Advax-adjuvanted recombinant protective antigen provides protection against inhalational anthrax that is further enhanced by addition of murabutide adjuvant

Clinical and Vaccine Immunology

Volumn 21, Issue 4, 2014, Pages 580-586

  Feinen, Brandon ^a   Petrovsky, Nikolai ^b   Verma, Anita ^a   Merkel, Tod J ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^b VAXINE PTY LTD   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAX VACCINE; BATCH AD1; CATHEPSIN; IMMUNOGLOBULIN G ANTIBODY; IMMUNOLOGICAL ADJUVANT; MURABUTIDE; POLYSACCHARIDE; POLYSACCHARIDE VACCINE; RECOMBINANT ANTIGEN; UNCLASSIFIED DRUG; ADVAX; ALUMINUM POTASSIUM SULFATE; ALUMINUM SULFATE; ANTHRAX TOXIN; BACTERIAL ANTIGEN; BACTERIAL TOXIN; BACTERIUM ANTIBODY; IMMUNOGLOBULIN G; INULIN; N ACETYLMURAMYLALANYL DEXTRO ISOGLUTAMINE; N-ACETYLMURAMYL-ALANYLGLUTAMINE-N-BUTYL ESTER; SUBUNIT VACCINE;

ADD ON THERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTHRAX; ANTIBACTERIAL ACTIVITY; ANTIBODY TITER; ARTICLE; BACILLUS ANTHRACIS; BACTERIAL STRAIN; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DRUG FORMULATION; DRUG POTENTIATION; FEMALE; HUMORAL IMMUNITY; IMMUNIZATION; IMMUNOGENICITY; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOSTIMULATION; IN VIVO STUDY; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROVOCATION TEST; PULMONARY ANTHRAX; RISK REDUCTION; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; SURVIVAL;

ACETYLMURAMYL-ALANYL-ISOGLUTAMINE; ADJUVANTS, IMMUNOLOGIC; ALUM COMPOUNDS; ANIMALS; ANTHRAX; ANTHRAX VACCINES; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL TOXINS; FEMALE; IMMUNOGLOBULIN G; IMMUNOLOGIC MEMORY; INULIN; MICE; SURVIVAL ANALYSIS; VACCINES, SUBUNIT;

EID: 84897946341     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00019-14     Document Type: Article

References (60)

1. Mock M, Fouet A. 2001. Anthrax. Annu. Rev. Microbiol. 55:647-671. http://dx.doi.org/10.1146/annurev.micro.55.1.647. (Pubitemid 32978119)
2. Barnes JM. 1947. The development of anthrax following the administration of spores by inhalation. Br. J. Exp. Pathol. 28:385-394.
3. Meselson M, Guillemin J, Hugh-Jones M, Langmuir A, Popova I, Shelokov A, Yampolskaya O. 1994. The Sverdlovsk anthrax outbreak of 1979. Science 266:1202-1208. http://dx.doi.org/10.1126/science.7973702. (Pubitemid 24371272)
4. Greene CM, Reefhuis J, Tan C, Fiore AE, Goldstein S, Beach MJ, Redd SC, Valiante D, Burr G, Buehler J, Pinner RW, Bresnitz E, Bell BP. 2002. Epidemiologic investigations of bioterrorism-related anthrax, New Jersey, 2001. Emerg. Infect. Dis. 8:1048-1055. http://dx.doi.org/10.3201/eid0810.020329. (Pubitemid 35256992)
5. Bhalla DK, Warheit DB. 2004. Biological agents with potential for misuse: a historical perspective and defensive measures. Toxicol. Appl. Pharmacol. 199:71-84. http://dx.doi.org/10.1016/j.taap.2004.03.009. (Pubitemid 39099457)
6. Brittingham KC, Ruthel G, Panchal RG, Fuller CL, Ribot WJ, Hoover TA, Young HA, Anderson AO, Bavari S. 2005. Dendritic cells endocytose Bacillus anthracis spores: implications for anthrax pathogenesis. J. Immunol. 174:5545-5552. (Pubitemid 40593195)
7. Cleret A, Quesnel-Hellmann A, Vallon-Eberhard A, Verrier B, Jung S, Vidal D, Mathieu J, Tournier JN. 2007. Lung dendritic cells rapidly mediate anthrax spore entry through the pulmonary route. J. Immunol. 178:7994-8001. (Pubitemid 46898070)
8. Guidi-Rontani C, Levy M, Ohayon H, Mock M. 2001. Fate of germinated Bacillus anthracis spores in primary murine macrophages. Mol. Microbiol. 42:931-938. http://dx.doi.org/10.1046/j.1365-2958.2001.02695.x. (Pubitemid 33078377)
9. Ross JM. 1957. The pathogenesis of anthrax following the administration of spores by the respiratory route. J. Pathol. Bacteriol. 73:485-494. http://dx.doi.org/10.1002/path.1700730219.
