GALECTIN-1 AND ITS ROLE IN DEVELOPMENT OF INNATE AND ADAPTIVE IMMUNITY
https://doi.org/10.15789/1563-0625-2012-1-2-21-32
Abstract
Abstract. Galectins comprise a family of β-galactoside-binding animal proteins, which are defined by
common homologies of their carbohydrate-recognizing domaine (affinity for poly-N-acetyllactosamine). These lectins bind to cell surface glycans and extracellular matrix, thus influencing various cellular events, including cell cycle, adhesion, migration, proliferation and apoptosis. Moreover, galectins are able to exert intracellular effects, and participate, e.g., in signal transduction, by interacting with other nuclear and cytoplasmic proteins. Galectin-1 is considered to play a special role in functional regulation of immune cell activity. Thus protein is a factor of immunocompetent cell cooperation, thus being able to modulate immune reactions. In this respect, galectin-1 is considered as a potential agent or a target for new methods aimed to correct pathological processes associated with imbalance of immune system. This article provides an overview of works devoted to a possible role of galectin-1 in development of typical features of innate and adaptive immunity.
common homologies of their carbohydrate-recognizing domaine (affinity for poly-N-acetyllactosamine). These lectins bind to cell surface glycans and extracellular matrix, thus influencing various cellular events, including cell cycle, adhesion, migration, proliferation and apoptosis. Moreover, galectins are able to exert intracellular effects, and participate, e.g., in signal transduction, by interacting with other nuclear and cytoplasmic proteins. Galectin-1 is considered to play a special role in functional regulation of immune cell activity. Thus protein is a factor of immunocompetent cell cooperation, thus being able to modulate immune reactions. In this respect, galectin-1 is considered as a potential agent or a target for new methods aimed to correct pathological processes associated with imbalance of immune system. This article provides an overview of works devoted to a possible role of galectin-1 in development of typical features of innate and adaptive immunity.
About the Authors
V. D. Yakushina
ГБОУ ВПО Сибирский государственный медицинский университет Минздравсоцразвития России, г. Томск
Russian Federation
Russian Federation
O. A. Vasilyeva
ГБОУ ВПО Сибирский государственный медицинский университет Минздравсоцразвития России, г. Томск
Russian Federation
Russian Federation
N. V. Ryazantseva
ГБОУ ВПО Сибирский государственный медицинский университет Минздравсоцразвития России, г. Томск
Russian Federation
Russian Federation
V. V. Novitsky
ГБОУ ВПО Сибирский государственный медицинский университет Минздравсоцразвития России, г. Томск
Russian Federation
Russian Federation
O. E. Savelyeva
ГБОУ ВПО Сибирский государственный медицинский университет Минздравсоцразвития России, г. Томск
Russian Federation
Russian Federation
T. S. Prokhorenko
ГБОУ ВПО Сибирский государственный медицинский университет Минздравсоцразвития России, г. Томск
Russian Federation
Russian Federation
E. G. Starikova
ГБОУ ВПО Сибирский государственный медицинский университет Минздравсоцразвития России, г. Томск
Russian Federation
Russian Federation
A. P. Zima
ГБОУ ВПО Сибирский государственный медицинский университет Минздравсоцразвития России, г. Томск
Russian Federation
Russian Federation
References
1. Almkvist J., Dahlgren C., Leffler H., Karlsson A. Activation of the neutrophil nicotinamide adenine dinucleotide phosphate oxidase by galectin-1 // J. Immunol. – 2002. – Vol. 168. – P. 4034-4041.
2. Barrionuevo P., Beigier-Bompadre M., Ilarregui J.M., Toscano M.A., Bianco G.A., Isturiz M.A., Rabinovich G.A. A novel function for galectin-1 at the crossroad of innate and adaptive immunity: galectin-1 regulates monocyte/macrophage physiology through a nonapoptotic ERK-dependent pathway // J. Immunol. – 2007. – Vol. 178. – P. 436-445.
3. Baum L.G., Blackall D.P., Arias-Magallano S., Nanigian D., Uh S.Y., Browne J.M., Hoffmann D., Emmanouilides C.E., Territo M.C., Baldwin G.C. Amelioration of graft versus host disease by galectin-1 // Clin. Immunol. – 2003. – Vol. 109. – P. 295-307.
