A novel strategy for tumour therapy combining cell apoptosis and active immunity induced by caspy2, a zebrafish caspase
Correction(s) for this article
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Erratum
- Volume 13Issue 9bJournal of Cellular and Molecular Medicine
- pages: 4084-4084
- First Published online: January 29, 2010
Lei Liu
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
These authors contributed equally to this work.
Search for more papers by this authorCorresponding Author
Hongxin Deng
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
These authors contributed equally to this work.
Correspondence to: Hongxin DENG and Yuquan Wei, State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Ke-yuan Road 4, No.1, Gao-peng Street, Chengdu, Sichuan, 610041, The People’s Republic of China.Tel.: +86–28-85164059Fax: +86–28-85164060E-mail: [email protected], [email protected]Search for more papers by this authorYongsheng Wang
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorPing Chen
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorYang Yang
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorHanshuo Yang
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorXiancheng Chen
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorLijuan Chen
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorWen Zhu
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorShufang Liang
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorJinliang Yang
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorZhiyong Qian
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorJiong Li
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorCorresponding Author
Yanjun Wen
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Correspondence to: Hongxin DENG and Yuquan Wei, State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Ke-yuan Road 4, No.1, Gao-peng Street, Chengdu, Sichuan, 610041, The People’s Republic of China.Tel.: +86–28-85164059Fax: +86–28-85164060E-mail: [email protected], [email protected]Search for more papers by this authorBin Kan
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorYongqiu Mao
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorXia Zhao
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorYuquan Wei
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorLei Liu
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
These authors contributed equally to this work.
Search for more papers by this authorCorresponding Author
Hongxin Deng
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
These authors contributed equally to this work.
Correspondence to: Hongxin DENG and Yuquan Wei, State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Ke-yuan Road 4, No.1, Gao-peng Street, Chengdu, Sichuan, 610041, The People’s Republic of China.Tel.: +86–28-85164059Fax: +86–28-85164060E-mail: [email protected], [email protected]Search for more papers by this authorYongsheng Wang
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorPing Chen
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorYang Yang
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorHanshuo Yang
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorXiancheng Chen
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorLijuan Chen
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorWen Zhu
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorShufang Liang
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorJinliang Yang
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorZhiyong Qian
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorJiong Li
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorCorresponding Author
Yanjun Wen
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Correspondence to: Hongxin DENG and Yuquan Wei, State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Ke-yuan Road 4, No.1, Gao-peng Street, Chengdu, Sichuan, 610041, The People’s Republic of China.Tel.: +86–28-85164059Fax: +86–28-85164060E-mail: [email protected], [email protected]Search for more papers by this authorBin Kan
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorYongqiu Mao
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorXia Zhao
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorYuquan Wei
State Key Laboratory of Biotherapy, West China Hospital and College of Life Science, Sichuan University, Chengdu, Sichuan, The People’s Republic of China
Search for more papers by this authorAbstract
Caspy2, a zebrafish protease, is an active caspase for inducing apoptosis in mammalian cells. To investigate whether caspy2-mediated apoptosis could be used in cancer therapy, its cDNA was amplified and cloned into eukaryotic expression vector pcDNA3.1+. The recombinant plasmid was mixed with cationic liposome and introduced into various tumour cell lines in vitro. Our data showed that caspy2 induced remarkable apoptosis of cancer cells in vitro. Treatment of mice-bearing CT26 colon carcinoma or MethA fibrosarcoma with intratumoral injection of liposome-caspy2 plasmid complex resulted in substantial killing of neoplastic cells and long-term survivors. Apoptotic cells were widely distributed in caspy2-treated tumour tissue. Infiltration of CD8+ T lymphocyte was also observed apparently in the tumour tissue after the treatment with caspy2. Tumour-specific major histocompatibility complex (MHC) class I-dependent CD8+ cytotoxic T lymphocyte activity was found by means of 51Cr release assay. In MethA model, the mice acquired a long-time protective immunity against the parental tumour cell re-challenge. These results indicated that caspy2 can act as both apoptosis inducer and immune response initiator, which may account for its extraordinary antitumour effect. Furthermore, in vivo depletion of CD8+ T lymphocytes could completely abrogate the antitumour immune activity, whereas the depletion of CD4+ cells showed partial abrogation. In this study, we developed a novel anticancer strategy that combines both induction of apoptosis and immune response in mice-bearing tumours with a single caspy2 gene. This approach may provide an important way for treatment of cancer.
