Crystal structure of phenylalanine ammonia lyase: Multiple helix dipoles implicated in catalysis

Biochemistry

Volumn 43, Issue 36, 2004, Pages 11403-11416

  Calabrese, Joseph C ^a   Jordan, Douglas B ^a,b   Boodhoo, Amechand ^a,c   Sariaslani, Sima ^a   Vannelli, Todd ^a,d  

^a DUPONT COMPANY   (United States)

^b NATIONAL CENTER FOR AGRICULTURAL UTILIZATION RESEARCH   (United States)

^c ELI LILLY AND COMPANY   (United States)

^d Cornell University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOCATION; ELECTROPHILICITY; PHENYLALANINE AMMONIA LYASE (PAL);

AMMONIA; CRYSTAL STRUCTURE; ENZYMES; HYDROGEN; PROTONS; SEPARATION; SUBSTRATES;

BIOCHEMISTRY;

3,5 DIHYDRO 5 METHYLIDENE 4H IMIDAZOL 4 ONE; HISTIDINE; HISTIDINE AMMONIALYASE; IMIDAZOLE DERIVATIVE; PHENYL GROUP; PHENYLALANINE; PHENYLALANINE AMMONIA LYASE; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CRYSTAL STRUCTURE; DIPOLE; ELECTRON TRANSPORT; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYME STRUCTURE; HELIX DIPOLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTON TRANSPORT; RHODOSPIRILLUM; RHODOSPORIDIUM TORULOIDES;

CATALYSIS; COENZYMES; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; FUNGAL PROTEINS; HISTIDINE; HISTIDINE AMMONIA-LYASE; IMIDAZOLES; MODELS, MOLECULAR; PHENYLALANINE; PHENYLALANINE AMMONIA-LYASE; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; RHODOTORULA; SUBSTRATE SPECIFICITY;

RHODOSPIRILLUM; RHODOSPORIDIUM; RHODOSPORIDIUM TORULOIDES;

EID: 4444306767     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049053+     Document Type: Article

References (56)

