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(Received for publication, May 12, 1995; and in revised form, July 5, 1995) From the
Three distinct cDNAs encoding the preproadipokinetic hormones I,
II, and III (prepro-AKH I, II, and III), respectively, of Locusta
migratoria have been isolated and sequenced. The three L.
migratoria AKH precursors have an overall architecture similar to
that of other precursors of the AKH/red pigment-concentrating hormone
(RPCH) family identified so far. The AKH I and II precursors of L.
migratoria are highly homologous to the Schistocerca gregaria and Schistocerca nitans AKH precursors. Although the L. migratoria AKH III precursor appears to be the least
homologous to the Manduca sexta, Drosophila
melanogaster, and Carcinus maenas AKH/RPCH precursors, we
favor the opinion that the L. migratoria AKH III precursor is
evolutionary more related to the M. sexta, D.
melanogaster, and C. maenas AKH/RPCH precursors than to
the AKH I and II precursors of S. gregaria, S.
nitans, or L. migratoria. In situ hybridization
showed signals for the different AKH mRNAs to be co-localized in cell
bodies of the glandular lobes of the corpora cardiaca. Northern blot
analysis revealed the presence of single mRNA species encoding the AKH
I precursor (
Three peptide hormones with hyperlipemic activity, the
adipokinetic hormones I, II and III (AKH (
Molecular biological studies have resulted in the
characterization of the structure of the AKH/RPCH precursors (a signal
peptide, AKH/RPCH, a Gly-(Lys/Arg)-Arg sequence, and an
AKH/RPCH-associated peptide (AAP/RAP), in this order) of S.
gregaria, S. nitans, M. sexta, D.
melanogaster, and Carcinus
maenas(11, 12, 13, 14, 15, 16, 17) . The biosynthesis of the AKHs in S. gregaria has been
elucidated in detail by O'Shea and
co-workers(13, 18, 19, 20, 21) .
The signal peptide is co-translationally removed from prepro-AKH,
generating pro-AKH. Next, proteolytic processing, which is preceded by
dimerization of two pro-AKHs (I/I, I/II, or II/II) via their single
COOH-terminal Cys residues, gives rise to two AKHs (I and/or II) and
one homo- or heterodimeric peptide consisting of two AAPs (I/I, I/II,
or II/II), a so-called AKH precursor-related peptide, as end products.
The biosynthesis of AKH I and II of L. migratoria proceeds via
the same pathway(3) . For the migratory locust, we now
present three cDNA sequences, each encoding a different AKH precursor.
The present data show that the AKH I and II precursors of L.
migratoria are highly homologous to their S. gregaria and S. nitans counterparts. The AKH III precursor of L.
migratoria appears to be more homologous to the L.
migratoria, S. gregaria, and S. nitans AKH I and
II precursors than to the M. sexta, D. melanogaster,
and C. maenas AKH/RPCH precursors. In addition, we show that
flight activity differentially increases the level of each prepro-AKH
mRNA.
The reaction mixture for 3` RACE of
the pro-AKH I and II cDNAs (PCR I) contained 4 µM degenerate AKH-A primer, 0.25 µM adaptor I primer,
and 1 µl of cDNA pool. Amplification products were separated by
agarose gel electrophoresis, and bands of approximately 380 and 300 bp
were excised and eluted in 20 µl of TE buffer each. Either 1 µl
of 20-fold diluted 380-bp fragment or 1 µl of 20-fold diluted
300-bp fragment was subjected to a nested PCR (PCR II) in a reaction
mixture containing 4 µM degenerate AKH-A primer and 0.25
µM adaptor II primer (see Table 2). The reaction
mixture for 3` RACE of the pro-AKH III cDNA (PCR III) contained 0.5
µM degenerate AKH-B primer, 0.5 µM adaptor
III primer, and 2 µl of cDNA pool. 2 µl of 50-fold diluted PCR
III was subjected to a nested PCR (PCR IV) in a reaction mixture
containing 0.5 µM degenerate AKH-C primer and 0.5
µM adaptor I primer. 2 µl of 50-fold diluted PCR IV
was subjected to a nested PCR (PCR V) in a reaction mixture containing
0.5 µM degenerate AKH-C primer and 0.5 µM adaptor II primer (see Table 2).
