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When Galectins Recognize Glycans: From Biochemistry to Physiology and Back Again
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In the past decade, increasing efforts have been devoted to the study of galectins, a family of evolutionarily conserved glycan-binding proteins with multifunctional properties. Galectins function, either intracellularly or extracellularly, as key biological mediators capable of monitoring changes occurring on the cell surface during fundamental biological processes such as cellular communication, inflammation, development, and differentiation. Their highly conserved structures, exquisite carbohydrate specificity, and ability to modulate a broad spectrum of biological processes have captivated a wide range of scientists from a wide spectrum of disciplines, including biochemistry, biophysics, cell biology, and physiology. However, in spite of enormous efforts to dissect the functions and properties of these glycan-binding proteins, limited information about how structural and biochemical aspects of these proteins can influence biological functions is available. In this review, we aim to integrate structural, biochemical, and functional aspects of this bewildering and ancient family of glycan-binding proteins and discuss their implications in physiologic and pathologic settings.
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Asakura, H., Kashio, Y., Nakamura, K., Seki, M., Dai, S., Shirato, Y., Abedin, M. J., Yoshida, N., Nishi, N., Imaizumi, T., et al. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.169.10.5912 · Cited by 140
Correa, S. G. (2002) · Glycobiology · doi:10.1093/glycob/cwg010 · Cited by 139
Regulated expression of galectin-1 during B-cell activation and implications for T-cell apoptosis
Zúñiga, E. I., Rabinovich, G. A., Iglesias, M. M., & Gruppi, A. (2001) · Journal of Leukocyte Biology · doi:10.1189/jlb.70.1.73 · Cited by 138
Self-citationBernardes, E. S., Silva, N. M., Ruas, L. P., Mineo, J. R., Loyola, A. M., Hsu, D. K., Liu, F., Chammas, R. J., & Roque‐Barreira, M. C. (2006) · American Journal Of Pathology · doi:10.2353/ajpath.2006.050636 · Cited by 137
Hahn, H. P., Pang, M., He, J., Hernandez, J. D., Yang, R.-Y., Li, L. Y., Wang, X., Liu, F., & Baum, L. G. (2004) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401485 · Cited by 137
Galectin-1 Binds Different CD43 Glycoforms to Cluster CD43 and Regulate T Cell Death
Hernandez, J. D., Nguyen, J. T., He, J., Wang, W., Ardman, B. M., Green, J. M., Fukuda, M., & Baum, L. G. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.8.5328 · Cited by 133
Galectin-3 interacts with naïve and primed neutrophils, inducing innate immune responses
Nieminen, J., St-Pierre, C., & Sato, S. (2005) · Journal of Leukocyte Biology · doi:10.1189/jlb.1204702 · Cited by 131
Expression and function of galectin-3, a β-galactoside-binding protein in activated T lymphocytes
Joo, H., Goedegebuure, P. S., Sadanaga, N., Nagoshi, M., von Bernstorff, W., & Eberlein, T. J. (2001) · Journal of Leukocyte Biology · doi:10.1189/jlb.69.4.555 · Cited by 130
Ahmad, N. (2004) · Glycobiology · doi:10.1093/glycob/cwh095 · Cited by 128
Paclik, D., Danese, S., Berndt, U., Wiedenmann, B., Dignass, A. U., & Sturm, A. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002629 · Cited by 125
Galectin-7 in the Control of Epidermal Homeostasis after Injury
Gendronneau, G., Sidhu, S., Delacour, D., Dang, T., Calonne, C., Houzelstein, D., Magnaldo, T., & Poirier, F. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-02-0166 · Cited by 123
Expression and Function ofXmsx-2Bin Dorso-Ventral Axis Formation in Gastrula Embryos
Onitsuka, I., Takeda, M., & Maéno, M. (2000) · ZOOLOGICAL SCIENCE · doi:10.2108/zsj.17.1107 · Cited by 122
