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Journal of Immunology Research
Volume 2017, Article ID 6976935, 9 pages
https://doi.org/10.1155/2017/6976935
Research Article

Beta-Defensin-2 and Beta-Defensin-3 Reduce Intestinal Damage Caused by Salmonella typhimurium Modulating the Expression of Cytokines and Enhancing the Probiotic Activity of Enterococcus faecium

Department of Experimental Medicine, University of Campania “Luigi Vanvitelli”, Via De Crecchio No. 7, 80138 Naples, Italy

Correspondence should be addressed to Alessandra Fusco; ti.ainapmacinu@ocsuf.ardnassela and Giovanna Donnarumma; ti.ainapmacinu@ammurannod.annavoig

Received 29 May 2017; Revised 9 August 2017; Accepted 5 September 2017; Published 9 November 2017

Academic Editor: Mitesh Dwivedi

Copyright © 2017 Alessandra Fusco 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. L. V. Hooper, D. R. Littman, and A. J. Macpherson, “Interactions between the microbiota and the immune system,” Science, vol. 336, pp. 1268–1273, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. W. S. Garrett, C. A. Gallini, T. Yatsunenko et al., “Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis,” Cell Host & Microbe, vol. 8, pp. 292–300, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. J. Bollrath and F. M. Powrie, “Controlling the frontier: regulatory T-cells and intestinal homeostasis,” Seminars in Immunology, vol. 25, pp. 352–357, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. P. J. Sansonetti, “Microbiota and the immune system, an amazing mutualism forged by co-evolution,” Seminars in Immunology, vol. 25, pp. 321-322, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. F. Bäckhed, H. Ding, T. Wang et al., “The gut microbiota as an environmental factor that regulates fat storage,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 44, pp. 15718–15723, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. R. Krajmalnik-Brown, Z. E. Ilhan, D. W. Kang, and J. K. DiBaise, “Effects of gut microbes on nutrient absorption and energy regulation,” Nutrition in Clinical Practice, vol. 27, no. 2, pp. 201–214, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. C. M. Franz, M. Huch, H. Abriouel, W. Holzapfel, and A. Gálvez, “Enterococci as probiotics and their implications in food safety,” International Journal of Food Microbiology, vol. 151, no. 2, pp. 125–140, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. N. I. Agudelo Higuita and M. M. Huycke, “Enterococcal disease, epidemiology, and implications for treatment,” in Enterococci: From Commensals to Leading Causes of Drug Resistant Infection [Internet], M. S. Gilmore, D. B. Clewell, Y. Ike, and N. Shankar, Eds., Massachusetts Eye and Ear Infirmary, Boston, 2014. View at Google Scholar
  9. C. A. Arias and B. E. Murray, “The rise of the Enterococcus: beyond vancomycin resistance,” Nature Reviews Microbiology, vol. 10, no. 4, pp. 266–278, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Benenson, M. J. Cohen, C. Block, S. Stern, Y. Weiss, and A. E. Moses JIRMI Group, “Vancomycin-resistant enterococci in long-term care facilities,” Infection Control and Hospital Epidemiology, vol. 30, no. 8, pp. 786–789, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. K. Fisher and C. Phillips, “The ecology, epidemiology and virulence of Enterococcus,” Microbiology, vol. 5, Part 6, pp. 1749–1757, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. E. Tarasova, E. Yermolenko, V. Donets et al., “The influence of probiotic Enterococcus faecium strain L5 on the microbiota and cytokines expression in rats with dysbiosis induced by antibiotics,” Beneficial Microbes, vol. 1, no. 3, pp. 265–270, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Thirabunyanon and P. Hongwittayakorn, “Potential probiotic lactic acid bacteria of human origin induce antiproliferation of colon cancer cells via synergic actions in adhesion to cancer cells and short-chain fatty acid bioproduction,” Applied Biochemistry and Biotechnology, vol. 169, no. 2, pp. 511–525, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. Z. Wang, W. Chai, M. Burwinkel et al., “Inhibitory influence of Enterococcus faecium on the propagation of swine influenza A virus in vitro,” PLoS One, vol. 8, no. 1, article e53043, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Miyazaki, S. Kamiya, T. Hanawa et al., “Effect of probiotic bacterial strains of Lactobacillus, Bifidobacterium, and Enterococcus on enteroaggregative Escherichia coli,” Journal of Infection and Chemotherapy, vol. 16, no. 1, pp. 10–18, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. I. F. Ness, D. B. Diep, and Y. Ike, “Enterococcal bacteriocins and antimicrobial proteins that contribute to niche control,” in Enterococci: From Commensals to Leading Causes of Drug Resistant Infection, M. S. Gilmore, D. B. Clewell, Y. Ike, and N. Shankar, Eds., Massachusetts Eye and Ear Infirmary, Boston, 2014. View at Google Scholar
