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Original Articles

Cisplatin protects mice from challenge of Cryptococcus neoformans by targeting the Prp8 intein

ORCID Icon, , , , , , , , & ORCID Icon show all
Pages 895-908 | Received 04 Feb 2019, Accepted 16 May 2019, Published online: 21 Jun 2019

References

  • Perfect JR. Fungal diagnosis: how do we do it and can we do better? Curr Med Res Opin. 2013;29(Suppl 4):3–11. doi: 10.1185/03007995.2012.761134
  • Brown GD, Denning DW, Gow NAR, et al. Hidden killers: human fungal infections. Sci Transl Med. 2012;4:165rv113. doi: 10.1126/scitranslmed.3004404
  • Gullo A. Invasive fungal infections: the challenge continues. Drugs. 2009;69(Suppl 1):65–73. doi: 10.2165/11315530-000000000-00000
  • Tuite NL, Lacey K. Overview of invasive fungal infections. Methods Mol Biol. 2013;968:1–23. doi: 10.1007/978-1-62703-257-5_1
  • Perfect JR, Bicanic T. Cryptococcosis diagnosis and treatment: What do we know now. Fungal Genet Biol. 2015;78:49–54. doi: 10.1016/j.fgb.2014.10.003
  • Chen Y, Toffaletti DL, Tenor JL, et al. The Cryptococcus neoformans transcriptome at the site of human meningitis. MBio. 2014;5:e01087-13. doi: 10.1128/mBio.01087-13
  • Brouwer AE, Rajanuwong A, Chierakul W, et al. Combination antifungal therapies for HIV-associated cryptococcal meningitis: a randomised trial. Lancet. 2004;363:1764–1767. doi: 10.1016/S0140-6736(04)16301-0
  • Husain S, Wagener MM, Singh N. Cryptococcus neoformans infection in organ transplant recipients: variables influencing clinical characteristics and outcome. Emerg Infect Dis. 2001;7:375–381. doi: 10.3201/eid0703.017302
  • MacDougall L, Kidd SE, Galanis E, et al. Spread of Cryptococcus gattii in British Columbia, Canada, and detection in the Pacific Northwest, USA. Emerg Infect Dis. 2007;13:42–50. doi: 10.3201/eid1301.060827
  • Byrnes EJ, Li W, Ren P, et al. A diverse population of Cryptococcus gattii molecular type VGIII in southern Californian HIV/AIDS patients. PLoS Pathog. 2011;7:e1002205. doi: 10.1371/journal.ppat.1002205
  • Byrnes EJ, Li W, Lewit Y, et al. Emergence and pathogenicity of highly virulent Cryptococcus gattii genotypes in the northwest United States. PLoS Pathog. 2010;6:e1000850. doi: 10.1371/journal.ppat.1000850
  • Denning DW, Pleuvry A, Cole DC. Global burden of chronic pulmonary aspergillosis complicating sarcoidosis. Eur Respir J. 2013;41:621–626. doi: 10.1183/09031936.00226911
  • Saag MS, Graybill RJ, Larsen RA, et al. Practice guidelines for the management of cryptococcal disease. Infectious Diseases Society of America. Clin Infect Dis. 2000;30:710–718. doi: 10.1086/313757
  • Walsh TJ, Anaissie EJ, Denning D, et al. Treatment of aspergillosis: clinical practice guidelines of the Infectious Diseases Society of America. Clin Infect Dis. 2008;46:327–360. doi: 10.1086/525258
  • Pfaller MA. Antifungal drug resistance: mechanisms, epidemiology, and consequences for treatment. Am J Med. 2012;125:S3–S13. doi: 10.1016/j.amjmed.2011.11.001
  • Ghannoum MA, Rice LB. Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin Microbiol Rev. 1999;12:501–517. doi: 10.1128/CMR.12.4.501
  • Howard SJ, Cerar D, Anderson MJ, et al. Frequency and evolution of Azole resistance in Aspergillus fumigatus associated with treatment failure. Emerg Infect Dis. 2009;15:1068–1076. doi: 10.3201/eid1507.090043
