Galectins as self/non-self recognition receptors in innate and adaptive immunity: An unresolved paradox

Frontiers in Immunology

Volumn 3, Issue JUL, 2012, Pages

  Vasta, Gerardo R ^a   Ahmed, Hafiz ^a   Nita Lazar, Mihai ^a   Banerjee, Aditi ^a   Pasek, Marta ^a   Shridhar, Surekha ^a,b   Guha, Prasun ^a   Fernández Robledo, José A ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b Essex Campus   (United States)

Author keywords

C type lectin; Galectin; Glycan ligands; Microbial recognition

Indexed keywords

EID: 84874201705     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00199     Document Type: Review

References (142)

1. Kaltner, H., Sabesan, S., Roy, R., Liu, B., Macaluso, F., and Brewer, C. F. (2004). Galectin-3 precipitates as a pentamer with synthetic multivalent carbohydrates and forms heteroge- neouscross-linkedcomplexes. J.Biol. Chem. 279,10841-10847.
2. Ahmed, H., Bianchet, M. A., Amzel, L. M., Hirabayashi, J., Kasai, K., Giga- Hama, Y., Tohda, H., and Vasta, G. R. (2002). Novel carbohydrate speci- ficity of the 16-kDa galectin from Caenorhabditis elegans: binding to blood group precursor oligosaccha- rides (type 1, type 2, Talpha, and Tbeta)andgangliosides.Glycobiology 12,451-461.
3. Ahmed, H., Du, S. J., O'Leary, N., and Vasta, G. R. (2004). Biochem- ical and molecular characterization of galectins from zebrafish (Danio rerio): notochord-specific expres- sion of a prototype galectin during earlyembryogenesis.Glycobiology 14, 219-232.
4. Ahmed, H., Pohl, J., Fink, N. E., Strobel, F., and Vasta, G. R. (1996). The primary structure and carbohydrate specificity of a beta-galactosyl-binding lectin from toad (Bufo arenarum Hensel) ovary reveal closer similarities to the mam- maliangalectin-1thantothe galectin from the clawed frog Xenopus lae- vis. J. Biol. Chem. 271, 33083- 33094.
5. Ahmed, H., and Vasta, G. R. (1994). Galectins: conservation of function- ally and structurally relevant amino acid residues defines two types of carbohydrate recognition domains. Glycobiology 4, 545-548.
6. Ahmed, H., and Vasta, G. R. (2008). Unlike mammalian GRIFIN, the zebrafish homologue (DrGRIFIN) representsafunctionalcarbohydrate- binding galectin. Biochem. Biophys. Res. Commun. 371,350-355.
7. Akira, S., Takeda, K., and Kaisho, T. (2001). Toll-like receptors: crit- ical proteins linking innate and acquiredimmunity. Nat. Immunol. 2, 675-680.
8. Anderson, A. C., Anderson, D. E., Bre- goli, L., Hastings, W. D., Kassam, N., Lei, C., Chandwaskar, R., Kar- man, J., Su, E. W., Hirashima, M., Bruce, J. N., Kane, L. P., Kuchroo, V. K., and Hafler, D. A. (2007). Pro- motionof tissueinflammationbythe immune receptor Tim-3 expressed on innate immune cells. Science 318, 1141-1143.
9. Bianchet, M. A., Ahmed, H., Vasta, G. R., and Amzel, L. M. (2000). Soluble beta-galactosyl-binding lectin (galectin) from toad ovary: crystallographic studies of two protein-sugarcomplexes. Proteins 40, 378-388.
10. Bianchet, M. A., Odom, E. W.,Vasta, G. R., and Amzel, L. M. (2002). A novel fucose recognition fold involved in innate immunity. Nat. Struct. Biol. 9, 628-634.
11. Bianchet, M. A., Odom, E. W., Vasta, G. R., and Amzel, L. M. (2010). Structure and specificity of a binary tandemdomainF-lectinfromstriped bass (Morone saxatilis). J. Mol. Biol. 401,239-252.
12. Bittel, P., and Robatzek, S. (2007). Microbe-associated molecular patterns (MAMPs) probe plant immunity. Curr. Opin. Plant Biol. 10, 335-341.
13. Brewer, C. F., Miceli, M. C., and Baum, L. G. (2002). Clusters, bundles, arraysandlattices:novelmechanisms for lectin-saccharide-mediated cellu- lar interactions. Curr. Opin. Struct. Biol. 12,616-623.
