The Structure of the GM-CSF Receptor Complex Reveals a Distinct Mode of Cytokine Receptor Activation

Cell

Volumn 134, Issue 3, 2008, Pages 496-507

  Hansen, Guido ^a   Hercus, Timothy R ^b   McClure, Barbara J ^b   Stomski, Frank C ^b   Dottore, Mara ^b   Powell, Jason ^b   Ramshaw, Hayley ^b   Woodcock, Joanna M ^b   Xu, Yibin ^a   Guthridge, Mark ^b   McKinstry, William J ^a   Lopez, Angel F ^b   Parker, Michael W ^a,c  

^a ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b HANSON INSTITUTE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

MOLIMMUNO; SIGNALING

Indexed keywords

GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR RECEPTOR; INTERLEUKIN 3 RECEPTOR; INTERLEUKIN 5 RECEPTOR;

ARTICLE; COMPLEX FORMATION; HUMAN; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

EID: 48449102092     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2008.05.053     Document Type: Article

References (53)

1. Bagley C.J., Woodcock J.M., Stomski F.C., and Lopez A.F. The structural and functional basis of cytokine receptor activation: lessons from the common beta subunit of the granulocyte-macrophage colony-stimulating factor, interleukin-3 (IL-3), and IL-5 receptors. Blood 89 (1997) 1471-1482
2. Barouch D.H., Santra S., Tenner-Racz K., Racz P., Kuroda M.J., Schmitz J.E., Jackson S.S., Lifton M.A., Freed D.C., Perry H.C., et al. Potent CD4+ T cell responses elicited by a bicistronic HIV-1 DNA vaccine expressing gp120 and GM-CSF. J. Immunol. 168 (2002) 562-568
3. Barry S.C., Korpelainen E., Sun Q., Stomski F.C., Moretti P.A., Wakao H., D'Andrea R.J., Vadas M.A., Lopez A.F., and Goodall G.J. Two contiguous residues in human interleukin-3, Asp21 and Glu22, selectively interact with the alpha- and beta-chains of its receptor and participate in function. J. Biol. Chem. 269 (1994) 8488-8492
4. Boulanger M.J., Chow D.C., Brevnova E.E., and Garcia K.C. Hexameric structure and assembly of the interleukin-6/IL-6 alpha-receptor/gp130 complex. Science 300 (2003) 2101-2104
5. Birnbaum R.A., O'Marcaigh A., Wardak Z., Zhang Y.Y., Dranoff G., Jacks T., Clapp D.W., and Shannon K.M. Nf1 and GM-CSF interact in myeloid leukemogenesis. Mol. Cell 5 (2000) 189-195
6. Brizzi M.F., Zini M.G., Aronica M.G., Blechman J.M., Yarden Y., and Pegoraro L. Convergence of signaling by interleukin-3, granulocyte-macrophage colony-stimulating factor, and mast cell growth factor on JAK2 tyrosine kinase. J. Biol. Chem. 269 (1994) 31680-31684
7. 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. Structure of the complete extracellular domain of the common beta subunit of the human GM-CSF, IL-3, and IL-5 receptors reveals a novel dimer configuration. Cell 104 (2001) 291-300
8. Carr P.D., Conlan F., Ford S., Ollis D.L., and Young I.G. An improved resolution structure of the human beta 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 (2006) 509-513
9. Cook A.D., Braine E.L., Campbell I.K., Rich M.J., and Hamilton J.A. Blockade of collagen-induced arthritis post-onset by antibody to granulocyte-macrophage colony-stimulating factor (GM-CSF): requirement for GM-CSF in the effector phase of disease. Arthritis Res. 3 (2001) 293-298
10. DeLano, W.L. (2002). DeLano Scientific (San Carlos, CA, USA). http://pymol.sourceforge.net/.
