Exploitation of differential homeostatic proliferation of T-cell subsets following chemotherapy to enhance the efficacy of vaccine-mediated antitumor responses

Cancer Immunology, Immunotherapy

Volumn 60, Issue 9, 2011, Pages 1227-1242

  Gameiro, Sofia R ^a   Caballero, Jorge A ^a   Higgins, Jack P ^a   Apelian, David ^b   Hodge, James W ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b GlobeImmune Inc   (United States)

Author keywords

Adjuvant chemotherapy; Cisplatin; Immunotherapy; Non small cell lung cancer; NSCLC; Vinorelbine

Indexed keywords

CANCER VACCINE; CARCINOEMBRYONIC ANTIGEN; CASPASE 3; CASPASE 7; CD40 ANTIGEN; CISPLATIN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; FAS ANTIGEN; FAS LIGAND; GENE PRODUCT; IMMUNOGLOBULIN; INTERLEUKIN 10; INTERLEUKIN 17; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NAIP1 PROTEIN; NAVELBINE; P21 ACTIVATED KINASE 7; PROTEIN LHX4; RECOMBINANT YEAST CARCINOEMBRYONIC ANTIGEN VACCINE; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; APOPTOSIS; ARTICLE; B LYMPHOCYTE; BASOPHIL; CANCER CELL CULTURE; CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CANCER SURVIVAL; CD3+ T LYMPHOCYTE; CD4+ CD25+ FOXP3+ T CELL; CD4+ T LYMPHOCYTE; CD40IG GENE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL SPECIFICITY; CELL SURFACE; CELLULAR IMMUNITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DOWN REGULATION; DRUG POTENTIATION; EOSINOPHIL COUNT; EXPERIMENTAL NEOPLASM; FEMALE; GENE; GENE EXPRESSION; IL 10 GENE; IN VITRO STUDY; IN VIVO STUDY; LEUKOPENIA; LEWIS CARCINOMA; LHX4 GENE; LUNG NON SMALL CELL CANCER; LYMPHOCYTE COUNT; LYMPHOCYTE DEPLETION; LYMPHOCYTE PROLIFERATION; MONOCYTE; MONOTHERAPY; MOUSE; NAIP1 GENE; NATURAL KILLER CELL; NEUTROPHIL COUNT; NONHUMAN; OVERALL SURVIVAL; PAK7 GENE; PANCYTOPENIA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SINGLE DRUG DOSE; SPLEEN CELL; SUB MYELOABLATIVE LEUKOPENIA; SURVIVAL TIME; T LYMPHOCYTE SUBPOPULATION; TNF GENE; TRAF1 GENE; TRANSGENIC MOUSE; TUMOR CELL DESTRUCTION; UPREGULATION;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CANCER VACCINES; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CHEMOTHERAPY, ADJUVANT; CISPLATIN; COMBINED MODALITY THERAPY; FEMALE; HUMANS; LUNG NEOPLASMS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SURVIVAL RATE; T-LYMPHOCYTE SUBSETS; VINBLASTINE;

EID: 80054701176     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-011-1020-8     Document Type: Article

References (68)

1. Parkin DM, Bray F, Ferlay J, Pisani P (2005) Global cancer statistics, 2002. CA Cancer J Clin 55:74-108 (Pubitemid 40372904)
2. Ferlay J, Autier P, Boniol M, Heanue M, Colombet M, Boyle P (2007) Estimates of the cancer incidence and mortality in Europe in 2006. Ann Oncol 18:581-592 (Pubitemid 46359643)
3. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ (2008) Cancer statistics, 2008. CA Cancer J Clin 58:71-96 (Pubitemid 351521864)
4. Winton T, Livingston R, Johnson D, Rigas J, Johnston M, Butts C, Cormier Y, Goss G, Inculet R, Vallieres E, Fry W, Bethune D, Ayoub J, Ding K, Seymour L, Graham B, Tsao MS, Gandara D, Kesler K, Demmy T, Shepherd F (2005) Vinorelbine plus cisplatin vs. observation in resected non-small-cell lung cancer. N Engl J Med 352:2589-2597 (Pubitemid 41007845)
