A novel role of cytosolic protein synthesis inhibition in aminoglycoside ototoxicity

Journal of Neuroscience

Volumn 33, Issue 7, 2013, Pages 3079-3093

  Francis, Shimon P ^a   Katz, Joshua ^a   Fanning, Kathryn D ^b   Harris, Kimberly A ^b   Nicholas, Brian D ^a   Lacy, Michael ^a   Pagana, James ^a   Agris, Paul F ^b   Shin, Jung Bum ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; AMINOGLYCOSIDE ANTIBIOTIC AGENT; GENTAMICIN; RIBOSOME RNA; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL SURVIVAL; CHICK; CONTROLLED STUDY; CORTI ORGAN; EMBRYO; EVOKED BRAIN STEM AUDITORY RESPONSE; EXPLANT; HAIR CELL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE TEST; IMMUNOREACTIVITY; MOUSE; NERVE CELL DEGENERATION; NONHUMAN; OTOTOXICITY; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; RIBOSOME SUBUNIT; THERMOSTABILITY; UTRICLE;

ALANINE; ALKYNES; AMINOGLYCOSIDES; ANIMALS; ANTI-BACTERIAL AGENTS; APOPTOSIS; BLOTTING, WESTERN; CELL COUNT; CHICK EMBRYO; CYTOSOL; EAR DISEASES; ENZYME ACTIVATION; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; GLYCINE; HAIR CELLS, AUDITORY; IMMUNOHISTOCHEMISTRY; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE; MICE, INBRED CBA; NIACINAMIDE; ORGAN CULTURE TECHNIQUES; PHENYLUREA COMPOUNDS; PROTEIN KINASE INHIBITORS; PROTEIN SYNTHESIS INHIBITORS; RNA, RIBOSOMAL;

EID: 84873616809     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3430-12.2013     Document Type: Article

References (67)

