Antigen encoded by vaccine vectors derived from human adenovirus serotype 5 is preferentially presented to CD8 + T lymphocytes by the CD8α + dendritic cell subset

Vaccine

Volumn 29, Issue 35, 2011, Pages 5892-5903

  Suleman, Muhammad ^a   Galea, Sandra ^a   Gavard, Françoise ^a   Merillon, Nathalie ^b   Klonjkowski, Bernard ^a   Tartour, Eric ^b   Richardson, Jennifer ^a  

^a INRA   (France)

^b PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

Author keywords

Adenovirus; Dendritic cell; Vaccine vector

Indexed keywords

ADENOVIRUS VECTOR; BETA GALACTOSIDASE; CD8ALPHA ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; VACCINE;

ADENOVIRUS 5; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; ENZYME ACTIVITY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENE; VIRUS ATTACHMENT; VIRUS GENE;

ADENOVIRUSES, HUMAN; ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, CD8; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; DENDRITIC CELLS; FEMALE; GENETIC VECTORS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; OVALBUMIN; TRANSDUCTION, GENETIC; VACCINES;

EID: 79960720454     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.06.071     Document Type: Article

References (71)

1. Shiver J.W., Fu T.M., Chen L., Casimiro D.R., Davies M.E., Evans R.K., et al. Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity. Nature 2002, 415(6869):331-335.
2. Casimiro D.R., Chen L., Fu T.M., Evans R.K., Caulfield M.J., Davies M.E., et al. Comparative immunogenicity in rhesus monkeys of DNA plasmid, recombinant vaccinia virus, and replication-defective adenovirus vectors expressing a human immunodeficiency virus type 1 gag gene. J Virol 2003, 77(11):6305-6313.
3. Millar J., Dissanayake D., Yang T.C., Grinshtein N., Evelegh C., Wan Y., et al. The magnitude of the CD8+ T cell response produced by recombinant virus vectors is a function of both the antigen and the vector. Cell Immunol 2007, 250(1-2):55-67.
4. Liu J., Ewald B.A., Lynch D.M., Denholtz M., Abbink P., Lemckert A.A., et al. Magnitude and phenotype of cellular immune responses elicited by recombinant adenovirus vectors and heterologous prime-boost regimens in rhesus monkeys. J Virol 2008, 82(10):4844-4852.
5. Rhee E.G., Blattman J.N., Kasturi S.P., Kelley R.P., Kaufman D.R., Lynch D.M., et al. Multiple innate immune pathways contribute to the immunogenicity of recombinant adenovirus vaccine vectors. J Virol 2011, 85(1):315-323.
6. Fejer G., Drechsel L., Liese J., Schleicher U., Ruzsics Z., Imelli N., et al. Key role of splenic myeloid DCs in the IFN-alphabeta response to adenoviruses in vivo. PLoS Pathog 2008, 4(11):e1000208.
7. Muruve D.A., Petrilli V., Zaiss A.K., White L.R., Clark S.A., Ross P.J., et al. The inflammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature 2008, 452(7183):103-107.
8. Steinman R.M., Gutchinov B., Witmer M.D., Nussenzweig M.C. Dendritic cells are the principal stimulators of the primary mixed leukocyte reaction in mice. J Exp Med 1983, 157(2):613-627.
9. Asselin-Paturel C., Boonstra A., Dalod M., et al. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat Immunol 2001, 2(12):1144-1150.
10. Grouard G., Rissoan M.C., Filgueira L., Durand I., Banchereau J., Liu Y.J. The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand. J Exp Med 1997, 185(6):1101-1111.
11. Nakano H., Yanagita M., Gunn M.D. CD11c(+)B220(+)Gr-1(+) cells in mouse lymph nodes and spleen display characteristics of plasmacytoid dendritic cells. J Exp Med 2001, 194(8):1171-1178.
12. O'Keeffe M., Hochrein H., Vremec D., Caminschi I., Miller J.L., Anders E.M., et al. Mouse plasmacytoid cells: long-lived cells, heterogeneous in surface phenotype and function, that differentiate into CD8(+) dendritic cells only after microbial stimulus. J Exp Med 2002, 196(10):1307-1319.
13. Villadangos J.A., Young L. Antigen-presentation properties of plasmacytoid dendritic cells. Immunity 2008, 29(3):352-361.