1. Hanson, K. R., and Havir, E. A. (1981) Phenylalanine Ammonia-Lyase, in The Biochemistry of Plants (Conn, E., Ed.) Vol. 7, pp 577-625, Academic Press, New York.
2. Rosler, J., Krekel, F., Amrhein, N., and Schmid, J. (1997) Maize phenylalanine ammonia-lyase has tyrosine ammonia-lyase activity, Plant Physiol. 113, 175-179.
3. Kyndt, J. A., Meyer, T. E., Cusanovich, M. A., and Van Beeumen, J. J. (2002) Characterization of a bacterial tyrosine ammonia lyase, a biosynthetic enzyme for the photoactive yellow protein, FEBS Lett. 512, 240-244.
4. Gatenby, A. A., Sariaslani, S., Tang, X. S., Qi, W. W., and Vannelli, T. (2002) Bioproduction of para-hydroxycinnamic acid, U.S. Patent 6,368,837 B1.
5. Turner, A. M., Simpson, A., Mcinnes, R., and Howell, P. L. (1997) Human argininosuccinate lyase: a structural basis for intragenic complementation, Proc. Natl. Acad. Sci. U.S.A. 94, 9063-9068.
6. Shi, W., Dunbar, J., Jayasekera, M. M. K., Viola, R. E., and Farber, G. K. (1997) The structure of L-aspartate ammonia-lyase from Escherichia coli, Biochemistry 36, 9136-9144.
7. Jayasekera, M. M. K., Shi, W., Farber, G. K., and Viola, R. E. (1997) Evaluation of functionally important amino acids in L-aspartate ammonia-lyase from Escherichia coli, Biochemistry 36, 9145-9150.
8. Levy, C. W., Buckley, P. A., Sedelnikova, S., Kato, Y., Asano, Y., Rice, D. W., and Baker, P. J. (2002) Insights into enzyme evolution revealed by the structure of methylaspartate ammonia lyase, Structure 10, 101-113.
9. Peterkofsky, A. (1962) The mechanism of action of histidase: amino-enzyme formation and partial reactions, J. Biol. Chem. 237, 787-795.
10. Rettig, M., Sigrist, A., and Rétey, J. (2000) Mimicking the reaction of phenylalanine ammonia-lyase by a synthetic model, Helv. Chim. Acta 83, 2246-2265.
11. Poppe, L. (2001) Methylidene-imidazolone: a novel electrophile for substrate activation, Curr. Opin. Chem. Biol. 5, 512-524.
12. Schuster, B., and Rétey, J. (1995) The mechanism of action of phenylalanine ammonia-lyase: the role of prosthetic dehydroalanine, Proc. Natl. Acad. Sci. U.S.A. 92, 8433-8437.
13. Skolaut, A., and Rétey, J. (2001) 1,4-Dihydro-L-phenylalanine-its synthesis and behavior in the phenylalanine ammonia-lyase reaction, Arch. Biochem. Biophys. 393, 187-191.
14. Schwede, T. F., Rétey, J., and Schulz, G. E. (1999) Crystal structure of histidine ammonia-lyase revealing a novel polypeptide modification as the catalytic electrophile, Biochemistry 38, 5355-5361.
15. Baedeker, M., and Schulz, G. E. (2002) Autocatalytic peptide cyclization during chain folding of histidine ammonia-lyase, Structure 10, 61-67.
16. Baedeker, M., and Schulz, G. E. (2002) Structures of two histidine ammonia-lyase modifications and implications for the catalytic mechanism, Eur. J. Biochem. 269, 1790-1797.
17. Rétey, J. (2003) Discovery and role of methylidene imidazolone, a highly electrophilic prosthetic group, Biochim. Biophys. Acta 1647, 179-184.
18. Langer, B., Langer, M, and Rétey, J. (2001) Methylidene- imidazolone (MIO) from histidine and phenylalanine ammonia-lyase, Adv. Protein Chem. 58, 175-214.
19. Rétey, J. (1996) Enzymatic catalysis by Friedel-Crafts-type reactions, Naturwissenschaften 83, 439-447.
20. Hermes, J. D., Weiss, P. M., and Cleland, W. W. (1985) Use of nitrogen-15 and deuterium isotope effects to determine the chemical mechanism of phenylalanine ammonia-lyase, Biochemistry 24, 2959-2967.
21. Gloge, A., Langer, B., Poppe, L., and Rétey, J. (1998) The behavior of substrate analogues and secondary deuterium isotope effects in the phenylalanine ammonia-lyase reaction, Arch. Biochem. Biophys. 359, 1-7.
22. Furuta, T., Takahashi, H., and Kasuya, Y (1990) Evidence for a carbanion intermediate in the elimination of ammonia from L-histidine catalyzed by histidine ammonia-lyase, J. Am. Chem. Soc. 112, 3633-3636.
23. Lewandowicz, A., Jemielity, J., Kanska, M., Zon, J., and Paneth, P. (1999) Tritium secondary kinetic isotope effect on phenylalanine ammonia-lyase-catalyzed reaction, Arch. Biochem. Biophys. 370, 216-221.
24. Lewis, B. E., and Schramm, V. L. (2003) Binding equilibrium isotope effects for glucose at the catalytic domain of human brain hexokinase, J. Am. Chem. Soc. 125, 4785-4798.
25. Xing., S., and Cekan, S. Z. (1983) Isotope effects of tritium in a ligand-antibody binding, Int. J. Appl. Radiat. Isot. 34, 957-958.
26. Röther, D., Poppe, L., Morlock, G., Viergutz, S., and Rétey, J. (2002) An active site homology model of phenylalanine ammonia-lyase from Petroselinum crispum, Eur. J. Biochem. 269, 3065-3075.
27. Hendrickson, W. A., Pahler, A., Smith, J. L., Satow, Y., Merritt, E. A., and Phizackerley, R. P. (1989) Crystal structure of core streptavidin determined from multiwavelength anomalous diffraction of synchrotron radiation, Proc. Natl. Acad. Sci. U.S.A. 86, 2190-2194.
28. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode, Methods Enzymol. 276, 307-326.
29. Sheldrick, G. M. (1998) Location of Heavy Atoms by Automated Patterson Interpretation, in Direct Methods for Solving Macromolecular Structures (Fortier, S., Ed.) pp 131-141, Kluwer Academic Publishers, Dordrecht, The Netherlands.
30. Weeks, C. M., and Miller, R. (1999) The design and implementation of SnB version 2.0, J. Appl. Crystallogr. 32, 120-124.
31. De La Fortelle, E., and Bricogne, G. (1997) Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods, Methods Enzymol. 276, 472-494.
32. Vagin, A., and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement, J. Appl. Crystallogr. 30, 1022-1025.
33. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models, Acta Crystallogr. A47, 110-119.
34. McRee, D. E. (1999) XtalView/Xfit - a versatile program for manipulating atomic coordinates and electron density, J. Struct. Biol. 125, 156-165.
35. Brünger, A. T., and Warren, G. L. (1998) Crystallography and NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr. D54, 905-921.
36. Brünger, A. T. (1992) The free R value: a novel statistical quantity for assessing the accuracy of crystal structures, Nature 355, 472-474.
37. Word, J. M., Lovell, S. C., Richardson, J. S., and Richardson, D. C. (1999) Asparagine and glutamine: using hydrogen atom contacts in the choice of side-chain amide orientation, J. Mol. Biol. 285, 1735-1747.
38. Lu, G. (2000) TOP: a new method for protein structure comparisons and similarity searches, J. Appl. Crystallogr. 33, 176-183.
39. Bailey, S. (1994) The CCP4 suite: programs for protein crystallography, Acta Crystallogr. D50, 760-763.
40. Carson, M. (1997) Ribbons, Methods Enzymol. 277, 493-505.
41. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Res. 22, 4673-4680.
42. Allwood, E. G., Davies, D. R., Gerrish, C., Ellis, B. E., and Bolwell, G. P. (1999) Phosphorylation of phenylalanine ammonia-lyase: evidence for a novel protein kinase and identification of the phosphorylated residue, FEES Lett. 457, 47-52.
43. Mitraki, A., Miller, S., and van Raaij, M. J. (2002) Review: conformation and folding of novel beta-structural elements in viral fiber proteins: the triple beta-spiral and triple beta-helix, J. Struct. Biol. A137, 236-247.
44. Havir, E. A., and Hanson, K. R. (1975) L-Phenylalanine ammonia-lyase (maize, potato, and Rhodotorula glutinis). Studies of the prosthetic group with nitromethane, Biochemistry 14, 1620-1626.
45. Sarkhel, S., Rich, A., and Egli, M. (2003) Water-nucleobase "stacking": H-π and lone pair-π interactions in the atomic resolution crystal structure of an RNA pseudoknot, J. Am. Chem. Soc. 125, 8998-8999.
46. Röther, D., Poppe, L., Viergutz, S., Langer, B., and Rétey, J. (2001) Characterization of the active site of histidine ammonia-lyase from Pseudomonas putida, Eur. J. Biochem. 268, 6011-6019.
47. Havir, E. A., and Hanson, K. R. (1968) L-Phenylalanine ammonia lyase. II. Mechanism and kinetic properties of the enzyme from potato tubers, Biochemistry 7, 1904-1914.
48. Langer, M., Pauling, A., and Rétey, J. (1995) The role of dehydroalanine in catalysis by histidine ammonia lyase, Angew. Chem., Int. Ed. Engl. 34, 1464-1465.
49. Phillips, B., and Glockshuber, R. (2002) Randomization of the entire active-site helix α1 of the thiol-disulphide oxidoreductase DsbA from Escherichia coli, J. Biol. Chem. 277, 43050-43957.
50. Jordan, D. B., Zheng, Y.-J., Locket, B. A., and Basarab, G. S. (2000) Stereochemistry of the enolization of scytalone by scytalone dehydratase, Biochemistry 39, 2276-2282.
51. Bruice, T. C., and Lightstone, F. C. (1999) Ground state and transition state contributions to the rate of intramolecular and enzymic reactions, Ace. Chem. Res. 32, 127-136.
52. Hol, W. G. (1985) The role of the alpha-helix dipole in protein function and structure, Prog. Biophys. Mol. Biol. 45, 149-195.
53. Thoden, J. B., Holden, H. M., Zhuang, Z., and Dunnaway-Mariano, D. (2002) X-ray crystallographic analyses of inhibitor and substrate complexes of wild-type and mutant 4-hydroxybenzoyl-CoA thioesterase, J. Biol. Chem. 277, 27468-27476.
54. Trickey, P., Wagner, M. A., Jorns, M. S., and Mathews, F. S. (1999) Monomeric sarcosine oxidase: structure of a covalently flavinylated amine oxidizing enzyme, Structure 7, 331-345.
55. Christenson, S. D., Liu, W., Toney, M. D., and Shen, B. (2003) A novel 4-methylideneimidazole-5-one-containing tyrosine aminomutase in enediyne antitumor antibiotic C-1027 biosynthesis, J. Am. Chem. Soc. 125, 6062-6063.
56. Christenson, S. D., Wu, W., Spies, M. A., and Shen, B. (2003) Kinetic analysis of the 4-methylideneimidazole-5-one-containing tyrosine aminomutase in enediyne antitumor antibiotic C-1027 biosynthesis, Biochemistry 42, 12708-12718.