Advertisement

Galectins pp 1-35 | Cite as

Evolving Mechanistic Insights into Galectin Functions

  • Connie M. Arthur
  • Marcelo Dias Baruffi
  • Richard D. Cummings
  • Sean R. StowellEmail author
Part of the Methods in Molecular Biology book series (MIMB, volume 1207)

Abstract

Galectins are an evolutionarily ancient family of glycan-binding proteins (GBPs) and are found in all animals. Although they were discovered over 30 years ago, ideas about their biological functions continue to evolve. Current evidence indicates that galectins, which are the only known GBPs that occur free in the cytoplasm and extracellularly, are involved in a variety of intracellular and extracellular pathways contributing to homeostasis, cellular turnover, cell adhesion, and immunity. Here we review evolving insights into galectin biology from a historical perspective and explore current evidence regarding biological roles of galectins.

Key words

Galectin Glycan binging protein (GBP) Homeostasis Cellular turnover Cell adhesion Immunity Neoplasia Carbohydrates 

Abbreviations

APC

Antigen presenting cell

DC

Dendritic cell

DTT

Dithiothreitol

εBP

Epsilon binding protein

ER

Endoplasmic reticulum

FITC

Fluorescein isothiocyanate

Gal-1

Galectin-1

Gal-2

Galectin-2

Gal-3

Galectin-3

Gal-4

Galectin-4

Gal-7

Galectin-7

Gal-8

Galectin-8

Gal-9

Galectin-9

Gal-10

Galectin-10

Gal-12

Galectin-12

GBP

Glycan binding protein

IFN-γ

Interferon gamma

IgE

Immunoglobulin E

IL-10

Interleukin-10

IL-5

Interleukin-5

IL-6

Interleukin 6

KO

Knockout

LacNAc

N-acetyllactosamine

LPS

Lipopolysaccharide

MOG

Myelin oligodendrocyte protein

NK cell

Natural Killer Cell

NKT cell

Natural Killer T cell

PKC

Protein kinase C

PLC-γ

Phospholipase C-gamma

polyLacNAc

Poly-N-acetyllactosamine

PS

Phosphatidylserine

TCR

T cell receptor

TGF-β

Transforming growth factor beta

TH1

T helper cells type 1

TH2

T helper cells type 2

TNF

Tumor necrosis actor

Tregs

Regulatory T cells

vWF

von Willebrand Factor

Notes

Acknowledgments

This work was supported in part by grants from the National Blood Foundation, American Society of Hematology and Hemophilia of Georgia to S.R.S.

