Stereoselective bimolecular phenoxy radical coupling by an auxiliary (dirigent) protein without an active center

Science

Volumn 275, Issue 5298, 1997, Pages 362-366

  Davin, Laurence B ^a   Wang, Huai Bin ^a   Crowell, Anastasia L ^a   Bedgar, Diana L ^a   Martin, Diane M ^a   Sarkanen, Simo ^b   Lewis, Norman G ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FREE RADICAL; LIGNAN; LIGNIN; OXIDOREDUCTASE; PINORESINOL;

ARTICLE; BIOSYNTHESIS; CHEMICAL REACTION; ENZYME ACTIVITY; NONHUMAN; OXIDATION; PLANT; PRIORITY JOURNAL; PROTEIN ANALYSIS; STEREOSPECIFICITY;

NON-PROGRAMMATIC;

DIMERIZATION; FLAVIN MONONUCLEOTIDE; FLAVIN-ADENINE DINUCLEOTIDE; FREE RADICALS; FURANS; KINETICS; LACCASE; LIGNANS; MOLECULAR CONFORMATION; OXIDATION-REDUCTION; OXIDOREDUCTASES; PHENOLS; PLANT PROTEINS; STEREOISOMERISM;

EID: 0031031957     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.275.5298.362     Document Type: Article

References (39)

