Nitric oxide in control of luminescence from hatchetfish (Argyropelecus hemigymnus) photophores
1 Department of Zoophysiology, Göteborg University, Box 463, SE 405 30
Göteborg, Sweden
2 Laboratory of Marine Biology, Catholic University of Louvain, B-1348
Louvain-la-Neuve, Belgium
3 Department of Biology and Marine Ecology, Messina University, 98166
Messina, Italy
* Author for correspondence (e-mail: jenny.kronstrom{at}zool.gu.se)
Accepted 24 May 2005
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Summary |
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Key words: Argyropelecus hemigymnus, bioluminescence, teleost fish, nitric oxide, nitric oxide synthase
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Introduction |
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Nitric oxide (NO) is a freely diffusible unconventional neurotransmitter
and neuromodulator molecule that is increasingly found to play an important
role in several physiological systems, from invertebrates to mammals
(Jacklet, 1997). Since the
presence of an NO system has been described in several fish species (Schober
et al., 1993; Olsson and Holmgren,
1997
; Nilsson and
Söderström, 1997
;
Cox et al., 2001
), we
investigated the possible role of NO as a neurotransmitter and/or modulator of
the adrenergic control of bioluminescence, using isolated ventral photophores
of Argyropelecus hemigymnus.
The results suggest that NO is produced in the photophores and is involved in modulation of the adrenergic control of Argyropelecus luminescence. It is hypothesized that the very variable capacity of photophores to produce and maintain the luminescence evoked by adrenaline is correlated to a large variability in endogenous nitric oxide synthase (NOS) activity in the isolated photophores.
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Materials and methods |
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Immunohistochemistry
Photophores (Fig. 1)
obtained from 10 individuals were used for immunohistochemistry. The tissues
were fixed for 1620 h in Zamboni's fixative [15% picric acid, 2%
formaldehyde in phosphate buffered saline (PBS, 0.9% NaCl, pH 7.2)]. After
repeated washing in 80% ethanol, the tissue was dehydrated (95%, 99.5%
ethanol, 30 min each), treated with xylene (30 min) and rehydrated (99.5%,
95%, 80% and 50% ethanol, 30 min each) to PBS. The tissues were stored
overnight in PBS with 30% sucrose before embedding in OCT (Sakura, Zoeterwude,
The Netherlands) or Agarose (Sigma Chemical Company, St Louis, MO, USA) and
quick frozen in isopentane chilled with liquid nitrogen. Frozen samples that
were not cut immediately were stored at 40°C until use.
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A cryostat microtome (Zeiss Microm International GmbH, Walldorf, Germany) was used to cut 10 µm sections, which were captured on chrome alum gelatine-coated slides and left overnight to dry. The slides were stored at 20°C until use.
Fluorescence histochemistry
To prevent non-specific staining, sections were preincubated with normal
donkey serum (10%) for 3060 min. Primary antibodies
(Table 1) were applied and the
sections incubated for 48 h. They were rinsed (3x 5 min in PB with 2%
NaCl) and incubated for 60 min with the secondary antibody
(Table 1). All incubations were
in a humid chamber at room temperature (20°C).
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Rinsing was repeated as described above and the preparations were mounted in Vectashield mounting medium (Vector Laboratories, Burlingame, CA, USA) then examined using a Nikon eclipse E1000 microscope (Nikon, Tokyo, Japan) equipped with a Nikon DMX1200 digital camera. Captured images were processed in Adobe Photoshop.
Avidinbiotin histochemistry
The sections were preincubated with normal donkey serum as described above.
Control tests with an additional preincubation with H2O2
(0.3 or 3% for 3 to 15 min) before the normal donkey serum incubation
demonstrated no endogenous peroxidase activity. The primary and secondary
antibodies (Table 1) were
applied according to the description above. The sections were then incubated
with avidin-biotinylated peroxidase complex (ABC Elite PK 6100 standard,
Vector Laboratories) for 30 min and subsequently developed in Vector Nova red
substrate kit (SK 4800, Vector Laboratories) for 3 min. The sections were
mounted in 50% glycerol and 50% carbonate buffer (pH 8.5) and examined as
described above.
