Some Important Milestones in the History of Glycobiology

Ajit Varki; Stuart Kornfeld

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Varki A, Cummings RD, Esko JD, et al., editors. Essentials of Glycobiology [Internet]. 4th edition. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2022.

Essentials of Glycobiology [Internet]. 4th edition.

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Online Appendix 1ASome Important Milestones in the History of Glycobiology

Ajit Varki and Stuart Kornfeld.

Year(s)	Primary Scientist(s)	Milestone	Chapters^a
1876	J.L.W. Thudichum	Glycosphingolipids (cerebrosides), sphingomyelin, and sphingosine	11
1888	H. Stillmark	Lectins as hemagglutinins	28, 30, 31
1891	H.E. Fischer	Stereoisomeric structure of glucose and other monosaccharides	2
1897	E. Buchner	Cell-free extracts carry out fermentation of carbohydrates	5
1900	K. Landsteiner	Human ABO blood groups as transfusion barriers	6, 13
1901	W. Koenigs and E. Knorr	Glycosylation chemistry	53
1909	P.A. Levene	Structure of ribose in RNA	2
1916	J. MacLean	Isolation of heparin as an anticoagulant	17, 38
1920	O. Meyerhof	Conversion of glycogen to lactic acid in muscle	5, 18
1925	P.A. Levene	Characterization of chondroitin sulfate and “mucoitin sulfate” (later, hyaluronan)	16, 17
1929	P.A. Levene	Structure of 2-deoxyribose in DNA	2
1929	W.N. Haworth	Pyranose and furanose ring structures of monosaccharides	2
1934	K. Meyer	Hyaluronan and hyaluronidase	16
1934–1938	G. Blix, E. Klenk	Sialic acids	15
1936	C.F. Cori, G.T. Cori	Glucose-1-phosphate as an intermediate in glycogen biosynthesis	18
1942–1946	G.K. Hirst, F.M. Burnet	Hemagglutination of influenza virus and “receptor-destroying enzyme”	15, 37
1942	E. Klenk, G. Blix	Gangliosides in brain	11, 15
1946	Z. Dische	Colorimetric determination of deoxypentoses and other carbohydrates	2
1948–1950	E. Jorpes, S. Gardell	Occurrence of N-sulfates in heparin and identification of heparan sulfate	17
1949	L.F. Leloir	Nucleotide sugars and their role in the biosynthesis of glycans	5
1950	Karl Schmid	Isolation of α1-acid glycoprotein (orosomucoid), a major serum glycoprotein	9
1952	W.T. Morgan, W.M. Watkins	Carbohydrate determinants of ABO blood group types	13
1952	E.A. Kabat	Relationship of ABO to Lewis blood groups and secretor vs. nonsecretor status	13
1952	A. Gottschalk	Sialic acid as the receptor for influenza virus	15
1952	T. Yamakawa	Globoside, the major glycosphingolipid of the erythrocyte membrane	11
1953	R. Lemieux	Synthesis of sucrose	53
1956–1963	M.R.J. Salton, J.M. Ghuysen, R.W. Jeanloz, N. Sharon, H.M. Flowers	Bacterial peptidoglycan backbone structure; major structural polysaccharides in nature (chitin, cellulose, and peptidoglycan) β1-4-linked throughout	21, 22, 23
1957	P.W. Robbins, F. Lipmann	Biosynthesis and characterization of PAPS, the donor for glycan sulfation	5, 17
1957	H. Faillard, E. Klenk	Crystallization of N-acetylneuraminic acid as product of influenza virus receptor-destroying enzyme (RDE) (“neuraminidase”)	15
1957–1963	J. Strominger, J.T. Park, H.R. Perkins, H.J. Rogers	Mechanism of peptidoglycan biosynthesis and site of penicillin action	21
1958	H. Muir	“Mucopolysaccharides” are covalently attached to proteins via serine	17
1958	J. Baddiley	Discovery of cell-wall teichoic acids	21
1960	D.C. Comb, S. Roseman	Structure and enzymatic synthesis of CMP-N-acetylneuraminic acid	5, 15
1960–1965	O. Westphal, O. Lüderitz, H. Nikaido, P.W. Robbins	Isolation of lipopolysaccharides and endotoxin glycans	21
