obtained. Serie8 I. ph=7-35. Temperature=00-30'. Into one of two large test-tubes were measured 5 c.c. of a 10 per
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1 THE TEMPERATURE COEFFICIENT AND THE APPARENT ENERGY OF ACTIVATION OF THE ENZYMATIC HYDROLYSIS OF ARGININE; WITH ADDITIONAL OBSERVATIONS UPON THE STABILITY OF ARGINASE UNDER VARIOUS CONDITIONS. By ANDREw HUNTER. From the Institute of Physiology, University of Glasgow. (Received for publication 23rd March 1934.) As a matter partly of theoretical, partly of practical, interest the temperature coefficient of the arginine-arginase reaction has been studied over a range of 00 to 500 C. and at two levels of hydrogen ion concentration-at or near the neutral point (within the range of maximum stability for the enzyme) and at or near a ph of 9-8 (the point of its maximum activity). Out of many relevant observations, made at different times and with different enzyme preparations, the four series described below suffice to exhibit the character of the results obtained. Serie8 I. ph=7-35. Temperature=00-30'. Into one of two large test-tubes were measured 5 c.c. of a 10 per cent. extract of dried liver powder in 50 per cent. glycerol; into the other 2 c.c. of an approximately 12 per cent. solution of arginine hydrochloride and 15 c.c. of a 0-25 M phosphate buffer solution of ph 7-8. By immersion of the tubes in a large bath of melting ice their contents were cooled to 0, whereupon, at a given instant, they were rapidly and thoroughly mixed. The mixture was at once returned to the icebath, and the tube containing it was closed by a stopper carrying a 5 c.c. pipette. To prevent too rapid melting of the ice the bath was placed in a refrigerator at 4. At appropriate intervals 5 c.c. of the mixture were transferred by the pipette to a "urea tube" containing, for the immediate inactivation of the enzyme, 5 drops of concentrated HCI. The sample was then boiled, cooled, and neutralised; and its urea content was determined by the urease method of Van Slyke and Cullen. The details of the technique employed have been described in a previous paper (1). Experiments at 100 and 200 were carried out in a similar way in electrically controlled water thermostats.
2 178 Hunter In the experiment at 300, for which also a water thermostat was employed, the procedure was modified in such a way as to avoid any risk of causing a partial heat-destruction of the enzyme before it was brought into contact with its substrate. The arginase solution itself was kept at 200, while, following the indications obtained in preliminary trials, the substrate was raised initially to a temperature of The mixture of the two assumed almost immediately the desired temperature of 300. The ph (at 200) of such a mixture as was used throughout this series was determined electrometrically, and found to be Its arginine concentration was ascertained by mixing 2 c.c. of the arginine solution with 20 c.c. of water, and estimating according to Kjeldahl the nitrogen content of 10 c.c. This was found to be mg., so that the quantity of substrate in each 5 c.c. sample, expressed in terms of potential urea nitrogen, was 7-62 mg. Series II. ph = Temperature = In Series I. the reaction velocity at 300 was already as great as could be conveniently and accurately measured. To observe the effects of still higher temperatures it was necessary to reduce the concentration of the enzyme. Experiments at 300, 400, and 500 were therefore carried out, in which the enzyme solution of Series I. was diluted five times with water, the other materials and the quantities remaining as before. The technique followed was that of the previous experiment at 300. In no case was the enzyme heated above 20 before the moment of contact with the substrate. The results of these first two series are shown in Table I. as well as graphically in figs. 1 and 2. In the table velocity coefficients (k) for each temperature have been calculated according to the empirical a formula kt = m log - x, in which a, t, and x have the usual signia -x fication, and m is an arbitrary constant (1). In Series I. m was taken as 20-8, in Series II. as 18-8; the data employed for the derivation of these values are indicated in the table by square brackets surrounding the corresponding values of k. Since the formula fits, as a rule, only the first half or so of the actual velocity curve, values of k corresponding to x values greater than, say, 4 0 are to be neglected. It will be seen that, subject to the restriction stated, k is practically constant at any one temperature up to 300. The curves of fig. 1 have been drawn not with reference directly to the experimental points, but by the use of the equation and the average values of k. The points fall on each curve almost as exactly as if it had been drawn through them deliberately. At 400 in Series II. k is no longer even approximately constant, but diminishes steadily as the reaction proceeds. This is an indication
