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Plant Physiol. (1998) 116: 1163-1168
N-Acylethanolamines: Formation and Molecular
Composition of a New Class of Plant Lipids1
Kent D. Chapman*,
Swati Tripathy,
Barney Venables, and
Arland D. Desouza
Department of Biological Sciences, Division of Biochemistry and
Molecular Biology, University of North Texas, Denton, Texas 76203-5220
(K.D.C., S.T., A.D.D.); and TRAC Laboratories, 113 South Cedar,
Denton, Texas 76201 (B.V.)
 |
ABSTRACT |
Recently, the biosynthesis of an
unusual membrane phospholipid,
N-acylphosphatidylethanolamine (NAPE), was found to
increase in elicitor-treated tobacco (Nicotiana tabacum
L.) cells (K.D. Chapman, A. Conyers-Hackson, R.A. Moreau, S. Tripathy
[1995] Physiol Plant 95: 120-126). Here we report
that before induction of NAPE biosynthesis,
N-acylethanolamine (NAE) is released from NAPE in cultured tobacco cells 10 min after treatment with the fungal elicitor
xylanase. In radiolabeling experiments [14C]NAE (labeled
on the ethanolamine carbons) increased approximately 6-fold in the
culture medium, whereas [14C]NAPE associated with cells
decreased approximately 5-fold. Two predominant NAE molecular species,
N-lauroylethanolamine and
N-myristoylethanolamine, were specifically identified by
gas chromatography-mass spectrometry in lipids extracted from culture
medium, and both increased in concentration after elicitor treatment.
NAEs were found to accumulate extracellularly only. A microsomal
phospholipase D activity was discovered that formed NAE from NAPE; its
activity in vitro was stimulated about 20-fold by mastoparan,
suggesting that NAPE hydrolysis is highly regulated, perhaps by
G-proteins. Furthermore, an NAE amidohydrolase activity that catalyzed
the hydrolysis of NAE in vitro was detected in homogenates of tobacco
cells. Collectively, these results characterize structurally a new
class of plant lipids and identify the enzymatic machinery involved in
its formation and inactivation in elicitor-treated tobacco cells.
Recent evidence indicating a signaling role for NAPE metabolism in
mammalian cells (H.H.O. Schmid, P.C. Schmid, V. Natarajan [1996] Chem
Phys Lipids 80: 133-142) raises the
possibility that a similar mechanism may operate in plant cells.
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INTRODUCTION |
NAPE is a widespread, albeit minor, membrane phospholipid in
animal and plant tissues (Schmid et al., 1990 ; Chapman and Moore, 1993). Its unusual structural features (a third fatty acid moiety linked to the amino head group of PE) impart stabilizing properties to
membrane bilayers (Domingo et al., 1994; LaFrance et al., 1997). NAPE
and its hydrolysis products, NAEs, are known to accumulate in
vertebrate tissues under pathological conditions (for review, see
Schmid et al., 1990). Recently, there has been renewed interest in NAEs
because of the contention that anandamide
(N-arachidonylethanolamine) is an endogenous ligand for the
cannabinoid receptor in mammalian brain (Devane et al., 1992; Fontana
et al., 1995; Schmid et al., 1996). The likely route for NAE formation
in neural and nonneural tissues, although the matter of some debate, is
via the signal-mediated hydrolysis of NAPE (DiMarzo et al., 1994;
Schmid et al., 1996; Sugiura, et al., 1996).
In plants little is known regarding the catabolism of NAPE. In
cottonseed microsomes NAPE was metabolized to NAE or NAlysoPE by PLD-
or PLA-type activities, respectively (Chapman et al., 1995b). However,
the metabolic fate of NAPE in vivo and the factors that regulate NAPE
hydrolysis remain largely unknown. We previously noted that the
biosynthesis of NAPE was increased in elicitor-treated cell suspensions
of tobacco (Nicotiana tabacum L.). Here we extend our
investigations with this model system to examine NAPE catabolism by
plant cells in vivo. NAE was released from NAPE, and it accumulated extracellularly. We identified by GC-MS these tobacco NAEs as N-lauroylethanolamine and
N-myristoylethanolamine. These NAEs were increased in
elicitor-treated cell suspensions. Furthermore, we detected the
enzymatic machinery capable of the release and the degradation of NAEs
in tobacco cells. To our knowledge this represents the first
identification of the NAE molecular species in plant cells. It is
tempting to speculate that NAPE hydrolysis in elicitor-treated plant
cells may be involved in a signaling pathway analogous to that found in
mammalian cells.