References

  1. 1.
    Varki A, Cummings R, Esko J, Freeze H, Stanley P, Bertozzi C, Hart G, Etzler M (2009) Essentials of Glycobiology, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYGoogle Scholar
  2. 2.
    Grewal PK, Uchiyama S, Ditto D, Varki N, Le DT, Nizet V, Marth JD (2008) The Ashwell receptor mitigates the lethal coagulopathy of sepsis. Nat Med 14(6):648–655. doi: 10.1038/nm1760, nm1760 [pii]PubMedPubMedCentralGoogle Scholar
  3. 3.
    Marth JD, Grewal PK (2008) Mammalian glycosylation in immunity. Nat Rev Immunol 8(11):874–887. doi: 10.1038/nri2417, nri2417 [pii]PubMedPubMedCentralGoogle Scholar
  4. 4.
    Cummings RD (2009) The repertoire of glycan determinants in the human glycome. Mol Biosyst 5(10):1087–1104. doi: 10.1039/b907931a PubMedGoogle Scholar
  5. 5.
    van Kooyk Y, Rabinovich GA (2008) Protein-glycan interactions in the control of innate and adaptive immune responses. Nat Immunol 9(6):593–601. doi: 10.1038/ni.f.203 PubMedGoogle Scholar
  6. 6.
    Offner H, Celnik B, Bringman TS, Casentini-Borocz D, Nedwin GE, Vandenbark AA (1990) Recombinant human beta-galactoside binding lectin suppresses clinical and histological signs of experimental autoimmune encephalomyelitis. J Neuroimmunol 28(2):177–184PubMedGoogle Scholar
  7. 7.
    Levi G, Tarrab-Hazdai R, Teichberg VI (1983) Prevention and therapy with electrolectin of experimental autoimmune myasthenia gravis in rabbits. Eur J Immunol 13(6):500–507. doi: 10.1002/eji.1830130613 PubMedGoogle Scholar
  8. 8.
    Kohatsu L, Hsu DK, Jegalian AG, Liu FT, Baum LG (2006) Galectin-3 induces death of Candida species expressing specific beta-1,2-linked mannans. J Immunol 177(7):4718–4726PubMedGoogle Scholar
  9. 9.
    Stowell SR, Arthur CM, Dias-Baruffi M, Rodrigues LC, Gourdine JP, Heimburg-Molinaro J, Ju T, Molinaro RJ, Rivera-Marrero C, Xia B, Smith DF, Cummings RD (2010) Innate immune lectins kill bacteria expressing blood group antigen. Nat Med 16(3):295–301. doi: 10.1038/nm.2103 PubMedPubMedCentralGoogle Scholar
  10. 10.
    Morell AG, Gregoriadis G, Scheinberg IH, Hickman J, Ashwell G (1971) The role of sialic acid in determining the survival of glycoproteins in the circulation. J Biol Chem 246(5):1461–1467PubMedGoogle Scholar
  11. 11.
    Van Den Hamer CJ, Morell AG, Scheinberg IH, Hickman J, Ashwell G (1970) Physical and chemical studies on ceruloplasmin. IX. The role of galactosyl residues in the clearance of ceruloplasmin from the circulation. J Biol Chem 245(17):4397–4402Google Scholar
  12. 12.
    Teichberg VI, Silman I, Beitsch DD, Resheff G (1975) A beta-D-galactoside binding protein from electric organ tissue of Electrophorus electricus. Proc Natl Acad Sci U S A 72(4):1383–1387PubMedPubMedCentralGoogle Scholar
  13. 13.
    Nowak TP, Haywood PL, Barondes SH (1976) Developmentally regulated lectin in embryonic chick muscle and a myogenic cell line. Biochem Biophys Res Commun 68(3):650–657, 0006-291X(76)91195-5 [pii]PubMedGoogle Scholar
  14. 14.
    de Waard A, Hickman S, Kornfeld S (1976) Isolation and properties of beta-galactoside binding lectins of calf heart and lung. J Biol Chem 251(23):7581–7587PubMedGoogle Scholar
  15. 15.
    Leffler H, Carlsson S, Hedlund M, Qian Y, Poirier F (2004) Introduction to galectins. Glycoconj J 19(7–9):433–440. doi: 10.1023/B:GLYC.0000014072.34840.04 PubMedGoogle Scholar
  16. 16.
    Simpson DL, Thorne DR, Loh HH (1977) Developmentally regulated lectin in neonatal rat brain. Nature 266(5600):367–369PubMedGoogle Scholar
  17. 17.
    Kobiler D, Barondes SH (1977) Lectin activity from embryonic chick brain, heart, and liver: changes with development. Dev Biol 60(1):326–330, 0012-1606(77)90130-0 [pii]PubMedGoogle Scholar
  18. 18.
    Kaufman SJ, Lawless ML (1980) Thiodigalactoside binding lectin and skeletal myogenesis. Differentiation 16(1):41–48PubMedGoogle Scholar
  19. 19.
    Tsuchiyama Y, Wada J, Zhang H, Morita Y, Hiragushi K, Hida K, Shikata K, Yamamura M, Kanwar YS, Makino H (2000) Efficacy of galectins in the amelioration of nephrotoxic serum nephritis in Wistar Kyoto rats. Kidney Int 58(5):1941–1952PubMedGoogle Scholar
  20. 20.
    Santucci L, Fiorucci S, Cammilleri F, Servillo G, Federici B, Morelli A (2000) Galectin-1 exerts immunomodulatory and protective effects on concanavalin A-induced hepatitis in mice. Hepatology 31(2):399–406. doi: 10.1002/hep.510310220 PubMedGoogle Scholar
  21. 21.
    Santucci L, Fiorucci S, Rubinstein N, Mencarelli A, Palazzetti B, Federici B, Rabinovich GA, Morelli A (2003) Galectin-1 suppresses experimental colitis in mice. Gastroenterology 124(5):1381–1394PubMedGoogle Scholar
  22. 22.
    Toscano MA, Bianco GA, Ilarregui JM, Croci DO, Correale J, Hernandez JD, Zwirner NW, Poirier F, Riley EM, Baum LG, Rabinovich GA (2007) Differential glycosylation of TH1, TH2 and TH-17 effector cells selectively regulates susceptibility to cell death. Nat Immunol 8(8):825–834. doi: 10.1038/ni1482 PubMedGoogle Scholar
  23. 23.
    Toscano MA, Commodaro AG, Ilarregui JM, Bianco GA, Liberman A, Serra HM, Hirabayashi J, Rizzo LV, Rabinovich GA (2006) Galectin-1 suppresses autoimmune retinal disease by promoting concomitant Th2- and T regulatory-mediated anti-inflammatory responses. J Immunol 176(10):6323–6332PubMedGoogle Scholar
  24. 24.
    Baum LG, Blackall DP, Arias-Magallano S, Nanigian D, Uh SY, Browne JM, Hoffmann D, Emmanouilides CE, Territo MC, Baldwin GC (2003) Amelioration of graft versus host disease by galectin-1. Clin Immunol 109(3):295–307PubMedGoogle Scholar
  25. 25.
    Blois SM, Ilarregui JM, Tometten M, Garcia M, Orsal AS, Cordo-Russo R, Toscano MA, Bianco GA, Kobelt P, Handjiski B, Tirado I, Markert UR, Klapp BF, Poirier F, Szekeres-Bartho J, Rabinovich GA, Arck PC (2007) A pivotal role for galectin-1 in fetomaternal tolerance. Nat Med 13(12):1450–1457PubMedGoogle Scholar
  26. 26.
    Levi G, Teichberg VI (1983) Selective interactions of electrolectins from eel electric organ and mouse thymus with mouse immature thymocytes. Immunol Lett 7(1):35–39PubMedGoogle Scholar
  27. 27.
    Baum LG, Pang M, Perillo NL, Wu T, Delegeane A, Uittenbogaart CH, Fukuda M, Seilhamer JJ (1995) Human thymic epithelial cells express an endogenous lectin, galectin-1, which binds to core 2 O-glycans on thymocytes and T lymphoblastoid cells. J Exp Med 181(3):877–887PubMedGoogle Scholar
  28. 28.
    Perillo NL, Pace KE, Seilhamer JJ, Baum LG (1995) Apoptosis of T cells mediated by galectin-1. Nature 378(6558):736–739. doi: 10.1038/378736a0 PubMedGoogle Scholar
  29. 29.
    van der Leij J, van den Berg A, Blokzijl T, Harms G, van Goor H, Zwiers P, van Weeghel R, Poppema S, Visser L (2004) Dimeric galectin-1 induces IL-10 production in T-lymphocytes: an important tool in the regulation of the immune response. J Pathol 204(5):511–518PubMedGoogle Scholar
  30. 30.
    Stowell SR, Qian Y, Karmakar S, Koyama NS, Dias-Baruffi M, Leffler H, McEver RP, Cummings RD (2008) Differential roles of galectin-1 and galectin-3 in regulating leukocyte viability and cytokine secretion. J Immunol 180(5):3091–3102PubMedGoogle Scholar
  31. 31.
    Cedeno-Laurent F, Opperman M, Barthel SR, Kuchroo VK, Dimitroff CJ (2012) Galectin-1 triggers an immunoregulatory signature in Th cells functionally defined by IL-10 expression. J Immunol 188(7):3127–3137. doi: 10.4049/jimmunol.1103433 PubMedPubMedCentralGoogle Scholar
  32. 32.
    Cedeno-Laurent F, Barthel SR, Opperman MJ, Lee DM, Clark RA, Dimitroff CJ (2010) Development of a nascent galectin-1 chimeric molecule for studying the role of leukocyte galectin-1 ligands and immune disease modulation. J Immunol 185(8):4659–4672. doi: 10.4049/jimmunol.1000715 PubMedPubMedCentralGoogle Scholar
  33. 33.
    Garin MI, Chu CC, Golshayan D, Cernuda-Morollon E, Wait R, Lechler RI (2006) Galectin-1: a key effector of regulation mediated by CD4 + CD25+ T cells. Blood 109(5):2058–2065PubMedGoogle Scholar
  34. 34.
    Juszczynski P, Ouyang J, Monti S, Rodig SJ, Takeyama K, Abramson J, Chen W, Kutok JL, Rabinovich GA, Shipp MA (2007) The AP1-dependent secretion of galectin-1 by Reed Sternberg cells fosters immune privilege in classical Hodgkin lymphoma. Proc Natl Acad Sci U S A 104(32):13134–13139. doi: 10.1073/pnas.0706017104 PubMedPubMedCentralGoogle Scholar
  35. 35.
    Stritesky GL, Yeh N, Kaplan MH (2008) IL-23 promotes maintenance but not commitment to the Th17 lineage. J Immunol 181(9):5948–5955, 181/9/5948 [pii]PubMedPubMedCentralGoogle Scholar
  36. 36.
    Sonderegger I, Iezzi G, Maier R, Schmitz N, Kurrer M, Kopf M (2008) GM-CSF mediates autoimmunity by enhancing IL-6-dependent Th17 cell development and survival. J Exp Med 205(10):2281–2294. doi: 10.1084/jem.20071119, jem.20071119 [pii]PubMedPubMedCentralGoogle Scholar
  37. 37.
    Chung CD, Patel VP, Moran M, Lewis LA, Miceli MC (2000) Galectin-1 induces partial TCR zeta-chain phosphorylation and antagonizes processive TCR signal transduction. J Immunol 165(7):3722–3729PubMedGoogle Scholar
