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J. Biol. Chem., Vol. 279, Issue 24, 25544-25548, June 11, 2004
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NMR Application Probes a Novel and Ubiquitous Family of Enzymes That Alter Monosaccharide Configuration*
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From the
Yusong-Gu, Gusong-Dong 373-1, Department of Chemistry and ¶Department of Biological Science, Korea Advanced Institute of Science and Technology, Daejon 305-701, Korea
Received for publication, February 24, 2004 , and in revised form, March 31, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONEXPERIMENTAL PROCEDURESRESULTS AND DISCUSSIONSREFERENCES |
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By exploiting nuclear magnetic resonance (NMR) techniques along with novel applications of saturation difference analysis, we deciphered the functions of the previously uncharacterized products of three bacterial genes, rbsD, fucU, and yiiL, which are part of the ribose, fucose, and rhamnose operons of Escherichia coli, respectively. We show that RbsD catalyzes the pyran to furan conversion of ribose, whereas FucU and YiiL are involved in the catalysis of the anomeric conversion of their respective sugars. It was observed that the anomeric exchange of only ribofuranose, not ribopyranose, occurs spontaneously in solution rationalizing its evolutionary incorporation into the nucleic acid. The RbsD and FucU proteins share sequence homology and belong to the same protein family that is found from eubacteria to human, whereas the YiiL homologues exist in archaebacteria and lower eukaryotes. These enzymes, including the galactose mutarotase, exhibit a certain degree of cross-specificity to structurally analogous sugars thereby encompassing all existing monosaccharides in terms of their reactivities. The ubiquitous presence of enzymes involved in the anomeric changes of monosaccharides highlights an importance of these activities in various cellular processes requiring efficient monosaccharide utilization.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONEXPERIMENTAL PROCEDURESRESULTS AND DISCUSSIONSREFERENCES |
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The
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anomeric change of a monosaccharide involving a pyran configuration is considered very slow, e.g. the rate of glucose mutarotation is 0.015 min-1 in water (1). The only known enzyme for such a process is galactose mutarotase (GalM of Escherichia coli), which accelerates the conversion between the - and -anomers of D-glucose and D-galactose (2–4) presumably by enhancing the efficiency of glycolysis. The enzymes involving sugar metabolism including glycosylation tend to be selective for the - or -anomer, and thus a slow anomeric conversion may cause a problem in utilizing sugar. There has been no report on proteins involving an – conversion of sugars other than glucose, perhaps because of the lack of a method for detecting mutarotation at equilibrium. The conventional methods can only detect a change in optical rotation caused by an equilibrium shift from either the - or -anomer, which requires a purified - or -anomer as a substrate (3).
Monosaccharides in general have - and -anomers of pyranose (six-membered ring, e.g. L-fucose and L-rhamnose) and often have additional - and -anomers of furanose (five-membered ring). D-Ribose, a key sugar moiety for the component of nucleic acids and ATP, exists in four different forms in solution, -pyranose (22%), -pyranose (58%), -furanose (7%), and -furanose (12%), with its open-chain form constituting less than 1% of the total ribose in solution. Ribose is transported as a -D-pyranoribose, which is the major form in solution and binds to the ribose-binding protein (RbsB) in the bacterial periplasm (5). However, the ribokinase (RbsK) involved in the next step of ribose metabolism recognizes -D-ribofuranose as a substrate (6). An apparent discrepancy in the substrate specificities for uptake and phosphorylation may require a novel component converting sugar anomers.
RbsD is a component of the rbs operon of E. coli (rbsDACBKR) (7–10), yet its function has not been clearly elucidated. The only clue to the biological function of RbsD was obtained with a mutant glucose transporter (ptsG) that allowed the uptake of ribose at a lower rate (11). Only when ribose is transported into E. coli by this inefficient transporter is the presence of RbsD critical. This is because the limited availability of ribose cannot support metabolism without RbsD. RbsD is weakly homologous to FucU, a component of the fucose operon, the function of which is also unknown. Both have been classified in the RbsD/FucU family of proteins. Members of this family are ubiquitous having been found in organisms from eubacteria to mammals (12). YiiL is an open reading frame of E. coli found in the rhamnose operon without any suspected function even with its homologs in other organisms including archaebacteria and eukaryote.
