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Review

Bacillus subtilis

A temperature resistant and needle free delivery system of immunogens

&
Pages 979-986 | Received 05 Apr 2012, Accepted 09 May 2012, Published online: 15 Jun 2012

References

  • Negri DR, Riccomi A, Pinto D, Vendetti S, Rossi A, Cicconi R, et al. Persistence of mucosal and systemic immune responses following sublingual immunization. Vaccine 2010; 28:4175 - 80; http://dx.doi.org/10.1016/j.vaccine.2010.04.013; PMID: 20412876
  • Yuki Y, Kiyono H. New generation of mucosal adjuvants for the induction of protective immunity.
  • Neutra MR, Kozlowski PA. Mucosal vaccines: the promise and the challenge. Nat Rev Immunol 2006; 6:148 - 58; http://dx.doi.org/10.1038/nri1777; PMID: 16491139
  • Cuburu N, Kweon MN, Song JH, Hervouet C, Luci C, Sun JB, et al. Sublingual immunization induces broad-based systemic and mucosal immune responses in mice. Vaccine 2007; 25:8598 - 610; http://dx.doi.org/10.1016/j.vaccine.2007.09.073; PMID: 17996991
  • Holmgren J, Czerkinsky C. Mucosal immunity and vaccines. Nat Med 2005; 11:Suppl S45 - 53; http://dx.doi.org/10.1038/nm1213; PMID: 15812489
  • Lee S, Belitsky BR, Brown DW, Brinker JP, Kerstein KO, Herrmann JE, et al. Efficacy, heat stability and safety of intranasally administered Bacillus subtilis spore or vegetative cell vaccines expressing tetanus toxin fragment C. Vaccine 2010; 28:6658 - 65; http://dx.doi.org/10.1016/j.vaccine.2010.08.016; PMID: 20709005
  • Armstrong ME, Lavelle EC, Loscher CE, Lynch MA, Mills KH. Proinflammatory responses in the murine brain after intranasal delivery of cholera toxin: implications for the use of AB toxins as adjuvants in intranasal vaccines. J Infect Dis 2005; 192:1628 - 33; http://dx.doi.org/10.1086/491739; PMID: 16206078
  • Lemiale F, Kong WP, Akyürek LM, Ling X, Huang Y, Chakrabarti BK, et al. Enhanced mucosal immunoglobulin A response of intranasal adenoviral vector human immunodeficiency virus vaccine and localization in the central nervous system. J Virol 2003; 77:10078 - 87; http://dx.doi.org/10.1128/JVI.77.18.10078-10087.2003; PMID: 12941918
  • Fujihashi K, Koga T, van Ginkel FW, Hagiwara Y, McGhee JR. A dilemma for mucosal vaccination: efficacy versus toxicity using enterotoxin-based adjuvants. Vaccine 2002; 20:2431 - 8; http://dx.doi.org/10.1016/S0264-410X(02)00155-X; PMID: 12057597
  • Holmgren J, Czerkinsky C. Mucosal immunity and vaccines. Nat Med 2005; 11:Suppl S45 - 53; http://dx.doi.org/10.1038/nm1213; PMID: 15812489
  • BenMohamed L, Belkaid Y, Loing E, Brahimi K, Gras-Masse H, Druilhe P. Systemic immune responses induced by mucosal administration of lipopeptides without adjuvant. Eur J Immunol 2002; 32:2274 - 81; http://dx.doi.org/10.1002/1521-4141(200208)32:8<2274::AID-IMMU2274>3.0.CO;2-C; PMID: 12209640
  • Zhang H, Zhang J, Streisand JB. Oral mucosal drug delivery: clinical pharmacokinetics and therapeutic applications. Clin Pharmacokinet 2002; 41:661 - 80; http://dx.doi.org/10.2165/00003088-200241090-00003; PMID: 12126458
  • Kozlowski PA, Williams SB, Lynch RM, Flanigan TP, Patterson RR, Cu-Uvin S, et al. Differential induction of mucosal and systemic antibody responses in women after nasal, rectal, or vaginal immunization: influence of the menstrual cycle. J Immunol 2002; 169:566 - 74; PMID: 12077289
