Different HIV pox viral vector-based vaccines and adjuvants can induce unique antigen presenting cells that modulate CD8 T cell avidity

Virology

Volumn 468, Issue , 2014, Pages 479-489

  Trivedi, Shubhanshi ^a   Jackson, Ronald J ^a   Ranasinghe, Charani ^a  

^a Biology and Environment   (Australia)

Author keywords

CD8+ T cell avidity; HIV vaccines; IL 13R 2 IL 4R antagonist; Lung dendritic cells; Poxvirus vectors

Indexed keywords

CD103 ANTIGEN; CD11B ANTIGEN; CD64 ANTIGEN; GLYCOPROTEIN P 15095; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 13; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; POXVIRUS VECTOR; ALPHA E INTEGRINS; ALPHA INTEGRIN; INTERLEUKIN 4 RECEPTOR TYPE II; LEUKOCYTE ANTIGEN;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LUNG DERIVED DENDRITIC CELL; MOUSE; NONHUMAN; RESPIRATORY TRACT MUCOSA; VACCINATION; VIRUS IMMUNITY; ANIMAL; BAGG ALBINO MOUSE; CYTOLOGY; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; METABOLISM; PHYSIOLOGY;

POXVIRIDAE;

ADJUVANTS, IMMUNOLOGIC; ADOPTIVE TRANSFER; AIDS VACCINES; ANIMALS; ANTIGEN-PRESENTING CELLS; ANTIGENS, CD; ANTIGENS, CD11B; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; INTEGRIN ALPHA CHAINS; INTERLEUKIN-13; LUNG; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; RECEPTORS, INTERLEUKIN-4, TYPE II; RESPIRATORY MUCOSA;

EID: 84907482378     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.09.004     Document Type: Article

References (70)

