Lactobacillus reuteri I5007 modulates intestinal host defense peptide expression in the model of IPEC-J2 cells and neonatal piglets

Nutrients

Volumn 9, Issue 6, 2017, Pages

  Liu, Hongbin ^a   Hou, Chengli ^a,b   Wang, Gang ^a   Jia, Hongmin ^a   Yu, Haitao ^a   Zeng, Xiangfang ^a   Thacker, Philip A ^c   Zhang, Guolong ^d   Qiao, Shiyan ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c UNIVERSITY OF SASKATCHEWAN   (Canada)

^d OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

Gut microbiota; Host defense peptide; Intestinal epithelial cells; Lactobacillus reuteri; Neonatal piglets

Indexed keywords

ACETIC ACID; BETA DEFENSIN 114; BETA DEFENSIN 129; BETA DEFENSIN 2; BETA DEFENSIN 3; BUTYRIC ACID; DEFENSIN; FORMIC ACID; G PROTEIN COUPLED RECEPTOR KINASE 41; G PROTEIN COUPLED RECEPTOR KINASE 43; LACTIC ACID; MUCIN 1; PATTERN RECOGNITION RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; POLYPEPTIDE ANTIBIOTIC AGENT; PROBIOTIC AGENT; PROPIONIC ACID; PROTEGRIN; PROTEIN KINASE; SHORT CHAIN FATTY ACID; UNCLASSIFIED DRUG; ANTIMICROBIAL CATIONIC PEPTIDE; BACTERIAL DNA; BETA DEFENSIN; BUTYRIC ACID DERIVATIVE; G PROTEIN COUPLED RECEPTOR; PROTEGRIN-1; VOLATILE FATTY ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COLON; COLONY FORMING UNIT; CONTROLLED STUDY; DIARRHEA; FECES ANALYSIS; GENE EXPRESSION; ILEUM; INTESTINE FLORA; JEJUNUM; LACTOBACILLUS REUTERI; MALE; NEWBORN; NONHUMAN; PIG; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; ANIMAL; CELL LINE; CHEMISTRY; CYTOLOGY; EPITHELIUM CELL; FECES; GENE EXPRESSION REGULATION; GENETICS; INTESTINE; METABOLISM; MICROBIOLOGY;

ANIMALS; ANIMALS, NEWBORN; ANTIMICROBIAL CATIONIC PEPTIDES; BETA-DEFENSINS; BUTYRATES; CELL LINE; DIARRHEA; DNA, BACTERIAL; EPITHELIAL CELLS; FATTY ACIDS, VOLATILE; FECES; GASTROINTESTINAL MICROBIOME; GENE EXPRESSION REGULATION; INTESTINES; LACTOBACILLUS REUTERI; MALE; PPAR GAMMA; PROBIOTICS; RECEPTORS, G-PROTEIN-COUPLED; SWINE;

EID: 85020307655     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu9060559     Document Type: Article

References (60)