  38. 38.
    Liu SD, Whiting CC, Tomassian T, Pang M, Bissel SJ, Baum LG, Mossine VV, Poirier F, Huflejt ME, Miceli MC (2008) Endogenous galectin-1 enforces class I-restricted TCR functional fate decisions in thymocytes. Blood 112(1):120–130. doi: 10.1182/blood-2007-09-114181, blood-2007-09-114181 [pii]PubMedPubMedCentralGoogle Scholar
  39. 39.
    Endharti AT, Zhou YW, Nakashima I, Suzuki H (2005) Galectin-1 supports survival of naive T cells without promoting cell proliferation. Eur J Immunol 35(1):86–97PubMedGoogle Scholar
  40. 40.
    Tribulatti MV, Figini MG, Carabelli J, Cattaneo V, Campetella O (2012) Redundant and antagonistic functions of galectin-1, -3, and -8 in the elicitation of T cell responses. J Immunol 188(7):2991–2999. doi: 10.4049/jimmunol.1102182 PubMedGoogle Scholar
  41. 41.
    Fukumori T, Takenaka Y, Yoshii T, Kim HR, Hogan V, Inohara H, Kagawa S, Raz A (2003) CD29 and CD7 mediate galectin-3-induced type II T-cell apoptosis. Cancer Res 63(23):8302–8311PubMedGoogle Scholar
  42. 42.
    Zhu C, Anderson AC, Schubart A, Xiong H, Imitola J, Khoury SJ, Zheng XX, Strom TB, Kuchroo VK (2005) The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat Immunol 6(12):1245–1252PubMedGoogle Scholar
  43. 43.
    Kashio Y, Nakamura K, Abedin MJ, Seki M, Nishi N, Yoshida N, Nakamura T, Hirashima M (2003) Galectin-9 induces apoptosis through the calcium-calpain-caspase-1 pathway. J Immunol 170(7):3631–3636PubMedGoogle Scholar
  44. 44.
    Tribulatti MV, Mucci J, Cattaneo V, Aguero F, Gilmartin T, Head SR, Campetella O (2007) Galectin-8 induces apoptosis in the CD4(high)CD8(high) thymocyte subpopulation. Glycobiology 17(12):1404–1412PubMedGoogle Scholar
  45. 45.
    Eshkar Sebban L, Ronen D, Levartovsky D, Elkayam O, Caspi D, Aamar S, Amital H, Rubinow A, Golan I, Naor D, Zick Y, Golan I (2007) The involvement of CD44 and its novel ligand galectin-8 in apoptotic regulation of autoimmune inflammation. J Immunol 179(2):1225–1235PubMedGoogle Scholar
  46. 46.
    Stillman BN, Hsu DK, Pang M, Brewer CF, Johnson P, Liu FT, Baum LG (2006) Galectin-3 and galectin-1 bind distinct cell surface glycoprotein receptors to induce T cell death. J Immunol 176(2):778–789PubMedGoogle Scholar
  47. 47.
    Bi S, Earl LA, Jacobs L, Baum LG (2008) Structural features of galectin-9 and galectin-1 that determine distinct T cell death pathways. J Biol Chem 283(18):12248–12258. doi: 10.1074/jbc.M800523200 PubMedPubMedCentralGoogle Scholar
  48. 48.
    Demetriou M, Granovsky M, Quaggin S, Dennis JW (2001) Negative regulation of T-cell activation and autoimmunity by Mgat5 N-glycosylation. Nature 409(6821):733–739. doi: 10.1038/35055582 PubMedGoogle Scholar
  49. 49.
    Demotte N, Stroobant V, Courtoy PJ, Van Der Smissen P, Colau D, Luescher IF, Hivroz C, Nicaise J, Squifflet JL, Mourad M, Godelaine D, Boon T, van der Bruggen P (2008) Restoring the association of the T cell receptor with CD8 reverses anergy in human tumor-infiltrating lymphocytes. Immunity 28(3):414–424. doi: 10.1016/j.immuni.2008.01.011, S1074-7613(08)00070-8 [pii]PubMedGoogle Scholar
  50. 50.
    Sturm A, Lensch M, Andre S, Kaltner H, Wiedenmann B, Rosewicz S, Dignass AU, Gabius HJ (2004) Human galectin-2: novel inducer of T cell apoptosis with distinct profile of caspase activation. J Immunol 173(6):3825–3837PubMedGoogle Scholar
  51. 51.
    Kubach J, Lutter P, Bopp T, Stoll S, Becker C, Huter E, Richter C, Weingarten P, Warger T, Knop J, Mullner S, Wijdenes J, Schild H, Schmitt E, Jonuleit H (2007) Human CD4 + CD25+ regulatory T cells: proteome analysis identifies galectin-10 as a novel marker essential for their anergy and suppressive function. Blood 110(5):1550–1558PubMedGoogle Scholar
  52. 52.
    Hokama A, Mizoguchi E, Sugimoto K, Shimomura Y, Tanaka Y, Yoshida M, Rietdijk ST, de Jong YP, Snapper SB, Terhorst C, Blumberg RS, Mizoguchi A (2004) Induced reactivity of intestinal CD4(+) T cells with an epithelial cell lectin, galectin-4, contributes to exacerbation of intestinal inflammation. Immunity 20(6):681–693PubMedGoogle Scholar
  53. 53.
    Nishida A, Nagahama K, Imaeda H, Ogawa A, Lau CW, Kobayashi T, Hisamatsu T, Preffer FI, Mizoguchi E, Ikeuchi H, Hibi T, Fukuda M, Andoh A, Blumberg RS, Mizoguchi A (2012) Inducible colitis-associated glycome capable of stimulating the proliferation of memory CD4+ T cells. J Exp Med 209(13):2383–2394. doi: 10.1084/jem.20112631 PubMedPubMedCentralGoogle Scholar
  54. 54.
    Cortegano I, del Pozo V, Cardaba B, de Andres B, Gallardo S, del Amo A, Arrieta I, Jurado A, Palomino P, Liu FT, Lahoz C (1998) Galectin-3 down-regulates IL-5 gene expression on different cell types. J Immunol 161(1):385–389PubMedGoogle Scholar
  55. 55.
    Norambuena A, Metz C, Vicuna L, Silva A, Pardo E, Oyanadel C, Massardo L, Gonzalez A, Soza A (2009) Galectin-8 induces apoptosis in Jurkat T cells by phosphatidic acid-mediated ERK1/2 activation supported by protein kinase A down-regulation. J Biol Chem 284(19):12670–12679. doi: 10.1074/jbc.M808949200 PubMedPubMedCentralGoogle Scholar
  56. 56.
    Gauthier L, Rossi B, Roux F, Termine E, Schiff C (2002) 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 99(20):13014–13019. doi: 10.1073/pnas.202323999 PubMedPubMedCentralGoogle Scholar
  57. 57.
    Rossi B, Espeli M, Schiff C, Gauthier L (2006) Clustering of pre-B cell integrins induces galectin-1-dependent pre-B cell receptor relocalization and activation. J Immunol 177(2):796–803PubMedGoogle Scholar
  58. 58.
    Elantak L, Espeli M, Boned A, Bornet O, Bonzi J, Gauthier L, Feracci M, Roche P, Guerlesquin F, Schiff C (2012) Structural basis for galectin-1-dependent pre-B cell receptor (pre-BCR) activation. J Biol Chem 287(53):44703–44713. doi: 10.1074/jbc.M112.395152 PubMedPubMedCentralGoogle Scholar
  59. 59.
    Espeli M, Mancini SJ, Breton C, Poirier F, Schiff C (2009) Impaired B-cell development at the pre-BII-cell stage in galectin-1-deficient mice due to inefficient pre-BII/stromal cell interactions. Blood 113(23):5878–5886. doi: 10.1182/blood-2009-01-198465 PubMedGoogle Scholar
  60. 60.
    Mourcin F, Breton C, Tellier J, Narang P, Chasson L, Jorquera A, Coles M, Schiff C, Mancini SJ (2011) Galectin-1-expressing stromal cells constitute a specific niche for pre-BII cell development in mouse bone marrow. Blood 117(24):6552–6561. doi: 10.1182/blood-2010-12-323113 PubMedGoogle Scholar
  61. 61.
    Anginot A, Espeli M, Chasson L, Mancini SJ, Schiff C (2013) Galectin 1 modulates plasma cell homeostasis and regulates the humoral immune response. J Immunol 190(11):5526–5533. doi: 10.4049/jimmunol.1201885 PubMedPubMedCentralGoogle Scholar
  62. 62.
    Tsai CM, Chiu YK, Hsu TL, Lin IY, Hsieh SL, Lin KI (2008) Galectin-1 promotes immunoglobulin production during plasma cell differentiation. J Immunol 181(7):4570–4579PubMedGoogle Scholar
  63. 63.
    Tsai CM, Guan CH, Hsieh HW, Hsu TL, Tu Z, Wu KJ, Lin CH, Lin KI (2011) Galectin-1 and galectin-8 have redundant roles in promoting plasma cell formation. J Immunol 187(4):1643–1652. doi: 10.4049/jimmunol.1100297 PubMedGoogle Scholar
  64. 64.
    Acosta-Rodriguez EV, Montes CL, Motran CC, Zuniga EI, Liu FT, Rabinovich GA, Gruppi A (2004) Galectin-3 mediates IL-4-induced survival and differentiation of B cells: functional cross-talk and implications during Trypanosoma cruzi infection. J Immunol 172(1):493–502PubMedGoogle Scholar
  65. 65.
    Karimi K, Arck PC (2010) Natural Killer cells: keepers of pregnancy in the turnstile of the environment. Brain Behav Immun 24(3):339–347. doi: 10.1016/j.bbi.2009.09.015 PubMedGoogle Scholar
  66. 66.
    Koopman LA, Kopcow HD, Rybalov B, Boyson JE, Orange JS, Schatz F, Masch R, Lockwood CJ, Schachter AD, Park PJ, Strominger JL (2003) Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J Exp Med 198(8):1201–1212. doi: 10.1084/jem.20030305 PubMedPubMedCentralGoogle Scholar
  67. 67.
    Molvarec A, Blois SM, Stenczer B, Toldi G, Tirado-Gonzalez I, Ito M, Shima T, Yoneda S, Vasarhelyi B, Rigo J Jr, Saito S (2011) Peripheral blood galectin-1-expressing T and natural killer cells in normal pregnancy and preeclampsia. Clin Immunol 139(1):48–56. doi: 10.1016/j.clim.2010.12.018 PubMedGoogle Scholar
  68. 68.
    Tsuboi S, Sutoh M, Hatakeyama S, Hiraoka N, Habuchi T, Horikawa Y, Hashimoto Y, Yoneyama T, Mori K, Koie T, Nakamura T, Saitoh H, Yamaya K, Funyu T, Fukuda M, Ohyama C (2011) A novel strategy for evasion of NK cell immunity by tumours expressing core2 O-glycans. EMBO J 30(15):3173–3185. doi: 10.1038/emboj.2011.215 PubMedPubMedCentralGoogle Scholar
  69. 69.
    Suzuki Y, Sutoh M, Hatakeyama S, Mori K, Yamamoto H, Koie T, Saitoh H, Yamaya K, Funyu T, Habuchi T, Arai Y, Fukuda M, Ohyama C, Tsuboi S (2012) MUC1 carrying core 2 O-glycans functions as a molecular shield against NK cell attack, promoting bladder tumor metastasis. Int J Oncol 40(6):1831–1838. doi: 10.3892/ijo.2012.1411 PubMedPubMedCentralGoogle Scholar
  70. 70.