Subsequently, the three different pro-AKH 3` RACE products were used
to screen a L. migratoria CC-specific cDNA library. The
nucleotide sequences of the longest AKH I, II, and III cDNAs and their
deduced amino acid sequences are shown in Fig. 1Fig. 2Fig. 3. The AKH I cDNA consists of 363
bp, including an open reading frame of 189 nucleotides encoding the L. migratoria AKH I precursor. The AKH II cDNA consists of 367
bp, including an open reading frame of 183 nucleotides encoding the L. migratoria AKH II precursor. The AKH III cDNA consists of
438 bp, including an open reading frame of 231 nucleotides encoding the L. migratoria AKH III precursor.
Figure 1:
Nucleotide sequence of the cDNA
encoding the AKH I precursor of L. migratoria and the deduced
amino acid sequence of the precursor. Nucleotides are numbered 5` to
3`, beginning with the first residue in the coding region for the
adipokinetic hormone I. Amino acid residues are numbered with the first
residue (Gln) of the hormone as 1. The asterisk indicates the
stop codon. The nucleotides corresponding to the polyadenylation signal
(AATAAA) are underlined.
Figure 2:
Nucleotide sequence of the cDNA encoding
the AKH II precursor of L. migratoria and the deduced amino
acid sequence of the precursor. For further details see the legend to Fig. 1.
Figure 3:
Nucleotide sequence of the cDNA encoding
the AKH III precursor of L. migratoria and the deduced amino
acid sequence of the precursor. For further details see the legend to Fig. 1.
Figure 4:
In situ hybridization of corpora
cardiaca of L. migratoria. Alternate transverse sections
through the CC containing cell bodies that show in situ hybridization signals for the pro-AKH I mRNA (I), for the
pro-AKH II mRNA (II), and for the pro-AKH III mRNA (III).
In
order to examine the full-length AKH mRNAs as well as to study the
effect of flight activity on the AKH gene expression, RNA was extracted
from CC of locusts that had flown for 1 h as well as from CC of resting
locusts. RNA blot analysis (Fig. 5) revealed that the mRNA
encoding the AKH I precursor clearly is the most predominant AKH
transcript expressed in the CC. In addition, flight activity caused the
steady-state levels of the AKH I and AKH II transcripts and the AKH III
transcripts to increase approximately 2.0 and 4.2 times, respectively.
Northern blot analysis also showed that the cDNAs encoding the AKH I,
II, and III precursors represent transcripts of
Figure 5:
Northern blot analysis of L.
migratoria AKH precursor mRNAs. A, hybridization of RNA
isolated from CC of locusts that had flown for 1 h (lanes indicated with F) as well as from CC of resting locusts (lanes indicated with R) with pro-AKH I cDNA probe (I), with pro-AKH II cDNA probe (II), and with
pro-AKH III cDNA probe (III) after washing with 1
Further processing of the three different L.
migratoria AAPs seems to be very unlikely, because at least
unprocessed L. migratoria AAPs I and II have been isolated in
the form of homo- or heterodimers, linked via their COOH-terminal Cys
residues(29) . In addition, also from S. gregaria and S. nitans, unprocessed AAPs can be isolated in the form of
homo- or heterodimers. In both Schistocerca species this
dimerization also has to precede the prohormone processing at the
Gly-Lys-Arg or Gly-Arg-Arg sequences(7) . The presence of
multiple bioactive peptides within single precursors is commonly
observed(30) . A consequence of such prohormone structures is
that multiple companion peptides may coordinately be synthesized and
released. If individual peptides within prohormones control different
though related physiological and/or behavioral processes, this mode of
synthesis and release may coordinate the component elements of a
complex physiological and/or behavioral repertoire(31) . This
situation is even more complex for the peptides derived from the AKH I
and II prohormones; dimerization of two pro-AKHs (I/I, I/II, or II/II)
followed by proteolytic processing may give rise to different
``bouquets'' of AKHs (I and/or II) in combination with homo-
or heterodimeric peptides consisting of two AAPs (I/I, I/II, or II/II).
Data on the possible formation of intra- or intermolecular disulfide
bridges of pro-AKH III are lacking so far.
Figure 6:
Comparison of AKH/RPCH precursors. A, the single-letter codes are used to designate amino acids.
