Advertisement

What Is the Future of Immunotherapy in Ovarian Cancer?

  • Lana E. Kandalaft
  • Klara Balint
  • Jonathan S. Berek
  • George Coukos
Chapter

Abstract

Over the past several years, significant progress has been made in the treatment of gynecologic cancers. However, continued improvements to existing therapies, as well as development of novel approaches to treat these diseases, will be necessary to further reduce mortality. With increasing evidence that ovarian cancer in particular is immunogenic, there is a good reason to investigate the potential of immunotherapies. Recent success in a number of immunotherapy clinical trials targeting other tumor types has laid the groundwork necessary to begin using similar therapies against ovarian and other gynecologic cancers. Here we review past experience and future opportunities for immunotherapy in ovarian cancer, with a focus on vaccines and adoptive T-cell therapy, as well as several nonspecific immunomodulators available for immediate clinical testing.

Keywords

Ovarian Cancer Adoptive Transfer Ovarian Cancer Patient Cancer Vaccine Chimeric Antigen Receptor 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Schlienger K, Chu CS, Woo EY, Rivers PM, Toll AJ, Hudson B, et al. TRANCE- and CD40 ligand-matured dendritic cells reveal MHC class I-restricted T cells specific for autologous tumor in late-stage ovarian cancer patients. Clin Cancer Res. 2003;9(4):1517–27. PubMed PMID: 12684428. Epub 2003/04/10.PubMedGoogle Scholar
  2. 2.
    Goodell V, Salazar LG, Urban N, Drescher CW, Gray H, Swensen RE, et al. Antibody immunity to the p53 oncogenic protein is a prognostic indicator in ovarian cancer. J Clin Oncol. 2006;24(5):762–8. PubMed PMID: 16391298.PubMedCrossRefGoogle Scholar
  3. 3.
    Hayashi K, Yonamine K, Masuko-Hongo K, Iida T, Yamamoto K, Nishioka K, et al. Clonal expansion of T cells that are specific for autologous ovarian tumor among tumor-infiltrating T cells in humans. Gynecol Oncol. 1999;74(1):86–92. PubMed PMID: 10385556.PubMedCrossRefGoogle Scholar
  4. 4.
    Halapi E, Yamamoto Y, Juhlin C, Jeddi-Tehrani M, Grunewald J, Andersson R, et al. Restricted T cell receptor V-beta and J-beta usage in T cells from interleukin-2-cultured lymphocytes of ovarian and renal carcinomas. Cancer Immunol Immunother. 1993;36(3):191–7. PubMed PMID: 8439980. Epub 1993/01/01.PubMedCrossRefGoogle Scholar
  5. 5.
    Fisk B, Blevins TL, Wharton JT, Ioannides CG. Identification of an immunodominant peptide of HER-2/neu protooncogene recognized by ovarian tumor-specific cytotoxic T lymphocyte lines. J Exp Med. 1995;181(6):2109–17. PubMed PMID: 7539040. Pubmed Central PMCID: 2192068. Epub 1995/06/01.PubMedCrossRefGoogle Scholar
  6. 6.
    Kooi S, Freedman RS, Rodriguez-Villanueva J, Platsoucas CD. Cytokine production by T-cell lines derived from tumor-infiltrating lymphocytes from patients with ovarian carcinoma: tumor-specific immune responses and inhibition of antigen-independent cytokine production by ovarian tumor cells. Lymphokine Cytokine Res. 1993;12(6):429–37. PubMed PMID: 8123759. Epub 1993/12/01.PubMedGoogle Scholar
  7. 7.
    Peoples GE, Goedegebuure PS, Smith R, Linehan DC, Yoshino I, Eberlein TJ. Breast and ovarian cancer-specific cytotoxic T lymphocytes recognize the same HER2/neu-derived peptide. Proc Natl Acad Sci U S A. 1995;92(2):432–6. PubMed PMID: 7831305.PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    Peoples GE, Anderson BW, Fisk B, Kudelka AP, Wharton JT, Ioannides CG. Ovarian cancer-associated lymphocyte recognition of folate binding protein peptides. Ann Surg Oncol. 1998;5(8):743–50. PubMed PMID: 9869522.PubMedCrossRefGoogle Scholar
  9. 9.
    Dadmarz RD, Ordoubadi A, Mixon A, Thompson CO, Barracchini KC, Hijazi YM, et al. Tumor-infiltrating lymphocytes from human ovarian cancer patients recognize autologous tumor in an MHC class II-restricted fashion. Cancer J Sci Am. 1996;2(5):263–72. PubMed PMID: 9166543. Epub 1996/10/01.PubMedGoogle Scholar
  10. 10.
    Santin AD, Bellone S, Ravaggi A, Pecorelli S, Cannon MJ, Parham GP. Induction of ovarian tumor-specific CD8+ cytotoxic T lymphocytes by acid-eluted peptide-pulsed autologous dendritic cells. Obstet Gynecol. 2000;96(3):422–30. PubMed PMID: 10960637. Epub 2000/08/29.PubMedCrossRefGoogle Scholar
  11. 11.
    Peoples GE, Schoof DD, Andrews JV, Goedegebuure PS, Eberlein TJ. T-cell recognition of ovarian cancer. Surgery. 1993;114(2):227–34. PubMed PMID: 8342128.PubMedGoogle Scholar
  12. 12.
    Albert ML, Darnell JC, Bender A, Francisco LM, Bhardwaj N, Darnell RB. Tumor-specific killer cells in paraneoplastic cerebellar degeneration. Nat Med. 1998;4(11):1321–4. PubMed PMID: 9809559. Epub 1998/11/11.PubMedCrossRefGoogle Scholar
  13. 13.
    Lanitis E, Poussin M, Hagemann IS, Coukos G, Sandaltzopoulos R, Scholler N, et al. Redirected antitumor activity of primary human lymphocytes transduced with a fully human anti-mesothelin chimeric receptor. Mol Ther. 2012;20(3):633–43.PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Odunsi K, Matsuzaki J, Karbach J, Neumann A, Mhawech-Fauceglia P, Miller A, et al. Efficacy of vaccination with recombinant vaccinia and fowlpox vectors expressing NY-ESO-1 antigen in ovarian cancer and melanoma patients. Proc Natl Acad Sci U S A. 2012;109(15):5797–802. PubMed PMID: 22454499. Pubmed Central PMCID: 3326498. Epub 2012/03/29.PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    Chu CS, Kim SH, June CH, Coukos G. Immunotherapy opportunities in ovarian cancer. Expert Rev Anticancer Ther. 2008;8(2):243–57. PubMed PMID: 18279065.PubMedCrossRefGoogle Scholar
  16. 16.
    Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, Regnani G, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med. 2003;348(3):203–13. PubMed PMID: 12529460. Epub 2003/01/17.PubMedCrossRefGoogle Scholar
  17. 17.
    Adams SF, Levine DA, Cadungog MG, Hammond R, Facciabene A, Olvera N, et al. Intraepithelial T cells and tumor proliferation: impact on the benefit from surgical cytoreduction in advanced serous ovarian cancer. Cancer. 2009;115(13):2891–902. PubMed PMID: 19472394. Epub 2009/05/28.PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Clarke B, Tinker AV, Lee C, Subramanian S, van de Rijn M, Turbin D, et al. Intraepithelial T cells and prognosis in ovarian carcinoma: novel associations with stage, tumor type and BRCA1 loss. Mod Pathol. 2009;22(3):393–402.PubMedCrossRefGoogle Scholar
  19. 19.
    Hamanishi J, Mandai M, Iwasaki M, Okazaki T, Tanaka Y, Yamaguchi K, et al. Programmed cell death 1 ligand 1 and tumor-infiltrating CD8+ T lymphocytes are prognostic factors of human ovarian cancer. Proc Natl Acad Sci U S A. 2007;104(9):3360–5. PubMed PMID: 17360651.PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Sato E, Olson SH, Ahn J, Bundy B, Nishikawa H, Qian F, et al. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci U S A. 2005;102(51):18538–43. PubMed PMID: 16344461. Pubmed Central PMCID: 1311741. Epub 2005/12/14.PubMedCentralPubMedCrossRefGoogle Scholar
  21. 21.
