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Mucosal Immunization with Polymeric Antigen Blsomp31 Using Alternative Delivery Systems Against Brucella Ovis in Rams T

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Mucosal Immunization with Polymeric Antigen Blsomp31 Using Alternative Delivery Systems Against Brucella Ovis in Rams T Veterinary Immunology and Immunopathology 209 (2019) 70–77 Contents lists available at ScienceDirect Veterinary Immunology and Immunopathology journal homepage: www.elsevier.com/locate/vetimm Mucosal immunization with polymeric antigen BLSOmp31 using alternative delivery systems against Brucella ovis in rams T Alejandra Graciela Díaza,g, Daniela Alejandra Quinterosb,g, Fernando Alberto Paolicchic, Mariana Alejandra Riverod, Santiago Daniel Palmab,g, Romina Paola Pardof, María Claussee,g, ⁎ Vanesa Zylbermanf,g, Fernando Alberto Goldbaumf,g, Silvia Marcela Esteina,g, a Laboratorio de Inmunología, Departamento de Sanidad Animal y Medicina Preventiva (SAMP), Centro de Investigación Veterinaria Tandil (CIVETAN-CONICET- CICPBA), Facultad de Ciencias Veterinarias (FCV), Universidad Nacional del Centro de la Provincia de Buenos Aires (UNCPBA), Tandil, 7000, Buenos Aires, Argentina b Departamento de Farmacia. Facultad Ciencias Químicas. Unidad de Investigación y Desarrollo en Tecnología Farmacéutica (UNITEFA-CONICET), Universidad Nacional de Córdoba, Argentina c Laboratorio de Bacteriología, Departamento de Producción Animal, Instituto Nacional de Tecnología Agropecuaria, Balcarce, 7620, Argentina d Área de Epidemiología. SAMP. CIVETAN-CONICET-CICPBA, FCV, UNCPBA, Tandil, Buenos Aires, Argentina e Área de Cirugía. Depto. Clínica. CIVETAN-CONICET-CICPBA, FCV, UNCPBA, Tandil, Buenos Aires, Argentina f Inmunova S.A., Buenos Aires, Argentina g Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina ARTICLE INFO ABSTRACT Keywords: Subcellular vaccines against ovine contagious epididymitis due Brucella ovis can solve some shortcomings as- BLSOmp31-Chitosan microspheres sociated with the use of Brucella melitensis Rev 1. We have demonstrated that the parenteral immunization with BLSOmp31-Poloxamer 407-Chitosan gel polymeric antigen BLSOmp31 emulsified in oil adjuvant conferred significant protection against B. ovis in rams. Mucosal immunization In our previous studies, we have characterized chitosan microspheres (ChMs) and a thermoresponsive and Lambs mucoadhesive in situ gel (Poloxamer 407-Ch) as two novel formulation strategies for the delivery of BLSOmp31 Immunogenicity in nasal as well as conjunctival mucosa. In the present work, we evaluated the immunogenicity and protection Partial protection Brucella ovis conferred by the intranasal and conjunctival immunization with these two mucosal delivery systems against B. ovis in rams. BLSOmp31-ChM administered by intranasal route and BLSOmp31-P407-Ch applied by intranasal or conjunctival routes induced systemic, local and preputial IgG and IgA antibody response. Neither formulation showed interference in the serological diagnosis. Thus, mucosal immunization using either formulation induced significant specific cellular immune responses (in vitro and in vivo) and it prevented the excretion of B. ovis in semen. Although these vaccines did not prevent infection in immunized rams, colonization reduction of infected organs and bacterial distribution differed significantly between vaccinated and unvaccinated rams. 1. Introduction (Moriyón et al., 2004). Consequently, research efforts have been fo- cusing on the development of novel vaccines for controlling B. ovis Brucella ovis causes a disease characterized by epididymitis and infection. Recently, a mutant B. ovis strain lacking a putative ATP- subfertility in rams, and occasional abortions in ewes as well as neo- binding cassette transporter (ΔabcBA) and encapsulated with alginate natal death, leading to significant economic loss worldwide. was found to confer protection against B. ovis in mice (Silva et al., Vaccination is recognized as the most suitable tool for control of the 2015a). It proved to be safe and also conferred protection against this disease in countries with moderate to high prevalence (Blasco, 1990). pathogen in rams but, its use could interfere in serodiagnosis of ovine Nowadays, the live B. melitensis Rev. 1 strain is considered the most brucellosis (Silva et al., 2015b). effective available vaccine against B. ovis (Blasco, 1997). However, this Therefore, subcellular preparations would offer a safer alternative vaccine displays a large number of shortcomings, including residual for controlling B. ovis infection (Menzies, 2012). Different studies have virulence, antibiotic resistance, pathogenicity for humans and, inter- previously demonstrated that outer membrane complex preparations of ferences with serodiagnosis which limit its global widespread use B. ovis (Hot Saline extracts (HS)) incorporated in selected adjuvants ⁎ Corresponding author at: Laboratorio