Galactosylation of IgG1 modulates FcγRIIB-mediated inhibition ofmurine autoimmune hemolytic anemia

Journal of Autoimmunity

Volumn 47, Issue , 2013, Pages 104-110

  Yamada, Kazunori ^a   Ito, Kiyoaki ^a   Furukawa, Jun Ichi ^b   Nakata, Junichiro ^a   Alvarez, Montserrat ^a   Verbeek, J Sjef ^c   Shinohara, Yasuro ^b   Izui, Shozo ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b HOKKAIDO UNIVERSITY   (Japan)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Autoimmune hemolytic anemia; Fc R; IgG glycosylation

Indexed keywords

ASPARAGINE LINKED OLIGOSACCHARIDE; AUTOANTIBODY; EYTHROCYTE MONOCLONAL ANTIBODY; FC RECEPTOR IIB; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G3; IRON; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNE HEMOLYTIC ANEMIA; BIOTRANSFORMATION; CHEMICAL MODIFICATION; COMPARATIVE STUDY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; GALACTOSYLATION; KUPFFER CELL; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOUSE; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; SIALYLATION; WILD TYPE;

AUTOIMMUNE HEMOLYTIC ANEMIA; FCΓR; IGG GLYCOSYLATION;

ANEMIA, HEMOLYTIC, AUTOIMMUNE; ANIMALS; ANTIBODIES, MONOCLONAL; AUTOANTIBODIES; ERYTHROCYTES; GALACTOSE; IMMUNOGLOBULIN G; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, IGG;

EID: 84888205517     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2013.09.001     Document Type: Article

References (48)

1. Howie J.B., Helyer B.J. The immunology and pathology of NZB mice. Adv Immunol 1968, 9:215-266.
2. Izui S. Autoimmune hemolytic anemia. Curr Opin Immunol 1994, 6:926-930.
3. Shibata T., Berney T., Reininger L., Chicheportiche Y., Ozaki S., Shirai T., et al. Monoclonal anti-erythrocyte autoantibodies derived from NZB mice cause autoimmune hemolytic anemia by two distinct pathogenic mechanisms. Int Immunol 1990, 2:1133-1141.
4. Azeredo da Silveira S., Kikuchi S., Fossati-Jimack L., Moll T., Saito T., Verbeek J.S., et al. Complement activation selectively potentiates the pathogenicity of the IgG2b and IgG3 isotypes of a high affinity anti-erythrocyte autoantibody. JExp Med 2002, 195:665-672.
5. Fossati-Jimack L., Ioan-Facsinay A., Reininger L., Chicheportiche Y., Watanabe N., Saito T., et al. Markedly different pathogenicity of four IgG isotype-switch variants of an anti-erythrocyte autoantibody is based on their respective capacity to interact invivo with the low-affinity FcγRIII. JExp Med 2000, 191:1293-1302.
6. Fossati-Jimack L., Reininger L., Chicheportiche Y., Clynes R., Ravetch J.V., Honjo T., et al. High pathogenic potential of low-affinity autoantibodies in experimental autoimmune hemolytic anemia. JExp Med 1999, 190:1689-1696.
7. Ravetch J.V., Kinet J.P. Fc receptors. Annu Rev Immunol 1991, 9:457-492.
8. Nimmerjahn F., Bruhns P., Horiuchi K., Ravetch J.V. FcγRIV: a novel FcR with distinct IgG subclass specificity. Immunity 2005, 23:41-51.
9. Nimmerjahn F., Ravetch J.V. Fcγ receptors: old friends and new family members. Immunity 2006, 24:19-28.
10. Baudino L., Nimmerjahn F., Azeredo da Silveira S., Martinez-Soria E., Saito T., Carroll M., et al. Differential contribution of three activating IgG Fc receptors (FcγRI, FcγRIII, and FcγRIV) to IgG2a- and IgG2b-induced autoimmune hemolytic anemia in mice. JImmunol 2008, 180:1948-1953.
11. Meyer D., Schiller C., Westermann J., Izui S., Hazenbos W.L.W., Verbeek J.S., et al. FcγRIII (CD16)-deficient mice show IgG isotope-dependent protection to experimental autoimmune hemolytic anemia. Blood 1998, 92:3997-4002.
12. Nimmerjahn F., Ravetch J.V. Divergent immunoglobulin-G subclass activity through selective Fc receptor binding. Science 2005, 310:1510-1512.
13. Takai T., Ono M., Hikida M., Ohmori H., Ravetch J.V. Augmented humoral and anaphylactic responses in FcγRII-deficient mice. Nature 1996, 379:346-349.
14. Ujike A., Ishikawa Y., Ono M., Yuasa T., Yoshino T., Fukumoto M., et al. Modulation of IgE-mediated systemic anaphylaxis by low-affinity Fc receptors for IgG. JExp Med 1999, 189:1573-1579.
15. Clynes R., Maizes J.S., Guinamard R., Ono M., Takai T., Ravetch J.V. Modulation of immune complex-induced inflammation invivo by the coordinate expression of activation and inhibitory Fc receptors. JExp Med 1999, 189:179-185.
16. b mice susceptible to collagen-induced arthritis. JExp Med 1999, 189:187-194.
17. Schiller C., Janssen-Graalfs I., Baumann U., Schwerter-Strumpf K., Izui S., Takai T., et al. Mouse FcγRII is a negative regulator of FcγRIII in IgG immune complex triggered inflammation but not in autoantibody induced hemolysis. Eur J Immunol 2000, 30:481-490.
18. Nakamura A., Yuasa T., Ujike A., Ono M., Nukiwa T., Ravetch J.V., et al. Fcγ receptor IIB-deficient mice develop Goodpasture's syndrome upon immunization with type IV collagen: a novel murine model for autoimmune glomerular basement membrane disease. JExp Med 2000, 191:899-905.
19. Parekh R.B., Dwek R.A., Sutton B.J., Fernandes D.L., Leung A., Stanworth D., et al. Association of rheumatoid arthritis and primary osteoarthritis with changes in the glycosylation pattern of total serum IgG. Nature 1985, 316:452-457.
20. Mizuochi T., Hamako J., Nose M., Titani K. Structural changes in the oligosaccharide chains of IgG in autoimmune MRL/Mp-lpr/lpr mice. JImmunol 1990, 145:1794-1798.
21. Malhotra R., Wormald M.R., Rudd P.M., Fischer P.B., Dwek R.A., Sim R.B. Glycosylation changes of IgG associated with rheumatoid arthritis can activate complement via the mannose-binding protein. Nat Med 1995, 1:237-243.
22. Kaneko Y., Nimmerjahn F., Ravetch J.V. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 2006, 313:670-673.
23. Scallon B.J., Tam S.H., McCarthy S.G., Cai A.N., Raju T.S. Higher levels of sialylated Fc glycans in immunoglobulin G molecules can adversely impact functionality. Mol Immunol 2007, 44:1524-1534.
24. Boross P., Arandhara V.L., Martin-Ramirez J., Santiago-Raber M.L., Carlucci F., Flierman R., et al. The inhibiting Fc receptor for IgG, FcγRIIB, is a modifier of autoimmune susceptibility. JImmunol 2011, 187:1304-1313.
25. Hazenbos W.L.W., Gessner J.E., Hofhuis F.M.A., Kuipers H., Meyer D., Heijnen I.A.F.M., et al. Impaired IgG-dependent anaphylaxis and Arthus reaction in FcγRIII (CD16) deficient mice. Immunity 1996, 5:181-188.
26. Wessels M.R., Butko P., Ma M., Warren H.B., Lage A.L., Carroll M.C. Studies of group B streptococcal infection in mice deficient in complement component C3 or C4 demonstrate an essential role for complement in both innate and acquired immunity. Proc Natl Acad Sci U S A 1995, 92:11490-11494.
27. Caulfield M.J., Stanko D. Apathogenic monoclonal antibody, G8, is characteristic of antierythrocyte autoantibodies from Coombs'-positive NZB mice. JImmunol 1992, 148:2068-2073.
28. Baudino L., Nimmerjahn F., Shinohara Y., Furukawa J.-I., Petry F., Verbeek J.S., et al. Impact of a three amino-acid deletion in the CH2 domain of murine IgG1 on Fc-associated effector functions. JImmunol 2008, 181:4107-4112.
29. Nakazawa K., Ando T., Kimura T., Narimatsu H. Cloning and sequencing of a full-length cDNA of mouse N-acetylglucosamine (β1-4) galactosyltransferase. JBiochem 1988, 104:165-168.
30. Neuberger M.S. Expression and regulation of immunoglobulin heavy gene transfected into lymphoid cells. EMBO J 1983, 2:1373-1378.
31. Simon T., Rajewsky K. "Enhancer-constitutive" vectors for the expression of recombinant antibodies. Nucleic Acids Res 1988, 16:354.
32. Nishimura S.-I., Niikura K., Kurogochi M., Matsushita T., Fumoto M., Hinou H., et al. High-throughput protein glycomics: combined use of chemoselective glycoblotting and MALDI-TOF/TOF mass spectrometry. Angew Chem Int Ed Engl 2004, 44:91-96.
33. Furukawa J.-I., Shinohara Y., Kuramoto H., Miura Y., Shimaoka H., Kurogochi M., et al. Comprehensive approach to structural and functional glycomics based on chemoselective glycoblotting and sequential tag conversion. Anal Chem 2008, 80:1094-1101.
34. Kita Y., Miura Y., Furukawa J., Nakano M., Shinohara Y., Ohno M., et al. Quantitative glycomics of human whole serum glycoproteins based on the standardized protocol for liberating N-glycans. Mol Cell Proteomics 2007, 6:1437-1445.
35. Miura Y., Shinohara Y., Furukawa J., Nagahori N., Nishimura S. Rapid and simple solid-phase esterification of sialic acid residues for quantitative glycomics by mass spectrometry. Chemistry 2007, 13:4797-4804.
36. Nose M., Wigzell H. Biological significance of carbohydrate chains on monoclonal antibodies. Proc Natl Acad Sci U S A 1983, 80:6632-6636.
37. Wright A., Morrison S.L. Effect of altered CH-associated carbohydrate structure on the functional properties and invivo fate of chimeric mouse-human immunoglobulin G1. JExp Med 1994, 180:1087-1096.
38. Nandakumar K.S., Collin M., Olsen A., Nimmerjahn F., Blom A.M., Ravetch J.V., et al. Endoglycosidase treatment abrogates IgG arthritogenicity: importance of IgG glycosylation in arthritis. Eur J Immunol 2007, 37:2973-2982.
39. Nimmerjahn F., Anthony R.M., Ravetch J.V. Agalactosylated IgG antibodies depend on cellular Fc receptors for invivo activity. Proc Natl Acad Sci U S A 2007, 104:8433-8437.
40. Keusch J., Lydyard P.M., Delves P.J. The effect on IgG glycosylation of altering β1,4-galactosyltransferase-1 activity in B cells. Glycobiology 1998, 8:1215-1220.
41. Parekh R., Isenberg D., Rook G., Roitt I., Dwek R., Rademacher T. Acomparative analysis of disease-associated changes in the glycosylation of serum IgG. JAutoimmun 1989, 2:101-114.
42. Bond A., Cooke A., Hay F.C. Glycosylation of IgG, immune complexes and IgG subclasses in the MRL-lpr/lpr mouse model of rheumatoid arthritis. Eur J Immunol 1990, 20:2229-2233.
43. Rademacher T.W., Williams P., Dwek R.A. Agalactosyl glycoforms of IgG autoantibodies are pathogenic. Proc Natl Acad Sci U S A 1994, 91:6123-6127.
44. Baudino L., Shinohara Y., Nimmerjahn F., Furukawa J.-I., Nakata M., Martinez-Soria E., et al. Crucial role of aspartic acid at position 265 in the CH2 domain for murine IgG2a and IgG2b Fc-associated effector functions. JImmunol 2008, 181:6664-6669.
45. Hadley A.G., Zupanska B., Kumpel B.M., Pilkington C., Griffiths H.L., Leader K.A., et al. The glycosylation of red cell autoantibodies affects their functional activity invitro. Br J Haematol 1995, 91:587-594.
46. Kumpel B.M., Wang Y., Griffiths H.L., Hadley A.G., Rook G.A. The biological activity of human monoclonal IgG anti-D is reduced by beta-galactosidase treatment. Hum Antib Hybrid 1995, 6:82-88.
47. Boyd P.N., Lines A.C., Patel A.K. The effect of the removal of sialic acid, galactose and total carbohydrate on the functional activity of Campath-1H. Mol Immunol 1995, 32:1311-1318.
48. Hulett M.D., Hogarth P.M. Molecular basis of Fc receptor function. Adv Immunol 1994, 57:1-127.