Catalysis, subcellular localization, expression and evolution of the targeting peptides degrading protease, AtPreP2

Plant and Cell Physiology

Volumn 46, Issue 6, 2005, Pages 985-996

  Bhushan, Shashi ^a   Ståhl, Annelie ^a   Nilsson, Stefan ^a   Lefebvre, Benoit ^b   Seki, Motoaki ^c   Roth, Christian ^d   McWilliam, David ^e   Wright, Sarah J ^e   Liberles, David A ^d   Shinozaki, Kazuo ^c   Bruce, Barry D ^e   Boutry, Marc ^b   Glaser, Elzbieta ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^c RIKEN   (Japan)

^d UNIVERSITY OF BERGEN   (Norway)

^e UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Chloroplasts; Dual targeting; Mitochondria; Presequence protease; Protein import; Zinc metalloprotease

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; NICOTIANA TABACUM;

COMPLEMENTARY DNA; METALLOPROTEINASE; PEPTIDE; PLANT DNA;

ACTIVE TRANSPORT; AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CATALYSIS; CELL FRACTIONATION; CHEMISTRY; CHLOROPLAST; ENZYME SPECIFICITY; ENZYMOLOGY; GENE; GENE EXPRESSION; GENETICS; MASS SPECTROMETRY; METABOLISM; MITOCHONDRION; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; TOBACCO; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; ARABIDOPSIS; BASE SEQUENCE; BIOLOGICAL TRANSPORT, ACTIVE; CATALYSIS; CHLOROPLASTS; DNA, COMPLEMENTARY; DNA, PLANT; EVOLUTION, MOLECULAR; GENE EXPRESSION; GENES, PLANT; MASS SPECTROMETRY; METALLOPROTEASES; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PEPTIDES; PLANTS, GENETICALLY MODIFIED; SUBCELLULAR FRACTIONS; SUBSTRATE SPECIFICITY; TOBACCO;

EID: 19444368052     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pci107     Document Type: Article

References (56)