1. M. Nose et al., Phytochemistry 39, 71 (1995).
2. N. G. Lewis and L. B. Davin, ACS Symp. Ser. 562, 202 (1994).
3. P. W. Paré, H.-B. Wang, L. B. Davin, N. G. Lewis, Tetrahedron Lett. 35, 4731 (1994).
4. M. A. Bernards, M. L. Lopez, J. Zajicek, N. G. Lewis, J. Biol. Chem. 270, 7382 (1995).
5. J. D. Bu'Lock, P. R. Leeming, H. G. Smith, J. Chem. Soc. 1962, 2085 (1962).
6. M. Miessner et al., Helv. Chim. Acta 74, 1205 (1991); V. J. Marmaras, N. D. Charalambidis, C. G. Zervas, Arch. Insect Biochem. Physiol. 31, 119 (1996).
7. M. Miessner et al., Helv. Chim. Acta 74, 1205 (1991); V. J. Marmaras, N. D. Charalambidis, C. G. Zervas, Arch. Insect Biochem. Physiol. 31, 119 (1996).
8. D. W. Cameron, Lord Todd, in Organic Substances of Natural Origin. Oxidative Coupling of Phenols, W. I. Taylor and A. R. Battersby, Eds. (Dekker, New York, 1967), vol. 1, pp. 203-241.
9. M. A. Ragan, Phytochemistry 23, 2029 (1984).
10. J. Iqbal, B. Bhatia, N. K. Nayyar, Chem. Rev. 94, 519 (1994).
11. K. Freudenberg, Science 148, 595 (1965).
12. T. Higuchi, Physiol. Plant. 10, 356 (1957); J. M. Harkin and J. R. Obst, Science 180, 296 (1973); K. Freudenberg, Nature 183, 1152; R. Sterjiades, J. F. D. Dean, G. Gamble, D. S. Himmelsbach, K.-E. L. Eriksson, Planta 190, 75 (1993); K. Freudenberg, J. M. Harkin, M. Reichert, T. Fukuzumi, Chem. Ber. 91, 581 (1958); W. Bao, D. M. O'Malley, R. Whetten, R. R. Sederoff, Science 260, 672 (1993); R. Sterjiades, J. F. D. Dean, K.-E. L. Eriksson, Plant Physiol. 99, 1162 (1992); H. S. Mason and M. Cronyn, J. Am. Chem. Soc. 77, 491 (1955); P. Udagama-Randeniya and R. Savidge, Electrophoresis 15, 1072 (1994); R. Savidge and P. Udagama-Randeniya, Phytochemistry 31, 2959 (1992); H. Koblitz and D. Koblitz, Nature 204, 199 (1964).
13. T. Higuchi, Physiol. Plant. 10, 356 (1957); J. M. Harkin and J. R. Obst, Science 180, 296 (1973); K. Freudenberg, Nature 183, 1152; R. Sterjiades, J. F. D. Dean, G. Gamble, D. S. Himmelsbach, K.-E. L. Eriksson, Planta 190, 75 (1993); K. Freudenberg, J. M. Harkin, M. Reichert, T. Fukuzumi, Chem. Ber. 91, 581 (1958); W. Bao, D. M. O'Malley, R. Whetten, R. R. Sederoff, Science 260, 672 (1993); R. Sterjiades, J. F. D. Dean, K.-E. L. Eriksson, Plant Physiol. 99, 1162 (1992); H. S. Mason and M. Cronyn, J. Am. Chem. Soc. 77, 491 (1955); P. Udagama-Randeniya and R. Savidge, Electrophoresis 15, 1072 (1994); R. Savidge and P. Udagama-Randeniya, Phytochemistry 31, 2959 (1992); H. Koblitz and D. Koblitz, Nature 204, 199 (1964).
14. T. Higuchi, Physiol. Plant. 10, 356 (1957); J. M. Harkin and J. R. Obst, Science 180, 296 (1973); K. Freudenberg, Nature 183, 1152; R. Sterjiades, J. F. D. Dean, G. Gamble, D. S. Himmelsbach, K.-E. L. Eriksson, Planta 190, 75 (1993); K. Freudenberg, J. M. Harkin, M. Reichert, T. Fukuzumi, Chem. Ber. 91, 581 (1958); W. Bao, D. M. O'Malley, R. Whetten, R. R. Sederoff, Science 260, 672 (1993); R. Sterjiades, J. F. D. Dean, K.-E. L. Eriksson, Plant Physiol. 99, 1162 (1992); H. S. Mason and M. Cronyn, J. Am. Chem. Soc. 77, 491 (1955); P. Udagama-Randeniya and R. Savidge, Electrophoresis 15, 1072 (1994); R. Savidge and P. Udagama-Randeniya, Phytochemistry 31, 2959 (1992); H. Koblitz and D. Koblitz, Nature 204, 199 (1964).