  • van Ginkel FW, Jackson RJ, Yuki Y, McGhee JR. Cutting edge: the mucosal adjuvant cholera toxin redirects vaccine proteins into olfactory tissues. J Immunol 2000; 165:4778 - 82; PMID: 11045998
  • Song JH, Nguyen HH, Cuburu N, Horimoto T, Ko SY, Park SH, et al. Sublingual vaccination with influenza virus protects mice against lethal viral infection. Proc Natl Acad Sci U S A 2008; 105:1644 - 9; http://dx.doi.org/10.1073/pnas.0708684105; PMID: 18227512
  • Kozlowski PA, Cu-Uvin S, Neutra MR, Flanigan TP. Comparison of the oral, rectal, and vaginal immunization routes for induction of antibodies in rectal and genital tract secretions of women. Infect Immun 1997; 65:1387 - 94; PMID: 9119478
  • Macdonald TT, Monteleone G. Immunity, inflammation, and allergy in the gut. Science 2005; 307:1920 - 5; http://dx.doi.org/10.1126/science.1106442; PMID: 15790845
  • Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004; 118:229 - 41; http://dx.doi.org/10.1016/j.cell.2004.07.002; PMID: 15260992
  • Hong HA, Duc H, Cutting SM. The use of bacterial spore formers as probiotics. FEMS Microbiol Rev 2005; 29:813 - 35; http://dx.doi.org/10.1016/j.femsre.2004.12.001; PMID: 16102604
  • Green DH, Wakeley PR, Page A, Barnes A, Baccigalupi L, Ricca E, et al. Characterization of two Bacillus probiotics. Appl Environ Microbiol 1999; 65:4288 - 91; PMID: 10473456
  • Oggioni MR, Ciabattini A, Cuppone AM, Pozzi G. Bacillus spores for vaccine delivery. Vaccine 2003; 21:Suppl 2 S96 - 101; http://dx.doi.org/10.1016/S0264-410X(03)00207-X; PMID: 12763690
  • Negri DR, Riccomi A, Pinto D, Vendetti S, Rossi A, Cicconi R, et al. Persistence of mucosal and systemic immune responses following sublingual immunization. Vaccine 2010; 28:4175 - 80; http://dx.doi.org/10.1016/j.vaccine.2010.04.013; PMID: 20412876
  • Detmer A, Glenting J. Live bacterial vaccines--a review and identification of potential hazards. Microb Cell Fact 2006; 5:23; http://dx.doi.org/10.1186/1475-2859-5-23; PMID: 16796731
  • Izadpanah A, Dwinell MB, Eckmann L, Varki NM, Kagnoff MF. Regulated MIP-3alpha/CCL20 production by human intestinal epithelium: mechanism for modulating mucosal immunity. Am J Physiol Gastrointest Liver Physiol 2001; 280:G710 - 9; PMID: 11254498
  • Modlin JF. Poliomyelitis in the United States: the final chapter?. JAMA 2004; 292:1749 - 51; http://dx.doi.org/10.1001/jama.292.14.1749; PMID: 15479943
  • Levine MM, Kaper JB. Live oral vaccines against cholera: an update. Vaccine 1993; 11:207 - 12; http://dx.doi.org/10.1016/0264-410X(93)90019-T; PMID: 8438619
  • Rennels MB, Glass RI, Dennehy PH, Bernstein DI, Pichichero ME, Zito ET, et al, United States Rotavirus Vaccine Efficacy Group. Safety and efficacy of high-dose rhesus-human reassortant rotavirus vaccines--report of the National Multicenter Trial. Pediatrics 1996; 97:7 - 13; PMID: 8545227
  • Belshe RB, Mendelman PM, Treanor J, King J, Gruber WC, Piedra P, et al. The efficacy of live attenuated, cold-adapted, trivalent, intranasal influenzavirus vaccine in children. N Engl J Med 1998; 338:1405 - 12; http://dx.doi.org/10.1056/NEJM199805143382002; PMID: 9580647
  • Iwasaki A, Kelsall BL. Freshly isolated Peyer’s patch, but not spleen, dendritic cells produce interleukin 10 and induce the differentiation of T helper type 2 cells. J Exp Med 1999; 190:229 - 39; http://dx.doi.org/10.1084/jem.190.2.229; PMID: 10432286
  • Wu HY, Weiner HL. Oral tolerance. Immunol Res 2003; 28:265 - 84; http://dx.doi.org/10.1385/IR:28:3:265; PMID: 14713719
