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Live and Heat-Killed Lactobacillus Rhamnosus GG: Effects on Proinflammatory and Anti-Inflammatory Cytokines/Chemokines in Gastro

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Live and Heat-Killed Lactobacillus Rhamnosus GG: Effects on Proinflammatory and Anti-Inflammatory Cytokines/Chemokines in Gastro 0031-3998/09/6602-0203 Vol. 66, No. 2, 2009 PEDIATRIC RESEARCH Printed in U.S.A. Copyright © 2009 International Pediatric Research Foundation, Inc. Live and Heat-Killed Lactobacillus rhamnosus GG: Effects on Proinflammatory and Anti-Inflammatory Cytokines/Chemokines in Gastrostomy-Fed Infant Rats NAN LI, W. MICHAEL RUSSELL, MARTHA DOUGLAS-ESCOBAR, NICK HAUSER, MARIELA LOPEZ, AND JOSEF NEU Department of Pediatrics [N.L., M.D.-E., N.H., M.L., J.N.], University of Florida, Gainesville, Florida 32610; Mead-Johnson Nutrition [W.M.R.], Evansville, Indiana 47721 ABSTRACT: Lactobacillus rhamnosus GG (LGG), a probiotics, The rational for use of killed rather than live agents stems ameliorates intestinal and other organ inflammation in infant rats. from studies showing that interactions of microbe-associated The hypothesis is that live and heat-killed LGG have similar effects molecular patterns (MAMPs) with Toll-like receptors (TLRs) on decreasing the inflammatory response induced by E. coli lipo- and other mucosal pattern recognition receptors (PRRs) likely polysaccharide (LPS) in the infant rat. Using a gastrostomy-fed rat model, 7-d-old rat pups were gastrostomy fed with or without live mediate some of the beneficial responses of probiotics. One LGG (108 or 1012 cfu ⅐ LϪ1 ⅐ kgϪ1 ⅐ dϪ1) for 6 d. In a separate study reported nonvirulent Salmonella strains whose direct experiment, LPS was administered to rat pups with or without live or interaction with model human epithelia attenuate IL-8 produc- heat-killed LGG (108 cfu ⅐ LϪ1 ⅐ kgϪ1 ⅐ dϪ1). Cytokine/chemokine tion elicited by various proinflammatory stimuli (14). The proteins were determined by ELISA or multiplex assay. Both live and mechanisms were found to be through abrogation of polyu- heat-killed LGG decreased LPS-induced cytokine-induced neutrophil biquitination of I kappa B-alpha degradation (14). More recent Ͻ chemoattractant-1 (CINC-1) production in liver and plasma (p studies also suggest that the epithelium and resident immune 0.05) and also showed a trend (p ϭ 0.09) in lungs. Live and cells do not simply tolerate commensal bacterial but are depen- heat-killed LGG ameliorated LPS-suppressed IL-10 level in lungs (p Ͻ 0.05). Both forms of LGG decreased IL-1b production in liver. dent on them (15). Commensal bacteria produce molecules such There was no difference between low and high doses of live LGG as lipopolysaccharide (LPS) (15), lipoteichoic acid (15), and CpG in the production of CINC-1, TNF-␣, and myeloperoxidase (MPO). nucleotides (16), which in turn interact in the normal intestine There was a trend of increase of claudin-1 in both live and heat-killed with a population of surface TLRs. The resultant ongoing sig- groups (p ϭ 0.08). In conclusion, both live and heat-killed LGG naling enhances the ability of the epithelial surface to withstand provided by the enteral route decrease LPS-induced proinflammatory injury while also priming the surface for enhanced repair re- mediators and increase anti-inflammatory mediators. (Pediatr Res sponses. Therefore, either the disruption of TLR signaling or the 66: 203–207, 2009) removal of TLR ligands (derived from intestinal microorgan- isms) compromises the ability of the intestinal surface to protect he majority of microbes in the human are found in the and repair itself in the face of inflammatory or infectious insult colon and distal small intestine and consist of more than T (15). It is thus intuitive that the interactive processes of microbes 1013 microorganisms (the “microbiota”), comprising nearly with the intestine do not necessarily depend on living and thus 500 species and 2 million genes (the “microbiome”) (1,2). proliferating microbes. This is mostly a mutually beneficial relationship, as evidenced by the important role the resident intestinal bacteria play in Our recent study in cell culture model showed that UV- nutrition (3), angiogenesis (4), and mucosal immunity (5). inactivated and live Lactobacillus rhamnosus GG (LGG) are Probiotics are live microbial agents thought to confer health equally effective in decreasing IL-8 production in the intesti- benefits to the host by maintaining an advantageous intestinal nal epithelium (17). If inactivated probiotic bacteria or their microecology. One example is that probiotics may be effica- products are able to provide similar beneficial effects as the cious in preventing necrotizing enterocolitis (NEC) and other live bacteria in vivo, the experiments we propose are critical diseases in infants (6,7). However, caveats have been raised before routine use of probiotics in newborn infants. Whether about their use in