Assessing the beneficial effect of Lactobacillus plantarum MS1 and Lactobacillus delbrueckii YN1 on colitis in a rat model
-
Manizheh Hajizadeh Varzeghan
,
Gholamreza Zarrini
,
Farzam Sheikhzadeh Hesari
,
Mohammad Hossein Modarressi
Abstract
Background and Objectives: Probiotics are effective in improving inflammatory bowel disease (IBD). This study assessed the effect of mesalazine and two candidate probiotics on the improvement of acetic acid (AA)-induced colitis model.
Materials and Methods: Lactobacillus plantarum MS1and Lactobacillus delbrueckii YN1 were used for IBD model in rat. Twenty-five male Wistar rats weighing 250 ± 50 grams were used in 5 classified groups: Control (CO); Colitis (CL); Colitis, Probiotic (CLP); Colitis, Mesalazine (CLM); Colitis, Probiotic, Mesalazine (CLPM) and the treatment period was 3 weeks. The rats were treated with mesalazine 30 mg/kg and probiotic 109 CFU/ml after induction of colitis. Histopathological and immunological analyses were performed to evaluate the effects of probiotic bacteria on IBD.
Results: The results showed that the probiotic bacteria reduced inflammation (P<0.05), extent (P<0.01), crypt abscesses (P<0.01), edema (P<0.05), inflammatory cell infiltration (P<0.5), and increased mucosa (P<0.001) in rats. Mesalazine administration in animals with colitis did not have a significant effect. Administration of probiotics in both CLP and CLPM groups reduced extent, crypt abscesses, edema, and inflammatory cell infiltration and showed an important role in the down-regulation of consolidation of pro-inflammatory factors (TNFα, IL-6, and IL-17), as well as up-regulation of anti-inflammatory factors such as IL-10.
Conclusion: Lactobacillus plantarum MS1 and Lactobacillus delbrueckii YN1 have shown significant potential in alleviating AA-induced colitis symptoms. Their administration leads to a marked reduction in pro-inflammatory cytokines such as TNF-α, IL-17, and IL-6, while enhancing IL-10 levels, indicating their promise as therapeutic candidates for inflammatory bowel disease (IBD).
1. Hamedi ZS, Manafi A, Hashemi SS, Mehrabani D, Seddighi A, Tanideh N, Mokhtari M. Healing effect of Hypericum perforatum in Burn Injuries. World J Plast Surg 2024;13:57-65.
2. Kucharzik T, Koletzko S, Kannengießer K, Dignaß A. Ulcerative colitis-diagnostic and therapeutic algorithms. Dtsch Arztebl Int 2020; 117: 564-574.
3. Xu Q, Hu M, Li M, Hou J, Zhang X, Gao Y, etal. Dietary bioactive peptide alanyl-glutamine attenuates dextran sodium sulfate-induced colitis by modulating gut microbiota. Oxid Med Cell Longev 2021; 2021: 5543003.
4. Dibekoğlu C, Erbaş O. Histone deacetylase inhibitor givinostat has ameliorative effect in the colitis model. Acta Cir Bras 2022; 37(5): e370503.
5. Alshehri D, Saadah O, Mosli M, Edris S, Alhindi R, Bahieldin A. Dysbiosis of gut microbiota in inflammatory bowel disease: Current therapies and potential for microbiota-modulating therapeutic approaches. Bosn J Basic Med Sci 2021; 21: 270-283.
6. Chen X, Zhao X, Wang H, Yang Z, Li J, Suo H. Prevent effects of Lactobacillus fermentum HY01 on dextran sulfate sodium-induced colitis in mice. Nutrients 2017; 9: 545.
7. Ravikoff Allegretti J, Courtwright A, Lucci M, Korzenik JR, Levine J. Marijuana use patterns among patients with inflammatory bowel disease. Inflamm Bowel Dis 2013; 19: 2809-2814.
8. Schicho R, Storr M. IBD: Patients with IBD find symptom relief in the Cannabis field. Nat Rev Gastroenterol Hepatol 2014; 11: 142-143.
9. Geier MS, Butler RN, Giffard PM, Howarth GS. Lactobacillus fermentum BR11, a potential new probiotic, alleviates symptoms of colitis induced by dextran sulfate sodium (DSS) in rats. Int J Food Microbiol 2007; 114: 267-274.
10. Peran L, Sierra S, Comalada M, Lara-Villoslada F, Bailón E, Nieto A, et al. 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 2007; 97: 96-103.
