FtsH recognizes proteins with unfolded structure and hydrolyzes the carboxyl side of hydrophobic residues

Journal of Biochemistry

Volumn 127, Issue 5, 2000, Pages 931-937

  Asahara, Yuko ^a   Atsuta, Kyoko ^a   Motohashi, Ken ^a,c   Taguchi, Hideki ^a   Yohda, Masafumi ^b   Yoshida, Masasuke ^a  

^a TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^b TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

Author keywords

ATP; Chymotrypsin like activity; FtsH; Progressive degradation; Unfolded structure; Zn2+ dependent protease

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; ALPHA LACTALBUMIN; BACTERIAL ENZYME; CASEIN; CHYMOTRYPSIN; PEPSIN A; PROTEINASE; ZINC;

ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVITY; ESCHERICHIA COLI; HYDROPHOBICITY; MOLECULAR CLONING; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTEIN STRUCTURE; THERMUS THERMOPHILUS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PROKARYOTA; THERMUS THERMOPHILUS;

EID: 0034079766     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.jbchem.a022689     Document Type: Article

References (46)

1. Suzuki, C.K., Rep, M., van Dijl, J.M., Suda, K., Grivell, L.A., and Schatz, G. (1997) ATP-dependent proteases that also chaperone protein biogenesis. Trends. Biochem. Sci. 22, 118-123
2. Gottesman, S. (1996) Proteases and their targets in Escherichia coli. Annu. Rev. Genet. 30, 465-506
3. Herman, C., Ogura, T., Tomoyasu, T., Hiraga, S., Akiyama, Y., Ito, K., Thomas, R., D'Ari, R., and Bouloc, P. (1993) Cell growth and lambda phage development controlled by the same essential Escherichia coli gene, ftsH/hflB. Proc. Natl. Acad. Sci. USA 90, 10861-10865
4. Akiyama, Y., Ogura, T., and Ito, K. (1994) Involvement of FtsH in protein assembly into and through the membrane. I. Mutations that reduce retention efficiency of a cytoplasmic reporter. J. Biol. Chem. 269, 5218-5224
5. Tomoyasu, T., Yuki, T., Morimura, S., Mori, H., Yamanaka, K., Niki, H., Hiraga, S., and Ogura, T. (1993) The Escherichia coli FtsH protein is a prokaryotic member of a protein family of putative ATPases involved in membrane functions, cell cycle control, and gene expression. J. Bacteriol. 175, 1344-1351
6. Tomoyasu, T., Yamanaka, K., Murata, K., Suzaki, T., Bouloc, P., Kato, A., Niki, H., Hiraga, S., and Ogura, T. (1993) Topology and subcellular localization of FtsH protein in Escherichia coli. J. Bacteriol. 175, 1352-1357
7. Akiyama, Y., Yoshihisa, T., and Ito, K. (1995) FtsH, a membrane-bound ATPase, forms a complex in the cytoplasmic membrane of Escherichia coli. J .Biol. Chem. 270, 23485-23490
8. Kihara, A., Akiyama, Y., and Ito, K. (1997) Host regulation of lysogenic decision in bacteriophage lambda: transmembrane modulation of FtsH (HflB), the cII degrading protease, by HflKC (HflA). Proc. Natl. Acad. Sci. USA 94, 5544-5549
9. Kihara, A., Akiyama, Y., and Ito, K. (1996) A protease complex in the Escherichia coli plasma membrane: HflKC (HflA) forms a complex with FtsH (HflB), regulating its proteolytic activity against SecY. EMBO J. 15, 6122-6131
10. Kihara, A., Akiyama, Y., and Ito, K. (1995) FtsH is required for proteolytic elimination of uncomplexed forms of SecY, an essential protein translocase subunit. Proc. Natl. Acad. Sci USA 92 4532-4536
11. Akiyama, Y., Kihara, A., and Ito, K. (1996) Subunit a of proton ATPase Fo sector is a substrate of the FtsH protease in Escherichia coli. FEBS Lett. 399, 26-28
