Single chain MHC I trimer-based DNA vaccines for protection against Listeria monocytogenes infection

Vaccine

Volumn 30, Issue 12, 2012, Pages 2178-2186

  Kim, Sojung ^a   Zuiani, Adam ^a   Carrero, Javier A ^a   Hansen, Ted H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CD4 + T cell help; DNA vaccine; Listeria monocytogenes infection; Memory CD8 + T cell; MHC I single chain trimers

Indexed keywords

BETA 2 MICROGLOBULIN; DNA VACCINE; EPITOPE; GAMMA INTERFERON; SINGLE CHAIN TRIMER MAJOR HISTOCOMPATIBILITY COMPLEX CLASS 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ARTICLE; BACTERIAL INFECTION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL SURFACE; CONTROLLED STUDY; DNA IMMUNIZATION; HUMAN; HUMAN CELL; LISTERIOSIS; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRUS INFECTION;

ANIMALS; ANTIGENS, BACTERIAL; ANTIGENS, CD; BACTERIAL LOAD; BETA 2-MICROGLOBULIN; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; ENZYME-LINKED IMMUNOSPOT ASSAY; EPITOPES, T-LYMPHOCYTE; FLOW CYTOMETRY; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNODOMINANT EPITOPES; INTERFERON-GAMMA; LEUKOCYTES, MONONUCLEAR; LISTERIA MONOCYTOGENES; LISTERIOSIS; LIVER; LYMPHOCYTE SUBSETS; MICE; MICE, INBRED BALB C; PLASMIDS; RECOMBINANT FUSION PROTEINS; SPLEEN; VACCINES, DNA;

EID: 84862790708     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2012.01.012     Document Type: Article

References (67)