11. Zhou B, Yuan Y, Zhang S, Guo C, Li X, Li G, et al. Intestinal flora and disease mutually shape the regional immune system in the intestinal tract. Front Immunol 2020; 11: 575.
12. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010; 464: 59-65.
13. Metzger RN, Krug AN, Eisenächer K. Enteric virome sensing-Its role in intestinal homeostasis and immunity. Viruses 2018; 10: 146.
14. Liu YW, Su YW, Ong WK, Cheng TH, 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 2011; 11: 2159-2166.
15. Xu Y, Xie Q, Zhang W, Zhu M, Chen X, Guo D, et al. Lactobacillus plantarum GMNL-662 and Lactobacillus plantarum 299v prevent osteoporosis in mice with colitis by down-regulating Akkermansia in the gut microbiome. J Funct Foods 2022; 99: 105328.
16. Hajizadeh Varzeghan M, Zarrini G, Hesari FS, Hossein M. Screening of lactic acid bacteria as suitable human probiotics isolated from Azerbaijan dairy products. New Cell Mol Biotechnol J 2023; 13: 31-49.
17. Manna MJ, Abu-Raghif A, Al-Saree OJAH. The value of doxycycline in acetic acide induce ulcerative colitis in rats. Int J Pharm Sci Res 2018; 9: 3567-3572.
18. Ali AA, Abd Al Haleem EN, Khaleel SA, Sallam AS. Protective effect of cardamonin against acetic acid-induced ulcerative colitis in rats. Pharmacol Rep 2017; 69: 268-275.
19. Rodiño-Janeiro BK, Martínez C, Fortea M, Lobo B, Pigrau M, Nieto A, et al. Decreased TESK1-mediated cofilin 1 phosphorylation in the jejunum of IBS-D patients may explain increased female predisposition to epithelial dysfunction. Sci Rep 2018; 8: 2255.
20. Hennebert O, Pelissier MA, Le Mee S, Wülfert E, Morfin R. Anti-inflammatory effects and changes in prostaglandin patterns induced by 7β-hydroxy-epiandrosterone in rats with colitis. J Steroid Biochem Mol Biol 2008; 110: 255-2562.
21. Calderón-Gómez E, Bassolas-Molina H, Mora-Buch R, Dotti I, Planell N, Esteller M, et al. Commensal-specific CD4+ cells from patients with Crohn’s disease have a T-helper 17 inflammatory profile. Gastroenterology 2016; 151: 489-500.e3.
22. Randhawa PK, Singh K, Singh N, Jaggi AS. A review on chemical-induced inflammatory bowel disease models in rodents. Korean J Physiol Pharmacol 2014; 18: 279-288.
23. Dicksved J, Schreiber O, Willing B, Petersson J, Rang S, Phillipson M, et al. Lactobacillus reuteri maintains a functional mucosal barrier during DSS treatment despite mucus layer dysfunction. PLoS One 2012; 7(9): e46399.
24. Hu R, Lin H, Li J, Zhao Y, Wang M, Sun X, et al. Probiotic Escherichia coli Nissle 1917- derived outer membrane vesicles enhance immunomodulation and antimicrobial activity in RAW264. 7 macrophages. BMC Microbiol 2020; 20: 268.
25. Guandalini S, Sansotta N. Probiotics in the treatment of inflammatory bowel disease. Adv Exp Med Biol 2019;1125:101-107.
26. Ashraf R, Shah NP. Immune system stimulation by probiotic microorganisms. Crit Rev Food Sci Nutr 2014; 54: 938-956.
27. Zhu C, Song K, Shen Z, Quan Y, Tan B, Luo W, et al. Roseburia intestinalis inhibits interleukin‑17 excretion and promotes regulatory T cells differentiation in colitis. Mol Med Rep 2018; 17: 7567-7574.
28. Su L, Ma F, An Z, Ji X, Zhang P, Yue Q, et al. The Metabolites of Lactobacillus fermentum F-B9-1 Relieved Dextran Sulfate Sodium-Induced Experimental Ulcerative Colitis in Mice. Front Microbiol 2022; 13: 865925.
29. Komatsu M, Kobayashi D, Saito K, Furuya D, Yagihashi A, Araake H, et al. Tumor necrosis factor-α in serum of patients with inflammatory bowel disease as measured by a highly sensitive immuno-PCR. Clin Chem 2001; 47: 1297-1301.
30. Kryczek I, Wang L, Wu K, Li W, Zhao E, Cui T, et al. Inflammatory regulatory T cells in the microenvironments of ulcerative colitis and colon carcinoma. Oncoimmunology 2016; 5(8): e1105430.