1. Abe, Y., Shodai, T., Muto, T., Mihara, K., Torii, H., Nishikawa, S., Endo, T. and Kohda, D. (2000) Structural basis of presequence recognition by the mitochondrial protein import receptor Tom20. Cell. 3:551-560.
2. Adam, Z., Adamska, I., Nakabayashi, K., Ostersetzer, O., Haussuhl, K., Manuell, A., Zheng, B., Vallon, O., Rodermel, S., Shinozaki, K. and Clarke, A. (2001) Chloroplast and mitochondrial proteases in Arabidopsis. A proposed nomenclature. Plant Physiol. 125: 1912-1918.
3. Arnold, I. and Langer, T. (2002) Membrane protein degradation by AAA proteases in mitochondria. Biochim. Biophys. Acta. 1592: 89-96.
4. Aronsson, H. and Jarvis, P. (2002) A simple method for isolating import-competent Arabidopsis chloroplasts. FEBS Lett. 529: 215-220.
5. Bhushan, S., Lefebvre, B., Ståhl, A., Wright, S.J., Bruce, B.D., Boutry, M. and Glaser, E. (2003) Dual targeting and function of a protease in mitochondria and chloroplasts. EMBO Rep. 4: 1073-1078.
6. Bruce, B.D. (2000) Chloroplastic transit peptides: structure, function and evolution. Trends Cell Biol. 10: 440-447.
7. Bruce, B.D., Perry, S., Froelich, J. and Keegstra, K. (1994) In vitro import of proteins into chloroplasts. In Plant Molecular Biology Manual, 2nd edn. Edited by Gelvin, S.B. and Schilferoot, R.A. Kluwer Academic Publishers, Dordrect, The Netherlands. pp. J1-J15.
8. Chew, O., Whelan, J. and Millar, A.H. (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J. Biol. Chem. 278: 46869-46877.
9. Cleary, S.P., Tan, F.C., Nakrieko, K.A., Thompson, S.J., Mullineaux, P.M., Creissen, G.P., von Stedingk, E., Glaser, E., Smith, A.C. and Robinson, C. (2002) Isolated plant mitochondria import chloroplast precursor proteins in vitro with the same efficiency as chloroplasts. J. Biol. Chem. 277: 5562-5569.
10. Duby, G., Oufattole, M. and Boutry, M. (2001) Hydrophobic residues within the predicted N-terminal amphiphilic alpha-helix of a plant mitochondrial targeting presequence play a major role in in vivo import. Plant J. 27: 539-549.
11. Duckworth, W.C., Bennett, R.G. and Hamel, F.G. (1998) Insulin degradation: progress and potential. Endocr. Rev. 19: 608-624.
12. Dyck, L.V., Pearce, D. and Sherman, F. (1994) PIM1 encodes a mitochondrial ATP-dependent protease that is required for mitochondrial function in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 7: 238-242.
13. Force, A., Lynch, M., Pickett, F.B., Amores, A. Yan, Y.L. and Postlethwait, J. (1999) Preservation of duplicate genes by complementary degenerative mutations. Genetics 151: 1531-1545.
14. Ginsberg, M.D., Feliciello, A., Jones, J.K., Avvedimento, E.V. and Gottesman, M.E. (2003) PKA-dependent binding of mRNA to the mitochondrial AKAP121 protein. J. Mol. Biol. 327: 885-897.
15. Glaser, S. and Cumsky, M. (1990a) Localization of a synthetic presequence that blocks protein import into mitochondria. J. Biol. Chem. 25: 8817-8822.
16. Glaser, S. and Cumsky, M. (1990b) A synthetic presequence reversibly inhibits protein import into yeast mitochondria. J. Biol. Chem. 25: 8808-8816.
17. Glaser, E., Sjöling, S., Tanudji, M. and Whelan, J. (1998) Mitochondrial protein import in plants. Signals, sorting, targeting and regulation. Plant Mol. Biol. 38:311-338.
18. Halperin, T., Zheng, B., Itzhaki, H., Clarke, A. and Adam, Z. (2001) Plant mitochondria contain proteolytic and regulatory subunits of the ATP-dependent Clp protease. Plant Mol. Biol. 45: 461-468.
19. Huelsenbeck, J.P. and Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
20. Hugosson, M. andreu, D., Boman, H. and Glaser, E. (1994) Antibacterial peptides and mitochondrial presequences affect mitochondrial coupling, respiration and protein import. Eur. J. Biochem. 223: 1027-1033.
21. Katju, V. and Lynch, M. (2003) The structure and early evolution of recently arisen gene duplicates in the Caenorhabditis elegans genome. Genetics 165: 1793-1803.
22. Laemmli, U. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 15: 680-685.
23. Lee, C., Grasso, C. and Sharlow, M.F. (2002) Multiple sequence alignment using partial order graphs. Bioinformatics 18: 452-464.
24. Liberles, D.A., Schreiber, D.R., Govindarajan, S., Chamberlin, S.G. and Benner, S.A. (2001) The Adaptive Evolution Database (TAED). Genome Biol. 2: 0028.1-0028.6.
25. Lister, R., Chew, O., Lee, M.N., Heazlewood, J.L., Clifton, R., Parker, K.L., Millar, A.H. and Whelan, J. (2004) A transcriptomic and proteomic characterization of the Arabidopsis mitochondrial protein import apparatus and its response to mitochondrial dysfunction. Plant Physiol. 134: 777-789.
26. Lu, Y. and Beavis, A.D. (1997) Effect of leader peptides on the permeability of mitochondria. J. Biol. Chem. 23: 13555-13561.
27. +-ATPase gene. Plant J. 14: 413-423.
28. Maliga, P., Sz-Breznovits, A. and Marton, L. (1973) Streptomycin- resistant plants from callus culture of haploid tobacco. Nat New Biol. 244: 29-30.
29. Matsuzaki, K., Murase, O., Fujii, N. and Miyajima, K. (1996) An antimicrobial peptide, magainin 2, induced rapid flip-flop of phospholipids coupled with pore formation and peptide translocation. Biochemistry. 35: 11361-11368.
