Cardiac morphodynamic remodelling in the growing eel (Anguilla anguilla L.)
1 Department of Pharmaco-Biology, University of Calabria, 87030 Arcavacata
di Rende, CS, Italy
2 Department of Cellular Biology, University of Calabria, 87030 Arcavacata
di Rende, CS, Italy
3 Department of Anatomy and Cell Biology, University of Cantabria, 39011,
Santander, Spain
* Author for correspondence (e-mail: cerramc{at}unical.it)
Accepted 28 May 2004
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Summary |
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The small eel hearts show a basal cardiac output lower than their large counterparts (heart rate fH, 38.93±2.82 and 52.7±1.8 beats min1, respectively; stroke volume VS, 0.27±0.017 and 0.37±0.016 ml kg1, respectively; means ± S.E.M.). The two groups show similar responses at increasing preload, but differ remarkably at increasing afterload. Small eel hearts decreased VS at afterload greater than 3 kPa, in contrast to larger hearts, which maintained constant VS up to 6 kPa. These changes in mechanical performance are related to structural differences.
Compared with the small eels, the large eels show an increase in the compacta thickness and in the diameter of the trabeculae in the spongiosa, together with reduction of the lacunary spaces. The increased compacta thickness is attained by enlargements of both the muscular and vascular compartments and reduction of the interstitium; consequently, this layer appears more compacted. Both compacta and spongiosa show higher number of myocytes together with reduced cross-sectional area and myofibrillar compartment. The compacta also shows an increased mitochondrial compartment. Our results document a cardiac morphodynamic remodelling in the growing eel.
Key words: fish, Anguilla anguilla, myocardial growth, cardiac performance, ventricular ultrastructure, compacta, spongiosa
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Introduction |
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An extensive amount of data from both human and experimental animal
cardiology has detailed the main aspects of ventricular remodelling of the
mammalian heart in response to volume and pressure loading. Ventricular
adaptation to volume loading involves the enlargement of the cavity volume by
increasing myocardial fibre length, with a parallel increase in the thickness
of the ventricular wall. On the other hand, ventricular adaptation to pressure
loading is matched by wall thickening through the parallel addition of
myofibrils, without a corresponding increase in luminal volume
(Braunwald, 1984). This is
illustrated by the paradigm of right and left ventricles of the mammalian
heart working as volume and pressure pumps, respectively. The morpho-dynamic
design of the right ventricle is well suited for ejecting relatively large
volumes of blood against relatively low blood pressure, while that of the left
ventricle is better suited for ejecting relatively low blood volumes against
higher blood pressure (Rushmer,
1972
).
The fish heart is capable of impressive morpho-functional rearrangements to
match the variable hemodynamic challenges resulting from developmental and
eco-physiological changes of the animal, such as changes in body size and
shifts in lifestyle patterns. A notable aspect of this cardiac flexibility is
evident in the close relationship between the structural organization of the
ventricular pump and the mechanical performance of the heart, evaluated in
terms of the relative contribution of pressure and volume work to the stroke
work (Tota and Gattuso, 1996).
In many fish, this relationship allows a distinction between ventricles
producing mainly volume work and those producing mainly pressure work
(Tota and Gattuso, 1996
). This
picture provides an insight into how the internal construction of the
ventricular chamber is adapted to its functional performance. On the other
hand, many fish species experience remarkable changes in cardiac mechanical
performance associated, for instance, with thermal acclimation
(Rodnick and Sidell, 1997
, and
references therein), or with changes in locomotive habits and/or body growth,
or both (Poupa and Lindstrom,
1983
). However, the mechanisms underlying these structural
readjustments are mostly unexplored, both phylogenetically and
ontogenetically. Studies on the parallel morphological and functional changes
of the heart experienced by a fish species during its life cycle could help to
elucidate the relationship between functional flexibility and
bio-constructional constraints of cardiac remodelling in fish.
