Tyrosine phenol-lyase and tryptophan indole-lyase encapsulated in wet nanoporous silica gels: Selective stabilization of tertiary conformations

Protein Science

Volumn 13, Issue 4, 2004, Pages 913-924

  Pioselli, Barbara ^a   Bettati, Stefano ^a   Demidkina, Tatyana V ^b   Zakomirdina, Lyudmila N ^b   Phillips, Robert S ^c   Mozzarelli, Andrea ^a  

^a UNIVERSITY OF PARMA   (Italy)

^b ENGELHARDT INSTITUTE OF MOLECULAR BIOLOGY   (Russian Federation)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

Catalysis; Conformational selection; Protein immobilization; Pyridoxal 5 phosphate; Silica gels

Indexed keywords

LYASE; PYRIDOXAL 5 PHOSPHATE; SILICA GEL; TRYPTOPHAN INDOLE LYASE; TYROSINE PHENOL LYASE; UNCLASSIFIED DRUG;

ARTICLE; BIOREACTOR; BIOSENSOR; CATALYSIS; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SUBSTRATE; GEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; STEADY STATE; STRUCTURE ANALYSIS;

BACTERIAL PROTEINS; CATALYSIS; CITROBACTER FREUNDII; ENZYME STABILITY; ENZYMES, IMMOBILIZED; KINETICS; PROTEIN CONFORMATION; PROTEUS VULGARIS; SILICON DIOXIDE; SUBSTRATE SPECIFICITY; TRYPTOPHANASE; TYROSINE PHENOL-LYASE;

EID: 1842507168     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.03492904     Document Type: Article

References (68)

