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Production platforms for biotherapeutic glycoproteins. Occurrence impact, and challenges of non-human sialylation
Open accessAbstract
One of the fastest growing fields in the pharmaceutical industry is the market for therapeutic glycoproteins. Today, these molecules play a major role in the treatment of various diseases, and include several protein classes, i.e., clotting factors, hormones, cytokines, antisera, enzymes, enzyme inhibitors, Ig-Fc-Fusion proteins, and monoclonal antibodies. Optimal glycosylation is critical for therapeutic glycoproteins, as glycans can influence their yield, immunogenicity and efficacy, which impact the costs and success of such treatments. While several mammalian cell expression systems currently used can produce therapeutic glycoproteins that are mostly decorated with human-like glycans, they can differ from human glycans by presenting two structures at the terminal and therefore most exposed position. First, natural human N-glycans are lacking the terminal Gal 1-3Gal (alpha-Gal) modification; and second, they do not contain the non-human sialic acid N-glycolylneuraminic acid (Neu5Gc). All humans spontaneously express antibodies against both of these glycan structures, risking increased immunogenicity of biotherapeutics carrying such non-human glycan epitopes. However, in striking contrast to the alpha-Gal epitope, exogenous Neu5Gc can be metabolically incorporated into human cells and presented on expressed glycoproteins in several possible epitopes. Recent work has demonstrated that this non-human sialic acid is found in widely varying amounts on biotherapeutic glycoproteins approved for treatment of various medical conditions. Neu5Gc on glycans of these medical agents likely originates from the production process involving the non-human mammalian cell lines and/or the addition of animal-derived tissue culture supplements. Further studies are needed to fully understand the impact of Neu5Gc in biotherapeutic agents. Similar concerns apply to human cells prepared for allo- or auto-transplantation, that have been grown in animal-derived tissue culture supplements.
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“Indeed, plants produce core α1,3-fructose and β1,2-xylose, which are completely absent in human cells and could be immunogenic (Karg et al., 2009;Ghaderi et al., 2012).”
From Therapeutic glycoprotein production in mammalian cells (2017) · cites this paper as Ghaderi et al., 2012
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Cites
Wiederschain, G. Y. (2009) · Biochemistry (Moscow) · doi:10.1134/s0006297909090156 · Cited by 4,089
Siglecs and their roles in the immune system
Crocker, P. R., Paulson, J. C., & Varki, A. P. (2007) · Nature reviews. Immunology · doi:10.1038/nri2056 · Cited by 2,032
Self-citationCetuximab-Induced Anaphylaxis and IgE Specific for Galactose-α-1,3-Galactose
Chung, C. H., Mirakhur, B., Chan, E., Le, Q.-T., Berlin, J., Morse, M., Murphy, B. A., Satinover, S. M., Hosen, J., Mauro, D., et al. (2008) · New England Journal of Medicine · doi:10.1056/nejmoa074943 · Cited by 1,521
The Impact of Glycosylation on the Biological Function and Structure of Human Immunoglobulins
Arnold, J. N., Wormald, M. R., Sim, R. B., Rudd, P. M., & Dwek, R. A. (2006) · Annual Review of Immunology · doi:10.1146/annurev.immunol.25.022106.141702 · Cited by 1,354
Chemical Diversity in the Sialic Acids and Related α-Keto Acids: An Evolutionary Perspective
Angata, T., & Varki, A. P. (2002) · Chemical Reviews · doi:10.1021/cr000407m · Cited by 1,254
Self-citationProduction of α1,3-Galactosyltransferase-Deficient Pigs