15. T. Higuchi, Physiol. Plant. 10, 356 (1957); J. M. Harkin and J. R. Obst, Science 180, 296 (1973); K. Freudenberg, Nature 183, 1152; R. Sterjiades, J. F. D. Dean, G. Gamble, D. S. Himmelsbach, K.-E. L. Eriksson, Planta 190, 75 (1993); K. Freudenberg, J. M. Harkin, M. Reichert, T. Fukuzumi, Chem. Ber. 91, 581 (1958); W. Bao, D. M. O'Malley, R. Whetten, R. R. Sederoff, Science 260, 672 (1993); R. Sterjiades, J. F. D. Dean, K.-E. L. Eriksson, Plant Physiol. 99, 1162 (1992); H. S. Mason and M. Cronyn, J. Am. Chem. Soc. 77, 491 (1955); P. Udagama-Randeniya and R. Savidge, Electrophoresis 15, 1072 (1994); R. Savidge and P. Udagama-Randeniya, Phytochemistry 31, 2959 (1992); H. Koblitz and D. Koblitz, Nature 204, 199 (1964).
16. T. Higuchi, Physiol. Plant. 10, 356 (1957); J. M. Harkin and J. R. Obst, Science 180, 296 (1973); K. Freudenberg, Nature 183, 1152; R. Sterjiades, J. F. D. Dean, G. Gamble, D. S. Himmelsbach, K.-E. L. Eriksson, Planta 190, 75 (1993); K. Freudenberg, J. M. Harkin, M. Reichert, T. Fukuzumi, Chem. Ber. 91, 581 (1958); W. Bao, D. M. O'Malley, R. Whetten, R. R. Sederoff, Science 260, 672 (1993); R. Sterjiades, J. F. D. Dean, K.-E. L. Eriksson, Plant Physiol. 99, 1162 (1992); H. S. Mason and M. Cronyn, J. Am. Chem. Soc. 77, 491 (1955); P. Udagama-Randeniya and R. Savidge, Electrophoresis 15, 1072 (1994); R. Savidge and P. Udagama-Randeniya, Phytochemistry 31, 2959 (1992); H. Koblitz and D. Koblitz, Nature 204, 199 (1964).
17. T. Higuchi, Physiol. Plant. 10, 356 (1957); J. M. Harkin and J. R. Obst, Science 180, 296 (1973); K. Freudenberg, Nature 183, 1152; R. Sterjiades, J. F. D. Dean, G. Gamble, D. S. Himmelsbach, K.-E. L. Eriksson, Planta 190, 75 (1993); K. Freudenberg, J. M. Harkin, M. Reichert, T. Fukuzumi, Chem. Ber. 91, 581 (1958); W. Bao, D. M. O'Malley, R. Whetten, R. R. Sederoff, Science 260, 672 (1993); R. Sterjiades, J. F. D. Dean, K.-E. L. Eriksson, Plant Physiol. 99, 1162 (1992); H. S. Mason and M. Cronyn, J. Am. Chem. Soc. 77, 491 (1955); P. Udagama-Randeniya and R. Savidge, Electrophoresis 15, 1072 (1994); R. Savidge and P. Udagama-Randeniya, Phytochemistry 31, 2959 (1992); H. Koblitz and D. Koblitz, Nature 204, 199 (1964).
18. T. Higuchi, Physiol. Plant. 10, 356 (1957); J. M. Harkin and J. R. Obst, Science 180, 296 (1973); K. Freudenberg, Nature 183, 1152; R. Sterjiades, J. F. D. Dean, G. Gamble, D. S. Himmelsbach, K.-E. L. Eriksson, Planta 190, 75 (1993); K. Freudenberg, J. M. Harkin, M. Reichert, T. Fukuzumi, Chem. Ber. 91, 581 (1958); W. Bao, D. M. O'Malley, R. Whetten, R. R. Sederoff, Science 260, 672 (1993); R. Sterjiades, J. F. D. Dean, K.-E. L. Eriksson, Plant Physiol. 99, 1162 (1992); H. S. Mason and M. Cronyn, J. Am. Chem. Soc. 77, 491 (1955); P. Udagama-Randeniya and R. Savidge, Electrophoresis 15, 1072 (1994); R. Savidge and P. Udagama-Randeniya, Phytochemistry 31, 2959 (1992); H. Koblitz and D. Koblitz, Nature 204, 199 (1964).
19. T. Higuchi, Physiol. Plant. 10, 356 (1957); J. M. Harkin and J. R. Obst, Science 180, 296 (1973); K. Freudenberg, Nature 183, 1152; R. Sterjiades, J. F. D. Dean, G. Gamble, D. S. Himmelsbach, K.-E. L. Eriksson, Planta 190, 75 (1993); K. Freudenberg, J. M. Harkin, M. Reichert, T. Fukuzumi, Chem. Ber. 91, 581 (1958); W. Bao, D. M. O'Malley, R. Whetten, R. R. Sederoff, Science 260, 672 (1993); R. Sterjiades, J. F. D. Dean, K.-E. L. Eriksson, Plant Physiol. 99, 1162 (1992); H. S. Mason and M. Cronyn, J. Am. Chem. Soc. 77, 491 (1955); P. Udagama-Randeniya and R. Savidge, Electrophoresis 15, 1072 (1994); R. Savidge and P. Udagama-Randeniya, Phytochemistry 31, 2959 (1992); H. Koblitz and D. Koblitz, Nature 204, 199 (1964).
