Identification and evaluation of improved 4=-O-(Alkyl) 4,5- disubstituted 2-Deoxystreptamines as next-generation aminoglycoside antibiotics

mBio

Volumn 5, Issue 5, 2014, Pages

  Duscha, Stefan ^a   Boukari, Heithem ^a   Shcherbakov, Dimitri ^a   Salian, Sumantha ^b   Silva, Sandrina ^b   Kendall, Ann ^c   Kato, Takayuki ^d   Akbergenov, Rashid ^a   Perez Fernandez, Deborah ^b   Bernet, Bruno ^b   Vaddi, Swapna ^e   Thommes, Pia ^e   Schacht, Jochen ^c   Crich, David ^d   Vasella, Andrea ^b   Böttger, Erik C ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^d WAYNE STATE UNIVERSITY   (United States)

^e Euprotec Limited   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2 DEOXYSTREPTAMINE DERIVATIVE; 4' DEOXY PAROMOMYCIN; 4' O (3 PHENYLPROPYL); 4' O (3 PHENYLPROPYL)PAROMOMYCIN; 4',6' O (3 PHENYLPROPYLIDENE)PAROMOMYCIN; AMINOALCOHOL; AMINOGLYCOSIDE ANTIBIOTIC AGENT; CYCLOPHOSPHAMIDE; GENTAMICIN; PAROMOMYCIN; UNCLASSIFIED DRUG; 2-DEOXYSTREPTAMINE; AMINOGLYCOSIDE; ANTIINFECTIVE AGENT; HEXOSAMINE; RNA 16S;

ALKYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ARTICLE; BIOCOMPATIBILITY; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DRUG ACTIVITY; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG POTENCY; DRUG RESEARCH; DRUG STRUCTURE; DRUG SYNTHESIS; EMBRYO; ESCHERICHIA COLI; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INFECTION; MALE; MAMMAL CELL; MINIMUM INHIBITORY CONCENTRATION; MOUSE; MYCOBACTERIUM SMEGMATIS; NEUTROPENIA; NONHUMAN; OTOTOXICITY; RNA TRANSLATION; SEPTICEMIA; STAPHYLOCOCCUS AUREUS; 3T3 CELL LINE; ANIMAL; BACTERIAL INFECTIONS; DRUG EFFECTS; GENETICS; GUINEA PIG; INSTITUTE FOR CANCER RESEARCH MOUSE; MICROBIAL SENSITIVITY TEST; PHYLOGENY; RIBOSOME; SYNTHESIS;

AMINOGLYCOSIDES; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL INFECTIONS; ESCHERICHIA COLI; GUINEA PIGS; HEXOSAMINES; MALE; MICE; MICE, INBRED ICR; MICROBIAL SENSITIVITY TESTS; NIH 3T3 CELLS; PHYLOGENY; RIBOSOMES; RNA, RIBOSOMAL, 16S; STAPHYLOCOCCUS AUREUS;

EID: 84908429123     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01827-14     Document Type: Article

References (45)

