Chem. Senses 27: 417-423,
2002
© Oxford University Press 2002
Are Polyamines Involved in Olfaction? An EAG and Biochemical Study in Periplaneta americana Antennae
1 CNRS, Laboratoire de Neurobiologie, FRE 2092, 31 chemin Joseph-Aiguier, F-13402 Marseille cedex 20, France 2 UMR 6116 Faculté des Sciences de St-Jérôme, Avenue Escadrille Normandie-Niemen, Boite 451, F-13397 Marseille cedex 20, France
Correspondence to be sent to: Alain Tirard, CNRS, IMEP, 31 chemin Joseph-Aiguier, F-13402 Marseille cedex 20, France. e-mail: tirard{at}lnb.cnrs-mrs.fr
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Abstract |
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Polyamines have been implicated in modulation of numerous cell functions. The purpose of this study was to assess the role of polyamines in intracellular regulation of insect antenna. Analysis of study data showed two main findings. First, in vivo treatment with the polyamine synthesis inhibitor
-difluoromethyl-ornithine enhanced the sensitivity of male
Periplaneta americana antenna to female pheromonal blend. Secondly,
polyamine modulated phosphorylation of several antennary proteins including
two found exclusively in antenna (30 and 48 kDa). In both of these exclusive
antennary proteins, phosphorylation changed after stimulation with the
pheromonal blend. These results suggest that polyamines play a regulatory role
in detection of female pheromonal blend and that modulation of protein
phosphorylation is one of the mechanisms involved in this regulation. |
Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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First described over 300 years ago (van Leeuwenhoek, 1678
), polyamines form an ubiquitous group of
low-molecular-weight aliphatic amines synthesized as intermediate products
during catabolism of arginin (Seiler,
1994). The most common polyamines, i.e. spermidine, spermine, and
their precursor putrescine, are present in significant quantities in all
living cells [for a review, see (Morgan
and Wallace, 1994)]. In mammals, polyamines are found in both
neurons and glial cells. The neuron is the main cellular locus of ornithine
decarboxylase (ODC), a key enzyme of the polyamine synthesis pathway
(Bernstein and Müller,
1999).
Polyamines have generated special interest because of their wide-ranging
ability to modulate biological activities underlying cellular signalling. In
the last two decades, many prokaryotic and eukaryotic physiological and
cellular functions including egg development in insects
(Kogan and Hagedorn, 2000)
have been shown to be polyamine-dependent [for a review, see
(Cohen, 1998)]. Polyamine
function has also been studied at the molecular level [for a review, see
(Igarashi and Kashiwagi,
2000)]. Previous studies have shown that polyamines not only
enhance transcription, processing and incorporation of RNA in ribosomes
(Blair, 1985) but also bind to
DNA and regulate gene expression
(Feuerstein et al.,
1991). Involvement of polyamines in regulation of
post-translational processes has also been reported. Our previous results in
the neural tissue of insects have shown that polyamines can modulate
intracellular protein phosphorylation patterns both positively and negatively
(Degrelle et al.,
1994).
Polyamines may act via protein kinases and phospho-protein phosphatases
(Morgan, 1990). In this
regard, in vitro experiments show that casein kinase II (CK II)
(Filhol et al.,
1991), a Ser/Thr protein kinase present in the nucleus and
cytoplasm of all eukaryotic cells, is markedly activated by polyamines. Leroy
et al. provided chemical evidence for the presence of a major
spermine binding domain on the ß subunit of CK II
(Leroy et al., 1995).
Polyamines have also been shown to stimulate phosphoprotein phosphatase 1 and
2A (Sjöholm and Honkanen,
2000). Spermine at physiological concentrations prevents
inactivation of protein kinase C (PKC) by reducing its insertion into the
hydrophobic core of the membrane (Monti
et al., 1994).
Polyamines have also been implicated in modulation of
N-methyl-D-aspartate (NMDA) receptors
(Romano and Williams, 1994)
involved in various forms of synaptic plasticity including some types of
associative long-term potentiation and long-term depression which may underlie
learning and memory (Collingridge and
Lester, 1989).
