An adipose tissue galectin controls endothelial cell function via preferential recognition of 3-fucosylated glycans.


Journal

FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484

Informations de publication

Date de publication:
01 2020
Historique:
received: 19 07 2019
revised: 08 10 2019
accepted: 21 10 2019
entrez: 10 1 2020
pubmed: 10 1 2020
medline: 8 7 2020
Statut: ppublish

Résumé

Upon overnutrition, adipocytes activate a homeostatic program to adjust anabolic pressure. An inflammatory response enables adipose tissue (AT) expansion with concomitant enlargement of its capillary network, and reduces energy storage by increasing insulin resistance. Galectin-12 (Gal-12), an endogenous lectin preferentially expressed in AT, plays a key role in adipocyte differentiation, lipolysis, and glucose homeostasis. Here, we reveal biochemical and biophysical determinants of Gal-12 structure, including its preferential recognition of 3-fucosylated structures, a unique feature among members of the galectin family. Furthermore, we identify a previously unanticipated role for this lectin in the regulation of angiogenesis within AT. Gal-12 showed preferential localization within the inner side of lipid droplets, and its expression was upregulated under hypoxic conditions. Through glycosylation-dependent binding to endothelial cells, Gal-12 promoted in vitro angiogenesis. Moreover, analysis of in vivo AT vasculature showed reduced vascular networks in Gal-12-deficient (Lgals12

Identifiants

pubmed: 31914594
doi: 10.1096/fj.201901817R
doi:

Substances chimiques

Galectins 0
Polysaccharides 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

735-753

Informations de copyright

© 2019 Federation of American Societies for Experimental Biology.