3 Temperature Coefficient of Enzymatic Hydrolysis of Arginine 179 TABLE I.-RESULTS AT PH 7*35. (SERIES I. AND II.) Series I. Series II. o E- o (a=7-62; Qio. X o 4. (a 7-62; Q1 0 E m =20-8). 0 0 m 18 ). -~~~~~ ~k -~k [0-142] loo! O [0-142] * j J [0-191) ) ) 0249* [0-191] '-0.385*.? l l ~ l * Initial value, as estimated by graphical extrapolation. that the enzyme is now suffering heat inactivation, an effect still more conspicuous in the greatly accelerated fall of k to be observed at 500. In such circumstances an average value of k would have no meaning. On the other hand, its initial value would reflect the accelerating effect of heat upon the reaction without complication by any concomitant destructive effect upon the enzyme. The initial value is not open to direct observation, but it may be estimated by plotting k against t and extrapolating to zero time. At 400 the resultant graph is a straight line, and the initial value given in the table cannot be seriously in error. At 500 the extrapolation is much less certain, and the result can only be offered as an approximation. It is possible that in Series II. heat inactivation was already to some extent in progress at 30 ; such, at any rate, might be the explanation of the fact that to obtain, even at this one temperature, a constant k it was necessary to use in the formula a value of m different from that which fitted the data of Series I. But destruction of the enzyme in nearly neutral solution at 300, and even destruction at 400, seem
4 180 Hunter at first to be inconsistent with the results of Hunter and Dauphinee (2), who found neutral arginase to be stable at 37. The probable explanation is that in the earlier experiments the enzyme was exposed to heat in greater concentration than in the present ones, and for a period not exceeding one hour. Under such conditions a slow destruction might easily escape detection; while, as the concentration of enzyme was diminished and the period of observation prolonged, it would HoURS 2 4 G 8 to FIG. 1.-Time-curves of Series I., at ph 7*35. Each curve is drawn to represent the equation kt = 20-8 log a- x, using for k the average values given in Table I. a -x become proportionately conspicuous. Confirmation of this explanation will be found in a later experiment. The actual time-course of the enzymatic reaction at any temperature depends naturally upon the balance between the two opposing effects of heat. Up to 400, as the graphs show, acceleration is either the only or the preponderating effect; but at 500 destruction has become so rapid, that after the first 90 minutes or so the rate of hydrolysis is actually lower than it is at 400. The extent of the destructive effect is made further evident in fig. 2 by the inclusion, along with the actual velocity curves, of dotted curves showing the course that would have been followed by the reaction, had the initial velocity coefficients been maintained throughout. From the average or initial velocity constants found temperature coefficients (Q1o) have been calculated, and are shown in the table, for each 100 interval from 00 to 500. It must be admitted that coefficients
5 Temperature Coefficient of Enzymatic Hydrolysis of Arginine 181 obtained in this way are still, in one respect at least, subject to correction. All measurements of reaction velocity have been represented as carried out at the same ph of This is not strictly true, for the Mqms. Urea. I 1 1 I N ( 1 (40 ) - 1WX I ~~I I Hours FiG. 2.-Time-curves of Series II., at ph The curve for 300 and the dotted curves for 400 and 500 represent the equation kt = 18-8 log_ - x, where k is the initial (for 300 the average) velocity coefficient given in Table I. The continuous curves for 400 and 500 are drawn through the experimental points, and represent the actual course of the reaction. ph must have varied with the temperature. The effect of this variation upon the calculated values of the coefficients cannot, however, have been very great, and in what follows it will be treated as negligible. 14 Series III. ph = Temperature = This series of experiments was designed to test the influence of temperatures varying from 00 to 400 at a ph close to the optimum of 9.8. The general plan was the same as that adopted in the first two VOL. XXIV., NO
