Residue determinants and sequence analysis of cold-adapted trypsins

Extremophiles

Volumn 3, Issue 3, 1999, Pages 205-219

  Schrøder Leiros, Hanna Kirsti ^a   Willassen, Nils Peder ^a   Smalås, Arne O ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

Author keywords

Cold adaptation; Psychrophilicity; Residue determinants; Sequence comparison; Trypsin

Indexed keywords

AMINO ACID SEQUENCE; CARBOXY TERMINAL SEQUENCE; ENZYME ANALYSIS; HYDROPHOBICITY; ISOLEUCINE; LEUCINE; PROTEIN STABILITY; TRYPSIN; VALINE;

AMINO ACID SEQUENCE; ANIMALS; ARGININE; COLD; HUMANS; METHIONINE; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE HOMOLOGY, AMINO ACID; TRYPSIN;

EID: 0344549848     PISSN: 14310651     EISSN: None     Source Type: Journal    
DOI: 10.1007/s007920050118     Document Type: Article

References (101)

1. Aghajari N, Feller G, Gerday C, Haser R (1998) Crystal structures of the psychrophilic α-amylase from Alteromonas haloplanctis in its native form and complexed with an inhibitor. Protein Sci 7:564-572
2. Aittaleb M, Hubner R, Lamotte-Brasseur J, Gerday C (1997) Cold adaptation parameters derived from cDNA sequencing and molecular modelling of elastase from Antarctic fish Notothenia neglecta. Protein Eng 10:475-477
3. Alvarez M, Zeelen JP, Mainfroid V, Rentier-Delrue F, Martial JA, Wyns L, Wierenga RK, Maes D (1998) Triose-phosphate isomerase (TIM) of the psychrophilic bacterium Vibrio marinus. Kinetic and structural properties. J Biol Chem 273:2199-2206
4. Arpigny JL, Feller G, Davail S, Genicot S, Narinx E, Zekhnini Z, Gerday C (1994) Molecular adaptations of enzymes from thermophilic and psychrophilic organisms. In: Gilles R (ed) Advances in comparative and environmental physiology, vol 20. Springer, Berlin Heidelberg New York, pp 269-295
5. Arpigny JL, Lamotte J, Gerday C (1997) Molecular adaptation to cold of an Antarctic bacterial lipase. J Mol Catal B 3:29-35
6. Ásgeirsson B, Fox JW, Bjarnason JB (1989) Purification and characterization of trypsin from the poikilotherm Gadus morhua. Eur J Biochem 180:85-94
7. Barrick D, Hughson FM, Baldwin RL (1994) Molecular mechanisms of acid denaturation. The role of histidine residues in the partial unfolding of apomyoglobin. J Mol Biol 237:588-601
8. Bartunik HD, Summers LJ, Bartsch HH (1989) Crystal structure of bovine β-trypsin at 1.5 Å resolution in a crystal form with low molecular packing density. Active site geometry, ion pairs and solvent structure. J Mol Biol 210:813-828
9. Berglund GI, Smalås AO, Hordvik A, Willassen NP (1995a) Structure of anionic salmon trypsin in a second crystal form. Acta Crystallogr D 51:725-730
10. Berglund GI, Willassen NP, Hordvik A, Smalås AO (1995b) Structure of native pancreatic elastase from North Atlantic salmon at 1.61 Å resolution. Acta Crystallogr D 51:925-937
11. Britton KL, Baker PJ, Borges KM, Engel PC, Pasquo A, Rice DW, Robb FT, Scandurra R, Stillman TJ, Yip KS (1995) Insights into thermal stability from a comparison of the glutamate dehydrogenases from Pyrococcus furiosus and Thermococcus litoralis. Eur J Biochem 229:688-695
12. Cohen T, Gertler A, Birk Y (1981a) Pancreatic proteolytic enzymes from carp (Cyprinus carpio)-I. Purification and physical properties of trypsin, chymotrypsin, elastase and carboxypeptidase B. Comp Biochem Physiol B 69:639-646
13. Cohen T, Gertler A, Birk Y (1981b) Pancreatic proteolytic enzymes from carp (Cyprinus carpio)-II. Kinetic properties and inhibition studies of trypsin, chymotrypsin, and elastase. Comp Biochem Physiol B 69:647-653
14. Craik CS, Choo QL, Swift GH, Quinto C, MacDonald RJ, Rutter WJ (1984) Structure of two related rat pancreatic trypsin genes. J Biol Chem 259:14255-14264
15. Davail S, Feller G, Narinx E, Gerday C (1994) Cold adaptation of proteins. Purification, characterization, and sequence of the heatlabile subtilisin from the Antarctic psychrophile Bacillus TA41. J Biol Chem 269:17448-17453
