A rationally designed TNF-α epitope-scaffold immunogen induces sustained antibody response and alleviates collagen-induced arthritis in mice

PLoS ONE

Volumn 11, Issue 9, 2016, Pages

  Zhang, Li ^a   Wang, Jin ^b   Xu, Aizhang ^a   Zhong, Conghao ^a   Lu, Wuguang ^c   Deng, Li ^e   Li, Rongxiu ^a,d  

^a Shanghai Jiao Tong University   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c Laboratory of Cellular and Molecular Biology Jiangsu Province Institute of Traditional Chinese Medicine   (China)

^d BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^e Shanghai HyCharm Inc   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DIPHTHERIA TOXIN; EPITOPE; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; VALYLSERYLARGINYLPHENYLALANYLALANYLISOLEUCYLSERYLTYROSYLGLUTAMINYLGLUTAMYLLYSYLVALYLASPARAGINYLLEUCYLLEUYLSERYLALANYLVALINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CD4+ T LYMPHOCYTE; COLLAGEN-INDUCED ARTHRITIS; CONTROLLED STUDY; DRUG SAFETY; FEMALE; HUMORAL IMMUNITY; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; INCIDENCE; MALE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RHEUMATOID ARTHRITIS; VACCINATION;

EID: 84992170267     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0163080     Document Type: Article

References (51)

