Acta Med. 2021, 64: 85-90

https://doi.org/10.14712/18059694.2021.15

The Effect of Lactobacillus casei on Experimental Porcine Inflammatory Bowel Disease Induced by Dextran Sodium Sulphate

Jan Bureša, Darina Kohoutováa,b, Jaroslav Květinaa, Věra Radochovác, Michal Pavlíkc, Aleš Tichýd, Stanislav Rejchrta, Marcela Kopáčováa, Tomáš Doudaa, David Vysloužile, Jaroslav Pejchale

a2nd Department of Internal Medicine – Gastroenterology, Charles University, Faculty of Medicine in Hradec Králové, University Hospital, Hradec Králové, Czech Republic
bThe Royal Marsden NHS Foundation Trust, London, United Kingdom
cAnimal Laboratory, University of Defence, Faculty of Military Health Sciences, Hradec Králové, Czech Republic
dDepartment of Radiobiology, University of Defence, Faculty of Military Health Sciences, Hradec Králové, Czech Republic
eDepartment of Toxicology and Military Pharmacy, University of Defence, Faculty of Military Health Sciences, Hradec Králové, Czech Republic

Received December 21, 2020
Accepted February 26, 2021

References

1. Larabi A, Barnich N, Nguyen HTT. New insights into the interplay between autophagy, gut microbiota and inflammatory responses in IBD. Autophagy 2019: 1–14.
2. de Vos WM, de Vos EAJ. Role of the intestinal microbiome in health and disease: from correlation to causation. Nutr Rev 2012; 70: S45–56. <https://doi.org/10.1111/j.1753-4887.2012.00505.x>
3. Venema K, Do Carmo AP. Future possibilities for pro- and prebiotics: Is the sky the limit? In: Venema K, Do Carmo AP, Eds. Probiotics and Prebiotics. Current Research and Future Trends. Norfolk: Caister Academic Press, 2015: 489–93.
4. Parker EA, Roy T, D’Adamo CR, Wieland LS. Probiotics and gastrointestinal conditions: An overview of evidence from the Cochrane Collaboration. Nutrition 2018; 45: 125–34. <https://doi.org/10.1016/j.nut.2017.06.024> <PubMed>
5. Kruis W, Fric P, Pokrotnieks J, Lukas M, et al. Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 2004; 53: 1617–23. <https://doi.org/10.1136/gut.2003.037747> <PubMed>
6. Derwa Y, Gracie DJ, Hamlin PJ, Ford AC. Systematic review with meta-analysis: the fficacy of probiotics in inflammatory bowel disease. Aliment Pharmacol Ther 2017; 46: 389–400. <https://doi.org/10.1111/apt.14203>
7. Gomollón F, Dignass A, Annese V, et al. 3rd European Evidence-based Consensus on the Diagnosis and Management of Crohn’s Disease 2016: Part 1: Diagnosis and medical management. J Crohns Colitis 2017; 11: 3–25. <https://doi.org/10.1093/ecco-jcc/jjw168>
8. Butterworth AD, Thomas AG, Akobeng AK. Probiotics for induction of remission in Crohn’s disease. Cochrane Database Syst Rev 2008; CD006634.
9. Doherty G, Bennett G, Patil S, Cheifetz A, Moss AC. Interventions for prevention of post-operative recurrence of Crohn’s disease. Cochrane Database Syst Rev 2009; CD006873.
10. Rolfe VE, Fortun PJ, Hawkey CJ, Bath-Hextall F. Probiotics for maintenance of remission in Crohn’s disease. Cochrane Database Syst Rev 2006; CD004826.
11. Danese S, Fiocchi C. Ulcerative colitis. N Engl J Med 2011; 365: 1713–25. <https://doi.org/10.1056/NEJMra1102942>
12. Magro F, Gionchetti P, Eliakim R, et al. Third European Evidence-based Consensus on Diagnosis and Management of Ulcerative Colitis. Part 1: Definitions, diagnosis, extra-intestinal manifestations, pregnancy, cancer surveillance, surgery, and ileo-anal pouch disorders. J Crohns Colitis 2017; 11: 649–70. <https://doi.org/10.1093/ecco-jcc/jjx008>
13. Harbord M, Eliakim R, Bettenworth D, et al. European Evidence-based Consensus on Diagnosis and Management of Ulcerative Colitis. Part 2: Current management. J Crohns Colitis 2017; 11: 1512. <https://doi.org/10.1093/ecco-jcc/jjx105>
14. Mallon P, McKay D, Kirk S, Gardiner K. Probiotics for induction of remission in ulcerative colitis. Cochrane Database Syst Rev 2007; CD005573.
