Attenuated Bordetella pertussis BPZE1 as a live vehicle for heterologous vaccine antigens delivery through the nasal route

Bioengineered Bugs

Volumn 2, Issue 6, 2011, Pages

  Li, Rui ^a,b   Lim, Annabelle ^a   Alonso, Sylvie ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b FUDAN UNIVERSITY   (China)

Author keywords

Adenylate cyclase; Autotransporter BrkA; Bordetella pertussis; BPZE1; Filamentous hemagglutinin FHA; Heterologous antigens; Live attenuated bacteria; Nasal vaccine delivery

Indexed keywords

ADENYLATE CYCLASE TOXIN; BACTERIAL ANTIGEN; DRUG CARRIER; HETEROLOGOUS ANTIGEN; PERTUSSIS TOXIN; PERTUSSIS VACCINE; RECOMBINANT VACCINE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANTIGEN PRESENTATION; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BORDETELLA PERTUSSIS; DRUG DELIVERY SYSTEM; HUMAN; IMMUNE RESPONSE; MUCOSAL IMMUNITY; NOSE MUCOSA; PERTUSSIS; PHASE 1 CLINICAL TRIAL (TOPIC); RESPIRATORY TRACT INFECTION; REVIEW; VACCINATION;

BORDETELLA PERTUSSIS;

EID: 80955149208     PISSN: 19491018     EISSN: 19491026     Source Type: Journal    
DOI: 10.4161/bbug.2.6.18167     Document Type: Review

References (55)