The European eel Anguilla anguilla L. represents an appropriate
model on which to study the morpho-functional changes that may occur in the
fish heart in association with body growth and changes in life style. The eel
has a complex life cycle which, following metamorphosis, includes a spawning
migration requiring high levels of swimming performance and elevated metabolic
demands (van Ginneken and van den
Thillart, 2000; Ellerby et
al., 2001
). Therefore, it may be expected that cardiac adaptation
plays a crucial role in these organism changes. The aim of this study was to
evaluate the relationship between changes in cardiac mechanical performance
and the structural organisation of the ventricle relative to body growth in
the European eel Anguilla anguilla L. Preliminary results of this
study have been reported in abstract form
(Cerra et al., 2002
).
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Materials and methods |
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Isolated and perfused in vitro working heart preparations
The hearts of seven small and seven large eels were removed from the
animals and placed in a dish of saline for cannulation. Two polyethylene
cannulae were secured in the ventral aorta and in the atrium (at the junction
with the sinus venosus), respectively. Once cannulated, hearts were connected
to a perfusion apparatus, as described by Tota et al.
(1991).
Briefly, the atrial input cannula was connected to an input reservoir, while the ventral aortic cannula was connected to an output reservoir. Input and output pressures were regulated by varying the height of reservoirs with respect to the level of Ringer solution in the perfusion chamber containing the heart.
The Ringer's solution contained the following components in g l1: NaCl 6.68, KCl 0.15, KH2PO4 0.05, MgSO4 0.35, (NH4)2SO4 0.05, CaCl2 0.14, glucose 1, Na2HPO4 0.227; pH was adjusted to 7.77.9 by adding NaHCO3 (about 1 g l1); the Ringer's solution was equilibrated with a mixture of O2:CO2 at 99.55:0.5%. Experiments were carried out at room temperature (1820°C).
Measurements and calculations
Pressure was measured through T-tubes placed immediately before the input
cannula and after the output cannula, and connected to two MP-20D pressure
transducers (Micron Instruments, Simi Valley, CA, USA) in conjunction with a
Unirecord 7050 (Ugo Basile, Comerio, Italy). Pressure measurements (input and
output) were expressed in kPa and corrected for cannula resistance. Heart rate
(fH) was calculated from pressure recording curves.
Cardiac output () was collected over 1
min and weighed; values were corrected for fluid density and expressed as
volume measurements. The afterload (mean aortic pressure) was calculated as
two-thirds of the diastolic pressure plus one-third of the maximum pressure
(Tota et al., 1991
). Stroke
volume (VS; cardiac output/heart rate, ml
kg1) was used as a measure of ventricular performance;
changes in VS were considered to be inotropic effects
(i.e. changes in the developed force at a given resting fibre length).
and VS were
normalized per kilogram of wet body mass. Ventricular stroke work
[WS; (afterload preload) x stroke
volume/ventricle mass, mJ g1;] served as an index of
systolic functionality (Imbrogno et al.,
2001
).
Experimental protocols
Basal conditions
Isolated perfused hearts were stabilized at the basal condition for
1520 min. For the two eel groups, afterload was set to 3 kPa.
was set to about 10 ml
min1 kg1 body mass for the small eels and
20 ml min1 kg1 body mass for the large
eels, by appropriately adjusting the filling pressure. Cardiac parameters were
simultaneously measured during the experiments. Hearts that did not stabilise
within 20 min from the onset of perfusion were discarded.
Physiological experimental protocols
To evaluate the FrankStarling response of the heart, after the
stabilization period (1520 min), starting from basal conditions,
filling pressure was increased until there was no further discernible increase
in . For each filling pressure
increase, the variables of cardiac performance were measured after a 5 min
perfusion with saline. Each increment was 0.5 cmH2O. The output
pressure was stable at 3 kPa.
To examine the ability of the heart to adjust pressure development in
response to increased peripheral resistances, starting from maximum
, the afterload was raised (about 5
cmH2O for each step) until cardiac pumping was sufficiently
compromised.
