A thylakoid processing protease is required for complete maturation of the lumen protein plastocyanin

Hageman, Johan; Robinson, Colin; Smeekens, Sjef; Weisbeek, Peter

doi:10.1038/324567a0

Cited by 163 publications

(100 citation statements)

References 13 publications

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“…The resulting intermediate form is then transported across the thylakoid membrane into the lumen via one of two energetically distinct pathways by means of the lumen-targeting domain. Maturation is effected by a lumen-facing thylakoid membrane-bound processing peptidase that results in the appearance of a smaller mature protein within the thylakoid lumen (Hageman et al, 1986;Shackleton and Robinson, 1991). Transthylakoid translocation mechanisms that have so far been identified are believed to each be specific for a subset of lumenal nuclear-encoded proteins.…”

Section: Introductionmentioning

confidence: 99%

A folded protein can be transported across the chloroplast envelope and thylakoid membranes.

Clark

Theg

1997

MBoC

161

109

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Many thylakoid lumenal proteins are nuclear encoded, cytosolically synthesized, and reach their functional location after posttranslational targeting across two chloroplast envelope membranes and the thylakoid membrane via proteinaceous transport systems. To study whether these transmembrane transport machineries can translocate folded structures, we overexpressed the 17-kDa subunit of the oxygen-evolving complex of photosystem II (prOE17) that had been modified to contain a unique C-terminal cysteine. This allowed us to chemically link a terminal 6.5-kDa bovine pancreatic trypsin inhibitor (BPTI) moiety to prOE17 to create the chimeric protein prOE17-BPTI. Redox reagents and an irreversible sulfhydryl-specific cross-linker, bis-maleimidohexane, were used to manipulate the structure of BPTI. Import of prOE17-BPTI into isolated chloroplasts and thylakoids demonstrates that the small tightly folded BPTI domain is carried across both the chloroplast envelopes and the ApH-dependent transmembrane transporter of the thylakoid membrane when linked to the correctly targeted OE17 precursor. Transport proceeded even when the BPTI moiety was internally cross-linked into a proteaseresistant form. These data indicate that unfolding is not a ubiquitous requirement for protein translocation and that at least some domains of targeted proteins can maintain a nonlinear structure during their translocation into and within chloroplasts.

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Section: Introductionmentioning

confidence: 99%

A folded protein can be transported across the chloroplast envelope and thylakoid membranes.

Clark

Theg

1997

MBoC

161

109

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“…[7]. The C-terminal domain appears to function as a thylakoidtransfer domain and is cleaved off upon translocation across the thylakoid membrane by the second processing protease located in the thylakoid lumen or on the lumenal face of the thylakoid membrane [8]. While the transit peptides of stromal proteins or the N-terminal domains of the transit peptides of thylakoid lumen proteins, which contain chloroplast-targeting signals, are characterized by high contents of hydroxylated amino acids (Ser, Thr) and basic amino acids (Arg, Lys) and the lack of acidic amino acids (Asp, Glu), previous statistical analyses did not reveal any obvious consensus sequences among transit peptides of different proteins [9].…”

mentioning

confidence: 99%

The chloroplast‐targeting domain of plastocyanin transit peptide can form a helical structure but does not have a high affinity for lipid bilayers