30. Moberg, P., Ståhl, A., Bhushan, S., Wright, S.J., Eriksson, A., Bruce, B.D. and Glaser, E. (2003) Characterization of a novel zinc metalloprotease involved in degrading targeting peptides in mitochondria and chloroplasts. Plant J. 36: 616-628.
31. 1beta presequence from Nicotiana plumbaginifolia. J. Mol. Biol. 336: 1129-1140.
32. Moore, R.C. and Purugganan, M.D. (2003) The early stages of duplicate gene evolution. Proc. Natl Acad. Sci. USA 100: 15682-15687.
33. Nicolay, K., Laterveer, F. and Heerde, W. (1994) Effects of amphipathic peptides, including presequences, on the functional integrity of rat liver mitochondrial membranes. J. Bioenerg. Biomembr. 26: 327-334.
34. Peeters, N. and Small, I. (2001) Dual targeting to mitochondria and chloroplasts. Biochim. Biophys. Acta 12: 54-63.
35. Perkins, D.N., Pappin, D.J., Creasy, D.M. and Cottrell, J.S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20: 3551-3567.
36. Pfanner, N. and Geissler, A. (2001) Versatility of the mitochondrial protein import machinery. Nat. Rev. Mol. Cell. Biol. 2: 339-349.
37. Rawling, N.D. and Barrett, A.J. (1991) Homologues of insulinase, a new super-family of metalloendopeptidases. Biochem. J. 275: 389-391.
38. Rehling, P., Wiedemann, N., Pfanner, N. and Truscott, K. (2001) The mitochondrial import machinery for preproteins. Crit. Rev. Biochem. Mol. Biol. 36: 291-336.
39. Richter, S. and Lamppa, G.K. (1998) A chloroplast processing enzyme functions as the general stromal processing peptidase. Proc. Natl Acad. Sci. USA 95: 7463-7468.
40. Richter, S. and Lamppa, G.K. (2002) Determinants for removal and degradation of transit peptides of chloroplast precursor proteins. J. Biol. Chem. 277: 43888-43894.
41. Roise, D., Horvath, S., Tomich, J., Richards, J. and Schatz, G. (1986) A chemically synthesized pre-sequence of an imported mitochondrial protein can form an amphiphilic helix and perturb natural and artificial phospholipid bilayers. EMBO J. 5: 1327-1334.
42. Roth, R.A. (1998) Introduction: clan ME containing pitrilysin and its relatives. In Handbook of Proteolytic Enzymes. Edited by Barrett, A.J., Rawlings, N.D. and Woessner, J.F. pp. 1360-1362. Academic Press, San Diego.
43. Roth, C., Betts, M.J., Steffansson, P., Saelensminde, G. and Liberles, D.A. (2005) The Adaptive Evolution Database (TAED): a phylogeny based tool for comparative genomics. Nucleic Acids Res. 33 (Database issue): D495-497.
44. Rudhe, C., Chew, O., Whelan, J. and Glaser, E. (2002) A novel in vitro import system for simultaneous import of precursor proteins into mitochondria and chloroplasts. Plant J. 30: 213-220.
45. Sagarra, M.D., Mayo, I., Marco, S., Rodriguez-Vilarino, S., Oliva, J., Carrascosa, J. and Castan, J. (1999) Mitochondrial localization and oligomeric structure of HClpP, the human homologue of E. coli ClpP. J. Mol. Biol. 1: 819-825.
46. 2-terminal amino acid sequences of precursor and mature forms of the ribulose-1, 5-bisphosphate carboxylase small subunit from Chlamydomonas reinhardtii. J. Cell Biol. 83: 615-622.
47. Seki, M., Narusaka, M., Kamiya, A., Ishida, J., Satou, M., Sakurai, T., Nakajima, M., Enju, A., Akiyama, K., Oono, Y., Muramatsu, M., Hayashizaki, Y., Kawai, J., Carninci, P., Itoh, M., Ishii, Y., Arakawa, T., Shibata, K., Shinagawa, A. and Shinozaki, K. (2002) Functional annotation of a full-length Arabidopsis cDNA collection. Science 296: 141-145.
48. Silva-Filho, M.C. (2003) One ticket for multiple destination: dual targeting of proteins to distinct subcellular location. Curr. Opin. Plant Biol. 6: 589-595.
49. Ståhl, A., Moberg, P., Ytterberg, J., Panfilov, O., Brockenhuus Von Lowenhielm, H., Nilsson, F. and Glaser, E. (2002) Isolation and identification of a novel mitochondrial metalloprotease (PreP) that degrades targeting presequences in plants. J. Biol. Chem. 277: 41931-41939.
50. Ståhl, A., Pavlov, P., Szigyarto, C. and Glaser, E. (2000) Rapid degradation of the presequence of the F1beta precursor of the ATP synthase inside mitochondria. Biochem. J. 349: 703-707.
51. Ståhl, A., Nilsson, S., Lundberg, P., Bhushan, S., Biverstahl, H., et al. (2005) Two Novel Targeting Peptide Degrading Proteases, PrePs, in Mitochondria and Chloroplasts, so Similar and Still Different. J. Mol. Biol. 349: 847-860.
52. Tabb, D.L., McDonald, W.H. and Yates, J.R. 3rd (2002) DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomic. Proteome Res. 1: 21-26.
53. von Heijne, G. (1986) Mitochondrial targeting sequences may form amphiphilic helices. EMBO J. 5: 1335-1342.
54. Von Stedingk, E.M., Pavlov, P.P., Grinkevich, V.A. and Glaser, E. (1997) Mitochondrial protein import: modification of sulfhydryl groups of the inner mitochondrial membrane import machinery in Solanum tuberosum inhibits protein import. Plant Mol. Biol. 35: 809-820.
55. Whelan, J., Knorpp, C. and Glaser, E. (1990) Sorting of precursor proteins between isolated spinach leaf mitochondria and chloroplasts. Plant Mol. Biol. 14: 977-982.
56. +-ATPase pma4 transcription promoter from Nicotiana plumbaginifolia activated by the CaMV 35S promoter enhancer. Plant Sci. 149: 157-165.