11. Dirksen U., Hattenhorst U., Schneider P., Schroten H., Göbel U., Böcking A., Müller K.M., Murray R., and Burdach S. Defective expression of granulocyte-macrophage colony-stimulating factor/interleukin-3/interleukin-5 receptor common beta chain in children with acute myeloid leukemia associated with respiratory failure. Blood 92 (1998) 1097-1103
12. Fagerholm S.C., Varis M., Stefanidakis M., Hilden T.J., and Gahmberg C.G. alpha-Chain phosphorylation of the human leukocyte CD11b/CD18 (Mac-1) integrin is pivotal for integrin activation to bind ICAMs and leukocyte extravasation. Blood 108 (2006) 3379-3386
13. Fleetwood A.J., Cook A.D., and Hamilton J.A. Functions of granulocyte-macrophage colony-stimulating factor. Crit. Rev. Immunol. 25 (2005) 405-428
14. Guthridge M.A., Stomski F.C., Thomas D., Woodcock J.M., Bagley C.J., Berndt M.C., and Lopez A.F. Mechanism of activation of the GM-CSF, IL-3, and IL-5 family of receptors. Stem Cells 16 (1998) 301-313
15. Guthridge M.A., Powell J.A., Barry E.F., Stomski F.C., McClure B.J., Ramshaw H., Felquer F.A., Dottore M., Thomas D.T., To B., et al. Growth factor pleiotropy is controlled by a receptor Tyr/Ser motif that acts as a binary switch. EMBO J. 25 (2006) 479-489
16. Haman A., Cadieux C., Wilkes B., Hercus T., Lopez A., Clark S., and Hoang T. Molecular determinants of the granulocyte-macrophage colony-stimulating factor receptor complex assembly. J. Biol. Chem. 274 (1999) 34155-34163
17. Hayashida K., Kitamura T., Gorman D.M., Arai K., Yokota T., and Miyajima A. 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. USA 87 (1990) 9655-9659
18. Hercus T.R., Bagley C.J., Cambareri B., Dottore M., Woodcock J.M., Vadas M.A., Shannon M.F., and Lopez A.F. Specific human granulocyte-macrophage colony-stimulating factor antagonists. Proc. Natl. Acad. Sci. USA 91 (1994) 5838-5842
19. Hercus T.R., Cambareri B., Dottore M., Woodcock J., Bagley C.J., Vadas M.A., Shannon M.F., and Lopez A.F. Identification of residues in the first and fourth helices of human granulocyte-macrophage colony-stimulating factor involved in biologic activity and in binding to the alpha- and beta-chains of its receptor. Blood 83 (1994) 3500-3508
20. James C., Ugo V., Le Couédic J.P., Staerk J., Delhommeau F., Lacout C., Garçon L., Raslova H., Berger R., Bennaceur-Griscelli A., et al. A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature 434 (2005) 1144-1148
21. Jenkins B.J., Le F., and Gonda T.J. A cell type-specific constitutive point mutant of the common beta-subunit of the human granulocyte-macrophage colony-stimulating factor (GM-CSF), interleukin (IL)-3, and IL-5 receptors requires the GM-CSF receptor alpha-subunit for activation. J. Biol. Chem. 274 (1999) 8669-8677
22. Korzenik J.R., Dieckgraefe B.K., Valentine J.F., Hausman D.F., Gilbert M.J., and Sargramostim in Crohn's Disease Study Group. Sargramostim for active Crohn's disease. N. Engl. J. Med. 352 (2005) 2193-2201
23. Lia F., Rajotte D., Clark S.C., and Hoang T. A dominant negative granulocyte-macrophage colony-stimulating factor receptor alpha chain reveals the multimeric structure of the receptor complex. J. Biol. Chem. 271 (1996) 28287-28293
24. Lilly M.B., Zemskova M., Frankel A.E., Salo J., and Kraft A.S. Distinct domains of the human granulocyte-macrophage colony-stimulating factor receptor alpha subunit mediate activation of Jak/Stat signaling and differentiation. Blood 97 (2001) 1662-1670
25. Lock P.D., Metcalf D., and Nicola N.A. Histidine-367 of the human common beta chain of the receptor is critical for high-affinity binding of human granulocyte-macrophage colony-stimulating factor. Proc. Natl. Acad. Sci. USA 91 (1994) 252-256
