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Inhibitory Effects of Bacillus Coagulans TL3 on the Ileal Oxidative Stress and Inflammation Induced by Lipopolysaccharide in Rats

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Abstract

This study aimed to explore the effect and mechanism of Bacillus coagulans TL3 (B. coagulans TL3) on ileal inflammatory injury induced by lipopolysaccharide (LPS). Animal models were established wherein male Wistar rats were randomly divided into four groups: a control group, an LPS group, a high-concentration B. coagulans (HBC) group, and a low-concentration B. coagulans (LBC) group. The results showed that the biochemical indices changed, significant pathological changes were found, the number of apoptotic cells increased in the ileal tissue of the LPS group rats; the protein expressions of NFκB, MYD88, TLR4, TNF-α, Il-6, IL-1β, Claudin-1, Occludin, and ZO-1 in the LPS group were significantly decreased. The biochemical indices, pathological changes, and protein expressions in rats subjected to intragastric administration with high or low concentrations of B. coagulans TL3, were significantly reversed compared with the LPS group. These results indicated that TL3 strain could protect rats against ileal oxidative stress and inflammation induced by LPS and the protective mechanism was related to inhibition of the toll-like receptor 4 (TLR4) / myeloid differentiation factor-88 (MyD88) signaling pathway.

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Data Availability

The data and materials that support the findings of this study are available from the corresponding author upon reasonable request.

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References

  1. Yuan Z, Yang L, Zhang X, Ji P, Wei Y (2020) Therapeutic effect of n-butanol fraction of Huang-lian-Jie-du Decoction on ulcerative colitis and its regulation on intestinal flora in colitis mice. Biomed Pharmacother 121:109638

    Article  CAS  Google Scholar 

  2. Kil DY, Stein HH (2010) Invited review: Management and feeding strategies to ameliorate the impact of removing antibiotic growth promoters from diets fed to weanling pigs. Can J Anim Sci 90:447–460

    Article  CAS  Google Scholar 

  3. Zhang X, Zhang J, Han Q, Wang X, Zhao S (2021) Antibiotics in mariculture organisms of different growth stages: tissue-specific bioaccumulation and influencing factors. Environ Pollut 288:117715

    Article  CAS  Google Scholar 

  4. Bogaard AEvd, Stobberingh EE, (2000) Epidemiology of resistance to antibiotics: Links between animals and humans. Int J Antimicrob Agents 14:327–335

    Article  Google Scholar 

  5. Pei LY, Ke YS, Zhao HH, Wang L, Jia C, Liu WZ, Fu QH, Shi MN, Cui J, Li SC (2019) Role of colonic microbiota in the pathogenesis of ulcerative colitis. BMC Gastroenterol 19:10

    Article  Google Scholar 

  6. Li Z, Qi X, Zhang X, Yu L, Gao L, Kong W, Chen W, Dong W, Luo L, Lu D (2022) TRDMT1 exhibited protective effects against LPS-induced inflammation in rats through TLR4-NF-κB/MAPK-TNF-αpathway. Anim Model Exp Med 5:172–182

    Article  CAS  Google Scholar 

  7. Mei-Xue LI, Zhou W, Hui L, Tao L, Huang LG, Yuan WM, Neonatology DO (2014) Establishment and evaluation of necrotizing enterocolitis models induced by LPS combined with formula feeding in neonatal rats. J Develop Med 1:21–27

    Google Scholar 

  8. Lavrentev FV, Ashikhmina MS, Ulasevich SA, Morozova OV, Iakovchenko NV (2021) Perspectives of Bacillus coagulans Mtcc 5856 in the production of fermented dairy products. LWT- Food Sci Technol 148:111623

    Article  CAS  Google Scholar 

  9. Gözde K, Zerrin E (2018) Potential use of Bacillus coagulans in the food industry. Foods 7:92

    Article  Google Scholar 

  10. Endres JR, Qureshi I, Farber T, Hauswirth J, Hirka G, Pasics I, Schauss AG (2011) One-year chronic oral toxicity with combined reproduction toxicity study of a novel probiotic, Bacillus coagulans, as a food ingredient. Food Chem Toxicol 49:1174–1182

