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Originally published In Press as doi:10.1074/jbc.M606962200 on August 17, 2006

J. Biol. Chem., Vol. 281, Issue 42, 31184-31187, October 20, 2006
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Selenocompounds Can Serve as Oxidoreductants with the Methionine Sulfoxide Reductase Enzymes*

Daphna Sagher{ddagger}, David Brunell{ddagger}, Nathan Brot§, Bert L. Vallee, and Herbert Weissbach{ddagger}1

From the {ddagger}Center for Molecular Biology and Biotechnology, Florida Atlantic University, Boca Raton, Florida 33431, the §Hospital for Special Surgery, Department of Microbiology and Immunology, Weill Medical College of Cornell University, New York, New York 10021, and the Harvard Medical School, Boston, Massachusetts 02115

Received for publication, July 21, 2006 , and in revised form, August 15, 2006.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 EXPERIMENTAL PROCEDURES
 RESULTS
 DISCUSSION
 REFERENCES
 
In a recent study on the reducing requirement for the methionine sulfoxide reductases (Msr) (Sagher, D., Brunell, D., Hejtmancik, J. F., Kantorow, M., Brot, N. & Weissbach, H. (2006) Proc. Natl. Acad. Sci. U. S. A. 103, 8656–8661), we have shown that thioredoxin, although an excellent reducing system for Escherichia coli MsrA and MsrB and bovine MsrA, is not an efficient reducing agent for either human MsrB2 (hMsrB2) or human MsrB3 (hMsrB3). In a search for another reducing agent for hMsrB2 and hMsrB3, it was recently found that thionein, the reduced, metal-free form of metallothionein, could function as a reducing system for hMsrB3, with weaker activity using hMsrB2. In the present study, we provide evidence that some selenium compounds are potent reducing agents for both hMsrB2 and hMsrB3.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
EXPERIMENTAL PROCEDURES
 RESULTS
 DISCUSSION
 REFERENCES
 
The methionine sulfoxide reductases (Msr)2 are a family of enzymes that can reduce either free or protein-bound methionine sulfoxide (met(o)) (1). The reduction of met(o) in proteins is catalyzed by either MsrA, which reduces the S epimer of met(o) (met-S-(o)), or the MsrB proteins, which reduce the R epimer of met(o) (met-R-(o)). Previous genetic studies with MsrA have shown that this enzyme plays an important role in protecting cells against oxidative damage and may also be involved in aging (1–4). Although thioredoxin (Trx) has been accepted as the reducing agent for MsrA, recent studies have shown that two of the members of the MsrB family, hMsrB2 and hMsrB3, do not use Trx efficiently (5). In a search for another reducing system for these MsrB enzymes, it was discovered that thionein (T), the reduced apoprotein of metallothionein (MT), could function as a reducing system for hMsrB3 and that Trx could reduce oxidized thionein (T(o)), permitting T to recycle (5). In previous studies on the oxidation and reduction of Zn-MT, it was shown that selenium compounds, such as selenocystamine (SeCm), can markedly increase the release of zinc from Zn-MT or the uptake of zinc by T, depending on the oxidation state of the protein (6). In the presence of a reducing agent such as GSH, the SeCm is reduced to selenocysteamine (SeCem) (7), which greatly accelerates the reduction of T(o) and the uptake of zinc to form Zn-MT (6). Previous studies have also shown that reduced selenium compounds can function as reducing agents for lipid hydroperoxides (8). One of the members of the Msr family, MsrB1, is a selenoprotein, although MsrB2 and MsrB3 do not contain selenium but are zinc proteins (9). In the present studies, we have examined the effect of SeCm and other selenium compounds on the activity of several Msr enzymes in the presence of either the Trx system or T.


