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Galectins in parasite infection and allergic inflammation

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Abstract

Galectins are increasingly recognised as important immunological mediators of homeostasis and disease regulation. This paper gives an overview of current knowledge of galectin involvement in parasite infection and allergic inflammation, two very different but immunologically linked phenomena. Galectins are produced by both the parasite and the host and appear to be intimately involved in parasite establishment, as well as directing the course of infection and the immune response. Host galectins have also been shown to be active participants in the recruitment of cells to sites of inflammation and modulating the effector function of mast cells, neutrophils and eosinophils. Moreover, the ability of galectins to induce differential expression of cytokine genes in leukocytes suggests that they are able to direct the nature of an adaptive immune response, in particular towards a T2-type allergic response. Published in 2004.

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References

  1. Mosmann TR, Sad S, The expanding universe of T-cell subsets: Th1, Th2 and more, Immunol Today 17, 138-46 (1996).

    Google Scholar 

  2. Costa JJ, Weller PF, Galli SJ, The cells of the allergic response: Mast cells, basophils, and eosinophils, Jama 278, 1815-22 (1997).

    Google Scholar 

  3. Balic A, Bowles VM, Meeusen EN, The immunobiology of gastrointestinal nematode infections in ruminants, Adv Parasitol 45, 181-241 (2000).

    Google Scholar 

  4. Yazdanbakhsh M, Kremsner PG, van Ree R, Allergy, parasites, and the hygiene hypothesis, Science 296, 490-4 (2002).

    Google Scholar 

  5. Klion AD, Donelson JE, OvGal BP, a filarial antigen with homology to vertebrate galactoside-binding proteins, Mol Biochem Parasitol 65, 305-15 (1994).

    Google Scholar 

  6. Newton SE, Monti JR, Greenhalgh CJ, Ashman K, Meeusen EN, cDNA cloning of galectins from third stage larvae of the parasitic nematode Teladorsagia circumcincta, Mol Biochem Parasitol 86, 143-53 (1997).

    Google Scholar 

  7. Greenhalgh CJ, Beckham SA, Newton SE, Galectins from sheep gastrointestinal nematode parasites are highly conserved, Mol Biochem Parasitol 98, 285-9 (1999).

    Google Scholar 

  8. Hirabayashi J, Ubukata T, Kasai K, Purification and molecular characterization of a novel 16-kDa galectin from the nematode Caenorhabditis elegans, J Biol Chem 271, 2497-505 (1996).

    Google Scholar 

  9. Arata Y, Akimoto Y, Hirabayashi J, Kasai K, Hirano H, An immunohistochemical study of the 32-kDa galectin (betagalactoside-binding lectin) in the nematode Caenorhabditis elegans, Histochem J 28, 201-7 (1996).

    Google Scholar 

  10. Dodd RB, Drickamer K, Lectin-like proteins in model organisms: Implications for evolution of carbohydrate-binding activity, Glycobiology 11, 71R-9R (2001).

    Google Scholar 

  11. Fradin C, Poulain D, Jouault T, beta-1,2-linked oligomannosides from Candida albicans bind to a 32-kilodalton macrophage membrane protein homologous to the mammalian lectin galectin-3, Infect Immun 68, 4391-8 (2000).

    Google Scholar 

  12. Pelletier I, Hashidate T, Urashima T, Nishi N, Nakamura T, Futai M, Arata Y, Kasai K, Hirashima M, Hirabayashi J, Sato S, Specific recognition of Leishmania major poly-beta-galactosyl epitopes by galectin-9: Possible implication of galectin-9 in interaction between L. major and host cells, J Biol Chem 278, 22223-30 (2003).

    Google Scholar 

  13. Pelletier I, Sato S, Specific recognition and cleavage of galectin-3 by Leishmania major through species-specific polygalactose epitope, J Biol Chem 277, 17663-70 (2002).

    Google Scholar 

  14. Auriault C, Ouaissi MA, Torpier G, Eisen H, Capron A, Proteolytic cleavage of IgG bound to the Fc receptor of Schistosoma mansoni schistosomula, Parasite Immunol 3, 33-44 (1981).

    Google Scholar 

  15. Moody TN, Ochieng J, Villalta F, Novel mechanism that Trypanosoma cruzi uses to adhere to the extracellular matrix mediated by human galectin-3, FEBS Lett 470, 305-8 (2000).