Intracellular polyamines modulate many ion channels
(Williams, 1997) including the
strongly inwardly rectifying potassium channels
(Lopatin et al.,
1995; Lee et al.,
1999; Guo and Lu,
2000a). Polyamines have also been shown to block cGMP-gated
channels of the retinal (Guo and Lu,
2000b) and olfactory membrane
(Lynch, 1999). Odour detection
by olfactory receptor neurons in mammals is mediated by Golf protein-coupled
receptors. When stimulated, these receptors induce a rapid increase in cAMP,
which in turn activates the olfactory-specific cyclic nucleotide-gated (CNG)
channel. Activation of these channels initiates neuronal depolarization and
mediates calcium (Ca2+) influx
(Menini, 1999).
In insects, olfactory transduction probably involves an IP3
cascade which leads to opening of IP3-dependent Ca2+
channels (Stengl et al.,
1999). PKC (Maida et
al., 2000) and Ca2+-dependent protein
phosphorylation (Schleicher et
al., 1994; Renucci et
al., 1996) have been implicated in this process. However, to
our knowledge, there is no direct evidence for either polyamine-dependent
regulation of odour detection or the presence or action of polyamines in
insect antennae. This study was designed to determine first whether polyamines
play a direct or indirect role in the control of the olfactory transduction
pathway in insects and second whether they modulate phosphorylation of
antennary proteins. The first question was addressed by electroantennography
(EAG) following treatment with -difluoromethyl-ornithine
(-DFMO), a known specific inhibitor of the polyamine synthesis pathway.
The second question was studied by sodium dodecyl sulphate
(SDS)—polyacrylamide gel electrophoresis (PAGE) after in vitro
phosphorylation of antenna extracts with or without addition of spermine.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Chemicals
Spermine was purchased from Sigma Aldrich Chimie (l'Isle d'Abeau Chesnes,
France) [
-32P]ATP (sp. act.: >4000 Ci/mmol) from ICN
Pharmaceuticals (Orsay, France), CK II from Upstate Biotechnology Incorporated
(Euromedex, Souffelweyersheim, France), and -DFMO from Ilex, Inc. (San
Antonio, TX).
Insects
Pending EAG recordings and phosphorylation experiments, newly emerged
Periplaneta americana males were isolated from females in 11 x
4 cm (diameter x depth) plastic dishes (three insects per dish). Dishes
were kept at 25-27C with a relative humidity of 70% and photocycle of 12 h
dark: 12 h light (dark phase beginning at 08:00 h). Insects were allowed free
access to dry dog food and water. All experiments were performed during the
first 8 h of the dark phase when sexual activity and sensitivity are optimal
(Hawkins and Rust, 1977).
Preparation of pheromonal blend
The natural pheromonal blend was obtained according to the impregnation
technique of Saas (Saas,
1983). Before the imaginal moult, 5-10 virgin females were
isolated from males in boxes containing Whatman no. 42 filter paper as shelter
material. After at least 2 weeks, the filter paper was removed and used as a
source of natural pheromonal blend. Comparative behavioural tests were carried
out to ascertain that the paper had the same attractive effect as a living
female. In the reference test, a receptive virgin female was introduced into a
plastic box containing three quiescent 20-day-old males. Within 15 s, males
stopped maintenance behaviour and crossed over to the female side of the box.
Wing fluttering was observed whenever a male made contact with another animal.
The same behaviour was observed within 15 s after introduction of each sheet
of filter paper impregnated with the pheromonal blend.
Electroantennography
Biological material
Fourteen -DFMO-treated males and 14 untreated males were used.
-DFMO treatment was performed on 10-day-old animals by replacing
drinking water with a 3% -DFMO solution. Treatment lasted for 5 days
and the solution was renewed every 2 days. Continuous video surveillance was
used to ascertain that treated as well as control animals drank regularly.
Odour cartridges
Odour cartridges used for EAG were prepared by sealing pieces (0.8 x
8 cm) of filter paper impregnated with the pheromonal blend in glass tubes.
Control cartridges were made with pieces of clean filter paper.
