A new cloning system based on the OprI lipoprotein for the production of recombinant bacterial cell wall-derived immunogenic formulations

Journal of Biotechnology

Volumn 157, Issue 1, 2012, Pages 50-63

  Basto, Afonso P ^a   Piedade, João ^b   Ramalho, Ruben ^c,d   Alves, Susana ^e,f   Soares, Helena ^d,g,h   Cornelis, Pierre ⁱ   Martins, Carlos ^a   Leitão, Alexandre ^j  

^a FACULDADE DE MEDICINA VETERINÁRIA   (Portugal)

^b INSTITUTO DE HIGIENE E MEDICINA TROPICAL   (Portugal)

^c INSTITUTO SUPERIOR TÉCNICO   (Portugal)

^d INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^e INRB UPA INIA   (Portugal)

^f UNIVERSITY OF PORTO   (Portugal)

^g UNIVERSITY OF LISBON   (Portugal)

^h INSTITUTO POLITÉCNICO DE LISBOA   (Portugal)

ⁱ VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^j INSTITUTO DE INVESTIGAÇÃO CIENTÍFICA TROPICAL   (Portugal)

more..

Author keywords

Adjuvant; Bacterial outer membrane proteins; Cloning vector; Immunomodulation; Outer membrane lipoprotein I; Pseudomonas

Indexed keywords

ADJUVANT; CLONING VECTOR; IMMUNOMODULATION; OUTER MEMBRANE; OUTER MEMBRANE PROTEIN; PSEUDOMONAS;

AFFINITY CHROMATOGRAPHY; ANTIGENS; BACTERIA; CELL MEMBRANES; CLONE CELLS; CLONING; ESCHERICHIA COLI; LIGANDS; PALMITIC ACID; PROTEINS; VACCINES; VIRUSES;

PATTERN RECOGNITION SYSTEMS;

ENDOTOXIN; LIPOPROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; OPRI LIPOPROTEIN; OUTER MEMBRANE PROTEIN; PATTERN RECOGNITION RECEPTOR; PLASMID VECTOR; RECOMBINANT ANTIGEN; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ANTIGEN EXPRESSION; ARTICLE; ATOMIC FORCE MICROSCOPY; BACTERIAL CELL WALL; BACTERIAL STRAIN; BACTERIUM CULTURE; CELL FRACTIONATION; DNA TEMPLATE; ESCHERICHIA COLI; IMMUNOGENICITY; IMMUNOMODULATION; MOLECULAR CLONING; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA;

AFRICAN SWINE FEVER VIRUS; ANIMALS; ANTIGENS, VIRAL; BACTERIAL PROTEINS; BASE SEQUENCE; CELLS, CULTURED; CLONING, MOLECULAR; DENDRITIC CELLS; ESCHERICHIA COLI; GENETIC VECTORS; LIPOPROTEINS; MACROPHAGES; MICE; MOLECULAR SEQUENCE DATA; PSEUDOMONAS AERUGINOSA; RECOMBINANT FUSION PROTEINS; TUMOR NECROSIS FACTOR-ALPHA;

AFRICAN SWINE FEVER VIRUS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 84855233470     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2011.11.006     Document Type: Article

References (75)

