Metabolic glycoengineering: Sialic acid and beyond

Glycobiology

Volumn 19, Issue 12, 2009, Pages 1382-1401

  Du, Jian ^a   Meledeo, M Adam ^a   Wang, Zhiyun ^a   Khanna, Hargun S ^a   Paruchuri, Venkata D P ^a   Yarema, Kevin J ^a  

^a Johns Hopkins University   (United States)

Author keywords

Carbohydrate based drugs; Glycosylation; Metabolic glycoengineering; Sialic acid

Indexed keywords

ALKYNE; AZIDE; FUCOSE; KETONE; MONOSACCHARIDE; N ACETYLGLUCOSAMINE; POLYMER; SIALIC ACID; SIALIC ACID DERIVATIVE; THIOL;

BIOENGINEERING; BIOSYNTHESIS; BRAIN DEVELOPMENT; BRAIN DISEASE; CARBOHYDRATE METABOLISM; CELL ADHESION; CELL SURFACE; CHEMICAL REACTION; CROSS LINKING; GLYCOBIOLOGY; GLYCOSYLATION; HUMAN; IMMUNOGENICITY; MAMMAL CELL; METABOLIC GLYCOENGINEERING; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; REVIEW;

ANIMALS; BIOMEDICAL ENGINEERING; BRAIN; CARBOHYDRATE METABOLISM; GLYCOMICS; HUMANS; MODELS, BIOLOGICAL; N-ACETYLNEURAMINIC ACID; POLYSACCHARIDES;

ANIMALIA;

EID: 71049165059     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwp115     Document Type: Review

References (182)

1. Agard NJ, Prescher JA, Bertozzi CR. 2004. A strain-promoted [3 + 2] azide-alkyne cycloaddition for covalent modification of biomolecules in living systems. J Am Chem Soc. 126:15046-15047.
2. Aich U, Campbell CT, Elmouelhi N, Weier CA, Sampathkumar S-G, Choi SS, Yarema KJ. 2008. Regioisomeric SCFA attachment to hexosamines separates metabolic flux from cytotoxcity and MUC1 suppression. ACS Chem Biol 3:230-240.
3. Aich U, Yarema KJ. 2008. Metabolic oligosaccharide engineering: Perspectives, applications, and future directions. In: Fraser-Reid B, Tatsuta K, Thiem J, editors. Glycosciences. Berlin Heidelberg: Springer-Verlag. p. 2136-2190.
4. Allende ML, Proia RL. 2002. Lubricating cell signaling pathways with gangliosides. Curr Opin Struct Biol. 12:587-592.
5. Angata K, Fukuda M. 2003. Polysialyltransferases: Major players in polysialic acid synthesis on the neural cell adhesion molecule. Biochimie. 85:195-206.
6. Angata T, Varki A. 2002. Chemical diversity in the sialic acids and related α-keto acids: An evolutionary perspective. Chem Rev. 102:439-469.
7. Bardor M, Nguyen DH, Diaz S, Varki A. 2005. Mechanism of uptake and incorporation of the non-human sialic acid N-glycolylneuraminic acid into human cells. J Biol Chem. 280:4228-4237.
8. Baskin JM, Prescher JA, Laughlin ST, Agard NJ, Chang PV, Miller IA, Lo A, Codelli JA, Bertozzi CR. 2007. Copper-free click chemistry for dynamic in vivo imaging. Proc Natl Acad Sci USA. 104:16793-16797.
9. Bieberich E, MacKinnon S, Silva J, Yu RK. 2001. Regulation of apoptosis during neuronal differentiation by ceramide and b-series complex gangliosides. J Biol Chem. 276:44396-44404.
10. Bistrup A, Bhakta S, Lee JK, Belov YY, Gunn MD, Zuo F-R, Chiao-Chain H, Kannagi R, Rosen SD, Hemmerich S. 1999. Sulfotransferases of two specificities function in the reconstitution of high endothelial cell ligands for L-selectin. J Cell Biol. 145:899-910.
11. Blix G. 1936. Über die Kohlenhydratgruppen des Submaxillarismucins. Hoppe-Seyler's Z Physiol Chem. 240:43-54.
12. Blix G, Gottschalk A, Klenk E. 1957. Proposed nomenclature in the field of neuraminic and sialic acids. Nature. 179:1088.
13. Bochner BS, Alvarez RA, Mehta P, Bovin NV, Blixt O, White JR, Schnaar RL. 2005. Glycan array screening reveals a candidate ligand for Siglec-8. J Biol Chem. 280:4307-4312.
14. Boeggeman E, Ramakrishnan B, Pasek M, Manzoni M, Puri A, Loomis KH, Waybright TJ, Qasba PK. 2009. Site specific conjugation of fluoroprobes to the remodeled Fc N-glycans of monoclonal antibodies using mutant glycosyltransferases: Application for cell surface antigen detection. Bioconjug Chem. 20:1228-1236.
15. Bond MR, Zhang H, Vu PD, Kohler JJ. 2009. Photocrosslinking of glycoconjugates using metabolically incorporated diazirine-containing sugars. Nat Protoc. 4:1044-1063.
16. Bork K, Reutter W, Gerardy-Schahn R, Horstkorte R. 2005. The intracellular concentration of sialic acid regulates the polysialylation of neural cell adhesion molecule. FEBS Lett. 579:5079-5083.