  • Mills KV, Johnson MA, Perler FB. Protein splicing: how inteins escape from precursor proteins. J Biol Chem. 2014;289:14498–14505. doi: 10.1074/jbc.R113.540310
  • Aranko AS, Wlodawer A, Iwai H. Nature's recipe for splitting inteins. Protein Eng Des Sel. 2014;27:263–271. doi: 10.1093/protein/gzu028
  • Eryilmaz E, Shah NH, Muir TW, et al. Structural and dynamical features of inteins and implications on protein splicing. J Biol Chem. 2014;289:14506–14511. doi: 10.1074/jbc.R113.540302
  • Novikova O, Topilina N, Belfort M. Enigmatic distribution, evolution, and function of inteins. J Biol Chem. 2014;289:14490–14497. doi: 10.1074/jbc.R114.548255
  • Paulus H. Inteins as targets for potential antimycobacterial drugs. Front Biosci. 2003;8:s1157–s1165. doi: 10.2741/1195
  • Paulus H. Protein splicing inhibitors as a new class of antimycobacterial agents. Drugs Future. 2007;32:973–984. doi: 10.1358/dof.2007.032.11.1140690
  • Zhang L, Zheng Y, Callahan B, et al. Cisplatin inhibits protein splicing, suggesting inteins as therapeutic targets in mycobacteria. J Biol Chem. 2011;286:1277–1282. doi: 10.1074/jbc.M110.171124
  • Chan H, Pearson CS, Green CM, et al. Exploring intein inhibition by platinum compounds as an antimicrobial strategy. J Biol Chem. 2016;291:22661–22670. doi: 10.1074/jbc.M116.747824
  • Butler MI, Goodwin TJ, Poulter RT. A nuclear-encoded intein in the fungal pathogen Cryptococcus neoformans. Yeast. 2001;18:1365–1370. doi: 10.1002/yea.781
  • Butler MI, Poulter RT. The PRP8 inteins in Cryptococcus are a source of phylogenetic and epidemiological information. Fungal Genet Biol. 2005;42:452–463. doi: 10.1016/j.fgb.2005.01.011
  • Liu XQ, Yang J. Prp8 intein in fungal pathogens: target for potential antifungal drugs. FEBS Lett. 2004;572:46–50. doi: 10.1016/j.febslet.2004.07.016
  • Pearl EJ, Tyndall JD, Poulter RT, et al. Sequence requirements for splicing by the Cne PRP8 intein. FEBS Lett. 2007;581:3000–3004. doi: 10.1016/j.febslet.2007.05.060
  • Hang J, Wan R, Yan C, et al. Structural basis of pre-mRNA splicing. Science. 2015;349:1191–1198. doi: 10.1126/science.aac8159
  • Yan C, Hang J, Wan R, et al. Structure of a yeast spliceosome at 3.6-angstrom resolution. Science. 2015;349:1182–1191. doi: 10.1126/science.aac7629
  • Brecher M, Li Z, Liu B, et al. A conformational switch high-throughput screening assay and allosteric inhibition of the flavivirus NS2B-NS3 protease. PLoS Pathog. 2017;13:e1006411. doi: 10.1371/journal.ppat.1006411
  • Li Z, Brecher M, Deng Y-Q, et al. Existing drugs as broad-spectrum and potent inhibitors for Zika virus by targeting NS2B-NS3 interaction. Cell Res. 2017;27:1046–1064. doi: 10.1038/cr.2017.88
  • Higuchi R, Krummel B, Saiki RK. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res. 1988;16:7351–7367. doi: 10.1093/nar/16.15.7351
  • Hiraga K, Derbyshire V, Dansereau JT, et al. Minimization and stabilization of the Mycobacterium tuberculosis recA intein. J Mol Biol. 2005;354:916–926. doi: 10.1016/j.jmb.2005.09.088
  • Kelley DS, Lennon CW, Li Z, et al. Mycobacterial DnaB helicase intein as oxidative stress sensor. Nat Commun. 2018;9:4363. doi: 10.1038/s41467-018-06554-x
  • Zhao Y, Li Z, Drozd SJ, et al. Crystal structure of mycoplasma arthritidis mitogen complexed with HLA-DR1 reveals a novel superantigen fold and a dimerized superantigen-MHC complex. Structure. 2004;12:277–288.
