Screening of second messengers involved in photocyte bioluminescence control of three ophiuroid species (Ophiuroidea: Echinodermata)
Laboratory of Marine Biology, Catholic University of Louvain, Place Croix du Sud, 3, B-1348 Louvain-la-Neuve, Belgium
* Author for correspondence (e-mail: vanderlinden{at}bani.ucl.ac.be)
Accepted 28 May 2003
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: invertebrate, echinoderm, ophiuroid, Amphiura filiformis, Ophiopsila aranea, Ophiopsila californica, bioluminescence, second messenger, cAMP, nervous system, photocyte
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
While an increasing amount of information exists on the extrinsic control
mechanisms of luminescence in ophiuroids, only few data are available
concerning the intrinsic control mechanisms leading to photocyte photogenesis.
The behaviour of all cells from one instant to another is governed by
signalling systems that translate external information into a limited
repertoire of internal signals, the second messengers
(Cobb and Laverack, 1967).
There are four main second messenger pathways discovered so far: cyclic AMP
(cAMP), cyclic GMP (cGMP), inositol triphosphate/diacylglycerol
(IP3/DAG) and calcium (Ca2+). Most studies concerning
second messengers have been performed on vertebrates and they are found in all
cell types studied so far. In echinoderms, it has been shown that
Ca2+ (Mallefet et al.,
1994
,
1998
), cyclic nucleotides and
IP3/DAG (De Bremaeker et al.,
2000b
) are involved in the luminescence control of the ophiuroid
A. squamata. Dewael and Mallefet
(2002b
) have also documented
the Ca2+ requirement for light emission in three other ophiuroid
species.
The aim of this work is thus to identify second messengers triggering
photogenesis in three ophiuroid species: A. filiformis, O. aranea and
O. californica. This was achieved by testing agonists and antagonists
of three second messenger pathways (cGMP, cAMP and IP3/DAG) on
light production. While most previous studies on bioluminescence control in
ophiuroids have been carried out on whole arms or arm segments (De Bremaeker
et al., 1996,
1999a
,b
;
Dewael and Mallefet,
2002a
,b
),
we analysed the luminous cells (photocytes) directly.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Experiments on dissociated photocytes
The method used is based on that described by De Bremaeker et al.
(2000b). First, the ophiuroids
were anaesthetized by immersion in 3.5% MgCl2 in artificial
seawater (ASW: 400.4 mmol l-1 NaCl, 9.9 mmol l-1
CaCl2, 9.6 mmol l-1 KCl, 52.3 mmol l-1
MgCl2, 27.7 mmol l-1 Na2SO4, 20
mmol l-1 Tris, pH 8.3). Next, since the arms are the only
luminescent body parts of the studied ophiuroid species, they were isolated
from the disc and chopped into tiny pieces before enzymatic digestion and
differential centrifugation. The enriched luminous-cell fraction was then
divided into aliquot parts (200 µl), and light emission was measured with a
FB12 Berthold luminometer (Pforzheim, Germany) linked to a personal computer.
Injection of drugs was controlled to avoid mechanical stimulation of
luminescence during the assays. Injections of corresponding volumes of ASW
served as controls before the assays. These controls indicated that
luminescence due to mechanical excitability was absent or negligible.
Stimulations
A stock solution of 400 mmol l-1 KCl was prepared in ASW without
NaCl to keep the same osmolarity as normal ASW. Stimulations were performed by
injection of potassium chloride (KCl) to a final dilution of 200 mmol
l-1; one experiment was carried out using 50 mmol l-1
KCl (see Results). For each experimental protocol, one aliquot part was
stimulated in normal ASW, as a control, while the other preparations were
first immersed in ASW containing the tested drug for 10 min before stimulation
with KCl.
Drugs
The following drugs were used in this study: bisindolylmaleimide (GF
109203X; Sigma, Bornem, Belgium);
N6,2'-o-dibutyryladenosine 3',5'-cyclic
monophosphate (db-cAMP; Sigma);
N2,2'-o-dibutyrylguanosine 3',5'-cyclic
monophosphate (db-cGMP; Sigma); forskolin (FSK; ICN, Irvine, CA, USA);
3-isobutyl-1-methyl-xanthine (IBMX; Sigma);
1-[6-{[17ß-3-methoxyestra-1,3,5(10)-trien-17-yl]amino}hexyl]-1H-pyr-role-2,5-dione
(U-73122; Sigma);
1-[6-{[17ß-3-methoxyestra-1,3,5(10)-trien-17-yl]amino}hexyl]-2,5-pyrrolidine-dione
(U-73343; ICN); pentoxifylline (Sigma);
cis-N-(2-phenylcyclopentyl)-azacyclotridec-1-en-2-amine
monohydrochloride (MDL-12,330A; Sigma); sodium nitroprusside (Na nitro;
Sigma); 9-tetrahydro-2-furanyl-9H-purin-6-amine (SQ22,536; Sigma).