1. Laxminarayan, R.; Matsoso, P.; Pant, S.; Brower, C.; Rottingen, J.A.; Klugman, K.; Davies, S. Access to effective antimicrobials: A worldwide challenge. Lancet 2016, 387, 168-175.
2. Nijnik, A.; Hancock, R. Host defence peptides: Antimicrobial and immunomodulatory activity and potential applications for tackling antibiotic-resistant infections. Emerg. Health Threats J. 2009, 2, e1.
3. Hancock, R.E.; Sahl, H.G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 2006, 24, 1551-1557.
4. Zeng, X.; Sunkara, L.T.; Jiang, W.; Bible, M.; Carter, S.; Ma, X.; Qiao, S.; Zhang, G. Induction of porcine host defense peptide gene expression by short-chain fatty acids and their analogs. PLoS ONE 2013, 8, e72922.
5. Gonzalez, L.M.; Williamson, I.; Piedrahita, J.A.; Blikslager, A.T.; Magness, S.T. Cell lineage identification and stem cell culture in a porcine model for the study of intestinal epithelial regeneration. PLoS ONE 2013, 8, e66465.
6. Meurens, F.; Summerfield, A.; Nauwynck, H.; Saif, L.; Gerdts, V. The pig: A model for human infectious diseases. Trends Microbiol. 2012, 20, 50-57.
7. Selsted, M.E.; Ouellette, A.J. Mammalian defensins in the antimicrobial immune response. Nat. Immunol. 2005, 6, 551-557.
8. Zanetti, M. Cathelicidins, multifunctional peptides of the innate immunity. J. Leukoc. Biol. 2004, 75, 39-48.
9. Talukder, P.; Satho, T.; Irie, K.; Sharmin, T.; Hamady, D.; Nakashima, Y.; Kashige, N.; Miake, F. Trace metal zinc stimulates secretion of antimicrobial peptide LL-37 from Caco-2 cells through ERK and p38 MAP kinase. Int. Immunopharmacol. 2011, 11, 141-144.
10. Fehlbaum, P.; Rao, M.; Zasloff, M.; Anderson, G.M. An essential amino acid induces epithelial beta -defensin expression. Proc. Natl. Acad. Sci. USA 2000, 97, 12723-12728.
11. Cederlund, A.; Kai-Larsen, Y.; Printz, G.; Yoshio, H.; Alvelius, G.; Lagercrantz, H.; Stromberg, R.; Jornvall, H.; Gudmundsson, G H.; Agerberth, B.; et al. Lactose in human breast milk an inducer of innate immunity with implications for a role in intestinal homeostasis. PLoS ONE 2013, 8, e53876.
12. Gombart, A.F.; Borregaard, N.; Koeffler, H.P. Human cathelicidin antimicrobial peptide (CAMP) gene is a direct target of the vitamin D receptor and is strongly up-regulated in myeloid cells by 1,25-dihydroxyvitamin D3. FASEB J. 2005, 19, 1067-1077.
13. Schlee, M.; Harder, J.; Koten, B.; Stange, E.F.; Wehkamp, J.; Fellermann, K. Probiotic lactobacilli and VSL#3 induce enterocyte beta-defensin 2. Clin. Exp. Immunol. 2008, 151, 528-535.
14. Zhang, J.; Deng, J.; Li, Y.; Yang, Q. The effect of Lactobacillus on the expression of porcine β-defensin-2 in the digestive tract of piglets. Livest. Sci. 2011, 138, 259-265.
15. Valeur, N.; Engel, P.; Carbajal, N.; Connolly, E.; Ladefoged, K. Colonization and immunomodulation by Lactobacillus reuteri ATCC 55730 in the human gastrointestinal tract. Appl. Environ. Microbiol. 2004, 70, 1176-1181.
16. Hou, C.; Zeng, X.; Yang, F.; Liu, H.; Qiao, S. Study and use of the probiotic Lactobacillus reuteri in pigs: A review. J. Anim. Sci. Biotechnol. 2015, 6, 14.
17. Hou, C.; Wang, Q.; Zeng, X.; Yang, F.; Zhang, J.; Liu, H.; Ma, Xi.; Qiao, Shiyan. Complete genome sequence of Lactobacillus reuteri I5007, a probiotic strain isolated from healthy piglet. J. Biotechnol. 2014, 179, 63-64.