1. Agard NJ, Prescher JA, Bertozzi CR (2004) A strain-promoted [3+2] azide-alkyne cycloaddition for covalent modification of biomolecules in living systems. J Am Chem Soc 126:15046-15047. CrossRef Medline
2. Beatty KE, Tirrell DA (2008) Two-color labeling of temporally defined protein populations in mammalian cells. Bioorg Med Chem Lett 18:5995-5999. CrossRef Medline
3. Bedwell DM, Kaenjak A, Benos DJ, Bebok Z, Bubien JK, Hong J, Tousson A, Clancy JP, Sorscher EJ (1997) Suppression of a CFTR premature stop mutation in a bronchial epithelial cell line. Nat Med 3:1280-1284. CrossRef Medline
4. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2:326-332. CrossRef Medline
5. Beugnet A, Tee AR, Taylor PM, Proud CG (2003) Regulation of targets of mTOR (mammalian target of rapamycin) signalling by intracellular amino acid availability. Biochem J 372:555-566. CrossRef Medline
6. Borovinskaya MA, Pai RD, Zhang W, Schuwirth BS, Holton JM, Hirokawa G, Kaji H, Kaji A, Cate JH (2007) Structural basis for aminoglycoside inhibition of bacterial ribosome recycling. Nat Struct Mol Biol 14:727-732. CrossRef Medline
7. 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. CrossRef Medline
8. Burke JF, Mogg AE (1985) Suppression of a nonsense mutation in mammalian cells in vivo by the aminoglycoside antibiotics G-418 and paromomy-cin. Nucleic Acids Res 13:6265-6272. CrossRef Medline
9. Burns J, Christophel JJ, Collado MSOL, Magnus C, Carfrae M, Corwin JT (2008) Reinforcement of cell junctions correlates with the absence of hair cell regeneration in mammals and its occurrence in birds. J Comp Neurol 414:396-414. Medline
10. Choo AY, Yoon SO, Kim SG, Roux PP, Blenis J (2008) Rapamycin differentially inhibits S6Ks and 4E-BP1 to mediate cell-type-specific repression of mRNA translation. Proc Natl Acad Sci U S A 105:17414-17419. CrossRef Medline
11. Coffin AB, Ou H, Owens KN, Santos F, Simon JA, Rubel EW, Raible DW (2010) Chemical screening for hair cell loss and protection in the ze-brafish lateral line. Zebrafish 7:3-11. CrossRef Medline
12. Davies J, Gorini L, Davis BD (1965) Misreading of RNA aminoglycoside codewords induced by antibiotics. Mol Pharmacol 1:93-106.
13. Dieterich DC, Link AJ, Graumann J, Tirrell DA, Schuman EM (2006) Selective identification of newly synthesized proteins in mammalian cells using bioorthogonal noncanonical amino acid tagging (BONCAT). Proc Natl Acad Sci U S A 103:9482-9487. CrossRef Medline
14. Dieterich DC, Hodas JJ, Gouzer G, Shadrin IY, Ngo JT, Triller A, Tirrell DA, Schuman EM (2010) In situ visualization and dynamics of newly synthesized proteins in rat hippocampal neurons. Nat Neurosci 13:897-905. CrossRef Medline
15. Garden GA, Canady KS, Lurie DI, Bothwell M, Rubel EW (1994) A biphasic change in ribosomal conformation during transneuronal degeneration is altered by inhibition of mitochondrial, but not cytoplasic protein synthesis. J Neurosci 14:1994-2008. Medline
16. Gebauer F, Hentze MW (2004) Molecular mechanisms of translational control. Nat Rev Mol Cell Biol 5:827-835. CrossRef Medline
17. Gillespie PG, Walker RG (2001) Molecular basis of mechanosensory transduction. Nature 413:194-202. CrossRef Medline
18. Guan MX (2011) Mitochondrial 12S rRNA mutations associated with aminoglycoside ototoxicity. Mitochondrion 11:237-245. CrossRef Medline
19. Hara K, Yonezawa K, Weng QP, Kozlowski MT, Belham C, Avruch J (1998) Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF-4E BP1 through a common effector mechanism. J Biol Chem 273:14484-14494. CrossRef Medline
20. Hinz FI, Dieterich DC, Tirrell DA, Schuman EM (2012) Non-canonical amino acid labeling in vivo to visualize and affinity purify newly synthesized proteins in larval zebrafish. ACS Chem Neurosci 3:40-49. CrossRef Medline
21. Hirose K, Sato E (2011) Comparative analysis of combination kanamycinfurosemide versus kanamycin alone in the mouse cochlea. Hearing Res 272:108-116. CrossRef
22. Holcik M, Sonenberg N (2005) Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6:318-327. CrossRef Medline
23. Hudspeth AJ (1989) How the ear's works work. Nature 341:397-404. CrossRef Medline
