Neurochemical fine tuning of a peripheral tissue: peptidergic and aminergic regulation of fluid secretion by Malpighian tubules in the tobacco hawkmoth M. sexta
1 Department of Zoology, Downing Street, University of Cambridge, Cambridge
CB2 3EJ, UK
2 Department of Zoology, Stockholm University, Svante Arrhenius väg 16,
SE-106 91 Stockholm, Sweden
3 Institute of Neuroscience, University of Oregon, Eugene, Oregon 97403
USA
* Author for correspondence (e-mail: shpm100{at}hermes.cam.ac.uk )
Accepted 15 April 2002
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Summary |
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We propose the hypothesis that the control in insects of physiological systems by hormones may not always involve tissue-specific hormones that force stereotypical responses in their target systems. Instead, there may exist in the extracellular fluid a continuous broadcast of information in the form of a chemical language to which some or all parts of the body continuously respond on a moment-to-moment basis, and which ensures a more effective and efficient coordination of function than could be achieved otherwise.
Key words: Manduca sexta, Malpighian tubule, leucokinin, cardioacceleratory peptide, crustacean cardioactive peptide, CCAP, CAP, TRP, tachykinin-related peptide, fluid secretion
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Introduction |
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In this paper we show that eight different substances, all but two of them likely to be hormones, affect fluid secretion by the Malpighian tubules of pharate adult tobacco hawkmoth Manduca sexta. These include the tachykinin-related peptides, TRPs, not known previously to have such an effect. To accommodate these findings, we provide a new description of how hormones may be involved in the control and regulation of insect tissues and organs.
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Materials and methods |
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Immunocytochemistry
Nervous systems, intestines and hearts of fifth instar larvae and pharate
adults of M. sexta were dissected and fixed in 4% paraformaldehyde in
0.1 mol l-1 sodium phosphate buffer for at least 4 h. The tissues
were used for immunocytochemistry on either cryostat sections (brains) or
whole mounts (all tissues). Standard peroxidase anti-peroxidase technique was
used (see Nässel, 1993;
Lundquist et al., 1994
). The
antiserum used (Code 9207-7) was raised in rabbit against locustatachykinin-I
(LomTK-I) conjugated to human serum albumin
(Nässel, 1993
). The
specificity of this antiserum has been tested extensively
(Nässel, 1993
;
Lundquist et al., 1994
). The
antiserum was used at a dilution of 1:1000 (in phosphate-buffered saline with
0.5% bovine serum albumin and 0.25% Triton X-100). As a control we performed
immunocytochemistry with the LomTK antiserum preabsorbed overnight with 20 and
50 nmol synthetic LomTK-I per 1000 µl diluted antiserum (1:1000).
Chemicals
Cyclic nucleotides and biogenic amines were obtained from Sigma. Synthetic
LomTK-I and TRPs of the cockroach Leucophaea maderae, LemTRP-1, and
TRP-4 were synthesized by Dr Å. Engström (Department of Medical and
Physiological Chemistry, Uppsala University, Sweden) as described in Muren and
Nässel (1996). CCAP and
CAP2b were synthesized by Research Genetics Inc. CAP2c, CAP1a and CAP1b were
obtained using the protocol described in Huesmann et al.
(1995
). Leukokinin I was
purchased from Peninsula Laboratories.
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Results |
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The effects of cyclic nucleotides on fluid secretion by M. sexta
Malpighian tubules
Cyclic nucleotides have potent effects on Malpighian tubule activity in a
variety of insects including, for example, the fruit fly Drosophila
melanogaster (Riegel et al.,
1998), the house cricket Acheta domestica
(Coast et al., 1991
), the
cabbage white butterfly Pieris brassicae
(Nicolson, 1976
) and the
blood-sucking bug Rhodnius prolixus
(Maddrell et al., 1971
).
Cyclic AMP (cAMP) always appears to be stimulatory whereas cyclic GMP can be
either stimulatory (e.g. Drosophila;
Dow and Maddrell, 1993
;
Dow et al., 1994
) or
inhibitory (e.g. R. prolixus;
Quinlan et al., 1997
).
Application of 1 mmol l-1 cAMP caused a significant increase in the
rate of fluid secretion by isolated M. sexta Malpighian tubules,
achieving a maximal 3.31-fold increase within 15 min compared to unstimulated
tubules (Fig. 2). Cyclic GMP,
applied at a concentration of 1 mmol l-1, also stimulated tubule
secretion rate (Fig. 2). The
time course for cGMP activation was similar to that of cAMP although the
maximal response for cGMP was slightly lower compared to that of cAMP
(2.86-fold increase).
|
The effects of various peptides on fluid secretion by M. sexta
Malpighian tubules
Leucokinins
We tested several different peptides from peptide families known to
stimulate tubules in other insect species on tubules isolated from pharate
adult M. sexta. One peptide tested was leucokinin I (LK-I),
representative of the leucokinin family of peptides (Holman et al., 1986).