    Jost S, Moreno-Nieves UY, Garcia-Beltran WF, Rands K, Reardon J, Toth I, Piechocka-Trocha A, Altfeld M, Addo MM (2013) Dysregulated Tim-3 expression on natural killer cells is associated with increased Galectin-9 levels in HIV-1 infection. Retrovirology 10(1):74. doi: 10.1186/1742-4690-10-74 PubMedPubMedCentralGoogle Scholar
  71. 71.
    Golden-Mason L, McMahan RH, Strong M, Reisdorph R, Mahaffey S, Palmer BE, Cheng L, Kulesza C, Hirashima M, Niki T, Rosen HR (2013) Galectin-9 functionally impairs natural killer cells in humans and mice. J Virol 87(9):4835–4845. doi: 10.1128/JVI.01085-12 PubMedPubMedCentralGoogle Scholar
  72. 72.
    Tang ZH, Liang S, Potter J, Jiang X, Mao HQ, Li Z (2013) Tim-3/galectin-9 regulate the homeostasis of hepatic NKT cells in a murine model of nonalcoholic fatty liver disease. J Immunol 190(4):1788–1796. doi: 10.4049/jimmunol.1202814 PubMedPubMedCentralGoogle Scholar
  73. 73.
    Miko E, Meggyes M, Bogar B, Schmitz N, Barakonyi A, Varnagy A, Farkas B, Tamas P, Bodis J, Szekeres-Bartho J, Illes Z, Szereday L (2013) Involvement of galectin-9/TIM-3 pathway in the systemic inflammatory response in early-onset preeclampsia. PLoS One 8(8):e71811. doi: 10.1371/journal.pone.0071811 PubMedPubMedCentralGoogle Scholar
  74. 74.
    Medzhitov R, Janeway CA Jr (1997) Innate immunity: impact on the adaptive immune response. Curr Opin Immunol 9(1):4–9PubMedGoogle Scholar
  75. 75.
    Karlsson A, Christenson K, Matlak M, Bjorstad A, Brown KL, Telemo E, Salomonsson E, Leffler H, Bylund J (2009) Galectin-3 functions as an opsonin and enhances the macrophage clearance of apoptotic neutrophils. Glycobiology 19(1):16–20PubMedGoogle Scholar
  76. 76.
    Rotshenker S, Reichert F, Gitik M, Haklai R, Elad-Sfadia G, Kloog Y (2008) Galectin-3/MAC-2, Ras and PI3K activate complement receptor-3 and scavenger receptor-AI/II mediated myelin phagocytosis in microglia. Glia 56(15):1607–1613. doi: 10.1002/glia.20713 PubMedGoogle Scholar
  77. 77.
    MacKinnon AC, Farnworth SL, Hodkinson PS, Henderson NC, Atkinson KM, Leffler H, Nilsson UJ, Haslett C, Forbes SJ, Sethi T (2008) Regulation of alternative macrophage activation by galectin-3. J Immunol 180(4):2650–2658PubMedGoogle Scholar
  78. 78.
    Papaspyridonos M, McNeill E, de Bono JP, Smith A, Burnand KG, Channon KM, Greaves DR (2008) Galectin-3 is an amplifier of inflammation in atherosclerotic plaque progression through macrophage activation and monocyte chemoattraction. Arterioscler Thromb Vasc Biol 28(3):433–440. doi: 10.1161/ATVBAHA.107.159160 PubMedGoogle Scholar
  79. 79.
    Sano H, Hsu DK, Apgar JR, Yu L, Sharma BB, Kuwabara I, Izui S, Liu FT (2003) Critical role of galectin-3 in phagocytosis by macrophages. J Clin Invest 112(3):389–397. doi: 10.1172/JCI17592 PubMedPubMedCentralGoogle Scholar
  80. 80.
    Ho MK, Springer TA (1982) Mac-2, a novel 32,000 Mr mouse macrophage subpopulation-specific antigen defined by monoclonal antibodies. J Immunol 128(3):1221–1228PubMedGoogle Scholar
  81. 81.
    Vaitaitis GM, Wagner DH Jr (2012) Galectin-9 controls CD40 signaling through a Tim-3 independent mechanism and redirects the cytokine profile of pathogenic T cells in autoimmunity. PLoS One 7(6):e38708. doi: 10.1371/journal.pone.0038708 PubMedPubMedCentralGoogle Scholar
  82. 82.
    Blois SM, Ilarregui JM, Tometten M, Garcia M, Orsal AS, Cordo-Russo R, Toscano MA, Bianco GA, Kobelt P, Handjiski B, Tirado I, Markert UR, Klapp BF, Poirier F, Szekeres-Bartho J, Rabinovich GA, Arck PC (2007) A pivotal role for galectin-1 in fetomaternal tolerance. Nat Med 13(12):1450–1457. doi: 10.1038/nm1680 PubMedGoogle Scholar
  83. 83.
    Barrionuevo P, Beigier-Bompadre M, Ilarregui JM, Toscano MA, Bianco GA, Isturiz MA, Rabinovich GA (2007) 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 178(1):436–445PubMedGoogle Scholar
  84. 84.
    Kojima K, Arikawa T, Saita N, Goto E, Tsumura S, Tanaka R, Masunaga A, Niki T, Oomizu S, Hirashima M, Kohrogi H (2011) Galectin-9 attenuates acute lung injury by expanding CD14- plasmacytoid dendritic cell-like macrophages. Am J Respir Crit Care Med 184(3):328–339. doi: 10.1164/rccm.201010-1566OC PubMedGoogle Scholar
  85. 85.
    de la Fuente H, Perez-Gala S, Bonay P, Cruz-Adalia A, Cibrian D, Sanchez-Cuellar S, Dauden E, Fresno M, Garcia-Diez A, Sanchez-Madrid F (2012) Psoriasis in humans is associated with down-regulation of galectins in dendritic cells. J Pathol 228(2):193–203. doi: 10.1002/path.3996 PubMedGoogle Scholar
  86. 86.
    Nishi Y, Sano H, Kawashima T, Okada T, Kuroda T, Kikkawa K, Kawashima S, Tanabe M, Goto T, Matsuzawa Y, Matsumura R, Tomioka H, Liu FT, Shirai K (2007) Role of galectin-3 in human pulmonary fibrosis. Allergol Int 56(1):57–65. doi: 10.2332/allergolint.O-06-449 PubMedGoogle Scholar
  87. 87.
    Iacobini C, Menini S, Ricci C, Blasetti Fantauzzi C, Scipioni A, Salvi L, Cordone S, Delucchi F, Serino M, Federici M, Pricci F, Pugliese G (2011) Galectin-3 ablation protects mice from diet-induced NASH: a major scavenging role for galectin-3 in liver. J Hepatol 54(5):975–983. doi: 10.1016/j.jhep.2010.09.020 PubMedGoogle Scholar
  88. 88.
    Jiang HR, Al Rasebi Z, Mensah-Brown E, Shahin A, Xu D, Goodyear CS, Fukada SY, Liu FT, Liew FY, Lukic ML (2009) Galectin-3 deficiency reduces the severity of experimental autoimmune encephalomyelitis. J Immunol 182(2):1167–1173PubMedGoogle Scholar
  89. 89.
    Volarevic V, Milovanovic M, Ljujic B, Pejnovic N, Arsenijevic N, Nilsson U, Leffler H, Lukic ML (2012) Galectin-3 deficiency prevents concanavalin A-induced hepatitis in mice. Hepatology 55(6):1954–1964. doi: 10.1002/hep.25542 PubMedGoogle Scholar
  90. 90.
    Fernandes Bertocchi AP, Campanhole G, Wang PH, Goncalves GM, Damiao MJ, Cenedeze MA, Beraldo FC, de Paula Antunes Teixeira V, Dos Reis MA, Mazzali M, Pacheco-Silva A, Camara NO (2008) A Role for galectin-3 in renal tissue damage triggered by ischemia and reperfusion injury. Transpl Int 21(10):999–1007. doi: 10.1111/j.1432-2277.2008.00705.x PubMedGoogle Scholar
  91. 91.
    Wu SY, Yu JS, Liu FT, Miaw SC, Wu-Hsieh BA (2013) Galectin-3 negatively regulates dendritic cell production of IL-23/IL-17-axis cytokines in infection by Histoplasma capsulatum. J Immunol 190(7):3427–3437. doi: 10.4049/jimmunol.1202122 PubMedGoogle Scholar
  92. 92.
    Nobumoto A, Oomizu S, Arikawa T, Katoh S, Nagahara K, Miyake M, Nishi N, Takeshita K, Niki T, Yamauchi A, Hirashima M (2009) Galectin-9 expands unique macrophages exhibiting plasmacytoid dendritic cell-like phenotypes that activate NK cells in tumor-bearing mice. Clin Immunol 130(3):322–330. doi: 10.1016/j.clim.2008.09.014 PubMedGoogle Scholar
  93. 93.
    Feuk-Lagerstedt E, Jordan ET, Leffler H, Dahlgren C, Karlsson A (1999) Identification of CD66a and CD66b as the major galectin-3 receptor candidates in human neutrophils. J Immunol 163(10):5592–5598PubMedGoogle Scholar
  94. 94.
    Karlsson A, Follin P, Leffler H, Dahlgren C (1998) Galectin-3 activates the NADPH-oxidase in exudated but not peripheral blood neutrophils. Blood 91(9):3430–3438PubMedGoogle Scholar
  95. 95.
    Dias-Baruffi M, Zhu H, Cho M, Karmakar S, McEver RP, Cummings RD (2003) Dimeric galectin-1 induces surface exposure of phosphatidylserine and phagocytic recognition of leukocytes without inducing apoptosis. J Biol Chem 278(42):41282–41293PubMedGoogle Scholar
  96. 96.
    Stowell SR, Karmakar S, Stowell CJ, Dias-Baruffi M, McEver RP, Cummings RD (2007) Human galectin-1, -2, and -4 induce surface exposure of phosphatidylserine in activated human neutrophils but not in activated T cells. Blood 109(1):219–227PubMedPubMedCentralGoogle Scholar
  97. 97.
    Stowell SR, Karmakar S, Arthur CM, Ju T, Rodrigues LC, Riul TB, Dias-Baruffi M, Miner J, McEver RP, Cummings RD (2009) Galectin-1 induces reversible phosphatidylserine exposure at the plasma membrane. Mol Biol Cell 20(5):1408–1418PubMedPubMedCentralGoogle Scholar
  98. 98.
    Lagasse E, Weissman IL (1994) bcl-2 inhibits apoptosis of neutrophils but not their engulfment by macrophages. J Exp Med 179(3):1047–1052PubMedGoogle Scholar
  99. 99.
    Stowell SR, Arthur CM, Mehta P, Slanina KA, Blixt O, Leffler H, Smith DF, Cummings RD (2008) Galectin-1, -2, and -3 exhibit differential recognition of sialylated glycans and blood group antigens. J Biol Chem 283(15):10109–10123. doi: 10.1074/jbc.M709545200 PubMedPubMedCentralGoogle Scholar
  100. 100.
    Stowell SR, Arthur CM, Slanina KA, Horton JR, Smith DF, Cummings RD (2008) Dimeric Galectin-8 induces phosphatidylserine exposure in leukocytes through polylactosamine recognition by the C-terminal domain. J Biol Chem 283(29):20547–20559PubMedPubMedCentralGoogle Scholar
  101. 101.
    Leonidas DD, Elbert BL, Zhou Z, Leffler H, Ackerman SJ, Acharya KR (1995) Crystal structure of human Charcot-Leyden crystal protein, an eosinophil lysophospholipase, identifies it as a new member of the carbohydrate-binding family of galectins. Structure 3(12):1379–1393PubMedGoogle Scholar
