Engineered binding to erythrocytes induces immunological tolerance to E. coli asparaginase

Science Advances

Volumn 1, Issue 6, 2015, Pages

  Lorentz, Kristen M ^a,b   Kontos, Stephan ^a,b   Diaceri, Giacomo ^a   Henry, Hugues ^c   Hubbell, Jeffrey A ^a,b,d,e  

^a EPFL   (Switzerland)

^b Anokion SA   (Switzerland)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^d UNIVERSITY OF CHICAGO   (United States)

^e ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGENS; BINS; BLOOD; CELL ENGINEERING; ENZYMES; ESCHERICHIA COLI; MAMMALS; PROTEINS;

CLINICAL COMPLICATIONS; DRUG CANDIDATES; HUMORAL IMMUNE RESPONSE; IMMUNE RESPONSE; THERAPEUTIC ENZYME; THERAPEUTIC PROTEIN; TOLERANCE INDUCTIONS; WILD-TYPE ENZYMES;

IMMUNE SYSTEM;

EID: 84936809151     PISSN: None     EISSN: 23752548     Source Type: Journal    
DOI: 10.1126/sciadv.1500112     Document Type: Article

References (36)

1. A. Nechansky, R. Kircheis, Immunogenicity of therapeutics: A matter of efficacy and safety. Expert Opin. Drug Discov. 5, 1067–1079 (2010).
2. M. P. Baker, H. M. Reynolds, B. Lumicisi, C. J. Bryson, Immunogenicity of protein therapeutics: The key causes, consequences and challenges. Self Nonself 1, 314–322 (2010).
3. M. S. Joly, R. P. Martin, S. Mitra-Kaushik, L. Phillips, A. D’Angona, S. M. Richards, A. M. Joseph, Transient low-dose methotrexate generates B regulatory cells that mediate antigen-specific tolerance to alglucosidase a. J. Immunol. 193, 3947–3958 (2014).
4. S. G. Banugaria, S. N. Prater, J. K. McGann, J. D. Feldman, J. A. Tannenbaum, C. Bailey, R. Gera, R. L. Conway, D. Viskochil, J. A. Kobori, A. S. Rosenberg, P. S. Kishnani, Bortezomib in the rapid reduction of high sustained antibody titers in disorders treated with therapeutic protein: Lessons learned from Pompe disease. Genet. Med. 15, 123–131 (2013).
5. R. P. Garay, R. El-Gewely, J. K. Armstrong, G. Garratty, P. Richette, Antibodies against polyethylene glycol in healthy subjects and in patients treated with PEG-conjugated agents. Expert Opin. Drug Deliv. 9, 1319–1323 (2012).
6. J. K. Armstrong, G. Hempel, S. Koling, L. S. Chan, T. Fisher, H. J. Meiselman, G. Garratty, Antibody against poly(ethylene glycol) adversely affects PEG-asparaginase therapy in acute lymphoblastic leukemia patients. Cancer 110, 103–111 (2007).
7. M. S. Hershfield, N. J. Ganson, S. J. Kelly, E. L. Scarlett, D. A. Jaggers, J. S. Sundy, Induced and pre-existing anti-polyethylene glycol antibody in a trial of every 3-week dosing of pegloti-case for refractory gout, including in organ transplant recipients. Arthritis Res. Ther. 16, R63 (2014).
8. A. S. De Groot, W. D. Martin, Reducing risk, improving outcomes: Bioengineering less immunogenic protein therapeutics. Clin. Immunol. 131, 189–201 (2009).
9. L. Moise, C. Song, W. D. Martin, R. Tassone, A. S. De Groot, D. W. Scott, Effect of HLA DR epitope deimmunization of Factor VIII in vitro and in vivo. Clin. Immunol. 142, 320–331 (2012).
10. A. S. Parker, Y. Choi, K. E. Griswold, C. Bailey-Kellogg, Structure-guided deimmunization of therapeutic proteins. J. Comput. Biol. 20, 152–165 (2013).
11. W. Liu, M. Onda, B. Lee, R. J. Kreitman, R. Hassan, L. Xiang, I. Pastan, Recombinant immu-notoxin engineered for low immunogenicity and antigenicity by identifying and silencing human B-cell epitopes. Proc. Natl. Acad. Sci. U.S.A. 109, 11782–11787 (2012).
12. J. R. Cantor, V. Panayiotou, G. Agnello, G. Georgiou, E. M. Stone, Engineering reduced-immunogenicity enzymes for amino acid depletion therapy in cancer. Methods Enzymol. 502, 291–319 (2012).
13. D. R. Green, T. Ferguson, L. Zitvogel, G. Kroemer, Immunogenic and tolerogenic cell death. Nat. Rev. Immunol. 9, 353–363 (2009).
14. T. S. Griffith, T. A. Ferguson, Cell death in the maintenance and abrogation of tolerance: The five Ws of dying cells. Immunity 35, 456–466 (2011).
15. S. Kontos, I. C. Kourtis, K. Y. Dane, J. A. Hubbell, Engineering antigens for in situ erythrocyte binding induces T-cell deletion. Proc. Natl. Acad. Sci. U.S.A. 110, E60–E68 (2013).
16. E. H. Panosyan, N. L. Seibel, S. Martin-Aragon, P. S. Gaynon, I. A. Avramis, H. Sather, J. Franklin, J. Nachman, L. J. Ettinger, M. La, P. Steinherz, L. J. Cohen, S. E. Siegel, V. I. Avramis, Children’s Cancer Group Study CCG-1961, Asparaginase antibody and asparaginase activity in children with higher-risk acute lymphoblastic leukemia: Children’s Cancer Group Study CCG-1961. J. Pediatr. Hematol. Oncol. 26, 217–226 (2004).
