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Tissue-specific changes in polyamine levels of neural tissue and fat body in adult crickets.

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Archives of Insect Biochemistry and Physiology 24:203-217 (1 993)
Tissue-Specific Changes in Polyamine Levels
of Neural Tissue and Fat Body in Adult
Crickets
Colette Strambi, Philippe Faure, Marielle Renucci, Pierre Charpin, Roger
Augier, Alain Tirard, and Alain Strambi
C N R S , Lnhurntoirc de NeurobioloXic, Marseille, Funrice
The three major polydmines-putrescine, sperniidine, and spermine-were studied
2nd changes of their levels were examined in extracts of cerebral ganglia and fat body
from adult Achets donwsticus. In nervous tissue, only spermidine and sperrnine were
present and spcrmine was two- to three-fold more abundant than spermidinc. The
polyarnine levels were high up to day 3 , decreased on day 4, and then reniained
relatively unchanged up to day 10. The spcrniidine/spermine ralios decreasedduring
the imaginal life. Higher spcrmidine titles were observed in the neural tissue of
egg-laying females cornparcd to virgin females. In the fat body, putrescine was
detected togethvr with spermidine and spermine. Spermidine and spernmine Icvels
were two-fold higher than putrcscine. Fat body of virgin females contained two times
mow polyaniines than male fat body. Low at emergence, spermjdine and spermine
concentrations peaked on days 2-3 only in females, and egg-laying was Characterized
b y an increase of putrescine and spermidine titres. Starvation did not change
polyamine contents, implying homeostatic regulation of the intracellular polyamine
metabolism. These data showing tissue specific changes in polyamine levels during
the imaginal life of Achet'i domesticus point to the physiological importance of
polyamines as possible intracellular regulators during adult insect development. c
I'JW Wiley-Li.5. In(.
Key words: Achcta domesticus, polyamines, neural tissue, fat body
INTRODUCTION
Numerous studies performed in vertebrates have documented the physiological importance of the major naturally occurring polyamines: putrescine,
spermidine a n d spermine [see for reviews 1-5 and for books 6, 71. These
polycations are required for growth and development. Their effects on gene
Arknowledgmcnts: l h e autliorS thank Dr. N. Seiler (Marion Merrell Dow Research Institute, France)
for helpful suggestions during the courw of this study.
Received February 16, 1993; accepted April 13, 1933
Address reprint requests to Colette Strambi, CNRS, Labortitoirede Nwrobiolugie, $ 1 Chemin loseph
Aiguier, 13402 Marseille Ccdex 20, Frmce.
0 1993 Wiley-Liss, Inc.
204
Strambi et al.
expression, suggesting a selective role in the expression of specific growth-related genes [8,9], as well as their function in cellular differentiation [ l O , l l ] have
been demonstrated. Moreover, endocrine stimuli are known to stimulate polyamine biosynthesis through the activation of ornithine decarboxylase (ODC"),
the first key enzyme in the polyamine biosynthetk pathway [12,13]. I'olyamines
are also able to modulate protein phosphorylation, either positively through the
activation of casein kinase TI or negatively through the activation of protein
phosphatases [ 14/15], It has been recently reported that membrane-associated
polyamines pldy a role in the regulation of the Ca + pump in the plasma
membrane via interactions with polyphosphoinositides [16].
In contrast, only a few studies have appeared concerning polyamines in
insects, and most of our knowledge concerns pre-imaginal development. For
example, polyamine determinations were performed throughout the life cycle
of D i w q h i l a iiielarzogaster [ 171 and Cnlliyhora erythroceplznla [18]as well as during
Drcxoyldn nielnirugnster embryogenesis [19]. Some studies also involved nondipteran groups [20-221. More recently, polyamines were analyzed during
specific steps of insect development in different tissues [23,24]. However,
precise data during adult development are lacking.
It must be added that the role of polyamines in insect physiology remains
unclear, despite the fact that putative effects of hormones on polyamines have
bccn suggested during insect development [23,25,26]. It has also been demonstra ted that polyamines could regulate insect protein phosphorylation [27-301.
