Characterization and immunotherapeutic implications for a novel antibody targeting interleukin (IL)-13 Receptor α2

Journal of Biological Chemistry

Volumn 287, Issue 36, 2012, Pages 30215-30227

  Balyasnikova, Irina V ^a   Wainwright, Derek A ^a   Solomaha, Elena ^a   Lee, Gina ^a   Han, Yu ^a   Thaci, Bart ^a   Lesniak, Maciej S ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AFFINITY RECEPTORS; BINDING AFFINITIES; COGNATE LIGANDS; COMPETITIVE BINDING ASSAY; CYTOTOXIC; GLIOBLASTOMA MULTIFORME; GLIOMA CELL LINES; HIGH AFFINITY; HIGH FREQUENCY; HYBRIDOMA CELLS; IN-VIVO; INTERLEUKIN-13 RECEPTOR; MONOCLONAL ANTIBODIES (MAB); N-LINKED GLYCOSYLATION; NATIVE CONFORMATION; NORMAL TISSUE; NUDE MICE; THERAPEUTIC USE; WILD TYPES;

BINDING ENERGY; CELL CULTURE; CLONE CELLS; CLONING; MONOCLONAL ANTIBODIES;

TUMORS;

INTERLEUKIN 13; INTERLEUKIN 13 RECEPTOR ALPHA2; INTERLEUKIN 13 RECEPTOR ALPHA2 MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY; RECOMBINANT INTERLEUKIN 13 RECEPTOR ALPHA1; RECOMBINANT INTERLEUKIN 13 RECEPTOR ALPHA2; RECOMBINANT RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; BINDING AFFINITY; CANCER IMMUNOTHERAPY; CELL SURFACE; CLONE; CONTROLLED STUDY; DRUG RECEPTOR BINDING; DRUG TARGETING; FEMALE; GLIOMA; GLIOMA CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN PROTEIN INTERACTION; SURVIVAL;

ANIMALS; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; ANTIBODIES, NEOPLASM; ANTIBODY AFFINITY; CHO CELLS; CRICETINAE; CRICETULUS; FEMALE; GLIOBLASTOMA; GLYCOSYLATION; HEK293 CELLS; HUMANS; HYBRIDOMAS; INTERLEUKIN-13 RECEPTOR ALPHA2 SUBUNIT; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASM TRANSPLANTATION; TRANSPLANTATION, HETEROLOGOUS;

MURINAE; MUS MUSCULUS;

EID: 84865729739     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.370015     Document Type: Article

References (46)

