Lectins: a primer for histochemists and cell biologists

Histochemistry and Cell Biology

Volumn 147, Issue 2, 2017, Pages 199-222

  Manning, Joachim C ^a   Romero, Antonio ^b   Habermann, Felix A ^a   García Caballero, Gabriel ^a   Kaltner, Herbert ^a   Gabius, Hans Joachim ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

Agglutinin; Glycoprotein; Glycosylation; Protein fold; Sialylation

Indexed keywords

GLYCAN; LEUKOAGGLUTININ; MONOSACCHARIDE; PLANT LECTIN; LECTIN;

ANTIGEN ANTIBODY REACTION; ARTOCARPUS HETEROPHYLLUS; BIOCHEMISTRY; CANAVALIA ENSIFORMIS; CYTOLOGY; ERYTHROCYTE; GRIFFONIA SIMPLICIFOLIA; HISTOCHEMISTRY; HISTORY; LIMAX FLAVUS; MAACKIA AMURENSIS; MEDICINE; NONHUMAN; PEANUT; PHASEOLUS VULGARIS; POLYPORUS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SAMBUCUS NIGRA; TRITICUM AESTIVUM; VISCUM ALBUM; ANIMAL; CHEMISTRY; GLYCOSYLATION; HUMAN; IMMUNOLOGY; PROTEIN FOLDING;

ANIMALS; CELL BIOLOGY; GLYCOSYLATION; HUMANS; LECTINS; PROTEIN FOLDING;

EID: 85007227709     PISSN: 09486143     EISSN: 1432119X     Source Type: Journal    
DOI: 10.1007/s00418-016-1524-6     Document Type: Review

References (111)

