Regulatory role of cardiolipin in the activity of an ATP-dependent protease, Lon, from Escherichia coli

Journal of Biochemistry

Volumn 149, Issue 5, 2011, Pages 519-527

  Minami, Noriko ^a   Yasuda, Tatsuji ^b   Ishii, Yoshiyuki ^c   Fujimori, Ko ^a   Amano, Fumio ^a  

^a OSAKA MEDICAL COLLEGE   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

AAA+ protein; ATPase; liposome; phospholipid; proteolysis

Indexed keywords

ADENOSINE TRIPHOSPHATE DEPENDENT PROTEINASE; CARDIOLIPIN; ENDOPEPTIDASE LA; LIPOSOME; MAGNESIUM; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLGLYCEROL;

ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME REGULATION; ESCHERICHIA COLI; MEMBRANE COMPONENT; NONHUMAN; PROTEIN DEGRADATION; PROTEIN INTERACTION;

CARDIOLIPINS; CASEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LIPOSOMES; PHOSPHOLIPIDS; PROTEASE LA;

ESCHERICHIA COLI;

EID: 79955438013     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvr036     Document Type: Article

References (39)

1. Charette, M.F., Henderson, G.W., and Markovitz, A. (1981) ATP hydrolysis-dependent protease activity of the lon (capR) protein of Escherichia coli K-12. Proc. Natl Acad. Sci. USA 78, 4728-4732 (Pubitemid 12225553)
2. 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 (Pubitemid 12225595)
3. 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 (Pubitemid 16219428)
4. 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
5. Goldberg, A.L. and Waxman, L. (1985) The role of ATP hydrolysis in the breakdown of proteins and peptides by protease La from Escherichia coli. J. Biol. Chem. 260, 12029-12034 (Pubitemid 16228360)
6. Gottesman, S., Gottesman, M., Shaw, J.E., and Pearson, M.L. (1981) Protein degradation in E. coli: the lon mutation and bacteriophage lambda N and cell protein stability. Cell 24, 225-233 (Pubitemid 11157147)
7. Maurizi, M.R. (1992) Proteases and protein degradation in Escherichia coli. Experientia 48, 178-201
8. Laskowska, E., Kuczynska-Wisnik, D., Skorko-Glonek, J., and Taylor, A. (1996) Degradation by proteases Lon, Clp and HtrA, of Escherichia coli proteins aggregated in vivo by heat shock; HtrA protease action in vivo and in vitro. Mol. Microbiol. 22, 555-571 (Pubitemid 26373839)
9. 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 (Pubitemid 34214798)
10. 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
11. Mizusawa, S. and Gottesman, S. (1983) Protein degradation in Escherichia coli: the lon gene controls the stability of sulA protein. Proc. Natl Acad. Sci. USA 80, 358-362
12. Schoemaker, J.M., Gayda, R.C., and 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 (Pubitemid 14147624)
13. Torres-Cabassa, A.S. and Gottesman, S. (1987) Capsule synthesis in Escherichia coli K-12 is regulated by proteolysis. J. Bacteriol. 169, 981-989 (Pubitemid 17043358)
14. Birghan, C., Mundt, E., and Gorbalenya, A.E. (2000) A non-canonical lon proteinase lacking the ATPase domain employs the ser-Lys catalytic dyad to exercise broad control over the life cycle of a double-stranded RNA virus. EMBO J. 19, 114-123 (Pubitemid 30009231)
15. 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 Lonprotease has a unique fold and a Ser-Lys dyad in the active site. J. Biol. Chem. 279, 8140-8148 (Pubitemid 38294705)
16. Chandu, D. and Nandi, D. (2004) Comparative genomics and functional roles of the ATP-dependent proteases Lon and Clp during cytosolic protein degradation. Res. Microbiol. 155, 710-719 (Pubitemid 39389126)
17. Fischer, H. and Glockshuber, R. (1994) A point mutation within the ATP-binding site inactivates both catalytic functions of the ATP-dependent protease La (Lon) from Escherichia coli. FEBS Lett. 356, 101-103 (Pubitemid 24374041)
18. Lee, A.Y., Hsu, C.H., and Wu, S.H. (2004) Functional domains of Brevibacillus thermoruber lon protease for oligomerization and DNA binding: role of N-terminal and sensor and substrate discrimination domains. J. Biol. Chem. 279, 34903-34912 (Pubitemid 39318126)
