Glycomics: Revealing the dynamic ecology and evolution of sugar molecules

Journal of Proteomics

Volumn 135, Issue , 2016, Pages 90-100

  Springer, Stevan A ^a,b   Gagneux, Pascal ^a,b  

^a University of California San Diego   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cellular ecology; Glycans; Glycoconjugates; Natural variation; Polymorphism

Indexed keywords

ANTIBODY; CARBOHYDRATE; DNA; GLYCAN; GLYCOCONJUGATE; GLYCOLIPID; GLYCOSAMINOGLYCAN; LIPID; MONOSACCHARIDE; PROTEIN; POLYSACCHARIDE;

BIOCHEMISTRY; BIOENGINEERING; CELL INTERACTION; CHEMICAL COMPOSITION; CHEMICAL INTERACTION; CHEMICAL STRUCTURE; ECOLOGY; ENVIRONMENTAL FACTOR; EUKARYOTE; EXTRACELLULAR MATRIX; GENETICS; GENOTYPE; GLYCOBIOLOGY; MOLECULAR BIOLOGY; MOLECULAR EVOLUTION; MUTAGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROKARYOTE; QUANTITATIVE ANALYSIS; REVIEW; SYNTHESIS; METABOLISM;

ECOLOGY; EVOLUTION, MOLECULAR; GLYCOMICS; POLYSACCHARIDES;

EID: 84960795442     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2015.11.022     Document Type: Review

References (102)