1. Ballesteros-Tato A., Leon B., Lund F.E., Randall T.D. Temporal changes in dendritic cell subsets, cross-priming and costimulation via CD70 control CD8(+) T cell responses to influenza. Nat. Immunol. 2010, 11:216-224.
2. Beaty S.R., Rose C.E., Sung S.S. Diverse and potent chemokine production by lung CD11bhigh dendritic cells in homeostasis and in allergic lung inflammation. J. Immunol. 2007, 178:1882-1895.
3. Beauchamp N.M., Busick R.Y., Alexander-Miller M.A. Functional divergence among CD103+ dendritic cell subpopulations following pulmonary poxvirus infection. J. Virol. 2010, 84:10191-10199.
4. Beauchamp N.M., Yammani R.D., Alexander-Miller M.A. CD8 marks a subpopulation of lung-derived dendritic cells with differential responsiveness to viral infection and toll-like receptor stimulation. J. Virol. 2012, 86:10640-10650.
5. Bedoui S., Whitney P.G., Waithman J., Eidsmo L., Wakim L., Caminschi I., Allan R.S., Wojtasiak M., Shortman K., Carbone F.R., Brooks A.G., Heath W.R. Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat. Immunol. 2009, 10:488-495.
6. Belyakov I.M., Derby M.A., Ahlers J.D., Kelsall B.L., Earl P., Moss B., Strober W., Berzofsky J.A. Mucosal immunization with HIV-1 peptide vaccine induces mucosal and systemic cytotoxic T lymphocytes and protective immunity in mice against intrarectal recombinant HIV-vaccinia challenge. P. Natl. Acad. Sci. USA 1998, 95:1709-1714.
7. Belyakov I.M., Kuznetsov V.A., Kelsall B., Klinman D., Moniuszko M., Lemon M., Markham P.D., Pal R., Clements J.D., Lewis M.G., Strober W., Franchini G., Berzofsky J.A. Impact of vaccine-induced mucosal high-avidity CD8+ CTLs in delay of AIDS viral dissemination from mucosa. Blood 2006, 107:3258-3264.
8. Belz G.T. Cutting edge: Conventional CD8[alpha]+ dendritic cells are generally involved in priming CTL immunity to viruses. J. Immunol. 2004, 172:1996-2000.
9. Belz G.T. 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, 101:8670-8675.
10. Belz G.T., Bedoui S., Kupresanin F., Carbone F.R., Heath W.R. Minimal activation of memory CD8+ T cell by tissue-derived dendritic cells favors the stimulation of naive CD8+ T cells. Nat. Immunol. 2007, 8:1060-1066.
11. Benlahrech A., Harris J., Meiser A., Papagatsias T., Hornig J., Hayes P., Lieber A., Athanasopoulos T., Bachy V., Csomor E., Daniels R., Fisher K., Gotch F., Seymour L., Logan K., Barbagallo R., Klavinskis L., Dickson G., Patterson S. Adenovirus vector vaccination induces expansion of memory CD4 T cells with a mucosal homing phenotype that are readily susceptible to HIV-1. Proc. Natl. Acad. Sci. USA 2009, 106:19940-19945.
12. Betts M.R., Nason M.C., West S.M., De Rosa S.C., Migueles S.A., Abraham J., Lederman M.M., Benito J.M., Goepfert P.A., Connors M., Roederer M., Koup R.A. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 2006, 107:4781-4789.
13. Boyle D.B., Coupar B.E. Construction of recombinant fowlpox viruses as vectors for poultry vaccines. Virus Res. 1988, 10:343-356.
14. Buchbinder S.P., Mehrotra D.V., Duerr A., Fitzgerald D.W., Mogg R., Li D., Gilbert P.B., Lama J.R., Marmor M., Del Rio C., McElrath M.J., Casimiro D.R., Gottesdiener K.M., Chodakewitz J.A., Corey L., Robertson M.N., Step Study Protocol T. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 2008, 372:1881-1893.
15. Clark R.H., Kenyon J.C., Bartlett N.W., Tscharke D.C., Smith G.L. Deletion of gene A41L enhances vaccinia virus immunogenicity and vaccine efficacy. J. Gen. Virol. 2006, 87:29-38.
16. Cook P.C., Jones L.H., Jenkins S.J., Wynn T.A., Allen J.E., MacDonald A.S. Alternatively activated dendritic cells regulate CD4(+) T-cell polarization in vitro and in vivo. Proc. Natl. Acad. Sci. USA 2012, 109:9977-9982.
17. Coupar B., Purcell D., Thomson S., Ramshaw I., Kent S., Boyle D. Fowlpox virus vaccines for HIV and SHIV clinical and pre-clinical trials. Vaccine 2006, 24:1378-1388.
18. del Rio M.L., Rodriguez-Barbosa J.I., Kremmer E., Forster R. CD103(-) and CD103(+) bronchial lymph node dendritic cells are specialized in presenting and cross-presenting innocuous antigen to CD4(+) and CD8(+) T cells. J. Immunol. 2007, 178:6861-6866.
