The activity of acetylcholinesterase (Ache) and butyrilcholinesterase (Bche) in the blood and the heart of 3 and 13 month old control male rats is considerably lower than in female rats. In 25 month old rats, no sex differences in the Ache and Bche were revealed in the heart. In 3 and 13 month old male and female rats, under conditions of muscular exercises, the Ache and Bche activity is lower, and in hypokinetic male rats -- higher than that in respective control animals. In all the rats, irrespective of sex, age, and motor conditions, Ache and Bche activity tended to decrease from the sinoatrial node to the heart apex

Antonova, G. A.

Rozanova, V. D.

English

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NASA TECHNICAL MEMORANDUM
	 NASA TM-75951
ACTIVITY OF CHOLINESTERASES OF BLOOD AND HEART
IN .RATS OF DIFFERENT SEX AND AGE DURING
MUSCULAR LOADS AND HYPOKINESIA
V. D. Rozanova, G. A. Antonova
(NASA--TM-75951) ACTIVITY OF C.HOLINESTERASES	 N80-15781
OF BLOOD AND .HEART IN RATS OF DIFFERENT SEX
AND AGE DURING MUSCULAR LOADS AND
HYPOKINESIA (National Aeronautics and Space
	 Unclas
Administration) 14 p HC A02/MF Afi1 CSCL 06C G3/51 46920
Translation of: "Aktivnost' kholine gteraz krovi i
serdtsa krys raznogo pola i vozrasta pri myshech-
nykh nagruzkakh i gipokinezii," Fiziologicheskiy
Zhurnal SSSR, Vol. 64, No. 7, July 1978, pp. 999-
1003.
t	 _
NATIONAL AERONAUTICS AND SPACE ADMINISTRATION
WASHINGTON, D.C. 20546	 DECEMBER 1979
ACTIVITY OF CHOLINESTERASES OF BLOOD AND HEART IN RATS OF 	 /999*
DIFFERENT SEX AND AGE DURING PIUSCULAR LOADS AND HYPOKINESIA
n t
d	 V. n. Rozanova and G. A. Antonova
Laboratory for Age-related and Comparative Pathophysiology
(Chief: I. A. Arshayskiy)
Institute of General Pathology and Pathophysiology, AMS USSR
*Moscow
The activity of acetylcholinesterase (Ache) and
butyrilcholinesterase (Bche) in the blood and the sections
of the heart in white male rats 3 and 13 months old was lower
than in females. In old animals (25 months) difference according
to sex in Ache and Bche activity in the sections of the heart
is absent. In males and females 3 and 13 months developing
under conditions of muscle loads, Ache and Bche activity in
the blood and all sections of the heart was lower, while in
those developing under conditions of hypokinesia it was higher
than in control rats. In rats of all age groups, regardless
of age, sex, or conditions of development, a decrease in Ache
and Bche activity was found from the sinoatrial node to the
heart apex.
Key words: acety"(.holinesterase, butyrilcholinesterase,
hypokinesia, muscle load.
Laboratory work has shown the significance of the
characteristics of skeletal-muscle development as a factor in
determining the level of energy expenditure and activity of the
* Numbers in margin indicate pagination of foreign text.
1
vegetative organs in the ontogenesis process, which has found
expression in the "energy principle of skeletal muscles,"
formulated by I. A. Arshayskiy 2-4 The development of the or-
ganism under conditions of systematic muscle load leads to
the economizing of vegetative functions, linked to the streng-
thening c , cholinesterase mechanisms of regulation -9 . In
connection with the fact that in previous works study was made
of changes in activity in, for the most part, true cholin-
esterase without differentiation according to sex  and only
in the blood9 , in the present work acetylcholinesterase (Ache)
and butyrilcholinesterase (Bche) activity was studied not only
in the blood, but also in the tissues of various sections of
the heart in rats (male and female) which developed under
varying levels of muscle load. In addition, the task was
assumed of investigating the changes in acetylcholinesterase
and butyrilcholinesterase activity according to sexual difference
in control males and females during the period from sexual
maturity to old age.
PROCEDURE
Studies were carried out on mongrel rats, male and
female. Animals in groups 1 and 2 (males and females) developed
from 1 to 3 months under load conditions from running on a
treadmill on alternate days with a gradual increase in running
time from 5 to 30 minutes. The third group (males) developed
from I to 3 months under conditions of hypokinesia, created
by being kept in narrow cages. Animals in group 4 (males)
developed from 1 to 13 months of age under load conditions from
N.	 24 .
running on alternate days from 30 to 100 minutes. Rats in
the first three groups were sacrificed at age 3 months and the
rats in group 4 at 13 months. At these same times, rats in
the three control groups of corresponding age and sex, which
developed under normal conditions, being kept in a vivarium,
were also sacrificed. In addition, in connection with the
second task, investigating the changes in acetylcholinesterase
and butyrilcholinesterase up to the period of aging, 3
additional groups of control rats were taken for study: females
13 months old, males and females 25 months old. From each
rat, blood was taken, as well as tissues from three sections
of the heart: regions of the sinoatrial and atrioventricular
nodes and the contractile myocardium of the apex of the left /1000
ventricle. Ache and Bche activity was determined by the method
of A. A. Pokrovskiy6
 in blood plasma and in tissue extracts
from the heart sections and was expressed in micromoles per
gram or per ml per minute. The substrate for determining
Ache activity was acetylcholineloride and for Bche, butyril-
