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Journal of Immunology Research
Volume 2016, Article ID 9171632, 13 pages
http://dx.doi.org/10.1155/2016/9171632
Research Article

Rotavirus Recombinant VP6 Nanotubes Act as an Immunomodulator and Delivery Vehicle for Norovirus Virus-Like Particles

Vaccine Research Center, University of Tampere, Biokatu 10, 33520 Tampere, Finland

Received 23 February 2016; Revised 5 July 2016; Accepted 19 July 2016

Academic Editor: Aurelia Rughetti

Copyright © 2016 Maria Malm 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. T. Vesikari, “Rotavirus vaccination: a concise review,” Clinical Microbiology and Infection, vol. 18, supplement 5, pp. 57–63, 2012. View at Publisher · View at Google Scholar · View at Scopus
  2. R. L. Ward and M. M. McNeal, “VP6: a candidate rotavirus vaccine,” The Journal of Infectious Diseases, vol. 202, supplement 1, pp. S101–S107, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. M. M. Patel, D. Steele, J. R. Gentsch, J. Wecker, R. I. Glass, and U. D. Parashar, “Real-world impact of rotavirus vaccination,” Pediatric Infectious Disease Journal, vol. 30, no. 1, pp. S1–S5, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Angel, M. A. Franco, and H. B. Greenberg, “Rotavirus immune responses and correlates of protection,” Current Opinion in Virology, vol. 2, no. 4, pp. 419–425, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. K. Zaman, D. D. Anh, J. C. Victor et al., “Efficacy of pentavalent rotavirus vaccine against severe rotavirus gastroenteritis in infants in developing countries in Asia: a randomised, double-blind, placebo-controlled trial,” The Lancet, vol. 376, no. 9741, pp. 615–623, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. S. A. Madhi, N. A. Cunliffe, D. Steele et al., “Effect of human rotavirus vaccine on severe diarrhea in African infants,” The New England Journal of Medicine, vol. 362, no. 4, pp. 289–298, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. V. Blazevic, S. Lappalainen, K. Nurminen, L. Huhti, and T. Vesikari, “Norovirus VLPs and rotavirus VP6 protein as combined vaccine for childhood gastroenteritis,” Vaccine, vol. 29, no. 45, pp. 8126–8133, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. K. Tamminen, S. Lappalainen, L. Huhti, T. Vesikari, and V. Blazevic, “Trivalent combination vaccine induces broad heterologous immune responses to norovirus and rotavirus in mice,” PLoS ONE, vol. 8, no. 7, article e70409, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Lappalainen, A. R. Pastor, K. Tamminen et al., “Immune responses elicited against rotavirus middle layer protein VP6 inhibit viral replication in vitro and in vivo,” Human Vaccines & Immunotherapeutics, vol. 10, no. 7, pp. 2039–2047, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. B. V. V. Prasad, G. J. Wang, J. P. M. Clerx, and W. Chiu, “Three-dimensional structure of rotavirus,” Journal of Molecular Biology, vol. 199, no. 2, pp. 269–275, 1988. View at Publisher · View at Google Scholar · View at Scopus
  11. P. A. Offit and G. Blavat, “Identification of the two rotavirus genes determining neutralization specificities,” Journal of Virology, vol. 57, no. 1, pp. 376–378, 1986. View at Google Scholar · View at Scopus
  12. M. K. Estes, “Rotaviruses,” in Fields Virology, D. M. Knipe, Ed., pp. 1917–1974, Lippincott Williams & Wilkins, Philadelphia, Pa, USA, 5th edition, 2007. View at Google Scholar
  13. M. K. Estes, S. E. Crawford, M. E. Penaranda et al., “Synthesis and immunogenicity of the rotavirus major capsid antigen using a baculovirus expression system,” Journal of Virology, vol. 61, no. 5, pp. 1488–1494, 1987. View at Google Scholar · View at Scopus
  14. F. Bugli, V. Caprettini, M. Cacaci et al., “Synthesis and characterization of different immunogenic viral nanoconstructs from rotavirus VP6 inner capsid protein,” International Journal of Nanomedicine, vol. 9, no. 1, pp. 2727–2739, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. A. H.-C. Choi, M. Basu, M. M. McNeal, J. D. Clements, and R. L. Ward, “Antibody-independent protection against rotavirus infection of mice stimulated by intranasal immunization with chimeric VP4 or VP6 protein,” Journal of Virology, vol. 73, no. 9, pp. 7574–7581, 1999. View at Google Scholar · View at Scopus
  16. A. Z. Kapikian, Y. Hoshino, and R. M. Chanock, “Reoviridae,” in Rotaviruses, B. N. Fields, D. M. Knipe, and P. M. Howley, Eds., chapter 55, pp. 2719–2769, Lippincott Williams & Wilkins, 4th edition, 2001. View at Google Scholar
