Correlation of an adenine-specific conformational change with the ATP-dependent peptidase activity of Escherichia coli Lon

Biochemistry

Volumn 43, Issue 23, 2004, Pages 7432-7442

  Patterson, Jessica ^a   Vineyard, Diana ^a   Thomas Wohlever, Jennifer ^a   Behshad, Ramona ^a   Burke, Morris ^b   Lee, Irene ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINETRIPHOSPHATE; CONFORMATIONS; ESCHERICHIA COLI; HYDROLYSIS; REACTION KINETICS; SENSORS;

CONFORMATIONAL CHANGES; NUCLEOTIDES; TRYPTIC DIGESTION;

BIOCHEMISTRY;

ADENINE; ADENINE NUCLEOTIDE DERIVATIVE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; ATP DEPENDENT PEPTIDASE; BACTERIAL PROTEIN; CYTIDINE TRIPHOSPHATE; ENDOPEPTIDASE LA; GUANOSINE TRIPHOSPHATE; PEPTIDASE; PEPTIDE; PEPTIDE FRAGMENT; PURINE DERIVATIVE; PYRIMIDINE DERIVATIVE; SERINE PROTEINASE; UNCLASSIFIED DRUG; URIDINE TRIPHOSPHATE;

ARTICLE; BINDING AFFINITY; BINDING SITE; CATALYSIS; CHEMICAL REACTION KINETICS; CONFORMATIONAL TRANSITION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ESCHERICHIA COLI; HYDROLYSIS; NONHUMAN; NUCLEOTIDE METABOLISM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN STRUCTURE;

ADENINE; AMINO ACID SEQUENCE; ATP-DEPENDENT PROTEASES; BINDING SITES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HEAT-SHOCK PROTEINS; KINETICS; MOLECULAR SEQUENCE DATA; NUCLEOSIDE-TRIPHOSPHATASE; NUCLEOTIDES; PEPTIDE FRAGMENTS; PEPTIDES; PROTEASE LA; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; SERINE ENDOPEPTIDASES; TRYPSIN;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; FELIS CATUS;

EID: 2942614922     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi036165c     Document Type: Article

References (42)

