The 0.93 Å crystal structure of sphericase: A calcium-loaded serine protease from Bacillus sphaericus

Journal of Molecular Biology

Volumn 332, Issue 5, 2003, Pages 1071-1082

  Almog, Orna ^a   González, Ana ^b,d   Klein, Daniela ^c   Greenblatt, Harry M ^c   Braun, Sergei ^c   Shoham, Gil ^c  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^d SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

Author keywords

Cold adaptation; Mesophilic; Serine protease; Sphericase; Subtilisin

Indexed keywords

AMINO ACID; CALCIUM ION; DISULFIDE; SERINE PROTEINASE; SUBTILISIN; WATER; CALCIUM; ION;

AMINO ACID SEQUENCE; ANALYTIC METHOD; ARTICLE; BACILLUS SPHAERICUS; BINDING AFFINITY; BINDING SITE; CALCIUM BINDING; CHEMICAL BOND; COMPARATIVE STUDY; CONTROLLED STUDY; CORRELATION ANALYSIS; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DIFFRACTION; MOLECULAR DYNAMICS; MOLECULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; BACILLUS; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COLD; DATA BASE; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS; PH; PHYSIOLOGY; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY;

BACILLI; BACILLUS SPHAERICUS;

AMINO ACID SEQUENCE; BACILLUS; BINDING SITES; CALCIUM; COLD; CRYSTALLOGRAPHY, X-RAY; DATABASES; HYDROGEN-ION CONCENTRATION; IONS; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID; SERINE ENDOPEPTIDASES; SUBTILISIN;

EID: 0041384380     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.07.011     Document Type: Article

References (56)

