Intradermal vaccination with un-adjuvanted sub-unit vaccines triggers skin innate immunity and confers protective respiratory immunity in domestic swine

Vaccine

Volumn 34, Issue 7, 2016, Pages 914-922

  Le Luduec, Jean Benoît ^a,b,c,d   Debeer, Sabine ^a,b,c,d   Piras, Fabienne ^e   Andréoni, Christine ^f   Boudet, Florence ^e   Laurent, Philippe ^g   Kaiserlian, Dominique ^a,b,c,d   Dubois, Bertrand ^a,b,c,d  

^a CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^b INSERM   (France)

^c UNIVERSITÉ DE LYON   (France)

^d CNRS   (France)

^e SANOFI PASTEUR   (France)

^f BOEHRINGER INGELHEIM PHARMA GMBH AND CO KG   (Germany)

^g BD Medical Pharmaceutical Systems   (France)

Author keywords

Anti viral immunity; Dendritic cells; Intradermal vaccination; Monocytes; Swine

Indexed keywords

ANTIBODY; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 2; PSEUDORABIES VACCINE; SUBUNIT VACCINE; TUMOR NECROSIS FACTOR ALPHA; VIRUS ANTIGEN; VIRUS GLYCOPROTEIN; CYTOKINE; NEUTRALIZING ANTIBODY; PSEUDORABIES VIRUS GLYCOPROTEINS; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN; VIRUS VACCINE;

ACTIVE IMMUNIZATION; ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY TITER; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DERMATITIS; DOMESTIC PIG; DRUG EFFECT; FEMALE; FLOW CYTOMETRY; HUMORAL IMMUNITY; IMMUNOHISTOCHEMISTRY; INFLAMMATORY INFILTRATE; INNATE IMMUNITY; MECHANICAL STRESS; MONOCYTE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTECTION; PSEUDORABIES; SKIN BIOPSY; SKIN STRUCTURE; UPREGULATION; VACCINATION; VIRAL RESPIRATORY TRACT INFECTION; ANIMAL; BLOOD; IMMUNOLOGY; INTRADERMAL DRUG ADMINISTRATION; PIG; PROCEDURES; SKIN;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CYTOKINES; DENDRITIC CELLS; FEMALE; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; IMMUNITY, INNATE; INJECTIONS, INTRADERMAL; PSEUDORABIES; SKIN; SWINE; VACCINATION; VACCINES, SUBUNIT; VIRAL ENVELOPE PROTEINS; VIRAL VACCINES;

EID: 84957805083     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2015.12.058     Document Type: Article

References (44)

