Factor H inhibits complement activation induced by liposomal and micellar drugs and the therapeutic antibody rituximab in vitro

Nanomedicine: Nanotechnology, Biology, and Medicine

Volumn 12, Issue 4, 2016, Pages 1023-1031

  Mészáros, Tamás ^a,b   Csincsi, Ádám I ^c   Uzonyi, Barbara ^d   Hebecker, Mario ^e   Fülöp, Tamás G ^a,b   Erdei, Anna ^c,d   Szebeni, János ^a,b   Józsi, Mihály ^c  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b SeroScience Ltd   (Hungary)

^c EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^d MTA ELTE Immunology Research Group Eötvös University   (Hungary)

^e HANS KNÖLL INSTITUTE   (Germany)

Author keywords

Complement; Factor H; Hypersensitivity; Nanomedicine; Pseudoallergy

Indexed keywords

MEDICAL NANOTECHNOLOGY; MONOCLONAL ANTIBODIES;

COMPLEMENT; COMPLEMENT ACTIVATIONS; FACTOR H; HYPERSENSITIVITY; HYPERSENSITIVITY REACTION; INTRAVENOUS APPLICATIONS; PSEUDOALLERGY; THERAPEUTIC ANTIBODIES;

CHEMICAL ACTIVATION;

AMPHOTERICIN B LIPID COMPLEX; COMPLEMENT FACTOR H; COMPLEMENT INHIBITOR; CREMOPHOR; LIPOSOME; PACLITAXEL; RITUXIMAB; DRUG CARRIER; MICELLE;

ALLERGIC REACTION; AMINO TERMINAL SEQUENCE; ARTICLE; COMPLEMENT ACTIVATION; COMPLEMENT ACTIVATION RELATED PSEUDOALLERGY; COMPLEMENT DEPENDENT CYTOTOXICITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; LIPOSOMAL DELIVERY; MICELLE; NANOMEDICINE; PARTICLE SIZE; DRUG EFFECTS; DRUG HYPERSENSITIVITY; IMMUNOLOGY; NEOPLASMS; NORMAL HUMAN; PATHOLOGY;

COMPLEMENT ACTIVATION; COMPLEMENT FACTOR H; DRUG CARRIERS; DRUG HYPERSENSITIVITY; HEALTHY VOLUNTEERS; HUMANS; LIPOSOMES; MICELLES; NANOMEDICINE; NEOPLASMS; RITUXIMAB;

EID: 84961223784     PISSN: 15499634     EISSN: 15499642     Source Type: Journal    
DOI: 10.1016/j.nano.2015.11.019     Document Type: Article

References (43)

