Mutated Ras-transfected, EBV-transformed lymphoblastoid cell lines as a model tumor vaccine for boosting T-cell responses against pancreatic cancer: a pilot trial.

Genetically modified lymphoblastoid cell lines (LCL) have been shown to be an attractive alternative source of antigen-presenting cells for cancer vaccination in vitro. We tested their application in patients with pancreatic cancer in a phase I clinical trial. As a model tumor antigen, we selected the point-mutated (codon 12) Ki-Ras p21 oncogene (muRas) frequently (∼85%) present in pancreatic adenocarcinoma. Autologous LCLs were established in vitro by spontaneous outgrowth from peripheral blood lymphocytes of seven pancreatic carcinoma patients and were genetically modified with an episomal Epstein-Barr virus (EBV)-based expression vector to express muRas (muRas-LCL). Weekly vaccinations with subcutaneous injection of 5×10(6) muRas-LCL were done. In six of seven patients, therapeutic vaccination elicited a T-cell response with an increase in the frequency of muRas-specific precursor cytotoxic T lymphocytes in the peripheral blood and positive delayed-type hypersensitivity reactions at the injection site. Besides local reactions and flu-like symptoms, there were no signs of toxicity and no acute EBV infection, onset of EBV-associated lymphoma, or other severe complications. A clinical response (stable disease) was observed for a short time period (2-4 months) in four of seven patients (57%), mostly in earlier tumor stages. Our results indicate that LCL presenting genetically modified antigen represent a valuable and easily available tool for in vivo autologous tumor vaccination. LCL can be transfected with any known tumor antigen and therefore should be further clinically investigated.

[1]  D. Berry,et al.  Vaccination with patient-specific tumor-derived antigen in first remission improves disease-free survival in follicular lymphoma. , 2011, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[2]  H. Yoshiyama,et al.  Cytokine signatures of transformed B cells with distinct Epstein–Barr virus latencies as a potential diagnostic tool for B cell lymphoma , 2011, Cancer science.

[3]  H. Ueno,et al.  Recent Developments in Cancer Vaccines , 2011, The Journal of Immunology.

[4]  H. Friess,et al.  Adjuvant chemotherapy with fluorouracil plus folinic acid vs gemcitabine following pancreatic cancer resection: a randomized controlled trial. , 2010, JAMA.

[5]  D. Schadendorf,et al.  Improved survival with ipilimumab in patients with metastatic melanoma. , 2010, The New England journal of medicine.

[6]  P. Kantoff,et al.  Sipuleucel-T immunotherapy for castration-resistant prostate cancer. , 2010, The New England journal of medicine.

[7]  U. Laufs,et al.  Integrin-linked kinase is a central mediator in angiotensin II type 1- and chemokine receptor CXCR4 signaling in myocardial hypertrophy. , 2010, Biochemical and biophysical research communications.

[8]  C. Kurts,et al.  Cross-priming in health and disease , 2010, Nature Reviews Immunology.

[9]  A. Bardelli,et al.  Molecular mechanisms of resistance to cetuximab and panitumumab in colorectal cancer. , 2010, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[10]  E. Jaffee,et al.  Use of tumour-responsive T cells as cancer treatment , 2009, The Lancet.

[11]  P. Coulie,et al.  Peripheral blood lymphocytes genetically modified to express the self/tumor antigen MAGE-A3 induce antitumor immune responses in cancer patients. , 2009, Blood.

[12]  M. Braga,et al.  Carcinoembryonic Antigen-Specific but Not Antiviral CD4+ T Cell Immunity Is Impaired in Pancreatic Carcinoma Patients1 , 2008, The Journal of Immunology.

[13]  Rong-Fu Wang CD8+ regulatory T cells, their suppressive mechanisms, and regulation in cancer. , 2008, Human immunology.

[14]  K. Hess,et al.  Phase 2 trial of oxaliplatin plus capecitabine (XELOX) as second‐line therapy for patients with advanced pancreatic cancer , 2008, Cancer.

[15]  P. Srivastava,et al.  "It is the antigen(s), stupid" and other lessons from over a decade of vaccitherapy of human cancer. , 2008, Seminars in immunology.

[16]  L. Emens Cancer vaccines: on the threshold of success , 2008, Expert opinion on emerging drugs.

[17]  B. Ancrile,et al.  Oncogenic ras-induced expression of cytokines: a new target of anti-cancer therapeutics. , 2008, Molecular interventions.

[18]  Carl G. Figdor,et al.  Dendritic-cell immunotherapy: from ex vivo loading to in vivo targeting , 2007, Nature Reviews Immunology.

[19]  P. Murawa,et al.  Erlotinib Plus Gemcitabine Compared With Gemcitabine Alone in Patients With Advanced Pancreatic Cancer: A Phase III Trial of the National Cancer Institute of Canada Clinical Trials Group , 2023, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[20]  E. Degl'innocenti,et al.  Type 2 Cytotoxic T Lymphocytes Modulate the Activity of Dendritic Cells Toward Type 2 Immune Responses1 , 2006, The Journal of Immunology.

[21]  M. Pfreundschuh,et al.  Naturally occurring T-cell response against mutated p21 ras oncoprotein in pancreatic cancer. , 2006, Clinical cancer research : an official journal of the American Association for Cancer Research.

[22]  A. Ribas Genetically modified dendritic cells for cancer immunotherapy. , 2005, Current gene therapy.

[23]  V. Schirrmacher 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 , 2005, Cancer Immunology, Immunotherapy.

