Vanadium Compounds - ACS Publications - American Chemical Society

Chapter 16

Vanadate-Containing Haloperoxidases and Acid Phosphatases: The Conserved Active Site

Downloaded by EMORY UNIV on August 15, 2015 | http://pubs.acs.org Publication Date: December 10, 1998 | doi: 10.1021/bk-1998-0711.ch016

Wieger Hemrika, Rokus Renirie, Henk Dekker, and Ron Wever E. C. Slater Institute, University of Amsterdam, Plantage Muidergracht 12, 1018 TV Amsterdam, The Netherlands We have shown that the amino acid residues contributing to the active site of vanadate-containing chloroperoxidase from the fungus Curvularia inaequalis, of which the crystal structure is known, are conserved within a large and diverse group of acid phosphatases, that include amongst others bacterial acid phosphatases, mammalian glucose-6-phosphatases and type 2 phosphatidic acid phosphatases. The suggestion that the active sites of these enzymes are structurally similar is confirmed by activity measurements showing that apochloro peroxidase exhibits phosphatase activity. These observations not only reveal interesting evolutionary relationships between these groups of enzymes but also have important implications for the research on acid phosphatases since structural data are lacking for this group of enzymes. Based on the conservation of the active sites we propose a new membrane topology model for glucose-6-phosphatase. Vanadate-containing haloperoxidases form a group of enzymes that have been isolated from seaweeds, fungi and a lichen (1-4). These enzymes catalyse the oxidation of a halide ( X ) to the corresponding hypohalous acid according to (1). +

H 0 + H + X " - > H 0 + HOX 2

2

2

[1]

In the presence of a suitable nucleophilic acceptor a second reaction can occur by which a diversity of halogenated compounds can be formed. Vanadate-containing haloperoxidases are named after the most electronegative halide they are able to oxidise implying that a chloroperoxidase is able to oxidise chloride, bromide and iodide and a bromoperoxidase only bromide and iodide. Hydrogen vanadate ( H V O 4 " ) , the prosthetic group of these enzymes, does not change its redox state during catalysis but remains in its highest (5 ) oxidation state. The metal most probably functions as a Lewis acid thus co-ordinating and activating the substrates in such a way that catalysis occurs. Vanadate-containing haloperoxidases are very chemo- and thermostable enzymes. They are also able to resist high concentrations of their substrate (H 0 ) and product (HOX) that would readily inactivate members of the other well known group of haloperoxidases; the heme-containing haloperoxidases as exemplified by the chloroperoxidase from the fungus Caldariomyces fumago (5) or myeloperoxidase which is present in white blood cells (6). +

2

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©1998 American Chemical Society In Vanadium Compounds; Tracey, A., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 1998.

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The above mentioned properties make the vanadate-containing haloperoxidases a very interesting research subject and as a result there has been a large increase in publications on this subject since the first isolation and identification of one such enzyme from seaweed (7,8) in the early eighties.


The Vanadate-containing Chloroperoxidase of Curvularia inaequalis For the last years research in our laboratory has mainly focused on the vanadatecontaining chloroperoxidase (V-CPO) from the fungus Curvularia inaequalis resulting in a description of its kinetic properties (9), the recent cloning and sequencing of the gene encoding this enzyme (10) and also (see the chapter by Messerschmidt, Prade and Wever in this book), in the determination of the X-ray structure of this enzyme (77). Furthermore a proposal for its physiological function has recently been put forward (72). The V-CPO gene codes for a protein of 609 amino acids with a calculated molecular mass of 67,488 kDa. The crystal structure of this enzyme at 2.1 A resolution (77) reveals that the protein has an overall cylindrical shape and measures approximately 50x80 Â. The secondary structure is mainly α-helical with two fourhelix bundles as main structural motifs of the tertiary structure. The vanadiumbinding centre (see Figure 1) is located on top of the second four-helix bundle and the residues binding the prosthetic group span a length of approximately 150 residues in the primary structure. The metal is co-ordinated to the Ν of H i s while 5 residues (Lys , A r g , Ser , G l y and Arg ) donate hydrogen bonds to the non-protein oxygens of vanadate. H i s is proposed to be an acid-base group in catalysis (//). Alignment of this V-CPO with the partial amino acid sequence of the vanadiumcontaining bromoperoxidase (V-BPO) of the seaweed Ascophyllum nodosum (7), an enzyme of which the catalytic mechanism is considered to be analogous to that of the V-CPO (9), revealed three stretches of high similarity in the regions providing the metal oxide binding site, whereas the similarity turned out to be very low in the intervening regions. Initial database searches using the entire V-CPO sequence revealed very little sequence similarity to other known proteins (10). By using the three stretches of amino acids that provide the metal oxide binding site as templates for database searches we have been able to show that such stretches are also present in at least three families of acid phosphatases that were previously considered unrelated (13). ε 2