4. Blaser C., Kaufmann M., M ller C., Zimmermann C., Wells V., Mallucci L., Pircher H. Beta-galactoside binding protein secreted by activated T cells inhibits antigen-induced proliferation of T cells. // Eur. J. Immunol. – 1998. – Vol. 28. – P. 2311-2319.
5. Blois S.M. Ilarregui J.M., Tometten M.,Garcia M., Orsal A.S., Cordo-Russo R., Toscano M.A., Bianco G.A., Kobelt P., Handjiski B., Tirado I., Markert U.R., Klapp B.F., Poirier F., Szekeres-Bartho J., Rabinovich G.A., Arck P.C. A pivotal role for galectin-1 in fetomaternal tolerance // Nat. Med. – 2007. – Vol. 13. – P.1450-1457.
6. Brandt B., Abou-Eladab E.F., Tiedge M., Walzel H. Role of the JNK/c-Jun/AP-1 signaling pathway in galectin-1-induced T-cell death // Cell Death Dis. – 2010. – Vol. 1, N 2. – P.:e23.
7. Chung C.D., Patel V.P., Moran M., Lewis L.A., Miceli M.C. Galectin-1 induces partial TCR zeta-chain phosphorylation and antagonizes processive TCR signal transduction // J. Immunol. – 2000. – Vol. 165. – P. 3722-3729.
8. Cooper D., Norling L.V., Perretti M. Novel insights into the inhibitory effects of Galectin-1 on neutrophil recruitment under flow // J. Leukoc. Biol. – 2008. – Vol. 83. – P. 1459-1466.
9. Correa S.G., Sotomayor C.E., Aoki M.P., Maldonado C.A., Rabinovich G.A. Opposite effects of galectin-1 on alternative metabolic pathways of L-arginine in resident, inflammatory, and activated macrophages // Glycobiology. – 2003. – Vol. 13. – P. 119-128.
10. Denzer K., Kleijmeer M.J., Heijnen H.F., Stoorvogel W., Geuze H.J. Exosome: frominternal vesicle of themultivesicular body to intercellular signaling device // J. Cell Sci. – 2000. – Vol. 113. – P. 3365-3374.
11. Endharti A.T., Zhou Y.W., Nakashima I., Suzuki H. Galectin-1 supports survival of naive T cells without promoting cell proliferation // Eur. J. Immunol. – 2005. – Vol. 35. – P. 86-97.
12. Espeli M., Mancini S.J., Breton C., Poirier F., Schiff C. 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. – Vol. 113. – P. 5878-5886.
13. Fuertes M.B., Molinero L.L., Toscano M.A., Ilarregui J.M., Rubinstein N., Fainboim L., Zwirner N.W., Rabinovich G.A. Regulated expression of galectin-1 during T-cell activation involves Lck and Fyn kinases and signaling through MEK1/ERK, p38 MAP kinase and p70S6 kinase // Mol. Cell Biochem. – 2004. – Vol. 267. – P. 177-185.
14. Fulcher J.A., Hashimi S.T., Levroney E.L., Pang M., Gurney K.B., Baum L.G., Lee B. Galectin-1-matured human monocyte-derived dendritic cells have enhanced migration through extracellular matrix // J. Immunol. – 2006. – Vol. 177. – P. 216-226.
15. Gandhi M.K., Moll G., Smith C., Dua U., Lambley E., Ramuz O., Gill D., Marlton P., Seymour J.F., Khanna R. Galectin-1 mediated suppression of Epstein-Barr virus specific T-cell immunity in classic Hodgkin lymphoma // Blood. – 2007. – Vol. 110. – P. 1326-1329.
16. Garin M.I., Chu C.C., Golshayan D., Cernuda-Morollon E., Wait R., Lechler R.I. Galectin-1: a key effector of regulation mediated byCD4+CD25+ Tcells // Blood. – 2007. – Vol. 109. – P. 2058-2065.
17. Gauthier L., Rossi B., Roux F., Termine E., Schiff C. 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. USA. – 2002. – Vol. 99. – P. 13014-13019.
18. Hahn H.P., Pang M., He J., Hernandez J.D., Yang R.Y., Li L.Y., Wang X., Liu F.T., Baum L.G. Galectin-1 induces nuclear translocation of endonuclease G in caspase- and cytochrome c-independent T cell death // Cell Death Differ. – 2004. – Vol. 11, N 12. – P. 1277-1286.
