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Lectin Histochemistry: Historical Perspectives, State of the Art, and the Future

  • Susan A. BrooksEmail author
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1560)

Abstract

Lectins, discovered more than 100 years ago and defined by their ability to selectively recognize specific carbohydrate structures, are ubiquitous in living organisms. Their precise functions are as yet under-explored and incompletely understood but they are clearly involved, through recognition of their binding partners, in a myriad of biological mechanisms involved in cell identity, adhesion, signaling, growth regulation, in health and disease. Understanding the complex “sugar code” represented by the glycome is a major challenge and at the forefront of current biological research. Lectins have been widely employed in histochemical studies to map glycosylation in cells and tissues. Here, a brief history of the discovery of lectins and early developments in their use is presented along with a selection of some of the most interesting and significant discoveries to emerge from use of lectin histochemistry. Further, an evaluation of the next generation of lectin-based technologies is presented, including the potential for designing recombinant lectins with more precisely defined binding characteristics, linking lectin-based studies with other technologies to answer fundamental questions in glycobiology, and approaches to exploring the interactions of lectins with their binding partners in more detail.

Key words

Lectin histochemistry History Carbohydrates Glycosylation Review Methodology Glycomics 

References

  1. 1.
    Boyd WC, Shapleigh E (1954) Separation of individuals of any blood group into secretors and non-secretors by use of a plant agglutinin (lectin). Blood 9:1195–1198Google Scholar
  2. 2.
    Goldstein IJ, Hughes RC, Monsigny M et al (1980) What should be called a lectin? Nature 285:66CrossRefGoogle Scholar
  3. 3.
    Kocourek J (1986) Historical background. In: Liener IR, Sharon N, Goldstein IJ (eds) The lectins: properties, functions and applications in biology and medicine. Academic Press, London, pp 3–33Google Scholar
  4. 4.
    Sharon N, Lis H (2004) History of lectins: from hemagglutinins to biological recognition molecules. Glycobiology 14:53R–63RCrossRefPubMedGoogle Scholar
  5. 5.
    Watkins WM, Morgan WT (1952) Neutralization of the anti-H agglutinin in eel serum by simple sugars. Nature 169:825–826CrossRefPubMedGoogle Scholar
  6. 6.
    Boyd WC, Reguera RM (1949) Haemagglutinating substances for human cells in various plants. J Immunol 62:333–339PubMedGoogle Scholar
  7. 7.
    Morgan WTJ, Watkins WM (1959) The inhibition of the haemagglutinins in plant seeds by human blood group substances and simple sugars. Br J Exp Pathol 34:94–103Google Scholar
  8. 8.
    Hudgin RL, Pricer WE Jr, Ashwell G et al (1974) The isolation and properties of a rabbit liver binding protein specific for asialoglycoproteins. J Biol Chem 249:5536–5543PubMedGoogle Scholar
  9. 9.
    Teichberg VI, Silman I, Beitsch DD et al (1975) A a-D-galactoside binding protein in the electric organ tissue of Electrophorus electricus. Proc Natl Acad Sci USA 72:1383–1387CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Ley K (2003) The role of selectins in inflammation and disease. Trends Mol Med 9:263–268CrossRefPubMedGoogle Scholar
  11. 11.
    Dommett RM, Klein N, Turner MW (2006) Mannose-binding lectin in innate immunity: past, present and future. Tissue Antigens 68:193–209CrossRefPubMedGoogle Scholar
  12. 12.
    Roth J (2011) Lectins for histochemical demonstration of glycans. Histochem Cell Biol 136:117–130CrossRefPubMedGoogle Scholar
  13. 13.
    Khan S, Brooks SA, Leathem AJC (1994) GalNAc-type glycoproteins in breast cancer – a 26 lectin study. J Pathol 172(Suppl):134AGoogle Scholar
  14. 14.
    Goldstein IJ, Poretz RD (1986) Chapter 2: isolation, physiochemical characterization, and carbohydrate-binding specificity of lectins. In: Liener IR, Sharon N, Goldstein IJ (eds) The lectins: properties, functions and applications in biology and medicine. Academic Press, London, pp 35–250Google Scholar
  15. 15.
    Miller R, Collowan J, Fish W (1982) Purification and molecular properties of a sialic acid-specific lectin from the slug Limax flavus. J Biol Chem 257:7574–7580PubMedGoogle Scholar
  16. 16.
    Mo HQ, Winter HC, Goldstein IJ (2000) Purification and characterisation of a Neu5Ac alpha2-6Gal beta1-4Glc/GalNAc-specific lectin from the fruiting body of the polypore mushroom Polporus squamosus. J Biol Chem 275:10623–10629CrossRefPubMedGoogle Scholar
