Elucidating the probiotic strategy with Pediococcus acidilactici BCB1H and Lactiplantibacillus plantarum HMX2 for restoring normal functions of gut and suppressing inflammation in a DSS-induced colitis animal model
Main Article Content
Keywords
DSS-induced colitis, dysbiosis, gut microbiota, L. plantarum HMX2, P. acidilactici BCB1H
Abstract
Background: Several inflammatory diseases, including colitis, are treated via probiotics but still the mechanism is not clear.
Objective: This study aimed to restore normal functioning of the gut and ameliorate inflammation in dextran sulfate sodium (DSS)-induced colitis mice via the probiotic intervention of Pediococcus acidilactici (P. acidilactici) BCB1H and Lactiplantibacillus plantarum (L. plantarum) HMX2.
Material and Methods: L. plantarum HMX2 and P. acidilactici BCB1H showed a remarkable reduction in the symptoms of DSS-induced colitis, including weight loss, shortening and damage of the colon, decreased tight junction protein, and pro-inflammatory cytokines in the blood of mice. Two treatment groups were administered with probiotic strains based on animal weight for a duration of 28 days; however, prior to this, DSS was induced.
Results: After consuming both probiotics, the levels of inflammatory markers, such as tumour necrosis factor alpha (TNF-α) and interleukins (IL-1β) exhibited a noticeable decline, indicating a reduction in inflammation. The Disease Activity indices for both probiotic-treated groups (P. acidilactici BCB1H- and L. plantarum HMX2-treated groups) were significantly lower (1±0.45, 1±0.36, 3±0.08, 1±0.18, respectively) than that for the DSS-treated group. Both these treatment strains significantly affected the markers of oxidative stress and inflammation (i.e., malondialdehyde [MDA], superoxide dismutase [SOD], and myeloperoxidase [MPO], compared to the intoxicated group. Similarly, the BCB1H- and HMX2-treated groups showed partial recovery, with improved hepatocyte structure and reduced inflammatory cell infiltration, compared to the intoxicated group. Polymerase chain reaction results of gel analysis showed crucial indicators that measure both colonic integrity and inflammation across four experimental groups of colitis-induced mice. Pro-inflammatory cytokines (TNF-α and IL-1β), E-cadherin, and MUC2 mucin served as evaluated markers across experimental groups.
Conclusion: Increased expression of these genes suggests that both probiotic strains successfully enhanced and restored normal functions of the gut and suppressed inflammation. This could be attributed to the combined immunomodulatory action of probiotics.
References
2 Amelia R, Philip K, Pratama YE, Purwati E. Characterization and probiotic potential of lactic acid bacteria isolated from dadiah sampled in West Sumatra. Food Sci Technol. 2020;41:746–52. 10.1590/fst.30020
3 Kim KJ, Paik H-D, Kim JY. Immune-enhancing effects of Lactiplantibacillus plantarum 200655 isolated from Korean kimchi in a cyclophosphamide-induced immunocompromised mouse model. J Microbiol Biotechnol 2021;31:726–32. 10.4014/jmb.2103.03028
4 Zhou X, Zhang D, Qi W, Hong T, Xiong T, Wu T, et al. Exopolysaccharides from Lactiplantibacillus plantarum NCU116 facilitate intestinal homeostasis by modulating intestinal epithelial regeneration and microbiota. J Agric Food Chem. 2021;69:7863–73. 10.1021/acs.jafc.1c01898
