Identification of cleavage sites and substrate proteins for two mitochondrial intermediate peptidases in Arabidopsis thaliana

Journal of Experimental Botany

Volumn 66, Issue 9, 2015, Pages 2691-2708

  Carrie, Chris ^a   Venne, A Saskia ^b   Zahedi, René P ^b   Soll, Jürgen ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b LEIBNIZ INSTITUT FÜR ANALYTISCHE WISSENSCHAFTEN ISAS E V   (Germany)

Author keywords

10R motif; ChaFRADIC method; Icp55; mitochondrial processing peptidase (MPP); Oct1

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; EUKARYOTA;

ARABIDOPSIS PROTEIN; PEPTIDE HYDROLASE;

ARABIDOPSIS; BINDING SITE; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENE EXPRESSION REGULATION; METABOLISM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BINDING SITES; GENE EXPRESSION REGULATION, PLANT; PEPTIDE HYDROLASES; SUBSTRATE SPECIFICITY;

EID: 84929359687     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv064     Document Type: Article

References (65)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 215, 403-410.
2. Bachmair A, Finley D, Varshavsky A. 1986. In vivo half-life of a protein is a function of its amino-terminal residue. Science 234, 179-186.
3. Becker T, Bottinger L, Pfanner N. 2012. Mitochondrial protein import: from transport pathways to an integrated network. Trends in Biochemical Sciences 37, 85-91.
4. Berglund AK, Pujol C, Duchene AM, Glaser E. 2009. Defining the determinants for dual targeting of amino acyl-tRNA synthetases to mitochondria and chloroplasts. Journal of Molecular Biology 393, 803-814.
5. Bienvenut WV, Sumpton D, Martinez A, Lilla S, Espagne C, Meinnel T, Giglione C. 2012. Comparative large scale characterization of plant versus mammal proteins reveals similar and idiosyncratic N-alpha-acetylation features. Molecular and Cellular Proteomics 11, M111.015131
6. Braun HP, Binder S, Brennicke A, et al. 2014. The life of plant mitochondrial complex I. Mitochondriondoi doi: 10.1016/j.mito.2014.02.006
7. Braun HP, Emmermann M, Kruft V, Schmitz UK. 1992. The general mitochondrial processing peptidase from potato is an integral part of cytochrome c reductase of the respiratory chain. The EMBO Journal 11, 3219-3227.
8. Burkhart JM, Schumbrutzki C, Wortelkamp S, Sickmann A, Zahedi RP. 2012. Systematic and quantitative comparison of digest efficiency and specificity reveals the impact of trypsin quality on MS-based proteomics. Journal of Proteomics 75, 1454-1462.
9. Carrie C, Giraud E, Duncan O, et al. 2010. Conserved and novel functions for Arabidopsis thaliana MIA40 in assembly of proteins in mitochondria and peroxisomes. The Journal of Biological Chemistry 285, 36138-36148.
10. Carrie C, Small I. 2013. A reevaluation of dual-targeting of proteins to mitochondria and chloroplasts. Biochimica et Biophysica Acta 1833, 253-259.
11. Carrie C, Whelan J. 2013. Widespread dual targeting of proteins in land plants: when, where, how and why. Plant Signaling and Behavior doi: 10.4161/psb.25034
12. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N. 2009. Importing mitochondrial proteins: machineries and mechanisms. Cell 138, 628-644.
13. Chang W, Soll J, Bolter B. 2014. A new member of the psToc159 family contributes to distinct protein targeting pathways in pea chloroplasts. Frontiers in Plant Science 5, 239.
14. Chew O, Whelan J, Millar AH. 2003. Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. The Journal of Biological Chemistry 278, 46869-46877.
15. Colaert N, Helsens K, Martens L, Vandekerckhove J, Gevaert K. 2009. Improved visualization of protein consensus sequences by iceLogo. Nature Methods 6, 786-787.
16. Dessi P, Rudhe C, Glaser E. 2000. Studies on the topology of the protein import channel in relation to the plant mitochondrial processing peptidase integrated into the cytochrome bc1 complex. The Plant Journal 24, 637-644.
17. Duchene AM, Giritch A, Hoffmann B, Cognat V, Lancelin D, Peeters NM, Zaepfel M, Marechal-Drouard L, Small ID. 2005. Dual targeting is the rule for organellar aminoacyl-tRNA synthetases in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 102, 16484-16489.
18. Emanuelsson O, Brunak S, von Heijne G, Nielsen H. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocols 2, 953-971.
19. Gakh O, Cavadini P, Isaya G. 2002. Mitochondrial processing peptidases. Biochimica et Biophysica Acta 1592, 63-77.
