Three-dimensional solution structure and backbone dynamics of a variant of human interleukin-3

Journal of Molecular Biology

Volumn 259, Issue 3, 1996, Pages 524-541

  Feng, Yiqing ^a   Klein, Barbara K ^a   McWherter, Charles A ^a  

^a PFIZER INC   (United States)

Author keywords

15N NMR relaxation; Cytokine structure; Dynamics; Four helical bundle; Growth factor

Indexed keywords

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

ARTICLE; CARBOXY TERMINAL SEQUENCE; HUMAN; HYDROPHOBICITY; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; STEREOCHEMISTRY; THREE DIMENSIONAL IMAGING;

EID: 0029938639     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0337     Document Type: Article

References (99)

1. Abdel-Meguid, S. S., Shieh, H.-S., Smith, W. W., Dayringer, H. E., Violand, B. N. & Bentle, L. A. (1987). Three-dimensional structure of a genetically engineered variant of porcine growth hormone. Proc. Natl Acad. Sci. USA, 84, 6434-6437.
2. Azam, M., Erdjument-Bromage, H., Kreider, B. L., Xia, M., Quelle, F., Basu, R., Saris, C., Tempst, P., Ihle, J. N. & Sandler, C. (1995). Interleukin-3 signals through multiple isoforms of STATS. EMBO J. 14, 1402-1411.
3. Bagley, C. J., Woodcock, J. M., Hercus, T. R., Shannon, F. M. & Lopez, A. F. (1995). Interaction of GM-CSF and IL-3 with the common β-chain of their receptors. J. Leukocyte Biol. 57, 739-746.
4. Banks, M., Graber, P., Proudfoot, A. E. I., Arod, C. Y., Allet, B., Bernard, A. R., Sebille, E., McKinnon, M., Wells, T. N. C. & Solari, R. (1995). Soluble interleukin-5 receptor α-chain binding assays: use for screening and analysis of interleukin-5 mutants. Anal Biochem. 230, 321-328.
5. Bazan, J. F. (1990). Haemopoietic receptors and helical cytokines. Immunol. Today, 11, 350-354.
6. Bazan, J. F. (1992). Unraveling the structure of IL-2. Science, 257, 410-412.
7. Biesma, B., Willemse, P. H. B., Mulder, N. H., Sleijfer, D. Th., Gietema, J. A., Mull, R., Limburg, P. C., Bourma, J., Vallenge, E. & de Vries, E. G. E. (1992). Effects of interleukin-3 after chemotherapy for advanced ovarian cancer. Blood, 80, 1141-1148.
8. Brooks, B. R., Bruccoleri, R. E., Olafson, B., States, D. J., Swaminathan, S. & Karplus, M. (1983). CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4, 187-217.
9. Brown, C. R., Pihl, C. E. & Kaushansky K. (1994). Mapping of human granulocyte-macrophage-colony-stimulating-factor domains interacting with the human granulocyte-macrophage-colony-stimulating-factor-receptor α-subunit. Eur. J. Biochem. 225, 873-880.
10. Brünger, A. T. (1988). Crystallographic refinement by simulated annealing. Application to a 2.8 Å resolution structure of aspartate aminotransferase. J. Mol. Biol. 203, 803-816.
11. Brünger, A. T. (1992). X-PLOR Version 3.1, A System for X-ray Crystallography and NMR, Yale University Press, New Haven, CT.
12. Carson, M. (1991). Ribbons 2.0. J. Appl. Crystallog. 24, 958-961.
13. Clore, G. M. & Gronenborn, A. M. (1987). Determination of three-dimensional structures of proteins in solution by nuclear magnetic resonance spectroscopy Protein Eng. 1, 275-288.
14. 1H NMR spectroscopy Biochemistry, 29, 7387-7401.
15. 15N NMR: comparisons with X-ray data for the Fab. Proteins: Struct. Funct. Genet. 15, 290-311.
16. Denzlinger, C., Walther, J., Wilmanns, W. & Gerhartz, H. H. (1993). Interleukin-3 enhances the endogenous leukotriene production. Blood, 81, 2466-2468.
17. de Vos, A. M., Ultsch, M. & Kossiakoff, A. A. (1992). Human growth hormone and extracellular domain of its receptor: crystal structure of the complex. Science, 255, 306-312.
18. Diederichs, K., Boone, T. & Karplus, P A. (1991). Novel fold and putative receptor binding site of granulocyte-macrophage colony-stimulating factor. Science, 254, 1779-1782.
