Non-toxic derivatives of LT as potent adjuvants

Vaccine

Volumn 29, Issue 8, 2011, Pages 1538-1544

  da Hora, Vanusa P ^a,b,c   Conceição, Fabricio R ^b   Dellagostin, Odir A ^b   Doolan, Denise L ^a  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b FEDERAL UNIVERSITY OF PELOTAS   (Brazil)

^c FEDERAL UNIVERSITY OF RIO GRANDE   (Brazil)

Author keywords

Adjuvant; LT; LTB; LTK63

Indexed keywords

A PR8 PROTEIN; BACTERIAL PROTEIN; CARCINOEMBRYONIC ANTIGEN; ESCHERICHIA COLI ENTEROTOXIN; GAMMA INTERFERON; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G3; IMMUNOMODULATING AGENT; INTERLEUKIN 2; KEYHOLE LIMPET HEMOCYANIN; KNOB PROTEIN; LTB; LTK63; MENINGOCOCCAL SEROGROUP C POLYSACCHARIDE CONJUGATE; PBCSP 242 310 PROTEIN; PNC1 TT PROTEIN; PROTEIN VP2; R1 PROTEIN; SUID HERPESVIRUS TYPE 1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; UREASE; VIRUS PROTEIN;

ADENOVIRUS INFECTION; ADJUVANT THERAPY; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIBODY TITER; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CYTOKINE RESPONSE; DENDRITIC CELL; DOSE RESPONSE; DRUG ACTIVITY; DRUG MEGADOSE; DRUG RECEPTOR BINDING; DRUG STRUCTURE; GRANULOCYTE; HELICOBACTER INFECTION; HERPES VIRUS INFECTION; HUMAN PAPILLOMAVIRUS TYPE 16; IMMUNOGENICITY; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOLOGICAL MEMORY; IMMUNOMODULATION; INFECTIOUS BURSAL DISEASE; INFLUENZA; MACROPHAGE; MUCOSAL IMMUNITY; MYCOPLASMOSIS; NATURAL KILLER CELL; NEOPLASM; NONHUMAN; PAPILLOMA; PERTUSSIS; PLASMODIUM BERGHEI INFECTION; PRIORITY JOURNAL; PROTOZOAL INFECTION; REVIEW; STREPTOCOCCUS PNEUMONIA; TH1 CELL; TH2 CELL; TOXOPLASMOSIS; TUBERCULOSIS;

EID: 79952693976     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2010.11.091     Document Type: Review

References (81)