Solutions of db-cAMP, db-cGMP, IBMX, pentoxifylline, Na nitro and SQ22,536
were dissolved in ASW; solutions of FSK, GF 109203X, MDL-12,330A, U-73122 and
U-73343 were dissolved in dimethylsulphoxide (DMSO) before dilution in ASW,
with a maximum of 1% DMSO at final concentration. This final DMSO dilution
alone had no effect. The concentrations used for the drugs were chosen from
previous studies on echinoderm tissues (Soliman,
1984a,b
;
Gustafson, 1990
;
Karaseva and Khotimchenko,
1995
; De Bremaeker et al.,
2000b
). Fresh solutions were prepared daily.
Different parameters were used in order to characterise the photogenesis: (1) Lmax, the maximum level of light emission expressed as a percentage of the control; (2) Ltot, total amount of light emitted expressed as a percentage of the control; (3) LT, latency time, the time elapsed between stimulation and the beginning of the light emission; (4) TLmax, the time between onset of light production and maximum light emission.
Statistical analyses [analysis of variance (ANOVA), Dunnet and Tukey tests]
were performed using SAS/STAT® software
(SAS Institute Inc.,
1990).
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
Effects of db-cGMP and guanylyl cyclase activator
The treatment of dissociated photocytes from A. filiformis, O.
aranea and O. californica with 10-4 mol
l-1 dibutyrylcGMP (db-cGMP), a membrane-permeable analogue of
guanosine 3',5'-cyclic monophosphate (cGMP) and 10-3
mol l-1 sodium nitroprusside (Na nitro), an activator of guanylyl
cyclase, did not induce luminescence without KCl application. After 10 min
treatment with db-cGMP or Na nitro, 200 mmol l-1 KCl was applied.
Controls were not treated with the drugs before KCl application. In both
Ophiopsila species, no significant differences in the parameters of
light emission were observed after KCl injection between the treated and the
control photocytes (Fig. 1). On
the other hand, in A. filiformis, 10-4 mol l-1
db-cGMP did inhibit light emission; only 5.89±1.68% of maximal light
intensity (Lmax) and 12.19±3.3% of the total amount
of emitted light (Ltot) remained. Na nitro
(10-3 mol l-1) treatment was ineffective in all three
species. Kinetic parameters (LT and TLmax) were
not modified in any cases.
|
Effects of db-cAMP, adenylyl cyclase activator and inhibitors
The treatment of dissociated photocytes from A. filiformis, O.
aranea and O. californica with 10-4 mol
l-1 dibutyryl-cAMP (db-cAMP), a membrane-permeable analogue of
adenosine 3',5'-cyclic monophosphate (cAMP), 10-4 mol
l-1 forskolin (FSK), an activator of adenylyl cyclase, as well as
10-5 mol l-1 MDL-12,330A and 10-5 mol
l-1 SQ22,536, two inhibitors of adenylyl cyclase, did not induce
luminescence prior to KCl application. Neither db-cAMP nor FSK showed a
significant effect on 200 mmol l-1 KCl-induced luminescence
(Fig. 2). Moreover,
10-4 mol l-1 FSK did not have any significant effect on
50 mmol l-1 KCl-induced luminescence (Lmax) in
all three species (Fig. 2). We
tested FSK on 50 mmol l-1 induced luminescence to highlight a
potential increase of light production since 50 mmol l-1 KCl does
not trigger a maximal light response (50% of 200 mmol l-1 KCl
light response). Only in O. californica did 10-4 mol
l-1 FSK decrease kinetic parameters of light production
(LT and TLmax;
Table 2).
