Periodate Oxidation of Glycopeptides from Ovalbumin*

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1 The Journal of Biochemistry, Vol. 60, No. 3, 1966 Periodate Oxidation of Glycopeptides from Ovalbumin* By MAYUMI MAKING and IKUO YAMASHINA (From the Department of Biological Chemistry, Faculty of Pharmaceutical Sciences, Kyoto University, Kyoto) (Received for publication, March 8, 1966) It is generally accepted that in glyco proteins one or more heterooligosaccharide chains are covalently linked to the polypeptide moiety. Stepwise periodate oxidation according to Smith (1) would be expected to provide much information on the structure of the oligosaccharide using rather simple procedures. Application of this technique directly to glycoproteins is not very fruitful, because the polypeptide part tends to undergo unwanted side reactions (2). The oxidation of glycopeptides with very few amino acids attached to the oligosaccharide has also been tried (3-5), but with unclear results, probably due to overoxidation and possible degradation of the amino acids. Montgomery et al. (6) inter alia have extensively investigated the Smith degradation of one of the simplest glycopeptides, the glycopeptide from oval bumin. This glycopeptide is composed of three residues of N-acetylglucosamine and five residues of mannose with one of the glucosamine residues linked to L-asparagine. Because of the incomplete purification of the products in each step, however, they were unable to attribute a definite chemical composition to each degraded glycopeptide. Thus, the stepwise degradation to the smallest glyco peptide, G1cNAe-NH-Asp(1-L-19-aspartamido- 2-acetamido-l, 2-dideoxy-ƒÀ-D-glucose), could not be followed. In the reinvestigation of the Smith degradation of the ovalbumin glycopeptide, we applied the periodate oxidation for a elatively short period, so that overoxidation was minimized. Particular attention was also 's Support was provided by a grant from the Ministry of Education, Japan. 262 paid to the purification of the degraded glyco peptides at each step. Thus, the three step degradation could be followed with good yield at each step and the smallest glyco peptide, G1cNAc-NH-Asp, could finally be isolated. These results led us to amend the tentative formula of Montgomery et al. (6) for the ovalbumin glycopeptide and to be further convinced of the asparagine glucosamine linkage in ovalbumin. EXPERIMENTAL Materials-The preparation of the glycopeptide from ovalbumin and the synthesis of G1cNAc-NH- Asp, 1-L-ƒÀ-aspartamido-2-acetamido-1, 2-dideoxy-ƒÀ-Dglucose, were performed as previously described (7, 8). Periodate Oxidation of Glycopeptides-Periodate oxida tion was carried out with 0.2 M sodium metaperiodate at 5 C in the dark. The concentration of the glycopeptide was in every case about 3 mm, which means that the oxidant was in at least ten fold excess of the theo retical. The period of oxidation was 3 hours except in the first step, where both 3 and 24 hours' oxidation were performed with essentially the same results. Reduction and Acid Treatment of the Oxidized Glyco peptides-to the reaction mixture after periodate oxidation was added an equal volume of 0.3 M borate buffer of ph 8.0 containing 0.45 M sodium borohydride. The reduction proceeded for 15 hours at 2 C and the alkaline reaction mixture (ph 10.5) was then brought to ph 5 with glacial acetic acid. After the excess of sodium borohydride had been decomposed, the ph of the solution was further lowered to 1.0 with 2 N H2SO4. The hydrolysis proceeded for 15 hours at room temperature (20-25 C). Purification of the Degraded Glycopeptides-The hydrolysate of the oxido-reduced glycopeptide at each step was submitted to desalting and purification by means of ion exchange and gel filtration. Thus, the hydrolysate was first treated with Dowex-1 ~8, mesh, acetate form, in order to replace

