Potent antitumor activity of IL-13 cytotoxin in human pancreatic tumors engineered to express IL-13 receptor α2 chain in vivo

Gene Therapy

Volumn 10, Issue 13, 2003, Pages 1116-1128

  Kawakami, K ^a   Kawakami, M ^a   Husain, S R ^a   Puri, R K ^a  

^a Division of Viral Products   (United States)

Author keywords

Gene transfer; Innate immunity; Nitric oxide; Orthotopic model; Tumor antigen

Indexed keywords

INTERLEUKIN 13 RECEPTOR; LIPOSOME; NITRIC OXIDE; RECOMBINANT INTERLEUKIN 13; RECOMBINANT INTERLEUKIN 2; IL13RA1 PROTEIN, HUMAN; IL13RA1 PROTEIN, MOUSE; IMMUNOTOXIN; INTERLEUKIN 13; INTERLEUKIN 13 RECEPTOR ALPHA1; INTERLEUKIN RECEPTOR; TUMOR ANTIGEN;

ALPHA CHAIN; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; CELL INFILTRATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG POTENTIATION; DRUG SENSITIVITY; GENE DELIVERY SYSTEM; GENE EXPRESSION; GENETIC ENGINEERING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IN VIVO STUDY; LIGAND BINDING; MACROPHAGE; MOUSE; NATURAL KILLER CELL; NEPHROTOXICITY; NONHUMAN; PANCREAS TUMOR; PLASMID; PRIORITY JOURNAL; REVIEW; TUMOR REGRESSION; TUMOR VOLUME; ANIMAL; ARTICLE; BINDING SITE; BIOSYNTHESIS; CANCER TRANSPLANTATION; GENE THERAPY; GENETICS; IMMUNOLOGY; INTRALESIONAL DRUG ADMINISTRATION; MACROPHAGE ACTIVATION; METABOLISM; METHODOLOGY; NUDE MOUSE; RADIOASSAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALIA;

ANIMALS; ANTIGENS, NEOPLASM; BINDING SITES; GENE EXPRESSION; GENE THERAPY; HUMANS; IMMUNOTOXINS; INJECTIONS, INTRALESIONAL; INTERLEUKIN-13; INTERLEUKIN-13 RECEPTOR ALPHA1 SUBUNIT; MACROPHAGE ACTIVATION; MICE; MICE, NUDE; MODELS, ANIMAL; NEOPLASM TRANSPLANTATION; NITRIC OXIDE; PANCREATIC NEOPLASMS; RADIOLIGAND ASSAY; RECEPTORS, INTERLEUKIN; RECEPTORS, INTERLEUKIN-13; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSFECTION;

EID: 0038262659     PISSN: 09697128     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.gt.3301956     Document Type: Review

References (50)