1. Chadwick S, Kriegel C, Amiji M. Delivery strategies to enhance mucosal vaccination. Expert Opin Biol Ther 2009; 9:427-40; PMID:19344280; DOI:10.1517/14712590902849224.
2. Garmory HS, Leary SE, Griffin KF, Williamson ED, Brown KA, Titball RW. The use of live attenuated bacteria as a delivery system for heterologous antigens. J Drug Target 2003; 11:471-9; PMID:15203915; DOI:10.1080/10611860410001670008.
3. Thole JE, van Dalen PJ, Havenith CE, Pouwels PH, Seegers JF, Tielen FD, et al. Live bacterial delivery systems for development of mucosal vaccines. Curr Opin Mol Ther 2000; 2:94-9; PMID:11249657.
4. De Magistris MT. Mucosal delivery of vaccine antigens and its advantages in pediatrics. Adv Drug Deliv Rev 2006; 58:52-67; PMID:16516335; DOI:10.1016/j. addr.2006.01.002.
5. de Gouw D, Diavatopoulos DA, Bootsma HJ, Hermans PW, Mooi FR. Pertussis: a matter of immune modulation. FEMS Microbiol Rev 2011; 35:441-74; PMID:21204863; DOI:10.1111/j.1574-6976.2010.00257.x.
6. Alonso S, Willery E, Renauld-Mongenie G, Locht C. Production of nontypeable Haemophilus influenzae HtrA by recombinant Bordetella pertussis with the use of filamentous hemagglutinin as a carrier. Infect Immun 2005; 73:4295-301; PMID:15972522; DOI:10.1128/ IAI.73.7.4295-301.2005.
7. Rijpkema SG, Adams T, Rigsby P, Xing DK, Corbel MJ. Investigation in a model system of the effects of combinations of anthrax and pertussis vaccines administered to service personnel in the 1991 Gulf War. Hum Vaccin 2005; 1:165-9; PMID:17012879; DOI:10.4161/hv.1.4.1989.
8. Roberts M, Maskell D, Novotny P, Dougan G. Construction and characterization in vivo of Bordetella pertussis aroA mutants. Infect Immun 1990; 58:732-9; PMID:2407655.
9. Mielcarek N, Riveau G, Remoue F, Antoine R, Capron A, Locht C. Homologous and heterologous protection after single intranasal administration of live attenuated recombinant Bordetella pertussis. Nat Biotechnol 1998; 16:454-7; PMID:9592394; DOI:10.1038/nbt0598-454.
10. Coppens I, Alonso S, Antoine R, Jacob-Dubuisson F, Renauld-Mongenie G, Jacobs E, et al. Production of Neisseria meningitidis transferrin-binding protein B by recombinant Bordetella pertussis. Infect Immun 2001; 69:5440-6; PMID:11500415; DOI:10.1128/ IAI.69.9.5440-6.2001.
11. Reveneau N, Alonso S, Jacob-Dubuisson F, Mercenier A, Locht C. Tetanus toxin fragment C-specific priming by intranasal infection with recombinant Bordetella pertussis. Vaccine 2001; 20:926-33; PMID:11738759; DOI:10.1016/S0264-410X(01)00380-2.
12. Mielcarek N, Debrie AS, Raze D, Bertout J, Rouanet C, Younes AB, et al. Live attenuated B. pertussis as a single-dose nasal vaccine against whooping cough. PLoS Pathog 2006; 2:65; PMID:16839199; DOI:10.1371/ journal.ppat.0020065.
13. Feunou PF, Ismaili J, Debrie AS, Huot L, Hot D, Raze D, et al. Genetic stability of the live attenuated Bordetella pertussis vaccine candidate BPZE1. Vaccine 2008; 26:5722-7; PMID:18762220; DOI:10.1016/j. vaccine.2008.08.018.
14. Skerry CM, Cassidy JP, English K, Feunou-Feunou P, Locht C, Mahon BP. A live attenuated Bordetella pertussis candidate vaccine does not cause disseminating infection in gamma interferon receptor knockout mice. Clin Vaccine Immunol 2009; 16:1344-51; PMID:19625486; DOI:10.1128/CVI.00082-09.
15. Fedele G, Bianco M, Debrie AS, Locht C, Ausiello CM. Attenuated Bordetella pertussis vaccine candidate BPZE1 promotes human dendritic cell CCL21-induced migration and drives a Th1/Th17 response. J Immunol 2011; 186:5388-96; PMID:21430219; DOI:10.4049/jimmunol.1003765.
16. World Health Organization (WHO) http://www.who.int/en/
17. Bamberger ES, Srugo I. What is new in pertussis? Eur J Pediatr 2008; 167:133-9; PMID:17668241; DOI:10.1007/s00431-007-0548-2.
18. He Q, Mertsola J. Factors contributing to pertussis resurgence. Future Microbiol 2008; 3:329-39; PMID:18505398; DOI:10.2217/17460913.3.3.329.
19. von König CH, Halperin S, Riffelmann M, Guiso N. Pertussis of adults and infants. Lancet Infect Dis 2002; 2:744-50; PMID:12467690; DOI:10.1016/S1473-3099(02)00452-8.
20. Ho SY, Chua SQ, Foo DG, Locht C, Chow VT, Poh CL, et al. Highly attenuated Bordetella pertussis strain BPZE1 as a potential live vehicle for delivery of heterologous vaccine candidates. Infect Immun 2008; 76:111-9; PMID:17954727; DOI:10.1128/IAI.00795-07.
