Thermodynamics and structure of a salmon cold active goose-type lysozyme

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 156, Issue 4, 2010, Pages 254-263

  Kyomuhendo, Peter ^a,b   Myrnes, Bjørnar ^a   Brandsdal, Bjørn Olav ^b   Smalås, Arne O ^b   Nilsen, Inge W ^b   Helland, Ronny ^b  

^a NOFIMA   (Norway)

^b UNIVERSITY OF TROMSØ   (Norway)

Author keywords

Differential scanning calorimetry; Goose type; Innate immunity; Lysozyme; Protein; Refolding; Salmon; Thermal tolerance; X ray crystallography

Indexed keywords

LYSOZYME; SALMON GOOSE TYPE LYSOZYME; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DIFFERENTIAL SCANNING CALORIMETRY; DISULFIDE BOND; ENZYME STRUCTURE; MELTING POINT; PRECIPITATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RENATURATION; TEMPERATURE ACCLIMATIZATION; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

ANSER; SALMO SALAR;

EID: 77954865677     PISSN: 10964959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpb.2010.04.002     Document Type: Article

References (65)

1. Arnold K., Bordoli L., Kopp J., Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 2006, 22:195-201.
2. Betz S.F. Disulfide bonds and the stability of globular proteins. Protein Sci. 1993, 2:1551-1558.
3. Collaborative Computational Project N. The CCP4 Suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol Crystallogr. 1994, 50:760-763.
4. Cooper A., Eyles S.J., Radford S.E., Dobson C.M. Thermodynamic consequences of the removal of a disulfide bridge from hen lysozyme. J. Mol. Biol. 1992, 225:939-943.
5. D'Amico S., Gerday C., Feller G. Structural determinants of cold adaptation and stability in a large protein. J. Biol. Chem. 2001, 276:25791-25796.
6. D'Amico S., Collins T., Marx J.C., Feller G., Gerday C. Psychrophilic microorganisms: challenges for life. EMBO Rep. 2006, 7:385-389.
7. DeLano W.L. The PyMOL Molecular Graphics System 2002, DeLano Scientific, Palo Alto, CA, USA.
8. Dianoux A.C., Jolles P. Study of a lysozyme poor in cystine and tryptophan: the lysozyme of goose egg-white. Biochim. Biophys. Acta 1967, 133:472-479.
9. Dill K.A. Dominant forces in protein folding. Biochemistry-US 1990, 29:7133-7155.
10. Evans P.R. SCALA. Proceedings of the CCP4 Study Weekend. Recent Advances in Phasing 1997, 97-102. Daresbury Laboratory, Warrington. K.S. Wilson, G. Davies, A.W. Ashton, S. Bailey (Eds.).
11. Feller G., Gerday C. Psychrophilic enzymes: hot topics in cold adaptation. Nat. Rev. Microbiol. 2003, 1:200-208.
12. Feller G., Narinx E., Arpigny J.L., Aittaleb M., Baise E., Genicot S., Gerday C. Enzymes from psychrophilic organisms. FEMS Microbiol. Rev. 1996, 18:189-202.
13. Fields P.A., Somero G.N. Hot spots in cold adaptation: localized increases in conformational flexibility in lactate dehydrogenase A(4) orthologs of Antarctic notothenioid fishes. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:11476-11481.
14. Georlette D., Damien B., Blaise V., Depiereux E., Uversky V.N., Gerday C., Feller G. Structural and functional adaptations to extreme temperatures in psychrophilic, mesophilic, and thermophilic DNA ligases. J. Biol. Chem. 2003, 278:37015-37023.
15. Georlette D., Blaise V., Collins T., D'Amico S., Gratia E., Hoyoux A., Marx J.C., Sonan G., Feller G., Gerday C. Some like it cold: biocatalysis at low temperatures. FEMS Microbiol. Rev. 2004, 28:25-42.
16. Gille C., Frommel C. STRAP: editor for Structural Alignments of Proteins. Bioinformatics 2001, 17:377-378.
17. Goto T., Abe Y., Kakuta Y., Takeshita K., Imoto T., Ueda T. Crystal structure of Tapes japonica Lysozyme with substrate analogue: structural basis of the catalytic mechanism and manifestation of its chitinase activity accompanied by quaternary structural change. J. Biol. Chem. 2007, 282:27459-27467.
18. Gouet P., Courcelle E., Stuart D.I., Metoz F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 1999, 15:305-308.
19. Grütter M.G., Weaver L.H., Matthews B.W. Goose lysozyme structure: an evolutionary link between hen and bacteriophage lysozymes?. Nature 1983, 303:828-831.
