Crystal structure and thermodynamic and kinetic stability of metagenome-derived LC-cutinase

Biochemistry

Volumn 53, Issue 11, 2014, Pages 1858-1869

  Sulaiman, Sintawee ^a   You, Dong Ju ^a,b   Kanaya, Eiko ^a   Koga, Yuichi ^a   Kanaya, Shigenori ^a  

^a OSAKA UNIVERSITY   (Japan)

^b Korea Basic Science Institute (KBSI)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCULAR DICHROISM SPECTROSCOPY; COVALENT BONDS; DENATURATION;

CONFORMATIONAL CHANGE; DEGRADING ACTIVITIES; GUANIDINE HYDROCHLORIDE; OPTIMAL TEMPERATURE; POLYETHYLENE GLYCOL (PEG); POLYETHYLENE TEREPHTHALATES (PET); THERMAL DENATURATION STUDIES; THERMAL DENATURATIONS;

KINETICS;

CUTINASE; GUANIDINE; LC CUTINASE; MACROGOL; POLYETHYLENE TEREPHTHALATE; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CRYSTALLIZATION; DENATURATION; DISSOCIATION CONSTANT; DISULFIDE BOND; ENZYME STABILITY; METAGENOME; NONHUMAN; NUCLEOPHILICITY; PH; PRIORITY JOURNAL; PROTEIN UNFOLDING; TEMPERATURE DEPENDENCE; THERMOBIFIDA ALBA; THERMOSTABILITY;

BINDING SITES; CARBOXYLIC ESTER HYDROLASES; CRYSTALLOGRAPHY, X-RAY; ENZYME STABILITY; KINETICS; METAGENOME; POLYETHYLENE TEREPHTHALATES; PROTEIN DENATURATION; STREPTOMYCES; THERMODYNAMICS;

EID: 84897051705     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi401561p     Document Type: Article

References (56)

