The three-dimensional structure at 2.4 Å resolution of glycosylated proteinase A from the lysosome-like vacuole of Saccharomyces cerevisiae

Journal of Molecular Biology

Volumn 267, Issue 4, 1997, Pages 899-915

  Aguilar, C F ^a   Cronin, N B ^a   Badasso, M ^a   Dreyer, T ^b   Newman, M P ^a   Cooper, J B ^a   Hoover, D J ^c   Wood, S P ^c   Johnson, M S ^a   Blundell, T L ^a  

^a Birkbeck College   (United Kingdom)

^b CARLSBERG LABORATORY   (Denmark)

^c PFIZER INC   (United States)

Author keywords

Active site; Aspartic proteinase; Diflurostatone inhibitor; Proteinase A; Vacuole

Indexed keywords

ASPARTIC PROTEINASE; CATHEPSIN D; OLIGOSACCHARIDE; PEPSIN A;

ARTICLE; CELL VACUOLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME CONFORMATION; ENZYME STRUCTURE; HYDROGEN BOND; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE;

EID: 0031564660     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0880     Document Type: Article

References (81)

1. Abad-Zapatero C., Rydel T. J., Erickson J. Revised 2.3 Å structure of porcine pepsin: evidence for a flexible subdomain. Proteins: Struct. Funct. Genet. 8:1990;62-81.
2. Abad-Zapatero C., Rydel T. J., Neidhart D. J., Luly J., Erickson J. W. Inhibitor binding induces structural changes in porcine pepsin. Advan. Exp. Med. Biol. 306:1991;9-21.
3. Abad-Zapatero C., Goldman R., Muchmore S. W., Hutchins C., Stewart K., Navaza J., Payne C. D., Ray T. L. Structure of a secreted aspartic protease from C. albicans complexed with a potent inhibitor: Implications for the design of antifungal agents. Protein Sci. 5:1996;640-652.
4. Andreeva N. S., Zdanov A. S., Gustchina A. E., Fedorov A. A. Structure of ethanol-inhibited porcine pepsin at 2Å resolution and binding of the methyl ester of phenylalanyl-diiodotyrosine to the enzyme. J. Mol. Chem. 259:1984;11353-11365.
5. Badasso M., Wood S. P., Aguilar C. F., Cooper J. B., Blundell T. L. Crystallization and preliminary crystallographic characterization of aspartic proteinase-A from baker's yeast and its complexes with inhibitors. J. Mol. Biol. 232:1993;701-703.
6. Bailey D., Cooper J. B., Veerapandian B., Blundell T. L., Atrash B., Jones D. M., Szelke M. X-ray-crystallographic studies of complexes of pepsatin A and a statine-containing human renin inhibitor with endothiapepsin. Biochem. J. 289:1993;363-371.
7. Baker E. N., Hubard R. E. Hydrogen bonding in globular proteins. Prog. Biophys. Mol. Biol. 44:1984;97-179.
8. Baldwin E. T., Bhat T. N., Gulnik S., Hosur M. V., Sowder R. C., Cachau R. E., Collins J., Silva A. M., Erickson J. W. Crystal structures of native and inhibited forms of human cathepsin D: implications for lysosomal targeting and drug design. Proc. Natl Acad. Sci., USA. 90:1993;6796-6800.
9. Baranski T. J., Faust P. L., Kornfeld S. Generation of a lysosomal-enzyme targeting signal in the secretory protein pepsinogen. Cell. 63:1990;281-291.
10. Blundell T. L., Jenkins J. A., Sewell B. T., Pearl L. H., Cooper J. B., Tickle I. J., Veerapandian B., Wood S. P. X-ray analyses of aspartic proteinases. I. The three-dimensional structure at 2.1 Å resolution of endothiapepsin. J. Mol. Biol. 214:1990;199-222.
11. Boger J. Renin inhibitors. Design of angiotensinogen transition-state analogs containing statine. Aspartic Proteinases and their Inhibitors. 1985;de Gruyter, Berlin.
12. Bott R., Subramanian E., Davies D. Three-dimensional structure of the complex of the Rhizopus chinensis carboxyl proteinase and pepstatin at 2.5 Å resolution. Biochemistry. 21:1982;6956-6962.
13. Brünger A. T. X-PLOR (Version 1.5) Manual. 1988;Yale University, New Haven.
14. Brünger A. T., Karplus M., Petsko G. A. Crystallographic refinement by simulated annealing: application to crambin. Acta Crystallog. sect. A. 45:1989;50-61.
15. CCP4. The SERC (UK) Collatorative Computing Project no. 4: A Suite of Programs for Protein Crystallography. 1979;distributed from Daresbury Laboratory, Warrington WA4 4AD.
16. Connolly M. L. Analytical molecular surface calculation. J. Appl. Crystallog. 16:1983;548-558.
