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In vitro and in vivo effects of myo-active peptides on larvae of the tomato moth Lacanobia oleracea and the cotton leaf worm Spodoptera littoralis (Lepidoptera; Noctuidae).

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60
Matthews et al.
Archives of Insect Biochemistry and Physiology 69:60–69 (2008)
In Vitro and In Vivo Effects of Myo-Active Peptides
on Larvae of the Tomato Moth Lacanobia oleracea
and the Cotton Leaf Worm Spodoptera littoralis
(Lepidoptera; Noctuidae)
H. J. Matthews,* N. Audsley, and R. J. Weaver
Neuropeptides from five different neuropeptide families [Manduca sexta allatostatin (Manse-AS), and Manse-AS deletion
analogue5-15, M. sexta allatotropin (Manse-AT), leucomyosuppressin, perisulfakinin, and myoinhibitory peptide I (MIP I)]
were assayed for their ability to affect the development and food consumption of penultimate and last larval instars of two
lepidopteran species, L. oleracea and S. littoralis. Injections of Manse-AS deletion analogue5-15, Manse-AT, perisulfakinin, and
MIP I had no observable effects on development, food consumption, or mortality compared to controls. Single injections of
Manse-AS significantly reduced the weight gain and increased mortality of L. oleracea and S. littoralis larvae compared to
controls. By contrast, feeding Manse-AS to L. oleracea had no such effects. These differences were probably due to the
degradation of the peptide by digestive enzymes in the foregut of L. oleracea. In studies in vitro, perisulfakinin, and MIP I had
no effect on the spontaneous foregut contractions of L. oleracea larvae. Leucomyosuppressin, however, had myoinhibitory
effects on the foregut. Single injections of leucomyosuppressin significantly reduced the weight gain and food consumption of
L. oleracea and S. littoralis larvae and increased mortality. These data suggest that the deleterious effects observed in vivo
were due to the myoinhibition by Manse-AS and leucomyosuppressin of the normal peristaltic movements of the gut either by
the intact peptide or by its cleavage products resulting from degradation in the haemolymph. Arch. Insect Biochem. Physiol.
69:60–69, 2008. © 2008 Wiley-Liss, Inc.
KEYWORDS: Allatostatin; allatotropin; leucomyosuppressin; perisulfakinin; myoinhibitory peptide
INTRODUCTION
Lepidopteran pests cause damage largely through
their feeding activities. Feeding and crop motility
are controlled by the stomatogastric nervous system
(Penzlin, 1985), and central to this system is the
frontal ganglion, which, in Lepidoptera, controls the
muscles of the foregut (Bushman and Nelson, 1990;
Miles and Booker, 1994, 1998). Muscular activity
of the foregut of larval Lepidoptera is regulated by
the myoinhibitory allatostatins and myostimulatory
allatotropin, which work together antagonistically
(Duve et al., 1999, 2000). In larvae of the tomato
moth Lacanobia oleracea, Manduca sexta allatostatin
(Manse-AS) (pEVRFRQCYFNPISCF-OH), M. sexta
allatotropin (Manse-AT) (GFKNVEMMTARGFNH2), and allatostatins of the Y/FXFGL-NH2 family are localized in the frontal ganglion, are
detected in the recurrent nerve that innervates the
muscles of the foregut, and have myoactivity on
Central Science Laboratory, Sand Hutton, York, United Kingdom
Contract grant sponsor: Pesticides Safety Directorate (DEFRA).
*Correspondence to: H. J. Matthews, Central Science Laboratory, Sand Hutton, York, YO41 1LZ, UK. E-mail: j.matthews@csl.gov.uk
Received 10 April 2007; Accepted 23 June 2008
© 2008 Wiley-Liss, Inc.
DOI: 10.1002/arch.20265
Published online in Wiley InterScience (www.interscience.wiley.com)
Archives of Insect Biochemistry and Physiology
October 2008
Effects of Myo-Active Peptides on Lepidoptera
the foregut (Duve et al., 2000; Audsley et al., 2005).
In larvae of the cotton leaf worm, Spodoptera
littoralis, a similar peptide profile has also been
identified from the frontal ganglion (Audsley et al.,
2005).