16. Delboni LF, Mande SC, Rentier-Delrue F, Mainfroid V, Turley S, Vellieux FM, Martial JA, Hol WG (1995) Crystal structure of recombinant triosephosphate isomerase from Bacillus stearothermophilus. An analysis of potential thermostability factors in six isomerases with known three-dimensional structures points to the importance of hydrophobic interactions. Protein Sci 4:2594-2604
17. Earnest T, Fauman E, Craik CS, Stroud R (1991) 1.59 Å structure of trypsin at 120 K: comparison of low temperature and room temperature structures. Proteins 10:171-187
18. Eijsink VG, Veltman OR, Aukema W, Vriend G, Venema G (1995) Structural determinants of the stability of thermolysin-like proteinases. Nat Struct Biol 2:374-379
19. Emi M, Nakamura Y, Ogawa M, Yamamoto T, Nishide T, Mori T, Matsubara K (1986) Cloning, characterization and nucleotide sequences of two cDNAs encoding human pancreatic trypsinogens. Gene 41:305-310
20. Fehlhammer H, Bode W (1975) The refined crystal structure of bovine β-trypsin at 1.8 Å resolution. I. Crystallization, data collection and application of Patterson search techniques. J Mol Biol 93:683-692
21. Feller G, Arpigny JL, Narnix E, Garday C (1997) Molecular adaptations of enzymes from psychrophilic organisms. Comp Biochem Physiol A 118:495-499
22. Feller G, Gerday C (1997) Psychrophilic enzymes: molecular basis of cold adaptation. Cell Mol Life Sci 53:830-841
23. Feller G, Lonhienne T, Deroanne C, Libioulle C, VanBeeumen J, Gerday C (1992) Purification, characterization, and nucleotide sequence of the thermolabile α-amylase from the Antarctic psychrotroph Alteromonas haloplanctis A23. J Biol Chem 267:5217-5221
24. Feller G, Narinx E, Arpigny JL, Aittaleb M, Baise E, Genicot S, Gerday C (1996) Enzymes from psychrophilic organisms. FEMS Microbiol Rev 18:189-202
25. Feller G, Payan F, Theys F, Qian M, Haser R, Gerday C (1994) Stability and structural analysis of α-amylase from the Antarctic psychrophile Alteromonas haloplanctis A23. Eur J Biochem 222: 441-447
26. Fersht AR, Serrano L (1993) Principles of protein stability derived from protein engineering experiments. Curr Opin Struct Biol 3:75-83
27. Fletcher TS, Alhadeff M, Craik CS, Largman C (1987) Isolation and characterization of a cDNA encoding rat cationic trypsinogen. Biochemistry 26:3081-3086
28. Gaboriaud C, Serre L, Guy-Crotte O, Forest E, Fontecilla-Camps JC (1996) Crystal structure of human trypsin 1: unexpected phosphorylation of Tyr151. J Mol Biol 259:995-1010
29. Gassner NC, Baase WA, Matthews BW (1996) A test of the "jigsaw puzzle" model for protein folding by multiple methionine substitutions within the core of T4 lysozyme. Proc Natl Acad Sci USA 93:12155-12158
30. Genicot S, Feller G, Gerday C (1988) Trypsin from antarctic fish (Papanotothenia magellanica forster) as compared with trout (Salmo gairdneri) trypsin. Comp Biochem Physiol B 90:601-609
31. Genicot S, Rentier-Delrue F, Edwards D, VanBeeumen J, Gerday C (1996) Trypsin and trypsinogen from an Antarctic fish molecular basis of cold adaptation. Biochim Biophys Acta 1298:45-57
32. Gerday C, Aittaleb M, Arpigny JL, Baise E, Chessa JP, Garsoux G, Petrescu I, Feller G (1997) Psychrophilic enzymes: a thermodynamic challenge. Biochim Biophys Acta 1342:119-131
33. Gerike U, Danson MJ, Russell NJ, Hough DW (1997) Sequencing and expression of the gene encoding a cold-active citrate synthase from an Antarctic bacterium, strain DS2-3R. Eur J Biochem 248:49-57
34. Gilberg A, Øverbø K (1990) Purification and characterization of pancreatic elastase from Atlantic cod (Gadus morhua). Comp Biochem Physiol B 97:775-782
35. Gudmundsdóttir A, Gudmundsdóttir E, Óskarsson S, Bjarnason JB, Eakin AK, Craik CS (1993) Isolation and characterization of cDNAs from Atlantic cod encoding two different forms of trypsinogen. Eur J Biochem 217:1091-1097