24. Hyde GE, Rubel EW (1995) Mitochondrial role in hair cell survival after injury. Otolaryngol Head Neck Surg 113:530-540. CrossRef Medline
25. Iordanov MS, Pribnow D, Magun JL, Dinh TH, Pearson JA, Chen SL, Magun BE (1997) Ribotoxic stress response: activation of the stress-activated protein kinase JNK1 by inhibitors of the peptidyl transferase reaction and by sequence-specific RNA damage to the alpha-sarcin/ricin loop in the 28S rRNA. Mol Cell Biol 17:3373-3381. Medline
26. Iqbal SM, Srivatsav CB (1984) Chloramphenicol ototoxicity. A case report. J Laryngol Otol 98:523-525. CrossRef Medline
27. Jandhyala DM, Ahluwalia A, Obrig T, Thorpe CM (2008) ZAK: a MAP3Kinase that transduces Shiga toxin-and ricin-induced proinflammatory cytokine expression. Cell Microbiol 10:1468-1477. CrossRef Medline
28. Kageyama A, Kusano I, Tamura T, Oda T, Muramatzu T (2002) Comparison of the apoptosis-inducing abilities of various protein synthesis inhibitors in U937 Cells. Biosci Biotech Biochem 66:835-839. CrossRef
29. Karaman MW, Herrgard S, Treiber DK, Gallant P, Atteridge CE, Campbell BT, Chan KW, Ciceri P, Davis MI, Edeen PT, Faraoni R, Floyd M, Hunt JP, Lockhart DJ, Milanov ZV, Morrison MJ, Pallares G, Patel HK, Pritchard S, Wodicka LM, et al. (2008) A quantitative analysis of kinase inhibitor selectivity. Nat Biotechnol 26:127-132. CrossRef Medline
30. Kasinath BS, Feliers D, Sataranatarajan K, Ghosh Choudhury G, Lee MJ, Mariappan MM (2009) Regulation of mRNA translation in renal physiology and disease. Am J Physiol Renal Physiol 297:1153-1165. Medline
31. Keller JN (2006) Interplay between oxidative damage, protein synthesis, and protein degradation in Alzheimer's disease. J Biomed Biotechnol 2006:12129. Medline
32. Kiick KL, Saxon E, Tirrell DA, Bertozzi CR (2002) Incorporation of azides into recombinant proteins for chemoselective modification by the Staudinger ligation. Proc Natl Acad Sci U S A 99:19-24. CrossRef Medline
33. Kochi SK, Collier RJ (1993) DNA fragmentation and cytolysis in U937 cells treated with diphteria toxin or other inhibitors of protein synthesis. Exp Cell Res 208:296-302. CrossRef Medline
34. Kolb HC, Sharpless KB (2003) The growing impact of click chemistry on drug discovery. Drug Discov Today 8:1128-1137. CrossRef Medline
35. Lockshin RA, Zakeri ZF (1992) Physiology and protein synthesis in programmed cell death: Early Synthesis and DNA degradation. Ann N Y Acad Sci 663:234-249. CrossRef
36. Lu J, Li Z, Zhu Y, Yang A, Li R, Zheng J, Cai Q, Peng G, Zheng W, Tang X, Chen B, Chen J, Liao Z, Yang L, Li Y, You J, Ding Y, Yu H, Wang J, Sun D, et al. (2010) Mitochondrial 12S rRNA variants in 1642 Han Chinese pediatric subjects with aminoglycoside-induced and nonsyndromic hearing loss. Mitochondrion 10:380-390. CrossRef Medline
37. Lu Z, Hunter T (2009) Degradation of activated protein kinases by ubiquitination. Annu Rev Biochem 78:435-475. CrossRef Medline
38. Lyford-Pike S, Vogelheim C, Chu E, Della Santina CC, Carey JP (2007) Gentamicin is primarily localized in vestibular type I hair cells after intratympanic administration. J Assoc Res Otolaryngol 4:497-508. Medline
39. Ma XM, Blenis J (2009) Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 10:307-318. CrossRef Medline
40. Magnet S, Blanchard JS (2005) Molecular insights into aminoglycoside action and resistance. Chem Rev 105:477-498. CrossRef Medline
41. Marcotti W, van Netten SM, Kros CJ (2005) The aminoglycoside antibiotic dihydrostreptomycin rapidly enters hair cells through the mechano-electrical transducer channels. J Physiol 567:505-521. CrossRef Medline
42. Matsui JI, Ogilvie JM, Warchol ME (2002) Inhibition of caspases prevents ototoxic and ongoing hair cell death. J Neurosci 22:1218-1227. Medline
43. 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 14:2012. Medline
44. Mesner PW, Winters TR, Green SH (1992) Nerve growth factor withdrawal-induced cell death in neuronal PC12 cells resembles that in sympathetic neurons. J Cell Biol 119:1669-1680. CrossRef Medline