    Article  CAS  Google Scholar 

  11. Khempaka S, Maliwan P, Okrathok S, Molee W (2018) Digestibility, productive performance, and egg quality of laying hens as affected by dried cassava pulp replacement with corn and enzyme supplementation. Trop Anim Health Prod 50:1239–1247

    Article  Google Scholar 

  12. Ou MS, Ingram LO, Shanmugam KT (2011) L(+)-Lactic acid production from non-food carbohydrates by thermotolerant Bacillus coagulans. J Ind Microbiol 38:599–605

    CAS  Google Scholar 

  13. Gowthami P, Muthukumar K, Velan M (2015) Utilization of coconut oil cake for the production of lipase using Bacillus coagulans VKL1. Biocontrol Sci 20:125–133

    Article  CAS  Google Scholar 

  14. Liu JJ, Reid G, Jiang Y, Turner MS, Tsai CC (2010) Activity of HIV entry and fusion inhibitors expressed by the human vaginal colonizing probiotic lactobacillus reuteri RC-14. Cell Microbiol 9:120–130

    Article  CAS  Google Scholar 

  15. Bomko TV, Nosalskaya TN, Kabluchko TV, Lisnyak YV, Martynov AV (2017) Immunotropic aspect of the Bacillus coagulans probiotic action. J Pharm Pharmacol 69:1033–1040

    Article  CAS  Google Scholar 

  16. Sanders ME, Guarner F, Guerrant R, Holt PR, Quigley EM, Sartor RB, Sherman PM, Mayer EA (2013) An update on the use and investigation of probiotics in health and disease. Gut 62:787–796

    Article  CAS  Google Scholar 

  17. Haldar L, Gandhi DN, Mazumdar D (2016) Functional and probiotic potential of indigenous bacillis coagulans and bacillus pumilus strains. Int J Microbiol 8:731–736

    Google Scholar 

  18. Jurenka JS (2012) (2013): Bacillus coagulans: monograph. Alternative Med Rev 17:76–81

    Google Scholar 

  19. Marrec CL, Hyronimus B, Bressollier P, Verneuil B, Urdaci MC (2000) Biochemical and genetic characterization of coagulin, a new antilisterial bacteriocin in the pediocin family of bacteriocins, produced by Bacillus coagulans I(4). Appl Environmental Microbiol 66:5213–5220

    Article  Google Scholar 

  20. Ivec M, Boti T, Koren SK, Jakobsen M, Weingartl H, Cenci A (2007) Interactions of macrophages with probiotic bacteria lead to increased antiviral response against vesicular stomatitis virus. Antiviral Res 75:266–274

    Article  CAS  Google Scholar 

  21. Massacci L, Tofani T, Forte, (2019) Dietary saccharomyces cerevisiae boulardii CNCM I-1079 positively affects performance and intestinal ecosystem in broilers during a campylobacter jejuni infection. Microolrganisms 7:596

    Article  CAS  Google Scholar 

  22. Mingmongkolchai S, Panbangred W (2018) BacillusBacillus probiotics: an alternative to antibiotics for livestock production. J Appl Microbiol 124:1334–1346

    Article  CAS  Google Scholar 

  23. Scott BM, Gutiérrez-Vázquez C, Sanmarco LM, Pereira J, Quintana FJ (2021) Self-tunable engineered yeast probiotics for the treatment of inflammatory bowel disease. Nat Med 27(7):1212–1222

    Article  CAS  Google Scholar 

  24. Xu J, Li Y, Yang Z, Li C, Liang H, Wu Z, Pu W (2018) Yeast probiotics shape the gut microbiome and improve the health of early-weaned piglets. Front Microbiol 23:9

    Google Scholar 

  25. Chorawala MR, Chauhan S, Patel R, Shah G (2021) Cell wall contents of probiotics (Lactobacillus species) protect against lipopolysaccharide (LPS)-induced murine colitis by limiting immuno-inflammation and oxidative stress. Probiotics Antimicrob Proteins 13:1005–1017

    Article  CAS  Google Scholar 

  26. Zhang B, Zhang H, Yu Y, Zhang R, Yang C (2021) Effects of Bacillus Coagulans on growth performance, antioxidant capacity, immunity function and gut health in broilers. Poult Sci 100:101168

