Stimulation of JH biosynthesis by the corpora allata of adult female Aedes aegypti in vitro: effect of farnesoic acid and Aedes allatotropin
1 Department of Biochemistry and Molecular Biophysics and Center for Insect
Science, University of Arizona, Tucson, AZ 85721-0088, USA
2 Department of Entomology and Center for Insect Science, University of
Arizona, AZ 85721, Tucson, USA
3 Laboratoire de Neuroendocrinologie des Insectes, Université de
Bordeaux I, Laboratoire de Neuroendocrinologie, 33405 Talence Cedex,
France
4 INRA, Centre de Recherches d'Antibes, 06606 Antibes Cedex,
France
* Author for correspondence (e-mail: fnoriega{at}email.arizona.edu)
Accepted 13 March 2003
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Summary |
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Key words: mosquito, Aedes, farnesoic acid, allatotropin, corporaallata, regulation, juvenile hormone.
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Introduction |
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JH levels in adult female A. aegypti were measured by Shapiro et
al. (1986). JH levels increase
during the first two days after adult emergence and remain high before
feeding. When a female takes a blood meal, the JH level falls rapidly during
the first three hours and reaches its lowest point 24 h after the blood meal.
Forty-eight hours after the blood meal, the JH level starts to rise, and after
96 h it is equivalent to the pre-blood meal value. JH titer is essentially
determined by the rate at which the CA synthesizes JH. The in vitro
and in vivo biosynthesis of JH in A. aegypti was studied by
Borovsky and collaborators (Borovsky and
Carlson, 1992
; Borovsky et al.,
1992
,
1994a
,b
);
they developed an `exposed corpus allata' assay, i.e. the headthorax
complex was incubated in the presence of different radioactive precursors
[methyl farnesoate (MF) and methionine].
Two groups of peptides, allatotropins (AT) and allatostatins (AS), which
either stimulate or inhibit JH synthesis, respectively, have been found in
insects from different orders. Although allatotropic activity has been
described in biological extracts from a number of species, such as the larvae
of the wax moth Galleria mellonella
(Bogus and Scheller, 1996),
adult locust Locusta migratoria
(Gadot et al., 1987
;
Lehmberg et al., 1992
),
crickets Gryllus bimaculatus and Acheta domesticus
(Lorenz and Hoffmann, 1995
),
true bug Pyrrhocoris apterus
(Hodkova et al., 1996
), Loreyi
leafworm Mythimna loreyi (Kou and
Chen, 2000
) and the honey bee Apis mellifera
(Gäde et al., 1997
), so
far only a single peptide has been chemically identified. This is the
Manduca sexta allatotropin (Mas-AT) identified from heads of the
pharate adult tobacco hornworm Manduca sexta
(Kataoka et al., 1989
), a
13-residue amidated peptide with the sequence GFKNVEMMTARGFamide that
stimulates adult CA in vitro but does not affect the activity of
larval or pupal CA (Kataoka et al.,
1989
). Mas-AT was also purified from the methanolic brain extracts
of the fall armyworm Spodoptera frugiperda
(Oeh et al., 2000
). It also
stimulates JH biosynthesis in other lepidopteran species, such as the tobacco
budworm Heliothis virescens
(Kataoka et al., 1989
), the
tomato moth Lacanobia oleracea (Audsley et al.,
1999
,
2000
) and S.
frugiperda (Oeh et al.,
2000
), and non-lepidopteran species, such as A. mellifera
larvae (Rachinsky and Feldlaufer,
2000
; Rachinsky et al.,
2000
) and the black blowfly Phormia regina
(Tu et al., 2001
). By use of
immunochemical and molecular techniques, Mas-AT has been shown to be present
in the brain of larval L. oleracea and the cotton leafworm
Spodoptera littoralis (Audsley et al.,
1999
,
2000
), the abdominal nervous
system of the cockroaches Leucophaea maderae and Periplaneta
americana (Rudwall et al.,
2000
), the true armyworm moth Pseudaletia unipuncta
(Truesdell et al., 2000
),
P. regina, the adult large milk-weed bug Oncopeltus
fasciatus, the adult oriental fruit fly Dacus dorsalis, larval
and adult M. loreyi and the larval tea silk moth Andraca
bipunctata (Tu et al.,
2002
). In addition, cDNAs encoding Mas-AT have been cloned from
M. sexta (Taylor et al.,
1996
), P. unipuncta
(Truesdell et al., 2000
) and
the silk moth Bombyx mori (Park
et al., 2002
).
