Structural and functional modularity of proteins in the de novo purine biosynthetic pathway

Protein Science

Volumn 18, Issue 5, 2009, Pages 881-892

  Li, Hui ^a,b   Fast, Walter ^a,c   Benkovic, Stephen J ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

De novo purine biosynthetic pathway; Domain swapping; Protein evolution

Indexed keywords

ADENOSINE TRIPHOSPHATE; ENZYME; HYBRID PROTEIN; N 5 CARBOXYLAMINOIMIDAZOLE RIBONUCLEOTIDE SYNTHETASE; PHOSPHORIBOSYLGLYCINAMIDE FORMYLTRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; ENZYME ACTIVITY; ESCHERICHIA COLI; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; PURINE SYNTHESIS; SEQUENCE HOMOLOGY;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; CARBOXY-LYASES; CATALYTIC DOMAIN; ESCHERICHIA COLI PROTEINS; HYDROXYMETHYL AND FORMYL TRANSFERASES; METABOLIC NETWORKS AND PATHWAYS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHORIC ACID ESTERS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PURINES; RECOMBINANT FUSION PROTEINS;

ESCHERICHIA COLI;

EID: 65649084878     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.95     Document Type: Article

References (42)

1. Aimi J, Qiu H, Williams J, Zalkin H, Dixon JE (1990) De novo purine nucleotide biosynthesis: cloning of human and avian cDNAs encoding the trifunctional glycinamide ribonucleotide synthetase-aminoimidazole ribonucleotide synthetase-glycinamide ribonucleotide transformylase by functional complementation in E. coli. Nucleic Acids Res 18:6665-6672. (Pubitemid 20386598)
2. Kan JL, Jannatipour M, Taylor SM, Moran RG (1993) Mouse cDNAs encoding a trifunctional protein of de novo purine synthesis and a related single-domain glycinamide ribonucleotide synthetase. Gene 137:195-202. (Pubitemid 24071633)
3. Doolittle RF, Bork P (1993) Evolutionarily mobile modules in proteins. Sci Am 269:50-56. (Pubitemid 23300853)
4. Scott KA, Steward A, Fowler SB, Clarke J (2002) Titin: a multidomain protein that behaves as the sum of its parts. J Mol Biol 315:819-829. (Pubitemid 34729329)
5. Mainfroid V, Goraj K, Rentier-Delrue F, Houbrechts A, Loiseau A, Gohimont AC, Noble ME, Borchert TV, Wierenga RK, Martial JA (1993) Replacing the (beta alpha)-unit 8 of E. coli TIM with its chicken homologue leads to a stable and active hybrid enzyme. Protein Eng 6:893-900. (Pubitemid 2014266)
6. Lang D, Thoma R, Henn-Sax M, Sterner R, Wilmanns M (2000) Structural evidence for evolution of the beta/alpha barrel scaffold by gene duplication and fusion. Science 289:1546-1550.
7. Hocker B, Beismann-Driemeyer S, Hettwer S, Lustig A, Sterner R (2001) Dissection of a (betaalpha)8-barrel enzyme into two folded halves. Nat Struct Biol 8:32-36.
8. Hocker B, Claren J, Sterner R (2004) Mimicking enzyme evolution by generating new (betaalpha)8-barrels from (betaalpha)4-half-barrels. Proc Natl Acad Sci USA 101:16448-16453.
9. Vogel C, Bashton M, Kerrison ND, Chothia C, Teichmann SA (2004) Structure, function and evolution of multidomain proteins. Curr Opin Struct Biol 14:208-216. (Pubitemid 38490788)
10. Ostermeier M, Benkovic SJ (2000) Evolution of protein function by domain swapping. Adv Protein Chem 55:29-77.
11. Galperin MY, Koonin EV (1997) A diverse superfamily of enzymes with ATP-dependent carboxylate-amine/thiol ligase activity. Protein Sci 6:2639-2643. (Pubitemid 28006703)
12. Waldrop GL, Rayment I, Holden HM (1994) Three-dimensional structure of the biotin carboxylase subunit of acetyl-CoA carboxylase. Biochemistry 33:10249-10256. (Pubitemid 24281789)
13. Thoden JB, Holden HM, Wesenberg G, Raushel FM, Rayment I (1997) Structure of carbamoyl phosphate synthetase: a journey of 96 A from substrate to product. Biochemistry 36:6305-6316. (Pubitemid 27231386)
14. Yamaguchi H, Kato H, Hata Y, Nishioka T, Kimura A, Oda J, Katsube Y (1993) Three-dimensional structure of the glutathione synthetase from Escherichia coli B at 2.0 A resolution. J Mol Biol 229:1083-1100. (Pubitemid 23091822)
15. Wolodko WT, Fraser ME, James MN, Bridger WA (1994) The crystal structure of succinyl-CoA synthetase from Escherichia coli at 2.5-A resolution. J Biol Chem 269:10883-10890. (Pubitemid 24198302)
16. Fan C, Moews PC, Walsh CT, Knox JR (1994) Vancomycin resistance: structure of D-alanine:D-alanine ligase at 2.3 A resolution. Science 266:439-443. (Pubitemid 124005186)
17. Wang W, Kappock TJ, Stubbe J, Ealick SE (1998) X-ray crystal structure of glycinamide ribonucleotide synthetase from Escherichia coli. Biochemistry 37:15647-15662. (Pubitemid 28524735)
18. Shindyalov IN, Bourne PE (1998) Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Protein Eng 11:739-747. (Pubitemid 28434482)