Controls performed to confirm the specificity of the secondary antibodies, by omission of the primary antibody, did not reveal non-specific staining with any of the secondary antibodies in the test (Fig. 2). Absorption tests where the primary antibody nNOS SC1025 was preincubated overnight with excess of blocking peptide [the antigen, NOS1 (K-20) P sc-1025P] resulted in considerable quenching of the immunoreaction produced with that antibody (Fig. 3).
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The preparations were transferred to a small Perspex chamber and inserted into a slot (10 mm length x 2 mm wide) cut in the chamber; the light emitting area of the photophores facing a thin wall of Perspex orientated towards the photo detector of a luminometer (Berthold FB12; Pforzheim, Germany). Using the Berthold Multiple Kinetics program, it was possible to record simultaneously the luminescence from six preparations. The light sensitivity was calibrated using a standard light source (Betalight, Saunders Technology, peaking at 470 nm) positioned in place of the tissue. The response was recorded on a laptop computer. The following parameters were used to characterize the luminescence: the time (min) elapsed from the beginning of light emission to the time of maximum light emission (TLmax), the intensity (in Mq s1) of maximum light emission (Lmax), and the time (min) to half-extinction of light emission (TL1/2).
Drugs and solutions
The following chemicals were used in this study: adrenaline (Federa,
Brussels, Belgium), dibutyryl-cGMP (Sigma), hydroxylamine hydrochloride (Acros
organics, Pittsburgh, PA, USA), pentoxifylline (Sigma),
(1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one (ODQ); Tocris Cookson Inc,
Ellisville, Missouri, USA), S-nitroso-N-acetylpenicillamine
(SNAP; Sigma), sodium nitroprusside (SNP; Sigma), L-thiocitrulline
(Acros organics). All chemicals were dissolved just before use and diluted as
required in a modified Hank's solution of the following composition (in mmol
l1): NaCl 188, KCl 7.4, CaCl2 2H2O
3.5, MgCl2 2H2O 2.4, saccharose 120, adjusted to pH 7.3
with Tris-HCl buffer. Saccharose was added to raise the osmolarity to that of
the blood serum of mesopelagic marine teleosts as measured by Griffith
(1981).
Design of the experiments
To compare the effects of drug treatments on adrenaline-induced
luminescence, six preparations (pairs of anterior and posterior halves of
three ventral organs) were inserted in the slot of six Perspex chambers
containing 500 µl Hank's solution and the zero level of light was
controlled. For each pair of ventral organ halves, one was used as a control
and maintained in saline, and the other was treated with a nitrergic drug,
starting 20 min before light induction. For light induction, both control and
treated photophores were stimulated with adrenaline at a final concentration
of 104 mol l1. In one set of experiments
with hydroxylamine, adrenaline stimulations were made first on both halves of
the ventral organ, and the nitrergic drug was added to one half when maximal
light production was reached. Anterior and posterior ventral organ halves
isolated from different fish were used alternatively as control and treated
preparations, in order to have the same number of control and treated
preparations in the different pairs. The complete experimental procedure was
performed at room temperature (18°C). Statistical analyses were performed
using Student's t-test, methods of correlation and linear regression;
each mean value is expressed with its standard error (mean ±
S.E.M.) and (N) equals the number of
preparations.
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Results |
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Antibodies raised against acetylated tubulin demonstrate the presence of nerve fibres in the filter area, as well as among the photocytes of Argyropelecus photophores (Fig. 4A,B). Nerve bundles of various diameters enter the photocyte chamber through the reflector layer at several locations and branch into thin fibre bundles or single fibres among the photocytes (Fig. 4B). In addition, fibres spread from a common point at the median narrowing of the photophore (where the reflector opens to the filter, Fig. 4C). The outer cell layers of the filter represent the most densely innervated area (Fig. 4A).
Nitric oxide synthase (NOS)-like immunoreactivity (NOS-LI IR) was frequently observed in nerve fibres, both in the nerve bundles leading into the photocyte chamber (Fig. 4E, compare also to Fig. 4B) and in thin varicose fibres running close to the photocytes (Fig. 4F,G). Positive NOS-LI IR was also observed in regularly distributed, unidentified intra- or extracellular structures closely associated with the plasma membrane of the photocytes (Fig. 4H).
