Co-Introduced Functional CCR2 Potentiates In Vivo Anti-Lung Cancer Functionality Mediated by T Cells Double Gene-Modified to Express WT1-Specific T-Cell Receptor

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Asai, Hiroaki ^a   Fujiwara, Hiroshi ^a,b   An, Jun ^a   Ochi, Toshiki ^a,c   Miyazaki, Yukihiro ^a   Nagai, Kozo ^a   Okamoto, Sachiko ^d   Mineno, Junichi ^d   Kuzushima, Kiyotaka ^e   Shiku, Hiroshi ^f   Inoue, Hirofumi ^a   Yasukawa, Masaki ^a,b  

^a EHIME UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b EHIME UNIVERSITY   (Japan)

^c PRINCESS MARGARET HOSPITAL   (Canada)

^d TAKARA BIO INC   (Japan)

^e AICHI CANCER CENTER HOSPITAL   (Japan)

^f MIE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CHEMOKINE RECEPTOR CCR2; GAMMA INTERFERON; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; T LYMPHOCYTE RECEPTOR; WT1 PROTEIN;

ADOPTIVE IMMUNOTHERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER IMMUNOTHERAPY; CCL2 GENE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL LINE; LUNG CANCER; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; RNA GENE; SIGNAL TRANSDUCTION; T LYMPHOCYTE; WT1 GENE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTERLEUKIN-2; LUNG NEOPLASMS; LYMPHOCYTE ACTIVATION; MICE; MUROMONAB-CD3; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, CCR2; REPRODUCIBILITY OF RESULTS; T-LYMPHOCYTES; TRANSFECTION; TRANSPLANTATION, HETEROLOGOUS; WT1 PROTEINS;

EID: 84874141705     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056820     Document Type: Article

References (48)

