Animal cells and systems

The Korean Society for Integrative Biology (한국통합생물학회)
권호 표지

Trigger Factor Interacts with DnaA Protein to Stimulate its Interaction with DnaA Box

  • Lee, Yong-Sun (Institute of Molecular Biology and Genetics, School of Biological Sciences, Seoul National University) ;
  • Lee, June (Institute of Molecular Biology and Genetics, School of Biological Sciences, Seoul National University) ;
  • Kim, Hak-Kyun (Institute of Molecular Biology and Genetics, School of Biological Sciences, Seoul National University) ;
  • Kang, Sukhyun (Institute of Molecular Biology and Genetics, School of Biological Sciences, Seoul National University) ;
  • Han, Joo-Seok (Institute of Molecular Biology and Genetics, School of Biological Sciences, Seoul National University) ;
  • Kim, Jae-Bum (Institute of Molecular Biology and Genetics, School of Biological Sciences, Seoul National University) ;
  • Hwang, Deog-Su (Institute of Molecular Biology and Genetics, School of Biological Sciences, Seoul National University)
  • Published : 2003.03.01
Download PDF
⟨ Previous Next ⟩

Abstract

While screening proteins that interact with DnaA protein, the initiator protein for Escherichia coil chromosomal DNA replication, we found a 52-kD sized protein which bound to DnaA protein in a salt-dependent manner. This protein was identified as trigger factor, a ribosome-associated peptidyl-prolyl- cisltrans isomerase with chaperone activity. Trigger factor was overproduced and purified to near homogeneity, and its effect on the function of DnaA protein was examined, Enhanced binding of DnaA protein to DnaA box with no apparent supershift in the gel-shift experiments suggested that trigger factor, by virtue of its chaperone activity, exerts a change on DnaA protein thus increasing its binding affinity for DnaA box.

