Protein-protein interactions indicate composition of a 480 kDa SELMA complex in the second outermost membrane of diatom complex plastids

Molecular Microbiology

Volumn 100, Issue 1, 2016, Pages 76-89

  Lau, Julia B ^a   Stork, Simone ^a   Moog, Daniel ^a,b   Schulz, Julian ^a   Maier, Uwe G ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEINS AND BINDING PROTEINS; CELL CYCLE PROTEIN; DERLIN PROTEIN; MEMBRANE PROTEIN; PROTEIN CDC48; PROTEIN RHOM1; PROTEIN RHOM3; PROTEIN UBX; PROTEINASE; UNCLASSIFIED DRUG; MULTIPROTEIN COMPLEX; PROTEIN BINDING;

ARTICLE; COMPUTER MODEL; CONTROLLED STUDY; DIATOM; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; PLASTID; PREDICTION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY; SYMBIONT SPECIFIC ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION LIKE MACHINERY; AMINO ACID SEQUENCE; GENETICS; INTRACELLULAR MEMBRANE; METABOLISM; PROTEIN ANALYSIS; PROTEIN TRANSPORT;

AMINO ACID SEQUENCE; DIATOMS; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; INTRACELLULAR MEMBRANES; MULTIPROTEIN COMPLEXES; PLASTIDS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN TRANSPORT;

EID: 84956908726     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13302     Document Type: Article

References (49)