5. Douillard JY, Rosell R, De Lena M, Carpagnano F, Ramlau R, Gonzales-Larriba JL, Grodzki T, Pereira JR, Le Groumellec A, Lorusso V, Clary C, Torres AJ, Dahabreh J, Souquet PJ, Astudillo J, Fournel P, Artal-Cortes A, Jassem J, Koubkova L, His P, Riggi M, Hurteloup P (2006) Adjuvant vinorelbine plus cisplatin versus observation in patients with completely resected stage IB-IIIA non-small-cell lung cancer (Adjuvant Navelbine International Trialist Association [ANITA]): a randomised controlled trial. Lancet Oncol 7:719-727 (Pubitemid 44283661)
6. Gridelli C, Rossi A, Maione P, Ferrara ML, Castaldo V, Sacco PC (2009) Vaccines for the treatment of non-small cell lung cancer: a renewed anticancer strategy. Oncologist 14:909-920
7. Reck M, von Pawel J, Zatloukal P, Ramlau R, Gorbounova V, Hirsh V, Leighl N, Mezger J, Archer V, Moore N, Manegold C (2009) Phase III trial of cisplatin plus gemcitabine with either placebo or bevacizumab as first-line therapy for nonsquamous non-small-cell lung cancer: AVAil. J Clin Oncol 27:1227-1234
8. Butts C, Murray N, Maksymiuk A, Goss G, Marshall E, Soulieres D, Cormier Y, Ellis P, Price A, Sawhney R, Davis M, Mansi J, Smith C, Vergidis D, Ellis P, MacNeil M, Palmer M (2005) Randomized phase IIB trial of BLP25 liposome vaccine in stage IIIB and IV non-small-cell lung cancer. J Clin Oncol 23:6674-6681 (Pubitemid 46190262)
9. Higano CS, Schellhammer PF, Small EJ, Burch PA, Nemunaitis J, Yuh L, Provost N, Frohlich MW (2009) Integrated data from 2 randomized, double-blind, placebo-controlled, phase 3 trials of active cellular immunotherapy with sipuleucel-T in advanced prostate cancer. Cancer 115:3670-3679
10. Spicer J, Chowdhury S, Harper P (2007) Targeting novel and established therapies for non-small cell lung cancer. Cancer Lett 250:9-16 (Pubitemid 46483839)
11. Schuster S, Neelapu S, Gause B, Muggia F, Gockerman J, Sotomayor E, Winter J, Flowers C, Stergiou A, Kwak L (2009) Idiotype vaccine therapy (BiovaxID) in follicular lymphoma in first complete remission: phase III clinical trial results. J Clin Oncol 27(18S):2
12. Wansley EK, Chakraborty M, Hance KW, Bernstein MB, Boehm AL, Guo Z, Quick D, Franzusoff A, Greiner JW, Schlom J, Hodge JW (2008) Vaccination with a recombinant Saccharomyces cerevisiae expressing a tumor antigen breaks immune tolerance and elicits therapeutic antitumor responses. Clin Cancer Res 14:4316-4325
13. Marshall JL, Hoyer RJ, Toomey MA, Faraguna K, Chang P, Richmond E, Pedicano JE, Gehan E, Peck RA, Arlen P, Tsang KY, Schlom J (2000) Phase I study in advanced cancer patients of a diversified prime-and-boost vaccination protocol using recombinant vaccinia virus and recombinant nonreplicating avipox virus to elicit anti-carcinoembryonic antigen immune responses. J Clin Oncol 18:3964-3973
14. Yang D, Stewart TJ, Smith KK, Georgi D, Abrams SI, LiuK (2008) Downregulation of IFN-gammaR in association with loss of Fas function is linked to tumor progression. Int J Cancer 122:350-362 (Pubitemid 350234721)
15. Wroblewski JM, Bixby DL, Borowski C, Yannelli JR (2001) Characterization of human non-small cell lung cancer (NSCLC) cell lines for expression of MHC, co-stimulatory molecules and tumor-associated antigens. Lung Cancer 33:181-194 (Pubitemid 32707899)
16. Remondo C, Cereda V, Mostbock S, Sabzevari H, Franzusoff A, Schlom J, Tsang KY (2009) Human dendritic cell maturation and activation by a heat-killed recombinant yeast (Saccharomyces cerevisiae) vector encoding carcinoembryonic antigen. Vaccine 27:987-994
