Slippery substrates impair ATP-dependent protease function by slowing unfolding

Journal of Biological Chemistry

Volumn 288, Issue 48, 2013, Pages 34729-34735

  Kraut, Daniel A ^a  

^a VILLANOVA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATP-DEPENDENT PROTEASE; EPSTEIN-BARR VIRUS; EVOLUTIONARY DISTANCE; PARTIAL DEGRADATION; POLYPEPTIDE CHAIN; PROTEIN DEGRADATION; SEQUENCE IDENTITY; SUBSTRATE PROTEINS;

AMINO ACIDS; DEGRADATION; PROTEINS; VIRUSES;

SUBSTRATES;

ADENOSINE TRIPHOSPHATE DEPENDENT PROTEINASE; ALANINE; BACTERIAL ENZYME; GLYCINE; PROTEASOME; PROTEIN CLPXP; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME DEFECT; ENZYME RELEASE; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; MOLECULAR EVOLUTION; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN UNFOLDING; SEQUENCE HOMOLOGY;

EID: 84889025427     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.512533     Document Type: Article

References (25)

1. Sauer, R. T., and Baker, T. A. (2011) AAA+ proteases: ATP-fueled machines of protein destruction. Annu. Rev. Biochem. 80, 587-612
2. Schrader, E. K., Harstad, K. G., and Matouschek, A. (2009) Targeting proteins for degradation. Nat. Chem. Biol. 5, 815-822
3. Koodathingal, P., Jaffe, N. E., Kraut, D. A., Prakash, S., Fishbain, S., Herman, C., and Matouschek, A. (2009) ATP-dependent proteases differ substantially in their ability to unfold globular proteins. J. Biol. Chem. 284, 18674-18684
4. Herman, C., Prakash, S., Lu, C. Z., Matouschek, A., and Gross, C. A. (2003) Lack of a robust unfoldase activity confers a unique level of substrate specificity to the universal AAA protease FtsH. Mol. Cell 11, 659-669
5. Gur, E., Vishkautzan, M., and Sauer, R. T. (2012) Protein unfolding and degradation by the AAA+ Lon protease. Protein Sci. 21, 268-278
6. Kraut, D. A., Israeli, E., Schrader, E. K., Patil, A., Nakai, K., Nanavati, D., Inobe, T., and Matouschek, A. (2012) Sequence- and species-dependence of proteasomal processivity. ACS Chem. Biol. 7, 1444-1453
7. Finley, D. (2009) Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu. Rev. Biochem. 78, 477-513
8. Lander, G. C., Martin, A., and Nogales, E. (2013) The proteasome under the microscope: the regulatory particle in focus. Curr. Opin. Struct. Biol. 23, 243-251
9. Lee, C., Schwartz, M. P., Prakash, S., Iwakura, M., and Matouschek, A. (2001) ATP-dependent proteases degrade their substrates by processively unraveling them from the degradation signal. Mol. Cell 7, 627-637
10. Liu, C. W., Corboy, M. J., DeMartino, G. N., and Thomas, P. J. (2003) Endoproteolytic activity of the proteasome. Science 299, 408-411
11. Rape, M., and Jentsch, S. (2002) Taking a bite: proteasomal protein processing. Nat. Cell Biol. 4, E113-E116
12. Palombella, V. J., Rando, O. J., Goldberg, A. L., and Maniatis, T. (1994) The ubiquitin-proteasome pathway is required for processing the NF-κB1 precursor protein and the activation of NF-κB. Cell 78, 773-785
13. Lin, L., and Ghosh, S. (1996) A glycine-rich region in NF-κB p105 functions as a processing signal for the generation of the p50 subunit. Mol. Cell Biol. 16, 2248-2254
14. Tian, L., Holmgren, R. A., and Matouschek, A. (2005) A conserved processing mechanism regulates the activity of transcription factors Cubitus interruptus and NF-κB. Nat. Struct. Mol. Biol. 12, 1045-1053
15. Levitskaya, J., Coram, M., Levitsky, V., Imreh, S., Steigerwald-Mullen, P. M., Klein, G., Kurilla, M. G., and Masucci, M. G. (1995) Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1. Nature 375, 685-688
16. Levitskaya, J., Sharipo, A., Leonchiks, A., Ciechanover, A., and Masucci, M. G. (1997) Inhibition of ubiquitin/proteasome-dependent protein degradation by the Gly-Ala repeat domain of the Epstein-Barr virus nuclear antigen 1. Proc. Natl. Acad. Sci. U.S.A. 94, 12616-12621
17. Sharipo, A., Imreh, M., Leonchiks, A., Brändén, C., and Masucci, M. G. (2001) cis-Inhibition of proteasomal degradation by viral repeats: impact of length and amino acid composition. FEBS Lett. 499, 137-142
18. Hoyt, M. A., Zich, J., Takeuchi, J., Zhang, M., Govaerts, C., and Coffino, P. (2006) Glycine-alanine repeats impair proper substrate unfolding by the proteasome. EMBO J. 25, 1720-1729
19. Daskalogianni, C., Apcher, S., Candeias, M. M., Naski, N., Calvo, F., and Fåhraeus, R. (2008) Gly-Ala repeats induce position- and substrate-specific regulation of 26 S proteasome-dependent partial processing. J. Biol. Chem. 283, 30090-30100
20. Too, P. H., Erales, J., Simen, J. D., Marjanovic, A., and Coffino, P. (2013) Slippery substrates impair function of a bacterial protease ATPase by un- balancing translocation versus exit. J. Biol. Chem. 288, 13243-13257
21. Hoops, S., Sahle, S., Gauges, R., Lee, C., Pahle, J., Simus, N., Singhal, M., Xu, L., Mendes, P., and Kummer, U. (2006) COPASI-a COmplex PAthway SImulator. Bioinformatics 22, 3067-3074
22. Fersht, A. R. (1999) Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding, 2nd Ed., p. 149, W.H. Freeman and Company, New York
23. Martin, A., Baker, T. A., and Sauer, R. T. (2008) Pore loops of the AAA+ ClpX machine grip substrates to drive translocation and unfolding. Nat. Struct. Mol. Biol. 15, 1147-1151
24. Erales, J., Hoyt, M. A., Troll, F., and Coffino, P. (2012) Functional asymmetries of proteasome translocase pore. J. Biol. Chem. 287, 18535-18543
25. Śledź, P., Unverdorben, P., Beck, F., Pfeifer, G., Schweitzer, A., Förster, F., and Baumeister, W. (2013) Structure of the 26S proteasome with ATP-γS bound provides insights into the mechanism of nucleotide-dependent substrate translocation. Proc. Natl. Acad. Sci. U.S.A. 110, 7264-7269