Given the role of these neuropeptides in foregut
motility, there is an interest in their use to suppress feeding of insect pests. Injection of ManseAS into L. oleracea larvae resulted in a reduction in
larval growth and feeding, and increased mortality
compared to control injected insects, most likely
due the myoinhibitory effects of Manse-AS on the
foregut. In contrast, injection of Manse-AT had no
effect (Audsley et al., 2001). Manse-AS5-15 is a deletion peptide produced by cleavage of Manse-AS
by haemolymph enzymes (Audsley et al., 2002b),
and inhibits foregut contractions in the L. oleracea
foregut in vitro at concentrations similar to those
of the intact peptide (Audsley et al., 2001).
As well as the allatostatins, other myoinhibitory
peptides inhibit gut contractions in various insects.
Six myoinhibitory peptides (termed MIP I–VI) were
identified from the ventral nerve cord of M. sexta,
and were shown to inhibit peristalsis of the anterior hindgut in adult M. sexta (Blackburn et al.,
1995, 2001). The most abundant and the most potent of these peptides was MIP I (AWQDLNSAWamide; Blackburn et al., 2001).
Leucomyosuppressin (pEDVDHVFLRF-NH2) is
a FMRF-related peptide (FaRP) originally isolated
from the cockroach Leucophaea maderae (Holman
et al., 1986). It has since been identified in the cockroaches, Periplaneta americana and Blattella germanica (Predel et al., 2001; Aguilar et al., 2004), the
honey bee Apis mellifera (Audsley and Weaver,
61
2006), and in species of Mantophasmatodea
(Predel et al., 2005), but as yet, not in lepidopteran
species. Leucomyosuppressin inhibits contractions
of the foregut and hindgut in P. americana (Predel
et al., 2001), L. maderaea (Cook and Wagner, 1991),
and B. germanica (Aguilar et al., 2004), and inhibits spontaneous midgut contractions in the cockroach Diploptera punctata (Fusé and Orchard, 1998).
When injected into adult B. germanica, it inhibited
food intake in a dose-dependant manner (Aguilar
et al., 2004).
Perisulfakinin (EQFDDY(SO3H)GHMRF-NH2)
is also a FaRP, isolated from the cockroach P.
americana (Veenstra, 1989). Perisulfakinin displays
sequence homology with vertebrate hormones of
the gastrin/CCK family, which are satiety-inducing peptides (Lee et al., 1994). In the cockroach
B. germanica, it induced foregut and hindgut contractions, and inhibited food intake when injected
into the haemolymph (Maestro et al., 2001). Perisulfakinin inhibits food intake in nymphs of the
locust, Schistocerca gregaria (Wei et al., 2000), although its mode of action was not determined.
The aim of the present study was to compare
the effects of various structurally different neuropeptides (Fig. 1) from different neuropeptide
families on feeding and development in larvae of
two species of lepidopteran pest insects, L. oleracea
and S. littoralis.
MATERIALS AND METHODS
Insects
Lacanobia oleracea and S. littoralis were reared
as described by Corbitt et al. (1996) on an artifi-
Fig. 1. Amino acid sequences and common
names of peptides used in this study.
Archives of Insect Biochemistry and Physiology
October 2008
62
Matthews et al.
cial diet and kept at 20°C, 65% relative humidity,
in a 16-h light:8-h dark photocycle. Larvae were
fed on a maize-based noctuid artificial diet (BioServ, Frenchtown, NJ).
were also tested on S. littoralis only: S. littoralis physiological saline (Davenport and Wright, 1985),
Dulbecco’s phosphate-buffered saline (Sigma), and
M. sexta saline (Chamberlin, 1989).
Peptides
Injection Assays With Neuropeptides
Manduca sexta allatostatin, deletion analogue
Manse-AS5-15 and MIP I were custom synthesized
at the Advanced Biotechnology Centre, Imperial
College, London, UK. Manduca sexta allatotropin
was purchased from Sigma-Aldrich (UK). Leucomyosuppressin and perisulfakinin were purchased
from Bachem (UK).
Prior to injection, Manse-AS and Manse-AS5-15
were dissolved in dimethyl sulphoxide (DMSO).
Manse-AT, MIP I, perisulfakinin, and leucomyosuppressin were dissolved in water. Newly ecdysed
fifth instar larvae (0–24 h old) of L. oleracea or S.
littoralis were anaesthetized under CO2 and injected
using a Hamilton syringe with either 3.8 µg (2
nmol) Manse-AS in 1 µl DMSO, 2.8 µg (2 nmol)
Manse-AS5-15 in 1 µl DMSO, 1.5 µg (1 nmol) ManseAT in 1 µl water, 6.2 µg (5.7 nmol) MIP I in 1 µl
water, 5.5 µg perisulfakinin (3.6 nmol) in 1 µl water or 18.9 µg (15 nmol) leucomyosuppressin in 3
µl water. Control insects were injected with the same
volumes of either DMSO or water as appropriate.
