Abstract
Gut microbiota has become a new therapeutic target in the treatment of inflammatory Bowel Disease (IBD). Probiotics are known for their beneficial effects and have shown good efficacy in the clinical treatment of IBD and animal models of colitis. However, how these probiotics contribute to the amelioration of IBD is largely unknown. In the current study, the DSS-induced mouse colitis model was treated with oral administration of Lactobacillus plantarum strains to investigate their effects on colitis. The results indicated that the L. plantarum strains improved dysbiosis and enhanced the abundance of beneficial bacteria related to short-chain fatty acids (SCFAs) production. Moreover, L. plantarum strains decreased the level of pro-inflammatory cytokines, i.e., IL-17A, IL-17F, IL-6, IL-22, and TNF-α and increased the level of anti-inflammatory cytokines, i.e., TGF-β, IL-10. Our result suggests that L. plantarum strains possess probiotic effects and can ameliorate DSS colitis in mice by modulating the resident gut microbiota and immune response.
Graphical abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request. Requests to access the datasets should be directed to CZ, email: chjzh@lzu.edu.cn School of Life Sciences, Lanzhou University, Lanzhou China.
Code availability
Not applicable.
Abbreviations
- CD:
-
Crohn’s disease
- DSS:
-
Dextran sulfate sodium
- ELISA:
-
Enzyme-linked immune-sorbent assay
- FMT:
-
Fecal microbiota transplantation
- IBD:
-
Inflammatory bowel disease
- IL-6/10/22/17A/17F:
-
Interleukin-6/10/22/17A/17F
- LAB:
-
Lactic acid bacteria
- PBS:
-
Phosphate-buffered saline
- SCFA:
-
Short-chain fatty acids
- TGF-β:
-
Transforming growth factor-β
- Th:
-
Helper T cell
- TNF-α:
-
Tumor necrosis factor-α
- Treg:
-
Regulatory T cell
- UC:
-
Ulcerative colitis
References
Arpaia N, Campbell C, Fan X, Dikiy S, Van Der Veeken J, Deroos P, Liu H, Cross JR, Pfeffer K, Coffer PJ, Rudensky AY (2013) Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504(7480):451–455. https://doi.org/10.1038/nature12726
Atarashi K, Umesaki Y, Honda K (2011) Microbiotal influence on T cell subset development. In Seminars in Immunology 23(2):146–153. https://doi.org/10.1016/j.smim.2011.01.010
Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, Fukuda S, Saito T, Narushima S, Hase K, Kim S, Fritz JV, Wilmes P, Ueha S, Matsushima K, Ohno H, Olle B, Sakaguchi S, Taniguchi T, … Honda K (2013) Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature, 500(7461), 232–236. https://doi.org/10.1038/nature12331
Bai AP, Ouyang Q, Xiao XR, Li SF (2006) Probiotics modulate inflammatory cytokine secretion from inflamed mucosa in active ulcerative colitis. Int J Clin Pract 60(3):284–288. https://doi.org/10.1111/j.1368-5031.2006.00833.x
Banks C, Bateman A, Payne R, Johnson P, Sheron N (2003) Chemokine expression in IBD. Mucosal chemokine expression is unselectively increased in both ulcerative colitis and Crohn’s disease. Journal of Pathology 199(1):28–35. https://doi.org/10.1002/path.1245
Bao Y, Zhang Y, Li H, Liu Y, Wang S, Dong X, Su F, Yao G, Sun T, Zhang H (2012) In vitro screen of Lactobacillus plantarum as probiotic bacteria and their fermented characteristics in soymilk. Annals of Microbiology 62(3):1311–1320. https://doi.org/10.1007/s13213-011-0377-4
Basset C, Holton J, Bazeos A, Vaira D, Bloom S (2004) Are Helicobacter species and enterotoxigenic Bacteroides fragilis involved in inflammatory bowel disease? Dig Dis Sci 49(9):1425–1432. https://doi.org/10.1023/B:DDAS.0000042241.13489.88
Bergman EN (1990) Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. In Physiological Reviews. 70(2):567–590. https://doi.org/10.1152/physrev.1990.70.2.567
Bouskra D, Brézillon C, Bérard M, Werts C, Varona R, Boneca IG, Eberl G (2008) Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 456(7221):507–510. https://doi.org/10.1038/nature07450
Boyle RJ, Robins-Browne RM, Tang MLK (2006) Probiotic use in clinical practice: What are the risks? In American Journal of Clinical Nutrition. 83(6):1256–1264. https://doi.org/10.1093/ajcn/83.6.1256