Phelps, C. J., Koike, C., Vaught, T. D., Boone, J. T., Wells, K. D., Chen, S.-H., Ball, S. F., Specht, S. M., Polejaeva, I. A., Monahan, J. A., et al. (2003) · Science · doi:10.1126/science.1078942 · Cited by 1,111
Baculovirus as versatile vectors for protein expression in insect and mammalian cells
Kost, T. A., Condreay, J. P., & Jarvis, D. L. (2005) · Nature Biotechnology · doi:10.1038/nbt1095 · Cited by 1,014
Human embryonic stem cells express an immunogenic nonhuman sialic acid
Martin, M. J., Muotri, A. R., Gage, F. H., & Varki, A. P. (2005) · Nature Medicine · doi:10.1038/nm1181 · Cited by 935
Self-citationJournal of the National Cancer Institute
(1993) · Journal of the American Dietetic Association · doi:10.1016/0002-8223(93)92324-q · Cited by 913
Wiseman, M. J. (2008) · Proceedings of The Nutrition Society · doi:10.1017/s002966510800712x · Cited by 902
Glycan-based interactions involving vertebrate sialic-acid-recognizing proteins
Varki, A. P. (2007) · Nature · doi:10.1038/nature05816 · Cited by 855
Self-citationN-Linked Glycosylation in Campylobacter jejuni and Its Functional Transfer into E. coli
Wacker, M., Linton, D., Hitchen, P. G., Lazar, M. N., Haslam, S. M., North, S. J., Panico, M., Morris, H. R., Dell, A., Wren, B. W., et al. (2002) · Science · doi:10.1126/science.298.5599.1790 · Cited by 780
Kuwaki, K., Tseng, Y., Dor, F. J. M. F., Shimizu, A., Houser, S. L., Sanderson, T. M., Lancos, C. J., Prabharasuth, D., Cheng, J. J., Moran, K., et al. (2004) · Nature Medicine · doi:10.1038/nm1171 · Cited by 693
Galili, U. (1993) · Immunology Today · doi:10.1016/0167-5699(93)90261-i · Cited by 659
Human uptake and incorporation of an immunogenic nonhuman dietary sialic acid
Tangvoranuntakul, P., Gagneux, P., Diaz, S., Bardor, M., Varki, N., Varki, A., & Muchmore, E. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2131556100 · Cited by 625
Self-citationRose, D., Boyar, A. P., & Wynder, E. L. (1986) · Cancer · doi:10.1002/1097-0142(19861201)58:11 · Cited by 593
A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence
Chou, H.-H., Takematsu, H., Diaz, S. L., Iber, J. C., Nickerson, E., Wright, K. L., Muchmore, E. A., Nelson, D. L., Warren, S. T., & Varki, A. P. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.20.11751 · Cited by 576
Self-citationAchievements and challenges of sialic acid research
Schauer, R. (2000) · Glycoconjugate Journal · doi:10.1023/a:1011062223612 · Cited by 572
Readily Available Tissue-Engineered Vascular Grafts
Dahl, S. L. M., Kypson, A. P., Lawson, J. H., Blum, J. L., Strader, J. T., Li, Y., Manson, R. J., Tente, W. E., DiBernardo, L. R., Hensley, M. T., et al. (2011) · Science Translational Medicine · doi:10.1126/scitranslmed.3001426 · Cited by 563
Pera, M. F., Reubinoff, B. E., & Trounson, A. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.1.5 · Cited by 557
Immunogenicity of protein therapeutics
Groot, A. S. D., & Scott, D. W. (2007) · Trends in Immunology · doi:10.1016/j.it.2007.07.011 · Cited by 544
Advances in the Biology and Chemistry of Sialic Acids
Chen, X., & Varki, A. P. (2009) · ACS Chemical Biology · doi:10.1021/cb900266r · Cited by 544
Self-citationProtein glycosylation in bacteria: sweeter than ever
Nothaft, H., & Szymanski, C. M. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2383 · Cited by 531
Diversity in cell surface sialic acid presentations: implications for biology and disease
Varki, N. M., & Varki, A. P. (2007) · Laboratory Investigation · doi:10.1038/labinvest.3700656 · Cited by 521
Self-citationMeat consumption and colorectal cancer risk: Dose‐response meta‐analysis of epidemiological studies
Norat, T., Lukanova, A., Ferrari, P., & Ríboli, E. (2001) · International Journal of Cancer · doi:10.1002/ijc.10126 · Cited by 510