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Vanadate-containing Haloperoxidases and Acid Phosphatases; A Conserved Active Site From our initial alignment, as presented in (13), it became clear that nearly all residues co-ordinating vanadate in V-CPO were conserved. This allowed the recognition of three separate domains that are highly similar among the aligned proteins. These three domains are connected however, by regions that are highly variable; both in sequence and in length. We thus suggested (13) that the binding pocket for vanadate in the peroxidases is similar to the phosphate-binding site in the aligned acid phosphatases. This is in agreement with the structural resemblance of vanadate and phosphate, with the observation that the vanadium-containing haloperoxidases rapidly loose their activity in phosphate-containing buffers and that reconstitution of the apo-BPO by vanadate is inhibited in the presence of phosphate (14). Furthermore, vanadate is recognised as a potent inhibitor of many different phosphatases (75). Since our initial database searches much improvement has been achieved in the available search algorithms and furthermore the linking of the databases, as done by the Entrez Browser provided by the National Centre for Biotechnology Information

In Vanadium Compounds; Tracey, A., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 1998.

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(NCBI), enabled us to quickly identify more than 40 (putative) proteins also containing domains 1, 2 and 3 in our more recent database searches (see also (16,17)). The conservation of the active sites among the presented enzymes, both in structure and residues binding the anions, prompted us to determine whether the apoCPO from C. inaequalis could also act as a phosphatase. Apo-Chloroperoxidase exhibits Acid Phosphatase Activity Since it is difficult to obtain pure apo-enzyme in sufficient amounts from C. inaequalis as needed for our experiments we decided to use recombinant enzyme produced from the C. inaequalis V-CPO gene in a newly developed Saccharomyces cerevisiae expression system (18). This enabled us to produce large quantities of pure recombinant enzyme (r-CPO) which was isolated as desrcribed (18) with the addition of an extra HPLC MonoQ step. After activation with vanadate the pure r-CPO behaves kinetically very similar to the enzyme as isolated from C. inaequalis. Figure 2 presents the results of an experiment in which the putative phosphatase activity of apo-r-CPO was assayed by measuring the release of p-nitrophenol (p-NP) from p-nitrophenyl phosphate (p-NPP), a commonly used phosphatase substrate. This figure shows that p-NPP hydrolysis correlates linearly with the amount of enzyme added, demonstrating that the apo-r-CPO has phosphatase activity. The presented data predict that vanadate and p-NPP compete for the same binding site in the apo-enzyme, implying that phosphatase and peroxidase activity are mutually exclusive. We have been able to show that this is indeed the case (13). Incubation of fully activated r-CPO with 0.5 mM p-NPP at pH 5.0 resulted in a rapid decrease of CPO activity which was not observed in the absence of p-NPP. The observed decrease of CPO activity could be prevented by the addition of extra ( 100 μΜ) vanadate We also determined the kinetic parameters of /?-NPP hydrolysis catalysed by apo-r-CPO as a function of pH (13). This revealed that V was only affected by a factor of 2 in the pH range 3.7-8.0 having an optimum at pH 5.0 (results not shown). The K for p-NPP remained approximately 50 μΜ in the pH range 4.5-8.0 but increased strongly in the pH range 3.7-4.5 (K 1.9 m M at pH 3.9), indicating that protonation of either a group on the free enzyme or the substrate itself is the cause of the reduced affinity for p-NPP. max

