The chloroplast ATP-dependent Clp protease in vascular plants - new dimensions and future challenges

Physiologia Plantarum

Volumn 145, Issue 1, 2012, Pages 235-244

  Clarke, Adrian K ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROPLAST PROTEIN; ENDOPEPTIDASE CLP;

ARABIDOPSIS; CELL SURVIVAL; CHLOROPLAST; ENZYME ACTIVATION; ENZYME SPECIFICITY; ENZYMOLOGY; METABOLISM; PLANT CELL; PLANT PHYSIOLOGY; PROTEIN DEGRADATION; REVIEW;

ARABIDOPSIS; CELL SURVIVAL; CHLOROPLAST PROTEINS; CHLOROPLASTS; ENDOPEPTIDASE CLP; ENZYME ACTIVATION; PLANT CELLS; PLANT PHYSIOLOGICAL PHENOMENA; PROTEOLYSIS; SUBSTRATE SPECIFICITY;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); TRACHEOPHYTA;

EID: 84859848962     PISSN: 00319317     EISSN: 13993054     Source Type: Journal    
DOI: 10.1111/j.1399-3054.2011.01541.x     Document Type: Review

References (40)

1. Adam Z, Adamska I, Nakabayashi K, Ostersetzer O, Haussuhl K, Manuell A, Zheng B, Vallon O, Rodermel SR, Shinozaki K, Clarke AK (2001) Chloroplast and mitochondrial proteases in Arabidopsis: a proposed nomenclature. Plant Physiol 125: 1912-1918
2. Akita M, Nielsen E, Keegstra K (1997) Identification of protein transport complexes in the chloroplastic envelope membranes via chemical cross-linking. J Cell Biol 136: 983-994
3. Andersson FI, Tryggvesson A, Sharon M, Diemand AV, Classen M, Best C, Schmidt R, Schelin J, Stanne TM, Bukau B, Robinson CV, Witt S, Mogk A, Clarke AK (2009) Structure and function of a novel type of ATP-dependent Clp protease. J Biol Chem 284: 13519-13532
4. Apel W, Schulze WX, Bock R (2010) Identification of protein stability determinants in chloroplasts. Plant J 63: 636-650
5. Baker TA, Sauer RT (2006) ATP-dependent proteases of bacteria: recognition logic and operating principles. Trends Biochem Sci 31: 647-653
6. Bustos SA, Golden SS (1992) Light-regulated expression of the psbD gene family in Synechococcus sp. PCC 7942: evidence for the role of duplicated psbD genes in cyanobacteria. Mol Gen Genet 232: 221-230
7. Clarke AK (1999) ATP-dependent Clp proteases in photosynthetic organisms: a cut above the rest! Ann Bot 83: 593-599
8. Clarke AK, Eriksson M-J (1996) The cyanobacterium Synechococcus sp. PCC 7942 possesses a close homologue to the chloroplast ClpC protein of higher plants. Plant Mol Biol 31: 721-730
9. Clarke AK, MacDonald TM, Sjögren LLE (2005) The ATP-dependent Clp protease in chloroplasts of higher plants. Physiol Plant 123: 406-412
10. Farrell CM, Grossman AD, Sauer RT (2005) Cytoplasmic degradation of ssrA-tagged proteins. Mol Microbiol 57: 1750-1761
11. Flynn JM, Neher SB, Kim Y-I, Sauer RT, Baker TA (2003) Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol Cell 11: 671-683
12. Kim YI, Levchenko I, Fraczkowska K, Woodruff RV, Sauer RT, Baker TA (2001) Molecular determinants of complex formation between Clp/Hsp100 ATPases and the ClpP peptidase. Nat Struct Biol 8: 230-233
13. Kim J, Rudella A, Ramirez Rodriguez V, Zybailov B, Olinares PDB, van Wijk KJ (2009) Subunits of the plastid ClpPR protease complex have differential contributions to embryogenesis, plastid biogenesis, and plant development in Arabidopsis. Plant Cell 21: 1669-1692
14. Kirstein J, Molière N, Dougan DA, Turgay K (2009) Adapting the machine: adaptor proteins for Hsp100/Clp and AAA+ proteases. Nat Rev Microbiol 7: 589-599
15. Koussevitzky S, Stanne TM, Peto CA, Giap T, Sjögren LLE, Zhao Y, Clarke AK, Chory J (2007) An Arabidopsis thaliana virescent mutant reveals a role for ClpR1 in plastid development. Plant Mol Biol 63: 85-96
16. Majeran W, Friso G, van Wijk KJ, Vallon O (2005) The chloroplast ClpP complex in Chlamydomonas reinhardtii contains an unusual high molecular mass subunit with a large apical domain. FEBS Lett 272: 5558-5571
17. Mogk A, Dougan D, Weibezahn J, Schlieker C, Turgay K, Bukau B (2004) Broad yet high substrate specificity: the challenge of AAA+ proteins. J Struct Biol 146: 90-98