Ventricular gross morphometry
The hearts of six small (heart mass 0.14±0.012 g; mean ±
S.E.M.) and six large (heart mass 0.67±0.5 g; mean ±
S.E.M.) eels were weighed immediately after sacrifice. The
ventricle was then separated from the atrium and the bulbus arteriosus, and
weighed to determine the relative ventricle mass (MRV:
ventricle mass x 100/body mass).
Morphometric analysis
The isolated hearts of six small and six large eels were blocked in
diastole with an excess of KCl, and fixed in Bouin's fixative or in 2.5%
glutaraldehyde in phosphate-buffered saline (PBS). Samples were then processed
for light or transmission electron microscopy (TEM), according to conventional
procedures.
For light microscopy, Bouin's-fixed samples were dehydrated in graded ethanol, embedded in Paraplast, and serially sectioned at 10 µm thickness. Selected sections were stained with Hematoxylin and Eosin.
For semithin sections and TEM, small cubes of tissue were taken from the middle anterior wall of the glutaraldehyde-fixed hearts. The pieces were then dehydrated in graded acetone and propylene oxide, and embedded in Araldite (Fluka, Chemie GmbH, Buchs, Switzerland). Semithin sections were cut with a LKB III ultratome, stained with 1% Toluidine Blue and inspected to determine orientation. Ultrathin sections were cut with a Leica Ultracut UCT, stained with uranyl acetate and lead citrate, and examined with a Zeiss ME 10C microscope. Micrographs of near-perfect cross-sections of ventricular myocytes were then obtained.
Images were digitalized by using Olympus Camedia Z200 (GmbH, Hamburg, Germany) connected with a Zeiss III photomicroscope (thick and semithin sections), or by using a scanner Umax IIc (UMAX Systems GmbH, Willich, Germany; TEM sections). Morphometrical evaluations were obtained on 256 grey value images using NIH Image 1.61 for Macintosh computer. Geometrical scaling was performed prior to start measurements on both light and TEM images. Each morphometric parameter was measured using at least 12 images for each animal. The thickness of the compacta was quantified by measuring the distance from the border between the epicardium and endocardium. To determine the cross-sectional area of myocytes and myofibrils, and the surface area of the mitochondria, the structures were outlined with the use of a specific software (i.e. lazo tool), which permitted selection of parts of an image in order to measure or modify them. Vascular and trabecular diameters were measured only when the structure possessed a maximum diameter/minimum diameter ratio of approximately 1. The percentage of surface area occupied by both the lacunary spaces and the myocardium was calculated by thresholding random images of different transverse sections of the whole ventricle in order to differentiate the lacunary spaces from the myocardium. The resulting area (in pixels) was subtracted from the total area of the section, thus obtaining the myocardial surface (in pixels).
Six additional hearts (three small, three large) were processed for scanning electron microscopy (SEM). Ventricle samples were dehydrated in graded acetone, dried by the critical point method, and gold-sputter-coated. Observations were made using a Philips SEM 501 scanning microscope.
Statistics
Values are presented as means ± S.E.M. We used Student's
t-test on absolute values for within-group comparison of the curves
(P<0.05 was taken as significant). Comparison between groups were
made using two-way analysis of variance (ANOVA). Significant differences were
detected using Duncan's multiple-range test (P<0.05).
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Results |
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Isolated and perfused in vitro working heart preparations
The in vitro isolated and perfused whole heart preparations work
at physiological loads (i.e. preload, 0.15 kPa; afterload, 3 kPa) and generate
values of output pressure (PO),
, VS,
WS and power that mimic the physiological values of the
animal, as previously described (Imbrogno
et al., 2001
). As indicated in Figs
1 and
2, the isolated and perfused
heart of the large eels showed an improved basal performance with respect to
their smaller counterparts. This is exemplified by the increased basal
fH (38.93±2.82 and 52.7±1.8 beats
min1 for small and large hearts, respectively) and
VS (0.27±0.017 and 0.37±0.016 ml
kg1 for small and large hearts, respectively).
|
|
When exposed to preload increases (up to 0.65 kPa), small and large hearts
revealed a similar FrankStarling response (Figs
1,
2), being very sensitive to
filling pressure increases, ranging from 0.15 to 0.6 kPa. In the two groups,
the maximum (29.29±2.12 and
37.51±1.05 ml min1 kg1 body mass
for small and large hearts, respectively) and the maximum
VS (0.65±0.05 and 0.66±0.008 ml
kg1 body mass for small and large hearts, respectively) were
obtained at an input pressure of 0.55 kPa.