1. Abbruzzetti, S., Viappiani, C., Bruno, S., and Mozzarelli, A. 2001. Enhanced geminate ligand rebinding upon photo-dissociation of silica gel-embedded myoglobin-CO. Chem. Phys. Lett. 346: 430-436.
2. Ahmed, S.A., Hyde, C.C., Thomas, G., and Miles, E.W. 1987. Microcrystals of tryptophan synthase α 2 β 2 complex from Salmonella typhimurium are catalytically active. Biochemistry 26: 5492-5498.
3. Antson, A.A., Demidkina, T.V., Gollnick, P., Dauter, Z., von Tersch, R.L., Long, J., Berezhnoy, S.N., Phillips, R.S., Harutyunyan, E.H., and Wilson, K.S. 1993. Three-dimensional structure of tyrosine phenol-lyase. Biochemistry 32: 4195-4206.
4. Bazhulina, N.P., Morozov, Y.V., Papisova, A.I., and Demidkina, T.V. 2000. Pyridoxal 5′-phoshate schiff base in Citrobacter freundii tyrosinephenollyase. Ionic and tautomeric equilibria. Eur. J. Biochem. 267: 1830-1836.
5. Besanger, T.R., Chen, Y., Deisingh, A.K., Hodgson, R., Jin, W., Mayer, S., Brook, M.A., and Brennan, J.D. 2003. Screening of inhibitors using enzymes entrapped in sol-gel-derived materials. Anal. Chem. 75: 2382-2391.
6. Bettati, S. and Mozzarelli, A. 1997. T state hemoglobin binds oxygen noncooperatively with allosteric effects of protons, inositol hexaphosphate, and chloride. J. Biol. Chem. 272: 32050-32055.
7. Bettati, S., Pioselli, B., Campanini, B., Viappiani, S., and Mozzarelli, A. 2004. Protein-doped nanoporous silica gels. In Encyclopedia of nanoscience and nanotechnology (ed. H.S. Nalwa), American Scientific Publishers, Stevenson Ranch, CA.
8. Brinker, C.J. and Scherer, G.W. 1990. Sol-gel science: The physics and chemistry of sol-gel processing. Academic Press, Boston.
9. Bruno, S., Bonaccio, M., Bettati, S., Rivetti, C., Viappiani, C., Abbruzzetti, S., and Mozzarelli, A. 2001. High and low oxygen affinity conformations of T state hemoglobin. Protein Sci. 10: 2401-2407.
10. Burkhard, P., Tai, C.H., Ristroph, C.M., Cook, P.F., and Jansonius, J.N. 1999. Ligand binding induces a large conformational change in O-acetylserine sulfhydrylase from Salmonella typhimurium. J. Mol. Biol. 291: 941-953.
11. Chen, H. and Phillips, R.S. 1993. Binding of phenol and analogues to alanine complexes of tyrosine phenol-lyase from Citrobacter freundii: Implications for the mechanism of α,β-elimination and alanine racemization. Biochemistry 32: 11591-11599.
12. Chen, H., Gollnick, P., and Phillips, R.S. 1995a. Site-directed mutagenesis of His343→Ala in Citrobacter freundii tyrosine phenol-lyase. Effects on the kinetic mechanism and rate-determining step. Eur. J. Biochem. 229: 540-549.
13. Chen, H.Y., Demidkina, T.V., and Phillips, R.S. 1995b. Site-directed mutagenesis of tyrosine-71 to phenylalanine in Citrobacter freundii tyrosine phenol-lyase: Evidence for dual roles of tyrosine-71 as a general acid catalyst in the reaction mechanism and in cofactor binding. Biochemistry 34: 12276-12283.
14. Chirico, G., Cannone, F., Beretta, S., Diaspro, A., Campanini, B., Bettati, S., Ruotolo, R., and Mozzarelli, A. 2002. Dynamics of green fluorescent protein mutant2 in solution, on spin-coated glasses, and encapsulated in wet silica gels. Protein Sci. 11: 1152-1161.
15. Das, T.K., Khan, I., Rousseau, D.L., and Friedman, J.M. 1998. Preservation of the native structure in myoglobin at low pH by sol-gel encapsulation. J. Am. Chem. Soc. 120: 10268-10269.
16. 2 thin-films - evidence for rotational mobility of encapsulated cytochrome c. Chem. Mater. 7: 1431-1434.
17. Demidkina, T.V., Barbolina, M.V., Faleev, N.G., Sundararaju, B., Gollnick, P.D., and Phillips, R.S. 2002. Threonine-124 and phenylalanine-448 in Citrobacter freundii tyrosine phenol-lyase are necessary for activity with L-tyrosine. Biochem. J. 363: 745-752.
18. Eggers, D.K. and Valentine, J.S. 2001. Molecular confinement influences protein structure and enhances thermal protein stability. Protein Sci. 10: 250-261.
19. Eliot, A.C. and Kirsch, J.F. 2002. Modulation of the internal aldimine pK(a)'s of 1-aminocyclopropane-1-carboxylate synthase and aspartate aminotransferase by specific active site residues. Biochemistry 41: 3836-3842.
20. Ellerby, L.M., Nishida, C.R., Nishida, F., Yamanaka, S.A., Dunn, B., Valentine, J.S., and Zink, J.I. 1992. Encapsulation of proteins in transparent porous silicate-glasses prepared by the sol-gel method. Science 255: 1113-1115.
21. Faeder, E.V. and Hammes, G.G. 1971. Kinetics studies of tryptophan synthetase. Interaction of substrates with the B subunit. Biochemistry 10: 1041-1045.
22. Gill, I. 2001. Bio-doped nanocomposite polymers: Sol-gel bioencapsulates. Chem. Mater. 13: 3404-3421.