|
|
On the other hand, MDL-12,330A and SQ22,536 strongly reduced 200 mmol l-1 KCl-induced luminescence in A. filiformis and O. aranea (Lmax; P<0.01, N=10; Fig. 2). Total amount of emitted light was also significantly decreased in both species (Table 3), and TLmax was increased in O. aranea for both drugs (Table 2). In O. californica, MDL-12,330A strongly decreased light parameters (Lmax, Fig. 2; Ltot, Table 3) and also increased TLmax (Table 2). SQ22,536 did not significantly reduce Lmax (Fig. 2) and Ltot (Table 3) but increased TLmax (Table 2) in this species.
|
Effects of phosphodiesterase inhibitors
In order to complete the study of a putative involvement of cyclic
nucleotides on luminescence control in A. filiformis, O. aranea and
O. californica, we tested two phosphodiesterase inhibitors,
10-4 mol l-1 IBMX and 10-4 mol l-1
pentoxifylline, which increase the intracellular level of both cAMP and cGMP.
None of these drugs induced luminescence without KCl application.
Fig. 3 shows that there is no
effect of pentoxifylline on KCl-induced luminescence, while 10-4
mol l-1 IBMX largely reduced Lmax
(55.2±24.3% of control) solely in A. filiformis. Total amount
of light was also decreased (Ltot=19.6±8.5% of
control) in this species. Nevertheless, higher (5x10-4 mol
l-1) and lower (10-5 mol l-1) IBMX
concentrations did not affect the KCl-induced light emission in comparison
with the 200 mmol l-1 KCl control (not shown). Kinetic parameters
were not modified by these treatments in any of these species.
|
Effects of phospholipase C and protein kinase C inhibitors
In order to investigate the putative involvement of phosphoinositides in
the triggering of photogenesis, we tested U-73122, a phospholipase C
inhibitor. It inhibits the hydrolysis of phosphatidylinositol 4,5-bisphosphate
(PIP2) into diacylglycerol (DAG) and inositol 1,4,5-trisphosphate
(IP3) and therefore leads to a decrease in calcium mobilization
from intracellular stores (Smallridge et
al., 1992; Yule and Williams,
1992
). The drug did not induce luminescence by itself but it
strongly inhibited KCl-induced light emission in all three species at a
concentration of 5x10-6 mol l-1
(Lmax, Fig.
4; Ltot,
Table 3). At
5x10-7 mol l-1, U-73122 still inhibited light
emission in A. filiformis and O. aranea
(Lmax, Fig.
4; Ltot,
Table 3) but not in O.
californica. Kinetic parameters were not modified in any conditions.
|
The inactive U-73122 analogue, U-73343, did not induce photogenesis by itself at a concentration of 5x10-6 mol l-1 but inhibited KCl-induced luminescence with the same efficiency as U-73122 in all three species (Fig. 4; Table 3). Kinetic parameters were not modified.
We also tested 5x10-7 mol l-1 GF 109203X, a protein kinase C inhibitor, in order to emphasise the putative activation of protein kinase C by DAG. Fig. 4 shows no effect of this drug on the KCl-induced luminescence in any of the species.
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
In the present study, we used KCl (200 mmol l-1) to trigger
photogenesis since the neurotransmitters involved in the luminous control of
both Ophiopsila species are still unknown. In A. filiformis,
even if ACh seems to be the main transmitter in luminescence control
(Dewael and Mallefet, 2002a),
this drug has no effect on dissociated photocytes. This lack of response could
be due to the dissociation process: the use of protease, a powerful enzyme
that dissociates cells, may alter the cholinergic receptors on the photocyte
membrane. Tests with papain, a milder enzyme
(Gillis and Anctil, 2001
; J.
Mallefet, personal communication), failed to improve the results, suggesting
that the dissociation process is not responsible for the lack of response. The
absence of an ACh-induced response might reflect the absence of cholinergic
receptors on the photocyte membrane. ACh receptors could be present on another
cell membrane, closely associated to the photocytes. This has been observed by
Dunlap et al. (1987
), who
showed that luminescence in the hydrozoan coelenterate Obelia
geniculata was mediated by support cells through gap junctions. However,
the presence of gap junctions has neither been demonstrated in ophiuroids (Y.
Dewael, D. Sonny and J. Mallefet, unpublished) nor, for that matter, in any
adult echinoderm species (Cobb,
1995
).
