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Cell Wall Contents of Probiotics (Lactobacillus species) Protect Against Lipopolysaccharide (LPS)-Induced Murine Colitis by Limiting Immuno-inflammation and Oxidative Stress

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Abstract

Currently, there are no effective therapeutic agents to limit intestinal mucosal damage associated with inflammatory bowel disease (IBD). Based on several clinical studies, probiotics have emerged as a possible novel therapeutic strategy for IBD; however, their possible mechanisms are still poorly understood. Although probiotics in murine and human improve disease severity, very little is known about the specific contribution of cell wall contents of probiotics in IBD. Herein, we investigated the protective effects of cell wall contents of three Lactobacillus species in lipopolysaccharide (LPS)-induced colitis rats. LPS-sensitized rats were rendered colitic by colonic instillation of LPS (500 µg/rat) for 14 consecutive days. Concurrently, cell wall contents isolated from 106 CFU of L. casei (LC), L. acidophilus (LA), and L. rhamnosus (LA) was given subcutaneously for 21 days, considering sulfasalazine (100 mg/kg, p.o.) as standard. The severity of colitis was assessed by body weight loss, food intake, stool consistency, rectal bleeding, colon weight/length, spleen weight, and histological analysis. Colonic inflammatory markers (myeloperoxidase activity, C-reactive protein, and pro-inflammatory cytokines) and oxidative stress markers (malondialdehyde, reduced glutathione, and nitric oxide) were also assayed. Cell wall contents of LC, LA, and LR significantly ameliorated the severity of colitis by reducing body weight loss and diarrhea and bleeding incidence, improving food intake, colon weight/length, spleen weight, and microscopic damage to the colonic mucosa. The treatment also reduced levels of inflammatory and oxidative stress markers and boosted anti-oxidant molecule. In conclusion, cell wall contents of LC, LA, and LR attenuate LPS-induced colitis by modulating immuno-inflammation and oxidative stress.

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References

  1. Kaser A, Zeissig S, Blumberg RS (2010) Inflammatory bowel disease. Annu Rev Immunol 28:573–621. https://doi.org/10.1146/annurev-immunol-030409-101225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Toumi R, Soufli I, Rafa H, Belkhelfa M, Biad A, Touil-Boukoffa C (2014) Probiotic bacteria lactobacillus and bifidobacterium attenuate inflammation in dextran sulfate sodium-induced experimental colitis in mice. Int J Immunopathol Pharmacol 27(4):615–627. https://doi.org/10.1177/039463201402700418

    Article  CAS  PubMed  Google Scholar 

  3. Asquith MJ, Boulard O, Powrie F, Maloy KJ (2010) Pathogenic and protective roles of MyD88 in leukocytes and epithelial cells in mouse models of inflammatory bowel disease. Gastroenterology 139(2):519–529. https://doi.org/10.1053/j.gastro.2010.04.045

    Article  CAS  PubMed  Google Scholar 

  4. Garrett WS, Gordon JI, Glimcher LH (2010) Homeostasis and inflammation in the intestine. Cell 140(6):859–870. https://doi.org/10.1016/j.cell.2010.01.023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Ahlawat S, Asha, Sharma KK (2020) Gut-organ axis: a microbial outreach and networking. Lett Appl Microbiol https://doi.org/10.1111/lam.13333

  6. Geier MS, Butler RN, Howarth GS (2007) Inflammatory bowel disease: current insights into pathogenesis and new therapeutic options; probiotics, prebiotics and synbiotics. Int J Food Microbiol 115(1):1–11. https://doi.org/10.1016/j.ijfoodmicro.2006.10.006

    Article  CAS  PubMed  Google Scholar 

  7. Mangerich A, Dedon PC, Fox JG, Tannenbaum SR, Wogan GN (2013) Chemistry meets biology in colitis-associated carcinogenesis. Free Radic Res 47(11):958–986. https://doi.org/10.3109/10715762.2013.832239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Stephens M, von der Weid PY (2019) Lipopolysaccharides modulate intestinal epithelial permeability and inflammation in a species-specific manner. Gut Microbes 11(3):421–432. https://doi.org/10.1080/19490976.2019.1629235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Zhang L, Wei X, Zhang R, Si D, Petitte JN, Ahmad B, Zhang M (2019) A novel peptide ameliorates LPS-induced intestinal inflammation and mucosal barrier damage via its antioxidant and antiendotoxin effects. Int J Mol Sci 20(16):3974. https://doi.org/10.3390/ijms20163974