Références

Grant RW, Dixit VD. Adipose tissue as an immunological organ. Obesity (Silver Spring). 2015;23:512‐518.
Grant R, Youm Y‐H, Ravussin A, Dixit VD. Quantification of adipose tissue leukocytosis in obesity. Methods Mol Biol. 2013;1040:195‐209.
Reilly SM, Saltiel AR. Adapting to obesity with adipose tissue inflammation. Nat Rev Endocrinol. 2017;13:633‐643.
Cao Y. Angiogenesis and vascular functions in modulation of obesity, adipose metabolism, and insulin sensitivity. Cell Metab. 2013;18:478‐489.
Vasta GR. Galectins as pattern recognition receptors: structure, function, and evolution. Adv Exp Med Biol. 2012;946:21‐36.
Rabinovich GA, Toscano MA. Turning “sweet” on immunity: galectin‐glycan interactions in immune tolerance and inflammation. Nat Rev Immunol. 2009;9:338‐352.
Croci DO, Cerliani JP, Pinto NA, Morosi LG, Rabinovich GA. Regulatory role of glycans in the control of hypoxia‐driven angiogenesis and sensitivity to anti‐angiogenic treatment. Glycobiology. 2014;24:1283‐1290.
Cerliani JP, Blidner AG, Toscano MA, Croci DO, Rabinovich GA. Translating the “Sugar Code” into immune and vascular signaling programs. Trends Biochem Sci. 2017;42:255‐273.
Rabinovich GA, Toscano MA, Jackson SS, Vasta GR. Functions of cell surface galectin‐glycoprotein lattices. Curr Opin Struct Biol. 2007;17:513‐520.
Liu F‐T, Patterson RJ, Wang JL. Intracellular functions of galectins. Biochim Biophys Acta. 2002;1572:263‐273.
Hirabayashi J, Kasai K. The family of metazoan metal‐independent beta‐galactoside‐binding lectins: structure, function and molecular evolution. Glycobiology. 1993;3:297‐304.
Cagnoni AJ, Perez Saez JM, Rabinovich GA, Marino KV. Turning‐off signaling by siglecs, selectins, and galectins: chemical inhibition of glycan‐dependent interactions in cancer. Front Oncol. 2016;6:109.
Dam TK, Brewer CF. Lectins as pattern recognition molecules: the effects of epitope density in innate immunity. Glycobiology. 2010;20:270‐279.
Dam TK, Brewer CF. Maintenance of cell surface glycan density by lectin‐glycan interactions: a homeostatic and innate immune regulatory mechanism. Glycobiology. 2010;20:1061‐1064.
Nio‐Kobayashi J. Tissue‐ and cell‐specific localization of galectins, β‐galactose‐binding animal lectins, and their potential functions in health and disease. Anat Sci Int. 2016;92:25‐36.
Sundblad V, Morosi LG, Geffner JR, Rabinovich GA. Galectin‐1: a jack‐of‐all‐trades in the resolution of acute and chronic inflammation. J Immunol. 2017;199:3721‐3730.
Ilarregui JM, Bianco GA, Toscano MA, Rabinovich GA. The coming of age of galectins as immunomodulatory agents: impact of these carbohydrate binding proteins in T cell physiology and chronic inflammatory disorders. Ann Rheum Dis. 2005;64(suppl_4):iv96–iv103.
Yang R‐Y, Hsu DK, Yu L, Chen H‐Y, Liu F‐T. Galectin‐12 is required for adipogenic signaling and adipocyte differentiation. J Biol Chem. 2004;279:29761‐29766.
Hotta K, Funahashi T, Matsukawa Y, et al. Galectin‐12, an adipose‐expressed galectin‐like molecule possessing apoptosis‐inducing activity. J Biol Chem. 2001;276:34089‐34097.
Yang RY, Hsu DK, Yu L, Ni J, Liu FT. Cell cycle regulation by galectin‐12, a new member of the galectin superfamily. J Biol Chem. 2001;276:20252‐20260.
Fasshauer M, Klein J, Lossner U, Paschke R. Negative regulation of adipose‐expressed galectin‐12 by isoproterenol, tumor necrosis factor alpha, insulin and dexamethasone. Eur J Endocrinol. 2002;147:553‐559.
Yang R‐Y, Yu L, Graham JL, et al. Ablation of a galectin preferentially expressed in adipocytes increases lipolysis, reduces adiposity, and improves insulin sensitivity in mice. Proc Natl Acad Sci USA. 2011;108:18696‐18701.
Wan L, Lin H‐J, Huang C‐C, et al. Galectin‐12 enhances inflammation by promoting M1 polarization of macrophages and reduces insulin sensitivity in adipocytes. Glycobiology. 2016;26:732‐744.
Eswar N, Webb B, Marti‐Renom MA, et al. Comparative protein structure modeling using modeller. Curr Protoc Bioinforma. 2006;15(1):5‐6.
Marti‐Renom MA, Stuart AC, Fiser A, Sanchez R, Melo F, Sali A. Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct. 2000;29:291‐325.
Fiser A, Do RK, Sali A. Modeling of loops in protein structures. Protein Sci. 2000;9:1753‐1773.
Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graph. 1996;14(27‐28):33‐38.
Case DA, Babin V, Berryman JT, et al. AMBER14. San Francisco: University of California; 2014.
Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Haak JR. Molecular‐dynamics with coupling to an external bath. J Chem Phys. 1984;81:3684‐3690.
van Gunsteren WF, Berendsen HJC. Computer simulation of molecular dynamics: methodology, applications, and perspectives in chemistry. Angew Chemie Int Ed English. 1990;29:992‐1023.
Hornak V, Abel R, Okur A, Strockbine B, Roitberg A, Simmerling C. Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins. 2006;65:712‐725.
Hanwell MD, Curtis DE, Lonie DC, Vandermeersch T, Zurek E, Hutchison GR. Avogadro: an advanced semantic chemical editor, visualization, and analysis platform. J Cheminform. 2012;4:17.
Trott O, Olson AJ. AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem. 2010;31:455‐461.
Seeliger D, de Groot BL. Ligand docking and binding site analysis with PyMOL and Autodock/Vina. J Comput Aided Mol Des. 2010;24:417‐422.
Rabinovich G, Castagna L, Landa C, Riera CM, Sotomayor C. Regulated expression of a 16‐kd galectin‐like protein in activated rat macrophages. J Leukoc Biol. 1996;59:363‐370.
Rapoport EM, Pochechueva TV, Kurmyshkina OV, et al. Solid‐phase assays for study of carbohydrate specificity of galectins. Biochem (Mosc). 2010;75:310‐319.
Rubin CS, Hirsch A, Fung C, Rosen OM. Development of hormone receptors and hormonal responsiveness in vitro. Insulin receptors and insulin sensitivity in the preadipocyte and adipocyte forms of 3T3‐L1 cells. J Biol Chem. 1978;253:7570‐7578.
Croci DO, Salatino M, Rubinstein N, et al. Disrupting galectin‐1 interactions with N‐glycans suppresses hypoxia‐driven angiogenesis and tumorigenesis in Kaposi's sarcoma. J Exp Med. 2012;209:1985‐2000.