1. Akira S. Pathogen recognition by innate immunity and its signaling. Proc. Jpn. Acad. Ser. B: Phys. Biol. Sci. 2009, 85:143-156.
2. Alaniz R.C., Deatherage B.L., Lara J.C., Cookson B.T. Membrane vesicles are immunogenic facsimiles of Salmonella typhimurium that potently activate dendritic cells, prime B and T cell responses, and stimulate protective immunity in vivo. J. Immunol. 2007, 179:7692-7701.
3. Aliahmadi E., Gramlich R., Grützkau A., Hitzler M., Krüger M., Baumgrass R., Schreiner M., Wittig B., Wanner R., Peiser M. TLR2-activated human langerhans cells promote Th17 polarization via IL-1β, TGF-β and IL-23. Eur. J. Immunol. 2009, 39:1221-1230.
4. Alves S.P., Bessa R.J.B. Comparison of two gas-liquid chromatograph columns for the analysis of fatty acids in ruminant meat. J. Chromatogr. A 2009, 1216:5130-5139.
5. Asensio C.J., Gaillard M.E., Moreno G., Bottero D., Zurita E., Rumbo M., van der Ley P., van der Ark A., Hozbor D. Outer membrane vesicles obtained from Bordetella pertussis Tohama expressing the lipid A deacylase PagL as a novel acellular vaccine candidate. Vaccine 2011, 29:1649-1656.
6. Blander J.M., Medzhitov R. Regulation of phagosome maturation by signals from Toll-like receptors. Science 2004, 304:1014-1018.
7. Blander J.M., Medzhitov R. Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature 2006, 440:808-812.
8. Braun V., Hantke K. Characterization of the free form of murein-lipoprotein from the outer membrane of Escherichia coli B/r. FEBS Lett. 1975, 60:26-28.
9. Buwitt-Beckmann U., Heine H., Wiesmüller K., Jung G., Brock R., Ulmer A.J. Lipopeptide structure determines TLR2 dependent cell activation level. FEBS J. 2005, 272:6354-6364.
10. Chen D.J., Osterrieder N., Metzger S.M., Buckles E., Doody A.M., DeLisa M.P., Putnam D. Delivery of foreign antigens by engineered outer membrane vesicle vaccines. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:3099-3104.
11. Chen H., Liu S., Liu H., Kwok Y., Lin C., Lin L., Chen M., Tsai J., Chang L., Chiu F., Lai L., Lian W., Yang C., Hsieh S., Chong P., Leng C. A novel technology for the production of a heterologous lipoprotein immunogen in high yield has implications for the field of vaccine design. Vaccine 2009, 27:1400-1409.
12. Christie W.W. Lipid Analysis: Isolation, Separation Identification and Structural Analysis of Lipids 2000, Amer. Oil Chemists Society. 3rd ed.
13. Coffman R.L., Sher A., Seder R.A. Vaccine adjuvants: putting innate immunity to work. Immunity 2010, 33:492-503.
14. Collins B.S. Gram-negative outer membrane vesicles in vaccine development. Discov. Med. 2011, 12:7-15.
15. Cornelis P., Bouia A., Belarbi A., Guyonvarch A., Kammerer B., Hannaert V., Hubert J.C. Cloning and analysis of the gene for the major outer membrane lipoprotein from Pseudomonas aeruginosa. Mol. Microbiol. 1989, 3:421-428.
16. Cornelis P., Sierra J.C., Lim A., Malur A., Tungpradabkul S., Tazka H., Leitão A., Martins C.V., di Perna C., Brys L., De Baetseller P., Hamers R. Development of new cloning vectors for the production of immunogenic outer membrane fusion proteins in Escherichia coli. Biotechnology (N.Y.) 1996, 14:203-208.
17. Cote-Sierra J., Jongert E., Bredan A., Gautam D.C., Parkhouse M., Cornelis P., De Baetselier P., Revets H. A new membrane-bound OprI lipoprotein expression vector. High production of heterologous fusion proteins in gram (-) bacteria and the implications for oral vaccination. Gene 1998, 221:25-34.
18. Cote-Sierra J., Bredan A., Toldos C.M., Stijlemans B., Brys L., Cornelis P., Segovia M., de Baetselier P., Revets H. Bacterial lipoprotein-based vaccines induce tumor necrosis factor-dependent type 1 protective immunity against Leishmania major. Infect. Immun. 2002, 70:240-248.
19. Cullen P.A., Lo M., Bulach D.M., Cordwell S.J., Adler B. Construction and evaluation of a plasmid vector for the expression of recombinant lipoproteins in Escherichia coli. Plasmid 2003, 49:18-29.
