N-glycosylation of mannose receptor (CD206) regulates glycan binding by C-type lectin domains

Abstract

The macrophage mannose receptor (MR, CD206) is a transmembrane endocytic lectin receptor, expressed in selected immune and endothelial cells, and is involved in immunity and maintaining homeostasis. Eight of the ten extracellular domains of the MR are C-type lectin domains (CTLDs) which mediate the binding of mannose, fucose, and GlcNAc in a calcium-dependent manner. Previous studies indicated that self-glycosylation of MR regulates its glycan binding. To further explore this structure–function relationship, we studied herein a recombinant version of mouse MR CTLD4-7 fused to human Fc-portion of IgG (MR-Fc). The construct was expressed in different glycosylation-mutant cell lines to study the influence of differential glycosylation on receptor glycan-binding properties. We conducted site-specific N- and O-glycosylation analysis and glycosylation site characterization using mass spectrometry by which several novel O-glycosylation sites were identified in mouse MR and confirmed in human full-length MR. This information guided experiments evaluating the receptor functionality by glycan microarray analysis in combination with glycan-modifying enzymes. Treatment of active MR-Fc with combinations of exoglycosidases, including neuraminidase and galactosidases, resulted in the loss of trans-binding (binding of MR CTLDs to non-MR glycans), due to unmasking of terminal, nonreducing GlcNAc in N-glycans of the MR CTLDs. Regalactosylation of N-glycans rescues mannose binding by MR-Fc. Our results indicate that glycans within the MR CTLDs act as a regulatory switch by masking and unmasking self-ligands, including terminal, nonreducing GlcNAc in N-glycans, which could control MR activity in a tissue- and cell-specific manner or which potentially affect bacterial pathogenesis in an immunomodulatory fashion. The macrophage mannose receptor (MR, CD206) is a transmembrane endocytic lectin receptor, expressed in selected immune and endothelial cells, and is involved in immunity and maintaining homeostasis. Eight of the ten extracellular domains of the MR are C-type lectin domains (CTLDs) which mediate the binding of mannose, fucose, and GlcNAc in a calcium-dependent manner. Previous studies indicated that self-glycosylation of MR regulates its glycan binding. To further explore this structure–function relationship, we studied herein a recombinant version of mouse MR CTLD4-7 fused to human Fc-portion of IgG (MR-Fc). The construct was expressed in different glycosylation-mutant cell lines to study the influence of differential glycosylation on receptor glycan-binding properties. We conducted site-specific N- and O-glycosylation analysis and glycosylation site characterization using mass spectrometry by which several novel O-glycosylation sites were identified in mouse MR and confirmed in human full-length MR. This information guided experiments evaluating the receptor functionality by glycan microarray analysis in combination with glycan-modifying enzymes. Treatment of active MR-Fc with combinations of exoglycosidases, including neuraminidase and galactosidases, resulted in the loss of trans-binding (binding of MR CTLDs to non-MR glycans), due to unmasking of terminal, nonreducing GlcNAc in N-glycans of the MR CTLDs. Regalactosylation of N-glycans rescues mannose binding by MR-Fc. Our results indicate that glycans within the MR CTLDs act as a regulatory switch by masking and unmasking self-ligands, including terminal, nonreducing GlcNAc in N-glycans, which could control MR activity in a tissue- and cell-specific manner or which potentially affect bacterial pathogenesis in an immunomodulatory fashion. The macrophage mannose receptor (MR, CD206) is a type 1 transmembrane endocytic lectin receptor and plays an essential role in immunity and homeostasis (1Martinez-Pomares L. The mannose receptor.J. Leukoc. Biol. 2012; 92: 1177-1186Crossref PubMed Scopus (382) Google Scholar). It is largely expressed in macrophages, dendritic cells, as well as in some endothelial cells, where it constantly shuttles between the plasma membrane and the endosomal compartment to endocytose ligands in a clathrin-dependent manner (2van der Zande H.J.P. Nitsche D. Schlautmann L. Guigas B. Burgdorf S. The mannose receptor: from endocytic receptor and biomarker to regulator of (Meta)Inflammation.Front. Immunol. 