Intrinsic evolutionary constraints on protease structure, enzyme acylation, and the identity of the catalytic triad

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 8, 2013, Pages

  Buller, Andrew R ^a   Townsend, Craig A ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Antibiotic stereochemistry; N terminal nucleophile; Peptidase

Indexed keywords

AMIDE; CYSTEINE; METHYL GROUP; NATURAL PRODUCT; NUCLEOPHILE; PROTEINASE; SERINE; THREONINE;

ACYLATION; AMINO TERMINAL SEQUENCE; ARTICLE; CATALYSIS; CHEMICAL ANALYSIS; CONCEPTUAL FRAMEWORK; CONVERGENT EVOLUTION; ENZYME ACTIVE SITE; ENZYME MECHANISM; ENZYME STRUCTURE; HYDROGEN BOND; NUCLEOPHILICITY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTON TRANSPORT; SITE DIRECTED MUTAGENESIS; STEREOCHEMISTRY; STEREOSPECIFICITY;

ACYLATION; BIOCATALYSIS; BIOLOGICAL EVOLUTION; ENZYME INHIBITORS; MODELS, MOLECULAR; PEPTIDE HYDROLASES; PROTEOLYSIS; PROTONS;

EID: 84874238669     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1221050110     Document Type: Article

References (85)

1. Warshel A, Naray-Szabo G, Sussman F, Hwang JK (1989) How do serine proteases really work? Biochemistry 28 (9):3629-3637.
2. Fersht A (1999) Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding (Freeman, New York).
3. Kraut J (1988) How do enzymes work? Science 242 (4878):533-540.
4. Warshel A (1998) Electrostatic origin of the catalytic power of enzymes and the role of preorganized active sites. J Biol Chem 273 (42):27035-27038.
5. Warshel A (1978) Energetics of enzyme catalysis. Proc Natl Acad Sci USA 75 (11):5250-5254.
6. Ekici OD, Paetzel M, Dalbey RE (2008) Unconventional serine proteases: Variations on the catalytic Ser/His/Asp triad configuration. Protein Sci 17 (12):2023-2037.
7. Milkowski C, Strack D (2004) Serine carboxypeptidase-like acytransferases. Phytochemistry 65 (5):517-524.
8. Chen L, et al. (2008) Structural basis for the catalytic mechanism of phosphothreonine lyase. Nat Struct Mol Biol 15 (1):101-102.
9. Rawlings ND, Barrett AJ, Bateman A (2012) MEROPS: The database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 40 (Database issue, D1): D343-D350.
10. Brannigan JA, et al. (1995) A protein catalytic framework with an N-terminal nucleophile is capable of self-activation. Nature 378 (6555):416-419.
11. Seemüller E, et al. (1995) Proteasome from Thermoplasma acidophilum: A threonine protease. Science 268 (5210):579-582.
12. Smith AJT, et al. (2008) Structural reorganization and preorganization in enzyme active sites: Comparisons of experimental and theoretically ideal active site geometries in the multistep serine esterase reaction cycle. J Am Chem Soc 130 (46):15361-15373.
13. Galperin MY, Walker DR, Koonin EV (1998) Analogous enzymes: Independent inventions in enzyme evolution. Genome Res 8 (8):779-790.
14. Polgár L (2005) The catalytic triad of serine peptidases. Cell Mol Life Sci 62 (19-20):2161-2172.
15. Robertus JD, Kraut J, Alden RA, Birktoft JJ (1972) Subtilisin; a stereochemical mechanism involving transition-state stabilization. Biochemistry 11 (23):4293-4303.
16. Neet KE, Koshland DE, Jr. (1966) The conversion of serine at the active site of subtilisin to cysteine: A "chemical mutation". Proc Natl Acad Sci USA 56 (5):1606-1611.
17. Polgar L, Bender ML (1966) A new enzyme containing a synthetically formed active site. Thiol-subtillisin. J Am Chem Soc 88 (13):3153-3154.
18. Carter P, Wells JA (1988) Dissecting the catalytic triad of a serine protease. Nature 332 (6164):564-568.