20. T. Higuchi, Physiol. Plant. 10, 356 (1957); J. M. Harkin and J. R. Obst, Science 180, 296 (1973); K. Freudenberg, Nature 183, 1152; R. Sterjiades, J. F. D. Dean, G. Gamble, D. S. Himmelsbach, K.-E. L. Eriksson, Planta 190, 75 (1993); K. Freudenberg, J. M. Harkin, M. Reichert, T. Fukuzumi, Chem. Ber. 91, 581 (1958); W. Bao, D. M. O'Malley, R. Whetten, R. R. Sederoff, Science 260, 672 (1993); R. Sterjiades, J. F. D. Dean, K.-E. L. Eriksson, Plant Physiol. 99, 1162 (1992); H. S. Mason and M. Cronyn, J. Am. Chem. Soc. 77, 491 (1955); P. Udagama-Randeniya and R. Savidge, Electrophoresis 15, 1072 (1994); R. Savidge and P. Udagama-Randeniya, Phytochemistry 31, 2959 (1992); H. Koblitz and D. Koblitz, Nature 204, 199 (1964).
21. T. Higuchi, Physiol. Plant. 10, 356 (1957); J. M. Harkin and J. R. Obst, Science 180, 296 (1973); K. Freudenberg, Nature 183, 1152; R. Sterjiades, J. F. D. Dean, G. Gamble, D. S. Himmelsbach, K.-E. L. Eriksson, Planta 190, 75 (1993); K. Freudenberg, J. M. Harkin, M. Reichert, T. Fukuzumi, Chem. Ber. 91, 581 (1958); W. Bao, D. M. O'Malley, R. Whetten, R. R. Sederoff, Science 260, 672 (1993); R. Sterjiades, J. F. D. Dean, K.-E. L. Eriksson, Plant Physiol. 99, 1162 (1992); H. S. Mason and M. Cronyn, J. Am. Chem. Soc. 77, 491 (1955); P. Udagama-Randeniya and R. Savidge, Electrophoresis 15, 1072 (1994); R. Savidge and P. Udagama-Randeniya, Phytochemistry 31, 2959 (1992); H. Koblitz and D. Koblitz, Nature 204, 199 (1964).
22. T. Higuchi, Physiol. Plant. 10, 356 (1957); J. M. Harkin and J. R. Obst, Science 180, 296 (1973); K. Freudenberg, Nature 183, 1152; R. Sterjiades, J. F. D. Dean, G. Gamble, D. S. Himmelsbach, K.-E. L. Eriksson, Planta 190, 75 (1993); K. Freudenberg, J. M. Harkin, M. Reichert, T. Fukuzumi, Chem. Ber. 91, 581 (1958); W. Bao, D. M. O'Malley, R. Whetten, R. R. Sederoff, Science 260, 672 (1993); R. Sterjiades, J. F. D. Dean, K.-E. L. Eriksson, Plant Physiol. 99, 1162 (1992); H. S. Mason and M. Cronyn, J. Am. Chem. Soc. 77, 491 (1955); P. Udagama-Randeniya and R. Savidge, Electrophoresis 15, 1072 (1994); R. Savidge and P. Udagama-Randeniya, Phytochemistry 31, 2959 (1992); H. Koblitz and D. Koblitz, Nature 204, 199 (1964).
23. O. R. Gottlieb and M. Yoshida, in Natural Products of Woody Plants: Chemicals Extraneous to the Lignocellulosic Cell Wall, J. W. Rowe and C. H. Kirk, Eds. (Springer-Verlag, Berlin, 1989) pp. 439-511; D. C. Ayres and J. D. Loike, Chemistry and Pharmacology of Natural Products: Lignans: Chemical, Biological and Clinical Properties (Cambridge Univ. Press, Cambridge, 1990).
24. O. R. Gottlieb and M. Yoshida, in Natural Products of Woody Plants: Chemicals Extraneous to the Lignocellulosic Cell Wall, J. W. Rowe and C. H. Kirk, Eds. (Springer-Verlag, Berlin, 1989) pp. 439-511; D. C. Ayres and J. D. Loike, Chemistry and Pharmacology of Natural Products: Lignans: Chemical, Biological and Clinical Properties (Cambridge Univ. Press, Cambridge, 1990).
25. H. Erdtman, Sven. Papperstidn. 42, 115 (1939).
26. L. B. Davin and N. G. Lewis, An. Acad. Bras. Cienc. 67 (Supl. 3), 363 (1995); L. B. Davin, D. L. Bedgar, T. Katayama, N. G. Lewis, Phytochemistry 31, 3869 (1992).
27. L. B. Davin and N. G. Lewis, An. Acad. Bras. Cienc. 67 (Supl. 3), 363 (1995); L. B. Davin, D. L. Bedgar, T. Katayama, N. G. Lewis, Phytochemistry 31, 3869 (1992).
28. Supplementary material describing protein solubilization and purification and a figure showing a gel filtration profile and ultraviolet-visible spectra can be accessed on the World Wide Web at http://www. science-mag.org/science/feature/beyond/#XXXX and can be ordered from AAAS (see any current masthead for ordering information).
29. -2), the radioactivity of the eluent being measured with a flow-through detector (Radiomatic, Model A120).
