Mutations that increase both Hsp90 ATPase activity in vitro and Hsp90 drug resistance in vivo

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1803, Issue 5, 2010, Pages 575-583

  Zurawska, Anna ^a,b   Urbanski, Jakub ^a,c,d   Matuliene, Jurgita ^e   Baraniak, Janina ^f   Klejman, Marcin P ^a   Filipek, Slawomir ^a,g   Matulis, Daumantas ^e   Bieganowski, Pawel ^a,h  

^a INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^b INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^c NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^d UTRECHT UNIVERSITY   (Netherlands)

^e VILNIUS UNIVERSITY   (Lithuania)

^f CENTRE OF MOLECULAR AND MACROMOLECULAR STUDIES   (Poland)

^g UNIVERSITY OF WARSAW   (Poland)

^h MOSSAKOWSKI MEDICAL RESEARCH CENTRE   (Poland)

Author keywords

17 AAG; Aha1; ATPase; Geldanamycin; Hsp90; Inhibitor; Radicicol

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; PROTEIN AHA1; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CELL MEMBRANE RESISTANCE; CONTROLLED STUDY; DRUG PROTEIN BINDING; DRUG RESISTANCE; ENZYME ACTIVITY; FUNGAL CELL; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SUBSTITUTION; BENZOQUINONES; BLOTTING, WESTERN; CHAPERONINS; DRUG RESISTANCE; ENZYME INHIBITORS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOPRECIPITATION; KIDNEY; LACTAMS, MACROCYCLIC; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 77951938125     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2010.03.002     Document Type: Article

References (46)