[24]  S. Holmes,et al.  Diversity and Recognition Efficiency of T Cell Responses to Cancer , 2004, PLoS medicine.

[25]  H. Burris,et al.  A randomized phase III study of rubitecan (ORA) vs. best choice (BC) in 409 patients with refractory pancreatic cancer report from a North-American multi-center study. , 2004, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[26]  Helen Hickey,et al.  A randomized trial of chemoradiotherapy and chemotherapy after resection of pancreatic cancer. , 2004, The New England journal of medicine.

[27]  R. Steinman,et al.  Dendritic Cells Initiate Immune Control of Epstein-Barr Virus Transformation of B Lymphocytes In Vitro , 2003, The Journal of experimental medicine.

[28]  R. Zinkernagel On natural and artificial vaccinations. , 2003, Annual review of immunology.

[29]  V. Engelhard,et al.  Route of Immunization with Peptide-pulsed Dendritic Cells Controls the Distribution of Memory and Effector T Cells in Lymphoid Tissues and Determines the Pattern of Regional Tumor Control , 2003, Journal of Experimental Medicine.

[30]  C. N. Coleman,et al.  CTCAE v3.0: development of a comprehensive grading system for the adverse effects of cancer treatment. , 2003, Seminars in radiation oncology.

[31]  M. Pfreundschuh,et al.  Use of spontaneous Epstein-Barr virus-lymphoblastoid cell lines genetically modified to express tumor antigen as cancer vaccines: mutated p21 ras oncogene in pancreatic carcinoma as a model. , 2002, Human gene therapy.

[32]  F. Marincola,et al.  A Phase I Study of Nonmyeloablative Chemotherapy and Adoptive Transfer of Autologous Tumor Antigen-Specific T Lymphocytes in Patients With Metastatic Melanoma , 2002, Journal of immunotherapy.

[33]  H. Kalthoff,et al.  Systemic and local immunosuppression in pancreatic cancer patients. , 2001, Clinical cancer research : an official journal of the American Association for Cancer Research.

[34]  M. Pfreundschuh,et al.  Gene-modified spontaneous Epstein-Barr virus-transformed lymphoblastoid cell lines as autologous cancer vaccines: Mutated p21 ras oncogene as a model , 2000, Cancer Gene Therapy.

[35]  A. Ribas,et al.  Immune deviation and Fas-mediated deletion limit antitumor activity after multiple dendritic cell vaccinations in mice. , 2000, Cancer research.

[36]  M. van Glabbeke,et al.  New guidelines to evaluate the response to treatment in solid tumors , 2000, Journal of the National Cancer Institute.

[37]  W. Britt,et al.  Simultaneous ex vivo expansion of cytomegalovirus and Epstein-Barr virus-specific cytotoxic T lymphocytes using B-lymphoblastoid cell lines expressing cytomegalovirus pp65. , 1999, Blood.

[38]  G. Schuler,et al.  Generation of large numbers of fully mature and stable dendritic cells from leukapheresis products for clinical application. , 1999, Journal of immunological methods.

[39]  F. Marincola,et al.  Immunologic and therapeutic evaluation of a synthetic peptide vaccine for the treatment of patients with metastatic melanoma , 1998, Nature Medicine.

[40]  M. Ladanyi,et al.  Human Epstein-Barr virus (EBV)-specific cytotoxic T lymphocytes home preferentially to and induce selective regressions of autologous EBV- induced B cell lymphoproliferations in xenografted C.B-17 scid/scid mice [published erratum appears in J Exp Med 1996 Sep 1;184(3):1199] , 1996, The Journal of experimental medicine.

[41]  O. Finn,et al.  Induction of cellular immunity in chimpanzees to human tumor-associated antigen mucin by vaccination with MUC-1 cDNA-transfected Epstein-Barr virus-immortalized autologous B cells. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[42]  A. Ben-nun,et al.  Endogenous antigen presentation by autoantigen-transfected Epstein-Barr virus-lymphoblastoid cells. I. Generation of human thyroid peroxidase-reactive T cells and their T cell receptor repertoire. , 1993, Journal of Clinical Investigation.

[43]  E. Kieff,et al.  Identification of target antigens for the human cytotoxic T cell response to Epstein-Barr virus (EBV): implications for the immune control of EBV-positive malignancies , 1992, The Journal of experimental medicine.

[44]  M. Pawlita,et al.  Local growth of a Burkitt's lymphoma versus disseminated invasive growth of the autologous EBV‐immortalized lymphoblastoid cells and their somatic cell hybrids in SCID mice , 1992, International journal of cancer.

[45]  C. Bangham,et al.  Specific human cytotoxic T cells recognize B-cell lines persistently infected with respiratory syncytial virus. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[46]  S. McLachlan,et al.  Cyclosporin A promotes spontaneous outgrowth in vitro of Epstein–Barr virus-induced B-cell lines , 1981, Nature.

[47]  C. P. Rhoads,et al.  Homotransplantation of human cell lines. , 1957, Bulletin of the New York Academy of Medicine.

[48]  C. Melief,et al.  Cancer immunology. , 2011, Current opinion in immunology.

[49]  Hisao Tajiri,et al.  Cancer immunotherapy by fusions of dendritic cells and tumor cells. , 2009, Immunotherapy.

[50]  M Van Glabbeke,et al.  New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. , 2000, Journal of the National Cancer Institute.

[51]  L. Sobin,et al.  TNM Classification of Malignant Tumours , 1987, UICC International Union Against Cancer.