Following injection, larvae were weighed and
placed individually in 250-ml plastic containers
(Autobar Ltd, Hemel Hempstead, UK) lined with
tissue paper and covered with a perforated lid. Larvae were fed artificial diet of known wet weight,
and kept under rearing conditions. The weight of
the larvae was subsequently monitored every two
or three days until they either pupated or died. All
data are means ± SE, n = 20–30. Food consumption was calculated by subtracting dry weight of
remaining diet (dried to constant weight at 90°C)
from converted dry weight of diet given to individual larvae. Dry weight of diet given to larvae
was determined using a conversion factor calculated from the ratio of wet weight to dry weight of
diet standards.
Foregut Contraction Assay
Sixth instar L. oleracea or S. littoralis larvae that
had been starved overnight were anaesthetised with
CO2 and dissected in a longitudinal well made in
the wax base in a dissecting dish. The dorsal surface
was opened by cutting from the level of the second
proleg to the back of the head capsule, allowing exposure of the foregut and anterior midgut. The cuticular flaps were pinned down and the foregut
washed several times with 200 µl of physiological
saline of the following composition (mM): Na+ 154,
K+ 2.7, Ca2+ 1.8, Cl– 160, hydroxyethylpiperazine
ethanesulphonic acid (HEPES) 12, and glucose 22,
pH 7.2 (Cook and Holman, 1978). The foregut
preparation was then immersed in 200 µl saline.
The number of peristaltic contractions were monitored over two 2-min periods to establish baseline
contractions. Insects were discarded if there was no
gut movement. Control saline was replaced with the
same volume of solution containing either leucomyosuppressin at concentrations between 10–12 and
10–7 M, MIP I at concentrations of 10–7 and 10–6 M,
or perisulfakinin at concentrations of 10–7 and 10–
6
M, and contractions monitored as above. Preliminary experiments had determined the most suitable
concentration range. Ten different larvae were used
for each concentration of peptide tested. The frequency of contractions in the presence of peptide
was then compared to the frequency of control
(baseline) levels. The following physiological salines
Feeding Assays With Manse-AS
Prior to feeding, Manse-AS was dissolved in
DMSO. Newly ecdysed fifth instar larvae (0–24 h
old) of L. oleracea that had been starved overnight
were fed a small piece of noctuid artificial diet
containing either 15 µg (7.9 nmol) Manse-AS in 1
µl DMSO or 1 µl DMSO only (controls). Larvae
Archives of Insect Biochemistry and Physiology
October 2008
Effects of Myo-Active Peptides on Lepidoptera
63
were left for 5 hours to consume the diet. Those
that did not consume the whole piece were discarded from the experiment. Larvae were then
weighed and subsequently monitored as for the
injection assays. All data are means ± SE (n = 20).
when tested in vitro, even with the addition of 10–8
M Manse-AT to stimulate contractions. Therefore,
none of the peptides (leucomyosuyppressin, MIP
I, or perisulfakinin) were tested in vitro on the foregut of S. littoralis.
Statistical Analysis
Effects of Neuropeptides on the Development and
Survival of L. oleracea Larvae
Dose-response results were analysed using
probit analysis. Larval weights and diet weights
were analysed using ANOVA followed by a multiple comparison test (Tukey’s) (significance level
P < 0.05). Larval survival was analysed using the
χ2 test (significance level P < 0.05).
RESULTS
Effects of Peptides on L. oleracea Foregut Peristalsis
Leucomyosuppressin had an inhibitory effect on
spontaneous contractile activity of the foregut of
L. oleracea causing a complete inhibition at 10–7
M. The inhibitory effects were rapid in onset, and
a dose-response curve for frequency of foregut contractions was produced between 10–12 M and 10–7
M leucomyosuppressin, giving an apparent EC50 of
2.2 × 10–11 M (Fig. 2).
Neither MIP I or perisulfakinin influenced contractions of the L. oleracea foregut at doses up to
10–6 M.
Effects of Peptides on S. littoralis Foregut Peristalsis
None of the physiological salines tested on S.
littoralis maintained foregut contractions in larvae
In all experiments, control mortality was low,
ranging from 0 to 16%.
