Roles of the N domain of the AAA+ Lon protease in substrate recognition, allosteric regulation and chaperone activity

Molecular Microbiology

Volumn 91, Issue 1, 2014, Pages 66-78

  Wohlever, Matthew L ^a   Baker, Tania A ^a   Sauer, Robert T ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; CHAPERONE; DEGRON; ENDOPEPTIDASE LA; PYRUVATE KINASE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; CLPX PROTEIN, E COLI; ENDOPEPTIDASE CLP; ESCHERICHIA COLI PROTEIN; HYBRID PROTEIN; LON PROTEIN, E COLI; SULA PROTEIN, E COLI;

ALLOSTERISM; AMINO TERMINAL SEQUENCE; ANISOTROPY; ARTICLE; BINDING AFFINITY; BINDING SITE; BIOTINYLATION; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; HYDROLYSIS; HYDROPHOBICITY; IN VIVO STUDY; MOLECULAR RECOGNITION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PURIFICATION; RESTRICTION SITE; TRANSACTIVATION ASSAY; CHEMISTRY; ENZYME SPECIFICITY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION;

ESCHERICHIA;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ALLOSTERIC REGULATION; BINDING SITES; ENDOPEPTIDASE CLP; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR CHAPERONES; MUTATION; PROTEASE LA; PROTEOLYSIS; RECOMBINANT FUSION PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84891165714     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12444     Document Type: Article

References (50)

