The Library

High glucose disrupts oligosaccharide recognition function via competitive inhibition : a potential mechanism for immune dysregulation in diabetes mellitus

Tools

Ilyas, Rebecca, Wallis, Russell, Soilleux, Elizabeth J., Townsend, Paul, Zehnder, Daniel, Tan, Bee K., Sim, Robert B., Lehnert, Hendrik, Randeva, Harpal S. and Mitchell, Daniel Anthony. (2011) High glucose disrupts oligosaccharide recognition function via competitive inhibition : a potential mechanism for immune dysregulation in diabetes mellitus. Immunobiology, Vol.216 (No.1-2). pp. 126-131. ISSN 0171-2985

Preview

PDF
WRAP_Mitchell_0483251-ml-230311-imbio_final_version.pdf - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader
Download (167Kb)

Official URL: http://dx.doi.org/10.1016/j.imbio.2010.06.002

Abstract

Diabetic complications include infection and cardiovascular disease. Within the immune system, host-pathogen and regulatory host-host interactions operate through binding of oligosaccharides by C-type lectin. A number of C-type lectins recognise oligosaccharides rich in mannose and fucose – sugars with similar structures to glucose. This raises the possibility that high glucose conditions in diabetes affect protein-oligosaccharide interactions via competitive inhibition. Mannose binding lectin, soluble DC-SIGN & DC-SIGNR, and surfactant protein D, were tested for carbohydrate binding in the presence of glucose concentrations typical of diabetes, via surface plasmon resonance and affinity chromatography. Complement activation assays were performed in high glucose. DC-SIGN and DC-SIGNR expression in adipose tissues was examined via immunohistochemistry. High glucose inhibited C-type lectin binding to high-mannose glycoprotein and binding of DC-SIGN to fucosylated ligand (blood group B) was abrogated in high glucose. Complement activation via the lectin pathway was inhibited in high glucose and also in high trehalose - a nonreducing sugar with glucoside stereochemistry. DC-SIGN staining was seen on cells with DC morphology within omental and subcutaneous adipose tissues. We conclude that high glucose disrupts C-type lectin function, potentially illuminating new perspectives on susceptibility to infectious and inflammatory disease in diabetes. Mechanisms involve competitive inhibition of carbohydrate-binding within sets of defined proteins, in contrast to broadly indiscriminate, irreversible glycation of proteins.

Item Type:

Journal Article

Subjects:

Q Science > QP Physiology

Divisions:

Faculty of Medicine > Warwick Medical School > Translational & Systems Medicine > Metabolic and Vascular Health
Faculty of Medicine > Warwick Medical School

Library of Congress Subject Headings (LCSH):

Diabetes -- Complications, Oligosaccharides, Lectins, Immune response -- Regulation

Journal or Publication Title:

Immunobiology

Publisher:

Elsevier

ISSN:

0171-2985

Official Date:

January 2011

Dates:

Date	Event
January 2011	Published

Volume:

Vol.216

Number:

No.1-2

Page Range:

pp. 126-131

Identification Number:

10.1016/j.imbio.2010.06.002

Status:

Peer Reviewed

Access rights to Published version:

Restricted or Subscription Access

Funder:

University of Warwick, Research Councils UK (RCUK), Wellcome Trust (London, England)

Grant number:

077400 (Wellcome)

References:

1. Ahmed, N., and Thornalley, P. J. 2007. Advanced glycation endproducts: what is their relevance to diabetic complications? Diabetes Obes Metab 9: 233.
2. Weis, W. I., Taylor, M. E., and Drickamer, K. 1998. The C-type lectin superfamily in the immune system. Immunol Rev 163: 19.
3. Turner, M. W. 1996. Mannose-binding lectin: the pluripotent molecule of the innate immune system. Immunol Today 17: 532.
4. Nauta, A. J., Raaschou-Jensen, N., Roos, A., Daha, M. R., Madsen, H. O., Borrias-Essers, M. C., Ryder, L. P., Koch, C., and Garred, P. 2003. Mannose-binding lectin engagement with late apoptotic and necrotic cells. Eur J Immunol 33: 2853.
5. Walport, M. J. 2001. Complement. First of two parts. N Engl J Med 344: 1058.
6. Walport, M. J. 2001. Complement. Second of two parts. N Engl J Med 344: 1140.
7. Ip, W. K., Takahashi, K., Moore, K. J., Stuart, L. M., and Ezekowitz, R. A. 2008. Mannose-binding lectin enhances Toll-like receptors 2 and 6 signaling from the phagosome. J Exp Med 205: 169.
8. Geijtenbeek, T. B., Torensma, R., van Vliet, S. J., van Duijnhoven, G. C., Adema, G. J., van Kooyk, Y., and Figdor, C. G. 2000. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100: 575.
9. Geijtenbeek, T. B., Kwon, D. S., Torensma, R., van Vliet, S. J., van Duijnhoven, G. C., Middel, J., Cornelissen, I. L., Nottet, H. S., KewalRamani, V. N., Littman, D. R., Figdor, C. G., and van Kooyk, Y. 2000. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100: 587.
10. Geijtenbeek, T. B., Krooshoop, D. J., Bleijs, D. A., van Vliet, S. J., van Duijnhoven, G. C., Grabovsky, V., Alon, R., Figdor, C. G., and van Kooyk, Y. 2000. DC-SIGN-ICAM-2 interaction mediates dendritic cell trafficking. Nat Immunol 1: 353.
11. Soilleux, E. J., Barten, R., and Trowsdale, J. 2000. DC-SIGN; a related gene, DC-SIGNR; and CD23 form a cluster on 19p13. J Immunol 165: 2937.
12. Pohlmann, S., Soilleux, E. J., Baribaud, F., Leslie, G. J., Morris, L. S., Trowsdale, J., Lee, B., Coleman, N., and Doms, R. W. 2001. DC-SIGNR, a DC-SIGN homologue expressed in endothelial cells, binds to human and simian immunodeficiency viruses and activates infection in trans. Proc Natl Acad Sci U S A 98: 2670.
13. 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.
14. Feinberg, H., Mitchell, D. A., Drickamer, K., and Weis, W. I. 2001. Structural basis for selective recognition of oligosaccharides by DC-SIGN and DC-SIGNR. Science 294: 2163.
15. Lee, R. T., Ichikawa, Y., Fay, M., Drickamer, K., Shao, M. C., and Lee, Y. C. 1991. Ligand-binding characteristics of rat serum-type mannose-binding protein (MBP-A). Homology of binding site architecture with mammalian and chicken hepatic lectins. J Biol Chem 266: 4810.
16. Mitchell, D. A., Fadden, A. J., and Drickamer, K. 2001. A novel mechanism of carbohydrate recognition by the C-type lectins DC-SIGN and DC-SIGNR.
Subunit organization and binding to multivalent ligands. J Biol Chem 276: 28939.
17. UKPDS. 1990. UK Prospective Diabetes Study 7: response of fasting plasma glucose to diet therapy in newly presenting type II diabetic patients, UKPDS Group. Metabolism 39: 905.
18. Holman, R. R., and Turner, R. C. 1981. The basal plasma glucose: a simple relevant index of maturity-onset diabetes. Clin Endocrinol (Oxf) 14: 279.
19. Turner, R. C., and Holman, R. R. 1995. Lessons from UK prospective diabetes study. Diabetes Res Clin Pract 28 Suppl: S151.
20. Wallis, R., and Drickamer, K. 1997. Asymmetry adjacent to the collagen-like domain in rat liver mannose-binding protein. Biochem J 325 ( Pt 2): 391.
21. Strong, P., Kishore, U., Morgan, C., Lopez Bernal, A., Singh, M., and Reid, K. B. 1998. A novel method of purifying lung surfactant proteins A and D from the lung lavage of alveolar proteinosis patients and from pooled amniotic fluid. J Immunol Methods 220: 139.
22. Seelen, M. A., Roos, A., Wieslander, J., Mollnes, T. E., Sjoholm, A. G., Wurzner, R., Loos, M., Tedesco, F., Sim, R. B., Garred, P., Alexopoulos, E., Turner, M. W., and Daha, M. R. 2005. Functional analysis of the classical, alternative, and MBL pathways of the complement system: standardization and validation of a simple ELISA. J Immunol Methods 296: 187.
23. Guo, Y., Feinberg, H., Conroy, E., Mitchell, D. A., Alvarez, R., Blixt, O., Taylor, M. E., Weis, W. I., and Drickamer, K. 2004. Structural basis for distinct ligand-binding and targeting properties of the receptors DC-SIGN and DC-SIGNR. Nat Struct Mol Biol 11: 591.
24. Paidassi, H., Tacnet-Delorme, P., Lunardi, T., Arlaud, G. J., Thielens, N. M., and Frachet, P. 2008. The lectin-like activity of human C1q and its implication in DNA and apoptotic cell recognition. FEBS Lett 582: 3111.
25. Carlow, D. A., Gold, M. R., and Ziltener, H. J. 2009. Lymphocytes in the peritoneum home to the omentum and are activated by resident dendritic cells. J Immunol 183: 1155.
26. Worthley, D. L., Bardy, P. G., and Mullighan, C. G. 2005. Mannose-binding lectin: biology and clinical implications. Intern Med J 35: 548.
27. Moller-Kristensen, M., Ip, W. K., Shi, L., Gowda, L. D., Hamblin, M. R., Thiel, S., Jensenius, J. C., Ezekowitz, R. A., and Takahashi, K. 2006. Deficiency of mannose-binding lectin greatly increases susceptibility to postburn infection with Pseudomonas aeruginosa. J Immunol 176: 1769.
28. Held, K., Thiel, S., Loos, M., and Petry, F. 2008. Increased susceptibility of complement factor B/C2 double knockout mice and mannan-binding lectin knockout mice to systemic infection with Candida albicans. Mol Immunol 45: 3934.
29. Lillegard, J. B., Sim, R. B., Thorkildson, P., Gates, M. A., and Kozel, T. R. 2006. Recognition of Candida albicans by mannan-binding lectin in vitro and in vivo. J Infect Dis 193: 1589.
30. Stuart, L. M., Takahashi, K., Shi, L., Savill, J., and Ezekowitz, R. A. 2005. Mannose-binding lectin-deficient mice display defective apoptotic cell clearance but no autoimmune phenotype. J Immunol 174: 3220.
31. Savill, J., and Fadok, V. 2000. Corpse clearance defines the meaning of cell death. Nature 407: 784.
32. Botto, M., Dell'Agnola, C., Bygrave, A. E., Thompson, E. M., Cook, H. T., Petry, F., Loos, M., Pandolfi, P. P., and Walport, M. J. 1998. Homozygous
C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet 19: 56.
33. Fernandez-Real, J. M., Straczkowski, M., Vendrell, J., Soriguer, F., Perez Del Pulgar, S., Gallart, L., Lopez-Bermejo, A., Kowalska, I., Manco, M., Cardona, F., Garcia-Gil, M. M., Mingrone, G., Richart, C., Ricart, W., and Zorzano, A. 2006. Protection from inflammatory disease in insulin resistance: the role of mannan-binding lectin. Diabetologia 49: 2402.
34. Reading, P. C., Allison, J., Crouch, E. C., and Anders, E. M. 1998. Increased susceptibility of diabetic mice to influenza virus infection: compromise of collectin-mediated host defense of the lung by glucose? J Virol 72: 6884.
35. Zeyda, M., Farmer, D., Todoric, J., Aszmann, O., Speiser, M., Gyori, G., Zlabinger, G. J., and Stulnig, T. M. 2007. Human adipose tissue macrophages are of an anti-inflammatory phenotype but capable of excessive pro-inflammatory mediator production. Int J Obes (Lond) 31: 1420.
36. Permana, P. A., Menge, C., and Reaven, P. D. 2006. Macrophage-secreted factors induce adipocyte inflammation and insulin resistance. Biochem Biophys Res Commun 341: 507.
37. Devaraj, S., Dasu, M. R., Rockwood, J., Winter, W., Griffen, S. C., and Jialal, I. 2008. Increased toll-like receptor (TLR) 2 and TLR4 expression in monocytes from patients with type 1 diabetes: further evidence of a proinflammatory state. J Clin Endocrinol Metab 93: 578.
38. Ghanim, H., Mohanty, P., Deopurkar, R., Sia, C. L., Korzeniewski, K., Abuaysheh, S., Chaudhuri, A., and Dandona, P. 2008. Acute modulation of toll-like receptors by insulin. Diabetes Care 31: 1827.
39. Krutzik, S. R., Tan, B., Li, H., Ochoa, M. T., Liu, P. T., Sharfstein, S. E., Graeber, T. G., Sieling, P. A., Liu, Y. J., Rea, T. H., Bloom, B. R., and Modlin, R. L. 2005. TLR activation triggers the rapid differentiation of monocytes into macrophages and dendritic cells. Nat Med 11: 653.
40. Caparros, E., Munoz, P., Sierra-Filardi, E., Serrano-Gomez, D., Puig-Kroger, A., Rodriguez-Fernandez, J. L., Mellado, M., Sancho, J., Zubiaur, M., and Corbi, A. L. 2006. DC-SIGN ligation on dendritic cells results in ERK and PI3K activation and modulates cytokine production. Blood 107: 3950.
41. Chaipan, C., Soilleux, E. J., Simpson, P., Hofmann, H., Gramberg, T., Marzi, A., Geier, M., Stewart, E. A., Eisemann, J., Steinkasserer, A., Suzuki-Inoue, K., Fuller, G. L., Pearce, A. C., Watson, S. P., Hoxie, J. A., Baribaud, F., and Pohlmann, S. 2006. DC-SIGN and CLEC-2 mediate human immunodeficiency virus type 1 capture by platelets. J Virol 80: 8951.
42. Ceriello, A. 2005. Postprandial hyperglycemia and diabetes complications: is it time to treat? Diabetes 54: 1.
43. Schilder, R. J., and Marden, J. H. 2006. Metabolic syndrome and obesity in an insect. Proc Natl Acad Sci U S A 103: 18805.
44. Bouyain, S., Silk, N. J., Fabini, G., and Drickamer, K. 2002. An endogenous Drosophila receptor for glycans bearing alpha 1,3-linked core fucose residues. J Biol Chem 277: 22566.