14. Carlsson, S., Oberg, C. T., Carlsson, M. C., Sundin, A., Nilsson, U. J., Smith, D., Cummings, R. D., Almkvist, J., Karlsson, A., and Leffler, H. (2007). Affinityof galectin-8anditscarbohy- draterecognitiondomainsforligands in solution and at the cell surface. Glycobiology 17,663-676.
15. Cartwright, J. R., Tharia, H. A., Burns, I., Shrive, A. K., Hoole, D., and Greenhough, T. J. (2004). Isolation and characterisation of pentraxin- like serum proteins from the common carp Cyprinus carpio. Dev. Comp. Immunol. 28,113-125.
16. Casadevall, A., and Pirofski, L. A. (2000). Host-pathogen interactions: basicconceptsof microbialcommensalism, colonization, infection, and disease. Infect. Immun. 68, 6511- 6518.
17. Cedeno-Laurent,F.,and Dimitroff,C. J. (2012). Galectin-1 research in T cell immunity: past, present and future. Clin. Immunol. 142,107-116.
18. Chen, H. Y., Fermin, A., Vardhana, S., Weng, I. C., Lo, K. F., Chang, E. Y., Maverakis, E., Yang, R. Y., Hsu, D. K., Dustin, M. L., and Liu, F. T. (2009). Galectin-3 negatively regulates TCR-mediated CD4+ T- cell activation at the immunological synapse. Proc. Natl. Acad. Sci. U.S.A. 106, 14496-14501.
19. Cho, M., and Cummings, R. D. (1995). Galectin-1, a beta-galactoside- binding lectin in Chinese hamster ovary cells. II. Localization and biosynthesis. J. Biol. Chem. 270, 5207-5212.
20. Cleves, A. E., Cooper, D. N., Barondes, S. H., and Kelly, R. B. (1996). A new pathwayforproteinexportinSaccha- romyces cerevisiae. J. Cell Biol. 133, 1017-1026.
21. Colnot, C., Ripoche, M. A., Scaerou, F., Foulis, D., and Poirier, F. (1996). Galectins in mouse embryogenesis. Biochem. Soc. Trans. 24, 141-146.
22. Colnot, C., Sidhu, S. S., Balmain, N., and Poirier, F. (2001). Uncoupling of chondrocytedeathandvascularinva- sion in mouse galectin 3 null mutant bones. Dev. Biol. 229,203-214.
23. Cook,M. T.,Hayball,P. J., Nowak, B. F., andHayball,J.D.(2005). Theopsonising activity of a pentraxin-like protein isolated from snapper (Pagrus auratus,Sparidae)serum.Dev.Comp. Immunol. 29,703-712.
24. Cooper, D. N. (2002). Galectinomics: finding themes in complexity. Biochim. Biophys. Acta 1572, 209-231.
25. Cummings, R. D., and Nyame, A. K. (1999). Schistosome glysoconju- gates. Biochim. Biophys. Acta 1455, 363-374.
26. Dam, T. K., and Brewer, C. F. (2008). Effects of clustered epitopes in multivalent ligand-receptor interactions. Biochemistry 47, 8470-8476.
27. Dam, T. K., and Brewer, C. F. (2010).Lectinsaspatternrecognition molecules: the effects of epitope density in innate immunity. Glycobiology 20,270-279.
28. Dam,T.K.,Gerken,T.A.,andBrewer,C. F. (2009). Thermodynamics of multivalent carbohydrate-lectin crosslinking interactions: importance of entropy in the bind and jump mechanism. Biochemistry 48,3822-3827.
29. Di Lella,S.,Marti,M.A.,Alvarez,R. M., Estrin, D. A., and Ricci, J. C. (2007). Characterization of the galectin-1 carbohydrate recognition domain in terms of solvent occupancy. J. Phys. Chem. B 111,7360-7366.
30. Di Lella, S., Sundblad, V., Cerliani, J. P., Guardia, C. M., Estrin, D. A., Vasta, G. R., and Rabinovich, G. A. (2011). When galectins recognize glycans: from biochemistry to physiology and back again. Biochemistry 50,7842-7857.
31. Dias-Baruffi, M., Zhu, H., Cho, M., Karmakar, S., Mcever, R. P., and Cummings, R. D. (2003). Dimeric galectin-1 induces surface exposure ofphosphatidylserineandphagocytic recognition of leukocytes without inducing apoptosis. J. Biol. Chem. 278, 41282-41293.
32. Echeverria, I., and Amzel, L. M. (2011). Disaccharide binding to galectin-1: free energy calculations and molecular recognition mechanism. Biophys. J. 100, 2283-2292.
