Engineering superior DNA vaccines: MHC class I single chain trimers bypass antigen processing and enhance the immune response to low affinity antigens

Vaccine

Volumn 28, Issue 8, 2010, Pages 1911-1918

  Li, Lijin ^a   Herndon, John M ^a   Truscott, Steven M ^a   Hansen, Ted H ^a,b   Fleming, Timothy P ^a,b   Goedegebuure, Peter ^a,b   Gillanders, William E ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Washington University in St Louis School of Medicine   (United States)

Author keywords

Antigen processing; DNA vaccine; MHC class I

Indexed keywords

BETA 2 MICROGLOBULIN; CANCER VACCINE; CD8 ANTIGEN; DNA VACCINE; EPITOPE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN BINDING; ANTIGEN PRESENTATION; ARTICLE; BINDING AFFINITY; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DISULFIDE BOND; DRUG EFFICACY; ENZYME LINKED IMMUNOSPOT ASSAY; EXPERIMENTAL NEOPLASM; GENE CONSTRUCT; GENE GUN; GENETIC ENGINEERING; HEAVY CHAIN; HELPER CELL; IMMUNE RESPONSE; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TREATMENT OUTCOME; TUMOR VOLUME; VACCINATION;

ANIMALS; ANTIGEN PRESENTATION; BETA 2-MICROGLOBULIN; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CHO CELLS; CRICETINAE; CRICETULUS; EPITOPES, T-LYMPHOCYTE; GENES, MHC CLASS I; HLA-A2 ANTIGEN; HUMANS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTAGENESIS, SITE-DIRECTED; NEOPLASM PROTEINS; OVALBUMIN; PROTEIN BINDING; PROTEIN ENGINEERING; UTEROGLOBIN; VACCINES, DNA;

EID: 76949090828     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2009.10.096     Document Type: Article

References (81)

