Development of a hypoallergenic recombinant parvalbumin for first-in-man subcutaneous immunotherapy of fish allergy

International Archives of Allergy and Immunology

Volumn 166, Issue 1, 2015, Pages 41-51

  Zuidmeer Jongejan, Laurian ^a   Huber, Hans ^b   Swoboda, Ines ^c   Rigby, Neil ^d   Versteeg, Serge A ^a   Jensen, Bettina M ^e   Quaak, Suzanne ^f   Akkerdaas, Jaap H ^a   Blom, Lars ^e   Asturias, Juan ^g   Bindslev Jensen, Carsten ^h   Bernardi, Maria L ^i,k   Clausen, Michael ^j   Ferrara, Rosa ^i,k   Hauer, Martina ^b   Heyse, Jet ^f   Kopp, Stephan ^b   Kowalski, Marek L ^l   Lewandowska Polak, Anna ^l   Linhart, Birgit ^c   Maderegger, Bernhard ^b   Maillere, Bernard ^m   Mari, Adriano ^i,k   Martinez, Alberto ^g   Mills, E N Clare ^d,n   Neubauer, Angela ^b   Nicoletti, Claudio ^d   Papadopoulos, Nikolaos G ^o   Portoles, Antonio ^p   Ranta Panula, Ville ^r   Santos Magadan, Sara ^q   Schnoor, Heidi J ^e   Sigurdardottir, Sigurveig T ⁱ   Stahl Skov, Per ^s   Stavroulakis, George ^o   Stegfellner, Georg ^b   Vázquez Cortés, Sonia ^q   Witten, Marianne ^e   Stolz, Frank ^b   Poulsen, Lars K ^e   Fernandez Rivas, Montserrat ^q   Valenta, Rudolf ^c   Van Ree, Ronald ^a   more..

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b BIOMAY AG   (Austria)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

^d INSTITUTE OF FOOD RESEARCH   (United Kingdom)

^e GENTOFTE UNIVERSITY HOSPITAL   (Denmark)

^f HAL Allergy BV   (Netherlands)

^g R and D Department   (Spain)

^h ODENSE UNIVERSITY HOSPITAL   (Denmark)

ⁱ LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

^j LANDSPITALI UNIVERSITY HOSPITAL   (Iceland)

^k Associ Centers for Molecular Allergology CAAM   (Italy)

^l MEDICAL UNIVERSITY OF LODZ   (Poland)

^m DIF   (France)

ⁿ UNIVERSITY OF MANCHESTER   (United Kingdom)

^o UNIVERSITY OF ATHENS   (Greece)

^p Departments of Clinical Pharmacology   (United States)

^q HOSPITAL CLÍNICO SAN CARLOS   (Spain)

^r UNIVERSITY OF TURKU   (Finland)

^s RefLab ApS   (Denmark)

more..

Author keywords

Allergen mutants; Carp; Cyprinus carpio; FAST; Fish; Food allergy; Immunotherapy; Parvalbumin; Recombinant hypoallergenic allergens; Toxicity

Indexed keywords

ALUMINUM HYDROXIDE; GUANOSINE PHOSPHATE; IMMUNOGLOBULIN G ANTIBODY; PARVALBUMIN; PLACEBO; ALLERGEN; CALCIUM BINDING PROTEIN; CYP C 1.01 PROTEIN, CARP; FISH PROTEIN; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; RECOMBINANT PROTEIN;