14. Heath W.R., Carbone F.R. Dendritic cell subsets in primary and secondary T cell responses at body surfaces. Nat Immunol 2009, 10(12):1237-1244.
15. Walton K.L., He J., Kelsall B.L., Sartor R.B., Fisher N.C. Dendritic cells in germ-free and specific pathogen-free mice have similar phenotypes and in vitro antigen presenting function. Immunol Lett 2006, 102(1):16-24.
16. Wilson N.S., Young L.J., Kupresanin F., Naik S.H., Vremec D., Heath W.R., et al. Normal proportion and expression of maturation markers in migratory dendritic cells in the absence of germs or Toll-like receptor signaling. Immunol Cell Biol 2008, 86(2):200-205.
17. Diao J., Winter E., Cantin C., Chen W., Xu L., Kelvin D., et al. In situ replication of immediate dendritic cell (DC) precursors contributes to conventional DC homeostasis in lymphoid tissue. J Immunol 2006, 176(12):7196-7206.
18. Liu K., Waskow C., Liu X., Yao K., Hoh J., Nussenzweig M. Origin of dendritic cells in peripheral lymphoid organs of mice. Nat Immunol 2007, 8(6):578-583.
19. Naik S.H., Metcalf D., van Nieuwenhuijze A., Wicks I., Wu L., O'Keeffe M., et al. Intrasplenic steady-state dendritic cell precursors that are distinct from monocytes. Nat Immunol 2006, 7(6):663-671.
20. Vremec D., Pooley J., Hochrein H., Wu L., Shortman K. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J Immunol 2000, 164(6):2978-2986.
21. Maldonado-Lopez R., De Smedt T., Michel P., Godfroid J., Pajak B., Heirman C., et al. CD8alpha+ and CD8alpha- subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J Exp Med 1999, 189(3):587-592.
22. den Haan J.M., Lehar S.M., Bevan M.J. CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J Exp Med 2000, 192(12):1685-1696.
23. Pooley J.L., Heath W.R., Shortman K. Cutting edge: intravenous soluble antigen is presented to CD4 T cells by CD8- dendritic cells, but cross-presented to CD8 T cells by CD8+ dendritic cells. J Immunol 2001, 166(9):5327-5330.
24. Schnorrer P., Behrens G.M., Wilson N.S., Pooley J.L., Smith C.M., El Sukkari D., et al. The dominant role of CD8+ dendritic cells in cross-presentation is not dictated by antigen capture. Proc Natl Acad Sci USA 2006, 103(28):10729-10734.
25. Dudziak D., Kamphorst A.O., Heidkamp G.F., Buchholz V.R., Trumpfheller C., Yamazaki S., et al. Differential antigen processing by dendritic cell subsets in vivo. Science 2007, 315(5808):107-111.
26. Poulin L.F., Salio M., Griessinger E., Anjos-Afonso F., Craciun L., Chen J.L., et al. Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha+ dendritic cells. J Exp Med 2010, 207(6):1261-1271.
27. Bachem A., Guttler S., Hartung E., Ebstein F., Schaefer M., Tannert A., et al. Superior antigen cross-presentation and XCR1 expression define human CD11c+CD141+ cells as homologues of mouse CD8+ dendritic cells. J Exp Med 2010, 207(6):1273-1281.
28. Contreras V., Urien C., Guiton R., Alexandre Y., Vu Manh T.P., Andrieu T., et al. Existence of CD8alpha-like dendritic cells with a conserved functional specialization and a common molecular signature in distant mammalian species. J Immunol 2010, 185(6):3313-3325.
29. Crozat K., Guiton R., Contreras V., Feuillet V., Dutertre C.A., Ventre E., et al. The XC chemokine receptor 1 is a conserved selective marker of mammalian cells homologous to mouse CD8alpha+ dendritic cells. J Exp Med 2010, 207(6):1283-1292.
30. Jongbloed S.L., Kassianos A.J., McDonald K.J., Clark G.J., Ju X., Angel C.E., et al. Human CD141+ (BDCA-3)+ dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J Exp Med 2010, 207(6):1247-1260.
31. Allan R.S., Smith C.M., Belz G.T., van Lint A.L., Wakim L.M., Heath W.R., et al. Epidermal viral immunity induced by CD8alpha+ dendritic cells but not by Langerhans cells. Science 2003, 301(5641):1925-1928.
32. Belz G.T., Smith C.M., Eichner D., Shortman K., Karupiah G., Carbone F.R., et al. Cutting edge: conventional CD8 alpha+ dendritic cells are generally involved in priming CTL immunity to viruses. J Immunol 2004, 172(4):1996-2000.
