Dissociation of antibacterial activity and aminoglycoside ototoxicity in the 4-monosubstituted 2-deoxystreptamine apramycin

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 27, 2012, Pages 10984-10989

  Matt, Tanja ^a   Ng, Chyan Leong ^b,e   Lang, Kathrin ^b   Sha, Su Hua ^c,f   Akbergenov, Rashid ^a   Shcherbakov, Dmitri ^a   Meyer, Martin ^a   Duscha, Stefan ^a   Xie, Jing ^c,g   Dubbaka, Srinivas R ^d   Perez Fernandez, Déborah ^d   Vasella, Andrea ^d   Ramakrishnan, V ^b   Schacht, Jochen ^c   Böttger, Erik C ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^d ETH ZURICH   (Switzerland)

^e UNIVERSITI KEBANGSAAN MALAYSIA   (Malaysia)

^f MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^g CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

Antibiotic; Deafness; Misreading; Mycobacteria; Translation

Indexed keywords

APRAMYCIN; GENTAMICIN; KANAMYCIN; NEOMYCIN; TOBRAMYCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBACTERIAL ACTIVITY; ANTIBIOTIC SENSITIVITY; ARTICLE; CELL DAMAGE; CELL LOSS; COCHLEA; CONCENTRATION RESPONSE; CONCEPTUAL FRAMEWORK; DRUG BINDING SITE; EX VIVO STUDY; EXPERIMENTAL GUINEA PIG; HAIR CELL; HEARING LOSS; IC 50; IN VIVO STUDY; MINIMUM INHIBITORY CONCENTRATION; MITOCHONDRIAL RIBOSOME; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OTOTOXICITY; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RIBOSOME; SYNTHESIS; THERMUS THERMOPHILUS; X RAY CRYSTALLOGRAPHY;

AMINOGLYCOSIDES; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; BACTERIAL INFECTIONS; BINDING SITES; DEAFNESS; DRUG DESIGN; GENTAMICINS; GUINEA PIGS; HAIR CELLS, AUDITORY; HEK293 CELLS; HUMANS; MICE; MITOCHONDRIA; MUTAGENESIS; MYCOBACTERIUM; NEBRAMYCIN; ORGAN CULTURE TECHNIQUES; PROTEIN BIOSYNTHESIS; PSEUDOMONAS AERUGINOSA; RABBITS; RETICULOCYTES; RIBOSOMES; STAPHYLOCOCCUS AUREUS;

CAVIA; CORYNEBACTERINEAE; EUKARYOTA; MYCOBACTERIUM TUBERCULOSIS;

EID: 84863599921     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1204073109     Document Type: Article

References (47)