1960–1970	R. Jeanloz, K. Meyer, A. Dorfman	Structural studies of glycosaminoglycans	16, 17
1961	S. Roseman, L. Warren	Biosynthesis of sialic acid	5, 15
1961–1965	G.E. Palade	Endoplasmic reticulum (ER)–Golgi pathway for glycoprotein biosynthesis and secretion	4
1962	A. Neuberger, R. Marshall, I. Yamashina, L.W. Cunningham	GlcNAc-Asn as the first defined carbohydrate-peptide linkage	9
1962	W.M. Watkins, W.Z. Hassid	Enzymatic synthesis of lactose from UDP-galactose and glucose	5
1962	J.A. Cifonelli, J. Ludowieg, A. Dorfman	Iduronic acid as a constituent of heparin	17
1962–1966	L. Roden, U. Lindahl	Identification of tetrasaccharide linking glycosaminoglycans to protein core of proteoglycans	17
1962	E.H. Eylar, R.W. Jeanloz	Demonstration of the presence of N-acetyllactosamine in α1-acid glycoprotein	14
1963	L. Svennerholm	Analysis and nomenclature of gangliosides	11
1963	D. Hamerman, J. Sandson	Covalent cross-linkage between hyaluronan and inter-α-trypsin inhibitor	16
1963–1964	B. Anderson, K. Meyer, V.P. Bhavanandan, A. Gottschalk	β-elimination of Ser/Thr-O-linked glycans	10
1963–1965	R. Kuhn, H. Wiegandt	Structure of GM1 and other brain gangliosides	11
1963–1966	M.J. Osborn, E.C. Heath	Discovery of Kdo in lipopolysaccharide (LPS)	21
1963–1967	B.L. Horecker, P.W. Robbins, H. Nakaido, M.J. Osborn	Lipid-linked intermediates in bacterial lipopolysaccharide and peptidoglycan biosynthesis	21
1964	V. Ginsburg	GDP-fucose and its biosynthesis from GDP-mannose	5
1964	B. Gesner, V. Ginsburg	Glycans control the migration of leukocytes to target organs	34
1965	L.W. Cunningham	Microheterogeneity of glycoprotein glycans	1, 9, 10
1965–1966	R.O. Brady	Glucocerebrosidase is the enzyme deficient in Gaucher disease	44
1965–1967	M.J. Osborn, A. Wright, P.W. Robbins, L. Rothfield, H. Nikaido, B.L. Horecker	Undecaprenol-linked intermediates in the biosynthesis of LPS O-antigens	21
1965–1975	J.E. Silbert, U. Lindahl	Cell-free biosynthesis of heparin and chondroitin sulfate	17
1965–1975	W. Pigman	Tandem repeat amino acid sequences with Ser or Thr as O-glycosylation sites in mucins	10
1966	M. Neutra, C. Leblond	Role of Golgi apparatus in protein glycosylation	4
1966–1969	B. Lindberg, S. Hakomori	Refinement of methylation analysis for determination of glycan linkages	50
1966–1976	R. Schauer	Multiple modifications of sialic acids in nature, their biosynthesis, and degradation	15
1967	L. Rodén, L.-Å. Fransson	Demonstration of a copolymeric structure for dermatan sulfate	17
1967	R.D. Marshall	N-glycosylation occurs only at asparagine residues in the motif Asn-X-Ser/Thr	9
1968	J.A. Cifonelli	Description of the domain structure of heparan sulfate	17
1968	R.L. Hill, K. Brew	α-lactalbumin as a modifier of galactosyltransferase specificity	6
1969	L. Warren, M.C. Glick, P.W. Robbins	Increased size of N-glycans in malignantly transformed cells	9, 47
1969	R.J. Winzler, R. Spiro	Structures of O-glycans from erythrocyte membranes and fetuin.	10
1969–1974	V.C. Hascall, S.W. Sajdera, H. Muir, D. Heinegård, T. Hardingham	Hyaluronan–proteoglycan interactions in cartilage	16, 17
1969	H. Tuppy, P. Meindl	Synthesis of 2-deoxy-2,3-didehydro-Neu5Ac as viral sialidase inhibitor	15
1968–1970	E. Neufeld	Identification of lysosomal enzyme deficiencies in the mucopolysaccharidoses	44
1969	G. Ashwell, A. Morell	Glycans can control the lifetime of glycoproteins in blood circulation	28
1970	K.O. Lloyd, J. Porath, I.J. Goldstein	Use of lectins for affinity purification of glycoproteins	48