ACUTE TOXICITY; ADJUVANT THERAPY; ALLERGENICITY; ALLERGY RAPID TEST; BASOPHIL HISTAMINE RELEASE ASSAY; CARP; CIRCULAR DICHROISM; CONTROLLED STUDY; ESCHERICHIA COLI; EXPERIMENTAL RABBIT; FEMALE; FISH ALLERGY; FOOD ALLERGY; GEL ELECTROPHORESIS; GEL PERMEATION CHROMATOGRAPHY; GOOD MANUFACTURING PRACTICE; HISTAMINE RELEASE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; MALE; MASS SPECTROMETRY; MOUSE; NONHUMAN; PATIENT; PERIPHERAL BLOOD MONONUCLEAR CELL; PHYSICAL CHEMISTRY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; RELEASE ASSAY; REPEATED DRUG DOSE; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; REVIEW; SUBCUTANEOUS IMMUNOTHERAPY; ANIMAL; BLOOD; CHEMISTRY; CLINICAL TRIAL; DESENSITIZATION; DOUBLE BLIND PROCEDURE; FOOD HYPERSENSITIVITY; GENE EXPRESSION; GENETICS; IMMUNOLOGY; LD50; METABOLISM; MONONUCLEAR CELL; MULTICENTER STUDY; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; PROTEIN FOLDING; PROTEIN STABILITY; RABBIT; RANDOMIZED CONTROLLED TRIAL; SUBCUTANEOUS DRUG ADMINISTRATION;

ALLERGENS; ANIMALS; CALCIUM-BINDING PROTEINS; CARPS; DESENSITIZATION, IMMUNOLOGIC; DOUBLE-BLIND METHOD; ESCHERICHIA COLI; FEMALE; FISH PROTEINS; FOOD HYPERSENSITIVITY; GENE EXPRESSION; HUMANS; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; INJECTIONS, SUBCUTANEOUS; LETHAL DOSE 50; LEUKOCYTES, MONONUCLEAR; MALE; MICE; PARVALBUMINS; PROTEIN FOLDING; PROTEIN STABILITY; RABBITS; RECOMBINANT PROTEINS;

EID: 84924689954     PISSN: 10182438     EISSN: 14230097     Source Type: Journal    
DOI: 10.1159/000371657     Document Type: Review

References (48)