Schindelin J, Arganda‐Carreras I, Frise E, et al. Fiji: an open‐source platform for biological‐image analysis. Nat Methods. 2012;9:676‐682.
Meynier C, Guerlesquin F, Roche P. Computational studies of human galectin‐1: role of conserved tryptophan residue in stacking interaction with carbohydrate ligands. J Biomol Struct Dyn. 2009;27:49‐58.
Ahmad N, Gabius H‐J, Sabesan S, Oscarson S, Brewer CF. Thermodynamic binding studies of bivalent oligosaccharides to galectin‐1, galectin‐3, and the carbohydrate recognition domain of galectin‐3. Glycobiology. 2004;14:817‐825.
Carlsson S, Oberg CT, Carlsson MC, et al. Affinity of galectin‐8 and its carbohydrate recognition domains for ligands in solution and at the cell surface. Glycobiology. 2007;17:663‐676.
Hirabayashi J, Hashidate T, Arata Y, et al. Oligosaccharide specificity of galectins: a search by frontal affinity chromatography. Biochim Biophys Acta. 2002;1572:232‐254.
Bum‐Erdene K, Leffler H, Nilsson UJ, Blanchard H. Structural characterisation of human galectin‐4 N‐terminal carbohydrate recognition domain in complex with glycerol, lactose, 3′‐sulfo‐lactose, and 2′‐fucosyllactose. Sci Rep. 2016;6:20289.
Cao Y. Angiogenesis modulates adipogenesis and obesity. J Clin Invest. 2007;117:2362‐2368.
Christiaens V, Lijnen HR. Angiogenesis and development of adipose tissue. Mol Cell Endocrinol. 2010;318:2‐9.
Corvera S, Gealekman O. Adipose tissue angiogenesis: impact on obesity and type‐2 diabetes. Biochim Biophys Acta. 2014;1842:463‐472.
Lijnen HR. Angiogenesis and obesity. Cardiovasc. Res. 2008;78:286‐293.
Cao Y. Adipose tissue angiogenesis as a therapeutic target for obesity and metabolic diseases. Nat Rev Drug Discov. 2010;9:107‐115.
Hefti MH, Vugt‐Van V, der Toorn CJ, Dixon R, Vervoort J. A novel purification method for histidine‐tagged proteins containing a thrombin cleavage site. Anal Biochem. 2001;295:180‐185.
Rubio I, Combita AL, Ortiz‐Reyes B, Navas M‐C. Hepatitis C virus core protein production and purification in a baculovirus expression system for biological assays. Biomedica. 2005;25:34‐45.
Garcia‐Vallejo JJ, van Kooyk Y. DC‐SIGN: the strange case of Dr. Jekyll and Mr. Hyde. Immunity. 2015;42(6):983‐985.
Noll AJ, Gourdine J‐P, Yu Y, Lasanajak Y, Smith DF, Cummings RD. Galectins are human milk glycan receptors. Glycobiology. 2016;26:655‐669.
Katiyar A, Lenka SK, Lakshmi K, Chinnusamy V, Bansal KC. In silico characterization and homology modeling of thylakoid bound ascorbate peroxidase from a drought tolerant wheat cultivar. Genomics, Proteomics & Bioinformatics. 2009;7(4):185‐193.
Guardia CMA, Gauto DF, Di Lella S, Rabinovich GA, Marti MA, Estrin DA. An integrated computational analysis of the structure, dynamics, and ligand binding interactions of the human galectin network. J Chem Inf Model. 2011;51:1918‐1930.
Bianchet MA, Odom EW, Vasta GR, Amzel LM. A novel fucose recognition fold involved in innate immunity. Nat Struct Biol. 2002;9:628‐634.
Ideo H, Seko A, Ishizuka I, Yamashita K. The N‐terminal carbohydrate recognition domain of galectin‐8 recognizes specific glycosphingolipids with high affinity. Glycobiology. 2003;13:713‐723.
Danielsen EM, Hansen GH. Lipid rafts in epithelial brush borders: atypical membrane microdomains with specialized functions. Biochim Biophys Acta. 2003;1617:1‐9.
Delacour D, Gouyer V, Zanetta J‐P, et al. Galectin‐4 and sulfatides in apical membrane trafficking in enterocyte‐like cells. J Cell Biol. 2005;169:491‐501.
Yang R‐Y, Xue H, Yu L, Velayos‐Baeza A, Monaco AP, Liu F‐T. Identification of VPS13C as a galectin‐12‐binding protein that regulates galectin‐12 protein stability and adipogenesis. PLoS One. 2016;11:e0153534.
Kumar J, Kline NL, Masison DC. Human DnaJB6 antiamyloid chaperone protects yeast from polyglutamine toxicity separately from spatial segregation of aggregates. Mol Cell Biol. 2018;38(23):e00437‐18.
Rodrigues T, Matafome P, Seica R. A vascular piece in the puzzle of adipose tissue dysfunction: mechanisms and consequences. Arch Physiol Biochem. 2014;120:1‐11.
Thijssen VL, Barkan B, Shoji H, et al. Tumor cells secrete galectin‐1 to enhance endothelial cell activity. Cancer Res. 2010;70:6216‐6224.
Croci DO, Cerliani JP, Dalotto‐Moreno T, et al. Glycosylation‐dependent lectin‐receptor interactions preserve angiogenesis in anti‐VEGF refractory tumors. Cell. 2014;156:744‐758.
Markowska AI, Liu F‐T, Panjwani N. Galectin‐3 is an important mediator of VEGF‐ and bFGF‐mediated angiogenic response. J Exp Med. 2010;207:1981‐1993.
Markowska AI, Jefferies KC, Panjwani N. Galectin‐3 protein modulates cell surface expression and activation of vascular endothelial growth factor receptor 2 in human endothelial cells. J Biol Chem. 2011;286:29913‐29921.
Delgado VMC, Nugnes LG, Colombo LL, et al. Modulation of endothelial cell migration and angiogenesis: a novel function for the “tandem‐repeat” lectin galectin‐8. FASEB J. 2011;25:242‐254.
Aanhane E, Schulkens IA, Heusschen R, et al. Different angioregulatory activity of monovalent galectin‐9 isoforms. Angiogenesis. 2018;21:545‐555.
Lijnen HR, Christiaens V, Scroyen I, et al. Impaired adipose tissue development in mice with inactivation of placental growth factor function. Diabetes. 2006;55:2698‐2704.
Nugroho DB, Ikeda K, Barinda AJ, et al. Neuregulin‐4 is an angiogenic factor that is critically involved in the maintenance of adipose tissue vasculature. Biochem Biophys Res Commun. 2018;503:378‐384.
Galic S, Oakhill JS, Steinberg GR. Adipose tissue as an endocrine organ. Mol Cell Endocrinol. 2010;316:129‐139.
Guilherme A, Virbasius JV, Puri V, Czech MP. Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol. 2008;9:367‐377.
Rutkowski JM, Davis KE, Scherer PE. Mechanisms of obesity and related pathologies: the macro‐ and microcirculation of adipose tissue. FEBS J. 2009;276:5738‐5746.
Tilg H, Moschen AR. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol. 2006;6:772‐783.
Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ. Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics. 2009;25:1189‐1191.

