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Original Article

Severe preeclampsia is characterized by increased placental expression of galectin-1

, MD, PhD, , , , , , , , , , , & show all
Pages 429-442 | Received 07 Sep 2007, Accepted 21 Feb 2008, Published online: 07 Jul 2009

References

  • Sibai B, Dekker G, Kupferminc M. Pre-eclampsia. Lancet 2005; 365: 785–799
  • Ness R B, Sibai B M. Shared and disparate components of the pathophysiologies of fetal growth restriction and preeclampsia. Am J Obstet Gynecol 2006; 195: 40–49
  • Romero R. Prenatal medicine: The child is the father of the man. Prenat Neonatal Med 1996; 1: 8–11
  • Roberts J M, Taylor R N, Musci T J, Rodgers G M, Hubel C A, McLaughlin M K. Preeclampsia: An endothelial cell disorder. Am J Obstet Gynecol 1989; 161: 1200–1204
  • Bretelle F, Sabatier F, Blann A, D'Ercole C, Boutiere B, Mutin M, Boubli L, Sampol J, Dignat-George F. Maternal endothelial soluble cell adhesion molecules with isolated small for gestational age fetuses: Comparison with pre-eclampsia. BJOG 2001; 108: 1277–1282
  • Johnson M R, Anim-Nyame N, Johnson P, Sooranna S R, Steer P J. Does endothelial cell activation occur with intrauterine growth restriction. BJOG 2002; 109: 836–839
  • Redman C W, Sargent I L. Latest advances in understanding preeclampsia. Science 2005; 308: 1592–1594
  • Poston L. Endothelial dysfunction in pre-eclampsia. Pharmacol Rep 2006; 58(Suppl)69–74
  • Brosens I A, Robertson W B, Dixon H G. The role of the spiral arteries in the pathogenesis of pre-eclampsia. J Pathol 1970; 101: vi
  • De Wolf F, Brosens I, Renaer M. Fetal growth retardation and the maternal arterial supply of the human placenta in the absence of sustained hypertension. Br J Obstet Gynaecol 1980; 87: 678–685
  • Pijnenborg R, Anthony J, Davey D A, Rees A, Tiltman A, Vercruysse L, van Assche A. Placental bed spiral arteries in the hypertensive disorders of pregnancy. Br J Obstet Gynaecol 1991; 98: 648–655
  • Myatt L. Role of placenta in preeclampsia. Endocrine 2002; 19: 103–111
  • Burton G J, Jauniaux E. Placental oxidative stress: From miscarriage to preeclampsia. J Soc Gynecol Investig 2004; 11: 342–352
  • Fisher S J. The placental problem: Linking abnormal cytotrophoblast differentiation to the maternal symptoms of preeclampsia. Reprod Biol Endocrinol 2004; 2: 53
  • Lyall F. Priming and remodelling of human placental bed spiral arteries during pregnancy – a review. Placenta 2005; 26(Suppl A)S31–36
  • Espinoza J, Romero R, Kim YM, Kusanovic J P, Hassan S, Erez O, Gotsch F, Than N G, Papp Z, Kim C J. Normal and abnormal transformation of the spiral arteries during pregnancy. J Perinat Med 2006; 34: 447–458
  • Kupferminc M J, Daniel Y, Englender T, Baram A, Many A, Jaffa A J, Gull I, Lessing J B. Vascular endothelial growth factor is increased in patients with preeclampsia. Am J Reprod Immunol 1997; 38: 302–306
  • Torry D S, Wang H S, Wang T H, Caudle M R, Torry R J. Preeclampsia is associated with reduced serum levels of placenta growth factor. Am J Obstet Gynecol 1998; 179: 1539–1544
  • Tidwell S C, Ho H N, Chiu W H, Torry R J, Torry D S. Low maternal serum levels of placenta growth factor as an antecedent of clinical preeclampsia. Am J Obstet Gynecol 2001; 184: 1267–1272
  • Torry D S, Mukherjea D, Arroyo J, Torry R J. Expression and function of placenta growth factor: Implications for abnormal placentation. J Soc Gynecol Investig 2003; 10: 178–188
