Folding and Association of an Extremely Stable Dimeric Protein from Sulfolobus islandicus

Journal of Molecular Biology

Volumn 336, Issue 1, 2004, Pages 227-240

  Zeeb, Markus ^a   Lipps, Georg ^a   Lilie, Hauke ^b   Balbach, Jochen ^a  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Folding kinetics; NMR; Protein dimer; Protein stability; Sulfolobus islandicus

Indexed keywords

DIMER; MONOMER; PROTEIN;

ARTICLE; CIRCULAR DICHROISM; CONCENTRATION (PARAMETERS); FLUORESCENCE SPECTROSCOPY; HEAT; KINETICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OPEN READING FRAME; PH; PLASMID; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY; SULFOLOBUS; SULFOLOBUS ISLANDICUS; ULTRACENTRIFUGATION;

SULFOLOBUS; SULFOLOBUS ISLANDICUS;

EID: 0346500473     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.12.003     Document Type: Article

References (50)

1. Zillig W., Kletzin A., Schleper C., Holz I., Janekovic D., Hain J., et al. Screening for Sulfolobales, their plasmids and their viruses in Icelandic solfataras. Syst. Appl. Microbiol. 16:1994;609-628.
2. Lipps G., Ibanez P., Stroessenreuther T., Hekimian K., Krauss G. The protein ORF80 from the acidophilic and thermophilic archaeon Sulfolobus islandicus binds highly site-specifically to double-stranded DNA and represents a novel type of basic leucine zipper protein. Nucl. Acids Res. 29:2001;4973-4982.
3. Lipps G., Rother S., Hart C., Krauss G. A novel type of replicative enzyme harbouring ATPase, primase and DNA polymerase activity. EMBO J. 22:2003;2516-2525.
4. Lipps G., Stegert M., Krauss G. Thermostable and site-specific DNA binding of the gene product ORF56 from the Sulfolobus islandicus plasmid pRN1, a putative archael plasmid copy control protein. Nucl. Acids Res. 29:2001;904-913.
5. Gomis-Rüth F.X., Sola M., Acebo P., Parraga A., Guasch A., Eritja R., et al. The structure of plasmid-encoded transcriptional repressor CopG unliganded and bound to its operator. EMBO J. 17:1998;7404-7415.
6. Breg J.N., van Opheusden J.H., Burgering M.J., Boelens R., Kaptein R. Structure of Arc repressor in solution: evidence for a family of beta-sheet DNA-binding proteins. Nature. 346:1990;586-589.
7. Jaenicke R. Stability and folding of domain proteins. Prog. Biophys. Mol. Biol. 71:1999;155-241.
8. Schmid F.X. Protein folding. Allen G. Proteins: A Comprehensive Treatise. 1999;153-215 JAI Press, Greenwich.
9. Gittelman M.S., Matthews C.R. Folding and stability of trp aporepressor from Escherichia coli. Biochemistry. 29:1990;7011-7020.
10. Mann C.J., Matthews C.R. Structure and stability of an early folding intermediate of Escherichia coli trp aporepressor measured by far-UV stopped-flow circular dichroism and 8-anilino-1-naphthalene sulfonate binding. Biochemistry. 32:1993;5282-5290.
11. Bowie J.U., Sauer R.T. Equilibrium dissociation and unfolding of the Arc repressor dimer. Biochemistry. 28:1989;7139-7143.
12. Milla M.E., Sauer R.T. P22 Arc repressor: folding kinetics of a single-domain, dimeric protein. Biochemistry. 33:1994;1125-1133.
13. Jaenicke R., Rudolph R., Heider I. Quaternary structure, subunit activity, and in vitro association of porcine mitochondrial malic dehydrogenase. Biochemistry. 18:1979;1217-1223.
14. Rudolph R., Fuchs I., Jaenicke R. Reassociation of dimeric cytoplasmic malate dehydrogenase is determined by slow and very slow folding reactions. Biochemistry. 25:1986;1662-1669.
15. Sterner R., Kleemann G.R., Szadkowski H., Lustig A., Hennig M., Kirschner K. Phosphoribosyl anthranilate isomerase from Thermotoga maritima is an extremely stable and active homodimer. Protein Sci. 5:1996;2000-2008.
16. Dams T., Jaenicke R. Stability and folding of dihydrofolate reductase from the hyperthermophilic bacterium Thermotoga maritima. Biochemistry. 38:1999;9169-9178.
17. Esser D., Rudolph R., Jaenicke R., Böhm G. The HU protein from Thermotoga maritima: recombinant expression, purification and physicochemical characterization of an extremely hyperthermophilic DNA-binding protein. J. Mol. Biol. 291:1999;1135-1146.
18. Thoma R., Henning M., Sterner R., Kirschner K. Structure and function of mutationally generated monomers dimeric phosphoribosylanthranilate isomerase from Thermotoga maritima. Struct. Fold. Des. 8:2000;265-276.
19. Kawamura S., Abe Y., Ueda T., Masumoto K., Imoto T., Yamasaki N., Kimura M. Investigation of the structural basis for thermostability of DNA-binding protein HU from Bacillus stearothermophilus. J. Biol. Chem. 273:1998;19982- 19987.
20. Grant S.K., Deckman I.C., Culp J.S., Minnich M.D., Brooks I.S., Hensley P., et al. Use of protein unfolding studies to determine the conformational and dimeric stabilities of HIV-1 and SIV proteases. Biochemistry. 31:1992;9491-9501.
21. Privalov P.L. Stability of proteins. Advan. Protein Chem. 33:1979;167-241.
22. Moll R., Schäfer G. Purification and characterisation of an archaebacterial succinate dehydrogenase complex from the plasma membrane of the thermoacidophile Sulfolobus acidocaldarius. Eur. J. Biochem. 201:1991;593-600.
