The mechanism of inhibition of protein synthesis by the proline-rich peptide oncocin

Nature Structural and Molecular Biology

Volumn 22, Issue 6, 2015, Pages 466-469

  Roy, Raktim N ^a   Lomakin, Ivan B ^a   Gagnon, Matthieu G ^a   Steitz, Thomas A ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOACYL TRANSFER RNA; AZITHROMYCIN; CHLORAMPHENICOL; ERYTHROMYCIN; HOMOHARRINGTONINE; MACROLIDE; MESSENGER RNA; ONC112; PEPTIDYL TRANSFER RNA; PROLINE RICH PROTEIN; RNA 23S; TRANSFER RNA; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE; ONCOCIN; PROTEIN SYNTHESIS INHIBITOR;

ANTIBIOTIC RESISTANCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; HYDROGEN BOND; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RIBOSOME; STATIC ELECTRICITY; THERMUS THERMOPHILUS; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

BACTERIA (MICROORGANISMS); THERMUS THERMOPHILUS;

ANTIMICROBIAL CATIONIC PEPTIDES; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN SYNTHESIS INHIBITORS; RIBOSOMES; THERMUS THERMOPHILUS;

EID: 84930417442     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.3031     Document Type: Article

References (32)

1. Yi, H.Y., Chowdhury, M., Huang, Y.D. & Yu, X.Q. Insect antimicrobial peptides and their applications. Appl. Microbiol. Biotechnol. 98, 5807-5822 (2014).
2. de Souza Cândido, E. et al. The use of versatile plant antimicrobial peptides in agribusiness and human health. Peptides 55, 65-78 (2014).
3. Li, W. et al. Proline-rich antimicrobial peptides: potential therapeutics against antibiotic-resistant bacteria. Amino Acids 46, 2287-2294 (2014).
4. Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature 415, 389-395 (2002).
5. Brogden, K.A., Ackermann, M., McCray, P.B. Jr. & Tack, B.F. Antimicrobial peptides in animals and their role in host defences. Int. J. Antimicrob. Agents 22, 465-478 (2003).
6. Otvos, L. Jr. Antibacterial peptides isolated from insects. J. Pept. Sci. 6, 497-511 (2000).
7. Kragol, G. et al. Identifcation of crucial residues for the antibacterial activity of the proline-rich peptide, pyrrhocoricin. Eur. J. Biochem. 269, 4226-4237 (2002).
8. Otvos, L. Jr. et al. Interaction between heat shock proteins and antimicrobial peptides. Biochemistry 39, 14150-14159 (2000).
9. Otvos, L. Jr. Antibacterial peptides and proteins with multiple cellular targets. J. Pept. Sci. 11, 697-706 (2005).
10. Kragol, G. et al. The antibacterial peptide pyrrhocoricin inhibits the ATPase actions of DnaK and prevents chaperone-assisted protein folding. Biochemistry 40, 3016-3026 (2001).
11. Knappe, D. et al. Oncocin (VDKPPYLPRPRPPRRIYNR-NH2): a novel antibacterial peptide optimized against gram-negative human pathogens. J. Med. Chem. 53, 5240-5247 (2010).
12. Hansen, A., Schafer, I., Knappe, D., Seibel, P. & Hoffmann, R. Intracellular toxicity of proline-rich antimicrobial peptides shuttled into mammalian cells by the cell-penetrating peptide penetratin. Antimicrob. Agents Chemother. 56, 5194-5201 (2012).
13. Zahn, M. et al. Structural studies on the forward and reverse binding modes of peptides to the chaperone DnaK. J. Mol. Biol. 425, 2463-2479 (2013).
14. Zahn, M. et al. Structural identifcation of DnaK binding sites within bovine and sheep bactenecin Bac7. Protein Pept. Lett. 21, 407-412 (2014).
15. Berthold, N. & Hoffmann, R. Cellular uptake of apidaecin 1b and related analogs in Gram-negative bacteria reveals novel antibacterial mechanism for proline-rich antimicrobial peptides. Protein Pept. Lett. 21, 391-398 (2014).
16. Krizsan, A. et al. Insect-derived proline-rich antimicrobial peptides kill bacteria by inhibiting bacterial protein translation at the 70 s ribosome. Angew. Chem. Int. Edn Engl. 53, 12236-12239 (2014).
17. Polikanov, Y.S., Steitz, T.A. & Innis, C.A. A proton wire to couple aminoacyl-tRNA accommodation and peptide-bond formation on the ribosome. Nat. Struct. Mol. Biol. 21, 787-793 (2014).
18. Bulkley, D., Innis, C.A., Blaha, G. & Steitz, T.A. Revisiting the structures of several antibiotics bound to the bacterial ribosome. Proc. Natl. Acad. Sci. USA 107, 17158-17163 (2010).
19. Wilson, D.N. On the specifcity of antibiotics targeting the large ribosomal subunit. Ann. NY Acad. Sci. 1241, 1-16 (2011).
20. Garreau de Loubresse, N. et al. Structural basis for the inhibition of the eukaryotic ribosome. Nature 513, 517-522 (2014).
21. Gürel, G., Blaha, G., Moore, P.B. & Steitz, T.A. U2504 determines the species specifcity of the A-site cleft antibiotics: the structures of tiamulin, homoharringtonine, and bruceantin bound to the ribosome. J. Mol. Biol. 389, 146-156 (2009).
22. Arenz, S. et al. Drug sensing by the ribosome induces translational arrest via active site perturbation. Mol. Cell 56, 446-452 (2014).
23. Arenz, S. et al. Molecular basis for erythromycin-dependent ribosome stalling during translation of the ErmBL leader peptide. Nat. Commun. 5, 3501 (2014).
24. Vázquez-Laslop, N. et al. Role of antibiotic ligand in nascent peptide-dependent ribosome stalling. Proc. Natl. Acad. Sci. USA 108, 10496-10501 (2011).
25. Vazquez-Laslop, N., Thum, C. & Mankin, A.S. Molecular mechanism of drug-dependent ribosome stalling. Mol. Cell 30, 190-202 (2008).
26. Knappe, D. et al. Rational design of oncocin derivatives with superior protease stabilities and antibacterial activities based on the high-resolution structure of the oncocin-DnaK complex. ChemBioChem 12, 874-876 (2011).
27. Jünemann, R. et al. In vivo deuteration of transfer RNAs: overexpression and large-scale purifcation of deuterated specifc tRNAs. Nucleic Acids Res. 24, 907-913 (1996).
28. Polikanov, Y.S., Blaha, G.M. & Steitz, T.A. How hibernation factors RMF, HPF, and YfA turn off protein synthesis. Science 336, 915-918 (2012).
29. Kabsch, W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795-800 (1993).
30. Winn, M.D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242 (2011).
31. Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
32. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).