Proteomic Amino-Termini Profiling Reveals Targeting Information for Protein Import into Complex Plastids

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Huesgen, Pitter F ^a   Alami, Meriem ^a   Lange, Philipp F ^a   Foster, Leonard J ^a   Schröder, Wolfgang P ^a,b   Overall, Christopher M ^a   Green, Beverley R ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; METHIONYL AMINOPEPTIDASE; PEPTIDASE;

ACETYLATION; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CELL NUCLEUS; CONSENSUS SEQUENCE; CYTOSOL; LIQUID CHROMATOGRAPHY; NONHUMAN; PLASTID; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN TRANSPORT; TANDEM MASS SPECTROMETRY; THALASSIOSIRA PSEUDONANA;

ACETYLATION; CHLOROPLAST PROTEINS; DIATOMS; PLASTIDS; PROTEIN TRANSPORT; PROTEOMICS;

EID: 84884170556     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074483     Document Type: Article

References (45)

1. Armbrust EV, (2009) The life of diatoms in the world's oceans. Nature 459: 185-192. doi:10.1038/nature08057. PubMed: 19444204.
2. Gibbs SP, (1981) The chloroplasts of some algal groups may have evolved from endosymbiotic eukaryotic algae. Ann N Y Acad Sci 361: 193-208. doi:10.1111/j.1749-6632.1981.tb54365.x. PubMed: 6941719.
3. Archibald JM, (2009) The puzzle of plastid evolution. Curr Biol 19: R81-R88. doi:10.1016/j.cub.2008.11.067. PubMed: 19174147.
4. Green BR, (2011) After the primary endosymbiosis: an update on the chromalveolate hypothesis and the origins of algae with Chl c. Photosynth Res 107: 103-115. doi:10.1007/s11120-010-9584-2. PubMed: 20676772.
5. Bolte K, Bullmann L, Hempel F, Bozarth A, Zauner S, et al. (2009) Protein targeting into secondary plastids. J Eukaryot Microbiol 56: 9-15. doi:10.1111/j.1550-7408.2008.00370.x. PubMed: 19335770.
6. Sheiner L, Striepen B, (2013) Protein sorting in complex plastids. Biochim Biophys Acta 1833: 352-359. doi:10.1016/j.bbamcr.2012.05.030. PubMed: 22683761.
7. Bruce BD, (2000) Chloroplast transit peptides: structure, function and evolution. Trends Cell Biol 10: 440-447. doi:10.1016/S0962-8924(00)01833-X. PubMed: 10998602.
8. Jarvis P, (2008) Targeting of nucleus-encoded proteins to chloroplasts in plants. New Phytol 179: 257-285. doi:10.1111/j.1469-8137.2008.02452.x. PubMed: 19086173.
9. Kilian O, Kroth PG, (2005) Identification and characterization of a new conserved motif within the presequence of proteins targeted into complex diatom plastids. Plant J 41: 175-183. doi:10.1111/j.1365-313X.2004.02294.x. PubMed: 15634195.
10. Gruber A, Vugrinec S, Hempel F, Gould SB, Maier U-G, et al. (2007) Protein targeting into complex diatom plastids: functional characterisation of a specific targeting motif. Plant Mol Biol 64: 519-530. doi:10.1007/s11103-007-9171-x. PubMed: 17484021.
11. Patron NJ, Waller RF, (2007) Transit peptide diversity and divergence: A global analysis of plastid targeting signals. BioEssays 29: 1048-1058. doi:10.1002/bies.20638. PubMed: 17876808.
12. Richter S, Zhong R, Lamppa G, (2005) Function of the stromal processing peptidase in the chloroplast import pathway. Physiol Plant 123: 362-368. doi:10.1111/j.1399-3054.2005.00476.x.
13. Huesgen PF, Overall CM, (2012) N- and C-terminal degradomics: new approaches to reveal biological roles for plant proteases from substrate identification. Physiol Plant 145: 5-17. doi:10.1111/j.1399-3054.2011.01536.x. PubMed: 22023699.
