PH regulation of the kinetic stability of the lipase from Thermomyces lanuginosus

Biochemistry

Volumn 52, Issue 1, 2013, Pages 264-276

  Wang, H ^a   Andersen, K K ^a   Sehgal, P ^a   Hagedorn, J ^b   Westh, P ^c   Borch, K ^d   Otzen, D E ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b ABBOTT GMBH AND CO KG   (Germany)

^c ROSKILDE UNIVERSITY   (Denmark)

^d NOVOZYMES A S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION BARRIERS; CONCENTRATION RANGES; CONFORMATIONAL RIGIDITY; CRITICAL NUMBERS; DISULFIDE BONDS; FORM CLUSTERS; GENERAL CHEMICALS; GUANIDINIUM CHLORIDES; INTRINSIC KINETICS; IONIC SURFACTANTS; KINETIC STABILITY; KINETIC TRAPPING; NATIVE STATE; NEGATIVE ELECTROSTATIC POTENTIAL; NET CHARGES; PH DEPENDENCE; PH RANGE; PH REGULATION; REFOLDING; SODIUM DODECYL SULFATE; SURFACTANT CONCENTRATIONS; THERMOMYCES LANUGINOSUS; THERMOMYCES LANUGINOSUS LIPASE;

CHEMICAL STABILITY; CHLORINE COMPOUNDS; COVALENT BONDS; DENATURATION; HYSTERESIS; MOLECULES; NONIONIC SURFACTANTS; PH; PROTEINS; SODIUM; SODIUM SULFATE; UREA;

KINETICS;

DECYLMALTOSIDE; DODECYL SULFATE SODIUM; GUANIDINE; IONIC SURFACTANT; THERMOMYCES LANUGINOSUS LIPASE; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL BINDING; CONCENTRATION (PARAMETERS); CONFORMATIONAL TRANSITION; ENZYME KINETICS; HYSTERESIS; MICELLE; PH; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STABILITY; SENSITIVITY ANALYSIS; STATIC ELECTRICITY;

ASCOMYCOTA; ENZYME STABILITY; GLUCOSIDES; HYDROGEN-ION CONCENTRATION; KINETICS; LIPASE; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DENATURATION; SODIUM DODECYL SULFATE; SURFACE-ACTIVE AGENTS; UREA;

THERMOMYCES LANUGINOSUS;

EID: 84872116347     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi301258e     Document Type: Article

References (45)

1. Sanchez-Ruiz, J. M. (2010) Protein kinetic stability Biophys. Chem. 148, 1-15
2. Cunningham, E. L., Jaswal, S. S., Sohl, J. L., and Agard, D. A. (1999) Kinetic stability as a mechanism for protease longevity Proc. Natl. Acad. Sci. U.S.A. 96, 11008-11014
3. Xia, K., Zhang, S., Solina, B. A., Barquera, B., and Colon, W. (2010) Do prokaryotes have more kinetically stable proteins than eukaryotic organisms? Biochemistry 49, 7239-7241
4. Machius, M., Declerck, N., Huber, R., and Wiegand, G. (2003) Kinetic stabilization of Bacillus licheniformis α-amylase through introduction of hydrophobic residues at the surface J. Biol. Chem. 278, 11546-11553
5. Mansfeld, J., Vriend, G., Dijkstra, B. W., Veltman, O. R., Van den Burg, B., Venema, G., Ulbrich-Hofmann, R., and Eijsink, V. G. (1997) Extreme stabilization of a thermolysin-like protease by an engineered disulfide bond J. Biol. Chem. 272, 11152-11156
6. Pozdnyakova, I., Guidry, J., and Wittung-Stafshede, P. (2001) Copper stabilizes azurin by decreasing the unfolding rate Arch. Biochem. Biophys. 390, 146-148
7. Rodriguez-Larrea, D., Minning, S., Borchert, T. V., and Sanchez-Ruiz, J. M. (2006) Role of solvation barriers in protein kinetic stability J. Mol. Biol. 360, 715-724
8. Houry, W. A., Frishman, D., Eckerskorn, C., Lottspeich, F., and Hartl, F. U. (1999) Identification of in vivo substrates of the chaperonin GroEL Nature 402, 147-154
9. Solis-Mendiola, S., Gutierrez-Gonzalez, L. H., Arroyo-Reyna, A., Padilla-Zuniga, J., Rojo-Dominguez, A., and Hernandez-Arana, A. (1998) pH dependence of the activation parameters for chymopapain unfolding: Influence of ion pairs on the kinetic stability of proteins Biochim. Biophys. Acta 1388, 363-372
10. Jaenicke, R. and Bohm, G. (1998) The stability of proteins in extreme environments Curr. Opin. Struct. Biol. 8, 738-748
11. Manning, M. and Colon, W. (2004) Structural basis of protein kinetic stability: Resistance to sodium dodecyl sulfate suggests a central role for rigidity and a bias toward β-sheet structure Biochemistry 43, 11248-11254
12. Jirgensons, B. (1961) Effect of detergents on the conformation of proteins. I. An abnormal increase of the optical rotatory dispersion constant Arch. Biochem. Biophys. 94, 59-67
13. Otzen, D. E. and Oliveberg, M. (2002) Conformational plasticity in folding of the split β-α-β protein S6: Evidence for burst-phase disruption of the native state J. Mol. Biol. 317, 613-627
14. Xia, K., Manning, M., Hesham, H., Lin, Q., Bystroff, C., and Colon, W. (2007) Identifying the subproteome of kinetically stable proteins via diagonal 2D SDS/PAGE Proc. Natl. Acad. Sci. U.S.A. 104, 17329-17334
15. Kelch, B. A. and Agard, D. A. (2007) Mesophile versus thermophile: Insights into the structural mechanisms of kinetic stability J. Mol. Biol. 370, 784-795
16. Nielsen, M. M., Andersen, K. K., Westh, P., and Otzen, D. E. (2007) Unfolding of β-sheet proteins in SDS Biophys. J. 92, 3674-3685
17. Otzen, D. E. (2002) Protein unfolding in detergents: Effect of micelle structure, ionic strength, pH, and temperature Biophys. J. 83, 2219-2230
18. Andersen, K. K., Westh, P., and Otzen, D. E. (2008) Global study of myoglobin-surfactant interactions Langmuir 24, 399-407
19. Mogensen, J. E., Sehgal, P., and Otzen, D. E. (2005) Activation, inhibition, and destabilization of Thermomyces lanuginosus lipase by detergents Biochemistry 44, 1719-1730
20. Kalyanasundaram, K. and Thomas, J. K. (1977) Environmental effects on vibronic band intensities in pyrene monomer fluorescence and their application in studies of micellar systems J. Am. Chem. Soc. 99, 2039-2044
21. Derewenda, U., Swenson, L., Wei, Y., Green, R., Kobos, P. M., Joerger, R., Haas, M. J., and Derewenda, Z. S. (1994) Conformational lability of lipases observed in the absence of an oil-water interface: Crystallographic studies of enzymes from the fungi Humicola lanuginosa and Rhizopus delemar J. Lipid Res. 35, 524-534
22. Dolinsky, T. J., Nielsen, J. E., McCammon, J. A., and Baker, N. A. (2004) PDB2PQR: An automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations Nucleic Acids Res. 32, W665-W667
23. Dolinsky, T. J., Czodrowski, P., Li, H., Nielsen, J. E., Jensen, J. H., Klebe, G., and Baker, N. A. (2007) PDB2PQR: Expanding and upgrading automated preparation of biomolecular structures for molecular simulations Nucleic Acids Res. 35, W522-W525
24. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Electrostatics of nanosystems: Application to microtubules and the ribosome Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041
25. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.
26. Mogensen, J. E., Sehgal, P., and Otzen, D. E. (2005) Activation, inhibition and destabilization of Thermomyces lanuginosus lipase by detergents Biochemistry 44, 1719-1730
27. Otzen, D. E. (2003) Folding of DsbB in mixed micelles: A kinetic analysis of the stability of a bacterial membrane protein J. Mol. Biol. 330, 641-649
28. Nielsen, A. D., Arleth, L., and Westh, P. (2005) Analysis of protein-surfactant interactions: A titration calorimetric and fluorescence spectroscopic investigation of interactions between Humicola insolens cutinase and an anionic surfactant Biochim. Biophys. Acta 1752, 124-132
29. Andersen, K. K., Oliveira, C. L. P., Larsen, K. L., Poulsen, F. M., Callisen, T. H., Westh, P., Pedersen, J. S., and Otzen, D. E. (2009) The role of decorated SDS micelles in sub-cmc protein denaturation and association J. Mol. Biol. 391, 207-226
30. Nielsen, M. M., Andersen, K. K., Westh, P., and Otzen, D. E. (2007) Unfolding of β-sheet proteins in SDS Biophys. J. 92, 3674-3685
31. Andersen, K., Westh, P., and Otzen, D. E. (2008) Global study of myoglobin-surfactant interactions Langmuir 24, 399-407
32. Otzen, D. E., Sehgal, P., and Westh, P. (2009) α-Lactalbumin is unfolded by all classes of detergents but with different mechanisms J. Colloid Interface Sci. 329, 273-283
33. Pitt-Rivers, R. and Impiombato, F. S. (1968) The binding of sodium dodecyl sulphate to various proteins Biochem. J. 109, 825-830
34. Liu, Y. and Guo, R. (2007) Interaction between casein and sodium dodecyl sulfate J. Colloid Interface Sci. 315, 685-692
35. Tanford, C. (1970) Protein denaturation. Part C. Theoretical models for the mechanism of denaturation Adv. Protein Chem. 24, 1-95
36. p-values in protein folding Protein Sci. 13, 3253-3263
37. Hammarstrom, P., Wiseman, R. L., Powers, E. T., and Kelly, J. W. (2003) Prevention of transthyretin amyloid disease by changing protein misfolding energetics Science 299, 713-716
38. Petrassi, H. M., Johnson, S. M., Purkey, H. E., Chiang, K. P., Walkup, T., Jiang, X., Powers, E. T., and Kelly, J. W. (2005) Potent and selective structure-based dibenzofuran inhibitors of transthyretin amyloidogenesis: Kinetic stabilization of the native state J. Am. Chem. Soc. 127, 6662-6671
39. Wiseman, R. L., Johnson, S. M., Kelker, M. S., Foss, T., Wilson, I. A., and Kelly, J. W. (2005) Kinetic stabilization of an oligomeric protein by a single ligand binding event J. Am. Chem. Soc. 127, 5540-5551
40. Jaswal, S. S., Sohl, J. L., Davis, J. H., and Agard, D. A. (2002) Energetic landscape of α-lytic protease optimizes longevity through kinetic stability Nature 415, 343-346
41. Sehgal, P., Bang Nielsen, S., Pedersen, S., Wimmer, R., and Otzen, D. E. (2007) Modulation of cutinase stability and structure by phospholipid detergents Biochim. Biophys. Acta 1774, 1544-1554
42. Costas, M., Rodriguez-Larrea, D., De Maria, L., Borchert, T. V., Gomez-Puyou, A., and Sanchez-Ruiz, J. M. (2009) Between-species variation in the kinetic stability of TIM proteins linked to solvation-barrier free energies J. Mol. Biol. 385, 924-937
43. Halskau, O., Jr., Perez-Jimenez, R., Ibarra-Molero, B., Underhaug, J., Munoz, V., Martinez, A., and Sanchez-Ruiz, J. M. (2008) Large-scale modulation of thermodynamic protein folding barriers linked to electrostatics Proc. Natl. Acad. Sci. U.S.A. 105, 8625-8630
44. Zarrine-Afsar, A., Zhang, Z., Schweiker, K. L., Makhatadze, G. I., Davidson, A. R., and Chan, H. S. (2012) Kinetic consequences of native state optimization of surface-exposed electrostatic interactions in the Fyn SH3 domain Proteins 80, 858-870
45. Mogensen, J. E., Ibsen, H., Lund, J., and Otzen, D. E. (2004) Elimination of an off-pathway folding intermediate by a single point mutation Biochemistry 43, 3357-3367