1. Cooper MR, Stewart DC, Kahl FR, Brown WM, Cordell AR. Medicine at the medical center then and now: one hundred years of progress. South Med J 2002;95(October (10)):1113-21.
2. Mbow ML, De Gregorio E, Valiante NM, Rappuoli R. New adjuvants for human vaccines. Curr Opin Immunol Jun 2010;22(3):411-6.
3. Reed SG, Bertholet S,Coler RN, Friede M. New orizonsinadjuvants for vaccine development. Trends Immunol 2009;30(January (1)):23-32.
4. Cox JC, Coulter AR. Adjuvants-a classification and review of their modes of action. Vaccine 1997;15(February (3)):248-56.
5. Pashine A, Valiante NM, Ulmer JB. Targeting the innate immune response with improved vaccine adjuvants. Nat Med 2005;11(April (Suppl. 4)):S63-8.
6. O'Hagan DT, Valiante NM. Recent advances in the discovery and delivery of vaccine adjuvants. Nat Rev Drug Discov 2003;2(September (9)):727-35.
7. Guy B.The perfect mix: recent progressinadjuvant research. Nat Rev Microbiol 2007;5(July (7)):505-17.
8. Schijns V, Brewer J. Immunopotentiators in modern vaccines (IMV-II) held in Malaga, Spain, May 18-20, 2005. Vaccine 2006;24(June (26)):5391-2.
9. Tritto E, Mosca F, De Gregorio E. Mechanism of action of licensed vaccine adjuvants. Vaccine 2009;27(May (25-26)):3331-4.
10. Cooper CL, Davis HL, Morris ML, Efler SM, Adhami MA, Krieg AM, et al. CPG 7909, an immunostimulatory TLR9 agonist oligodeoxynucleotide, as adjuvant to Engerix-B HBV vaccine in healthy adults: a double-blind phase I/II study. J Clin Immunol 2004;24(November (6)):693-701.
11. Kaisho T, Akira S. Toll-like receptors as adjuvant receptors. Biochim Biophys Acta 2002;1589(February (1)):1-13.
12. Aucouturier J, Dupuis L, Deville S, Ascarateil S, Ganne V, Montanide ISA. 720 and 51: a new generation of water in oil emulsions as adjuvants for human vaccines. Expert Rev Vaccines 2002;1(June (1)):111-8.
13. Simmons CP, Ghaem-Magami M, Petrovska L, Lopes L, Chain BM, Williams NA, et al. Immunomodulation using bacterial enterotoxins. Scand J Immunol 2001;53(March (3)):218-26.
14. Conceicao FR, Moreira AN, Dellagostin OA. A recombinant chimera composed of R1 repeat region of Mycoplasma hyopneumoniae P97 adhesin with Escherichia coli heat-labile enterotoxin B subunit elicits immune response in mice. Vaccine 2006;24(July (29-30)):5734-43.
15. Romero JF, Ciabattini A, Guillaume P, Frank G, Ruggiero P, Pettini E, et al. Intranasal administration of the synthetic polypeptide from the C-terminus of the circumsporozoite protein of Plasmodium berghei with the modified heat-labile toxin of Escherichia coli (LTK63) induces a complete protection against malaria challenge. Vaccine 2009;27(February (8)):1266-71.
16. Yamamoto T, Tamura T, Yokota T. Primary structure of heat-labile enterotoxin produced by Escherichia coli pathogenic for humans. J Biol Chem 1984;259(April (8)):5037-44.
17. Hofstra H,WitholtB. Heat-labile enterotoxin inEscherichia coli. Kinetics of associationofsubunits into periplasmic holotoxin. J Biol Chem 1985;260(December (29)):16037-44.
18. Sixma TK, Kalk KH, van Zanten BA, Dauter Z, Kingma J, Witholt B, et al. Refined structure of Escherichia coli heat-labile enterotoxin, a close relative of cholera toxin. J Mol Biol 1993;230(April (3)):890-918.
19. Sixma TK, Pronk SE, Kalk KH, Wartna ES, van Zanten BA, Witholt B,et al. Crystal structure of a cholera toxin-related heat-labile enterotoxin from E. coli. Nature 1991;351(May (6325)):371-7.
20. Gill DM, Rappaport RS. Origin of the enzymatically active A1 fragment of cholera toxin. J Infect Dis 1979;139(June (6)):674-80.