1. Herbst RS, Heymach JV, Lippman SM, (2008) Lung cancer. N Engl J Med 359: 1367-1380.
2. Rosenberg SA, (2011) Cell transfer immunotherapy for metastatic solid cancer-what clinicians need to know. Nat Rev Clin Oncol 8: 577-585.
3. Robbins PF, Morgan RA, Feldman SA, Yang JC, Sherry RM, et al. (2011) Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol 29: 917-924.
4. Kalos M, Levine BL, Porter DL, Katz S, Grupp SA, et al. (2011) T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med 3: 95ra73.
5. Louis CU, Savoldo B, Dotti G, Pule M, Yvon E, et al. (2011) Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood 118: 6050-6056.
6. Ochi T, Fujiwara H, Okamoto S, An J, Nagai K, et al. (2011) Novel adoptive T-cell immunotherapy using a WT1-specific TCR vector encoding silencers for endogenous TCRs shows marked antileukemia reactivity and safety. Blood 118: 1495-1503.
7. Nagai K, Ochi T, Fujiwara H, An J, Shirakata T, et al. (2012) Aurora kinase A-specific T-cell receptor gene transfer redirects T lymphocytes to display effective antileukemia reactivity. Blood 119: 368-376.
8. Okamoto S, Mineno J, Ikeda H, Fujiwara H, Yasukawa M, et al. (2009) Improved expression and reactivity of transduced tumor-specific TCRs in human lymphocytes by specific silencing of endogenous TCR. Cancer Res 69: 9003-9011.
9. Bendle GM, Linnemann C, Hooijkaas AI, Bies L, de Witte MA, et al. (2010) Lethal graft-versus-host disease in mouse models of T cell receptor gene therapy. Nat Med 16: 565-570 561p following 570.
10. Oji Y, Miyoshi S, Maeda H, Hayashi S, Tamaki H, et al. (2002) Overexpression of the Wilms' tumor gene WT1 in de novo lung cancers. Int J Cancer 100: 297-303.
11. Hayashi S, Oji Y, Kanai Y, Teramoto T, Kitaichi M, et al. (2012) Low Wilms' tumor gene expression in tumor tissues predicts poor prognosis in patients with non-small-cell lung cancer. Cancer Invest 30: 165-171.
12. Makita M, Hiraki A, Azuma T, Tsuboi A, Oka Y, et al. (2002) Antilung cancer effect of WT1-specific cytotoxic T lymphocytes. Clin Cancer Res 8: 2626-2631.
13. Ohminami H, Yasukawa M, Fujita S, (2000) HLA class I-restricted lysis of leukemia cells by a CD8(+) cytotoxic T-lymphocyte clone specific for WT1 peptide. Blood 95: 286-293.
14. Ramos CA, Dotti G, (2011) Chimeric antigen receptor (CAR)-engineered lymphocytes for cancer therapy. Expert Opin Biol Ther 11: 855-873.
15. Kershaw MH, Wang G, Westwood JA, Pachynski RK, Tiffany HL, et al. (2002) Redirecting migration of T cells to chemokine secreted from tumors by genetic modification with CXCR2. Hum Gene Ther 13: 1971-1980.
16. Di Stasi A, De Angelis B, Rooney CM, Zhang L, Mahendravada A, et al. (2009) T lymphocytes coexpressing CCR4 and a chimeric antigen receptor targeting CD30 have improved homing and antitumor activity in a Hodgkin tumor model. Blood 113: 6392-6402.
17. Craddock JA, Lu A, Bear A, Pule M, Brenner MK, et al. (2010) Enhanced tumor trafficking of GD2 chimeric antigen receptor T cells by expression of the chemokine receptor CCR2b. J Immunother 33: 780-788.
18. Peng W, Ye Y, Rabinovich BA, Liu C, Lou Y, et al. (2010) Transduction of tumor-specific T cells with CXCR2 chemokine receptor improves migration to tumor and antitumor immune responses. Clin Cancer Res 16: 5458-5468.
19. Moon EK, Carpenito C, Sun J, Wang LC, Kapoor V, et al. (2011) Expression of a functional CCR2 receptor enhances tumor localization and tumor eradication by retargeted human T cells expressing a mesothelin-specific chimeric antibody receptor. Clin Cancer Res 17: 4719-4730.
20. William WN Jr, Glisson BS, (2011) Novel strategies for the treatment of small-cell lung carcinoma. Nat Rev Clin Oncol 8: 611-619.
21. Nakao M, Yamana H, Imai Y, Toh Y, Toh U, et al. (1995) HLA A2601-restricted CTLs recognize a peptide antigen expressed on squamous cell carcinoma. Cancer Res 55: 4248-4252.
22. Gomi S, Nakao M, Niiya F, Imamura Y, Kawano K, et al. (1999) A cyclophilin B gene encodes antigenic epitopes recognized by HLA-A24-restricted and tumor-specific CTLs. J Immunol 163: 4994-5004.
23. Calogero A, Hospers GA, Kruse KM, Schrier PI, Mulder NH, et al. (2000) Retargeting of a T cell line by anti MAGE-3/HLA-A2 alpha beta TCR gene transfer. Anticancer Res 20: 1793-1799.
24. Ito M, Hiramatsu H, Kobayashi K, Suzue K, Kawahata M, et al. (2002) NOD/SCID/gamma(c)(null) mouse: an excellent recipient mouse model for engraftment of human cells. Blood 100: 3175-3182.
25. Ochi T, Fujiwara H, Suemori K, Azuma T, Yakushijin Y, et al. (2009) Aurora-A kinase: a novel target of cellular immunotherapy for leukemia. Blood 113: 66-74.
