WT1 peptide vaccine as a paradigm for "cancer antigen-derived peptide"-based immunotherapy for malignancies: Successful induction of anti-cancer effect by vaccination with a single kind of WT1 peptide

Anti-Cancer Agents in Medicinal Chemistry

Volumn 9, Issue 7, 2009, Pages 787-797

  Oka, Yoshihiro ^a   Tsuboi, Akihiro ^a   Fujiki, Fumihiro ^a   Li, Zheyu ^a   Nakajima, Hiroko ^a   Hosen, Naoki ^a   Shirakata, Toshiaki ^a   Nishida, Sumiyuki ^a   Oji, Yusuke ^a   Kawase, Ichiro ^a   Sugiyama, Haruo ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Cancer; CTL; Helper; Immunotherapy; Peptide; Vaccine; WT1

Indexed keywords

PEPTIDE VACCINE; UNCLASSIFIED DRUG; WT1 PEPTIDE VACCINE;

ACUTE GRANULOCYTIC LEUKEMIA; AMINO ACID SEQUENCE; BREAST CANCER; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CANCER PATIENT; CHRONIC MYELOID LEUKEMIA; CHRONIC MYELOMONOCYTIC LEUKEMIA; CLINICAL TRIAL; CYTOTOXIC T LYMPHOCYTE; DRUG EFFICACY; DRUG MECHANISM; DRUG RESPONSE; DRUG TARGETING; GLIOBLASTOMA; HEMATOLOGIC MALIGNANCY; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; KIDNEY CANCER; LOW DRUG DOSE; LUNG CANCER; MALIGNANT NEOPLASTIC DISEASE; MINIMAL RESIDUAL DISEASE; MULTIPLE MYELOMA; MYELODYSPLASTIC SYNDROME; NONHUMAN; OUTCOME ASSESSMENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUALITY OF LIFE; REVIEW; RHABDOMYOSARCOMA; SOLID TUMOR; SYSTEMIC DISEASE;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, NEOPLASM; CANCER VACCINES; CLINICAL TRIALS AS TOPIC; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOTHERAPY; MICE; NEOPLASMS; PEPTIDES; T-LYMPHOCYTES, CYTOTOXIC; WT1 PROTEINS;

EID: 73449117871     PISSN: 18715206     EISSN: None     Source Type: Journal    
DOI: 10.2174/187152009789056958     Document Type: Review

References (87)

1. Oka, Y.; Tsuboi, A.; Oji, Y.; Kawase, I.; Sugiyama, H. WT1 peptide vaccine for the treatment of cancer. Curr. Opin. Immunol., 2008, 20(2), 211-220.
2. Yamagami, T.; Sugiyama, H.; Inoue, K.; Ogawa, H.; Tatekawa, T.; Hirata, M.; Kudoh, T.; Akiyama, T.; Murakami, A.; Maekawa, T.; Kishimoto T. Growth inhibition of human leukemic cells by WT1 (Wilms tumor gene) antisense oligodeoxynucleotides: implications for the involvement of WT1 in leukemogenesis. Blood, 1996, 87(7), 2878-2884.
3. Inoue, K.; Tamaki, H.; Ogawa, H.; Oka, Y.; Soma, T.; Tatekawa, T.; Oji, Y.; Tsuboi, A.; Kim, E.H.; Kawakami, M.; Akiyama, T.; Kishimoto, T., Sugiyama, H. Wilms' tumor gene (WT1) competes with differentiation-inducing signal in hematopoietic progenitor cells. Blood, 1998, 91(8), 2969-2976.
4. Tsuboi, A.; Oka Y.; Ogawa, H.; Elisseeva, O.A.; Tamaki, H.; Oji, Y.; Kim, E.H.; Soma, T.; Tatekawa, T.; Kawakami, M.; Kishimoto, T.; Sugiyama, H. Constitutive expression of the Wilms' tumor gene WT1 inhibits the differentiation of myeloid progenitor cells but promotes their proliferation in response to granulocyte-colony stimulating factor (G-CSF). Leuk. Res., 1999, 23(5), 499-505.
5. Sugiyama, H. Wilms' tumor gene WT1: its oncogenic function and clinical application. Int. J. Hematol., 2001, 73(2), 177-187.
6. Inoue, K.; Sugiyama, H.; Ogawa, H.; Nakagawa, M.; Yamagami, T.; Miwa, H.; Kita, K.; Hiraoka, A.; Masaoka, T.; Nasu, K.; Kyo, T.; Dohy, H.; Nakauchi, H.; Ishidate, T.; Akiyama, T.; Kishimoto, T. WT1 as a new prognostic factor and a new marker for the detection of minimal residual disease in acute leukemia. Blood, 1994, 84(9), 3071-3079.