1. Tang D.C., Devit M., and Johnston S.A. Genetic immunization is a simple method for eliciting an immune response. Nature 356 (1992) 152-154
2. Cox G.J., Zamb T.J., and Babiuk L.A. Bovine herpesvirus 1: immune responses in mice and cattle injected with plasmid DNA. J Virol 67 (1993) 5664-5667
3. Davis H.L., Michel M.L., and Whalen R.G. DNA-based immunization induces continuous secretion of hepatitis B surface antigen and high levels of circulating antibody. Hum Mol Genet 2 (1993) 1847-1851
4. Fynan E.F., Webster R.G., Fuller D.H., Haynes J.R., Santoro J.C., and Robinson H.L. DNA vaccines: protective immunizations by parenteral, mucosal, and gene gun inoculations. Proc Natl Acad Sci U S A 90 (1993) 11478-11482
5. Ulmer J.B., Donnelly J.J., Parker S.E., Rhodes G.H., Felgner P.L., Dwarki V.J., et al. Heterologous protection against influenza by injection of DNA encoding a viral protein. Science 259 (1993) 1745-1749
6. Wang B., Ugen K.E., Srikantan V., Agadjanyan M.G., Dang K., Refaeli Y., et al. Gene inoculation generates immune responses against human immunodeficiency virus type 1. Proc Natl Acad Sci USA 90 (1993) 4156-4160
7. Donnelly J.J., Ulmer J.B., Shiver J.W., and Liu M.A. DNA vaccines. Annu Rev Immunol 15 (1997) 617-648
8. Gurunathan S., Klinman D.M., and Seder R.A. DNA vaccines: immunology, application, and optimization. Annu Rev Immunol 18 (2000) 927-974
9. Kutzler M.A., and Weiner D.B. DNA vaccines: ready for prime time?. Nat Rev Genet 9 (2008) 776-788
10. Lee A.H., Suh Y.S., Sung J.H., Yang S.H., and Sung Y.C. Comparison of various expression plasmids for the induction of immune response by DNA immunization. Mol Cells 7 (1997) 495-501
11. Andre S., Seed B., Eberle J., Schraut W., Bultmann A., and Haas J. Increased immune response elicited by DNA vaccination with a synthetic gp120 sequence with optimized codon usage. J Virol 72 (1998) 1497-1503
12. Trumpfheller C., Finke J.S., Lopez C.B., Moran T.M., Moltedo B., Soares H., et al. Intensified and protective CD4+ T cell immunity in mice with anti-dendritic cell HIV gag fusion antibody vaccine. J Exp Med 203 (2006) 607-617
13. Nchinda G., Kuroiwa J., Oks M., Trumpfheller C., Park C.G., Huang Y., et al. The efficacy of DNA vaccination is enhanced in mice by targeting the encoded protein to dendritic cells. J Clin Invest 118 (2008) 1427-1436
14. Chan K., Lee D.J., Schubert A., Tang C.M., Crain B., Schoenberger S.P., et al. The roles of MHC class II, CD40, and B7 co-stimulation in CTL induction by plasmid DNA. J Immunol 166 (2001) 3061-3066
15. Boyer J.D., Robinson T.M., Kutzler M.A., Parkinson R., Calarota S.A., Sidhu M.K., et al. SIV DNA vaccine co-administered with IL-12 expression plasmid enhances CD8 SIV cellular immune responses in cynomolgus macaques. J Med Primatol 34 (2005) 262-270
16. Schadeck E.B., Sidhu M., Egan M.A., Chong S.Y., Piacente P., Masood A., et al. A dose sparing effect by plasmid encoded IL-12 adjuvant on a SIVgag-plasmid DNA vaccine in rhesus macaques. Vaccine 24 (2006) 4677-4687
17. Chong S.Y., Egan M.A., Kutzler M.A., Megati S., Masood A., Roopchard V., et al. Comparative ability of plasmid IL-12 and IL-15 to enhance cellular and humoral immune responses elicited by a SIVgag plasmid DNA vaccine and alter disease progression following SHIV(89.6P) challenge in rhesus macaques. Vaccine 25 (2007) 4967-4982
18. Hirao L.A., Wu L., Khan A.S., Hokey D.A., Yan J., Dai A., et al. Combined effects of IL-12 and electroporation enhances the potency of DNA vaccination in macaques. Vaccine 26 (2008) 3112-3120
19. Sumida S.M., Mckay P.F., Truitt D.M., Kishko M.G., arthur J.C., Seaman M.S., et al. Recruitment and expansion of dendritic cells in vivo potentiate the immunogenicity of plasmid DNA vaccines. J Clin Invest 114 (2004) 1334-1342
20. Calarota S., Bratt G., Nordlund S., Hinkula J., Leandersson A.C., Sandstrom E., et al. Cellular cytotoxic response induced by DNA vaccination in HIV-1-infected patients. Lancet 351 (1998) 1320-1325
21. MacGregor R.R., Boyer J.D., Ugen K.E., Lacy K.E., Gluckman S.J., Bagarazzi M.L., et al. First human trial of a DNA-based vaccine for treatment of human immunodeficiency virus type 1 infection: safety and host response. J Infect Dis 178 (1998) 92-100
22. Wang R., Doolan D.L., Le T.P., Hedstrom R.C., Coonan K.M., Charoenvit Y., et al. Induction of antigen-specific cytotoxic T lymphocytes in humans by a malaria DNA vaccine. Science 282 (1998) 476-480
23. + responses to viruses: cell biology, cellular immunology, and mathematical models. Immunity 21 (2004) 149-153
24. Chapatte L., Ayyoub M., Morel S., Peitrequin A.L., Levy N., Servis C., et al. Processing of tumor-associated antigen by the proteasomes of dendritic cells controls in vivo T cell responses. Cancer Res 66 (2006) 5461-5468
