Skip to main content
Log in

Expression of catalase in Lactobacillus fermentum and evaluation of its anti-oxidative properties in a dextran sodium sulfate induced mouse colitis model

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Lactic acid bacteria are generally sensitive to hydrogen peroxide (H2O2). Lactobacillus plantarum ATCC14431 is one of the few lactic acid bacteria able to degrade H2O2 through the action of a manganese-dependent catalase (containing the katA gene). However, it is not a natural inhabitant of the intestinal tract and its bio-efficacy and survival in the gastrointestinal tract have never been tested. In this study, we successfully expressed the katA gene from L. plantarum ATCC14431 in L. fermentum I5007 and the recombinant L. fermentum exhibited almost 20-fold higher catalase activity than the empty vector control. The anti-oxidative properties of this catalase-producing L. fermentum were evaluated using a dextran sodium sulphate (DSS) induced colitis mice model. Compared with the control, mice receiving DSS alone had increased diarrhea and mucosa histological scores (P < 0.05), as well as lipid peroxidation (P < 0.05), myeloperoxidase (P < 0.05), and active NF-κB in colonic tissue (P < 0.05). Similar to vitamin E, treatment with recombinant L. fermentum mitigate these effects accompanied by a improvement in mucosa histological scores in the proximal colon (P < 0.05) and decreased lipid peroxidation (P < 0.05), myeloperoxidase (P < 0.05) and active NF-κB in colonic tissue (P < 0.05). In conclusion, the expression of catalase in L. fermentum increased its ability to survive when exposed to aerated environment in vitro and conferred the anti-oxidative and anti-inflammatory effects in the DSS induced colitis model.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aukrust TW, Brurberg MB, Nes IF (1995) Transformation of Lactobacillus by electroporation. Methods Mol Biol 47:201–208

    CAS  Google Scholar 

  • Bhattacharyya S, Dudeja PK, Tobacman JK (2009) ROS, Hsp27, and IKKbeta mediate dextran sodium sulfate (DSS) activation of IkappaBa, NFkappaB, and IL-8. Inflamm Bowel Dis 15(5):673–683

    Article  Google Scholar 

  • Bowie AG, Moynagh PN, O’Neill LA (1997) Lipid peroxidation is involved in the activation of NF-kappaB by tumor necrosis factor but not interleukin-1 in the human endothelial cell line ECV304. Lack of involvement of H2O2 in NF-kappaB activation by either cytokine in both primary and transformed endothelial cells. J Biol Chem 272(41):25941–25950

    Article  CAS  Google Scholar 

  • Calfee-Mason KG, Spear BT, Glauert HP (2004) Effects of vitamin E on the NF-kappaB pathway in rats treated with the peroxisome proliferator, ciprofibrate. Toxicol Appl Pharmacol 199(1):1–9

    Article  CAS  Google Scholar 

  • Carrier J, Aghdassi E, Cullen J, Allard JP (2002) Iron supplementation increases disease activity and vitamin E ameliorates the effect in rats with dextran sulfate sodium-induced colitis. J Nutr 132(10):3146–3150

    CAS  Google Scholar 

  • Carroll IM, Andrus JM, Bruno-Barcena JM, Klaenhammer TR, Hassan HM, Threadgill DS (2007) 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 293(4):G729–G738

    Article  CAS  Google Scholar 

  • de Moreno de LeBlanc A, LeBlanc JG, Perdigon G, Miyoshi A, Langella P, Azevedo V, Sesma F (2008) Oral administration of a catalase-producing Lactococcus lactis can prevent a chemically induced colon cancer in mice. J Med Microbiol 57(Pt 1):100–105

    Google Scholar 

  • de Vries W, Stouthamer AH (1969) Factors determining the degree of anaerobiosis of Bifidobacterium strains. Arch Microbiol 65(3):275–287

    Google Scholar 

  • Fons M, HégéT Ladiré M, Raibaud P, Ducluzeau R, Maguin E (1997) Isolation and characterization of a plasmid from Lactobacillus fermentum conferring erythromycin resistance. Plasmid 37(3):199–203

    Article  CAS  Google Scholar 

  • Gaudier E, Michel C, Segain JP, Cherbut C, Hoebler C (2005) The VSL# 3 probiotic mixture modifies microflora but does not heal chronic dextran-sodium sulfate-induced colitis or reinforce the mucus barrier in mice. J Nutr 135(12):2753–2761