21. Spangler BD. Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol Rev 1992;56(December (4)):622-47.
22. de Haan L, Verweij WR, Feil IK, Holtrop M, Hol WG, Agsteribbe E, et al. Role of GM1 binding in the mucosal immunogenicity and adjuvant activity of the Escherichia coli heat-labile enterotoxin and its B subunit. Immunology 1998;94(July (3)):424-30.
23. Pizza M,Giuliani MM, Fontana MR, Monaci E,Douce G,Dougan G,etal. Mucosal vaccines: non toxic derivatives of LT and CT as mucosal adjuvants. Vaccine 2001;19(March (17-19)):2534-41.
24. Alone PV, Garg LC, Secretory. GM1 receptor binding role of N-terminal region of LTB in Vibrio cholerae. Biochem Biophys Res Commun 2008;376(November (4)):770-4.
25. Ryan EJ, McNeela E, Pizza M, Rappuoli R, O'Neill L, Mills KH. Modulation of innate and acquired immune responses by Escherichia coli heat-labile toxin: distinct pro- and anti-inflammatory effects of the nontoxic AB complex and the enzyme activity. J Immunol 2000;165(November (10)):5750-9.
26. Petrovska L,Lopes L, Simmons CP, Pizza M, Dougan G,Chain BM. Modulation of dendritic cell endocytosis and antigen processing pathways by Escherichia coli heat-labile enterotoxin and mutant derivatives. Vaccine 2003;21(March (13-14)):1445-54.
27. Pitcovski J, Bazak Z, Wasserman E, Elias O, Levy A, Peretz T, et al. Heat labile enterotoxin of E. coli: a potential adjuvant for transcutaneous cancer immunotherapy. Vaccine 2006;24(January (5)):636-43.
28. Fu N, Khan S, Quinten E, de Graaf N, Pemberton AJ, Rivett AJ, et al. Effective CD8(+) T cell priming and tumor protection by enterotoxin B subunit-conjugated peptides targeted to dendritic cells. Vaccine 2009;27(August (38)):5252-8.
29. Fromantin C, Jamot B, Cohen J, Piroth L, Pothier P, Kohli E. Rotavirus 2/6 viruslike particles administered intranasally in mice, with or without the mucosal adjuvants cholera toxin and Escherichia coli heat-labile toxin, induce aTh1/Th2-like immune response. J Virol 2001;75(November (22)):11010-6.
30. Weltzin R, Guy B, Thomas Jr WD, Giannasca PJ, Monath TP. Parenteral adjuvant activities of Escherichia coli heat-labile toxin and its B subunit for immunization of mice against gastric Helicobacter pylori infection. Infect Immun 2000;68(May (5)):2775-82.
31. Stephenson I, Zambon MC, Rudin A, Colegate A, Podda A, Bugarini R, etal. Phase I evaluation of intranasal trivalent inactivated influenza vaccine with nontox-igenic Escherichia coli enterotoxin and novel biovector as mucosal adjuvants, using adult volunteers. J Virol 2006;80(May (10)):4962-70.
32. Domingos MO, Andrade RG, Barbaro KC, Borges MM, Lewis DJ, New RR. Influence of the A and B subunits of cholera toxin (CT) and Escherichia coli toxin (LT) on TNF-alpha release from macrophages. Toxicon 2009;53(April (5)):570-7.
33. Stevens LA, Moss J, Vaughan M, Pizza M, Rappuoli R. Effects of site-directed mutagenesis of Escherichia coli heat-labile enterotoxin on ADP-ribosyltransferase activity and interaction with ADP-ribosylation factors. Infect Immun 1999;67(January (1)):259-65.
34. Fingerut E, Gutter B, Goldway M, Eliahoo D, Pitcovski J. B subunit of E. coli enterotoxin as adjuvant and carrier in oral and skin vaccination. Vet Immunol Immunopathol 2006;112(August (3-4)):253-63.
35. Pizza M, Fontana MR, Giuliani MM, Domenighini M, Magagnoli C, Giannelli V, et al. A genetically detoxified derivative of heat-labile Escherichia coli enterotoxin induces neutralizing antibodies against the A subunit. J Exp Med 1994;180(December (6)):2147-53.
