Transport of CtpA protein from the cyanobacterium Synechocystis 6803 across the thylakoid membrane in chloroplasts

European Journal of Biochemistry

Volumn 249, Issue 2, 1997, Pages 497-504

  Karnauchov, Ivan ^a   Herrmann, Reinhold G ^a   Pakrasi, Himadri B ^b   Klösgen, Ralf Bernd ^a,c  

^a UNIVERSITY OF MUNICH   (Germany)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Botanisches Institut der Universitat   (Germany)

Author keywords

Protein transport; Sec dependent pathway; Synechocystis sp. PCC 6803; Thylakoid membrane; pH dependent pathway

Indexed keywords

PROTEINASE;

ARTICLE; CHLOROPLAST; CYANOBACTERIUM; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTEIN TRANSPORT; SPINACH; THYLAKOID MEMBRANE;

CYANOBACTERIA; SPINACIA OLERACEA; SYNECHOCYSTIS SP.; SYNECHOCYSTIS SP. PCC 6803;

EID: 0030702065     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1997.t01-1-00497.x     Document Type: Article

References (49)

1. Barbrook, A. C., Packer, J. C. L. & Howe, C. J. (1993) Components of the protein translocation machinery in the thermophilic cyanobacterium Phormidium laminosum, Biochem. Biophys. Res. Commun. 197, 874-877.
2. Berghöfer, J., Karnauchov, I., Herrmann, R. G. & Klösgen, R. B. (1995) Isolation and characterization of a cDNA encoding the SecA protein from spinach chloroplasts: evidence for azide-resistance of Sec-dependent protein translocation across thylakoid membranes of spinach, J. Biol. Chem. 270, 18 341-18 346.
3. Berghöfer, J. & Klösgen, R. B. (1996) Isolation and characterization of a cDNA encoding the SecY protein from spinach chloroplasts (accession no. Z54351) (PGR96-090), Plant Physiol. 112, 863.
4. Cai, D., Herrmann, R. G. & Klösgen, R. B. (1993) The 20 kDa apoprotein of the CP24 complex of photosystem II: an alternative model to study import and intra-organellar routing of nuclear-encoded thylakoid proteins, Plant J. 3, 383-392.
5. Chaddock, A. M., Mant, A., Karnauchov, I., Brink, S., Herrmann, R. G., Klösgen, R. B. & Robinson, C. (1995) A new type of signal peptide: central role of a twin-arginine motif in transfer signals for the ΔpH-dependent thylakoidal protein translocase, EMBO J. 14, 2715-2722.
6. Chamberlain, J. P. (1979) Fluorographic detection of radioactivity in polyacrylamide gels with the water-soluble fluor sodium salicylate. Anal. Biochem. 98, 132-135.
7. Clausmeyer, S., Klösgen, R. B. & Herrmann, R. G (1993) Protein import into chloroplasts: the hydrophilic lumenal proteins exhibit unexpected import and sorting specificities in spite of structurally conserved transit peptides, J. Biol. Chem. 268, 13 869-13 876.
8. Cline, K., Ettinger, W. F. & Theg, S. M. (1992) Protein-specific energy requirements for protein transport across or into thylakoid membranes, J. Biol. Chem. 267, 2688-2696.
9. Cline, K., Henry, R., Li, C. & Yuan, J. (1993) Multiple pathways for protein transport into or across the thylakoid membrane, EMBO J. 12, 4105-4114.
10. Franklin, A. E. & Hoffman, N. E. (1993) Characterization of a chloroplast homologue of the 54-kDa subunit of the signal recognition particle. J. Biol. Chem. 268, 22 175-22 180.
11. Hand, J. M., Szabo, L. J., Vasconcelos, A. C. & Cashmore, A. R. (1989) The transit peptide of a thylakoid membrane protein is functionally equivalent to a stroma-targeting sequence, EMBO J. 8, 3195-3206.
12. Henry, R., Carrigan, M., McCaffery, M., Ma, X. & Cline, K. (1997) Targeting determinants and proposed evolutionary basis for the Sec and the ΔpH protein transport systems in chloroplast thylakoid membranes, J. Cell Biol. 136, 823-832.
13. Hulford, A., Hazell, L., Mould, R. M. & Robinson, C. (1994) Two distinct mechanisms for the translocation of proteins across the thylakoid membrane, one requiring the presence of a stromal protein factor and nucleotide triphosphates, J. Biol. Chem. 169, 3251-3256.
14. Inagaki, N., Yamamoto, Y., Mori, H. & Satoh, K. (1996) Carboxyl-terminal processing protease for the D7 precursor protein: cloning and sequencing of the spinach cDNA. Plant Mol. Biol. 30, 39-50.
