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Brachyspira Hyodysenteriae and B ORIGINAL RESEARCH published: 04 May 2017 doi: 10.3389/fmicb.2017.00723 Brachyspira hyodysenteriae and B. pilosicoli Proteins Recognized by Sera of Challenged Pigs Vanessa Casas 1, 2 †, Arantza Rodríguez-Asiain 1 †, Roberto Pinto-Llorente 1, Santiago Vadillo 3, Montserrat Carrascal 1 and Joaquin Abian 1, 2* 1 CSIC/UAB Proteomics Laboratory, IIBB-CSIC, IDIBAPS, Barcelona, Spain, 2 Faculty of Medicine, Autonomous University of Barcelona, Barcelona, Spain, 3 Departamento Sanidad Animal, Facultad de Veterinaria, Universidad de Extremadura, Cáceres, Spain The spirochetes Brachyspira hyodysenteriae and B. pilosicoli are pig intestinal pathogens that are the causative agents of swine dysentery (SD) and porcine intestinal spirochaetosis (PIS), respectively. Although some inactivated bacterin and recombinant Edited by: vaccines have been explored as prophylactic treatments against these species, no Juarez Antonio Simões Quaresma, Federal University of Pará, Brazil effective vaccine is yet available. Immunoproteomics approaches hold the potential Reviewed by: for the identification of new, suitable candidates for subunit vaccines against SD and Michael P. Murtaugh, PIS. These strategies take into account the gene products actually expressed and University of Minnesota, USA present in the cells, and thus susceptible of being targets of immune recognition. In Manuel Vilanova, Universidade do Porto, Portugal this context, we have analyzed the immunogenic pattern of two B. pilosicoli porcine *Correspondence: isolates (the Spanish farm isolate OLA9 and the commercial P43/6/78 strain) and one Joaquin Abian B. hyodysenteriae isolate (the Spanish farm V1). The proteins from the Brachyspira [email protected] lysates were fractionated by preparative isoelectric focusing, and the fractions were †These authors have contributed equally to this work. analyzed by Western blot with hyperimmune sera from challenged pigs. Of the 28 challenge-specific immunoreactive bands detected, 21 were identified as single proteins Specialty section: by MS, while the other 7 were shown to contain several major proteins. None of these This article was submitted to Microbial Immunology, proteins were detected in the control immunoreactive bands. The proteins identified a section of the journal included 11 from B. hyodysenteriae and 28 from the two B. pilosicoli strains. Eight Frontiers in Microbiology proteins were common to the B. pilosicoli strains (i.e., elongation factor G, aspartyl-tRNA Received: 31 January 2017 synthase, biotin lipoyl, TmpB outer membrane protein, flagellar protein FlaA, enolase, Accepted: 07 April 2017 Published: 04 May 2017 PEPCK, and VspD), and enolase and PEPCK were common to both species. Many Citation: of the identified proteins were flagellar proteins or predicted to be located on the cell Casas V, Rodríguez-Asiain A, surface and some of them had been previously described as antigenic or as bacterial Pinto-Llorente R, Vadillo S, virulence factors. Here we report on the identification and semiquantitative data of Carrascal M and Abian J (2017) Brachyspira hyodysenteriae and these immunoreactive proteins which constitute a unique antigen collection from these B. pilosicoli Proteins Recognized by bacteria. Sera of Challenged Pigs. Front. Microbiol. 8:723. Keywords: Brachyspira, vaccine, immunoblot, mass spectrometry, antigen, flagellar protein, swine dysentery, doi: 10.3389/fmicb.2017.00723 spirochaetosis Frontiers in Microbiology | www.frontiersin.org 1 May 2017 | Volume 8 | Article 723 Casas et al. The Brachyspira Immunoproteome INTRODUCTION such as outer-membrane proteins BmpB (La et al., 2004), SmpB (Holden et al., 2008), or variable surface proteins (Vsp) (Witchell Bacteria in the Brachyspiraceae family are gram-negative et al., 2006, 2011). Similar to an attempt to formulate a vaccine and spiral-shaped Spirochaetes. Members of this phylum are based on the ferritin protein FtnA (Davis et al., 2005), none characterized by their unique motility and a loosely coiled of these antigens provided enough protection for SD. On the morphology caused by the existence of periplasmic flagella other hand, several surface proteins of B. pilosicoli (ClpX and two (Charon and Goldstein, 2002). Species of the Brachyspiraceae putative oligopeptide-binding proteins) have been evaluated as family are anaerobic, host-associated intestinal bacteria in candidates for vaccination against IS (Movahedi and Hampson, pigs, humans and other species, and can cause gastrointestinal 2007, 2010). pathologies and mortality (Stanton, 2006). Currently, the The recent publication of the genome sequences of Brachyspiraceae comprises 16 species. B. hyodysenteriae B. hyodysenteriae and B. pilosicoli provided a useful tool for and B. pilosicoli are