Cyclic nucleotides
We used db-cGMP, the membrane-permeable cGMP analogue (Soliman,
1984a,b
;
Gustafson, 1990
), and Na
nitro, the guanylyl cyclase activator
(Karaseva and Khotimchenko,
1995
), to test the effect of an increase in intracellular cGMP on
photogenesis. 10-4 mol l-1 db-cGMP had no effect on the
KCl-induced luminescence of dissociated photocytes from O. aranea and
O. californica. By contrast, db-cGMP decreased the luminescence in
A. filiformis. Although the effect is important (less than 6% of the
control luminescence remains), the mechanism of an increase in intracellular
cGMP remains unclear. Indeed, Na nitro, the activator of guanylyl cyclase,
which is supposed to have the same final effect, i.e. an increase in
intracellular cGMP level, did not affect light emission in any of the species.
These contradicting results could come from the fact that guanylyl cyclase
activation is not mediated by NO in ophiuroids, whereas Na nitro acts on NO
production, which then stimulates guanylyl cyclase activation. Consequently,
we suggest that the cGMP pathway is not involved in the luminescence of either
Ophiopsila species but could be involved in an inhibitory
luminescence modulation in A. filiformis. cGMP acting as a negative
second messenger has already been observed in echinoderms: it blocks the
reinitiation of meiosis in the oocytes of the holothurian Stichopus
japonicus (Karaseva and Khotimchenko,
1995
), it reduces the Ca2+ influx and counteracts the
stimulatory action of Ca2+ in the muscular activity of larvae of
the sea urchin Psammechinus miliaris
(Gustafson, 1990
). On the
other hand, the cGMP pathway is not involved in the regulation of luminescence
in the ophiuroid A. squamata (De
Bremaeker et al., 2000b
).
The cAMP analogue db-cAMP (Soliman,
1984a,b
;
Gustafson, 1990
) and FSK, the
adenylyl cyclase activator (Karaseva and
Khotimchenko, 1995
), had no effect on 200 mmol l-1
KCl-induced luminescence of dissociated photocytes from O. aranea, O.
californica and A. filiformis. It is therefore assumed that an
increase of both external and intracellular cAMP concentration in photocytes
does not affect 200 mmol l-1 KCl-induced luminescence. On the other
hand, a decrease of cAMP concentration, produced by the adenylyl cyclase
inhibitors MDL-12,330A (Lippe and
Ardizzone, 1991
) and SQ22,536
(Fabbri et al., 1991
;
Lippe and Ardizzone, 1991
;
Goldsmith and Abrams, 1992
;
Shi and Bunney, 1992
),
strongly reduced Lmax and Ltot in
A. filiformis and O. aranea. It also increased
TLmax in both Ophiopsila species.
These contradicting results may be explained by the nature of stimulation.
Since KCl already triggers maximal intensity of light by photocyte
depolarisation (Mallefet and Dubuisson,
1995; De Bremaeker et al.,
2000b
; Dewael and Mallefet,
2002a
), it is not very likely to observe a potentiation of this
maximal light emission. This is the reason why we tested the adenylyl cyclase
activator FSK on non-maximal light emission triggered by 50 mmol
l-1 KCl. This latter treatment did not significantly potentiate
light production in all three species but decreased kinetic parameters of
light production (LT and TLmax) in O.
californica. This may result from the fact that cAMP is not the only
pathway controlling luminescence, and increasing cAMP on its own does not
subsequently increase light emission. Nevertheless, the effect of FSK on
kinetic parameters in O. californica is important since it increases
the rate of photocyte light response (shown by a decrease of LT and
TLmax).
Given the results, we can suggest that the cAMP pathway is partly involved
in the luminescence control of all three ophiuroid species. Similar results
were observed in the ophiuroid A. squamata, where cAMP was involved
in ACh-induced luminescence (De Bremaeker
et al., 2000b). The second messenger cAMP is formed by the
hydrolysis of ATP by adenylyl cyclase. When a neurotransmitter fixes G
protein-coupled receptors, the heterotrimeric G protein binds to GTP and
dissociates into G
-GTP and Gß
. The
former product can stimulate adenylyl cyclase, leading to an increase of
intracellular cAMP concentration (Hille,
2001
). cAMP can activate protein kinase A, which is involved in
the regulation of receptors and structural proteins and the opening and
closing of ion channels. It will, among other effects, increase
Ca2+ influx (Kennedy,
1994
). Ca2+ and cAMP pathways may interact at several
levels since cytosolic calcium can affect the cAMP cascade by binding to
calmodulin. The calcium-calmodulin complex alters the activity of adenylyl
cyclase and phosphodiesterase enzymes
(Kebabian, 1992
).