  • Miller A, Lider O, Roberts AB, Sporn MB, Weiner HL. Suppressor T cells generated by oral tolerization to myelin basic protein suppress both in vitro and in vivo immune responses by the release of transforming growth factor beta after antigen-specific triggering. Proc Natl Acad Sci U S A 1992; 89:421 - 5; http://dx.doi.org/10.1073/pnas.89.1.421; PMID: 1370356
  • Amuguni H, Lee S, Kerstein KO, Brown DW, Belitsky BR. HerrmannJE, Keusch GT,Sonenshein AL,Tzipori S. Sublingual immunization with an engineered Bacillus subtilis strain expressing tetanus toxin fragment C induces systemic and mucosal immune responses in piglets. [Epub ahead of print] Microbes Infect 2011; PMID: 22198093
  • Bergquist C, Lagergård T, Holmgren J. Anticarrier immunity suppresses the antibody response to polysaccharide antigens after intranasal immunization with the polysaccharide-protein conjugate. Infect Immun 1997; 65:1579 - 83; PMID: 9125533
  • Johansson EL, Rask C, Fredriksson M, Eriksson K, Czerkinsky C, Holmgren J. Antibodies and antibody-secreting cells in the female genital tract after vaginal or intranasal immunization with cholera toxin B subunit or conjugates. Infect Immun 1998; 66:514 - 20; PMID: 9453604
  • Staats HF, Montgomery SP, Palker TJ. Intranasal immunization is superior to vaginal, gastric, or rectal immunization for the induction of systemic and mucosal anti-HIV antibody responses. AIDS Res Hum Retroviruses 1997; 13:945 - 52; http://dx.doi.org/10.1089/aid.1997.13.945; PMID: 9223410
  • Imaoka K, Miller CJ, Kubota M, McChesney MB, Lohman B, Yamamoto M, et al. Nasal immunization of nonhuman primates with simian immunodeficiency virus p55gag and cholera toxin adjuvant induces Th1/Th2 help for virus-specific immune responses in reproductive tissues. J Immunol 1998; 161:5952 - 8; PMID: 9834076
  • Rudin A, Riise GC, Holmgren J. Antibody responses in the lower respiratory tract and male urogenital tract in humans after nasal and oral vaccination with cholera toxin B subunit. Infect Immun 1999; 67:2884 - 90; PMID: 10338495
  • Amuguni JH, Lee S, Kerstein KO, Brown DW, Belitsky BR, Herrmann JE, et al. Sublingually administered Bacillus subtilis cells expressing tetanus toxin C fragment induce protective systemic and mucosal antibodies against tetanus toxin in mice. Vaccine 2011; 29:4778 - 84; http://dx.doi.org/10.1016/j.vaccine.2011.04.083; PMID: 21565244
  • Cuburu N, Kweon MN, Hervouet C, Cha HR, Pang YY, Holmgren J, et al. Sublingual immunization with nonreplicating antigens induces antibody-forming cells and cytotoxic T cells in the female genital tract mucosa and protects against genital papillomavirus infection. J Immunol 2009; 183:7851 - 9; http://dx.doi.org/10.4049/jimmunol.0803740; PMID: 19933861
  • Kildsgaard J, Brimnes J, Jacobi H, Lund K. Sublingual immunotherapy in sensitized mice. Ann Allergy Asthma Immunol 2007; 98:366 - 72; http://dx.doi.org/10.1016/S1081-1206(10)60884-8; PMID: 17458434
  • Duc H, Hong HA, Fairweather N, Ricca E, Cutting SM. Bacterial spores as vaccine vehicles. Infect Immun 2003; 71:2810 - 8; http://dx.doi.org/10.1128/IAI.71.5.2810-2818.2003; PMID: 12704155
  • Hoang TH, Hong HA, Clark GC, Titball RW, Cutting SM. Recombinant B. subtilis Expressing the Clostridium perfringens Alpha Toxoid Is a Candidate Orally Delivered Vaccine against Necrotic Enteritis. Infect Immun 2008 November 1, 2008; 76(11):5257-65.