2021; 12: 765034Crossref PubMed Scopus (35) Google Scholar). The MR belongs to the MR family, including M-type phospholipase A2 receptor, DEC-205/gp200-MR6, and Endo180/uPARAP. The extracellular portion is composed of an N-terminal cysteine-rich domain, a fibronectin-type II domain, and 8 C-type lectin domains (CTLDs) (3East L. Isacke C.M. The mannose receptor family.Biochim. Biophys. Acta. 2002; 1572: 364-386Crossref PubMed Scopus (515) Google Scholar). The MR cysteine-rich domain binds sulfated glycans (4Fiete D.J. Beranek M.C. Baenziger J.U. A cysteine-rich domain of the “mannose” receptor mediates GalNAc-4-SO4 binding.Proc. Natl. Acad. Sci. U. S. A. 1998; 95: 2089-2093Crossref PubMed Scopus (158) Google Scholar, 5Leteux C. Chai W. Loveless R.W. Yuen C.T. Uhlin-Hansen L. Combarnous Y. et al.The cysteine-rich domain of the macrophage mannose receptor is a multispecific lectin that recognizes chondroitin sulfates A and B and sulfated oligosaccharides of blood group Lewis(a) and Lewis(x) types in addition to the sulfated N-glycans of lutropin.J. Exp. Med. 2000; 191: 1117-1126Crossref PubMed Scopus (153) Google Scholar, 6Liu Y. Chirino A.J. Misulovin Z. Leteux C. Feizi T. Nussenzweig M.C. et al.Crystal structure of the cysteine-rich domain of mannose receptor complexed with a sulfated carbohydrate ligand.J. Exp. Med. 2000; 191: 1105-1116Crossref PubMed Scopus (116) Google Scholar) and the fibronectin-type II domain is known to bind collagen (7Napper C.E. Drickamer K. Taylor M.E. Collagen binding by the mannose receptor mediated through the fibronectin type II domain.Biochem. J. 2006; 395: 579-586Crossref PubMed Scopus (78) Google Scholar). Via the CTLDs, the receptor has been reported to bind mannose (Man), GlcNAc, fucose (Fuc), and glucose in a calcium-dependent manner (8Taylor M.E. Bezouska K. Drickamer K. Contribution to ligand binding by multiple carbohydrate-recognition domains in the macrophage mannose receptor.J. Biol. Chem. 1992; 267: 1719-1726Abstract Full Text PDF PubMed Google Scholar, 9Shepherd V.L. Lee Y.C. Schlesinger P.H. Stahl P.D. L-Fucose-terminated glycoconjugates are recognized by pinocytosis receptors on macrophages.Proc. Natl. Acad. Sci. U. S. A. 1981; PubMed Scopus Google Scholar, M.E. Drickamer K. binding of ligands by the macrophage mannose receptor.J. Biol. Chem. Full Text PDF PubMed Google Scholar, P.D. Schlesinger P.H. binding of and by macrophages.Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar, Y. Drickamer K. et analysis of carbohydrate binding by the macrophage mannose receptor Biol. Chem. 2021; Full Text Full Text PDF PubMed Scopus Google Scholar). the MR CTLDs, has carbohydrate expressed as a recombinant (8Taylor M.E. Bezouska K. Drickamer K. Contribution to ligand binding by multiple carbohydrate-recognition domains in the macrophage mannose receptor.J. Biol. Chem. 1992; 267: 1719-1726Abstract Full Text PDF PubMed Google Scholar, M.E. Drickamer K. binding of ligands by the macrophage mannose receptor.J. Biol. Chem. Full Text PDF PubMed Google Scholar). expressed with the binds mannose with the as CTLDs the of as is that the CTLDs are (8Taylor M.E. Bezouska K. Drickamer K. Contribution to ligand binding by multiple carbohydrate-recognition domains in the macrophage mannose receptor.J. Biol. Chem. 1992; 267: 1719-1726Abstract Full Text PDF PubMed Google Scholar, M.E. Drickamer K. binding of ligands by the macrophage mannose receptor.J. Biol. Chem. Full Text PDF PubMed Google Scholar). ligands of the MR CTLDs are and N-glycans, which are a of different types in control and K. C. J. et and N-glycans in recognized by the mannose receptor Sci. 2021; PubMed Scopus Google Scholar). The MR is a sites in mouse and in and on using C. Y. et of the human through J. PubMed Scopus Google it several O-glycosylation with of identified by analysis M.E. Stahl P.D. Drickamer K. structure of the mannose receptor multiple carbohydrate-recognition Biol. Chem. Full Text PDF PubMed Google Scholar). MR glycosylation been reported to ligand binding the CTLDs Y. T. J. C. et the lectin of the macrophage mannose receptor.J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar) and studies differential MR glycan different Y. L. C.M. D.J. L. et analysis of mannose receptor from Biophys. PubMed Scopus Google of the sites or O-glycosylation sites are in or and the glycosylation influence We reported that and in and of J. et and in of and glycan-binding Chem. Biol. 2021; Full Text Full Text PDF PubMed Scopus Google and in glycosylation of the MR could influence its it that the of the MR is and and could on that influence glycosylation of the cells, as or to and a 2012; PubMed Scopus Google Scholar). to the analysis of structure–function of the