Publications

The list below includes publications that employed the expression technologies as well as constructs or proteins derived from Repository efforts.

Peer-reviewed publications:

General methods of mammalian cell expression

Moremen, K.W., Ramiah, A., Stuart, M., Steel, J., Meng, L., Forouhar, F., Moniz, H.A., Gahlay, G., Gao, Z., Chapla, D., Wang, S., Yang, J.-Y., Prabahkar, P. K., Johnson, R., dela Rosa, M., Geisler, C., Nairn, A.V., Wu, S.-C., Tong, L., Gilbert, H.J., LaBaer, J., and Jarvis, D.L. (2018) Expression system for structural and functional studies of human glycosylation enzymes. Nature Chem. Biol. 14, 156-162 [PMID:29251719; PMC5774587]

Subedi, G.P., Moniz, H., Johnson, R.W., Moremen, K.W., and Barb, A.W. (2015) High yield expression of recombinant human proteins with the transient transfection of HEK293 cells in suspension. J. Vis. Exp. 106:e53568 [PMID: 26779721] [PMC4780855]

Characterization of Glycosylation Enzymes produced in the Repository

Thieker, D., Xu, Y., Chapla, D., Nora, C., Qiu, H., Felix, T., Wang, L., Moremen, K.W., Liu, J., Esko, J., and Woods, R.J. (2018) Downstream products are potent inhibitors of the heparan sulfate 2-O-sulfotransferase Scientific Reports 8, 11823 [PMID:30087361; PMC6081452].

Jensen, J.K., Busse-Wicher, M., Poulsen, C.P., Fangel, J.U., Smith, P.J., Yang, J.-Y., Peña, M.-J., Dinesen, M.H., Martens, H.J., Melkonian, M., Wong, G.K, Moremen, K.W., Wilkerson, C.G., Scheller, H.V., Dupree, P., Ulvskov, P., Urbanowicz, B.R., and Harholt, J. (2018) Identification of an algal xylan synthase KfXYS1 proves that there is functional orthology between algal and plant cell wall biosynthesis. New Phytologist. 218, 1049-1060. [PMID:29460505; PMC5902652]

Hanes, M.S., Moremen, K.W., Cummings, R.D. (2017) Biochemical characterization of functional domains of the chaperone Cosmc. PLOS One, 12:e0180242. [PMID:28665962; PMC5493369]

Urbanowicz, B.R., Bharadwaj, V.S., Alahuhta, M., Peña, M.J., Lunin, V.V., Bomble, Y.J., Wang, S., Yang, J.-Y., Tuomivaara, S., Himmel, M.E., Moremen, K.W., York, W.S., and Crowley, M.F. (2017) Structural, Mutagenic and In Silico studies of Xyloglucan Fucosylation in Arabidopsis thaliana Suggest a Water-Mediated Mechanism. Plant J. 91: 931-949. [PMID:28670741; PMC5735850]

Sheikh, M.O., Halmo, S.M., Patel, S., Middleton, D., Takeuchi, H., Schafer, C.M., West, C.M., Haltiwanger, R.S., Avci, F.Y., Moremen, K.W., and Wells, L. (2017) Rapid screening of sugar-nucleotide donor specificities of putative glycosyltransferases Glycobiology, 27, 206-212. [PMID:28177478; PMC5789813]

Halmo, S.M., Singh, D., Patel, S., Wang, S., Edlin, E., Boons, G.J., Moremen, K.W., Live, D.H., and Wells, L. (2017) Protein O-linked mannose β-1,4-N-acetylglucosaminyltransferase 2 (POMGNT2) is a Gatekeeper Enzyme for Functional Glycosylation of α-Dystroglycan. J. Biol. Chem. 292, 2101-2109. [PMID:27932460; PMC5313085]

Li, T., Huang, M., Liu, L., Wang, S., Moremen, K.W., Boons, G.J. (2016) Divergent Chemoenzymatic Synthesis of Asymmetrical Core Fucosylated and Core-Unmodified N-Glycans. Chemistry 22, 18742-18746 [PMID:27798819] [ PMC5442444]

Calderon, A.D., Liu, Y., Li, X., Wang, X., Chen, X., Li, L., and Wang, P.G. (2016) Substrate specificity of FUT8 and chemoenzymatic synthesis of core-fucosylated asymmetric N-glycans. Org. Biomol. Chem. 14, 4027-4031 [PMID:27080952] [PMC4852481]