Fulcher, J. A., Hashimi, S. T., Levroney, E. L., Pang, M., Gurney, K. B., Baum, L. G., & Lee, B. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.1.216 · Cited by 119
Dam, T. K., Gerken, T. A., & Brewer, C. F. (2009) · Biochemistry · doi:10.1021/bi9002919 · Cited by 119
Rabinovich, G. A., Ramhorst, R., Rubinstein, N., Corigliano, A., Daroqui, M. C., Joffé, E. B. D. K., & Fainboim, L. (2002) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401009 · Cited by 118
Self-citationAhmad, N., Gabius, H., Kaltner, H., André, S., Kuwabara, I., Liu, F.-T., Oscarson, S., Norberg, T., & Brewer, C. F. (2002) · Canadian Journal of Chemistry · doi:10.1139/v02-162 · Cited by 116
Galectin-12, an Adipose-expressed Galectin-like Molecule Possessing Apoptosis-inducing Activity
Hotta, K., Funahashi, T., Matsukawa, Y., Takahashi, M., Nishizawa, H., Kishida, K., Matsuda, M., Kuriyama, H., Kihara, S., Nakamura, T., et al. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m105097200 · Cited by 115
Inagaki, Y., Sohma, Y., Horie, H., Nozawa, R., & Kadoya, T. (2000) · European Journal of Biochemistry · doi:10.1046/j.1432-1033.2000.01311.x · Cited by 114
Novel insights into the inhibitory effects of Galectin-1 on neutrophil recruitment under flow
Cooper, D., Norling, L. V., & Perretti, M. (2008) · Journal of Leukocyte Biology · doi:10.1189/jlb.1207831 · Cited by 114
Galectin multimerization and lattice formation are regulated by linker region structure
Earl, L. A., Bi, S., & Baum, L. G. (2010) · Glycobiology · doi:10.1093/glycob/cwq144 · Cited by 114
Strongly enhanced IL-10 production using stable galectin-1 homodimers
van der Leij, J., van den Berg, A., Harms, G., Eschbach, H., Vos, H. J., Zwiers, P. J., van Weeghel, R., Groen, H., Poppema, S., & Visser, L. (2006) · Molecular Immunology · doi:10.1016/j.molimm.2006.02.011 · Cited by 111
Sequence and Mapping of Galectin-5, a β-Galactoside-binding Lectin, Found in Rat Erythrocytes
Gitt, M. A., Wiser, M. F., Leffler, H., Herrmann, J., Xia, Y.-R., Massa, S. M., Cooper, D. N. W., Lusis, A. J., & Barondes, S. H. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.10.5032 · Cited by 111
Motrán, C. C., Molinder, K. M., Liu, S. D., Poirier, F., & Miceli, M. C. (2008) · European Journal of Immunology · doi:10.1002/eji.200838295 · Cited by 110
Cerliani, J. P., Stowell, S. R., Mascanfroni, I. D., Arthur, C. M., Cummings, R. D., & Rabinovich, G. A. (2010) · Journal of Clinical Immunology · doi:10.1007/s10875-010-9494-2 · Cited by 110
Self-citationInhibitory control of endothelial galectin‐1 on in vitro and in vivo lymphocyte trafficking
Norling, L. V., Sampaio, A. L. F., Cooper, D., & Perretti, M. (2007) · The FASEB Journal · doi:10.1096/fj.07-9268com · Cited by 110
Breuilh, L., Vanhoutte, F., Fontaine, J., van Stijn, C. M. W., Tillie‐Leblond, I., Capron, M., Faveeuw, C., Jouault, T., van Die, I., Gosset, P., et al. (2007) · Infection and Immunity · doi:10.1128/iai.02006-06 · Cited by 109
Nesmelova, I. V., Ermakova, E. A., Daragan, V. A., Pang, M., Menéndez, M., Lagartera, L., Solı́s, D., Baum, L. G., & Mayo, K. H. (2010) · Journal of Molecular Biology · doi:10.1016/j.jmb.2010.02.033 · Cited by 108
Ligand Reduces Galectin-1 Sensitivity to Oxidative Inactivation by Enhancing Dimer Formation
Stowell, S. R., Cho, M., Feasley, C. L., Arthur, C. M., Song, X., Colucci, J. K., Karmakar, S., Mehta, P., Dias‐Baruffi, M., McEver, R. P., et al. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m808925200 · Cited by 106
Fernández, G. C., Ilarregui, J. M., Rubel, C. J., Toscano, M. A., Gomez, S. A., Bompadre, M. B., Isturiz, M. A., Rabinovich, G. A., & Palermo, M. S. (2004) · Glycobiology · doi:10.1093/glycob/cwi026 · Cited by 105
Self-citationChen, H., Sharma, B. B., Yu, L., Zuberi, R. I., Weng, I., Kawakami, Y., Kawakami, T., Hsu, D. K., & Liu, F. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.8.4991 · Cited by 104
Galectin-1 Induces Reversible Phosphatidylserine Exposure at the Plasma Membrane
