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J. Biol. Chem., Vol. 277, Issue 24, 21332-21340, June 14, 2002
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From the a Centre for Protein Technology TNO-WU, Bomenweg 2,
6700 EV Wageningen, b Laboratory of Biochemistry,
Department of Agrotechnology and Food Sciences, Wageningen University,
Dreijenlaan 3, 6703 HA Wageningen, c Laboratory of Food
Chemistry, Department of Agrotechnology and Food Sciences, Bomenweg 2,
6700 EV, Wageningen University, Wageningen, e Swammerdam
Institute for Life Sciences, Faculty of Science, University of
Amsterdam, Nieuwe Achtergracht 166, 1018 WV Amsterdam, g ATO,
Bornsesteeg 59, 6708 PD, Wageningen, and h TNO Food and
Nutrition Research, Utrechtseweg 48, 3700 AJ
Zeist, The Netherlands
Received for publication, February 19, 2002, and in revised form, March 27, 2002
Ferulic acid (FA) is an abundantly present
phenolic constituent of plant cell walls. Kinetically controlled
incubation of FA and the tripeptide Gly-Tyr-Gly (GYG) with horseradish
peroxidase and H2O2 yielded a range of
new cross-linked products. Two predominant series of hetero-oligomers
of FA linked by dehydrogenation to the peptidyl tyrosine were
characterized by electrospray ionization (tandem) mass spectrometry.
One series comprises GYG coupled with 4-7 FA moieties linked by
dehydrogenation, of which one is decarboxylated. In the second series
4-9 FA moieties linked by dehydrogenation, of which two are
decarboxylated, are coupled to the tripeptide. A third series comprises
three hetero-oligomers in which the peptidyl tyrosine is linked to 1-3
FA moieties of which none is decarboxylated. Two mechanisms for the
formation of the FA-Tyr oligomers that result from the dualistic,
concentration-dependent chemistry of FA and their possible
role in the regulation of plant cell wall tissue growth are presented.
Plant peroxidases (donor: hydrogen-peroxide
oxidoreductases, EC 1.11.1.7) have often been suggested to be
involved in the biosynthesis of complex plant cell wall macromolecules
constituting lignin and suberin tissues. Lignins are located in the
primary and secondary walls of specific plant cells and are synthesized for mechanical strength, defense, and water transport in terrestrial vascular plants. The temporal and spatial correlation between lignin
synthesis and peroxidase catalysis has been suggested based on studies
of the enzyme, the hydroxycinnamic acid substrates, and the
hydrogen peroxide co-substrate in vivo. In lignin
tissues of transgenic plants, the Arabidopsis ATP A2
peroxidase promoter directs GUS reporter gene expression,
indicating involvement of the peroxidase in the assembly of the lignin
polymer (1). After administration of the reducing substrate
[13C]ferulic acid to wheat cell walls for extended
duration, elevated levels of ferulic acid in the lignin-like tissues
were revealed by in situ solid state 13C NMR
(2). In Pinus taeda cell suspension cultures, lignin synthesis is correlated with the generation of the oxidizing
co-substrate H2O2 (3). Suberin provides a
physical barrier to moisture loss in plants as well as a defensive
shield against pathogens. In the potato, a
H2O2-generating system with
NAD(P)H-dependent oxidase-like properties is temporarily
associated with suberin synthesis (4), and the polyaromatic domain of
suberins in wound-healing potato (Solanum tuberosum) tubers
is constituted of polymers derived from hydroxycinnamic acid (5).
Ferulic acid (FA,1
3-(4-hydroxy-3-methoxyphenyl)-2-propenoic acid), a hydroxycinnamic acid
that is often found to be esterified to plant cell wall polysaccharides
(6, 7) is a good substrate for most plant peroxidases. The x-ray
structure of horseradish peroxidase C (HRP C) in complex with FA (8)
provides molecular insight into the initial abstraction of the hydroxyl
hydrogen via one-electron oxidation and subsequent deprotonation of the cation radical, resulting in the FA free radical. Dehydrodimers of FA
stemming from radical combination have been identified in plant cell
walls (9-13). In vitro, similar FA dehydrodimers have been
identified after incubation of peroxidase with either free FA or FA
esterified to pectins and arabinoxylans (14). Recently, it was reported
that in incubations with lignin peroxidase, higher polymers of ferulic
acid are formed, and the structures of two dehydrotrimers were assigned
by 1H NMR (15).