    Google Scholar 

  16. Giordanengo L, Gea S, Barbieri G, Rabinovich GA, Anti-galectin-1 autoantibodies in human Trypanosoma cruzi infection: Differential expression of this beta-galactoside-binding protein in cardiac Chagas' disease, Clin Exp Immunol 124, 266-73 (2001).

    Google Scholar 

  17. Chung CD, Patel VP, Moran M, Lewis LA, Carrie Miceli M, Galectin-1 induces partial TCR zeta-chain phosphorylation and antagonizes processive TCR signal transduction, J Immunol 165, 3722-9 (2000).

    Google Scholar 

  18. Zuniga E, Rabinovich GA, Iglesias MM, Gruppi A, Regulated expression of galectin-1 during B-cell activation and implications for T-cell apoptosis, J Leukoc Biol 70, 73-9 (2001).

    Google Scholar 

  19. Zuniga E, Gruppi A, Hirabayashi J, Kasai KI, Rabinovich GA, Regulated expression and effect of galectin-1 on Trypanosoma cruz-infected macrophages: Modulation of microbicidal activity and survival, Infect Immun 69, 6804-12 (2001).

    Google Scholar 

  20. Dunphy JL, Balic A, Barcham GJ, Horvath AJ, Nash AD, Meeusen EN, Isolation and characterization of a novel inducible mammalian Galectin, J Biol Chem 275, 32106-13 (2000).

    Google Scholar 

  21. Meeusen EN, Balic A, Do eosinophils have a role in the killing of helminth parasites?, Parasitol Today 16, 95-101 (2000).

    Google Scholar 

  22. Nawa Y, Ishikawa N, Tsuchiya K, Horii Y, Abe T, Khan AI, Bing S, Itoh H, Ide H, Uchiyama F, Selective effector mechanisms for the expulsion of intestinal helminthes, Parasite Immunol 16, 333-8 (1994).

    Google Scholar 

  23. Harrison GB, Pulford HD, Gatehouse TK, Shaw RJ, Pfeffer A, Shoemaker CB, Studies on the role of mucus and mucosal hypersensitivity reactions during rejection of Trichostrongylus colubriformis from the intestine of immune sheep using an experimental challenge model, Int J Parasitol 29, 459-68 (1999).

    Google Scholar 

  24. Wasano K, Hirakawa Y, Recombinant galectin-1 recognizes mucin and epithelial cell surface glycocalyces of gastrointestinal tract, J Histochem Cytochem 45, 275-83 (1997).

    Google Scholar 

  25. Foster PS, Mould AW, Yang M, Mackenzie J, Mattes J, Hogan SP, Mahalingam S, McKenzie AN, Rothenberg ME, Young IG, Matthaei KI, Webb DC, Elemental signals regulating eosinophil accumulation in the lung, Immunol Rev 179, 173-81 (2001).

    Google Scholar 

  26. Weller PF, Eosinophils: Structure and functions, Curr Opin Immunol 6, 85-90 (1994).

    Google Scholar 

  27. Truong MJ, Gruart V, Liu FT, Prin L, Capron A, Capron M, IgE-binding molecules (Mac-2/epsilon BP) expressed by human eosinophils. Implication in IgE-dependent eosinophil cytotoxicity, Eur J Immunol 23, 3230-5 (1993).

    Google Scholar 

  28. Leonidas DD, Elbert BL, Zhou Z, Leffler H, Ackerman SJ, Acharya KR, Crystal structure of human Charcot-Leyden crystal protein, an eosinophil lysophospholipase, identifies it as a new member of the carbohydrate-binding family of galectins, Structure 3, 1379-93 (1995).

    Google Scholar 

  29. Dunphy JL, Barcham GJ, Bischof RJ, Young AR, Nash A, Meeusen EN, Isolation and characterization of a novel eosinophilspecific galectin released into the lungs in response to allergen challenge, J Biol Chem 277, 14916-24 (2002).

    Google Scholar 

  30. Matsumoto R, Matsumoto H, Seki M, Hata M, Asano Y, Kanegasaki S, Stevens RL, Hirashima M, Human ecalectin, a variant of human galectin-9, is a novel eosinophil chemoattractant produced by T lymphocytes, J Biol Chem 273, 16976-84 (1998).

    Google Scholar 

  31. Ackerman SJ, Weil GJ, Gleich GJ, Formation of Charcot-Leyden crystals by human basophils, J Exp Med 155, 1597-609 (1982).

