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Thromb Haemost 2019; 119(08): 1265-1273
DOI: 10.1055/s-0039-1692720
Theme Issue Article
Georg Thieme Verlag KG Stuttgart · New York

Glycans and Glycan-Binding Proteins in Atherosclerosis

Veit Eckardt
1   Institute for Cardiovascular Prevention, Faculty of Medicine, Ludwig-Maximilians-Universität München, Munich, Germany
,
Christian Weber
1   Institute for Cardiovascular Prevention, Faculty of Medicine, Ludwig-Maximilians-Universität München, Munich, Germany
2   German Centre for Cardiovascular Research, Partner Site Munich Heart Alliance, Munich, Germany
,
Philipp von Hundelshausen 
1   Institute for Cardiovascular Prevention, Faculty of Medicine, Ludwig-Maximilians-Universität München, Munich, Germany
2   German Centre for Cardiovascular Research, Partner Site Munich Heart Alliance, Munich, Germany
› Author Affiliations Funding This work was supported by Deutsche Forschungsgemeinschaft (SFB914 B08 [to C.W.], SFB1123 A1 [to C.W.], A2 [to P.v.H], INST 409/150–1 FUGG [to C.W.]).
Further Information

Publication History

08 March 2019

14 May 2019

Publication Date:
02 July 2019 (online)

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Abstract

Complex glycans are readily accessible on the endothelium and on cell and plasma components. They interact with glycan-binding proteins which translate their structure into function. Advanced analytical tools are available to investigate their structure and functional interactions. Modifications to glycan structures which alter their capacity to bind proteins are particularly relevant in atherosclerosis. We summarize the regulatory role of glycans and their binding partners in the development of the disease. Given their complexity, accessibility, and important functional role, glycans and glycan-binding proteins represent promising diagnostic tools and therapeutic targets.

Keywords

glycocalyx - glycosaminoglycan - chemokine - selectin - galectin - low-density lipoprotein

Note: The review process for this paper was fully handled by Gregory Y. H. Lip, Editor-in-Chief.


 