  102. 102.
    Ackerman SJ, Corrette SE, Rosenberg HF, Bennett JC, Mastrianni DM, Nicholson-Weller A, Weller PF, Chin DT, Tenen DG (1993) Molecular cloning and characterization of human eosinophil Charcot-Leyden crystal protein (lysophospholipase). Similarities to IgE binding proteins and the S-type animal lectin superfamily. J Immunol 150(2):456–468PubMedGoogle Scholar
  103. 103.
    Hirashima M, Ueno M, Kamiya K, Higuchi S, Matsumoto R (1991) Functional heterogeneity of human eosinophil chemotactic lymphokines. Lymphokine Cytokine Res 10(6):481–486PubMedGoogle Scholar
  104. 104.
    Matsumoto R, Matsumoto H, Seki M, Hata M, Asano Y, Kanegasaki S, Stevens RL, Hirashima M (1998) Human ecalectin, a variant of human galectin-9, is a novel eosinophil chemoattractant produced by T lymphocytes. J Biol Chem 273(27):16976–16984PubMedGoogle Scholar
  105. 105.
    Asakura H, Kashio Y, Nakamura K, Seki M, Dai S, Shirato Y, Abedin MJ, Yoshida N, Nishi N, Imaizumi T, Saita N, Toyama Y, Takashima H, Nakamura T, Ohkawa M, Hirashima M (2002) Selective eosinophil adhesion to fibroblast via IFN-gamma-induced galectin-9. J Immunol 169(10):5912–5918PubMedGoogle Scholar
  106. 106.
    Saita N, Goto E, Yamamoto T, Cho I, Tsumori K, Kohrogi H, Maruo K, Ono T, Takeya M, Kashio Y, Nakamura K, Hirashima M (2002) Association of galectin-9 with eosinophil apoptosis. Int Arch Allergy Immunol 128(1):42–50, 58002PubMedGoogle Scholar
  107. 107.
    Imaizumi T, Kumagai M, Sasaki N, Kurotaki H, Mori F, Seki M, Nishi N, Fujimoto K, Tanji K, Shibata T, Tamo W, Matsumiya T, Yoshida H, Cui XF, Takanashi S, Hanada K, Okumura K, Yagihashi S, Wakabayashi K, Nakamura T, Hirashima M, Satoh K (2002) Interferon-gamma stimulates the expression of galectin-9 in cultured human endothelial cells. J Leukoc Biol 72(3):486–491PubMedGoogle Scholar
  108. 108.
    Laing JG, Robertson MW, Gritzmacher CA, Wang JL, Liu FT (1989) Biochemical and immunological comparisons of carbohydrate-binding protein 35 and an IgE-binding protein. J Biol Chem 264(4):1097–1110PubMedGoogle Scholar
  109. 109.
    Gritzmacher CA, Robertson MW, Liu FT (1988) IgE-binding protein. Subcellular location and gene expression in many murine tissues and cells. J Immunol 141(8):2801–2806PubMedGoogle Scholar
  110. 110.
    Robertson MW, Albrandt K, Keller D, Liu FT (1990) Human IgE-binding protein: a soluble lectin exhibiting a highly conserved interspecies sequence and differential recognition of IgE glycoforms. Biochemistry 29(35):8093–8100PubMedGoogle Scholar
  111. 111.
    Frigeri LG, Zuberi RI, Liu FT (1993) Epsilon BP, a beta-galactoside-binding animal lectin, recognizes IgE receptor (Fc epsilon RI) and activates mast cells. Biochemistry 32(30):7644–7649PubMedGoogle Scholar
  112. 112.
    Chen HY, Sharma BB, Yu L, Zuberi R, Weng IC, Kawakami Y, Kawakami T, Hsu DK, Liu FT (2006) Role of galectin-3 in mast cell functions: galectin-3-deficient mast cells exhibit impaired mediator release and defective JNK expression. J Immunol 177(8):4991–4997PubMedGoogle Scholar
  113. 113.
    Suzuki Y, Inoue T, Yoshimaru T, Ra C (2008) Galectin-3 but not galectin-1 induces mast cell death by oxidative stress and mitochondrial permeability transition. Biochim Biophys Acta 1783(5):924–934. doi: 10.1016/j.bbamcr.2008.01.025 PubMedGoogle Scholar
  114. 114.
    Rabinovich GA, Sotomayor CE, Riera CM, Bianco I, Correa SG (2000) Evidence of a role for galectin-1 in acute inflammation. Eur J Immunol 30(5):1331–1339. doi: 10.1002/(SICI)1521-4141(200005)30:5<1331::AID-IMMU1331>3.0.CO;2-H PubMedGoogle Scholar
  115. 115.
    Kolev M, Le Friec G, Kemper C (2013) The role of complement in CD4(+) T cell homeostasis and effector functions. Semin Immunol 25(1):12–19. doi: 10.1016/j.smim.2013.04.012 PubMedGoogle Scholar
  116. 116.
    Romaniuk MA, Croci DO, Lapponi MJ, Tribulatti MV, Negrotto S, Poirier F, Campetella O, Rabinovich GA, Schattner M (2012) Binding of galectin-1 to alphaIIbbeta(3) integrin triggers “outside-in” signals, stimulates platelet activation, and controls primary hemostasis. FASEB J 26(7):2788–2798. doi: 10.1096/fj.11-197541 PubMedGoogle Scholar
  117. 117.
    Pacienza N, Pozner RG, Bianco GA, D’Atri LP, Croci DO, Negrotto S, Malaver E, Gomez RM, Rabinovich GA, Schattner M (2008) The immunoregulatory glycan-binding protein galectin-1 triggers human platelet activation. FASEB J 22(4):1113–1123. doi: 10.1096/fj.07-9524com PubMedGoogle Scholar
  118. 118.
    Romaniuk MA, Tribulatti MV, Cattaneo V, Lapponi MJ, Molinas FC, Campetella O, Schattner M (2010) Human platelets express and are activated by galectin-8. Biochem J 432(3):535–547. doi: 10.1042/BJ20100538 PubMedGoogle Scholar
  119. 119.
    Zappelli C, van der Zwaan C, Thijssen-Timmer DC, Mertens K, Meijer AB (2012) Novel role for galectin-8 protein as mediator of coagulation factor V endocytosis by megakaryocytes. J Biol Chem 287(11):8327–8335. doi: 10.1074/jbc.M111.305151 PubMedPubMedCentralGoogle Scholar
  120. 120.
    Saint-Lu N, Oortwijn BD, Pegon JN, Odouard S, Christophe OD, de Groot PG, Denis CV, Lenting PJ (2012) Identification of galectin-1 and galectin-3 as novel partners for von Willebrand factor. Arterioscler Thromb Vasc Biol 32(4):894–901. doi: 10.1161/ATVBAHA.111.240309 PubMedGoogle Scholar
  121. 121.
    Cao Z, Said N, Amin S, Wu HK, Bruce A, Garate M, Hsu DK, Kuwabara I, Liu FT, Panjwani N (2002) Galectins-3 and -7, but not galectin-1, play a role in re-epithelialization of wounds. J Biol Chem 277(44):42299–42305. doi: 10.1074/jbc.M200981200 PubMedGoogle Scholar
  122. 122.
    Cao Z, Said N, Wu HK, Kuwabara I, Liu FT, Panjwani N (2003) Galectin-7 as a potential mediator of corneal epithelial cell migration. Arch Ophthalmol 121(1):82–86PubMedGoogle Scholar
  123. 123.
    Gendronneau G, Sidhu SS, Delacour D, Dang T, Calonne C, Houzelstein D, Magnaldo T, Poirier F (2008) Galectin-7 in the control of epidermal homeostasis after injury. Mol Biol Cell 19(12):5541–5549. doi: 10.1091/mbc.E08-02-0166 PubMedPubMedCentralGoogle Scholar
  124. 124.
    Watt DJ, Jones GE, Goldring K (2004) The involvement of galectin-1 in skeletal muscle determination, differentiation and regeneration. Glycoconj J 19(7–9):615–619. doi: 10.1023/B:GLYC.0000014093.23509.92 PubMedGoogle Scholar
  125. 125.
    Georgiadis V, Stewart HJ, Pollard HJ, Tavsanoglu Y, Prasad R, Horwood J, Deltour L, Goldring K, Poirier F, Lawrence-Watt DJ (2007) Lack of galectin-1 results in defects in myoblast fusion and muscle regeneration. Dev Dyn 236(4):1014–1024. doi: 10.1002/dvdy.21123 PubMedGoogle Scholar
  126. 126.
    Dias-Baruffi M, Stowell SR, Song SC, Arthur CM, Cho M, Rodrigues LC, Montes MA, Rossi MA, James JA, McEver RP, Cummings RD (2010) Differential expression of immunomodulatory galectin-1 in peripheral leukocytes and adult tissues and its cytosolic organization in striated muscle. Glycobiology 20(5):507–520. doi: 10.1093/glycob/cwp203 PubMedPubMedCentralGoogle Scholar
  127. 127.
    Cerri DG, Rodrigues LC, Stowell SR, Araujo DD, Coelho MC, Oliveira SR, Bizario JC, Cummings RD, Dias-Baruffi M, Costa MC (2008) Degeneration of dystrophic or injured skeletal muscles induces high expression of Galectin-1. Glycobiology 18(11):842–850PubMedGoogle Scholar
  128. 128.
    Ahmed H, Du SJ, Vasta GR (2009) Knockdown of a galectin-1-like protein in zebrafish (Danio rerio) causes defects in skeletal muscle development. Glycoconj J 26(3):277–283. doi: 10.1007/s10719-008-9178-9 PubMedGoogle Scholar
  129. 129.
    Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275(5302):964–967PubMedGoogle Scholar
  130. 130.
    Ishikawa A, Imaizumi T, Yoshida H, Nishi N, Nakamura T, Hirashima M, Satoh K (2004) Double-stranded RNA enhances the expression of galectin-9 in vascular endothelial cells. Immunol Cell Biol 82(4):410–414. doi: 10.1111/j.0818-9641.2004.01248.x PubMedGoogle Scholar
  131. 131.
    Cooper D, Norling LV, Perretti M (2008) Novel insights into the inhibitory effects of Galectin-1 on neutrophil recruitment under flow. J Leukoc Biol 83(6):1459–1466. doi: 10.1189/jlb.1207831 PubMedGoogle Scholar
  132. 132.
    Norling LV, Sampaio AL, Cooper D, Perretti M (2008) Inhibitory control of endothelial galectin-1 on in vitro and in vivo lymphocyte trafficking. FASEB J 22(3):682–690. doi: 10.1096/fj.07-9268com PubMedGoogle Scholar
  133. 133.
    Nieminen J, St-Pierre C, Bhaumik P, Poirier F, Sato S (2008) Role of galectin-3 in leukocyte recruitment in a murine model of lung infection by Streptococcus pneumoniae. J Immunol 180(4):2466–2473PubMedGoogle Scholar
  134. 134.
    Cooper D, Iqbal AJ, Gittens BR, Cervone C, Perretti M (2012) The effect of galectins on leukocyte trafficking in inflammation: sweet or sour? Ann N Y Acad Sci 1253:181–192. doi: 10.1111/j.1749-6632.2011.06291.x PubMedGoogle Scholar
  135. 135.
    Thijssen VL, Poirier F, Baum LG, Griffioen AW (2007) Galectins in the tumor endothelium: opportunities for combined cancer therapy. Blood 110(8):2819–2827. doi: 10.1182/blood-2007-03-077792 PubMedGoogle Scholar
