Lactobacillus plantarum BSGP201683 Isolated from giant panda feces attenuated inflammation and improved gut microflora in mice challenged with enterotoxigenic Escherichia coli

Frontiers in Microbiology

Volumn 8, Issue SEP, 2017, Pages

  Liu, Qian ^a   Ni, Xueqin ^a   Wang, Qiang ^b   Peng, Zhirong ^a   Niu, Lili ^b   Wang, Hengsong ^a   Zhou, Yi ^a   Sun, Hao ^c   Pan, Kangcheng ^c   Jing, Bo ^c   Zeng, Dong ^a  

^a SICHUAN AGRICULTURAL UNIVERSITY   (China)

^b Chengdu Wildlife Institute   (China)

^c Key Laboratory of Animal Diseases and Human Health of Sichuan Province   (China)

Author keywords

Enterotoxigenic Escherichia coli K88; Gut microflora; Immune response; Intestinal barrier; Lactobacillus plantarum BSGP201683

Indexed keywords

AMINE OXIDASE (COPPER CONTAINING); CLAUDIN 1; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LACTIC ACID; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN ZO1; TIGHT JUNCTION PROTEIN; TOLL LIKE RECEPTOR 4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM ISOLATION; BACTEROIDETES; BLOOD ANALYSIS; COLONY FORMING UNIT; CONTROLLED STUDY; ENTERITIS; ENTEROBACTERIACEAE; ENTEROTOXIGENIC ESCHERICHIA COLI; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FECES ANALYSIS; INTESTINE FLORA; LACTOBACILLUS PLANTARUM; LEUKOCYTE; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SPECTROPHOTOMETRY;

EID: 85030165656     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.01885     Document Type: Article

References (60)