    Article  CAS  Google Scholar 

  27. Liu JB, Yan HL, Zhang Y, Hu YD, Zhang HF (2020) Effects of stale maize on growth performance, immunity, intestinal morphology and antioxidant capacity in broilers. Asian Australas J Anim Sci 33:605–614

    Article  CAS  Google Scholar 

  28. Sasaki H, mura Ma, Hamamoto, Murano, Toshina, Katsu, (2010) Prostaglandin E2 inhibits lesion formation in dextran sodium sulphate-induced colitis in rats and reduces the levels of mucosal inflammatory cytokines. Scand J Immunol 51:23–28

    Article  Google Scholar 

  29. Won-Tak C, Marcela S, Zhao L, Lindsay A, Namrata S, Liao X, Drage MG, Maria W, Cheng J, Lauwers GY (2021) Hypermucinous, goblet cell-deficient and crypt cell dysplasias in inflammatory bowel disease are often associated with flat/invisible endoscopic appearance and advanced neoplasia on follow-up. J Crohns Colitis 16:98–108

    Google Scholar 

  30. Fu R, Liang C, Chen D, Yan H, Yu B (2021) Effects of dietary Bacillus coagulans and yeast hydrolysate supplementation on growth performance, immune response and intestinal barrier function in weaned piglets. J Anim Physiol a Anim Nutr 105:898–907

    Article  CAS  Google Scholar 

  31. Narimatsu K, Higashiyama M, Kurihara C, Takajo T, Maruta K (2015) Toll-like receptor (TLR) 2 agonists ameliorate indomethacin-induced murine ileitis by suppressing the TLR4 signaling. Gastroenterol Hepatol 30:1610–1617

    Article  CAS  Google Scholar 

  32. Li BX, Li WY, Tian YB, Guo SX, Cao N (2019) Polysaccharide of atractylodes macrocephala koidz enhances cytokine secretion by stimulating the TLR4–MyD88–NF- κ B signaling pathway in the mouse spleen. J Med Food 22:937–943

    Article  CAS  Google Scholar 

  33. Álvarez B, Revilla C, Doménech N, Pérez C, Martínez P, Alonso F, Ezquerra A, Domíguez J (2007) Expression of toll-like receptor 2 (TLR2) in porcine leukocyte subsets and tissues. Vet Immunol Immunopathol 128:272

    Article  Google Scholar 

  34. Parlato M, Yeretssian G (2014) NOD-like receptors in intestinal homeostasis and epithelial tissue repair. Int J Mol Sci 15:9594–9627

    Article  CAS  Google Scholar 

  35. Tohno MAY, Shimazu T, Katoh S, Wang JM, Aso H, Takada H, Kawai Y, Saito T, Kitazawa H, Ueda W (2007) Molecular cloning and functional characterization of porcine nucleotide-binding oligomerization domain-2 (NOD2). Mol Immunol 45:194–203

    Article  Google Scholar 

  36. Brj A, Ksc B, Sh C, Snh C, Kjr C, Ml D, Hja A (2021) Rosmarinic acid represses colitis-associated colon cancer: a pivotal involvement of the TLR4-mediated NF-κB-STAT3 axis - Sciencedirect. Neoplasia 23:561–573

    Article  Google Scholar 

  37. Doyle A, Zhang G, Fattah E, Eissa NT, Li YP (2011) Toll-like receptor 4 mediates lipopolysaccharide-induced muscle catabolism via coordinate activation of ubiquitin-proteasome and autophagy-lysosome pathways. FASEB J 25:99–110

    Article  CAS  Google Scholar 

  38. Xu H, Hao S, Gan F, Wang H, Xu J, Liu D, Huang K (2017) Invitro immune toxicity of ochratoxin A in porcine alveolar macrophages: a role for the ROS-relative TLR4/MyD88 signaling pathway. Chemico-biologic interact 272:107–116

    Article  CAS  Google Scholar 

  39. Ulluwishewa D, Anderson RC, Mcnabb WC, Moughan PJ, Wells JM, Roy NC (2011) Regulation of tight junction permeability by intestinal bacteria and dietary components. J Nutr 141:769–776