1. + dermal dendritic cells. Immunity 2008, 29(Sep (3)):497-510.
2. Teunissen M.B., Haniffa M., Collin M.P. Insight into the immunobiology of human skin and functional specialization of skin dendritic cell subsets to innovate intradermal vaccination design. Curr Top Microbiol Immunol 2012, 351:25-76.
3. Liard C., Munier S., Arias M., Joulin-Giet A., Bonduelle O., Duffy D., et al. Targeting of HIV-p24 particle-based vaccine into differential skin layers induces distinct arms of the immune responses. Vaccine 2011, 29(Aug (37)):6379-6391.
4. Etchart N., Desmoulins P.O., Chemin K., Maliszewski C., Dubois B., Wild F., et al. Dendritic cells recruitment and in vivo priming of CD8(+) CTL induced by a single topical or transepithelial immunization via the Buccal mucosa with measles virus nucleoprotein. J Immunol 2001, 167(1):384-391.
5. Lambert P.H., Laurent P.E. Intradermal vaccine delivery: will new delivery systems transform vaccine administration?. Vaccine 2008, 26(Jun (26)):3197-3208.
6. Laurent P.E., Bonnet S., Alchas P., Regolini P., Mikszta J.A., Pettis R., et al. Evaluation of the clinical performance of a new intradermal vaccine administration technique and associated delivery system. Vaccine 2007, 25(Dec (52)):8833-8842.
7. Frenck R.W., Belshe R., Brady R.C., Winokur P.L., Campbell J.D., Treanor J., et al. Comparison of the immunogenicity and safety of a split-virion, inactivated, trivalent influenza vaccine (Fluzone(R)) administered by intradermal and intramuscular route in healthy adults. Vaccine 2011, 29(Aug (34)):5666-5674.
8. Ansaldi F., Canepa P., Ceravolo A., Valle L., de Florentiis D., Oomen R., et al. Intanza((R)) 15 mcg intradermal influenza vaccine elicits cross-reactive antibody responses against heterologous A(H3N2) influenza viruses. Vaccine 2012, 30(Apr (18)):2908-2913.
9. Icardi G., Orsi A., Ceravolo A., Ansaldi F. Current evidence on intradermal influenza vaccines administered by Soluvia licensed micro injection system. Hum Vaccin Immunother 2012, 8(1):67-75.
10. Holland D., Booy R., De Looze F., Eizenberg P., McDonald J., Karrasch J., et al. Intradermal influenza vaccine administered using a new microinjection system produces superior immunogenicity in elderly adults: a randomized controlled trial. J Infect Dis 2008, 198(Sep (5)):650-658.
11. Morelon E., Pouteil Noble C., Daoud S., Cahen R., Goujon-Henry C., Weber F., et al. Immunogenicity and safety of intradermal influenza vaccination in renal transplant patients who were non-responders to conventional influenza vaccination. Vaccine 2010, 28(Oct (42)):6885-6890.
12. Le Borgne M., Etchart N., Goubier A., Lira S.A., Sirard J.C., van Rooijen N., et al. Dendritic cells rapidly recruited into epithelial tissues via CCR6/CCL20 are responsible for CD8(+) T cell crosspriming in vivo. Immunity 2006, 24(2):191-201.
13. Kool M., Soullie T., van Nimwegen M., Willart M.A., Muskens F., Jung S., et al. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J Exp Med 2008, 205(4):869-882.
14. Mosca F., Tritto E., Muzzi A., Monaci E., Bagnoli F., Iavarone C., et al. Molecular and cellular signatures of human vaccine adjuvants. Proc Natl Acad Sci USA 2008, 105(Jul (30)):10501-10506.
15. Meurens F., Summerfield A., Nauwynck H., Saif L., Gerdts V. The pig: a model for human infectious diseases. Trends Microbiol 2012, 20(1):50-57.
16. Summerfield A., Meurens F., Ricklin M.E. The immunology of the porcine skin and its value as a model for human skin. Mol Immunol 2015, 66(Jul (1)):14-21.
17. Vardaxis N.J., Brans T.A., Boon M.E., Kreis R.W., Marres L.M. Confocal laser scanning microscopy of porcine skin: implications for human wound healing studies. J Anat 1997, 190(May (Pt 4)):601-611.
18. Debeer S., Le Luduec J.B., Kaiserlian D., Laurent P., Nicolas J.F., Dubois B., et al. Comparative histology and immunohistochemistry of porcine versus human skin. Eur J Dermatol: EJD 2013, 23(4):456-466.
19. Bautista E.M., Gregg D., Golde W.T. Characterization and functional analysis of skin-derived dendritic cells from swine without a requirement for in vitro propagation. Vet Immunol Immunopathol 2002, 88(Sep (3-4)):131-148.
20. Marquet F., Bonneau M., Pascale F., Urien C., Kang C., Schwartz-Cornil I., et al. Characterization of dendritic cells subpopulations in skin and afferent lymph in the swine model. PLoS ONE 2011, 6(1):e16320.