M

M

Vanadate-containing Bromoperoxidases, a Slightly Different Active Site? Figure 3 shows the alignment of domains 1, 2 and 3 of V-CPO of C. inaequalis, V BPO of A. nodosum and 8 (putative) phosphatases or proteins that are representatives of the more recently found homologues (see also Figure 3). The alignment reveals one striking difference between the V-CPOs and the acid phosphatases on one hand and the V-BPO on the other. Since our initial alignment (73) it has become clear (see Messerschmidt and Wever in this book) that residue 24 of the partial amino acid sequence of V - B P O is not an asparagine but a lysine. This residue therefore corresponds to L y s of domain 1 of V-CPO of C. inaequalis. This implies that in the V-BPO there are seven residues -and not six as in V-CPO and the acid phosphatasesbridging the Lys and Arg residues. The presence of an extra residue in domain 1 of V-BPO may be a factor determining the enzyme's high preference of bromide over chloride as a substrate. This is given weight by the fact L y s of the C. inaequalis enzyme also forms a hydrogen-bond with an oxygen (OV4) of the catalytic peroxointermediate (79) (see also the chapter by Messerschmidt, Prade and Wever) and thus may play an important role on activating the bound peroxide. The slightly different geometry of the active site which will be the consequence of the additional amino acid in domain 1 of V-BPO might result in a less polarised peroxo-intermediate and therefore in its inability to oxidise the more electronegative chloride ion at physiological concentrations. The presence of a histidine (His ) in domain 1 of the 353

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Figure 1. Active site of the V-CPO of C. inaequalis showing the conserved amino acid residues donated by Domain 1 (Κ , R ), Domain 2 S , G \ H ) and Domain 3 (R , H ) and the hydrogen-bonding pattern around the prosthetic group. 360

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apo-CPO concentration (nM) Figure 2. Phosphatase activity as a function of apo-r-CPO concentration. The enzyme was incubated with 1 mM p-NPP at 25 °C in 100 m M citrate (pH 5.0). After 4.5 hours reaction mixtures were quenched with NaOH and production of p-NP was measured at 410 nm using 6 = 18.3 m M ' c m at pH 12. Each measurement was carried out in triplo. 1

410nm



350W

Domain 1

Κ Ε KW Ε F - Ε

G-ô-Pase

Domain 2 Κ Ρ Ρ FP AY PSGH AT F G G 409 90 Τ Ρ Τ PSGH AT XN G 1 0 5 182 Κ Ε Μ PSGH SS F Τ F 197 161 Κ Ε G Y]S G H SS F S Ml76 74 159 L DG F R Τ Τ "PSGH SS Ε S F 1 150 Ν Ε Τ GY PSGH t I F A A 165 102 S I G GF PSGH SS I S A 117 148 L R ΚNGI PSGH T A Y G Τ 163 99 H A A DD PS@H GT VI F 114 109 C E T GP GS PSGH A M GT A 1 24

394

Domain 3

Figure 3. Alignment of V-CPO of C. inaequalis with representatives of the enzymes proposed to contain a structurally similar active site. Residues identical in 50% or more of the sequences are given in bold face and boxed. The numbers indicate the start and end positions of the domains in the respective proteins. Histidines aligning with the vanadate co-ordinating histidine from V-CPO are indicated by an asterisk, histidines aligning to the proposed acid base histidine of V-CPO are indicated by a diamond.

L ν F[gw l L - F

L S G V36S 21W Y Q KWQ V H RF A RP Ε A L G 37 ,29 D ι A K Y S I - GRL RP H F I A144 I A ΚΎΤ I - GS L RP H F L Ai32 T M prot 115N F I KNW I - GRL RP D F L D130 PGPB si Τ G A KjA L F - ΕΕ Ρ RP F T V Y 1 0 6 A 95 Neutral Pase 8°GG l K|R l L - κ I Ρ RP FF ΤV LH F135 Acid Pase 1 2 0 A s A[K!K Y Y - MRT RP Mig-13 76 W Τ MG H L F - HD P RP F V D H 91 GQl RP lYWWV 88 73

V-CPO V-BPO Wunen PAP2


C. inaequalis A. nodosum Drosophila Mouse S. cerevisiae H. influenzae T. clenticola S. typ/iimiiriuui S. typhi mu ri 11 ni Human

Ν) Ν)

221

V-BPO may also be an important difference between the bromoperoxidase and the chloroperoxidases/acid phosphatases.