    Shah CA, Allison KH, Garcia RL, Gray HJ, Goff BA, Swisher EM. Intratumoral T cells, tumor-associated macrophages, and regulatory T cells: association with p53 mutations, circulating tumor DNA and survival in women with ovarian cancer. Gynecol Oncol. 2008;109(2):215–9. PubMed PMID: 18314181.PubMedCrossRefGoogle Scholar
  22. 22.
    Woo EY, Chu CS, Goletz TJ, Schlienger K, Yeh H, Coukos G, et al. Regulatory CD4(+)CD25(+) T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer. Cancer Res. 2001;61(12):4766–72. PubMed PMID: 11406550. Epub 2001/06/19.PubMedGoogle Scholar
  23. 23.
    Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med. 2004;10(9):942–9. PubMed PMID: 15322536. Epub 2004/08/24.PubMedCrossRefGoogle Scholar
  24. 24.
    Kryczek I, Wei S, Zhu G, Myers L, Mottram P, Cheng P, et al. Relationship between B7-H4, regulatory T cells, and patient outcome in human ovarian carcinoma. Cancer Res. 2007;67(18):8900–5. PubMed PMID: 17875732.PubMedCrossRefGoogle Scholar
  25. 25.
    Buckanovich RJ, Facciabene A, Kim S, Benencia F, Sasaroli D, Balint K, et al. Endothelin B receptor mediates the endothelial barrier to T cell homing to tumors and disables immune therapy. Nat Med. 2008;14(1):28–36. PubMed PMID: 18157142.PubMedCrossRefGoogle Scholar
  26. 26.
    Kandalaft LE, Facciabene A, Buckanovich RJ, Coukos G. Endothelin B receptor, a new target in cancer immune therapy. Clin Cancer Res. 2009;15(14):4521–8. PubMed PMID: 19567593. Epub 2009/07/02.PubMedCentralPubMedCrossRefGoogle Scholar
  27. 27.
    Yoshihara K, Tsunoda T, Shigemizu D, Fujiwara H, Hatae M, Masuzaki H, et al. High-risk ovarian cancer based on 126-gene expression signature is uniquely characterized by downregulation of antigen presentation pathway. Clin Cancer Res. 2012;18(5):1374–85. PubMed PMID: 22241791. Epub 2012/01/14.PubMedCrossRefGoogle Scholar
  28. 28.
    Rosenberg SA, Dudley ME. Adoptive cell therapy for the treatment of patients with metastatic melanoma. Curr Opin Immunol. 2009;21(2):233–40. PubMed PMID: 19304471. Epub 2009/03/24.PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Edwards RP, Gooding W, Lembersky BC, Colonello K, Hammond R, Paradise C, et al. Comparison of toxicity and survival following intraperitoneal recombinant interleukin-2 for persistent ovarian cancer after platinum: twenty-four-hour versus 7-day infusion. J Clin Oncol. 1997;15(11):3399–407. PubMed PMID: 9363872.PubMedGoogle Scholar
  30. 30.
    Vlad AM, Budiu RA, Lenzner DE, Wang Y, Thaller JA, Colonello K, et al. A phase II trial of intraperitoneal interleukin-2 in patients with platinum-resistant or platinum-refractory ovarian cancer. Cancer Immunol Immunother. 2010;59(2):293–301. PubMed PMID: 19690855. Epub 2009/08/20.PubMedCrossRefGoogle Scholar
  31. 31.
    Hodi FS, Butler M, Oble DA, Seiden MV, Haluska FG, Kruse A, et al. Immunologic and clinical effects of antibody blockade of cytotoxic T lymphocyte-associated antigen 4 in previously vaccinated cancer patients. Proc Natl Acad Sci U S A. 2008;105(8):3005–10. PubMed PMID: 18287062. Epub 2008/02/22.PubMedCentralPubMedCrossRefGoogle Scholar
  32. 32.
    Hodi FS, Mihm MC, Soiffer RJ, Haluska FG, Butler M, Seiden MV, et al. Biologic activity of cytotoxic T lymphocyte-associated antigen 4 antibody blockade in previously vaccinated metastatic melanoma and ovarian carcinoma patients. Proc Natl Acad Sci U S A. 2003;100(8):4712–7. PubMed PMID: 12682289.PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Fujita K, Ikarashi H, Takakuwa K, Kodama S, Tokunaga A, Takahashi T, et al. Prolonged disease-free period in patients with advanced epithelial ovarian cancer after adoptive transfer of tumor-infiltrating lymphocytes. Clin Cancer Res. 1995;1(5):501–7. PubMed PMID: 9816009.PubMedGoogle Scholar
  34. 34.
    Aoki Y, Takakuwa K, Kodama S, Tanaka K, Takahashi M, Tokunaga A, et al. Use of adoptive transfer of tumor-infiltrating lymphocytes alone or in combination with cisplatin-containing chemotherapy in patients with epithelial ovarian cancer. Cancer Res. 1991;51(7):1934–9. PubMed PMID: 2004379.PubMedGoogle Scholar
  35. 35.
    Hung CF, Wu TC, Monie A, Roden R. Antigen-specific immunotherapy of cervical and ovarian cancer. Immunol Rev. 2008;222:43–69. PubMed PMID: 18363994. Pubmed Central PMCID: 2692865. Epub 2008/03/28.PubMedCentralPubMedCrossRefGoogle Scholar
  36. 36.
    Odunsi K, Sabbatini P. Harnessing the immune system for ovarian cancer therapy. Am J Reprod Immunol. 2008;59(1):62–74. PubMed PMID: 18154597. Epub 2007/12/25.PubMedCrossRefGoogle Scholar
  37. 37.
    Sabbatini P, Odunsi K. Immunologic approaches to ovarian cancer treatment. J Clin Oncol. 2007;25(20):2884–93. PubMed PMID: 17617519. Epub 2007/07/10.PubMedCrossRefGoogle Scholar
  38. 38.
    Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med. 2004;10(9):909–15. PubMed PMID: 15340416.PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    Sabbatini P, Spriggs D, Aghajanian C, Hensley M, Tew W, Konner J, et al. Consolidation strategies in ovarian cancer: observations for future clinical trials. Gynecol Oncol. 2010;116(1):66–71. PubMed PMID: 19836827. Epub 2009/10/20.PubMedCrossRefGoogle Scholar
  40. 40.
    Reinartz S, Kohler S, Schlebusch H, Krista K, Giffels P, Renke K, et al. Vaccination of patients with advanced ovarian carcinoma with the anti-idiotype ACA125: immunological response and survival (phase Ib/II). Clin Cancer Res. 2004;10(5):1580–7. PubMed PMID: 15014007.PubMedCrossRefGoogle Scholar
  41. 41.
    Gulley JL, Arlen PM, Tsang KY, Yokokawa J, Palena C, Poole DJ, et al. Pilot study of vaccination with recombinant CEA-MUC-1-TRICOM poxviral-based vaccines in patients with metastatic carcinoma. Clin Cancer Res. 2008;14(10):3060–9. PubMed PMID: 18483372. Pubmed Central PMCID: 2673097. Epub 2008/05/17.PubMedCentralPubMedCrossRefGoogle Scholar
  42. 42.
    Disis ML, Goodell V, Schiffman K, Knutson KL. Humoral epitope-spreading following immunization with a HER-2/neu peptide based vaccine in cancer patients. J Clin Immunol. 2004;24(5):571–8. PubMed PMID: 15359116.PubMedCrossRefGoogle Scholar
  43. 43.
    Chianese-Bullock KA, Irvin Jr WP, Petroni GR, Murphy C, Smolkin M, Olson WC, et al. A multipeptide vaccine is safe and elicits T-cell responses in participants with advanced stage ovarian cancer. J Immunother. 2008;31(4):420–30. PubMed PMID: 18391753. Epub 2008/04/09.PubMedCrossRefGoogle Scholar
  44. 44.