   EXPERIMENTAL PROCEDURES
TOP
 ABSTRACT
 INTRODUCTION
 EXPERIMENTAL PROCEDURES
RESULTS
 DISCUSSION
 REFERENCES
 
Methionine sulfoxide, dabsyl chloride (4-N,N-dimethylaminoazobenzene-4-sulfonyl chloride, DABS-Cl), SeCm, SeCem, selenocystine, sodium selenite (Na2SeO3), sodium selenate (Na2SeO4), selenomethionine, ebselen, and other chemicals were purchased from Sigma, unless specified otherwise. DABS-met-S-(o) and DABS-met-R-(o) were prepared by derivatizing the amino group of met-R-(o) or met-S-(o) with DABS-Cl (10, 11). Trx and Trx reductase (Escherichia coli), bovine MsrA (bMsrA), E. coli MsrA and MsrB (eMsrA and eMsrB), and human MsrBs (hMsrB2 and hMsrB3) were overexpressed in E. coli and purified as described previously (5, 12–14).

Preparation of T—T was prepared from bovine liver Zn-MT as described previously (5). Briefly, the liver 100,000 x g supernatant was heated and fractionated on a sizing column, and then Zn-MT-1 and Zn-MT-2 were purified by DE-52 anion-exchange chromatography. Zn-MT-1 and Zn-MT-2 fractions from the DE-52 column were dialyzed against 10 mM HCl to produce metal-free T. T was stored in 10 mM HCl at 4 °C and added to the reaction mixture just before initiation of the incubation. Incubations were routinely carried out for 20 min to minimize oxidation of T, which occurs at neutral pH (5, 15).

Colorimetric Assay for Msr Activity—This assay is based on the reduction of DABS-met-(o) to DABS-L-met (5) using a modification of a previously described procedure (16). Reaction mixtures contained 100 mM Tris, pH 7.4, 100 nmol of the indicated DABS met(o) epimer, 1–5 µg of purified Msr enzyme, as indicated, and the appropriate reducing system, 15 mM DTT, 5.6 nmol of T, or the Trx system (1 mM NADPH, 2.4 µg of Trx reductase, and 10 µg of Trx) and 50 µM SeCm were added where indicated. The total reaction volume was 200 µl, and the incubations were done at 37 °C for 20 min unless otherwise indicated. Reactions were terminated by adding 200 µl of 1 M sodium acetate, pH 6.0, followed by 100 µl of acetonitrile and extracted with 1 ml of benzene. 100 nmol of the product, DABS-L-met, extracted into the benzene layer, gave an optical density of 1.7 at 436 nm. Under these incubation conditions, the enzymatic reactions were proportional to enzyme concentration until 70% (70 nmol) of the substrate was reduced. The results are presented as nmol of product formed in the incubations in the specified time. Each assay was repeated a minimum of four times, and the results in the tables represent typical experiments.


Figure 1
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  		FIGURE 1.
Structure of selenium compounds. A, SeCm. B, SeCem. C, selenocystine. D, selenocysteine.

 

   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 EXPERIMENTAL PROCEDURES
 RESULTS
DISCUSSION
 REFERENCES
 
In looking for agents that could stimulate the reaction of the Msr enzymes with either Trx or T, selenium compounds were considered because of their known ability to act as oxidoreductants in reactions involving Trx (17) and MT (6). In the present studies, we used SeCm (Fig. 1A), an organic diselenium compound that can be reduced to the selenol, SeCem (Fig. 1B), as a model compound. Table 1 summarizes the results using five members of the Msr family: eMsrA, eMsrB, bMsrA, hMsrB2, and hMsrB3. All of the reactions in Table 1 contained NADPH and Trx reductase. As seen in Table 1, column 1, in the absence of E. coli Trx or SeCm, there was no Msr activity. In the presence of Trx (Table 1, column 2), good activity was seen with eMsrA, eMsrB, and bMsrA with low activity observed with hMsrB2 and hMsrB3, as reported earlier (5). In these experiments, E. coli Trx reductase was used; however, we have shown previously that mammalian Trx reductase is also not active with hMsrB2 and hMsrB3 (5). Table 1, column 3 shows that the addition of SeCm to the Trx reducing system has only a small effect on the activity of the E. coli enzymes, eMsrA and eMsrB (10–20% stimulation). These enzymes are known to use the Trx system most efficiently (5). In contrast, the activities of bMsrA and especially the two human MsrBs, hMsrB2 and hMsrB3, are markedly stimulated by the presence of SeCm. The bMsrA activity increases more than 3-fold, and the activity of both hMsrB2 and hMsrB3 increase 30–50-fold in the presence of SeCm. Until now, the only reducing agent that has given good activity with hMsrB2 has been DTT. However, it is evident from the results in Table 1, column 3, that the Trx reducing system can function with hMsrB2 in the presence of a selenol compound. To determine whether hydrogen transfer to SeCm catalyzed by Trx reductase requires Trx, Trx was omitted in the experiments shown in Table 1 column 4. As seen in column 4, all of the enzymes have significant activity, demonstrating that Trx reductase can transfer hydrogen directly from NADPH to SeCm to form SeCem. These results indicate that SeCem can supply the reducing power for the Msr enzymes. It should be noted that SeCm by itself had no activity in the absence of an Msr enzyme or a reducing system.


