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BioMed Research International
Volume 2017, Article ID 6747482, 8 pages
https://doi.org/10.1155/2017/6747482
Research Article

Recombinant Lactococcus lactis Expressing Haemagglutinin from a Polish Avian H5N1 Isolate and Its Immunological Effect in Preliminary Animal Trials

Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Warsaw, Poland

Correspondence should be addressed to Agnieszka K. Szczepankowska; lp.waw.bbi@pezczsaga

Received 19 December 2016; Revised 20 January 2017; Accepted 24 January 2017; Published 22 February 2017

Academic Editor: Bernd H. Rehm

Copyright © 2017 Agnieszka K. Szczepankowska 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. E. Morello, L. G. Bermúdez-Humarán, D. Llull et al., “Lactococcus lactis, an efficient cell factory for recombinant protein production and secretion,” Journal of Molecular Microbiology and Biotechnology, vol. 14, no. 1–3, pp. 48–58, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. J. M. Wells and A. Mercenier, “Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteria,” Nature Reviews Microbiology, vol. 6, no. 5, pp. 349–362, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. L. Steidler, P. Rottiers, and B. Coulie, “Actobiotics™ as a novel method for cytokine delivery: the interleukin-10 case,” Annals of the New York Academy of Sciences, vol. 1182, pp. 135–145, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. L. G. Bermúdez-Humarán, P. Kharrat, J.-M. Chatel, and P. Langella, “Lactococci and lactobacilli as mucosal delivery vectors for therapeutic proteins and DNA vaccines,” Microbial Cell Factories, vol. 10, no. 1, article S4, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. D. S. Pontes, M. S. P. De Azevedo, J.-M. Chatel, P. Langella, V. Azevedo, and A. Miyoshi, “Lactococcus lactis as a live vector: heterologous protein production and DNA delivery systems,” Protein Expression and Purification, vol. 79, no. 2, pp. 165–175, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Wang, Z. Gao, Y. Zhang, and L. Pan, “Lactic acid bacteria as mucosal delivery vehicles: a realistic therapeutic option,” Applied Microbiology and Biotechnology, vol. 100, no. 13, pp. 5691–5701, 2016. View at Publisher · View at Google Scholar · View at Scopus
  7. P. Mannam, K. F. Jones, and B. L. Geller, “Mucosal vaccine made from live, recombinant Lactococcus lactis protects mice against pharyngeal infection with Streptococcus pyogenes,” Infection and Immunity, vol. 72, no. 6, pp. 3444–3450, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. K. Robinson, L. M. Chamberlain, K. M. Schofield, J. M. Wells, and R. W. F. Le Page, “Oral vaccination of mice against tetanus with recombinant Lactococcus lactis,” Nature Biotechnology, vol. 15, no. 7, pp. 653–657, 1997. View at Publisher · View at Google Scholar · View at Scopus
  9. K.-Q. Xin, Y. Hoshino, Y. Toda et al., “Immunogenicity and protective efficacy of orally administered recombinant Lactococcus lactis expressing surface-bound HIV Env,” Blood, vol. 102, no. 1, pp. 223–228, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. Q. Zhang, J. Zhong, and L. Huan, “Expression of hepatitis B virus surface antigen determinants in Lactococcus lactis for oral vaccination,” Microbiological Research, vol. 166, no. 2, pp. 111–120, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. K. Adel-Patient, S. Ah-Leung, C. Creminon et al., “Oral administration of recombinant Lactococcus lactis expressing bovine β-lactoglobulin partially prevents mice from sensitization,” Clinical and Experimental Allergy, vol. 35, no. 4, pp. 539–546, 2005. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Medina, E. Vintiñi, J. Villena, R. Raya, and S. Alvarez, “Lactococcus lactis as an adjuvant and delivery vehicle of antigens against pneumococcal respiratory infections,” Bioengineered Bugs, vol. 1, no. 5, pp. 313–325, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. M. J. Smelt, B. J. de Haan, P. A. Bron et al., “L. plantarum, L. salivarius, and L. lactis attenuate Th2 responses and increase Treg frequencies in healthy mice in a strain dependent manner,” PLOS ONE, vol. 7, no. 10, Article ID e47244, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. C. O. Elson and M. T. Dertzbaugh, “Mucosal adjuvants,” in Handbook of Mucosal Immunology, R. Ogra, J. Mestecky, M. E. Lamm et al., Eds., pp. 967–986, Academic Press, New York, NY, USA, 3rd edition, 2005. View at Google Scholar