    Tsuda N, Mochizuki K, Harada M, Sukehiro A, Kawano K, Yamada A, et al. Vaccination with predesignated or evidence-based peptides for patients with recurrent gynecologic cancers. J Immunother (1997). 2004;27(1):60–72. PubMed PMID: 14676634.CrossRefGoogle Scholar
  45. 45.
    Chu CS, Boyer J, Coukos G, Rubin SC, Morgan MA, Bendig DL. Autologous dendritic cell (IDD-6) vaccination as consolidation for advanced ovarian cancer. In: SGO annual meeting on women’s cancer. Tampa; 2008.Google Scholar
  46. 46.
    Hernando JJ, Park TW, Kubler K, Offergeld R, Schlebusch H, Bauknecht T. Vaccination with autologous tumour antigen-pulsed dendritic cells in advanced gynaecological malignancies: clinical and immunological evaluation of a phase I trial. Cancer Immunol Immunother. 2002;51(1):45–52. PubMed PMID: 11845259. Epub 2002/02/15.PubMedCrossRefGoogle Scholar
  47. 47.
    Gong J, Nikrui N, Chen D, Koido S, Wu Z, Tanaka Y, et al. Fusions of human ovarian carcinoma cells with autologous or allogeneic dendritic cells induce antitumor immunity. J Immunol. 2000;165(3):1705–11. PubMed PMID: 10903782.PubMedGoogle Scholar
  48. 48.
    Ioannides CG, Platsoucas CD, Freedman RS. Immunological effects of tumor vaccines: II. T cell responses directed against cellular antigens in the viral oncolysates. In Vivo. 1990;4(1):17–24. PubMed PMID: 2103838.PubMedGoogle Scholar
  49. 49.
    Ioannides CG, Platsoucas CD, Patenia R, Kim YP, Bowen JM, Morris M, et al. T-cell functions in ovarian cancer patients treated with viral oncolysates: I. Increased helper activity to immunoglobulins production. Anticancer Res. 1990;10(3):645–53. PubMed PMID: 2142392.PubMedGoogle Scholar
  50. 50.
    Schirrmacher V. Clinical trials of antitumor vaccination with an autologous tumor cell vaccine modified by virus infection: improvement of patient survival based on improved antitumor immune memory. Cancer Immunol Immunother. 2005;54(6):587–98. PubMed PMID: 15526097.PubMedCrossRefGoogle Scholar
  51. 51.
    Benencia F, Courreges MC, Conejo-Garcia JR, Mohammed-Hadley A, Coukos G. Direct vaccination with tumor cells killed with ICP4-deficient HSVd120 elicits effective antitumor immunity. Cancer Biol Ther. 2006;5(7):867–74. PubMed PMID: 16861891.PubMedCrossRefGoogle Scholar
  52. 52.
    Benencia F, Courreges MC, Coukos G. Whole tumor antigen vaccination using dendritic cells: comparison of RNA electroporation and pulsing with UV-irradiated tumor cells. J Transl Med. 2008;6:21. PubMed PMID: 18445282.PubMedCentralPubMedCrossRefGoogle Scholar
  53. 53.
    Benencia F, Courreges MC, Fraser NW, Coukos G. Herpes virus oncolytic therapy reverses tumor immune dysfunction and facilitates tumor antigen presentation. Cancer Biol Ther. 2008;7(8):1194–205. PubMed PMID: 18458533.PubMedCrossRefGoogle Scholar
  54. 54.
    Carter SL, Cibulskis K, Helman E, McKenna A, Shen H, Zack T, et al. Absolute quantification of somatic DNA alterations in human cancer. Nat Biotechnol. 2012;30(5):413–21.PubMedCrossRefGoogle Scholar
  55. 55.
    Odunsi K, Qian F, Matsuzaki J, Mhawech-Fauceglia P, Andrews C, Hoffman EW, et al. Vaccination with an NY-ESO-1 peptide of HLA class I/II specificities induces integrated humoral and T cell responses in ovarian cancer. Proc Natl Acad Sci U S A. 2007;104(31):12837–42. PubMed PMID: 17652518. Pubmed Central PMCID: 1937553. Epub 2007/07/27.PubMedCentralPubMedCrossRefGoogle Scholar
  56. 56.
    Neller MA, López JA, Schmidt CW. Antigens for cancer immunotherapy. Semin Immunol. 2008;20(5):286–95.PubMedCrossRefGoogle Scholar
  57. 57.
    Cannon MJ, O’Brien TJ. Cellular immunotherapy for ovarian cancer. Expert Opin Biol Ther. 2009;9(6):677–88. PubMed PMID: 19456205. Epub 2009/05/22.PubMedCentralPubMedCrossRefGoogle Scholar
  58. 58.
    van der Bruggen P, Traversari C, Chomez P, Lurquin C, De Plaen E, Van den Eynde B, et al. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science. 1991;254(5038):1643–7. PubMed PMID: 1840703. Epub 1991/12/13.PubMedCrossRefGoogle Scholar
  59. 59.
    Pardoll DM. Spinning molecular immunology into successful immunotherapy. Nat Rev Immunol. 2002;2(4):227–38. PubMed PMID: 12001994.PubMedCrossRefGoogle Scholar
  60. 60.
    Gulley JL. Therapeutic vaccines: the ultimate personalized therapy? Human Vaccin Immunother. 2013;9(1):219–21. PubMed PMID: 22995839.CrossRefGoogle Scholar
  61. 61.
    June CH. Adoptive T, cell therapy for cancer in the clinic. J Clin Invest. 2007;117(6):1466–76. PubMed PMID: 17549249. Epub 2007/06/06.PubMedCentralPubMedCrossRefGoogle Scholar
  62. 62.
    Dudley ME, Wunderlich JR, Yang JC, Sherry RM, Topalian SL, Restifo NP, et al. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol. 2005;23(10):2346–57. PubMed PMID: 15800326.PubMedCentralPubMedCrossRefGoogle Scholar
  63. 63.
    Yee C, Thompson JA, Byrd D, Riddell SR, Roche P, Celis E, et al. Adoptive T cell therapy using antigen-specific CD8+ T cell clones for the treatment of patients with metastatic melanoma: in vivo persistence, migration, and antitumor effect of transferred T cells. Proc Natl Acad Sci U S A. 2002;99(25):16168–73. PubMed PMID: 12427970. Epub 2002/11/13.PubMedCentralPubMedCrossRefGoogle Scholar
  64. 64.
    Perret R, Ronchese F. Memory T cells in cancer immunotherapy: which CD8 T-cell population provides the best protection against tumours? Tissue Antigens. 2008;72(3):187–94. PubMed PMID: 18627571. Epub 2008/07/17.PubMedCrossRefGoogle Scholar
  65. 65.
    Gattinoni L, Finkelstein SE, Klebanoff CA, Antony PA, Palmer DC, Spiess PJ, et al. Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells. J Exp Med. 2005;202(7):907–12. PubMed PMID: 16203864. Pubmed Central PMCID: 1397916. Epub 2005/10/06.PubMedCentralPubMedCrossRefGoogle Scholar
  66. 66.
    Huang J, Kerstann KW, Ahmadzadeh M, Li YF, El-Gamil M, Rosenberg SA, et al. Modulation by IL-2 of CD70 and CD27 expression on CD8+ T cells: importance for the therapeutic effectiveness of cell transfer immunotherapy. J Immunol. 2006;176(12):7726–35. PubMed PMID: 16751420. Epub 2006/06/06.PubMedCentralPubMedGoogle Scholar
  67. 67.
    Powell Jr DJ, Dudley ME, Robbins PF, Rosenberg SA. Transition of late-stage effector T cells to CD27+ CD28+ tumor-reactive effector memory T cells in humans after adoptive cell transfer therapy. Blood. 2005;105(1):241–50. PubMed PMID: 15345595. Epub 2004/09/04.PubMedCentralPubMedCrossRefGoogle Scholar
  68. 68.
    Shen X, Zhou J, Hathcock KS, Robbins P, Powell Jr DJ, Rosenberg SA, et al. Persistence of tumor infiltrating lymphocytes in adoptive immunotherapy correlates with telomere length. J Immunother (1997). 2007;30(1):123–9. PubMed PMID: 17198091. Epub 2007/01/02.CrossRefGoogle Scholar
  69. 69.
