Phenotype, functions and fate of adoptively transferred tumor draining lymphocytes activated ex vivo in mice with an aggressive weakly immunogenic mammary carcinoma

BMC Immunology

Volumn 11, Issue , 2010, Pages

  Miller, Catriona H T ^a   Graham, Laura ^a   Bear, Harry D ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRYOSTATIN; CD69 ANTIGEN; CYCLOPHOSPHAMIDE; GAMMA INTERFERON; IONOMYCIN;

ADOPTIVE IMMUNOTHERAPY; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CARCINOMA; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FATE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DEPLETION; EX VIVO STUDY; IMMUNOGENICITY; LYMPH NODE; LYMPHOCYTE; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PHENOTYPE; SPLEEN; T LYMPHOCYTE; TUMOR REGRESSION; ANIMAL; BREAST TUMOR; CANCER TRANSPLANTATION; CARCINOMA; CELL MOTION; DRUG EFFECT; IMMUNOLOGY; IMMUNOPHENOTYPING; LYMPHOCYTE ACTIVATION; METABOLISM; PATHOLOGY; TUMOR ASSOCIATED LEUKOCYTE; TUMOR ESCAPE;

ANIMALS; BREAST NEOPLASMS; BRYOSTATINS; CARCINOMA; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CELL PROLIFERATION; IMMUNOPHENOTYPING; IMMUNOTHERAPY, ADOPTIVE; IONOMYCIN; LYMPH NODES; LYMPHOCYTE ACTIVATION; LYMPHOCYTES, TUMOR-INFILTRATING; MICE; NEOPLASM REGRESSION, SPONTANEOUS; NEOPLASM TRANSPLANTATION; TUMOR ESCAPE;

EID: 78049379784     PISSN: None     EISSN: 14712172     Source Type: Journal    
DOI: 10.1186/1471-2172-11-54     Document Type: Article

References (66)

1. Saleh F, Renno W, Klepacek I, Ibrahim G, Dashti H, Asfar S, Behbehani A, Al-Sayer H, Dashti A. Direct evidence on the immune-mediated spontaneous regression of human cancer: an incentive for pharmaceutical companies to develop a novel anti-cancer vaccine. Curr Pharm Des 2005, 11:3531-3543. 10.2174/138161205774414556, 16248806.
2. Saleh FH, Crotty KA, Hersey P, Menzies SW. Primary melanoma tumour regression associated with an immune response to the tumour-associated antigen melan-A/MART-1. Int J Cancer 2001, 94:551-557. 10.1002/ijc.1491, 11745443.
3. Boon T, Cerottini JC, Van den Eynde B, Van der Bruggen P, Van Pel A. Tumor antigens recognized by T lymphocytes. Annu Rev Immunol 1994, 12:337-365. 10.1146/annurev.iy.12.040194.002005, 8011285.
4. Chang AE, Li Q, Jiang G, Sayre DM, Braun TM, Redman BG. Phase II trial of autologous tumor vaccination, anti-CD3-activated vaccine-primed lymphocytes, and interleukin-2 in stage IV renal cell cancer. J Clin Oncol 2003, 21:884-890. 10.1200/JCO.2003.08.023, 12610189.
5. Cohen PA, Peng LM, Kjaergaard J, Plautz GE, Finke JH, Koski GK, Czerniecki BJ, Shu SY. T-cell adoptive therapy of tumors: Mechanisms of improved therapeutic performance. Crit Rev Immunol 2001, 21:215-248.
6. Crossland KD, Lee VK, Chen W, Riddell SR, Greenberg PD, Cheever MA. T cells from tumor-immune mice nonspecifically expanded in vitro with anti-CD3 plus IL-2 retain specific function in vitro and can eradicate disseminated leukemia in vivo. J Immunol 1991, 146:4414-4420.
7. Dudley ME, Rosenberg SA. Adoptive-cell-transfer therapy for the treatment of patients with cancer. Nat Rev Cancer 2003, 3:666-675. 10.1038/nrc1167, 2305722, 12951585.
