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Kinetics of Hemoglobin-Carbon Monoxide Reactions Measured

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Kinetics of Hemoglobin-Carbon Monoxide Reactions Measured Proc. Natl. Acad. Sci. USA Vol. 74, No. 7, pp. 2620-2623, July 1977 Chemistry Kinetics of hemoglobin-carbon monoxide reactions measured with a superconducting magnetometer: A new method for fast reactions in solution (magnetic susceptibility/flash photolysis/metalloproteins) JOHN S. PHILO Department of Physics, Stanford University, Stanford, California 94305 Communicated by William M. Fairbank, April 25,1977 ABSTRACT A new technique for measuring fast reactions a superconducting quantum interference device (SQUID) in solution has been demonstrated. The changes in magnetic magnetometer that can sense very susceptibility during the recombination reaction of human small magnetic fields. It is hemoglobin with carbon monoxide after flash photolysis have primarily the very low noise and fast response of the SQUID been measured with a new high-sensitivity instrument using magnetometer that make kinetic experiments possible. cryogenic technology. The rate constants determined at 200 (pH The instrument may be operated in two modes. To measure 7.3) are in excellent agreement with those obtained by photo- the total susceptibility of a sample, the change in magnetometer metric techniques [Gray, R. D. (1974) J. Biol. Chem. 249, 2879-2885]. A unique capability of this new method is the de- output is recorded as the sample is inserted into the sensing coil. termination of the magnetic susceptibilities of short-lived re- In this mode, the instrument can resolve a change in volume action intermediates. The magnetic moment of the intermediate susceptibility* of 9 X 1012, which is equivalent to a change of species Hb4(CO)3 was found to be 4.9 ± 0.1 jtB in 0.1 M phos- 0.0001% of the susceptibility of a typical diamagnetic sample phate buffer by partial photolysis experiments. This value agrees (such as a protein in solution). This is an improvement of about with the predictions of two-state allosteric models of coopera- two orders of magnitude over vibrating sample, force, or other tivity in hemoglobin. Possible applications and improvements SQUID systems. The system is calibrated with a sample whose in this technique are discussed. susceptibility is known. In the second operating mode, the Magnetic susceptibility measurements have often been used sample remains fixed within the sensing coil, and changes in by chemists and biochemists to probe the electronic states of susceptibility due to chemical reactions, temperature changes, transition metal ions. Such measurements can yield information etc., are measured. This mode was used for these kinetic ex- on the symmetry and strength of ligand fields and the oxidation periments. The system response time is 300 us. For kinetic ex- state of the ion, as well as on the strength of interactions between periments, the susceptometer is characterized by a white noise clusters of ions. Magnetochemical methods have been partic- spectrum above 5 Hz with a rms level of 1.1 X 10-11 (Hz)-1/2, ularly helpful in studies of metalloproteins and of synthetic or a concentration of a spin 'k species of 0.70,uM(Hz)-1/2. The analogues of their active sites. present sample Dewar configuration permits sample temper- The power of many physical techniques has been greatly atures in the -5 to 100° range; low-temperature experiments extended by their use in kinetic studies to measure reaction rates are possible with slight modifications. Sample temperature may and the properties of intermediate species not present in be regulated to +0.0010. This instrument will be described in equilibrium. However, conventional magnetic susceptibility detail elsewhere. instruments generally lack both the sensitivity and time reso- Flash Photolysis Experiments. For these experiments, the lution necessary for measuring fast reactions in solution. In our HbCO solution is placed in a cylindrical quartz bulb (0.30 cm3) laboratory, we have been applying superconducting technology which is placed within the sensing coil for the duration of the to construct a very-high-sensitivity magnetic susceptibility experiment. A Lucite rod serves as a light pipe to carry the instrument for research in biophysics and chemistry. In addition photolytic flash to the sample. A commercial photographic flash to higher precision and sensitivity for equilibrium measure- unit was used with a flash input energy of 50 J and a pulse du- ments, we hoped through this approach to achieve sufficient ration of 1 ms. Up to 80 mj of visible photons reached the time resolution for kinetic measurements. This paper reports sample. The susceptibility changes after the flash were recorded measurements of the kinetics of the reaction of human adult on a digital signal averager. The interval between flashes was hemoglobin with carbon monoxide and a measurement of the 20 s, and usually 32 or 64 transients were averaged. The