The invariant phenylalanine of precursor proteins discloses the importance of Omp85 for protein translocation into cyanelles

BMC Evolutionary Biology

Volumn 7, Issue 1, 2007, Pages

  Wunder, Tobias ^a   Martin, Roman ^a   Löffelhardt, Wolfgang ^b   Schleiff, Enrico ^a,c   Steiner, Jürgen M ^b  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF VIENNA   (Austria)

^c Department of Biosciences ^*  (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID BINDING PROTEIN; MEMBRANE PROTEIN; OMP85 PROTEIN; PHENYLALANINE; PROTEIN DERIVATIVE; PROTEIN PRECURSOR; UNCLASSIFIED DRUG; ALGAL PROTEIN; FERREDOXIN NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE REDUCTASE; LIPOSOME; OUTER MEMBRANE PROTEIN;

ALGA; ARTICLE; CYANELLE; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; GENE TRANSFER; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASTID; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN TRANSPORT; PROTEOLIPOSOME; ACTIVE TRANSPORT; ANABAENA; CYANOPHORA; DIATOM; METABOLISM; PROTEIN BINDING; RED ALGA;

ALGAE; BACTERIA (MICROORGANISMS); CYANOBACTERIA; EMBRYOPHYTA; GLAUCOCYSTOPHYCEAE; PROKARYOTA;

ACTIVE TRANSPORT, CELL NUCLEUS; ALGAE; ALGAE, RED; ALGAL PROTEINS; ANABAENA; BACTERIAL OUTER MEMBRANE PROTEINS; CYANOPHORA; DIATOMS; FERREDOXIN-NADP REDUCTASE; LIPOSOMES; PHENYLALANINE; PLASTIDS; PROTEIN BINDING; PROTEIN PRECURSORS; PROTEIN TRANSPORT;

EID: 38849128215     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-7-236     Document Type: Article

References (47)

1. Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. N Rodriguez-Ezpeleta H Brinkmann SC Burey B Roure G Burger W Löffelhardt HJ Bohnert H Philippe BF Lang, Curr Biol 2005 15 1325 1330 10.1016/j.cub.2005.06.040 16051178
2. Gene transfer to the nucleus and the evolution of chloroplasts. W Martin B Stoebe V Goremykin S Hapsmann M Hasegawa KV Kowallik, Nature 1998 393 162 165 10.1038/30234 11560168
3. The cyanelle (muroplast) of Cyanophora paradoxa : a paradigm for endosymbiotic organelle evolution. W Löffelhardt HJ Bohnert, Symbiosis Dordrecht: Kluwer Academic Publishers, Seckbach, J, 2001 111 130
4. Evolution: red algal genome affirms a common origin of all plastids. GI McFadden GG van Dooren, Curr Biol 2004 14 R514 R516 10.1016/j.cub.2004.06.041 15242632
5. N-acetylputrescine as a characteristic constituent of cyanelle peptidoglycan in glaucocystophyte algae. B Pfanzagl G Allmaier ER Schmid MA de Pedro W Löffelhardt, J Bacteriol 1996 178 6994 6997 8955325
6. Transit peptide diversity and divergence: a global analysis of plastid targeting signals. NJ Patron RF Waller, Bioessays 2007 29 1048 1058 10.1002/bies.20638 17876808
7. Protein translocation into and within cyanelles. JM Steiner W Löffelhardt, Mol Membr Biol 2005 22 123 132 10.1080/09687860500041411 16092530
8. Homologous protein import machineries in chloroplasts and cyanelles. JM Steiner F Yusa JA Pompe W Löffelhardt, Plant J 2005 44 646 652 10.1111/j.1365-313X.2005.02559.x 16262713
9. Protein targeting into complex diatom plastids:functional characterization of a specific targeting motif. A Gruber S Vugrinec F Hempel SB Gould UG Maier PG Kroth, Plant Mol Biol 2007 64 519 530 10.1007/s11103-007-9171- x 17484021
10. Protein targeting into the complex plastid of cryptophytes. SB Gould MS Sommer K Hadfi S Zauner PG Kroth UG Maier, J Mol Evol 2006 62 674 681 10.1007/s00239-005-0099-y 16752208
11. Generation of 10,154 Expressed Sequence Tags from a Leafy Gametophyte of a Marine Red Alga, Porphyra yezoensis. I Nikaido E Asamizu M Nakajima Y Nakamura N Saga S Tabata, DNA Research 2000 7 223 227 10.1093/dnares/7.3.223 10907854
12. The β-barrel shaped polypeptide transporter, an old concept for precursor protein transfer across membranes. W Löffelhardt A von Haeseler E Schleiff, Symbiosis 2007 44 33 42
13. The role of lipids in plastid protein transport. BD Bruce, Plant Mol Biol 1998 38 223 246 10.1023/A:1006094308805 9738969
14. Chloroplast transit peptides: structure, function and evolution. BD Bruce, Trends Cell Biol 2000 10 440 447 10.1016/S0962-8924(00)01833-X 10998602
15. Properties of integral membrane protein structures: derivation of an implicit membrane potential. MB Ulmschneider MS Sansom A Di Nola, Proteins 2005 59 252 265 10.1002/prot.20334 15723347
16. Interactions controlling the membrane binding of basic protein domains: phenylalanine and the attachment of the myristoylated alanine-rich C-kinase substrate protein to interfaces. K Victor J Jacob DS Cafiso, Biochem 1999 38 12527 12536 10.1021/bi990847b
17. Structure of the monomeric outer-membrane porin OmpG in the open and closed conformation. O Yildiz KR Vinothkumar P Goswami W Kühlbrandt, EMBO J 2006 25 3702 3713 16888630 10.1038/sj.emboj.7601237
18. Crystal structure of osmoporin OmpC from E. coli at 2.0 Å A Basle G Rummel P Storici JP Rosenbusch T Schirmer, J Mol Biol 2006 362 933 942 10.1016/j.jmb.2006.08.002 16949612
19. Substrate recognition by the AAA+ chaperone ClpB. C Schlieker J Weibezahn H Patzelt P Tessarz C Strub K Zeth A Erbse J Schneider-Mergener JW Chin PG Schultz B Bukau A Mogk, Nat Struct Mol Biol 2004 11 607 615 10.1038/nsmb787 15208691
20. Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. M Struyve M Moons J Tommassen, J Mol Biol 1991 218 141 148 10.1016/0022-2836(91)90880-F 1848301
21. Assembly factor Omp85 recognizes its outer membrane protein substrates by a species-specific C-terminal motif. V Robert EB Volokhina F Senf MP Bos P Van Gelder J Tommassen, PLoS Biol 2006 4 e377 17090219 10.1371/journal.pbio.0040377
22. http://bacteria.kazusa.or.jp/cyanobase
23. Membrane heredity and early chloroplast evolution. T Cavalier-Smith, Trends Plant Sci 2000 5 174 182 10.1016/S1360-1385(00)01598-3 10740299