neonates. Case reports of sepsis from live microorganisms are necessary to provide a beneficial probiotics in immunocompromised infants (8–10) have raised response seen with probiotics, or whether the same killed, concern about short-term detrimental effects. Furthermore, nonproliferating agents are able to result in similar effects establishment of the early intestinal microbiota in prematures requires further investigation. In this study, we hypothesized may be long term and result in unforeseen detrimental side that heat killed LGG will regulate intestinal inflammation effects, as evidenced in recent studies (11–13). similar to live LGG. Received January 5, 2009; accepted April 10, 2009. Abbreviations: CINC-1, Cytokine-induced neutrophil chemoattractant-1, Correspondence: Josef Neu, M.D., Department of Pediatrics, College of Medicine, Uni- versity of Florida, PO Box 100296, Gainesville, FL 32610; e-mail: [email protected]fl.edu LGG, Lactobacillus rhamnosus GG, LPS, Lipopolysaccharide, MPO, my- Supported by a Grant from Mead Johnson Nutrition. eloperoxidase, NEC, necrotizing enterocolitis 203 204 LI ET AL. METHODS formed. Multiplex bead kits were purchased from LINCO Research, Inc. (St. Charles, MO). Cytokines/chemokines were analyzed by a kit that included the Bacteria and related preparations. LGG powder was a gift from Mead- following: granulocyte-macrophage colony-stimulating factor (GMCSF), Johnson Nutritionals. Live LGG was stored at 4°C. The activity of this IFN-␥, IL-1␣, IL-1␤, IL-2, IL-4, IL-5, IL-6, IL-10, IL-12p70, IL-18, mono- powder is ϳ3.6 ϫ 1011 cfu ⅐ gϪ1. Heat-killed LGG was prepared by heating cyte chemoattractant protein-1 (MCP-1), GRO/KC [rat cytokine-induced bacteria at 80°C for 20 min at a concentration of 1010 cfu ⅐ LϪ1 in PBS and neutrophil chemoattractant-1 (CINC-1), rodent IL-8 equivalent chemokine], then diluted at different concentrations in rat milk substitute (RMS). Effec- and TNF-␣. Multiplex assay was performed according to the manufacturer’s tiveness of the heat killing method was confirmed as follows: Samples of instructions. Standard curves for each cytokine/chemokine were generated by LGG before and after heat killing were diluted in PBS and plated on L agar; using the reference concentrations supplied by the manufacturers. Raw data 0.2 mL of the heat-killed sample was plated on L agar. The plates were (mean fluorescent intensity) were analyzed by MasterPlex Quantitation Soft- incubated under anaerobic conditions for 72 h at 37°C. The untreated sample ware (MiraiBio, Inc., Alameda, CA) to obtain concentration values. was at 5.4 ϫ 1010 cells ⅐ LϪ1. No colonies arose from the 0.2-mL heat-killed ELISA for CINC-1, TNF-␣, and IL-10. After screened by Cytokine sample; the minimum detection is 5000 cells ⅐ LϪ1. Multiplex Assays, certain cytokines were evaluated by ELISA. Samples were Animals. The University of Florida Institutional Animal Care and Use isolated from cellular extracts of whole tissues. To evaluate proinflammatory Committee approved the following study. In two separate experiments, and anti-inflammatory cytokines, liver, lungs, small intestine, and plasma Sprague-Dawley (Taconic, Germantown, NY) infant rats were randomly CINC-1, IL-10, and TNF-␣ were determined by TiteZyme Enzyme Immu- assigned to four gastrostomy feeding groups with five rats per group. Mother- nometric Assay kits for rat growth-related oncogene (GRO)/CINC-1, IL-10, reared rats of the same age were used as reference controls. Gastrostomy and TNF-␣ (Assay Designs, Ann Arbor, MI), respectively. Absorbance was feeding using the rat infant “pup-in-the-cup” model began ond7oflife determined at 450 nm, and concentration was calculated using the equation through feeding tubes constructed from 24-cm sections of polyethylene tubing derived from a linear standard curve. that were inserted into the stomach, as previously described (18). This is a Immunoblotting for tight junctions. Small intestinal samples were har- commonly used model in studies of developmental nutrition when it is vested and homogenized in western lysis buffer (10 mM Tris-HCl, pH 7.6, important to manipulate nutritional composition in the absence of maternal 150 mM NaCl, 2 mM EDTA, 1% SDS) with protease inhibitors. Protein was feedings. The gastrostomy placement was done under isoflurane anesthesia. measured using the BioRad Dc Protein Assay (BioRad, Hercules, CA). Equal Timer-controlled syringe pumps were connected to the feeding tubes and amount of protein from each sample was separated on 12.5% SDS-PAGE and were set to feed the rats for the first 20 min of every hour at a weight- then transferred to PVDF membrane. Blots were blocked by 5% nonfat milk dependent flow rate. All the gastrostomy-fed groups received the same and incubated with primary antibodies (claudin-1, occludin obtained from quantity of fat and carbohydrates, and the protein component was similar to Zymed Laboratory Inc., South San Francisco, CA)
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