    Zhou J, Shen X, Huang J, Hodes RJ, Rosenberg SA, Robbins PF. Telomere length of transferred lymphocytes correlates with in vivo persistence and tumor regression in melanoma patients receiving cell transfer therapy. J Immunol. 2005;175(10):7046–52. PubMed PMID: 16272366. Epub 2005/11/08.PubMedCentralPubMedGoogle Scholar
  70. 70.
    Hinrichs CS, Borman ZA, Cassard L, Gattinoni L, Spolski R, Yu Z, et al. Adoptively transferred effector cells derived from naive rather than central memory CD8+ T cells mediate superior antitumor immunity. Proc Natl Acad Sci U S A. 2009;106(41):17469–74. PubMed PMID: 19805141. Epub 2009/10/07.PubMedCentralPubMedCrossRefGoogle Scholar
  71. 71.
    Suhoski MM, Golovina TN, Aqui NA, Tai VC, Varela-Rohena A, Milone MC, et al. Engineering artificial antigen-presenting cells to express a diverse array of co-stimulatory molecules. Mol Ther. 2007;15(5):981–8. PubMed PMID: 17375070.PubMedCrossRefGoogle Scholar
  72. 72.
    Sadelain M, Riviere I, Brentjens R. Targeting tumours with genetically enhanced T lymphocytes. Nat Rev Cancer. 2003;3(1):35–45. PubMed PMID: 12509765. Epub 2003/01/02.PubMedCrossRefGoogle Scholar
  73. 73.
    Walker RE, Bechtel CM, Natarajan V, Baseler M, Hege KM, Metcalf JA, et al. Long-term in vivo survival of receptor-modified syngeneic T cells in patients with human immunodeficiency virus infection. Blood. 2000;96(2):467–74. PubMed PMID: 10887107. Epub 2000/07/11.PubMedGoogle Scholar
  74. 74.
    Brocker T, Karjalainen K. Adoptive tumor immunity mediated by lymphocytes bearing modified antigen-specific receptors. Adv Immunol. 1998;68:257–69. PubMed PMID: 9505091.PubMedCrossRefGoogle Scholar
  75. 75.
    Gross G, Waks T, Eshhar Z. Expression of immunoglobulin-T-cell receptor chimeric molecules as functional receptors with antibody-type specificity. Proc Natl Acad Sci U S A. 1989;86(24):10024–8. PubMed PMID: 2513569. Pubmed Central PMCID: 298636. Epub 1989/12/01.PubMedCentralPubMedCrossRefGoogle Scholar
  76. 76.
    Pinthus JH, Waks T, Kaufman-Francis K, Schindler DG, Harmelin A, Kanety H, et al. Immuno-gene therapy of established prostate tumors using chimeric receptor-redirected human lymphocytes. Cancer Res. 2003;63(10):2470–6. PubMed PMID: 12750268.PubMedGoogle Scholar
  77. 77.
    Freedman RS, Edwards CL, Kavanagh JJ, Kudelka AP, Katz RL, Carrasco CH, et al. Intraperitoneal adoptive immunotherapy of ovarian carcinoma with tumor-infiltrating lymphocytes and low-dose recombinant interleukin-2: a pilot trial. J Immunother Emphasis Tumor Immunol. 1994;16(3):198–210. PubMed PMID: 7834119.PubMedCrossRefGoogle Scholar
  78. 78.
    Ioannides CG, Den Otter W. Concepts in immunotherapy of cancer: introduction. In Vivo. 1991;5(6):551–2. PubMed PMID: 1810436.PubMedGoogle Scholar
  79. 79.
    Theoret MR, Cohen CJ, Nahvi AV, Ngo LT, Suri KB, Powell Jr DJ, et al. Relationship of p53 overexpression on cancers and recognition by anti-p53 T cell receptor-transduced T cells. Hum Gene Ther. 2008;19(11):1219–32. PubMed PMID: 19848582. Epub 2009/10/24.PubMedCentralPubMedCrossRefGoogle Scholar
  80. 80.
    Riley JL, June CH, Blazar BR. Human T regulatory cell therapy: take a billion or so and call me in the morning. Immunity. 2009;30(5):656–65. PubMed PMID: 19464988. Epub 2009/05/26.PubMedCentralPubMedCrossRefGoogle Scholar
  81. 81.
    Parkhurst MR, Joo J, Riley JP, Yu Z, Li Y, Robbins PF, et al. Characterization of genetically modified T-cell receptors that recognize the CEA:691–699 peptide in the context of HLA-A2.1 on human colorectal cancer cells. Clin Cancer Res. 2009;15(1):169–80.PubMedCentralPubMedCrossRefGoogle Scholar
  82. 82.
    Robbins PF, Li YF, El-Gamil M, Zhao Y, Wargo JA, Zheng Z, et al. Single and dual amino acid substitutions in TCR CDRs can enhance antigen-specific T cell functions. J Immunol. 2008;180(9):6116–31. PubMed PMID: 18424733. Epub 2008/04/22.PubMedCentralPubMedGoogle Scholar
  83. 83.
    June CH, Blazar BR, Riley JL. Engineering lymphocyte subsets: tools, trials and tribulations. Nat Rev Immunol. 2009;9(10):704–16. PubMed PMID: 19859065. Epub 2009/10/28.PubMedCentralPubMedCrossRefGoogle Scholar
  84. 84.
    Wang G, Chopra RK, Royal RE, Yang JC, Rosenberg SA, Hwu P. A T cell-independent antitumor response in mice with bone marrow cells retrovirally transduced with an antibody/Fc-gamma chain chimeric receptor gene recognizing a human ovarian cancer antigen. Nat Med. 1998;4(2):168–72. PubMed PMID: 9461189.PubMedCrossRefGoogle Scholar
  85. 85.
    Parker LL, Do MT, Westwood JA, Wunderlich JR, Dudley ME, Rosenberg SA, et al. Expansion and characterization of T cells transduced with a chimeric receptor against ovarian cancer. Hum Gene Ther. 2000;11(17):2377–87. PubMed PMID: 11096442.PubMedCrossRefGoogle Scholar
  86. 86.
    Wilkie S, Picco G, Foster J, Davies DM, Julien S, Cooper L, et al. Retargeting of human T cells to tumor-associated MUC1: the evolution of a chimeric antigen receptor. J Immunol. 2008;180(7):4901–9. PubMed PMID: 18354214. Epub 2008/03/21.PubMedGoogle Scholar
  87. 87.
    Carpenito C, Milone MC, Hassan R, Simonet JC, Lakhal M, Suhoski MM, et al. Control of large, established tumor xenografts with genetically retargeted human T cells containing CD28 and CD137 domains. Proc Natl Acad Sci U S A. 2009;106(9):3360–5. PubMed PMID: 19211796. Pubmed Central PMCID: 2651342. Epub 2009/02/13.PubMedCentralPubMedCrossRefGoogle Scholar
  88. 88.
    Kershaw MH, Westwood JA, Parker LL, Wang G, Eshhar Z, Mavroukakis SA, et al. A phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer. Clin Cancer Res. 2006;12(20 Pt 1):6106–15. PubMed PMID: 17062687.PubMedCentralPubMedCrossRefGoogle Scholar
  89. 89.
    Song DG, Ye Q, Carpenito C, Poussin M, Wang LP, Ji C, et al. In vivo persistence, tumor localization, and antitumor activity of CAR-engineered T cells is enhanced by costimulatory signaling through CD137 (4-1BB). Cancer Res. 2011;71(13):4617–27. PubMed PMID: 21546571. Epub 2011/05/07.PubMedCrossRefGoogle Scholar
  90. 90.
    Berd D, Mastrangelo MJ. Active immunotherapy of human melanoma exploiting the immunopotentiating effects of cyclophosphamide. Cancer Invest. 1988;6(3):337–49. PubMed PMID: 3167614. Epub 1988/01/01.PubMedCrossRefGoogle Scholar
  91. 91.