  • References

  • 1 Rakus JF, Mahal LK. New technologies for glycomic analysis: toward a systematic understanding of the glycome. Annu Rev Anal Chem (Palo Alto, Calif) 2011; 4: 367-392
    CrossrefPubMedGoogle Scholar
  • 2 Ohtsubo K, Marth JD. Glycosylation in cellular mechanisms of health and disease. Cell 2006; 126 (05) 855-867
    CrossrefPubMedGoogle Scholar
  • 3 Landsteiner K. Ueber Agglutinationserscheinungen normalen menschlichen Blutes. Wien Klin Wochenschr 1901; 46: 1132-1134
    PubMedGoogle Scholar
  • 4 Watkins WM, Morgan WTJ. Neutralization of the anti-H agglutinin in eel serum by simple sugars. Nature 1952; 169 (4307): 825-826
    CrossrefPubMedGoogle Scholar
  • 5 Watkins WM, Morgan WTJ. Inhibition by simple sugars of enzymes which decompose the blood-group substances. Nature 1955; 175 (4459): 676-677
    CrossrefPubMedGoogle Scholar
  • 6 Schunkert H, König IR, Kathiresan S. , et al; Cardiogenics; CARDIoGRAM Consortium. Large-scale association analysis identifies 13 new susceptibility loci for coronary artery disease. Nat Genet 2011; 43 (04) 333-338
    CrossrefPubMedGoogle Scholar
  • 7 Teslovich TM, Musunuru K, Smith AV. , et al. Biological, clinical and population relevance of 95 loci for blood lipids. Nature 2010; 466 (7307): 707-713
    CrossrefPubMedGoogle Scholar
  • 8 Reilly MP, Li M, He J. , et al; Myocardial Infarction Genetics Consortium; Wellcome Trust Case Control Consortium. Identification of ADAMTS7 as a novel locus for coronary atherosclerosis and association of ABO with myocardial infarction in the presence of coronary atherosclerosis: two genome-wide association studies. Lancet 2011; 377 (9763): 383-392
    CrossrefPubMedGoogle Scholar
  • 9 Zhong M, Zhang H, Reilly JP. , et al. ABO blood group as a model for platelet glycan modification in arterial thrombosis. Arterioscler Thromb Vasc Biol 2015; 35 (07) 1570-1578
    CrossrefPubMedGoogle Scholar
  • 10 Stillmark H. Ueber Ricin, ein giftiges Ferment aus den Samen von Ricinus comm. L. und einigen anderen Euphorbiaceen [M.D. dissertation]. Dorpat: Kaiserliche Universität zu Dorpat; 1888
    PubMedGoogle Scholar
  • 11 Gabius H-J, Siebert H-C, André S, Jiménez-Barbero J, Rüdiger H. Chemical biology of the sugar code. ChemBioChem 2004; 5 (06) 740-764
    CrossrefPubMedGoogle Scholar
  • 12 Sharon N, Lis H. History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology 2004; 14 (11) 53R-62R
    CrossrefPubMedGoogle Scholar
  • 13 Lindahl U. Heparan sulfate-protein interactions--a concept for drug design?. Thromb Haemost 2007; 98 (01) 109-115
    Article in Thieme ConnectPubMedGoogle Scholar
  • 14 Petitou M, van Boeckel CAA. A synthetic antithrombin III binding pentasaccharide is now a drug! What comes next?. Angew Chem Int Ed Engl 2004; 43 (24) 3118-3133
    CrossrefPubMedGoogle Scholar
  • 15 Mueller RL, Scheidt S. History of drugs for thrombotic disease. Discovery, development, and directions for the future. Circulation 1994; 89 (01) 432-449
    CrossrefPubMedGoogle Scholar
  • 16 Marki A, Esko JD, Pries AR, Ley K. Role of the endothelial surface layer in neutrophil recruitment. J Leukoc Biol 2015; 98 (04) 503-515
    CrossrefPubMedGoogle Scholar
  • 17 Tarbell JM, Cancel LM. The glycocalyx and its significance in human medicine. J Intern Med 2016; 280 (01) 97-113
    CrossrefPubMedGoogle Scholar
  • 18 Taylor ME, Drickamer K, Schnaar RL, Etzler ME, Varki A. Discovery and classification of glycan-binding proteins. In: Varki A, Cummings RD, Esko JD. , et al, eds. Essentials of Glycobiology. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 2015: 361-372
    Google Scholar
