Transduction of human T cells with a novel T-cell receptor confers anti-HCV reactivity

PLoS Pathogens

Volumn 6, Issue 7, 2010, Pages 1-13

  Zhang, Yi ^a   Liu, Yeuying ^a   Moxley, Kelly M ^a   Golden Mason, Lucy ^b   Hughes Jr , Michael G ^a   Liu, Tongxin ^a   Heemskerk, Mirjam H M ^c   Rosen, Hugo R ^b   Nishimura, Michael I ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; HLA A2 ANTIGEN; INTERLEUKIN 2; NONSTRUCTURAL PROTEIN 3; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; LYMPHOCYTE ANTIGEN RECEPTOR; NS3 PROTEIN, HEPATITIS C VIRUS; TUMOR ANTIGEN; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CANCER CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL CLONE; CELL FUNCTION; CELL ISOLATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; LIVER CELL CARCINOMA; MOUSE; NONHUMAN; PERIPHERAL LYMPHOCYTE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; VIRUS IDENTIFICATION; VIRUS REACTIVATION; ANTIGEN PRESENTATION; CELL CULTURE; GENETIC TRANSDUCTION; GENETICS; HEPATITIS; IMMUNOLOGY; IMMUNOTHERAPY; METHODOLOGY; NEOPLASM; TUMOR CELL LINE;

HEPATITIS C VIRUS;

ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CELLS, CULTURED; HEPACIVIRUS; HEPATITIS; HUMANS; IMMUNOTHERAPY; JURKAT CELLS; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; TRANSDUCTION, GENETIC; VIRAL NONSTRUCTURAL PROTEINS;

EID: 77957671100     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001018     Document Type: Article

References (61)