In the small hearts, increases of the output pressure
PO reduced and
VS starting from the first increment. In contrast, the
large hearts were able to sustain increases of PO up to 6
kPa without any significant decrease in VS. Further
increases of afterload significantly compromised cardiac function (Figs
1,
2). Gradual increase of either
preload or afterload did not significantly modify fH in
either of the two heart groups (Figs
1,
2).
Morphology and morphometry
Both small and large eels showed the typical mixed type of ventricle
consisting of an outer compact layer and an inner spongy layer
(Fig. 3). Eel ventricular
growth was achieved by increasing both the compacta thickness and the
trabecular diameters in the spongiosa (Fig.
3, Table 1). This
occurred without a parallel increase in free ventricular lumen. On the
contrary, the surface area of the lacunary spaces was significantly reduced
with growth (Table 1), the
ventricle appearing more `muscularized'. The increase in thickness of the
compacta was accompanied by an increase in the number of vascular profiles,
and in the surface area occupied by vessels, as indicated by a significant
lower myocardium/vessel ratio (Fig.
3, Table 1). In
addition, analysis of the percentage of the surface area occupied by
myocardium, vessels and interstitium in the compacta revealed that myocardium
and vessels undergo a significant increase with growth. However, the
interstitium undergoes a significant decrease
(Table 1). In the spongiosa,
due to the absence of vessels, it is only possible to measure the percentage
of the surface area occupied by the myocardium and the interstitium, and we
did not find significant modifications in either of the two parameters with
growth, although a similar trend in increasing the surface area occupied by
the myocardium and in decreasing that of the interstitium was detected
(Table 1).
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|
In the compacta, the number of myocytes increased with growth, while the cellular cross-sectional area decreased, the myofibrillar compartment decreased, and the mitochondrial compartment increased. In the spongiosa, there was also an increase in cell number with growth, and a decrease in the cross-sectional area and in the myofibrillar compartment. However, the mitochondrial compartment of the spongiosa did not show any significant modification with growth.
When the two eel groups were compared, the compacta of the small eels contained larger myocytes, a smaller myofibrillar compartment, and a smaller mitochondrial compartment than the spongiosa. In the large eels, however, the compacta contained smaller myocytes than the spongiosa, a larger myofibrillar compartment, and a similar mitochondrial compartment (Table 1). Thus, compacta myocytes, despite becoming smaller in size than the spongiosa myocytes with heart growth, contain a higher amount of myofibrillar material.
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Discussion |
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The relationship between heart and ventricular growth vs body
growth, not previously recorded in A. anguilla, shows that heart
growth is linearly related to body growth and that in the two eel groups the
ventricle mass represents the same percentage of the total body mass. Although
a complex network of factors such as cold acclimation, relative cardiac work,
sexual maturity, etc., may modify the rate of ventricular growth in teleosts
(Houlihan et al., 1988;
Graham and Farrell, 1989
;
Clark and Rodnick, 1998
), the
linear increase in ventricle mass during growth of the animal is well
documented (Poupa et al.,
1981
; Franklin and Davie,
1992
, and references therein).