A Conserved Active Site; Consequences for the Acid Phosphatases The common architecture of the active sites of enzymes carrying domains 1, 2 and 3 may have important consequences for research in the acid phosphatase field since for none of these enzymes structural data are available Figure 4 shows a dendrogram which is based on the alignment of the complete protein sequences. It should be noted that by using this approach not all domains 1, 2 and 3 are aligned. It does enable us however, to recognise the different protein families that together constitute a newly identified superfamily. Since a histidine is ligating the vanadate in the vanadate-containing haloperoxidases and apparently the phosphate substrate in the phosphatases we propose to call this superfamily the histidine phosphatase/peroxidase superfamily. Inspection of Figure 4 reveals a bias towards (putative) membrane bound proteins in this superfamily. Until now the only groups (marked by an S in Figure 3) that are shown to consist of soluble proteins are the vanadate-containing haloperoxidases and the non-specific bacterial acid phosphatases (20). A New Membrane Topology for Glucose-6-Phosphatase The knowledge that domains 1, 2 and 3 should be in close contact in order to constitute an active site can be an extra tool in determining the membrane topology of the membrane-bound enzymes contained in the superfamily. We have recently used this knowledge to predict a new membrane topology for the mammalian glucose-6-phosphatase (G-6Pase) family (21). Glucose-6-phosphatase (G-6-Pase) is an enzyme tightly associated with the endoplasmatic reticulum (ER) and nuclear membranes of liver and kidney cells (22) and based on its hydropathy profile six membrane-spanning helices were predicted (23, 24). G-6-Pase catalyses the last step in both gluconeogenesis and glycogenolysis and as such it is the key enzyme in glucose homeostasis (22). G-6Pase is also known to be efficiently and competitively inhibited by vanadate. This fact may well be a factor contributing to the insulin mimetic effect of vanadate. Glycogen storage disease type 1 (von Gierke disease) is an autosomal recessive disorder -with an incidence of about 1:100, 000 in humans- that is the consequence of the absence of G-6-Pase activity. This disorder is characterised by severe clinical manifestations such as hypoglycemia, growth retardation, hepatomegaly, kidney enlargement, hyperlipidemia, hyperuriceamia and lactic acidosis (25, 26). Without dietary treatment patients suffering from this disease die early, usually in their teens, of liver and kidney complications (27). Four missense mutations in the gene encoding human G-6-Pase were recently identified in patients (23). A subsequent nearsaturation mutagenesis study (28) revealed that A r g was absolutely required for enzyme activity. In our alignment (see figure 1) A r g corresponds to A r g of V-CPO, a residue donating hydrogen-bonds to vanadate. Since it is known that a histidine is the phosphate acceptor during catalysis of G-6-Pase the authors (28) also mutated 4 conserved histidines predicted to reside on the same (luminal) side of the ER membrane as Arg . H i s turned out to be the only histidine absolutely required for phosphatase activity. This is in agreement with our alignment since H i s " of G-6Pase corresponds to His of V-CPO, a residue which may function as an acid-base group in catalysis (77). H i s of G-6-Pase was not mutated but we predict that mutation of this residue will also abolish enzyme activity. H i s of G-6-Pase corresponds to H i s of V-CPO, the residue covalently linking the metal. It is likely therefore, that in G-6-Pase His , and not His as suggested (28), is the phosphate acceptor. Consequently, A r g , His and H i s of G-6-Pase have to reside at the same side of the ER membrane. 83

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Protein

Accession

S.cerevisiae

Pred. T M prot

S.cerevisiae

YDR5()3c

Pred. T M prot

C.elegans

T28D9.3

Wunen

Drosophila

U73822

ER T M prot.

Rat

Y07783

Transi. c D N A

Human

U79294

H 0 ind. prot

Mouse

L43371

PAP 2

Rat

U90556

PAP 2

Mouse

D84367

0RF2

D. mobilis

X06190

0RF8

R. erythropolis

Z82(X)5

0 R F 8(2)

R. erythropolis

Z82004

V-CPO

E. didymospora Y l 1877

V-CPO

D. biseptata

unpublished

V-CPO

C. inaequalis

S53117

Acid Phos.

Ζ mobilis

Ρ14924

Acid Phos.

S. typhimurium P26976

Apyrase

Sh.flexneri

U04539

Acid Phos.

P. stuartii

X64820

A c i d Phos.

Ph. morganii

P28581

PGPB

H. influenzae

1075131

PGPB

E. coli

G67260

Hyp. prot

M.janischii

Q57819

2


Species

Pred. T M prot

2

YDR284C

BcrC (permease)/?, licheniformis P42334 Hyp. prot

B. subtilis

BcrC like prot. E. coli Mig-13

Z82987 AEÎXXJ186

S. typhimurium AF020809

His. kinase

L. lactis

U81489

0RF2

B. megaterium

Z21972

Pred. T M prot

S.cerevisiae

P53223

G-6-Pase

Rat

P35575

G-6-Pase

Mouse

U91573

G-6-Pase

Human

P35575

G-6-Pase

Dog

U91844

T13C5.6 prot

C. elegans

U39648

Phosphatase

T. denticola

L25421

YodM

B. subtilis

AF015775

Figure 4. Dendrogram of proteins containing the conserved domains 1, 2 and 3. The dendrogram is based on a Clustal W alignment (default parameters) using the complete protein sequences.