  17. H. Khan, S. Flint, and P. L. Yu, “Enterocins in food preservation,” International Journal of Food Microbiology, vol. 141, no. 1-2, pp. 1–10, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. F. Leroy, M. R. Foulquié Moreno, and L. De Vuyst, “Enterococcus faecium RZS C5, an interesting bacteriocin producer to be used as a co-culture in food fermentation,” International Journal of Food Microbiology, vol. 88, no. 2-3, pp. 235–240, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. D. Taras, W. Vahjen, M. Macha, and O. Simon, “Performance, diarrhea incidence, and occurrence of virulence genes during long-term administration of a probiotic strain to sows and piglets,” Journal of Animal Science, vol. 84, no. 3, pp. 608–617, 2006. View at Publisher · View at Google Scholar
  20. A. Zeyner and E. Boldt, “Effects of a probiotic Enterococcus faecium strain supplemented from birth to weaning on diarrhoea patterns and performance of piglets,” Journal of Animal Physiology and Animal Nutrition, vol. 90, no. 1-2, pp. 25–31, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Klingspor, A. Bondzio, H. Martens et al., “Enterococcus faecium NCIMB 10415 modulates epithelial integrity, heat shock protein, and proinflammatory cytokine response in intestinal cells,” Mediators of Inflammation, vol. 2015, Article ID 304149, 11 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  22. L. R. Schiller, “Infectious disease: a germy world-food-borne infections in 2009,” Nature Reviews Gastroenterology & Hepatology, vol. 6, no. 4, pp. 197-198, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. A. T. Gewirtz, A. S. Rao, P. O. Simon Jr et al., “Salmonella typhimurium induces epithelial IL-8 expression via Ca(2+)-mediated activation of the NF-κB pathway,” The Journal of Clinical Investigation, vol. 105, no. 1, pp. 79–92, 2000. View at Publisher · View at Google Scholar
  24. M. S. Kim, Y. S. Yoon, J. G. Seo, H. G. Lee, M. J. Chung, and D. Y. Yum, “A study on the prevention of salmonella infection by using the aggregation characteristics of lactic acid bacteria,” Toxicology Research, vol. 29, no. 2, pp. 129–135, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. S. P. Brown, L. Le Chat, and F. Taddei, “Evolution of virulence: triggering host inflammation allows invading pathogens to exclude competitors,” Ecology Letters, vol. 11, no. 1, pp. 44–51, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. Y. J. Yang, C. C. Chuang, H. B. Yang, C. C. Lu, and B. S. Sheu, “Lactobacillus acidophilus ameliorates H. pylori-induced gastric inflammation by inactivating the Smad7 and NFκB pathways,” BMC Microbiology, vol. 12, p. 38, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. L. R. McCabe, R. Irwin, L. Schaefer, and R. A. Britton, “Probiotic use decreases intestinal inflammation and increases bone density in healthy male but not female mice,” Journal of Cellular Physiology, vol. 228, no. 8, pp. 1793–1798, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Dimitrijevic, N. Ivanovic, G. Mathiesen et al., “Effects of Lactobacillus rhamnosus LA68 on the immune system of C57BL/6 mice upon oral administration,” The Journal of Dairy Research, vol. 81, no. 2, pp. 202–207, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. N. Ivanovic, R. Minic, L. Dimitrijevic, S. Radojevic Skodric, I. Zivkovic, and B. Djordjevic, “Lactobacillus rhamnosus LA68 and Lactobacillus plantarum WCFS1 differently influence metabolic and immunological parameters in high fat diet-induced hypercholesterolemia and hepatic steatosis,” Food & Function, vol. 6, no. 2, pp. 558–565, 2015. View at Publisher · View at Google Scholar · View at Scopus
  30. C. Li, S. P. Nie, K. X. Zhu et al., “Lactobacillus plantarum NCU116 improves liver function, oxidative stress and lipid metabolism in rats with high fat diet induced non-alcoholic fatty liver disease,” Food & Function, vol. 5, no. 12, pp. 3216–3223, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. G. Donnarumma, I. Paoletti, A. Fusco et al., “β-defensins: work in progress,” Advances in Experimental Medicine and Biology, vol. 901, pp. 59–76, 2016. View at Publisher · View at Google Scholar · View at Scopus
  32. A. Fusco, L. Coretti, V. Savio, E. Buommino, F. Lembo, and G. Donnarumma, “Biofilm formation and immunomodulatory activity of proteus mirabilis clinically isolated strains,” International Journal of Molecular Sciences, vol. 18, no. 2, p. 414, 2017. View at Publisher · View at Google Scholar
  33. T. Ganz, “Defensins: antimicrobial peptides of innate immunity,” Nature Reviews. Immunology, vol. 3, no. 9, pp. 710–720, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. J. Harder, J. Bartels, E. Christophers, and J. M. Schroder, “Isolation and characterization of human β-defensin-3, a novel human inducible peptide antibiotic,” The Journal of Biological Chemistry, vol. 276, no. 8, pp. 5707–5713, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Dunsche, Y. Açil, H. Dommisch, R. Siebert, J. M. Schröder, and S. Jepsen, “The novel human beta-defensin-3 is widely expressed in oral tissues,” European Journal of Oral Sciences, vol. 110, no. 2, pp. 121–124, 2002. View at Publisher · View at Google Scholar
