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Epithelial Cell Adhesion and Gastrointestinal Colonization of Lactobacillus in Poultry

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Epithelial Cell Adhesion and Gastrointestinal Colonization of Lactobacillus in Poultry Epithelial cell adhesion and gastrointestinal colonization of Lactobacillus in poultry Megan A. Spivey , Sadie L. Dunn-Horrocks , and Tri Duong 1 Department of Poultry Science, Texas A&M University, College Station 77843-2472 ABSTRACT Administration of probiotic Lactobacillus 78. However, when colonization was evaluated in the cultures is an important alternative to the use of an- ileum and cecum of broiler chicks, L. crispatus TDCC Downloaded from https://academic.oup.com/ps/article-abstract/93/11/2910/2730493 by guest on 13 November 2018 tibiotic growth promoters and has been demonstrated 75 and L. gallinarum TDCC 77 were more persistent to improve animal health, growth performance, and than L. crispatus TDCC 76 and L. gallinarum TDCC preharvest food safety in poultry production. Where- 78. The reduction of growth in medium supplemented as gastrointestinal colonization is thought to be criti- with oxgal was greater for L. gallinarum TDCC 78 than cal to their probiotic functionality, factors important L. gallinarum TDCC 77, suggesting that whereas adhe- to Lactobacillus colonization in chickens are not well sion was similar for the 2 strains, the difference in colo- understood. In this study we investigate epithelial cell nization between L. gallinarum strains may be due in adhesion in vitro and colonization of Lactobacillus in part to their bile sensitivity. This study demonstrates vivo in broiler chickens. Adhesion of Lactobacillus cul- that whereas adhesion to epithelial cells may be impor- tures to epithelial cells was evaluated using the chicken tant in predicting gastrointestinal colonization, other LMH cell line. Lactobacillus cultures were able adhere factors including bile tolerance may also contribute to effectively to LMH cells relative to Bacillus subtilis and the colonization of Lactobacillus in poultry. Addition- Salmonella Typhimurium. Epithelial cell adhesion was ally, the chicken LMH cell line is expected to provide a similar for Lactobacillus crispatus TDCC 75, L. cristpa- platform for investigating mechanisms of Lactobacillus tus TDCC 76, and Lactobacillus gallinarum TDCC 77, adhesion to epithelial tissue and evaluating the probi- and all 3 were more adherent than L. gallinarum TDCC otic potential Lactobacillus in poultry. Key words: Lactobacillus , probiotic , adhesion , colonization , LMH cell 2014 Poultry Science 93 :2910–2919 http://dx.doi.org/ 10.3382/ps.2014-04076 INTRODUCTION istration has also been shown to reduce colonization by Campylobacter (Ghareeb et al., 2012; Neal-McKinney Lactobacillus species are common inhabitants of the et al., 2012), Clostridium (La Ragione et al., 2004), and gastrointestinal tract and are often used as probiot- Salmonella (Chen et al., 2012; Ghareeb et al., 2012), ics due to their health promoting properties (Klaen- improving the microbial food safety of poultry. hammer et al., 2008). Probiotics, sometimes called Colonization and persistence in the gastrointestinal direct-fed microbials when used in livestock animals tract are thought to be critical for the realization of (Sanders, 2008), are often seen as alternatives to the probiotic benefits (Bernet et al., 1994; Mack et al., use of antibiotic growth promoters in poultry produc- 1999) and serve as important criteria for the selection of tion (Patterson and Burkholder, 2003; o’Bryan et al., probiotic microorganisms (Klaenhammer et al., 2005). 2008; Huyghebaert et al., 2011). The administration of Understanding how Lactobacillus species colonize chick- probiotic lactobacilli has been demonstrated to stimu- ens will be important in the selection of more effec- late immune responses (Haghighi et al., 2005; Sato et tive probiotic cultures and their application in poultry al., 2009; Brisbin et al., 2011), improve digestive health production. While the ability of probiotic lactobacilli (Gusils et al., 1999; Kim et al., 2012), and improve to colonize the gastrointestinal tract of poultry is mul- growth performance (Loh et al., 2010; Shim et al., 2012; tifactorial, adherence to epithelial cells is thought to Askelson et al., 2014) in poultry. Lactobacillus admin- contribute to colonization. The ability of Lactobacillus species to adhere to epi- thelial tissues and colonize poultry has been reported © 2014 Poultry Science Association Inc. (Jin et al., 1996; Edelman et al., 2002; Bouzaine et al., Received April 1, 2014. Accepted August 8, 2014. 