21. Li R, Lim A, Ow ST, Phoon MC, Locht C, Chow VT, et al. Development of live attenuated Bordetella pertussis strains expressing the universal influenza vaccine candidate M2e. Vaccine 2011; 29:5502-11; PMID:21624415; DOI:10.1016/j.vaccine.2011.05.052.
22. Renauld-Mongénie G, Cornette J, Mielcarek N, Menozzi FD, Locht C. Distinct roles of the N-terminal and C-terminal precursor domains in the biogenesis of the Bordetella pertussis filamentous hemagglutinin. J Bacteriol 1996; 178:1053-60; PMID:8576038.
23. Clantin B, Delattre AS, Rucktooa P, Saint N, Meli AC, Locht C, et al. Structure of the membrane protein FhaC: a member of the Omp85-TpsB transporter superfamily. Science 2007; 317:957-61; PMID:17702945; DOI:10.1126/science.1143860.
24. Hodak H, Clantin B, Willery E, Villeret V, Locht C, Jacob-Dubuisson F. Secretion signal of the filamentous haemagglutinin, a model two-partner secretion substrate. Mol Microbiol 2006; 61:368-82; PMID:16771844; DOI:10.1111/j.1365-2958.2006.05242.x.
25. Alonso S, Reveneau N, Pethe K, Locht C. Eightykilodalton N-terminal moiety of Bordetella pertussis filamentous hemagglutinin: adherence, immunogenicity and protective role. Infect Immun 2002; 70:4142-7; PMID:12117922; DOI:10.1128/IAI.70.8.4142-7.2002.
26. Mielcarek N, Cornette J, Schacht AM, Pierce RJ, Locht C, Capron A, et al. Intranasal priming with recombinant Bordetella pertussis for the induction of a systemic immune response against a heterologous antigen. Infect Immun 1997; 65:544-50; PMID:9009311.
27. Hodak H, Jacob-Dubuisson F. Current challenges in autotransport and two-partner protein secretion pathways. Res Microbiol 2007; 158:631-7; PMID:17913468; DOI:10.1016/j.resmic.2007.08.001.
28. Ruiz-Olvera P, Ruiz-Pérez F, Sepulveda NV, Santiago-Machuca A, Maldonado-Rodríguez R, Garcia-Elorriaga G, et al. Display and release of the Plasmodium falciparum circumsporozoite protein using the autotransporter MisL of Salmonella enterica. Plasmid 2003; 50:12-27; PMID:12826054; DOI:10.1016/S0147-619X(03)00047-7.
29. Zhu C, Ruiz-Perez F, Yang Z, Mao Y, Hackethal VL, Greco KM, et al. Delivery of heterologous protein antigens via hemolysin or autotransporter systems by an attenuated ler mutant of rabbit enteropathogenic Escherichia coli. Vaccine 2006; 24:3821-31; PMID:16098637; DOI:10.1016/j.vaccine.2005.07.024.
30. Veiga E, de Lorenzo V, Fernández LA. Structural tolerance of bacterial autotransporters for folded passenger protein domains. Mol Microbiol 2004; 52:1069-80; PMID:15130125; DOI:10.1111/j.1365-2958.2004.04014.x.
31. Barnes MG, Weiss AA. BrkA protein of Bordetella pertussis inhibits the classical pathway of complement after C1 deposition. Infect Immun 2001; 69:3067-72; PMID:11292725; DOI:10.1128/IAI.69.5.3067-72.2001.
32. Elder KD, Harvill ET. Strain-dependent role of BrkA during Bordetella pertussis infection of the murine respiratory tract. Infect Immun 2004; 72:5919-24; PMID:15385494; DOI:10.1128/IAI.72.10.5919-24.2004.
33. Oliver DC, Huang G, Nodel E, Pleasance S, Fernandez RC. A conserved region within the Bordetella pertussis autotransporter BrkA is necessary for folding of its passenger domain. Mol Microbiol 2003; 47:1367-83; PMID:12603741; DOI:10.1046/j.1365-2958.2003.03377.x.
34. Cainelli Gebara VC, Risoléo L, Lopes AP, Ferreira VR, Quintilio W, Lépine F, et al. Adjuvant and immunogenic activities of the 73 kDa N-terminal alpha-domain of BrkA autotransporter and Cpn60/60 kDa chaperonin of Bordetella pertussis. Vaccine 2007; 25:621-9; PMID:17011680; DOI:10.1016/j.vaccine.2006.08.033.
35. Xin KW, Chow VT, Alonso S. Exploring the versatility of the autotransporter BrkA for the presentation of Enterovirus 71 vaccine candidates at the surface of attenuated Bordetella pertussis. Procedia in Vaccinology 2009; 2:66-72.
36. Harvill ET, Cotter PA, Yuk MH, Miller JF. Probing the function of Bordetella bronchiseptica adenylate cyclase toxin by manipulating host immunity. Infect Immun 1999; 67:1493-500; PMID:10024599.
37. + T cell epitopes. J Immunol 1996; 156:4697-706; PMID:8648115.
