Systemic blockade of sialylation in mice with a global inhibitor of sialyltransferases

Journal of Biological Chemistry

Volumn 289, Issue 51, 2014, Pages 35149-35158

  Macauley, Matthew S ^a   Arlian, Britni M ^a   Rillahan, Cory D ^a,b   Pang, Poh Choo ^c   Bortell, Nikki ^a   Marcondes, Maria Cecilia G ^a   Haslam, Stuart M ^c   Dell, Anne ^c   Paulson, James C ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY;

GLOBAL INHIBITORS; PHARMACOLOGICAL BLOCKADE; PHARMACOLOGICAL INHIBITION; SIALIC ACIDS; SIALOSIDE; SIALYLATION; SIALYLTRANSFERASE; SIALYLTRANSFERASES;

MAMMALS;

N ACETYLNEURAMINIC ACID DERIVATIVE; SIALIC ACID; SIALOSIDE; SIALYLTRANSFERASE; UNCLASSIFIED DRUG; 2,4,7,8,9-PENTAACETYL-3FAX-NEUCO2M; ENZYME INHIBITOR; GLYCOLIPID; GLYCOPROTEIN; N ACETYLNEURAMINIC ACID; POLYSACCHARIDE; SIALIC ACID DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD; BRAIN; CELL VIABILITY; CONTROLLED STUDY; FAILURE TO THRIVE; GLOMERULUS; HEART; KIDNEY; KIDNEY DYSFUNCTION; LEUKOCYTE; LIVER; LIVER DYSFUNCTION; LUNG; MALE; MOUSE; NONHUMAN; PROTEINURIA; SIALYLATION; SPLEEN; TESTIS; TISSUE DISTRIBUTION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CARDIAC MUSCLE; DOSE RESPONSE; DRUG EFFECTS; FLOW CYTOMETRY; MASS SPECTROMETRY; METABOLISM; TIME FACTOR; WESTERN BLOTTING;

MUS;

ANIMALS; BLOTTING, WESTERN; BRAIN; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; FLOW CYTOMETRY; GLYCOLIPIDS; GLYCOPROTEINS; KIDNEY; LEUKOCYTES; LIVER; LUNG; MALE; MASS SPECTROMETRY; MICE, INBRED C57BL; MYOCARDIUM; N-ACETYLNEURAMINIC ACID; POLYSACCHARIDES; SIALIC ACIDS; SIALYLTRANSFERASES; SPLEEN; TIME FACTORS;

EID: 84919372718     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.606517     Document Type: Article

References (47)