18. Huang, C.; Qiao, S.; Li, D.; Piao, X.; Ren, J. Effects of lactobacilli on the performance, diarrhea incidence, VFA concentration and gastrointestinal microbial flora of weaning pigs. Asian Australas. J. Anim. Sci. 2004, 17, 401-409.
19. Li, X.J.; Yue, L.Y.; Guan, X.F.; Qiao, S.Y. The adhesion of putative probiotic lactobacilli to cultured epithelial cells and porcine intestinal mucus. J. Appl. Microbiol. 2008, 104, 1082-1091.
20. Wang, X.; Yang, F.; Liu, C.; Zhou, H.; Wu, G.; Qiao, S.; Li, D.; Wang, J. Dietary Supplementation with the Probiotic Lactobacillus fermentum I5007 and the Antibiotic Aureomycin Differentially Affects the Small Intestinal Proteomes of Weanling Piglets. J. Nutr. 2011, 142, 7-13.
21. Yu, H.F.; Wang, A.N.; Li, X.J.; Qiao, S.Y. Effect of viable Lactobacillus fermentum on the growth performance, nutrient digestibility and immunity of weaned pigs. J. Anim. Feed Sci. 2008, 17, 61-69.
22. Liu, H.; Zhang, J.; Zhang, S.; Yang, F.; Thacker, P.A.; Zhang, G.; Qiao, S.; Ma, X. Oral administration of Lactobacillus fermentum I5007 favors intestinal development and alters the intestinal microbiota in formula-fed piglets. J. Agric. Food Chem. 2014, 62, 860-866.
23. Wang, A.N.; Cai, C.J.; Zeng, X.F.; Zhang, F.R.; Zhang, G.L.; Thacker, P.A.; Wang, J.J.; Qiao, S.Y. Dietary supplementation with. J. Appl. Microbiol. 2013, 114, 1582-1591.
24. Hou, C.; Liu, H.; Zhang, J.; Zhang, S.; Yang, F.; Zeng, X.; Thacker, P.; Zhang, G.; Qiao, S. Intestinal Microbiota Succession and Immunomodulatory Consequences after Introduction of Lactobacillus reuteri I5007 in Neonatal Piglets. PLoS ONE 2015, 10, e0119505.
25. Marquardt, R.R.; Jin, L.Z.; Kim, J.W.; Fang, L.; Frohlich, A.A.; Baidoo, S.K. Passive protective effect of egg-yolk antibodies against enterotoxigenic Escherichia coli K88+ infection in neonatal and early-weaned piglets. FEMS Immunol. Med. Microbiol. 1999, 23, 283-288.
26. Ou, D.; Li, D.; Cao, Y.; Li, X.; Yin, J.; Qiao, S.; Wu, G. Dietary supplementation with zinc oxide decreases expression of the stem cell factor in the small intestine of weanling pigs. J. Nutr. Biochem. 2007, 18, 820-826.
27. Aranda, P.S.; LaJoie, D.M.; Jorcyk, C.L. Bleach gel: A simple agarose gel for analyzing RNA quality. Electrophoresis 2012, 33, 366-369.
28. Arce, C.; Ramirez-Boo, M.; Lucena, C.; Garrido, J.J. Innate immune activation of swine intestinal epithelial cell lines (IPEC-J2 and IPI-2I) in response to LPS from Salmonella typhimurium. Comp. Immunol. Microbiol. Infect. Dis. 2010, 33, 161-174.
29. Li, B.; Zerby, H.N.; Lee, K. Heart fatty acid binding protein is upregulated during porcine adipocyte development. J. Anim. Sci. 2007, 85, 1651-1659.
30. Li, G.; Su, H.; Zhou, Z.; Yao, W. Identification of the porcine G protein-coupled receptor 41 and 43 genes and their expression pattern in different tissues and development stages. PloS ONE 2014, 9, e97342.
31. Mariani, V.; Palermo, S.; Fiorentini, S.; Lanubile, A.; Giuffra, E. Gene expression study of two widely used pig intestinal epithelial cell lines: IPEC-J2 and IPI-2I. Vet. Immunol. Immunopathol. 2009, 131, 278-284.
32. Qiu, J.; Jin, X. Development and optimization of organic acid analysis in tobacco with ion chromatography and suppressed conductivity detection. J. Chromatogr. A 2002, 950, 81-88.
33. Wehkamp, J.; Harder, J.; Wehkamp, K.; Wehkamp-von Meissner, B.; Schlee, M.; Enders, C.; Sonnenborn, U.; Nuding, S.; Bengmark, S.; Fellermann, K.; et al. NF-κB-and AP-1-mediated induction of human beta defensin-2 in intestinal epithelial cells by Escherichia coli Nissle 1917: A novel effect of a probiotic bacterium. Infect. Immun. 2004, 72, 5750-5758.
