Structural and Mechanistic Exploration of Acid Resistance: Kinetic Stability Facilitates Evolution of Extremophilic Behavior

Journal of Molecular Biology

Volumn 368, Issue 3, 2007, Pages 870-883

  Kelch, Brian A ^a   Eagen, Kyle P ^b   Erciyas, F Pinar ^a,b   Humphris, Elisabeth L ^b   Thomason, Adam R ^b   Mitsuiki, Shinji ^c   Agard, David A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c KYUSHU SANGYO UNIVERSITY   (Japan)

Author keywords

acid stability; electrostatics; folding transition state structure; kinetic stability; protein folding

Indexed keywords

ACID; BACTERIAL ENZYME; NOCARDIOPSIS ALBA PROTEASE A; PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; ELECTRICITY; ENERGY; ENERGY TRANSFER; ENZYME KINETICS; ENZYME STRUCTURE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN DOMAIN; SENSITIVITY ANALYSIS; TITRIMETRY;

NOCARDIOPSIS ALBA;

EID: 34047133713     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.02.032     Document Type: Article

References (79)

1. Jaenicke R. Protein stability and molecular adaptation to extreme conditions. Eur. J. Biochem. 202 (1991) 715-728
2. Scandurra R., Consalvi V., Chiaraluce R., Politi L., and Engel P.C. Protein stability in extremophilic archaea. Front. Biosci. 5 (2000) D787-D795
3. Kumar S., and Nussinov R. How do thermophilic proteins deal with heat?. Cell Mol. Life Sci. 58 (2001) 1216-1233
4. Russell R.J., and Taylor G.L. Engineering thermostability: lessons from thermophilic proteins. Curr. Opin. Biotechnol. 6 (1995) 370-374
5. Fersht A. Structure and Mechanism in Protein Science. 2nd edit. (1999), Freeman, New York
6. Goto Y., and Nishikiori S. Role of electrostatic repulsion in the acidic molten globule of cytochrome c. J. Mol. Biol. 222 (1991) 679-686
7. Chen H.M., You J.L., Markin V.S., and Tsong T.Y. Kinetic analysis of the acid and the alkaline unfolded states of staphylococcal nuclease. J. Mol. Biol. 220 (1991) 771-778
8. Ionescu R.M., and Eftink M.R. Global analysis of the acid-induced and urea-induced unfolding of staphylococcal nuclease and two of its variants. Biochemistry 36 (1997) 1129-1140
9. Flanagan M.A., Garcia-Moreno B., Friend S.H., Feldmann R.J., Scouloudi H., and Gurd F.R. Contributions of individual amino acid residues to the structural stability of cetacean myoglobins. Biochemistry 22 (1983) 6027-6037
10. Hughson F.M., and Baldwin R.L. Use of site-directed mutagenesis to destabilize native apomyoglobin relative to folding intermediates. Biochemistry 28 (1989) 4415-4422
11. Geierstanger B., Jamin M., Volkman B.F., and Baldwin R.L. Protonation behavior of histidine 24 and histidine 119 in forming the pH 4 folding intermediate of apomyoglobin. Biochemistry 37 (1998) 4254-4265
12. Barrick D., and Baldwin R.L. Three-state analysis of sperm whale apomyoglobin folding. Biochemistry 32 (1993) 3790-3796
13. Cooper J.B., Khan G., Taylor G., Tickle I.J., and Blundell T.L. X-ray analyses of aspartic proteinases. II. Three-dimensional structure of the hexagonal crystal form of porcine pepsin at 2.3 A resolution. J. Mol. Biol. 214 (1990) 199-222
14. Fushinobu S., Ito K., Konno M., Wakagi T., and Matsuzawa H. Crystallographic and mutational analyses of an extremely acidophilic and acid-stable xylanase: biased distribution of acidic residues and importance of Asp37 for catalysis at low pH. Protein Eng. 11 (1998) 1121-1128
15. Bonisch H., Schmidt C.L., Schafer G., and Ladenstein R. The structure of the soluble domain of an archaeal Rieske iron-sulfur protein at 1.1 A resolution. J. Mol. Biol. 319 (2002) 791-805
16. Kashiwagi T., Kunishima N., Suzuki C., Tsuchiya F., Nikkuni S., Arata Y., and Morikawa K. The novel acidophilic structure of the killer toxin from halotolerant yeast demonstrates remarkable folding similarity with a fungal killer toxin. Structure 5 (1997) 81-94
17. Bender M., and Sturtevant J.M. The heat of the inactivation of pepsin. J. Am. Chem. Soc. 69 (1947) 607-612