12. Akiyama, Y., Kihara, A., Tokuda, H., and Ito, K. (1996) FtsH (HflB) is an ATP-dependent protease selectively acting on SecY and some other membrane proteins. J. Biol. Chem 271, 31196-31201
13. Tomoyasu, T., Gamer, J., Bukau, B., Kanemori, M., Mori, H., Rutman, A.J., Oppenheim, A.B., Yura, T., Yamanaka, K., Niki, H., Hiraga, S., and Ogura, T. (1995) Escherichia coli FtsH is a membrane-bound, ATP-dependent protease which degrades the heat-shock transcription factor sigma 32. EMBO J. 14, 2551-2560
14. Tatsuta, T., Tomoyasu, T., Bukau, B., Kitagawa, M., Mori, H., Karata, K., and Ogura, T. (1998) Heat shock regulation in the ftsH null mutant of Escherichia coli: dissection of stability and activity control mechanisms of sigma32 in vivo. Mol. Microbiol. 30, 583-593
15. Herman, C., Thevenet, D., D'An, R., and Bouloc, P. (1995) Degradation of sigma 32, the heat shock regulator in Escherichia coli, is governed by HflB. Proc. Natl. Acad. Sci. USA 92, 3516-3520
16. Banuett, F., Hoyt, M.A., McFarlane, L., Echols, H., and Herskowitz, I. (1986) hflB, a new Escherichia coli locus regulating lysogeny and the level of bacteriophage lambda ell protein J. Mol. Biol. 187, 213-224
17. Shetland, Y., Koby, S., Teff, D., Mansur, N., Oren, D.A., Tatematsu, K., Tomoyasu, T., Kessel, M., Bukau, B., Ogura, T. and Oppenheim, A.B. (1997) Proteolysis of the phage lambda CII regulatory protein by FtsH (HflB) of Escherichia coli. Mol. Microbiol. 24, 1303-1310
18. Ogura, T., Inoue, K., Tatsuta, T., Suzaki, T., Karata, K., Young, K., Su, L.H., Fierke, C.A., Jackman, J.E., Raetz, C.R., Coleman, J., Tomoyasu, T., and Matsuzawa, H. (1999) Balanced biosynthesis of major membrane components through regulated degradation of the committed enzyme of lipid A biosynthesis by the AAA protease FtsH (HflB) in Escherichia coli. Mol. Microbiol. 31, 833-844
19. Kihara, A., Akiyama, Y., and Ito, K. (1999) Dislocation of membrane proteins in FtsH-mediated proteolysis. EMBO J. 18 2970-2981
20. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual pp. 1339-1341, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
21. Amada, K., Yohda, M., Odaka, M., Endo, I., Ishii, N., Taguchi, H., and Yoshida, M. (1995) Molecular cloning, expression, and characterization of chaperonin-60 and chaperonin-10 from a thermophilic bacterium, Thermus thermophilus HB8. J. Biochem. 118, 347-354
22. Motohashi, K., Yohda, M., Endo, I., and Yoshida, M. (1996) A novel factor required for the assembly of the DnaK and DnaJ chaperones of Thermus thermophilus. J. Biol. Chem. 271, 17343-17348
23. Kunkel, T.A., Bebenek, K., and McClary, J. (1991) Efficient site-directed mutagenesis using uracil-containing DNA. Methods Enzymol. 204, 125-139
24. Geladopoulos, T.P., Sotiroudis, T.G., and Evangelopoulos, A.E. (1991) A malachite green colorimetric assay for protein phosphatase activity. Anal. Biochem. 192, 112-116
25. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
26. Yamada, T., Akutsu, N., Miyazaki, K., Kakinuma, K., Yoshida, M., and Oshima, T. (1990) Purification, catalytic properties, and thermal stability of threo-Ds-3-isopropylmalate dehydrogenase coded by leuB gene from an extreme thermophile, Thermus thermophilus strain HB8. J. Biochem. 108, 449-456
27. Motohashi, K., Taguchi, H., Ishii, N., and Yoshida, M. (1994) Isolation of the stable hexameric DnaK·DnaJ complex from Thermus thermophilus. J. Biol. Chem. 269, 27074-27079
28. + is an indispensable cofactor for GrpE stimulation of ATPase activity of DnaK X DnaJ complex from Thermus thermophilus FEBS Lett. 412, 633-636