19. Ding, D. X.-H., Rivas, C. I., Heaney M. L., Raines, M. A., Vera, J. C. & Golde, D. W. (1994). The alpha subunit of the human granulocyte-macrophage colony-stimulating factor receptor signals for glucose transport via a phosphorylation-independent pathway Proc. Natl Acad. Sci. USA, 91, 2537-2541.
20. Dorssers, L. C., Mostert, M. C., Burger, H., Janssen, C., Lemson, P. J., van Lambalgen, R., Wagemaker, G. & van Leen, R. W. (1991). Receptor and antibody interactions of human interleukin-3 characterized by mutational analysis. J. Biol. Chem. 266, 21310-21317.
21. Ealick, S. E., Cook W. J., Vijay-Kumar, S., Carson, M., Nagabhushan, T. L., Trotta, P. P. & Bugg, C. E. (1991). Three-dimensional structure of recombinant human interferon-gamma. Science, 252, 698-702.
22. 15N NMR relaxation. Biochemistry, 33, 5984-6003.
23. 15N NMR resonance assignments, secondary structure, and backbone topology of a variant of human interleukin-3. Biochemistry, 34, 6540-6551.
24. 1H nuclear magnetic resonance spectroscopy Biochemistry, 29, 1566-1572.
25. Freeman, J. J., Parr, G. R., Hecht, R. I., Morris, J. C. & McKearn, J. P (1991). Secondary structure of human interleukin-3. Int. J. Biochem. 23, 353-360.
26. Ganser, A. (1993). Clinical results with recombinant human interleukin-3. Cancer Invest. 11, 212-218.
27. Ganser, A., Lindemann, A., Seipelt, G., Ottman, O. G., Hermann, F., Eder, M., Frisch, J., Schulz, G., Mertlesmann, R. & Hoelzer, D. (1990). Effects of recombinant human interleukin-3 in patients with normal hematopoiesis and in patients with bone marrow failure. Blood, 76, 666-676.
28. Gearing, D. P., King, J. A., Gough, N. M. & Nicola, N. A. (1989). Expression cloning of a receptor for human granulocyte-macrophage colony-stimulating factor. EMBO J. 8, 3667-3676.
29. Gough, N. M. & Kelso, A. (1989). GM-CSF expression is preferential to multi-CSF (IL-3) expression in murine T lymphocyte clones. Growth factors, 1, 287-298.
30. Graber, P., Proudfoot, A. E. I., Talabot, F., Bernard, A., McKinnon, M., Banks, M., Fattah, D., Soalri, R., Peitsch, M. C. & Wells, T. N. C. (1995). Identification of key charged residues of human interleukin-5 in receptor binding and cellular activation. J. Biol. Chem. 270, 15762-15769.
31. Haak-Frendscho, M., Arai, N., Arai, K.-I., Baeza, M. L., Finn, M. & Kaplan, A. P. (1988). Human recombinant granulocyte-macrophage colony-stimulating factor and interleukin 3 cause basophil histamine release. J. Clin. Invest. 82, 17-20.
32. Hayashida, K., Kitamura, T., Gorman, D. M., Arai, K., Yokota, T. & 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. USA, 87, 9655-9659.
33. Herrmann, F., Brugger, W., Kanz, L. & Mertelsmann, R. (1992) . In vivo biology and therapeutic potential of hematopoietic growth factors and circulating progenitor cells. Semin. Oncol. 19, 422-431.
34. Hill, C. P., Osslund, T. D. & Eisenberg, D. (1993). The structure of granulocyte-colony-stimulating factor and its relationship to other growth factors. Proc. Natl Acad. Sci. USA, 90, 5167-5171.
35. 13C-labeled protein. J. Magn. Reson. 86, 204-209.
36. Jones, T. A., Zou, J. Y., Cowan, S. W. & Kjeldgaard, M. (1991). Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A, 47, 110-119.
37. Kabsch, W. & Sander, C. (1983). Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577-2637.
38. Kaushansky K., Shoemaker, S. G., Broudy V. C., Lin, N. L., Matous, J. V., Alderman, E. M., Aghajanian, J. D., Szklut, P. J., VanDyke, R. E., Pearce, M. K. & Abrams, J. S. (1992). Structure-function relationships of interleukin-3. J. Clin. Invest. 90, 1879-1888.
39. 15N-labeled proteins. J. Magn. Reson. 86, 110-126.