36. Dickinson BL, Clements JD. Dissociation of Escherichia coli heat-labile enterotoxin adjuvanticity from ADP-ribosyltransferase activity. Infect Immun 1995;63(May (5)):1617-23.
37. Giuliani MM, Del Giudice G, Giannelli V, Dougan G, Douce G, Rappuoli R, et al. Mucosal adjuvanticity and immunogenicity of LTR72, a novel mutant of Escherichia coli heat-labile enterotoxin with partial knockout of ADP-ribosyltransferase activity. J Exp Med 1998;187(April (7)):1123-32.
38. Kende M, Tan X, Wlazlowski C, Williams R, Lindsey C, Del Giudice G. Enhancement of intranasal vaccination with recombinant chain A ricin vaccine (rRV) in mice by the mucosal adjuvants LTK63 and LTR72. Vaccine 2007;25(April (16)):3219-27.
39. Brynjolfsson SF, Bjarnarson SP, Mori E, Del Giudice G, Jonsdottir I. Neonatal immune response and serum bactericidal activity induced by a meningo-coccal conjugate vaccine is enhanced by LT-K63 and CpG2006. Vaccine 2008;26(August (35)):4557-62.
40. Zhang GG, Li DX, Zhang HH, Zeng YM, Chen L. Enhancement of mucosal immune response against the M2eHBc+antigen in mice with the fusion expression products of LTB and M2eHBc+through mucosal immunization route. Vet Res Commun 2009;33(October (7)):735-47.
41. Haan L, Verweij WR, Holtrop M, Brands R, van Scharrenburg GJ, Palache AM, et al. Nasal or intramuscular immunization of mice with influenza subunit antigen and the B subunit of Escherichia coli heat-labile toxin induces IgA- or IgG-mediated protective mucosal immunity. Vaccine 2001;19(April (20-22)):2898-907.
42. Xu Y, Zhang H, Xu X. Enhancement of vaccine potency by fusing modified LTK63 into human papillomavirus type 16 chimeric virus-like particles. FEMS Immunol Med Microbiol 2008;52(January (1)):99-109.
43. Guerena-Burgueno F, Hall ER, Taylor DN, Cassels FJ, Scott DA, Wolf MK, et al. Safety and immunogenicity of a prototype enterotoxigenic Escherichia coli vaccine administered transcutaneously. Infect Immun 2002;70(April (4)):1874-80.
44. 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 USA 2008;105(February (5)):1644-9.
45. Zhou WY, Shi Y, Wu C, Zhang WJ, Mao XH, Guo G, et al. Therapeutic efficacy of a multi-epitope vaccine against Helicobacter pylori infection in BALB/c mice model. Vaccine 2009;27(August (36)):5013-9.
46. Zhou F, Goodsell A, Uematsu Y, Vajdy M. Prolonged protection against Intranasal challenge with influenza virus following systemic immunization or combinations of mucosal and systemic immunizations with a heat-labile toxin mutant. Clin Vaccine Immunol 2009;16(April (4)):471-8.
47. Palma C, Iona E, Giannoni F, Pardini M, Brunori L, Fattorini L, et al. The LTK63 adjuvant improves protection conferred by Ag85B DNA-protein prime-boosting vaccination against Mycobacterium tuberculosis infection by dampening IFN-gamma response. Vaccine 2008;26(August (33)):4237-43.
48. Bonenfant C, Dimier-Poisson I, Velge-Roussel F, Buzoni-Gatel D, Del Giudice G, Rappuoli R, et al. Intranasal immunization with SAG1 and nontoxic mutant heat-labile enterotoxinsprotects miceagainst Toxoplasmagondii. Infect Immun 2001;69(March (3)):1605-12.
49. Facciabene A, Aurisicchio L, Elia L, Palombo F, Mennuni C, Ciliberto G, et al. Vectors encoding carcinoembryonic antigen fused to the B subunit of heat-labile enterotoxin elicit antigen-specific immune responses and antitumor effects. Vaccine 2007;26(December (1)):47-58.
50. Guidry JJ, Cardenas L, Cheng E, Clements JD. Role of receptor binding in toxicity, immunogenicity, and adjuvanticity of Escherichia coli heat-labile enterotoxin. Infect Immun 1997;65(December (12)):4943-50.
