N-linked glycosylation of IL-13Rα2 is essential for optimal IL-13 inhibitory activity

FASEB Journal

Volumn 20, Issue 13, 2006, Pages

  Kioi, Mitomu ^a   Seetharam, Saraswathy ^a   Puri, Raj K ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

Author keywords

Allergic and inflammatory diseases; Cancer; ECD; Type I cytokine receptor

Indexed keywords

HYBRID PROTEIN; INTERLEUKIN 13; INTERLEUKIN 13 RECEPTOR ALPHA2; MONOMER; STAT6 PROTEIN; IL13RA1 PROTEIN, HUMAN; INTERLEUKIN 13 RECEPTOR ALPHA1; PRIMER DNA; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; BIOLOGICAL ACTIVITY; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DEGLYCOSYLATION; ESCHERICHIA COLI; GLYCOSYLATION; HUMAN; HUMAN CELL; ISOTOPE LABELING; LYMPHOMA CELL LINE; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; ANIMAL; CELL DIVISION; CELL LINE; CELL STRAIN COS1; CELL SURVIVAL; CERCOPITHECUS; DRUG EFFECT; GENETICS; MOLECULAR CLONING; MOUSE; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PLASMID; RETROVIRUS;

ESCHERICHIA COLI; MAMMALIA;

ANIMALS; BASE SEQUENCE; CELL DIVISION; CELL LINE; CELL SURVIVAL; CERCOPITHECUS AETHIOPS; CLONING, MOLECULAR; COS CELLS; DNA PRIMERS; GLYCOSYLATION; HUMANS; INTERLEUKIN-13; INTERLEUKIN-13 RECEPTOR ALPHA1 SUBUNIT; MICE; PLASMIDS; RECOMBINANT PROTEINS; RETROVIRIDAE;

EID: 33845608432     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-5995fje     Document Type: Article

References (41)