40. 15N inverse detected heteronuclear NMR spectroscopy Biochemistry, 28, 8972-8979.
41. Kay L. E., Keifer, P. & Saarinen, T. (1992). Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity J. Am. Chem. Soc. 114, 10663-10664.
42. 2O saturation. J. Magn. Reson. sect. A, 109, 129-133.
43. Kitamura, T. & Miyajima, A. (1992). Functional reconstitution of the human interleukin-3 receptor. Blood, 80, 84-90.
44. Kitamura, T., Sato, N., Arai, K.-I. & Miyajima, A. (1991). Expression cloning of the human IL-3 receptor cDNA reveals a shared (3 subunit for the human IL-3 and GM-CSF receptors. Cell, 66, 1165-1174.
45. 15N NMR spectroscopy Biochemistry, 31, 4856-4866.
46. Kraulis, P. J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.
47. Kraulis, P. J., Clore, G. M., Nilges, M., Jones, T. A., Pettersson, G., Knowles, J. & Gronenborn, A. M. (1989). Determination of the three-dimensional solution structure of the C-terminal domain of cellobiohydrolase I from Trichoderma reesei. A study using nuclear magnetic resonance and hybrid distance geometry-dynamical simulated annealing. Biochemistry, 28, 7241-7257.
48. Lee, B. & Richards, F. M. (1971). The interpretation of protein structures: estimation of static accessibility J. Mol. Biol. 55, 379-400.
49. Liepinsh, E., Otting, G. & Wüthrich, K. (1992). Contributions from hydration of carboxylate groups to the spectrum of water-polypeptide proton-proton Overhauser effects in aqueous solution. J. Biomol. NMR, 2, 447-465.
50. Lipari, G. & Szabo, A. (1982). Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. J. Am. Chem. Soc. 104, 4546-4559.
51. Lokker, N. A., Strittmatter, U., Steiner, C., Fagg, B., Graff, P., Kocher, H. P. & Zenke, G. (1991a). Mapping the epitopes of neutralizing anti-human IL-3 monoclonal antibodies: implications for structure-activity relationship. J. Immunol. 146, 893-898.
52. Lokker, N. A., Zenke, G., Strittmatter, U., Fagg, B. & Mora, N. R. (1991b). Structure-activity relationship study of human interleukin-3: role of the C-terminal region for biological activity EMBO J. 10, 2125-2131.
53. Lopez, A. F., Eglinton, J. M., Gillis, D., Park, L. S., Clark, S. & Vadas, M. A. (1989). Reciprocal inhibition of binding between interleukin-3 and granulocyte colony-stimulating factor to human eosinophils. Proc. Natl Acad. Sci. USA, 86, 7022-7026.
54. Lopez, A. F., Shannon, M. F., Barry, S., Phillips, J. A., Cambareri, B., Dottore, M., Simmons, P. & Vadas, M. A. (1992a). A human interleukin 3 analog with increased biological and binding activities. Proc. Natl Acad. Sci. USA, 89, 11842-11846.
55. Lopez, A. F., Shannon, M. F., Hercus, T., Nicola, N. A., Cambareri, B., Dottore, M., Layton, M. J., Eglinton, L. & Vadas, M. A. (1992b). 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, 909-916.
56. Lovejoy B., Cascio, D. & Eisenberg, D. (1993). Crystal structure of canine and bovine granulocyte-colony stimulating factor (G-CSF). J. Mol. Biol. 234, 640-653.
57. 15N-labeled proteins. J. Am. Chem. Soc. 111, 1515-1517.
58. McKay D. B. (1992). Response to commentary on unraveling the structure of IL-2. Science, 257, 412-413.
59. Metcalf, D. & Nicola, N. A. (1995). The Hemopoietic Colony-Stimulating Factors. From Biology to Clinical Applications, Cambridge University Press, Cambridge, UK.
60. Milburn, M. V., Hassell, A. M., Lambert, M. H., Jordan, S. R., Proudfoot, A. E. I., Graber, P. & Wells, T. N. C. (1993). A novel dimer configuration revealed by the crystal structure at 2.4 Å resolution of human interleukin-5. Nature, 363, 172-176.
61. Mott, H. R., Driscoll, P. C., Boyd, J., Cooke, R. M., Weir, M. P. & Campbell, I. D. (1992). Secondary structure of human interleukin 2 from 3D heteronuclear NMR experiments. Biochemistry, 31, 7741-7744.