A previous study has shown that calcium movements are required in the
luminescence of the three studied ophiuroid species
(Dewael and Mallefet, 2002b).
In the absence of extracellular calcium, photogenesis is strongly inhibited;
pharmacological experiments indicate that calcium channels involved in the
luminescence control appear to be of the voltage-dependent L-type in A.
filiformis and O. californica but not in O. aranea.
Eventually, the intracellular increase of Ca2+ concentration would
lead to the triggering of the light reaction, through a mechanism not yet
understood.
The phosphodiesterase inhibitors IBMX and pentoxifylline did not modify the
KCl-induced luminescence in O. aranea and O. californica. In
A. filiformis, only 10-4 mol l-1 IBMX decreased
light emission; higher and lower concentrations had no effect. Knowing that
IBMX is also an antagonist of adenosine receptors, the effect could be due to
the blockade of these receptors. Although adenosine is not a transmitter for
luminescence (Dewael and Mallefet,
2002a), one cannot exclude that IBMX inhibition might be due to
blockade of adenosine neuromodulation of photogenesis. This neuromodulatory
effect has been described in A. squamata, where adenosine potentiates
ACh-induced luminescence (De Bremaeker et
al., 2000a
).
Phospholipase C and protein kinase C inhibitors
Treatment with U-73122, a phospholipase C inhibitor
(Yule and Williams, 1992),
strongly reduced KCl-induced luminescence in the three species at a
concentration of 5x10-6 mol l-1. At a lower
concentration (5x10-7 mol l-1), it still inhibited
light emission in A. filiformis and O. aranea but not in
O. californica. Since U-73122 has been reported to have some
unspecific effects (Alter et al.,
1994
), we used its inactive analogue U-73343
(5x10-6 mol l-1;
Bleasdale et al., 1990
;
Smith et al., 1990
) as a
negative control. This drug did not induce photogenesis by itself but
inhibited KCl-induced luminescence with the same efficiency as U-73122. It
supports the evidence that the effects of U-73122 are unspecific. Moreover,
quantitative assays of labelled IP3 have shown the absence of
IP3 production when photocytes are stimulated (results not shown),
suggesting that bioluminescence control is not mediated by IP3
production. Conversely, IP3 involvement in luminescence control has
previously been shown in A. squamata
(De Bremaeker et al., 2000b
),
where it mediated ATP- and ACh-induced luminescence. These results highlight
that luminous control mechanisms differ between ophiuroid species.
We tested the putative involvement of DAG in photogenesis control using GF
109203X, a protein kinase C inhibitor
(Toullec et al., 1991;
Martiny-Baron et al., 1993
).
This drug did not affect light emission, suggesting that DAG-activated protein
kinase C is not used in photogenesis. Consequently, we suggest that the
IP3/DAG pathway is not involved in the luminescence control of all
three ophiuroid species.
In conclusion, this study shows that IP3 and DAG are not
involved in the luminescence control of Amphiura filiformis, Ophiopsila
aranea and Ophiopsila californica. cGMP could be involved in an
inhibitory mechanism in A. filiformis. We suggest that the production
of cAMP in photocytes of all three ophiuroid species is a step in the
transduction signal leading to photogenesis. These rises in cAMP level and
intracellular calcium concentration are therefore likely to be crucial factors
responsible for light emission. The final steps of intrinsic luminescence
control and the nature of luminescent systems remain to be discovered. We have
presented evidence that luminescence control in ophiuroids is species-specific
since the second messengers involved in bioluminescence control vary between
species (A. squamata, A. filiformis, O. aranea and O.
californica). This diversity had been observed at different levels
previously: in extrinsic control mechanisms
(Dewael and Mallefet, 2002a)
and in calcium channels (Dewael and
Mallefet, 2002b
). It is also noteworthy that A.
filiformis presents a higher intra-specific variability in luminous
capabilities than O. aranea and O. californica
(Dupont et al., 2001
; Dewael
and Mallefet,
2002a
,b
;
present study).