1. Adkinson N.F., Essayan D., Gruchalla R., Haggerty H., Kawabata T., Sandler J.D., et al. Task force report: future research needs for the prevention and management of immune-mediated drug hypersensitivity reactions. J Allergy Clin Immunol 2002, 109(3):S461-S478.
2. Demoly P., Lebel B., Messaad D., Sahla H., Rongier M., Daurès J.P., et al. Predictive capacity of histamine release for the diagnosis of drug allergy. Allergy 1999, 54(5):500-506.
3. Szebeni J. Complement activation-related pseudoallergy: a stress reaction in blood triggered by nanomedicines and biologicals. Mol Immunol 2014, 61(2):163-173.
4. Lasser E.C., Lang J.H., Lyon S.G., Hamblin A.E. Complement and contrast material reactors. J Allergy Clin Immunol 1979, 64(2):105-112.
5. Lenz H.J. Management and preparedness for infusion and hypersensitivity reactions. Oncologist 2007, 12(5):601-609.
6. Cheifetz A., Mayer L. Monoclonal antibodies, immunogenicity, and associated infusion reactions. Mt Sinai J Med 2005, 72(4):250-256.
7. Szebeni J. Complement activation-related pseudoallergy caused by liposomes, micellar carriers of intravenous drugs, and radiocontrast agents. Crit Rev Ther Drug Carrier Syst 2001, 18(6):567-606.
8. Ricklin D., Hajishengallis G., Yang K., Lambris J.D. Complement: a key system for immune surveillance and homeostasis. Nat Immunol 2010, 11(9):785-797.
9. Rodríguez de Córdoba S., Esparza-Gordillo J., Goicoechea de Jorge E., Lopez-Trascasa M., Sánchez-Corral P. The human complement factor H: functional roles, genetic variations and disease associations. Mol Immunol 2004, 41(4):355-367.
10. Ferreira V.P., Pangburn M.K., Cortés C. Complement control protein factor H: the good, the bad, and the inadequate. Mol Immunol 2010, 47(13):2187-2197.
11. Kopp A., Hebecker M., Svobodová E., Józsi M. Factor H: a complement regulator in health and disease, and a mediator of cellular interactions. Biomolecules 2012, 2(1):46-75.
12. Szebeni J., Muggia F.M., Alving C.R. Complement activation by Cremophor EL as a possible contributor to hypersensitivity to paclitaxel: an in vitro study. J Natl Cancer Inst 1998, 90(4):300-306.
13. Szebeni J., Bedocs P., Rozsnyay Z., Weiszhár Z., Urbanics R., Rosivall L., et al. Liposome-induced complement activation and related cardiopulmonary distress in pigs: factors promoting reactogenicity of Doxil and Am Bisome. Nanomedicine 2012, 8(2):176-184.
14. Castiblanco-Valencia M.M., Fraga T.R., Silva L.B., Monaris D., Abreu P.A., Strobel S., et al. Leptospiral immunoglobulin-like proteins interact with human complement regulators factor H, FHL-1, FHR-1, and C4BP. J Infect Dis 2012, 205(6):995-1004.
15. Hebecker M., Alba-Domínguez M., Roumenina L.T., Reuter S., Hyvärinen S., Dragon-Durey M.A., et al. An engineered construct combining complement regulatory and surface-recognition domains represents a minimal-size functional factor H. J Immunol 2013, 191(2):912-921.
16. van den Hoven J.M., Nemes R., Metselaar J.M., Nuijen B., Beijnen J.H., Storm G., et al. Complement activation by PEGylated liposomes containing prednisolone. Eur J Pharm Sci 2013, 49(2):265-271.
17. Józsi M., Prechl J., Bajtay Z., Erdei A. Complement receptor type 1 (CD35) mediates inhibitory signals in human B lymphocytes. J Immunol 2002, 168(6):2782-2788.
18. Wu J., Wu Y.Q., Ricklin D., Janssen B.J., Lambris J.D., Gros P. Structure of complement fragment C3b-factor H and implications for host protection by complement regulators. Nat Immunol 2009, 10(7):728-733.
19. Józsi M., Oppermann M., Lambris J.D., Zipfel P.F. The C-terminus of complement factor H is essential for host cell protection. Mol Immunol 2007, 44(10):2697-2706.
20. Kajander T., Lehtinen M.J., Hyvärinen S., Bhattacharjee A., Leung E., Isenman D.E., et al. Dual interaction of factor H with C3d and glycosaminoglycans in host-nonhost discrimination by complement. Proc Natl Acad Sci U S A 2011, 108(7):2897-2902.
21. Morgan H.P., Schmidt C.Q., Guariento M., Blaum B.S., Gillespie D., Herbert A.P., et al. Structural basis for engagement by complement factor H of C3b on a self surface. Nat Struct Mol Biol 2011, 18(4):463-470.
22. Heinen S., Hartmann A., Lauer N., Wiehl U., Dahse H.M., Schirmer S., et al. Factor H-related protein 1 (CFHR-1) inhibits complement C5 convertase activity and terminal complex formation. Blood 2009, 114(12):2439-2447.