  15. K. Fujihashi, T. Koga, F. W. Van Ginkel, Y. Hagiwara, and J. R. McGhee, “A dilemma for mucosal vaccination: efficacy versus toxicity using enterotoxin-based adjuvants,” Vaccine, vol. 20, no. 19-20, pp. 2431–2438, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. G. Perdigón, R. Fuller, and R. Raya, “Lactic acid bacteria and their effect on the immune system,” Current Issues in Intestinal Microbiology, vol. 2, no. 1, pp. 27–42, 2001. View at Google Scholar · View at Scopus
  17. A. Mercenier, H. Müller-Alouf, and C. Grangette, “Lactic acid bacteria as live vaccines,” Current Issues in Molecular Biology, vol. 2, no. 1, pp. 17–25, 2000. View at Google Scholar · View at Scopus
  18. A. E. Wold, U. I. Dahlgren, L. A. Hanson, I. Mattsby-Baltzer, and T. Midvetdt, “Difference between bacterial and food antigens in mucosal immunogenicity,” Infection and Immunity, vol. 57, no. 9, pp. 2666–2673, 1989. View at Google Scholar · View at Scopus
  19. I. Mierau and M. Kleerebezem, “10 Years of the nisin-controlled gene expression system (NICE) in Lactococcus lactis,” Applied Microbiology and Biotechnology, vol. 68, no. 6, pp. 705–717, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. I. Mierau, P. Leij, I. van Swam et al., “Industrial-scale production and purification of a heterologous protein in Lactococcus lactis using the nisin-controlled gene expression system NICE: the case of lysostaphin,” Microbial Cell Factories, vol. 4, article no. 15, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. J. J. Skehel and D. C. Wiley, “Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin,” Annual Review of Biochemistry, vol. 69, pp. 531–569, 2000. View at Publisher · View at Google Scholar · View at Scopus
  22. L. Du, G. Zhao, S. Sun et al., “A critical HA1 neutralizing domain of H5N1 influenza in an optimal conformation induces strong cross-protection,” PLoS ONE, vol. 8, no. 1, Article ID e53568, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. H. R. Haghighi, L. R. Read, S. M. M. Haeryfar, S. Behboudi, and S. Shariff, “Identification of a dual-specific T cell epitope of the hemagglutinin antigen of an H5 avian influenza virus in chickens,” PLoS ONE, vol. 4, no. 11, Article ID e7772, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Jiang, R. Li, L. Du, and S. Liu, “Roles of the hemagglutinin of influenza A virus in viral entry and development of antiviral therapeutics and vaccines,” Protein and Cell, vol. 1, no. 4, pp. 342–354, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. D. L. Suarez and S. Schultz-Cherry, “Immunology of avian influenza virus: a review,” Developmental and Comparative Immunology, vol. 24, no. 2-3, pp. 269–283, 2000. View at Publisher · View at Google Scholar · View at Scopus
  26. http://www.who.int/influenza/human_animal_interface/en/.
  27. B. E. Terzaghi and W. E. Sandine, “Improved medium for lactic streptococci and their bacteriophages,” Journal of Applied Microbiology, vol. 29, no. 6, pp. 807–813, 1975. View at Google Scholar · View at Scopus
  28. J. Sambrook, E. F. Fritsch, and T. Maniatis, Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA, 2nd edition, 1989.
  29. H. Holo and I. F. Nes, “High-frequency transformation, by electroporation, of Lactococcus lactis subsp. cremoris grown with glycine in osmotically stabilized media,” Applied and Environmental Microbiology, vol. 55, no. 12, pp. 3119–3123, 1989. View at Google Scholar · View at Scopus
  30. J. M. Wells, P. W. Wilson, P. M. Norton, M. J. Gasson, and R. W. F. Le Page, “Lactococcus lactis: high‐level expression of tetanus toxin fragment C and protection against lethal challenge,” Molecular Microbiology, vol. 8, no. 6, pp. 1155–1162, 1993. View at Publisher · View at Google Scholar · View at Scopus
  31. L. G. Bermúdez-Humarán, “Lactococcus lactis as a live vector for mucosal delivery of therapeutic proteins,” Human Vaccines, vol. 5, no. 4, pp. 264–267, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. K. K. Yam, P. Pouliot, M. M. N'diaye, S. Fournier, M. Olivier, and B. Cousineau, “Innate inflammatory responses to the Gram-positive bacterium Lactococcus lactis,” Vaccine, vol. 26, no. 22, pp. 2689–2699, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. K. Szatraj, A. K. Szczepankowska, V. Sazyńska et al., “Expression of avian influenza haemagglutinin (H5) and chicken interleukin 2 (chIL-2) under control of the ptcB promoter in Lactococcus lactis,” Acta Biochimica Polonica, vol. 61, no. 3, pp. 609–614, 2014. View at Google Scholar · View at Scopus