17. Cooper J. B., Foundling S. I., Hemmings A., Blundell T. L., Jones D. M., Hallet A., Szelke M. The structure of a synthetic pepsin inhibitor complexed with endothiapepsin. Eur. J. Biochem. 169:1987a;215-221.
18. Cooper J. B., Foundling S. I., Blundell T. L., Arrowsmith R. J., Harris C. J., Champness J. N. A rational approach to the design of antihypertensives: X-ray studies of complexes between aspartic proteinases and aminoalcohol renin inhibitors. Leeming P. R. Topics in Medicinal Chemistry. 1987b;Royal Society of Chemistry, London.
19. Cooper J. B., Foundling S. I., Blundell T. L., Boger J., Jupp R. A., Kay J. X-ray studies of aspartic proteinase-statine inhibitor complexes. Biochemistry. 28:1989;8596-8603.
20. Cooper J. B., Khan G., Taylor G., Tickle I. J., Blundell T. L. X-ray analyses of aspartic proteinases. II. Three-dimensional structure of the hexagonal crystal form of porcine pepsin at 2.3 Å resolution. J. Mol. Biol. 214:1990;199-222.
21. Crowther R. A., Blow D. M. A. method for positioning a known molecule in an unknown crystal structure. Acta Crystallog. 23:1967;544-548.
22. Cutfield S. M., Dodson E. J., Anderson B. F., Moody P. C. E., Marshall C. J., Sullivan P. A., Cutfield J. F. The crystal structure of a major secreted aspartic proteinase from Candida albicans in complexes with two inhibitors. Structure. 3:1955;1261-1271.
23. Dealwis C. G., Frazao C., Badasso M., Cooper J. B., Tickle I. J., Driessen H., Blundell T. L., Murakami K., Miyazaki H., Sueiras-Diaz J., Jones D. M., Szelke M. X-ray analysis at 2.0Å resolution of mouse submaxillary renin complexed with a decapeptide inhibitor CH-66, based on the 4-16 fragment of rat angiotensinogen. J. Mol. Biol. 236:1994;342-360.
24. Dhanaraj V., Dealwis C. G., Frazao C., Badasso M., Sibanda B. L., Tickle I. J., Cooper J. B., Driessen H. P. C., Newman M., Aguilar C., Wood S. P., Blundell T. L., Hobart P. M., Geoghegan K. F., Ammirati M. J., Danley D. E., O'Connor B. A., Hoover D. J. X-ray analyses of peptide inhibitor complexes define the structural basis of specificity for human and mouse renins. Nature. 357:1992;466-472.
25. Dodson E. J. Molecular replacement: the method and its problems. Machin P. Molecular Replacement, Proceedings of the Daresbury Study Weekend. 1985;CCP4, Daresbury Laboratory, UK.
26. Dreyer T. Substrate specificity of proteinase A from Saccharomyces cerevisiae. Carlsberg Res. Commun. 54:1989;85-97.
27. Dreyer T., Halkier B., Svendsen I., Ottesen M. Primary structure of the aspartic proteinase A from Saccharomyces cerevisiae. Carlsberg Res. Commun. 51:1986;27-41.
28. Einspahr H. M. Protein-carbohydrate interactions in biological systems. Trans Am. Crystallog. Assoc. 25:1989;1-22.
29. Fearon K., Spaltenstein A., Hopkins P. B., Gelb M. H. Fluoroketone containing peptides as inhibitors of human renin. J. Med. Chem. 30:1987;1617-1622.
30. Feisenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 39:1985;783-791.
31. Foundling S. I., Cooper J. B., Watson J., Cleasby F. E., Pearl L. H., Sibanda B. L., Hemmings A., Wood S. P., Blundell T. L., Valler T. L., Kay J., Boger J., Dunn B. M., Leckie B. J., Jones D. M., Atrash B., Hallet A., Szelke M. High resolution X-ray analysis of renin inhibitor-aspartic proteinase complexes. Nature. 327:1987;349-352.
32. Fraser M. E., Strynadka N. C. J., Barttlet P. A., Hanson J. E., James M. N. G. Crystallographic analysis of transition-state mimics bound to penicillopepsin: phosphorus-containing peptide analogues. Biochemistry. 31:1992;5201-5214.
33. Gilliland G. L., Winbourne E. L., Nachman J., Wlodawer A. The three-dimensional structure of recombinant bovine chymosin at 2.3 Å resolution. Proteins: Struct. Funct. Genet. 8:1990;82-101.
34. Haneef I., Moss D. S., Stanford M. J., Borkakoti N. Restrained structure-factor least-squares refinement of protein structures using a vector processing computer. Acta Crystallog. sect. A. 41:1985;426-433.
35. Higashi T. The processing of diffraction data taken on a screenless Weissenberg camera for macromolecular crystallography. J. Appl. Crystallog. 22:1989;9-18.
36. Hoover D. J., Rosati R. L., Wester R. T. Norstatine and nor-cyclostatine polypeptides. US Patent 4 814 342, Example 8C. 1989.