  • Maynard S E, Min J Y, Merchan J, Lim K H, Li J, Mondal S, Libermann T A, Morgan J P, Sellke F W, Stillman I E, et al. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 2003; 111: 649–658
  • Chaiworapongsa T, Romero R, Espinoza J, Bujold E, Kim Y M, Goncalves L F, Gomez R, Edwin S. Evidence supporting a role for blockade of the vascular endothelial growth factor system in the pathophysiology of preeclampsia. Young Investigator Award. Am J Obstet Gynecol 2004; 190: 1541–1547
  • Levine R J, Maynard S E, Qian C, Lim K H, England L J, Yu K F, Schisterman E F, Thadhani R, Sachs B P, Epstein F H, et al. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004; 350: 672–683
  • Malamitsi-Puchner A, Boutsikou T, Economou E, Sarandakou A, Makrakis E, Hassiakos D, Creatsas G. Vascular endothelial growth factor and placenta growth factor in intrauterine growth-restricted fetuses and neonates. Mediators Inflamm 2005; 2005: 293–297
  • Bujold E, Romero R, Chaiworapongsa T, Kim Y M, Kim G J, Kim M R, Espinoza J, Goncalves L F, Edwin S, Mazor M. Evidence supporting that the excess of the sVEGFR-1 concentration in maternal plasma in preeclampsia has a uterine origin. J Matern Fetal Neonatal Med 2005; 18: 9–16
  • Chaiworapongsa T, Romero R, Kim Y M, Kim G J, Kim M R, Espinoza J, Bujold E, Goncalves L, Gomez R, Edwin S, et al. Plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated prior to the clinical diagnosis of pre-eclampsia. J Matern Fetal Neonatal Med 2005; 17: 3–18
  • Padavala S, Pope N, Baker P, Crocker I. An imbalance between vascular endothelial growth factor and its soluble receptor in placental villous explants of intrauterine growth-restricted pregnancies. J Soc Gynecol Investig 2006; 13: 40–47
  • Levine R J, Lam C, Qian C, Yu K F, Maynard S E, Sachs B P, Sibai B M, Epstein F H, Romero R, Thadhani R, et al. Soluble endoglin and other circulating antiangiogenic factors in preeclampsia. N Engl J Med 2006; 355: 992–1005
  • Crispi F, Dominguez C, Llurba E, Martin-Gallan P, Cabero L, Gratacos E. Placental angiogenic growth factors and uterine artery Doppler findings for characterization of different subsets in preeclampsia and in isolated intrauterine growth restriction. Am J Obstet Gynecol 2006; 195: 201–207
  • Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim Y M, Bdolah Y, Lim K H, Yuan H T, Libermann T A, et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 2006; 12: 642–649
  • Wallner W, Sengenberger R, Strick R, Strissel P L, Meurer B, Beckmann M W, Schlembach D. Angiogenic growth factors in maternal and fetal serum in pregnancies complicated by intrauterine growth restriction. Clin Sci (Lond) 2007; 112: 51–57
  • Espinoza J, Romero R, Nien J K, Gomez R, Kusanovic J P, Goncalves L F, Medina L, Edwin S, Hassan S, Carstens M, et al. Identification of patients at risk for early onset and/or severe preeclampsia with the use of uterine artery Doppler velocimetry and placental growth factor. Am J Obstet Gynecol 2007; 196: 326.e1–326.e13
  • Chaiworapongsa T, Espinoza J, Gotsch F, Kim Y M, Kim G J, Goncalves L F, Edwin S, Kusanovic J P, Erez O, Than N G, et al. The maternal plasma soluble vascular endothelial growth factor receptor-1 concentration is elevated in SGA and the magnitude of the increase relates to Doppler abnormalities in the maternal and fetal circulation. J Matern Fetal Neonatal Med 2008; 21: 25–40
