Successful eradication of established peritoneal ovarian tumors in SCID-Beige mice following adoptive transfer of T cells genetically targeted to the MUC16 antigen

Clinical Cancer Research

Volumn 16, Issue 14, 2010, Pages 3594-3606

  Chekmasova, Alena A ^a   Rao, Thapi D ^a   Nikhamin, Yan ^a   Park, Kay J ^a   Levine, Douglas A ^a   Spriggs, David R ^a   Brentjens, Renier J ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUC16 ANTIGEN; RETROVIRUS VECTOR; TUMOR ANTIGEN; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CYTOKINE RELEASE; CYTOTOXICITY; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NONHUMAN; OVARY TUMOR; PRIORITY JOURNAL; SCID MOUSE; T LYMPHOCYTE; TUMOR CELL; TUMOR CELL LINE;

ANIMALS; CA-125 ANTIGEN; CYTOTOXICITY TESTS, IMMUNOLOGIC; FEMALE; HUMANS; IMMUNOTHERAPY, ADOPTIVE; MEMBRANE PROTEINS; MICE; MICE, SCID; OVARIAN NEOPLASMS; PERITONEAL NEOPLASMS; T-LYMPHOCYTES; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 77954712252     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-10-0192     Document Type: Article

References (67)

1. Singh AP, Senapati S, Ponnusamy MP, et al. Clinical potential of mucins in diagnosis, prognosis, and therapy of ovarian cancer. Lancet Oncol 2008;9:1076-85.
2. Sun CC, Ramirez PT, Bodurka DC. Quality of life for patients with epithelial ovarian cancer. Nat Clin Pract Oncol 2007;4:18-29. (Pubitemid 46017691)
3. Brentjens RJ, Latouche JB, Santos E, et al. Eradication of systemic B-cell tumors by genetically targeted human T lymphocytes costimulated by CD80 and interleukin-15. Nat Med 2003;9:279-86.
4. Hwu P, Yang JC, Cowherd R, et al. In vivo antitumor activity of T cells redirected with chimeric antibody/T-cell receptor genes. Cancer Res 1995;55:3369-73.
5. Imai C, Mihara K, Andreansky M, et al. Chimeric receptors with 4-1BB signaling capacity provoke potent cytotoxicity against acute lymphoblastic leukemia. Leukemia 2004;18:676-84. (Pubitemid 38500185)
6. Kershaw MH, Westwood JA, Parker LL, et al. A phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer. Clin Cancer Res 2006;12:6106-15.
7. Kochenderfer JN, Feldman SA, Zhao Y, et al. Construction and preclinical evaluation of an anti-CD19 chimeric antigen receptor. J Immunother 2009;32:689-702.
8. Loskog A, Giandomenico V, Rossig C, Pule M, Dotti G, Brenner MK. Addition of the CD28 signaling domain to chimeric T-cell receptors enhances chimeric T-cell resistance to T regulatory cells. Leukemia 2006;20:1819-28. (Pubitemid 44574993)
9. Maher J, Brentjens RJ, Gunset G, Riviere I, Sadelain M. Human T-lymphocyte cytotoxicity and proliferation directed by a single chimeric TCRζ/CD28 receptor. Nat Biotechnol 2002;20:70-5. (Pubitemid 34044918)
10. Moeller M, Haynes NM, Trapani JA, et al. A functional role for CD28 costimulation in tumor recognition by single-chain receptor-modified T cells. Cancer Gene Ther 2004;11:371-9.
11. Parker LL, Do MT, Westwood JA, et al. Expansion and characterization of T cells transduced with a chimeric receptor against ovarian cancer. Hum Gene Ther 2000;11:2377-87.
12. Sadelain M, Brentjens R, Riviere I. The promise and potential pitfalls of chimeric antigen receptors. Curr Opin Immunol 2009;21:215-23.
13. Stephan MT, Ponomarev V, Brentjens RJ, et al. T cell-encoded CD80 and 4-1BBL induce auto- and transcostimulation, resulting in potent tumor rejection. Nat Med 2007;13:1440-9. (Pubitemid 350224246)
14. Daly T, Royal RE, Kershaw MH, et al. Recognition of human colon cancer by T cells transduced with a chimeric receptor gene. Cancer Gene Ther 2000;7:284-91. (Pubitemid 30194564)
15. Jensen MC, Cooper LJ, Wu AM, Forman SJ, Raubitschek A. Engineered CD20-specific primary human cytotoxic T lymphocytes for targeting B-cell malignancy. Cytotherapy 2003;5:131-8. (Pubitemid 36596497)
16. Pule MA, Savoldo B, Myers GD, et al. Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med 2008;14:1264-70.
17. Savoldo B, Rooney CM, Di Stasi A, et al. Epstein Barr virus specific cytotoxic T lymphocytes expressing the anti-CD30ζ artificial chimeric T-cell receptor for immunotherapy of Hodgkin disease. Blood 2007;110:2620-30.
18. 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-γ chain chimeric receptor gene recognizing a human ovarian cancer antigen. Nat Med 1998;4:168-72. (Pubitemid 28137370)
