Prophylactic anti-D preparations display variable decreases in Fc-fucosylation of anti-D

Transfusion

Volumn 55, Issue 3, 2015, Pages 553-562

  Kapur, Rick ^a,b   Della Valle, Luciana ^a,b   Verhagen, Onno J H M ^a,b   Hipgrave Ederveen, Agnes ^c   Ligthart, Peter ^d   De Haas, Masja ^a,b   Kumpel, Belinda ^e   Wuhrer, Manfred ^c   Van Der Schoot, C Ellen ^a,b   Vidarsson, Gestur ^a,b  

^a SANQUIN RESEARCH   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d CENTRAL LABORATORY   (Netherlands)

^e NHS BLOOD AND TRANSPLANT   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; FC RECEPTOR; IMMUNOGLOBULIN G1; RHESUS D ANTIBODY; ALLOANTIBODY; FCGR3A PROTEIN, HUMAN; FUCOSE; GALACTOSE; IMMUNOGLOBULIN FC FRAGMENT; IMMUNOGLOBULIN G; RHO(D) ANTIBODY;

ADULT; ARTICLE; BLOOD DONOR; BLOOD SAMPLING; CHEMICAL MODIFICATION; CONTROLLED STUDY; ERYTHROCYTE; FEMALE; FUCOSYLATION; GALACTOSYLATION; GLYCOSYLATION; HUMAN; IMMUNOPROPHYLAXIS; MALE; MIDDLE AGED; NORMAL HUMAN; PREGNANCY; PREGNANT WOMAN; BLOOD; CHEMISTRY; COMPARATIVE STUDY; IMMUNIZATION; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METABOLISM; PROTEIN PROCESSING; RH ISOIMMUNIZATION; SEXUAL DEVELOPMENT;

ADULT; BLOOD DONORS; FEMALE; FUCOSE; GALACTOSE; GLYCOSYLATION; HUMANS; IMMUNIZATION; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G; ISOANTIBODIES; MALE; MIDDLE AGED; PREGNANCY; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, IGG; RH ISOIMMUNIZATION; SEX CHARACTERISTICS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84924457035     PISSN: 00411132     EISSN: 15372995     Source Type: Journal    
DOI: 10.1111/trf.12880     Document Type: Article

References (39)

1. Kumpel BM, Elson CJ,. Mechanism of anti-D-mediated immune suppression-a paradox awaiting resolution? Trends Immunol 2001; 22: 26-31.
2. Bruin M, Bierings M, Uiterwaal C, et-al. Platelet count, previous infection and FCGR2B genotype predict development of chronic disease in newly diagnosed idiopathic thrombocytopenia in childhood: results of a prospective study. Br J Haematol 2004; 127: 561-567.
3. Breunis WB, van Mirre E, Bruin M, et-al. Copy number variation of the activating FCGR2C gene predisposes to idiopathic thrombocytopenic purpura. Blood 2008; 111: 1029-1038.
4. Miescher S, Spycher MO, Amstutz H, et-al. A single recombinant anti-RhD IgG prevents RhD immunization: association of RhD-positive red blood cell clearance rate with polymorphisms in the FcgammaRIIA and FcgammaIIIA genes. Blood 2004; 103: 4028-4035.
5. Beliard R, Waegemans T, Notelet D, et-al. A human anti-D monoclonal antibody selected for enhanced FcgammaRIII engagement clears RhD+ autologous red cells in human volunteers as efficiently as polyclonal anti-D antibodies. Br J Haematol 2008; 141: 109-119.
6. Kumpel BM, De Haas M, Koene HR, et-al. Clearance of red cells by monoclonal IgG3 anti-D in vivo is affected by the VF polymorphism of Fcgamma RIIIa (CD16). Clin Exp Immunol 2003; 132: 81-86.
7. Nimmerjahn F, Ravetch JV,. Anti-inflammatory actions of intravenous immunoglobulin. Annu Rev Immunol 2008; 26: 513-533.
8. Ferrara C, Stuart F, Sondermann P, et-al. The carbohydrate at FcgammaRIIIa Asn-162. An element required for high affinity binding to non-fucosylated IgG glycoforms. J Biol Chem 2006; 281: 5032-5036.
9. Ferrara C, Grau S, Jager C, et-al. Unique carbohydrate-carbohydrate interactions are required for high affinity binding between FcgammaRIII and antibodies lacking core fucose. Proc Natl Acad Sci U S A 2011; 108: 12669-12674.
10. Shields RL, Lai J, Keck R, et-al. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J Biol Chem 2002; 277: 26733-26740.
11. Yamane-Ohnuki N, Satoh M,. Production of therapeutic antibodies with controlled fucosylation. Mabs 2009; 1: 230-236.
12. Yver A, Homery MC, Fuseau E, et-al. Pharmacokinetics and safety of roledumab, a novel human recombinant monoclonal anti-RhD antibody with an optimized Fc for improved engagement of FCgammaRIII, in healthy volunteers. Vox Sang 2012; 103: 213-222.
13. Kapur R, Kustiawan I, Vestrheim A, et-al. A prominent lack of IgG1 Fc-fucosylation of platelet-alloantibodies in pregnancy. Blood 2014; 123: 471-480.
14. Kapur R, Della Valle L, Sonneveld M, et-al. Low anti-RhD IgG-Fc-fucosylation in pregnancy: a new variable predicting severity in haemolytic disease of the fetus and newborn. Br J Haematol 2014; 166: 936-945. [Correction added after online publication 19-September-2014: The article title has been updated.]
15. Thorpe SJ, Sands D, Fox B, et-al. A global standard for anti-D immunoglobulin: international collaborative study to evaluate a candidate preparation. Vox Sang 2003; 85: 313-321.
16. Vidarsson G, Stemerding AM, Stapleton NM, et-al. FcRn: an IgG receptor on phagocytes with a novel role in phagocytosis. Blood 2006; 108: 3573-3579.
17. Stapleton NM, Andersen JT, Stemerding AM, et-al. Competition for FcRn-mediated transport gives rise to short half-life of human IgG3 and offers therapeutic potential. Nat Commun 2011; 2: 599.
18. Selman MH, Derks RJ, Bondt A, et-al. Fc specific IgG glycosylation profiling by robust nano-reverse phase HPLC-MS using a sheath-flow ESI sprayer interface. J Proteomics 2012; 75: 1318-1329.
19. Einarsdottir HK, Selman MH, Kapur R, et-al. Comparison of the Fc glycosylation of fetal and maternal immunoglobulin G. Glycoconj J 2013; 30: 147-157.
20. Bakovic MP, Selman MH, Hoffmann M, et-al. High-throughput IgG Fc N-glycosylation profiling by mass spectrometry of glycopeptides. J Proteome Res 2013; 12: 821-831.
21. Ferrara C, Brunker P, Suter T, et-al. Modulation of therapeutic antibody effector functions by glycosylation engineering: influence of Golgi enzyme localization domain and co-expression of heterologous beta1, 4-N-acetylglucosaminyltransferase III and Golgi alpha-mannosidase II. Biotechnol Bioeng 2006; 93: 851-861.
22. Lubenko A, Williams M, Johnson A, et-al. Monitoring the clearance of fetal RhD-positive red cells in FMH following RhD immunoglobulin administration. Transfus Med 1999; 9: 331-335.
23. Olovnikova NI, Belkina EV, Drize NI, et-al. [Fast clearance of the rhesus-positive erythrocytes by monoclonal anti-rhesus antibodies-an insufficient condition for effective prophylaxis of rhesus-sensitization]. Biull Eksp Biol Med 2000; 129: 77-81.
24. Kumpel BM,. Efficacy of RhD monoclonal antibodies in clinical trials as replacement therapy for prophylactic anti-D immunoglobulin: more questions than answers. Vox Sang 2007; 93: 99-111.
25. De Haas M, Koene HR, Kleijer M, et-al. A triallelic Fc gamma receptor type IIIA polymorphism influences the binding of human IgG by NK cell Fc gamma RIIIa. J Immunol 1996; 156: 2948-2955.
26. Koene HR, Kleijer M, Algra J, et-al. Fc gammaRIIIa-158V/F polymorphism influences the binding of IgG by natural killer cell Fc gammaRIIIa, independently of the Fc gammaRIIIa-48L/R/H phenotype. Blood 1997; 90: 1109-1114.
27. Branch DR, Scofield TL, Moulds JJ, et-al. Unexpected suppression of anti-Fya and prevention of hemolytic disease of the fetus and newborn after administration of Rh immune globulin. Transfusion 2011; 51: 816-819.
28. Branch DR, Shabani F, Lund N, et-al. Antenatal administration of Rh-immune globulin causes significant increases in the immunomodulatory cytokines transforming growth factor-beta and prostaglandin E2. Transfusion 2006; 46: 1316-1322.
29. Karsten CM, Pandey MK, Figge J, et-al. Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of FcgammaRIIB and dectin-1. Nat Med 2012; 18: 1401-1406.
30. Kaneko Y, Nimmerjahn F, Ravetch JV,. Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 2006; 313: 670-673.
31. Anthony RM, Kobayashi T, Wermeling F, et-al. Intravenous gammaglobulin suppresses inflammation through a novel T(H)2 pathway. Nature 2011; 475: 110-113.
32. von Gunten S, Shoenfeld Y, Blank M, et-al. IVIG pluripotency and the concept of Fc-sialylation: challenges to the scientist. Nat Rev Immunol 2014; 14: 349.
33. Campbell IK, Miescher S, Branch DR, et-al. Therapeutic effect of IVIG on inflammatory arthritis in mice is dependent on the Fc portion and independent of sialylation or basophils. J Immunol 2014; 192: 5031-5038.
34. Leontyev D, Katsman Y, Branch DR,. Mouse background and IVIG dosage are critical in establishing the role of inhibitory Fcgamma receptor for the amelioration of experimental ITP. Blood 2012; 119: 5261-5264.
35. Winkler A, Berger M, Ehlers M,. Anti-rhesus D prophylaxis in pregnant women is based on sialylated IgG antibodies. F1000Res 2013; 2: 169.
36. Guo N, Liu Y, Masuda Y, et-al. Repeated immunization induces the increase in fucose content on antigen-specific IgG N-linked oligosaccharides. Clin Biochem 2005; 38: 149-153.
37. Siberil S, de Romeuf C, Bihoreau N, et-al. Selection of a human anti-RhD monoclonal antibody for therapeutic use: impact of IgG glycosylation on activating and inhibitory Fc gamma R functions. Clin Immunol 2006; 118: 170-179.
38. Armour KL, Parry-Jones DR, Beharry N, et-al. Intravascular survival of red cells coated with a mutated human anti-D antibody engineered to lack destructive activity. Blood 2006; 107: 2619-2626.
39. Thorpe SJ, Sands D, Fox B, et-al. Collaborative study for establishment of a global standard for the potency assay of human anti-D immunoglobulin. Pharmeuropa Bio 2004; 2003: 9-26.