Praissman, J.L., Willer, T., Sheikh, M.O., Toi, A., Chitayat, D., Lin, Y.Y., Lee, H., Stalnkaker, S., Wang, S., Prabhakar, P, Nelson, S.F., Stemple D.L., Moore, S.A., Moremen, K.W., Campbell, K.P., and Wells. L. (2016) The Functional O-Mannose Glycan on α-Dystroglycan Contains a Phospho-ribitol Primed for Matriglycan Addition. eLife, 5: e14473 [PMID:27130732] [PMC4924997]

Revoredo, L., Wang, S., Bennett, E.P., Clausen, H., Moremen, K.W., Jarvis, D.L., Ten Hagen, K., Tabak, L. A., and Gerken, T.A. (2016) Mucin Type O-Glycosylation is Controlled by Short and Long Range Glycopeptide Substrate Recognition that Varies Among Members of the Polypeptide GalNAc Transferase (ppGalNAc-T) Family. Glycobiology 26: 360-76. [PMID: 26610890] [PMC4767052]

Wu, l., Viola, C.M., Brzozowski, A.M., and Davies G.J. (2015) Structural characterization of human heparanase reveals insights into substrate recognition. Nat Struct Mol Biol 22, 1016-1023 [PMID:26575439] [PMC5008439]

Czuchry, D., Desormeaux, P., Stuart, M., Jarvis, D.L., Matta, K., Szarek, W.A., and Brockhausen, I. 2015. Synthesis of the sialyl-T antigen: Biochemical characterization of a novel a2,3-sialyltransferase WbwA from pathogenic Escherichia coli serotype O104 and comparison to human ST3GAL1. J. Bacteriol., 197:3760-3768. [PMC4652054]

Praissman, J.L., Live, D.H., Wang, S., Ramiah, A., Moremen, K.W., and Wells L. (2014) B4GAT1 is the Priming Enzyme for the LARGE-dependent Functional Glycosylation of -Dystroglycan. eLife, 3, e03943. [PMID 25279697] [PMC4227051]

Gao, Y., Aryal, R.P., Ju, T., Cummings, R.D., Gahlay, G., Jarvis, D.L., Matta, K.L., Vlahakis, J.Z., Szarek, W.A., and Brockhausen, I. 2013. Acceptor specificities and selective inhibition of recombinant human Gal- and GlcNAc-transferases that synthesize core structures 1, 2, 3 and 4 of O-glycans. Biochim. Biophys. Acta, 1830:4274-4281. [PMC4002258]

Gerken, T., Revoredo, L., Thome, J.J.C., Tabak, L.A., Vester-Christensen, M.B., Clausen, H., Gahlay, G.K., Jarvis,
D.L., Johnson, R.Y., Moniz, H.A., and Moremen, K.W. (2013) The Lectin Domain of the Polypeptide GalNAc Transferase Family of Glycosyltransferases (ppGalNAc T's) Acts as a Switch Directing Glycopeptide Substrate Glycosylation in an N- or C- Direction, Further Controlling Mucin-Type O-Glycosylation. J. Biol. Chem. 288, 19900-14 [PMID 23689369] [PMC3707691]

Liu, S., Meng, L. Moremen, K.W., and Prestegard, J.H. (2009) NMR structural characterization of substrates bound to the alpha-2,6-sialyltransferase, ST6Gal-I. Biochemistry, 48, 11211-11219 [PMID19845399] [PMC2790006]

Macnaughtan, M.A., Tian, F., Liu, S., Meng, L., Park, S., Azadi, P., Moremen, K.W., and Prestegard, J.H. (2008) 13C-Sialic Acid Labeling of Glycans on Glycoproteins Using ST6Gal-I J. Am. Chem. Soc. 130, 11864-11865 [PMID 18700760] [PMC2640832]

Structure determination of Glycosylation Enzymes produced in the Repository

 Kadirvelraj, R., Yang, J.-Y., Sanders, J.H., Liu, L., Ramiah, A., Prabhakar, P.K., Boons, G.-J., Wood, Z.A., and Moremen, K.W. (2018) Human N-acetylglucosaminyltransferase II substrate recognition uses a modular architecture that includes a convergent exosite. Proc. Natl. Acad. Sci. USA, 115:4637-4642. [PMID:29666272; PMC5939069]