Fraser, G. E. (1999) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/70.3.532s · Cited by 489
Key, T. J., Fraser, G. E., Thorogood, M., Appleby, P. N., Beral, V., Reeves, G., Burr, M. L., Chang-Claude, J., Frentzel-Beyme, R., Kuzma, J. W., et al. (1999) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/70.3.516s · Cited by 484
Plant‐specific glycosylation patterns in the context of therapeutic protein production
Gomord, V., Fitchette, A., Menu‐Bouaouiche, L., Saint‐Jore‐Dupas, C., Plasson, C., Michaud, D., & Faye, L. J.-Y. (2010) · Plant Biotechnology Journal · doi:10.1111/j.1467-7652.2009.00497.x · Cited by 425
Process economics of industrial monoclonal antibody manufacture
Farid, S. S. (2006) · Journal of Chromatography B · doi:10.1016/j.jchromb.2006.07.037 · Cited by 394
Bardor, M., Nguyen, D., Diaz, S. L., & Varki, A. P. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m412040200 · Cited by 390
Self-citationExpression systems for therapeutic glycoprotein production
Durocher, Y., & Butler, M. (2009) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2009.10.008 · Cited by 386
Implications of the presence of N-glycolylneuraminic acid in recombinant therapeutic glycoproteins
Ghaderi, D., Taylor, R. E., Padler-Karavani, V., Diaz, S., & Varki, A. (2010) · Nature Biotechnology · doi:10.1038/nbt.1651 · Cited by 372
Self-citationThe Molecular Basis for the Absence ofN-Glycolylneuraminic Acid in Humans
Irie, A., Koyama, S., Kozutsumi, Y., Kawasaki, T., & Suzuki, A. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.25.15866 · Cited by 371
Chou, H.-H., Hayakawa, T., Diaz, S. L., Krings, M., Indriati, E., Leakey, M. G., Pääbo, S., Satta, Y., Takahata, N., & Varki, A. P. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.182257399 · Cited by 351
Self-citationKoren, E., Smith, H. W., Shores, E., Shankar, G., Finco-Kent, D., Rup, B., Barrett, Y., Devanarayan, V., Gorovits, B., Gupta, S., et al. (2008) · JIM - Journal of Immunological Methods · doi:10.1016/j.jim.2008.01.001 · Cited by 332
Varki, A. P. (2001) · American Journal of Physical Anthropology · doi:10.1002/ajpa.10018 · Cited by 327
Self-citationPadler-karavani, V., Yu, H., Cao, H.-Z., Chokhawala, H. A., Karp, F., Varki, N., Chen, X., & Varki, A. (2008) · Glycobiology · doi:10.1093/glycob/cwn072 · Cited by 322
Self-citationGlycosylation engineering in yeast: the advent of fully humanized yeast
Hamilton, S. R., & Gerngross, T. U. (2007) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2007.09.001 · Cited by 322
The animal sialyltransferases and sialyltransferase-related genes: a phylogenetic approach
Harduin‐Lepers, A., Mollicone, R., Delannoy, P., & Oriol, R. (2005) · Glycobiology · doi:10.1093/glycob/cwi063 · Cited by 307
Qian, J., Liu, T., Yang, L., Daus, A., Crowley, R., & Zhou, Q. (2007) · Analytical Biochemistry · doi:10.1016/j.ab.2007.01.023 · Cited by 294
Regulation of Macropinocytosis by p21-activated Kinase-1
Dharmawardhane, S., Schürmann, A., Sells, M. A., Chernoff, J., Schmid, S. L., & Bokoch, G. (2000) · Molecular Biology of the Cell · doi:10.1091/mbc.11.10.3341 · Cited by 290
Iliopoulou, E. G., Kountourakis, P., Karamouzis, M. V., Doufexis, D., Ardavanis, A. S., Baxevanis, C. N., Rigatos, G. A., Papamichail, M., & Perez, S. A. (2010) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-010-0904-3 · Cited by 277
Malykh, Y. N., Schauer, R., & Shaw, L. (2001) · Biochimie · doi:10.1016/s0300-9084(01)01303-7 · Cited by 275
Anti‐N‐glycolylneuraminic acid antibodies identified in healthy human serum
Zhu, A., & Hurst, R. (2002) · Xenotransplantation · doi:10.1034/j.1399-3089.2002.02138.x · Cited by 274
