Galectin-5 is bound onto the surface of rat reticulocyte exosomes and modulates vesicle uptake by macrophages

Blood

Volumn 115, Issue 3, 2010, Pages 696-705

  Barrès, Céline ^a   Blanc, Lionel ^a   Bette Bobillo, Pascale ^a   André, Sabine ^b   Mamoun, Robert ^a   Gabius, Hans Joachim ^b   Vidal, Michel ^a  

^a UNIVERSITÉ DE MONTPELLIER   (France)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIN; GALACTOSE; GALECTIN; GALECTIN 5; GLYCOCONJUGATE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; UNCLASSIFIED DRUG; MEMBRANE ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL COMPARTMENTALIZATION; CELL FRACTIONATION; CELL MATURATION; CELL SURFACE; CYTOSOL; ENDOSOME; ERYTHROCYTE; EXOSOME; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE MICROSCOPY; MACROPHAGE; MEMBRANE VESICLE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; RAT; RETICULOCYTE; TEMPERATURE; WESTERN BLOTTING; ANIMAL; METABOLISM; PHYSIOLOGY; PROTEIN BINDING; PROTEIN TRANSPORT; SECRETORY PATHWAY; SPRAGUE DAWLEY RAT; TRANSPORT AT THE CELLULAR LEVEL; TRANSPORT VESICLE;

ANIMALS; ANTIGENS, SURFACE; BIOLOGICAL TRANSPORT; EXOSOMES; GALECTINS; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 2; MACROPHAGES; PROTEIN BINDING; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RETICULOCYTES; SECRETORY PATHWAY; TRANSPORT VESICLES;

EID: 77449102731     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-07-231449     Document Type: Article

References (53)

1. Pan BT, Teng K, Wu C, Adam M, Johnstone RM. Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J Cell Biol. 1985;101(3):942-948.
2. Blanc L, De Gassart A, Geminard C, Bette-Bobillo P, Vidal M. Exosome release by reticulocytes-an integral part of the red blood cell differentiation system. Blood Cells Mol Dis. 2005;35(1):21-26. (Pubitemid 40922771)
3. de Gassart A, Géminard C, Février B, Raposo G, Vidal M. Lipid raft-associated proteins sorting in exosomes. Blood. 2003;102(13):4336- 4344. (Pubitemid 37494093)
4. Vidal M, Mangeat P, Hoekstra D. Aggregation reroutes molecules from a recycling to a vesicle-mediated secretion pathway during reticulocyte maturation. J Cell Sci. 1997;110(16):1867-1877. (Pubitemid 27384788)
5. Géminard C, de Gassart A, Blanc L, Vidal M. Degradation of AP2 during reticulocyte maturation enhances binding of hsc70 and Alix to a common site on TfR for sorting into exosomes. Traffic. 2004;5(3):181-195. (Pubitemid 38379937)
6. Lee JC, Gimm JA, Lo AJ, et al. Mechanism of protein sorting during erythroblast enucleation: role of cytoskeletal connectivity. Blood. 2004; 103(5):1912-1919.
7. Soni S, Bala S, Gwynn B, Sahr KE, Peters LL, Hanspal M. Absence of erythroblast macrophage protein (Emp) leads to failure of erythroblast nuclear extrusion. J Biol Chem. 2006;281(29): 20181-20189. (Pubitemid 44065792)
8. Eshghi S, Vogelezang MG, Hynes RO, Griffith LG, Lodish HF. α4β1 integrin and erythropoietin mediate temporally distinct steps in erythropoiesis: integrins in red cell development. J Cell Biol. 2007;177(5):871-880. (Pubitemid 46873092)
9. Chasis JA, Mohandas N. Erythroblastic islands: niches for erythropoiesis. Blood. 2008;112(3): 470-478.
10. Rieu S, Géminard C, Rabesandratana H, Sainte-Marie J, Vidal M. Exosomes released during reticulocyte maturation bind to fibronectin via integrin α4β1. Eur J Biochem. 2000;267(2):583-590. (Pubitemid 30072918)
11. Johnstone RM. Maturation of reticulocytes: formation of exosomes as a mechanism for shedding membrane proteins. Biochem Cell Biol. 1992;70(3-4):179-190.
12. Gabius HJ. Probing the cons and pros of lectin-induced immunomodulation: case studies for the mistletoe lectin and galectin-1. Biochimie. 2001; 83(7):659-666.
13. Gabius HJE. The sugar code. In: Gabius HJE, ed. Fundamentals of Glycosciences. Weinheim, Germany: Wiley-VCH; 2009:1-159.
14. Skutelsky E, Farquhar MG. Variations in distribution of con A receptor sites and anionic groups during red blood cell differentiation in the rat. J Cell Biol. 1976;71(1):218-231.
15. Skutelsky E, Bayer EA. Cell-type-related segregation of surface galactosyl-containing components at an early developmental stage in hemopoietic bone marrow cells in the rabbit. J Cell Biol. 1983;96(1):184-190.
16. Gabius HJ. Cell surface ligands: the why and how of their functionnality as biochemical signals in lectin-mediated information transfer. Crit Rev Immunol. 2006;26(1):43-79.
17. AndréS, Sanchez-Ruderisch H, Nakagawa H, et al. Tumor suppressor p16INK4a-modulator of glycomic profile and galectin-1 expression to increase susceptibility to carbohydrate-dependent induction of anoikis in pancreatic carcinoma cells. FEBS J. 2007;274(13):3233-3256. (Pubitemid 47028461)
18. Harrison FL, Chesterton CJ. Erythroid developmental agglutinin is a protein lectin mediating specific cell-cell adhesion between differentiating rabbit erythroblasts. Nature. 1980;286(5772): 502-504.
19. Harrison FL, Catt JW. Intra- and extracellular distribution of an endogenous lectin during erythropoiesis. J Cell Sci. 1986;84:201-212.
20. Gitt MA, Wiser MF, Leffler H, et al. Sequence and mapping of galectin-5, a beta-galactoside-binding lectin, found in rat erythrocytes. J Biol Chem. 1995;270(10):5032-5038.
21. AndréS, Kojima S, Prahl I, Lensch M, Unverzagt C, Gabius HJ. Introduction of extended LEC14- type branching into core-fucosylated biantennary N-glycan. FEBS J. 2005;272(8):1986-1998.
22. Dam TK, Gabius HJ, Andre S, Kaltner H, Lensch M, Brewer CF. Galectins bind to the multivalent glycoprotein asialofetuin with enhanced affinities and a gradient of decreasing binding constants. Biochemistry. 2005;44(37):12564- 12571. (Pubitemid 41324347)
23. Wu AM, Singh T, Wu JH, Lensch M, AndréS, Gabius HJ. Interaction profile of galectin-5 with free saccharides and mammalian glycoproteins: probing its fine specificity and the effect of naturally clustered ligand presentation. Glycobiology. 2006;16(6):524-537. (Pubitemid 43779048)
24. Beer A, Andre S, Kaltner H, et al. Human galectins as sensors for apoptosis/necrosis-associated surface changes of granulocytes and lymphocytes. Cytometry A. 2008;73(2):139-147.
25. Nickel W. Unconventional secretion: an extracellular trap for export of fibroblast growth factor 2. J Cell Sci. 2007;120(Pt 14):2295-2299. (Pubitemid 47232202)
26. Théry C, Boussac M, Veron P, et al. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol. 2001;166(12): 7309-7318. (Pubitemid 32525606)
27. Keryer-Bibens C, Pioche-Durieu C, Villemant C, et al. Exosomes released by EBV-infected nasopharyngeal carcinoma cells convey the viral latent membrane protein 1 and the immunomodulatory protein galectin 9. BMC Cancer. 2006;6:283. (Pubitemid 46218055)
28. Lensch M, Lohr M, Russwurm R, et al. Unique sequence and expression profiles of rat galectins-5 and -9 as a result of species-specific gene divergence. Int J Biochem Cell Biol. 2006;38(10): 1741-1758. (Pubitemid 43947656)
29. AndréS, Kaltner H, Lensch M, et al. Determination of structural and functional overlap/divergence of five proto-type galectins by analysis of the growth-regulatory interaction with ganglioside GM1 in silico and in vitro on human neuroblastoma cells. Int J Cancer. 2005;114(1):46-57. (Pubitemid 40194308)
30. Houzelstein D, Goncalves IR, Fadden AJ, et al. Phylogenetic analysis of the vertebrate galectin family. Mol Biol Evol. 2004;21(7):1177-1187. (Pubitemid 38823721)
31. Sarafian V, Jadot M, Foidart JM, et al. Expression of Lamp-1 and Lamp-2 and their interactions with galectin-3 in human tumor cells. Int J Cancer. 1998;75(1):105-111. (Pubitemid 28113984)
32. Fornstedt N, Porath J. Characterization studies on a new lectin found in seeds of Vicia ervilia. FEBS Lett. 1975;57(2):187-191.
33. Vidal MJ, Stahl PD. The small GTP-binding proteins Rab4 and ARF are associated with vesicles released during reticulocyte maturation. Eur J Cell Biol. 1993;60(2):261-267.
34. Harrison FL, Beswick TM, Chesterton CJ. Separation of haemopoietic cells for biochemical investigation. Preparation of erythroid and myeloid cells from human and laboratory-animal bone marrow and the separation of erythroblasts according to their state of maturation. Biochem J. 1981;194(3):789-796.
35. Cans C, Passer BJ, Shalak V, et al. Translationally controlled tumor protein acts as a guanine nucleotide dissociation inhibitor on the translation elongation factor eEF1A. Proc Natl Acad Sci U S A. 2003;100(24):13892-13897. (Pubitemid 37499162)
36. Lohr M, Lensch M, AndréS, et al. Murine homodimeric adhesion/growth-regulatory galectins-1, -2 and -7: comparative profiling of gene/ promoter sequences by database mining, of expression by RT-PCR/immunohistochemistry and of contact sites for carbohydrate ligands by computational chemistry. Folia Biol (Praha). 2007; 53(4):109-128. (Pubitemid 47054479)
37. Blanc L, Barres C, Bette-Bobillo P, Vidal M. Reticulocyte-secreted exosomes bind natural IgM antibodies: involvement of a ROS-activatable endosomal phospholipase iPLA2. Blood. 2007; 110(9):3407-3416. (Pubitemid 350110308)
38. Steck TL, Kant JA. Preparation of impermeable ghosts and inside-out vesicles from erythrocyte membranes. Methods Enzymol. 1974;31(Pt A): 172-181.
39. Vidal M, Hoekstra D. In vitro fusion of reticulocyte endocytic vesicles with liposomes. J Biol Chem. 1995;270(30):17823-17829.
40. Dardalhon V, Géminard C, Reggio H, Vidal M, Sainte-Marie J. Fractionation analysis of the endosomal compartment during rat reticulocyte maturation. Cell Biol Int. 2002;26(8):669-678.
41. Parolini I, Sargiacomo M, Lisanti MP, Peschle C. Signal transduction and glycophosphatidylinositol-linked proteins (LYN, LCK, CD4, CD45, G proteins and CD55) selectively localize in triton-insoluble plasma membrane domains of human leukemic cell lines and normal granulocytes. Blood. 1996;87(9):3783-3794. (Pubitemid 26129606)
42. Hsu DK, Liu FT. Regulation of cellular homeostasis by galectins. Glycoconj J. 2004;19(7-9):507-515.
43. Stein BS, Bensch KG, Sussman HH. Complete inhibition of transferrin recycling by monensin in K562 cells. J Biol Chem. 1984;259(23):14762-14772.
44. De Gassart A, Trentin B, Martin M, et al. Exosomal sorting of the cytoplasmic domain of bovine leukemia virus TM Env protein. Cell Biol Int. 2009;33(1):36-48.
45. Savina A, Furlan M, Vidal M, Colombo MI. Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J Biol Chem. 2003;278(22):20083- 20090. (Pubitemid 36799202)
46. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, Kirchhausen T. Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell. 2006;10(6):839-850.
47. Klibi J, Niki T, Riedel A, et al. Blood diffusion and Th1-suppressive effects of galectin-9-containing exosomes released by Epstein-Barr virus-infected nasopharyngeal carcinoma cells. Blood. 2009;113(9):1957-1966.
48. Kopitz J, AndréS, von Reitzenstein C, et al. Homodimeric galectin-7 (p53-induced gene 1) is a negative growth regulator for human neuroblastoma cells. Oncogene. 2003;22(40):6277-6288. (Pubitemid 37281657)
49. Wang J, Lu ZH, Gabius HJ, Rohowsky-Kochan C, Ledeen RW, Wu G. Cross-linking of GM1 ganglioside by galectin-1 mediates regulatory T-cell activity involving TRPC5 channel activation: possible role in suppressing experimental autoimmune encephalomyelitis. J Immunol. 2009;182(7):4036-4045.
50. Amzallag N, Passer BJ, Allanic D, et al. TSAP6 facilitates the secretion of translationally controlled tumor protein/histamine-releasing factor via a nonclassical pathway. J Biol Chem. 2004; 279(44):46104-46112. (Pubitemid 39491604)
51. Morelle W, Stechly L, Andre S, et al. Glycosylation pattern of brush border-associated glycoproteins in enterocyte-like cells: involvement of complex-type N-glycans in apical trafficking. Biol Chem. 2009;390(7):529-544.
52. Stechly L, Morelle W, Dessein AF, et al. Galectin-4-regulated delivery of glycoproteins to the brush border membrane of enterocyte-like cells. Traffic. 2009;10(4):438-450.
53. van Vliet SJ, Saeland E, van Kooyk Y. Sweet preferences of MGL: carbohydrate specificity and function. Trends Immunol. 2008;29(2): 83-90.