The three domains of signal sequence, AKH/RPCH, and AAP/RAP are set
apart. Amino acids that represent the site for enzymic precursor
cleavage and carboxyl-terminal amidation are joined to the AKH/RPCH
sequence. Gaps (indicated by hyphens) were introduced
optionally to achieve maximum similarity as well as taking into account
conservative amino acid substitutions. B, UPGMA tree for the
AKH precursors of L. migratoria (indicated by Lom AKH
I, Lom AKH II, and Lom AKH III), S. gregaria (Scg AKH I and Scg AKH II), S. nitans (Scn AKH I and Scn AKH II), M. sexta (Mas AKH), and D. melanogaster (Drm
AKH), and the RPCH precursor of C. maenas (Cam
RPCH).
The results of the Northern blot
analysis revealed that the prepro-AKH I, II, and III cDNAs very likely
are full-length, assuming an average poly(A) tail of 200 nucleotides (Fig. 5). Interestingly, the ratio of steady-state AKH I, AKH
II, and AKH III mRNA levels seems to be similar to the ratio of the AKH
I, AKH II, and AKH III peptides (14:2:1) present in the CC of resting
locusts(3, 33) . Because each AKH may have a different
though related function, we reasoned that flight activity might induce
a differential pattern of expression of the AKH genes in the CC.
Indeed, a remarkable increase in the level of the AKH III transcript
( From the above experiments it may be concluded
that the three different forms of AKH mRNA and as a result the three
different forms of AKH precursors are co-expressed in the same cells of
the corpora cardiaca of L. migratoria.
The nucleotide sequence(s) reported in this paper has been submitted
to the GenBank(TM)/EMBL Data Bank with accession number(s)
X86799[GenBank],
X86800[GenBank], and
X86801[GenBank].
Volume 270,
Number 39,
Issue of September 29, pp. 23038-23043, 1995
©1995 by The American Society for Biochemistry and Molecular Biology, Inc.
DIFFERENTIAL EXPRESSION OF THE DISTINCT ADIPOKINETIC HORMONE
PRECURSOR GENES DURING FLIGHT ACTIVITY (*)
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
FOOTNOTES
ACKNOWLEDGEMENTS
REFERENCES
570 bases), AKH II precursor (
600 bases), and
AKH III precursor (
670 bases), respectively. Interestingly, flight
activity increased steady-state levels of the AKH I and II mRNAs
(
2.0 times each) and the AKH III mRNA (
4.2 times) in the
corpora cardiaca.
)I, II and III;
see Table 1)(1, 2, 3) , are synthesized
by the glandular neurosecretory cells of the corpora cardiaca (CC) of
the migratory locust, Locusta migratoria. These peptides are
members of a large family of structurally related but functionally
diverse peptides (the AKH/RPCH family)(4) . In the adult
locust, the AKHs I and II are released into the hemolymph during flight
and are involved in the mobilization of lipid and carbohydrate from the
fat body to serve as energy substrates for the flight
muscles(4, 5, 6, 7) . Data on the
release and functioning of AKH III are lacking so far. Isolation and
characterization of CC peptides revealed that two other locust species, Schistocerca gregaria and Schistocerca nitans, each
contain two AKHs that are mutually identical(1, 8) ,
whereas Manduca sexta and Drosophila melanogaster each contain only one AKH (9, 10) (see Table 1).
Preparation of mRNA and Polymerase Chain
Reaction
Total RNA was extracted from CC of male L.
migratoria by the method of Chirgwin et al.(22) .
Poly(A)-rich RNA was prepared using Dynabeads-oligo dT (Dynal A.S.). Partial pro-AKH cDNAs were amplified from the RNA
based on the principle of 3` RACE(23) . Using a DNA Thermal
Cycler (Perkin-Elmer), each polymerase chain reaction (PCR)
amplification was performed in a 100-µl reaction mixture containing
10 µl of 10
PCR buffer (HT Biotechnology Ltd.), 200
µM dNTPs (Pharmacia), primers and templates as indicated (Table 2), and 1 unit of SuperTaq DNA polymerase (HT
Biotechnology Ltd.). The mixture was overlaid with 70 µl of light
mineral oil (Sigma).