1. Jaenicke R., Zavodszky P. Proteins under extreme physical conditions. FEBS. Letters. 268:1990;344-349.
2. Szilagyi A., Zavodszky P. Structural basis for the extreme thermostability of D-glyceraldehyde-3-phosphate dehydrogenase from Thermotoga maritima: analysis based on homology modelling. Protein Eng. 8:1995;779-789.
3. Szilagyi A., Zavodszky P. Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey. Struct. Fold. Des. 8:2000;493-504.
4. Gerday C., Aittaleb M., Bentahir M., Chessa J.P., Claverie P., Collins T., et al. Cold-adapted enzymes: from fundamentals to biotechnology. Trends Biotechnol. 18:2000;103-107.
5. Davail S., Feller G., Narinx E., Gerday C. Sequence of the subtilisin-encoding gene from an antarctic psychrotroph Bacillus TA41. Gene. 119:1992;143-144.
6. Davail S., Feller G., Narinx E., Gerday C. Cold adaptation of proteins. Purification, characterization, and sequence of the heat-labile subtilisin from the antarctic psychrophile Bacillus TA41. J. Biol. Chem. 269:1994;17448-17453.
7. Feller G., Lonhienne T., Deroanne C., Libioulle C., Van Beeumen J., Gerday C. Purification, characterization, and nucleotide sequence of the thermolabile alpha-amylase from the antarctic psychrotroph Alteromonas haloplanctis A23. J. Biol. Chem. 267:1992;5217-5221.
8. Feller G., Payan F., Theys F., Qian M., Haser R., Gerday C. Stability and structural analysis of alpha-amylase from the antarctic psychrophile Alteromonas haloplanctis A23. Eur. J. Biochem. 222:1994;441-447.
9. Kim S.Y., Hwang K.Y., Kim S.H., Sung H.C., Han Y.S., Cho Y. Structural basis for cold adaptation. Sequence, biochemical properties, and crystal structure of malate dehydrogenase from a psychrophile Aquaspirillium arcticum. J. Biol. Chem. 274:1999;11761-11777.
10. Wintrode P.L., Arnold F.H. Temperature adaptation of enzymes: lessons from laboratory evolution. Advan. Protein Chem. 55:2000;161-225.
11. Wintrode P.L., Miyazaki K., Arnold F.H. Cold adaptation of a mesophilic subtilisin-like protease by laboratory evolution. J. Biol. Chem. 275:2000;31635-31640.
12. Wintrode P.L., Miyazaki K., Arnold F.H. Patterns of adaptation in a laboratory evolved thermophilic enzyme. Biochim. Biophys. Acta. 1549:2001;1-8.
13. Narinx E., Baise E., Gerday C. Subtilisin from psychrophilic antarctic bacteria: characterization and site-directed mutagenesis of residues possibly involved in the adaptation to cold. Protein. Eng. 10:1997;1271-1279.
14. Gallagher T., Bryan P., Gilliland G.L. Calcium-independent subtilisin by design. Protein: Struct. Funct. Genet. 16:1993;205-213.
15. Ha N.C., Oh B.C., Shin S., Kim H.J., Oh T.K., Kim Y.O., et al. Crystal structures of a novel, thermostable phytase in partially and fully calcium-loaded states. Nature Struct. Biol. 7:2000;147-153.
16. 2+ ions on inactivation between 30 and 70 degrees C of the extracellular proteinase from Pseudomonas fluorescens 22F. Milchwissenschaft-Milk Sci. Intl. 54:1999;436-438.
17. Strausberg S.L., Alexander P.A., Gallagher D.T., Gilliland G.L., Barnett B.L., Bryan P.N. Directed evolution of a subtilisin with calcium-independent stability. Biotechnology (NY). 13:1995;669-673.
18. Arnold F.H., Wintrode P.L., Miyazaki K., Gershenson A. How enzymes adapt: lessons from directed evolution. Trends Biochem. Sci. 26:2001;100-106.
19. Feller G., Zekhnini Z., Lamotte-Brasseur J., Gerday C. Enzymes from cold-adapted microorganisms. The class C beta-lactamase from the antarctic psychrophile Psychrobacter immobilis. A5. Eur. J. Biochem. 244:1997;186-191.
20. Aghajari N., Feller G., Gerday C., Haser R. Structures of the psychrophilic Alteromonas haloplanctis alpha-amylase give insights into cold adaptation at a molecular level. Structure. 6:1998;1503-1516.
21. Gerike U., Russell R.J., Danson M.J., Russell N.J., Hough D.W., Taylor G.L. Preliminary crystallographic studies of citrate synthase from an Antarctic psychrotolerant bacterium. Acta Crystallog. sect. D. 54:1998;1012-1013.
22. Aghajari N., Van Petegem F., Villeret V., Chessa J.P., Gerday C., Haser R., Van Beeumen J. Crystal structures of a psychrophilic metalloprotease reveal new insights into catalysis by cold-adapted proteases. Proteins: Struct. Funct. Genet. 50:2003;636-647.
23. Pantoliano M.W., Whitlow M., Wood J.F., Rollence M.L., Finzel B.C., Gilliland G.L., et al. The engineering of binding affinity at metal ion binding sites for the stabilization of proteins: subtilisin as a test case. Biochemistry. 27:1988;8311-8317.
24. Siezen R.J., Leunissen J.A. Subtilases: the superfamily of subtilisin-like serine proteases. Protein Sci. 6:1997;501-523.
25. Almog O., Klein D., Braun S., Shoham G. Crystallization and preliminary crystallographic analysis of sfericase. A Bacillus sphaericus calcium-dependent serine proteinase. J. Mol. Biol. 235:1994;760-762.
