Apoptotic cells selectively uptake minor glycoforms of vitronectin from serum

Apoptosis

Volumn 18, Issue 4, 2013, Pages 373-384

  Malagolini, Nadia ^a   Catera, Mariangela ^a   Osorio, Hugo ^b,c   Reis, Celso A ^b,c   Chiricolo, Mariella ^a   Dall'Olio, Fabio ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b UNIVERSITY OF PORTO   (Portugal)

^c University of Porto   (Portugal)

Author keywords

Apoptosis; Glycosylation; Mortalin; Sialylation; Tubulin; Vitronectin

Indexed keywords

BETA TUBULIN; LIPOCORTIN 5; PROCASPASE 3; PROPIDIUM IODIDE; SIALIC ACID; SIALOGLYCOPROTEIN; TRANSFERRIN; VITRONECTIN;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ELECTROPHORETIC MOBILITY; ENZYME ACTIVITY; GLYCOSYLATION; HUMAN; HUMAN CELL; ISOELECTRIC FOCUSING; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROCESSING; SAMBUCUS NIGRA; SIALYLATION;

ANIMALS; APOPTOSIS; BIOLOGICAL TRANSPORT; CATTLE; CELL LINE, TUMOR; CELL MEMBRANE; HSP70 HEAT-SHOCK PROTEINS; HUMANS; N-ACETYLNEURAMINIC ACID; NEOPLASMS; PLANT LECTINS; PROTEIN ISOFORMS; RIBOSOME INACTIVATING PROTEINS; SERUM; TUBULIN; VITRONECTIN;

BOVINAE; EUKARYOTA; SAMBUCUS NIGRA;

EID: 84876054126     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-013-0812-z     Document Type: Article

References (56)

1. Erwig LP, Henson PM (2008) Clearance of apoptotic cells by phagocytes. Cell Death Differ 15:243-250
2. Ravichandran KS, Lorenz U (2007) Engulfment of apoptotic cells: signals for a good meal. Nat Rev Immunol 7:964-974
3. 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
4. Kinchen JM, Ravichandran KS (2007) Journey to the grave: signaling events regulating removal of apoptotic cells. J Cell Sci 120:2143-2149
5. 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
6. Bilyy R, Kit Y, Hellman U, Tryndyak V, Kaminskyy V, Stoika R (2005) In vivo expression and characteristics of novel alpha-d-mannose-rich glycoprotein markers of apoptotic cells. Cell Biol Int 29:920-928
7. Bilyy R, Stoika R (2007) Search for novel cell surface markers of apoptotic cells. Autoimmunity 40:249-253
8. Franz S, Herrmann K, Fuhrnrohr 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
9. 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
10. 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
11. 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
12. 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
13. Rapoport E, Le Pendu J (1999) Glycosylation alterations of cells in late phase apoptosis from colon carcinomas. Glycobiology 9:1337-1345
14. 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
15. Sarter K, Mierke C, Beer A, Frey B, Fuhrnrohr BG, Schulze C, Franz S (2007) Sweet clearance: involvement of cell surface glycans in the recognition of apoptotic cells. Autoimmunity 40:345-348
16. Malagolini N, Chiricolo M, Marini M, Dall'Olio F (2009) Exposure of α2,6-sialylated lactosaminic chains marks apoptotic and necrotic death in different cell types. Glycobiology 19:172-181
17. 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
18. Weinstein J, de Souza-e-Silva U, Paulson JC (1982) Purification of a Gal β 1,4GlcNAc α 2,6 sialyltransferase and a Gal β 1,3(4)GlcNAc α 2,3 sialyltransferase to homogeneity from rat liver. J Biol Chem 257:13835-13844
19. 2- terminal signal anchor. J Biol Chem 262:17735-17743
20. Dall'Olio F (2000) The sialyl-α2,6-lactosaminyl-structure: biosynthesis and functional role. Glycoconj J 17:669-676
21. Deutsch HF (1954) Fetuin: the mucoprotein of fetal calf serum. J Biol Chem 208:669-678
22. Barnes DW, Silnutzer J (1983) Isolation of human serum spreading factor. J Biol Chem 258:12548-12552
23. Spik G, Bayard B, Fournet B, Strecker G, Bouquelet S, Montreuil J (1975) Studies on glycoconjugates. LXIV. Complete structure of two carbohydrate units of human serotransferrin. FEBS Lett 50:296-299
24. 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
25. Dall'Olio F, Chiricolo M, Lollini P, Lau JT (1995) Human colon cancer cell lines permanently expressing α2,6-sialylated sugar chains by transfection with rat β-galactoside α 2,6 sialyltransferase cDNA. Biochem Biophys Res Commun 211:554-561
26. Preissner KT, Reuning U (2011) Vitronectin in vascular context: facets of a multitalented matricellular protein. Semin Thromb Hemost 37:408-424
27. Kitagaki-Ogawa H, Yatohgo T, Izumi M, Hayashi M, Kashiwagi H, Matsumoto I, Seno N (1990) Diversities in animal vitronectins. Differences in molecular weight, immunoreactivity and carbohydrate chains. Biochim Biophys Acta 1033:49-56
28. Nakashima N, Miyazaki K, Ishikawa M, Yatohgo T, Ogawa H, Uchibori H, Matsumoto I, Seno N, Hayashi M (1992) Vitronectin diversity in evolution but uniformity in ligand binding and size of the core polypeptide. Biochim Biophys Acta 1120:1-10
29. Stepanek O, Brdicka T, Angelisova P, Horvath O, Spicka J, Stockbauer P, Man P, Horejsi V (2011) Interaction of late apoptotic and necrotic cells with vitronectin. PLoS ONE 6:e19243
30. Ogawa H, Yoneda A, Seno N, Hayashi M, Ishizuka I, Hase S, Matsumoto I (1995) Structures of the N-linked oligosaccharides on human plasma vitronectin. Eur J Biochem 230:994-1000
31. Stockmann A, Hess S, Declerck P, Timpl R, Preissner KT (1993) Multimeric vitronectin. Identification and characterization of conformation-dependent self-association of the adhesive protein. J Biol Chem 268:22874-22882
32. Sano K, Asanuma-Date K, Arisaka F, Hattori S, Ogawa H (2007) Changes in glycosylation of vitronectin modulate multimerization and collagen binding during liver regeneration. Glycobiology 17:784-794
33. Seales EC, Jurado GA, Brunson BA, Wakefield JK, Frost AR, Bellis SL (2005) Hypersialylation of β1 integrins, observed in colon adenocarcinoma, may contribute to cancer progression by up-regulating cell motility. Cancer Res 65:4645-4652
34. Semel AC, Seales EC, Singhal A, Eklund EA, Colley KJ, Bellis SL (2002) Hyposialylation of integrins stimulates the activity of myeloid fibronectin receptors. J Biol Chem 277:32830-32836
35. Sanchez-Ruderisch H, Detjen KM, Welzel M, Andre S, Fischer C, Gabius HJ, Rosewicz S (2011) Galectin-1 sensitizes carcinoma cells to anoikis via the fibronectin receptor α5β1-integrin. Cell Death Differ 18:806-816
36. Savill J, Dransfield I, Hogg N, Haslett C (1990) Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 343:170-173
37. Fadok VA, Savill JS, Haslett C, Bratton DL, Doherty DE, Campbell PA, Henson PM (1992) Different populations of macrophages use either the vitronectin receptor or the phosphatidylserine receptor to recognize and remove apoptotic cells. J Immunol 149:4029-4035
38. Fadok VA, Warner ML, Bratton DL, Henson PM (1998) CD36 is required for phagocytosis of apoptotic cells by human macrophages that use either a phosphatidylserine receptor or the vitronectin receptor (αvβ3). J Immunol 161:6250-6257
39. Meesmann HM, Fehr EM, Kierschke S, Herrmann M, Bilyy R, Heyder P, Blank N, Krienke S, Lorenz HM, Schiller M (2010) Decrease of sialic acid residues as an eat-me signal on the surface of apoptotic lymphocytes. J Cell Sci 123:3347-3356
40. Bilyy RO, Shkandina T, Tomin A, Munoz LE, Franz S, Antonyuk V, Kit YY, Zirngibl M, Furnrohr BG, Janko C, Lauber K, Schiller M, Schett G, Stoika RS, Herrmann M (2012) Macrophages discriminate glycosylation patterns of apoptotic cell-derived microparticles. J Biol Chem 287:496-503
41. Bae HB, Zmijewski JW, Deshane JS, Zhi D, Thompson LC, Peterson CB, Chaplin DD, Abraham E (2012) Vitronectin inhibits neutrophil apoptosis through activation of integrin-associated signaling pathways. Am J Respir Cell Mol Biol 46:790-796
42. Seiffert D (1997) Constitutive and regulated expression of vitronectin. Histol Histopathol 12:787-797
43. Deocaris CC, Kaul SC, Wadhwa R (2009) The versatile stress protein mortalin as a chaperone therapeutic agent. Protein Pept Lett 16:517-529
44. Garrido C, Solary E (2003) A role of HSPs in apoptosis through "protein triage"? Cell Death Differ 10:619-620
45. Creagh EM, Carmody RJ, Cotter TG (2000) Heat shock protein 70 inhibits caspase-dependent and -independent apoptosis in Jurkat T cells. Exp Cell Res 257:58-66
46. Beere HM (2004) "The stress of dying": the role of heat shock proteins in the regulation of apoptosis. J Cell Sci 117:2641-2651
47. Bhattacharyya T, Karnezis AN, Murphy SP, Hoang T, Freeman BC, Phillips B, Morimoto RI (1995) Cloning and subcellular localization of human mitochondrial hsp70. J Biol Chem 270:1705-1710
48. Gasnier F, Ardail D, Lerme F, Simonot C, Vaganay E, Louisot P, Gateau-Roesch O (1994) Further characterization of mitochondrial outer membrane: evidence for the presence of two endogenous sialylated glycoproteins. J Biochem (Tokyo) 116:643-648
49. Avidan A, Perlmutter M, Tal S, Oraki O, Kapp T, Krelin Y, Elkabets M, Dotan S, Apte RN, Lichtenstein RG (2009) Differences in the sialylation patterns of membrane stress proteins in chemical carcinogen-induced tumors developed in BALB/c and IL-1alpha deficient mice. Glycoconj J 26:1181-1195
50. Carre M, Andre N, Carles G, Borghi H, Brichese L, Briand C, Braguer D (2002) Tubulin is an inherent component of mitochondrial membranes that interacts with the voltage-dependent anion channel. J Biol Chem 277:33664-33669
51. Ireland CM, Pittman SM (1995) Tubulin alterations in taxol-induced apoptosis parallel those observed with other drugs. Biochem Pharmacol 49:1491-1499
52. Hino M, Kijima-Suda I, Nagai Y, Hosoya H (2003) Glycosylation of the α- and b-tubulin by sialyloligosaccharides. Zool Sci 20:709-715
53. Cassatella MA, Cappelli R, Della BV, Grzeskowiak M, Dusi S, Berton G (1988) Interferon-gamma activates human neutrophil oxygen metabolism and exocytosis. Immunology 63:499-506
54. 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
55. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275
56. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685