1. Purdy, R. E. and Kolattukudy, P. E. (1975) Hydrolysis of plant cuticle by plant pathogens. Purification, amino acid composition, and molecular weight of two isozymes of cutinase and a nonspecific esterase from Fusarium solani f. pisi Biochemistry 14, 2824-2831
2. Carvalho, C. M. L., Aires-Barros, M. R., and Cabral, J. M. S. (1998) Cutinase structure, function and biocatalytic applications Electron. J. Biotechnol. 1, 160-173
3. Longhi, S. and Cambillau, C. (1999) Structure-activity of cutinase, a small lipolytic enzyme Biochim. Biophys. Acta 1441, 185-196
4. Dutta, K., Sen, S., and Veeranki, V. D. (2009) Production, characterization and applications of microbial cutinases Process Biochem. 44, 127-134
5. Chen, S., Su, L., Chen, J., and Wu, J. (2013) Cutinase: Characteristics, preparation, and application Biotechnol. Adv. 31, 1754-1767
6. Nyon, M. P., Rice, D. W., Berrisford, J. M., Hounslow, A. M., Moir, A. J. G., Huang, H., Nathan, S., Mahadi, N. M., Bakar, F. D. A., and Craven, C. J. (2009) Catalysis by Glomerella cingulata cutinase requires conformational cycling between the active and inactive states of its catalytic triad J. Mol. Biol. 385, 226-235
7. Liu, Z., Gosser, Y., Baker, P. J., Ravee, Y., Lu, Z., Alemu, G., Li, H., Butterfoss, G. L., Kong, X.-P., Gross, R., and Montclare, J. K. (2009) Structural and functional studies of Aspergillus oryzae cutinase: Enhanced thermostability and hydrolytic activity of synthetic ester and polyester degradation J. Am. Chem. Soc. 131, 15711-15716
8. Fernandes, A. T., Pereira, M. M., Silva, C. S., Lindley, P. F., Bento, I., Melo, E. P., and Martins, L. O. (2011) The removal of a disulfide bridge in CotA-laccase changes the slower motion dynamics involved in copper binding but has no effect on the thermodynamic stability JBIC, J. Biol. Inorg. Chem. 16, 641-651
9. Kodama, Y., Masaki, K., Kondo, H., Suzuki, M., Tsuda, S., Nagura, T., Shimba, N., Suzuki, E., and Iefuji, H. (2009) Crystal structure and enhanced activity of a cutinase-like enzyme from Cryptococcus sp. strain S-2 Proteins 77, 710-717
10. Pio, T. F. and Macedo, G. A. (2009) Cutinases: Properties and industrial applications Adv. Appl. Microbiol. 66, 77-95
11. Araújo, R., Silva, C., O'Neill, A., Micaelo, N., Guebitz, G., Soares, C. M., Casal, M., and Cavaco-Paulo, A. (2007) Tailoring cutinase activity towards polyethylene terephthalate and polyamide 6,6 fibers J. Biotechnol. 128, 849-857
12. Silva, C., Da, S., Silva, N., Matamá, T., Araújo, R., Martins, M., Chen, S., Chen, J., Wu, J., Casal, M., and Cavaco-Paulo, A. (2011) Engineered Thermobifida fusca cutinase with increased activity on polyester substrates Biotechnol. J. 6, 1230-1239
13. Thumarat, U., Nakamura, R., Kawabata, T., Suzuki, H., and Kawai, F. (2012) Biochemical and genetic analysis of a cutinase-type polyesterase from a thermophilic Thermobifida alba AHK119 Appl. Microbiol. Biotechnol. 95, 419-340
14. Herrero Acero, E., Ribitsch, D., Dellacher, A., Zitzenbacher, S., Marold, A., Steinkellner, G., Gruber, K., Schwab, H., and Guebitz, G. M. (2013) Surface engineering of a cutinase from Thermobifida cellulosilytica for improved polyester hydrolysis Biotechnol. Bioeng. 110, 2581-2590
15. Zhang, Y., Wang, L., Chen, J., and Wu, J. (2013) Enhanced activity toward PET by site-directed mutagenesis of Thermobifida fusca cutinase-CBM fusion protein Carbohydr. Polym. 97, 124-129
16. Ribitsch, D., Yebra, A. O., Zitzenbacher, S., Wu, J., Nowitsch, S., Steinkellner, G., Greimel, K., Doliska, A., Oberdorfer, G., Gruber, C. C., Gruber, K., Schwab, H., Stana-Kleinschek, K., Acero, E. H., and Guebitz, G. M. (2013) Fusion of binding domains to Thermobifida cellulosilytica cutinase to tune sorption characteristics and enhancing PET hydrolysis Biomacromolecules 14, 1769-1776
17. Sulaiman, S., Yamato, S., Kanaya, E., Kim, J.-J., Koga, Y., Takano, K., and Kanaya, S. (2012) Isolation of a novel cutinase homolog with polyethylene terephthalate-degrading activity from leaf-branch compost by using a metagenomic approach Appl. Environ. Microbiol. 78, 1556-1562