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., Rodrigues, E.M., Tan, J.C., et al. (2013) An apicoplast localized ubiquitylation system is required for the import of nuclear-encoded plastid proteins. PLoS Pathog 9: e1003426.
3. Alberts, S.M., Sonntag, C., Schäfer, A., and Wolf, D.H. (2009) Ubx4 modulates cdc48 activity and influences degradation of misfolded proteins of the endoplasmic reticulum. J Biol Chem 284: 16082-16089.
4. 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.
5. Bagola, K., Mehnert, M., Jarosch, E., and Sommer, T. (2011) Protein dislocation from the ER. Biochim Biophys Acta 1808: 925-936.
6. 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.
7. Bernsel, A., Viklund, H., Hennerdal, A., and Elofsson, A. (2009) TOPCONS: consensus prediction of membrane protein topology. Nucleic Acids Res 37: W465-W468.
8. Bolte, K., Bullmann, L., Hempel, F., Bozarth, A., Zauner, S., and Maier, U.G. (2009) Protein targeting into secondary plastids. J Eukaryot Microbiol 56: 9-15.
9. 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.
10. Brossier, F., Jewett, T.J., Sibley, L.D., and Urban, S. (2005) A spatially localized rhomboid protease cleaves cell surface adhesins essential for invasion by Toxoplasma. Proc Natl Acad Sci USA 102: 4146-4151.
11. Cabantous, S., Terwilliger, T.C., and Waldo, G.S. (2005) Protein tagging and detection with engineered self-assembling fragments of green fluorescent protein. Nat Biotechnol 23: 102-107.
12. Cavalier-Smith, T. (1999) Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 46: 347-366.
13. Chen, C.Y., Malchus, N.S., Hehn, B., Stelzer, W., Avci, D., Langosch, D., and Lemberg, M.K. (2014) Signal peptide peptidase functions in ERAD to cleave the unfolded protein response regulator XBP1u. EMBO J 33: 2492-2506.
14. Daboussi, F., Leduc, S., Maréchal, A., Dubois, G., Guyot, V., Perez-Michaut, C., et al.(2014) Genome engineering empowers the diatom Phaeodactylum tricornutum for biotechnology. Nat Commun 5: 3831.
15. Dowse, T.J. and Soldati, D. (2005) Rhomboid-like proteins in Apicomplexa: phylogeny and nomenclature. Trends Parasitol 21: 254-258.
16. Dowse, T.J., Pascall, J.C., Brown, K.D., and Soldati, D. (2005) Apicomplexan rhomboids have a potential role in microneme protein cleavage during host cell invasion. Int J Parasitol 35: 747-756.
17. Felsner, G., Sommer, M.S., Gruenheit, N., Hempel, F., Moog, D., Zauner, S., Martin, W., and Maier, U.G. (2011) 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.
18. Fleig, L., Bergbold, N., Sahasrabudhe, P., Geiger, B., Kaltak, L., and Lemberg, M.K. (2012) Ubiquitin-dependent intramembrane rhomboid protease promotes ERAD of membrane proteins. Mol Cell 47: 558-569.
19. Gould, S.B., Waller, R.F., and McFadden, G.I. (2008) Plastid evolution. Ann Rev Plant Biol 59: 491-517.
20. Gould, S.B., Maier, U.G., and Martin, W.F. (2015) Protein Import and the Origin of Red Complex Plastids. Curr Biol 25: R515-R521.
21. Greenblatt, E.J., Olzmann, J.A., and Kopito, R.R. (2012) Making the cut: intramembrane cleavage by a rhomboid protease promotes ERAD. Nat Struct Mol Biol 19: 979-981.
22. Gruber, A., Vugrinec, S., Hempel, F., Gould, S.B., Maier, U.G., and Kroth, P.G. (2007) Protein targeting into complex diatom plastids: functional characterisation of a specific targeting motif. Plant Mol Biol 64: 519-530.
23. Hampton, R.Y. and Sommer, T. (2012) Finding the will and the way of ERAD substrate retrotranslocation. Curr Opin Cell Biol 24: 460-466.
24. 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.
25. 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.
26. Kerppola, T.K. (2006) Visualization of molecular interactions by fluorescence complementation. Nat Rev Mol Cell Biol 7: 449-456.
27. 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.
28. Kilian, O., Benemann, C.S., Niyogi, K.K., and Vick, B. (2011) High-efficiency homologous recombination in the oil-producing alga Nannochloropsis sp. Proc Natl Acad Sci USA 108: 21265-21269.
29. Lau, J.B., Stork, S., Moog, D., Sommer, M.S., and Maier, U.G. (2015) N-terminal lysines are essential for protein translocation via a modified ERAD system in complex plastids. Mol Microbiol 96: 609-620.
30. Lin, J.W., Meireles, P., Prudêncio, M., Engelmann, S., Annoura, T., Sajid, M. et al. (2013) Loss-of-function analyses defines vital and redundant functions of the Plasmodium rhomboid protease family. Mol Microbiol 88: 318-338.
31. Marchler-Bauer, A., Lu, S., Anderson, J.B., Chitsaz, F., Derbyshire, M.K., DeWeese-Scott, C. et al. (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39: D225-D229.
32. Martin, W. (2010) Evolutionary origins of metabolic compartmentalization in eukaryotes. Philos Trans R Soc Lond B Biol Sci 365: 847-855.
33. 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.
34. O'Donnell, R.A., Hackett, F., Howell, S.A., Treeck, M., Struck, N., Krnajski, Z. et al. (2006) Intramembrane proteolysis mediates shedding of a key adhesin during erythrocyte invasion by the malaria parasite. J Cell Biol 174: 1023-1033.
35. 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.
36. Petersen, J., Ludewig, A.K., Michael, V., Bunk, B., Jarek, M., Baurain, D., and Brinkmann, H. (2014) Chromera velia, endosymbioses and the rhodoplex hypothesis-plastid evolution in cryptophytes, alveolates, stramenopiles, and haptophytes (CASH lineages). Genome Biol Evol 6: 666-684.
37. Schliebs, W., Girzalsky, W., and Erdmann, R. (2010) Peroxisomal protein import and ERAD: variations on a common theme. Nat Rev Mol Cell Biol 11: 885-890.
38. 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.
39. Schuberth, C. & Buchberger, A. (2008) UBX domain proteins: major regulators of the AAA ATPase Cdc48/p97. Cell Mol Life Sci 65: 2360-2371.
40. Smith, M.H., Ploegh, H.L., and Weissman, J.S. (2011) Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science 334: 1086-1090.
41. 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.
42. 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.
43. Stork, S., Lau, J., Moog, D., and Maier, U.G. (2013) Three old and one new: protein import into red algal-derived plastids surrounded by four membranes. Protoplasma 250: 1013-1023.
44. Strisovsky, K., Sharpe, H.J., and Freeman, M. (2009) Sequence-specific intramembrane proteolysis: identification of a recognition motif in rhomboid substrates. Mol Cell 36: 1048-1059.
45. Urban, S. (2006) Rhomboid proteins: conserved membrane proteases with divergent biological functions. Genes Dev 20: 3054-3068.
46. Urban, S. (2010) Taking the plunge: integrating structural, enzymatic and computational insights into a unified model for membrane-immersed rhomboid proteolysis. Biochem J 425: 501-512.
47. Weyman, P.D., Beeri, K., Lefebvre, S.C., Rivera, J., McCarthy, J.K., Heuberger, A.L., et al. (2015) Inactivation of Phaeodactylum tricornutum urease gene using transcription activator-like effector nuclease-based targeted mutagenesis. Plant Biotechnol J 13: 460-470.
48. Wittig, I., Braun, H.P., and Schägger, H. (2006) Blue native PAGE. Nat Protoc 1: 418-428.
49. Zhao, G., Zhou, X., Wang, L., Li, G., Schindelin, H., and Lennarz, W.J. (2007) Studies on peptide: N-glycanase-p97 interaction suggest that p97 phosphorylation modulates endoplasmic reticulum-associated degradation. Proc Natl Acad Sci USA 104: 8785-8790.