1. Berzofsky J.A., Ahlers J.D., Belyakov I.M. Strategies for designing and optimizing new generation vaccines. Nat Rev Immunol 2001, 1(December (3)):209-219.
2. Kutzler M.A., Weiner D.B. DNA vaccines: ready for prime time?. Nat Rev Genet 2008, 9(October (10)):776-788.
3. Mottez E., Langlade-Demoyen P., Gournier H., Martinon F., Maryanski J., Kourilsky P., et al. Cells expressing a major histocompatibility complex class I molecule with a single covalently bound peptide are highly immunogenic. J Exp Med 1995, 181(February (2)):493-502.
4. Yu Y.Y., Netuschil N., Lybarger L., Connolly J.M., Hansen T.H. Cutting edge: single-chain trimers of MHC class I molecules form stable structures that potently stimulate antigen-specific T cells and B cells. J Immunol 2002, 168(April (7)):3145-3149.
5. Truscott S.M., Lybarger L., Martinko J.M., Mitaksov V.E., Kranz D.M., Connolly J.M., et al. Disulfide bond engineering to trap peptides in the MHC class I binding groove. J Immunol 2007, 178(May (10)):6280-6289.
6. Lybarger L., Yu Y.Y., Miley M.J., Fremont D.H., Myers N., Primeau T., et al. Enhanced immune presentation of a single-chain major histocompatibility complex class I molecule engineered to optimize linkage of a C-terminally extended peptide. J Biol Chem 2003, 278(July (29)):27105-27111.
7. Truscott S.M., Wang X., Lybarger L., Biddison W.E., McBerry C., Martinko J.M., et al. Human major histocompatibility complex (MHC) class I molecules with disulfide traps secure disease-related antigenic peptides and exclude competitor peptides. J Biol Chem 2008, 283(March (12)):7480-7490.
8. Mitaksov V., Truscott S.M., Lybarger L., Connolly J.M., Hansen T.H., Fremont D.H. Structural engineering of pMHC reagents for T cell vaccines and diagnostics. Chem Biol 2007, 14(August (8)):909-922.
9. Hansen T.H., Lybarger L. Exciting applications of single chain trimers of MHC-I molecules. Cancer Immunol Immunother 2006, 55(February (2)):235-236.
10. Kim S., Poursine-Laurent J., Truscott S.M., Lybarger L., Song Y.J., Yang L., et al. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 2005, 436(August (7051)):709-713.
11. Cheung Y.K., Cheng S.C., Sin F.W., Chan K.T., Xie Y. Induction of T-cell response by a DNA vaccine encoding a novel HLA-A*0201 severe acute respiratory syndrome coronavirus epitope. Vaccine 2007, 25(August (32)):6070-6077.
12. Zhang Y., Li S., Shan M., Pan X., Zhuang K., He L., et al. Hepatitis B virus core antigen epitopes presented by HLA-A2 single-chain trimers induce functional epitope-specific CD8+ T-cell responses in HLA-A2.1/Kb transgenic mice. Immunology 2007, 121(May (1)):105-112.
13. Huang C.H., Peng S., He L., Tsai Y.C., Boyd D.A., Hansen T.H., et al. Cancer immunotherapy using a DNA vaccine encoding a single-chain trimer of MHC class I linked to an HPV-16 E6 immunodominant CTL epitope. Gene Ther 2005, 12(August (15)):1180-1186.
14. Palmowski M.J., Parker M., Choudhuri K., Chiu C., Callan M.F., van der Merwe P.A., et al. A single-chain H-2Db molecule presenting an influenza virus nucleoprotein epitope shows enhanced ability at stimulating CD8+ T cell responses in vivo. J Immunol 2009, 182(April (8)):4565-4571.
15. Kim S., Li L., McMurtrey C.P., Hildebrand W.H., Weidanz J.A., Gillanders W.E., et al. Single-chain HLA-A2 MHC trimers that incorporate an immundominant peptide elicit protective T cell immunity against lethal West Nile virus infection. J Immunol 2010, 184(April (8)):4423-4430.
16. Li L., Herndon J.M., Truscott S.M., Hansen T.H., Fleming T.P., Goedegebuure P., et al. Engineering superior DNA vaccines: MHC class I single chain trimers bypass antigen processing and enhance the immune response to low affinity antigens. Vaccine 2010, 28(February (8)):1911-1918.
17. Hung C.F., Tsai Y.C., He L., Wu T.C. DNA vaccines encoding Ii-PADRE generates potent PADRE-specific CD4+ T-cell immune responses and enhances vaccine potency. Mol Ther 2007, 15(June (6)):1211-1219.
18. Pamer E.G. Immune responses to Listeria monocytogenes. Nat Rev Immunol 2004, 4(October (10)):812-823.
19. Zenewicz L.A., Shen H. Innate and adaptive immune responses to Listeria monocytogenes: a short overview. Microbes Infect 2007, 9(August (10)):1208-1215.
20. Finelli A., Kerksiek K.M., Allen S.E., Marshall N., Mercado R., Pilip I., et al. MHC class I restricted T cell responses to Listeria monocytogenes, an intracellular bacterial pathogen. Immunol Res 1999, 19(2-3):211-223.