20. Dillon S., Agrawal A., Van Dyke T., Landreth G., McCauley L., Koh A., Maliszewski C., Akira S., Pulendran B. A Toll-like receptor 2 ligand stimulates Th2 responses in vivo, via induction of extracellular signal-regulated kinase mitogen-activated protein kinase and c-Fos in dendritic cells. J. Immunol. 2004, 172:4733-4743.
21. van Duin D., Medzhitov R., Shaw A.C. Triggering TLR signaling in vaccination. Trends Immunol. 2006, 27:49-55.
22. Durand V., Mackenzie J., de Leon J., Mesa C., Quesniaux V., Montoya M., Le Bon A., Wong S.Y.C. Role of lipopolysaccharide in the induction of type I interferon-dependent cross-priming and IL-10 production in mice by meningococcal outer membrane vesicles. Vaccine 2009, 27:1912-1922.
23. Filip C., Fletcher G., Wulff J.L., Earhart C.F. Solubilization of the cytoplasmic membrane of Escherichia coli by the ionic detergent sodium-lauryl sarcosinate. J. Bacteriol. 1973, 115:717-722.
24. Gao D., Mondal T.K., Lawrence D.A. Lead effects on development and function of bone marrow-derived dendritic cells promote Th2 immune responses. Toxicol. Appl. Pharmacol. 2007, 222:69-79.
25. Gartner T., Baeten M., Otieno S., Revets H., De Baetselier P., Huygen K. Mucosal prime-boost vaccination for tuberculosis based on TLR triggering OprI lipoprotein from Pseudomonas aeruginosa fused to mycolyl-transferase Ag85A. Immunol. Lett. 2007, 111:26-35.
26. Ghielmetti M., Reschner A., Zwicker M., Padovan E. Synthetic bacterial lipopeptide analogs: structural requirements for adjuvanticity. Immunobiology 2005, 210:211-215.
27. Ghielmetti M., Zwicker M., Ghielmetti T., Simon M.M., Villiger P.M., Padovan E. Synthetic bacterial lipopeptide analogs facilitate naive CD4+ T cell differentiation and enhance antigen-specific HLA-II-restricted responses. Eur. J. Immunol. 2005, 35:2434-2442.
28. Hirschfeld M., Kirschning C.J., Schwandner R., Wesche H., Weis J.H., Wooten R.M., Weis J.J. Cutting edge: inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by toll-like receptor 2. J. Immunol. 1999, 163:2382-2386.
29. Holst J., Martin D., Arnold R., Huergo C.C., Oster P., O'Hallahan J., Rosenqvist E. Properties and clinical performance of vaccines containing outer membrane vesicles from Neisseria meningitidis. Vaccine 2009, 27(Suppl. 2):B3-B12.
30. Huleatt J.W., Jacobs A.R., Tang J., Desai P., Kopp E.B., Huang Y., Song L., Nakaar V., Powell T.J. Vaccination with recombinant fusion proteins incorporating Toll-like receptor ligands induces rapid cellular and humoral immunity. Vaccine 2007, 25:763-775.
31. Inouye S., Takeishi K., Lee N., DeMartini M., Hirashima A., Inouye M. Lipoprotein from the outer membrane of Escherichia coli: purification, paracrystallization, and some properties of its free form. J. Bacteriol. 1976, 127:555-563.
32. Ishii K.J., Akira S. Toll or toll-free adjuvant path toward the optimal vaccine development. J. Clin. Immunol. 2007, 27:363-371.
33. Jenkins T.C., Thies E.J., Mosley E.E. Direct methylation procedure for converting fatty amides to fatty acid methyl esters in feed and digesta samples. J. Agric. Food Chem. 2001, 49:2142-2145.
34. Kamalakkannan S., Murugan V., Jagannadham M.V., Nagaraj R., Sankaran K. Bacterial lipid modification of proteins for novel protein engineering applications. Protein Eng. Des. Sel. 2004, 17:721-729.
35. Kawai T., Akira S. The roles of TLRs, RLRs and NLRs in pathogen recognition. Int. Immunol. 2009, 21:317-337.
36. Keenan J.I., Rijpkema S.G., Durrani Z., Roake J.A. Differences in immunogenicity and protection in mice and guinea pigs following intranasal immunization with Helicobacter pylori outer membrane antigens. FEMS Immunol. Med. Microbiol. 2003, 36:199-205.
37. Kesty N.C., Kuehn M.J. Incorporation of heterologous outer membrane and periplasmic proteins into Escherichia coli outer membrane vesicles. J. Biol. Chem. 2004, 279:2069-2076.