26. Dauter Z., Lamzin V.S., Wilson K.S. Proteins at atomic resolution. Curr. Opin. Struct. Biol. 5:1995;784-790.
27. Sheldrick G.M., Schneider T.R. SHELXL: high-resolution refinement. Methods Enzymol. 277:1997;319-343.
28. Wati M.R., Thanabalu T., Porter A.G. Gene from tropical Bacillus sphaericus encoding a protease closely related to subtilisins from Antarctic bacilli. Biochim. Biophys. Acta. 1352:1997;56-62.
29. Servant P., Rosso M.L., Hamon S., Poncet S., Del cluse A., Rapoport G. Production of Cry11A and Cry11Ba toxins in Bacillus sphaericus confers toxicity towards Aedes aegypti and resistant Culex populations. Appl. Environ. Microbiol. 65:1999;3021-3026.
30. Kuhn P., Knapp M., Soltis S.M., Ganshaw G., Thoene M., Bott R. The 0.78 Å structure of a serine protease: Bacillus lentus subtilisin. Biochemistry. 37:1998;13446-13452.
31. Gilliland G.L., Gallagher T., Bryan P. Crystal structure analysis of subtilisin BPN′ mutants engineered for studying thermal stability. Bott R., Betzel C. Subtilisin Enzymes: Practical Protein Engineering. 1996;159-169 Plenum Press, New York.
32. Bode W., Papamokos E., Musil D. The high-resolution X-ray crystal structure of the complex formed between subtilisin Carlsberg and eglin c, an elastase inhibitor from the leech Hirudo medicinalis. Structural analysis, subtilisin structure and interface geometry. Eur. J. Biochem. 166:1987;673-692.
33. Teplyakov A.V., Kuranova I.P., Harutyunyan E.H., Vainshtein B.K., Frommel C., Hohne W.E., Wilson K.S. Crystal structure of thermitase at 1.4 Å resolution. J. Mol. Biol. 214:1990;261-279.
34. Betzel C., Teplyakov A.V., Harutyunyan E.H., Saenger W., Wilson K.S. Thermitase and proteinase K: a comparison of the refined three-dimensional structures of the native enzymes. Protein Eng. 3:1990;161-172.
35. Thornton J.M. Disulfide bridges in globular proteins. J. Mol. Biol. 151:1981;261-287.
36. Ravelli R.B., McSweeney S.M. The 'fingerprint' that X-rays can leave on structures. Struct. Fold. Des. 8:2000;315-328.
37. Burmeister W.P. Structural changes in a cryo-cooled protein crystal owing to radiation damage. Acta Crystallog. sect. D. 56:2000;328-341.
38. Brodersen D.E., Etzerodt M., Madsen P., Celis J.E., Thogersen H.C., Nyborg J., Kjeldgaard M. EF-hands at atomic resolution: the structure of human psoriasin (S100A7) solved by MAD phasing. Structure. 6:1998;477-489.
39. McPhalen C.A., Strynadka N.C., James M.N.G. Calcium-binding sites in proteins: a structural perspective. Advan. Protein Chem. 42:1991;77-144.
40. Einspahr H., Cook W.J., Bugg C.E. Conformational flexibility in single-stranded oligonucleotides: crystal structure of a hydrated calcium salt of adenylyl-(3′-5′)-adenosine. Biochemistry. 20:1981;5788-5794.
41. Almog O., Gallagher D.T., Ladner J.E., Strausberg S., Alexander P., Bryan P., Gilliland G.L. Structural basis of thermostability. Analysis of stabilizing mutations in subtilisin BPN′ J. Biol. Chem. 277:2002;27553-27558.
42. Myers P.S., Yousten A.A. Localization of a mosquito-larval toxin of Bacillus sphaericus 1593. Appl. Environ. Microbiol. 39:1980;1205-1211.
43. Narinx E., Davail S., Feller G., Gerday C. Nucleotide and derived amino acid sequence of the subtilisin from the antarctic psychrotroph Bacillus TA39. Biochim. Biophys. Acta. 1131:1992;111-113.
44. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
45. Leslie A.G.W. Joint CCP4+ESF-EAMCB. NewsLetter on Protein Crystallog. 26:1992;4-8.
46. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D. 50:1994;760-763.
47. delaFortelle E., Bricogne G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276:1997;472-494.
48. Cowtan K. Error estimation and bias correction in phase-improvement calculations. Acta Crystallog. sect. D. 55:1999;1555-1567.
49. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallog. sect. D. 53:1997;240-255.
50. Engh R.A., Huber R. Accurate bond and angle parameters for X-ray protein-structure refinement. Acta Crystallog. sect. A. 47:1991;392-400.
51. Navaza J., Saludjian P. AMoRe: an automated molecular replacement program package. Methods Enzymol. 276:1997;581-594.
52. Murshudov G.N., Vagin A.A., Lebedev A., Wilson K.S., Dodson E.J. Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallog. sect. D. 55:1999;247-255.
53. Tronrud D.E. Conjugate-direction minimization: an improved method for the refinement of macromolecules. Acta Crystallog. sect. A. 48:1992;912-916.
54. Perrakis A., Morris R., Lamzin V.S. Automated protein model building combined with iterative structure refinement. Nature Struct. Biol. 6:1999;458-463.
55. Brunger A.T., Nilges M. Computational challenges for macromolecular structure determination by X-ray crystallography and solution NMR-spectroscopy. Quart. Rev. Biophys. 26:1993;49-125.
56. Diederichs K., Karplus P.A. Improved R-factors for diffraction data analysis in macromolecular crystallography. Nature Struct. Biol. 4:1997;269-275.