N-glycosylation profile of recombinant human soluble Fc{gamma} receptor III

Noriko Takahashi2, Joel Cohen-Solal3, Annie Galinha3, Wolf Herman Fridman3, Catherine Sautès-Fridman3 and Koichi Kato1,2

2 Graduate School of Pharmaceutical Sciences, Nagoya City University, Mizuho-ku, Nagoya 467-8603, Japan; and 3 INSERM Unité 255, Centre de Recherches Biomedicales des Cordeliers, 15 rue de I’Ecole de Medecine, 75270 Paris, France

Received on March 6, 2002; revised on April 22, 2002; accepted on April 22, 2002


    Abstract
 Top
 Abstract
 Introduction
 Results
 Discussion
 Materials and methods
 Acknowledgments
 Abbreviations
 References
 
N-glycans of human Fc{gamma} receptor III (Fc{gamma}R III) are believed to be involved in the interaction with complement receptor type 3 (CR3) (Sehgal et al. [1993] J. Immunol., 150, 4571–4580). Recombinant human soluble Fc{gamma}RIII (rhsFc{gamma}RIII), which is produced in baby hamster kidney (BHK) cells, has been shown to interact with CR3 in a manner similar to native Fc{gamma}RIII. We elucidated the N-glycosylation profiles of rhsFc{gamma}RIII by the 3D high-performance liquid chromatography mapping technique. It was revealed that the N-glycans of rhsFc{gamma}RIII are much more divergent (consisting of 20 neutral, 7 monosialyl, 4 disialyl, 5 trisialyl, and 1 tetrasialyl oligosaccharides) than those previously determined for BHK-expressed mouse sFc{gamma}RII, notwithstanding close structural similarity of polypeptide chains between the two sFc{gamma}Rs. Particularly, high-mannose type oligosaccharides are specifically expressed on rhsFc{gamma}RIII.

Key words: BHK cell/N-glycan/soluble Fc{gamma} receptor/3D HPLC mapping


    Introduction
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 Abstract
 Introduction
 Results
 Discussion
 Materials and methods
 Acknowledgments
 Abbreviations
 References
 
Receptors for the Fc portion of IgG (Fc{gamma}R) are a heterogeneous family of transmembrane glycoproteins that mediate a variety of effector and regulatory functions in hematopoietic cells.

In mice and humans, three classes of Fc{gamma}Rs—Fc{gamma}RI, Fc{gamma}RII, and Fc{gamma}RIII—have been described (Fridman et al., 1992Go; Hulett and Hogarth, 1994Go). Fc{gamma}RI has high affinity for monomeric IgG, whereas Fc{gamma}RII and Fc{gamma}RIII exhibit low affinity for monomeric IgG but bind IgG-containing immune complexes with high avidity. Fc{gamma}RII and Fc{gamma}RIII possess similar extracellular regions composed of two Ig-like domains. There exist a variety of isoforms of the individual classes of Fc{gamma}Rs (Fridman et al., 1993Go). For example, isoforms for human Fc{gamma}RIII are transmembrane Fc{gamma}RIIIa and glycosylphosphatidylinositol (GPI)-linked Fc{gamma}RIIIb, coded by two separate genes. Some of those isoforms are expressed as soluble form (sFc{gamma}R) that consist of their extracellular domains produced by proteolytic cleavage (Huizinga et al., 1990Go; Sautès et al., 1991Go).

Human Fc{gamma}RIIIb and its soluble counterpart interact not only with IgG but also with cell surface receptors, such as complement receptor type 3 (CR3; CD11b/CD18) (Petty and Todd, 1993Go; Galon et al., 1996Go). It has been reported that the glycosylation of (s)Fc{gamma}RIII is involved in its interactions with classical (IgG) and nonclassical (CR3) ligands. Glycosylation of sFc{gamma}RIII plays an inhibitory role in the interaction with human IgG3 but not IgG1 (Galon et al., 1997Go; van den Nieuwenhof et al., 2000Go). On the other hand, the interaction with CR3 is mediated by carbohydrate moieties expressed on (s)Fc{gamma}RIII molecules (Sehgal et al., 1993Go; Galon et al., 1996Go). Although structural basis of the interactions between IgG and Fc{gamma}Rs has been provided by nuclear magnetic resonance spectroscopy (Kato et al., 2000Go) and X-ray crystallography (Sondermann et al., 2000Go; Radaev et al., 2001Go) by use of recombinant sFc{gamma}Rs, the role of Fc{gamma}RIII glycosylation in its binding of ligands has not been fully elucidated from structural aspects.