Buttó LF, Haller D (2016) Dysbiosis in intestinal inflammation: Cause or consequence. In the International Journal of Medical Microbiology. 306(5):302–309. https://doi.org/10.1016/j.ijmm.2016.02.010
Canani RB, Costanzo MD, Leone L, Pedata M, Meli R, Calignano A (2011) Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J Gastroenterol 17(12):1519–1528. https://doi.org/10.3748/wjg.v17.i12.1519
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pẽa AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, … Knight R (2010). QIIME allows analysis of high-throughput community sequencing data. In Nature Methods. 7(5): 335–336. https://doi.org/10.1038/nmeth.f.303
Celiberto LS, Bedani R, Rossi EA, Cavallini DCU (2017) Probiotics: The scientific evidence in the context of inflammatory bowel disease. Crit Rev Food Sci Nutr 57(9):1759–1768. https://doi.org/10.1080/10408398.2014.941457
Chassaing B, Aitken JD, Malleshappa M, Vijay-Kumar M (2014) Dextran sulfate sodium (DSS)-induced colitis in mice. Current Protocols in Immunology, SUPPL.104. https://doi.org/10.1002/0471142735.im1525s104
D’Incà R, Barollo M, Scarpa M, Grillo AR, Brun P, Vettorato MG, Castagliuolo I, Sturniolo GC (2011) Rectal administration of Lactobacillus casei DG modifies flora composition and toll-like receptor expression in colonic mucosa of patients with mild ulcerative colitis. Dig Dis Sci 56(4):1178–1187. https://doi.org/10.1007/s10620-010-1384-1
De LeBlanc AMD, LeBlanc JG (2014) Effect of probiotic administration on the intestinal microbiota, current knowledge and potential applications. World Journal of Gastroenterology 20(44):16518–16528. https://doi.org/10.3748/wjg.v20.i44.16518
de Moreno de LeBlanc A, del Carmen S, Zurita-Turk M, Santos Rocha C, van de Guchte M, Azevedo V, Miyoshi A, LeBlanc JG (2011) Importance of IL-10 Modulation by Probiotic Microorganisms in Gastrointestinal Inflammatory Diseases. ISRN Gastroenterology 2011:1–11. https://doi.org/10.5402/2011/892971
del Carmen S, de Moreno de LeBlanc A, LeBlanc JG (2016) Development of a potential probiotic yogurt using selected anti-inflammatory lactic acid bacteria for prevention of colitis and carcinogenesis in mice. Journal of Applied Microbiology 121(3):821–830. https://doi.org/10.1111/jam.13213
Deplancke B, Finster K, Graham WV, Collier CT, Thurmond JE, Gaskins HR (2003) Gastrointestinal and microbial responses to sulfate-supplemented drinking water in mice. Exp Biol Med 228(4):424–433. https://doi.org/10.1177/153537020322800413
Ding WQ, Lin GJ, Xu SR, Qian LP (2001) Changes of interleukin level in ulcerative colitis patients. Fudan University Journal of Medical Sciences 28(4):330–333
Dohi T, Fujihashi K, Rennert PD, Iwatani K, Kiyono H, McGhee JR (1999) Hapten-induced colitis is associated with colonic patch hypertrophy and T helper cell 2-type responses. J Exp Med 189(8):1169–1179. https://doi.org/10.1084/jem.189.8.1169
Dupont AW, Dupont HL (2011) The intestinal microbiota and chronic disorders of the gut. In Nature Reviews Gastroenterology and Hepatology. 8(9):523–531. https://doi.org/10.1038/nrgastro.2011.133
Fava F, Danese S (2011) Intestinal microbiota in inflammatory bowel disease: Friend of foe? World J Gastroenterol 17(5):557–566. https://doi.org/10.3748/wjg.v17.i5.557
Fernandez EM, Valenti V, Rockel C, Hermann C, Pot B, Boneca IG, Grangette C (2011) Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide. Gut 60(8):1050–1059. https://doi.org/10.1136/gut.2010.232918
Fontana L, Bermudez-Brito M, Plaza-Diaz J, Muñoz-Quezada S, Gil A (2013) Sources, isolation, characterisation and evaluation of probiotics. British Journal of Nutrition, 109(SUPPL. 2). https://doi.org/10.1017/S0007114512004011
Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR (2007) Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proceedings of the National Academy of Sciences of the United States of America 104(34):13780–13785. https://doi.org/10.1073/pnas.0706625104
