ENZYMOLOGY AND MECHANOCHEMISTRY OF TISSUES AND CELLS

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• Document Number (FOIA) /ESDN (CREST): CIA-RDP80T00246A002700060002-4
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• Document Creation Date: December 21, 2016
• Document Release Date: November 25, 2008
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1,ity, At fiteat applied to muscle, the same epprocch could
be 7SLr~~k ~~ ~)ubseauently to almost all knot n forms of biol
gioa1 ipjvement?
ENZYMOLOGY AND MECHANOCHE?IIISTRY OF TISSUES
W.A.ENGELHARDT (Moscow)
Orly one aspect of this problem will be considered here, that
of the enzymatic factors of the function of biological mots.
much wider soope a namely that of the role of eI zymes as i
tegral ?ewpouents of elementary physiological mechani +as?
The subject which it is intended to discuss here may be
regarded as a particular ogee of the biological problem of
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bviouo reasons It is with arAuocle that tie begin, Ade-
R00i,'etriPhor phate (ATP) has long ago boon recognized ca tho
Immediate source of energy for the performanoe of the work
Of musolee Retrospectively it appears puzzling that for a
cconaiderable length of time no attempt has been made to in.
vQ~itigate do nature of the interaction of ATP, ao bearer
of potential chemical energy, with the contractile substano?
Of muscle, its structural proteins, The study of muscle so-
1pity py seeded along two independent, completely separate
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lines. One of these lines was the, study of the metabolic
processes, wich finally provide the energy for muscular cont.
raction. The brilliant work of Meyerhof and Parnas, Joseph
and Doroty Needham, Carl and Gerty Cori, their teams, and
numerous other investigators had led to a detailed knowledge
of the metabolic processes in muscle. This knowledge appeared
almost exhaustive, and its main result was the above-mentioned
recognition of the role of ATP in the energetics of muscle.
The other line of research was the study of muscle pro-
teins. Danilewsky in Russia, Ktihne in Germany were among the
first to attack this field. Of fundamental importance were
the investigations of Edeall and Muralt, and of Weber about
the properties of myosin, unanimously regarded as the predo-
minant component of the contractile mechanism of the muscle
fiber. Later the discovery of actin by Straub was another sig-
nificant step in this field.
To everyone engaged in the study of muscle it has always
been evident that the work of muscle is the result of inter-
action between low-molecular, crystalloid products of the
metabolic changes going on in muscle, with the macromoleoular
protein substances which constitute the mechanical framework
of the muscle fibrill, its contractile mechanism. This state-
ment is almost a truism. Nevertheless, as already mentioned,
the two lines of study of muscular activity developed inde-
pendently, as if separated by a deep gap. The possibility of
overbridging this gap, of bringing the two lines of approach
to a close contact, arose from studies of enzymological oha-
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ranter. The enzyme, adenosinetriphosphatase (the conventional
name, ATPase will be used) was found to represent the link
which connects the biochemical and the mechanical events, res-
ponsible for muscular contraction,,
once this connecting link was revealed, it. became possible
to speak of "m e c h a n o c h e m 1 s t r y" as a new sphere
of research, where mechanical and chemical phenomena are stu-
died in their mutual interrelations, under the different as-
pects, associated with the performance of mechanical work,
as during muscular contraction, or with the various other
forms of movement in-biological objects.
ATPase is the enzyme which splits adenosinetriphosphate
and liberates the chemical energy, accumulated in its high-
energy (macroergic, as we call them) phosphate bonds. Thus
the motive force is furnished for the performance of mecha-
nical work. The study of this enzyme, which we undertook, in
collaboration with Dr Liubimova, led to the unexpected dis-
covery that the enzymatic activity belonged to myosin, the
protein which constitutes the basis of the contractile subs-
tance of muscle. On other words, the contractile substances
eatalixee itself the reaction which yields the enrgy for the
0 ontract ion.
The logical development of these studies was to investi?
gate whether ATP, the substrate of the enzymatic activity of
myosin, might not produce some changes of the physical proper-
ties of myosin itself, and thus lead to the mechanical effects,
associated with the processes of contraction or relaxation.
