Two novel targeting peptide degrading proteases, PrePs, in mitochondria and chloroplasts, so similar and still different

Journal of Molecular Biology

Volumn 349, Issue 4, 2005, Pages 847-860

  Ståhl, Annelie ^a   Nilsson, Stefan ^a   Lundberg, Pontus ^a   Bhushan, Shashi ^a   Biverståhl, Henrik ^a   Moberg, Per ^a   Morisset, Magali ^a   Vener, Alexander ^b   Mäler, Lena ^a   Langel, Ulo ^a   Glaser, Elzbieta ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b LINKÖPING UNIVERSITY   (Sweden)

Author keywords

Chloroplast; Degradation; Mitochondria; Protease; Targeting

Indexed keywords

METALLOPROTEINASE; PEPTIDE; PITRILYSIN; PROTEIN PREPI; PROTEIN PREPII; SERINE; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARABIDOPSIS; ARTICLE; CHLOROPLAST; ENZYME ACTIVITY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN STRUCTURE; STRUCTURAL HOMOLOGY; STRUCTURAL PROTEOMICS;

ARABIDOPSIS THALIANA;

EID: 21144447897     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.04.023     Document Type: Article

References (63)

1. K. Esser, B. Tursun, M. Ingenhoven, G. Michaelis, and E. Pratje A novel two-step mechanism for removal of a mitochondrial signal sequence involves the mAAA complex and the putative rhomboid protease Pcp1 J. Mol. Biol. 323 2002 835 843
2. A. Sokolenko, E. Pojidaeva, V. Zinchenko, V. Panichkin, V.M. Glaser, R.G. Herrmann, and S.V. Shestakov The gene complement for proteolysis in the cyanobacterium Synechocystis sp. PCC 6803 and Arabidopsis thaliana chloroplasts Curr. Genet. 41 2002 291 310
3. I. Arnold, and T. Langer Membrane protein degradation by AAA proteases in mitochondria Biochim. Biophys. Acta 1592 2002 89 96
4. M. Kaser, and T. Langer Protein degradation in mitochondria Semin. Cell Dev. Biol. 11 2000 181 190
5. M. Rep, and L.A. Grivell The role of protein degradation in mitochondrial function and biogenesis Curr. Genet. 30 1996 367 380
6. S. Gottesman, and M.R. Maurizi Regulation by proteolysis: energy-dependent proteases and their targets Microbiol. Rev. 56 1992 592 621
7. Z. Adam, and A.K. Clarke Cutting edge of chloroplast proteolysis Trends Plant Sci. 7 2002 451 456
8. M. Lindahl, S. Tabak, L. Cseke, E. Pichersky, B. Andersson, and Z. Adam Identification, characterization, and molecular cloning of a homologue of the bacterial FtsH protease in chloroplasts of higher plants J. Biol. Chem. 271 1996 29329 29334
9. M. Chen, Y. Choi, D.F. Voytas, and S. Rodermel Mutations in the Arabidopsis VAR2 locus cause leaf variegation due to the loss of a chloroplast FtsH protease Plant J. 22 2000 303 313
10. H. Stahlberg, E. Kutejova, K. Suda, B. Wolpensinger, A. Lustig, and G. Schatz Mitochondrial Lon of Saccharomyces cerevisiae is a ring-shaped protease with seven flexible subunits Proc. Natl Acad. Sci. USA 96 1999 6787 6790
11. R. Sarria, A. Lyznik, C.E. Vallejos, and S.A. Mackenzie A cytoplasmic male sterility-associated mitochondrial peptide in common bean is post-translationally regulated Plant Cell. 10 1998 1217 1228
12. Z. Adam, I. Adamska, K. Nakabayashi, O. Ostersetzer, K. Haussuhl, and A. Manuell Chloroplast and mitochondrial proteases in Arabidopsis. A proposed nomenclature Plant Physiol. 125 2001 1912 1918
13. J.B. Peltier, D.R. Ripoll, G. Friso, A. Rudella, Y. Cai, and J. Ytterberg Clp protease complexes from photosynthetic and non-photosynthetic plastids and mitochondria of plants, their predicted three-dimensional structures, and functional implications J. Biol. Chem. 279 2004 4768 4781
14. K. Haussuhl, B. Andersson, and I. Adamska A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II EMBO J. 20 2001 713 722
15. M. Lensch, R.G. Herrmann, and A. Sokolenko Identification and characterization of SppA, a novel light-inducible chloroplast protease complex associated with thylakoid membranes J. Biol. Chem. 276 2001 33645 33651
16. M. Buchler, U. Tisljar, and D.H. Wolf Proteinase yscD (oligopeptidase yscD) Structure, function and relationship of the yeast enzyme with mammalian thimet oilgopeptidase (metalloendopeptidase, EP 24.15) Eur. J. Biochem. 219 1994 627 639
17. M. Kaser, M. Kambacheld, B. Kisters-Woike, and T. Langer Oma1, a novel membrane-bound metallopeptidase in mitochondria with activities overlapping with the m-AAA protease J. Biol. Chem. 278 2003 46414 46423