33. Elola, M. T., Wolfenstein-Todel, C., Troncoso, M. F., Vasta, G. R., and Rabinovich, G. A. (2007). Galectins: matricellularglycan-bindingproteins linking cell adhesion, migration, and survival. Cell.Mol.LifeSci.64, 1679-1700.
34. Fang, R., Mantle, M., and Ceri, H. (1993). Characterization of quail intestinal mucin as a ligand for endogenous quail lectin. Biochem. J. 293 (Pt 3),867-872.
35. Feinberg, H., Park-Snyder, S., Kolatkar, A. R., Heise, C. T., Taylor, M. E., and Weis, W. I. (2000). Structure of a C-type carbohydrate recognition domain from the macrophage man- nose receptor. J. Biol. Chem. 275, 21539-21548.
36. Fogel, S., Guittaut, M., Legrand, A., Monsigny,M.,and Hebert,E. (1999). The tat protein of HIV-1 induces galectin-3 expression. Glycobiology 9, 383-387.
37. Fujita, T., Matsushita, M., and Endo, Y. (2004).Thelectin-complementpathway - its role in innate immunity and evolution. Immunol. Rev. 198, 185-202.
38. Fukumori, T., Kanayama, H. O., and Raz,A. (2007). The role of galectin-3 incancerdrugresistance.DrugResist. Update 10, 101-108.
39. Fukumori, T., Takenaka, Y., Yoshii, T., Kim, H. R., Hogan, V., Inohara, H., Kagawa,S.,and Raz,A. (2003). CD29 and CD7 mediate galectin-3-induced type II T-cell apoptosis. Cancer Res. 63,8302-8311.
40. Fuller, J. R., Pitzer, J. E., Godwin, U., Albertino, M., Machon, B. D., Kearse, K. P., and Mcconnell, T. J. (2004). Characterization of the molecular chaperone calnexin in the channel catfish, Ictalurus punctatus, and its association with MHC class II molecules. Dev. Comp. Immunol. 28, 603-617.
41. Garred, P., Larsen, F., Seyfarth, J., Fujita, R., and Madsen, H. O. (2006). Mannose-binding lectin and its genetic variants. Genes Immun. 7, 85-94.
42. Gerwick, L., Corley-Smith, G., and Bayne, C. J. (2007). Gene transcript changes in individual rainbow trout livers following an inflammatorystimulus. FishShellfishImmunol. 22, 157-171.
43. Gorski, J. P., Liu, F. T., Artigues, A., Castagna, L. F., and Osdoby, P. (2002). New alternatively spliced form of galectin-3, a member of the beta-galactoside-binding animal lectin family, contains a predicted transmembrane-spanning domain and a leucine zipper motif. J. Biol. Chem. 277,18840-18848.
44. Greenspan, N. S. (2001). Dimensions of antigen recognition and levels of immunological specificity. Adv. Cancer Res. 80, 147-187.
45. Guevremont, M., Martel-Pelletier, J., Boileau, C., Liu, F. T., Richard, M., Fernandes, J. C., Pelletier, J. P., and Reboul, P. (2004). Galectin-3 surface expression on human adult chondrocytes: a potential substrate for collagenase-3. Ann. Rheum. Dis. 63, 636-643.
46. He, J., and Baum, L. G. (2004). Presen- tation of galectin-1 by extracellular matrix triggers T cell death. J. Biol. Chem. 279,4705-4712.
47. la, C., Jeffs, S., Longstaff, C., Stieh, D., Hag-garty, B., Vanham, G., Schols, D., Balzarini, J., Jones, I. M., Hoxie, J., Shattock, R., and Kelly, C. G. (2011). DC-SIGN increases the affinity of HIV-1envelopeglycoproteininteraction with CD4. PLoS ONE 6, e28307. doi: 10.1371/journal.pone.0028307
48. Hirabayashi, J., and Kasai, K. (1993). The family of metazoan metal-in- dependent beta-galactoside-binding lectins: structure, function and molecular evolution. Glycobiology 3, 297-304.
49. Houzelstein, D., Goncalves, I. R., Fadden, A. J., Sidhu, S. S., Cooper, D. N., Drickamer,K.,Leffler,H.,andPoirier, F.(2004).Phylogeneticanalysisof the vertebrate galectin family. Mol. Biol. Evol. 21,1177-1187.
50. Hsu,D.K.,Hammes,S.R.,Kuwabara,I., Greene, W. C., and Liu, F. T. (1996). Human T lymphotropic virus-I infection of human T lymphocytes induces expression of the betagalactoside-binding lectin, galectin-3. Am. J. Pathol. 148,1661-1670.