In the present study, we examined the levels of polyamines during the
beginning of the imaginal life in the cricket Adictn donzcsticus. Previous studies
had demonstrated that during the first days of imaginal life, juvenile hormone
(JH) induced vitellogenin synthesis in the fat body and stimulated oocyte
growth [31-331. Recent findings also suggest that juvenile hormone may regulate polyamine biosynthesis during vitellogenesis in Drosoplzila nielcrizogtlster
[34]. It therefore seemed of interest to analyze polyamines in different tissues of
Adiefa dniiiesticirs and to determine if their temporal variations present a tissuespecific pattern, suggesting tissue-specific differences in the biosynthesis of
these polycations.
+
MATERIALS AND METHODS
Rearing Conditions
Insects were reared under a long day photoperiod (16h lighti8h dark) at 29°C
and 55% relative humidity. They were fed bran, wheat germ, and ground rabbit
chow; water was continuously available. Newly emerged adult females were
isolated and reared up to day 10 as virgins. Some females were maintained in
the presence of males and provided with an egg-laying substrate. They mated
and usually laid eggs from day 5; they were sacrificed on day 10, and their
spermatheca were checked to ascertain the success of mating. For starvation
experiments, isolated females were allowed to drink but were maintained
*Abbreviations used: I t 1 = juvenile IiorniniiP: ODC = ornithineclecarbnxylase; RP-HPLC = reverse
phase 11 i g1 p e r h rm aiice I iqu icl c hromdtograph y
Polyamines in Brain and Fat Body of Adult Crickets 205
without any food, either from emergence up to day 4 or from day 6 up to day
10. Adult males were studied from emergence to day 4.
Polyamine Determination
Insects were cold anesthetized at 0°C for 15 min before dissection. The
cerebral ganglia (brain plus suboesophageal ganglion) were dissected out in
saline, corpora cardiaca, and corpora allata, as well as frontal ganglion and any
trace of fat body were carefully removed. Internal fat body was extirpated under
saline [35] containing: Hepes 10 mM, NaCl 150 mM, KCll2 mM, MgC12 3 mM,
glucose 40 mM, CaC12 15 mM, adjusted to pH 7.2 and 390 mosmol. Tissue
samples were cleaned of hemolymph by rinsing with iced saline and after brief
blotting on filter paper, they were rapidly sonicated in 75 pl of ice-cold 0.4 N
HC104 (Merck) and then centrifuged at 10,000 g during 4 min at 4°C. The
supernatants were collected and stored at -20°C until further analysis; 100 pl of
0.1 N NaOH were added to the pellets for protein determination according to
the method of Bradford [36], using bovine serum albumin as a standard.
For polyamine determination, the tissue extracts and the standards were
dansylated according to a procedure described by Seiler [37]. Hemolymph and
tissue extracts were treated with a protocol adapted from Besson et al. [23].
Hydrochloride salts of putrescine, cadaverine, spermidine, spermine, and 1,7diarninoheptane (used as an internal standard) were purchased from Sigma,
dissolved in 0.4 N HC104 and used to prepare mixed polyamine standards.
Dansylation proceeded in glass vials by mixing 40 p1of HClO4 extracts, 10 p1 of
5 pM 1,7-diaminoheptane (internal standard), and 100 pl of 0.3 M Na2C03
(Mcrck), Initiated by adding 200 ~1 of a freshly prepared dansyl chloride (Sigma)
solution (5 mg/ml) in acetone (SDS, spectrosol grade), the reaction was allowed
to proceed overnight in the dark at room temperature.
The separation and quantification of polyamines were performed by reverse
phase high-performance liquid chromatography (RP-HPLC) using a Waters
system comprised of two model 510 pumps, a Wisp 700 autosampler, and a
NEC APC4 data module recorder integrator. A Merck F 1050 fluorescence
spectrophotometer detected fluorescence (350 nm excitation and 495 nm emission). The separations were performed on a RP18 Merck Lichrocart (25 x 4 mm,
5 pm) precolumn and a RP18, 100 CH Merck column (125 x 4 mm; spherical
packing 5 km). The solvent system was an acetonitrile/water gradient [23] at a
flow rate of 1 mlimin : acetonitrile 60% in water for 7 min, then acetonitrile 90%
for 10 min, and a 100% acetonitrile purge for 5 min. The column was re-equilibrated to initial 60% acetonitrile conditions during 10 min between two successive injections. For each determination, the dansylated samples were diluted 1:1
with acetonitrile and 100 p1 were injected onto the column equilibrated in 60%
acetonitrile.
