Taurine Decreases Lesion Severity In the Hearts of Cardiomyopathy Hamsters
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LE JOURNAL CANADIEN DES SCIENCES NEUROLOG1QUES
Quebec Cooperative Study
of Friedreich's Ataxia
Taurine Decreases Lesion Severity In
the Hearts of Cardiomyopathy Hamsters
JAMSHID AZARI, PETER BRUMBAUGH, ANDRE BARBEAU, RYAN HUXTABLE
SUMMARY: Cardiomyopathic Syrian at one and two months of age have the INTRODUCTION
hamsters develop necrotic lesions conse- same concentrations of calcium, magne- There are a number of studies
quent upon calcium overload from 60 days sium and iron in the quadrants of the heart, indicating that alterations in calcium
of age onward. Taurine, given as a 0.1M except in the left ventricle, which has uptake and content in the heart are
solution in place of drinking water for one significantly higher concentration of cal- closely related to the cardiac necrotic
month prior to sacrifice of animals of cium. Calcium concentrations are 70%, process (Bloom and Davis, 1974;
initial age 35 days, decreased the severity of 1320% and 2100% higher respectively in Fleckenstein, 1975; Fleckenstein et al.,
subsequently developing cardiac lesions by one month, two month andfive month old 1974). The calcium overload may be
40%. Calcium concentration in the heart animals. Five month old animals differ
caused by a number of mechanisms.
was decreased by 57%. Magnesium and slightly but significantly in iron (17%
iron concentrations were unaltered. Tau- decrease) and magnesium concentrations Hartman and Booth (1960) have
rine given in a similar manner for 4 months (17% increase). suggested that sympathetic overacti-
had a protective effect, decreasing lesion Cardiomyopathic hamsters have insigni- vity secondary to lesions of the vagal
severity by 21% and calcium concentration ficant differences in ^-adrenergic receptor nuclei may be one mechanism leading
by 35%. Magnesium concentrations were density compared to random-bred animals to myocardial damage. In such a case,
increased by 12%. Compared to random- and have a significantly higher rate of the cardiac muscle is abnormally
bred animals, cardiomyopathic hamsters taurine influx. sensitive to adrenergic stimulation,
which thus causes an increased flux of
calcium across the cell membrane. In
RfiSUMfi: Les hamsters syriens cardio- controles, les hamsters cardiomyopa- view of the crucial role different
myopathiques developpent des lesions thiques ont la meme concentration en membrane systems such as sarcolem-
necrotiques subse'quentes a une surcharge calcium, magnesium et fer aux divers ma, sarcoplasmic reticulum, and the
calcique a partir de la 60emejournee d'age. quadrants du coeur, sauf au ventricule mitochondria play in regulating cal-
La taurine, donnee en solution 0.1 M au gauche oil la concentration en calcium est cium fluxes and the levels of intracel-
lieu d'eau potable et ce pendant un mois ignificativement elevee. Cette concentra- lular calcium, various investigators
avant le sacrifice des animaux d'age initial tion de calcium est augmentee de 70%,
have directed their attention to study-
de 35 jours, a pu diminuer la severite des 1320% et 2100% respectivement a un mois,
Idsions cardiaques eventuelles par 40%. La deux mois et cinq mois. A cinq mois il y a ing the role of these membranes in the
concentration cardiaque du calcium dimi- une legere modification significative dufer pathogenesis of heart failure (Dhalla,
nue de 57% alors que les concentrations de (diminution de 17%) et du magnesium 1974; Lindenmayer et al., 1971; Nayler
magnesium et de fer sont inchange'es. La (augmentation de 17%). et al., 1971). Decreased ability of the
taurine donnee defacon semblable pour 4 Ces hamsters cardiomyopathiques ne sarcoplasmic reticulum from hearts
mois a toujours un effet protecteur, semblent pas montrer de differences dans having different types of failure to
diminuant la severite des lesions de 21% et la densite des recepteurs fi-adrenergiques, accumulate calcium has been inter-
la concentration du calcium de 35%. La mais le taux d'entree (influx) de la taurine preted in terms of a defect in the
concentration du magnesium augmenle de est significativement augmente.
12%. Par comparaison aux animaux process of excitation-contraction cou-
pling (Dhalla et al., 1975; Muir et al.,
1970; Sulakhe and Dhalla, 1971).