51. Hughes,D.T.,andSperandio,V.(2008). Inter-kingdom signalling: communication between bacteria and their hosts. Nat. Rev. Microbiol. 6, 111-120.
52. Ideo, H., Matsuzaka, T., Nonaka, T., Seko, A., and Yamashita, K. (2011). Galectin-8-N-domain recog- nition mechanism for sialylated and sulfated glycans. J. Biol. Chem. 286, 11346-11355.
53. Ilarregui, J. M., Croci, D. O., Bianco, G. A., Toscano, M. A., Salatino, M., Vermeulen, M. E., Geffner, J. R., and Rabinovich, G. A. (2009). Tolerogenic signals delivered by dendritic cells to T cells through a galectin-1-driven immunoregulatory circuit involving interleukin 27 and interleukin 10. Nat. Immunol. 10, 981-991.
54. Iliev, D. B., Roach, J. C., Mackenzie, S., Planas, J. V., and Goetz, F. W. (2005). Endotoxin recognition: in fish or not in fish? FEBS Lett. 579,6519-6528.
55. Ip, W. K., Takahashi, K., Ezekowitz, R. A., and Stuart, L. M. (2009). Mannose-binding lectin and innate immunity. Immunol. Rev. 230,9-21.
56. Khalturin, K., Panzer, Z., Cooper, M. D.,and Bosch,T. C. (2004). Recogni- tion strategies in the innate immune system of ancestral chordates. Mol. Immunol. 41, 1077-1087.
57. Kingeter, L. M., and Lin, X. (2012). C-type lectin receptor-induced NF- kappaB activation in innate immune and inflammatory responses. Cell. Mol. Immunol. 9,105-112.
58. Kohatsu, L., Hsu, D. K., Jegalian, A. G., Liu, F.-T., and Baum, L. G. (2006). Galectin-3 induces death of Candida species expressing specific beta-1,2- linked mannans. J. Immunol. 177, 4718-4726.
59. Krejcirikova, V., Pachl, P., Fabry, M., Maly, P., Rezacova, P., and Brynda, J. (2011). Structure of the mouse galectin-4 N-terminal carbohydrate-recognition domain reveals the mechanismof oligosacchariderecognition. Acta Crystallogr. D Biol. Crystallogr. 67,204-211.
60. Li, Y., Feng, J., Geng, S., Wei, H., Chen, G., Li, X., Wang, L., Wang, R., Peng, H., Han, G., and Shen, B. (2011). The N- and C-terminal carbohydraterecognitiondomainsof galectin-9contributedifferentlytoits multiple functions in innate immu- nity and adaptive immunity. Mol. Immunol. 48,670-677.
61. Liao, D. I., Kapadia, G., Ahmed, H., Vasta, G. R., and Herzberg, O. (1994). Structure of S-lectin, a developmentally regulated vertebrate beta-galactoside-binding protein. Proc. Natl. Acad. Sci. U.S.A. 91, 1428-1432.
62. Lipkowitz, M. S., Leal-Pinto, E., Cohen, B. E., and Abramson, R. G. (2004). Galectin9isthesugar-regulatedurate transporter/channel UAT. Glycoconj. J. 19,491-498.
63. Liu, F. T., and Hsu, D. K. (2007). The roleof galectin-3inpromotionof the inflammatory response. Drug News Perspect. 20, 455-460.
64. Liu,F. T.,and Rabinovich,G. A. (2005). Galectins as modulators of tumour progression. Nat. Rev. Cancer 5, 29-41.
65. Liu, F. T., Yang, R. Y., and Hsu, D. K. (2012). Galectins in acute and chronic inflammation. Ann. N.Y. Acad. Sci. 1253,80-91.
66. Liu, Y., and Eisenberg, D. (2002). 3D domain swapping: as domains continue to swap. Protein Sci. 11, 1285- 1299.
67. Lobsanov, Y. D., Gitt, M. A., Leffler, H., Barondes, S. H., and Rini, J. M. (1993). X-ray crystal structure of the human dimeric S-Lac lectin, L-14-II, in complex with lactose at 2.9-A resolution. J. Biol. Chem. 268, 27034-27038.
68. Loeb, J. A., and Drickamer, K. (1988). Conformational changes in the chicken receptor for endocyto- sis of glycoproteins. Modulation of ligand-binding activity by Ca2+ and pH. J. Biol. Chem. 263, 9752-9760.
69. Ludwig,I.S.,Geijtenbeek,T.B.,andVan Kooyk,Y.(2006).Twowaycommunication between neutrophils and dendritic cells. Curr. Opin. Pharmacol. 6, 408-413.