1. Angata, T., and Varki, A. (2002) Chemical diversity in the sialic acids and related α-keto acids: an evolutionary perspective. Chem. Rev. 102, 439-469
2. Varki, A. (2007) Glycan-based interactions involving vertebrate sialic-ac-id-recognizing proteins. Nature 446, 1023-1029
3. Rosen, S. D. (2004) Ligands for L-selectin: homing, inflammation, and beyond. Annu. Rev. Immunol. 22, 129-156
4. Crocker, P. R., Paulson, J. C., and Varki, A. (2007) Siglecs and their roles in the immune system. Nat. Rev. Immunol. 7, 255-266
5. Neu, U., Bauer, J., and Stehle, T. (2011) Viruses and sialic acids: rules of engagement. Curr. Opin. Struct. Biol. 21, 610-618
6. 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., and Dell, A. (2011) Human sperm binding is mediated by the sialyl-Lewis(x) oligosaccharide on the zona pellucida. Science 333, 1761-1764
7. Hildebrandt, H., and Dityatev, A. (2013) Polysialic acid in brain development and synaptic plasticity. Top. Curr. Chem., in press
8. Ednie, A. R., and Bennett, E. S. (2012) Modulation of voltage-gated ion channels by sialylation. Compr. Physiol. 2, 1269-1301
9. Quaggin, S. E. (2007) Sizing up sialic acid in glomerular disease. J. Clin. Invest. 117, 1480-1483
10. Schwarzkopf, M., Knobeloch, K.-P., Rohde, E., Hinderlich, S., Wiechens, N., Lucka, L., Horak, I., Reutter, W., and Horstkorte, R. (2002) Sialylation is essential for early development in mice. Proc. Natl. Acad. Sci. U.S.A. 99, 5267-5270
11. Fuster, M. M., and Esko, J. D. (2005) The sweet and sour of cancer: glycans as novel therapeutic targets. Nat. Rev. Cancer 5, 526-542
12. Paulson, J. C., and Rademacher, C. (2009) Glycan terminator. Nat. Struct. Mol. Biol. 16, 1121-1122
13. Paulson, J. C., Weinstein, J., and Schauer, A. (1989) Tissue-specific expression of sialyltransferases. J. Biol. Chem. 264, 10931-10934
14. Kitagawa, H., and Paulson, J. C. (1994) Differential expression of five sialyltransferase genes in human tissues. J. Biol. Chem. 269, 17872-17878
15. Kono, M., Ohyama, Y., Lee, Y. C., Hamamoto, T., Kojima, N., and Tsuji, S. (1997) Mouse -galactoside -2,3-sialyltransferases: comparison of in vitro substrate specificities and tissue specific expression. Glycobiology 7, 469-479
16. Hennet, T., Chui, D., Paulson, J. C., and Marth, J. D. (1998) Immune regulation by the ST6Gal sialyltransferase. Proc. Natl. Acad. Sci. U.S.A. 95, 4504-4509
17. Frommhold, D., Ludwig, A., Bixel, M. G., Zarbock, A., Babushkina, I., Weissinger, M., Cauwenberghs, S., Ellies, L. G., Marth, J. D., Beck-Sickinger, A. G., Sixt, M., Lange-Sperandio, B., Zernecke, A., Brandt, E., Weber, C., Vestweber, D., Ley, K., and Sperandio, M. (2008) Sialyltransferase ST3Gal-IV controls CXCR2-mediated firm leukocyte arrest during inflammation. J. Exp. Med. 205, 1435-1446
18. Priatel, J. J., Chui, D., Hiraoka, N., Simmons, C. J., Richardson, K. B., Page, D. M., Fukuda, M., Varki, N. M., and Marth, J. D. (2000) The ST3Gal-I sialyltransferase controls CD8- T lymphocyte homeostasis by modulating O-glycan biosynthesis. Immunity 12, 273-283
19. Orr, S. L., Le, D., Long, J. M., Sobieszczuk, P., Ma, B., Tian, H., Fang, X., Paulson, J. C., Marth, J. D., and Varki, N. (2013) A phenotype survey of 36 mutant mouse strains with gene-targeted defects in glycosyltransferases or glycan-binding proteins. Glycobiology 23, 363-380
20. Yang, W. H., Nussbaum, C., Grewal, P. K., Marth, J. D., and Sperandio, M. (2012) Coordinated roles of ST3Gal-VI and ST3Gal-IV sialyltransferases in the synthesis of selectin ligands. Blood 120, 1015-1026
