Crystal structure of the mouse interleukin-3 β-receptor: Insights into interleukin-3 binding and receptor activation

Biochemical Journal

Volumn 463, Issue 3, 2014, Pages 393-403

  Carr, Paul D ^a   Ewens, Cameron L ^b   Dai, Jin ^b   Ollis, David L ^a   Murphy, James M ^c,d   Jackson, Colin J ^a   Young, Ian G ^b  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b Biology and Environment   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Cytokine receptor; Ectodomain; Granulocyte macrophage colony stimulating factor (GM CSF); Interleukin 3 (IL 3); Interleukin 5 (IL 5); Surface entropy reduction

Indexed keywords

BETA C RECEPTOR; CD131 ANTIGEN; HOMODIMER; INTERLEUKIN 3; RECEPTOR; UNCLASSIFIED DRUG; RECOMBINANT PROTEIN;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; LIGAND BINDING; MOLECULAR EVOLUTION; MOLECULAR MODEL; MOUSE; NONHUMAN; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; RECEPTOR ACTIVATION; TRANSCRIPTION INITIATION; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; CYTOKINE RECEPTOR COMMON BETA SUBUNIT; EVOLUTION, MOLECULAR; INTERLEUKIN-3; MICE; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS;

EID: 84907843570     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20140863     Document Type: Article

References (61)