14. Kleifeld O, Doucet A, Auf dem Keller U, Prudova A, Schilling O,et al (2010) Isotopic labeling of terminal amines in complex samples identifies protein N-termini and protease cleavage products. Nat Biotechnol 28: 281-288. doi:10.1038/nbt.1611. PubMed: 20208520.
15. Lange PF, Overall CM, (2013) Protein TAILS: when termini tell tales of proteolysis and function. Curr Opin Chem Biol 17: 73-82. doi:10.1016/j.cbpa.2012.11.025. PubMed: 23298954.
16. Berges JA, Franklin DJ, Harrison PJ, (2001) Evolution of an artificial seawater medium: improvements in enriched seawater, artificial water over the last two decades. J Phycol 37: 1138-1145. doi:10.1046/j.1529-8817.2001.01052.x.
17. Kleifeld O, Doucet A, Prudova A, Keller UAD, Gioia M, et al. (2011) Identifying and quantifying proteolytic events and the natural N terminome by terminal amine isotopic labeling of substrates. Nat Protoc 6: 1578-1611. doi:10.1038/nprot.2011.382. PubMed: 21959240. doi:10.1038/nprot.2011.382.
18. Rappsilber J, Mann M, Ishihama Y, (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc 2: 1896-1906. doi:10.1038/nprot.2007.261. PubMed: 17703201.
19. Craig R, Beavis RC, (2004) TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20: 1466-1467. doi:10.1093/bioinformatics/bth092. PubMed: 14976030.
20. Keller A, Nesvizhskii AI, Kolker E, Aebersold R, (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74: 5383-5392. doi:10.1021/ac025747h. PubMed: 12403597.
21. Deutsch EW, Mendoza L, Shteynberg D, Farrah T, Lam H, et al. (2010) A guided tour of the Trans-Proteomic Pipeline. Proteomics 10: 1150-1159. doi:10.1002/pmic.200900375. PubMed: 20101611.
22. Colaert N, Helsens K, Martens L, Vandekerckhove J, Gevaert K, (2009) Improved visualization of protein consensus sequences by iceLogo. Nat Methods 6: 786-787. doi:10.1038/nmeth1109-786. PubMed: 19876014.
23. Meinnel T, Giglione C, (2008) Tools for analyzing and predicting N-terminal protein modifications. Proteomics 8: 626-649. doi:10.1002/pmic.200700592. PubMed: 18203265.
24. auf dem Keller U, Prudova A, Eckhard U, Fingleton B, Overall CMAuf dem Keller U, e al (2013) Systems-level analysis of proteolytic events in increased vascular permeability and complement activation in skin inflammation. Sci Signal 6rs2-: rs2 doi:10.1126/scisignal.2003512. PubMed: 23322905.
25. Mahrus S, Trinidad JC, Barkan DT, Sali A, Burlingame AL, et al. (2008) Global Sequencing of Proteolytic Cleavage Sites in Apoptosis by Specific Labeling of Protein N Termini. Cell 134: 866-876. doi:10.1016/j.cell.2008.08.012. PubMed: 18722006.
26. Frottin F, Martinez A, Peynot P, Mitra S, Holz RC, et al. (2006) The proteomics of N-terminal methionine cleavage. Mol Cell Proteomics 5: 2336-2349. doi:10.1074/mcp.M600225-MCP200. PubMed: 16963780.
27. Helbig AO, Gauci S, Raijmakers R, van Breukelen B, Slijper M, et al. (2010) Profiling of N-acetylated protein termini provides in-depth Insights into the N-terminal nature of the proteome. Mol Cell Proteomics 9: 928-939. doi:10.1074/mcp.M900463-MCP200. PubMed: 20061308.
28. Van Damme P, Arnesen T, Gevaert K, (2011) Protein alpha-N-acetylation studied by N-terminomics. FEBS J 278: 3822-3834. doi:10.1111/j.1742-4658.2011.08230.x. PubMed: 21736701.
29. Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, et al. (2008) Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLOS ONE 3: e1994. doi:10.1371/journal.pone.0001994. PubMed: 18431481.