Therefore, to gain deeper insights into this question, human sFc{gamma}RIII expressed by an appropriate mammalian expression system are required. Expression systems to produce high amounts of recombinant sFc{gamma}Rs of eukariotic cell lines have been developed (Teillaud et al., 1994Go; Sautès et al., 1994Go). We have shown that recombinant human sFc{gamma}RIII (rhsFc{gamma}RIII), which is produced in baby hamster kidney (BHK) cells, conserve the ability to interact with CR3, which is comparable to that of native sFc{gamma}RIII purified from human serum (Galon et al., 1996Go). This strongly indicates that rhsFc{gamma}RIII and the native sFc{gamma}RIII glycoproteins carry common glycan structure(s) essential for interaction with CR3.

Here we report the N-glycosylation profile of rhsFc{gamma}RIII produced in BHK cells. By use of a 3D high-performance liquid chromatography (HPLC) mapping technique (Takahashi et al., 1995aGo, 1998; Tomiya et al., 1988Go), structures of N-glycans expressed on rhsFc{gamma}RIII have been determined throughout, discriminating possible isomers resulting from partial galactosylation and sialylation. The N-glycosylation profile thus obtained has been compared with that of recombinant mouse sFc{gamma}RII (rmsFc{gamma}RII) produced in BHK cells. Similarity and difference of the N-glycosylation profiles between rhsFc{gamma}RIII and rmsFc{gamma}RII are discussed in light of their function.


    Results
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 Abstract
 Introduction
 Results
 Discussion
 Materials and methods
 Acknowledgments
 Abbreviations
 References
 
Separation of N-glycans by three successive HPLC steps
The pyridylamine (PA)-glycans released from sFc{gamma}RIII were separated into neutral (N), monosialyl (MS), disialyl (DS), trisialyl (TS), and tetrasialyl (TeS) oligosaccharide fractions by DEAE-5PW column (first HPLC) (Figure 1A). All ionic charges in the sFc{gamma}RIII could be attributable to {alpha}-sialic acids, because all acidic fractions changed to neutral species after Arthrobacter {alpha}-sialidase digestion (data not shown).




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Fig. 1. PA-glycan separation leading to the 3D map. The neutral and sialylated PA-glycan mixture obtained from rhsFC{gamma}RIII was separated on two different columns. (A) By the first HPLC on the DEAE column, PA-glycans are separated according to their sialic acid content. (B) Each of the neutral (N) and monosialyl (MS), disialyl (DS), trisialyl (TS), and tetrasialyl (TeS) N-glycans was individually separated on the second, ODS column. The molar ratios of the N, MS, DS, TS, and TeS fractions were, respectively, 77.6, 15.7, 4.0, 1.5, and 1.2%. Those were calculated from their peak areas in the individual elution profiles on the ODS column, because neutral PA-glycans might pass through the DEAE column with contaminants.

 
Each of these fractions were applied to the octadecylsilica (ODS) column, using exactly the same chromatographic conditions for neutral and all sialylated derivatives (Figure 1B). The resulting fractions were numbered in order of elution time, that is, N10, MS1, or DS3. Each of the PA-labeled fractions thus coded was further fractionated by molecular size using the amide-silica column. The fractions separated on the amide-silica columns were alphabetically coded in order of elution time. N8 fraction was separated into N8a and N8b; N10 into N10a, N10b, and N10c; N11 into N11a, N11b, and N11c; and the monosialyl fraction MS3 into MS3a and MS3b. Other ODS fractions appeared as single peaks on amide-silica column (data not shown). Although disialyl DS5 could still not be resolved on this step, it contains two components that were unambiguously differentiated only after digestion with ß-galactosidase and ß-N-acetylhexosaminidase.