8. Goedegebuure PS, Douville LM, Li H, Richmond GC, Schoof DD, Scavone M, Eberlein TJ. Adoptive immunotherapy with tumor-infiltrating lymphocytes and interleukin-2 in patients with metastatic malignant melanoma and renal cell carcinoma: A pilot study. J Clin Oncol 1995, 13:1939-1949.
9. Harada M, Okamoto T, Omoto K, Tamada K, Takenoyama M, Hirashima C, Ito O, Kimura G, Nomoto K. Specific immunotherapy with tumour-draining lymph node cells cultured with both anti-CD3 and anti-CD28 monoclonal antibodies. Immunol 1996, 87:447-453.
10. Morse MA, Clay TM, Lyerly HK. Current status of adoptive immunotherapy of malignancies. Expert Opin Biol Ther 2002, 2:237-247. 10.1517/14712598.2.3.237, 11890864.
11. Nijhuis EWP, Wiel-van Kemenade EVD, Figdor CG, Van Lier RAW. Activation and expansion of tumour-infiltrating lymphocytes by anti-CD3 and anti-CD28 monoclonal antibodies. Cancer Immunol Immunother 1990, 32:245-250. 10.1007/BF01741708, 2175673.
12. Plautz GE, Cohen PA, Shu S. Considerations on clinical use of T cell immunotherapy for cancer. Arch. Immunol Ther Exp (Warsz) 2003, 51:245-257.
13. Ribas A, Butterfield LH, Glaspy JA, Economou JS. Current developments in cancer vaccines and cellular immunotherapy. J Clin Oncol 2003, 21:2415-2432. 10.1200/JCO.2003.06.041, 12805342.
14. Schoof DD, Selleck CM, Massaro AF, Jung SE, Eberlein TJ. Activation of human tumor-infiltrating lymphocytes by monoclonal antibodies directed to the CD3 complex. Cancer Res 1990, 50:1138-1143.
15. Yoshizawa H, Chang AE, Shu S. Specific adoptive immunotherapy mediated by tumor-draining lymph node cells sequentially activated with anti-CD3 and IL-2. J Immunol 1991, 147:729-737.
16. Alexander JP, Kudoh S, Melsop KA, Hamilton TA, Edinger MG, Tubbs RR, Sica D, Tuason L, Klein E, Bukowski RM. T-cells infiltrating renal cell carcinoma display a poor proliferative response even though they can produce interleukin 2 and express interleukin 2 receptors. Cancer Res 1993, 53:1380-1387.
17. Correa MR, Ochoa AC, Ghosh P, Mizoguchi H, Harvey L, Longo DL. Sequential development of structural and functional alterations in T cells from tumor-bearing mice. J Immunol 1997, 158:5292-5296.
18. Danna EA, Sinha P, Gilbert M, Clements VK, Pulaski BA, Ostrand-Rosenberg S. Surgical removal of primary tumor reverses tumor-induced immunosuppression despite the presence of metastatic disease. Cancer Res 2004, 64:2205-2211. 10.1158/0008-5472.CAN-03-2646, 15026364.
19. Tuttle TM, Inge TH, Bethke KP, McCrady CW, Pettit GR, Bear HD. Activation and growth of murine tumor-specific T-cells which have in vivo activity with bryostatin 1. Cancer Res 1992, 52:548-553.
20. Tuttle TM, Bethke KP, Inge TH, McCrady CW, Pettit GR, Bear HD. Bryostatin 1-activated T cells can traffic and mediate tumor regression. J Surg Res 1992, 52:543-548. 10.1016/0022-4804(92)90126-K, 1528028.
21. Tuttle TM, McCrady CW, Inge TH, Salour M, Bear HD. γ-interferon plays a key role in T-cell-induced tumor regression. Cancer Res 1993, 53:833-839.