1. Adam, C., Picard, M., Déquard-Chablat, M., Sellem, C.H., Hermann-Le Denmat, S., and Contamine, V. (2012) Biological roles of the Podospora anserina mitochondrial Lon protease and the importance of its N-domain. PLoS ONE 7: e38138.
2. Amerik, A.Y., Antonov, V.K., Gorbalenya, A.E., Kotova, S.A., Rotanova, T.V., and Shimbarevich, E.V. (1991) Site-directed mutagenesis of La protease. A catalytically active serine residue. FEBS Lett 287: 211-214.
3. Bernstein, S.H., Venkatesh, S., Li, M., Lee, J., Lu, B., Hilchey, S.P., etal. (2012) The mitochondrial ATP-dependent Lon protease: a novel target in lymphoma death mediated by the synthetic triterpenoid CDDO and its derivatives. Blood 119: 3321-3329.
4. Breidenstein, E.B.M., Janot, L., Strehmel, J., Fernandez, L., Taylor, P.K., Kukavica-Ibrulj, I., etal. (2012) The Lon protease is essential for full virulence in Pseudomonas aeruginosa. PLoS ONE 7: e49123.
5. Cha, S.S., An, Y.J., Lee, C.R., Lee, H.S., Kim, Y.G., Kim, S.J., etal. (2010) Crystal structure of Lon protease: molecular architecture of gated entry to a sequestered degradation chamber. EMBO J 29: 3520-3530.
6. Cheng, I., Mikita, N., Fishovitz, J., Frase, H., Wintrode, P., and Lee, I. (2012) Identification of a region in the N-terminus of Escherichia coli Lon that affects ATPase, substrate translocation and proteolytic activity. J Mol Biol 418: 208-225.
7. Chung, C.H., and Goldberg, A.L. (1981) The product of the lon (capR) gene in Escherichia coli is the ATP-dependent protease, protease La. Proc Natl Acad Sci USA 78: 4931-4935.
8. Coleman, J.L., Katona, L.I., Kuhlow, C., Toledo, A., Okan, N.A., Tokarz, R., etal. (2009) Evidence that two ATP-dependent (Lon) proteases in Borrelia burgdorferi serve different functions. PLoS Pathog 5: e1000676.
9. Cordell, S.C., Robinson, E.J., and Löwe, J. (2003) Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ. Proc Natl Acad Sci USA 100: 7889-7894.
10. Duman, R.E., and Löwe, J. (2010) Crystal structures of Bacillus subtilis Lon protease. J Mol Biol 401: 653-670.
11. Ebel, W., Skinner, M.M., Dierksen, K.P., Scott, J.M., and Trempy, J.E. (1999) A conserved domain in Escherichia coli Lon protease is involved in substrate discriminator activity. J Bacteriol 181: 2236-2243.
12. Fenton, W.A., Kashi, Y., Furtak, K., and Horwich, A.L. (1994) Residues in chaperonin GroEL required for polypeptide binding and release. Nature 371: 614-619.
13. Glynn, S.E., Nager, A.R., Baker, T.A., and Sauer, R.T. (2012) Dynamic and static components power unfolding in topologically closed rings of a AAA+ proteolytic machine. Nat Struct Mol Biol 19: 616-622.
14. Gora, K.G., Cantin, A., Wohlever, M., Joshi, K.K., Perchuk, B.S., Chien, P., etal. (2013) Regulated proteolysis of a transcription factor complex is critical to cell cycle progression in Caulobacter crescentus. Mol Microbiol 87: 1277-1289.
15. Gottesman, S., Halpern, E., and Trisler, P. (1981) Role of sulA and sulB in filamentation by lon mutants of Escherichia coli K-12. J Bacteriol 148: 265-273.
16. Gottesman, S., Roche, E., Zhou, Y., and Sauer, R.T. (1998) The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system. Genes Dev 12: 1338-1347.
17. Gur, E. (2013) The Lon AAA+ protease. Subcell Biochem 66: 35-51.
18. Gur, E., and Sauer, R.T. (2008) Recognition of misfolded proteins by Lon, a AAA(+) protease. Genes Dev 22: 2267-2277.
19. Gur, E., and Sauer, R.T. (2009) Degrons in protein substrates program the speed and operating efficiency of the AAA+ Lon proteolytic machine. Proc Natl Acad Sci USA 106: 18503-18508.
20. Gur, E., Vishkautzan, M., and Sauer, R.T. (2012) Protein unfolding and degradation by the AAA+ Lon protease. Protein Sci 21: 268-278.
21. Higashitani, A., Ishii, Y., Kato, Y., and Koriuchi, K. (1997) Functional dissection of a cell-division inhibitor, SulA, of Escherichia coli and its negative regulation by Lon. Mol Gen Genet 254: 351-357.
22. Hinnerwisch, J., Fenton, W.A., Furtak, K.J., Farr, G.W., and Horwich, A.L. (2005) Loops in the central channel of ClpA chaperone mediate protein binding, unfolding, and translocation. Cell 121: 1029-1041.
23. Hori, O., Ichinoda, F., Tamatani, T., Yamaguchi, A., Sato, N., Ozawa, K., etal. (2002) Transmission of cell stress from endoplasmic reticulum to mitochondria: enhanced expression of Lon protease. J Cell Biol 157: 1151-1160.
24. Ingmer, H., and Brøndsted, L. (2009) Proteases in bacterial pathogenesis. Res Microbiol 160: 704-710.
25. Ishii, Y., and Amano, F. (2001) Regulation of SulA cleavage by Lon protease by the C-terminal amino acid of SulA, histidine. Biochem J 358: 473-480.
