Mucosal co-immunization of mice with recombinant lactococci secreting VapA antigen and leptin elicits a protective immune response against Rhodococcus equi infection

Vaccine

Volumn 30, Issue 1, 2011, Pages 95-102

  Cauchard, S ^a   Bermudez Humaran L G ^b   Blugeon, S ^b   Laugier, C ^a   Langella, P ^b   Cauchard, J ^a  

^a FRENCH AGENCY FOR FOOD   (France)

^b AGROPARISTECH   (France)

Author keywords

Immunization; Lactococcus; Leptin; Mucosal; Rhodococcus; VapA

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 4; LEPTIN; PROTEIN A; RECOMBINANT ANTIGEN; BACTERIAL PROTEIN; BACTERIAL VACCINE; CYTOKINE; DRUG CARRIER; IMMUNOLOGICAL ADJUVANT; RECOMBINANT VACCINE; VAPA PROTEIN, RHODOCOCCUS EQUI;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL COUNT; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CLINICAL EVALUATION; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG DOSAGE FORM COMPARISON; FEMALE; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOMODULATION; IN VITRO STUDY; LACTOCOCCUS LACTIS; LIVER; MOUSE; MUCOSA; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN SECRETION; RHODOCOCCUS EQUI; SPLEEN CELL; TH1 CELL; TH2 CELL; ACTINOMYCETALES INFECTION; ANIMAL; BACTERIAL LOAD; BAGG ALBINO MOUSE; GENETICS; IMMUNOLOGY; MICROBIOLOGY; MONONUCLEAR CELL; MUCOSAL ADMINISTRATION; SECRETION; SPLEEN;

ACTINOMYCETALES INFECTIONS; ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, MUCOSAL; ANIMALS; BACTERIAL LOAD; BACTERIAL PROTEINS; BACTERIAL VACCINES; CYTOKINES; DRUG CARRIERS; FEMALE; LACTOCOCCUS LACTIS; LEPTIN; LEUKOCYTES, MONONUCLEAR; LIVER; MICE; MICE, INBRED BALB C; RHODOCOCCUS EQUI; SPLEEN; VACCINES, SYNTHETIC;

EID: 84858598550     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.10.026     Document Type: Article

References (50)