    CAS  Google Scholar 

  • Gill HS, Rutherfurd KJ, Prasad J, Gopal PK (2000) Enhancement of natural and acquired immunity by Lactobacillus rhamnosus (HN001), Lactobacillus acidophilus (HN017) and Bifidobacterium lactis (HN019). Br J Nutr 83(2):167–176

    Article  CAS  Google Scholar 

  • Gonzalez R, Sanchez de Medina F, Galvez J, Rodriguez-Cabezas ME, Duarte J, Zarzuelo A (2001) Dietary vitamin E supplementation protects the rat large intestine from experimental inflammation. Int J Vitam Nutr Res 71(4):243–250

    Article  CAS  Google Scholar 

  • Hartmann G, Bidlingmaier C, Siegmund B, Albrich S, Schulze J, Tschoep K, Eigler A, Lehr HA, Endres S (2000) Specific type IV phosphodiesterase inhibitor rolipram mitigates experimental colitis in mice. J Pharmacol Exp Ther 292(1):22–30

    CAS  Google Scholar 

  • He J, Sakaguchi K, Suzuki T (2012) Acquired tolerance to oxidative stress in Bifidobacterium longum 105-A via expression of a catalase gene. Appl Environ Microbiol 78(8):2988–2990

    Article  CAS  Google Scholar 

  • Horton RM, Hunt HD, Ho SN, Pullen JK, Pease LR (1989) Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77(1):61–68

    Article  CAS  Google Scholar 

  • Huang CH, Qiao SY, Li DF, Piao XS, Ren JP (2004) Effects of Lactobacilli on the performance, diarrhea incidence, VFA concentration and gastrointestinal microbial flora of weaning pigs. Asian Austral J Anim 17(3):401–409

    Google Scholar 

  • Isolauri E, Juntunen M, Rautanen T, Sillanaukee P, Koivula T (1991) A human Lactobacillus strain (Lactobacillus casei sp strain GG) promotes recovery from acute diarrhea in children. Pediatrics 88(1):90–97

    CAS  Google Scholar 

  • Kawasaki S, Mimura T, Satoh T, Takeda K, Niimura Y (2006) Response of the microaerophilic Bifidobacterium species, B. boum and B. thermophilum, to oxygen. Appl Environ Microbiol 72(10):6854–6858

    Article  CAS  Google Scholar 

  • Kono Y, Fridovich I (1983) Isolation and characterization of the pseudocatalase of Lactobacillus plantarum. J Biol Chem 258(10):6015–6019

    CAS  Google Scholar 

  • Kruidenier L, Verspaget HW (2002) Review article: oxidative stress as a pathogenic factor in inflammatory bowel disease-radicals or ridiculous? Aliment Pharmacol Ther 16(12):1997–2015

    Article  CAS  Google Scholar 

  • Laroui H, Ingersoll SA, Liu HC, Baker MT, Ayyadurai S, Charania MA, Laroui F, Yan Y, Sitaraman SV, Merlin D (2012) Dextran sodium sulfate (DSS) induces colitis in mice by forming nano-lipocomplexes with medium-chain-length fatty acids in the colon. PLoS ONE 7(3):e32084

    Article  CAS  Google Scholar 

  • LeBlanc JG, del Carmen S, Miyoshi A, Azevedo V, Sesma F, Langella P, Bermudez-Humaran LG, Watterlot L, Perdigon G, de Moreno de LeBlanc A (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

    Article  CAS  Google Scholar 

  • Lee IA, Bae EA, Lee JH, Lee H, Ahn YT, Huh CS, Kim DH (2010) Bifidobacterium longum HY8004 attenuates TNBS-induced colitis by inhibiting lipid peroxidation in mice. Inflamm Res 59(5):359–368

    Article  CAS  Google Scholar 

  • Li N, Karin M (1999) Is NF-kappaB the sensor of oxidative stress? FASEB J 13(10):1137–1143

    CAS  Google Scholar 

  • Li XJ, Yue LY, Guan XF, Qiao SY (2008) The adhesion of putative probiotic lactobacilli to cultured epithelial cells and porcine intestinal mucus. J Appl Microbiol 104(4):1082–1091