Experimental set-up
After cold anaesthesia, antennae were removed using microsurgical scissors
and mounted between two stainless steel electrodes (Syntech, Hilversum, The
Netherlands). Contact was maintained using electrically conductive gel
(Spectra 360, Parker Laboratories, Orange NJ, USA) which also prolonged
antenna viability by preventing loss of haemolymph. The pheromonal blend was
applied to the antenna by blowing a pulse of air (920 ml/min) through the
cartridge into a metal conduit carrying a continuous stream of humidified
carbon-filtered air (20 ml/s) over the antenna. To prevent `pressure shock',
the air blown through the cartridge was diverted from the stream in the main
conduit so that the total air flow over the antenna was constant. A recovery
period of 90 s was allowed between each stimulus to avoid receptor adaptation.
Odour cartridges were replaced after stimulation of two or three antennae.
Antenna response was expressed in millivolts (mV). Amplified data was stored
on a computer via an interface unit and data acquisition card (IDAC,
Syntech).
Data analysis
Pre-processing of data was performed using on EAG 2.3b software (Syntech).
For further analysis, data were transferred from EAG 2.3b to SchoolStat
v2.0.8. Responses were expressed as means in millivolts. Significant
differences (P<0.05) between two population were evaluated using
the nonparametric Mann—Whitney test.
Protein phosphorylation
Tissue and extract preparations
After cold anaesthesia, both antennae were removed from 15-day-old males.
One antenna from each animal was exposed to the paper impregnated with the
pheromonal blend and the other antenna was exposed to clean filter paper.
After 15 s of exposure, antennae were frozen in nitrogen and stored at
-20°C pending protein phosphorylation experiments. To allow identification
of polypeptides specific to the antenna by comparison with those contained in
other organs, the cerci, fat body, brain and legs were also dissected from the
same insects and stored under the same conditions.
Immediately before phosphorylation experiments, frozen tissues were
powdered at -80°C in a tissue grinder (Kontes/Fisher, Illkirch, France)
and homogenized in a buffer containing 20 mM Tris-HCl, 2 mM
ethylenediaminetetraacetic acid (EDTA) and 5 mM
ethyleneglycol-bis(betaaminoethyl-ether)-N,N,N',N'-tetraacetic
acid (EGTA), adjusted to pH 7.5. Homogenates were clarified by centrifugation
at 200 g for 5 min and the supernatants used immediately. All
procedures were carried out at 4C. Protein content in samples was estimated as
described by Bradford (Bradford,
1976) using bovine serum albumin as the standard. Extracts were
diluted to 1 µg protein per µl.
b. In vitro phosphorylation and SDS-PAGE separation
In vitro phosphorylation was performed by incubation in a medium
(final volume, 50 µl) containing 50 mM phosphate buffer pH 7.0, 10 mM
MgCl2, and 10 µM [-32P]ATP (1.3 µCi). The
reaction was initiated by adding 20 µg of biological extract per lane.
Incubation lasted 3 min at 37°C. When added, spermine was used at a final
concentration of 2 mM and CK II at 10 mU. If necessary, inactivation of
protein kinases was performed by heating samples to 55°C for 5 min. The
reaction was stopped by addition of 12.5 µl of a five-fold concentrated
SDS-sample buffer and heating to 90°C for 3 min as described by Laemmli
(Laemmli, 1970). Incubation
mixtures were then submitted to SDS—PAGE in 12.5% gels. After drying,
labelled polypeptides were visualized by autoradiography using Fuji RX films.
The duration of autoradiography was 48 h for all samples except brain extracts
(<24 h). All experiments were performed in triplicate.
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Effect of
-DFMO on male P. americana antenna sensitivity to
female pheromonal blend
As shown in Figure 1, the
response (in mV) of antennae from control males was significantly higher after
exposure to cartridges containing filter paper impregnated with the female
pheromonal blend (0.490 ± 0.19) than clean filter paper (0.110 ±
0.06). This was also the case for antennae from the -DFMO-treated males
(0.799 ± 0.4 versus 0.130 ± 0.07). Further comparison showed
that the mean response to the female pheromonal blend was significantly higher
for the 14 antennae from -DFMO-treated males than for the 14 antennae
from untreated control males (0.779 ± 0.4 versus 0.49 ± 0.19,
Mann—Whitney U-test, P = 0.021). This finding
demonstrates that -DFMO treatment significantly enhanced the
sensitivity of male antenna to the female pheromonal blend.