1. Debinski, W., Obiri, N. I., Powers, S. K., Pastan, I., and Puri, R. K. (1995) Human glioma cells overexpress receptors for interleukin 13 and are extremely sensitive to a novel chimeric protein composed of interleukin 13 and pseudomonas exotoxin. Clin. Cancer Res. 1, 1253-1258
2. Joshi, B. H., Plautz, G. E., and Puri, R. K. (2000) Interleukin-13 receptor αchain: a novel tumor-associated transmembrane protein in primary explants of human malignant gliomas, Cancer Res. 60, 1168-1172
3. Jarboe, J. S., Johnson, K. R., Choi, Y., Lonser, R. R., and Park, J. K. (2007) Expression of interleukin-13 receptor α2 in glioblastoma multiforme: implications for targeted therapies. Cancer Res. 67, 7983-7986
4. Kawakami, K., Terabe, M., Kawakami, M., Berzofsky, J. A., and Puri, R. K. (2006) Characterization of a novel human tumor antigen interleukin-13 receptor α2 chain. Cancer Res. 66, 4434-4442
5. Fujisawa, T., Joshi, B., Nakajima, A., and Puri, R. K. (2009) A novel role of interleukin-13 receptor α2 in pancreatic cancer invasion and metastasis. Cancer Res. 69, 8678-8685
6. Debinski, W., Slagle, B., Gibo, D. M., Powers, S. K., and Gillespie, G. Y. (2000) Expression of a restrictive receptor for interleukin 13 is associated with glial transformation. J. Neurooncol. 48, 103-111
7. Aman, M. J., Tayebi, N., Obiri, N. I., Puri, R. K., Modi, W. S., and Leonard, W. J. (1996) cDNA cloning and characterization of the human interleukin 13 receptor α chain. J. Biol. Chem. 271, 29265-29270
8. Gauchat, J. F., Schlagenhauf, E., Feng, N. P., Moser, R., Yamage, M., Jeannin, P., Alouani, S., Elson, G., Notarangelo, L. D., Wells, T., Eugster, H. P., and Bonnefoy, J. Y. (1997) A novel 4-kb interleukin-13 receptor α mRNA expressed in human B, T, and endothelial cells encoding an alternate type-II interleukin-4/interleukin-13 receptor. Eur. J. Immunol. 27, 971-978
9. Akaiwa, M., Yu, B., Umeshita-Suyama, R., Terada, N., Suto, H., Koga, T., Arima, K., Matsushita, S., Saito, H., Ogawa, H., Furue, M., Hamasaki, N., Ohshima, K., and Izuhara, K. (2001) Localization of human interleukin 13 receptor in non-haematopoietic cells. Cytokine 13, 75-84
10. Rahaman, S. O., Sharma, P., Harbor, P. C., Aman, M. J., Vogelbaum, M. A., and Haque, S. J. (2002) IL-13Rα2, a decoy receptor for IL-13 acts as an inhibitor of IL-4-dependent signal transduction in glioblastoma cells. Cancer Res. 62, 1103-1109
11. Fichtner-Feigl, S., Strober, W., Kawakami, K., Puri, R. K., and Kitani, A. (2006) IL-13 signaling through the IL-13α2 receptor is involved in induction of TGF-β1 production and fibrosis. Nat. Med. 12, 99-106
12. Shimamura, T., Fujisawa, T., Husain, S. R., Joshi, B., and Puri, R. K. (2010) Interleukin 13 mediates signal transduction through interleukin 13 receptor α2 in pancreatic ductal adenocarcinoma: role of IL-13 Pseudomonas exotoxin in pancreatic cancer therapy. Clin. Cancer Res. 16, 577-586
13. Fujisawa, T., Joshi, B. H., and Puri, R. K. (2012) IL-13 regulates cancer invasion and metastasis through IL-13Rα2 via ERK/AP-1 pathway in mouse model of human ovarian cancer. Int. J. Cancer 131, 344-356
14. Murphy, E. V., Zhang, Y., Zhu, W., and Biggs, J. (1995) The human glioma pathogenesis-related protein is structurally related to plant pathogenesis-related proteins and its gene is expressed specifically in brain tumors. Gene 159, 131-135
15. Rich, T., Chen, P., Furman, F., Huynh, N., and Israel, M. A. (1996) RTVP-1, a novel human gene with sequence similarity to genes of diverse species, is expressed in tumor cell lines of glial but not neuronal origin. Gene 180, 125-130