19. den Haan J.M., Bevan M.J. Constitutive versus activation-dependent cross-presentation of immune complexes by CD8+ and CD8- dendritic cells in vivo. J. Exp. Med. 2002, 196:817-827.
20. 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, 192:1685-1696.
21. Desch A.N., Henson P.M., Jakubzick C.V. Pulmonary dendritic cell development and antigen acquisition. Immunol. Res. 2013, 55:178-186.
22. Falivene J., DEL Medico Zajac M.P., Pascutti M.F., Rodriguez A.M., Maeto C., Perdiguero B., Gomez C.E., Esteban M., Calamante G., Gherardi M.M Improving the MVA vaccine potential by deleting the viral gene coding for the IL-18 binding protein. PloS One 2012, 7:e32220.
23. Furuhashi K., Suda T., Hasegawa H., Suzuki Y., Hashimoto D., Enomoto N., Fujisawa T., Nakamura Y., Inui N., Shibata K., Nakamura H., Chida K. Mouse lung CD103+ and CD11bhigh dendritic cells preferentially induce distinct CD4+ T-cell responses. Am. J. Respir. Cell Mol. Biol. 2012, 46:165-172.
24. Garcia-Arriaza J., Najera J.L., Gomez C.E., Tewabe N., Sorzano C.O., Calandra T., Roger T., Esteban M. A candidate HIV/AIDS vaccine (MVA-B) lacking vaccinia virus gene C6L enhances memory HIV-1-specific T-cell responses. PloS One 2011, 6:e24244.
25. Geurts van Kessel C.H., Willart M.A., van Rijt L.S., Muskens F., Kool M., Baas C., Thielemans K., Bennett C., Clausen B.E., Hoogsteden H.C., Osterhaus A.D., Rimmelzwaan G.F., Lambrecht B.N. Clearance of influenza virus from the lung depends on migratory langerin+CD11b- but not plasmacytoid dendritic cells. J. Exp Med. 2008, 205:1621-1634.
26. Gomez C.E., Perdiguero B., Garcia-Arriaza J., Esteban M. Clinical applications of attenuated MVA poxvirus strain. Expert Rev. Vaccin. 2013.
27. Guilliams M., Lambrecht B.N., Hammad H. Division of labor between lung dendritic cells and macrophages in the defense against pulmonary infections. Mucosal Immunol. 2013, 6:464-473.
28. Heath W.R., Carbone F.R. Dendritic cell subsets in primary and secondary T cell responses at body surfaces. Nat. Immunol. 2009, 10:1237-1244.
29. Hervouet C., Luci C., Bekri S., Juhel T., Bihl F., Braud V.M., Czerkinsky C., Anjuere F. Antigen-bearing dendritic cells from the sublingual mucosa recirculate to distant systemic lymphoid organs to prime mucosal CD8 T cells. Mucosal Immunol. 2014, 7:280-291.
30. Ho A.W., Prabhu N., Betts R.J., Ge M.Q., Dai X., Hutchinson P.E., Lew F.C., Wong K.L., Hanson B.J., Macary P.A., Kemeny D.M. Lung CD103+ dendritic cells efficiently transport influenza virus to the lymph node and load viral antigen onto MHC class I for presentation to CD8 T cells. J. Immunol. 2011, 187:6011-6021.
31. Hohl T.M., Rivera A., Lipuma L., Gallegos A., Shi C., Mack M., Pamer E.G. Inflammatory monocytes facilitate adaptive CD4 T cell responses during respiratory fungal infection. Cell Host Microbe 2009, 6:470-481.
32. Iijima N., Mattei L.M., Iwasaki A. Recruited inflammatory monocytes stimulate antiviral Th1 immunity in infected tissue. Proc. Natl. Acad. Sci. USA 2011, 108:284-289.
33. Jackson R.J., Boyle D.B., Ranasinghe C. Progresses in DNA-Based Heterologous Prime-Boost Immunization Strategies. Methods Mol. Biol. 2014, 1143:61-90.
34. Jackson R.J., Worley M., Trivedi S., Ranasinghe C. Novel HIV IL-4R antagonist vaccine strategy can induce both high avidity CD8 T and B cell immunity with greater protective efficacy. Vaccine 2014, 32:5703-5714.
35. Jenkins S.J., Ruckerl D., Thomas G.D., Hewitson J.P., Duncan S., Brombacher F., Maizels R.M., Hume D.A., Allen J.E. IL-4 directly signals tissue-resident macrophages to proliferate beyond homeostatic levels controlled by CSF-1. J. Exp. Med. 2013, 210:2477-2491.
36. Jeyanathan M., Damjanovic D., Shaler C.R., Lai R., Wortzman M., Yin C., Zganiacz A., Lichty B.D., Xing Z. Differentially imprinted innate immunity by mucosal boost vaccination determines antituberculosis immune protective outcomes, independent of T-cell immunity. Mucosal Immunol. 2013, 6:612-625.