17. Bernstein MB, Chakraborty M, Wansley EK, Guo Z, Franzusoff A, Mostbock S, Sabzevari H, Schlom J, Hodge JW (2008) Recombinant Saccharomyces cerevisiae (yeast-CEA) as a potent activator of murine dendritic cells. Vaccine 26:509-521
18. Everson G, Tong M, Jacobson I, Do D, Re R, Mi M, Fa F (2006) Interim results from a randomized, double-blind, placebo-controlled phase 1b study in subjects with chronic HCV after treatment with GI-5005, a yeast-based HCV immunotherapy targeting NS3 and core proteins [abstract]. Hepatology 44:697A
19. Whiting S, Cohn A, Morse M, O'Neil S, Bellgrau D, Duke R, Franzusoff A (2006) Treatment of Ras mutation-bearing solid tumor using whole recombinant S. cerevisiae yeast expressing mutated Ras: preliminary safety and immunogenicity results from a phase I trial (poster). ASCO Gastrointestinal Cancers Symposium, San Francisco, CA
20. Arriagada R, Bergman B, Dunant A, Le Chevalier T, Pignon JP, Vansteenkiste J (2004) Cisplatin-based adjuvant chemotherapy in patients with completely resected non-small-cell lung cancer. N Engl J Med 350:351-360 (Pubitemid 38101630)
21. Wozniak AJ, Crowley JJ, Balcerzak SP, Weiss GR, Spiridonidis CH, Baker LH, Albain KS, Kelly K, Taylor SA, Gandara DR, Livingston RB (1998) Randomized trial comparing cisplatin with cisplatin plus vinorelbine in the treatment of advanced non-smallcell lung cancer: a Southwest Oncology Group study. J Clin Oncol 16:2459-2465 (Pubitemid 28309041)
22. Shukuya T, Takahashi T, Tamiya A, Ono A, Igawa S, Tsuya A, Nakamura Y, Murakami H, Naito T, Kaira K, Endo M, Yamamoto N (2009) Evaluation of the safety and compliance of 3-week cycles of vinorelbine on days 1 and 8 and cisplatin on day 1 as adjuvant chemotherapy in Japanese patients with completely resected pathological stage IB to IIIA non-small cell lung cancer: a retrospective study. Jpn J Clin Oncol 39:158-162
23. Chustecka Z Cisplatin and Vinorelbine Standard of Care in Lung Cancer. In: WebMED (ed) Medscape Today. Medscape Medical News, 10/02/2006. Accessed 07 Aug 2010
24. Bretti S, Berruti A, Gorzegno G, La Ciura P, Paze E, Celano A, Grecchi G, Perroni D, Bumma C, Dogliotti L (1996) Multicenter Phase II trial of intermediate dose cisplatin and vinorelbine in inoperable non-small cell lung cancer patients. Lung Cancer 14:353-360 (Pubitemid 26191595)
25. Gebbia V, Galetta D, Lorusso V, Caruso M, Verderame F, Pezzella G, Borsellino N, Durini E, Valenza R, Agostara B, Colucci G (2008) Cisplatin plus weekly vinorelbine versus cisplatin plus vinorelbine on days 1 and 8 in advanced non-small cell lung cancer: a prospective randomized phase III trial of the G.O.I.M. (Gruppo Oncologico Italia Meridionale). Lung Cancer 61:369-377
26. Song CK, Han HD, Noh KH, Kang TH, Park YS, Kim JH, Park ES, Shin BC, Kim TW (2007) Chemotherapy enhances CD8(?) T cell-mediated antitumor immunity induced by vaccination with vaccinia virus. Mol Ther 15:1558-1563 (Pubitemid 47099313)
27. Tseng CW, Hung CF, Alvarez RD, Trimble C, Huh WK, Kim D, Chuang CM, Lin CT, Tsai YC, He L, Monie A, Wu TC (2008) Pretreatment with cisplatin enhances E7-specific CD8? T-Cellmediated antitumor immunity induced by DNA vaccination. Clin Cancer Res 14:3185-3192