18. Buzzell A., and Sturtevant J.M. The heat of denaturation of pepsin. J. Am. Chem. Soc. 74 (1952) 1983-1987
19. Edelhoch H. The denaturation of pepsin. I. Macromolecular changes. J. Am. Chem. Soc. 79 (1957) 6100-6109
20. Favilla R., Parisoli A., and Mazzini A. Alkaline denaturation and partial refolding of pepsin investigated with DAPI as an extrinsic probe. Biophys. Chem. 67 (1997) 75-83
21. Schafer K., Magnusson U., Scheffel F., Schiefner A., Sandgren M.O., Diederichs K., et al. X-ray structures of the maltose-maltodextrin-binding protein of the thermoacidophilic bacterium Alicyclobacillus acidocaldarius provide insight into acid stability of proteins. J. Mol. Biol. 335 (2004) 261-374
22. Settembre E.C., Chittuluru J.R., Mill C.P., Kappock T.J., and Ealick S.E. Acidophilic adaptations in the structure of Acetobacter aceti N5-carboxyaminoimidazole ribonucleotide mutase (PurE). Acta Crystallog. sect. D Biol. Crystallog. 60 (2004) 1753-1760
23. Walter R.L., Ealick S.E., Friedman A.M., Blake II R.C., Proctor P., and Shoham M. Multiple wavelength anomalous diffraction (MAD) crystal structure of rusticyanin: a highly oxidizing cupredoxin with extreme acid stability. J. Mol. Biol. 263 (1996) 730-751
24. Botuyan M.V., Toy-Palmer A., Chung J., Blake II R.C., Beroza P., Case D.A., and Dyson H.J. NMR solution structure of Cu(I) rusticyanin from Thiobacillus ferrooxidans: Structural basis for the extreme acid stability and redox potential. J. Mol. Biol. 263 (1996) 752-767
25. Forrer P., Chang C., Ott D., Wlodawer A., and Pluckthun A. Kinetic stability and crystal structure of the viral capsid protein SHP. J. Mol. Biol. 344 (2004) 179-193
26. Rodriguez-Larrea D., Minning S., Borchert T.V., and Sanchez-Ruiz J.M. Role of solvation barriers in protein kinetic stability. J. Mol. Biol. 360 (2006) 715-724
27. Kaushik J.K., Ogasahara K., and Yutani K. The unusually slow relaxation kinetics of the folding-unfolding of pyrrolidone carboxyl peptidase from a hyperthermophile, Pyrococcus furiosus. J. Mol. Biol. 316 (2002) 991-1003
28. Eder J., Rheinnecker M., and Fersht A.R. Folding of subtilisin BPN′: role of the pro-sequence. J. Mol. Biol. 233 (1993) 293-304
29. Baker D., Sohl J.L., and Agard D.A. A protein-folding reaction under kinetic control. Nature 356 (1992) 263-265
30. Sohl J.L., Jaswal S.S., and Agard D.A. Unfolded conformations of alpha-lytic protease are more stable than its native state. Nature 395 (1998) 817-819
31. Truhlar S.M., Cunningham E.L., and Agard D.A. The folding landscape of Streptomyces griseus protease B reveals the energetic costs and benefits associated with evolving kinetic stability. Protein Sci. 13 (2004) 381-390
32. Peters R.J., Shiau A.K., Sohl J.L., Anderson D.E., Tang G., Silen J.L., and Agard D.A. Pro region C-terminus:protease active site interactions are critical in catalyzing the folding of alpha-lytic protease. Biochemistry 37 (1998) 12058-12067
33. Sauter N.K., Mau T., Rader S.D., and Agard D.A. Structure of alpha-lytic protease complexed with its pro region. Nauret Struct. Biol. 5 (1998) 945-950
34. Cunningham E.L., and Agard D.A. Disabling the folding catalyst is the last critical step in alpha-lytic protease folding. Protein Sci. 13 (2004) 325-331
35. Jaswal S.S., Truhlar S.M., Dill K.A., and Agard D.A. Comprehensive analysis of protein folding activation thermodynamics reveals a universal behavior violated by kinetically stable proteases. J. Mol. Biol. 347 (2005) 355-366
36. Jaswal S.S., Sohl J.L., Davis J.H., and Agard D.A. Energetic landscape of alpha-lytic protease optimizes longevity through kinetic stability. Nature 415 (2002) 343-346
37. Mitsuiki S., Sakai M., Moriyama Y., Goto M., and Furukawa K. Purification and some properties of a keratinolytic enzyme from an alkaliphilic Nocardiopsis sp, TOA-1. Biosci. Biotechnol. Biochem. 66 (2002) 164-167
38. Rupley J.A. Susceptibility to attack by proteolytic enzymes. Methods Enzymol. 11 (1967) 905-917
39. Park C., and Marqusee S. Probing the high energy states in proteins by proteolysis. J. Mol. Biol. 343 (2004) 1467-1476
40. Park C., and Marqusee S. Pulse proteolysis: a simple method for quantitative determination of protein stability and ligand binding. Nature Methods 2 (2005) 207-212
41. Fujinaga M., Delbaere L.T., Brayer G.D., and James M. N. Refined structure of alpha-lytic protease at 1.7 A resolution. Analysis of hydrogen bonding and solvent structure. J. Mol. Biol. 184 (1985) 479-502
42. Fuhrmann C.N., Kelch B.A., Ota N., and Agard D.A. The 0.83 A resolution crystal structure of alpha-lytic protease reveals the detailed structure of the active site and identifies a source of conformational strain. J. Mol. Biol. 338 (2004) 999-1013
43. James M.N., Sielecki A.R., Brayer G.D., Delbaere L. T., and Bauer C.A. Structures of product and inhibitor complexes of Streptomyces griseus protease A at 1.8 A resolution. A model for serine protease catalysis. J. Mol. Biol. 144 (1980) 43-88
44. Huang K., Lu W., Anderson S., Laskowski Jr. M., and James M.N. Water molecules participate in proteinase-inhibitor interactions: crystal structures of Leu18, Ala18, and Gly18 variants of turkey ovomucoid inhibitor third domain complexed with Streptomyces griseus proteinase B. Protein Sci. 4 (1995) 1985-1997
45. Kitadokoro K., Tsuzuki H., Nakamura E., Sato T., and Teraoka H. Purification, characterization, primary structure, crystallization and preliminary crystallographic study of a serine proteinase from Streptomyces fradiae ATCC 14544. Eur. J. Biochem. 220 (1994) 55-61
46. Nienaber V.L., Breddam K., and Birktoft J.J. A glutamic acid specific serine protease utilizes a novel histidine triad in substrate binding. Biochemistry 32 (1993) 11469-11475
47. Truhlar S.M., and Agard D.A. The folding landscape of an alpha-lytic protease variant reveals the role of a conserved beta-hairpin in the development of kinetic stability. Protein 61 (2005) 105-114
48. Mace J.E., Wilk B.J., and Agard D.A. Functional linkage between the active site of alpha-lytic protease and distant regions of structure: scanning alanine mutagenesis of a surface loop affects activity and substrate specificity. J. Mol. Biol. 251 (1995) 116-134
49. Mace J.E., and Agard D.A. Kinetic and structural characterization of mutations of glycine 216 in alpha-lytic protease: a new target for engineering substrate specificity. J. Mol. Biol. 254 (1995) 720-736
50. Craik C.S., Roczniak S., Largman C., and Rutter W.J. The catalytic role of the active site aspartic acid in serine proteases. Science 237 (1987) 909-913
51. Sprang S., Standing T., Fletterick R.J., Stroud R.M., Finer-Moore J., Xuong N.H., et al. The three-dimensional structure of Asn102 mutant of trypsin: role of Asp102 in serine protease catalysis. Science 237 (1987) 905-909
52. Carter P., and Wells J.A. Dissecting the catalytic triad of a serine protease. Nature 332 (1988) 564-568
53. Nakagawa S., and Umeyama H. Role of catalytic residues in the formation of a tetrahedral adduct in the acylation reaction of bovine beta-trypsin. A molecular orbital study. J. Mol. Biol. 179 (1984) 103-123
54. Reiling K.K., Krucinski J., Miercke L.J., Raymond W.W., Caughey G.H., and Stroud R.M. Structure of human pro-chymase: a model for the activating transition of granule-associated proteases. Biochemistry 42 (2003) 2616-2624
55. Hedstrom L., Lin T.Y., and Fast W. Hydrophobic interactions control zymogen activation in the trypsin family of serine proteases. Biochemistry 35 (1996) 4515-4523
56. Karshikoff A., and Ladenstein R. Ion pairs and the thermotolerance of proteins from hyperthermophiles: a "traffic rule" for hot roads. Trends Biochem. Sci. 26 (2001) 550-556
57. Plaxco K.W., Simons K.T., and Baker D. Contact order, transition state placement and the refolding rates of single domain proteins. J. Mol. Biol. 277 (1998) 985-994
58. Jaswal S.S. Thermodynamics, Kinetics and Landscapes in alpha-Lytic Protease: A Role for Pro Regions in Kinetic Stability (2000), University of California, San Francisco
59. Stackhouse T., Onuffer J.J., Matthews C.R., Ahmed S.A., and Miles E.W. The role of protein folding in the evolution of protein sequences. Cold Spring Harb. Symp. Quant. Biol. 52 (1987) 537-544
60. Kragelund B.B., Hojrup P., Jensen M.S., Schjerling C.K., Juul E., Knudsen J., and Poulsen F.M. Fast and one-step folding of closely and distantly related homologous proteins of a four-helix bundle family. J. Mol. Biol. 256 (1996) 187-200
61. Perl D., Welker C., Schindler T., Schroder K., Marahiel M.A., Jaenicke R., and Schmid F.X. Conservation of rapid two-state folding in mesophilic, thermophilic and hyperthermophilic cold shock proteins. Nature Struct. Biol. 5 (1998) 229-235
62. Schindler T., Graumann P.L., Perl D., Ma S., Schmid F.X., and Marahiel M.A. The family of cold shock proteins of Bacillus subtilis. Stability and dynamics in vitro and in vivo. J. Biol. Chem. 274 (1999) 3407-3413
63. Chiti F., Taddei N., White P.M., Bucciantini M., Magherini F., Stefani M., and Dobson C.M. Mutational analysis of acylphosphatase suggests the importance of topology and contact order in protein folding. Nature Struct. Biol. 6 (1999) 1005-1009
64. Clarke J., Cota E., Fowler S.B., and Hamill S.J. Folding studies of immunoglobulin-like beta-sandwich proteins suggest that they share a common folding pathway. Structure 7 (1999) 1145-1153
65. Martinez J.C., and Serrano L. The folding transition state between SH3 domains is conformationally restricted and evolutionarily conserved. Nature Struct. Biol. 6 (1999) 1010-1016
66. Gunasekaran K., Eyles S.J., Hagler A.T., and Gierasch L.M. Keeping it in the family: folding studies of related proteins. Curr. Opin. Struct. Biol. 11 (2001) 83-93
67. Hollien J., and Marqusee S. Comparison of the folding processes of T. thermophilus and E. coli ribonucleases H. J. Mol. Biol. 316 (2002) 327-340
68. Vallee-Belisle A., Turcotte J.F., and Michnick S.W. raf RBD and ubiquitin proteins share similar folds, folding rates and mechanisms despite having unrelated amino acid sequences. Biochemistry 43 (2004) 8447-8458
69. Truhlar S.M. Decoupled Folding and Functional Landscapes Allow alpha-Lytic Protease and Streptomyces griseus Protease B to Develop Novel Native-State Properties (2004), University of California, San Francsico
70. Derman A.I., and Agard D.A. Two energetically disparate folding pathways of alpha-lytic protease share a single transition state. Nature Struct. Biol. 7 (2000) 394-397
71. Lejbkowicz F., Kudinsky R., Samet L., Belavsky L., Barzilai M., and Predescu S. Identification of Nocardiopsis dassonvillei in a blood sample from a child. Am. J. Infect. Dis. 1 (2005) 1-4
72. Otwinowski Z.M.W. Processing of X-ray diffraction data collected in oscillation mode. In: Carter C.W.S., and Sweet R.M. (Eds). Methods in Enzymology vol. 276 (1997), Academic Press, New York 307-326
73. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D Biol. Crystallog. 54 (1998) 905-921
74. Jones T.A., Bergdoll M., and Kjeldgaard M. O: a macromolecular modeling environment. In: Bugg C.E.S. (Ed). Crystallographic and Modeling Methods in Molecular Design (1990), Springer-Verlag, New York 189-195
75. Laskowski R.A., Macarthur M.W., Moss D.S., and Thornton J.M. Procheck-A program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26 (1993) 283-291
76. Shindyalov I.N., and Bourne P.E. Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Protein Eng. 11 (1998) 739-747
77. DeLano W.L. The PyMOL Molecular Graphics System (2002), DeLano Scientific, San Carlos, CA
78. Potterton E., McNicholas S., Krissinel E., Cowtan K., and Noble M. The CCP4 molecular-graphics project. Acta Crystallog. sect. D Biol. Crystallog. 58 (2002) 1955-1957
79. Potterton L., McNicholas S., Krissinel E., Gruber J., Cowtan K., Emsley P., et al. Developments in the CCP4 molecular-graphics project. Acta Crystallog. sect. D Biol. Crystallog. 60 (2004) 2288-2294