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Ezperiments of this kind weq :i,odo alQo,-t
in two different geographical pointy in Woeoou a d g r~) Cc -
bridge, and the problem was attacked on differ?nt l3ve10. our
group in Moscow (Engelhardt, Liubimove and Meitina) used
macro-systems - myosin threads as models of muscle fibers,
The experiments of the Cambridge group (Joseph and Doroty
Aeddham,Dainty, Kleinzeller, Shi Chang-,Shen and Lawrence)
were on the molecular level - with myosin solutions,. It is
on these two levels that the whole further research on the
biochemistry of muscular contraction, - or, as we may call it,
on the mechanochemistry or muscle and other objects, -proce-
eded and is still going on.
The results of the very first experiments were clear-
out and unambiguous. In both oases, in completely different
manners, profound changes of the physical properties of myosin
were observed under the influence of ATP,
In the experiments of the Cambridge group the effect
consisted in an instanteneous drop of viscosity of the pro-
tein solution, indicating profound changoo of molecular shape
of the protein particles. This effect deserves to be desig-
nated in the beiochemical literature as the "Needham effect",
because it is one of the most conspicuous effects in the
field of mechanochemistry, and has played a decisive role
in the study of muscle proteins, for the discovery of actin
in particular. On the other hand the experiments with myesln
threads initiated a series of ,numerous invest igatione in which
different kinds of "muscle models" were used, of increasing
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perfection and complexity: oriented or dehydrated (g.lyceri-
n ated) myosin threads, glycerinLted muscle fibrills or strips,
whole muscle preparations.
Two features of the mechanochemical machinery, as it
appears from the above-mentioned results, deserve to be
specially pointed out. First, the enzymatic nature of the
cortractile substance, and second - the reciprocal character
of the interaction of enzyme and sulstrate in this case. The
fact that myosin, when reacting with ATP as its substrate not
only produces a change of the substrate (as all enzymes do),
but at the same time itself undergoes characteristic chauiges
of its properties, prorated Needham to propose the admirable
designation of myosin as a "contractile enzyme", And conse-
quently it became possible to regbrd muscular contraction as
being "essentially an enzyme - substrate combination". We now
may say that these results were due to lucky chance, namely,
that at that time the methods of fractionation and purifica-
tion of muscle proteins were not as elaborated as they are
now. In fact, with highly purified myosin the experiments
would have been negative, for it is only when myosin is com-
bined with another substance (in muscle - with the other pro-
tein, actin, in the form of actomyosin) that directly obser-
vable changes of physical properties are produced by ATP.
When we "purify" myosin, separate it from actin, its
properties are changed: the catalytic aetivity'remains un-
affected, myosin is still an enzyme, but the contractility
is lost, myosin is no more a "contractile enzyme". This eta-
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tement should not be taken too rigorously. Some of our own
observations, with Dr.Kafiani, when threads of compressed
surface-spread myosin monolayers, according to Hayashi, were
used, as well as unpublished results of Dr.Cheesemam, in
London, who studied area /pressure diagrams of surface spread
myosin, both point to the possibility that even highly pu-
.rifled myosin, free of actin, still posseses a certain degree
of physical susceptibility towards ATP,But this question is
it is of minor impor-
can be left without .
"myosin* and *aotomyo-
indiscriminately,
instance ionic effects,
still far from being settled/ and as
tance for the present discussion, it
further consideration, and the terms
sin* will be used here in most cases
Evidently other factors, as for
also take part in the complex phenomena of musoular activity
or biological motility in general. But these are beyond the
scope of the present discussion and their nature is rar from
being sufficiently understood. But apart from the euzym?-
substrate type of reactions there is another important kind
which must be mentioned here. Whereas the enzyme-substrate
reactions represent interactions of low-molecular substances
with maoromolecuiar partners, the other type of reactions,
which seem to play an important role in mechanochemioal
phenomena, are those where maoromoleoular compounds Int-
eract with one another,,The prototype of such reactions has
already been mentioned - It is the reaction between myosin
and actin, the formation and dissociation of aotomyosin,
As will be shown later, there is already some evidence?that
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other substances as well may rem complexes with myosin,
influencing its properties in a manner which closely resemb-
lea the effect observed when myosin reacts with actin.