37. Keefer M.C., Frey S.E., Elizaga M., Metch B., De Rosa S.C., Barroso P.F., Tomaras G., Cardinali M., Goepfert P., Kalichman A., Philippon V., McElrath M.J., Jin X., Ferrari G., Defawe O.D., Mazzara G.P., Montefiori D., Pensiero M., Panicali D.L., Corey L., Network N.H.V.T. A phase I trial of preventive HIV vaccination with heterologous poxviral-vectors containing matching HIV-1 inserts in healthy HIV-uninfected subjects. Vaccine 2011, 29:1948-1958.
38. Kelleher A.D., Puls R.L., Bebbington M., Boyle D., Ffrench R., Kent S.J., Kippax S., Purcell D.F., Thomson S., Wand H., Cooper D.A., Emery S. A randomized, placebo-controlled phase I trial of DNA prime, recombinant fowlpox virus boost prophylactic vaccine for HIV-1. Aids 2006, 20:294-297.
39. Kent S.J., Dale C.J., Ranasinghe C., Stratov I., de Rose R., Chea S., Montefiori D.C., Thomson S., Ramshaw I.A., Coupar B.E.H., Boyle D.B., Law M., Wilson K.M., Ramsay A.J. Mucosally-administered human-simian immunodeficiency virus DNA and fowlpoxvirus-based recombinant vaccines reduce acute phase viral replication in macaques following vaginal challenge with CCR5-tropic SHIVSF162P3. Vaccine 2005, 23:5009-5021.
40. Kim T.S., Braciale T.J. Respiratory dendritic cell subsets differ in their capacity to support the induction of virus-specific cytotoxic CD8(+) T Cell responses. PloS One 2009, 4.
41. Kozlowski P.A., Neutra M.R. The role of mucosal immunity in prevention of HIV transmission. Curr. Mol. Med. 2003, 3:217-228.
42. Kroger C.J., Amoah S., Alexander-Miller M.A. Cutting edge: dendritic cells prime a high avidity CTL response independent of the level of presented antigen. J. Immunol. 2008, 180:5784-5788.
43. Lambrecht B.N., Hammad H. Lung dendritic cells in respiratory viral infection and asthma: from protection to immunopathology. Ann. Rev Immunol. 2012, 30:243-270.
44. Landsman L., Jung S. Lung macrophages serve as obligatory intermediate between blood monocytes and alveolar macrophages. J. Immunol. 2007, 179:3488-3494.
45. Lee H.K. Differential roles of migratory and resident DCs in T cell priming after mucosal or skin HSV-1 infection. J. Exp. Med. 2009, 206:359-370.
46. 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, 26:519-531.
47. Lipscomb M.F., Lyons C.R., Nunez G., Ball E.J., Stastny P., Vial W., Lem V., Weissler J., Miller L.M., Toews G.B. Human alveolar macrophages-Hla-Dr-positive macrophages that are poor stimulators of a primary mixed leukocyte reaction. J. Immunol. 1986, 136:497-504.
48. Mata M., Travers P.J., Liu Q., Frankel F.R., Paterson Y. The MHC class I-restricted immune response to HIV-gag in BALB/c mice selects a single epitope that does not have a predictable MHC-binding motif and binds to Kd through interactions between a glutamine at P3 and pocket D. J. Immunol. 1998, 161:2985-2993.
49. Misharin A.V., Morales-Nebreda L., Mutlu G.M., Budinger G.R., Perlman H. Flow cytometric analysis of macrophages and dendritic cell subsets in the mouse lung. Am. J. Respir. Cell Mol. Biol. 2013, 49:503-510.
50. Moron G., Rueda P., Casal I., Leclerc C. CD8alpha- CD11b+ dendritic cells present exogenous virus-like particles to CD8+ T cells and subsequently express CD8alpha and CD205 molecules. J. Exp. Med. 2002, 195:1233-1245.
51. Nakano H., Lin K.L., Yanagita M., Charbonneau C., Cook D.N., Kakiuchi T., Gunn M.D. Blood-derived inflammatory dendritic cells in lymph nodes stimulate acute T helper type 1 immune responses. Nat. Immunol. 2009, 10:394-402.
52. Pillai V.K., Kannanganat S., Penaloza-Macmaster P., Chennareddi L., Robinson H.L., Blackwell J., Amara R.R. Different patterns of expansion, contraction and memory differentiation of HIV-1 Gag-specific CD8 T cells elicited by adenovirus type 5 and modified vaccinia Ankara vaccines. Vaccine 2011, 29:5399-5406.
53. Plantinga M., Guilliams M., Vanheerswynghels M., Deswarte K., Branco-Madeira F., Toussaint W., Vanhoutte L., Neyt K., Killeen N., Malissen B., Hammad H., Lambrecht B.N. Conventional and monocyte-derived CD11b(+) dendritic cells initiate and maintain T helper 2 cell-mediated immunity to house dust mite allergen. Immunity 2013, 38:322-335.