7. Ogawa, H.; Tamaki, H.;. Ikegame, K.; Soma, T.; Kawakami, M.; Tsuboi, A.; Kim, E.H.; Hosen, N.; Murakami, M.; Fujioka, T.; Masuda, T.; Taniguchi, Y.; Nishida, Oji, Y.; Oka, Y.; Sugiyama, H. The usefulness of monitoring WT1 gene transcripts for the prediction and management of relapse following allogeneic stem cell transplantation in acute type leukemia. Blood, 2003, 101(5), 1698-1704.
8. Cilloni, D.; Gottardi, E.; Fava, M.; Messa, F.; Carturan, S.; Busca, A.; Guerrasio, A.; Saglio, G. Usefulness of quantitative assessment of the WT1 gene transcript as a marker for minimal residual disease detection. Blood, 2003, 102(2), 773-774.
9. Cilloni, D.; Messa, F.; Arruga, F.; Defilippi, I.; Gottardi, E.; Fava, M.; Carturan, S.; Catalano, R.; Bracco, E.; Messa, E.; Nicoli, P.; Diverio, D.; Sanz, M.A.; Martinelli, G.; Lo-Coco, F.; Saglio, G. Early prediction of treatment outcome in acute myeloid leukemia by measurement of WT1 transcript levels in peripheral blood samples collected after chemotherapy. Haematologica, 2008, 93(6), 921-924.
10. Candoni, A.; Tiribelli, M.; Toffoletti, E.; Cilloni, D.; Chiarvesio, A.; Michelutti, A.; Simeone. E.; Pipan, C.; Saglio, G.; Fanin, R. Quantitative assessment of WT1 gene expression after allogeneic stem cell transplantation is a useful tool for monitoring minimal residual disease in acute myeloid leukemia. Eur. J. Haematol., 2009, 82(1), 61-68.
11. Nakatsuka, S-I.; Oji, Y.; Horiuchi, T.; Kanda, T.; Kitagawa, M.; Takeuchi, T.; Kawano, K.; Kuwae, Y.; Yamauchi, A.; Okumura, M.; Kitamura, Y.; Oka, Y.; Kawase, I.; Sugiyama, H.; Aozasa K. Immunohistochemical detection of WT1 protein in a variety of cancer cells. Mod. Pathol., 2006,19(6), 804-814.
12. Oka, Y.; Tsuboi, A.; Elisseeva, O.A.; Udaka, K.; Sugiyama, H. WT1 as a novel target antigen for cancer immunotherapy. Curr. Cancer Drug Targets, 2002, 2(1), 45-54.
13. Gaiger, A.; Reese, V.; Disis, M.L.; Cheever, M.A. Immunity to WT1 in the animal model and in patients with acute myeloid leukemia. Blood, 2000, 96(4), 1480-1489.
14. Gaiger, A.; Carter, L.; Greinix, H.; Carter, D.; McNeill, P.D.; Houghton, R.L.; Cornellison, C.D.; Vedvick, T.S.; Skeiky, Y.A.; Cheever, M.A. WT1-specific serum antibodies in patients with leukemia. Clin. Cancer Res., 2001, 7(3 Suppl), 761s-765s.
15. Elisseeva, O.A.; Oka, Y.; Tsuboi, A.; Ogata, K.; Wu, F.; Kim, E.H.; Soma, T.; Tamaki, H.; Kawakami, M.; Oji, Y.; Hosen, N.; Kubota, T.; Nakagawa, M.; Yamagami, T.; Hiraoka, A.; Tsukaguchi, M.; Udaka, K.; Ogawa, H.; Kishimoto, T.; Nomura, T.; Sugiyama, H. Humoral immune responses against Wilms tumor gene WT1 product in patients with hematopoietic malignancies. Blood, 2002, 99(9), 3272-3279.
16. Wu, F.; Oka, Y.; Tsuboi, A.; Elisseeva, O.A.; Ogata, K.; Nakajima, H.; Fujiki, F.; Masuda, T.; Murakami, M.; Yoshihara, S.; Ikegame, K.; Hosen, N.; Kawakami, M.; Nakagawa, M.; Kubota, T.; Soma, T.; Yamagami, T.; Tsugaguchi, M.; Ogawa, H.; Oji, Y.; Hamaoka, T.; Kawase, I.; Sugiyama, H. Th1-biased humoral immune responses against Wilms tumor gene WT1 product in the patients with hematopoietic malignancies. Leukemia, 2005, 19(2), 268-274.
17. Oji, Y.; Kitamura, Y.; Kamino, E.; Kitano, A.; Sawabata, N.; Inoue, M.; Mori, M.; Nakatsuka, S-I.; Sakaguchi, N.; Miyazaki, K.; Nakamura, M.; Fukuda, I.; Nakamura, J.; Tatsumi, N.; Takakuwa, T.; Nishida, S.; Shirakata, T.; Hosen, N.; Tsuboi, A.; Nezu, R.; Maeda, H.; Oka, Y.; Kawase, I.; Aozasa, K.; Okumura, M.; Miyoshi, S.; Sugiyama, H. WT1 IgG antibody for early detection of nonsmall cell lung cancer and as its prognostic factor. Int. J. Cancer, 2009, 125, 381-387.