well-known Brachyspira intestinal the exploration of new candidates for inclusion in vaccination pathogens in pigs, responsible for swine dysentery (SD, a processes. To date, the genome sequence of 20 strains of severe mucohaemorrhagic colitis) (Alvarez-Ordóñez et al., 2013) B. hyodysenteriae (including the reference strain WA1, ATCC and porcine intestinal spirochaetosis (PIS, porcine spirochaetal 49526) (Black et al., 2015) and three strains of B. pilosicoli diarrhea, a mild, non-haemorrhagic colitis), respectively (Trott (porcine isolates P43/6/78 and 95/1,000, and an avian isolate et al., 1996; Stanton, 2006). B2904) (Wanchanthuek et al., 2010; Mappley et al., 2012; Lin SD is produced by B. hyodysenteriae, a restricted pig- et al., 2013) have been published. The availability of these data associated species, and is a disease present worldwide that has an enables extensive in silico analysis to identify vaccine candidates, important economic impact on the farming business. SD mainly which can then be expressed and tested together in a subunit affects pigs in the growing-finishing periods. This contributes vaccine. The potential of this reverse vaccinology approach was to the high cost of the disease, which is associated not only demonstrated by Song et al. who explored the development of with mortality, which is relatively low when animals are treated a vaccine against SD using a partial genome sequence of the (Hamdy, 1974), but also with high morbidity, growth retardation B. hyodysenteriae WA1 strain (Song et al., 2009). More recently, and the need for continual in-feed medication. a list of 33 ORF candidates to vaccine targets has been patented Unlike most Brachyspira species, B. pilosicoli has a wide host (Bellgard et al., 2015). These genes were selected on the basis range. It is zoonotic in pigs, poultry, dogs and humans (Hampson of their homology with known amino acid sequences of surface et al., 2006), in which it can lead to intestinal spirochaetosis (IS). proteins, secreted proteins and virulence factors from other In humans, the prevalence of IS is very uneven, much higher in species. developing regions than in industrialized regions (Tsinganou and Despite these important advances on the genomic level, its Gebbers, 2010). translation to proteomic knowledge of B. hyodysenteriae and The treatment for the control of a Brachyspira infection B. pilosicoli is still a challenge. Undoubtedly, future studies involves the use of multiple antimicrobial agents (Alvarez- focused on the description of Brachyspira proteomes will be Ordóñez et al., 2013). Nevertheless, several studies have necessary to design an effective vaccination strategy. In this highlighted the increasing occurrence of B. hyodysenteriae and regard, we recently characterized a subset of proteins exposed B. pilosicoli isolates resistant to these antibiotics in many on the cell surface (surfaceome) of B. hyodysenteriae and countries (Molnar, 1996; Karlsson et al., 2001; Rohde et al., B. pilosicoli (Casas et al., 2016). This will not only contribute 2004; Hidalgo et al., 2009; Ohya and Sueyoshi, 2010; Pringle to select good candidates for a vaccine, but will also impart et al., 2012), greatly compromising the efficacy of this global biological knowledge about invasive and pathogenic mechanisms treatment. of Brachyspira. Since Joens et al. described that pigs that recovered from In this study, we extended our proteomic approach to identify SD acquired immunological protection, and therefore rarely potential immunogenic proteins from B. hyodysenteriae and relapse when re-exposed to the infective agent (Joens et al., B. pilosicoli. For this purpose we studied the immunoproteome 1979), several endeavors have been launched to design a vaccine. of two B. pilosicoli strains (the isolate OLA9 and the commercial Unfortunately, these attempts have not been successful to date, ATCC strain P43/6/78) and one B. hyodysenteriae isolate (isolate and no effective vaccine against B. hyodysenteriae or B. pilosicoli V1). Cell lysates were fractionated using preparative off-gel is available. Early approaches in this area included immunization isoelectrofocusing and the fractions were separated by SDS- with an inactivated bacterin (Hampson, 2000) or attenuated PAGE. The gels were immunoblotted using pig immune-sera, strains (Hyatt et al., 1994). In addition to conferring only and the reactive bands were identified by mass spectrometry. partial protection in the best cases, these strategies entailed a Brachyspira isolates came from Spanish farms. It was reported cumbersome anaerobic-culture of Brachyspira which was not that during 2001-2003, more than 30% of commercial pig appropriate for large-scale production. farms in Spain had at least one positive for B. pilosicoli or In recent years, the
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