Browse > Article
http://dx.doi.org/10.4014/jmb.1802.02019

Probiotic Potential of Enterococcus faecium Isolated from Chicken Cecum with Immunomodulating Activity and Promoting Longevity in Caenorhabditis elegans  

Sim, Insuk (Department of Integrated Biomedical and Life Sciences, College of Health Science, Korea University)
Park, Keun-Tae (Department of Research and Development Center, Milae Resources ML Co. Ltd.)
Kwon, Gayeung (Department of Public Health Science (BK21 PLUS Program), Graduate School, Korea University)
Koh, Jong-Ho (Department of Bio-Food Analysis and Processing, Bio-Campus Korea Polytechnic College)
Lim, Young-Hee (Department of Integrated Biomedical and Life Sciences, College of Health Science, Korea University)
Publication Information
Journal of Microbiology and Biotechnology / v.28, no.6, 2018 , pp. 883-892 More about this Journal
Abstract
Probiotics, including Enterococcus faecium, confer a health benefit on the host. An Enterococcus strain was isolated from healthy chicken cecum, identified as E. faecium by 16S rDNA gene sequence analysis, and designated as E. faecium L11. To evaluate the potential of E. faecium L11 as a probiotic, the gastrointestinal tolerance, immunomodulatory activity, and lifespan extension properties of the strain were assayed. E. faecium L11 showed >66% and >62% survival in artificial gastric juice (0.3% pepsin, pH 2.5) and simulated small intestinal juice (0.5% bile salt and 0.1% pancreatin), respectively. Heat-killed E. faecium L11 significantly (p < 0.05) increased immune cell proliferation compared with controls, and stimulated the production of cytokines (IL-6 and $TNF-{\alpha}$) by activated macrophages obtained from ICR mice. In addition, E. faecium L11 showed a protective effect against Salmonella Typhimurium infection in Caenorhabditis elegans. In addition, feeding E. faecium L11 significantly (p < 0.05) extended the lifespan of C. elegans compared with the control. Furthermore, genes related to aging and host defense were upregulated in E. faecium L11-fed worms. In conclusion, E. faecium L11, which prolongs the lifespan of C. elegans, may be a potent probiotic supplement for livestock.
Keywords
Enterococcus faecium; immunomodulatory activity; probiotics; Caenorhabditis elegans; lifespan extension;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Millet AC, Ewbank JJ. 2004. Immunity in Caenorhabditis elegans. Curr. Opin. Immunol. 16: 4-9.   DOI
2 Okuyama T, Inoue H, Ookuma S, Satoh T, Kano K, Honjoh S, et al. 2010. The ERK-MAPK pathway regulates longevity through SKN-1 and insulin-like signaling in Caenorhabditis elegans. J. Biol. Chem. 285: 30274-30281.   DOI
3 Engelmann I, Pujol N. 2010. Innate immunity in C. elegans, pp. 105-121. In Soderhall K (ed), Invertebrate Immunity. Advances in Experimental Medicine and Biology, Vol. 708. Springer, Boston, MA.
4 Araujo TF, Ferreira CLDLF. 2013. The genus Enterococcus as probiotic: safety concerns. Braz. Arch. Biol. Technol. 56: 457-466.   DOI
5 Wu D, Rea SL, Yashin AI, Johnson TE. 2006. Visualizing hidden heterogeneity in isogenic populations of C. elegans. Exp. Gerontol. 41: 261-270.   DOI
6 Burdine R D, Stern M J. 1996. Easy RNA isolation from C. elegans: a TRIZOL based method. Worm Breed. Gaz. 14: 10.
7 Greer E L, Dowlatshahi D , Banko MR, Villen J, Hoang K , Blanchard D, et al. 2007. An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr. Biol. 17: 1646-1656.   DOI
8 Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, et al. 2012. Primer3 - new capabilities and interfaces. Nucleic Acids Res. 40: e115.   DOI
9 Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the $2^{-{\Delta}{\Delta}CT}$ method. Methods 25: 402-408.   DOI
10 Zhao Y, Zhao L, Z heng X , Fu T, Guo H , Ren F. 2013. Lactobacillus salivarius strain FDB89 induced longevity in Caenorhabditis elegans by dietary restriction. J. Microbiol. 51: 183-188.   DOI
11 Joint FAO/WHO Working Group. 2002. Guidelines for the evaluation of probiotics in foods. Food and Agricultural Organization of the United Nations and World Health Organization FAO/WHO, London, Ontario, Canada.