23. Gill, I. and Ballesteros, A. 1998. Encapsulation of biologicals within silicate, siloxane, and hybrid sol-gel polymers: An efficient and generic approach. J. Am. Chem. Soc. 120: 8587-8598.
24. -. 2000. Bioencapsulation within synthetic polymers (Part 1): Sol-gel encapsulated biologicals. Trends Biotech. 18: 282-296.
25. Gonnelli, M. and Strambini, G.B. 2003. Structure and dynamics of proteins encapsulated in silica hydrogels by Trp phosphorescence. Biophys. Chem. 104: 155-169.
26. Gottfried, D.S., Kagan, A., Hoffman, B.M., and Friedman, J.M. 1999. Impeded rotation of a protein in a sol-gel matrix. J. Phys. Chem. B 103: 2803-2807.
27. Hartnett, A.M., Ingersoll, C.M., Baker, G.A., and Bright, F.V. 1999. Kinetics and thermodynamics of free flavins and the flavin-based redox active site within glucose oxidase dissolved in solution or sequestered within a sol-gel-derived glass. Anal. Chem. 71: 1215-1224.
28. Ikushiro, H., Hayashi, H., Kawata, Y., and Kagamiyama, H. 1998. Analysis of the pH- and ligand-induced spectral transitions of tryptophanase: Activation of the coenzyme at the early steps of the catalytic cycle. Biochemistry 37: 3043-3052.
29. Isupov, M.N., Antson, A.A., Dodson, E.J., Dodson, G.G., Dementieva, I.S., Zakomirdina, L.N., Wilson, K.S., Dauter, Z., Lebedev, A.A. and Harutyunyan, E.H. 1998. Crystal structure of tryptophanase. J. Mol. Biol. 276: 603-623.
30. Jin, W. and Brennan, J.D. 2002. Properties and applications of proteins encapsulated within sol-gel derived materials. Anal. Chim. Acta 461: 1-36.
31. Johnson, P. and Whateley, T.L. 1971. Use of polymerizing silica gel systems for the immobilization of trypsin. J. Colloid Interface Sci. 37: 557-563.
32. Jordan, J.D., Dunbar, R.A., and Bright, F.V. 1995. Dynamics of acrylodan-labeled bovine and human serum-albumin entrapped in a sol-gel-derived biogel. Anal. Chem. 67: 2436-2443.
33. Juszczak, L.J. and Friedman, J.M. 1999. UV resonance Raman spectra of ligand binding intermediates of sol-gel encapsulated hemoglobin. J. Biol. Chem. 274: 30357-30360.
34. Kallen, R.G., Korpela, T., Martell, A.E., Matsushina, Y., Metzler, C.M., Metzler, D.E., Morozov, Y.V., Ralston, I.M., Savin, F.A., Torchinsky, Y.M., et al. 1985. Chemical and spectroscopic properties of pyridoxal and pyridoxamine phosphates. In Transaminases (eds. P. Christen and D.E. Metzler), pp. 38. Wiley, New York.
35. Khan, I., Shannon, C.F., Dantsker, D., Friedman, A.J., Perez-Gonzalez-de-Apodaca, J., and Friedman, J.M. 2000. Sol-gel trapping of functional intermediates of hemoglobin: Geminate and bimolecular recombination studies. Biochemistry 39: 16099-16109.
36. Kiick, D.M. and Phillips, R.S. 1988. Mechanistic deductions from kinetic isotope effects and pH studies of pyridoxal phosphate dependent carbon-carbon lyases: Erwinia herbicola and Citrobacter freundii tyrosine phenol-lyase. Biochemistry 27: 7333-7338.
37. Klimov, D.K., Newfield, D., and Thirumalai, D. 2002. Simulations of β-hairpin folding confined to spherical pores using distributed computing. Proc. Natl. Acad. Sci. 99: 8019-8024.
38. Kumagai, H., Yamada, H., Matsui, H., Ohkishi, H., and Ogata, K. 1970. Tyrosine phenol lyase I. Purification, crystallization, and properties. J. Biol. Chem. 245: 1767-1772.
39. Malashkevich, V.N., Toney, M.D., and Jansonius, J.N. 1993. Crystal structures of true enzymatic reaction intermediates: Aspartate and glutamate ketimines in aspartate aminotransferase. Biochemistry 32: 13451-13462.
40. McIninch, J.K. and Kantrowitz, E.R. 2001. Use of silicate sol-gels to trap the R and T quaternary conformational states of pig kidney fructose-1,6-bisphosphatase. Biochim. Biophys. Acta 1547: 320-328.
41. McPhalen, C.A., Vincent, M.G., Picot, D., Jansonius, J.N., Lesk, A.M., and Chothia, C. 1992. Domain closure in mitochondrial aspartate aminotransferase. J. Mol. Biol. 227: 197-213.
42. Metzler, C.M., Viswanath, R., and Metzler, D.E. 1991. Equilibria and absorption spectra of tryptophanase. J. Biol. Chem. 266: 9374-9381.
43. Mozzarelli, A. and Bettati, S. 2001. Functional properties of immobilized proteins. In Physical properties and applications (ed. H.S. Nalwa), pp. 55-97. Overseas Publishers Association, Singapore.
44. Mozzarelli, A., Peracchi, A., Rossi, G.L., Ahmed, S.A., and Miles, E.W. 1989. Microspectrophotometric studies on single crystals of the tryptophan synthase α 2 β 2 complex demonstrate formation of enzyme-substrate intermediates. J. Biol. Chem. 264: 15774-15780.
45. Mozzarelli, A., Bettati, S., Pucci, A.M., Burkhard, P., and Cook, P.F. 1998. Catalytic competence of O-acetylserine sulfhydrylase in the crystal probed by polarized absorption microspectrophotometry. J. Mol. Biol. 283: 135-146.