26. Lopez A.F., Shannon M.F., Hercus T., Nicola N.A., Cambareri B., Dottore M., Layton M.J., Eglinton L., and Vadas M.A. Residue 21 of human granulocyte-macrophage colony-stimulating factor is critical for biological activity and for high but not low affinity binding. EMBO J. 11 (1992) 909-916
27. McClure B.J., Hercus T.R., Cambareri B.A., Woodcock J.M., Bagley C.J., Howlett G.J., and Lopez A.F. Molecular assembly of the ternary granulocyte-macrophage colony-stimulating factor receptor complex. Blood 101 (2003) 1308-1315
28. Mellman I., and Steinman R.M. Dendritic cells: specialized and regulated antigen processing machines. Cell 106 (2001) 255-258
29. Murphy J.M., Ford S.C., Wiedemann U.M., Carr P.D., Ollis D.L., and Young I.G. A novel functional epitope formed by domains 1 and 4 of the human common beta-subunit is involved in receptor activation by granulocyte macrophage colony-stimulating factor and interleukin 5. J. Biol. Chem. 278 (2003) 10572-10577
30. Muto A., Watanabe S., Itoh T., Miyajima A., Yokota T., and Arai K. Roles of the cytoplasmic domains of the alpha and beta subunits of human granulocyte-macrophage colony-stimulating factor receptor. J. Allergy Clin. Immunol. 96 (1995) 1100-1114
31. Muto A., Watanabe S., Miyajima A., Yokota T., and Arai K. The beta subunit of human granulocyte-macrophage colony-stimulating factor receptor forms a homodimer and is activated via association with the alpha subunit. J. Exp. Med. 183 (1996) 1911-1916
32. Parganas E., Wang D., Stravopodis D., Topham D.J., Marine J.C., Teglund S., Vanin E.F., Bodner S., Colamonici O.R., van Deursen J.M., et al. JAK2 is essential for signaling through a variety of cytokine receptors. Cell 93 (1998) 385-395
33. Quelle F.W., Sato N., Witthuhn B.A., Inhorn R.C., Eder M., Miyajima A., Griffin J.D., and Ihle J.N. JAK2 associates with the beta c chain of the receptor for granulocyte-macrophage colony-stimulating factor, and its activation requires the membrane-proximal region. Mol. Cell. Biol. 14 (1994) 4335-4341
34. Rajotte D., Cadieux C., Haman A., Wilkes B.C., Clark S.C., Hercus T., Woodcock J.M., Lopez A., and Hoang T. Crucial role of the residue R280 at the F'-G' loop of the human granulocyte/macrophage colony-stimulating factor receptor alpha chain for ligand recognition. J. Exp. Med. 185 (1997) 1939-1950
35. Ramshaw H.S., Bardy P.G., Lee M.A., and Lopez A.F. Chronic myelomonocytic leukemia requires granulocyte-macrophage colony-stimulating factor for growth in vitro and in vivo. Exp. Hematol. 30 (2002) 1124-1131
36. Rawlings J.S., Rosler K.M., and Harrison D.A. The JAK/STAT signaling pathway. J. Cell Sci. 117 (2004) 1281-1283
37. Rossjohn J., McKinstry W.J., Woodcock J.M., McClure B.J., Hercus T.R., Parker M.W., Lopez A.F., and Bagley C.J. Structure of the activation domain of the GM-CSF/IL-3/IL-5 receptor common beta-chain bound to an antagonist. Blood 95 (2000) 2491-2498
38. Rozwarski D.A., Diederichs K., Hecht R., Boone T., and Karplus P.A. Refined crystal structure and mutagenesis of human granulocyte-macrophage colony-stimulating factor. Proteins 26 (1996) 304-313
39. Sakamaki K., Miyajima I., Kitamura T., and Miyajima A. Critical cytoplasmic domains of the common beta subunit of the human GM-CSF, IL-3 and IL-5 receptors for growth signal transduction and tyrosine phosphorylation. EMBO J. 11 (1992) 3541-3549
40. Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 103 (2000) 211-225
41. Soldi R., Primo L., Brizzi M.F., Sanavio F., Aglietta M., Polentarutti N., Pegoraro L., Mantovani A., and Bussolino F. Activation of JAK2 in human vascular endothelial cells by granulocyte-macrophage colony-stimulating factor. Blood 89 (1997) 863-872
42. Stauber D.J., Debler E.W., Horton P.A., Smith K.A., and Wilson I.A. Crystal structure of the IL-2 signaling complex: paradigm for a heterotrimeric cytokine receptor. Proc. Natl. Acad. Sci. USA 103 (2006) 2788-2793
43. Stomski F.C., Sun Q., Bagley C.J., Woodcock J., Goodall G., Andrews R.K., Berndt M.C., and Lopez A.F. Human interleukin-3 (IL-3) induces disulfide-linked IL-3 receptor alpha- and beta-chain heterodimerization, which is required for receptor activation but not high-affinity binding. Mol. Cell. Biol. 16 (1996) 3035-3046
44. Stomski F.C., Woodcock J.M., Zacharakis B., Bagley C.J., Sun Q., and Lopez A.F. Identification of a Cys motif in the common beta chain of the interleukin 3, granulocyte-macrophage colony-stimulating factor, and interleukin 5 receptors essential for disulfide-linked receptor heterodimerization and activation of all three receptors. J. Biol. Chem. 273 (1998) 1192-1199
45. Sun X., Hodge L.M., Jones H.P., Tabor L., and Simecka J.W. Co-expression of granulocyte-macrophage colony-stimulating factor with antigen enhances humoral and tumor immunity after DNA vaccination. Vaccine 20 (2002) 1466-1474
46. Tavernier J., Tuypens T., Verhee A., Plaetinck G., Devos R., Van der Heyden J., Guisez Y., and Oefner C. Identification of receptor-binding domains on human interleukin 5 and design of an interleukin 5-derived receptor antagonist. Proc. Natl. Acad. Sci. USA 92 (1995) 5194-5198
47. Wang X., Rickert M., and Garcia K.C. Structure of the quaternary complex of interleukin-2 with its alpha, beta, and gammac receptors. Science 310 (2005) 1159-1163
48. Watanabe S., Itoh T., and Arai K. JAK2 is essential for activation of c-fos and c-myc promoters and cell proliferation through the human granulocyte-macrophage colony-stimulating factor receptor in BA/F3 cells. J. Biol. Chem. 271 (1996) 12681-12686
49. Wells J.A., and de Vos A.M. Hematopoietic receptor complexes. Annu. Rev. Biochem. 65 (1996) 609-634
50. Wilson-Rawls J., Xie S., Liu J., Laneuville P., and Arlinghaus R.B. P210 Bcr-Abl interacts with the interleukin 3 receptor beta(c) subunit and constitutively induces its tyrosine phosphorylation. Cancer Res. 56 (1996) 3426-3430
51. Woodcock J.M., Zacharakis B., Plaetinck G., Bagley C.J., Qiyu S., Hercus T.R., Tavernier J., and Lopez A.F. Three residues in the common beta 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 (1994) 5176-5185
52. Woodcock J.M., Bagley C.J., Zacharakis B., and Lopez A.F. A single tyrosine residue in the membrane-proximal domain of the granulocyte-macrophage colony-stimulating factor, interleukin (IL)-3, and IL-5 receptor common beta-chain is necessary and sufficient for high affinity binding and signaling by all three ligands. J. Biol. Chem. 271 (1996) 25999-26006
53. Woodcock J.M., McClure B.J., Stomski F.C., Elliott M.J., Bagley C.J., and Lopez A.F. The human granulocyte-macrophage colony-stimulating factor (GM-CSF) receptor exists as a preformed receptor complex that can be activated by GM-CSF, interleukin-3, or interleukin-5. Blood 90 (1997) 3005-3017