A recombinant Bifidobacterium bifidum BGN4 strain expressing the streptococcal superoxide dismutase gene ameliorates inflammatory bowel disease

Triantafillidis JK, Nasioulas G, Kosmidis PA. Colorectal cancer and inflammatory bowel disease: epidemiology, risk factors, mechanisms of carcinogenesis and prevention strategies. Anticancer Res. 2009;29:2727–37. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S. Expert consensus document: the international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014. https://doi.org/10.1038/nrgastro.2014.66. Matthes H, Krummenerl T, Giensch M, Wolff C, Schulze J. Clinical trial: probiotic treatment of acute distal ulcerative colitis with rectally administered Escherichia coli Nissle 1917 (EcN). BMC Complement Altern Med. 2010;10:1–8. Tursi A, Brandimarte G, Papa A, Giglio A, Elisei W, Giorgetti GM, Forti G, Morini S, Hassan C, Pistoia MA. Treatment of relapsing mild-to-moderate ulcerative colitis with the probiotic VSL# 3 as adjunctive to a standard pharmaceutical treatment: a double-blind, randomized, placebo-controlled study. Am J Gastroenterol. 2010;105:2218. D’Incà R, Barollo M, Scarpa M, Grillo AR, Brun P, Vettorato MG, Castagliuolo I, Sturniolo GC. Rectal administration of Lactobacillus casei DG modifies flora composition and toll-like receptor expression in colonic mucosa of patients with mild ulcerative colitis. Dig Dis Sci. 2011;56:1178–87. Wildt S, Nordgaard I, Hansen U, Brockmann E, Rumessen JJ. A randomised double-blind placebo-controlled trial with Lactobacillus acidophilus La-5 and Bifidobacterium animalis subsp. lactis BB-12 for maintenance of remission in ulcerative colitis. J Crohn’s Colitis. 2011;5:115–21. de Moreno de LeBlanc A, Del Carmen S, Chatel J-M, Miyoshi A, Azevedo V, Langella P, Bermúdez-Humarán LG, LeBlanc JG. Current review of genetically modified lactic acid bacteria for the prevention and treatment of colitis using murine models. Gastroenterol Res Pract. 2015. https://doi.org/10.1155/2015/146972. Gardlik R, Palffy R, Celec P. Recombinant probiotic therapy in experimental colitis in mice. Folia Biol. 2012;58:238. Steidler L, Neirynck S, Huyghebaert N, Snoeck V, Vermeire A, Goddeeris B, Cox E, Remon JP, Remaut E. Biological containment of genetically modified Lactococcus lactis for intestinal delivery of human interleukin 10. Nat Biotechnol. 2003;21:785–9. Larrosa M, González-Sarrías A, Yáñez-Gascón MJ, Selma MV, Azorín-Ortuño M, Toti S, Tomás-Barberán F, Dolara P, Espín JC. Anti-inflammatory properties of a pomegranate extract and its metabolite urolithin-A in a colitis rat model and the effect of colon inflammation on phenolic metabolism. J Nutr Biochem. 2010;21:717–25. Shiratora Y, Aoki S, Takada H, Kiriyama H, Ohto K, Hai K, Teraoka H, Matano S, Matsumoto K, Kamii K. Oxygen-derived free radical generating capacity of polymorphonuclear cells in patients with ulcerative colitis. Digestion. 1989;44:163–71. Hur SJ, Kang SH, Jung HS, Kim SC, Jeon HS, Kim IH, Lee JD. Review of natural products actions on cytokines in inflammatory bowel disease. Nutr Res. 2012;32:801–16. Lakhan SE, Kirchgessner A. Neuroinflammation in inflammatory bowel disease. J Neuroinflammation. 2010;7:1–12. Rochat T, Bermúdez-Humarán L, Gratadoux J-J, Fourage C, Hoebler C, Corthier G, Langella P. Anti-inflammatory effects of Lactobacillus casei BL23 producing or not a manganese-dependant catalase on DSS-induced colitis in mice. Microb Cell Fact. 2007;6:1–10. Bruno-Bárcena JM, Andrus JM, Libby SL, Klaenhammer TR, Hassan HM. Expression of a heterologous manganese superoxide dismutase gene in intestinal lactobacilli provides protection against hydrogen peroxide toxicity. Appl Environ Microbiol. 