1. 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. U.S.A. 78, 4931-4935.
2. Gottesman, S., Gottesman, M. E., Shaw, J. E., and Pearson, M. L. (1981) Protein degradation in E. coli: the lon mutation and bacteriophage lambda N and cll protein stability, Cell. 24, 225-233.
3. Goldberg, A. L., Moerschell, R. P., Chung, C. H., and Maurizi, M. R. (1994) ATP-dependent protease La (lon) from Escherichia coli, Methods Enzymol. 244, 350-375.
4. Gottesman, S., Maurizi, M. R. (1992) Regulation by Proteolysis: Enegry-Dependent Proteases and Their Targets, Microbiol. Rev. 56, 592-621.
5. Gottesman, S. (1996) Proteases and their targets in Escherichia coli, Annu. Rev. Genet. 30, 465-506.
6. Maurizi, M. R. (1992) Proteases and protein degradation in Escherichia coli, Experientia 48, 178-201.
7. Charrette, M., Henderson, G. W., and Markovitz, A. (1981) ATP hydrolysis-dependent activity of the lon (capR) protein of E. coli K12, Proc. Natl. Acad. Sci. U.S.A. 78, 4728-4732.
8. Schoemaker, J. M., Gayda, R. C., Markovitz, A. (1984) Regulation of cell division in Escherichia coli: SOS induction and cellular location of the sulA protein, a key to lon-associated filamentation and death, J. Bacteriol. 158, 551-561.
9. Goff, S. A., and Goldberg, A. L. (1985) Production of abnormal proteins in E. coli stimulates transcription of lon and other heat shock genes, Cell 41, 587-595.
10. Chin, D. T., Goff, S. A., Webster, T., Smith, T., and Goldberg, A. L. (1988) Sequence of the lon gene in Escherichia coli. A heat-shock gene which encodes the ATP-dependent protease La, J. Biol. Chem. 263, 11718-11728.
11. Amerik, A., Chistiakov, L. G., Ostroumova, N. I., Gurevich, A. I., and Antonov, V. K. (1988) [Cloning, expression and structure of the functionally active shortened lon gene in Escherichia coli], Bioorg. Khim. 14, 408-411.
12. Botos, I., Melnikov, E. E., Cherry, S., Tropea, J. E., Khalatova, A. G., Rasulova, F., Dauter, Z., Maurizi, M. R., Rotanova, T. V., Wlodawer, A., and Gustchina, A. (2004) The catalytic domain of Escherichia coli Lon protease has a unique fold and a Ser-Lys dyad in the active site, J. Biol. Chem. 279, 8140-8148.
13. Botos, I., Melnikov, E. E., Cherry, S., Tropea, J. E., Khalatova, A. G., Rasulova, F., Dauter, Z., Maurizi, M. R., Rotanova, T. V., Wlodawer, A., and Gustchina, A. (2004) J. Struct. Biol. 146, 113-122.
14. Rohrwild, M., Coux, O., Huang, H. C., Moerschell, R. P., Yoo, S. J., Seol, J. H., Chung, C. H., and Goldberg, A. L. (1996) HslV-HslU: A novel ATP-dependent protease complex in Escherichia coli related to the eukaryotic proteasome, Proc. Natl. Acad. Sci. U.S.A. 93, 5808-5813.
15. Rohrwild, M., Pfeifer, G., Santarius, U., Muller, S. A., Huang, H. C., Engel, A., Baumeister, W., and Goldberg, A. L. (1997) The ATP-dependent HslVU protease from Escherichia coli is a four-ring structure resembling the proteasome, Nat. Struct. Biol. 4, 133-139.
16. Goldberg, A. L., Akopian, T. N., Kisselev, A. F., Lee, D. H., Rohrwild, M. (1997) New insights into the mechanisms and importance of the proteasome in intracellular protein degradation, Biol. Chem. 378, 131-140.
17. Yoo, S. J., Seol, J. H., Shin, D. H., Rohrwild, M., Kang, M. S., Tanaka, K., Goldberg, A. L., and Chung, C. H. (1996) Purification and characterization of the heat shock proteins HslV and HslU that form a new ATP-dependent protease in Escherichia coli, J. Biol. Chem. 271, 14035-14040.
18. 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.
19. Reid, B. G., Fenton, W. A., Horwich, A. L., and Weber-Ban, E. U. (2001) ClpA mediates directional translocation of substrate proteins into the ClpP protease, Proc. Natl. Acad. Sci. U.S.A. 98, 3768-3772.
20. Ishikawa, T., Beuron, F., Kessel, M., Wickner, S., Maurizi, M. R., and Steven, A. C. (2001) Translocation pathway of protein substrates in ClpAP protease, Proc. Natl. Acad. Sci. U.S.A. 98, 4328-4333.