  • 19 Cummings RD. The repertoire of glycan determinants in the human glycome. Mol Biosyst 2009; 5 (10) 1087-1104
    CrossrefPubMedGoogle Scholar
  • 20 Yang Y, Franc V, Heck AJR. Glycoproteomics: a balance between high-throughput and in-depth analysis. Trends Biotechnol 2017; 35 (07) 598-609
    CrossrefPubMedGoogle Scholar
  • 21 Palaniappan KK, Bertozzi CR. Chemical glycoproteomics. Chem Rev 2016; 116 (23) 14277-14306
    CrossrefPubMedGoogle Scholar
  • 22 Smith DF, Cummings RD. Application of microarrays for deciphering the structure and function of the human glycome. Mol Cell Proteomics 2013; 12 (04) 902-912
    CrossrefPubMedGoogle Scholar
  • 23 Hirabayashi J, Yamada M, Kuno A, Tateno H. Lectin microarrays: concept, principle and applications. Chem Soc Rev 2013; 42 (10) 4443-4458
    CrossrefPubMedGoogle Scholar
  • 24 Sieve I, Münster-Kühnel AK, Hilfiker-Kleiner D. Regulation and function of endothelial glycocalyx layer in vascular diseases. Vascul Pharmacol 2018; 100: 26-33
    CrossrefPubMedGoogle Scholar
  • 25 Scott DW, Patel RP. Endothelial heterogeneity and adhesion molecules N-glycosylation: implications in leukocyte trafficking in inflammation. Glycobiology 2013; 23 (06) 622-633
    CrossrefPubMedGoogle Scholar
  • 26 Aird WC. Spatial and temporal dynamics of the endothelium. J Thromb Haemost 2005; 3 (07) 1392-1406
    CrossrefPubMedGoogle Scholar
  • 27 Hahn C, Schwartz MA. Mechanotransduction in vascular physiology and atherogenesis. Nat Rev Mol Cell Biol 2009; 10 (01) 53-62
    PubMedGoogle Scholar
  • 28 Handel TM, Johnson Z, Crown SE, Lau EK, Proudfoot AE. Regulation of protein function by glycosaminoglycans--as exemplified by chemokines. Annu Rev Biochem 2005; 74: 385-410
    CrossrefPubMedGoogle Scholar
  • 29 Weber C, Badimon L, Mach F, van der Vorst EPC. Therapeutic strategies for atherosclerosis and atherothrombosis: past, present and future. Thromb Haemost 2017; 117 (07) 1258-1264
    Article in Thieme ConnectPubMedGoogle Scholar
  • 30 Gisterå A, Hansson GK. The immunology of atherosclerosis. Nat Rev Nephrol 2017; 13 (06) 368-380
    PubMedGoogle Scholar
  • 31 Reitsma S, Oude Egbrink MGA, Heijnen VVT. , et al. Endothelial glycocalyx thickness and platelet-vessel wall interactions during atherogenesis. Thromb Haemost 2011; 106 (05) 939-946
    Article in Thieme ConnectPubMedGoogle Scholar
  • 32 Massberg S, Brand K, Grüner S. , et al. A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation. J Exp Med 2002; 196 (07) 887-896
    CrossrefPubMedGoogle Scholar
  • 33 Nagy N, Freudenberger T, Melchior-Becker A. , et al. Inhibition of hyaluronan synthesis accelerates murine atherosclerosis: novel insights into the role of hyaluronan synthesis. Circulation 2010; 122 (22) 2313-2322
    CrossrefPubMedGoogle Scholar
  • 34 Reine TM, Kusche-Gullberg M, Feta A, Jenssen T, Kolset SO. Heparan sulfate expression is affected by inflammatory stimuli in primary human endothelial cells. Glycoconj J 2012; 29 (01) 67-76
    CrossrefPubMedGoogle Scholar
  • 35 Nieuwdorp M, Meuwese MC, Mooij HL. , et al. Tumor necrosis factor-α inhibition protects against endotoxin-induced endothelial glycocalyx perturbation. Atherosclerosis 2009; 202 (01) 296-303
    CrossrefPubMedGoogle Scholar
  • 36 Nieuwdorp M, Holleman F, de Groot E. , et al. Perturbation of hyaluronan metabolism predisposes patients with type 1 diabetes mellitus to atherosclerosis. Diabetologia 2007; 50 (06) 1288-1293
    CrossrefPubMedGoogle Scholar
  • 37 van den Berg BM, Spaan JAE, Vink H. Impaired glycocalyx barrier properties contribute to enhanced intimal low-density lipoprotein accumulation at the carotid artery bifurcation in mice. Pflugers Arch 2009; 457 (06) 1199-1206
