Identification of a potential hydrophobic peptide binding site in the C-terminal arm of trigger factor

Protein Science

Volumn 16, Issue 6, 2007, Pages 1165-1175

  Shi, Yi ^a,b   Fan, Dong Jie ^a,b   Li, Shu Xin ^a,b   Zhang, Hong Jie ^a   Perrett, Sarah ^a   Zhou, Jun Mei ^a  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Binding site; Bis ANS; Chaperone; Hydrophobic interaction; Trigger factor

Indexed keywords

4,4' DIANILINO 1,1' BINAPHTHYL 5,5' DISULFONIC ACID DIPOTASSIUM; 8 ANILINO 1 NAPHTHALENESULFONIC ACID; ASPARAGINE; CHAPERONE; CHYMOTRYPSIN A; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; LYSINE; PEPTIDE; POTASSIUM DERIVATIVE; TRYPSIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; COMPUTER MODEL; ESCHERICHIA COLI; HYDROPHOBICITY; LYSOSOME; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; STOICHIOMETRY; ULTRAVIOLET RADIATION;

ANILINO NAPHTHALENESULFONATES; BINDING SITES; ESCHERICHIA COLI PROTEINS; HYDROPHOBICITY; MODELS, MOLECULAR; PEPTIDES; PEPTIDYLPROLYL ISOMERASE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; ULTRAVIOLET RAYS;

ESCHERICHIA COLI;

EID: 34249778396     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.062623707     Document Type: Article

References (47)