Shankar, G., Pendley, C. E., & Stein, K. E. (2007) · Nature Biotechnology · doi:10.1038/nbt1303 · Cited by 262
Willett, W. C. (2000) · The Oncologist · doi:10.1634/theoncologist.5-5-393 · Cited by 249
Diet: Fat, Meat, and Prostate Cancer
Kolonel, L. N. (2001) · Epidemiologic Reviews · doi:10.1093/oxfordjournals.epirev.a000798 · Cited by 237
Seed‐based expression systems for plant molecular farming
Boothe, J. G., Nykiforuk, C. L., Shen, Y., Zaplachinski, S., Szarka, S. J., Kuhlman, P. S., Murray, E. W., Morck, D. W., & Moloney, M. M. (2010) · Plant Biotechnology Journal · doi:10.1111/j.1467-7652.2010.00511.x · Cited by 235
In Planta Protein Sialylation through Overexpression of the Respective Mammalian Pathway
Castilho, A., Strasser, R., Stadlmann, J., Grass, J., Jeż, J., Gattinger, P., Kunert, R., Quendler, H., Pabst, M., Leonard, R., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.088401 · Cited by 230
Multiple changes in sialic acid biology during human evolution
Varki, A. P. (2008) · Glycoconjugate Journal · doi:10.1007/s10719-008-9183-z · Cited by 222
Self-citationHeiskanen, A., Satomaa, T., Tiitinen, S. L., Laitinen, A., Mannelin, S., Impola, U., Mikkola, M., Olsson, C., Miller‐Podraza, H., Blomqvist, M., et al. (2006) · Stem Cells · doi:10.1634/stemcells.2006-0444 · Cited by 215
Fucose in N-glycans: from plant to man
Staudacher, E. (1999) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/s0304-4165(99)00181-6 · Cited by 213
Hedlund, M., Padler‐Karavani, V., Varki, N. M., & Varki, A. P. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803943105 · Cited by 204
Self-citationN -Glycolylneuraminic Acid Deficiency in Mice: Implications for Human Biology and Evolution
Hedlund, M., Tangvoranuntakul, P., Takematsu, H., Long, J. M., Housley, G. D., Kozutsumi, Y., Suzuki, A., Wynshaw-Boris, A. J., Ryan, A. F., Gallo, R. L., et al. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00379-07 · Cited by 197
Self-citationModifications of cell surface sialic acids modulate cell adhesion mediated by sialoadhesin and CD22
Kelm, S., Schauer, R., Manuguerra, J., Groß, H., & Crocker, P. R. (1994) · Glycoconjugate Journal · doi:10.1007/bf00731309 · Cited by 196
Mortality among California Seventh-Day Adventists for selected cancer sites.
Phillips, R. L., Garfinkel, L., Kuzma, J. W., Beeson, W. L., Lotz, T. M., & Brin, B. N. (1980) · PubMed · Cited by 188
Mortality among California Seventh-Day Adventists for selected cancer sites.
Phillips, R. L., Garfinkel, L., Kuzma, J., Beeson, W., Lotz, T., & Brin, B. N. (1980) · Journal of the National Cancer Institute · doi:10.1093/jnci/65.5.1097 · Cited by 187
A combined method for producing homogeneous glycoproteins with eukaryotic N-glycosylation
Schwarz, F., Huang, W., Li, C., Schulz, B. L., Lizak, C., Palumbo, A., Numao, S., Neri, D., Aebi, M., & Wang, L. (2010) · Nature Chemical Biology · doi:10.1038/nchembio.314 · Cited by 186
Higashi, H., Hirabayashi, Y., Fukui, Y., Naiki, M., Matsumoto, M., Ueda, S., & Kato, S. (1985) · PubMed · Cited by 178
Higashi, H., NAIKI, M., Matuo, S., & OKOUCHI, K. (1977) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(77)90169-3 · Cited by 174
GlycoPEGylation of recombinant therapeutic proteins produced in Escherichia coli
DeFrees, S. A., Wang, Z., Xing, R., Scott, A. E., Wang, J., Zopf, D., Gouty, D. L., Sjoberg, E. R., Panneerselvam, K., der Linden, E. C. M. B.-V., et al. (2006) · Glycobiology · doi:10.1093/glycob/cwl004 · Cited by 174
Cao, H., & Crocker, P. R. (2010) · Immunology · doi:10.1111/j.1365-2567.2010.03368.x · Cited by 172
Engineering of glycosylation in yeast and other fungi: current state and perspectives