Tubules treated with LK-I showed a rapid, dose-dependent increase in the rate
of fluid secretion (Fig. 3). Tubules responded very rapidly to all three LK-I concentrations tested (1
µmol l-1, 10 µmol l-1 and 100 µmol
l-1), reaching near maximal response levels within a few minutes of
LK-I application. The maximal secretion rate at 100 µmol l-1
LK-I was 2.21-fold higher than the unstimulated rate.
|
Cardioacceleratory peptides
A second set of peptides tested for possible Malpighian tubule activity
belong to the cardioacceleratory peptides (CAPs) category. The CAPs,
originally isolated from M. sexta, are a set of five peptides (CAP1a,
CAP1b, CAP2a, CAP2b and CAP2c) that cause an increase in heart rate when
applied to an isolated M. sexta heart
(Tublitz et al., 1991). Two of
the CAPs, CAP2a and CAP2b, have been sequenced
(Cheung et al., 1992
;
Huesmann et al., 1995
).
Because sequence analysis has demonstrated that CAP2a is identical to a
previously identified crustacean peptide, crustacean cardioactive peptide
(CCAP; Stangier et al., 1987), it is referred to as CCAP. CCAP has no effect
on fluid secretion activity when tested on pharate adult M. sexta
Malpighian tubules at a concentration of 1 µmol l-1
(Fig. 4). CAP2b at a
concentration of 1 µmol l-1 also proved to be ineffective
(Fig. 4), a somewhat surprising
result considering that CAP2b regulates tubule activity in D.
melanogaster (Davies et al.,
1995
) and R. prolixus
(Quinlan et al., 1997
).
Although M. sexta tubules were insensitive to CCAP and CAP2b, they
did respond to the other CAPs. A mixture of CAP1a and CAP1b applied at a dose
of 1 nerve cord equivalent elicited a relatively rapid rise in the rate of
fluid secretion (Fig. 4).
CAP1a/1b application nearly doubled fluid secretion rate, reaching a maximum
within 15 min of peptide application. Fluid secretion declined thereafter but
remained above basal levels for the duration of the experiment (90 min). In
contrast to the response to CAP1a/1b, tubules responded differently to CAP2c.
CAP2c, at a dose of 1 nerve cord equivalent, caused a small but detectable
increase in fluid secretion rate, but this was very slow to develop, reaching
a maximal stimulation rate of 1.31-fold a full 40 min after CAP2c was applied
(Fig. 4).
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Tachykinin-related peptides
The tachykinin-related peptides (TRPs) are a family of small peptides
originally found in the locust Locusta migratoria
(Schoofs et al., 1993).
Subsequently many TRPs have been isolated from other insect species
(Nässel, 1999
). TRPs are
categorized by a C-terminal amino acid sequence of
FX1GX2Ramide, where X2 is either a valine
(V), threonine (T) or methionine (M). We tested three different TRPs:
locustatachykinin-1 from L. migratoria (Lom TK-1; GPSGFYGVRamide;
Schoofs et al., 1993
) and two
TRPs from Leucophaea maderae (Lem TRP-1, APSGFLGVRamide; and Lem
TRP-4, APSGFMGMRamide; Muren and
Nässel, 1996
). Each TRP was tested at four different
concentrations ranging from 1 nmol l-1 to 1 µmol l-1.
In general the response of pharate adult M. sexta tubules to all
three TRPs was the same; each TRP produced a dose-dependent increase in the
rate of fluid secretion (Fig.
5A-C). The time course of the TRP-induced response was relatively
slow compared to the other peptides tested. Maximal response for each TRP was
achieved approximately 30-40 min after TRP application. In terms of relative
potency, Lem TRP-1 was the most potent TRP tested in this study, followed by
Lom TK-1 and Lem TRP-4. At a concentration of 1 µmol l-1, Lem
TRP-1 elicited a maximal increase in the rate of fluid secretion of 2.83-fold
compared to the secretion rate of control tubules, whereas Lem TRP-4 at the
same concentration produced only a 1.68-fold rise in secretion rate. In
contrast to the CAPs and leucokinin, TRP effects on tubule secretion activity
were not long lasting, declining to near-basal levels within 20-25 min after
the maximal response was achieved. Addition of a second TRP to tubules already
stimulated by a maximal concentration of a different TRP had little or no
effect (data not shown).
|
The possible role of cAMP in mediating leucokinin responses
To begin to elucidate the intracellular pathways mediating the effects of
leucokinin, we tested the effects of adding 60 µmol l-1 LK-I to
tubules previously treated with 1 mmol l-1 cAMP (maximal
stimulation is achieved by concentrations of cAMP at and above 100 µmol
l-1; N.J.V.S. and S.H.P.M., unpublished results) and also the
effect of adding the same agents in the reverse order on a different set of
tubules from the same insects. The results are shown in
Fig. 6. The effect of cAMP
alone was much greater than that of LK-I alone, and it is also clear that the
effects of both substances together are the same as with cAMP alone. Thus the
effects of LK-I are not additive to those of cAMP. It is possible, therefore,
that LK-I might exert its effects on the rate of fluid secretion through cAMP
as a second messenger. These results are in contrast to observations on adult
D. melanogaster tubules where the effects of leucokinin IV are
additive to those of cAMP and there is clear evidence that leucokinin action
does not involve cAMP but is mediated by changes in internal [Ca2+]
(Davies et al., 1995).