    CrossrefPubMedGoogle Scholar
  • 38 Ori A, Wilkinson MC, Fernig DG. A systems biology approach for the investigation of the heparin/heparan sulfate interactome. J Biol Chem 2011; 286 (22) 19892-19904
    CrossrefPubMedGoogle Scholar
  • 39 Ricard-Blum S, Lisacek F. Glycosaminoglycanomics: where we are. Glycoconj J 2017; 34 (03) 339-349
    CrossrefPubMedGoogle Scholar
  • 40 Xu D, Esko JD. Demystifying heparan sulfate-protein interactions. Annu Rev Biochem 2014; 83: 129-157
    CrossrefPubMedGoogle Scholar
  • 41 Gerhardt T, Ley K. Monocyte trafficking across the vessel wall. Cardiovasc Res 2015; 107 (03) 321-330
    CrossrefPubMedGoogle Scholar
  • 42 Axelsson J, Xu D, Kang BN. , et al. Inactivation of heparan sulfate 2-O-sulfotransferase accentuates neutrophil infiltration during acute inflammation in mice. Blood 2012; 120 (08) 1742-1751
    PubMedGoogle Scholar
  • 43 Wang L, Fuster M, Sriramarao P, Esko JD. Endothelial heparan sulfate deficiency impairs L-selectin- and chemokine-mediated neutrophil trafficking during inflammatory responses. Nat Immunol 2005; 6 (09) 902-910
    CrossrefPubMedGoogle Scholar
  • 44 Koenen RR, von Hundelshausen P, Nesmelova IV. , et al. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat Med 2009; 15 (01) 97-103
    CrossrefPubMedGoogle Scholar
  • 45 von Hundelshausen P, Koenen RR, Sack M. , et al. Heterophilic interactions of platelet factor 4 and RANTES promote monocyte arrest on endothelium. Blood 2005; 105 (03) 924-930
    CrossrefPubMedGoogle Scholar
  • 46 von Hundelshausen P, Agten SM, Eckardt V. , et al. Chemokine interactome mapping enables tailored intervention in acute and chronic inflammation. Sci Transl Med 2017; 9 (384) eaah6650
    CrossrefPubMedGoogle Scholar
  • 47 Wang L, Brown JR, Varki A, Esko JD. Heparin's anti-inflammatory effects require glucosamine 6-O-sulfation and are mediated by blockade of L- and P-selectins. J Clin Invest 2002; 110 (01) 127-136
    CrossrefPubMedGoogle Scholar
  • 48 Rehm M, Bruegger D, Christ F. , et al. Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia. Circulation 2007; 116 (17) 1896-1906
    CrossrefPubMedGoogle Scholar
  • 49 Vigetti D, Genasetti A, Karousou E. , et al. Proinflammatory cytokines induce hyaluronan synthesis and monocyte adhesion in human endothelial cells through hyaluronan synthase 2 (HAS2) and the nuclear factor-kappaB (NF-kappaB) pathway. J Biol Chem 2010; 285 (32) 24639-24645
    CrossrefPubMedGoogle Scholar
  • 50 Homann S, Grandoch M, Kiene LS. , et al. Hyaluronan synthase 3 promotes plaque inflammation and atheroprogression. Matrix Biol 2018; 66: 67-80
    CrossrefPubMedGoogle Scholar
  • 51 Grandoch M, Bollyky PL, Fischer JW. Hyaluronan: a master switch between vascular homeostasis and inflammation. Circ Res 2018; 122 (10) 1341-1343
    CrossrefPubMedGoogle Scholar
  • 52 Skålén K, Gustafsson M, Rydberg EK. , et al. Subendothelial retention of atherogenic lipoproteins in early atherosclerosis. Nature 2002; 417 (6890): 750-754
    CrossrefPubMedGoogle Scholar
  • 53 Gustafsen C, Olsen D, Vilstrup J. , et al. Heparan sulfate proteoglycans present PCSK9 to the LDL receptor. Nat Commun 2017; 8 (01) 503
    CrossrefPubMedGoogle Scholar
  • 54 Weber C. Platelets and chemokines in atherosclerosis: partners in crime. Circ Res 2005; 96 (06) 612-616
    CrossrefPubMedGoogle Scholar
  • 55 Coenen DM, Mastenbroek TG, Cosemans JMEM. Platelet interaction with activated endothelium: mechanistic insights from microfluidics. Blood 2017; 130 (26) 2819-2828