1. Springer S.A., Gagneux P. Glycan evolution in response to collaboration, conflict, and constraint. J. Biol. Chem. 2013, 288:6904-6911.
2. Marth J.D. A unified vision of the building blocks of life. Nat. Cell Biol. 2008, 10:1015-1016.
3. Bishop J.R., Gagneux P. Evolution of carbohydrate antigens-microbial forces shaping host glycomes?. Glycobiology 2007, 17:23R-34R.
4. Kasaai M.R. Various methods for determination of the degree of N-acetylation of chitin and chitosan: a review. J. Agric. Food Chem. 2009, 57:1667-1676.
5. Honke K., Taniguchi N. Sulfotransferases and sulfated oligosaccharides. Med. Res. Rev. 2002, 22:637-654.
6. Muramatsu T., Muramatsu H. Carbohydrate antigens expressed on stem cells and early embryonic cells. Glycoconj. J. 2004, 21:41-45.
7. Yang W.H., Aziz P.V., Heithoff D.M., Mahan M.J., Smith J.W., Marth J.D. An intrinsic mechanism of secreted protein aging and turnover. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:13657-13662.
8. Springer S.A., Crespi B.J., Swanson W.J. Beyond the phenotypic gambit: molecular behavioural ecology and the evolution of genetic architecture. Mol. Ecol. 2011, 20:2240-2257.
9. Ridley B.L., O'Neill M.A., Mohnen D. Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 2001, 57:929-967.
10. Carpita N.C., Gibeaut D.M. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J. 1993, 3:1-30.
11. Esko J.D., Kimata K., Lindahl U. Proteoglycans and sulfated glycosaminoglycans. Essentials of Glycobiology 2009.
12. Sorensen I., Domozych D., Willats W.G. How have plant cell walls evolved?. Plant Physiol. 2010, 153:366-372.
13. Biermann C.H., Marks J.A., Vilela-Silva A.C., Castro M.O., Mourao P.A. Carbohydrate-based species recognition in sea urchin fertilization: another avenue for speciation?. Evol. Dev. 2004, 6:353-361.
14. Pang P.C., Chiu P.C., Lee C.L., Chang L.Y., Panico M., Morris H.R., Haslam S.M., Khoo K.H., Clark G.F., Yeung W.S., Dell A. Human sperm binding is mediated by the sialyl-Lewis(x) oligosaccharide on the zona pellucida. Science 2011, 333:1761-1764.
15. Tecle E., Gagneux P. Sugar coated sperm: unravelling the function of the mammalian sperm glycocalyx. Mol. Reprod. Dev. 2015, 82:635-650.
16. Hennen E., Czopka T., Faissner A. Structurally distinct LewisX glycans distinguish subpopulations of neural stem/progenitor cells. J. Biol. Chem. 2011, 286:16321-16331.
17. Mirouse V., Christoforou C.P., Fritsch C., Johnston D.S., Ray R.P. Dystroglycan and perlecan provide a basal cue required for epithelial polarity during energetic stress. Dev. Cell 2009, 16:83-92.
18. Ikonen E., Simons K. Protein and lipid sorting from the trans-Golgi network to the plasma membrane in polarized cells. Semin. Cell Dev. Biol. 1998, 9:503-509.
19. Matsuo I., Kimura-Yoshida C. Extracellular distribution of diffusible growth factors controlled by heparan sulfate proteoglycans during mammalian embryogenesis. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2014, 369.
20. Fenderson B.A., Stamenkovic I., Aruffo A. Localization of hyaluronan in mouse embryos during implantation, gastrulation and organogenesis. Differentiation 1993, 54:85-98.
21. Ohtsubo K., Marth J.D. Glycosylation in cellular mechanisms of health and disease. Cell 2006, 126:855-867.
22. Hart G.W. Three Decades of research on O-GlcNAcylation - a major nutrient sensor that regulates signaling, transcription and cellular metabolism. Front. Endocrinol. (Lausanne) 2014, 5:183.
23. Varki A. Since there are PAMPs and DAMPs, there must be SAMPs? Glycan "self-associated molecular patterns" dampen innate immunity, but pathogens can mimic them. Glycobiology 2011, 21:1121-1124.
24. Boller T., Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 2009, 60:379-406.
25. Kono H., Rock K.L. How dying cells alert the immune system to danger. Nat. Rev. Immunol. 2008, 8:279-289.
26. Ashwell G., Harford J. Carbohydrate-specific receptors of the liver. Annu. Rev. Biochem. 1982, 51:531-554.
27. Grewal P.K., Uchiyama S., Ditto D., Varki N., Le D.T., Nizet V., Marth J.D. The Ashwell receptor mitigates the lethal coagulopathy of sepsis. Nat. Med. 2008, 14:648-655.
28. Schnaar R.L., Gerardy-Schahn R., Hildebrandt H. Sialic acids in the brain: gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration. Physiol. Rev. 2014, 94:461-518.