10. Dixon TC, Fadl AA, Koehler TM, Swanson JA, Hanna PC. 2000. Early Bacillus anthracis-macrophage interactions: intracellular survival survival and escape. Cell. Microbiol. 2:453-463. http://dx.doi.org/10.1046/j.1462-5822.2000.00067.x. (Pubitemid 32049317)
11. Hu H, Sa Q, Koehler TM, Aronson AI, Zhou D. 2006. Inactivation of Bacillus anthracis spores in murine primary macrophages. Cell. Microbiol. 8:1634-1642. http://dx.doi.org/10.1111/j.1462-5822.2006.00738.x. (Pubitemid 44350022)
12. Kang TJ, Fenton MJ, Weiner MA, Hibbs S, Basu S, Baillie L, Cross AS. 2005. Murine macrophages kill the vegetative form of Bacillus anthracis. Infect. Immun. 73:7495-7501. http://dx.doi.org/10.1128/IAI.73.11.7495-7501.2005. (Pubitemid 41587654)
13. Dixon TC, Meselson M, Guillemin J, Hanna PC. 1999. Anthrax. N. Engl. J. Med. 341:815-826. http://dx.doi.org/10.1056/NEJM199909093411107. (Pubitemid 29420478)
14. Young JA, Collier RJ. 2007. Anthrax toxin: receptor binding, internalization, pore formation, and translocation. Annu. Rev. Biochem. 76:243-265. http://dx.doi.org/10.1146/annurev.biochem.75.103004.142728.
15. Duesbery NS, Webb CP, Leppla SH, Gordon VM, Klimpel KR, Copeland TD, Ahn NG, Oskarsson MK, Fukasawa K, Paull KD, Vande Woude GF. 1998. Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science 280:734-737. http://dx.doi.org/10.1126/science.280.5364.734. (Pubitemid 28243347)
16. Vitale G, Pellizzari R, Recchi C, Napolitani G, Mock M, Montecucco C. 1998. Anthrax lethal factor cleaves the N-terminus of MAPKKs and induces tyrosine/threonine phosphorylation of MAPKs in cultured macrophages. Biochem. Biophys. Res. Commun. 248:706-711. http://dx.doi.org/10.1006/bbrc.1998.9040. (Pubitemid 28404486)
17. Hoover DL, Friedlander AM, Rogers LC, Yoon IK, Warren RL, Cross AS. 1994. Anthrax edema toxin differentially regulates lipopolysaccha-ride- induced monocyte production of tumor necrosis factor alpha and interleukin-6 by increasing intracellular cyclic AMP. Infect. Immun. 62:4432-4439. (Pubitemid 24301974)
18. Leppla SH. 1982. Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proc. Natl. Acad. Sci. U. S. A. 79:3162-3166. http://dx.doi.org/10.1073/pnas.79.10. 3162. (Pubitemid 12008374)
19. Tournier JN, Quesnel-Hellmann A, Mathieu J, Montecucco C, Tang WJ, Mock M, Vidal DR, Goossens PL. 2005. Anthrax edema toxin cooperates with lethal toxin to impair cytokine secretion during infection of dendritic cells. J. Immunol. 174:4934-4941.
20. Iacono-Connors LC, Welkos SL, Ivins BE, Dalrymple JM. 1991. Protection against anthrax with recombinant virus-expressed protective antigen in experimental animals. Infect. Immun. 59:1961-1965.
21. Chichester JA, Manceva SD, Rhee A, Coffin MV, Musiychuk K, Mett V, Shamloul M, Norikane J, Streatfield SJ, Yusibov V. 16 January 2013. A plant-produced protective antigen vaccine confers protection in rabbits against a lethal aerosolized challenge with Bacillus anthracis Ames spores. Hum. Vaccin. Immunother. http://dx.doi.org/10.4161/hv.23233.