22. Tuttle TM, Fleming MF, Hogg PS, Inge TH, Bear HD. Low-dose cyclophosphamide overcomes metastasis-induced immunosuppression. Ann Surg Oncol 1994, 1:53-58. 10.1007/BF02303541, 7834429.
23. Yee C. Adoptive T cell therapy--immune monitoring and MHC multimers. Clin Immunol 2003, 106:5-9. 10.1016/S1521-6616(02)00015-3, 12584044.
24. Cantrell D. T cell antigen receptor signal transduction pathways. Annu Rev Immunol 1996, 14:259-274. 10.1146/annurev.immunol.14.1.259, 8717515.
25. Kazanietz MG, Lewin NE, Gao F, Pettit GR, Blumberg PM. Binding of [26-3H]bryostatin 1 and analogs to calcium- dependent and calcium-independent protein kinase C isozymes. Mol Pharmacol 1994, 46:374-379.
26. Pettit GR, Herald SL, Doubek DL, Arnold E, Clardy J. Isolation and structure of bryostatin 1. J Am Chem Soc 1982, 104:6846-6848.
27. Chatila T, Silverman L, Miller R, Geha R. Mechanisms of T cell activation by the calcium ionophore ionomycin. J Immunol 1989, 143:1283-1289.
28. Chin CS, Miller CH, Graham L, Parviz M, Zacur S, Patel B, Duong A, Bear HD. Bryostatin 1/ionomycin (B/I) ex vivo stimulation preferentially activates L-selectinlow tumor-sensitized lymphocytes. Int Immunol 2004, 16:1283-1294. 10.1093/intimm/dxh130, 15262898.
29. Kagamu H, Shu SY. Purification of L-selectinlow cells promotes the generation of highly potent CD4 antitumor effector T lymphocytes. J Immunol 1998, 160:3444-3452.
30. Kjaergaard J, Shu SY. Tumor infiltration by adoptively transferred T cells is independent of immunologic specificity but requires down-regulation of L-selectin expression. J Immunol 1999, 163:751-759.
31. Parviz M, Chin CS, Graham LJ, Miller C, Lee C, George K, Bear HD. Successful adoptive immunotherapy with vaccine-sensitized T cells, despite no effect with vaccination alone in a weakly immunogenic tumor model. Cancer Immunol Immunother 2003, 52:739-750. 10.1007/s00262-003-0405-8, 12827306.
32. Aruga A, Aruga E, Tanigawa K, Bishop DK, Sondak VK, Chang AE. Type 1 versus type 2 cytokine release by Vb T cell subpopulations determines the in vivo antitumor reactivity: IL-10 mediates a suppressive role. J Immunol 1997, 159:664-673.
33. Lowes MA, Bishop GA, Crotty K, Barnetson RS, Halliday GM. T helper 1 cytokine mRNA is increased in spontaneously regressing primary melanomas. J Invest Dermatol 1997, 108:914-919. 10.1111/1523-1747.ep12292705, 9182821.
34. Tsung K, Meko JB, Peplinski GR, Tsung TL, Norton JA. IL-12 induces T helper-1 directed antitumor responses. J Immunol 1997, 158:3359-3365.
35. Winter H, Hu HM, McClain K, Urba WJ, Fox BA. Immunotherapy of melanoma: A dichotomy in the requirement for IFN-γ in vaccine-induced antitumor immunity versus adoptive immunotherapy. J Immunol 2001, 166:7370-7380.
36. Zitvogel L, Mayordomo JI, Tjandrawan T, Deleo AB, Clarke MR, Lotze MT, Storkus WJ. Therapy of murine tumors with tumor peptide-pulsed dendritic cells: Dependence on T cells, B7 costimulation, and T helper cell 1-associated cytokines. J Exp Med 1996, 183:87-97. 10.1084/jem.183.1.87, 2192415, 8551248.
