JXB Advance Access originally published online on November 15, 2004
Journal of Experimental Botany 2005 56(411):357-363; doi:10.1093/jxb/eri021
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RESEARCH PAPER |
FtsH-mediated repair of the photosystem II complex in response to light stress
1Wolfson Laboratories, Department of Biological Sciences, Imperial College London, S. Kensington campus, London SW7 2AZ, UK
2Laboratory of Photosynthesis, Institute of Microbiology, Academy of Sciences, T
ebo
, Czech Republic
3Institute of Physical Biology, University of South Bohemia, Zamek 136, Nove Hrady, Czech Republic
* To whom correspondence should be addressed. Fax: +44 (0) 20 7594 5267. E-mail: p.nixon{at}imperial.ac.uk
Received 21 May 2004; Accepted 26 August 2004
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Abstract |
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Top
Abstract
IntroductionA common feature of light stress in plants, algae, and cyanobacteria is the light-induced damage to the photosystem II complex (PSII), which catalyses the photosynthetic oxidation of water to molecular oxygen. A repair cycle operates to replace damaged subunits within PSII, in particular, the D1 reaction centre polypeptide, by newly synthesized copies. As yet the molecular details of this physiologically important process remain obscure. A key aspect of the process that has attracted much attention is the identity of the protease or proteases involved in D1 degradation. The results are summarized here of recent mutagenesis experiments that were designed to assess the functional importance of the DegP/HtrA and FtsH protease families in the cyanobacterium Synechocystis sp. PCC 6803. Based on these results and the analysis of Arabidopsis mutants, a general model for PSII repair is suggested in which FtsH complexes alone are able to degrade damaged D1.
Key words: Cyanobacteria, DegP/HtrA proteases, FtsH proteases, light stress, photoinhibition
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Introduction |
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An inevitable side-reaction of oxygenic photosynthesis is the light-induced formation of reactive oxygen species (ROS) during photosynthetic electron transport (Asada, 1999
). Despite the presence of scavenging enzymes, ROS cause damage to a broad spectrum of cellular components including protein, pigment, lipids, and nucleic acid. The chief target in the thylakoid membrane is the photosystem II complex (PSII) which functions as a water:plastoquinone oxidoreductase (Prasil et al., 1992; Aro et al., 1993; Ohad et al., 1994). Damage to PSII is thought to be due mainly to the action of singlet oxygen generated from triplet chlorophyll species formed following charge recombination within PSII. However, the highly oxidizing species generated by PSII to oxidize water can also cause damage. These two processes are sometimes referred to as acceptor- and donor-side mechanisms, respectively (Barber and Andersson, 1992).
Although PSII is composed of over 25 subunits, the reaction centre subunit D1 appears to be the chief site of photodamage in PSII (Kyle et al., 1984; Ohad et al., 1984; reviewed by Aro et al., 1993; Adir et al., 2003). The reason for this is probably due to the fact that D1 plays a key role in binding the CaMn oxygen-evolving complex and the chlorophyll molecules involved in the charge recombination reactions that can form singlet oxygen (Diner and Rappaport, 2002). However, it is increasingly clear that damage is not exclusive to D1 and, depending upon illumination conditions, other PSII subunits are damaged such as D2 and CP43 (Komenda and Masojídek, 1995).
A key feature of D1 that has been recognized since 1974 is its rapid synthesis and degradation in response to light (Bottomley et al., 1974; Eaglesham and Ellis, 1974). This is assumed to reflect a repair cycle that is used to replace a damaged D1 subunit within a damaged PSII complex by a newly synthesized copy (Aro et al., 1993). A remarkable feature of this process is the specificity. Only the damaged subunit is replaced; the rest of the subunits in the complex appear to be recycled. As yet, the molecular details of PSII repair are ill-defined, despite the fact that PSII is considered to represent one of the most vulnerable enzymes in plants to light stress, not only because of its relatively high rates of damage but also because the repair process itself is sensitive to ROS (Nishiyama et al., 2001).