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MATERIALS AND METHODS |
Cell Cultures, Elicitor Treatment, and Lipid Extractions
Tobacco (Nicotiana tabacum L. cv KY-14) cell
suspensions were subcultured every 7 d (Chapman et al., 1995a);
cell suspensions in log phase were treated with elicitor (xylanase, 1 µg/mL) as previously described (Chapman et al., 1995a). Control and
experimental treatments were carried out on aliquots of the same
population of cells. Culture supernatants were separated from cells by
filtration. Cells were quick frozen in liquid N2,
powdered in a mortar, and added to boiling 2-propanol in a ratio of
0.8:2 (grams fresh weight of cells:milliliters of 2-propanol). Culture
supernatants were added directly to 2-propanol in the same ratio (v/v)
without freezing. Lipids were extracted from samples with chloroform
(Bligh and Dyer, 1959). For radiolabeling experiments in vivo,
cells in log phase (3-4 d after subculture) were incubated
for 4 h with [1,2-14C]ethanolamine (2 µCi; 3 µCi µmol 1,
NEN) before treatment with elicitor.
Lipid Analyses
To assess radiolabeled ethanolamine-containing lipids, total
lipids were subjected to TLC and radiometric scanning, as described previously (Chapman and Moore, 1993; Chapman et al., 1995a, 1995b). For
structural characterization, NAE was separated from the total lipid
extracts by a combination of Si gel cartridge chromatography and TLC
(Chapman and Moore, 1993; Chapman et al., 1995b).
Ethanolamine-containing lipids were identified on TLC plates by
co-chromatography with authentic standards (Chapman and Moore, 1993;
Chapman et al., 1995b; Sandoval et al., 1995). NAE-enriched fractions
were recovered from Si gel plates in chloroform,
O-acetylated (Fontana et al., 1995), and analyzed by GC-MS
(model 5970 mass spectrometer equipped with a capillary interface to a
model 5890 series II gas chromatograph, Hewlett-Packard). Derivatized
samples in chloroform were chromatographed on a 30-m × 0.25-mm
capillary column (Supelcowax 10, Supelco, Bellefonte, PA) with an oven
temperature program of 100°C for 2 min, increased to 240°C at
10°C/min, and then held at 240°C for an additional 32 min. The
injector temperature was 200°C and the inlet carrier gas (He) was
5 p.s.i. Synthetic NAEs were treated in the same manner, but with
different TLC plates and glassware as a precaution to avoid
contamination with these analytes. Synthetic NAE molecular species were
kindly provided by Dr. Daniele Piomelli (The Neurosciences Institute,
San Diego, CA) and their purity was verified by GC-MS.
Tobacco cell NAPE was purified by TLC and digested with
Streptomyces chromofuscus PLD (Chapman and Moore, 1993). The
NAEs derived from NAPE were derivatized and analyzed by GC-MS (as
described above).
PLD and Amidohydrolase Assays
Tobacco cells (approximately 12 g fresh weight) were
homogenized and microsomes isolated as previously described (Chapman et
al., 1995a, 1995b). Radiolabeled NAPE was prepared fresh for each
experiment from equimolar amounts of
sn-1,2-dioleoylphosphatidyl[2-14C]ethanolamine
(31.5 nmol; 31.8 nCi/nmol, Amersham) and palmitoyl chloride
(Dawson et al., 1969) and purified by one-dimensional TLC (Chapman and
Moore, 1993; Chapman et al., 1995b). Approximately 20,000 dpm were used
per assay, and samples were sonicated briefly after the addition of the
substrate (in 20 µL of diethyl ether). Reactions were carried out at
32°C in a final volume of 1 mL with shaking (120 rpm). Assays were
buffered with potassium phosphate (100 mm, pH 6.0) and were
started by the addition of the substrate, 14C-labeled NAPE. Assay reaction mixtures were
incubated for 30 min and stopped by the addition of 2 mL of boiling
2-propanol. Lipids were extracted from the alcohol-water mixture into
chloroform and separated by TLC (Chapman et al., 1995b). Released NAE
was quantified by radiometric scanning (Bioscan System 200 Imaging Scanner, Bioscan, Washington, DC) and/or liquid-scintillation counting
as described previously (Chapman et al., 1995b).
NAE amidohydrolase activity was measured by following the hydrolysis of
[14C]NAE (release of water-soluble
[14C]ethanolamine).
