteins in oncogenic transformation. Proceedings of the National Academy of Sciences USA 91, 8324-8328.
89. Wiesgigl, M. and Clos, J. (2001). Heat shock protein 90 homeostasis controls stage differentiation in Leishmania donovani. Molecular Biology of the Cell 12, 3307-3316. (Pubitemid 33108466)
90. Wilson, M. E., Andersen, K. A. and Britigan, B. E. (1994). Response of Leishmania chagasi promastigotes to oxidant stress. Infection and Immunity 62, 5133-5141.
91. Workman, P., Burrows, F., Neckers, L. and Rosen, N. (2007). Drugging the cancer chaperone HSP90: Combinatorial therapeutic exploitation of oncogene addiction and tumor stress. Annals of the New York Academy of Sciences 1113, 202-216. (Pubitemid 350015011)
92. Zhang, T., Hamza, A., Cao, X., Wang, B., Yu, S., Zhan, C. G. and Sun, D. (2008). A novel Hsp90 inhibitor to disrupt Hsp90/Cdc37 complex against pancreatic cancer cells. Molecular Cancer Therapeutics 7, 162-170. doi: 10.1158/1535-7163.MCT-07-0484.
93. Zilberstein, D. and Shapira, M. (1994). The role of pH and temperature in the development of Leishmania parasites. Annual Review of Microbiology 48, 449-470. (Pubitemid 24334105)
94. Zilka, A., Garlapati, S., Dahan, E., Yaolsky, V. and Shapira, M. (2001). Developmental regulation of HSP83 in Leishmania: Transcript levels are controlled by the efficiency of 3? RNA processing and preferential translation is directed by a determinant in the 3′ UTR. Journal of Biological Chemistry 11, 11.