Identification of a key lysine residue in heat shock protein 90 required for azole and echinocandin resistance in Aspergillus fumigatus

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 4, 2014, Pages 1889-1896

  Lamoth, Fréd́eric ^a,c   Juvvadi, Praveen R ^a   Soderblom, Erik J ^b   Moseley, M Arthur ^b   Asfaw, Yohannes G ^a   Steinbacha, William J ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY   (United States)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CASPOFUNGIN; ECHINOCANDIN; HEAT SHOCK PROTEIN 90; LYSINE; PHOSPHOPEPTIDE; PYRROLE; TRICHOSTATIN A; VORICONAZOLE;

ACETYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIFUNGAL RESISTANCE; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; ASPERGILLUS FUMIGATUS; CANDIDA ALBICANS; CONTROLLED STUDY; DEACETYLATION; FUNGAL VIRULENCE; INVASIVE ASPERGILLOSIS; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; TANDEM MASS SPECTROMETRY;

ANTIFUNGAL AGENTS; ASPERGILLUS FUMIGATUS; AZOLES; DRUG RESISTANCE, FUNGAL; ECHINOCANDINS; HSP90 HEAT-SHOCK PROTEINS; LYSINE;

EID: 84896907500     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02286-13     Document Type: Article

References (44)

1. Steinbach WJ, Marr KA, Anaissie EJ, Azie N, Quan SP, Meier-Kriesche HU, Apewokin S, Horn DL. 2012. Clinical epidemiology of 960 patients with invasive aspergillosis from the PATH Alliance registry. J. Infect. 65:453-464. http://dx.doi.org/10.1016/j.jinf.2012.08.003.
2. Walsh TJ, Anaissie EJ, Denning DW, Herbrecht R, Kontoyiannis DP, Marr KA, Morrison VA, Segal BH, Steinbach WJ, Stevens DA, van Burik JA, Wingard JR, Patterson TF. 2008. Treatment of aspergillosis: clinical practice guidelines of the Infectious Diseases Society of America. Clin. Infect. Dis. 46:327-360. http://dx.doi.org/10.1086/525258. (Pubitemid 351265310)
3. Howard SJ, Cerar D, Anderson MJ, Albarrag A, Fisher MC, Pasqualotto AC, Laverdiere M, Arendrup MC, Perlin DS, Denning DW. 2009. Frequency and evolution of Azole resistance in Aspergillus fumigatus associated with treatment failure. Emerg. Infect. Dis. 15:1068-1076. http://dx.doi.org/10.3201/eid1507.090043.
4. Marr K, Schlamm H, Rottinghaus ST, Jagannatha S, Bow EJ, Wingard JR, Pappas P, Hebrecht R, Walsh TJ, Maertens J. 2012. A randomised, double-bind study of combination antifungal therapy with voriconazole and anidulafungin versus voriconazole monotherapy for primary treatment of invasive aspergillosis, abstr LB2812. Absourcestr. 22nd Eur. Congr. Clin. Microbiol. Infect. Dis., London, United Kingdom, 31 March to 3 April 2012.
5. Cowen LE. 2008. The evolution of fungal drug resistance: modulating the trajectory from genotype to phenotype. Nat. Rev. Microbiol. 6:187-198. http://dx.doi.org/10.1038/nrmicro1835. (Pubitemid 351256314)
6. Cowen LE, Singh SD, Kohler JR, Collins C, Zaas AK, Schell WA, Aziz H, Mylonakis E, Perfect JR, Whitesell L, Lindquist S. 2009. Harnessing Hsp90 function as a powerful, broadly effective therapeutic strategy for fungal infectious disease. Proc. Natl. Acad. Sci. U. S. A. 106:2818-2823. http://dx.doi.org/10.1073/pnas.0813394106.
7. Lamoth F, Juvvadi PR, Fortwendel JR, Steinbach WJ. 2012. Heat shock protein 90 is required for conidiation and cell wall integrity in Aspergillus fumigatus. Eukaryot. Cell 11:1324-1332. http://dx.doi.org/10.1128/EC.00032-12.