38. Tartz S, Rüssmann H, Kamanova J, Sebo P, Sturm A, Heussler V, et al. Complete protection against P. berghei malaria upon heterologous prime/boost immunization against circumsporozoite protein employing Salmonella type III secretion system and Bordetella adenylate cyclase toxoid. Vaccine 2008; 26:5935-43; PMID:18804138; DOI:10.1016/j.vaccine.2008.08.057.
39. Loucká J, Schlecht G, Vodolánová J, Leclerc C, Sebo P. Delivery of a MalE CD4(+)-T-cell epitope into the major histocompatibility complex class II antigen presentation pathway by Bordetella pertussis adenylate cyclase. Infect Immun 2002; 70:1002-5; PMID:11796640.
40. Ladant D, Glaser P, Ullmann A. Insertional mutagenesis of Bordetella pertussis adenylate cyclase. J Biol Chem 1992; 267:2244-50; PMID:1733931.
41. Osicka R, Osicková A, Basar T, Guermonprez P, Rojas M, Leclerc C, et al. Delivery of CD8(+) T-cell epitopes into major histocompatibility complex class I antigen presentation pathway by Bordetella pertussis adenylate cyclase: delineation of cell invasive structures and permissive insertion sites. Infect Immun 2000; 68:247-56; PMID:10603395; DOI:10.1128/IAI.68.1.247-56.2000.
42. Fayolle C, Osickova A, Osicka R, Henry T, Rojas MJ, Saron MF, et al. Delivery of multiple epitopes by recombinant detoxified adenylate cyclase of Bordetella pertussis induces protective antiviral immunity. J Virol 2001; 75:7330-8; PMID:11462005; DOI:10.1128/ JVI.75.16.7330-8.2001.
43. + T cell epitope from lymphocytic choriomeningitis virus. Proc Natl Acad Sci USA 1997; 94:3314-9; PMID:9096390; DOI:10.1073/ pnas.94.7.3314.
44. Karimova G, Fayolle C, Gmira S, Ullmann A, Leclerc C, Ladant D. Charge-dependent translocation of Bordetella pertussis adenylate cyclase toxin into eukaryotic cells: implication for the in vivo delivery of CD8(+) T cell epitopes into antigen-presenting cells. Proc Natl Acad Sci USA 1998; 95:12532-7; PMID:9770520; DOI:10.1073/pnas.95.21.12532.
45. Simsova M, Sebo P, Leclerc C. The adenylate cyclase toxin from Bordetella pertussis-a novel promising vehicle for antigen delivery to dendritic cells. Int J Med Microbiol 2004; 293:571-6; PMID:15149033; DOI:10.1078/1438-4221-00291.
46. Relman DA, Domenighini M, Tuomanen E, Rappuoli R, Falkow S. Filamentous hemagglutinin of Bordetella pertussis: nucleotide sequence and crucial role in adherence. Proc Natl Acad Sci USA 1989; 86:2637-41; PMID:2539596; DOI:10.1073/pnas.86.8.2637.
47. Tamura M, Nogimori K, Murai S, Yajima M, Ito K, Katada T, et al. Subunit structure of islet-activating protein, pertussis toxin, in conformity with the A-B model. Biochemistry 1982; 21:5516-22; PMID:6293544; DOI:10.1021/bi00265a021.
48. Hanski E, Farfel Z. Bordetella pertussis invasive adenylate cyclase. Partial resolution and properties of its cellular penetration. J Biol Chem 1985; 260:5526-32; PMID:2859287.
49. Wilson R, Read R, Thomas M, Rutman A, Harrison K, Lund V, et al. Effects of Bordetella pertussis infection on human respiratory epithelium in vivo and in vitro. Infect Immun 1991; 59:337-45; PMID:1987048.
50. Walker KE, Weiss AA. Characterization of the dermonecrotic toxin in members of the genus Bordetella. Infect Immun 1994; 62:3817-28; PMID:8063398.
51. Wilson R, Read R, Thomas M, Rutman A, Harrison K, Lund V, et al. Effects of Bordetella pertussis infection on human respiratory epithelium in vivo and in vitro. Infect Immun 1991; 59:337-45; PMID:1987048.
52. Leininger E, Roberts M, Kenimer JG, Charles IG, Fairweather N, Novotny P, et al. Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc Natl Acad Sci USA 1991; 88:345-9; PMID:1988935; DOI:10.1073/pnas.88.2.345.
53. Geuijen CA, Willems RJ, Bongaerts M, Top J, Gielen H, Mooi FR. Role of the Bordetella pertussis minor fimbrial subunit, FimD, in colonization of the mouse respiratory tract. Infect Immun 1997; 65:4222-8; PMID:9317030.
54. Fernandez RC, Weiss AA. Cloning and sequencing of a Bordetella pertussis serum resistance locus. Infect Immun 1994; 62:4727-38; PMID:7927748.
55. Amano K, Fukushi K, Watanabe M. Biochemical and immunological comparison of lipopolysaccharides from Bordetella species. J Gen Microbiol 1990; 136:481-7; PMID:2118165.