18. Scheibenbogen, C.; Letsch, A.; Thiel, E.; Schmittel, A.; Mailaender, V.; Baerwolf, S.; Nagorsen, D.; Keilholz, U. CD8 T-cell responses to Wilms tumor gene product WT1 and proteinase 3 in patients with acute myeloid leukemia. Blood, 2002, 100(6), 2132-2137.
19. Rezvani, K,; Grube, M.; Brenchley, J.M.; Sconochia, G.; Fujiwara, H.; Price, D.; Gostick, E.; Yamada, K.; Melenhorst, J.; Childs, R.; Henzel, N.; Douek, D.C.; Barrett, A.J. Functional leukemiaassociated antigen-specific memory CD8+ T cells exist in healthy individuals and in patients with chronic myelogenous leukemia before and after stem cell transplantation. Blood, 2003, 102(8), 2892-2900.
20. Rezvani, K., Brenchley, J.M.; Price, D.A.; Kilical, Y.; Gostick, E.; Sewell, A.K.; Li, J.; Mielke, S.; Douek, D.C.; Barrett, A.J. T-Cell responses directed against multiple HLA-A*0201-restricted epitopes derived from wilms' tumor 1 protein in patients with leukemia and healthy donors: identification, quantification, and characterization. Clin. Cancer Res., 2005, 11(24), 8799-8807.
21. Morita, Y.; Heike, Y.; Kawakami, M.; Miura, O.; Nakatsuka, S.; Ebisawa, M.; Mori, S.; Tanosaki, R.; Fukuda, T.; Kim, S.W.; Tobinai, K.; Takaue, Y. Monitoring of WT1-specific cytotoxic T lymphocytes after allogeneic hematopoietic stem cell transplantation. Int. J. Cancer, 2006, 119(6), 1360-1367.
22. Gillmore, R.; Xue, S.A.; Holler, A.; Kaeda, J.; Hadjiminas, D.; Healy, V.; Dina, R.; Parry, S.C.; Bellantuono, I.; Ghani, Y.; Coombes, R.C.; Waxman, J.; Stauss, H.J. Detection of Wilms' tumor antigen-specific CTL in tumor-draining lymph nodes of patients with early breast cancer. Clin. Cancer Res., 2006, 12(1), 34-42.
23. Rezvani, K.; Yong, A.S.; Savani, B.N.; Mielke, S.; Keyvanfar, K.; Gostick. E.; Price, D.A.; Douek, D.C.; Barrett, A.J. Graft-versus-leukemia effect associated with detectable Wilms tumor-1 specific T lymphocytes after allogeneic stem-cell transplantation for acute lymphoblastic leukemia. Blood, 2007, 110(6), 1924-1932.
24. Yong, A.S.; Keyvanfar, K.; Eniafe, R.; Savani, B.N.; Rezvani, K.; Sloand, E.M.; Goldman, J.M.; Barrett, A.J. Hematopoietic stem cells and progenitors of chronic myeloid leukemia express leukemia-associated antigens: implications for the graft-versus-leukemia effect and peptide vaccine-based immunotherapy. Leukemia, 2008, 22(9), 1721-1727.
25. Oka, Y.; Tsuboi, A.; Fujiki, F.; Shirakata, T.; Nishida, S.; Hosen, N.; Nakajima, H.; Li, Z.; Kawase, I.; Oji, Y.; Sugiyama, H. "Cancer antigen WT1 protein-derived peptide"-based treatment of cancer -toward the further development. Curr. Med. Chem. 2008, 15(29), 3052-3061.
26. Oka, Y.; Elisseeva, O.A.; Tsuboi, A.; Ogawa, H.; Tamaki, H.; Li, H.; Oji, Y.; Kim, E. H.; Soma, T.; Asada, M.; Ueda, K.; Maruya, E.; Saji, H.; Kishimoto, T.; Sugiyama, H. Human cytotoxic T lymphocyte responses specific for peptides of wild-type Wilms' tumor gene (WT1) product. Immunogenetics, 2000, 51(2), 99-107.
27. Gao, L.; Bellantuono, I.; Elsasser, A.; Marley, SB.; Gordon, M.Y.; Goldman, J.M.; Stauss, H.J. Selective elimination of leukemic CD34(+) progenitor cells by cytotoxic T lymphocytes specific for WT1. Blood, 2000, 95(7), 2198-2203.
28. Ohminami, H.; Yasukawa, M.; Fujita, S. HLA class I-restricted lysis of leukemia cells by a CD8(+) cytotoxic T-lymphocyte clone specific for WT1 peptide. Blood, 2000, 95(1), 286-293.