Urbanowicz, B.R., Bharadwaj, V.S., Alahuhta, M., Peña, M.J., Lunin, V.V., Bomble, Y.J., Wang, S., Yang, J.-Y., Tuomivaara, S., Himmel, M.E., Moremen, K.W., York, W.S., and Crowley, M.F. (2017) Structural, Mutagenic and In Silico studies of Xyloglucan Fucosylation in Arabidopsis thaliana Suggest a Water-Mediated Mechanism. Plant J. 91: 931-949. [PMID:28670741; PMC5735850]

Xiang, Y., Karaveg, K., and Moremen, K.W. (2016) Substrate recognition and catalysis by GH47 a-mannosidases involved in Asn-linked glycan maturation in the mammalian secretory pathway. Proc. Natl. Acad. Sci. USA, 113: E7890-E7899. [PMID:27856750] [PMC5150396]

Zhang, C, Zhang, T., Zou, J., Miller, C.J., Gorkhali, R., Yang, J.-Y., Schilmiller, A., Wang, S., Huang, K., Brown, E.M., Moremen, K.W., Hu, J., and Yang, J.J. (2016) Structural Basis for Regulation of Human Calcium-Sensing Receptor by Magnesium Ions and an Unexpected Tryptophan Derivative Co-agonist Science Advances, 2: e1600241 [PMID: 27386547] [PMC4928972]

Meng, L., Forouhar, F., Thieker, D., Gao, Z., Ramiah, A., Moniz, H., Xiang, Y., Seetharaman, J., Milaninia, S., Su, M., Bridger, R., Veillon, l., Azadi, P., Kornhaber, G., Wells, L., Montelione, G. T., Woods, R.J., Tong, L., and Moremen. K.W. (2013) Enzymatic basis for N-glycan sialylation: structure of rat α2,6-sialyltransferase (ST6GAL1) reveals conserved and unique features for glycan sialylation. J. Biol. Chem. 288, 34680-98 [PMID 24155237] [PMC3843080]

Use of enzymes generated in the Repository for glycan synthesis

Liu, L., Prudden, A.R., Capicciotti, C.J., Bosman, G.P., Yang, J.Y., Chapla, D.G., Moremen, K.W., and Boons, G.J. (2018) Streamlining the Chemoenzymatic Synthesis of Complex N-Glycans by a Stop and Go Strategy. Nature Chem. in press

Epp, A., Hobusch, J., Bartsch, Y., Eschweiler, S., Möbs, C., Hall, A., Morris, S.C., Petzold, D., Lilienthal, G.-M., Engellenner, C., Bitterling,J., Petry,J., Rahmöller,R., Collin, M., Moremen, K.W., Strait, R.T., Blanchard, V., Petersen, A., Gemoll, T., Habermann, J.K., Petersen, F., Nandy, A., Kahlert, H., Hertl, M., Pfützner, W., Jappe, U., Finkelman, F.D., and Ehlers, M. (2018) Sialylation of IgG antibodies inhibits IgG-mediated allergic reactions. J. Allergy Clin. Immunol. 141, 399-402. [PMID:28728998; PMC5758435]

Benedetti, E., Pučić-Baković, M., Keser, T., Wahl, A., Hassinen, H., Trbojević Akmačić , I., Vila, M., Razdorov , G., Stambuk , J., Klarić,L., Ugrina, I., Selman, M., Wuhrer, M., Rudan, I., Polasek, O., Caroline Hayward, C., Grallert, H., Strauch, K., Peters, A., Meitinger, T., Gieger, C., Yang, J.-Y., Lui, L., Boons, G.-J., Kellokumpu , S., Moremen, K.W., Bovin, N., Theis, F.J., Lauc, G., and Krumsiek, J. (2017) Network inference from glycoproteomics data reveals new reactions in the IgG glycosylation pathway. Nat Commun. 8, 1483. [PMID:29440641; PMC5811429]

Prudden, A.R., Liu, L., Capicciotti, C.J., Wolfert, M.A., Wang, S., Gao, Z., Meng, L., Moremen, K.W., Boons, G.-J. (2017) Synthesis of asymmetrical multi-antennary human milk oligosaccharides. Proc. Natl. Acad. Sci. USA 114, 6954-6959 [PMID:28630345; PMC5502611]

Bello,C., Wang, S., Meng, L., Moremen, K.W., and Becker, C.F.W. (2015) A PEGylated Photocleavable Auxiliary Mediates the Site-Specific Glycosylation and Native Chemical Ligation of Peptides. Angew Chem Int Ed Engl. 54:7711-5 [PMID 25980981] [PMC4524672]