5 Duary RK, Bhausaheb MA, Batish VK, Grover S. Anti-inflammatory and immunomodulatory efficacy of indigenous probiotic Lactiplantibacillus plantarum Lp91 in colitis mouse model. Mol Biol Rep. 2012;39:4765–75. 10.1007/s11033-011-1269-1
6 Ma Y, Fei Y, Han X, Liu G, Fang J. Lactiplantibacillus plantarum alleviates obesity by altering the composition of the gut microbiota in high-fat diet-fed mice. Front Nutr. 2022;9:947367. 10.3389/fnut.2022.947367
7 Li C, Nie S-P, Zhu K-X, Ding Q, Li C, Xiong T, et al. Lactiplantibacillus plantarum NCU116 improves liver function, oxidative stress and lipid metabolism in rats with high fat diet induced non-alcoholic fatty liver disease. Food Funct. 2014;5:3216–23. 10.1039/C4FO00549J
8 Jeong S, Kim Y, Park S, Lee D, Lee J, Hlaing SP, et al. Lactiplantibacillus plantarum metabolites elicit anticancer effects by inhibiting autophagy-related responses. Molecules. 2023;28:1890. 10.3390/molecules28041890
9 Zhang C-X, Wang H-Y, Chen T-X. Interactions between intestinal microflora/probiotics and the immune system. Biomed Res. Int. 2019;2019:919. 10.1155/2019/6764919
10 Jang YJ, Kim W-K., Han, D. H., Lee, K., Ko, G. Lactobacillus fermentum species ameliorate dextran sulfate sodium-induced colitis by regulating the immune response and altering gut microbiota. Gut Microbes. 2019;10:696–711. 10.1080/19490976.2019.1589281
11 Hill D, Sugrue I, Tobin C, Hill C, Stanton C., Ross RP. The Lactobacillus casei group: History and health related applications. Front Microbiol. 2018;9:107. 10.3389/fmicb.2018.02107
12 Gill HS, Guarner F. Probiotics and human health: A clinical perspective. Postgrad Med J. 2004;80:516–26. 10.1136/pgmj.2003.008664
13 Wang J, Ji H, Wang S, Liu H, Zhang W, Zhang D, et al. Probiotic lactiplantibacillus plantarum promotes intestinal barrier function by strengthening the epithelium and modulating gut microbiota. Front Microbiol. 2018;9:1953. 10.3389/fmicb.2018.01953
14 Ewaschuk JB, Dieleman LA. Probiotics and prebiotics in chronic inflammatory bowel diseases. World J Gastroenterol WJ. 2006;12:5941. 10.3748/wjg.v12.i37.5941
15 Li Q, Zheng T, Ding H, Chen J, Li B, Zhang Q, et al. Exploring the benefits of probiotics in gut inflammation and diarrhea—from an antioxidant perspective. Antioxidants. 2023;12:1342. 10.3390/antiox12071342
16 Chassaing B, Aitken JD, Malleshappa M, Vijay-Kumar M. Dextran sulfate sodium (DSS)-induced colitis in mice. Curr Protoc Immunol. 2014;104:15–25. 10.1002/0471142735.im1525s104
17 Eichele DD, Kharbanda KK. Dextran sodium sulfate colitis murine model: An indispensable tool for advancing our understanding of inflammatory bowel diseases pathogenesis. World J Gastroenterol. 2017;23:6016. 10.3748/wjg.v23.i33.6016
18 Kanwal S, Joseph TP, Aliya S, Song S, Saleem MZ, Nisar MA, et al. Attenuation of DSS-induced colitis by dictyophoraindusiata polysaccharide (DIP) via modulation of gut microbiota and inflammatory-related signaling pathways. J Funct Foods. 2020;64:103641. 10.1016/j.jff.2019.103641
19 Zhang W-Q, Quan K-Y, Feng C-J, Zhang T, He Q-W, Kwok L-Y, et al. The Lactobacillus gasseri G098 strain mitigates symptoms of DSS-induced inflammatory bowel disease in mice. Nutrients. 2022;14:3745. 10.3390/nu14183745
