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

Molecular Biology of the Cell

Volumn 8, Issue 5, 1997, Pages 923-934

  Clark, Sonya A ^a,b   Theg, Steven M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PLANT GENE EXPRESSION CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VEGETABLE PROTEIN;

ARTICLE; CHLOROPLAST; CROSS LINKING; MEMBRANE TRANSPORT; NONHUMAN; PHOTOSYSTEM II; PHYTOCHEMISTRY; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; THYLAKOID MEMBRANE;

BOVINAE;

EID: 0030918441     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.8.5.923     Document Type: Article

References (48)

1. Alefsen, H., Waegemann, K., and Soll, J. (1994). Analysis of the chloroplast protein import machinery. J. Plant Physiol. 144, 339-345.
2. America, T., Hageman, J., Guéra, A., Rook, F., Archer, K., Keegstra, K., and Weisbeek, P. (1994). Methotrexate does not block import of a DHFR fusion protein into chloroplasts. Plant Mol. Biol. 24, 283-294.
3. Cline, K., Ettinger, W.F., and Theg, S.M. (1992). Protein-specific energy requirements for protein transport across or into thylakoid membranes. Two lumenal proteins are transported in the absence of ATP. J. Biol. Chem. 267, 2688-2696.
4. Cline, K., Henry, R., Li, C., and Yuan, J. (1993). Multiple pathways for protein transport into or across the thylakoid membrane. EMBO J. 12, 4105-4114.
5. Creighton, A.M., Hulford, A., Mant, A., Robinson, D., and Robinson, C. (1995). A monomeric, tightly folded stromal intermediate on the delta pH-dependent thylakoidal protein transport pathway. J. Biol. Chem. 270, 1663-1669.
6. Creighton, T.E. (1975). The two-disulfide intermediates and the folding pathway of reduced pancreatic trypsin inhibitor. J. Mol. Biol. 95, 167-199.
7. Creighton, T.E. (1977). Effects of urea and guanidine-HCl on the folding and unfolding of pancreatic trypsin inhibitor. J. Mol. Biol. 113, 313-328.
8. Creighton, T.E. (1980). Counting integral numbers of amino acids per polypeptide chain. Nature 284, 487-489.
9. Creighton, T.E., and Goldberg, D.P. (1984). Kinetic role of a metastable native-like two-disulfide species in the folding transition of bovine trypsin inhibitor. J. Mol. Biol. 179, 497-526.
10. della-Cioppa, G., and Kishore, G.M. (1988). Import of a precursor protein into chloroplasts is inhibited by the herbicide glyphosate. EMBO J. 7, 1299-1305.
11. Dworetzky, S.I., Lanford, R.E., and Feldherr, C.M. (1988). The effects of variations in the number and sequence of targeting signals on nuclear uptake. J. Cell Biol. 107, 1279-1287.
12. Eilers, M., Hwang, S., and Schatz, G. (1988). Unfolding and refolding of a purified precursor protein during import into isolated mitochondria. EMBO J. 7, 1139-1145.
13. Eilers, M., and Schatz, G. (1986). Binding of a specific ligand inhibits import of a purified precursor protein into mitochondria. Nature 322, 228-232.
14. Endo, T., Kawakami, M., Goto, A., America, T., Weisbeek, P., and Nakai, M. (1994). Chloroplast protein import: chloroplast envelopes and thylakoids have different abilities to unfold proteins. Eur. J. Biochem. 225, 403-409.
15. Ettinger, W.F., and Theg, S.M. (1991). Physiologically active chloroplasts contain pools of unassembled extrinsic proteins of the photosynthetic oxygen-evolving enzyme complex in the thylakoid lumen. J. Cell Biol. 115, 321-328.
16. Ettinger, W.F., and Theg, S.M. (1992). Sequence of the cDNA encoding the 17-kilodalton protein of the photosynthetic oxygen-evolving complex of pea. Plant Physiol. 99, 791-793.
17. Feldherr, C.M., Kallenbach, E., and Schultz, N. (1984). Movement of a karyophilic proteins through the nuclear pore of oocytes. J. Cell Biol. 99, 2216-2222.
18. Glover, J.R., Andrews, D.W., and Rachubinski, R.A. (1994). Saccharomyces cerevisiae peroxisomal thiolase is imported as a dimer. Proc. Natl. Acad. Sci. USA 91, 10541-10545.
19. Gray, J.C., and Row, P.E. (1995). Protein translocation across the chloroplast envelope membranes. Trends Cell Biol. 5, 243-247.
20. Guéra, A., America, T., van Waas, M., and Weisbeek, P.J. (1993). A strong protein unfolding activity is associated with the binding of precursor chloroplast proteins to chloroplast envelopes. Plant Mol. Biol. 23, 309-324.
21. Hageman, J., Robinson, C., Smeekens, S., and Weisbeek, P. (1986). A thylakoid processing protease is required for complete maturation of the lumen protein plastocyanin. Nature 324, 567-569.
22. Hamman, B.D., and Johnson, A.E. (1996). The internal diameter of the protein translocation pore is greater than 30 angstroms. Mol. Biol. Cell 7(suppl), 436a (Abstract).
23. Hanein, D., Matlack, K.E.S., Jungnickel, B., Plath, K., Kalies, K.U., Miller, K.R., Rapoport, T.A., and Akey, C.W. (1996). Oligomeric rings of the sec61p complex induced by ligands required for protein translocation. Cell 87, 721-732.
24. Hardie, K.R., Schulze, A., Parker, M.W., and Buckley, J.T. (1995). Vibrio spp secrete proaerolysin as a folded dimer without the need for disulfide bond formation. Mol. Microbiol. 17, 1035-1044.