34. Topping, D.L.; Clifton, P.M. Short-chain fatty acids and human colonic function: Roles of resistant starch and nonstarch polysaccharides. Physiol. Rev. 2001, 81, 1031-1064.
35. Weber, N.; Nielsen, J.P.; Jakobsen, A.S.; Pedersen, L.L.; Hansen, C.F.; Pedersen, K.S. Occurrence of diarrhoea and intestinal pathogens in non-medicated nursery pigs. Acta Vet. Scand. 2015, 57, 64.
36. Sang, Y.; Blecha, F. Porcine host defense peptides: Expanding repertoire and functions. Dev. Comp. Immunol. 2009, 33, 334-343.
37. Dou, X.; Han, J.; Song, W.; Dong, N.; Xu, X.; Zhang, W.; Shan, A. Sodium butyrate improves porcine host defense peptide expression and relieves the inflammatory response upon Toll-like receptor 2 activation and histone deacetylase inhibition in porcine kidney cells. Oncotarget 2017, 8, 26532-26551.
38. Gallo, R.L.; Hooper, L.V. Epithelial antimicrobial defence of the skin and intestine. Nat. Rev. Immunol. 2012, 12, 503-516.
39. Yoon, J.H.; Ingale, S.L.; Kim, J.S.; Kim, K.H.; Lohakare, J.; Park, Y.K.; Kwon, I K.; Chae, B J. Effects of dietary supplementation with antimicrobial peptide-P5 on growth performance, apparent total tract digestibility, faecal and intestinal microflora and intestinal morphology of weanling pigs. J. Sci. Food Agric. 2013, 93, 587-592.
40. Wen, L.F.; He, J.G. Dose-response effects of an antimicrobial peptide, a cecropin hybrid, on growth performance, nutrient utilisation, bacterial counts in the digesta and intestinal morphology in broilers. Br. J. Nutr. 2012, 108, 1756-1763.
41. Cullen, T.W.; Schofield, W.B.; Barry, N.A.; Putnam, E.E.; Rundell, E.A.; Trent, M.S.; Degnan, P H.; Booth, C J.; Yu, H.; Goodman, A L. Gut microbiota. Antimicrobial peptide resistance mediates resilience of prominent gut commensals during inflammation. Science 2015, 347, 170-175.
42. Goyette-Desjardins, G.; Auger, J.P.; Xu, J.; Segura, M.; Gottschalk, M. Streptococcus suis, an important pig pathogen and emerging zoonotic agent-an update on the worldwide distribution based on serotyping and sequence typing. Emerg. Microbes. Infect. 2014, 3, e45.
43. Basson, M.D.; Liu, Y.; Hanly, A.M.; Emenaker, N.J.; Shenoy, S.G.; Rothberg, B.E.G. Identification and comparative analysis of human colonocyte short-chain fatty acid response genes. J. Gastrointest. Surg. 2000, 4, 501-512.
44. Sanderson, I.R. Short chain fatty acid regulation of signaling genes expressed by the intestinal epithelium. J. Nutr. 2004, 134, 2450S-2454S.
45. Alex, S.; Lange, K.; Amolo, T.; Grinstead, J.S.; Haakonsson, A.K.; Szalowska, E.; Koppen, A.; Mudde, K.; Haenen, D.; Roelofsen, H.; et al. Short-chain fatty acids stimulate angiopoietin-like 4 synthesis in human colon adenocarcinoma cells by activating peroxisome proliferator-activated receptor γ. Mol. Cell. Biol. 2013, 33, 1303-1316.
46. Brown, A.J.; Goldsworthy, S.M.; Barnes, A.A.; Eilert, M.M.; Tcheang, L.; Daniels, D.; Muir, A.I.; Wigglesworth, M.J.; Kinghorn, I.; Fraser, N.J. The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J. Biol. Chem. 2003, 278, 11312-11319.
47. Tazoe, H.; Otomo, Y.; Kaji, I.; Tanaka, R.; Karaki, S.I.; Kuwahara, A. Roles of short-chain fatty acids receptors, GPR41 and GPR43 on colonic functions. J. Physiol. Pharmacol. 2008, 59 (Suppl. 2), 251-262.