    Radojcic V, Bezak KB, Skarica M, Pletneva MA, Yoshimura K, Schulick RD, et al. Cyclophosphamide resets dendritic cell homeostasis and enhances antitumor immunity through effects that extend beyond regulatory T cell elimination. Cancer Immunol Immunother. 2009. PubMed PMID: 19590872. Epub 2009/07/11.Google Scholar
  92. 92.
    Shurin GV, Tourkova IL, Kaneno R, Shurin MR. Chemotherapeutic agents in noncytotoxic concentrations increase antigen presentation by dendritic cells via an IL-12-dependent mechanism. J Immunol. 2009;183(1):137–44. PubMed PMID: 19535620. Epub 2009/06/19.PubMedCrossRefGoogle Scholar
  93. 93.
    Ghiringhelli F, Menard C, Puig PE, Ladoire S, Roux S, Martin F, et al. Metronomic cyclophosphamide regimen selectively depletes CD4+CD25+ regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol Immunother. 2007;56(5):641–8. PubMed PMID: 16960692. Epub 2006/09/09.PubMedCrossRefGoogle Scholar
  94. 94.
    Schiavoni G, Mattei F, Di Pucchio T, Santini SM, Bracci L, Belardelli F, et al. Cyclophosphamide induces type I interferon and augments the number of CD44(hi) T lymphocytes in mice: implications for strategies of chemoimmunotherapy of cancer. Blood. 2000;95(6):2024–30. PubMed PMID: 10706870.PubMedGoogle Scholar
  95. 95.
    Zhang L, Dermawan K, Jin M, Liu R, Zheng H, Xu L, et al. Differential impairment of regulatory T cells rather than effector T cells by paclitaxel-based chemotherapy. Clin Immunol. 2008;129(2):219–29. PubMed PMID: 18771959. Epub 2008/09/06.PubMedCrossRefGoogle Scholar
  96. 96.
    Nehme A, Julia AM, Jozan S, Chevreau C, Bugat R, Canal P. Modulation of cisplatin cytotoxicity by human recombinant interferon-gamma in human ovarian cancer cell lines. Eur J Cancer. 1994;30A(4):520–5. PubMed PMID: 8018412. Epub 1994/01/01.PubMedCrossRefGoogle Scholar
  97. 97.
    Melichar B, Hu W, Patenia R, Melicharova K, Gallardo ST, Freedman R. rIFN-gamma-mediated growth suppression of platinum-sensitive and -resistant ovarian tumor cell lines not dependent upon arginase inhibition. J Transl Med. 2003;1(1):5. PubMed PMID: 14572312.PubMedCentralPubMedCrossRefGoogle Scholar
  98. 98.
    Wall L, Burke F, Smyth JF, Balkwill F. The anti-proliferative activity of interferon-gamma on ovarian cancer: in vitro and in vivo. Gynecol Oncol. 2003;88(1 Pt 2):S149–51. PubMed PMID: 12586108.PubMedCrossRefGoogle Scholar
  99. 99.
    Freedman RS, Kudelka AP, Kavanagh JJ, Verschraegen C, Edwards CL, Nash M, et al. Clinical and biological effects of intraperitoneal injections of recombinant interferon-gamma and recombinant interleukin 2 with or without tumor-infiltrating lymphocytes in patients with ovarian or peritoneal carcinoma. Clin Cancer Res. 2000;6(6):2268–78. PubMed PMID: 10873077.PubMedGoogle Scholar
  100. 100.
    Kooi S, Zhang HZ, Patenia R, Edwards CL, Platsoucas CD, Freedman RS. HLA class I expression on human ovarian carcinoma cells correlates with T-cell infiltration in vivo and T-cell expansion in vitro in low concentrations of recombinant interleukin-2. Cell Immunol. 1996;174(2):116–28. PubMed PMID: 8954611.PubMedCrossRefGoogle Scholar
  101. 101.
    Duda DG, Sunamura M, Lozonschi L, Kodama T, Egawa S, Matsumoto G, et al. Direct in vitro evidence and in vivo analysis of the antiangiogenesis effects of interleukin 12. Cancer Res. 2000;60(4):1111–6. PubMed PMID: 10706132. Epub 2000/03/08.PubMedGoogle Scholar
  102. 102.
    Ohta M, Mitomi T, Kimura M, Habu S, Katsuki M. Anomalies in transgenic mice carrying the human interleukin-2 gene. Tokai J Exp Clin Med. 1990;15(4):307–15. PubMed PMID: 2130538.PubMedGoogle Scholar
  103. 103.
    Capitini CM, Chisti AA, Mackall CL. Modulating T-cell homeostasis with IL-7: preclinical and clinical studies. J Intern Med. 2009;266(2):141–53. PubMed PMID: 19623690. Epub 2009/07/23.PubMedCentralPubMedCrossRefGoogle Scholar
  104. 104.
    Ribas A. Update on immunotherapy for melanoma. J Natl Compr Canc Netw. 2006;4(7):687–94. PubMed PMID: 16884670. Epub 2006/08/04.PubMedGoogle Scholar
  105. 105.
    Andersson A, Yang SC, Huang M, Zhu L, Kar UK, Batra RK, et al. IL-7 promotes CXCR3 ligand-dependent T cell antitumor reactivity in lung cancer. J Immunol. 2009;182(11):6951–8. PubMed PMID: 19454692. Epub 2009/05/21.PubMedCrossRefGoogle Scholar
  106. 106.
    Sharma S, Wang J, Huang M, Paul RW, Lee P, McBride WH, et al. Interleukin-7 gene transfer in non-small-cell lung cancer decreases tumor proliferation, modifies cell surface molecule expression, and enhances antitumor reactivity. Cancer Gene Ther. 1996;3(5):302–13. PubMed PMID: 8894249. Epub 1996/09/01.PubMedGoogle Scholar
  107. 107.
    Shanmugham LN, Petrarca C, Frydas S, Donelan J, Castellani ML, Boucher W, et al. IL-15 an immunoregulatory and anti-cancer cytokine. Recent advances. J Exp Clin Cancer Res. 2006;25(4):529–36. PubMed PMID: 17310844. Epub 2007/02/22.PubMedGoogle Scholar
  108. 108.
    Brandt K, Singh PB, Bulfone-Paus S, Ruckert R. Interleukin-21: a new modulator of immunity, infection, and cancer. Cytokine Growth Factor Rev. 2007;18(3–4):223–32. PubMed PMID: 17509926. Epub 2007/05/19.PubMedCrossRefGoogle Scholar
  109. 109.
    Thompson JA, Curti BD, Redman BG, Bhatia S, Weber JS, Agarwala SS, et al. Phase I study of recombinant interleukin-21 in patients with metastatic melanoma and renal cell carcinoma. J Clin Oncol. 2008;26(12):2034–9. PubMed PMID: 18347008. Epub 2008/03/19.PubMedCrossRefGoogle Scholar
  110. 110.
    Carroll RG, Carpenito C, Shan X, Danet-Desnoyers G, Liu R, Jiang S, et al. Distinct effects of IL-18 on the engraftment and function of human effector CD8 T cells and regulatory T cells. PLoS One. 2008;3(9):e3289. PubMed PMID: 18818761. Pubmed Central PMCID: 2538560. Epub 2008/09/27.PubMedCentralPubMedCrossRefGoogle Scholar
  111. 111.
    Robertson MJ, Mier JW, Logan T, Atkins M, Koon H, Koch KM, et al. Clinical and biological effects of recombinant human interleukin-18 administered by intravenous infusion to patients with advanced cancer. Clin Cancer Res. 2006;12(14 Pt 1):4265–73. PubMed PMID: 16857801.PubMedCrossRefGoogle Scholar
  112. 112.
    Robertson MJ, Kirkwood JM, Logan TF, Koch KM, Kathman S, Kirby LC, et al. A dose-escalation study of recombinant human interleukin-18 using two different schedules of administration in patients with cancer. Clin Cancer Res. 2008;14(11):3462–9. PubMed PMID: 18519778.PubMedCrossRefGoogle Scholar
  113. 113.