26. Betts MR, Brenchley JM, Price DA, De Rosa SC, Douek DC, et al. (2003) Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J Immunol Methods 281: 65-78.
27. Pockaj BA, Sherry RM, Wei JP, Yannelli JR, Carter CS, et al. (1994) Localization of 111indium-labeled tumor infiltrating lymphocytes to tumor in patients receiving adoptive immunotherapy. Augmentation with cyclophosphamide and correlation with response. Cancer 73: 1731-1737.
28. Harlin H, Meng Y, Peterson AC, Zha Y, Tretiakova M, et al. (2009) Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res 69: 3077-3085.
29. Zhang T, Somasundaram R, Berencsi K, Caputo L, Gimotty P, et al. (2006) Migration of cytotoxic T lymphocytes toward melanoma cells in three-dimensional organotypic culture is dependent on CCL2 and CCR4. Eur J Immunol 36: 457-467.
30. Metelitsa LS, Wu HW, Wang H, Yang Y, Warsi Z, et al. (2004) Natural killer T cells infiltrate neuroblastomas expressing the chemokine CCL2. J Exp Med 199: 1213-1221.
31. Penido C, Costa MF, Souza MC, Costa KA, Candea AL, et al. (2008) Involvement of CC chemokines in gamma-delta T lymphocyte trafficking during allergic inflammation: the role of CCL2/CCR2 pathway. Int Immunol 20: 129-139.
32. Soria G, Yaal-Hahoshen N, Azenshtein E, Shina S, Leider-Trejo L, et al. (2008) Concomitant expression of the chemokines RANTES and MCP-1 in human breast cancer: a basis for tumor-promoting interactions. Cytokine 44: 191-200.
33. Zhang J, Lu Y, Pienta KJ, (2010) Multiple roles of chemokine (C-C motif) ligand 2 in promoting prostate cancer growth. J Natl Cancer Inst 102: 522-528.
34. Berencsi K, Rani P, Zhang T, Gross L, Mastrangelo M, et al. (2011) In vitro migration of cytotoxic T lymphocyte derived from a colon carcinoma patient is dependent on CCL2 and CCR2. J Transl Med 9: 33.
35. Niiya M, Niiya K, Kiguchi T, Shibakura M, Asaumi N, et al. (2003) Induction of TNF-alpha, uPA, IL-8 and MCP-1 by doxorubicin in human lung carcinoma cells. Cancer Chemother Pharmacol 52: 391-398.
36. Park JR, Digiusto DL, Slovak M, Wright C, Naranjo A, et al. (2007) Adoptive transfer of chimeric antigen receptor re-directed cytolytic T lymphocyte clones in patients with neuroblastoma. Mol Ther 15: 825-833.
37. Allavena P, Sica A, Solinas G, Porta C, Mantovani A, (2008) The inflammatory micro-environment in tumor progression: the role of tumor-associated macrophages. Crit Rev Oncol Hematol 66: 1-9.
38. Song L, Asgharzadeh S, Salo J, Engell K, Wu HW, et al. (2009) Valpha24-invariant NKT cells mediate antitumor activity via killing of tumor-associated macrophages. J Clin Invest 119: 1524-1536.
39. Sica A, Saccani A, Bottazzi B, Polentarutti N, Vecchi A, et al. (2000) Autocrine production of IL-10 mediates defective IL-12 production and NF-kappa B activation in tumor-associated macrophages. J Immunol 164: 762-767.
40. Daurkin I, Eruslanov E, Stoffs T, Perrin GQ, Algood C, et al. (2011) Tumor-associated macrophages mediate immunosuppression in the renal cancer microenvironment by activating the 15-lipoxygenase-2 pathway. Cancer Res 71: 6400-6409.
41. Izhak L, Wildbaum G, Jung S, Stein A, Shaked Y, et al. (2012) Dissecting the autocrine and paracrine roles of the CCR2-CCL2 axis in tumor survival and angiogenesis. PLoS One 7: e28305.
42. Kumar A, Humphreys TD, Kremer KN, Bramati PS, Bradfield L, et al. (2006) CXCR4 physically associates with the T cell receptor to signal in T cells. Immunity 25: 213-224.
43. Kremer KN, Humphreys TD, Kumar A, Qian NX, Hedin KE, (2003) Distinct role of ZAP-70 and Src homology 2 domain-containing leukocyte protein of 76 kDa in the prolonged activation of extracellular signal-regulated protein kinase by the stromal cell-derived factor-1 alpha/CXCL12 chemokine. J Immunol 171: 360-367.
44. Patrussi L, Ulivieri C, Lucherini OM, Paccani SR, Gamberucci A, et al. (2007) p52Shc is required for CXCR4-dependent signaling and chemotaxis in T cells. Blood 110: 1730-1738.
45. Schaeuble K, Hauser MA, Singer E, Groettrup M, Legler DF, (2011) Cross-talk between TCR and CCR7 signaling sets a temporal threshold for enhanced T lymphocyte migration. J Immunol 187: 5645-5652.
46. Ichinohasama R, Oji Y, Yokoyama H, Takeuchi K, Fujiwara T, et al. (2010) Sensitive immunohistochemical detection of WT1 protein in tumors with anti-WT1 antibody against WT1 235 peptide. Cancer Sci 101: 1089-1092.
47. Oka Y, Tsuboi A, Taguchi T, Osaki T, Kyo T, et al. (2004) Induction of WT1 (Wilms' tumor gene)-specific cytotoxic T lymphocytes by WT1 peptide vaccine and the resultant cancer regression. Proc Natl Acad Sci U S A 101: 13885-13890.
48. Deshmane SL, Kremlev S, Amini S, Sawaya BE, (2009) Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 29: 313-326.