36. Gudmundsdóttir A, Óskarsson S, Eakin AE, Craik CS, Bjarnason JB (1994) Atlantic cod cDNA encoding a psychrophilic chymotrypsinogen. Biochim Biophys Acta 1219:211-214
37. Gudmundsdóttir E, Spilliaert R, Yang Q, Craik CS, Bjarnason JB, Gudmundsdóttir A (1996) Isolation and characterization of two cDNAs from Atlantic cod encoding two distinct psychrophilic elastases. Comp Biochem Physiol B 113:795-801
38. Haney P, Konisky J, Koretke KK, Luthey-Schulten Z, Wolynes PG (1997) Structural basis for thermostability and identification of potential active site residues for adenylate kinases from the archaeal genus Methanococcus. Proteins 28:117-130
39. Hartley BS, Kauffman DL (1966) Corrections to the amino acid sequence of bovine chymotrypsinogen A. Biochem J 101:229-231
40. Hedstrom L, Farr-Jones S, Kettner CA, Rutter WJ (1994a) Converting trypsin to chymotrypsin: ground-state binding does not determine substrate specificity. Biochemistry 33:8764-8769
41. Hedstrom L, Perona JJ, Rutter WJ (1994b) Converting trypsin to chymotrypsin: residue 172 is a substrate specificity determinant. Biochemistry 33:8757-8763
42. Hedstrom L, Szilagy L, Rutter WJ (1992) Converting trypsin to chymotrypsin: the role of surface loops. Science 255:1249-1253
43. Heimstad ES (1996) Structural and dynamical comparison of two homologous enzymes. Exploring the protein dynamics of salmon and bovine trypsin with molecular dynamics simulations. Doctoral thesis. Institute of Mathematical and Physical Sciences, Department of Chemistry, University of Tromsø, Norway
44. Heimstad ES, Hansen LK, Smalås AO (1995) Comparative molecular dynamics simulation studies of salmon and bovine trypsins in aqueous solution. Protein Eng 8:379-388
45. Helland R, Leiros I, Willassen NP, Berglund GI, Smalås AO (1998) The crystal structure of anionic salmon trypsin in complex with bovine pancreatic trypsin inhibitor. Eur J Biochem 256:317-324
46. Hermodson MA, Ericsson LH, Neurath H, Walsh KA (1973) Determination of the amino acid sequence of porcine trypsin by sequenator analysis. Biochemistry 12:3146-3153
47. Hjelmeland K, Raa J (1982) Characteristics of two trypsin type isozymes isolated from the arctic fish capelin (Mallotus villosus). Comp Biochem Physiol B 71:557-562
48. Huang Q, Liu S, Tang Y (1993) Refined 1.6 Å resolution crystal structure of the complex formed between porcine β-trypsin and MCTI-A, a trypsin inhibitor of the squash family. Detailed comparison with bovine β-trypsin and its complex. J Mol Biol 229:1022-1036
49. Ishii A, Suzuki M, Sahara T, Takada Y, Sasaki S, Fukunaga N (1993) Genes encoding two isocitrate dehydrogenase isozymes of a psychrophilic bacterium, Vibrio sp. strain ABE-1. J Bacteriol 175:6873-6880
50. Jaenicke R (1990) Protein structure and function at low temperatures. Philos Trans R Soc Lond B Biol Sci 326:535-551
51. Jaenicke R (1991) Protein stability and molecular adaptation to extreme conditions. Eur J Biochem 202:715-728
52. Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577-2637
53. Kalác J (1976) Comparative study of mackerel (Scomber scombrus) anionic trypsin and bovine trypsin. Biologia (Bratisl) 31:973-982
54. Kang J, Wiegand U, Müller-Hill B (1992) Identification of cDNAs encoding two novel rat pancreatic serine proteases. Gene 110:181-187
55. Karlsen S, Hough E, Olsen RL (1998) The crystal structure and proposed amino acid sequence of a pepsin from Atlantic cod (Gadus morhua). Acta Crystallogr D 54:32-46
56. Kimland M, Russick C, Marks WH, Borgstrom A (1989) Immunoreactive anionic and cationic trypsin in human serum. Clin Chim Acta 184:31-46
57. Kozlovskaya EP, Elyakova LA (1974) Purification and properties of trypsin-like enzymes from the starfish Lysastrosoma anthosticta. Biochim Biophys Acta 371:63-70
58. Kristjansson MM, Ásgeirsson B, Bjarnason JB (1997) Serine proteinases from cold-adapted organisms. Adv Exp Med Biol 415:27-46
59. Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105-132
60. Le Huerou I, Wicker C, Guilloteau P, Toullec R, Puigserver A (1990) Isolation and nucleotide sequence of cDNA clone for bovine pancreatic anionic trypsinogen. Structural identity within the trypsin family. Eur J Biochem 193:767-773
61. Leth-Larsen R, Ásgeirsson B, Thorolfsson M, Norregaard-Madsen M, Hojrup P (1996) Structure of chymotrypsin variant B from Atlantic cod, Gadus morhua. Biochim Biophys Acta 1297:49-56
62. Lütcke H, Rausch U, Vasiloudes P, Scheele GA, Kern HF (1989) A fourth trypsinogen (P23) in the rat pancreas induced by CCK. Nucleic Acids Res 17:6736-6736
63. MacDonald RJ, Stary SJ, Swift GH (1982) Two similar but nonallelic rat pancreatic trypsinogens. Nucleotide sequences of the cloned cDNAs. J Biol Chem 257:9724-9732
64. Malakauskas SM, Mayo SL (1998) Design, structure and stability of a hyperthermophilic protein variant. Nat Struct Biol 5:470-475
65. Male R, Lorens JB, Smalås AO, Torrissen KR (1995) Molecular cloning and characterization of anionic and cationic variants of trypsin from Atlantic salmon. Eur J Biochem 232:677-685
66. Marquart M, Walter J, Deisenhofer J, Bode W, Huber R (1983) The geometry of the reactive site and of the peptide groups in trypsin. trypsinogen and its complexes with inhibitors. Acta Crystallogr B 39:480-490
67. Marshall CJ (1997) Cold-adapted enzymes. Trends Biotechnol 15:359-364
68. Martínez A, Olsen RL, Serra JL (1988) Purification and characterization of two trypsin-like enzymes from the digestive tract of anchovy Engraulis encrasicholus. Comp Biochem Physiol B 91:677-684
69. Mikes O, Holeysovsky V, Tomasek V, Sorm F (1966) Covalent structure of bovine trypsinogen. The position of the remaining amides. Biochem Biophys Res Commun 24:346-352
70. Mine S, Ueda T, Hashimoto Y, Imoto T (1997) Improvement of the refolding yield and solubility of hen egg-white lysozyme by altering the Met residue attached to its N-terminus to Ser. Protein Eng 10:1333-1338
71. Mrabet NT, van den Broeck A, van den Brande I, Stanssens P, Laroche Y, Lambeir AM, Matthijssens G, Jenkins J, Chiadmi M, van Tilbeurgh H, Rey F, Janini J, Quax WJ, Lasters I, de Maeyer M, Wodak SJ (1992) Arginine residues as stabilizing elements in proteins. Biochemistry 31:2239-2253
72. Muñoz V, Serrano L (1995) Elucidating the folding problem of helical peptides using empirical parameters. II. Helix macrodipole effects and rational modification of the helical content of natural peptides. J Mol Biol 245:275-296
73. Osnes KK, Mohr V (1985) On the purification and characterization of three anionic, serine-type peptide hydrolases from Antarctic krill Euphausia superba. Comp Biochem Physiol B 82:607-619
74. Outzen H, Berglund GI, Smalås AO, Willassen NP (1996) Temperature and pH sensitivity of trypsins from Atlantic salmon (Salmo salar) in comparison with bovine and porcine trypsin. Comp Biochem Physiol B 115:33-45
75. Pinsky SD, LaForge KS, Scheele G (1985) Differential regulation of trypsinogen mRNA translation: full-length mRNA sequences encoding two oppositely charged trypsinogen isoenzymes in the dog pancreas. Mol Cell Biol 5:2669-2676
76. Raae AJ, Walther BT (1989) Purification and characterization of chymotrypsin, trypsin and elastase like proteinases from cod (Gadus morhua L.). Comp Biochem Physiol B 93:317-324
77. Read RJ, James MN (1988) Refined crystal structure of Streptomyces griseus trypsin at 1.7 Å resolution. J Mol Biol 200:523-551
78. Roach JC, Wang K, Gan L, Hood L (1997) The molecular evolution of the vertebrate trypsinogens. J Mol Evol 45:640-652
79. Rypniewski WR, Dambmann C, von der Osten C, Dauter M, Wilson KS (1995) Structure of inhibited trypsin from Fusarium oxysporum at 1.55 Å. Acta Crystallogr D 51:73-84
80. Rypniewski WR, Perrakis A, Vorgias CE, Wilson KS (1994) Evolutionary divergence and conservation of trypsin. Protein Eng 7:57-64