Tyrosine, both as free amino acid and in peptides or proteins, is also
a substrate for many plant peroxidases. After one-electron oxidation
and subsequent deprotonation, a tyrosine radical species is formed that
can combine with another tyrosine radical at either the phenolic oxygen
or at one of the ortho positions of the aromatic ring (16).
Dityrosines and higher oligomers resulting from peroxidase-mediated combination of tyrosine radicals have been characterized for
tyrosine-containing peptides (17-19). The in vivo
occurrence of dityrosines in proteins was first demonstrated in insect
cuticulum (20). Upon elicitor and wound induction of bean and
soybean cell walls, a rapid oxidative cross-linking of the
(hydroxy)proline-rich glycoproteins was demonstrated (21). These
structural proteins contain highly repetitive peptide sequences, among
which the tyrosine-containing Val-Tyr-Lys-Pro-Pro pentapeptide.
In vitro, dityrosines stemming from peroxidase catalysis in
proteins were demonstrated in soluble collagens and in wheat prolamine
(22).
Because both FA and tyrosine are subject to peroxidase-mediated
oligomerization, we rationalized that hetero-coupling of these substrates should be feasible (19). Such peroxidase-mediated hetero-coupling could provide an explanation for the occurrence of
protein-carbohydrate complexes in plant cell walls and the incorporation of FA and other hydroxycinnamic derivatives into lignin
and suberin tissues on a protein template. From an earlier study with
the tripeptide Gly-Tyr-Gly (GYG) and FA, we established conditions that
resulted in covalent linkage of FA and the peptidyl tyrosine (19).
Evidence was provided for the peroxidase-mediated formation of GYG
oligomers linked by dehydrogenation, ranging from dimers to pentamers
that are oxidatively cross-linked to either one or two molecules of FA
(19). In the present study we have further explored the mechanism of
hetero-adduct formation of GYG and FA. Complementary to the
aforementioned studies (2, 3, 5, 9, 10, 13) in which the constituting
precursor moieties in plant cell wall tissue were deduced from the
in vivo synthesized biopolymer, we now present the in
vitro synthesis of the biopolymer by HRP and
H2O2 from the hypothesized FA precursor on a
tyrosine template.
Glycine-tyrosine-glycine (GYG) was obtained from Bachem,
Bubendorf, Switzerland. HRP (type VI-A) and FA were obtained from Sigma. Hydrogen peroxide (30% v/v) was obtained from Merck. All other
chemicals were of analytical grade.
Incubation--
Solutions of 12.44 mM ferulic acid
and 12.44 mM H2O2 (kept on ice) in
50 mM sodium phosphate, pH 8.0, containing 10% (v/v) acetonitrile were continuously and simultaneously added to the incubation mixture using two peristaltic pumps (LKB Bromma 2232 Microperpex S). The incubation mixture, thermostatted at 20 °C, contained 25 mM GYG and 1.25 mg of HRP in an initial volume
of 10 ml of 50 mM sodium phosphate, pH 8.0. 20 ml of the FA
solution and 20 ml of the H2O2 solution were
added over a 15-min period. After another 10 min of incubation, the
reaction mixture was frozen in liquid nitrogen, freeze-dried, and
stored at 4 °C until analysis.
HPLC-MS--
For liquid chromatography-MS analysis, 20 µl of
the reaction mixture (10 mg of lyophilisate redissolved in 100 µl of
MilliQ water) was separated on a 150 × 2.1-mm Alltima C18 column
(Alltech, Breda, The Netherlands) running in 0.03% (v/v)
trifluoroacetic acid in water at a flow rate of 0.2 ml/min. Elution was
performed with a linear gradient of 0-40% acetonitrile in 0.03%
(v/v) trifluoroacetic acid in water over a 45-min period.
Mass spectrometric analysis was performed with a LCQ ion trap (Finnigan
MAT 95, San José, CA) with the use of electrospray ionization and detection in the positive ion mode. The capillary spray
voltage was 2.5 kV, and the capillary temperature was 200 °C. The
instrument was controlled by Xcalibur software. The accuracy of the
mass determinations is ±0.5 Da. After a full MS scan, ions with a mass
to charge (m/z) ratio within 10 m/z units of the most abundant ion were selected
and subjected to collision-induced dissociation (CID, MS2).
The five most abundant product ions resulting from the first stage of
CID were fragmented further by a second stage of CID (MS3).
