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Conformational Studies of A-Globin in 1-Propanol: Propensity of The Proc. Natl. Acad. Sci. USA Vol. 84, pp. 7014-7018, October 1987 Biochemistry Conformational studies of a-globin in 1-propanol: Propensity of the alcohol to limit the sites of proteolytic cleavage (semisynthesis/a-helical conformation/protein structure/organic cosolvents/segmental flexibility) K. SUBRAMONIA IYER AND A. SEETHARAMA ACHARYA The Rockefeller University, 1230 York Avenue, New York, NY 10021 Communicated by Christian B. Anfinsen, June 15, 1987 ABSTRACT Selective condensation of the unprotected The protease-catalyzed reverse proteolysis for the semi- fragments ofa-globin-namely, a1..30 and a31.141-is catalyzed synthesis of noncovalent analogues of proteins has been by Staphylococcus aureus V8 protease in the presence of 25% emerging as a useful procedure to prepare covalent variants 1-propanol. The propensity of 1-propanol to induce the a- of proteins (7). The presence of organic cosolvents is crucial helical conformation and to generate a "native-like" topology for the protease-catalyzed ligation of the complementary for the polypeptide chain has been now investigated in an fragments of the fragment-complementing systems, and so attempt to understand the molecular basis of this enzyme- far glycerol has been found to be the only good cosolvent for catalyzed stereospecific condensation. Removal of heme from these investigations (5). However, during the course of our the a-chain decreases the overall a-helical conformation of the semisynthetic studies of a-chain from the complementary protein considerably. A significant amount of the a-helical fragments, we found that 1-propanol was a better organic conformation is restored in the presence of25% 1-propanol and cosolvent compared with glycerol for the V8 protease- the digestion ofa-globin by V8 protease becomes more selective catalyzed reformation ofGlu-30-Arg-31 peptide bonds in an concomitant with the increase in helicity. V8 protease digestion equimolar mixture of fragments a1_30 and a31.47 as well as ofa-globin at pH 6.0 and 40C occurs at Glu-30, Asp47, Glu-27, a1_30 and a31.141 (8, 9). Efficient semisynthesis occurred even and Glu-23 in the absence of 1-propanol. In the presence of when the concentration of 1-propanol was as low as 25% and 25% 1-propanol, the digestion is selective to the peptide bond with the heme-free globin fragments. Furthermore, the ofGlu-30. This selectivity appears to be a characteristic feature semisynthesis was very specific for the Glu-30 and Arg-31 of the native conformation of a-chain (polypeptide chain with peptide bond. V8 protease did not induce the peptide bond bound heme). 1-Propanol induces the a-helical conformation formation in shorter amino-terminal fragments with carbox- into RNase S. peptide also. However, this increased helical yl-terminal glutamic acid-i.e., a1.23, a1.27, and a31.141. The conformation did not protect the RNase S peptide from V8 selectivity in the reverse proteolysis in the fragment-com- protease digestion at the Glu-9-Arg-10 peptide bond. RNase plementing system is generally considered as a reflection of S is in an a-helical conformation in RNase an the "native-like" ordered structure in the mixture of com- peptide S, plementary fragments (7). However with a-chain, the remov- interacting fragment-complementing system of S protein and S al of heme to prepare the apoprotein (globin) results in the peptide. S peptide is resistant to V8 protease hydrolysis in this loss of "native conformation" of the polypeptide chain. conformation. Thus, the resistance of a peptide bond in a Therefore, it appeared that 1-propanol may be inducing a segment of a protein to protease digestion appears to be a native-like conformation in the globin fragments or globin consequence of the secondary structure as well as the tertiary under the solvent conditions used for semisynthesis. In an interactions of this segment with the rest of the molecule. The attempt to begin to answer these aspects, we have now results suggest that the 1-propanol induces a-helical confor- investigated the influence of 1-propanol on the overall con- mation into segments of a-globin as well as packing of these formation of a-globin using far-ultraviolet circular dichroism helices in a native-like topology. (far-UV CD) and susceptibility of the polypeptide chain to proteolysis in the presence of 1-propanol. There has been considerable interest in recent years in the structure of proteins in organic solvents (1). The low- MATERIALS AND METHODS temperature studies ofenzymes, cryoenzymology, as well as low-temperature crystallography have necessitated the use of Hemoglobin A (HbA) and a-chain of HbA that reacted with organic solvents in these protein structural studies (2). In p-hydroxymercuribenzoate (pHMB) were