Returning to the purely enzymological side of the
problem, it must be stated, that the question whether myosin
itself is the ATPase, or the enzyme is a separate entity, only
bound to the contractile protein has been discussed lively
and during a considerable lenght of time. The main objection
seemed to be based not on convinving experimental evidence
but rather on a preconceived opinion which could be shemati-
c ally formulated thus: "There is so much myosin in muscle
that it cannot be an enzyme". The logic of the argument is
or the same kind as if one would insist that haemoglobin
cannot be a catalytically active protein because there is too
much haemoglobin in a blood cell. The verdict of time,that
most exacting judge in matters of science, has been decidedly
in favout of the identity of myosin and ATPase. The evidence
has been of two kinds, preparative and functional.
All attempts to obtain preparatively from myosin some
fraction where the enzymatic activity would be conbentrated
and the other characteristic properties of myosin (for
example its actinecombining property) would be absent, have
failed. Taking into account the difficulties and limitations
of the yet available methods of fractionation and separation
of proteins, only positive results are decisive. The value
of negative results, that Is-of the failure to separate a
presumed mixture into its components are of very limited
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value. Therefore much more weight has to be attributed to less
direct, but in this case more reliable, functional evidence,
based on the parallelism; or, on the contrary, independence of
the changes of the properties of the presumed separate compo.
nents of a complex under as different conditions as-possible,
Evidence of this kind is available, from different laborato-
ries,
Bailey and Perry were the first to show an almost exact
parallelism of the changes of ATPase activity and actin..
binding property of myosin preparations treated with the
thiol poison, iodosobenzoate.
My collaborator, Dr Iarovaia, in the Moscow University,
carried out'similer experiments, using a wider range of fac..
tore, affecting the enzymatic activity of myosin - heat de..
naturation, pretreatement at different pH, action of cadmium
and silver 'ions. An almost exactly identical behaviour of
enzymatic activity and of actin.-binding property was found,
In the work of Mrs Venkatern in our laboratory photochemical
changes of myosin have been studied, and here again a paral-
lelism between loss of enzymatic activity and decrease of
the actie..binding capacity was observed.
It would be a very strained interpretation indeed to
regard this as a mere coincidence, and to ascribe to two
separate proteins such a completely identical behaviour to-
ward so widely differing factors-as temperature,iH, thiol
poisons, photochemical action, The conclusion can only be
drawn that both properties belong to one and the same pro-
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tein, It is for this protein, possessing the ATPaee activity
and the property to combine with actin that the name of m y -
o a I n In the strict sense of the word etiould be reserved,
Not only, in the intact molecule of myosin, but even In
the primary products of its breakdown by a mild ac'tio'n of
proteolytic enzymes, in the "meromyosins" of Andrew Szent-
Gybrgyi, both abovementioned properties continnue to be
associated with one and the same fraction.
The mechanochemical effect- changes of physical properti-
es under the influence of ATP, - depends strictly on two con-
ditions: the enzymatic activity must be maintained, and myo-
site must be combined with a partner which imparts the necessa-
ry physical reactivity. In muscle the role of this partner
belongs to actin. But under experimental conditions actin
appears not to be the only substance which can produce the
said effect,
In suspensions of actomyosin gel or of finely dispersed
muscle fibrils ATP produces a marked effect of syneresis: the
particles shrink and when they are oentrifuaed the volume of - ~~
the sediment is considerably reduced; actin-free myosin gel
suspension does not show this effect. But it has been shown
by Ashmarin in Leningrad, that if mayosin Is treated with
certain dyes, for instance congo-red, the compound myosin-dye
behaves exactly in the same manner as does the complex myosin+
actin.
Syneeresis is not a phenomenon to which we could attri-
tute any signiricant role in the processes of muscular ac-
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tivity; and dyes are evidently far from being agents of bio-
l ogical nature. Duch more importance has therefore to be
attributed to recent experiments of Dr.Vorobjev, one of my
former pupils, in Leningrad. By adding native, non-depolime-
rized nucleic acid to a myosin solution, Vorobjev obtained
from such a mixture threads (we may call them "nucleo.-myosin
threads") of considerable strength, which when extended by
a load would contract anisodimentionally under the action of
added ATP, lifting the load and thus performing mechanical
work. This behaviour of the nucleo-myosin thread resembled
in all details that of glycerinated actomyos in threads ex-
tensively studied by Weber and his associates, The improtant
point is that the characteristic effect is observed only
as long as the enzymatic,_ATPase activity of myosin remains
unimpaired. Myosin solutions which have lost their ATP&se
activity will not yield mechanoohemically active threads.