1. Wandinger S.K., Richter K., Buchner J. The Hsp90 chaperone machinery. J. Biol. Chem. 2008, 283:18473-18477.
2. Pearl L.H., Prodromou C., Workman P. The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem. J. 2008, 410:439-453.
3. Chadli A., Felts S.J., Toft D.O. GCUNC45 is the first Hsp90 co-chaperone to show alpha/beta isoform specificity. J. Biol. Chem. 2008, 283:9509-9512.
4. Didelot C., Lanneau D., Brunet M., Bouchot A., Cartier J., Jacquel A., Ducoroy P., Cathelin S., Decologne N., Chiosis G., Dubrez-Daloz L., Solary E., Garrido C. Interaction of heat-shock protein 90 beta isoform (HSP90 beta) with cellular inhibitor of apoptosis 1 (c-IAP1) is required for cell differentiation. Cell Death Differ. 2008, 15:859-866.
5. Kunisawa J., Shastri N. Hsp90alpha chaperones large C-terminally extended proteolytic intermediates in the MHC class I antigen processing pathway. Immunity 2006, 24:523-534.
6. Taherian A., Krone P.H., Ovsenek N. A comparison of Hsp90alpha and Hsp90beta interactions with cochaperones and substrates. Biochem. Cell Biol. 2008, 86:37-45.
7. Shinozaki F., Minami M., Chiba T., Suzuki M., Yoshimatsu K., Ichikawa Y., Terasawa K., Emori Y., Matsumoto K., Kurosaki T., Nakai A., Tanaka K., Minami Y. Depletion of hsp90beta induces multiple defects in B cell receptor signaling. J. Biol. Chem. 2006, 281:16361-16369.
8. Voss A.K., Thomas T., Gruss P. Mice lacking HSP90beta fail to develop a placental labyrinth. Development 2000, 127:1-11.
9. Metchat A., Akerfelt M., Bierkamp C., Delsinne V., Sistonen L., Alexandre H., Christians E.S. Mammalian heat shock factor 1 is essential for oocyte meiosis and directly regulates Hsp90 alpha expression. J. Biol. Chem. 2009, 284:9521-9528.
10. Prodromou C., Panaretou B., Chohan S., Siligardi G., O'Brien R., Ladbury J.E., Roe S.M., Piper P.W., Pearl L.H. The ATPase cycle of Hsp90 drives a molecular 'clamp' via transient dimerization of the N-terminal domains. EMBO J. 2000, 19:4383-4392.
11. Richter K., Walter S., Buchner J. The co-chaperone Sba1 connects the ATPase reaction of Hsp90 to the progression of the chaperone cycle. J. Mol. Biol. 2004, 342:1403-1413.
12. McLaughlin S.H., Sobott F., Yao Z.P., Zhang W., Nielsen P.R., Grossmann J.G., Laue E.D., Robinson C.V., Jackson S.E. The co-chaperone p23 arrests the Hsp90 ATPase cycle to trap client proteins. J. Mol. Biol. 2006, 356:746-758.
13. Lotz G.P., Lin H., Harst A., Obermann W.M. Aha1 binds to the middle domain of Hsp90, contributes to client protein activation, and stimulates the ATPase activity of the molecular chaperone. J. Biol. Chem. 2003, 278:17228-17235.
14. Panaretou B., Siligardi G., Meyer P., Maloney A., Sullivan J.K., Singh S., Millson S.H., Clarke P.A., Naaby-Hansen S., Stein R., Cramer R., Mollapour M., Workman P., Piper P.W., Pearl L.H., Prodromou C. Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone aha1. Mol. Cell 2002, 10:1307-1318.
15. Meyer P., Prodromou C., Liao C., Hu B., Roe S.M., Vaughan C.K., Vlasic I., Panaretou B., Piper P.W., Pearl L.H. Structural basis for recruitment of the ATPase activator Aha1 to the Hsp90 chaperone machinery. EMBO J. 2004, 23:1402-1410.
16. Smith D.F., Whitesell L., Nair S.C., Chen S., Prapapanich V., Rimerman R.A. Progesterone receptor structure and function altered by geldanamycin, an hsp90-binding agent. Mol. Cell. Biol. 1995, 15:6804-6812.
17. Sharma S.V., Agatsuma T., Nakano H. Targeting of the protein chaperone, HSP90, by the transformation suppressing agent, radicicol. Oncogene 1998, 16:2639-2645.
18. Schulte T.W., Neckers L.M. The benzoquinone ansamycin 17-allylamino-17-demethoxygeldanamycin binds to HSP90 and shares important biologic activities with geldanamycin. Cancer Chemother. Pharmacol. 1998, 42:273-279.
19. Roe S.M., Prodromou C., O'Brien R., Ladbury J.E., Piper P.W., Pearl L.H. Structural basis for inhibition of the Hsp90 molecular chaperone by the antitumor antibiotics radicicol and geldanamycin. J. Med. Chem. 1999, 42:260-266.
20. Neckers L. Heat shock protein 90: the cancer chaperone. J. Biosci. 2007, 32:517-530.
21. Pearl L.H., Prodromou C., Workman P. The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem. J. 2008, 410:439-453.
22. Robinson J.S., Klionsky D.J., Banta L.M., Emr S.D. Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol. Cell. Biol. 1988, 8:4936-4948.
23. Brachmann C.B., Davies A., Cost G.J., Caputo E., Li J., Hieter P., Boeke J.D. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 1998, 14:115-132.
24. F.M. Ausbel, R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, K. Struhl, in: F.M. Ausbel, R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, K. Struhl (Eds.), Short protocols in molecular biology, John Wiley & Sons, Inc., N.Y., 1999, pp. 13.11-13.33, 13.50-13.56.
25. Mumberg D., Muller R., Funk M. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 1995, 156:119-122.