choliniodide. The data were processed statistically according
to Student.
RESULTS OF THE INVESTIGATION AND DISCUSSION
In comparing the data from the control animals 3,
13, and 25 months old it is clear that the activity of the
enzymes under study in the blood is lower in males than in
females: Ache by 60, 39, and 32% and Bche by 70, 49, and 63%
3
P _^
respectively (see table). Comparison of the enzyme activity
values from the sections of the heart also shows that in males
of 3 and 13 months they are significantly lower than in
females. In old rats (25 months) the sex-related differences
in activity values for Ache and Bche in the sections of the
heart are leveled out or are absent. In the blood these
differences do not disappear, but for Bche they even increase
in comparison with 13 month olds.
Development of animals under conditions of systematic
muscle loads induces a significant decrease in Ache and Bche
activity in males and females as compared to the values in
control rats of corresponding age and sex. in 3 month old
males this decrease, in the majority of tests, is much sharper
than in females of the same age. Ache activity in the blood
of male test animals was lowered., compared to control males,
by 33%, while in test females the figure was 25%. The degree
of decrease in Ache and Behe activity in test males in the
atrioventricular node (by 65 and 69%) and Bche activity in
the myocardium (key 70%) compared to the decrease in test
females (by 46, 38, and 35%) is also quite sharp. In the
remaining cases no substantial differences were found in the
degree of decrease in Ache and Bche activity in test males
and females as compared to control animals. With regard to
the decrease in the absolute values of all the indices under
study in test males of 3 and 13 months, they were in all cases
significantly lower than in test females.
Vj
	 4
1-'
The development of males from 1 to 13 months under
conditions of hypokinesia leads to the opposite changes in
the activity of the enzymes under investigation. In them a
significant increase is noted in Ache and Bche activity in
the blood and in almost all sections of the heart (by 61--91%)
compared to 3 month old control males. In the sinoatrial and
atrioventricular nodes the increase in Ache activity under
hypokinesia was markedly less (by 46 and 31%).
Examination of the dynamics of the changes in Ache
and Bche in the sections of the heart allows the determination
of a decrease in the activity of these enzymes from the sino-
atrial node to the atrioventricular node and to the apex of
the heart. This decrease of 40-58% in the majority of cases
takes place in all control and test rats regardless of age,
sex, and level of muscle activity. Only in 3 month old control
females is the gradient of enzyme activity less pronounced.
It should also be observed that in the blood Ache
activity is higher than Bche activity, while in the heart
tissues, on the other hand, Bche activity is higher than or
does not differ from Ache activity.
The sharp differences according to sex, revealed in
the study, of the activity level of enzymes that break down
acetylcholine in control rats allows us to assume a higher
level of cholinergi c background in regulation in males than
in females. These differences are more sharply pronounced in
the third month of life (the period when sexual maturity
5
begins) and decrease somewhat by 13 months -- the end of the
reproductive period, when the first symptoms of aging appear.
Previous laboratory works 10 , 11 have shown that male
and female rats differ in the level of development of their
skeletal musculatvrc and the level of energy and activity
in their vegetati•,^e organs. In males, the 02 requirement
and heart rate at 4 and 13 months are 13, 18, 15, and 16%
lower respectively than in females 10 '11It may be assumed
that lowered Ache and Bche activity in the blood of males
	 /1002
provides a more pronounced economizing of energy expenditure
in them at rest than in females. Lowered Ache and Bche ac-
tivity in the region of the sinoauricular node in 3 and 13
month old control males coincides with lower heart rate values
in these age groups (305±9.1 and 292±4.7 per minute) as
compared to the females (36015.1 and 34413.9 per minute). Since
tonus vagus is hardly pronounced in rats 2 , it may be assumed
that the lower heart rate values in males are due to lowered
Ache activity in the pacemaking node of the heart. By old age
(25 months), sex-related differences in Ache and Bche activity
in tissues from the sections of the heart almost disappear.
This may be explained by the decrease in acetylcholine synthesis
in the auricle in old rats, in connection with decreased
choline acetylase activity5 . Our data on the disappearance by
age 25 months of sex-related differences in Ache activity
at the sinoatrial node allows us to assume the absence of
differences in old rats with respect to acetylcholine content
6
k'
Acetylcholinesterase and butyrilcholinesterase activity in the
blood ( mole/ml/min) and in the cardiac tissues ( mole/g/min)
in rats of various age (males and females): controls (C), those
developing under conditions of muscle load (M) and hypokinesia
(H)	 (M + m) .
Age (In Acet lcholinesterase Activity
months Blood Sinoatrial Node i!
and sex) C M	 H C	 M
3d' 0.86 t 0.58	 1.65 1.54	 1.00 t	 2.	 t
0.03 0.05	 0.01 0„03	 0.009	 0.03
3° 2.14 t 1.60	 - 3.20 t	 2.10 ±	 -
0.01 0.02	 - 0.02	 0.04
13d' 0.95 ± 0.82 t
	