2 Periodate Oxidation of Ovalbumin Glycopeptides 263 inorganic anions by acetate. The effluent after con centration was then passed down a column of Dowex-50 ~4, mesh (H+ form). The size of the column was 2 x 20 cm. for 25 mg. of the parent glycopeptide and was reduced in proportion to moles of glycopeptide with each successive degradation step. Glycopeptides and Na+ ions were retained by the resin. After washing the column with water, elution of the glycopeptides was carried out with 0.15 M pyridine acetic acid buffer of ph 5.0. Eluted glycopeptides were detected by the orcinol reaction for mannose at the first step and by the ninhydrin reaction at the second and third steps. The glycopeptide fractions were evaporated to dryness. Contamination by sodium ions of the glycopeptide fractions was in most cases insignificant, but when it occurred, as judged by the presence of salt crystals (sodium acetate) in the dried materials, the glyco peptide fractions were again passed down the Dowex-50 column. The salt-free dried materials were dissolved in 1.0 ml. of 0.1 M acetic acid and passed through a column of Sephadex G-25 (2 ~ 83 cm., in every case) which had been equilibrated with the same solvent. Determination of Sugars-The orcinol-h2so4 reaction (9) for mannose without hydrolysis, and the Elson - Morgan reaction (10) for glucosamine after hydrolysis in 2 N HCl for 16 hours at 100 C, were used. Determination of Amino Groups and Amino Acids-The ninhydrin method according to Y e m m and C o c k i n g (11) was used. Aspartic acid was determined in the acid hydrolysate (2 N HCl, 100 C, 16 hours) following chromatography according to Bush et al. (12). In some instances, aspartic acid and glucosamine in the acid hydrolysate were determined using an amino acid analyzer (Model KLA 3, Hitachi). The results were the same as those obtained by the separately performed analyses. Paper Chromatography-Two solvents were used. Solvent I ; phenol-water (4: 1, v/v) in an atmosphere of ammonia, Solvent II; isobutyric acid-0.5n aq. ammonia (5: 3, v/v). Paper Electrophoresis-Pyridine -acetic acid-water (1 : 10: 89, v/v, ph 3.6) was used and 75 volts per cm. were applied over a period of one hour, with cooling in n-hexane. RESULTS The First Step Degradation-Twenty-five mg. of the glycopeptide from ovalbumin were degraded. The pattern of gel filtration is shown in Fig. IA. The fractions indicated by arrows were collected and evaporated to FIG. 1. Gel filtration of the products of each degradative step. Column : Sephadex G-25, 2 X 83 cm. Solvent : 0.1 M acetic acid. Flow rate : 4 ml. per hour. Fraction volume : 2.3 ml. for A, 2.6 ml, for B, and 1.9 ml. for C. Determination : Orcinol-H2S04 reaction for A (0.2 ml. from each fraction), and ninhydrin reaction for B and C (0.3 ml. and 0.5 ml. from each fraction, respectively). dryness. Each fraction, dissolved in one ml. of 0.1 M acetic acid, was then separately passed through the same Sephadex column. After repeated gel filtration, the major fraction was homogeneous in paper chro matography and paper electrophoresis, while the minor fraction was a mixture of at least two components with yet unidentified struc tures. Rf values on paper chromatography

3 264 M. MAKING and I. YAMASHINA are given in Table I. The analytical values (Table II) show that the major fraction, the degraded glycopeptide, contained three moles less of mannose and one mole less of glucos amine compared to the parent glycopeptide. The yield of the reaction was satisfactorily high. After passing through the Dowex-2 column, the yield, determined by the glucosamine analysis, was about 90% of the theoretical. A similar yield was still achieved after the Dowex-50 treatment. The overall yield after gel filtration was about 80%, of which at least 85% was present in the major fraction. These figures show that we are dealing with the major reaction products. The Second Step Degradation-The degraded glycopeptide, the major fraction as above, was oxidized with periodate. The pattern of the gel filtration of the oxido-reduced and hydrolyzed glycopeptide is shown in Fig. 1$. The major fraction, indicated by the arrow, was homogeneous on paper chromatography and paper electrophoresis. Rf values are shown in Table I. This compound was found to be composed of two moles of glucosamine, with one of them apparently TABLE R f Values of Degraded Glycopeptides and Reference Substances on Paper Chromatography I 1) See experimental part in the text. 2) Reference I : 1-L-ƒÀ-aspartamido-2-acetamido-1, 2-dideoxy-ƒÀ-D-glucose. Reference II : 1-L-ƒ -aspartamido-2-acetamido-1,2-dideoxy-ƒà-d-glucose. TABLE Analytical Values" of the Degraded Glycopeptides II 1) All values are given with reference to 1 mole of aspartic acid.