Presence of calcium ions, which are known to be indispensib-
1 e activators of ATPase is also necessary for the meohanoche-
mical effect; in presence of the chelating agents EDTA (ethy-
lene-diaminotetraacetate) which removes Ca ions, the threads
do no more contract on addition of ATP; on the contrarya
they begin to extend under the load, because now the plas-
tifying effect cf ATP, found by Weber, becomes apparente
on addition of an excess of calcium, surpassing the molar
concentration of EDTA, the ATPase activity is reetorede
and the thread begins again to contract on addition of ATP.
This dernostrates unambiguously the fundamental role of the
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enzymatic property for the appearance of iechanochemictl
reactivity. Certain facts, which will be mentioned a little
later, seem to indicate that the formation of nucleomyosin
is perhaps not merely an experimental trick, but may actually
take the place of actomyosin formation in cases where actin
is absent in a certain kind of cells.
The nature of muscular. activity is a vast and extremely
multiform problem, where morphology and biochemistry, thermo.
dynamics and enzymology, energetics and colloid chemistry
are closely interconnected. I have - admittedly arbitrarily,.
selected a few aspects among this multitude, and outlined
them in a most schematic way. Muscle is the object, in which
living Nature has reached the utmost perfection in the trans.
formation of chemical energy into mechanical work and mOwe?
ment. But motility is one of the fundamental, most universal'
manifestations of life. Its forms are very diversified: pure-
ly protoplasmic flow, as observed in mywomycetes; ameboid
movement; intracellular movement during mitosis; movement
..f spirillae, flagellate bacteria, protozoa, animal and
plant sperm cells; eventually rapid movement is observed in
higher plants, for example in insectivorous species of Mimosa
pudica; and finally in the animal kingdom all the diversity
of muscular movement, from the very slow motion of plain
muscles to the enormous velocity in an insect wing.
The question can be raised: Nature elaborated completely
different fundamental mechanisms to produce each of these
very different forms of motion? Or are all these forms of
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movement based on some common, elementary principles? At fist
eight it may appear hardly probable that such profoundly-
dif-ferent types of motion, as for example ileggelar and muscular,
have anything in common from the biochemical point of view,
But it is exactly in the field of biochemistry that the idea
becomes more and more evident that elements of far-reaching
unity are. encountered along with the almost boundless di-
versity of living forms. Throughout the animate kingdom, to
its very extremes, from a bacterial cell to the brain tissue
of man, we find operating fundamentally identical metabolic
mechanisms, such for example as that of cellular respiration,
with all its complicated system of enzymes and coenzymes, in-
tricate cyclic reaction sequences, extremely refined acco paa-
nying phenomena responsible for the accumulation of energy
of oxydative processes in the form of high energy phosphate
compounds, and so on.
If this "unity among diversity' is firmly established in
the field of biochemical dynamics, it is not unreasonable to
expect that the same principle can be encountered in the
field of biological kinematics, in the sense that all the
diverse forms of biological motility have similar, common
to all of them, fundamental biochemical mechanisms, During
the last decade considerable experimental evidence in favour
of this assumption has accumulated, and it is intended to
give here a brief review of It.
But first it will be necessary to summarize the crits-
ria which can help us to decide whether similar mechanisms
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to the one of muscular contraction are involved in the uts.er
forms of motility.
Schematically these criteria are the following:
1) Analytical demonstration of ATP in the motile objects,
and cessation of movement as soon as the-store of ATP is ex-
hausted.
2) Demonstration of the presence of proteins, with pro-
perties resembling those of the "classical" contractile subs-
tance, namely myosin or actomyosin. The properties to be
looked for would be: a)susceptibility to physical changes
(viscosity,bire(ringence) under the influence of ATP;
b) contraction effects produced by ATP
c) ATPase properties of the protein.
3) Demonstration of kinematic effects, produced by the
application of ATP from the outside to the objects in their
native state or after mild treatment (yoerination)
4) Demonstration of.the presence of a sufficiently high
ATPase activity, and correspondence of the level of activity
with the motile efficiency.
Obviously, these different criteria are not equally reli-
able, especially when taken separately. The conclusions be-
come much more definite, if several independent criteria can
be satisfied.