    Peng G, Guo Z, Kiniwa Y, Voo KS, Peng W, Fu T, et al. Toll-like receptor 8-mediated reversal of CD4+ regulatory T cell function. Science. 2005;309(5739):1380–4. PubMed PMID: 16123302.PubMedCrossRefGoogle Scholar
  114. 114.
    Crellin NK, Garcia RV, Hadisfar O, Allan SE, Steiner TS, Levings MK. Human CD4+ T cells express TLR5 and its ligand flagellin enhances the suppressive capacity and expression of FOXP3 in CD4+CD25+ T regulatory cells. J Immunol. 2005;175(12):8051–9. PubMed PMID: 16339542. Epub 2005/12/13.PubMedGoogle Scholar
  115. 115.
    Tabiasco J, Devevre E, Rufer N, Salaun B, Cerottini JC, Speiser D, et al. Human effector CD8+ T lymphocytes express TLR3 as a functional coreceptor. J Immunol. 2006;177(12):8708–13. PubMed PMID: 17142772. Epub 2006/12/05.PubMedGoogle Scholar
  116. 116.
    Manegold C, Gravenor D, Woytowitz D, Mezger J, Hirsh V, Albert G, et al. Randomized phase II trial of a toll-like receptor 9 agonist oligodeoxynucleotide, PF-3512676, in combination with first-line taxane plus platinum chemotherapy for advanced-stage non-small-cell lung cancer. J Clin Oncol. 2008;26(24):3979–86. PubMed PMID: 18711188. Epub 2008/08/20.PubMedCrossRefGoogle Scholar
  117. 117.
    Link BK, Ballas ZK, Weisdorf D, Wooldridge JE, Bossler AD, Shannon M, et al. Oligodeoxynucleotide CpG 7909 delivered as intravenous infusion demonstrates immunologic modulation in patients with previously treated non-Hodgkin lymphoma. J Immunother. 2006;29(5):558–68. PubMed PMID: 16971811. Epub 2006/09/15.PubMedCrossRefGoogle Scholar
  118. 118.
    Leonard JP, Link BK, Emmanouilides C, Gregory SA, Weisdorf D, Andrey J, et al. Phase I trial of toll-like receptor 9 agonist PF-3512676 with and following rituximab in patients with recurrent indolent and aggressive non Hodgkin’s lymphoma. Clin Cancer Res. 2007;13(20):6168–74. PubMed PMID: 17947483. Epub 2007/10/20.PubMedCrossRefGoogle Scholar
  119. 119.
    Carpentier A, Laigle-Donadey F, Zohar S, Capelle L, Behin A, Tibi A, et al. Phase 1 trial of a CpG oligodeoxynucleotide for patients with recurrent glioblastoma. Neuro Oncol. 2006;8(1):60–6. PubMed PMID: 16443949. Epub 2006/01/31.PubMedCentralPubMedCrossRefGoogle Scholar
  120. 120.
    Stockfleth E, Trefzer U, Garcia-Bartels C, Wegner T, Schmook T, Sterry W. The use of toll-like receptor-7 agonist in the treatment of basal cell carcinoma: an overview. Br J Dermatol. 2003;149 Suppl 66:53–6. PubMed PMID: 14616352. Epub 2003/11/18.PubMedCrossRefGoogle Scholar
  121. 121.
    Adams S, O’Neill DW, Nonaka D, Hardin E, Chiriboga L, Siu K, et al. Immunization of malignant melanoma patients with full-length NY-ESO-1 protein using TLR7 agonist imiquimod as vaccine adjuvant. J Immunol. 2008;181(1):776–84. PubMed PMID: 18566444. Epub 2008/06/21.PubMedCentralPubMedGoogle Scholar
  122. 122.
    Koido S, Hara E, Homma S, Torii A, Toyama Y, Kawahara H, et al. Dendritic cells fused with allogeneic colorectal cancer cell line present multiple colorectal cancer-specific antigens and induce antitumor immunity against autologous tumor cells. Clin Cancer Res. 2005;11(21):7891–900. PubMed PMID: 16278414. Epub 2005/11/10.PubMedCrossRefGoogle Scholar
  123. 123.
    den Brok MH, Sutmuller RP, Nierkens S, Bennink EJ, Toonen LW, Figdor CG, et al. Synergy between in situ cryoablation and TLR9 stimulation results in a highly effective in vivo dendritic cell vaccine. Cancer Res. 2006;66(14):7285–92. PubMed PMID: 16849578. Epub 2006/07/20.CrossRefGoogle Scholar
  124. 124.
    Lesimple T, Neidhard EM, Vignard V, Lefeuvre C, Adamski H, Labarriere N, et al. Immunologic and clinical effects of injecting mature peptide-loaded dendritic cells by intralymphatic and intranodal routes in metastatic melanoma patients. Clin Cancer Res. 2006;12(24):7380–8. PubMed PMID: 17189411. Epub 2006/12/26.PubMedCrossRefGoogle Scholar
  125. 125.
    Hamdy S, Molavi O, Ma Z, Haddadi A, Alshamsan A, Gobti Z, et al. Co-delivery of cancer-associated antigen and toll-like receptor 4 ligand in PLGA nanoparticles induces potent CD8+ T cell-mediated anti-tumor immunity. Vaccine. 2008;26(39):5046–57. PubMed PMID: 18680779. Epub 2008/08/06.PubMedCrossRefGoogle Scholar
  126. 126.
    Ramakrishna V, Vasilakos JP, Tario Jr JD, Berger MA, Wallace PK, Keler T. Toll-like receptor activation enhances cell-mediated immunity induced by an antibody vaccine targeting human dendritic cells. J Transl Med. 2007;5:5. PubMed PMID: 17254349. Epub 2007/01/27.PubMedCentralPubMedCrossRefGoogle Scholar
  127. 127.
    Fong L, Small EJ. Anti-cytotoxic T-lymphocyte antigen-4 antibody: the first in an emerging class of immunomodulatory antibodies for cancer treatment. J Clin Oncol. 2008;26(32):5275–83. PubMed PMID: 18838703. Epub 2008/10/08.PubMedCrossRefGoogle Scholar
  128. 128.
    Curiel TJ, Wei S, Dong H, Alvarez X, Cheng P, Mottram P, et al. Blockade of B7-H1 improves myeloid dendritic cell-mediated antitumor immunity. Nat Med. 2003;9(5):562–7. PubMed PMID: 12704383.PubMedCrossRefGoogle Scholar
  129. 129.
    Liu SM, Meng Q, Zhang QX, Wang SD, Liu ZJ, Zhang XF. Expression and significance of B7-H1 and its receptor PD-1 in human gastric carcinoma. Zhonghua Zhong Liu Za Zhi. 2008;30(3):192–5. PubMed PMID: 18756934. Epub 2008/09/02. chi.PubMedGoogle Scholar
  130. 130.
    Hirano F, Kaneko K, Tamura H, Dong H, Wang S, Ichikawa M, et al. Blockade of B7-H1 and PD-1 by monoclonal antibodies potentiates cancer therapeutic immunity. Cancer Res. 2005;65(3):1089–96. PubMed PMID: 15705911.PubMedGoogle Scholar
  131. 131.
    Blank C, Mackensen A. Contribution of the PD-L1/PD-1 pathway to T-cell exhaustion: an update on implications for chronic infections and tumor evasion. Cancer Immunol Immunother. 2007;56(5):739–45. PubMed PMID: 17195077. Epub 2006/12/30.PubMedCrossRefGoogle Scholar
  132. 132.
    Berger R, Rotem-Yehudar R, Slama G, Landes S, Kneller A, Leiba M, et al. Phase I safety and pharmacokinetic study of CT-011, a humanized antibody interacting with PD-1, in patients with advanced hematologic malignancies. Clin Cancer Res. 2008;14(10):3044–51. PubMed PMID: 18483370. Epub 2008/05/17.PubMedCrossRefGoogle Scholar
  133. 133.
    Benencia F, Coukos G. T regulatory cell depletion can boost DC-based vaccines. Cancer Biol Ther. 2005;28:4(6). PubMed PMID: 15917649.Google Scholar
  134. 134.