37. Hu HM, Urba WJ, Fox BA. Gene-modified tumor vaccine with therapeutic potential shifts tumor-specific T cell response from type 2 to type 1 cytokine profile. J Immunol 1998, 161:3033-3041.
38. Gattinoni L, Klebanoff CA, Palmer DC, Wrzesinski C, Kerstann K, Yu Z, Finkelstein SE, Theoret MR, Rosenberg SA, Restifo NP. Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8(+) T cells. J Clin Invest 2005, 115:1616-1626. 10.1172/JCI24480, 1137001, 15931392.
39. Klebanoff CA, Gattinoni L, Torabi-Parizi P, Kerstann K, Cardones AR, Finkelstein SE, Palmer DC, Antony PA, Hwang ST, Rosenberg SA, Waldmann TA, Restifo NP. Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc Natl Acad Sci USA 2005, 102:9571-9576. 10.1073/pnas.0503726102, 1172264, 15980149.
40. Wrzesinski C, Restifo NP. Less is more: lymphodepletion followed by hematopoietic stem cell transplant augments adoptive T-cell-based anti-tumor immunotherapy. Curr Opin Immunol 2005, 17:195-201. 10.1016/j.coi.2005.02.002, 2254579, 15766681.
41. Wherry EJ, Ahmed R. Memory CD8 T-cell differentiation during viral infection. J Virol 2004, 78:5535-5545. 10.1128/JVI.78.11.5535-5545.2004, 415833, 15140950.
42. Wherry EJ, Teichgraber V, Becker TC, Masopust D, Kaech SM, Antia R, Von Andrian UH, Ahmed R. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol 2003, 4:225-234. 10.1038/ni889, 12563257.
43. Sallusto F, Geginat J, Lanzavecchia A. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu Rev Immunol 2004, 22:745-63. 10.1146/annurev.immunol.22.012703.104702, 15032595.
44. Lanzavecchia A, Sallusto F. Understanding the generation and function of memory T cell subsets. Curr Opin Immunol 2005, 17:326-332. 10.1016/j.coi.2005.04.010, 15886125.
45. Roberts AD, Ely KH, Woodland DL. Differential contributions of central and effector memory T cells to recall responses. J Exp Med 2005, 202:123-133. 10.1084/jem.20050137, 2212898, 15983064.
46. Tough DF. Deciphering the relationship between central and effector memory CD8+ T cells. Trends Immunol 2003, 24:404-407. 10.1016/S1471-4906(03)00169-8, 12909449.
47. Hiura T, Kagamu H, Miura S, Ishida A, Tanaka H, Tanaka J, Gejyo F, Yoshizawa H. Both regulatory T cells and antitumor effector T cells are primed in the same draining lymph nodes during tumor progression. J Immunol 2005, 175:5058-5066.
48. Jabbari A, Harty JT. The generation and modulation of antigen-specific memory CD8 T cell responses. J Leukoc Biol 2006, 80:16-23. 10.1189/jlb.0206118, 16684891.
49. Badovinac VP, Porter BB, Harty JT. Programmed contraction of CD8(+) T cells after infection. Nat Immunol 2002, 3:619-626. 10.1038/nrm880, 12055624.
50. Barber DL, Wherry EJ, Ahmed R. Cutting edge: rapid in vivo killing by memory CD8 T cells. J Immunol 2003, 171:27-31.
51. Jabbari A, Harty JT. Secondary memory CD8+ T cells are more protective but slower to acquire a central-memory phenotype. J Exp Med 2006, 203:919-932. 10.1084/jem.20052237, 2118270, 16567385.
52. Roberts AD, Woodland DL. Cutting edge: effector memory CD8+ T cells play a prominent role in recall responses to secondary viral infection in the lung. J Immunol 2004, 172:6533-6537.
53. Veiga-Fernandes H, Walter U, Bourgeois C, McLean A, Rocha B. Response of naive and memory CD8+ T cells in antigen stimulation in vivo. Nature Immunology 2000, 1:47-53. 10.1038/76907, 10881174.