26. Whitesell L., Mimnaugh E.G., De Costa B., Myers C.E., Neckers L.M. Inhibition of heat shock protein HSP90-pp 60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:8324-8328.
27. Cikotiene I., Kazlauskas E., Matuliene J., Michailoviene V., Torresan J., Jachno J., Matulis D. 5-Aryl-4-(5-substituted-2, 4-dihydroxyphenyl)-1, 2, 3-thiadiazoles as inhibitors of Hsp90 chaperone. Bioorg. Med. Chem. Lett. 2009, 19:1089-1092.
28. Piper P.W., Panaretou B., Millson S.H., Trumana A., Mollapour M., Pearl L.H., Prodromou C. Yeast is selectively hypersensitised to heat shock protein 90 (Hsp90)-targetting drugs with heterologous expression of the human Hsp90beta, a property that can be exploited in screens for new Hsp90 chaperone inhibitors. Gene 2003, 302:165-170.
29. David C.L., Smith H.E., Raynes D.A., Pulcini E.J., Whitesell L. Expression of a unique drug-resistant Hsp90 ortholog by the nematode Caenorhabditis elegans. Cell Stress Chaperones 2003, 8:93-104.
30. Piper P.W., Millson S.H., Mollapour M., Panaretou B., Siligardi G., Pearl L.H., Prodromou C. Sensitivity to Hsp90-targeting drugs can arise with mutation to the Hsp90 chaperone, cochaperones and plasma membrane ATP binding cassette transporters of yeast. Eur. J. Biochem. 2003, 270:4689-4695.
31. MacLean M.J., Llordella M.M., Bot N., Picard D. A yeast-based assay reveals a functional defect of the Q488H polymorphism in human Hsp90alpha. Biochem. Biophys. Res. Commun. 2005, 337:133-137.
32. Jayanthan A., Fowler J., Hawkins L., Lamers F., Teja B., Incoronato A., Anderson R., Narendran A. Effects of Hsp90 inhibition in neuroblastoma: analysis of drug sensitivity, target modulation and the influence of bone marrow microenvironment. J. Exp. Ther. Oncol. 2008, 7:183-193.
33. Barginear M.F., Van Poznak C., Rosen N., Modi S., Hudis C.A., Budman D.R. The heat shock protein 90 chaperone complex: an evolving therapeutic target. Curr. Cancer Drug Targets 2008, 8:522-532.
34. Shah N.P., Sawyers C.L. Mechanisms of resistance to STI571 in Philadelphia chromosome-associated leukemias. Oncogene 2003, 22:7389-7395.
35. Engelman J.A., Janne P.A. Mechanisms of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancer. Clin. Cancer Res. 2008, 14:2895-2899.
36. Antonescu C.R., Besmer P., Guo T., Arkun K., Hom G., Koryotowski B., Leversha M.A., Jeffrey P.D., Desantis D., Singer S., Brennan M.F., Maki R.G., DeMatteo R.P. Acquired resistance to imatinib in gastrointestinal stromal tumor occurs through secondary gene mutation. Clin. Cancer Res. 2005, 11:4182-4190.
37. Diehl M.C., Idowu M.O., Kimmelshue K., York T.P., Elmore L.W., Holt S.E. Elevated expression of nuclear Hsp90 in invasive breast tumors. Cancer Biol. Ther. 2009, 8:1952-1961.
38. McCarthy M.M., Pick E., Kluger Y., Gould-Rothberg B., Lazova R., Camp R.L., Rimm D.L., Kluger H.M. HSP90 as a marker of progression in melanoma. Ann. Oncol. 2008, 19:590-594.
39. Pick E., Kluger Y., Giltnane J.M., Moeder C., Camp R.L., Rimm D.L., Kluger H.M. High HSP90 expression is associated with decreased survival in breast cancer. Cancer Res. 2007, 67:2932-2937.
40. Guo W., Reigan P., Siegel D., Zirrolli J., Gustafson D., Ross D. Formation of 17-allylamino-demethoxygeldanamycin (17-AAG) hydroquinone by NAD(P)H:quinone oxidoreductase 1: role of 17-AAG hydroquinone in heat shock protein 90 inhibition. Cancer Res. 2005, 65:10006-10015.
41. Douglas M., Lim A.R., Porter J.R., West K., Pink M.M., Ge J., Wylie A.A., Tibbits T.T., Biggs K., Curtis M., Palombella V.J., Adams J., Fritz C.C., Normant E. The antiproliferative activity of the heat shock protein 90 inhibitor IPI-504 is not dependent on NAD(P)H:quinone oxidoreductase 1 activity in vivo. Mol. Cancer Ther. 2009, 8:3369-3378.
42. Holmes J.L., Sharp S.Y., Hobbs S., Workman P. Silencing of HSP90 cochaperone AHA1 expression decreases client protein activation and increases cellular sensitivity to the HSP90 inhibitor 17-allylamino-17-demethoxygeldanamycin. Cancer Res. 2008, 68:1188-1197.
43. Ali M.M., Roe S.M., Vaughan C.K., Meyer P., Panaretou B., Piper P.W., Prodromou C., Pearl L.H. Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 2006, 440:1013-1017.
44. Prodromou C., Siligardi G., O'Brien R., Woolfson D.N., Regan L., Panaretou B., Ladbury J.E., Piper P.W., Pearl L.H. Regulation of Hsp90 ATPase activity by tetratricopeptide repeat (TPR)-domain co-chaperones. EMBO J. 1999, 18:754-762.
45. Forafonov F., Toogun O.A., Grad I., Suslova E., Freeman B.C., Picard D. p23/Sba1p protects against Hsp90 inhibitors independently of its intrinsic chaperone activity. Mol. Cell. Biol. 2008, 28:3446-3456.
46. Prodromou C., Nuttall J.M., Millson S.H., Roe S.M., Sim T.S., Tan D., Workman P., Pearl L.H., Piper P.W. Structural basis of the radicicol resistance displayed by a fungal hsp90. ACS Chem. Biol. 2009, 4:289-297.