Effects of adjuvants for human use in systemic lupus erythematosus (SLE)-prone (New Zealand black/New Zealand white) F1 mice

Clinical and Experimental Immunology

Volumn 175, Issue 1, 2014, Pages 32-40

  Favoino, E ^a   Favia, E I ^a   Digiglio, L ^a   Racanelli, V ^a   Shoenfeld, Y ^b   Perosa, F ^a  

^a UNIVERSITY OF BARI MEDICAL SCHOOL   (Italy)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

Adjuvant; ASIA syndrome; Autoimmune disease; NZB NZW; Peptide; Vaccine

Indexed keywords

ADDAVAX; ALUMINUM HYDROXIDE; DNA ANTIBODY; FREUND ADJUVANT; MIFAMURTIDE; PHOSPHATE BUFFERED SALINE; RIBONUCLEOPROTEIN ANTIBODY; SM ANTIBODY; SQUALENE; UNCLASSIFIED DRUG;

ADJUVANT THERAPY; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DRUG EFFECT; FEMALE; HUMAN; IMMUNIZATION; MOUSE; MOUSE STRAIN; NEW ZEALAND BLACK MOUSE; NEW ZEALAND WHITE MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEINURIA; SYSTEMIC LUPUS ERYTHEMATOSUS; TOXICITY;

ADJUVANT; ASIA SYNDROME; AUTOIMMUNE DISEASE; NZB/NZW; PEPTIDE; VACCINE;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, ANTINUCLEAR; DRUG EVALUATION, PRECLINICAL; HUMANS; IMMUNIZATION, SECONDARY; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; PROTEINURIA; TIME FACTORS;

EID: 84888860237     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/cei.12208     Document Type: Article

References (53)