19. Hollyman D, Stefanski J, Przybylowski M, et al. Manufacturing validation of biologically functional T cells targeted to CD19 antigen for autologous adoptive cell therapy. J Immunother 2009;32:169-80.
20. Lamers CH, Sleijfer S, Vulto AG, et al. Treatment of metastatic renal cell carcinoma with autologous T-lymphocytes genetically retargeted against carbonic anhydrase IX: first clinical experience. J Clin Oncol 2006;24:e20-2.
21. Till BG, Jensen MC, Wang J, et al. Adoptive immunotherapy for indolent non-Hodgkin lymphoma and mantle cell lymphoma using genetically modified autologous 20-specific T cells. Blood 2008;112:2261-71.
22. + T lymphocytes are prognostic factors of human ovarian cancer. Proc Natl Acad Sci U S A 2007;104:3360-5.
23. Leffers N, Gooden MJ, de Jong RA, et al. Prognostic significance of tumor-infiltrating T-lymphocytes in primary and metastatic lesions of advanced stage ovarian cancer. Cancer Immunol Immunother 2009;58:449-59.
24. +/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci U S A 2005;102:18538-43.
25. Zhang L, Conejo-Garcia JR, Katsaros D, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 2003;348:203-13.
26. Curiel TJ, Coukos G, Zou L, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004;10:942-9.
27. Leffers N, Lambeck AJ, de Graeff P, et al. Survival of ovarian cancer patients overexpressing the tumour antigen p53 is diminished in case of MHC class I down-regulation. Gynecol Oncol 2008;110:365-73.
28. Nelson BH. The impact of T-cell immunity on ovarian cancer outcomes. Immunol Rev 2008;222:101-16.
29. Wolf D, Wolf AM, Rumpold H, et al. The expression of the regulatory T cell-specific forkhead box transcription factor FoxP3 is associated with poor prognosis in ovarian cancer. Clin Cancer Res 2005;11:8326-31.
30. Badgwell D, Bast RC, Jr. Early detection of ovarian cancer. Dis Markers 2007;23:397-410.
31. Bast RC, Jr., Badgwell D, Lu Z, et al. New tumor markers: CA125 and beyond. Int J Gynecol Cancer 2005;15 Suppl 3:274-81.
32. Fritsche HA, Bast RC. CA 125 in ovarian cancer: advances and controversy. Clin Chem 1998;44:1379-80.
33. Krivak TC, Tian C, Rose GS, Armstrong DK, Maxwell GL. A Gynecologic Oncology Group Study of serum CA-125 levels in patients with stage III optimally debulked ovarian cancer treated with intraperitoneal compared to intravenous chemotherapy: an analysis of patients enrolled in GOG 172. Gynecol Oncol 2009;115:81-5.
34. O'Brien TJ, Beard JB, Underwood LJ, Dennis RA, Santin AD, York L. The CA 125 gene: an extracellular superstructure dominated by repeat sequences. Tumour Biol 2001;22:348-66.
35. Bellone S, Anfossi S, O'Brien TJ, et al. Generation of CA125-specific cytotoxic T lymphocytes in human leukocyte antigen-A2.1-positive healthy donors and patients with advanced ovarian cancer. Am J Obstet Gynecol 2009;200:75.e1-10.
36. Berek JS. Immunotherapy of ovarian cancer with antibodies: a focus on oregovomab. Expert Opin Biol Ther 2004;4:1159-65.
37. O'Brien TJ, Tanimoto H, Konishi I, Gee M. More than 15 years of CA 125: what is known about the antigen, its structure and its function. Int J Biol Markers 1998;13:188-95.
38. Dharma Rao T, Park KJ, Smith-Jones P, et al. Novel monoclonal antibodies against proximal (carboxy-terminal) portions of MUC16. Appl Immunohistochem Mol Morphol 2010, May 7, 2010 Epub ahead of print. PMID 20453816.
39. Liu J, Yang G, Thompson-Lanza JA, et al. A genetically defined model for human ovarian cancer. Cancer Res 2004;64:1655-63.
40. Wang Z, Raifu M, Howard M, et al. Universal PCR amplification of mouse immunoglobulin gene variable regions: the design of degenerate primers and an assessment of the effect of DNA polymerase 3′to 5′ exonuclease activity. J Immunol Methods 2000;233:167-77.
41. Doenecke A, Winnacker EL, Hallek M. Rapid amplification of cDNA ends (RACE) improves the PCR-based isolation of immunoglobulin variable region genes from murine and human lymphoma cells and cell lines. Leukemia 1997;11:1787-92.
42. Gong MC, Latouche JB, Krause A, Heston WD, Bander NH, Sadelain M. Cancer patient T cells genetically targeted to prostate-specific membrane antigen specifically lyse prostate cancer cells and release cytokines in response to prostate-specific membrane antigen. Neoplasia 1999;1:123-7.
43. Orlandi R, Gussow DH, Jones PT, Winter G. Cloning immunoglobulin variable domains for expression by the polymerase chain reaction. Proc Natl Acad Sci U S A 1989;86:3833-7.