1. French GL. 2010. The continuing crisis in antibiotic resistance. Int. J. Antimicrob. Agents 36(Suppl 3):S3-S7. http://dx.doi.org/10.1016/S0924 -8579(10)70003-0.
2. Payne DJ, Gwynn MN, Holmes DJ, Pompliano DL. 2007. Drugs for bad bugs: confronting the challenges of antibacterial discovery. Nat. Rev. Drug Discov. 6:29-40. http://dx.doi.org/10.1038/nrd2201.
3. Wright GD, Sutherland AD. 2007. New strategies for combating multidrug-resistant bacteria. Trends Mol. Med. 13:260 -267. http:// dx.doi.org/10.1016/j.molmed.2007.04.004.
4. Fischbach MA, Walsh CT. 2009. Antibiotics for emerging pathogens. Science 325:1089-1093. http://dx.doi.org/10.1126/science.1176667.
5. Newman DJ, Cragg GM. 2007. Natural products as sources of new drugs over the last 25 years. J. Nat. Prod. 70:461-477. http://dx.doi.org/10.1021/ np068054v.
6. World Health Organization. 2007. Critically important antimicrobials for human medicine. Categorization for the development of risk management strategies to contain antimicrobial resistance due to non-human antimicrobial use. Report of the SecondWHOExpert Meeting, Copenhagen, 29 to 31 May 2007. World Health Organization, Geneva, Switzerland. http://www.who.int/foodborne_disease/resistance/antimicrobials _human.pdf.
7. Chambers HF. 1996. Chemotherapy of microbial diseases, p 1103-1121. In Hardman JG, Limbird LE (ed), Goodmann&Gilman's the pharmaceutical basis of therapeutics, 10th ed. The McGraw-Hill Companies, New York, NY.
8. Hanberger H, Edlund C, Furebring M, Giske CG, Melhus A, Nilsson LE, Petersson J, Sjölin J, Ternhag A, Werner M, Eliasson E, Swedish Reference Group for Antibiotics (SRGA). 2013. Rational use of aminoglycosides- review and recommendations by the Swedish Reference Group for Antibiotics (SRGA). Scand. J. Infect. Dis. 45:161-175. http:// dx.doi.org/10.3109/00365548.2012.747694.
9. Davies J, Gorini L, Davis BD. 1965. Misreading of RNA codewords induced by aminoglycoside antibiotics. Mol. Pharmacol. 1:93-106.
10. Cabañas MJ, Vázquez D, Modolell J. 1978. Inhibition of ribosomal translocation by aminoglycoside antibiotics. Biochem. Biophys. Res. Commun. 83:991-997. http://dx.doi.org/10.1016/0006-291X(78)91493 -6.
11. Peske F, Savelsbergh A, Katunin VI, Rodnina MV, Wintermeyer W. 2004. Conformational changes of the small ribosomal subunit during elongation factor G-dependent tRNA-mRNA translocation. J. Mol. Biol. 343:1183-1194. http://dx.doi.org/10.1016/j.jmb.2004.08.097.
12. Feldman MB, Terry DS, Altman RB, Blanchard SC. 2010. Aminoglycoside activity observed on single pre-translocation ribosome complexes. Nat. Chem. Biol. 6:244. http://dx.doi.org/10.1038/nchembio0310-244a.
13. Carter AP, Clemons WM, Brodersen DE, Morgan-Warren RJ, Wimberly BT, Ramakrishnan V. 2000. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407:340-348. http://dx.doi.org/10.1038/35030019.
14. François B, Russell RJ, Murray JB, Aboul-ela F, Masquida B, Vicens Q, Westhof E. 2005. Crystal structures of complexes between aminoglycosides and decoding A site oligonucleotides: role of the number of rings and positive charges in the specific binding leading to miscoding. Nucleic Acids Res. 33:5677-5690. http://dx.doi.org/10.1093/nar/gki862.
15. Pfister P, Hobbie S, Vicens Q, Böttger EC, Westhof E. 2003. The molecular basis for A-site mutations conferring aminoglycoside resistance: relationship between ribosomal susceptibility and X-ray crystal structures. Chembiochem 4:1078 -1088. http://dx.doi.org/10.1002/ cbic.200300657.
16. Pfister P, Hobbie S, Brull C, Corti N, Vasella A, Westhof E, Böttger EC. 2005. Mutagenesis of 16S rRNA C1409-G1491 base-pair differentiates between 6'OH and 6'NH3+ aminoglycosides. J. Mol. Biol. 346:467-475. http://dx.doi.org/10.1016/j.jmb.2004.11.073.