1. Giguere S, Prescott JF. Clinical manifestations, diagnosis, treatment and prevention of Rhodococcus equi infections in foals. Vet Microbiol 1997;56:313-34.
2. Yamshchikov AV, Schuetz A, Lyon GM. Rhodococcus equi infection. Lancet Infect Dis 2010;10:350-9.
3. Ulivieri S, Oliveri G. Cerebellar abscess due to Rhodococcus equi in an immunocompetent patient: case report and literature review. J Neurosurg Sci 2006;50:127-9.
4. Hondalus MK. Pathogenesis and virulence of Rhodococcus equi. Vet Microbiol 1997;56:257-68.
5. Letek M, Ocampo-Sosa AA, Sanders M, Fogarty U, Buckley T, Leadon DP, et al. Evolution of the Rhodococcus equi vap pathogenicity island seen through comparison of host-associated vapA and vapB virulence plasmids. J Bacteriol 2008;190:5797-805.
6. Takai S, Hines SA, Sekizaki T, Nicholson VM, Alperin DA, Osaki M, et al. DNA sequence and comparison of virulence plasmids from Rhodococcus equi ATCC 33701 and 103. Infect Immun 2000;68:6840-7.
7. Takai S, Koike K, Ohbushi S, Izumi C, Tsubaki S. Identification of 15-kilodalton to 17-kilodalton antigens associated with virulent Rhodococcus equi. J Clin Microbiol 1991;29:439-43.
8. Jain S, Bloom BR, Hondalus MK. Deletion of vapA encoding Virulence Associated Protein A attenuates the intracellular actinomycete Rhodococcus equi. Mol Microbiol 2003;50:115-28.
9. Hooper-McGrevy KE, Giguere S, Wilkie BN, Prescott JF. Evaluation of equine immunoglobulin specific for Rhodococcus equi virulence-associated proteins A and C for use in protecting foals against Rhodococcus equi-induced pneumonia. Am J Vet Res 2001;62:1307-13.
10. Prescott JF, Patterson MC, Nicholson VM, Morein B, Yager JA. Assessment of the immunogenic potential of Rhodococcus equi virulence associated protein (VapA) in mice. Vet Microbiol 1997;56:213-25.
11. Cauchard J, Sevin C, Ballet JJ, Taouji S. Foal IgG and opsonizing anti-Rhodococcus equi antibodies after immunization of pregnant mares with a protective VapA candidate vaccine. Vet Microbiol 2004;104:73-81.
12. Dawson TR, Horohov DW, Meijer WG, Muscatello G. Current understanding of the equine immune response to Rhodococcus equi An immunological review of R. equi pneumonia. Vet Immunol Immunopathol 2010;135:1-11.
13. Jacks S, Giguère S, Crawford PC, Castleman WL. Experimental infection of neonatal foals with Rhodococcus equi triggers adult-like gamma interferon induction. Clin Vaccine Immunol 2007;14:669-77.
14. Wagner B, Burton A, Ainsworth D. Interferon-gamma, interleukin-4 and interleukin-10 production by T helper cells reveals intact Th1 and regulatory TR1 cell activation and a delay of the Th2 cell response in equine neonates and foals. Vet Res 2010;41:47.
15. Takai S, Hidaka D, Fujii M, Shindoh Y, Murata T, Nakanishi S, et al. Serum antibody responses of foals to virulence-associated 15- to 17-kilodalton antigens of Rhodococcus equi. Vet Microbiol 1996;52:63-71.
16. Chirino-Trejo JM, Prescott JF, Yager JA. Protection of foals against experimental Rhodococcus equi pneumonia by oral immunization. Can J Vet Res 1987;51:444-7.
17. Hooper-McGrevy KE, Wilkie BN, Prescott JF. Virulence-associated proteinspecific serum immunoglobulin G-isotype expression in young foals protected against Rhodococcus equi pneumonia by oral immunization with virulent R. equi. Vaccine 2005;23:5760-7.
18. Oliveira AF, Ferraz LC, Brocchi M, Roque-Barreira MC. Oral administration of a live attenuated Salmonella vaccine strain expressing the VapA protein induces protection against infection by Rhodococcus equi. Microbes Infect 2007;9:382-90.
19. Lopez AM, Townsend HG, Allen AL, Hondalus MK. Safety and immunogenicity of a live-attenuated auxotrophic candidate vaccine against the intracellular pathogen Rhodococcus equi. Vaccine 2008;26:998-1009.
20. Bermúdez-Humarán LG, Langella P, Miyoshi A, Gruss A, Guerra RT, Montes de Oca-Luna R, et al. Production of human papillomavirus type 16 E7 protein in Lactococcus lactis. Appl Environ Microbiol 2002;68:917-22.
21. Morello E, Bermúdez-Humarán LG, Llull D, Solé V, Miraglio N, Langella P, et al. Lactococcus lactis, an efficient cell factory for recombinant protein production and secretion. J Mol Microbiol Biotechnol 2008;14:48-58.
22. Steidler L, Hans W, Schotte L, Neirynck S, Obermeier F, Falk W, et al. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science 2000;289:1352-5.
23. Bermúdez-Humarán LG. Lactococcus lactis as a live vector for mucosal delivery of therapeutic proteins. Hum Vaccine 2009;5:264-7.
24. Cortes-Perez NG, Lefèvre F, Corthier G, Adel-Patient K, Langella P, Bermúdez-Humarán LG. Influence of the route of immunization and the nature of the bacterial vector on immunogenicity of mucosal vaccines based on lactic acid bacteria. Vaccine 2007;25:6581-8.
25. Medina M, Villena J, Vintiñi E, Hebert EM, Raya R, Alvarez S. Nasal immunization with Lactococcus lactis expressing the pneumococcal protective protein A induces protective immunity in mice. Infect Immun 2008;76: 2696-705.