29. Makita, M.; Hiraki, A.; Azuma, T.; Tsuboi, A.; Oka, Y.; Sugiyama, H.; Fujita, S.; Tanimoto, M.; Harada, M.; Yasukawa, M. Antilung cancer effect of WT1-specific cytotoxic T lymphocytes. Clin. Cancer Res., 2002, 8(8), 2626-2631.
30. Bellantuono, I.; Gao, L.; Parry S.; Marley, S.; Dazzi, F.; Apperley, J.; Goldman, J.M.; Stauss, H.J. Two distinct HLA-A0201-presented epitopes of the Wilms tumor antigen 1 can function as targets for leukemia-reactive CTL. Blood, 2002, 100(10), 3835-3837.
31. Azuma, T.; Makita, M.; Ninomiya, K.; Fujita, S.; Harada, M.; Yasukawa, M. Identification of a novel WT1-derived peptide which induces human leucocyte antigen-A24-restricted antileukaemia cytotoxic T lymphocytes. Br. J. Haematol., 2002, 116(3), 601-603.
32. Tsuboi, A.; Oka, Y.; Udaka, K.; Murakami, M.; Masuda, T.; Nakano, A.; Nakajima, H.; Yasukawa, M.; Hiraki, A.; Oji, Y.; Kawakami, M.; Hosen, N.; Fujioka, T.; Wu, F.; Taniguchi, Y.; Nishida, S.; Asada, M.; Ogawa, H.; Kawase, I.; Sugiyama, H. Enhanced induction of human WT1-specific cytotoxic T lymphocytes with a 9-mer WT1 peptide modified at HLA-A*2402-binding residues. Cancer Immunol. Immunother., 2002, 51(11-12), 614-620.
33. Gao, L.; Xue, S.A.; Hasserjian, R.; Cotter, F.; Kaeda, J.; Goldman, J.M.; Dazzi, F.; Stauss, H.J. Human cytotoxic T lymphocytes specific for Wilms' tumor antigen-1 inhibit engraftment of leukemia-initiating stem cells in non-obese diabetic-severe combined immunodeficient recipients. Transplantation, 2003, 75(9), 1429-1436.
34. Doubrovina, E.S.; Doubrovin, M.M.; Lee, S.; Shieh, J.H.; Heller, G.; Pamer, E.; O'Reilly, R.J. 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(21), 7207-7219.
35. Koesters, R.; Linnebacher, M.;Coy, J.F.; Germann, A.; Schwitalle, Y.; Findeisen, P.; von Knebel, M.; Doeberitz, M. WT1 is a tumor-associated antigen in colon cancer that can be recognized by in vitro stimulated cytotoxic T cells. Int. J. Cancer, 2004, 109(3), 385-392.
36. Savage, P.; Gao, L.; Vento, K.; Cowburn, P.; Man, S.; Steven, N.; Ogg, G.; McMichael, A.; Epenetos, A.; Goulmy, E.; Stauss, H.J. Use of B cell-bound HLA-A2 class I monomers to generate high-avidity, allo-restricted CTLs against the leukemia-associated protein Wilms tumor antigen. Blood, 2004, 103(12), 4613-4615.
37. Li, Z.; Oka, Y.; Tsuboi, A.; Masuda, T.; Tatsumi, N.; Kawakami, M.; Fujioka, T.; Sakaguchi, N.; Nakajima, H.; Fujiki, F.; Udaka, K.; Oji, Y.; Kawase, I.; Sugiyama, H. WT1 235, a ninemer peptide derived from Wilms' tumor gene product, is a candidate peptide for the vaccination of HLA-A*0201- positive patients with hematopoietic malignancies. Int. J. Hematol., 2005, 82(5), 458-459.
38. Pinilla-Ibarz, J.; May, R.J.; Korontsvit, T.; Gomez, M.; Kappel, B.; Zakhaleva, V.; Zhang, R.H.; Scheinberg, D.A. Improved human T-cell responses against synthetic HLA-0201 analog peptides derived from the WT1 oncoprotein. Leukemia, 2006, 20(11), 2025-2033.
39. Rammensee, H.G..; Friede, T.; Stevanoviic, S. MHC ligands and peptide motifs: first listing. Immunogenetics, 1995, 41(4), 178-228.
40. 187 as an HLA-A*0206-restricted, WT1-specific CTL epitope. Microbiol. Immunol., 2008, 52(11), 551-558.
41. Asemissen, A.M.; Keilholz, U.; Tenzer, S.; Müller, M.; Walter, S.; Stevanovic, S.; Schild, H.; Letsch, A.; Thiel, E.; Rammensee, HG..; Scheibenbogen, C. Identification of a highly immunogenic HLA-A*01-binding T cell epitope of WT1. Clin. Cancer Res., 2006, 12(24), 7476-7482.
