The HU protein from Thermotoga maritima: Recombinant expression, purification and physicochemical characterization of an extremely hyperthermophilic DNA-binding protein

Journal of Molecular Biology

Volumn 291, Issue 5, 1999, Pages 1135-1146

  Esser, Dirk ^a   Rudolph, Rainer ^a   Jaenicke, Rainer ^b   Böhm, Gerald ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

DNA stability; DNA binding protein; Histone like protein; Hyperthermophilic protein; Thermotoga maritima

Indexed keywords

DNA BINDING PROTEIN; DNA FRAGMENT; DOUBLE STRANDED DNA; HISTONE; RECOMBINANT PROTEIN;

ARTICLE; CIRCULAR DICHROISM; DNA DEGRADATION; EUBACTERIUM; ION EXCHANGE CHROMATOGRAPHY; MOLECULAR CLONING; MOLECULAR MODEL; NONHUMAN; PHYSICAL CHEMISTRY; PRECIPITATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SURFACE PLASMON RESONANCE; THERMOPHILIC BACTERIUM;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; THERMOTOGA MARITIMA;

EID: 0033520513     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3022     Document Type: Article

References (55)

1. Bailey M., Hagmar P., Millar D. P., Davidson B. E., Tong G., Haralambidis J., Sawyer W. H. Interaction between the Escherichia coli regulatory protein TyrR and DNA: a fluorescence footprinting study. Biochemistry. 34:1995;15802-15812.
2. Bewley C. A., Gronenborn A. M., Clore G. M. Minor groove-binding architectural proteins: structure, function, and DNA recognition. Annu. Rev. Biophys. Biomol. Struct. 27:1998;105-131.
3. Böhm G., Jaenicke R. Correlation functions as a tool for protein modeling and structure analysis. Protein Sci. 1:1992;1269-1278.
4. Böhm G., Jaenicke R. Relevance of sequence statistics for the extremophilic behavior of proteins. Int. J. Pept. Protein Res. 43:1994;97-106.
5. Böhm G., Muhr R., Jaenicke R. Quantitative analysis of protein far UV circular dichroism spectra by neural networks. Protein Eng. 5:1992;191-195.
6. Bonnefoy E., Rouvière-Yaniv J. HU and IHF, two homologous histone-like proteins of Escherichia coli, form different protein-DNA complexes with short DNA fragments. EMBO J. 10:1991;687-696.
7. Bonnefoy E., Takahashi M., Yaniv J. R. DNA-binding parameters of the HU protein of Escherichia coli to cruciform DNA. J. Mol. Biol. 242:1994;16-29.
8. Boubrik F., Bonnefoy E., Rouvière-Yaniv J. HU and IHF: similarities and differences in Escherichia coli, the lack of HU is not compensated for by IHF. Res. Microbiol. 142:1991;239-247.
9. Brown B. M., Bowie J. U., Sauer R. T. Arc repressor is tetrameric when bound to operator DNA. Biochemistry. 29:1990;11189-11195.
10. Broyles S. S., Pettijohn D. E. Interaction of the Escherichia coli HU protein with DNA. Evidence for formation of nucleosome-like structures with altered DNA helical pitch. J. Mol. Biol. 187:1986;47-60.
11. Bruck I., Woodgate R., McEntee K., Goodman M. F. Purification of a soluble UmuD'C complex from Escherichia coli. Cooperative binding of UmuD'C to single-stranded DNA. J. Biol. Chem. 271:1996;10767-10774.
12. Cann J. R., Pfenninger O., Pettijohn D. E. Theory of the mobility-shift assay of nonspecific protein-DNA complexes governed by conditional probabilities: the HU:DNA complex. Electrophoresis. 16:1995;881-887.
13. Castaing B., Zelwer C., Laval J., Boiteux S. HU protein of Escherichia coli binds specifically to DNA that contains single-strand breaks or gaps. J. Biol. Chem. 270:1995;10291-10296.
14. Connolly M. L. The molecular surface package. J. Mol. Graph. 11:1993;139-141.
15. Coombs R. O., Cann J. R. Extended theory of the electrophoretic mobility-shift analysis of nonspecific protein-DNA complexes, featuring cooperativity. Electrophoresis. 17:1996;12-19.
16. Dams T., Böhm G., Auerbach G., Bader G., Schurig H., Jaenicke R. Homo-dimeric recombinant dihydrofolate reductase from Thermotoga maritima shows extreme intrinsic stability. Biol. Chem. 379:1998;367-371.
17. Drlica K., Rouvière-Yaniv J. Histone-like proteins of bacteria. Microbiol. Rev. 51:1987;301-319.
18. Ellenberger T., Landy A. A good turn for DNA: the structure of integration host factor bound to DNA. Structure. 5:1997;153-157.
19. Flashner Y., Gralla J. D. DNA dynamic flexibility and protein recognition: differential stimulation by bacterial histone-like protein HU. Cell. 54:1988;713-721.
20. Frishman D., Argos P. Knowledge-based protein secondary structure assignment. Proteins: Struct. Funct. Genet. 23:1995;566-579.
21. Goshima N., Inagaki Y., Otaki H., Tanaka H., Hayashi N., Imamoto F., Kano Y. Chimeric HU-IHF proteins that alter DNA-binding ability. Gene. 118:1992;97-102.
22. Härd T., Sayre M. H., Geiduschek E. P., Kearns D. R. A type II DNA-binding protein genetically engineered for fluorescence spectroscopy: the "arm" of transcription factor I binds in the DNA grooves. Biochemistry. 28:1989;2813-2819.
23. Heck H. D. Statistical theory of cooperative binding to proteins. The Hill equation and the binding potential. J. Am. Chem. Soc. 93:1971;23-29.
24. Hodges-Garcia Y., Hagerman P. J., Pettijohn D. E. DNA ring closure mediated by protein HU. J. Biol. Chem. 264:1989;14621-14623.