  136. 136.
    Thijssen VL, Postel R, Brandwijk RJ, Dings RP, Nesmelova I, Satijn S, Verhofstad N, Nakabeppu Y, Baum LG, Bakkers J, Mayo KH, Poirier F, Griffioen AW (2006) Galectin-1 is essential in tumor angiogenesis and is a target for antiangiogenesis therapy. Proc Natl Acad Sci U S A 103(43):15975–15980. doi: 10.1073/pnas.0603883103 PubMedPubMedCentralGoogle Scholar
  137. 137.
    Nangia-Makker P, Honjo Y, Sarvis R, Akahani S, Hogan V, Pienta KJ, Raz A (2000) Galectin-3 induces endothelial cell morphogenesis and angiogenesis. Am J Pathol 156(3):899–909. doi: 10.1016/S0002-9440(10)64959-0 PubMedPubMedCentralGoogle Scholar
  138. 138.
    Fukushi J, Makagiansar IT, Stallcup WB (2004) NG2 proteoglycan promotes endothelial cell motility and angiogenesis via engagement of galectin-3 and alpha3beta1 integrin. Mol Biol Cell 15(8):3580–3590. doi: 10.1091/mbc.E04-03-0236 PubMedPubMedCentralGoogle Scholar
  139. 139.
    D’Haene N, Sauvage S, Maris C, Adanja I, Le Mercier M, Decaestecker C, Baum L, Salmon I (2013) VEGFR1 and VEGFR2 involvement in extracellular galectin-1- and galectin-3-induced angiogenesis. PLoS One 8(6):e67029. doi: 10.1371/journal.pone.0067029 PubMedPubMedCentralGoogle Scholar
  140. 140.
    Freitag N, Tirado-Gonzalez I, Barrientos G, Herse F, Thijssen VL, Weedon-Fekjaer SM, Schulz H, Wallukat G, Klapp BF, Nevers T, Sharma S, Staff AC, Dechend R, Blois SM (2013) Interfering with Gal-1-mediated angiogenesis contributes to the pathogenesis of preeclampsia. Proc Natl Acad Sci U S A 110(28):11451–11456. doi: 10.1073/pnas.1303707110 PubMedPubMedCentralGoogle Scholar
  141. 141.
    Delgado VM, Nugnes LG, Colombo LL, Troncoso MF, Fernandez MM, Malchiodi EL, Frahm I, Croci DO, Compagno D, Rabinovich GA, Wolfenstein-Todel C, Elola MT (2011) Modulation of endothelial cell migration and angiogenesis: a novel function for the “tandem-repeat” lectin galectin-8. FASEB J 25(1):242–254. doi: 10.1096/fj.09-144907 PubMedGoogle Scholar
  142. 142.
    Jouve N, Despoix N, Espeli M, Gauthier L, Cypowyj S, Fallague K, Schiff C, Dignat-George F, Vely F, Leroyer AS (2013) The involvement of CD146 and its novel ligand Galectin-1 in apoptotic regulation of endothelial cells. J Biol Chem 288(4):2571–2579. doi: 10.1074/jbc.M112.418848 PubMedPubMedCentralGoogle Scholar
  143. 143.
    Barondes SH, Cooper DN, Gitt MA, Leffler H (1994) Galectins. Structure and function of a large family of animal lectins. J Biol Chem 269(33):20807–20810PubMedGoogle Scholar
  144. 144.
    Sato S, Hughes RC (1994) Regulation of secretion and surface expression of Mac-2, a galactoside-binding protein of macrophages. J Biol Chem 269(6):4424–4430PubMedGoogle Scholar
  145. 145.
    Cho M, Cummings RD (1995) Galectin-1, a beta-galactoside-binding lectin in Chinese hamster ovary cells. II. Localization and biosynthesis. J Biol Chem 270(10):5207–5212PubMedGoogle Scholar
  146. 146.
    Lindstedt R, Apodaca G, Barondes SH, Mostov KE, Leffler H (1993) Apical secretion of a cytosolic protein by Madin-Darby canine kidney cells. Evidence for polarized release of an endogenous lectin by a nonclassical secretory pathway. J Biol Chem 268(16):11750–11757PubMedGoogle Scholar
  147. 147.
    Liu FT, Patterson RJ, Wang JL (2002) Intracellular functions of galectins. Biochim Biophys Acta 1572(2–3):263–273PubMedGoogle Scholar
  148. 148.
    Shimura T, Takenaka Y, Tsutsumi S, Hogan V, Kikuchi A, Raz A (2004) Galectin-3, a novel binding partner of beta-catenin. Cancer Res 64(18):6363–6367. doi: 10.1158/0008-5472.CAN-04-1816 PubMedGoogle Scholar
  149. 149.
    Kim SJ, Choi IJ, Cheong TC, Lee SJ, Lotan R, Park SH, Chun KH (2010) Galectin-3 increases gastric cancer cell motility by up-regulating fascin-1 expression. Gastroenterology 138(3):1035–1045.e1031–1032. doi: 10.1053/j.gastro.2009.09.061 PubMedGoogle Scholar
  150. 150.
    Shalom-Feuerstein R, Cooks T, Raz A, Kloog Y (2005) Galectin-3 regulates a molecular switch from N-Ras to K-Ras usage in human breast carcinoma cells. Cancer Res 65(16):7292–7300. doi: 10.1158/0008-5472.CAN-05-0775 PubMedGoogle Scholar
  151. 151.
    Yoshii T, Fukumori T, Honjo Y, Inohara H, Kim HR, Raz A (2002) Galectin-3 phosphorylation is required for its anti-apoptotic function and cell cycle arrest. J Biol Chem 277(9):6852–6857. doi: 10.1074/jbc.M107668200 PubMedGoogle Scholar
  152. 152.
    Mazurek N, Conklin J, Byrd JC, Raz A, Bresalier RS (2000) Phosphorylation of the beta-galactoside-binding protein galectin-3 modulates binding to its ligands. J Biol Chem 275(46):36311–36315. doi: 10.1074/jbc.M003831200 PubMedGoogle Scholar
  153. 153.
    Oka N, Nakahara S, Takenaka Y, Fukumori T, Hogan V, Kanayama HO, Yanagawa T, Raz A (2005) Galectin-3 inhibits tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis by activating Akt in human bladder carcinoma cells. Cancer Res 65(17):7546–7553. doi: 10.1158/0008-5472.CAN-05-1197 PubMedGoogle Scholar
  154. 154.
    Lee YJ, Song YK, Song JJ, Siervo-Sassi RR, Kim HR, Li L, Spitz DR, Lokshin A, Kim JH (2003) Reconstitution of galectin-3 alters glutathione content and potentiates TRAIL-induced cytotoxicity by dephosphorylation of Akt. Exp Cell Res 288(1):21–34PubMedGoogle Scholar
  155. 155.
    Fukumori T, Takenaka Y, Oka N, Yoshii T, Hogan V, Inohara H, Kanayama HO, Kim HR, Raz A (2004) Endogenous galectin-3 determines the routing of CD95 apoptotic signaling pathways. Cancer Res 64(10):3376–3379. doi: 10.1158/0008-5472.CAN-04-0336 PubMedGoogle Scholar
  156. 156.
    Yang RY, Hsu DK, Liu FT (1996) Expression of galectin-3 modulates T-cell growth and apoptosis. Proc Natl Acad Sci U S A 93(13): 6737–6742PubMedPubMedCentralGoogle Scholar
  157. 157.
    Bernerd F, Sarasin A, Magnaldo T (1999) Galectin-7 overexpression is associated with the apoptotic process in UVB-induced sunburn keratinocytes. Proc Natl Acad Sci U S A 96(20):11329–11334PubMedPubMedCentralGoogle Scholar
  158. 158.
    Paz A, Haklai R, Elad-Sfadia G, Ballan E, Kloog Y (2001) Galectin-1 binds oncogenic H-Ras to mediate Ras membrane anchorage and cell transformation. Oncogene 20(51):7486–7493. doi: 10.1038/sj.onc.1204950 PubMedGoogle Scholar
  159. 159.
    Yang RY, Hsu DK, Yu L, Chen HY, Liu FT (2004) Galectin-12 is required for adipogenic signaling and adipocyte differentiation. J Biol Chem 279(28):29761–29766. doi: 10.1074/jbc.M401303200 PubMedGoogle Scholar
  160. 160.
    Yang RY, Yu L, Graham JL, Hsu DK, Lloyd KC, Havel PJ, Liu FT (2011) Ablation of a galectin preferentially expressed in adipocytes increases lipolysis, reduces adiposity, and improves insulin sensitivity in mice. Proc Natl Acad Sci U S A 108(46):18696–18701. doi: 10.1073/pnas.1109065108 PubMedPubMedCentralGoogle Scholar
  161. 161.
    Delacour D, Gouyer V, Zanetta JP, Drobecq H, Leteurtre E, Grard G, Moreau-Hannedouche O, Maes E, Pons A, Andre S, Le Bivic A, Gabius HJ, Manninen A, Simons K, Huet G (2005) Galectin-4 and sulfatides in apical membrane trafficking in enterocyte-like cells. J Cell Biol 169(3):491–501. doi: 10.1083/jcb.200407073 PubMedPubMedCentralGoogle Scholar
  162. 162.
    Delacour D, Cramm-Behrens CI, Drobecq H, Le Bivic A, Naim HY, Jacob R (2006) Requirement for galectin-3 in apical protein sorting. Curr Biol 16(4):408–414. doi: 10.1016/j.cub.2005.12.046 PubMedGoogle Scholar
  163. 163.
    Thurston TL, Wandel MP, von Muhlinen N, Foeglein A, Randow F (2012) Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature 482(7385):414–418. doi: 10.1038/nature10744 PubMedPubMedCentralGoogle Scholar
  164. 164.
    Vyakarnam A, Dagher SF, Wang JL, Patterson RJ (1997) Evidence for a role for galectin-1 in pre-mRNA splicing. Mol Cell Biol 17(8): 4730–4737PubMedPubMedCentralGoogle Scholar
  165. 165.
    Vyakarnam A, Lenneman AJ, Lakkides KM, Patterson RJ, Wang JL (1998) A comparative nuclear localization study of galectin-1 with other splicing components. Exp Cell Res 242(2):419–428. doi: 10.1006/excr.1998.4111 PubMedGoogle Scholar
  166. 166.
    Park JW, Voss PG, Grabski S, Wang JL, Patterson RJ (2001) Association of galectin-1 and galectin-3 with Gemin4 in complexes containing the SMN protein. Nucleic Acids Res 29(17):3595–3602PubMedPubMedCentralGoogle Scholar
  167. 167.
    Wang W, Park JW, Wang JL, Patterson RJ (2006) Immunoprecipitation of spliceosomal RNAs by antisera to galectin-1 and galectin-3. Nucleic Acids Res 34(18):5166–5174. doi: 10.1093/nar/gkl673 PubMedPubMedCentralGoogle Scholar
  168. 168.
    Paron I, Scaloni A, Pines A, Bachi A, Liu FT, Puppin C, Pandolfi M, Ledda L, Di Loreto C, Damante G, Tell G (2003) Nuclear localization of Galectin-3 in transformed thyroid cells: a role in transcriptional regulation. Biochem Biophys Res Commun 302(3):545–553PubMedGoogle Scholar
  169. 169.
    Nakahara S, Hogan V, Inohara H, Raz A (2006) Importin-mediated nuclear translocation of galectin-3. J Biol Chem 281(51):39649–39659. doi: 10.1074/jbc.M608069200 PubMedGoogle Scholar