1. Archambaud, C., Nahori, M. A., Soubigou, G., Bécavin, C., Laval, L., Lechat, P., et al. (2012). Impact of lactobacilli on orally acquired listeriosis. Proc. Natl. Acad. Sci. U.S.A. 109, 16684-16689. doi: 10.1073/pnas.1212809109
2. Baehner, R. L. (1975). Microbe ingestion and killing by neutrophils: normal mechanisms and abnormalities. Clin. Haematol. 4, 609-633.
3. Barba-Vidal, E., Castillejos, L., López-Colom, P., Rivero Urgell, M., Moreno Mu-oz, J. A., and Martín-Orúe, S. M. (2017). Evaluation of the probiotic strain Bifidobacterium longum subsp. Infantis CECT 7210 capacities to improve health status and fight digestive pathogens in a piglet model. Front. Microbiol. 8:533. doi: 10.3389/fmicb.2017.00533
4. Barletta, F., Ochoa, T. J., and Cleary, T. G. (2013). Multiplex Real-Time PCR (MRT-PCR) for Diarrheagenic. Methods Mol. Biol. 943, 307-314. doi: 10.1007/978-1-60327-353-4_21
5. Bartosch, S., Fite, A., Macfarlane, G. T., and McMurdo, M. E. (2004). Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Appl. Environ. Microbiol. 70, 3575-3581. doi: 10.1128/AEM.70.6.3575-3581.2004
6. Bouhnik, Y., Raskine, L., Simoneau, G., Vicaut, E., Neut, C., Flourié, B., et al. (2004). The capacity of nondigestible carbohydrates to stimulate fecal bifidobacteria in healthy humans: a double-blind, randomized, placebo-controlled, parallel-group, dose-response relation study. Am. J. Clin. Nutr. 80:1658.
7. Candela, M., Perna, F., Carnevali, P., Vitali, B., Ciati, R., Gionchetti, P., et al. (2008). Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 production. Int. J. Food Microbiol. 125, 286-292. doi: 10.1016/j.ijfoodmicro.2008.04.012
8. Cassatella, M. A. (1999). Neutrophil-derived proteins: selling cytokines by the pound. Adv. Immunol. 73, 369-509. doi: 10.1016/S.0065-2776(08)60791-9
9. Chen, X. I., Yin, M., Wang, X., Pu, Z., Ma, Y., and Chen, Z. (2015). Isolation and preliminary identification of intestinal pathogens of captive giant panda (In Chinese). J. Mianyang Normal Univ. doi: 10.3969/j.issn.1672-612x.2015.02.001
10. Chen, X. Y., Woodward, A., Zijlstra, R. T., and Gänzle, M. G. (2014). Exopolysaccharides synthesized by Lactobacillus reuteri protect against enterotoxigenic Escherichia coli in piglets. Appl. Environ. Microbiol. 80, 5752. doi: 10.1128/AEM.01782-14
11. Collado, M. C., Grzeskowiak, L., and Salminen, S. (2007). Probiotic strains and their combination inhibit in vitro adhesion of pathogens to pig intestinal mucosa. Curr. Microbiol. 55, 260-265. doi: 10.1007/s00284-007-0144-8
12. Collado, M. C., Isolauri, E., and Salminen, S. (2008). Specific probiotic strains and their combinations counteract adhesion of Enterobacter sakazakii to intestinal mucus. FEMS Microbiol. Lett. 285, 58-64. doi: 10.1111/j.1574-6968.2008.01211.x
13. Demissie, D. E., Kaplan, S. L., Romero, J. R., Leake, J. A., Barson, W. J., Halasa, N. B., et al. (2013). Altered neutrophil counts at diagnosis of invasive meningococcal infection in children. Pediatr. Infect. Dis. J. 32, 1070-1072. doi: 10.1097/INF.0b013e31829e31f1
14. Duchet-Suchaux, M., Le Maitre, C., and Bertin, A. (1990). Differences in susceptibility of inbred and outbred infant mice to enterotoxigenic Escherichia coli of bovine, porcine and human origin. J. Med. Microbiol. 31, 185-190. doi: 10.1099/00222615-31-3-185
15. Elli, M., Zink, R., Rytz, A., Reniero, R., and Morelli, L. (2000). Iron requirement of Lactobacillus spp. in completely chemically defined growth media. J. Appl. Microbiol. 88, 695-703. doi: 10.1046/j.1365-2672.2000.01013.x
16. Ewaschuk, J. B., Naylor, J. M., and Zello, G. A. (2005). D-lactate in human and ruminant metabolism. J. Nutr. 135, 1619-1625.
