Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2016, Article ID 1340903, 10 pages
http://dx.doi.org/10.1155/2016/1340903
Research Article

The Influence of Probiotic Lactobacillus casei in Combination with Prebiotic Inulin on the Antioxidant Capacity of Human Plasma

Department of Immunopathology, Faculty of Biomedical Sciences and Postgraduate Training, Medical University of Lodz, Ulica Zeligowskiego 7/9, 90-752 Lodz, Poland

Received 14 September 2015; Revised 5 February 2016; Accepted 11 February 2016

Academic Editor: Vasantha Rupasinghe

Copyright © 2016 Paulina Kleniewska et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. D. Ray, B.-W. Huang, and Y. Tsuji, “Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling,” Cellular Signalling, vol. 24, no. 5, pp. 981–990, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. J. E. Klaunig, Z. Wang, X. Pu, and S. Zhou, “Oxidative stress and oxidative damage in chemical carcinogenesis,” Toxicology and Applied Pharmacology, vol. 254, no. 2, pp. 86–99, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Valko, C. J. Rhodes, J. Moncol, M. Izakovic, and M. Mazur, “Free radicals, metals and antioxidants in oxidative stress-induced cancer,” Chemico-Biological Interactions, vol. 160, no. 1, pp. 1–40, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. P. Song and M. H. Zou, “Roles of reactive oxygen species in physiology and pathology,” in Atherosclerosis: Risks, Mechanisms, and Therapies, H. Wang and C. Patterson, Eds., pp. 379–392, John Wiley & Sons, Hoboken, NJ, USA, 2015. View at Google Scholar
  5. K. Apel and H. Hirt, “Reactive oxygen species: metabolism, oxidative stress, and signal transduction,” Annual Review of Plant Biology, vol. 55, pp. 373–399, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. T. Fukai and M. Ushio-Fukai, “Superoxide dismutases: role in redox signaling, vascular function, and diseases,” Antioxidants and Redox Signaling, vol. 15, no. 6, pp. 1583–1606, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. I. N. Zelko, T. J. Mariani, and R. J. Folz, “Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression,” Free Radical Biology and Medicine, vol. 33, no. 3, pp. 337–349, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Chen, P. Sayana, X. Zhang, and W. Le, “Genetics of amyotrophic lateral sclerosis: an update,” Molecular Neurodegeneration, vol. 28, no. 8, pp. 1–15, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Miriyala, I. Spasojevic, A. Tovmasyan et al., “Manganese superoxide dismutase, MnSOD and its mimics,” Biochimica et Biophysica Acta (BBA)—Molecular Basis of Disease, vol. 1822, no. 5, pp. 794–814, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. C. D. Putnam, A. S. Arvai, Y. Bourne, and J. A. Tainer, “Active and inhibited human catalase structures: ligand and NADPH binding and catalytic mechanism,” Journal of Molecular Biology, vol. 296, no. 1, pp. 295–309, 2000. View at Publisher · View at Google Scholar · View at Scopus
  11. P. Chelikani, I. Fita, and P. C. Loewen, “Diversity of structures and properties among catalases,” Cellular and Molecular Life Sciences, vol. 61, no. 2, pp. 192–208, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. R. Francik, M. Krośniak, I. Sanocka, H. Bartoń, T. Hebda, and S. Francik, “Aronia melanocarpa treatment and antioxidant status in selected tissues in wistar rats,” BioMed Research International, vol. 2014, Article ID 457085, 9 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. E. Lubos, J. Loscalzo, and D. E. Handy, “Glutathione peroxidase-1 in health and disease: from molecular mechanisms to therapeutic opportunities,” Antioxidants and Redox Signaling, vol. 15, no. 7, pp. 1957–1997, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. G. R. Gibson and M. B. Roberfroid, “Dietary modulation of the human colonic microbiota. Introducing the concept of prebiotics,” Journal of Nutrition, vol. 125, no. 6, pp. 1401–1412, 1995. View at Google Scholar · View at Scopus
  15. B. Poljsak, “Strategies for reducing or preventing the generation of oxidative stress,” Oxidative Medicine and Cellular Longevity, vol. 2011, Article ID 194586, 15 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. B. M. Hybertson, B. Gao, S. K. Bose, and J. M. McCord, “Oxidative stress in health and disease: the therapeutic potential of Nrf2 activation,” Molecular Aspects of Medicine, vol. 32, no. 4–6, pp. 234–246, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. I. F. F. Benzie and J. J. Strain, “The ferric reducing ability of plasma (FRAP) as a measure of ‘antioxidant power’: the FRAP assay,” Analytical Biochemistry, vol. 239, no. 1, pp. 70–76, 1996. View at Publisher · View at Google Scholar · View at Scopus
  18. https://www.caymanchem.com/pdfs/707002.pdf.