  • Boucher P, Sato H, Sato Y, Locht C. Neutralizing antibodies and immunoprotection against pertussis and tetanus obtained by use of a recombinant pertussis toxin-tetanus toxin fusion protein. Infect Immun 1994; 62:449 - 56; PMID: 7507893
  • Zhou Z, Xia H, Hu X, Huang Y, Li Y, Li L, et al. Oral administration of a Bacillus subtilis spore-based vaccine expressing Clonorchis sinensis tegumental protein 22.3 kDa confers protection against Clonorchis sinensis. Vaccine 2008; 26:1817 - 25; http://dx.doi.org/10.1016/j.vaccine.2008.02.015; PMID: 18329763
  • Turnbull PC. Anthrax vaccines: past, present and future. Vaccine 1991; 9:533 - 9; http://dx.doi.org/10.1016/0264-410X(91)90237-Z; PMID: 1771966
  • Hoa NT, Baccigalupi L, Huxham A, Smertenko A, Van PH, Ammendola S, et al. Characterization of Bacillus species used for oral bacteriotherapy and bacterioprophylaxis of gastrointestinal disorders. Appl Environ Microbiol 2000; 66:5241 - 7; http://dx.doi.org/10.1128/AEM.66.12.5241-5247.2000; PMID: 11097897
  • Senesi S, Celandroni F, Tavanti A, Ghelardi E. Molecular characterization and identification of Bacillus clausii Strains marketed for use in oral bacteriotherapy. Appl Environ Microbiol 2001; 67:834 - 9; http://dx.doi.org/10.1128/AEM.67.2.834-839.2001; PMID: 11157251
  • O’Hagan DT, MacKichan ML, Singh M. Recent developments in adjuvants for vaccines against infectious diseases. Biomol Eng 2001; 18:69 - 85; http://dx.doi.org/10.1016/S1389-0344(01)00101-0; PMID: 11566599
  • Huang J-M, Hong HA, Van Tong H, Hoang TH, Brisson A, Cutting SM. Mucosal delivery of antigens using adsorption to bacterial spores. Vaccine 2010; 28:1021 - 30; http://dx.doi.org/10.1016/j.vaccine.2009.10.127; PMID: 19914191
  • Wang Y, Zhang Z. [Bacterial spore--a new vaccine vehicle--a review]. Wei Sheng Wu Xue Bao 2008; 48:413 - 7; PMID: 18479073
  • The Trouble in Tracing Opportunistic Pathogens. Cholangitis due to Bacillus in a French Hospital Caused by a Strain Related to an Italian Probiotic?. Microb Ecol Health Dis 2000; 12:99 - 101; http://dx.doi.org/10.1080/089106000435491
  • Wang J, Fung DY. Alkaline-fermented foods: a review with emphasis on pidan fermentation. Crit Rev Microbiol 1996; 22:101 - 38; http://dx.doi.org/10.3109/10408419609106457; PMID: 8817079
  • Raychaudhuri S, Rock KL. Fully mobilizing host defense: building better vaccines. Nat Biotechnol 1998; 16:1025 - 31; http://dx.doi.org/10.1038/3469; PMID: 9831030
  • Simon O, Vahjen W, Taras D. Potential of probiotics in pig nutrition. Feed Mix (2007) 15, pp. 2-3. 34.