26. Kenniston, J.A., Baker, T.A., Fernandez, J.M., and Sauer, R.T. (2003) Linkage between ATP consumption and mechanical unfolding during the protein processing reactions of an AAA+ degradation machine. Cell 114: 511-520.
27. Lee, A.Y., Tsay, S.S., Chen, M.Y., and Wu, S.H. (2004) Identification of a gene encoding Lon protease from Brevibacillus thermoruber WR-249 and biochemical characterization of its thermostable recombinant enzyme. Eur J Biochem 271: 834-844.
28. Li, M., Rasulova, F., Melnikov, E.E., Rotanova, T.V., Gustchina, A., Maurizi, M.R., etal. (2005) Crystal structure of the N-terminal domain of E. coli Lon protease. Protein Sci 14: 2895-2900.
29. Li, M., Gustchina, A., Rasulova, F.S., Melnikov, E.E., Maurizi, M.R., Rotanova, T.V., etal. (2010) Structure of the N-terminal fragment of Escherichia coli Lon protease. Acta Crystallogr D Biol Crystallogr 66: 865-873.
30. Löwe, J., van den Ent, F., and Amos, L.A. (2004) Molecules of the bacterial cytoskeleton. Annu Rev Biophys Biomol Struct 33: 177-198.
31. Luce, K., and Osiewacz, H.D. (2009) Increasing organismal healthspan by enhancing mitochondrial protein quality control. Nat Cell Biol 11: 852-858.
32. Martin, A., Baker, T.A., and Sauer, R.T. (2008a) Protein unfolding by a AAA+ protease is dependent on ATP-hydrolysis rates and substrate energy landscapes. Nat Struct Mol Biol 15: 139-145.
33. Martin, A., Baker, T.A., and Sauer, R.T. (2008b) Pore loops of the AAA+ ClpX machine grip substrates to drive translocation and unfolding. Nat Struct Mol Biol 15: 1147-1151.
34. Melnikov, E.E., Andrianova, A.G., Morozkin, A.D., Stepnov, A.A., Makhovskaya, O.V., Botos, I., etal. (2008) Limited proteolysis of E. coli ATP-dependent protease Lon - a unified view of the subunit architecture and characterization of isolated enzyme fragments. Acta Biochim Pol 55: 281-296.
35. Nager, A.R., Baker, T.A., and Sauer, R.T. (2011) Stepwise unfolding of a β barrel protein by the AAA+ ClpXP protease. J Mol Biol 413: 4-16.
36. Park, E., Rho, Y.M., Koh, O.J., Ahn, S.W., Seong, I.S., Song, J.J., etal. (2005) Role of the GYVG pore motif of HslU ATPase in protein unfolding and translocation for degradation by HslV peptidase. J Biol Chem 280: 22892-22898.
37. Rep, M., van Dijl, J.M., Suda, K., Schatz, G., Grivell, L.A., and Suzuki, C.K. (1996) Promotion of mitochondrial membrane complex assembly by a proteolytically inactive yeast Lon. Science 274: 103-106.
38. Robertson, G.T., Kovach, M.E., Allen, C.A., Ficht, T.A., and Roop, R.M. (2000) The Brucella abortus Lon functions as a generalized stress response protease and is required for wild-type virulence in BALB/c mice. Mol Microbiol 35: 577-588.
39. Rosen, R., Biran, D., Gur, E., Becher, D., Hecker, M., and Ron, E.Z. (2002) Protein aggregation in Escherichia coli: role of proteases. FEMS Microbiol Lett 207: 9-12.
40. Roudiak, S.G., and Shrader, T.E. (1998) Functional role of the N-terminal region of the Lon protease from Mycobacterium smegmatis. Biochemistry 37: 11255-11263.
41. Rudyak, S.G., and Shrader, T.E. (2000) Polypeptide stimulators of the Ms-Lon protease. Protein Sci 9: 1810-1817.
42. Sauer, R.T., and Baker, T.A. (2011) AAA+ proteases: ATP-fueled machines of protein destruction. Annu Rev Biochem 80: 587-612.
43. Siddiqui, S.M., Sauer, R.T., and Baker, T.A. (2004) Role of the processing pore of the ClpX AAA+ ATPase in the recognition and engagement of specific protein substrates. Genes Dev 18: 369-374.
44. Stinson, B.M., Nager, A.R., Glynn, S.E., Schmitz, K.R., Baker, T.A., and Sauer, R.T. (2013) Nucleotide binding and conformational switching in the hexameric ring of a AAA+ machine. Cell 153: 628-639.
45. Tomoyasu, T., Mogk, A., Langen, H., Goloubinoff, P., and Bukau, B. (2001) Genetic dissection of the roles of chaperones and proteases in protein folding and degradation in the Escherichia coli cytosol. Mol Microbiol 40: 397-413.
46. Vabulas, R.M., Raychaudhuri, S., Hayer-Hartl, M., and Hartl, F.U. (2010) Protein folding in the cytoplasm and the heat shock response. Cold Spring Harb Perspect Biol 2: 1-18.
47. Van Melderen, L., and Gottesman, S. (1999) Substrate sequestration by a proteolytically inactive Lon mutant. Proc Natl Acad Sci USA 96: 6064-6071.
48. Vieux, E.F., Wohlever, M.L., Chen, J.Z., Sauer, R.T., and Baker, T.A. (2013) Distinct quaternary structures of the AAA+ Lon protease control substrate degradation. Proc Natl Acad Sci USA 110: E2002-E2008.
49. Wohlever, M.L., Nager, A.R., Baker, T.A., and Sauer, R.T. (2013) Engineering fluorescent protein substrates for the AAA+ Lon protease. Protein Eng Des Sel 26: 299-305.
50. Wright, R., Stephens, C., Zweiger, G., Shapiro, L., and Alley, M.R. (1996) Caulobacter Lon protease has a critical role in cell-cycle control of DNA methylation. Genes Dev 10: 1532-1542.