22. Watkinson A, Soliakov A, Ganesan A, Hirst K, Lebutt C, Fleetwood K, Fusco PC, Fuerst TR, Lakey JH. 2013. Increasing the potency of an alhydrogel-formulated anthrax vaccine by minimizing antigen-adjuvant interactions. Clin. Vaccine Immunol. 20:1659-1668. http://dx.doi.org/10.1128/ CVI.00320-13.
23. Gorse GJ, Keitel W, Keyserling H, Taylor DN, Lock M, Alves K, Kenner J, Deans L, Gurwith M. 2006. Immunogenicity and tolerance of ascending doses of a recombinant protective antigen (rPA102) anthrax vaccine: a randomized, double-blinded, controlled, multicenter trial. Vaccine 24: 5950-5959. http://dx.doi.org/10.1016/j.vaccine.2006.05.044. (Pubitemid 44080366)
24. Campbell JD, Clement KH, Wasserman SS, Donegan S, Chrisley L, Kotloff KL. 2007. Safety, reactogenicity and immunogenicity of a recombinant protective antigen anthrax vaccine given to healthy adults. Hum. Vaccin. 3:205-211. http://dx.doi.org/10.4161/hv.3.5.4459. (Pubitemid 47598179)
25. Fowler K, McBride BW, Turnbull PC, Baillie LW. 1999. Immune correlates of protection against anthrax. J. Appl. Microbiol. 87:305. http://dx.doi.org/10. 1046/j.1365-2672.1999.00898.x.
26. Boyaka PN, Tafaro A, Fischer R, Leppla SH, Fujihashi K, McGhee JR. 2003. Effective mucosal immunity to anthrax: neutralizing antibodies and Th cell responses following nasal immunization with protective antigen. J. Immunol. 170:5636-5643. (Pubitemid 36617855)
27. Sloat BR, Cui Z. 2006. Nasal immunization with anthrax protective antigen protein adjuvanted with polyriboinosinic-polyribocytidylic acid induced strong mucosal and systemic immunities. Pharm. Res. 23:1217-1226. http://dx.doi.org/10. 1007/s11095-006-0206-9. (Pubitemid 43946144)
28. Petrovsky N, Aguilar JC. 2004. Vaccine adjuvants: current state and future trends. Immunol. Cell Biol. 82:488-496. http://dx.doi.org/10.1111/j.0818- 9641.2004.01272.x. (Pubitemid 39421058)
29. Petrovsky N, Cooper PD. 2011. Carbohydrate-based immune adjuvants. Expert Rev. Vaccines 10:523-537. http://dx.doi.org/10.1586/erv.11.30.
30. Cooper PD, Petrovsky N. 2011. Delta inulin: a novel, immunologically active, stable packing structure comprising beta-D-[2 -> 1] poly(fructofuranosyl) alpha-D-glucose polymers. Glycobiology 21:595-606. http://dx.doi.org/10.1093/glycob/cwq201.
31. Cooper PD, Barclay TG, Ginic-Markovic M, Petrovsky N. 2013. The polysaccharide inulin is characterized by an extensive series of periodic isoforms with varying biological actions. Glycobiology 23:1164-1174. http://dx.doi.org/10.1093/glycob/cwt053.
32. Lobigs M, Pavy M, Hall RA, Lobigs P, Cooper P, Komiya T, Toriniwa H, Petrovsky N. 2010. An inactivated Vero cell-grown Japanese encephalitis vaccine formulated with Advax, a novel inulin-based adjuvant, induces protective neutralizing antibody against homologous and heterologous flaviviruses. J. Gen. Virol. 91:1407-1417. http://dx.doi.org/10.1099/vir.0.019190-0.
33. Petrovsky N, Larena M, Siddharthan V, Prow NA, Hall RA, Lobigs M, Morrey J. 2013. An inactivated cell culture Japanese encephalitis vaccine (JE-ADVAX) formulated with delta inulin adjuvant provides robust heterologous protection against West Nile encephalitis via cross-protective memory B cells and neutralizing antibody. J. Virol. 87:10324-10333. http://dx.doi.org/10.1128/JVI. 00480-13.
34. Honda-Okubo Y, Saade F, Petrovsky N. 2012. Advax, a polysaccharide adjuvant derived from delta inulin, provides improved influenza vaccine protection through broad-based enhancement of adaptive immune responses. Vaccine 30:5373-5381. http://dx.doi.org/10.1016/j.vaccine.2012.06.021.