31. Li Y, Zhang T, Guo C, Geng M, Gai S, Qi W, et al. Bacillus subtilis RZ001 improves intestinal integrity and alleviates colitis by inhibiting the Notch signalling pathway and activating ATOH-1. Pathog Dis 2020; 78: ftaa016.
32. Federico A, Tuccillo C, Grossi E, Abbiati R, Garbagna N, Romano M, et al. The effect of a new symbiotic formulation on plasma levels and peripheral blood mononuclear cell expression of some pro-inflammatory cytokines in patients with ulcerative colitis: a pilot study. Eur Rev Med Pharmacol Sci 2009; 13: 285-293.
33. Noviello D, Mager R, Roda G, Borroni RG, Fiorino G, Vetrano S. The IL23-IL17 immune axis in the treatment of ulcerative colitis: successes, defeats, and ongoing challenges. Front Immunol 2021; 12: 611256.
2. Kucharzik T, Koletzko S, Kannengießer K, Dignaß A. Ulcerative colitis-diagnostic and therapeutic algorithms. Dtsch Arztebl Int 2020; 117: 564-574.
3. Xu Q, Hu M, Li M, Hou J, Zhang X, Gao Y, etal. Dietary bioactive peptide alanyl-glutamine attenuates dextran sodium sulfate-induced colitis by modulating gut microbiota. Oxid Med Cell Longev 2021; 2021: 5543003.
4. Dibekoğlu C, Erbaş O. Histone deacetylase inhibitor givinostat has ameliorative effect in the colitis model. Acta Cir Bras 2022; 37(5): e370503.
5. Alshehri D, Saadah O, Mosli M, Edris S, Alhindi R, Bahieldin A. Dysbiosis of gut microbiota in inflammatory bowel disease: Current therapies and potential for microbiota-modulating therapeutic approaches. Bosn J Basic Med Sci 2021; 21: 270-283.
6. Chen X, Zhao X, Wang H, Yang Z, Li J, Suo H. Prevent effects of Lactobacillus fermentum HY01 on dextran sulfate sodium-induced colitis in mice. Nutrients 2017; 9: 545.
7. Ravikoff Allegretti J, Courtwright A, Lucci M, Korzenik JR, Levine J. Marijuana use patterns among patients with inflammatory bowel disease. Inflamm Bowel Dis 2013; 19: 2809-2814.
8. Schicho R, Storr M. IBD: Patients with IBD find symptom relief in the Cannabis field. Nat Rev Gastroenterol Hepatol 2014; 11: 142-143.
9. Geier MS, Butler RN, Giffard PM, Howarth GS. Lactobacillus fermentum BR11, a potential new probiotic, alleviates symptoms of colitis induced by dextran sulfate sodium (DSS) in rats. Int J Food Microbiol 2007; 114: 267-274.
10. Peran L, Sierra S, Comalada M, Lara-Villoslada F, Bailón E, Nieto A, et al. 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 2007; 97: 96-103.
11. Zhou B, Yuan Y, Zhang S, Guo C, Li X, Li G, et al. Intestinal flora and disease mutually shape the regional immune system in the intestinal tract. Front Immunol 2020; 11: 575.
12. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010; 464: 59-65.
13. Metzger RN, Krug AN, Eisenächer K. Enteric virome sensing-Its role in intestinal homeostasis and immunity. Viruses 2018; 10: 146.
14. Liu YW, Su YW, Ong WK, Cheng TH, 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 2011; 11: 2159-2166.
15. Xu Y, Xie Q, Zhang W, Zhu M, Chen X, Guo D, et al. Lactobacillus plantarum GMNL-662 and Lactobacillus plantarum 299v prevent osteoporosis in mice with colitis by down-regulating Akkermansia in the gut microbiome. J Funct Foods 2022; 99: 105328.
16. Hajizadeh Varzeghan M, Zarrini G, Hesari FS, Hossein M. Screening of lactic acid bacteria as suitable human probiotics isolated from Azerbaijan dairy products. New Cell Mol Biotechnol J 2023; 13: 31-49.
17. Manna MJ, Abu-Raghif A, Al-Saree OJAH. The value of doxycycline in acetic acide induce ulcerative colitis in rats. Int J Pharm Sci Res 2018; 9: 3567-3572.
18. Ali AA, Abd Al Haleem EN, Khaleel SA, Sallam AS. Protective effect of cardamonin against acetic acid-induced ulcerative colitis in rats. Pharmacol Rep 2017; 69: 268-275.