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  		TABLE 1
Effect of SeCm on the activity of Msr proteins using the Trx reducing system

Incubation conditions and assay are described under "Experimental Procedures." All of the incubations contained Trx reductase (2.4 µg) and NADPH (1 mM). Where indicated, Trx (10 µg) and/or SeCm (50 µM) were added. Enzyme amounts used were as follows: 1.6 µg of eMsrA (70 pmol); 2.7 µg of eMsrB (175 pmol); 3 µg of bMsrA (120 pmol); 2.0 µg of hMsrB2 (95 pmol); 2.2 µg of hMsrB3 (110 pmol). Incubations were for 20 minutes. SeCm, in the absence of either Trx reductase plus NADPH or an Msr enzyme, was not active (data not shown).

 


Figure 2
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  		FIGURE 2.
Effect of SeCm concentration on the activity of hMsrB3 using either the Trx reducing system (•–•) or T ({blacksquare}–{blacksquare}) as the reducing agent. hMsrB3 was incubated with the Trx reducing system (Trx, Trx reductase, and NADPH, see "Experimental Procedures" and Table 1) or with 5.6 nmol of T as the reducing agent (see "Experimental Procedures" and Table 2). Amounts of enzyme used were 2.2 µg of hMsrB3 with T and 1.1 µg with the Trx system. SeCm was added at the concentrations specified. A 20-min incubation was used.

 
As reported earlier, (5) T can serve as a reducing agent for all of the Msr enzymes tested, with hMsrB2 showing the least activity. Table 2 shows the results of experiments using T in place of the Trx reducing system, with and without SeCm. In the presence of SeCm, there is also a marked stimulation of T activity with all of the Msr enzymes, including hMsrB2. Once again, the most striking effects are seen with bMsrA, hMsrB2, and hMsrB3. These results indicate that T, similar to Trx and Trx reductase, can reduce SeCm to SeCem, which can supply the reducing system for the Msr enzymes. The activity with DTT, a commonly used in vitro reducing agent, is also shown in Table 2. The activity with all of the Msr enzymes in the presence of T and SeCm is similar to or better than that obtained with DTT.


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  		TABLE 2
Effect of SeCm on the activity of Msr proteins using thionein (T) as the reducing agent

Incubation conditions and assay are described under "Experimental Procedures." In these experiments, Trx, Trx reductase, and NADPH were omitted, and 5.6 nmol of T or 15 mM DTT were added where indicated. The amounts of bMsrA, hMsrB2, hMsrB3, and SeCm used were the same as in Table I. However, 3.2 µg of eMsrA and 5.4 µg of eMsrB were used. Incubations were for 20 minutes.

 


Figure 3
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  		FIGURE 3.
Time curve of hMsrB3 activity using the Trx reducing system either with (•–•) or without ({blacksquare}–{blacksquare})50 µM SeCm. Details of the incubation are described under "Experimental Procedures."

 


Figure 4
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  		FIGURE 4.
Putative reaction mechanism for reduction of the various Msr enzymes by Trx, T, and SeCm. A, MsrA or other Msr enzymes that contain a second cysteine, in addition to the catalytic cysteine, that is capable of forming a disulfide bond on the enzyme. B, MsrB2 and MsrB3, examples of enzymes that do not contain a second free cysteine.

 
Fig. 2 shows the effect of SeCm concentration on the activity of hMsrB3 using either the Trx reducing system or T as the reducing agent. Under the assay conditions, 50 µM SeCm appears to be the saturating concentration for T, whereas for the Trx-dependent reaction, the maximal activity requires more than 150 µM SeCm.