    Article  CAS  PubMed Central  Google Scholar 

  10. Plaza-Diaz J, Ruiz-Ojeda FJ, Gil-Campos M, Gil A (2019) Mechanisms of action of probiotics. Adv Nutr 10(suppl1):S49–S66. https://doi.org/10.1093/advances/nmy063

    Article  PubMed  PubMed Central  Google Scholar 

  11. Grimoud J, Durand H, de Souza S et al (2010) In vitro screening of probiotics and synbiotics according to anti-inflammatory and anti-proliferative effects. Int J Food Microbiol 144(1):42–50. https://doi.org/10.1016/j.ijfoodmicro.2010.09.007

    Article  CAS  PubMed  Google Scholar 

  12. Vanderpool C, Yan F, Polk DB (2008) Mechanisms of probiotic action: implications for therapeutic applications in inflammatory bowel diseases. Inflamm Bowel Dis 14(11):1585–1596. https://doi.org/10.1002/ibd.20525

    Article  PubMed  Google Scholar 

  13. LeBlanc JG, del Carmen S, Miyoshi A et al (2011) Use of superoxide dismutase and catalase producing lactic acid bacteria in TNBS induced Crohn’s disease in mice. J Biotechnol 151(3):287–293. https://doi.org/10.1016/j.jbiotec.2010.11.008

    Article  CAS  PubMed  Google Scholar 

  14. Sengul N, Isık S, Aslım B, Ucar G, Demirbag AE (2011) The effect of exopolysaccharide-producing probiotic strains on gut oxidative damage in experimental colitis. Dig Dis Sci 56(3):707–714. https://doi.org/10.1007/s10620-010-1362-7

    Article  PubMed  Google Scholar 

  15. Amaretti A, di Nunzio M, Pompei A, Raimondi S, Rossi M, Bordoni A (2013) Antioxidant properties of potentially probiotic bacteria: in vitro and in vivo activities. Appl Microbiol Biotechnol 97(2):809–817. https://doi.org/10.1007/s00253-012-4241-7

    Article  CAS  PubMed  Google Scholar 

  16. Songisepp E, Kals J, Kullisaar T, Mandar R, Hutt P, Zilmer M, Mikelsaar M (2005) Evaluation of the functional efficacy of an antioxidative probiotic in healthy volunteers. Nutr J 4:22. https://doi.org/10.1186/1475-2891-4-22.10.1186/1475-2891-4-22

    Article  PubMed  PubMed Central  Google Scholar 

  17. Ishikawa H, Akedo I, Umesaki Y, Tanaka R, Imaoka A, Otani T (2003) Randomized controlled trial of the effect of bifidobacteria-fermented milk on ulcerative colitis. J Am Coll Nutr 22(1):56–63. https://doi.org/10.1080/07315724.2003.10719276

    Article  PubMed  Google Scholar 

  18. LoreaBaroja M, Kirjavainen PV, Hekmat S, Reid G (2007) Anti-inflammatory effects of probiotic yogurt in inflammatory bowel disease patients. Clin Exp Immunol 149(3):470–479. https://doi.org/10.1111/j.1365-2249.2007.03434.x

    Article  CAS  Google Scholar 

  19. Simren M, Ohman L, Olsson J, Svensson U, Ohlson K, Posserud I, Strid H (2010) Clinical trial: the effects of a fermented milk containing three probiotic bacteria in patients with irritable bowel syndrome – a randomized, double-blind, controlled study. Aliment Pharmacol Ther 31(2):218–227. https://doi.org/10.1111/j.1365-2036.2009.04183.x

    Article  CAS  PubMed  Google Scholar 

  20. Haller D, Antoine JM, Bengmark S, Enck P, Rijkers GT, Lenoir-Wijnkoop I (2010) Guidance for substantiating the evidence for beneficial effects of probiotics: probiotics in chronic inflammatory bowel disease and the functional disorder irritable bowel syndrome. J Nutr 140(3):690S-697S. https://doi.org/10.3945/jn.109.113746

    Article  CAS  PubMed  Google Scholar 

  21. Steed H, Macfarlane GT, Blackett KL et al (2010) Clinical trial: the microbiological and immunological effects of synbiotic consumption - a randomized double-blind placebo-controlled study in active Crohn’s disease. Aliment Pharmacol Ther 32(7):872–883. https://doi.org/10.1111/j.1365-2036.2010.04417.x