Following injection into fifth instar L. oleracea,
Manse-AS had a significant effect on the subsequent
growth and development of larvae. The mean weight
of Manse-AS-injected larvae was significantly lower
than that of controls (Fig. 3). In addition, the percentage mortality of treated larvae was significantly
higher (45%) compared to controls.
In contrast, feeding Manse-AS to L. oleracea had
no effect on the subsequent weight of larvae or
their mortality compared to controls.
When leucomyosuppressin was injected into fifth
instar L. oleracea, the weight of larvae post-injection
was significantly reduced compared to controls (Fig.
4). Although not significantly different to controls,
mortality of leucomyosuppressin-injected larvae increased to 32% at 14 days post-injection.
Neither Manse-AS5-15, allatotropin, MIP I, or
perisulfakinin had any significant effects on the
development of larval L. oleracea at the doses tested.
There were no significant differences between the
weight of control and peptide-injected larvae. There
were also no significant differences between survival of control and peptide-injected larvae in any
of the above treatments.
Fig. 2. Dose-response curve for the inhibition of peristalsis of the foregut of
sixth instar L. oleracea larvae by leucomyosuppressin. Means ± SE, n = 10.
Archives of Insect Biochemistry and Physiology
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Matthews et al.
Fig. 3. The effects of Manse-AS
on L. oleracea and S. littoralis larval weight. Each histogram bar
represents mean weight (mg) of
larval L. oleracea or S. littoralis
injected as day 1 fifth instar
with either 3.8 µg Manse-AS in
1 µl DMSO or 1 µl DMSO (controls). Error bars represent standard errors.
Effects of Neuropeptides on the Development and
Survival of S. littoralis Larvae
In all experiments, control mortality was low,
ranging from 0 to 8%.
The injection of Manse-AS into fifth instar S.
littoralis larvae caused a significant reduction in
weight gain compared to controls (Fig. 3). The
survival of Manse-AS-injected larvae was also affected. Mortality was 32% in Manse-AS-injected
larvae and this was found to be significantly
higher than controls.
Spodoptera littoralis larvae that had been injected
with either allatotropin, MIP I, or perisulfakinin
did not exhibit any significant effects on larval development compared to their respective controls.
The weight of S. littoralis larvae from day 1 fifth
instar through to pupation was not significantly
affected by injection of the above peptides. Mortality of larvae post-injection was low in both
allatotropin- and MIP 1–injected insects, ranging
from 4 to 8%, and was not significantly different
than controls. Mortality in perisulfakinin-injected
insects was significantly higher than controls.
Injection of leucomyosuppressin into fifth instar S. littoralis larvae caused a significant reduction
in weight gain throughout their development to
pupation compared to controls (Fig. 4). Mortality
of larvae was also significantly higher for peptideinjected larvae (48%) compared to controls.
Effects of Neuropeptides on Food
Consumption of L. oleracea
Lacanobia oleracea larvae that had been injected
with either Manse-AS5-15, MIP I, or perisulfakinin
Fig. 4. The effects of leucomyosuppressin on L. oleracea
and S. littoralis larval weight.
Each histogram bar represents
mean weight (mg) of larval L.
oleracea or S. littoralis injected as
day 1 fifth instar with either
18.9 µg leucomyosuppressin in
3 µl water or 3 µl water (controls). Error bars represent standard errors.
Archives of Insect Biochemistry and Physiology
October 2008
Effects of Myo-Active Peptides on Lepidoptera
did not show any significant differences in food
consumption compared to controls.
Feeding Manse-AS to fifth instar larvae had no
significant effect on their subsequent food consumption through to pupation compared to controls.
Injection of leucomyosuppressin into fifth instar
L. oleracea caused a significant reduction in food consumption compared to water-injected controls. Food
consumption was reduced in leucomyosuppressininjected larvae throughout their development to
sixth instar (Fig. 5). At its maximum (day 9), each
control larva had consumed an average of 275 mg
food (dry weight) compared to 179 mg for leucomyosuppressin-injected larvae.
Effects of Neuropeptides on Food
Consumption of S. littoralis
Spodoptera littoralis larvae that had been injected
with either MIP I or perisulfakinin did not show
any significant differences in food consumption
post-injection compared to their controls.