20. Helland R., Larsen L.R., Finstad S., Kyomuhendo P., Larsen A.N. The crystal structure of g-type lysozyme from Atlantic cod (Gadus morhua L.) in complex with NAG oligomers sheds new light on substrate binding and the catalytic mechanism. Cell. Mol. Life Sci. 2009, 66:2585-2598.
21. Hikima J., Minagawa S., Hirono I., Aoki T. Molecular cloning, expression and evolution of the Japanese flounder goose-type lysozyme gene, and the lytic activity of its recombinant protein. Biochim. Biophys. Acta 2001, 1520:35-44.
22. Hirakawa H., Ochi A., Kawahara Y., Kawamura S., Torikata T., Kuhara S. Catalytic reaction mechanism of goose egg-white lysozyme by molecular modelling of enzyme substrate complex. J. Biochem. 2008, 144:753-761.
23. Honda Y., Fukamizo T. Substrate binding subsites of chitinase from barley seeds and lysozyme from goose egg-white. Biochim. Biophys. Acta. Prot. Struct. Mol. Enz. 1998, 1388:53-65.
24. Irwin D.M., Gong Z. Molecular evolution of vertebrate goose-type lysozyme genes. J. Mol. Evol. 2003, 56:234-242.
25. Isaacs N.W., Machin K.J., Masakuni M. 3-Dimensional structure of goose-type lysozyme from the egg-white of the Australian Black Swan, Cygnus-Atratus. Aust. J. Biol. Sci. 1985, 38:13-22.
26. Ito Y., Yoshikawa A., Hotani T., Fukuda S., Sugimura K., Imoto T. Amino acid sequences of lysozymes newly purified from invertebrates imply wide distribution of a novel class in the lysozyme family. Eur. J. Biochem. 1999, 259:456-461.
27. Jollès P. Lysozymes: Model Enzymes in Biochemistry and Biology 1996, Birkhäuser Verlag, Basel.
28. Jollès P., Jollès J. What's new in lysozyme research? Always a model system, today as yesterday. Mol. Cell. Biochem. 1984, 63:165-189.
29. Jones T.A., Zou J.Y., Cowan S.W., 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. 1991, 47:110-119.
30. Kabsch W., Sander C. Dictionary of protein secondary structure - pattern-recognition of hydrogen-bonded and geometrical features. Biopolymers 1983, 22:2577-2637.
31. Kawamura S., Ohno K., Ohkuma M., Chijiiwa Y., Torikata T. Experimental verification of the crucial roles of Glu(73) in the catalytic activity and structural stability of goose type lysozyme. J. Biochem. 2006, 140:75-85.
32. Kawamura S., Ohkuma M., Chijiiwa Y., Kohno D., Nakagawa H., Hirakawa H., Kuhara S., Torikata T. Role of disulfide bonds in goose-type lysozyme. FEBS J. 2008, 275:2818-2830.
33. Kyomuhendo P., Myrnes B., Nilsen I.W. A cold active salmon goose-type lysozyme with high heat tolerance. Cell. Moll. Life. Sci. 2007, 64:2841-2847.
34. Larsen A.N., Solstad T., Svineng G., Seppola M., Jorgensen T.O. Molecular characterisation of a goose-type lysozyme gene in Atlantic cod (Gadus morhua L.). Fish Shellfish Immunol 2009, 26:122-132.
35. Lavigne R., Briers Y., Hertveldt K., Robben J., Volckaert G. Identification and characterization of a highly thermostable bacteriophage lysozyme. Cell. Moll. Life. Sci. 2004, 61:2753-2759.
36. Leslie A.G.W. Recent changes to the MOSFLM package for processing film and image plate data. In Joint CCP4 and ESF-EACBM Newsletters on Protein Crystallography 1992, 26. Daresbury Laboratory, Warrington, UK.
37. Maenaka K., Matsushima M., Song H., Sunada F., Watanabe K., Kumagai I. Dissection of protein-carbohydrate interactions in mutant hen egg-white lysozyme complexes and their hydrolytic activity. J. Mol. Biol. 1995, 247:281-293.
38. Marx J.C., Collins T., D'Amico S., Feller G., Gerday C. Cold-adapted enzymes from marine Antarctic microorganisms. Mar. Biotechnol. (NY) 2007, 9:293-304.
39. Masschalck B., Michiels C.W. Antimicrobial properties of lysozyme in relation to foodborne vegetative bacteria. Crit. Rev. Microbiol. 2003, 29:191-214.
40. Matsuo K., Watanabe H., Tate S.I., Tachibana H., Gekko K. Comprehensive secondary-structure analysis of disulfide variants of lysozyme by synchrotron-radiation vacuum-ultraviolet circular dichroism. Proteins 2009, 77:191-201.
41. McDonald I.K., Thornton J.M. Satisfying hydrogen-bonding potential in proteins. J. Mol. Biol. 1994, 238:777-793.
42. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr., Sect. D: Biol. Crystallogr. 1997, 53:240-255.