|
Immunocytochemical localization of TRP-like material in the M. sexta
CNS
To determine the possible neuronal source(s) of TRP acting on the
Malpighian tubules, we employed immunocytochemistry. The LomTK antiserum used
in this study is known to recognize the well-preserved carboxy terminus of
TRPs in insects and crustaceans
(Nässel, 1993;
Lundquist et al., 1994
;
Muren and Nässel, 1996
;
Christie et al., 1997
). This
antiserum does not cross-react with other known insect peptides
(Lundquist et al., 1994
;
Muren and Nässel, 1996
;
Christie et al., 1997
).
Preabsorption controls of antiserum with synthetic LomTK-I performed here
abolished all immunoreactivity in M. sexta. We thus propose that the
material reacting with the antiserum is related to the insect TRPs.
A small subset of neurons in the central nervous system of larval and adult M. sexta had LomTK-like immunoreactive (LTKLI) material; most of these immunoreactive neurons were located in the brain. The brain of the fifth instar larva, for example, contains about 60 LTKLI neuronal cell bodies (Figs 7A, 8A). These form extensive arborizations in brain neuropil (Figs 7B, 8B). One pair of large neurons (DN in Fig. 7) with extensive arborizations in the brain send axons to the ventral nerve cord.
|
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In the adult brain a large number (more than 100 in the midbrain and additional ones in the optic lobe) of LTKLI neurons are present. These supply immunoreactive processes to major neuropil regions such as the central body (Fig. 9A), the calyces of the mushroom bodies (Fig. 9B), the lobula plate and medulla of the optic lobes (Fig. 9C-E) and the antennal lobes (Fig. 9F,G). In the antennal lobes all the conventional glomeruli (Fig. 9F), as well as those of the macroglomerular complex (Fig. 9G), contain varicose LTKLI fibres.
|
The ganglia of the ventral nerve cord of fifth-instar larvae contain smaller numbers of LTKLI cell bodies: the suboesophageal ganglion has five pairs, the thoracic ganglia each have two bilateral pairs and a dorsal unpaired neuron medially, the unfused abdominal ganglia each have only one pair, and there are three pairs in the fused terminal ganglion (Fig. 10). In the abdominal ganglia there are LTKLI processes arborizing in the central neuropil (Fig. 8C,D). Some of these appear to be derived from afferent sensory axons in the root of nerve 1 (Fig. 8C). No efferent axons were seen in any ganglion, but intersegmental LTKLI axons interconnect the ventral nerve cord, as well as the cord and the brain (see Fig. 7B). The abdominal ganglia of pharate adults displayed an additional pair of LTKLI cells anteriorly; in the thoracic ganglia the immunoreactivity in cell bodies was weak and inconsistent. The afferent LTKLI fibres of the anterior abdominal nerve roots were not seen in pharate adults. Neither in the brain nor in the ventral nerve cord could we resolve LTKLI material in neurosecretory cells with efferent axons terminating in neurohaemal release sites (such as the corpora cardiaca and segmental perisympathetic organs).
|
Immunocytochemical localization of TRP-like material in
peripheral tissues in M. sexta
The larval heart did not contain any LTKLI. In the midgut of both larvae
and pharate adults there are LTKLI endocrine cells
(Fig. 8E-G), especially at the
base of the Malpighian tubules. These endocrine cells span the epithelium and
reach both the gut lumen and the outer surface of the gut
(Fig. 8F,G). No
immunoreactivity was found associated with the foregut, hindgut or Malpighian
tubules proper. Similar LTKLI endocrine cells were found in L.
migratoria and it was shown that these cells are the likely to be the
source of circulating TRPs in the locust
(Winther and Nässel,
2001).
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Discussion |
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Peptidergic regulation of fluid secretion in M. sexta
We find that several classes of peptides cause an increase in the rate of
fluid secretion in M. sexta Malpighian tubules: the leucokinins,
cardioacceleratory peptides and tachykinin-related peptides.
The only leucokinin investigated, leucokinin I (DPAFNSWG-NH2),
stimulated rapid fluid secretion in M. sexta tubules
(Fig. 3), an effect similar to
that previously observed in the mosquito Aedes egypti
(Hayes et al., 1989), the
cricket Acheta domestica (Coast et
al., 1991
) and in adult D. melanogaster
(O'Donnell et al., 1996
).
