The hetero-hexameric nature of a chloroplast AAA+ FtsH protease contributes to its thermodynamic stability

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Moldavski, Ofer ^a   Levin Kravets, Olga ^b   Ziv, Tamar ^c   Adam, Zach ^a   Prag, Gali ^b  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

^c TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PEPTIDES AND PROTEINS; PROTEIN FTSH; PROTEIN FTSH1; PROTEIN FTSH2; PROTEIN FTSH5; PROTEIN FTSH8; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; ADENOSINE TRIPHOSPHATE DEPENDENT PROTEINASE; ARABIDOPSIS PROTEIN; EPITOPE; FTSH5 PROTEIN, ARABIDOPSIS; HYBRID PROTEIN; M AAA PROTEASES; M-AAA PROTEASES; MEMBRANE PROTEIN; METALLOPROTEINASE; MULTIENZYME COMPLEX; VAR2 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; CHLOROTYPE; COMPLEX FORMATION; CONTROLLED STUDY; HYDROGEN BOND; HYDROPHILICITY; HYDROPHOBICITY; ION TRAP MASS SPECTROMETRY; MOLECULAR INTERACTION; NONHUMAN; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STABILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; THERMOSTABILITY; THERMUS THERMOPHILUS; TRANSCRIPTION REGULATION; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; CHLOROPLAST; ENZYME STABILITY; ENZYMOLOGY; GENETICS; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; PROTEIN MULTIMERIZATION; PROTEIN SUBUNIT; PROTEIN TRANSPORT; THERMODYNAMICS; THYLAKOID; TRANSGENIC PLANT;

ARABIDOPSIS; EUKARYOTA; PROKARYOTA;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ATP-DEPENDENT PROTEASES; CHLOROPLASTS; ENZYME STABILITY; EPITOPES; MASS SPECTROMETRY; MEMBRANE PROTEINS; METALLOENDOPEPTIDASES; METALLOPROTEASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIENZYME COMPLEXES; PLANTS, GENETICALLY MODIFIED; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; THERMODYNAMICS; THYLAKOIDS;

EID: 84860433169     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036008     Document Type: Article

References (52)