Keywords

References

  1. Atlung T, Loibner-Olesen A, and Hansen FG (1985) Overproduction of DnaA protein stimulates initiation of chromosome and minichromosome replication in Escherichia coli Mol Gen Genet 206: 51-59 https://doi.org/10.1007/BF00326535
  2. Bramhill D and Kornberg A (1988a) Duplex opening by DnaA protein at novel sequences in initiation of replication at the origin of the E. coli chromosome. Cell 52: 743-755 https://doi.org/10.1016/0092-8674(88)90412-6
  3. Bramhill D and Kornberg A (1988b) A model for initiation at origins of DNA replication. Cell 54: 915-918 https://doi.org/10.1016/0092-8674(88)90102-X
  4. Burgers PJM, Kornberg A, and Sakakibara Y (1981) The dnaN codes for the ${\beta}-subunit$ of DNA polymerase III holoenzyme of E. coll Proc Natl Acad Sci USA 78: 5391-5395 https://doi.org/10.1073/pnas.78.9.5391
  5. Cassler MR, Grimwade JE, and Leonard AC (1995) Cell cycle-specific changes in nucleoprotein complexes at a chromosomal replication origin. EMBO J 14: 5833-5841
  6. Crooke E and Wickner W (1987) Trigger factor: a soluble protein that folds pro-OmpA into a membrane-assembly-competent form. Proc Natl Acad Sci USA 84: 5216-5220 https://doi.org/10.1073/pnas.84.15.5216
  7. Crooke E, Thresher R, Hwang DS, Griffith J, and Kornberg A (1993) Replicatively active complexes of DnaA protein and the Escherichia coli chromosomal origin observed in the electron microscope. J Mol Biol 233: 16-24 https://doi.org/10.1006/jmbi.1993.1481
  8. Deuerling E, Schulze-Specking A, Tomoyasu T, Mogk A, and Bukau B (1999) Trigger factor and DnaK cooperate in folding of newy synthesized proteins. Nature 400: 693-696 https://doi.org/10.1038/23301
  9. Fuller RS and Kornberg A (1983) Purified DnaA protein in initiation of replication at the Escherichia coli chromosomal origin of replication. Proc Natl Acad Sci USA 80: 5817-5821 https://doi.org/10.1073/pnas.80.19.5817
  10. Fuller RS, Kaguni JM, and Kornberg A (1981) Enzymatic replication of the origin of the Escherichia coli chromosome. Proc Natl Acad Sci USA 78: 7370-7374 https://doi.org/10.1073/pnas.78.12.7370
  11. Guthrie B and Wickner W (1990) Trigger factor depletion or overproduction causes defective cell division but does not block protein export. J Bacteriol 172: 5555-5562 https://doi.org/10.1128/jb.172.10.5555-5562.1990
  12. Hesterkamp T, Hauser S, Lutcke H, and Bukau B (1996) Escherichia coli trigger factor is a prolyl isomerase that associates with nascent polypeptide chains. Proc Natl Acad Sci USA 93: 4437-4441 https://doi.org/10.1073/pnas.93.9.4437
  13. Hirota Y, Mordoh J, and Jacob F (1970) On the process of cellular division in Escherichia coli. III. Thermosensitive mutants of Escherichia coli altered in the process of DNA initiation. J Mol Biol 53: 369-387 https://doi.org/10.1016/0022-2836(70)90072-0
  14. Huang GC, Li ZY, Zhou JM, and Fischer G (2000) Assisted folding of Dglyceraldehyde-3-phosphate dehydrogenase by trigger factor. Protein Sci 9: 1254-1261 https://doi.org/10.1110/ps.9.6.1254
  15. Hupp TR and Kaguni JM (1993) Activation of DnaA5 protein by GrpE and DnaK heat shock proteins in initiation of DNA replication in Escherichia coli. J Biol Chem 268: 13137-13142
  16. Hwang DS and Kaguni JM (1988) Purification and characterization of the dna46 gene product. J Biol Chem 263: 10625-10632
  17. Hwang DS and Kornberg A (1990) A novel protein binds a key origin sequence to block replication of E. coli minichromosome. Cell 63: 325-331 https://doi.org/10.1016/0092-8674(90)90165-B
  18. Hwang DS, Crooke E, and Kornberg A (1990) Aggregated DnaA protein is dissociated and activated for DNA replication by phospholipase or DnaK protein. J Biol Chem 265: 19244-19248
  19. Jenkins AJ, March JB, Oliver IR, and Masters M (1986) A DNA fragment containing the groE genes can suppress mutations in the Escherichia coli dnaA gene. Mol Gen Genet 202: 446-454 https://doi.org/10.1007/BF00333275
  20. Kandror O and Goldberg AL (1997) Trigger factor is induced upon cold shock and enhances viability of Escherichia coli at low temperatures. Proc Natl Acad Sci USA 94: 4978-4981 https://doi.org/10.1073/pnas.94.10.4978
  21. Kandror O, Sherman M, Rhode M, and Goldberg AL (1995) Trigger factor is involved in GroEL-dependent protein degradation in Escherichia coli and promotes binding of GroEL to unfolded proteins. EMBO J 14: 6021-6027