  • Hong HA, Duc H, Cutting SM. The use of bacterial spore formers as probiotics. FEMS Microbiol Rev 2005; 29:813 - 35; http://dx.doi.org/10.1016/j.femsre.2004.12.001; PMID: 16102604
  • Barnes AG, Cerovic V, Hobson PS, Klavinskis LS. Bacillus subtilis spores: a novel microparticle adjuvant which can instruct a balanced Th1 and Th2 immune response to specific antigen. Eur J Immunol 2007; 37:1538 - 47; http://dx.doi.org/10.1002/eji.200636875; PMID: 17474150
  • Duc H, Hong HA, Fairweather N, Ricca E, Cutting SM. Bacterial spores as vaccine vehicles. Infect Immun 2003; 71:2810 - 8; http://dx.doi.org/10.1128/IAI.71.5.2810-2818.2003; PMID: 12704155
  • Hoang TH, Hong HA, Clark GC, Titball RW, Cutting SM. Recombinant Bacillus subtilis expressing the Clostridium perfringens alpha toxoid is a candidate orally delivered vaccine against necrotic enteritis. Infect Immun 2008; 76:5257 - 65; http://dx.doi.org/10.1128/IAI.00686-08; PMID: 18779344
  • Bumann D, Hueck C, Aebischer T, Meyer TF. Recombinant live Salmonella spp. for human vaccination against heterologous pathogens. FEMS Immunol Med Microbiol 2000; 27:357 - 64; http://dx.doi.org/10.1111/j.1574-695X.2000.tb01450.x; PMID: 10727892
  • Casula G, Cutting SM. Bacillus probiotics: spore germination in the gastrointestinal tract. Appl Environ Microbiol 2002; 68:2344 - 52; http://dx.doi.org/10.1128/AEM.68.5.2344-2352.2002; PMID: 11976107
  • Duc H, Hong HA, Cutting SM. Germination of the spore in the gastrointestinal tract provides a novel route for heterologous antigen delivery. Vaccine 2003; 21:4215 - 24; http://dx.doi.org/10.1016/S0264-410X(03)00492-4; PMID: 14505901
  • Driks A. Bacillus subtilis spore coat. Microbiol Mol Biol Rev 1999; 63:1 - 20; PMID: 10066829
  • Rhee KJ, Sethupathi P, Driks A, Lanning DK, Knight KL. Role of commensal bacteria in development of gut-associated lymphoid tissues and preimmune antibody repertoire. J Immunol 2004; 172:1118 - 24; PMID: 14707086
  • Isticato R, Cangiano G, Tran HT, Ciabattini A, Medaglini D, Oggioni MR, et al. Surface display of recombinant proteins on Bacillus subtilis spores. J Bacteriol 2001; 183:6294 - 301; http://dx.doi.org/10.1128/JB.183.21.6294-6301.2001; PMID: 11591673
  • Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, Azevedo V, et al. The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 1997; 390:249 - 56; http://dx.doi.org/10.1038/36786; PMID: 9384377
  • Medaglini D, Ciabattini A, Spinosa MR, Maggi T, Marcotte H, Oggioni MR, et al. Immunization with recombinant Streptococcus gordonii expressing tetanus toxin fragment C confers protection from lethal challenge in mice. Vaccine 2001; 19:1931 - 9; http://dx.doi.org/10.1016/S0264-410X(00)00434-5; PMID: 11228363
  • Robinson K, Chamberlain LM, Schofield KM, Wells JM, Le Page RW. Oral vaccination of mice against tetanus with recombinant Lactococcus lactis. Nat Biotechnol 1997; 15:653 - 7; http://dx.doi.org/10.1038/nbt0797-653; PMID: 9219268
