Oral administration of Lactococcus lactis expressing recombinant 15-lipoxygenase-1 (15 LOX-1) modulates chemically induced colitis in mice
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Abstract
Abstract
Background: Inflammatory bowel disease (IBD), such as Crohn’s disease and ulcerative colitis, are characterized by extensive inflammation due to dysregulation of the innate and adaptive immune system whose exact etiology is not yet completely understood. Currently there is no cure for IBD, thus the search for new molecules capable of controlling IBD and their delivery to the site of inflammation are the goal of many researchers. The aim of this work was to evaluate the anti-inflammatory effect of the oral administration of a Lactococcus (L.) lactis strain producing 15-lipoxygenase-1 (15-LOX-1) using a dextran sodium sulfate (DSS)-induced IBD mouse model. Methods: The anti-inflammatory strain L. lactislacti NCDO 2118 was modified to produce active 15-LOX-1 and tested in in a DSS induced IBD mouse model. Results: This 15-LOX-1 producing L. lactis was effective in the prevention of the intestinal damage associated to inflammatory bowel disease in a murine model and decreased pro-inflammatory cytokines such as IFN-γ and IL-4 while increasing the anti-inflammatory cytokine IL-10. L. lactis NCDO 2118 acts not just as a tool to delivery 15-LOX-1 in the inflamed gut mucosa but still retains its anti-inflammatory effects. Conclusions: This strain could be used in novel adjunct IBD treatment protocols.
Article Details
How to Cite
CARVALHO, Rodrigo Dias de Oliveira et al.
Oral administration of Lactococcus lactis expressing recombinant 15-lipoxygenase-1 (15 LOX-1) modulates chemically induced colitis in mice.
Medical Research Archives, [S.l.], v. 4, n. 7, nov. 2016.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/612>. Date accessed: 04 dec. 2024.
Keywords
colitis; inflammation; lactic acid bacteria; Lactococcus lactis; lipoxygenase; imunomodulation
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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Uderhardt S, Herrmann M, Oskolkova OV, Aschermann S, Bicker W, Ipseiz N, Sarter K, Frey B, Rothe T, Voll R, et al: 12/15-lipoxygenase orchestrates the clearance of apoptotic cells and maintains immunologic tolerance. Immunity 2012, 36:834-846.
Uderhardt S, Kronke G: 12/15-lipoxygenase during the regulation of inflammation, immunity, and self-tolerance. Journal of molecular medicine 2012, 90:1247-1256.
Diniz-Luerce T, Gomes-Santos AC, Santos Rocha C, Moreira TG, Cruz DN, Lemos L, Sousa AL, Bastos Pereira V, Azevedo M, Moraes K, et al: Anti-inflammatory effects of Lactococcus lactis NCDO 2118 during the remission period of chemically-induced colitis. Gut Pathogens 2014.
Stevceva L, Pavli P, Husband AJ, Doe WF: The inflammatory infiltrate in the acute stage of the dextran sulphate sodium induced colitis: B cell response differs depending on the percentage of DSS used to induce it. BMC Clin Pathol 2001, 1:3.
Alex P, Zachos NC, Nguyen T, Gonzales L, Chen TE, Conklin LS, Centola M, Li X: Distinct cytokine patterns identified from multiplex profiles of murine DSS and TNBS-induced colitis. Inflammatory bowel diseases 2009, 15:341-352.
Dieleman LA, Palmen MJ, Akol H, Bloemena E, Pena AS, Meuwissen SG, Van Rees EP: Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines. Clinical and experimental immunology 1998, 114:385-391.
McCafferty DM, Sihota E, Muscara M, Wallace JL, Sharkey KA, Kubes P: Spontaneously developing chronic colitis in IL-10/iNOS double-deficient mice. American journal of physiology Gastrointestinal and liver physiology 2000, 279:G90-99.