45. Meyuhas O (2000) Synthesis of the translational apparatus is regulated at the translational level. Eur J Biochem 267:6321-6330. CrossRef Medline
46. Moazed D, Noller HF (1987) Interaction of antibiotics with functional sites in 16S ribosomal RNA. Nature 327:389-394. CrossRef Medline
47. Oesterle EC, Campbell S (2009) Supporting cell characteristics in long-deafened aged mouse ears. J Assoc Res Otolaryngol 10:525-544. CrossRef Medline
48. Pestka JJ (2010) Deoxynivalenol: mechanisms of action, human exposure, and toxicological relevance. Arch Toxicol 84:663-679. CrossRef Medline
49. Pirvola U, Xing-Qun L, Virkkala J, Saarma M, Murakata C, Camoratto AM, Walton KM, Ylikoski J (2000) Rescue of hearing, auditory hair cells, and neurons by CEP-1347/KT7515, an inhibitor of c-Jun N-terminal kinase activation. J Neurosci 20:43-50. Medline
50. Ramachandran A, Moellering DR, Ceaser E, Shiva S, Xu J, Darley-Usmar V (2002) Inhibition of mitochondrial protein synthesis results in increased endothelial cell susceptibility to nitric oxide-induced apoptosis. Proc Natl Acad Sci U S A 99:6643-6648. CrossRef Medline
51. Recht MI, Douthwaite S, Puglisi JD (1999) Basis for prokaryotic specificity of action of aminoglycoside antibiotics. EMBO J 18:3133-3138. CrossRef Medline
52. Rehen SK, Varella MH, Freitas FG, Moraes MO, Linden R (1996) Contrasting effects of protein synthesis inhibition and of cyclic AMP on apoptosis in the developing retina. Development 122:1439-1448. Medline
53. Richardson GP, Forge A, Kros CJ, Fleming J, Brown SD, Steel KP (1997) Myosin VIIA is required for aminoglycoside accumulation in cochlear hair cells. J Neurosci 17:9506-9519. Medline
54. Rybak LP, Whitworth CA (2005) Ototoxicity: therapeutic opportunities. Drug Discov Today 10:1313-1321. CrossRef Medline
55. Sauter KA, Magun EA, Iordanov MS, Magun BE (2010) ZAK is required for doxorubicin, a novel ribotoxic stressor, to induce SAPK activation and apoptosis in HaCaT cells. Cancer Biol Ther 10:258-266. CrossRef Medline
56. Scheunemann AE, Graham WD, Vendeix FA, Agris PF (2010) Binding of aminoglycoside antibiotics to helix 69 of 23S rRNA. Nucleic Acids Res 38:3094-3105. CrossRef Medline
57. Schmitz C, Hilpert J, Jacobsen C, Boensch C, Christensen EI, Luft FC, Willnow TE (2002) Megalin deficiency offers protection from renal aminoglycoside accumulation. J Biol Chem 277:618-622. Medline
58. Schröder M, Kaufman RJ (2005) The mammalian unfolded protein response. Annu Rev Biochem 74:739-789. CrossRef Medline
59. Sonenberg N, Hinnebusch AG (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136:731-745. CrossRef Medline
60. Steyger PS, Peters SL, Rehling J, Hordichok A, Dai CF (2003) Uptake of gentamicin by bullfrog saccular hair cells in vitro. J Assoc Res Otolaryngol 4:565-578. CrossRef Medline
61. Sundin DP, Sandoval R, Molitoris BA (2001) Gentamicin inhibits renal protein and phospholipid metabolism in rats: implications involving intracellular trafficking. J Am Soc Nephrol 12:114-123. Medline
62. Taylor RR, Nevill G, Forge A (2008) Rapid hair cell loss: a mouse model for cochlear lesions. J Assoc Res Otolaryngol 9:44-64. CrossRef Medline
63. Tran Ba Huy P, Bernard P, Schacht J (1986) Kinetics of gentamicin uptake and release in the rat. Comparison of inner ear tissues and fluids with other organs. J Clin Invest 77:1492-1500. CrossRef Medline
64. Wang J, Van De Water TR, Bonny C, de Ribaupierre F, Puel JL, Zine A (2003) A peptide inhibitor of c-Jun N-terminal kinase protects against both aminoglycoside and acoustic trauma-induced auditory hair cell death and hearing loss. J Neurosci 23:8596-8607. Medline
65. Wang X, Proud CG (2007) Methods for studying signal-dependent regulation of translation factor activity. Methods Enzymol 431:113-142. CrossRef Medline
66. Wilhelm S, Carter C, Lynch M, Lowinger T, Dumas J, Smith RA, Schwartz B, Simantov R, Kelley S (2006) Discovery and development of sorafenib: a multikinase inhibitor for treating cancer. Nat Rev Drug Discov 5:835-844. CrossRef Medline
67. Xie J, Talaska AE, Schacht J (2011) New developments in aminoglycoside therapy and ototoxicity. Hearing research 281:28-37. CrossRef Medline