  • Trollfors B, Knutsson N, Taranger J, Mark A, Bergfors E, Sundh V, et al. Diphtheria, tetanus and pertussis antibodies in 10-year-old children before and after a booster dose of three toxoids: implications for the timing of a booster dose. Eur J Pediatr 2006; 165:14 - 8; http://dx.doi.org/10.1007/s00431-005-1763-3; PMID: 16249929
  • Rappuoli R, Pizza M, Douce G, Dougan G. Structure and mucosal adjuvanticity of cholera and Escherichia coli heat-labile enterotoxins. Immunol Today 1999; 20:493 - 500; http://dx.doi.org/10.1016/S0167-5699(99)01523-6; PMID: 10529776
  • Ciabattini A, Parigi R, Isticato R, Oggioni MR, Pozzi G. Oral priming of mice by recombinant spores of Bacillus subtilis. Vaccine 2004; 22:4139 - 43; http://dx.doi.org/10.1016/j.vaccine.2004.05.001; PMID: 15474704
  • Lee S, Belitsky BR, Brinker JP, Kerstein KO, Brown DW, Clements JD, et al. Development of a Bacillus subtilis-based rotavirus vaccine. Clin Vaccine Immunol 2010; 17:1647 - 55; http://dx.doi.org/10.1128/CVI.00135-10; PMID: 20810679
  • Helting TB, Nau HH. Analysis of the immune response to papain digestion products of tetanus toxin. Acta Pathol Microbiol Immunol Scand C 1984; 92:59 - 63; PMID: 6711309
  • Lavelle EC, O’Hagan DT. Delivery systems and adjuvants for oral vaccines. Expert Opin Drug Deliv 2006; 3:747 - 62; http://dx.doi.org/10.1517/17425247.3.6.747; PMID: 17076597
  • Chadwick S, Kriegel C, Amiji M. Delivery strategies to enhance mucosal vaccination. Expert Opin Biol Ther 2009; 9:427 - 40; http://dx.doi.org/10.1517/14712590902849224; PMID: 19344280
  • Mauriello EM, Duc H, Isticato R, Cangiano G, Hong HA, De Felice M, et al. Display of heterologous antigens on the Bacillus subtilis spore coat using CotC as a fusion partner. Vaccine 2004; 22:1177 - 87; http://dx.doi.org/10.1016/j.vaccine.2003.09.031; PMID: 15003646
  • Byrne MP, Smith TJ, Montgomery VA, Smith LA. Purification, potency, and efficacy of the botulinum neurotoxin type A binding domain from Pichia pastoris as a recombinant vaccine candidate. Infect Immun 1998; 66:4817 - 22; PMID: 9746584
  • Umland TC, Wingert LM, Swaminathan S, Furey WF, Schmidt JJ, Sax M. Structure of the receptor binding fragment HC of tetanus neurotoxin. Nat Struct Biol 1997; 4:788 - 92; http://dx.doi.org/10.1038/nsb1097-788; PMID: 9334741
  • Emsley P, Fotinou C, Black I, Fairweather NF, Charles IG, Watts C, et al. The structures of the H(C) fragment of tetanus toxin with carbohydrate subunit complexes provide insight into ganglioside binding. J Biol Chem 2000; 275:8889 - 94; http://dx.doi.org/10.1074/jbc.275.12.8889; PMID: 10722735
  • Lacy DB, Stevens RC. Sequence homology and structural analysis of the clostridial neurotoxins. J Mol Biol 1999; 291:1091 - 104; http://dx.doi.org/10.1006/jmbi.1999.2945; PMID: 10518945

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