- 1.40 t
	
0.50 f
	
-
0.01 0.01	 - 0.04	 0.007
	 -
13Q 1.55 -	 - 2.65 t
	
-	 -
0.01 -	 - 0.01	 -	 -
25e 1.04 t
-	 -
1.47 ±	 -	 -
0.03 -	 - 0.01	 -	 -
25d 1.53 f -	 - 1.49*t	 -	 -
0.01 -	 - 0.02	 -	 -
Atrioventricular Node M ocardium of Left Ventr.
30 1. 22 t 0.38	 1.60 0.93	 0.39t1.50 t
0.02 0.04	 0.01 0.009	 0.01	 0.03
3 2.60 t 1„40 ±	 - 2.60 f	 1.20 f-
0.01 0.02	 - 0.03	 0.04	 -
13 cd 1.00 f 0.40 ±	 - 0.66 f	 0.29 t	 -
0.01 0.009	 - 0.02	 0.01	 -
139 1.40 -	 - 1.18 ±	 -	 -
0.008 -	 - 0.01	 -	 -
25,,jf 0.05 f -	 - 0.69 ±	 -	 -
0.89* -	 - 0.01	 -	 -
256' 0.89*f -	 - 0.73*±	 -	 -
0.007 -	 - 0.01	 -	 -
7
Age (In But rilcholinesterase Activity
months Blood Sinoatrial Node
and sex) C M H	 C M	 H~
c v t1.7 5 ± 1.13	 3.00 f
0.02 0.03 0.01	 0.01 0.01	 0.009
3 ? 2.50 t 1.28 f -	 3.80 t 2.50 t	 -
0.03 0.01 -	 0.009 0.01	 -
13 d 0.75 f 0.45 t -	 1.70 ± 1.46 ±	 -
0.02 0.01 -	 0.03 0.01	 -
13 1.48 f - -	 2.75 ± -	 -
0.003 - -	 0.02 -	 -
25 dt 0.72 f - -	 2.16 ± -	 -
0.008 - -	 0.01 -	 -
25 dl 1.97 t - -	 2.21 f -	 -
0.01 - -	 0.01 -	 -
Atrioventricular Node Myocardium of Left Ventr.
3 d' -.^ J 0.49	 2.90 1.22 t 0.36	 2.00±
0.009 0.01	 0.03 0.04 0.03	 0.02
3 2.90 f 1.80 ±	 - 2.90 t 1.90 t
	