Identification of N-glycan structures
Structural assignment of all neutral and sialyl N-glycans from sFc{gamma}RIII was performed by 2D mapping technique, as described elsewhere (Takahashi et al., 1995aGo). Except for six compounds (monosialyl MS1, MS4, and MS5 and disialyl DS2, DS3, and DS5), coordinates of all N-glycans from sFc{gamma}RIII coincided with those of known N-glycans on the map. Therefore, they were tentatively assigned to the known N-glycans as shown in Table TI. Then, cochromatography on ODS and amide-silica columns of each of the sample PA-glycans with the corresponding reference compound confirmed those assignments. The coordinate sets of six compounds (monosialyl MS1, MS4, and MS5; disialyl DS2, DS3, and DS5) do not match, by direct comparison, with any of the reference compounds available on the 2D map accumulated prior to this study.





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Table I. N-Glycan structures of rhsFc{gamma}RIII.

F, Fuc; G, Gal; GalN, GalNAc; GN, GlcNAc; M, Man, S, Neu5Ac; R, Mß4GNß4(F{alpha}6)GN-PA; R', Mß4GNß4GN-PA.

 
Determination of novel sialyl N-glycan structures
It has been established that deciphering the {alpha}(2,6)- versus {alpha}(2,3)-sialylation can be made by the differential glucose unit (GU) changes of on the amide-silica column (Takahashi et al., 1995aGo,b). After sialidase digestion, its GU value on the amide-silica column increases by about 0.4/residue of Neu5Ac if Neu5Ac is {alpha}(2,3)-linked, but little change is observed for Neu5Ac{alpha}(2,6). Because GU changes on the amide-silica column on the sialidase treatment of the N-glycans from sFc{gamma}RIII were approximately + 0.4/residue of Neu5Ac, we concluded that all the Neu5Ac are {alpha}(2,3)-linked in this glycoprotein. After sialidase digestion, MS1 released sialic acid and changed into the known neutral triantennary compound 310.18, whereas MS4 as well as MS5 were converted into the known neutral tetraantennary compound 410.16 (Figure 2). To determine which branch was terminated with an {alpha}(2,3)-sialic acid residue, intact MS1, MS4, and MS5 were digested with ß-galactosidase and then with ß-N-acetylhexosaminidase. Because MS1 was expected to change into a monosialyl monoantennary compound on the 2D map, the resultant coordinates should coincide with one of the three possible references found in Figure 2B.




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Fig. 2. (A) The change of coordinates on the 2D map of PA-oligosaccharide MS1, MS4, and MS5. Starting materials, MS1, MS4, and MS5 were sequentially digested with {alpha}-(2,3)-sialidase (dashed-line arrows) or with ß-galactosidase and ß-N-acetylhexosaminidase (solid-line arrows). Open circles, unkown glycans; closed circles, reference compounds with the structures (B) shown.

 
The coordinates of MS1 changed from (12.0, 8.4) to (11.8, 5.6), indicating that the most reliable candidate is 1A2-110.4 (Figure 2). (When coordinates are cited in this article, they are always listed in the order of GU[ODS], GU[amide].) By cochromatography, we confirmed that the digestion product of MS1 is identical with 1A2-110.4 among the three possible candidates. On the basis of these data, we conclude that the position of sialylation in MS1 is at the Galß4GlcNAcß2Man{alpha}3 branch.

Similarly, the resultant compounds from the ß-galactosidase and ß-N-acetylhexosaminidase digestion of MS4 and MS5 were expected to be one of the following four monosialyl monoantennary compounds: 1A2-110.8, 1A2-110.4, 1A2-110.3, and 1A2-110.9 found in Figure 2B.

On the enzymatic treatments, the coordinates of MS4 and MS5 changed from (15.2, 9.7) and (15.6, 9.7) to (11.8, 5.6) and (14.3, 5.5), respectively (Figure 2). The strongest candidates among the four possible aforementioned structures were 1A2-110.4 (11.8, 5.6) for the digested MS4, and 1A2-110.3 (14.2, 5.5) for the digested MS5. By cochromatography, we confirmed that the digestion products of MS4 and MS5 are identical with 1A2-110.4 and 1A2-110.3, respectively, among the four possible candidates. On the basis of these data we conclude that the position of sialylation in these compounds, specifically, Galß4GlcNAcß2Man{alpha}3 branch in MS4 and Galß4GlcNAcß2Man{alpha}6 branch in MS5. The structures of MS1, MS4, MS5 thus identified are included in Table TI.