    Prasad SJ, Farrand KJ, Matthews SA, Chang JH, McHugh RS, Ronchese F. Dendritic cells loaded with stressed tumor cells elicit long-lasting protective tumor immunity in mice depleted of CD4+CD25+ regulatory T cells. J Immunol. 2005;174(1):90–8. PubMed PMID: 15611231.PubMedGoogle Scholar
  135. 135.
    Waldmann TA. Daclizumab (anti-Tac, Zenapax) in the treatment of leukemia/lymphoma. Oncogene. 2007;26(25):3699–703. PubMed PMID: 17530023. Epub 2007/05/29.PubMedCrossRefGoogle Scholar
  136. 136.
    Kreijveld E, Koenen HJ, Klasen IS, Hilbrands LB, Joosten I. Following anti-CD25 treatment, a functional CD4+CD25+ regulatory T-cell pool is present in renal transplant recipients. Am J Transplant. 2007;7(1):249–55. PubMed PMID: 17109733. Epub 2006/11/18.PubMedCrossRefGoogle Scholar
  137. 137.
    Nussenblatt RB, Fortin E, Schiffman R, Rizzo L, Smith J, Van Veldhuisen P, et al. Treatment of noninfectious intermediate and posterior uveitis with the humanized anti-Tac mAb: a phase I/II clinical trial. Proc Natl Acad Sci U S A. 1999;96(13):7462–6. PubMed PMID: 10377437. Epub 1999/06/23.PubMedCentralPubMedCrossRefGoogle Scholar
  138. 138.
    Przepiorka D, Kernan NA, Ippoliti C, Papadopoulos EB, Giralt S, Khouri I, et al. Daclizumab, a humanized anti-interleukin-2 receptor alpha chain antibody, for treatment of acute graft-versus-host disease. Blood. 2000;95(1):83–9. PubMed PMID: 10607689. Epub 1999/12/23.PubMedGoogle Scholar
  139. 139.
    Lehky TJ, Levin MC, Kubota R, Bamford RN, Flerlage AN, Soldan SS, et al. Reduction in HTLV-I proviral load and spontaneous lymphoproliferation in HTLV-I-associated myelopathy/tropical spastic paraparesis patients treated with humanized anti-Tac. Ann Neurol. 1998;44(6):942–7. PubMed PMID: 9851439. Epub 1998/12/16.PubMedCrossRefGoogle Scholar
  140. 140.
    Vincenti F, Nashan B, Light S. Daclizumab: outcome of phase III trials and mechanism of action. Double Therapy and the Triple Therapy Study Groups. Transplant Proc. 1998;30(5):2155–8. PubMed PMID: 9723424. Epub 1998/09/02.PubMedCrossRefGoogle Scholar
  141. 141.
    Rech AJ, Vonderheide RH. Clinical use of anti-CD25 antibody daclizumab to enhance immune responses to tumor antigen vaccination by targeting regulatory T cells. Ann N Y Acad Sci. 2009;1174:99–106. PubMed PMID: 19769742. Epub 2009/09/23.PubMedCrossRefGoogle Scholar
  142. 142.
    Chiang CL, Ledermann JA, Egla A, Elizabeth B, Katz DR, Chain BM. Oxidation of ovarian epithelial cancer cells by hypochlorous acid enhances immunogenicity and stimulates T cells that recognize autologous primary tumor. Clin Cancer Res. 2008;14(15):10.Google Scholar
  143. 143.
    Melichar B, Patenia R, Gallardo S, Melicharova K, Hu W, Freedman RS. Expression of CD40 and growth-inhibitory activity of CD40 ligand in ovarian cancer cell lines. Gynecol Oncol. 2007;104(3):707–13. PubMed PMID: 17166566. Epub 2006/12/15.PubMedCrossRefGoogle Scholar
  144. 144.
    Hakkarainen T, Hemminki A, Pereboev AV, Barker SD, Asiedu CK, Strong TV, et al. CD40 is expressed on ovarian cancer cells and can be utilized for targeting adenoviruses. Clin Cancer Res. 2003;9(2):619–24. PubMed PMID: 12576427. Epub 2003/02/11.PubMedGoogle Scholar
  145. 145.
    Gallagher NJ, Eliopoulos AG, Agathangelo A, Oates J, Crocker J, Young LS. CD40 activation in epithelial ovarian carcinoma cells modulates growth, apoptosis, and cytokine secretion. Mol Pathol. 2002;55(2):110–20. PubMed PMID: 11950960. Pubmed Central PMCID: 1187159. Epub 2002/04/16.PubMedCentralPubMedCrossRefGoogle Scholar
  146. 146.
    Ciaravino G, Bhat M, Manbeian CA, Teng NN. Differential expression of CD40 and CD95 in ovarian carcinoma. Eur J Gynaecol Oncol. 2004;25(1):27–32. PubMed PMID: 15053058. Epub 2004/04/01.PubMedGoogle Scholar
  147. 147.
    Toutirais O, Gervais A, Cabillic F, Le Gallo M, Coudrais A, Leveque J, et al. Effects of CD40 binding on ovarian carcinoma cell growth and cytokine production in vitro. Clin Exp Immunol. 2007;149(2):372–7. PubMed PMID: 17565609. Pubmed Central PMCID: 1941941. Epub 2007/06/15.PubMedCentralPubMedCrossRefGoogle Scholar
  148. 148.
    Ghamande S, Hylander BL, Oflazoglu E, Lele S, Fanslow W, Repasky EA. Recombinant CD40 ligand therapy has significant antitumor effects on CD40-positive ovarian tumor xenografts grown in SCID mice and demonstrates an augmented effect with cisplatin. Cancer Res. 2001;61(20):7556–62. PubMed PMID: 11606394. Epub 2001/10/19.PubMedGoogle Scholar
  149. 149.
    Schwartz RN, Stover L, Dutcher J. Managing toxicities of high-dose interleukin-2. Oncology (Williston Park). 2002;16(11 Suppl 13):11–20. PubMed PMID: 12469935. Epub 2002/12/10.Google Scholar
  150. 150.
    Brandenburg S, Takahashi T, de la Rosa M, Janke M, Karsten G, Muzzulini T, et al. IL-2 induces in vivo suppression by CD4(+)CD25(+)Foxp3(+) regulatory T cells. Eur J Immunol. 2008;38(6):1643–53. PubMed PMID: 18493984. Epub 2008/05/22.PubMedCrossRefGoogle Scholar
  151. 151.
    Allan NC, Richards SM, Shepherd PC. UK Medical Research Council randomised, multicentre trial of interferon-alpha n1 for chronic myeloid leukaemia: improved survival irrespective of cytogenetic response. The UK Medical Research Council’s Working Parties for Therapeutic Trials in Adult Leukaemia. Lancet. 1995;345(8962):1392–7. PubMed PMID: 7760609. Epub 1995/06/03.PubMedCrossRefGoogle Scholar
  152. 152.
    Anger B, Porzsolt F, Leichtle R, Heinze B, Bartram C, Heimpel H. A phase I/II study of recombinant interferon alpha 2a and hydroxyurea for chronic myelocytic leukemia. Blut. 1989;58(6):275–8. PubMed PMID: 2736308. Epub 1989/06/01.PubMedCrossRefGoogle Scholar
  153. 153.
    Foon KA, Roth MS, Bunn Jr PA. Alpha interferon treatment of low-grade B-cell non-Hodgkin’s lymphomas, cutaneous T-cell lymphomas, and chronic lymphocytic leukemia. Semin Oncol. 1986;13(3 Suppl 2):35–42. PubMed PMID: 3532334. Epub 1986/09/01.Google Scholar
  154. 154.
    Hersey P, Hasic E, MacDonald M, Edwards A, Spurling A, Coates AS, et al. Effects of recombinant leukocyte interferon (rIFN-alpha A) on tumour growth and immune responses in patients with metastatic melanoma. Br J Cancer. 1985;51(6):815–26. PubMed PMID: 3873953. Epub 1985/06/01.PubMedCentralPubMedCrossRefGoogle Scholar
  155. 155.