Pourcq, K. D., Schutter, K. D., & Callewaert, N. (2010) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-010-2721-1 · Cited by 167
Brooks, S. A. (2004) · Molecular Biotechnology · doi:10.1385/mb:28:3:241 · Cited by 166
Factors controlling the glycosylation potential of the Golgi apparatus
Varki, A. P. (1998) · Trends in Cell Biology · doi:10.1016/s0962-8924(97)01198-7 · Cited by 165
Self-citationPotential impact of the non‐human sialic acid N‐glycolylneuraminic acid on transplant rejection risk
Padler‐Karavani, V., & Varki, A. (2011) · Xenotransplantation · doi:10.1111/j.1399-3089.2011.00622.x · Cited by 162
Self-citationYin, J., Hashimoto, A., Izawa, M., Miyazaki, K., Chen, G.-Y., Takematsu, H., Kozutsumi, Y., Suzuki, A., Furuhata, K., Cheng, F.-L., et al. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-2615 · Cited by 160
Chinese hamster ovary cells can produce galactose-α-1,3-galactose antigens on proteins
Bosques, C. J., Collins, B. E., Meador, J. W., Sarvaiya, H., Murphy, J. L., DelloRusso, G., Bulik, D. A., Hsu, I.-H., Washburn, N., Sipsey, S. F., et al. (2010) · Nature Biotechnology · doi:10.1038/nbt1110-1153 · Cited by 159
Loss of N-Glycolylneuraminic Acid in Human Evolution
der Linden, E. C. M. B.-V., Sjoberg, E. R., Juneja, L. R., Crocker, P. R., Varki, N. M., & Varki, A. P. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.12.8633 · Cited by 158
Self-citationTaylor, R. E., Gregg, C. J., Padler‐Karavani, V., Ghaderi, D., Yu, H., Huang, S., Sorensen, R. U., Chen, X., Jaime Inostroza, S., Nizet, V., et al. (2010) · The Journal of Experimental Medicine · doi:10.1084/jem.20100575 · Cited by 156
Self-citationAlu -mediated inactivation of the human CMP- N -acetylneuraminic acid hydroxylase gene
Hayakawa, T., Satta, Y., Gagneux, P., Varki, A. P., & Takahata, N. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.191268198 · Cited by 154
Self-citationByrne, B. J., Donohoe, G. G., & O’Kennedy, R. J. (2007) · Drug Discovery Today · doi:10.1016/j.drudis.2007.02.010 · Cited by 151
Nucleotide sugar transporters of the Golgi apparatus
Berninsone, P. M., & Hirschberg, C. B. (2000) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(00)00128-7 · Cited by 151
Diaz, S. L., Padler‐Karavani, V., Ghaderi, D., Hurtado‐Ziola, N., Yu, H., Chen, X., der Linden, E. C. M. B.-V., Varki, A. P., & Varki, N. M. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004241 · Cited by 147
Self-citationNguyen, D. H., Tangvoranuntakul, P., & Varki, A. P. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.1.228 · Cited by 145
Self-citationLewis, A. L., Desa, N., Hansen, E. E., Knirel, Y. A., Gordon, J. I., Gagneux, P., Nizet, V., & Varki, A. P. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902431106 · Cited by 141
Self-citationShaw, L., & Schauer, R. (1988) · Biological Chemistry Hoppe-Seyler · doi:10.1515/bchm3.1988.369.1.477 · Cited by 139
Castilho, A., Gattinger, P., Grass, J., Jeż, J., Pabst, M., Altmann, F., Gorfer, M., Strasser, R., & Steinkellner, H. (2011) · Glycobiology · doi:10.1093/glycob/cwr009 · Cited by 135
Padler‐Karavani, V., Hurtado‐Ziola, N., Pu, M., Yu, H., Huang, S., Muthana, S. M., Chokhawala, H. A., Cao, H., Secrest, P., Friedmann‐Morvinski, D., et al. (2011) · Cancer Research · doi:10.1158/0008-5472.can-10-4102 · Cited by 133
Self-citationGenetic engineering of recombinant glycoproteins and glycosylation pathway in mammalian host cells
Grabenhorst, E., Schlenke, P., Pohl, S., Nimtz, M., & Conradt, H. S. (1999) · Glycoconjugate Journal · doi:10.1023/a:1026466408042 · Cited by 131
Merrick, J. M., Zadarlik, K., & Milgrom, F. (2009) · International Archives of Allergy and Applied Immunology · doi:10.1159/000232140 · Cited by 127
Characterization of Mouse Sialyltransferase Genes: Their Evolution and Diversity