Electrophysiological studies, using patch-clamp techniques and microspectrofluorimetric measurements of free intracellular calcium concentrations, are planned to bring some new clues to the signal transduction pathways of light emission in ophiuroids.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Alter, C. A., Amagasu, M., Shah, K., Jolly, Y. C., Major, C. and Wolf, B. A. (1994). U-73122 does not specifically inhibit phospholipase C in rat pancreatic islets and insulin-secreting ß-cell lines. Life Sci. 54,107 -112.[CrossRef]
Bleasdale, J. E., Thakur, N. R., Gremban, R. S., Bundy, G. L., Fitzpatrick, F. A., Smith, R. J. and Bunting, S. (1990). Selective inhibition of receptor-coupled phospholipase C-dependent processes in human platelets and polymorphonuclear neutrophils. J. Pharmacol. Exp. Ther. 255,756 -768.[Abstract]
Campbell, A. K. (1989). Living light: biochemistry, function and biomedical applications. Essays Biochem. 24,41 -80.[Medline]
Cobb, J. L. S. (1995). The nervous system of Echinodermata: recent results and new approaches. In The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach (ed. O. Breidbach and W. Kutsch), pp.407 -424. Basel: Birkhauser Verlag.
Cobb, J. L. S. and Laverack, M. S. (1967). Neuromuscular system in echinoderms. Symp. Zool. Soc. Lond. 20,25 -51.
De Bremaeker, N., Baguet, F. and Mallefet, J. (1999a). Characterization of acetylcholine-induced luminescence in Amphipholis squamata (Echinodermata: Ophiuroidea). Belg. J. Zool. 129,353 -362.
De Bremaeker, N., Baguet, F., Thorndyke, M. C. and Mallefet,
J. (1999b). Modulatory effects of some amino acids and
neuropeptides on luminescence in the brittlestar Amphipholis
squamata. J. Exp. Biol.
202,1785
-1791.
De Bremaeker, N., Dewael, Y., Baguet, F. and Mallefet, J. (2000b). Involvement of cyclic nucleotides and IP3 in the regulation of luminescence in the brittlestar Amphipholis squamata (Echinodermata). Luminescence 15,159 -163.[CrossRef][Medline]
De Bremaeker, N., Mallefet, J. and Baguet, F. (1996). Luminescence control in the brittlestar Amphipholis squamata: effect of cholinergic drugs. Comp. Biochem Physiol. 115C,75 -82.
De Bremaeker, N., Mallefet, J. and Baguet, F.
(2000a). Effects of catecholamines and purines on the
luminescence of Amphipholis squamata (Echinodermata). J.
Exp. Biol. 203,2015
-2023.
Dewael, Y. and Mallefet, J. (2002a).
Luminescence in ophiuroids (Echinodermata) does not share a common nervous
control in all species. J. Exp. Biol.
205,799
-806.
Dewael, Y. and Mallefet, J. (2002b). Calcium involvement in the luminescence control of three ophiuroid species (Echinodermata). Comp. Biochem. Physiol. 131C,153 -160.
Dunlap, K., Takeda, K. and Brehm, P. H. (1987). Calcium triggered luminescence via gap junctions in Obelia photocytes. Nature 325,60 -62.[Medline]
Dupont, S., Mallefet, J. and Dewael, Y. (2001). Natural bioluminescence as a genetic marker for ophiuroid species. Belg. J. Zool. 131,89 -94.
Fabbri, E., Brighenti, L. and Ottolenghi, C. (1991). Inhibition of adenylyl cyclase of catfish and rat hepatocyte membranes by 9-(tetrahydro-2-furyl)adenine (SQ22536). J. Enzym. Inhib. 5,87 -98.[Medline]
Gillis, M.-A. and Anctil, M. (2001). Monoamine release by neurons of a primitive nervous system: an amperometric study. J. Neurochem. 76,1774 -1784.[CrossRef][Medline]
Goldsmith, B. A. and Abrams, T. W. (1992). cAMP modulates multiple K+ currents increasing spike duration and excitability in Aplysia sensory neurons. Proc. Natl. Acad. Sci. USA 89,11481 -11485.[Abstract]
Gustafson, T. (1990). Pharmacological control of muscular activity in the sea urchin larva. III. Role of cyclic nucleotides. Comp. Biochem. Physiol. C 95,133 -143.[Medline]
Hastings, J. W. (1983). Diversity, chemistry and evolution of bioluminescence. J. Mol. Evol. 19,309 -321.[Medline]
Herring, P. J. (1987). Systematic distribution of bioluminescence in living organisms. J. Biolum. Chemilum. 1,147 -163.
Hille, B. (2001). Ion Channels of Excitable Membranes. 3rd Edition. Chapter 7, pp.201 -236. Sunderland: Sinauer Associates.