17. Bourgeaux V, Piller F, Piller V. 2005. Two-step enzymatic synthesis of UDP-N-acetylgalactosamine. Bioorg Med Chem Lett. 15:5459-5462.
18. Breen KC, Georgopoulou N. 2003. The role of protein phosphorylation in α2,6(N)-sialyltransferase activity. Biochem Biophys Res Commun 309:32-35.
19. Brinkman-Van der Linden EC, Sjoberg ER, Juneja LR, Crocker PR, Varki N, Varki A. 2000. Loss of N-glycolylneuraminic acid in human evolution. Implications for sialic acid recognition by siglecs. J Biol Chem. 275:8633-8640.
20. Brossmer R, Gross HJ. 1994. Fluorescent and photoactivatable sialic acids. Meth Enzymol. 247:177-193.
21. Brusés JL, Rutishauser U. 2001. Roles, regulation, and mechanism of polysialic acid function during neural development. Biochimie. 83:635-643.
22. Campbell CT, Aich U, Weier CA, Wang JJ, Choi SS, Wen MM, Maisel K, Sampathkumar S-G, Yarema KJ. 2008. Targeting pro-invasive oncogenes with short chain fatty acid-hexosamine analogs inhibits the mobility of metastatic MDA-MB-231 breast cancer cell. J Med Chem. 51:8135-8147.
23. Campbell CT, Sampathkumar S-G, Weier C, Yarema KJ. 2007. Metabolic oligosaccharide engineering: Perspectives, applications, and future directions. Mol Biosyst. 3:187-194.
24. Campbell CT, Yarema KJ. 2005. Large-scale approaches for glycobiology. Gen Biol. 6:236.
25. Chefalo P, Pan Y, Nagy N, Guo Z, Harding CV. 2006. Efficient metabolic engineering of GM3 on tumor cells by N-phenylacetyl-D-mannosamine. Biochemistry. 45:3733-3739.
26. Chefalo P, Pan Y-B, Nagy N, Harding C, Guo Z-W. 2004. Preparation and immunological studies of protein conjugates of N-acylneuraminic acids. Glycoconj J. 20:407-414.
27. Chen HY, Challa AK, Varki A. 2006. 9-O-Acetylation of exogenously added ganglioside GD3. The GD3 molecule induces its own O acetylation machinery. J Biol Chem. 281:7825-7833.
28. Cheresh DA, Reisfeld RA, Varki A. 1984. O-Acetylation of disialoganglioside GD3 by human melanoma cells creates a unique antigenic determinant. Science. 225:844-846.
29. Chou HH, Hayakawa T, Diaz S, Krings M, Indriati E, Leakey M, Paabo S, Satta Y, Takahata N, Varki A. 2002. Inactivation of CMP-N acetylneuraminic acid hydroxylase occurred prior to brain expansion during human evolution. Proc Natl Acad Sci USA. 99:11736-11741.
30. Chou HH, Takematsu H, Diaz S, Iber J, Nickerson E, Wright KL, Muchmore EA, Nelson DL, Warren ST, Varki A. 1998. A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence. Proc Natl Acad Sci USA. 95:11751-11756.
31. Collins BE, Fralich TJ, Itonori S, Ichikawa Y, Schnaar RL. 2000. Conversion of cellular sialic acid expression from N-acetyl- to N-glycolylneuraminic acid using a synthetic precursor, N glycolylmannosamine pentaacetate: Inhibition of myelin-associated glycoprotein binding to neural cells. Glycobiology. 10:11-20.
32. Comb DG, Roseman S. 1960. The sialic acids: I. The structure and enzymatic synthesis of N-acetylneuraminic acid. J Biol Chem. 235:2529-2537.
33. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, Brown R, Baldwin S, Kraemer P, Scheff S, et al. 1994. Inactivation of the N CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature. 367:455-459.
34. Crocker PR, Varki A. 2001. Siglecs in the immune system. Immunology 103:137-145.
35. Dafik L, d'Alarcao M, Kumar K. 2008. Fluorination of mammalian cell surfaces via the sialic acid biosynthetic pathway. Bioorg Med Chem Lett. 18:5945-5947.
36. Dam TK, Brewer CF. 2002. Thermodynamic studies of lectin - carbohydrate interactions by isothermal titration calorimetry. Chem Rev. 102:387-429.
37. Daubeuf S, Aucher A, Sampathkumar SG, Preville X, Yarema KJ, Hudrisier D. 2007. Chemical labels metabolically installed into the glycoconjugates of the target cell surface can be used to track lymphocyte/target cell interplay via trogocytosis: Comparisons with lipophilic dyes and biotin. Immunol Invest. 36:687-712.
38. De Bank PA, Kellam B, Kendall DA, Shakesheff KM. 2003. Surface engineering of living myoblasts via selective periodate oxidation. Biotechnol Bioeng. 81:800-808.
39. Eckhardt M, Mühlenhoff M, Bethe A, Gerardy-Schahn R. 1996. Expression cloning of the Golgi CMP-sialic acid transporter. Proc Natl Acad Sci USA. 93:7572-7576.
40. Eisenberg I, Avidan N, Potikha T, Hochner H, Chen M, Olender T, Barash M, Shemesh M, Sadeh M, Grabov-Nardin G, et al. 2001. The UDP-N acetylglucosamine 2-epimerase/N-acetylmannosamine kinase gene is mutated in recessive hereditary inclusion body myopathy. Nat Genet 29:83-87.