References
- 1 Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer . 1972; 26: 239–57.
- 2 Savill J, Fadok V. Corpse clearance defines the meaning of cell death. Nature . 2000; 407: 784–8.
- 3 Bhutia S, Maiti TK. Targeting tumors with peptides from natural sources. Trends Biotechnol . 2008; 26: 210–7.
- 4 Call JA, Eckhardt SG, Camidge DR. Targeted manipulation of apoptosis in cancer treatment. Lancet Oncol . 2008; 9: 1002–11.
- 5 Brown JM, Attardi LD. The role of apoptosis in cancer development and treatment response. Nat Rev Cancer . 2005; 5: 231–7.
- 6 Thompson CB. Apoptosis in the pathogenesis and treatment of disease. Science . 1995; 267: 1456–62.
- 7 Bellamy CO, Malcomson RD, Harrison DJ, et al . Cell death in health and disease: the biology and regulation of apoptosis. Semin Cancer Biol . 1995; 6: 3–16.
- 8 Lauber K, Blumenthal SG, Waibel M, et al . Clearance of apoptotic cells: getting rid of the corpses. Mol Cell . 2004; 14: 277–87.
- 9 Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature . 1998; 392: 245–52.
- 10 Albert ML, Sauter B, Bhardwaj N. Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature . 1998; 392: 86–9.
- 11 Bellone M, Iezzi G, Rovere P, et al . Processing of engulfed apoptotic bodies yields T cell epitopes. J Immunol . 1997; 159: 5391–9.
- 12 Leitner WW, Restifo NP. DNA vaccines and apoptosis: to kill or not to kill J Clin Invest . 2003; 112: 22–4.
- 13 Zitvogel L, Casares N, Péquignot MO, et al . The immune response against dying tumor cells. Adv Immunol . 2004; 84: 131–79.
- 14 Casares N, Pequignot MO, Tesniere A, et al . Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med . 2005; 202: 1691–1701.
- 15 Nowak AK, Lake RA, Marzo AL, et al . Induction of tumor cell apoptosis in vivo increases tumor antigen cross-presentation, cross-priming rather than cross-tolerizing host tumor-specific CD8 T cells. J Immunol . 2003; 170: 4905–13.
- 16 Sasaki S, Amara RR, Oran AE, et al . Apoptosis-mediated enhancement of DNA-raised immune responses by mutant caspases. Nat Biotechnol . 2001; 19: 543–7.
- 17 Hoffmann TK, Meidenbauer N, Dworacki G, et al . Generation of tumor-specific T-lymphocytes by cross-priming with human dendritic cells ingesting apoptotic tumor cells. Cancer Res . 2000; 60: 3542–9.
- 18 Thornberry NA, Lazebnik Y. Caspases: enemies within. Science . 1998; 281: 1312–6.
- 19 Masumoto J, Zhou W, Chen FF, et al . Caspy, a zebrafish caspase, activated by ASC oligomerization is required for pharyngeal arch development. J Biol Chem . 2003; 278: 4268–76.
- 20 Matzinger P. The danger model: a renewed sense of self. Science . 2002; 296: 301–5.
- 21 Ding HF, Fisher DE. Induction of apoptosis in cancer: new therapeutic opportunities. Ann Med . 2002; 34: 451–69.
- 22 Michaeli D. Vaccines and monoclonal antibodies. Semin Oncol . 2005; 32: 82–6.
- 23 Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods . 1983; 65: 55–63.