Before RP-HPLC analysis, an additional purification adapted from Birnbaum
et al. [24] was applied to fat body extracts. After dansylation, the fat body
samples were mixed with 70 pl H g , vortexed, and applied to a Waters Sep-Pak
C18 cartridge. The Sep-Pak was washed with 4 ml of 20% methanol and the
polyamines were eluted with 2 ml of 100% methanol.
206
Strambi et al.
Data Analysis
The major polyamines were identified by their retention times compared to
those of standard polyamines. Peak areas were automatically measured by the
integrator and evaluated according to the calibration method [24]. Mixed polyamine standards from 10 to 70 pmol were reacted and chromatographed to
establish linear standard curves from which the absolute amounts of the polyamines were calculated. The absolute limit of detection per injection was -1
pmol for dansylated spermidine and dansyiated spermine and 7 pmol for
dansylated putrescine. Two blank injections were routinely run between calibrations and sample analysis.
The results were expressed as mean values * SEM. Significance of differences
(P < .02) was evaluated using the Mann-Whitney U test.
RESULTS
As seen in Figure 1, large differences were observed in the amount of each of
the polyamines in the different biological samples. Spermidine and spermine,
but not putrescine were detected in the nervous tissue (Fig. la). However,
putrescine could easily be detected in fat body extracts (Fig. l b ) as well as in
hemolymph samples where it represents the major polyamine (Fig. lc).
Developmental Changes in the Polyamine Levels in Adult Neural Tissue
Virgin females and males. The polyamine levels in cerebral ganglia were
studied from 3 h after emergence up to day 10 (Fig. 2). Generally, spermidine
and spermine concentrations exhibited a similar temporal pattern. In virgin
females (Fig. 2a), the polyamine concentrations significantly increased ( P < .02)
between emergence and day 1 (day 1, spermidine; 1,992 _t 187 pmol/mg;
syermine: 4,062 5 303 prnol/mg), remained high up to day 3, significantly ( P <
,005) dropped on day 4 (spermidine: 1,060 t 111 pmollmg; spermine: 2,714 -+
264 pmol/mg), and remained roughly constant thereafter {on day 30, spermidine: 1,234 I67 pmol/mg; spermine: 2,851 -C 126 pmollmg). Spermine was
present in higher quantities than spermidine; however, the spermidineispermine ratio significantly decreased ( P < .001) from day 1 (SD/SP: 0.49) to day 4
(SD/SP: 0.38).
A parallel study was performed in adult males (Fig. 2b). Although CNS
polyamine levels seemed to be somewhat lower in males than in females, the
differences were not significant. The main results were similar in both sexes.
As in virgin females, polyamine concentrations were significantly higher ( P
< .02) a t the onset of imaginal life, then dropped on day 3 and remained
relatively unchanged. The few titres recorded from 10-day-old adult males
did not differ significantly from those recorded for 4-day-old males (data not
Fig. 1 . RP-I iPLC separations of dansyldted polyaniines from different cricket tissues. (a) Cerebral
gangli;l: Only spermidine and spermine were detectable; (b) Fat body: Putrescine, spermidine, and
sperniinc appeared on the trace; ( c )tiernolymph: Large quantities of putrescine as well a s spermidine
and5perminewercevident. P = putrescine; SD = spermidine; SP = 5pcrmine; D A l i = 1,7-cliaminoheptane ( ~ d d e as
d internal standard).
DAH
r
0.00
0.00
v
I
I
I
f .oo
0 . b
1 .50
2.00
retention time (x 10' min)
"1'
L
0.00
0
I
.oo
!
b
DAH
I
0.50
I
1 00
I
1.50
I
2.00
retention time (x 10' min)
I
0.00
0.00
P
SD
I
I
0.50
1 .oo
retention time (X 10' min)
I
I
1.50
2.00
208
Strambi et al.