1. Baram, D., Pyetan, E., Sittner, A., Auerbach-Nevo, T., Bashan, A., and Yonath, A. 2005. Structure of trigger factor binding domain in biologically homologous complex with eubacterial ribosome reveals its chaperone action. Proc. Natl. Acad. Sci. 102: 12017-12022.
2. Cantor, C.R. and Schimmel, P.R. 1980. Biophysical chemistry. W.H. Freeman and Company. San Francisco, CA.
3. Deuerling, E. and Bukau, B. 2004. Chaperone-assisted folding of newly synthesized proteins in the cytosol. Crit. Rev. Biochem. Mol. Biol. 39: 261-277.
4. Ferbitz, L., Maier, T., Patzelt, H., Bukau, B., Deuerling, E., and Ban, N. 2004. Trigger factor in complex with the ribosome forms a molecular cradle for nascent proteins. Nature 431: 590-596.
5. Genevaux, P., Keppel, F., Schwager, F., Langendijk-Genevaux, P.S., Hartl, F.U., and Georgopoulos, C. 2004. In vivo analysis of the overlapping functions of DnaK and trigger factor. EMBO Rep. 5: 195-200.
6. Hartl, F.U. and Hayer-Hartl, M. 2002. Molecular chaperones in the cytosol: From nascent chain to folded protein. Science 295: 1852-1858.
7. Hesterkamp, T. and Bukau, B. 1996. Identification of the prolyl isomerase domain of Escherichia coli trigger factor. FEBS Lett. 385: 67-71.
8. 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. 93: 4437-4441.
9. Hesterkamp, T., Deuerling, E., and Bukau, B. 1997. The amino-terminal 118 amino acids of Escherichia coli trigger factor constitute a domain that is necessary and sufficient for binding to ribosomes. J. Biol. Chem. 272: 21865-21871.
10. Hoffmann, A., Merz, F., Rutkowska, A., Zachmann-Brand, B., Deuerling, E., and Bukau, B. 2006. Trigger factor forms a protective shield for nascent polypeptides at the ribosome. J. Biol. Chem. 281: 6539-6545.
11. Houry, W.A. 2001. Chaperone-assisted protein folding in the cell cytoplasm. Curr. Protein Pept. Sci. 2: 227-244.
12. Huang, C.Y. 1982. Determination of binding stoichiometry by the continuous variation method: The Job plot. Methods Enzymol. 87: 509-525.
13. Huang, G.C., Li, Y., Zhou, J.M., and Fischer, G. 2000. Assisted folding of D-glyceraldehyde-3-phosphate dehydrogenase by trigger factor. Protein Sci. 9: 1254-1261.
14. Huang, G.C., Chen, J.J., Liu, C.P., and Zhou, J.M. 2002. Chaperone and antichaperone activities of trigger factor. Eur. J. Biochem. 269: 4516-4523.
15. Kramer, G., Patzelt, H., Rauch, T., Kurz, T.A., Vorderwulbecke, S., Bukau, B., and Deuerling, E. 2004a. Trigger factor peptidyl-prolyl cis/trans isomerase activity is not essential for the folding of cytosolic proteins in Escherichia coli. J. Biol. Chem. 279: 14165-14170.
16. Kramer, G., Rutkowska, A., Wegrzyn, R.D., Patzelt, H., Kurz, T.A., Merz, F., Rauch, T., Vorderwulbecke, S., Deuerling, E., and Bukau, B. 2004b. Functional dissection of Escherichia coli trigger factor: Unraveling the function of individual domains. J. Bacteriol. 186: 3777-3784.
17. Lakowicz, J.R. 1983. Principles of fluorescence spectroscopy. Plenum Press, New York and London, UK.
18. Lee, G.J., Roseman, A.M., Saibil, H.R., and Vierling, E. 1997. A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO J. 16: 659-671.
19. Li, Z.Y. and Zhou, J.M. 2000. Conformational change of dihydrofolate reductase near the active site after thiol modification: Detected by limited proteolysis. Biochim. Biophys. Acta 1481: 37-44.
20. Li, Z.Y., Liu, C.P., Zhu, L.Q., Jing, G.Z., and Zhou, J.M. 2001. The chaperone activity of trigger factor is distinct from its isomerase activity during coexpression with adenylate kinase in Escherichia coli. FEBS Lett. 506: 108-112.
21. Liang, J.J. and Liu, B.F. 2006. Fluorescence resonance energy transfer study of subunit exchange in human lens crystallins and congenital cataract crystallin mutants. Protein Sci. 15: 1619-1627.
22. Liang, S.J., Lin, Y.Z., Zhou, J.M., Tsou, C.L., Wu, P.Q., and Zhou, Z.K. 1990. Dissociation and aggregation of D-glyceraldehyde-3-phosphate dehydrogenase during denaturation by guanidine hydrochloride. Biochim. Biophys. Acta 1038: 240-246.
23. Liu, C.P. and Zhou, J.M. 2004. Trigger factor-assisted folding of bovine carbonic anhydrase II. Biochem. Biophys. Res. Commun. 313: 509-515.
24. Liu, C.P., Perrett, S., and Zhou, J.M. 2005a. Dimeric trigger factor stably binds folding-competent intermediates and cooperates with the DnaK-DnaJ-GrpE chaperone system to allow refolding. J. Biol. Chem. 280: 13315-13320.
25. Liu, C.P., Li, Z.Y., Huang, G.C., Perrett, S., and Zhou, J.M. 2005b. Two distinct intermediates of trigger factor are populated during guanidine denaturation. Biochimie 87: 1023-1031.