223 Figure 5 shows our new model for the membrane topology of G-6-Pase which is based on the presented evidence concerning the nature of the G-6-Pase active site and the results of two new algorithms for the prediction of membrane-spanning domains (29-32). These algorithms independently predict nine transmembrane helices in G-6Pase as opposed to the previous topology model (23, 24). With this newly predicted topology all residues aligning to the active site residues of V-CPO are situated on the same -luminal- side of the ER-membrane. We propose therefore that helices II, III. IV and V are in close contact and provide the glucose-6-phosphate binding and hydrolysis site of G-6-Pase. In our model H i s of G-6-Pase is the nucleophile forming the phosphohistidine enzyme-substrate intermediate. The phosphate moiety is positioned by interaction of the negatively charged oxygens with the positively charged Lys , A r g and A r g . while analogous to V-CPO Ser and Gly may also donate hydrogen bonds. H i s " may provide the proton needed to liberate the glucose moiety. 176

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Drosophila Protein Wunen Another Membrane Bound Phosphatase Another important protein family shown in figure 3 is that of which Wunen (33) and plasma membrane bound (type 2) phosphatidic acid phosphatase PAP2 (34) are members. Wunen is a Drosophila protein that is responsible for the guiding of germ cells in embryonic development from the lumen of the developing gut towards the mesoderm were they enter the gonads (33). Until now nothing is known about the enzymatic activity of Wunen but the occurrence of domains 1, 2 and 3 (see figure 1) and its high similarity to PAP2 -also containing domains 1, 2 and 3- (see figure 1) suggests that Wunen like PAP2 is an acid phosphatase. Research on P A P has recently received an important impetus with the recognition that its enzymatic activity is not only involved in glycerolipid biosynthesis but that by balancing the levels of the two lipid second messengers diacylglycerol and phosphatidic acid it may also play in important role in signal transduction (see (35) and references therein). It should be noted that the predicted membrane topology of Wunen and PAP2 (33, 34) is in agreement with a phosphatase active site consisting of the amino acid residues provided by domains 1, 2 and 3. V-CPO and the High Molecular Weight Acid Phosphatases; A Similar but not Conserved Active Site. The above presented data indicate that the vanadium-containing haloperoxidases and the phosphatases with a homologous active site have divergently evolved from a common ancestor. Strikingly, the opposite -convergent evolution- also seems to have occurred since the active site of V-CPO resembles that of another class of acid phosphatases -the high molecular weight acid phosphatases (HMWAPs)- both in geometry and in residues contributing to the active site. In this context however, it is important to stress that no sequence similarity is found with this class of enzymes. The resemblance is most evident from the crystal structure of the active site of rat prostatic acid phosphatase complexed with vanadate (36) which is bound in the same trigonal bipyramidal geometry as in V-CPO. This co-ordination is analogous to the transition state in the reaction mechanism of several phosphatases (37). Furthermore, in rat prostatic acid phosphatase the vanadate is also covalently linked to a histidine (His ) while Arg , Arg , A r g and His are within hydrogen-bonding distance. The binding of vanadate to His gives crystallographic evidence for the proposed role of a histidine as a nucleophile in the formation of the phosphoryl adduct (37). Our data suggest that such a role can also be fulfilled by His in apo-CPO and thus most probably also by the corresponding histidines of the phosphatases contained in the alignment. 12

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Figure 5. Newly proposed nine transmembrane helix topology model for G6-Pase. Residues predicted to be on the membrane interface are depicted as open ovals. Putative G-6-Pase active site residues are depicted as open circles.