43. Nilsen I.W., Overbo K., Sandsdalen E., Sandaker E., Sletten K., Myrnes B. Protein purification and gene isolation of chlamysin, a cold-active lysozyme-like enzyme with antibacterial activity. FEBS Lett. 1999, 464:153-158.
44. Nilsen I.W., Myrnes B., Edvardsen R.B., Chourrout D. Urochordates carry multiple genes for goose-type lysozyme and no genes for chicken- or invertebrate-type lysozymes. Cell. Moll. Life. Sci. 2003, 60:2210-2218.
45. Pace C.N., Grimsley G.R., Thomson J.A., Barnett B.J. Conformational stability and activity of ribonuclease-T1 with zero, one, and two intact disulfide bonds. J. Biol. Chem. 1988, 263:11820-11825.
46. Pace C.N., Shirley B.A., McNutt M., Gajiwala K. Forces contributing to the conformational stability of proteins. FASEB J. 1996, 10:75-83.
47. Perrakis A., Morris R., Lamzin V.S. Automated protein model building combined with iterative structure refinement. Nat. Struct. Biol. 1999, 6:458-463.
48. Pooart J., Torikata T., Araki T. Enzymatic properties of rhea lysozyme. Biosci., Biotechnol. Biochem. 2005, 69:103-112.
49. Savan R., Aman A., Sakai M. Molecular cloning of G type lysozyme cDNA in common carp (Cyprinus carpio L.). Fish Shellfish Immunol 2003, 15:263-268.
50. Siddiqui K.S., Cavicchioli R. Improved thermal stability and activity in the cold-adapted lipase B from Candida antarctica following chemical modification with oxidized polysaccharides. Extremophiles 2005, 9:471-476.
51. Siddiqui K.S., Cavicchioli R. Cold-adapted enzymes. Annu. Rev. Biochem. 2006, 75:403-433.
52. Smalås A.O., Leiros H.H., Os V., Willassen N.P. Cold adapted enzymes. Biotechnol. Annu. Rev. 2000, 6:1-57.
53. Thammasirirak S., Torikata T., Takami K., Murata K., Araki T. Purification and characterization of goose type lysozyme from cassowary (Casuarius casuarius) egg-white. Biosci., Biotechnol. Biochem. 2001, 65:584-592.
54. Thammasirirak S., Torikata T., Takami K., Murata K., Araki T. Study of the physicochemical stability of cassowary (Casuarius casuarius) goose-type lysozyme. Proceedings of Faculty of Agriculture Kyushu Tokai University 2002, 21:9-15.
55. Trefethen J.M., Pace C.N., Scholtz J.M., Brems D.N. Charge-charge interactions in the denatured state influence the folding kinetics of ribonuclease Sa. Protein Sci. 2005, 14:1934-1938.
56. Vagin A.A.T.A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 1997, 30:1022-1025.
57. Vriend G. What If - a molecular modeling and dug design program. J. Mol. Graph. 1990, 8:52-56.
58. Weaver L.H., Matthews B.W. Structure of bacteriophage-T4 lysozyme refined at 1.7 a resolution. J. Mol. Biol. 1987, 193:189-199.
59. Weaver L.H., Grutter M.G., Remington S.J., Gray T.M., Isaacs N.W., Matthews B.W. Comparison of goose-type, chicken-type, and phage-type lysozymes illustrates the changes that occur in both amino acid sequence and three-dimensional structure during evolution. J. Mol. Evol. 1984, 21:97-111.
60. Weaver L.H., Grutter M.G., Matthews B.W. The refined structures of goose lysozyme and its complex with a bound trisaccharide show that the "goose-type" lysozymes lack a catalytic aspartate residue. J. Mol. Biol. 1995, 245:54-68.
61. Wetzel R., Perry L.J., Baase W.A., Becktel W.J. Disulfide bonds and thermal-stability in T4 lysozyme. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:401-405.
62. Yin Z.X., He J.G., Deng W.X., Chan S.M. Molecular cloning, expression of orange-spotted grouper goose-type lysozyme cDNA, and lytic activity of its recombinant protein. Dis. Aquatic Org. 2003, 55:117-123.
63. Zhao J., Song L., Li C., Zou H., Ni D., Wang W., Xu W. Molecular cloning of an invertebrate goose-type lysozyme gene from Chlamys farreri, and lytic activity of the recombinant protein. Mol. Immunol. 2007, 44:1198-1208.
64. Zhou Y.Q., Hall C.K., Karplus M. The calorimetric criterion for a two-state process revisited. Protein Sci. 1999, 8:1064-1074.
65. Zou H., Song L., Xu W., Yang G. Molecular cloning and characterisation analysis of cDNA encoding g-type lysozyme from scallop (Argopectens irradians). High Tech. Lett. 2005, 15:101-106.