15. Naidoo K, Gordon M, Fagbemi AO, Thomas AG, Akobeng AK. Probiotics for maintenance of remission in ulcerative colitis. Cochrane Database Syst Rev 2011; CD007443.
16. Nguyen N, Zhang B, Holubar SD, Pardi DS, Singh S. Treatment and prevention of pouchitis after ileal pouch-anal anastomosis for chronic ulcerative colitis. Cochrane Database Syst Rev 2019; CD001176.
17. Tamaru T, Kobayashi H, Kishimoto S, Kajiyama G, Shimamoto F, Brown WR. Histochemical study of colonic cancer in experimental colitis of rats. Dig Dis Sci 1993; 38: 529–37. <https://doi.org/10.1007/BF01316510>
18. Dieleman LA, Ridwan BU, Tennyson GS, Beagley KW, Bucy RP, Elson CO. Dextran sulphate sodium-induced colitis occurs in severe combined immunodeficient mice. Gastroenterology 1994; 107: 1643–52. <https://doi.org/10.1016/0016-5085(94)90803-6>
19. Ni J, Chen SF, Hollander D. Effects of dextran sulphate sodium on intestinal epithelial cells and intestinal lymphocytes. Gut 1996; 39: 234–41. <https://doi.org/10.1136/gut.39.2.234> <PubMed>
20. Bassaganya-Riera J, Hontecillas R. CLA and n-3 PUFA differentially modulate clinical activity and colonic PPAR-responsive gene expression in a pig model of experimental IBD. Clin Nutr 2006; 25: 454–65. <https://doi.org/10.1016/j.clnu.2005.12.008>
21. Lackeyram D, Young D, Kim CJ, et al. Interleukin-10 is differentially expressed in the small intestine and the colon experiencing chronic inflammation and ulcerative colitis induced by dextran sodium sulphate in young pigs. Physiol Res 2017; 66: 147–62. <https://doi.org/10.33549/physiolres.933259>
22. Xiao Y, Yan H, Diao H, et al. Early Gut Microbiota Intervention Suppresses DSS-Induced Inflammatory Responses by Deactivating TLR/NLR Signalling in Pigs. Sci Rep 2017; 7: 3224. <https://doi.org/10.1038/s41598-017-03161-6> <PubMed>
23. Kararli TT. Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory animals. Biopharm Drug Dispos 1995; 16: 351–80. <https://doi.org/10.1002/bdd.2510160502>
24. Suenderhauf C, Parrott N. A physiologically based pharmacokinetic model of the minipig: data compilation and model implementation. Pharm Res 2013; 30: 1–15. <https://doi.org/10.1007/s11095-012-0911-5>
25. Ke S, Fang S, He M, Huang X, et al. Age-based dynamic changes of phylogenetic composition and interaction networks of health pig gut microbiome feeding in a uniformed condition. BMC Vet Res 2019; 15: 172. <https://doi.org/10.1186/s12917-019-1918-5> <PubMed>
26. Shin D, Chang SY, Bogere P, et al. Beneficial roles of probiotics on the modulation of gut microbiota and immune response in pigs. PLoS ONE 2019; 14: e0220843. <https://doi.org/10.1371/journal.pone.0220843> <PubMed>
27. Wang X, Tsai T, Deng F, et al. Longitudinal investigation of the swine gut microbiome from birth to market reveals stage and growth performance associated bacteria. Microbiome 2019; 7: 109. <https://doi.org/10.1186/s40168-019-0721-7> <PubMed>
28. Bures J, Pejchal J, Kvetina J, et al. Morphometric analysis of the porcine gastrointestinal tract in a 10-day high-dose indomethacin administration with or without probiotic bacteria Escherichia coli Nissle 1917. Hum Exp Toxicol 2011; 30: 1955–62. <https://doi.org/10.1177/0960327111403174>
29. Bures J, Smajs D, Kvetina J, et al. Bacteriocinogeny in experimental pigs treated with indomethacin and Escherichia coli Nissle. World J Gastroenterol 2011; 17: 609–17. <https://doi.org/10.3748/wjg.v17.i5.609> <PubMed>
30. Santiago-López L, Hernández-Mendoza A, Vallejo-Cordoba B, Mata-Haro V, Wall-Medrano A, González-Córdova AF. Milk fermented with Lactobacillus fermentum ameliorates indomethacin-induced intestinal inflammation: An exploratory study. Nutrients 2019; 11: e1610. <https://doi.org/10.3390/nu11071610> <PubMed>