Maron R, Hancock WW, Slavin A, Hattori M, Kuchroo V, Weiner HL: Genetic susceptibility or resistance to autoimmune encephalomyelitis in MHC congenic mice is associated with differential production of pro- and anti-inflammatory cytokines. International immunology 1999, 11:1573-1580.
Sartor RB: Microbial and dietary factors in the pathogenesis of chronic, immune-mediated intestinal inflammation. Advances in experimental medicine and biology 2006, 579:35-54.
Strober W, Fuss I, Mannon P: The fundamental basis of inflammatory bowel disease. The Journal of clinical investigation 2007, 117:514-521.
Marteau P: Living drugs for gastrointestinal diseases: the case for probiotics. Digestive diseases 2006, 24:137-147.
Nielsen OH, Munck LK: Drug insight: aminosalicylates for the treatment of IBD. Nature clinical practice Gastroenterology & hepatology 2007, 4:160-170.
de Moreno de Leblanc A, Del Carmen S, Zurita-Turk M, Santos Rocha C, van de Guchte M, Azevedo V, Miyoshi A, Leblanc JG: Importance of IL-10 modulation by probiotic microorganisms in gastrointestinal inflammatory diseases. ISRN gastroenterology 2011, 2011:892971.
FAO/WHO: Evaluation of health and nutritional properties of powder milk and live lactic acid bacteria. Food and Agriculture Organization of the United Nations and World Health Organization Expert Consultation Report 2001, Available from http://www.fao.org/ag/agn/agns/micro_probiotics_en.asp.
Hormannsperger G, Haller D: Molecular crosstalk of probiotic bacteria with the intestinal immune system: clinical relevance in the context of inflammatory bowel disease. International journal of medical microbiology : IJMM 2010, 300:63-73.
Duwat P, Cesselin B, Sourice S, Gruss A: Lactococcus lactis, a bacterial model for stress responses and survival. International journal of food microbiology 2000, 55:83-86.
Bolotin A, Wincker P, Mauger S, Jaillon O, Malarme K, Weissenbach J, Ehrlich SD, Sorokin A: The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome research 2001, 11:731-753.
Chopin A, Chopin MC, Moillo-Batt A, Langella P: Two plasmid-determined restriction and modification systems in Streptococcus lactis. Plasmid 1984, 11:260-263.
Pontes DS, de Azevedo MS, Chatel JM, Langella P, Azevedo V, Miyoshi A: Lactococcus lactis as a live vector: heterologous protein production and DNA delivery systems. Protein expression and purification 2011, 79:165-175.
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, 289:1352-1355.
Han W, Mercenier A, Ait-Belgnaoui A, Pavan S, Lamine F, van S, II, Kleerebezem M, Salvador-Cartier C, Hisbergues M, Bueno L, et al: Improvement of an experimental colitis in rats by lactic acid bacteria producing superoxide dismutase. Inflamm Bowel Dis 2006, 12:1044-1052.
Motta JP, Bermudez-Humaran LG, Deraison C, Martin L, Rolland C, Rousset P, Boue J, Dietrich G, Chapman K, Kharrat P, et al: Food-grade bacteria expressing elafin protect against inflammation and restore colon homeostasis. Science translational medicine 2012, 4:158ra144.
Brash AR, Boeglin WE, Chang MS: Discovery of a second 15S-lipoxygenase in humans. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:6148-6152.
Lee YW, Kuhn H, Kaiser S, Hennig B, Daugherty A, Toborek M: Interleukin 4 induces transcription of the 15-lipoxygenase I gene in human endothelial cells. Journal of lipid research 2001, 42:783-791.
Mangino MJ, Brounts L, Harms B, Heise C: Lipoxin biosynthesis in inflammatory bowel disease. Prostaglandins & other lipid mediators 2006, 79:84-92.
Shureiqi I, Chen D, Day RS, Zuo X, Hochman FL, Ross WA, Cole RA, Moy O, Morris JS, Xiao L, et al: Profiling lipoxygenase metabolism in specific steps of colorectal tumorigenesis. Cancer prevention research 2010, 3:829-838.