Oligodeoxynucleotide Primers
Oligodeoxynucleotide
primers were obtained from Pharmacia: oligo(dT) adaptor primer,
5`-GACTCGAGTCGACATCGATTTTTTTTTTTTTTTTTTTT-3`; adaptor I primer,
5`-CGCTCTAGAGACTCGAGTCGACATCGA-3`; adaptor II primer,
5`-CGCGAGCTCGAGTCGACATCGATTT-3`; adaptor III primer,
5`-CGCGCTCTAGAGACTCGAGTCGACAT-3`; degenerate AKH-A primer,
5`-CGCGGATCCCA(A/G)CTIAA(T/C)TT(T/C)(A/T)CI(C/G)CI(A/G/T)(A/G)ITGGG-3`;
degenerate AKH-B primer,
5`-CGCGCGGATCCCA(A/G)CT(G/A/T/C)AA(T/C)TT(T/C)AC(G/A/T/C)CCIT-3`;
degenerate AKH-C primer,
5`-CGCGGATCCCA(A/G)CT(G/A/T/C)AA(T/C)TT(T/C)AC(G/A/T/C)CC(G/A/T/C)TGG-3`;
T3-PCR primer, 5`-CGCGGTACCAAATTAACCCTCACTAAAGGG-3`; and T7-PCR primer,
5`-CGCGGTACCTGTAATACGACTCACTATAGG-3`. The degenerate AKH-A primer was
designed based on the amino acid sequences of the AKHs I, II, and III
(amino acids 1-9), respectively; the degenerate AKH-B and -C
primers were based on the amino acid sequence of AKH III only (amino
acids 1-7).3`-End Amplification of Pro-AKH I, II, and III
cDNA
Poly(A)-rich RNA (0.5 µg) was heated to 65 °C for 3
min, rapidly cooled on ice, and incubated in a 10-µl reaction
mixture containing 0.75 µM oligo(dT) adaptor primer at 42
°C for 1 h and then at 50 °C for 20 min, using a first strand
cDNA synthesis kit (Amersham International). The reaction mixture was
diluted to 100 µl with TE buffer (10 mM Tris/HCl, 1 mM EDTA, pH 8.0), heated to 95 °C for 5 min, and stored at
-20 °C (cDNA pool).DNA Cloning and Sequence Analysis
Amplification
products were separated by agarose gel electrophoresis, excised,
eluted, cut (making use of the restriction enzyme recognition sites
present at the 5`-ends of the primers), subcloned into pBluescript
vectors (Stratagene), and transformed into Escherichia coli competent cells. Nucleotide sequences were determined from both
DNA strands by the dideoxy chain termination method (24) using
primers prepared according to known plasmid or insert sequences.Construction and Screening of a CC-specific cDNA Library
of L. migratoria
An unidirectional, oligo(dT)-primed cDNA
library (3.5
10
initial clones) of the CC of L. migratoria was constructed in the ZAP Express vector
(Stratagene). Approximately 5 10
recombinant phages
of the amplified library were adsorbed to replica Hybond-N filters (Amersham International) and subsequently hybridized with
the radioactively labeled pro-AKH I-, II-, and III-specific 3` RACE
products, respectively (see above). After purification by rescreening
at a lower plaque density, positive pro-AKH-ZAP Express clones were
converted to recombinant pBK-CMV plasmids using in vivo excision.
Preparation of Digoxigenin-labeled cRNA Probes
The
pro-AKH I-, II-, and III-specific cDNAs were amplified using the T3-PCR
and T7-PCR primers (see above) flanking the multiple cloning site
sequences of the pBK-CMV plasmid, separated by agarose gel
electrophoresis, excised, eluted, and resuspended in diethyl
pyrocarbonate-treated water. For sense or antisense digoxigenin RNA
labeling by in vitro transcription, 200 ng of DNA template was
incubated at 37 °C for 2 h in a 20-µl reaction mixture
containing 40 mM Tris/HCl, pH 8.0, 6 mM
MgCl
, 10 mM dithiothreitol, 10 mM spermidin, 10 mM NaCl, 1 mM ATP, 1 mM CTP, 1 mM GTP, 0.85 mM UTP, 0.15 mM digoxigenin-labeled UTP, and 60 units of T3 RNA polymerase
(Pharmacia) or 60 units of T7 RNA polymerase (Pharmacia), respectively.