    Google Scholar 

  32. Giembycz MA, Lindsay MA, Pharmacology of the eosinophil, Pharmacol Rev 51, 213-340 (1999).

    Google Scholar 

  33. Dyer KD, Rosenberg HF, Eosinophil Charcot-Leyden crystal protein binds to beta-galactoside sugars, Life Sci 58, 2073-82 (1996).

    Google Scholar 

  34. Ackerman SJ, Liu L, Kwatia MA, Savage MP, Leonidas DD, Swaminathan GJ, Acharya KR, Charcot-Leyden crystal protein (galectin-10) is not a dual-function galectin with lysophospholipase activity, but binds a lysophospholipase inhibitor in a novel structural fashion, J Biol Chem 7, 7 (2002).

    Google Scholar 

  35. Gleich GJ, Adolphson CR, Leiferman KM, Eosinophils. In Inflammation: Basic principles and clinical correlates, edited by Gallin JI, Goldstein IM and Snyderman R (Raven Press, Ltd., New York, 1992), pp. 663-700.

    Google Scholar 

  36. Janeway CA, Travers P, Walport M, Capra JD, Immunobiology: The immune system in health and disease (Current Biology Publications, London, 1999).

    Google Scholar 

  37. Frigeri LG, Zuberi RI, Liu FT, Epsilon BP, a beta-galactosidebinding animal lectin, recognizes IgE receptor (Fc epsilon RI) and activates mast cells, Biochemistry 32, 7644-9 (1993).

    Google Scholar 

  38. Liu FT, Albrandt K, Mendel E, Kulczycki A, Jr., Orida NK, Identi-fication of an IgE-binding protein by molecular cloning, Proc Natl Acad Sci U S A 82, 4100-4 (1985).

    Google Scholar 

  39. Cherayil BJ, Weiner SJ, Pillai S, The Mac-2 antigen is a galactosespecific lectin that binds IgE, J Exp Med 170, 1959-72 (1989).

    Google Scholar 

  40. Liu FT, S-type mammalian lectins in allergic inflammation, Immunol Today 14, 486-90 (1993).

    Google Scholar 

  41. Frigeri LG, Liu FT, Surface expression of functional IgE binding protein, an endogenous lectin, on mast cells and macrophages, J Immunol 148, 861-7 (1992).

    Google Scholar 

  42. Matsumoto R, Hirashima M, Kita H, Gleich GJ, Biological activities of ecalectin: A novel eosinophil-activating factor, J Immunol 168, 1961-7 (2002).

    Google Scholar 

  43. Woo HJ, Shaw LM, Messier JM, Mercurio AM, The major nonintegrin laminin binding protein of macrophages is identical to carbohydrate binding protein 35 (Mac-2), J Biol Chem 265, 7097-9 (1990).

    Google Scholar 

  44. Sato S, Hughes RC, 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, 6983-90 (1992).

    Google Scholar 

  45. Massa SM, Cooper DN, Leffler H, Barondes SH, L-29, an endogenous lectin, binds to glycoconjugate ligands with positive cooperativity, Biochemistry 32, 260-7 (1993).

    Google Scholar 

  46. Zhou Q, Cummings RD, L-14 lectin recognition of laminin and its promotion of in vitro cell adhesion, Arch Biochem Biophys 300, 6-17 (1993).

    Google Scholar 

  47. Ozeki Y, Matsui T, Yamamoto Y, Funahashi M, Hamako J, Titani K, Tissue fibronectin is an endogenous ligand for galectin-1, Glycobiology 5, 255-61 (1995).

    Google Scholar 

  48. Levy Y, Arbel-Goren R, Hadari YR, Eshhar S, Ronen D, Elhanany E, Geiger B, Zick Y, Galectin-8 functions as a matricellular modulator of cell adhesion, J Biol Chem 276, 31285-95 (2001).

    Google Scholar 

  49. Hughes RC, Galectins as modulators of cell adhesion, Biochimie 83, 667-76 (2001).

    Google Scholar 

  50. Sato S, Ouellet N, Pelletier I, Simard M, Rancourt A, Bergeron MG, Role of galectin-3 as an adhesion molecule for neutrophil extravasation during streptococcal pneumonia, J Immunol 168, 1813-22 (2002).

    Google Scholar 

  51. Colnot C, Ripoche MA, Milon G, Montagutelli X, Crocker PR, Poirier F, Maintenance of granulocyte numbers during acute peritonitis is defective in galectin-3-null mutant mice, Immunology 94, 290-6 (1998).

    Google Scholar 

  52. Hsu DK, Yang RY, Pan Z, Yu L, Salomon DR, Fung-Leung WP, Liu FT, Targeted disruption of the galectin-3 gene results in attenuated peritoneal inflammatory responses,AmJ Pathol 156, 1073-83 (2000).

    Google Scholar 

  53. Metzger H, Alcaraz G, Hohman R, Kinet JP, Pribluda V, Quarto R, The receptor with high affinity for immunoglobulin E, Annu Rev Immunol 4, 419-70 (1986).

    Google Scholar 

  54. Gounni AS, Lamkhioued B, Ochiai K, Tanaka Y, Delaporte E, Capron A, Kinet JP, Capron M, High-affinity IgE receptor on eosinophils is involved in defence against parasites, Nature 367, 183-6 (1994).

    Google Scholar 

  55. Kita H, Kaneko M, Bartemes KR, Weiler DA, Schimming AW, Reed CE, Gleich GJ, Does IgE bind to and activate eosinophils from patients with allergy?, J Immunol 162, 6901-11 (1999).

    Google Scholar 

  56. Truong MJ, Gruart V, Kusnierz JP, Papin JP, Loiseau S, Capron A, Capron M, Human neutrophils express immunoglobulin E (IgE)-binding proteins (Mac-2/epsilon BP) of the S-type lectin family: Role in IgE-dependent activation, J Exp Med 177, 243-8 (1993).

    Google Scholar 

  57. Yamaoka A, Kuwabara I, Frigeri LG, Liu FT, A human lectin, galectin-3 (epsilon bp/Mac-2), stimulates superoxide production by neutrophils, J Immunol 154, 3479-87 (1995).

    Google Scholar 

  58. Liu FT, Hsu DK, Zuberi RI, Kuwabara I, Chi EY, Henderson WR, Jr., Expression and function of galectin-3, a beta-galactosidebinding lectin, in human monocytes and macrophages,AmJ Pathol 147, 1016-28 (1995).

    Google Scholar 

  59. Dor PJ, Ackerman SJ, Gleich GJ, Charcot-Leyden crystal protein and eosinophil granule major basic protein in sputum of patients with respiratory diseases, Am Rev Respir Dis 130, 1072-7 (1984).

    Google Scholar 

  60. Cortegano I, del Pozo V, Cardaba B, de Andres B, Gallardo S, del Amo A, Arrieta I, Jurado A, Palomino P, Liu FT and Lahoz C, Galectin-3 down-regulates IL-5 gene expression on different cell types, J Immunol 161, 385-9 (1998).

    Google Scholar 

  61. Foster PS, Hogan SP, Yang M, Mattes J, Young IG, Matthaei KI, Kumar RK, Mahalingam S, Webb DC, Interleukin-5 and eosinophils as therapeutic targets for asthma, Trends Mol Med 8, 162-7 (2002).

    Google Scholar 

  62. Vasta GR, Quesenberry M, Ahmed H, O'Leary N, C-type lectins and galectins mediate innate and adaptive immune functions: Their roles in the complement activation pathway, Dev Comp Immunol 23, 401-20 (1999).

    Google Scholar 

  63. Dell A, Haslam SM, Morris HR, Khoo KH, Immunogenic glycoconjugates implicated in parasitic nematode diseases, Biochim Biophys Acta 1455, 353–62 (1999).

    Google Scholar 

  64. Cummings RD, Nyame AK, Schistosome glycoconjugates, Biochim Biophys Acta 1455, 363-74 (1999).

    Google Scholar 

  65. Offner H, Celnik B, Bringman TS, Casentini-Borocz D, Nedwin GE, Vandenbark AA, Recombinant human beta-galactoside binding lectin suppresses clinical and histological signs of experimental autoimmune encephalomyelitis, J Neuroimmunol 28, 177-84 (1990).

    Google Scholar 

  66. Rabinovich GA, Daly G, Dreja H, Tailor H, Riera CM, Hirabayashi J, Chernajovsky Y, Recombinant galectin-1 and its genetic delivery suppress collagen-induced arthritis via T cell apoptosis, J Exp Med 190, 385-98 (1999).

    Google Scholar 

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Young, A.R., Meeusen, E.N. Galectins in parasite infection and allergic inflammation. Glycoconj J 19, 601–606 (2002). https://doi.org/10.1023/B:GLYC.0000014091.00844.0a

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