Metabolism of vertebrate amino sugars with N-glycolyl groups: Incorporation of N-glycolylhexosamines into mammalian glycans by feeding N- glycolylgalactosamine

Journal of Biological Chemistry

Volumn 287, Issue 34, 2012, Pages 28898-28916

  Bergfeld, Anne K ^a   Pearce, Oliver M T ^a   Diaz, Sandra L ^a   Lawrence, Roger ^a   Vocadlo, David J ^c   Choudhury, Biswa ^a   Esko, Jeffrey D ^a   Varki, Ajit ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c SIMON FRASER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHETIC PATHWAY; BREAKDOWN PRODUCTS; CELL SURFACES; CHINESE HAMSTER OVARY CELLS; CHONDROITIN; ENZYMATIC REACTION; GLYCANS; HEPARAN SULFATES; HEXOSAMINES; KEY ENZYMES; MAMMALIAN ENZYMES; METABOLIC INTERMEDIATES; METABOLIC PATHWAYS; N-ACETYLNEURAMINIC ACID; N-GLYCOLYLNEURAMINIC ACID; O-GLYCANS; O-GLYCOSYLATION; SALVAGE PATHWAY; SIALIC ACIDS;

BIOCHEMISTRY; BIOSYNTHESIS; CARBOXYLIC ACIDS; DEGRADATION; ENZYMES; GLUCOSE; MAMMALS; MASS SPECTROMETRY;

METABOLISM;

AMINOSUGAR; CHONDROITIN SULFATE; DERMATAN SULFATE; GANGLIOSIDE; GLYCAN DERIVATIVE; HEXOSAMINE; N GLYCOLOYLNEURAMINIC ACID; N GLYCOLYLGALACTOSAMINE; N GLYCOLYLHEXOSAMINE; SIALIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOHYDRATE METABOLISM; CARBOHYDRATE TRANSPORT; CATABOLISM; CELL METABOLISM; CONTROLLED STUDY; EMBRYO; ENZYME METABOLISM; EPIMERIZATION; FEMALE; GLYCOLYSIS; GLYCOSYLATION; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ANALYSIS;

ANIMALS; CARBOHYDRATE EPIMERASES; CHO CELLS; CHONDROITIN SULFATES; CRICETINAE; CRICETULUS; DERMATAN SULFATE; HEPARITIN SULFATE; HUMANS; MICE; MICE, KNOCKOUT; N-ACETYLNEURAMINIC ACID; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); URIDINE DIPHOSPHATE SUGARS;

EID: 84865216752     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.363499     Document Type: Article

References (69)

1. Bergfeld, A. K., Pearce, O. M., Diaz, S. L., Pham, T., and Varki, A. (2012) Metabolism of vertebrate amino sugars with N-glycolyl groups. Elucidating the intracellular fate of the non-human sialic acid N-glycolylneuraminic acid. J. Biol. Chem. 287, jbc.M112.363549(1801)
2. Varki, A., Cummings, R. D., Esko, J. D., Freeze, H. H., Stanley, P., Bertozzi, C. R., Hart, G. W., and Etzler, M. E. (2009) in Essentials of Glycobiology (Varki, A., Cummings, R. D., Esko, J. D., Freeze, H. H., Stanley, P., Bertozzi, C. R., Hart, G. W., and Etzler, M. E., eds) Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
3. Stanley, P., Schachter, H., and Taniguchi, N. (2009) in Essentials of Glycobiology (Varki, A., Cummings, R. D., Esko, J. D., Freeze, H. H., Stanley, P., Bertozzi, C. R., Hart, G. W., and Etzler, M. E., eds) pp. 101-114, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
4. Brockhausen, I., Schachter, H., and Stanley, P. (2009) in Essentials of Glycobiology (Varki, A., Cummings, R. D., Esko, J. D., Freeze, H. H., Stanley, P., Bertozzi, C. R., Hart, G. W., and Etzler, M. E., eds) pp. 115-128, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