Besides stimulating JH biosynthesis, Mas-AT displays a multifunctional
character in M. sexta and other insects, including inhibition of ion
transport in M. sexta midgut (Lee
et al., 1998), stimulation of foregut contractions in the moths
Helicoverpa armigera (at extremely low concentrations) and L.
oleracea (Duve et al.,
1999
,
2000
) and acceleration of heart
rate in L. maderae, P. americana
(Rudwall et al., 2000
),
pharate adult M. sexta (Veenstra
et al., 1994
) and P. unipuncta
(Koladich et al., 2002
).
Mas-AT also plays a role in circuits relaying photic information from
circadian photoreceptors to the central pacemaker in L. maderae
(Petri et al., 2002
).
Recently, immunocytochemistry using an antiserum to MAS-AT revealed that an
allatotropin-immunoreactive peptide is present in the abdominal ganglia of the
mosquito Aedes aegypti (Veenstra
and Costes, 1999). The allatotropin-immunoreactive peptide was
isolated and its structure determined to be APFRNSEMMTARGFamide (Aedes-AT); in
addition, a cDNA encoding this peptide was cloned
(Veenstra and Costes,
1999
).
In the present study, we demonstrate the stage-specific stimulatory effects of Aedes-AT and of the JH precursor farnesoic acid (FA) on adult female A. aegypti CA activity in vitro.
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Materials and methods |
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Insects
Aedes aegypti (L.) of the Rockefeller strain were reared at
28°C and 80% relative humidity under a photoperiod cycle of 16 h:8 h
light:dark as previously described
(Noriega et al., 1999). The
newly emerged females were collected within 1 h of emergence, and during that
period females did not feed. For females older than 1 h (i.e. sugar-fed
females), a 3.0% sucrose solution was provided ad libitum. Only
virgin females were used in this study.
In vitro radiochemical assay for CA activity
For preparation of isolated CA complexes, mosquitoes were immobilized by
brief exposure to ice. After cutting off the legs, wings, antennae and
abdomen, the anterior half of the body was pinned to a silicon dissecting dish
and covered with a drop of mosquito saline buffer (138 mmol
l1 NaCl, 8.4 mmol l1 KCl, 4 mmol
l1 CaCl2, 2 mmol l1
MgCl2, 12 mmol l1 NaH2PO4,
12 mmol l1 Na2HPO4 and 42.5 mmol
l1 sucrose). The thorax was split open and the corpora
allata (CA) plus corpora cardiaca (CC) complex attached to the aorta was
exposed by carefully removing the thoracic muscles, cuticle and other tissues
from the neck region using a razor-blade scalpel, fine forceps and scissors.
The aorta and CACC complex, connected to the brain and head capsule,
were isolated. This facilitated the visualization and transfer of the
complexes. In all the experiments described in this paper we used CA + CC +
aorta + brain + head capsule preparations, which we will refer to as `CA
complexes'.
After dissection, the CA complexes were held in tissue culture medium M-199
(Specialty Media, Phillipsburg, NJ, USA) without methionine, containing 2%
Ficoll 400 and 25 mmol l1 Hepes (pH 6.5). After a
pre-incubation of 12 h to consume intraglandular methionine, the CA
complexes were transferred into a carbowax-coated flat-bottomed glass tube
containing 100 µl of sterile tissue culture medium M-199 with 25 mmol
l1 Hepes (pH 6.5) and 2% Ficoll 400 containing
L-[methyl-3H]methionine [specific activity 2.963.11 TBq
mmol1 (8084 Ci mmol1); Amersham
Pharmacia, Piscataway, IL, USA] as described by Feyereisen and Tobe
(1981) and Feyereisen
(1985
). The final
concentration of methionine in the medium was 50 µmol l1,
and the specific activity was 0.56 TBq mmol l1 (15 Ci mmol
l1). Under these conditions, the incorporation of
L-[methyl-3H]methionine into JH III was linear for at least 6
h.
CA were cultured in the dark at 30°C for 4 h under continuous gentle agitation on an ADAMSTM Nutator Mixer (Becton-Dickinson, Franklin Lakes, NJ, USA). Incubations were terminated by the addition of 100 µl 1% EDTA, and 100 µl methanol containing 25 µg each cold JH III and MF were used as carriers and internal standards. At the end of the experiment, the incubation medium and the gland were extracted together with methanol/hexane (1:10 v/v) and were separated by thin-layer chromatography (TLC). After TLC separation [developed in 2:1 (v/v) hexane/ethyl acetate], the JH and MF bands were detected under UV light, cut, put into 10 ml scintillation cocktail overnight and assayed for 3H. The quantities of JH and MF produced in the experiment were then calculated from the specific activity of the L-[methyl-3H]methionine in the medium, assuming a specific incorporation ratio of 1 (non-isotopic dilution).