17. Fasano, A., and Shea-Donohue, T. (2005). Mechanisms of disease: the role of intestinal barrier function in the pathogenesis of gastrointestinal autoimmune diseases. Nat. Clin. Pract. Gastroenterol. Hepatol. 2, 416-422. doi: 10.1038/ncpgasthep0259
18. Fiesel, A., Gessner, D. K., Most, E., and Eder, K. (2014). Effects of dietary polyphenol-rich plant products from grape or hop on pro-inflammatory gene expression in the intestine, nutrient digestibility and faecal microbiota of weaned pigs. BMC Vet. Res. 10:196. doi: 10.1186/s12917-014-0196-5
19. Frece, J., Kos, B., Beganovic, J., Vukovic, S., and Šuškovic, J. (2006). In vivo testing of functional properties of three selected probiotic strains. World J. Microbiol. Biotechnol. 21, 1401-1408. doi: 10.1007/s11274-005-5741-8
20. Galdeano, C., and Perdigon, G. (2004). Role of viability of probiotic strains in their persistence in the gut and in mucosal immune stimulation. J. Appl. Microbiol. 97:673. doi: 10.1111/j.1365-2672.2004.02353.x
21. Gareau, M. G., Sherman, P. M., and Walker, W. A. (2010). Probiotics and the gut microbiota in intestinal health and disease. Nat. Rev. Gastroenterol. Hepatol. 7, 503-514. doi: 10.1038/nrgastro.2010.117
22. Geier, M. S., Mikkelsen, L. L., Torok, V. A., Allison, G. E., Olnood, C. G., Boulianne, M., et al. (2010). Comparison of alternatives to in-feed antimicrobials for the prevention of clinical necrotic enteritis. J. Appl. Microbiol. 109, 1329-1338. doi: 10.1111/j.1365-2672.2010.04758.x
23. Groschwitz, K. R., and Hogan, S. P. (2009). Intestinal barrier function: molecular regulation and disease pathogenesis. J. Allergy Clin. Immunol. 124, 21-22. doi: 10.1016/j.jaci.2009.05.038
24. Guo, X., Xia, X., Tang, R., Zhou, J., Zhao, H., and Wang, K. (2008). Development of a real-time PCR method for Firmicutes and Bacteroidetes in faeces and its application to quantify intestinal population of obese and lean pigs. Lett. Appl. Microbiol. 47, 367-373. doi: 10.1111/j.1472-765X.2008.02408.x
25. Hooper, L. V. (2009). Do symbiotic bacteria subvert host immunity? Nat. Rev. Microbiol. 7, 367-374. doi: 10.1038/nrmicro2114
26. Hunt, L., Gupta-Wright, A., Simms, V., Tamba, F., Knott, V., Tamba, K., et al. (2015). Clinical presentation, biochemical, and haematological parameters and their association with outcome in patients with Ebola virus disease: an observational cohort study. Lancet Infect. Dis. 15, 1292-1299. doi: 10.1016/S1473-3099(15)00144-9
27. Jones, S. E., and Versalovic, J. (2009). Probiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors. BMC Microbiol. 9:935. doi: 10.1186/1471-2180-9-35
28. Lee, J. S., Awji, E. G., Lee, S. J., Tassew, D. D., Park, Y. B., Park, K. S., et al. (2012). Effect of Lactobacillus plantarum CJLP243 on the growth performance and cytokine response of weaning pigs challenged with enterotoxigenic Escherichia coli. J. Anim. Sci. 90, 3709-3717. doi: 10.2527/jas.2011-4434
29. Li, X. Q., Zhu, Y-H., Zhang, H-F., Yue, Y., Cai, Z-X., Lu, Q-P., et al. (2012). Risks associated with high-dose Lactobacillus rhamnosus in an Escherichia coli model of piglet diarrhoea: intestinal microbiota and immune imbalances. PLoS ONE 7:e40666. doi: 10.1371/journal.pone.0040666
30. Liu, H., French, B. A., Nelson, T. J., Li, J., Tillman, B., and French, S. W. (2015). IL-8 signaling is up regulated in alcoholic hepatitis and DDC fed mice with Mallory denk bodies (MDBs) present. Exp. Mol. Pathol. 99, 320-325. doi: 10.1016/j.yexmp.2015.08.002
31. Mennigen, R., and Bruewer, M. (2009). Effect of probiotics on intestinal barrier function. Ann. N. Y. Acad. Sci. 1165, 183-189. doi: 10.1111/j.1749-6632.2009.04059.x