18. Ternström, T., Svendsen, A., Akke, M., and Adlercreutz, P. (2005) Unfolding and inactivation of cutinases by AOT and guanidine hydrochloride Biochim. Biophys. Acta 1748, 74-83
19. Goodwin, T. W. and Morton, R. A. (1946) The spectrophotometric determination of tyrosine and tryptophan in proteins Biochem. J. 40, 628-632
20. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326
21. Vagin, A. and Teplyakov, A. (1997) MOLREP: An Automated Program for Molecular Replacement J. Appl. Crystallogr. 30, 1022-1025
22. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: Programs for protein crystallography Acta Crystallogr. D50, 760-763
23. Langer, G., Cohen, S. X., Lamzin, V. S., and Perrakis, A. (2008) Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7 Nat. Protoc. 3, 1171-1179
24. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D53, 240-255
25. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132
26. Mukaiyama, A., Takano, K., Haruki, M., Morikawa, M., and Kanaya, S. (2004) Kinetically robust monomeric protein from a hyperthermophile Biochemistry 43, 13859-13866
27. Pace, C. N. (1990) Measuring and increasing protein stability Trends Biotechnol. 8, 93-98
28. Kitadokoro, K., Thumarat, U., Nakamura, R., Nishimura, K., Karatani, H., Suzuki, H., and Kawai, F. (2012) Crystal structure of cutinase Est119 from Thermobifida alba AHK119 that can degrade modified polyethylene terephthalate at 1.76 Å resolution Polym. Degrad. Stab. 97, 771-775
29. Wei, Y., Swenson, L., Castro, C., Derewenda, U., Minor, W., Arai, H., Aoki, J., Inoue, K., Servin-Gonzalez, L., and Derewenda, Z. S. (1998) Structure of a microbial homologue of mammalian platelet-activating factor acetylhydrolases: Streptomyces exfoliatus lipase at 1.9 Å resolution Structure 6, 511-519
30. Ollis, D. L., Cheah, E., Cygler, M., Dijkstra, B., Frolow, F., Franken, S. M., Harel, M., Remington, S. J., Silman, I., and Schrag, J. (1992) The α /β hydrolase fold Protein Eng. 5, 197-211
31. Kawai, F., Thumarat, U., Kitadokoro, K., Waku, T., Tada, T., Tanaka, N., and Kawabata, T. (2013) Comparison of polyester-degrading cutinases from genus Thermobifida. In Green Polymer Chemistry: Biocatalysis and Materials II (Cheng, H. N., Gross, R. A., and Smith, P. B., Eds.) pp 111-120, ACS Symposium Series 1144, American Chemical Society, Washington, DC.
32. Zielenkiewicz, W., Swierzewski, R., Attanasio, F., and Rialdi, G. (2006) Thermochemical, volumetric and spectroscopic properties of lysozyme- poly(ethylene) glycol system J. Therm. Anal. Calorim. 83, 587-595
33. Fletcher, J. E., Spector, A. A., and Ashbrook, J. D. (1970) Analysis of macromolecule-ligand binding by determination of stepwise equilibrium constants Biochemistry 9, 4580-4587
34. Okada, J., Okamoto, T., Mukaiyama, A., Tadokoro, T., You, D.-J., Chon, H., Koga, Y., Takano, K., and Kanaya, S. (2010) Evolution and thermodynamics of the slow unfolding of hyperstable monomeric proteins BMC Evol. Biol. 10, 207
35. Hu, X., Thumarat, U., Zhang, X., Tang, M., and Kawai, F. (2010) Diversity of polyester-degrading bacteria in compost and molecular analysis of a thermoactive esterase from Thermobifida alba AHK119 Appl. Microbiol. Biotechnol. 87, 771-779
36. Ribitsch, D., Acero, E. H., Greimel, K., Eiteljoerg, I., Trotscha, E., Freddi, G., Schwab, H., and Guebitz, G. M. (2012) Characterization of a new cutinase from Thermobifida alba for PET-surface hydrolysis Biocatal. Biotransform. 30, 2-9
37. Herrero Acero, E., Ribitsch, D., Steinkellner, G., Gruber, K., Greimel, K., Eiteljoerg, I., Trotscha, E., Wei, R., Zimmermann, W., Zinn, M., Cavaco-Paulo, A., Freddi, G., Schwab, H., and Guebitz, G. (2011) Enzymatic Surface Hydrolysis of PET: Effect of Structural Diversity on Kinetic Properties of Cutinases from Thermobifida Macromolecules 44, 4632-4640