-
0.01 0.04	 - 0.01 0.02	 -
13 d` 1.18 t 0.39 #	 - 0.74 f 0.29 *	 -
0.02 0.01	 - 0.03 0.01	 -
13 1.46 -	 - 1.14 -	 -
0.01 -	 - 0.01 -	 -
25 d' 1.37 f -	 - 0.98 -	 -
0.01 -	 - 0.05 -	 -
25 1.43*f -	 - 1.23 f -	 -
0.02 -	 - 0.006 -	 -
Note. The differences between values in males and females
cvitfiin each age group as well as in groups M and H are
statistically reliable as compared to the corresponding control
group. Unreliability of sex-related differences in groups
of rats 25 months old is denoted by the asterisk *. The number
of 3 month old animals in groups C and M is always 10, in
group H -- 7; 13 month old males in group C -- 10; in all
remaining groups --- 5.
V
	 8
and choline acetylase activity.
The sharp differences according to sex that we dis-
covered in the activity of the enzymes that break down acety-
choline allow us to conclude that studies on questions of
neuro-humoral regulation in pubertal rats should be carried
out with obligatory division of them according to sex.
Previous laboratory studiesl0oll
 have shown that
muscle loads lead by age 4 and 13 months to a decrease in
basal metabolism in males by 19 and 26% and in females by 23
and 18% compared to control rats of corresponding age and sex.
In test rats of both sexes, the heart rate also decreased in
comparison with control animals. Comparison of data from the
present work with material from previous laboratory studies
allows the conclusion that the decrease in Ache activity in
the blood and in cardiac tissues is associated with the econo-
mizing of energy expenditure and activity of the heart. This
conclusion is substantiated by analysis of the data obtained
from 3 month old males raised under condition s
 of hypokinesia.
Increased Ache activity in them is associated with increased
energy expenditure and heart rate10,11 as compared to control
`	 rats and especially to rats developing from the age of one
month under conditions of muscle load.
A previous study 10 has shown that in rats of both
sexes by age 4 months, the catecholamine content in the adrenal
glands and in the truncus cerebri is raised and in males this
increase is even slightly greater than in females. In connection
9
F^
6'
with this, the differences by se-x, in energy expenditure and
cardiac activity under resting conditions, as well as the
decrease in these indices in rats developing under conditions of
muscle loads, may basically be explained by the substantial
decrease in Ache activity in the blood and in cardiac tissues.
The decrease we found in Ache and Bche activity in
the direction from the sinoatrial node to the apex of the
heart in rats of all control and test groups is apparently
linked to the gradient of the heart's automatic activity and
to the peculiarities of acetylcholine distribution 13,14 . This
gradient takes place in animals of other species and is
determined, as shownl , from the first day of life.
It should be noted that the dynamics of age-related
changes in Ache and Bche activity in the blood and cardiac
tissues are different in control males and females developing
under normal conditions. In males from 3 to 25 months Ache
and Bche activity changes insignificantly, while in females
a sharp decrease is noted. In this way, the disappearance of
sharp sex-related differences in Ache and Bche activity by
old age occurs basically by way of the decrease among the
females.
LITERATURE
1. Antonova, G. A. "Dinamika aktivnosti atsetilkholin- i
butirilkholinesterazy v tkanyakh serdtsa u sobak v postnatal'nom
ontogeneze" ("Dynamics of Acetylcholinesterase and butyril-
cholinesterase Activity in Cardiac Tissues of Dogs in
postnatal ontogenesis"). Byulleten' eksperimental'noy biologii
10
^I	