54. Ranasinghe C., Eyers F., Stambas J., Boyle D.B., Ramshaw I.A., Ramsay A.J. A comparative analysis of HIV-specific mucosal/systemic T cell immunity and avidity following rDNA/rFPV and poxvirus-poxvirus prime boost immunisations. Vaccine 2011, 29:3008-3020.
55. Ranasinghe C., Medveczky J.C., Woltring D., Gao K., Thomson S., Coupar B.E., Boyle D.B., Ramsay A.J., Ramshaw I.A. Evaluation of fowlpox-vaccinia virus prime-boost vaccine strategies for high-level mucosal and systemic immunity against HIV-1. Vaccine 2006, 24:5881-5895.
56. Ranasinghe C., Ramshaw I.A. Immunization route-dependent expression of IL-4/IL-13 can modulate HIV-specific CD8(+) CTL avidity. Eur. J. Immunol. 2009, 39:1819-1830.
57. Ranasinghe C., Trivedi S., Stambas J., Jackson R.J. Unique IL-13Ralpha2-based HIV-1 vaccine strategy to enhance mucosal immunity, CD8(+) T-cell avidity and protective immunity. Mucosal Immunol 2013.
58. Ranasinghe C., Trivedi S., Wijesundara D.K. and Jackson R.J., IL-4 and IL-13 receptors: Roles in immunity and powerful vaccine adjuvants, Cytokine Growth Factor Rev., in press. http://dx.doi.org/10.1016/j.cytogfr.2014.07.010.
59. Ranasinghe C., Turner S.J., McArthur C., Sutherland D.B., Kim J.H., Doherty P.C., Ramshaw I.A. Mucosal HIV-1 pox virus prime-boost immunization induces high-avidity CD8+ T cells with regime-dependent cytokine/granzyme B profiles. J. Immunol. 2007, 178:2370-2379.
60. Shacklett B.L., Ferre A.L. Mucosal immunity in HIV controllers: the right place at the right time. Curr. Opin. Hiv. Aids. 2011, 6:202-207.
61. Skinner M.A., Laidlaw S.M., Eldaghayes I., Kaiser P., Cottingham M.G. Fowlpox virus as a recombinant vaccine vector for use in mammals and poultry. Expert Rev. Vaccin. 2005, 4:63-76.
62. Smyth L.A., Hervouet C., Hayday T., Becker P.D., Ellis R., Lechler R.I., Lombardi G., Klavinskis L.S. Acquisition of MHC:peptide complexes by dendritic cells contributes to the generation of antiviral CD8(+) T Cell immunity in vivo. J. Immunol. 2012, 189:2274-2282.
63. Somogyi P., Frazier J., Skinner M.A. Fowlpox virus host range restriction: gene expression, DNA replication, and morphogenesis in nonpermissive mammalian cells. Virology 1993, 197:439-444.
64. Staib C., Kisling S., Erfle V., Sutter G. Inactivation of the viral interleukin 1beta receptor improves CD8+ T-cell memory responses elicited upon immunization with modified vaccinia virus Ankara. J Gen. Virol. 2005, 86:1997-2006.
65. Sung S.S.J., Fu S.M., Rose C.E., Gaskin F., Ju S.T., Beaty S.R. A major lung CD103 (alpha(E))-beta(7) integrin-positive epithelial dendritic cell population expressing Langerin and tight junction proteins. J. Immunol. 2006, 176:2161-2172.
66. Tabata Y., Khurana Hershey G.K. IL-13 receptor isoforms: breaking through the complexity. Curr. Allergy Asthma Rep. 7 2007, 338-345.
67. Teigler J.E., Phogat S., Franchini G., Hirsch V.M., Michael N.L., Barouch D.H. The canarypox virus vector ALVAC induces distinct cytokine responses compared to the vaccinia virus-based vectors MVA and NYVAC in rhesus monkeys. J. Virol. 2014, 88:1809-1814.
68. Veazey R.S., de Maria M., Chalifoux L.V., Shvetz D.E., Pauley D.R., Knight H.L., Rosenzweig M., Johnson R.P., Desrosiers R.C., Lackner A.A. Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 1998, 280:427-431.
69. Waithman J., Allan R.S., Kosaka H., Azukizawa H., Shortman K., Lutz M.B., Heath W.R., Carbone F.R., Belz G.T. Skin-derived dendritic cells can mediate deletional tolerance of class I-Restricted self-reactive T cells. J. Immunol. 2007, 179:4535-4541.
70. Wijesundara D.K., Ranasinghe C., Jackson R.J., Lidbury B.A., Parish C.R., Quah J.C. Use of an in vivo FTA assay to assess the magnitude, functional avidity and epitope variant cross-reactivity of T cell responses following HIV-1 recombinant poxvirus vaccination. PloS One 2014, 9(8):e105366. 10.1371/journal.pone.0105366.