1. Tracey KJ, Cerami A. Tumor necrosis factor: a pleiotropic cytokine and therapeutic target. Annual review of medicine. 1994; 45: 491-503. doi: 10.1146/annurev.med.45.1.491 PMID: 8198398.
2. Monaco C, Nanchahal J, Taylor P, Feldmann M. Anti-TNF therapy: past, present and future. International immunology. 2015; 27(1): 55-62. Epub Nov 19. doi: 10.1093/intimm/dxu102 PMID: 25411043; PubMed Central PMCID: PMC4279876.
3. Feldmann M, Maini RN. TNF defined as a therapeutic target for rheumatoid arthritis and other autoimmune diseases Nature medicine. 2003; 9(11): 1433-. PMID: 14520364.
4. Feldmann M, Steinman L. Design of effective immunotherapy for human autoimmunity. Nature. 2005; 435(7042): 612-9. doi: 10.1038/nature03727 PMID: 15931214.
5. Tracey D, Klareskog L, Sasso EH, Salfeld JG, Tak PP. Tumor necrosis factor antagonist mechanisms of action: a comprehensive review. Pharmacology & therapeutics. 2008; 117(2): 244-79. Epub Oct 26. doi: 10.1016/j.pharmthera.2007.10.001 PMID: 18155297.
6. van Schie KA, Hart MH, de Groot ER, Kruithof S, Aarden LA, Wolbink GJ, et al. The antibody response against human and chimeric anti-TNF therapeutic antibodies primarily targets the TNF binding region. Annals of the rheumatic diseases. 2015; 74(1): 311-4. Epub Oct 23. doi: 10.1136/annrheumdis-2014-206237 PMID: 25342759.
7. Vincent FB, Morand EF, Murphy K, Mackay F, Mariette X, Marcelli C. Antidrug antibodies (ADAb) to tumour necrosis factor (TNF)-specific neutralising agents in chronic inflammatory diseases: a real issue, a clinical perspective. Annals of the rheumatic diseases. 2013; 72(2): 165-78. Epub Nov 24. doi: 10.1136/annrheumdis-2012-202545 PMID: 23178294.
8. Jia T, Pan Y, Li J, Wang L. Strategies for active TNF-alpha vaccination in rheumatoid arthritis treatment. Vaccine. 2013; 31(38): 4063-8. Epub Jul 8. doi: 10.1016/j.vaccine.2013.06.101 PMID: 23845805.
9. Dalum I. Therapeutic antibodies elicited by immunization against TNF-a. Nature Biotechnology. 1999; 17(7): 666-9. PMID: 10404159.
10. Le Buanec H, Delavallee L, Bessis N, Paturance S, Bizzini B, Gallo R, et al. TNFalpha kinoid vaccination-induced neutralizing antibodies to TNFalpha protect mice from autologous TNFalpha-driven chronic and acute inflammation. Proceedings of the National Academy of Sciences of the United States of America. 2006; 103(51): 19442-7. Epub Dec 8. doi: 10.1073/pnas.0604827103 PMID: 17158801; PubMed Central PMCID: PMC1748245
11. Durez P, Vandepapeliere P, Miranda P, Toncheva A, Berman A, Kehler T, et al. Therapeutic vaccination with TNF-Kinoid in TNF antagonist-resistant rheumatoid arthritis: a phase II randomized, controlled clinical trial. PloS one. 2014; 9(12): e113465. doi: 10.1371/journal.pone.0113465 PMID: 25517733; PubMed Central PMCID: PMC4269456.
12. Waterston A, Gumbrell L, Bratt T, Waller S, Gustav-Aspland J, LgcyHermenier C, et al. Phase I study of TNF alpha AutoVaccIne in patients with metastatic cancer. Cancer Immunology Immunotherapy. 2005; 54(9): 848-57. doi: 10.1007/s00262-005-0661-x PMID: WOS:000230316800004.
13. Grunewald J, Tsao ML, Perera R, Dong L, Niessen F, Wen BG, et al. Immunochemical termination of self-tolerance. Proceedings of the National Academy of Sciences of the United States of America. 2008; 105(32): 11276-80. Epub Aug 6. doi: 10.1073/pnas.0804157105 PMID: 18685087; PubMed Central PMCID: PMC2516224.
14. Capini CJ, Bertin-Maghit SM, Bessis N, Haumont PM, Bernier EM, Muel EG, et al. Active immunization against murine TNFalpha peptides in mice: generation of endogenous antibodies cross-reacting with the native cytokine and in vivo protection. Vaccine. 2004; 22(23-24): 3144-53. doi: 10.1016/j.vaccine.2004.01.064 PMID: 15297067.
15. Corti A. Tumor necrosis factor: methods and protocols: Springer Science & Business Media; 2004.
16. Elshabrawy HA, Fan J, Haddad CS, Ratia K, Broder CC, Caffrey M, et al. Identification of a broad-spectrum antiviral small molecule against severe acute respiratory syndrome coronavirus and Ebola, Hendra, and Nipah viruses by using a novel high-throughput screening assay. Journal of virology. 2014; 88(8): 4353-65. doi: 10.1128/JVI.03050-13 PMID: 24501399; PubMed Central PMCID: PMC3993759.
17. Lavy S, Marks ES, Abramsky O. Parkinsonism and hyperthyroidism. European neurology. 1974; 12 (1): 20-7. PMID: 4414985
18. Zhao WS, Wang J, Ma XJ, Yang Y, Liu Y, Huang LD, et al. Relative motions between left flipper and dorsal fin domains favour P2X4 receptor activation. Nature communications. 2014; 5: 4189. doi: 10.1038/ncomms5189 PMID: 24943126.
