Galactose oxidase pro-sequence cleavage and cofactor assembly are self-processing reactions
Galactose oxidase pro-sequence cleavage and cofactor assembly are self-processing reactions
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DOI:
10.1021/ja993385y
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发表时间:
2000-02-09
影响因子:
15
通讯作者:
Dooley, DM
中科院分区:
文献类型:
--
作者:
Rogers, MS;Baron, AJ;Dooley, DM
Galactose oxidase is a member of a growing class of proteins with novel posttranslationally modified redox-active amino acids (see Figure 1). 1 The unusual nature of these modifications has stimulated interest in the mechanisms by which such cofactors are generated. Recently, the biogenesis of the 2, 4, 5-trihydroxyphenylalanine quinone (TPQ) cofactor of amine oxidase has been defined. 2 The oxidation of tyrosine to TPQ requires only copper ions and dioxygen, and is not dependent on any accessory proteins. 3 Analogous experiments with galactose oxidase have been hampered by the lack of sufficient quantities of pure precursor (unprocessed, copper-free) protein. Here we report the isolation of an apo, pro-enzyme form of galactose oxidase, and demonstrate that cleavage of the pro-sequence and assembly of the characteristic Tyr•-Cys cofactor are self-processing reactions. Figure 1 illustrates the critical features of the galactose oxidase active site. 4 In the oxidized (active) state tyrosine 272, which is posttranslationally cross-linked to cysteine 228 via a thioether bond, is oxidized to a radical. Thus the [Cu (II) Tyr•-Cys] unit acts as a two-electron acceptor in the oxidation of a wide variety of alcohols to the corresponding aldehydes. The posttranslational cross-link is believed to modulate the reactivity and redox potential of the tyrosyl radical. 5, 6 C228 may aid in stabilization of the radical by virtue of the electron-donating properties of the sulfur atom. 5 The oxidized form of galactose oxidase displays a characteristic set of electronic transitions (vida infra) that are also observed in glyoxal oxidase, a galactose oxidase homologue. 7 Heterologous expression8 of the Fusarium protein in Aspergillus nidulans under copper-limited conditions resulted in the appearance of multiple protein forms (Figure 2). The molecular weights of the SDS-PAGE bands in Figure 2a, established to be galactose oxidase by Western blotting, 8 were estimated as 70.2, 68.5, and∼ 65.5 kDa. N-terminal sequencing established that the fastest migrating protein (lower band,∼ 65.5 kDa) corresponds to mature, wild-type galactose oxidase. Mature galactose oxidase migrates on SDS-PAGE with an anomalous molecular weight (65.5 kDa as compared to 68.5 kDa predicted by the sequence), owing to the thioether bond, which produces a stable loop thus preventing full unfolding on treatment with SDS. 8 The middle band (Figure 2a) has an estimated Mr that correlates with the mass of the mature galactose oxidase amino acid sequence, suggesting that it is a form of galactose oxidase lacking the thioether bond. This behavior is mirrored by the variant C228G, which is unable to generate a thioether bond. 8 Finally, the upper band (Figure 2a), having an estimated Mr of 70.2 kDa, corresponds to the pro-form with the pro-sequence attached, which was confirmed by the N-terminal sequence data (Table 1). These data suggest that prosequence cleavage and thioether bond formation are separable reactions in vivo.Purification of a homogeneous form of unprocessed galactose oxidase was achieved for the first time by performing growth of the organism and protein purification under strictly metal-free conditions (Figure 2b). 9 Addition of Cu (II) and aerobic incubation result in conversion to the mature form as monitored by SDSPAGE (Figure 2b). This suggests that both pro-sequence cleavage and thioether bond formation are copper-mediated reactions. Cleavage of the pro-sequence is not due to extraneous or intrinsic protease activity because the reaction occurred when a proteaseinhibitor cocktail (Sigma P-8215) was present during the incubation with Cu (II). Importantly, this cocktail …