[14C]NAE was prepared by enzymatic digestion of
[14C]NAPE (prepared as described above) with
S. chromofuscus PLD (Chapman and Moore, 1993). Approximately
5000 dpm of [14C]NAE (in a small volume of
methanol) was added to aliquots of homogenates or microsomes and
incubated for 30 min at 30°C. Lipids were extracted from enzyme
reaction mixtures, and radioactivity in aqueous and organic fractions
was quantified by liquid-scintillation counting. Enzyme activity was
calculated based on the radiospecific activity of the original
[14C]dioleoyl PE used for NAPE synthesis (as
described above).
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RESULTS |
Radiolabeling experiments in vivo (ethanolamine-containing lipids
were specifically radiolabeled with
[1,2-14C]ethanolamine) demonstrated the
occurrence of a xylanase-stimulated NAE release into the culture medium
10 min after treatment (Table I). This
release appeared to be at the expense of NAPE, because radiolabeled
cellular NAPE declined dramatically in elicitor-treated cells. There
was little relative change in other ethanolamine-containing lipids.
Replicate experiments, although varying in the efficiency of
incorporation of radiolabel into lipids, consistently showed a release
of NAE at the expense of NAPE when cells were treated with elicitor.
The decrease in radiolabeled NAPE was not completely accounted for by
the increase in radiolabeled NAE in the culture medium. We speculate
that an amidohydrolase activity (see below) may be responsible for the
subsequent metabolism of NAE.
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Table I.
Release of 14C-labeled NAE from elicitor
(xylanase)-treated tobacco cells (5 g fresh weight)
Values represent the mean dpm and sd of four independent
experiments.
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The NAEs that were specifically released into the tobacco cell culture
medium after xylanase treatment were identified by GC-MS as
N-lauroylethanolamine (NAE 12:0) and
N-myristoylethanolamine (NAE 14:0) (Fig.
1). EIMS and retention times in GC of the
O-acetylated derivatives of the endogenously released NAEs
from tobacco cells were identical with authentic standards. Other types
of NAEs (longer or unsaturated acyl chains) were not detected in
tobacco cell suspensions. There was a measurable increase in both NAE
molecular species 10 min after xylanase treatment, although not as
pronounced as that inferred from radiolabeling experiments. In GC-MS
experiments NAE 12:0 and NAE 14:0 in the culture medium were estimated
to increase about 2-fold after elicitor treatment (from 5.6 to 10.0 and
3.6 to 8.4 ng/g fresh weight of cells, respectively). The apparent
discrepancy between results from radiolabeling experiments and results
from GC-MS experiments may be attributable to losses during
processing/derivatization of samples for GC.
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| Figure 1.
EIMS of NAEs. O-Acetylated
derivatives of putative tobacco NAE 12:0 (A), synthetic NAE 12:0 (B),
synthetic NAE 14:0 (C), and putative tobacco NAE 14:0 (D) were analyzed
by GC-MS. Retention times in GC and molecular ions [M]+
in EIMS of tobacco NAEs were identical to those of synthetic compounds
(33.5 min and m/z 285 for NAE 12:0; 45.6 min and
m/z 313 for NAE 14:0). Before GC-MS, tobacco NAEs were
partially purified by TLC from total lipid extracts and derivatized
according to Fontana et al. (1995). The synthetic NAEs were treated in
the same manner, but with different TLC plates and glassware as a precaution to avoid contamination.
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Single-ion chromatograms (m/z 145, major diagnostic ion
characteristic of NAEs) for NAE-enriched samples from cells and culture medium of unelicited and elicitor-treated cells are compared in Figure
2. NAE 12:0 and NAE 14:0 (identified
by their respective EIMS, Fig. 1) were detected in culture medium, but
were barely detectable in lipids from cells. These data suggest that
NAEs are released into the extracellular medium and do not accumulate intracellularly. The low levels of intracellular NAEs may be caused by
the degradation of these molecules by an amidohydrolase activity (see
below). In separate experiments we confirmed that lauric acid and
myristic acid were present endogenously as the predominant N-acyl constituents of tobacco NAPE (not shown). Longer
N-acyl chains, as previously identified in cottonseed
(Chapman and Moore, 1993; Sandoval et al., 1995), were not detected in
tobacco cells. This may be indicative of different physiological roles
for NAPE metabolism in these different cell types or different
developmental stages (germinated seeds versus cell suspensions).
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| Figure 2.