31. Osaka T, Moriyama E, Arai S, et al. Meta-analysis of fecal microbiota and metabolites in experimental colitic mice during the inflammatory and healing phases. Nutrients 2017; 9: e1329. <https://doi.org/10.3390/nu9121329> <PubMed>
32. Zhang Y, Zhao X, Zhu Y, Ma J, Ma H, Zhang H. Probiotic mixture protects dextran sulphate sodium-induced colitis by altering tight junction protein expressions and increasing tregs. Mediators Inflamm 2018; 2018: 9416391.
33. Wang G, Liu Y, Lu Z, et al. The ameliorative effect of a Lactobacillus strain with good adhesion ability against dextran sulphate sodium-induced murine colitis. Food Funct 2019; 10: 397–409. <https://doi.org/10.1039/C8FO01453A>
34. Wasilewska E, Zlotkowska D, Wroblewska B. Yogurt starter cultures of Streptococcus thermophilus and Lactobacillus bulgaricus ameliorate symptoms and modulate the immune response in a mouse model of dextran sulphate sodium-induced colitis. J Dairy Sci 2019; 102: 37–53. <https://doi.org/10.3168/jds.2018-14520>
35. Tveden-Nyborg P, Bergmann TK, Lykkesfeldt J. Basic & clinical pharmacology & toxicology policy for experimental and clinical studies. Basic Clin Pharmacol Toxicol 2018; 123: 233–5. <https://doi.org/10.1111/bcpt.13059>
36. Explanatory Report on the European Convention for the Protection of Vertebrate Animals Used for Experimental and Other Scientific Purposes (ETS 123). Strasbourg: Council of Europe, 2009.
37. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 2010; 8: e1000412. <https://doi.org/10.1371/journal.pbio.1000412> <PubMed>
38. Appleyard CB, Wallace JL. Reactivation of hapten-induced colitis and its prevention by anti-inflammatory drugs. Am J Physiol 1995; 269: G119–125.
39. Pejchal J, Sinkorova Z, Tichy A, et al. Epidermal Growth Factor Attenuates Delayed Ionizing Radiation-Induced Tissue Damage in Bone Marrow Transplanted Mice. Radiat Res 2016; 186: 264–74. <https://doi.org/10.1667/RR14247.1>
40. Venema K, Meijerink M. Lactobacilli as probiotics: Discovering new functional aspects and target sites. In: Venema K, Do Carmo AP, Eds. Probiotics and Prebiotics. Current Research and Future Trends. Norfolk: Caister Academic Press, 2015: 29–41.
41. Rochat T, Bermúdez-Humarán L, Gratadoux JJ, et al. Anti-inflammatory effects of Lactobacillus casei BL23 producing or not a manganese-dependant catalase on DSS-induced colitis in mice. Microb Cell Fact 2007; 6: 22. <https://doi.org/10.1186/1475-2859-6-22> <PubMed>
42. Watterlot L, Rochat T, Sokol H, et al. Intragastric administration of a superoxide dismutase-producing recombinant Lactobacillus casei BL23 strain attenuates DSS colitis in mice. Int J Food Microbiol 2010; 144: 35–41. <https://doi.org/10.1016/j.ijfoodmicro.2010.03.037>
43. Wong CC, Zhang L, Li ZJ, et al. Protective effects of cathelicidin-encoding Lactococcus lactis in murine ulcerative colitis. J Gastroenterol Hepatol 2012; 27: 1205–12. <https://doi.org/10.1111/j.1440-1746.2012.07158.x>
44. Yoon S-W, Lee C-H, Kim J-Y, Kim J-Y, Sung M-H, Poo H. Lactobacillus casei secreting alpha-MSH induces the therapeutic effect on DSS-induced acute colitis in Balb/c mice. J Microbiol Biotechnol 2008; 18: 1975–83.
45. Qiu ZB, Chen J, Chen JJ, et al. Effect of recombinant Lactobacillus casei expressing interleukin-10 in dextran sulphate sodium-induced colitis mice. J Dig Dis 2013; 14: 76–83. <https://doi.org/10.1111/1751-2980.12006>
46. Chung YW, Choi JH, Oh T-Y, Eun CS, Han DS. Lactobacillus casei prevents the development of dextran sulphate sodium-induced colitis in Toll-like receptor 4 mutant mice. Clin Exp Immunol 2008; 151: 182–9. <https://doi.org/10.1111/j.1365-2249.2007.03549.x> <PubMed>
47. Kokesova A, Frolova L, Kverka M, et al. Oral administration of probiotic bacteria (E. coli Nissle, E. coli O83, Lactobacillus casei) influences the severity of dextran sodium sulphate-induced colitis in BALB/c mice. Folia Microbiol (Praha) 2006; 51: 478–84. <https://doi.org/10.1007/BF02931595>
