In vitro evolved non-aggregating and thermostable lipase: Structural and thermodynamic investigation

Journal of Molecular Biology

Volumn 413, Issue 3, 2011, Pages 726-741

  Kamal, Md Zahid ^a   Ahmad, Shoeb ^a   Molugu, Trivikram Rao ^a   Vijayalakshmi, Amash ^a   Deshmukh, Mandar V ^a   Sankaranarayanan, Rajan ^a   Rao, Nalam Madhusudhana ^a  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

Author keywords

aggregation prone intermediate; differential scanning calorimetry; NMR; thermal unfolding; X ray crystallography

Indexed keywords

TRIACYLGLYCEROL LIPASE;

AMINO ACID SEQUENCE; ARTICLE; BACILLUS SUBTILIS; CONTROLLED STUDY; DIFFERENTIAL SCANNING CALORIMETRY; GENE MUTATION; HYDROPHOBICITY; IN VITRO STUDY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN UNFOLDING; STRUCTURE ANALYSIS; THERMODYNAMICS; THERMOSTABILITY; WILD TYPE; X RAY CRYSTALLOGRAPHY;

BACILLUS SUBTILIS;

EID: 80054692390     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.09.002     Document Type: Article

References (62)

1. Fink A.L. Protein aggregation: folding aggregates, inclusion bodies and amyloid Folding Des. 3 1998 R9 R23
2. Khurana R., Gillespie J.R., Talapatra A., Minert L.J., Ionescu-Zanetti C., Millett I., and Fink A.L. Partially folded intermediates as critical precursors of light chain amyloid fibrils and amorphous aggregates Biochemistry 40 2001 3525 3535 (Pubitemid 32242809)
3. Horwich A. Protein aggregation in disease: a role for folding intermediates forming specific multimeric interactions J. Clin. Invest. 110 2002 1221 1232 (Pubitemid 35285746)
4. Bondos S.E., and Bicknell A. Detection and prevention of protein aggregation before, during, and after purification Anal. Biochem. 316 2003 223 231 (Pubitemid 36444552)
5. Roodveldt C., Aharoni A., and Tawfik D.S. Directed evolution of proteins for heterologous expression and stability Curr. Opin. Struct. Biol. 15 2005 50 56 (Pubitemid 40249509)
6. Lawrence M.S., Phillips K.J., and Liu D.R. Supercharging proteins can impart unusual resilience J. Am. Chem. Soc. 129 2007 10110 10112 (Pubitemid 47312950)
7. Elcock A.H., and McCammon J.A. Electrostatic contributions to the stability of halophilic proteins J. Mol. Biol. 280 1998 731 748 (Pubitemid 28336377)
8. Jackel C., Kast P., and Hilvert D. Protein design by directed evolution Annu. Rev. Biophys. 37 2008 153 173
9. Eijsink V.G., Gaseidnes S., Borchert T.V., and van den Burg B.B. Directed evolution of enzyme stability Biomol. Eng. 22 2005 21 30 (Pubitemid 40602590)
10. Jespers L., Schon O., Famm K., and Winter G. Aggregation-resistant domain antibodies selected on phage by heat denaturation Nat. Biotechnol. 22 2004 1161 1165 (Pubitemid 39166856)
11. Famm K., Hansen L., Christ D., and Winter G. Thermodynamically stable aggregation-resistant antibody domains through directed evolution J. Mol. Biol. 376 2008 926 931
12. Acharya P., Rajakumara E., Sankaranarayanan R., and Rao N.M. Structural basis of selection and thermostability of laboratory evolved Bacillus subtilis lipase J. Mol. Biol. 341 2004 1271 1281 (Pubitemid 39092314)
13. Ahmad S., Kamal M.Z., Sankaranarayanan R., and Rao N.M. Thermostable Bacillus subtilis lipases: in vitro evolution and structural insight J. Mol. Biol. 381 2008 324 340
14. Kamal M.Z., Ahmad S., Yedavalli P., and Rao N.M. Stability curves of laboratory evolved thermostable mutants of a Bacillus subtilis lipase Biochim. Biophys. Acta 1804 2010 1850 1856
15. Ahmad S., and Rao N.M. Thermally denatured state determines refolding in lipase: mutational analysis Protein Sci. 18 2009 1183 1196
16. Pace C.N., Shirley B.A., and Thompson J.A. Mechanism of protein folding E.D. Creighton, Protein Structure: A Practical Approach 1998 Oxford Press Oxford, UK 311 330
17. Vieille C., and Zeikus G.J. Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability Microbiol. Mol. Biol. Rev. 65 2001 1 43 (Pubitemid 32204286)