5. Macauley, M. S., Chan, J., Zandberg, W., He, Y., Whitworth, G. A., Stubbs, K. A., Yuzwa, S., Varki, A., Davies, G. J., and Vocadlo, D. J. (2012) Metabolism of vertebrate amino sugars with N-glycolyl groups. Intracellular O-GlcNGc, UDP-GlcNGc, and the biochemical and structural rationale for the substrate tolerance of O-GlcNAcase. J. Biol. Chem. 287, jbc.M112.363721 (1802)
6. Schnaar, R. L., Suzuki, A., and Stanley, P. (2009) in Essentials of Glycobiology (Varki, A., Cummings, R. D., Esko, J. D., Freeze, H. H., Stanley, P., Bertozzi, C. R., Hart, G. W., and Etzler, M. E., eds) pp. 129-142, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
7. Esko, J. D., Kimata, K., and Lindahl, U. (2009) in Essentials of Glycobiology (Varki, A., Cummings, R. D., Esko, J. D., Freeze, H. H., Stanley, P., Bertozzi, C. R., Hart, G. W., and Etzler, M. E., eds) pp. 229-248, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
8. Cohen, M., and Varki, A. (2010) The sialome. Far more than the sum of its parts. OMICS 14, 455-464
9. Shaw, L., and Schauer, R. (1988) The biosynthesis of N- glycoloylneuraminic acid occurs by hydroxylation of the CMP-glycoside of N-acetylneuraminic acid. Biol. Chem. Hoppe-Seyler 369, 477-486
10. Kozutsumi, Y., Kawano, T., Yamakawa, T., and Suzuki, A. (1990) Participation of cytochrome b5 in CMP-N-acetylneuraminic acid hydroxylation in mouse liver cytosol. J. Biochem. 108, 704-706
11. Shaw, L., Schneckenburger, P., Carlsen, J., Christiansen, K., and Schauer, R. (1992) Mouse liver cytidine-′-monophosphate-N-acetylneuraminic acid hydroxylase. Catalytic function and regulation. Eur. J. Biochem. 206, 269-277
12. Kawano, T., Kozutsumi, Y., Takematsu, H., Kawasaki, T., and Suzuki, A. (1993) Regulation of biosynthesis of N-glycolylneuraminic acid-containing glycoconjugates. Characterization of factors required for NADH-dependent cytidine 5′-monophosphate-N-acetylneuraminic acid hydroxylation. Glycoconj. J. 10, 109-115 (Pubitemid 23168578)
13. Shaw, L., Schneckenburger, P., Schlenzka, W., Carlsen, J., Christiansen, K., Jürgensen, D., and Schauer, R. (1994) CMP-N-acetylneuraminic acid hydroxylase from mouse liver and pig submandibular glands. Interaction with membrane-bound and soluble cytochrome b5-dependent electron transport chains. Eur. J. Biochem. 219, 1001-1011 (Pubitemid 24050971)
14. Takematsu, H., Kawano, T., Koyama, S., Kozutsumi, Y., Suzuki, A., and Kawasaki, T. (1994) Reaction mechanism underlying CMP-N-acetylneuraminic acid hydroxylation in mouse liver. Formation of a ternary complex of cytochrome b5, CMP-N-acetylneuraminic acid, and a hydroxylation enzyme. J. Biochem. 115, 381-386
15. Kawano, T., Koyama, S., Takematsu, H., Kozutsumi, Y., Kawasaki, H., Kawashima, S., Kawasaki, T., and Suzuki, A. (1995) Molecular cloning of cytidine monophospho-N-acetylneuraminic acid hydroxylase. Regulation of species- and tissue-specific expression of N-glycolylneuraminic acid. J. Biol. Chem. 270, 16458-16463
16. Schlenzka, W., Shaw, L., Kelm, S., Schmidt, C. L., Bill, E., Trautwein, A. X., Lottspeich, F., and Schauer, R. (1996) CMP-N-acetylneuraminic acid hydroxylase. The first cytosolic Rieske iron-sulfur protein to be described in Eukarya. FEBS Lett. 385, 197-200 (Pubitemid 26169815)