Furthermore, NOS-LI IR was present within the cells of the filter. The immunoreaction was most intense in the outer cell layers, and showed a gradual reduction inwards through the filter area (Fig. 4D). Sometimes only the outer cells contained NOS-LI IR. This gradient was most prominent when using the nNOS sc1025 antibody. Occasionally the most lateral cells of the filter appeared without staining in an otherwise strongly immunoreactive filter. Within the individual filter cells, NOS-LI IR was evenly distributed in the cytoplasm while the nucleus and possibly the perinuclear space appear unstained. A few nerve fibres containing NOS-LI IR were seen among the filter cells situated close to the photocytes.
There appears to be a variation in NOS expression between individuals as well as within the same photophore. Variations were seen both in the labelling of the filter cell cytoplasm and in the presence of NOS-LI IR in nerves and other structures among the photocytes. In six out of ten individuals the immunoreactivity in structures among the photocytes was considerable, while it was hardly detectable in the remaining four. Weak NOS-LI IR among photocytes does not correlate with low immunoreactivity in the filter cells.
Antibodies against the three mammalian isoforms of NOS (neuronal NOS, nNOS; inducible NOS, iNOS; and endothelial NOS, eNOS) and one universal NOS (uNOS) antibody were used in the study (Table 1). Labelling varied slightly between different antibodies. Both antibodies against nNOS showed distinct nerve like structures among the photocytes. The N-terminal directed antibody nNOS sc1025 gave stronger labelling in the outer filter cells, while the C-terminal directed nNOS 31030 showed a more homogenous stain throughout the filter (this gradient is likely to be a fixation artefact, with the fixative affecting the N terminal more than the C terminal). The antibodies against iNOS and eNOS usually labelled the cytoplasm of the filter cells weaker than the antibodies against nNOS, and the labelling among the photocytes using these antibodies had a less distinct appearance. Furthermore, the antibody against iNOS gave a diffuse staining inside the photocytes. The universal antibody stained all structures weaker than the other antibodies used in the study.
Pharmacology
Control responses
Addition of adrenaline at a final concentration of 104
mol l1 to control photophores always evoked a slow and long
sustained emission of light. In this first series of experiments, the mean
maximal value of the light response (Lmax) measured on 21
preparations (184.80±96.71 Mq s1) was reached in
36.40±3.9 min (TLmax) and half-extinction
(TL1/2) occurred 43.78±6.27 min afterwards. The
amplitude of the light response was extremely variable among preparations and
was not correlated to the time to reach Lmax
(TLmax) or to the half-extinction time
(TL1/2). These parameters were not significantly different
between the halves of the ventral light organ.
Effects of NO donors
Sodium nitroprusside (SNP)
The effects of the NO donor SNP were tested. Application of SNP at
103 mol l1 for 20 min on isolated
preparations did not induce light emission.
The effects of adrenaline were either enhanced or reduced after SNP treatment. One group of seven preparations showed a significant increase of the amplitude of the light emitted (+132.5±51.9 Mq s1). All individuals in this group had a low control value of Lmax (47.2±16.7 Mq s1). The other group of 14 preparations showed a significant decrease of the light emission (198.4±85.7 Mq s1). Individuals in this group had either a high or a low control value (Fig. 5).
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A closer analysis of the data in the group where a decrease in light
emission was obtained shows that the effect of SNP on the adrenergic response
(i.e. the difference in Lmax magnitude,
Lmax) calculated for each pair of treated and
control photophores, varies with the Lmax value of the
control preparation (Fig. 5). A
regression line with a negative slope was calculated. These results suggest
that the effect of SNP is not constant, but is dependent on the capacity of
the photophore to luminesce in response to adrenaline. In contrast, the
preparations reacting with an increased Lmax after SNP
treatment did not show any such correlation.
No significant correlation was observed between
TLmax and Lmax, suggesting that
SNP does not affect a mechanism controlling the rate of light production
(Table 2). Similarly,
extinction rate of the light emission does not seem to be affected by SNP
since the mean
TL1/2 is not significantly different
from control.
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S-nitroso-N-acetylpenicillamine (SNAP)
In this second series of experiments, we studied the effects of SNAP, an NO
source releasing a large proportion of NO oxidation products
(Lemaire et al., 1999). We
studied the effect of SNAP at 103 mol l1
on the adrenergic response of 13 pairs of preparations.