19. Rodiño-Janeiro BK, Martínez C, Fortea M, Lobo B, Pigrau M, Nieto A, et al. Decreased TESK1-mediated cofilin 1 phosphorylation in the jejunum of IBS-D patients may explain increased female predisposition to epithelial dysfunction. Sci Rep 2018; 8: 2255.
20. Hennebert O, Pelissier MA, Le Mee S, Wülfert E, Morfin R. Anti-inflammatory effects and changes in prostaglandin patterns induced by 7β-hydroxy-epiandrosterone in rats with colitis. J Steroid Biochem Mol Biol 2008; 110: 255-2562.
21. Calderón-Gómez E, Bassolas-Molina H, Mora-Buch R, Dotti I, Planell N, Esteller M, et al. Commensal-specific CD4+ cells from patients with Crohn’s disease have a T-helper 17 inflammatory profile. Gastroenterology 2016; 151: 489-500.e3.
22. Randhawa PK, Singh K, Singh N, Jaggi AS. A review on chemical-induced inflammatory bowel disease models in rodents. Korean J Physiol Pharmacol 2014; 18: 279-288.
23. Dicksved J, Schreiber O, Willing B, Petersson J, Rang S, Phillipson M, et al. Lactobacillus reuteri maintains a functional mucosal barrier during DSS treatment despite mucus layer dysfunction. PLoS One 2012; 7(9): e46399.
24. Hu R, Lin H, Li J, Zhao Y, Wang M, Sun X, et al. Probiotic Escherichia coli Nissle 1917- derived outer membrane vesicles enhance immunomodulation and antimicrobial activity in RAW264. 7 macrophages. BMC Microbiol 2020; 20: 268.
25. Guandalini S, Sansotta N. Probiotics in the treatment of inflammatory bowel disease. Adv Exp Med Biol 2019;1125:101-107.
26. Ashraf R, Shah NP. Immune system stimulation by probiotic microorganisms. Crit Rev Food Sci Nutr 2014; 54: 938-956.
27. Zhu C, Song K, Shen Z, Quan Y, Tan B, Luo W, et al. Roseburia intestinalis inhibits interleukin‑17 excretion and promotes regulatory T cells differentiation in colitis. Mol Med Rep 2018; 17: 7567-7574.
28. Su L, Ma F, An Z, Ji X, Zhang P, Yue Q, et al. The Metabolites of Lactobacillus fermentum F-B9-1 Relieved Dextran Sulfate Sodium-Induced Experimental Ulcerative Colitis in Mice. Front Microbiol 2022; 13: 865925.
29. Komatsu M, Kobayashi D, Saito K, Furuya D, Yagihashi A, Araake H, et al. Tumor necrosis factor-α in serum of patients with inflammatory bowel disease as measured by a highly sensitive immuno-PCR. Clin Chem 2001; 47: 1297-1301.
30. Kryczek I, Wang L, Wu K, Li W, Zhao E, Cui T, et al. Inflammatory regulatory T cells in the microenvironments of ulcerative colitis and colon carcinoma. Oncoimmunology 2016; 5(8): e1105430.
31. Li Y, Zhang T, Guo C, Geng M, Gai S, Qi W, et al. Bacillus subtilis RZ001 improves intestinal integrity and alleviates colitis by inhibiting the Notch signalling pathway and activating ATOH-1. Pathog Dis 2020; 78: ftaa016.
32. Federico A, Tuccillo C, Grossi E, Abbiati R, Garbagna N, Romano M, et al. The effect of a new symbiotic formulation on plasma levels and peripheral blood mononuclear cell expression of some pro-inflammatory cytokines in patients with ulcerative colitis: a pilot study. Eur Rev Med Pharmacol Sci 2009; 13: 285-293.
33. Noviello D, Mager R, Roda G, Borroni RG, Fiorino G, Vetrano S. The IL23-IL17 immune axis in the treatment of ulcerative colitis: successes, defeats, and ongoing challenges. Front Immunol 2021; 12: 611256.
| Files | ||
| Issue | Vol 17 No 5 (2025) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v17i5.19889 | |
| Keywords | ||
| Inflammatory bowel disease Probiotics Inflammatory cytokines Lactic acid bacteria | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Hajizadeh Varzeghan M, Zarrini G, Sheikhzadeh Hesari F, Modarressi MH. Assessing the beneficial effect of Lactobacillus plantarum MS1 and Lactobacillus delbrueckii YN1 on colitis in a rat model. Iran J Microbiol. 2025;17(5):804-813.