19. Tang W, Lu Y, Tian QY, Zhang Y, Guo FJ, Liu GY, et al. The growth factor progranulin binds to TNF receptors and is therapeutic against inflammatory arthritis in mice. Science. 2011; 332(6028): 478-84. Epub Mar 10. doi: 10.1126/science.1199214 PMID: 21393509; PubMed Central PMCID: PMC3104397.
20. Nagahira K, Fukuda Y, Terakawa M, Hashino J, Nasu T, Nakazato H, et al. Epitope mapping of monoclonal antibodies to tumor necrosis factor-a. Immunology Letters. 1995; 46(1-2): 135-41. PMID: 7590909.
21. Capini CJ Active immunization against murine TNF peptides in mice: generation of endogenous antibodies cross-reacting with the native cytokine and in vivo protection. Vaccine. 2004; 22(23-24): 3144-53. PMID: 15297067.
22. Ladokhin AS pH-triggered conformational switching along the membrane insertion pathway of the diphtheria toxin T-domain. Toxins. 2013; 5(8): 1362-80. doi: 10.3390/toxins5081362 PMID: 23925141; PubMed Central PMCID: PMC3760040.
23. Malito E, Bursulaya B, Chen C, Lo Surdo P, Picchianti M, Balducci E, et al. Structural basis for lack of toxicity of the diphtheria toxin mutant CRM197. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109(14): 5229-34. Epub Mar 19. doi: 10.1073/pnas.1201964109 PMID: 22431623; PubMed Central PMCID: PMC3325714.
24. Bentley AA, Merkulov SM, Peng Y, Rozmarynowycz R, Qi X, Pusztai-Carey M, et al. Chimeric glutathione S-transferases containing inserts of kininogen peptides: potential novel protein therapeutics. The Journal of biological chemistry. 2012; 287(26): 22142-50. Epub May 10. doi: 10.1074/jbc.M112.372854 PMID: 22577144; PubMed Central PMCID: PMC3381172.
25. Brunet AP, Huang ES, Huffine ME, Loeb JE, Weltman RJ, Hecht MH. The role of turns in the structure of an alpha-helical protein. Nature. 1993; 364(6435): 355-8. doi: 10.1038/364355a0 PMID: 8332196.
26. Diethelm-Okita BM, Okita DK, Banaszak L, Conti-Fine BM. Universal epitopes for human CD4+ cells on tetanus and diphtheria toxins. The Journal of infectious diseases. 2000; 181(3): 1001-9. doi: 10.1086/315324 PMID: 10720523.
27. Fraser CC, Altreuter DH, Ilyinskii P, Pittet L, LaMothe RA, Keegan M, et al. Generation of a universal CD4 memory T cell recall peptide effective in humans, mice and non-human primates. Vaccine. 2014; 32(24): 2896-903. Epub Feb 26. doi: 10.1016/j.vaccine.2014.02.024 PMID: 24583006.
28. Carmicle S, Steede NK, Landry SJ. Antigen three-dimensional structure guides the processing and presentation of helper T-cell epitopes. Molecular immunology. 2007; 44(6): 1159-68. Epub Aug 8. doi: 10.1016/j.molimm.2006.06.014 PMID: 16893568.
29. So T, Ito H, Hirata M, Ueda T, Imoto T. Contribution of conformational stability of hen lysozyme to induction of type 2 T-helper immune responses. Immunology. 2001; 104(3): 259-68. PMID: 11722640; PubMed Central PMCID: PMCPMC1783307.
30. Ohkuri T, Nagatomo S, Oda K, So T, Imoto T, Ueda T. A protein's conformational stability is an immunologically dominant factor: evidence that free-energy barriers for protein unfolding limit the immuno-genicity of foreign proteins. Journal of immunology. 2010; 185(7): 4199-205. Epub Sep 3. doi: 10.4049/jimmunol.0902249 PMID: 20817878.
31. Barrera P, Joosten LA, den Broeder AA, van de Putte LB, van Riel PL, van den Berg WB. Effects of treatment with a fully human anti-tumour necrosis factor alpha monoclonal antibody on the local and systemic homeostasis of interleukin 1 and TNFalpha in patients with rheumatoid arthritis. Annals of the rheumatic diseases. 2001; 60(7): 660-9. PMID: 11406520; PubMed Central PMCID: PMC1753753.
32. Skwarczynski M, Toth I. Peptide-based synthetic vaccines. Chem Sci. 2016; 7(2): 842-54.
33. Jones LH Recent advances in the molecular design of synthetic vaccines. Nature chemistry. 2015; 7 (12): 952-60. doi: 10.1038/nchem.2396 PMID: 26587710.
34. Li W, Joshi MD, Singhania S, Ramsey KH, Murthy AK. Peptide Vaccine: Progress and Challenges. Vaccines. 2014; 2(3): 515-36. doi: 10.3390/vaccines2030515 PMID: 26344743; PubMed Central PMCID: PMC4494216.
35. Correia BE, Ban YE, Holmes MA, Xu H, Ellingson K, Kraft Z, et al. Computational design of epitope-scaffolds allows induction of antibodies specific for a poorly immunogenic HIV vaccine epitope. Structure. 2010; 18(9): 1116-26. doi: 10.1016/j.str.2010.06.010 PMID: 20826338.