19. Rotanova, T.V., Botos, I., Melnikov, E.E., Rasulova, F., Gustchina, A., Maurizi, M.R., and Wlodawer, A. (2006) Slicing a protease: structural features of the ATP-dependent Lon proteases gleaned from investigations of isolated domains. Protein Sci. 15, 1815-1828 (Pubitemid 44141499)
20. Starkova, N.N., Koroleva, E.P., Rumsh, L.D., Ginodman, L.M., and Rotanova, T.V. (1998) Mutations in the proteolytic domain of Escherichia coli protease Lon impair the ATPase activity of the enzyme. FEBS Lett. 422, 218-220 (Pubitemid 28064546)
21. Park, S.C., Jia, B., Yang, J.K., Van, D.L., Shao, Y.G., Han, S.W., Jeon, Y.J., Chung, C. H., and Cheong, G.W. (2006) Oligomeric structure of the ATP-dependent protease La (Lon) of Escherichia coli. Mol. Cells 21, 129-134
22. Chung, C.H. and Goldberg, A.L. (1982) DNA stimulates ATP-dependent proteolysis and protein-dependent ATPase activity of protease La from Escherichia coli. Proc. Natl Acad. Sci. USA 79, 795-799
23. Fu, G.K., Smith, M.J., and Markovitz, D.M. (1997) Bacterial protease Lon is a site-specific DNA-binding protein. J. Biol. Chem. 272, 534-538 (Pubitemid 27021191)
24. Charette, M.F., Henderson, G.W., Doane, L.L., and Markovitz, A. (1984) DNA-stimulated ATPase activity on the lon (CapR) protein. J. Bacteriol. 158, 195-201 (Pubitemid 14127493)
25. Nomura, K., Kato, J., Takiguchi, N., Ohtake, H., and Kuroda, A. (2004) Effects of inorganic polyphosphate on the proteolytic and DNA-binding activities of Lon in Escherichia coli. J. Biol. Chem. 279, 34406-34410 (Pubitemid 39318066)
26. Kuroda, A. (2006) A polyphosphate-lon protease complex in the adaptation of Escherichia coli to amino acid starvation. Biosci. Biotechnol. Biochem. 70, 325-331 (Pubitemid 43289411)
27. Kuroda, A., Nomura, K., Ohtomo, R., Kato, J., Ikeda, T., Takiguchi, N., Ohtake, H., and Kornberg, A. (2001) Role of inorganic polyphosphate in promoting ribosomal protein degradation by the Lon protease in E. coli. Science 293, 705-708 (Pubitemid 32728674)
28. Sonezaki, S., Kondo, A., Oba, T., Ishii, Y., Kato, Y., and Nakayama, H. (1994) Overproduction and purification of Lon protease from Escherichia coli using a maltose-binding protein fusion system. Appl. Microbiol. Biotechnol. 42, 313-318 (Pubitemid 24373912)
29. Sonezaki, S., Okita, K., Oba, T., Ishii, Y., Kondo, A., and Kato, Y. (1995) Protein substrates and heat shock reduce the DNA-binding ability of Escherichia coli Lon protease. Appl. Microbiol. Biotechnol. 44, 484-488 (Pubitemid 26024370)
30. 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 (Pubitemid 32826365)
31. Ishii, Y., Sonezaki, S., Iwasaki, Y., Miyata, Y., Akita, K., Kato, Y., and Amano, F. (2000) Regulatory role of C-terminal residues of SulA in its degradation by Lon protease in Escherichia coli. J. Biochem. 127, 837-844 (Pubitemid 30317908)
32. 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 (Pubitemid 32324526)
33. Maurizi, M.R. (1987) Degradation in vitro of bacteriophage lambda N protein by Lon protease from Escherichia coli. J. Biol. Chem. 262, 2696-2703
34. 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 (Pubitemid 34810016)
35. Haines, T.H. and Dencher, N.A. (2002) Cardiolipin: a proton trap for oxidative phosphorylation. FEBS Lett. 528, 35-39 (Pubitemid 35257995)
36. Ortiz, A., Killian, J.A., Verkleij, A.J., and Wilschut, J. (1999) Membrane fusion and the lamellar-toinverted- hexagonal phase transition in cardiolipin vesicle systems induced by divalent cations. Biophys. J. 77, 2003-2014 (Pubitemid 29463161)
37. Sekimizu, K. and Kornberg, A. (1988) Cardiolipin activation of dnaA protein, the initiation protein of replication in Escherichia coli. J. Biol. Chem. 263, 7131-7135
38. Gold, V.A.M., Robson, A., Bao, H., Romantsov, T., Duong, F., and Collinson, I. (2010) The action of cardiolipin on the bacterial translocon. Proc. Natl Acad. Sci. USA 107, 10044-10049
39. Cerbon, J. and del Carmen Lopez-Sanchez, R. (2003) Diacylglycerol generated during sphingomyelin synthesis is involved in protein kinase C activation and cell proliferation in Madin-Darby canine kidney cells. Biochem. J. 373, 917-924 (Pubitemid 36981102)