225 A Role of Aspartate in Peroxidase/Acid Phosphatase Catalysis? High molecular weight acid phosphatases also contain an aspartate residue in their active site. Mutational studies on this residue (Asp ) in rat prostatic acid phosphatase and the corresponding Asp in E. coli acid phosphatase indicated that this residue is involved in the protonation of the leaving group in the phosphatase reaction (38, 39). Strikingly, an aspartate residue (Asp ) is also found in the active site of V-CPO and both its position and the preliminary results of the analysis of an Asp -Ala mutation -which is produced using our S. cerevisiae expression system- indicate that this residue also has an important role in V-CPO catalysis. In the alignment however no conserved aspartate is found implying either that such a residue is not important for the catalytic mechanism of the aligned acid phosphatases or that it is contained in a stretch of non conserved residues. Considering the very low degree of sequence conservation outside the conserved domains in the histidine phosphatase/peroxidase family, we consider the latter explanation more likely. In this context it may be important to note that D -V mutations are identified in French patients suffering from von Gierke disease (40). In the six transmembrane helix topology model this residue was situated in the middle of the predicted first transmembrane helix. In the newly proposed topology model this residue is situated in the NH -terminal loop at the luminal side of the ER membrane. It is thus very well possible that this loop folds on to the active site and that Asp of G-6-Pase fulfils a role similar to that of Asp of V-CPO. 258

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3S

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3S

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Concluding Remarks. It is just two years ago when we first realised that the active site histidines of "our" V-CPO were conserved in two regions of the secreted class A bacterial acid phosphatases and thus that the vanadate-containing haloperoxidases were not such an odd group of enzymes as we thought they were. Since then many surprising homologues have been identified in species ranging from E. coli to human. Since structural data are absent for these enzymes and off course since many of the proteins have still unidentified functions, recognition of the three domains gives insight into the nature and the structure of the active sites. Furthermore, in the case of membrane proteins -of which there seem to be many in this protein family- positioning of the domains may lead to proposals for the membrane topology model as we showed for G-6-Pase. Acknowledgments This work was supported by the Netherlands Foundation for Chemical Research (SON) and was made possible by financial support from the Netherlands Organisation for Scientific Research (NWO) and the Netherlands Technology Foundation (STW) and the Netherlands Association of Biotechnology Centres (ABON). Literature Cited (1) Wever, R. In Biochemistry of Global Change; Oremland, R. S., Ed.; Chapman and Hall: New York, 1991, p 811-824. (2) Vilter, H. In Metal ions in Biological systems; Sigel, H., Sigel, Α., Eds.; Marcel Dekker, Inc: New York, Basel, Hong Kong, 1995; Vol. 31, p 326-362. (3) Vollenbroek, E. G. M.; Simons, L. H.; Van Schijndel, J. W. P. M.; Barnett, P.; Balzar, M.; Dekker, H. L.; Van der Linden, C.; Wever, R. Biochem. Soc. Trans. 1995, 23, 267-271. (4) Plat, H.; Krenn, Β. E.; Wever, R. Biochemical J. 1987, 248, 277-279.