Stowell, S. R., Karmakar, S., Arthur, C. M., Ju, T., Rodrigues, L. C., Riul, T. B., Dias‐Baruffi, M., Miner, J. J., McEver, R. P., & Cummings, R. D. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-07-0786 · Cited by 103
Paclik, D., Berndt, U., Guzy, C., Dankof, A., Danese, S., Holzloehner, P., Rosewicz, S., Wiedenmann, B., Wittig, B. M., Dignass, A. U., et al. (2007) · Journal of Molecular Medicine · doi:10.1007/s00109-007-0290-2 · Cited by 102
Sato, M., Nishi, N., Shoji, H., Seki, M., Hashidate, T., Hirabayashi, J., KASAI, K., Hata, Y., Suzuki, S., Hirashima, M., et al. (2002) · Glycobiology · doi:10.1093/glycob/12.3.191 · Cited by 101
Hsu, D. K., Yang, R., & Liu, F. (2006) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(06)17018-4 · Cited by 99
Espéli, M., Mancini, S. J. C., Breton, C. S., Poirier, F., & Schiff, C. (2009) · Blood · doi:10.1182/blood-2009-01-198465 · Cited by 99
Involvement of CD2 and CD3 in galectin-1 induced signaling in human Jurkat T-cells
Walzel, H. (2000) · Glycobiology · doi:10.1093/glycob/10.2.131 · Cited by 99
Almkvist, J., Fäldt, J., Dahlgren, C., Leffler, H., & Karlsson, A. (2001) · Infection and Immunity · doi:10.1128/iai.69.2.832-837.2001 · Cited by 96
Activation of Tim-3–Galectin-9 pathway improves survival of fully allogeneic skin grafts
Wang, F. Y., He, W., Jin, Y., Wu, K., Zhou, H., Zhang, W., & Chen, Z. K. (2008) · Transplant Immunology · doi:10.1016/j.trim.2008.01.008 · Cited by 93
Rabinovich, G. A., & Ilarregui, J. M. (2009) · Immunological Reviews · doi:10.1111/j.1600-065x.2009.00787.x · Cited by 92
Self-citationFulcher, J. A., Chang, M. H., Wang, S., Almazan, T., Hashimi, S. T., Eriksson, A., Wen, X., Pang, M., Baum, L., Singh, R., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.037507 · Cited by 88
Rossi, B., Espéli, M., Schiff, C., & Gauthier, L. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.2.796 · Cited by 87
Galectin-8 Induces Apoptosis in the CD4highCD8high Thymocyte Subpopulation
Tribulatti, M. V., Mucci, J., Cattaneo, V., Agüero, F., Gilmartin, T., Head, S. R., & Campetella, O. (2007) · Glycobiology · doi:10.1093/glycob/cwm104 · Cited by 87
Galectin-12 Is Required for Adipogenic Signaling and Adipocyte Differentiation
Yang, R., Hsu, D. K., Yu, L., Chen, H., & Liu, F. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m401303200 · Cited by 86
Characterization of Galectin-9-Induced Death of Jurkat T Cells
Lü, L., Nakagawa, R., Kashio, Y., Ito, A., Shoji, H., Nishi, N., Hirashima, M., Yamauchi, A., & Nakamura, T. (2006) · The Journal of Biochemistry · doi:10.1093/jb/mvm019 · Cited by 85
Norambuena, A., Metz, C., Vicuña, L., Silva, A., Pardo, E., Oyanadel, C., Massardo, L., González, A., & Soza, A. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m808949200 · Cited by 84
Than, N. G., Romero, R. J., Erez, O., Weckle, A. L., Tarca, A. L., Hotra, J. W., Abbas, A., Han, Y. M., Kim, S.-S., Kusanovic, J. P., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807606105 · Cited by 80
Garner, O. B., Aguilar, H. C., Fulcher, J. A., Levroney, E. L., Harrison, R., Wright, L., Robinson, L. R., Aspericueta, V., Panico, M., Haslam, S. M., et al. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000993 · Cited by 77
Dendritic Cells Expressing Transgenic Galectin-1 Delay Onset of Autoimmune Diabetes in Mice
Perone, M. J., Bertera, S., Tawadrous, Z. S., Shufesky, W. J., Piganelli, J. D., Baum, L. G., Trucco, M., & Morelli, A. E. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.8.5278 · Cited by 76
Coupling pathogen recognition to innate immunity through glycan-dependent mechanisms
Davicino, R. C., Eliçabe, R. J., Genaro, M. S. D., & Rabinovich, G. A. (2011) · International Immunopharmacology · doi:10.1016/j.intimp.2011.05.002 · Cited by 76
Self-citationIntracellular galectin‐9 activates inflammatory cytokines in monocytes