The growing eel ventricle shows enhanced hemodynamic performance, both
under basal and load-stimulated conditions. This is expressed by the increased
basal fH and VS, and by the better
capacity shown by the heart of the large eels to maintain work against higher
PO. As the animal (and, thus, the heart and the ventricle)
grows, fH significantly increases from 38.93±2.82
to 52.7±1.8 beats min1. The fH
values in the isolated cardiac preparation fall within the range usually
reported in anguillidae in vivo (A. japonica:
Chan and Chow, 1976; A.
australis schmidtii: Davie and
Forster, 1980
; A. anguilla L.:
Soulier et al., 1988
) and
in vitro (A. dieffenbachii:
Davie et al., 1992
; A.
anguilla: Imbrogno et al.,
2001
, and references therein). Although the importance of
fH as an index of cardiac performance is well known, there
is scant information concerning the ontogenetic changes of
fH in the eel, or in other teleosts. In particular, as
extensively reviewed by Farrell and Jones
(1992
), while in mammals an
allometric relationship exists between fH and body mass,
so that resting and maximal fH values are higher in
smaller mammals, there is no evidence for a similar allometric relationship in
teleosts. In juvenile and adult trout, the increased body mass relates
positively with an increased cardiac performance, expressed by enhancement of
both fH and VS
(Mirkovic and Rombough, 1998
).
We observed here that, in the large eels, the higher fH is
associated with a higher VS obtained at the same filling
pressure. Taken together, these variations represent the physiological
evidence of an increased basal cardiac performance in the large eels.
In fish, the control of or, more
precisely, the increase in VS, is chiefly achieved by
increasing the filling pressure (Starling's law)
(Farrell and Jones, 1992
). Our
data indicate that there is no variation of cardiac mechanical behaviour in
response to increments in the filling pressure in either of the two eel
groups. However, large eels possess an enhanced cardiac ability to work
against high PO. In fact, the heart of the small eels
fails when PO values higher than 3 kPa are applied.
The dynamic data correlate with modifications of the ventricular
architecture observed during growth. In large eels, the ventricle becomes more
`muscularized', by increasing both the thickness of the compacta and the
diameter of the trabeculae in the spongiosa, together with a reduction of the
lacunary spaces. The increased muscularization and the reduction of the
lacunary spaces resemble the situation described in the compact mammalian
ventricle, where pressure overload is counterbalanced by wall thickening and
reduction of the lumen (Braunwald,
1984). The increase in thickness of the compact myocardium during
cardiac growth is common to many fish species (Ciprinus carpio:
Bass et al., 1973
; Salmo
salar: Poupa et al.,
1974
; Thunnus thynnus:
Poupa et al., 1981
; Salmo
gairdneri: Farrell et al.,
1988
). In the eel, the enlargement of the
epicardiumendocardium distance found in the large animals is paralleled
by an increase in vascularization of the compacta. Clearly, thickening of the
compacta increases the diffusion distances from the blood perfusing the
ventricle and from the subepicardial vessels. In mammalian and non-mammalian
growing hearts, hypoxia appears to be the trigger for an increased
capillarization of the compact myocardium through tightly controlled local
mechanisms (Poupa and Lindstrom,
1983
; Tomanek et al.,
1999
). These include mechanical (e.g. myocardial stretch),
metabolic and growth factors such as vascular endothelial growth factor (VEGF)
and basic fibroblast growth factor (bFGF)
(Tomanek and Ratajska, 1997
,
and references therein). The role of both lower
PO2 and stretch in increasing VEGF levels,
which in turn stimulates endothelial growth, is well acknowledged
(Hudlicka and Brown, 1993
).
For example, in the developing rat heart, hypoxia raises VEGF levels by
increasing the stability of its mRNA and by enhancing its mRNA transcription
rate (Luscinskas and Lawler,
1994
). Moreover, in their study on the trout (Oncorhynchus
mykiss) heart ventricle, showing that the rate of protein synthesis was
higher in the coronary-perfused compacta than in the spongiosa, Houlihan et
al. (1988
) suggested an
intimate link between force of ventricular contraction, coronary perfusion and
protein synthesis in the compacta. On the basis of these considerations, we
suggest that in the growing eels, the enlarged vascular supply of the compacta
is designed to cope with the metabolic and energetic demands of the deeper
myocardial cells.