32. Mileti, E., Matteoli, G., Iliev, I. D., and Rescigno, M. (2009). Comparison of the immunomodulatory properties of three probiotic strains of Lactobacilli using complex culture systems: prediction for in vivo efficacy. PLoS ONE 4:e7056. doi: 10.1371/journal.pone.0007056
33. Mizumachi, K., Aoki, R., Ohmori, H., Saeki, M., and Kawashima, T. (2009). Effect of fermented liquid diet prepared with Lactobacillus plantarum LQ80 on the immune response in weaning pigs. Animal 3, 670-676. doi: 10.1017/S1751731109003978
34. Nakamura, K., Arakawa, K., Kawai, Y., Yasuta, N., Chujo, T., Watanabe, M., et al. (2013). Food preservative potential of gassericin A-containing concentrate prepared from cheese whey culture supernatant of Lactobacillus gasseri LA39. Anim. Sci. J. 84, 144-149. doi: 10.1111/j.1740-0929.2012.01048.x
35. Nataro, J. P., and Kaper, J. B. (1998). Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11, 142.
36. Nguyen, T. D., Kang, J. H., and Lee, M. S. (2007). Characterization of Lactobacillus plantarum PH04, a potential probiotic bacterium with cholesterol-lowering effects. Int. J. Food Microbiol. 113, 358-361. doi: 10.1016/j.ijfoodmicro.2006.08.015
37. Nishida, S., Ishii, M., Nishiyama, Y., Abe, S., Ono, Y., and Sekimizu, K. (2017). Lactobacillus paraplantarum 11-1 isolated from rice bran pickles activated innate immunity and improved survival in a silkworm bacterial infection model. Front. Microbiol. 8:436. doi: 10.3389/fmicb.2017.00436
38. Pandey, N., Malik, R. K., Kaushik, J. K., and Singroha, G. (2013). Gassericin A: a circular bacteriocin produced by Lactic acid bacteria Lactobacillus gasseri. World J. Microbiol. Biotechnol. 29, 1977-1987. doi: 10.1007/s11274-013-1368-3
39. Peng, Z., Zeng, D., Wang, Q., Niu, L., Ni, X., Zou, F., et al. (2016). Decreased microbial diversity and Lactobacillus group in the intestine of geriatric giant pandas (Ailuropoda melanoleuca). World J. Microbiol. Biotechnol. 32, 1-10. doi: 10.1007/s11274-016-2034-3
40. Porter, C. K., Riddle, M. S., Tribble, D. R., Louis Bougeois, A., McKenzie, R., Isidean, S. D., et al. (2011). A systematic review of experimental infections with enterotoxigenic Escherichia coli (ETEC). Vaccine 29, 5869-5885. doi: 10.1016/j.vaccine.2011.05.021
41. Ren, W., Liu, S., Chen, S., Zhang, F., Li, N., Yin, J., et al. (2013). Dietary L-glutamine supplementation increases Pasteurella multocida burden and the expression of its major virulence factors in mice. Amino Acids 45, 947-955. doi: 10.1007/s00726-013-1551-8
42. Rinttilä, T., Kassinen, A., Malinen, E., Krogius, L., and Palva, A. (2004). Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J. Appl. Microbiol. 97, 1166-1177. doi: 10.1111/j.1365-2672.2004.02409.x
43. Roselli, M., Finamore, A., Britti, M. S., Konstantinov, S. R., Smidt, H., de Vos, W. M., et al. (2007). The novel porcine Lactobacillus sobrius strain protects intestinal cells from enterotoxigenic Escherichia coli K88 infection and prevents membrane barrier damage. J. Nutr. 137, 2709-2716.
44. Suzuki, T. (2013). Regulation of intestinal epithelial permeability by tight junctions. Cell. Mol. Life Sci. 70, 631-659. doi: 10.1007/s00018-012-1070-x
45. Taur, Y., and Pamer, E. G. (2013). The intestinal microbiota and susceptibility to infection in immunocompromised patients. Curr. Opin. Infect. Dis. 26, 332-337. doi: 10.1097/QCO.0b013e3283630dd3
46. Wang, K., Qi, Y., Yi, S., Pei, Z., Pan, N., and Hu, G. (2016). Mouse duodenum as a model of inflammation induced by enterotoxigenic Escherichia coli K88. J. Veter. Res. 60, 19-23. doi: 10.1515/jvetres-2016-0004
