Neutron and X-ray crystallographic analysis of Achromobacter protease I at pD 8.0: Protonation states and hydration structure in the free-form

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1834, Issue 8, 2013, Pages 1642-1647

  Ohnishi, Yuki ^a   Yamada, Taro ^a   Kurihara, Kazuo ^b   Tanaka, Ichiro ^a   Sakiyama, Fumio ^c   Masaki, Takeharu ^a   Niimura, Nobuo ^a  

^a IBARAKI UNIVERSITY   (Japan)

^b JAPAN ATOMIC ENERGY AGENCY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

Achromobacter protease I; Protonation states; Reaction mechanism; Serine protease; Single crystal X ray neutron diffraction

Indexed keywords

ACHROMOBACTER PROTEASE I; BRINASE; CALCIUM; HISTIDINE; HYDROGEN; HYDROXYL GROUP; IMIDAZOLE; LYSINE; SERINE PROTEINASE; UNCLASSIFIED DRUG; APROTININ; LYSYL ENDOPEPTIDASE; PROTON; TRYPSIN; WATER;

ACHROMOBACTER; ACIDITY; ARTICLE; CHEMICAL STRUCTURE; CRYSTAL STRUCTURE; HYDRATION; HYDROGEN BOND; HYPOTHESIS; NEUTRON DIFFRACTION; NEUTRON SCATTERING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DATA BANK; PROTON TRANSPORT; X RAY CRYSTALLOGRAPHY; X RAY DIFFRACTION; ANIMAL; BINDING SITE; CATALYSIS; CATTLE; CHEMISTRY; ENZYME ACTIVE SITE; METABOLISM; PROTEIN CONFORMATION;

ACHROMOBACTER; BOVINAE;

ANIMALS; APROTININ; BINDING SITES; CATALYSIS; CATALYTIC DOMAIN; CATTLE; CRYSTALLOGRAPHY, X-RAY; HYDROGEN BONDING; MODELS, MOLECULAR; NEUTRON DIFFRACTION; PROTEIN CONFORMATION; PROTONS; SERINE ENDOPEPTIDASES; TRYPSIN; WATER;

EID: 84879244792     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2013.05.012     Document Type: Article

References (27)