    CrossrefPubMedGoogle Scholar
  • 56 McEver RP. Selectins: initiators of leucocyte adhesion and signalling at the vascular wall. Cardiovasc Res 2015; 107 (03) 331-339
    CrossrefPubMedGoogle Scholar
  • 57 Wagner DD, Frenette PS. The vessel wall and its interactions. Blood 2008; 111 (11) 5271-5281
    CrossrefPubMedGoogle Scholar
  • 58 Sperandio M, Gleissner CA, Ley K. Glycosylation in immune cell trafficking. Immunol Rev 2009; 230 (01) 97-113
    CrossrefPubMedGoogle Scholar
  • 59 Eriksson EE, Xie X, Werr J, Thoren P, Lindbom L. Importance of primary capture and L-selectin-dependent secondary capture in leukocyte accumulation in inflammation and atherosclerosis in vivo. J Exp Med 2001; 194 (02) 205-218
    CrossrefPubMedGoogle Scholar
  • 60 Cambi A, Figdor CG. Dual function of C-type lectin-like receptors in the immune system. Curr Opin Cell Biol 2003; 15 (05) 539-546
    CrossrefPubMedGoogle Scholar
  • 61 Sperandio M, Smith ML, Forlow SB. , et al. P-selectin glycoprotein ligand-1 mediates L-selectin-dependent leukocyte rolling in venules. J Exp Med 2003; 197 (10) 1355-1363
    CrossrefPubMedGoogle Scholar
  • 62 Zarbock A, Ley K, McEver RP, Hidalgo A. Leukocyte ligands for endothelial selectins: specialized glycoconjugates that mediate rolling and signaling under flow. Blood 2011; 118 (26) 6743-6751
    CrossrefPubMedGoogle Scholar
  • 63 An G, Wang H, Tang R. , et al. P-selectin glycoprotein ligand-1 is highly expressed on Ly-6Chi monocytes and a major determinant for Ly-6Chi monocyte recruitment to sites of atherosclerosis in mice. Circulation 2008; 117 (25) 3227-3237
    CrossrefPubMedGoogle Scholar
  • 64 Dong ZM, Chapman SM, Brown AA, Frenette PS, Hynes RO, Wagner DD. The combined role of P- and E-selectins in atherosclerosis. J Clin Invest 1998; 102 (01) 145-152
    CrossrefPubMedGoogle Scholar
  • 65 Quach ME, Chen W, Li R. Mechanisms of platelet clearance and translation to improve platelet storage. Blood 2018; 131 (14) 1512-1521
    CrossrefPubMedGoogle Scholar
  • 66 Wandall HH, Rumjantseva V, Sørensen AL. , et al. The origin and function of platelet glycosyltransferases. Blood 2012; 120 (03) 626-635
    PubMedGoogle Scholar
  • 67 Sørensen AL, Rumjantseva V, Nayeb-Hashemi S. , et al. Role of sialic acid for platelet life span: exposure of β-galactose results in the rapid clearance of platelets from the circulation by asialoglycoprotein receptor-expressing liver macrophages and hepatocytes. Blood 2009; 114 (08) 1645-1654
    PubMedGoogle Scholar
  • 68 Grewal PK, Uchiyama S, Ditto D. , et al. The Ashwell receptor mitigates the lethal coagulopathy of sepsis. Nat Med 2008; 14 (06) 648-655
    CrossrefPubMedGoogle Scholar
  • 69 Ward SE, O'Sullivan JM, Drakeford C. , et al. A novel role for the macrophage galactose-type lectin receptor in mediating von Willebrand factor clearance. Blood 2018; 131 (08) 911-916
    CrossrefPubMedGoogle Scholar
  • 70 Li Y, Fu J, Ling Y. , et al. Sialylation on O-glycans protects platelets from clearance by liver Kupffer cells. Proc Natl Acad Sci U S A 2017; 114 (31) 8360-8365
    CrossrefPubMedGoogle Scholar
  • 71 Nioi P, Sigurdsson A, Thorleifsson G. , et al. Variant ASGR1 associated with a reduced risk of coronary artery disease. N Engl J Med 2016; 374 (22) 2131-2141
    CrossrefPubMedGoogle Scholar
  • 72 Yang A, Gyulay G, Mitchell M, White E, Trigatti BL, Igdoura SA. Hypomorphic sialidase expression decreases serum cholesterol by downregulation of VLDL production in mice. J Lipid Res 2012; 53 (12) 2573-2585
    CrossrefPubMedGoogle Scholar