So far most of the understanding of the processes involved in PSII repair has been based upon experimental data obtained from higher plants, mainly from experiments conducted in vitro. However, a variety of recent work suggests that the cyanobacterium Synechocystis sp. PCC 6803 is likely to play an important role in investigating PSII repair, particularly for studies in vivo, and that many of the features could be conserved in the chloroplast. Recent advances in determining the structure of PSII from the related cyanobacterium Thermosynechococcus elongatus have also strengthened the case for using Synechocystis 6803 (Ferreira et al., 2004). In this paper, recent work from our laboratories on the role of FtsH proteases in D1 degradation is summarized and our current working model of PSII repair is described.
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The PSII repair cycle in cyanobacteria |
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Figure 1 presents a hypothetical scheme for PSII repair in cyanobacteria such as Synechocystis. This model is based largely on schemes developed for D1 replacement in the chloroplast (Aro et al., 1993
). The key aspects are (i) photodamage to PSII so that electron transport is impaired, (ii) induction of a conformational change that signals the need to remove the damaged subunit, (iii) monomerization of PSII and partial disassembly of the PSII complex to allow access to the damaged subunit, (iv) degradation of damaged D1 and synchronized replacement by a newly synthesized subunit (Komenda and Barber, 1995), and (v) rebinding of various extrinsic proteins and the light-driven assembly (termed photoactivation) of the CaMn cluster, which can only occur after C-terminal processing of the D1 subunit.
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Probing the role of the DegP/HtrA and FtsH families of protease in D1 degradation in vivo |
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Recently, much interest has focused on the identification of proteases that are involved in the degradation of damaged D1. Based on a variety of studies conducted in vitro, a model has been proposed for chloroplasts in which damaged D1 is removed through the action of two proteases (reviewed by Adam and Clarke, 2002
). DegP2, which is a member of the DegP/HtrA family of serine proteases, is proposed to perform the primary cleavage event within the QB-binding pocket (Haußühl et al., 2001) in a GTP-regulated process (Spetea et al., 1999), after which, the two breakdown products are removed by one or more members of the FtsH protease family (Lindahl et al., 1996, 2000).
In Synechocystis 6803, among the 62 predicted proteases/peptidases (Sokolenko et al., 2002), there are three potential members of the DegP/HtrA family of proteases, termed HtrA (slr1204), HhoA (sll1679), and HhoB (sll 1427). This class of protease possesses the catalytic triad typical of serine proteases and contains PDZ domains involved in binding to the C-terminal region of target proteins. Structurally DegP/HtrA proteases are thought to be hexameric and to form a chamber in which either refolding or proteolysis of protein occurs (reviewed by Clausen et al., 2002). To test the involvement of the DegP/HtrA proteases in PSII repair, a triple mutant has been constructed in which all three genes were insertionally inactivated. Although growth of the mutant is sensitive to high irradiance (Silva et al., 2002), recent pulse-chase analyses and oxygen-evolution assays indicate little effect on PSII repair and D1 turnover (PJ Nixon, unpublished data). These data therefore suggest that these proteases are not crucial for D1 turnover in Synechocystis 6803. Given this it is likely that the involvement of DegP2 in PSII repair in chloroplasts might have occurred after the divergence of cyanobacteria and chloroplasts. Importantly, though, PSII repair has not so far been examined in a degP2 mutant in vivo, so it remains unclear how relevant the DegP2 pathway is for D1 cleavage in planta.
The FtsH proteases are membrane-bound, and contain an AAA+ module (ATPase associated with various cellular activities) and a Zn2+-binding site which catalyses proteolysis (Fig. 2A) (Ogura et al., 1991). The C-terminus might also contain a leucine zipper (Shotland et al., 2000). In Synechocystis 6803 there are four potential FtsH proteases, two of which are crucial for cell viability (slr1390 and slr1604) and two that are dispensable (slr0228 and sll1463) (Mann et al., 2000). Recent studies on an slr0228 insertion mutant have revealed that this particular member is needed for photoprotection, and is required for normal rates of D1 degradation in vivo as assessed in pulse-chase assays (Silva et al., 2003). Importantly, full-length D1 was stabilized in the mutant during light stress and there was no evidence for the accumulation of D1 fragments, which would be expected if the role of FtsH were solely to remove D1 fragments. FtsH (slr0228 and slr1604) were also found at low levels in His-tagged PSII preparations of Synechocystis 6803 (Kashino et al., 2002; Silva et al., 2003). Although there are a number of interpretations of these data, the simplest model is one in which FtsH (slr0228) plays a direct role in the early stages of D1 degradation, not just in the removal of breakdown fragments.