19. Corey DR, Craik CS (1992) An investigation into the minimum requirements for peptide hydrolysis by mutation of the catalytic triad of trypsin. J Am Chem Soc 114 (5):1784-1790.
20. Kisselev AF, Songyang Z, Goldberg AL (2000) Why does threonine, and not serine, function as the active site nucleophile in proteasomes? J Biol Chem 275 (20):14831-14837.
21. Rawlings ND, Barrett AJ (1994) Families of serine peptidases. Methods Enzymol 244:19-61.
22. Paetzel M, Dalbey RE (1997) Catalytic hydroxyl/amine dyads within serine proteases. Trends Biochem Sci 22 (1):28-31.
23. Khayat R, et al. (2003) Structural and biochemical studies of inhibitor binding to human cytomegalovirus protease. Biochemistry 42 (4):885-891.
24. Simón L, Goodman JM (2010) Enzyme catalysis by hydrogen bonds: The balance between transition state binding and substrate binding in oxyanion holes. J Org Chem 75 (6):1831-1840.
25. Simón L, Goodman JM (2012) Hydrogen-bond stabilization in oxyanion holes: Grand jeté to three dimensions. Org Biomol Chem 10 (9):1905-1913.
26. Fülöp V, Böcskei Z, Polgár L (1998) Prolyl oligopeptidase: An unusual beta-propeller domain regulates proteolysis. Cell 94 (2):161-170.
27. Wahlgren WY, et al. (2011) The catalytic aspartate is protonated in the Michaelis complex formed between trypsin and an in vitro evolved substrate-like inhibitor: A refined mechanism of serine protease action. J Biol Chem 286 (5):3587-3596.
28. Kim JS, et al. (2002) Navigation inside a protease: Substrate selection and product exit in the tricorn protease from Thermoplasma acidophilum. J Mol Biol 324 (5):1041-1050.
29. Szyk A, Maurizi MR (2006) Crystal structure at 1.9A of E. coli ClpP with a peptide covalently bound at the active site. J Struct Biol 156 (1):165-174.
30. Mac Sweeney A, et al. (2000) Crystal structure of delta-chymotrypsin bound to a peptidyl chloromethyl ketone inhibitor. Acta Crystallogr D Biol Crystallogr 56 (Pt 3):280-286.
31. Storer AC, Ménard R (1994) Catalytic mechanism in papain family of cysteine peptidases. Methods Enzymol 244:486-500.
32. Baird TT, Jr., Wright WD, Craik CS (2006) Conversion of trypsin to a functional threonine protease. Protein Sci 15 (6):1229-1238.
33. Derst C, Wehner A, Specht V, Röhm KH (1994) States and functions of tyrosine residues in Escherichia coli asparaginase II. Eur J Biochem 224 (2):533-540.
34. Mileni M, et al. (2009) Binding and inactivation mechanism of a humanized fatty acid amide hydrolase by alpha-ketoheterocycle inhibitors revealed from cocrystal structures. J Am Chem Soc 131 (30):10497-10506.
35. Cygler M, et al. (1993) Relationship between sequence conservation and three-dimensional structure in a large family of esterases, lipases, and related proteins. Protein Sci 2 (3):366-382.
36. Strynadka NCJ, et al. (1992) Molecular structure of the acyl-enzyme intermediate in beta-lactam hydrolysis at 1.7 A resolution. Nature 359 (6397):700-705.
37. Ollis DL, et al. (1992) The alpha/beta hydrolase fold. Protein Eng 5 (3):197-211.
38. Brenner C (2002) Catalysis in the nitrilase superfamily. Curr Opin Struct Biol 12 (6):775-782.
39. Garavito RM, Rossmann MG, Argos P, Eventoff W (1977) Convergence of active center geometries. Biochemistry 16 (23):5065-5071.
40. Löwe J, et al. (1995) Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 A resolution. Science 268 (5210):533-539.