For nanospray MS, 10 µl of the redissolved reaction mixture was
diluted with acetonitrile (1:1) and loaded in a conductive metal-coated
(coating 3AP) nanospray tip (2-mm internal diameter) (NewObjective,
Woburn, MA) using a Gelloader pipette tip (Eppendorf). Nanospray
conditions used were 25 units of nitrogen backing pressure and 1.2-kV
ionization spray voltage, and the heated desolvation capillary was held
at 200 °C. 500 scans detected in the positive-ion mode were averaged.
After freeze-drying the incubation mixture, a yellow/orange powder
was obtained. Nanoelectrospray MS of the redissolved lyophilisate revealed two dominant series of products (Fig.
1). The most abundant ion series starts
at m/z 830.36 and proceeds with average
m/z increases of 192 to ions with apparent
m/z values of 1022.40, 1215.58, 1407.47, and
1598.87. The other series starts at m/z 978.25 and proceeds with average m/z increases of 192 to
ions with apparent m/z values of 1170.32, 1362.29, 1554.42, 1746.54, and 1938.27. The difference of 192 between
the ions in both series corresponds to FA linked by dehydrogenation.
According to the total ion current after reverse phase HPLC of the
redissolved incubation mixture, species with m/z
829.8, 1021.9, and 978.0 are the three most abundant ions (Fig.
2a). Figs. 2, b-g,
show the single ion chromatograms of the reverse phase HPLC elution of
these and three other selected species with a m/z
of 341.0, 1213.8, and 873.9 (mono-isotopic), respectively. All these
species are singly charged, as apparent from the
m/z difference of 1 between the first 3 13C isotopes in the partial mass spectra obtained by
selection of ions within 10 m/z units from the
ion of interest (data not shown). Therefore, the molecular mass of the
compounds is considered equal to the apparent m/z
values.
The most abundant species is the ion with an apparent
m/z value of 829.8 (mono-isotopic). The mass
corresponds to a hetero-tetramer of 1 GYG linked by dehydrogenation to
a decarboxylated trimer of FA. In the single ion chromatogram of this
compound (Fig. 2, panel c), two main isomers, nearly base
line-resolved, were detected. Upon collision-induced dissociation of
the m/z 829.8 ions, positively charged product
ions with m/z 636.0 and 441.8 result (Fig.
3, panel c), stemming from
consecutive loss of 2 FA moieties (194 Da each). The fragment ions with
m/z 366.8 and 339.0 originate from further
dissociation of the m/z 441.8 ion after
consecutive loss of Gly and CO from the peptide moiety, resulting in
the b2 and a2 ion of the modified tripeptide, as is proved by collision of the isolated m/z 441.8 ion during a second
stage of CID (MS3).
Horseradish Peroxidase-catalyzed Oligomerization of Ferulic Acid
on a Template of a Tyrosine-containing Tripeptide*
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
MATERIALS AND METHODS
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
RESULTS
TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
View larger version (12K):
[in a new window]
Fig. 1.
Nano-electrospray mass spectrum of the
redissolved incubation mixture.
View larger version (16K):
[in a new window]
Fig. 2.
Reverse phase-HPLC-MS chromatogram of the
crude incubation mixture. a, total ion current. Single ion
chromatograms of m/z species of 341.0 (b), 829.9 (c), 1021.9 (d), 1213.8 (e), 873.9 (f), and 978.1 (g).
View larger version (17K):
[in a new window]
Fig. 3.
Fragmentation spectra of CID
(MS2) of m/z species of
829.9 (c), 1021.9 (d), 1213.8 (e), 873.9 (f), 978.1 (g), and 1170.3 (h); for convenience,
the letter designating each fragmentation spectrum corresponds to the
letter indicating the concomitant single ion chromatogram in Fig. 2 and
therefore starts at c.
The second predominant ion, m/z 1021.9 (mono-isotopic), corresponds to dehydrogenation linkage of another FA moiety to the hetero-tetramer with a m/z of 829.8 and is assigned to a hetero-pentamer of 1 GYG linked by dehydrogenation to 4 FA molecules, of which one is decarboxylated. In the single ion chromatogram of this compound, several co-eluting isomers were detected (Fig. 2, panel d). Upon CID of any of these m/z 1021.9 ions, positively charged product ions with m/z 827.6, 635.4, and 441.8 result (Fig. 3, panel d), stemming from consecutive losses of 3 FA moieties (194, 192, and 194 Da). A second stage of CID (MS3) on both the isolated m/z 827.6 and isolated m/z 635.4 fragment ions results in the same m/z 441.8 fragment ion as resulted from CID of the hetero-tetramer, indicating the same structural element in the hetero-pentamer.