The mutarotase seems to be critical in supporting fast energy generation by an organism when the substrate preference of metabolic enzymes for import or isomerization/phosphorylation is biased toward a specific anomer. Indeed, an uptake preference was reported for an -anomer of N-fluoro-N-deoxy-D-glucose derivatives, which is incorporated 2.5-fold times more rapidly than its -anomer (13). Although sugar utilization is crucial for the survival of the cell, nothing is known about the anomeric conversion and its metabolic implication for D-ribose, L-fucose, and L-rhamnose. Here, we characterize the functions of three E. coli genes, rbsD, fucU, and yiiL as mutarotases involved in the metabolism of these monosaccharides. These findings may demonstrate an importance of anomeric change in sugar utilization.
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EXPERIMENTAL PROCEDURES |
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TOPABSTRACTINTRODUCTIONEXPERIMENTAL PROCEDURESRESULTS AND DISCUSSIONSREFERENCES |
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Cloning and Protein Purification—The genes encoding RbsD, FucU, YiiL, and RbsK were cloned with their termination codons into a pET21a vector (Novagen, NdeI/XhoI) expressing intact forms of proteins without an attached tag. The N terminally His-tagged FucU was constructed with the pQE30 vector (Qiagen, BamH1/PstI). All proteins were expressed in an E. coli strain (BL21 DE3), and the His-tagged forms were purified with a nickel-nitrilotriacetic acid column (Qiagen). The intact forms were purified using the HiTrap-Q column (Amersham Biosciences) after ammonium sulfate precipitation, followed by gel permeation chromatography using Superdex 75 (Amersham Biosciences).
Determination of Molecular Weight—Gel permeation chromatography was carried out using Biosep Sec-S3000 HPLC column (Phenomenex, 300x7.8 mm). All experiments were performed at room temperature in the buffer solution (pH 7.5) containing 2 mM dithiothreitol, 50 mM sodium phosphate, and 100 mM sodium chloride. The molecular weights were estimated from the retention times of the molecular size markers: aldolase, 11.58 min; dimer of bovine serum albumin, 11.41 min; bovine serum albumin, 14.61 min; cytochrome c, 14.70 min; ubiquitin, 14.81 min.
Leaking Assay for D-Ribose—Cells were harvested after growth in M9 medium with 0.4% glycerol and then were washed and resuspended in the buffer (pH 7.0, 10 mM sodium phosphate buffer). [14C]D-Ribose (DuPont, 51.1 mCi/mM, 2 mM) was added to a final concentration of 2.0 µM. After incubation at 30 °C for 20 min, the sugar was diluted to 1:1000 with cold D-ribose. Aliquots were sampled through filtration and washing with the same buffer by using a 0.45-mm pore size nitrocellulose filter (Amicon) at different time intervals. The radioactivity was measured in a scintillation mixture after drying.
Saturation Difference Experiment—All NMR spectra were recorded in 99% D2O buffer (pH 7.5, 50 mM sodium phosphate and 100 mM sodium chloride) with the Varian UNITY INOVA instrument (600 MHz), in which the ligand to protein ratio was fixed to 200. The first and second free induction decays were obtained by presaturating the selected peak (H1' peak of the - or -anomer) and a 0.12 ppm neighborhood with a 180-degree shift of the receiver phase, respectively. As a result, only a saturated peak was observed in the absence of a chemical exchange among the anomers. However, the equivalent peaks of different anomers are also included for comparison in cases where the chemical exchanges are observed.