41. Elmouelhi N, Aich U, Paruchuri VDP, Meledeo MA, Campbell CT, Wang JJ, Srinivas R, Khanna HS,Yarema KJ. 2009. Hexosamine template. A platform for modulating gene expression and for sugar-based drug discovery. J Med Chem. 52:2515-2530.
42. Faure C, Chalazonitis A, Rhéaume C, Bouchard G, Sampathkumar S-G, Yarema KJ, Gershon MD. 2007. Gangliogenesis in the enteric nervous system: Roles of the polysialylation of the neural cell adhesion molecule and its regulation by bone morphogenetic protein-4. Dev Dyn 236:44-59.
43. Fernandes Filho JA, Shapiro BE. 2004. Tay-Sachs disease. Arch Neurol 61:1466-1468.
44. Frand AR, Cuozzo JW, Kaiser CA. 2000. Pathways for protein disulphide bond formation. Trends Cell Biol. 10:203-210.
45. Gabius HJ. 2008. Glycans: Bioactive signals decoded by lectins. Biochem Soc Trans. 36:1491-1496.
46. Gabius H-J, Siebert H-C, André S, Jiménez-Barbero J, Rúdiger H. 2004. Chemical biology of the sugar code. ChemBioChem. 5:740-764.
47. Gagiannis D, Gossrau R, Reutter W, Zimmermann-Kordmann M, Horstkorte R. 2007. Engineering the sialic acid in organs of mice using N propanoylmannosamine. Biochim Biophys Acta. 1770:297-306.
48. Galeano B, Klootwijk R, Manoli I, Sun M, Ciccone C, Darvish D, Starost MF, Zerfas PM, Hoffmann VJ, Hoogstraten-Miller S, et al. 2007. Mutation in the key enzyme of sialic acid biosynthesis causes severe glomerular proteinuria and is rescued by N-acetylmannosamine. J Clin Invest. 117:1585-1594.
49. Goon S, Bertozzi CR. 2002. Metabolic substrate engineering as a tool for glycobiology. J Carbohydr Chem. 21:943-977.
50. Goon S, Schilling B, Tullius MV, Gibson BW, Bertozzi CR. 2003. Metabolic incorporation of unnatural sialic acids into Haemophilus ducreyi lipooligosaccharides. Proc Natl Acad Sci USA. 18:3089-3094.
51. Gross HJ, Brossmer R. 1988. Enzymatic introduction of a fluorescent sialic acid into oligosaccharide chains of glycoproteins. Eur J Biochem. 177:583-589.
52. Gross HJ, Brossmer R. 1995. Enzymatic transfer of sialic acids modified at C-5 employing four different sialyltransferases. Glycoconj J. 12:739-746.
53. Gross HJ, Rose U, Krause JM, Paulson JC, Schmid K, Feeny RE, Brossmer R. 1989. Transfer of synthetic sialic acid analogues to N- and O linked glycoprotein glycans using four different mammalian sialyltransferases. Biochemistry. 28:7386-7392.
54. Gross HJ. 1992. Fluorescent CMP-sialic acids as a tool to study the specificity of the CMP-sialic acid carrier and the glycoconjugate sialylation in permeabilized cells. Eur J Biochem. 203:269-275.
55. Gurcel C, Vercoutter-Edouart A-S, Fonbonne C, Mortuaire M, Salvador A, Michalski J-C, Lemoine J. 2008. Identification of new O-GlcNAc modified proteins using a click-chemistry-based tagging. Anal Bioanal Chem. 390:2089-2097.
56. Hackenberger CPR, Hinderlich S. 2007. Chemoselective labeling of engineered fucosylated glycoproteins. ChemBioChem. 8:1763-1765.
57. Hadfield AF, Mella SL, Sartorelli AC. 1983. N-acetyl-D-mannosamine analogues as potential inhibitors of sialic acid biosynthesis. J Pharm Sci. 72:748-751.
58. Hakomori S-I. 2002. The glycosynapse. Proc Natl Acad Sci USA. 99:225-232.
59. Han S, Collins BE, Bengtson P, Paulson JC. 2005. Homo-multimeric complexes of CD22 revealed by in situ photoaffinity protein-glycan crosslinking. Nat Chem Biol. 1:93-97.
60. Hanai N, Dohi T, Nores GA, Hakomori S. 1998. A novel ganglioside, de- N-acetyl-GM3 (II3NeuNH2LacCer), acting as a strong promoter for epidermal growth factor receptor kinase and as a stimulator for cell growth. J Biol Chem. 263:6296-6301.
61. Hang HC, Bertozzi CR. 2001. Ketone isoteres of 2-N-acetamidosugars as substrates for metabolic cell surface engineering. J Am Chem Soc 123:1242-1243.
62. Hang HC, Yu C, Kato DL, Bertozzi CR. 2003. A metabolic labeling approach toward proteomic analysis of mucin-type O-linked glycosylation. Proc Natl Acad Sci USA. 100:14846-14851.
63. Hanover JA. 2001. Glycan-dependent signaling: O-Linked N acetylglucosamine. FASEB J. 15:1865-1876.
64. Hashimoto K, Goto S, Kawano S, Aoki-Kinoshita KF, Ueda N, Hamajima M, Kawasaki T, Kanehisa M. 2006. KEGG as a glycome informatics resource. Glycobiology. 16:63R-70R.
65. Hayrinen J, Jennings H, Raff HV, Rougon G, Hanai N, Gerardy-Schahn R, Finne J. 1995. Antibodies to polysialic acid and its N-propyl derivative: Binding properties and interaction with human embryonal brain glycopeptides. J Infect Dis. 171:1481-1490.