Frank DN, Robertson CE, Hamm CM, Kpadeh Z, Zhang T, Chen H, Zhu W, Sartor RB, Boedeker EC, Harpaz N, Pace NR, Li E (2011) Disease phenotype and genotype are associated with shifts in intestinal-associated microbiota in inflammatory bowel diseases. Inflamm Bowel Dis 17(1):179–184. https://doi.org/10.1002/ibd.21339
Frazier TH, DiBaise JK, McClain CJ (2011) Gut microbiota, intestinal permeability, obesity-induced inflammation, and liver injury. Journal of Parenteral and Enteral Nutrition, 35(5 SUPPL.). https://doi.org/10.1177/0148607111413772
Friedman G, George J (2000) Treatment of refractory “Pouchitis” with prebiotic and probiotic therapy. Gastroenterology 118(4):A778. https://doi.org/10.1016/s0016-5085(00)85255-5
Fuentes S, Rossen NG, Van Der Spek MJ, Hartman JHA, Huuskonen L, Korpela K, Salojärvi J, Aalvink S, De Vos WM, D’Haens GR, Zoetendal EG, Ponsioen CY (2017) Microbial shifts and signatures of long-term remission in ulcerative colitis after fecal microbiota transplantation. ISME J 11(8):1877–1889. https://doi.org/10.1038/ismej.2017.44
Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T, Takahashi M, Fukuda NN, Murakami S, Miyauchi E, Hino S, Atarashi K, Onawa S, Fujimura Y, Lockett T, … Ohno H (2013). Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature, 504(7480), 446–450. https://doi.org/10.1038/nature12721
Gaboriau-Routhiau V, Rakotobe S, Lécuyer E, Mulder I, Lan A, Bridonneau C, Rochet V, Pisi A, De Paepe M, Brandi G, Eberl G, Snel J, Kelly D, Cerf-Bensussan N (2009) The Key Role of Segmented Filamentous Bacteria in the Coordinated Maturation of Gut Helper T Cell Responses. Immunity 31(4):677–689. https://doi.org/10.1016/j.immuni.2009.08.020
Garrett WS, Gordon JI, Glimcher LH (2010) Homeostasis and Inflammation in the Intestine. In Cell 140(6):859–870. https://doi.org/10.1016/j.cell.2010.01.023
Ghoshal UC, Gwee KA, Holtmann G, Li Y, Park SJ, Simadibrata M, Sugano K, Wu K, Quigley EMM, Cohen H (2018) The role of the microbiome and the use of probiotics in gastrointestinal disorders in adults in the Asia-Pacific region - background and recommendations of a regional consensus meeting. Journal of Gastroenterology and Hepatology (australia) 33(1):57–69. https://doi.org/10.1111/jgh.13840
Gill N, Wlodarska M, Finlay BB (2010) The future of mucosal immunology: Studying an integrated system-wide organ. In Nature Immunology 11(7):558–560. https://doi.org/10.1038/ni0710-558
Håkansson A, Tormo-Badia N, Baridi A, Xu J, Molin G, Hagslätt ML, Karlsson C, Jeppsson B, Cilio CM, Ahrné S (2014) Immunological alteration and changes of gut microbiota after dextran sulfate sodium (DSS) administration in mice. Clinical and Experimental Medicine 15(1):107–120. https://doi.org/10.1007/s10238-013-0270-5
Halfvarson J, Brislawn CJ, Lamendella R, Vázquez-Baeza Y, Walters WA, Bramer LM, D’Amato M, Bonfiglio F, McDonald D, Gonzalez A, McClure EE, Dunklebarger MF, Knight R, Jansson JK (2017) Dynamics of the human gut microbiome in inflammatory bowel disease. Nature Microbiology, 2. https://doi.org/10.1038/nmicrobiol.2017.4
Hamer HM, Jonkers D, Venema K, Vanhoutvin S, Troost FJ, Brummer RJ (2008) Review article: The role of butyrate on colonic function. In Alimentary Pharmacology and Therapeutics 27(2):104–119. https://doi.org/10.1111/j.1365-2036.2007.03562.x
Hegazy SK, El-Bedewy MM (2010) Effect of probiotics on pro-inflammatory cytokines and NF-κb activation in ulcerative colitis. World J Gastroenterol 16(33):4145–4151. https://doi.org/10.3748/wjg.v16.i33.4145
Heimesaat MM, Fischer A, Siegmund B, Kupz A, Niebergall J, Fuchs D, Jahn HK, Freudenberg M, Loddenkemper C, Batra A, Lehr HA, Liesenfeld O, Blaut M, Göbel UB, Schumann RR, Bereswill S (2007) Shift towards pro-inflammatory intestinal bacteria aggravates acute murine colitis via toll-like receptors 2 and 4. PLoS ONE, 2(7). https://doi.org/10.1371/journal.pone.0000662
Hyung KE, Moon BS, Kim B, Park ES, Park SY, Hwang KW (2017) Lactobacillus plantarum isolated from kimchi suppresses food allergy by modulating cytokine production and mast cells activation. Journal of Functional Foods 29:60–68. https://doi.org/10.1016/j.jff.2016.12.016