    Article  CAS  Google Scholar 

  • Lih-Brody L, Powell SR, Collier KP, Reddy GM, Cerchia R, Kahn E, Weissman GS, Katz S, Floyd RA, McKinley MJ, Fisher SE, Mullin GE (1996) Increased oxidative stress and decreased antioxidant defenses in mucosa of inflammatory bowel disease. Dig Dis Sci 41(10):2078–2086

    Article  CAS  Google Scholar 

  • Lindgren SE, Dobrogosz WJ (1990) Antagonistic activities of lactic acid bacteria in food and feed fermentations. FEMS Microbiol Lett 87(1–2):149–163

    Article  CAS  Google Scholar 

  • Pigeolet E, Corbisier P, Houbion A, Lambert D, Michiels C, Raes M, Zachary MD, Remacle J (1990) Glutathione peroxidase, superoxide dismutase, and catalase inactivation by peroxides and oxygen derived free radicals. Mech Ageing Dev 51(3):283–297

    Article  CAS  Google Scholar 

  • Raza S, Graham SM, Allen SJ, Sultana S, Cuevas L, Hart CA (1995) Lactobacillus GG promotes recovery from acute nonbloody diarrhea in Pakistan. Pediatr Infect Dis J 14(2):107–111

    Article  CAS  Google Scholar 

  • Rochat T, Gratadoux JJ, Gruss A, Corthier G, Maguin E, Langella P, van de Guchte M (2006) Production of a heterologous nonheme catalase by Lactobacillus casei: an efficient tool for removal of H2O2 and protection of Lactobacillus bulgaricus from oxidative stress in milk. Appl Environ Microbiol 72(8):5143–5149

    Article  CAS  Google Scholar 

  • Rochat T, Bermudez-Humaran L, Gratadoux JJ, Fourage C, Hoebler C, Corthier G, Langella P (2007) Anti-inflammatory effects of Lactobacillus casei BL23 producing or not a manganese-dependant catalase on DSS-induced colitis in mice. Microb Cell Fact 6:22

    Article  Google Scholar 

  • Shimizu T, Igarashi J, Ohtuka Y, Oguchi S, Kaneko K, Yamashiro Y (2001) Effects of n-3 polyunsaturated fatty acids and vitamin E on colonic mucosal leukotriene generation, lipid peroxidation, and microcirculation in rats with experimental colitis. Digestion 63(1):49–54

    Article  CAS  Google Scholar 

  • Sinha AK (1972) Colorimetric assay of catalase. Anal Biochem 47(2):389–394

    Article  CAS  Google Scholar 

  • van de Guchte M, Ehrlich SD, Maguin E (2001) Production of growth-inhibiting factors by Lactobacillus delbrueckii. J Appl Microbiol 91(1):147–153

    Article  Google Scholar 

  • Wang A, Yu H, Gao X, Li X, Qiao S (2009) Influence of Lactobacillus fermentum I5007 on the intestinal and systemic immune responses of healthy and E. coli challenged piglets. Antonie Van Leeuwenhoek 96(1):89–98

    Article  CAS  Google Scholar 

  • Watterlot L, Rochat T, Sokol H, Cherbuy C, Bouloufa I, Lefevre F, Gratadoux JJ, Honvo-Hueto E, Chilmonczyk S, Blugeon S, Corthier G, Langella P, Bermudez-Humaran LG (2010) Intragastric administration of a superoxide dismutase-producing recombinant Lactobacillus casei BL23 strain attenuates DSS colitis in mice. Int J Food Microbiol 144(1):35–41

    Article  CAS  Google Scholar 

  • Yoshida Y, Umeno A, Shichiri M (2013) Lipid peroxidation biomarkers for evaluating oxidative stress and assessing antioxidant capacity in vivo. J Clin Biochem Nutr 52(1):9–16

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China PR (NO. 30930066) and National Key Basic Research Program of China (973 Program) 2012CB124702.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shiyan Qiao.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 32 kb)

11274_2013_1395_MOESM2_ESM.docx

Supplementary material 2 The capability of three different promoters to drive green fluorescent protein expression (DOCX 191 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, J., Liu, H., Wang, Q. et al. Expression of catalase in Lactobacillus fermentum and evaluation of its anti-oxidative properties in a dextran sodium sulfate induced mouse colitis model. World J Microbiol Biotechnol 29, 2293–2301 (2013). https://doi.org/10.1007/s11274-013-1395-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11274-013-1395-0

Keywords

Navigation