18. A.M. van der Bliek, and C.M. Koehler A mitochondrial rhomboid protease Dev. Cell 4 2003 769 770
19. A. Stahl, P. Moberg, J. Ytterberg, O. Panfilov, and H. Brockenhuus Von Lowenhielm Isolation and identification of a novel mitochondrial metalloprotease (PreP) that degrades targeting pre-sequences in plants J. Biol. Chem. 277 2002 41931 41939
20. P. Moberg, A. Stahl, S. Bhushan, S.J. Wright, A. Eriksson, B.D. Bruce, and E. Glaser Characterization of a novel zinc metalloprotease involved in degrading targeting peptides in mitochondria and chloroplasts Plant J. 36 2003 616 628
21. N.D. Rawlings, and A.J. Barrett Homologues of insulinase, a new superfamily of metalloendopeptidases Biochem. J. 275 1991 389 391
22. S. Bhushan, B. Lefebvre, A. Stahl, S.J. Wright, B.D. Bruce, M. Boutry, and E. Glaser Dual targeting and function of a protease in mitochondria and chloroplasts EMBO Rep. 4 2003 1073 1078
23. S. Bhushan, A. Stahl, S. Nilsson, B. Lefebvre, M. Seki, and C. Roth Subcellular localization, expression and evolution of the targeting peptides degrading protease AtPreP2 Plant Cell Physiol. 2005 [epub ahead of print]
24. E. Glaser, and P. Dessi Integration of the mitochondrial-processing peptidase into the cytochrome bc1 complex in plants J. Bioenerg. Biomembr. 31 1999 259 274
25. S. Richter, and G.K. Lamppa Structural properties of the chloroplast stromal processing peptidase required for its function in transit peptide removal J. Biol. Chem. 278 2003 39497 39502
26. G. von Heijne Mitochondrial targeting sequences may form amphiphilic helices EMBO J. 5 1986 1335 1342
27. Y. Abe, T. Shodai, T. Muto, K. Mihara, H. Torii, and S. Nishikawa Structural basis of pre-sequence recognition by the mitochondrial protein import receptor Tom20 Cell 100 2000 551 560
28. I. Krimm, P. Gans, J.F. Hernandez, G.J. Arlaud, and J.M. Lancelin A coil-helix instead of a helix-coil motif can be induced in a chloroplast transit peptide from Chlamydomonas reinhardtii Eur. J. Biochem. 265 1999 171 180
29. H.L. Wienk, R.W. Wechselberger, M. Czisch, and B. de Kruijff Structure, dynamics, and insertion of a chloroplast targeting peptide in mixed micelles Biochemistry 39 2000 8219 8227
30. S.M. Glaser, and M.G. Cumsky Localization of a synthetic pre-sequence that blocks protein import into mitochondria J. Biol. Chem. 265 1990 8817 8822
31. K. Nicolay, F.D. Laterveer, and W.L. van Heerde Effects of amphipathic peptides, including pre-sequences, on the functional integrity of rat liver mitochondrial membranes J. Bioenerg. Biomembr. 26 1994 327 334
32. D. Roise, S.J. Horvath, J.M. Tomich, J.H. Richards, and G. Schatz 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 1986 1327 1334
33. P. Pinnaduwage, and B.D. Bruce In vitro interaction between a chloroplast transit peptide and chloroplast outer envelope lipids is sequence-specific and lipid class-dependent J. Biol. Chem. 271 1996 32907 32915
34. R. van't Hof, and B. de Kruijff Transit sequence-dependent binding of the chloroplast precursor protein ferredoxin to lipid vesicles and its implications for membrane stability FEBS Letters 361 1995 35 40
35. P. Moberg, S. Nilsson, A. Stahl, A.C. Eriksson, E. Glaser, and L. Maler NMR solution structure of the mitochondrial F1beta pre-sequence from Nicotiana plumbaginifolia J. Mol. Biol. 336 2004 1129 1140
36. Q.H. Dai, C. Tommos, E.J. Fuentes, M.R. Blomberg, P.L. Dutton, and A.J. Wand Structure of a de novo designed protein model of radical enzymes J. Am. Chem. Soc. 124 2002 10952 10953
37. F.F. Vajdos, M. Ultsch, M.L. Schaffer, K.D. Deshayes, J. Liu, N.J. Skelton, and A.M. de Vos Crystal structure of human insulin-like growth factor-1: detergent binding inhibits binding protein interactions Biochemistry 40 2001 11022 11029
38. N.J. Skelton, J. Kordel, and W.J. Chazin Determination of the solution structure of Apo calbindin D9k by NMR spectroscopy J. Mol. Biol. 249 1995 441 462
39. M. Arretz, H. Schneider, B. Guiard, M. Brunner, and W. Neupert Characterization of the mitochondrial processing peptidase of Neurospora crassa J. Biol. Chem. 269 1994 4959 4967
40. S. Sjoling, A.C. Eriksson, and E. Glaser A helical element in the C-terminal domain of the N. plumbaginifolia F1 beta pre-sequence is important for recognition by the mitochondrial processing peptidase J. Biol. Chem. 269 1994 32059 32062