33. Smith C.M., Belz G.T., Wilson N.S., Villadangos J.A., Shortman K., Carbone F.R., et al. Cutting edge: conventional CD8 alpha+ dendritic cells are preferentially involved in CTL priming after footpad infection with herpes simplex virus-1. J Immunol 2003, 170(9):4437-4440.
34. Belz G.T., Smith C.M., Kleinert L., Reading P., Brooks A., Shortman K., et al. Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc Natl Acad Sci USA 2004, 101(23):8670-8675.
35. Allan R.S., Waithman J., Bedoui S., Jones C.M., Villadangos J.A., Zhan Y., et al. Migratory dendritic cells transfer antigen to a lymph node-resident dendritic cell population for efficient CTL priming. Immunity. 2006, 25(1):153-162.
36. Hildner K., Edelson B.T., Purtha W.E., Diamond M., Matsushita H., Kohyama M., et al. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 2008, 322(5904):1097-1100.
37. Lindsay R.W., Darrah P.A., Quinn K.M., Wille-Reece U., Mattei L.M., Iwasaki A., et al. CD8+ T cell responses following replication-defective adenovirus serotype 5 immunization are dependent on CD11c+ dendritic cells but show redundancy in their requirement of TLR and nucleotide-binding oligomerization domain-like receptor signaling. J Immunol 2010, 185(3):1513-1521.
38. Graham F.L., Smiley J., Russell W.C., Nairn R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol 1977, 36(1):59-74.
39. Moore M.W., Carbone F.R., Bevan M.J. Introduction of soluble protein into the class I pathway of antigen processing and presentation. Cell 1988, 54(6):777-785.
40. Karttunen J., Sanderson S., Shastri N. Detection of rare antigen-presenting cells by the lacZ T-cell activation assay suggests an expression cloning strategy for T-cell antigens. Proc Natl Acad Sci USA 1992, 89(13):6020-6024.
41. Haicheur N., Benchetrit F., Amessou M., Leclerc C., Falguieres T., Fayolle C., et al. The B subunit of Shiga toxin coupled to full-size antigenic protein elicits humoral and cell-mediated immune responses associated with a Th1-dominant polarization. Int Immunol 2003, 15(10):1161-1171.
42. Winzler C., Rovere P., Rescigno M., Granucci F., Penna G., Adorini L., et al. Maturation stages of mouse dendritic cells in growth factor-dependent long-term cultures. J Exp Med 1997, 185(2):317-328.
43. Kozak M. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 1986, 44(2):283-292.
44. Chartier C., Degryse E., Gantzer M., Dieterle A., Pavirani A., Mehtali M. Efficient generation of recombinant adenovirus vectors by homologous recombination in Escherichia coli. J Virol 1996, 70(7):4805-4810.
45. Sweeney J.A., Hennessey J.P. Evaluation of accuracy and precision of adenovirus absorptivity at 260nm under conditions of complete DNA disruption. Virology 2002, 295(2):284-288.
46. Liu F., Song Y., Liu D. Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene Ther 1999, 6(7):1258-1266.
47. Zhang G., Budker V., Wolff J.A. High levels of foreign gene expression in hepatocytes after tail vein injections of naked plasmid DNA. Hum Gene Ther 1999, 10(10):1735-1737.
48. He Y., Pimenov A.A., Nayak J.V., Plowey J., Falo L.D., Huang L. Intravenous injection of naked DNA encoding secreted flt3 ligand dramatically increases the number of dendritic cells and natural killer cells in vivo. Hum Gene Ther 2000, 11(4):547-554.
49. Lyman S.D., James L., Vanden Bos T., de Vries P., Brasel K., Gliniak B., et al. Molecular cloning of a ligand for the flt3/flk-2 tyrosine kinase receptor: a proliferative factor for primitive hematopoietic cells. Cell 1993, 75(6):1157-1167.
50. Maraskovsky E., Brasel K., Teepe M., Roux E.R., Lyman S.D., Shortman K., et al. Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell subpopulations identified. J Exp Med 1996, 184(5):1953-1962.
51. Haicheur N., Bismuth E., Bosset S., Adotevi O., Warnier G., Lacabanne V., et al. The B subunit of Shiga toxin fused to a tumor antigen elicits CTL and targets dendritic cells to allow MHC class I-restricted presentation of peptides derived from exogenous antigens. J Immunol 2000, 165(6):3301-3308.
