AliCHIVE
FISHERIES AND MARINE SERVICE
Translation Series No. 4151
The effect of acute hypothermia on the composition of mitochondrial
lipids in the myocardium of warm-blooded animals
by A.P. Shepelev
Original title:. Vliyanie ostroi gipotermii na sostav lipidov mitikhondri miokarda
teplokrovnykh zhivotnykh
From: Fiziol. Zh. SSSR I.M. Sechenova 63(3): 442-447-, 1977
Translated by the Translation Bureau (CJB)
Multilingual Services Division
Department of the Secretary of State of Canada
bepartment of Fisheries and the Environment
Fisheries and Marine Service
Halifax Laboratory
Halifax, N.S.
•
1977
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TITLE IN ENGLISH - TITRE ANGLAIS
. The effect of acute hypothermia on the composition of mitochodrial lipids
In the myocardium of warm-blooded animals.
TITLE IN FOREIGN LANGUAGE (TRANSLITERATE FOREIGN CHARACTERS)
TITRE EN LANGUE éTRANGCRE (TRANSCRIRE EN CARACTÈRES ROMAINS)
Vliyanie.ostroi gipotermii na sostav lipidoy mitikhondri miokarda
teplokrovnykh zhivotnykh.
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riZiOlOgiCheSksi 7.hurnal SSSU im. I.M. Sechenova
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Sechenoy physiological journal of the USSR
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Russian
Fiziologicheski zhurnal SSSR iin. I.M. Sechenova - (Sechenov physiological
journal of the USSR) Vol. 63, No. 3, 1977. USSR.
UDC 612.58
The effect of acute hypothermia on the composition of mitochondrial lipids
in the mocardium of warm-blooded animals.
By A,P. Shopelev, Department of biochemistry (Chairman, E.K. Alimova),
State medical institute, Rostov-on-Don.
(Summary)
In experiments on dogs end albino rats it was established that an
artificial reduction of body temperature by 8 - 10e brings about a change
in the phospholipid spectrum of the mitochondriai lipids of the myocardium
and an increase in - tho unsaturated fatty acid content. On decreasing
the body temperature by 18 - 20 ° , the p,olyene fatty acid content in
the mitochondria of dog myocardia decreases, vhilo in the mitochondria of
albino rat mocardia a high degree of lipid unsaturation is retained.
The role of these changes in assuring mitochondrial functions under
conditions of. hnothermia is discussed, as well as the pôssibility that
animais' resistance) to low temperatures depands on the degree of
re,elgiunma_
. en.t. of the membrane lipids.
* Numbers in the right-hand margin indicate th.o corresponding
pages in the original (trans.).
$. 05.4100-1 0-31
442*
(Text)
It has been ààown by numerous studies conducted on microorganisms,
plants, fish, birds and warm-blooded animals that changes in the temperature
of the environment are accompanied by definite Shifts in the lipid comp-osition of the subcellular structures of these organisms. On reduction
of environmental temperature the quantity of unsaturated fatty acids
in the membrane lipids rises . and/or the content of saturated fatty
acids with a shorter hydrocarbon chain increases, while an increase in
environmental temperature brings about changes of an opposite nature
(3,
4, 6, 13). The change in lipid composition is . probably a compensatory
mechanism which preserves the membrane lipids in an optimal state of
aggregation, which in turn ensures that the membranes can function
under the altered conditions (7).
•
It could be supposed that similar mechanisms should also come
into play on acute cooling, and that the capacity for a corresponding
rearrangement of the membrane lipids is•one of the factors determining
the individual and specific sensitivity of animal organisms to the
effect of cold.
In order •o test this supposition, a comperative study of the
mitochondrial lipid compoSition of dog and albino rat myocardia at
various levels of acute hypothermia was carried out.
Method.
The axperiments were conducted on 18 dogs weighing 12 - 14 kg.
and 45 albino rats weighing 150 -• 180 g. Reduction of body temperature
was effected by immersing the animal in an
lee
bath. The changes in
body temperature were followed with rectally inserted thermocouples.