1. De Vries, J. E. (1998) The role of IL-13 and its receptor in allergy and inflammatory responses. J. Allergy Clin. Immunol. 102, 165-169
2. Wynn, T. A. (2003) IL-13 effector functions. Annu. Rev. Immunol. 21, 425-456
3. Kelly-Welch, A. E., Hanson, E. M., Boothby, M. R., and Keegan, A. D. (2003) Interleukin-4 and interleukin-13 signaling connections maps. Science 300, 1527-1528
4. Zhu, Z., Homer, R. J., Wang, Z., Chen, Q., Geba, G. P., Wang, J., Zhang, Y., and Elias, J. A. (1999) Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J. Clin. Invest. 103, 779-788
5. Wills-Karp, M., Luyimbazi, J., Xu, X., Schofield, B., Neben, T. Y., Karp, C. L., and Donaldson, D. D. (1998) Interleukin-13: central mediator of allergic asthma. Science 282, 2258-2261
6. Grunig, G., Warnock, M., Wakil, A. E., Venkayya, R., Brombacher, F., Rennick, D. M., Sheppard, D., Mohrs, M., Donaldson, D. D., Locksley, R. M., et al. (1998) Requirement for IL-13 independently of IL-4 in experimental asthma. Science 282, 2261-2263
7. Aversa, G., Punnonen, J., Cocks, B. G., de Waal Malefytqq, R., Vega, F., Jr., Zurawski, S. M., Zurawski, G., and de Vries, J. E. (1993) An interleukin 4 (IL-4) mutant protein inhibits both IL-4 or IL-13-induced human immunoglobulin G4 (IgG4) and IgE synthesis and B cell proliferation: support for a common component shared by IL-4 and IL-13 receptors. J. Exp. Med. 178, 2213-2218
8. Lefort, S., Vita, N., Reeb, R., Caput, D., and Ferrara, P. (1995) IL-13 and IL-4 share signal transduction elements as well as receptor components in TF-1 cells. FEBS Lett. 366, 122-126
9. Hilton, D. J., Zhang, J. G., Metcalf, D., Alexander, W. S., Nicola, N. A., and Willson, T. A. (1996) Cloning and characterization of a binding subunit of the interleukin 13 receptor that is also a component of the interleukin 4 receptor. Proc. Natl. Acad. Sci. U. S. A. 93, 497-501
10. 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 alpha chain. J. Biol. Chem. 271, 29265-29270
11. Caput, D., Laurent, P., Kaghad, M., Lelias, J. M., Lefort, S., Vita, N., and Ferrara, P. (1996) Cloning and characterization of a specific interleukin (IL)-13 binding protein structurally related to the IL-5 receptor alpha chain. J. Biol. Chem. 271, 16921-16926
12. 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., et al. (1998) The murine IL-13 receptor alpha 2: molecular cloning, characterization, and comparison with murine IL-13 receptor alpha 1. J. Immunol. 161, 2317-2324
13. Kawakami, K., Takeshita, F., and Puri, R. K. (2001) Identification of distinct roles for a dileucine and a tyrosine internalization motif in the interleukin (IL)-13 binding component IL-13 receptor alpha 2 chain. J. Biol. Chem. 276, 25114-25120
14. Kawakami, K., Taguchi, J., Murata, T., and Puri, R. K. (2001) The interleukin-13 receptor alpha2 chain: an essential component for binding and internalization but not for interleukin-13-induced signal transduction through the STAT6 pathway. Blood 97, 2673-2679
15. Rahaman, S. O., Sharma, P., Harbor, P. C., Aman, M. J., Vogelbaum, M. A., and Haque, S. J. (2002) IL-13R(alpha)2, a decoy receptor for IL-13 acts as an inhibitor of IL-4-dependent signal transduction in glioblastoma cells. Cancer Res. 62, 1103-1109
16. Rahaman, S. O., Vogelbaum, M. A., and Haque, S. J. (2005) Aberrant Stat3 signaling by interleukin-4 in malignant glioma cells: involvement of IL-13Ralpha2. Cancer Res. 65, 2956-2963
17. Obiri, N. I., Hillman, G. G., Haas, G. P., Sud, S., and Puri, R. K. (1993) Expression of high affinity interleukin-4 receptors on human renal cell carcinoma cells and inhibition of tumor cell growth in vitro by interleukin-4. J. Clin. Invest. 91, 88-93
18. Murata, T., Obiri, N. I., Debinski, W., and Puri, R. K. (1997) Structure of IL-13 receptor: analysis of subunit composition in cancer and immune cells. Biochem. Biophys. Res. Commun. 238, 90-94
19. Kioi, M., Kawakami, K., and Puri, R. K. (2004) Analysis of antitumor activity of an interleukin-13 (IL-13) receptor-targeted cytotoxin composed of IL-13 antagonist and Pseudomonas exotoxin. Clin. Cancer Res. 10, 6231-6238
20. Kioi, M., Kawakami, K., and Puri, R. K. (2004) Mechanism of action of interleukin-13 antagonist (IL-13E13K) in cells expressing various types of IL-4R. Cell. Immunol. 229, 41-51
21. Kitamura, T., Tojo, A., Kuwaki, T., Chiba, S., Miyazono, K., Urabe, A., and Takaku, F. (1989) Identification and analysis of human erythropoietin receptors on a factor-dependent cell line, TF-1. Blood 73, 375-380
22. Debinski, W., Obiri, N. I., Pastan, I., and Puri, R. K. (1995) 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. 270, 16775-16780