54. Polak L, Geleick H, Turk JL. Reversal by cyclophosphamide of tolerance in contact sensitization. Tolerance induced by prior feeding with DNCB. Immunology 1975, 28:939-942. 1445923, 1132885.
55. Yasunami R, Bach JF. Anti-suppressor effect of cyclophosphamide on the development of spontaneous diabetes in NOD mice. Eur J Immunol 1988, 18:481-484. 10.1002/eji.1830180325, 2965652.
56. Mitsuoka A, Baba M, Morikawa S. Enhancement of delayed hypersensitivity by depletion of suppressor T cells with cyclophosphamide in mice. Nature 1976, 262:77-78. 10.1038/262077a0, 1084484.
57. Rollinghoff M, Starzinski-Powitz A, Pfizenmaier K, Wagner H. Cyclophosphamide-sensitive T lymphocytes suppress the in vivo generation of antigen-specific cytotoxic T lymphocytes. J Exp Med 1977, 145:455-459. 10.1084/jem.145.2.455, 2180611, 299883.
58. Asherson GL, Ptak W. Contact and delayed hypersensitivity in the mouse. I. Active sensitization and passive transfer. Immunology 1968, 15:405-416. 1409462, 4177017.
59. Maguire JRHC, Ettore VL. Enhancement of dinitrochlorobenzene (DNCB) contact sensitization by cyclophosphamide in the guinea pig. J Invest Dermatol 1967, 48:39-43.
60. Sullivan S, Bergstresser PR, Streilein JW. Analysis of dose response of trinitrochlorobenzene contact hypersensitivity induction in mice: pretreatment with cyclophosphamide reveals an optimal sensitizing dose. J Invest Dermatol 1990, 94:711-716. 10.1111/1523-1747.ep12876288, 2324526.
61. Beyer M, Kochanek M, Darabi K, Popov A, Jensen M, Endl E, Knolle PA, Thomas RK, von Bergwelt-Baildon M, Debey S, Hallek M, Schultze JL. Reduced frequencies and suppressive function of CD4+CD25hi regulatory T cells in patients with chronic lymphocytic leukemia after therapy with fludarabine. Blood 2005, 106:2018-2025. 10.1182/blood-2005-02-0642, 15914560.
62. Lutsiak ME, Semnani RT, De PR, Kashmiri SV, Schlom J, Sabzevari H. Inhibition of CD4(+)25+ T regulatory cell function implicated in enhanced immune response by low-dose cyclophosphamide. Blood 2005, 105:2862-2868. 10.1182/blood-2004-06-2410, 15591121.
63. Ikezawa Y, Nakazawa M, Tamura C, Takahashi K, Minami M, Ikezawa Z. Cyclophosphamide decreases the number, percentage and the function of CD25+ CD4+ regulatory T cells, which suppress induction of contact hypersensitivity. J Dermatol Sci 2005, 39:105-112. 10.1016/j.jdermsci.2005.02.002, 15899580.
64. Ghiringhelli F, Larmonier N, Schmitt E, Parcellier A, Cathelin D, Garrido C, Chauffert B, Solary E, Bonnotte B, Martin F. CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative. Eur J Immunol 2004, 34:336-344. 10.1002/eji.200324181, 14768038.
65. Ercolini AM, Ladle BH, Manning EA, Pfannenenstiel LW, Armstrong TD, Machiels JPH, Bieler JG, Emens LA, Reilly T, Jaffee EM. Recruitment of latent pools of high-avidity CD8+ T cells to the antitumor immune response. J Exp Med 2007, 201:1591-1602.
66. Proietti E, Greco G, Garrone B, Baccarini S, Mauri C, Venditti M, Carlei D, Belardelli F. Importance of cyclophosphamide-induced bystander effect on T cells for a successful tumor eradication in response to adoptive immunotherapy in mice. J Clin Invest 1998, 101:429-441. 10.1172/JCI1348, 508583, 9435316.