35. Cristillo AD, Ferrari MG, Hudacik L, Lewis B, Galmin L, Bowen B, Thompson D, Petrovsky N, Markham P, Pal R. 2011. Induction of mucosal and systemic antibody and T-cell responses following prime-boost immunization with novel adjuvanted human immunodeficiency virus-1-vaccine formulations. J. Gen. Virol. 92:128-140. http://dx.doi.org/10.1099/vir.0.023242-0.
36. Saade F, Honda-Okubo Y, Trec S, Petrovsky N. 2013. A novel hepatitis B vaccine containing Advax, a polysaccharide adjuvant derived from delta inulin, induces robust humoral and cellular immunity with minimal reactogenicity in preclinical testing. Vaccine 31:1999-2007. http://dx.doi.org/10.1016/j.vaccine. 2012.12.077.
37. Gordon DL, Sajkov D, Woodman RJ, Honda-Okubo Y, Cox MM, Heinzel S, Petrovsky N. 2012. Randomized clinical trial of immunogenicity and safety of a recombinant H1N1/2009 pandemic influenza vaccine containing Advax polysaccharide adjuvant. Vaccine 30:5407-5416. http://dx.doi.org/10.1016/j.vaccine.2012.06. 009.
38. Philpott DJ, Girardin SE. 2004. The role of Toll-like receptors and Nod proteins in bacterial infection. Mol. Immunol. 41:1099-1108. http://dx.doi.org/10.1016/j.molimm.2004.06.012. (Pubitemid 39345391)
39. Strominger JL. 2007. Bacterial cell walls, innate immunity and immunoadjuvants. Nat. Immunol. 8:1269-1271. http://dx.doi.org/10.1038/ni1207- 1269. (Pubitemid 350131160)
40. Vidal VF, Casteran N, Riendeau CJ, Kornfeld H, Darcissac EC, Capron A, Bahr GM. 2001. Macrophage stimulation with Murabutide, an HIV-suppressive muramyl peptide derivative, selectively activates extracellular signal-regulated kinases 1 and 2, C/EBPbeta and STAT1: role of CD14 and Toll-like receptors 2 and 4. Eur. J. Immunol. 31:1962-1971. http://dx.doi.org/10.1002/1521- 4141(200107)31:71962::AID-IMMU1962 3.0.CO;2-V.
41. Cho HJ, Kim JY, Lee Y, Kim JM, Kim YB, Chun T, Oh YK. 2010. Enhanced humoral and cellular immune responses after sublingual immunization against human papillomavirus 16 L1 protein with adjuvants. Vaccine 28:2598-2606. http://dx.doi.org/10.1016/j.vaccine.2010.01.013.
42. Darcissac EC, Bahr GM, Pouillart PR, Riveau GJ, Parant MA. 1996. Selective potentiation of cytokine expression in human whole blood by murabutide, a muramyl dipeptide analogue. Cytokine 8:658-666. http://dx.doi.org/10.1006/cyto.1996.0088. (Pubitemid 26326832)
43. Darcissac EC, Truong MJ, Dewulf J, Mouton Y, Capron A, Bahr GM. 2000. The synthetic immunomodulator murabutide controls human immunodeficiency virus type 1 replication at multiple levels in macrophages and dendritic cells. J. Virol. 74:7794-7802. http://dx.doi.org/10.1128/JVI.74.17.7794-7802.2000. (Pubitemid 30641624)
44. Geddes K, Magalhaes JG, Girardin SE. 2009. Unleashing the therapeutic potential of NOD-like receptors. Nat. Rev. Drug Discov. 8:465-479. http://dx.doi.org/10.1038/nrd2783.