1. National Centers for Disease Control and Prevention. Hepatitis C Fact Sheet, http://www.cdc.gov/ncidod/diseases/hepatitis/c/fact/html.
2. World Health Organization (2000) Hepatitis C - Global Surveillance Update. Weekly Epidemiological Record 75: 17-28.
3. Centers for Disease Control and Prevention Web site on Hepatitis C: http://www.cdc.gov/.
4. Scientific Registry of Transplant Recipients (SRTR): OPTN/SRTR Annual report: transplant data 1993-2002. (Chapter VII). Available: www.ustransplantorg. 2003.
5. Adam R, McMaster P, O'Grady JG, Castaing D, Klempnauer JL, et al. (2003) European Liver Transplant Association. Liver Transpl. 1231 p.
6. McHutchison JG, Fried MW (2003) Current therapy for hepatitis C: pegylated interferon and ribavirin. Clin Liver Dis 7: 149-161.
7. Rehermann B (2000) Interaction between the hepatitis C virus and the immune system. Semin Liver Dis 20: 127-141.
8. Missale GR, Bertoni V, Lamonaca A, Valli M, Massari C, et al. (1996) Different clinical behaviors of acute hepatitis C virus infection are associated with different vigor of the anti-viral cell-mediated immune response. J Clin Invest 98: 706-714.
9. Thimme R, Oldach D, Chang KM, Steiger C, Ray SC, et al. (2001) Chisari. Determinants of viral clearance and persistence during acute hepatitis C virus infection. J Exp Med 194: 1395-1406.
10. Seifert U, Liermann H, Racanelli V, Halenius A, Wiese M, et al. (2004) Hepatitis C virus mutation affects proteasomal epitope processing. J Clin Invest 114: 250-259.
11. Pavio N, Lai MM (2003) The hepatitis C virus persistence: how to evade the immune system? J Biosci 28: 287-304.
12. Tester I, Smyk-Pearson S, Wang P, Wertheimer A, Yao E, et al. (2005) Immune evasion versus recovery following acute hepatitis c virus infection from a shared source. J Exp Med 201: 1725-1731.
13. Cole DJ, Weil DP, Shilyansky J, Custer M, Kawakami Y, et al. (1995) Characterization of the functional specificity of a cloned T-cell receptor heterodimer recognizing the MART-1 melanoma antigen. Cancer Res 55:748-52.
14. Clay TM, Custer MC, Sachs J, Hwu P, Rosenberg SA (1999) and Nishimura M. I. Efficient transfer of a tumor antigen-reactive TCR to human peripheral blood lymphocytes confers anti-tumor reactivity. J Immunol 163: 507-513.
15. Orentas RJ, Roskopf SJ, Nolan GP, Nishimura MI (2001) Retroviral transduction of a T cell receptor specific for an Epstein- Barr virus-encoded peptide. Clin Immunol 98: 220-228.
16. Heemskerk HMH, Hoogeboom M, de Paus RA, Willemze R, Falkenburg JF (2002) Redirection towards anti-leukemic reactivity of CMV specific peripheral T lymphocytes using T cell receptor gene transfer. Blood 100: 218A-219A.
17. Rubinstein MP, Kadima AN, Salem ML, Nguyen CL, Gillanders W, et al. (2003) Transfer of TCR Genes into Mature T Cells Is Accompanied by the Maintenance of Parental T Cell Avidity. J Immunol 170: 1209-1217.
18. Stanislawski T, Voss RH, Lotz C, Sadovnikova E, Willemsen RA, et al. (2001) Circumventing tolerance to a human MDM2-derived tumor antigen by TCR gene transfer. Nat Immunol 2: 962-970.
19. Ueno TH, Tomiyama M, Fujiwara S, Takiguchi M (2004) Functionally impaired HIV-specific CD8 T cells show high affinity TCR-ligand interactions. J Immunol 173: 5451-5457.
20. Scholten KB, Schreurs MW, Ruizendaal JJ, Kueter EW, Kramer D, et al. (2005) Preservation and redirection of HPV16E7-specific T cell receptors for immunotherapy of cervical cancer. Clin Immunol 114: 119-129.
21. van der Veken LT, Hoogeboom M, de Paus RA, Willemze R, Falkenburg JH, et al. (2005) HLA class II restricted T-cell receptor gene transfer generates CD4(+) T cells with helper activity as well cytotoxic capacity. Gene Ther 12:1686-95.
22. Tsuji T, Yasukawa M, Matsuzaki J, Ohkuri T, Chamoto K, et al. (2005) Generation of tumor-specific, HLA class I-restricted human Th1 and Tc1 cells by cell engineering with tumor peptide-specific T-cell receptor genes. Blood 106:470-476.