19. Thoden JB, Kappock TJ, Stubbe J, Holden HM (1999) Three-dimensional structure of N5-carboxyaminoimidazole ribonucleotide synthetase: a member of the ATP grasp protein superfamily. Biochemistry 38:15480-15492. (Pubitemid 129503588)
20. Thoden JB, Firestine SM, Nixon A, Benkovic SJ, Holden HM (2000) Molecular structure of Escherichia coli PurT-encoded glycinamide ribonucleotide transformylase. Biochemistry 39:8791-8802. (Pubitemid 30602788)
21. Thoden JB, Firestine SM, Benkovic SJ, Holden HM (2002) PurT-encoded glycinamide ribonucleotide transformylase: accomodation of adenosine nucleotide analogs within the active site. J Biol Chem 277:23898-23908.
22. Marolewski AE, Mattia KM, Warren MS, Benkovic SJ (1997) Formyl phosphate: a proposed intermediate in the reaction catalyzed by Escherichia coli PurT GAR transformylase. Biochemistry 36:6709-6716. (Pubitemid 27242329)
23. Marolewski A, Smith JM, Benkovic SJ (1994) Cloning and characterization of a new purine biosynthetic enzyme: a non-folate glycinamide ribonucleotide transformylase from E. coli. Biochemistry 33:2531-2537. (Pubitemid 24099660)
24. Mueller EJ, Meyer E, Rudolph J, Davisson VJ, Stubbe J (1994) N5-carboxyaminoimidazole ribonucleotide: evidence for a new intermediate and two new enzymatic activities in the de novo purine biosynthetic pathway of Escherichia coli. Biochemistry 33:2269-2278. (Pubitemid 24099627)
25. Sauers CK, Jencks WP, Groh S (1975) Alcohol-bicarbonate-water system. Structure-reactivity studies on the equilibriums for formation of alkyl monocarbonates and on the rates of their decomposition in aqueous alkali. J Am Chem Soc 97:5546-5553.
26. Nixon AE, Warren MS, Benkovic SJ (1997) Assembly of an active enzyme by the linkage of two protein modules. Proc Natl Acad Sci USA 94:1069-1073. (Pubitemid 27087805)
27. Inglese J, Johnson DL, Shiau A, Smith JM, Benkovic SJ (1990) Subcloning, characterization, and affinity labeling of Escherichia coli glycinamide ribonucleotide transformylase. Biochemistry 29:1436-1443. (Pubitemid 20063373)
28. Klein C, Chen P, Arevalo JH, Stura EA, Marolewski A, Warren MS, Benkovic SJ, Wilson IA (1995) Towards structure-based drug design: crystal structure of a multisubstrate adduct complex of glycinamide ribonucleotide transformylase at 1.96 A resolution. J Mol Biol 249:153-175.
29. Nixon AE, Benkovic SJ (2000) Improvement in the efficiency of formyl transfer of a GAR transformylase hybrid enzyme. Protein Eng 13:323-327. (Pubitemid 30339354)
30. Ostermeier M, Shim JH, Benkovic SJ (1999) A combinatorial approach to hybrid enzymes independent of DNA homology. Nat Biotechnol 17:1205-1209.
31. Sorensen IS, Dandanell G (1997) Identification and sequence analysis of Sulfolobus solfataricus purE and purK genes. FEMS Microbiol Lett 154:173-180. (Pubitemid 27404528)
32. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640-6645. (Pubitemid 30412767)
33. Meyer E, Leonard NJ, Bhat B, Stubbe J, Smith JM (1992) Purification and characterization of the purE, purK, and purC gene products: identification of a previously unrecognized energy requirement in the purine biosynthetic pathway. Biochemistry 31:5022-5032.
34. Thoden JB, Holden HM, Firestine SM (2008) Structural analysis of the active site geometry of N5-carboxyaminoimidazole ribonucleotide synthetase from Escherichia coli. Biochemistry 47:13346-13353. (Pubitemid 350301905)
35. Gots JS, Benson CE, Jochimson B, Koduri KR. Microbial models and regulatory elements in the control of purine metabolism. In: Elliott K, Fitzsimons DW, Eds. (1976) Purine and pyrimidine metabolism. Amsterdam: Elsevier, pp 23-42.
36. Lutz S, Benkovic SJ (2000) Homology-independent protein engineering. Curr Opin Biotechnol 11:319-324. (Pubitemid 30598924)
37. Mootz HD, Marahiel MR (1999) Design and application of multimodular peptide synthetases. Curr Opin Biotechnol 10:341-348. (Pubitemid 29373947)
38. Nygaard P, Smith JM (1993) Evidence for a novel glycinamide ribonucleotide transformylase in Escherichia coli. J Bacteriol 175:3591-3597. (Pubitemid 23163405)
39. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59. (Pubitemid 19125653)
40. Lutz S, Ostermeier M, Benkovic SJ (2001) Rapid generation of incremental truncation libraries for protein engineering using alpha-phosphothioate nucleotides. Nucleic Acids Res 29(4):E16.
41. Pechere JF, Capony JP (1967) On the colorimetric determination of acyl phosphate. Anal Biochem 22:536-539.
42. Kappock TJ, Ealick SE, Stubbe J (2000) Modular evolution of the purine biosynthetic pathway. Curr Opin Chem Biol 4:567-572. (Pubitemid 30599339)