Evolutionary considerations in relating oligosaccharide diversity to biological function.

The oligosaccharide chains (glycans) attached to cell surface and extracellular proteins and lipids are known to mediate many important biological roles. However, for many glycans, there are still no evident functions that are of obvious benefit to the organism that synthesizes them. There is also no clear explanation for the extreme complexity and diversity of glycans that can be found on a given glycoconjugate or cell type. Based on the limited information available about the scope and distribution of this diversity among taxonomic groups, it is difficult to see clear trends or patterns consistent with different evolutionary lineages. It appears that closely related species may not necessarily share close similarities in their glycan diversity, and that more derived species may have simpler as well as more complex structures. Intraspecies diversity can also be quite extensive, often without obvious functional relevance. We suggest one general explanation for these observations, that glycan diversification in complex multicellular organisms is driven by evolutionary selection pressures of both endogenous and exogenous origin. We argue that exogenous selection pressures mediated by viral and microbial pathogens and parasites that recognize glycans have played a more prominent role, favoring intra- and interspecies diversity. This also makes it difficult to appreciate and elucidate the specific endogenous roles of the glycans within the organism that synthesizes them.

[1]  Joseph,et al.  Transcriptional Regulation of the Liver &Galactoside a2,6- Sialyltransferase by Glucocorticoids* , 2001 .

[2]  Lau,et al.  Regulation of ,&Galactoside ac2,6-Sialyltransferase Gene Expression by Dexamethasone* , 2001 .

[3]  R. Bontrop,et al.  Characterization of the ABO blood group genes in macaques: evidence for convergent evolution. , 2008, Tissue antigens.

[4]  S. Tsuboi,et al.  Core 2 oligosaccharide biosynthesis distinguishes between selectin ligands essential for leukocyte homing and inflammation. , 1998, Immunity.

[5]  L. Hurst,et al.  Sex and conflict. , 1998, Science.

[6]  B. Charlesworth,et al.  Why sex and recombination? , 1998, Science.

[7]  N. Sharon Lectins: From obscurity into the limelight , 1998, Protein science : a publication of the Protein Society.

[8]  M. Taylor,et al.  Evolving views of protein glycosylation. , 1998, Trends in biochemical sciences.

[9]  J. Marth,et al.  Immune regulation by the ST6Gal sialyltransferase. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[10]  S. Kornfeld Diseases of abnormal protein glycosylation: an emerging area. , 1998, The Journal of clinical investigation.

[11]  M. Costache,et al.  Evolution of Fucosyltransferase Genes in Vertebrates* , 1997, The Journal of Biological Chemistry.

[12]  K. Takamiya,et al.  Genetic remodeling of gangliosides resulted in the enhanced reactions to the foreign substances in skin. , 1997, Glycobiology.

[13]  J. Marth,et al.  Alpha-Mannosidase-II Deficiency Results in Dyserythropoiesis and Unveils an Alternate Pathway in Oligosaccharide Biosynthesis , 1997, Cell.

[14]  K. Yoshikawa,et al.  Tissue-specific knockout of the mouse Pig-a gene reveals important roles for GPI-anchored proteins in skin development. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[15]  A. Wiley Why We Get Sick: The New Science of Darwinian Medicine , 1997 .

[16]  Y. Iwakura,et al.  Growth retardation and early death of β‐1, 4‐galactosyltransferase knockout mice with augmented proliferation and abnormal differentiation of epithelial cells , 1997, The EMBO journal.

[17]  M. Costache,et al.  Molecular Cloning and Expression of a Bovine α(1,3)-Fucosyltransferase Gene Homologous to a Putative Ancestor Gene of the Human FUT3-FUT5-FUT6 Cluster* , 1997, The Journal of Biological Chemistry.

[18]  Yasuhiro Takeuchi,et al.  Infection of human cells by an endogenous retrovirus of pigs , 1997, Nature Medicine.

[19]  P. Hasty,et al.  Targeted mutation in beta1,4-galactosyltransferase leads to pituitary insufficiency and neonatal lethality. , 1997, Developmental biology.

[20]  G S Kansas,et al.  Selectins and their ligands: current concepts and controversies. , 1996, Blood.

