Gentamicin inhibits HSP70-assisted protein folding by interfering with substrate recognition

FEBS Letters

Volumn 584, Issue 4, 2010, Pages 645-651

  Yamamoto, Soh ^a   Nakano, Shunsuke ^a   Owari, Kensuke ^a   Fuziwara, Kazuhiko ^a   Ogawa, Nobuaki ^a   Otaka, Michiro ^b   Tamaki, Kumiko ^b   Watanabe, Sumio ^b   Komatsuda, Atsushi ^c   Wakui, Hideki ^c   Sawada, Ken ichi ^c   Kubota, Hiroshi ^a   Itoh, Hideaki ^a  

^a AKITA UNIVERSITY   (Japan)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c AKITA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Antibiotics; Gentamicin; Heat shock protein with subunit molecular masses of 70kDa; Molecular chaperone

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; GENTAMICIN; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 70; LUCIFERASE;

AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DRUG PROTEIN BINDING; DRUG TARGETING; ENZYME ACTIVITY; ENZYME SUBSTRATE; FIREFLY; HYDROPHOBICITY; IN VITRO STUDY; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; SURFACE PLASMON RESONANCE;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; BINDING SITES; CHROMATOGRAPHY, AFFINITY; GENTAMICINS; HSP40 HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; LUCIFERASES, FIREFLY; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN FOLDING; SURFACE PLASMON RESONANCE;

EID: 77649273630     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2009.12.021     Document Type: Article

References (40)