prepared as we have described (10). Globin from a-chain was prepared by the addition, many enzyme-catalyzed reactions are also being method of Rossi-Fanelli et al. (11). Staphylococcus aureus investigated in organic media to enhance the industrial V8 protease was obtained from Miles Laboratories (Naper- applications, specifically to take advantage of the high ville, IL). selectivity and specificity of the enzyme (3). With proteases, CD Spectra. The CD spectra was measured in an Aviv it has been possible to achieve "reverse proteolysis"-i.e., 6ODS spectropolarimeter fitted with a thermostated cell use proteases to catalyze the synthesis of peptide bonds by holder. Ellipticity values at 222 nm were converted to mean incorporating large amounts of organic solvents (i.e., like molar residue ellipticity values using the equation: [10222 = ethylene glycol, glycerol, etc.) in the reaction mixtures (4). Mr/100LC, where 6 = degrees, L = cell path length (dm), C The reformation of ribonuclease A from RNase S (5) and = concentration (g/ml), and Mr = mean residue molecular nuclease A from nuclease T (6) are the classical examples of weight. this reverse proteolysis approach for semisynthesis of pro- Digestion by V8 Protease. pHMB a-chain (in the carbon- teins (7). monoxy form) and a-globin at a concentration of 1 mg/ml in 10 mM NH4OAc at pH 6 or pH 8 was incubated with V8 The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" Abbreviations: pHMB, p-hydroxymercuribenzoate; RP-HPLC, re- in accordance with 18 U.S.C. §1734 solely to indicate this fact. versed-phase HPLC. 7014 Downloaded by guest on September 27, 2021 Biochemistry: lyer and Acharya Proc. Natl. Acad. Sci. USA 84 (1987) 7015 protease for 24 hr and the substrate-to-enzyme ratio was from the unprotected globin fragments a1l30 and a31_141 maintained at 200:1. After digestion at the desired tempera- suggest that the conformation of a-globin in 25% 1-propanol ture, the digests were lyophilized and analyzed by reversed- at pH 6.0 is probably native-like-i.e., the topology of the phase HPLC (RP-HPLC) (12). helical segments of a-globin may resemble that of a-chain. The digestion of a-globin by V8 protease at pH 6.0 was RESULTS carried out in the presence and absence of 1-propanol and compared with that of a-chain to determine whether the 1-Propanol-Induced Increase in the Helicity of a-Globin. overall tertiary interactions of a-globin in 1-propanol have The high helical content of a-chain is a consequence of the any native-like features. A 24-hr digestion was carried out so cooperative noncovalent interaction ofthe polypeptide chain that the small differences in the activity of V8 protease [in the and heme (13). Removal ofheme results in a considerable loss presence and absence of 1-propanol (25%)] do not complicate of a-helical conformation of polypeptide chain (Fig. 1). CD the interpretation of the results. At pH 6.0, the a-globin was spectra of a-globin in the absence of 1-propanol (Fig. 1) digested extensively by V8 protease both at 25°C and 37°C reveals that >50% of the molar ellipticity of the a-chain was (Fig. 2C). On the other hand, when the temperature was lost on removal of heme. 0222 of a-globin at pH 6.0 and 40C was only about 40% of the a-chain. However, when 1- lowered to 4°C, the digestion was significantly limited. The propanol was incorporated into the system, the helical four components eluting around 30, 32, 36, and 45 min content of a-globin was significantly increased. 6222 of a- represent the fragments a1l23, a1.27, a1l30, and a3147, respec- globin in 25% 1-propanol was nearly 80% of that of a-chain. tively (15), and represent the four small molecular weight Thus, the loss of secondary structure of the a-chain that components (Fig. 2A) generated as the major cleavage occurs concomitant with the removal ofheme is compensated to a considerable degree on inclusion of25% 1-propanol in the buffer. The propensity of the apoprotein to take up the more a-helical conformation is a function of 1-propanol concen- tration (Fig. 1 Inset). However, the increase in the ellipticity of the a-globin at 0222 is not directly related to the concen- tration of the alcohol. In the range of 0-10%, a very small change in the secondary structure of the protein was ob- served. On the other hand, in the range of 10-25% 1- propanol, a significant increase in the value of 0222 occurred. Further increase in the concentration of 1-propanol induced only a small change in the value of 0222. Trifluoroethanol is an organic solvent that is generally used to determine the propensity of polypeptide fragments of protein to take up an a-helical conformation (14). Therefore, it was of interest to determine the relative efficiency of trifluoroethanol and 1-propanol to induce the a-helical con- formation to a-globin.
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