1971–1973	L.F. Leloir	Dolichylphosphosugars are intermediates in protein N-glycosylation	5, 9
1971–1975	P. Kraemer, J.E. Silbert	Heparan sulfate as a common constituent of vertebrate cell surfaces	17
1971–1980	B. Toole	Hyaluronan in differentiation, morphogenesis, and development	16
1972–1982	S. Hakomori	Lacto- and globo-series glycosphingolipids as developmentally regulated and tumor-associated antigens	11, 47
1972	J.F.G. Vliegenthart	High-field proton nuclear magnetic resonance (NMR) spectroscopy for structural analysis of glycans	2, 50
1973	W.E. van Heyningen	Glycosphingolipids are receptors for bacterial toxins	37, 42
1973	J. Montreuil, R.G. Spiro, R. Kornfeld	A common pentasaccharide core structure of all N-glycans	9
1974	C.E. Ballou	Structure of yeast mannans and generation of yeast mannan mutants	23, 49
1974	A.L. Tarentino, T.H. Plummer, F. Maley, N. Koide, T. Muramatsu	Purification and characterization of Endo-b-N-acetylglucosaminidase H and D	50
1975	V.I. Teichberg	Identification of the first galectin	36
1975	V.T. Marchesi	Primary structure of glycophorin, the first known transmembrane glycoprotein	4, 9, 10
1975–1976	U.B. Sleytr, J.L. Strominger	Protein glycosylation in thermophilic gram-positive bacteria and in Archaea	21, 22
1975–1980	A. Kobata	N- and O-glycan structural elucidation using multiple convergent techniques	2, 9, 10
1975–1980	P. Stanley, S. Kornfeld, R.C. Hughes	Lectin-resistant cell lines with glycosylation defects	49
1977	W.J. Lennarz	Asn-X-Ser/Thr necessary and sufficient for lipid-mediated N-glycosylation	9
1977	I. Ofek, D. Mirelman, N. Sharon	Cell-surface glycans as attachment sites for infectious bacteria	37, 42
1977–1978	S. Kornfeld, P.W. Robbins	Biosynthesis and processing of intermediates of N-glycans in protein glycosylation	9
1977	R.L. Hill, R. Barker	First purification of a glycosyltransferase involved in protein glycosylation	6, 9
1977	N. Koide, T. Muramatsu	IgG Fc glycans have a role in immunologic interactions	7
1978	C. Svanborg	Glycosphingolipids as receptors for bacterial adhesion	11, 37, 42
1978	D. Solter, B.B. Knowles	Discovery of stage-specific embryonic antigens (e.g. SSEA-1 [Lewis x])	41
1979	R.R. Schmidt	Trichloroacetimidate glycosylation method	53
1979–1982	E. Neufeld, S. Kornfeld, K. Von Figura, W. Sly	The mannose-6-phosphate pathway for lysosomal enzyme trafficking	33
1980–1981	J. Rothman, R. Schekman	Cell-free analysis of ER–Golgi transport pathway for glycoconjugates	4
1980–1983	F.A. Troy, J. Finne, S. Inoue, Y. Inoue	Structure of polysialic acids in bacteria and vertebrates	15
1980	H. Schachter	Role of glycosyltransferases in N- and O-glycan branching	6, 9, 10
1980–1982	V.N. Reinhold, A. Dell, A.L. Burlingame	Mass spectrometry for structural analysis of glycans	50, 51
1980–1985	S. Hakomori, Y. Nagai	Glycosphingolipids as modulators of transmembrane signaling	11
1981	R.P. Silver, W.F. Vann	Expression of bacterial polysaccharide from cloned genes in a heterologous host	21
1981–1985	M.J. Ferguson, I. Silman, M. Low	Structural definition of glycosylphosphatidylinositol (GPI) anchors	12
1982	J. Paulson, R. Hill	Differential influenza virus binding to a2-6- and a2-3-linked sialic acids	42
1982	U. Lindahl, R.D. Rosenberg	Specific sulfated heparin pentasaccharide sequence recognized by antithrombin	17, 38
1982	C. Hirschberg, R. Fleischer	Transport of sugar nucleotides into the Golgi apparatus	4, 9, 10
1983	C.R.H. Raetz	Discovery of lipid X, 2,3-diacyl-glucosamine-1-P, confirmation of lipid A structure	21