1. Parlakpinar H., Tasdemir S., Polat A., Bay-Karabulut A., Vardi N., Ucar M., Acet A. Protective role of caffeic acid phenethyl ester (cape) on gentamicin-induced acute renal toxicity in rats. Toxicology 2005, 207:169-177.
2. Al-Majed A.A., Mostafa A.M., Al-Rikabi A.C., Al-Shabanah O.A. Protective effects of oral arabic gum administration on gentamicin-induced nephrotoxicity in rats. Pharmacol. Res. 2002, 46:445-451.
3. Komatsuda A., et al. Altered localization of 73-kilodalton heat-shock protein in rat kidneys with gentamicin-induced acute tubular injury. Lab. Invest. 1993, 68:687-695.
4. Walker P.D., Barri Y., Shah S.V. Oxidant mechanisms in gentamicin nephrotoxicity. Renal Fail. 1999, 21:433-442.
5. Miyazaki T., et al. 73-kDa molecular chaperone HSP73 is a direct target of antibiotic gentamicin. J. Biol. Chem. 2004, 279:17295-17300.
6. Flaherty K.M., DeLuca-Flaherty C., McKay D.B. Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature 1990, 346:623-628.
7. Mayer M.P., Bukau B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol. Life Sci. 2005, 62:670-684.
8. Morshauser R.C., Wang H., Flynn G.C., Zuiderweg E.R. The peptide-binding domain of the chaperone protein Hsc70 has an unusual secondary structure topology. Biochemistry 1995, 34:6261-6266.
9. Swain J.F., Dinler G., Sivendran R., Montgomery D.L., Stotz M., Gierasch L.M. Hsp70 chaperone ligands control domain association via an allosteric mechanism mediated by the interdomain linker. Mol. Cell 2007, 26:27-39.
10. Bertelsen E.B., Chang L., Gestwicki J.E., Zuiderweg E.R. Solution conformation of wild-type E. coli Hsp70 (DnaK) chaperone complexed with ADP and substrate. Proc. Natl. Acad. Sci. USA 2009, 106:8471-8476.
11. Zhu X., Zhao X., Burkholder W.F., Gragerov A., Ogata C.M., Gottesman M.E., Hendrickson W.A. Structural analysis of substrate binding by the molecular chaperone DnaK. Science 1996, 272:1606-1614.
12. Schmid D., Baici A., Gehring H., Christen P. Kinetics of molecular chaperone action. Science 1994, 263:971-973.
13. Greene L.E., Zinner R., Naficy S., Eisenberg E. Effect of nucleotide on the binding of peptides to 70-kDa heat shock protein. J. Biol. Chem. 1995, 270:2967-2973.
14. Palleros D.R., Reid K.L., Shi L., Welch W.J., Fink A.L. ATP-induced protein-Hsp70 complex dissociation requires K+ but not ATP hydrolysis. Nature 1993, 365:664-666.
15. Freeman B.C., Myers M.P., Schumacher R., Morimoto R.I. Identification of a regulatory motif in Hsp70 that affects ATPase activity, substrate binding and interaction with HDJ-1. EMBO J. 1995, 14:2281-2292.
16. Bukau B., Weissman J., Horwich A. Molecular chaperones and protein quality control. Cell 2006, 125:443-451.
17. Fan C.Y., Lee S., Cyr D.M. Mechanisms for regulation of Hsp70 function by Hsp40. Cell Stress Chaperones 2003, 8:309-316.
18. Polier S., Dragovic Z., Hartl F.U., Bracher A. Structural basis for the cooperation of Hsp70 and Hsp110 chaperones in protein folding. Cell 2008, 133:1068-1079.
19. Xu Z., Page R.C., Gomes M.M., Kohli E., Nix J.C., Herr A.B., Patterson C., Misra S. Structural basis of nucleotide exchange and client binding by the Hsp70 cochaperone Bag2. Nat. Struct. Mol. Biol. 2008, 15:1309-1317.
20. Otaka M., et al. The induction mechanism of the molecular chaperone HSP70 in the gastric mucosa by Geranylgeranylacetone (HSP-inducer). Biochem. Biophys. Res. Commun. 2007, 353:399-404.
21. Wang C., Lee M.R. High-level expression of soluble rat hsc70 in Escherichia coli: purification and characterization of the cloned enzyme. Biochem. J. 1993, 294(Pt 1):69-77.
22. Terlecky S.R., Chiang H.L., Olson T.S., Dice J.F. Protein and peptide binding and stimulation of in vitro lysosomal proteolysis by the 73-kDa heat shock cognate protein. J. Biol. Chem. 1992, 267:9202-9209.
23. Flynn G.C., Chappell T.G., Rothman J.E. Peptide binding and release by proteins implicated as catalysts of protein assembly. Science 1989, 245:385-390.
24. Wegele H., Wandinger S.K., Schmid A.B., Reinstein J., Buchner J. Substrate transfer from the chaperone Hsp70 to Hsp90. J. Mol. Biol. 2006, 356:802-811.
25. Tapley T.L., Cupp-Vickery J.R., Vickery L.E. Sequence-dependent peptide binding orientation by the molecular chaperone DnaK. Biochemistry 2005, 44:12307-12315.
26. Hartl F.U., Hayer-Hartl M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 2002, 295:1852-1858.
27. Rudiger S., Buchberger A., Bukau B. Interaction of Hsp70 chaperones with substrates. Nat. Struct. Biol. 1997, 4:342-349.
28. Suh W.C., Lu C.Z., Gross C.A. Structural features required for the interaction of the Hsp70 molecular chaperone DnaK with its cochaperone DnaJ. J. Biol. Chem. 1999, 274:30534-30539.
29. Soti C., Nagy E., Giricz Z., Vigh L., Csermely P., Ferdinandy P. Heat shock proteins as emerging therapeutic targets. Br. J. Pharmacol. 2005, 146:769-780.
30. Donnelly A., Blagg B.S. Novobiocin and additional inhibitors of the Hsp90 C-terminal nucleotide-binding pocket. Curr. Med. Chem. 2008, 15:2702-2717.
31. Ishida R., et al. Cisplatin differently affects amino terminal and carboxyl terminal domains of HSP90. FEBS Lett. 2008, 582:3879-3883.
32. Liebscher M., Jahreis G., Lucke C., Grabley S., Raina S., Schiene-Fischer C. Fatty acyl benzamido antibacterials based on inhibition of DnaK-catalyzed protein folding. J. Biol. Chem. 2007, 282:4437-4446.
33. Pacifici G.M. Clinical pharmacokinetics of aminoglycosides in the neonate: a review. Eur. J. Clin. Pharmacol. 2009, 65:419-427.
34. Zietse R., Zoutendijk R., Hoorn E.J. Fluid, electrolyte and acid-base disorders associated with antibiotic therapy. Nat. Rev. Nephrol. 2009, 5:193-202.
35. Schmitz C., Hilpert J., Jacobsen C., Boensch C., Christensen E.I., Luft F.C., Willnow T.E. Megalin deficiency offers protection from renal aminoglycoside accumulation. J. Biol. Chem. 2002, 277:618-622.
36. El Mouedden M., Laurent G., Mingeot-Leclercq M.P., Tulkens P.M. Gentamicin-induced apoptosis in renal cell lines and embryonic rat fibroblasts. Toxicol. Sci. 2000, 56:229-239.
37. Sandoval R.M., Molitoris B.A. Gentamicin traffics retrograde through the secretory pathway and is released in the cytosol via the endoplasmic reticulum. Am. J. Physiol. Renal Physiol. 2004, 286:F617-F624.
38. Servais H., Van Der Smissen P., Thirion G., Van der Essen G., Van Bambeke F., Tulkens P.M., Mingeot-Leclercq M.P. Gentamicin-induced apoptosis in LLC-PK1 cells: involvement of lysosomes and mitochondria. Toxicol. Appl. Pharmacol. 2005, 206:321-333.
39. Priyamvada S., Priyadarshini M., Arivarasu N.A., Farooq N., Khan S., Khan S.A., Khan M.W., Yusufi A.N. Studies on the protective effect of dietary fish oil on gentamicin-induced nephrotoxicity and oxidative damage in rat kidney. Prostaglandins Leukot. Essent. Fatty Acids 2008, 78:369-381.
40. Itoh H., Tashima Y. The stress (heat shock) proteins. Int. J. Biochem. 1991, 23:1185-1191.