There are also reports concerning
changes in the ability of mitochondria
from failing hearts to transport
calcium (Dhalla, 1976; Sordahl et al.,
1973). Defects in sarcolemma have
received little attention due to the
From the Departments of Pharmacology and difficulties of isolating cardiac sarco-
Pathology, College of Medicine, University of Arizona,
Health Sciences Center, Tuscon and the Department of lemma in a pure form. Recently, Singh
Neurobiology, Clinical Research Instituteof Montreal. and co-workers (1975) have shown
Reprint requests for the complete supplement on that the sarcolemmal fraction ob-
Friedreich's ataxia (Phase three) to: Dr. Andrd tained from cardiomyopathic ham-
Barbeau, Clinical Research Institute of Montreal, 110 sters in advanced stages of myopathy
Pine Avenue West, Montreal, Quebec, Canada, H2W
1R7. had lower activities of Ca 2+ -ATPase,
Vol. 7 No. 4 NOVEMBER 1980-435
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Mg2+-ATPase, and N a \ K+-ATPase. calcium in the cardiomyopathy, and distilled deionized water. Precipitated
Furthermore, activation of adenylate the effect of taurine in controlling proteins were filtered, and the solution
cyclase by epinephrine and sodium calcium overload and necrotic lesion analyzed by conventional atomic ab-
fluoride is markedly depressed. These severity in advance stages of cardio- sorption spectrophotometry with a
membrane enzymes in particular par- myopathy. Varian AA5. An air/acetylene flame
ticipate in raising and lowering the was used for iron and a nitrous
intracellular level of ionized calcium. MATERIALS AND METHODS oxide/acetylene flame for calcium and
Thus, sarcolemmal abnormalities re- Male cardiomyopathic Syrian gol- magnesium. The analytical wave lengths
sulting in altered enzymatic activity den hamsters (CM) of the Bio 14.6 used were 422.7, 285.2, and 248.3 nm
may be responsible for calcium strain and random bred control ham- respectively for calcium, magnesium,
overload. sters (RB) were purchased from and iron.
Although the precise mechanism(s) Telaco, Bar Harbor, Maine. 3 H- Taurine Analysis: Animals were
causing calcium overload is not clear, a Taurine and 3H-dihydroalprenolol sacrificed by decapitation and hearts
number of pharmacological agents were purchased from New England removed, washed in saline, and
have been used to control the calcium Nuclear, Mass. dissected. After being transferred to
overload. Dhalla (1976) has suggested Heart Perfusion: Male hamsters pre-weighed centrifuge tubes, the
heart failure resulting from calcium weighing 100-120g were used. One tissues were diluted 1:10 with 3.5% 5-
overload at early stages can be hour following heparin treatment sulfosalicylic acid, sonicated to homo-
prevented by use of verapamil, propra- (2000 IU/kg), hamsters were anes- genity, contrifuged, and the superna-
nolol or other agents capable of thesized with sodium nembutal (50 tant analyzed for taurine on a
antagonizing calcium movement into mg/kg i.p.) and the heart removed and Beckman model 118C amino acid
the myocardium. Verapamil has been transferred to ice-chilled well-oxygenated analyzer.
shown to be effective in controlling the 0.9% saline containing 5.5 mM glucose. Receptor Binding Assay: Tissue
calcium overload in cardiomyopathies The aorta was cannulated and the from each heart ventricle was homo-
(Jasmin and Bajusz, 1975). Taurine (2- hearts perfused retrogradely at a flow genized with a polytron (Brinkman;
aminoethane sulfonic acid), is a rate of 4 ml/min in a non-recirculating setting 5 for 30 sec) to make a 2.5%
naturally occurring /3-amino acid system with oxygenated Kreb-Henseleit homogenate in 0.05 M Na+-K+ phos-
which is abundant in the mammalian bicarbonate buffer (pH 7.4) containing phate buffer (pH 7.4). The homoge-
heart (Jacobsen and Smith, 1968). 5.5mM glucose. After five minutes of nate was passed through several layers
There are reports that taurine has a perfusion, the buffer was switched to of cheese cloth, and centrifuged at
calcium modulating effect in the heart one containing [3H]taurine (25/nM; 48,000g for 20 min in a Sorvall RC2-B
(Dolara et al., 1973; Guidotti et al., 0.05 /iCi/ml) and substrate perfusion centrifuge. The supernatant was mea-
1971). Taurine has been shown to continued for 4 min, followed by a 5 sured and discarded. The pellets were
increase the affinity of calcium for min washout period. Influx was deter- suspended in Na+-K+ phosphate buffer
various intracellular structures (Dola- mined in two ways: (i) measurement of in a volume equal to that of the
ra et al., 1973, Huxtable and Bressler, the difference in radioactivity of the discarded supernatant. The suspen-
1973). Experimentally, alterations in perfusate and effluent, and (ii) mea- sion was rehomogenized for 5 sec. /3-