26. Quigley BR, Hatkoff M, Thanassi DG, Ouattara M, Eichenbaum Z, Scott JR. A foreign protein incorporated on the Tip of T3 pili in Lactococcus lactis elicits systemic and mucosal immunity. Infect Immun 2010;78:1294-303.
27. de Ruyter PG, Kuipers OP, Beerthuyzen MM, van Alen-Boerrigter I, de Vos WM. Functional analysis of promoters in the nisin gene cluster of Lactococcus lactis. J Bacteriol 1996;178:3434-9.
28. Kuipers OP, de Ruyter PG, Kleerebezem M, de Vos WM. Quorum sensingcontrolled gene expression in lactic acid bacteria. J Biotechnol 1998;64:15-21.
29. Bermúdez-Humarán LG, Langella P, Commissaire J, Gilbert S, Le Loir Y, L'Haridon R, et al. Controlled intra- or extracellular production of staphylococcal nuclease and ovine omega interferon in Lactococcus lactis. FEMS Microbiol Lett 2003;224:307-13.
30. Bermúdez-Humarán LG, Cortes-Perez NG, Le Loir Y, Alcocer-González JM, Tamez-Guerra RS, de Oca-Luna RM, et al. An inducible surface presentation system improves cellular immunity against human papillomavirus type 16 E7 antigen in mice after nasal administration with recombinant lactococci. J Med Microbiol 2004;53:427-33.
31. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM. Positional cloning of the mouse obese gene and its human homologue. Nature 1994;372:425-32.
32. Lord GM, Matarese G, Howard JK, Baker RJ, Bloom SR, Lechler RI. Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature 1998;394:897-901.
33. Mattioli B, Straface E, Matarrese P, Quaranta MG, Giordani L, Malorni W, et al. Leptin as an immunological adjuvant: enhanced migratory and CD8+ T cell stimulatory capacity of human dendritic cells exposed to leptin. FASEB J 2008;22:2012-22.
34. Mattioli B, Straface E, Quaranta MG, Giordani L, Viora M. Leptin promotes differentiation and survival of human dendritic cells and licenses them for Th1 priming. J Immunol 2005;174:6820-8.
35. Sánchez-Margalet V, Martín-Romero C, Santos-Alvarez J, Goberna R, Najib S, Gonzalez-Yanes C. Role of leptin as an immunomodulator of blood mononuclear cells: mechanisms of action. Clin Exp Immunol 2003;133:11-9.
36. Bermúdez-Humarán LG, Nouaille S, Zilberfarb V, Corthier G, Gruss A, Langella P, et al. Effects of intranasal administration of a leptin-secreting Lactococcus lactis recombinant on food intake, body weight, and immune response of mice. Appl Environ Microbiol 2007;73:5300-7.
37. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual. 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1989.
38. Langella P, Le Loir Y, Ehrlich SD, Gruss A. Efficient plasmid mobilization by pIP501 in Lactococcus lactis subsp. lactis. J Bacteriol 1993;175:5806-13.
39. Barbey C, Budin-Verneuil A, Cauchard S, Hartke A, Laugier C, Pichereau V, et al. Proteomic analysis and immunogenicity of secreted proteins from Rhodococcus equi ATCC 33701. Vet Microbiol 2009;135:334-45.
40. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-75.
41. Valosky J, Hishiki H, Zaoutis TE, Coffin SE. Induction of mucosal B-cell memory by intranasal immunization of mice with respiratory syncitial virus. Clin Diagn Lab Immunol 2005;12:171-9.
42. Oliveira ML, Arêas AP, Campos IB, Monedero V, Perez-Martínez G, Miyaji EN, et al. Induction of systemic and mucosal immune response and decrease in Streptococcus pneumoniae colonization by nasal inoculation of mice with recombinant lactic acid bacteria expressing pneumococcal surface antigen A. Microbes Infect 2006;8:1016-24.
43. Yam KK, Pouliot P, N'diaye MM, Fournier S, Olivier M, Cousineau B. Innate inflammatory responses to the Gram-positive bacterium Lactococcus lactis. Vaccine 2008;26:2689-99.
44. Kim SY, Lim JH, Choi SW, Kim M, Kim ST, Kim MS, et al. Preferential effects of leptin on CD4 T cells in central and peripheral immune system are critically linked to the expression of leptin receptor. Biochem Biophys Res Commun 2010;394:562-8.
45. Cheun HI, Kawamoto K, Hiramatsu M, Tamaoki H, Shirahata T, Igimi S, et al. Protective immunity of SpaA-antigen producing Lactococcus lactis against Erysipelothrix rhusiopathiae infection. J Appl Microbiol 2004;96:1347-53.
46. Ramasamy R, Yasawardena S, Zomer A, Venema G, Kok J, Leenhouts K. Immunogenicity of a malaria parasite antigen displayed by Lactococcus lactis in oral immunizations. Vaccine 2006;24:3900-8.
47. Vinti {ogonek}ni E, Villena J, Alvarez S, Medina M. Administration of a probiotic associated with nasal vaccination with inactivated Lactococcus lactis-PppA induces effective protection against pneumoccocal infection in young mice. Clin Exp Immunol 2010;159:351-62.
48. 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.
49. Christie GE, Farnham PJ, Platt T. Synthetic sites for transcription termination and a functional comparison with tryptophan operon termination sites in vitro. Proc Natl Acad Sci USA 1981;78:4180-4.
50. Kok J, van der Vossen JM, Venema G. Construction of plasmid cloning vectors for lactic streptococci which also replicate in Bacillus subtilis and Escherichia coli. Appl Environ Microbiol 1984;48:726-31.