20 min of SNAP application did not induce luminescence. As described for
SNP, it was found that one group of preparations (N=5) showed a
significant increase of Lmax value (+32.85±11.78 Mq
s1), while the other group (N=8) showed a
significant decrease of Lmax (52.56±16.71 Mq
s1). The differences (Lmax) vary
as a function of Lmax values of the control preparations:
a highly significant correlation was calculated
(Fig. 5). As the negative slope
of the regression line is not different from that found for SNP, it is
suggested that SNP and SNAP have similar effects on adrenaline-induced
luminescence of photophores.
No significant difference in the effects of adrenaline on
TLmax between control and treated preparations was
obtained (Table 2), suggesting
that SNAP does not affect the processes controlling the rate of light
production. On the other hand, TL1/2 is highly
significantly negative, showing that SNAP accelerates the extinction rate.
This effect of SNAP on the light extinction of treated preparations is
correlated (P<0.001) to TL1/2 of control
preparations. In this case, a significant regression line with a negative
slope (0.60±0.12) could be calculated, indicating that SNAP
accelerates the extinction rate more the slower the initial rate of light
extinction.
Hydroxylamine
A series of eight light organs was used to study the effect of
hydroxylamine, which is converted to NO when catalase activity is present in
the treated organ (DeMaster et al.,
1989). Among the eight hydroxylamine (103 mol
l1) treated preparations, four preparations were completely
inhibited when stimulated with adrenaline; the other four preparations showed
a very feeble response with a mean amplitude reduced to 3.23±0.95% of
the control (Fig. 6A).
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Effects of NOS inhibitor
Although NO donors affect the light response to adrenaline, this finding
cannot be used to assert that NO can be generated in the photophores and
involved in the control of luminescence. To examine the potential endogenous
generation of NO in the light emission of the light organs, we studied the
effects of L-thiocitrulline, a potent inhibitor of both
constitutive and inducible isoforms of NOS
(Narayanan and Griffith, 1994)
on the adrenergic response of photophores.
The effects of thicitrulline were examined using 13 pairs of control and
treated preparations. 20 min pre-treatment with L-thiocitrulline at
103 mol l1 failed to induce luminescence
of isolated light organs, but affected the response to a subsequent exposure
to adrenaline (Fig. 7).
Fig. 7A shows that for the
different pairs of photophores, the Lmax change induced by
L-thiocitrulline (Lmax) is related to
Lmax of the control photophore. The relationship is highly
significant (P<0.002) with a negative slope
(1.02±0.18) for the calculated regression line. The analysis
shows that
Lmax is positive in the range of low
Lmax values; the lower the capacity of adrenaline to
induce light on its own, the stronger the potentiation caused by
L-thiocitrulline. Highly luminescing photophores can instead be
predicted to be inhibited by NOS blockade.
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Effects on the cyclic GMP pathway
Since NO is the most potent and effective activator of soluble guanylate
cyclase (Maréchal and Gailly,
1999), we investigated whether the effects of NO occur
via the synthesis of cyclic guanosine monophosphate (cGMP), the
possible second messenger between NO and luminescence inhibition.
To test this hypothesis, we first investigated the effects of dibutyrylguanosine 5',5'-cyclic monophosphate (db-cGMP) a membrane-permeable analogue of cGMP, on the adrenergic light response in a series of 14 light organs. The application of db-cGMP at 103 mol l1 for 20 min did not induce luminescence. The pattern of the adrenergic response was similar in both treated and control preparations and no significant differences were observed between TLmax, Lmax and TL1/2 values.
To test the presence of guanylate cyclase in the light organs and its
possible activation by endogenous NO production, we examined the effects of
ODQ, a potent and selective inhibitor of NO-sensitive guanylate cyclase
(Garthwaite, 1995) in another
series of six light organs.
During the 20 min treatment of the preparations with ODQ at 103 mol l1, no light emission was detected; the mean value of the parameters of the response to adrenaline (TLmax, Lmax and TL1/2) was similar in both treated and control preparations.
To test the possible rapid catabolism of endogenous cGMP by the catalytic activity of phosphodiesterase in the light organs, we studied the effects of pentoxiphylline, an inhibitor of phosphodiesterases. In this case, as in the case of db-cGMP and ODQ, we did not observe any significant effect on the adrenergic light response.