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RESULTS AND DISCUSSIONS |
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TOPABSTRACTINTRODUCTIONEXPERIMENTAL PROCEDURESRESULTS AND DISCUSSIONSREFERENCES |
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Characterization of RbsD as Pyranase—Previous demonstration of mutarotase activities was made through the change of optical rotation (3), requiring a specific purified anomer. This allowed a measurement of only unidirectional conversion rate. Here, we exploited a one-dimensional saturation difference (SD1) NMR technique for analyzing conversions between specific sugar isoforms as well as a one-dimensional saturation transfer difference (STD) technique (14) for monitoring sugar binding to the target protein (Fig. 1). The specific line-broadening (Fig. 2A, top) for the peaks of
-ribofuranose/-ribopyranose as well as the STD spectrum by RbsD (Fig. 2A, middle, 0.5 versus 5 s) revealed that RbsD binds specifically to the -furan and -pyran forms of ribose. The peak of the STD spectrum obtained with a shorter saturation time indicates a direct association of the monosaccharide, for in such condition, the effects of T1-relaxation time and the secondary saturation transfer through the chemical exchange are minimized. The appearance of the -furanose peak in the STD spectrum is because of a fast spontaneous exchange between the - and -ribofuranoses (see below). RbsK specifically binds to ribofuranose, perhaps with a preference for the -furan form (Fig. 2A, bottom, 0.5 versus 5 s), which is consistent with the x-ray crystallography results (6).
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RbsD considerably increases the exchange rate between
-ribofuranose and -ribopyranose (Fig. 2B), which was also confirmed by two-dimensional nuclear Overhauser effect spectroscopy (Fig. 2C) and two-dimensional total correlation spectroscopy experiments (data not shown). The same signed peaks shown by saturation in all spectra indicate that they originated from the chemical exchanges. RbsD catalytically and specifically reduces the activation energy barrier between these two forms of ribose, because the saturation transfer from one peak to another mainly depends on the chemical exchange between two exchangeable states that are at equilibrium. Because the substrate for RbsK is -ribofuranose, we believe that the activity of RbsD on its -ribopyranose substrate is crucial in cells that are actively utilizing ribose.
Spontaneous Interconversion of Ribofuranoses and Its Evolutionary Implication—As indicated in the previous STD spectrum (Fig. 2A), the fast spontaneous conversion between - and -ribofuranoses was observed, which appears to play a role in enhancing the substrate availability of RbsK. This fast exchange between - and -ribofuranoses was also confirmed by SD (Fig. 2B, blue) and two-dimensional nuclear Overhauser effect spectroscopy experiments (Fig. 2C-1) performed in the absence of the RbsD protein. The furanose is likely to have a lower energy barrier for ring opening than pyranose. We also observed the fast exchange between the - and -furans of ribose 5-phosphate and among the -furan, -furan, and linear forms of ketoses (D-xylulose and D-ribulose), the intermediates of sugar catabolism.
It is tempting to speculate that the evolutionary choice of ribofuranose as a component of nucleic acids might have resulted from the advantage gained by its fast exchange rate between - and -anomers. It was shown that DNA with a pyranose moiety, 2'-deoxy-D-allose, forms a more stable DNA duplex (4'–6' linkage) because of the fact that pyranose forms more rigid backbone than furanose. In contrast, RNA containing D-allose is unstable because of the steric hindrance from the bulk pyranose ring. Thus, it is conceivable that the furan backbone was energetically favored in the RNA world (15). Kinetically, pyranoses have very slow anomeric exchange rates (1) causing a difficulty in incorporating the -configuration during the prebiotic sugar-base coupling. However, the anomers of furanose inherently have fast exchange rates and thus either the -or -anomer can be properly selected during the reaction.