17. Hobbie SN, Pfister P, Brüll C, Westhof E, Böttger EC. 2005. Analysis of the contribution of individual substituents in 4,6-aminoglycosideribosome interaction. Antimicrob. Agents Chemother. 49:5112-5118. http://dx.doi.org/10.1128/AAC.49.12.5112-5118.2005.
18. Hobbie SN, Pfister P, Bruell C, Sander P, François B, Westhof E, Böttger EC. 2006. Binding of neomycin-class aminoglycoside antibiotics to mutant ribosomes with alterations in the A site of 16S rRNA. Antimicrob. Agents Chemother. 50:1489 -1496. http://dx.doi.org/10.1128/ AAC.50.4.1489-1496.2006.
19. Recht MI, Douthwaite S, Puglisi JD. 1999. Basis for prokaryotic specificity of action of aminoglycoside antibiotics. EMBO J. 18:3133-3138. http://dx.doi.org/10.1093/emboj/18.11.3133.
20. Böttger EC, Springer B, Prammananan T, Kidan Y, Sander P. 2001. Structural basis for selectivity and toxicity of ribosomal antibiotics.EMBO Rep. 2:318-323. http://dx.doi.org/10.1093/embo-reports/kve062.
21. Hobbie SN, Kalapala SK, Akshay S, Bruell C, Schmidt S, Dabow S, Vasella A, Sander P, Böttger EC. 2007. Engineering the rRNA decoding site of eukaryotic cytosolic ribosomes in bacteria. Nucleic Acids Res. 35: 6086-6093. http://dx.doi.org/10.1093/nar/gkm658.
22. Fan-Minogue H, Bedwell DM. 2008. Eukaryotic ribosomal RNA determinants of aminoglycoside resistance and their role in translational fidelity. RNA 14:148-157. http://dx.doi.org/10.1261/rna.805208.
23. Matt T, Akbergenov R, Shcherbakov D, Böttger EC. 2010. The ribosomal A-site: decoding, drug target, and disease. Isr. J. Chem. 50:60-70. http://dx.doi.org/10.1002/ijch.201000003.
24. Forge A, Schacht J. 2000. Aminoglycoside antibiotics. Audiol. Neurootol. 5:3-22. http://dx.doi.org/10.1159/000013861.
25. Duggal P, Sarkar M. 2007. Audiologic monitoring of multi-drug resistant tuberculosis patients on aminoglycoside treatment with long term followup. BMC Ear Nose Throat Disord. 7:5. http://dx.doi.org/10.1186/1472 -6815-7-5.
26. Prezant TR, Agapian JV, Bohlman MC, Bu X, Oztas S, Qiu WQ, Arnos KS, Cortopassi GA, Jaber L, Rotter JI, Shohat M, Fischel-Ghodsian N. 1993. Mitochondrial ribosomal RNA mutation associated with both antibiotic-induced and non-syndromic deafness. Nat. Genet. 4:289-294. http://dx.doi.org/10.1038/ng0793-289.
27. Zhao H, Li R, Wang Q, Yan Q, Deng JH, Han D, Bai Y, Young WY, Guan MX. 2004. Maternally inherited aminoglycoside-induced and non- syndromic deafness is associated with the novel C1494T mutation in the mitochondrial 12S rRNA gene in a large Chinese family. Am. J. Hum. Genet. 74:139-152. http://dx.doi.org/10.1086/381133.
28. Hobbie SN, Bruell CM, Akshay S, Kalapala SK, Shcherbakov D, Böttger EC. 2008. Mitochondrial deafness alleles confer misreading of the genetic code. Proc. Natl. Acad. Sci. U. S. A. 105:3244-3249. http://dx.doi.org/ 10.1073/pnas.0707265105.
29. Hobbie SN, Akshay S, Kalapala SK, Bruell CM, Shcherbakov D, Böttger EC. 2008. Genetic analysis of interactions with eukaryotic rRNA identify the mitoribosome as target in aminoglycoside ototoxicity. Proc. Natl. Acad. Sci. U. S. A. 105:20888 -20893. http://dx.doi.org/10.1073/ pnas.0811258106.
30. Matt T, Ng CL, Lang K, Sha SH, Akbergenov R, Shcherbakov D, Meyer M, Duscha S, Xie J, Dubbaka SR, Perez-Fernandez D, Vasella A, Ramakrishnan V, Schacht J, Böttger EC. 2012. Dissociation of antibacterial activity and aminoglycoside ototoxicity in the 4-monosubstituted 2-deoxystreptamine apramycin. Proc. Natl. Acad. Sci. U. S. A. 109: 10984-10989. http://dx.doi.org/10.1073/pnas.1204073109.
31. Shulman E, Belakhov V, Wei G, Kendall A, Meyron-Holtz EG, Ben- Shachar D, Schacht J, Baasov T. 2014. Designer aminoglycosides that selectively inhibit cytoplasmic rather than mitochondrial ribosomes show decreased ototoxicity: a strategy for the treatment of genetic diseases. J. Biol. Chem. 289:2318-2330. http://dx.doi.org/10.1074/jbc.M113.533588.