1. Kobayashi, M., Van Leeuwen, B. H., Elsbury, S., Martinson, M. E., Young, I. G. and Hapel, A. J. (1989) Interleukin-3 is significantly more effective than other colony-stimulating factors in long-term maintenance of human bone marrow-derived colony-forming cells in vitro. Blood 73, 1836-1841 PubMed
2. Lopez, A. F., Lyons, A. B., Eglinton, J. M., Park, L. S., To, L. B., Clark, S. C. and Vadas, M. A. (1990) Specific binding of human interleukin-3 and granulocyte-macrophage colony-stimulating factor to human basophils. J. Allergy Clin. Immunol. 85, 99-102 CrossRef PubMed
3. Robin, C., Ottersbach, K., Durand, C., Peeters, M., Vanes, L., Tybulewicz, V. and Dzierzak, E. (2006) An unexpected role for IL-3 in the embryonic development of hematopoietic stem cells. Dev. Cell 11, 171-180 CrossRef PubMed
4. Lantz, C. S., Boesiger, J., Song, C. H., Mach, N., Kobayashi, T., Mulligan, R. C., Nawa, Y., Dranoff, G. and Galli, S. J. (1998) Role for interleukin-3 in mast-cell and basophil development and in immunity to parasites. Nature 392, 90-93 CrossRef PubMed
5. Jiang, X., Lopez, A., Holyoake, T., Eaves, A. and Eaves, C. (1999) Autocrine production and action of IL-3 and granulocyte colony-stimulating factor in chronic myeloid leukemia. Proc. Natl. Acad. Sci. U.S.A. 96, 12804-12809 CrossRef PubMed
6. Delwel, R., Dorssers, L., Touw, I., Wagemaker, G. and Lowenberg, B. (1987) Human recombinant multilineage colony stimulating factor (interleukin-3): stimulator of acute myelocytic leukemia progenitor cells in vitro. Blood 70, 333-336 PubMed
7. Testa, U., Riccioni, R., Militi, S., Coccia, E., Stellacci, E., Samoggia, P., Latagliata, R., Mariani, G., Rossini, A., Battistini, A., Lo-Coco, F. and Peschle, C. (2002) Elevated expression of IL-3Rα in acute myelogenous leukemia is associated with enhanced blast proliferation, increased cellularity, and poor prognosis. Blood 100, 2980-2988 CrossRef PubMed
8. Nievergall, E., Ramshaw, H. S., Yong, A. S., Biondo, M., Busfield, S. J., Vairo, G., Lopez, A. F., Hughes, T. P., White, D. L. and Hiwase, D. K. (2014) Monoclonal antibody targeting of IL-3 receptor α with CSL362 effectively depletes CML progenitor and stem cells. Blood 123, 1218-1228 CrossRef PubMed
9. Jin, L., Lee, E. M., Ramshaw, H. S., Busfield, S. J., Peoppl, A. G., Wilkinson, L., Guthridge, M. A., Thomas, D., Barry, E. F., Boyd, A. et al. (2009) Monoclonal antibody-mediated targeting of CD123, IL-3 receptor α chain, eliminates human acute myeloid leukemic stem cells. Cell Stem Cell 5, 31-42 CrossRef PubMed
10. Murphy, J. M. and Young, I. G. (2006) IL-3, IL-5, and GM-CSF signaling: crystal structure of the human β-common receptor. Vitam. Horm. 74, 1-30 CrossRef PubMed
11. Gorman, D. M., Itoh, N., Kitamura, T., Schreurs, J., Yonehara, S., Yahara, I., Arai, K. and Miyajima, A. (1990) Cloning and expression of a gene encoding an interleukin 3 receptor-like protein: identification of another member of the cytokine receptor gene family. Proc. Natl. Acad. Sci. U.S.A. 87, 5459-5463 CrossRef PubMed
12. Hayashida, K., Kitamura, T., Gorman, D. M., Arai, K., Yokota, T. and Miyajima, A. (1990) Molecular cloning of a second subunit of the receptor for human granulocyte-macrophage colony-stimulating factor (GM-CSF): reconstitution of a high-affinity GM-CSF receptor. Proc. Natl. Acad. Sci. U.S.A. 87, 9655-9659 CrossRef PubMed
13. Kitamura, T., Hayashida, K., Sakamaki, K., Yokota, T., Arai, K. and Miyajima, A. (1991) Reconstitution of functional receptors for human granulocyte/macrophage colony-stimulating factor (GM-CSF): evidence that the protein encoded by the AIC2B cDNA is a subunit of the murine GM-CSF receptor. Proc. Natl. Acad. Sci. U.S.A. 88, 5082-5086 CrossRef PubMed
14. Tavernier, J., Devos, R., Cornelis, S., Tuypens, T., Van der Heyden, J., Fiers, W. and Plaetinck, G. (1991) A human high affinity interleukin-5 receptor (IL5R) is composed of an IL5-specific α chain and a β chain shared with the receptor for GM-CSF. Cell 66, 1175-1184 CrossRef PubMed
15. Itoh, N., Yonehara, S., Schreurs, J., Gorman, D. M., Maruyama, K., Ishii, A., Yahara, I., Arai, K. and Miyajima, A. (1990) Cloning of an interleukin-3 receptor gene: a member of a distinct receptor gene family. Science 247, 324-327 CrossRef PubMed
16. Gorman, D. M., Itoh, N., Jenkins, N. A., Gilbert, D. J., Copeland, N. G. and Miyajima, A. (1992) Chromosomal localization and organization of the murine genes encoding the β subunits (AIC2A and AIC2B) of the interleukin 3, granulocyte/macrophage colony-stimulating factor, and interleukin 5 receptors. J. Biol. Chem. 267, 15842-15848 PubMed
17. Hara, T. and Miyajima, A. (1992) Two distinct functional high affinity receptors for mouse interleukin-3 (IL-3). EMBO J. 11, 1875-1884 PubMed