1. Sharp MF, Lopata AL: Fish allergy: in review. Clin Rev Allergy Immunol 2014; 46:258-271.
2. Lopata AL, Lehrer SB: New insights into seafood allergy. Curr Opin Allergy Clin Immunol 2009; 9:270-277.
3. Narisety SD, Keet CA: Sublingual vs oral im-munotherapy for food allergy: identifying the right approach. Drugs 2012; 72:1977-1989.
4. Nelson HS, Lahr J, Rule R, Bock A, Leung D: Treatment of anaphylactic sensitivity to peanuts by immunotherapy with injections of aqueous peanut extract. J Allergy Clin Immunol 1997; 99:744-751.
5. Oppenheimer JJ, Nelson HS, Bock SA, Chris-tensen F, Leung DY: Treatment of peanut allergy with rush immunotherapy. J Allergy Clin Immunol 1992; 90:256-262.
6. Valenta R: The future of antigen-specific im-munotherapy of allergy. Nat Rev Immunol 2002; 2:446-453.
7. Zuidmeer-Jongejan L, Fernandez-Rivas M, Poulsen LK, Neubauer A, Asturias J, Blom L, Boye J, Bindslev-Jensen C, Clausen M, Ferr-ara R, Garosi P, Huber H, Jensen BM, Koppel-man S, Kowalski ML, Lewandowska-Polak A, Linhart B, Maillere B, Mari A, Martinez A, Mills CE, Nicoletti C, Opstelten DJ, Papado-poulos NG, Portoles A, Rigby N, Scala E, Schnoor HJ, Sigursdottir S, Stavroulakis G, Stolz F, Swoboda I, Valenta R, van den Hout R, Versteeg SA, Witten M, van Ree R: FAST: towards safe and effective subcutaneous im-munotherapy of persistent life-threatening food allergies. Clin Transl Allergy 2012; 2:5.
8. Swoboda I, Bugajska-Schretter A, Linhart B, Verdino P, Keller W, Schulmeister U, Sperr WR, Valent P, Peltre G, Quirce S, Douladiris N, Papadopoulos NG, Valenta R, Spitzauer S: A recombinant hypoallergenic parvalbumin mutant for immunotherapy of IgE-mediated fish allergy. J Immunol 2007; 178:6290-6296.
9. Griesmeier U, Vazquez-Cortes S, Bublin M, Radauer C, Ma Y, Briza P, Fernandez-Rivas M, Breiteneder H: Expression levels of parv-albumins determine allergenicity of fish species. Allergy 2010; 65:191-198.
10. Van Do T, Elsayed S, Florvaag E, Hordvik I, Endresen C: Allergy to fish parvalbumins: studies on the cross-reactivity of allergens from 9 commonly consumed fish. J Allergy Clin Immunol 2005; 116:1314-1320.
11. Elsayed S, Apold J: Immunochemical analysis of cod fish allergen M: locations of the immu-noglobulin binding sites as demonstrated by the native and synthetic peptides. Allergy 1983; 38:449-459.
12. Aas K, Jebsen JW: Studies of hypersensitivity to fish. Partial purification and crystallization of a major allergenic component of cod. Int Arch Allergy Appl Immunol 1967; 32:1-20.
13. Berchtold MW: Structure and expression of genes encoding the three-domain Ca2+-bind-ing proteins parvalbumin and oncomodulin. Biochim Biophys Acta 1989; 1009:201-215.
14. Heizmann CW, Hunziker W: Intracellular calcium-binding proteins: more sites than insights. Trends Biochem Sci 1991; 16:98-103.
15. Ikura M: Calcium binding and conformation-al response in EF-hand proteins. Trends Bio-chem Sci 1996; 21:14-17.
16. Bugajska-Schretter A, Elfman L, Fuchs T, Kapiotis S, Rumpold H, Valenta R, Spitzauer S: Parvalbumin, a cross-reactive fish allergen, contains IgE-binding epitopes sensitive to periodate treatment and Ca2+ depletion. J Allergy Clin Immunol 1998; 101:67-74.
17. Swoboda I, Bugajska-Schretter A, Verdino P, Keller W, Sperr WR, Valent P, Valenta R, Spitzauer S: Recombinant carp parvalbumin, the major cross-reactive fish allergen: a tool for diagnosis and therapy of fish allergy. J Immunol 2002; 168:4576-4584.
18. Bugajska-Schretter A, Grote M, Vangelista L, Valent P, Sperr WR, Rumpold H, Pastore A, Reichelt R, Valenta R, Spitzauer S: Purification, biochemical, and immunological characterisation of a major food allergen: different immunoglobulin E recognition of the apo-and calcium-bound forms of carp parvalbu-min. Gut 2000; 46:661-669.