38. Khan S., Bijker M.S., Weterings J.J., Tanke H.J., Adema G.J., van Hall T., Drijfhout J.W., Melief C.J.M., Overkleeft H.S., van der Marel G.A., Filippov D.V., van der Burg S.H., Ossendorp F. Distinct uptake mechanisms but similar intracellular processing of two different toll-like receptor ligand-peptide conjugates in dendritic cells. J. Biol. Chem. 2007, 282:21145-21159.
39. Kim J.Y., Doody A.M., Chen D.J., Cremona G.H., Shuler M.L., Putnam D., DeLisa M.P. Engineered bacterial outer membrane vesicles with enhanced functionality. J. Mol. Biol. 2008, 380:51-66.
40. Kiura K., Kataoka H., Yasuda M., Inoue N., Shibata K. The diacylated lipopeptide FSL-1 induces TLR2-mediated Th2 responses. FEMS Immunol. Med. Microbiol. 2006, 48:44-55.
41. Leitão A., Malur A., Cartaxeiro C., Vasco G., Cruz B., Cornelis P., Martins C.L. Bacterial lipoprotein based expression vectors as tools for the characterisation of African swine fever virus (ASFV) antigens. Arch. Virol. 2000, 145:1639-1657.
42. Leitão A., Malur A., Cornelis P., Martins C.L. Identification of a 25-aminoacid sequence from the major African swine fever virus structural protein VP72 recognised by porcine cytotoxic T lymphocytes using a lipoprotein based expression system. J. Virol. Methods 1998, 75:113-119.
43. Li G.B., Lu G.X. Adherent cells in granulocyte-macrophage colony-stimulating factor-induced bone marrow-derived dendritic cell culture system are qualified dendritic cells. Cell. Immunol. 2010, 264:4-6.
44. Liang M.D., Bagchi A., Warren H.S., Tehan M.M., Trigilio J.A., Beasley-Topliffe L.K., Tesini B.L., Lazzaroni J., Fenton M.J., Hellman J. Bacterial peptidoglycan-associated lipoprotein: a naturally occurring toll-like receptor 2 agonist that is shed into serum and has synergy with lipopolysaccharide. J. Infect. Dis. 2005, 191:939-948.
45. Lombardi V., Van Overtvelt L., Horiot S., Moussu H., Chabre H., Louise A., Balazuc A., Mascarell L., Moingeon P. Toll-like receptor 2 agonist Pam3CSK4 enhances the induction of antigen-specific tolerance via the sublingual route. Clin. Exp. Allergy 2008, 38:1819-1829.
46. Loots K., Revets H., Goddeeris B.M. Attachment of the outer membrane lipoprotein (OprI) of Pseudomonas aeruginosa to the mucosal surfaces of the respiratory and digestive tract of chickens. Vaccine 2008, 26:546-551.
47. Lutz M.B., Kukutsch N., Ogilvie A.L., Rössner S., Koch F., Romani N., Schuler G. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 1999, 223:77-92.
48. Manicassamy S., Pulendran B. Modulation of adaptive immunity with Toll-like receptors. Semin. Immunol. 2009, 21:185-193.
49. McConnell M.J., Rumbo C., Bou G., Pachón J. Outer membrane vesicles as an acellular vaccine against Acinetobacter baumannii. Vaccine 2011, 29:5705-5710.
50. Meng G., Grabiec A., Vallon M., Ebe B., Hampel S., Bessler W., Wagner H., Kirschning C.J. Cellular recognition of tri-/di-palmitoylated peptides is independent from a domain encompassing the N-terminal seven leucine-rich repeat (LRR)/LRR-like motifs of TLR2. J. Biol. Chem. 2003, 278:39822-39829.
51. Mitchell D., Yong M., Schroder W., Black M., Tirrell M., Olive C. Dual stimulation of MyD88-dependent Toll-like receptors induces synergistically enhanced production of inflammatory cytokines in murine bone marrow-derived dendritic cells. J. Infect. Dis. 2010, 202:318-329.
52. Mizuno T., Kageyama M. Isolation of characterization of a major outer membrane protein of Pseudomonas aeruginosa. Evidence for the occurrence of a lipoprotein. J. Biochem. 1979, 85:115-122.
53. Moyle P.M., Toth I. Self-adjuvanting lipopeptide vaccines. Curr. Med. Chem. 2008, 15:506-516.
54. Oursel D., Loutelier-Bourhis C., Orange N., Chevalier S., Norris V., Lange C.M. Identification and relative quantification of fatty acids in Escherichia coli membranes by gas chromatography/mass spectrometry. Rapid Commun. Mass Spectrom. 2007, 21:3229-3233.
55. Palm N.W., Medzhitov R. Pattern recognition receptors and control of adaptive immunity. Immunol. Rev. 2009, 227:221-233.
56. Park S.B., Jang H.B., Nho S.W., Cha I.S., Hikima J., Ohtani M., Aoki T., Jung T.S. Outer membrane vesicles as a candidate vaccine against Edwardsiellosis. PLoS One 2011, 6(3):e17629.