Use of enzymes generated in the Repository for cell surface remodeling

Jiang, H., López-Aguilar, A., Meng, L., Gao, Z., Liu, Y., Tian, X., Yu, G., Ovryn. B., Moremen, K.W., Wu, P. (2018) Modulating Cell-Surface Receptor Signaling and Ion Channel Functions by In Situ Glycan Editing. Angew Chem Int Ed Engl. 57, 967-971. [PMID:29292859; PMC5779621]

Lopez Aguilar, A., Meng, L., Hou, X., Li, W., Moremen, K.W. Wu, P. (2018) Sialyltransferase-based Chemoenzymatic Histology for the Detection of N- and O- glycans. Bioconjugate Chem. 29, 1231-1239. [PMID:29569918; PMC5972038]

Briard, J.G., Jiang, H., Moremen, K.W., Macauley, M.S., and Wu, P. (2018) Cell-Based Glycan Arrays for Probing Glycan–Glycan Binding Protein Interactions. Nature Commun. 9: 880 [PMID:29491407; PMC5830402]

Rouhanifard, S.H., Aguilar, A.L., Meng, L., Izumori, K., Moremen, K.W., and Wu, P. (2018) Engineered glycocalyx regulates stem cell proliferation in crypt organoids. Cell Chem. Biol. 25, 1-8. [PMID:29429899; PMC5910180]

Sun, T., Yu, S., Zhao, P., Meng, L., Moremen, K.W., Wells, L., Steet, R., and Boons, G.-J.,A One-step Selective Exo-enzymatic Labeling (SEEL) Strategy for the Biotinylation and Identification of Glycoproteins of Living Cells. J.A.C.S. in press

Yu SH, Zhao P, Sun T, Gao Z, Moremen KW, Boons GJ, Wells L, Steet R. (2016) Selective exo-enzymatic labeling detects increased cell surface sialoglycoprotein expression upon megakaryocytic differentiation. J. Biol. Chem. 291:3982-9 [PMID: 26733198] [PMC4759176]

Mbua, N.E., Li, X., Heather R. Flanagan-Steet, H.R., Meng, L., Moremen, K.W., Wolfert, M.A., Steet, R., and Geert-Jan Boons, G.-J. (2013) Selective Exo-Enzymatic Labeling (SEEL) of N-Glycans of Living Cells by Recombinant ST6Gal I. Angewandte, 52, 13012-5. [PMID 24129959] [PMC3869382]

Use of mammalian expression platform developed in the Repository for production of proteins outside of the Repository

Moure, M.J., Eletsky, A., Gao, Q., Morris, L. Yang, J.Y., Chapla, D., Zhao, Y., Zong, C., Boons, G.J., Moremen, K.W., and Prestegard, J.H. (2018) Paramagnetic Tags for Glycosylation sites in Glycoproteins: Structural Constraints on Heparan Sulfate Binding to Robo1. ACS Chem Biol in press, DOI: 10.1021/acschembio.8b00511 [PMID:30063822, PMC6161356]

Zhang, C., Zhuo, Y., Moniz, H.A., Wang, S., Moremen, K.W., Prestegard, J.H., Brown, E., Yang, J.J. (2014) Direct Determination of Multiple Ligand Interactions with the Extracellular Domain of the Calcium Sensing Receptor. J. Biol. Chem. 289: 33529-42 [PMID 25305020] [PMC4246106]

Urbanowicz, B., Peña, M.J., Moniz, H.A., Moremen, K.W., York, W.S. (2014) Two Arabidopsis Proteins Synthesize Acetylated Xylan in Vitro, Plant J. 80, 197-206 [PMID 25141999] [PMC4184958]

Lamanna, W.C., Lawrence, R., Sarrazin, S., Lameda-Diaz, C., Gordts, P.L.S.M., Moremen, K.W., and Esko, J.D. (2012) A Genetic Model of Substrate Reduction Therapy for Mucopolysaccharidosis. J Biol Chem. 287, 36283-90. [PMID 22952226] [ PMC3476295]

Barb, A.W., Meng, L., Gao, Z., Johnson, R.W., Moremen, K.W., and Prestegard, J.H. (2012) NMR Characterization of Immunoglobulin G Fc Glycan Motion on Enzymatic Sialylation. Biochemistry, 51, 4618-26. [PMID 22574931] [PMC3447994]