    Article  CAS  PubMed  Google Scholar 

  22. Cha BK, Jung SM, Choi CH et al (2012) The effect of a multispecies probiotic mixture on the symptoms and fecal microbiota in diarrhea-dominant irritable bowel syndrome: a randomized, double-blind, placebo-controlled trial. J Clin Gastroenterol 46(3):220–227. https://doi.org/10.1097/MCG.0b013e31823712b1

    Article  Google Scholar 

  23. Niv E, Naftali T, Hallak R, Vaisman N (2005) The efficacy of Lactobacillus reuteri ATCC 55730 in the treatment of patients with irritable bowel syndrome – a double blind, placebo-controlled, randomized study. Clin Nutr 24(6):925–931. https://doi.org/10.1016/j.clnu.2005.06.001

    Article  PubMed  Google Scholar 

  24. Bousvaros A, Guandalini S, Baldassano RN et al (2005) A randomized, double-blind trial of Lactobacillus GG versus placebo in addition to standard maintenance therapy for children with Crohn’s disease. Inflamm Bowel Dis 11(9):833–839. https://doi.org/10.1097/01.mib.0000175905.00212.2c

    Article  PubMed  Google Scholar 

  25. Marteau P, Lemann M, Seksik P et al (2006) Ineffectiveness of Lactobacillus johnsonii LA1 for prophylaxis of postoperative recurrence in Crohn’s disease: a randomized, double blind, placebo controlled GETAID trial. Gut 55(6):842–847. https://doi.org/10.1136/gut.2005.076604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Chermesh I, Tamir A, Reshef R et al (2007) Failure of Synbiotic 2000 to prevent postoperative recurrence of Crohn’s disease. Dig Dis Sci 52(2):385–389. https://doi.org/10.1007/s10620-006-9549-7

    Article  PubMed  Google Scholar 

  27. Patel RB, Prajapati KD, Sonara BM et al (2014) Ameliorative potential of aliskiren in experimental colitis in mice. Eur J Pharmacol 737:70–76. https://doi.org/10.1016/j.ejphar.2014.05.009

    Article  CAS  PubMed  Google Scholar 

  28. Siegmund B, Rieder F, Albrich S et al (2001) Adenosine kinase inhibitor GP515 improves experimental colitis in mice. J Pharmacol Exp Ther 296(1):99–105

    CAS  PubMed  Google Scholar 

  29. Perez S, Talens-Visconti R, Rius-Perez S, Finamor I, Sastre J (2017) Redox signaling in the gastrointestinal tract. Free Radic Biol Med 104:75–103. https://doi.org/10.1016/j.freeradbiomed.2016.12.048

    Article  CAS  PubMed  Google Scholar 

  30. Podolsky DK (2002) Inflammatory bowel disease. N Engl J Med 347(6):417–429. https://doi.org/10.1056/NEJMra020831

    Article  CAS  PubMed  Google Scholar 

  31. Lebeer S, Claes IJJ, Vanderleyden J (2012) Anti-inflammatory potential of probiotics: lipoteichoic acid makes a difference. Trends Microbiol 20(1):5–10. https://doi.org/10.1016/j.tim.2011.09.004

    Article  CAS  PubMed  Google Scholar 

  32. Fessler MB, Malcolm KC, Duncan MW, Worthen GS (2002) A genomic and proteomic analysis of activation of the human neutrophil by lipopolysaccharide and its mediation by p38 mitogen-activated protein kinase. J Biol Chem 277(35):31291–31302. https://doi.org/10.1074/jbc.M200755200

    Article  CAS  PubMed  Google Scholar 

  33. Torres-Rodríguez ML, García-Chavez E, Berhow M, de Mejia EG (2016) Anti-inflammatory and anti-oxidant effect of Calea urticifolia lyophilized aqueous extract on lipopolysaccharide-stimulated RAW 264.7 macrophages. J Ethnopharmacol 188:266–274. https://doi.org/10.1016/j.jep.2016.04.057

    Article  CAS  PubMed  Google Scholar 

  34. Liu M, Li S, Wang X, Zhu Y, Zhang J, Liu H, Jia L (2018) Characterization, anti-oxidation and anti-inflammation of polysaccharides by Hypsizygus marmoreus against LPS-induced toxicity on lung. Int J Biol Macromol 111:121–128. https://doi.org/10.1016/j.ijbiomac.2018.01.010

    Article  CAS  PubMed  Google Scholar 

  35. Hotta T, Yoshida N, Yoshikawa T, Sugino S, Kondo M (1986) Lipopolysaccharide-induced colitis in rabbits. Res Exp Med (Berl) 186(1):61–69. https://doi.org/10.1007/BF01851834