51. Cao S, Zhang Y, Liu F, Wang Q, Zhang Q, Liu Q, et al. Secretory expression and purification of recombinant Escherichia coli heat-labile enterotoxin B subunit and its applications on intranasal vaccination of hantavirus. Mol Biotechnol 2009;41(February (2)):91-8.
52. De Haan L, Hearn AR, Rivett AJ, Hirst TR. Enhanced delivery of exogenous peptides into the class I antigen processing and presentation pathway. Infect Immun 2002;70(June (6)):3249-58.
53. Nashar TO, Betteridge ZE, Mitchell RN. Evidence for a role ofganglioside GM(1) in antigen presentation: binding enhances presentation of Escherichia coli enterotoxinBsubunit (EtxB)toCD4(+)Tcells. Int Immunol 2001;13(4):541-51.
54. Bone H, Eckholdt S, Williams NA. Modulation of B lymphocyte signalling by the B subunit of Escherichia coli heat-labile enterotoxin. Int Immunol 2002;14(June (6)):647-58.
55. Williams NA. Immune modulation by the cholera-like enterotoxin B-subunits: from adjuvant to immunotherapeutic. Int J Med Microbiol 2000;290(4-5):447-53.
56. Yamamoto M, McGhee JR, Hagiwara Y, Otake S, Kiyono H. Genetically manipulated bacterial toxin as a new generation mucosal adjuvant. Scand J Immunol 2001;53(3):211-7.
57. Nashar TO, Hirst TR, Williams NA. Modulation of B-cell activation by the B subunit of Escherichia coli enterotoxin: receptor interaction up-regulates MHC class II, B7, CD40, CD25 and ICAM-1. Immunology 1997;91(4):572-8.
58. Zhou WY, Shi Y, Wu C, Zhang WJ, Mao XH, Guo G, et al. Therapeutic efficacy of a multi-epitope vaccine against Helicobacter pylori infection in BALB/c mice model. Vaccine 2009;27(36):5013-9.
59. Zhang X, Yuan Z, Duan Q, Zhu H, Yu H, Wang Q. Mucosal immunity in mice induced by orally administered transgenic rice. Vaccine 2009;27(March (10)):1596-600.
60. Fingerut E, Gutter B, Meir R, Eliahoo D, Pitcovski J. Vaccine adjuvant activity of recombinant subunit B of E. coli enterotoxin produced in yeast. Vaccine 2005;23(September (38)):4685-96.
61. Fischer G, Conceicao FR, Leite FPL, Moraes CM, Ferreira LN, Vilela CO, et al. Recombinant Escherichia coli heat-labile enterotoxin B subunit humoral adjuvant effect depends on dose and administration route. World J Microbiol Biotechnol 2009;26(March (3)):489-95.
62. Richards CM, Aman AT, Hirst TR, Hill TJ, Williams NA. Protective mucosal immunity to ocular herpes simplex virus type 1 infection in mice by using Escherichia coli heat-labile enterotoxin B subunit as an adjuvant. J Virol 2001;75(February (4)):1664-71.
63. Yamanaka H, Ishibashi D, Yamaguchi N, Yoshikawa D, Nakamura R, Okimura N, et al. Enhanced mucosal immunogenicity of prion protein following fusion with Bsubunit of Escherichia coli heat-labile enterotoxin. Vaccine 2006;24(April (15)):2815-23.
64. Ricci S, Medaglini D, Rush CM, Marcello A, Peppoloni S, Manganelli R, et al. Immunogenicity of the B monomer of Escherichia coli heat-labile toxin expressed on the surface of Streptococcus gordonii. Infect Immun 2000;68(February (2)):760-6.
65. Giannelli V, Fontana MR, Giuliani MM, Guangcai D, Rappuoli R, Pizza M. Protease susceptibility and toxicity of heat-labile enterotoxins with a mutation in the active site or in the protease-sensitive loop. Infect Immun 1997;65(January (1)):331-4.
66. De Haan L, Holtrop M, Verweij WR, Agsteribbe E, Wilschut J. Mucosal immunogenicity and adjuvant activity of the recombinant A subunit of the Escherichia coli heat-labile enterotoxin. Immunology 1999;97(August (4)):706-13.