20 Sun M-C, Zhang F-C, Yin X, Cheng B-J, Zhao C-H, Wang Y-L, et al. Lactobacillus reuteri F-9-35 prevents DSS-Induced colitis by inhibiting proinflammatory gene expression and restoring the gutmicrobiota in mice. J Food Sci. 2018;83:2645–52. 10.1111/1750-3841.14326
21 Guo N, Lv L. Mechanistic insights into the role of probiotics in modulating immune cells in ulcerative colitis. Immun Inflamm Dis. 2023;11:e1045. 10.1002/iid3.1045
22 Kim H, Yoo M-S, Jeon H, Shim J-J, Park W-J, Kim J-Y, et al. Probiotic properties and safety evaluation of Lactiplantibacillus plantarum HY7718 with superior storage stability isolated from fermented squid. Microorganisms. 2023;11:2254. 10.3390/microorganisms11092254
23 Molodecky NA, Soon IS, Rabi DM, Ghali WA, Ferris M, Chernoff G, et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology. 2012;142:46–54.e42. 10.1053/j.gastro.2011.10.001
24 Alemany-Cosme E, Sáez-González E, Moret I, Mateos B, Iborra M, Nos P, et al. Oxidative stress in the pathogenesis of Crohn’s disease and the interconnection with immunological response, microbiota, external environmental factors, and epigenetics. Antioxidants (Basel). 2021;10:64. 10.3390/antiox10010064
25 Haneishi Y, Furuya Y, Hasegawa M, Picarelli A, Rossi M., Miyamoto J. Inflammatory bowel diseases and gut microbiota. Int J Mol Sci. 2023;24:817. 10.3390/ijms24043817
26 Buttó LF, Haller D. Dysbiosis in intestinal inflammation: Cause or consequence. Int J Med Microbiol. 2016;306:302–9. 10.1016/j.ijmm.2016.02.010
27 Guenther C, Josenhans C, Wehkamp J. Crosstalk between microbiota, pathogens and the innate immune responses. Int J Med Microbiol. 2016;306:257–65. 10.1016/j.ijmm.2016.03.003
28 Chen D, Lv J, Han T, Kan J, Jin CH, Liu J. Hepatic antioxidant and gut ecological modulation properties of long-term intake of tea (Camellia sinensis L.) flower extract in vivo. Quality Assurance and Safety of Crops & Foods. 2023;15(3):11–21. 10.15586/qas.v15i3.1209
29 Song W, Lv W, Bi N, Wang G. Tectorigenin suppresses the viability of gastric cancer cells in vivo and in vitro. Quality Assurance and Safety of Crops & Foods. 2023;15(3):117–125. 10.15586/qas.v15i3.1357
30 Aziz T, Shabbir MA, Sarwar A, Yang Z, Lin L, Al-Megrin WAI, Shami A, Alwethaynani MS, Alhhazmi AA, Al-Asmari F, Al-Joufi FA, Fallatah D. Revealing Lactiplantibacillus Plantarum K25 Derived (Z)-18-Octadec-9-Enolide in Modulating Aquaporin-8 in Colorectal Cancer by Bridging the Gut Microbiome and Membrane Biology. Cell Biochem Biophys. 2025;1–16. 10.1007/s12013-025-01853-9
31 Vargas Robles H, Citalán Madrid AF, García Ponce A, Silva Olivares A, Shibayama M, Betanzos A, et al. Experimental colitis is attenuated by cardioprotective diet supplementation that reduces oxidative stress, inflammation, and mucosal damage. Oxidative Med Cell Longev. 2016;2016:1–9. 10.1155/2016/8473242
32 Wang C, Chen J. microRNAs as therapeutic targets in intestinal diseases. ExRNA 2019;1:1–12. 10.1186/s41544-019-0026-9
33 Ul Ain N, Naveed M, Aziz T, Shabbir MA, Al Asmari F, Abdi G, Sameeh MY, Alhhazmi AA. Mix-match synthesis of nanosynbiotics from probiotics and prebiotics to counter gut dysbiosis via AI integrated formulation profiling. Sci Rep. 2024;8;14(1):18397. 10.1038/s41598-024-69515-z
34 Ahmad W, Din AU, Khan TM, Rehman MU, Hassan A, Aziz T, Alharbi M, Wu J. Lacticaseibacillusparacasei BNCC345679 revolutionizes DSS-induced colitis and modulates gut microbiota. Front Microbiol. 2024;15:1343891. 10.3389/fmicb.2024.1343891