  170. 170.
    Nakahara S, Oka N, Wang Y, Hogan V, Inohara H, Raz A (2006) Characterization of the nuclear import pathways of galectin-3. Cancer Res 66(20):9995–10006. doi: 10.1158/0008-5472.CAN-06-1772 PubMedGoogle Scholar
  171. 171.
    Takenaka Y, Fukumori T, Yoshii T, Oka N, Inohara H, Kim HR, Bresalier RS, Raz A (2004) Nuclear export of phosphorylated galectin-3 regulates its antiapoptotic activity in response to chemotherapeutic drugs. Mol Cell Biol 24(10):4395–4406PubMedPubMedCentralGoogle Scholar
  172. 172.
    Ueda S, Kuwabara I, Liu FT (2004) Suppression of tumor growth by galectin-7 gene transfer. Cancer Res 64(16):5672–5676. doi: 10.1158/0008-5472.CAN-04-0985 PubMedGoogle Scholar
  173. 173.
    Hsu DK, Liu FT (2004) Regulation of cellular homeostasis by galectins. Glycoconj J 19(7–9):507–515. doi: 10.1023/B:GLYC.0000014080.95829.52 PubMedGoogle Scholar
  174. 174.
    Thijssen VL, Barkan B, Shoji H, Aries IM, Mathieu V, Deltour L, Hackeng TM, Kiss R, Kloog Y, Poirier F, Griffioen AW (2010) Tumor cells secrete galectin-1 to enhance endothelial cell activity. Cancer Res 70(15):6216–6224. doi: 10.1158/0008-5472.CAN-09-4150 PubMedGoogle Scholar
  175. 175.
    Croci DO, Salatino M, Rubinstein N, Cerliani JP, Cavallin LE, Leung HJ, Ouyang J, Ilarregui JM, Toscano MA, Domaica CI, Croci MC, Shipp MA, Mesri EA, Albini A, Rabinovich GA (2012) Disrupting galectin-1 interactions with N-glycans suppresses hypoxia-driven angiogenesis and tumorigenesis in Kaposi’s sarcoma. J Exp Med 209(11):1985–2000. doi: 10.1084/jem.20111665 PubMedPubMedCentralGoogle Scholar
  176. 176.
    Takenaka Y, Fukumori T, Raz A (2004) Galectin-3 and metastasis. Glycoconj J 19(7–9):543–549. doi: 10.1023/B:GLYC.0000014084.01324.15 PubMedGoogle Scholar
  177. 177.
    Swann JB, Smyth MJ (2007) Immune surveillance of tumors. J Clin Invest 117(5):1137–1146. doi: 10.1172/JCI31405 PubMedPubMedCentralGoogle Scholar
  178. 178.
    Dalotto-Moreno T, Croci DO, Cerliani JP, Martinez-Allo VC, Dergan-Dylon S, Mendez-Huergo SP, Stupirski JC, Mazal D, Osinaga E, Toscano MA, Sundblad V, Rabinovich GA, Salatino M (2013) Targeting galectin-1 overcomes breast cancer-associated immunosuppression and prevents metastatic disease. Cancer Res 73(3):1107–1117. doi: 10.1158/0008-5472.CAN-12-2418 PubMedGoogle Scholar
  179. 179.
    Soldati R, Berger E, Zenclussen AC, Jorch G, Lode HN, Salatino M, Rabinovich GA, Fest S (2012) Neuroblastoma triggers an immunoevasive program involving galectin-1-dependent modulation of T cell and dendritic cell compartments. Int J Cancer 131(5):1131–1141. doi: 10.1002/ijc.26498 PubMedGoogle Scholar
  180. 180.
    Ouyang J, Plutschow A, Pogge von Strandmann E, Reiners KS, Ponader S, Rabinovich GA, Neuberg D, Engert A, Shipp MA (2013) Galectin-1 serum levels reflect tumor burden and adverse clinical features in classical Hodgkin lymphoma. Blood 121(17):3431–3433. doi: 10.1182/blood-2012-12-474569 PubMedGoogle Scholar
  181. 181.
    Barondes SH, Castronovo V, Cooper DN, Cummings RD, Drickamer K, Feizi T, Gitt MA, Hirabayashi J, Hughes C, Kasai K et al (1994) Galectins: a family of animal beta-galactoside-binding lectins. Cell 76(4):597–598PubMedGoogle Scholar
  182. 182.
    Levi G, Teichberg VI (1981) Isolation and physicochemical characterization of electrolectin, a beta-D-galactoside binding lectin from the electric organ of Electrophorus electricus. J Biol Chem 256(11):5735–5740PubMedGoogle Scholar
  183. 183.
    Tracey BM, Feizi T, Abbott WM, Carruthers RA, Green BN, Lawson AM (1992) Subunit molecular mass assignment of 14,654 Da to the soluble beta-galactoside-binding lectin from bovine heart muscle and demonstration of intramolecular disulfide bonding associated with oxidative inactivation. J Biol Chem 267(15):10342–10347PubMedGoogle Scholar
  184. 184.
    Hirabayashi J, Kasai K (1991) Effect of amino acid substitution by sited-directed mutagenesis on the carbohydrate recognition and stability of human 14-kDa beta-galactoside-binding lectin. J Biol Chem 266(35):23648–23653PubMedGoogle Scholar
  185. 185.
    Cho M, Cummings RD (1995) Galectin-1, a beta-galactoside-binding lectin in Chinese hamster ovary cells. I. Physical and chemical characterization. J Biol Chem 270(10):5198–5206PubMedGoogle Scholar
  186. 186.
    Pande AH, Gupta RK, Sumati HK (2003) Oxidation of goat hepatic galectin-1 induces change in secondary structure. Protein Pept Lett 10(3):265–275PubMedGoogle Scholar
  187. 187.
    Clerch LB, Whitney P, Hass M, Brew K, Miller T, Werner R, Massaro D (1988) Sequence of a full-length cDNA for rat lung beta-galactoside-binding protein: primary and secondary structure of the lectin. Biochemistry 27(2):692–699PubMedGoogle Scholar
  188. 188.
    Stowell SR, Cho M, Feasley CL, Arthur CM, Song X, Colucci JK, Karmakar S, Mehta P, Dias-Baruffi M, McEver RP, Cummings RD (2009) Ligand reduces galectin-1 sensitivity to oxidative inactivation by enhancing dimer formation. J Biol Chem 284(8):4989–4999. doi: 10.1074/jbc.M808925200 PubMedPubMedCentralGoogle Scholar
  189. 189.
    Inagaki Y, Sohma Y, Horie H, Nozawa R, Kadoya T (2000) Oxidized galectin-1 promotes axonal regeneration in peripheral nerves but does not possess lectin properties. Eur J Biochem 267(10):2955–2964PubMedGoogle Scholar
  190. 190.
    Kadoya T, Oyanagi K, Kawakami E, Hasegawa M, Inagaki Y, Sohma Y, Horie H (2005) Oxidized galectin-1 advances the functional recovery after peripheral nerve injury. Neurosci Lett 380(3):284–288. doi: 10.1016/j.neulet.2005.01.054 PubMedGoogle Scholar
  191. 191.
    Jaffe EK (2005) Morpheeins – a new structural paradigm for allosteric regulation. Trends Biochem Sci 30(9):490–497. doi: 10.1016/j.tibs.2005.07.003 PubMedGoogle Scholar
  192. 192.
    Ochieng J, Fridman R, Nangia-Makker P, Kleiner DE, Liotta LA, Stetler-Stevenson WG, Raz A (1994) Galectin-3 is a novel substrate for human matrix metalloproteinases-2 and -9. Biochemistry 33(47):14109–14114PubMedGoogle Scholar
  193. 193.
    Guevremont M, Martel-Pelletier J, Boileau C, Liu FT, Richard M, Fernandes JC, Pelletier JP, Reboul P (2004) Galectin-3 surface expression on human adult chondrocytes: a potential substrate for collagenase-3. Ann Rheum Dis 63(6):636–643. doi: 10.1136/ard.2003.007229 PubMedPubMedCentralGoogle Scholar
  194. 194.
    Brewer CF, Miceli MC, Baum LG (2002) Clusters, bundles, arrays and lattices: novel mechanisms for lectin-saccharide-mediated cellular interactions. Curr Opin Struct Biol 12(5):616–623PubMedGoogle Scholar
  195. 195.
    Nishi N, Shoji H, Seki M, Itoh A, Miyanaka H, Yuube K, Hirashima M, Nakamura T (2003) Galectin-8 modulates neutrophil function via interaction with integrin alphaM. Glycobiology 13(11):755–763PubMedGoogle Scholar
  196. 196.
    Nishi N, Itoh A, Shoji H, Miyanaka H, Nakamura T (2006) Galectin-8 and galectin-9 are novel substrates for thrombin. Glycobiology 16(11):15C–20C. doi: 10.1093/glycob/cwl028 PubMedGoogle Scholar
  197. 197.
    Merkle RK, Cummings RD (1988) Asparagine-linked oligosaccharides containing poly-N-acetyllactosamine chains are preferentially bound by immobilized calf heart agglutinin. J Biol Chem 263(31):16143–16149PubMedGoogle Scholar
  198. 198.
    Brewer CF (2004) Thermodynamic binding studies of galectin-1, -3 and -7. Glycoconj J 19(7–9):459–465. doi: 10.1023/B:GLYC.0000014075.62724.d0 PubMedGoogle Scholar
  199. 199.
    Hirabayashi J, Hashidate T, Arata Y, Nishi N, Nakamura T, Hirashima M, Urashima T, Oka T, Futai M, Muller WE, Yagi F, Kasai K (2002) Oligosaccharide specificity of galectins: a search by frontal affinity chromatography. Biochim Biophys Acta 1572(2–3):232–254PubMedGoogle Scholar
  200. 200.
    Dam TK, Gabius HJ, Andre S, Kaltner H, Lensch M, Brewer CF (2005) Galectins bind to the multivalent glycoprotein asialofetuin with enhanced affinities and a gradient of decreasing binding constants. Biochemistry 44(37):12564–12571. doi: 10.1021/bi051144z PubMedGoogle Scholar
  201. 201.
    Sorme P, Kahl-Knutsson B, Huflejt M, Nilsson UJ, Leffler H (2004) Fluorescence polarization as an analytical tool to evaluate galectin-ligand interactions. Anal Biochem 334(1):36–47. doi: 10.1016/j.ab.2004.06.042 PubMedGoogle Scholar
  202. 202.
    Lepur A, Salomonsson E, Nilsson UJ, Leffler H (2012) Ligand induced galectin-3 protein self-association. J Biol Chem 287(26):21751–21756. doi: 10.1074/jbc.C112.358002 PubMedPubMedCentralGoogle Scholar
  203. 203.
    Stowell SR, Arthur CM, Mehta P, Slanina KA, Blixt O, Leffler H, Smith DF, Cummings RD (2008) Galectins-1, -2 and -3 exhibit differential recognition of sialylated glycans and blood group antigens. J Biol Chem 283:10109–10123PubMedPubMedCentralGoogle Scholar
  204. 204.
    Stowell SR, Dias-Baruffi M, Penttila L, Renkonen O, Nyame AK, Cummings RD (2004) Human galectin-1 recognition of poly-N-acetyllactosamine and chimeric polysaccharides. Glycobiology 14(2):157–167PubMedGoogle Scholar
  205. 205.