41. Groll M, et al. (1997) Structure of 20S proteasome from yeast at 2.4 A resolution. Nature 386 (6624):463-471.
42. Seemuller E, Lupas A, Baumeister W (1996) Autocatalytic processing of the 20S proteasome. Nature 382 (6590):468-471.
43. Perler FB, Xu MQ, Paulus H (1997) Protein splicing and autoproteolysis mechanisms. Curr Opin Chem Biol 1 (3):292-299.
44. Liu Y, Guan C, Aronson NN, Jr. (1998) Site-directed mutagenesis of essential residues involved in the mechanism of bacterial glycosylasparaginase. J Biol Chem 273 (16):9688-9694.
45. Cheng H, Grishin NV (2005) DOM-fold: A structure with crossing loops found in DmpA, ornithine acetyltransferase, and molybdenum cofactor-binding domain. Protein Sci 14 (7):1902-1910.
46. Buller AR, Freeman MF, Wright NT, Schildbach JF, Townsend CA (2012) Insights into cis-autoproteolysis reveal a reactive state formed through conformational rearrangement. Proc Natl Acad Sci USA 109 (7):2308-2313.
47. Jung ME, Piizzi G (2005) gem-disubstituent effect: Theoretical basis and synthetic applications. Chem Rev 105 (5):1735-1766.
48. Buller AR, et al. (2012) Autoproteolytic activation of ThnT results in structural reorganization necessary for substrate binding and catalysis. J Mol Biol 422 (4):508-518.
49. Korza HJ, Bochtler M (2005) Pseudomonas aeruginosa LD-carboxypeptidase, a serine peptidase with a Ser-His-Glu triad and a nucleophilic elbow. J Biol Chem 280 (49):40802-40812.
50. Street TO, Fitzkee NC, Perskie LL, Rose GD (2007) Physical-chemical determinants of turn conformations in globular proteins. Protein Sci 16 (8):1720-1727.
51. Pace HC, et al. (2000) Crystal structure of the worm NitFhit Rosetta Stone protein reveals a Nit tetramer binding two Fhit dimers. Curr Biol 10 (15):907-917.
52. Motherwell WB, Bingham MJ, Six Y (2001) Recent progress in the design and synthesis of artificial enzymes. Tetrahedron 57 (22):4663-4686.
53. Kipnis Y, Baker D (2012) Comparison of designed and randomly generated catalysts for simple chemical reactions. Protein Sci 21 (9):1388-1395.
54. Gerlt JA, Babbitt PC (2009) Enzyme (re) design: Lessons from natural evolution and computation. Curr Opin Chem Biol 13 (1):10-18.
55. Röthlisberger D, et al. (2008) Kemp elimination catalysts by computational enzyme design. Nature 453 (7192):190-195.
56. Siegel JB, et al. (2010) Computational design of an enzyme catalyst for a stereoselective bimolecular Diels-Alder reaction. Science 329 (5989):309-313.
57. Richter F, et al. (2012) Computational design of catalytic dyads and oxyanion holes for ester hydrolysis. J Am Chem Soc 134 (39):16197-16206.
58. Page MGP, Heim J (2009) New molecules from old classes: Revisiting the development of beta-lactams. IDrugs 12 (9):561-565.
59. Fisher JF, Meroueh SO, Mobashery S (2005) Bacterial resistance to beta-lactam antibiotics: Compelling opportunism, compelling opportunity. Chem Rev 105 (2):395-424.
60. Paetzel M, Dalbey RE, Strynadka NCJ (1998) Crystal structure of a bacterial signal peptidase in complex with a beta-lactam inhibitor. Nature 396 (6707):186-190.
61. Fenteany G, et al. (1995) Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 268 (5211):726-731.
62. Huang ZW, et al. (2008) Structural basis for activation and inhibition of the secreted chlamydia protease CPAF. Cell Host Microbe 4 (6):529-542.
63. Groll M, Huber R, Potts BCM (2006) Crystal structures of Salinosporamide A (NPI-0052) and B (NPI-0047) in complex with the 20S proteasome reveal important consequences of beta-lactone ring opening and a mechanism for irreversible binding. J Am Chem Soc 128 (15):5136-5141.