45. Telzak E, Wolff SM, Dinarello CA, Conlon T, el Kholy A, Bahr GM, Choay JP, Morin A, Chedid L. 1986. Clinical evaluation of the immunoadjuvant murabutide, a derivative of MDP, administered with a tetanus toxoid vaccine. J. Infect. Dis. 153:628-633. http://dx.doi.org/10.1093/infdis/153.3.628. (Pubitemid 16135674)
46. Tada H, Aiba S, Shibata K, Ohteki T, Takada H. 2005. Synergistic effect of Nod1 and Nod2 agonists with toll-like receptor agonists on human dendritic cells to generate interleukin-12 and T helper type 1 cells. Infect. Immun. 73:7967-7976. http://dx.doi.org/10.1128/IAI.73.12.7967-7976.2005. (Pubitemid 41740282)
47. Traub S, von Aulock S, Hartung T, Hermann C. 2006. MDP and other muropeptides- direct and synergistic effects on the immune system. J. Endotoxin Res. 12:69-85. http://dx.doi.org/10.1179/096805106X89044. (Pubitemid 47470157)
48. Viala J, Sansonetti P, Philpott DJ. 2004. Nods and 'intracellular' innate immunity. C. R. Biol. 327:551-555. http://dx.doi.org/10.1016/j.crvi.2004.02. 010. (Pubitemid 38979505)
49. Vidal V, Dewulf J, Bahr GM. 2001. Enhanced maturation and functional capacity of monocyte-derived immature dendritic cells by the synthetic immunomodulator murabutide. Immunology 103:479-487. http://dx.doi.org/10.1046/j. 1365-2567.2001.01269.x. (Pubitemid 32744395)
50. Amiel C, De La Tribonniere X, Vidal V, Darcissac E, Mouton Y, Bahr GM. 2002. Clinical tolerance and immunologic effects after single or repeated administrations of the synthetic immunomodulator murabutide in HIV-1-infected patients. J. Acquir. Immune Defic. Syndr. 30:294-305. http://dx.doi.org/10.1097/ 00126334-200207010-00005 http://dx.doi.org/10.1097/00042560-200207010-00005. (Pubitemid 34774077)
51. Jackson EM, Herbst-Kralovetz MM. 2012. Intranasal vaccination with murabutide enhances humoral and mucosal immune responses to a virus-like particle vaccine. PLoS One 7:e41529. http://dx.doi.org/10.1371/journal.pone. 0041529.
52. Ali R, Kumar S, Naqvi RA, Sheikh IA, Rao DN. 2013. Multiple antigen peptide consisting of B- and T-cell epitopes of F1 antigen of Y. pestis showed enhanced humoral and mucosal immune response in different strains of mice. Int. Immunopharmacol. 15:97-105. http://dx.doi.org/10.1016/j.intimp.2012.10.029.
53. Bahr GM, Darcissac E, Bevec D, Dukor P, Chedid L. 1995. Immunopharmacological activities and clinical development of muramyl peptides with particular emphasis on murabutide. Int. J. Immunopharmacol. 17:117-131. http://dx.doi.org/10.1016/0192-0561(94)00094-5.
54. Loving CL, Khurana T, Osorio M, Lee GM, Kelly VK, Stibitz S, Merkel TJ. 2009. Role of anthrax toxins in dissemination, disease progression, and induction of protective adaptive immunity in the mouse aerosol challenge model. Infect. Immun. 77:255-265. http://dx.doi.org/10.1128/IAI.00633-08.
55. Loving CL, Kennett M, Lee GM, Grippe VK, Merkel TJ. 2007. Murine aerosol challenge model of anthrax. Infect. Immun. 75:2689-2698. http://dx.doi.org/10. 1128/IAI.01875-06. (Pubitemid 46870149)
56. Weissleder R, Tung CH, Mahmood U, Bogdanov A, Jr. 1999. In vivo imaging of tumors with protease-activated near-infrared fluorescent probes. Nat. Biotechnol. 17:375-378. http://dx.doi.org/10.1038/7933. (Pubitemid 29166041)
57. Wright JG, Quinn CP, Shadomy S, Messonnier N. 2010. Use of anthrax vaccine in the United States: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2009. MMWR Recomm. Rep. 59(rr06):1-30.
58. Grun JL, Maurer PH. 1989. Different T helper cell subsets elicited in mice utilizing two different adjuvant vehicles: the role of endogenous interleukin 1 in proliferative responses. Cell. Immunol. 121:134-145. http://dx.doi.org/10.1016/0008-8749(89)90011-7. (Pubitemid 19160191)
59. Little SF, Ivins BE, Webster WM, Fellows PF, Pitt ML, Norris SL, Andrews GP. 2006. Duration of protection of rabbits after vaccination with Bacillus anthracis recombinant protective antigen vaccine. Vaccine 24:2530-2536. http://dx.doi.org/10.1016/j.vaccine.2005.12.028. (Pubitemid 43290383)
60. Weeratna RD, Makinen SR, McCluskie MJ, Davis HL. 2005. TLR agonists as vaccine adjuvants: comparison of CpG ODN and Resiquimod (R-848). Vaccine 23:5263-5270. http://dx.doi.org/10.1016/j.vaccine.2005.06.024. (Pubitemid 41443432)