66. Hedlund M, Padler-Karavani V, Varki NM, Varki A. 2008. Evidence for a human-specific mechanism for diet and antibody-mediated inflammation in carcinoma progression. Proc Natl Acad Sci USA. 105:18936-18941.
67. Herrler G, Gross HJ, Milks G, Paulson JC, Klenk HD, Brossmer R. 1990. Use of a sialic acid analogue to analyze the importance of the receptor-destroying enzyme for the interaction of influenza C virus with cells. Acta Histochem Suppl. 40:39-41.
68. Higa HH, Rogers GN, Paulson JC. 1985. Influenza virus hemagglutinins differentiate between receptor determinants bearing N-acetyl-, N-glycolyl-, and N,O-diacetylneuraminic acids. Virology. 144:279-282.
69. Hinderlich S, Berger M, Schwarzkopf M, Effertz K, Reutter W. 2000. Molecular cloning and characterization of murine and human N acetylglucosamine kinase. Eur J Biochem. 267:3301-3308.
70. Horstkorte R, Mühlenhoff M, Reutter W, Nöhring S, Zimmermann-Kordmann M, Gerardy-Schahn R. 2004. Selective inhibition of polysialyltransferase ST8SiaII by unnatural sialic acids. Exp Cell Res. 298:268-274.
71. Hsu T-L, Hanson SR, Kishikawa K, Wang S-K, Sawa M, Wong C-H. 2007. Alkynyl sugar analogs for the labeling and visualization of glycoconjugates in cells. Proc Natl Acad Sci USA. 104:2614-2619.
72. Irie A, Koyama S, Kozutsumi Y, Kawasaki T, Suzuki A. 1998. The molecular basis for the absence of N-glycolylneuraminic acid in humans. J Biol Chem. 273:15866-15871.
73. Iwasaki Y, Tabata E, Kurita K, Akiyoshi K. 2005. Selective cell attachment to a biomimetic polymer surface through the recognition of cell-surface tags. Bioconjug Chem. 16:567-575.
74. Iwasaki Y, Maie H, Akiyoshi K. 2007. Cell-specific delivery of polymeric nanoparticles to carbohydrate-tagging cells. Biomacromolecules. 8:3162-3168.
75. Jacobs CL, Goon S, Yarema KJ, Hinderlich S, Hang HC, Chai DH, Bertozzi CR. 2001. Substrate specificity of the sialic acid biosynthetic pathway. Biochemistry. 40:12864-12874.
76. Jin ES, Jones JG, Merritt M, Burgess SC, Malloy CR, Sherry AD. 2004. Glucose production, gluconeogenesis, and hepatic tricarboxylic acid cycle fluxes measured by nuclear magnetic resonance analysis of a single glucose derivative. Anal Biochem. 327:149-155.
77. Jones MB, Teng H, Rhee JK, Baskaran G, Lahar N, Yarema KJ. 2004. Characterization of the cellular uptake and metabolic conversion of acetylated N-acetylmannosamine (ManNAc) analogues to sialic acids. Biotechnol Bioeng. 85:394-405.
78. Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, Kawashima S, Katayama T, Araki M, Hirakawa M. 2006. From genomics to chemical genomics: Newdevelopments in KEGG. Nucleic Acids Res. 34:D354-D357.
79. Kannagi R. 2002. Regulatory roles of carbohydrate ligands for selectins in the homing of lymphocytes. Curr Opin Struct Biol. 12:599-608.
80. Kayser H, Zeitler R, Kannicht C, Grunow D, Nuck R, Reutter W. 1992a. Biosynthesis of a nonphysiological sialic acid in different rat organs, using N-propanoyl-D-hexosamines as precursors. J Biol Chem. 267:16934-16938.
81. Kayser H, Geilen CC, Paul C, Zeitler R, Reutter W. 1992b. Incorporation of N-acyl-2-amino-2-deoxy-hexoses into glycosphingolipids of the pheochromocytoma cell line PC 12. FEBS Lett. 301:137-140.
82. Keppler OT, Hinderlich S, Langner J, Schwartz-Albiez R, Reutter W, Pawlita M. 1999. UDP-GlcNAc 2-epimerase: A regulator of cell surface sialylation. Science. 284:1372-1376.
83. Keppler OT, Horstkorte R, Pawlita M, Schmidt C, Reutter W. 2001. Biochemical engineering of the N-acyl side chain of sialic acid: Biological implications. Glycobiology. 11:11R-18R.
84. Keppler OT, Stehling P, Herrmann M, Kayser H, Grunow D, Reutter W, Pawlita M. 1995. Biosynthetic modulation of sialic acid-dependent virus-receptor interactions of two primate polyoma viruses. J Biol Chem. 270:1308-1314.
85. Khidekel N, Arndt S, Lamarre-Vincent N, Lippert A, Poulin-Kerstien KG, Ramakrishnan B, Qasba PK, Hsieh-Wilson LC. 2003. A chemoenzymatic approach toward the rapid and sensitive detection of O-GlcNAc posttranslational modifications. J Am Chem Soc. 125(52):16162-16163.
86. Khidekel N, Ficarro SB, Peters EC, Hsieh-Wilson LC. 2004. Exploring the O-GlcNAc proteome: Direct identification of O GlcNAc-modified proteins from the brain. Proc Natl Acad Sci USA 101:13132-13137.
