Oral administration of Lactobacillus plantarum 06CC2 prevents experimental colitis in mice via an anti‑inflammatory response

Tanaka,Akihito; Kanmura,Shuji; Morinaga,Yuko; Kawabata,Katsuto; Arima,Shiho; Sasaki,Fumisato; Nasu,Yuichirou; Tanoue,Shiroh; Hashimoto,Shinichi; Takeshita,Masahiko; Takeda,Shiro; Ido,Akio

doi:10.3892/mmr.2020.10925

Oral administration of Lactobacillus plantarum 06CC2 prevents experimental colitis in mice via an anti‑inflammatory response

Authors:
- Akihito Tanaka
- Shuji Kanmura
- Yuko Morinaga
- Katsuto Kawabata
- Shiho Arima
- Fumisato Sasaki
- Yuichirou Nasu
- Shiroh Tanoue
- Shinichi Hashimoto
- Masahiko Takeshita
- Shiro Takeda
- Akio Ido
View Affiliations

Affiliations: Digestive and Lifestyle Diseases, Department of Human and Environmental Sciences, Kagoshima University Graduate School of Medical and Dental Sciences, Kagoshima 890‑8544, Japan, Research and Development Division, Minami Nihon Rakuno Kyodo Co., Ltd., Miyazaki 885‑0073, Japan, Department of Animal Science and Biotechnology, School of Veterinary Medicine, Azabu University, Kanagawa 252‑5201, Japan
Published online on: January 9, 2020 https://doi.org/10.3892/mmr.2020.10925
Pages: 1181-1191
Copyright: © Tanaka et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Dysbiosis of the enteric microbiota causes gastrointestinal diseases, including colitis. The present study investigated the beneficial effect of Lactobacillus plantarum 06CC2 in experimental colitis in mice. An experimental colitis model in C57BL6 mice was induced using dextran sulfate sodium. Mice were orally administered 06CC2 (06CC2 group) or PBS only (control group) by gavage. The disease activity index (DAI), histological grading, and colon tissue and colonic lamina propria mononuclear cells (LPMCs) were examined macroscopically and histopathologically, and the expression levels of inflammation‑associated cytokines (IL‑6, IL‑12, TNF‑α and IL‑10) in these samples were determined. Compared with the control group, the 06CC2 group exhibited a significantly lower DAI (1.5±0.8 vs. 0.2±0.3, respectively; P<0.05) and pathology score (6.3±1.5 vs. 3.8±1.3, respectively; P<0.05). IL‑10 expression in colonic LPMCs was higher in the 06CC2 group than in the control group, although there was no significant difference in IFN‑γ, IL‑6 or IL‑12 expression in colonic LPMCs between the two groups. In addition, 06CC2 stimulated the production of IL‑10 from CD11b‑positive cells and CD11c‑positive cells in the colon. The 06CC2 strain induced IL‑10 production in the colon and attenuated colon inflammation.

