Chaperone activity of Cyp18 through hydrophobic condensation that enables rescue of transient misfolded molten globule intermediates

Biochemistry

Volumn 49, Issue 6, 2010, Pages 1137-1145

  Moparthi, Satish Babu ^a   Fristedt, Rikard ^a   Mishra, Rajesh ^b   Almstedt, Karin ^a   Karlsson, Martin ^a   Hammarstr̈om, Per ^a   Carlsson, Uno ^a  

^a LINKÖPING UNIVERSITY   (Sweden)

^b UNIVERSITY OF ALLAHABAD   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING DATA; CHAPERONE ACTIVITY; CITRATE SYNTHASE; CYCLOPHILIN; FOLDING REACTIONS; HUMAN CARBONIC ANHYDRASE II; ISOMERASES; MISFOLDING; MOLTEN GLOBULE; MULTI DOMAINS; NATIVE PROTEINS; NATIVE-STATE PROTEIN; PROTEIN SUBSTRATE; REFOLDING; SINGLE DOMAINS; SUBSTRATE PROTEINS;

CARBONIC ANHYDRASE; CONDENSATION; HYDROPHOBICITY; PROTEINS;

REACTION INTERMEDIATES;

CARBONATE DEHYDRATASE II; CHAPERONIN; CITRATE SYNTHASE; CYCLOPHILIN; CYCLOPHILIN 18; UNCLASSIFIED DRUG;

ARTICLE; CATALYST; HUMAN; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STABILITY;

ANILINO NAPHTHALENESULFONATES; CARBONIC ANHYDRASE II; CYCLOPHILINS; ENZYME STABILITY; FLUORESCENT DYES; HUMANS; HYDROPHOBICITY; MOLECULAR CHAPERONES; MOLECULAR WEIGHT; MUTAGENESIS, SITE-DIRECTED; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY; UP-REGULATION;

EID: 76749168158     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi901997q     Document Type: Article

References (48)

1. Schmid, F. X. (2001) Prolyl isomerases. Adv. Protein Chem. 59, 243-282.
2. Fangḧanel, J., and Fischer, G. (2004) Insights into the catalytic mechanism of peptidyl prolyl cis/trans isomerases. Front. Biosci. 9, 3453-3478.
3. Wilkinson, B., and Gilbert, H. F. (2004) Protein disulfide isomerase. Biochim. Biophys. Acta 1699, 35-44.
4. Tu, B. P., and Weissmann, J. S. (2004) Oxidative protein folding in eukaryotes: Mechanisms and consequences. J. Cell Biol. 164, 341-346.
5. Handshuhmacher, R. E., Harding, M. W., Rice, J., Drugge, R. J., and Speicher, D. W. (1984) Cyclophilin: A specific cytosolic binding protein for cyclosporin A. Science 226, 544-547.
6. Fischer, G., Wittmann-Liebold, B., Lang, K., Kiefhaber, T., and Schmid, F. X. (1989) Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature 337, 476-478.
7. Takahashi, N., Hayano, T., and Suzuki, M. (1989) Peptidyl-prolyl cis-trans isomerase is the cyclosporin A-binding protein cyclophilin. Nature 337, 473-475.
8. Freskgå rd, P.-O., Bergenhem, N., Jonsson, B.-H., Svensson, M., and Carlsson, U. (1992) Isomerase and chaperone activity of prolyl isomerase in the folding of carbonic anhydrase. Science 258, 466-468.
9. Kern, G., Kern, D., Schmid, F. X., and Fischer, G. (1994) Reassessment of the putative chaperone function of prolyl-cis/transisomerases. FEBS Lett. 348, 145-148.
10. Kern, G., Kern, D., Schmid, F. X., and Fischer, G. (1995) A kinetic analysis of the folding of human carbonic anhydrase II and its catalysis by cyclophilin. J. Biol. Chem. 270, 740-745.
11. Bose, S., Weikl, T., B̈ugl, H., and Buchner, J. (1996) Chaperone function of Hsp90-associated proteins. Science 274, 1718-1720.
12. Freeman, B. C., Toft, D. O., and Morimoto, R. (1996) Molecular chaperone machines: Chaperone activities of the cyclophilin Cyp-40 and the steroid aporeceptor-associated protein p23. Science 274, 1718-1720.
13. Pirkl, F., and Buchner, J. (2001) Functional analysis of the Hsp90-associated human peptidyl prolyl cis/trans isomerases FKBP51, FKBP52 and Cyp40. J. Mol. Biol. 308, 795-806.
14. Ramm, K., and Pl̈uckthun, A. (2000) The periplasmic Escherichia coli peptidylprolyl cis,trans-isomerase FkpA. II. Isomerase-independent chaperone activity in vitro. J. Biol. Chem. 275, 17106-17113.
15. Behrens, S., Maier, R., de Cock, H., Schmid, F. X., and Gross, C. A. (2001) The SurA periplasmic PPIase lacking its parvulin domains functions in vivo and has chaperone activity. EMBO J. 20, 285-294.
16. Huang, G. C., Li, Z. Y., Zhou, J. M., and Fischer, G. (2000) Assisted folding of D-glyceraldehyde-3-phosphate dehydrogenase by trigger factor. Protein Sci. 9, 1254-1261.
17. Kurek, I., Pirkl, F., Fischer, E., Buchner, J., and Breiman, A. (2002) Wheat FKBP73 functions in vitro as a molecular chaperone independently of its peptidyl prolyl cis-trans isomerase activity. Planta 215, 119-126.
18. Ideno, A., Furutani, M., Iba, Y., Kurosawa, Y., and Maruyama, T. (2002) FK506 binding protein from the hyperthermophilic archaeon Pyrococcus horikoshii suppresses the aggregation of proteins in Escherichia coli. Appl. Environ. Microbiol. 68, 464-469.
19. Ideno, A., Yoshida, T., Iida, T., Furutani, M., and Maruyama, T. (2001) FK506-binding protein of the hyperthermophilic archaeum, Thermococcus sp. KS-1, a cold-shock-inducible peptidyl-prolyl cistrans isomerase with activities to trap and refold denatured proteins. Biochem. J. 357, 465-471.
20. Furutani, M., Ideno, A., Iida, T., and Maruyama, T. (2000) FK506 Binding Protein from a thermophilic archaeon, Methanococcus thermolithotrophicus, has chaperone-like activity in vitro. Biochemistry 39, 453-462.
21. Chakraborty, A., Das, I., Datta, R., Sen, B., Bhattacharyya, D., Mandal, C., and Datta, A. K. (2002) A single-domain cyclophilin from Leishmania donovani reactivates soluble aggregates of adenosine kinase by isomerase-independent chaperone function. J. Biol. Chem. 277, 47451-47460.
22. Scholz, C., Eckert, B., Hagn, F., Schaarschidt, P., Balbach, J., and Schmid, F. X. (2006) SlyD proteins from different species exhibt high prolyl isomerase and chaperone activities. Biochemistry 45, 20-33.
23. Buchner, J., Schmidt, M., Fuchs, M., Jaenicke, R., Rudolph, R., Schmid, F. X., and Kiefhaber, T. (1991) GroE facilitates refolding of citrate synthase by suppressing aggregation. Biochemistry 30, 1586-1591.
24. Zhi, W., Landrmy, S. J., Gierasch, L. M., and Srere, P. A. (1992) Renaturation of citrate synthase: Influence of denaturant and folding assistants. Protein Sci. 1, 522-529.
25. Nair, S. K., Calderone, T. L., Christanson, D. W., and Fierke, C. (1991) Altering the mouth of a hydrophobic pocket. Structure and kinetics of human carbonic anhydrase II mutants at residue Val-121. J. Biol. Chem. 266, 17320-17325.
26. Zydowsky, L. D., Etzkorn, F. A., Chang, H. Y., Ferguson, S. B., Stolz, L. A., Ho, S. I., and Walsh, C. T. (1992) Active site mutants of human cyclophilin A separate peptidyl-prolyl isomerase activity from cyclosporin A binding and calcineurin inhibition. Protein Sci. 1, 1092-1099.
27. Merlin, C., Masters, M., McAteer, S., and Coulson, A. (2003) Why is carbonic anhydrase essential to Escherichia coli? J. Bacteriol. 185, 6415-6424.
28. Mårtensson, L. G., Jonsson, B. H., Andersson, M., Kihlgren, A., Bergenhem, N., and Carlsson, U. (1992) Role of an evolutionarily invariant serine for the stability of human carbonic anhydrase II. Biochim. Biophys. Acta 1118, 179-186.
29. Mårtensson, L. G., Jonsson, B. H., Freskgård, P. O., Kihlgren, A., Svensson, M., and Carlsson, U. (1993) Characterization of folding intermediates of human carbonic anhydrase II: Probing substructure by chemical labeling of SH groups introduced by site-directed mutagenesis. Biochemistry 32, 224-231.
30. Mårtensson, L. G., Karlsson, M., and Carlsson, U. (2002) Dramatic stabilization of the native state of human carbonic anhydrase II by an engineered disulfide bond. Biochemistry 41, 15867-15875.
31. Scholz, C., Schindler, T., Dolinski, K., Heitman, J., and Schmid, F. X. (1997) Cyclophilin active site mutants have native prolyl isomerase activity with a protein substrate. FEBS Lett. 414, 69-73.
32. Carlsson, U., Henderson, L. E., and Lindskog, S. (1973) Denaturation and reactivation of human carbonic anhydrases in guanidine hydrochloride and urea. Biochim. Biophys. Acta 310, 376-387.
33. Almstedt, K., Mårtensson, L.-G., Carlsson, U., and Hammarstr̈om, P. (2008) Thermodynamic interrogation of a folding disease: Mutant mapping of position 107 in human carbonic anhydrase II linked to marble brain disease. Biochemistry 47, 1288-1298.
34. Fransson, C., Freskgård, P.-O., Herbertsson, H., Johansson, A., Jonasson, P., Mårtensson, L.-G., Svensson, M., Jonsson, B.-H., and Carlsson, U. (1992) Cis-trans isomerization is rate-determining in the reactivation of denatured human carbonic anhydrase II as evidenced by proline isomerase. FEBS Lett. 296, 90-94.
35. Mishra, R., Seckler, R., and Bhat, R. (2005) Efficient refolding of aggregation-prone citrate synthase by polyol osmolytes: How well are protein folding and stability aspects coupled? J. Biol. Chem. 280, 15553-15560.
36. Srere, P. A., Brazil, H., and Gonen, L. (1963) The citrate-condensing enzyme of pigeon breast muscle and moth flight muscle. Acta Chem. Scand. 17, S129-S134.
37. Almstedt, K., Lundqvist, M., Carlsson, J., Karlsson, M., Persson, B., Jonsson, B.-H., Carlsson, U., and Hammarstr̈om, P. (2004) Unfolding a folding disease: Folding, misfolding and aggregation of the marble brain syndrome-associated mutant H107Y of human carbonic anhydrase II. J. Mol. Biol. 342, 619-633.
38. Semisotnov, G. V., Rodionova, N. A., Razgulyaev, O. I., Uversky, V. N., Gripas, A. F., and Gilmanshin, R. I. (1991) Study of the "molten globule" intermediate state in protein folding by a hydrophobic fluorescent probe. Biopolymers 31, 119-128.
39. Persson, M., Lindgren, M., Hammarstr̈om, P., Svensson, M., Jonsson, B.-H., and Carlsson, U. (1999) EPR mapping of interactions between spin-labeled variants of human carbonic anhydrase II and GroEL. Evidence for increased flexibility of the hydrophobic core by the interaction. Biochemistry 38, 432-441.
40. Hammarstr̈om, P., Persson, M., and Carlsson, U. (2001) Protein compactness measured by FRET: Human carbonic anhydrase II is considerably expanded by the interaction of GroEL. J. Biol. Chem. 276, 21765-21775.
41. Moparthi, S. B., Hammarstr̈om, P., and Carlsson, U. (2009) A Nonessential Role for Arg 55 in Cyclophilin 18 for Catalysis of Proline Isomerization during Protein Folding. Protein Sci. 18, 475-479.
42. Andersson, D., Freskgård, P.-O., Jonsson, B.-H., and Carlsson, U. (1997) Formation of local asymmetric structures in the slow folding reaction of human carbonic anhydrase II. Biochemistry 36, 4623-4630.
43. Schiene-Fischer, C., Habazetti, J., Tradler, T., and Fischer, G. (2002) Evaluation of similarities in the cis/trans isomerase function of trigger factor and DnaK. Biol. Chem. 383, 1865-1873.
44. Persson, M., Aronsson, G., Bergenhem, N., Freskgård, P.-O., Jonsson, B.-H., Surin, B. P., Spangfort, M. D., and Carlsson, U. (1995) GroEL/ES-mediated refolding of human carbonic anhydrase II: Role of N-terminal helices as recognition motifs for GroEL. Biochim. Biophys. Acta 1247, 195-200.
45. Karlsson, M., Mårtensson, L.-G., Olofsson, P., and Carlsson, U. (2004) Circumnavigating misfolding traps in the energy landscape through protein engineering: Suppression of molten globule and aggregation in carbonic anhydrase. Biochemistry 43, 6803-6807.
46. Smajlovic, A., Berbic, S., Schiene-Fischer, C., Tusek-Znidaric, M., Taler, A., Jenko-Kokalj, S., Turk, D., and Zerovnik, E. (2009) Essential rol of Pro 74 in stefin B amyloid-fibril formation: Dual action of cyclophilin A on the process. FEBS Lett. 583, 1114-1120.
47. Mikol, V., Kallen, J., Pfl̈ugl, G., and Walkinshaw, M. D. (1993) X-ray structure of a monomeric cyclophilin A-cyclosporin A crystal complex at 2.1 Å resolution. J. Mol. Biol. 234, 1119-1130.
48. Ou, W.-B., Wei, L., Park, Y.-D., and Zhou, H.-M. (2001) Chaperonelike activity of peptidyl-prolyl cis-trans isomerase during creatin kinase refolding. Protein Sci. 10, 2346-2355.