15. Kaneko, T., Sato, S., Kotani, H., Tanaka, A., Asamizu, E., Nakamura, Y., Miyajima, N., Hirosawa, M., Sugiura, M., Sasamoto, S., Kimura, T., Hosouchi, T., Matsuno, A., Muraki, A., Nakazaki, N., Naruo, K., Okumura, S., Shimpo, S., Takeuchi, C., Wada, T., Watanabe, A., Yamada, M., Yasuda, M. & Tabala, S. (1996a) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions, DNA Res. 3, 109-136.
16. Kaneko, T., Sato, S., Kotani, H., Tanaka, A., Asamizu, B., Nakamura, Y., Miyajima, N., Hirosawa, M., Sugiura, M., Sasamoto, S., Kimura, T., Hosouchi, T. Matsuno, A., Muraki, A., Nakazaki, N., Naruo, K., Okumura, S., Shimpo, S., Takeuchi, C., Wada, T., Watanabe, A., Yamada, M., Yasuda, M. & Tabata, S. (1996b) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions (supplement), DNA Res. 3, 185-209.
17. Kapazoglou, A., Sagliocco, F. & Dure, L. (1995) PSII-T, a new nuclear encoded lumenal protein from photosystem II, J. Biol. Chem. 270, 12 197-12 202.
18. Karnauchov, I., Cai, D., Schmidt, I., Herrmann, R. G. & Klösgen, R. B. (1994) The thylakoid translocation of subunit 3 of photosystem I, the psaF gene product, depends on a bipartite transit peptide and proceeds along an azide-sensitive pathway, J. Biol. Chem. 269, 32 871-32 878.
19. Klösgen, R. B., Brock, I. W., Herrmann, R. G. & Robinson, C. (1992) Proton gradient-driven import of the 16kDa oxygen-evolving complex protein as the full precursor protein by isolated thylakoids. Plant Mol. Biol. 18, 1031-1034.
20. Klösgen, R. B. (1997) Protein transport into and across the thylakoid membrane, J. Photochem. Photobiol. B: Biol. 38, 1-9.
21. Knott, T. G. & Robinson, C. (1994) The SecA inhibitor, azide, reversibly blocks the translocation of a subset of proteins across the chloroplast thylakoid membrane, J. Biol. Chem. 269, 7843-7846.
22. Kuhn, A., Wickner, W. & Kreil, G. (1986) The cytoplasmic carboxy terminus of M13 procoat is required for the membrane insertion of its central domain, Nature 322, 335-339.
23. Kumar, P. A., Kruse, E., Andriesse, X., Weisbeek, P. & Kloppstech, K. (1993) Integration of a cyanobacterial protein involved in nitrate reduction (narB) into isolated Synechococcus but not into pea thylakoid membranes, Eur. J. Biochem. 214, 533-537.
24. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.
25. Laidler, V., Chaddock, A. M., Knott, T. G., Walker, D. & Robinson, C. (1995) A SecY homolog in Arabidopsis thaliana, J. Biol. Chem. 270, 17 664-17 667.
26. Lamppa, G. K. (1988) The chlorophyll a/b-binding protein inserts into the thylakoids independent of its cognate transit peptide. J. Biol. Chem. 263, 14 996-14 999.
27. Li., X., Henry, R., Yuan, J., Cline, K. & Hoffman, N. E. (1995) A chloroplast homologue of the signal recognition particle subunit SRP54 is involved in the posttranslational integration of a protein into thylakoid membranes, Proc. Natl Acad. Sci. USA 92, 3789-3793.
28. Mant, A., Skovgaard Nielsen, V., Knott, T. G., Lindberg Møller, B. & Robinson, C. (1994) Multiple mechanisms for the targeting of photosystem I subunits F. H. K. L. and N into and across the thylakoid membrane. J. Biol. Chem. 269, 27 303-27 309.
29. Mant, A., Schmidt, I., Herrmann, R. G., Robinson, C. & Klösgen, R. B. (1995) Sec-dependent thylakoid protein translocation: ΔpH-requirement is dictated by passenger protein and ATP concentration. J. Biol. Chem. 270, 23 275-23 281.
30. Michl, D., Robinson, C., Shackleton, J. B., Herrmann, R. G. & Klösgen, R. B. (1994) Targeting of proteins to the thylakoids by bipartite presequences: CFoII is imported by a novel, third pathway, EMBO J. 13, 1310-1317.
31. Miller, J. D., Bernstein, H. D. & Walter, P. (1994) Interaction of E coli Ffh/4.5S ribonucleoprotein and FtsY mimics that of mammalian signal recognition particle and its receptor, Nature 367, 657-659.