2005). However, microbial factors important to gastro- 1 Corresponding author: [email protected] intestinal persistence of Lactobacillus in poultry are not 2910 LACTOBACILLUS ADHESION AND COLONIZATION 2911 well characterized. Aggregation, cell wall hydrophobic- try (Larson et al., 2008). The LMH cell line has also ity, and adhesion to extracellular components including been used to identify genes important in cellular inva- intestinal mucus, fibronectin, and basement membrane sion by Salmonella Enteritidis (Shah et al., 2012) and matrix have been used as in vitro measures of the ad- characterize the association of Clostridium perfringens herence of Lactobacillus strains to poultry epithelia NetB toxin to necrotic enteritis in chickens (Keyburn et (Edelman et al., 2002; Ehrmann et al., 2002; Gusils et al., 2008). Thus, utility of the chicken LMH epithelial al., 2003; Bouzaine et al., 2005; Taheri et al., 2009; Ro- cell line for the investigation of host-microbe interac- cha et al., 2012). Additionally, dissected tissue sections tions in the gastrointestinal tract of poultry has been (Fuller and Brooker, 1974; Edelman et al., 2002), pri- well established. mary chicken intestinal epithelial cells (Jin et al., 1996; In this study, we evaluated the adhesion of poultry- Garriga et al., 1998; Lin et al., 2007), and the HEp- derived strains of Lactobacillus crispatus and Lactoba- 2 (Ehrmann et al., 2002) and Caco-2 (Messaoudi et cillus gallinarum to the LMH epithelial cell line in vitro Downloaded from https://academic.oup.com/ps/article-abstract/93/11/2910/2730493 by guest on 13 November 2018 al., 2012) human epithelial cell lines have been used to and their colonization in vivo in broiler chicks to gain evaluate the potential of Lactobacillus cultures as poul- a better understanding of bacterium-host interactions try probiotics. Whereas cultured epithelial cell lines in chickens. are the most widely applied models for evaluating the adhesion of microorganisms (Ouwehand and Salminen, MATERIALS AND METHODS 2003), adherence of Lactobacillus cultures to a poultry- specific epithelial cell line has not been reported previ- Bacterial Strains ously. The lack of a species-specific cell culture model has been an obstacle to investigations of Lactobacillus The bacterial strains used in this study are listed adhesion and its contribution to gastrointestinal coloni- in Table 1. Lactobacillus strains were cultured using zation in poultry. deMan, Rogosa, and Sharpe (MRS) medium (Difco, The chicken LMH epithelial cell line (Kawaguchi et Franklin Lakes, NJ) in 10% CO2 at 37°C with rifampi- al., 1987), derived from a hepatocellular carcinoma, cin (Rif; EMD Chemicals Inc., San Diego, CA) added represents a cell line potentially useful for the investi- when appropriate. Salmonella Typhimurium and Ba- gation of probiotic functionality in poultry. The LMH cillus subtilis were cultured using tryptic soy medium cell line has been used previously as an in vitro model (TSA/TSB; Difco) aerobically at 37°C. For adhesion to investigate mechanisms of Campylobacter jejuni colo- assays, 18 h cultures of bacteria were harvested by cen- nization in poultry. Competitive inhibition between C. trifugation, washed 3 times with PBS, and subsequent- jejuni F38011 and C. jejuni 02–833L for adherence to ly resuspended in PBS to achieve the desired concen- gastrointestinal epithelia was demonstrated using the tration for inoculation onto LMH cells. chicken LMH epithelial cell line and verified in broiler chicks in vivo by Konkel et al. (2007). Additionally, Selection of Rifampicin-Resistant LMH cells were used to demonstrate that the adhesins Lactobacillus Cultures CadF and FlpA contribute to C. jejuni colonization in broiler chicks by mediating adherence to epithelial cells To generate rifampicin resistant (Rifr) cultures for (Flanagan et al., 2009), that autoinducer-2 expression use in in vitro adhesion and in vivo colonization assays, contributes to C. jejuni colonization by regulating ad- Lactobacillus cultures were serially transferred in MRS hesion to host tissues (Quinones et al., 2009), and that broth supplemented with up to 100 μg·mL−1 Rif and the cytokine response to C. jejuni in chicken compared subsequently plated onto MRS agar supplemented with −1 with humans contributes to its commensalism in poul- 100 μg·mL Rif. Following incubation in 10% CO2 at Table 1. Bacterial strains used in this study Strain Relevant characteristic Source or reference Lactobacillus crispatus ST1 Chicken crop isolate Ojala et al., 2010 JCM 5810 Chicken fecal isolate JCM1 TDCC 75 Rifr variant of L. crispatus ST1 This study TDCC 76 Rifr variant of L. crispatus JCM 5810 This study Lactobacillus gallinarum ATCC 33199T Chicken crop isolate, type strain ATCC2 JCM 8782 Chicken fecal isolate JCM TDCC 77 Rifr variant of L. gallinarum ATCC 33199 This study TDCC 78 Rifr variant of L. gallinarum JCM 8782 This study Bacillus subtilis ATCC 23857 Strain 168, genome sequenced variant ATCC Salmonella Typhimurium USDA-ARS,3 primary poultry isolate Byrd et al., 1998 1JCM = Japan Collection of Microorganisms. 2ATCC = American Type Culture Collection.
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