  19. https://www.caymanchem.com/pdfs/706002.pdf.
  20. https://www.caymanchem.com/pdfs/703102.pdf.
  21. D. Martarelli, M. C. Verdenelli, S. Scuri et al., “Effect of a probiotic intake on oxidant and antioxidant parameters in plasma of athletes during intense exercise training,” Current Microbiology, vol. 62, no. 6, pp. 1689–1696, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. H. An, H. Zhou, Y. Huang et al., “High-level expression of heme-dependent catalase gene katA from Lactobacillus sakei protects Lactobacillus rhamnosus from oxidative stress,” Molecular Biotechnology, vol. 45, no. 2, pp. 155–160, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. P. Hütt, H. Andreson, T. Kullisaar et al., “Effects of a synbiotic product on blood antioxidative activity in subjects colonized with Helicobacter pylori,” Letters in Applied Microbiology, vol. 48, no. 6, pp. 797–800, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Kullisaar, E. Songisepp, M. Mikelsaar, K. Zilmer, T. Vihalemm, and M. Zilmer, “Antioxidative probiotic fermented goats' milk decreases oxidative stress-mediated atherogenicity in human subjects,” British Journal of Nutrition, vol. 90, no. 2, pp. 449–456, 2003. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Mikelsaar and M. Zilmer, “Lactobacillus fermentum ME-3—an antimicrobial and antioxidative probiotic,” Microbial Ecology in Health and Disease, vol. 21, no. 1, pp. 1–27, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. E. Songisepp, J. Kals, T. Kullisaar et al., “Evaluation of the functional efficacy of an antioxidative probiotic in healthy volunteers,” Nutrition Journal, vol. 4, article 22, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. M. A. Uskova and L. V. Kravchenko, “Antioxidant properties of lactic acid bacteria—probiotic and yogurt strains,” Voprosy Pitaniia, vol. 78, no. 2, pp. 18–23, 2009. View at Google Scholar · View at Scopus
  28. A. Amaretti, M. di Nunzio, A. Pompei, S. Raimondi, M. Rossi, and A. Bordoni, “Antioxidant properties of potentially probiotic bacteria: in vitro and in vivo activities,” Applied Microbiology and Biotechnology, vol. 97, no. 2, pp. 809–817, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. A. S. Hathout, S. R. Mohamed, A. A. El-Nekeety, N. S. Hassan, S. E. Aly, and M. A. Abdel-Wahhab, “Ability of Lactobacillus casei and Lactobacillus reuteri to protect against oxidative stress in rats fed aflatoxins-contaminated diet,” Toxicon, vol. 58, no. 2, pp. 179–186, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Gagnon, P. Savard, A. Rivière, G. Lapointe, and D. Roy, “Bioaccessible antioxidants in milk fermented by Bifidobacterium longum subsp. longum strains,” BioMed Research International, vol. 2015, Article ID 169381, 12 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  31. Q. Shen, N. Shang, and P. Li, “In vitro and in vivo antioxidant activity of bifidobacterium animalis 01 isolated from centenarians,” Current Microbiology, vol. 62, no. 4, pp. 1097–1103, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Chamari, A. Djazayery, M. Jalali, H. Sadrzadeh Yeganeh, S. Hosseini, and R. Heshmat, “The effect of daily consumption of probiotic and conventional yogurt on some oxidative stress factors in plasma of young healthy women,” ARYA Atherosclerosis Journal, vol. 4, no. 4, pp. 175–179, 2008. View at Google Scholar