Single-ion chromatograms at m/z 145 of O-acetylated, NAE-enriched samples from unelicited
(control) cells and medium and xylanase-treated cells and medium. Peaks
identified by electron-impact MS as NAE 12:0 and NAE 14:0 are labeled.
Other lipid molecules in the chromatograms did not show mass spectra
characteristic of NAEs (Fontana et al., 1995; see text).
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Two other abundant lipid species in these chromatograms, one at 48.5 min and one at 59.8 min, were present in the cell and medium samples,
but appeared more abundant in the medium after elicitor treatment
(similar to the results for NAEs). EIMS of these species (not shown)
indicated that they were likely bis-O-acetylated derivatives
of monoacylglycerols, palmitylglycerol and stearylglycerol, respectively. Diagnostic ions in both spectra of
[M-175]+, representing the fatty acyl moiety,
were evident (at m/z 239 for palmityl and at m/z
267 for stearyl). Also, the prominent ion in both spectra was at
m/z 159, which would correspond to the derivatized glyceryl
fragment ion. Although our experimental results do not address the
origin of these lipids, their occurrence suggests the involvement of
PLA (and phospholipase C, or PLD and phosphatidic acid phosphatase)
action on membrane phospholipids.
A microsomal enzyme activity from tobacco cells was identified that
hydrolyzed NAPE to NAE in vitro (Fig. 3).
The tobacco PLD-type activity was present in cytosolic fractions as
well. NAE formation by tobacco microsomes was stimulated somewhat by Ca2+ and GTP- -S. However, the activity was
inhibited by concentrations of Triton X-100 that are known to stimulate
a similar PLD activity previously characterized in mammalian liver
(Schmid et al., 1996). Most notably, the tobacco microsomal PLD
activity toward exogenously supplied [14C]NAPE
was increased about 20-fold in the presence of mastoparan, suggesting
the possibility of G-protein-mediated regulation of NAPE hydrolysis. It
should be pointed out that a direct stimulation of tobacco PLD activity
by mastoparan, as opposed to involvement of an activated G-protein,
cannot be ruled out. The xylanase protein preparation itself had no
hydrolytic activity toward NAPE in vitro, and adding elicitor to the
microsomes did not stimulate PLD activity above control levels (not
shown).
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| Figure 3.
NAE formation from NAPE by tobacco microsomal PLD.
Plus signs below the treatment indicate the addition of that component to the reaction mixture (microsomes, 0.04 mg of protein; cytosol, 0.025 mg of protein; calcium, 15 mm; Triton X-100, 2 mg/mL; GTP, 3 mm; GTP--S, a nonhydrolyzable GTP analog, 25 µm; and mastoparan, 25 µm). Reactions were
carried out at 30°C in a final volume of 1 mL with shaking (120 rpm).
Assays were started by adding the substrate (14C-labeled
NAPE) and stopped by adding 2-propanol. Released NAE was quantified by
radiometric scanning (System 200 Imaging Scanner, Bioscan) (Chapman et
al., 1995a) of TLC separations of lipids extracted from reaction
mixtures. Values are the averages of duplicate samples (in all cases
the range was less than 14%) and are representative of several
replicate experiments.
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Because only trace levels of NAEs were detected in cellular lipid
extracts, we postulated that there was an intracellular NAE
amidohydrolase activity like that found in some mammalian tissues
(Desarnaud et al., 1995; Ueda et al., 1995) that could catalyze the
hydrolysis of NAE. Such an activity was readily detected in tobacco
cell homogenates and membranes (Table
II), although the latter accounted for
only a small proportion of the total activity. This hydrolytic activity
released water-soluble radioactivity from
[14C]NAE (radiolabeled on carbon 2 of the
ethanolamine) and was inactivated by boiling the cell fractions.
Consequently, we conclude that an amidohydrolase-type activity is
present in tobacco cells and could be responsible for the rapid removal
of free intracellular NAE.
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Table II.
Enzymatic hydrolysis of
N-palmitoyl[2-14C]ethanolamine by homogenates and
membranes of tobacco cells
Activity was quantified as the amount of water-soluble radioactive
[2-14C]ethanolamine released after 30 min and is
attributed to an amidohydrolase-type enzyme. Values represent the
average enzyme activity and sd from three independent
cell-fractionation experiments.