20. Gawryluk RM, Chisholm KA, Pinto DM, Gray MW. 2014. Compositional complexity of the mitochondrial proteome of a unicellular eukaryote (Acanthamoeba castellanii, supergroup Amoebozoa) rivals that of animals, fungi, and plants. Journal of Proteomics 109C, 400-416.
21. Ge C, Spanning E, Glaser E, Wieslander A. 2014. Import determinants of organelle-specific and dual targeting peptides of mitochondria and chloroplasts in Arabidopsis thaliana. Molecular Plant 7, 121-136.
22. Glaser E, Dessi P. 1999. Integration of the mitochondrial-processing peptidase into the cytochrome bc1 complex in plants. Journal of Bioenergetics and Biomembranes 31, 259-274.
23. Glaser E, Sjoling S, Tanudji M, Whelan J. 1998. Mitochondrial protein import in plants. Signals, sorting, targeting, processing and regulation. Plant Molecular Biology 38, 311-338.
24. Graciet E, Wellmer F. 2010. The plant N-end rule pathway: structure and functions. Trends in Plant Science 15, 447-453.
25. Hawlitschek G, Schneider H, Schmidt B, Tropschug M, Hartl FU, Neupert W. 1988. Mitochondrial protein import: identification of processing peptidase and of PEP, a processing enhancing protein. Cell 53, 795-806.
26. Hirst J, Carroll J, Fearnley IM, Shannon RJ, Walker JE. 2003. The nuclear encoded subunits of complex I from bovine heart mitochondria. Biochimica et Biophysica Acta 1604, 135-150.
27. Hooper CM, Tanz SK, Castleden IR, Vacher MA, Small ID, Millar AH. 2014. SUBAcon: a consensus algorithm for unifying the subcellular localization data of the Arabidopsis proteome. Bioinformatics 30, 3356-3364.
28. Huang S, Taylor NL, Whelan J, Millar AH. 2009. Refining the definition of plant mitochondrial presequences through analysis of sorting signals, N-terminal modifications, and cleavage motifs. Plant Physiology 150, 1272-1285.
29. Isaya G, Kalousek F, Fenton WA, Rosenberg LE. 1991. Cleavage of precursors by the mitochondrial processing peptidase requires a compatible mature protein or an intermediate octapeptide. The Journal of Cell Biology 113, 65-76.
30. Isaya G, Miklos D, Rollins RA. 1994. MIP1, a new yeast gene homologous to the rat mitochondrial intermediate peptidase gene, is required for oxidative metabolism in Saccharomyces cerevisiae. Molecular Cell Biology 14, 5603-5616.
31. Karimi M, Inze D, Depicker A. 2002. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 7, 193-195.
32. Kleffmann T, Russenberger D, von Zychlinski A, Christopher W, Sjolander K, Gruissem W, Baginsky S. 2004. The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Current Biology 14, 354-362.
33. Koop HU, Steinmuller K, Wagner H, Rossler C, Eibl C, Sacher L. 1996. Integration of foreign sequences into the tobacco plastome via polyethylene glycol-mediated protoplast transformation. Planta 199, 193-201.
34. Kruft V, Eubel H, Jansch L, Werhahn W, Braun HP. 2001. Proteomic approach to identify novel mitochondrial proteins in Arabidopsis. Plant Physiology 127, 1694-1710.
35. Kwasniak M, Pogorzelec L, Migdal I, Smakowska E, Janska H. 2012. Proteolytic system of plant mitochondria. Physiologia Plantarum 145, 187-195.
36. Li B, Takahashi D, Kawamura Y, Uemura M. 2012a. Comparison of plasma membrane proteomic changes of Arabidopsis suspension-cultured cells (T87 Line) after cold and ABA treatment in association with freezing tolerance development. Plant and Cell Physiology 53, 543-554.
37. Li L, Carrie C, Nelson C, Whelan J, Millar AH. 2012b. Accumulation of newly synthesized F1 in vivo in arabidopsis mitochondria provides evidence for modular assembly of the plant F1Fo ATP synthase. The Journal of Biological Chemistry 287, 25749-25757.
38. Li L, Nelson CJ, Carrie C, Gawryluk RM, Solheim C, Gray MW, Whelan J, Millar AH. 2013. Subcomplexes of ancestral respiratory complex I subunits rapidly turn over in vivo as productive assembly intermediates in Arabidopsis. The Journal of Biological Chemistry 288, 5707-5717.
39. Lister R, Carrie C, Duncan O, Ho LH, Howell KA, Murcha MW, Whelan J. 2007. Functional definition of outer membrane proteins involved in preprotein import into mitochondria. The Plant Cell 19, 3739-3759.
40. Millar AH, Heazlewood JL, Kristensen BK, Braun HP, Moller IM. 2005. The plant mitochondrial proteome. Trends in Plant Science 10, 36-43.
41. Mitschke J, Fuss J, Blum T, Hoglund A, Reski R, Kohlbacher O, Rensing SA. 2009. Prediction of dual protein targeting to plant organelles. New Phytologist 183, 224-235.
42. Mossmann D, Meisinger C, Vogtle FN. 2012. Processing of mitochondrial presequences. Biochimica et Biophysica Acta 1819, 1098-1106.
