Adoptively transferred human lung tumor specific cytotoxic T cells can control autologous tumor growth and shape tumor phenotype in a SCID mouse xenograft model

Journal of Translational Medicine

Volumn 5, Issue , 2007, Pages

  Oflazoglu, Ezogelin ^a   Elliott, Mark ^b   Takita, Hiroshi ^a   Ferrone, Soldano ^a   Henderson, Robert A ^b   Repasky, Elizabeth A ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b GLAXOSMITHKLINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HLA ANTIGEN CLASS 1; INTERLEUKIN 2; TUMOR ANTIGEN; CYTOKINE; EPITOPE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER IMMUNOTHERAPY; CD8+ T LYMPHOCYTE; CELL INTERACTION; CELL ISOLATION; CELL SURVIVAL; CELL TRANSFER; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; EFFECTOR CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LUNG TUMOR; MALE; MEMORY CELL; MOUSE; NONHUMAN; PHENOTYPE; SCID MOUSE; TUMOR CELL LINE; TUMOR GROWTH; TUMOR XENOGRAFT; ADOPTIVE TRANSFER; ANIMAL; ANTIBODY SPECIFICITY; CELL PROLIFERATION; CYTOTOXICITY; DRUG SCREENING; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; MOUSE MUTANT; PATHOLOGY; SECRETION; TIME; TUMOR ASSOCIATED LEUKOCYTE;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, NEOPLASM; CELL PROLIFERATION; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; EPITOPES; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOLOGIC MEMORY; LUNG NEOPLASMS; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MICE; MICE, SCID; ORGAN SPECIFICITY; PHENOTYPE; T-LYMPHOCYTES, CYTOTOXIC; TIME FACTORS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 34547824143     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-5-29     Document Type: Article

References (58)

1. Nakao M Yamana H Imai Y Toh Y Toh U Kimura A Yanoma S Kakegawa T Itoh K HLA-A 2601-restricted CTLs recognize a peptide antigen expressed on squamous cell carcinoma Cancer Res 1995, 55:4248-4255 7671230
2. Weynants P Thonnard J Marchand M Delos M Boon T Coulie PG Derivation of tumor-specific cytolytic T-cell clones from two lung cancer patients with long survival Am J Resp Crit Care Med 1999, 159:55-62 9872818
3. Karanikas V Colau D Baurain JF Chiari R Thonnard J Gutierrez-Roelens I Goffinet C Van Schaftingen EV Weynants P Boon T Coulie PG High frequency of cytolytic T lymphocytes directed against a tumor-specific mutated antigen detectable with HLA tetramers in the blood of a lung carcinoma patient with long survival Cancer Res 2001, 61:3718-24 11325844
4. Nishizaka S Gomi S Harada K Oizumi K Itoh K Shichijo S A new tumor-rejection antigen recognized by cytotoxic T lymphocytes infiltrating into a lung adenocarcinoma Cancer Res 2000, 60:4830-7 10987294
5. Mami-Chouaib F Echchakir H Dorothee G Vergnon I Chouaib S Antitumor cytotoxic T-lymphocyte response in human lung carcinoma: Identification of a tumor-associated antigen Immunol Rev 2002, 188:114-21 10.1034/ j.1600-065X.2002.18810.x 12445285
6. Sogn JA Tumor Immunology: The glass is half full Immunity 1998, 9:757-763 10.1016/S1074-7613(00)80641-X 9881966
7. Marincola FM Jaffee EM Hicklin DJ Ferrone S Escape of human solid tumors from T-cell recognition: Molecular mechanisms and functional significance Adv Immunol 2000, 74:181-273 10605607
8. Berke G The binding and lysis of target cells by cytotoxic T lymphocytes: Molecular and cellular aspects Ann Rev Immunol 1994, 12:735-773 10.1146/annurev.iy.12.040194.003511
9. Restifo NP Wunderlich JR Biology of cellular immune responses Biologic therapy of cancer Philadelphia: JB Lippincott Company De Vita VT, Hellman S, Rosenberg SA 1995, 3:37