57. Piedade, J., 2003. Expressão em Escherichia coli da proteína Nef do vírus da imunodefi{ligature}ciência humana tipo 1 (VIH-1) como produto de fusão com a lipoproteína OprI da membrana externa de Pseudomonas aeruginosa e indução de imunidade humoral anti-Nef em modelo animal. Ph.D. Thesis. Universidade Nova de Lisboa, Lisbon, Portugal.
58. Rau H., Revets H., Cornelis P., Titzmann A., Ruggli N., McCullough K.C., Summerfield A. Efficacy and functionality of lipoprotein OprI from Pseudomonas aeruginosa as adjuvant for a subunit vaccine against classical swine fever. Vaccine 2006, 24:4757-4768.
59. Reis A.L., Parkhouse R.M.E., Penedos A.R., Martins C., Leitão A. Systematic analysis of longitudinal serological responses of pigs infected experimentally with African swine fever virus. J. Gen. Virol. 2007, 88:2426-2434.
60. Remans K., Pauwels K., van Ulsen P., Buts L., Cornelis P., Tommassen J., Savvides S.N., Decanniere K., Van Gelder P. Hydrophobic surface patches on LolA of Pseudomonas aeruginosa are essential for lipoprotein binding. J. Mol. Biol. 2010, 401:921-930.
61. Revets H., Pynaert G., Grooten J., De Baetselier P. Lipoprotein I, a TLR2/4 ligand modulates Th2-driven allergic immune responses. J. Immunol. 2005, 174:1097-1103.
62. Rioux C.R., Bergeron H., Lin L., Grothe S., O'Connor-McCourt M., Lau P.C. A fusion plasmid for the synthesis of lipopeptide-antigen chimeras in Escherichia coli. Gene 1992, 116:13-20.
63. Schild S., Nelson E.J., Camilli A. Immunization with Vibrio cholerae outer membrane vesicles induces protective immunity in mice. Infect. Immun. 2008, 76:4554-4563.
64. Schlosser E., Mueller M., Fischer S., Basta S., Busch D.H., Gander B., Groettrup M. TLR ligands and antigen need to be coencapsulated into the same biodegradable microsphere for the generation of potent cytotoxic T lymphocyte responses. Vaccine 2008, 26:1626-1637.
65. Schroeder J., Aebischer T. Recombinant outer membrane vesicles to augment antigen-specific live vaccine responses. Vaccine 2009, 27:6748-6754.
66. Sieling P.A., Chung W., Duong B.T., Godowski P.J., Modlin R.L. Toll-like receptor 2 ligands as adjuvants for human Th1 responses. J. Immunol. 2003, 170:194-200.
67. Tokuda H. Biogenesis of outer membranes in Gram-negative bacteria. Biosci. Biotechnol. Biochem. 2009, 73:465-473.
68. Toshchakov V., Jones B.W., Perera P.-Y., Thomas K., Cody M.J., Zhang S., Williams B.R.G., Major J., Hamilton T.A., Fenton M.J., Vogel S.N. TLR4, but not TLR2, mediates IFN-β-induced STAT1α/β-dependent gene expression in macrophages. Nat. Immunol. 2002, 3:392-398.
69. Trinchieri G., Sher A. Cooperation of Toll-like receptor signals in innate immune defence. Nat. Rev. Immunol. 2007, 7:179-190.
70. ünal C.M., Schaar V., Riesbeck K. Bacterial outer membrane vesicles in disease and preventive medicine. Semin. Immunopathol. 2010, (Epub ahead of print). 10.1007/s00281-010-0231-y.
71. van de Waterbeemd B., Streefland M., van der Ley P., Zomer B., van Dijken H., Martens D., Wijffels R., van der Pol L. Improved OMV vaccine against Neisseria meningitidis using genetically engineered strains and a detergent-free purification process. Vaccine 2010, 28:4810-4816.
72. Warshakoon H.J., Hood J.D., Kimbrell M.R., Malladi S., Wu W.Y., Shukla N.M., Agnihotri G., Sil D., David S.A. Potential adjuvantic properties of innate immune stimuli. Hum. Vaccin. 2009, 5:381-394.
73. Watts C., West M.A., Zaru R. TLR signalling regulated antigen presentation in dendritic cells. Curr. Opin. Immunol. 2010, 22:124-130.
74. Weinberg G.A., Towler D.A., Munson R.S. Lipoproteins of Haemophilus influenzae type b. J. Bacteriol. 1988, 170:4161-4164.
75. Wille-Reece U., Wu C., Flynn B.J., Kedl R.M., Seder R.A. Immunization with HIV-1 Gag protein conjugated to a TLR7/8 agonist results in the generation of HIV-1 Gag-specific Th1 and CD8+ T cell responses. J. Immunol. 2005, 174:7676-7683.