DS5 was converted into the known tetraantennary reference 410.16 on releasing sialic acids. ß-Galactosidase and ß-N-acetylhexosaminidase digestion of DS5 gave rise to two fractions, DSx (14.5, 6.6) and DSy (16.1, 6.6) at a molar ratio of 1:1 on the 2D map. Because any possible disialyl biantennary compounds as references were not available, the structures of DSx and Dsy could be only estimated to be that shown in Scheme S1 on the basis of GU differences computed from the contributions of each component monosaccharide unit in a specific position expressed in GU (Tomiya and Takahashi, 1998Go). These results indicated that DS5 was a 1:1 mixture of two disialyl tetraantennary compounds; see Scheme S2.



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Scheme 1. Proposed structures of DSx and Dsy.

 


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Scheme 2. Proposed structures of disiayl tetraantennary glycans constituting DS5.

 
In a similar way, it was revealed that DS2 and DS3, with prevalence of 0.7% and 0.6%, respectively, were disialyl tetraantennary compounds. However, because of the limited amount of the sample, the positions of the two sialic acid residues could not be unambiguously assigned.


    Discussion
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 Abstract
 Introduction
 Results
 Discussion
 Materials and methods
 Acknowledgments
 Abbreviations
 References
 
In the present article, we have identified 39 major N-glycan structures of rhsFc{gamma}RIII produced in BHK cells, which consist of 20 neutral (77.6%), 7 monosialyl (15.7%), 6 disialyl (4.0%), 5 trisialyl (1.5%), and 1 tetrasialyl (1.2%) oligosaccharides. Fourteen percent of the total N-glycans is of high-mannose type. The complex-type N-glycans are fucosylated exclusively by {alpha}(1,6) linkage and lack bisecting GlcNAc. Sialylation occurs through {alpha}(2,3) but not {alpha}(2,6) linkage. All of these features are consistent with those so far reported for glycoproteins expressed by BHK cells (Tomiya et al., 1993Go; Nimtz et al., 1993Go; Takahashi et al., 1998Go). GalNAc residue(s) were contained in 5.9% of the total N-glycans instead of terminal Gal residue, for example, N13 and MS6 in Table TI. This type of glycosylation has been observed for other recombinant glycoproteins produced in BHK cells but has never been found in those produced in Chinese hamster ovary cells most likely due to the absence of a functional ß4-GalNAc transferase (Tsuda et al., 1988Go). As reported previously, urinary kallidinogenase (Tomiya et al., 1993Go) and human urokinase (Bergwerff et al., 1995Go) produced in natural human kidney have plenty of GalNAc-containing N-glycans. It is possible that production of GalNAc-containing N-glycans is characteristic for kidney(-derived) cells.

In a previous publication, we determined 18 major N-glycan structures of rmsFc{gamma}RII (Takahashi et al., 1998Go). Figure 3 compares the N-glycosylation profile of rhsFc{gamma}RIII determined in the present study with that of rmsFc{gamma}RII by plotting all sample coordinates on the 2D map. Much more divergent N-glycan structures are exhibited by rhsFc{gamma}RIII than by rmsFc{gamma}RII. In particular, high-mannose type N-glycans (from N1 to N5 in Table TI, and Figure 3A) are expressed only by rhsFc{gamma}RIII. Furthermore, larger multiantennary complex type oligosaccharides are predominant in the rhsFc{gamma}RIII. Indeed, for rhsFc{gamma}RIII, the most abundant glycan is a typical tetraantennary N12 (18%) and the total content of tetraantennary group (including N12) is 43%. On the contrary, most of the oligosaccharides of rmsFc{gamma}RII are biantennary N-glycans and prevalence of tetraantennary glycan is only 0.9%.



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Fig. 3. Comparison of N-glycosylation profiles between rhsFc{gamma}RIII (A, B) and rmsFc{gamma}RII (C, D) on the 2D map. The elution positions of all neutral (A, C) and monosialyl (B, D) PA-glycans are expressed as GU. The common notations of the glycans were used between rhsFc{gamma}RIII and rmsFc{gamma}RII. The structures of glycans coded as 010.1 and 1A2-110.3 have been described in the literature (Takahashi et al., 1998Go). The glycans whose prevalence is more and less than 3% are represented with larger and smaller circles, respectively.