  • 73 Bartlett AL, Grewal T, De Angelis E, Myers S, Stanley KK. Role of the macrophage galactose lectin in the uptake of desialylated LDL. Atherosclerosis 2000; 153 (01) 219-230
    CrossrefPubMedGoogle Scholar
  • 74 Ray KK, Landmesser U, Leiter LA. , et al. Inclisiran in patients at high cardiovascular risk with elevated LDL cholesterol. N Engl J Med 2017; 376 (15) 1430-1440
    CrossrefPubMedGoogle Scholar
  • 75 Nair JK, Willoughby JLS, Chan A. , et al. Multivalent N-acetylgalactosamine-conjugated siRNA localizes in hepatocytes and elicits robust RNAi-mediated gene silencing. J Am Chem Soc 2014; 136 (49) 16958-16961
    CrossrefPubMedGoogle Scholar
  • 76 Pothineni NVK, Karathanasis SK, Ding Z, Arulandu A, Varughese KI, Mehta JL. LOX-1 in atherosclerosis and myocardial ischemia: biology, genetics, and modulation. J Am Coll Cardiol 2017; 69 (22) 2759-2768
    CrossrefPubMedGoogle Scholar
  • 77 Chen M, Kakutani M, Naruko T. , et al. Activation-dependent surface expression of LOX-1 in human platelets. Biochem Biophys Res Commun 2001; 282 (01) 153-158
    CrossrefPubMedGoogle Scholar
  • 78 Chatterjee M, Rath D, Schlotterbeck J. , et al. Regulation of oxidized platelet lipidome: implications for coronary artery disease. Eur Heart J 2017; 38 (25) 1993-2005
    CrossrefPubMedGoogle Scholar
  • 79 Hayashida K, Kume N, Murase T. , et al. Serum soluble lectin-like oxidized low-density lipoprotein receptor-1 levels are elevated in acute coronary syndrome: a novel marker for early diagnosis. Circulation 2005; 112 (06) 812-818
    CrossrefPubMedGoogle Scholar
  • 80 Matthijsen RA, de Winther MPJ, Kuipers D. , et al. Macrophage-specific expression of mannose-binding lectin controls atherosclerosis in low-density lipoprotein receptor-deficient mice. Circulation 2009; 119 (16) 2188-2195
    CrossrefPubMedGoogle Scholar
  • 81 Saevarsdottir S, Oskarsson OO, Aspelund T. , et al. Mannan binding lectin as an adjunct to risk assessment for myocardial infarction in individuals with enhanced risk. J Exp Med 2005; 201 (01) 117-125
    CrossrefPubMedGoogle Scholar
  • 82 Varki A, Schnaar RL, Crocker PR. I-type lectins. In: Varki A, Cummings RD, Esko JD. , et al, eds. Essentials of Glycobiology. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 2015: 453-467
    Google Scholar
  • 83 Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 2007; 7 (09) 678-689
    CrossrefPubMedGoogle Scholar
  • 84 Xiong Y-S, Wu A-L, Lin Q-S. , et al. Contribution of monocytes Siglec-1 in stimulating T cells proliferation and activation in atherosclerosis. Atherosclerosis 2012; 224 (01) 58-65
    CrossrefPubMedGoogle Scholar
  • 85 Xiong Y-S, Wu A-L, Mu D. , et al. Inhibition of siglec-1 by lentivirus mediated small interfering RNA attenuates atherogenesis in apoE-deficient mice. Clin Immunol 2017; 174: 32-40
    CrossrefPubMedGoogle Scholar
  • 86 Xiong Y-S, Zhou Y-H, Rong G-H. , et al. Siglec-1 on monocytes is a potential risk marker for monitoring disease severity in coronary artery disease. Clin Biochem 2009; 42 (10-11): 1057-1063
    CrossrefPubMedGoogle Scholar
  • 87 Draude G, von Hundelshausen P, Frankenberger M, Ziegler-Heitbrock HW, Weber C. Distinct scavenger receptor expression and function in the human CD14(+)/CD16(+) monocyte subset. Am J Physiol 1999; 276 (04) H1144-H1149
    PubMedGoogle Scholar
  • 88 Miller MC, Ludwig A-K, Wichapong K. , et al. Adhesion/growth-regulatory galectins tested in combination: evidence for formation of hybrids as heterodimers. Biochem J 2018; 475 (05) 1003-1018
    CrossrefPubMedGoogle Scholar
  • 89 Gabius H-J, Manning JC, Kopitz J, André S, Kaltner H. Sweet complementarity: the functional pairing of glycans with lectins. Cell Mol Life Sci 2016; 73 (10) 1989-2016