25. Jaenicke R., Böhm G. The stability of proteins in extreme environments. Curr. Opin. Struct. Biol. 8:1998;738-748.
26. Jaenicke R., Schurig H., Beaucamp N., Ostendorp R. Structure and stability of hyperstable proteins: glycolytic enzymes from hyperthermophilic bacterium Thermotoga maritima. Advan. Protein Chem. 48:1996;181-269.
27. Kawamura S., Kakuta Y., Tanaka I., Hikichi K., Kuhara S., Yamasaki N., Kimura M. Glycine-15 in the bend between two alpha-helices can explain the thermostability of DNA binding protein HU fromBacillus stearothermophilus. Biochemistry. 35:1996;1195-1200.
28. Kawamura S., Tanaka I., Yamasaki N., Kimura M. Contribution of a salt bridge to the thermostability of DNA binding protein HU from Bacillus stearothermophilus determined by site-directed mutagenesis. J. Biochem. (Tokyo). 121:1997;448-455.
29. 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.
30. Kraulis P. J. M OLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
31. Lavoie B. D., Chaconas G. A second high affinity HU binding site in the phage Mu transpososome. J. Biol. Chem. 269:1994;15571-15576.
32. Lavoie B. D., Shaw G. S., Millner A., Chaconas G. Anatomy of a flexer-DNA complex inside a higher-order transposition intermediate. Cell. 85:1996;761-771.
33. Losso M. A., Pawlik R. T., Canonaco M. A., Gualerzi C. O. Proteins from the prokaryotic nucleoid. Eur. J. Biochem. 155:1986;27-32.
34. Merritt E. A., Bacon D. J. R ASTER 3D: photorealistic molecular graphics. Methods Enzymol. 277:1997;505-524.
35. Murphy L. D., Zimmerman S. B. Macromolecular crowding effects on the interaction of DNA with Escherichia coli DNA-binding proteins: a model for bacterial nucleoid stabilization. Biochim. Biophys. Acta. 1219:1994;277-284.
36. Nichol L. W., Smith G. D., Ogston A. G. The effects of isomerization and polymerization on the binding of ligands to acceptor molecules: implications in metabolic control. Biochim. Biophys. Acta. 184:1969;1-10.
37. Nicholls A., Sharp K. A., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11:1991;281-296.
38. Oberto J., Rouvière-Yaniv J. Serratia marcescens contains a heterodimeric HU protein like Escherichia coli and Salmonella typhimurium. J. Bacteriol. 178:1996;293-297.
39. Ostendorp R., Auerbach G., Jaenicke R. Extremely thermostable L(+)-lactate dehydrogenase from Thermotoga maritima cloning: characterization, and crystallization of the recombinant enzyme in its tetrameric and octameric state. Protein Sci. 5:1996;862-873.
40. Padas P. M., Wilson K. S., Vorgias C. E. The DNA-binding protein HU from mesophilic and thermophilic bacilli: gene cloning, overproduction and purification. Gene. 117:1992;39-44.
41. Paull T. T., Haykinson M. J., Johnson R. C. The non-specific DNA-binding and bending proteins HMG1 and HMG2 promote the assembly of complex nucleoprotein structures. Genes Dev. 7:1993;1521-1534.
42. Pontiggia A., Negri A., Beltrame M., Bianchi M. E. Protein HU binds specifically to kinked DNA. Mol. Microbiol. 7:1993;343-350.
43. Rice P. A., Yang S., Mizuuchi K., Nash H. A. Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn. Cell. 87:1996;1295-1306.
44. Rudolph R., Böhm G., Lilie H., Jaenicke R. Folding proteins. Creighton T. E. Protein Function: A Practical Approach. 1996;IRL Press, Oxford University Press, Oxford.
45. Sâli A., Blundell T. L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234:1993;779-815.
46. Schurig H., Beaucamp N., Ostendorp R., Jaenicke R., Adler E., Knowles J. R. Phosphoglycerate kinase and triosephosphate isomerase from the hyperthermophilic bacterium Thermotoga maritima form a covalent bifunctional enzyme complex. EMBO J. 14:1995;442-451.
47. Scopes R. K. Measurement of protein by spectrophotometry at 205 nm. Anal. Biochem. 59:1974;277-282.
48. Shimizu M., Miyake M., Kanke F., Matsumoto U., Shindo H. Characterization of the binding of HU and IHF, homologous histone-like proteins of Escherichia coli, to curved and uncurved DNA. Biochim. Biophys. Acta. 1264:1995;330-336.
49. Sippl M. J. Knowledge based potentials for proteins. Curr. Opin. Struct. Biol. 5:1995;229-235.
50. 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.
51. Vis H., Mariani M., Vorgias C. E., Wilson K. S., Kaptein R., Boelens R. Solution structure of the HU protein from Bacillus stearothermophilus. J. Mol. Biol. 254:1995;692-703.
52. Vriend G. W HAT I F: a molecular modeling and drug design program. J. Mol. Graph. 8:1990;52-56.
53. Welfle H., Misselwitz R., Welfle K., Groch N., Heinemann U. Salt-dependent and protein-concentration-dependent changes in the solution structure of the DNA-binding histone-like protein, HBsu, from Bacillus subtilis. Eur. J. Biochem. 204:1992;1049-1055.
54. White S. W., Appelt K., Wilson K. S., Tanaka I. A structural motif that bends DNA. Proteins: Struct. Funct. Genet. 5:1989;281-288.
55. Wilson K. S., Vorgias C. E., Tanaka I., White S. W., Kimura M. The thermostability of DNA-binding protein HU from bacilli. Protein Eng. 4:1990;11-22.