 
It has been reported that on human polymorphonuclear leukocytes, Fc{gamma}RIII, but not Fc{gamma}RII, expresses Conacavalin A binding and endoglycosidase H–sensitive oligosaccharides (Kimberly et al., 1989Go). On the basis of all these data, we suggest that expression of the high-mannose type oligosaccharides is specific for human Fc{gamma}RIII, and they can be at least partially reproduced in the recombinant soluble form produced by BHK cells.

The lectin-like site of CR3 has been shown to be responsible for binding to GPI-anchored Fc{gamma}RIII as well as to rhsFc{gamma}RIII (Stöckl et al., 1995Go; Galon et al., 1996Go). The lectin-like site of CR3 binds mannose-rich compounds such as zymosan (Ross et al., 1985Go), and the Fc{gamma}RIII-CR3 cocapping is inhibited by N-acetyl-D-glucosamine, {alpha}-methyl-D-mannoside, and D-mannose, but not by glucose, galactose, N-acetyl-neuraminic acid, fucose, sorbitol, fructose, nor sucrose (Yamamoto et al., 1989Go). Inhibitory effects by {alpha}- or ß-methyl-D-mannoside have been observed for the rhsFc{gamma}RIII-CR3 interaction (Galon et al., 1996Go). One intriguing possibility is that the interaction of CR3 with Fc{gamma}RIIIb involves the lectin-like region of CD11b and the high-mannose type oligosaccharide(s) characteristically exhibited by Fc{gamma}RIII.

The human sFc{gamma}RIII used in the present study possesses six possible N-glycosylation sites (positions 37, 44, 63, 73, 162, and 169), whereas mouse sFc{gamma}RII has four sites (positions 36, 63, 138, and 145). Thus most of the glycosylation sites are not conserved, although these two glycoproteins share 50% amino acid identity with each other. We suggest that the local environment (e.g., local conformational factors) surrounding the individual glycosylation sites affect the processing of the expressed glycans, resulting in differential overall glycosylation profiles between the two glycoproteins with close structural similarlity of polypeptide chains. If this is true, it is quite likely that different glycosylation sites in human Fc{gamma}RIII molecules exhibit different N-glycosylation profiles. Analyses of site-specific glycosylations of the recombinant human Fc{gamma}RIII is under way in our laboratory.


    Materials and methods
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 Abstract
 Introduction
 Results
 Discussion
 Materials and methods
 Acknowledgments
 Abbreviations
 References
 
Enzymes
Glycoamidase A (also known as glycopeptidase A) from sweet almond (Takahashi, 1977Go), ß-galactosidase and ß-N-acetylhexosaminidase from jack bean were purchased from Seikagaku Kogyo (Tokyo). Sialidase from Arthrobacter ureafaciens was obtained from Nacalai Tesque (Kyoto, Japan). Trypsin, chymotrypsin, and pronase were from Sigma (St. Louis, MO).

The PA-derivatives of isomalto-oligosaccharides (4–20 glucose residues) and of reference N-glycans (code numbers, M5.1, M6.1, M8.2, 110.1, 110.3, 210.1, 210.2, 210.3, 210.4, 310.8, 410.9, 410.12, 410.13, and 410.16) were purchased from Seikagaku Kogyo. (The known N-glycan structures are coded in "The Elution Coordinate Database for 2-D/3-D Sugar Map" [http://www.gak.co.jp/FCCA], which contains information of more than 400 kinds of N-glycans.) The following PA-glycans were prepared by known methods: M6.10 and M7.7 were obtained from M9.1 by jack bean {alpha}-mannosidase digestion (Tomiya et al., 1991); 410.42 was prepared from recombinant erythropoietin (Tomiya et al., 1993Go); 410.15 was from 3A5-410.16 by ß-galactosidase then sialidase digestion; 210.4b, 1A2-210.3, 1A3-210.4, 1A4-210.4, 1A2-210.4a1, 2A4-210.4, 3A2-310.18, 3A3-410.16, 3A5-410.16, 3A6-410.16, and 4A2-410.16 were from mouse sFc{gamma}RII (Takahashi et al., 1998Go); and 310.18, 2A3-310.18 and 3A4-410.16 were from human integrin (Nakagawa et al., 1996Go).