1. Ahuja A, Shupe J, Dunn R, Kashgarian M, Kehry MR, Shlomchik MJ. Depletion of B cells in murine lupus: efficacy and resistance. J Immunol 2007; 179:3351-3361.
2. van Vollenhoven RF, Gunnarsson I, Welin-Henriksson E etal. Biopsy-verified response of severe lupus nephritis to treatment with rituximab (anti-CD20 monoclonal antibody) plus cyclophosphamide after biopsy-documented failure to respond to cyclophosphamide alone. Scand J Rheumatol 2004; 33:423-427.
3. Leandro MJ, Cambridge G, Edwards JC, Ehrenstein MR, Isenberg DA. B-cell depletion in the treatment of patients with systemic lupus erythematosus: a longitudinal analysis of 24 patients. Rheumatology (Oxf) 2005; 44:1542-1545.
4. Smith KG, Jones RB, Burns SM, Jayne DR. Long-term comparison of rituximab treatment for refractory systemic lupus erythematosus and vasculitis: remission, relapse, and re-treatment. Arthritis Rheum 2006; 54:2970-2982.
5. Tokunaga M, Saito K, Kawabata D etal. Efficacy of rituximab (anti-CD20) for refractory systemic lupus erythematosus involving the central nervous system. Ann Rheum Dis 2007; 66:470-475.
6. Perosa F, Prete M, Racanelli V, Dammacco F. CD20-depleting therapy in autoimmune diseases: from basic research to the clinic. J Intern Med 2010; 267:260-277.
7. Reddy V, Jayne D, Close D, Isenberg D. B-cell depletion in SLE: clinical and trial experience with rituximab and ocrelizumab and implications for study design. Arthritis Res Ther 2013; 15 (Suppl. 1):S2.
8. Perosa F, Favoino E, Caragnano MA, Dammacco F. Generation of biologically active linear and cyclic peptides has revealed a unique fine specificity of rituximab and its possible cross-reactivity with acid sphingomyelinase-like phosphodiesterase 3b precursor. Blood 2006; 107:1070-1077.
9. Perosa F, Favoino E, Vicenti C etal. Two structurally different rituximab-specific CD20 mimotope peptides reveal that rituximab recognizes two different CD20-associated epitopes. J Immunol 2009; 182:416-423.
10. Andrews BS, Eisenberg RA, Theofilopoulos AN etal. Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains. J Exp Med 1978; 148:1198-1215.
11. Ploegh HL. Bridging B cell and T cell recognition of antigen. J Immunol 2007; 179:7193.
12. Eisenbarth SC, Colegio OR, O'Connor W, Sutterwala FS, Flavell RA. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature 2008; 453:1122-1126.
13. Hogenesch H, Dunham A, Hansen B, Anderson K, Maisonneuve JF, Hem SL. Formulation of a killed whole cell pneumococcus vaccine-effect of aluminum adjuvants on the antibody and IL-17 response. J Immune Based Ther Vaccines 2011; 9:5.
14. Marichal T, Ohata K, Bedoret D etal. DNA released from dying host cells mediates aluminum adjuvant activity. Nat Med 2011; 17:996-1002.
15. Baylor NW, Egan W, Richman P. Aluminum salts in vaccines-US perspective. Vaccine 2002; 20 (Suppl. 3):S18-S23.
16. Frazer IH, Leggatt GR, Mattarollo SR. Prevention and treatment of papillomavirus-related cancers through immunization. Annu Rev Immunol 2011; 29:111-138.
17. Pedersen C, Breindahl M, Aggarwal N etal. Randomized trial: immunogenicity and safety of coadministered human papillomavirus-16/18 AS04-adjuvanted vaccine and combined hepatitis A and B vaccine in girls. J Adolesc Health 2012; 50:38-46.
18. Beebe GW, Simon AH, Vivona S. Long-term mortality follow-up of Army recruits who received adjuvant influenza virus vaccine in 1951-1953. Am J Epidemiol 1972; 95:337-346.
19. Moss RB, Giermakowska W, Lanza P etal. Cross-clade immune responses after immunization with a whole-killed gp120-depleted human immunodeficiency virus type-1 immunogen in incomplete Freund's adjuvant (HIV-1 immunogen, REMUNE) in human immunodeficiency virus type-1 seropositive subjects. Viral Immunol 1997; 10:221-228.
20. Weber JS, Hua FL, Spears L, Marty V, Kuniyoshi C, Celis E. A phase I trial of an HLA-A1 restricted MAGE-3 epitope peptide with incomplete Freund's adjuvant in patients with resected high-risk melanoma. J Immunother 1999; 22:431-440.
21. Della Cioppa G, Nicolay U, Lindert K etal. Superior immunogenicity of seasonal influenza vaccines containing full dose of MF59 ((R)) adjuvant: results from a dose-finding clinical trial in older adults. Hum Vaccin Immunother 2012; 8:216-227.
22. Esposito S, Selicorni A, Daleno C etal. Immunogenicity, safety and tolerability of monovalent 2009 pandemic influenza A/H1N1 MF59-adjuvanted vaccine in children and adolescents with Williams or Cornelia De Lange syndrome. Hum Vaccin 2011; 7:613-617.
23. Satoh M, Treadwell EL, Reeves WH. Pristane induces high titers of anti-Su and anti-nRNP/Sm autoantibodies in BALB/c mice. Quantitation by antigen capture ELISAs based on monospecific human autoimmune sera. J Immunol Methods 1995; 182:51-62.
24. Satoh M, Kuroda Y, Yoshida H etal. Induction of lupus autoantibodies by adjuvants. J Autoimmun 2003; 21:1-9.
25. Katzav A, Kivity S, Blank M, Shoenfeld Y, Chapman J. Adjuvant immunization induces high levels of pathogenic antiphospholipid antibodies in genetically prone mice: another facet of the ASIA syndrome. Lupus 2012; 21:210-216.