View Figures

View References

1	Khor B, Gardet A and Xavier RJ: Genetics and pathogenesis of inflammatory bowel disease. Nature. 474:307–317. 2011. View Article : Google Scholar : PubMed/NCBI
2	Garrett WS, Lord GM, Punit S, Lugo-Villarino G, Mazmanian SK, Ito S, Glickman JN and Glimcher LH: Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell. 131:33–45. 2007. View Article : Google Scholar : PubMed/NCBI
3	Elinav E, Strowig T, Kau AL, Henao-Mejia J, Thaiss CA, Booth CJ, Peaper DR, Bertin J, Eisenbarth SC, Gordon JI and Flavell RA: NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell. 145:745–757. 2011. View Article : Google Scholar : PubMed/NCBI
4	Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, Fukuda S, Saito T, Narushima S, Hase K, et al: Treg induction by a rationally selected mixture of clostridia strains from the human microbiota. Nature. 500:232–236. 2013. View Article : Google Scholar : PubMed/NCBI
5	Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, Cheng G, Yamasaki S, Saito T, Ohba Y, et al: Induction of colonic regulatory T cells by indigenous Clostridium species. Science. 331:337–341. 2011. View Article : Google Scholar : PubMed/NCBI
6	Round JL and Mazmanian SK: Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci USA. 107:12204–12209. 2010. View Article : Google Scholar : PubMed/NCBI
7	Round JL, Lee SM, Li J, Tran G, Jabri B, Chatila TA and Mazmanian SK: The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science. 332:974–977. 2011. View Article : Google Scholar : PubMed/NCBI
8	Sartor RB: Microbial influences in inflammatory bowel diseases. Gastroenterology. 134:577–594. 2008. View Article : Google Scholar : PubMed/NCBI
9	Kostic AD, Xavier RJ and Gevers D: The microbiome in inflammatory bowel disease: Current status and the future ahead. Gastroenterology. 146:1489–1499. 2014. View Article : Google Scholar : PubMed/NCBI
10	Llopis M, Antolin M, Carol M, Borruel N, Casellas F, Martinez C, Espín-Basany E, Guarner F and Malagelada JR: Lactobacillus casei downregulates commensals' inflammatory signals in Crohn's disease mucosa. Inflammatory Bowel Dis. 15:275–283. 2009. View Article : Google Scholar
11	Kelly D, Campbell JI, King TP, Grant G, Jansson EA, Coutts AG, Pettersson S and Conway S: Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nat Immunol. 5:104–112. 2004. View Article : Google Scholar : PubMed/NCBI
12	Liu YW, Su YW, Ong WK, Cheng TH and Tsai YC: Oral administration of Lactobacillus plantarum K68 ameliorates DSS-induced ulcerative colitis in BALB/c mice via the anti-inflammatory and immunomodulatory activities. Int Immunopharmacol. 11:2159–2166. 2011. View Article : Google Scholar : PubMed/NCBI
13	Takeda S, Yamasaki K, Takeshita M, Kikuchi Y, Tsend-Ayush C, Dashnyam B, Ahhmed AM, Kawahara S and Muguruma M: The investigation of probiotic potential of lactic acid bacteria isolated from traditional Mongolian dairy products. Anim Sci J. 82:571–579. 2011. View Article : Google Scholar : PubMed/NCBI
14	Takeda S, Takeshita M, Kikuchi Y, Dashnyam B, Kawahara S, Yoshida H, Watanabe W, Muguruma M and Kurokawa M: Efficacy of oral administration of heat-killed probiotics from Mongolian dairy products against influenza infection in mice: Alleviation of influenza infection by its immunomodulatory activity through intestinal immunity. Int Immunopharmacol. 11:1976–1983. 2011. View Article : Google Scholar : PubMed/NCBI
15	Egger B, Bajaj-Elliott M, MacDonald TT, Inglin R, Eysselein VE and Büchler MW: Characterisation of acute murine dextran sodium sulphate colitis: Cytokine profile and dose dependency. Digestion. 62:240–248. 2000. View Article : Google Scholar : PubMed/NCBI
16	Murthy SN, Cooper HS, Shim H, Shah RS, Ibrahim SA and Sedergran DJ: Treatment of dextran sulfate sodium-induced murine colitis by intracolonic cyclosporin. Dig Dis Sci. 38:1722–1734. 1993. View Article : Google Scholar : PubMed/NCBI
17	Hayashi A, Sato T, Kamada N, Mikami Y, Matsuoka K, Hisamatsu T, Hibi T, Roers A, Yagita H, Ohteki T, et al: A single strain of Clostridium butyricum induces intestinal IL-10-producing macrophages to suppress acute experimental colitis in mice. Cell Host Microbe. 13:711–722. 2013. View Article : Google Scholar : PubMed/NCBI
18	Cooper HS, Murthy SN, Shah RS and Sedergran DJ: Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest. 69:238–249. 1993.PubMed/NCBI
19	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI
20	Takeda S, Fujimoto R, Takenoyama SI, Takedhita M, Kikuchi Y, Tsend-Ayush C, Dashnyam B, Muguruma M and Kawahara S: Application of probiotics from Mongolian dairy products to fermented dairy products and its effects on human defecation. Food Sci Technol Res. 19:245–253. 2013. View Article : Google Scholar
21	Mabalirajan U, Dinda AK, Kumar S, Roshan R, Gupta P, Sharma SK and Ghosh B: Mitochondrial structural changes and dysfunction are associated with experimental allergicasthma. J Immunol. 181:3540–3548. 2008. View Article : Google Scholar : PubMed/NCBI
