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Circular Polarization of Fluorescence of Probes Bound to Chymotrypsin

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Circular Polarization of Fluorescence of Probes Bound to Chymotrypsin Proc. Nat. ASad. Sci. USA Vol. 69, No. 3, pp. 769-772, March 1972 Circular Polarization of Fluorescence of Probes Bound to Chymotrypsin. Change in Asymmetric Environment upon Electronic Excitation* (circularly polarized luminescence/proteins/fluoresent probes) JOSEPH SCHLESSINGERt AND IZCHAK Z. STEINBERG Chemical Physics Department, Weizmann Institute of Science, Rehovot, Israel Communicated by Harold A. Scheraga, January 13, 197S ABSTRACT The circular polarization of fluorescence excited. The site, strength, rigidity, and geometry of binding is related to the conformational asymmetry of the emitting of a fluorescent probe to a protein molecule may thus molecule in the first singlet excited state in the same way differ that circular dichroism is related to the conformational in the ground and excited states. The use of fluorescence asymmetry of the absorbing molecule in the electronic for the study of the binding and the environment of the ground state. By measurement of these optical pheno- chromophore in the ground state, therefore, involves the mena, the induced asymmetry of two chromophores bound basic assumption that in the case under investigation no to chymotrypsin (EC 3.4.4.5) when in the ground state Was compared with the induced asymmetry of the ligands major changes have occurred in the bound chromophore when in the excited state. The two chromophores studied upon electronic excitation. Detection and examination of such were 2-p-toluidinylnaphthalene-6.sulfonate (TNS), bound changes is therefore of much interest and importance. at a specific site which is not the active site of the protein, In this study, the changes in the interaction of a protein and an anthraniloyl group, bound at the active site of the molecule and an attached extrinsic chromophore caused by enzyme. Both chromophores showed a change in induced asymmetry upon electronic excitation, the effect being electronic excitation of the chromophore are followed by the particularly large in the case of the TNS chromophore. optical rotatory power of the chromophore in the ground It is thus concluded that the orientation of TNS in the state and the excited state. Asymmetric molecules or chromo- binding site, its freedom of rotation in its site, the strength phores situated in an asymmetric environment are, as a rule, of binding, or even the site of binding of the dye to the protein might have changed upon electronic excitation. circularly dichroic, i.e., they absorb left-handed and right- handed circularly polarized light to different extents. In Fluorescent small molecules bound to proteins are useful as other words, the probability of transition from the ground probes in the study of the structure of proteins. Thus, the to the excited state differs when such molecules or chromo- intensity and spectrum of emission of various fluorescent phores are exposed to right-handed or left-handed circularly dyes have yielded invaluable information concerning the polarized light. An absorption band is circularly dichroic degree of polarity of the sites at which the dyes are bound if the relevant excitation involves both an electric and a (1, 2). Similarly, the extent of linear polarization of the light magnetic transition dipole moment and if the two transition emitted by dyes bound to proteins has been used for the moments are not orthogonal in space (7). Analogously, when investigation of the rotational diffusion of the protein mole- the above conditions are fulfilled for a radiative transition cules, or of segments of the molecules, and has thus allowed from an excited state to the ground state, i.e., in luminescence, deductions concerning the size and rigidity of the macro- the light emitted by the luminescent molecules in solution molecules (2-4). will be partly circularly polarized (7, 8). If the absorption In the interpretation of fluorescence data in terms of and emission processes involve exactly the same pairs of molecular structure one should be aware of the fact that the quantum states, the extent of circular dichroism (CD) and the fluorescence emitted by a chromophore is related to, and degree of circular polarization of the luminescence are related yields information about, the electronically excited chro- to each other by a simple expression (see below). It may be mophore (5, 6). It is well known that molecules in the excited recalled that, with few exceptions, fluorescence involves a state may have both physical and chemical properties that transition between the same pair of electronic states (Si -- So) are markedly different from those of the molecules in the as the absorption process in the long-wavelength absorption ground- state. Though short (about 10-9-10-7 sec for fluores- band (So SO). The vibrational states involved and the cence), the lifetime of the molecules in the excited state is positions of the nuclei are, however, different in the two still long enough to allow many reactions and conformational processes. Changes in the conformation or environment of an changes to take place during the period the molecule is optically active chromophore are thus readily disclosed by a comparison of the CD of the chromophore and the circular Abbreviation: TNS, 27p-toluidinylnaphthalene-6-sulfonate. polarization of its fluorescence. Circular polarization of * Presented in part at the 41st Annual Meeting of the Israel fluorescence emitted by systems of biological interest has Chemical Society, October 1971. apparently not been reported before. t Part of Ph.D. thesis to be submitted by J. Schlessinger to the Haugland and Stryer have prepared an anthraniloyl Feinberg Graduate School, The Weizmann Institute of Science; derivative of a-chymotrypsin (EC 3.4.4.5) in which the Rehovot, Israel. attached chromophore is covalently bound at the active site 769 Downloaded by guest on September 29, 2021 770 Biochemistry: Schlessinger and Steinberg Proc. Nat. Acad. Sci. USA 69 (1972) of the enzyme (9). This derivative was used to study the amplified and monitored. Full details of the instrument and rotational diffusion of a-chymotrypsin by the measurement the procedures for its calibration are described elsewhere of the linear polarization of the anthraniloyl fluorescence (9). (12). The spectral bandwidth for the excitation beam was McClure and Edelman have prepared another derivative of 30 nm, while the spectral resolution of the emitted light was a-chymotrypsin in which 2-p-toluidinylnaphthalene-6-sul- 15 nm. fonate (TNS) is bound noncovalently at a specific site, The protein solutions were deaerated by purified nitrogen which is not the active site (10). From the intensity and prior to the measurements of circular polarization of the spectrum of the fluorescence of the dye attached to the protein, luminescence and were kept under nitrogen in a hermetically it was deduced that the binding site is hydrophobic. The closed fluorescence cell during the measurements. The asymmetry induced in' these chromophores upon binding is exclusion of oxygen was necessary since the intense and reported herewith. Changes in the induced asymmetry of the continuous illumination of the solutions caused a decrease anthraniloyl and TNS chromophores were observed upon in fluorescence if oxygen was present, probably as a result electronic excitation of these chromophores, the change for of some photooxidation reactions. The deaeration was the TNS chromophore being particularly large. performed in the apparatus shown in Fig. 1. The solvent MATERIALS AND METHODS (and TNS in the studies of the chymotrypsin-TNS complex) was placed in the flask (A), and a weighed amount of protein a-Chymotrypsin was a product of Worthington Biochemical was placed in the test tube (B). Purified nitrogen gas was Corp., Lot no. CDI 8LK. p-Nitrophenyl anthranilate was a bubbled through the solvent for about 3 hr. The solvent was gift from Mr. A. Carmel, who prepared the material (Carmel, then transferred to the test tube (B). After the protein A., to be published). 2-p-Toluidinylnaphthalene-6-sulfonate completely dissolved in the solvent, the solution was trans- (TNS) was a gift from Dr. M. Shinitzky. All other reagents ferred to the fluorescence cell (C), and the Teflon stopcock were of analytical grade. (D) was closed. This procedure practically eliminated the Anthraniloyl chymotrypsin was prepared according to the detrimental effect of the illumination on the protein solutions. procedure developed by Haugland and Stryer (9). It was The exact concentration of the solutes was determined lyophylized and kept refrigerated after preparation. The spectrophotometrically. measurements were made within 1 week after preparation All measurements were made at room temperature (about of the protein derivative. 220). We prepared the chymotrypsin-TNS complex by mixing the protein with the dye, the total concentrations in the RESULTS AND DISCUSSION mixture being 4 X 10-4 M and 2 X 10-6 M, respectively. The absorption and CD spectra of the chymotrypsin-TNS Fresh preparations were used daily. complex in the range of 335-400 nm are presented in Fig. 2. Corrected fluorescence spectra were obtained with a The concentrations of the protein and dye were 4 X 10-4 M Turner 210 "spectro" fluorimeter. Measurements of CD and 2 X 10-5 M, respectively, in 0.1 M Tris buffer (pH were made with a Spectropolarimeter model 60, Cary (Palo 8.05). The CD is expressed as Ai = El- Er, i.e., the difference Alto, Calif.), with accessory 6001 for measurements of CD. between the molar extinction coefficients for left-handed and The circular polarization
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