Jing Y, Li A, Liu Z, Yang P, Wei J, Chen X, Zhao T, Bai Y, Zha L, Zhang C (2018) Absorption of Codonopsis pilosula Saponins by Coexisting Polysaccharides Alleviates Gut Microbial Dysbiosis with Dextran Sulfate Sodium-Induced Colitis in Model Mice. BioMed Research International, 2018. https://doi.org/10.1155/2018/1781036
Jo SG, Noh EJ, Lee JY, Kim G, Choi JH, Lee ME, Song JH, Chang JY, Park JH (2016) Lactobacillus curvatus WiKim38 isolated from kimchi induces IL-10 production in dendritic cells and alleviates DSS-induced colitis in mice. J Microbiol 54(7):503–509. https://doi.org/10.1007/s12275-016-6160-2
Koh A, De Vadder F, Kovatcheva-Datchary P, Bäckhed F (2016) From dietary fiber to host physiology: Short-chain fatty acids as key bacterial metabolites. In Cell 165(6):1332–1345. https://doi.org/10.1016/j.cell.2016.05.041
Kolho KL, Korpela K, Jaakkola T, Pichai MVA, Zoetendal EG, Salonen A, De Vos WM (2015) Fecal microbiota in pediatric inflammatory bowel disease and its relation to inflammation. Am J Gastroenterol 110(6):921–930. https://doi.org/10.1038/ajg.2015.149
Lahtinen P, Mattila E, Anttila VJ, Tillonen J, Teittinen M, Nevalainen P, Salminen S, Satokari R, Arkkila P (2017) Fecal microbiota transplantation in patients with Clostridium difficile and significant comorbidities as well as in patients with new indications: A case series. World J Gastroenterol 23(39):7174–7184. https://doi.org/10.3748/wjg.v23.i39.7174
Le B, Yang SH (2018) Efficacy of Lactobacillus plantarum in prevention of inflammatory bowel disease. In Toxicology Reports 5:314–317. https://doi.org/10.1016/j.toxrep.2018.02.007
Li C, Chen Y, Kwok LY, Chen X, Yu H, Yang H, Yang J, Xue J, Sun T, Zhang H (2015) Identification of potential probiotic Lactobacillus plantarum isolates with broad-spectrum antibacterial activity. Dairy Science and Technology 95(3):381–392. https://doi.org/10.1007/s13594-014-0206-1
Li C, Song J, Kwok L, Wang J, Dong Y, Yu H, Hou Q, Zhang H, Chen Y (2017) Influence of Lactobacillus plantarum on yogurt fermentation properties and subsequent changes during post fermentation storage. Journal of Dairy Science 100(4):2512–2525. https://doi.org/10.3168/jds.2016-11864
Liu CJ, Tang XD, Yu J, Zhang HY, Li XR (2017) Gut microbiota alterations from different Lactobacillus probiotic-fermented yogurt treatments in slow-transit constipation. Journal of Functional Foods 38:110–118. https://doi.org/10.1016/j.jff.2017.08.037
Luo A, Leach ST, Barres R, Hesson LB, Grimm MC, Simar D (2017) The microbiota and epigenetic regulation of t helper 17/regulatory T cells: In search of a balanced immune system. Frontiers in Immunology 8(APR):417. https://doi.org/10.3389/fimmu.2017.00417
Machiels K, Joossens M, Sabino J, De Preter V, Arijs I, Eeckhaut V, Ballet V, Claes K, Van Immerseel F, Verbeke K, Ferrante M, Verhaegen J, Rutgeerts P, Vermeire S (2014) A decrease in the butyrate-producing species roseburia hominis and faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut 63(8):1275–1283. https://doi.org/10.1136/gutjnl-2013-304833
Mahida YR, Wu K, Jewell DP (1989) Enhanced production of interleukin 1-β by mononuclear cells isolated from mucosa with active ulcerative colitis of Crohn’s disease. Gut 30(6):835–838. https://doi.org/10.1136/gut.30.6.835
Malin M, Suomalainen H, Saxelin M, Isolauri E (1996) Promotion of iga immune response in patients with crohn’s disease by oral bacteriotherapy with lactobacillus gg. Ann Nutr Metab 40(3):137–145. https://doi.org/10.1159/000177907
Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, Frangeul L, Nalin R, Jarrin C, Chardon P, Marteau P, Roca J, Dore J (2006) Reduced diversity of fecal microbiota in Crohn’s disease revealed by a metagenomic approach. Gut 55(2):205–211. https://doi.org/10.1136/gut.2005.073817
Manichanh, Chaysavanh, Borruel, N., Casellas, F., & Guarner, F. (2012). The gut microbiota in IBD. In Nature Reviews Gastroenterology and Hepatology (Vol. 9, Issue 10, pp. 599–608). https://doi.org/10.1038/nrgastro.2012.152