1. Agrawal BBL, Goldstein IJ (1965) Specific binding of concanavalin A to cross-linked dextran gel. Biochem J 96:23c–25c
2. André S, Kaltner H, Kayser K, Murphy PV, Gabius H-J (2016) Merging carbohydrate chemistry with lectin histochemistry to study inhibition of lectin binding by glycoclusters in the natural tissue context. Histochem Cell Biol 145:185–199
3. Antonopoulos A, North SJ, Haslam SM, Dell A (2011) Glycosylation of mouse and human immune cells: insights emerging from N-glycomics analyses. Biochem Soc Trans 39:1334–1340
4. Aulthouse AL, Solursh M (1987) The detection of a precartilage, blastema-specific marker. Dev Biol 120:377–384
5. Barbieri L, Battelli MG, Stirpe F (1993) Ribosome-inactivating proteins from plants. Biochim Biophys Acta 1154:237–282
6. Barondes SH (1988) Bifunctional properties of lectins: lectins redefined. Trends Biochem Sci 13:480–482
7. Bennett HS (1963) Morphological aspects of extracellular polysaccharides. J Histochem Cytochem 11:14–23
8. Bhide GP, Colley KJ (2017) Sialylation of N-glycans: mechanism, cellular compartmentalization and function. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1520-x
9. Bird GWG (1989) Lectins in immunohematology. Transfus Med Rev 3:55–62
10. Bittiger H, Schnebli HP (eds) (1976) Concanavalin A as a tool. Wiley, London
11. Borrebaeck CAK, Carlsson R (1989) Lectins as mitogens. Adv Lectin Res 2:1–27
12. Boyd WC (1954) The proteins of immune reactions. In: Neurath H, Bailey K (eds) The proteins, vol 2, part 2. Academic Press, New York, pp 756–844
13. Boyd WC (1963) The lectins: their present status. Vox Sang 8:1–32
14. Boyd WC, Shapleigh E (1954) Specific precipitating activity of plant agglutinins (lectins). Science 119:419
15. Brinkman-Van der Linden EC, Sonnenburg JL, Varki A (2002) Effects of sialic acid substitutions on recognition by Sambucus nigra agglutinin and Maackia amurensis hemagglutinin. Anal Biochem 303:98–104
16. Buddecke E (2009) Proteoglycans. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 199–216
17. Chargaff E (1970) Vorwort zu einer Grammatik der Biologie. Hundert Jahre Nukleinsäureforschung. Experientia 26:810–816
18. Chargaff E (1977) Voices in the labyrinth. Seabury Press, New York
19. Clerc F, Reiding KR, Jansen BC, Kammeijer GS, Bondt A, Wuhrer M (2016) Human plasma protein N-glycosylation. Glycoconj J 33:309–343
20. Corfield AP (2015) Mucins: a biologically relevant glycan barrier in mucosal protection. Biochim Biophys Acta 1850:236–252
21. Corfield AP (2017) Protein glycosylation: a primer for histochemists and cell biologists. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1526-4
22. Corfield AP, Berry M (2015) Glycan variation and evolution in the eukaryotes. Trends Biochem Sci 40:351–359
23. Dahm R (2005) Friedrich Miescher and the discovery of DNA. Dev Biol 278:274–288
24. Edelman GM, Cunningham BA, Reeke GN Jr, Becker JW, Waxdal MJ, Wang JL (1972) The covalent and three-dimensional structure of concanavalin A. Proc Natl Acad Sci USA 69:2580–2584
25. Eichwald E (1865) Beiträge zu Chemie der gewebbildenden Substanzen und ihrer Abkömmlinge. I. Ueber das Mucin, besonders der Weinbergschnecke. Ann Chem Pharm 134:177–211
26. Einhoff W, Fleischmann G, Freier T, Kummer H, Rüdiger H (1986) Interactions between lectins and other components of leguminous protein bodies. Biol Chem Hoppe Seyler 367:15–25
27. Elfstrand M (1898) Ueber blutkörperchenagglutinierende Eiweisse. In: Kobert R (ed) Görbersdorfer Veröffentlichungen. F. Enke, Stuttgart, pp 1–159
28. Endo Y (1989) Mechanism of action of ricin and related toxic lectins on the inactivation of eukaryotic ribosomes. Adv Lectin Res 2:60–73
29. Feinberg H, Rowntree TJ, Tan SL, Drickamer K, Weis WI, Taylor ME (2013) Common polymorphisms in human langerin change specificity for glycan ligands. J Biol Chem 288:36762–36771
30. Gabius H-J (1997) Animal lectins. Eur J Biochem 243:543–576
31. Gabius H-J (2002) Animal lectins and life: a guided tour into the realm of the sugar code. Biochim Biophys Acta 1572:163–164
32. Gabius H-J (ed) (2009a) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim
33. Gabius H-J (2009b) Animal and human lectins. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 317–328
34. Gabius H-J (2015) The magic of the sugar code. Trends Biochem Sci 40:341
35. Gabius H-J, Roth J (2017) An introduction to the sugar code. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1521-9
36. Gabius H-J, Springer WR, Barondes SH (1985) Receptor for the cell binding site of discoidin I. Cell 42:449–456
37. Gabius H-J, Bodanowitz S, Schauer A (1988) Endogenous sugar-binding proteins in human breast tissue and benign and malignant breast lesions. Cancer 61:1125–1131