23. Timmann C., Leippe M., Horstmann R.D. Two major serum components antigenically related to complement factor H are different glycosylation forms of a single protein with no factor H-like complement regulatory functions. J Immunol 1991, 146(4):1265-1270.
24. Szebeni J., Fontana J.L., Wassef N.M., Mongan P.D., Morse D.S., Dobbins D.E., et al. Hemodynamic changes induced by liposomes and liposome-encapsulated hemoglobin in pigs: a model for pseudoallergic cardiopulmonary reactions to liposomes. Role of complement and inhibition by soluble CR1 and anti-C5a antibody. Circulation 1999, 99(17):2302-2309.
25. Smith G.P., Smith R.A. Membrane-targeted complement inhibitors. Mol Immunol 2001, 38(2-3):249-255.
26. Smith R.A. Targeting anticomplement agents. Biochem Soc Trans 2002, 30(Pt 6):1037-1041.
27. Ricklin D., Lambris J.D. Complement in immune and inflammatory disorders: therapeutic interventions. J Immunol 2013, 190(8):3839-3847.
28. Kishore U., Sim R.B. Factor H as a regulator of the classical pathway activation. Immunobiology 2012, 217(2):162-168.
29. Kuznetsova N.R., Vodovozova E.L. Differential binding of plasma proteins by liposomes loaded with lipophilic prodrugs of methotrexate and melphalan in the bilayer. Biochemistry (Mosc) 2014, 79(8):797-804.
30. Schmidt C.Q., Bai H., Lin Z., Risitano A.M., Barlow P.N., Ricklin D., et al. Rational engineering of a minimized immune inhibitor with unique triple-targeting properties. J Immunol 2013, 190(11):5712-5721.
31. Nichols E.M., Barbour T.D., Pappworth I.Y., Wong E.K., Palmer J.M., Sheerin N.S., et al. An extended mini-complement factor H molecule ameliorates experimental C3 glomerulopathy. Kidney Int 2015, 88(6):1314-1322. 10.1038/ki.2015.233.
32. Strobel S., Abarrategui-Garrido C., Fariza-Requejo E., Seeberger H., Sánchez-Corral P., Józsi M. Factor H-related protein 1 neutralizes anti-factor H autoantibodies in autoimmune hemolytic uremic syndrome. Kidney Int 2011, 80(4):397-404.
33. Goicoechea de Jorge E., Caesar J.J., Malik T.H., Patel M., Colledge M., Johnson S., et al. Dimerization of complement factor H-related proteins modulates complement activation in vivo. Proc Natl Acad Sci U S A 2013, 110(12):4685-4690.
34. Tortajada A., Yébenes H., Abarrategui-Garrido C., Anter J., García-Fernández J.M., Martínez-Barricarte R., et al. C3 glomerulopathy-associated CFHR1 mutation alters FHR oligomerization and complement regulation. J Clin Invest 2013, 123(6):2434-2446.
35. Józsi M., Tortajada A., Uzonyi B., Goicoechea de Jorge E., Rodríguez de Córdoba S. Factor H-related proteins determine complement-activating surfaces. Trends Immunol 2015, 36(6):374-384.
36. Baldo B.A. Adverse events to monoclonal antibodies used for cancer therapy: focus on hypersensitivity responses. Oncoimmunology 2013, 2(10):e26333. [1-15].
37. Kimby E. Tolerability and safety of rituximab (MabThera). Cancer Treat Rev 2005, 31(6):456-473.
38. Boross P., Leusen J.H. Mechanisms of action of CD20 antibodies. Am J Cancer Res 2012, 2(6):676-690.
39. Hörl S., Bánki Z., Huber G., Ejaz A., Windisch D., Muellauer B., et al. Reduction of complement factor H binding to CLL cells improves the induction of rituximab-mediated complement-dependent cytotoxicity. Leukemia 2013, 27(11):2200-2208.
40. Hakobyan S., Tortajada A., Harris C.L., de Córdoba S.R., Morgan B.P. Variant-specific quantification of factor H in plasma identifies null alleles associated with atypical hemolytic uremic syndrome. Kidney Int 2010, 78(8):782-788.
41. Harris C.L., Heurich M., Rodriguez de Cordoba S., Morgan B.P. The complotype: dictating risk for inflammation and infection. Trends Immunol 2012, 33(10):513-521.
42. Kozma G.T., Mészáros T., Zs Weiszhár, Schneider T., Rosta A., Urbanics R., et al. Variable association of complement activation by rituximab and paclitaxel in cancer patients in vivo and in their screening serum in vitro with clinical manifestations of hypersensitivity: a pilot study. Eur J Nanomed 2015, 7(4):289-301.
43. Fülöp T.G., Józsi M., Metselaar J., Storm G., Rosivall L., Szebeni J. The possible role of factor H in complement activation-related pseudoallergy (CARPA): a failed attempt to correlate blood levels of FH with liposome-induced hypersensitivity reactions in patients with autoimmune disease. Eur J Nanomed 2015, 7(1):7-14.