Exposure of α2,6-sialylated lactosaminic chains marks apoptotic and necrotic death in different cell types

Glycobiology

Volumn 19, Issue 2, 2009, Pages 172-181

  Malagolini, Nadia ^a   Chiricolo, Mariella ^a   Marini, Marina ^a   Dall'Olio, Fabio ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Apoptosis; Cell death; Necrosis; Sambucus nigra agglutinin; Sialylation

Indexed keywords

ALPHA2,6 SIALYLATED LACTOSAMINE; CARBOHYDRATE DERIVATIVE; GLUCOSAMINE DERIVATIVE; GLYCOPROTEIN; LECTIN; N ACETYLGLUCOSAMINE; SIALIDASE; SIALYLTRANSFERASE; SUGAR; UNCLASSIFIED DRUG; AMINOSUGAR; BETA D GALACTOSIDE ALPHA 2 6 SIALYLTRANSFERASE; BETA-D-GALACTOSIDE ALPHA 2-6-SIALYLTRANSFERASE; LACTOSAMINE;

ANIMAL CELL; APOPTOSIS; ARTICLE; BINDING SITE; BLADDER CANCER; BREAST CELL; CANCER CELL; CARBOHYDRATE ANALYSIS; CELL DEATH; CONTROLLED STUDY; GLYCOSYLATION; HEAT TREATMENT; HUMAN; HUMAN CELL; INTESTINE CELL; MAACKIA; MOUSE; NEUTROPHIL; NONHUMAN; PANCREAS CELL; PEANUT; PHASEOLUS VULGARIS; POLYPORUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SAMBUCUS NIGRA; ANIMAL; METABOLISM; NECROSIS; TUMOR CELL CULTURE;

ARACHIS HYPOGAEA; BASIDIOMYCOTA; MAACKIA AMURENSIS; MUS; PHASEOLUS VULGARIS; POLYPORUS SQUAMOSUS; SAMBUCUS NIGRA;

AMINO SUGARS; ANIMALS; APOPTOSIS; CELL DEATH; GLYCOSYLATION; HUMANS; LECTINS; MICE; NECROSIS; SAMBUCUS NIGRA; SIALYLTRANSFERASES; TUMOR CELLS, CULTURED;

EID: 58149337104     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwn122     Document Type: Article

References (42)

1. Akamatsu S, Yazawa S, Zenita K, Matsumoto H, Tachikawa T, Kannagi R. 1996. Elevation of an alpha(1,3)fucosyltransferase activity correlated with apoptosis in the human colon adenocarcinoma cell fine, HT-29. Glycoconj J. 13:1021-1029.
2. Akgul C, Moulding DA, Edwards SW. 2001. Molecular control of neutrophil apoptosis. FEBS Lett. 487:318-322.
3. Azuma Y, Kurusu Y, Sato H, Higai K, Matsumoto K. 2007. Increased expression of Lewis X and Y antigens on the cell surface and FUT 4 mRNA during granzyme B-induced Jurkat cell apoptosis. Biol Pharm Bull. 30:655-660.
4. Azuma Y, Taniguchi A, Matsumoto K. 2000. Derease in cell surface sialic acid in etoposide-treated Jurkat cells and the role of cell surface sialidase. Glycoconj J. 17:301-306.
5. Batisse C, Marquet J, Greffard A, Fleury-Feith J, Jaurand MC, Pilatte Y. 2004. Lectin-based three-color flow cytometric approach for studying cell surface glycosylation changes that occur during apoptosis. Cytometry A. 62:81-88.
6. Bleesing JJ, Morrow MR, Uzel G, Fleisher TA. 2001. Human T cell activation induces the expression of a novel CD45 isoform that is analogous to murine B220 and is associated with altered O-glycan synthesis and onset of apoptosis. Cell Immunol. 213:72-81.
7. Brockhausen I, Lehotay M, Yang JM, Qin W, Young D, Lucien J, Coles J, Paulsen H. 2002. Glycoprotein biosynthesis in porcine aortic endothelial cells and changes in the apoptotic cell population. Glycobiology. 12:33-45.
8. Chai F, Truong-Tran AQ, Evdokiou A, Young GP, Zalewski PD. 2000. Intracellular zinc depletion induces caspase activation and p21 Waf1/ Cip1 cleavage in human epithelial cell lines. J Infect Dis. 182(Suppl 1):S85-S92.
9. Chandrasekaran EV, Xue J, Xia J, Locke RD, Matta KL, Neelamegham S. 2008. Reversible sialylation: Synthesis of cytidine 5′-monophospho- N- acetylneuraminic acid from cytidine 5′-monophosphate with alpha2,3-sialyl O-glycan-, glycolipid-, and macromolecule-based donors yields diverse sialylated products. Biochemistry. 47:320-330.
10. Chiricolo M, Malagolini N, Bonfiglioli S, Dall'Olio F. 2006. Phenotypic changes induced by expression of β-galactoside α2,6-sialyltransferase I in the human colon cancer cell line SW948. Glycobiology. 16:146-154.
11. Dall'Olio F, Chiricolo M. 2001. Sialyltransferases in cancer. Glycoconj J. 18:941-850.
12. Dall'Olio F, Malagolini N, Chiricolo M. 2006. β-Galactoside α2,6-sialyltransferase and the sialyl α2,6-galactosyl-linkage in tissues and cell lines. Methods Mol Biol. 347:157-170.
13. Dall'Olio F, Malagolini N, Serafini-Cessi F. 1992. Enhanced CMP-NeuAc:GAl β-1,4G1cNAc-R α 2,6-sialyltransferase activity of human colon cancer xenografts in athymic nude mice and of xenograft-derived cell lines. Int J Cancer. 50:325-330.
14. Duvall E, Wyllie AH, Morris RG. 1985. Macrophage recognition of cells undergoing programmed cell death (apoptosis). Immunology. 56:351-358.
15. Fadok VA, Voelker DR, Campbell PA, Cohen JJ, Bratton DL, Henson PM. 1992. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol. 148:2207-2216.
16. Franz S, Frey B, Sheriff A, Gaipl US, Beer A, Voll RE, Kalden JR, Herrmann M. 2006. Lectins detect changes of the glycosylation status of plasma membrane constituents during late apoptosis. Cytometry A. 69:230-239.
17. Franz S, Herrmann K, Fuhmrohr B, Sheriff A, Frey B, Gaipl US, Voll RE, Kalden JR, Jack HM, Herrmann M. 2007. After shrinkage apoptotic cells expose internal membrane-derived epitopes on their plasma membranes. Cell Death Differ. 14:733-742.
18. Hall SE, Savill JS, Henson PM, Haslett C. 1994. Apoptotic neutrophils are phagocytosed by fibroblasts with participation of the fibroblast vitronectin receptor and involvement of a mannose/fucose-specific lectin. J Immunol. 153:3218-3227.
19. Hammarstrom S, Hammarstrom ML, Sundblad G, Amarp J, Lonngren J. 1982. Mitogenic leukoagglutinin from Phaseolus vulgaris binds to a pentasaccharide unit in N-acetyllactosarrkine-type glycoprotein glycans. Proc Natl Acad Sci USA. 79:1611-1615.
20. Hart SP, Ross JA, Ross K, Haslett C, Dransfield I. 2000. Molecular characterization of the surface of apoptotic neutrophils: Implications for functional downregulation and recognition by phagocytes. Cell Death Differ. 7:493-503.
21. Hennet T, Chui D, Paulson JC, Marth JD. 1998. Immune regulation by the ST6Gal sialyltransferase. Proc Nad Acad Sci USA. 95:4504-4509.
22. Hoebeke J, Foriers A, Schreiber AB, Strosberg AD. 1978. Equilibrium and kinetic studies of the binding of Lens culinaris lectin to rabbit erythrocytes by a quantitative fluorometric method. Biochemistry. 17:5000-5005.
23. Ito K, Miyagawa K, Matsumoto M, Yabuno S, Kawakami N, Hamaguchi T, Iizuka M, Minamiura N. 2006. Evidence for the transglycosylation of complex type oligosaccharides of glycoproteins by endo-beta-N cetylglucosaminidase HS. Arch Biochem Biophys. 454:89-99.
24. Kim SM, Lee JS, Lee YH, Kim WJ, Do SI, Choo YK, Park YI. 2007. Increased alpha2,3-sialylation and hyperglycosylation of N-glycans in embryonic rat cortical neurons during camptothecin-induced apoptosis. Mol Cells. 24:416-423.
25. Knibbs RN, Goldstein IJ, Ratcliffe RM, Shibuya N. 1991. Characterization of the carbohydrate binding specificity of the leukoagglutinating lectin from Maackia amurensis. Comparison with other sialic acid-specific lectins. J Biol Chem. 266:83-88.
26. Krzewinski-Recchi MA, Julien S, Juliant S, Teintenier-Lelievre M, Samyn-Petit B, Montiel MD, Mir AM, Cerutti M, Harduin-Lepers A, Delannoy P. 2003. Identification and functional expression of a second human β-galactoside α2,6-sialylfransferase, ST6Gal II. Eur J Biochem. 270:950-961.
27. Lotan R, Skutelsky E, Danon D, Sharon N. 1975. The purification, composition, and specificity of the anti-T lectin from peanut (Arachis hypogaea). J Biol Chem. 250:8518-8523.
28. Marini M, Frabetti F, Canaider S, Dini L, Falcieri E, Poirier GG. 2001. Modulation of caspase-3 activity by zinc ions and by the cell redox state. Exp Cell Res. 266:323-312.
29. Morris RG, Hargreaves AD, Duvall E, Wyllie All. 1984. Hormone-induced cell death: 2. Surface changes in thymocytes undergoing apoptosis. Am J Pathol. 115:426-436.
30. Nasirikenari M, Segal BH, Ostberg JR, Urbasic A, Lau JT. 2006. Altered granulopoietic profile and exaggerated acute neutrophilic inflammation in mice with targeted deficiency in the sialyltransferase ST6Gal I. Blood. 108:3397-3405.
31. Rapoport E, Le Pendu J. 1999. Glycosylation alterations of cells in late phase apoptosis from colon carcinomas. Glycobiology. 9:1337-1345.
32. Rapoport EM, Sapot'ko YB, Pazynina GV, Bojenko VK, Bovin NV. 2005. Sialoside-binding macrophage lectins in phagocytosis of apoptotic bodies. Biochemistry (Mosc). 70:330-338.
33. Russell L, Waring P, Beaver JP. 1998. Increased cell surface exposure of fucose residues is a late event in apoptosis. Biochem Biophys Res Commun. 250:449-453.
34. Sarter K, Mierke C, Beer A, Frey B, Fuhrurohr BG, Schulze C, Franz S. 2007. Sweet clearance: Involvement of cell surface glycans in the recognition of apoptotic cells. Autoimmunity. 40:345-348.
35. Shibuya N, Goldstein IJ, Broekaert WF, Nsimba-Lubaki M, Peeters B, Peumans WJ. 1987. The elderberry (Sambucus nigra L.) bark lectin recognizes the Neu5Ac(α 2-6)Gal/GalNAc sequence. J Biol Chem. 262:1596-1601.
36. Takashima S, Tsuji S, Tsujimoto M. 2002. Characterization of thesecond type of human β-galactoside ,6-sialyltransferase (ST6Gal II), which sialylates Galβ1,4GlcNAc structures on oligosaccharides preferentially. Genomic analysis of human sialyltransferase genes. J Biol Chem. 277:45719-45728.
37. Toma V, Zuber C, Winter HC, Goldstein IJ, Roth J. 2001. Application of a lectin from the mushroom Polysporus squamosus for the histochemical detection of the NeuAcα2,6Galβ1,4Glc/GlcNAc sequence of N-linked oligosaccharides: A comparison with the Sambucus nigra lectin. Histochem Cell Biol. 116:183-193.
38. Van Damme EJ, Barre A, Rouge P, Van Leuven F, Peumans WJ. 1996. The NeuAcα2,6Gal/GalNAc-binding lectin from elderberry (Sambucus nigra bark, a type-2 ribosome-inactivating protein with an unusual specificity and structure. Eur J Biochem. 235:128-137.
39. Van Lenten L, Ashwell G. 1971. Studies on the chemical and enzymatic modification of glycoproteins. A general method for the tritiation of sialic acid-containing glycoproteins. J Biol Chem. 246:1889-1894.
40. Vandivier RW, Henson PM, Douglas IS. 2006. Burying the dead: The impact of failed apoptotic cell removal (efferocytosis) on chronic inflammatory lung disease. Chest. 129:1673-1682.
41. 2-terminal signal anchor. J Biol Chem. 262:17735-17743.
42. Zhang S, Cai M, Zhang SW, Hu Y, Gu JX. 2003. Involvement of beta 1,4-galactosyltransferase 1 and Gal beta1→4GlcNAc groups in human hepatocarcinoma cell apoptosis. Mol Cell Biochem. 243:81-86.