4 Periodate Oxidation of Ovalbumin Glycopeptides 265 attached to asparagine, as shown in Table II. Thus, two moles of mannose had been removed during the second step degradation. The presence of a minute amount of orcinol- H2SO4 reacting substance in this fraction (equivalent to 0.08 mole mannose with reference to 1 mole of aspartic acid) does not seem to cause any change in this conclusion. The overall yield after the gel filtration was comparable to that found for the first step degradation. The Third Step Degradation-The major fraction of Fig. lb was further degraded, producing the pattern of gel filtration shown in Fig. 1C. Of the three fractions observed, the major one was homogeneous on paper chromatography and paper electrophoresis. The others were also nearly homogeneous, but they, amounting to only 10-15% of the total, were not examined further. The R f value of one of the minor fractions (that indicated by the arrow in Fig. IC) is shown in Table I. The major fraction was found to be indistinguishable from the synthetic 1-L-ƒÀ-aspartamido-2-acetamido-1, D-glucose in paper chromatography and paper electrophoresis in which the spot appeared characteristically bluish purple on staining with ninhydrin. These criteria of identity have been discussed previously (8). The isomer, I-L-ƒ -aspartamido-2-acetamido-1, 2- dideoxy-ƒà-d-glucose, as one of the most similar compounds, had a slightly higher Rf value in Solvent I with a purple ninhydrin colour. The identification was also consistent with the analytical results, shown in Table II. The overall yield of the major fraction was about 60% of the theoretical. DISCUSSION Application of the Smith degradation to glycopeptides has often been attempted, but with unclear results. By isolating the products of each degradative step in a homogeneous state, we were able to demonstrate a stepwise degradation of the ovalbumin glycopeptide. A rather short period of periodate oxidation might have also been favourable in giving a fairly simple pattern of degradation products at each step. Thus, the parent glycopeptide, 2-dideoxy-ƒÀ- (Man)5(GlcNAc)2-NH-Asp yielded GIcNAc- NH-Asp through (Man)2(G1cNAc)2-NH-Asp and (G1cNAc)2-NH-Asp. The fact that the smallest glycopeptide, GIcNAc-NH-Asp, could be isolated and identified is of extreme importance. The evidence presented by us and others for the asparagine-glucosamine linkage in ovalbumin was based upon the isolation of the compound, in poor yield, by means of partial acid hydro lysis of the parent glycopeptide. Isolation of the compound by means of a stepwise degra dation with good yield as presented in this paper is most conclusive for this linkage, leav ing little possibility of other types of linkage. Concerning the oligosaccharide structure of the glycopeptide, we are still unable to present a whole picture. However, combining the results of methylation, enzymatic breakdown and partial hydrolysis obtained by others with the authors' present results, it is possible to suggest some reasonable structures. The findings which have been obtained by other workers and us may be summarized as follows. (1) Two moles of formic acid are produced upon periodate oxidation, which indicates that two out of five mannose residues are located at non-reducing termini unless there is any glycosidic linkage to C-6 of inner mannose residues (6). (2) Methylation studies have provided evidence that out of five mannose residues, two are located at the non-reducing termini (6). Furthermore, one mannose is substituted at C-3, one at C-2, and one at C-2 and C-4 (6). (3) One out of three glucosamine residues could be split off by ƒà-n-acetylglueosaminidase [EC ]. This glucosamine must be located at one of the non-reducing termini (13-15). (4) Partial acid hydrolysis of the parent glycopeptide yielded, among others, degraded glycopeptides which contained only one glucosamine with one or two mannose residues (6,16,17 ). This indicates that at least two mannose residues are linked to glucosamine which is located at the nearest position to aspartic acid.