21. Ellies, L. G., Sperandio, M., Underhill, G. H., Yousif, J., Smith, M., Priatel, J. J., Kansas, G. S., Ley, K., and Marth, J. D. (2002) Sialyltransferase specificity in selectin ligand formation. Blood 100, 3618-3625
22. Nagafuku, M., Okuyama, K., Onimaru, Y., Suzuki, A., Odagiri, Y., Yamashita, T., Iwasaki, K., Fujiwara, M., Takayanagi, M., Ohno, I., and Inokuchi, J. (2012) CD4 and CD8 T cells require different membrane gangliosides for activation. Proc. Natl. Acad. Sci. U.S.A. 109, E336-E342
23. Eckhardt, M., Bukalo, O., Chazal, G., Wang, L., Goridis, C., Schachner, M., Gerardy-Schahn, R., Cremer, H., and Dityatev, A. (2000) Mice deficient in the polysialyltransferase ST8SiaIV/PST-1 allow discrimination of the roles of neural cell adhesion molecule protein and polysialic acid in neural development and synaptic plasticity. J. Neurosci. 20, 5234-5244
24. Angata, K., Long, J. M., Bukalo, O., Lee, W., Dityatev, A., Wynshaw-Boris, A., Schachner, M., Fukuda, M., and Marth, J. D. (2004) Sialyltransferase ST8Sia-II assembles a subset of polysialic acid that directs hippocampal axonal targeting and promotes fear behavior. J. Biol. Chem. 279, 32603-32613
25. Krocher, T., Malinovskaja, K., Jurgenson, M., Aonurm-Helm, A., Zharkovskaya, T., Kalda, A., Rockle, I., Schiff, M., Weinhold, B., Gerardy-Schahn, R., Hildebrandt, H., and Zharkovsky, A. (2013) Schizophrenia-like phenotype of polysialyltransferase ST8SIA2-deficient mice. Brain Struct. Funct., in press
26. Yoshikawa, M., Go, S., Takasaki, K., Kakazu, Y., Ohashi, M., Nagafuku, M., Kabayama, K., Sekimoto, J., Suzuki, S., Takaiwa, K., Kimitsuki, T., Matsumoto, N., Komune, S., Kamei, D., Saito, M., Fujiwara, M., Iwasaki, K., and Inokuchi, J. (2009) Mice lacking ganglioside GM3 synthase exhibit complete hearing loss due to selective degeneration of the organ of Corti. Proc. Natl. Acad. Sci. U.S.A. 106, 9483-9488
27. Okada, M., Itoh Mi, M., Haraguchi, M., Okajima, T., Inoue, M., Oishi, H., Matsuda, Y., Iwamoto, T., Kawano, T., Fukumoto, S., Miyazaki, H., Furukawa, K., and Aizawa, S. (2002) B-series Ganglioside deficiency exhibits no definite changes in the neurogenesis and the sensitivity to Fas-mediated apoptosis but impairs regeneration of the lesioned hypoglossal nerve. J. Biol. Chem. 277, 1633-1636
28. Ellies, L. G., Ditto, D., Levy, G. G., Wahrenbrock, M., Ginsburg, D., Varki, A., Le, D. T., and Marth, J. D. (2002) Sialyltransferase ST3Gal-IV operates as a dominant modifier of hemostasis by concealing asialoglycoprotein receptor ligands. Proc. Natl. Acad. Sci. U.S.A. 99, 10042-10047
29. Rillahan, C. D., Antonopoulos, A., Lefort, C. T., Sonon, R., Azadi, P., Ley, K., Dell, A., Haslam, S. M., and Paulson, J. C. (2012) Global metabolic inhibitors of sialyl- and fucosyltransferases remodel the glycome. Nat. Chem. Biol. 8, 661-668
30. Burkart, M. D., Vincent, S. P., Düffels, A., Murray, B. W., Ley, S. V., and Wong, C. H. (2000) Chemo-enzymatic synthesis of fluorinated sugar nucleotide: useful mechanistic probes for glycosyltransferases. Bioorg. Med. Chem. 8, 1937-1946
31. Lairson, L. L., Henrissat, B., Davies, G. J., and Withers, S. G. (2008) Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 77, 521-555
32. Galeano, B., Klootwijk, R., Manoli, I., Sun, M., Ciccone, C., Darvish, D., Starost, M. F., Zerfas, P. M., Hoffmann, V. J., Hoogstraten-Miller, S., Krasnewich, D. M., Gahl, W. A., and Huizing, M. (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