36. Correia BE, Bates JT, Loomis RJ, Baneyx G, Carrico C, Jardine JG, et al. Proof of principle for epi-tope-focused vaccine design. Nature. 2014; 507(7491): 201-6. Epub Feb 5. doi: 10.1038/nature12966 PMID: 24499818; PubMed Central PMCID: PMC4260937.
37. Ofek G, Guenaga FJ, Schief WR, Skinner J, Baker D, Wyatt R, et al. Elicitation of structure-specific antibodies by epitope scaffolds. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107(42): 17880-7. Epub Sep 27. doi: 10.1073/pnas.1004728107 PMID: 20876137; PubMed Central PMCID: PMC2964213.
38. Liljeroos L, Malito E, Ferlenghi I, Bottomley MJ. Structural and Computational Biology in the Design of Immunogenic Vaccine Antigens. Journal of immunology research. 2015; 2015: 156241. EpubOct 7. doi: 10.1155/2015/156241 PMID: 26526043; PubMed Central PMCID: PMC4615220.
39. Nielsen FS, Sauer J, Backlund J, Voldborg B, Gregorius K, Mouritsen S, et al. Insertion of foreign T cell epitopes in human tumor necrosis factor alpha with minimal effect on protein structure and biological activity. The Journal of biological chemistry. 2004; 279(32): 33593-600. Epub Jun 1. doi: 10.1074/jbc.M403072200 PMID: 15173183.
40. Dakappagari NK, Lute KD, Rawale S, Steele JT, Allen SD, Phillips G, et al. Conformational HER-2/neu B-cell epitope peptide vaccine designed to incorporate two native disulfide bonds enhances tumor cell binding and antitumor activities. The Journal of biological chemistry. 2005; 280(1): 54-63. Epub Oct 26. doi: 10.1074/jbc.M411020200 PMID: 15507452.
41. Johnson N, Pickett MA, Watt PJ, Clarke IN, Heckels JE. Construction of an epitope vector utilising the diphtheria toxin B-subunit. FEMS microbiology letters. 1997; 146(1): 91-6. PMID: 8997711.
42. Romaniuk SI, Kolibo DB, Komisarenko SV. Perspectives of application of recombinant diphtheria toxin derivatives. Bioorganicheskaia khimiia. 2012; 38(6): 639-52. PMID: 23547467.
43. Pobre K, Tashani M, Ridda I, Rashid H, Wong M, Booy R. Carrier priming or suppression: understanding carrier priming enhancement of anti-polysaccharide antibody response to conjugate vaccines. Vaccine. 2014; 32(13): 1423-30. Epub Jan 31. doi: 10.1016/j.vaccine.2014.01.047 PMID: 24492014.
44. Bhattacharya P, Thiruppathi M, Elshabrawy HA, Alharshawi K, Kumar P, Prabhakar BS. GM-CSF: An immune modulatory cytokine that can suppress autoimmunity. Cytokine. 2015; 75(2): 261-71. doi: 10.1016/j.cyto.2015.05.030 PMID: 26113402; PubMed Central PMCID: PMC4553090.
45. Bhattacharya P, Budnick I, Singh M, Thiruppathi M, Alharshawi K, Elshabrawy H, et al. Dual Role of GM-CSF as a Pro-Inflammatory and a Regulatory Cytokine: Implications for Immune Therapy. Journal of interferon & cytokine research: the official journal of the International Society for Interferon and Cytokine Research. 2015; 35(8): 585-99. doi: 10.1089/jir.2014.0149 PMID: 2580378; PubMed Central PMCID: PMC4529096.
46. Gathungu G, Kim MO, Ferguson JP, Sharma Y, Zhang W, Ng SM, et al. Granulocyte-macrophage colony-stimulating factor autoantibodies: a marker of aggressive Crohn's disease. Inflammatory bowel diseases. 2013; 19(8): 1671-80. doi: 10.1097/MIB.0b013e318281f506 PMID: 23749272; PubMed Central PMCID: PMC3707315.
47. McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. The New England journal of medicine. 2011; 365(23): 2205-19. doi: 10.1056/NEJMra1004965 PMID: 22150039.
48. Rowin J, Thiruppathi M, Arhebamen E, Sheng J, Prabhakar BS, Meriggioli MN. Granulocyte macrophage colony-stimulating factor treatment of a patient in myasthenic crisis: effects on regulatory T cells. Muscle & nerve. 2012; 46(3): 449-53. doi: 10.1002/mus.23488 PMID: 22907239; PubMed Central PMCID: PMC3428740.
49. Biton J, Semerano L, Delavallee L, Lemeiter D, Laborie M, Grouard-Vogel G, et al. Interplay between TNF and regulatory T cells in a TNF-driven murine model of arthritis. Journal of immunology. 2011; 186(7): 3899-910. doi: 10.4049/jimmunol.1003372 PMID: 21346237.
50. Farooq SM, Ashour HM. Type II collagen induces peripheral tolerance in BALB/c mice via the generation of CD8+ T regulatory cells. PloS one. 2012; 7(11): e48635. doi: 10.1371/journal.pone.0048635 PMID: 23133648; PubMed Central PMCID: PMC3487721.
51. Farooq SM, Kumar A, Ashour HM. Eye-mediated immune tolerance to Type II collagen in arthritis-prone strains of mice. Journal of cellular and molecular medicine. 2014; 18(12): 2512-8. doi: 10.1111/jcmm.12376 PMID: 25211510; PubMed Central PMCID: PMC4302655.