de Inmunología, CIVETAN, CONICET, Facultad de Ciencias Veterinarias, Universidad Nacional del Centro de la Provincia de Buenos Aires, Tandil, Buenos Aires, Pinto 399, Argentina. E-mail address: [email protected] (S.M. Estein). https://doi.org/10.1016/j.vetimm.2019.02.005 Received 2 June 2018; Received in revised form 5 February 2019; Accepted 9 February 2019 0165-2427/ © 2019 Elsevier B.V. All rights reserved. A.G. Díaz, et al. Veterinary Immunology and Immunopathology 209 (2019) 70–77 conferred a similar degree of protection against B. ovis in mice and rams 2.2. Animals as B. melitensis Rev. 1 (Blasco et al., 1993; Muñoz et al., 2006; Da Costa Martins et al., 2012). Forty Romney Marsh-Corriedale 6-month-old lambs seronegative to Recombinant proteins and DNA vaccines have been explored for Brucella ovis were purchased from a brucellosis-free herd. Lambs re- their value as potential protective immunogens against B. ovis in the mained in BL3 facilities until the end of the studies (Campo mouse model (Estein et al., 2003; Cassataro et al., 2007; Pasquevich Experimental de SENASA (Servicio Nacional de Sanidad y Calidad et al., 2010, 2011). Among them, a polymeric antigen BLSOmp31 Agroalimentaria)), Azul, Buenos Aires, Argentina). All the experiment constructed by Brucella Lumazina Sinthetase (BLS) decorated with a was carried out following ethical 101 guidelines of the Animal Welfare protective epitope of Brucella Outer Membrane Protein Omp31 is con- Committee of the Faculty of Veterinary Medicine, 102 Universidad sidered an attractive vaccine candidate against ovine brucellosis Nacional del Centro de la Provincia de Buenos Aires (Internal 120 (Cassataro et al., 2007; Estein et al., 2009). In fact, parenteral im- Protocol: 03/2014; Approval date: 28,05, 2014). munization with this immunogen emulsified in oil adjuvant (In- complete Freund Adjuvant (IFA)) elicited a similar protective immunity 2.3. BLSOmp31 production against B. ovis in mice than B. melitensis Rev. 1 (Cassataro et al., 2007). Furthermore, immunization of lambs with this antigen conferred pro- Recombinant BLSOmp31 was expressed in Escherichia coli BL21 tection against B. ovis and it did not interfere in routine serological tests (Stratagene, USA), and was purified according to the procedure pre- for rough (R) or smooth (S) Brucella, suggesting that immunization with viously developed by Laplagne et al. (2004). BLSOmp31could be compatible with an eradication brucellosis program (Estein et al., 2009; Díaz et al., 2013). 2.4. Preparation of vaccines Since B. ovis can invade hosts through the mucosal membranes, it is desirable to obtain a local immune response to block both colonization All vaccines had the same concentration of BLSOmp31 (500 μg/ and disease development. In this regard, mucosal immunization with an animal/dose). BLSOmp31-P407-Ch gel vaccine was prepared and appropriate vaccine delivery vehicle and adjuvant has been shown to characterized as previously described (Díaz et al., 2016a). Briefly, Po- induce both protective mucosal and systemic immune responses in the loxamer 407 (16% w/v) (BASF, Germany) was added to an aqueous absence of needles (Yuki and Kiyono, 2009; Chadwick et al., 2010). solution of BLSOmp31. Chitosan (0.25% w/v) and was dissolved in a Interestingly, there is evidence of a significant degree of compartmen- 0.5% acetic acid solution (Parafarm, Argentina). talization within the common mucosal immune system. The use of one ChMs was prepared using the spray-drying technique and mucosal route of immunization will trigger the immune responses lo- BLSOmp31 was adsorbed by ionic interaction to the ChMs surface. As a cally, systemically, and in at least one distal mucosal site (Wilson and control vaccine, we used BLSOmp31-IFA as previously described by Obradovic, 2015). Estein et al. (2009). Relatively few studies have been carried out using anti-Brucella subunit vaccine administered by oral, IN or CONJ routes as an alter- 2.5. Experimental design native to obtain immunity against this pathogen in mice or guinea pigs with variable results (Bhattacharjee et al., 2002, 2006; Pasquevich Scheme of experimental design is summarized in Fig. 1. et al., 2011; da Costa Martins et al, 2012). As regards, Senevirathne et al. (2019) demonstrated that a cocktail of five conserved antigens of 2.5.1. Vaccination schedule Brucella spp. administered by IN in mice conferred significant protec- Five groups of 8 lambs were immunized as follows: G1) BLSOmp31- tion against the B. abortus nasal challenge. However, although labora- ChM (0.5 mL/nostril), G2) BLSOmp31-P407-Ch gel by IN route tory animals are a valuable tool to evaluate vaccines in brucellosis, (0.5 mL/nostril), G3) BLSOmp31-P407-Ch gel by CONJ via (0.05 mL/ finding in these models cannot easily be extrapolated to susceptible sac), G4) BLSOmp31-IFA administered by IM route (2 mL/dose) hosts (Silva et al., 2011). (SIGMA,
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