43. Murcha MW, Lister R, Ho AY, Whelan J. 2003. Identification, expression, and import of components 17 and 23 of the inner mitochondrial membrane translocase from Arabidopsis. Plant Physiology 131, 1737-1747.
44. Naamati A, Regev-Rudzki N, Galperin S, Lill R, Pines O. 2009. Dual targeting of Nfs1 and discovery of its novel processing enzyme, Icp55. The Journal of Biological Chemistry 284, 30200-30208.
45. Nett JH, Trumpower BL. 1999. Intermediate length Rieske iron-sulfur protein is present and functionally active in the cytochrome bc1 complex of Saccharomyces cerevisiae. The Journal of Biological Chemistry 274, 9253-9257.
46. Ou WJ, Ito A, Okazaki H, Omura T. 1989. Purification and characterization of a processing protease from rat liver mitochondria. The EMBO Journal 8, 2605-2612.
47. Peltier JB, Ytterberg AJ, Sun Q, van Wijk KJ. 2004. New functions of the thylakoid membrane proteome of Arabidopsis thaliana revealed by a simple, fast, and versatile fractionation strategy. The Journal of Biological Chemistry 279, 49367-49383.
48. Rudhe C, Clifton R, Chew O, Zemam K, Richter S, Lamppa G, Whelan J, Glaser E. 2004. Processing of the dual targeted precursor protein of glutathione reductase in mitochondria and chloroplasts. Journal of Molecular Biology 343, 639-647.
49. Schweiger R, Muller NC, Schmitt MJ, Soll J, Schwenkert S. 2012. AtTPR7 is a chaperone-docking protein of the Sec translocon in Arabidopsis. Journal of Cell Science 125, 5196-5207.
50. Stames EM, O'Toole JF. 2013. Mitochondrial aminopeptidase deletion increases chronological lifespan and oxidative stress resistance while decreasing respiratory metabolism in S. cerevisiae. PLoS ONE 8, e77234.
51. Tanz SK, Castleden I, Hooper CM, Vacher M, Small I, Millar HA. 2013. SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis. Nucleic Acids Research 41, D1185-1191.
52. Teixeira PF, Glaser E. 2013. Processing peptidases in mitochondria and chloroplasts. Biochimica et Biophysica Acta 1833, 360-370.
53. Thingholm TE, Palmisano G, Kjeldsen F, Larsen MR. 2010. Undesirable charge-enhancement of isobaric tagged phosphopeptides leads to reduced identification efficiency. Journal of Proteome Research 9, 4045-4052.
54. Varshavsky A. 2011. The N-end rule pathway and regulation by proteolysis. Protein Science 20, 1298-1345.
55. Venne AS, Vogtle FN, Meisinger C, Sickmann A, Zahedi RP. 2013. Novel highly sensitive, specific, and straightforward strategy for comprehensive N-terminal proteomics reveals unknown substrates of the mitochondrial peptidase Icp55. Journal of Proteome Research 12, 3823-3830.
56. Vogtle FN, Prinz C, Kellermann J, Lottspeich F, Pfanner N, Meisinger C. 2011. Mitochondrial protein turnover: role of the precursor intermediate peptidase Oct1 in protein stabilization. Molecular Biology of the Cell 22, 2135-2143.
57. Vogtle FN, Wortelkamp S, Zahedi RP, et al. 2009. Global analysis of the mitochondrial N-proteome identifies a processing peptidase critical for protein stability. Cell 139, 428-439.
58. von Heijne G. 1986. Mitochondrial targeting sequences may form amphiphilic helices. The EMBO Journal 5, 1335-1342.
59. von Heijne G, Steppuhn J, Herrmann RG. 1989. Domain structure of mitochondrial and chloroplast targeting peptides. European Journal of Biochemistry 180, 535-545.
60. Whelan J, Hugosson M, Glaser E, Day DA. 1995a. Studies on the import and processing of the alternative oxidase precursor by isolated soybean mitochondria. Plant Molecular Biology 27, 769-778.
61. Whelan J, Smith MK, Meijer M, Yu JW, Badger MR, Price GD, Day DA. 1995b. Cloning of an additional cDNA for the alternative oxidase in tobacco. Plant Physiology 107, 1469-1470.
62. Wilce MC, Bond CS, Dixon NE, Freeman HC, Guss JM, Lilley PE, Wilce JA. 1998. Structure and mechanism of a proline-specific aminopeptidase from Escherichia coli. Proceedings of the National Academy of Sciences, USA 95, 3472-3477.
63. Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D. 2004. A molecular timeline for the origin of photosynthetic eukaryotes. Molecular Biology and Evolution 21, 809-818.
64. Zhang XP, Sjoling S, Tanudji M, Somogyi L, Andreu D, Eriksson LE, Graslund A, Whelan J, Glaser E. 2001. Mutagenesis and computer modelling approach to study determinants for recognition of signal peptides by the mitochondrial processing peptidase. The Plant Journal 27, 427-438.
65. Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, Sun Q, van Wijk KJ. 2008. Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS ONE 3, e1994.