3
Studies were carried out at the following stages of the experiment:
1 - intact animals (group 1 - control), 2 - reduction of body temperature
by 8 - 1e (group 11)
3 - reduction of body temperature by 18 - 20 ° (group III),
The animals were killed by decapitation. After Washing, the cardiac
muscles were ground into Small pieces and homogenised for 60 sec. in a
0.25 M saccharose solution containing 0.001 M EDTA. To remove the nuclei from
intact cells, the homogenate
was centrifuged for 10 pin. at 600g.
The mitochondrie fraction was separated by centrifuging the supernatant
liquid at 6,500 g for 10 min. The mitochondria precipitate was washed
twice by resuspension in the medium from which it had been precipitated and
repetition
of
centrifuging (8). The entire operation of mitodhondria
separation mus carried out at a temperature of O e - -fe. Electron micro-scopy showed a high degree of purity in the separated mitochondria
free -Lin, on the basis of Which we shall subsequently refer to this
fraction simply as "the mitoChondria". The lipids were extracted with a
chloroform-methanol mixture (2:1). Separation of the .phospholipids into
fractions was effected in a thin layer of silica gel in a chloroformmethanol-water system (65:25:4), while the quantities of individual
phospholipids were determined from the lipid phosphorus content (16).
The quantity of cholesterol was determined by the Lieberman-Burchart .
'reaction (1). Analysis of the fatty acid composition was carried out
by the gas-liquid chromatography method (with u "Tsvet-4" chromatograph,
a copper capilliary as the column, polypropyleneglycol adipete as the
immobile phase; hydrogen as the mobile phase and a flame ionization
detector).
443
4
Table 1.
The fatty acid composition of the mitoChondrial lipids of the
dog myocardium et various levels of acute hypothermia.
Fatty acids
.
Animal groups
II
Myristic
Myristooleic
PaImitic
Palmitooleic
Ileptadecanoic
Stearic
Oleic
Linoleic
Linolenic
Arachidic
Eicosenoi
Mcosadienoic
Eicosatrienoic
Arachidonic
Behenic
Docosatrienoic
Docosapentaenoic
Docosahexaenoic
Saturated
Unsaturated
Monoene,_
Folyene
*
0.5440.05
0.1ft0.01
13.99.t0.50
0.70+0.04
0.58+0.04
23.5441.03
20.16+0.76
18.85+0.45
0.40+0.04
0.92+0.06
0.50+0.04
0.83+0.07
1.17.i10.11
14.03+0.42
0.84+0.05
0.36+0.02
0.82+0.06
1.18+0.12
40.79±1.89
59.1641.29
21.524:0.66
37.64+1.48
III
0 3 2+0.05*
0.2540.02*
15.7040.79
0.56*0.06
0.9440.19*
26.03+0.96
21.4310.84
17.63+1.97
0.3440.05
0.60+0.05*
0.74+0.06*
0.8640.06
0.9540.11
11.20+0.62
0.52+0.04
0.44+0.05
0.8010.06
0.56+0.07*
43.8711.80
55.96+1.95
22.9811.66
. 32.9811.84
0.2640.02*
0.22+0.02*
12.18+0.45
0.80A0.07
0.31+0.02*
19.10+1.01*
20.7041.43
16.8340.79
0.27.4.0.02>
0.854-.0.06
0.85+0.06*
1.12+0.08*
1.98+0.06*
19.78e.35*
0.45*0.03*
0.80±0.05›
1.20à0.09*
2.75±0.11*
33.1511.63*
66.87+2.12*
22.57+1.84
44.3042.10*
Reliability of change from group I figure - p <0.05.
Results of the investipation.
The mitochondrial lipids of the dog myocardium contain a quite
considerable quantity of unsaturated fatty acids, and the level of
polyene
acids exceeds that of monoene acids 1.7 times (table 1).
0
Reduction of the do 's body temperature by 8 - 10 is accOmpanied
by an increase in the degree of unsatUration of the lipids, which is
connected with an increase in the relative content of arachidic acid
end a definite decrease in the quantity of stearic acid. The quantities
of the most unsaturated acids
(docoaapentgenoic
and docosahexaenoic)
5
Table 2.
The fatty acid composition of the mitochondrial lipids of the
albino rat myocardium at various levels of acute hypothermia.