37. James M. N. G., Sielecki A. R. Structure and refinement of penicillopepsin at 1.8 Å resolution. J. Mol. Biol. 163:1983;299-361.
38. James M. N. G., Sielecki A. R. Stereochemical analysis of peptide bond hydrolysis catalysed by the aspartic proteinase penicillo-pepsin. Biochemistry. 24:1985;3701-3713.
39. James M. N. G., Sielecki A. R. Molecular structure of an aspartic proteinase zymogen, porcine pepsinogen, at 1.8 Å resolution. Nature. 319:1986;33-38.
40. James M. N. G., Sielecki A. R., Salituro R., Rich D. H., Hoffman T. Conformational flexibility in the active site of aspartyl proteinases revealed by a pepstatin fragment binding to penicillopepsin. Proc. Natl Acad. Sci., USA. 79:1982;6137-6142.
41. James M. N. G., Sielecki A. R., Hayakawa K., Gelb M. H. Crystallographic analysis of transition-state mimics bound to penicillopepsin: difluorostatine- and difluorostatone-containing peptide. Biochemistry. 31:1992;3872-3886.
42. Johnson M. S., Šali A., Blundell T. L. Phylogenetic relationships from three-dimensional protein structures. Methods Enzymol. 183:1990a;670-690.
43. Johnson M. S., Sutcliffe M. J., Blundell T. L. Molecular anatomy: phyletic relationships derived from three-dimensional structures of proteins. J. Mol. Evol. 30:1990b;43-59.
44. Jones E. W. Genetic approaches to the study of protease function and proteolysis in Saccharomyces cerevisiae. Spencer J. F. T., Spencer D. M., Smith A. R. W. Yeast Genetics, Fundamental and Applied Aspects. 1983;Springer-Verlag, New York.
45. Jones T. A. A graphics model building and refinement system for macromolecules. J. Appl. Crystallog. 11:1978;268-272.
46. Kabsch W., Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 22:1983;2577-2637.
47. Klionsky D. J., Banta M. L., Emr S. D. Intracellular sorting and processing of a yeast vacuolar hydrolase: proteinase A propeptide contains vacuolar targeting information. Mol. Cell. Biol. 8:1988;2105-2116.
48. Kostka V. Aspartic Proteinases and their Inhibitors. 1985;de Gruyter, Berlin.
49. Laskowski R. A., MacArthur M. W., Moss D. S., Thornton J. M. PROCHECK (Version 2.0). 1992;University College, London.
50. Luzzatti V. Treatment of statistical errors in the determination of crystal structures. Acta Crystallog. 5:1952;802-810.
51. Matile P., Wiemken A. The vacuole as the lysosome of the yeast cell. Arch. Microbiol. 56:1967;148-155.
52. Messerschmidt A., Pflugrath J. W. Crystal orientation and X-ray pattern prediction routines for area-dectector diffractometer systems in macro-molecular crystallography. J. Appl. Crystallog. 20:1987;306-315.
53. Metcalf P., Fusek M. Two crystal structures for cathepsin D: the lysosomal targeting signal and active site. EMBO J. 12:1993;1293-1302.
54. Navaza J. AmoRe: an automated package for molecular replacement. Acta Crystallog. sect. A. 50:1994;588-591.
55. Newman M. P., Safro M., Frazao C., Khan G., Zdanov A., Tickle I. J., Blundell T. L., Andreeva N. Structure and refinement at 2.2 Å resolution of bovine chymosin. J. Mol. Biol. 221:1991;1295-1309.
56. Newman M., Watson F., Roychowdhury P., Jones H., Badasso M., Cleasby A., Wood S. P., Tickle I. J., Blundell T. L. Structure and refinement at 2.9 Å resolution of the aspartic proteinase from Mucor pusillus. J. Mol. Biol. 230:1993;260-283.
57. Parris K. D., Hoover D. J., Damon D. B., Davies D. R. Synthesis and crystallographic analysis of two rhizopuspepsin inhibitor complexes. Biochemistry. 31:1992;8125-8141.
58. Pearl L. H., Blundell T. L. The active site of aspartic proteinases. FEBS Letters. 174:1984;96-101.
59. Read R. J. Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallog. sect. A. 42:1986;140-149.
60. Richardson J. S. The anatomy and taxonomy of protein structure. Advan. Protein Chem. 34:1981;167-339.
61. Rupp S., Wolf D. H. Biogenesis of the yeast vacuole (lysosome). Eur. J. Biochem. 231:1995;115-125.
62. Šali A., Blundell T. L. The definition of topological equivalence in homologous and analogous structures: A procedure involving comparison of local properties and structural relationships through simulated annealing and dynamic programming. J. Mol. Biol. 212:1990;403-428.
