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Science 26 July 1996:
Vol. 273. no. 5274, pp. 464 - 471
DOI: 10.1126/science.273.5274.464
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Research Articles

Functional Mimicry of a Protein Hormone by a Peptide Agonist: The EPO Receptor Complex at 2.8 Å

Oded Livnah, Enrico A. Stura, Dana L. Johnson, Steven A. Middleton, Linda S. Mulcahy, Nicholas C. Wrighton, William J. Dower, Linda K. Jolliffe, Ian A. Wilson *

The functional mimicry of a protein by an unrelated small molecule has been a formidable challenge. Now, however, the biological activity of a 166-residue hematopoietic growth hormone, erythropoietin (EPO), with its class 1 cytokine receptor has been mimicked by a 20-residue cyclic peptide unrelated in sequence to the natural ligand. The crystal structure at 2.8 Å resolution of a complex of this agonist peptide with the extracellular domain of EPO receptor reveals that a peptide dimer induces an almost perfect twofold dimerization of the receptor. The dimer assembly differs from that of the human growth hormone (hGH) receptor complex and suggests that more than one mode of dimerization may be able to induce signal transduction and cell proliferation. The EPO receptor binding site, defined by peptide interaction, corresponds to the smaller functional epitope identified for hGH receptor. Similarly, the EPO mimetic peptide ligand can be considered as a minimal hormone, and suggests the design of nonpeptidic small molecule mimetics for EPO and other cytokines may indeed be achievable.

O. Livnah, E. A. Stura, and I. A. Wilson are in the Department of Molecular Biology and at the Skaggs Institute of Chemical Biology, The Scripps Research Institute, 10666 North Torrey Pines Road, La Jolla, CA 92037, USA. D. L. Johnson, S. A. Middleton, L. S. Mulcahy, and L. K. Jolliffe are at the R. W. Johnson Pharmaceutical Research Institute, Drug Discovery Research, 1000 Route 202, Box 300, Raritan, NJ 08869, USA. N. C. Wrighton and W. J. Dower are at Affymax Research Institute, 4001 Miranda Avenue, Palo Alto, CA 94304, USA.
*   To whom all correspondence should be addressed.


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K. N. Morris, K. B. Jensen, C. M. Julin, M. Weil, and L. Gold (1998)
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Human erythropoietin dimers with markedly enhanced in vivo activity.
A. J. Sytkowski, E. D. Lunn, K. L. Davis, L. Feldman, and S. Siekman (1998)
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F. C. Stomski, J. M. Woodcock, B. Zacharakis, C. J. Bagley, Q. Sun, and A. F. Lopez (1998)
J. Biol. Chem. 273, 1192-1199
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K. M. Moritz, G. B. Lim, and E. M. Wintour (1997)
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J. E. Layton, J. Iaria, D. K. Smith, and H. R. Treutlein (1997)
J. Biol. Chem. 272, 29735-29741
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S. Atwell, M. Ultsch, A. M. De Vos, and J. A. Wells (1997)
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J. Exp. Med. 185, 1939-1950
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Bioactive Peptide Design Based on Protein Surface Epitopes. A CYCLIC HEPTAPEPTIDE MIMICS CD4 DOMAIN 1 CCprime LOOP AND INHIBITS CD4 BIOLOGICAL FUNCTION.
T. Satoh, J. M. Aramini, S. Li, T. M. Friedman, J. Gao, A. E. Edling, R. Townsend, U. Koch, S. Choksi, M. W. Germann, et al. (1997)
J. Biol. Chem. 272, 12175-12180
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Cell Surface Organization of the Erythropoietin Receptor Complex Differs Depending on its Mode of Activation.
K. Tarr, S. S. Watowich, and G. D. Longmore (1997)
J. Biol. Chem. 272, 9099-9107
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Two Restricted Sites on the Surface of the Nerve Growth Factor Molecule Independently Determine Specific TrkA Receptor Binding and Activation.
K. Kullander, D. Kaplan, and T. Ebendal (1997)
J. Biol. Chem. 272, 9300-9307
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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.
C. J. Bagley, J. M. Woodcock, F. C. Stomski, and A. F. Lopez (1997)
Blood 89, 1471-1482
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Mutagenesis Studies of the Human Erythropoietin Receptor. ESTABLISHMENT OF STRUCTURE-FUNCTION RELATIONSHIPS.
F. P. Barbone, S. A. Middleton, D. L. Johnson, F. J. McMahon, J. Tullai, R. H. Gruninger, A. E. Schilling, L. K. Jolliffe, and L. S. Mulcahy (1997)
J. Biol. Chem. 272, 4985-4992
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Activating Mutations in Cytokine Receptors: Implications for Receptor Function and Role in Disease.
T. J. Gonda and R. J. D'Andrea (1997)
Blood 89, 355-369
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Homodimerization of Erythropoietin Receptor by a Bivalent Monoclonal Antibody Triggers Cell Proliferation and Differentiation of Erythroid Precursors.
H. Schneider, W. Chaovapong, D. J. Matthews, C. Karkaria, R. T. Cass, H. Zhan, M. Boyle, T. Lorenzini, S. G. Elliott, and L. B. Giebel (1997)
Blood 89, 473-482
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A computer screening approach to immunoglobulin superfamily structures and interactions: Discovery of small non-peptidic CD4 inhibitors as novel immunotherapeutics.
S. Li, J. Gao, T. Satoh, T. M. Friedman, A. E. Edling, U. Koch, S. Choksi, X. Han, R. Korngold, and Z. Huang (1997)
PNAS 94, 73-78
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Ligand Discrimination in Signaling through an ErbB4 Receptor Homodimer.
C. Sweeney, C. Lai, D. J. Riese II, A. J. Diamonti, L. C. Cantley, and K. L. Carraway III (2000)
J. Biol. Chem. 275, 19803-19807
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Three Loops of the Common gamma Chain Ectodomain Required for the Binding of Interleukin-2 and Interleukin-7.
F. Olosz and T. R. Malek (2000)
J. Biol. Chem. 275, 30100-30105
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Identification of Critical Residues in Bovine IFNAR-1 Responsible for Interferon Binding.
E. C. Cutrone and J. A. Langer (2001)
J. Biol. Chem. 276, 17140-17148
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Determination of the Disulfide Structure and N-Glycosylation Sites of the Extracellular Domain of the Human Signal Transducer gp130.
R. L. Moritz, N. E. Hall, L. M. Connolly, and R. J. Simpson (2001)
J. Biol. Chem. 276, 8244-8253
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Systematic Evolution of a DNA Aptamer Binding to Rat Brain Tumor Microvessels. SELECTIVE TARGETING OF ENDOTHELIAL REGULATORY PROTEIN PIGPEN.
M. Blank, T. Weinschenk, M. Priemer, and H. Schluesener (2001)
J. Biol. Chem. 276, 16464-16468
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Reengineering Granulocyte Colony-stimulating Factor for Enhanced Stability.
B. Bishop, D. C. Koay, A. C. Sartorelli, and L. Regan (2001)
J. Biol. Chem. 276, 33465-33470
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Structural basis for the interaction of the fluorescence probe 8-anilino-1-naphthalene sulfonate (ANS) with the antibiotic target MurA.
E. Schonbrunn, S. Eschenburg, K. Luger, W. Kabsch, and N. Amrhein (2000)
PNAS 97, 6345-6349
   Abstract »    Full Text »    PDF »


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