Fig. 3 shows a time curve for hMsrB3 activity using the Trx reducing system in the presence or absence of 50 µM SeCm. The reaction is close to linear for up to 20 min and is dependent on SeCm.

Other selenium compounds were tested for their ability to serve as reducing agents with MsrB2 and MsrB3. As shown in Table 3, selenocystine (Fig. 1C), which can be reduced to selenocysteine (Fig. 1D), can efficiently support the Msr activity in the presence of the complete Trx system. Some activity, although much lower, was also detected with sodium selenite in the presence of the Trx system. It should be noted that the concentration of selenite used was 25 µM, which was optimal. Higher concentrations of selenite inhibited the reaction. However, unlike SeCm, these selenocompounds could not accept hydrogens from E. coli Trx reductase in the absence of Trx (data not shown). This was previously reported for selenite (22). Three other selenium compounds tested, sodium selenate, ebselen, and selenomethionine, were inactive under the same conditions.


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  		TABLE 3
Effect of addition of selenite and selenocystine to hMsrB reactions containing the Trx system

Incubation conditions and assay using the Trx reducing system (NADPH, Trx reductase and Trx) are as described under "Experimental Procedures" and Table I. Selenocystine (50 µM) and sodium selenite (25 µM) were used where indicated. Enzyme amounts used were as follows: 2.2 µg of hMsrB3 and 1.6 µg of hMsrB2.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 EXPERIMENTAL PROCEDURES
 RESULTS
 DISCUSSION
REFERENCES
 
It appears that the Trx system is the primary reducing system for the MsrA enzymes as well as for eMsrB. However, the low activity of both hMsrB2 and hMsrB3 with Trx as the reducing system suggested that there should be another reducing system in mammalian cells for these enzymes. The recent finding (5) that T can reduce hMsrB3 and that T(o) could be reduced by the Trx system has focused attention on the possible role of T as a cellular reducing agent, in addition to its role in binding metals. Since neither Trx nor T functioned well with hMsrB2, it seemed clear that there may be other factors that play a role in supplying the reducing system for hMsrB2 and, very likely, for hMsrB3. It has been known that selenium compounds can accelerate the binding of zinc to T and the release of zinc from Zn-MT in the presence of GSH and GSSG, respectively (6). In addition, previous work has demonstrated that Trx reductase can catalyze the reduction of oxidized selenium compounds such as selenocystine and ebselen and that reduced selenium compounds can reduce small molecules such as H2O2 (17) or lipid hydroperoxides (8) as well as ferricytochrome c (22). It is also known that selenium-containing enzymes can receive hydrogen directly from mammalian Trx reductase, also a selenoprotein (23). The present studies confirm that SeCm and other selenium compounds, such as selenite and selenocystine, can be reduced by the Trx reducing system, i.e. NADPH, Trx reductase, and Trx. In the case of SeCm, there is efficient reduction to SeCem even in the absence of Trx, demonstrating that E. coli Trx reductase is able to directly reduce SeCm to SeCem. Once reduced, the SeCem formed is a potent reducing agent for hMsrB2 and hMsrB3. As reported previously (5), Trx is a poor reducing agent for both hMsrB2 and hMsrB3. However, in the presence of SeCm, the Trx reducing system is very effective with the MsrB enzymes. The SeCem, formed by the reduction of SeCm, appears to be an intermediate hydrogen carrier between the Trx reducing system and the oxidized MsrB enzyme intermediate. A similar situation appears true for T, which is also a much more efficient reducing agent for the MsrB enzymes in the presence of SeCm. In this case, T reduces SeCm to SeCem, which serves as the direct reducing agent. In the case of the MsrA enzymes and eMsrB, which have at least one additional free cysteine to form a disulfide, it is known that the oxidized enzymes contain a disulfide bond that must be reduced in order for the enzyme to recycle (18–21). These enzymes showed much less stimulation by SeCm in the presence of Trx or T. In contrast, neither hMsrB2 nor hMsrB3 have a free cysteine to form a disulfide bond with the cysteine at the catalytic site, and it has been postulated that the sulfenic acid intermediates on both MsrB2 and MsrB3 are directly reduced by Trx (24). Our results suggest that Trx is a poor reducing agent for these enzymes but that in vitro, Trx and T can be potent reducing agents in the presence of an appropriate selenium compound, such as SeCm or selenocystine. These reactions are summarized in Fig. 4. We should note that we have not studied MsrB1, a known selenoprotein that also contains a second cysteine capable of forming a Se–S bond on the enzyme (24), because of the difficulty in expressing the recombinant protein.