17. V. I. Avramis, E. V. Avramis, W. Hunter, M. C. Long, Immunogenicity of native or pegylated E. coli and Erwinia asparaginases assessed by ELISA and surface plasmon resonance (SPR-biacore) assays of IgG antibodies (Ab) in sera from patients with acute lymphoblastic leukemia (ALL). Anticancer Res. 29, 299–302 (2009).
18. H. F. Oettgen, P. A. Stephenson, M. K. Schwartz, R. D. Leeper, L. Tallai, C. C. Tan, B. D. Clarkson, R. B. Golbey, I. H. Krakoff, D. A. Karnofsky, M. L. Murphy, J. H. Burchenal, Toxicity of E. coli L-asparaginase in man. Cancer 25, 253–278 (1970).
19. S. Kontos, J. A. Hubbell, Improving protein pharmacokinetics by engineering erythrocyte affinity. Mol. Pharm. 7, 2141–2147 (2010).
20. U. K. Narta, S. S. Kanwar, W. Azmi, Pharmacological and clinical evaluation of L-asparaginase in the treatment of leukemia. Crit. Rev. Oncol. Hematol. 61, 208–221 (2007).
21. W.-W. Chien, S. Allas, N. Rachinel, P. Sahakian, M. Julien, C. Le Beux, C.-E. Lacroix, T. Abribat, G. Salles, Pharmacology, immunogenicity, and efficacy of a novel pegylated recombinant Erwinia chrysanthemi-derived L-asparaginase. Invest. New Drugs 32, 795–805 (2014).
22. C. Rizzari, Shedding light on the asparaginase galaxy. Blood 123, 1976–1978 (2014).
23. F. Nimmerjahn, P. Bruhns, K. Horiuchi, J. V. Ravetch, FcgRIV: A novel FcR with distinct IgG subclass specificity. Immunity 23, 41–51 (2005).
24. P. Bruhns, Properties of mouse and human IgG receptors and their contribution to disease models. Blood 119, 5640–5649 (2012).
25. C. M. Snapper, T. M. McIntyre, R. Mandler, L. M. Pecanha, F. D. Finkelman, A. Lees, J. J. Mond, Induction of IgG3 secretion by interferon g: A model for T cell–independent class switching in response to T cell–independent type 2 antigens. J. Exp. Med. 175, 1367–1371 (1992).
26. J. Nikolich-Žugich, Aging of the T cell compartment in mice and humans: From no naive expectations to foggy memories. J. Immunol. 193, 2622–2629 (2014).
27. C. Domenech, X. Thomas, S. Chabaud, A. Baruchel, F. Gueyffier, F. Mazingue, A. Auvrignon, S. Corm, H. Dombret, P. Chevallier, C. Galambrun, F. Huguet, F. Legrand, F. Mechinaud, N. Vey, I. Philip, D. Liens, Y. Godfrin, D. Rigal, Y. Bertrand, L-Asparaginase loaded red blood cells in refractory or relapsing acute lymphoblastic leukaemia in children and adults: Results of the GRASPALL 2005-01 randomized trial. Br. J. Haematol. 153, 58–65 (2011).
28. S. Vadlamudi, M. Padarathsingh, V. S. Waravdekar, A. Goldin, Factors influencing the therapeutic activity of L-asparaginase (NSC 109229) in leukemic (L5178Y) mice. Cancer Res. 30, 1467–1472 (1970).
29. P. Gaitonde, A. Peng, R. M. Straubinger, R. B. Bankert, S. V. Balu-Iyer, Phosphatidylserine reduces immune response against human recombinant Factor VIII in Hemophilia A mice by regulation of dendritic cell function. Clin. Immunol. 138, 135–145 (2011).
30. M. S. Macauley, F. Pfrengle, C. Rademacher, C. M. Nycholat, A. J. Gale, A. von Drygalski, J. C. Paulson, Antigenic liposomes displaying CD22 ligands induce antigen-specific B cell apoptosis. J. Clin. Invest. 123, 3074–3083 (2013).
31. + and IL-10–producing splenic macrophages and maintained by T regulatory cells. J. Immunol. 187, 2405–2417 (2011).
32. A. Lutterotti, S. Yousef, A. Sputtek, K. H. Stürner, J.-P. Stellmann, P. Breiden, S. Reinhardt, C. Schulze, M. Bester, C. Heesen, S. Schippling, S. D. Miller, M. Sospedra, R. Martin, Antigen-specific tolerance by autologous myelin peptide-coupled cells: A phase 1 trial in multiple sclerosis. Sci. Transl. Med. 5, 188ra75 (2013).
33. S. Kasagi, P. Zhang, L. Che, B. Abbatiello, T. Maruyama, H. Nakatsukasa, P. Zanvit, W. Jin, J. E. Konkel, W. Chen, In vivo-generated antigen-specific regulatory T cells treat autoimmunity without compromising antibacterial immune response. Sci. Transl. Med. 6, 241ra78 (2014).
34. B. K. Albertsen, H. Schrøder, P. Jakobsen, V. I. Avramis, H.-J. Müller, K. Schmiegelow, N. T. Carlsen, Antibody formation during intravenous and intramuscular therapy with Erwinia asparaginase. Med. Pediatr. Oncol. 38, 310–316 (2002).
35. M. P. Lutolf, N. Tirelli, S. Cerritelli, L. Cavalli, J. A. Hubbell, Systematic modulation of Michael-type reactivity of thiols through the use of charged amino acids. Bioconjug. Chem. 12, 1051–1056 (2001).
36. S. Rivera, F. J. López-Soriano, J. Azcón-Bieto, J. M. Argilés, Blood amino acid compartmentation in mice bearing Lewis lung carcinoma. Cancer Res. 47, 5644–5646 (1987).