A combined computational and structural model of the full-length human prolactin receptor

Nature Communications

Volumn 7, Issue , 2016, Pages

  Bugge, Katrine ^a   Papaleo, Elena ^a   Haxholm, Gitte W ^a   Hopper, Jonathan T S ^b   Robinson, Carol V ^b   Olsen, Johan G ^a   Lindorff Larsen, Kresten ^a   Kragelund, Birthe B ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE RECEPTOR; CYTOKINE RECEPTOR CLASS I; PROLACTIN RECEPTOR; UNCLASSIFIED DRUG;

ARCHITECTURE; COMPUTER SIMULATION; DOMAIN STRUCTURE; MASS SPECTROMETRY; MODELING; NUCLEAR MAGNETIC RESONANCE; PROTEIN; X-RAY;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CARBOXY TERMINAL SEQUENCE; COMPUTATIONAL MODEL; CRYSTAL STRUCTURE; DIMERIZATION; HETERONUCLEAR NUCLEAR MAGNETIC RESONANCE; HUMAN; HYDRODYNAMICS; HYDROGEN BOND; LIGAND BINDING; MASS SPECTROMETRY; MATHEMATICAL MODEL; MICELLE; NATIVE MASS SPECTROMETRY; NITROGEN NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; OLIGOMERIZATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN SECONDARY STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SIZE EXCLUSION CHROMATOGRAPHY; STRUCTURAL MODEL; X RAY CRYSTALLOGRAPHY; ALPHA HELIX; CHEMISTRY; ISOLATION AND PURIFICATION; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROCEDURES; PROTEIN DOMAIN; SMALL ANGLE SCATTERING;

CRYSTALLOGRAPHY, X-RAY; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MICELLES; MODELS, MOLECULAR; PROTEIN CONFORMATION, ALPHA-HELICAL; PROTEIN DOMAINS; RECEPTORS, PROLACTIN; SCATTERING, SMALL ANGLE;

EID: 84968764921     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11578     Document Type: Article

References (70)