  • Erez O, Romero R, Espinoza J, Fu W, Todem D, Kusanovic J P, Gotsch F, Edwin S, Nien J K, Chaiworapongsa T, et al. The change in concentrations of angiogenic and anti-angiogenic factors in maternal plasma between the first and second trimesters in risk assessment for the subsequent development of preeclampsia and small-for-gestational age. J Matern Fetal Neonatal Med 2008; 21: 279–287
  • Romero R, Nien J K, Espinoza J, Todem D, Fu W, Chung H, Kusanovic J P, Gotsch F, Erez O, Mazaki-Tovi S, et al. A longitudinal study of angiogenic (placental growth factor) and anti-angiogenic (soluble endoglin and soluble VEGF receptor-1) factors in normal pregnancy and patients destined to develop preeclampsia and deliver a small-for-gestational-age neonate. J Matern Fetal Neonatal Med 2008; 21: 9–23
  • Robertson W B, Brosens I, Dixon G. Maternal uterine vascular lesions in the hypertensive complications of pregnancy. Perspect Nephrol Hypertens 1976; 5: 115–127
  • Campbell S, Diaz-Recasens J, Griffin D R, Cohen-Overbeek T E, Pearce J M, Willson K, Teague M J. New Doppler technique for assessing uteroplacental blood flow. Lancet 1983; 1: 675–677
  • Harrington K F, Campbell S, Bewley S, Bower S. Doppler velocimetry studies of the uterine artery in the early prediction of pre-eclampsia and intra-uterine growth retardation. Eur J Obstet Gynecol Reprod Biol 1991; 42(Suppl)S14–20
  • Papageorghiou A T, Yu C K, Bindra R, Pandis G, Nicolaides K H. Multicenter screening for pre-eclampsia and fetal growth restriction by transvaginal uterine artery Doppler at 23 weeks of gestation. Ultrasound Obstet Gynecol 2001; 18: 441–449
  • Granger J P, Alexander B T, Llinas M T, Bennett W A, Khalil R A. Pathophysiology of preeclampsia: Linking placental ischemia/hypoxia with microvascular dysfunction. Microcirculation 2002; 9: 147–160
  • Sacks G P, Studena K, Sargent K, Redman C W. Normal pregnancy and preeclampsia both produce inflammatory changes in peripheral blood leukocytes akin to those of sepsis. Am J Obstet Gynecol 1998; 179: 80–86
  • Gervasi M T, Chaiworapongsa T, Pacora P, Naccasha N, Yoon B H, Maymon E, Romero R. Phenotypic and metabolic characteristics of monocytes and granulocytes in preeclampsia. Am J Obstet Gynecol 2001; 185: 792–797
  • Redman C W, Sargent I L. The pathogenesis of pre-eclampsia. Gynecol Obstet Fertil 2001; 29: 518–522
  • Chaiworapongsa T, Yoshimatsu J, Espinoza J, Kim Y M, Berman S, Edwin S, Yoon B H, Romero R. Evidence of in vivo generation of thrombin in patients with small-for-gestational-age fetuses and pre-eclampsia. J Matern Fetal Neonatal Med 2002; 11: 362–367
  • Chaiworapongsa T, Gervasi M T, Refuerzo J, Espinoza J, Yoshimatsu J, Berman S, Romero R. Maternal lymphocyte subpopulations (CD45RA+ and CD45RO+) in preeclampsia. Am J Obstet Gynecol 2002; 187: 889–893
  • Bartha J L, Romero-Carmona R, Comino-Delgado R. Inflammatory cytokines in intrauterine growth retardation. Acta Obstet Gynecol Scand 2003; 82: 1099–1102
  • Redman C W, Sacks G P, Sargent I L. Preeclampsia: An excessive maternal inflammatory response to pregnancy. Am J Obstet Gynecol 1999; 180: 499–506
  • Kim Y M, Romero R, Oh S Y, Kim C J, Kilburn B A, Armant D R, Nien J K, Gomez R, Mazor M, Saito S, et al. Toll-like receptor 4: A potential link between “danger signals”, the innate immune system, and preeclampsia. Am J Obstet Gynecol 2005; 193: 921–927
  • Bonney E A. Preeclampsia: A view through the danger model. J Reprod Immunol 2007; 76: 68–74