16. Stupp, R., Mason, W. P., van den Bent, M. J., Weller, M., Fisher, B., Taphoorn, M. J., Belanger, K., Brandes, A. A., Marosi, C., Bogdahn, U., Curschmann, J., Janzer, R. C., Ludwin, S. K., Gorlia, T., Allgeier, A., Lacombe, D., Cairncross, J. G., Eisenhauer, E., and Mirimanoff, R. O. (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 352, 987-996
17. Kunwar, S., Prados, M. D., Chang, S. M., Berger, M. S., Lang, F. F., Piepmeier, J. M., Sampson, J. H., Ram, Z., Gutin, P. H., Gibbons, R. D., Aldape, K. D., Croteau, D. J., Sherman, J. W., and Puri, R. K. (2007) Direct intracerebral delivery of cintredekin besudotox (IL13-PE38QQR) in recurrent malignant glioma: a report by the Cintredekin Besudotox Intraparenchymal Study Group. J. Clin. Oncol. 25, 837-844
18. Wykosky, J., Gibo, D. M., Stanton, C., and Debinski, W. (2008) Interleukin- 13 receptor α2, EphA2, and Fos-related antigen 1 as molecular denominators of high-grade astrocytomas and specific targets for combinatorial therapy. Clin. Cancer Res. 14, 199-208
19. Debinski, W., Gibo, D. M., Obiri, N. I., Kealiher, A., and Puri, R. K. (1998) Novel anti-brain tumor cytotoxins specific for cancer cells. Nat. Biotechnol. 16, 449-453
20. Kawakami, M., Kawakami, K., and Puri, R. K. (2002) Intratumor administration of interleukin 13 receptor-targeted cytotoxin induces apoptotic cell death in human malignant glioma tumor xenografts. Mol. Cancer Ther. 1, 999-1007
21. Husain, S. R., and Puri, R. K. (2000) Interleukin-13 fusion cytotoxin as a potent targeted agent for AIDS-Kaposi's sarcoma xenograft. Blood 95, 3506-3513
22. Bartolazzi, A., Nocks, A., Aruffo, A., Spring, F., and Stamenkovic, I. (1996) Glycosylation of CD44 is implicated in CD44-mediated cell adhesion to hyaluronan. J. Cell Biol. 132, 1199-1208
23. Kioi, M., Seetharam, S., and Puri, R. K. (2008) Targeting IL-13Rα2-positive cancer with a novel recombinant immunotoxin composed of a single-chain antibody and mutated Pseudomonas exotoxin. Mol. Cancer Ther. 7, 1579-1587
24. Pini, A., and Bracci, L. (2000) Phage display of antibody fragments. Curr. Protein Pept. Sci. 1, 155-169
25. Ross, J. S., Gray, K., Gray, G. S., Worland, P. J., and Rolfe, M. (2003) Anticancer antibodies. Am. J. Clin. Pathol. 119, 472-485
26. Souriau, C., and Hudson, P. J. (2003) Recombinant antibodies for cancer diagnosis and therapy. Expert Opin. Biol. Ther. 3, 305-318
27. Köhler, G., and Milstein, C. (1975) Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256, 495-497
28. Arima, K., Sato, K., Tanaka, G., Kanaji, S., Terada, T., Honjo, E., Kuroki, R., Matsuo, Y., and Izuhara, K. (2005) Characterization of the interaction between interleukin-13 and interleukin-13 receptors. J. Biol. Chem. 280, 24915-24922
29. Sampson, J. H., Crotty, L. E., Lee, S., Archer, G. E., Ashley, D. M., Wikstrand, C. J., Hale, L. P., Small, C., Dranoff, G., Friedman, A. H., Friedman, H. S., and Bigner, D. D. (2000) Unarmed, tumor-specific monoclonal antibody effectively treats brain tumors. Proc. Natl. Acad. Sci. U.S.A. 97, 7503-7508
30. Kioi, M., Seetharam, S., and Puri, R. K. (2006) N-Linked glycosylation of IL-13Rα2 is essential for optimal IL-13 inhibitory activity. FASEB J. 20, 2378-2380
31. McKenzie, A. N., Culpepper, J. A., de Waal Malefyt, R., Brière, F., Punnonen, J., Aversa, G., Sato, A., Dang, W., Cocks, B. G., and Menon, S. (1993) Interleukin 13, a T-cell-derived cytokine that regulates human monocyte and B-cell function. Proc. Natl. Acad. Sci. U.S.A. 90, 3735-3739