17. Chou, H. H., Takematsu, H., Diaz, S., Iber, J., Nickerson, E., Wright, K. L., Muchmore, E. A., Nelson, D. L., Warren, S. T., and Varki, A. (1998) A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence. Proc. Natl. Acad. Sci. U.S.A. 95, 11751-11756
18. Irie, A., Koyama, S., Kozutsumi, Y., Kawasaki, T., and Suzuki, A. (1998) The molecular basis for the absence of N-glycolylneuraminic acid in humans. J. Biol. Chem. 273, 15866-15871 (Pubitemid 28298210)
19. Hayakawa, T., Aki, I., Varki, A., Satta, Y., and Takahata, N. (2006) Fixation of the human-specific CMP-N-acetylneuraminic acid hydroxylase pseudogene and implications of haplotype diversity for human evolution. Genetics 172, 1139-1146 (Pubitemid 43345445)
20. Varki, A. (2001) N-Glycolylneuraminic acid deficiency in humans. Biochimie 83, 615-622
21. Higashi, H., Hirabayashi, Y., Fukui, Y., Naiki, M., Matsumoto, M., Ueda, S., and Kato, S. (1985) Characterization of N-glycolylneuraminic acid-containing gangliosides as tumor-associated Hanganutziu-Deicher antigen in human colon cancer. Cancer Res. 45, 3796-3802 (Pubitemid 15226460)
22. Miyoshi, I., Higashi, H., Hirabayashi, Y., Kato, S., and Naiki, M. (1986) Detection of 4-O-acetyl-N-glycolylneuraminyl lactosylceramide as one of tumor-associated antigens in human colon cancer tissues by specific antibody. Mol. Immunol. 23, 631-638 (Pubitemid 16035006)
23. Hirabayashi, Y., Higashi, H., Kato, S., Taniguchi, M., and Matsumoto, M. (1987) Occurrence of tumor-associated ganglioside antigens with Hanganutziu-Deicher antigenic activity on human melanomas. Jpn. J. Cancer Res. 78, 614-620 (Pubitemid 17106247)
24. Kawachi, S., Saida, T., Uhara, H., Uemura, K., Taketomi, T., and Kano, K. (1988) Heterophile Hanganutziu-Deicher antigen in ganglioside fractions of human melanoma tissues. Int. Arch. Allergy Appl. Immunol. 85, 381-383 (Pubitemid 18078921)
25. Devine, P. L., Clark, B. A., Birrell, G. W., Layton, G. T., Ward, B. G., Alewood, P. F., and McKenzie, I. F. (1991) The breast tumor-associated epitope defined by monoclonal antibody 3E1.2 is an O-linked mucin carbohydrate containing N-glycolylneuraminic acid. Cancer Res. 51, 5826-5836
26. Malykh, Y. N., Schauer, R., and Shaw, L. (2001)N-Glycolylneuraminic acid in human tumors. Biochimie 83, 623-634
27. Diaz, S. L., Padler-Karavani, V., Ghaderi, D., Hurtado-Ziola, N., Yu, H., Chen, X., Brinkman-Van der Linden, E. C., Varki, A., and Varki, N. M. (2009) Sensitive and specific detection of the non-human sialic acid N-glycolylneuraminic acid in human tissues and biotherapeutic products. PLoS ONE 4, e4241
28. Tangvoranuntakul, P., Gagneux, P., Diaz, S., Bardor, M., Varki, N., Varki, A., and Muchmore, E. (2003) Human uptake and incorporation of an immunogenic nonhuman dietary sialic acid. Proc. Natl. Acad. Sci. U.S.A. 100, 12045-12050 (Pubitemid 37271512)
29. Bardor, M., Nguyen, D. H., Diaz, S., and 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 (Pubitemid 40288589)
