The role of antibodies in enzyme treatments and therapeutic strategies

Best Practice and Research: Clinical Endocrinology and Metabolism

Volumn 29, Issue 2, 2015, Pages 183-194

  Bigger, Brian W ^a   Saif, Muhammad ^b   Linthorst, Gabor E ^c  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b MANCHESTER ROYAL INFIRMARY   (United Kingdom)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

antibodies; biomarker; lysosomal storage diseases enzyme replacement therapy; response

Indexed keywords

AGALSIDASE ALFA; AGALSIDASE BETA; ANTIBODY; ARYLSULFATASE; GLUCOSYLCERAMIDASE; LARONIDASE; LYSOSOME ENZYME; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CD20; UNCLASSIFIED DRUG; ALLOANTIBODY; ALPHA GALACTOSIDASE; ENZYME; GLUCAN 1,4 ALPHA GLUCOSIDASE;

ANTIBODY PRODUCTION; ANTIBODY TITER; B LYMPHOCYTE; BONE MARROW TRANSPLANTATION; CLINICAL TRIAL (TOPIC); ENZYME INHIBITION ASSAY; ENZYME REPLACEMENT; FABRY DISEASE; GAUCHER DISEASE; GLYCOGEN STORAGE DISEASE TYPE 2; HUMAN; IMMUNE EVASION; IMMUNE RESPONSE; IMMUNOASSAY; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; INFUSION RELATED REACTION; LYSOSOME STORAGE DISEASE; MEASUREMENT; MUCOPOLYSACCHARIDOSIS; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); REVIEW; TREATMENT OUTCOME; TREATMENT RESPONSE; GLYCOGEN STORAGE DISEASE TYPE II; IMMUNOLOGY; LYSOSOMAL STORAGE DISEASES;

ALPHA-GALACTOSIDASE; ANTIBODIES; ENZYME REPLACEMENT THERAPY; ENZYMES; FABRY DISEASE; GAUCHER DISEASE; GLUCAN 1,4-ALPHA-GLUCOSIDASE; GLUCOSYLCERAMIDASE; GLYCOGEN STORAGE DISEASE TYPE II; HUMANS; ISOANTIBODIES; LYSOSOMAL STORAGE DISEASES;

EID: 84929514007     PISSN: 1521690X     EISSN: 15321908     Source Type: Journal    
DOI: 10.1016/j.beem.2015.01.006     Document Type: Review

References (81)

1. T.M. Cox, and M.B. Cachón-González The cellular pathology of lysosomal diseases J Pathol 226 2011 241 254
2. T. Braulke, and J.S. Bonifacino Sorting of lysosomal proteins Biochim Biophys Acta 1793 2009 605 614
3. S. Porter Human immune response to recombinant human proteins J Pharm Sci 90 2001 1 11
4. A. Yoshioka, K. Fukutake, J. Takamatsu Kogenate Post-Marketing Surveillance Study Group Clinical evaluation of recombinant factor VIII preparation (Kogenate) in previously treated patients with hemophilia A: descriptive meta-analysis of post-marketing study data Int J Hematol 84 2006 158 165
5. A.J. Spijker, J. Poortman, and J.H. Thijssen Decrease of circulating insulin antibodies in two patients treated with continuous subcutaneous infusion of human insulin (recombinant DNA) Diabetes Care 5 Suppl. 2 1982 171 174
6. S.E. Fineberg, J.A. Galloway, and N.S. Fineberg Immunogenicity of recombinant DNA human insulin Diabetologia 25 1983 465 469
7. U. Di Mario, P. Arduini, and C. Tiberti Immunogenicity of biosynthetic human insulin. Humoral immune response in diabetic patients beginning insulin treatment and in patients previously treated with other insulins Diabetes Res Clin Pract 2 1986 317 324
8. H.J. Zeisel, A. Lutz, and W. Petrykowski von Immunogenicity of a mammalian cell-derived recombinant human growth hormone preparation during long-term treatment Horm Res 37 Suppl. 2 1992 47 55
9. L. Laricchia-Robbio, S. Moscato, and A. Genua Naturally occurring and therapy-induced antibodies to human granulocyte colony-stimulating factor (G-CSF) in human serum J Cell Physiol 173 1997 219 226
10. J.M. Urra, M. la Torre de, and R. Alcazar Rapid method for detection of anti-recombinant human erythropoietin antibodies as a new form of erythropoietin resistance Clin Chem 43 1997 848 849
11. R.J. Spiegel, J.R. Spicehandler, and S.L. Jacobs Low incidence of serum neutralizing factors in patients receiving recombinant alfa-2b interferon (Intron A) Am J Med 80 1986 223 228
12. M.A. Saif, B.W. Bigger, and K.E. Brookes Hematopoietic stem cell transplantation improves the high incidence of neutralizing allo-antibodies observed in Hurler's syndrome after pharmacological enzyme replacement therapy Haematologica 97 2012 1320 1328
13. S.M. Richards Immunologic considerations for enzyme replacement therapy in the treatment of lysosomal storage disorders Mol Genet Metab 105 2012 443 449
14. J. Oldenburg, and A. Pavlova Genetic risk factors for inhibitors to factors VIII and IX Haemophilia 12 Suppl. 6 2006 15 22
15. P.S. Kishnani, P.C. Goldenberg, and S.L. DeArmey Cross-reactive immunologic material status affects treatment outcomes in Pompe disease infants Mol Genet Metab 99 2010 26 33
16. A.R. Mire-Sluis, Y.C. Barrett, and V. Devanarayan Recommendations for the design and optimization of immunoassays used in the detection of host antibodies against biotechnology products J Immunol Methods 289 2004 1 16
17. G. Shankar, E. Shores, and C. Wagner Scientific and regulatory considerations on the immunogenicity of biologics Trends Biotechnol 24 2006 274 280
18. S. Gupta, V. Devanarayan, and D. Finco Recommendations for the validation of cell-based assays used for the detection of neutralizing antibody immune responses elicited against biological therapeutics J Pharm Biomed Anal 55 2011 878 888
19. R.O. Brady, J.F. Tallman, and W.G. Johnson Replacement therapy for inherited enzyme deficiency. Use of purified ceramidetrihexosidase in Fabry's disease N Engl J Med 289 1973 9 14
20. N.W. Barton, R.O. Brady, and J.M. Dambrosia Replacement therapy for inherited enzyme deficiency-macrophage- targeted glucocerebrosidase for Gaucher's disease N Engl J Med 324 1991 1464 1470
21. G.J. Murray, K.D. Howard, and S.M. Richards Gaucher's disease: lack of antibody response in 12 patients following repeated intravenous infusions of mannose terminal glucocerebrosidase J Immunol Methods 137 1991 113 120
22. M. Rosenberg, W. Kingma, and M.A. Fitzpatrick Immunosurveillance of alglucerase enzyme therapy for Gaucher patients: induction of humoral tolerance in seroconverted patients after repeat administration Blood 93 1999 2081 2088
23. K. Starzyk, S. Richards, and J. Yee The long-term international safety experience of imiglucerase therapy for Gaucher disease Mol Genet Metab 90 2007 157 163
24. R.O. Brady, G.J. Murray, and K.L. Oliver Management of neutralizing antibody to Ceredase in a patient with type 3 Gaucher disease Pediatrics 100 1997 E11
25. H. Zhao, L.A. Bailey, and G.A. Grabowski Enzyme therapy of gaucher disease: clinical and biochemical changes during production of and tolerization for neutralizing antibodies Blood Cells Mol Dis 30 2003 90 96
26. D.P. Germain, C.R. Kaneski, and R.O. Brady Mutation analysis of the acid beta-glucosidase gene in a patient with type 3 Gaucher disease and neutralizing antibody to alglucerase Mutat Res 483 2001 89 94
27. E. Ponce, J. Moskovitz, and G. Grabowski Enzyme therapy in Gaucher disease type 1: effect of neutralizing antibodies to acid beta-glucosidase Blood 90 1997 43 48
28. D. Fabbro, R.J. Desnick, and G.A. Grabowski Gaucher disease: genetic heterogeneity within and among the subtypes detected by immunoblotting Am J Hum Genet 40 1987 15 31
29. V.L. Tybulewicz, M.L. Tremblay, and M.E. LaMarca Animal model of Gaucher's disease from targeted disruption of the mouse glucocerebrosidase gene Nature 357 1992 407 410
30. van Gelder CM, Hoogeveen-Westerveld M, Kroos MA, et al. Enzyme therapy and immune response in relation to CRIM status: the Dutch experience in classic infantile Pompe disease. J Inherit Metab Dis [Epub ahead of print, PMID: 24715333]
31. S.G. Banugaria, T.T. Patel, and J. Mackey Persistence of high sustained antibodies to enzyme replacement therapy despite extensive immunomodulatory therapy in an infant with Pompe disease: need for agents to target antibody-secreting plasma cells Mol Genet Metab 105 2012 677 680
32. D.S. Bali, J.L. Goldstein, and S. Banugaria Predicting cross-reactive immunological material (CRIM) status in Pompe disease using GAA mutations: lessons learned from 10 years of clinical laboratory testing experience Am J Med Genet Part C Semin Med Genet 160C 2012 40 49
33. A.T. van der Ploeg, P.R. Clemens, and D. Corzo A randomized study of alglucosidase alfa in late-onset Pompe's disease N Engl J Med 362 2010 1396 1406
34. J.M. de Vries, N.A. van der Beek, and M.A. Kroos High antibody titer in an adult with Pompe disease affects treatment with alglucosidase alfa Mol Genet Metab 101 2010 338 345
35. R. Schiffmann, J.B. Kopp, and H.A. Austin Enzyme replacement therapy in Fabry disease: a randomized controlled trial J Am Med Assoc 285 2001 2743 2749
36. C.M. Eng, N. Guffon, and W.R. Wilcox Safety and efficacy of recombinant human alpha-galactosidase A-replacement therapy in Fabry's disease N Engl J Med 345 2001 9 16
37. D. Blom, D. Speijer, and G.E. Linthorst Recombinant enzyme therapy for Fabry disease: absence of editing of human alpha-galactosidase A mRNA Am J Hum Genet 72 2003 23 31
38. K. Lee, X. Jin, and K. Zhang A biochemical and pharmacological comparison of enzyme replacement therapies for the glycolipid storage disorder Fabry disease 2005
39. A.C. Vedder, G.E. Linthorst, and G. Houge Treatment of Fabry disease: outcome of a comparative trial with agalsidase alfa or beta at a dose of 0.2 mg/kg PLoS One 2 2007 e598
40. B.K. Burton, D.A.H. Whiteman, and Investigators OBOTH Incidence and timing of infusion-related reactions in patients with mucopolysaccharidosis type II (Hunter syndrome) on idursulfase therapy in the real-world setting: a perspective from the Hunter Outcome Survey (HOS) Mol Genet Metab 103 2011 113 120
41. B.E. Smid, S.L. Hoogendijk, and F.A. Wijburg A revised home treatment algorithm for Fabry disease: influence of antibody formation Mol Genet Metab 2013 1 6
42. D. Bodensteiner, C.R. Scott, and K.B. Sims Successful reinstitution of agalsidase beta therapy in Fabry disease patients with previous IgE-antibody or skin-test reactivity to the recombinant enzyme Genet Med 10 2008 353 358
43. G.E. Linthorst, C.E.M. Hollak, and W.E. Donker-Koopman Enzyme therapy for Fabry disease: neutralizing antibodies toward agalsidase alpha and beta Kidney Int 66 2004 1589 1595
44. T. Ohashi, M. Sakuma, and T. Kitagawa Influence of antibody formation on reduction of globotriaosylceramide (GL-3) in urine from Fabry patients during agalsidase beta therapy Mol Genet Metab 92 2007 271 273
45. FDA briefing document Fabrazyme.
46. T. Ohashi, S. Iizuka, and H. Ida Reduced alpha-Gal A enzyme activity in Fabry fibroblast cells and Fabry mice tissues induced by serum from antibody positive patients with Fabry disease Mol Genet Metab 94 2008 313 318
47. P.D. Whitfield, J. Calvin, and S. Hogg Monitoring enzyme replacement therapy in Fabry disease-role of urine globotriaosylceramide J Inherit Metab Dis 28 2005 21 33
48. M.J. van Breemen, S.M. Rombach, and N. Dekker Reduction of elevated plasma globotriaosylsphingosine in patients with classic Fabry disease following enzyme replacement therapy Biochim Biophys Acta 1812 2011 70 76
49. S.M. Rombach, J.M.F.G. Aerts, and B.J.H.M. Poorthuis Long-term effect of antibodies against infused alpha-galactosidase a in fabry disease on plasma and urinary (lyso)Gb3 reduction and treatment outcome PLoS One 7 2012 e47805
50. B. Bénichou, S. Goyal, and C. Sung A retrospective analysis of the potential impact of IgG antibodies to agalsidase β on efficacy during enzyme replacement therapy for Fabry disease Mol Genet Metab 96 2009 4 12
51. J. Lubanda, E. Anijalg, and V. Bzdúch Evaluation of a low dose, after a standard therapeutic dose, of agalsidase beta during enzyme replacement therapy in patients with Fabry disease Genet Med 11 2009 256 264
52. S.M. Rombach, B.E. Smid, and M.G. Bouwman Long term enzyme replacement therapy for Fabry disease: effectiveness on kidney, heart and brain Orphanet J Rare Dis 8 2013 47
53. W.R. Wilcox, G.E. Linthorst, and D.P. Germain Anti-α-galactosidase A antibody response to agalsidase beta treatment: data from the Fabry registry Mol Genet Metab 105 2012 443 449
54. H. Schellekens The immunogenicity of therapeutic proteins and the Fabry antibody standardization initiative Clin Ther 30 Suppl. B 2008 S50 S51
55. R.M. Shull, E.D. Kakkis, and M.F. McEntee Enzyme replacement in a canine model of Hurler syndrome Proc Natl Acad Sci U S A 91 1994 12937 12941
56. R. Kakavanos, C.T. Turner, and J.J. Hopwood Immune tolerance after long-term enzyme-replacement therapy among patients who have mucopolysaccharidosis I Lancet 361 2003 1608 1613
57. J.E. Wraith, L.A. Clarke, and M. Beck Enzyme replacement therapy for mucopolysaccharidosis I: a randomized, double-blinded, placebo-controlled, multinational study of recombinant human alpha-L-iduronidase (laronidase) J Pediatr 144 2004 581 588
58. S.E. Lipinski, M.J. Lipinski, and A. Burnette Desensitization of an adult patient with Pompe disease and a history of anaphylaxis to alglucosidase alfa Mol Genet Metab 98 2009 319 321
59. P. Dickson, M. Peinovich, and M. Mcentee Immune tolerance improves the efficacy of enzyme replacement therapy in canine mucopolysaccharidosis I J Clin Invest 118 2008 2868 2876
60. K.P. Ponder Immune response hinders therapy for lysosomal storage diseases J Clin Invest 118 2008 2686 2689
61. J.E. Wraith, M. Beck, and R. Lane Enzyme replacement therapy in patients who have mucopolysaccharidosis I and are younger than 5 years: results of a multinational study of recombinant human alpha-L-iduronidase (laronidase) Pediatrics 120 2007 e37 46
62. R.F. Wynn, and J.J. Boelens Bone-marrow transplantation in non-malignant disease Lancet 374 2009 856 858
63. K.J. Langford-Smith, J. Mercer, and J. Petty Heparin cofactor II-thrombin complex and dermatan sulphate:chondroitin sulphate ratio are biomarkers of short- and long-term treatment effects in mucopolysaccharide diseases J Inherit Metab Dis 34 2011 499 508
64. J. Cox-Brinkman, M.A. van den Bergh Weerman, and F.A. Wijburg Ultrastructural analysis of dermal fibroblasts in mucopolysaccharidosis type I: effects of enzyme replacement therapy and hematopoietic cell transplantation Ultrastruct Pathol 34 2010 126 132
65. E.J. Langereis, N. van Vlies, and H.J. Church Biomarker responses correlate with antibody status in mucopolysaccharidosis type I patients on long-term enzyme replacement therapy Mol Genet Metab 14 2015 129 137
66. J. Muenzer, J.E. Wraith, and M. Beck A phase II/III clinical study of enzyme replacement therapy with idursulfase in mucopolysaccharidosis II (Hunter syndrome) Genet Med 8 2006 465 473
67. J. Muenzer, M. Gucsavas-Calikoglu, and S.E. McCandless A phase I/II clinical trial of enzyme replacement therapy in mucopolysaccharidosis II (Hunter syndrome) Mol Genet Metab 90 2007 329 337
68. J. Muenzer, M. Beck, and C.M. Eng Long-term, open-labeled extension study of idursulfase in the treatment of Hunter syndrome Genet Med 13 2011 95 101
69. L.A. Clarke, H. Hemmelgarn, and K. Colobong Longitudinal observations of serum heparin cofactor II-thrombin complex in treated mucopolysaccharidosis I and II patients J Inherit Metab Dis 35 2011 355 362
70. A.J. Barbier, B. Bielefeld, and D.A.H. Whiteman The relationship between anti-idursulfase antibody status and safety and efficacy outcomes in attenuated mucopolysaccharidosis II patients aged 5 years and older treated with intravenous idursulfase Mol Genet Metab 110 2013 303 310
71. STRIVE Investigators, C.J. Hendriksz, and B. Burton Efficacy and safety of enzyme replacement therapy with BMN 110 (elosulfase alfa) for morquio A syndrome (mucopolysaccharidosis IVA): a phase 3 randomised placebo-controlled study J Inherit Metab Dis 37 2014 979 990
72. B. Schweighardt, T. Tompkins, and K. Lau Immunogenicity of elosulfase alfa, an enzyme replacement therapy in patients with morquio a syndrome: results from MOR-004, a phase III trial Clin Ther 2014 1 10
73. P. Harmatz, Z.-F. Yu, and R. Giugliani Enzyme replacement therapy for mucopolysaccharidosis VI: evaluation of long-term pulmonary function in patients treated with recombinant human N-acetylgalactosamine 4-sulfatase J Inherit Metab Dis 33 2010 51 60
74. M.M. Brands, M. Hoogeveen-Westerveld, and M.A. Kroos Mucopolysaccharidosis type VI phenotypes-genotypes and antibody response to galsulfase Orphanet J Rare Dis 8 2013 51
75. H. Debiec, V. Valayannopoulos, and O. Boyer Allo-immune membranous nephropathy and recombinant aryl sulfatase replacement therapy: a need for tolerance induction therapy J Am Soc Nephrol 25 2014 675 680
76. T.E. Hunley, D. Corzo, and M. Dudek Nephrotic syndrome complicating alpha-glucosidase replacement therapy for Pompe disease Pediatrics 114 2004 e532 e535
77. A.C. Vedder, F. Breunig, and W.E. Donker-Koopman Treatment of Fabry disease with different dosing regimens of agalsidase: effects on antibody formation and GL-3 Mol Genet Metab 94 2008 319 325
78. C.L. Kempton, and S.L. Meeks Toward optimal therapy for inhibitors in hemophilia Blood 124 2014 3365 3372
79. C. Leissinger, C.D. Josephson, and S. Granger Rituximab for treatment of inhibitors in haemophilia A Thromb Haemost 112 2014 445 458
80. N.J. Mendelsohn, Y.H. Messinger, and A.S. Rosenberg Elimination of antibodies to recombinant enzyme in Pompe's disease N Engl J Med 360 2009 194 195
81. S.G. Banugaria, S.N. Prater, and J.K. McGann Bortezomib in the rapid reduction of high sustained antibody titers in disorders treated with therapeutic protein: lessons learned from Pompe disease Genet Med 15 2012 123 131