8. Lamoth F, Juvvadi PR, Gehrke C, Steinbach WJ. 2013. In vitro activity of calcineurin and heat shock protein 90 Inhibitors against Aspergillus fumigatus azole- and echinocandin-resistant strains. Antimicrob. Agents Chemother. 57:1035-1039. http://dx.doi.org/10.1128/AAC.01857-12.
9. Whitesell L, Lindquist SL. 2005. HSP90 and the chaperoning of cancer. Nat. Rev. Cancer. 5:761-772. http://dx.doi.org/10.1038/nrc1716. (Pubitemid 41400776)
10. Cowen LE, Lindquist S. 2005. Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 309:2185-2189. http://dx.doi.org/10.1126/science.1118370. (Pubitemid 41396062)
11. Singh SD, Robbins N, Zaas AK, Schell WA, Perfect JR, Cowen LE. 2009. Hsp90 governs echinocandin resistance in the pathogenic yeast Candida albicans via calcineurin. PLoS Pathog. 5:e1000532. http://dx.doi.org/10.1371/journal. ppat.1000532.
12. Lamoth F, Juvvadi PR, Gehrke C, Asfaw YG, Steinbach WJ. 4 October 2013. Transcriptional activation of heat shock protein 90 (Hsp90) mediated via a proximal promoter region as trigger of caspofungin resistance in Aspergillus fumigatus. J. Infect. Dis. http://dx.doi.org/10.1093/infdis/jit530.
13. Mollapour M, Neckers L. 2012. Post-translational modifications of Hsp90 and their contributions to chaperone regulation. Biochim. Biophys. Acta 1823:648-655. http://dx.doi.org/10.1016/j.bbamcr.2011.07.018.
14. Mollapour M, Tsutsumi S, Kim YS, Trepel J, Neckers L. 2011. Casein kinase 2 phosphorylation of Hsp90 threonine 22 modulates chaperone function and drug sensitivity. Oncotarget 2:407-417.
15. Soroka J, Wandinger SK, Mausbacher N, Schreiber T, Richter K, Daub H, Buchner J. 2012. Conformational switching of the molecular chaperone Hsp90 via regulated phosphorylation. Mol. Cell 45:517-528. http://dx.doi.org/10.1016/j. molcel.2011.12.031.
16. Scroggins BT, Robzyk K, Wang D, Marcu MG, Tsutsumi S, Beebe K, Cotter RJ, Felts S, Toft D, Karnitz L, Rosen N, Neckers L. 2007. An acetylation site in the middle domain of Hsp90 regulates chaperone function. Mol. Cell 25:151-159. http://dx.doi.org/10.1016/j.molcel.2006.12.008. (Pubitemid 46049066)
17. Bali P, Pranpat M, Bradner J, Balasis M, Fiskus W, Guo F, Rocha K, Kumaraswamy S, Boyapalle S, Atadja P, Seto E, Bhalla K. 2005. Inhibition of histone deacetylase 6 acetylates and disrupts the chaperone function of heat shock protein 90: a novel basis for antileukemia activity of histone deacetylase inhibitors. J. Biol. Chem. 280: 26729-26734. http://dx.doi.org/10.1074/jbc. C500186200. (Pubitemid 41040705)
18. Kovacs JJ, Murphy PJ, Gaillard S, Zhao X, Wu JT, Nicchitta CV, Yoshida M, Toft DO, Pratt WB, Yao TP. 2005. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol. Cell 18:601-607. http://dx.doi.org/10.1016/j.molcel.2005.04.021. (Pubitemid 40726236)
19. Nimmanapalli R, Fuino L, Bali P, Gasparetto M, Glozak M, Tao J, Moscinski L, Smith C, Wu J, Jove R, Atadja P, Bhalla K. 2003. Histone deacetylase inhibitor LAQ824 both lowers expression and promotes proteasomal degradation of Bcr-Abl and induces apoptosis of imatinib mesy-late- sensitive or -refractory chronic myelogenous leukemia-blast crisis cells. Cancer Res. 63:5126-5135. (Pubitemid 37022654)
