N-terminal lysines are essential for protein translocation via a modified ERAD system in complex plastids

Molecular Microbiology

Volumn 96, Issue 3, 2015, Pages 609-620

  Lau, Julia B ^a   Stork, Simone ^a   Moog, Daniel ^a,b   Sommer, Maik S ^c   Maier, Uwe G ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b DALHOUSIE UNIVERSITY   (Canada)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LYSINE; ALGAL PROTEIN; LYSIN; MUCOPROTEIN;

AMINO ACID COMPOSITION; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE TRANSPORT; COMPLEX FORMATION; COMPUTER MODEL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; IN VIVO STUDY; MOLECULAR DYNAMICS; NONHUMAN; PERIPLASTIDAL MEMBRANE; PLASTID MEMBRANE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TARGETING; PROTEIN TRANSPORT; SYMBIONT SPECIFIC ERAD LIKE MACHINERY; UBIQUITINATION; BIOLOGICAL MODEL; INTRACELLULAR MEMBRANE; METABOLISM; PLASTID; RED ALGA;

ALGAE;

ALGAL PROTEINS; INTRACELLULAR MEMBRANES; MODELS, BIOLOGICAL; MUCOPROTEINS; PLASTIDS; PROTEIN TRANSPORT; RHODOPHYTA;

EID: 84928425570     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12959     Document Type: Article

References (41)