87. Kim EJ, Jones MB, Rhee JK, Sampathkumar S-G, Yarema KJ. 2004. Establishment of N-acetylmannosamine (ManNAc) analogue-resistant cell lines as improved hosts for sialic acid engineering applications. Biotechnol Prog. 20:1674-1682.
88. Kim EJ, Sampathkumar S-G, Jones MB, Rhee JK, Baskaran G, Yarema KJ. 2004. Characterization of the metabolic flux and apoptotic effects of O-hydroxyl- and N-acetylmannosamine (ManNAc) analogs in Jurkat (human T-lymphoma-derived) cells. J Biol Chem. 279:18342-18352.
89. Klenk E. 1941. Neuraminsäure, das Spaltprodukt eines neuen Gehirnlipoids. Hoppe-Seyler's Z Physiol Chem. 268:50-58.
90. Kontou M, Bauer C, Reutter W, Horstkorte R. 2008. Sialic acid metabolism is involved in the regulation of gene expression during neuronal differentiation of PC12 cells. Glycoconj J. 25:237-244.
91. Ladeby R, Wirenfeldt M, Dalmau I, Gregersen R, García-Ovejero D, Babcock A, Owens T, Finsen B. 2005. Proliferating resident microglia express the stem cell antigen CD34 in response to acute neural injury. Glia. 50:121-131.
92. Lanza F, Healy L, Sutherland DR. 2001. Structural and functional features of the CD34 antigen: An update. J Biol Regul Homeost Agents 15:1-13.
93. Lau KS, Partridge EA, Grigorian A, Silvescu CI, Reinhold VN, Demetriou M, Dennis JW. 2007. Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation. Cell. 129:123-134.
94. Laughlin ST, Baskin JM, Amacher SL, Bertozzi CR. 2008. In vivo imaging of membrane-associated glycans in developing zebrafish. Science. 320:664-667.
95. Lavis LD. 2008. Ester bonds in prodrugs. ACS Chem Biol. 3:203-206.
96. Lawrence SM, Huddleston KA, Pitts LR, Nguyen N, Lee YC, Vann WF, Coleman TA, Betenbaugh MJ. 2000. Cloning and expression of the human N acetylneuraminic acid phosphate synthase gene with 2-keto-3- deoxy-D-glycero-D-galacto-nononic acid biosynthetic ability. J Biol Chem. 275:17869-17877.
97. Lee JH, Baker TJ, Mahal LK, Zabner J, Bertozzi CR, Wiemar DF, Welsh MJ. 1999. Engineering novel cell surface receptors for virus-mediated gene transfer. J Biol Chem. 274:21878-21884.
98. Lemieux GA, Bertozzi CR. 1998. Chemoselective ligation reactions with proteins, oligosaccharides and cells. Trends Biotechnol. 16:506-513.
99. Lemieux GA, Bertozzi CR. 2001. Modulating cell surface immunoreactivity by metabolic induction of unnatural carbohydrate antigens. Chem Biol 8:265-275.
100. Lemieux GA,Yarema KJ, Jacobs CL, Bertozzi CR. 1999. Exploiting differences in sialoside expression for selective targeting of MRI contrast reagents. J Am Chem Soc. 121:4278-4279.
101. Li Y-T, Maskos K, Chou C-W, Cole RB, Li S-C. 2003. Presence of an unusual GM2 derivative, taurine-conjugated GM2, in Tay-Sachs brain. J Biol Chem. 278:35286-35291.
102. Ligos JM, de Lera TL, Hinderlich S, Guinea B, Sánchez L, Roca R, Valencia A, Bernad A. 2002. Functional interaction between the Ser/Thr kinase PKL12 and N-acetylglucosamine kinase, a prominent enzyme implicated in the salvage pathway for GlcNAc recycling. J Biol Chem 277:6333-6343.
103. Liu T, Guo Z, Yang Q, Sad S, Jennings HJ. 2000. Biochemical engineering of surface α2,8 polysialic acid for immunotargeting tumor cells. J Biol Chem. 275:32832-32836.
104. Luchansky SJ, Yarema KJ, Takahashi S, Bertozzi CR. 2003. GlcNAc 2-epimerase can serve a catabolic role in sialic acid metabolism. J Biol Chem. 278:8036-8042.
105. Lundquist JJ, Toone EJ. 2002. The cluster glycoside effect. Chem Rev 102:555-578.
106. a and sialyl Lex. Arch Biochem Biophys. 426:122-131.
107. Mahal LK, Charter NW, Angata K, Fukuda M, Koshland DE Jr, Bertozzi CR. 2001. A small-molecule modulator of poly-α2,8-sialic acid expression on cultured neurons and tumor cells. Science. 294:380-382.
108. Mahal LK, Yarema KJ, Bertozzi CR. 1997. Engineering chemical reactivity on cell surfaces through oligosaccharide biosynthesis. Science. 276:1125-1128.
109. Mahal LK, Yarema KJ, Lemieux GA, Bertozzi CR. 1999. Chemical approaches to glycobiology: Engineering cell surface sialic acids for tumor targeting. In: Inoue Y, Lee YC, Troy II FA, editors. Sialobiology and Other Novel Forms of Glycosylation. Osaka (Japan): Gakushin Publishing Company. p. 273-280.
110. Malicdan MCV, Noguchi S, Hayashi YK, Nonaka I, Nishino I. 2009. Prophylactic treatment with sialic acid metabolites precludes the development of the myopathic phenotype in the DMRV-hIBM mouse model. Nat Med. 15:690-695.