Characterization of proteins generated using mammalian cell expression methods developed in the Repository

Amos, R.A., Pattathil, S., Yang, J.Y., Atmodjo, M.A., Urbanowicz, B.R., Moremen, K.W., Mohnen, D. (2018) A two-phase model for the non-processive biosynthesis of homoglacturonan polysaccharides by the GAUT1:GAUT7 complex. J. Biol. Chem. in press. [PMID:30327429; PMC in process]

Muchero, W., Sondreli, K.L., Chen, J.-G., Urbanowicz, B.R., Zhang, J., Singan, V., Yang, Y., Brueggeman, R.S., Franco-Coronado, J., Abraham, N., Yang, J.-Y., Moremen, K.W., Weisberg, A.J., Chang, J.H., Lindquist, E., Berry, K., Ranjan, P., Jawdy, S., Schmutz, J., Tuskan, G.A., LeBoldus, J.M. (2018) Association mapping, transcriptomics, and transient expression identify candidate genes mediating plant-pathogen interactions in a tree. Proc. Natl. Acad. Sci. USA in press. [PMID:30337484; PMC in process]

Voiniciuc, C., Engle, K., Günl, M., Dieluweit, S., Heinrich-Wilhelm Schmidt, M., Yang, J.-Y., Moremen, K.W., Mohnen, D., and Usadel B. (2018) Identification of Key Enzymes for Pectin Synthesis in Arabidopsis Seed Mucilage. Plant Physiol in press, doi: 10.1104/pp.18.00584. [PMID:30228108; PMC in process]

Gao, Q., Yang, J.Y., Moremen, K.W., Flanagan, J.G., and Prestegard, J.H. (2018) Structural Characterization of a Heparan Sulfate Pentamer Interacting with LAR-Ig1-2. Biochemistry 57, 2189-2199. [PMID: 29570275; PMC6015444]

Zhao, Y., Yang, J.Y., Thieker, D.F., Xu, Y., Zong, C., Boons, G.-J., Liu, J., Woods, R.J., Moremen, K.W., Amster. I.J. (2018) Traveling wave ion mobility spectrometry (TWIMS) study of the Robo1-heparan sulfate interaction J. Amer. Soc. Mass Spectrom 6:1153-1165 [PMID:29520710; PMC6004239]

Gao, Q., Chen,C.Y., Zong, C., Wang, S., Morris, L.C., Boons, G.-J., Moremen, K.W., and Prestegard J.H. (2016) Structural Aspects of Heparan Sulfate Binding to Robo1-D12. ACS Chemical Biology in press.

Zhuo,Y., Yang, J.-Y., Moremen, K.W., and Prestegard, J. (2016) Glycosylation alters dimerization properties of a cell-surface signaling protein, CEACAM1. J. Biol. Chem. in press

Li Z, Moniz HA, Wang, S., Ramiah A, Zhang, F. Moremen KW, Linhardt, R.J.,and Sharp JS (2015) High Structural Resolution Hydroxyl Radical Protein Footprinting Reveals an Extended Robo1-Heparin Binding Interface. J. Biol. Chem. 290:10729-40. [PMID 25752613] [PMC4409239]

Zhang, F., Moniz, H.A., Walcott, B., Moremen, K.W., Wang, L., and Linhardt, R.J. (2014) Probing the impact of GFP tagging on Robo1-heparin interaction, Glycoconj J., 4, 299-307. [PMID 24748467] [PMC4118743]

Prestegard, J.H., Agard, D.A., Moremen, K.W., Lavery, L.A., Morris, L.C., Pederson, K. (2014) Sparse Labeling of Proteins: Structural Characterization from Long Range Constraints. J. Mag. Res., 241, 32-40 [PMID 24656078] [PMC3964372]

Zhang, F., Moniz, H., Walcott, B., Moremen, K., Linhardt, R.J., Wang, L. (2013) Characterization of the Interaction between Robo1 and Heparin and other Glycosaminoglycans. Biochimie, 95, 2345-53. [PMID 23994753] [PMC3871176]

Reviews:

Moremen, K.W., Tiemeyer, M., and Nairn A.V. (2012) Vertebrate protein glycosylation: diversity, synthesis, and function Nat. Rev. Cell Mol. Biol. 13, 448-62 [PMID 22722607] [PMC3934011]