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Discussion |
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Immunohistochemistry
NOS immunoreactivity was localised to several different structures: in
nerves throughout the photophores, in plasma membrane-associated structures of
photocytes, and apparently in the cytoplasm of the filter cells. This agrees
with an involvement of NO in the control of light production and/or emission
from the photophore. Varicose nerve fibres running close to the photocytes,
and the plasma membrane-associated stores of NOS-LI IR material, may be
directly involved in the control of light production, while nerve fibres
innervating the filter area and cytoplasmic NOS in the filter cells may be
involved in the control of light emission from the photophores.
The plasma membrane-associated stores of NOS might be vesicles or
organelles. In neurons from the brain of the Atlantic salmon,
nNOS-immunoreactivity has been detected in mitochondrial membranes as well as
in vesicles (Holmqvist and Ekström,
1997). Furthermore eNOS-immunoreactivity has been found in
mitochondria closely associated to the cell membrane in skeletal muscle from
rat (Kobzik et al., 1995
).
In this study, we have investigated the involvement of NOS/NO in adrenaline
induced light production, but it is feasible that NO is involved in other,
both general (metabolic) and specific, processes in the photophores. Our
positive results, together with previous histochemical results in other
non-mammalian vertebrates including teleosts
(Holmqvist et al., 1994;
Holmqvist and Ekström,
1997
; Olsson and Holmgren,
1997
; Karila and Holmgren,
1997
; Funakoshi et al.,
1999
), suggest that NOS is a highly conserved enzyme amongst
vertebrates. Several studies have established the presence of n-type NOS and
i-type NOS, but not eNOS, in teleost fish (e.g.
Laing et al., 1999
;
Øjan et al., 2000; Cox et al.,
2001
; Jennings, 2004). The antibodies used in the present study
were raised against the mammalian isoforms of NOS (nNOS, eNOS, iNOS). The
strongest and most distinct staining was obtained with antibodies raised
against the C-terminal or the N-terminal of nNOS, and occurred in nerve-like
structures as well as in structures that are not expected to express or
contain nNOS (filter cell cytoplasm, mitochondria-like structures). This
suggests that the NOS isoform(s) present in the light organ of hatchetfish
is/are more similar to mammalian nNOS than to mammalian eNOS or iNOS. A
conclusive determination of the identity of NOS type(s) in the light organ
needs further molecular study but is outside the aims of the present work.
Effects of NO donors
Our results show that all the tested NO donors (SNP, SNAP and
hydroxylamine) affected, in a specific way, the amplitude of the light
response evoked by adrenaline. SNAP and hydroxylamine in addition increased
the rate of light extinction.
Hydroxylamine completely inhibits the light response of the isolated light
organ, and induces a rapid extinction of luminescence induced by adrenaline.
Hydroxylamine is a known precursor of nitric oxide in biological systems that
exhibit a catalase activity (Keilin and
Nicholls, 1958; DeMaster et
al., 1989
). Catalase, unlike superoxide dismutase and glutathione
peroxidase, is present in mesopelagic fish tissues
(Janssens et al., 2000
). Our
results suggest the presence of catalase in Argyropelecus light
organs, and a synthesis of nitric oxide that should mediate the
hydroxylamine-induced inhibition and extinction of luminescence. In this case,
the generation of NO by endogenous catalase in the light organ seems to be a
potent inhibitor of luminescence.
The inhibitory effect of the NO-donors SNP and SNAP is not constant but depends on the capacity of the preparation to luminescence: inhibition is maximal in light organs that produce a large adrenaline-induced luminescence, and it is minimal in those showing a low adrenergic response. The high variability of the inhibitory effect agrees with the very large variability of the NO synthase activity present in the photophores as revealed by immunohistochemistry.
The low adrenergic light emission of some light organs could be due to a high endogenous NOS activity; in this situation the contribution of an external source of NO (SNP or SNAP) might not cause an additional inhibitory effect. On the other hand, in light organs that show a large adrenergic response, the endogenous NOS activity might be too low to affect the light emission; in this case the external source of NO could exert an inhibitory effect.