67. Williams AE, Edwards L, Humphreys IR, Snelgrove R, Rae A, Rappuoli R, et al. Innate imprinting by the modified heat-labile toxin of Escherichia coli (LTK63) provides generic protection against lung infectious disease. J Immunol 2004;173(December (12)):7435-43.
68. Ryan EJ, McNeela E, Murphy GA, Stewart H, O'Hagan D, Pizza M, et al. Mutants of Escherichia coli heat-labile toxin act as effective mucosal adjuvants for nasal delivery of an acellular pertussis vaccine: differential effects of the non-toxic AB complex and enzyme activity on Th1 and Th2 cells. Infect Immun 1999;67(December (12)):6270-80.
69. Tritto E, Muzzi A, Pesce I, Monaci E, Nuti S, Galli G, et al. The acquired immune response to the mucosal adjuvant LTK63 imprints the mouse lung with a protective signature. J Immunol 2007;179(October (8)):5346-57.
70. Olafsdottir TA, Hannesdottir SG, Giudice GD, Trannoy E, Jonsdottir I. Effects of LT-K63 and CpG2006onphenotype and function of murine neonatal lymphoid cells. Scand J Immunol 2007;66(October (4)):426-34.
71. Simmons CP, Mastroeni P, Fowler R, Ghaem-maghami M, Lycke N, Pizza M, et al. MHC class I-restricted cytotoxic lymphocyte responses induced by enterotoxin-based mucosal adjuvants. J Immunol 1999;163(December (12)):6502-10.
72. Ugozzoli M, Santos G, Donnelly J, O'Hagan DT. Potency of a genetically detoxified mucosal adjuvant derived from the heat-labile enterotoxin of Escherichia coli (LTK63) is not adversely affected by the presence of preexisting immunity to the adjuvant. J Infect Dis 2001;183(January (2)):351-4.
73. Rocha ADR, Conceicao FR, Grassmann AA, Lagranha VL, Dellagostin OA. B subunit of Escherichia coli heat-labile enterotoxin as adjuvant of humoral immune response in recombinant BCG vaccination. Can J Microbiol 2008;54(August (8)):677-86.
74. Qiao XY, Li GW, Wang XQ,Li XJ, Liu M, Li YJ. Recombinant porcine rotavirus VP4 and VP4-LTB expressed in Lactobacillus casei induced mucosal and systemic antibody responses in mice. BMC Microbiol 2009;(December):9.
75. Lim JG, Kim JA, Chung HJ, Kim TG, Kim JM, Lee KR, et al. Expression of functional pentameric heat-labile enterotoxin B subunit of Escherichia coli in Saccharomyces cerevisiae. J Microbiol Biotechnol 2009;19(May (5)):502-10.
76. Ma XY, Bi Y, Zheng WY, Li LF. Comparative study on characterization of recombinant B subunit of E. coli heat-labile enterotoxin (rLTB) prepared from E. coli and P. pastoris. J Microbiol Biotechnol 2010;20(March (3)):550-7.
77. Kim TG, Kim BG, Kim MY, Choi JK, Jung ES, Yang MS. Expression and immuno-genicity of enterotoxigenic Escherichia coli heat-labile toxin B subunit in transgenic rice callus. Mol Biotechnol 2009;44(January (1)):14-21.
78. Kim TG, Kim MY, Kim BG, Kang TJ, Kim YS, Jang YS, et al. Synthesis and assembly of Escherichia coli heat-labile enterotoxin B subunit in transgenic lettuce (Lactuca sativa). Protein Expr Purif 2007;51(1):22-7.
79. Loc NH, Bach NH, Kim TG, Yang MS. Tissue culture and expression of Escherichia coli heat-labile enterotoxin B subunit in transgenic Peperomia pellucida. Protein Expr Purif 2010;72(July (1)):82-6.
80. Kang TJ, Han SC, Kim MY, Kim YS, Yang MS. Expression of non-toxic mutant of Escherichia coli heat-labile enterotoxin in tobacco chloroplasts. Protein Expr Purif 2004;38(November (1)):123-8.
81. Covone MG, Brocchi M, Palla E, Dias da Silveira W, Rappuoli R, Galeotti CL. Levels of expression and immunogenicity of attenuated Salmonella enterica serovar typhimurium strains expressing Escherichia coli mutant heat-labile enterotoxin. Infect Immun 1998;66(January (1)):224-31.