Leucokinins have been biochemically isolated from several insect species,
including lepidopterans (Torfs et al.,
1999
), although not from M. sexta. However, it is likely
that M. sexta contains leucokinin or leucokinin-like peptides since
leucokinin-like immunoreactivity has been reported in a bilateral pair of
neurosecretory cells in the M. sexta abdominal nerve cord that
project axons to the neurohaemal perivisceral organs
(Chen et al., 1994
). The same
study reported that the leucokinin-like immunopositive cells are also
immunopositive for M. sexta diuretic hormone
(Audsley et al., 1993
),
suggesting that these neurons are involved in hormonally regulating Malpighian
tubule activity. The direct effect of leucokinin I on isolated M.
sexta tubules reported here supports this hypothesis.
Among the cardioacceleratory peptides (CAPs) tested, a CAP1a/1b mixture and
CAP2c, both of which have been partially purified from M. sexta nerve
cord extracts (Cheung et al.,
1992), each caused an increase in the rate of fluid secretion. The
time course of the two responses was quite different
(Fig. 4), suggesting that each
may be mediated by a separate receptor and intracellular pathway.
Unexpectedly, CAP2b is without effect on fluid secretion by M.
sexta tubules. This result is surprising because CAP2b is a potent
regulator of tubule activity in other insects, stimulating fluid secretion in
D. melanogaster (Davies et al.,
1995,
1997
) and inhibiting fluid
secretion in R. prolixis (Quinlan
et al., 1997
). Although is it clear that CAP2b does not act on
pharate adult tubules, it is possible that CAP2b affects fluid secretion in
larval Malpighian tubules, but support for this hypothesis must await the
results of future experiments.
All three tachykinin-related peptides (TRPs) tested, like leucokinin I, CAP
1a/1b and CAP2c, cause an increase in the rate of fluid secretion by M.
sexta Malphigian tubules (Fig.
5). This may indicate a physiological role for them because the
immunocytochemical data presented here (Figs
7,8,9,10)
indicate the presence of TRP-like material in neurons in the M. sexta
CNS and also in certain peripheral locations. Although TRPs have not been
isolated from M. sexta, their effects on M. sexta tubules,
TRP-like immunoreactivity in the M. sexta CNS, plus the large number
of closely related peptides in the TRP peptide family and their broad
distribution in several other insects
(Nässel, 1999), combine
to suggest the possibility that M. sexta contains endogenous TRPs.
Interestingly, we could not detect TRPs in traditional neurosecretory cells in
the CNS of M. sexta. Thus the likely source of any circulating TRPs
that might act on the Malpighian tubules is the endocrine cells of the midgut.
Similar TRP-containing endocrine cells have been demonstrated in the midgut of
L. migratoria and recently it has been demonstrated that locust TRPs
(LomTKs) can be released from the midgut and that the haemolymph contains
nanomolar levels of TRPs (Winther and
Nässel, 2001
).
The presence of TRPLI cells in M. sexta suggests that the TRPs used in this study, although obtained from other species, are probably binding to endogenous M. sexta TRP receptors on tubules, mimicking the actions of endogenous TRPs that are yet to be identified. Moreover, two results suggest the testable hypothesis that the heterologous TRPs applied here might be acting through a common receptor and intracellular pathway. The time course of tubule activation and the duration of the effect was similar for all three TRPs (Fig. 5). In addition, application of a second TRP on tubules already stimulated by a maximal concentration of a different TRP failed to produce any further increase in fluid secretion rate (data not shown). Although these data are indirect, they support the hypothesis that the TRPs are acting through a common receptor-mediated pathway.
Coordination and control of peripheral tissues by multiple chemical
signals
A defining characteristic of any metazoan animal is a system to coordinate
and control the functioning of the different parts of the body, provided by
the central nervous system (CNS) in most animals. The CNS exerts its control
in two main ways: by direct innervation of different organs and by the release
into the extracellular fluid of hormones, either neurohormones directly from
the central nervous system or other hormones from glands themselves controlled
by the central nervous system. For example, to control the complex moulting
process and metamorphosis, insects use a range of different hormones,
including 20-hydroxyecdysone, the juvenile hormones, eclosion hormone,
ecdysis-triggering hormone, CCAP and bursicon.
Surprisingly large numbers of substances, hormones and other compounds, are
found to affect even such relatively simple insect organs as the Malpighian
tubules. There are at least six groups of neuropeptides so far known to affect
the rate of fluid secretion: (1) the diuretic hormones related to the
corticotrophin-releasing factors of vertebrates
(Kay et al., 1992;
Audsley et al., 1993
;
Coast, 1996
); (2) the
leucokinins, which stimulate rapid fluid secretion by the Malpighian tubules
of Aedes egypti (Hayes et al.,
1989
) and adult D. melanogaster
(O'Donnell et al., 1996
); (3)
the cardioacceleratory peptides, primarily CAP2b in D. melanogaster
(Davies et al., 1995
,
1997
) and R. prolixus
(Quinlan et al., 1997
); (4)
the calcitonin-like diuretic hormones
(Furuya et al., 2000
;
Coast et al., 2001
); (5) the
TRPs (present study); and (6) the recently discovered antidiuretic factor in
the beetle Tenebrio molitor
(Eigenheer et al., 2002
),
found to be unrelated to any other known biologically active neuropeptide. In
addition to peptidergic regulation, insect Malpighian tubules are also
controlled by simple biogenic amines such as dopamine and 5-hydroxytryptamine
(5-HT; e.g. Maddrell et al.,
1971
,
1991
;
Morgan and Mordue, 1984
).
Finally, cAMP and cGMP applied extracellularly cause acceleration of secretion
by tubules of many insects, but those of adult D. melanogaster are so
sensitive to these compounds as to raise the possibility that they may act as
hormones (Riegel et al.,
1998
).
We report here a wide range of compounds, all likely to derive from the
central nervous system, that affect fluid secretion rates by Malpighian
tubules of adult M. sexta. The tubules are stimulated by two biogenic
amines (serotonin and octopamine), two cyclic nucleotides (cAMP and cGMP), and
three different peptide classes (leucokinins, CAPs and TRPs); a separate study
has shown that a fourth peptide, M. sexta diuretic hormone, Mas-DH,
also stimulates fluid secretion by M. sexta tubules
(Audsley et al., 1993). The
variety of stimulants is matched by a concomitant variety in the effects they
produce on fluid secretion, particularly in their speed of action and the
extent of stimulation. M. sexta tubules appear to be regulated by at
least eight different chemical substances, all of which are thought to be
endogenous and all of which cause large increases in the rate of fluid
secretion.
One explanation for such a range of stimulants is that many separate
hormones may be needed to control separate activities of the tubules. For
example, locust diuretic peptide and locustakinin work via different
second messengers and differentially affect movements of Na+ and
K+ ions (Coast,
1995). In adult D. melanogaster, separate controls exist
for accelerating the V-ATPase that drives secretion and for changes in
chloride permeability that allows anions to follow active transport of cations
(O'Donnell et al., 1996
).
Other activities of tubules, not directly part of fluid transport mechanisms,
such as alkaloid transport by M. sexta tubules
(Maddrell and Gardiner, 1976
)
or transport of proline by locust tubules
(Chamberlin and Phillips,
1982
), might in principle be affected by hormones, although none
such has yet been discovered. Any increase in such transport, however, would
certainly affect the rate of fluid secretion, although the effect would have
to be very large to modify the rate of fluid secretion significantly. We think
it unlikely that many of the eight different controlling agents we describe
here, all of which have large effects on the rate of fluid secretion, exert
their effects via changes in pathways not directly concerned with
fluid secretion. Indeed, they are not tissue-specific hormones that force
stereotypical responses by their target tissue, which becomes abundantly clear
with the finding that they affect other organs in the insect.
All the substances tested in this paper also have cardioacceleratory
effects on the pharate adult heart in M. sexta
(Tublitz and Truman, 1985;
Tublitz et al., 1991
;
Cheung et al., 1992
; Heusmann
et al., 1995; and H. McGraw and N. J. Tublitz, unpublished data) and the
concentrations of these substances that produced threshold and maximal effects
on the heart are similar to those observed when the same substances are
applied to pharate adult Malpighian tubules, i.e. the effective physiological
concentrations are the same for both tissues. It is reasonable to predict,
therefore, that these substances, if released into the blood as hormones,
would probably act on both the heart and the Malpighian tubules. All the
evidence to date in M. sexta for all the substances tested here
indicate that they are likely to be released humorally. For example, three of
the four peptide classes (CAPs, leucokinins and diuretic hormone-like
peptides) that stimulate fluid secretion in M. sexta have been shown
to be immunolocalized to neurosecretory cells in the abdominal nerve cord that
project to the neurohaemal perivisceral organs (PVOs;
Ewer et al., 1997
;
Chen et al., 1994
).
Octopamine-containing ventral unpaired median cells also terminate at the PVOs
(Lehman et al., 2000
), and
some serotonergic neurons in M. sexta project to neurohaemal release
sites (Radwan et al., 1989
).
Finally the immunocytochemical data presented here for the TRPs suggest that
they too might act in a hormonal fashion, possibly by release from the midgut.
Hence every substance tested in this study, with the exception of the two
cyclic nucleotides, has the potential to act as a hormone in M.
sexta.
To explain the wide range of compounds that can affect at least two different insect organs, a new hypothesis, speculative at this stage, may be needed. We suggest that in the extracellular fluid of an insect is an ever-changing array of different chemical signals, be they peptides, amines or other compounds, that direct the most appropriate functioning of one or more parts of the body. Put more fancifully, we suggest that there may exist in the extracellular fluid a continuous broadcast of information in the form of a chemical language, to which many or all parts of the body continuously respond on a moment-to-moment basis and which, because of the greater information in it, ensures a more effective and efficient coordination of function than could be achieved by a series of single, tissue-specific hormones that force stereotypical responses by their target tissue(s).
