The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein

Plant Cell

Volumn 12, Issue 3, 2000, Pages 419-431

  Lindahl, Marika ^a   Spetea, Cornelia ^b,c   Hundal, Torill ^b,c   Oppenheim, Amos B ^a   Adam, Zach ^a   Andersson, Bertil ^b,c  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c LINKÖPING UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ESCHERICHIA COLI;

EID: 0034031132     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.12.3.419     Document Type: Article

References (55)

1. Adam, Z. (1996). Protein stability and degradation in chloroplasts. Plant Mol. Biol. 32, 773-783.
2. 0 sector is a substrate of the FtsH protease in Escherichia coll. FEBS Lett. 399, 26-28.
3. Akiyama, Y., Kihara, A., Tokuda, H., and Ito, K. (1996b). FtsH (HfIB) is an ATP-dependent protease selectively acting on SecY and some other membrane proteins. J. Biol. Chem. 271, 31196-31201.
4. Andersson, B., and Aro, E.-M. (1997). Proteolytic activities and proteases of plant chloroplasts. Physiol. Plant. 100, 780-793.
5. Andersson, B., and Barber, J. (1994). Composition, organization and dynamics of thylakoid membranes. In Advances in Molecular and Cell Biology, E.E. Bittar, ed (Greenwich, UK: Jai Press Inc.), pp. 1-53.
6. Andersson, B., Åkerlund, H.E., and Albertsson, P.Å. (1976). Separation of subchloroplast membrane particles by counter-current distribution. Biochim. Biophys. Acta 423, 122-132.
7. Arlt, H., Tauer, R., Feldmann, H., Neupert, W., and Langer, T. (1996). The YTA10-12 complex, an AAA protease with chaperone-like activity in the inner membrane of mitochondria. Cell 85, 875-885.
8. Aro, E.-M., Virgin, I., and Andersson, B. (1993). Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta 1143, 113-134.
9. Barber, J., and Andersson, B. (1992). Too much of a good thing: Light can be bad for photosynthesis. Trends Biochem. Sci. 17, 61-66.
10. Clarke, A.K. (1999). ATP-dependent Clp proteases in photosynthetic organisms - A cut above the rest! Ann. Bot. 83, 593-599.
11. de Las Rivas, J., Shipton, C.A., Ponticos, M., and Barber, J. (1993). Acceptor side mechanism of photoinduced proteolysis of the D1 protein in photosystem II reaction centers. Biochemistry 32, 6944-6950.
12. Gottesman, S. (1996). Proteases and their targets in Escherichia coll. Annu. Rev. Genet. 30, 465-506.
13. Greenberg, B.M., Gaba, V., Mattoo, A.K., and Edelman, M. (1987). Identification of a primary in vivo degradation product of the rapidly turning-over 32 KD protein of photosystem II. EMBO J. 6, 2865-2869.
14. Guelin, E., Rep, M., and Grivell, L.A. (1996). Afg3p, a mitochondrial ATP-dependent metalloprotease, is involved in degradation of mitochondrially-encoded Cox1, Cox3, Cob, Su6, Su8 and Su9 subunits of the inner membrane complexes III, IV and V. FEBS Lett. 381, 42-46.
15. Hankamer, B., Morris, E.P., and Barber, J. (1999). Revealing the structure of the oxygen-evolving core dimer of photosystem II by cryoelectron crystallography. Nat. Struct. Biol. 6, 560-564.
16. 32, the heat shock regulator in Escherichia coli, is governed by HflB. Proc. Natl. Acad. Sci. USA 92, 3516-3520.
17. Herman, C., Thevenet, 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.
18. Hideg, E., Kalai, T., Hideg, K., and Vass, I. (1998). Photoinhibition of photosynthesis in vivo results in singlet oxygen production detection via nitroxide-induced fluorescence quenching in broad bean leaves. Biochemistry 37, 11405-11411.
19. 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. USA 95, 12135-12140.
20. Itzhaki, H., Naveh, L., Lindahl, M., Cook, M., and Adam, Z. (1998). Identification and characterization of DegP, a serine protease associated with the luminal side of the thylakoid membrane. J. Biol. Chem. 273, 7094-7098.
21. Jansen, M.A., Depka, B., Trebst, A., and Edelman, M. (1993). Engagement of specific sites in the plastoquinone niche regulates degradation of the D1 protein in photosystem II. J. Biol. Chem. 268, 21246-21252.
22. Keiler, K.C., Waller, P.R.H., and Sauer, R.T. (1996). Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271, 990-993.
23. 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.
24. 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.
25. Kihara, A., Akiyama, Y., and Ito, K. (1998). Different pathways for protein degradation by the FtsH/HflKC membrane-embedded protease complex: An implication from the interference by a mutant form of a new substrate protein, YccA. J. Mol. Biol. 279, 175-188.
26. Kihara, A., Akiyama, Y., and Ito, K. (1999). Dislocation of membrane proteins in FtsH-mediated proteolysis. EMBO J. 18, 2970-2981.
27. Kyle, D.J., Ohad, I., and Arntzen, C.J. (1984). Membrane protein damage and repair: Selective loss of a quinone-protein function in chloroplast membranes. Proc. Natl. Acad. Sci. USA 81, 4070-4074.
28. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
29. Leonhard, K., Herrmann, J.M., Stuart, R.A., Mannhaupt, G., Neupert, W., and Langer, T. (1996). AAA proteases with catalytic sites on opposite membrane surfaces comprise a proteolytic system for the ATP-dependent degradation of inner membrane proteins in mitochondria. EMBO J. 15, 4218-4229.