20. Yu X, Guo ZS, Marcu MG, Neckers L, Nguyen DM, Chen GA, Schrump DS. 2002. Modulation of p53, ErbB1, ErbB2, and Raf-1 expression in lung cancer cells by depsipeptide FR901228. J. Natl. Cancer Inst. 94:504-513. http://dx.doi.org/10. 1093/jnci/94.7.504. (Pubitemid 34411289)
21. Robbins N, Leach MD, Cowen LE. 2012. Lysine deacetylases Hda1 and Rpd3 regulate Hsp90 function thereby governing fungal drug resistance. Cell Rep. 2:878-888. http://dx.doi.org/10.1016/j.celrep.2012.08.035.
22. Juvvadi PR, Belina D, Soderblom EJ, Moseley MA, Steinbach WJ. 2013. Filamentous fungal-specific septin AspE is phosphorylated in vivo and interacts with actin, tubulin and other septins in the human pathogen Aspergillus fumigatus. Biochem. Biophys. Res. Commun. 431:547-553. http://dx.doi.org/10. 1016/j.bbrc.2013.01.020.
23. Shimizu K, Keller NP. 2001. Genetic involvement of a cAMP-dependent protein kinase in a G protein signaling pathway regulating morphological and chemical transitions in Aspergillus nidulans. Genetics 157:591-600. (Pubitemid 32165018)
24. Beausoleil SA, Villen J, Gerber SA, Rush J, Gygi SP. 2006. A probabilitybased approach for high-throughput protein phosphorylation analysis and site localization. Nat. Biotechnol. 24:1285-1292. http://dx.doi.org/10.1038/ nbt1240. (Pubitemid 44564776)
25. Wang YH, Tsay YG, Tan BC, Lo WY, Lee SC. 2003. Identification and characterization of a novel p300-mediated p53 acetylation site, lysine 305. J. Biol. Chem. 278:25568-25576. http://dx.doi.org/10.1074/jbc.M212574200. (Pubitemid 36835309)
26. Szewczyk E, Nayak T, Oakley CE, Edgerton H, Xiong Y, Taheri-Talesh N, Osmani SA, Oakley BR. 2006. Fusion PCR and gene targeting in Aspergillus nidulans. Nat. Protoc. 1:3111-3120. http://dx.doi.org/10.1038/nprot.2006.405.
27. Langfelder K, Philippe B, Jahn B, Latge JP, Brakhage AA. 2001. Differential expression of the Aspergillus fumigatus pksP gene detected in vitro and in vivo with green fluorescent protein. Infect. Immun. 69:6411-6418. http://dx.doi.org/10.1128/IAI.69.10.6411-6418.2001. (Pubitemid 32885206)
28. Pinchai N, Perfect BZ, Juvvadi PR, Fortwendel JR, Cramer RA, Jr, Asfaw YG, Heitman J, Perfect JR, Steinbach WJ. 2009. Aspergillus fumigatus calcipressin CbpA is involved in hyphal growth and calcium homeostasis. Eukaryot. Cell 8:511-519. http://dx.doi.org/10.1128/EC.00336-08.
29. Juvvadi PR, Fortwendel JR, Rogg LE, Burns KA, Randell SH, Steinbach WJ. 2011. Localization and activity of the calcineurin catalytic and regulatory subunit complex at the septum is essential for hyphal elongation and proper septation in Aspergillus fumigatus. Mol. Microbiol. 82:1235-1259. http://dx.doi.org/10.1111/j.1365-2958.2011.07886.x.
30. Burt ET, Daly R, Hoganson D, Tsirulnikov Y, Essmann M, Larsen B. 2003. Isolation and partial characterization of Hsp90 from Candida albicans. Ann. Clin. Lab. Sci. 33:86-93. (Pubitemid 36337003)
31. Steinbach WJ, Benjamin DK, Jr, Trasi SA, Miller JL, Schell WA, Zaas AK, Foster WM, Perfect JR. 2004. Value of an inhalational model of invasive aspergillosis. Med. Mycol. 42:417-425. http://dx.doi.org/10.1080/ 13693780410001712034. (Pubitemid 39445473)
32. Rocha EM, Garcia-Effron G, Park S, Perlin DS. 2007. A Ser678Pro substitution in Fks1p confers resistance to echinocandin drugs in Aspergillus fumigatus. Antimicrob. Agents Chemother. 51:4174-4176. http://dx.doi.org/10. 1128/AAC.00917-07.\ (Pubitemid 350057823)