    Article  CAS  Google Scholar 

  36. Im E, Riegler FM, Pothoulakis C, Rhee SH (2012) Elevated lipopolysaccharide in colon evokes intestinal inflammation, aggravated in immune modulator-impaired mice. Am J Physiol Gastrointest Liver Physiol 303(4):G490-497. https://doi.org/10.1152/ajpgi.00120.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Martin JC, Beriou G, Josien R (2016) Dextran sulfate sodium (DSS)-induced acute colitis in the rat. Methods Mol Biol 1371:197–203. https://doi.org/10.1007/978-1-4939-3139-2_12

    Article  CAS  PubMed  Google Scholar 

  38. Ashrafi F, Kowsari F, Darakhshandeh A, Adibi P (2014) Composite lymphoma in a patient with ulcerative colitis: a case report. Int J Hematol Oncol Stem Cell Res 8(4):45–48

    PubMed  PubMed Central  Google Scholar 

  39. Oustamanolakis P, Koutroubakis IE, Kouroumalis EA (2011) Diagnosing anemia in inflammatory bowel disease: beyond the established markers. J Crohns Colitis 5(5):381–391. https://doi.org/10.1016/j.crohns.2011.03.010

    Article  PubMed  Google Scholar 

  40. Krawisz JE, Sharon P, Stenson WF (1984) Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Assessment of inflammation in rat and hamster models. Gastroenterology 87(6):1344–1350

    Article  CAS  PubMed  Google Scholar 

  41. Arab HH, Al-Shorbagy MY, Abdallah DM, Nassar NN (2014) Telmisartan attenuates colon inflammation, oxidative perturbations and apoptosis in a rat model of experimental inflammatory bowel disease. PLoS One 9(5):e97193. https://doi.org/10.1371/journal.pone.0097193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Zizzo MG, Caldara G, Bellanca A, Nuzzo D, Di Carlo M, Serio R (2018) Preventive effects of guanosine on intestinal inflammation in 2, 4-dinitrobenzene sulfonic acid (DNBS)-induced colitis in rats. Inflammopharmacology 27(2):349–359. https://doi.org/10.1007/s10787-018-0506-9

    Article  CAS  PubMed  Google Scholar 

  43. Cario E (2010) Toll-like receptors in inflammatory bowel diseases: a decade later. Inflamm Bowel Dis 16(9):1583–1597. https://doi.org/10.1002/ibd.21282

    Article  PubMed  Google Scholar 

  44. Sproston NR, Ashworth JJ (2018) Role of C-reactive protein at sites of inflammation and infection. Front Immunol 9:754. https://doi.org/10.3389/fimmu.2018.00754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Finamore A, Ambra R, Nobili F et al (2018) Redox role of Lactobacillus casei shirota against the cellular damage induced by 2,2′-azobis (2-amidinopropane) dihydrochloride-induced oxidative and inflammatory stress in enterocytes-like epithelial cells. Front Immunol 9:1131. https://doi.org/10.3389/fimmu.2018.01131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Baghbani-Arani F, Asgary V, Hashemi A (2019) Cell-free extracts of Lactobacillus acidophilus and Lactobacillus delbrueckii display antiproliferative and antioxidant activities against HT-29 cell line. Nutr Cancer 11:1–10. https://doi.org/10.1080/01635581.2019.1685674

    Article  CAS  Google Scholar 

  47. Lee SI, Kim HS, Koo JM, Kim IH (2016) Lactobacillus acidophilus modulates inflammatory activity by regulating the TLR4 and NF-κB expression in porcine peripheral blood mononuclear cells after lipopolysaccharide challenge. Br J Nutr 115(4):567–575. https://doi.org/10.1017/S0007114515004857

    Article  CAS  PubMed  Google Scholar 

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This work was supported by K. B. Institute of Pharmaceutical Education and Research, Gandhinagar, Gujarat, India.

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Correspondence to Mehulkumar Ramanlal Chorawala.

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Chorawala, M.R., Chauhan, S., Patel, R. et al. Cell Wall Contents of Probiotics (Lactobacillus species) Protect Against Lipopolysaccharide (LPS)-Induced Murine Colitis by Limiting Immuno-inflammation and Oxidative Stress. Probiotics & Antimicro. Prot. 13, 1005–1017 (2021). https://doi.org/10.1007/s12602-020-09738-4

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