  17. 17.
    Wang WC, Cummings RD (1988) The immobilised leukoagglutinin from the seeds of Maakia amurensis binds with high affinity to complex type asn-linked oligosaccharides containing terminal sialic acid a2,3 linked to penultimate galactose residues. J Biol Chem 263:4576–4585PubMedGoogle Scholar
  18. 18.
    Taatjes DJ, Roth J, Peumans W et al (1988) Elderberry bark lectin-gold techniques for the detection of NeuAc (alpha2,6) Gal/GalNAc sequences : applications and limitations. Histochem J 20:478–490CrossRefPubMedGoogle Scholar
  19. 19.
    Coons AH, Creech HJ, Jones RN (1941) Immunological properties of an antibody containing a fluorescent group. Proc Soc Exp Biol Med 47:200–202CrossRefGoogle Scholar
  20. 20.
    Coons AH, Leduc EH, Connolly JM (1955) Studies on antibody production. I: a method for the histochemical demonstration of specific antibody and its application to a study of the hyperimmune rabbit. J Exp Med 102:49–60CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Coons AH, Kaplan MH (1950) Localisation of antigen in tissue cells. J Exp Med 91:1–13CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Polak JM, Van Noorden S (1997) Introduction to immunocytochemistry, 2nd edn, Chapter 1 introduction. Royal Microscopical Society Handbooks number 37. Bios Scientific Publishers Ltd, Oxford, pp 1–4Google Scholar
  23. 23.
    Aub JC, Tieslau C, Lankester A (1963) Reactions of normal and tumour cell surfaces to enzymes. I wheat-germ lipase and associated mucopolysaccharides. Proc Natl Acad Sci USA 50:613–619CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Inbar M, Sachs L (1969) Interaction of the carbohydrate-binding protein concanavalin A with normal and transformed cells. Proc Natl Acad Sci USA 63:1418–1425CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Sela BA, Lis H, Sharon N et al (1970) Different locations of carbohydrate-containing sites at the surface membrane of normal and transformed mammalian cells. J Membr Biol 3:267–279CrossRefPubMedGoogle Scholar
  26. 26.
    Sharon N (1977) Lectins. Sci Am 236:108–119CrossRefPubMedGoogle Scholar
  27. 27.
    Brooks SA, Carter TM, Royle L et al (2008) Altered glycosylation of proteins in cancer: what is the potential for new anti-tumour strategies? Anticancer Agents Med Chem 8:2–21CrossRefPubMedGoogle Scholar
  28. 28.
    Varki A, Cummings R, Esko J et al (1999) Essentials of glycobiology. Cold Spring Harbour Laboratory Press, New YorkGoogle Scholar
  29. 29.
    Brooks SA, Dwek MV, Schumacher U (2002) Functional and molecular glycobiology. Bios Scientific Publishers Ltd, OxfordGoogle Scholar
  30. 30.
    Brooks SA, Leathem AJC (1995) Expression of GalNAc glycoproteins by breast cancers. BJC 71:1033–1038CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Brooks SA (2000) The involvement of Helix pomatia lectin (HPA) binding N-acetylgalactosamine glycans in cancer progression. Histol Histopathol 15:143–158PubMedGoogle Scholar
  32. 32.
    Springer GF, Desai PR, Tegtmeyer H et al (1994) T/Tn antigen vaccine is effective and safe in preventing recurrence of advanced human breast carcinoma. Cancer Biother 9:5–15CrossRefGoogle Scholar
  33. 33.
    Lo-Man R, Vichier-Guerre S, Bay S et al (2001) Anti-tumor immunity provided by a synthetic multiple antigenic glycopeptide displaying tri-Tn glycotope. J Immunol 166:2849–2854CrossRefPubMedGoogle Scholar
  34. 34.
    Hanisch FG, Baldus SE (1997) The Thompsen-Friedenreich (TF) antigen: A critical review on the structural, biosynthetic and histochemical aspects of a pancarcinoma-associated antigen. Histol Histopathol 12:263–281PubMedGoogle Scholar
  35. 35.
    Fernandes B, Sagman U, Auger M et al (1991) Beta 1–6 branched oligosaccharides as a marker of tumour progression in human breast and colon neoplasia. Cancer Res 51:718–723PubMedGoogle Scholar
  36. 36.
    Dennis JW, Laferte S, Waghorne C et al (1987) Beta 1–6 branching of Asn-linked oligosaccharides is directly associated with metastasis. Science 236:582–585CrossRefPubMedGoogle Scholar
  37. 37.
    Yousefi S, Higgins E, Daoling Z et al (1991) Increased UDP-GlcNAc:Gal beta 1–3 GalNAc-R (GlcNAc to GalNAc) beta 1–6 N-acetylglucosaminyltransferase activity in metastatic murine tumor cell lines. Control of polylactosamine synthesis. J Biol Chem 266:1772–1782PubMedGoogle Scholar
  38. 38.
    Goss PE, Cl R, Bailey D et al (1997) Phase I clinical trial of the oligosaccharide processing inhibitor swainsonine in patients with advanced malignancies. Clin Cancer Res 3:1077–1086PubMedGoogle Scholar
  39. 39.