35 Algieri F, Garrido-Mesa J, Vezza T, Rodríguez-Sojo MJ, Rodríguez-Cabezas ME, Olivares M, et al. Intestinal anti-inflammatory effects of probiotics in DNBS-colitis via modulation of gut microbiota and microRNAs. Eur J Nutr. 2021;60:2537–51. 10.1007/s00394-020-02441-8
36 Seyedian SS, Nokhostin F, Malamir MD. A review of the diagnosis, prevention, and treatment methods of inflammatory bowel disease. J Med Life. 2019;12:113. 10.25122/jml-2018-0075
37 Mitropoulou M-A, Fradelos EC, Lee KY, Malli F, Tsaras K, Christodoulou NG, et al. Quality of life in patients with inflammatory bowel disease: Importance of psychological symptoms. Cureus. 2022;14:e28502. 10.7759/cureus.28502
38 Curr D, Ianiro G, Pecere S, Bibb S, Cammarota G. Probiotics, fibre and herbal medicinal products for functional and inflammatory bowel disorders. Br J Pharmacol. 2017;174:1426–49. 10.1111/bph.13632
39 Osman N, Adawi D, Molin G, Ahrne S, Berggren A, Jeppsson B. Bifidobacterium infantis strains with and without a combination of oligofructose and inulin (OFI) attenuate inflammation in DSS-induced colitis in rats. BMC Gastroenterol. 2006;6:31. 10.1186/1471-230X-6-31
40 Zhang X, Li M, Wei D, Wang X, Chen X, Xing L. Disruption of the fatty acid Δ6-desaturase gene in the oil-producing fungus Mortierellaisabellina by homologous recombination. Curr Microbiol. 2007;55:128–34. 10.1007/s00284-006-0641-1
41 Allonsius CN, van den Broek MFL, De Boeck I, Kiekens S, Oerlemans EFM, Kiekens F, et al. Interplay between Lactobacillus rhamnosus and Candida and the involvement of exopolysaccharides. Microb Biotechnol. 2017;10:1753–63. 10.1111/1751-7915.12799
42 Bancroft John D, Gamble Marilyn G. Theory and practice of histological techniques, 6th ed. Philadelphia, PA: Churchill Livingstone Elsevier; ©2008, 725 p.
43 Din AU, Hasan A, Zhu Y, Zhang K, Wang Y, Li T, et al. Inhibitory effect of Bifidobacterium bifidum ATCC 29521 on colitis and its mechanism. J Nutr Biochem. 2020;79:108353. 10.1016/j.jnutbio.2020.108353
44 Li D, Chen H, Mao B, Yang Q, Zhao J, Gu Z, et al. Microbial biogeography and core microbiota of the rat digestive tract. Sci Rep. 2017;8:45840. 10.1038/srep45840
45 Das KM. Pharmacotherapy of inflammatory bowel disease. Postgrad Med. 1983;74:141–51. 10.1080/00325481.1983.11698537
46 Plessas S, Nouska C, Karapetsas A, Kazakos S, Alexopoulos A, Mantzourani I, et al. Isolation, characterization and evaluation of the probiotic potential of a novel Lactobacillus strain isolated from Feta-type cheese. Food Chem. 2017;226:102–8. 10.1016/j.foodchem.2017.01.052
47 Arellano K, Vazquez J, Park H, Lim J, Ji Y, Kang HJ, et al. Safety evaluation and whole-genome annotation of Lactobacillus plantarum strains from different sources with special focus on isolates from green tea. Probiotics Antimicrob. Prot. 2020;12:1057–70. 10.1007/s12602-019-09620-y
48 Wang P, Wu Z, Wu J, Pan D, Zeng X, Cheng K. Effects of salt stress on carbohydrate metabolism of Lactobacillus plantarum ATCC 14917. Curr Microbiol. 2016;73:491–7. 10.1007/s00284-016-1087-8
49 Ahn E-M, Kim S-J. The improving effect of gastrodiaelatablume on DSS-induced colitis in mice. Biomed Sci Lett. 2018;24:168–74. 10.15616/BSL.2018.24.3.168