Preparation of sFc{gamma}RIII
The cDNA encoding the NA2 form of human Fc{gamma}RIII-B ectodomains (194-amino-acid-long including a 7-amino-acid C-terminal stop linker) was expressed in the BHK cell line. The rhsFc{gamma}RIII glycoprotein was purified by ion exchange and affinity chromatography as described (Sautès et al., 1994Go). Sodium dodecyl sulfate–polyacrylamide gel electrophoresis analysis showed that the material was 99% pure and migrated with apparent molecular mass 47 to 56 kDa.

Preparation of PA N-glycans from sFc{gamma}RIII and analysis by 3D HPLC mapping technique
One milligram of rhsFc{gamma}RIII was used as starting material. Experimental procedures of liberation and PA-derivatization of N-glycans and chromatographic conditions have been described in detail elsewhere (Nakagawa et al., 1995Go; Takahashi et al., 1995aGo). Briefly, sFc{gamma}RIII was proteolyzed with trypsin and chymotrypsin mixture. The proteolysate was further digested with glycoamidase A to liberate N-glycans. After removing the peptidic materials, the reducing ends of N-glycans were reductively aminated with a fluorescent reagent, 2-aminopyridine using sodium cyanoborohydride (Yamamoto et al., 2001Go).

The mixture of PA-oligosaccharides was separated by HPLC on a diethylaminoethyl (DEAE) column according to the sialic acid content. Each separated fraction was then applied to an ODS HPLC column. Then each of the fraction separated on the ODS column was applied to the amide-silica column for the separation on the basis of their sizes. The elution times of a given PA-oligosaccharides on ODS and amide-silica columns, both of which are calibrated in GUs, provide a unique set of coordinates on the 2D map. The coordinates of the PA-glycans originating from sFc{gamma}RIII were compared with those of the authentic reference compounds.

The GUs of all unknown N-glycans were first compared with those of the reference N-glycans on the 2D map. We then select a few references from the data as candidates whose coordinates coincided with those of the sample within allowable error (± 5%). The sample PA-glycan and each of the selected references were coinjected onto ODS and amide-silica columns. Identification was made judging whether they are eluted simultaneously giving a single peak on both HPLC profiles.

For further confirmation, the sample PA-glycan was digested with one or more exoglycosidases. At each step of the trimming, the elution positions of the resultant PA-glycans were examined as to whether they could be identified with the expected reference compound. The trimming and comparison was continued until the product from the sample compound became coincidental with a reference PA-oligosaccharide on the map.

Each PA-glycan (approximately 50 pmol) isolated on the ODS and amide-silica columns was digested by exoglycosidases ({alpha}-sialidase from A. ureafaciens, ß-galactosidase and ß-N-acetylhexosaminidase from jack bean under the conditions described elsewhere; Nakagawa et al., 1995Go).


    Acknowledgments
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 Abstract
 Introduction
 Results
 Discussion
 Materials and methods
 Acknowledgments
 Abbreviations
 References
 
This investigation was supported in parts by INSERM-SJPC joint research program, Grant-in-Aid for Scientific Research (13470498) from the Ministry of Education, Culture, Sports, Science and Technology; Takeda Science Foundation; and the Mochida Memorial Foundation for Medical and Pharmaceutical Research.


    Abbreviations
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 Abstract
 Introduction
 Results
 Discussion
 Materials and methods
 Acknowledgments
 Abbreviations
 References
 
BHK, baby hamster kidney; CR3, complement receptor type 3; Fc{gamma}R, receptor for Fc portion of IgG, GU, glucose unit; HPLC, high-performance liquid chromatography; ODS, octadecylsilica; PA, pyridylamine; sFc{gamma}R, soluble Fc{gamma}R; rhsFc{gamma}R, recombinant human soluble Fc{gamma}R; rmsFc{gamma}R, recombinant mouse soluble Fc{gamma}R.


    Footnotes
 
1 To whom correspondence should be addressed; E-mail: kkato@phar.nagoya-u.ac.jp Back


    References
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 Abstract
 Introduction
 Results
 Discussion
 Materials and methods
 Acknowledgments
 Abbreviations
 References
 
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