    Brooks SA, Leathem AJC, Schumacher U (1997) Lectin histochemistry, a concise practical handbook. Royal Microscopical Society handbook series number 36. Bios Scientific Publishers Ltd, OxfordGoogle Scholar
  40. 40.
    Laine RA (1997) The information-storing potential of the sugar code. In: Gabius H-J, Gabius S (eds) Glycosciences: status and perspectives. Chapman and Hall, London, pp 1–4Google Scholar
  41. 41.
    Gabius H-J, Kayser K (2014) Introduction to glycopathology : the concept, the tools and the perspectives. Diagn Pathol 9:4CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Hu D, Tateno H, Hirabayashi J (2015) Lectin engineering, a molecular evolutionary approach to expanding lectin utilities. Molecules 20:7637–7656CrossRefPubMedGoogle Scholar
  43. 43.
    Markiv A, Peiris D, Curley GP et al (2001) Identification, cloning, and characterization of two N-acetylgalactosamine-binding lectins from the albumen gland of Helix pomatia. J Biol Chem 286:20260–20266CrossRefGoogle Scholar
  44. 44.
    Adamczyk B, Tharmalingam T, Rudd PM (2012) Glycans as cancer biomarkers. Biochim Biophys Acta 1820:1347–1353CrossRefPubMedGoogle Scholar
  45. 45.
    Tateno H, Uchiyama N, Kuno A et al (2007) A novel strategy for mammalian cell surface glcome profiling using lectin microarray. Glycobiology 17:1138–1146CrossRefPubMedGoogle Scholar
  46. 46.
    Pilobello K, Slawek DE, Mahal LK (2007) A ratiometric lectin microarray approach to analysis of the dynamic mammalian glycome. Proc Natl Acad Sci USA 104:11534–11539CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Hsu K-L, Pilobello KT, Mahal LK (2007) Analysing the dynamic bacterial glycome with a lectin microarray approach. Nat Chem Biol 2:153–157CrossRefGoogle Scholar
  48. 48.
    Schumacher U, Adam E, Brooks SA et al (1995) Lectin binding properties of human breast cancer cell lines and human milk with particular reference to Helix pomatia agglutinin. J Histochem Cytochem 43:275–281CrossRefPubMedGoogle Scholar
  49. 49.
    Dwek MV, Lacey HA, Streets AJ et al (2001) Helix pomatia agglutinin lectin-binding oligosaccharides of aggressive breast cancer. Int J Cancer 95:79–85CrossRefPubMedGoogle Scholar
  50. 50.
    Peiris D, Ossondo M, Fry S et al (2015) Identification of O-linked glycoproteins binding to the lectin Helix pomatia agglutinin as markers of metastatic colorectal cancer. PLoS One 10(10), e0138345. doi: 10.1371/journal.pone.0138345 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Gabius H-J, Schroter C, Gabius S et al (1990) Binding of T-antigen bearing neoglycoprotein and peanut agglutinin to cultured tumour cells and breast carcinomas. J Histochem Cytochem 38:1625–1631CrossRefPubMedGoogle Scholar
  52. 52.
    Habermann FA, Andre S, Kaltner H et al (2011) Galectins as tools for glycan mapping in histology: comparison of their binding profiles to bovine zona pellucida by confocal scanning electron microscopy. Histochem Cell Biol 135:539–552CrossRefPubMedGoogle Scholar
  53. 53.
    Johnson QR, Lindsay RJ, Petridis L et al (2015) Investigation of carbohydrate recognition via computer simulation. Molecules 20:7700–7718CrossRefPubMedGoogle Scholar
  54. 54.
    Park S, Lee MR, Pyo SJ et al (2004) Carbohydrate chips for studying high-throughput carbohydrate-protein interactions. J Am Chem Soc 126:4812–4819CrossRefPubMedGoogle Scholar
  55. 55.
    Fukui S, Feizi T, Galustian C et al (2002) Oligosaccharide microarrays for high throughput detection and specificity assignments of carbohydrate-protein interactions. Nat Biotechnol 20:1011–1107CrossRefPubMedGoogle Scholar
  56. 56.
    Jelinek R, Kolusheva S (2004) Carbohydrate biosensors. Chem Rev 104:5987–6015CrossRefPubMedGoogle Scholar
  57. 57.
    Zhang X, Yadavalli VK (2009) Functionalized self-assembled monolayers for measuring single molecule lectin carbohydrate interactions. Anal Chim Acta 649:1–7CrossRefPubMedGoogle Scholar
  58. 58.
    Yan C, Yersin A, Afrin R et al (2009) Single molecular dynamic interactions between glycophorin A and lectin as probed by atomic force microscopy. Biophys Chem 144:72–77CrossRefPubMedGoogle Scholar
  59. 59.
    Gour N, Verma S (2008) Synthesis and AFM studies of lectin-carbohydrate self-assemblies. Tetrahedron 64:7331–7337CrossRefGoogle Scholar
  60. 60.
    Stubke K, Wicklein D, Herich L et al (2012) Selectin-deficiency reduces the number of spontaneous metastases in a xenograft model of human breast cancer. Cancer Lett 321:89–99CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media LLC 2017

Authors and Affiliations

  1. 1.Department of Biological & Medical SciencesOxford Brookes UniversityHeadington, OxfordUK

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