30. Banda, K., Gregg, C. J., Chow, R., Varki, N., and Varki, A. (2012) Metabolism of vertebrate amino sugars with N-glycolyl groups. Mechanisms underlying gastrointestinal incorporation of the non-human sialic acid xenoautoantigen, N-glycolylneuraminic acid. J. Biol. Chem. 287, J. Biol. Chem. 287, jbc.M112.364182 (1803)
31. Padler-Karavani, V., Yu, H., Cao, H., Chokhawala, H., Karp, F., Varki, N., Chen, X., and Varki, A. (2008) Diversity in specificity, abundance, and composition of anti-Neu5Gc antibodies in normal humans. Potential implications for disease. Glycobiology 18, 818-830
32. Nguyen, D. H., Tangvoranuntakul, P., and Varki, A. (2005) Effects of natural human antibodies against a nonhuman sialic acid that metabolically incorporates into activated and malignant immune cells. J. Immunol. 175, 228-236 (Pubitemid 40884323)
33. Varki, N. M., Strobert, E., Dick, E. J., Jr., Benirschke, K., and Varki, A. (2011) Biomedical differences between human and nonhuman hominids: potential roles for uniquely human aspects of sialic acid biology. Annu. Rev. Pathol. 6, 365-393
34. Verheijen, F. W., Verbeek, E., Aula, N., Beerens, C. E., Havelaar, A. C., Joosse, M., Peltonen, L., Aula, P., Galjaard, H., van der Spek, P. J., and Mancini, G. M. (1999) A new gene, encoding an anion transporter, is mutated in sialic acid storage diseases. Nat. Genet. 23, 462-465
35. Dube, D. H., Prescher, J. A., Quang, C. N., and Bertozzi, C. R. (2006) Probing mucin-type O-linked glycosylation in living animals. Proc. Natl. Acad. Sci. U.S.A. 103, 4819-4824
36. Pouilly, S., Piller, V., and Piller, F. (2012) Metabolic glycoengineering through the mammalian GalNAc salvage pathway. FEBS J. 279, 586 -598
37. Pouilly, S., Bourgeaux, V., Piller, F., and Piller, V. (2012) Evaluation of analogues of GalNAc as substrates for enzymes of the mammalian GalNAc pathway. ACS Chem. Biol. 7, 753-760
38. Hang, H. C., Yu, C., Kato, D. L., and Bertozzi, C. R. (2003) A metabolic labeling approach toward proteomic analysis of mucin-type O-linked glycosylation. Proc. Natl. Acad. Sci. U.S.A. 100, 14846-14851 (Pubitemid 37517979)
39. Laughlin, S. T., and Bertozzi, C. R. (2007) Metabolic labeling of glycans with azido sugars and subsequent glycan-profiling and visualization via Staudinger ligation. Nat. Protoc. 2, 2930-2944
40. Laughlin, S. T., Baskin, J. M., Amacher, S. L., and Bertozzi, C. R. (2008) In vivo imaging of membrane-associated glycans in developing zebrafish. Science 320, 664-667 (Pubitemid 351928348)
41. Jourdian, G. W., and Roseman, S. (1962) The sialic acids. II. Preparation of N-glycolylhexosamines, N-glycolylhexosamine 6-phosphates, glycolyl coenzyme A, and glycolyl glutathione. J. Biol. Chem. 237, 2442-2446
42. Auwerx, J. (1991) The human leukemia cell line, THP-1. A multifaceted model for the study of monocyte-macrophage differentiation. Experientia 47, 22-31
43. Boehmelt, G., Wakeham, A., Elia, A., Sasaki, T., Plyte, S., Potter, J., Yang, Y., Tsang, E., Ruland, J., Iscove, N. N., Dennis, J. W., and Mak, T. W. (2000) Decreased UDP-GlcNAc levels abrogate proliferation control in EMeg32-deficient cells. EMBO J. 19, 5092-5104