- 24 Wei YQ, Zhao X, Kariya Y, et al . Induction of autologous tumor killing by heat treatment of fresh human tumor cells: involvement of gamma delta T cells and heat shock protein 70. Cancer Res . 1996; 56: 1104–10.
- 25 Mashino K, Sadanaga N, Tanaka F, et al . Effective strategy of dendritic cell-based immunotherapy for advanced tumor-bearing hosts: the critical role of Th1-dominant immunity. Mol Cancer Ther . 2002; 1: 785–94.
- 26 Takeda K, Yamaguchi N, Akiba H, et al . Induction of tumor-specific T cell immunity by anti-DR5 antibody therapy. J Exp Med . 2004; 199: 437–48.
- 27 Uno T, Takeda K, Kojima Y, et al . Eradication of established tumors in mice by a combination antibody-based therapy. Nat Med . 2006; 12: 693–8.
- 28 Selenko N, Maidic O, Draxier S, et al . CD20 antibody (C2B8)-induced apoptosis of lymphoma cells promotes phagocytosis by dendritic cells and cross-priming of CD8+ cytotoxic T cells. Leukemia . 2001; 15: 1619–26.
- 29 Barczyk K, Kreuter M, Pryjma J, et al . Serum cytochrome c indicates in vivo apoptosis and can serve as a prognostic marker during cancer therapy. Int J Cancer . 2005; 116: 167–73.
- 30 Renz A, Berdel WE, Kreuter M, et al . Rapid extracellular release of cytochrome c is specific for apoptosis and marks cell death in vivo. Blood . 2001; 98: 1542–8.
- 31
Miller JF,
Morahan G,
Allison J.
Extrathimic acquisition of tolerance by T lymphocytes.
Cold Spring Harb Symp Quant Bio
. 1989; 2: 807–13.
10.1101/SQB.1989.054.01.094 Google Scholar
- 32 Chattergoon MA, Kim JJ, Yang JS, et al . Targeted antigen delivery to antigen-presenting cells including dendritic cells by engineered Fas-mediated apoptosis. Nat Biotechnol . 2000; 18: 974–9.
- 33 Plautz GE, Yang ZY, Wu BY, et al . Immunotherapy of malignancy by in vivo gene transfer into tumors. Proc Natl Acad Sci USA . 1993; 90: 4645–9.
- 34 Albert ML, Pearce SF, Francisco LM, et al . Immature dendritic cells phagocytose apoptotic cells via alphavbeta5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J Exp Med . 1998; 188: 1359–68.
- 35 Bennett SR, Carbone FR, Karamalis F, et al . Induction of a CD8+ cytotoxic T lymphocyte response by cross-priming requires cognate CD4+ T cell help. J Exp Med . 1997; 186: 65–70.
- 36 Hu HM, Winter H, Urba WJ, et al . Divergent roles for CD4+ T cells in the priming and effector/memory phases of adoptive immunotherapy. J Immunol . 2000; 165: 4246–53.
- 37 Machy P, Serre K, Baillet M, et al. Induction of MHC class I presentation of exogenous antigen by dendritic cells is controlled by CD4+ T cells engaging class II molecules in cholesterol-rich domains. J Immunol . 2002; 168: 1172–80.
- 38 Pardoll DM, Topalian SL. The role of CD4+ T cell responses in antitumor immunity. Curr Opin Immunol . 1998; 10: 588–94.
- 39 Ossendorp F, Mengede E, Camps M, et al . Specific T helper cell requirement for optimal induction of cytotoxic T lymphocytes against major histocompatibility complex class II negative tumors. J Exp Med . 1998; 187: 693–702.
- 40 Dolan BP, Gibbs KD, Ostrand-Rosenberg S. Tumor-specific CD4+ T cells are activated by “cross-dressed” dendritic cells presenting peptide-MHC class II complexes acquired from cell-based cancer vaccines. J Immunol . 2006; 176: 1447–55.
- 41 Romagnani S. The Th1/Th2 paradigm. Immunol Today . 1997; 18: 263–6.
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