It should be emphasised that the increase in thickness of the compacta is
accompanied by an increase in the muscular and vascular components per area,
and by a reduction of the interstitium. A similar trend is observed in the
spongiosa. Although the reduction of the interstitium in the compacta is an
overestimation due to the increase of the vascular compartment, our data
indicate that, with growth, the compacta not only increases in thickness but
becomes more compacted. This occurs together with an increase in the amount of
collagen, as it can be observed in semithin sections
(Fig. 3) and after Syrius Red
staining (own unpublished observations). The increase in the amount of
collagen increases stiffness of the compacta, adds structural resilience, and
should contribute to the increased mechanical performance (for an example, see
Weber, 1989).
At the ultrastructural level, the ventricular myocardial modifications
occurring during growth are characterised by an increased cellularity
(expressed as number of cells/units of surface area) and by a decrease in the
cross-sectional area of the myocytes. This indicates, albeit indirectly, that
the increase in mass of the eel ventricle occurs through hyperplasia.
Hyperplasic ventricular growth is common to many fish species, although
hypertrophy has also been shown to play an important role
(Farrell et al., 1988;
Bailey et al., 1997
;
Clark and Rodnick, 1998
). In
fact, it has been reported that myocyte proliferation not only plays a
substantial role in the increase in myocyte mass during fish heart growth, but
also that the role of hyperplasia has been underestimated
(Clark and Rodnick, 1998
). The
importance of cardiac hyperplasia in teleosts is highlighted by the recent
findings in adult zebrafish heart ventricle, which indicate extensive
cardiomyocyte proliferation able to regenerate the injured outer compact
myocardium (Poss et al.,
2002
). Notably, the growth mode of the two layers, compacta and
spongiosa, appears to differ slightly. Compacta and spongiosa myocytes become
smaller during growth, reducing their myofibrillar compartment. However, this
reduction is threefold smaller in the compacta than in the spongiosa. In
addition, the compacta shows an increase in the mitochondrial compartment that
is not observed in the spongiosa. The decrease in cellular cross-sectional
area observed in both compacta and spongiosa during ventricular growth may
represent an advantage to counteract the constraints imposed by the low
area-to-volume ratio, which comes from the absence of a transverse tubule
network (Santer, 1985
;
Rodnick and Sidell, 1997
;
Harwood et al., 2002
, and
references therein). Thus, in the growing eel ventricle, the strategic
decrease of the diffusion distances for small molecules could probably help to
cope with the increased mechanical efficiency of the ventricular wall. In this
perspective, the increment of the mitochondrial compartment, which occurs in
the compacta during growth, is important. Since mitochondria, in association
with myofibrils, represent a basic index of the potential cardiac work
(Kayar et al., 1986
;
Barth et al., 1992
), we suggest
that, in the presence of both an accelerated contractile rhythm and a higher
pumping capacity, the enlargement of the mitochondrial compartment provides
the myofibrillar apparatus with an adequate amount of energetic compounds. A
number of signalling mechanisms and transcription factors are known to
contribute to the coordinated increase in mitochondrial content that is
associated with cardiac growth in response to increased afterload
(Leary et al., 2002
, and
references therein). The increase in the mitochondrial compartment of the
compacta myocytes with growth, together with the smaller decrement of the
myofibrillar compartment, suggests that the compacta may sustain a higher
workload than the spongiosa.
In conclusion, the cardiac ventricle of the eel undergoes important morphodynamic changes during ontogenetic growth. The ventricle of small eels, with its limited response to pressure overload and large lacunary spaces, appears better adapted to produce volume work. In contrast, the ventricle of the large eels is better suited to produce pressure work. These changes in heart performance are accompanied, both in the compacta and in the spongiosa, by an increase in cell number per unit area and a decrease in cellular cross-sectional area. The compacta of the large eels also exhibits an increased vascularization, probably matching the enhanced contractile demands.
Although the intimate molecular mechanisms underlying this cardiac morphodynamic remodelling were not directly addressed by this study, our results strongly suggest that the growing eel heart represents a useful model system for investigating basic aspects of ventricular plasticity from organ to cellular, subcellular and molecular levels.
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Acknowledgments |
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