38. Chen, S., Su, L., Billig, S., Zimmermann, W., Chen, J., and Wu, J. (2010) Biochemical characterization of the cutinases from Thermobifida fusca J. Mol. Catal. B: Enzym. 63, 121-127
39. Pace, C. N., Grimsley, G. R., Thomson, J. A., and Barnett, B. J. (1988) Conformational stability and activity of ribonuclease T1 with zero, one, and two intact disulfide bonds J. Biol. Chem. 263, 11820-11825
40. Piatek, R., Bruździak, P., Wojciechowski, M., Zalewska-Piatek, B., and Kur, J. (2010) The noncanonical disulfide bond as the important stabilizing element of the immunoglobulin fold of the Dr fimbrial DraE subunit Biochemistry 49, 1460-1468
41. Schulenburg, C., Weininger, U., Neumann, P., Meiselbach, H., Stubbs, M. T., Sticht, H., Balbach, J., Ulbrich-Hofmann, R., and Arnold, U. (2010) Impact of the C-terminal disulfide bond on the folding and stability of onconase ChemBioChem 11, 978-986
42. Mason, J. M., Bendall, D. S., Howe, C. J., and Worrall, J. A. R. (2012) The role of a disulfide bridge in the stability and folding kinetics of Arabidopsis thaliana cytochrome c6A Biochim. Biophys. Acta 1824, 311-318
43. Matsumura, M., Becktel, W. J., Levitt, M., and Matthews, B. W. (1989) Stabilization of phage T4 lysozyme by engineered disulfide bonds Proc. Natl. Acad. Sci. U.S.A. 86, 6562-6566
44. Kanaya, S., Katsuda-Nakai, C., and Ikehara, M. (1991) Importance of the positive charge cluster in Escherichia coli ribonuclease HI for the effective binding of the substrate J. Biol. Chem. 266, 11621-11627
45. Boone, C. D., Habibzadegan, A., Tu, C., Silverman, D. N., and McKenna, R. (2013) Structural and catalytic characterization of a thermally stable and acid-stable variant of human carbonic anhydrase II containing an engineered disulfide bond Acta Crystallogr. D69, 1414-1422
46. Vinther, T. N., Norrman, M., Ribel, U., Huus, K., Schlein, M., Steensgaard, D. B., Pedersen, T. Å., Pettersson, I., Ludvigsen, S., Kjeldsen, T., Jensen, K. J., and Hubálek, F. (2013) Insulin analog with additional disulfide bond has increased stability and preserved activity Protein Sci. 22, 296-305
47. Wozniak-Knopp, G. and Rüker, F. (2012) A C-terminal interdomain disulfide bond significantly stabilizes the Fc fragment of IgG Arch. Biochem. Biophys. 526, 181-187
48. Schmidt, B., Ho, L., and Hogg, P. J. (2006) Allosteric disulfide bonds Biochemistry 45, 7429-7433
49. H3 domain Protein Sci. 17, 95-106
50. Giver, L., Gershenson, A., Freskgard, P.-O., and Arnold, F. H. (1998) Directed evolution of a thermostable esterase Proc. Natl. Acad. Sci. U.S.A. 95, 12809-12813
51. Karshikoff, A. and Ladenstein, R. (2001) Ion pairs and the thermotolerance of proteins from hyperthermophiles: A "traffic rule" for hot roads Trends Biochem. Sci. 26, 550-556
52. Nguyen, T.-N., Angkawidjaja, C., Kanaya, E., Koga, Y., Takano, K., and Kanaya, S. (2012) Activity, stability, and structure of metagenome-derived LC11-RNase H1, a homolog of Sulfolobus tokodaii RNase H1 Protein Sci. 21, 553-561
53. You, D.-J., Chon, H., Koga, Y., Takano, K., and Kanaya, S. (2007) Crystal structure of type 1 ribonuclease H from hyperthermophilic archaeon Sulfolobus tokodaii: Role of arginine 118 and C-terminal anchoring Biochemistry 46, 11494-11503
54. Pace, C. N., Fu, H., Fryar, K. L., Landua, J., Trevino, S. R., Shirley, B. A., Hendricks, M. M., Iimura, S., Gajiwala, K., Scholtz, J. M., and Grimsley, G. R. (2011) Contribution of hydrophobic interactions to protein stability J. Mol. Biol. 408, 514-528
55. Watanabe, K., Chishiro, K., Kitamura, K., and Suzuki, Y. (1991) Proline residues responsible for thermostability occur with high frequency in the loop regions of an extremely thermostable oligo-1,6-glucosidase from Bacillus thermoglucosidasius KP1006 J. Biol. Chem. 266, 24287-24294
56. Boutz, D. R., Cascio, D., Whitelegge, J., Perry, L. J., and Yeates, T. O. (2007) Discovery of a thermophilic protein complex stabilized by topologically interlinked chains J. Mol. Biol. 368, 1332-1344 Technology