The in vivo significance of the role of selenium in the Msr reactions is not clear. It would be of great interest if one could identify a naturally occurring selenium compound in mammalian cells, similar to SeCem, that can act as an intermediate hydrogen carrier between Trx (or T) and the MsrB enzymes, similar to what has been observed in the in vitro studies described here. It should be noted that SeCm and selenite have been identified as selenium metabolites in human urine (25), but there is no evidence that they function as oxidoreductants. Selenocysteine is normally found in selenoproteins, where it can function as an oxidoreductant, and one should consider the possibility that there is a selenoprotein in cells that can transfer hydrogen directly to the Msr enzymes. Although the possible role of selenium compounds as cellular reducing agents for the Msr enzymes remains unclear, administering compounds such as SeCm or selenocystine might be a novel way to increase the intracellular activity of the Msr enzymes, especially MsrB2 and MsrB3.

There are some data on the effect of selenium-deficient diets on Msr activity. Mice on a selenium-deficient diet have lower in vitro levels of MsrB activity, which are presumed to be due to reduced MsrB1 activity since MsrB1 is a selenoprotein (26). However, based on the studies here, one might expect lower activity of both MsrB2 and MsrB3, in vivo, if a selenium compound is able to function as an oxidoreductant for MsrB2 and MsrB3 in cells. Thus, a selenium-deficient diet could result in a severe reduction of total MsrB activity in cells.


   FOOTNOTES
 
* This is Contribution P200524 from the Center of Excellence in Biomedical and Marine Biotechnology, Florida Atlantic University, Boca Raton, FL, which partially funded these studies. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. Back

1 To whom correspondence should be addressed: Center for Molecular Biology and Biotechnology, FL Atlantic University, 777 Glades Rd., Boca Raton, FL 33431. Tel.: 561-297-2596; Fax: 561-297-2594; E-mail: hweissba{at}fau.edu.

2 The abbreviations used are: Msr, methionine sulfoxide reductase; hMsr, human methionine sulfoxide reductase; eMsr, E. coli methionine sulfoxide reductase; bMsr, bovine methionine sulfoxide reductase; met(o), methionine sulfoxide; Trx, thioredoxin; MT, metallothionein; T, thionein; T(o), oxidized thionein; SeCm, selenocystamine; SeCem, selenocysteamine; DABS, 4-N,N-dimethylaminoazobenzene-4-sulfonyl; DTT, dithiothreitol. Back


   ACKNOWLEDGMENTS
 
We express our thanks to Dr. Edmond Fischer for helpful advice and guidance.