1. Gale EF, Cundliffe E, Reynolds PE, Richmond MH, Waring MJ (1981) The Molecular Basis of Antibiotic Action (London, John Wiley and Sons) 2nd Ed.
2. Chambers HF (1996) Chemotherapy of microbial diseases. Goodman and Gilman's The Pharmaceutical Basis of Therapeutics (McGraw-Hill, New York), 10th Ed.
3. Moazed D, Noller HF (1987) Interaction of antibiotics with functional sites in 16S ribosomal RNA. Nature 327:389-394. (Pubitemid 17075811)
4. Davies JL, Gorini L, Davis BD (1965) Misreading of RNA codewords induced by aminoglycoside antibiotics. Mol Pharmacol 1:93-106.
5. Benveniste R, Davies J (1973) Structure-activity relationships among the aminoglycoside antibiotics: Role of hydroxyl and amino groups. Antimicrob Agents Chemother 4:402-409.
6. Cabañas MJ, Vázquez D, Modolell J (1978) Inhibition of ribosomal translocation by aminoglycoside antibiotics. Biochem Biophys Res Commun 83:991-997. (Pubitemid 9004489)
7. Pape T, Wintermeyer W, Rodnina MV (2000) Conformational switch in the decoding region of 16S rRNA during aminoacyl-tRNA selection on the ribosome. Nat Struct Biol 7:104-107. (Pubitemid 30082505)
8. 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. (Pubitemid 39387819)
9. Feldman MB, Terry DS, Altman RB, Blanchard SC (2010) Aminoglycoside activity observed on single pre-translocation ribosome complexes. Nat Chem Biol 6:54-62.
10. Carter AP, et al. (2000) Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407:340-348.
11. Vicens Q, Westhof E (2001) Crystal structure of paromomycin docked into the eubacterial ribosomal decoding A site. Structure 9:647-658. (Pubitemid 32772887)
12. François B, et al. (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. (Pubitemid 41548834)
13. Hobbie SN, Pfister P, Brüll C, Westhof E, Böttger EC (2005) Analysis of the contribution of individual substituents in 4,6-aminoglycoside- ribosome interaction. Antimicrob Agents Chemother 49:5112-5118. (Pubitemid 41778928)
14. 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. (Pubitemid 32401527)
15. Böttger EC (2007) Antimicrobial agents targeting the ribosome: The issue of selectivity and toxicity - lessons to be learned. Cell Mol Life Sci 64:791-795.
16. Fan-Minogue H, Bedwell DM (2008) Eukaryotic ribosomal RNA determinants of aminoglycoside resistance and their role in translational fidelity. RNA 14:148-157.
17. Forge A, Schacht J (2000) Aminoglycoside antibiotics. Audiol Neurootol 5:3-22. (Pubitemid 30093591)
18. Davies J (2007) In the beginning there was streptomycin. Aminoglycoside Antibiotics (John Wiley & Sons, Hoboken, NJ).
19. Prezant TR, et al. (1993) Mitochondrial ribosomal RNA mutation associated with both antibiotic-induced and non-syndromic deafness. Nat Genet 4:289-294. (Pubitemid 23205179)
20. Xie J, Talaska AE, Schacht J (2011) New developments in aminoglycoside therapy and ototoxicity. Hear Res 281:28-37.
21. Leitner MG, Halaszovich CR, Oliver D (2011) Aminoglycosides inhibit KCNQ4 channels in cochlear outer hair cells via depletion of phosphatidylinositol(4, 5)bisphosphate. Mol Pharmacol 79:51-60.
22. Basile AS, et al. (1996) N-methyl-D-aspartate antagonists limit aminoglycoside antibiotic- induced hearing loss. Nat Med 2:1338-1343.
23. Sha SH, Schacht J (1998) Are aminoglycoside antibiotics excitotoxic? Neuroreport 9: 3893-3895.
24. Kalinec GM, et al. (2005) Pivotal role of Harakiri in the induction and prevention of gentamicin-induced hearing loss. Proc Natl Acad Sci USA 102:16019-16024. (Pubitemid 41552860)
25. Sha SH, Schacht J (1999) Stimulation of free radical formation by aminoglycoside antibiotics. Hear Res 128:112-118.
26. Talaska AE, Schacht J (2007) Adverse effects of aminoglycoside therapy. Aminoglycoside Antibiotics (John Wiley & Sons, Hoboken, NJ).
27. Jiang H, Sha SH, Schacht J (2006) Rac/Rho pathway regulates actin depolymerization induced by aminoglycoside antibiotics. J Neurosci Res 83:1544-1551. (Pubitemid 43845000)
28. Hobbie SN, et al. (2008) Mitochondrial deafness alleles confer misreading of the genetic code. Proc Natl Acad Sci USA 105:3244-3249. (Pubitemid 351723538)
29. Hobbie SN, et al. (2008) Genetic analysis of interactions with eukaryotic rRNA identify the mitoribosome as target in aminoglycoside ototoxicity. Proc Natl Acad Sci USA 105: 20888-20893.
30. Pieczenik SR, Neustadt J (2007) Mitochondrial dysfunction and molecular pathways of disease. Exp Mol Pathol 83:84-92. (Pubitemid 46842959)
31. Wu SB, Ma YS, Wu YT, Chen YC, Wei YH (2010) Mitochondrial DNA mutation-elicited oxidative stress, oxidative damage, and altered gene expression in cultured cells of patients with MERRF syndrome. Mol Neurobiol 41:256-266.
32. O'Connor S, Lam LK, Jones ND, Chaney MO (1976) Apramycin, a unique aminocyclitol antibiotic. J Org Chem 41:2087-2092.
33. Ryden R, Moore BJ (1977) The in vitro activity of apramycin, a new aminocyclitol antibiotic. J Antimicrob Chemother 3:609-613. (Pubitemid 8233194)
34. Perzynski S, Cannon M, Cundliffe E, Chahwala SB, Davies J (1979) Effects of apramycin, a novel aminoglycoside antibiotic on bacterial protein synthesis. Eur J Biochem 99:623-628. (Pubitemid 10241795)
35. Hobbie SN, et al. (2007) Engineering the rRNA decoding site of eukaryotic cytosolic ribosomes in bacteria. Nucleic Acids Res 35:6086-6093. (Pubitemid 350018572)
36. Wimberly BT, et al. (2000) Structure of the 30S ribosomal subunit. Nature 407: 327-339.
37. Grentzmann GJ, Ingram JA, Kelly PJ, Gesteland RF, Atkins JF (1998) A dual-luciferase reporter system for studying recoding signals. RNA 4:479-486. (Pubitemid 28160788)
38. Salas-Marco J, Bedwell DM (2005) Discrimination between defects in elongation fidelity and termination efficiency provides mechanistic insights into translational readthrough. J Mol Biol 348:801-815. (Pubitemid 40544383)
39. Kramer EB, Vallabhaneni H, Mayer LM, Farabaugh PJ (2010) A comprehensive analysis of translational missense errors in the yeast Saccharomyces cerevisiae. RNA 16: 1797-1808.
40. Han Q, et al. (2005) Molecular recognition by glycoside pseudo base pairs and triples in an apramycin-RNA complex. Angew Chem Int Ed Engl 44:2694-2700. (Pubitemid 40689568)
41. Wright GD, Berghuis AM, Mobashery S (1998) Aminoglycoside antibiotics. Structures, functions, and resistance. Adv Exp Med Biol 456:27-69.
42. Mukherjee JS, et al. (2004) Programmes and principles in treatment of multidrug-resistant tuberculosis. Lancet 363:474-481. (Pubitemid 38210067)
43. Livermore DM, et al. (2011) Activity of aminoglycosides, including ACHN-490, against carbapenem-resistant Enterobacteriaceae isolates. J Antimicrob Chemother 66:48-53.
44. Zheng JL, Gao WQ (1996) Differential damage to auditory neurons and hair cells by ototoxins and neuroprotection by specific neurotrophins in rat cochlear organotypic cultures. Eur J Neurosci 8:1897-1905. (Pubitemid 26302284)
45. Chen F-Q, Schacht J, Sha SH (2009) Aminoglycoside-induced histone deacetylation and hair cell death in the mouse cochlea. J Neurochem 108:1226-1236.
46. Garetz SL, Schacht J (1996) Ototoxicity: Of mice and men. Clinical Aspects of Hearing. Handbook of Auditory Research, eds van de Water TR, Popper AN, Fay RR. (Springer, New York), Vol. 7, pp 116-154.
47. Harvey SC, Li X, Skolnick P, Kirst HA (2000) The antibacterial and NMDA receptor activating properties of aminoglycosides are dissociable. Eur J Pharmacol 387:1-7. (Pubitemid 30035366)