19. He J., Baum L.G. Endothelial cell expression of galectin-1 induced by prostate cancer cells inhibits T-cell transendothelial migration // Lab. Invest. – 2006. – Vol. 86, N 6. – P. 578-590. Hughes R.C. Secretion of the galectin family of mammalian carbohydrate-binding proteins // Biochim. Biophys. Acta. – 1999. – Vol. 1473. – P. 172-185.
20. Ilarregui J.M., Croci D.O., Bianco G.A., Toscano M.A., Salatino M., Vermeulen M.E., Geffner J.R., Rabinovich G.A. 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. – Vol. 10, N 9. – P. 981-991.
21. Ion G., Fajka-Boja R., T th G.K., Caron M., Monostori E. Role of p56lck and ZAP70-mediated tyrosine phosphorylation in galectin-1-induced cell death // Cell Death Differ. – 2005. – Vol. 12, N 8. – P. 1145-1147.
22. Juszczynski P., Ouyang J., Monti S., Rodig S.J., Takeyama K., Abramson J., Chen W., Kutok J.L., Rabinovich G.A., Shipp M.A. The AP1-dependent secretion of galectin-1 by Reed Sternberg cells fosters immune privilege in classical Hodgkin lymphoma // Proc. Natl. Acad. Sci. USA. – 2007. – Vol. 104. – P. 13134-13139.
23. Karmakar S., Stowell S.R., Cummings R.D., McEver R.P. Galectin-1 signaling in leukocytes requires expression of complex-type N-glycans // Glycobiology. – 2008. – Vol. 18. – P. 770-778.
24. Kopcow H.D., Rosetti F., Leung Y., Allan D.S., Kutok J.L., Strominger J.L. T cell apoptosis at the maternal-fetal interface in early human pregnancy, involvement of galectin-1 // Proc. Natl. Acad. Sci. USA. – 2008. – Vol. 105. – P. 18472-18477.
25. Kuo P.L., Hung J.Y., Huang S.K., Chou S.H., Cheng D.E., Jong Y.J., Hung C.H., Yang C.J., Tsai Y.M., Hsu Y.L., Huang M.S. Lung cancerderived galectin-1 mediates dendritic cell anergy through inhibitor of DNA binding 3/IL-10 signaling pathway // J. Immunol. – 2011. – Vol. 186, N 3. – P. 1521-1530.
26. La M., Cao T.V., Cerchiaro G., Chilton K., Hirabayashi J., Kasai K., Oliani S.M., Chernajovsky Y., Perretti M. A novel biological activity for galectin-1: inhibition of leukocyte-endothelial cell interactionsin experimental inflammation // Am. J. Pathol. – 2003. – Vol. 163. – P. 1505-1515.
27. Levi G., Tarrab-Hazdai R., Teichberg V.I. Prevention and therapy with electrolectin of experimental autoimmune myasthenia gravis in rabbits // Eur. J. Immunol. – 1983. – Vol. 13. – P. 500-507.
28. Liu F.T., Patterson R.J., Wang J.L. Intracellular functions of galectins // Biochim. Biophys. Acta. – 2002. – Vol. 1572. – P. 263-273.
29. Liu F.T., Rabinovich G.A. Galectins: regulators of acute and chronic inflammation // Ann. N. Y. Acad. Sci. – 2010. – Vol. 1183. – P. 158-182.
30. Liu S.D., Tomassian T., Bruhn K.W., Miller J.F., Poirier F., Miceli M.C. Galectin-1 tunes TCR binding and signal transduction to regulate CD8 burst size // J. Immunol. 2009. – Vol. 182. – P. 5283-5295.
31. Liu S.D., Whiting C.C., Tomassian T., Pang M., Bissel S.J., Baum L.G., Mossine V.V., Poirier F., Huflejt M.E., Miceli M.C. Endogenous galectin-1 enforces class I-restricted TCR functional fate decisions in thymocytes // Blood. – 2008. – Vol. 112. – P. 120-130.