Takashima, S. (2008) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.80025 · Cited by 125
Hamadeh, R. M., Jarvis, G. A., Galili, U., Mandrell, R. E., Zhou, P., & Griffiss, J. M. (1992) · Journal of Clinical Investigation · doi:10.1172/jci115706 · Cited by 125
Insect cell technology is a versatile and robust vaccine manufacturing platform
Mena, J. A., & Kamen, A. (2011) · Expert Review of Vaccines · doi:10.1586/erv.11.24 · Cited by 124
Biosynthesis of N-Glycolyneuraminic Acid
Muchmore, E. A., Milewski, M., Varki, A. P., & Diaz, S. L. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)47049-x · Cited by 118
Self-citationHara, S., Yamaguchi, M., Takemori, Y., Nakamura, M., & Ohkura, Y. (1986) · Journal of Chromatography B Biomedical Sciences and Applications · doi:10.1016/s0378-4347(00)80766-5 · Cited by 115
Varki, N. M., Strobert, E. A., Dick, E. J., Benirschke, K., & Varki, A. P. (2011) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-011110-130315 · Cited by 114
Self-citationYuen, C., Storring, P. L., Tiplady, R. J., Izquierdo, M., Wait, R., Gee, C. K., Gerson, P., Lloyd, P., & Cremata, J. A. (2003) · British Journal of Haematology · doi:10.1046/j.1365-2141.2003.04307.x · Cited by 106
Carbohydrate analysis throughout the development of a protein therapeutic
Higgins, E. A. (2009) · Glycoconjugate Journal · doi:10.1007/s10719-009-9261-x · Cited by 102
Hokke, C. H., Bergwerff, A. A., van Dedem, G. W. K., van Oostrum, J., Kamerling, J. P., & Vliegenthart, J. F. G. (1990) · FEBS Letters · doi:10.1016/0014-5793(90)81427-p · Cited by 101
Xenotransplantation: the importance of the Galα1,3Gal epitope in hyperacute vascular rejection
Joziasse, D. H., & Oriol, R. (1999) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/s0925-4439(99)00056-3 · Cited by 98
Über die Erzeugung heterospezifischer Hämagglutinine durch Injektion artfremden Serums
Deicher, H. (1926) · Medical Microbiology and Immunology · doi:10.1007/bf02176298 · Cited by 94
Success stories in molecular farming—a brief overview
Faye, L. J.-Y., & Gomord, V. (2010) · Plant Biotechnology Journal · doi:10.1111/j.1467-7652.2010.00521.x · Cited by 93
N-glycosylation Engineering of Biopharmaceutical Expression Systems
Jacobs, P. P., & Callewaert, N. (2009) · Current Molecular Medicine · doi:10.2174/156652409789105552 · Cited by 92
Evidence for efficient uptake and incorporation of sialic acid by eukaryotic cells
Oetke, C., Hinderlich, S., Brossmer, R., Reutter, W. G., Pawlita, M., & Keppler, O. T. (2001) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.2001.02379.x · Cited by 90
Ailor, E., Takahashi, N., Tsukamoto, Y., Masuda, K., Rahman, B. A., Jarvis, D. L., Lee, Y. C., & Betenbaugh, M. J. (2000) · Glycobiology · doi:10.1093/glycob/10.8.837 · Cited by 84
Borys, M., Dalal, N. G., Abu‐Absi, N. R., Khattak, S. F., Jing, Y., Xing, Z., & Li, Z. J. (2009) · Biotechnology and Bioengineering · doi:10.1002/bit.22644 · Cited by 83
The perspectives for porcine-to-human xenografts
Petersen, B., Carnwath, J. W., & Niemann, H. (2008) · Comparative Immunology Microbiology and Infectious Diseases · doi:10.1016/j.cimid.2007.11.014 · Cited by 82
Participation of Cytochrome b5 in CMP-N- Acetylneuraminic Acid Hydroxylation in Mouse Liver Cytosol1
Kozutsumi, Y., Kawano, T., Yamakawa, T., & Suzuki, A. (1990) · The Journal of Biochemistry · doi:10.1093/oxfordjournals.jbchem.a123268 · Cited by 74
Hanganutziu-Deicher Antigen and Antibody in Pathologic Sera and Tissues
Nishimaki, T., Kano, K., & Milgrom, F. (1979) · The Journal of Immunology · doi:10.4049/jimmunol.122.6.2314 · Cited by 73
A Comprehensive Phylogenetic Analysis of Rieske and Rieske-Type Iron-Sulfur Proteins