SNAP and hydroxylamine, in addition, accelerated the rate of light
extinction of the adrenergic response, as indicated by the reduced
TL1/2 value, while SNP apparently did not. A possible
explanation for the differences in magnitude and character of the response is
that the same concentration of NO donor may give different concentrations of
NO as well as different proportions of NO vs oxidation products.
Furthermore, different donors may produce NO in different tissue compartments
(extracellular vs intracellular;
Ioannidis et al., 1996;
Ohta et al., 1997
). Similarly,
the fact that SNP in several cases increases, rather than decreases, the
maximal light production appears to be anomalous. The mechanisms behind this
need further investigation. Nevertheless, the increase in light production,
when it occurs, is restricted to weakly luminescing photophores. Possibly,
NO-production is used as a link in several, counteracting mechanisms balancing
the output of light from the photophores in the countershading situation.
Effects of NOS inhibition
The effect of NOS-inhibition on maximal light production, with a large
stimulation of weakly luminescing photophores and a weaker or no stimulation
of some of the strongly luminescing photophores, is compatible with the view
that the capacity of the photophores to respond to adrenaline is inversely
proportional to the activity of (endogenous) NOS in the photophores. The fact
that some highly luminescing photophores instead respond with a decrease in
maximal intensity may appear more inexplicable, but supports the theory above
that several mechanisms depending on NO production are involved in balancing
the output from the light organ for countershading. Notably, the inhibition of
NOS seems to synchronize kinetics of generation and extinction in photophore
luminescence.
Similar multifaceted roles for NO, depending on the conditions and levels
of its production, have been proposed in other physiological systems. NO
production has been reported to improve mammalian heart efficiency
(Bernstein et al., 1996), as
well as the efficiency of skeletal muscle
(Maréchal and Gailly,
1999
). We could speculate that in the light organ, a minimal
production of NO is essential to control the proportion of chemical energy
effectively transformed into light. Clearly, further studies of the effects of
NO on light organ metabolism are needed.
Mechanism of NO action
The physiological effects of NO in many tissues are mediated either by
cGMP, formed by guanylate cyclase when stimulated by NO, or by modulation of
mitochondrial respiration by competing with oxygen for cytochrome oxidase
(Shen et al., 1994;
Brown, 1995
;
Stamler et al., 1997
). Since
our results show that addition of exogenous db-cGMP, as well as inhibitors of
c-GMP catabolism or NO-sensitive guanylate cyclase, have no effect on the
adrenergic light emission, it is very likely that the NO-cGMP pathway is not
important in the light production of the isolated light organs of
Argyropelecus hemigymnus. Instead, we suggest that in
Argyropelecus photophores, NO affects luminescence levels, by
modulating mitochondrial respiration of the light organ. It is known that the
capacity of isolated photophores to produce light increases in proportion to
the intensity of the resting respiration rate measured before the adrenergic
light response (Baguet and Mallefet,
2000
) and that during light production, the oxygen consumption
initially drops and then increases to a level slightly below the initial
resting level (Mallefet and Baguet,
1985
,
1991
).
Concluding remarks
According to the countershading hypothesis, the photophores of
Argyropelecus can luminesce continuously
(Clarke, 1963), the intensity
being rapidly adjusted and modulated to match that of the background twilight.
Amongst all the neurotransmitters tested, adrenaline alone induces
luminescence of Argyropelecus photophores in vitro, and it
is generally accepted that an adrenergic stimulatory nervous system should be
responsible for the tonic luminescence of the photophores. However, it is
likely that some balancing inhibitory mechanism is necessary to perfectly
match the background levels of light. Unfortunately, all the previously tested
neurotransmitters failed to induce any extinction of the luminescence.
Based on the present results, we can now speculate that NO has a specific
behavioural role to modulate the light emission of the luminescing photophore.
By a reversible inhibition of mitochondrial respiration of the luminous cells,
NO could rapidly change the luminescence level generated by the adrenergic
nervous system. Furthermore, a large difference in NOS expression or activity
among the different preparations may account for the well-known high
variability in the amplitude and the extinction rate of the adrenergic light
responses of light organs isolated from Argyropelecus
(Baguet and Marechal,
1978).
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List of abbreviations |
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Acknowledgments |
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References |
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