1984	G. Hart	Intracellular protein glycosylation by O-GlcNAc	19
1984	J. Jaeken	Description of “carbohydrate-deficient glycoprotein syndromes”	45
1984	P. Albersheim, A. Darvill	Free glycans serve as specific signaling molecules in plants	40
1984	Y.A. Knirel	Discovery of pseudaminic acid the first prokaryotic nonulosonic acid	15
1984–1990	J. Esko	Replica plate selection of mutants with altered glycosaminoglycan biosynthesis	17
1984	I. Vlodavsky	Isolation of heparanase	17
1985	R.B. Parekh, R.A. Dwek, T.W. Rademacher, A. Kobata	Rheumatoid arthritis associated with changes in IgG glycosylation	7, 46
1985	S. Kusumoto, T. Shiba, C. Galanos, O. Luderitz, E.T. Rietschel, O. Westphal, H. Brade	Synthesis of lipid A and confirmation of endotoxic properties	21
1985	M. Klagsbrun, D. Gospodarowicz	Discovery of heparin–FGF interactions	38
1986	W.J. Whelan	Glycogen is a glycoprotein synthesized on a glycogenin primer	18
1986	J.U. Baenziger	Structures of sulfated N-glycans of pituitary hormones	14, 31
1986	Y. Inoue, S. Inoue	Discovery of 2-keto-3-deoxynononic acid (Kdn) in rainbow trout eggs	15
1986	P.K. Qasba, J. Shaper, N. Shaper	Cloning of first animal glycosyltransferase	6
1987	A. Imberty, S Perez	Double helical structure of starch	24
1987	Y-C. Lee	High-performance anion-exchange chromatography of oligosaccharides with pulsed amperometric detection (HPAEC-PAD)	50
1988	K. Drickamer	Prediction of carbohydrate recognition domains (CRDs) from primary structures	28, 34
1989	G.W. Hart, P. Englund	Glycosylphosphatidylinositol anchor biosynthetic pathway in trypanosomes	43
1989	M. Bevilacqua, E. Butcher, B. Furie, L. Lasky, R. McEver, S. Rosen, B. Seed, M. Siegelman, L. Stoolman, I. Weissman, J Magnani, S. Hakomori, J. Paulson, M. Tiemeyer, M. Fukuda, A. Varki, R. Cummings, M.A. Gimbrone, R.S. Cotran, J.J.Woodruff	Discovery of selectins and selectin ligands	34
1990	F. Yamamoto, H. Clausen, S. Hakomori	Molecular genetic basis for ABO blood groups—cloning of the A/B glycosyltransferases	14
1990–2005	Fu-Tong Liu, G. Rabinovich, R. Cummings, G. Vasta, L. Baum	Discovery of the roles of galectins in innate and adaptive immunity.	36
1990–2006	P. Orlean, D.E. Levin, A. Conzelmann, H. Riezman, Y. Jigami	Identification of genes involved in GPI anchor biosynthesis and transport in Saccharomyces cerevisiae	12
1991	B. Henrissat	Classification of glycoside hydrolases	8
1991	R. Brady	Enzyme replacement therapy via mannose receptor for Gaucher disease	31, 44
1991	A. Varki, S. Hedrick	Glycosylation modification in mice by expressing a degradative enzyme	6
1992–1997	R. Gilmore, M. Aebi, L. Lehle, N. Dean, W. Lennarz	Molecular identification of oligosaccharyltransferase	6,9
1992–1997	W. Reutter, C. Bertozzi	Metabolic incorporation of unnatural monosaccharide precursors, bioorthogonal glycan labeling in living systems	56
1993	T. Kinoshita, J. Takeda	Somatic mutations in PIGA gene cause paroxysmal nocturnal hemoglobinuria	45, 46
1993	S. van Boeckel, M. Petitou	Synthesis of heparin anticoagulant pentasaccharide	17, 53
1993–1999	T. Kinoshita	Glycosylphosphatidylinositol anchor biosynthetic genes in mammals	12
1993–1998	P. Crocker, A. Varki	Discovery of and classification of Siglecs	35
1993–2004	F.K. Hagen, L.A. Tabak, K. G. Ten Hagen, T. A. Fritz	First cloning and crystal structure of ppGalNAcT, identification of functional subclasses	10
1994	P. Stanley, J. Marth, J. Lowe	Inactivation of glycosyltransferase genes in mice	9, 41