21. Zaba L.C., Fuentes-Duculan J., Steinman R.M., Krueger J.G., Lowes M.A. Normal human dermis contains distinct populations of CD11c+BDCA-1+ dendritic cells and CD163+FXIIIA+ macrophages. J Clin Invest 2007, 117(9):2517-2525.
22. Vandeputte J., Chappuis G., Fargeaud D., Precausta P., Guillemin F., Brun A., et al. Vaccination against pseudorabies with glycoprotein gI+ or glycoprotein gI- vaccine. Am J Vet Res 1990, 51(7):1100-1106.
23. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25(Dec (4)):402-408.
24. Ezquerra A., Revilla C., Alvarez B., Perez C., Alonso F., Dominguez J. Porcine myelomonocytic markers and cell populations. Dev Comp Immunol 2009, 33(3):284-298.
25. Bullido R., Alonso F., Gomez del Moral M., Ezquerra A., Alvarez B., Ortuno, et al. Monoclonal antibody 2F4/11 recognizes the alpha chain of a porcine beta 2 integrin involved in adhesion and complement mediated phagocytosis. J Immunol Methods 1996, 195(Sep (1-2)):125-134.
26. Coffman R.L., Sher A., Seder R.A. Vaccine adjuvants: putting innate immunity to work. Immunity 2010, 33(Oct (4)):492-503.
27. Brandtzaeg P., Johansen F.E. Mucosal B cells: phenotypic characteristics, transcriptional regulation, and homing properties. Immunol Rev 2005, 206(Aug):32-63.
28. Chakarov S., Fazilleau N. Monocyte-derived dendritic cells promote T follicular helper cell differentiation. EMBO Mol Med 2014, 6(5):590-603.
29. Weber F.C., Nemeth T., Csepregi J.Z., Dudeck A., Roers A., Ozsvari B., et al. Neutrophils are required for both the sensitization and elicitation phase of contact hypersensitivity. J Exp Med 2015, 212(1):15-22.
30. Nickoloff B.J., Naidu Y. Perturbation of epidermal barrier function correlates with initiation of cytokine cascade in human skin. J Am Acad Dermatol 1994, 30(4):535-546.
31. Dickel H., Gambichler T., Kamphowe J., Altmeyer P., Skrygan M. Standardized tape stripping prior to patch testing induces upregulation of Hsp90, Hsp70, IL-33, TNF-alpha and IL-8/CXCL8 mRNA: new insights into the involvement of 'alarmins'. Contact Dermatitis 2010, 63(Oct (4)):215-222.
32. del Pilar Martin M., Weldon W.C., Zarnitsyn V.G., Koutsonanos D.G., Akbari H., Skountzou I., et al. Local response to microneedle-based influenza immunization in the skin. MBio 2012, 3(2):e00012-e12.
33. Liu L., Zhou X., Shi J., Xie X., Yuan Z. Toll-like receptor-9 induced by physical trauma mediates release of cytokines following exposure to CpG motif in mouse skin. Immunology 2003, 110(Nov (3)):341-347.
34. Wang B., Amerio P., Sauder D.N. Role of cytokines in epidermal Langerhans cell migration. J Leukocyte Biol 1999, 66(Jul (1)):33-39.
35. Dubois B., Barthélémy C., Durand I., Liu Y.J., Caux C., Brière F. Towards a role of triggering cells in the germinal center reaction: triggering of B cell proliferation and isotype switching. J Immunol 1999, 162:3428-3436.
36. Abadie V., Badell E., Douillard P., Ensergueix D., Leenen P.J., Tanguy M., et al. Neutrophils rapidly migrate via lymphatics after Mycobacterium bovis BCG intradermal vaccination and shuttle live bacilli to the draining lymph nodes. Blood 2005, 106(Sep (5)):1843-1850.
37. Duffy D., Perrin H., Abadie V., Benhabiles N., Boissonnas A., Liard C., et al. Neutrophils transport antigen from the dermis to the bone marrow, initiating a source of memory CD8+ T cells. Immunity 2012, 37(Nov (5)):917-929.
38. Leon B., Lopez-Bravo M., Ardavin C. Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 2007, 26(4):519-531.
39. Soehnlein O., Lindbom L., Weber C. Mechanisms underlying neutrophil-mediated monocyte recruitment. Blood 2009, 114(Nov (21)):4613-4623.
40. Mantovani A., Cassatella M.A., Costantini C., Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol 2011, 11(8):519-531.
41. Beauvillain C., Delneste Y., Scotet M., Peres A., Gascan H., Guermonprez P., et al. Neutrophils efficiently cross-prime naive T cells in vivo. Blood 2007, 110(Oct (8)):2965-2973.
42. Yang C.W., Strong B.S., Miller M.J., Unanue E.R. Neutrophils influence the level of antigen presentation during the immune response to protein antigens in adjuvants. J Immunol 2010, 185(Sep (5)):2927-2934.
43. Chamorro S., Revilla C., Alvarez B., Alonso F., Ezquerra A., Dominguez J. Phenotypic and functional heterogeneity of porcine blood monocytes and its relation with maturation. Immunology 2005, 114(1):63-71.
44. Chamorro S., Revilla C., Gomez N., Alvarez B., Alonso F., Ezquerra A., et al. In vitro differentiation of porcine blood CD163- and CD163+ monocytes into functional dendritic cells. Immunobiology 2004, 209(1-2):57-65.