The Reaction Specificities of the Thylakoidal Processing Peptidase and Escherichia Coli Leader Peptidase Are Identical

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1989 Dec 1

PMID 2684650

Citations 31

Authors

C Halpin

P D Elderfield

H E James

R Zimmermann

B Dunbar

C Robinson

Affiliations

Soon will be listed here.

Abstract

Proteins which are transported across the bacterial plasma membrane, endoplasmic reticulum and thylakoid membrane are usually synthesized as larger precursors containing amino-terminal targeting signals. Removal of the signals is carried out by specific, membrane-bound processing peptidases. In this report we show that the reaction specificities of these three peptidases are essentially identical. Precursors of two higher plant thylakoid lumen proteins are efficiently processed by purified Escherichia coli leader peptidase. Processing of one precursor, that of the 23 kd photosystem II protein, by both the thylakoidal and E. coli enzymes generates the correct mature amino terminus. Similarly, leader (signal) peptides of both eukaryotic and prokaryotic origin are cleaved by partially purified thylakoidal processing peptidase. No evidence of incorrect processing was obtained. Both leader peptidase and thylakoidal peptidase are inhibited by a synthetic leader peptide.

Citing Articles

Functional diversification of thylakoidal processing peptidases in Arabidopsis thaliana.

Hsu S, Endow J, Ruppel N, Roston R, Baldwin A, Inoue K PLoS One. 2011; 6(11):e27258.

PMID: 22087276 PMC: 3210150. DOI: 10.1371/journal.pone.0027258.

Keep the balloon deflated: the significance of protein maturation for thylakoid flattening.

Endow J, Ruppel N, Inoue K Plant Signal Behav. 2010; 5(6):721-3.

PMID: 21135574 PMC: 3001570. DOI: 10.4161/psb.5.6.11662.

The significance of protein maturation by plastidic type I signal peptidase 1 for thylakoid development in Arabidopsis chloroplasts.

Shipman-Roston R, Ruppel N, Damoc C, Phinney B, Inoue K Plant Physiol. 2010; 152(3):1297-308.

PMID: 20097790 PMC: 2832241. DOI: 10.1104/pp.109.151977.

Interactions that drive Sec-dependent bacterial protein transport.

Rusch S, Kendall D Biochemistry. 2007; 46(34):9665-73.

PMID: 17676771 PMC: 2675607. DOI: 10.1021/bi7010064.

Purification and Characterization of a Membrane-Bound Protease from Chlamydomonas reinhardtii.

Hoober J, Hughes M Plant Physiol. 1992; 99(3):932-7.

PMID: 16669021 PMC: 1080566. DOI: 10.1104/pp.99.3.932.

References

Zimmermann R, Mollay C . Import of honeybee prepromelittin into the endoplasmic reticulum. Requirements for membrane insertion, processing, and sequestration. J Biol Chem. 1986; 261(27):12889-95. View

Smeekens S, Bauerle C, Hageman J, Keegstra K, Weisbeek P . The role of the transit peptide in the routing of precursors toward different chloroplast compartments. Cell. 1986; 46(3):365-75. DOI: 10.1016/0092-8674(86)90657-4. View

Zwizinski C, Wickner W . Purification and characterization of leader (signal) peptidase from Escherichia coli. J Biol Chem. 1980; 255(16):7973-7. View

Kuwabara T, Reddy K, Sherman L . Nucleotide sequence of the gene from the cyanobacterium Anacystis nidulans R2 encoding the Mn-stabilizing protein involved in photosystem II water oxidation. Proc Natl Acad Sci U S A. 1987; 84(23):8230-4. PMC: 299515. DOI: 10.1073/pnas.84.23.8230. View

Bohni P, Deshaies R, Schekman R . SEC11 is required for signal peptide processing and yeast cell growth. J Cell Biol. 1988; 106(4):1035-42. PMC: 2115025. DOI: 10.1083/jcb.106.4.1035. View