  33. X. Shen, D. Yi, X. Ni et al., “Effects of lactobacillus plantarum on production performance, immune characteristics, antioxidant status, and intestinal microflora of bursin-immunized broilers,” Canadian Journal of Microbiology, vol. 60, no. 4, pp. 193–202, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Yadav, S. Jain, and P. R. Sinha, “Oral administration of dahi containing probiotic Lactobacillus acidophilus and Lactobacillus casei delayed the progression of streptozotocin-induced diabetes in rats,” Journal of Dairy Research, vol. 75, no. 2, pp. 189–195, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Rajpal and V. K. Kansal, “Probiotic Dahi containing Lactobacillus acidophilus and Bifidobacterium bifidum stimulates antioxidant enzyme pathways in rats,” Milchwissenschaft, vol. 64, no. 3, pp. 287–290, 2009. View at Google Scholar · View at Scopus
  36. T. Balog, S. Sobočanec, V. Šverko et al., “The influence of season on oxidant-antioxidant status in trained and sedentary subjects,” Life Sciences, vol. 78, no. 13, pp. 1441–1447, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Kodydková, L. Vávrová, M. Kocík, and A. Žák, “Human catalase, its polymorphisms regulation and changes of its activity in different diseases,” Folia Biologica, vol. 60, no. 4, pp. 153–167, 2014. View at Google Scholar · View at Scopus
  38. L. Rönnberg, A. Kauppila, J. Leppäluoto, H. Martikainen, and O. Vakkuri, “Circadian and seasonal variation in human preovulatory follicular fluid melatonin concentration,” Journal of Clinical Endocrinology and Metabolism, vol. 71, no. 2, pp. 493–496, 1990. View at Publisher · View at Google Scholar · View at Scopus
  39. Y. Ito, T. Iida, Y. Yamamura et al., “Relationships between salivary melatonin levels, quality of sleep, and stress in young Japanese females,” International Journal of Tryptophan Research, vol. 6, supplement 1, pp. 75–85, 2013. View at Publisher · View at Google Scholar
  40. J. Schröder, M. Dören, B. Schneider, and M. Oettel, “Are the antioxidative effects of 17β-estradiol modified by concomitant administration of a progestin?” Maturitas, vol. 25, no. 2, pp. 133–139, 1996. View at Publisher · View at Google Scholar · View at Scopus
  41. L. Góth, Lenkey A, and W. N. Bigler, “Blood catalase deficiency and diabetes in Hungary,” Diabetes Care, vol. 24, no. 10, pp. 1839–1840, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. N. Niikawa, Y. Fukushima, N. Taniguchi, S. Iizuka, and T. Kajii, “Chromosome abnormalities involving 11p13 and low erythrocyte catalase activity,” Human Genetics, vol. 60, no. 4, pp. 373–375, 1982. View at Publisher · View at Google Scholar · View at Scopus
  43. R. A. Omar, Y.-J. Chyan, A. C. Andorn, B. Poeggeler, N. K. Robakis, and M. A. Pappolla, “Increased expression but reduced activity of antioxidant enzymes in Alzheimer's disease,” Journal of Alzheimer's Disease, vol. 1, no. 3, pp. 139–145, 1999. View at Google Scholar · View at Scopus
  44. D. Gao, Z. Gao, and G. Zhu, “Antioxidant effects of Lactobacillus plantarum via activation of transcription factor Nrf2,” Food and Function, vol. 4, no. 6, pp. 982–989, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. A. N. Wang, X. W. Yi, H. F. Yu, B. Dong, and S. Y. Qiao, “Free radical scavenging activity of Lactobacillus fermentum in vitro and its antioxidative effect on growing-finishing pigs,” Journal of Applied Microbiology, vol. 107, no. 4, pp. 1140–1148, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. H. S. Ejtahed, J. Mohtadi-Nia, A. Homayouni-Rad, M. Niafar, M. Asghari-Jafarabadi, and V. Mofid, “Probiotic yogurt improves antioxidant status in type 2 diabetic patients,” Nutrition, vol. 28, no. 5, pp. 539–543, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. F. Gan, X. Chen, S. F. Liao et al., “Selenium-enriched probiotics improve antioxidant status, immune function, and selenoprotein gene expression of piglets raised under high ambient temperature,” Journal of Agricultural and Food Chemistry, vol. 62, no. 20, pp. 4502–4508, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Pandey, A. Singh, P. Kumar, A. Chaudhari, and G. Nareshkumar, “Probiotic Escherichia coli CFR 16 producing pyrroloquinoline quinone (PQQ) ameliorates 1,2-dimethylhydrazine-induced oxidative damage in colon and liver of rats,” Applied Biochemistry and Biotechnology, vol. 173, no. 3, pp. 775–786, 2014. View at Publisher · View at Google Scholar · View at Scopus