46. Mozzarelli, A., Campanini, B., Bettati, S., and Peracchi, A. 2000, Functional properties of immobilized pyroxidal 5′ phosphate dependent enzymes probed by absorption microspectrophotometry. In Biochemistry and molecular biology of vitamin B6 and PQQ-dependent proteins (eds. A. Iriarte et al.), pp. 230-232. Birkhauser Verlag, Basel, Switzerland.
47. Phillips, R.S. 1987. Reactions of O-acyl-L-serines with tryptophanase, tyrosine phenol-lyase, and tryptophan synthase. Arch. Biochem. Biophys. 256: 302-310.
48. -. 1991. Reaction of indole and analogues with amino acid complexes of Escherichia coli tryptophan indole-lyase: Detecfion of a new reaction intermediate by rapid-scanning stopped-flow spectrophotometry. Biochemistry 30: 5927-5934.
49. Phillips, R.S., Miles, E.W., and Cohen, L.A. 1984. Interactions of tryptophan synthase, tryptophanase, and pyridoxal phosphate with oxindolyl-L-alanine and 2,3-dihydro-L-tryptophan: Support for an indolenine intermediate in tryptophan metabolism. Biochemistry 23: 6228-6234.
50. Phillips, R.S., Demidkina, T.V., Zakormirdina, L.N., Bruno, S., Ronda, L., and Mozzarelli, A. 2002. Crystals of tryptophan indole-lyase and tyrosine phenol-lyase form stable quinonoid complexes. J. Biol. Chem. 277: 21592-21597.
51. Phillips, R.S., Demidkina, T.V., and Faleev, N.G. 2003. Structure and mechanism of tryptophan indole-lyase and tyrosine phenol-lyase. Biochim. Biophys. Acta 1647: 167-172.
52. Reetz, M.T. and Jaeger, K.E. 1998. Overexpression, immobilization and biotechnological application of Pseudomonas lipases. Chem. Phys. Lipids 93: 3-14.
53. Schirch, V., Shostak, K., Zamora, M., and Guatam-Basak, M. 1991. The origin of reaction specificity in serine hydroxymethyltransferase. J. Biol. Chem. 266: 759-764.
54. Schneider, T.R., Gerhardt, E., Lee, M., Liang, P.H., Anderson, K.S., and Schlichting, I. 1998. Loop closure and intersubunit communication in tryptophan synthase. Biochemistry 37: 5394-5406.
55. Shen, C.Y. and Kostic, N.M. 1997. Kinetics of photoinduced electron-transfer reactions within sol-gel silica glass doped with zinc cytochrome c. Study of electrostatic effects in confined liquids. J. Am. Chem. Soc. 119: 1304-1312.
56. Shibayama, N. and Saigo, S. 1995. Fixation of the quaternary structures of human adult haemoglobin by encapsulation in transparent porous silica gels. J. Mol. Biol. 251: 203-209.
57. -. 1999. Kinetics of the allosteric transition in hemoglobin within silicate sol-gels. J. Am. Chem. Soc. 121: 444-445.
58. -. 2001. Direct observation of two distinct affinity conformations in the T state human deoxyhemoglobin. FEBS Lett. 492: 50-53.
59. -. 2003. Oxygen equilibrium properties of myoglobin locked in the liganded and unliganded conformations. J. Am. Chem. Soc. 125: 3780-3783.
60. Suelter, C.H., Wang, J., and Snell, E.E. 1976. Direct spectrophotometric assay of tryptophanase. FEBS Lett. 66: 230-.
61. Sundararaju, B., Antson, A.A., Phillips, R.S., Demidkina, T.V., Barbolina, M.V., Gollnick, P., Dodson, G.G., and Wilson, K.S. 1997. The crystal structure of Citrobacter freundii tyrosine phenol-lyase complexed with 3-(4′-hydroxyphenyl)propionic acid, together with site-directed mutagenesis and kinetic analysis, demonstrates that arginine 381 is required for substrate specificity. Biochemistry 36: 6502-6510.
62. Takagi, F., Koga, N., and Takada, S. 2003. How protein thermodynamics and folding mechanisms are altered by the chaperonin cage: Molecular simulations. Proc. Natl. Acad. Sci. 100: 11367-11372.
63. Thirumalai, D., Klimov, D.K., and Lorimer, G.H. 2003. Caging helps protein fold. Proc. Natl. Acad. Sci. 100: 11195-11197.
64. von Tersch, R.L., Secundo, F., Phillips, R.S., and Newton, M.G. 1996. Preparation of fluorinated aminoacid with tyrosine phenol lyase: Effects of fluorination on the reaction kinetics and mechanism of tyrosine phenol lyase and tyrosine protein kinase. In Biomedical application of fluorine chemistry (eds. I. Ojima et al.), pp. 95-104. American Chemical Society, Washington, DC.
65. Watanabe, T. and Snell, E.E. 1977. The interaction of Escherichia coli tryptophanase with various amino and their analogs. Active site mapping. J. Biochem. (Tokyo) 82: 733.
66. West, J.M. and Kantrowitz, E.R. 2003. Trapping specific quaternary states of the allosteric enzyme aspartate transcarbamoylase in silica matrix sol-gels. J. Am. Chem. Soc. 125: 9924-9925.
67. Zakormirdina, L.N., Kulikova, V.V., Gogoleva, O.I., Dementieva, I.S., Faleev, N.G., and Demidkina, T.V. 2002. Tryptophan indole-lyase from Proteus vulgaris: Kinetic and spectral properties. Biochemistry (Moscow) 67: 1437-1445.
68. Zhou, H.X. and Dill, K.A. 2001. Stabilization of proteins in confined spaces. Biochemistry 40: 11289-11293.