    Creagan ET, Ahmann DL, Green SJ, Long HJ, Frytak S, O’Fallon JR, et al. Phase II study of low-dose recombinant leukocyte A interferon in disseminated malignant melanoma. J Clin Oncol. 1984;2(9):1002–5. PubMed PMID: 6470751. Epub 1984/09/01.PubMedGoogle Scholar
  156. 156.
    Creagan ET, Ahmann DL, Green SJ, Long HJ, Rubin J, Schutt AJ, et al. Phase II study of recombinant leukocyte A interferon (rIFN-alpha A) in disseminated malignant melanoma. Cancer. 1984;54(12):2844–9. PubMed PMID: 6498762. Epub 1984/12/15.PubMedCrossRefGoogle Scholar
  157. 157.
    Kirkwood JM, Ernstoff M. Melanoma: therapeutic options with recombinant interferons. Semin Oncol. 1985;12(4 Suppl 5):7–12. PubMed PMID: 2417333. Epub 1985/12/01.PubMedGoogle Scholar
  158. 158.
    Kirkwood JM, Ernstoff MS, Davis CA, Reiss M, Ferraresi R, Rudnick SA. Comparison of intramuscular and intravenous recombinant alpha-2 interferon in melanoma and other cancers. Ann Intern Med. 1985;103(1):32–6. PubMed PMID: 4003987. Epub 1985/07/01.PubMedCrossRefGoogle Scholar
  159. 159.
    Quesada JR, Swanson DA, Gutterman JU. Phase II study of interferon alpha in metastatic renal-cell carcinoma: a progress report. J Clin Oncol. 1985;3(8):1086–92. PubMed PMID: 4020410. Epub 1985/08/01.PubMedGoogle Scholar
  160. 160.
    Levens W, Rubben H, Ingenhag W. Long-term interferon treatment in metastatic renal cell carcinoma. Eur Urol. 1989;16(5):378–81. PubMed PMID: 2776808. Epub 1989/01/01.PubMedGoogle Scholar
  161. 161.
    Rinehart JJ, Young D, Laforge J, Colborn D, Neidhart JA. Phase I/II trial of interferon-beta-serine in patients with renal cell carcinoma: immunological and biological effects. Cancer Res. 1987;47(9):2481–5. PubMed PMID: 3567933. Epub 1987/05/01.PubMedGoogle Scholar
  162. 162.
    Berek JS, Markman M, Stonebraker B, Lentz SS, Adelson MD, DeGeest K, et al. Intraperitoneal interferon-alpha in residual ovarian carcinoma: a phase II gynecologic oncology group study. Gynecol Oncol. 1999;75(1):10–4. PubMed PMID: 10502418.PubMedCrossRefGoogle Scholar
  163. 163.
    Berek JS, Welander C, Schink JC, Grossberg H, Montz FJ, Zigelboim J. A phase I-II trial of intraperitoneal cisplatin and alpha-interferon in patients with persistent epithelial ovarian cancer. Gynecol Oncol. 1991;40(3):237–43. PubMed PMID: 2013446.PubMedCrossRefGoogle Scholar
  164. 164.
    Markman M, Belinson J, Webster K, Zanotti K, Morrison B, Jacobs B, et al. Phase 2 trial of interferon-beta as second-line treatment of ovarian cancer, fallopian tube cancer, or primary carcinoma of the peritoneum. Oncology. 2004;66(5):343–6. PubMed PMID: 15331919.PubMedCrossRefGoogle Scholar
  165. 165.
    Hall GD, Brown JM, Coleman RE, Stead M, Metcalf KS, Peel KR, et al. Maintenance treatment with interferon for advanced ovarian cancer: results of the Northern and Yorkshire gynaecology group randomised phase III study. Br J Cancer. 2004;91(4):621–6. PubMed PMID: 15305182. Pubmed Central PMCID: 2364769.PubMedCentralPubMedCrossRefGoogle Scholar
  166. 166.
    Windbichler GH, Hausmaninger H, Stummvoll W, Graf AH, Kainz C, Lahodny J, et al. Interferon-gamma in the first-line therapy of ovarian cancer: a randomized phase III trial. Br J Cancer. 2000;82(6):1138–44. PubMed PMID: 10735496.PubMedCentralPubMedCrossRefGoogle Scholar
  167. 167.
    Alberts DS, Marth C, Alvarez RD, Johnson G, Bidzinski M, Kardatzke DR, et al. Randomized phase 3 trial of interferon gamma-1b plus standard carboplatin/paclitaxel versus carboplatin/paclitaxel alone for first-line treatment of advanced ovarian and primary peritoneal carcinomas: results from a prospectively designed analysis of progression-free survival. Gynecol Oncol. 2008;109(2):174–81. PubMed PMID: 18314182. Epub 2008/03/04.PubMedCrossRefGoogle Scholar
  168. 168.
    Vakkila J, Lotze MT. Inflammation and necrosis promote tumour growth. Nat Rev Immunol. 2004;4(8):641–8. PubMed PMID: 15286730.PubMedCrossRefGoogle Scholar
  169. 169.
    Kelly MG, Alvero AB, Chen R, Silasi DA, Abrahams VM, Chan S, et al. TLR-4 signaling promotes tumor growth and paclitaxel chemoresistance in ovarian cancer. Cancer Res. 2006;66(7):3859–68. PubMed PMID: 16585214. Epub 2006/04/06.PubMedCrossRefGoogle Scholar
  170. 170.
    Kim KH, Xie Y, Tytler EM, Woessner R, Mor G, Alvero AB. KSP inhibitor ARRY-520 as a substitute for paclitaxel in type I ovarian cancer cells. J Transl Med. 2009;7:63. PubMed PMID: 19619321. Epub 2009/07/22.PubMedCentralPubMedCrossRefGoogle Scholar
  171. 171.
    Elgueta R, Benson MJ, de Vries VC, Wasiuk A, Guo Y, Noelle RJ. Molecular mechanism and function of CD40/CD40L engagement in the immune system. Immunol Rev. 2009;229(1):152–72. PubMed PMID: 19426221. Epub 2009/05/12.PubMedCrossRefGoogle Scholar
  172. 172.
    Scarlett UK, Cubillos-Ruiz JR, Nesbeth YC, Martinez DG, Engle X, Gewirtz AT, et al. In situ stimulation of CD40 and toll-like receptor 3 transforms ovarian cancer-infiltrating dendritic cells from immunosuppressive to immunostimulatory cells. Cancer Res. 2009;69(18):7329–37. PubMed PMID: 19738057. Pubmed Central PMCID: 2754806. Epub 2009/09/10.PubMedCentralPubMedCrossRefGoogle Scholar
  173. 173.
    Kedl RM, Jordan M, Potter T, Kappler J, Marrack P, Dow S. CD40 stimulation accelerates deletion of tumor-specific CD8(+) T cells in the absence of tumor-antigen vaccination. Proc Natl Acad Sci U S A. 2001;98(19):10811–6. PubMed PMID: 11526222. Pubmed Central PMCID: 58556. Epub 2001/08/30.PubMedCentralPubMedCrossRefGoogle Scholar
  174. 174.
    Manning EA, Ullman JG, Leatherman JM, Asquith JM, Hansen TR, Armstrong TD, et al. A vascular endothelial growth factor receptor-2 inhibitor enhances antitumor immunity through an immune-based mechanism. Clin Cancer Res. 2007;13(13):3951–9. PubMed PMID: 17606729. Epub 2007/07/04.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag London 2014

Authors and Affiliations

  • Lana E. Kandalaft
    • 1
  • Klara Balint
    • 1
  • Jonathan S. Berek
    • 2
    • 3
  • George Coukos
    • 1
  1. 1.Department of Obstetrics and Gynecology, Ovarian Cancer Research CenterPerelman School of Medicine at the University of Pennsylvania, Smilow Center for Translational ResearchPhiladelphiaUSA
  2. 2.Department of Obstetrics and GynecologyStanford University School of MedicineStanfordUSA
  3. 3.Stanford Cancer Institute Obstetrics and GynecologyStanford Women’s Cancer CenterStanfordUSA

Personalised recommendations