1994	A. Parodi, A. Helenius, J. Bergeron, D.Y. Thomas, D.B. Williams	Calnexin/calreticulin facilitate glycoprotein folding in ER	7, 39
1995–2001	N. Taniguchi, J.W. Dennis, M. Demetriou	N-glycan modifications impact receptor signaling, immunity, growth, carcinogenesis and metastasis	9, 47
1995	L. Powell, A. Varki	Definition of I-type lectins	35
1996	H. Freeze, T. Marquardt	Mannose corrects N-glycosylation in one type of congenital disorder of glycosylation	45
1996–1998	A. Polissi, C. Georgopoulos, C.R.H. Raetz	Discovery of MsbA, the lipid A transporter	21
1997	P.M. Rudd, R.A. Dwek	High-performance liquid chromatography (HPLC)-based glycan analysis	9, 10
1997	J. Egrie	Enhancement of erythropoietin activity through glycoengineering	57
1997–2000	F.M. Platt, T.D. Butters, A. Zimram, R.A. Dwek, J. Shayman	Glycosphingolipid synthase inhibitors for therapy of glycolipid storage diseases	44, 55
1998	C.M. West	Discovery of complex cytoplasmic glycosylation in Dictyostelium	18
1998	B. Henrissat	CAZy database available online	31, 52
1998	M. Aebi, Y. Yamaguchi, K. Kato, J. Weissman	Glycans regulate ER-associated degradation (ERAD)	39
1998	A. Suzuki, A. Varki	Inactivating mutation of CMP-Neu5Ac hydroxylase in humans	15,20
1999	P. Guerry, M. Aebi, C. Szymanski, M. Young	Prokaryotes make N-linked glycans	21, 22
1999	P. Gagneux, A. Varki	Evolutionary synthesis relating glycan diversity to intrinsic and extrinsic function	20
1999	C.W. von der Lieth	Development of platforms for glycoinformatics	52
2000	R. Haltiwanger, K. Irvine, P. Stanley, F. Vogt, H. Clausen, S. Cohen	Glycosyltransferases are essential components of Notch signaling pathway	13, 14, 26
2001	P. Seeberger, C.-H. Wong	Automated glycan synthesis	53
2001	P.K. Qasba	Crystal structure of b1-4GalT-I in complex with a-lactalbumin	6
2001	J. Hofsteenge	Discovery of C-mannosylation	2
2001	K. Campbell, T. Endo	Defective synthesis of dystroglycan O-mannose glycans in muscular dystrophy	45
2001	T. Ju, R. Cummings	Core 1 b-galactosyltransferase stability requires the unique chaperone Cosmc	10
2001–2005	L. Borsig, N.M. Varki, A Varki	P- and L-selectin facilitation of tumor metastasis, inhibitable by heparin	34, 47
2001–2006	T. Angata, N.M. Varki, A Varki,	Human-specific changes in CD33-related Siglecs	35
2002	K.G. Ten Hagen, D.T. Tran, H. Clausen	Discovery that a ppGalNAcT is essential for viability	10, 26
2002	T. Feizi, D. Wang, P.H. Seeberger, C-H. Wong, R. Cummings, J. Paulson, O. Blixt	Invention of natural and synthetic glycan microarrays	52
2002	C. Costello, A. Dell	Matrix-assisted laser desorption/ionization (MALDI)-mass spectrometry of glycans	50, 51
2005	L.K. Mahal, J. Hirabayashi	Lectin microarrays for glycomic analysis	48
2006	A.M. Almeida, Y. Murakami, T. Kinoshita, A. Karadimitris	Discovery of inherited GPI deficiency	12, 45, 46
2006	T. Angata, T. Hayakawa, M. Nakamura	Discovery of paired Siglec receptors	35

: This time line of events is deliberately terminated about 15 years ago, on the assumption that it can take a long time to be certain that a particular discovery or milestone has had a major impact on the field.
^a: Indicates main chapter(s) of this book in which the relevant topics are covered.

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Varki A, Kornfeld S. Some Important Milestones in the History of Glycobiology. In: Varki A, Cummings RD, Esko JD, et al., editors. Essentials of Glycobiology [Internet]. 4th edition. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2022. Online Appendix 1A.
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