48. Leser, T.D.; Mølbak, L. Better living through microbial action: The benefits of the mammalian gastrointestinal microbiota on the host. Environ. Microbiol. 2009, 11, 2194-2206.
49. Lopez, C.A.; Kingsbury, D.D.; Velazquez, E.M.; Baumler, A.J. Collateral damage: Microbiota-derived metabolites and immune function in the antibiotic era. Cell Host Microbe 2014, 16, 156-163.
50. Savard, P.; Lamarche, B.; Paradis, M.E.; Thiboutot, H.; Laurin, E.; Roy, D. Impact of Bifidobacterium animalis subsp. lactis BB-12 and, Lactobacillus acidophilus LA-5-containing yoghurt, on fecal bacterial counts of healthy adults. Int. J. Food Microbiol. 2011, 149, 50-57.
51. Yamano, T.; Iino, H.; Takada, M.; Blum, S.; Rochat, F.; Fukushima, Y. Improvement of the human intestinal flora by ingestion of the probiotic strain Lactobacillus johnsonii La1. Br. J. Nutr. 2006, 95, 303-312.
52. Lahti, L.; Salonen, A.; Kekkonen, R.A.; Salojärvi, J.; Jalanka-Tuovinen, J.; Palva, A.; Orešič, M.; de Vos, W.M. Associations between the human intestinal microbiota, Lactobacillus rhamnosus GG and serum lipids indicated by integrated analysis of high-throughput profiling data. PeerJ 2013, 1, e32.
53. Rajkumar, H.; Kumar, M.; Das, N.; Kumar, S.N.; Challa, H.R.; Nagpal, R. Effect of Probiotic Lactobacillus salivarius UBL S22 and Prebiotic Fructo-oligosaccharide on Serum Lipids, Inflammatory Markers, Insulin Sensitivity, and Gut Bacteria in Healthy Young Volunteers: A Randomized Controlled Single-Blind Pilot Study. J. Cardiovasc. Pharmacol. Ther. 2015, 20, 289-298.
54. Berni, C.R.; Sangwan, N.; Stefka, A.T.; Nocerino, R.; Paparo, L.; Aitoro, R.; Calignano, A.; Khan, A A.; Gilbert, J.A.; Nagler, C.R. Lactobacillus rhamnosus GG-supplemented formula expands butyrate-producing bacterial strains in food allergic infants. ISME J. 2015, 10, 742-750.
55. Kristensen, N.B.; Bryrup, T.; Allin, K.H.; Nielsen, T.; Hansen, T.H.; Pedersen, O. Alterations in fecal microbiota composition by probiotic supplementation in healthy adults: A systematic review of randomized controlled trials. Genome. Med. 2016, 8, 52.
56. Morita, H.; Shiratori, C.; Murakami, M.; Takami, H.; Toh, H.; Kato, Y.; Nakajima, F.; Takagi, M.; Akita, H.; Masaoka, T.; et al. Sharpea azabuensis gen. nov., sp. nov., a Gram-positive, strictly anaerobic bacterium isolated from the faeces of thoroughbred horses. Int. J. Syst. Evol. Microbiol. 2008, 58, 2682-2686.
57. Eloe-Fadrosh, E.A.; Brady, A.; Crabtree, J.; Drabek, E.F.; Ma, B.; Mahurkar, A.; Ravel, J.; Haverkamp, M.; Fiorino, A.M.; Botelho, C.; et al. Functional dynamics of the gut microbiome in elderly people during probiotic consumption. MBio 2015, 6, doi:10.1128/mBio.00231-15
58. McNulty, N.P.; Yatsunenko, T.; Hsiao, A.; Faith, J.J.; Muegge, B.D.; Goodman, A.L.; Henrissat, B.; Oozeer, R.; Cools-Portier, S.; Gobert, G.; et al. The Impact of a Consortium of Fermented Milk Strains on the Gut Microbiome of Gnotobiotic Mice and Monozygotic Twins. Sci. Transl. Med. 2011, 3, 106ra106.
59. Chu, H.; Mazmanian, S.K. Innate immune recognition of the microbiota promotes host-microbial symbiosis. Nat. Immunol. 2013, 14, 668-675.
60. Turroni, F.; Milani, C.; Duranti, S.; Mancabelli, L.; Mangifesta, M.; Viappiani, A.; Lugli, G.A.; Ferrario, C.; Gioiosa, L.; Ferrarini, A.; et al. Deciphering bifidobacterial-mediated metabolic interactions and their impact on gut microbiota by a multi-omics approach. ISME J. 2016, 10, 1656-1668.