Mao S, Zhang R, Wang D, Zhu W (2012) The diversity of the fecal bacterial community and its relationship with the concentration of volatile fatty acids in the feces during subacute rumen acidosis in dairy cows. BMC Veterinary Research, 8. https://doi.org/10.1186/1746-6148-8-237
Marotz CA, Zarrinpar A (2016) Treating obesity and metabolic syndrome with fecal microbiota transplantation. In Yale Journal of Biology and Medicine 89(3):383–388
Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Di Yu, Schilter HC, Rolph MS, MacKay F, Artis D, Xavier RJ, Teixeira MM, MacKay CR (2009) Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 461(7268):1282–1286. https://doi.org/10.1038/nature08530
Matthies C, Evers S, Ludwig W, Schink B (2000) Anaerovorax odorimutans gen. nov., sp. nov., a putrescine-fermenting, strictly anaerobic bacterium. International Journal of Systematic and Evolutionary Microbiology 50(4):1591–1594. https://doi.org/10.1099/00207713-50-4-1591
Melgar S, Karlsson A, Michaëlsson E (2005). Acute colitis induced by dextran sulfate sodium progresses to chronicity in C57BL/6 but not in BALB/c mice: Correlation between symptoms and inflammation. American Journal of Physiology - Gastrointestinal and Liver Physiology, 288(6 51–6). https://doi.org/10.1152/ajpgi.00467.2004
Michail S, Durbin M, Turner D, Griffiths AM, Mack DR, Hyams J, Leleiko N, Kenche H, Stolfi A, Wine E (2012) Alterations in the gut microbiome of children with severe ulcerative colitis. Inflamm Bowel Dis 18(10):1799–1808. https://doi.org/10.1002/ibd.22860
Miele E, Pascarella F, Giannetti E, Quaglietta L, Baldassano RN, Staiano A (2009) Effect of a probiotic preparation (VSL#3) on induction and maintenance of remission in children with ulcerative colitis. Am J Gastroenterol 104(2):437–443. https://doi.org/10.1038/ajg.2008.118
Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, Reyes JA, Shah SA, LeLeiko N, Snapper SB, Bousvaros A, Korzenik J, Sands BE, Xavier RJ, Huttenhower C (2012). Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biology, 13(9). https://doi.org/10.1186/gb-2012-13-9-r79
Mulder DJ, Noble AJ, Justinich CJ, Duffin JM (2014) A tale of two diseases: The history of inflammatory bowel disease. In Journal of Crohn’s and Colitis 8(5):341–348. https://doi.org/10.1016/j.crohns.2013.09.009
Murthy SNS, Cooper HS, Shim H, Shah RS, Ibrahim SA, Sedergran DJ (1993) Treatment of dextran sulfate sodium-induced murine colitis by intracolonic cyclosporin. Dig Dis Sci 38(9):1722–1734. https://doi.org/10.1007/BF01303184
Nagalingam NA, Kao JY, Young VB (2011) Microbial ecology of the murine gut associated with the development of dextran sodium sulfate-induced colitis. Inflamm Bowel Dis 17(4):917–926. https://doi.org/10.1002/ibd.21462
Neurath MF (2014) Cytokines in inflammatory bowel disease. In Nature Reviews Immunology 14(5):329–342. https://doi.org/10.1038/nri3661
Ng SC, Shi HY, Hamidi N, Underwood FE, Tang W, Benchimol EI, Panaccione R, Ghosh S, Wu JCY, Chan FKL, Sung JJY, Kaplan GG (2017) Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. The Lancet 390(10114):2769–2778. https://doi.org/10.1016/S0140-6736(17)32448-0
Oliva S, Di Nardo G, Ferrari F, Mallardo S, Rossi P, Patrizi G, Cucchiara S, Stronati L (2012) Randomized clinical trial: The effectiveness of Lactobacillus reuteri ATCC 55730 rectal enema in children with active distal ulcerative colitis. Aliment Pharmacol Ther 35(3):327–334. https://doi.org/10.1111/j.1365-2036.2011.04939.x
Park JS, Joe I, Rhee PD, Jeong CS, Jeong G (2017) A lactic acid bacterium isolated from kimchi ameliorates intestinal inflammation in DSS-induced colitis. J Microbiol 55(4):304–310. https://doi.org/10.1007/s12275-017-6447-y
Peran L, Sierra S, Comalada M, Lara-Villoslada F, Bailón E, Nieto A, Concha Á, Olivares M, Zarzuela A, Xaus J, Gálvarez J (2007) A comparative study of the preventative effects exerted by two probiotics, Lactobacillus reuteri and Lactobacillus fermentum, in the trinitrobenzenesulfonic acid model of rat colitis. Br J Nutr 97(1):96–103. https://doi.org/10.1017/S0007114507257770