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In the case of Arabidopsis thaliana, nine FtsH homologues are targeted to the chloroplast (Sakamoto et al., 2003
). Mutation of FtsH2 (VAR2) and FtsH5 (VAR1) give rise to a yellow variegated phenotype, whereas ftsH1, ftsH6 or ftsH8 mutants show no visible phenotypic difference to WT (Sakamoto et al., 2003). Importantly both var1 (ftsH5) and var2 (ftsH2) mutants show impaired PSII repair (Bailey et al., 2002; Sakamoto et al., 2002). In the case of var2, degradation of damaged D1 was blocked at an early stage, in a similar manner to that observed in the cyanobacterial ftsH (slr0228) mutant (Bailey et al., 2002). It therefore seems that the role of FtsH in PSII repair and D1 turnover might be conserved in both cyanobacteria and higher plants. |
Model for FtsH-mediated D1 degradation |
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Based on what is known about the mechanism of FtsH proteases, particularly in E. coli (Akiyama and Ito, 2003
) and mitochondria (Langer, 2000), a general model for D1 degradation in cyanobacteria and chloroplasts has been suggested (Silva et al., 2003). It is proposed that FtsH (either homo- or hetero-oligomeric) forms a hexameric ring in the membrane. Damaged D1 is then translocated through a central pore in an ATP-driven process and subsequently degraded at the Zn2+-centre (Fig. 2B). The key feature of FtsH-mediated proteolysis of membrane proteins in E. coli is that it is a highly processive reaction (Akiyama, 2002) and can occur from either the N- or C-terminus (Chiba et al., 2002), or possibly from the ends generated after an FtsH-mediated endoproteolytic cleavage event (Shotland et al., 2000). Given that the Zn2+-binding site is likely to be located on the stromal side of the membrane (Lindahl et al., 1996), proteolysis would be initiated from stromally exposed regions of D1 such as the N-terminus or after cleavage in the QB-binding pocket. Proteolysis from the N-terminus is particularly attractive, as this would allow potential synchronization between the co-translational insertion of a newly synthesized D1 subunit into PSII and the removal of the damaged subunit. It would also explain why N-terminal phosphorylation of D1 and other PSII core subunits might control their degradation in the chloroplast (Koivuniemi et al., 1995).
In order to confirm this model it will probably be necessary to develop an in vitro assay for studying FtsH-mediated degradation of D1, probably along the lines of one recently developed for E. coli FtsH, which required the use of a membrane-based system rather than detergent-solubilized enzyme and substrate (Akiyama and Itoh, 2003).
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What is the signal that triggers D1 degradation in vivo? |
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Studies in E. coli have highlighted three factors that are important for FtsH-mediated degradation of membrane proteins: (i) the exposed N-terminus of the target protein must be of sufficient length (greater than 20 residues) to engage FtsH; the precise sequence being less important (Chiba et al., 2000
), (ii) the target protein must be in a relatively unfolded or destabilized state as FtsH is a weak unfoldase (Herman et al., 2003), and (iii) FtsH must contain transmembrane helices, possibly to interact with the target membrane protein (Akiyama and Ito, 2001).
Exposure of PSII to light is known to damage pigments and to oxidize protein side-chains (Sharma et al., 1997), both of which will act to destabilize the PSII structure. As mentioned earlier, the involvement of D1 in binding many of the key co-factors in PSII means that D1 is potentially more liable to damage and destabilization. This, in combination with an accessible N-terminus, would be the trigger for FtsH-mediated proteolysis to proceed. Initial binding of FtsH to PSII could be through the interaction of transmembrane helices or even through sequences on the lumenal side of the membrane. In this respect, Bailey and colleagues (Bailey et al., 2002) have highlighted an 81-amino-acid sequence of FtsH that is predicted to lie in the lumen of the chloroplast. This region is highly conserved in oxygenic photosynthetic organisms, perhaps because it is involved in recognizing sequences in PSII.