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In vitro effects of spermine and CK II on male antennal protein phosphorylation
As shown in Figure 2, lane B, over 12 phosphopolypeptides were routinely observed in control antennae. Addition of 2 mM spermine (lane A) enhanced phosphorylation of the 22, 23, 26/27, 30, 33, 37, 48, 51, 54 and 120 kDa phosphopolypeptides. On the other hand, phosphorylation of the 45, 86 and 91 kDa phosphopolypeptides decreased. Heat inactivation of protein kinases (lane C) led to the disappearance of the phosphorylated bands while addition of CK II after protein kinase inactivation (lane D) led to the appearance of the 24, 25, 30, 32, 54, 56, 74, 86 and 120 kDa phosphopolypeptides. So, these results shows that the 30, 54, 86 and 120 kDa proteins whose phosphorylation is stimulated by spermine are also substrates for CK II.
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Tissue specificity
Since the antenna contains nervous tissue, cuticle, muscle and lymph, we attempted to identify phosphoproteins specific to the antenna by comparison with other types of tissue from the same animal. Accordingly, phosphoproteins from the leg, fat body, cerci and brain were separated after in vitro phosphorylation in the presence of spermine. As shown in Figure 3, the 30 and 48 kDa phosphoproteins were detected only in antennae. Although not always strongly phosphorylated, all other phosphoproteins were present in one or more other tissues. Since the same amount (20 µg) of protein was used in all experiments, it appears that protein kinase activity and/or protein substrates were high in antennae as compared with other organs. This difference was especially great in comparison with the leg, cerci and fat body but not with the brain, especially with regard to the 37 and 51 kDa phosphoproteins.
Effect of pheromonal blend
Figure 4 shows the results of experiments using isolated male antennae exposed to either filter paper impregnated with the female pheromonal blend or clean filter paper. In control experiments using no modulator, phosphorylation of the 58, 51, 48 and 45 kDa polypeptides increased after exposure to the pheromonal blend whereas phosphorylation of the 120 kDa polypeptide decreased. When phosphorylation was performed in the presence of spermine, pre-exposure to the pheromonal blend strongly enhanced phosphorylation of the 54, 48 and 33 kDa polypeptides. Conversely, phosphorylation of the specific antennal 30 kDa polypeptide as well as of the 23, 27-28, 37 and 120 kDa polypeptides decreased.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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The EAG data described in this report demonstrate enhancement of the sensitivity of insect antenna to female pheromonal blend after treatment with
-DFMO. According to the literature [for a review, see
(Cohen, 1998)], -DFMO is
a specific inhibitor of ODC, i.e. the rate-limiting enzyme for polyamine
synthesis in mammals. In insects, our previous studies confirmed that
administration of -DFMO in drinking water for a 5 day period resulted
in a decrease in polyamine levels in fat body and neural tissue
(Cayre et al., 1996).
These findings strongly suggest that polyamines play a regulatory role in
olfactory detection.
The mechanism by which a decrease in polyamine level leads to increase in
olfactory sensitivity is still not clear. A possible explanation could involve
action of polyamines on ion channels. Indeed, endogenous polyamines, in
particular spermine, have been found to block or modulate several types of ion
channels (Lopatin et al.,
1995; Lee et al.,
1999; Lu and Ding,
1999). In the olfactory system, Lynch showed that polyamines
induced strong inward rectification in the CNG channel
(Lynch, 1999). To our
knowledge all data have been obtained on mammals and nothing is known of the
action of polyamines on insect CNG channels.