  • Barondes S H, Castronovo V, Cooper D N, Cummings R D, Drickamer K, Feizi T, Gitt M A, Hirabayashi J, Hughes C, Kasai K, et al. Galectins: A family of animal beta-galactoside-binding lectins. Cell 1994; 76: 597–598
  • Leonidas D D, Elbert B L, Zhou Z, Leffler H, Ackerman S J, Acharya K R. 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 1995; 3: 1379–1393
  • Visegrady B, Than N G, Kilar F, Sumegi B, Than G N, Bohn H. Homology modelling and molecular dynamics studies of human placental tissue protein 13 (galectin-13). Protein Eng 2001; 14: 875–880
  • Leffler H, Carlsson S, Hedlund M, Qian Y, Poirier F. Introduction to galectins. Glycoconj J 2004; 19: 433–440
  • Houzelstein D, Goncalves I R, Fadden A J, Sidhu S S, Cooper D N, Drickamer K, Leffler H, Poirier F. Phylogenetic analysis of the vertebrate galectin family. Mol Biol Evol 2004; 21: 1177–1187
  • Buzas E I, Gyorgy B, Pasztoi M, Jelinek I, Falus A, Gabius H J. Carbohydrate recognition systems in autoimmunity. Autoimmunity 2006; 39: 691–704
  • Lopez-Lucendo M F, Solis D, Andre S, Hirabayashi J, Kasai K, Kaltner H, Gabius H J, Romero A. Growth-regulatory human galectin-1: Crystallographic characterisation of the structural changes induced by single-site mutations and their impact on the thermodynamics of ligand binding. J Mol Biol 2004; 343: 957–970
  • Brewer F C. Binding and cross-linking properties of galectins. Biochim Biophys Acta 2002; 1572: 255–262
  • Rabinovich G A, Baum L G, Tinari N, Paganelli R, Natoli C, Liu F T, Iacobelli S. Galectins and their ligands: Amplifiers, silencers or tuners of the inflammatory response. Trends Immunol 2002; 23: 313–320
  • Elola M T, Chiesa M E, Alberti A F, Mordoh J, Fink N E. Galectin-1 receptors in different cell types. J Biomed Sci 2005; 12: 13–29
  • Kasai K, Hirabayashi J. Galectins: A family of animal lectins that decipher glycocodes. J Biochem (Tokyo) 1996; 119: 1–8
  • Villalobo A, Gabius H. Signaling pathways for transduction of the initial message of the glycocode into cellular responses. Acta Anat (Basel) 1998; 161: 110–129
  • Gabius H J, Andre S, Kaltner H, Siebert H C. The sugar code: Functional lectinomics. Biochim Biophys Acta 2002; 1572: 165–177
  • Camby I, Le Mercier M, Lefranc F, Kiss R. Galectin-1: A small protein with major functions. Glycobiology 2006; 16: 137–157
  • Hirabayashi J, Kasai K. Human placenta beta-galactoside-binding lectin. Purification and some properties. Biochem Biophys Res Commun 1984; 122: 938–944
  • Hirabayashi J, Kasai K. Complete amino acid sequence of a beta-galactoside-binding lectin from human placenta. J Biochem (Tokyo) 1988; 104: 1–4
  • Couraud P O, Casentini-Borocz D, Bringman T S, Griffith J, McGrogan M, Nedwin G E. Molecular cloning, characterization, and expression of a human 14-kDa lectin. J Biol Chem 1989; 264: 1310–1316
  • Bevan B H, Kilpatrick D C, Liston W A, Hirabayashi J, Kasai K. Immunohistochemical localization of a beta-D-galactoside-binding lectin at the human maternofetal interface. Histochem J 1994; 26: 582–586
  • Walzel H, Neels P, Bremer H, Kohler H, Raab N, Barten M, Brock J. Immunohistochemical and glycohistochemical localization of the beta-galactoside-binding S-type lectin in human placenta. Acta Histochem 1995; 97: 33–42
  • Maquoi E, van den Brule F A, Castronovo V, Foidart J M. Changes in the distribution pattern of galectin-1 and galectin-3 in human placenta correlates with the differentiation pathways of trophoblasts. Placenta 1997; 18: 433–439