Ligumsky M, Simon PL, Karmeli F, Rachmilewitz D: Role of interleukin 1 in inflammatory bowel disease--enhanced production during active disease. Gut 1990, 31:686-689.
Zuo X, Wu Y, Morris JS, Stimmel JB, Leesnitzer LM, Fischer SM, Lippman SM, Shureiqi I: Oxidative metabolism of linoleic acid modulates PPAR-beta/delta suppression of PPAR-gamma activity. Oncogene 2006, 25:1225-1241.
Dubuquoy L, Rousseaux C, Thuru X, Peyrin-Biroulet L, Romano O, Chavatte P, Chamaillard M, Desreumaux P: PPARgamma as a new therapeutic target in inflammatory bowel diseases. Gut 2006, 55:1341-1349.
Altmann R, Hausmann M, Spottl T, Gruber M, Bull AW, Menzel K, Vogl D, Herfarth H, Scholmerich J, Falk W, Rogler G: 13-Oxo-ODE is an endogenous ligand for PPARgamma in human colonic epithelial cells. Biochemical pharmacology 2007, 74:612-622.
Lindley AR, Crapster-Pregont M, Liu Y, Kuperman DA: 12/15-lipoxygenase is an interleukin-13 and interferon-gamma counterregulated-mediator of allergic airway inflammation. Mediators of inflammation 2010, 2010.
Kundumani-Sridharan V, Dyukova E, Hansen DE, 3rd, Rao GN: 12/15-Lipoxygenase mediates high-fat diet-induced endothelial tight junction disruption and monocyte transmigration: a new role for 15(S)-hydroxyeicosatetraenoic acid in endothelial cell dysfunction. The Journal of biological chemistry 2013, 288:15830-15842.
Uderhardt S, Herrmann M, Oskolkova OV, Aschermann S, Bicker W, Ipseiz N, Sarter K, Frey B, Rothe T, Voll R, et al: 12/15-lipoxygenase orchestrates the clearance of apoptotic cells and maintains immunologic tolerance. Immunity 2012, 36:834-846.
Uderhardt S, Kronke G: 12/15-lipoxygenase during the regulation of inflammation, immunity, and self-tolerance. Journal of molecular medicine 2012, 90:1247-1256.
Diniz-Luerce T, Gomes-Santos AC, Santos Rocha C, Moreira TG, Cruz DN, Lemos L, Sousa AL, Bastos Pereira V, Azevedo M, Moraes K, et al: Anti-inflammatory effects of Lactococcus lactis NCDO 2118 during the remission period of chemically-induced colitis. Gut Pathogens 2014.
Stevceva L, Pavli P, Husband AJ, Doe WF: The inflammatory infiltrate in the acute stage of the dextran sulphate sodium induced colitis: B cell response differs depending on the percentage of DSS used to induce it. BMC Clin Pathol 2001, 1:3.
Alex P, Zachos NC, Nguyen T, Gonzales L, Chen TE, Conklin LS, Centola M, Li X: Distinct cytokine patterns identified from multiplex profiles of murine DSS and TNBS-induced colitis. Inflammatory bowel diseases 2009, 15:341-352.
Dieleman LA, Palmen MJ, Akol H, Bloemena E, Pena AS, Meuwissen SG, Van Rees EP: Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines. Clinical and experimental immunology 1998, 114:385-391.
McCafferty DM, Sihota E, Muscara M, Wallace JL, Sharkey KA, Kubes P: Spontaneously developing chronic colitis in IL-10/iNOS double-deficient mice. American journal of physiology Gastrointestinal and liver physiology 2000, 279:G90-99.
Maron R, Hancock WW, Slavin A, Hattori M, Kuchroo V, Weiner HL: Genetic susceptibility or resistance to autoimmune encephalomyelitis in MHC congenic mice is associated with differential production of pro- and anti-inflammatory cytokines. International immunology 1999, 11:1573-1580.