52. Vingert B., Adotevi O., Patin D., Jung S., Shrikant P., Freyburger L., et al. The Shiga toxin B-subunit targets antigen in vivo to dendritic cells and elicits anti-tumor immunity. Eur J Immunol 2006, 36(5):1124-1135.
53. McKenna H.J., Stocking K.L., Miller R.E., Brasel K., De Smedt T., Maraskovsky E., et al. Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood 2000, 95(11):3489-3497.
54. O'Keeffe M., Hochrein H., Vremec D., Pooley J., Evans R., Woulfe S., et al. Effects of administration of progenipoietin 1, Flt-3 ligand, granulocyte colony-stimulating factor, and pegylated granulocyte-macrophage colony-stimulating factor on dendritic cell subsets in mice. Blood 2002, 99(6):2122-2130.
55. Wilson N.S., Behrens G.M., Lundie R.J., Smith C.M., Waithman J., Young L., et al. Systemic activation of dendritic cells by Toll-like receptor ligands or malaria infection impairs cross-presentation and antiviral immunity. Nat Immunol 2006, 7(2):165-172.
56. Bergelson J.M., Cunningham J.A., Droguett G., Kurt-Jones E.A., Krithivas A., Hong J.S., et al. Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science 1997, 275(5304):1320-1323.
57. Burgert H.G., Maryanski J.L., Kvist S. " E3/19K" protein of adenovirus type 2 inhibits lysis of cytolytic T lymphocytes by blocking cell-surface expression of histocompatibility class I antigens. Proc Natl Acad Sci USA 1987, 84(5):1356-1360.
58. Porgador A., Yewdell J.W., Deng Y., Bennink J.R., Germain R.N. Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity 1997, 6(6):715-726.
59. Pulendran B., Ahmed R. Translating innate immunity into immunological memory: implications for vaccine development. Cell 2006, 124(4):849-863.
60. Luber C.A., Cox J., Lauterbach H., Fancke B., Selbach M., Tschopp J., et al. Quantitative proteomics reveals subset-specific viral recognition in dendritic cells. Immunity 2010, 32(2):279-289.
61. Segura E., Villadangos J.A. Antigen presentation by dendritic cells in vivo. Curr Opin Immunol 2009, 21(1):105-110.
62. Mount A.M., Smith C.M., Kupresanin F., Stoermer K., Heath W.R., Belz G.T. Multiple dendritic cell populations activate CD4+ T cells after viral stimulation. PLoS ONE 2008, 3(2):e1691.
63. Mercier S., Verhaagh S., Goudsmit J., Lemckert A., Monteil M., Havenga M., et al. Adenovirus fibre exchange alters cell tropism in vitro but not transgene-specific T CD8+ immune responses in vivo. J Gen Virol 2004, 85(Pt 5):1227-1236.
64. Cheng C., Gall J.G., Kong W.P., Sheets R.L., Gomez P.L., King C.R., et al. Mechanism of ad5 vaccine immunity and toxicity: fiber shaft targeting of dendritic cells. PLoS Pathog 2007, 3(2):e25.
65. Baker A.H., McVey J.H., Waddington S.N., Di Paolo N.C., Shayakhmetov D.M. The influence of blood on in vivo adenovirus bio-distribution and transduction. Mol Ther 2007, 15(8):1410-1416.
66. Savina A., Peres A., Cebrian I., Carmo N., Moita C., Hacohen N., et al. The small GTPase Rac2 controls phagosomal alkalinization and antigen crosspresentation selectively in CD8(+) dendritic cells. Immunity 2009, 30(4):544-555.
67. Schulz O. Reis e Sousa Cross-presentation of cell-associated antigens by CD8alpha+ dendritic cells is attributable to their ability to internalize dead cells. Immunology 2002, 107(2):183-189.
68. Iyoda T., Shimoyama S., Liu K., Omatsu Y., Akiyama Y., Maeda Y., et al. The CD8+ dendritic cell subset selectively endocytoses dying cells in culture and in vivo. J Exp Med 2002, 195(10):1289-1302.
69. Matheoud D., Perie L., Hoeffel G., Vimeux L., Parent I., Maranon C., et al. Cross-presentation by dendritic cells from live cells induces protective immune responses in vivo. Blood 2010, 115(22):4412-4420.
70. Shortman K., Heath W.R. The CD8+ dendritic cell subset. Immunol Rev 2010, 234(1):18-31.
71. Anjuere F., Martin P., Ferrero I., Fraga M.L., Del Hoyo G.M., Wright N., et al. Definition of dendritic cell subpopulations present in the spleen Peyer's patches, lymph nodes, and skin of the mouse. Blood 1999, 93(2):590-598.