18. van Pouderoyen G., Eggert T., Jaeger K.E., and Dijkstra B.W. The crystal structure of Bacillus subtilis lipase: a minimal α/β hydrolase fold enzyme J. Mol. Biol. 309 2001 215 226 (Pubitemid 32553519)
19. Evans S.V. SETOR: hardware-lighted three-dimensional solid model representations of macromolecules J. Mol. Graphics 11 1993 134 138
20. Hardy F., Vriend G., Veltman O.R., van der Vinne B., Venema G., and Eijsink V.G. Stabilization of Bacillus stearothermophilus neutral protease by introduction of prolines FEBS Lett. 317 1993 89 92 (Pubitemid 23043945)
21. Watanabe K., Masuda T., Ohashi H., Mihara H., and Suzuki Y. Multiple proline substitutions cumulatively thermostabilize Bacillus cereus ATCC7064 oligo-1,6-glucosidase. Irrefragable proof supporting the proline rule Eur. J. Biochem. 226 1994 277 283 (Pubitemid 24379045)
22. Gaseidnes S., Synstad B., Jia X., Kjellesvik H., Vriend G., and Eijsink V.G. Stabilization of a chitinase from Serratia marcescens by Gly → Ala and Xxx → Pro mutations Protein Eng. 16 2003 841 846 (Pubitemid 37517388)
23. Richardson J.S., and Richardson D.C. Amino acid preferences for specific locations at the ends of alpha helices Science 240 1988 1648 1652
24. Watanabe K., Hata Y., Kizaki H., Katsube Y., and Suzuki Y. The refined crystal structure of Bacillus cereus oligo-1,6-glucosidase at 2.0 Å resolution: structural characterization of proline-substitution sites for protein thermostabilization J. Mol. Biol. 269 1997 142 153 (Pubitemid 27243627)
25. Takano K., Higashi R., Okada J., Mukaiyama A., Tadokoro T., Koga Y., and Kanaya S. Proline effect on the thermostability and slow unfolding of a hyperthermophilic protein J. Biochem. 145 2009 79 85
26. Lijnzaad P., Berendsen H.J.C., and Argos P. A method for detecting hydrophobic patches protein Proteins: Struct., Funct., Genet. 26 1996 192 203 (Pubitemid 26365313)
27. Tsodikov O.V., Record M.T., and Sergeev Y.V. Novel computer program for fast exact calculation of accessible and molecular surface areas and average surface curvature J. Comput. Chem. 23 2002 600 609 (Pubitemid 34312083)
28. Eisenhaber F., and Argos P. Hydrophobic regions on protein surfaces: definition based on hydration shell structure and a quick method for their computation Protein Eng. 9 1996 1121 1133
29. Schmid F.X. Prolyl isomerase: enzymatic catalysis of slow protein-folding reactions Annu. Rev. Biophys. Biomol. Struct. 22 1993 123 142
30. Williams A.D., Portelius E., Kheterpal I., Guo J.T., Cook K.D., Xu Y., and Wetzel R. Mapping Aβ amyloid fibril secondary structure using scanning proline mutagenesis J. Mol. Biol. 335 2004 833 842 (Pubitemid 38352823)
31. 20-29 Biochemistry 38 1999 1811 1818
32. Conchillo-Sole O., de Groot N.S., Aviles F.X., Vendrell J., Daura X., and Ventura S. AGGRESCAN: a server for the prediction and evaluation of "hot spots" of aggregation in polypeptides BMC Bioinformatics 8 2007 65
33. Pawar A.P., Dubay K.F., Zurdo J., Chiti F., Vendruscolo M., and Dobson C.M. Prediction of "aggregation-prone" and "aggregation- susceptible" regions in proteins associated with neurodegenerative diseases J. Mol. Biol. 350 2005 379 392 (Pubitemid 40805470)
34. Cole R., and Loria J.P. FAST-Modelfree: a program for rapid automated analysis of solution NMR spin-relaxation data J. Biomol. NMR 26 2003 203 213 (Pubitemid 36758441)
35. α nuclear spin relaxation J. Biomol. NMR 9 1997 287 298 (Pubitemid 127505389)
36. Palmer A.G. III Inertia and Diffusion Tensors 2003 Columbia University New York, NY
37. Lee D., Hilty C., Wider G., and Wuthrich K. Effective rotational correlation times of proteins from NMR relaxation interference J. Magn. Reson. 178 2006 72 76 (Pubitemid 41774013)
38. Henzler-Wildman K.A., Lei M., Thai V., Kerns S.J., Karplus M., and Kern D. A hierarchy of timescales in protein dynamics is linked to enzyme catalysis Nature 450 2007 913 916 (Pubitemid 350231333)
39. Zscherp C., Aygun H., Engels J.W., and Mantele W. Effect of proline to alanine mutation on the thermal stability of the all-β-sheet protein tendamistat Biochim. Biophys. Acta 1651 2003 139 145 (Pubitemid 38234561)