One attractive feature of this model is that FtsH would act to remove destabilized D1, and potentially other PSII subunits, no matter where the damage had occurred. Thus a precise triggering event need not commit D1 to degradation; rather it could be the accumulation of many destabilizing events. In principle, it should be possible to isolate D1 mutants that have slower rates of D1 degradation because of enhanced stabilization of structure or perturbed interaction with FtsH. Interestingly mutants in both the QB-binding pocket, at D1-Ser264 and D1-Ala263 (Dalla Chiesa et al., 1997), and at D1-His92 on the lumenal side of the membrane, slow D1 degradation (Lupínková and Komenda, 2004). What is clear is that the so-called ‘PEST’-like sequence located close to the QB-binding pocket of D1, and suggested to be important for D1 degradation (Greenberg et al., 1987), is not required for D1 turnover (Nixon et al., 1995).
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The oligomeric structure of FtsH and its possible interaction with prohibitins |
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Given the importance of FtsH (slr0228) for the removal of damaged D1 in Synechocystis 6803, future studies will aim to clarify the location and oligomeric organization of slr0228 in the membrane. In the case of A. thaliana, initial indications are that VAR2 might exist both as a homocomplex and a heterocomplex with VAR1 (Sakamoto et al., 2003
). Rodermel and co-workers have also shown that overexpression of FtsH8 can rescue the ftsH2 (var2) mutation, so it seems likely that the chloroplast FtsH subunits could assemble to give rise to a heterogeneous population of hexameric complexes, each with a potentially different activity (Yu et al., 2004).
Of particular interest will be the identification of possible interacting partners of FtsH (slr0228). In E. coli it is known that FtsH forms a supercomplex with the HflKC complex (Saikawa et al., 2004), and in yeast mitochondria with a large heterooligomeric prohibitin complex (Steglich et al., 1999). Both HflKC and prohibitin are members of the SPFH (stomatin, prohibitin, flotillin, HflKC) superfamily of proteins (Tavernarakis et al., 1999). One role of the prohibitin complex in yeast mitochondria is to stabilize newly synthesized membrane subunits (Nijtmans et al., 1999). Consequently, members of the SPFH family might be involved in PSII repair, possibly either to stabilize newly synthesized D1 prior to insertion into a PSII complex in a post-translational step, or to stabilize other PSII subunits to prevent unwanted FtsH mediated proteolysis (Silva and Nixon, 2001). In this regard, it is interesting to note that there are a number of prohibitin and stomatin homologues predicted from analysis of the Synechocystis genome sequence.
Another key question that has been addressed is whether FtsH (slr0228) functions solely in PSII repair or whether it has a general role in the removal of damaged or unassembled proteins from the thylakoid membrane. Recent experiments have been performed to look at protein turnover in PSII mutants unable to assemble a functional PSII complex because synthesis of a key PSII subunit is blocked. In all cases degradation of the remaining PSII subunits, which usually occurs rapidly in the presence of FtsH (slr0228) is reduced dramatically in its absence (PJ Nixon, unpublished data). These data therefore provide evidence in favour of a general role for FtsH (slr0228) in the removal of unassembled and/or damaged proteins from the membrane.
