The effect of carbohydrate moiety structure on the immunoregulatory activity of lactoferrin in vitro

• Autorzy: Zimecki M. , Artym J. , Kocieba M. , Duk M. , Kruzel M. L.
• Języki publikacji: EN

Abstrakty

EN

The aim of this study was to evaluate the immunoregulatory effects of recombinant human lactoferrin (rhLF) in two in vitro models: (1) the secondary humoral immune response to sheep erythrocytes (SRBC); and (2) the mixed lymphocyte reaction (MLR). We compared the non-sialylated glycoform of rhLF as expressed by glycoengineered Pichia pastoris with one that was further chemically sialylated. In an earlier study, we showed that sialylated rhLF could reverse methotrexate-induced suppression of the secondary immune response of mouse splenocytes to SRBC, and that the phenomenon is dependent on the interaction of lactoferrin (LF) with sialoadhesin (CD169). We found that the immunorestorative activity of sialylated rhLF is also dependent on its interaction with the CD22 antigen, a member of the immunoglobulin superfamily that is expressed by B lymphocytes. We also demonstrated that only sialylated rhLF was able to inhibit the MLR reaction. MLR was inhibited by bovine lactoferrin (bLF), a glycoform that has a more complex glycan structure. Desialylated bLF and lactoferricin, a bLF-derived peptide devoid of carbohydrates, did not express such inhibitory activity. We showed that the interaction of LF with sialic acid receptors is essential for at least some of the immunoregulatory activity of this glycoprotein.

Słowa kluczowe

EN

carbohydrate; immunoregulatory activity; lactoferrin; in vitro; human recombinant lactoferrin; sialic acid; humoral immune response; mixed lymphocyte reaction; glycoprotein; immune suppression

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2014
• Tom: 19
• Numer: 2
• Opis fizyczny: p.284-296,fig.,ref.

Twórcy

autor

Zimecki M.

• Department of Experimental Therapy, Institute of Immunology and Experimental Therapy, Weigla 12, 53-114 Wroclaw, Poland

autor

Artym J.

• Department of Experimental Therapy, Institute of Immunology and Experimental Therapy, Weigla 12, 53-114 Wroclaw, Poland

autor

Kocieba M.

• Department of Experimental Therapy, Institute of Immunology and Experimental Therapy, Weigla 12, 53-114 Wroclaw, Poland

autor

Duk M.

• Department of Immunochemistry, Institute of Immunology and Experimental Therapy, Weigla 12, 53-114 Wroclaw

autor

Kruzel M. L.