29. Walker, J.E., Saraste, M., Runswick, M.J., and Gay, N.J. (1982) Distantly related sequences in the α-and β-subunits of ATP synthase, myosin, kinases, and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1, 945-951
30. Swaffield, J.C., Bromberg, J.F., and Johnston, S.A. (1992) Alterations in a yeast protein resembling HIV Tat-binding protein relieve requirement for an acidic activation domain in GAL4 [published erratum appears in Nature (1992) 360, 768]. Nature 357, 698-700
31. Lin, X., Loy, J.A., Sussman, F., and Tang, J. (1993) Conformational instability of the N-and C-terminal lobes of porcine pepsin in neutral and alkaline solutions. Protein Sci. 2, 1383-1390
32. Privalov, P.L., Mateo, P.L., Khechinashvili, N.N., Stepanov, V.M., and Revina, L.P. (1981) Comparative thermodynamic study of pepsinogen and pepsin structure. J. Mol. Biol. 152 445-464
33. Kuwajima, K., Garvey, E.P., Finn, B.E., Matthews, C.R., and Sugai, S. (1989) Transient intermediates in the folding of dihydrofolate reductase as detected by far-ultraviolet circular dichroism spectroscopy. Biochemistry 30, 7693-7703
34. Creighton, T.E. and Ewbank, J.J. (1994) Structural characterization of the disulfide folding intemediates of bovine α-lactalbumin. Biochemistry 32, 3694-3707
35. Okazaki, A., Katsumata, K., and Kuwajima, K. (1997) Hydrogen-exchange kinetics of reduced α-lactalbumin bound to the chaperonin GroEL. J. Biochem. 121, 534-541
36. 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
37. Karata, K., Inagawa, T., Wilkinson, A.J., Tatsuta, T., and Ogura, T. (1999) Dissecting the role of a conserved motif (the second region of homology) in the AAA family of ATPases. Site-directed mutagenesis of the ATP-dependent protease FtsH. J. Biol Chem. 274, 26225-26232
38. Akiyama, Y., Yoshihisa, T., and Ito, K. (1995) FtsH, a membrane-bound ATPase, forms a complex in the cytoplasmic membrane of Escherichia coli. J. Biol. Chem. 270, 23485-23490
39. Herman, C., Thévenet, D., Bouloc, P., Walker, G.C., and D'Ari, R. (1998) Degradation of carboxy-terminal-tagged cytoplasmic proteins by the Escherichia coli protease HflB (FtsH) Genes Dev. 12, 1348-1355
40. Begg, K.J., Tomoyasu, T., Donachie, W.D., Khattar, M., Niki, H., Yamanaka, K., Hiraga, S., and Ogura, T. (1992) Escherichia coli mutant Y16 is a double mutant carrying thermosensitive ftsH and ftsI mutations. J. Bacteriol. 174, 2416-2417
41. Akiyama, Y., Shirai, Y., and Ito, K. (1994) Involvement of FtsH in protein assembly into and through the membrane. II. Dominant mutations affecting FtsH functions. J. Biol. Chem 269, 5225-5229
42. Waxman, L. and Goldberg, A.L. (1985) Protease La, the lon gene product, cleaves specific fluorogenic peptides in an ATP-dependent reaction. J. Biol .Chem. 260, 12022-12028
43. 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. USA 93, 5808-5813
44. Wilk, S. and Orlowski, M. (1983) Evidence that pituitary cation-sensitive neutral endopeptidase is a multicatalytic protease complex. J. Neurochem. 40, 842-849
45. Tanaka, K., Ii, K., Ichihara, A., Waxman, L., and Goldberg, A.L. (1986) A high molecular weight protease in the cytosol of rat liver. 1. Purification, enzymological properties, and tissue distribution. J. Biol. Chem. 261, 15197-15203
46. Akiyama, Y. (1999) Self-processing of FtsH and its implication for the cleavage specificity of this protease. Biochemistry 38, 11693-11699