42. Knights, A.J.; Zaniou, A.; Rees, R.C.; Pawelec, G.; Müller, L. Prediction of an HLA-DR-binding peptide derived from Wilms' tumour 1 protein and demonstration of in vitro immunogenicity of WT1(124-138)-pulsed dendritic cells generated according to an optimised protocol. Cancer Immunol. Immunother., 2002, 51(5), 271-281.
43. Müller, L.; Knights, A.; Pawelec, G. Synthetic peptides derived from the Wilms' tumor 1 protein sensitize human T lymphocytes to recognize chronic myelogenous leukemia cells. Hematol. J., 2003, 4(1), 57-66.
44. Guo, Y.; Niiya, H.; Azuma T.; Uchida N.; Yakushijin, Y.; Sakai, I.; Hato,T.; Takahashi, M.; Senju S.; Nishimura, Y.; Yasukawa, M. Direct recognition and lysis of leukemia cells by WT1-specific CD4+ T lymphocytes in a HLA class II-restricted manner. Blood, 2005, 106(4), 1415-1418.
45. Kobayashi, H.; Nagato, T.; Aoki, N.; Sato, K.; Kimura, S.; Tateno, M.; Celis, E. Defining MHC class II T helper epitopes for WT1 tumor antigen. Cancer Immunol. Immunother., 2006, 55(7), 850-860.
46. Fujiki, F.; Oka, Y.; Tsuboi, A.; Kawakami, M.; Kawakatsu, M.; Nakajima, H.; Elisseeva, O.A.; Harada, Y.; Ito, K.; Li, Z.; Tatsumi, N.; Sakaguchi, N.; Fujioka, T.; Masuda, T.; Yasukawa, M.; Udaka, K.; Kawase, I.; Oji, Y.; Sugiyama, H. Identification and characterization of a WT1(Wilms' tumor gene) protein-derived HLADRB1* 0405-restricted 16-mer helper peptide that promotes the induction and activation of WT1-specific cytotoxic T lymphocytes. J. Immunother., 2007, 30(3), 282-293.
47. + T cells that recognize and kill human malignant mesothelioma tumor cells. Clin. Cancer Res., 2007, 13(15), 4547-4555.
48. + T cells. Microbiol. Immunol., 2008, 52(12), 591-600.
49. Phan, G.Q.; Touloukian, C.E.; Yang, J.C.; Restifo, N.P.; Sherry, R.M.; Hwu, P.; Topalian, S.L.; Schwartzentruber, D.J.; Seipp, C.A.; Freezer, L.J.; Morton, K.E.; Mavroukakis, S.A.; White, D.E.; Rosenberg, S.A. Immunization of patients with metastatic melanoma using both class I- and class II-restricted peptides from melanoma-associated antigens. J. Immunother., 2003, 26(4), 349-356.
50. Khong, H.T.; Yang, J.C.; Topalian, S.Z.; Sherry, R.M.; Mavroukakis, S.A.; White, D.E.; Rosenberg, S.A. Immunization of HLAA* 0201 and/or HLA-DPbeta1*04 patients with metastatic melanoma using epitopes from the NY-ESO-1 antigen. J. Immunother., 2004, 27(6), 472-477.
51. Slingluff, C.L.Jr; Petroni, G.R.; Olson, W.; Czarkowski, A.; Grosh, W.W.; Smolkin, M.; Chianese-Bullock, K.A.; Neese, P.Y.; Deacon, D.H.; Nail, C.; Merrill, P.; Fink, R.; Patterson, J.W.; Rehm, P.K. Helper T-cell responses and clinical activity of a melanoma vaccine with multiple peptides from MAGE and melanocytic differentiation antigens. J. Clin. Oncol., 2008, 26(30), 4973-4980.
52. + Regulatory T Cells: Implications for Immunotherapy. Cancer Res., 2008, 68(15), 6350-6359.
53. Oka, Y.; Tsuboi, A.; Elisseeva, O.A.; Nakajima, H.; Fujiki, F.; Kawakami, M.; Shirakata, T.; Nishida, S.; Hosen, N.; Oji, Y.; Kawase, I.; Sugiyama, H. WT1 Peptide Cancer Vaccine for Patients with Hematopoietic Malignancies and Solid Cancers. TheSientificWorldJournal, 2007, 7, 649-665.
54. Hori, A.; Kami, M.; Kim, S-W.; Murashige, N.; Sakiyama, M.; Kojima, R.; Hamaki, T.; Makimoto, A.; Miyakoshi, S.; Masuo, S.; Taniguchi, S.; Kunitoh, H.; Takaue, Y. Urgent need for a validated tumor response evaluation system for use in immunotherapy. Bone Marrow Transplant., 2004, 33(2), 255-256.