In the single ion chromatogram of the third consecutive hetero-oligomer in this series of hetero-oligomers, m/z 1213.8, 1 minor isomer and 2 co-eluting major isomers were detected (Fig. 2, panel e). These are assigned to a hetero-hexamer of 1 GYG peptide linked by dehydrogenation to 5 FA, of which 1 is decarboxylated. Upon CID of any of these isomers, fragment ions with m/z 1019.9 (loss of one FA, 194 Da), m/z 827.8 (loss of second FA, 192 Da), m/z 635.9 (loss of third FA, 192 Da) and predominantly fragment ions of m/z 441.9, 366.8, and 339.0 result (Fig. 3, panel e). The three "fingerprint" ions again demonstrate a constituting moiety similar to that in the preceding compounds in this series.
One higher hetero-oligomer in this series was found (Fig. 1), and this m/z 1407.3 species is assigned to a hetero-heptamer of 1 GYG and 6 FA, of which 1 is decarboxylated. CID of this ionized compound predominantly yielded the fragment ions with m/z 825.9 (loss of 3 FA moieties) and 441.8 (loss of 5 FA moieties) and is concluded to contain the same structural element. The full ion series with m/z values of 829.9, 1021.9, 1214.4, and 1405.8 are assigned to GYG-FA oligomers linked by dehydrogenation containing 3, 4, 5, or 6 FA moieties respectively, each containing the same structural element consisting of a covalent adduct of 1 GYG and decarboxylated FA. The base line-resolved-eluting m/z 341.0 species (Fig. 2, panel b) are assigned to isomeric decarboxylated dehydrodimers of FA.
The third predominant ion in the total ion current, m/z 978.1 (Fig. 2, panel a), is assigned to a hetero-pentamer of 1 GYG linked by dehydrogenation to 4 FA moieties, of which 2 are decarboxylated. Several minor isomers elute separated from two major isomers that co-elute (Fig. 2, panel g). CID of these isomers results in fragment ions with m/z 783.4 and 590.0 (Fig. 3, panel g), corresponding to the consecutive loss of two FA moieties (194 Da). Loss of a third, decarboxylated, FA (148 Da) leads to the main fingerprint fragment ion with m/z 441.8 and the other two fingerprint ions with m/z 366.8 and 339.0 (Fig. 3, panel g). Therefore the core structural element is concluded to be the same as for the single fold decarboxylated series of hetero-oligomers.
The second predominant product in this ion series, m/z 1170.3 (Fig. 1), corresponds to dehydrogenation linkage of another FA moiety to the 2-fold decarboxylated hetero-pentamer with m/z 978.1 and is assigned to a hetero-hexamer of 1 GYG linked by dehydrogenation to 5 FA molecules, of which 2 are decarboxylated. In the single ion chromatogram of this compound (data not shown), several co-eluting isomers were detected at a retention time similar to that of the m/z 978.1 species. Upon ESI and CID of any of these m/z 1170 species, positively charged ions with m/z 976.8, 783.9, 590.0, and 441.8 result (Fig. 3, panel h), originating from consecutive losses of 4 FA moieties (194, 193, 194, and 148). The full series of ions starting at m/z 978.3 (Fig. 1) are therefore assigned to hetero-oliogomers of 1 GYG coupled by dehydrogenation with 4-9 FA moieties, of which 2 are decarboxylated.
The m/z 873.9 ion (Fig. 1 and the chromatogram in
Fig. 2f) is assigned to a hetero-tetramer of 3 nondecarboxylated FA moieties and 1 GYG. This m/z
value of this species corresponds to 2 FA molecules linked by
dehydrogenation and 1 FA molecule not linked by dehydrogenation to GYG.
CID of these ions (Fig. 3, panel f) results in different
product ions as compared with the series of 1- and 2-fold
decarboxylated hetero-oligomers, and the fingerprint ions from the
former series are completely absent. This implies that the ion with a
m/z of 873.9 cannot contain the
m/z 441.9 moiety like the former series of
hetero-oligomers. The main fragment ion is that with
m/z 295.8, corresponding to the GYG ion after loss of the FA moieties. No higher hetero-oligomers containing exclusively nondecarboxylated FA moieties were found. However, two
smaller nondecarboxylated hetero-oligomers, m/z
488 (hetero-dimer) and m/z 680 (hetero-trimer),
were formed in minor amounts (Fig. 1). Interestingly, these compounds
were main products in a previous incubation (19).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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In this study it is shown that the kinetically controlled incubation of FA and GYG with peroxidase and H2O2 results in a complex range of (isomeric) products of different degrees of polymerization. Because isolation of these products for NMR characterization is not straightforward, mass spectrometry including a first and second stage of collision-induced dissociation was the method of choice to elucidate the range of products and their compositional structural elements.