23. Oshima, Y., and Puri, R. K. (2001) Characterization of a powerful high affinity antagonist that inhibits biological activities of human interleukin-13. J. Biol. Chem. 276, 15185-15191
24. 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
25. Joshi, B. H., Plautz, G. E., and Puri, R. K. (2000) Interleukin-13 receptor alpha chain: a novel tumor-associated transmembrane protein in primary explants of human malignant gliomas. Cancer Res. 60, 1168-1172
26. 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
27. Kawakami, K., Kawakami, M., Joshi, B. H., and Puri, R. K. (2001) Interleukin-13 receptor-targeted cancer therapy in an immunodeficient animal model of human head and neck cancer. Cancer Res. 61, 6194-6200
28. Ding, D. X., Vera, J. C., Heaney, M. L., and Golde, D. W. (1995) N-glycosylation of the human granulocyte-macrophage colonystimulating factor receptor alpha subunit is essential for ligand binding and signal transduction. J. Biol. Chem. 270, 24580-24584
29. Cole, A. R., Hall, N. E., Treutlein, H. R., Eddes, J. S., Reid, G. E., Moritz, R. L., and Simpson, R. J. (1999) Disulfide bond structure and N-glycosylation sites of the extracellular domain of the human interleukin-6 receptor. J. Biol. Chem. 274, 7207-7215
30. Bastian, W., Zhu, J., Way, B., Lockwood, D., and Livingston, J. (1993) Glycosylation of Asn397 or Asn418 is required for normal insulin receptor biosynthesis and processing. Diabetes 42, 966-974
31. Niu, L., Heaney, M. L., Vera, J. C., and Golde, D. W. (2000) High-affinity binding to the GM-CSF receptor requires intact N-glycosylation sites in the extracellular domain of the beta subunit. Blood 95, 3357-3362
32. Logsdon, N. J., Jones, B. C., Allman, J. C., Izotova, L., Schwartz, B., Pestka, S., and Walter, M. R. (2004) The IL-10R2 binding hot spot on IL-22 is located on the N-terminal helix and is dependent on N-linked glycosylation. J. Mol. Biol. 342, 503-514
33. Yoshikawa, M., Nakajima, T., Tsukidate, T., Matsumoto, K., Iida, M., Otori, N., Haruna, S., Moriyama, H., and Saito, H. (2003) TNF-alpha and IL-4 regulate expression of IL-13 receptor alpha2 on human fibroblasts. Biochem. Biophys. Res. Commun. 312, 1248-1255
34. Daines, M. O., and Hershey, G. K. (2002) A novel mechanism by which interferon-gamma can regulate interleukin (IL)-13 responses. Evidence for intracellular stores of IL-13 receptor alpha-2 and their rapid mobilization by interferon-gamma. J. Biol. Chem. 277, 10387-10393
35. Gonzalez-Moreno, O., Calvo, A., Joshi, B. H., Abasolo, I., Leland, P., Wang, Z., Montuenga, L., Puri, R. K., and Green, J. E. (2005) Gene expression profiling identifies IL-13 receptor alpha 2 chain as a therapeutic target in prostate tumor cells overexpressing adrenomedullin. Int. J. Cancer 114, 870-878
36. Jakubzick, C., Choi, E. S., Kunkel, S. L., Evanoff, H., Martinez, F. J., Puri, R. K., Flaherty, K. R., Toews, G. B., Colby, T. V., Kazerooni, E. A., et al. (2004) Augmented pulmonary IL-4 and IL-13 receptor subunit expression in idiopathic interstitial pneumonia. J. Clin. Pathol. 57, 477-486
37. Jakubzick, C., Choi, E. S., Joshi, B. H., Keane, M. P., Kunkel, S. L., Puri, R. K., and Hogaboam, C. M. (2003) Therapeutic attenuation of pulmonary fibrosis via targeting of IL-4- and IL-13-responsive cells. J. Immunol. 171, 2684-2693
38. Chiaramonte, M. G., Mentink-Kane, M., Jacobson, B. A., Cheever, A. W., Whitters, M. J., Goad, M. E., Wong, A., Collins, M., Donaldson, D. D., Grusby, M. J., et al. (2003) Regulation and function of the interleukin 13 receptor alpha 2 during a T helper cell type 2-dominant immune response. J. Exp. Med. 197, 687-701
39. Zhang, J. G., Hilton, D. J., Willson, T. A., McFarlane, C., Roberts, B. A., Moritz, R. L., Simpson, R. J., Alexander, W. S., Metcalf, D., and Nicola, N. A. (1997) Identification, purification, and characterization of a soluble interleukin (IL)-13-binding protein. Evidence that it is distinct from the cloned Il-13 receptor and Il-4 receptor alpha-chains. J. Biol. Chem. 272, 9474-9480
40. Mentink-Kane, M. M., Cheever, A. W., Thompson, R. W., Hari, D. M., Kabatereine, N. B., Vennervald, B. J., Ouma, J. H., Mwatha, J. K., Jones, F. M., Donaldson, D. D., et al. (2004) IL-13 receptor alpha 2 down-modulates granulomatous inflammation and prolongs host survival in schistosomiasis. Proc. Natl. Acad. Sci. U. S. A. 101, 586-590
41. Taube, C., Duez, C., Cui, Z. H., Takeda, K., Rha, Y. H., Park, J. W., Balhorn, A., Donaldson, D. D., Dakhama, A., and Gelfand, E. W. (2002) The role of IL-13 in established allergic airway disease. J. Immunol. 169, 6482-6489