226 (5) Hager, L. P.; Morris, D. R.; Brown, F. S.; Eberwein, H. J. Biol. Chem. 1966, 241, 1769-1777. (6) Zeng, J.; Fenna, R. E. J. Mol. Biol. 1992, 226, 185-207. (7) Vilter, H. Phytochemistry 1984, 23, 1387-1390. (8) De Boer, E.; Van Kooyk, Y.; Tromp, M. G. M.; Plat, H.; Wever, R. Biochim. Biophys. Acta 1986, 869, 48-53. (9) van Schijndel, J. W. P. M.; Barnett, P.; Roelse, J.; Vollenbroek, E. G. M.; Wever. R. Eur. J. Biochem 1994, 225, 151-157. (10) Simons, L. H.; Barnett, P.; Vollenbroek, E. G. M.; Dekker, H. L.; Muijsers, A. O.; Messerschmidt, Α.; Wever, R. Eur. J. Biochem. 1995, 229, 566-574. (11) Messerschmidt, Α.; Wever, R. Proc. Natl. Acad. Sci. USA 1996, 93, 392-396. (12) Barnett, P.; Kruidbosch, D. L.; Hemrika, W.; Dekker, H. L.; Wever, R. Biochim. Biophys. Acta 1997, 1352, 73-84. (13) Hemrika, W.; Renirie, R.; Dekker, H. L.; Barnett, P.; Wever, R. Proc. Natl. Acad. Sci. USA 1997, 94, 2145-2149. (14) Tromp, M. G. M.; Van, T. T.; Wever, R. Biochim. Biophys. Acta 1991, 1079, 5356. (15) Stankiewicz, P. J.; Tracey, A. S.; Crans, D. C. In Metal Ions in Biological Systems; Sigel, H., Sigel, Α., Eds.; Marcel Dekker, Inc: New York, Basel, Hong Kong, 1995; Vol. 31,p660-662. (16) Stukey, J.; Carman, G. M. Protein Sci. 1997, 6, 469-472. (17) Neuwald, A. F. Protein Sci. 1997, 6, 1764-1767. (18) Barnett, P.; Hondmann, D. H.; Simons, L. H.; Ter Steeg, P. F.; Wever, R. In International Patent Application (PCT) WO 95/27046 1995. (19) Messerschmidt, Α.; Prade, L.; Wever, R. Biol. Chem. 1997, 378, 309-315. (20) Thaller, M. C.; Berlutti, F.; Schippa, S.; Lombardi, G.; Rossolini, G. M. Microbiol. 1994, 140, 1341-1350. (21) Hemrika, W.; Wever, R. FEBS Lett. 1997, 409, 317-319. (22) Nordlie, R. C.; Sukalski, K. A. In The Enzymes of Biological Membranes; Martosoni, A. N., Ed.; Plenum Press: New York, 1985; Vol. 2nd Ed.,p349-398. (23) Lei, Κ. J.; Shelly, L. L.; Pan, C. J.; Sidbury, J. B.; Yang Chou, J. Science 1993, 262, 580-583. (24) Shelly, L. L.; Lei, K. J.; Pan, C. J.; Sakata, S. F.; Ruppert, S.; Schutz, G.; Yang Chan, J. J. Biol. Chem. 1993, 268, 21482-21485. (25) Beaudet, A. L. In Harrison's Principle of Internal Medicine; Wilson, J. D., Braunwald, E., Isselbacher, K. J., Petersdorf, R. G., Martin, J. B., Fauci, J. S., Root, R. K., Eds.; McGraw-Hill: New York, 1991; Vol. 12th Ed., p 1854-1860. (26) Hers, H. G.; Van Hoof, F.; Barsy, T. In The Metabolic Basis of Inherited Diseases; Scriver, C. R., Beaudet, A. L., Charles, R., Sly, W. S., Valle, D., Eds.; McGraw-Hill, Inc.: New York, 1989,p425-452. (27) Lei, K.-J.; Chen, H.; Pan, C., -J.; Ward, J. M.; Mosinger, B.; Lee, E. J.; Westphal, H.; Mansfield, B. C.; Chou, J. Y. Nature Genetics 1996, 13, 203-209. (28) Lei, K. J.; Pan, C. J.; Liu, J. L.; Shelly, L. L.; Yang Chou, J. J. Biol. Chem 1995, 270, 11882-11886. (29) Hoffman, K.; Stoffel, W. Biol. Chem. Hoppe Seyler 1993, 347, 166-170. (30) Rost, B.; Sander, C. J. Mol. Biol. 1993, 232, 584-599. (31) Rost, B.; Sander, C. Proteins 1994, 19, 55-72. (32) Rost, B.; Sander, C. Proteins 1994, 20, 216-226. (33) Zhang, N.; Zhang, J., Purcell, K. J.,; Cheng, Y.; Howard, K. Nature 1996, 385, 64-67. (34) Kai, M.; Wada, I.; Imai, S.; Sakane, F.; Kanoh, H. J. Biol. Chem. 1996, 271, 18931-18938. (35) Kanoh, H.; Kai, M.; Wada, I. Biochim. Biophys. Acta 1997, 1348, 56-62. (36) Lindqvist, Y.; Schneider, G.; Vihko, P. Eur. J. Biochem. 1994, 221, 139-142. (37) Van Etten, R. L.; Hickey, M. E. Arch. Biochem. Biophys. 1977, 183, 250-259.


227


(38) Ostanin, Κ.; Saeed, Α.; Van Etten, R. L. J. Biol. Chem. 1994, 269, 8971-8978. (39) Porvari, K. S.; Herrala, A. M.; Kurkela, R.; Taavitsainen, P. Α.; Lindqvist, Y.; Schneider, G.; Vihko, P. T. J. Biol. Chem. 1994, 269, 22642-22646. (40) Chevalier-Porst, F.; Bozon, D.; Bonardot, Α.; Bruni, N.; Mithieux, G.; Mathieu, M.; Maire, I. J. Med. Genet. 1996, 33, 358-360.


Vanadium Compounds - ACS Publications - American Chemical Society

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