  • Vicovac L, Jankovic M, Cuperlovic M. Galectin-1 and -3 in cells of the first trimester placental bed. Hum Reprod 1998; 13: 730–735
  • Jeschke U, Mayr D, Schiessl B, Mylonas I, Schulze S, Kuhn C, Friese K, Walzel H. Expression of galectin-1, -3 (gal-1, gal-3) and the Thomsen–Friedenreich (TF) antigen in normal, IUGR, preeclamptic and HELLP placentas. Placenta 2007; 28: 1165–1173
  • Dettin L, Rubinstein N, Aoki A, Rabinovich G A, Maldonado C A. Regulated expression and ultrastructural localization of galectin-1, a proapoptotic beta-galactoside-binding lectin, during spermatogenesis in rat testis. Biol Reprod 2003; 68: 51–59
  • Sakaguchi M, Shingo T, Shimazaki T, Okano H J, Shiwa M, Ishibashi S, Oguro H, Ninomiya M, Kadoya T, Horie H, et al. A carbohydrate-binding protein, galectin-1, promotes proliferation of adult neural stem cells. Proc Natl Acad Sci U S A 2006; 103: 7112–7117
  • 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; 5: 241–251
  • He J, Baum L G. Presentation of galectin-1 by extracellular matrix triggers T cell death. J Biol Chem 2004; 279: 4705–4712
  • 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; 30: 1331–1339
  • 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; 28: 177–184
  • Rabinovich G A, 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; 190: 385–398
  • 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; 31: 399–406
  • 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 regulatory-mediated anti-inflammatory responses. J Immunol 2006; 176: 6323–6332
  • 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; 109: 295–307
  • Baum L G, Seilhamer J J, Pang M, Levine W B, Beynon D, Berliner J A. Synthesis of an endogenous lectin, galectin-1, by human endothelial cells is up-regulated by endothelial cell activation. Glycoconj J 1995; 12: 63–68
  • Kim C W, Cho E H, Lee Y J, Kim Y H, Hah Y S, Kim D R. Disease-specific proteins from rheumatoid arthritis patients. J Korean Med Sci 2006; 21: 478–484
  • Rabinovich G A, Iglesias M M, Modesti N M, Castagna L F, Wolfenstein-Todel C, Riera C M, Sotomayor C E. Activated rat macrophages produce a galectin-1-like protein that induces apoptosis of T cells: Biochemical and functional characterization. J Immunol 1998; 160: 4831–4840
  • Zuniga E, Gruppi A, Hirabayashi J, Kasai K I, Rabinovich G A. Regulated expression and effect of galectin-1 on Trypanosoma cruzi-infected macrophages: Modulation of microbicidal activity and survival. Infect Immun 2001; 69: 6804–6812
  • Garin M I, Chu C C, Golshayan D, Cernuda-Morollon E, Wait R, Lechler R I. Galectin-1: A key effector of regulation mediated by CD4+CD25+ T cells. Blood 2007; 109: 2058–2065
  • Gil C D, Cooper D, Rosignoli G, Perretti M, Oliani S M. Inflammation-induced modulation of cellular galectin-1 and -3 expression in a model of rat peritonitis. Inflamm Res 2006; 55: 99–107
  • Rabinovich G A, Gruppi A. Galectins as immunoregulators during infectious processes: From microbial invasion to the resolution of the disease. Parasite Immunol 2005; 27: 103–114
  • Sibai B M, Ewell M, Levine R J, Klebanoff M A, Esterlitz J, Catalano P M, Goldenberg R L, Joffe G. Risk factors associated with preeclampsia in healthy nulliparous women. The Calcium for Preeclampsia Prevention (CPEP) Study Group. Am J Obstet Gynecol 1997; 177: 1003–1010