44. Sjoberg, E. R., Manzi, A. E., Khoo, K. H., Dell, A., and Varki, A. (1992) Structural and immunological characterization of O-acetylated GD2. Evidence that GD2 is an acceptor for ganglioside O-acetyltransferase in human melanoma cells. J. Biol. Chem. 267, 16200-16211
45. Menezes, J., Leibold, W., Klein, G., and Clements, G. (1975) Establishment and characterization of an Epstein-Barr virus (EBC)-negative lymphoblastoid B cell line (BJA-B) from an exceptional EBV-genome-negative African Burkitt's lymphoma. Biomedicine 22, 276-284
46. Keppler, O. T., Hinderlich, S., Langner, J., Schwartz-Albiez, R., Reutter, W., and Pawlita, M. (1999) UDP-GlcNAc 2-epimerase. A regulator of cell-surface sialylation. Science 284, 1372-1376 (Pubitemid 29289666)
47. Kingsley, D. M., and Krieger, M. (1984) Receptor-mediated endocytosis of low density lipoprotein. Somatic cell mutants define multiple genes required for expression of surface-receptor activity. Proc. Natl. Acad. Sci. U.S.A. 81, 5454-5458 (Pubitemid 14000505)
48. Esko, J. D. (2001) Special considerations for proteoglycans and glycosaminoglycans and their purification. Curr. Protoc. Mol. Biol. Chapter 17, Unit 17.2
49. Lawrence, R., Olson, S. K., Steele, R. E., Wang, L., Warrior, R., Cummings, R. D., and Esko, J. D. (2008) Evolutionary differences in glycosaminoglycan fine structure detected by quantitative glycan reductive isotope labeling. J. Biol. Chem. 283, 33674-33684
50. Lawrence, R., Lu, H., Rosenberg, R. D., Esko, J. D., and Zhang, L. (2008) Disaccharide structure code for the easy representation of constituent oligosaccharides from glycosaminoglycans. Nat. Methods 5, 291-292 (Pubitemid 351455150)
51. Carlson, D. M. (1968) Structures and immunochemical properties of oligosaccharides isolated from pig submaxillary mucins. J. Biol. Chem. 243, 616-626
52. Plummer, T. H., Jr., and Tarentino, A. L. (1991) Purification of the oligosaccharide-cleaving enzymes of Flavobacterium meningosepticum. Glycobiology 1, 257-263
53. Hayes, B. K., Freeze, H. H., and Varki, A. (1993) Biosynthesis of oligosaccharides in intact Golgi preparations from rat liver. Analysis of N-linked glycans labeled by UDP-[6-3H]N-acetylglucosamine. J. Biol. Chem. 268, 16139-16154 (Pubitemid 23229910)
54. Dell, A., Khoo, K. H., Panico, M., McDowell, R. A., Etienne, A. T., Reason, A. J., and Morris, H. R. (1993) in Glycobiology: A Practical Approach (Fukuda, M., and Kobata, A., eds) pp. 187-222, Oxford University Press, Oxford, UK
55. Jang-Lee, J., North, S. J., Sutton-Smith, M., Goldberg, D., Panico, M., Morris, H., Haslam, S., and Dell, A. (2006) Glycomic profiling of cells and tissues by mass spectrometry. Fingerprinting and sequencing methodologies. Methods Enzymol. 415, 59-86 (Pubitemid 44751091)
56. Ceroni, A., Maass, K., Geyer, H., Geyer, R., Dell, A., and Haslam, S. M. (2008) GlycoWorkbench. A tool for the computer-assisted annotation of mass spectra of glycans. J. Proteome Res. 7, 1650-1659