  • Topilina NI, Green CM, Jayachandran P, et al. Sufb intein of Mycobacterium tuberculosis as a sensor for oxidative and nitrosative stresses. Proc Natl Acad Sci U S A. 2015;112:10348–10353. doi: 10.1073/pnas.1512777112
  • Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 1997;276:307–326. doi: 10.1016/S0076-6879(97)76066-X
  • Adams PD, Afonine PV, Bunkóczi G, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr. 2010;66:213–221. doi: 10.1107/S0907444909052925
  • Emsley P, Lohkamp B, Scott WG, et al. Features and development of Coot. Acta Crystallogr D Biol Crystallogr. 2010;66:486–501. doi: 10.1107/S0907444910007493
  • Klepser ME, Ernst EJ, Ernst ME, et al. Evaluation of endpoints for antifungal susceptibility determinations with LY303366. Antimicrob Agents Chemother. 1998;42:1387–1391. doi: 10.1128/AAC.42.6.1387
  • Moussa NM, Ghannoum MA, Whittaker PA, et al. Effects of cisplatin and two novel palladium complexes on Candida albicans. Microbios. 1990;62:165–178.
  • Paulmurugan R, Gambhir SS. Monitoring protein-protein interactions using split synthetic renilla luciferase protein-fragment-assisted complementation. Anal Chem. 2003;75:1584–1589. doi: 10.1021/ac020731c
  • Chong S, Xu MQ. Protein splicing of the Saccharomyces cerevisiae VMA intein without the endonuclease motifs. J Biol Chem. 1997;272:15587–15590. doi: 10.1074/jbc.272.25.15587
  • Derbyshire V, Wood DW, Wu W, et al. Genetic definition of a protein-splicing domain: functional mini-inteins support structure predictions and a model for intein evolution. Proc Natl Acad Sci U S A. 1997;94:11466–11471. doi: 10.1073/pnas.94.21.11466
  • Azad T, Tashakor A, Hosseinkhani S. Split-luciferase complementary assay: applications, recent developments, and future perspectives. Anal Bioanal Chem. 2014;406:5541–5560. doi: 10.1007/s00216-014-7980-8
  • Jiang Y, Bernard D, Yu Y, et al. Split Renilla luciferase protein fragment-assisted complementation (SRL-PFAC) to characterize Hsp90-Cdc37 complex and identify critical residues in protein/protein interactions. J Biol Chem. 2010;285:21023–21036. doi: 10.1074/jbc.M110.103390
  • Gangopadhyay JP, Jiang SQ, Paulus H. An in vitro screening system for protein splicing inhibitors based on green fluorescent protein as an indicator. Anal Chem. 2003;75:2456–2462. doi: 10.1021/ac020756b
  • Iversen PW, Beck B, Chen YF, et al. HTS Assay Validation. doi:NBK83783 [bookaccession] (2004).
  • Van Roey P, Pereira B, Li Z, et al. Crystallographic and mutational studies of Mycobacterium tuberculosis recA mini-inteins suggest a pivotal role for a highly conserved aspartate residue. J Mol Biol. 2007;367:162–173. doi: 10.1016/j.jmb.2006.12.050
  • Ding Y, Xu M-Q, Ghosh I, et al. Crystal structure of a mini-intein reveals a conserved catalytic module involved in side chain cyclization of asparagine during protein splicing. J Biol Chem. 2003;278:39133–39142. doi: 10.1074/jbc.M306197200
  • Werner E, Wende W, Pingoud A, et al. High resolution crystal structure of domain I of the Saccharomyces cerevisiae homing endonuclease PI-SceI. Nucleic Acids Res. 2002;30:3962–3971. doi: 10.1093/nar/gkf523
  • Zhao Y, Upadhyay S, Lin X. PAS domain protein Pas3 interacts with the chromatin modifier Bre1 in regulating cryptococcal morphogenesis. MBio. 2018;9:e02135-18. doi: 10.1128/mBio.02135-18
  • Perfect JR, Dismukes W, Dromer F, et al. Clinical practice guidelines for the management of cryptococcal disease: 2010 update by the infectious diseases society of america. Clin Infect Dis. 2010;50:291–322. doi: 10.1086/649858
