Histone deacetylase inhibition as an alternative strategy against invasive aspergillosis

Frontiers in Microbiology

Volumn 6, Issue FEB, 2015, Pages

  Lamoth, Frédéric ^a,b   Juvvadi, Praveen R ^a   Steinbach, William J ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Antifungal resistance; Antifungal therapy; Aspergillus fumigatus; Heat shock protein 90; Lysine deacetylases; Trichostatin A

Indexed keywords

AMPHOTERICIN B; CASPOFUNGIN; CHAPERONE; FLUCONAZOLE; GELDANAMYCIN; HEAT SHOCK PROTEIN 90; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; POSACONAZOLE; SIRTUIN; TRICHOSTATIN A; VORICONAZOLE;

ANTIFUNGAL ACTIVITY; ASPERGILLUS FUMIGATUS; ASPERGILLUS NIDULANS; ASPERGILLUS ORYZAE; CANDIDA ALBICANS; ENZYME ACTIVITY; EVOLUTIONARY ADAPTATION; FUNGUS GROWTH; GENE DELETION; GENE REPRESSION; GENE SEQUENCE; GENETIC TRANSCRIPTION; HUMAN; INVASIVE ASPERGILLOSIS; LOMENTOSPORA PROLIFICANS; MAGNAPORTHE ORYZAE; MUTATIONAL ANALYSIS; OXIDATIVE STRESS; PHASE 2 CLINICAL TRIAL (TOPIC); PLASMODIUM FALCIPARUM; RANDOMIZED CONTROLLED TRIAL (TOPIC); SACCHAROMYCES CEREVISIAE; SHORT SURVEY; STRESS; TOXOPLASMA GONDII; VIRULENCE;

ASPERGILLUS; ASPERGILLUS FUMIGATUS;

EID: 84927553790     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00096     Document Type: Short Survey

References (55)