Wickner W, Moore K, Dibb N, Geissert D, Rice M . Inhibition of purified Escherichia coli leader peptidase by the leader (signal) peptide of bacteriophage M13 procoat. J Bacteriol. 1987; 169(8):3821-2. PMC: 212473. DOI: 10.1128/jb.169.8.3821-3822.1987. View

Kirwin P, Elderfield P, Robinson C . Transport of proteins into chloroplasts. Partial purification of a thylakoidal processing peptidase involved in plastocyanin biogenesis. J Biol Chem. 1987; 262(34):16386-90. View

von Heijne G, Steppuhn J, Herrmann R . Domain structure of mitochondrial and chloroplast targeting peptides. Eur J Biochem. 1989; 180(3):535-45. DOI: 10.1111/j.1432-1033.1989.tb14679.x. View

von Heijne G . Signal sequences. The limits of variation. J Mol Biol. 1985; 184(1):99-105. DOI: 10.1016/0022-2836(85)90046-4. View

10.

Austen B, Hermon-Taylor J, Kaderbhai M, Ridd D . Design and synthesis of a consensus signal sequence that inhibits protein translocation into rough microsomal vesicles. Biochem J. 1984; 224(1):317-25. PMC: 1144429. DOI: 10.1042/bj2240317. View

11.

von Heijne G . Patterns of amino acids near signal-sequence cleavage sites. Eur J Biochem. 1983; 133(1):17-21. DOI: 10.1111/j.1432-1033.1983.tb07424.x. View

12.

Kronenberg H, Fennick B, Vasicek T . Transport and cleavage of bacterial pre-beta-lactamase by mammalian microsomes. J Cell Biol. 1983; 96(4):1117-9. PMC: 2112328. DOI: 10.1083/jcb.96.4.1117. View

13.

Kirwin P, Elderfield P, Williams R, Robinson C . Transport of proteins into chloroplasts. Organization, orientation, and lateral distribution of the plastocyanin processing peptidase in the thylakoid network. J Biol Chem. 1988; 263(34):18128-32. View

14.

Wolfe P, Silver P, Wickner W . The isolation of homogeneous leader peptidase from a strain of Escherichia coli which overproduces the enzyme. J Biol Chem. 1982; 257(13):7898-902. View

15.

Melton D, Krieg P, Rebagliati M, Maniatis T, Zinn K, Green M . Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984; 12(18):7035-56. PMC: 320141. DOI: 10.1093/nar/12.18.7035. View

16.

Robinson C, Ellis R . Transport of proteins into chloroplasts. Partial purification of a chloroplast protease involved in the processing of important precursor polypeptides. Eur J Biochem. 1984; 142(2):337-42. DOI: 10.1111/j.1432-1033.1984.tb08291.x. View

17.

Muller M, Ibrahimi I, Chang C, Walter P, Blobel G . A bacterial secretory protein requires signal recognition particle for translocation across mammalian endoplasmic reticulum. J Biol Chem. 1982; 257(20):11860-3. View

18.

Jackson R, Blobel G . Post-translational cleavage of presecretory proteins with an extract of rough microsomes from dog pancreas containing signal peptidase activity. Proc Natl Acad Sci U S A. 1977; 74(12):5598-602. PMC: 431824. DOI: 10.1073/pnas.74.12.5598. View

19.

Wallace T, Stewart A, Pappin D, Howe C . Gene sequence for the 9 kDa component of Photosystem II from the cyanobacterium Phormidium laminosum indicates similarities between cyanobacterial and other leader sequences. Mol Gen Genet. 1989; 216(2-3):334-9. DOI: 10.1007/BF00334373. View

20.

Lei S, Lin H, Wang S, Callaway J, Wilcox G . Characterization of the Erwinia carotovora pelB gene and its product pectate lyase. J Bacteriol. 1987; 169(9):4379-83. PMC: 213756. DOI: 10.1128/jb.169.9.4379-4383.1987. View