26. Lookene, A., Zhang, L., Tougu, V., and Olivecrona, G. 2003. 1,1′-bis(anilino)-4-,4′-bis(naphtalene)-8,8′-disulfonate acts as an inhibitor of lipoprotein lipase and competes for binding with apolipoprotein CII. J. Biol. Chem. 278: 37183-37194.
27. Ludlam, A.V., Moore, B.A., and Xu, Z. 2004. The crystal structure of ribosomal chaperone trigger factor from Vibrio cholerae. Proc. Natl. Acad. Sci. 101: 13436-13441.
28. Maier, T., Ferbitz, L., Deuerling, E., and Ban, N. 2005. A cradle for new proteins: Trigger factor at the ribosome. Curr. Opin. Struct. Biol. 15: 204-212.
29. Merz, F., Hoffmann, A., Rutkowska, A., Zachmann-Brand, B., Bukau, B., and Deuerling, E. 2006. The C-terminal domain of E. coli trigger factor represents the central module of its chaperone activity. J. Biol. Chem. 281: 31963-31971.
30. Panda, M., Smoot, A.L., and Horowitz, P.M. 2001. The 4,4′-dipyridyl disulfideinduced formation of GroEL monomers is cooperative and leads to increased hydrophobic exposure. Biochemistry 40: 10402-10410.
31. Patzelt, H., Kramer, G., Rauch, T., Schonfeld, H.J., Bukau, B., and Deuerling, E. 2002. Three-state equilibrium of Escherichia coli trigger factor. Biol. Chem. 383: 1611-1619.
32. Prasad, A.R., Luduena, R.F., and Horowitz, P.M. 1986a. Bis(8-anilinonaphthalene-1-sulfonate) as a probe for tubulin decay. Biochemistry 25: 739-742.
33. Prasad, A.R., Luduena, R.F., and Horowitz, P.M. 1986b. Detection of energy transfer between tryptophan residues in the tubulin molecule and bound bis(8-anilinonaphthalene-1-sulfonate), an inhibitor of microtubule assembly, that binds to a flexible region on tubulin. Biochemistry 25: 3536-3540.
34. Schlunzen, F., Wilson, D.N., Tian, P., Harms, J.M., McInnes, S.J., Hansen, H.A., Albrecht, R., Buerger, J., Wilbanks, S.M., and Fucini, P. 2005. The binding mode of the trigger factor on the ribosome: Implications for protein folding and SRP interaction. Structure 13: 1685-1694.
35. Scholz, C., Stoller, G., Zarnt, T., Fischer, G., and Schmid, F.X. 1997. Cooperation of enzymatic and chaperone functions of trigger factor in the catalysis of protein folding. EMBO J. 16: 54-58.
36. Seale, J.W., Martinez, J.L., and Horowitz, P.M. 1995. Photoincorporation of 4,4′-bis(1-anilino-8-naphthalenesulfonic acid) into the apical domain of GroEL: Specific information from a nonspecific probe. Biochemistry 34: 7443-7449.
37. Seale, J.W., Brazil, B.T., and Horowitz, P.M. 1998. Photoincorporation of fluorescent probe into GroEL: Defining site of interaction. Methods Enzymol. 290: 318-323.
38. Sharma, K.K., Kaur, H., Kumar, G.S., and Kester, K. 1998a. Interaction of 1,1′-bi(4-anilino)naphthalene-5,5′-disulfonic acid with α-crystallin. J. Biol. Chem. 273: 8965-8970.
39. Sharma, K.K., Kumar, G.S., Murphy, A.S., and Kester, K. 1998b. Identification of 1,1′-bi(4-anilino)naphthalene-5,5′-disulfonic acid binding sequences in α-crystallin. J. Biol. Chem. 273: 15474-15478.
40. Sheluho, D. and Ackerman, S.H. 2001. An accessible hydrophobic surface is a key element of the molecular chaperone action of Atp11p. J. Biol. Chem. 276: 39945-39949.
41. Shi, L., Palleros, D.R., and Fink, A.L. 1994. Protein conformational changes induced by 1,1′-bis(4-anilino-5-naphthalenesulfonic acid): Preferential binding to the molten globule of DnaK. Biochemistry 33: 7536-7546.
42. Smoot, A.L., Panda, M., Brazil, B.T., Buckle, A.M., Fersht, A.R., and Horowitz, P.M. 2001. The binding of bis-ANS to the isolated GroEL apical domain fragment induces the formation of a folding intermediate with increased hydrophobic surface not observed in tetradecameric GroEL. Biochemistry 40: 4484-4492.
43. Stoller, G., Rucknagel, K.P., Nierhaus, K.H., Schmid, F.X., Fischer, G., and Rahfeld, J.U. 1995. A ribosome-associated peptidyl-prolyl cis/trans isomerase identified as the trigger factor. EMBO J. 14: 4939-4948.
44. Tomic, S., Johnson, A.E., Hartl, F.U., and Etchells, S.A. 2006. Exploring the capacity of trigger factor to function as a shield for ribosome bound polypeptide chains. FEBS Lett. 580: 72-76.
45. Valent, Q.A., Kendall, D.A., High, S., Kusters, R., Oudega, B., and Luirink, J. 1995. Early events in preprotein recognition in E. coli: Interaction of SRP and trigger factor with nascent polypeptides. EMBO J. 14: 5494-5505.
46. Zarnt, T., Tradler, T., Stoller, G., Scholz, C., Schmid, F.X., and Fischer, G. 1997. Modular structure of the trigger factor required for high activity in protein folding. J. Mol. Biol. 271: 827-837.
47. Zeng, L.L., Yu, L., Li, Z.Y., Perrett, S., and Zhou, J.M. 2006. Effect of Cterminal truncation on the molecular chaperone function and dimerization of Escherichia coli trigger factor. Biochimie 88: 613-619.