Qiu X, Zhang M, Yang X, Hong N, Yu C (2013) Faecalibacterium prausnitzii upregulates regulatory T cells and anti-inflammatory cytokines in treating TNBS-induced colitis. Journal of Crohn’s and Colitis, 7(11). https://doi.org/10.1016/j.crohns.2013.04.002
Reid G, Younes JA, Van Der Mei HC, Gloor GB, Knight R, Busscher HJ (2011) Microbiota restoration: Natural and supplemented recovery of human microbial communities. In Nature Reviews Microbiology 9(1):27–38. https://doi.org/10.1038/nrmicro2473
Rombeau JL, Kripke SA (1990) Metabolic and intestinal effects of short-chain fatty acids. J Parenter Enter Nutr 14(5 SUPPL.):181S-185S. https://doi.org/10.1177/014860719001400507
Round JL, Mazmanian SK (2010) Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci USA 107(27):12204–12209. https://doi.org/10.1073/pnas.0909122107
Saez-Lara MJ, Gomez-Llorente C, Plaza-Diaz J, Gil A (2015) The role of probiotic lactic acid bacteria and bifidobacteria in the prevention and treatment of inflammatory bowel disease and other related diseases: A systematic review of randomized human clinical trials. In BioMed Research International (Vol. 2015). https://doi.org/10.1155/2015/505878
Sakata T, Kojima T, Fujieda M, Takahashi M, Michibata T (2003) Influences of probiotic bacteria on organic acid production by pig caecal bacteria in vitro. Proceedings of the Nutrition Society 62(1):73–80. https://doi.org/10.1079/pns2002211
Santacruz A, Collado MC, García-Valdés L, Segura MT, Marítn-Lagos JA, Anjos T, Martí-Romero M, Lopez RM, Florido J, Campoy C, Sanz Y (2010) Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br J Nutr 104(1):83–92. https://doi.org/10.1017/S0007114510000176
Sartor RB (2008) Microbial Influences in Inflammatory Bowel Diseases. Gastroenterology 134(2):577–594. https://doi.org/10.1053/j.gastro.2007.11.059
Schenk M, Bouchon A, Seibold F, Mueller C (2007) TREM-1 - Expressing intestinal macrophages crucially amplify chronic inflammation in experimental colitis and inflammatory bowel diseases. J Clin Investig 117(10):3097–3106. https://doi.org/10.1172/JCI30602
Scheppach W (1994) Effects of short chain fatty acids on gut morphology and function. Gut, 35(1 SUPPL.). https://doi.org/10.1136/gut.35.1_Suppl.S35
Schloss PD, Handelsman J (2006) Toward a census of bacteria in soil. PLoS Comput Biol 2(7):0786–0793. https://doi.org/10.1371/journal.pcbi.0020092
Schneider SM, Girard-Pipau F, Filippi J, Hébuterne X, Moyse D, Hinojosa GC, Pompei A, Rampal P (2005) Effects of Saccharomyces boulardii on fecal short-chain fatty acids and microflora in patients on long-term total enteral nutrition. World J Gastroenterol 11(39):6165–6169. https://doi.org/10.3748/wjg.v11.i39.6165
Schultsz C, Van den Berg FM, Kate FWT, Tytgat GNJ, Dankert J (1999) The intestinal mucus layer from patients with inflammatory bowel disease harbors high numbers of bacteria compared with controls. Gastroenterology 117(5):1089–1097. https://doi.org/10.1016/S0016-5085(99)70393-8
Seksik P, Adresse C (2010) Microbiote intestinal et MICI ✰ Gut microbiota and IBD PATHOLOGIES LIÉES AU MICROBIOTE. Gastroenterol Clin Biol 34:44–51
Shanahan F (2000) Probiotics and inflammatory bowel disease: Is there a scientific rationale? Inflamm Bowel Dis 6(2):107–115. https://doi.org/10.1097/00054725-200005000-00007
Sheil B, Shanahan F, O’Mahony L (2007) Probiotic effects on inflammatory bowel disease. Journal of Nutrition, 137(3). https://doi.org/10.1093/jn/137.3.819s
Shen ZH, Zhu CX, Quan YS, Yang ZY, Wu S, Luo WW, Tan B, Wang XY (2018) Relationship between intestinal microbiota and ulcerative colitis: Mechanisms and clinical application of probiotics and fecal microbiota transplantation. In the World Journal of Gastroenterology 24(1):5–14. https://doi.org/10.3748/wjg.v24.i1.5