Injection of leucomyosuppressin, however,
caused a significant reduction in the amount of
food consumed by the larvae post-injection compared to water-injected controls. This reduction was
apparent throughout their development to sixth
instar (Fig. 5). The maximum amount of food was
consumed at day 11, with an average of 216 mg
(dry weight) per control larva compared to 171 mg
per leucomyosuppressin-injected larva.
65
DISCUSSION
Larvae of the two noctuid species L. oleracea and
S. littoralis possess similar peptide profiles from
their frontal ganglia. Three types of peptides were
identified from frontal ganglion extracts; ManseAS, Manse-AT, and F/YXFGL-NH2 allatostatins, implicating them in the regulation of feeding activity
(Audsley et al., 2005). This was confirmed in larval L. oleracea with Manse-AS, which inhibits foregut peristalsis in vitro and suppresses feeding
activity causing mortality following injection into
the haemolymph (Audsley et al., 2001). Results
from the present study, which used a lower dose
(3.8 µg Manse-AS per larva), showed similar but
less pronounced effects, as might be expected given
its dose-dependent effects (Audsley et al., 2001).
Manse-AS was also biologically active following injection into larval S. littoralis at the same dose, causing a reduction in weight gain and increased
mortality compared to controls. In vitro studies
have confirmed the ability of high doses of ManseAS to inhibit foregut contractions completely in L.
oleracea (Duve et al., 2000; Matthews et al., 2006;
2007) and it is probably this myoinhibition that
is causing the effects on weight gain and mortality
observed in this and other studies (Audsley et al.,
2001). Although the in vitro activity of Manse-AS
on the foregut of S. littoralis has not been shown,
it is likely that Manse-AS is acting in vivo in a
myoinhibitory manner in this species given the
Fig. 5. The effects of leucomyosuppressin
on L. oleracea and S. littoralis food consumption. Each histogram bar represents
mean dry weight (mg) of cumulative food
consumption by larval L. oleracea or S.
littoralis injected as day 1 fifth instar with
either 18.9 µg leucomyosuppressin in 3 µl
water or 3 µl water (controls). Error bars
represent standard errors.
Archives of Insect Biochemistry and Physiology
October 2008
66
Matthews et al.
similarity of the results obtained. Injection of 1
nmol (ca. 1.9 µg) Manse-AS, however, twice daily
into a different but related species, the fall armyworm S. frugiperda, had little effect on growth and
development (Oeh et al., 2001).
Although Manse-AT has myostimulatory effects
on the foregut of L. oleracea (Duve et al., 2000;
Audsley et al., 2005; Matthews et al., 2007), it did
not affect development or food consumption when
injected (this study; Audsley et al., 2001). Larval S.
littoralis were also developmentally unaffected by this
peptide, in contrast to the effects reported by Oeh
et al. (2001), where twice daily injections of ManseAT into S. frugiperda larvae reduced weight gain and
increased mortality in this closely related species.
In addition, the duration of the penultimate and
the last larval instars were prolonged in the survivors and injections of Manse-AT into adult female
moths shortened the moths’ lifespan thereby reducing the total number of deposited eggs. The authors suggest that the effects of Manse-AT could
have been caused by the intact peptide or by its
cleavage products, since it was rapidly degraded by
S. frugiperda larval haemolymph with a half-life
ranging from 1 to 5 min (Oeh et al, 2001). Although Oeh et al. (2001) did not determine the
mode of action of Manse-AT in vivo in S. frugiperda,
its myotropic effects in vitro have been confirmed
in other Noctuid species, for example Heliothis
virescens (Oeh et al., 2003), H. armigera (Duve et
al., 1999), and L. oleracea (Duve et al., 2000;
Audsley et al., 2005).
The contrasting results between different lepidopteran species are difficult to explain. They may
largely be due to the different rates of degradation
of the two peptides by haemolymph enzymes and/
or the relative activities of cleavage products resulting from this degradation. The degradation of
Manse-AS by haemolymph from L. oleracea is rapid
(half-life ca. 3.5 min), resulting in three major cleavage products (Manse-AS5-15, 6-15, 7-15; Audsley et al.,
2002b). In vitro, only Manse-AS5-15 had any myoinhibitory activity on the foregut of L. oleracea larvae (Audsley et al., 2001; Matthews et al., 2006).