  17. J. Lepault, I. Petitpas, I. Erk et al., “Structural polymorphism of the major capsid protein of rotavirus,” The EMBO Journal, vol. 20, no. 7, pp. 1498–1507, 2001. View at Publisher · View at Google Scholar · View at Scopus
  18. I. Schwartz-Cornil, Y. Benureau, H. Greenberg, B. A. Hendrickson, and J. Cohen, “Heterologous protection induced by the inner capsid proteins of rotavirus requires transcytosis of mucosal immunoglobulins,” Journal of Virology, vol. 76, no. 16, pp. 8110–8117, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. M. A. Franco, J. Angel, and H. B. Greenberg, “Immunity and correlates of protection for rotavirus vaccines,” Vaccine, vol. 24, no. 15, pp. 2718–2731, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Lappalainen, A. R. Pastor, M. Malm et al., “Protection against live rotavirus challenge in mice induced by parenteral and mucosal delivery of VP6 subunit rotavirus vaccine,” Archives of Virology, vol. 160, no. 8, pp. 2075–2078, 2015. View at Publisher · View at Google Scholar · View at Scopus
  21. M. S. Aiyegbo, G. Sapparapu, B. W. Spiller et al., “Human rotavirus VP6-specific antibodies mediate intracellular neutralization by binding to a quaternary structure in the transcriptional pore,” PLoS ONE, vol. 8, no. 5, Article ID e61101, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. J. W. Burns, M. Siadat-Pajouh, A. A. Krishnaney, and H. B. Greenberg, “Protective effect of rotavirus VP6-specific IgA monoclonal antibodies that lack neutralizing activity,” Science, vol. 272, no. 5258, pp. 104–107, 1996. View at Publisher · View at Google Scholar · View at Scopus
  23. B. Corthésy, Y. Benureau, C. Perrier et al., “Rotavirus anti-VP6 secretory immunoglobulin A contributes to protection via intracellular neutralization but not via immune exclusion,” Journal of Virology, vol. 80, no. 21, pp. 10692–10699, 2006. View at Publisher · View at Google Scholar · View at Scopus
  24. V. Blazevic, M. Malm, D. Arinobu, S. Lappalainen, and T. Vesikari, “Rotavirus capsid VP6 protein acts as an adjuvant in vivo for norovirus virus-like particles in a combination vaccine,” Human Vaccines & Immunotherapeutics, vol. 12, no. 3, pp. 740–748, 2016. View at Publisher · View at Google Scholar
  25. M. J. Redmond, H. B. Ohmann, H. P. A. Hughes et al., “Rotavirus particles function as immunological carriers for the delivery of peptides from infectious agents and endogenous proteins,” Molecular Immunology, vol. 28, no. 3, pp. 269–278, 1991. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Peralta, P. Molinari, and O. Taboga, “Chimeric recombinant rotavirus-like particles as a vehicle for the display of heterologous epitopes,” Virology Journal, vol. 6, article 192, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. C. Foged, B. Brodin, S. Frokjaer, and A. Sundblad, “Particle size and surface charge affect particle uptake by human dendritic cells in an in vitro model,” International Journal of Pharmaceutics, vol. 298, no. 2, pp. 315–322, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. R. A. Benson, M. K. L. Macleod, B. G. Hale, A. Patakas, P. Garside, and J. M. Brewer, “Antigen presentation kinetics control T cell/dendritic cell interactions and follicular helper T cell generation in vivo,” eLife, vol. 4, Article ID e06994, 2015. View at Publisher · View at Google Scholar · View at Scopus
  29. S. D. Xiang, A. Scholzen, G. Minigo et al., “Pathogen recognition and development of particulate vaccines: does size matter?” Methods, vol. 40, no. 1, pp. 1–9, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Lappalainen, K. Tamminen, T. Vesikari, and V. Blazevic, “Comparative immunogenicity in mice of rotavirus VP6 tubular structures and virus-like particles,” Human Vaccines and Immunotherapeutics, vol. 9, no. 9, pp. 1991–2001, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Rodríguez, C. Wood, R. Sanchez-López, R. M. Castro-Acosta, O. T. Ramírez, and L. A. Palomares, “Understanding internalization of rotavirus VP6 nanotubes by cells: towards a recombinant vaccine,” Archives of Virology, vol. 159, no. 5, pp. 1005–1015, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Banchereau and R. M. Steinman, “Dendritic cells and the control of immunity,” Nature, vol. 392, no. 6673, pp. 245–252, 1998. View at Publisher · View at Google Scholar · View at Scopus
  33. P. J. Murray and T. A. Wynn, “Protective and pathogenic functions of macrophage subsets,” Nature Reviews Immunology, vol. 11, no. 11, pp. 723–737, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. V. L. MacKay and E. E. Moore, “Inventors. AnonymousImmortalized dendritic cells,” US patent. 1997.