  49. M. A. Ghoneim and S. S. Moselhy, “Antioxidant status and hormonal profile reflected by experimental feeding of probiotics,” Toxicology and Industrial Health, 2013. View at Publisher · View at Google Scholar
  50. S. Kapila, R. Kapila, S. Reddi, and P. R. Sinha, “Oral administration of probiotic Lactobacillus casei spp. casei ameliorates oxidative stress in rats,” International Journal of Current Microbiology and Applied Sciences, vol. 3, no. 9, pp. 670–684, 2014. View at Google Scholar
  51. E. Fabian and I. Elmadfa, “The effect of daily consumption of probiotic and conventional yoghurt on oxidant and anti-oxidant parameters in plasma of young healthy women,” International Journal for Vitamin and Nutrition Research, vol. 77, no. 2, pp. 79–88, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. E. Vaghef-Mehrabany, A. Homayouni-Rad, B. Alipour, S. K. Sharif, L. Vaghef-Mehrabany, and S. Alipour-Ajiry, “Effects of probiotic supplementation on oxidative stress indices in women with rheumatoid arthritis: a randomized double-blind clinical trial,” Journal of the American College of Nutrition, 2015. View at Publisher · View at Google Scholar
  53. M. L. Stecchini, M. Del Torre, and M. Munari, “Determination of peroxy radical-scavenging of lactic acid bacteria,” International Journal of Food Microbiology, vol. 64, no. 1-2, pp. 183–188, 2001. View at Publisher · View at Google Scholar · View at Scopus
  54. R. Chauhan, A. S. Vasanthakumari, H. Panwar et al., “Amelioration of colitis in mouse model by exploring antioxidative potentials of an indigenous probiotic strain of Lactobacillus fermentum Lf1,” BioMed Research International, vol. 2014, Article ID 206732, 12 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. T. Cecchi, M. Savini, S. Silvi, M. C. Verdenelli, and A. Cresci, “Optimisation of the measurement of the antioxidant activity of probiotics and pathogens: a crucial step towards evidence-based assessment of health claims and production of effective functional foods,” Food Analytical Methods, vol. 8, no. 2, pp. 312–320, 2014. View at Publisher · View at Google Scholar · View at Scopus
  56. Y. Ishii, S. Sugimoto, N. Izawa, T. Sone, K. Chiba, and K. Miyazaki, “Oral administration of Bifidobacterium breve attenuates UV-induced barrier perturbation and oxidative stress in hairless mice skin,” Archives of Dermatological Research, vol. 306, no. 5, pp. 467–473, 2014. View at Publisher · View at Google Scholar · View at Scopus
  57. K. H. S. Farvin, C. P. Baron, N. S. Nielsen, and C. Jacobsen, “Antioxidant activity of yoghurt peptides: part 1-in vitro assays and evaluation in ω-3 enriched milk,” Food Chemistry, vol. 123, no. 4, pp. 1081–1089, 2010. View at Publisher · View at Google Scholar
  58. K. H. S. Farvin, C. P. Baron, N. S. Nielsen, J. Otte, and C. Jacobsen, “Antioxidant activity of yoghurt peptides: part 2—characterisation of peptide fractions,” Food Chemistry, vol. 123, no. 4, pp. 1090–1097, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. H. Korhonen and A. Pihlanto, “Bioactive peptides: production and functionality,” International Dairy Journal, vol. 16, no. 9, pp. 945–960, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Hayes, C. Stanton, G. F. Fitzgerald, and R. P. Ross, “Putting microbes to work: diary fermentation, cell factories and bioactive peptides. Part II: bioactive peptide functions,” Biotechnology Journal, vol. 2, no. 4, pp. 435–449, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. M.-Y. Lin and F.-J. Chang, “Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356,” Digestive Diseases and Sciences, vol. 45, no. 8, pp. 1617–1622, 2000. View at Publisher · View at Google Scholar · View at Scopus