It is, therefore, surprising that injection of the
cleavage product Manse-AS5-15 had no effect on L.
oleracea larvae in vivo. However, when injected,
Manse-AS5-15 will be subject to degration by aminopeptidases in the haemolymph that sequentially
cleave amino acids from the N-terminus (Audsley
et al., 2002b). The removal of a single amino acid
from Manse-AS5-15 would render this peptide inactive in vivo, because the truncated analogue ManseAS6-15 has no biological activity on the foregut of
L. oleracea larvae (Matthews et al., 2006). This metabolism may occur before the truncated peptide
can interact with the receptor, whereas the time
taken for aminopeptidases to inactivate the intact
peptide (Manse-AS1-15) by the sequential removal
of five N-terminal residues, may enable an active
truncated form of the peptide to interact with the
receptors in the foregut.
In contrast, feeding Manse-AS to L. oleracea larvae had no significant effects on growth, development, survival, or food consumption. This lack
of measureable activity is most likely due to the
enzymatic inactivation of the peptide in the gut
and the ability of the peptide to penetrate the gut
epithelium to reach its target receptors on the
basolateral side of the gut. Audsley et al. (2002a)
report that Manse-AS was rapidly degraded to
Manse-AS4-15 and Manse-AS6-15 by trypsin-like enzymes associated with the foregut. Given that the
truncated analogue Manse-AS5-15 has myoinhibitory
activity, it would be reasonable to assume that the
larger product, Manse-AS4-15 would also be active.
However, this has not been tested in vitro.
In the present study, leucomyosuppressin was the
only other peptide tested, that had a significant effect on the growth and mortality of L. oleracea and
S. littoralis larvae. This peptide has a very different
structure to the allatostatins and it must be assumed
that different receptors are responsible for its actions
(Duve et al., 1995). Indeed, there is evidence from
other species that this is the case (Cook et al., 1993;
Vilaplana et al., 2004). Leucomyosuppressin had a
powerful myoinhibitory effect on both the foregut
and hindgut of adult B. germanica (Aguilar et al.,
2004). The authors suggest that these myoinhibitory
effects result in the accumulation of food in the
foregut, which in turn inhibits food intake by the
cockroaches because of the persistence of signals
Archives of Insect Biochemistry and Physiology
October 2008
Effects of Myo-Active Peptides on Lepidoptera
from gut stretch receptors. Since leucomyosuppressin had a myoinhibitory effect on the L. oleracea
foregut in vitro, this may explain the effects observed in vivo in L. oleracea and, by inference, in
S. littoralis.
Although perisulfakinin (like leucomyosuppressin) is a FaRP, it had no effect when tested in
vitro on the foregut of L. oleracea or when injected
into L. oleracea or S. littoralis. Perisulfakinin belongs to a family of insect neuropeptides known
as the sulfakinins, which have myotropic and
antifeedant effects (Maestro et al., 2001; Orchard
et al., 2001). Mousley et al. (2004) found perisulfakinin to be inactive against the body wall
muscle of the nematode Ascaris suum. They suggest that this could reflect the unusual structure
of this peptide, possessing a sulphated tyrosyl residue unique to this subfamily of arthropod FaRPs.
In the dipteran Calliphora vomitoria, perisulfakinin
had no effect on crop contractions in vitro (Haselton et al., 2006). The authors propose that although it has myotropic and anti-feedant effects
in insects other than P. americana, the amino acid
sequence may be specific enough to prevent it from
binding to blow fly alimentary tissue receptors on
the crop, if present. These results might explain why
this peptide had no effect on foregut peristalsis in
L. oleracea in vitro or when injected into larval L.
oleracea or S. littoralis. In addition, a lepidopteran
sulfakinin has yet to be identified.
All six myoinhibitory peptides isolated from the
ventral nerve cord of M. sexta inhibit peristalsis of
the anterior hindgut in vitro (Blackburn et al.,
1995, 2001). Whilst MIP I was the most potent of
these, it had no effect when assayed against the
foregut of L. oleracea in vitro or when injected into
L. oleracea or S. littoralis larvae. It is conceivable
that receptors for MIP I are not present in the foregut, or that when injected this peptide is rapidly
inactivated by haemolymph enzymes.
ACKNOWLEDGMENTS
The authors are very grateful to Hannah Bradish
for the supply of insects used in this study. In addition, we acknowledge DEFRA for supplying a
Archives of Insect Biochemistry and Physiology
October 2008
67
license to obtain and keep S. littoralis (License no.
PLH251C/5491(10/2006)).
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myo, oleracea, worm, littoral, cotton, spodoptera, leaf, vitro, lepidoptera, tomato, effect, moth, lacanobia, activ, larvae, vivo, noctuidae, peptide
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