Chloroplastic Hsp100 chaperones ClpC2 and ClpD interact in vitro with a transit peptide only when it is located at the N-terminus of a protein

BMC Plant Biology

Volumn 12, Issue , 2012, Pages

  Bruch, Eduardo M ^a   Rosano, Germán L ^a   Ceccarelli, Eduardo A ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

Author keywords

Chloroplasts; Clp; Hsp100 chaperones; Protein import; Transit peptide

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; HEAT SHOCK PROTEIN; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CHEMISTRY; CHLOROPLAST; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN TRANSPORT;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; HEAT-SHOCK PROTEINS; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT;

EID: 84862187624     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-12-57     Document Type: Article

References (37)

1. Neuwald AF, Aravind L, Spouge JL, Koonin EV. AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 1999, 9:27-43.
2. Ogura T, Wilkinson AJ. AAA + superfamily ATPases: common structure-diverse function. Genes Cells 2001, 6:575-597. 10.1046/j.1365-2443.2001.00447.x, 11473577.
3. Snider J, Thibault G, Houry WA. The AAA + superfamily of functionally diverse proteins. Genome Biol 2008, 9:216. 10.1186/gb-2008-9-4-216, 2643927, 18466635.
4. Maurizi MR, Xia D. Protein binding and disruption by Clp/Hsp100 chaperones. Structure 2004, 12:175-183.
5. Schirmer EC, Glover JR, Singer MA, Lindquist S. HSP100/Clp proteins: a common mechanism explains diverse functions. Trends Biochem Sci 1996, 21:289-296.
6. Stanne TM, Pojidaeva E, Andersson FI, Clarke AK. Distinctive types of ATP-dependent Clp proteases in cyanobacteria. J Biol Chem 2007, 282:14394-14402. 10.1074/jbc.M700275200, 17371875.
7. Porankiewicz J, Wang J, Clarke AK. New insights into the ATP-dependent Clp protease: Escherichia coli and beyond. Mol Microbiol 1999, 32:449-458. 10.1046/j.1365-2958.1999.01357.x, 10320569.
8. Gottesman S, Roche E, Zhou Y, Sauer RT. The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system. Genes Dev 1998, 12:1338-1347. 10.1101/gad.12.9.1338, 316764, 9573050.
9. Adam Z, Rudella A, van Wijk KJ. Recent advances in the study of Clp, FtsH and other proteases located in chloroplasts. Curr Opin Plant Biol 2006, 9:234-240. 10.1016/j.pbi.2006.03.010, 16603408.
10. Rosano GL, Bruch EM, Ceccarelli EA. Insights into the CLP/HSP100 chaperone system from chloroplasts of Arabidopsis thaliana. J Biol Chem 2011, 286:29671-29680. 10.1074/jbc.M110.211946, 21737456.
11. Zheng B, Halperin T, Hruskova-Heidingsfeldova O, Adam Z, Clarke AK. Characterization of Chloroplast Clp proteins in Arabidopsis: Localization, tissue specificity and stress responses. Physiol Plant 2002, 114:92-101. 10.1034/j.1399-3054.2002.1140113.x, 11982939.
12. Kovacheva S, Bedard J, Wardle A, Patel R, Jarvis P. Further in vivo studies on the role of the molecular chaperone, Hsp93, in plastid protein import. Plant J 2007, 50:364-379. 10.1111/j.1365-313X.2007.03060.x, 17376159.
13. Li HM, Chiu CC. Protein transport into chloroplasts. Annu Rev Plant Biol 2010, 61:157-180. 10.1146/annurev-arplant-042809-112222, 20192748.
14. Strittmatter P, Soll J, Bolter B. The chloroplast protein import machinery: a review. Methods Mol Biol 2010, 619:307-321. 10.1007/978-1-60327-412-8_18, 20419418.
15. Nielsen E, Akita M, vila-Aponte J, Keegstra K. Stable association of chloroplastic precursors with protein translocation complexes that contain proteins from both envelope membranes and a stromal Hsp100 molecular chaperone. EMBO J 1997, 16:935-946. 10.1093/emboj/16.5.935, 1169694, 9118955.
16. Kovacheva S, Bedard J, Patel R, Dudley P, Twell D, Rios G, Koncz C, Jarvis P. In vivo studies on the roles of Tic110, Tic40 and Hsp93 during chloroplast protein import. Plant J 2005, 41:412-428.