18. Moore SD, Sauer RT (2007) The tmRNA system for translational surveillance and ribosome rescue. Ann Rev Biochem 76: 101-124
19. Nakagawara E, Sakuraba Y, Yamasato A, Tanaka R, Tanaka A (2007) Clp protease controls chlorophyll b synthesis by regulating the level of chlorophyllide a oxygenase. Plant J 49: 800-809
20. Neher SB, Villen J, Oakes EC, Bakalarski CE, Sauer RT, Gygi SP, Baker TA (2006) Proteomic profiling of ClpXP substrates after DNA damage reveals extensive instability within SOS regulon. Mol Cell 22: 193-204
21. Nishimura K, Ashida H, Ogawa T, Yokota A (2010) A DEAD box protein is required for formation of a hidden break in Arabidopsis chloroplast 23S rRNA. Plant J 63: 766-777
22. Ogle JM, Ramakrishnan V (2005) Structural insights into translational fidelity. Annu Rev Biochem 74: 129-177
23. Olinares PDB, Kim J, van Wijk KJ (2011a) The Clp protease system: a central component of the chloroplast protease network. Biochim Biophys Acta 1807: 999-1011
24. Olinares PDB, Kim J, Davis JI, van Wijk KJ (2011b) Subunit stoichiometry, evolution, and functional implications of an asymmetric plant plastid ClpP/R protease complex in Arabidopsis. Plant Cell 23: 2348-2361
25. Peltier J, Ytterberg J, Liberles DA, Roepstorff P, van Wijk KJ (2001) Identification of a 350-kDa ClpP protease complex with 10 different Clp isoforms in chloroplast of Arabidopsis thaliana. J Biol Chem 276: 16318-16327
26. Peltier J, Ripoll DR, Friso G, Rudella A, Cai Y, Ytterberg J, Giacomelli L, Pillardy P, van Wijk KJ (2004) 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: 4768-4781
27. Porankiewicz J, Wang J, Clarke AK (1999) New insights into the ATP-dependent Clp protease: Escherichia coli and beyond. Mol Microbiol 32: 449-458
28. Ravid T, Hochstrasser M (2008) Diversity of degradation signals in the ubiquitin-proteasome system. Nat Rev Mol Cell Biol 9: 679-690
29. Sakamoto W (2006) Protein degradation machineries in plastids. Ann Rev Plant Biol 57: 599-621
30. Sakuraba Y, Tanaka R, Yamasato A, Tanaka A (2009) Determination of a chloroplast degron in the regulatory domain of chlorophyllide a oxygenase. J Biol Chem 284: 36689-36699
31. Schelin J, Lindmark F, Clarke AK (2002) The clpP multigene family for the ATP-dependent Clp protease in the cyanobacterium Synechococcus. Microbiol 148: 2255-2265
32. Sjögren LLE, Stanne TM, Zheng B, Sutinen S, Clarke AK (2006) Structural and functional insights into the chloroplast ATP-dependent Clp protease in Arabidopsis. Plant Cell 18: 2635-2649
33. Sjögren LLE, Clarke AK (2011a) Assembly of the chloroplast ATP-dependent Clp protease in Arabidopsis is regulated by the ClpT accessory proteins. Plant Cell 23: 322-332
34. Sjögren LLE, Clarke AK (2011b) Studying proteases and protein turnover in Arabidopsis chloroplasts. In: Jarvis RP (ed) Chloroplast Research in Arabidopsis. Methods in Molecular Biology, Vol. 774. Springer, Dordrecht, pp. 225-240
35. Sokolenko A, Pojidaeva E, Zinchenko V, Panichkin V, Glaser VM, Herrmann HG, Shestakov SV (2002) The gene complement for proteolysis in the cyanobacterium Synechocystis sp. PCC 6803 and Arabidopsis thaliana chloroplasts. Curr Genet 41: 291-310
36. Stanne TM, Pojidaeva E, Andersson FI, Clarke AK (2007) Distinctive types of ATP-dependent Clp proteases in cyanobacteria. J Biol Chem 282: 14394-14402
37. Stanne TM, Sjögren LLE, Koussevitzky S, Clarke AK (2009) Identification of new protein substrates for the chloroplast ATP-dependent Clp protease supports its constitutive role in Arabidopsis. Biochem J 417: 257-268
38. + ATPases in protein degradation from bacteria to eukaryotes. Curr Opin Struct Biol 19: 209-217
39. Wang J, Hartling JA, Flanagan JM (1997) The structure of ClpP at 2.3 Å resolution suggests a model for ATP-dependent proteolysis. Cell 91: 447-456
40. Zheng B, Halperin T, Hruskova-Heidingsfeldova O, Adam Z, Clarke AK (2002) Characterization of chloroplast Clp proteins in Arabidopsis: localization, tissue specificity and stress responses. Physiol Plant 114: 92-101