  • Rajasingham R, Rolfes MA, Birkenkamp KE, et al. Cryptococcal meningitis treatment strategies in resource-limited settings: a cost-effectiveness analysis. PLoS Med. 2012;9:e1001316. doi: 10.1371/journal.pmed.1001316
  • Kontoyiannis DP, Lionakis M, Lewis R, et al. Zygomycosis in a tertiary-care cancer center in the era of Aspergillus-active antifungal therapy: a case-control observational study of 27 recent cases. J Infect Dis. 2005;191:1350–1360. doi: 10.1086/428780
  • Denning DW, Park S, Lass-Florl C, et al. High-frequency triazole resistance found In nonculturable Aspergillus fumigatus from lungs of patients with chronic fungal disease. Clin Infect Dis. 2011;52:1123–1129. doi: 10.1093/cid/cir179
  • Zuger A, Louie E, Holzman RS, et al. Cryptococcal disease in patients with the acquired immunodeficiency syndrome. Diagnostic features and outcome of treatment. Ann Intern Med. 1986;104:234–240. doi: 10.7326/0003-4819-104-2-234
  • Sipsas NV, Kontoyiannis DP. Clinical issues regarding relapsing aspergillosis and the efficacy of secondary antifungal prophylaxis in patients with hematological malignancies. Clin Infect Dis. 2006;42:1584–1591. doi: 10.1086/503844
  • Boelaert JR, Goddeeris KH, Vanopdenbosch LJ, et al. Relapsing meningitis caused by persistent cryptococcal antigens and immune reconstitution after the initiation of highly active antiretroviral therapy. AIDS. 2004;18:1223–1224. doi: 10.1097/00002030-200405210-00023
  • Gubbins PO, McConnell SA, Penzak SR. Drug interactions in infectious Diseases. New York: Humana Press; 2001.
  • Moen MD, Lyseng-Williamson KA, Scott LJ. Liposomal amphotericin B: a review of its use as empirical therapy in febrile neutropenia and in the treatment of invasive fungal infections. Drugs. 2009;69:361–392. doi: 10.2165/00003495-200969030-00010
  • Kauffman CA. Fungal infections. Proc Am Thorac Soc. 2006;3:35–40. doi: 10.1513/pats.200510-110JH
  • Green CM, Novikova O, Belfort M. The dynamic intein landscape of eukaryotes. Mob DNA. 2018;9(4):1–16.
  • Fernandes JA, Prandini THR, Castro MA, et al. Evolution and application of inteins in Candida species: a review. Front Microbiol. 2016;7:1585. doi: 10.3389/fmicb.2016.01585
  • Lennon CW, Stanger M, Belfort M. Protein splicing of a recombinase intein induced by ssDNA and DNA damage. Genes Dev. 2016;30:2663–2668. doi: 10.1101/gad.289280.116
  • Kuhn AN, Reichl EM, Brow DA. Distinct domains of splicing factor Prp8 mediate different aspects of spliceosome activation. Proc Natl Acad Sci U S A. 2002;99:9145–9149. doi: 10.1073/pnas.102304299
  • Green CM, Li Z, Novikova O, et al. Spliceosomal Prp8 intein at the crossroads of protein and RNA splicing. Under review (2019). doi:10.1101/502781
  • Pearl EJ, Bokor AA, Butler MI, et al. Preceding hydrophobic and beta-branched amino acids attenuate splicing by the CnePRP8 intein. Biochim Biophys Acta. 2007;1774:995–1001. doi: 10.1016/j.bbapap.2007.05.015
  • Grainger RJ, Beggs JD. Prp8 protein: at the heart of the spliceosome. RNA. 2005;11:533–557. doi: 10.1261/rna.2220705
  • Dasari S, Tchounwou PB. Cisplatin in cancer therapy: molecular mechanisms of action. Eur J Pharmacol. 2014;740:364–378. doi: 10.1016/j.ejphar.2014.07.025
  • Kelland L. The resurgence of platinum-based cancer chemotherapy. Nat Rev Cancer. 2007;7:573–584. doi: 10.1038/nrc2167