Fatty acids
I
Myristic
Myristooleic
Falmitic
Palmitooleic
Ileptadecanoic
Stearic
Oleic
Linoleic
Linolenic
Arachidic
Eicosenoic
Eicosadienoic
Eicosatrienoic
Arachidonic
Behenic
•
Docosatrienoic
Docosapentanenoic
Docosahexaenoic
Saturated
Unsaturated
Mono one
Polyene
*
Animal groups
II
0.42*0.06
0.24+0.02
16.30-11.24
1.55*0.08
0.96d.0.06
18.94±0.69
16.03*0.80
18.56±1.14
0.3110.03
0.84+0.06
1.0210.06
0.46t0.03
1.43zb0.08
15.92+0.70
1.54t0.06
1.48+0.07
0.94t0.06
2.92t0.16
38.80*1.83
60.69+2.30
18.69+1.05
42.02-11.20
III
0.3310.03
0.25+0.02*
0.1910.02
10.8910.70*
0.46+0.04*
0.4710.0 3 *
13.j9±0.50*
10.35+0.45*
19.3311.20
0.1910.02*
0.2110.02*
0.68+0.04*
0.2610.02*
i.18±0.18*
24.3811.60*
1.1310.05
4.31±0.15e
3 .32t0.27*
5.41t0.40*
26.4011.26*
72.68:12.08*
12.6010.52*
60.08+1.94*
0.19+0.02
12.18+0.84*
0.76170.05*
0.423- 0.03*
17.8310.80
9.04t0.56*
20.32t1. 3 2
0.251.0.02
0.35:10.02*
0.2610.02
0.380.03
3.62+0.22*
23.51+1.40*
0.30k0.02*
3.14±0.26*
1.0510.08
5. 980,20*
31;20+,1.23*
68.9212.26*
10.4710.90*
58.4512.16*
Reliability of change from group I figure - p< 0.05.
also increase
On further decrease of the dog's body temperature
(group III), the relative amounts of arachidonic and docosahaexenoic
acids in the mitochondrial lipids of the myocardia decrease considerably,
while the quantities of palmitic and stearic acids grow higher than the
levels originally indicated. The total polyene acid content decreases,
and the proportion of saturated to unsaturated acids increases by
comparison with the intact animals.
In the mitochondrial lipids of the myocardium of the Intact rat •
(table 2), the polyene fatty acid content is higher, while the stearic
'acid content is lower, thauin the mitochondrial lipids of the
myocardium of the intact dog. The changes in the fatty acid composition
es hypothermia sets in are also somewhat different. On reduction of
the albino rat's body temperature by 8 - 10 0 , the amount of eicosa-trienoic, arachidonic, docosatrienoic, docosapentaemoic and docosahexaenoic
acids in the mitochondrial lipids of the myocardium grows considerably,
While at the same time the relative con.tent—of palmitic , stearic and
oleic acids undergoes a definite decrease. The total unsaturated fatty
acid content rises, as do the proportion of polyene to monoene acids
and the proportion of polyene to saturated acids. Reduction of the body
temperature by 18 - 20 ° is marked by a stabilisation in the altered levels
of arachidonic, oleic and palmitic acids and a return of the relative
stearic acid content to the levels originally indicated.
dog myocardium (table 3),
— Of the mitochondrial phospholipide of the
the phosphatidyl ethanolamine, phosphatidyl choline and diphosphatidyl
glycerol (cardiolipid) fractions are the most important quantitatively
speaking. Reduction of the dog's body temperature by 8 - 10° brings about
an increase in the relative content of phosphatidyl inositols and
phosphatidyl ethanolamines, while at the same time the level of phosphatidyl
cholines decreases. On further reduction of the body temperature by
18 - 20 ° , the phosphatidyl inositol fraction disappears almost completely
from the mitochondrial lipids of the dog myocordium, the phosphatidyl
serine content definitely decreases and the phosphatidyl choline level
rises.
The composition of the myocardium mitochondria of the albino rat
does not differ qualitatively from the phospholipid coMposition of the
* Translator's note:
Literally., inositol phosphatides.
7
" Table 3.
Content of cholesterol and phospholipid fractions in the
myocardium mitodhindria of the dog and albino rat at various
levels of acute hypothermia.(in %).