29. Lackie P.M., Zuber C., Roth J. Polysialic acid of the neural cell adhesion molecule (N-CAM) is widely expressed during organogenesis in mesodermal and endodermal derivatives. Differentiation 1994, 57:119-131.
30. Compagno D., Jaworski F.M., Gentilini L., Contrufo G., Gonzalez Perez I., Elola M.T., Pregi N., Rabinovich G.A., Laderach D.J. Galectins: major signaling modulators inside and outside the cell. Curr. Mol. Med. 2014, 14:630-651.
31. Chen H.Y., Weng I.C., Hong M.H., Liu F.T. Galectins as bacterial sensors in the host innate response. Curr. Opin. Microbiol. 2014, 17:75-81.
32. McEver R.P., Moore K.L., Cummings R.D. Leukocyte trafficking mediated by selectin-carbohydrate interactions. J. Biol. Chem. 1995, 270:11025-11028.
33. Genbacev O.D., Prakobphol A., Foulk R.A., Krtolica A.R., Ilic D., Singer M.S., Yang Z.Q., Kiessling L.L., Rosen S.D., Fisher S.J. Trophoblast L-selectin-mediated adhesion at the maternal-fetal interface. Science 2003, 299:405-408.
34. Flint H.J., Bayer E.A., Rincon M.T., Lamed R., White B.A. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat. Rev. Microbiol. 2008, 6:121-131.
35. Smant G., Stokkermans J.P., Yan Y., de Boer J.M., Baum T.J., Wang X., Hussey R.S., Gommers F.J., Henrissat B., Davis E.L., Helder J., Schots A., Bakker J. Endogenous cellulases in animals: isolation of beta-1, 4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:4906-4911.
36. Backhed F., Ley R.E., Sonnenburg J.L., Peterson D.A., Gordon J.I. Host-bacterial mutualism in the human intestine. Science 2005, 307:1915-1920.
37. Zivkovic A.M., German J.B., Lebrilla C.B., Mills D.A. Human milk glycobiome and its impact on the infant gastrointestinal microbiota. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(Suppl. 1):4653-4658.
38. Ilg K., Yavuz E., Maffioli C., Priem B., Aebi M. Glycomimicry: display of the GM3 sugar epitope on Escherichia coli and Salmonella enterica sv Typhimurium. Glycobiology 2010, 20:1289-1297.
39. Vimr E.R., Kalivoda K.A., Deszo E.L., Steenbergen S.M. Diversity of microbial sialic acid metabolism. Microbiol. Mol. Biol. Rev. 2004, 68:132-153.
40. Surana N. K., and D. L. Kasper. The yin yang of bacterial polysaccharides: lessons learned from B. fragilis PSA. Immunol. Rev. 2012, 245:13-26.
41. Hooper L.V., Gordon J.I. Glycans as legislators of host-microbial interactions: spanning the spectrum from symbiosis to pathogenicity. Glycobiology 2001, 11:1R-10R.
42. Gagneux P., Varki A. Evolutionary considerations in relating oligosaccharide diversity to biological function. Glycobiology 1999, 9:747-755.
43. Lehotzky R.E., Partch C.L., Mukherjee S., Cash H.L., Goldman W.E., Gardner K.H., Hooper L.V. Molecular basis for peptidoglycan recognition by a bactericidal lectin. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:7722-7727.
44. Cohen M., Zhang X.Q., Senaati H.P., Chen H.W., Varki N.M., Schooley R.T., Gagneux P. Influenza A penetrates host mucus by cleaving sialic acids with neuraminidase. Virol. J. 2013, 10:321.
45. Lindberg A.A. Bacteriophage receptors. Annu. Rev. Microbiol. 1973, 27:205-241.
46. Reitter J.N., Means R.E., Desrosiers R.C. A role for carbohydrates in immune evasion in AIDS. Nat. Med. 1998, 4:679-684.
47. Cook J.D., Lee J.E. The secret life of viral entry glycoproteins: moonlighting in immune evasion. PLoS Pathog. 2013, 9.
48. Smit C.H., van Diepen A., Nguyen D.L., Wuhrer M., Hoffmann K.F., Deelder A.M., Hokke C.H. Glycomic analysis of life stages of the human parasite Schistosoma mansoni reveals developmental expression profiles of functional and antigenic glycan motifs. Mol. Cell. Proteomics 2015, 14:1750-1769.
49. King R.A. Statictical ecology. Annual Reviews of Statistics and its Application 2014, 1:401-426.
50. Yang Z., Bielawski J.P. Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 2000, 15:496-503.
51. Zeng Q., Sukumaran J., Wu S., Rodrigo A. Neutral models of microbiome evolution. PLoS Comput. Biol. 2015, 11.
52. Barton N.H., Keightley P.D. Understanding quantitative genetic variation. Nat. Rev. Genet. 2002, 3:11-21.
53. Koenig J.E., Spor A., Scalfone N., Fricker A.D., Stombaugh J., Knight R., Angenent L.T., Ley R.E. Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(Suppl 1):4578-4585.