With these considerations in mind, the question can be
discussed now, what experimental evidence is available, con-
cerning the oasic principles which govern the function of
motility in the different biological objects.
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Spermatozoa have been the object of our studies carrie
a d
out in collaboration with Dr.I3urnasheva
result have been brierly mentioned in a
the "Advances in enzymology). The sperm
ciable amounts of ATP. Under favourable
sis, presence of glucose) the ATP level
long periods. If the cells are deprived
The two fractions can readily be separate;' bye d if r
(some of the earlier
review article in
cells contain appre-
conditions (aeroblo-
remains constant over
or glucose and their,
respiration is stopped by removal of oxygen or by cyanide
poisoning, a steady decrease of the ATP content is observed,
and at the same time the motility falls.As soon as the ATP
store is exhausted the cells become motionless. When normal
conditions are restored, ATP is synthetized in the cells, and
at the same time motility reappears,
By treating sperm cells with solvents, used for the
extraction of myosin from muscles, a protein preparation has
been obtained, which resembled in several respects myosin.
The protein, for which the name "speraosin"was proposed, has
similar with myosin solubility properties, and possesses
an appreciable ATPase activity.
Burnasheva suoeeded in an elegant way to denonstx?ate
that both sperrnosine and the ATPase activity are localized
in the notile part of the sperm cell, in its tail. By expos-
ing spermstozoa to ecreful].y controlled mechanical treatment
in a blendor it has been possible to dissect the eellsobx-eak
off the tails from the nucleus-carrying head of the sperm,
centrifugation. It was the motile part of the sperm r?c.A.L,
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oe of the.energy-bearing metabolic product, ATP. This reac-
tivity appears only when myosin is combined with a certain
partner ? actin in nusole, a dye In Ashmarin's experiments,
mentioned, myosin, as such, when free of actin, does not
show the properties which we designated as mechanochemical
reactivity: changes of physical properties under the influen-
the tail, which contained practically the whole ATPase ac-
tivity found in the intact cells, and spermosine could be
obtained from this same fraction.
Attempts to obtain some kind of mechanochemical effects
with spermosin, as they are shown by actomyosin, were at
first unsuccessful. But the following experiment permitted
to obtain a positive .result in this respect also. As already
nucleic acid in those of Vorobjev, From sperm cells no pro-
tein with the properties of actin could be isolated, and
the negative results mentioned might have been due to the
absence of such an necessary partner for the spermosine
isolated from the cells. Now Ivanov in Moscow has shown very
clearly that the reaction between myosin and actin is comp
lately devoid of species specificity: myosin from one source
will react in exactly normal manner with actins prepared from
different animal species. Taking in consideration this
lack of specificity of the contractile proteins, Burnasheva
examined the possibility of combining spermosin with actin
prepared from muscle.
The results almost exceeded our expectations. Addition
of actin to the spermosin solution resulted in a consider-
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able increase of viscosity, of the same order as observed
in an experiment with myosin. When ATP is added to this mix-
ture, there is an abrupt drop of viscosity, again exactly
in the same manner, as observed in experiments with myosin.
It is evident that spermosin forms p complex with actin,
just as actomyosin is formed from myosin and actin. We may
call this complex aacto-spermosinn, in analogy with acto-
myosin.
No answer is so far available to the question- what subs-
tance takes the place of actin in the sperm cell to corm the
mechanochemically reactive complex with spermosin. The alrea-
dy mentioned experiments of Vorobjev with nucleic acid suggest
one possible answer to this question. The sperm call is ext-
remely rich in nucleic acid. Would not a part of it be used
in the cell not as carrier of hereditary information, but
as a component of the chemical machinery of the motor appara-
tus of the cell? But here we have to wait for furhter ex-
perimental results.
Attempts to restore the motility of spermatozoa which
had become motionless because of the exhaustion of the ATP
reserves or the cell by supplying ATP from the outside, in
the surrounding medium, remained unsuccessful. In experiments
of this kind only positive results are of value, as negative
ones may be due to the impermeability of the oell to the
energy-bearing nucleotide.