    Article  CAS  Google Scholar 

  40. Gosain A, Gamelli RL (2005) Role of the gastrointestinal tract in burn sepsis. J Burn Care Rehabil 26:85–91

    Article  Google Scholar 

  41. Rfel M, Huber O (2013) Modulation of tight junction structure and function by kinases and phosphatases targeting occludin. J Biomed Biotechnol 2012:807356

    Google Scholar 

  42. González-Mariscal L, Tapia R, Chamorro D (2008) Crosstalk of tight junction components with signaling pathways. BBA Biomembranes 1778:729–756

    Article  Google Scholar 

  43. Jiang Y, Song J, Xu Y, Liu C, Qian W, Bai T, Hou X (2021) Piezo1 regulates intestinal epithelial function by affecting the tight junction protein claudin-1 via the ROCK pathway. Life Sci 275:119254

    Article  CAS  Google Scholar 

  44. Weber CR, Nalle SC, Tretiakova M, Rubin DT, Turner JR (2008) Claudin-1 and claudin-2 expression is elevated in inflammatory bowel disease and may contribute to early neoplastic transformation. Lab Invest 88:1110–1120

    Article  CAS  Google Scholar 

  45. Yu T, Lu XJ, Li JY, Shan TD, Huang CZ, Ouyang H, Yang HS, Xu JH, Zhong W, Xia ZS (2016) Overexpression of miR-429 impairs intestinal barrier function in diabetic mice by down-regulating occludin expression. Cell Tissue Res 366:341–352

    Article  CAS  Google Scholar 

  46. Balda MS (1996) Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. J Cell Biol 134:1031–1049

    Article  CAS  Google Scholar 

  47. Anonymous (2021) Enterococcus faecium HDRsEf1 inhibits LPS-induced downregulation of ZO-1 expression via TLR2/4-mediated JNK/AP-1 signalling pathways. J Appl Microbiol 132:605–617

    Google Scholar 

  48. Park SY, Jang H, Kim SY, Kim D, Park Y, Kee SH (2021) Expression of E-cadherin in epithelial cancer cells increases cell motility and directionality through the localization of ZO-1 during collective cell migration. Bioengineering 8:65

    Article  CAS  Google Scholar 

  49. Stuart RO, Nigam SK (1995) Regulated assembly of tight junctions by protein kinase C. Proc Natl Acad Sci 92:6072–6076

    Article  CAS  Google Scholar 

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Acknowledgments

The study was supported by Shenyang Agricultural University

Funding

This research was funded by the key grant Project of Liaoning Provincial Department of Education (Grants No. LJKZ0632); the National Natural Science Foundation of China (Grants No. 31972746; Grants No. 31772809; Grants No. 31872538).

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Author notes

  1. Jia Chen, Jing Cai and Jiaxi Lin have contributed equally to this work and should be considered co-first authors.

Authors and Affiliations

  1. College of Animal Science & Veterinary Medicine, Shenyang Agricultural University, Shenyang, 110866, China

    Jia Chen, Jing Cai, Jiaxi Lin, Ziyang Cheng & Miao Long

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Contributions

JC, JC, JL, ZC contributed to investigation. JC contributed to writing—original draft preparation. JC contributed to writing—review and editing. ML contributed to supervision. All authors have read and agreed to the published version of the manuscript. All authors have approved the final version of the manuscript and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated resolved. All persons designated as authors quality for authorship and all those who qualify for authorship are listed.

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Correspondence to Miao Long.

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The authors have no conflicts of interest to disclose.

Ethical Approval

The experiments were permitted by the Shenyang Agricultural University under the Laboratory Animal Care Ethics Committee (People’s Republic of China Animal Ethics Regulations and Guidelines) for animal experiments ((Permit No. 2019091402).

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Chen, J., Cai, J., Lin, J. et al. Inhibitory Effects of Bacillus Coagulans TL3 on the Ileal Oxidative Stress and Inflammation Induced by Lipopolysaccharide in Rats. Curr Microbiol 80, 84 (2023). https://doi.org/10.1007/s00284-022-03171-2

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