47. Wang, Y., Xu, N., Xi, A., Ahmed, Z., Zhang, B., and Bai, X. (2009). Effects of Lactobacillus plantarum MA2 isolated from Tibet kefir on lipid metabolism and intestinal microflora of rats fed on high-cholesterol diet. Appl. Microbiol. Biotechnol. 84, 341-347. doi: 10.1007/s00253-009-2012-x
48. Wen, K., Li, G., Bui, T., Liu, F., Li, Y., Kocher, J., et al. (2012). High dose and low dose Lactobacilli acidophilus exerted differential immune modulating effects on T cell immune responses induced by an oral human rotavirus vaccine in gnotobiotic pigs. Vaccine 30, 1198-1207. doi: 10.1016/j.vaccine.2011.11.107
49. Wen, K., Liu, F., Li, G., Bai, M., Kocher, J., Yang, X., et al. (2015). Lactobacillus rhamnosus GG dosage affects the adjuvanticity and protection against rotavirus diarrhea in gnotobiotic pigs. J. Pediatr. Gastroenterol. Nut. 60:834. doi: 10.1097/MPG.0000000000000694
50. Wijtten, P. J., van der Meulen, J., and Verstegen, M. W. (2011). Intestinal barrier function and absorption in pigs after weaning: a review. Br. J. Nutr. 105, 967-981. doi: 10.1017/S0007114510005660
51. Wu, Y., Wang, Y., Zhou, H., Wang, B., Sun, Q., Fu, A., et al. (2017). ProbioticBacillus amyloliquefaciensSC06 induces autophagy to protect against pathogens in macrophages. Front. Microbiol. 8:469. doi: 10.3389/fmicb.2017.00469
52. Xun, W., Shi, L., Zhou, H., Hou, G., Cao, T., and Zhao, C. (2015). Effects of curcumin on growth performance, jejunal mucosal membrane integrity, morphology and immune status in weaned piglets challenged with enterotoxigenic Escherichia coli. Int. Immunopharmacol. 27, 46-52. doi: 10.1016/j.intimp.2015.04.038
53. Yang, K. M., Jiang, Z. Y., Zheng, C. T., Wang, L., and Yang, X. F. (2014). Effect of on diarrhea and intestinal barrier function of young piglets challenged with enterotoxigenic K88. J. Anim. Sci. 92, 1496-14503. doi: 10.2527/jas.2013-6619
54. Yin, M., Zhang, L., Sun, X. M., Mao, L. F., and Pan, J. (2009). Lack of apoE causes alteration of cytokines expression in young mice liver. Mol. Biol. Rep. 37, 2049-2054. doi: 10.1007/s11033-009-9660-x
55. Yu, Q., Yuan, L., Deng, J., and Yang, Q. (2015). Lactobacillus protects the integrity of intestinal epithelial barrier damaged by pathogenic bacteria. Front. Cell. Infect. Microbiol. 5:26. doi: 10.3389/fcimb.2015.00026
56. Zhang, Z., Xu, Y. Q., Liu, H. Y., Lai, T., Ma, J. L., Wang, J. F., et al. (2010). Evaluation of Lactobacillus rhamnosus GG using an Escherichia coli K88 model of piglet diarrhoea: effects on diarrhoea incidence, faecal microflora and immune responses. Vet. Microbiol. 141, 142-148. doi: 10.1016/j.vetmic.2009.09.003
57. Zhao, L., Luo, L., Jia, W., Xiao, J., Huang, G., Tian, G., et al. (2014). Serum diamine oxidase as a hemorrhagic shock biomarker in a rabbit model. PLoS ONE 9:e102285. doi: 10.1371/journal.pone.0102285
58. Zhong, W., Zhao, Y., McClain, C. J., Kang, Y. J., and Zhou, Z. (2010). Inactivation of hepatocyte nuclear factor-4a mediates alcohol-induced downregulation of intestinal tight junction proteins. Am. J. Physiol. Gastrointest. Liver Physiol. 299, 1251-1254. doi: 10.1152/ajpgi.00515.2009
59. Zhu, Y. H., Li, X. Q., Zhang, W., Zhou, D., Liu, H. Y., Wang, J. F., et al. (2014). Dose-dependent effects of Lactobacillus rhamnosus on serum interleukin-17 production and intestinal T-cell responses in pigs challenged with Escherichia coli. Appl. Environ. Microbiol. 80, 1787-1798. doi: 10.1128/AEM.03668-13
60. Zughaier, S. M., Zimmer, S. M., Datta, A., Carlson, R. W., and Stephens, D. S. (2005). Differential induction of the toll-like receptor 4-MyD88-dependent and-independent signaling pathways by endotoxins. Infect. Immun. 73, 2940-2950. doi: 10.1128/IAI.73.5.2940-2950.2005