Matsuura, A., Tsukada, J., Mizobe, T., Higashi, T., Mouri, F., Tanikawa, R., Yamauchi, A., Hirashima, M., & Tanaka, Y. (2009) · Genes to Cells · doi:10.1111/j.1365-2443.2009.01287.x · Cited by 72
Nagae, M., Nishi, N., Murata, T., Usui, T., Nakamura, T., Wakatsuki, S., & Kato, R. (2008) · Glycobiology · doi:10.1093/glycob/cwn121 · Cited by 72
Nishi, N., Abe, A., Iwaki, J., Yoshida, H., Itoh, A., Shoji, H., Kamitori, S., Hirabayashi, J., & Nakamura, T. (2008) · Glycobiology · doi:10.1093/glycob/cwn089 · Cited by 71
Suzuki, Y., Inoué, T., Yoshimaru, T., & Ra, C. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2008.01.025 · Cited by 69
Galectin-3 modulates T cell activity and is reduced in the inflamed intestinal epithelium in IBD
Müller, S., Schaffer, T., Flogerzi, B., Fleetwood, A. J., Weimann, R., Schoepfer, A. M., & Seibold, F. (2006) · Inflammatory Bowel Diseases · doi:10.1097/01.mib.0000225341.37226.7c · Cited by 67
Galectin-1 induced activation of the apoptotic death-receptor pathway in human Jurkat T lymphocytes
Brandt, B., Büchse, T., Abou-eladab, E., Tiedge, M., Krause, E., Jeschke, U., & Walzel, H. (2008) · Histochemistry and Cell Biology · doi:10.1007/s00418-008-0395-x · Cited by 65
Miller, M. C., Nesmelova, I. V., Platt, D., Klyosov, A. A., & Mayo, K. H. (2009) · Biochemical Journal · doi:10.1042/bj20090265 · Cited by 64
Silva, E., Lorenzato, L. R., Nihei, O. K., Junqueira, M. D. S., Rabinovich, G. A., Hsu, D. K., Liu, F., Savino, W., Chammas, R. J., & Villa‐Verde, D. M. S. (2007) · American Journal Of Pathology · doi:10.2353/ajpath.2007.060389 · Cited by 63
Self-citationAssociation of Galectin-9 with Eosinophil Apoptosis
Saita, N., Goto, E., Yamamoto, T., et al. (2002) · International Archives of Allergy and Immunology · doi:10.1159/000058002 · Cited by 62
Iurisci, I., Cumashi, A., Sherman, A. A., Tsvetkov, Y. E., Tinari, N., Piccolo, E., DʼEgidio, M., Adamo, V., Natoli, C., Rabinovich, G. A., et al. (2009) · PubMed · Cited by 61
Self-citationGalectin-1 Promotes Immunoglobulin Production during Plasma Cell Differentiation
Tsai, C., Chiu, Y.-K., Hsu, T.-L., Lin, I., Hsieh, S.-L., & Lin, K. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.7.4570 · Cited by 60
Dam, T. K., & Brewer, F. (2010) · Glycobiology · doi:10.1093/glycob/cwq084 · Cited by 58
Potential roles of galectins in myeloid differentiation into three different lineages
Abedin, M. J., Kashio, Y., Seki, M., Nakamura, K., & Hirashima, M. (2003) · Journal of Leukocyte Biology · doi:10.1189/jlb.0402163 · Cited by 56
Endogenous galectin-1 enforces class I–restricted TCR functional fate decisions in thymocytes
Liu, S. D., Whiting, C. C., Tomassian, T., Pang, M., Bissel, S. J., Baum, L. G., Mossine, V. V., Poirier, F., Huflejt, M. E., & Miceli, M. C. (2008) · Blood · doi:10.1182/blood-2007-09-114181 · Cited by 54
Ford, M. G., Weimar, T., Köhli, T., & Woods, R. J. (2003) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.10428 · Cited by 51
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Induction of Cell Adhesion by Galectin-8 and its Target Molecules in Jurkat T-Cells
Yamamoto, H., Nishi, N., Shoji, H., Itoh, A., Lü, L., Hirashima, M., & Nakamura, T. (2007) · The Journal of Biochemistry · doi:10.1093/jb/mvm223 · Cited by 50
Laderach, D. J., Compagno, D., Toscano, M. A., Croci, D. O., Dergan‐Dylon, S., Salatino, M., & Rabinovich, G. A. (2009) · IUBMB Life · doi:10.1002/iub.281 · Cited by 50
Self-citationEnhanced apoptotic activity of a structurally optimized form of galectin-1
Bättig, P. (2004) · Molecular Immunology · doi:10.1016/j.molimm.2004.02.004 · Cited by 45
Role of p56lck and ZAP70-mediated tyrosine phosphorylation in galectin-1-induced cell death
Ion, G., Fajka‐Boja, R., Tóth, G. K., et al. (2005) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401628 · Cited by 45
Is human galectin-1 activity modulated by monomer/dimer equilibrium?