In both the series of 1-fold decarboxylated and the series of 2-fold
decarboxylated hetero-oligomers the difference in mass between the
compounds was always 192 Da, a mass difference expected for
dehydrogenation linkage of FA to each preceding compound in a
constitutive fashion. Unambiguous assignment of the ions of the
compounds to the constituting moieties of the two series of hetero-oligomers is provided by CID. Upon CID of a hetero-oligomer, the
covalent linkages in the proximity of the C-C bond that connects the
four aromatic moieties A, B, C, and Tyr (Fig.
4, structure 5h e.g.) are most
susceptible to fragmentation due to the high probability of the
presence of the proton in this acetal-type structural moiety. After
loss of two neutral FA moieties, the 441.9 fragment results (Fig. 4,
structure 5h4). Further fragmentation of this
fragment (MS3) resulted in the b2 and a2 ions (Fig. 4,
structures 5h6 and 5h7) that
further validates the assignment of the 441.9 fingerprint ion as GYG
linked to the decarboxylated FA moiety. The presence of the fragment
ion of 441.9 (Fig. 3, panels c, d, e,
g, and h) in all MS2 spectra of
compounds of the one- or 2-fold decarboxylated hetero-oligomers and the
fragments of 367 and 339 in the MS3 spectrum of the parent
mass 441.9 clearly indicates that the GYG peptide bound to the
decarboxylated FA moiety (Fig. 4, all structures, ring C) is
always one of the constituting moieties of at least 1 isomer of the 1- and 2-fold decarboxylated hetero-oligomers. Most of the other, isomeric
hetero-tetramers (Fig. 6b, structures 5a-h) are
unlikely to lead to the fingerprint fragment ions as outlined for
isomer 5h in Fig. 4. However, these species may well contribute to the total ion current of the compound of interest but not
participate in the fragmentation pattern of a co-eluting isomer.
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In contrast to the 1- and 2-fold decarboxylated hetero-oligomers, the fragmentation of the 873.9 species (Fig. 3, panel f) does not lead to product ions corresponding to the m/z 441.9 structural element (Fig. 4, structure 5h4). This nondecarboxylated hetero-oligomer results mainly in an m/z 295.8 product ion (Fig. 3, panel f), which corresponds to GYG with no decarboxylated FA moiety attached. This distinct product ion pattern was also found for nondecarboxylated FA-GYG-FA and FA-GYG in a previous study, where GYG was kept in excess over FA (19) during the incubation. Higher hetero-oligomers of this type were not found in those studies nor in the present one.
This discrepancy between the wide range of decarboxylated, further
oligomerized hetero-oligomers and the limited range of nondecarboxylated, maximally tetrameric hetero-oligomers suggests two
different mechanisms for the covalent attachment of FA to the tyrosine
template. Under the conditions applied, the main route occurs via
radical attack on the vinylic bond of the decarboxylated FA dimer (Fig.
5a, structures 2a
and 2b), whereas the minor route proceeds via de- or
nondehydrogenation addition of the non-decarboxylated monomeric FA
radical. The main route deduced from the present data is supported by a
recently proposed mechanism for the lignin peroxidase-catalyzed
homo-trimerization of FA (15). This mechanism comprises an attack by a
phenoxy-FA radical (Fig. 5a, structure 1a) on the
vinylic bond of a decarboxylated FA dehydrodimer (Fig. 5,
structures 2a and 2b). The initially formed
trimeric FA radical species resulting from this attack (Fig.
5b, structures 3a-d) can be oxidized and, after
deprotonation, result in a FA trimer, as was authenticated by one- and
two-dimensional 1H NMR (15). Decarboxylated dehydrodimers
of FA were also formed in the present HRP-mediated incubation of GYG
with FA (Fig. 2, panel b).
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Because GYG radicals are continuously present (Fig.
6a, structures 4a
and 4b) in the hetero-incubation, as follows from the presence of GYG dimers (data not shown), two routes can directly lead
to a hetero-oligomer. Combination of the trimeric FA radical (Fig.