Another mechanism that could be involved to some extent in the polyamine
effect is protein phosphorylation. It has been demonstrated that CNG channels
are regulated not only through the direct action of cyclic nucleotides, but
also via phosphorylation catalysed by PKC
(Müller et al.,
1998). Data presented in this study demonstrate that polyamines
can modulate protein phosphorylation in antennae. However, the affected
proteins have not been fully characterized and none of them exhibit a subunit
with a molecular weight corresponding to any of the known CNG channels. Thus
it can be assumed either that polyamines do not modulate the phosphorylation
of these channels or that the channels affected by polyamines have not yet
been characterized. The second possibility may open an avenue for further
research, especially in insects.
Schleicher et al. showed that stimulation of Heliotis
virescens antennal preparations using a pheromonal blend led to the
stimulation of the phosphorylation of two proteins at 55 and 70 kDa
(Schleicher et al.,
1994). This stimulation was suppressed by inhibitors of PKC.
Although they were not characterized by those authors, these proteins might be
the same as the 54 and 70 kDa shown to be substrates for PKC and to be
affected by a pheromonal blend in antennal preparations of P.
americana (Renucci et al.,
1996). The present work demonstrates that the 54 kDa protein is
also a substrate for CK II. This finding leads us to speculate that the 54
protein may be the ß subunit of the tubulin. In this regard it is
noteworthy that the 53.5/54 kDa protein was clearly identified as the tubulin
ß subunit in previous experiments using a specific antibody in the brain
of the cricket Acheta domesticus and bee Apis mellifera
(Degrelle, 1996). Since the
importance of multisite phosphorylation of key proteins is well documented
(Cohen, 2000), our finding that
spermine inhibits and stimulates phosphorylation of the 48 and 86 kDa
proteins, respectively, is of interest because previous findings have shown
that the 48 kDa protein is stimulated by cyclic nucleotides while the 86 kDa
protein is stimulated by PKC activators
(Renucci et al.,
1996).
Although direct involvement of polyamines in regulation of cell functions
has been well documented (Cohen,
1998), the role of polyamines as intermediates in the transduction
of hormonal and other regulatory signals remains highly conjectural. Cayre
et al. implicated polyamines in transduction of the juvenile hormone
message in insect neural tissue (Cayre
et al., 1997). Regulation of protein phosphorylation by
polyamines has been observed in mammals
(Cochet and Chambaz, 1983) and
insects (Combest and Gilbert,
1992). The underlying mechanism involves stimulation of CK II in a
process implicating binding of polyamine to a specific site on the regulatory
subunit (Leroy et al.,
1997). We have demonstrated a regulation of CK II activity
according to the hormonal status in the insect nervous system
(Degrelle et al.,
1997).
Although we did not actually demonstrate an effect of polyamines on the phosphorylation of potential subunits of CNG channels, our data suggests a possible regulatory role via proteins with specialized functions. Phosphorylation of the 30 and 48 kDa proteins which are specific to antennae is affected by polyamines and changes after the detection of the pheromonal blend. Our results also suggest that modification of protein status via CK II is probably one of the mechanisms involved in this regulation. To definitively prove the presented hypothesis, the involved proteins must be identified, localized to the olfactory receptor neurons and compared to receptor potentials and nerve impulse responses recorded from single pheromone-sensitive neurons.
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Acknowledgments |
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We are grateful to Andrew Corsini for his help in the preparation of the English text and to Laure Du Cos de Saint Barthelemy for her help in the video surveillance experiments.
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References |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Bernstein, H.-G. and Müller, M. (1999) The cellular localization of the L-ornithine decarboxylase/polyamine system in normal and diseased central nervous systems. Prog. Neurobiol, 57,485 -505.[Web of Science][Medline]
Blair, D.G.R. (1985) Activation of mammalian RNA polymerises by polyamines. Int. J. Biochem.,17 , 23-30.[Web of Science][Medline]
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem.,72 , 248-254.[Web of Science][Medline]
Cayre, M., Strambi, C., Charpin, P., Augier, R., Renucci, M. and Strambi, A. (1996) Inhibition of polyamine biosynthesis alters ovi-position behavior in female crickets.Behav. Neurosci. , 110,1117 -1125.[Web of Science][Medline]
Cayre, M., Strambi, C., Charpin, P., Augier, R. and
Strambi, A. (1997) Specific requirement of putrescine
for the mitogenic action of juvenile hormone on adult insect neuroblasts.Proc. Natl. Acad. Sci. USA
, 94,8238
-8242.
