Functional impact of manipulation on the relative orientation of human prolactin receptor domains

Biochemistry

Volumn 50, Issue 23, 2011, Pages 5333-5344

  Liu, Wei ^a   Brooks, Charles L ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLASS 1; COEXPRESSED; CYTOKINE RECEPTOR; EXTRACELLULAR; HORMONE BINDING; HUMAN EMBRYONIC KIDNEYS; HUMAN ERYTHROPOIETIN; HUMAN GROWTH HORMONE; INCREASED FLEXIBILITY; JANUS KINASE 2; MOLECULAR MECHANISM; PISTON MOVEMENT; PROLACTIN RECEPTORS; RECEPTOR ACTIVITY; RELATIVE ORIENTATION; ROTATION MECHANISM; SPATIAL RELATIONSHIPS; TRANSMEMBRANES; TWO DOMAINS; WILD TYPES;

DIMERS; ENZYME ACTIVITY; PHOSPHORYLATION; ROTATION;

AMINO ACIDS;

ALANINE; GLYCINE; HOMODIMER; JANUS KINASE 2; MUTANT PROTEIN; PROLACTIN; PROLACTIN RECEPTOR;

AMINO ACID SEQUENCE; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN VARIANT; WILD TYPE;

CELLS, CULTURED; HUMANS; JANUS KINASE 2; MUTATION; PHOSPHORYLATION; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, PROLACTIN;

EID: 79958833444     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101931u     Document Type: Article

References (55)