• Health Science Center, University of Texas, Houston, Texas, USA

Bibliografia

• 1. Legrand, D., Pierce, A., Elass, E., Carpentier, M., Mariller, C. and Mazurier, J. Lactoferrin structure and functions. Adv. Exp. Med. Biol. 606 (2008) 163–194.
• 2. Vogel, H.J. Lactoferrin, a bird's eye view. Biochem. Cell Biol. 90 (2012) 233–244.
• 3. Kruzel, M.L., Actor, J.K., Boldogh, I. and Zimecki, M. Lactoferrin in health and disease. Postepy Hig. Med. Dosw. 61 (2007) 261–267.
• 4. Kruzel, M.L., Actor, J.K., Radak, Z., Bacsi, A., Saavedra-Molina, A. and Boldogh, I. Lactoferrin decreases LPS-induced mitochondrial dysfunction in cultured cells and in animal endotoxemia model. Innate Immun. 16 (2010) 67–79.
• 5. Jonasch, E., Stadler, W.M., Bukowski, R.M., Hayes, T.G., Varadhachary, A., Malik, R., Figlin, R.A. and Srinivas, S. Phase 2 trial of talactoferrin in previously treated patients with metastatic renal cell carcinoma. Cancer 113 (2008) 72–77.
• 6. Baldi, A., Ioannis, P., Chiara, P., Eleonora, F., Roubini, C. and Vittorio, D. Biological effects of milk proteins and their peptides with emphasis on those related to the gastrointestinal ecosystem. J. Dairy Res. 72 (2005) 66–72.
• 7. Weinberg, E.D. Iron, infection, and neoplasia. Clin. Physiol. Biochem. 4 (1986) 50–60.
• 8. Hendrixson, D.R., Qiu, J., Shewry, S.C., Fink, D.L., Petty, S., Baker, E.N., Plaut, A.G. and St Geme, J.W., 3rd. Human milk lactoferrin is a serine protease that cleaves Haemophilus surface proteins at arginine-rich sites. Mol. Microbiol. 47 (2003) 607–617.
• 9. Appelmelk, B.J., An, Y.Q., Geerts, M., Thijs, B.G., de Boer, H.A., MacLaren, D.M., de Graaff, J. and Nuijens, J.H. Lactoferrin is a lipid A-binding protein. Infect. Immun. 62 (1994) 2628–2632.
• 10. Zimecki, M., Mazurier, J., Machnicki, M., Wieczorek, Z., Montreuil, J. and Spik, G. Immunostimulatory activity of lactotransferrin and maturation of CD4- CD8- murine thymocytes. Immunol. Lett. 30 (1991) 119–123.
• 11. Zimecki, M., Mazurier, J., Spik, G. and Kapp, J.A. Human lactoferrin induces phenotypic and functional changes in murine splenic B cells. Immunology 86 (1995) 122–127.
• 12. Artym, J. and Zimecki, M. The effects of lactoferrin on myelopoiesis: can we resolve the controversy? Postepy Hig. Med. Dosw. 61 (2007) 129–150.
• 13. Legrand, D., Elass, E., Carpentier, M. and Mazurier, J. Interactions of lactoferrin with cells involved in immune function. Biochem. Cell Biol. 84 (2006) 282–290.
• 14. Fischer, R., Debbabi, H., Dubarry, M., Boyaka, P. and Tome, D. Regulation of physiological and pathological Th1 and Th2 responses by lactoferrin. Biochem. Cell Biol. 84 (2006) 303–311.
• 15. Zimecki, M., Stepniak, D., Szynol, A. and Kruzel, M.L. Lactoferrin regulates proliferative response of human peripheral blood mononuclear cells to phytohemagglutinin and mixed lymphocyte reaction. Arch. Immunol. Ther. Exp. (Warsz.). 49 (2001) 147–154.
• 16. Suzuki, Y.A., Lopez, V. and Lonnerdal, B. Mammalian lactoferrin receptors: structure and function. Cell. Mol. Life Sci. 62 (2005) 2560–2575.
• 17. Curran, C.S., Demick, K.P. and Mansfield, J.M. Lactoferrin activates macrophages via TLR4-dependent and -independent signaling pathways. Cell. Immunol. 242 (2006) 23–30.
• 18. Ando, K., Hasegawa, K., Shindo, K., Furusawa, T., Fujino, T., Kikugawa, K., Nakano, H., Takeuchi, O., Akira, S., Akiyama, T., Gohda, J., Inoue, J. and Hayakawa, M. Human lactoferrin activates NF-kappaB through the Toll-like receptor 4 pathway while it interferes with the lipopolysaccharide-stimulated TLR4 signaling. FEBS J. 277 (2010) 2051–2066.
• 19. Chien, Y.J., Chen, W.J., Hsu, W.L. and Chiou, S.S. Bovine lactoferrin inhibits Japanese encephalitis virus by binding to heparan sulfate and receptor for low density lipoprotein. Virology 379 (2008) 143–151.
• 20. van Berkel, P.H., Geerts, M.E., van Veen, H.A., Mericskay, M., de Boer, H.A. and Nuijens, J.H. N-terminal stretch Arg2, Arg3, Arg4 and Arg5 of human lactoferrin is essential for binding to heparin, bacterial lipopolysaccharide, human lysozyme and DNA. Biochem. J. 328 ( Pt 1) (1997) 145–151.
• 21. Elass-Rochard, E., Legrand, D., Salmon, V., Roseanu, A., Trif, M., Tobias, P.S., Mazurier, J. and Spik, G. Lactoferrin inhibits the endotoxin interaction with CD14 by competition with the lipopolysaccharide-binding protein. Infect. Immun. 66 (1998) 486–491.
• 22. Legrand, D., Vigie, K., Said, E.A., Elass, E., Masson, M., Slomianny, M.C., Carpentier, M., Briand, J.P., Mazurier, J. and Hovanessian, A.G. Surface nucleolin participates in both the binding and endocytosis of lactoferrin in target cells. Eur. J. Biochem. 271 (2004) 303–317.
• 23. Shin, K., Wakabayashi, H., Yamauchi, K., Yaeshima, T. and Iwatsuki, K. Recombinant human intelectin binds bovine lactoferrin and its peptides. Biol. Pharm. Bull. 31 (2008) 1605–1608.
• 24. Kerrigan, A.M. and Brown, G.D. C-type lectins and phagocytosis. Immunobiology 214 (2009) 562–575.
• 25. Paulson, J.C., Macauley, M.S. and Kawasaki, N. Siglecs as sensors of self in innate and adaptive immune responses. Ann. N.Y. Acad. Sci. 1253 (2012) 37–48.
• 26. Kocieba, M., Zimecki, M., Kruzel, M. and Actor, J. The adjuvant activity of lactoferrin in the generation of DTH to ovalbumin can be inhibited by bovine serum albumin bearing alpha-D-mannopyranosyl residues. Cell. Mol. Biol. Lett. 7 (2002) 1131–1136.
• 27. Groot, F., Geijtenbeek, T.B., Sanders, R.W., Baldwin, C.E., SanchezHernandez, M., Floris, R., van Kooyk, Y., de Jong, E.C. and Berkhout, B. Lactoferrin prevents dendritic cell-mediated human immunodeficiency virus type 1 transmission by blocking the DC-SIGN-gp120 interaction. J. Virol. 79 (2005) 3009–3015.
• 28. Choi, B.K., Actor, J.K., Rios, S., d'Anjou, M., Stadheim, T.A., Warburton, S., Giaccone, E., Cukan, M., Li, H., Kull, A., Sharkey, N., Gollnick, P., Kocieba, M., Artym, J., Zimecki, M., Kruzel, M.L. and Wildt, S. Recombinant human lactoferrin expressed in glycoengineered Pichia pastoris: effect of terminal N-acetylneuraminic acid on in vitro secondary humoral immune response. Glycoconj. J. 25 (2008) 581–593.
• 29. Baveye, S., Elass, E., Fernig, D.G., Blanquart, C., Mazurier, J. and Legrand, D. Human lactoferrin interacts with soluble CD14 and inhibits expression of endothelial adhesion molecules, E-selectin and ICAM-1, induced by the CD14-lipopolysaccharide complex. Infect. Immun. 68 (2000) 6519–6525.
• 30. Hwang, S.A., Wilk, K., Kruzel, M.L. and Actor, J.K. A novel recombinant human lactoferrin augments the BCG vaccine and protects alveolar integrity upon infection with Mycobacterium tuberculosis in mice. Vaccine 27 (2009) 3026–3034.
• 31. Artym, J., Zimecki, M. and Kruzel, M.L. Effect of lactoferrin on the methotrexate-induced suppression of the cellular and humoral immune response in mice. Anticancer Res. 24 (2004) 3831–3836.
• 32. O'Neill, A.S., van den Berg, T.K. and Mullen, G.E. Sialoadhesin - a macrophage-restricted marker of immunoregulation and inflammation. Immunology 138 (2013) 198–207.
• 33. Sunshine, G.H., Katz, D.R. and Czitrom, A.A. Heterogeneity of stimulator cells in the murine mixed leukocyte response. Eur. J. Immunol. 12 (1982) 9–15.
• 34. Unanue, E.R. Antigen-presenting function of the macrophage. Annu. Rev. Immunol. 2 (1984) 395–428.
• 35. Nitschke, L. CD22 and Siglec-G: B-cell inhibitory receptors with distinct functions. Immunol. Rev. 230 (2009) 128–143.
• 36. Lisowska, E., Duk, M. and Wu, A.M. Preparation of biotinylated lectins and application in microtiter plate assays and Western blotting. In: A Laboratory Guide to Biotin-Labeling in Biomolecule Analysis, BioMethods 7 (1996) 115–129.
• 37. Endo, Y. and Kobata, A. Partial purification and characterization of an endoalpha-N-acetylgalactosaminidase from the culture of medium of Diplococcus pneumoniae. J. Biochem. 80 (1976) 1–8.
• 38. Drzeniek, Z., Krotkiewski, H., Syper, D. and Lisowska, E. Reactivity of glycosidase-treated, blood-group M and N glycopeptides with lectins. Carbohydr. Res. 120 (1983) 315–321.
• 39. Mishell, R.I. and Dutton, R.W. Immunization of dissociated spleen cell cultures from normal mice. J. Exp. Med. 126 (1967) 423–442.
• 40. Hansen, M.B., Nielsen, S.E. and Berg, K. Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J. Immunol. Methods. 119 (1989) 203–210.
• 41. Vogel, H.J., Schibli, D.J., Jing, W., Lohmeier-Vogel, E.M., Epand, R.F. and Epand, R.M. Towards a structure-function analysis of bovine lactoferricin and related tryptophan- and arginine-containing peptides. Biochem. Cell Biol. 80 (2002) 49–63.
• 42. Sato, S., Tuscano, J.M., Inaoki, M. and Tedder, T.F. CD22 negatively and positively regulates signal transduction through the B lymphocyte antigen receptor. Semin. Immunol. 10 (1998) 287–297.
• 43. Rosenthal, G.J., Weigand, G.W., Germolec, D.R., Blank, J.A. and Luster, M.I. Suppression of B cell function by methotrexate and trimetrexate. Evidence for inhibition of purine biosynthesis as a major mechanism of action. J. Immunol. 141 (1988) 410–416.
• 44. Genestier, L., Paillot, R., Fournel, S., Ferraro, C., Miossec, P. and Revillard, J.P. Immunosuppressive properties of methotrexate: apoptosis and clonal deletion of activated peripheral T cells. J. Clin. Invest. 102 (1998) 322–328.
• 45. Danzer, C.P., Collins, B.E., Blixt, O., Paulson, J.C. and Nitschke, L. Transitional and marginal zone B cells have a high proportion of unmasked CD22: implications for BCR signaling. Int. Immunol. 15 (2003) 1137–1147.
• 46. Kawasaki, Y., Sato, K., Shinmoto, H. and Dosako, S. Role of basic residues of human lactoferrin in the interaction with B lymphocytes. Biosci. Biotechnol. Biochem. 64 (2000) 314–318.
• 47. Artym, J., Zimecki, M., Paprocka, M. and Kruzel, M.L. Orally administered lactoferrin restores humoral immune response in immunocompromised mice. Immunol. Lett. 89 (2003) 9–15.
• 48. Actor, J.K., Hwang, S.A., Olsen, M., Zimecki, M., Hunter, R.L., Jr. and Kruzel, M.L. Lactoferrin immunomodulation of DTH response in mice. Int. Immunopharmacol. 2 (2002) 475–486.
• 49. Boswell, H.S., Nerenberg, M.I., Scher, I. and Singer, A. Role of accessory cells in B cell activation. III. Cellular analysis of primary immune response deficits in CBA/N mice: presence of an accessory cell-B cell interaction defect. J. Exp. Med. 152 (1980) 1194–1309.
• 50. Nakae, S., Asano, M., Horai, R. and Iwakura, Y. Interleukin-1 beta, but not interleukin-1 alpha, is required for T-cell-dependent antibody production. Immunology 104 (2001) 402–409.
• 51. Zucali, J.R., Broxmeyer, H.E., Levy, D. and Morse, C. Lactoferrin decreases monocyte-induced fibroblast production of myeloid colony-stimulating activity by suppressing monocyte release of interleukin-1. Blood 74 (1989) 1531–1536.
• 52. Leutwyler, C., Schalch, L. and Jungi, T.W. Evidence for interleukin-1 beta being a necessary but not sufficient co-stimulatory signal in monocytedependent anti-CD3-mediated T-cell triggering. Immunol. Lett. 38 (1993) 33–39.
• 53. Zimecki, M., Kocieba, M. and Kruzel, M. Immunoregulatory activities of lactoferrin in the delayed type hypersensitivity in mice are mediated by a receptor with affinity to mannose. Immunobiology 205 (2002) 120–131.