[21]  K. Takamiya,et al.  Mice with disrupted GM2/GD2 synthase gene lack complex gangliosides but exhibit only subtle defects in their nervous system. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[22]  J. Gordon,et al.  A Model of Host-Microbial Interactions in an Open Mammalian Ecosystem , 1996, Science.

[23]  M. Salmivirta,et al.  Heparan sulfate : a piece of information , 2004 .

[24]  Petr Malý,et al.  The α(1,3)Fucosyltransferase Fuc-TVII Controls Leukocyte Trafficking through an Essential Role in L-, E-, and P-selectin Ligand Biosynthesis , 1996, Cell.

[25]  D. J. Carrigan,et al.  Plasmodium falciparum merozoite adhesion is mediated by sialic acid. , 1996, Biochemical and biophysical research communications.

[26]  C. Gahmberg,et al.  Why mammalian cell surface proteins are glycoproteins. , 1996, Trends in biochemical sciences.

[27]  L. Hooper,et al.  From legumes to leukocytes: biological roles for sulfated carbohydrates , 1996, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[28]  R. Rother,et al.  The α-Galactosyl Epitope: A Sugar Coating That Makes Viruses and Cells Unpalatable , 1996, Cell.

[29]  R. Epand,et al.  Glycophorin as a receptor for Sendai virus. , 1996, Biochemistry.

[30]  S. Tsuji,et al.  Molecular cloning and functional analysis of sialyltransferases. , 1996, Journal of biochemistry.

[31]  R. Oriol,et al.  A Missense Mutation in the FUT6 Gene Results in Total Absence of α3-Fucosylation of Human α1-Acid Glycoprotein* , 1996, The Journal of Biological Chemistry.

[32]  C. Schengrund,et al.  Ganglioside‐Induced Adherence of Botulinum and Tetanus Neurotoxins to Adducin , 1996, Journal of neurochemistry.

[33]  J. Baenziger Glycosylation: to what end for the glycoprotein hormones? , 1996, Endocrinology.

[34]  M. Ikawa,et al.  Glycosylphosphatidylinositol-anchor-deficient mice: implications for clonal dominance of mutant cells in paroxysmal nocturnal hemoglobinuria. , 1996, Blood.

[35]  J. Lau,et al.  Transcription of the β-galactoside α2,6-sialyltransferase gene in B lymphocytes is directed by a separate and distinct promoter† , 1996 .

[36]  A. Tarentino,et al.  Porcine Fibrinogen Glycopeptides: Substrates for Detecting Endo-β-N-acetylglucosaminidases F2and F3 , 1996 .

[37]  C. Porter,et al.  Sensitization of cells and retroviruses to human serum by (αl-3) galactosyltransferase , 1996, Nature.

[38]  W. Weis,et al.  Structural basis of lectin-carbohydrate recognition. , 1996, Annual review of biochemistry.

[39]  N. Sharon Carbohydrate-lectin interactions in infectious disease. , 1996, Advances in experimental medicine and biology.

[40]  Maurice W. Sabelis,et al.  The Dynamics of Multiple Infection and the Evolution of Virulence , 1995, The American Naturalist.

[41]  K. Karlsson,et al.  Microbial recognition of target-cell glycoconjugates. , 1995, Current opinion in structural biology.

[42]  P. Malý,et al.  Oocyte Galα1,3Gal Epitopes Implicated in Sperm Adhesion to the Zona Pellucida Glycoprotein ZP3 Are Not Required for Fertilization in the Mouse (*) , 1995, The Journal of Biological Chemistry.

[43]  J. Dennis,et al.  Complex asparagine-linked oligosaccharides in Mgat1-null embryos. , 1995, Glycobiology.

[44]  Ajit Varki,et al.  Oligosaccharides in vertebrate development , 1995 .

[45]  G. Lennon,et al.  Sequence and expression of a candidate for the human Secretor blood group alpha(1,2)fucosyltransferase gene (FUT2). Homozygosity for an enzyme-inactivating nonsense mutation commonly correlates with the non-secretor phenotype. , 1995, The Journal of biological chemistry.

[46]  G. Lennon,et al.  Molecular cloning of a human genomic region containing the H blood group alpha(1,2)fucosyltransferase gene and two H locus-related DNA restriction fragments. Isolation of a candidate for the human Secretor blood group locus. , 1995, The Journal of biological chemistry.