5 266 M. MAKING and I. YAMASHINA ON the basis of these results combined with their Smith degradation, M o n t g o m e r y et al. (6) tentatively proposed the following structure for the ovalbumin glycopeptide. If this structure is correct, then the Smith degradation would proceed in the following way. (I) (Man)2(G1cNAc)2-NH-Asp (Man)(G1cNAc)-NH-Asp GIcNAc-NH-Asp. This process is not consistent with our results. We therefore propose an alternative structure (II) with the minimum alteration of (I). of the first step degradation, the results being in accord with the structure (I). This inconsistency between structure (I) and (II), however, appears to have arisen mainly from incomplete purification of the degraded glycopeptide at each step in the experiments of Montgomery et al. (6), since neither purity of the degraded glycopeptides nor the quantities of these methylated sugars were reported by them. The complete strucrure of the oligosac charide of the ovalbumin glycopeptide must await the results of methylation studies and enzymatic analyses with glycosidases of the purified degradation products. In a preliminary account, C u n n i n g h a m et al. (18) have reported recently variations in the composition and structure of the oligosaccharide units in ovalbumin glyco peptides. We have not been aware of this variation in our glycopeptide preparation. However, the present investigation is of value in affording a systematic experimental proce dure for the stepwise degradation of glyco peptides, which should be applicable to glycopeptides generally. Besides this, it may be presumed that at least the partial structure, (Man)2(G1cNAc)2-NH-Asp, would be common to a series of ovalbumin glycopeptides, since all of the glycopeptides isolated by C u n n- i n g h a m et al. (18) contained at least two glucosamine and five mannose residues per one mole of aspartic acid. SUMMARY The compositions of the intermediates during the stepwise degradation are all in accord with the experimental results. This proposed structure, however, is not consistent with the results of the methylation studies in which Montgomery et al. (6) claimed that they were able to detect 2, 3, 4, 6 - tetramethylmannose and 2, 4, 6- trimethylmannose by methylating the product 1. The Smith degradation of the glyco peptide from ovalbumin was carried out with careful purification of the products of each step degradation. 2. The degradation proceeded in the following way : (Man)5(GlcNAc)3-NH-Asp-> (Man)2(G1cNAc)2-NH-Asp --- * (GlcNAc)2 -NH- Asp---.G1cNAc-NH-Asp. The final product was indistinguishable from the synthetic 1-LƒÀ - aspartamido acetamido-1, 2-dideoxy-ƒÀ-Dglucose. 3. One possible structure of the glycopeptide is presented on the basis of the present investigation and of the combined informations from other workers.

6 Periodate Oxidation of Ovalbumin Glycopeptides 267 The authors are indebted to Dr. A. Yama moto of Kyushu University for the gift of 1-L-ƒ - aspartamido-2-acetamido-1,2-dideoxy - ƒà - n - glucose. They are grateful to Dr. J. E. Scott, Rheumatism Research Unit, Canadian Red Cross Memorial Hospital, England, for revising the manuscript. REFERENCES (1) Goldstein, I.J., Hay, G.W., Lewis, B.A., and Smith, F., " Methods in Carbohydrate Chemistry ", ed. by R.L. Whistler, Academic Press Inc., New York, Vol. V, p. 361 (1965) (2) Clamp, J.R., and Hough, L., Biochem. J., 94, 17 (1965) (3) Rothfus, J.A., and Smith, E.L., J. Biol. Chem., 238, 1402 (1963) (4) Chatterjee, A.K., and Montgomery, R., Arch. Biochem. Biophys., 99, 426 (1962) (5) Clamp, J.R., and Hough, L., Biochem. J., 94, 502 (1965) (6) Montgomery, R., Wu, Y.C., and Lee, Y.C., Biochemistry (1965) (7) Yamashina, I., and Makino, M., J. Biochem., 51, 359 (1962) (8) Yamashina, I., Makino, M., Ban-I, K., and Kojima, T., J. Biochem., 58, 168 (1965) (9) Hewitt, L.F., Biochem. J., 31, 360 (1937) (10) Svennerholm, L., Acta Soc. Med. Upsaliensis, 61, 287 (1956) (11) Yemm, E.W., and Cocking, E.C., Analyst, 80, 209 (1955) (12) Bush, H., Hurlbert, R., and Drotter, R., J. Biol. Chem., 196, 717 (1962) (13) Clamp, J.R., and Hough, L., Chem. Ind., 82 (1963) (14) Kaufman, H.H., and Marshall, R.D., `Abstracts of the Sixth International Congress of Bio chemistry, New York', Vol. 11, p. 92 (1964) (15) Muramatsu, T., and Egami, F., Japan. J. Exptl. Med., 35, 171 (1965) (16) Yamashina, I., Ban-I, K., and Makino, M., `Abstracts of 147th Meeting of the American Chemical Society, Philadelphia', p. 7c (1964) (17) Montgomery, R., Lee, Y.C., and Wu, Y.C., Biochemistry, 4, 566 (1965) (18) Cunningham, L., Ford, J.D., and Rainey, J.M., Biochim. et Biophys. Acta, 101, 233 (1965)

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