57. Sarkar, A. K., Fritz, T. A., Taylor, W. H., and Esko, J. D. (1995) Disaccharide uptake and priming in animal cells. Inhibition of sialyl Lewis X by acetylated Galβ1→4GlcNAc β-O-naphthalenemethanol. Proc. Natl. Acad. Sci. U.S.A. 92, 3323-3327
58. Pastuszak, I., Drake, R., and Elbein, A. D. (1996) Kidney N-acetylgalactosamine (GalNAc)-1-phosphate kinase, a new pathway of GalNAc activation. J. Biol. Chem. 271, 20776-20782 (Pubitemid 26281863)
59. Wang-Gillam, A., Pastuszak, I., Stewart, M., Drake, R. R., and Elbein, A. D. (2000) Identification and modification of the uridine-binding site of the UDP-GalNAc (GlcNAc) pyrophosphorylase. J. Biol. Chem. 275, 1433-1438 (Pubitemid 30051203)
60. Głowacka, D., Zwierz, K., Gindzieński, A., and Gałasiśki, W. (1978) The metabolism of UDP-N-acetyl-D-glucosamine in the human gastric mucous membrane. II. The activity of UDP-N- acetylglucosamine 4-epimerase (EC 5.1.3.7.). Biochem. Med. 19, 202-210
61. Hinderlich, S., Stäsche, R., Zeitler, R., and Reutter, W. (1997) A bifunctional enzyme catalyzes the first two steps in N-acetylneuraminic acid biosynthesis of rat liver. Purification and characterization of UDP-N-acetylglucosamine 2-epimerase/N-acetylmannosamine kinase. J. Biol. Chem. 272, 24313-24318
62. Roseman, S., Jourdian, G. W., Watson, D., and Rood, R. (1961) Enzymatic synthesis of sialic acid 9-phosphates. Proc. Natl. Acad. Sci. U.S.A. 47, 958-961
63. Maliekal, P., Vertommen, D., Delpierre, G., and Van Schaftingen, E. (2006) Identification of the sequence encoding N-acetylneuraminate-9-phosphate phosphatase. Glycobiology 16, 165-172 (Pubitemid 43125972)
64. Boyce, M., Carrico, I. S., Ganguli, A. S., Yu, S. H., Hangauer, M. J., Hubbard, S. C., Kohler, J. J., and Bertozzi, C. R. (2011) Metabolic cross-talk allows labeling of O-linked β-N-acetylglucosamine-modified proteins via the N-acetylgalactosamine salvage pathway. Proc. Natl. Acad. Sci. U.S.A. 108, 3141-3146
65. Kingsley, D. M., Kozarsky, K. F., Hobbie, L., and Krieger, M. (1986) Reversible defects in O-linked glycosylation and LDL receptor expression in a UDP-Gal/UDP-GalNAc 4-epimerase-deficient mutant. Cell 44, 749-759 (Pubitemid 16073971)
66. North, S. J., Huang, H. H., Sundaram, S., Jang-Lee, J., Etienne, A. T., Trollope, A., Chalabi, S., Dell, A., Stanley, P., and Haslam, S. M. (2010) Glycomics profiling of Chinese hamster ovary cell glycosylation mutants reveals N-glycans of a novel size and complexity. J. Biol. Chem. 285, 5759-5775
67. Bulai, T., Bratosin, D., Artenie, V., and Montreuil, J. (2002) Characterization of a sialate pyruvate-lyase in the cytosol of human erythrocytes. Biochimie 84, 655-660 (Pubitemid 35282539)
68. Schauer, R., Sommer, U., Krüger, D., van Unen, H., and Traving, C. (1999) The terminal enzymes of sialic acid metabolism: acylneuraminate pyruvate-lyases. Biosci. Rep. 19, 373-383 (Pubitemid 30169338)
69. Varki, A., and Sharon, N. (2009) in Essentials of Glycobiology (Varki, A., Cummings, R. D., Esko, J. D., Freeze, H. H., Stanley, P., Bertozzi, C. R., Hart, G. W., and Etzler, M. E., eds) pp. 1-22, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY