Immunogenicity of biotherapy used in psoriasis: The science behind the scenes

Journal of Investigative Dermatology

Volumn 135, Issue 1, 2015, Pages 31-38

  Jullien, Denis ^a   Prinz, Jörg C ^b   Nestle, Frank O ^c  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITY OF MUNICH   (Germany)

^c ST THOMAS HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADALIMUMAB; DRUG ANTIBODY; ETANERCEPT; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G4; INFLIXIMAB; METHOTREXATE; TOCILIZUMAB; TUMOR NECROSIS FACTOR INHIBITOR; USTEKINUMAB; BIOLOGICAL PRODUCT; EPITOPE; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY;

ANTIBODY RESPONSE; ANTIGEN ANTIBODY COMPLEX; BIOLOGICAL THERAPY; DEAMINATION; DESENSITIZATION; DRUG BINDING SITE; DRUG BLOOD LEVEL; DRUG EFFICACY; DRUG SAFETY; HELPER CELL; HUMAN; HUMORAL IMMUNITY; IMMUNOGENICITY; INJECTION SITE REACTION; PRIORITY JOURNAL; PSORIASIS; REVIEW; THROMBOEMBOLISM; DERMATOLOGY; IMMUNOLOGY;

ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIBODIES, NEUTRALIZING; BIOLOGICAL PRODUCTS; DERMATOLOGY; EPITOPES; HUMANS; PSORIASIS;

EID: 84925230736     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2014.295     Document Type: Review

References (84)

1. Adişen E, Aral A, Aybay C et al. (2010) Anti-infliximab antibody status and its relation to clinical response in psoriatic patients: a pilot study. J Dermatol 37:708-13
2. Anderson PJ (2005) Tumor necrosis factor inhibitors: clinical implications of their different immunogenicity profiles. Semin Arthritis Rheum 34(Suppl 1):19-22
3. Astermark J (2012) Prevention and prediction of inhibitor risk. Haemophilia 18(Suppl 4):38-42
4. Baert F, Noman M, Vermeire S et al. (2003) Influence of immunogenicity on the long-term efficacy of infliximab in Crohn's disease. N Engl J Med 348:601-8
5. Bartelds GM, de Groot E, Nurmohamed MT et al. (2010) Surprising negative association between IgG1 allotype disparity and anti-adalimumab formation: a cohort study. Arthritis Res Ther 12:R221
6. Bartelds GM, Krieckaert CL, Nurmohamed MT et al. (2011) Development of antidrug antibodies against adalimumab and association with disease activity and treatment failure during long-term follow-up. JAMA 305:1460-8
7. Bavbek S, Aydn O, Ataman S et al. (2011) Injection-site reaction to etanercept: role of skin test in the diagnosis of such reaction and successful desensitization. Allergy 66:1256-7
8. Ben-Horin S, Waterman M, Kopylov U et al. (2013) Addition of an immunomodulator to infliximab therapy eliminates antidrug antibodies in serum and restores clinical response of patients with inflammatory bowel disease. Clin Gastroenterol Hepatol 11:444-7
9. Bendtzen K, Geborek P, Svenson M et al. (2006) Individualized monitoring of drug bioavailability and immunogenicity in rheumatoid arthritis patients treated with the tumor necrosis factor alpha inhibitor infliximab. Arthritis Rheum 54:3782-9
10. Brinks V, Weinbuch D, Baker M et al. (2013) Preclinical models used for immunogenicity prediction of therapeutic proteins. Pharm Res 30:1719-28
11. Burmester GR, Rubbert-Roth A, Cantagrel A et al. (2014) A randomised, double-blind, parallel-group study of the safety and efficacy of subcutaneous tocilizumab versus intravenous tocilizumab in combination with traditional disease-modifying antirheumatic drugs in patients with moderate to severe rheumatoid arthritis (SUMMACTA study). Ann Rheum Dis 73:69-74
12. Cantini F, Niccoli L, Nannini C et al. (2008) Frequency and duration of clinical remission in patients with peripheral psoriatic arthritis requiring secondline drugs. Rheumatology 47:872-6
13. Cassinotti A, Travis S (2009) Incidence and clinical significance of immunogenicity to infliximab in Crohn's disease: a critical systematic review. Inflamm Bowel Dis 15:1264-75
14. Chen DY, Chen YM, Tsai WC et al. (2014) Significant associations of antidrug antibody levels with serum drug trough levels and therapeutic response of adalimumab and etanercept treatment in rheumatoid arthritis. Ann Rheum Dis; e-pub ahead of print 17 January 2014
15. Chirmule N, Jawa V, Meibohm B (2012) Immunogenicity to therapeutic proteins: impact on PK/PD and efficacy. AAPS J 14:296-302
16. Christen U, Thuerkauf R, Stevens R et al. (1999) Immune response to a recombinant human TNFR55-IgG1 fusion protein: auto-antibodies in rheumatoid arthritis (RA) and multiple sclerosis (MS) patients have neither neutralizing nor agonist activities. Hum Immunol 60: 774-90
17. Clark M (2000) Antibody humanization: a case of the 'Emperor's new clothes'? Immunol Today 21:397-402
18. Dervieux T, Weinblatt ME, Kivitz A et al. (2013) Methotrexate polyglutamation in relation to infliximab pharmacokinetics in rheumatoid arthritis. Ann Rheum Dis 72:908-10
19. Ducourau E, Mulleman D, Paintaud G et al. (2011) Antibodies toward infliximab are associated with low infliximab concentration at treatment initiation and poor infliximab maintenance in rheumatic diseases. Arthritis Res Ther 13:R105
20. Emi Aikawa N, de Carvalho JF, Artur Almeida Silva C et al. (2010) Immunogenicity of anti-TNF-a agents in autoimmune diseases. Clin Rev Allergy Immunol 38:82-9
21. Enbrel (etanercept), Pfizer Inc Summary of Product Characteristics October 2013
22. Esposito M, Gisondi P, Cassano N et al. (2013) Survival rate of anti-TNF alpha treatments for psoriasis in routine dermatological practice: a multicenter observational study. Br J Dermatol 169:666-72
23. European Medicines Agency (2006) Guideline on similar biological medicinal products containing biotechnology-derived proteins as active substance: Non-clinical and clinical issues. EMEA: London (http://www.ema. europa.eu/docs/en-GB/document-library/Scientific-guideline/2009/09/ WC500003920.pdf)
24. European Medicines Agency (2007) Guideline on immunogenicity assessment of biotechnology-derived therapeutic proteins. EMEA: London (http:// www.ema.europa.eu/docs/en-GB/document-library/Scientific-guideline/ 2009/09/WC500003946.pdf)
25. European Medicines Agency (2012) Guideline on similar biological medicinal products containing monoclonal antibodies-non-clinical and clinical issues. EMEA: London (http://www.ema.europa.eu/docs/en-GB/ document-library/Scientific-guideline/2012/06/WC500128686.pdf)
26. Food and Drug Administration (2013) Immunogenicity assessment for therapeutic protein products. FDA: Rockville, MD (http://www.fda.gov/ downloads/Drugs/GuidanceComplianceRegulatoryInformation/Guidances/ UCM338856.pdf)
27. Garcês S, Demengeot J, Benito-Garcia E (2013) The immunogenicity of anti-TNF therapy in immune-mediated inflammatory diseases: a systematic review of the literature with a meta-analysis. Ann Rheum Dis 72: 1947-55
28. Garman RD, Munroe K, Richards SM (2004) Methotrexate reduces antibody responses to recombinant human a-galactosidase A therapy in a mouse model of Fabry disease. Clin Exp Immunol 137:496-502
29. Gniadecki R, Kragballe K, Dam TN et al. (2011) Comparison of drug survival rates for adalimumab, etanercept and infliximab in patients with psoriasis vulgaris. Br J Dermatol 164:1091-6
30. Gordon KB, Gottlieb AB, Leonardi CL et al. (2006) Clinical response in psoriasis patients discontinued from and then reinitiated on etanercept therapy. J Dermatolog Treat 17:9-17
31. Gottlieb AB, Evans R, Li S et al. (2004) Infliximab induction therapy for patients with severe plaque-type psoriasis: a randomized, double-blind, placebocontrolled trial. J Am Acad Dermatol 51:534-42
32. Hall J, Findeisen J (2013) Successful etanercept desensitization in a patient with severe injection site reactions. J Clin Rheumatol 19:407-8
33. Harris JM, Martin NE, Modi M (2001) Pegylation: a novel process for modifying pharmacokinetics. Clin Pharmacokinet 40:539-51
34. Hart MH, de Vrieze H, Wouters D et al. (2011) Differential effect of drug interference in immunogenicity assays. J Immunol Methods 372:196-203
35. Hoffmann JH, Hartmann M, Enk AH et al. (2011) Autoantibodies in psoriasis as predictors for loss of response and anti-infliximab antibody induction. Br J Dermatol 165:1355-8
36. Hong DI, Bankova L, Cahill KN et al. (2012) Allergy to monoclonal antibodies: cutting-edge desensitization methods for cutting-edge therapies. Expert Rev Clin Immunol 8:43-52
37. Hsu L, Armstrong AW (2013) Anti-drug antibodies in psoriasis: a critical evaluation of clinical significance and impact on treatment response. Expert Rev Clin Immunol 9:949-58
38. Hsu L, Snodgrass BT, Armstrong AW (2014) Anti-drug antibodies in psoriasis: a systematic review. Br J Dermatol 170:261-73
39. Humira (adalimumab), AbbVie Summary of Product Characteristics September 2013
40. Jamnitski A, Bartelds GM, Nurmohamed MT et al. (2011) The presence or absence of antibodies to infliximab or adalimumab determines the outcome of switching to etanercept. Ann Rheum Dis 70:284-8
41. Jani M, Barton A, Warren RB et al. (2014) The role of DMARDs in reducing the immunogenicity of TNF inhibitors in chronic inflammatory diseases. Rheumatology (Oxford) 53:213-22
42. Joseph A, Munroe K, Housman M et al. (2008) Immune tolerance induction to enzyme-replacement therapy by co-administration of short-term, lowdose methotrexate in a murine Pompe disease model. Clin Exp Immunol 152:138-46
43. Joseph A, Neff K, Richard J et al. (2012) Transient low-dose methotrexate induces tolerance to murine anti-thymocyte globulin and together they promote long-term allograft survival. J Immunol 189:732-43
44. Jullien D (2012) [Anti-drug antibodies, auto-antibodies and biotherapy in psoriasis]. Ann Dermatol Venereol 139(Suppl 2):S58-67
45. Koo J, Lebwohl M (1999) Duration of remission of psoriasis therapies. Am Acad Dermatol 41:51-9
46. Korswagen LA, Bertelds GM, Krieckaert CLM et al. (2011) Venous and arterial thromboembolic events in adalimumab-treated patients with antiadalimumab antibodies. Arthritis Rheum 63:877-83
47. Krieckaert C, Rispens T, Wolbink G (2012a) Immunogenicity of biological therapeutics: from assay to patient. Curr Opin Rheumatol 24:306-11
48. Krieckaert CL, Nurmohamed MT, Wolbink GJ (2012b) Methotrexate reduces immunogenicity in adalimumab treated rheumatoid arthritis patients in a dose dependent manner. Ann Rheum Dis 71:1914-5
49. Lecluse LL, Driessen RJ, Spuls PI et al. (2010) Extent and clinical consequences of antibody formation against adalimumab in patients with plaque psoriasis. Arch Dermatol 146:127-32
50. Maini RN, Breedveld FC, Kalden JR et al. (1998) Therapeutic efficacy of multiple intravenous infusions of anti-tumor necrosis factor alpha monoclonal antibody combined with low-dose weekly methotrexate in rheumatoid arthritis. Arthritis Rheum 41:1552-63
51. Mehren CR, Gniadecki R (2012) Dose-creep of Infliximab during psoriasis treatment: an observational study. Acta Derm Venereol 92:355-7
52. Menter A, Feldman SR, Weinstein GD et al. (2007) A randomized comparison of continuous vs. intermittent infliximab maintenance regimens over 1 year in the treatment of moderate-to-severe plaque psoriasis. J Am Acad Dermatol 56:e1-15
53. Menter A, Tyring SK, Gordon K et al. (2008) Adalimumab therapy for moderate to severe psoriasis: a randomized, controlled phase III trial. J Am Acad Dermatol 58:106-15
54. Menting SP, van Lümig PP, de Vries AC et al. (2014) Extent and consequences of antibody formation against adalimumab in patients with psoriasis: oneyear follow-up. JAMA Dermatol 150:130-6
55. Meyer MW, Zachariae C, Bendtzen K et al. (2012) Lack of anti-drug antibodies in patients with psoriasis well-controlled on long-term treatment with tumour necrosis factor inhibitors. Acta Derm Venereol 92:362-4
56. Nast A, Boehncke WH, Mrowietz U et al. (2012) S3-Guidelines on the treatment of psoriasis vulgaris (English version). Update. J Dtsch Dermatol Ges 10(Suppl 2):S1-95
57. Noiles K, Vender R (2009) Biologic survival. J Drugs Dermatol 8:329-33
58. Ortonne J-P, Griffiths C, Daudén E et al. (2008) Efficacy and safety of continuous versus paused etanercept treatment in patients with moderate-tosevere psoriasis over 54 weeks: the CRYSTEL study. Expert Rev Dermatol 3:657-65
59. Papp K, Crowley J, Ortonne JP et al. (2011) Adalimumab for moderate to severe chronic plaque psoriasis: efficacy and safety of retreatment and disease recurrence following withdrawal from therapy. Br J Dermatol 164:434-41
60. Parenky A, Myler H, Amaravadi L et al. (2014) New FDA draft guidance on immunogenicity. AAPS J 16:499-503
61. Park W, Hrycaj P, Jeka S et al. (2013) A randomised, double-blind, multicentre, parallel-group, prospective study comparing the pharmacokinetics, safety, and efficacy of CT-P13 and innovator infliximab in patients with ankylosing spondylitis: the PLANETAS study. Ann Rheum Dis 72: 1605-12
62. Pink AE, Fonia A, Allen MH et al. (2010) Antinuclear antibodies associate with loss of response to antitumour necrosis factor-alpha therapy in psoriasis: a retrospective, observational study. Br J Dermatol 162:780-5
63. Plasencia C, Pascual-Salcedo D, Nuño L et al. (2012) Influence of immunogenicity on the efficacy of longterm treatment of spondyloarthritis with infliximab. Ann Rheum Dis 71:1955-60
64. Radstake TR, Svenson M, Eijsbouts AM et al. (2009) Formation of antibodies against infliximab and adalimumab strongly correlates with functional drug levels and clinical responses in rheumatoid arthritis. Ann Rheum Dis 68:1739-45
65. Reich K, Nestle FO, Papp K et al. (2005) Infliximab induction and maintenance therapy for moderate-to-severe psoriasis: a phase III, multicentre, doubleblind trial. Lancet 366:1367-74
66. Rispens T, Hart MH, Ooijevaar-de Heer P et al. (2013) Drug interference in immunogenicity assays depends on valency. J Pharm Biomed Anal 85:179-85
67. Rojas JR, Taylor RP, Cunningham MR et al. (2005) Formation, distribution, and elimination of infliximab and anti-infliximab immune complexes in cynomolgus monkeys. J Pharmacol Exp Ther 313:578-85
68. Schellekens H (2002) Immunogenicity of therapeutic proteins: clinical implications and future prospects. Clin Ther 24:1720-40
69. Schellekens H, Hennink WE, Brinks V (2013) The immunogenicity of polyethylene glycol: facts and fiction. Pharm Res 30:1729-34
70. Scott DW (2014) Inhibitors-cellular aspects and novel approaches for tolerance. Haemophilia 20(Suppl 4):80-6
71. Svenson M, Geborek P, Saxne T et al. (2007) Monitoring patients treated with anti-TNF-a biopharmaceuticals: assessing serum infliximab and antiinfliximab antibodies. Rheumatology (Oxford) 46:1828-34
72. Takahashi H, Tsuji H, Ishida-Yamamoto A et al. (2013) Plasma trough levels of adalimumab and infliximab in terms of clinical efficacy during the treatment of psoriasis. J Dermatol 40:39-42
73. Thalayasingam N, Isaacs JD (2011) Anti-TNF therapy. Best Pract Res Clin Rheumatol 25:549-67
74. Tsoi LC, Spain SL, Knight J et al. (2012) Identification of 15 new psoriasis susceptibility loci highlights the role of innate immunity. Nat Genet 44:1341-8
75. Tyring S, Gordon KB, Poulin Y et al. (2007) Long-term safety and efficacy of 50 mg of etanercept twice weekly in patients with psoriasis. Arch Dermatol 143:719-26
76. van der Laken CJ, Voskuyl AE, Roos JC (2007) Imaging and serum analysis of immune complex formation of radiolabelled infliximab and antiinfliximab in responders and non-responders to therapy for rheumatoid arthritis. Ann Rheum Dis 66:253-6
77. van Schouwenburg PA, Bartelds GM, Hart MH et al. (2010) A novel method for the detection of antibodies to adalimumab in the presence of drug reveals "hidden" immunogenicity in rheumatoid arthritis patients. J Immunol Methods 362:82-8
78. van Schouwenburg PA, Krieckaert CL, Nurmohamed M et al. (2012) IgG4 production against adalimumab during long term treatment of RA patients. J Clin Immunol 32:1000-6
79. van Schouwenburg PA, Rispens T, Wolbink GJ (2013) Immunogenicity of anti-TNF biologic therapies for rheumatoid arthritis. Nat Rev Rheumatol 9:164-72
80. Vincent FB, Morand EF, Murphy K et al. (2013) Antidrug antibodies (ADAb) to tumour necrosis factor (TNF)-specific neutralising agents in chronic inflammatory diseases: a real issue, a clinical perspective. Ann Rheum Dis 72:165-78
81. Wolbink GJ, Aarden LA, Dijkmans BA (2009) Dealing with immunogenicity of biologicals: assessment and clinical relevance. Curr Opin Rheumatol 21:211-5
82. Xue L, Rup B (2013) Evaluation of pre-existing antibody presence as a risk factor for posttreatment anti-drug antibody induction: analysis of human clinical study data for multiple biotherapeutics. AAPS J 15:893-6
83. Yanover C, Jain N, Pierce G et al. (2011) Pharmacogenetics and the immunogenicity of protein therapeutics. Nat Biotechnol 29:870-3
84. Zhu Y, Shankar G, Yeilding N et al. (2010) Immunogenicity assessment of ustekinumab in Phase 3 studies in patients with moderate to severe plaque psoriasis. 19th Annual Congress of the European Academy of Dermatology and Venereology; 6-10 October 2010; Gothenburg, p563