;
i me.aitsin , 1973, 76, 12, 7 - 9.
2. Arshayskiy, I. A. Ocherki o vozrastno fiziolo ii
("Outline of Age-related Physiology"),  P	 .: Me itsi.na,
Moscow, 1967.
3. Arshayskiy, I. A. "Rol' energeticlieskikh faktorov v 	 /1003
kachestve vedushchikh zakonomernostey ontogeneza" ("The Role
of Energy Factors as the Primary Factors in Ontogenesis"),
in the book Vedushchie fakto ontogeneza ("Primary Factors
of Ontogenes'1	 P	 .: Nau ova Du a, Kiev, 1972, 43 - 72.
4. Arshayskiy, I. A. "Fiziologicheskie mekhanizmy nekotorykh
osnovnykh zakonomernostey ontogeneza" (Physiological Mechanisms
of Several Basic Factors in Ontogenesis"). Uspekhi fiziolo-
gicheskikh nauk, 1971, 2, 4, 100 - 141.
5. Verkhratskiy, N. S. "Obmen mediatorov i reaktsiya effektorov
na kholinergicheskie i adrenergicheskie vliyaniya v starosti"
("Mediator Metabolism and Effector Reaction to Cholinergic and
Adrenergic Influences in Old Age"). Dissertation, Kiev, 1971.
6. Pokrovskiy, A. A. Rukovodstvo po izucheni u pitaniyya i
zdorov' a naseleniya ("Han oO or the Study of the Nutrition
and Health of the Populace"). Moscow, 1966, 144 - 147.
7. Rozanova, V. D. Ocherki po eks2erimental l noy vozrastno
farmako12 ii ("Outli-n-7-67 Experimental Age-Related P arma-
co ogy	 Publ.: Meditsina, Leningrad, 1968.
8. Rozanova, V. D. "Negro-gumoral'nye mekhanizmy regulyatsii
gomeostazisa i intensivnosti costa v razlichnye vozrastnye
periody" ("Neuro-Humoral Mechanisms for the Regulation of
Homeostasis and Growth Intensity in Various Age Periods"). In
the book Vedushchie faktor ontogeneza_ ("Major Factors of
Ontogenesis	 Pu .: Naukova dZFMa,--Kiev, 1972, 232 - 243.
9. Rozanova, V. D., Musin, B. S. "Razvitie dykhatel'noy i
serdechno-sosudistoy sistem u krys v ontogeneze v usloviyakh
trenirovki (k mekhanizmu vozniknove:liya tonusa vagusa)" ("De-
velopment of Respiratory and Cadiovascular Systems in Rats in
Ontogenesis under Active Conditions (toward the mechanism of
development of tonus vagus)"). Fiziologicheskiy zhurnal SSSR,
1968, 52, 11, 1327 - 1333.
10. Rozanova, V. D., Savkiv, T. G., Khodorova, N. A. "lzmenenic
energotrat i soderzhaniya katekholaminov v mozge i nadpochech-
nikakh u krys v usloviyakh myshechnykh nagruzok i pri gipo-
kinezii" ("Changes in Energy Expenditure and Catecholamine
Content in the Brain and Adrenal Glands of Rats under Conditions
of Muscle Load and tinder Hypokinesia"). Fiziolgicheskiy
zhurnal SSSR, 1976, 62, 2 1 304 - 309.
11
L
If
11. Savkiv, T. G. K kharakteristike osobennostey ener etiki
organizma v zavisimosti ot pola pri razvitii v usloviyakh
c s viva razlichny1ch form s e etno-m s ec n 	 na ruzo
C c Zterist c Features of Energy in the Organism as related
to Se" during Development under Conditions of Various Forms
of Skeletal Muscle Loads"). Dissertation, Moscow, 1974.
12. Ugol:baeva, I. S. "Osobennosti gomeostaticheskoy reaktsii pri
gipoksicheskoy gipoksii u sobak v razlichnye vozrastnye
periody' ("Features of Homeostatic Reaction During Hypoxic
Hypoxia in Dogs at Variot r. Age Periods") . BBu^l, leten'
eksperimental'noy biologii i me&-tsiny, 196 , 38, 9,-34 - 39.
13. Vlk I., Tucek, S. "Distribution of Acetylcholine in the Auricles
of the Mammalian Heart. Physiol. bohemoslov., 1961, 10,
65 - 69.
14. Vlk I., Tucek, S. "Changes in the Acetylcholine content and
Cholinesterase activity in dog atria during early postnatal
period:" Physiol. bohemoslov, 1962, 11, 53 - 57.
Received 26 September 1977
COPYRIGHT HOLDER: Izd.atel'Stvo "Nauka"
Fiziologicheskiy zhurnal SSSR im.
1. M. Sechenova, 1978
^_ w
12


Activity of cholinesterases of blood and heart in rats of different sex and age during muscular loads and hypokinesia

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