Next, the DNA template was removed by adding 5 units of RNase-free
DNase I (Pharmacia) and incubation at 37 °C for 15 min.In Situ Hybridization
In situ hybridization was performed essentially as described by Bogerd et al.(25) with the following changes. The CC were
immersed in 2% paraformaldehyde/0.2% glutaraldehyde in
phosphate-buffered saline (137 mM NaCl, 2.7 mM KCl,
4.3 mM NaHPO
7HO, 1.4
mM KHPO, pH 7.3) and fixed at 4 °C
for 1 h. For hybridizations 5 ng/80 µl digoxigenin-labeled cRNA
probes were used. Alkaline phosphatase staining was performed for 24 h. Northern Blot Analysis
Total RNA was prepared as
described above from CC of resting L. migratoria, as well as
from CC of L. migratoria that had flown for 1 h, and 1.35
µg/lane of each type of CC RNA was treated with glyoxal/dimethyl
sulfoxide according to Thomas(26) , electrophoresed through a
1.6% agarose gel, and then transferred to Hybond-N membrane (Amersham International). Pro-AKH I-, II-, and
III-specific 3` RACE products and a locust 18 S rRNA cDNA fragment,
respectively, were used as probes, after labeling with
[
-P]dATP by random oligodeoxynucleotide
priming, using a random primed DNA labeling kit (Boehringer Mannheim).
The membranes were prehybridized, hybridized, and washed using standard
techniques(27) . BaFBr:Eu
-based phosphor
screens were exposed to the membranes in 20
25-cm cassettes at
room temperature. After exposure, phosphor screens were scanned on a
PhosphorImager SI (Molecular Dynamics), and phosphor images were
analyzed with ImageQuant version 4.1 software (Molecular Dynamics).
Primary Structure of the Prepro-AKH I, II, and III
mRNAs
Partial pro-AKH cDNAs were amplified from L.
migratoria CC mRNA based on the principle of 3` RACE described by
Frohman(23) . To this end, we used degenerate
oligodeoxynucleotide primers based on the amino acid sequences of the
AKHs I, II and III (see Table 2). Two distinct bands of PCR
products (PCR II) of approximately 380 and 300 bp and one band of PCR
products (PCR V) of approximately 450 bp were detected in agarose gel
electrophoresis. The putative pro-AKH I and II cDNAs were identified by
sequence analysis of several clones derived from both the 380- and the
300-bp bands, whereas the putative pro-AKH III cDNA was identified by
sequence analysis of several clones derived from the 450-bp band.
Primary Structure of the AKH I, II, and III
Preprohormones
In view of the(-3, -1) rule for
signal peptidase recognition (28) and considering that the
overall architecture of the L. migratoria AKH I, II, and III
precursors is similar to that of their S. gregaria, S.
nitans, M. sexta, D. melanogaster, and C.
maenas counterparts (see below and (11, 12, 13, 14, 15, 16, 17) ),
we predict that the NH-terminal parts constitute signal
peptides that are most probably cleaved off between Ala (amino acid 22)
and Gln (amino acid 23) for all three Locusta AKH precursors.
The AKH I, II, and III prohormones contain Gly-Lys-Arg (for pro-AKH I
and III) or Gly-Arg-Arg (for pro-AKH II) sequences, of which the
(Lys/Arg)-Arg pairs may serve as sites for prohormone convertase
processing and of which the Gly is considered as the donor for
COOH-terminal amidation of the AKHs. If these sites are recognized, AKH
I (amino acids 1-10) and AAP I (amino acids 14-41) are
generated from the AKH I prohormone. In a similar way, AKH II (amino
acids 1-8) and AAP II (amino acids 12-39) are generated
from the AKH II prohormone, and AKH III (amino acid 1-8) and AAP
III (amino acid 12-55) are generated from the AKH III prohormone. Expression of the Prepro-AKH I, II, and III
Transcripts
The sites of expression of the three AKH mRNAs in
the L. migratoria CC were studied using in situ hybridization. Cell bodies showing mainly co-localized signals for
all three AKH mRNAs were present in the CC (Fig. 4). No
hybridization signals were found using the sense RNA probes.
570,
600, and
670 bases, respectively.
SSC,
0.1% SDS at 65 °C for 2 15 min. Indicated are the
0.16-1.77-kb RNA size markers (Life Technologies, Inc.). B, after stripping off the AKH cDNA probes, the membranes were
hybridized with an 18 S RNA cDNA probe and washed with 1 SSC,
0.1% SDS at 65 °C for 2 15 min for standardization of the
amount of RNA loaded in each lane.