6 182 Hunter series, but the buffer used was a phosphate-phenolsulphonate mixture of the kind employed previously by Hunter and Morrell (1), the arginine salt was added in the form of a 9-6 per cent. solution, and the enzyme lqms UreN I II Nf I Ire ^ Hours FIG. 3.-Time-curves of Series III., at ph The curves for 00, 100, and ~~~~~~~~~~~~~~~~a 0 200, and the dotted curve for 300, represent the equation kt =21-1 log -x, a-x where k has the average (for 300 the initial) value given in Table II. The continuous curves for 300 and 400 are drawn to fit the experimental points. No theoretical curve is drawn for 400, since the initial value of k at that temperature is too uncertain. extract was prepared from a different and less active sample of liver These components were mixed in the proportions of 15 c.c., powder. 3 c.c., and 5 c.c. respectively. The resulting mixtures had a ph (measured at 200) of Each contained, in 5 c.c., arginine equivalent to 8-24 mg. of urea nitrogen, as determined in this instance by the arginase method of Hunter and Dauphinee (3). Their arginine concentration was therefore higher, while their arginase content was lower, than in Series I. The five needful experiments of this series had to be spread over
7 Temperature Coefficient of Enzymatic Hydrolysis of Arginine 183 a period of twelve days; but, in order to make sure that the activity of the enzyme had not diminished during that interval, an extra experiment at 20 (making six in all) was performed eight days after the first. The two showed a sufficient measure of agreement, the second indicating actually a slightly greater degree of activity in the enzyme than the first. The results, including both experiments at 200, are exhibited in Table II. and fig. 3. The velocity and temperature coefficients of the TABLE II.-RESULTS AT PH (SERIES III.) Reaction M.ue Tempera. time in Mgun. urea0n ture. hours. (X.) (a =8-24; m=21-.1). (t.) 3* } * [0-128]) 10-5* [0-128] J T2*34 ( P I ~~3.0 (} o J 22. ~2 42 l ] J ~~39620j4' * IJ * Initial value, as estimated by graphical extrapolation. table were calculated in the same manner as before. The value of m (21.1) used in the computation of k yields, it will be seen, constant values for temperatures up to 20. This constancy, dependent as it is upon an entirely arbitrary choice of m, conceals the fact, already demonstrated (1, 2), that even at room temperatures the enzyme undergoes at ph 9-8 a spontaneous inactivation; but it may be taken
8 184 Hunter to show that the inactivation caused by excess of hydroxyl ions is not, within the range of temperature in question, appreciably accelerated by heat. The values of Q for 00 to 200 may therefore be accepted as expressing the full accelerating influence of rise of temperature upon reaction velocity. At 300 it is obvious, from the rather rapid fall of k, that the rate of destruction of the enzyme has now greatly increased; but, as the fall is almost exactly linear in relation to time, it is possible to estimate graphically an initial value, and therefore to calculate Q for At 400 the speed of destruction has become so great that this is no longer feasible. It will be noted that the inactivating effect of any given temperature at ph 9-85 is roughly equivalent to that of a temperature 100 higher at ph The destruction of arginase at 400 was actually so rapid in this series, that the amount of urea produced within the first 30 minutes was already less than it had been at 30. Even at 300 the rate of destruction was relatively high; for, when the velocity curve for that temperature is compared, as in fig. 3, with the curve for 200, it is evident that from the fourth or fifth hour onward the two are converging, and that after fourteen hours or so urea production at the lower temperature will surpass that at the higher. In a later experiment (see fig. 4) the crossing of the curves for 300 and 200 at a high ph is seen to take place even earlier-about the sixth hour. Not only do these observations confirm those of Hunter