19. Skov PS, Pelck I, Ebbesen F, Poulsen LK: Hy-persensitivity to the diphtheria component in the Di-Te-Pol vaccine. A type I allergic reaction demonstrated by basophil histamine release. Pediatr Allergy Immunol 1997; 8: 156-158.
20. Linhart B, Bigenzahn S, Hartl A, Lupinek C, Thalhamer J, Valenta R, Wekerle T: Costimu-lation blockade inhibits allergic sensitization but does not affect established allergy in a mu-rine model of grass pollen allergy. J Immunol 2007; 178:3924-3931.
21. Parish CR, Glidden MH, Quah BJ, Warren HS: Use of the intracellular fluorescent dye CFSE to monitor lymphocyte migration and proliferation. Curr Protoc Immunol 2009;chapt 4:unit4.9, DOI: 10.1002/0471142735.im0409s84.
22. Clark AT, Islam S, King Y, Deighton J, Anag-nostou K, Ewan PW: Successful oral tolerance induction in severe peanut allergy. Allergy 2009; 64:1218-1220.
23. Keet CA, Frischmeyer-Guerrerio PA, Thyag-arajan A, Schroeder JT, Hamilton RG, Boden S, Steele P, Driggers S, Burks AW, Wood RA: The safety and efficacy of sublingual and oral immunotherapy for milk allergy. J Allergy Clin Immunol 2012; 129:448.e5-455.e5.
24. Varshney P, Jones SM, Scurlock AM, Perry TT, Kemper A, Steele P, Hiegel A, Kamilaris J, Carlisle S, Yue X, Kulis M, Pons L, Vickery B, Burks AW: A randomized controlled study of peanut oral immunotherapy: clinical desensitization and modulation of the allergic response. J Allergy Clin Immunol 2011; 127: 654-660.
25. Anagnostou K, Clark A, King Y, Islam S, Deighton J, Ewan P: Efficacy and safety of high-dose peanut oral immunotherapy with factors predicting outcome. Clin Exp Allergy 2011; 41:1273-1281.
26. Burks AW, Jones SM, Wood RA, Fleischer DM, Sicherer SH, Lindblad RW, Stablein D, Hen-ning AK, Vickery BP, Liu AH, Scurlock AM, Shreffler WG, Plaut M, Sampson HA: Oral im-munotherapy for treatment of egg allergy in children. N Engl J Med 2012; 367: 233-243.
27. Dupont C, Kalach N, Soulaines P, Legoue-Morillon S, Piloquet H, Benhamou PH: Cow's milk epicutaneous immunotherapy in children: a pilot trial of safety, acceptability, and impact on allergic reactivity. J Allergy Clin Immunol 2010; 125:1165-1167.
28. Nouri-Aria KT, Wachholz PA, Francis JN, Ja-cobson MR, Walker SM, Wilcock LK, Staple SQ, Aalberse RC, Till SJ, Durham SR: Grass pollen immunotherapy induces mucosal and peripheral IL-10 responses and blocking IgG activity. J Immunol 2004; 172:3252-3259.
29. Plewako H, Wosinska K, Arvidsson M, Bjor-kander J, Hakansson L, Rak S: Production of interleukin-12 by monocytes and interferon-gamma by natural killer cells in allergic patients during rush immunotherapy. Ann Allergy Asthma Immunol 2006; 97:464-468.
30. Senti G, Johansen P, Martinez GJ, Prinz Var-icka BM, Kundig TM: Efficacy and safety of allergen-specific immunotherapy in rhinitis, rhinoconjunctivitis, and bee/wasp venom allergies. Int Rev Immunol 2005; 24:519-531.
31. Boyle RJ, Elremeli M, Hockenhull J, Cherry MG, Bulsara MK, Daniels M, Oude Elberink JN: Venom immunotherapy for preventing allergic reactions to insect stings. Cochrane Database Syst Rev 2012; 10:CD008838.
32. Durham SR, Walker SM, Varga EM, Jacobson MR, O'Brien F, Noble W, Till SJ, Hamid QA, Nouri-Aria KT: Long-term clinical efficacy of grass-pollen immunotherapy. N Engl J Med 1999; 341:468-475.
33. Kiel MA, Roder E, Gerth Van Wijk R, Al MJ, Hop WC, Rutten-van Mölken MP: Real-life compliance and persistence among users of subcutaneous and sublingual allergen immu-notherapy. J Allergy Clin Immunol 2013; 132: 353-360.
34. Brozek JL, Terracciano L, Hsu J, Kreis J, Com-palati E, Santesso N, Fiocchi A, Schunemann HJ: Oral immunotherapy for IgE-mediated cow's milk allergy: a systematic review and meta-analysis. Clin Exp Allergy 2012; 42:363-374.