the level of taurine in the heart are surement of [ 3 H]taurine remaining in Adrenergic receptors were assayed by
rather hard to achieve (Awapara, the heart following washout. Hearts the method of Bylund and Snyder
1956; Sturman, 1973). However, tau- were homogenized in 8 volumes of 5% (1976). Tissue homogenated contain-
rine concentrations increase in both trichloroacetic acid and centrifuged at ing 80 fxg protein were incubated for 30
human and experimental congestive 40,000 xg for 20 min. The radioac- min at 25° C in 2 ml of 0.05M Na+-K+
heart failure (Huxtable and Bressler, tivity in the deproteinized superna- phosphate buffer containing 0.25 /zM
1974; Peterson et al., 1973). Based on 3
tant was determined by liquid scintil- H-dihydroalprenolol (58 Ci/mmole,
the switterionic nature of taurine at lation counting. NEN) in the presence and absence of
physiological pH, and its strong dipole Spectral Analysis: CM and RB 0.1 ^M (-)-propanolol. The reaction
moment, Huxtable (1976) has sugges- animals were sacrificed by decapita- was terminated by vacuum filtration
ted taurine, through its interaction tion. Hearts were removed and washed through GF/B glass fiber filters
with the zwitterionic phospholipid in 0.9% saline solution containing followed by four 5 ml rinses with
structure of membrane, causes confor- 5.5mM glucose. Atria, right and left buffer at 25° C. Bound 3 H-DHA
mational changes by virtue of stabili- ventricles were dissected, washed and retained on the filter was extracted in 9
zing charge separation. Such confor- blot-dried before transfer to pre- ml of a toluene-based scintillation
mational changes result in alteration in weighed calcium-free volumetric flasks. cocktail and radioactivity counted.
ion flux and cation affinity. Thus, The samples were digested for one Specific 3 H-DHA binding was defined
McBroom and Welty (1977) have hour in 65% ultrapure nitric acid (EM as the binding displaceable by 0.1 /*M
shown taurine to decrease calcium Laboratories, Elmford, New York) on (-)-propranolol.
overload in cardiomyopathic ham- a steam bath. Sufficient ionization Protein Determination: Protein de-
sters. This work is designed to buffer was added to make the final termination for receptor binding stu-
establish the site for calcium overload, solution 1000 ppm cesium. After being dies of the ventricle were performed by
the involvement of other ions beside cooled, the samples were diluted with the method of Lowry et al. (1951).
436-NOVEMBER 1980 Taurine in Cardiomyopathic Hamsters
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Sample Preparation for Histology: We have, therefore, used animals of 30 tend to be higher than in control
Animals were sacrificed by decapita- - 40 days of age as prelesion, and animals. The increase is statistically
tion, hearts rapidly removed, and animals 60 - 70 days of age as significant only in the left atrium
transferred to ice chilled 0.9% saline. postlesion to elucidate which changes (Table 3). The general increase in
The hearts were perfused through the precede the appearance of lesions and taurine content is consistent with the
aorta with cold saline to remove the which changes occur after the appear- higher influx rate of taurine observed
blood, and sectioned transversely into ance of lesions. in the Langendorff-perfused isolated
upper and lower halves. Each time an Cation concentrations in the qua- heart (Table 4).
alternating half was fixed in 10% drants of the heart are illustrated in
buffered-formalin. The other half was Table I for pre- and post-lesion Protective Effect of Taurine on
used for ion and taurine determina- animals. Compared to non-cardiomy- Cardiomyopathic Lesions
tions. Hematoxilin-eosin stained 6 fj. opathic random-bred animals, prele- Both pre- and post-lesion animals
sections were prepared from paraffin- sion hamsters have higher calcium showed decreases in cardiac calcium
embedded tissues. Von-Kossa stained :oncentrations in the left ventricle concentrations of 50 - 60% when
sections were prepared for further only. After lesioning, there is a marked maintained on 0.1M taurine in drink-
confirmation of calcium deposition in increase in left ventricular calcium, but ing water for one month (Tables 5 and
the myocardium. The microscopic again, the atria and right ventricle are 6). The concentrations of iron and
slides were evaluated for calcium unaffected. Magnesium and iron con- magnesium were unaltered (data not
deposition in a blind study. Grading centrations are unchanged in cardio- shown). This treatment caused the
was based on 0-4+ scale with 4+ myopathic hamsters relative to control cardiac taurine content to be slightly
representing the highest level. animals. but significantly elevated (Table 5).