81. Schrøder H-K, Willassen NP, Smalås AO (1998) Structure of a non-psychrophilic trypsin from a cold-adapted fish species. Acta Crystallogr D 54:780-798
82. Serrano L, Day AG, Fersht AR (1993) Step-wise mutation of barnase to binase. A procedure for engineering increased stability of proteins and an experimental analysis of the evolution of protein stability. J Mol Biol 233:305-312
83. Shi YB, Brown DD (1990) Developmental and thyroid hormone-dependent regulation of pancreatic genes in Xenopus laevis. Genes Dev 4:1107-1113
84. Simpson BK, Haard NF (1984a) Purification and characterization of trypsin from the Greenland cod (Gadus ogac). 1. Kinetic and thermodynamic characteristics. Can J Biochem Cell Biol 62:894-900
85. Simpson BK, Haard NF (1984b) Trypsin from Greenland cod, Gadus ogac. Isolation and comparative properties. Comp Biochem Physiol B 79:613-622
86. Smalås AO, Heimstad ES, Hordvik A, Willassen NP, Male R (1994) Cold adaption of enzymes: structural comparison between salmon and bovine trypsins. Proteins 20:149-166
87. Stevenson BJ, Hagenbuchle O, Wellauer PK (1986) Sequence organisation and transcriptional regulation of the mouse elastase II and trypsin genes. Nucleic Acids Res 14:8307-8330
88. Tani T, Kawashima I, Mita K, Takiguchi Y (1990) Nucleotide sequence of the human pancreatic trypsinogen III cDNA. Nucleic Acids Res 18:1631-1631
89. Tanji M, Yakabe E, Kageyama T, Takahashi K (1996) The primary structure of the major pepsinogen from the gastric mucosa of tuna stomach. J Biochem (Tokyo) 120:647-656
90. Tanner JJ, Hecht RM, Krause KL (1996) Determinants of enzyme thermostability observed in the molecular structure of Thermus aquaticus D-glyceraldehyde-3-phosphate dehydrogenase at 2.5 Å resolution. Biochemistry 35:2597-2609
91. Titani K, Ericsson LH, Neurath H, Walsh KA (1975) Amino acid sequence of dogfish trypsin. Biochemistry 14:1358-1366
92. Uchida N, Tsukayama K, Nishide E (1984) Properties of two main anionic trypsins from the pyloric caeca of chum salmon. Bull Jpn Soc Sci Fish 50:313-321
93. Voytek P, Gjessing EC (1971) Studies of an anionic trypsinogen and its active enzyme from porcine pancreas. J Biol Chem 246:508-516
94. Wallon G, Lovett ST, Magyar C, Svingor A, Szilagyi A, Zavodszky P, Ringe D, Petsko GA (1997) Sequence and homology model of 3-isopropylmalate dehydrogenase from the psychrotrophic bacterium Vibrio sp. 15 suggest reasons for thermal instability. Protein Eng 10:665-672
95. Wang K, Gan L, Lee I, Hood L (1995) Isolation and characterization of the chicken trypsinogen gene family. Biochem J 307:471-479
96. Watanabe K, Masuda T, Ohashi H, Mihara H, Suzuki Y (1994) Multiple proline substitutions cumulatively thermostabilize Bacillus cereus ATCC7064 oligo-1,6-glucosidase. Irrefragable proof supporting the proline rule. Eur J Biochem 226:277-283
97. Winter WP, Neurath H (1970) Purification and properties of a trypsin-like enzyme from the starfish Evasterias trochelii. Biochemistry 9: 4673-4679
98. Yip KS, Stillman TJ, Britton KL, Artymiuk PJ, Baker PJ, Sedelnikova SE, Engel PC, Pasquo A, Chiaraluce R, Consalvi V (1995) The structure of Pyrococcus furiosus glutamate dehydrogenase reveals a key role for ion-pair networks in maintaining enzyme stability at extreme temperatures. Structure (Lond) 3:1147-1158
99. Yoshinaka R, Sato M, Suzuki T, Ikeda S (1983a) Enzymatic characterization of anionic trypsin of the catfish (Parasilurus asotus). Comp Biochem Physiol B 77:1-6
100. Yoshinaka R, Suzuki T, Sato M, Ikeda S (1983b) Purification and some properties of anionic trypsin from the catfish pancreas. Bull Jpn Soc Sci Fish 49:207-212
101. Zhang XJ, Baase WA, Shoichet BK, Wilson KP, Matthews BW (1995) Enhancement of protein stability by the combination of point mutations in T4 lysozyme is additive. Protein Eng 8:1017-1022