system magnetic moment of an intermediate in this reaction. time constant could be varied upward from its lower limit of 300 jss and was normally set at 1 ms. All experiments were done MATERIALS AND METHODS at pH 7.3 and 20' ± 0.1'. Data Analysis. Because the iron in HbCO is diamagnetic and Magnetic Susceptibility Instrument. The essential elements in Hb it is paramagnetic (S=2), the changes in magnetic sus- of the magnetic susceptometer are indicated in Fig. 1. The ceptibility are directly proportional to the change in Hb con- samples are placed within a room temperature Dewar flask and centration.t In all these experiments, at equilibrium the Hb is are magnetized in the homogeneous field (0.43 T) of a super- conducting electromagnet. The sample's magnetization pro- * Note that SI units are used here; to convert to cgs units, divide by duces changes in the magnetic field at a superconducting 4ir. sensing coil. These magnetic field changes are transmitted to t Strictly speaking, the proportionality holds only if the magnetic moment of each heme is independent of the ligation state of the Abbreviation: SQUID, superconducting quantum interference de- others. This is not always true (see Results), but this is a small effect vice. and may be ignored for most purposes. 2620 Downloaded by guest on September 25, 2021 Chemistry: Philo Proc. Natl. Acad. Sci. USA 74 (1977) 2621 AK= 5x101 C,, VACUUM ROOM TEMPERATURE 040 80 100 ~~~~~~~~~160 SPACE z 0 40 100 TIME AFTER FLASH (ims) FIG. 2. Magnetic susceptibility changes after flash photolysis of HbCO. The scale in SI volume susceptibility units is indicated by the vertical segment. The initial negative offscale change is an experi- mental artifact (see Results). Total [Hb] = 38.5 MM; [CO] = 130 AM; 0.1 M phosphate, pH 7.3; 20°. Average of 64 transients. System time constant = 1 Ms. FIG. 1. Schematic cross section of magnetic susceptometer. from the error matrix and the estimated uncertainties Xm and with and is therefore The [CO]eq. fully saturated CO diamagnetic. the the entire reaction change in susceptibility from its equilibrium value was con- For partial photolysis experiments verted directly to Hb concentration by using the known molar record was used, and it was assumed that the dimers and susceptibility difference between Hb and HbCO in the buffer Hb4(CO)3 intermediates react at the same rate. These experi- used (1). ments were conducted at very low [CO]eq (small A), and K(0) rate of Hb with CO after and the fraction e'/Xn were treated as adjustable parameters. The of recombination photolysis The dimers were assumed to have the same molar susceptibility was analyzed to find an effective value for e', the rate constant for the forward reaction. Such an analysis is complicated by the as do free chains. dissociation of 20-30% of the Hb tetramers into dimers at the Sample Preparation and Reagents. Human Hb A was pu- from whole blood and was concentrations used in these experiments (2). Further, as a rified by the toluene procedure (3) on a G-25 filtration consequence of heme-heme interaction, the apparent value stripped of organic phosphates Sephadex gel column. The fraction of MetHb was initially less than 1%. of e' increases with fractional saturation. However, the primary was obtained from Chemical purpose of these was to demonstrate the validity 2,3-Diphosphoglycerate Sigma experiments was to of the new technique. Therefore, for purposes of comparison Co. as the pentacyclohexammonium salt and converted with the rate constants obtained by spectrophotometric tech- the free acid on a Dowex 50W X 8 (H form) column. 2,2- (Bis-Tris) was niques by Gray (2), a constant value for over the final 70% Bis(hydroxymethyl)-2,2',2"-nitrilotriethanol of the (tetramer) reaction has been assumed. Over this range, obtained from Aldrich Chemical Co., purified sodium di- T. the fast dimer reaction has already gone essentially to com- thionite from J. Baker Chemic4l Co., and CO from Liquid pletion. Because the pseudo-first-order criterion [CO] >> [Hb] Carbonic Corp. were was not always met in these experiments, the more general Solutions containing CO prepared by diluting buffer second-order formulation was used. Differences between the saturated with CO at atmospheric pressure at 200 with de- oxygenated buffers, assuming a CO solubility of 1.0 mM. A few a and f# subunits have been neglected. The rate of HbCO dis- sociation is very slow and therefore the back reaction may be grains of sodium dithionite were added directly to the syringe neglected. The kinetic equations therefore become: used to fill the sample bulbs to remove residual dissolved 02- Heme concentrations were measured in a Beckman DK2-A [Hbk [1] the extinction of [Hb]o exp ff'[CO]eq t} spectrophotometer by using coefficients [Co]t [Co]o Banerjee et al. (4). in which the subscripts refer to concentrations at times 0 and RESULTS t and at equilibrium. If CO is in great excess, its concentration remains essentially constant, the denominators in Eq.
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