  62. V. J. Koller, B. Marian, R. Stidl et al., “Impact of lactic acid bacteria on oxidative DNA damage in human derived colon cells,” Food and Chemical Toxicology, vol. 46, no. 4, pp. 1221–1229, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. S. S. Choi, Y. Kim, K. S. Han, S. You, S. Oh, and S. H. Kim, “Effects of Lactobacillus strains on cancer cell proliferation and oxidative stress in vitro,” Letters in Applied Microbiology, vol. 42, no. 5, pp. 452–458, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. D. G. Duman, Z. N. Ö. Kumral, F. Ercan, M. Deniz, G. Can, and B. Çağlayan Yeğen, “Saccharomyces boulardii ameliorates clarithromycin- and methotrexate-induced intestinal and hepatic injury in rats,” British Journal of Nutrition, vol. 110, no. 3, pp. 493–499, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. T. Şahin, S. Aydin, O. Yüksel et al., “Effects of the probiotic agent Saccharomyces boulardii on the DNA damage in acute necrotizing pancreatitis induced rats,” Human and Experimental Toxicology, vol. 26, no. 8, pp. 653–661, 2007. View at Publisher · View at Google Scholar · View at Scopus
  66. A. Suryavanshi, A. Agarwal, A. Kaler et al., “Comparative studies on the antioxidant potential of vanillin-producing Saccharomyces boulardii extracts,” Oxidants and Antioxidants in Medical Science, vol. 2, no. 3, pp. 201–209, 2013. View at Publisher · View at Google Scholar
  67. H. Annuk, J. Shchepetova, T. Kullisaar, E. Songisepp, M. Zilmer, and M. Mikelsaar, “Characterization of intestinal lactobacilli as putative probiotic candidates,” Journal of Applied Microbiology, vol. 94, no. 3, pp. 403–412, 2003. View at Publisher · View at Google Scholar · View at Scopus
  68. M. Kumar, A. Kumar, R. Nagpal et al., “Cancer-preventing attributes of probiotics: an update,” International Journal of Food Sciences and Nutrition, vol. 61, no. 5, pp. 473–496, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. D. Najgebauer-Lejko, “Effect of green tea supplementation on the microbiological, antioxidant, and sensory properties of probiotic milks,” Dairy Science and Technology, vol. 94, no. 4, pp. 327–339, 2014. View at Publisher · View at Google Scholar · View at Scopus
  70. G. Grompone, P. Martorell, S. Llopis et al., “Anti-inflammatory Lactobacillus rhamnosus CNCM I-3690 strain protects against oxidative stress and increases lifespan in Caenorhabditis elegans,” PLoS ONE, vol. 7, no. 12, Article ID e52493, 2012. View at Publisher · View at Google Scholar · View at Scopus
  71. S. Kapila, Vibha, and P. Sinha, “Antioxidative and hypocholesterolemic effect of Lactobacillus casei ssp casei (biodefensive properties of lactobacilli),” Indian Journal of Medical Sciences, vol. 60, no. 9, pp. 361–370, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. B. G. Spyropoulos, E. P. Misiakos, C. Fotiadis, and C. N. Stoidis, “Antioxidant properties of probiotics and their protective effects in the pathogenesis of radiation-induced enteritis and colitis,” Digestive Diseases and Sciences, vol. 56, no. 2, pp. 285–294, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. J. Lee, K.-T. Hwang, M.-Y. Chung, D.-H. Cho, and C.-S. Park, “Resistance of Lactobacillus casei KCTC 3260 to reactive oxygen species (ROS): role for a metal ion chelating effect,” Journal of Food Science, vol. 70, no. 8, pp. M388–M391, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. J. Sun, X.-L. Hu, G.-W. Le, and Y.-H. Shi, “Lactobacilli prevent hydroxy radical production and inhibit Escherichia coli and Enterococcus growth in system mimicking colon fermentation,” Letters in Applied Microbiology, vol. 50, no. 3, pp. 264–269, 2010. View at Publisher · View at Google Scholar