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DISCUSSION |
Recent studies indicated that NAPE biosynthesis was increased in
elicitor-treated tobacco cells (Chapman et al., 1995a). Approximately 2 h were required for the maximum induction of NAPE biosynthesis, as judged by enzyme activity and lipid accumulation, suggesting that
NAPE biosynthesis was not involved in the early membrane permeability-related events of pathogen perception. Instead, we hypothesized that the increase in NAPE biosynthesis might be required to replenish NAPE levels depleted by the signal-mediated hydrolysis of
NAPE. The results presented here are consistent with such a hypothesis.
The tobacco-cell/fungal-elicitor model system has been used by a number
of research groups to identify and characterize various components
involved in plant defense responses. These include changes in ion flux
across the plasma membrane (Bailey et al., 1992), changes in plasma
membrane lipid metabolism (Moreau and Presig, 1993; Moreau et al.,
1994; Chapman et al., 1995a), transient protein (Tyr) phosphorylation
(Suzuki and Shinshi, 1995), induction of phytoalexin biosynthesis
(Moreau and Presig, 1993), induction of ethylene biosynthesis (Anderson
et al., 1993), induction of pathogenesis-related protein expression
(Lotan and Fluhr, 1990), and induction of defense gene expression
(Bailey et al., 1995; Suzuki et al., 1995). Recently, a receptor for
the xylanase protein was identified in tobacco plasma membranes
(Hanania and Avni, 1997), and a single gene trait has been linked to
xylanase sensitivity (Bailey et al., 1993). Hence, our work on the
regulation of NAPE metabolism in tobacco cells treated with xylanase
may be relevant to signal-transduction pathways in plant defense
responses. Additional work to characterize the biological effects of
NAEs on plant cells will be necessary to understand the possible
role of NAEs in plant cell signaling.
Other workers have implicated PLD induction in plant pathogen
perception or wounding (Ryu and Wang, 1996; Young et al., 1996; Wang,
1997). Young et al. (1996) reported changes in plasma membrane distribution of a rice PLD in response to bacterial pathogens. In other
studies a mastoparan-stimulated PLD activity was reported in carnation
petals and Chlamydomonas eugametos cells; however, the
endogenous lipid substrate was not identified (Munnik et al., 1995).
Our results are consistent with an emerging role for a highly regulated
PLD activity(ies) (Causier and Milner, 1996; Ryu and Wang, 1996; Pappan
et al., 1997; Wang, 1997) that is involved in signal transduction
pathways in plants. Moreover, our studies identify at least one type of
endogenous membrane lipid substrate for PLD and characterize for the
first time to our knowledge the structure of the hydrolysis products,
NAEs.
The NAEs identified here have shorter acyl chains than the
biologically active neurotransmitters (anandamide; Devane et al., 1992)
or the closely related sleep-inducing compounds (oleoylamide; Cravatt
et al., 1995) found in mammalian brain. Nonetheless, there are many
similarities in NAE metabolism evident from our results that are shared
between plants and animals. First, the molecular origin of NAE appears
to be a relatively minor membrane phospholipid (NAPE). Second, NAEs are
released from NAPE in a signal-mediated fashion and accumulate
extracellularly. A PLD appears to catalyze the formation of NAE and an
amidohydrolase appears to be responsible for its intracellular
degradation. Whereas a signaling role for these NAEs in plants has yet
to be firmly established, the emerging role for NAE as a signaling
molecule in mammalian tissues (Schmid et al., 1996) and the
similarities in its metabolism suggest that this mechanism may be
widespread in evolution.
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FOOTNOTES |
1
This research was supported by grants from the
U.S. Department of Agriculture-National Research Initiative Competitive
Grants Program to K.D.C., agreement nos. 94-37304-1230 and
96-35304-3862.
*
Corresponding author; e-mail kent{at}jove.acs.unt.edu; fax
1-940-565-4136.
Received September 9, 1997;
accepted November 26, 1997.
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ABBREVIATIONS |
Abbreviations:
EIMS, electron-impact mass spectrum(a).
NAE, N-acylethanolamine.
NAPE, N-acylphosphatidylethanolamine.
PE, phosphatidylethanolamine.
PLA, phospholipase A.
PLD, phospholipase D.
X:Y, a fatty acyl group containing X carbon atoms and Y
cis double bonds.
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ACKNOWLEDGMENTS |
We thank Dr. Daniele Piomelli for providing the synthetic NAEs
and also for insightful discussions regarding NAPE metabolism in
mammalian neurons. We also thank Drs. James D. Anderson, Bryan Bailey,
and James Jennings for helpful discussions relating to elicitor
treatment of tobacco cells.
| |
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Top
Abstract
Introduction