For example, from the complexity of effects produced by the substances tested in this study on the Malpighian tubules and the heart, we think that these substances may act in concert with each other and with other circulating hormones to produce physiologically distinct responses in these and other target tissues in M. sexta.
It is not a requirement of our hypothesis that hormones that affect one
system must always affect other systems. As noted above, CAP2b, a potent
cardiac stimulant in pharate adult M. sexta, has no effect on the
Malpighian tubules of the same insect at the same stage. And, in locusts, the
ion-transport peptide (ITP) has no effect on the Malpighian tubules, although
it has potent effects on active transport of Cl- by the rectum and
ileum, while Locusta-DH, a stimulant of the Malpighian tubules, has no effect
on the rectum and ileum (Coast et al.,
1999). Some organs may require specific signals at times and may
ignore others.
If the arguments advanced here are correct, they may go some way towards
explaining the difficulties in interpretation surrounding other hormonally
controlled systems in insects and other animals. For example, the way in which
hormones are thought to be involved in the control of events leading up to
ecdysis in insects (the emergence of an insect from its cast skin as the
culmination of the moulting process) has become ever more complex
(Ewer et al., 1997;
Kingan et al., 1997
;
O'Brien and Taghert, 1998
). If
it is the case that events in an animal are at least partly controlled by an
internal language with a rich array of `words' (each a circulating chemical
signal), then this complexity should not be surprising, but expected.
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Acknowledgments |
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References |
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Audsley, N., Coast, G. M. and Schooley, D. A.
(1993). The effects of M. sexta diuretic hormone on
fluid transport by the Malpighian tubules and cryptonephric complex of M.
sexta. J. Exp. Biol. 178,231
-243.
Chamberlin, M. E. and Phillips, J. E. (1982). Regulation of hemolymph amino acid levels and active secretion of proline by Malpighian tubules of locusts. Can. J. Zool. 60,2745 -2752.
Chen, Y., Veenstra, J. A., Davis, N. T. and Hagedorn, H. H. (1994). Leucokinin and diuretic hormone immunoreactivity in the tobacco hornworm, M. sexta, and co-localization of this immunoreactivity in lateral neurosecretory cells of the abdominal ganglia. Cell Tissue Res. 278,493 -507.[Medline]
Cheung, C. C., Loi, P. K., Sylwester, A. W., Lee, T. D. and Tublitz, N. J. (1992). Primary structure of a cardioactive neuropeptide from the tobacco hawkmoth, M. sexta. FEBS Lett. 313,165 -168.[Medline]
Christie, A. C., Lundquist, C. T., Nässel, D. R. and
Nusbaum, M. P. (1997). Two novel tachykinin-related peptides
from the nervous system of the crab Cancer borealis. J. Exp.
Biol. 200,2279
-2294.
Coast, G. M. (1995). Synergism between diuretic peptides controlling ion and fluid transport in insect Malpighian tubules. Regul. Pept. 57,283 -296.[Medline]
Coast, G. M. (1996). Synergism between diuretic peptides controlling ion and fluid transport in insect Malpighian tubules. Peptides 17,327 -336.[Medline]
Coast, G. M., Cusinato, O., Kay, I. and Goldsworthy, G. J. (1991). An evaluation of the role of cAMP as an intracellular second messenger in Malpighian tubules of the house cricket, Acheta domesticus. J. Insect Physiol. 37,563 -573.
Coast, G. M., Meredith, J. and Phillips, J. E.
(1999). Target organ specificity of major neuropeptide stimulants
in locust excretory systems. J. Exp. Biol.
202,3195
-3203.
Coast, G. M., Webster, S. G., Schegg, K. M., Tobe, S. S. and
Schooley, D. A. (2001). The Drosophila melanogaster
homologue of an insect calcitoninlike diuretic peptide stimulates V-ATPase
activity in fruit fly Malpighian tubules. J. Exp.
Biol. 204,1795
-1804.
Davies, S. A., Huesmann, G. R., Maddrell, S. H. P., O'Donnell,
M. J., Skaer, N. J. V., Dow, J. A. T. and Tublitz, N. J.
(1995). CAP2b, a cardioacceleratory peptide, is present in
Drosophila and stimulates fluid secretion by Malpighian tubules via
cyclic GMP. Am. J. Physiol.
269,R1321
-R1326.
Davies, S. A., Stewart, E. J., Huesmann, G. R., Skaer, N. J. V., Maddrell, S. H. P., Tublitz, N. J. and Dow, J. A. T. (1997). Neuropeptide stimulation of the nitric oxide signalling pathway in Drosophila melanogaster Malpighian tubules. Amer. J. Physiol. 273,823 -827.
Dow, J. A. T. and Maddrell, S. H. P. (1993). Fluid secretion by the Malpighian tubule of Drosophila melanogaster is stimulated by nitric oxide and cyclic GMP. J. Physiol. 473,233 P.