25. Henry, R., Kapazoglou, A., McCaffery, M., and Cline, K. (1994). Differences between lumen targeting domains of chloroplast transit peptides determine pathway specificity for thylakoid transport. J. Biol. Chem. 269, 10189-10192.
26. Jascur, T., Goldenberg, D.P., Vestweber, D., and Schatz, G. (1992). Sequential translocation of an artificial precursor protein across the two mitochondrial membranes. J. Biol. Chem. 267, 13636-13641.
27. Klösgen, R.B., Brock, I.W., Herrmann, R.G., and Robinson, C. (1992). Proton gradient-driven import of the 16 kDa oxygen-evolving complex protein as the full precursor protein by isolated thylakoids. Plant Mol. Biol. 18, 1031-1034.
28. Ko, K., and Ko, Z.W. (1992). Carboxyl-terminal sequences can influence the in vitro import and intraorganellar targeting of chloroplast protein precursors. J. Biol. Chem. 267, 13910-13916.
29. Muller, G., and Zimmermann, R. (1988). Import of honeybee prepromellitin into the endoplasmic reticulum: energy requirements for membrane insertion. EMBO J. 7, 639-648.
30. Nakai, M., Nohara, T., Sugita, D., and Endo, T. (1994). Identification and characterization of the sec-A protein homologue in the cyanobacterium Synechococcus PCC7942. Biochem. Biophys. Res. Commun. 200, 844-851.
31. Nielsen, V.S., Mant, A., Knoetzel, J., Møller, B.L., and Robinson, C. (1994). Import of barley photosystem-I subunit-n into the thylakoid lumen is mediated by a bipartite presequence lacking an intermediate processing site - role of the delta-pH in translocation across the thylakoid membrane. J. Biol. Chem. 269, 3762-3766.
32. Rassow, J., Hartl, F.-U., Guiard, B., Pfanner, N., and Neupert, W. (1990). Polypeptides traverse the mitochondrial envelope in an extended state. FEBS Lett. 275, 190-194.
33. Reed, J.E., Cline, K., Stephens, L.C., Bacot, K.O., and Viitanen, P., V (1990). Early events in the import/assembly pathway of an integral thylakoid protein. Eur. J. Biochem. 194, 33-42.
34. Reinbothe, S., Reinbothe, C., Runge, S., and Apel, K. (1995). Enzymatic product formation impairs both the chloroplast receptor-binding function as well as translocation competence of the NADPH: protochlorophyllide oxidoreductase, a nuclear-encoded plastid precursor protein. J. Cell Biol. 129, 299-308.
35. Reisfeld, R. (1962). Disk electrophoresis of basic proteins and peptides on polyacrylamide gels. Nature 195, 281-283.
36. Roffey, R.A., and Theg, S.M. (1996). Analysis of the import of the carboxyl-terminal truncations of the 23-kilodalton subunit of the oxygen-evolving complex suggests that its structure is an important determinant for thylakoid transport. Plant Physiol. 111, 1329-1338.
37. Schatz, G., and Dobberstein, B. (1996). Common principles of protein translocation across membranes. Science 271, 1519-1525.
38. H+ and ATP function at different steps of the catalytic cycle of preprotein translocase. Cell 64, 927-939.
39. Schnell, D.J., and Blobel, G. (1993). Identification of intermediates in the pathway of protein import into chloroplasts and their localization to envelope contact sites. J. Cell Biol. 120, 103-115.
40. Scott, S.V., and Theg, S.M. (1996). A new chloroplast protein import intermediate reveals distinct reveals distinct translocation machineries in the two envelope membranes: energetics and mechanistic implications. J. Cell Biol. 132, 63-75.
41. Shackleton, J.B., and Robinson, C. (1991). Transport of proteins into chloroplasts: the thylakoidal processing peptidase is a signal-type peptidase with stringent substrate requirements at the -3 and -1 positions. J. Biol. Chem. 266, 12152-12156.
42. Tani, K., and Mizushima, S. (1991). A chemically cross-linked non-linear proOmpA molecule can be translocated into everted membrane vesicles of Escherichia coli in the presence of the proton motive force. FEBS Lett. 285, 127-131.
43. Theg, S.M., and Scott, S.V. (1993). Protein import into chloroplasts. Trends Cell Biol. 3, 186-190.
44. Vestweber, D., and Schatz, G. (1988). A chimeric mitochondrial precursor protein with internal disulfide bridges blocks import of authentic precursors into mitochondria and allows quantitation of import sites. J. Cell Biol. 107, 2037-2043.
45. Walton, P.A., Hill, P.E., and Subramani, S. (1995). Import of stably folded proteins into peroxisomes. Mol. Biol. Cell 6, 675-683.
46. Wolfe, P.B., and Wickner, W. (1984). Bacterial leader peptidase, a membrane protein without a leader peptide, uses the same export pathway as presecretory proteins. Cell 36, 1067-1072.
47. Wu, C., Seibert, S.S., and Ko, K. (1994). Identification of chloroplast envelope proteins in close physical proximity to a partially translocated chimeric precursor. J. Biol. Chem. 269, 32264-32271.
48. Yuan, J., Henry, R., McCaffery, M., and Cline, K. (1994). SecA homolog in protein transport within chloroplasts: evidence for endosymbiont derived sorting. Science 266, 796-798.