18. Murphy, J. M., Ford, S. C., Olsen, J. E., Gustin, S. E., Jeffrey, P. D., Ollis, D. L. and Young, I. G. (2004) Interleukin-3 binding to the murine βIL-3 and human βc receptors involves functional epitopes formed by domains 1 and 4 of different protein chains. J. Biol. Chem. 279, 26500-26508 CrossRef PubMed
19. Wang, H. M., Ogorochi, T., Arai, K. and Miyajima, A. (1992) Structure of mouse interleukin 3 (IL-3) binding protein (AIC2A): amino acid residues critical for IL-3 binding. J. Biol. Chem. 267, 979-983 PubMed
20. Babon, J. J., Lucet, I. S., Murphy, J. M., Nicola, N. A. and Varghese, L. N. (2014) The molecular regulation of Janus kinase (JAK) activation. Biochem. J. 462, 1-13 CrossRef PubMed
21. Chen, J., Olsen, J., Ford, S., Mirza, S., Walker, A., Murphy, J. M. and Young, I. G. (2009) A new isoform of interleukin-3 receptor α with novel differentiation activity and high affinity binding mode. J. Biol. Chem. 284, 5763-5773 CrossRef PubMed
22. Mirza, S., Chen, J., Wen, B., Ewens, C. L., Dai, J., Murphy, J. M. and Young, I. G. (2010) Two modes of β-receptor recognition are mediated by distinct epitopes on mouse and human interleukin-3. J. Biol. Chem. 285, 22370-22381 CrossRef PubMed
23. Carr, P. D., Conlan, F., Ford, S., Ollis, D. L. and Young, I. G. (2006) An improved resolution structure of the human β common receptor involved in IL-3, IL-5 and GM-CSF signalling which gives better definition of the high-affinity binding epitope. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 62, 509-513 CrossRef PubMed
24. Carr, P. D., Gustin, S. E., Church, A. P., Murphy, J. M., Ford, S. C., Mann, D. A., Woltring, D. M., Walker, I., Ollis, D. L. and Young, I. G. (2001) Structure of the complete extracellular domain of the common β subunit of the human GM-CSF, IL-3, and IL-5 receptors reveals a novel dimer configuration. Cell 104, 291-300 CrossRef PubMed
25. Hansen, G., Hercus, T. R., McClure, B. J., Stomski, F. C., Dottore, M., Powell, J., Ramshaw, H., Woodcock, J. M., Xu, Y., Guthridge, M. et al. (2008) The structure of the GM-CSF receptor complex reveals a distinct mode of cytokine receptor activation. Cell 134, 496-507 CrossRef PubMed
26. Murphy, J. M., Ford, S. C., Wiedemann, U. M., Carr, P. D., Ollis, D. L. and Young, I. G. (2003) A novel functional epitope formed by domains 1 and 4 of the human common β-subunit is involved in receptor activation by granulocyte macrophage colony-stimulating factor and interleukin 5. J. Biol. Chem. 278, 10572-10577 CrossRef PubMed
27. Cooper, D. R., Boczek, T., Grelewska, K., Pinkowska, M., Sikorska, M., Zawadzki, M. and Derewenda, Z. (2007) Protein crystallization by surface entropy reduction: optimization of the SER strategy. Acta Crystallogr. D Biol. Crystallogr. 63, 636-645 CrossRef PubMed
28. csubunit of the human IL-5, IL-3 and GM-CSF receptors. Eur. J. Biochem. 268, 2905-2911 CrossRef PubMed
29. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C. and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 CrossRef PubMed
30. Stein, N. (2008) CHAINSAW: a program for mutating pdb files used as templates in molecular replacement. J. Appl. Crystallogr. 41, 641-643 CrossRef
31. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 CrossRef PubMed
32. Cowtan, K. (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D Biol. Crystallogr. 62, 1002-1011 CrossRef PubMed
33. Murshudov, G. N., Vagin, A. A. and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 CrossRef PubMed
34. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K. and Terwilliger, T. C. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954 CrossRef PubMed
35. DiMaio, F., Echols, N., Headd, J. J., Terwilliger, T. C., Adams, P. D. and Baker, D. (2013) Improved low-resolution crystallographic refinement with Phenix and Rosetta. Nat. Methods 10, 1102-1104 CrossRef PubMed
36. Ramachandran, G. N., Ramakrishnan, C. and Sasisekharan, V. (1963) Stereochemistry of polypeptide chain configurations. J. Mol. Biol. 7, 95-99 CrossRef PubMed
37. Kirby, N. M., Mudie, S. T., Hawley, A. M., Cookson, D. J., Mertens, H. D. T., Cowieson, N. and Samardzic-Boban, V. (2013) A low-background-intensity focusing small-angle X-ray scattering undulator beamline. J. Appl. Crystallogr. 46, 1670-1680 CrossRef
38. Murphy, J. M., Czabotar, P. E., Hildebrand, J. M., Lucet, I. S., Zhang, J. G., Alvarez-Diaz, S., Lewis, R., Lalaoui, N., Metcalf, D., Webb, A. I. et al. (2013) The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 39, 443-453 CrossRef PubMed