54. Kashyap P.C., Marcobal A., Ursell L.K., Smits S.A., Sonnenburg E.D., Costello E.K., Higginbottom S.K., Domino S.E., Holmes S.P., Relman D.A., Knight R., Gordon J.I., Sonnenburg J.L. Genetically dictated change in host mucus carbohydrate landscape exerts a diet-dependent effect on the gut microbiota. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:17059-17064.
55. Grafen A. Natural selection, kin selection and group selection. Behavioural Ecology an Evolutionary Approach 1984, 62-84. Blackwell Scientific Publications, Oxford. J.R. Krebs, N.B. Davies (Eds.).
56. Hendry A.P., Kinnison M.T. An introduction to microevolution: rate, pattern, process. Genetica 2001, 112-113:1-8.
57. Pigliucci M. An extended synthesis for evolutionary biology. Ann. N. Y. Acad. Sci. 2009, 1168:218-228.
58. Day T., Bonduriansky R. A unified approach to the evolutionary consequences of genetic and nongenetic inheritance. Am. Nat. 2011, 178:E18-E36.
59. Hardiville S., Hart G.W. Nutrient regulation of signaling, transcription, and cell physiology by O-GlcNAcylation. Cell Metab. 2014, 20:208-213.
60. Barrett R.D., Hoekstra H.E. Molecular spandrels: tests of adaptation at the genetic level. Nat. Rev. Genet. 2011, 12:767-780.
61. Lowe J.B., Marth J.D. A genetic approach to Mammalian glycan function. Annu. Rev. Biochem. 2003, 72:643-691.
62. Springer S.A., Diaz S.L., Gagneux P. Parallel evolution of a self-signal: humans and new world monkeys independently lost the cell surface sugar Neu5Gc. Immunogenetics 2014, 66:671-674.
63. Galili U., Shohet S.B., Kobrin E., Stults C.L., Macher B.A. Man, apes, and Old World monkeys differ from other mammals in the expression of alpha-galactosyl epitopes on nucleated cells. J. Biol. Chem. 1988, 263:17755-17762.
64. Takeuchi Y., Porter C.D., Strahan K.M., Preece A.F., Gustafsson K., Cosset F.L., Weiss R.A., Collins M.K. Sensitization of cells and retroviruses to human serum by (alpha 1-3) galactosyltransferase. Nature 1996, 379:85-88.
65. Wolver S.E., Sun D.R., Commins S.P., Schwartz L.B. A peculiar cause of anaphylaxis: no more steak? The journey to discovery of a newly recognized allergy to galactose-alpha-1,3-galactose found in mammalian meat. J. Gen. Intern. Med. 2013, 28:322-325.
66. Cooper D.K. Identification of alpha Gal as the major target for human anti-pig antibodies. Xenotransplantation 2009, 16:47-49.
67. Kristian S.A., Hwang J.H., Hall B., Leire E., Iacomini J., Old R., Galili U., Roberts C., Mullis K.B., Westby M., Nizet V. Retargeting pre-existing human antibodies to a bacterial pathogen with an alpha-Gal conjugated aptamer. J. Mol. Med. (Berl.) 2015, 93:619-631.
68. Chou H.H., Hayakawa T., Diaz S., Krings M., Indriati E., Leakey M., Paabo S., Satta Y., Takahata N., Varki A. Inactivation of CMP-N-acetylneuraminic acid hydroxylase occurred prior to brain expansion during human evolution. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:11736-11741.
69. Ghaderi D., Springer S.A., Ma F., Cohen M., Secrest P., Taylor R.E., Varki A., Gagneux P. Sexual selection by female immunity against paternal antigens can fix loss of function alleles. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:17743-17748.
70. Ng P.S., Bohm R., Hartley-Tassell L.E., Steen J.A., Wang H., Lukowski S.W., Hawthorne P.L., Trezise A.E., Coloe P.J., Grimmond S.M., Haselhorst T., von Itzstein M., Paton A.W., Paton J.C., Jennings M.P. Ferrets exclusively synthesize Neu5Ac and express naturally humanized influenza A virus receptors. Nat. Commun. 2014, 5:5750.
71. Schwarz F., Fong J.J., Varki A. Human-specific evolutionary changes in the biology of siglecs. Adv. Exp. Med. Biol. 2015, 842:1-16.
72. Aymard J.P. [Karl Landsteiner (1868-1943) and the discovery of blood groups]. Transfus. Clin. Biol. 2012, 19:244-248.
73. Yamamoto F., Cid E., Yamamoto M., Saitou N., Bertranpetit J., Blancher A. An integrative evolution theory of histo-blood group ABO and related genes. Sci. Rep. 2014, 4:6601.
74. Marionneau S., Ruvoen N., Le Moullac-Vaidye B., Clement M., Cailleau-Thomas A., Ruiz-Palacois G., Huang P., Jiang X., Le Pendu J. Norwalk virus binds to histo-blood group antigens present on gastroduodenal epithelial cells of secretor individuals. Gastroenterology 2002, 122:1967-1977.