70. Lund, V., and Olafsen, J. A. (1999). Changes in serum concentration of a serum amyloid P-like pentraxin in Atlantic salmon, Salmo salar L., during infection and inflamma- tion. Dev. Comp. Immunol. 23, 61-70.
71. Marschal, P., Herrmann, J., Leffler, H., Barondes, S. H., and Cooper, D. N. (1992). Sequence and specificity of a soluble lactose-binding lectin from Xenopus laevis skin. J. Biol. Chem. 267,12942-12949.
72. Marth, J. D., and Grewal, P. K. (2008). Mammalian glycosylation in immunity. Nat. Rev. Immunol. 8, 874-887.
73. Martinez, V. G., Pellizzari, E. H., Diaz, E.S.,Cigorraga,S.B.,Lustig,L.,Den- duchis,B.,Wolfenstein-Todel,C.,and Iglesias, M. M. (2004). Galectin-1, a cell adhesion modulator, induces apoptosis of rat Leydig cells in vitro. Glycobiology 14,127-137.
74. Mascanfroni, I. D., Cerliani, J. P., Dergan-Dylon, S., Croci, D. O., Ilarregui, J. M., and Rabinovich, G. A. (2011). Endogenous lectins shape the function of dendritic cells and tailor adaptive immunity: mechanisms and biomedical appli- cations. Int. Immunopharmacol. 11, 833-841.
75. Medzhitov, R., and Janeway, C. A. Jr. (2002). Decoding the patterns of self and nonself by the innate immune system. Science 296,298-300.
76. Mercier, S., St-Pierre, C., Pelletier, I., Ouellet, M., Tremblay, M. J., and Sato, S. (2008). Galectin-1 promotes HIV-1 infectivity in macrophages through stabilization of viral adsorp- tion. Virology 371,121-129.
77. Miao, E. A., and Warren, S. E. (2010). Innate immune detection of bacte- rial virulence factors via the NLRC4 inflammasome. J. Clin. Immunol. 30, 502-506.
78. Morris, S., Ahmad, N., Andre, S., Kaltner, H., Gabius, H. J., Brenowitz, M., and Brewer, F. (2004). Quaternary solution structures of galectins- 1, -3, and -7. Glycobiology 14, 293-300.
79. Myskova, J., Svobodova, M., Beverley, S. M., and Volf, P. (2007). A lipophosphoglycan-independent development of Leishmania in permissive sand flies. Microbes Infect. 9, 317-324.
80. Nagae, M., Nishi, N., Murata, T., Usui, T., Nakamura, T., Wakatsuki, S., and Kato,R.(2009).Structuralanalysisof the recognition mechanism of poly- N-acetyllactosamine by the human galectin-9 N-terminal carbohydrate recognition domain. Glycobiology 19, 112-117.
81. Nonaka, M. (2011). The complement C3proteinfamilyininvertebrates.ISJ 8,21-32.
82. Ogden, A. T., Nunes, I., Ko, K., Wu, S., Hines, C. S., Wang, A. F., Hegde, R. S.,and Lang,R. A. (1998). GRIFIN,a novel lens-specific protein related to thegalectinfamily.J.Biol.Chem.273, 28889-28896.
83. Ohtsubo, K., and Marth, J. D. (2006). Glycosylationincellularmechanisms of health and disease. Cell 126, 855-867.
84. Ohtsubo, K., Takamatsu, S., Minowa, M. T., Yoshida, A., Takeuchi, M., and Marth, J. D. (2005). Dietary and geneticcontrolofglucosetransporter 2 glycosylation promotes insulin secretioninsuppressingdiabetes.Cell 123,1307-1321.
85. Okumura, C. Y., Baum, L. G., and Johnson, P. J. (2008). Galectin-1 on cervical epithelial cells is a receptor for the sexually transmitted human parasite Trichomonas vaginalis. Cell. Microbiol. 10, 2078-2090.
86. Ouellet, M., Mercier, S., Pelletier, I., Bounou, S., Roy, J., Hirabayashi, J., Sato, S., and Tremblay, M. J. (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, 4120-4126.
87. Ozaki, K., Inoue, K., Sato, H., Iida, A., Ohnishi, Y., Sekine, A., Odashiro, K., Nobuyoshi,M.,Hori,M.,Nakamura, Y., and Tanaka, T. (2004). Functional variation in LGALS2 confers risk of myocardial infarction and regulates lymphotoxin-alphasecretioninvitro. Nature 429,72-75.