1. Stock D, Gibbons C, Arechaga I, Leslie AG, Walker JE, (2000) The rotary mechanism of ATP synthase. Curr Opin Struct Biol 10: 672-679.
2. Ogura T, Wilkinson AJ, (2001) AAA+ superfamily ATPases: common structure-diverse function. Genes Cells 6: 575-597.
3. Hanson PI, Whiteheart SW, (2005) AAA+ proteins: have engine, will work. Nat Rev Mol Cell Biol 6: 519-529.
4. Bar-Nun S, Glickman MH, (2011) Proteasomal AAA-ATPases: Structure and function. Biochim Biophys Acta.
5. Smith DM, Fraga H, Reis C, Kafri G, Goldberg AL, (2011) ATP binds to proteasomal ATPases in pairs with distinct functional effects, implying an ordered reaction cycle. Cell 144: 526-538.
6. Langer T, (2000) AAA proteases: cellular machines for degrading membrane proteins. Trends Biochem Sci 25: 247-251.
7. Tatsuta T, Langer T, (2009) AAA proteases in mitochondria: diverse functions of membrane-bound proteolytic machines. Res Microbiol 160: 711-717.
8. Adam Z, Rudella A, van Wijk KJ, (2006) Recent advances in the study of Clp, FtsH and other proteases located in chloroplasts. Curr Opin Plant Biol 9: 234-240.
9. Sakamoto W, (2006) Protein degradation machineries in plastids. Annu Rev Plant Biol 57: 599-621.
10. Steglich G, Neupert W, Langer T, (1999) Prohibitins regulate membrane protein degradation by the m-AAA protease in mitochondria. Mol Cell Biol 19: 3435-4342.
11. Adam Z, Zaltsman A, Sinvany-Villalobo G, Sakamoto W, (2005) FtsH proteases in chloroplasts and cyanobacteria. Physiol Plant 123: 386-390.
12. Sakamoto W, Zaltsman A, Adam Z, Takahashi Y, (2003) Coordinated regulation and complex formation of YELLOW VARIEGATED1 and YELLOW VARIEGATED2, chloroplastic FtsH metalloproteases involved in the repair cycle of photosystem II in Arabidopsis thylakoid membranes. Plant Cell 15: 2843-2855.
13. Urantowka A, Knorpp C, Olczak T, Kolodziejczak M, Janska H, (2005) Plant mitochondria contain at least two i-AAA-like complexes. Plant Mol Biol 59: 239-252.
14. Sinvany-Villalobo G, Davydov O, Ben-Ari G, Zaltsman A, Raskind A, et al. (2004) Expression in multigene families. Analysis of chloroplast and mitochondrial proteases. Plant Physiol 135: 1336-1345.
15. Friso G, Giacomelli L, Ytterberg AJ, Peltier JB, Rudella A, et al. (2004) In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions, and a plastid proteome database. Plant Cell 16: 478-499.
16. Yu F, Park S, Rodermel SR, (2004) The Arabidopsis FtsH metalloprotease gene family: interchangeability of subunits in chloroplast oligomeric complexes. Plant J 37: 864-876.
17. Chen M, Choi Y, Voytas DF, Rodermel S, (2000) Mutations in the Arabidopsis VAR2 locus cause leaf variegation due to the loss of a chloroplast FtsH protease. Plant J 22: 303-313.
18. Takechi K, Sodmergen, Murata M, Motoyoshi F, Sakamoto W, (2000) The YELLOW VARIEGATED (VAR2) locus encodes a homologue of FtsH, an ATP- dependent protease in Arabidopsis. Plant Cell Physiol 41: 1334-1346.
19. Sakamoto W, Tamura T, Hanba-Tomita Y, Sodmergen, Murata M, (2002) The VAR1 locus of Arabidopsis encodes a chloroplastic FtsH and is responsible for leaf variegation in the mutant alleles. Genes Cells 7: 769-780.
20. Zaltsman A, Feder A, Adam Z, (2005) Developmental and light effects on the accumulation of FtsH protease in Arabidopsis chloroplasts - implications for thylakoid formation and photosystem II maintenance. Plant J 42: 609-617.
21. Lindahl M, Spetea C, Hundal T, Oppenheim AB, Adam Z, et al. (2000) The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein. Plant Cell 12: 419-431.
22. Bailey S, Thompson E, Nixon PJ, Horton P, Mullineaux CW, et al. (2002) A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo. J Biol Chem 277: 2006-2011.
23. Kato Y, Miura E, Ido K, Ifuku K, Sakamoto W, (2009) The variegated mutants lacking chloroplastic FtsHs are defective in D1 degradation and accumulate reactive oxygen species. Plant Physiol 151: 1790-1801.
24. Yoshioka M, Uchida S, Mori H, Komayama K, Ohira S, et al. (2006) Quality control of photosystem II. Cleavage of reaction center D1 protein in spinach thylakoids by FtsH protease under moderate heat stress. J Biol Chem 281: 21660-21669.
25. Chen J, Burke JJ, Velten J, Xin Z, (2006) FtsH11 protease plays a critical role in Arabidopsis thermotolerance. Plant J 48: 73-84.