Lipid fractions
Dog
I
Cholesterol
3.35i0.09
PhosPhatidyl inositols
5.814,0.31
PhosPhatidyl cholines
35.01+1.00
Fhosphatidyl ethanolamines 36.921.02
PhosPhatidyl serines
5.33-10.31
Diphosphatidyl glycerols
16.28+1.03
II
Rat
III
5.70±0.18
3.35±0.11
8.89+0.60* trace qty.
31.421.06* 39.871.32*
40.831.3*
42.154:1.40*
3.10L0.30*
4.870 $2
14.02+0.81 - 13.84+ 0.86
II
2.75-k0.08
7.52+0.51
32.94+1.12
32.704-1.05
5.42+0.30
21.5671.41
* Reliability of change from group I figure - p
III
2.850.1? 3.45+0.101
12.1811.30 -x 3.60+0.29
30.26+1.24 27.71+1.16
39.1841.67*53.02±2.34
6.42+0.54 2.68+0.12J
11.7040.68*12.2940.62 1
0.05.
myocardium of the intdct dog (table 3). The changes in the phospholipid
canposition of the mitochondria in the myocardium of the albino rat on
a body temperature reduction of 8 - 10 ° are basically emilar to the
changes that develop in the dog myocardium at the sanie level of hypo-thermia. However, the more considerable decrease in the quantity of
diphosphatidyl glycerols should be noted. On reduction of the body
temperature by 18 - 20 the relative content of phosphatidyl inositols
and phosphatidyl serines decreases in the mitochondria of the albino rat
myocardium, the low figures for the diphosphatidyl glycerol content are
retained and, in distinction to the changes in the dog myocardium, the
445
quantity of phosphatidyl ethanolamines increases considerably, while the
level of phosphatidyl cholines decreases.
The mitodhondria of the dog myocardium are distinguished by a
higher.cholesterol content. The cholesterol content of the mitochondria
both of the do g myocardium and of the albino rat myocardium remain virtually
unchanged on decrease of the animal's body temperature by 8 - 10 ° , but
they Clow a definite increase under conditions of deep hypothermia
(reduction of body temperature by 18 - 20 0 ).
Discussion of results.
The modification of the fatty acid composition of the myocardium
mitochondrie that occurs during the development of hypothermia is
probably of a compensatory nature, aimed at preserving the biological
properties of the membranes under the new temperature conditions. It
is well known that.the lipids in the structure of biological membranes
are in a liquid crystal state, which not only makes possible the essential
degree of permeability, but also creates conditions for the enzyme
proteins to undergo conformational changes corresponding to optimal
activity. The state of aggregation of the hydrophobic layer of the
biomembranes depends ()lathe lipid composition and on the surrounding
temperature. Thermally induced structural rearrangements connected with
the solidification of the lipids are characterised by a sharp decrease
in the activity of the enzymes that are tightly bound to the membrane.
The magnitude of the thermally induced rearrangements is determined
principally by the length of the chain and the degree of unsaturation
of the fatty acids that make up the structure of the membrane phospho.
. -lipids, and also by the proporton of phospholipide to cholesterol.
The more pronounced increase in the degree of unsaturation
of the mitochondrial lipids of the myocardium of . the albino rat, as
compared with the changes developing in the dog myocardium, on decrease
of the body temperature by 8 - 10? and, especially, by 18 - 20 41 could, •
apparently, be one of the reasons for the . rat's greater resistance to
the action of low temperatures, due to a lowering of the temperature of
the phase change and preservation of the liquid crystal structure pethe
membranes under the altered temperature conditions.