Endo

Kawamura

Nakai

1992

European Journal of Biochemistry

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Conformational properties and interactions with lipid membranes were studied for the chemically synthesized peptides PC(1-37) and PC(1-43), corresponding to the N-terminal37 and 43 residues, respectively, of the transit peptide of the precursor to plastocyanin of Silene pratensis. PC(1-43) covers the entire chloroplast targeting domain of the transit peptide. CD spectra of PC(1-37) and PC(1-43) showed that both peptides have little ordered structure in aqueous solutions but form partially helical conformations in the presence of detergent micelles or in methanol. Vesicle disruption and direct-binding experiments revealed, however, that neither PC(1-37) nor PC(1-43) had a high affinity for lipid membranes. Since in the intact plastocyanin transit peptide the chloroplast-targeting domain is followed by a hydrophobic thylakoid-transfer domain, the plastocyanin precursor may well be transported to the chloroplast surface first with the aid of the thylakoid-transfer domain. The chloroplast-targeting domain may then form a helical structure in the lipid environments, and a chloroplast-specific motif displayed on the helical structure may be recognized by a receptor protein located at the chloroplast envelope membranes.Most chloroplast proteins are encoded by nuclear genes, synthesized on cytosolic ribosomes, usually as precursors with a transient N-terminal extension called a transit peptide, and imported into chloroplasts (for reviews see [l, 21). Information for targeting proteins to chloroplasts is most likely contained in transit peptides; many artificial fusion proteins consisting of the transit peptide of a stromal protein precursor and a non-plastid passenger protein can be successfully transported to the chloroplast stroma both in vitro and in vivo [3-71. Thylakoid lumen proteins such as plastocyanin carry a transit peptide consisting of two functionally distinct domains : the N-terminal positively charged hydrophilic domain and the Cterminal hydrophobic domain resembling a signal peptide of secretory proteins. The N-terminal domain is proteolytically removed in the stroma and is functionally equivalent to the transit peptide of stromal proteins; it can be replaced by a stromal transit peptide without affecting the import propertiesCorrespondence to

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“…Whereas the SPP preparation processed each precursor to the intermediate size as previously shown (Hageman et al, 1986;James et al, 1989), no cleavage products were detectable after incubation with MPP (data not shown). MPP is thus specific for mitochondrial precursor proteins, whereas SPP appears to cleave both types of precursor.…”

Section: Cleavage Of Mitochondrial Precursor Proteins By a Preparatiomentioning

confidence: 82%

“…Some imported proteins, such as those destined for the thylakoid lumen or the niitochondrial intermembrane space, are processed only to an intermediate form by SPP or MPP, and maturation is completed by a second processing peptidase located in the thylakoid membrane or mitochondrial inner membrane (Hageman et al, 1986;Schneider et al, 1991).…”

mentioning

confidence: 99%

Efficient but aberrant cleavage of mitochondrial precursor proteins by the chloroplast stromal processing peptidase

Bassham

Creighton

Arretz

et al. 1994

European Journal of Biochemistry

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Cytosol-synthesised chloroplast and mitochondrial precursor proteins are proteolytically processed after import by highly specific, metal-dependent soluble enzymes : the stromal processing peptidase (SPP) and the matrix processing peptidase (MPP), respectively. We have used in vitro processing assays to compare the reaction specificities of highly purified preparations of pea SPP and Neurospora crassa MPP, both of which are unable to cleave a variety of 'foreign' proteins. We show that SPP can cleave all five mitochondrial precursor proteins tested, namely cyclophilin, the p subunit of the F,-ATPase complex, the Rieske FeS protein, the a-MPP subunit and cytochrome 6,. In contrast, MPP is unable to cleave any chloroplast precursor proteins tested. Several of the mitochondrial precursor proteins are cleaved more efficiently by SPP than are many authentic chloroplast precursor proteins but, in each case, cleavage takes place at a site or sites which are Nterminal to the authentic MPP site; pre-cyclophilin is cleaved 5 residues upstream of the MPP site and the precursor of the p subunit of the F,-ATPase complex is cleaved at sites 5 and 12 residues upstream. We discuss the implications of these data for the SPP reaction mechanism.

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A thylakoid processing protease is required for complete maturation of the lumen protein plastocyanin

Cited by 163 publications

References 13 publications

A folded protein can be transported across the chloroplast envelope and thylakoid membranes.

A folded protein can be transported across the chloroplast envelope and thylakoid membranes.

The chloroplast‐targeting domain of plastocyanin transit peptide can form a helical structure but does not have a high affinity for lipid bilayers

Efficient but aberrant cleavage of mitochondrial precursor proteins by the chloroplast stromal processing peptidase

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