22	Rossi O, Khan MT, Schwarzer M, Hudcovic T, Srutkova D, Duncan SH, Stolte EH, Kozakova H, Flint HJ, Samsom JN, et al: Faecalibacterium prausnitzii strain HTF-F and its extracellular polymeric matrix attenuate clinical parameters in DSS-induced colitis. PLoS One. 10:e01230132015. View Article : Google Scholar : PubMed/NCBI
23	Atarashi K and Honda K: Microbiota in autoimmunity and tolerance. Curr Opin Immunol. 23:761–768. 2011. View Article : Google Scholar : PubMed/NCBI
24	Li H, Gong Y, Xie Y, Sun Q and Li Y: Clostridium butyricum protects the epithelial barrier by maintaining tight junction protein expression and regulating microflora in a murine model of dextran sodium sulfate-induced colitis. Scand J Gastroenterol. 53:1031–1042. 2018. View Article : Google Scholar : PubMed/NCBI
25	Liu YW, Ong WK, Su YW, Hsu CC, Cheng TH and Tsai YC: Anti-inflammatory effects of Lactobacillus brevis K65 on RAW 264.7 cells and in mice with dextran sulphate sodium-induced ulcerative colitis. Benef Microbes. 7:387–396. 2016. View Article : Google Scholar : PubMed/NCBI
26	Sun MC, Zhang FC, Yin X, Cheng BJ, Zhao CH, Wang YL, Zhang ZZ, Hao HW, Zhang TH and Ye HQ: Lactobacillus reuteri F-9-35 prevents DSS-induced colitis by inhibiting proinflammatory gene expression and restoring the gut Microbiota in mice. J Food Sci. 83:2645–2652. 2018. View Article : Google Scholar : PubMed/NCBI
27	Hori S, Nomura T and Sakaguchi S: Control of regulatory T cell development by the transcription factor Foxp3. Science. 299:1057–1061. 2003. View Article : Google Scholar : PubMed/NCBI
28	Fontenot JD, Gavin MA and Rudensky AY: Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol. 4:330–336. 2003. View Article : Google Scholar : PubMed/NCBI
29	Khattri R, Cox T, Yasayko SA and Ramsdell F: An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat. Immunol. 4:337–342. 2003.
30	Maloy KJ and Powrie F: Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature. 474:298–306. 2011. View Article : Google Scholar : PubMed/NCBI
31	Sydora BC, MacFarlane SM, Lupicki M, Dmytrash AL, Dieleman LA and Fedorak RN: An imbalance in mucosal cytokine profile causes transient intestinal inflammation following an animal's first exposure to faecal bacteria and antigens. Clin Exp Immunol. 161:187–196. 2010. View Article : Google Scholar : PubMed/NCBI
32	Franke A, Balschun T, Karlsen TH, Sventoraityte J, Nikolaus S, Mayr G, Domingues FS, Albrecht M, Nothnagel M, Ellinghaus D, et al: Sequence variants in IL10, ARPC2 and multiple other loci contribute to ulcerative colitis susceptibility. Nat Genet. 40:1319–1323. 2008. View Article : Google Scholar : PubMed/NCBI
33	Coelho T, Andreoletti G, Ashton JJ, Pengelly RJ, Gao Y, RamaKrishnan A, Batra A, Beattie RM, Williams AP and Ennis S: Immuno-genomic profiling of patients with inflammatory bowel disease: A systematic review of genetic and functional in vivo studies of implicated genes. Inflamm Bowel Dis. 20:1813–1819. 2014. View Article : Google Scholar : PubMed/NCBI
34	Santana G, Bendicho MT, Santana TC, Reis LB, Lemaire D and Lyra AC: The TNF-α-308 polymorphism may affect the severity of Crohn's disease. Clinics (Sao Paulo). 66:1373–1378. 2011. View Article : Google Scholar : PubMed/NCBI
35	Hedges SR, Sibley DA, Mayo MS, Hook EW III and Russell MW: Cytokine and antibody responses in women infected with Neisseria gonorrhoeae: Effects of concomitant infections. J Infect Dis. 178:742–751. 1998. View Article : Google Scholar : PubMed/NCBI
36	Honda K and Littman DR: The microbiome in infectious disease and inflammation. Annu Rev Immunol. 30:759–795. 2012. View Article : Google Scholar : PubMed/NCBI
37	Maynard CL, Harrington LE, Janowski KM, Oliver JR, Zindl CL, Rudensky AY and Weaver CT: Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3- precursor cells in the absence of interleukin 10. Nat Immunol. 8:931–941. 2007. View Article : Google Scholar : PubMed/NCBI
38	Rubtsov YP, Rasmussen JP, Chi EY, Fontenot J, Castelli L, Ye X, Treuting P, Siewe L, Roers A, Henderson WR Jr, et al: Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity. 28:546–558. 2008. View Article : Google Scholar : PubMed/NCBI
39	Okayasu I, Hatakeyama S, Yamada M, Ohkusa T, Inagaki Y and Nakaya R: A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology. 98:694–702. 1990. View Article : Google Scholar : PubMed/NCBI
40	Alex P, Zachos NC, Nguyen T, Gonzales L, Chen TE, Conklin LS, Centola M and Li X: Distinct cytokine patterns identified from multiplex profiles of murine DSS and TNBS-induced colitis. Inflammatory Bowel Dis. 15:341–352. 2009. View Article : Google Scholar
41	Hsieh MC, Tsai WH, Jheng YP, Su SL, Wang SY, Lin CC, Chen YH and Chang WW: The beneficial effects of Lactobacillus reuteri ADR-1 or ADR-3 consumption on type 2 diabetes mellitus: A randomized, double-blinded, placebo-controlled trial. Sci Rep. 8:167912018. View Article : Google Scholar : PubMed/NCBI