    Leppanen A, Stowell S, Blixt O, Cummings RD (2005) Dimeric Galectin-1 Binds with High Affinity to {alpha}2,3-Sialylated and Non-sialylated Terminal N-Acetyllactosamine Units on Surface-bound Extended Glycans. J Biol Chem 280(7):5549–5562PubMedGoogle Scholar
  206. 206.
    Zhuo Y, Chammas R, Bellis SL (2008) Sialylation of beta1 integrins blocks cell adhesion to galectin-3 and protects cells against galectin-3-induced apoptosis. J Biol Chem 283(32):22177–22185. doi: 10.1074/jbc.M8000015200 PubMedPubMedCentralGoogle Scholar
  207. 207.
    Carlsson S, Oberg CT, Carlsson MC, Sundin A, Nilsson UJ, Smith D, Cummings RD, Almkvist J, Karlsson A, Leffler H (2007) Affinity of galectin-8 and its carbohydrate recognition domains for ligands in solution and at the cell surface. Glycobiology 17(6):663–676. doi: 10.1093/glycob/cwm026 PubMedGoogle Scholar
  208. 208.
    Miyanishi N, Nishi N, Abe H, Kashio Y, Shinonaga R, Nakakita S, Sumiyoshi W, Yamauchi A, Nakamura T, Hirashima M, Hirabayashi J (2007) Carbohydrate-recognition domains of galectin-9 are involved in intermolecular interaction with galectin-9 itself and other members of the galectin family. Glycobiology 17(4):423–432. doi: 10.1093/glycob/cwm001 PubMedGoogle Scholar
  209. 209.
    Poland PA, Rondanino C, Kinlough CL, Heimburg-Molinaro J, Arthur CM, Stowell SR, Smith DF, Hughey RP (2011) Identification and characterization of endogenous galectins expressed in Madin Darby canine kidney cells. J Biol Chem 286(8):6780–6790. doi: 10.1074/jbc.M110.179002 PubMedPubMedCentralGoogle Scholar
  210. 210.
    Cha SK, Ortega B, Kurosu H, Rosenblatt KP, Kuro OM, Huang CL (2008) Removal of sialic acid involving Klotho causes cell-surface retention of TRPV5 channel via binding to galectin-1. Proc Natl Acad Sci U S A 105(28):9805–9810. doi: 10.1073/pnas.0803223105 PubMedPubMedCentralGoogle Scholar
  211. 211.
    Carlsson S, Carlsson MC, Leffler H (2007) Intracellular sorting of galectin-8 based on carbohydrate fine specificity. Glycobiology 17(9):906–912. doi: 10.1093/glycob/cwm059 PubMedGoogle Scholar
  212. 212.
    Kopitz J, von Reitzenstein C, Burchert M, Cantz M, Gabius HJ (1998) Galectin-1 is a major receptor for ganglioside GM1, a product of the growth-controlling activity of a cell surface ganglioside sialidase, on human neuroblastoma cells in culture. J Biol Chem 273(18):11205–11211PubMedGoogle Scholar
  213. 213.
    Hullin-Matsuda F, Kobayashi T (2007) Monitoring the distribution and dynamics of signaling microdomains in living cells with lipid-specific probes. Cell Mol Life Sci 64(19–20):2492–2504. doi: 10.1007/s00018-007-7281-x PubMedGoogle Scholar
  214. 214.
    Kopitz J, Ballikaya S, Andre S, Gabius HJ (2012) Ganglioside GM1/galectin-dependent growth regulation in human neuroblastoma cells: special properties of bivalent galectin-4 and significance of linker length for ligand selection. Neurochem Res 37(6):1267–1276. doi: 10.1007/s11064-011-0693-x PubMedGoogle Scholar
  215. 215.
    Sato S, St-Pierre C, Bhaumik P, Nieminen J (2009) Galectins in innate immunity: dual functions of host soluble beta-galactoside-binding lectins as damage-associated molecular patterns (DAMPs) and as receptors for pathogen-associated molecular patterns (PAMPs). Immunol Rev 230(1):172–187. doi: 10.1111/j.1600-065X.2009.00790.x PubMedGoogle Scholar
  216. 216.
    Neth O, Jack DL, Dodds AW, Holzel H, Klein NJ, Turner MW (2000) Mannose-binding lectin binds to a range of clinically relevant microorganisms and promotes complement deposition. Infect Immun 68(2):688–693PubMedPubMedCentralGoogle Scholar
  217. 217.
    Stowell SR, Winkler AM, Maier CL, Arthur CM, Smith NH, Girard-Pierce KR, Cummings RD, Zimring JC, Hendrickson JE (2012) Initiation and regulation of complement during hemolytic transfusion reactions. Clin Dev Immunol 2012:307093. doi: 10.1155/2012/307093 PubMedPubMedCentralGoogle Scholar
  218. 218.
    Debierre-Grockiego F, Niehus S, Coddeville B, Elass E, Poirier F, Weingart R, Schmidt RR, Mazurier J, Guerardel Y, Schwarz RT (2010) Binding of Toxoplasma gondii glycosylphosphatidylinositols to galectin-3 is required for their recognition by macrophages. J Biol Chem 285(43):32744–32750. doi: 10.1074/jbc.M110.137588 PubMedPubMedCentralGoogle Scholar
  219. 219.
    van den Berg TK, Honing H, Franke N, van Remoortere A, Schiphorst WE, Liu FT, Deelder AM, Cummings RD, Hokke CH, van Die I (2004) LacdiNAc-glycans constitute a parasite pattern for galectin-3-mediated immune recognition. J Immunol 173(3):1902–1907PubMedGoogle Scholar
  220. 220.
    Moody TN, Ochieng J, Villalta F (2000) Novel mechanism that Trypanosoma cruzi uses to adhere to the extracellular matrix mediated by human galectin-3. FEBS Lett 470(3):305–308PubMedGoogle Scholar
  221. 221.
    Kleshchenko YY, Moody TN, Furtak VA, Ochieng J, Lima MF, Villalta F (2004) Human galectin-3 promotes Trypanosoma cruzi adhesion to human coronary artery smooth muscle cells. Infect Immun 72(11):6717–6721. doi: 10.1128/IAI.72.11.6717-6721.2004 PubMedPubMedCentralGoogle Scholar
  222. 222.
    Quattroni P, Li Y, Lucchesi D, Lucas S, Hood DW, Herrmann M, Gabius HJ, Tang CM, Exley RM (2012) Galectin-3 binds Neisseria meningitidis and increases interaction with phagocytic cells. Cell Microbiol 14(11):1657–1675. doi: 10.1111/j.1462-5822.2012.01838.x PubMedPubMedCentralGoogle Scholar
  223. 223.
    Levroney EL, Aguilar HC, Fulcher JA, Kohatsu L, Pace KE, Pang M, Gurney KB, Baum LG, Lee B (2005) Novel innate immune functions for galectin-1: galectin-1 inhibits cell fusion by Nipah virus envelope glycoproteins and augments dendritic cell secretion of proinflammatory cytokines. J Immunol 175(1):413–420PubMedGoogle Scholar
  224. 224.
    Pelletier I, Hashidate T, Urashima T, Nishi N, Nakamura T, Futai M, Arata Y, Kasai K, Hirashima M, Hirabayashi J, Sato S (2003) Specific recognition of Leishmania major poly-beta-galactosyl epitopes by galectin-9: possible implication of galectin-9 in interaction between L. major and host cells. J Biol Chem 278(25):22223–22230. doi: 10.1074/jbc.M302693200 PubMedGoogle Scholar
  225. 225.
    Yang ML, Chen YH, Wang SW, Huang YJ, Leu CH, Yeh NC, Chu CY, Lin CC, Shieh GS, Chen YL, Wang JR, Wang CH, Wu CL, Shiau AL (2011) Galectin-1 binds to influenza virus and ameliorates influenza virus pathogenesis. J Virol 85(19):10010–10020. doi: 10.1128/JVI.00301-11 PubMedPubMedCentralGoogle Scholar
  226. 226.
    Mercier S, St-Pierre C, Pelletier I, Ouellet M, Tremblay MJ, Sato S (2008) Galectin-1 promotes HIV-1 infectivity in macrophages through stabilization of viral adsorption. Virology 371(1):121–129. doi: 10.1016/j.virol.2007.09.034 PubMedGoogle Scholar
  227. 227.
    Ouellet M, Mercier S, Pelletier I, Bounou S, Roy J, Hirabayashi J, Sato S, Tremblay MJ (2005) Galectin-1 acts as a soluble host factor that promotes HIV-1 infectivity through stabilization of virus attachment to host cells. J Immunol 174(7):4120–4126PubMedGoogle Scholar
  228. 228.
    Arthur CM, Cummings RD, Stowell SR (2014) Using glycan microarrays to understand immunity. Curr Opin Chem Biol 18:55–61. doi: 10.1016/j.cbpa.2013.12.017 PubMedGoogle Scholar
  229. 229.
    Stowell SR, Arthur CM, McBride R, Berger O, Razi N, Heimburg-Molinaro J, Rodrigues JP, Noll AJ, von Gunten S, Smith DF, Knirel YA, Paulson JC, Cummings RD (2014) Microbial glycan microarrays define key features of host-microbial interactions. Nat Chem Biol 10(6):470–476PubMedPubMedCentralGoogle Scholar
  230. 230.
    St-Pierre C, Manya H, Ouellet M, Clark GF, Endo T, Tremblay MJ, Sato S (2011) Host-soluble galectin-1 promotes HIV-1 replication through a direct interaction with glycans of viral gp120 and host CD4. J Virol 85(22):11742–11751. doi: 10.1128/JVI.05351-11 PubMedPubMedCentralGoogle Scholar
  231. 231.
    Okumura CY, Baum LG, Johnson PJ (2008) Galectin-1 on cervical epithelial cells is a receptor for the sexually transmitted human parasite Trichomonas vaginalis. Cell Microbiol 10(10):2078–2090. doi: 10.1111/j.1462-5822.2008.01190.x PubMedGoogle Scholar
  232. 232.
    Kamhawi S, Ramalho-Ortigao M, Pham VM, Kumar S, Lawyer PG, Turco SJ, Barillas-Mury C, Sacks DL, Valenzuela JG (2004) A role for insect galectins in parasite survival. Cell 119(3):329–341PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Connie M. Arthur
    • 1
  • Marcelo Dias Baruffi
    • 2
  • Richard D. Cummings
    • 3
  • Sean R. Stowell
    • 4
    Email author
  1. 1.The Department of Pathology and Laboratory MedicineEmory University School of MedicineAtlantaUSA
  2. 2.Department of Clinical Analyses, Toxicology and Food Sciences, Faculty of Pharmaceutical Sciences of Ribeirão PretoUniversity of Sao PauloRibeirão Preto-SPBrazil
  3. 3.Department of BiochemistryEmory University School of MedicineAtlantaUSA
  4. 4.Center for Transfusion and Cellular Therapies, Department of Pathology and Laboratory MedicineEmory University School of MedicineAtlantaUSA

Personalised recommendations