Effect of RbsD and RbsK on the Leakage of D-Ribose from the Cell—The effect of RbsD in vivo is achieved either by an enhancement of ribose uptake (data not shown) or an attenuation of sugar leakage (11). The leakage of D-ribose from E. coli cells decreases with the presence of RbsD, irrespective of RbsK (Fig. 3). The positive effect of RbsK on attenuating ribose leakage was expected, because this protein catalyzes the phosphorylation of ribose to ribose 5-phosphate, which is impermeable to the lipid membrane. It was reported that imported galactose easily leaks out of the cell when its kinase is impaired (16). It seems likely that the sugar concentration in the periplasm is maintained at a specific concentration by an active influx of the sugar from the medium into the cell and by a considerable amount of leakage of the sugar from the cytoplasm when RbsD and/or RbsK are absent. Thus, the absence of RbsD and RbsK leads to an initial burst of sugar leakage, which might be due mainly to the sugar leakage from the periplasm, because the outer membrane is more permeable to sugars than the inner membrane. We observed that the effect of RbsD on leakage is much smaller than the effect of RbsK presumably because the former is involved in a more reversible change than the latter (that is anomeric conversion versus phosphorylation).
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Residues Involved in the Pyranase Activity—The mechanism of mutarotation was investigated recently with the E. coli galactose mutarotase (3), in which the rate-determining step in the reaction is the protonation of O-5 and deprotonation of the OH group in the C-1 position, resulting in a ring-breakage. The prime candidate for this activity is a histidine residue (pKa
6.0). E. coli RbsD contains two conserved histidine residues, His-20 and His-106, which were mutated to alanines (H20A and H106A). Although His-20 is highly conserved in RbsD/FucU family members, His-106 is variable in the FucU subgroup. The mutant proteins were able to form an oligomer as is the case for the wild type, which was confirmed by gel permeation chromatography (Table I). The STD analysis indicates that both mutants bind to ribose as much as the wild type does (Fig. 4A, top). The H20A change completely abolished the pyranase activity, whereas H106A retained one-third of the original activity (Fig. 4A, bottom), which is consistent with the results of ribose utilization on minimal plates (Fig. 4B). The results are expected from the structure of Bacillus subtilis RbsD (12) indicating that His-20 in RbsD is in close proximity to the O-4 position of ribopyranose, and His-106 is in close proximity to the OH at C-1 position of ribopyranose. The mechanism is proposed in Fig. 4C.
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FucU Exhibits Mutarotase and Pyranase Activities—Using the same NMR techniques, we assessed the role of E. coli FucU in L-fucose metabolism. It was suspected that L-fucose is a ligand for FucU, because the exchange rate between
- and -fucopyranoses without FucU was too slow to be detected by our SD NMR technique (Fig. 5A). We discovered that FucU binds to both - and -fucopyranose and accelerates the conversion between them. The kcat/Km (M-1·sec-1) of FucU for the - and -forms was roughly estimated from our SD experiments as 65,100 ± 970 and 27,900 ± 420, respectively.2 With this technique, we were able to measure the enzymatic constants for both anomeric forms at the same time. Although RbsD did not show any activity for L-fucose as a substrate (data not shown), FucU exhibited a pyranase activity for D-ribose (Fig. 5B). The pyranase activity of FucU for ribose is roughly half that of RbsD, although the degree of sugar binding is similar (data not shown). The mutarotase and pyranase activity of FucU was also confirmed by two-dimensional nuclear Overhauser effect spectroscopy experiments (data not shown).
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Configuration of Sugar OH Group Determines the Specificity of Mutarotases—Because sugars are first metabolized by their isomerases and kinases, the mutarotases (aldose 1-epimerases) have to be coupled with these enzymes (2, 3, 9, 17) in terms of their substrate specificities. From the analysis of specificities for monosaccharide substrates reported previously for a variety of isomerases, we realized that the ability of one isomerase for several monosaccharides is common and that both isomerase (data not shown) and mutarotase activities are categorized according to their substrate configurations (Table II). The structures of all monosaccharides are presented here in terms of their differences from the D-ribopyranose backbone. D-Allose, an analogue of ribopyranose, is also a substrate for the pyranase (supplemental Fig. 1). Here, -allopyranose binds to RbsD, in which the conversion is between -allofuranose and -allopyranose. The metabolic pathways of allose and ribose are intertwined in E. coli by sharing a common regulator, alsR (or rpiR), for the expression of the rpiB gene (or alsI), which encodes ribose phosphate isomerase (or allose isomerase) (18, 19). It was reported also that L-galactose and D-arabinose could be metabolized through the L-fucose pathway (20), which belongs to the same category in Table II. This indicates that sugars with the same orientations of OH groups are likely to utilize the same metabolic pathway.