5b, structures 3a-d) with the peptidyl tyrosine
radical of an oxidized GYG (Fig. 5a, structures
4a or 4b) results in a hetero-tetramer comprising 3 FA
and 1 GYG (Fig. 6b, structures 5a-h). Attack of
the GYG radical on the vinylic bond of the decarboxylated FA dimer and
subsequent combination of the resulting hetero-trimeric radical with
another FA radical also leads to the hetero-tetramer, whereas attack of
the hetero-trimeric radical on another decarboxylated FA dimer leads to
a 2-fold decarboxylated hetero-pentamer. These routes, both via
decarboxylated FA dimers, appear to be important in the oligomerization
to higher FA oligomers on the peptide since the higher hetero-oligomers
always are 1- or 2-fold-decarboxylated. Any of the 1-fold
decarboxylated hetero-tetramers (Fig. 6b, structures 5a-h) or 2-fold decarboxylated hetero-pentamers evolved from this reaction path still has several sites for further oligomerization to
higher hetero-oligomers.
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On the basis of the similar product pattern of polymerization of FA by either Lignin peroxidase or HRP, it was suggested that FA oligomerization is governed by radical chemistry rather than enzyme specificity (15). These findings are in agreement with our data, which show that it is the chemistry of the enzymatically primarily formed radical products and especially the chemistry of the decarboxylated dehydrodimers of FA that leads to oligomerization. The GYG-FA hetero-oligomers found in the present study are clearly distinct from the ones found in a previous study (19). This shows that the type of oligomerization is strongly dependent on the substrate concentrations and kinetic control of the reaction.
Our present findings confirm the suggestion of Ward et al. (15) that the peroxidase-induced cross-linking of FA leads to higher oligomers than the trimers they identified by NMR. Furthermore, the attachment of higher oligomers of FA bound to a peptidyl tyrosine would supply a spatial basis for the covalent anchoring of easy diffusible small phenols on a tyrosine template in a plant cell wall protein and supports the often hypothesized template-guided in situ polymerization process of lignin (23-25). During growth or stress, increased levels of FA in the plant can result in differentiation of the type of tissue formed in a similar fashion as the kinetically and stoichiometrically controlled polymerization of FA described in this paper. The phenolic moiety enables oxidation of the molecule as a trigger for oxidative polymerization, whereas the vinylic moiety stabilizes the radical and allows further polymerization after decarboxylative dimerization.
Just as the peptide oligomers in a previous study always appeared to be
blocked for further oligomerization by two nondecarboxylated FA
molecules linked by dehydrogenation to the growing peptide oligomer
(19), low concentrations of the FA monomer in plants can block possible
sites for growth either on an esterified FA or on a protein-tyrosine
template. High levels of FA statistically enhance dimerization to the
decarboxylated FA dimers that enable further polymerization as
established in the present study. The regulation of plant cell wall
growth via control of the level of FA would therefore be amplified by
an intrinsic feature of FA chemistry inevitably associated with FA
concentration in the presence of peroxidases. We suggest that FA and
possibly related cinnamic acid derivatives can exert two opposite
effects on the growth of plant cell wall tissue, solely dependent on
the incident concentration.
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ACKNOWLEDGEMENT |
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We are grateful to Richard Blaauw for helpful discussions.
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FOOTNOTES |
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* This research was supported by the Ministry of Economic Affairs of The Netherlands through the program Innovatief Onderzoek Programma-Industrial Proteins and by AVEBE, DMV-International, Hercules, Quest International, and Unilever.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
d Present address: Dept. of Biomolecular Mass Spectrometry, Utrecht University, Sorbonnelaan 16, 3584 CA Utrecht, The Netherlands.
f Present address: Pamgene BV, P. O. Box 1345, 5200 BJ, Hertogenbosch, The Netherlands.
i Present address: FOM institute for Atomic and Molecular Physics, Amsterdam, The Netherlands.
j Present address: DSM Food Specialties, A. Fleminglaan 1, 2600 MA Delft, The Netherlands.
k To whom correspondence should be addressed. Tel.: 31-317484469; Fax: 31-317484893; E-mail: Fons.voragen@chem.fdsci.wag-ur.nl.
Published, JBC Papers in Press, March 29, 2002, DOI 10.1074/jbc.M201679200
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ABBREVIATIONS |
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The abbreviations used are: FA, ferulic acid; HRP, horseradish peroxidase; HPLC, high pressure liquid chromatography; MS, mass spectrometry; MS2, tandem mass spectrometry; MS3, subsequent CID after spectrometry MS; CID, collision-induced dissociation.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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