35. Sheikh A, Nurmatov U, Venderbosch I, Bischoff E: Oral immunotherapy for the treatment of peanut allergy: systematic review of six case series studies. Prim Care Respir J 2012; 21:41-49.
36. Fisher HR, Du Toit G, Lack G: Specific oral tolerance induction in food allergic children: is oral desensitisation more effective than allergen avoidance?: a meta-analysis of published RCTs. Arch Dis Child 2011; 96:259-264.
37. Jutel M, Jaeger L, Suck R, Meyer H, Fiebig H, Cromwell O: Allergen-specific immunother-apy with recombinant grass pollen allergens. J Allergy Clin Immunol 2005; 116:608-613.
38. Niederberger V, Horak F, Vrtala S, Spitzauer S, Krauth MT, Valent P, Reisinger J, Pelz-mann M, Hayek B, Kronqvist M, Gafvelin G, Gronlund H, Purohit A, Suck R, Fiebig H, Cromwell O, Pauli G, van Hage-Hamsten M, Valenta R: Vaccination with genetically engineered allergens prevents progression of allergic disease. Proc Natl Acad Sci USA 2004; 101(suppl 2):14677-14682.
39. Pauli G, Larsen TH, Rak S, Horak F, Pastorel-lo E, Valenta R, Purohit A, Arvidsson M, Ka-vina A, Schroeder JW, Mothes N, Spitzauer S, Montagut A, Galvain S, Melac M, Andre C, Poulsen LK, Malling HJ: Efficacy of recombi-nant birch pollen vaccine for the treatment of birch-allergic rhinoconjunctivitis. J Allergy Clin Immunol 2008; 122:951-960.
40. Reisinger J, Horak F, Pauli G, van Hage M, Cromwell O, König F, Valenta R, Niederberg-er V: Allergen-specific nasal IgG antibodies induced by vaccination with genetically modified allergens are associated with reduced nasal allergen sensitivity. J Allergy Clin Immunol 2005; 116:347-354.
41. van der Ventel ML, Nieuwenhuizen NE, Kirstein F, Hikuam C, Jeebhay MF, Swoboda I, Brombacher F, Lopata AL: Differential responses to natural and recombinant allergens in a murine model of fish allergy. Mol Immunol 2011; 48:637-646.
42. Pree I, Shamji MH, Kimber I, Valenta R, Durham SR, Niederberger V: Inhibition of CD23-dependent facilitated allergen binding to B cells following vaccination with genetically modified hypoallergenic Bet v 1 molecules. Clin Exp Allergy 2010; 40:1346-1352.
43. Gafvelin G, Thunberg S, Kronqvist M, Gron-lund H, Gronneberg R, Troye-Blomberg M, Akdis M, Fiebig H, Purohit A, Horak F, Reis-inger J, Niederberger V, Akdis CA, Cromwell O, Pauli G, Valenta R, van Hage M: Cytokine and antibody responses in birch-pollen-allergic patients treated with genetically modified derivatives of the major birch pollen allergen Bet v 1. Int Arch Allergy Immunol 2005; 138: 59-66.
44. Burks AW, Calderon MA, Casale T, Cox L, Demoly P, Jutel M, Nelson H, Akdis CA: Update on allergy immunotherapy: American Academy of Allergy, Asthma & Immunology/European Academy of Allergy and Clinical Immunology/PRACTALL consensus report. J Allergy Clin Immunol 2013; 131:1288-1296.
45. Focke-Tejkl M, Valenta R: Safety of engineered allergen-specific immunotherapy vaccines. Curr Opin Allergy Clin Immunol 2012; 12:555-563.
46. Mackenzie KJ, Fitch PM, Leech MD, Ilch-mann A, Wilson C, McFarlane AJ, Howie SE, Anderton SM, Schwarze J: Combination peptide immunotherapy based on T-cell epitope mapping reduces allergen-specific IgE and eosinophilia in allergic airway inf lammation. Immunology 2013; 138: 258-268.
47. Guidance for Industry, Estimating the Maximum Safe, Starting Dose in Initial Clinical Trials for Therapeutics in Adult Healthy Volunteers. US Department of Health and Human Services, Food and Drug Administration, Center for Drug Evaluation and Research (CDER), 2005, pp 1-30, http://www. fda.gov/downloads/Drugs/Guidances/UCM078932.pdf.
48. Center for Drug Evaluation and Research, Center for Biologics Evaluation and Research: Estimating the Safe Starting Dose in Clinical Trials for Therapeutics in Adult Healthy Volunteers. Rockville, US Food & Drug Administration, 2002.