39. Murphy, J. M., Lucet, I. S., Hildebrand, J. M., Tanzer, M. C., Young, S. N., Sharma, P., Lessene, G., Alexander, W. S., Babon, J. J., Silke, J. and Czabotar, P. E. (2014) Insights into the evolution of divergent nucleotide-binding mechanisms among pseudokinases revealed by crystal structures of human and mouse MLKL. Biochem. J. 457, 369-377 CrossRef PubMed
40. Kershaw, N. J., Murphy, J. M., Liau, N. P., Varghese, L. N., Laktyushin, A., Whitlock, E. L., Lucet, I. S., Nicola, N. A. and Babon, J. J. (2013) SOCS3 binds specific receptor-JAK complexes to control cytokine signaling by direct kinase inhibition. Nat. Struct. Mol. Biol. 20, 469-476 CrossRef PubMed
41. Varghese, L. N., Ungureanu, D., Liau, N. P., Young, S. N., Laktyushin, A., Hammaren, H., Lucet, I. S., Nicola, N. A., Silvennoinen, O., Babon, J. J. and Murphy, J. M. (2014) Mechanistic insights into activation and SOCS3-mediated inhibition of myeloproliferative neoplasm-associated JAK2 mutants from biochemical and structural analyses. Biochem. J. 458, 395-405 CrossRef PubMed
42. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J. and Svergun, D. I. (2003) PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36, 1277-1282 CrossRef
43. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503 CrossRef
44. Svergun, D., Barberato, C. and Koch, M. H. J. (1995) CRYSOL: a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28, 768-773 CrossRef
45. Rambo, R. P. and Tainer, J. A. (2011) Characterizing flexible and intrinsically unstructured biological macromolecules by SAS using the Porod-Debye law. Biopolymers 95, 559-571 CrossRef PubMed
46. Franke, D. and Svergun, D. I. (2009) DAMMIF, a program for rapid ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 42, 342-346 CrossRef
47. Murphy, J. M., Metcalf, D., Young, I. G. and Hilton, D. J. (2010) A convenient method for preparation of an engineered mouse interleukin-3 analog with high solubility and wild-type bioactivity. Growth Factors 28, 104-110 CrossRef PubMed
48. Yao, S., Young, I. G., Norton, R. S. and Murphy, J. M. (2011) Murine interleukin-3: structure, dynamics, and conformational heterogeneity in solution. Biochemistry 50, 2464-2477 CrossRef PubMed
49. Lyskov, S. and Gray, J. J. (2008) The RosettaDock server for local protein-protein docking. Nucleic Acids Res. 36, W233-W238 CrossRef PubMed
50. Lyskov, S., Chou, F. C., Conchuir, S. O., Der, B. S., Drew, K., Kuroda, D., Xu, J., Weitzner, B. D., Renfrew, P. D., Sripakdeevong, P. et al. (2013) Serverification of molecular modeling applications: the Rosetta Online Server that Includes Everyone (ROSIE). PLoS ONE 8, e63906 CrossRef PubMed
51. Bazan, J. F. (1990) Structural design and molecular evolution of a cytokine receptor superfamily. Proc. Natl. Acad. Sci. U.S.A. 87, 6934-6938 CrossRef PubMed
52. de Vos, A. M., Ultsch, M. and Kossiakoff, A. A. (1992) Human growth hormone and extracellular domain of its receptor: crystal structure of the complex. Science 255, 306-312 CrossRef PubMed
53. Syed, R. S., Reid, S. W., Li, C., Cheetham, J. C., Aoki, K. H., Liu, B., Zhan, H., Osslund, T. D., Chirino, A. J., Zhang, J. et al. (1998) Efficiency of signalling through cytokine receptors depends critically on receptor orientation. Nature 395, 511-516 CrossRef PubMed
54. Boehr, D. D., Nussinov, R. and Wright, P. E. (2009) The role of dynamic conformational ensembles in biomolecular recognition. Nat. Chem. Biol. 5, 789-796 CrossRef PubMed
55. comchimeras. FEBS Lett. 460, 99-102 CrossRef PubMed
56. 15N heteronuclear correlation spectra acquired with band-selective pulses. J. Magn. Reson. 211, 243-247 CrossRef PubMed
57. 15N resonance assignments of a highly-soluble murine interleukin-3 analogue with wild-type bioactivity. Biomol. NMR Assign. 4, 73-77 CrossRef PubMed
58. Krissinel, E. and Henrick, K. (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60, 2256-2268 CrossRef PubMed
59. Kleywegt, G. J. and Jones, T. A. (1997) Detecting folding motifs and similarities in protein structures. Methods Enzymol. 277, 525-545 CrossRef PubMed
60. Woodcock, J. M., Bagley, C. J., Zacharakis, B. and Lopez, A. F. (1996) A single tyrosine residue in the membrane-proximal domain of the granulocyte-macrophage colony-stimulating factor, interleukin (IL)-3, and IL-5 receptor common β-chain is necessary and sufficient for high affinity binding and signaling by all three ligands. J. Biol. Chem. 271, 25999-26006 CrossRef PubMed
61. Woodcock, J. M., Zacharakis, B., Plaetinck, G., Bagley, C. J., Qiyu, S., Hercus, T. R., Tavernier, J. and Lopez, A. F. (1994) Three residues in the common β chain of the human GM-CSF, IL-3 and IL-5 receptors are essential for GM-CSF and IL-5 but not IL-3 high affinity binding and interact with Glu21 of GM-CSF. EMBO J. 13, 5176-5185 PubMed