1. Bazan, J. F. (1990) Structural design and molecular evolution of a cytokine receptor superfamily Proc. Natl. Acad. Sci. U.S.A. 87, 6934-6938
2. Bole-Feysot, C., Goffin, V., Edery, M., Binart, N., and Kelly, P. A. (1998) Prolactin (PRL) and its receptor: Actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice Endocr. Rev. 19, 225-268 (Pubitemid 29117815)
3. Hooper, K. P., Padmanabhan, R., and Ebner, K. E. (1993) Expression of the extracellular domain of the rat liver prolactin receptor and its interaction with ovine prolactin J. Biol. Chem. 268, 22347-22352 (Pubitemid 23318278)
4. Goffin, V. and Kelly, P. A. (1997) The prolactin/growth hormone receptor family: Structure/function relationships Journal of Mammary Gland Biology and Neoplasia 2, 7-17 (Pubitemid 127717408)
5. Clevenger, C. V. and Kline, J. B. (2001) Prolactin receptor signal transduction Lupus 10, 706-718 (Pubitemid 33041663)
6. Chilton, B. S. and Hewetson, A. (2005) Prolactin and growth hormone signaling Curr. Top. Dev. Biol. 68, 1-23 (Pubitemid 43588865)
7. Kelly, P. A., Djiane, J., Postel-Vinary, M. C., and Edery, M. (1991) The prolactin/growth hormone receptor family Endocr. Rev. 12, 235-251
8. Nagano, M. and Kelly, P. A. (1992) Absence of a putative ATP/GTP binding site in the rat prolactin receptor Biochem. Biophys. Res. Commun. 183, 610-618
9. Cambell, G. S., Argetsinger, L. S., Ihle, J. N., Kelly, P. A., Rillema, J. A., and Carter-Su, C. (1994) Activation of JAK2 tyrosine kinase by prolactin receptor in Nb2 cells and mouse mammary gland explants Proc. Natl. Acad. Sci. U.S.A. 91, 5232-5236 (Pubitemid 24174300)
10. Rui, H., Kirken, R. A., and Farrar, W. L. (1994) Activation of receptor-associated tyrosine kinase JAK2 by prolactin J. Biol. Chem. 269, 5364-5368 (Pubitemid 24239533)
11. Lebrun, J. J., Ali, S., Sofer, L., Ullrich, A., and Kelly, P. A. (1994) Prolactin-induced proliferation in Nb2 cells involves tyrosine phosphorylation of the prolactin receptor and its associated tyrosine kinase J. Biol. Chem. 269, 14021-14026
12. Ren, R., Mayer, B. J., Cicchetti, P., and Baltimore, D. (1993) Identification of ten amino acid proline-rich SH3 binding site Science 259, 1157-1161 (Pubitemid 23085353)
13. Lebrun, J. J., Ali, S., Ullrich, A., and Kelly, P. A. (1995) Proline-rich sequence-mediated JAK2 association to the prolactin receptor is required but not sufficient for signal transduction J. Biol. Chem. 270, 10664-10670
14. Pezet, A., Buteau, H., Kelly, P. A., and Edery, M. (1997) The last proline of Box 1 is essential for association with JAK2 and functional activation of the prolactin receptor Mol. Cell. Endocrinol. 129, 199-208 (Pubitemid 27281535)
15. Wakao, H., Gouilleux, F., and Groner, B. (1994) Mammary gland factor (MGF) is a novel member of the cytokine regulated transcription factor gene family and confers the prolactin response EMBO J. 13, 2182-2191 (Pubitemid 24139732)
16. Gouilleux, F., Wakao, H., Mundt, M., and Groner, B. (1994) Prolactin induces phosphorylation of Tyr694 of STAT5 (MGF), a prerequisite for DNA binding and induction of transcription EMBO J. 13, 4361-4369 (Pubitemid 24295208)
17. Rui, H., Lebrun, J. J., Kirken, R. A., Kelly, P. A., and Farrar, W. L. (1994) JAK2 activation and cell proliferation induced by antibody-mediated prolactin receptor dimerization Endocrinology 135, 1299-1306 (Pubitemid 24307502)
18. Gertler, A., Grosclaude, J., Strasburger, C. J., Nir, S., and Djiane, J. (1996) Real-time kinetic measurements of the interactions between lactogenic hormones and prolactin-receptor extracellular domains from several species support the model of hormone-induced transient receptor dimerization J. Biol. Chem. 271, 24482-24491 (Pubitemid 26333184)
19. Livnah, O., Stura, E. A., Middleton, S. A., Johnson, D. L., Jolliffe, L. K., and Wilson, I. A. (1999) Crystallographic evidence for preformed dimers of erythropoietin receptor before ligand activation Science 283, 987-990
20. Constantinescu, S. N., Keren, T., Socolovsky, M., Nam, H.-S., Henis, Y. I., and Lodish, H. F. (2001) Ligand-independent oligomerization of cell-surface erythropoietin receptor is mediated by the transmembrane domain Proc. Natl. Acad. Sci. U.S.A. 98, 4379-4384 (Pubitemid 32294985)
21. Gent, J., van Kerkhof, P., Roza, M., Bu, G., and Strous, G. J. (2002) Ligand-independent growth hormone receptor dimerization occurs in the endoplasmic reticulum and is required for ubiquitin system-dependent endocytosis Proc. Natl. Acad. Sci. U.S.A. 99, 9858-9863 (Pubitemid 34831137)