88. Partridge, E. A., Le Roy, C., Di Guglielmo, G. M., Pawling, J., Cheung, P., Granovsky, M., Nabi, I. R., Wrana, J. L., and Dennis, J. W. (2004). Regulation of cytokine receptors by Golgi N-glycan processing and endocytosis. Science 306, 120-124.
89. Patterson, R. J., Wang, W., and Wang, J. L. (2004). Understanding the biochemical activities of galectin-1 and galectin-3 in the nucleus. Glycoconj. J. 19,499-506.
90. Perillo, N. L., Marcus, M. E., and Baum, L. G. (1998). Galectins: versatile modulators of cell adhesion, cell proliferation, and cell death. J. Mol. Med. (Berl) 76, 402-412.
91. Perkins, F. O. (1996). The structure of Perkinsus marinus (Mackin, Owen and Collier, 1950) Levine, 1978 with comments on taxonomy and phylogeny of Perkinsus spp. J. Shellfish Res. 15,67-87.
92. Poirier, F. (2002). Roles of galectins in vivo.Biochem. Soc. Symp. 69,95-103.
93. Poirier, F., Timmons, P. M., Chan, C. T., Guenet, J. L., and Rigby, P. W. (1992). Expression of the L14 lectin during mouse embryogenesis suggests multiple roles during pre- and post-implantation development. Development 115,143-155.
94. Puche, A. C., Poirier, F., Hair, M., Bartlett, P. F., and Key, B. (1996). Role of galectin-1 in the developing mouse olfactory system. Dev. Biol. 179,274-287.
95. Rabinovich, G. A., Baum, L. G., Tinari, N., Paganelli, R., Natoli, C., Liu, F. T., and Iacobelli, S. (2002a). Galectins and their ligands: amplifiers, silencers or tuners of the inflammatory response? Trends Immunol. 23, 313-320.
96. Rabinovich,G.A.,Liu,F. T.,Hirashima, M., and Anderson, A. (2007a). An emerging role for galectins in tuning the immune response: lessons fromexperimentalmodelsof inflammatory disease, autoimmunity and cancer. Scand. J. Immunol. 66, 143-158.
97. Rabinovich, G. A., Rubinstein, N., and Toscano, M. A. (2002b). Role of galectins in inflammatory and immunomodulatory processes. Biochim. Biophys. Acta 1572, 274-284.
98. Rabinovich, G. A., and Toscano, M. A. (2009). Turning "sweet" on immu- nity: galectin-glycan interactions in immune tolerance and inflamma- tion. Nat. Rev. Immunol. 9, 338-352.
99. Rabinovich, G. A., Toscano, M. A., Jackson, S. S., and Vasta, G. R. (2007b). Functions of cell surface galectin-glycoprotein lattices. Curr. Opin. Struct. Biol. 17,513-520.
100. Rapoport, E. M., Andre, S., Kurmyshkina,O.V.,Pochechueva,T.V.,Severov, V. V., Pazynina, G. V., Gabius, H.-J., and Bovin, N. V. (2008). Galectinloaded cells as a platform for the profiling of lectin specificity by fluorescent neoglycoconjugates: a case study on galectins-1 and -3 and the impact of assay setting. Glycobiology 18, 315-324.
101. Rubinstein,N.,Ilarregui,J.M.,Toscano, M. A., and Rabinovich, G. A. (2004). The role of galectins in the initiation, amplification and resolution of the inflammatory response. Tissue Antigens 64, 1-12.
102. Saouros, S., Edwards-Jones, B., Reiss, M., Sawmynaden, K., Cota, E., Simpson, P., Dowse, T. J., Jakle, U., Ramboarina, S., Shivarattan, T., Matthews, S., and Soldati-Favre, D. (2005). A novel galectin-like domain from Toxoplasma gondii micronemal protein 1 assists the folding, assembly, and transport of a cell adhesion complex. J. Biol. Chem. 280, 38583-38591.
103. Sato, A., Mayer, W. E., Overath, P., and Klein, J. (2003). Genes encoding putative natural killer cell C-type lectin receptors in teleostean fishes. Proc. Natl. Acad. Sci. U.S.A. 100, 7779-7784.
104. Sato, S., and Hughes, R. C. (1992). Binding specificity of a baby hamster kidney lectin for H type I and II chains, polylactosamine glycans, and appropriately glycosylated forms of laminin and fibronectin. J. Biol. Chem. 267,6983-6990.
105. Sato, S., and Hughes, R. C. (1994). Regulation of secretion and surface expression of Mac-2, a galactoside-binding protein of macrophages. J. Biol. Chem. 269, 4424-4430.