Sokol H, Seksik P, Rigottier-Gois L, Lay C, Lepage P, Podglajen I, Marteau P, Doré J (2006) Specificities of the fecal microbiota in inflammatory bowel disease. Inflamm Bowel Dis 12(2):106–111. https://doi.org/10.1097/01.MIB.0000200323.38139.c6
Stackebrandt E, Goebel BM (1994) Taxonomic note: A place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. In the International Journal of Systematic Bacteriology 44(4):846–849. https://doi.org/10.1099/00207713-44-4-846
Sun KY, Xu DH, Xie C, Plummer S, Tang J, Yang XF, Ji XH (2017a) Lactobacillus paracasei modulates LPS-induced inflammatory cytokine release by monocyte-macrophages via the up-regulation of negative regulators of NF-kappaB signaling in a TLR2-dependent manner. Cytokine 92:1–11. https://doi.org/10.1016/j.cyto.2017.01.003
Sun M, Wu W, Liu Z, Cong Y (2017b) Microbiota metabolite short chain fatty acids, GPCR, and inflammatory bowel diseases. In Journal of Gastroenterology,52(1). https://doi.org/10.1007/s00535-016-1242-9
Swidsinski A, Ladhoff A, Pernthaler A, Swidsinski S, LoeningBaucke V, Ortner M, Weber J, Hoffmann U, Schreiber S, Dietel M, Lochs H (2002) Mucosal flora in inflammatory bowel disease. Gastroenterology 122(1):44–54. https://doi.org/10.1053/gast.2002.30294
Swidsinski A, Dörffel Y, Loening-Baucke V, Theissig F, Rückert JC, Ismail M, Rau WA, Gaschler D, Weizenegger M, Kühn S, Schilling J, Dörffel WV (2011) Acute appendicitis is characterized by local invasion with Fusobacterium nucleatum/necrophorum. Gut 60(1):34–40. https://doi.org/10.1136/gut.2009.191320
Taghipour N, Molaei M, Mosaffa N, Rostami-Nejad M, Aghdaei HA, Anissian A, Azimzadeh P, Zali MR (2016) An experimental model of colitis induced by dextran sulfate sodium from acute progresses to chronicity in C57BL/6: Correlation between conditions of mice and the environment. Gastroenterology and Hepatology from Bed to Bench 9(1):45–52. https://doi.org/10.22037/ghfbb.v1i9.868
Takagi H, Kanai T, Okazawa A, Kishi Y, Sato T, Takaishi H, Inoue N, Ogata H, Iwao Y, Hoshino K, Takeda K, Akira S, Watanabe M, Ishii H, Hibi T (2003) Contrasting action of IL-12 and IL-18 in the development of dextran sodium sulfate colitis in mice. Scand J Gastroenterol 38(8):837–844. https://doi.org/10.1080/00365520310004047
Tan AH, Chong CW, Song SL, Teh CSJ, Yap IKS, Loke MF, Tan YQ, Yong H. Sen, Mahadeva S, Lang AE, Lim SY (2018) Altered gut microbiome and metabolome in patients with multiple system atrophy. In Movement Disorders 33(1):174–176. https://doi.org/10.1002/mds.27203
Therkelsen SP, Hetland G, Lyberg T, Lygren I, Johnson E (2016) Cytokine Levels After Consumption of a Medicinal Agaricus blazei Murill-Based Mushroom Extract, AndoSan™, in Patients with Crohn’s Disease and Ulcerative Colitis in a Randomized Single-Blinded Placebo-Controlled Study. Scand J Immunol 84(6):323–331. https://doi.org/10.1111/sji.12476
Vilela EG, da Gama Torres HO, Martin FP, de Lourdes de Abreu Ferrari M, Andrade MM, da Cunha AS (2012) Evaluation of inflammatory activity in Crohn’s disease and ulcerative colitis. World Journal of Gastroenterology 18(9):872–881. https://doi.org/10.3748/wjg.v18.i9.872
Wang Lv, Christophersen CT, Sorich MJ, Gerber JP, Angley MT, Conlon MA (2011) Low relative abundances of the mucolytic bacterium Akkermansia muciniphila and Bifidobacterium spp. in feces of children with autism. Applied and Environmental Microbiology 77(18):6718–6721. https://doi.org/10.1128/AEM.05212-11
Wang Z, Bao Y, Zhang Y, Zhang J, Yao G, Wang S, Zhang H (2013) Effect of Soymilk Fermented with Lactobacillus plantarum P-8 on Lipid Metabolism and Fecal Microbiota in Experimental Hyperlipidemic Rats. Food Biophys 8(1):43–49. https://doi.org/10.1007/s11483-012-9282-z
Wang L, Zhang J, Guo Z, Kwok L, Ma C, Zhang W, Lv Q, Huang W, Zhang H (2014) Effect of oral consumption of probiotic Lactobacillus planatarum P-8 on fecal microbiota, SIgA, SCFAs, and TBAs of adults of different ages. Nutrition 30(7–8):776-783.e1. https://doi.org/10.1016/j.nut.2013.11.018