Auteurs

Sebastián M Maller (SM)

Laboratorio de Glicómica Funcional y Molecular, Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Técnicas (IBYME-CONICET), Buenos Aires, Argentina.
Laboratorio de Inmunopatología, Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Técnicas (IBYME-CONICET), Buenos Aires, Argentina.

Alejandro J Cagnoni (AJ)

Laboratorio de Glicómica Funcional y Molecular, Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Técnicas (IBYME-CONICET), Buenos Aires, Argentina.

Nadia Bannoud (N)

Laboratorio de Inmunopatología, Facultad de Ciencias Médicas, Instituto de Histología y Embriología de Mendoza (IHEM), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Universidad Nacional de Cuyo, Mendoza, Argentina.

Lorena Sigaut (L)

Departamento de Física, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires and Instituto de Física de Buenos Aires (IFIBA-CONICET), Buenos Aires, Argentina.

Juan M Pérez Sáez (JM)

Laboratorio de Inmunopatología, Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Técnicas (IBYME-CONICET), Buenos Aires, Argentina.

Lía I Pietrasanta (LI)

Departamento de Física, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires and Instituto de Física de Buenos Aires (IFIBA-CONICET), Buenos Aires, Argentina.
Centro de Microscopías Avanzadas (CMA), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina.

Ri-Yao Yang (RY)

Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas.

Fu-Tong Liu (FT)

Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan.

Diego O Croci (DO)

Laboratorio de Inmunopatología, Facultad de Ciencias Médicas, Instituto de Histología y Embriología de Mendoza (IHEM), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Universidad Nacional de Cuyo, Mendoza, Argentina.
Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Cuyo, Mendoza, Argentina.

Santiago Di Lella (S)

Instituto de Química Biológica, Ciencias Exactas y Naturales (IQUIBICEN-CONICET), Buenos Aires, Argentina.
Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina.

Victoria Sundblad (V)

Laboratorio de Inmunopatología, Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Técnicas (IBYME-CONICET), Buenos Aires, Argentina.

Gabriel A Rabinovich (GA)

Laboratorio de Inmunopatología, Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Técnicas (IBYME-CONICET), Buenos Aires, Argentina.
Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina.

Karina V Mariño (KV)

Laboratorio de Glicómica Funcional y Molecular, Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Técnicas (IBYME-CONICET), Buenos Aires, Argentina.

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