1. Augenbraun, M., Livingston, J., Parker, R., Lederman, S., Chavoustie, S., Morgan, F., et al. (2013). "Fluconazole and MGCD290 in vulvo vaginal candidiasis (VVC): results from a randomized phase II study (1330), " in IDWeek 2013, October 2-6, 2013, San Francisco, CA.
2. Baidyaroy, D., Brosch, G., Ahn, J. H., Graessle, S., Wegener, S., Tonukari, N. J., et al. (2001). A gene related to yeast HOS2 histone deacetylase affects extracellular depolymerase expression and virulence in a plant pathogenic fungus. Plant Cell 13, 1609-1624. doi: 10.1105/tpc.13.7.1609.
3. Bali, P., Pranpat, M., Bradner, J., Balasis, M., Fiskus, W., Guo, F., et al. (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. doi: 10.1074/jbc.C500186200.
4. Blum, G., Kainzner, B., Grif, K., Dietrich, H., Zelger, B., Sonnweber, T., et al. (2013). In vitro and in vivo role of heat shock protein 90 in Amphotericin B resistance of Aspergillus terreus. Clin. Microbiol. Infect. 19, 50-55. doi: 10.1111/j.1469-0691.2012.03848.x.
5. Brosch, G., Loidl, P., and Graessle, S. (2008). Histone modifications and chromatin dynamics: a focus on filamentous fungi. FEMS Microbiol. Rev. 32, 409-439. doi: 10.1111/j.1574-6976.2007.00100.x.
6. Carmen, A. A., Griffin, P. R., Calaycay, J. R., Rundlett, S. E., Suka, Y., and Grunstein, M. (1999). Yeast HOS3 forms a novel trichostatin A-insensitive homodimer with intrinsic histone deacetylase activity. Proc. Natl. Acad. Sci. U.S.A. 96, 12356-12361. doi: 10.1073/pnas.96.22.12356.
7. Choudhary, C., Kumar, C., Gnad, F., Nielsen, M. L., Rehman, M., Walther, T. C., et al. (2009). Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325, 834-840. doi: 10.1126/science.1175371.
8. Cowen, L. E. (2013). The fungal Achilles' heel: targeting Hsp90 to cripple fungal pathogens. Curr. Opin. Microbiol. 16, 377-384. doi: 10.1016/j.mib.2013.03.005.
9. Cowen, L. E., and Lindquist, S. (2005). Hsp90 potentiates the rapid evolution of new traits: drug resistance in diverse fungi. Science 309, 2185-2189. doi: 10.1126/science.1118370.
10. Cowen, L. E., Singh, S. D., Kohler, J. R., Collins, C., Zaas, A. K., Schell, W. A., et al. (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. doi: 10.1073/pnas.0813394106.
11. Ding, S. L., Liu, W., Iliuk, A., Ribot, C., Vallet, J., Tao, A., et al. (2010). The tig1 histone deacetylase complex regulates infectious growth in the rice blast fungus Magnaporthe oryzae. Plant Cell 22, 2495-2508. doi: 10.1105/tpc.110.074302.
12. Duvic, M., Talpur, R., Ni, X., Zhang, C., Hazarika, P., Kelly, C., et al. (2007). Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood 109, 31-39. doi: 10.1182/blood-2006-06-025999.
13. Duvic, M., Olsen, E. A., Breneman, D., Pacheco, T. R., Parker, S., Vonderheid, E. C., et al. (2009). Evaluation of the long-term tolerability and clinical benefit of vorinostat in patients with advanced cutaneous T-cell lymphoma. Clin. Lymphoma Myeloma 9, 412-416. doi: 10.3816/CLM.2009.n.082.
14. Fouladi, M., Park, J. R., Stewart, C. F., Gilbertson, R. J., Schaiquevich, P., Sun, J., et al. (2010). Pediatric phase I trial and pharmacokinetic study of vorinostat: a Children's Oncology Group phase I consortium report. J. Clin. Oncol. 28, 3623-3629. doi: 10.1200/JCO.2009.25.9119.
15. Glozak, M. A., Sengupta, N., Zhang, X., and Seto, E. (2005). Acetylation and deacetylation of non-histone proteins. Gene 363, 15-23. doi: 10.1016/j.gene.2005.09.010.
16. Graessle, S., Dangl, M., Haas, H., Mair, K., Trojer, P., Brandtner, E. M., et al. (2000). Characterization of two putative histone deacetylase genes from Aspergillus nidulans. Biochim. Biophys. Acta 1492, 120-126. doi: 10.1016/S0167-4781(00)00093-2.
17. Henrikson, J. C., Hoover, A. R., Joyner, P. M., and Cichewicz, R. H. (2009). A chemical epigenetics approach for engineering the in situ biosynthesis of a cryptic natural product from Aspergillus niger. Org. Biomol. Chem. 7, 435-438. doi: 10.1039/b819208a.
18. Izawa, M., Takekawa, O., Arie, T., Teraoka, T., Yoshida, M., Kimura, M., et al. (2009). Inhibition of histone deacetylase causes reduction of appressorium formation in the rice blast fungus Magnaporthe oryzae. J. Gen. Appl. Microbiol. 55, 489-498. doi: 10.2323/jgam.55.489.
19. Kawauchi, M., and Iwashita, K. (2014). Functional analysis of histone deacetylase and its role in stress response, drug resistance and solid-state cultivation in Aspergillus oryzae. J. Biosci. Bioeng 118, 172-176. doi: 10.1016/j.jbiosc.2014.02.004.