HPLC and mass spectral analysis of products synthesized by CA
complexes
Detection of radiolabeled products was done using a Beckman Gold HPLC
system model 126, with an Ultrasphere® C18 reverse-phase HPLC
column (250x4.6 mm, 5 µm particles) and a scanning model 167 UV
detector set at 214 nm. The column was eluted using a linear gradient of
40100% acetonitrile in H2O. The separating conditions were
as follows: solvent flow rate, 1 ml min1; gradient,
05 min 40% CH3CN, 545 min 40100%
CH3CN (linear gradient), 4550 min 100% CH3CN,
5055 min, 40% CH3CN. Data from HPLC were detected and
analyzed using the Beckman Gold system software. The recovery calculated from
the UV traces was usually 7098%. 1 ml fractions were diluted with 10 ml
scintillation cocktail and analyzed for 3H.
The peaks from HPLC were analyzed by chemical ionization mass spectroscopy
(MS) using a Finnigan-Matt ITS 40® ion trap MS interfaced to a
Varian Star 3400® gas chromatograph with a cool-on-column
injector as described by Teal et al.
(2000). Identification of JH
homologs was based on comparison of fragmentation patterns (60300 amu)
and retention indexes of compounds eluting during analysis of natural product
samples with those of synthetic standards.
Statistical analysis
Statistical analysis of the data was performed by t-test or
one-way analysis of variance (ANOVA) with Tukey's post-test using GraphPad
Prism version 3.00 for Windows (GraphPad Software; San Diego, CA, USA). The
results were expressed as means ± S.E.M. and considered significantly
different at P<0.05. Values of percentage stimulation of JH
synthesis by treatment were calculated via the following formula: 100
x (activity with allatotropin or FA activity without
allatotropin or FA) / activity without allatotropin or FA.
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Results |
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Doseresponse relationship between exogenous FA and JH and
MF biosynthesis in vitro
The CA complexes from insects with high basal JH III biosynthetic activity
(2-day-old sugar-fed females) were incubated in M-199 media containing
L-[methyl-3H]-methionine and various concentrations of FA.
Fig. 1A shows that, in the
absence of FA, the rate of JH III biosynthesis was 15.56 fmol
complex1 h1. JH III biosynthesis was
markedly stimulated (approximately 9-fold) in the presence of 10 µmol
l1 FA, and this stimulation remained constant when the
concentration of FA was increased up to 160 µmol l1. On
the other hand, when we used CA complexes from insects with low basal JH III
biosynthetic activity (4-day-old sugar-fed females), JH III biosynthesis
augmented with FA increases up to a concentration of 40 µmol
l1 FA and then remained constant when the concentration of
FA was further increased up to 160 µmol l1
(Fig. 1B).
|
CA complexes of 2-day-old sugar-fed females accumulated MF in the presence of FA. There was a linear relationship between MF increases and FA concentration in the medium (r2=0.86). A similar trend was found in 4-day-old sugar-fed females (r2=0.92). Maximal stimulation occurred at an FA concentration of 40 µmol l1, and so in all subsequent experiments a concentration of 40 µmol l1 FA was used.
Stimulation of JH biosynthesis by Aedes-AT
The effect of increasing concentrations of Aedes-AT
(1012106 mol l1)
was tested on glands from 1-day-old (high basal activity;
Fig. 2A) and 3-day-old (low
basal activity; Fig. 2B)
sugar-fed females. Fig. 2C
shows that high rates of JH III biosynthesis (>50% increase) were observed
over a narrow range of Aedes-AT concentrations
(109108 mol l1)
in 1-day-old sugar-fed females, and over a wider range
(1010106 mol l1)
in 3-day-old sugar-fed females. MF biosynthesis was similar in CA treated with
Aedes-AT and in controls when glands from 1-day-old and 3-day-old females were
used (Fig. 2A,B). Maximal
stimulation occurred at an Aedes-AT concentration of 109 mol
l1, and so in all subsequent experiments a concentration of
109 mol l1 Aedes-AT was used.
|
Response of CA to Aedes-AT in vitro
Aedes-AT did not affect JH production in CA dissected from newly emerged
females and females 12 h after emergence. However, incubation of CA complexes
from 1-day-old sugar-fed females with Aedes-AT resulted in a significant
increase in rates of JH biosynthesis (Fig.
