Myeloid glycosylation defects lead to a spontaneous common variable immunodeficiency-like condition with associated hemolytic anemia and antilymphocyte autoimmunity

Journal of Immunology

Volumn 192, Issue 12, 2014, Pages 5561-5570

  Ryan, Sean O ^a   Abbott, Derek W ^a   Cobb, Brian A ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; IMMUNOGLOBULIN G; N ACETYLGLUCOSAMINYLTRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; AUTOIMMUNITY; BONE MARROW CELL; CELL LINEAGE; CELL METABOLISM; CELL SELECTION; CELL SURFACE; COMMON VARIABLE IMMUNODEFICIENCY; CONTROLLED STUDY; CROSS REACTION; DISEASE ACTIVITY; GENE; GENE FUNCTION; GENE IDENTIFICATION; GLYCOSYLATION; HEMOLYTIC ANEMIA; IMMUNE RESPONSE; LYMPHOCYTE FUNCTION; LYMPHOCYTOPENIA; MGAT2 GENE; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ANEMIA, HEMOLYTIC, AUTOIMMUNE; ANIMALS; AUTOANTIBODIES; COMMON VARIABLE IMMUNODEFICIENCY; CROSS REACTIONS; ERYTHROCYTES; GLYCOSYLATION; HUMANS; IMMUNITY, HUMORAL; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; MICE; MICE, KNOCKOUT; MYELOID CELLS; N-ACETYLGLUCOSAMINYLTRANSFERASES; ORGAN SPECIFICITY; T-LYMPHOCYTES;

EID: 84902193130     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400385     Document Type: Article

References (33)

1. International Union of Immunological Societies. 1999. Primary immunodeficiency diseases. Report of an IUIS Scientific Committee. Clin. Exp. Immunol. 118(Suppl 1):1-28.
2. Salzer, U., K. Warnatz, and H. H. Peter. 2012. Common variable immunodeficiency - an update. Arthritis Res. Ther. 14:223.
3. Park, J. H., E. S. Resnick, and C. Cunningham-Rundles. 2011. Perspectives on common variable immune deficiency. Ann. N. Y. Acad. Sci. 1246:41-49.
4. Lee, J. J., I. Rauter, L. Garibyan, E. Ozcan, T. Sannikova, S. R. Dillon, A. C. Cruz, R. M. Siegel, R. Bram, H. Jabara, and R. S. Geha. 2009. The murine equivalent of the A181E TACI mutation associated with common variable immunodeficiency severely impairs B-cell function. Blood 114:2254-2262.
5. Resnick, E. S., and C. Cunningham-Rundles. 2012. The many faces of the clinical picture of common variable immune deficiency. Curr. Opin. Allergy Clin. Immunol. 12:595-601.
6. Bateman, E. A., L. Ayers, R. Sadler, M. Lucas, C. Roberts, A. Woods, K. Packwood, J. Burden, D. Harrison, N. Kaenzig, et al. 2012. T cell phenotypes in patients with common variable immunodeficiency disorders: associations with clinical phenotypes in comparison with other groups with recurrent infections. Clin. Exp. Immunol. 170:202-211.
7. Giovannetti, A., M. Pierdominici, F. Mazzetta, M. Marziali, C. Renzi, A. M. Mileo, M. De Felice, B. Mora, A. Esposito, R. Carello, et al. 2007. Unravelling the complexity of T cell abnormalities in common variable immunodeficiency. J. Immunol. 178:3932-3943.
8. Mouillot, G., M. Carmagnat, L. Gérard, J. L. Garnier, C. Fieschi, N. Vince, L. Karlin, J. F. Viallard, R. Jaussaud, J. Boileau, et al. 2010. B-cell and T-cell phenotypes in CVID patients correlate with the clinical phenotype of the disease. J. Clin. Immunol. 30:746-755.
9. Agarwal, S., and C. Cunningham-Rundles. 2009. Autoimmunity in common variable immunodeficiency. Curr. Allergy Asthma Rep. 9:347-352.
10. Cunningham-Rundles, C. 2008. Autoimmune manifestations in common variable immunodeficiency. J. Clin. Immunol. 28(Suppl. 1):S42-S45.
11. Ryan, S. O., S. M. Leal, Jr., D. W. Abbott, E. Pearlman, and B. A. Cobb. 2014. Mgat2 ablation in the myeloid lineage leads to defective glycoantigen T cell responses. Glycobiology 24:262-271.
12. Lai, Z., and J. R. Schreiber. 2011. Outer membrane protein complex of Meningococcus enhances the antipolysaccharide antibody response to pneumococcal polysaccharide-CRM197 conjugate vaccine. Clin. Vaccine Immunol. 18:724-729.
13. Ryan, S. O., A. M. Vlad, K. Islam, J. Gariépy, and O. J. Finn. 2009. Tumorassociated MUC1 glycopeptide epitopes are not subject to self-tolerance and improve responses to MUC1 peptide epitopes in MUC1 transgenic mice. Biol. Chem. 390:611-618.
14. Ryan, S. O., J. A. Bonomo, F. Zhao, and B. A. Cobb. 2011. MHCII glycosylation modulates Bacteroides fragilis carbohydrate antigen presentation. J. Exp. Med. 208:1041-1053.
15. Ryan, S. O., J. L. Johnson, and B. A. Cobb. 2013. Neutrophils confer T cell resistance to myeloid-derived suppressor cell-mediated suppression to promote chronic inflammation. J. Immunol. 190:5037-5047.
16. Gruber, W. C., D. A. Scott, and E. A. Emini. 2012. Development and clinical evaluation of Prevnar 13, a 13-valent pneumocococcal CRM197 conjugate vaccine. Ann. N. Y. Acad. Sci. 1263:15-26.
17. Podjasek, J. C., and R. S. Abraham. 2012. Autoimmune cytopenias in common variable immunodeficiency. Front. Immunol. 3:189.
18. Guazzi, V., F. Aiuti, I. Mezzaroma, F. Mazzetta, G. Andolfi, A. Mortellaro, M. Pierdominici, R. Fantini, M. Marziali, and A. Aiuti. 2002. Assessment of thymic output in common variable immunodeficiency patients by evaluation of T cell receptor excision circles. Clin. Exp. Immunol. 129:346-353.
19. Ye, M., H. Iwasaki, C. V. Laiosa, M. Stadtfeld, H. Xie, S. Heck, B. Clausen, K. Akashi, and T. Graf. 2003. Hematopoietic stem cells expressing the myeloid lysozyme gene retain long-term, multilineage repopulation potential. Immunity 19:689-699.
20. Sellon, R. K., S. Tonkonogy, M. Schultz, L. A. Dieleman, W. Grenther, E. Balish, D. M. Rennick, and R. B. Sartor. 1998. Resident enteric bacteria are necessary for development of spontaneous colitis and immune system activation in interleukin-10-deficient mice. Infect. Immun. 66:5224-5231.
21. Haury, M., A. Sundblad, A. Grandien, C. Barreau, A. Coutinho, and A. Nobrega. 1997. The repertoire of serum IgM in normal mice is largely independent of external antigenic contact. Eur. J. Immunol. 27:1557-1563.
22. Amaral, J. F., D. A. Foschetti, F. A. Assis, J. S. Menezes, N. M. Vaz, and A. M. Faria. 2006. Immunoglobulin production is impaired in protein-deprived mice and can be restored by dietary protein supplementation. Braz. J. Med. Biol. Res. 39:1581-1586.
23. Jaeken, J. 2010. Congenital disorders of glycosylation. Ann. N. Y. Acad. Sci. 1214:190-198.
24. Saldova, R., L. Royle, C. M. Radcliffe, U. M. Abd Hamid, R. Evans, J. N. Arnold, R. E. Banks, R. Hutson, D. J. Harvey, R. Antrobus, et al. 2007. Ovarian cancer is associated with changes in glycosylation in both acute-phase proteins and IgG. Glycobiology 17:1344-1356.
25. Turner, G. A., M. T. Goodarzi, and S. Thompson. 1995. Glycosylation of a-1-proteinase inhibitor and haptoglobin in ovarian cancer: evidence for two different mechanisms. Glycoconj. J. 12:211-218.
26. Thompson, S., E. Dargan, I. D. Griffiths, C. A. Kelly, and G. A. Turner. 1993. The glycosylation of haptoglobin in rheumatoid arthritis. Clin. Chim. Acta 220:107-114.
27. Gravel, P., C. Walzer, C. Aubry, L. P. Balant, B. Yersin, D. F. Hochstrasser, and J. Guimon. 1996. New alterations of serum glycoproteins in alcoholic and cirrhotic patients revealed by high resolution two-dimensional gel electrophoresis. Biochem. Biophys. Res. Commun. 220:78-85.
28. Mann, A. C., C. O. Record, C. H. Self, and G. A. Turner. 1994. Monosaccharide composition of haptoglobin in liver diseases and alcohol abuse: large changes in glycosylation associated with alcoholic liver disease. Clin. Chim. Acta 227:69-78.
29. Goodarzi, M. T., and G. A. Turner. 1998. Reproducible and sensitive determination of charged oligosaccharides from haptoglobin by PNGase F digestion and HPAEC/PAD analysis: glycan composition varies with disease. Glycoconj. J. 15:469-475.
30. Demetriou, M., M. Granovsky, S. Quaggin, and J. W. Dennis. 2001. Negative regulation of T-cell activation and autoimmunity by Mgat5 N-glycosylation. Nature 409:733-739.
31. Wang, Y., J. Tan, M. Sutton-Smith, D. Ditto, M. Panico, R. M. Campbell, N. M. Varki, J. M. Long, J. Jaeken, S. R. Levinson, et al. 2001. Modeling human congenital disorder of glycosylation type IIa in the mouse: conservation of asparagine-linked glycan-dependent functions in mammalian physiology and insights into disease pathogenesis. Glycobiology 11:1051-1070.
32. De Vera, M. J., L. Al-Harthi, and A. T. Gewurz. 2004. Assessing thymopoiesis in patients with common variable immunodeficiency as measured by T-cell receptor excision circles. Ann. Allergy Asthma Immunol. 93:478-484.
33. Kimmig, S., G. K. Przybylski, C. A. Schmidt, K. Laurisch, B. Möwes, A. Radbruch, and A. Thiel. 2002. Two subsets of naive T helper cells with distinct T cell receptor excision circle content in human adult peripheral blood. J. Exp. Med. 195:789-794