and its role in and we a analysis of the MR in different glycosylation-mutant cell the we that the of glycosylation MR activity is Y. T. J. C. et the lectin of the macrophage mannose receptor.J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). we a recombinant composed of the MR CTLD4-7 and the IgG portion to the role of MR glycosylation in binding. The MR-Fc was expressed in the cell lines and to and human cell MR-Fc binding to glycan was with site-specific N- and studies the glycan of the MR-Fc that its loss or of or trans-binding of that the binding of MR CTLDs to non-MR and to this Our that the masking of or unmasking of of nonreducing GlcNAc in N-glycans the glycan binding of the MR CTLDs. To explore the influence of glycosylation on MR binding to glycan we the mouse fused to the Fc-portion of human IgG (MR-Fc). MR-Fc is a to study the glycan ligands of the CTLDs K. C. J. et and N-glycans in recognized by the mannose receptor Sci. 2021; PubMed Scopus Google Scholar). We expressed the MR-Fc in cell with different glycan are by a in a glycosylation in Full Text PDF PubMed Scopus Google in an in The MR-Fc was expressed in the cell which has a to and a in in N-glycans Y. of cell lines PubMed Scopus Google Scholar). a MR-Fc was expressed in as well as MR-Fc from cell lines were glycan binding using the glycan microarray and the binds to and glycans and glycan on the and bind to the glycan and the the to we it to and to and N-glycans or from to on the with the from the the and bind to the the and binding to the B and and glycan A and to study MR-Fc glycan we of to further explore the sites of glycosylation and of glycan We a to MR-Fc glycan-binding different The different mannose including and and The was with which to the mannose in a calcium-dependent manner as expressed in are in due to the to the glycan was using was confirmed by lectin and the in a to the loss of activity and of were using in binding results that of from a active MR-Fc in loss of receptor trans-binding to This that the of glycan binding by is of its of MR-Fc were using to the of N-glycans MR-Fc mannose binding. and of N-glycans affect binding to the and of the N-glycans from the and to bind to the in which receptors the binding as the MR-Fc and This that is glycan binding by the MR-Fc that of the N-glycans the receptor The MR-Fc has in the and and on MR in and and in the IgG A site-specific characterization using analysis was to the of MR glycosylation in its glycan binding and The were largely on glycan glycosylation sites and are on the glycosylation this O-glycosylation as the was to and the the an to the was with neuraminidase and to and This analysis MR-Fc expressed in cells, as the 1 expressed by site characterization was as as the which could by and a of in neuraminidase the of the in is and which to a combination of are the in and that the of glycans the as and indicate in of a glycosylation site in this were to including the glycan The with the is the of in a with N-glycans and of in this in MR-Fc. The and in were as in MR-Fc using was in the and N-glycans glycans with and and N-glycans, of the N-glycans and the of were and to to the a of N-glycans to with and as well as and N-glycans was in the with the glycan and N-glycans N-glycans with and and N-glycans A portion of this glycosylation site is with a of and different were to to the of the and were the glycans to in the different with and as well as and of N-glycans were The of the IgG Fc-portion IgG glycosylation MR-Fc of which N-glycans MR sites within is a portion of or N-glycans in the site in of glycans with terminal, nonreducing This was as are in the GlcNAc is a reported ligand of the MR CTLDs (8Taylor M.E. Bezouska K. Drickamer K. Contribution to ligand binding by multiple carbohydrate-recognition domains in the macrophage mannose receptor.J. Biol. Chem. 1992; 267: 1719-1726Abstract Full Text PDF PubMed Google Scholar, 9Shepherd V.L. Lee Y.C. Schlesinger P.H. Stahl P.D. L-Fucose-terminated glycoconjugates are recognized by pinocytosis receptors on macrophages.Proc. Natl. Acad. Sci. U. S. A. 1981; PubMed Scopus Google Scholar, P.D. Schlesinger P.H. binding of and by macrophages.Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar, Y. Drickamer K. et analysis of carbohydrate binding by the macrophage mannose receptor Biol. Chem. 2021; Full Text Full Text PDF PubMed Scopus Google and we confirmed that as we bind to the on the glycan K. C. J. et and N-glycans in recognized by the mannose receptor Sci. 2021; PubMed Scopus Google Scholar). binding to GlcNAc was in of glycan or studies from K. C. J. et and N-glycans in recognized by the mannose receptor Sci. 2021; PubMed Scopus Google Scholar). MR-Fc bind to the on the in to the GlcNAc could a to the mannose we the and by and with neuraminidase and to the glycan were to bind to the of and as a with neuraminidase and a and of and results in the of MR-Fc. of with mannose or GlcNAc, mannose binding and We further that the bind to and with GlcNAc or mannose, with that GlcNAc is a ligand of the MR-Fc in this The analysis of indicated the of which in a portion of of and was on the full-length recombinant human MR to the that the is an of the of the MR-Fc. the recombinant full-length MR was in cells, the N-glycans to with we an with resulted in binding to the and Our results indicate that of terminal, nonreducing GlcNAc the activity of the full-length with the results in the MR-Fc MR and MR-Fc glycan which to GlcNAc we could mannose binding of MR-Fc. was and by A to This resulted in loss of as by binding to the of the mannose binding and binding to the as the active and of the using its binding to the The of was confirmed by lectin and binding of results that GlcNAc on MR-Fc the receptor trans-binding to mannose and that or the of N-glycans, mannose binding in The site-specific analysis of the the of O-glycosylation in the receptor We further the full-length human full-length MR to the of O-glycosylation sites between human and mouse MR. to O-glycosylation sites were identified in MR-Fc and to in the full-length human MR of site are in the identified sites were in the between the CTLDs. The of to O-glycosylation sites and in the full-length human MR. MR-Fc and human full-length was to within the The between and was the it The were and to in MR-Fc. site within the of was in The in human full-length MR to glycosylation sites and The to in mouse MR-Fc. and glycosylation sites were identified within the in the where was identified in the human full-length MR. site was in the between and The between and the transmembrane domain of MR was in the human full-length MR and it to O-glycosylation sites and of the MR-Fc 1 or the and The of and are with as the the glycans of and we identified the role of MR glycosylation in the glycan-binding of its CTLDs. A combination of and site-specific glycosylation site characterization by the of masking terminal, nonreducing GlcNAc to MR-Fc glycan trans-binding The MR-Fc expressed in or was the activity was the of in mannose binding. The active receptor its to bind mannose with neuraminidase and which results in N-glycans with the of MR-Fc in was by GlcNAc, and in an MR-Fc. the by masking GlcNAc on with or by of the N-glycans are a of MR-Fc expressed in cells, which glycan-binding Our results that mannose and GlcNAc to the MR CTLDs, potentially in binding or and binding. Our results are in with a study by et Y. T. J. C. et the lectin of the macrophage mannose receptor.J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar) experiments to different This study the glycan-binding of MR expressed in in and to Y. T. J. C. et the lectin of the macrophage mannose receptor.J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). with it was that and MR were to bind mannose the of the MR in to endocytose was and binding of sulfated through the cysteine-rich domain was the full-length receptor expressed in and bind mannose could bind sulfated analysis of the full-length MR expressed in as the results the to that is the glycosylation that regulates the activity of MR Y. T. J. C. et the lectin of the macrophage mannose receptor.J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). in we as neuraminidase and as well as by on the recombinant full-length MR and to MR by unmasking or masking of We the site-specific MR-Fc glycosylation and that of MR-Fc sites a with GlcNAc, the sites The of as the MR in the study by et Y. T. J. C. et the lectin of the macrophage mannose receptor.J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar) is an of the full-length MR Our results the of site-specific as a the analysis of further of is the MR the compartment in Stahl P.D. of the mannose receptor from the Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). MR was with the of of the and MR the and is of O-glycosylation and in the where is to with which to the glycan resulted in MR it was that of the MR in the Stahl P.D. of the mannose receptor from the Biol. Chem. Full Text Full Text PDF PubMed Scopus Google which with the addition of to and GlcNAc has been reported as a ligand of the MR CTLDs (8Taylor M.E. Bezouska K. Drickamer K. Contribution to ligand binding by multiple carbohydrate-recognition domains in the macrophage mannose receptor.J. Biol. Chem. 1992; 267: 1719-1726Abstract Full Text PDF PubMed Google Scholar, 9Shepherd V.L. Lee Y.C. Schlesinger P.H. Stahl P.D. L-Fucose-terminated glycoconjugates are recognized by pinocytosis receptors on macrophages.Proc. Natl. Acad. Sci. U. S. A. 1981; PubMed Scopus Google Scholar, P.D. Schlesinger P.H. binding of and by macrophages.Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar, Y. Drickamer K. et analysis of carbohydrate binding by the macrophage mannose receptor Biol. Chem. 2021; Full Text Full Text PDF PubMed Scopus Google it a of and in the as mannose K. activity a C-type 1992; PubMed Scopus Google Scholar). expressed or bind GlcNAc, the binds to GlcNAc and to mannose (8Taylor M.E. Bezouska K. Drickamer K. Contribution to ligand binding by multiple carbohydrate-recognition domains in the macrophage mannose receptor.J. Biol. Chem. 1992; 267: 1719-1726Abstract Full Text PDF PubMed Google Scholar). we MR-Fc ligands using glycan and binding was to glycans or glycan of the we that the MR-Fc to on the S. glycan microarray K. C. J. et and N-glycans in recognized by the mannose receptor Sci. 2021; PubMed Scopus Google Scholar) as well as to that are by or MR has been reported to in the of which by the receptor with C.E. Taylor M.E. of the macrophage mannose receptor.J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). that experiments that the receptor binds glycan on the receptor, it due to the binding of receptor due to receptor binding and of the in the of of the receptor was which is the in the of and mannose using J. S. A. et the mannose receptor by of and the mannose receptor.J. Biol. Chem. 2006; Full Text Full Text PDF PubMed Scopus Google Scholar). It that of the receptor in the study N-glycans, in receptor the of or mannose the of MR in was in a J. S. A. et the mannose receptor by of and the mannose receptor.J. Biol. Chem. 2006; Full Text Full Text PDF PubMed Scopus Google Scholar). of studies indicate that the of receptor results in or this to further of and MR been from a and Baenziger J.U. of by the Natl. Acad. Sci. U. S. A. 2000; PubMed Scopus Google Scholar). the is to mannose the was receptor binding with sulfated the cysteine-rich domain Baenziger J.U. of by the Natl. Acad. Sci. U. S. A. 2000; PubMed Scopus Google Scholar). It that the of receptor which to differential glycan and of the receptor in a manner. We confirmed MR sites that are between and O-glycosylation sites were identified in MR-Fc and in the human full-length in the between the CTLDs. study of the human MR the of O-glycosylation in the between to M.E. Stahl P.D. Drickamer K. structure of the mannose receptor multiple carbohydrate-recognition Biol. Chem. Full Text PDF PubMed Google Scholar). We to O-glycosylation sites in this O-glycosylation site reported was in the between and which was confirmed in mouse and human by mass in combination with experiments some further information MR C.E. Taylor M.E. of the macrophage mannose receptor.J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). The on sites of and are and to was reported between and in experiments C.E. Taylor M.E. of the macrophage mannose receptor.J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar). The between has been confirmed by a study using CTLD4-7 M.E. Drickamer K. binding of ligands by the macrophage mannose receptor.J. Biol. Chem. Full Text PDF PubMed Google Scholar). results with O-glycosylation site The in between CTLDs identified O-glycosylation site or a O-glycosylation site as between and The that were to to to O-glycosylation a structure of the receptor was in studies in combination with which indicated a structure of the receptor C.E. Taylor M.E. of the macrophage mannose receptor.J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google Scholar) and it was that in some of the to binding a of studies were to the structure of the receptor, that it in the and which is J. S. A. et the mannose receptor by of and the mannose receptor.J. Biol. Chem. 2006; Full Text Full Text PDF PubMed Scopus Google Scholar, and of the mannose receptor Sci. PubMed Scopus Google Scholar). that the receptor is between the plasma membrane and endosomal compartment where the ligand is this could a regulatory with the the structure and J. S. A. et the mannose receptor by of and the mannose receptor.J. Biol. Chem. 2006; Full Text Full Text PDF PubMed Scopus Google Scholar). Our study that the of the MR CTLDs by MR glycosylation