106. Sato, S., and Nieminen, J. (2004). Seeing strangers or announcing "danger": galectin-3 in two models of innate immunity. Glycoconj. J. 19, 583-591.
107. Schroder, H. C., Ushijima, H., Theis, C., Seve, A. P., Hubert, J., and Muller, W. E. (1995). Expression of nuclear lectin carbohydrate-binding protein 35 in human immunodefi- ciency virus type 1-infected Molt-3 cells. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 9,340-348.
108. Schwarz, F. P., Ahmed, H., Bianchet, M. A., Amzel, L. M., and Vasta, G. R. (1998). Thermodynamics of bovine spleengalectin-1bindingtodisaccharides: correlation with structure and its effect on oligomerization at the denaturation temperature. Biochemistry 37, 5867-5877.
109. Seetharaman, J., Kanigsberg, A., Slaaby, R., Leffler, H., Barondes, S. H., and Rini, J. M. (1998). X-ray crystal structure of the human galectin-3 carbohydrate recognition domain at 2.1-A resolution. J. Biol. Chem. 273, 13047-13052.
110. Seong, S.-Y., and Matzinger, P. (2004). Hydrophobicity: an ancient damage- associatedmolecularpatternthatinitiates innate immune responses. Nat. Rev. Immunol. 4, 469-478.
111. Shirai, T., Matsui, Y., Shionyu-Mitsuyama, C., Yamane, T., Kamiya, H., Ishii, C., Ogawa, T., and Muramoto, K. (2002). Crystal structure of a conger eel galectin (congerin II) at 1.45A resolution: implication for the accelerated evolution of a new ligand-binding site followinggeneduplication.J.Mol.Biol.321, 879-889.
112. Shirai, T., Mitsuyama, C., Niwa, Y., Matsui, Y., Hotta, H., Yamane, T., Kamiya, H., Ishii, C., Ogawa, T., and Muramoto, K. (1999). Highresolution structure of the conger eel galectin, congerin I, in lactoseliganded and ligand-free forms: emergence of a new structure class by accelerated evolution. Structure 7, 1223-1233.
113. Shoji, H., Deltour, L., Nakamura, T., Tajbakhsh, S., and Poirier, F. (2009). Expression pattern and role of Galectin1 during early mouse myogenesis. Dev. Growth Differ. 51, 607-615.
114. Shoji, H., Nishi, N., Hirashima, M., and Nakamura, T. (2003). Characteriza- tion of the Xenopus galectin family. Three structurally different types as in mammals and regulated expression during embryogenesis. J. Biol. Chem. 278,12285-12293.
115. Sparrow, C. P., Leffler, H., and Barondes, S. H. (1987). Multiple soluble beta-galactoside-binding lectins from human lung. J. Biol. Chem. 262, 7383-7390.
116. Stalz, H., Roth, U., Schleuder, D., Macht, M., Haebel, S., Strupat, K., Peter-Katalinic, J., and Hanisch, F. G. (2006). The Geodia cydonium galectin exhibits prototype and chimera-type characteristics and a unique sequence polymorphism within its carbohydrate recognition domain. Glycobiology 16, 402-414.
117. Stowell, S. R., Arthur, C. M., Dias-Baruffi, M., Rodrigues, L. C., Gourdine,J. P.,Heimburg-Molinaro,J.,Ju, T., Molinaro, R. J., Rivera-Marrero, C., Xia, B., Smith, D. F., and Cummings, R. D. (2010). Innate immune lectins kill bacteria expressing blood group antigen. Nat. Med. 16, 295-301.
118. 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., and Cummings, R. D. (2009). Ligand reduces galectin-1 sensitivitytooxidativeinactivationby enhancing dimer formation. J. Biol. Chem. 284,4989-4999.
119. Stowell, S. R., Qian, Y., Karmakar, S., Koyama, N. S., Dias-Baruffi, M., Leffler,H.,Mcever,R.P.,andCummings, R. D. (2008). Differential roles of galectin-1 and galectin-3 in regulating leukocyte viability and cytokine secretion. J. Immunol. 180, 3091- 3102.
120. Takenaka, Y., Fukumori, T., and Raz, A. (2004). Galectin-3 and metastasis. Glycoconj. J. 19, 543-549.
121. Tasumi, S., and Vasta, G. R. (2007). A galectin of unique domain organization from hemocytes of the Eastern oyster (Crassostrea virginica)is a receptor for the protistan parasite Perkinsus marinus. J. Immunol. 179, 3086-3098.