[47]  J. C. Jamieson,et al.  Release of sialyltransferases from rat liver Golgi membranes by a cathepsin D-like proteinase: comparison of the release of Galβ 1-4GlcNAcα2–6 sialyltransferase, Galβ 1–3(4)GlcNAcα 2–3 sialyltransferase and lactosylceramide α2–3 sialyltransferase (SAT-1) , 1995 .

[48]  D. Green,et al.  A Genetic Herd‐Immunity Model for the Maintenance of MHC Polymorphism , 1995, Immunological reviews.

[49]  H. Wiegandt The chemical constitution of gangliosides of the vertebrate nervous system , 1995, Behavioural Brain Research.

[50]  T. Terashima,et al.  Immunohistochemical localization of minor gangliosides in the rat central nervous system. , 1994, Glycobiology.

[51]  J. Black,et al.  Developmental Regulation of β-Galactoside α2,6-Sialyltransferase in Small Intestine Epithelium , 1994 .

[52]  J. Lowe,et al.  Molecular Basis for Lewis a( 1,3/1,4)-Fucosyltransferase Gene Deficiency (FUT3) Found in Lewis-negative Indonesian Pedigrees* , 2001 .

[53]  C. Chitnis,et al.  Receptor and ligand domains for invasion of erythrocytes by Plasmodium falciparum. , 1994, Science.

[54]  R. Oriol,et al.  Molecular basis for plasma α(1,3)-fucosyltransferase gene deficiency (FUT6) , 1994 .

[55]  D. Alford,et al.  Fusion of influenza virus with sialic acid-bearing target membranes. , 1994, Biochemistry.

[56]  M. Nowak,et al.  Adaptive evolution of highly mutable loci in pathogenic bacteria , 1994, Current Biology.

[57]  N. Sharon,et al.  Protein glycosylation. Structural and functional aspects. , 1993, European journal of biochemistry.

[58]  U. Galili Interaction of the natural anti-Gal antibody with alpha-galactosyl epitopes: a major obstacle for xenotransplantation in humans. , 1993, Immunology today.

[59]  H. Rahmann,et al.  Variability in brain ganglioside content and composition of endothermic mammals, heterothermic hibernators and ectothermic fishes , 1993, Neurochemistry International.

[60]  M. Roberts,et al.  The effect of DNA sequence divergence on sexual isolation in Bacillus. , 1993, Genetics.

[61]  J. M. Smith,et al.  How clonal are bacteria? , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[62]  J. C. Jamieson,et al.  Sialyltransferase: a novel acute-phase reactant. , 1993, Comparative biochemistry and physiology. B, Comparative biochemistry.

[63]  T. Terashima,et al.  Differential distribution of major gangliosides in rat central nervous system detected by specific monoclonal antibodies. , 1993, Glycobiology.

[64]  A. Varki,et al.  Biological roles of oligosaccharides: all of the theories are correct , 1993, Glycobiology.

[65]  R. Eddy,et al.  Chromosome mapping and organization of the human beta-galactoside alpha 2,6-sialyltransferase gene. Differential and cell-type specific usage of upstream exon sequences in B-lymphoblastoid cells. , 1993, The Journal of biological chemistry.

[66]  P. Lance,et al.  n-butyrate reduces the expression of beta-galactoside alpha 2,6-sialyltransferase in Hep G2 cells. , 1992, The Journal of biological chemistry.

[67]  J. Haynes,et al.  A malaria invasion receptor, the 175-kilodalton erythrocyte binding antigen of Plasmodium falciparum recognizes the terminal Neu5Ac(alpha 2- 3)Gal- sequences of glycophorin A , 1992, The Journal of cell biology.

[68]  A. Kobata Structures and functions of the sugar chains of glycoproteins. , 1988, European journal of biochemistry.

[69]  J. Esko Genetic analysis of proteoglycan structure, function and metabolism. , 1991, Current opinion in cell biology.

[70]  U. Galili,et al.  Gene sequences suggest inactivation of alpha-1,3-galactosyltransferase in catarrhines after the divergence of apes from monkeys. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[71]  J. Howard Disease and evolution , 1991, Nature.