  • Report of the National High Blood Pressure Education Program Working Group on High Blood Pressure in Pregnancy. Am J Obstet Gynecol 2000; 183: S1–22
  • Alexander G R, Himes J H, Kaufman R B, Mor J, Kogan M. A United States national reference for fetal growth. Obstet Gynecol 1996; 87: 163–168
  • Fu W J, Hu J, Spencer T, Carroll R, Wu G. Statistical models in assessing fold change of gene expression in real-time RT-PCR experiments. Comput Biol Chem 2006; 30: 21–26
  • Bonferroni C E. Il calcolo delle assicurazioni su gruppi di teste. Studi in Onore del Professore Salvatore Orto Carboni. Rome 1935; 13–60
  • Redline R W, Boyd T, Campbell V, Hyde S, Kaplan C, Khong T Y, Prashner H R, Waters B L. Maternal vascular underperfusion: Nosology and reproducibility of placental reaction patterns. Pediatr Dev Pathol 2004; 7: 237–249
  • Redline R W, Heller D, Keating S, Kingdom J. Placental diagnostic criteria and clinical correlation—a workshop report. Placenta 2005; 26(Suppl A)S114–117
  • Ozeki Y, Matsui T, Yamamoto Y, Funahashi M, Hamako J, Titani K. Tissue fibronectin is an endogenous ligand for galectin-1. Glycobiology 1995; 5: 255–261
  • Phillips B, Knisley K, Weitlauf K D, Dorsett J, Lee V, Weitlauf H. Differential expression of two beta-galactoside-binding lectins in the reproductive tracts of pregnant mice. Biol Reprod 1996; 55: 548–558
  • Iglesias M M, Rabinovich G A, Ivanovic V, Sotomayor C, Wolfenstein-Todel C. Galectin-1 from ovine placenta—amino-acid sequence, physicochemical properties and implications in T-cell death. Eur J Biochem 1998; 252: 400–407
  • Prior I A, Muncke C, Parton R G, Hancock J F. Direct visualization of Ras proteins in spatially distinct cell surface microdomains. J Cell Biol 2003; 160: 165–170
  • Nickel W. Unconventional secretory routes: Direct protein export across the plasma membrane of mammalian cells. Traffic 2005; 6: 607–614
  • Jeschke U, Karsten U, Wiest I, Schulze S, Kuhn C, Friese K, Walzel H. Binding of galectin-1 (gal-1) to the Thomsen–Friedenreich (TF) antigen on trophoblast cells and inhibition of proliferation of trophoblast tumor cells in vitro by gal-1 or an anti-TF antibody. Histochem Cell Biol 2006; 126: 437–444
  • Moiseeva E P, Williams B, Goodall A H, Samani N J. Galectin-1 interacts with beta-1 subunit of integrin. Biochem Biophys Res Commun 2003; 310: 1010–1016
  • Peters D G, Kassam A B, Feingold E, Heidrich-O’Hare E, Yonas H, Ferrell R E, Brufsky A. Molecular anatomy of an intracranial aneurysm: Coordinated expression of genes involved in wound healing and tissue remodeling. Stroke 2001; 32: 1036–1042
  • Lotan R, Belloni P N, Tressler R J, Lotan D, Xu X C, Nicolson G L. Expression of galectins on microvessel endothelial cells and their involvement in tumour cell adhesion. Glycoconj J 1994; 11: 462–468
  • Perillo N L, Pace K E, Seilhamer J J, Baum L G. Apoptosis of T cells mediated by galectin-1. Nature 1995; 378: 736–739
  • 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 interactions in experimental inflammation. Am J Pathol 2003; 163: 1505–1515
  • Danese S, Dejana E, Fiocchi C. Immune regulation by microvascular endothelial cells: Directing innate and adaptive immunity, coagulation, and inflammation. J Immunol 2007; 178: 6017–6022
  • He J, Baum L G. Endothelial cell expression of galectin-1 induced by prostate cancer cells inhibits T-cell transendothelial migration. Lab Invest 2006; 86: 578–590