32. Mould, R. M., Shackleton, J. B. & Robinson, C. (1991) Protein transport into chloroplasts: requirement for the efficient import of two lumenal oxygen-evolving complex proteins into isolated thylakoids, J. Biol. Chem. 266, 17 286-17 290.
33. Nakai, M., Tanaka, A., Omata, T. & Endo, T. (1992) Cloning and characterization of the secY gene from the cyanobacterium Synechococcus PCC7942, Biochim. Biophys. Acta 1171, 113-116.
34. Nakai, M., Nohara, T., Sugita, D. & Endo, T. (1994) Identification and characterization of the secA protein homologue in the cyanobacterium Synechococcus PCC7942, Biochem. Biophys. Res. Commun. 200, 844-851.
35. Nielsen, V. S., Mant, A., Knoetzel, J., Lindberg Møller, B. & Robinson, C. (1994) Import of barley photosystem I subunit N into the thylakoid lumen is mediated by a bipartite presequence lacking an intermediate cleavage site: role of the ΔpH in translocation across the thylakoid membrane, J. Biol. Chem. 269, 3762-3766.
36. Nohara, T., Nakai, M., Goto, A. & Endo, T. (1995) Isolation and characterization of the cDNA for pea chloroplast SecA. Evolutionary conservation of the bacterial-type SecA-dependent protein transport within chloroplasts, FEBS Lett. 364, 305-308.
37. Oelmüller, R., Herrmann, R. G. & Pakrasi, H. B. (1996) Molecular studies of CtpA, the carboxy-terminal processing protease for the D1 protein of the photosystem II reaction center in higher plants, J. Biol. Chem. 271, 21 848-21 852.
38. Oliver, D. B., Cabelli, R. J., Dolan, K. M. & Jarosik, G. P. (1990) Azide-resistant mutants of Escherichia coli alter the SecA protein, an azide-sensitive component of the protein export machinery. Proc. Natl Acad. Sci. USA 87, 8227-8231.
39. Pugsley, A. P. (1993) The complete general secretory pathway in gram-negative bacteria, Microbiol. Rev. 57, 50-108.
40. Robinson, C., Cai, D., Hulford, A., Brock, I. W., Michl, D., Hazell, L., Schmidt, I., Herrmann, R. G. & Klösgen, R. B. (1994) The presequence of a chimeric construct dictates which of two mechanisms are utilised for translocation across the thylakoid membrane: evidence for the existence of two distinct translocation systems, EMBO J. 13, 279-285.
41. Robinson, D., Karnauchov, I., Herrmann, R. G., Klösgen, R. B. & Robinson, C. (1996) Protease-sensitive thylakoidal import machinery for the Sec-. ΔpH- and signal recognition particle-dependent protein targeting pathways, but not for CFo-II integration, Plant J. 10, 149-155.
42. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989) Molecular cloning. A laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
43. Sanger, F., Nicklen, S. & Coulson, A. R. (1977) DNA sequencing with chain terminating inhibitors, Proc. Natl Acad. Sci. USA 74, 5463-5467.
44. Shestakov, S. V., Anbudurai, P. R., Stunbekova, G. E., Gadzhiev, A., Lind, L. K. & Pakrasi, H. B. (1994) Molecular cloning and characterization of the ctpA gene encoding a carboxyl-terminal processing protease. Analysis of a spontaneous photosystem II-deficient mutant strain of the cyanobacterium Synechocystis sp. PCC 6803, J. Biol. Chem. 269, 19 354-19 359.
45. Theg, S., Bauerle, C., Olsen, L., Selman, B. & Keegstra, K. (1989) Internal ATP is the only energy requirement for the translocation of precursor proteins across chloroplastic membranes, J. Biol. Chem. 264, 6730-6736.
46. Viitanen, P. V., Doran, K. R. & Dunsmuir, P. (1988) What is the role of the transit peptide in thylakoid integration of the light-harvesting chlorophyll a/b protein? J. Biol. Chem. 263, 15 000-15 007.
47. von Heijne, G. (1985) Signal sequences. The limits of variation, J. Mol. Biol. 184, 99-105.
48. Yuan, J. & Cline, K. (1994) Plastocyanin and the 33 kDa subunit of the oxygen-evolving complex are transported into thylakoids with similar requirements as predicted from pathway specificity. J. Biol. Chem. 269, 18 463-18 467.
49. Yuan, J., Henry, R., McCaffery, M. & Cline, K. (1994) SecA homolog in protein transport within chloroplasts: evidence for endosymbiont-derived sorting, Science 266, 796-798.