23. Engels B, Noessner E, Frankenberger B, Blankenstein T, Schendel DJ, et al. (2005) Redirecting human T lymphocytes toward renal cell carcinoma specificity by retroviral transfer of T cells receptor genes. Hum Gene Ther 16: 799-810.
24. Callender GG, Rosen HR, Roszkowski JJ, Lyons GE, Li M, et al. (2006) Identification of a CD8-Independent Hepatitis C Virus-Specific T Cell Receptor That Does Not Require CD8 For Target Cell Recognition. Hepatology 43:973-81.
25. Zhao Y, Bennett AD, Zheng Z, Wang QJ, Robbins PF, et al. (2007) Highaffinity TCRs generated by phage display provide CD4+ T cells with the ability to recognize and kill tumor cell lines. J Immunol 179: 5845-54.
26. Xue SA, Gao L, Hart D, Gillmore R, Qasim W, et al. (2005) Elimination of human leukemia cells in NOD/SCID mice by WT1-TCR gene-transduced human T cells. Blood 106: 3062-7.
27. Varela-Rohena A, Molloy PE, Dunn SM, Li Y, Suhoski MM, et al. (2008) Control of HIV-1 immune escape by CD8 T cells expressing enhanced T-cell receptor. Nat Med 14: 1390-5.
28. Dossett ML, Teague RM, Schmitt TM, Tan X, Cooper LJ, et al. (2009) Adoptive Immunotherapy of Disseminated Leukemia With TCR-transduced, CD8(+) T Cells Expressing a Known Endogenous TCR. Mol Ther 17: 742-9.
29. Duval L, Schmidt H, Kaltoft K, Fode K, Jensen JJ, Sorensen SM, et al. (2006) Adoptive transfer of allogeneic cytotoxic T lymphocytes equipped with a HLAA2 restricted MART-1 T-cell receptor: a phase I trial in metastatic melanoma. Clin Cancer Res 12: 1229-36.
30. Morgan RA, Dudley ME, Wunderlich JR, Hughes MS, Yang JC, et al. (2006) Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314: 126-9.
31. Johnson LA, Morgan RA, Dudley ME, Cassard L, Yang JC, et al. (2009) Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 2009 114: 535-46.
32. Rosen HR, Hinrichs DJ, Leistikow RL, Callender G, Wertheimer AM, et al. (2004) Cutting Edge: Identification of Hepatitis C Virus-Specific CD8+ T Cells Restricted by Donor HLA Alleles following Liver Transplantation. J Immunol 173: 5355-5359.
33. Rehermann B (2009) Hepatitis C virus versus innate and adaptive immune responses: a tale of coevolution and coexistence. J Clin Invest 119: 1745-54.
34. Wedemeyer H, Mizukoshi E, Davis AR, Bennink JR, Rehermann B (2001) Cross-reactivity between hepatitis C virus and Influenza A virus determinantspecific cytotoxic T cells. J Virol 75: 11392-400.
35. Chang KM, Rehermann B, McHutchison JG, Pasquinelli C, Southwood S, Sette A, Chisari FV (1997) Immunological significance of cytotoxic T lymphocyte epitope variants in patients chronically infected by the hepatitis C virus. J Clin Invest 100: 2376-85.
36. Shilyansky J, Nishimura MI, Yannelli JR, Kawakami Y, Jacknin LS, et al. (1994) T-cell receptor usage by melanoma-specific clonal and highly oligoclonal tumorinfiltrating lymphocyte lines. Proc Natl Acad Sci 91: 2829-2833.
37. Nishimura MI, YKawakami P, Charmley B, O'Neil J, Shilyansky JR, et al. (1994) T-cell receptor repertoire in tumor-infiltrating lymphocytes. Analysis of melanoma-specific long-term lines. J Immunother 16: 85-94.
38. Lyons GE, Roszkowski JJ, Mann S, Yee C, Kast WM, et al. (2006) TCR Tetramer Binding and the Lack There of Does Not Necessitate Antigen Reactivity in TCR Transduced T Cells. Cancer. Immunol Immunother 55:1142-50.
39. Lyons GE, Moore T, Brasic N, Li M, Roszkowski JJ, et al. (2006) Influence of Human CD8 on Antigen Recognition by TCR Transduced Cells. Cancer Res 66: 11455-61.
40. Morgan RA, Dudley ME, Yu YYL, Zheng Z, et al. (2003) High Efficiency TCR Gene Transfer into Primary Human Lymphocytes Affords Avid Recognition of Melanoma Tumor Antigen Glycoprotein 100 and Does Not Alter the Recognition of Autologous Melanoma Antigens. J Immunol 171: 3287-95.