  75. Y.-C. Wang, R.-C. Yu, and C.-C. Chou, “Antioxidative activities of soymilk fermented with lactic acid bacteria and bifidobacteria,” Food Microbiology, vol. 23, no. 2, pp. 128–135, 2006. View at Publisher · View at Google Scholar · View at Scopus
  76. V. P. Kodali and R. Sen, “Antioxidant and free radical scavenging activities of an exopolysaccharide from a probiotic bacterium,” Biotechnology Journal, vol. 3, no. 2, pp. 245–251, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. N. Şengül, B. Aslım, G. Uçar et al., “Effects of exopolysaccharide-producing probiotic strains on experimental colitis in rats,” Diseases of the Colon and Rectum, vol. 49, no. 2, pp. 250–258, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. W. Han, A. Mercenier, A. Ait-Belgnaoui et al., “Improvement of an experimental colitis in rats by lactic acid bacteria producing superoxide dismutase,” Inflammatory Bowel Diseases, vol. 12, no. 11, pp. 1044–1052, 2006. View at Publisher · View at Google Scholar · View at Scopus
  79. I. M. Carroll, J. M. Andrus, J. M. Bruno-Bárcena, T. R. Klaenhammer, H. M. Hassan, and D. S. Threadgill, “Anti-inflammatory properties of Lactobacillus gasseri expressing manganese superoxide dismutase using the interleukin 10-deficient mouse model of colitis,” The American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 293, no. 4, pp. G729–G738, 2007. View at Publisher · View at Google Scholar · View at Scopus
  80. T. Kullisaar, M. Zilmer, M. Mikelsaar et al., “Two antioxidative lactobacilli strains as promising probiotics,” International Journal of Food Microbiology, vol. 72, no. 3, pp. 215–224, 2002. View at Publisher · View at Google Scholar · View at Scopus
  81. S. K. Chang and H. M. Hassan, “Characterization of superoxide dismutase in Streptococcus thermophilus,” Applied and Environmental Microbiology, vol. 63, no. 9, pp. 3732–3735, 1997. View at Google Scholar · View at Scopus
  82. A. de Moreno de LeBlanc, J. G. LeBlanc, G. Perdigón et al., “Oral administration of a catalase-producing Lactococcus lactis can prevent a chemically induced colon cancer in mice,” Journal of Medical Microbiology, vol. 57, no. 1, pp. 100–105, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. H. An, Z. Zhai, S. Yin, Y. Luo, B. Han, and Y. Hao, “Coexpression of the superoxide dismutase and the catalase provides remarkable oxidative stress resistance in lactobacillus rhamnosus,” Journal of Agricultural and Food Chemistry, vol. 59, no. 8, pp. 3851–3856, 2011. View at Publisher · View at Google Scholar · View at Scopus
  84. L.-X. Wang, K. Liu, D.-W. Gao, and J.-K. Hao, “Protective effects of two Lactobacillus plantarum strains in hyperlipidemic mice,” World Journal of Gastroenterology, vol. 19, no. 20, pp. 3150–3156, 2013. View at Publisher · View at Google Scholar · View at Scopus
  85. F. Lutgendorff, R. M. Nijmeijer, P. A. Sandström et al., “Probiotics prevent intestinal barrier dysfunction in acute pancreatitis in rats via induction of ileal mucosal glutathione biosynthesis,” PLoS ONE, vol. 4, no. 2, Article ID e4512, 2009. View at Publisher · View at Google Scholar · View at Scopus
  86. L. P. van Minnen, H. M. Timmerman, F. Lutgendorff et al., “Modification of intestinal flora with multispecies probiotics reduces bacterial translocation and improves clinical course in a rat model of acute pancreatitis,” Surgery, vol. 141, no. 4, pp. 470–480, 2007. View at Publisher · View at Google Scholar · View at Scopus