48. Chae JM, Chang MH, Heo W, et al. LB-9, novel probiotic lactic acid bacteria, ameliorates dextran sodium sulphate-induced colitis in mice by inhibiting TNF-α-mediated apoptosis of intestinal epithelial cells. J Med Food 2019; 22: 271–6. <https://doi.org/10.1089/jmf.2018.4236>
49. Yoda K, Miyazawa K, Hosoda M, Hiramatsu M, Yan F, He F. Lactobacillus GG-fermented milk prevents DSS-induced colitis and regulates intestinal epithelial homeostasis through activation of epidermal growth factor receptor. Eur J Nutr 2014; 53: 105–15. <https://doi.org/10.1007/s00394-013-0506-x> <PubMed>
50. Liu X-J, Yu R, Zou K-F. Probiotic mixture VSL#3 alleviates dextran sulphate sodium-induced colitis in mice by downregulating T follicular helper cells. Curr Med Sci 2019; 39: 371–8. <https://doi.org/10.1007/s11596-019-2045-z>
51. Zakostelska Z, Kverka M, Klimesova K, et al. Lysate of probiotic Lactobacillus casei DN-114 001 ameliorates colitis by strengthening the gut barrier function and changing the gut microenvironment. PLoS ONE 2011; 6: e27961. <https://doi.org/10.1371/journal.pone.0027961> <PubMed>
52. Sang L-X, Chang B, Dai C, Gao N, Liu W-X, Jiang M. Heat-killed VSL#3 ameliorates dextran sulphate sodium (DSS)-induced acute experimental colitis in rats. Int J Mol Sci 2013; 15: 15–28. <https://doi.org/10.3390/ijms15010015> <PubMed>
53. Sang L-X, Chang B, Wang B-Y, Liu W-X, Jiang M. Live and heat-killed probiotic: effects on chronic experimental colitis induced by dextran sulphate sodium (DSS) in rats. Int J Clin Exp Med 2015; 8: 20072–8.
54. Herías MV, Koninkx JFJG, Vos JG, Huis in’t Veld JHJ, van Dijk JE. Probiotic effects of Lactobacillus casei on DSS-induced ulcerative colitis in mice. Int J Food Microbiol 2005; 103: 143–55. <https://doi.org/10.1016/j.ijfoodmicro.2004.11.032>
55. Vetuschi A, Latella G, Sferra R, Caprilli R, Gaudio E. Increased proliferation and apoptosis of colonic epithelial cells in dextran sulphate sodium-induced colitis in rats. Dig Dis Sci 2002; 47: 1447–57. <https://doi.org/10.1023/A:1015931128583>
56. Araki Y, Mukaisyo K, Sugihara H, Fujiyama Y, Hattori T. Increased apoptosis and decreased proliferation of colonic epithelium in dextran sulphate sodium-induced colitis in mice. Oncol Rep 2010; 24: 869–74. <https://doi.org/10.3892/or.2010.869>
57. de Souza HSP, West GA, Rebert N, de la Motte C, Drazba J, Fiocchi C. Increased levels of survivin, via association with heat shock protein 90, in mucosal T cells from patients with Crohn’s disease. Gastroenterology 2012; 143: 1017–26.e9. <https://doi.org/10.1053/j.gastro.2012.06.039> <PubMed>
58. Mennigen R, Nolte K, Rijcken E, et al. Probiotic mixture VSL#3 protects the epithelial barrier by maintaining tight junction protein expression and preventing apoptosis in a murine model of colitis. Am J Physiol Gastrointest Liver Physiol 2009; 296: G1140–9. <https://doi.org/10.1152/ajpgi.90534.2008>
59. Bassaganya-Riera J, Viladomiu M, Pedragosa M, De Simone C, Carbo A, Shaykhutdinov R, et al. Probiotic bacteria produce conjugated linoleic acid locally in the gut that targets macrophage PPAR γ to suppress colitis. PLoS ONE 2012; 7: e31238. <https://doi.org/10.1371/journal.pone.0031238> <PubMed>
60. Mar JS, Nagalingam NA, Song Y, Onizawa M, Lee JW, Lynch SV. Amelioration of DSS-induced murine colitis by VSL#3 supplementation is primarily associated with changes in ileal microbiota composition. Gut Microbes 2014; 5: 494–503. <https://doi.org/10.4161/gmic.32147>
61. Venema K. Functional aspects of the endogenous microbiota that benefit the host. In: Venema K, Do Carmo AP, Eds. Probiotics and Prebiotics. Current Research and Future Trends. Norfolk: Caister Academic Press, 2015: 221–33.
front cover

ISSN 1211-4286 (Print) ISSN 1805-9694 (Online)

Open access journal

Archive