1. Jemal A, Thomas A, Murray T, Thun M. Cancer statistics 2002. CA Cancer J Clin 2002; 52: 23-47.
2. Lillemoe KD. Current management of pancreatic carcinoma. Ann Surg 1995; 221: 133-148.
3. Giantonio BJ et al. Superantigen-based immunotherapy: a phase I trial of PNU-214565, a monoclonal antibody-staphylococcal enterotoxin A recombinant fusion protein, in advanced pancreatic and colorectal cancer. J Clin Oncol 1997; 15: 1994-2007.
4. Mulvihill S et al. Safety and feasibility of injection with an E1B-55 kDa gene-deleted, replication selective adenovirus (ONYX-015) into primary carcinomas of the pancreas: a phase I trial. Gene Ther 2001; 8: 308-315.
5. Löhr M et al. Microencapsulated cell-mediated treatment of inoperable pancreatic carcinoma. Lancet 2001; 357: 1591-1592.
6. Minty A et al. Interleukin-13 is a new human lymphokine regulating inflammatory and immune responses. Nature 1993; 36: 248-251.
7. Serve H et al. Inhibition of proliferation and clonal growth of human breast cancer cells by interleukin 13. Cancer Res 1996; 56: 3583-3588.
8. Lebel-Binay S et al. Experimental gene therapy of cancer using tumor cells engineered to secrete interleukin-13. Eur J Immunol 1995; 25: 2340-2348.
9. Kawakami M, Leland P, Kawakami K, Puri RK. Mutation and functional analysis of IL-13 receptors in human malignant glioma cells. Oncol Res 2001; 12: 459-467.
10. Obiri NI, Debinski W, Leonard WJ, Puri RK. Receptor for interleukin 13: interaction with interleukin 4 by a mechanism that does not involve the common γ chain shared by receptors for interleukins 2, 4, 7, 9 and 15. J Biol Chem 1995; 270: 8797-8804.
11. Murata T, Obiri NI, Debinski W, Puri RK. Human ovarian carcinoma cell lines express IL-4 and IL-13 receptors: comparison between IL-4- and IL-13-induced signal transduction. Int J Cancer 1997; 70: 230-240.
12. Obiri NI et al. The IL-13 receptor structure differs on various cell types and may share more than one component with IL-4 receptor. J Immunol 1997; 158: 756-764.
13. c chain of the IL-2 receptor. J Biol Chem 1997; 272: 20251-20258.
14. Murata T, Obiri NI, Puri RK. Structure of and signal transduction through interleukin-4 and interleukin-13 receptors. Int J Mol Med 1998; 1: 551-557.
15. Joshi BH, Plautz GE, Puri RK. IL-13 receptor α chain: a novel tumor associated transmembrane protein in primary explants of human malignant gliomas. Cancer Res 2000; 60: 1168-1172.
16. Aman MJ et al. cDNA cloning and characterization of the human interleukin 13 receptor α chain. J Biol Chem 1996; 271: 29265-29270.
17. Hilton DJ et al. Cloning and characterization of a binding subunit of the interleukin-13 receptor that is a component of the interleukin-4 receptor. Proc Natl Acad Sci USA 1996; 93: 497-501.
18. Miloux B et al. Cloning of the human IL-13Rα1 chain and reconstitution with the IL-4Rα of a functional IL-4/IL-13 receptor complex. FEBS Lett 1997; 401: 163-166.
19. Nelms K et al. The IL-4 receptor: signaling mechanisms and biologic functions. Annu Rev Immunol 1999; 17: 701-738.
20. Caput D et al. Cloning and characterization of a specific interleukin (IL)-13 binding protein structurally related to the IL-5 receptor α chain. J Biol Chem 1996; 271: 16921-16926.
21. Donaldson DD et al. The murine IL-13 receptor α2: molecular cloning, characterization, and comparison with murine IL-13 receptor α1. J Immunol 1998; 161: 2317-2324.
22. Kawakami K, Taguchi J, Murata T, Puri RK. The interleukin-13 receptor α2 chain: an essential component for binding and internalization but not for IL-13 induced signal transduction through STAT6 pathway. Blood 2001; 97: 2673-2679.
23. Kawakami K, Takeshita F, Puri RK. Identification of distinct roles for a dileucine and a tyrosine internalization motif in the interleukin-13 binding component IL-13 receptor α2 chain. J Biol Chem 2001; 276: 25114-25120.
24. Murata T, Obiri NI, Debinski W, Puri RK. Structure of IL-13 receptor: analysis of composition in cancer and immune cells. Biochem Biophys Res Commun 1997; 238: 90-94.
25. Husain SR, Puri RK. Interleukin-13 fusion cytotoxin as a potent targeted agent for AIDS-Kaposi's sarcoma xenograft. Blood 2000; 95: 3506-3513.
26. Joshi BH, Kawakami K, Leland P, Puri RK. Heterogeneity of interleukin-13 receptor expression and subunit structure in squamous cell carcinoma of head and neck: differential sensitivity to a chimeric fusion protein comprised of interleukin-13 and a mutated form of Pseudomonas exotoxin. Clin Cancer Res 2002; 8: 1948-1956.