  22. Katayama T, Kubota T, Kurokawa K, Crooke E, and Sekimizu K (1998) The initiator function of DnaA protein is negatively regulated by the sliding clamp of the E. coli chromosomal replicase. Cell 94: 61-71 https://doi.org/10.1016/S0092-8674(00)81222-2
  23. Kornberg A and Baker TA (1992) DNA replication, second ed., W. H. Freeman and Company, New York
  24. Lobner-Olesen A, Skarstad K, Hansen FG, Meyenburg KV, and Boye E (1989) The DnaA protein determines the initiation mass of Escherichia coli K-12. Cell 57: 881-889 https://doi.org/10.1016/0092-8674(89)90802-7
  25. Lee YS Hwang DS (1997) Occlusion of RNA polymerase by oligomerization of DnaA protein over the dnaA promoter of Escherichia coli. J Biol Chem 272: 83-88 https://doi.org/10.1074/jbc.272.1.83
  26. Messer W and Weigel C (1996) Regulation of chromosome replication, in: Neidhardt FC, Curtiss III R, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (Eds.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, Second Edition, American Society for Microbiology, Washington D. C, Vol. 2, pp. 1579-1601
  27. Meyenburg KV and Hansen FG (1987) Regulation of chromosome replication, in: Neidhardt FC, Ingraham JL, Low KB, Magasanik B, Schaechter M, Umbarger HE (Eds.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, American Society for Microbiology, Washington D. C, Vol. 2, pp. 1555-1577
  28. Nishihara K, Kanemori M, Yanagi H, and Yura T (2000) Overexpression of trigger factor prevents aggregation of recombinant proteins in Escherichia coli. Appl Environ Microbiol 66: 884-889 https://doi.org/10.1128/AEM.66.3.884-889.2000
  29. Sakakibara Y and Yuasa S (1982) Continuous synthesis of the dnaA gene product of Escherichia coli in the cell cycle. Mol Gen Genet 186: 87-94 https://doi.org/10.1007/BF00422917
  30. Samitt CE, Hansen FG, Miller JF, and Schaechter M (1989) In vivo studies of DnaA binding to the origin of replication of Escherichia coli. EMBO J 8: 989-993
  31. Schaper S and Messer W (1995) Interaction of the initiator protein DnaA of Escherichia coli with its DNA targel. J Biol Chem 270: 17622-17626 https://doi.org/10.1074/jbc.270.29.17622
  32. Sekimizu K, Bramhill D, and Kornberg A (1987) ATP activates DnaA protein in initiating replication of plasmids bearing the origin of the E. coli chromosome. Cell 50: 259-265 https://doi.org/10.1016/0092-8674(87)90221-2
  33. Sharma SK (1997) Designer affinity purifications of recombinant proteins, in: P. Matejtschuk (Ed.), Affinity Separations: A Practical Approach, IRL Press at Oxford University Press: 197-218
  34. Skarstad K and Boye E (1994) The initiator protein DnaA: evolution, properties and function. Biochim Biophys Acta 1217: 111-130 https://doi.org/10.1016/0167-4781(94)90025-6
  35. Skarstad K, Lobner-Olesen A, Atlung T, Meyenburg KV, and Boye E (1989) Initiation of DNA replication in Escherichia coli after overproduction of the DnaA protein. Mol Gen Genet 218: 50-56 https://doi.org/10.1007/BF00330564
  36. Stoller G, Rucknagel KP, Nierhaus KH, Schmid FX, Fischer G, and Rahfeld JU (1995) A ribosome-associated peptidyl-prolyl cis/trans isomerase identified as the trigger factor. EMBO J 14: 4939-4948
  37. Sutton MD and Kaguni JM (1997) Threonine 435 of Escherichia coli DnaA protein confers sequence-specific DNA binding activity. J Biol Chem 272: 23017-23024 https://doi.org/10.1074/jbc.272.33.20317
  38. Teter SA, Houry WA, Ang D, Tradler T, Rockabrand D, Fischer G, Blum P, Georgopoulos C, and Hartl FU (1999) Polypeptide flux through bacterial Hsp70: DnaK cooperates with trigger factor in chaperoning nascent chains. Cell 97: 755-765 https://doi.org/10.1016/S0092-8674(00)80787-4
  39. Theisen PW, Grimwade JE, LeopardAC, BoganJA, and Helmstetter CE (1993) Correlation of gene transcription with the time of initiation of chromosome replication in Escherichia coli. Mol Microbiol 10: 575-584 https://doi.org/10.1111/j.1365-2958.1993.tb00929.x
  40. Thony B, Hwang DS, Fradkin L, and Kornberg A (1991) iciA, an Escherichia coli gene encoding a specific inhibitor of chromosomal initiation of replication in vitro. Proc Natl Acad Sci USA 88: 4066-4070 https://doi.org/10.1073/pnas.88.10.4066
  41. Woelker B and Messer W (1993) The structure of the initiation complex at the replication origin, oriC, of Escherichia coli. Nucleic Acids Res 21: 5025-5033 https://doi.org/10.1093/nar/21.22.5025