10. Finn OJ Tumor rejection antigens recognized by T lymphocytes Curr Opin Immunol 1993, 5:701-708 10.1016/0952-7915(93)90124-B 8240731
11. Finke JH Zea AH Stanley J Loss of T cell receptor zeta chain and p56lck in T cell infiltrating human renal cell carcinoma Cancer Res 1993, 53:5613-5616 8242613
12. Mizoguchi H O'Shea JJ Longo DL Loeffler CM McVicar DW Ochoa AC Alterations in signal transduction molecules in T lymphocytes from tumor bearing mice Science 1992, 258:1795-1798 10.1126/science.1465616 1465616
13. Levey DL Srivastava PK Alterations in T cells of cancer-bearers Immunol Today 1996, 17:365-368 10.1016/0167-5699(96)10013-X 8783496
14. Loeffler CM Smyth MJ Longo DL Kopp WC Harvey LK Tribble HR Tase JE Urba WJ Leonard AS Young HA Ochoa AC Immunoregulation in cancer-bearing hosts. Downregulation of gene expression and cytotoxic function in CD8+ T cells J Immunol 1992, 149:949-956 1353099
15. Sulitzeanu D Immunosuppressive factors in human cancer Adv Cancer Res 1993, 60:247-267 7678060
16. Chouaib S Asselin-Paturel C Mami-Chouaib F Caignard A Blay JY The host-tumor immune conflict: From immunosuppression to resistance and destruction Immunol Today 1997, 18:493-497 10.1016/S0167-5699(97)01115-8 9357142
17. Jain RK Barriers to drug delivery in solid tumors Scientific American 1994, 271:58-65 8066425
18. Jain RK Delivery of molecular and cellular medicine to solid tumors Microcirculation 1997, 4:1-123 9110280
19. Melief CJM Tumor eradication by adoptive transfer of cytotoxic T lymphocytes Adv Cancer Res 1992, 58:143-75 1532109
20. Gattinoni L Powell DJ Jr Rosenberg SA Restifo NP Adoptive immunotherapy for cancer: Building on success Nat Rev Immunol 2006, 6:383-93 1473162 16622476 10.1038/nri1842
21. Rosenberg SA Immunotherapy of cancer using interleukin 2: Current status and future prospects Immunol Today 1988, 9:58-62 10.1016/ 0167-5699(88)91261-3 3076761
22. Topalian SL Muul LM Solomon D Rosenberg SA Expansion of human tumor infiltrating lymphocytes for use in immunotherapy trials J Immunol Methods 1987, 102:127-141 3305708
23. Topalian SL Solomon D Avis FP Chang AE Freerksen DL Linehan WM Lotze MT Robertson CN Seipp SA Simon P Simpson CG Rosenberg SA Immunotherapy of patients with advanced cancer by tumor infiltrating lymphocytes and recombinant interleukin 2; a pilot study J Clin Oncol 1988, 6:839-853 3259261
24. Crowley NJ Vervaert CE Seigler HF Human xenograft-nude mouse model of adoptive immunotherapy with human melanoma specific cytotoxic T cells Cancer Res 1992, 52:394-399 1728411
25. Boon T Tumor antigens recognized by cytolytic T lymphocytes: Present perspectives for specific immunotherapy Int J Cancer 1993, 54:177-180 10.1002/ijc.2910540202 8486420
26. Brichard V van Pel A Wolfel T Wolfel C De Plaen E Lethe B Coulie P Boon T The tyrosinase gene codes for an antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas J Exp Med 1993, 178:489-95 10.1084/jem.178.2.489 8340755
27. Verra NC Jorritsma A Weijer K Ruizendaal JJ Voordouw A Weder P Hooijberg E Schumacher TN Haanen JB Spits H Luiten RM Human telomerase reverse transcriptase-transduced human cytotoxic T cells suppress the growth of human melanoma in immunodeficient mice Cancer Res 2004 64 2153 61 10.1158/0008-5472.CAN-03-1339 15026357
28. Finke JH Rayman P Edinger M Characterization of a human renal cell carcinoma specific cytotoxic CD8+ T cell line J Immunother 1992, 11:1-11 10.1097/00002371-199201000-00001 1734943
29. Freedman RS Ionnides CG Mathioudakis G Platsoucas CD Novel immunologic strategies in ovarian carcinoma Am J Obstet Gynecol 1992, 167:1470-1478 1332480