32. Matarrese P., Tinari A., Mormone E., Bianco G.A., Toscano M.A., Ascione B., Rabinovich G.A., Malorni W. Galectin-1 sensitizes resting human T lymphocytes to Fas (CD95)-mediated cell death via mitochondrial hyperpolarization, budding, and fission // J. Biol Chem. – 2005. – Vol. 280, N 8. – P. 6969-6985.
33. Mercier S., St-Pierre C., Pelletier I., Ouellet M., Tremblay M.J., Sato S. Galectin-1 promotes HIV-1 in- fectivity in macrophages through stabilization of viral adsorption // Virology. – 2008. – Vol. 371. – P. 121-129.
34. Motran C.C., Molinder K.M., Liu S.D., Poirier F., Miceli M.C. Galectin-1 functions as a Th2 cytokine that selectively induces Th1 apoptosis and promotes Th2 function // Eur. J. Immunol. – 2008. – Vol. 38. – P. 3015-3027.
35. Nguyen J.T., Evans D.P., Galvan M., Pace K.E., Leitenberg D., Bui T.N., Baum L.G. CD45 modulates galectin-1-induced T cell death: regulation by expression of core 2 O-glycans // J. Immunol. – 2001. – Vol. 167. – P. 5697-5707.
36. Nickel W. The mystery of nonclassical protein secretion // Eur. J. Biochem. – 2003. – Vol. 270. – P. 2109-2119.
37. Norling L.V., Sampaio A.L., Cooper D., Perretti M. Inhibitory control of endothelial galectin-1 on in vitro and in vivo lymphocyte trafficking // FASEB J. – 2008. – Vol. 22. – P. 682-690.
38. Offner H., Celnik B., Bringman T.S., Casentini-Borocz D., Nedwin G.E., Vandenbark A.A. Recombinant human beta-galactoside binding lectin suppresses clinical and histological signs of experimental autoimmune encephalomyelitis // J. Neuroimmunol. – 1990. – Vol. 28. – P. 177-184.
39. Pacienza N., Pozner R.G., Bianco G.A., D’Atri L.P., Croci D.O., Negrotto S., Malaver E., Gomez R.M., Rabinovich G.A., Schattner M. The immunoregulatory glycan-binding protein galectin-1 triggers human platelet activation // FASEB J. – 2008. – Vol. 22. – P. 1113-1123.
40. Perillo N.L., Pace K.E., Seilhamer J.J., Baum L.G. Apoptosis of T cells mediated by galectin-1 // Nature. – 1995. – Vol. 378. – P. 736-739.
41. Perone M.J., Bertera S., Shufesky W.J. Divito S.J., Montecalvo A., Mathers A.R., Larregina A.T., Pang M., Seth N., Wucherpfennig K.W., Trucco M., Baum L.G., Morelli A.E. Suppression of autoimmune diabetes by soluble galectin-1 // J. Immunol. – 2009. – Vol. 182. – P. 2641-2653.
42. Perone M.J., Bertera S., Tawadrous Z.S., Shufesky W.J., Piganelli J.D., Baum L.G., Trucco M., Morelli A.E. Dendritic cells expressing transgenic galectin-1 delay onset of autoimmune diabetes in mice // J. Immunol. – 2006. – Vol. 177. – P. 5278-5289.
43. Rabinovich G., Daly G., Dreja H., Tailor H., Riera C.M., Hirabayashi J., Chernajovsky Y. Recombinant galectin-1 and its genetic delivery suppress collagen-induced arthritis via T cell apoptosis // J. Exp. Med. – 1999. – Vol. 190. – P. 385-397.
44. Rabinovich G.A., Ariel A., Hershkoviz R., Hirabayashi J., Kasai K.I., Lider O. Specific inhibition of T-cell adhesion to extracellular matrix and proinflammatory cytokine secretion by human recombinant galectin-1 // Immunology 1999. – Vol. 97. – P. 100-106.
45. Rabinovich G.A., Liu F.T., Hirashima M., Anderson A. An emerging role for galectins in tuning the immune response: lessons from experimental models of inflammatory disease, autoimmunity and cancer // Scand. J. Immunol. – 2007. – Vol. 66. – P. 143-158.
46. Rabinovich G.A., Ramhorst R.E., Rubinstein N., Corigliano A., Daroqui M.C., Kier-Joffe E.B., Fainboim L. Induction of allogenic Tcell hyporesponsiveness by galectin-1-mediated apoptotic and non-apoptotic mechanisms // Cell Death Differ. – 2002. – Vol. 9. – P. 661-670.