26. Silva P, Thompson E, Bailey S, Kruse O, Mullineaux CW, et al. (2003) FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp PCC 6803. The Plant cell 15: 2152-2164.
27. Komenda J, Tichy M, Prasil O, Knoppova J, Kuvikova S, et al. (2007) The exposed N-terminal tail of the D1 subunit is required for rapid D1 degradation during photosystem II repair in Synechocystis sp PCC 6803. The Plant cell 19: 2839-2854.
28. Zaltsman A, Ori N, Adam Z, (2005) Two types of FtsH protease subunits are required for chloroplast biogenesis and Photosystem II repair in Arabidopsis. Plant Cell 17: 2782-2790.
29. Yu F, Park S, Rodermel SR, (2005) Functional redundancy of AtFtsH metalloproteases in thylakoid membrane complexes. Plant Physiol 138: 1957-1966.
30. Krzywda S, Brzozowski AM, Verma C, Karata K, Ogura T, et al. (2002) The crystal structure of the AAA domain of the ATP-dependent protease FtsH of Escherichia coli at 1.5 A resolution. Structure 10: 1073-1083.
31. Bieniossek C, Schalch T, Bumann M, Meister M, Meier R, et al. (2006) The molecular architecture of the metalloprotease FtsH. Proc Natl Acad Sci U S A 103: 3066-3071.
32. Suno R, Niwa H, Tsuchiya D, Zhang X, Yoshida M, et al. (2006) Structure of the whole cytosolic region of ATP-dependent protease FtsH. Mol Cell 22: 575-585.
33. Bieniossek C, Niederhauser B, Baumann UM, (2009) The crystal structure of apo-FtsH reveals domain movements necessary for substrate unfolding and translocation. Proc Natl Acad Sci U S A 106: 21579-21584.
34. Dolan MA, Noah JW, Hurt D, (2012) Comparison of common homology modeling algorithms: application of user-defined alignments. Methods in molecular biology (Clifton, N J) 857: 399-414.
35. Ren X, Kloer DP, Kim YC, Ghirlando R, Saidi LF, et al. (2009) Hybrid structural model of the complete human ESCRT-0 complex. Structure (London, England: 1993) 17: 406-416.
36. Prag G, Watson H, Kim YC, Beach BM, Ghirlando R, et al. (2007) The Vps27/Hse1 complex is a GAT domain-based scaffold for ubiquitin-dependent sorting. Developmental cell 12: 973-986.
37. Chothia C, Janin J, (1975) Principles of protein-protein recognition. Nature 256: 705-708.
38. Chothia C, (1975) Structural invariants in protein folding. Nature 254: 304-308.
39. Eisenberg D, McLachlan AD, (1986) Solvation energy in protein folding andbinding. Nature 319: 199-203.
40. Vallone B, Miele AE, Vecchini P, Chiancone E, Brunori M, (1998) Free energy of burying hydrophobic residues in the interface between protein subunits. Proc Natl Acad Sci U S A 95: 6103-6107.
41. Miura E, Kato Y, Matsushima R, Albrecht V, Laalami S, et al. (2007) The balance between protein synthesis and degradation in chloroplasts determines leaf variegation in Arabidopsis yellow variegated mutants. Plant Cell 19: 1313-1328.
42. Yu F, Liu X, Alsheikh M, Park S, Rodermel S, (2008) Mutations in SUPPRESSOR OF VARIEGATION1, a factor required for normal chloroplast translation, suppress var2-mediated leaf variegation in Arabidopsis. Plant Cell 20: 1786-1804.
43. Schroda M, Vallon O, (2008) Chaperones and chaperone-associated proteases in Chlamydomonas. In The New Chlamydomonas Sourcebook, Stern D (ed) 2: 671-729.
44. Arlt H, Tauer R, Feldmann H, Neupert W, Langer T, (1996) The YTA10-12 complex, an AAA protease with chaperone-like activity in the inner membrane of mitochondria. Cell 85: 875-885.
45. Augustin S, Gerdes F, Lee S, Tsai FT, Langer T, et al. (2009) An intersubunit signaling network coordinates ATP hydrolysis by m-AAA proteases. Mol Cell 35: 574-585.
46. Combet C, Jambon M, Deléage G, Geourjon C, (2002) Geno3D an automated protein modelling Web server. Bioinformatics 18: 213-214.
47. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystalog 53: 240-255.
48. DeLano WL, (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA.
49. Project CC (1994) The CCP4 suite: programs for protein crystallography. Acta Crystalog 50: 760-763.
50. Clough SJ, Bent AF, (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
51. Aronsson H, Jarvis P, (2002) A simple method for isolating import-competent Arabidopsis chloroplasts. FEBS Lett 529: 215-220.
52. Beer I, Barnea E, Ziv T, Admon A, (2004) Improving large-scale proteomics by clustering of mass spectrometry data. Proteomics 4: 950-960.