   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 EXPERIMENTAL PROCEDURES
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Weissbach, H., Resnick, L., and Brot, N. (2005) Biochim. Biophys. Acta 1703, 203–212[Medline] [Order article via Infotrieve]
  2. Ruan, H., Tang, X. D., Chen, M. L., Joiner, M. L., Sun, G., Brot, N., Weissbach, H., Heinemann, S. H., Iverson, L., Wu, C. F., and Hoshi, T. (2002) Proc. Natl. Acad. Sci. U. S. A. 99, 2748–2753[Abstract/Free Full Text]
  3. Moskovitz, J., Bar-Noy, S., Williams, W. M., Requena, J., Berlett, B. S., and Stadtman, E. R. (2001) Proc. Natl. Acad. Sci. U. S. A. 98, 12920–12925[Abstract/Free Full Text]
  4. Koc, A., Gasch, A. P., Rutherford, J. C., Kim, H. Y., and Gladyshev, V. N. (2004) Proc. Natl. Acad. Sci. U. S. A. 101, 7999–8004[Abstract/Free Full Text]
  5. Sagher, D., Brunell, D., Hejtmancik, J. F., Kantorow, M., Brot, N., and Weissbach, H. (2006) Proc. Natl. Acad. Sci. U. S. A. 103, 8656–8661[Abstract/Free Full Text]
  6. Chen, Y., and Maret, W. (2001) Eur. J. Biochem. 268, 3346–3353[Medline] [Order article via Infotrieve]
  7. Chaudiere, J., Courtin, O., and Leclaire, J. (1992) Arch. Biochem. Biophys. 296, 328–336[CrossRef][Medline] [Order article via Infotrieve]
  8. Björnstedt, M., Hamberg, M., Kumar, S., Xue, J., and Holmgren, A. (1995) J. Biol. Chem. 270, 11761–11764[Abstract/Free Full Text]
  9. Kim, H.-Y., and Gladyshev, V. N. (2004) Mol. Biol. Cell 15, 1055–1064[Abstract/Free Full Text]
  10. Lavine, T. (1947) J. Biol. Chem. 169, 477–491[Free Full Text]
  11. Minetti, G., Balduini, C., and Brovelli, A. (1994) Ital. J. Biochem. (Engl. Ed.) 43, 273–283[Medline] [Order article via Infotrieve]
  12. Lowther, W. T., Weissbach, H., Etienne, F., Brot, N., and Matthews, B. W. (2002) Nat. Struct. Biol. 9, 348–352[Medline] [Order article via Infotrieve]
  13. Rahman, M. A., Nelson, H., Weissbach, H., and Brot, N. (1992) J. Biol. Chem. 267, 15549–15551[Abstract/Free Full Text]
  14. Moskovitz, J., Weissbach, H., and Brot, N. (1996) Proc. Natl. Acad. Sci. U. S. A. 93, 2095–2099[Abstract/Free Full Text]
  15. Klein, D., Sato, S., and Summer, K. H. (1994) Anal. Biochem. 221, 405–409[CrossRef][Medline] [Order article via Infotrieve]
  16. Etienne, F., Resnick, L., Sagher, D., Brot, N., and Weissbach, H. (2003) Biochem. Biophys. Res. Commun. 312, 1005–1010[CrossRef][Medline] [Order article via Infotrieve]
  17. Zhao, R., and Holmgren, A. (2002) J. Biol. Chem. 277, 39456–39462[Abstract/Free Full Text]
  18. Lowther, W. T., Brot, N., Weissbach, H., Honek, J. F., and Matthews, B. W. (2000) Proc. Natl. Acad. Sci. U. S. A. 97, 6463–6468[Abstract/Free Full Text]
  19. Lowther, W. T., Brot, N., Weissbach, H., and Matthews, B. W. (2000) Biochemistry 39, 13307–13312[CrossRef][Medline] [Order article via Infotrieve]
  20. Boschi-Muller, S., Azza, S., Sanglier-Cianferani, S., Talfournier, F., Van Dorsselear, A., and Branlant, G. (2000) J. Biol. Chem. 275, 35908–35913[Abstract/Free Full Text]
  21. Antoine, M., Boschi-Muller, S., and Branlant, G. (2003) J. Biol. Chem. 278, 45352–45357[Abstract/Free Full Text]
  22. Kumar, S., Björnstedt, M., and Holmgren, A. (1992) Eur. J. Biochem. 207, 435–439[Medline] [Order article via Infotrieve]
  23. Björnstedt, M., Xue, J., Huang, W., Akesson, B., and Holmgren, A. (1994) J. Biol. Chem. 269, 29382–29384[Abstract/Free Full Text]
  24. Kim, H.-Y., and Gladyshev, V. N. (2005) PLoS Biol. 3, e375, 1–10[CrossRef][Medline] [Order article via Infotrieve]
  25. Francesconi, K. A., and Pannier, F. (2004) Clin. Chem. 50, 2240–2253[Abstract/Free Full Text]
  26. Moskovitz, J., and Stadtman, E. R. (2003) Proc. Natl. Acad. Sci. U. S. A. 100, 7486–7490[Abstract/Free Full Text]

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HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
 All ASBMB Journals   Molecular and Cellular Proteomics 
 Journal of Lipid Research   ASBMB Today 
Copyright © 2006 by the American Society for Biochemistry and Molecular Biology.
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