27. Kawakami K, Kawakami M, Joshi BH, Puri RK. Interleukin-13 receptor-targeted cancer therapy in an immunodeficient animal model of human head and neck cancer. Cancer Res 2001; 61: 6194-6200.
28. Murata T, Husain SR, Mohri H, Puri RK. Two different IL-13 receptor chains are expressed in normal human skin fibroblasts, and IL-4 and IL-13 mediate signal transduction through a common pathway. Int Immunol 1998; 10: 1103-1110.
29. Maini A et al. Interleukin-13 receptors on human prostate carcinoma cell lines represent a novel target for a chimeric protein composed of IL-13 and a mutated form of Pseudomonas exotoxin. J Urol 1997; 158: 948-953.
30. Kawakami K, Husain SR, Bright RK, Puri RK. Gene transfer of interleukin-13 receptor α2 chain dramatically enhances the antitumor effect of IL-13 receptor-targeted cytotoxin in human prostate cancer xenografts. Cancer Gene Ther 2001; 8: 861-868.
31. Leland P et al. Human breast carcinoma cells express type II IL-4 receptors and are sensitive to antitumor activity of a chimeric IL-4-Pseudomonas exotoxin fusion protein in vitro and in vivo. Mol Med 2000; 6: 165-178.
32. Debinski W, Obiri NI, Pastan I, Puri RK. A novel chimeric protein composed of interleukin 13 and Pseudomonas exotoxin is highly cytotoxic to human carcinoma cells expressing receptors for interleukin 13 and interleukin 4. J Biol Chem 1995; 270: 16775-16780.
33. Puri RK et al. Targeting of interleukin-13 receptor on human renal cell carcinoma cells by a recombinant chimeric protein composed of interleukin-13 and a truncated form of Pseudomonas exotoxin A (PE38QQR). Blood 1996; 87: 4333-4339.
34. Husain SR, Joshi BH, Puri RK. Interleulin-13 receptor as a unique target for anti-glioblastoma therapy. Int J Cancer 2001; 92: 168-175.
35. Kawakami K, Joshi BH, Puri RK. Sensitization of cancer cells to interleukin 13-Pseudomonas exotoxin-induced cell death by gene transfer of interleukin 13 receptor α chain. Hum Gene Ther 2000; 11: 1829-1835.
36. Puri RK et al. In vitro and in vivo suppression of interleukin-2-activated killer cell activity by chimeric proteins between interleukin-2 and Pseudomonas exotoxin. Cell Immunol 1992; 143: 324-334.
37. Kawakami K, Kawakami M, Husain SR, Puri RK. Targeting interleukin-4 receptors for effective pancreatic cancer therapy Cancer Res 2002; 62: 3575-3580.
38. Terabe M et al. NKT cell-mediated repression of tumor immunosurveillance by IL-13 and the IL-4R-STAT6 pathway Nat Immunol 2000; 1: 515-520.
39. Kawakami K et al. In vivo over-expression of IL-13 receptor α2 chain inhibits tumorigenicity of human breast and pancreatic tumors in immunodeficient mice. J Exp Med 2001; 194: 1743-1754.
40. Kawakami M, Kawakami K, Puri RK. Apoptotic pathways of cell death induced by an interleukin-13 receptor-targeted recombinant cytotoxin in head and neck cancer cells. Cancer Immunol Immunother 2002; 50: 691-700.
41. Kawakami M, Kawakami K, Puri RK. Intratumoral administration of interleukin 13 receptor-targeted cytotoxin induces apoptotic cell death in human malignant glioma tumor xenografts. Mol Cancer Ther 2002; 1: 999-1007.
42. Gold DV, Alisauskas R, Sharkey RM. Targeting of xenografted pancreatic cancer with a new monoclonal antibody, PAM4. Cancer Res 1995; 55: 1105-1110.
43. Frankel AE, Kreitman RJ, Sausville EA. Targeted toxins. Clin Cancer Res 2000; 6: 326-334.
44. Oshima Y, Joshi BH, Puri RK. Conversion of interleukin-13 into a high affinity agonist by a single amino acid substitution. J Biol Chem 2000; 275: 14375-14380.
45. Sanchez GI et al. Immunogenicity and protective efficacy of a Plasmodium yoelii Hsp60 DNA vaccine in BALB/c mice. Infect Immun 2001; 69: 3897-3905.
46. Obiri NI et al. Expression of high affinity interleukin-4 receptors on human renal carcinoma cells and inhibition of tumor growth in vitro by interleukin-4. J Clin Invest 1993; 91: 88-93.
47. Puri RK et al. Expression of high affinity IL4 receptors on murine sarcoma cells and receptor mediated cytotoxicity of tumor cells to chimeric protein between IL-4 and Pseudomonas exotoxin. Cancer Res 1991; 51: 3011-3017.
48. Templeton NS et al. Improved DNA:liposome complexes for increased systemic derivery and gene expression. Nat Biotechnol 1997; 15: 647-652.
49. Bastian NR et al. Induction of iron-derived EPR signals in murine cancers by nitric oxide. J Biol Chem 1994; 269: 5127-5131.
50. Yim C-Y et al. Nitric oxide synthesis contributes to IL-2-induced antitumor responses against intraperitoneal Meth A tumor. J Immunol 1995; 155: 4382-4390.