21. Neuwald, A. F., Aravind, L., Spouge, J. L., and Koonin, E. V. (1999) AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes, Genome Res. 9, 27-43.
22. Ogura, T., and Wilkinson, A. J. (2001) AAA+ superfamily ATPases: common structure-diverse function, Genes Cells 6, 575-597.
23. Thomas-Wohlever, J., and Lee, I. (2002) Kinetic characterization of the peptidase activity of Escherichia coli Lon reveals the mechanistic similarities in ATP-dependent hydrolysis of peptide and protein substrates, Biochemistry 41, 9418-9425.
24. Lee, I., and Berdis, A. J. (2001) Adenosine triphosphate-dependent degradation of a fluorescent lambda N substrate mimic by Lon protease, Anal. Biochem. 291, 74-83.
25. Hoskins, J. R., Pak, M., Maurizi, M. R., and Wickner, S. (1998) The role of the ClpA chaperone in proteolysis by ClpAP, Proc. Natl. Acad. Sci. U.S.A. 95, 12135-12140.
26. Reid, B. G., Fenton, W. A., Horwich, A. L., Weber-Ban, E. U. (2001) ClpA mediates directional translocation of substrate proteins into the ClpP protease, Proc. Natl. Acad. Sci. U.S.A. 98, 3768-3772.
27. Wang, J., Song, J. J., Seong, I. S., Franklin, M. C., Kamtekar, S., Eom, S. H., and Chung, C. H. (2001) Nucleotide-dependent conformational changes in a protease-associated ATPase HslU, Structure 9, 1107-1116.
28. Gilbert, S. P., and Mackey, A. T. (2000) Kinetics: a tool to study molecular motors, Methods 22, 337-354.
29. Lanzetta, P. A., Alvarez, L. J., Reinach, P. S., and Candia, O. A. (1979) An improved assay for nanomole amounts of inorganic phosphate, Anal. Biochem. 100, 95-97.
30. Copeland, R. A. (1996) Enzymes. A practical introduction to structure, mechanism and data analysis, VCH Publishers, New York.
31. Menon, A. S., and Goldberg, A. L. (1987) Protein substrates activate the ATP-dependent protease La by promoting nucleotide binding and release of bound ADP, J. Biol. Chem. 262, 14929-14934.
32. Menon, A. S., and Goldberg, A. L. (1987) Binding of nucleotides to the ATP-dependent protease La from Escherichia coli, J. Biol. Chem. 262, 14921-14928.
33. Waxman, L., and Goldberg, A. L. (1986) Selectivity of intracellular proteolysis: protein substrates activate the ATP-dependent protease (La), Science 232, 500-503.
34. Waxman, L., and Goldberg, A. L. (1982) Protease La from Escherichia coli hydrolyzes ATP and proteins in a linked fashion, Proc. Natl. Acad. Sci. U.S.A. 79, 4883-4887.
35. Vasilyeva, O. V., Kolygo, K. B., Leonova, Y. F., Potapenko, N. A., and Ovchinnikova, T. V. (2002) Domain structure and ATP-induced conformational changes in Escherichia coli protease Lon revealed by limited proteolysis and autolysis, FEBS Lett. 526, 66-70.
36. Smith, C. K., Baker, T. A., and Sauer, R. T. (1999) Lon and Clp family proteases and chaperones share homologous substrate-recognition domains, Proc. Natl. Acad. Sci. U.S.A. 96, 6678-6682.
37. Wickner, S., and Maurizi, M. R. (1999) Here's the hook: similar substrate binding sites in the chaperone domains of Clp and Lon, Proc. Natl. Acad. Sci. U.S.A. 96, 8318-8320.
38. Bochtler, M., Hartmann, C., Song, H. K., Bourenkov, G. P., Bartunik, H. D., and Huber, R. (2000) The structures of HslU and the ATP-dependent protease HslU-HslV, Nature 403, 800-805.
39. Wang, J., Song, J. J., Franklin, M. C., Kamtekar, S., Im, Y. J., Rho, S. H., Seong, I. S., Lee, C. S., Chung, C. H., and Eom, S. H. (2001) Crystal structures of the HslVU peptidase-ATPase complex reveal an ATP-dependent proteolysis mechanism, Structure 9, 177-184.
40. Sousa, M. C., Trame, C. B., Tsuruta, H., Wilbanks, S. M., Reddy, V. S., and McKay, D. B. (2000) Crystal and solution structures of an HslUV protease-chaperone complex, Cell 103, 633-643.
41. Pate, E., Franks-Skiba, K., White, H., and Cooke, R. (1993) The use of differing nucleotides to investigate cross-bridge kinetics, J. Biol. Chem. 268, 10046-10053.
42. Park, S., Ajtai, K., and Burghardt, T. P. (1997) Mechanism for Coupling Free Energy in ATPase to the Myosin Active Site, Biochemistry 36, 3368-3372.