55. Kawakami, M.; Oka, Y.; Tsuboi, A.; Harada, Y.; Elisseeva, O.A.; Furukawa, Y.; Tsukaguchi, M.; Shirakata, T.; Nishida, S.; Nakajima, H.; Morita, S.; Sakamoto, J.; Kawase, I.; Oji, Y.; Sugiyama, H. Clinical and immunological responses to very low-dose vaccination with WT1 peptide( 5μg/body) in a patient with chronic myelomonocytic leukemia. Int. J. Hematol., 2007, 85(5), 426-429.
56. Tsuboi, A.; Oka, Y.; Nakajima, H.; Fukuda, Y.; Elisseeva, O.A.; Yoshihara, S.; Hosen, N.; Ogata, A.; Kito, K.; Fujiki, F.; Nishida, S.; Shirakata, T.; Ohno, S.; Yasukawa, M.; Oji, Y.; Kawakami, M.; Morita, S.; Sakamoto, J.; Udaka, K.; Kawase, I.; Sugiyama, H. Wilms tumor gene WT1 peptide-based immunotherapy induced a minimal response in a patient with advanced, therapy-resistant multiple myeloma. Int. J. Hematol., 2007, 86(5), 414-417.
57. + T cells in disease-free melanoma patients before and after boosting immunization. Clin. Cancer Res., 2008, 14(16), 5270-5283.
58. Oka Y, Udaka K, Tsuboi A, Elisseeva OA, Ogawa H, Aozasa K, Kishimoto T, Sugiyama H. Cancer immunotherapy targeting wilms' tumor gene WT1 product. J. Immunol., 2000, 164(4), 1873-1880.
59. Tsuboi, A., Oka, Y.; Ogawa, H.; Elisseeva, O.A.; Li, H.; Kawasaki, K.; Aozasa, K.; Kishimoto, T.; Udaka, K.; Sugiyama, H. Cytotoxic T-lymphocyte responses elicited to Wilms' tumor gene WT1 product by DNA vaccination. J. Clin. Immunol., 2000, 20(3), 195-202.
60. Nakajima, H.; Kawasaki, K.; Oka, Y.; Tsuboi, A.; Kawakami, M.; Ikegame, K.; Hoshida, Y.; Fujiki, F.; Nakano, A.; Masuda, T.; Wu, F.; Taniguchi, Y.; Yoshihara, S.; Elisseeva, O.A.; Oji, Y.; Ogawa, H.; Azuma, I.; Kawase, I.; Aozasa, K.; Sugiyama, H. WT1 peptide vaccination combined with BCG-CWS is more efficient for tumor eradication than WT1 peptide vaccination alone. Cancer Immunol. Immunother., 2004, 53(7), 617-624.
61. Yano, A.; Komatsu, T.; Ishibashi, M.; Udaka, K. Potent CTL induction by a whole cell pertussis vaccine in anti-tumor peptide immunotherapy. Microbiol. Immunol., 2007, 51(7), 685-699.
62. Ramirez, F.; Ghani, Y.; Gao L.; Stauss, H. Dendritic cell immunization induces nonprotective WT1-specific CTL responses in mouse. J. Immunother., 2007, 30(2), 140-149.
63. Oka, Y.; Tsuboi, A.; Murakami, M.; Hirai, M.; Tominaga, N.; Nakajima, H.; Elisseeva, O.A.; Masuda, T.; Nakano, A.; Kawakami, M.; Oji, Y.; Ikegame, K.; Hosen, N.; Udaka, K.; Yasukawa, M.; Ogawa, H.; Kawase, I.; Sugiyama, H. Wilms tumor gene peptide-based immunotherapy for patients with overt leukemia from myelodysplastic syndrome (MDS) or MDS with myelofibrosis. Int. J. Hematol., 2003, 78(1), 56-61.
64. Mailaender, V.; Scheibenbogen, C.; Thiel, E.; Letsch, A.; Blau, I.W.; Keilholz, U. Complete remission in a patient with recurrent acute myeloid leukemia induced by vaccination with WT1 peptide in the absence of hematological or renal toxicity. Leukemia, 2004, 18(1), 165-166.
65. Tsuboi, A.; Oka, Y.; Osaki, T.; Kumagai, T.; Tachibana, I.; Hayashi, S.; Murakami, M.; Nakajima, H.; Elisseeva, O.A.; Wu, F.; Masuda, T.; Yasukawa, M.; Oji, Y.; Kawakami, M.; Hosen, N.; Ikegame, K.; Yoshihara, S.; Udaka, K.; Nakatsuka, S.; Aozasa, K.; Kawase, I.; Sugiyama, H. WT1 peptide-based immunotherapy for patients with lung cancer : report of two cases. Microbiol. Immunol., 2004, 48(3), 175-184.