3A). Aedes-AT had no effect on JH production on CA from 2-day-old
sugar-fed females, but CA complexes from 3-, 4- and 6-day-old sugar-fed
females showed significantly higher JH levels in response to Aedes-AT; the
peptide did not affect JH biosynthesis on CA from 5- and 7-day-old sugar-fed
females. Aedes-AT did not induce significant increases in MF biosynthesis by
CA complexes when compared with controls
(Fig. 3B)
|
Allatotropin makes CA capable for JH production
CA complexes were dissected from females within 1 h of emergence and were
incubated with FA (40 µmol l1), Aedes-AT
(109 mol l1) or both. CA complexes from
newly emerged females showed a very low basal level of JH biosynthesis in
vitro. Biosynthesis of JH III in the presence of either FA or Aedes-AT
was also very low and similar to those from unstimulated CA complexes
(approximately 2.03 fmol complex1 h1).
However, incubation of CA complexes from newly emerged females with Aedes-AT
plus FA resulted in a 17-fold increase in the production of JH III (35 fmol
complex1 h1;
Fig. 4A). FA, Aedes-AT or both
did not result in significant increases of MF levels when compared with
controls (Fig. 4B).
|
Effect of Aedes-AT in the presence of FA
Simultaneous application of Aedes-AT and FA to the CA complexes of 0.5-,
2-, 4- and 6-day-old females had the same effects as applying FA alone
(Fig. 5). Addition of Aedes-AT
plus FA resulted in a large increase in JH biosynthesis in all cases
(Fig. 5A). MF increases in the
CA complex treated with FA or FA plus Aedes-AT were elevated when compared
with untreated controls (Fig.
5B); however, MF from the CA complexes treated with FA was higher
than from CA that had been treated with FA plus Aedes-AT
(Fig. 5B).
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Discussion |
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Responsiveness of CA complexes to FA
Exogenous FA, at optimal concentrations in the range of 2040 µmol
l1, is utilized by corpora allata in vitro to
enhance rates of JH synthesis (Feyereisen
et al., 1984; Tobe and Stay,
1985
; Gadot and Applebaum,
1986
). The addition of FA to the incubation medium containing
isolated corpora allata results in a significant stimulation of JH
biosynthesis in Schistocerca gregaria, P. americana, D. punctata
(Pratt et al., 1975
;
Feyereisen et al., 1981
),
Tenebrio molitor (Weaver et al.,
1980
), M. sexta (Unni
et al., 1991
) and A. mellifera
(Rachinsky et al., 2000
).
Moreover, Borovsky et al.
(1994b
) found that mosquito
A. aegypti ovary can synthesize JH III from FA in vivo and
in vitro.
The terminal two steps in JH III biosynthesis are: (1) the methylation of
FA to MF, catalyzed by O-methyl transferase, and (2) an epoxidation
of MF to JH III, catalyzed by methyl farnesoate epoxidase
(Tobe and Stay, 1985). The
addition of 40 µmol l1 FA to CA dissected from newly
emerged female A. aegypti showed no stimulation in MF or JH III
production (Fig. 4). However,
CA dissected from sugar-fed females 12 h after emergence showed an enormous
(60-fold) increase in JH III biosynthesis. A 9-fold increase in JH III
biosynthesis was found in CA dissected from sugar-fed females 2, 4 and 6 days
after emergence. These results suggest that at least two terminal enzymes for
JH biosynthesis are not activated in newly emerged females, O-methyl
transferase and methyl farnesoate epoxidase; they are progressively activated
when the CA mature, and after this maturation is completed they are kept at a
relatively high level. The same phenomenon was described in newly emerged
(01 day) adult female L. migratoria
(Gadot and Applebaum,
1986
).
In CA from 2- and 4-day-old sugar-fed female A. aegypti, an increase in FA concentration (more than 40 µmol l1) resulted in a linear increase of MF in the glands without causing a significant increase in JH biosynthesis. This observation suggests that such high FA concentrations saturate the methyl farnesoate epoxidase, a situation that probably does not occur under physiological conditions.
MF accumulation in the corpora allata also occurred in other insects under
certain experimental conditions. Specific inhibition of methyl farnesoate
epoxidase activity by 1,5-disubstituted imidazoles resulted in an increase in
MF content in D. punctata
(Unnithan et al., 1995).