30. Faber LM van Luxemburg-Heijs SAP Willemze R Falkenburg JHF Generation of leukemia-reactive cytotoxic T lymphocytes clones from the HLA-identical bone marrow donor of a patient with leukemia J Exp Med 1992, 176:1283-9 10.1084/jem.176.5.1283 1402674
31. Nijmeijer BA Willemze R Falkenburg JH An animal model for human cellular immunotherapy: Specific eradication of human acute lymphoblastic leukemia by cytotoxic T lymphocytes in NOD/scid mice Blood 2002, 100:654-60 10.1182/blood.V100.2.654 12091361
32. Hambach L Nijmeijer BA Aghai Z Schie ML Wauben MH Falkenburg JH Goulmy E Human cytotoxic T lymphocytes specific for a single minor histocompatibility antigen HA-1 are effective against human lymphoblastic leukaemia in NOD/scid mice Leukemia 2006, 20:371-4 10.1038/ sj.leu.2404056 16357839
33. Kowolik CM Topp MS Gonzalez S Pfeiffer T Olivares S Gonzalez N Smith DD Forman SJ Jensen MC Cooper LJ CD28 costimulation provided through a CD19-specific chimeric antigen receptor enhances in vivo persistence and antitumor efficacy of adoptively transferred T cells Cancer Res 2006, 66:10995-1004 10.1158/0008-5472.CAN-06-0160 17108138
34. Doubrovina ES Doubrovin MM Lee S Shieh JH Heller G Pamer E O'Reilly RJ In vitro stimulation with WT1 peptide-loaded Epstein-Barr virus-positive B cells elicits high frequencies of WT1 peptide-specific T cells with in vitro and in vivo tumoricidal activity Clin Cancer Res 2004, 10:7207-19 10.1158/1078-0432.CCR-04-1040 15534094
35. Feuerer M Beckhove P Bai L Solomayer EF Bastert G Diel IJ Pedain C Oberniedermayr M Schirrmacher V Umansky V Therapy of human tumors in NOD/ SCID mice with patient-derived reactivated memory T cells from bone marrow Nat Med 2001, 7:452-8 10.1038/86523 11283672
36. Beckhove P Feuerer M Dolenc M Schuetz F Choi C Sommerfeldt N Schwendemann J Ehlert K Altevogt P Bastert G Schirrmacher V Umansky V Specifically activated memory T cell subsets from cancer patients recognize and reject xenotransplanted autologous tumors J Clin Invest 2004, 114:67-76 437963 15232613 10.1172/JCI200420278
37. Visonneau S Cesano A Torosian MH Santoli D Cell therapy of a highly invasive human breast carcinoma implanted in immunodeficient (SCID) mice Clin Cancer Res 1997, 3:1491-500 9815835
38. Wright SE Rewers-Felkins KA Quinlin IS Eldridge PW Zorsky PE Klug PP Phillips CA Philip R Adoptive immunotherapy of mucin1 expressing adenocarcinomas with mucin1 stimulated human peripheral blood mononuclear cells Int J Mol Med 2002, 9:401-4 11891536
39. Stam NJ Spits H Ploegh HL Monoclonal antibodies raised against denatured HLA-B locus heavy chains permit biochemical characterization of certain HLA-C locus products J Immunol 1986, 137:2299-2306 3760563
40. Perosa F Luccarelli G Prete M Favoino E Ferrone S Dammacco F Beta 2-microglobulin-free HLA class I heavy chain epitope mimicry by monoclonal antibody HC-10-specific peptide J Immunol 2003, 171:1918-1926 12902494
41. Tanaka T Tsudo M Karasuyama H Kitamura F Kono T Hatakeyama M Taniguchi T Miyasaka M A novel monoclonal antibody against murine IL-2 receptor-chain: Characterization of receptor expression in normal lymphoid cells and EL-4 cells J Immunol 1991, 147:2222-8 1918958
42. Hayashi Y Hoon DS Park MS Terasaki PI Morton DL Cytotoxic T cell lines recognize autologous and allogeneic melanomas with share or crossreactive HLA-A Cancer Immunol Immunother 1992, 34:419-423 10.1007/ BF01741754 1373343
43. Sabzevari H Reisfeld RA Human Cytotoxic T-Cells suppress the growth of spontaneous melanoma metastases in SCID/hu Mice Cancer Res 1993, 53:4933-4937 8402683
