Redirecting cell-type specific cytokine responses with engineered interleukin-4 superkines

Nature Chemical Biology

Volumn 8, Issue 12, 2012, Pages 990-998

  Junttila, Ilkka S ^a,b,c   Creusot, Remi J ^d   Moraga, Ignacio ^d   Bates, Darren L ^d   Wong, Michael T ^d   Alonso, Michael N ^d   Suhoski, Megan M ^d   Lupardus, Patrick ^d   Meier Schellersheim, Martin ^a   Engleman, Edgar G ^d   Utz, Paul J ^d   Fathman, C Garrison ^d   Paul, William E ^a   Garcia, K Christopher ^d  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^c FIMLAB LABORATORIES   (Finland)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 13 RECEPTOR ALPHA1; INTERLEUKIN 4 RECEPTOR TYPE I; INTERLEUKIN 4A RECEPTOR TYPE I; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CELL ACTIVATION; CELL DIFFERENTIATION; CELL TYPE; CHEMICAL STRUCTURE; CONTROLLED STUDY; CYTOKINE RESPONSE; DENDRITIC CELL; HUMAN; HUMAN CELL; MONOCYTE; PRIORITY JOURNAL; PROTEIN FOLDING; RECEPTOR BINDING; SIGNAL TRANSDUCTION;

CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINE; CYTOKINES; DENDRITIC CELLS; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HUMANS; IMMUNOLOGIC FACTORS; INTERLEUKIN-4; MUTATION; PHENOTYPE; PHOSPHORYLATION; PROTEIN ENGINEERING; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, INTERLEUKIN-4; SIGNAL TRANSDUCTION; STAT6 TRANSCRIPTION FACTOR; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84870308987     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.1096     Document Type: Article

References (31)