SP
ISD
a
P
Fig. 2. Dcvelopment changes in neural ti5we polyamine content during the beginning of imaginal
lite. The cerebral ganglia collected from emergence up to day 10 for virgin females (virg.) (a), and
from emergence up to day 4 for males (b) were assayed as described in Material and Methods. Each
column represents the mean value t S.E. Numbers indicate sample sizes. SD = sperrnidine; SP =
q~errnine;CNS = central nervoussystem.
shown). The spermidineispermine ratio differed during male imaginal development, significantly decreasing ( P < -02) from emergence (SD/SP:0.51) to day
3 (SD/SP:0.41).
Egg-laying and fasting females. As compared to virgin females, mated
females allowed to lay eggs presented an increased vitellogenic activity since
they continuously laid eggs from day 5 after emergence. We analyzed polyamine levels in the nervous tissue from 10-day-old egg-laying females (Fig. 3).
Spermidine levels were slightly but significantly higher ( P < .02)than those
recorded in virgin females homogenates of the same age.
In order to rule out the possible influence of nutritional factors, we also
compared the polyamine content of neural tissue of starved virgin females
versus fed virgin females (Fig. 3). No differences could be detected in spermidine or spermine, either after a starvation imposed from emergence to day 4 or
after a fasting period lasting from day 6 to day 10.
Polyamines in Brain and Fat Body of Adult Crickets 209
Fig. 3. Alterations in neural tissue polyamine levels from egg-laying and fasting females. Mated
females allowed to lay eggs were sacrificed on day 10. Virgin females (virg,) starved from emergence
up to day 4 or from day 6 up to day 10 were assdyed on day 4 or on day 10, respectively. The values
recorded can be compared to those observed in virgin females reared in standard conditions. It must
be noted that the total protein content of brain plus sub-oesophageal ganglion (-95 p g per complex)
was not significantly different for all animals studied. Each column represents the mean value s S.E.
Numhprs indicate saniple sizes. SD = spermidine; SP = spermine; CNS = central nervous system;
egg-lay. = egg-layingfwnales.
Developmental Changes in the Polyamine Levels in Adult Fat Body
Virgin females and males. The changes in fat body polyamine content
during adult development are shown in Figure 4. In contrast to data collected
for the nervous tissue, detectable putrescine amounts were present in fat body
extracts, although the levels of putrescine were low as compared to those of
spermidine and spermine.
In virgin females fat body, the putrescine level was very low at emergence
(1.9 ? 0.42 nmolimg), rapidly increased and was significantly higher on day 2
( P < .005), and then continued to increase up to the values recorded on day 10
(11.3 k 1.6 nmollmg). Female spermidine and spermine contents were in the
same range at emergence (spermidine: 6.8 & 1.04 nmollmg; spermine: 8.6 * 1.4
nmolimg). Their titres significantly peaked ( P < .001) on days 2 and 3, then
showed a marked reduction on day 4 ( P < ,002). Thereafter, the spermidine
content did not significantly differ from day 4 to day 10, whereas spermine level
rose between day 4 and day 6 then remained unchanged up to day 10. On day
10, spermidine and spermine concentrations were similar and close to 20 rf: 2.5
nmolimg.
The polyamine content of male fat body samples showed several differences
compared to female samples at the same times in adult development. At
emergence, all three polyamine levels were roughly half of those recorded in
females. Although their titres described the same initial increase as was seen in
females between emergence and days 2-3, the spermidine and spermine contents did not significantly drop on day 4. It also should be noted that in
10-day-old males, the fat body exhibited about four- to fivefold less polyarnines
210
Strambi et al.
virgin females
m males
Fig. 4. Developmenhl changes in fat body polyarnine content during the beginning of imaginal life.
Fat body from virgin females (light columns) was collected from emergence up to day 10. Fat body
from males (dark columns) was collected from emergence up to day 4 and on day 10. The samples
were assayed as described in Material and Methods. Each column represents the mean value 1- S.E.