44. Hamann D Baars PA Rep MHG Hooibrink B Kerkhof-Garde SR Klein MR van Lier RA Phenotypic and functional separation of effector and memory human CD8+ T cells J Exp Med 1997, 186:1407 10.1084/jem.186.9.1407 9348298
45. Fukada K Sobao Y Tomiyama H Oka S Takiguchi M Functional expression of the chemokine receptor CCR5 on virus epitope specific memory and effector CD8+ T cells J Immunol 2002, 168:2225-2232 11859109
46. Egilmez NK Hess SD Chen FA Takita H Conway TF Bankert RB Human CD4+ effector T cells mediate indirect interleukin-12- and interferon-gamma-dependent suppression of autologous HLA-negative lung tumor xenografts in severe combined immunodeficient mice Cancer Res 2002, 62:2611-7 11980657
47. Bosma M Carroll A The SCID mouse mutant: Definition, characterization, and potential uses Annu Rev Immunol 1991, 9:323 10.1146/ annurev.iy.09.040191.001543 1910681
48. Bankert RB Egilmez NK Hess SD Human-SCID mouse chimeric models for the evaluation of anti-cancer therapies Trend Immunol 2001, 22:386-93 10.1016/S1471-4906(01)01943-3
49. Xu Y Silver DF Yang NP Oflazoglu E Hempling RE Piver MS Repasky EA Characterization of human ovarian carcinomas in a SCID mouse model Gynecologic Oncology 1999, 72:161-70 10.1006/gyno.1998.5238 10021295
50. Bankert RB Umemoto Y Sugiyama Chen FA Repasky E Yokota S Human lung tumors, patients' peripheral blood lymphocytes and tumor infiltrating lymphocytes propagated in scid mice Curr Top Microbial Immunol 1989, 152:201-210
51. Sakakibara T Xu Y Bumpers HL Chen FA Bankert RB Arredondo MA Edge SB Repasky EA Growth and metastasis of surgical specimens of human breast carcinomas in SCID mice Cancer J Sci Am 1996, 2(5)291-300 9166547
52. Naka T Sugamura K Hylander BL Widmer MB Rustum YM Repasky EA Effects of tumor necrosis factor-related apoptosis-inducing ligand alone and in combination with chemotherapeutic agents on patients' colon tumors grown in SCID mice Cancer Res 2002, 62:5800-6 12384541
53. Hylander BL Pitoniak R Penetrante RB Gibbs JF Oktay D Cheng J Repasky EA The anti-tumor effect of Apo2L/TRAIL on patient pancreatic adenocarcinomas grown as xenografts in SCID mice J Transl Med 2005, 3:22 1156958 15943879 10.1186/1479-5876-3-22
54. Khong HT Wang QJ Rosenberg SA Identification of multiple antigens recognized by tumor-infiltrating lymphocytes from a single patient: Tumor escape by antigen loss and loss of MHC expression J Immunother 2004, 27:184-90 10.1097/00002371-200405000-00002 15076135
55. Kedl RM Schaefer BC Kappler JW Marrack P T cells down-modulate peptide-MHC complexes on APCs in vivo Nature Immunol 2002, 3(1)27-32 10.1038/ni742
56. Shankaran V Ikeda H Bruce AT White JM Swanson PE Old LJ Schreiber RD IFN gamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity Nature 2001, 410:1107-1111 10.1038/35074122 11323675
57. Tsai L Ohlen C Ljunggren HG Karre K Hansson M Kiessling R Effect of IFN-gamma treatment and in vivo passage of murine tumor cell lines on their sensitivity to lymphokine-activated killer (LAK) cell lysis in vitro; association with H-2 expression on the target cells Int J Cancer 1989, 44:669-74 10.1002/ijc.2910440419 2507452
58. Kono K Halapi E Hising C Petersson M Gerdin E Vanky F Kiessling R Mechanisms of escape from CD8+ T-cell clones specific for the HER-2/neu proto-oncogene expressed in ovarian carcinomas: Related and unrelated to decreased MHC class 1 expression Int J Cancer 1997, 70:112-9 10.1002/ (SICI)1097-0215(19970106)70:1<112::AID-IJC17>3.0.CO;2-N 8985099