Dow, J. A. T., Maddrell, S. H. P., Davies, S.-A., Skaer, N. J.
V. and Kaiser, K. (1994). A novel role for the nitric
oxide/cyclic GMP signalling pathway: the control of epithelial function in
Drosophila. Am. J. Physiol.
266,R1716
-R1719.
Eigenheer, R. A., Nicolson, S. W., Schegg, K. M., Hull, J. J.
and Schooley, D. A. (2002). Identification of a potent
antidiuretic factor acting on beetle Malpighian tubules. Proc.
Natl. Acad. Sci. USA 99,84
-89.
Ewer, J., Gammie, S. C. and Truman, J. W.
(1997). Control of insect ecdysis by a positive-feedback
endocrine system: roles of eclosion hormone and ecdysis triggering hormone.
J. Exp. Biol. 200,869
-881.
Furuya, K., Milchak, R. J., Schegg, K. M., Zhang, J. R., Tobe,
S. S., Coast, G. M. and Schooley, D. A. (2000). Cockroach
diuretic hormones: Characterization of a calcitonin-like peptide in insects.
Proc. Natl. Acad. Sci. USA
97,6469
-6474.
Hayes, T. K., Pannabecker, T. L., Hinckley, D. J., Holman, G. M., Nachman, R. J., Petzel, D. H. and Beyenbach, K. W. (1989). Leucokinins, a new family of ion transport stimulators and inhibitors in insect Malpighian tubules. Life Sci. 44,1259 -1266.[Medline]
Holman, G. M., Cook, B. J. and Nachman, R. J. (1996). Primary structure and synthesis of a blocked myotropic neuropeptide isolated from the cockroach, Leucophaea maderae. Comp. Biochem. Physiol. C 85,219 -224.
Huesmann, G. R., Cheung, C. C., Loi, P. K., Lee, T. D., Swiderek, K. M. and Tublitz, N. J. (1995). Amino acid sequence of CAP2b, an insect cardioacceleratory peptide from the tobacco hawkmoth, M. sexta. FEBS Lett. 371,311 -314.[Medline]
Kay, I., Patel, M., Coast, G. M., Totty, N. F., Mallet, A. I. and Goldsworthy, G. J. (1992). Isolation, characterization and biological activity of a CRF-related diuretic peptide from Periplaneta americana L. Regul. Pept. 42,111 -122.[Medline]
Kingan, T. G., Gray, W., Zitnan, D. and Adams, M. E.
(1997). Regulation of ecdysis-triggering hormone release by
eclosion hormone. J. Exp. Biol.
200,3245
-3256.
Lehman, H. K., Klukas, K. A., Gilchrist, L. S. and Mesce, K. A. (2000). Steroid regulation of octopamine expression during metamorphic development of the moth M. sexta. J. Comp. Neurol. 424,283 -296.[Medline]
Lundquist, C. T., Clottens, F. L., Holman, G. L., Riehm, J. P., Bonkale, W. and Nässel, D. R. (1994). Locustatachykinin immunoreactivity in the blowfly central nervous system and intestine. J. comp. Neurol. 341,225 -240.[Medline]
Maddrell, S. H. P., Pilcher, D. E. M. and Gardiner, B. O. C. (1969). Stimulatory effect of 5-hydroxytryptamine (serotonin) on secretion by Malpighian tubules of insects. Nature, Lond. 222,784 -785.[Medline]
Maddrell, S. H. P., Pilcher, D. E. M. and Gardiner, B. O. C. (1971). Pharmacology of the Malpighian tubules of Rhodnius and Carausius: the structure-activity relationship of tryptamine analogues and the role of cyclic AMP. J. Exp. Biol. 54,779 -804.[Medline]
Maddrell, S. H. P. and Gardiner, B. O. C. (1976). Excretion of alkaloids by Malpighian tubules of insects. J. Exp. Biol. 64,267 -281.[Abstract]
Maddrell, S. H. P., Herman, W. S., Mooney, R. L. and Overton, J. A. (1991). 5-Hydroxytryptamine: a second diuretic hormone in Rhodnius. J. Exp. Biol. 156,557 -566.[Abstract]
Maddrell, S. H. P., Herman, W. S., Farndale, R. W. and Riegel,
J. A. (1993). Synergism of hormones controlling epithelial
fluid transport in an insect. J. Exp. Biol.
174, 65-80.