  35. L. Huhti, V. Blazevic, K. Nurminen, T. Koho, V. P. Hytönen, and T. Vesikari, “A comparison of methods for purification and concentration of norovirus GII-4 capsid virus-like particles,” Archives of Virology, vol. 155, no. 11, pp. 1855–1858, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. L. Svensson, B. B. Finlay, D. Bass, C.-H. von Bonsdorff, and H. B. Greenberg, “Symmetric infection of rotavirus on polarized human intestinal epithelial (Caco-2) cells,” Journal of Virology, vol. 65, no. 8, pp. 4190–4197, 1991. View at Google Scholar · View at Scopus
  37. D. A. Hume, “The many alternative faces of macrophage activation,” Frontiers in Immunology, vol. 6, article 370, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. D. A. Hume, “Macrophages as APC and the dendritic cell myth,” The Journal of Immunology, vol. 181, no. 9, pp. 5829–5835, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Geginat, G. Nizzoli, M. Paroni et al., “Immunity to pathogens taught by specialized human dendritic cell subsets,” Frontiers in Immunology, vol. 6, article 527, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. R. M. Steinman, “The dendritic cell system and its role in immunogenicity,” Annual Review of Immunology, vol. 9, no. 1, pp. 271–296, 1991. View at Publisher · View at Google Scholar · View at Scopus
  41. N. L. Harris and F. Ronchese, “The role of B7 costimulation in T-cell immunity,” Immunology & Cell Biology, vol. 77, no. 4, pp. 304–311, 1999. View at Publisher · View at Google Scholar · View at Scopus
  42. V. Blazevic, C. M. Trubey, and G. M. Shearer, “Analysis of the costimulatory requirements for generating human virus-specific in vitro T helper and effector responses,” Journal of Clinical Immunology, vol. 21, no. 4, pp. 293–302, 2001. View at Publisher · View at Google Scholar · View at Scopus
  43. L. J. Berghaus, J. N. Moore, D. J. Hurley et al., “Innate immune responses of primary murine macrophage-lineage cells and RAW 264.7 cells to ligands of Toll-like receptors 2, 3, and 4,” Comparative Immunology, Microbiology and Infectious Diseases, vol. 33, no. 5, pp. 443–454, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Abe, H. Takahashi, H. Hamazaki, N. Miyano-Kurosaki, Y. Matsuura, and H. Takaku, “Baculovirus induces an innate immune response and confers protection from lethal influenza virus infection in mice,” Journal of Immunology, vol. 171, no. 3, pp. 1133–1139, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Istrate, I. Douagi, A. Charpilienne et al., “Bone marrow dendritic cells internalize live RF-81 bovine rotavirus and rotavirus-like particles (RF 2/6-GFP-VLP and RF 82/6/7-VLP) but are only activated by live bovine rotavirus,” Scandinavian Journal of Immunology, vol. 65, no. 6, pp. 494–502, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. P. Stoitzner, M. Zanella, U. Ortner et al., “Migration of langerhans cells and dermal dendritic cells in skin organ cultures: augmentation by TNF-α and IL-1β,” Journal of Leukocyte Biology, vol. 66, no. 3, pp. 462–470, 1999. View at Google Scholar · View at Scopus
  47. P. Rieckmann, J. M. Tuscano, and J. H. Kehrl, “Tumor necrosis factor-α (TNF-α) and interleukin-6 (IL-6) in B-lymphocyte function,” Methods, vol. 11, no. 1, pp. 128–132, 1997. View at Publisher · View at Google Scholar · View at Scopus
  48. B.-G. Xiao, C.-Z. Lu, and H. Link, “Cell biology and clinical promise of G-CSF: immunomodulation and neuroprotection,” Journal of Cellular and Molecular Medicine, vol. 11, no. 6, pp. 1272–1290, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Xu, M. Höglund, L. Hàkansson, and P. Venge, “Granulocyte colony-stimulating factor (G-CSF) induces the production of cytokines in vivo,” British Journal of Haematology, vol. 108, no. 4, pp. 848–853, 2000. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Xu, Y. Yang, C. Wang, and B. Jiang, “Rotavirus and coxsackievirus infection activated different profiles of toll-like receptors and chemokines in intestinal epithelial cells,” Inflammation Research, vol. 58, no. 9, pp. 585–592, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. E. E. Rollo, K. P. Kumar, N. C. Reich et al., “The epithelial cell response to rotavirus infection,” Journal of Immunology, vol. 163, no. 8, pp. 4442–4452, 1999. View at Google Scholar · View at Scopus