1. Agrawal, S., van Dooren, G.G., Beatty, W.L., and Striepen, B. (2009) Genetic evidence that an endosymbiont-derived endoplasmic reticulum-associated protein degradation (ERAD) system functions in import of apicoplast proteins. J Biol Chem 284: 33683-33691.
2. Agrawal, S., Chung, D.W., Ponts, N., van Dooren, G.G., Prudhomme, J., Brooks, C.F., etal. (2013) An apicoplast localized ubiquitylation system is required for the import of nuclear-encoded plastid proteins. PLoS Pathog 9: e1003426.
3. Apt, K.E., Kroth-Pancic, P.G., and Grossman, A.R. (1996) Stable nuclear transformation of the diatom Phaeodactylum tricornutum. Mol Gen Genet 252: 572-579.
4. Bendtsen, J.D., Nielsen, H., von Heijne, G., and Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795.
5. Bolte, K., Gruenheit, N., Felsner, G., Sommer, M.S., Maier, U.G., and Hempel, F. (2011) Making new out of old: recycling and modification of an ancient protein translocation system during eukaryotic evolution. Mechanistic comparison and phylogenetic analysis of ERAD, SELMA and the peroxisomal importomer. Bioessays. 33: 368-376.
6. Bowler, C., Allen, A.E., Badger, J.H., Grimwood, J., Jabbari, K., Kuo, A., etal. (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456: 239-244.
7. Brodsky, J.L. (2012) Cleaning up: ER-associated degradation to the rescue. Cell 151: 1163-1167.
8. Cabantous, S., Terwilliger, T.C., and Waldo, G.S. (2005) Protein tagging and detection with engineered selfassembling fragments of green fluorescent protein. Nat Biotechnol 23: 102-107.
9. Chen, Z., Chen, Y.Z., Wang, X.F., Wang, C., Yan, R.X., and Zhang, Z. (2011) Prediction of ubiquitination sites by using the composition of k-spaced amino acid pairs. PLoS ONE 6: e22930.
10. Claessen, J.H., Kundrat, L., and Ploegh, H.L. (2012) Protein quality control in the ER: balancing the ubiquitin checkbook. Trends Cell Biol 22: 22-32.
11. Curtis, B.A., Tanifuji, G., Burki, F., Gruber, A., Irimia, M., Maruyama, S., etal. (2012) Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492: 59-65.
12. Eilers, M., and Schatz, G. (1986) Binding of a specific ligand inhibits import of a purified precursor protein into mitochondria. Nature 322: 228-232.
13. Emanuelsson, O., Nielsen, H., Brunak, S., and von Heijne, G. (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005-1016.
14. Felsner, G., Sommer, M.S., Gruenheit, N., Hempel, F., Moog, D., Zauner, S., etal. (2010) ERAD components in organisms with complex red plastids suggest recruitment of a preexisting protein transport pathway for the periplastid membrane. Genome Biol Evol 3: 140-150.
15. Foth, B.J., Ralph, S.A., Tonkin, C.J., Struck, N.S., Fraunholz, M., Roos, D.S., etal. (2003) Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299: 705-708.
16. Gould, S.B., Sommer, M.S., Kroth, P.G., Gile, G.H., Keeling, P.J., and Maier, U.G. (2006) Nucleus-to-nucleus gene transfer and protein retargeting into a remnant cytoplasm of cryptophytes and diatoms. Mol Biol Evol 23: 2413-2422.
17. Gould, S.B., Waller, R.F., and McFadden, G.I. (2008) Plastid evolution. Annu Rev Plant Biol 59: 491-517.
18. Gschloessl, B., Guermeur, Y., and Cock, J.M. (2008) HECTAR: a method to predict subcellular targeting in heterokonts. BMC Bioinform 9: 393.
19. Hampton, R.Y., and Sommer, T. (2012) Finding the will and the way of ERAD substrate retrotranslocation. Curr Opin Cell Biol 24: 460-466.
20. Heiny, S.R., Pautz, S., Recker, M., and Przyborski, J.M. (2014) Protein traffic to the Plasmodium falciparum apicoplast: evidence for a sorting branch point at the Golgi. Traffic 15: 1290-1304.
21. Hempel, F., Bullmann, L., Lau, J., Zauner, S., and Maier, U.G. (2009) ERAD-derived preprotein transport across the second outermost plastid membrane of diatoms. Mol Biol Evol 26: 1781-1790.
22. Hempel, F., Felsner, G., and Maier, U.G. (2010) New mechanistic insights into pre-protein transport across the second outermost plastid membrane of diatoms. Mol Microbiol 76: 793-801.
23. Hirakawa, Y., Burki, F., and Keeling, P.J. (2012) Genome-based reconstruction of the protein import machinery in the secondary plastid of a chlorarachniophyte alga. Eukaryot Cell 11: 324-333.
24. Keeling, P.J. (2013) The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu Rev Plant Biol 64: 583-607.
25. Kilian, O., and Kroth, P.G. (2005) Identification and characterization of a new conserved motif within the presequence of proteins targeted into complex diatom plastids. Plant J 41: 175-183.
26. Martin, W. (2010) Evolutionary origins of metabolic compartmentalization in eukaryotes. Philos Trans R Soc Lond B Biol Sci 365: 847-855.
27. Mehnert, M., Sommer, T., and Jarosch, E. (2014) Der1 promotes movement of misfolded proteins through the endoplasmic reticulum membrane. Nat Cell Biol 16: 77-86.
28. Moog, D., Stork, S., Zauner, S., and Maier, U.G. (2011) In silico and in vivo investigations of proteins of a minimized eukaryotic cytoplasm. Genome Biol Evol 3: 375-382.
29. Peschke, M., Moog, D., Klingl, A., Maier, U.G., and Hempel, F. (2013) Evidence for glycoprotein transport into complex plastids. Proc Natl Acad Sci USA 110: 10860-10865.
30. Ponts, N., Saraf, A., Chung, D.W., Harris, A., Prudhomme, J., Washburn, M.P., Florens, L., and Le Roch, K.G. (2011) Unraveling the ubiquitome of the human malaria parasite. J Biol Chem 286: 40320-40330.
31. Radivojac, P., Vacic, V., Haynes, C., Cocklin, R.R., Mohan, A., Heyen, J.W., etal. (2010) Identification, analysis, and prediction of protein ubiquitination sites. Proteins 78: 365-380.
32. Rapoport, T.A. (2007) Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450: 663-669.
33. Sato, S. (2011) The apicomplexan plastid and its evolution. Cell Mol Life Sci 68: 1285-1296.
34. Schleiff, E., and Becker, T. (2011) Common ground for protein translocation: access control for mitochondria and chloroplasts. Nat Rev Mol Cell Biol 12: 48-59.
35. Schuberth, C., and Buchberger, A. (2005) Membrane-bound Ubx2 recruits Cdc48 to ubiquitin ligases and their substrates to ensure efficient ER-associated protein degradation. Nat Cell Biol 7: 999-1006.
36. Sommer, M.S., Gould, S.B., Lehmann, P., Gruber, A., Przyborski, J.M., and Maier, U.G. (2007) Der1-mediated preprotein import into the periplastid compartment of chromalveolates? Mol Biol Evol 24: 918-928.
37. Stein, A., Ruggiano, A., Carvalho, P., and Rapoport, T.A. (2014) Key steps in ERAD of luminal ER proteins reconstituted with purified components. Cell 158: 1375-1388.
38. Stork, S., Moog, D., Przyborski, J.M., Wilhelmi, I., Zauner, S., and Maier, U.G. (2012) Distribution of the SELMA translocon in secondary plastids of red algal origin and predicted uncoupling of ubiquitin-dependent translocation from degradation. Eukaryot Cell 11: 1472-1481.
39. Tung, C.W., and Ho, S.Y. (2008) Computational identification of ubiquitylation sites from protein sequences. BMC Bioinform 9: 310.
40. Wittig, I., Braun, H.P., and Schagger, H. (2006) Blue native PAGE. Nat Protoc 1: 418-428.
41. Zimorski, V., Ku, C., Martin, W.F., and Gould, S.B. (2014) Endosymbiotic theory for organelle origins. Curr Opin Microbiol 22C: 38-48.