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Where does PSII repair occur in cyanobacteria? |
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Although functional PSII complexes are definitely found in the thylakoid membrane of cyanobacteria, there is still uncertainty about the location of the sites of synthesis, assembly and repair. In chloroplasts, repair of PSII is thought to take place in the stromal lamellae (Aro et al., 1993
). For Synechocystis 6803, immunochemical data have indicated that D1, D2, cytochrome b-559, and the PsbO subunit can be found in the cytoplasmic membrane (Smith and Howe, 1993; Zak et al., 2001). It has therefore been suggested that the cytoplasmic membrane might be the site of synthesis of the minimal PSII reaction centre complex, consisting of D1, D2, and cytochrome b-559, which then migrates into the thylakoid membrane to be assembled into the holoenzyme (Smith and Howe, 1993; Zak et al., 2001). However, pulse–chase experiments have not yet been conducted to confirm that these subunits are first incorporated into the cytoplasmic membrane. This means that it is still possible that the PSII subunits found in the cytoplasmic membrane could be in the process of being degraded rather than assembled (Smith and Howe, 1993). Another complication could be that the cytoplasmic membrane fraction used in the localization studies might contain other types of membrane system, distinct to the thylakoid and cytoplasmic membrane. Since it is still unclear how proteins and lipids move between the cytoplasmic and thylakoid membrane systems, it is possible that there might be an interconnecting membrane system in which assembly and repair occurs, that co-purifies with the cytoplasmic membrane fraction. Alternatively, if there is no physical connection between the thylakoid and cytoplasmic membranes, a vesicular transport system must be invoked (Westphal et al., 2001). |
Are ROS involved in D1 degradation in vivo? |
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A wide variety of studies conducted in vitro have led to speculation that ROS are potential candidates for cleaving D1 in vivo (Mishra et al., 1994
; Miyao et al., 1995). In such a scenario, the primary cleavage event in the QB-binding pocket would be mediated by ROS. However, one of the most dramatic observations following high-light treatment of both the ftsH (slr0228) mutant and var2 mutant of A. thaliana is the persistence of full-length D1 in the thylakoid membrane, despite extensive inactivation of the PSII complex, and under conditions where D1 is degraded in the WT controls. In the authors' opinion this is convincing evidence against an obligatory role for ROS in the direct cleavage of D1 during PSII repair in vivo.
In agreement with earlier conclusions (Komenda and Masojídek, 1995; Lupínková and Komenda, 2004), it is felt that D1 degradation in vivo should be considered to occur in two modes depending on the severity of the irradiation and the capacity for repair: (i) under ‘normal’ conditions a totally enzymatic process (mediated by FtsH) performs the selective replacement of damaged D1, without producing detectable breakdown products, and (ii) ROS-mediated non-enzymatic reactions occur under more ‘extreme’ conditions when the ‘normal’ enzymatic removal of damaged subunits cannot keep pace with the rate of damage by ROS. Under these latter circumstances the resulting breakdown fragments and aggregates that are observed might resemble the products studied in vitro. Consequently, caution is urged when linking breakdown fragments generated in vitro (or under extreme conditions in vivo) to the ‘normal’ enzymatic process of D1 turnover.
However, it is probable that under the more ‘extreme’ conditions of photodamage, oxidized forms of D1 and the other PSII subunits, as well as their adducts, can be removed from the cell by additional proteases not used in the ‘normal’ enzymatic process. These could include the DegP/HtrA proteases and other uncharacterized soluble proteases (Yamamoto, 2001; Mizusawa et al., 2003). However, this route for PSII repair is likely to be less specific and slower than the FtsH-mediated pathway.
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Acknowledgements |
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We are extremely grateful to the BBSRC for financial support. JK also acknowledges support from the GACR (project no.203/04/0800), Czech Ministry of Education (projects no. LN00A141 and MSM123100002), and Academy of Sciences (Research Concept no. AV0Z5020903). We would also like to thank our various collaborators: Paulo Silva (University of Lisbon, Portugal), Shaun Bailey, Colin Robinson, and Nick Mann (Warwick University, UK), Elinor Thompson and Conrad Mullineaux (University College London, UK), Imre Vass (Szeged, Hungary), and Olaf Kruse (University of Bielefeld, Germany).
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References |
|---|
Adam Z, Clarke AK. 2002. Cutting edge of proteolysis. Trends in Plant Science 7, 451–456.[CrossRef][ISI][Medline]
Adir N, Zer H, Shochat S, Ohad I. 2003. Photoinhibition—a historical perspective. Photosynthesis Research 76, 343–370.[CrossRef][ISI][Medline]
Akiyama Y. 2002. Proton-motive force stimulates the proteolytic activity of FtsH, a membrane-bound ATP-dependent protease in Escherichia coli. Proceedings of the National Academy of Sciences, USA. 99, 8066–8071.
Akiyama Y, Ito K. 2001. Roles of homo-oligomerization and membrane association in ATPase and proteolytic activities of FtsH in vitro. Biochemistry 40, 7687–7693.[Medline]
Akiyama Y, Ito K. 2003. Reconstitution of membrane proteolysis by FtsH. Journal of Biological Chemistry 278, 18146–18153.
Aro E-M, Virgin I, Andersson B. 1993. Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochimica et Biophysica Acta 1143, 113–134.[Medline]
Asada K. 1999. The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50, 601–639.[CrossRef][ISI][Medline]
Bailey S, Thompson E, Nixon PJ, Horton P, Mullineaux CW, Robinson C, Mann NH. 2002. A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the PSII repair cycle in vivo. Journal of Biological Chemistry 277, 2006–2011.
Barber J, Andersson B. 1992. Too much of a good thing: light can be bad for photosynthesis. Trends in Biochemical Science 17, 61–66.
Bottomley W, Spencer D, Whitfeld PR. 1974. Protein synthesis in isolated spinach chloroplasts: comparison of light-driven and ATP-driven synthesis. Archives of Biochemistry and Biophysics 164, 106–117.[CrossRef][ISI][Medline]
Chiba S, Akiyama Y, Mori H, Matsuo E, Ito K. 2000. Length recognition at the N-terminal tail for the initiation of FtsH-mediated proteolysis. EMBO Reports 1, 47–52.[CrossRef][ISI][Medline]
Chiba S, Akiyama Y, Ito K. 2002. Membrane protein degradation by FtsH can be initiated from either end. Journal of Bacteriology 184, 4775–4782.
Clausen T, Southan C, Ehrmann M. 2002. The HtrA family of proteases: implications for protein composition and cell fate. Molecular Cell 10, 443–455.[CrossRef][ISI][Medline]
Dalla Chiesa M, Friso G, Deak Z, Vass I, Barber J, Nixon PJ. 1997. Reduced turnover of the D1 polypeptide and photoactivation of electron transfer in novel herbicide resistant mutants of Synechocystis sp. PCC 6803. European Journal of Biochemistry 248, 731–740.[ISI][Medline]
Diner BA, Rappaport F. 2002. Structure, dynamics, and energetics of the primary photochemistry of PSII of oxygenic photosynthesis. Annual Review of Plant Biology 53, 551–580.[CrossRef][Medline]
Eaglesham ARJ, Ellis RJ. 1974. Protein synthesis in chloroplasts. II. Light-driven synthesis of membrane proteins by isolated pea chloroplasts. Biochimica et Biophysica Acta 335, 396–407.
Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S. 2004. Architecture of the photosynthetic oxygen-evolving center. Science 303, 1782–1784.
Greenberg BM, Gaba V, Mattoo AK, Edelman M. 1987. Identification of a primary in vivo degradation product of the rapidly turning-over 32 kDa protein of PSII. EMBO Journal 6, 2865–2869.[ISI][Medline]
Haußühl K, Andersson B, Adamska I. 2001. A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant PSII. EMBO Journal 20, 713–722.[CrossRef][ISI][Medline]
Herman C, Prakash S, Lu CZ, Matouschek A, Gross CA. 2003. Lack of robust unfoldase activity confers a unique level of substrate specificity to the universal AAA protease FtsH. Molecular Cell 11, 659–669.[CrossRef][ISI][Medline]
Kashino Y, Lauber WM, Carroll JA, Wang Q, Whitmarsh J, Satoh K, Pakrasi HB. 2002. Proteomic analysis of a highly active PSII preparation from the cyanobacterium Synechocystis sp. PCC 6803 reveals the presence of novel polypeptides. Biochemistry 41, 8004–8012.[CrossRef][Medline]
Koivuniemi A, Aro E-M, Andersson B. 1995. Degradation of the D1 and D2 proteins of PSII in higher plants is regulated by reversible phosphorylation. Biochemistry 34, 16022–16029.[CrossRef][Medline]
Komenda J, Barber J. 1995. Comparison of psbO and psbH deletion mutants of Synechocystis PCC 6803 indicates that degradation of D1 protein is regulated by the QB site and dependent on protein synthesis. Biochemistry 34, 9625–9631.[CrossRef][Medline]
Komenda J, Masojídek J. 1995. Functional and structural changes of the PSII complex induced by high irradiance in cyanobacterial cells. European Journal of Biochemistry 233, 677–682.[ISI][Medline]
Kyle DJ, Ohad I, Arntzen CJ. 1984. Membrane protein damage and repair: selective loss of a quinone-protein function in chloroplast membranes. Proceedings of the National Academy of Sciences, USA 81, 4070–4074.
Langer T. 2000. AAA proteases: cellular machines for degrading membrane proteins. Trends in Biochemical Science 25, 247–251.
Lindahl M, Tabak S, Cseke L, Pichersky E, Andersson B, Adam Z. 1996. Identification, characterization and molecular cloning of a homologue of the bacterial FtsH protease in chloroplasts of higher plants. Journal of Biological Chemistry 271, 29329–29334.
Lindahl M, Spetea C, Hundal T, Oppenheim AB, Adam Z, Andersson B. 2000. The thylakoid FtsH protease plays a role in the light-induced turnover of the PSII D1 protein. The Plant Cell 12, 419–431.
Lupínková L, Komenda J. 2004. Oxidative modifications of the photosystem two D1 protein by reactive oxygen species: from isolated protein to cyanobacterial cells. Photochemistry and Photobiology 79, 152–162.[CrossRef][ISI][Medline]
Mann N, Novac N, Mullineaux C, Newman J, Bailey S, Robinson C. 2000. Involvement of an FtsH homologue in the assembly of functional photosystem I in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Letters 479, 72–77.[CrossRef][ISI][Medline]
Mishra NP, Francke C, van Gorkom H J, Ghanotakis DF. 1994. Destructive role of singlet oxygen during aerobic illumination of the PSII core complex. Biochimica et Biophysica Acta 1186, 81–90.
Miyao M, Ikeuchi M, Yamamoto N, Ono T. 1995. Specific degradation of the D1 protein of PSII by treatment with hydrogen peroxide in darkness: implications for the mechanism of degradation of the D1 protein under illumination. Biochemistry 34, 10019–10026.[CrossRef][Medline]
Mizusawa N, Tomo T, Satoh K, Miyao M. 2003. Degradation of the D1 protein of PSII under illumination in vivo: two different pathways involving cleavage and intermolecular cross-linking. Biochemistry 42, 10034–10044.[CrossRef][Medline]
Nijtmans LG, de Jong L, Artal Sanz M, Coates PJ, Berden JA, Back JW, Muijsers AO, van der Spek H, Grivell LA. 2000. Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. EMBO Journal 19, 2444–2451.[CrossRef][ISI][Medline]
Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A, Murata N. 2001. Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO Journal 20, 5587–5594.[CrossRef][ISI][Medline]
Nixon PJ, Komenda J, Barber J, Deak Z, Vass I, Diner BA. 1995. Deletion of the PEST-like region of photosystem two modifies the QB-binding pocket but does not prevent rapid turnover of D1. Journal of Biological Chemistry 270, 14919–14927.
Ogura T, Tomoyasu T, Yuki T, Morimura S, Begg KJ, Donachie WD, Mori H, Niki H, Hiraga S. 1991. Structure and function of the ftsH gene in Escherichia coli. Researches in Microbiology 142, 279–282.[CrossRef]
Ohad I, Kyle DJ, Arntzen CJ. 1984. Membrane protein damage and repair: removal and replacement of inactivated 32-kilodalton polypeptides in chloroplast membranes. Journal of Cell Biology 270, 14919–14927.
Ohad I, Keren N, Zer H, Gong H, Mor TS, Gal A, Tal S, Domovich Y. 1994. Light-induced degradation of the PSII reaction centre D1 protein in vivo: an integrative approach. In: Baker NR, Bowyer JR, eds. Photoinhibition of photosynthesis. Oxford: Bios Scientific Publishers, 161–177.
Prasil O, Adir N, Ohad I. 1992. Dynamics of PSII: mechanism of photoinhibition and recovery processes. In: Barber J, ed. The photosystems: structure, function and molecular biology. Amsterdam: Elsevier Science Publishers, 295–248.