25. Del val M., Schlicht H.J., Ruppert T., Reddehase M.J., and Koszinowski U.H. Efficient processing of an antigenic sequence for presentation by MHC class I molecules depends on its neighboring residues in the protein. Cell 66 (1991) 1145-1153
26. Eisenlohr L.C., Yewdell J.W., and Bennink J.R. Flanking sequences influence the presentation of an endogenously synthesized peptide to cytotoxic T lymphocytes. J Exp Med 175 (1992) 481-487
27. Heemels M.T., and Ploegh H. Generation, translocation, and presentation of MHC class I-restricted peptides. Annu Rev Biochem 64 (1995) 463-491
28. Deng Y., Yewdell J.W., Eisenlohr L.C., and Bennink J.R. MHC affinity, peptide liberation, T cell repertoire, and immunodominance all contribute to the paucity of MHC class I-restricted peptides recognized by antiviral CTL. J Immunol 158 (1997) 1507-1515
29. Yu Y.Y., Netuschil N., Lybarger L., Connolly J.M., and 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 168 (2002) 3145-3149
30. + cytotoxic T lymphocytes from breast cancer patients. Breast Cancer Res Treat 88 (2004) 29-41
31. Crew M.D., Cannon M.J., Phanavanh B., and Garcia-Borges C.N. An HLA-E single chain trimer inhibits human NK cell reactivity towards porcine cells. Mol Immunol 42 (2005) 1205-1214
32. 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 12 (2005) 1180-1186
33. Primeau T., Myers N.B., Yu Y.Y., Lybarger L., Wang X., Truscott S.M., et al. Applications of major histocompatibility complex class I molecules expressed as single chains. Immunol Res 32 (2005) 109-121
34. Hung C.F., Calizo R., Tsai Y.C., He L., and Wu T.C. A DNA vaccine encoding a single chain trimer of HLA-A2 linked to human mesothelin peptide generates anti-tumor effects against human mesothelin-expressing tumors. Vaccine 25 (2007) 127-135
35. Lilienfeld B.G., Crew M.D., Forte P., Baumann B.C., and Seebach J.D. Transgenic expression of HLA-E single chain trimer protects porcine endothelial cells against human natural killer cell-mediated cytotoxicity. Xenotransplantation 14 (2007) 126-134
36. + T cell responses in HLA-A2.1/Kb transgenic mice. Immunology 121 (2007) 105-112
37. Choudhuri K., Wiseman D., Brown M.H., Gould K., and Van Der Merwe P.A. T cell receptor triggering is critically dependent on the dimensions of its peptide-MHC ligand. Nature 436 (2005) 578-582
38. Hudrisier D., Riond J., Garidou L., Duthoit C., and Joly E. T cell activation correlates with an increased proportion of antigen among the materials acquired from target cells. Eur J Immunol 35 (2005) 2284-2294
39. 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 436 (2005) 709-713
40. Howarth M., Williams A., Tolstrup A.B., and Elliott T. Tapasin enhances MHC class I peptide presentation according to peptide half-life. Proc Natl Acad Sci U S A 101 (2004) 11737-11742
41. Watson M.A., and Fleming T.P. Mammaglobin, a mammary-specific member of the uteroglobin gene family, is overexpressed in human breast cancer. Cancer Res 56 (1996) 860-865
42. 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 278 (2003) 27105-27111
43. Mitaksov V., Truscott S.M., Lybarger L., Connolly J.M., Hansen T.H., and Fremont D.H. Structural engineering of pMHC reagents for T cell vaccines and diagnostics. Chem Biol 14 (2007) 909-922
44. 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 178 (2007) 6280-6289
45. Porgador A., Yewdell J.W., Deng Y., Bennink J.R., and Germain R.N. Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity 6 (1997) 715-726
46. Bins A.D., Jorritsma A., Wolkers M.C., Hung C.F., Wu T.C., Schumacher T.N., et al. A rapid and potent DNA vaccination strategy defined by in vivo monitoring of antigen expression. Nat Med 11 (2005) 899-904
47. 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 283 (2008) 7480-7490
48. Dyall R., Bowne W.B., Weber L.W., Lemaoult J., Szabo P., Moroi Y., et al. Heteroclitic immunization induces tumor immunity. J Exp Med 188 (1998) 1553-1561
49. Gold J.S., Ferrone C.R., Guevara-Patino J.A., Hawkins W.G., Dyall R., Engelhorn M.E., et al. A single heteroclitic epitope determines cancer immunity after xenogeneic DNA immunization against a tumor differentiation antigen. J Immunol 170 (2003) 5188-5194
50. Yu Z., Theoret M.R., Touloukian C.E., Surman D.R., Garman S.C., Feigenbaum L., et al. Poor immunogenicity of a self/tumor antigen derives from peptide-MHC-I instability and is independent of tolerance. J Clin Invest 114 (2004) 551-559
51. Houghton A.N., and Guevara-patino J.A. Immune recognition of self in immunity against cancer. J Clin Invest 114 (2004) 468-471
52. Wooldridge L., Van den berg H.A., Glick M., Gostick E., Laugel B., Hutchinson S.L., et al. Interaction between the CD8 coreceptor and major histocompatibility complex class I stabilizes T cell receptorantigen complexes at the cell surface. J Biol Chem 280 (2005) 27491-27501