  52. I. Margine, L. Martinez-Gil, Y.-Y. Chou, and F. Krammer, “Residual baculovirus in insect cell-derived influenza virus-like particle preparations enhances immunogenicity,” PLoS ONE, vol. 7, no. 12, article e51559, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. T. Abe, H. Hemmi, H. Miyamoto et al., “Involvement of the Toll-like receptor 9 signaling pathway in the induction of innate immunity by baculovirus,” Journal of Virology, vol. 79, no. 5, pp. 2847–2858, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. E. M. Deal, K. Lahl, C. F. Narváez, E. C. Butcher, and H. B. Greenberg, “Plasmacytoid dendritic cells promote rotavirus-induced human and murine B cell responses,” The Journal of Clinical Investigation, vol. 123, no. 6, pp. 2464–2474, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. T. Fifis, A. Gamvrellis, B. Crimeen-Irwin et al., “Size-dependent immunogenicity: therapeutic and protective properties of nano-vaccines against tumors,” The Journal of Immunology, vol. 173, no. 5, pp. 3148–3154, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Mayor and R. E. Pagano, “Pathways of clathrin-independent endocytosis,” Nature Reviews Molecular Cell Biology, vol. 8, no. 8, pp. 603–612, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. C. Reis E Sousa, P. D. Stahl, and J. M. Austyn, “Phagocytosis of antigens by Langerhans cells in vitro,” The Journal of Experimental Medicine, vol. 178, no. 2, pp. 509–519, 1993. View at Publisher · View at Google Scholar · View at Scopus
  58. F. Sallusto, M. Cella, C. Danieli, and A. Lanzavecchia, “Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products,” Journal of Experimental Medicine, vol. 182, no. 2, pp. 389–400, 1995. View at Publisher · View at Google Scholar · View at Scopus
  59. R. M. Steinman and J. Swanson, “The endocytic activity of dendritic cells,” The Journal of Experimental Medicine, vol. 182, no. 2, pp. 283–288, 1995. View at Publisher · View at Google Scholar · View at Scopus
  60. L. Pelkmans and A. Helenius, “Endocytosis via caveolae,” Traffic, vol. 3, no. 5, pp. 311–320, 2002. View at Publisher · View at Google Scholar · View at Scopus
  61. Z. Liu and P. A. Roche, “Macropinocytosis in phagocytes: regulation of MHC class-II-restricted antigen presentation in dendritic cells,” Frontiers in Physiology, vol. 6, article 1, 2015. View at Publisher · View at Google Scholar · View at Scopus
  62. M. K. Ghosh, E. Dériaud, M.-F. Saron et al., “Induction of protective antiviral cytotoxic T cells by a tubular structure capable of carrying large foreign sequences,” Vaccine, vol. 20, no. 9-10, pp. 1369–1377, 2002. View at Publisher · View at Google Scholar · View at Scopus
  63. D. Vercauteren, R. E. Vandenbroucke, A. T. Jones et al., “The use of inhibitors to study endocytic pathways of gene carriers: optimization and pitfalls,” Molecular Therapy, vol. 18, no. 3, pp. 561–569, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. V. M. Pietiäinen, V. Marjomäki, J. Heino, and T. Hyypiä, “Viral entry, lipid rafts and caveosomes,” Annals of Medicine, vol. 37, no. 6, pp. 394–403, 2005. View at Publisher · View at Google Scholar · View at Scopus
  65. L. A. Mulcahy, R. C. Pink, and D. R. Carter, “Routes and mechanisms of extracellular vesicle uptake,” Journal of Extracellular Vesicles, vol. 3, Article ID 24641, 2014. View at Publisher · View at Google Scholar
  66. L. Buonaguro, M. L. Tornesello, M. Tagliamonte et al., “Baculovirus-derived human immunodeficiency virus type 1 virus-like particles activate dendritic cells and induce ex vivo T-cell responses,” Journal of Virology, vol. 80, no. 18, pp. 9134–9143, 2006. View at Publisher · View at Google Scholar · View at Scopus