30. A substantial difference was noted in the subsequent turnover of the lignan products observed after E-coniferyl alcohol depletion. With the laccase alone no turnover occurred, but when both proteins were present the disappearance of the products was significant. In order to understand the difference, assays were conducted where bovine serum albumin (BSA) and ovalbumin were individually added to the laccase-containing solutions at concentrations matching the weight concentrations of the dirigent protein. In this way, it was established that the differences in product turnover were simply due to stabilization of laccase activity at the higher protein concentrations, although interestingly the dirigent protein, BSA, and ovalbumin afforded somewhat different degrees of protection. The findings were quite comparable when a fungal laccase (from Trametes versicolor) was used in place of the plant laccase.
31. -1), and buffer (0.1 M MES-Hepes-sodium acetate, pH 5.0) in a total volume of 250 μl. After 1 hour incubation, the reaction mixture was extracted with EtOAc as described in (16), but with the addition of an internal standard and omission of radiochemical carriers. After reversed-phase column chromatography, the enzymatically formed pinoresinol was collected, freeze-dried, redissolved in methanol (100 μl), and subjected to chiral column chromatography (Daicel, Chiralcel OD, 50 mm by 4.6 mm) with detection at 280 nm and analysis by mass spectral fragmentation in the El mode (Waters, Integrity System)
32. A. Usaitis and R. Makuska, Polymer 35, 4896 (1994).
33. T. C. Bruice, Acc. Chem. Res. 13, 256 (1980).
34. 2O) and, after 30-min incubation at 30°C, the enzymatically formed FMN was separated from the protein mixture by filtration through a Centricon 10 (Amicon) microconcentrator.
35. -1, 8.3 kBq) were used as substrates and, after 6-hour incubation at 30°C, the reaction mixture was extracted with EtOAc but without addition of radiochemical carriers.
36. T. Deyama, Chem. Pharm. Bull. 31, 2993 (1983).
37. -1). Assays with dirigent protein, with or without FMN, were incubated at 30°C for 1 hour, whereas assays with Forsythia laccase or fraction III with or without dirigent protein were incubated at 30°C for 15 min.
38. -1 enzyme) were as follows: with respect to the laccase, 0.200 ± 0.001 and 3.9 ± 0.2 for (±)-erythro/threo guaiacylglycerol 8-O-4′-coniferyl alcohol ethers, 0.3000 ± 0.0003 and 13.1 ± 0.6 for (±)-dehydrodiconiferyl alcohols, and 0.300 ± 0.0002 and 7.54 ± 0.50 for (±)-pinoresinols; with respect to the fraction III oxidase (estimated to have a native molecular weight of 80 KD), 2.2 ± 0.3 and 0.20 ± 0.03 for (+)-erythro/threo guaiacylglycerol 8-O-4-coniferyl alcohol ethers, 2.2 ± 0.2 and 0.7 ± 0.1 for (±)-dehydrodiconiferyl alcohols, and 3.7 ± 0.7 and 0.6 ± 0.1 for (±)-pinoresinols.
39. Dedicated to the memories of J. L. Varner and K. V. Sarkanen. We thank the National Science Foundation (MCB-9219586), the U. S. Department of Energy (DE-FG06-91ER20022), and the DOE-NSF-USDA (DE-FG06-94ER20160) and Plant Biochemistry Research and Training Center (D.M.M. and A.L.C.) for summer undergraduate and graduate assistantships, respectively). Support through Minnesota Agricultural Experiment Station Project 43-68 (Hatch Funds) (S.S.) is also gratefully acknowledged, as are T. C. Bruice and V. Massey for valuable discussions and P. Sakata (PerSeptive Biosystem) for assistance during critical phases of the project.