21. Pamer E.G. Direct sequence identification and kinetic analysis of an MHC class I-restricted Listeria monocytogenes CTL epitope. J Immunol 1994, 152(January (2)):686-694.
22. Sijts A.J., Neisig A., Neefjes J., Pamer E.G. Two Listeria monocytogenes CTL epitopes are processed from the same antigen with different efficiencies. J Immunol 1996, 156(January (2)):683-692.
23. Pamer E.G., Harty J.T., Bevan M.J. Precise prediction of a dominant class I MHC-restricted epitope of Listeria monocytogenes. Nature 1991, 353(October (6347)):852-855.
24. Ramsburg E.A., Publicover J.M., Coppock D., Rose J.K. Requirement for CD4 T cell help in maintenance of memory CD8 T cell responses is epitope dependent. J Immunol 2007, 178(May (10)):6350-6358.
25. Gao F.G., Khammanivong V., Liu W.J., Leggatt G.R., Frazer I.H., Fernando G.J. Antigen-specific CD4+ T-cell help is required to activate a memory CD8+ T cell to a fully functional tumor killer cell. Cancer Res 2002, 62(November (22)):6438-6441.
26. Sun J.C., Williams M.A., Bevan M.J. CD4+ T cells are required for the maintenance, not programming, of memory CD8+ T cells after acute infection. Nat Immunol 2004, 5(September (9)):927-933.
27. Hamilton S.E., Jameson S.C. The nature of the lymphopenic environment dictates protective function of homeostatic-memory CD8+ T cells. Proc Natl Acad Sci USA 2008, 105(November (47)):18484-18489.
28. de Goer de Herve M.G., Cariou A., Simonetta F., Taoufik Y. Heterospecific CD4 help to rescue CD8 T cell killers. J Immunol 2008, 181(November (9)):5974-5980.
29. Hao S., Yuan J., Xiang J. Nonspecific CD4(+) T cells with uptake of antigen-specific dendritic cell-released exosomes stimulate antigen-specific CD8(+) CTL responses and long-term T cell memory. J Leukoc Biol 2007, 82(October (4)):829-838.
30. Tsukamoto T., Takeda A., Yamamoto T., Yamamoto H., Kawada M., Matano T. Impact of cytotoxic-T-lymphocyte memory induction without virus-specific CD4+ T-Cell help on control of a simian immunodeficiency virus challenge in rhesus macaques. J Virol 2009, 83(September (18)):9339-9346.
31. Carrero J.A., Calderon B., Unanue E.R. Lymphocytes are detrimental during the early innate immune response against Listeria monocytogenes. J Exp Med 2006, 203(April (4)):933-940.
32. Carrero J.A., Calderon B., Unanue E.R. Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. J Exp Med 2004, 200(August (4)):535-540.
33. Lauvau G., Vijh S., Kong P., Horng T., Kerksiek K., Serbina N., et al. Priming of memory but not effector CD8 T cells by a killed bacterial vaccine. Science 2001, 294(November (5547)):1735-1739.
34. Cornell K.A., Bouwer H.G., Hinrichs D.J., Barry R.A. Genetic immunization of mice against Listeria monocytogenes using plasmid DNA encoding listeriolysin O. J Immunol 1999, 163(July (1)):322-329.
35. Fensterle J., Grode L., Hess J., Kaufmann S.H. Effective DNA vaccination against listeriosis by prime/boost inoculation with the gene gun. J Immunol 1999, 163(October (8)):4510-4518.
36. Yoshida A., Nagata T., Uchijima M., Koide Y. Protective CTL response is induced in the absence of CD4+ T cells and IFN-γ by gene gun DNA vaccination with a minigene encoding a CTL epitope of Listeria monocytogenes. Vaccine 2001, 19(July (30)):4297-4306.
37. Hovav A.H., Panas M.W., Rahman S., Sircar P., Gillard G., Cayabyab M.J., et al. Duration of antigen expression in vivo following DNA immunization modifies the magnitude, contraction, and secondary responses of CD8+ T lymphocytes. J Immunol 2007, 179(November (10)):6725-6733.
38. Sun J.C., Bevan M.J. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 2003, 300(April (5617)):339-342.
39. Shedlock D.J., Shen H. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 2003, 300(April (5617)):337-339.
40. van B.J., Schoenberger S.P., Verreck F., Amons R., Offringa R., Koning F. Efficient loading of HLA-DR with a T helper epitope by genetic exchange of CLIP. Proc Natl Acad Sci USA 1997, 94(July (14)):7499-7502.
41. Nagata T., Aoshi T., Suzuki M., Uchijima M., Kim Y.H., Yang Z., et al. Induction of protective immunity to Listeria monocytogenes by immunization with plasmid DNA expressing a helper T-cell epitope that replaces the class II-associated invariant chain peptide of the invariant chain. Infect Immun 2002, 70(May (5)):2676-2680.
42. Kim D., Monie A., He L., Tsai Y.C., Hung C.F., Wu T.C. Role of IL-2 secreted by PADRE-specific CD4+ T cells in enhancing E7-specific CD8+ T-cell immune responses. Gene Ther 2008, 15(May (9)):677-687.