Elevated concentrations of exogenous FA led to an accumulation of MF in
corpora allata from P. americana
(Pratt et al., 1975
). In
G. bimaculatus, MF accumulation was observed after treatment of the
glands with either 20 µmol l1 or 200 µmol
l1 farnesol (Wennauer
and Hoffmann, 1988
). In most insects, however, FA stimulation does
not result in MF accumulation, suggesting that the epoxidative capacity of the
corpora allata is generally greater than their capacity for the
esterification. Meanwhile, under unstimulated conditions, there is no such
increase of MF in sugar-fed A. aegypti females. Thus, two different
mechanisms seem to be responsible for the low rate of JH production by the
sugar-fed A. aegypti 2 days after emergence: (1) a limitation in the
production of JH precursors and (2) a rate limitation in the terminal step of
JH biosynthesis.
Responsiveness of corpora allata complex to Aedes-AT
In the present study, Aedes-AT stimulated maximal JH biosynthesis in
vitro (up to 6-fold) in 0.5- and 3-day-old sugar-fed virgin females of
A. aegypti (Figs 3,
4). These maximal levels of
stimulation for Aedes-AT were similar to those previously found for Mas-AT
during in vitro experiments using CA of various insects: up to
2.2-fold increase of JH in A. mellifera
(Rachinsky et al., 2000), up
to three times increase in larval L. oleracea
(Audsley et al., 2000
), a
2.6-fold increase in sugar-fed adult females of P. regina
(Tu et al., 2001
) and up to a
6-fold increase in adult M. sexta
(Kataoka et al., 1989
).
However, the maximal level of stimulation by Aedes-AT in A. aegypti
was lower than those by Mas-AT in either S. frugiperda (approximately
7-fold; Oeh et al., 2000
) or
in day 0 (approximately 15-fold) and day 6 (approximately 10-fold) adult
virgin female of P. unipuncta
(Koladich et al., 2002
).
In adult sugar-fed virgin A. aegypti, Aedes-AT exhibited a
stage-specific stimulation of JH biosynthesis in a dose-dependent manner, with
a maximal concentration of approximately
108109 mol l1; a
concentration similar to the titer of the peptide found in the hemolymph of
most insect species [106 mol l1 in P.
unipuncta and 108 mol l1 in L.
oleracea and P. regina
(Audsley et al., 2000;
Koladich et al., 2002
;
Tu et al., 2001
)]. Taken
together, these results suggest that Aedes-AT is indeed a true allatotropic
factor in A. aegypti.
Aedes-AT stimulation of JH and MF synthesis in the presence of
FA
The kinetics of FA- and Aedes-AT-stimulated activities of CA complexes were
different (Figs 1,
2); FA-stimulated rates of JH
III biosynthesis exceeded by far those of Aedes-AT-stimulated rates. MF
increases were more elevated in FA-stimulated CA complexes than in FA +
Aedes-AT-stimulated CA. MF increases were not observed in the
Aedes-AT-stimulated CA. These results suggest that the activity of methyl
farnesoate epoxidase is lower than that of O-methyl transferase in
FA-stimulated CA complexes. One possible explanation for these changes in MF
and JH III concentrations is that methyl farnesoate epoxidase was more
activated than O-methyl transferase when stimulated by Aedes-AT in
the presence of FA, while both enzymes (O-methyl transferase and
methyl farnesoate epoxidase) were equally stimulated by Aedes-AT in the
absence of FA.
With the exception of CA from newly emerged females, when CA complexes were
incubated with Aedes-AT in the presence of FA, there were no additional
increases in the rates of JH III biosynthesis, suggesting that Aedes-AT is
involved in activating some rate-limiting step(s) preceding FA biosynthesis.
Thus, when FA is added to the incubated CA, these rate-limiting steps are
avoided, and synthesis of JH III is exclusively dependent on methyl-transfer
and epoxidation. The same results have been found in FA- and
allatotropin-stimulated CA of adult female L. migratoria
(Gadot and Applebaum, 1986).
In newly emerged virgin female A. aegypti, Aedes-AT had the ability
to stimulate CA complexes to synthesize JH III only in the presence of FA.
These data suggest the existence of an additional mechanism of CA stimulation
in newly emerged females. Specific inhibitors for O-methyl
transferase and methyl farnesoate epoxidase might be useful to elucidate the
different stimulation pathways used by FA and Aedes-AT.
In summary, these studies demonstrate that Aedes-AT is a true allatotropin,
which shows a doseresponse relationship and age-specific effects, in
A. aegypti. After the original description published by Kataoka et
al. (1989), this is the first
report confirming the CA-stimulatory activity of an allatotropin that is
different from Mas-AT. These studies also reveal that FA stimulated JH
biosynthesis and caused MF increases, while Aedes-AT did not, indicating that
these two regulators differentially modulate the activity of the enzymes
involved in the terminal steps of JH biosynthesis.
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Acknowledgments |
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References |
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