and Dauphinee (2) upon the ready destructibility of arginase by heat in media of high ph, but they exemplify the difficulty, and indeed the impossibility, of singling out any particular temperature as the " optimum." An optimum temperature can, in fact, be spoken of only with due reference to the concentrations of enzyme and substrate, the degree of hydrolysis to be accomplished, and other circumstances. At ph 9-8 the optimum for most conditions will be lower than 400, and for many lower than 300. At ph 7-4 it is less readily influenced, and will in most circumstances lie not far from 400. As there is no absolute optimum of temperature, so likewise is there no absolute optimum of ph. This was pointed out in an earlier paper (1); to which may now be added, that the higher the temperature the more strikingly does the relative meaning of optimum ph become manifest. An instance in point will be found in fig. 4, which, although dealing with a later experiment, may conveniently be referred to here. The graph shows, e.g., that the production of 5 mg. of urea N at 200 would be accomplished much more rapidly at ph 9 6 than at 7*1; whereas at 300 the degree of hydrolysis specified would evidently be reached sooner at 7-1. Such considerations as these have a practical application in the use of arginase for the determination of arginine. Here the object is to effect a complete hydrolysis within a reasonable time. Obviously a
9 Temperature Coefficient of Enzymatic Hydrolysis of Arginine 185 ph of 9-8 and a temperature of 40, or even 300, would provide conditions quite unlikely to accomplish this aim: the enzyme would probably be completely inactivated before the whole quantity of substrate could be hydrolysed. On the other hand, at room temperature and ph 7 the enzyme would be perfectly stable, but hydrolysis would be inconveniently slow. The combination of a temperature of 370 and a ph of about 8-4, recommended by Hunter and Dauphinee (3), offers a compromise, which in practice has been found entirely suitable. Whether it represents the best compromise possible could only be settled by a much longer series of experiments than the present. Series IV. ph=7.1 and 9-6. Temperature_ The temperature coefficients obtained at ph 9-85 were decidedly lower than the corresponding ones at ph Unfortunately the two sets of observations had not been made under identical conditions of enzyme and substrate concentration, buffer composition, etc. The possibility existed, therefore, that the ph factor was not the only one responsible for the differences found. In order to clarify this point experiments were performed in which ph and temperature were the only variables. The ph levels compared were, as before, in the neighbourhood of the neutral and the optimum points respectively. At each of these a determination of reaction velocities at two temperatures only would suffice, it was felt, to settle the question. Series IV. is representative of the experiments made upon this plan. The technique followed was the same as that of Series III. The arginine solution was of slightly lower concentration, so that the amount in each specimen (determined by the arginase method) corresponded to only 7i846 mg. of urea nitrogen. The enzyme solution (a diluted extract of fresh liver) was rather more active than that of Series III., but only about one-fourth as active as that of Series I. The ph of the two mixtures made up was 7-10 and 9-60 respectively. The results appear in Table III. and fig. 4. The data for ph 7-1 indicate, as will be seen, a slow yet unmistakable inactivation at 300, associated here, as in Series II., with a rather low concontration of enzyme. There is no difficulty, however, in extrapolating the values of k to zero time, and securing a reliable value for Q. At ph 9-6 velocity coefficients, if calculated by the formula which fits the data at 7-1, fall so rapidly, even at 20, that the accurate estimation of initial values is quite impossible. This fall is in accord with previous experience, and expresses doubtless the destructive effect of excessive alkalinity (1). To make possible under these circumstances an estimate of the relative initial velocities at 20 and 30 it is necessary to use in the calculations such a value of m as will make k at 200 reasonably constant. When this is done (see the tenth column of the table), we