62. Mui, A., Muto, A., Sakamaki, K., Sato, N., Kinoshita, T., Watanabe, S., Yokota, T., Arai, K. & Miyajima, A. (1994). Function of the common β subunit of the GM-CSF/IL-3/IL-5 receptors. Advan. Expt. Med. Biol. 365, 217-223.
63. Nilges, M. W. (1995). Calculation of protein structures with ambiguous distance restraints. Automated assignment of ambiguous NOE cross-peaks and disulphide connectivities. J. Mol. Biol. 245, 645-660.
64. Nilges, M. W., Clore, G. M. & Gronenborn, A. M. (1988). Determination of three-dimensional structures of proteins from interproton distance data by hybrid distance geometry-dynamical simulated annealing calculations. FEBS Letters, 229, 317-324.
65. Nishida, J., Yoshida, M., Arai, K. & Yokota, T. (1991). Definition of a GC-rich motif as regulatory sequence of the IL-3 gene by CLE2/GC box of the GM-CSF gene in T cell activation. Int. Immunol. 3, 245-254.
66. Olins, P. O., Bauer, S. C., Braford-Goldberg, S., Sterbenz, K., Polazzi, J. O., Caparon, M. H., Klein, B. K., Easton, A. M., Paik, K., Klover, J. A., Thiele, B. R. & McKearn, J. P. (1995). Saturation mutagenesis of human interleukin-3. J. Biol. Chem. 270, 23754-23760.
67. 13C heteronuclear NMR spectroscopy. J. Am. Chem. Soc. 113, 4371-4380.
68. Pandit, J., Bohm, A., Jancarik, J., Halenbeck, R., Koths, K. & Kim, S.-H. (1992). Three-dimensional structure of dimeric human recombinant macrophage colony-stimulating factor. Science, 258, 1358-1362.
69. Parry D., Minasian, E. & Leach, S. (1988). Conformational homologies among cytokines: interleukins and colony stimulating factors. J. Mol. Recog. 1, 107-110.
70. Parry, D., Minasian, E. & Leach, S. (1991). Cytokine conformations: predictive studies. J. Mol. Recog. 4, 63-75.
71. 2O. J. Magn. Reson. sect. B, 103, 197-201.
72. Powers, R., Garrett, D. S., March, C. J., Frieden, E. A., Gronenborn, A. M. & Clore, G. M. (1992). Three-dimensional solution structure of human interleukin-4 by multidimensional heteronuclear magnetic resonance spectroscopy. Science, 256, 1673-1677.
73. Quelle, F., Sato, N., Witthuhn, B., Inhorn, R., Eder, M., Miyajima, A., Griffin, J. & Ihle, J. (1994). 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, 4335-4341.
74. Redfield, C., Boyd, J., Smith, L. J., Smith, R. A. G. & Dobson, C. M. (1992). Secondary structure and topology of human interleukin 4 in solution. Biochemistry, 31, 10431-10437.
75. Robinson, R. C., Grey L. M., Staunton, D. Vankelecom, H., Vernallis, A. B., Moreau, J.-F., Stuart, D. I., Heath, J. K. & Jones, E. Y. (1994). The crystal structure and biological function of leukemia inhibitory factor: implications for receptor binding. Cell, 77, 1101-1016.
76. Rozwarski, D. A., Gronenborn, A. M., Clore, G. M., Bazan, J. F., Bohm, A., Wlodawer, A., Hatada, M. & Karplus, P. A. (1994). Structural comparisons among the short-chain helical cytokines. Structure, 2, 159-173.
77. Schneider, D. M., Dellwo, M. J. & Wand, A. J. (1992). Fast internal main-chain dynamics of human ubiquitin. Biochemistry, 31, 3645-3652.
78. Schrader, J. W. & Clark-Lewis, I. (1982). A T cell-derived factor stimulating multipotential hemopoietic stem cells; molecular weight and distinction from T cell growth factor and T cell-derived granulocyte-macrophage colony-stimulating factor. J. Immunol. 129, 30-35.
79. Senda, T., Shimazu, T., Matsuda, S., Kawano, G., Shimizu, H., Nakamura, K. T. & Mitsui, Y. (1992). Three-dimensional crystal structure of recombinant murine interferon-β. EMBO J. 11, 3193-3201.
80. Shanafelt, A. B., Johnson, K. E. & Kastelein, R. A. (1991a). Identification of critical residues in human and mouse granulocyte-macrophage colony-stimulating factor and their involvement in species specificity J. Biol. Chem. 266, 13804-13810.