47. Rabinovich G.A., Sotomayor C.E., Riera C.M., Bianco I., Correa S.G. Evidence of a role for galectin-1 in acute inflammation // Eur. J. Immunol. – 2000. – Vol. 30. – P. 1331-1339.
48. Rodig S.J., Ouyang J., Juszczynski P., Currie T., Law K., Neuberg D.S., Rabinovich G.A., Shipp M.A., Kutok J.L. AP1-dependent galectin-1 expression delineates classical hodgkin and anaplastic large cell lymphomas from other lymphoid malignancies with shared molecular features // Clin. Cancer Res. - 2008. – Vol. 14. – P. 3338-3344.
49. 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. – Vol. 177. – P. 796-803.
50. Rubinstein N., Alvarez M., Zwirner N.W., Toscano M.A., Ilarregui J.M., Bravo A., Mordoh J., Fainboim L., Podhajcer O.L., Rabinovich G.A. Targeted inhibition of galectin-1 gene expression in tumor cells results in heightened T cell-mediated rejection; A potential mechanism of tumor-immune privilege // Cancer Cell. – 2004. – Vol. 5. – P. 241-251.
51. Santucci L., Fiorucci S., Cammilleri F., Servillo G., Federici B., Morelli A. Galectin-1 exerts immunomodulatory and protective effects on concanavalin A-induced hepatitis in mice // Hepatology. – 2000. – Vol. 31. – P. 399-406.
52. Santucci L., Fiorucci S., Rubinstein N., Mencarelli A., Palazzetti B., Federici B., Rabinovich G.A., Morelli A. Galectin-1 suppresses experimental colitis in mice // Gastroenterology. – 2003. – Vol. 124. – P. 1381-1394.
53. Seelenmeyer C., Wegehingel S., Tews I., Kunzler M., Aebi M., Nickel W. Cell surface counter receptors are essential components of the unconventional export machinery of galectin-1 // J. Cell Biol. – 2005. – Vol. 171. – P. 373-381.
54. Stillman B.N., Hsu D.K., Pang M., Brewer C.F., Johnson P., Liu F.T., Baum L.G. Galectin-3 and galectin-1 bind distinct cell surface glycoprotein receptors to induce T cell death // J. Immunol. – 2006. – Vol. 176. – P. 778-789.
55. Stowell S.R., Karmakar S., Arthur C.M., Ju T., Rodrigues L.C., Riul T.B., Dias-Baruffi M., Miner J., McEver R.P., Cummings R.D. Galectin-1 induces reversible phosphatidylserine exposure at the plasma membrane // Mol. Biol. Cell. – 2009. – Vol. 20. – P. 1408-1418.
56. Stowell S.R., Karmakar S., Stowell C.J., Dias-Baruffi M., McEver R.P., Cummings R.D. Human galectin-1, -2, and -4 induce surface exposure of phosphatidylserine in activated human neutrophils but not in activated T cells // Blood. – 2007. – Vol. 109. – P. 219-227.
57. Stowell S.R., Qian Y., Karmakar S, Koyama N.S., Dias-Baruffi M., Leffler H., McEver R.P., Cummings R.D. Differential roles of galectin- 1 and galectin-3 in regulating leukocyte viability and cytokine secretion // J. Immunol. – 2008. – Vol. 180. – P. 3091-3102.
58. Sugimoto N., Oida T., Hirota K., Nakamura K, Nomura T., Uchiyama T., Sakaguchi S. Foxp3-dependent and -independent molecules specific for CD25+CD4+ natural regulatory T cells revealed by DNA microarray analysis // Int. Immunol. – 2006. – Vol. 18. – P. 1197-1209.
59. Suzuki Y., Inoue T., Yoshimaru T., Ra C. Galectin-3 but not galectin-1 induces mast cell death by oxidative stress and mitochondrial permeability transition // Biochim. Biophys. Acta. – 2008. – Vol. 1783. – P. 924-934.
60. Tabrizi S.J., Niiro H., Masui M., Yoshimoto G., Iino T., Kikushige Y., Wakasaki T., Baba E., Shimoda S., Miyamoto T., Hara T., Akashi K. T cell leukemia/lymphoma 1 and galectin-1 regulate survival/cell death pathways in human naïve and IgM+ memory B cells through altering balances in Bcl-2 family proteins // J. Immunol. – 2009. – Vol. 182. – P. 1490-1499.