50 Kono Y. Reprint of: generation of superoxide radical during autoxidation of hydroxylamine and an assay for superoxide dismutase. Arch Biochem Biophys. 2022;726:109247. 10.1016/j.abb.2022.109247
51 Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979;95:351–8. 10.1016/0003-2697(79)90738-3
52 Eiserich JP, Hristova M, Cross CE, Jones AD, Freeman BA, Halliwell B, et al. Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature. 1998;391:393–7. 10.1038/34923
53 Dejban P, Nikravangolsefid N, Chamanara M, Dehpour A, Rashidian A. The role of medicinal products in the treatment of inflammatory bowel diseases (IBD) through inhibition of TLR4/NF-kappaB pathway. Phytother Res. 2021;35(2):835–45. 10.1002/ptr.6866
54 Muzes G, Molnár B, Tulassay Z, Sipos F. Changes of the cytokine profile in inflammatory bowel diseases. World J Gastroenterol (WJG). 2012;18:5848. 10.3748/wjg.v18.i41.5848
55 Capaldo CT, Farkas AE, Hilgarth RS, Krug SM, Wolf MF, Benedik JK, et al. A. proinflammatory cytokine-induced tight junction remodeling through dynamic self-assembly of claudins. Mol Biol Cell. 2014;25:2710–9. 10.1091/mbc.e14-02-0773
56 Al-Sadi R, Boivin M, Ma T. Mechanism of cytokine modulation of epithelial tight junction barrier. Front Biosci A J Virtual Libr. 2009;14:2765. 10.2741/3413
57 Guo J, Liao M, Wang J. TLR4 signaling in the development of colitis-associated cancer and its possible interplay with microRNA-155. Cell Commun Signal. 2021;19:90. 10.1186/s12964-021-00771-6
58 Pisani A, Rausch P, Bang C, Ellul S, Tabone T, Marantidis Cordina C, et al. Dysbiosis in the gut microbiota in patients with inflammatory bowel disease during remission. Microbiol Spectr. 2022;10:e00616-22. 10.1128/spectrum.00616-22
59 Kim D-Y, Lee T-S, Jung D-H, Song E-J, Jang A-R, Park J-Y, et al. Oral administration of Lactobacillus sakei CVL-001 improves recovery from dextran sulfate sodium-induced colitis in mice by microbiota modulation. Microorganisms. 2023;11:1359. 10.3390/microorganisms11051359
60 Baldelli V, Scaldaferri F, Putignani L, Del Chierico F. The role of Enterobacteriaceae in gut microbiota dysbiosis in inflammatory bowel diseases. Microorganisms. 2021;9:697. 10.3390/microorganisms9040697
61 Chassaing B, Aitken JD, Malleshappa M, Vijay-Kumar M. Dextran sulfate sodium (DSS)-induced colitis in mice. Curr Protoc Immunol. 2014;104:15–25. 10.1002/0471142735.im1525s104
62 Choi S, Woo J-K, Jang Y-S, Kang J-H, Jang J-E, Yi T-H, et al. Fermented Pueraria lobata extract ameliorates dextran sulfate sodium-induced colitis by reducing pro-inflammatory cytokines and recovering intestinal barrier function. Lab Anim Res. 2016;32:151–9. 10.5625/lar.2016.32.3.151
63 Ahn E-M, Kim S-J. The improving effect of gastrodiaelatablume on DSS-induced colitis in mice. Biomed Sci Lett. 2018;24:168–74. 10.15616/BSL.2018.24.3.168
64 Silva JP, Navegantes-Lima KC, Oliveira AL, Rodrigues DV, Gaspar SL, Monteiro VV, et al. Protective mechanisms of butyrate on inflammatory bowel disease. Curr Pharm Des. 2018;24:4154–66. 10.2174/1381612824666181001153605
65 Wang Y, Xie Q, Zhang Y, Ma W, Ning K, Xiang J-Y, et al. Combination of probiotics with different functions alleviate DSS-induced colitis by regulating intestinal microbiota, IL-10, and barrier function. Appl Microbiol Biotechnol. 2020;104:335–49. 10.1007/s00253-019-10259-6