Numbers indicate sample sizes. nd = a55ay not done. (a) Putrescine levels; (b)sperrnidine levels; (c)
sperniine levels.
than did virgin female fat body of the same age (putrescine: 2 t 0.6 nmol/mg;
spermidine: 3.3 5 0.2 nmol/mg; spermine: 5.1 2 0.3 nmol/mg).
Egglaying and fasting females. As shown in Figure 5, egg-laying females
exhibited a large and significant increase of their fat body putrescine (P < .001)
and spermidine levels (P < .002) compared to levels recorded for virgin female
fat body samples. Starvation from emergence to day 4 did not change the fat
body polyamine content, whereas females fasting from day 6 to day 10 presented a significant decrease ( P < .002) only in their spermine titer (Fig. 5).
Polyamines in Brain and Fat Body of Adult Crickets 211
6
Fig. 5 . Alterations in fat body polyarnine levels from egg-laying and fasting females. Mated females
allowed to lay eggs were sacrificed on day 10. Virgin females (virg.) starved from emergence to day
4 or from day 6 to day 10 were assayed on day 4 or on day 10, respectively. The values recorded can
be compared to those observed in virgin females re,ired in standard conditions. Each column
represents mean value 5 S.E. Numbers indicate sample sizes. egg-lay. = egg-layingfemales.
DISCUSSION
As alluded to in the Introduction, our knowledge on polyamine distribution
and functions in insects is far from satisfactory. Most of the available data were
collected from embryonic and pre-imaginal stages. Only recently, Birnbaum et
al. [34] described a juvenile hormone (JH) stimulation of ornithine decarboxylase (ODC) activity during the vitellogenesis of Drosophila melaiiogaster.
212
Strambi et al.
Whereas polyamine levels in vertebrates nervous tissue have been determined in a variety of species [for review, 38,391, the only comparable data in
insects were obtained from brain-nerve cord complex during the fifth larval
instar of Mandiica sexta [24]. With the exception of the guinea pig, which
presented high putrescine levels in the range of 90 nmollg [40], the mammalian
brain was classically characterized by a relatively low putrescine concentration,
close to 10-15 nmol/g wet weight. The spermidine titres in mammalian brain
tissue usually varied between 300 and 600 nmol/g wet weight and were higher
than spermine levels, which were found to be between 300 and 400 nmol/g wet
weight [38,39]. Thus the data obtained for the nervous tissue of Manduca sexfa
during larval-pupal development: presence of putrescine (240 nmol/g wet
weight) and higher levels of spermidine (700 nmol/g wet weight) than of
spermine (210 nmol/g wet weight) [24], followed the pattern recorded in
vertebrates. By contrast, in the adult cricket central nervous system, putrescine
was not detectable and spermine was about threefold more represented than
spermidine. A similar distribution was observed in mouse neuroblastoma cells
in culture during their stationary phase [41]. From different works devoted to
the complex biosynthetic pathway of polyamines [42 and for review see 51, it is
now well known that putrescine inhibits spermine synthase. Thus in the absence
of putrescine, polyamine metabolism is shifted to the formation of spermine
from spermidine; such a regulation may be taking place in cricket nervous
tissue. It must also be remembered that in vertebrate nervous tissue, whereas
spermidine was found to be more abundant in nerves, spermine concentrations
were higher in neuron rich structures 1381, which is the case of insect neural
ganglia. The polyamine distribution observed in cricket appeared to be tissuespecific, especially with respect to the absence of detectable putrescine in
nervous tissue.
The protein content of cerebroid suboesophageal ganglia remained constant during the first 10 days of imaginal life in adult cricket. Therefore, the
changes observed in polyamine levels and in spermidine/spermine ratios
imply changes in polyamine metabolism during the early stages of adult life.
The temporal alterations observed in polyamine content (i.e., initially high, then
sharply dropping on day 4) were similar in both sexes and differed from those
described during the 5th larval instar of Manduccr sexta 1241. Our data in adult
cricket nervous tissue can be compared to the fluctuations recorded in rat
developing brain where levels of spermidine, high after birth, decreased before
the weaning period [43]. Similar observations were performed in numerous
other species [for review, see 38, 39, 441, and it is widely believed that in the
developing brain, high polyamine levels coincide with the maximal neuronal
proliferation and then gradually decline with brain maturation.