64. Zeiler E, et al. (2011) Vibralactone as a tool to study the activity and structure of the ClpP1P2 complex from Listeria monocytogenes. Angew Chem Int Ed Engl 50 (46):11001-11004.
65. Ehmann DE, et al. (2012) Avibactam is a covalent, reversible, non-β-lactam β-lactamase inhibitor. Proc Natl Acad Sci USA 109 (29):11663-11668.
66. Fisher HF, Conn EE, Vennesland B, Westheimer FH (1953) The enzymatic transfer of hydrogen. I. The reaction catalyzed by alcohol dehydrogenase. J Biol Chem 202 (2):687-697.
67. Emsley P, Cowtan K (2004) Coot: Model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60 (Pt 12 Pt 1):2126-2132.
68. Tamada T, et al. (2009) 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 (31):11033-11040.
69. Wlodawer A, et al. (2001) Carboxyl proteinase from Pseudomonas defines a novel family of subtilisin-like enzymes. Nat Struct Biol 8 (5):442-446.
70. Silvaggi NR, Anderson JW, Brinsmade SR, Pratt RF, Kelly JA (2003) The crystal structure of phosphonate-inhibited D-Ala-D-Ala peptidase reveals an analogue of a tetrahedral transition state. Biochemistry 42 (5):1199-1208.
71. Håkansson K, Wang AHJ, Miller CG (2000) The structure of aspartyl dipeptidase reveals a unique fold with a Ser-His-Glu catalytic triad. Proc Natl Acad Sci USA 97 (26):14097-14102.
72. Chung IYW, Paetzel M (2011) Crystal structure of a viral protease intramolecular acyl-enzyme complex: Insights into cis-cleavage at the VP4/VP3 junction of Tellina birnavirus. J Biol Chem 286 (14):12475-12482.
73. Wang Y, Zhang Y, Ha Y (2006) Crystal structure of a rhomboid family intramembrane protease. Nature 444 (7116):179-180.
74. Zhu L, et al. (2011) Peptide aldehyde inhibitors challenge the substrate specificity of the SARS-coronavirus main protease. Antiviral Res 92 (2):204-212.
75. Watt W, et al. (1999) The atomic-resolution structure of human caspase-8, a key activator of apoptosis. Structure 7 (9):1135-1143.
76. Sokabe M, et al. (2002) The X-ray crystal structure of pyrrolidone-carboxylate peptidase from hyperthermophilic archaea Pyrococcus horikoshii. J Struct Funct Genomics 2 (3):145-154.
77. Biarrotte-Sorin S, et al. (2006) Crystal structure of a novel beta-lactam-insensitive peptidoglycan transpeptidase. J Mol Biol 359 (3):533-538.
78. Lorenz IC, Marcotrigiano J, Dentzer TG, Rice CM (2006) Structure of the catalytic domain of the hepatitis C virus NS2-3 protease. Nature 442 (7104):831-835.
79. Du XL, et al. (2000) Crystal structure of an intracellular protease from Pyrococcus horikoshii at 2-A resolution. Proc Natl Acad Sci USA 97 (26):14079-14084.
80. Schröder E, Phillips C, Garman E, Harlos K, Crawford C (1993) X-ray crystallographic structure of a papain-leupeptin complex. FEBS Lett 315 (1):38-42.
81. Mossessova E, Lima CD (2000) Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol Cell 5 (5):865-876.
82. Russo AT, White MA, Watowich SJ (2006) The crystal structure of the Venezuelan equine encephalitis alphavirus nsP2 protease. Structure 14 (9):1449-1458.
83. Xu Q, et al. (2009) Structural basis of murein peptide specificity of a gamma-D-glutamyl-l-diamino acid endopeptidase. Structure 17 (2):303-313.
84. Suh H-Y, et al. (2012) Crystal structure of DeSI-1, a novel deSUMOylase belonging to a putative isopeptidase superfamily. Proteins 80 (8):2099-2104.
85. Chen VB, et al. (2010) MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66 (Pt 1):12-21.