1. Bole-Feysot, C., Goffin, V., Edery, M., Binart, N. & Kelly, P. A. Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr. Rev. 19, 225-268 (1998).
2. Ben-Jonathan, N., Hugo, E. R., Brandebourg, T. D. & LaPensee, C. R. Focus on prolactin as a metabolic hormone. Trends Endocrinol. Metab. 17, 110-116 (2006).
3. Ormandy, C. J. et al. Null mutation of the prolactin receptor gene produces multiple reproductive defects in the mouse. Genes Dev. 11, 167-178 (1997).
4. Gillam, M. P., Molitch, M. E., Lombardi, G. & Colao, A. Advances in the treatment of prolactinomas. Endocr. Rev. 27, 485-534 (2006).
5. Bernard, V., Young, J., Chanson, P. & Binart, N. New insights in prolactin: pathological implications. Nat. Rev. Endocrinol 11, 265-275 (2015).
6. Carver, K. C., Arendt, L. M. & Schuler, L. A. Complex prolactin crosstalk in breast cancer: new therapeutic implications. Mol. Cell. Endocrinol. 307, 1-7 (2009).
7. Clevenger, C. V., Gadd, S. L. & Zheng, J. New mechanisms for PRLr action in breast cancer. Trends Endocrinol. Metab. 20, 223-229 (2009).
8. Sackmann-Sala, L. & Goffin, V. in Recent Advances in Prolactin Research. (ed. Diakonova, M.), 221-242. (Springer, 2015).
9. Liongue, C. & Ward, A. C. Evolution of class I cytokine receptors. BMC Evol. Biol. 7, 1-15 (2007).
10. Haxholm, G. W. et al. Intrinsically disordered cytoplasmic domains of two cytokine receptors mediate conserved interactions with membranes. Biochem. J. 468, 495-506 (2015).
11. Olsen, J. G. & Kragelund, B. B. Who climbs the tryptophan ladder? On the structure and function of the WSXWS motif in cytokine receptors and thrombospondin repeats. Cytokine Growth Factor Rev. 25, 337-341 (2014).
12. Dagil, R. et al. The WSXWS motif in cytokine receptors is a molecular switch involved in receptor activation: Insight from structures of the prolactin receptor. Structure 20, 270-282 (2012).
13. Lebrun, J.-J., Ali, S., Ullrich, A. & Kelly, P. A. Proline-rich sequence-mediated Jak2 association to the prolactin receptor is required but not sufficient for signal transduction. J. Biol. Chem. 270, 10664-10670 (1995).
14. Goupille, O., Daniel, N., Bignon, C., Jolivet, G. & Djiane, J. Prolactin signal transduction to milk protein genes: carboxy-terminal part of the prolactin receptor and its tyrosine phosphorylation are not obligatory for JAK2 and STAT5 activation. Mol. Cell. Endocrinol. 127, 155-169 (1997).
15. DaSilva, L., Howard, O. M., Rui, H., Kirken, R. A. & Farrar, W. L. Growth signaling and JAK2 association mediated by membrane-proximal cytoplasmic regions of prolactin receptors. J. Biol. Chem. 269, 18267-18270 (1994).
16. Gadd, S. L. & Clevenger, C. V. Ligand-independent dimerization of the human prolactin receptor isoforms: functional implications. Mol. Endocrinol. 20, 2734-2746 (2006).
17. Brooks, A. J. et al. Mechanism of activation of protein kinase JAK2 by the growth hormone receptor. Science 344, 1249783-1249783 (2014).
18. Qazi, A. M., Tsai-Morris, C.-H. & Dufau, M. L. Ligand-independent homo- and heterodimerization of human prolactin receptor variants: inhibitory action of the short forms by heterodimerization. Mol. Endocrinol. 20, 1912-1923 (2006).
19. Broutin, I. et al. Crystal structure of an affinity-matured prolactin complexed to its dimerized receptor reveals the topology of hormone binding site 2. J. Biol. Chem. 285, 8422-8433 (2010).
20. van Agthoven, J. et al. Structural characterization of the stem-stem dimerization interface between prolactin receptor chains complexed with the natural hormone. J. Mol. Biol. 404, 112-126 (2010).
21. Jomain, J.-B. et al. Structural and thermodynamic bases for the design of pure prolactin receptor antagonists: X-ray structure of Del1-9-G129R-hPRL. J. Biol. Chem. 282, 33118-33131 (2007).
22. Teilum, K. et al. Solution structure of human prolactin. J. Mol. Biol. 351, 810-823 (2005).
23. Brown, R. J. et al. Model for growth hormone receptor activation based on subunit rotation within a receptor dimer. Nat. Struct. Mol. Biol. 12, 814-821 (2005).