  • Frauli M, Ludwig H. Demonstration of the ability of Hofbauer cells to phagocytose exogenous antibodies. Eur J Obstet Gynecol Reprod Biol 1987; 26: 135–144
  • Zaccheo D, Pistoia V, Castellucci M, Martinoli C. Isolation and characterization of Hofbauer cells from human placental villi. Arch Gynecol Obstet 1989; 246: 189–200
  • Matsubara S, Takayama T, Yamada T, Usui R, Izumi A, Watanabe T, Ohkuchi A, Shibahara H, Sato I, Suzuki M. Hofbauer cell activation and its increased glucose-6-phosphate dehydrogenase activity in second trimester-spontaneous abortion: An ultrastructural dual staining enzyme-cytochemical study. Am J Reprod Immunol 2003; 49: 202–209
  • Taniguchi T, Matsuzaki N, Kameda T, Shimoya K, Jo T, Saji F, Tanizawa O. The enhanced production of placental interleukin-1 during labor and intrauterine infection. Am J Obstet Gynecol 1991; 165: 131–137
  • Saito S, Kasahara T, Sakakura S, Umekage H, Harada N, Ichijo M. Detection and localization of interleukin-8 mRNA and protein in human placenta and decidual tissues. J Reprod Immunol 1994; 27: 161–172
  • Blumenstein M, Keelan J A, Bowen-Shauver J M, Mitchell M D. Suppressors of cytokine signaling proteins in human preterm placental tissues. J Mol Endocrinol 2005; 35: 165–175
  • Moussa M, Mognetti B, Dubanchet S, Menu E, Roques P, Dormont D, Barre-Sinoussi F, Chaouat G. Expression of beta chemokines in explants and trophoblasts from early and term human placentae. Am J Reprod Immunol 2001; 46: 309–317
  • 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; 13: 119–128
  • 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; 178: 436–445
  • Than G N, Bohn H, Szabo D G. Advances in pregnancy-related protein research. CRC Press, Boca Raton, FL 1993; 1–333
  • Chaouat G, Ledee-Bataille N, Zourbas S, Ostojic S, Dubanchet S, Martal J, Frydman R. Cytokines, implantation and early abortion: Re-examining the Th1/Th2 paradigm leads to question the single pathway, single therapy concept. Am J Reprod Immunol 2003; 50: 177–186
  • Keelan J A, Mitchell M D. Placental cytokines and preeclampsia. Front Biosci 2007; 12: 2706–2727
  • Hunt J S, Vassmer D, Ferguson T A, Miller L. Fas ligand is positioned in mouse uterus and placenta to prevent trafficking of activated leukocytes between the mother and the conceptus. J Immunol 1997; 158: 4122–4128
  • Munn D H, Zhou M, Attwood J T, Bondarev I, Conway S J, Marshall B, Brown C, Mellor A L. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 1998; 281: 1191–1193
  • Phillips T A, Ni J, Pan G, Ruben S M, Wei Y F, Pace J L, Hunt J S. TRAIL (Apo-2L) and TRAIL receptors in human placentas: Implications for immune privilege. J Immunol 1999; 162: 6053–6059
  • Kayisli U A, Selam B, Guzeloglu-Kayisli O, Demir R, Arici A. Human chorionic gonadotropin contributes to maternal immunotolerance and endometrial apoptosis by regulating Fas–Fas ligand system. J Immunol 2003; 171: 2305–2313
  • Niederkorn J Y. See no evil, hear no evil, do no evil: The lessons of immune privilege. Nat Immunol 2006; 7: 354–359
  • Lei Z M, Yang M, Li X, Takikawa O, Rao C V. Upregulation of placental indoleamine 2,3-dioxygenase by human chorionic gonadotropin. Biol Reprod 2007; 76: 639–644
  • Rabinovich G A, Ariel A, Hershkovitz 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; 97: 100–106
  • 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; 44: 506–513