38. Gabius H-J, Gabius S, Zemlyanukhina TV, Bovin NV, Brinck U, Danguy A, Joshi SS, Kayser K, Schottelius J, Sinowatz F, Tietze LF, Vidal-Vanaclocha F, Zanetta J-P (1993) Reverse lectin histochemistry: design and application of glycoligands for detection of cell and tissue lectins. Histol Histopathol 8:369–383
39. Gabius H-J, André S, Jiménez-Barbero J, Romero A, Solís D (2011) From lectin structure to functional glycomics: principles of the sugar code. Trends Biochem Sci 36:298–313
40. Gabius H-J, Kaltner H, Kopitz J, André S (2015) The glycobiology of the CD system: a dictionary for translating marker designations into glycan/lectin structure and function. Trends Biochem Sci 40:360–376
41. Gabius H-J, Manning JC, Kopitz J, André S, Kaltner H (2016) Sweet complementarity: the functional pairing of glycans with lectins. Cell Mol Life Sci 73:1989–2016
42. García Caballero G, Flores-Ibarra A, Michalak M, Khasbiullina N, Bovin NV, André S, Manning JC, Vértesy S, Ruiz FM, Kaltner H, Kopitz J, Romero A, Gabius H-J (2016a) Galectin-related protein: an integral member of the network of chicken galectins. 1. From strong sequence conservation of the gene confined to vertebrates to biochemical characteristics of the chicken protein and its crystal structure. Biochim Biophys Acta 1860:2285–2297
43. García Caballero G, Kaltner H, Michalak M, Shilova NV, Yegres M, André S, Ludwig A-K, Manning JC, Schmidt S, Schnölzer M, Bovin NV, Reusch D, Kopitz J, Gabius H-J (2016b) Chicken GRIFIN: a homodimeric member of the galectin network with canonical properties and a unique expression profile. Biochimie 128–129:34–47
44. Gilbert HJ, Knox JP, Boraston AB (2013) Advances in understanding the molecular basis of plant cell wall polysaccharide recognition by carbohydrate-binding modules. Curr Opin Struct Biol 23:669–677
45. Goldstein IJ, Poretz RD (1986) Isolation, physicochemical characterization, and carbohydrate-binding specificity of lectins. In: Liener IE, Sharon N, Goldstein IJ (eds) The lectins. Properties, functions, and applications in biology and medicine. Academic Press, Orlando, pp 33–247
46. Gready JN, Zelensky AN (2009) Routes in lectin evolution: case study on the C-type lectin-like domains. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 329–346
47. Habermann FA, André S, Kaltner H, Kübler D, Sinowatz F, Gabius H-J (2011) Galectins as tools for glycan mapping in histology: comparison of their binding profiles to the bovine zona pellucida by confocal laser scanning microscopy. Histochem Cell Biol 135:539–552
48. Hardman KD, Ainsworth CF (1972) Structure of concanavalin A at 2.4-Å resolution. Biochemistry 11:4910–4919
49. Hartley MR, Lord JM (2004) Cytotoxic ribosome-inactivating lectins from plants. Biochim Biophys Acta 1701:1–14
50. Higuero AM, Díez-Revuelta N, Abad-Rodríguez J (2017) The sugar code in neuronal physiology. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1519-3
51. Hughes-Jones NC, Gardner B (2002) Red cell agglutination: the first description by Creite (1869) and further observations made by Landois (1875) and Landsteiner (1901). Br J Haematol 119:889–893
52. Inamdar SR, Eligar SM, Ballal S, Belur S, Kalraiya RD, Swamy BM (2016) Exquisite specificity of mitogenic lectin from Cephalosporium curvulum to core fucosylated N-glycans. Glycoconj J 33:19–28
53. n antigen: structural simplicity and biological complexity. Angew Chem Int Ed 50:1770–1791
54. Kaltner H, Gabius H-J (2012) A toolbox of lectins for translating the sugar code: the galectin network in phylogenesis and tumors. Histol Histopathol 27:397–416
55. Kaltner H, Toegel S, García Caballero G, Manning JC, Ledeen RW, Gabius H-J (2017) Galectins: their network and roles in immunity/tumor growth control. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1522-8
56. Kayser K, Bovin NV, Korchagina EY, Zeilinger C, Zeng F-Y, Gabius H-J (1994) Correlation of expression of binding sites for synthetic blood group A-, B-, and H-trisaccharides and for sarcolectin with survival of patients with bronchial carcinoma. Eur J Cancer 30A:653–657
57. Kelm S, Schauer R, Manuguerra JC, Gross HJ, Crocker PR (1994) Modifications of cell surface sialic acids modulate cell adhesion mediated by sialoadhesin and CD22. Glycoconj J 11:576–585
58. Kilpatrick DC (2000) Handbook of animal lectins. Properties and biomedical applications. Wiley, Chichester
59. Kilpatrick DC, Green C (1992) Lectins as blood typing reagents. Adv Lectin Res 5:51–94
60. Knospe C (1984) Ein Beitrag zur Frage der Herkunft der Cardiadrüsen der Katze. Z mikrosk-anat Forsch 98:764–774
61. Kopitz J (2017) Lipid glycosylation: a primer for histochemists and cell biologists. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1518-4