111. Malykh YN, Schauer R, Shaw L. 2001. N-Glycolylneuraminic acid in human tumours. Biochimie. 83:623-634.
112. Mantey LR, Keppler OT, Pawlita M, Reutter W, Hinderlich S. 2001. Efficient biochemical engineering of cellular sialic acids using an unphysiological sialic acid precursor in cells lacking UDP-N acetylglucosamine 2-epimerase. FEBS Lett. 503:80-84.
113. Marquardt T, John K, Freeze HH, Harns E, Vesteweber D. 1999. Correction of leukocyte adhesion deficiency type II with oral fucose. Blood. 94:3976-3985.
114. Martin SE, Peterson BR. 2003. Non-natural cell surface receptors: Synthetic peptides capped with N-cholesterylglycine efficiently deliver proteins into mammalian cells. Bioconjug Chem. 14:67-74.
115. McCarty OJT, Mousa SA, Bray PF, Konstantopoulos K. 2000. Immobilized platelets support human colon carcinoma cell tethering, rolling, and firm adhesion under dynamic flow conditions. Blood. 96:1789-1797.
116. Meutermans W, Le GT, Becker B. 2006. Carbohydrates as scaffolds in drug discovery. ChemMedChem. 1:1164-1194.
117. Mitsuoka C, Ohmori K, Kimura N, Kanamori A, Komba S, Ishida H, Kiso M, Kannagi R. 1999. Regulation of selectin binding activity by cyclization of sialic acid moiety of carbohydrate ligands on human leukocytes. Proc Natl Acad Sci USA. 96:1597-1602.
118. Miyazaki T, Angata K, Seeberger PH, Hindsgaul O, Fukuda M. 2008. CMP substitutions preferentially inhibit polysialic acid synthesis. Glycobiology. 18:187-194.
119. Monica TJ, Andersen DC, Goochee CF. 1997. A mathematical model of sialylation of N-linked oligosaccharides in the trans-Golgi network. Glycobiology. 7:515-521.
120. Morgan BL, Winick M. 1980. Effects of administration of N acetylneuraminic acid (NANA) on brain NANA content and behavior. J Nutr. 110:416-424.
121. Mühlenhoff M, Eckhardt M, Gerardy-Schahn R. 1998. Polysialic acid: Three-dimensional structure, biosynthesis, and function. Curr Opin Struct Biol. 8:558-564.
122. Murrell MP, Yarema KJ, Levchenko A. 2004. The systems biology of glycosylation. ChemBioChem. 5:1334-1447.
123. Nandi A, Sprung R, Barma DK, Zhao Y, Kim SC, Falck JR, Zhao Y. 2006. Global identification of O-GlcNAc-modified proteins. Anal Chem 78:452-458.
124. Nauman DA, Bertozzi CR. 2001. Kinetic parameters for small-molecule drug delivery by covalent cell surface targeting. Biochim Biophys Acta. 1568:147-154.
125. Oetke C, Brossmer R, Mantey LR, Hinderlich S, Isecke R, Reutter W, Keppler OT, Pawlita M. 2002. Versatile biosynthetic engineering of sialic acid in living cells using synthetic sialic acid analogues. J Biol Chem. 277:6688-6695.
126. Oetke C, Hinderlich S, Brossmer R, Reutter W, Pawlita M, Keppler OT. 2001. Evidence for efficient uptake and incorporation of sialic acid by eukaryotic cells. Eur J Biochem. 268:4553-4561.
127. Qasba PK, Boeggeman E, Ramakrishnan B. 2008. Site-specific linking of biomolecules via glycan residues using glycosyltransferases. Biotechnol Prog. 24:520-526.
128. Rideout D. 1986. Self-assembling cytotoxins. Science. 233:561-563.
129. Rideout D, Calogeropoulou T, Jaworski J, McCarthy M. 1990. Synergism through direct covalent bonding between agents: A strategy for rational design of chemotherapeutic combinations. Biopolymers. 29:247-262.
130. Sampathkumar S-G, Campbell CT, Weier C, Yarema KJ. 2006. Short-chain fatty acid-hexosamine cancer prodrugs: The sugar matters! Drug Future 31:1099-1116.
131. Sampathkumar S-G, Jones MB, Meledeo MA, Campbell CT, Choi SS, Hida K, Gomutputra P, Sheh A, Gilmartin T, Head SR, et al. 2006. Targeting glycosylation pathways and the cell cycle: Sugar-dependent activity of butyrate-carbohydrate cancer prodrugs. Chem Biol. 13:1265-1275.
132. Sampathkumar S-G, Jones MB,Yarema KJ. 2006. Metabolic expression of thiol-derivatized sialic acids on the cell surface and their quantitative estimation by flow cytometry. Nat Protoc. 1:1840-1851.
133. Sampathkumar S-G, Li AV, Jones MB, Sun Z, Yarema KJ. 2006. Metabolic installation of thiols into sialic acid modulates adhesion and stem cell biology. Nat Chem Biol. 2:149-152.
134. Sampathkumar S-G, Li A,Yarema KJ. 2006a. Sialic acid and the central nervous system: Perspectives on biological functions, detection, imaging methods and manipulation. CNS Neurol Disord - Drug Targets. 5:425-440.
135. Sampathkumar S-G, Li AV, Yarema KJ. 2006b. Synthesis of non-natural ManNAc analogs for the expression of thiols on cell surface sialic acids. Nat Protoc. 1:2377-2385.