75. Neil S.J., McKnight A., Gustafsson K., Weiss R.A. HIV-1 incorporates ABO histo-blood group antigens that sensitize virions to complement-mediated inactivation. Blood 2005, 105:4693-4699.
76. Adibekian, A., P. Stallforth, M. Hecht, D. B. Werz, P. Gagneux, and P. H. Seeberger. Comparative bioinformatics analysis of the mammalian and bacterial glycomes. Chem. Sci. 2: 337-344.
77. Schwarz F., Aebi M. Mechanisms and principles of N-linked protein glycosylation. Curr. Opin. Struct. Biol. 2011, 21:576-582.
78. Stanley P., Schachter H., Taniguchi N. N-Glycans. Essentials of Glycobiology 2009.
79. Hang I., Lin C.W., Grant O.C., Fleurkens S., Villiger T.K., Soos M., Morbidelli M., Woods R.J., Gauss R., Aebi M. Analysis of site-specific N-glycan remodellingI in the ER and the Golgi. Glycobiology 2015.
80. Stepan H., Staudacher E. Optimization of monosaccharide determination using anIthranilic acid and 1-phenyl-3-methyl-5-pyrazolone for gastropod analysis. Anal. Biochem. 2011, 418:24-29.
81. Brockhausen I., Schachter H., Stanley P. O-GalNAc Glycans. Essentials of Glycobiology 2009.
82. Stanford K.I., Bishop J.R., Foley E.M., Gonzales J.C., Niesman I.R., Witztum J.L., Esko J.D. Syndecan-1 is the primary heparan sulfate proteoglycan mediating hepatic clearance of triglyceride-rich lipoproteins in mice. J. Clin. Invest. 2009, 119:3236-3245.
83. Crawford B.E., Garner O.B., Bishop J.R., Zhang D.Y., Bush K.T., Nigam S.K., Esko J.D. Loss of the heparan sulfate sulfotransferase, Ndst1, in mammary epithelial cells selectively blocks lobuloalveolar development in mice. PLoS One 2010, 5.
84. Miller G.M., Hsieh-Wilson L.C. Sugar-dependent modulation of neuronal development, regeneration, and plasticity by chondroitin sulfate proteoglycans. Exp. Neurol. 2015.
85. Schnaar R.L., Suzuki A., Stanley P. Glycosphingolipids. Essentials of Glycobiology 2009.
86. Ferguson M.A.J., Kinoshita T., Hart G.W. Glycosylphosphatidylinositol Anchors. Essentials of Glycobiology 2009.
87. Schaffer C., Graninger M., Messner P. Prokaryotic glycosylation. Proteomics 2001, 1:248-261.
88. Freeze H.H., Haltiwanger R.S. Other Classes of ER/Golgi-derived Glycans. Essentials of Glycobiology 2009.
89. Defaus S., Gupta P., Andreu D., Gutierrez-Gallego R. Mammalian protein glycosylation-structure versus function. Analyst 2014, 139:2944-2967.
90. Ito S. Form and function of the glycocalyx on free cell surfaces. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 1974, 268:55-66.
91. Sharon N., Lis H. History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology 2004, 14:53R-62R.
92. O'Reilly M.K., Paulson J.C. Multivalent ligands for siglecs. Methods Enzymol. 2010, 478:343-363.
93. Paulson J.C., Blixt O., Collins B.E. Sweet spots in functional glycomics. Nat. Chem. Biol. 2006, 2:238-248.
94. Tissot B., North S.J., Ceroni A., Pang P.C., Panico M., Rosati F., Capone A., Haslam S.M., Dell A., Morris H.R. Glycoproteomics: past, present and future. FEBS Lett. 2009, 583:1728-1735.
95. Moothoo D.N., Naismith J.H. A general method for co-crystallization of concanavalin A with carbohydrates. Acta Crystallogr. D Biol. Crystallogr. 1999, 55:353-355.
96. Huang M.L., Cohen M., Fisher C.J., Schooley R.T., Gagneux P., Godula K. Determination of receptor specificities for whole influenza viruses using multivalent glycan arrays. Chem. Commun. (Camb.) 2015, 51:5326-5329.
97. Orr S.L., Le D., Long J.M., Sobieszczuk P., Ma B., Tian H., Fang X., Paulson J.C., Marth J.D., Varki N. A phenotype survey of 36 mutant mouse strains with gene-targeted defects in glycosyltransferases or glycan-binding proteins. Glycobiology 2013, 23:363-380.
98. Freeze H.H., Eklund E.A., Ng B.G., Patterson M.C. Neurological aspects of human glycosylation disorders. Annu. Rev. Neurosci. 2015, 38:105-125.
99. Crocker P.R., Paulson J.C., Varki A. Siglecs and their roles in the immune system. Nat. Rev. Immunol. 2007, 7:255-266.
100. Chang P.V., Prescher J.A., Hangauer M.J., Bertozzi C.R. Imaging cell surface glycans with bioorthogonal chemical reporters. J. Am. Chem. Soc. 2007, 129:8400-8401.
101. Cohen M., Varki A. Modulation of glycan recognition by clustered saccharide patches. Int. Rev. Cell Mol. Biol. 2014, 308:75-125.
102. Moremen K.W., Tiemeyer M., Nairn A.V. Vertebrate protein glycosylation: diversity, synthesis and function. Nat. Rev. Mol. Cell Biol. 2012, 13:448-462.