122. Tomizawa, T., Kigawa, T., Saito, K., Koshiba, S., Inoue, M., and Yokoyama, S. (2005). Solution structure of the C-terminal gal-bind lectin domain from human galectin-4. Structural Genomics and Proteomics Initiative (RSGI),Riken.
123. Troncoso, M. F., Elola, M. T., Croci, D. O., and Rabinovich, G. A. (2012). Integrating structure and function of "tandem-repeat" galectins. Front. Biosci. (Schol Ed) 4,864-887.
124. van der Vlist, M., van der Aar, A. M., Gringhuis, S. I., and Geijtenbeek, T. B. (2011). Innate signaling in HIV-1 infection of dendritic cells. Curr. Opin. HIV AIDS 6,348-352.
125. Vasta, G. R. (2009). Roles of galectins in infection. Nat. Rev. Microbiol. 7, 424-438.
126. Vasta, G. R., and Ahmed, H. (2009). Animal Lectins: A Functional View. Boca Raton, FL: CRC Press (Taylor & Francis Group).
127. Vasta, G. R., Ahmed, H., Amzel, L. M., andBiahchet,M.A.(1997).Galectins from amphibian species: carbohy-drate specificity, molecular structure and evolution. Trends Blycosci. Glycotechnol. 9, 131-144.
128. Vasta, G. R., Hunt, J. C., Marchalonis, J. J.,andFish,W.W.(1986).Galactosyl- binding lectins from the tunicate Didemnum candidum. Purification and physicochemical characterization. J. Biol. Chem. 261,9174-9181.
129. Vasta, G. R., Quesenberry, M., Ahmed, H., and O'Leary, N. (1999). C- type lectins and galectins mediate innate and adaptive immune functions: their roles in the complement activation pathway. Dev. Comp. Immunol. 23, 401-420.
130. Vilches,C.,and Parham,P. (2002). KIR: diverse, rapidly evolving receptors of innateandadaptiveimmunity.Annu. Rev. Immunol. 20,217-251.
131. Vokhmyanina, O. A., Rapoport, E. M., Ryzhov, I. M., Korchagina, E. Y., Pazynina, G. V., Severov, V. V., Kaltner, H., Andre, S., Gabius, H. J., and Bovin, N. V. (2011). Carbohydrate specificity of chicken and human tandem-repeat-type galectins-8 in composition of cells. Biochemistry (Mosc) 76,1185-1192.
132. Volf, P., Benkova, I., Myskova, J., Sadlova, J., Campino, L., and Ravel, C. (2007). Increased transmission potential of Leishmania major/Leishmania infantum hybrids. Int. J. Parasitol. 37,589-593.
133. Vyakarnam, A., Dagher, S. F., Wang, J. L., and Patterson, R. J. (1997). Evidence for a role for galectin-1 in pre-mRNA splicing. Mol. Cell. Biol. 17,4730-4737.
134. Wallis, R. (2002). Structural and functional aspects of complement activation by mannose-binding protein. Immunobiology 205,433-445.
135. Walser, P. J., Haebel, P. W., Kunzler, M., Sargent, D., Kues, U., Aebi, M., and Ban, N. (2004). Structure and functional analysis of the fungal galectin CGL2. Structure 12, 689-702.
136. Walser,P.J.,Kues,U.,Aebi,M.,andKunzler, M. (2005). Ligand interactions of the Coprinopsis cinerea galectins. Fungal Genet. Biol. 42, 293-305.
137. Weis, W. I., Drickamer, K., and Hendrickson, W. A. (1992). Structure of a C-type mannose-binding protein complexed with an oligosaccharide. Nature 360,127-134.
138. Weis, W. I., Kahn, R., Fourme, R., Drickamer, K., and Hendrickson, W. A. (1991). Structure of the calcium-dependent lectin domain from a rat mannose-binding protein deter- mined by MAD phasing. Science 254, 1608-1615.
139. Weis, W. I., Taylor, M. E., and Drickamer, K. (1998). The C-type lectin superfamily in the immune system. Immunol. Rev. 163,19-34.
140. Yoshino, T. P., Dinguirard, N., Kunert, J., and Hokke, C. H. (2008). Molecular and functional characterization of a tandem-repeat galectin from the freshwater snail Biomphalaria glabrata, intermediate host of the human blood fluke Schistosoma mansoni. Gene 411, 46-58.
141. Zelensky,A.N.,andGready,J.E.(2005). TheC-typelectin-likedomainsupefamily. FEBS J. 272,6179-6217.
142. Zhou,Q.,and Cummings,R. D. (1990). The S-type lectin from calf heart tissue binds selectively to the carbohydrate chains of laminin. Arch. Biochem. Biophys. 281, 27-35