23. Perl D., Welker C., Schindler T., Schröder K., Marahiel M.A., Jaenicke R., Schmid F.X. Conservation of rapid two-state folding in mesophilic, thermophilic and hyperthermophilic cold shock proteins. Nature Struct. Biol. 5:1998;229-235.
24. Jaenicke R., Böhm G. The stability of proteins in extreme environments. Curr. Opin. Struct. Biol. 8:1998;738-748.
25. Jaenicke R., Böhm G. Thermostability of proteins from Thermotoga maritima. Methods Enzymol. 334:2001;438-469.
26. Jaenicke R., Lilie H. Folding and association of oligomeric and multimeric proteins. Advan. Protein Chem. 53:2000;329-401.
27. Mok Y.K., de Prat Gay G., Butler P.J., Bycroft M. Equilibrium dissociation and unfolding of the dimeric human papillomavirus strain-16 E2 DNA-binding domain. Protein Sci. 5:1996;310-319.
28. Dürr E., Jelesarov I., Bosshard H.R. Extremely fast folding of a very stable leucine zipper with a strengthened hydrophobic core and lacking electrostatic interactions between helices. Biochemistry. 38:1999;870-880.
29. Kretschmar M., Jaenicke R. Stability of a homo-dimeric Ca(2+)-binding member of the beta gamma-crystallin superfamily: DSC measurements on spherulin 3a from Physarum polycephalum. J. Mol. Biol. 291:1999;1147-1153.
30. 19F NMR. Proc. Natl Acad. Sci. USA. 89:1992;7222-7226.
31. Russell B.S., Melenkivitz R., Bren K.L. NMR investigation of ferricytochrome c unfolding: detection of an equilibrium unfolding intermediate and residual structure in the denatured state. Proc. Natl Acad. Sci. USA. 97:2000;8312-8317.
32. Zeeb M., Rösner H., Zeslawski W., Canet D., Holak T.A., Balbach J. Protein folding and stability of human CDK inhibitor p19INK4d. J. Mol. Biol. 315:2002;447-457.
33. Wendt H., Leder L., Harma H., Jelesarov I., Baici A., Bosshard H.R. Very rapid, ionic strength-dependent association and folding of a heterodimeric leucine zipper. Biochemistry. 36:1997;204-213.
34. Zitzewitz J.A., Bilsel O., Luo J., Jones B.E., Matthews C.R. Probing the folding mechanism of a leucine zipper peptide by stopped-flow circular dichroism spectroscopy. Biochemistry. 34:1995;12812-12819.
35. Mok Y.K., Bycroft M., de Prat-Gay G. The dimeric DNA binding domain of the human papillomavirus E2 protein folds through a monomeric intermediate which cannot be native-like. Nature Struct. Biol. 3:1996;711-717.
36. Zitzewitz J.A., Ibarra-Molero B., Fishel D.R., Terry K.L., Matthews C.R. Preformed secondary structure drives the association reaction of GCN4-p1, a model coiled-coil system. J. Mol. Biol. 296:2000;1105-1116.
37. Wendt H., Berger C., Baici A., Thomas R.M., Bosshard H.R. Kinetics of folding of leucine zipper domains. Biochemistry. 34:1995;4097-4107.
38. Laurents D.V., Corrales S., Elias-Arnanz M., Sevilla P., Rico M., Padmanabhan S. Folding kinetics of phage 434 Cro protein. Biochemistry. 39:2000;13963-13973.
39. Grättinger M., Dankesreiter A., Schurig H., Jaenicke R. Recombinant phosphoglycerate kinase from the hyperthermophilic bacterium Thermotoga maritima: catalytic, spectral and thermodynamic properties. J. Mol. Biol. 280:1998;525-533.
40. Myers J.K., Pace C.N., Scholtz J.M. Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4:1995;2138-2148.
41. Wassenberg D., Liebl W., Jaenicke R. Maltose-binding protein from the hyperthermophilic bacterium Thermotoga maritima: stability and binding properties. J. Mol. Biol. 295:2000;279-288.
42. Cavagnero S., Debe D.A., Zhou Z.H., Adams M.W., Chan S.I. Kinetic role of electrostatic interactions in the unfolding of hyperthermophilic and mesophilic rubredoxins. Biochemistry. 37:1998;3369-3376.
43. Ogasahara K., Nakamura M., Nakura S., Tsunasawa S., Kato I., Yoshimoto T., Yutani K. The unusually slow unfolding rate causes the high stability of pyrrolidone carboxyl peptidase from a hyperthermophile Pyrococcus furiosus: equilibrium and kinetic studies of guanidine hydrochloride-induced unfolding and refolding. Biochemistry. 37:1998;17537-17544.
44. Pace C.N. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131:1986;266-280.
45. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
46. Gill S.C., von Hippel P.H. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182:1989;319-326.
47. Schellman J.A. Solvent denaturation. Biopolymers. 17:1978;1305-1322.
48. Tanford C. Protein denaturation C. Theoretical models for the mechanism of denaturation. Advan. Protein Chem. 24:1970;1-95.
49. Backes H., Berens C., Helbl V., Walter S., Schmid F.X., Hillen W. Combinations of the alpha-helix-turn-alpha-helix motif of TetR with respective residues from LacI or 434Cro: DNA recognition, inducer binding, and urea-dependent denaturation. Biochemistry. 36:1997;5311-5322.
50. Mori S., Abeygunawardana C., Johnson M.O., van Zijl P.C. Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new fast HSQC (FHSQC) detection scheme that avoids water saturation. J. Magn. Reson. ser. B. 108:1995;94-98.