Giudicelli, V., Lutomski, D., Lévi‐Strauss, M., Bladier, D., Joubert‐Caron, R., & Caron, M. (1997) · Glycobiology · doi:10.1093/glycob/7.3.323-a · Cited by 42
Galectin-1 signaling in leukocytes requires expression of complex-type N-glycans
Karmakar, S., Stowell, S. R., Cummings, R. D., & McEver, R. P. (2008) · Glycobiology · doi:10.1093/glycob/cwn066 · Cited by 39
Characterization of galectin-9-induced death of Jurkat T-cells
陸, 亮. (2007) · Medical Entomology and Zoology · Cited by 36
Ilarregui, J. M., & Rabinovich, G. A. (2010) · NeuroImmunoModulation · doi:10.1159/000258712 · Cited by 32
Self-citationGuardia, C. M. A., Gauto, D. F., Lella, S. D., Rabinovich, G. A., Marti, M. A., & Estrin, D. A. (2011) · Journal of Chemical Information and Modeling · doi:10.1021/ci200180h · Cited by 31
Self-citationA role for galectin-3 in CD13-mediated homotypic aggregation of monocytes
Mina‐Osorio, P., Soto‐Cruz, I., & Ortega, E. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.12.081 · Cited by 29
Critical Role of the Solvent Environment in Galectin-1 Binding to the Disaccharide Lactose
Lella, S. D., Ma, L., Ricci, J. C. D., Rabinovich, G. A., Asher, S. A., & Álvarez, R. M. S. (2009) · Biochemistry · doi:10.1021/bi801855g · Cited by 25
Self-citationZhou, D., Ge, H., Sun, J., Gao, Y., Teng, M., & Niu, L. (2008) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.22003 · Cited by 24
Unusual structural stability and ligand induced alterations in oligomerization of a galectin
Surolia, A., Swaminathan, C. P., Ramkumar, R., & Podder, S. K. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)00432-8 · Cited by 20
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Self-citationDisaccharide Binding to Galectin-1: Free Energy Calculations and Molecular Recognition Mechanism
Echeverria, I., & Amzel, L. M. (2011) · Biophysical Journal · doi:10.1016/j.bpj.2011.03.032 · Cited by 18
Iglesias, M. M., Elola, M. T., Martínez, V. G., Fink, N. E., & Wolfenstein‐Todel, C. (2003) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/s1570-9639(03)00119-5 · Cited by 16
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Metadata
- Authors
- Di Lella, S., Sundblad, V., Cerliani, J. P., Guardia, C. M., Estrin, D. A., Vasta, G. R., & Rabinovich, G. A.
- Venue
- Biochemistry
- Publisher
- American Chemical Society (ACS)
- Published
- 2011-08-26
- Volume
- 50
- Issue
- 37
- Pages
- 7842-7857
- ISSN
- 0006-2960 (ISSN-L)
- 1520-4995
- OpenAlex
- W1967989660
- Cited by
- 282
- References
- 179
- FWCI
- 7.00
- Type
- journal article
- Language
- en
- Open access
- green
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