136. Sarkar AK, Fritz TA, Taylor WH, Esko JD. 1995. Disaccharide uptake and priming in animal cells: Inhibition of sialyl Lewis X by acetylated Gal β1,4GlcNAc β-O-naphthalenemethanol. Proc Natl Acad Sci USA 92:3323-3327.
137. Sawa M, Hsu T-L, Itoh T, Sugiyama M, Hanson SR, Vogt PK, Wong C-H. 2006. Glycoproteomic probes for fluorescent imaging of fucosylated glycans in vivo. Proc Natl Acad Sci USA. 103:12371-12376.
138. Saxon E, Bertozzi CR. 2000. Cell surface engineering by a modified Staudinger reaction. Science. 287:2007-2010.
139. Saxon E, Luchansky SJ, Hang HC, Yu C, Lee SC, Bertozzi CR. 2002. Investigating cellular metabolism of synthetic azidosugars with the Staudinger ligation. J Am Chem Soc. 124:14893-14902.
140. Schauer R. 2000. Achievements and challenges of sialic acid research. Glycoconj J. 17:485-499.
141. Schilling B, Goon S, Samuels NM, Gaucher SP, Leary JA, Bertozzi CR, Gibson BW. 2001. Biosynthesis of sialylated lipooligosaccharides in Haemophilus ducreyi is dependent on exogenous sialic acid and not mannosamine. Incorporation studies using N-acylmannosamine analogues, N-glycolylneuraminic acid, and 13C-labeled N acetylneuraminic acid. Biochemistry. 40:12666-12677.
142. Schmidt C, Stehling P, Schnitzer J, Reutter W, Horstkorte R. 1998. Biochemical engineering of neural cell surfaces by the synthetic N propanoyl-substituted neuraminic acid precursor. J Biol Chem. 273:19146-19152.
143. Schnaar RL. 2004. Glycolipid-mediated cell-cell recognition in inflammation and nerve regeneration. Arch Biochem Biophys. 426:163-172.
144. Schnaar RL, Freeze HH. 2008. A "glyconutrient sham". Glycobiology 18:652-657.
145. Schwartz EL, Hadfield AF, Brown AE, Sartorelli AC. 1983. Modification of sialic acid metabolism of murine erythroleukemia cells by analogs of N-acetylmannosamine. Biochim Biophys Acta. 762:489-497.
146. Seppala R, Lehto VP, Gahl WA. 1999. Mutations in the human UDP-N acetylglucosamine 2-epimerase gene define the disease sialuria and the allosteric site of the enzyme. Am J Hum Genet. 64:1563-1569.
147. Seppala R, Tietze F, Krasnewich D, Weiss P, Ashwell G, Barsh G, Thomas GH, Packman S, Gahl WA. 1991. Sialic acid metabolism in sialuria fibroblasts. J Biol Chem. 266:7456-7461.
148. Shah MM, Fujiyama K, Flynn CR, Joshi L. 2003. Sialylated endogenous glycoconjugates in plant cells. Nat Biotechnol. 21:1470-1471.
149. Shinya K, Ebina M, Yamada S, Ono M, Kasai N, Kawaoka Y. 2006. Avian flu: Influenza virus receptors in the human airway. Nature. 440:435-436.
150. Simpson MA, Cross H, Proukakis C, Priestman DA, Neville DCA, Reinkensmeier G, Wang H, Wiznitzer M, Gurtz K, Verganelaki A, et al. 2004. Infantile-onset symptomatic epilepsy syndrome caused by a homozygous loss-of-function mutation of GM3 synthase. Nat Genet. 36:1225-1229.
151. Sprung R, Nandi A, Chen Y, Chan Kim S, Barma D, Falck JR, Zhao Y. 2005. Tagging-via-substrate strategy for probing O-GlcNAc modified proteins. J Proteome Res. 4:950-957.
152. Suzuki Y, Ito T, Suzuki T, Holland J, Robert E, Chambers TM, Kiso M, Ishida H, Kawaoka Y. 2000. Sialic acid species as a determinant of the host range of influenza A viruses. J Virol. 74:11825-11831.
153. Tanaka Y, Kohler JJ. 2008. Photoactivatable crosslinking sugars for capturing glycoprotein interactions. J Am Chem Soc. 130:3278-3279.
154. Tangvoranuntakul P, Gagneux P, Diaz S, Bardor M, Varki N, Varki A, Muchmore E. 2003. Human uptake and incorporation of an immunogenic nonhuman dietary sialic acid. Proc Natl Acad Sci USA. 100:12045-12050.
155. Tanner ME. 2005. The enzymes of sialic acid biosynthesis. Bioorg Chem 33:216-228.
156. Tate MC, García AJ, Keselowsky BG, Schumm MA, Archer DR, LaPlac MC. 2004. Specific β1 integrins mediate adhesion, migration, and differentiation of neural progenitors derived from the embryonic striatum. Mol Cell Neurosci. 27:22-31.
157. Thoden JB, Holden HM. 2005. The molecular architecture of human N acetylgalactosamine kinase. J Biol Chem. 280:32784-32791.
158. Varki A. 1997. Selectin ligands: Will the real ones please stand up? J Clin Invest. 99:158-162.
159. Varki A. 2002. Loss of N-glycolylneuraminic acid in humans: Mechanisms, consequences, and implications for hominid evolution.Am J Phys Anthropol. 116:54-69.