Schmidt, C. L., & Shaw, L. (2001) · Journal of Bioenergetics and Biomembranes · doi:10.1023/a:1005616505962 · Cited by 71
Validation of immunoassays used to assess immunogenicity to therapeutic monoclonal antibodies
Geng, D., Shankar, G., Schantz, A., Rajadhyaksha, M., Davis, H. M., & Wagner, C. L. (2005) · Journal of Pharmaceutical and Biomedical Analysis · doi:10.1016/j.jpba.2005.04.045 · Cited by 71
What's fueling the biotech engine—2009–2010
Aggarwal, S. (2010) · Nature Biotechnology · doi:10.1038/nbt1110-1165 · Cited by 70
Fu, D., & van HALBEEK, H. (1992) · Analytical Biochemistry · doi:10.1016/s0003-2697(05)80010-7 · Cited by 70
Production of Complex Multiantennary N-Glycans in Nicotiana benthamiana Plants
Nagels, B., Damme, E. J. M. V., Pabst, M., Callewaert, N., & Weterings, K. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.110.168773 · Cited by 68
Glycan Engineering and Production of 'Humanized' Glycoprotein in Yeast Cells
Chiba, Y., & Akeboshi, H. (2009) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.32.786 · Cited by 67
Sonnenburg, J. L. (2003) · Glycobiology · doi:10.1093/glycob/cwh039 · Cited by 65
Kim, Y. K., Shin, H. S., Tomiya, N., Lee, Y. C., Betenbaugh, M. J., & Chi, H. J. (2005) · Biotechnology and Bioengineering · doi:10.1002/bit.20605 · Cited by 64
Evolution of Glycan DiversityPreprint
Varki, A. P., Freeze, H. H., & Gagneux, P. (2009) · Europe PMC (PubMed Central) · doi:10.1101/glycobiology.3e.020 · Cited by 62
Self-citationYoo, E. M., Chintalacharuvu, K. R., Penichet, M. L., & Morrison, S. L. (2002) · Journal of Immunological Methods · doi:10.1016/s0022-1759(01)00559-2 · Cited by 61
Chenu, S., Grégoire, A., Malykh, Y. N., Visvikis, A., Monaco, L., Shaw, L., Schauer, R., Marc, A., & Goergen, J. (2003) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/s0304-4165(03)00137-5 · Cited by 45
Zhang, J., & Kesteloot, H. (2005) · Nutrition and Cancer · doi:10.1207/s15327914nc5301_8 · Cited by 43
Tahara, H., Ide, K., Basnet, N. B., Tanaka, Y., Matsuda, H., Takematsu, H., Kozutsumi, Y., & Ohdan, H. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0902857 · Cited by 41
The influence of natural antibody specificity on antigen immunogenicity
Benatuil, L., Kaye, J., Rich, R. F., Fishman, J. A., Green, W. R., & Iacomini, J. (2005) · European Journal of Immunology · doi:10.1002/eji.200526146 · Cited by 41
Malykh, Y. N., Shaw, L., & Schauer, R. (1998) · Glycoconjugate Journal · doi:10.1023/a:1006959016011 · Cited by 41
Hanganutziu-Deicher antibodies in infectious mononucleosis and other diseases.
Morito, T., Kano, K., & Milgrom, F. (1982) · The Journal of Immunology · doi:10.4049/jimmunol.129.6.2524 · Cited by 40
(2013) · Glycoconjugate Journal · doi:10.1007/10719.1573-4986 · Cited by 33
Jiang, Y., Li, F., Zha, D., Potgieter, T. I., Mitchell, T., Moore, R., Cukan, M. C., Houston-Cummings, N. R., Nylen, A., Drummond, J. E., et al. (2010) · Protein Expression and Purification · doi:10.1016/j.pep.2010.11.004 · Cited by 28
Survey of Hanganutziu and Deicher Antibodies in Operated Patients
HIGASHIHARA, T., Takeshima, T., Anzai, M., Tomioka, M., Matsumoto, K., Nishida, K., Kitamura, Y., Okinaga, K., & Naiki, M. (2009) · International Archives of Allergy and Applied Immunology · doi:10.1159/000235434 · Cited by 25
Kim, Y. K., Kim, K. R., Kang, D. G., Jang, S. Y., Kim, Y. H., & Chi, H. J. (2011) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2011.03.021 · Cited by 24
Genetically Modified Animals and Pharmacological Research
Wells, D. J. (2010) · Handbook of experimental pharmacology · doi:10.1007/978-3-642-10324-7_9 · Cited by 23
Immunological studies on Kawasaki disease. I. Appearance of Hanganutziu-Deicher antibodies.