61. Terness P., Kallikourdis M., Betz A.G., Rabinovich G.A., Saito S., Clark D.A. Tolerance signaling molecules and pregnancy: IDO, galectins,
62. and the renaissance of regulatory T cells // Am. J. Reprod. Immunol. – 2007. – Vol. 58. – P. 238-254.
63. Toscano M.A., Bianco G.A., Ilarregui J.M., Croci D.O., Correale J., Hernandez J.D., Zwirner N.W., Poirier F., Riley E.M., Baum L.G., Rabinovich G.A. Differential glycosylation of T(H)1, T(H)2 and T(H)-17 effector cells selectively regulates susceptibility to cell death // Nat. Immunol. – 2007. – Vol. 8. – P. 825-834.
64. Toscano M.A., Commodaro A.G., Ilarregui J.M., Bianco G.A., Liberman A., Serra H.M., Hirabayashi J., Rizzo L.V., Rabinovich G.A. Galectin-1 suppresses autoimmune retinal disease by promoting concomitant Th2- and T regulatorymediated anti-inflammatory responses // J. Immunol. – 2006. – Vol. 176. – P. 6323-6332.
65. Tsai C.M., Chiu Y.K., Hsu T.L., Lin I.Y., Hsieh S.L., Lin K.I. Galectin-1 promotes immunoglobulin production during plasma cell differentiation // J. Immunol. – 2008. – Vol. 181. – P. 4570-4579.
66. Valenzuela H.F., Pace K.E., Cabrera P.V., White R., Porvari K., Kaija H., Vihko P., Baum L.G. O-glycosylation regulates LNCaP prostate cancer cell susceptibility to apoptosis induced by galectin-1 // Cancer Res. – 2007. – Vol. 67. – P. 6155-6162.
67. Van Der Leij J., van den Berg A., Harms G., Eschbach H., Vos H., Zwiers P., van Weeghel R., Groen H., Poppema S., Visser L. Strongly enhanced IL-10 production using stable galectin-1 homodimers // Mol. Immunol. – 2007. – Vol. 44. – P. 506-513.
68. Vyakarnam A., Dagher S.F., Wang J.L. Patterson R.J. Evidence for a role for galectin-1 in pre-mRNA splicing // Mol. Cell Biol. – 1997. – Vol. 17. – P. 4730-4737.
69. Wang J., Lu Z.H., Gabius H.J., Rohowsky-Kochan C., Ledeen R.W., 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. – Vol. 182. – P. 4036-4045.
70. Yang R.Y., Rabinovich G.A., Liu F.T. Galectins: structure, function and therapeutic potential // Expert Rev Mol Med. – 2008. – Vol. 13;10:e17.
71. Yu X., Siegel R., Roeder R.G. Interaction of the B cell-specific transcriptional coactivator OCA-B and galectin-1 and a possible role in regulating BCRmediated B cell proliferation // J. Biol Chem. –
72. – Vol. 281. – P. 15505-15516.
73. Zuniga E., Gruppi A., Hirabayashi J., Kasai K.I., Rabinovich G.A. Regulated expression and effect of galectin-1 on Trypanosoma cruziinfected macrophages: modulation of microbicidal activity and survival // Infect. Immun. – 2001. – Vol. 69. – P. 6804-6812.
74. Zuniga E., Rabinovich G.A., Iglesias M.M., Gruppi A. Regulated expression of galectin-1 during B-cell activation and implications for T-cell apoptosis // J. Leukoc. Biol. – 2001. – Vol. 70. – P. 73-79.
Review
For citations:
Yakushina V.D., Vasilyeva O.A., Ryazantseva N.V., Novitsky V.V., Savelyeva O.E., Prokhorenko T.S., Starikova E.G., Zima A.P. GALECTIN-1 AND ITS ROLE IN DEVELOPMENT OF INNATE AND ADAPTIVE IMMUNITY. Medical Immunology (Russia). 2012;14(1-2):21-32. (In Russ.) https://doi.org/10.15789/1563-0625-2012-1-2-21-32
Views:
1694
Email this article 