63. Šali A., Veerapandian B., Cooper J. B., Foundling S. I., Hoover D. J., Blundell T. L. High-resolution X-ray diffraction study of the complex between endothiapepsin and an oligopeptide inhibitor: the analysis of the inhibitor binding and description of the rigid body shift in the enzyme. EMBO J. 8:1989;2179-2188.
64. Šali A., Veerapandian B., Cooper J. B., Moss D. S., Hofmann T., Blundell T. L. Domain flexibility in aspartic proteinases. Proteins: Struct. Funct. Genet. 12:1992;158-170.
65. Sakabe N. X-ray diffraction data collection system for modern protein crystallography with Weissenberg camera and an imaging plate using synchrotron radiation. Nucl. Instrum. Methods. A303:1991;448-463.
66. Sharp K. A., Nicholls A. DELPHI (Version 3.0) Manual. 1990;Columbia University, New York.
67. Sibanda B. L., Blundell T. L., Thornton J. M. Conformation of β-hairpins in protein structures. A systematic classification with applications to modelling by homology, electron density fitting and protein engineering. J. Mol. Biol. 206:1989;759-777.
68. Sielecki A. R., Hayakawa K., Fujinaga M., Murphy M. E. P., Fraser M., Muir A. K., Carilli C. T., Lewicki J. A., Baxter J. D., James M. N. G. Structure of recombinant human renin, a target for cardiovascular drugs, at 2.5 Å resolution. Science. 243:1989;1346-1351.
69. Sielecki A. R., Fedorov A. A., Boodhoo A., Andreeva N. S., James M. N. G. The molecular and crystal structures of monoclinic porcine pepsin refined at 1.8 Å resolution. J. Mol. Biol. 214:1990;143-170.
70. Srinivasan N., Blundell T. L. An evaluation of the performance of an automated procedure for comparative modelling of protein tertiary structure. Protein Eng. 6:1993;501-512.
71. Suguna K., Bott R. R., Padlan E. A., Subramanian E., Shefiff S., Cohen G. H., Davies D. R. Structure and refinement at 1.8 Å resolution of the aspartic proteinase from Rhizopus chinensis. J. Mol. Biol. 196:1987a;877-900.
72. Suguna K., Padlan E. A., Smith C. W., Carlson W. D., Davies D. R. Binding of a reduced peptide-inhibitor to the aspartic proteinase from Rhizopus chinensis: implications for a mechanism of action. Proc. Natl Acad. Sci., USA. 84:1987b;7009-7013.
73. Suguna K., Padlan E. A., Bott R. B., Boger J., Parris K. D., Davies D. R. Structures of complexes of rhizopuspepsin with pepstatin and other statine-containing inhibitors. Proteins: Struct. Funct. Genet. 13:1992;195-205.
74. Sutcliffe M. J., Haneef I., Carney D., Blundell T. L. Knowledge based modelling of homologous proteins, part I: 3-dimensional frameworks derived from simultaneous superposition of multiple structures. Protein Eng. 1:1987;377-384.
75. Teichert U., Mechler B., Muller H., Wolf D. H. Lysosomal (vacuolar) proteinases of yeast are essential catalysts for protein degradation, differentiation, and cell survival. J. Bio. Chem. 264:1989;16037-16045.
76. Tickle I. Review of space group general translation functions that make use of known structure informaiton and can be expanded as Fourier series. Machin P. Molecular Replacement, Proceedings of the Daresbury Study Weekend. 1985;CCP4, Daresbury Laboratory, UK.
77. van den Hazel H., Kielland-Brandt M. C., Winther J. R. Random substitution of large parts of the propeptide of yeast proteinase A. J. Biol. Chem. 270:1995;8602-8609.
78. Veerapandian B., Cooper J. B., Šali A., Blundell T. L. The three-dimensional strucutre of endothiapepsin complexed with a transition-state isostere inhibitor of renin at 1.6 Å resolution. J. Mol. Biol. 216:1990;1017-1029.
79. Veerapandian B., Cooper J. B., Šali A., Blundell T. L., Rosati R. L., Dominy B. W., Damon D. B., Hoover D. J. Direct observation by X-ray analysis of the tetrahedral 'intermediate' of aspartic proteinases. Protein Sci. 1:1992;322-328.
80. Westphal V., Marcusson E. G., Winther J. R., Emr S. D. Multiple pathways for the vacuolar sorting of yeast proteinase A. J. Biol. Chem. 271:1996;11865-11870.
81. Woodford C. A., Noble J. A., Garman J. D., Tam M. F., Innis M. A., Jones E. W. Phenotypic analysis of proteinase A mutants. J. Biol. Chem. 268:1993;8990-8998.