1. Leonard, W.J. Type I cytokines and interferons and their receptors. in Fundamental Immunology (ed. Paul, W.) 741-774 (Lippinscott-Raven, Philadelphia, 1999).
2. Ihle, J.N. Cytokine receptor signalling. Nature 377, 591-594 (1995).
3. Stroud, R.M. & Wells, J.A. Mechanistic diversity of cytokine receptor signaling across cell membranes. Sci. STKE 2004, re7 (2004).
4. Wang, X., Lupardus, P., Laporte, S.L. & Garcia, K.C. Structural biology of shared cytokine receptors. Annu. Rev. Immunol. 27, 29-60 (2009).
5. Cunningham, B.C. et al. Dimerization of the extracellular domain of the human growth hormone receptor by a single hormone molecule. Science 254, 821-825 (1991). (Pubitemid 21917402)
6. LaPorte, S.L. et al. Molecular and structural basis of cytokine receptor pleiotropy in the interleukin-4/13 system. Cell 132, 259-272 (2008).
7. Junttila, I.S. et al. Tuning sensitivity to IL-4 and IL-13: differential expression of IL-4Rα, IL-13Rα1, and ?c regulates relative cytokine sensitivity. J. Exp. Med. 205, 2595-2608 (2008).
8. Ito, T. et al. Distinct structural requirements for interleukin-4 (IL-4) and IL-13 binding to the shared IL-13 receptor facilitate cellular tuning of cytokine responsiveness. J. Biol. Chem. 284, 24289-24296 (2009).
9. Mueller, T.D., Zhang, J.L., Sebald, W. & Duschl, A. Structure, binding, and antagonists in the IL-4/IL-13 receptor system. Biochim. Biophys. Acta 1592, 237-250 (2002). (Pubitemid 35284881)
10. Nelms, K., Keegan, A.D., Zamorano, J., Ryan, J.J. & Paul, W.E. The IL-4 receptor: signaling mechanisms and biologic functions. Annu. Rev. Immunol. 17, 701-738 (1999). (Pubitemid 29241138)
11. Kelly-Welch, A.E., Hanson, E.M., Boothby, M.R. & Keegan, A.D. Interleukin-4 and interleukin-13 signaling connections maps. Science 300, 1527-1528 (2003). (Pubitemid 36686713)
12. Hage, T., Sebald, W. & Reinemer, P. Crystal structure of the interleukin-4/receptor α chain complex reveals a mosaic binding interface. Cell 97, 271-281 (1999). (Pubitemid 29194277)
13. Andrews, A.L., Holloway, J.W., Holgate, S.T. & Davies, D.E. IL-4 receptor α is an important modulator of IL-4 and IL-13 receptor binding: implications for the development of therapeutic targets. J. Immunol. 176, 7456-7461 (2006). (Pubitemid 43849048)
14. Andrews, A.L., Holloway, J.W., Puddicombe, S.M., Holgate, S.T. & Davies, D.E. Kinetic analysis of the interleukin-13 receptor complex. J. Biol. Chem. 277, 46073-46078 (2002). (Pubitemid 35417594)
15. Heller, N.M. et al. Type I IL-4Rs selectively activate IRS-2 to induce target gene expression in macrophages. Sci. Signal. 1, ra17 (2008).
16. Kraich, M. et al. A modular interface of IL-4 allows for scalable affinity without affecting specificity for the IL-4 receptor. BMC Biol. 4, 13 (2006).
17. Wenzel, S., Wilbraham, D., Fuller, R., Getz, E.B. & Longphre, M. Effect of an interleukin-4 variant on late phase asthmatic response to allergen challenge in asthmatic patients: results of two phase 2a studies. Lancet 370, 1422-1431 (2007). (Pubitemid 47576168)
18. Boder, E.T. & Wittrup, K.D. Yeast surface display for screening combinatorial polypeptide libraries. Nat. Biotechnol. 15, 553-557 (1997). (Pubitemid 27251573)
19. Conrad, D.H. et al. Effect of B cell stimulatory factor-1 (interleukin 4) on Fc? and Fc? receptor expression on murine B lymphocytes and B cell lines. J. Immunol. 139, 2290-2296 (1987). (Pubitemid 17152124)
20. Siegel, J.P. & Mostowski, H.S. A bioassay for the measurement of human interleukin-4. J. Immunol. Methods 132, 287-295 (1990). (Pubitemid 20281888)
21. Gavutis, M., Jaks, E., Lamken, P. & Piehler, J. Determination of the two-dimensional interaction rate constants of a cytokine receptor complex. Biophys. J. 90, 3345-3355 (2006).
22. Wong, M.T. et al. Regulation of human TH9 differentiation by type I interferons and IL-21. Immunol. Cell Biol. 88, 624-631 (2010).
23. Dauer, M. et al. Mature dendritic cells derived from human monocytes within 48 hours: a novel strategy for dendritic cell differentiation from blood precursors. J. Immunol. 170, 4069-4076 (2003). (Pubitemid 36428169)
24. Levin, A.M. et al. Exploiting a natural conformational switch to engineer an interleukin-2 'superkine'. Nature 484, 529-533 (2012).
25. Pillet, A.H. et al. IL-2 induces conformational changes in its preassembled receptor core, which then migrates in lipid raft and binds to the cytoskeleton meshwork. J. Mol. Biol. 403, 671-692 (2010).
26. O'Shea, J.J. & Paul, W.E. Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells. Science 327, 1098-1102 (2010).
27. Sosman, J.A., Fisher, S.G., Kefer, C., Fisher, R.I. & Ellis, T.M. A phase I trial of continuous infusion interleukin-4 (IL-4) alone and following interleukin-2 (IL-2) in cancer patients. Ann. Oncol. 5, 447-452 (1994). (Pubitemid 24159651)
28. Lutz, M.B. et al. Differential functions of IL-4 receptor types I and II for dendritic cell maturation and IL-12 production and their dependency on GM-CSF. J. Immunol. 169, 3574-3580 (2002).
29. Creusot, R.J. et al. A short pulse of IL-4 delivered by DCs electroporated with modified mRNA can both prevent and treat autoimmune diabetes in NOD mice. Mol. Ther. 18, 2112-2120 (2010).
30. Creusot, R.J. et al. Tissue-targeted therapy of autoimmune diabetes using dendritic cells transduced to express IL-4 in NOD mice. Clin. Immunol. 127, 176-187 (2008).
31. Krutzik, P.O. & Nolan, G.P. Fluorescent cell barcoding in flow cytometry allows high-throughput drug screening and signaling profiling. Nat. Methods 3, 361-368 (2006).