Nucleotide-dependent substrate recognition by the AAA+ HslUV protease (original) (raw)

References

  1. Gottesman, S. Proteolysis in bacterial regulatory circuits. Annu. Rev. Cell Dev. Biol. 19, 565–587 (2003).
    Article CAS Google Scholar
  2. Chiba, S., Akiyama, Y., Mori, H., Matsuo, E. & Ito, K. Length recognition at the N-terminal tail for the initiation of FtsH-mediated proteolysis. EMBO Rep. 1, 47–52 (2000).
    Article CAS Google Scholar
  3. Bochtler, M., Ditzel, L., Groll, M. & Huber, R. Crystal structure of heat shock locus V (HslV) from Escherichia coli. Proc. Natl. Acad. Sci. USA 94, 6070–6074 (1997).
    Article CAS Google Scholar
  4. Bochtler, M. et al. The structures of HslU and the ATP-dependent protease HslU-HslV. Nature 403, 800–805 (2000).
    Article CAS Google Scholar
  5. Sousa, M.C., Kessler, B.M., Overkleeft, H.S. & McKay, D.B. Crystal structure of HslUV complexed with a vinyl sulfone inhibitor: corroboration of a proposed mechanism of allosteric activation of HslV by HslU. J. Mol. Biol. 318, 779–785 (2002).
    Article CAS Google Scholar
  6. Sousa, M.C. et al. Crystal and solution structures of an HslUV protease–chaperone complex. Cell 103, 633–643 (2000).
    Article CAS Google Scholar
  7. Song, H.K. et al. Mutational studies on HslU and its docking mode with HslV. Proc. Natl. Acad. Sci. USA 97, 14103–14108 (2000).
    Article CAS Google Scholar
  8. Wang, J. et al. Nucleotide-dependent conformational changes in a protease-associated ATPase HslU. Structure 9, 1107–1116 (2001).
    Article CAS Google Scholar
  9. Trame, C.B. & McKay, D.B. Structure of Haemophilus influenzae HslU protein in crystals with one-dimensional disorder twinning. Acta Crystallogr. D 57, 1079–1090 (2001).
  10. Rohrwild, M. et al. The ATP-dependent HslUV protease from Escherichia coli is a four-ring structure resembling the proteasome. Nat. Struct. Biol. 4, 133–139 (1997).
    Article CAS Google Scholar
  11. Kanemori, M., Nishihara, K., Yanagi, H. & Yura, T. Synergistic roles of HslVU and other ATP-dependent proteases in controlling in vivo turnover of sigma32 and abnormal proteins in Escherichia coli. J. Bacteriol. 179, 7219–7225 (1997).
    Article CAS Google Scholar
  12. Missiakas, D., Schwager, F., Betton, J.-M., Georgopoulos, C. & Rania, S. Identification and characterization of HslV HslU (ClpQ ClpY) proteins involved in overall proteolysis of misfolded proteins in Escherichia coli. EMBO J. 15, 6899–6909 (1996).
    Article CAS Google Scholar
  13. Wu, W.-F., Zhou, Y. & Gottesman, S. Redundant in vivo proteolytic activities of Escherichia coli Lon and the ClpYQ (HslUV) protease. J. Bacteriol. 181, 3681–3687 (1999).
    CAS PubMed PubMed Central Google Scholar
  14. Chuang, S. & Blattner, F.R. Characterization of twenty-six new heat shock genes of Escherichia coli. J. Bacteriol. 175, 5242–5252 (1993).
    Article CAS Google Scholar
  15. Seong, I.S., Oh, J.Y., Yoo, S.J., Seol, J.H. & Chung, C.H. ATP-dependent degradation of SulA, a cell division inhibitor, by the HslUV protease in Escherichia coli. FEBS Lett. 456, 211–214 (1999).
    Article CAS Google Scholar
  16. Nishii, W. & Takahashi, L. Determination of the cleavage sites in SulA, a cell division inhibitor, by the ATP-dependent HslVU protease from Escherichia coli. FEBS Lett. 553, 351–354 (2003).
    Article CAS Google Scholar
  17. Kwon, A.R., Trame, C.B. & McKay, D.B. Kinetics of protein substrate degradation by HslUV. J. Struct. Biol. 146, 141–147 (2004).
    Article CAS Google Scholar
  18. Waldburger, C.D., Schildbach, J.F. & Sauer, R.T. Are buried salt bridges important for protein stability and conformational specificity? Nat. Struct. Biol. 2, 122–128 (1995).
    Article CAS Google Scholar
  19. Carrion-Vazquez, M. et al. Mechanical and chemical unfolding of a single protein: a comparison. Proc. Natl. Acad. Sci. USA 96, 3694–3699 (1999).
    Article CAS Google Scholar
  20. Kenniston, J.A., Baker, T.A., Fernandez, J.M. & Sauer, R.T. Linkage between ATP consumption and mechanical unfolding during the protein processing reactions of an AAA+ degradation machine. Cell 114, 511–520 (2003).
    Article CAS Google Scholar
  21. Breg, J.N., Opheusden, J.H.v., Burgering, M.J., Boelens, R. & Kaptein, R. Structure of Arc repressor in solution: evidence for a family of β-sheet DNA-binding proteins. Nature 346, 586–589 (1990).