33. Clinical and Laboratory Standards Institute. 2008. Reference method for broth dilution antifungal susceptibility testing of filamentous fungi, 2nd ed. CLSI document M38-A2. Clinical and Laboratory Standards Institute, Wayne, PA.
34. Hwang CS, Shemorry A, Varshavsky A. 2010. N-terminal acetylation of cellular proteins creates specific degradation signals. Science 327:973-977. http://dx.doi.org/10.1126/science.1183147.
35. Pfaller MA, Messer SA, Georgopapadakou N, Martell LA, Besterman JM, Diekema DJ. 2009. Activity of MGCD290, a Hos2 histone deacetylase inhibitor, in combination with azole antifungals against opportunistic fungal pathogens. J. Clin. Microbiol. 47:3797-3804. http://dx.doi.org/10.1128/JCM.00618-09.
36. Smith WL, Edlind TD. 2002. Histone deacetylase inhibitors enhance Candida albicans sensitivity to azoles and related antifungals: correlation with reduction in CDR and ERG upregulation. Antimicrob. Agents Chemother. 46:3532-3539. http://dx.doi.org/10.1128/AAC.46.11.3532-3539.2002. (Pubitemid 35192922)
37. Eyrich B, Sickmann A, Zahedi RP. 2011. Catch me if you can: mass spectrometry-based phosphoproteomics and quantification strategies. Proteomics 11:554-570. http://dx.doi.org/10.1002/pmic.201000489.
38. Cervoni N, Szyf M. 2001. Demethylase activity is directed by histone acetylation. J. Biol. Chem. 276:40778-40787. http://dx.doi.org/10.1074/jbc. M103921200.
39. Tribus M, Galehr J, Trojer P, Brosch G, Loidl P, Marx F, Haas H, Graessle S. 2005. HdaA, a major class 2 histone deacetylase of Aspergillus nidulans, affects growth under conditions of oxidative stress. Eukaryot. Cell 4:1736-1745. http://dx.doi.org/10.1128/EC.4.10.1736-1745.2005. (Pubitemid 41484232)
40. Trojer P, Brandtner EM, Brosch G, Loidl P, Galehr J, Linzmaier R, Haas H, Mair K, Tribus M, Graessle S. 2003. Histone deacetylases in fungi: novel members, new facts. Nucleic Acids Res. 31:3971-3981. http://dx.doi.org/10.1093/ nar/gkg473. (Pubitemid 37442276)
41. Tribus M, Bauer I, Galehr J, Rieser G, Trojer P, Brosch G, Loidl P, Haas H, Graessle S. 2010. A novel motif in fungal class 1 histone deacetylases is essential for growth and development of Aspergillus. Mol. Biol. Cell 21:345-353. http://dx.doi.org/10.1091/mbc.E09-08-0750.
42. Sanderson L, Taylor GW, Aboagye EO, Alao JP, Latigo JR, Coombes RC, Vigushin DM. 2004. Plasma pharmacokinetics and metabolism of the histone deacetylase inhibitor trichostatin a after intraperitoneal administration to mice. Drug Metab. Dispos. 32:1132-1138. http://dx.doi.org/10.1124/dmd.104. 000638. (Pubitemid 39287587)
43. Elaut G, Laus G, Alexandre E, Richert L, Bachellier P, Tourwe D, Rogiers V, Vanhaecke T. 2007. A metabolic screening study of trichostatin A (TSA) and TSA-like histone deacetylase inhibitors in rat and human primary hepatocyte cultures. J. Pharmacol. Exp. Ther. 321:400-408. http://dx.doi.org/10.1124/jpet. 106.116202. (Pubitemid 46463891)
44. Kaliszczak M, Trousil S, Aberg O, Perumal M, Nguyen QD, Aboagye EO. 2013. A novel small molecule hydroxamate preferentially inhibits HDAC6 activity and tumour growth. Br. J. Cancer 108:342-350. http://dx.doi.org/10.1038/bjc.2012. 576.