41. S. Kuzela, and A.L. Goldberg Mitochondrial ATP-dependent protease from rat liver and yeast Methods Enzymol. 244 1994 376 383
42. L. Young, K. Leonhard, T. Tatsuta, J. Trowsdale, and T. Langer Role of the ABC transporter Mdl1 in peptide export from mitochondria Science 291 2001 2135 2138
43. M.W. Thompson, S.K. Singh, and M.R. Maurizi Processive degradation of proteins by the ATP-dependent Clp protease from Escherichia coli. Requirement for the multiple array of active sites in ClpP but not ATP hydrolysis J. Biol. Chem. 269 1994 18209 18215
44. A. Serizawa, P.M. Dando, and A.J. Barrett Characterization of a mitochondrial metallopeptidase reveals neurolysin as a homologue of thimet oligopeptidase J. Biol. Chem. 270 1995 2092 2098
45. M. Desautels, and A.L. Goldberg Liver mitochondria contain an ATP-dependent, vanadate-sensitive pathway for the degradation of proteins Proc. Natl Acad. Sci. USA 79 1982 1869 1873
46. X.P. Zhang, and E. Glaser Interaction of plant mitochondrial and chloroplast signal peptides with the Hsp70 molecular chaperone Trends Plant Sci. 7 2002 14 21
47. D.O. Daley, K.L. Adams, R. Clifton, S. Qualmann, A.H. Millar, and J.D. Palmer Gene transfer from mitochondrion to nucleus: novel mechanisms for gene activation from Cox2 Plant J. 30 2002 11 21
48. M.W. Murcha, D. Elhafez, H. Millar, and J. Whelan The N-terminal extension of plant mitochondrial carrier proteins is removed by two-step processing: the first cleavage is by the mitochondrial processing peptidase J. Mol. Biol. 344 2004 443 454
49. A. Mukhopadhyay, P. Hammen, M. Waltner-Law, and H. Weiner Timing and structural consideration for the processing of mitochondrial matrix space proteins by the mitochondrial processing peptidase (MPP) Protein Sci. 11 2002 1026 1035
50. E.S. Song, A. Mukherjee, M.A. Juliano, J.S. Pyrek, J.P. Goodman Jr, L. Juliano, and L.B. Hersh Analysis of the subsite specificity of rat insulysin using fluorogenic peptide substrates J. Biol. Chem. 276 2001 1152 1155
51. F. Authier, B.I. Posner, and J.J. Bergeron Insulin-degrading enzyme Clin. Invest. Med. 19 1996 149 160
52. F.G. Hamel, B.D. Gehm, M.R. Rosner, and W.C. Duckworth Identification of the cleavage sites of transforming growth factor alpha by insulin-degrading enzymes Biochim. Biophys. Acta 1338 1997 207 214
53. W.C. Duckworth, R.G. Bennett, and F.G. Hamel Insulin degradation: progress and potential Endocr. Rev. 19 1998 608 624
54. G.S. Yi, B.S. Choi, and H. Kim Structures of wild-type and mutant signal sequences of Escherichia coli ribose binding protein Biophys. J. 66 1994 1604 1611
55. J. Rizo, F.J. Blanco, B. Kobe, M.D. Bruch, and L.M. Gierasch Conformational behavior of Escherichia coli OmpA signal peptides in membrane mimetic environments Biochemistry 32 1993 4881 4894
56. J.D. Jones, C.J. McKnight, and L.M. Gierasch Biophysical studies of signal peptides: implications for signal sequence functions and the involvement of lipid in protein export J. Bioenerg. Biomembr. 22 1990 213 232
57. C. Karslake, M.E. Piotto, Y.K. Pak, H. Weiner, and D.G. Gorenstein 2D NMR and structural model for a mitochondrial signal peptide bound to a micelle Biochemistry 29 1990 9872 9878
58. D. Roise, F. Theiler, S.J. Horvath, J.M. Tomich, J.H. Richards, D.S. Allison, and G. Schatz Amphiphilicity is essential for mitochondrial pre-sequence function EMBO J. 7 1988 649 653
59. A.B. Taylor, B.S. Smith, S. Kitada, K. Kojima, H. Miyaura, and Z. Otwinowski Crystal structures of mitochondrial processing peptidase reveal the mode for specific cleavage of import signal sequences Structure (Camb) 3 2001 615 625
60. N. Pfanner, and N. Wiedemann Mitochondrial protein import: two membranes, three translocases Curr. Opin. Cell Biol. 14 2002 400 411
61. K.N. Truscott, K. Brandner, and N. Pfanner Mechanisms of protein import into mitochondria Curr. Biol. 13 2003 R326 R337
62. P. Lundberg, M. Magzoub, M. Lindberg, M. Hallbrink, J. Jarvet, and L.E. Eriksson Cell membrane translocation of the N-terminal (1-28) part of the prion protein Biochem. Biophys. Res. Commun. 299 2002 85 90
63. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685