28. Bae SH, Park YJ, Park JB, Choi YS, Kim MS, Sin JI (2007) Therapeutic synergy of human papillomavirus E7 subunit vaccines plus cisplatin in an animal tumor model: causal involvement of increased sensitivity of cisplatin-treated tumors to CTL-mediated killing in therapeutic synergy. Clin Cancer Res 13:341-349 (Pubitemid 46121888)
29. Merritt RE, Mahtabifard A, Yamada RE, Crystal RG, Korst RJ (2003) Cisplatin augments cytotoxic T-lymphocyte-mediated antitumor immunity in poorly immunogenic murine lung cancer. J Thorac Cardiovasc Surg 126:1609-1617 (Pubitemid 37449195)
30. Sundelin K, Roberg K, Grenman R, Hakansson L (2007) Effects of cisplatin, alpha-interferon, and 13-cis retinoic acid on the expression of Fas (CD95), intercellular adhesion molecule-1 (ICAM-1), and epidermal growth factor receptor (EGFR) in oral cancer cell lines. J Oral Pathol Med 36:177-183
31. Matsuzaki I, Suzuki H, Kitamura M, Minamiya Y, Kawai H, Ogawa J (2000) Cisplatin induces fas expression in esophageal cancer cell lines and enhanced cytotoxicity in combination with LAK cells. Oncology 59:336-343
32. Ngan VK, Bellman K, Hill BT, Wilson L, Jordan MA (2001) Mechanism of mitotic block and inhibition of cell proliferation by the semisynthetic Vinca alkaloids vinorelbine and its newer derivative vinflunine. Mol Pharmacol 60:225-232 (Pubitemid 32595250)
33. Clarke P, Mann J, Simpson JF, Rickard-Dickson K, Primus FJ (1998) Mice transgenic for human carcinoembryonic antigen as a model for immunotherapy. Cancer Res 58:1469-1477 (Pubitemid 28193610)
34. Robbins PF, Kantor JA, Salgaller M, Hand PH, Fernsten PD, Schlom J (1991) Transduction and expression of the human carcinoembryonic antigen gene in a murine colon carcinoma cell line. Cancer Res 51:3657-3662
35. Schmitz J, Reali E, Hodge JW, Patel A, Davis G, Schlom J, Greiner JW (2002) Identification of an interferon-gamma-inducible carcinoembryonic antigen (CEA) CD8(?) T-cell epitope, which mediates tumor killing in CEA transgenic mice. Cancer Res 62:5058-5064 (Pubitemid 34984434)
36. Nagai N, Ogata H, Wada Y, Tsujino D, Someya K, Ohno T, Masuhara K, Tanaka Y, Takahashi H, Nagai H, Kato K, Koshiba Y, Igarashi T, Yokoyama A, Kinameri K, Kato T, Kurita Y (1998) Population pharmacokinetics and pharmacodynamics of cisplatin in patients with cancer: analysis with the NONMEM program. J Clin Pharmacol 38:1025-1034 (Pubitemid 28524450)
37. Urien S, Lokiec F (2004) Population pharmacokinetics of total and unbound plasma cisplatin in adult patients. Br J Clin Pharmacol 57:756-763 (Pubitemid 38748043)
38. Garnett CT, Schlom J, Hodge JW (2008) Combination of docetaxel and recombinant vaccine enhances T-cell responses and antitumor activity: effects of docetaxel on immune enhancement. Clin Cancer Res 14:3536-3544
39. Kagi D, Vignaux F, Ledermann B, Burki K, Depraetere V, Nagata S, Hengartner H, Golstein P (1994) Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity. Science 265:528-530 (Pubitemid 24264998)
40. Kataoka T, Shinohara N, Takayama H, Takaku K, Kondo S, Yonehara S, Nagai K (1996) Concanamycin A, a powerful tool for characterization and estimation of contribution of perforinand Fas-based lytic pathways in cell-mediated cytotoxicity. J Immunol 156:3678-3686 (Pubitemid 26139940)
41. Abraham J, Gulley J, Allegra C (2005) Bethesda handbook of clinical oncology, 2nd edn. Lippincott Williams & Wilkins, Philadelphia
42. Leveque D, Jehl F (1996) Clinical pharmacokinetics of vinorelbine. Clin Pharmacokinet 31:184-197 (Pubitemid 26335905)