has been reported a of Y. L. C.M. D.J. L. et analysis of mannose receptor from Biophys. PubMed Scopus Google Scholar) and it that this a regulatory to control the activity of MR CTLDs in a tissue- or cell-specific manner. bind or glycans on cell which trans-binding of cells, and could trans-binding Y.C. of the binding lectin regulates its to mediate cell PubMed Google Scholar). the this regulatory switch of unmasking MR on the receptor and receptor trans-binding to to from the immune A of including in to glycan which immunomodulatory pathogenesis J. of and 2012; PubMed Scopus Google Scholar, J. in pathogenesis and PubMed Scopus Google Scholar). Our on the structure–function of MR and further studies to to this switch is in recombinant full-length MR with expressed in mouse cell was from IgG from and from and were from neuraminidase and from and from from and from GlcNAc and from were from indicated and were with MR-Fc the fused to the Fc-portion of human IgG L. S. ligands of carbohydrate domains of the mannose receptor in macrophages, endothelial and to and J. Immunol. PubMed Scopus Google Scholar) from L. were by Y. of cell lines PubMed Scopus Google Scholar) and lines were from was with with to the The were with in a by the were with MR-Fc and were in with and were in with and were in with and were in with and in The the was MR-Fc was from cell using The was with the on a by with and MR-Fc using and with 1 MR-Fc was further to microarray MR-Fc was with and neuraminidase was by neuraminidase were MR-Fc was with and 1 was by MR-Fc and human full-length MR were to neuraminidase and full-length MR of was with and to the with the addition of 1 neuraminidase and or were with or to the with the addition of 1 neuraminidase and To study the of MR-Fc a of was with neuraminidase and To was using A as and in of were with 1 and was by of 1 from to of in and 1 by We a glycan microarray to MR-Fc glycan-binding of mannose were as and the and were using the with with a as by the were to the and as to and were on the were some been which were to the study as to the the were and The of the was by the in a of in 1 were from this in and ten in which were using a were to the were different in with in the of to the were to that by the and with to or that the of the was of are in a control lectin were and were using a as S. T. C. M.E. et glycan ligand of glycan binding Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar). MR-Fc binding was in binding and 1 on a by with and with a IgG in 1 on a The were with by and a the binding was in the of of The were using a and was using the The glycan were binding the as MR-Fc binding was on the glycan S. T. C. M.E. et glycan ligand of glycan binding Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar) C. K. B. Y. et of by glycan-binding involved in and 2021; Scopus Google Scholar) and on the 1 The human full-length MR was binding on the with an the of in the MR-Fc from cells, 8 and 1 human full-length MR were with or to the MR-Fc was with to the including the addition of A portion of the human full-length MR was with 1 neuraminidase and further The were to and as Y. et analysis of human PubMed Scopus Google Scholar). were with of in The the was and of was and on a were and in a The were further was on an to an mass as J. S. K. et B cell PubMed Scopus Google Scholar). MR-Fc were in in and a with A in and on a using a of to B by to B The mass was the the were to and were in the a of within a of to a of and of a of The were selected in a within a mass of to a of and an of is in of or or and in the with a of with the mass an of and a of was in a manner with and in the with a of with the mass an of and a of the analysis of the human full-length MR is in the was using version was as with a of the and mass was to The glycan was and The were on and with a were selected and further of was in an manner as D. et a spectrometry of PubMed Scopus Google Scholar). The that were identified on on and glycan were on and was The been to the the Y. J. C. D. S. S. et al.The in a mass PubMed Scopus Google Scholar) with the The glycan microarray the is in the or D. This information J. S. K. et B cell PubMed Scopus Google Scholar, D. et a spectrometry of PubMed Scopus Google Scholar). K. S. is an of of this to We the MR-Fc and the We the of and K. and D. C. A. Y. L. C. J. and D. C. K. J. and D. C. A. Y. J. D. and D. C. K. S. K. A. Y. and C. K. S. K. A. Y. L. C. J. and D. C. This was by the to K. S. and by an to D. C. The is the of the and the of the of

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