12 Zhao T, Li Y, Liu B, Bronson RT, Halaweish I, Alam HB. 2014. Histone deacetylase III as a potential therapeutic target for the treatment of lethal sepsis. J. Trauma Acute Care Surg. 77: 913-919.   DOI
13 Mishra K, Padwad Y, Jain M, Karan D, Ganju L, Sawhney R. 2006. Aqueous extract of Rhodiola imbricata rhizome stimulates proinflammatory mediators via phosphorylated $l{\kappa}B$ and transcription factor nuclear factor-${\kappa}B$. Immunopharmacol. Immunotoxicol. 28: 201-212.   DOI
14 Turvey SE, Broide DH. 2010. Innate immunity. J. Allergy Clin. Immunol. 125: S24-S32.   DOI
15 Ricciardi A, Blaiotta G, Di Cerbo A, Succi M, Aponte M. 2014. Behaviour of lactic acid bacteria populations in Pecorino di Carmasciano cheese samples submitted to environmental conditions prevailing in the gastrointestinal tract: evaluation by means of a polyphasic approach. Int. J Food Microbiol. 179: 64-71.   DOI
16 Argyri AA, Zoumpopoulou G, Karatzas KAG, Tsakalidou E, Nychas GJE, Panagou EZ, et al. 2013. Selection of potential probiotic lactic acid bacteria from fermented olives by in vitro tests. Food Microbiol. 33: 282-291.   DOI
17 Hwang JH, Yang HS, Ra KS, Park SS, Yu KW. 2013. Intestinal immune system-modulating activity through Peyer's patch of flavonoid glycoside purified from Citrus unshiu peel. J. Food Biochem. 37: 151-160.   DOI
18 Li N, Russell WM, Douglas-Escobar M, Hauser N, Lopez M, Neu J. 2009. Live and heat-killed Lactobacillus rhamnosus GG: effects on proinflammatory and anti-inflammatory cytokines/ chemokines in gastrostomy-fed infant rats. Pediatr. Res. 66: 203-207.   DOI
19 Ranke J, Molter K, Stock F, Bottin-Weber U, Poczobutt J, Hoffmann J, et al. 2004. Biological effects of imidazolium ionic liquids with varying chain lengths in acute Vibrio fischeri and WST-1 cell viability assays. Ecotoxicol. Environ. Saf. 58: 396-404.   DOI
20 Yoon T J, Yu K-W, Shin K-S, Suh HJ. 2008. Innate immune stimulation of exo-polymers prepared from Cordyceps sinensis by submerged culture. Appl. Microbiol. Biotechnol. 80: 1087-1093.   DOI
21 Thomas TP, Goonewardena SN, Majoros IJ, Kotlyar A, Cao Z, Leroueil PR, et al. 2011. Folate-targeted nanoparticles show efficacy in the treatment of inflammatory arthritis. Arthritis Rheum. 63: 2671-2680.   DOI
22 Stiernagle T. 1999. Maintenance of C. elegans, pp. 51-67. In Hope IA (ed.), C. elegans: A Practical Approach. Oxford University Press, New York.
23 Gruber J , Ng LF, Poovathingal S K, Halliwell B . 2009. Deceptively simple but simply deceptive- Caenorhabditis elegans lifespan studies: considerations for aging and antioxidant effects. FEBS Lett. 583: 3377-3387.   DOI
24 Komura T, Ikeda T, Yasui C, Saeki S, Nishikawa Y . 2013. Mechanism underlying prolongevity induced by bifidobacteria in Caenorhabditis elegans. Biogerontology 14: 73-87.   DOI
25 Ikeda T, Yasui C, Hoshino K, Arikawa K, Nishikawa Y. 2007. Influence of lactic acid bacteria on longevity of Caenorhabditis elegans and host defense against Salmonella enterica serovar enteritidis. Appl. Environ. Microbiol. 73: 6404-6409.   DOI
26 Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.   DOI
27 Lee J, Yun HS, Cho KW, Oh S, Kim SH, Chun T, et al. 2011. Evaluation of probiotic characteristics of newly isolated Lactobacillus spp.: immune modulation and longevity. Int. J. Food Microbiol. 148: 80-86.   DOI
28 Ye M, Sun L, Yang R, Wang Z, Qi K. 2017. The optimization of fermentation conditions for producing cellulase of Bacillus amyloliquefaciens and its application to goose feed. R. Soc. Open Sci. 4: 171012.   DOI
29 Messaoudi S, Kergourlay G, Rossero A, Ferchichi M, Prevost H, Drider D, et al. 2011. Identification of lactobacilli residing in chicken ceca with antagonism against Campylobacter. Int. Microbiol. 14: 103-110.