62. Krüpe M (1956) Blutgruppenspezifische pflanzliche Eiweißkörper, Phytagglutinine. F. Enke, Stuttgart
63. Lis H, Sharon N (1981) Affinity chromatography for the purification of lectins (a review). J Chromatogr 215:361–372
64. Lohr M, Kaltner H, Schwartz-Albiez R, Sinowatz F, Gabius H-J (2010) Towards functional glycomics by lectin histochemistry: strategic probe selection to monitor core and branch-end substitutions and detection of cell-type and regional selectivity in adult mouse testis and epididymis. Anat Histol Embryol 39:481–493
65. Loris R (2002) Principles of structures of animal and plant lectins. Biochim Biophys Acta 1572:198–208
66. Lucocq JM, Roth J (1984) Applications of immunocolloids in light microscopy. III. Demonstration of antigenic and lectin-binding sites in semithin resin sections. J Histochem Cytochem 32:1075–1083
67. Mayer S, Raulf M-K, Lepenies B (2017) C-type lectins: their network and roles in immunity/pathogen recognition. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1523-7
68. Mitchell SW (1860) Researches upon the venom of the rattlesnake. Smithson Contrib Knowl XII:89–90
69. Mitchell SW, Reichert ET (1886) Researches upon the venoms of poisonous serpents. Smithson Contrib Knowl XXVI:155
70. Moise A, André S, Eggers F, Krzeminski M, Przybylski M, Gabius H-J (2011) Toward bioinspired galectin mimetics: identification of ligand-contacting peptides by proteolytic-excision mass spectrometry. J Am Chem Soc 133:14844–14847
71. Nagae M, Yamaguchi Y (2015) Sugar recognition and protein-protein interaction of mammalian lectins conferring diverse functions. Curr Opin Struct Biol 34:108–115
72. Nowell PC (1960) Phytohemagglutinin: an inhibitor of mitosis in cultures of normal human leukocytes. Cancer Res 20:462–466
73. Patsos G, Corfield AP (2009) O-Glycosylation: structural diversity and function. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 111–137
74. Percec V, Leowanawat P, Sun HJ, Kulikov O, Nusbaum CD, Tran TM, Bertin A, Wilson DA, Peterca M, Zhang S, Kamat NP, Vargo K, Moock D, Johnston ED, Hammer DA, Pochan DJ, Chen Y, Chabre YM, Shiao TC, Bergeron-Brlek M, André S, Roy R, Gabius H-J, Heiney PA (2013) Modular synthesis of amphiphilic Janus glycodendrimers and their self-assembly into glycodendrimersomes and other complex architectures with bioactivity to biomedically relevant lectins. J Am Chem Soc 135:9055–9077
75. Pita R (2009) Toxin weapons: from World War I to jihadi terrorism. Toxin Rev 28:219–237
76. Quiocho FA (1986) Carbohydrate-binding proteins: tertiary structures and protein-sugar interactions. Annu Rev Biochem 55:287–315
77. Reuter G, Gabius H-J (1996) Sialic acids: structure-analysis-metabolism-occurrence-recognition. Biol Chem Hoppe Seyler 377:325–342
78. Reuter G, Gabius H-J (1999) Eukaryotic glycosylation: whim of nature or multipurpose tool? Cell Mol Life Sci 55:368–422
79. Roth J (1983a) Application of lectin-gold complexes for electron microscopic localization of glycoconjugates on thin sections. J Histochem Cytochem 31:987–999
80. Roth J (1983b) The colloidal gold marker system for light and electron microscopic cytochemistry. In: Bullock GR, Petrusz P (eds) Techniques in immunocytochemistry. Academic Press, London, pp 217–284
81. Roth J (1996) Protein glycosylation in the endoplasmic reticulum and the Golgi apparatus and cell-type specificity of cell surface glycoconjugate expression: analysis by protein A-gold and lectin-gold techniques. Histochem Cell Biol 106:79–92
82. Roth J (2011) Lectins for histochemical demonstration of glycans. Histochem Cell Biol 136:117–130
83. Roth J, Zuber C (2017) Quality control of glycoprotein folding and ERAD: the role of N-glycan handling, EDEM1 and OS-9. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1513-9
84. Roth J, Lucocq JM, Charest PM (1984) Light and electron microscopic demonstration of sialic acid residues with the lectin from Limax flavus: a cytochemical affinity technique with the use of fetuin-gold complexes. J Histochem Cytochem 32:1167–1176
85. Roth J, Wang Y, Eckhardt AE, Hill RL (1994) Subcellular localization of the UDP-N-acetyl-d-galactosamine: polypeptide N-acetylgalactosaminyltransferase-mediated O-glycosylation reaction in the submaxillary gland. Proc Natl Acad Sci USA 91:8935–8939
86. Roy R, Murphy PV, Gabius H-J (2016) Multivalent carbohydrate-lectin interactions: how synthetic chemistry enables insights into nanometric recognition. Molecules 21:629
87. Roy R, Cao Y, Kaltner H, Kottari N, Shiao TC, Belkhadem K, André S, Manning JC, Murphy PV, Gabius H-J (2017) Teaming up synthetic chemistry and histochemistry for activity screening in galectin-directed inhibitor design. Histochem Cell Biol 147(2). doi:10.1007/s00418-016-1525-5