66. Oka, Y.; Tsuboi, A.; Taguchi, T.; Osaki, T.; Kyo, T.; Nakajima, H.; Elisseeva, O.A.; Oji, Y.; Kawakami, M.; Ikegame, K.; Hosen, N.; Yoshihara, S.; Wu, F.; Fujiki, F.; Murakami, M.; Masuda, T.; Nishida, S.; Shirakata, T.; Nakatsuka, S.; Sasaki, A.; Udaka, K.; Dohy, H.; Aozasa, K.; Noguchi, S.; Kawase, I.; Sugiyama, H. Induction of WT1 (Wilms' tumor gene )-specific cytotoxic T lymphocytes by WT1 peptide vaccine and the resultant cancer regression. Proc. Natl. Acad. Sci. USA, 2004, 101(38), 13885-13890.
67. Morita, S.; Oka, Y.; Tsuboi, A.; Kawakami, M.; Maruno, M.; Izumoto, S.; Osaki, T.; Taguchi, T.; Ueda, T.; Myoui, A.; Nishida, S.; Shirakata, T.; Ohno, S.; Oji, Y.; Aozasa, K.; Hatazawa, J.; Udaka, K.; Yoshikawa, H.; Yoshimine, T.; Noguchi, S.; Kawase, I.; Nakatsuka, S.; Sugiyama, H.; Sakamoto, J. A Phase I/II Trial of a WT1(Wilms' tumor gene) peptide vaccine in patients with solid malignancy : Safety assessment based on the phase I data. Jpn. J. Clin. Oncol., 2006, 36(4), 231-236.
68. Iiyama, T.; Udaka, K.; Takeda, S.; Takeuchi, T.; Adachi, Y.C.; Ohtsuki, Y.; Tsuboi, A.; Nakatsuka, S.; Elisseeva, O.A. Oji, Y.; Kawakami, M.; Nishida, S.; Shirakata, T.; Oka, Y.; Shuin, T.; Sugiyama, H. WT1 (Wilms' Tumor 1) peptide immunotherapy for renal cell carcinoma. Microbiol., Immunol., 2007, 51(5), 519-530.
69. Rezvani, K.; Yong, A.S.; Mielke, S.; Savani, B.N.; Musse, L.; Superata, J.; Jafarpour, B.; Boss, C.; Barrett, A.J. Leukemia-associated antigen-specific T-cell responses following combined PR1 and WT1 peptide vaccination in patients with myeloid malignancies. Blood, 2008, 111(1), 236-242.
70. Izumoto, S.; Tsuboi, A.; Oka, Y.; Suzuki, T.; Hashiba, T.; Kagawa, N.; Hashimoto, N.; Maruno, M.; Elisseeva, O.A.; Shirakata, T.; Kawakami, M.; Oji, Y.; Nishida, S.; Ohno, S.; Nakatsuka, S-I.; Kawase, I.; Aozasa, K.; Hatazawa, J.; Morita, S.; Sakamoto, J.; Sugiyama, H.; Yoshimine, T. Phase II clinical trial of Wilms tumor 1 peptide vaccination for patients with recurrent glioblastoma. J. Neurosurg., 2008, 108(5), 963-971.
71. Kitawaki, T.; Kadowaki, N.; Kondo, T.; Ishikawa, T.; Ichinohe, T.; Teramukai, S.; Fukushima, M.; Kasai, Y.; Maekawa, T.; Uchiyama, T. Potential of dendritic-cell immunotherapy for relapse after allogeneic hematopoietic stem cell transplantation, shown by WT1 peptide- and keyhole-limpet-hemocyanin- pulsed, donor-derived dendritic-cell vaccine for acute myeloid leukemia. Am. J. Hematol. 2008, 83(4), 315-317.
72. Ohta, H.; Hashii, Y.; Yoneda, A.; Takizawa, S.; Kusuki, S.; Tokimasa, S.; Fukuzawa, M.; Tsuboi, A.; Murao, A.; Oka, Y.; Oji, Y.; Aozasa, K.; Nakatsuka, S.; Sugiyama, H.; Ozono, K. WT1 (Wilms Tumor 1) peptide immunotherapy for childhood rhabdomyosarcoma: A Case Report. Pediatr. Hematol. Oncol., 2009, 26(1), 74-83.
73. Yasukawa, M.; Fujiwara H.; Ochi T.; Suemori K.; Narumi, H.; Azuma, T.; Kuzushima, K. Clinical efficacy of WT1 peptide vaccination in patients with acute myelogenous leukemia and myelodysplastic syndrome. Am. J. Hematol., 2009, 84(5), 314-315.
74. Keilholz, U.; Letsch, A.; Busse, A.; Asemissen, A.M.; Bauer, S.; Blau, I.W.; Hofmann, W-K.; Uharek, L.; Tiehl, E., Scheibenbogen, C. A clinical and immunological phase II trial of Wilms tumor gene product 1 (WT1) peptide vaccination in patients with AML and MDS. Blood, 2009, 113(26), 6541-6548.