20. Kawauchi, M., Nishiura, M., and Iwashita, K. (2013). Fungus-specific sirtuin HstD coordinates secondary metabolism and development through control of LaeA. Eukaryot. Cell 12, 1087-1096. doi: 10.1128/EC.00003-13.
21. Konig, C. C., Scherlach, K., Schroeckh, V., Horn, F., Nietzsche, S., Brakhage, A. A., et al. (2013). Bacterium induces cryptic meroterpenoid pathway in the pathogenic fungus Aspergillus fumigatus. Chembiochem 14, 938-942. doi: 10.1002/cbic.201300070.
22. Kovacs, J. J., Murphy, P. J., Gaillard, S., Zhao, X., Wu, J. T., Nicchitta, C. V., et al. (2005). HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol. Cell 18, 601-607. doi: 10.1016/j.molcel.2005.04.021.
23. Kurdistani, S. K., and Grunstein, M. (2003). Histone acetylation and deacetylation in yeast. Nat. Rev. Mol. Cell Biol. 4, 276-284. doi: 10.1038/nrm1075.
24. Kwon-Chung, K. J., and Sugui, J. A. (2013). Aspergillus fumigatus-what makes the species a ubiquitous human fungal pathogen? PLoS Pathog. 9:e1003743. doi: 10.1371/journal.ppat.1003743.
25. Lamoth, F., Alexander, B. D., Juvvadi, P. R., and Steinbach, W. J. (2015). Antifungal activity of compounds targeting the Hsp90-calcineurin pathway against various mould species. J. Antimicrob. Chemother. doi: 10.1093/jac/dku549 [Epub ahead of print].
26. Lamoth, F., Juvvadi, P. R., Fortwendel, J. R., and Steinbach, W. J. (2012). Heat shock protein 90 is required for conidiation and cell wall integrity in Aspergillus fumigatus. Eukaryot. Cell 11, 1324-1332. doi: 10.1128/EC.00032-12.
27. Lamoth, F., Juvvadi, P. R., and Steinbach, W. J. (2014a). Heat shock protein 90 (Hsp90): a novel antifungal target against Aspergillus fumigatus. Crit. Rev. Microbiol. doi: 10.3109/1040841X.2014.947239 [Epub ahead of print].
28. Lamoth, F., Juvvadi, P. R., Gehrke, C., Asfaw, Y. G., and Steinbach, W. J. (2014b). Transcriptional activation of heat shock protein 90 mediated via a proximal promoter region as trigger of caspofungin resistance in Aspergillus fumigatus. J. Infect. Dis. 209, 473-481. doi: 10.1093/infdis/jit530.
29. Lamoth, F., Juvvadi, P. R., Soderblom, E. J., Moseley, M. A., Asfaw, Y. G., and Steinbach, W. J. (2014c). Identification of a key lysine residue in heat shock protein 90 required for azole and echinocandin resistance in Aspergillus fumigatus. Antimicrob. Agents Chemother. 58, 1889-1896. doi: 10.1128/AAC.02286-13.
30. Lee, I., Oh, J. H., Shwab, E. K., Dagenais, T. R., Andes, D., and Keller, N. P. (2009). HdaA, a class 2 histone deacetylase of Aspergillus fumigatus, affects germination and secondary metabolite production. Fungal Genet. Biol. 46, 782-790. doi: 10.1016/j.fgb.2009.06.007.
31. Li, Y., Wang, C., Liu, W., Wang, G., Kang, Z., Kistler, H. C., et al. (2011). The HDF1 histone deacetylase gene is important for conidiation, sexual reproduction, and pathogenesis in Fusarium graminearum. Mol. Plant Microbe Interact. 24, 487-496. doi: 10.1094/MPMI-10-10-0233.
32. Mollapour, M., and Neckers, L. (2012). Post-translational modifications of Hsp90 and their contributions to chaperone regulation. Biochim. Biophys. Acta 1823, 648-655. doi: 10.1016/j.bbamcr.2011.07.018.
33. Nimmanapalli, R., Fuino, L., Bali, P., Gasparetto, M., Glozak, M., Tao, J., et al. (2003). Histone deacetylase inhibitor LAQ824 both lowers expression and promotes proteasomal degradation of Bcr-Abl and induces apoptosis of imatinib mesylate-sensitive or-refractory chronic myelogenous leukemia-blast crisis cells. Cancer Res. 63, 5126-5135.
34. Park, J. H., Kim, S. H., Choi, M. C., Lee, J., Oh, D. Y., Im, S. A., et al. (2008). Class II histone deacetylases play pivotal roles in heat shock protein 90-mediated proteasomal degradation of vascular endothelial growth factor receptors. Biochem. Biophys. Res. Commun. 368, 318-322. doi: 10.1016/j.bbrc.2008.01.056.
35. Pfaller, M. A., Messer, S. A., Georgopapadakou, N., Martell, L. A., Besterman, J. M., and Diekema, D. J. (2009). Activity of MGCD290, a Hos2 histone deacetylase inhibitor, in combination with azole antifungals against opportunistic fungal pathogens. J. Clin. Microbiol. 47, 3797-3804. doi: 10.1128/JCM.00618-09.
36. Robbins, N., Leach, M. D., and Cowen, L. E. (2012). Lysine deacetylases Hda1 and Rpd3 regulate Hsp90 function thereby governing fungal drug resistance. Cell Rep. 2, 878-888. doi: 10.1016/j.celrep.2012.08.035.