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Prediction of YiiL as Mutarotase—Our efforts to catalog the substrate specificities of all mutarotase activities revealed two groups of orphan sugars that differ at the C-3 or -4 position. Mutarotase reactions with the C-3 group, which comprises D-xylose, D-quinovose, and D-glucose, appear to be catalyzed by galactose mutarotase (3). In eubacteria, D-glucose is imported using the phosphoenolpyruvate-glucose phosphotransferase system, which couples transport with phosphorylation without the need of mutarotase activity. The poor catalytic activity of Lactococcus lactis GalM (3) for sugars with different C-3 configurations may be because of the existence of the PTS system. Interestingly, human aldose 1-epimerase, a GalM counterpart, exhibits higher activity with D-glucose than with D-galactose (2). However, the C-4 group, which comprises L-lyxose, L-rhamnose, and L-mannose, was not utilized by any of the known mutarotases. When we inspected genes in the rhamnose operon, we found an interesting candidate of the mutarotase gene, yiiL. Using the SD NMR technique (Fig. 5C), we observed that the protein indeed mediates the
– conversion of rhamnose.
Novel Family of Mutarotases from Bacteria to Higher Eukaryotes—In this study, we were able to determine the enzymatic functions of the RbsD, FucU, and YiiL proteins and bestow on them the names of pyranase, type-II mutarotase, and type-III mutarotase, respectively, with the galactose mutarotase being type-I enzyme. These three mutarotases are structurally distinct, because both the sizes (galactose mutarotase GalM, 346 amino acids; FucU, 140 amino acids; and YiiL, 104 amino acids) and oligomeric states differ (Table I). RbsD/FucU and YiiL seem to require multimeric or dimeric structures for their enzymatic activity, because the N terminally His-tagged FucU is an inactive monomer. In addition, the pyran-furan conversion is considered unique from other types of mutarotation (e.g. – conversion of pyranose), although their underlying chemistries are the same.
There are a number of RbsD/FucU isoforms in the mouse and human that are generated by alternative splicing, which are more closely related to FucU than to RbsD (supplemental Fig. 2). L-Fucose is an indispensable sugar in higher eukaryotes and is involved in a variety of cellular processes including cell surface recognition, glycosylation, and signaling. The lack of fucosylation is caused by genetic disorders (21, 22), whereas its increase is observed in cancer cells (23). The presence of an RbsK homolog in human cells may suggest the presence of RbsD activity in human cells. It is known that human blood contains 100 µM ribose that can be used as an effective energy source without accumulating lactate. A therapeutic role of ribose in ischemia was also reported (24, 25), perhaps because the ribose metabolism achieves fast supply of ATP. Delineating the cellular functions of eukaryotic FucU homologs would be a future challenge.
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FOOTNOTES |
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* This work was supported in part by the Creative Research Initiative Program and Grant BK21 (to C. P. and B.-S. C.). 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.
The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. 1 and 2.
Supported by the BK21 project.
|| Both authors contributed equally to this work.
** To whom correspondence may be addressed. Tel.: 82-42-869-2828; Fax: 82-42-869-2810; E-mail: byongseok.choi{at}kaist.ac.kr. To whom correspondence may be addressed. Tel.: 82-42-869-2629; Fax: 82-42-869-2610; E-mail: ckpark{at}kaist.ac.kr.