  36. J. M. Ageitos, A. Sánchez-Pérez, P. Calo-Mata, and T. G. Villa, “Antimicrobial peptides (AMPs): ancient compounds that represent novel weapons in the fight against bacteria,” Biochemical Pharmacology, vol. 133, pp. 117–138, 2016. View at Publisher · View at Google Scholar · View at Scopus
  37. F. Niyonsaba, H. Ogawa, and I. Nagaoka, “Human β-defensin-2 functions as a chemotactic agent for tumour necrosis factor-α-treated human neutrophils,” Immunology, vol. 111, no. 3, pp. 273–281, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. P. Morganti, A. Fusco, I. Paoletti et al., “Anti-inflammatory, immunomodulatory, and tissue repair activity on human keratinocytes by green innovative nanocomposites,” Materials, vol. 10, no. 7, p. 843, 2017. View at Publisher · View at Google Scholar
  39. J. Harder, J. Bartels, E. Christophers, and J. M. Schröder, “A peptide antibiotic from human skin,” Nature, vol. 387, no. 6636, p. 861, 1997. View at Publisher · View at Google Scholar · View at Scopus
  40. B. A. Dale and S. Krisanaprakornkit, “Defensin antimicrobial peptides in the oral cavity,” Journal of Oral Pathology & Medicine, vol. 30, no. 6, pp. 321–332, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. D. G. Carothers, S. M. Graham, H. P. Jia, M. R. Ackermann, B. F. Tack, and P. B. McCray Jr, “Production of β-defensin antimicrobial peptides by maxillary sinus mucosa,” American Journal of Rhinology, vol. 15, no. 3, pp. 175–179, 2001. View at Publisher · View at Google Scholar
  42. A. M. McDermott, R. L. Redfern, B. Zhang, Y. Pei, L. Huang, and R. J. Proske, “Defensin expression by the cornea: multiple signalling pathways mediate IL-1β stimulation of hBD-2 expression by human corneal epithelial cells,” Investigative Ophthalmology & Visual Science, vol. 44, no. 5, pp. 1859–1865, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. R. Ley, D. Peterson, and J. Gordon, “Ecological and evolutionary forces shaping microbial diversity in the human intestine,” Cell, vol. 124, pp. 837–848, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. J. Qin, R. Li, J. Raes et al., “A human gut microbial gene catalogue established by metagenomic sequencing,” Nature, vol. 464, pp. 59–65, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. A. P. A. Hendrickx, W. van Schaik, and R. J. L. Willems, “The cell wall architecture of Enterococcus faecium: from resistance to pathogenesis,” Future Microbiology, vol. 8, no. 8, pp. 993–1010, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. N. Silva, G. Igrejas, A. Gonçalves, and P. Poeta, “Commensal gut bacteria: distribution of Enterococcus species and prevalence of Escherichia coli phylogenetic groups in animals and humans in Portugal,” Annales de Microbiologie, vol. 62, no. 2, pp. 449–459, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. L. Eckmann, M. F. Kagnoff, and J. Fierer, “Intestinal epithelial cells as watchdogs for the natural immune system,” Trends in Microbiology, vol. 3, pp. 118–120, 1995. View at Publisher · View at Google Scholar · View at Scopus
  48. L. Eckmann, M. F. Kagnoff, and J. Fierer, “Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry,” Infection and Immunity, vol. 61, pp. 4569–4574, 1993. View at Google Scholar
  49. B. A. McCormick, S. P. Colgan, C. Delp-Archer, S. I. Miller, and J. L. Madara, “Salmonella typhimurium attachment to human intestinal epithelial monolayers: transcellular signalling to subepithelial neutrophils,” The Journal of Cell Biology, vol. 123, pp. 895–907, 1993. View at Publisher · View at Google Scholar
  50. H. C. Jung, L. Eckmann, S. K. Yang et al., “A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion,” The Journal of Clinical Investigation, vol. 95, pp. 55–65, 1995. View at Publisher · View at Google Scholar
  51. A. R. Franz, G. Steinbach, M. Kron, and F. Pohlandt, “Reduction of unnecessary antibiotic therapy in newborn infants using interleukin-8 and C-reactive protein as markers of bacterial infections,” Pediatrics, vol. 104, pp. 447–453, 1999. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Krueger, M. S. Nauck, S. Sang, R. Hentschel, H. Wieland, and R. Berner, “Cord blood levels of interleukin-6 and interleukin-8 for the immediate diagnosis of early-onset infection in premature infants,” Biology of the Neonate, vol. 80, pp. 118–123, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Pasupuleti, A. Schmidtchen, and M. Malmsten, “Antimicrobial peptides: key components of the innate immune system,” Critical Reviews in Biotechnology, vol. 32, no. 2, pp. 143–171, 2012. View at Publisher · View at Google Scholar · View at Scopus