9
The changes in the fatty acid composition cerrelate with the shifts
in the phospholipid spectrum. Of the mitochondrial lipids in the
myocardium, the most unsaturated are the phosphatidyl inositols
and the Phosphatidyl ethanolamines, Wbile the phosphatidyl serines have
a lesser degree of unsaturation (12). We can assume that the daange in
the unsaturation of themitochondrial lipids of the animal myocardium
on artificial reduction of body temperature are dependent upon fluctuations
in the relative amount of these fractions. The variations in the relative . 446
content of phosphatidyl inositols and phosphatidyl serines are of
particular interest. The' phosphatidyl inositols and-phosphatidyl
serines
are the most rapidly metabolizingfractions of phospholipids (5), and their
level depends on the state of antioxidative activity and the intensity
of the peroxidation process (2). We established previously (9) that in
the terminal period of hypothermia the'processes of peroxide folmation
are stimulated in the organisai of marm-blooded animals and the antioxidative
activity of the lipids decreases. As a consequence of these disturbances
not only can the quantity of unsaturated fatty acids undergoing free-radical
oxidation decrease, but also the phosphatidyl inositols and phosphatidyl
serines can leave the mitochondrial membranes more rapidly, which leads
to a decrease in the relatiVe content of these fractions (2). The changes
in the mitochondrie of the dog myocardium are particularly demonstrative
in this respect. On decrease of the body temperature by 18 - 20 ° , the
phosphatidyl inositols can be detdrmined only in trace quantities in
the mitodhondrial lipids, while the level of polyene acids is lower than
in the mitochondrial lipids of the myocardium of the intact animals.
The degree of unsaturation of the phospholipids also determines
•
1.0
the temperature characteristics of the actfvity of the en7ymes that
are bound to the membranes (11).
For processes of oxidative phosphorylation to occur, the participation
of- phospholipids with unsaturated fatty acids is'also essential. The
decrease in the content of unsaturated fatty acids in the mitoChondria
is also accompanied by a decrease in the concentration of a 1ia3 cytochromes,
in the activity of succinate oxidase and NADN
2
oxidase
- (17)
and in the quantity of ATP molecules formed on the oxidatiOn of
substrates (15).
The increase in the relative content of unsaturated phosphatidyl
inositols and phosphatidyl ethanolamines in the mitodhondrial lipids of
the albino ratte myocardium on reduction of the body temperature by
8 -
le,
and the increase in the phosphatidyl ethanolamines on reduction
of th bodytanperature by 18 - 200 must obviously facilitate the
contractile function of the myocardium by supplying a definite quantity of
energy. Possibly this is what explains the information (14) that cessation
of cardiac activity in rats on a diet contaiining a supplement of corn
oil, which is unsaturated, occurs at a .lower temperature (+7.2) than in
rats on a diet containing coconut oil, which is saturated (at-1-12.9 ° ).
On the other hand, the introduction of natural and synthetic antioxidants
prolongs the life of albino rats under low temperature conditions (10)',
which may be due not only to inhibition of the free-radical oxidation of
the lipids, but also to a decrease in the microviscosity of the membranes (2).
.
Reduction of dogs' body temperature by 18 - 20 ° generally leads
to their death, While albino rata under similar conditions retain their
viability in 100A of en ses and die onlY after reduction of the body
temperature by 27 - 300 .
11
Heart failure is one of the main causes of the death of warmblooded animals resulting from acute cooling. We can assume that the
limtedopPnsaryibltes
in the dog's organism are insufficient
to prevent structural rearrangements and lateral separation of phases
in the mitochondria). membranes on acute cooling, which is accompanied
by an intensification of the free-radical oxidation of lipids and the
irreversible destruction of lipid-protein membrane complexes.
Aparently . the albino rat's more perfect mechanisms for the transformation of membrane formations, daveloped.in-thproceseof.evolution,
are one of the factors enabling the albino rat to retain viability under
conditions of more substantial reduction of body temperature than those
endured by the dog.
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of blood. Moscow, 1953.
A.V. Alesonko, E.M. Molochkina, N.P. Palemine,
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'
nocrynsmo G VII 1376
THE ACUTE HYPOTHERMIA EFFECT ON THE
COMPOSITION OF THE MITOCHONDRIA LIPIDS IN THE
MYOCARDIUM OF WARM—BLOODED ANIMALS
A. P. Shepelev
Medical Institute, Rostov on Don
In dogs and albino rats, artificial drop of body temperature by 8-10 ° C elicits change
of phospholipid spectre and increases amount of unsaturated fatty acids in lipids of the
myocardium mitochondria. Drop of the temperaturo by l8-20° C der.reased amount of
polyen fatty acids in dogs but caused no changes in the high amount of unsaturated lipids in vats. Rolo of tiles° facts in mitochonclrial functions during hypothermia and
possible depemlenco of the animals resistance against low temperature of the degree of
membrane lipids reori,mnization, are discussed.