24. Liu, W. & Brooks, C. Functional impact of manipulation on the relative orientation of human prolactin receptor domains. Biochemistry 50, 5333-5344 (2011).
25. Toyoshima, C., Nakasako, M., Nomura, H. & Ogawa, H. Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 A resolution. Nature 405, 647-655 (2000).
26. Cherezov, V. et al. High-resolution crystal structure of an engineered human b2-adrenergic G protein-coupled receptor. Science 318, 1258-1265 (2007).
27. Bugge, K., Steinocher, H., Brooks, A. J., Lindorff-Larsen, K. & Kragelund, B. B. Exploiting hydrophobicity for efficient production of transmembrane helices for structure determination by NMR spectroscopy. Anal. Chem. 87, 9126-9131 (2015).
28. Rath, A., Glibowicka, M., Nadeau, V. G., Chen, G. & Deber, C. M. Detergent binding explains anomalous SDS-PAGE migration of membrane proteins. Proc. Natl Acad. Sci. U.S.A. 106, 1760-1765 (2009).
29. Laganowsky, A., Reading, E., Hopper, J. T. S. & Robinson, C. V. Mass spectrometry of intact membrane protein complexes. Nat. Protoc. 8, 639-651 (2013).
30. Schwarzinger, S. et al. Sequence-dependent correction of random coil NMR chemical shifts. J. Am. Chem. Soc. 123, 2970-2978 (2001).
31. Shen, Y. & Bax, A. Identification of helix capping and beta-turn motifs from NMR chemical shifts. J. Biomol. NMR 52, 211-232 (2012).
32. Shen, Y. & Bax, A. Protein backbone chemical shifts predicted from searching a database for torsion angle and sequence homology. J. Biomol. NMR 38, 289-302 (2007).
33. Vuister, G. W. & Bax, A. Quantitative J correlation-a new approach for measuring homonuclear 3-bond J(H(N)H(Alpha) coupling-constants in 15N-enriched proteins. J. Am. Chem. Soc. 115, 7772-7777 (1993).
34. Rieping, W., Bardiaux, B., Bernard, A., Malliavin, T. E. & Nilges, M. ARIA2: automated NOE assignment and data integration in NMR structure calculation. Bioinformatics 23, 381-382 (2007).
35. Brünger, A. T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. Sect. D Biol. Crystallogr. 54, 905-921 (1998).
36. Svensson, L. A. et al. Crystal structure of a prolactin receptor antagonist bound to the extracellular domain of the prolactin receptor. J. Biol. Chem. 283, 19085-19094 (2008).
37. Kulkarni, M. V. et al. Two independent histidines, one in human prolactin and one in its receptor, are critical for pH-dependent receptor recognition and activation. J. Biol. Chem. 285, 38524-38533 (2010).
38. Kossiakoff, A. A. et al. Ternary complex between placental lactogen and the extracellular domain of the prolactin receptor. Nat. Struct. Biol 7, 808-815 (2000).
39. Svergun, D., Barberato, C. & Koch, M. H. J. CRYSOL-a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr 28, 768-773 (1995).
40. Ozenne, V. et al. Flexible-meccano: a tool for the generation of explicit ensemble descriptions of intrinsically disordered proteins and their associated experimental observables. Bioinformatics 28, 1463-1470 (2012).
41. Weidemann, T., Höfinger, S., Müller, K. & Auer, M. Beyond dimerization: a membrane-dependent activation model for interleukin-4 receptor-mediated signalling. J. Mol. Biol. 366, 1365-1373 (2007).
42. van Meer, G. & de Kroon, A. I. P. M. Lipid map of the mammalian cell. J. Cell Sci. 124, 5-8 (2011).
43. Fernández, C., Hilty, C., Wider, G. & Wüthrich, K. Lipid-protein interactions in DHPC micelles containing the integral membrane protein OmpX investigated by NMR spectroscopy. Proc. Natl Acad. Sci. U.S.A. 99, 13533-13537 (2002).
44. Kuèerka, N., Nieh, M. P. & Katsaras, J. Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature. Biochim. Biophys. Acta-Biomembr. 1808, 2761-2771 2011.
45. The Uniprot Consortium. UniProt: a hub for protein information. Nucleic Acids Res. 43, D204-D212 (2015).
46. Tallet, E. et al. Investigation of prolactin receptor activation and blockade using time-resolved fluorescence resonance energy transfer. Front. Endocrinol. (Lausanne) 2, 1-17 (2011).