41. Roszkowski JJ, Yu DC, Rubinstein MP, McKee MD, Cole DJ, et al. (2003) CD8-independent tumor cell recognition is a property of the T cell receptor and not the T cell. J Immunol 170: 2582-9.
42. Roszkowski JJ, Lyons GE, Kast WM, Yee C, Van Besien K, et al. (2005) Simultaneous Generation of CD8+ and CD4+ Melanoma Reactive T Cells By Retroviral Mediated TCR Gene Transfer. Cancer Res 65: 1570-1576.
43. Heller KN, Gurer C, Münz C (2006) Virus-specific CD4+ T cells: ready fordirect attack. J Exp Med 203: 805-8.
44. Alexander-Miller MA, Leggatt GR, Berzofsky JA (1996) Selective expansion of high- or low-avidity cytotoxic T lymphocytes and efficacy for adoptive immunotherapy. Proc Natl Acad Sci U S A 93: 4102-7.
45. Zeh HJ, 3rd, Perry-Lalley D, Dudley ME, Rosenberg SA, Yang JC (1999) High avidity CTLs for two self-antigens demonstrate superior in vitro and in vivo antitumor efficacy. J Immunol 162: 989-94.
46. Hofmann M, Radsak M, Rechtsteiner G, Wiemann K, Günder M, et al. (2004) T cell avidity determines the level of CTL activation. Eur J Immunol 34: 1798-806.
47. Slifka MK, Whitton JL (2001) Functional avidity maturation of CD8(+) T cells without selection of higher affinity TCR. Nat Immunol 2: 711-7.
48. Holler PD, Lim AR, Cho BK, Rund LA, Kranz DM (2001) CD8(2) T cell transfectants that express a high affinity T cell receptor exhibit enhanced peptide-dependent activation. J Exp Med 194: 1043-52.
49. Holler PD, Kranz DM (2003) Quantitative analysis of the contribution of TCR/ pepMHC affinity and CD8 to T cell activation. Immunity 18: 255-64.
50. Moore TV, Lyons GE, Brasic N, Roszkowski JJ, Voelkl S, et al. (2009) Relationship between CD8-dependent antigen recognition, T cell functional avidity, and tumor cell recognition. Cancer Immunol Immunother 58: 719-28.
51. Swain SL, Agrewala JN, Brown DM, Jelley-Gibbs DM, Golech S, et al. (2006) CD4+ T-cell memory: generation and multi-faceted roles for CD4+ T cell in protective immunity to influenza. Immunol Rev 211: 8-22.
52. Aslan N, Yurdaydin C, Wiegand J, Greten T, Ciner A, et al. (2006) Cytotoxic CD4 T cells in viral hepatitis. J Viral Hepat 13: 505-14.
53. Zhang Y, Chaux P, Stroobant V, Eggermont AM, Corthals J, et al. (2003) A MAGE-3 peptide presented by HLA-DR1 to CD4+ T cells that were isolated from a melanoma patient vaccinated with a MAGE-3 protein. J Immunol 171: 219-25.
54. Heemskerk MH, Hoogeboom M, Hagedoom R, Kester MG, Willemze R, et al. (2004) Reprogramming of virus-specific T cells into leukemia-reactive T cells using T cell receptor gene transfer. J Exp Med 199: 885-894.
55. Langerman A, Callendar GG, Nishimura MI (2004) Engineering Bifunctional T Cells as a Treatment for Immunotherapy Resistant Tumors. J Trans Med 2: 42.
56. Weinhold M, Sommermeyer D, Uckert W, Blankenstein T (2007) Dual T cell receptor expressing CD8+ T cells with tumor- and self-specificity can inhibit tumor growth without causing severe autoimmunity. J Immunol 179:5534-5542.
57. Sobesky R, Feray C, Rimlinger F, Derian N, Dos Santos A, et al. (2007) Distinct hepatitis C virus core and F protein quasispecies in tumoral and nontumoral hepatocytes isolated via microdissection. Hepatology 46: 1704-1712.
58. Mommaas B, van Halteren AGS, Pool J, van der Veken L,Wieles B, et al. (2005) Adult and cord blood T cells can acquire HA-1 specificity through HA-1 T-cell receptor gene transfer. Haematologica 90: 1415-1421.
59. Morita S, Kojima T, Kitamura T (2000) Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Therapy 7: 1063-1066.
60. Fujio K, Misaki Y, Setoguchi K, Morita S, Kawahata K, et al. (2000) Functional reconstitution of Class-II MHC-restricted T cell immunity mediated by retroviral transfer of the abTCR complex. J Immunol 165: 528-533.
61. Walter EA, Greenberg PD, Gilbert MJ, Finch RJ, Watanabe KS, et al. (1995) Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. N Engl JMed 333: 1038-1044.