Takiguchi, M., Tamura, T., Goto, M., Kusakawa, S., Milgrom, F., & Kano, K. (1984) · PubMed Central · Cited by 22
Panitumumab: A Fully Human Monoclonal Antibody with Activity in Metastatic Colorectal Cancer
Saadeh, C. E., & Lee, H. S. (2007) · Annals of Pharmacotherapy · doi:10.1345/aph.1h492 · Cited by 20
Studies on Hanganutziu-Deicher Antigens-Antibodies
MORITO, T., Nishimaki, T., Masaki, M., Yoshida, H., Kasukawa, R., Nakarai, H., & Kano, K. (2009) · International Archives of Allergy and Applied Immunology · doi:10.1159/000234135 · Cited by 19
Heterophile Hanganutziu-Deicher Antigen in Ganglioside Fractions of Human Melanoma Tissues
Kawachi, S., Saida, T., Uhara, H., Uemura, K., Taketomi, T., & Kano, K. (2009) · International Archives of Allergy and Applied Immunology · doi:10.1159/000234536 · Cited by 18
Hillar, A., & Jarvis, D. L. (2010) · Glycobiology · doi:10.1093/glycob/cwq099 · Cited by 12
Manufacturing of Biopharmaceuticals and Implications for Biosimilars
Wurm, F. M. (2007) · Kidney & Blood Pressure Research · doi:10.1159/000107094 · Cited by 5
Human Embryonic Stem Cells Contaminated
Hampton, T. (2005) · JAMA · doi:10.1001/jama.293.7.789 · Cited by 1
Hemispheric difference in human skin color
Chaplin, G., & Jablonski, N. G. (1998) · American Journal of Physical Anthropology · doi:10.1002/(sici)1096-8644(199810)107:2
Self-citation
Flagged first, then by citations
Research works printed but not linked: 7
- Borys MC, 2009, Biotechnol Bioeng
- Dahl SL, 2011, Sci Transl Med, 3
- Hanganutziu M, 1924, CR Séances Soc Biol, 91, 1457
- Higashi H, 1985, Cancer Research, 45, 3796
- Stanley P, 2009, Essentials of Glycobiology, 101
- Takiguchi M, 1984, Clin Exp Immunol, 56, 345
- Varki A, 2009, Essentials of Glycobiology, 281
Cited by
Sorted by citations
Human cell lines for biopharmaceutical manufacturing: history, status, and future perspectives
Dumont, J., Euwart, D., Mei, B., Estes, S., & Kshirsagar, R. (2016) · Critical Reviews in Biotechnology · doi:10.3109/07388551.2015.1084266 · Cited by 483
Chemically modified and conjugated antimicrobial peptides against superbugs
Li, W., Separovic, F., O’brien-simpson, N. M., & Wade, J. D. (2021) · Chemical Society Reviews · doi:10.1039/d0cs01026j · Cited by 443
Liu, L. (2015) · Journal of Pharmaceutical Sciences · doi:10.1002/jps.24444 · Cited by 428
Emerging principles for the therapeutic exploitation of glycosylation
Dalziel, M., Crispin, M., Scanlan, C. N., Zitzmann, N., & Dwek, R. A. (2014) · Science · doi:10.1126/science.1235681 · Cited by 447
The art of CHO cell engineering: A comprehensive retrospect and future perspectives
Fischer, S., Handrick, R., & Otte, K. (2015) · Biotechnology Advances · doi:10.1016/j.biotechadv.2015.10.015 · Cited by 336
Metadata
- Authors
- Ghaderi, D., Zhang, M., Hurtado-Ziola, N., & Varki, A.
- Affiliations
- University of California San Diego (US)
- Corresponding author
- Varki, Ajit
- Venue
- Biotechnology and Genetic Engineering Reviews
- Publisher
- Informa UK Limited
- Published
- 2012-01
- Volume
- 28
- Issue
- 1
- Pages
- 147-176
- ISSN
- 0264-8725 (ISSN-L)
- 2046-5556
- OpenAlex
- W1997984454
- Cited by
- 320
- References
- 128
- Citations by year
- 2026: 9 · 2025: 11 · 2024: 15 · 2023: 13 · 2022: 22 · 2021: 29 · 2020: 29 · 2019: 30 · 2018: 25 · 2017: 30 · 2016: 24 · 2015: 36 · 2014: 23 · 2013: 21 · 2012: 3
- FWCI
- 10.68
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Biotechnology and Genetic Engineering Reviews (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Glycosylation and Glycoproteins Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Viral Infectious Diseases and Gene Expression in Insects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Transgenic Plants and Applications
- Keywords
- N-glycolylneuraminic acid, alpha-gal epitope, therapeutic glycoproteins, biologic therapy, N-glycosylation, immunogenicity, sialic acid, monoclonal antibodies
- MeSH terms
- Animals, Antibodies, Monoclonal, Epitopes, Biotechnology, Carbohydrate Sequence, Cattle, Cells, Cultured, Culture Media, Disaccharides, Glycoproteins, Glycosylation, Cricetinae, Humans, Insecta, Rabbits, Recombinant Proteins, Sialic Acids, Swine, Cell Culture Techniques, Mice
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