43. Alexander J., Sidney J., Southwood S., Ruppert J., Oseroff C., Maewal A., et al. Development of high potency universal DR-restricted helper epitopes by modification of high affinity DR-blocking peptides. Immunity 1994, 1(December (9)):751-761.
44. Geginat G., Schenk S., Skoberne M., Goebel W., Hof H. A novel approach of direct ex vivo epitope mapping identifies dominant and subdominant CD4 and CD8 T cell epitopes from Listeria monocytogenes. J Immunol 2001, 166(February (3)):1877-1884.
45. Hansen T., Yu Y.Y., Fremont D.H. Preparation of stable single-chain trimers engineered with peptide, beta2 microglobulin, and MHC heavy chain. Curr Protoc ImmunolI November 2009, [Chapter 17:Unit17].
46. Hansen T.H., Connolly J.M., Gould K.G., Fremont D.H. Basic and translational applications of engineered MHC class I proteins. Trends Immunol 2010, 31(October (10)):363-369.
47. Rogers H.W., Unanue E.R. Neutrophils are involved in acute, nonspecific resistance to Listeria monocytogenes in mice. Infect Immun 1993, 61(December (12)):5090-5096.
48. Czuprynski C.J., Brown J.F., Maroushek N., Wagner R.D., Steinberg H. Administration of anti-granulocyte mAb RB6-8C5 impairs the resistance of mice to Listeria monocytogenes infection. J Immunol 1994, 152(February (4)):1836-1846.
49. Sallusto F., Lanzavecchia A., Araki K., Ahmed R. From vaccines to memory and back. Immunity 2010, 33(October (4)):451-463.
50. Bourgeois C., Tanchot C. Mini-review CD4 T cells are required for CD8 T cell memory generation. Eur J Immunol 2003, 33(December (12)):3225-3231.
51. Bourgeois C., Rocha B., Tanchot C. A role for CD40 expression on CD8+ T cells in the generation of CD8+ T cell memory. Science 2002, 297(September (5589)):2060-2063.
52. Bennett S.R., Carbone F.R., Karamalis F., Flavell R.A., Miller J.F., Heath W.R. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 1998, 393(June (6684)):478-480.
53. Ridge J.P., Di R.F., Matzinger P. A conditioned dendritic cell can be a temporal bridge between a CD4+ T-helper and a T-killer cell. Nature 1998, 393(June (6684)):474-478.
54. Schoenberger S.P., Toes R.E., van der Voort E.I., Offringa R., Melief C.J. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 1998, 393(June (6684)):480-483.
55. Sun J.C., Bevan M.J. Cutting edge: long-lived CD8 memory and protective immunity in the absence of CD40 expression on CD8 T cells. J Immunol 2004, 172(March (6)):3385-3389.
56. Lee B.O., Hartson L., Randall T.D. CD40-deficient, influenza-specific CD8 memory T cells develop and function normally in a CD40-sufficient environment. J Exp Med 2003, 198(December (11)):1759-1764.
57. Krieg A.M. CpG motifs in bacterial DNA and their immune effects. Annu Rev Immunol 2002, 20:709-760.
58. Bode C., Zhao G., Steinhagen F., Kinjo T., Klinman D.M. CpG DNA as a vaccine adjuvant. Expert Rev Vaccines 2011, 10(April (4)):499-511.
59. Babiuk S., Mookherjee N., Pontarollo R., Griebel P., van Drunen Littel-van den Hurk S., Hecker R., et al. TLR9-/- and TLR9+/+ mice display similar immune responses to a DNA vaccine. Immunology 2004, 113(September (1)):114-120.
60. Rottembourg D., Filippi C.M., Bresson D., Ehrhardt K., Estes E.A., Oldham J.E., et al. Essential role for TLR9 in prime but not prime-boost plasmid DNA vaccination to activate dendritic cells and protect from lethal viral infection. J Immunol 2010, 184(June (12)):7100-7107.
61. Feltquate D.M., Heaney S., Webster R.G., Robinson H.L. Different T helper cell types and antibody isotypes generated by saline and gene gun DNA immunization. J Immunol 1997, 158(March (5)):2278-2284.
62. Strugnell R.A., Drew D., Mercieca J., DiNatale S., Firez N., Dunstan S.J., et al. DNA vaccines for bacterial infections. Immunol Cell Biol 1997, 75(August (4)):364-369.
63. Belz G.T., Shortman K., Bevan M.J., Heath W.R. CD8alpha+ dendritic cells selectively present MHC class I-restricted noncytolytic viral and intracellular bacterial antigens in vivo. J Immunol 2005, 175(July (1)):196-200.
64. 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(November (5904)):1097-1100.
65. 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(September (5641)):1925-1928.
66. Wakim L.M., Bevan M.J. Cross-dressed dendritic cells drive memory CD8+ T-cell activation after viral infection. Nature 2011, 471(March (7340)):629-632.
67. Lauterbach H., Gruber A., Ried C., Cheminay C., Brocker T. Insufficient APC capacities of dendritic cells in gene gun-mediated DNA vaccination. J Immunol 2006, 176(April (8)):4600-4607.