1 The abbreviations used are: SD, saturation difference; STD, saturation transfer difference.
2 K.-S. Ryu, C. Kim, I. Kim, S. Yoo, B.-S. Choi, and C. Park, manuscript submitted.
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONEXPERIMENTAL PROCEDURESRESULTS AND DISCUSSIONSREFERENCES |
|---|
- Livingstone, G., Franks, F., and Aspinall, L. J. (1977) J. Solution Chem. 6, 203-216
- Timson, D. J., and Reece, R. J. (2003) FEBS Lett. 543, 21-24[CrossRef][Medline] [Order article via Infotrieve]
- Thoden, J. B., Kim, J., Raushel, F. M., and Holden, H. M. (2002) J. Biol. Chem. 277, 45458-45465
[Abstract/Free Full Text] - Thoden, J. B., Kim, J., Raushel, F. M., and Holden, H. M. (2003) Protein Sci. 12, 1051-1059[CrossRef][Medline] [Order article via Infotrieve]
- Mowbray, S. L., and Cole, L. B. (1992) J. Mol. Biol. 225, 155-175[CrossRef][Medline] [Order article via Infotrieve]
- Sigrell, J. A., Cameron, A. D., and Mowbray, S. L. (1999) J. Mol. Biol. 290, 1009-1018[CrossRef][Medline] [Order article via Infotrieve]
- Willis, R. C., and Furlong, C. E. (1974) J. Biol. Chem. 249, 6926-6929
[Abstract/Free Full Text] - Iida, A., Harayama, S., Iino, T., and Hazelbauer, G. L. (1984) J. Bacteriol. 158, 674-682
[Abstract/Free Full Text] - Izumori, K., Rees, A. W., and Elbein, A. D. (1975) J. Biol. Chem. 250, 8085-8087
[Abstract/Free Full Text] - Park, Y., Cho, Y. J., Ahn, T., and Park, C. (1999) EMBO J. 18, 4149-4156[Medline] [Order article via Infotrieve]
- Oh, H., Park, Y., and Park, C. (1999) J. Biol. Chem. 274, 14006-14011
[Abstract/Free Full Text] - Kim, M. S., Shin, J., Lee, W., Lee, H. S., and Oh, B. H. (2003) J. Biol. Chem. 278, 28173-28180
[Abstract/Free Full Text] - O'Connell, T. M., Gabel, S. A., and London, R. E. (1994) Biochemistry 33, 10985-10992[Medline] [Order article via Infotrieve]
- Mayer, M., and Meyer, B. (2001) J. Am. Chem. Soc. 123, 6108-6117[CrossRef][Medline] [Order article via Infotrieve]
- Eschenmoser, A. (1999) Science 284, 2118-2124
[Abstract/Free Full Text] - Horecker, B. L., Thomas, J., and Monod, J. (1960) J. Biol. Chem. 235, 1580-1585
[Free Full Text] - Korndorfer, I. P., Fessner, W. D., and Matthews, B. W. (2000) J. Mol. Biol. 300, 917-933[CrossRef][Medline] [Order article via Infotrieve]
- Kim, C., Song, S., and Park, C. (1997) J. Bacteriol. 179, 7631-7637
[Abstract/Free Full Text] - Poulsen, T. S., Chang, Y. Y., and Hove-Jensen, B. (1999) J. Bacteriol. 181, 7126-7130
[Abstract/Free Full Text] - Zhu, Y., and Lin, E. C. (1986) J. Mol. Evol. 23, 259-266[Medline] [Order article via Infotrieve]
- Becker, D. J., and Lowe, J. B. (2003) Glycobiology 13, 41R-53R
[Abstract/Free Full Text] - Freeze, H. H. (2001) Glycobiology 11, 129R-143R
[Abstract/Free Full Text] - Noda, K., Miyoshi, E., Gu, J., Gao, C. X., Nakahara, S., Kitada, T., Honke, K., Suzuki, K., Yoshihara, H., Yoshikawa, K., Kawano, K., Tonetti, M., Kasahara, A., Hori, M., Hayashi, N., and Taniguchi, N. (2003) Cancer Res. 63, 6282-6289
[Abstract/Free Full Text] - Foker, J. E. (August 12, 1986) U. S. Patent 4,605,644
- Foker, J. E. (January 12, 1988) U. S. Patent 4,719,201
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