Organization of the AKH I, II, and III
Preprohormones
We have cloned and characterized three different
abundant cDNAs, which are co-expressed in cells of the glandular lobes
of the corpora cardiaca of L. migratoria. The proteins encoded
by the cDNAs are organized as preprohormones. After co-translational
removal of their 22-amino-acid signal peptides, the resulting
prohormones are likely to be cleaved to generate two bioactive
peptides. Isolation and characterization of L. migratoria CC
peptides(3, 29) revealed that, indeed, the glycine
residue in combination with the dibasic residues following the AKH
sequence (residues 11-13 for the AKH I prohormone, and residues
9-11 for the AKH II and III prohormones; Fig. 1Fig. 2Fig. 3) are used as the actual signals
for COOH-terminal amidation of AKH and prohormone convertase
processing.Comparison of the AKH I, II, and III Preprohormones with
Other AKH/RPCH Preprohormones
The amino acid sequences of the
three L. migratoria AKH precursors were compared with the
amino acid sequences of the AKH/RPCH precursors of S. gregaria(13, 14) , S. nitans(11) , M. sexta(12) , D. melanogaster(15) ,
and C. maenas(17) (Fig. 6). As expected, the Locusta AKH I precursor revealed a high amino acid identity to
the Schistocerca AKH I (89-92%) and II (59-63%)
precursors, whereas the amino acid identity to the Manduca, Drosophila, and Carcinus AKH/RPCH precursors
(
30%) was much lower. In addition, the Locusta AKH II
precursor also showed a high amino acid identity to the Schistocerca AKH I (57%) and II (80-82%) precursors.
Again, the amino acid identity to the Manduca, Drosophila, and Carcinus AKH/RPCH precursors
(30%) was lower. Nucleotide identity was also very high (i.e. 86% for the Locusta AKH I precursor with the Schistocerca AKH I precursors and 84-86% for the Locusta AKH II precursor with the Schistocerca AKH II
precursors). Comparison of the Locusta AKH III precursor with
the AKH I and II precursors of L. migratoria, S.
gregaria, and S. nitans showed relatively low percentages
of amino acid and nucleotide identity. However, the L. migratoria AKH III precursor is different with respect to the AAP region;
instead of 28 amino acids (the length of the AAPs I and II in Locusta and Schistocerca species), the AAP III is 44
amino acids in length. Interestingly, the M. sexta AAP, the D. melanogaster AAP, and the C. maenas RAP are also
longer (34, 46, and 74 amino acids long, respectively) than the Locusta and Schistocerca AAP-I and AAP-II. In
addition, the Locusta AAP III, the Manduca AAP, the Drosophila AAP, as well as the Carcinus RAP each
contain two Cys residues. Although the homology of the Locusta AKH III precursor with the Manduca, Drosophila,
and Carcinus AKH/RPCH precursors is rather low (32%), we
favor the opinion that the Locusta AKH III precursor is
evolutionary more related to the Manduca, Drosophila,
and Carcinus AKH/RPCH precursors than to the AKH I and II
precursors of L. migratoria, S. gregaria, and S.
nitans. Future experiments may show whether the presence of two
Cys residues in the AAPs/RAP of the Locusta AKH III, the Manduca AKH, the Drosophila AKH, and the Carcinus RPCH precursors is involved in the possible formation of intra- or
intermolecular disulfide bridges, which could further substantiate this
notion.
Expression of the AKH I, II, and III Preprohormone
Transcripts
The results of in situ hybridization
experiments (Fig. 4) showed that the signals for the three
AKH-preprohormone mRNAs are co-localized in neurosecretory cells of the
glandular lobes of the L. migratoria CC, which further extends
earlier immunocytochemical observations using antisera specific for the
AKHs I and II(32) .4.2 times) was found in comparison with the increase of the
levels of AKH I and II transcripts (
2.0 times each) (Fig. 5). Thus, the experiments suggest a stimulus-dependent
differential pattern of expression of the AKH genes in one type of
neurosecretory cell. The remarkable difference in flight-induced AKH
III versus AKH I and II mRNA increase may shed new light on a
possible role for AKH III during flight activity. In addition, these
results are in accordance with the observed enhancement of the
production of secretory granules by the trans-Golgi network in
flight-stimulated adipokinetic cells of L. migratoria(34) .
)
We thank Drs. Wil J. A. Van Marrewijk and Jacques H.
B. Diederen for expert advice and critical reading of the manuscript.
©1995 by The American Society for Biochemistry and Molecular Biology, Inc.
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