47. Arkin, I. T. & Brunger, A. T. Statistical analysis of predicted transmembrane alpha-helices. Biochim. Biophys. Acta-Protein Struct. Mol. Enzymol. 1429, 113-128 (1998).
48. Momany, C. et al. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nature 3, 842-848 (1996).
49. de Planque, M. R. R. & Killian, J. A. Protein-lipid interactions studied with designed transmembrane peptides: role of hydrophobic matching and interfacial anchoring. Mol. Membr. Biol. 20, 271-284 (2003).
50. Kim, S. et al. Transmembrane glycine zippers: physiological and pathological roles in membrane proteins. Proc. Natl Acad. Sci. U.S.A. 102, 14278-14283 (2005).
51. Li, Q., Wong, Y. L., Huang, Q. & Kang, C. Structural insight into the transmembrane domain and the juxtamembrane region of the erythropoietin receptor in micelles. Biophys. J. 107, 2325-2336 (2014).
52. Li, Q., Lei Wong, Y., Yueqi Lee, M., Li, Y. & Kang, C. Solution structure of the transmembrane domain of the mouse erythropoietin receptor in detergent micelles. Sci. Rep. 5, 1-10 (2015).
53. Adamian, L. & Liang, J. Interhelical hydrogen bonds and spatial motifs in membrane proteins: polar clamps and serine zippers. Proteins Struct. Funct. Genet. 47, 209-218 (2002).
54. Ulmschneider, M. B. & Sansom, M. S. Amino acid distributions in integral membrane protein structures. Biochim. Biophys. Acta 1512, 1-14 (2001).
55. He, K. et al. Janus kinase 2 determinants for growth hormone receptor association, surface assembly, and signaling. Mol. Endocrinol. 17, 2211-2227 (2003).
56. Wallweber, H. J. A., Tam, C., Franke, Y., Starovasnik, M. A. & Lupardus, P. J. Structural basis of recognition of interferon-a receptor by tyrosine kinase 2. Nat. Struct. Mol. Biol. 21, 443-448 (2014).
57. Bah, A. et al. Folding of an intrinsically disordered protein by phosphorylation as a regulatory switch. Nature 519, 106-109 (2015).
58. Hernández, H. & Robinson, C. V. Determining the stoichiometry and interactions of macromolecular assemblies from mass spectrometry. Nat. Protoc. 2, 715-726 (2007).
59. Delaglio, F. et al. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995).
60. Vranken, W. F. et al. The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins Struct. Funct. Bioinform. 59, 687-696 (2005).
61. Orekhov, V. Y. & Jaravine, V. A. Analysis of non-uniformly sampled spectra with multi-dimensional decomposition. Prog. Nucl. Magn. Reson. Spectrosc. 59, 271-292 (2011).
62. Veglia, G., Zeri, A. C., Ma, C. & Opella, S. J. Deuterium/hydrogen exchange factors measured by solution nuclear magnetic resonance spectroscopy as indicators of the structure and topology of membrane proteins. Biophys. J. 82, 2176-2183 (2002).
63. Doreleijers, J. F. et al. CING: an integrated residue-based structure validation program suite. J. Biomol. NMR 54, 267-283 (2012).
64. Oxenoid, K. & Chou, J. J. The structure of phospholamban pentamer reveals a channel-like architecture in membranes. Proc. Natl Acad. Sci. U.S.A. 102, 10870-10875 (2005).
65. Konarev, P. V., Petoukhov, M. V., Volkov, V. V. & Svergun, D. I. ATSAS 2.1, a program package for small-angle scattering data analysis. J. Appl. Crystallogr. 39, 277-286 (2006).
66. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
67. Jones, J. A., Wilkins, D. K., Smith, L. J. & Dobson, C. M. Characterisation of protein unfolding by NMR diffusion measurements. J. Biomol. NMR 10, 199-203 (1997).
68. Danielsson, J., Jarvet, J., Damberg, P. & Gräslund, A. Two-site binding of b-cyclodextrin to the Alzheimer Ab(1-40) peptide measured with combined PFG-NMR diffusion and induced chemical shifts. Biochemistry 43, 6261-6269 (2004).
69. Ortega, A., Amorós, D. & García De La Torre, J. Prediction of hydrodynamic and other solution properties of rigid proteins from atomic- and residue-level models. Biophys. J. 101, 892-898 (2011).
70. Šali, A. & Blundell, T. L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815 (1993).