37. Rundlett, S. E., Carmen, A. A., Kobayashi, R., Bavykin, S., Turner, B. M., and Grunstein, M. (1996). HDA1 and RPD3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription. Proc. Natl. Acad. Sci. U.S.A. 93, 14503-14508. doi: 10.1073/pnas.93.25.14503.
38. Sanderson, L., Taylor, G. W., Aboagye, E. O., Alao, J. P., Latigo, J. R., Coombes, R. C., et al. (2004). Plasma pharmacokinetics and metabolism of the histone deacetylase inhibitor trichostatin a after intraperitoneal administration to mice. Drug Metab. Dispos. 32, 1132-1138. doi: 10.1124/dmd.104.000638.
39. Scroggins, B. T., Robzyk, K., Wang, D., Marcu, M. G., Tsutsumi, S., Beebe, K., et al. (2007). An acetylation site in the middle domain of Hsp90 regulates chaperone function. Mol. Cell 25, 151-159. doi: 10.1016/j.molcel.2006.12.008.
40. Shwab, E. K., Bok, J. W., Tribus, M., Galehr, J., Graessle, S., and Keller, N. P. (2007). Histone deacetylase activity regulates chemical diversity in Aspergillus. Eukaryot. Cell 6, 1656-1664. doi: 10.1128/EC.00186-07.
41. Singh, S. D., Robbins, N., Zaas, A. K., Schell, W. A., Perfect, J. R., and Cowen, L. E. (2009). Hsp90 governs echinocandin resistance in the pathogenic yeast Candida albicans via calcineurin. PLoS Pathog. 5:e1000532. doi: 10.1371/journal.ppat.1000532.
42. Smith, W. L., and Edlind, T. D. (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. doi: 10.1128/AAC.46.11.3532-3539.2002.
43. Strobl, J. S., Cassell, M., Mitchell, S. M., Reilly, C. M., and Lindsay, D. S. (2007). Scriptaid and suberoylanilide hydroxamic acid are histone deacetylase inhibitors with potent anti-Toxoplasma gondii activity in vitro. J. Parasitol. 93, 694-700. doi: 10.1645/GE-1043R.1.
44. Tekaia, F., and Latge, J. P. (2005). Aspergillus fumigatus: saprophyte or pathogen? Curr. Opin. Microbiol. 8, 385-392. doi: 10.1016/j.mib.2005.06.017.
45. Trenholme, K., Marek, L., Duffy, S., Pradel, G., Fisher, G., Hansen, F. K., et al. (2014). Lysine acetylation in sexual stage malaria parasites is a target for antimalarial small molecules. Antimicrob. Agents Chemother. 58, 3666-3678. doi: 10.1128/AAC.02721-13.
46. Tribus, M., Bauer, I., Galehr, J., Rieser, G., Trojer, P., Brosch, G., et al. (2010). A novel motif in fungal class 1 histone deacetylases is essential for growth and development of Aspergillus. Mol. Biol. Cell 21, 345-353. doi: 10.1091/mbc.E09-08-0750.
47. Tribus, M., Galehr, J., Trojer, P., Brosch, G., Loidl, P., Marx, F., et al. (2005). HdaA, a major class 2 histone deacetylase of Aspergillus nidulans, affects growth under conditions of oxidative stress. Eukaryot. Cell 4, 1736-1745. doi: 10.1128/EC.4.10.1736-1745.2005.
48. Trojer, P., Brandtner, E. M., Brosch, G., Loidl, P., Galehr, J., Linzmaier, R., et al. (2003). Histone deacetylases in fungi: novel members, new facts. Nucleic Acids Res. 31, 3971-3981. doi: 10.1093/nar/gkg473.
49. Tsuji, N., Kobayashi, M., Nagashima, K., Wakisaka, Y., and Koizumi, K. (1976). A new antifungal antibiotic, trichostatin. J. Antibiot. (Tokyo) 29, 1-6. doi: 10.7164/antibiotics.29.1.
50. West, A. C., and Johnstone, R. W. (2014). New and emerging HDAC inhibitors for cancer treatment. J. Clin. Invest. 124, 30-39. doi: 10.1172/JCI69738.
51. Wiederhold, N. P. (2007). Attenuation of echinocandin activity at elevated concentrations: a review of the paradoxical effect. Curr. Opin. Infect. Dis. 20, 574-578. doi: 10.1097/QCO.0b013e3282f1be7f.
52. Wierman, M. B., and Smith, J. S. (2014). Yeast sirtuins and the regulation of aging. FEMS Yeast Res. 14, 73-88. doi: 10.1111/1567-1364.12115.
53. Yang, Y., Rao, R., Shen, J., Tang, Y., Fiskus, W., Nechtman, J., et al. (2008). Role of acetylation and extracellular location of heat shock protein 90alpha in tumor cell invasion. Cancer Res. 68, 4833-4842. doi: 10.1158/0008-5472.CAN-08-0644.
54. Yu, X., Guo, Z. S., Marcu, M. G., Neckers, L., Nguyen, D. M., Chen, G. A., et al. (2002). Modulation of p53, ErbB1, ErbB2, and Raf-1 expression in lung cancer cells by depsipeptide FR901228. J. Natl. Cancer Inst. 94, 504-513. doi: 10.1093/jnci/94.7.504.
55. Zhou, Q., Agoston, A. T., Atadja, P., Nelson, W. G., and Davidson, N. E. (2008). Inhibition of histone deacetylases promotes ubiquitin-dependent proteasomal degradation of DNA methyltransferase 1 in human breast cancer cells. Mol. Cancer Res. 6, 873-883. doi: 10.1158/1541-7786.MCR-07-0330.