Morgan, P. J. and Mordue, W. (1984). 5-hydroxytryptamine stimulates fluid secretion in locust Malpighian tubules independently of cAMP. Comp. Biochem. Physiol. C 79,305 -310.[Medline]
Muren, J. E. and Nässel, D. R. (1996). Isolation of five tachykinin-related peptides from the midgut of the cockroach Leucophaea maderae: existence of N-terminally extended isoforms. Regul. Peptides 65,185 -196.[Medline]
Nässel, D. R. (1993). Insect myotropic peptides: Differential distribution of locustatachykinin- and leucokinin-like immunoreactive neurons in the locust brain. Cell Tissue Res. 274,27 -40.[Medline]
Nässel, D. R. (1999). Tachykinin-related peptides in invertebrates: a review. Peptides 20,141 -158.[Medline]
Nicolson, S. W. (1976). Diuresis in the cabbage white butterfly, Pieris brassicae: fluid secretion by the Malpighian tubules. J. Insect Physiol. 22,1347 -1356.
Nicolson, S. W. and Millar, R. P. (1983). Effects of biogenic amines and hormones on butterfly Malpighian tubules: dopamine stimulates fluid secretion. J. Insect Physiol. 29,611 -615.
O'Brien, M. A. and Taghert, P. H. (1998). A
peritracheal neuropeptide system in insects: release of myomodulin-like
peptides at ecdysis. J. Exp. Biol.
201,193
-209.
O'Donnell, M. J., Dow, J. A. T., Huesmann, G. R., Tublitz, N. J. and Maddrell, S. H. P. (1996). Separate control of anion and cation transport in Malpighian tubules of Drosophila melanogaster.J. Membr. Biol. 132,63 -76.
Orchard, I. (1989). Serotonergic neurohaemal tissue in Rhodnius prolixus: synthesis, release and uptake of serotonin. J. Insect Physiol. 35,943 -947.
Prier, K. R., Hwa, O. and Tublitz, N. J.
(1994). Modulating a modulator: Biogenic amines at subthreshold
levels potentiate peptide-mediated cardioexcitation in an insect heart.
J. Exp. Biol. 197,377
-392.
Quinlan, M. C., Tublitz, N. J. and O'Donnell, M. J.
(1997). Anti-diuresis in the blood-feeding insect Rhodnius
prolixus Stål: the peptide CAP2b and cyclic GMP inhibit Malpighian
tubule fluid secretion. J. Exp. Biol.
200,2363
-2367.
Radwan, W. A., Granger, N. A. and Lauder, J. M. (1989). Development and distribution of serotonin in the central nervous system of M. sexta sexta during embryogenesis. II. The ventral ganglia. Int. J. Dev. Neurosci. 7, 43-53.[Medline]
Ramsay, J. A. (1954). Active transport of water by the Malpighian tubules of the stick insect, Dixippus morosus (Orthoptera; Phasmidae). J. Exp. Biol. 31,104 -113.
Riegel, J. A., Maddrell, S. H. P., Farndale, R. W. and Caldwell,
F. M. (1998). Stimulation of fluid secretion of Malpighian
tubules of Drosophila memaogaster by cyclic nucleotides of inosine,
cytidine, thymidine and uridine. J. Exp. Biol.
201,3411
-3418.
Schoofs, L., Vanden Broeck, J. and de Loof, A. (1993). The myotropic peptides of Locusta migratoria: Structures, distribution, functions and receptors. Insect Biochem. Mol. Biol. 23,859 -881.[Medline]
Spring, J. H. (1990). Endocrine regulation of diuresis in insects. J. Insect Physiol. 36, 13-22.
Stangier, J., Hilbich, C., Dircksen, H. and Keller, R. (1988). Distribution of a novel cardioactive neuropeptide (CCAP) in the nervous system of the shore crab Carcinus maenas.Peptides 9,795 -800.[Medline]
Torfs, P., Nieto, J., Veelaert, D., Boon, D., van de Water, G.,
Waelkens, E., Derua, R., Calderon, J., de Loof, A. and Schoofs, L.
(1999). The kinin peptide family in invertebrates.
Ann. NY Acad. Sci. 897,361
-373.
Tublitz, N. (1989). Insect cardioactive peptides: neurohormonal regulation of cardiac activity by two cardioacceleratory peptides during flight in the tobacco hawkmoth, M. sexta. J. Exp. Biol. 142,31 -48.[Abstract]
Tublitz, N. J., Brink, D., Broadie, K. S., Loi, P. K. and Sylwester, A. W. (1991). From behavior to molecules: an integrated approach to the study of neuropeptides. Trends Neurosci. 14,254 -259.[Medline]
Tublitz, N. J. and Loi, P. K. (1993). Steroid
regulation of transmitter phenotype in individual insect peptidergic neurons.
II. The prepupal peak of 20-OH ecdysone directly induces bursicon expression.
J. Exp. Biol. 181,195
-213.
Tublitz, N. J. and Truman, J. W. (1985). Insect cardioactive peptides. I. Distribution and molecular characteristics of two cardioacceleratory peptides in the tobacco hawkmoth, M. sexta. J. Exp. Biol. 114,365 -379.[Abstract]
Winther, Å. M. E. and Nässel, D. R.
(2001). Intestinal peptides as circulating hormones: release of
tachykinin-related peptide from the locust and cockroach midgut. J.
Exp. Biol 204,1269
-1280.
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