160. Villavicencio-Lorini P, Laabs S, Danker K, Reutter W, Horstkorte R. 2002. Biochemical engineering of the acyl side chain of sialic acids stimulates integrin-dependent adhesion of HL60 cells to fibronectin. J Mol Med. 80:671-677.
161. Viswanathan K, Lawrence S, Hinderlich S, Yarema KJ, Lee YC, Betenbaugh M. 2003. Engineering sialic acid synthetic ability into insect cells: Identifying metabolic bottlenecks and devising strategies to overcome them. Biochemistry. 42:15215-15225.
162. Vocadlo DJ, Hang HC, Kim E-J, Hanover JA, Bertozzi CR. 2003. A chemical approach for identifying O-GlcNAc-modified proteins in cells. Proc Natl Acad Sci USA. 100:9116-9121.
163. Wang B, Brand-Miller J. 2003. The role and potential of sialic acid in human nutrition. Eur J Clin Nutr. 57:1351-1369.
164. Wang B, Brand Miller J, McNeil Y, McVeagh P. 1998. Sialic acid concentration of brain gangliosides: Variation among eight mammalian species. Comp Biochem Physiol A Mol Integr Physiol. 119A:435-439.
165. Wang B, McVeagh P, Petocz P, Brand-Miller J. 2003. Brain ganglioside and glycoprotein sialic acid in breastfed compared with formula-fed infants. Am J Clin Nutr. 78:1024-1029.
166. Wang Q, Ekanayaka SA, Wu J, Zhang J, Guo Z. 2008. Synthetic and immunological studies of 5′-N-phenylacetyl sTn to develop carbohydrate-based cancer vaccines and to explore the impacts of linkage between carbohydrate antigens and carrier proteins. Bioconjug Chem 19:2060-2067.
167. Wang Q, Zhang J, Guo Z. 2007. Efficient glycoengineering of GM3 on melanoma cell and monoclonal antibody-mediated selective killing of the glycoengineered cancer cell. Bioorg Med Chem. 15:7561-7567
168. Wang Z, Sun Z, Li AV, Yarema KJ. 2006. Roles for GNE outside of sialic acid biosynthesis: Modulation of sialyltransferase and BiP expression, GM3 and GD3 biosynthesis, proliferation and apoptosis, and ERK1/2 phosphorylation. J Biol Chem. 281:27016-27028.
169. Wang-Gillam A, Pastuszak I, Elbein AD. 1998. A 17-amino acid insert changes UDP-N-acetylhexosamine pyrophosphorylase specificity from UDP-GalNAc to UDP-GlcNAc. J Biol Chem. 273:27055-27057.
170. Weihofen WA, Berger M, Chen H, Saenger W, Hinderlich S. 2006. Structures of human N-acetylglucosamine kinase in two complexes with N acetylglucosamine and with ADP/glucose: Insights into substrate specificity and regulation. J Mol Biol. 364:388-399.
171. Wieser JR, Heisner A, Stehling P, Oesch R, Reutter W. 1996. In vivo modulated N-acyl side chain of N-acetylneuraminic acid modulates the cell-dependent inhibition of growth. FEBS Lett. 395:170-173.
172. Wu J, Guo Z. 2006. Improving the antigenicity of sTn antigen by modification of its sialic acid residue for development of glycoconjugate cancer vaccines. Bioconjug Chem. 17:1537-1544.
173. Yamamoto H, Oviedo A, Sweeley C, Saito T, Moskal JR. 2001. α2,6-Sialylation of cell-surface N-glycans inhibits glioma formation in vivo. Cancer Res. 61:6822-6829.
174. Yarema KJ. 2001. New directions in carbohydrate engineering: A metabolic substrate-based approach to modify the cell surface display of sialic acids. BioTechniques. 31:384-393.
175. Yarema KJ. 2002. A metabolic substrate-based approach to engineering new chemical reactivity into cellular sialoglycoconjugates. In: Al-Rubeai M, editor. Cell Engineering Vol. 3. Glycosylation. Dordrecht (The Netherlands): Kluwer Academic Publishers. p. 171-196.
176. Yarema KJ, Bertozzi CR. 1998. Chemical approaches to glycobiology and emerging carbohydrate-based therapeutic agents. Curr Opin Chem Biol 2:49-61.
177. Yarema KJ, Goon S, Bertozzi CR. 2001. Metabolic selection of glycosylation defects in human cells. Nat Biotechnol. 19:553-558.
178. Yarema KJ, Mahal LK, Bruehl RE, Rodriguez EC, Bertozzi CR. 1998. Metabolic delivery of ketone groups to sialic acid residues. Application to cell surface glycoform engineering. J Biol Chem. 273:31168-31179.
179. Yarema KJ, Sun Z. 2005. A photochemical snapshot of CD22 binding. Nat Chem Biol. 1:69-70.
180. Yoshikawa M, Go S, Takasaki K, Kakazu Y, Ohashi M, Nagafuku M, Kabayama K, Sekimoto J, Suzuki S, Takaiwa K, et al. 2009. Mice lacking ganglioside GM3 synthase exhibit complete hearing loss due to selective degeneration of the organ of Corti. Proc Natl Acad Sci USA. 106:9483-9488.
181. Yu RK, Bieberich E, Xia T, Zeng G. 2004. Regulation of ganglioside biosynthesis in the nervous system. J Lipid Res. 45:783-793.
182. Zeng Y, Ramya TNC, Dirksen A, Dawson PE, Paulson JC. 2009. High-efficiency labeling of sialylated glycoproteins on living cells. Nat Meth. 6:207-299.