2004;70:4702–10. Carroll IM, Andrus JM, Bruno-Bárcena JM, Klaenhammer TR, Hassan HM, Threadgill DS. Anti-inflammatory properties of Lactobacillus gasseri expressing manganese superoxide dismutase using the interleukin 10-deficient mouse model of colitis. Am J Physiol Gastrointest Liver Physiol. 2007;293:G729–38. Han W, Mercenier A, Ait-Belgnaoui A, Pavan S, Lamine F, van Swam II, Kleerebezem M, Salvador-Cartier C, Hisbergues M, Bueno L. Improvement of an experimental colitis in rats by lactic acid bacteria producing superoxide dismutase. Inflamm Bowel Dis. 2006;12:1044–52. Watterlot L, Rochat T, Sokol H, Cherbuy C, Bouloufa I, Lefèvre F, Gratadoux J-J, Honvo-Hueto E, Chilmonczyk S, Blugeon S. 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. Saraiva M, Vieira P, O’garra A. Biology and therapeutic potential of interleukin-10. J Exp Med. 2020. https://doi.org/10.1084/jem.20190418. Del Carmen S, de LeBlanc AdM, Levit R, Azevedo V, Langella P, Bermúdez-Humarán LG, LeBlanc JG. Anti-cancer effect of lactic acid bacteria expressing antioxidant enzymes or IL-10 in a colorectal cancer mouse model. Int Immunopharmacol. 2017;42:122–9. Guimarães V, Innocentin S, Chatel J-M, Lefèvre F, Langella P, Azevedo V, Miyoshi A. A new plasmid vector for DNA delivery using lactococci. Genet Vaccines Ther. 2009;7:1–7. Steidler L, Hans W, Schotte L, Neirynck S, Obermeier F, Falk W, Fiers W, Remaut E. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science. 2000;289:1352–5. Kumar M, Yadav AK, Verma V, Singh B, Mal G, Nagpal R, Hemalatha R. Bioengineered probiotics as a new hope for health and diseases: an overview of potential and prospects. Future Microbiol. 2016;11:585–600. Mauras A, Chain F, Faucheux A, Ruffié P, Gontier S, Ryffel B, Butel M-J, Langella P, Bermúdez-Humarán LG, Waligora-Dupriet A-J. A new Bifidobacteria expression system (BEST) to produce and deliver interleukin-10 in Bifidobacterium bifidum. Front Microbiol. 2018;9:3075. Zuo F, Chen S, Marcotte H. Engineer probiotic bifidobacteria for food and biomedical applications—current status and future prospective. Biotechnol Adv. 2020. https://doi.org/10.1016/j.biotechadv.2020.107654. Lin Z, Ku S, Lim T, Park SY, Park MS, Ji GE, O’Brien K, Hwang KT. Antioxidant and anti-inflammatory properties of recombinant Bifidobacterium bifidum BGN4 expressing antioxidant enzymes. Microorganisms. 2021;9:595. Hong N, Ku S, Yuk K, Johnston TV, Ji GE, Park MS. Production of biologically active human interleukin-10 by Bifidobacterium bifidum BGN4. Microb Cell Fact. 2021;20:1–14. Araki Y, Mukaisyo K-I, Sugihara H, Fujiyama Y, Hattori T. Increased apoptosis and decreased proliferation of colonic epithelium in dextran sulfate sodium-induced colitis in mice. Oncol Rep. 2010;24:869–74. Xu X, Lin S, Yang Y, Gong X, Tong J, Li K, Li Y. Histological and ultrastructural changes of the colon in dextran sodium sulfate-induced mouse colitis. Exp Ther Med. 2020;20:1987–94. Boirivant M, Strober W. The mechanism of action of probiotics. Curr Opin Gastroenterol. 