Our data showed that the polyamine titres in cricket nervous tissue were
unaffected by starvation, implying that there is a homeostatic component in the
developmental regulation of polyamine metabolism. Comparatively in the rat
brain, putrescine and spermidine levels were unchanged during reversible
hypoglycaemic coma, although a sharp increase in putrescine level was observed 3 h after recovery [45].
Hormonal or environmental factors are known to act on polyamine metabolism. For example, the interruption of active maternal behavior caused a de-
+
Polyamines in Brain and Fat Body of Adult Crickets 213
crease in brain polyamine levels in young rats [46]. Here, we showed that mated
egg-laying females of Acheta doinesticus exhibited an increase in brain spermidine levels, an effect that could possibly be due to the elevation of JH titre
observed in these females [47]. Consistent with this suggestion, removal of the
cricket corpora allata (which secrete JH) led to a significant decrease of spermidine concentration in the nervous tissue [48].
The polyamine content of the cricket fat body revealed a tissue-specific
pattern in the polyamine distribution as well as in their developmental profiles.
Putrescine was easily detected in fat body, although its titre was twofold less
than that of spermidine or spermine. The relative proportions of fat body
polyamines differed in larval M a ~ d t r c asexta [24] and in adult Acheta domesticus.
In the cricket, they appeared to be closer to the data recorded in rat liver, where
spermidine and spermine were in the same range, whereas putrescine levels
were much lower [49]. It is noteworthy that cricket fat body polyamine titres
were twofold higher in females than in males.
The proportions and roles of the natural polyamines were reviewed in recent
works [5,7,50-521. It is generally true that proliferating tissues have higher
putrescine and spermidine concentrations than corresponding nonproliferating
tissues. Moreover, numerous studies indicated a role for polyamines in protein
and RNA biosynthesis [19,53,54]. Thus the marked peak in fat body polyamine
concentrations observed on days 2-3 in adult female crickets, as well as the
higher values recorded in egg-laying females compared to virgin females, could
possibly be associated with vitellogenin synthesis. Since previous data showed
that increasing JH titres in young adult females of Acheta donzesticzts [31] coincide
with vitellogenin appearance [31,32,55], a function for JH in the regulation of
insect polyamine titres could be indicated. Recent experimental data, demonstrating JH stimulation of ODC activity during vitellogenesis in Dvosophila
rnelaiqaster [34], are consistent with this hypothesis.
Starvation did not strongly affect the polyamine content of fat body. Similar
results were reported fox vertebrate liver: no changes were observed in the total
spermidine and spermine contents in livers of chicks starved for 12 hours [56].
By contrast, in rat and mice, food deprivation decreased liver spermidine levels
and to a lesser extent those of spermine and led to an enhancement of liver
polyamine catabolism [49]. In Achefa dornesticus, the significant decrease in
spermine content observed in the fat body of females starved from day 6 to day
10 might result from polyamine interconversion reactions, which regulate, in
vertebrates, the intracellular polyamine metabolism [for review see 571,
The specific fluctuations in polyamine titres that characterize the cricket
nervous tissue mimic changes observed in vertebrates during brain maturation
[44]. However, if it is conceded that polyamines play a major role in the
maturation of brain cells, the exact sequence by which they assume this control
remains to be determined. Recent studies point to a regulatory role for polyamines in protein phosphorylation [58] and suggest that polyamines could be
considered as messengers in the regulation of casein kinase 11 activity in the cell
response to growth factors and hormones [59,60]. In insects, some recent findings may support this hypothesis: during the pre-imaginal life of Manduca sexta,
polyamines acting either through the stimulation of phosphatase activity or via
casein kinase 11, modulated the phosphorylation of several phosphoproteins
214
Strambi et al.
from the nervous tissue j27-291, Moreover, in Acheta domesticus, preliminary
studies revealed the ability of polyamines to modulate, in the nervous tissue
and the fat body, the phosphorylation of specific phosphoproteins that are
under hormonal control [48,61]. All these data support the concept that, in
invertebrates as well as in vertebrates, polyamines are important regulators of
cell functions.
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