Wasilewski A, Zielińska M, Storr M, Fichna J (2015) Beneficial effects of probiotics, prebiotics, synbiotics, and psychobiotics in inflammatory bowel disease. In Inflammatory Bowel Diseases 21(7):1674–1682. https://doi.org/10.1097/MIB.0000000000000364
Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z, Järnerot G, Tysk C, Jansson JK, Engstrand L (2010). A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology, 139(6). https://doi.org/10.1053/j.gastro.2010.08.049
WJ Y (2013) Characteristics of fecal flora in patients with Crohn ’s disease and intestinal tuberculosis and its differential diagnosis. Chinese Medicine Guide 1:529–530
Wlodarska M, Kostic AD, Xavier RJ (2015) An integrative view of microbiome-host interactions in inflammatory bowel diseases. In Cell Host and Microbe 17(5):577–591. https://doi.org/10.1016/j.chom.2015.04.008
Woywodt A, Ludwig D, Neustock P, Kruse A, Schwarting K, Jantschek G, Kirchner H, Stange EF (1999) Mucosal cytokine expression, cellular markers and adhesion molecules in inflammatory bowel disease. Eur J Gastroenterol Hepatol 11(3):267–276. https://doi.org/10.1097/00042737-199903000-00010
Xue L, He J, Gao N, Lu X, Li M, Wu X, Liu Z, Jin Y, Liu J, Xu J, Geng Y (2017) Probiotics may delay the progression of nonalcoholic fatty liver disease by restoring the gut microbiota structure and improving intestinal endotoxemia. Scientific Reports, 7. https://doi.org/10.1038/srep45176
Yang Y, Chen G, Yang Q, Ye J, Cai X, Tsering P, Cheng X, Hu C, Zhang S, Cao P (2017) Gut microbiota drive the attenuation of dextran sulfate sodium-induced colitis by Huangqin decoction. Oncotarget 8(30):48863–48874. https://doi.org/10.18632/oncotarget.16458
Zhang X, Zhao Y, Zhang M, Pang X, Xu J, Kang C, Li M, Zhang C, Zhang Z, Zhang Y, Li X, Ning G, Zhao L (2012) Structural changes of gut microbiota during berberine-mediated prevention of obesity and insulin resistance in high-fat diet-fed rats. PLoS ONE, 7(8). https://doi.org/10.1371/journal.pone.0042529
Zhang F, Li Y, Wang X, Wang S, Bi D (2019) The Impact of Lactobacillus plantarum on the Gut Microbiota of Mice with DSS-Induced Colitis. BioMed Research International, 2019. https://doi.org/10.1155/2019/3921315
Acknowledgements
We acknowledge the Jiangsu Science and Technology Major Project and Gansu Science and Technology Major Project for financial support. The authors also wish to express their gratitude to Pro. Dr. Heping Zhang (Inner Mongolia Agricultural University) for providing the L. plantarum strains.
Funding
This work was supported by the Jiangsu Science and Technology Major Project [BA2016036], and Gansu Science and Technology Major Project [17ZD2FA009].
Author information
Authors and Affiliations
Contributions
IK, JW and CZ designed the study; JW and IK performed the DSS experiment; TC and CL and NU collected and processed the samples for the next experiment; PY and XC tested the short-chain fatty acids; YB and LZ measured the cytokines; JW, IK, and YJ analyzed and interpreted the data; JW and IK wrote the manuscript; IK edit the manuscript and conducted the publishing process; TC gave the technical support and conceptual advice. CZ also guided and supervised us during the whole manuscript process. All authors have read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics Approval for Animal Use
This study protocol was approved by the Ethics Committee of Animal Experiments and the institutional review board of Lanzhou University.
Informed consent
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Research involving Human Participants
Not applicable.
Conflicts of Interest
The authors Israr Khan et al. declare that they have no conflict of interest/The authors have no conflicts of interest to declare that are relevant to the content of this article.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Khan, I., Wei, J., Li, A. et al. Lactobacillus plantarum strains attenuated DSS-induced colitis in mice by modulating the gut microbiota and immune response. Int Microbiol 25, 587–603 (2022). https://doi.org/10.1007/s10123-022-00243-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10123-022-00243-y