32. Donaldson, D. D., Whitters, M. J., Fitz, L. J., Neben, T. Y., Finnerty, H., Henderson, S. L., O'Hara, R. M., Jr., Beier, D. R., Turner, K. J., Wood, C. R., and Collins, M. (1998) The murine IL-13 receptor α2: molecular cloning, characterization, and comparison with murine IL-13 receptor α1. J. Immunol. 161, 2317-2324
33. Hansen, H. J., Goldenberg, D. M., Newman, E. S., Grebenau, R., and Sharkey, R. M. (1993) Characterization of second-generation monoclonal antibodies against carcinoembryonic antigen. Cancer 71, 3478-3485
34. Kuan, C. T., Wikstrand, C. J., Archer, G., Beers, R., Pastan, I., Zalutsky, M. R., and Bigner, D. D. (2000) Increased binding affinity enhances targeting of glioma xenografts by EGFRvIII-specific scFv. Int. J. Cancer 88, 962-969
35. Imperiali, B., and Rickert, K. W. (1995) Conformational implications of asparagine-linked glycosylation. Proc. Natl. Acad. Sci. U.S.A. 92, 97-101
36. Sondermann, P., Huber, R., Oosthuizen, V., and Jacob, U. (2000) The 3.2-Å crystal structure of the human IgG1 Fc fragment-FcγRIII complex. Nature 406, 267-273
37. Krapp, S., Mimura, Y., Jefferis, R., Huber, R., and Sondermann, P. (2003) Structural analysis of human IgG-Fc glycoforms reveals a correlation between glycosylation and structural integrity. J. Mol. Biol. 325, 979-989
38. Fernandes, H., Cohen, S., and Bishayee, S. (2001) Glycosylation-induced conformational modification positively regulates receptor-receptor association: a study with an aberrant epidermal growth factor receptor (EGFR-vIII/ ΔEGFR) expressed in cancer cells. J. Biol. Chem. 276, 5375-5383
39. Hsu, Y. F., Ajona, D., Corrales, L., Lopez-Picazo, J. M., Gurpide, A., Montuenga, L. M., and Pio, R. (2010) Complement activation mediates cetuximab inhibition of non-small cell lung cancer tumor growth in vivo. Mol. Cancer 9, 139
40. Cartron, G., Watier, H., Golay, J., and Solal-Celigny, P. (2004) From the bench to the bedside: ways to improve rituximab efficacy. Blood 104, 2635-2642
41. de Haij, S., Jansen, J. H., Boross, P., Beurskens, F. J., Bakema, J. E., Bos, D. L., Martens, A., Verbeek, J. S., Parren, P. W., van de Winkel, J. G., and Leusen, J. H. (2010) In vivo cytotoxicity of type I CD20 antibodies critically depends on Fc receptor ITAM signaling. Cancer Res. 70, 3209-3217
42. Minn, A. J., Kang, Y., Serganova, I., Gupta, G. P., Giri, D. D., Doubrovin, M., Ponomarev, V., Gerald, W. L., Blasberg, R., and Massagué, J. (2005) Distinct organ-specific metastatic potential of individual breast cancer cells and primary tumors. J. Clin. Investig. 115, 44-55
43. Kawakami, M., Kawakami, K., Kasperbauer, J. L., Hinkley, L. L., Tsukuda, M., Strome, S. E., and Puri, R. K. (2003) Interleukin-13 receptor α2 chain in human head and neck cancer serves as a unique diagnostic marker. Clin. Cancer Res. 9, 6381-6388
44. Husain, S. R., Obiri, N. I., Gill, P., Zheng, T., Pastan, I., Debinski, W., and Puri, R. K. (1997) Receptor for interleukin 13 on AIDS-associated Kaposi's sarcoma cells serves as a new target for a potent Pseudomonas exotoxin-based chimeric toxin protein. Clin. Cancer Res. 3, 151-156
45. Puri, R. K., Leland, P., Obiri, N. I., Husain, S. R., Kreitman, R. J., Haas, G. P., Pastan, I., and Debinski, W. (1996) 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 87, 4333-4339
46. Joshi, B. H., Leland, P., and Puri, R. K. (2003) Identification and characterization of interleukin-13 receptor in human medulloblastoma and targeting these receptors with interleukin-13-Pseudomonas exotoxin fusion protein. Croat. Med. J. 44, 455-462