24. Endosymbiosis and evolution of the plant cell. GI McFadden, Curr Opin Plant Biol 1999 2 513 519 10.1016/S1369-5266(99)00025-4 10607659
25. Molecular machinery for non-vesicular trafficking of ceramide. K Hanada K Kumagai S Yasuda Y Miura M Kawano M Fukasawa M Nishijima, Nature 2003 426 803 809 10.1038/nature02188 14685229
26. Hiding behind hydrophobicity. Transmembrane segments in mass spectrometry. LA Eichacker B Granvogl O Mirus BC Müller C Miess E Schleiff, J Biol Chem 2004 279 50915 50922 10.1074/jbc.M405875200 15452135
27. The evolutionarily related beta-barrel polypeptide transporters from Pisum sativum and Nostoc PCC7120 contain two distinct functional domains. F Ertel O Mirus R Bredemeier S Moslavac T Becker E Schleiff, J Biol Chem 2005 280 28281 28289 10.1074/jbc.M503035200 15951438
28. Functional and phylogenetic properties of the pore-forming beta-barrel transporters of the Omp85 family. R Bredemeier T Schlegel F Ertel A Vojta L Borissenko MT Bohnsack M Groll A von Haeseler E Schleiff, J Biol Chem 2007 282 1882 1890 10.1074/jbc.M609598200 17088246
29. In vitro interaction between a chloroplast transit peptide and chloroplast outer envelope lipids is sequence-specific and lipid class-dependent. P Pinnaduwage BD Bruce, J Biol Chem 1996 271 32907 32915 10.1074/jbc.271.51.32907 8955132
30. Transit sequence-dependent binding of the chloroplast precursor protein ferredoxin to lipid vesicles and its implications for membrane stability. R van 't Hof B de Kruijff, FEBS Lett 1995 361 35 40 10.1016/0014-5793(95)00135-V 7890037
31. Biophysical characterization of a transit peptide directing chloroplast protein import. SM Theg FJ Geske, Biochem 1992 31 5053 5060 10.1021/bi00136a018
32. The secondary structure of the ferredoxin transit sequence is modulated by its interaction with negatively charged lipids. L Horniak M Pilon R van 't Hof B de Kruijff, FEBS Lett 1993 334 241 246 10.1016/0014-5793(93)81720-K 8224253
33. Biogenesis of the Gram-negative bacterial outer membrane. MP Bos J Tommassen, Curr Opin Microbiol 2004 7 61061 6 10.1016/j.mib.2004.10.011
34. Membrane protein insertion: mixing eukaryotic and prokaryotic concepts. E Schleiff J Soll, EMBO Rep 2005 6 1023 1027 16264426 10.1038/sj.embor.7400563
35. Molecular architecture and function of the Omp85 family of proteins. IE Gentle L Burri T Lithgow, Mol Microbiol 2005 58 1216 1225 16313611
36. POTRA: a conserved domain in the FtsQ family and a class of beta-barrel outer membrane proteins. L Sanchez-Pulido D Devos S Genevrois M Vicente A Valencia, Trends Biochem Sci 2003 28 523 526 10.1016/j.tibs.2003.08.003 14559180
37. A polyglycine stretch is necessary for proper targeting of the protein translocation channel precursor to the outer envelope membrane of chloroplasts. K Inoue K Keegstra, Plant J 2003 34 661 669 10.1046/j.1365-313X.2003.01755.x 12787247
38. Conserved pore-forming regions in polypeptide-transporting proteins. S Moslavac O Mirus R Bredemeier J Soll A von Haeseler E Schleiff, FEBS J 2005 272 1367 1378 10.1111/j.1742-4658.2005.04569.x 15752354
39. A derivative of lipid A is involved in signal recognition particle/SecYEG-dependent and -independent membrane integrations. K Nishiyama A Ikegami M Moser E Schiltz H Tokuda M Müller, J Biol Chem 2006 281 35667 35676 10.1074/jbc.M608228200 17008318
40. Protein import into chloroplasts. J Soll E Schleiff, Nat Rev Mol Cell Biol 2004 5 198 208 10.1038/nrm1333 14991000
41. Determination of liposome size: a tool for protein reconstitution. A Vojta J Scheuring N Neumaier O Mirus S Weinkauf E Schleiff, Anal Biochem 2005 347 24 33 10.1016/j.ab.2005.09.003 16236237
42. Lipid composition of outer leaflet of chloroplast outer envelope determines topology of OEP7. E Schleiff R Tien M Salomon J Soll, Mol Biol Cell 2001 12 4090 4102 11739803
43. http://genome.jgi-psf.org/Phatr2/Phatr2.home.html
44. http://merolae.biol.s.u-tokyo.ac.jp/
45. http://align.bmr.kyushu-u.ac.jp/mafft/online/server/
46. Improvement in accuracy of multiple sequence alignment using novel group-to-group sequence alignment algorithm with piecewise linear gap cost. S Yamada O Gotoh H Yamana, BMC Bioinformatics 2006 7 524 17137519 10.1186/1471-2105-7-524
47. http://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi