Galectins and microenvironmental niches during hematopoiesis

Current Opinion in Hematology

Volumn 18, Issue 6, 2011, Pages 443-451

  Rabinovich, Gabriel A ^a   Vidal, Michel ^b  

^a INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

^b UNIVERSITÉ DE MONTPELLIER   (France)

Author keywords

galectins; hematopoiesis; microenvironmental niches

Indexed keywords

ECALECTIN; GALECTIN; GALECTIN 1; GALECTIN 10; GALECTIN 3; GALECTIN 4; GALECTIN 5; GLYCOCONJUGATE; GLYCOPROTEIN; GLYCOSPHINGOLIPID; UNCLASSIFIED DRUG;

APOPTOSIS; B LYMPHOCYTE; CELL INTERACTION; ERYTHROBLAST; HEMATOPOIESIS; HUMAN; MYELOPOIESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RETICULOCYTE; REVIEW; SIGNAL TRANSDUCTION; STROMA CELL; T LYMPHOCYTE; THYMOCYTE;

CELL PROLIFERATION; GALECTINS; HEMATOPOIESIS; HUMANS;

EID: 80054748349     PISSN: 10656251     EISSN: 15317048     Source Type: Journal    
DOI: 10.1097/MOH.0b013e32834bab18     Document Type: Review

References (104)

1. Takaku T, Malide D, Chen J, et al. Hematopoiesis in 3 dimensions: Human and murine bone marrow architecture visualized by confocal microscopy. Blood 2010; 116:e41-e55.
2. Kiel MJ, Morrison SJ. Uncertainty in the niches that maintain haematopoietic stem cells. Nat Rev Immunol 2008; 8:290-301. (Pubitemid 351432804)
3. Singbrant S, Russell MR, Jovic T, et al. Erythropoietin couples erythropoiesis, B lymphopoiesis, and bone homeostasis within the bone marrow microenvironment. Blood 2011; 115:4689-4698.
4. Barondes SH, Castronovo V, Cooper DN, et al. Galectins: A family of animal beta-galactoside-binding lectins. Cell 1994; 76:597-598. (Pubitemid 24070645)
5. Hirabayashi J, Hashidate T, Arata Y, et al. Oligosaccharide specificity of galectins: A search by frontal affinity chromatography. Biochim Biophys Acta 2002; 1572:232-254. (Pubitemid 35246347)
6. Yang RY, Rabinovich GA, Liu FT. Galectins: Structure, function and therapeutic potential. Expert Rev Mol Med 2008; 10:e17.
7. Sundblad V, Croci DO, Rabinovich GA. Regulated expression of galectin-3, a multifunctional glycan-binding protein, in haematopoietic and nonhaematopoietic tissues. Histol Histopathol 26:247-265.
8. Rabinovich GA, Ilarregui JM. Conveying glycan information into T-cell homeostatic programs: A challenging role for galectin-1 in inflammatory and tumor microenvironments. Immunol Rev 2009; 230:144-159.
9. Liu FT, Rabinovich GA. Galectins: Regulators of acute and chronic inflammation. Ann N Y Acad Sci 2010; 1183:158-182.
10. Laderach DJ, Compagno D, Toscano MA, et al. Dissecting the signal transduction pathways triggered by galectin-glycan interactions in physiological and pathological settings. IUBMB Life 2010; 62:1-13.
11. Delacour D, Koch A, Jacob R. The role of galectins in protein trafficking. Traffic 2009; 10:1405-1413.
12. Zhuo Y, Bellis SL. Emerging role of alpha2,6-sialic acid as a negative regulator of galectin binding and function. J Biol Chem 2011; 286:5935-5941.
13. Rabinovich GA, Toscano MA, Jackson SS, Vasta GR. Functions of cell surface galectin-glycoprotein lattices. Curr Opin Struct Biol 2007; 17:513-520. (Pubitemid 350019014)
14. Boscher C, Dennis JW, Nabi IR. Glycosylation, galectins and cellular signaling. Curr Opin Cell Biol 2011 [Epub ahead of print].
15. Stillman BN, Hsu DK, Pang M, et al. Galectin-3 and galectin-1 bind distinct cell surface glycoprotein receptors to induce T cell death. J Immunol 2006; 176:778-789. (Pubitemid 43099674)
16. Nguyen JT, Evans DP, Galvan M, et al. CD45 modulates galectin-1-induced T cell death: Regulation by expression of core 2 O-glycans. J Immunol 2001; 167:5697-5707. (Pubitemid 33062760)
17. Wang J, Lu ZH, Gabius HJ, et al. 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; 182:4036-4045.
18. Rossi B, Espeli M, Schiff C, Gauthier L. Clustering of pre-B cell integrins induces galectin-1-dependent pre-B cell receptor relocalization and activation. J Immunol 2006; 177:796-803. (Pubitemid 44036579)
19. Fulcher JA, Chang MH, Wang S, et al. Galectin-1 co-clusters CD43/CD45 on dendritic cells and induces cell activation and migration through Syk and protein kinase C signaling. J Biol Chem 2009; 284:26860-26870.
20. Ilarregui JM, Croci DO, Bianco GA, et al. Tolerogenic signals delivered by dendritic cells to T cells through a galectin-1-driven immunoregulatory circuit involving interleukin 27 and interleukin 10. Nat Immunol 2009; 10:981-991.
21. Hsieh SH, Ying NW, Wu MH, et al. Galectin-1, a novel ligand of neuropilin-1, activates VEGFR-2 signaling and modulates the migration of vascular endothelial cells. Oncogene 2008; 27:3746-3753. (Pubitemid 351912963)
22. Bessis M. Erythroblastic island, functional unity of bone marrow. Rev Hematol 1958; 13:8-11.
23. Manwani D, Bieker JJ. The erythroblastic island. Curr Top Dev Biol 2008; 82:23-53.
24. Chasis JA, Mohandas N. Erythroblastic islands: Niches for erythropoiesis. Blood 2008; 112:470-478.
25. Rhodes MM, Kopsombut P, Bondurant MC, et al. Adherence to macrophages in erythroblastic islands enhances erythroblast proliferation and increases erythrocyte production by a different mechanism than erythropoietin. Blood 2008; 111:1700-1708. (Pubitemid 351213462)
26. Hanspal M, Hanspal JS. The association of erythroblasts with macrophages promotes erythroid proliferation and maturation: A 30-kD heparin-binding protein is involved in this contact. Blood 1994; 84:3494-3504. (Pubitemid 24352914)
27. Sato S, St-Pierre C, Bhaumik P, Nieminen J. Galectins in innate immunity: Dual functions of host soluble beta-galactoside-binding lectins as damageassociated molecular patterns (DAMPs) and as receptors for pathogenassociated molecular patterns (PAMPs). Immunol Rev 2009; 230:172-187.
28. Crocker PR, Gordon S. Isolation and characterization of resident stromal macrophages and hematopoietic cell clusters from mouse bone marrow. J Exp Med 1985; 162:993-1014. (Pubitemid 16248204)
29. Harrison FL, Chesterton CJ. Erythroid developmental agglutinin is a protein lectin mediating specific cell-cell adhesion between differentiating rabbit erythroblasts. Nature 1980; 286:502-504. (Pubitemid 10017687)
30. Harrison FL, Catt JW. Intra- and extracellular distribution of an endogenous lectin during erythropoiesis. J Cell Sci 1986; 84:201-212.
31. Cerra RF, Gitt MA, Barondes SH. Three soluble rat beta-galactoside- binding lectins. J Biol Chem 1985; 260:10474-10477. (Pubitemid 16252219)
32. 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; 270:5032-5038.
33. Wada J, Kanwar YS. Identification and characterization of galectin-9, a novel beta-galactoside-binding mammalian lectin. J Biol Chem 1997; 272:6078-6086. (Pubitemid 27102450)
34. 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; 38:1741-1758. (Pubitemid 43947656)
35. Lutomski D, Fouillit M, Bourin P, et al. Externalization and binding of galectin-1 on cell surface of K562 cells upon erythroid differentiation. Glycobiology 1997; 7:1193-1199. (Pubitemid 28015808)
36. Altheide TK, Hayakawa T, Mikkelsen TS, et al. System-wide genomic and biochemical comparisons of sialic acid biology among primates and rodents: Evidence for two modes of rapid evolution. J Biol Chem 2006; 281:25689-25702. (Pubitemid 44401958)
37. Sadahira Y, Yasuda T, Kimoto T. Regulation of Forssman antigen expression during maturation of mouse stromal macrophages in haematopoietic foci. Immunology 1991; 73:498-504.
38. Yoshida H, Kawane K, Koike M, et al. Phosphatidylserine-dependent engulfment by macrophages of nuclei from erythroid precursor cells. Nature 2005; 437:754-758. (Pubitemid 41486546)
39. Freeman GJ, Casasnovas JM, Umetsu DT, DeKruyff RH. TIM genes: A family of cell surface phosphatidylserine receptors that regulate innate and adaptive immunity. Immunol Rev 235:172-189.
40. Zhu C, Anderson AC, Schubart A, et al. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat Immunol 2005; 6:1245-1252. (Pubitemid 43045636)
41. Stowell SR, Karmakar S, Stowell CJ, et al. Human galectin-1, -2, and -4 induce surface exposure of phosphatidylserine in activated human neutrophils but not in activated T cells. Blood 2007; 109:219-227. (Pubitemid 46053062)
42. Stowell SR, Arthur CM, Slanina KA, et al. Dimeric Galectin-8 induces phosphatidylserine exposure in leukocytes through polylactosamine recognition by the C-terminal domain. J Biol Chem 2008; 283:20547-20559.
43. Lee JC, Gimm JA, Lo AJ, et al. Mechanism of protein sorting during erythroblast enucleation: Role of cytoskeletal connectivity. Blood 2004; 103:1912-1919. (Pubitemid 38268991)
44. Salomao M, Chen K, Villalobos J, et al. Hereditary spherocytosis and hereditary elliptocytosis: Aberrant protein sorting during erythroblast enucleation. Blood 2010; 116:267-269. This study relates the aberrant sorting of proteins during enucleation in hereditary spherocytosis and elliptocytosis. Major cytoskeletal proteins (e.g. band 3, Rh-associated antigen, glycophorin A or C) are missorted to the extruded nucleus instead of being segregated to the reticulocyte.
45. Keerthivasan G, Small S, Liu H, et al. Vesicle trafficking plays a novel role in erythroblast enucleation. Blood 2010; 116:3331-3340. Various selective inhibitors and the knockdown of clathrin have been used to demonstrate that endocytic vesicle trafficking has a critical role during enucleation. Endocytic vesicles are targeted to the nucleus in which they accumulate, coalesce and fuse with the plasma membrane contributing to separation between the extruding nucleus and nascent reticulocyte.
46. 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; 71:218-231.
47. 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; 96:184-190. (Pubitemid 13155576)
48. Sano H, Hsu DK, Apgar JR, et al. Critical role of galectin-3 in phagocytosis by macrophages. J Clin Invest 2003; 112:389-397. (Pubitemid 38063767)
49. Chen K, Liu J, Heck S, et al. Resolving the distinct stages in erythroid differentiation based on dynamic changes in membrane protein expression during erythropoiesis. Proc Natl Acad Sci U S A 2009; 106:17413-17418.
50. Zhang J, Randall MS, Loyd MR, et al. Mitochondrial clearance is regulated by Atg7-dependent and -independent mechanisms during reticulocyte maturation. Blood 2009; 114:157-164.
51. Liu J, Guo X, Mohandas N, et al. Membrane remodeling during reticulocyte maturation. Blood 2010; 115:2021-2027.
52. Pan BT, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: Selective externalization of the receptor. Cell 1983; 33:967-977. (Pubitemid 13074002)
53. Harding C, Heuser J, Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol 1983; 97:329-339.
54. Iacopetta BJ, Morgan EH, Yeoh GC. Receptor-mediated endocytosis of transferrin by developing erythroid cells from the fetal rat liver. J Histochem Cytochem 1983; 31:336-344. (Pubitemid 13039737)
55. Barres C, Blanc L, Bette-Bobillo P, et al. Galectin-5 is bound onto the surface of rat reticulocyte exosomes and modulates vesicle uptake by macrophages. Blood 2010; 115:696-705. Galectin-5 is found associated with the endosomal compartment and on the surface of rat reticulocyte exosomes, suggesting a translocation from the cytosol into the endosome lumen. A possible role in segregation/sorting of suitable galactose-bearing glycoconjugates is discussed.
56. Wu AM, Singh T, Wu JH, et al. 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; 16:524-537. (Pubitemid 43779048)
57. 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; 10:438-450.
58. Schneider D, Greb C, Koch A, et al. Trafficking of galectin-3 through endosomal organelles of polarized and nonpolarized cells. Eur J Cell Biol 2010; 89:788-798.
59. Merlin J, Stechly L, de Beauce S, et al. Galectin-3 regulates MUC1 and EGFR cellular distribution and EGFR downstream pathways in pancreatic cancer cells. Oncogene 2011; 30:2514-2525. This study reports the regulation of MUCI and EGFR internalization and subcellular localization by galectin-3 in pancreatic cancer cells. Depletion of galectin-3 by RNA interference modifies oncogenic signaling pathways downstream of MUC1 and EGFR.
60. Mishra R,Grzybek M, Niki T, et al.Galectin-9 trafficking regulates apical-basal polarity in Madin-Darby canine kidney epithelial cells. Proc Natl Acad Sci U S A 2010; 107:17633-17638. Galectin-9 is internalized and recycled back to the apical membrane in MDCK cells. Sorting and delivery of the Forssman glycosphingolipid was impaired in the galectin-9 shRNA cells. This galectin-glycolipid interaction is critical to maintain epithelial integrity and cell polarity.
61. 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; 113:1957-1966.
62. Zomer A, Vendrig T, Hopmans ES, et al. Exosomes: Fit to deliver small RNA. Commun Integr Biol 2010; 3:447-450.
63. Byon JC, Papayannopoulou T. MicroRNAs: Allies or foes in erythropoiesis? J Cell Physiol 2011. doi: 10.1002/jcp.22729 [Epub ahead of print].
64. Nagasawa T. Microenvironmental niches in the bone marrow required for B-cell development. Nat Rev Immunol 2006; 6:107-116. (Pubitemid 43361586)
65. Monroe JG. ITAM-mediated tonic signalling through pre-BCR and BCR complexes. Nat Rev Immunol 2006; 6:283-294.
66. Gauthier L, Rossi B, Roux F, et al. Galectin-1 is a stromal cell ligand of the pre-B cell receptor (BCR) implicated in synapse formation between pre-B and stromal cells and in pre-BCR triggering. Proc Natl Acad Sci U S A 2002; 99:13014-13019.
67. Espeli M, Mancini SJ, Breton C, et al. Impaired B-cell development at the pre- BII-cell stage in galectin-1-deficient mice due to inefficient pre-BII/stromal cell interactions. Blood 2009; 113:5878-5886.
68. Mourcin F, Breton C, Tellier J, et al. Galectin-1 expressing stromal cells constitute a specific niche for pre-BII cell development in mouse bone marrow. Blood 2011; 117:6552-6561. In this study, the authors characterized stromal cells that express galectin-1 and constitute a specific cellular niche for pre-BII cells in mouse bone marrow. These stromal cells are distinct from IL7-secreting stromal cells, arguing for a migration of early B cells from IL7+ to galectin-1+ niches during their differentiation.
69. Zuniga E, Rabinovich GA, Iglesias MM, Gruppi A. Regulated expression of galectin-1 during B-cell activation and implications for T-cell apoptosis. J Leukoc Biol 2001; 70:73-79. (Pubitemid 32613665)
70. Tsai CM, Chiu YK, Hsu TL, et al. Galectin-1 promotes immunoglobulin production during plasma cell differentiation. J Immunol 2008; 181:4570-4579.
71. Acosta-Rodriguez EV, Montes CL, Motran CC, et al. Galectin-3 mediates IL-4-induced survival and differentiation of B cells: Functional cross-talk and implications during Trypanosoma cruzi infection. J Immunol 2004; 172:493-502. (Pubitemid 38020505)
72. Hogquist KA, Baldwin TA, Jameson SC. Central tolerance: Learning selfcontrol in the thymus. Nat Rev Immunol 2005; 5:772-782. (Pubitemid 41400851)
73. Perillo NL, Uittenbogaart CH, Nguyen JT, Baum LG. Galectin-1, an endogenous lectin produced by thymic epithelial cells, induces apoptosis of human thymocytes. J Exp Med 1997; 185:1851-1858. (Pubitemid 27242206)
74. Pace KE, Lee C, Stewart PL, Baum LG. Restricted receptor segregation into membrane microdomains occurs on human T cells during apoptosis induced by galectin-1. J Immunol 1999; 163:3801-3811. (Pubitemid 29450905)
75. Earl LA, Bi S, Baum LG. Galectin multimerization and lattice formation are regulated by linker region structure. Glycobiology 2011; 21:6-12.
76. Villa-Verde DM, Silva-Monteiro E, Jasiulionis MG, et al. Galectin-3 modulates carbohydrate-dependent thymocyte interactions with the thymic microenvironment. Eur J Immunol 2002; 32:1434-1444. (Pubitemid 34546272)
77. Silva-Monteiro E, Reis Lorenzato L, Kenji Nihei O, et al. Altered expression of galectin-3 induces cortical thymocyte depletion and premature exit of immature thymocytes during Trypanosoma cruzi infection. Am J Pathol 2007; 170:546-556. (Pubitemid 47339392)
78. Bi S, Earl LA, Jacobs L, Baum LG. Structural features of galectin-9 and galectin-1 that determine distinct T cell death pathways. J Biol Chem 2008; 283:12248-12258.
79. Tribulatti MV, Mucci J, Cattaneo V, et al. Galectin-8 induces apoptosis in the CD4(high)CD8(high) thymocyte subpopulation. Glycobiology 2007; 17:1404-1412. (Pubitemid 350131316)
80. Liu SD, Whiting CC, Tomassian T, et al. Endogenous galectin-1 enforces class I-restricted TCR functional fate decisions in thymocytes. Blood 2008; 112:120-130.
81. Rabinovich GA, Toscano MA. Turning 'sweet' on immunity: Galectin-glycan interactions in immune tolerance and inflammation. Nat Rev Immunol 2009; 9:338-352.
82. Cooper D, Ilarregui JM, Pesoa SA, et al. Multiple functional targets of the immunoregulatory activity of galectin-1: Control of immune cell trafficking, dendritic cell physiology, and T-cell fate. Methods Enzymol 2010; 480:199-244.
83. Garin MI, Chu CC, Golshayan D, et al. Galectin-1: A key effector of regulation mediated by CD4+CD25+ T cells. Blood 2007; 109:2058-2065. (Pubitemid 46348206)
84. Kubach J, Lutter P, Bopp T, et al. Human CD4+CD25+ regulatory T cells: Proteome analysis identifies galectin-10 as a novel marker essential for their anergy and suppressive function. Blood 2007; 110:1550-1558. (Pubitemid 47443971)
85. Gieseke F, Bohringer J, Bussolari R, et al. Human multipotent mesenchymal stromal cells use galectin-1 to inhibit immune effector cells. Blood 116:3770-3779.
86. Rabinovich GA, Ramhorst RE, Rubinstein N, et al. Induction of allogenic T-cell hyporesponsiveness by galectin-1-mediated apoptotic and nonapoptotic mechanisms. Cell Death Differ 2002; 9:661-670. (Pubitemid 34618872)
87. Cerliani JP, Stowell SR, Mascanfroni ID, et al. Expanding the universe of cytokines and pattern recognition receptors: Galectins and glycans in innate immunity. J Clin Immunol 2011; 31:10-21.
88. Abedin MJ, Kashio Y, Seki M, et al. Potential roles of galectins in myeloid differentiation into three different lineages. J Leukoc Biol 2003; 73:650-656. (Pubitemid 38040478)
89. Vas V, Fajka-Boja R, Ion G, et al. Biphasic effect of recombinant galectin-1 on the growth and death of early hematopoietic cells. Stem Cells 2005; 23:279-287. (Pubitemid 40239522)
90. Mascanfroni ID, Cerliani JP, Dergan-Dylon S, et al. Endogenous lectins shape the function of dendritic cells and tailor adaptive immunity: Mechanisms and biomedical applications. Int Immunopharmacol 2011; 11:831-838.
91. Kuo PL, Hung JY, Huang SK, et al. Lung cancer-derived galectin-1 mediates dendritic cell anergy through inhibitor of DNA binding 3/IL-10 signaling pathway. J Immunol 186:1521-1530.
92. Barrionuevo P, Beigier-Bompadre M, Ilarregui JM, et al. A novel function for galectin-1 at the crossroad of innate and adaptive immunity: Galectin-1 regulates monocyte/macrophage physiology through a nonapoptotic ERKdependent pathway. J Immunol 2007; 178:436-445. (Pubitemid 46033627)
93. MacKinnon AC, Farnworth SL, Hodkinson PS, et al. Regulation of alternative macrophage activation by galectin-3. J Immunol 2008; 180:2650-2658.
94. Anderson AC, Anderson DE, Bregoli L, et al. Promotion of tissue inflammation by the immune receptor Tim-3 expressed on innate immune cells. Science 2007; 318:1141-1143. (Pubitemid 350134897)
95. Chen HY, Sharma BB, Yu L, et al. Role of galectin-3 in mast cell functions: Galectin-3-deficient mast cells exhibit impaired mediator release and defective JNK expression. J Immunol 2006; 177:4991-4997. (Pubitemid 44527568)
96. Niki T, Tsutsui S, Hirose S, et al. Galectin-9 is a high affinity IgE-binding lectin with antiallergic effect by blocking IgE-antigen complex formation. J Biol Chem 2009; 284:32344-32352.
97. Ge XN, Bahaie NS, Kang BN, et al. Allergen-induced airway remodeling is impaired in galectin-3-deficient mice. J Immunol 2010; 185:1205-1214.
98. Nishi N, Shoji H, Seki M, et al. Galectin-8 modulates neutrophil function via interaction with integrin alphaM. Glycobiology 2003; 13:755-763. (Pubitemid 37407105)
99. Fernandez GC, Ilarregui JM, Rubel CJ, et al. Galectin-3 and soluble fibrinogen act in concert to modulate neutrophil activation and survival: Involvement of alternative MAPK pathways. Glycobiology 2005; 15:519-527. (Pubitemid 41214397)
100. Larson MK, Watson SP. A product of their environment: Do megakaryocytes rely on extracellular cues for proplatelet formation? Platelets 2006; 17:435-440. (Pubitemid 44665565)
101. Malara A, Gruppi C, Rebuzzini P, et al. Megakaryocyte-matrix interaction within bone marrow: New roles for fibronectin and factor XIII-A. Blood 117:2476-2483.
102. Pallotta I, Lovett M, Rice W, et al. Bone marrow osteoblastic niche: A new model to study physiological regulation of megakaryopoiesis. PLoS One 2009; 4:e8359.
103. D'Atri LP, Pozner RG, Nahmod KA, et al. Paracrine regulation of megakaryo/ thrombopoiesis by macrophages. Exp Hematol 2011; 763-772.
104. Pacienza N, Pozner RG, Bianco GA, et al. The immunoregulatory glycanbinding protein galectin-1 triggers human platelet activation. FASEB J 2008; 22:1113-1123. (Pubitemid 351519966)