30 Anandharaj M, Sivasankari B. 2014. Isolation of potential probiotic Lactobacillus oris HMI68 from mother's milk with cholesterol-reducing property. J. Biosci. Bioeng. 118: 153-159.   DOI
31 Bautista-Gallego J, Arroyo-Lopez F, Rantsiou K, Jimenez- Diaz R, Garrido-Fernandez A, Cocolin L. 2013. Screening of lactic acid bacteria isolated from fermented table olives with probiotic potential. Food Res. Int. 50: 135-142.   DOI
32 Cotter PD, Ross RP, Hill C. 2013. Bacteriocins - a viable alternative to antibiotics? Nat. Rev. Microbiol. 11: 95-105.   DOI
33 Tellez G, Pixley C, Wolfenden R, Layton S , Hargis B. 2012. Probiotics/direct fed microbials for Salmonella control in poultry. Food Res. Int. 45: 628-633.   DOI
34 Salim H, Kang H, Akter N , Kim D , Kim J , Kim M, et al. 2013. Supplementation of direct-fed microbials as an alternative to antibiotic on growth performance, immune response, cecal microbial population, and ileal morphology of broiler chickens. Poult. Sci. 92: 2084-2090.   DOI
35 Cao G, Zeng X, Chen A, Zhou L, Zhang L , Xiao Y, et al. 2013. Effects of a probiotic, Enterococcus faecium, on growth performance, intestinal morphology, immune response, and cecal microflora in broiler chickens challenged with Escherichia coli K88. Poult. Sci. 92: 2949-2955.   DOI
36 Huang Y, Li Y, Huang Q , Cui Z , Yu D, Rajput IR, et al. 2012. Effect of orally administered Enterococcus faecium EF1 on intestinal cytokines and chemokines production of suckling piglets. Pak. Vet. J. 32: 81-84.
37 Scharek L, Guth J, Reiter K, Weyrauch K, Taras D, Schwerk P, et al. 2005. Influence of a probiotic Enterococcus faecium strain on development of the immune system of sows and piglets. Vet. Immunol. Immunopathol. 105: 151-161.   DOI
38 Valeriano VD, Parungao-Balolong MM, Kang DK. 2014. In vitro evaluation of the mucin-adhesion ability and probiotic potential of Lactobacillus mucosae LM1. J. Appl. Microbiol. 117: 485-497.   DOI
39 Zhang R, Hou A. 2013. Host-microbe interactions in Caenorhabditis elegans. ISRN Microbiol. 2013: 356451.
40 Brestoff JR, Artis D. 2013. Commensal bacteria at the interface of host metabolism and the immune system. Nat. Immunol. 14: 676-684.   DOI
41 Hooper LV, Littman DR, Macpherson AJ. 2012. Interactions between the microbiota and the immune system. Science 336: 1268-1273.   DOI
42 Niu X, Wang Y, Li W, Zhang H, Wang X, Mu Q, et al. 2015. Esculin exhibited anti-inflammatory activities in vivo and regulated TNF-${\alpha}$ and IL-6 production in LPS-stimulated mouse peritoneal macrophages in vitro through MAPK pathway. Int. Immunopharmacol. 29: 779-786.   DOI
43 Schepetkin IA, Xie G, Kirpotina LN, Klein RA, Jutila MA, Quinn MT. 2008. Macrophage immunomodulatory activity of polysaccharides isolated from Opuntia polyacantha. Int. Immunopharmacol. 8: 1455-1466.   DOI
44 Renshaw M, Rockwell J, Engleman C, Gewirtz A, Katz J, Sambhara S. 2002. Cutting edge: impaired Toll-like receptor expression and function in aging. J. Immunol. 169: 4697-4701.   DOI
45 Radtke S, Wuller S, Yang X-P, Lippok BE, Mutze B, Mais C, et al. 2010. Cross-regulation of cytokine signalling: proinflammatory cytokines restrict IL-6 signalling through receptor internalisation and degradation. J. Cell Sci. 123: 947-959.   DOI
46 Grompone G, Martorell P, Llopis S, Gonzalez N, Genoves S, Mulet AP, et al. 2012. Anti-inflammatory Lactobacillus rhamnosus CNCM I-3690 strain protects against oxidative stress and increases lifespan in Caenorhabditis elegans. PLoS One 7: e52493.   DOI
47 Kurz CL, Ewbank JJ. 2003. Caenorhabditis elegans: an emerging genetic model for the study of innate immunity. Nat. Rev. Genet. 4: 380-390.
48 Signorini M, Soto L, Zbrun M, Sequeira G, Rosmini M, Frizzo L. 2012. Impact of probiotic administration on the health and fecal microbiota of young calves: a meta-analysis of randomized controlled trials of lactic acid bacteria. Res. Vet. Sci. 93: 250-258.   DOI
49 Wang Z, Burwinkel M, Chai W, Lange E, Blohm U, Breithaupt A, et al. 2014. Dietary Enterococcus faecium NCIMB 10415 and zinc oxide stimulate immune reactions to trivalent influenza vaccination in pigs but do not affect virological response upon challenge infection. PLoS One 9: e87007.   DOI
50 Tsai Y-T, Cheng P-C, Pan T-M. 2012. The immunomodulatory effects of lactic acid bacteria for improving immune functions and benefits. Appl. Microbiol. Biotechnol. 96: 853-862.   DOI