88. Rüdiger H, Gabius H-J (2009a) The history of lectinology. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 261–268
89. Rüdiger H, Gabius H-J (2009b) Plant lectins. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 301–315
90. Ruiz FM, Scholz BA, Buzamet E, Kopitz J, André S, Menendez M, Romero A, Solís D, Gabius H-J (2014) Natural single amino acid polymorphism (F19Y) in human galectin-8: detection of structural alterations and increased growth-regulatory activity on tumor cells. FEBS J 281:1446–1464
91. Schecher G, Rüdiger H (1994) Interaction of the soybean (Glycine max) seed lectin with components of the soybean protein body membrane. Biol Chem Hoppe Seyler 375:829–832
92. Schlossman SF, Kabat EA (1962) Specific fractionation of a population of antidextran molecules with combining sites of various sizes. J Exp Med 116:535–552
93. Sharon N (1998) Lectins: from obscurity into the limelight. Protein Sci 7:2042–2048
94. Sjoberg ER, Powell LD, Varki A (1994) Natural ligands of the B cell adhesion molecule CD22b can be masked by 9-O-acetylation of sialic acids. J Cell Biol 126:549–562
95. Solís D, Bovin NV, Davis AP, Jiménez-Barbero J, Romero A, Roy R, Smetana K Jr, Gabius H-J (2015) A guide into glycosciences: how chemistry, biochemistry and biology cooperate to crack the sugar code. Biochim Biophys Acta 1850:186–235
96. Stillmark H (1888) Ueber Ricin, ein giftiges Ferment aus den Samen von Ricinus comm. L. und einigen anderen Euphorbiaceen. Schnakenburg’s Buchdruckerei, Dorpat
97. Straus W (1981) Cytochemical detection of mannose-specific receptors for glycoproteins with horseradish peroxidase as a ligand. Histochemistry 73:39–47
98. Sumner JB, Howell SF (1935) The non-identity of jack bean agglutinin with crystalline urease. J Immunol 29:133–134
99. Sumner JB, Howell SF (1936) Identification of hemagglutinin of jack bean with concanavalin A. J Bacteriol 32:227–237
100. Swanson MD, Boudreaux DM, Salmon L, Chugh J, Winter HC, Meagher JL, André S, Murphy PV, Oscarson S, Roy R, King S, Kaplan MH, Goldstein IJ, Tarbet EB, Hurst BL, Smee DF, de la Fuente C, Hoffmann HH, Xue Y, Rice CM, Schols D, García JV, Stuckey JA, Gabius H-J, Al-Hashimi HM, Markovitz DM (2015) Engineering a therapeutic lectin by uncoupling mitogenicity from antiviral activity. Cell 163:746–758
101. Taatjes DJ, Schaub U, Roth J (1987) Light microscopical detection of antigens and lectin binding sites with gold-labelled reagents on semi-thin Lowicryl K4M sections: usefulness of the photochemical silver reaction for signal amplification. Histochem J 19:235–245
102. Taatjes DJ, Roth J, Peumans W, Goldstein IJ (1988) Elderberry bark lectin: gold techniques for the detection of Neu5Acα2,6Gal/GalNAc sequences: applications and limitations. Histochem J 20:478–490
103. Taylor ME, Drickamer K (2014) Convergent and divergent mechanisms of sugar recognition across kingdoms. Curr Opin Struct Biol 28:14–22
104. Toma V, Zuber C, Winter HC, Goldstein IJ, Roth J (2001) Application of a lectin from the mushroom Polysporus squamosus for the histochemical detection of the NeuAcα2,6Galβ1,4Glc/GlcNAc sequence of N-linked oligosaccharides: a comparison with the Sambucus nigra lectin. Histochem Cell Biol 116:183–193
105. Wilson IBH, Paschinger H, Rendic D (2009) Glycosylation of model and ‘lower’ organisms. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 139–154
106. Worbs S, Kohler K, Pauly D, Avondet MA, Schaer M, Dorner MB, Dorner BG (2011) Ricinus communis intoxications in human and veterinary medicine: a summary of real cases. Toxins 3:1332–1372
107. Zhang S, Moussodia R-O, Vértesy S, André S, Klein ML, Gabius H-J, Percec V (2015a) Unraveling functional significance of natural variations of a human galectin by glycodendrimersomes with programmable glycan surface. Proc Natl Acad Sci USA 112:5585–5590
108. Zhang S, Moussodia R-O, Murzeau C, Sun HJ, Klein ML, Vértesy S, André S, Roy R, Gabius H-J, Percec V (2015b) Dissecting molecular aspects of cell interactions using glycodendrimersomes with programmable glycan presentation and engineered human lectins. Angew Chem Int Ed 54:4036–4040
109. Zimmermann B, Thies M (1984) Alterations of lectin binding during chondrogenesis of mouse limb buds. Histochemistry 81:353–361
110. Zuber C, Roth J (2009) N-Glycosylation. In: Gabius H-J (ed) The sugar code. Fundamentals of glycosciences. Wiley, Weinheim, pp 87–110
111. Zuber C, Paulson JC, Toma V, Winter HC, Goldstein IJ, Roth J (2003) Spatiotemporal expression patterns of sialoglycoconjugates during nephron morphogenesis and their regional and cell type-specific distribution in adult rat kidney. Histochem Cell Biol 120:143–160