53. Wooldridge L., Lissina A., Vernazza J., Gostick E., Laugel B., Hutchinson S.L., et al. Enhanced immunogenicity of CTL antigens through mutation of the CD8 binding MHC class I invariant region. Eur J Immunol 37 (2007) 1323-1333
54. Holmberg K., Mariathasan S., Ohteki T., Ohashi P.S., and Gascoigne N.R. TCR binding kinetics measured with MHC class I tetramers reveal a positive selecting peptide with relatively high affinity for TCR. J Immunol 171 (2003) 2427-2434
55. Shedlock D.J., and Shen H. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300 (2003) 337-339
56. Sun J.C., and Bevan M.J. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 300 (2003) 339-342
57. 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 1 (1994) 751-761
58. + T cell immune responses and enhances vaccine potency. Mol Ther 15 (2007) 1211-1219
59. Watson M.A., Dintzis S., Darrow C.M., Voss L.E., Dipersio J., Jensen R., et al. Mammaglobin expression in primary, metastatic, and occult breast cancer. Cancer Res 59 (1999) 3028-3031
60. Fleming T.P., and Watson M.A. Mammaglobin, a breast-specific gene, and its utility as a marker for breast cancer. Ann N Y Acad Sci 923 (2000) 78-89
61. + T cell epitopes derived from mammaglobin-A, a tumor-associated antigen of human breast cancer. Int J Cancer 102 (2002) 499-506
62. + cytotoxic T lymphocytes against breast cancer cells by stimulation with mammaglobin-A-pulsed dendritic cells. Breast Cancer Res Treat 79 (2003) 133-136
63. Narayanan K., Jaramillo A., Benshoff N.D., Campbell L.G., Fleming T.P., Dietz J.R., et al. Response of established human breast tumors to vaccination with mammaglobin-A cDNA. J Natl Cancer Inst 96 (2004) 1388-1396
64. + T cells in breast cancer immunity following mammaglobin-A DNA vaccination using HLA-class-I tetramers. Breast Cancer Res Treat 110 (2008) 453-463
65. Luescher I.F., Vivier E., Layer A., Mahiou J., Godeau F., Malissen B., et al. CD8 modulation of T cell antigen receptor-ligand interactions on living cytotoxic T lymphocytes. Nature 373 (1995) 353-356
66. Gao G.F., Tormo J., Gerth U.C., Wyer J.R., Mcmichael A.J., Stuart D.I., et al. Crystal structure of the complex between human CD8alpha(alpha) and HLA-A2. Nature 387 (1997) 630-634
67. Arcaro A., Gregoire C., Bakker T.R., Baldi L., Jordan M., Goffin L., et al. CD8beta endows CD8 with efficient coreceptor function by coupling T cell receptor/CD3 to raft-associated CD8/p56(lck) complexes. J Exp Med 194 (2001) 1485-1495
68. Alexander M.A., Damico C.A., Wieties K.M., Hansen T.H., and Connolly J.M. Correlation between CD8 dependency and determinant density using peptide-induced Ld-restricted cytotoxic T lymphocytes. J Exp Med 173 (1991) 849-858
69. Mitchison N.A., and O'malley C. Three-cell-type clusters of T cells with antigen-presenting cells best explain the epitope linkage and noncognate requirements of the in vivo cytolytic response. Eur J Immunol 17 (1987) 1579-1583
70. + T cell help. J Exp Med 186 (1997) 65-70
71. + T helper-antigen-presenting cells. J Immunol 174 (2005) 7497-7505
72. Bevan M.J. Helping the CD8(+) T cell response. Nat Rev Immunol 4 (2004) 595-602
73. + T cell longevity and avoidance of TRAIL-mediated apoptosis. Proc Natl Acad Sci U S A 105 (2008) 5201-5206
74. Watson M.A., and Fleming T.P. Isolation of differentially expressed sequence tags from human breast cancer. Cancer Res 54 (1994) 4598-4602
75. Watson M.A., Darrow C., Zimonjic D.B., Popescu N.C., and Fleming T.P. Structure and transcriptional regulation of the human mammaglobin gene, a breast cancer-associated member of the uteroglobin gene family localized to chromosome 11q13. Oncogene 16 (1998) 817-824
76. Tanaka Y., Amos K.D., Fleming T.P., Eberlein T.J., and Goedegebuure P.S. Mammaglobin-A is a tumor-associated antigen in human breast carcinoma. Surgery 133 (2003) 74-80
77. Goedegebuure P.S., Watson M.A., Viehl C.T., and Fleming T.P. Mammaglobin-based strategies for treatment of breast cancer. Curr Cancer Drug Targets 4 (2004) 531-542
78. Viehl C.T., Tanaka Y., Chen T., Frey D.M., Tran A., Fleming T.P., et al. Tat mammaglobin fusion protein transduced dendritic cells stimulate mammaglobin-specific CD4 and CD8 T cells. Breast Cancer Res Treat 91 (2005) 271-278
79. Viehl C.T., Frey D.M., Phommaly C., Chen T., Fleming T.P., Gillanders W.E., et al. Generation of mammaglobin-A-specific CD4 T cells and identification of candidate CD4 epitopes for breast cancer vaccine strategies. Breast Cancer Res Treat (2007)
80. Bourgeois C., Veiga-Fernandes H., Joret A.M., Rocha B., and Tanchot C. CD8 lethargy in the absence of CD4 help. Eur J Immunol 32 (2002) 2199-2207
81. + T lymphocytes. Nature 421 (2003) 852-856