43. Ramlau R, Zatloukal P, Jassem J, Schwarzenberger P, Orlov SV, Gottfried M, Pereira JR, Temperley G, Negro-Vilar R, Rahal S, Zhang JK, Negro-Vilar A, Dziewanowska ZE (2008) Randomized phase III trial comparing bexarotene (L1069-49)/cisplatin/ vinorelbine with cisplatin/vinorelbine in chemotherapy-naïve patients with advanced or metastatic non-small-cell lung cancer: SPIRIT I. J Clin Oncol 26:1886-1892
44. Capitini CM, Chisti AA, Mackall CL (2009) Modulating T-cell homeostasis with IL-7: preclinical and clinical studies. J Intern Med 266:141-153
45. Williams KM, Hakim FT, Gress RE (2007) T cell immune reconstitution following lymphodepletion. Semin Immunol 19:318-330 (Pubitemid 350181530)
46. Hakim FT, Cepeda R, Kaimei S, Mackall CL, McAtee N, Zujewski J, Cowan K, Gress RE (1997) Constraints on CD4 recovery postchemotherapy in adults: thymic insufficiency and apoptotic decline of expanded peripheral CD4 cells. Blood 90:3789-3798 (Pubitemid 27473453)
47. von Mehren M, Arlen P, Gulley J, Rogatko A, Cooper HS, Meropol NJ, Alpaugh RK, Davey M, McLaughlin S, Beard MT, Tsang KY, Schlom J, Weiner LM (2001) The influence of granulocyte macrophage colony-stimulating factor and prior chemotherapy on the immunological response to a vaccine (ALVAC-CEA B7.1) in patients with metastatic carcinoma. Clin Cancer Res 7:1181-1191 (Pubitemid 32708668)
48. Zitvogel L, Apetoh L, Ghiringhelli F, Kroemer G (2008) Immunological aspects of cancer chemotherapy. Nat Rev Immunol 8:59-73
49. Casares N, Pequignot MO, Tesniere A, Ghiringhelli F, Roux S, Chaput N, Schmitt E, Hamai A, Hervas-Stubbs S, Obeid M, Coutant F, Metivier D, Pichard E, Aucouturier P, Pierron G, Garrido C, Zitvogel L, Kroemer G (2005) Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med 202:1691-1701 (Pubitemid 41815875)
50. Arlen PM, Pazdur M, Skarupa L, Rauckhorst M, Gulley JL (2006) A randomized phase II study of docetaxel alone or in combination with PANVAC-V (vaccinia) and PANVAC-F (fowlpox) in patients with metastatic breast cancer (NCI 05-C- 0229). Clin Breast Cancer 7:176-179 (Pubitemid 44044019)
51. Ramlau R, Quoix E, Rolski J, Pless M, Lena H, Levy E, Krzakowski M, Hess D, Tartour E, Chenard MP, Limacher JM, Bizouarne N, Acres B, Halluard C, Velu T (2008) A phase II study of Tg4010 (Mva-Muc1-Il2) in association with chemotherapy in patients with stage III/IV Non-small cell lung cancer. J Thorac Oncol 3:735-744
52. Nowak AK, Robinson BW, Lake RA (2003) Synergy between chemotherapy and immunotherapy in the treatment of established murine solid tumors. Cancer Res 63:4490-4496 (Pubitemid 36951021)
53. Dudley ME, Wunderlich JR, Robbins PF, Yang JC, Hwu P, Schwartzentruber DJ, Topalian SL, Sherry R, Restifo NP, Hubicki AM, Robinson MR, Raffeld M, Duray P, Seipp CA, Rogers- Freezer L, Morton KE, Mavroukakis SA, White DE, Rosenberg SA (2002) Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298:850-854 (Pubitemid 35231542)
54. Douillard JY, Tribodet H, Aubert D, Shepherd FA, Rosell R, Ding K, Veillard AS, Seymour L, Le Chevalier T, Spiro S, Stephens R, Pignon JP (2010) Adjuvant cisplatin and vinorelbine for completely resected non-small cell lung cancer: subgroup analysis of the Lung Adjuvant Cisplatin Evaluation. J Thorac Oncol 5:220-228
55. Mackall CL, Hakim FT, Gress RE (1997) Restoration of T-cell homeostasis after T-cell depletion. Semin Immunol 9:339-346 (Pubitemid 28021491)