Saikawa N, Akiyama Y, Ito K. 2004. FtsH exists in an exceptionally large complex containing HflKC in the plasma membrane of Escherichia coli. Journal of Structural Biology 146, 123–129.[CrossRef][ISI][Medline]
Sakamoto W, Tamura T, Hanba-Tomita Y, Murata M. 2002. The VAR1 locus of Arabidopsis encodes a chloroplastic FtsH and is responsible for leaf variegation in the mutant alleles. Genes Cells 7, 769–780.[Abstract]
Sakamoto W, Zaltsman A, Adam Z, Takahashi Y. 2003. Coordinated regulation and complex formation of YELLOW VARIEGATED1 and YELLOW VARIEGATED2, chloroplastic FtsH metalloproteases involved in the repair cycle of PSII in Arabidopsis thylakoid membranes. The Plant Cell 15, 2843–2855.
Sharma J, Panico M, Shipton CA, Nilsson F, Morris HR, Barber J. 1997. Primary structure characterization of the PSII D1 and D2 subunits. Journal of Biological Chemistry 272, 33158–33166.
Shotland Y, Shifrin A, Ziv T, Teff D, Koby S, Kobiler O, Oppenheim AB. 2000. Proteolysis of bacteriophage lambda CII by Escherichia coli FtsH (HflB). Journal of Bacteriology 182, 3111–3116.
Silva P, Nixon PJ. 2001. Identification of possible assembly and repair factors in photosystem II preparations of Synechocystis sp. PCC 6803: a new model for D1 turnover. 12th International Congress of Photosynthesis. Brisbane-Australia: CSIRO Publishing.
Silva P, Choi Y-J, Hassan HAG, Nixon PJ. 2002. Involvement of the HtrA family of proteases in the protection of the cyanobacterium Synechocystis PCC 6803 from light stress and in the repair of PSII. Philosophical Transactions of the Royal Society, London B 357, 1461–1468.
Silva P, Thompson E, Bailey S, Kruse O, Mullineaux CW, Robinson C, Mann NH, Nixon PJ. 2003. FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp. PCC 6803. The Plant Cell 15, 2152–2164.
Smith D, Howe CJ. 1993. The distribution of photosystem I and PSII polypeptides between the cytoplasmic and thylakoid membranes of cyanobacteria. FEMS Microbiology Letters 110, 341–348.
Sokolenko A, Pojidaeva E, Zinchenko V, Panichkin V, Glaser VM, Herrmann RG, Shestakov SV. 2002. The gene complement for proteolysis in the cyanobacterium Synechocystis sp. PCC 6803 and Arabidopsis thaliana chloroplasts. Current Genetics 41, 291–310.[CrossRef][ISI][Medline]
Spetea C, Hundal T, Lohmann F, Andersson B. 1999. GTP bound to chloroplast thylakoid membranes is required for light-induced, multienzyme degradation of the PSII D1 protein. Proceedings of the National Academy of Sciences, USA 96, 6547–6552.
Steglich G, Neupert W, Langer T. 1999. Prohibitins regulate membrane protein degradation by the m-AAA protease in mitochondria. Molecular and Cellular Biology 19, 3435–3442.
Tavernarakis N, Driscoll M, Kyrpides NC. 1999. The SPFH domain: implicated in regulating targeted protein turnover in stomatins and other membrane-associated proteins. Trends in Biochemical Science 24, 425–427.
Westphal S, Heins L, Soll J, Vothknecht UC. 2001. Vipp1 deletion mutant of Synechocystis: a connection between bacterial phage shock and thylakoid biogenesis? Proceedings of the National Academy of Sciences, USA 98, 4243–4248.
Yamamoto Y. 2001. Quality control of PSII. Plant Cell Physiology 42, 121–128.
Yu F, Park S, Rodermel SR. 2004. The Arabidopsis FtsH metalloprotease gene family: interchangeability of subunits in chloroplast oligomeric complexes. The Plant Journal 37, 864–876.[CrossRef][ISI][Medline]
Zak E, Norling B, Maitra R, Huang F, Andersson B, Pakrasi HB. 2001. The initial steps of biogenesis of cyanobacterial photosystems occur in plasma membranes. Proceedings of the National Academy of Sciences, USA 98, 13443–13448.
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