[72]  D. Wilson,et al.  Species specificity in mouse glycophorin. , 1991, Biochemical and biophysical research communications.

[73]  J. Lau,et al.  Transcriptional regulation of the liver beta-galactoside alpha 2,6-sialyltransferase by glucocorticoids. , 1990, The Journal of biological chemistry.

[74]  J. Lau,et al.  Tissue-specific expression of beta-galactoside alpha-2,6-sialyltransferase. Transcript heterogeneity predicts a divergent polypeptide. , 1989, The Journal of biological chemistry.

[75]  J. Paulson,et al.  Glycoproteins: what are the sugar chains for? , 1989, Trends in biochemical sciences.

[76]  K. Hård,et al.  Analysis of N-acetyl-4-O-acetylneuraminic-acid-containing N-linked carbohydrate chains released by peptide-N4-(N-acetyl-beta-glucosaminyl)asparagine amidase F. Application to the structure determination of the carbohydrate chains of equine fibrinogen. , 1989, European journal of biochemistry.

[77]  J. Lau,et al.  Regulation of beta-galactoside alpha 2,6-sialyltransferase gene expression by dexamethasone. , 1989, The Journal of biological chemistry.

[78]  S. Shohet,et al.  Man, apes, and Old World monkeys differ from other mammals in the expression of alpha-galactosyl epitopes on nucleated cells. , 1988, The Journal of biological chemistry.

[79]  J. Haynes,et al.  Falciparum malaria parasites invade erythrocytes that lack glycophorin A and B (MkMk). Strain differences indicate receptor heterogeneity and two pathways for invasion. , 1987, The Journal of clinical investigation.

[80]  N. Katunuma,et al.  Structures of Sugar Chains of Human Kidney γ-Glutamyltranspeptidase , 1986 .

[81]  N. Katunuma,et al.  Structures of sugar chains of human kidney gamma-glutamyltranspeptidase. , 1986, Journal of biochemistry.

[82]  P. Debeire,et al.  Primary structure of two major glycans of bovine fibrinogen. , 1985, European journal of biochemistry.

[83]  T. Higashi,et al.  The structures of the carbohydrate moieties of mouse kidney gamma-glutamyltranspeptidase: occurrence of X-antigenic determinants and bisecting N-acetylglucosamine residues. , 1985, Archives of biochemistry and biophysics.

[84]  N. Katunuma,et al.  Difference in the sugar chains of two subunits and of isozymic forms of rat kidney gamma-glutamyltranspeptidase. , 1983, Archives of biochemistry and biophysics.

[85]  J C Jamieson,et al.  Glycoprotein biosynthesis during the acute-phase response to inflammation. , 1983, Canadian journal of biochemistry and cell biology = Revue canadienne de biochimie et biologie cellulaire.

[86]  H. Nader,et al.  Structural differences of heparan sulfates according to the tissue and species of origin. , 1983, Biochemical and biophysical research communications.

[87]  N. Katunuma,et al.  Structural studies of the carbohydrate moieties of rat kidney gamma-glutamyltranspeptidase. An extremely heterogeneous pattern enriched with nonreducing terminal N-acetylglucosamine residues. , 1983, The Journal of biological chemistry.

[88]  S. Tonegawa,et al.  Somatic generation of antibody diversity. , 1976, Nature.

[89]  A. Kobata,et al.  Carbohydrate Structures of Bovine Kidney γ-Glutamyltranspeptidase , 1983 .

[90]  A. Kobata,et al.  Carbohydrate structures of bovine kidney gamma-glutamyltranspeptidase. , 1983, Journal of biochemistry.

[91]  J. Takamatsu,et al.  Comparative studies on the structures of the carbohydrate moieties of human fibrinogen and abnormal fibrinogen Nagoya. , 1982, Journal of Biochemistry (Tokyo).

[92]  C. Dietrich,et al.  Distribution of sulfated mucopolysaccharides in invertebrates. , 1977, The Journal of biological chemistry.

[93]  P. Feldman Evolution of sex , 1975, Nature.

[94]  L. V. Valen,et al.  Two modes of evolution , 1974, Nature.

[95]  T. Dobzhansky Nothing in Biology Makes Sense Except in the Light of Evolution , 1973 .