81. Shanafelt, A. B., Miyajima, A., Kitamura, T. & Kastelein, R. A. (1991b). The amino-terminal helix of GM-CSF and IL-5 governs high affinity binding to their receptors. EMBO J. 10, 4105-4112.
82. Smith, L. J., Redfield, C., Boyd, J., Lawrence, G. M. P., Edwards, R. G., Smith, R. A. G. & Dobson, C. M. (1992). Human interleukin 4: the solution structure of a four-helix bundle protein. J. Mol. Biol. 224, 899-904.
83. Somers, W., Ultsch, M., de Vos, A. M. & Kossiakoff, A. A. (1994). The X-ray structure of a growth hormone-prolactin receptor complex. Nature, 372, 478-481.
84. 15N NMR relaxation measurements. Biochemistry, 31, 4394-4406.
85. Takaki, S., Murata, Y., Kitamura, T., Miyajima, A., Tominaga, A. & Takatsu, K. (1993). Reconstitution of the functional receptors for murine and human interleukin 5. J. Expt. Med. 177, 1523-1529.
86. Tavernier, J., Devos, R., Cornelis, S., Tuypens, T., Van der Heyden, J., Fiers, W. & 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.
87. Tavernier, J., Guisez, Y., Devos, R., Plaetinck, G., Heyden, J. van der & Oefner, C. (1994). Analysis of human interleukin-5 mutants: implications for receptor activation. Challenges Mod. Med. 8, 99-107.
88. Thomas, J. W., Baum, C. M., Hood, W. F., Klein, B. K., Monahan, J. B., Paik, K., Staten, N., Abrams, M. & McKearn, J. P (1995). Potent interleukin-3 receptor agonist with selectively enhanced hematopoietic activity relative to recombinant human interleukin-3. Proc. Natl Acad. Sci. USA, 92, 3779-3783.
89. Ultsch, M. H., Somers, W., Kossiakoff, A. A. & de Vos, A. M. (1994). The crystal structure of affinity-matured human growth hormone at 2 Å resolution. J. Mol. Biol. 236, 286-299.
90. Walter, M. R. & Nagabhushan, T. L. (1995). Crystal structure of interleukin 10 reveals an Interferon γ-like fold. Biochemistry, 34, 12118-12125.
91. Walter, M. R., Cook, W. J., Ealick, S. E., Nagabhushan, T. L., Trotta, P. P. & Bugg, C. E. (1992). Three-dimensional structure of recombinant human granulocyte-macrophage colony-stimulating factor. J. Mol. Biol. 224, 1075-1085.
92. Werner, J. M., Breeze, A. L., Kara, B., Rosenbrock, G., Boyd, J., Soffe, N. & Campbell, I. D. (1994). Secondary structure and backbone dynamics of human granulocyte colony-stimulating factor in solution. Biochemistry, 33, 7184-7192.
93. Wlodawer, A., Pavlovsky, A. & Gutschina, A. (1992). Crystal structure of human recombinant interleukin-4 at 2.25 Å resolution. FEBS Letters, 309, 59-64.
94. Woodcock, J. M., Zacharakis, B., Plaetinck, G., Bagley, C. J., Qiyu, S., Hercus, T. R., Tavernier, J. & 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.
95. Wüthrich, K. (1986). NMR of Proteins and Nucleic Acids. Wiley New York.
96. Yang, Y.-C., Ciarletta, A. B., Temple, P. A., Chung, M. P., Kovacic, S., Witek-Glannotti, J. S., Leary A. C., Kriz, R., Donahue, R. E., Wong, G. G. & Clark, S. C. (1986). Human IL-3 (multi-CSF): identification by expression cloning of a novel hematopoietic growth factor related to murine IL-3. Cell, 47, 3-10.
97. Zink, T., Ross, A., Ambrosius, D., Rudolph, R. & Holak, T. A. (1992). Secondary structure of human granulocyte colony-stimulating factor derived from NMR spectroscopy FEBS Letters, 314, 435-439.
98. Zink, T., Ross, A., Lüers, K., Cieslar, C., Rudolph, R. & Holak, T. A. (1994). Structure and dynamics of the human granulocyte colony-stimulating factor determined by NMR spectroscopy Loop mobility in a four-helix-bundle protein. Biochemistry, 33, 8453-8463.
99. Zuiderweg, E. R. P. & Fesik, S. W. (1989). Heteronuclear three-dimensional NMR spectroscopy of the inflammatory protein C5a. Biochemistry, 28, 2387-2391.