  34. M. C. Martínez-Cuesta, M. J. Gasson, and A. Narbad, “Heterologous expression of the plant coumarate: CoA ligase in Lactococcus lactis,” Letters in Applied Microbiology, vol. 40, no. 1, pp. 44–49, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. I. Mierau, K. Olieman, J. Mond, and E. J. Smid, “Optimization of the Lactococcus lactis nisin-controlled gene expression system NICE for industrial applications,” Microbial Cell Factories, vol. 4, article 16, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Monné, W. C. Ka, D.-J. Slotboom, and E. R. S. Kunji, “Functional expression of eukaryotic membrane proteins in Lactococcus lactis,” Protein Science, vol. 14, no. 12, pp. 3048–3056, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. D. T. W. Ng and C. A. Sarkar, “Nisin-inducible secretion of a biologically active single-chain insulin analog by Lactococcus lactis NZ9000,” Biotechnology and Bioengineering, vol. 108, no. 8, pp. 1987–1996, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. W. Sybesma, E. Van Den Born, M. Starrenburg et al., “Controlled modulation of folate polyglutamyl tail length by metabolic engineering of Lactococcus lactis,” Applied and Environmental Microbiology, vol. 69, no. 12, pp. 7101–7107, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. P. Kaiser, “Advances in avian immunology-prospects for disease control: a review,” Avian Pathology, vol. 39, no. 5, pp. 309–324, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Gambaryan, S. Yamnikova, D. Lvov et al., “Receptor specificity of influenza viruses from birds and mammals: new data on involvement of the inner fragments of the carbohydrate chain,” Virology, vol. 334, no. 2, pp. 276–283, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. M. N. Matrosovich, T. Y. Matrosovich, T. Gray, N. A. Roberts, and H.-D. Klenk, “Human and avian influenza viruses target different cell types in cultures of human airway epithelium,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 13, pp. 4620–4624, 2004. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Stevens, O. Blixt, L. Glaser et al., “Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities,” Journal of Molecular Biology, vol. 355, no. 5, pp. 1143–1155, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. N. G. Cortes-Perez, L. G. Bermúdez-Humarán, Y. Le Loir et al., “Mice immunization with live lactococci displaying a surface anchored HPV-16 E7 oncoprotein,” FEMS Microbiology Letters, vol. 229, no. 1, pp. 37–42, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. N. G. Cortes-Perez, V. Azevedo, J. M. Alcocer-González et al., “Cell-surface display of E7 antigen from human papillomavirus type-16 in Lactococcus lactis and in Lactobacillus plantarum using a new cell-wall anchor from lactobacilli,” Journal of Drug Targeting, vol. 13, no. 2, pp. 89–98, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. N. G. Cortes-Perez, F. Lefèvre, G. Corthier, K. Adel-Patient, P. Langella, and L. G. Bermúdez-Humarán, “Influence of the route of immunization and the nature of the bacterial vector on immunogenicity of mucosal vaccines based on lactic acid bacteria,” Vaccine, vol. 25, no. 36, pp. 6581–6588, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Nouaille, L. G. Bermúdez-Humarán, K. Adel-Patient et al., “Improvement of bovine β-lactoglobulin production and secretion by Lactococcus lactis,” Brazilian Journal of Medical and Biological Research, vol. 38, no. 3, pp. 353–359, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. L. G. Bermúdez-Humarán, N. G. Cortes-Perez, Y. Le Loir et al., “Fusion to a carrier protein and a synthetic propeptide enhances E7 HPV-16 production and secretion in Lactococcus lactis,” Biotechnology Progress, vol. 19, no. 3, pp. 1101–1104, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. L. G. Bermúdez-Humarán, P. Langella, A. Miyoshi et al., “Production of human papillomavirus type 16 E7 protein in Lactococcus lactis,” Applied and Environmental Microbiology, vol. 68, no. 2, pp. 917–922, 2002. View at Publisher · View at Google Scholar · View at Scopus
  49. N. K. Jain and I. Roy, “Effect of trehalose on protein structure,” Protein Science, vol. 18, no. 1, pp. 24–36, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Bahey-El-Din, “Lactococcus lactis-based vaccines from laboratory bench to human use: an overview,” Vaccine, vol. 30, no. 4, pp. 685–690, 2012. View at Publisher · View at Google Scholar · View at Scopus