Cochet, C. and Chambaz, E.M. (1983) Polyamine-mediated protein phosphorylations: a possible target for intracellular polyamine action. Mol. Cell. Endocrinol.,30 , 247-266.[Web of Science][Medline]
Cohen, S.S. (1998) A Guide to the Polyamines. Oxford University Press, Oxford.
Cohen, P. (2000) The regulation of protein function by multisite phosphorylation—a 25 year update.Trends Biochem. Sci. , 25,596 -601.[Web of Science][Medline]
Collingridge, G.L. and Lester, R.A. (1989) Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacol. Rev.,40 , 143-210.
Combest, W.L. and Gilbert, L.I. (1992) Polyamines modulate multiple protein phosphorylation pathways in the insect prothoracic gland. Mol. Cell. Endocrinol.,83 , 11-19.[Web of Science][Medline]
Degrelle, F. (1996) Etude des protéines phosphorylables du tissu nerveux d'Acheta domesticus et d'Apis mellifera. PhD, Université d'Aix-Marseille III, France.
Degrelle, F., Tirard, A., Strambi, C., Renucci, M. and Strambi, A. (1994) Protein phosphorylation in the neural tissue of an adult cricket (Acheta domesticus): endogenous substrates and their protein kinases. J. Insect Physiol.,40 , 293-302.
Degrelle, F., Renucci, M., Charpin, P. and Tirard, A. (1997) Casein kinase II activity in the brain of an insect, Acheta domesticus: characterization and hormonal regulation. Arch. Insect Biochem. Physiol.,34 , 69-81.[Web of Science][Medline]
Feuerstein, B.G., Williams, L.D., Basu, H.S. and Marton, L.J. (1991) Implications and concepts of polyamine—nucleic acid interactions. J. Cell. Biochem., 46,37 -47.[Web of Science][Medline]
Filhol, O., Cochet, C., Delagoutte, T. and Chambaz, E.M. (1991) Polyamine binding activity of casein kinase II. Biochem. Biophys. Res. Commun.,180 , 945-952.[Web of Science][Medline]
Guo, D.L. and Lu, Z. (2000a)
Mechanism of IRK1 channel block by intracellular polyamines.J. Gen. Physiol.
, 115,799
-813.
Guo, D.L. and Lu, Z. (2000b)
Mechanism of cGMP-gated channel block by intracellular polyamines.J. Gen. Physiol.
, 115,783
-797.
Hawkins, W.A. and Rust, M.K. (1977) Factors influencing male sexual response in the American cockroach Periplaneta americana. J. Chem. Ecol.,3 , 85-99.
Igarashi, K. and Kashiwagi, K. (2000) Polyamines: mysterious modulators of cellular functions.Biochem. Biophys. Res. Commun. , 271,559 -564.[Web of Science][Medline]
Kogan, P.H. and Hagedorn, H.H. (2000) Polyamines, and effects from reducing their synthesis during egg development in the yellow fever mosquito, Aedes aegypti. J. Insect Physiol., 46,1079 -1095.[Web of Science][Medline]
Laemmli, U.K. (1970) Cleavage of structure proteins during the assembly of the head of the bacteriophage T4.Nature , 227,680 -685.[Medline]
Lee, J.K., Scott, A.J. and Weiss, J.N.
(1999) Novel gating mechanism of polyamine block in the
strong inward rectifier K channel Kir2.1. J. Gen.
Physiol., 113,555
-563.
Leroy, D., Schmid, N., Behr J.-P., Filhol, O., Pares, S., Garin,
J., Bourgarit J.-J., Chambaz, E.M. and Cochet, C.
(1995) Direct identification of a polyamine binding domain on
the regulatory subunit of the protein kinase casein kinase II by photoaffinity
labeling. J. Biol. Chem., 270,17400
-17406.