    Article CAS Google Scholar
  22. Milla, M.E. & Sauer, R.T. Critical side-chain interactions at a subunit interface in the Arc repressor dimer. Biochemistry 34, 3344–3351 (1995).
    Article CAS Google Scholar
  23. Burgering, M.J.M., Hald, M., Boelens, R., Breg, J.N. & Kaptein, R. Hydrogen exchange studies of the Arc repressor: evidence for a monomeric folding intermediate. Biopolymers 35, 217–226 (1995).
    Article CAS Google Scholar
  24. Schlieker, C. et al. Substrate recognition by the AAA+ chaperone ClpB. Nat. Struct. Mol. Biol. 11, 607–615 (2004).
    Article CAS Google Scholar
  25. Siddiqui, S.M., Sauer, R.T. & Baker, T.A. Role of the processing pore of the ClpX AAA+ ATPase in the recognition and engagement of specific protein substrates. Genes Dev. 18, 369–374 (2004).
    Article CAS Google Scholar
  26. Sondek, J., Lambright, D.G., Noel, J.P., Hamm, H.E. & Sigler, P.B. GTPase mechanism of G proteins from the 1.7-Å crystal structure of transducin α•GDP•AlF4−. Nature 372, 276–279 (1994).
    Article CAS Google Scholar
  27. Ishii, Y. et al. Regulatory role of C-terminal residues of SulA in its degradation by Lon protease in Escherichia coli. J. Biochem. 127, 837–844 (2000).
    Article CAS Google Scholar
  28. Kwon, A.R., Kesseler, B.M., Overkleeft, H.S. & McKay, D.B. Structure and reactivity of an asymmetric complex between HslV and I-domain deleted HslU, a prokaryotic homolog of the eukaryotic proteasome. J. Mol. Biol. 330, 185–195 (2003).
    Article CAS Google Scholar
  29. Levchenko, I., Seidel, M., Sauer, R.T. & Baker, T.A. A specificity-enhancing factor controls substrate delivery to the ClpXP degradation machine. Science 289, 2354–2356 (2000).
    Article CAS Google Scholar
  30. Milla, M.E., Brown, B.M., Waldbuger, C.D. & Sauer, R.T. P22 Arc repressor: transition state properties inferred from mutational effects on the rates of protein unfolding and refolding. Biochemistry 39, 12494–12502 (1995).
    Google Scholar
  31. Bowie, J.U. & Sauer, R.T. Equilibrium dissociation and unfolding of the Arc repressor dimer. Biochemistry 28, 7139–7143 (1989).
    Article CAS Google Scholar
  32. Kim, Y.-I., Burton, R.E., Burton, B.M., Sauer, R.T. & Baker, T.A. Dynamics of substrate denaturation and translocation by the ClpXP degradation machine. Mol. Cell 5, 639–648 (2000).
    Article CAS Google Scholar
  33. Burton, R.E., Siddiqui, S.M., Kim, Y.-I., Baker, T.A. & Sauer, R.T. Effects of protein stability and structure on substrate processing by the ClpXP unfolding and degradation machine. EMBO J. 20, 3092–3100 (2001).
    Article CAS Google Scholar
  34. Lee, C., Schwartz, M.P., Prakash, S., Iwakura, M. & Matouschek, A. ATP-dependent proteases degrade their substrates by processively unraveling them from the degradation signal. Mol. Cell 7, 627–637 (2001).
    Article CAS Google Scholar
  35. Kenniston, J.A., Burton, R.E., Siddiqui, S.M., Baker, T.A. & Sauer, R.T. Effects of local protein stability and the geometric position of the substrate degradation tag on the efficiency of ClpXP denaturation and degradation. J. Struct. Biol. 146, 130–140 (2004).
    Article CAS Google Scholar
  36. Schildbach, J.F., Milla, M.E., Jeffrey, P.D., Raumann, B.E. & Sauer, R.T. Crystal structure, folding, and operator binding of the hyperstable Arc repressor mutant PL8. Biochemistry 34, 1405–1412 (1995).
    Article CAS Google Scholar
  37. Robinson, C.R. & Sauer, R.T. Striking stabilization of Arc repressor by an engineered disulfide bond. Biochemistry 39, 12494–12502 (2000).
    Article CAS Google Scholar
  38. Bolon, D.N., Grant, R.A., Baker, T.A. & Sauer, R.T. Nucleotide-dependent substrate handoff from the SspB adaptor to the AAA+ ClpXP protease. Mol. Cell 16, 343–350 (2004).
    Article CAS Google Scholar
  39. Singh, S.K., Grimaud, R., Hoskins, J.R., Wickner, S. & Maurizi, M.R. Unfolding and internalization of proteins by the ATP-dependent proteases ClpXP and ClpAP. Proc. Natl. Acad. Sci. USA 97, 8898–8903 (2000).
    Article CAS Google Scholar
  40. Gottesman, S., Roche, E., Zhou, Y. & Sauer, R.T. The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the ssrA-tagging system. Genes Dev. 12, 1338–1347 (1998).
    Article CAS Google Scholar

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