56. Rosenberg SA, Sportes C, Ahmadzadeh M, Fry TJ, Ngo LT, Schwarz SL, Stetler-Stevenson M, Morton KE, Mavroukakis SA, Morre M, Buffet R, Mackall CL, Gress RE (2006) IL-7 administration to humans leads to expansion of CD8? and CD4? Cells but a relative decrease of CD4? T-regulatory cells. J Immunother 29:313-319 (Pubitemid 44297299)
57. Sportes C, Hakim FT, Memon SA, Zhang H, Chua KS, Brown MR, Fleisher TA, Krumlauf MC, Babb RR, Chow CK, Fry TJ, Engels J, Buffet R, Morre M, Amato RJ, Venzon DJ, Korngold R, Pecora A, Gress RE, Mackall CL (2008) Administration of rhIL-7 in humans increases in vivo TCR repertoire diversity by preferential expansion of naive T cell subsets. J Exp Med 205:1701-1714 (Pubitemid 351962032)
58. Melchionda F, Fry TJ, Milliron MJ, McKirdy MA, Tagaya Y, Mackall CL (2005) Adjuvant IL-7 or IL-15 overcomes immunodominance and improves survival of the CD8? memory cell pool. J Clin Invest 115:1177-1187 (Pubitemid 40629036)
59. Curti B, Thompson J, Puri S, Do D, Re R, Mi M, Fa F (2008) Cyclophosphamide and fludarabine treatment prior to reconstitution with PBMC and immunotherapy improves PSA-DT in men with androgen-independent prostate cancer. International Society for Biological Therapy of Cancer 23rd Annual Meeting 32
60. Kochenderfer JN, Simpson JL, Chien CD, Gress RE (2007) Vaccination regimens incorporating CpG-containing oligodeoxynucleotides and IL-2 generate antigen-specific antitumor immunity from T-cell populations undergoing homeostatic peripheral expansion after BMT. Blood 110:450-460 (Pubitemid 47026868)
61. Rech AJ, Vonderheide RH (2009) 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 1174:99-106
62. Lutsiak ME, Semnani RT, De Pascalis R, Kashmiri SV, Schlom J, Sabzevari H (2005) Inhibition of CD4?CD25? T regulatory cell function implicated in enhanced immune response by lowdose cyclophosphamide. Blood 105:2862-2868 (Pubitemid 40446280)
63. 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 (2005) Reduced frequencies and suppressive function of CD4? CD25hi regulatory T cells in patients with chronic lymphocytic leukemia after therapy with fludarabine. Blood 106:2018-2025 (Pubitemid 41291715)
64. Andersson A, Yang SC, Huang M, Zhu L, Kar UK, Batra RK, Elashoff D, Strieter RM, Dubinett SM, Sharma S (2009) IL-7 promotes CXCR3 ligand-dependent T cell antitumor reactivity in lung cancer. J Immunol 182:6951-6958
65. Huber C, Bobek N, Kuball J, Thaler S, Hoffarth S, Theobald M, Schuler M (2005) Inhibitors of apoptosis confer resistance to tumour suppression by adoptively transplanted cytotoxic T-lymphocytes in vitro and in vivo. Cell Death Differ 12:317-325 (Pubitemid 40520683)
66. Bougras G, Cartron PF, Gautier F, Martin S, LeCabellec M, Meflah K, Gregoire M, Vallette FM (2004) Opposite role of Bax and BCL-2 in the anti-tumoral responses of the immune system. BMC Cancer 4:54
67. Hayakawa A, Kawamoto Y, Nakajima H, Sakai J, Takasawa R, Nakashima I, Magae J, Tanuma S (2008) Bid truncation mediated by caspases-3 and -9 in vinorelbine-induced apoptosis. Apoptosis 13:523-530
68. Ramakrishnan R, Assudani D, Nagaraj S, Hunter T, Cho HI, Antonia S, Altiok S, Celis E, Gabrilovich DI (2010) Chemotherapy enhances tumor cell susceptibility to CTL-mediated killing during cancer immunotherapy in mice. J Clin Invest 120:1111-1124