Karaseva, E. M. and Khotimchenko, Y. S. (1995). Effects of compounds elevating cyclic nucleotide levels on dithiothreitol-induced oocyte maturation in the holothurian Stichopus japonicus. Comp. Biochem. Physiol. 111C,441 -444.[CrossRef]
Kebabian, J. W. (1992). The cyclic AMP cascade: a signal transduction system. Neurotransmissions 8, 1-8.
Kennedy, M. B. (1994). Seconds messagers et fonction neuronale In Introduction à la Neurobiologie Moléculaire (ed. Z. W. Hall), pp.207 -246. Paris: Médecine-Sciences Flammarion.
Lippe, C. and Ardizzone, C. (1991). Actions of vasopressin and isoprenaline on the ionic transport across the isolated frog skin in the presence and the absence of adenylyl cyclase inhibitors MDL 12330 and SQ22536. Comp. Biochem. Physiol. 99C,209 -211.
Mallefet, J. (1999). Physiology of bioluminescence in echinoderms. In Echinoderm Research 1998 (ed. M. D. Candia Carnevali and F. Bonasoro), pp.93 -102. Rotterdam: Balkema.
Mallefet, J., Ajuzie, C. C. and Baguet, F. (1994). Aspect of calcium dependence of light emission in the ophiuroid Amphipholis squamata (Echinodermata). In Echinoderms Through Time (ed. B. David, A. Guille, J.-P. Feral and M. Roux), pp. 455-460. Rotterdam: Balkema.
Mallefet, J., Chabot, B., De Bremaeker, N. and Baguet, F. (1998). Evidence for a calcium requirement in Amphipholis squamata (Ophiuroidea) luminescence. In Echinoderms (ed. R. Mooi and M. Telford), pp.387 -392. San Francisco, Rotterdam: Balkema.
Mallefet, J. and Dubuisson, M. (1995). Preliminary results of luminescence control in isolated arms of Ophiopsila aranea (Echinodermata). Belg. J. Zool. 125,167 -173.
Martiny-Baron, G., Kazanietz, M. G., Mischak, H., Blumberg, P.
M., Kochs, G., Hug, H., Marme, D. and Schächtele, C.
(1993). Selective inhibition of protein kinase C isozymes by the
indolocarbazole Gö 6976. J. Biol. Chem.
268,9194
-9197.
SAS Institute Inc. (1990). SAS/STAT User's Guide, Version 6, vol. 2. Fourth Edition. North Carolina: SAS Institute Inc.
Shi, W. X. and Bunney, B. S. (1992). Roles of intracellular cAMP and protein kinase A in the actions of dopamine and neurotensin on midbrain dopamine neurons. J. Neurosci. 12,2433 -2438.[Abstract]
Smallridge, R. C., Kiang, J. G., Gist, I. D., Fein, H. G. and Galloway, R. J. (1992). U-73122, an aminosteroid phospholipase C antagonist, noncompetitively inhibits thyrotropin-releasing hormone effects in GH3 rat pituitary cells. Endocrinology 131,1883 -1888.[Abstract]
Smith, R. J., Sam, L. M., Justen, J. M., Bundy, G. L., Bala, G. A. and Bleasdale, J. E. (1990). Receptor-coupled signal transduction in human polymorphonuclear neutrophils: effects of a novel inhibitor of phospholipase C-dependent processes on cell responsiveness. J. Pharmacol. Exp. Ther. 253,688 -697.[Abstract]
Soliman, S. (1984a). Pharmacological control of ciliary activity in the young sea urchin larva: chemical studies on the role of cyclic nucleotides. Comp. Biochem. Physiol. 78C,175 -181.[CrossRef]
Soliman, S. (1984b). Pharmacological control of ciliary activity in the young sea urchin larva. Studies on the role of Ca2+ and cyclic nucleotides. Comp. Biochem. Physiol. 78C,183 -191.[CrossRef]
Toullec, D., Pianetti, P., Coste, H., Bellevergue, P.,
Grand-Perret, T., Ajakane, M., Baudet, V., Boissin, P., Boursier, E. and
Loriolle, F. (1991). The bisindolylmaleimide GF 109203X is a
potent and selective inhibitor of protein kinase C. J. Biol.
Chem. 266,15771
-15781.
Yule, D. I. and Williams, J. A. (1992). U-73122
inhibits Ca++ oscillations in response to cholecystokinin and
carbachol but not JMV-180 in rat pancreatic acinar cells. J. Biol.
Chem. 267,13830
-13835.