Calculation: Statistical analyses were It seems unlikely that the calcium Oral taurine given for one month,
performed on Wang Series 700 Pro- overload is due to increased /J-adrenergic was also effective in decreasing the
grammable Calculator. All values are receptor density. The binding of a subsequent severity of lesion develop-
expressed as mean ± standard error of specific ^-adrenergic ligand, 3 H-dihy- ment by some 40% (Table 5). The
mean (SEM) and a difference with droalprenolol, is increased by some system used to determine lesion
probability ofTHE CANADIAN JOURNAL OF NEUROLOGICAL SCIENCES
TABLE 2
^-Adrenergic Receptor Binding
in Hearts from 90 Day Old Hamsters
Heart: Body Wet Heart Wt fmole/'H-dihydroalprenolol bound
Ratio x 1(P (mg) mg protein g tissue heart
RB 3.3 ±0.1 395 ± 9 6.0 ± 0.3 334.8 ± 32.5 131.4 ±10.7
CM 4.0 ±0.1 533 ±20 8.5 ± 1.0" 371.2 ±26.6 197.4 ± 34.8
a
p < 0.05
Data shown as mean ± SEM for five hearts per group.
compare CM hamsters without tau- TABLE 3
rine in Table 5 and Table 6). When Regional Concentration of Taurine
animals are maintained on drinking in Hearts of 30 - 40 Day Old Hamsters
water containing taurine, however,
cardiac taurine content does not Taurine (/umole/g wet wt)
decrease over the 4 month treatment LOCATION RB CM
period. In CM hamsters with ad-
vanced cardiomyopathy, the cardiac right atrium 26.4 ± 3.3 36.8 ± 9.3
content of calcium is increased to an
even greater degree, and changes also left atrium 26.7 ± 1.7 33.5 ± 1.0"
appear in the concentrations of other right ventricle 36.3 ± 5.9 35.0 ± 2.0
cations. Magnesium levels are signifi- left ventricle 26.9 ± 3.6 29.4 ± 1.8
cantly elevated, and iron levels signifi- TOTAL TAURINE 28.5 ± 2.3 30.8 ± 2.8
cantly depressed, when compared to
RB hamsters (Table 6). We conclude a
p < 0.025
that taurine treatment has no effect on
Data shown as mean ± SEM for four hearts per group.
the changes in magnesium content but
antagonizes the increase in calcium
and the decrease in iron. TABLE 4
Rale of Taurine Infl AX
DISCUSSION
INFLUX RATE
A major defect in the cardiomyo- Dry Heart nmole/min/g nmole/min/g
Wet Heart
pathy Syrian hamster is an increased Weight (g) Weight (g) wet wt dry wt
permeability of the heart cell mem-
brane to calcium. The resultant RB 393 ± 7 86 ± 2 3.1 ± 0 . 2 14.0 ± 0.8
calcium overload appears to beat least
partially responsible for the energy CM 411 ± 11 84 ± 3 4.6 ± 0.3* 22.6 ± 1.8*
depletion, and necrotic lesions that
develop in the hearts of these animals. * p < 0.005
Although genetic in origin, the cardio- The isolated hearts from 70 - 80 day old hamsters were perfused by Langendorff technique.
myopathic lesions do not develop until The hearts were perfused at a flow rate of 4 ml/min with Krebs-Henseleit buffer for five
around 60 days after birth. Animals of minutes. Then buffer was switched to one containing 25 juM taurine (0.05 /iCi/ml) and
30 days of age, therefore, may be perfused for five minutes. Following the perfusion with substrate, there was a five minute
washout. The rate of influx was determined from the radioactivity remaining in the heart.
referred to as pre-lesion, and animals Data shown as mean ± SEM for five hearts in each group.
of 60 days and upwards as post-lesion.