33. Ito, M., Sugihara, K., Asaka, T., Toyama, T., Yoshihara, T., Furuichi, K., Wada, T., and Asano, M. (2012) Glycoprotein hyposialylation gives rise to a nephrotic-like syndrome that is prevented by sialic acid administration in GNE V572L point-mutant mice. PLoS One 7, e29873
34. Weinhold, B., Sellmeier, M., Schaper, W., Blume, L., Philippens, B., Kats, E., Bernard, U., Galuska, S. P., Geyer, H., Geyer, R., Worthmann, K., Schiffer, M., Groos, S., Gerardy-Schahn, R., and Münster-Kühnel, A. K. (2012) Deficits in sialylation impair podocyte maturation. J. Am. Soc. Nephrol. 23, 1319-1328
35. Burkart, M., Zhang, Z., Hung, S., and Wong, C. (1997) A new method for the synthesis of fluoro-carbohydrates and glycosides using selectfluor. J. Am. Chem. Soc. 119, 11743-11746
36. Nicholls, J. M., Moss, R. B., and Haslam, S. M. (2013) The use of sialidase therapy for respiratory viral infections. Antivir. Res. 98, 401-409
37. North, S. J., Jang-Lee, J., Harrison, R., Canis, K., Ismail, M. N., Trollope, A., Antonopoulos, A., Pang, P. C., Grassi, P., Al-Chalabi, S., Etienne, A. T., Dell, A., and Haslam, S. M. (2010) Mass spectrometric analysis of mutant mice. Methods Enzymol. 478, 27-77
38. 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
39. Comelli, E. M., Head, S. R., Gilmartin, T., Whisenant, T., Haslam, S. M., North, S. J., Wong, N. K., Kudo, T., Narimatsu, H., Esko, J. D., Drickamer, K., Dell, A., and Paulson, J. C. (2006) A focused microarray approach to functional glycomics: transcriptional regulation of the glycome. Glycobiology 16, 117-131
40. Takamatsu, S., Antonopoulos, A., Ohtsubo, K., Ditto, D., Chiba, Y., Le, D. T., Morris, H. R., Haslam, S. M., Dell, A., Marth, J. D., and Taniguchi, N. (2010) Physiological and glycomic characterization of N-acetylglucosami-nyltransferase-IVa and -IVb double deficient mice. Glycobiology 20, 485-497
41. Orth, S. R., and Ritz, E. (1998) The nephrotic syndrome. N. Engl. J. Med. 338, 1202-1211
42. Gelberg, H., Healy, L., Whiteley, H., Miller, L. A., and Vimr, E. (1996) In vivo enzymatic removal of -236-linked sialic acid from the glomerular filtration barrier results in podocyte charge alteration and glomerular injury. Lab. Invest. 74, 907-920
43. Büll, C., Boltje, T. J., Wassink, M., de Graaf, A. M., van Delft, F. L., den Brok, M. H., and Adema, G. J. (2013) Targeting aberrant sialylation in cancer cells using a fluorinated sialic acid analog impairs adhesion, migration, and in vivo tumor growth. Mol. Cancer Ther. 12, 1935-1946
44. Gloster, T. M., Zandberg, W. F., Heinonen, J. E., Shen, D. L., Deng, L., and Vocadlo, D. J. (2011) Hijacking a biosynthetic pathway yields a glycosyltransferase inhibitor within cells. Nat. Chem. Biol. 7, 174-181
45. Zandberg, W. F., Kumarasamy, J., Pinto, B. M., and Vocadlo, D. J. (2012) Metabolic inhibition of sialyl-Lewis X biosynthesis by 5-thiofucose remodels the cell surface and impairs selectin-mediated cell adhesion. J. Biol. Chem. 287, 40021-40030
46. Barthel, S. R., Antonopoulos, A., Cedeno-Laurent, F., Schaffer, L., Hernandez, G., Patil, S. A., North, S. J., Dell, A., Matta, K. L., Neelamegham, S., Haslam, S. M., and Dimitroff, C. J. (2011) Peracetylated 4-fluoro-glucosamine reduces the content and repertoire of N- and O-glycans without direct incorporation. J. Biol. Chem. 286, 21717-21731
47. Okeley, N. M., Alley, S. C., Anderson, M. E., Boursalian, T. E., Burke, P. J., Emmerton, K. M., Jeffrey, S. C., Klussman, K., Law, C. L., Sussman, D., Toki, B. E., Westendorf, L., Zeng, W., Zhang, X., Benjamin, D. R., and Senter, P. D. (2013) Development of orally active inhibitors of protein and cellular fucosylation. Proc. Natl. Acad. Sci. U.S.A. 110, 5404-5409