40. Karlsson M., Martensson L.G., Olofsson P., and Carlsson U. Circumnavigating misfolding traps in the energy landscape through protein engineering: suppression of molten globule and aggregation in carbonic anhydrase Biochemistry 43 2004 6803 6807 (Pubitemid 38697579)
41. Durrschmidt P., Mansfeld J., and Ulbrich-Hofmann R. An engineered disulfide bridge mimics the effect of calcium to protect neutral protease against local unfolding FEBS J. 272 2005 1523 1534 (Pubitemid 40444940)
42. Singh S.M., Cabello-Villegas J., Hutchings R.L., and Mallela K.M. Role of partial protein unfolding in alcohol-induced protein aggregation Proteins 78 2010 2625 2637
43. Bemporad F., Vannocci T., Varela L., Azuaga A.I., and Chiti F. A model for the aggregation of the acylphosphatase from Sulfolobus solfataricus in its native-like state Biochim. Biophys. Acta 1784 2008 1986 1996
44. Chiti F., and Dobson C.M. Amyloid formation by globular proteins under native conditions Nat. Chem. Biol. 5 2009 15 22
45. Chiti F., Stefani M., Taddei N., Ramponi G., and Dobson C.M. Rationalization of the effects of mutations on peptide and protein aggregation rates Nature 424 2003 805 808 (Pubitemid 37021713)
46. Chiti F., and Dobson C.M. Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75 2006 333 366 (Pubitemid 44118036)
47. Markwell M.A., Hass S.M., Tolbert N.E., and Bieber L.L. Protein determination in membrane and lipoprotein samples: manual and automated procedures Methods Enzymol. 72 1981 296 303
48. Walter T.S., Mancini E.J., Kadlec J., Graham S.C., Assenberg R., and Ren J. Semi-automated microseeding of nanolitre crystallization experiments Acta Crystallogr., Sect. F: Struct. Biol. Cryst. Commun. 64 2008 14 18
49. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode Macromol. Crystallogr., Part A, 1997 276 1997 307 326 (Pubitemid 27085611)
50. Vagin A., and Teplyakov A. MOLREP: an automated program for molecular replacement J. Appl. Crystallogr. 30 1997 1022 1025 (Pubitemid 127485985)
51. Bailey S. The CCP4 suite: programs for protein crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 1994 760 763
52. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., and Grosse-Kunstleve R.W. Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallogr., Sect. D: Biol. Crystallogr. 54 1998 905 921
53. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models Acta Crystallogr., Sect. A: Found. Crystallogr. 47 1991 110 119
54. Marley J., Lu M., and Bracken C. A method for efficient isotopic labeling of recombinant proteins J. Biomol. NMR 20 2001 71 75 (Pubitemid 32519656)
55. Cavanagh J., Fairbrother W.J., Palmer A.G., Rance M., and Skelton N.J. Protein NMR Spectroscopy 2007 Academic Press New York, NY
56. Keller R., and Wuthrich K. Computer-Aided Resonance Assignment (CARA) 2004 Verlag Goldau Cantina, Switzerland
57. Goddard T.D., and Kneller D.G. Sparky 3.112 2004 University of California San Francisco, CA
58. d'Auvergne E.J., and Gooley P.R. Optimisation of NMR dynamic models. I. Minimisation algorithms and their performance within the model-free and Brownian rotational diffusion spaces J. Biomol. NMR 40 2008 107 119
59. d'Auvergne E.J., and Gooley P.R. Optimisation of NMR dynamic models. II. A new methodology for the dual optimisation of the model-free parameters and the Brownian rotational diffusion tensor J. Biomol. NMR 40 2008 121 133
60. Palmer A.G. III Modelfree 4.1 2000 Columbia University New York, NY http://biochemistry.hs.columbia.edu/labs/palmer/software/modelfree.html
61. Mandel A.M., Akke M., and Palmer A.G. Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme J. Mol. Biol. 246 1995 144 163
62. de la Torre J.G., Huertas M.L., and Carrasco B. HYDRONMR: prediction of NMR relaxation of globular proteins from atomic-level structures and hydrodynamic calculations J. Magn. Reson. 147 2000 138 146