In hamsters at the prelesioning stage, days. Prior to the appearance of compared to control animals, al-
no difference in calcium concentration lesions, and immediately after the though this increase is significant only
is found between the left and right appearance of lesions, the cations iron in the right ventricle. In general, altera-
ventricles. However, compared to and magnesium are not altered in tions in cardiac taurine concentrations
random-bred control animals, the concentration compared to control are not easy to achieve. However,
calcium content is significantly ele- animals. However, in the old animals, taurine concentrations are markedly
vated in the left ventricle. The excess of magnesium concentrations are eleva- elevated in hearts in congestive failure
calcium massively increases with the ted, and iron concentrations depressed. in both animals and humans (Huxtable
development of lesions. In old animals Taurine concentrations tend to be and Bressler, 1974; Peterson et al.,
(120 days of age), calcium levels are higher in the heart of animals prior to 1973). It has been shown that the p-
even more increased over those at 60 the development of lesions when adrenergic agonist, isoproterenol, sti-
438-NOVEMBER 1980 Taurine in Cardiomyopathic Hamsters
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mulates the rate of influx of taurine in TABLE 5
the isolated perfused rat heart (Hux- Effect of Oral Taurine on Lesion Development
table and C h u b b , 1977). Adrenergic in the Hearts of Cardiomyopathic Hamsters
stimulation of influx is probably
responsible for the elevations in Water Taurine
cardiac taurine concentrations found (10) (18)
in congestive failure. An increased rate
of taurine influx into the heart of car- Serum taurine 0.64 ± 0.05 0.80 ± 0.07
diomyopathic hamsters is also ob- (/umole/ml)
served (Table 4), and this may also be Cardiac taurine 133.8 ± 5 . 7 154.5 ± 5.8°
due to increased adrenergic tone. The (jumole/dry weight)
fact that in 30 day old animals taurine
Cardiac calcium 814 ± 113 353 ± 74b
concentration is only marginally ele-
(jig/g tissue)
vated relative to control hamsters
suggests that taurine efflux is pro- Lesion score 3.0 ± 0 . 4 1.8±0.3 b
bably also somewhat increased.
a = p < 0.025
When animals in the pre-lesioning b = p < 0.010
stage are maintained on 0.1M taurine
solution in place of tap water, calcium Cardiomyopathic hamsters 30 - 40 days old were placed on 0.1 M taurine or distilled water
as drinking water for one month prior to sacrifice. Data shown as mean ± SEM.
accumulation is markedly decreased in
the heart after one month. In addition, The association of decreased cal- feature of Friedreich's ataxia is the
areas of calcium-induced necrosis are cium accumulation, and decreased presence of cardiomyopathy. Hearts
also markedly diminished. A modest severity of lesions after oral taurine from Friedreich's ataxia patients can
increase in cardiac taurine concen- treatment suggests that taurine is show severe and diffuse intracellular
tration accompanies these effects of having a protective effect due to a fibrosis, and some areas of intracellu-
taurine (Table 5). When animals are modulatory action on calcium entry. It lar calcification (Sanchez-Casis et al.,
maintained on taurine solution for 4 has recently been demonstrated that 1976). The actions of taurine on the
months, the protective effects of taurine increases the affinity for cardiomyopathy of cardiomyopathic
taurine still persist (Table 6). Calcium calcium of a calcium binding site on Syrian hamsters may serve as a
accumulation and degree of lesioning the heart cell sarcolemma, thus bring- paradigm for similar cardiomyopa-
are decreased, but magnesium and ing about a lowering of free calcium thies in humans.
iron concentrations are unaffected, levels within the cell (Chovan et al.,
indicating that the effects of taurine 1979). ACKNOWLEDGEMENTS
are peculiar to calcium.
Taurine is a relatively nontoxic This work was supported by USPHS grant HL 19394
These findings confirm and extend substance — a normal constituent of and by a grant from 1'Association Canadienne de
l'Ataxie de Friedreich.
previous studies, in which when human diet — which has potential use
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TABLE 6
Effect of Taurine on Cation Concentrations
and Lesion Score in Advanced Stages of Cardiomyopathy
pmole/g dry wt Lesion
Ca Mg Fe Taurine Score
RB 172 ± 18 858 ± 11 206 ± 2 105 ± 10 0.0
CM WITHOUT
TAURINE 3775 ± 221 1008 ± 8" 171 ±4" 107 ± 6 3.3 ±0.5
CM PLUS TAURINE 2472 ± 543 1006 ± 22" 191 ± 4" 142 ± 11" 2.6 ± 0.4
a = p < 0.001
b = p < 0.025
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