1. T. Masaki, M. Tanabe, K. Nakamura, M. Soejima, Studies on a new proteolytic enzyme from Achromobacter lyticus M497-1. I. Purification and some enzymatic properties, Biochim. Biophys. Acta 660 (1981) 44-50. (Pubitemid 11045613)
2. F. Sakiyama, T. Masaki, Lysyl endopeptidase of Achromobacter lyticus, Methods Enzymol. 244 (1994) 126-137.
3. T. Masaki, T. Fujihashi, K. Nakamura, M. Soejima, Studies on a new proteolytic enzyme from Achromobacter lyticus M497-1. II. Purification and some enzymatic properties, Biochim. Biophys. Acta 660 (1981) 51-55. (Pubitemid 11045614)
4. S. Tsunasawa, T. Masaki, M. Hirose, M. Soejima, F. Sakiyama, The primary structure and structural characteristics of Achromobacter lyticus protease I, a lysine-specific serine protease, J. Biol. Chem. 264 (1989) 3832-3839.
5. S. Norioka, S. Ohta, T. Ohara, S.I. Lim, F. Sakiyama, Identification of three catalytic triad constituents and Asp-225 essential for function of lysine-specific serine protease, Achromobacter protease I, J. Biol. Chem. 269 (1994) 17025-17029. (Pubitemid 24204017)
6. K. Shiraki, F. Sakiyama, Histidine 210 mutant of a trypsin-type Achromobacter protease I shows broad optimum pH range, J. Biosci. Bioeng. 93 (2002) 331-333. (Pubitemid 34539148)
7. K. Shiraki, S. Norioka, S. Li, F. Sakiyama, Contribution of an imidazole-indole stack to high catalytic potency of a lysine-specific serine protease, Achromobacter protease I, J. Biochem. 131 (2002) 213-218. (Pubitemid 34194356)
8. K. Shiraki, S. Norioka, S. Li, K. Yokota, F. Sakiyama, Electrostatic role of aromatic ring stacking in the pH-sensitive modulation of a chymotrypsin-type serine protease, Achromobacter protease I, Eur. J. Biochem. 269 (2002) 4152-4158. (Pubitemid 34994910)
9. N. Niimura, A. Podjarny, Hydrogen, Protons, and Hydration in Bio-macromolecules, IUCr Monographs on Crystallography 25, Oxford University Press, 2011, ISBN 978-0-19-957886-3. 1-233.
10. K. Kawamura, T. Yamada, K. Kurihara, T. Tamada, R. Kuroki, I. Tanaka, H. Takahashi, N. Niimura, X-ray and neutron protein crystallographic analysis of the trypsin-BPTI complex, Acta Crystallogr. D67 (2011) 140-148.
11. A.A. Kossiakoff, Use of the neutron diffraction-H/D exchange technique to determine the conformational dynamics of trypsin, Basic Life Sci. 27 (1984) 281-304.
12. A.A. Kossiakoff, S.A. Spencer, Direct determination of the protonation states of aspartic acid-102 and histidine-57 in the tetrahedral intermediate of the serine proteases: neutron structure of trypsin, Biochemistry 20 (1981) 6462-6474.
13. A.A. Kossiakoff, S.A. Spencer, Neutron diffraction identifies His 57 as the catalytic base in trypsin, Nature 288 (1980) 414-416.
14. T. Tamada, T. Kinoshita, K. Kurihara, M. Adachi, T. Ohhara, K. Imai, R. Kuroki, T. Tada, Combined high-resolution neutron and x-ray analysis of inhibited elastase confirms the active-site oxyanion hole but rules against a low-barrier hydrogen bond, J. Am. Chem. Soc. 131 (2009) 11033-11040.
15. P.F. Glasoe, F.A. Long, Use of glass electrodes to measure acidities in deuterium oxide, J. Phys. Chem. 64 (1960) 188-190.
16. Z. Otwinowski, W. Minor, Processing of X-ray diffraction data collected in oscillation mode, in: C.W. Carter Jr., R.M. Sweet (Eds.), Methods in enzymology, Macromolecu-lar Crystallography, part A, vol. 276, Academic Press, New York, 1997, pp. 307-326. (Pubitemid 27085611)
17. N. Niimura, S. Arai, K. Kurihara, T. Chatake, I. Tanaka, R. Bau, Recent results on hydrogen and hydration in biology studied by neutron macromolecular crystallography, Cell. Mol. Life Sci. 63 (2006) 285-300. (Pubitemid 43202311)
18. N. Niimura, Y. Karasawa, I. Tanaka, J. Miyahara, K. Akahashi, H. Saito, S. Koizumi, M. Hidaka, An imaging plate neutron detector, Nucl. Instrum. Meth. A349 (1994) 521-525.
19. K. Kurihara, I. Tanaka, M.M. Refai, A. Ostermann, N. Niimura, A new neutron single-crystal diffractometer dedicated for biological macromolecules (BIX-4), J. Synchrotron Radiat. 11 (2004) 68-71. (Pubitemid 40085637)
20. Y. Ohnishi, T. Masaki, T. Yamada, K. Kurihara, I. Tanaka, N. Niimura, A preliminary neutron diffraction analysis of Achromobacter protease I, J. Phys. Conf. Ser. 251 (2010) 012032.
21. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.-W. Hung, G.J. Kapral, R.W. Grosse-Kunstleve, A.J. McCoy, N.W. Moriarty, R. Oeffner, R.J. Read, D.C. Richardson, J.S. Richardson, T.C. Terwilliger, P.H. Zwart, PHENIX: a comprehensive Python-based system for macromolecular structure solution, Acta Crystallogr. D66 (2010) 213-221.
22. P. Emsley, B. Lohkamp, W.G. Scott, K. Cowtan, Features and development of Coot, Acta Crystallogr. D66 (2010) 486-501.
23. T. Chatake, A. Ostermann, K. Kurihara, F.G. Parak, N. Niimura, Hydration in proteins observed by high-resolution neutron crystallography, Proteins 50 (2003) 516-523. (Pubitemid 36158463)
24. The PyMOL Molecular Graphics System, Version 1.2r3pre, Schrödinger, LLC, 2009.
25. J.L. Markley, W.M. Westler, Protonation-state dependence of hydrogen bond strengths and exchange rates in a serine protease catalytic triad: bovine chymo-trypsinogen A, Biochemistry 35 (1996) 11092-11097. (Pubitemid 26298743)
26. M.E. McGrath, J.R. Vásquez, C.S. Craik, A.S. Yang, B. Honig, R.J. Fletterick, Perturbing the polar environment of Asp102 in trypsin: consequences of replacing conserved Ser214, Biochemistry 31 (1992) 3059-3064.
27. 214 is crucial for substrate binding to serine proteases, J. Biol. Chem. 277 (2002) 40260-40264. (Pubitemid 35215597)