  • Rorive S, Belot N, Decaestecker C, Lefranc F, Gordower L, Micik S, Maurage C A, Kaltner H, Ruchoux M M, Danguy A, et al. Galectin-1 is highly expressed in human gliomas with relevance for modulation of invasion of tumor astrocytes into the brain parenchyma. Glia 2001; 33: 241–255
  • Camby I, Belot N, Rorive S, Lefranc F, Maurage C A, Lahm H, Kaltner H, Hadari Y, Ruchoux M M, Brotchi J, et al. Galectins are differentially expressed in supratentorial pilocytic astrocytomas, astrocytomas, anaplastic astrocytomas and glioblastomas, and significantly modulate tumor astrocyte migration. Brain Pathol 2001; 11: 12–26
  • Le Q T, Shi G, Cao H, Nelson D W, Wang Y, Chen E Y, Zhao S, Kong C, Richardson D, O'Byrne K J, et al. Galectin-1: A link between tumor hypoxia and tumor immune privilege. J Clin Oncol 2005; 23: 8932–8941
  • Saussez S, Lorfevre F, Lequeux T, Laurent G, Chantrain G, Vertongen F, Toubeau G, Decaestecker C, Kiss R. The determination of the levels of circulating galectin-1 and -3 in HNSCC patients could be used to monitor tumor progression and/or responses to therapy. Oral Oncol 2008; 44: 86–93
  • Daroqui C M, Ilarregui J M, Rubinstein N, Salatino M, Toscano M A, Vazquez P, Bakin A, Puricelli L, Bal de Kier J E, Rabinovich G A. Regulation of galectin-1 expression by transforming growth factor beta1 in metastatic mammary adenocarcinoma cells: Implications for tumor-immune escape. Cancer Immunol Immunother 2007; 56: 491–499
  • Koopman L A, Kopcow H D, Rybalov B, Boyson J E, Orange J S, Schatz F, Masch R, Lockwood C J, Schachter A D, Park P J, et al. Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J Exp Med 2003; 198: 1201–1212
  • Aluvihare V R, Kallikourdis M, Betz A G. Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 2004; 5: 266–271
  • Trowsdale J, Betz A G. Mother's little helpers: Mechanisms of maternal–fetal tolerance. Nat Immunol 2006; 7: 241–246
  • 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, et al. A pivotal role for galectin-1 in fetomaternal tolerance. Nat Med 2007; 13: 1450–1457
  • Than N G, Wildman D E, Erez O, Edwin S S, Espinoza J, Kim C J, Han Y M, Mazaki-Tovi S, Kusanovic J P, Hassan S, et al. Trophoblast, galectin-1 and pre-eclampsia. Am J Obstet Gynecol 2006; 195: S138
  • Wilczynski J R. Immunological analogy between allograft rejection, recurrent abortion and pre-eclampsia—the same basic mechanism. Hum Immunol 2006; 67: 492–511
  • van der Leij J, van den Berg A, Blokzijl T, Harms G, van Goor H, Zwiers P, van Weeghel R, Poppema S, Visser L. Dimeric galectin-1 induces IL-10 production in T-lymphocytes: An important tool in the regulation of the immune response. J Pathol 2004; 204: 511–518
  • 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; 267: 177–185
  • Keelan J A, Marvin K W, Sato T A, Coleman M, McCowan L M, Mitchell M D. Cytokine abundance in placental tissues: Evidence of inflammatory activation in gestational membranes with term and preterm parturition. Am J Obstet Gynecol 1999; 181: 1530–1536
  • Starzl T E, Zinkernagel R M. Antigen localization and migration in immunity and tolerance. N Engl J Med 1998; 339: 1905–1913
  • Matzinger P. The danger model: A renewed sense of self. Science 2002; 296: 301–305
  • Sato S. Galectins as molecules of danger signal, which could evoke an immune response to infection. Trends Glycosci Glyc 2002; 14: 285–301
  • Moffett A, Loke C. Immunology of placentation in eutherian mammals. Nat Rev Immunol 2006; 6: 584–594

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