26. Satoh M, Kumar A, Kanwar YS, Reeves WH. Anti-nuclear antibody production and immune-complex glomerulonephritis in BALB/c mice treated with pristane. Proc Natl Acad Sci USA 1995; 92:10934-10938.
27. Kuroda Y, Akaogi J, Nacionales DC etal. Distinctive patterns of autoimmune response induced by different types of mineral oil. Toxicol Sci 2004; 78:222-228.
28. Borenstein D. Siliconosis: a spectrum of illness. Semin Arthritis Rheum 1994; 24:1-7.
29. Agmon-Levin N, Shoenfeld Y. Chronic fatigue syndrome with autoantibodies-the result of an augmented adjuvant effect of hepatitis-B vaccine and silicone implant. Autoimmun Rev 2008; 8:52-55.
30. Israeli E. Gulf War syndrome as a part of the autoimmune (autoinflammatory) syndrome induced by adjuvant (ASIA). Lupus 2012; 21:190-194.
31. Lacson AG, D'Cruz CA, Gilbert-Barness E, Sharer L, Jacinto S, Cuenca R. Aluminum phagocytosis in quadriceps muscle following vaccination in children: relationship to macrophagic myofasciitis. Pediatr Dev Pathol 2002; 5:151-158.
32. Agmon-Levin N, Zafrir Y, Paz Z, Shilton T, Zandman-Goddard G, Shoenfeld Y. Ten cases of systemic lupus erythematosus related to hepatitis B vaccine. Lupus 2009; 18:1192-1197.
33. Blank M, Israeli E, Shoenfeld Y. When APS (Hughes syndrome) met the autoimmune/inflammatory syndrome induced by adjuvants (ASIA). Lupus 2012; 21:711-714.
34. Zafrir Y, Agmon-Levin N, Paz Z, Shilton T, Shoenfeld Y. Autoimmunity following hepatitis B vaccine as part of the spectrum of 'Autoimmune (Auto-inflammatory) Syndrome induced by Adjuvants' (ASIA): analysis of 93 cases. Lupus 2012; 21:146-152.
35. Shoenfeld Y, Selmi C, Zimlichman E, Gershwin ME. The autoimmunologist: geoepidemiology, a new center of gravity, and prime time for autoimmunity. J Autoimmun 2008; 31:325-330.
36. Shoenfeld Y, Agmon-Levin N. 'ASIA'-autoimmune/inflammatory syndrome induced by adjuvants. J Autoimmun 2011; 36:4-8.
37. Rosenblum H, Shoenfeld Y, Amital H. The common immunogenic etiology of chronic fatigue syndrome: from infections to vaccines via adjuvants to the ASIA syndrome. Infect Dis Clin North Am 2011; 25:851-863.
38. Vera-Lastra O, Medina G, Cruz-Dominguez MP, Jara LJ, Shoenfeld Y. Autoimmune/inflammatory syndrome induced by adjuvants (Shoenfeld's syndrome): clinical and immunological spectrum. Expert Rev Clin Immunol 2013; 9:361-373.
39. Bassi N, Luisetto R, Del PD etal. Induction of the 'ASIA' syndrome in NZB/NZWF1 mice after injection of complete Freund's adjuvant (CFA). Lupus 2012; 21:203-209.
40. Isenberg DA, Dudeney C, Williams W etal. Measurement of anti-DNA antibodies: a reappraisal using five different methods. Ann Rheum Dis 1987; 46:448-456.
41. Putterman C, Limpanasithikul W, Edelman M, Diamond B. The double edged sword of the immune response: mutational analysis of a murine anti-pneumococcal, anti-DNA antibody. J Clin Invest 1996; 97:2251-2259.
42. Frese-Schaper M, Zbaeren J, Gugger M, Monestier M, Frese S. Reversal of established lupus nephritis and prolonged survival of New Zealand black × New Zealand white mice treated with the topoisomerase I inhibitor irinotecan. J Immunol 2010; 184:2175-2182.
43. Dubois EL, Horowitz RE, Demopoulos HB, Teplitz R. NZB/NZW mice as a model of systemic lupus erythematosus. JAMA 1966; 195:285-289.
44. Oscherwitz J, Hankenson FC, Yu F, Cease KB. Low-dose intraperitoneal Freund's adjuvant: toxicity and immunogenicity in mice using an immunogen targeting amyloid-beta peptide. Vaccine 2006; 24:3018-3025.
45. Gilkeson GS, Ruiz P, Pippen AM, Alexander AL, Lefkowith JB, Pisetsky DS. Modulation of renal disease in autoimmune NZB/ NZW mice by immunization with bacterial DNA. J Exp Med 1996; 183:1389-1397.
46. Eisenberg RA, Tan EM, Dixon FJ. Presence of anti-Sm reactivity in autoimmune mouse strains. J Exp Med 1978; 147:582-587.
47. Monneaux F, Dumortier H, Steiner G, Briand JP, Muller S. Murine models of systemic lupus erythematosus: B and T cell responses to spliceosomal ribonucleoproteins in MRL/Fas(lpr) and (NZB × NZW)F(1) lupus mice. Int Immunol 2001; 13:1155-1163.
48. Nikoopour E, Schwartz JA, Huszarik K etal. Th17 polarized cells from nonobese diabetic mice following mycobacterial adjuvant immunotherapy delay type 1 diabetes. J Immunol 2010; 184:4779-4788.
49. Yoshizaki A, Yanaba K, Ogawa A, Asano Y, Kadono T, Sato S. Immunization with DNA topoisomerase I and Freund's complete adjuvant induces skin and lung fibrosis and autoimmunity via interleukin-6 signaling. Arthritis Rheum 2011; 63:3575-3585.
50. Llorente L, Richaud-Patin Y, Garcia-Padilla C etal. Clinical and biologic effects of anti-interleukin-10 monoclonal antibody administration in systemic lupus erythematosus. Arthritis Rheum 2000; 43:1790-1800.
51. Peng H, Wang W, Zhou M, Li R, Pan HF, Ye DQ. Role of interleukin-10 and interleukin-10 receptor in systemic lupus erythematosus. Clin Rheumatol 2013; 32:1255-1266.
52. Toth LA, Dunlap AW, Olson GA, Hessler JR. An evaluation of distress following intraperitoneal immunization with Freund's adjuvant in mice. Lab Anim Sci 1989; 39:122-126.
53. Tomljenovic L, Shaw CA. Mechanisms of aluminum adjuvant toxicity and autoimmunity in pediatric populations. Lupus 2012; 21:223-230.