75. Azuma, T.; Otsuki, T.; Kuzushima, K.; Froelich, C.J.; Fujita, S.; Yasukawa, M. Myeloma cells are highly sensitive to the granule exocytosis pathway mediated by WT1-specific cytotoxic T lymphocytes. Clin. Cancer Res., 2004, 10(21), 7402-7412.
76. Noguchi, M,; Itoh, K.; Suekane, S.; Yao, A.; Suetsugu, N.; Katagiri, K.; Yamada, A.; Yamana, H.; Noda, S. Phase I trial of patient-oriented vaccination in HLA-A2-positive patients with metastatic hormone-refractory prostate cancer. Cancer Sci., 2004, 95(1), 77-84.
77. Bocchia, M.; Gentili, S.; Abruzzese, E.; Fanelli, A.; Iiuliano, F.; Tabilio, A.; Amabile, M.; Forconi, F.; Gozzetti, A.; Raspadori, D.; Amadori, S.; Lauria, F. Effect of a p210 multipeptide vaccine associated with imatinib or interferon in patients with chronic myeloid leukaemia and persistent residual disease: a multicentre observational trial. Lancet, 2005, 365(9460), 657-662.
78. Chong G, Morse MA. Combining cancer vaccines with chemotherapy. Expert. Opin. Pharmacother., 2005, 6(16), 2813-2820.
79. Suzuki, E.; Kapoor. V.; Jassar, A.S.; Kaiser, L.R.; Albelda, S.M. Gemcitabine selectively eliminates slpenic Gr-1+/CD11b+ myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin. Cancer Res., 2005, 11(18), 6713-6721.
80. Drakos, E.; Rassidakis, G.Z.; Tsioli, P.; Lai, R.; Jones, D.; Medeiros, L.J. Differential expression of WT1 gene product in non-Hodgkin lymphomas. Appl. Immunohistochem. Mol. Morphol., 2005, 13(2), 132-137.
81. Busse, A.; Gökbuget, N.; Siehl, J.M.; Hoelzer, D.; Schwartz, S.; Rietz, A.; Thiel, E.; Keilholz, U. Wilms' tumor gene 1 (WT1) expression in subtypes of acute lymphoblastic leukemia (ALL) of adults and impact on clinical outcome. Ann. Hematol., 2009, (in press).
82. Oji, Y.; Miyoshi, S.; Maeda, H.; Hayashi, S.; Tamaki, H.; Nakatsuka, S.; Yao, M.; Takahashi, E.; Nakano. Y.; Hirabayashi, H.; Shintani, Y.; Oka, Y.; Tsuboi, A.; Hosen, N.; Asada, M.; Fujioka, T.; murakami. M.; Kanato, K.; Motomura, M.; Kim, E.H.; Kawakami, M.; Ikegame, K.; Ogawa, H.; Aozasa, K.; Kawase, I.; Sugiyama, H. Over expression of the Wilims' tumor gene WT1 in de novo lung cnacers. Int. J. Cancer, 2002, 100(3), 297-303.
83. Oji, Y.; Suzuki, T.; Nakano, Y.; Maruno, M.; Nakatsuka, S.; Jomgeow, T.; Abeno, S.; Tatsumi, N.; Yokota, A.; Aoyagi, S.; Nakazawa, T.; Ito, K.; Kanato, K.; Shirakata, T.; Nishida, S.; hosen, N.; kawakami, M.; Tsuboi, A.; Oka, Y.; Aozasa, K.; Yoshimine, T.; Sugiyama, H. Overexpression of the Wilms' tumor gene WT1 in primary astrocytic tumors. Cancer Sci., 2004, 95(10), 822-827.
84. Barbaric, D.; Corthals, S.L.; Jastaniah, W.A.; Asalanian, S.; Shimizu, H.; Reid, G..S.; Schultz, K.R. Detection of WT1-specific T cells in paediatric acute lymphoblastic leukaemia patients in first remission. Br. J. Haematol., 2008, 141(2), 271-273.
85. Traggiai, E.; Chicha, L.; Mazzucchelli, L.; Bronz, L.; Piffaretti, J.C.; Lanzavecchia, A.; Manz, M.G. Development of a human adaptive immune system in cord blood cell-transplanted mice. Science, 2004, 304(5667), 104-107.
86. Koyanagi, Y.; Tanaka, Y.; Ito, M.; Yamamoto, N. Humanized mice for human retrovirus infection. Curr. Top. Microbiol. Immunol., 2008, 324, 133-148.
87. Wagner, N.; Michiels, J.F.; Schedl, A.; Wagner, K.D. The Wilms' tumor suppressor WT1 is involved in endomethorial cell proliferation and migration: expression in tumor vessels in vivo. Oncogene, 2008, 27(26), 3662-3672.