10 186 Hunter TABLE IL. RESULTS AT PH 7-10 AND PH 9-6. (SERIES IV.) A. ph B. ph = j (a7(a-7846). (a 7846; Q_0. Q10 3to 24-4). 4;1 _ '4- - -_ "e=^4 0 ~~~~~~~ 0 to ~~~~~~~~~~24-4. to [0186] ' l035 [0 401]l ii50l ) 0426 i ? '? ) *42 il 0) * *4296 * J 00 10, * : , * 2 * ) *7 68 * J * Initial valute, as estimate(l by graphical interpolation. have a situation similar to that in Series III. and Table II. At 30 k still presents a rather rapid fall, due to the accelerating effect of the 100 rise upon destruction; but the values can be extrapolated with little uncertainty to The procedure is of course quite arbitrary, and the initial k values so obtained have no evident physical significance; but, as they are proportional to the initial velocities, they can be utilised for the calculation of a temperature coefficient. It will be seen that the two coefficients here found for the interval at ph 7 1 and 9 6 are not very different from the corresponding ones in Table I. and Table II. respectively, and, further, that the ratio which one bears to the other is practically the same for the later pair (1P21) as for the earlier (1.27). It would seem, therefore, that for the temperature interval in question, and presumably for other intervals also, other factors than ph have had little, if any, influence upon the temperature coefficients. The values found in the four different series of experiments are accordingly comparable. To facilitate the comparison all values of Q1o reported have been assembled in Table IV. In the same table are shown also the apparent energies of activation (E), in calories per gram-molecule, calculated from the temperature - coefficients bv the famiiliar equation E =lnq10 RT 2 The collected results thus shown call for little further cominent. Very similar results have been reported for a number of hydrolytic enzymes (4). As usual the temperature coefficient falls with rising temperature. Between 10 and 30 at ph 7335 this fall appears to obey the law of Arrhenius, so that the calculated energy of activation
11 Temperature Coefficient of Enzymatic Hydrolysis of Arginine 187 within this interval is constant. With this exception the energy of activation, following the general rule for enzymatic reactions, diminishes as the temperature increases. Temperature coefficient and energy of activation are seen to be dependent also upon ph, being smaller, HOURS FIG. 4.-Time-curves of Series IV. The 0 points were obtained at ph 7-10, * points at At ph 7-1 the 200 curve and the dotted curve at 30 follow the a equation kt =24-4 log -x. For the dotted curves a at -x ph 9-6 the arbitrary constant of the equation has been altered to The values assigned to k are the average or initial ones shown in Table III. for any one interval, at the optimum ph than near the neutral point; and, if one may take the four sets of values for as of equal reliability, they increase the more, the further (on the acid side) the optimum is departed from. In this respect the behaviour of arginase would be analogous to that of saccharase. For this enzyme the variation of the apparent heat of activation with ph was explained by Nelson and Bloomfield (5) as the consequence of a shift, with changing 12
12 188 Temperature Coefficient of Enzymatic Hydrolysis of Arginine TABLE IV.-TEMPERATURE COEFFICIENTS AND ENERGIES OF ACTIV-ATION. temperature, of the position of the ph-activity curve. That a similar shift occurs with arginase is probable enough, but has not yet been demonstrated. SUMMARY. The temperature coefficient of the arginine-arginase reaction at a ph of 7-35 varies from 2-70 for 0-10 to about 1-54 for At ph 9-85 it is smaller, and falls from 2-34 for 0-10 to 1-73 for The calculated energies of activation corresponding range fromn 15,200 to 8660 and from 13,000 to Incidental observations have emphasised the great lability of the enzyme, and particularly its susceptibility to heat, in alkaline media. Its relative stability near the neutral point has been confirmed, although even there it has been found to undergo gradual destruction at temperatures as low as 300. REFERENCES. (1) HuNTER, A., and MORRELL, J. A. (1933). This Journal, 23, 89. (2) HUNTER, A., and DAUPHINEE, J. A. (1933). Ibid., 23, 119. (3) HUNTER, A., and DAUPHINEE, J. A. (1930). J. Biol. Chem., 85, 627. (4) WAKSMAN, S. A., and DAVISON, W. C. (1926). Enzymes, Baltimore. (5) NELSON, J. M., and BLOOMFIELD, G. (1924). J. Amer. Chem. Soc., 46, 1025.
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