This explanation of the negative results of our experi-
ments is supported by observations on other types of yivi
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objects, possessing flagellar motion, as carried out by
Weber and his associates. They used flagellated protozoa,
t rypano es , and giant sperm cells of the sr_razhopper, Th
material was treated with carefully selected concentrations
of glycerol. This treatemeht removed low-molecular substances
and water-soluble proteins, whereas the structural proteins,
responsible for the movement of the flagella, being in the
gel state, remained undissolved. At the same time the permea-
bility; of the surface layers is profoundly changed, so that
the contractile mechanism becomes easily accessible to ATP,
applied from outside. Sich preparations, designated as
"flagellar models", perform regular movements when ATP is ap-
plied, even in the case when the flagella are broken off from
the body of the cell. As a pretreatement with glycerine was
necoesary to obtain this erfect, it may be concluded that the
negative result in our experiments was actually due to the
presence of a permeability barrier, which prevented the access
of ATP to the essential parts of the contractile apparatus of
the flagellae.
Summarizing the results obtained in the study of flagge-
lar movement, it can be stated that in this case almost all
of the criteria enumerated above are satisfactorily met.
A far-going similarity of the basic enzymatic and meohanoche-
mical factors of this type of motility and that of muscular
contraction may be regarded as firmly established.
Even the most primitive form of biological movement, name-
ly the flow of protoplasm in myxom:ycetes displays certain
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features in common with muscular motion. Fibrillar protein,
resembling in properties myosin, has been described in these
organisms, and ATP is involved in the processes of protoplas-
mic flow. Of great interest are the contribution of Weber's
group, in which different forms of cellular movement have been
extensively studied. Ameboid movement, contraction of fibro-
blasts, and even the most refined processes of displacements
of the chromosomal apparatus during the mitotic cycle have
been shown in these investigations to be in many respects
closely similar to muscular contraction, although the veloci-
ty differs by about three orders. Preparations of contractile
proteins have been obtained from motile cells, by methods
similar to those used for the isolation of myosin from muscle.
These proteins resembled actomyosin, as their viscosity de-
creased after addition of ATP, and they possessed ATPase
tivity; in gel form the proteins contracted when treated with
ATP. 1.7oreover, glycerinated "cellular models" have been pre-
pared, w;iich reacted by specific transformations on addition
of ATP The authors advanced the view, that from these primiti-
ve Proms of biological motion the highly specialized muscu'epr
mechanism has been developed in the course of evolution.,
Finally I will venture to make a step still further, and
leaving; objects o' animal origin, mention the observations of
my collaborator, Poglasov, who experimented with higher plants.
Here only one of the criteria which I mentioned has been ?i r
followed up, namely the distribution of ATPase act
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examined in a variety of plants, possesing motility and devoid
of this property.
It was found that the leaves of mimosa pudica posses a
high ATPase activity.Towards autumn or when kept in unfavour--
able conditions in the. laboratory the plants gradually loose
their motor reaction - the rapid folding of leaves when touched,
and this was accompanied by a marked decrease, sometimes almost
complete disappearance, of the enzymatic activity. Numerous
other plants that have been investigated, which do not possess
the motile function,exhibited very low, often scarcely detec-
table ATPase activity of the leaves. Even closely related
species, such as Acaoia,belonging to the same family, had hard-
ly perceptible activity. Only in one variety, which did not
display mobility, an appreciable ATPase activity of the leaves
was found, but still consirably less t1lan that observed in
Mimosa pudica. perhaps we have to deal here with a kind of
rudiment, in the sense that the enzymatic activity has remai-
ned while some other link of the motility mechanism was al-
ready lost,
Attemptp to isolate some specific protein from mimosa
leaves, which could be regarded as responsible for the motile
function, - some hypothetical "mimosin", - have so far failed.
A
This is not/stonishing, as the extraction of proteins in
their native state from leaf material is known to be a diffi..-
cult task, often hardly possible at all and usually involving
rather drastic treatement; and one of the most characteris-
tic properties of contractile proteins, at least those of
animal origin, is their extreme lability,
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 Approved For Release 2008/11/25: CIA-RDP80T00246AO02700060002-4
We clearly realize that the information obtained on
plant material is as yet very poor.perhaps I may close
my lecture with an invitation to our colleagues living in
warmer countries, and having at their disposal a much more
numerous and more readily accessible choice of *b.1o_
objects, to undertake corresponding experiments. perhaps
the idea of "unity among diversity" could thus obtain
further support.
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