44. Brentjens RJ, Santos E, Nikhamin Y, et al. Genetically targeted T cells eradicate systemic acute lymphoblastic leukemia xenografts. Clin Cancer Res 2007;13:5426-35.
45. Riviere I, Brose K, Mulligan RC. Effects of retroviral vector design on expression of human adenosine deaminase in murine bone marrow transplant recipients engrafted with genetically modified cells. Proc Natl Acad Sci U S A 1995;92:6733-7.
46. Quintas-Cardama A, Yeh RK, Hollyman D, et al. Multifactorial optimization of gammaretroviral gene transfer into human T lymphocytes for clinical application. Hum Gene Ther 2007;18:1253-60.
47. Latouche JB, Sadelain M. Induction of human cytotoxic T lymphocytes by artificial antigen-presenting cells. Nat Biotechnol 2000;18:405-9.
48. Santos EB, Yeh R, Lee J, et al. Sensitive in vivo imaging of T cells using a membrane-bound Gaussia princeps luciferase. Nat Med 2009;15:338-44.
49. + T-cell memory in tumor immunology and immunotherapy. Immunol Rev 2006;211:214-24.
50. Raspollini MR, Castiglione F, Rossi Degl'innocenti D, et al. Tumour-infiltrating γ/δ T-lymphocytes are correlated with a brief disease-free interval in advanced ovarian serous carcinoma. Ann Oncol 2005;16:590-6.
51. Tomsova M, Melichar B, Sedlakova I, Steiner I. Prognostic significance of CD3+ tumor-infiltrating lymphocytes in ovarian carcinoma. Gynecol Oncol 2008;108:415-20.
52. Woo EY, Chu CS, Goletz TJ, 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;61:4766-72.
53. Lamers CH, Langeveld SC, Groot-van Ruijven CM, Debets R, Sleijfer S, Gratama JW. Gene-modified T cells for adoptive immunotherapy of renal cell cancer maintain transgene-specific immune functions in vivo. Cancer Immunol Immunother 2007;56:1875-83.
54. Barber A, Sentman CL. Chimeric NKG2D T cells require both T celland host-derived cytokine secretion and perforin expression to increase tumor antigen presentation and systemic immunity. J Immunol 2009;183:2365-72.
55. Barber A, Zhang T, DeMars LR, Conejo-Garcia J, Roby KF, Sentman CL. Chimeric NKG2D receptor-bearing T cells as immunotherapy for ovarian cancer. Cancer Res 2007;67:5003-8.
56. Barber A, Zhang T, Sentman CL. Immunotherapy with chimeric NKG2D receptors leads to long-term tumor-free survival and development of host antitumor immunity in murine ovarian cancer. J Immunol 2008;180:72-8.
57. Carpenito C, Milone MC, Hassan R, 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;106:3360-5.
58. Kershaw MH, Westwood JA, Hwu P. Dual-specific T cells combine proliferation and antitumor activity. Nat Biotechnol 2002;20:1221-7.
59. Westwood JA, Smyth MJ, Teng MW, et al. Adoptive transfer of T cells modified with a humanized chimeric receptor gene inhibits growth of Lewis-Y-expressing tumors in mice. Proc Natl Acad Sci U S A 2005;102:19051-6.
60. Wilkie S, Picco G, Foster J, et al. Retargeting of human T cells to tumor-associated MUC1: the evolution of a chimeric antigen receptor. J Immunol 2008;180:4901-9.
61. Yoon SH, Lee JM, Cho HI, et al. Adoptive immunotherapy using human peripheral blood lymphocytes transferred with RNA encoding Her-2/neu-specific chimeric immune receptor in ovarian cancer xenograft model. Cancer Gene Ther 2009;16:489-97.
62. Hung CF, Wu TC, Monie A, Roden R. Antigen-specific immunotherapy of cervical and ovarian cancer. Immunol Rev 2008;222:43-69.
63. Park KJ, Soslow R, Linkov I, Rao TD, Spriggs DR. The extracellular portion of the MUC16 cytoplasmic domain is detectable in ovarian carcinomas using novel monoclonal antibody, 4H11. Mod Pathol 2008;21:217-8A.
64. Bluestone JA, Abbas AK. Natural versus adaptive regulatory T cells. Nat Rev Immunol 2003;3:253-7.
65. Bunt SK, Clements VK, Hanson EM, Sinha P, Ostrand-Rosenberg S. Inflammation enhances myeloid-derived suppressor cell cross-talk by signaling through Toll-like receptor 4. J Leukoc Biol 2009;85:996-1004.
66. Ozao-Choy J, Ma G, Kao J, et al. The novel role of tyrosine kinase inhibitor in the reversal of immune suppression and modulation of tumor microenvironment for immune-based cancer therapies. Cancer Res 2009;69:2514-22.
67. Morgan RA, Yang JC, Kitano M, Dudley ME, Laurencot CM, Rosenberg SA. Case report of a serious adverse event following the administration of T cells transduced with a chimeric antigen receptor recognizing ERBB2. Mol Ther 2010;18:843-51.