Leroy, D., Heriché, J.K., Filhol, O., Chambaz, E.M.
and Cochet, C. (1997) Binding of polyamines to an
autonomous domain of the regulatory subunit of protein kinase CKII induces a
conformational change in the holoenzyme. J. Biol. Chem.,272
, 20820-20827.
Lopatin, A.N., Makhina, E.N. and Nichols, C.G.
(1995) The mechanism of inward rectification of potassium
channels: `long-pore plugging' by cytoplasmic polyamines. J. Gen.
Physiol., 106,923
-955.
Lu, Z. and Ding, L. (1999) Blockade
of a retinal cGMP-gated channel by polyamines. J. Gen.
Physiol., 113,35
-43.
Lynch, J.W. (1999) Rectification of the olfactory cyclic nucleotide-gated channel by intracellular polyamines.J. Membr. Biol. , 170,213 -227.[Web of Science][Medline]
Maida, R., Redkozubov, A. and Ziegelberger, G. (2000) Identification of PLCß and PKC in pheromone receptor neurons of Antheraea polyphemus.Neuroreport , 11,1773 -1776.[Web of Science][Medline]
Menini, A. (1999) Calcium signalling and regulation in olfactory neurons. Curr. Opin. Neurobiol.,9 , 419-26.[Web of Science][Medline]
Monti, M.G., Marveti, G., Ghiaroni, S., Piccinini, G., Pernecco, L. and Moruzzi, M.S. (1994) Spermine protects protein kinase C from phospholipid-induced inactivation.Experientia , 50,953 -957.[Web of Science][Medline]
Morgan, D.M.L. (1990) Polyamines and cellular regulation: perspectives. Biochem. Soc. Trans.,18 , 1080-1083.[Web of Science][Medline]
Morgan, D.M.L. and Wallace, H.M. (1994) Polyamines in clinical and basic sciences: introductory remarks.Biochem. Soc. Trans. , 22,845 -846.[Web of Science][Medline]
Müller, F., Bönigk, W., Sesti, F. and Frings,
S. (1998) Phosphorylation of mammalian olfactory cyclic
nucleotide-gated channels increases ligand sensitivity. J.
Neurosci., 18,164
-173.
Renucci, M., Tirard, A., Sreng, L., Khlat, J. and Clément J-L (1996) Phosphorylation of cockroach antennal polypeptides: effects of second messengers and pheromonal blend.Experientia , 52,762 -768.
Romano, C. and Williams, K. (1994) Modulation of NMDA receptors by polyamines. In Carter, C.J. (ed.),The Neuropharmacology of Polyamines . Academic Press, London, pp. 81-106.
Saas, H. (1983) Production, release and effectiveness of two female sex pheromone components of Periplaneta americana. J. Comp. Physiol., 152,309 -317.
Schleicher, S., Boekhoff, I., Konietzko, U. and Breer, H. (1994) Pheromone induced phosphorylation of antennal proteins from insects. J. Comp. Physiol. B,164 , 76-80.
Seiler, N. (1994) Formation, catabolism and properties of the natural polyamines. In Carter, C. (ed.), The Neuropharmacology of Polyamines. Academic Press, London, pp.1 -36.
Sjöholm, A. and Honkanen, R.E. (2000) Polyamines regulate serine/threonine phosphatases in insulin-secreting cells. Pancreas,20 , 32-37.[Web of Science][Medline]
Stengl, M., Ziegelberger, G., Boekhoff, I. and Krieger, J. (1999) Perireceptor events and transduction mechanisms in insect olfaction. In Hanson, B.S. (ed.) Insect Olfaction. Springer, Berlin, pp.49 -66.
van Leeuwenhoek, A. (1678) Observationes D. Anthonii Leeuwenhoek, de natis e semine genitali animalculis.Philos Trans R Soc , 12,1040 -1043.
Williams, K. (1997) Modulation and block of ion channels: a new biology of polyamines. Cell. Signal.,9 , 1-13.[Web of Science][Medline]
Accepted January 28, 2002
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