17. Constan D, Froehlich JE, Rangarajan S, Keegstra K. A stromal Hsp100 protein is required for normal chloroplast development and function in Arabidopsis. Plant Physiol 2004, 136:3605-3615. 10.1104/pp.104.052928, 527159, 15516497.
18. Su PH, Li HM. Stromal Hsp70 is important for protein translocation into pea and Arabidopsis chloroplasts. Plant Cell 2010, 22:1516-1531. 10.1105/tpc.109.071415, 2899880, 20484004.
19. Levchenko I, Luo L, Baker TA. Disassembly of the Mu transposase tetramer by the ClpX chaperone. Genes Dev 1995, 9:2399-2408. 10.1101/gad.9.19.2399, 7557391.
20. Wickner S, Gottesman S, Skowyra D, Hoskins J, McKenney K, Maurizi MR. A molecular chaperone, ClpA, functions like DnaK and DnaJ. Proc Natl Acad Sci U S A 1994, 91:12218-12222. 10.1073/pnas.91.25.12218, 45408, 7991609.
21. Tobias JW, Shrader TE, Rocap G, Varshavsky A. The N-end rule in bacteria. Science 1991, 254:1374-1377. 10.1126/science.1962196, 1962196.
22. Sauer RT, Baker TA. AAA + Proteases: ATP-Fueled Machines of Protein Destruction. Annu Rev Biochem 2011, 80:587-612. 10.1146/annurev-biochem-060408-172623, 21469952.
23. Rial DV, Arakaki AK, Ceccarelli EA. Interaction of the targeting sequence of chloroplast precursors with Hsp70 molecular chaperones. Eur J Biochem 2000, 267:6239-6248. 10.1046/j.1432-1327.2000.01707.x, 11012678.
24. Rial DV, Ottado J, Ceccarelli EA. Precursors with altered affinity for Hsp70 in their transit peptides are efficiently imported into chloroplasts. J Biol Chem 2003, 278:46473-46481. 10.1074/jbc.M306684200, 12970339.
25. Guo F, Maurizi MR, Esser L, Xia D. Crystal structure of ClpA, an Hsp100 chaperone and regulator of ClpAP protease. J Biol Chem 2002, 277:46743-46752. 10.1074/jbc.M207796200, 12205096.
26. Creighton TE. Proteins: Structures and Molecular Properties. 2011, W. H. Freeman, Second.
27. Fitzkee NC, Rose GD. Reassessing random-coil statistics in unfolded proteins. Proc Natl Acad Sci U S A 2004, 101:12497-12502. 10.1073/pnas.0404236101, 514656, 15314216.
28. Hoskins JR, Wickner S. Two peptide sequences can function cooperatively to facilitate binding and unfolding by ClpA and degradation by ClpAP. Proc Natl Acad Sci U S A 2006, 103:909-914. 10.1073/pnas.0509154103, 1347992, 16410355.
29. Burton RE, Siddiqui SM, Kim YI, Baker TA, Sauer RT. Effects of protein stability and structure on substrate processing by the ClpXP unfolding and degradation machine. EMBO J 2001, 20:3092-3100. 10.1093/emboj/20.12.3092, 150209, 11406586.
30. Gur E, Sauer RT. Recognition of misfolded proteins by Lon, a AAA(+) protease. Genes Dev 2008, 22:2267-2277. 10.1101/gad.1670908, 2518814, 18708584.
31. Hoskins JR, Yanagihara K, Mizuuchi K, Wickner S. ClpAP and ClpXP degrade proteins with tags located in the interior of the primary sequence. Proc Natl Acad Sci U S A 2002, 99:11037-11042. 10.1073/pnas.172378899, 123206, 12177439.
32. Sharrocks AD. A T7 expression vector for producing N- and C-terminal fusion proteins with glutathione S-transferase. Gene 1994, 138:105-108. 10.1016/0378-1119(94)90789-7, 8125285.
33. Serra EC, Krapp AR, Ottado J, Feldman MF, Ceccarelli EA, Carrillo N. The precursor of pea ferredoxin-NADP + reductase synthesized in Escherichia coli contains bound FAD and is transported into chloroplasts. J Biol Chem 1995, 270:19930-19935. 10.1074/jbc.270.34.19930, 7650008.
34. Serra EC, Carrillo N, Krapp AR, Ceccarelli EA. One-step purification of plant ferredoxin-NADP + oxidoreductase expressed in Escherichia coli as fusion with glutathione S-transferase. Protein Expr Purif 1993, 4:539-546. 10.1006/prep.1993.1071, 8286951.
35. Rial DV, Ceccarelli EA. Removal of DnaK contamination during fusion protein purifications. Protein Expr Purif 2002, 25:503-507. 10.1016/S1046-5928(02)00024-4, 12182832.
36. Rosano GL, Ceccarelli EA. Rare codon content affects the solubility of recombinant proteins in a codon bias-adjusted Escherichia coli strain. Microb Cell Fact 2009, 8:41. 10.1186/1475-2859-8-41, 2723077, 19630980.
37. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685. 10.1038/227680a0, 5432063.