30. Leonhard, K., Stiegler, A., Neupert, W., and Langer, T. (1999). Chaperone-like activity of the AAA domain of the yeast Yme1 AAA protease. Nature 398, 348-351.
31. Levchenko, I., Smith, C.K., Walsh, N.P., Sauer, R.T., and Baker, T.A. (1997). PDZ-like domains mediate binding specificity in the Clp/Hsp100 family of chaperones and protease regulatory subunits. Cell 91, 939-947.
32. Lindahl, M., Tabak, S., Cseke, L., Pichersky, E., Andersson, B., and Adam, Z. (1996). Identification, characterization, and molecular cloning of a homologue of the bacterial FtsH protease in chloroplasts of higher plants. J. Biol. Chem. 271, 29329-29334.
33. Mattoo, A.K., Hoffman-Falk, H., Marder, J.B., and Edelman, M. (1984). Regulation of protein metabolism: Coupling of photosynthetic electron transport to in vivo degradation of the rapidly metabolized 32-kilodalton protein of the chloroplast membranes. Proc. Natl. Acad. Sci. USA 81, 1380-1384.
34. Melis, A. (1999). Photosystem-II damage and repair cycle in chloroplasts: What modulates the rate of photodamage? Trends Plant Sci. 4, 130-135.
35. Nakai, T., Yasuhara, T., Fujiki, Y., and Ohashi, A. (1995). Multiple genes, including a member of the AAA family, are essential for degradation of unassembled subunit 2 of cytochrome c oxidase in yeast mitochondria. Mol. Cell. Biol. 15, 4441-4452.
36. Nakajima, Y., Yoshida, S., Inoue, Y., and Ono, T. (1996). Occupation of the Q(B)-binding pocket by a photosystem II inhibitor triggers dark cleavage of the D1 protein subjected to brief preillumination. J. Biol. Chem. 271, 17383-17389.
37. B-protein in isolated pea thylakoids. EMBO J. 4, 1655-1659.
38. Ostersetzer, O., and Adam, Z. (1997). Light-stimulated degradation of an unassembled Rieske FeS protein by a thylakoid-bound protease: The possible role of the FtsH protease. Plant Cell 9, 957-965.
39. Pajic, A., Tauer, R., Feldmann, H., Neupert, W., and Langer, T. (1994). Yta10p is required for the ATP-dependent degradation of polypeptides in the inner membrane of mitochondria. FEBS Lett. 353, 201-206.
40. Prasil, O., Adir, N., and Ohad, I. (1992). Dynamics of photosystem II: Mechanism of photoinhibition and recovery processes. In Topics in Photosynthesis (Amsterdam: Elsevier Science Publishers), pp. 295-348.
41. Rhee, K.H., Morris, E.P., Barber, J., and Kuhlbrandt, W. (1998). Three-dimensional structure of the plant photosystem II reaction centre at 8 A resolution. Nature 396, 283-286.
42. Roobol-Boza, M., and Andersson, B. (1996). Isolation of hydrophobic membrane proteins by perfusion chromatography-Purification of photosystem II reaction centers from spinach chloroplasts. Anal. Biochem. 235, 127-133.
43. Salter, A.H., Virgin, I., Hagman, A., and Andersson, B. (1992). On the molecular mechanism of light-induced D1 protein degradation in PSII core particles. Biochemistry 31, 3990-3998.
44. Shanklin, J., Dewitt, N.D., and Flanagan, J.M. (1995). The stroma of higher plant plastids contain ClpP and ClpC, functional homologs of Escherichia coli ClpP and ClpA: An archetypal two-component ATP-dependent protease. Plant Cell 7, 1713-1722.
45. Shipton, C.A., and Barber, J. (1994). In vivo and in vitro photoinhibition reactions generate similar degradation fragments of D1 and D2 photosystem-II reaction-centre proteins. Eur. J. Biochem. 220, 801-808.
46. Shetland, Y., Koby, S., Teff, D., Mansur, N., Oren, O.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.
47. Sokolenko, A., Lerbs-Mache, S., Altschmied, L., and Herrmann, R.G. (1998). Clp protease complexes and their diversity in chloroplasts. Planta 207, 286-295.
48. Spetea, C., Hundal, T., Lohmann, F., and Andersson, B. (1999). GTP bound to the chloroplast thylakoid membranes is required for light-induced multi-enzyme degradation of photosystem II D1 protein. Proc. Natl. Acad. Sci. USA 96, 6547-6552.
49. Telfer, A., Bishop, S.M., Phillips, D., and Barber, J. (1994). Isolated photosynthetic reaction center of photosystem II as a sensitizer for the formation of singlet oxygen. Detection and quantum yield determination using a chemical trapping technique. J. Biol. Chem. 269, 13244-13253.
50. Tomoyasu, T., Yamanaka, K., Murata, K., Suzaki, T., Bouloc, P., Kato, A., Niki, H., Hiraga, S., and Ogura, T. (1993a). Topology and subcellular localization of FtsH protein in Escherichia coll. J. Bacteriol. 175, 1352-1357.
51. Tomoyasu, T., Yuki, T., Morimura, S., Mori, H., Yamanaka, K., Niki, H., Hiraga, S., and Ogura, T. (1993b). 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.
52. 32. EMBO J. 14, 2551-2560.
53. van Wijk, K.J., Roobol-Boza, M., Kettunen, R., Andersson, B., and Aro, E.-M. (1997). Synthesis and assembly of the D1 protein into photosystem II: Processing of the C terminus and identification of the initial assembly partners and complexes during photosystem II repair. Biochemistry 36, 6178-6186.
54. A species promote chlorophyll triplet formation. Proc. Natl. Acad. Sci. USA 89, 1408-1412.
55. Zer, H., Prasil, O., and Ohad, I. (1994). Role of plastoquinol oxidoreduction in regulation of photochemical reaction center II D1 protein turnover in vivo. J. Biol. Chem. 269, 17670-17676.