32. Aggen JB, Armstrong ES, Goldblum AA, Dozzo P, Linsell MS, Gliedt MJ, Hildebrandt DJ, Feeney LA, Kubo A, Matias RD, Lopez S, Gomez M, Wlasichuk KB, Diokno R, Miller GH, Moser HE. 2010. Synthesis and spectrum of the neoglycoside ACHN-490. Antimicrob. Agents Chemother. 54:4636-4642. http://dx.doi.org/10.1128/AAC.00572-10.
33. Zhao F, Zhao Q, Blount KF, Han Q, Tor Y, Hermann T. 2005. Molecular recognition of RNA by neomycin and a restricted neomycin derivative. Angew. Chem. Int. Ed. Engl. 44:5329-5334. http://dx.doi.org/ 10.1002/anie.200500903.
34. Hanessian S, Giguere A, Grzyb J, Maianti JP, Saavedra OM, Aggen JB, Linsell MS, Goldblum AA, Hildebrandt DJ, Kane TR, Dozzo P, Gliedt MJ, Matias RD, Feeney LA, Armstrong ES. 2011. Toward overcoming Staphylococcus aureus aminoglycoside resistance mechanisms with a functionally designed neomycin analogue. ACS Med. Chem. Lett. 2:924-928. http://dx.doi.org/10.1021/ml200202y.
35. Vakulenko SB, Mobashery S. 2003. Versatility of aminoglycosides and prospects for their future. Clin. Microbiol. Rev. 16:430 - 450. http:// dx.doi.org/10.1128/CMR.16.3.430-450.2003.
36. Magnet S, Blanchard JS. 2005. Molecular insights into aminoglycoside action and resistance. Chem. Rev. 105:477- 498. http://dx.doi.org/ 10.1021/cr0301088.
37. Houghton JL, Green KD, Chen W, Garneau-Tsodikova S. 2010. The future of aminoglycosides: the end or renaissance? Chembiochem 11: 880-902. http://dx.doi.org/10.1002/cbic.200900779.
38. Francis SP, Katz J, Fanning KD, Harris KA, Nicholas BD, Lacy M, Pagana J, Agris PF, Shin JB. 2013. A novel role of cytosolic protein synthesis inhibition in aminoglycoside ototoxicity. J. Neurosci. 33: 3079-3093. http://dx.doi.org/10.1523/JNEUROSCI.3430-12.2013.
39. Perez-Fernandez D, Shcherbakov D, Matt T, Leong NC, Kudyba I, Duscha S, Boukari H, Patak R, Dubbaka SR, Lang K, Meyer M, Akbergenov R, Freihofer P, Vaddi S, Thommes P, Ramakrishnan V, Vasella A, Böttger EC. 2014. 4'-O-substitutions determine selectivity of aminoglycoside antibiotics. Nat. Commun. 5:3112. http://dx.doi.org/ 10.1038/ncomms4112.
40. Pathak R, Perez-Fernandez D, Nandurdikar R, Kalapala SK, Böttger EC, Vasella A. 2008. Synthesis and evaluation of paromomycin derivatives modified at C(4'). Helv. Chim. Acta 91:1533-1552. http://dx.doi.org/ 10.1002/hlca.200890167.
41. Kandasamy J, Atia-Glikin D, Shulman E, Shapira K, Shavit M, Belakhov V, Baasov T. 2012. Increased selectivity toward cytoplasmic versus mitochondrial ribosome confers improved efficiency of synthetic aminoglycosides in fixing damaged genes: a strategy for treatment of genetic diseases caused by nonsense mutations. J. Med. Chem. 55:10630-10643. http:// dx.doi.org/10.1021/jm3012992.
42. Bowes J, Brown AJ, Hamon J, Jarolimek W, Sridhar A, Waldron G, Whitebread S. 2012. Reducing safety-related drug attrition: the use of in vitro pharmacological profiling. Nat. Rev. Drug Discov. 11:909 -922. http://dx.doi.org/10.1038/nrd3845.
43. Sucheck SJ, Wong AL, Koeller KM, Boehr DD, Draker K, Sears P, Wright GD, Wong CH. 2000. Design of bifunctional antibiotics that target bacterial rRNA and inhibit resistance-causing enzymes. J. Am. Chem. Soc. 122:5230-5231. http://dx.doi.org/10.1021/ja000575w.
44. Bastida A, Hidalgo A, Chiara JL, Torrado M, Corzana F, Pérez- Cañadillas JM, Groves P, Garcia-Junceda E, Gonzalez C, Jimenez- Barbero J, Asensio JL. 2006. Exploring the use of conformationally locked aminoglycosides as a new strategy to overcome bacterial resistance. J. Am. Chem. Soc. 128:100-116. http://dx.doi.org/10.1021/ja0543144.
45. Wright GD, Berghuis AM, Mobashery S. 1998. Aminoglycoside antibiotics- structure, function and resistance, p 27-69. In Rosen B, Mobashery S (ed), Resolving the antibiotic paradox. Springer Verlag, New York, NY.