2007;23:679–92. Kruidenier La, Verspaget H. oxidative stress as a pathogenic factor in inflammatory bowel disease—radicals or ridiculous? Aliment Pharmacol Ther. 2002;16:1997–2015. Kruidenier L, van Meeteren ME, Kuiper I, Jaarsma D, Lamers CB, Zijlstra FJ, Verspaget HW. Attenuated mild colonic inflammation and improved survival from severe DSS-colitis of transgenic Cu/Zn-SOD mice. Free Radic Biol Med. 2003;34:753–65. Lih-Brody L, Powell SR, Collier KP, Reddy GM, Cerchia R, Kahn E, Weissman GS, Katz S, Floyd RA, McKinley MJ. Increased oxidative stress and decreased antioxidant defenses in mucosa of inflammatory bowel disease. Dig Dis Sci. 1996;41:2078–86. Del Carmen S, de Moreno de LeBlanc A, Martin R, Chain F, Langella P, Bermúdez-Humarán LG, LeBlanc JG. Genetically engineered immunomodulatory Streptococcus thermophilus strains producing antioxidant enzymes exhibit enhanced anti-inflammatory activities. Appl Environ Microbiol. 2014;80:869–77. LeBlanc JG, del Carmen S, Miyoshi A, Azevedo V, Sesma F, Langella P, Bermúdez-Humarán LG, Watterlot L, Perdigon G, de LeBlanc AdM. Use of superoxide dismutase and catalase producing lactic acid bacteria in TNBS induced Crohn’s disease in mice. J Biotechnol. 2011;151:287–93. Islam M, Murata T, Fujisawa M, Nagasaka R, Ushio H, Bari A, Hori M, Ozaki H. Anti-inflammatory effects of phytosteryl ferulates in colitis induced by dextran sulphate sodium in mice. Br J Pharmacol. 2008;154:812–24. Liu X, Wang J. Anti-inflammatory effects of iridoid glycosides fraction of Folium syringae leaves on TNBS-induced colitis in rats. J Ethnopharmacol. 2011;133:780–7. Sanchez-Muñoz F, Dominguez-Lopez A, Yamamoto-Furusho JK. Role of cytokines in inflammatory bowel disease. World J Gastroenterol. 2008;14:4280. Cho E-j, Shin J-S, Noh Y-S, Cho Y-W, Hong S-J, Park J-H, Lee JY, Lee J-Y, Lee K-T. Anti-inflammatory effects of methanol extract of Patrinia scabiosaefolia in mice with ulcerative colitis. J Ethnopharmacol. 2011;136:428–35. Kwon KH, Murakami A, Hayashi R, Ohigashi H. Interleukin-1β targets interleukin-6 in progressing dextran sulfate sodium-induced experimental colitis. Biochem Biophys Res Commun. 2005;337:647–54. Kühn R, Löhler J, Rennick D, Rajewsky K, Müller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993;75:263–74. Bermúdez-Humarán LG, Motta J-P, Aubry C, Kharrat P, Rous-Martin L, Sallenave J-M, Deraison C, Vergnolle N, Langella P. Serine protease inhibitors protect better than IL-10 and TGF-β anti-inflammatory cytokines against mouse colitis when delivered by recombinant lactococci. Microb Cell Fact. 2015;14:1–11. Fedorak RN, Gangl A, Elson CO, Rutgeerts P, Schreiber S, Wild G, Hanauer SB, Kilian A, Cohard M, LeBeaut A. Recombinant human interleukin 10 in the treatment of patients with mild to moderately active Crohn’s disease. Gastroenterology. 2000;119:1473–82. Moore KW, de Waal Malefyt R, Coffman RL, O’Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol. 2001;19:683–765. Groux H, O’Garra A, Bigler M, Rouleau M, Antonenko S, De Vries JE, Roncarolo MG. A CD4+T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature. 1997;389:737–42. Cocconcelli PS, Cattivelli D, Gazzola S. Gene transfer of vancomycin and tetracycline resistances among Enterococcus faecalis during cheese and sausage fermentations. Int J Food Microbiol. 2003;88:315–23. Devirgiliis C, Zinno P, Perozzi G. Update on antibiotic resistance in foodborne Lactobacillus and Lactococcus species. Front Microbiol. 2013;4:301. Moubareck C, Gavini F, Vaugien L, Butel M, Doucet-Populaire F. Antimicrobial susceptibility of bifidobacteria. J Antimicrob Chemother. 2005;55:38–44. Ku S, Park MS, Ji GE, You HJ. Review on Bifidobacterium bifidum BGN4: functionality and nutraceutical applications as a probiotic microorganism. Int J Mol Sci. 2016;17:1544. Ku S-M, You H-J, Ji G-E. Enhancement of anti-tumorigenic polysaccharide production, adhesion, and branch formation of Bifidobacterium bifidum BGN4 by phytic acid. Food Sci Biotechnol. 2009;18:749–54.