30. Terashima M, Specht M, Hippler M, (2011) The chloroplast proteome: a survey from the Chlamydomonas reinhardtii perspective with a focus on distinctive features. Curr Genet 57: 151-168. doi:10.1007/s00294-011-0339-1. PubMed: 21533645.
31. Oudot-Le Secq M-P, Grimwood J, Shapiro H, Armbrust EV, Bowler C, et al. (2007) Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana: comparison with other plastid genomes of the red lineage. Mol Genet Genomics 277: 427-439. doi:10.1007/s00438-006-0199-4. PubMed: 17252281.
32. Lange PF, Overall CM, (2011) TopFIND, a knowledgebase linking protein termini with function. Nat Methods 8: 703-704. doi:10.1038/nmeth.1669. PubMed: 21822272.
33. Bienvenut WV, Espagne C, Martinez A, Majeran W, Valot B, et al. (2011) Dynamics of post-translational modifications and protein stability in the stroma of Chlamydomonas reinhardtii chloroplasts. Proteomics 11: 1734-1750. doi:10.1002/pmic.201000634. PubMed: 21462344.
34. Bienvenut WV, Sumpton D, Martinez A, Lilla S, Espagne C, et al. (2012) Comparative large scale characterization of plant versus mammal proteins reveals similar and idiosyncratic N-alpha-acetylation features. Mol Cell Proteomics 11: M111.015131-M111.015131. doi:10.1074/mcp.M111.015131.
35. Apt KE, Zaslavkaia L, Lippmeier JC, Lang M, Kilian O, et al. (2002) In vivo characterization of diatom multipartite plastid targeting signals. J Cell Sci 115: 4061-4069. doi:10.1242/jcs.00092. PubMed: 12356911.
36. Felsner G, Sommer MS, Maier UG, (2010) The physical and functional borders of transit peptide-like sequences in secondary endosymbionts. BMC Plant Biol 10: 223. doi:10.1186/1471-2229-10-223. PubMed: 20958984.
37. Hempel F, Bullmann L, Lau J, Zauner S, Maier U-G, (2009) ERAD-derived preprotein transport across the second outermost plastid membrane of diatoms. Mol Biol Evol 26: 1781-1790. doi:10.1093/molbev/msp079. PubMed: 19377060.
38. Moog D, Stork S, Zauner S, Maier U-G, (2011) In silico and in vivo investigations of proteins of a minimized eukaryotic cytoplasm. Gen Biol Evol 3: 375-382. doi:10.1093/gbe/evr031.
39. Hirakawa Y, Ishida KI, (2010) Internal plastid-targeting signal found in a RubisCO small subunit protein of a chlorarachniophyte alga. Plant J 64: 402-410. doi:10.1111/j.1365-313X.2010.04334.x. PubMed: 21049565.
40. Vögtle FN, Wortelkamp S, Zahedi RP, Becker D, Leidhold C, et al. (2009) Global Analysis of the Mitochondrial N-Proteome Identifies a Processing Peptidase Critical for Protein Stability. Cell 139: 428-439. doi:10.1016/j.cell.2009.07.045. PubMed: 19837041.
41. Emanuelsson O, Nielsen H, Heijne GV, (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8: 978-984. doi:10.1110/ps.8.5.978. PubMed: 10338008.
42. Apel W, Schulze WX, Bock R, (2010) Identification of protein stability determinants in chloroplasts. Plant J 63: 636-650. doi:10.1111/j.1365-313X.2010.04268.x. PubMed: 20545891.
43. Varshavsky A, (2011) The N-end rule pathway and regulation by proteolysis. Protein Sci 20: 1298-1345. doi:10.1002/pro.666. PubMed: 21633985.
44. Adam Z, Frottin F, Espagne C, Meinnel T, Giglione C, (2011) Interplay between N-terminal methionine excision and FtsH protease is essential for normal chloroplast development and function in Arabidopsis. Plant Cell 23: 3745-3760. doi:10.1105/tpc.111.087239. PubMed: 22010036.
45. Chaal BK, Green BR, (2005) Protein import pathways in "complex"chloroplasts derived from secondary endosymbiosis involving a red algal ancestor. Plant Molecular Biol 57: 333-342. doi:10.1007/s11103-004-7848-y.