    CrossrefPubMedGoogle Scholar
  • 90 Stowell SR, Arthur CM, Mehta P. , et al. Galectin-1, -2, and -3 exhibit differential recognition of sialylated glycans and blood group antigens. J Biol Chem 2008; 283 (15) 10109-10123
    CrossrefPubMedGoogle Scholar
  • 91 Saint-Lu N, Oortwijn BD, Pegon JN. , et al. Identification of galectin-1 and galectin-3 as novel partners for von Willebrand factor. Arterioscler Thromb Vasc Biol 2012; 32 (04) 894-901
    CrossrefPubMedGoogle Scholar
  • 92 O'Sullivan JM, Jenkins PV, Rawley O. , et al. Galectin-1 and galectin-3 constitute novel-binding partners for factor VIII. Arterioscler Thromb Vasc Biol 2016; 36 (05) 855-863
    CrossrefPubMedGoogle Scholar
  • 93 Romaniuk MA, Croci DO, Lapponi MJ. , et al. Binding of galectin-1 to αIIbβ3 integrin triggers “outside-in” signals, stimulates platelet activation, and controls primary hemostasis. FASEB J 2012; 26 (07) 2788-2798
    CrossrefPubMedGoogle Scholar
  • 94 Pacienza N, Pozner RG, Bianco GA. , et al. The immunoregulatory glycan-binding protein galectin-1 triggers human platelet activation. FASEB J 2008; 22 (04) 1113-1123
    CrossrefPubMedGoogle Scholar
  • 95 Bombeli T, Schwartz BR, Harlan JM. Adhesion of activated platelets to endothelial cells: evidence for a GPIIbIIIa-dependent bridging mechanism and novel roles for endothelial intercellular adhesion molecule 1 (ICAM-1), alphavbeta3 integrin, and GPIbalpha. J Exp Med 1998; 187 (03) 329-339
    CrossrefPubMedGoogle Scholar
  • 96 Cattaneo V, Tribulatti MV, Carabelli J, Carestia A, Schattner M, Campetella O. Galectin-8 elicits pro-inflammatory activities in the endothelium. Glycobiology 2014; 24 (10) 966-973
    CrossrefPubMedGoogle Scholar
  • 97 Romaniuk MA, Tribulatti MV, Cattaneo V. , et al. Human platelets express and are activated by galectin-8. Biochem J 2010; 432 (03) 535-547
    CrossrefPubMedGoogle Scholar
  • 98 MacKinnon AC, Liu X, Hadoke PWF, Miller MR, Newby DE, Sethi T. Inhibition of galectin-3 reduces atherosclerosis in apolipoprotein E-deficient mice. Glycobiology 2013; 23 (06) 654-663
    CrossrefPubMedGoogle Scholar
  • 99 Papaspyridonos M, McNeill E, de Bono JP. , et al. Galectin-3 is an amplifier of inflammation in atherosclerotic plaque progression through macrophage activation and monocyte chemoattraction. Arterioscler Thromb Vasc Biol 2008; 28 (03) 433-440
    CrossrefPubMedGoogle Scholar
  • 100 Liu F-T, Hsu DK, Zuberi RI, Kuwabara I, Chi EY, Henderson Jr WR. Expression and function of galectin-3, a β-galactoside-binding lectin, in human monocytes and macrophages. Am J Pathol 1995; 147 (04) 1016-1028
    PubMedGoogle Scholar
  • 101 Kim K, Mayer EP, Nachtigal M. Galectin-3 expression in macrophages is signaled by Ras/MAP kinase pathway and up-regulated by modified lipoproteins. Biochim Biophys Acta 2003; 1641 (01) 13-23
    PubMedGoogle Scholar
  • 102 Zhu W, Sano H, Nagai R, Fukuhara K, Miyazaki A, Horiuchi S. The role of galectin-3 in endocytosis of advanced glycation end products and modified low density lipoproteins. Biochem Biophys Res Commun 2001; 280 (04) 1183-1188
    CrossrefPubMedGoogle Scholar
  • 103 Rong JX, Shapiro M, Trogan E, Fisher EA. Transdifferentiation of mouse aortic smooth muscle cells to a macrophage-like state after cholesterol loading. Proc Natl Acad Sci U S A 2003; 100 (23) 13531-13536
    CrossrefPubMedGoogle Scholar
  • 104 Nachtigal M, Ghaffar A, Mayer EP. Galectin-3 gene inactivation reduces atherosclerotic lesions and adventitial inflammation in ApoE-deficient mice. Am J Pathol 2008; 172 (01) 247-255
    CrossrefPubMedGoogle Scholar