22. Brown, R. J., Adams, J. J., Pelekanos, R. A., Wan, Y., McKinstry, W. J., Palethorpe, K., Seeber, R. M., Monks, T. A., Eidne, K. A., Parker, M. W., and Waters, M. J. (2005) Model for growth hormone receptor activation based on subunit rotation within a receptor dimer Nat. Struct. Mol. Biol. 12, 814-821 (Pubitemid 43086257)
23. Qazi, A. M., Tsai-Morris, C-H, and Dufau, M. L. (2006) Ligand-independent homo- and heterodimerization of human prolactin receptor variants: Inhibitory action of the short forms by heterodimerization Mol. Endocrinol. 20, 1912-1923 (Pubitemid 44148093)
24. Gadd, S. L. and Clevenger, C. V. (2006) Ligand-independent dimerization of the human prolactin receptor isoforms: Functional implications Mol. Endocrinol. 20, 2734-2746 (Pubitemid 44833532)
25. Li, Y., Kumar, K. G., Tang, W., Spiegelman, V. S., and Fuchs, S. Y. (2004) Negative regulation of prolactin receptor stability and signaling mediated by SCF(β-TrCP) E3 ubiquitin ligase Mol. Cell. Biol. 24, 4038-4048 (Pubitemid 38496180)
26. Varghese, B., Barriere, H., Carbone, C. J., Banerjee, A., Swaminathan, G., Plotnikov, A., Xu, P., Peng, J., Goffin, V., Lukacs, G. L., and Fuchs, S. Y. (2008) Polyubiquitination of prolactin receptor stimulates its internalization, postinternalization sorting, and degradation via the lysosomal pathway Mol. Cell. Biol. 28, 5275-5287
27. Clevenger, C. V., Gadd, S. L., and Zheng, J. (2009) New mechanisms for PRLr action in breast cancer Trends Endocrinol. Metab. 20, 223-229
28. Remy, I., Wilson, I. A., and Michnick, S. W. (1999) Erythropoietin receptor activation by a ligand-induced conformation change Science 283, 990-993
29. 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
30. Kossiakoff, A. A., Somers, W., Ultsch, M., Andow, K., Muller, Y. A., and De Vos, A. M. (1994) Comparison of the intermediate complexes of human growth hormone bound to the human growth hormone and prolactin receptors Protein Sci. 3, 1697-1704
31. Ottemann, K. M., Xiao, W., Shin, Y. K., and Koshland, D. E. (1999) A piston model for transmembrane signaling of the aspartate receptor Science 285, 1751-1754 (Pubitemid 29428878)
32. van Agthoven, J., Zhang, C., Tallet, E., Raynal, B., Hoos, S., Baron, B., England, P., Goffin, V., and Broutin, I. (2010) Structural characterization of the stem-stem dimerization interface between prolactin receptor chains complexed with the natural hormone J. Mol. Biol. 404, 112-126
33. Constantinescu, S. N., Huang, L.-J., Nam, H., and Lodish, H. F. (2001) The erythropoietin receptor cytosolic juxtamembrane domain contains an essential, precisely oriented, hydrophobic motif Mol. Cell 7, 377-385 (Pubitemid 32206505)
34. Padmanabhan, S., Marqusee, S., Ridgeway, T., Laue, T. M., and Baldwin, R. L. (1990) Relative helix-forming tendencies of nonpolar amino acids Nature 344, 268-270
35. Waters, M. J., Hoang, H. N., Fairlie, D. P., Pelekanos, R. A., and Brown, R. J. (2006) New insights into growth hormone action J. Mol. Endocrinol. 36, 1-7 (Pubitemid 43273660)
36. Lennon, G. G., Auffray, C., Polymeropoulos, M., and Soares, M. B. (1996) The I.M.A.G.E. consortium: An integrated molecular analysis of genomes and their expression Genomics 33, 151-152
37. Graham, F. L., Smiley, J., Russell, W. C., and Nairn, R. (1977) Characteristics of a human cell line transformed by DNA from human adenovirus type 5 J. Gen. Virol. 36, 59-74
38. Peterson, F. C., Anderson, P. J., Berliner, L. J., and Brooks, C. L. (1999) Expression, folding, and characterization of small proteins with increasing disulfide complexity by a pT7-7-derived phagemid Protein Expression Purif. 15, 16-23 (Pubitemid 29321464)
39. Lee, R. C., Walters, J. A., Reyland, M. E., and Anderson, S. M. (1999) Constitutive activation of the prolactin receptor results in the induction of growth factor-independent proliferation and constitutive activation of signaling molecules J. Biol. Chem. 274, 10024-10034
40. Neilson, L. M., Zhu, J., Xie, J., Malabarba, M. G., Sakamoto, K., Wagner, K., Kirken, R. A., and Rui, H. (2007) Coactivation of Jak1 positively modulates prolactin-Jak2 signaling in breast cancer: Recruitment of ERK and Stat3 and enhancement of Akt and Stat5a/b pathways Mol. Endocrinol. 21, 2218-2232 (Pubitemid 47347383)
41. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72, 248-254
42. Watowich, S. S., Wu, H., Socolovsky, M., Klingmuller, U., Constantinescu, S. N., and Lodish, H. F. (1996) Cytokine receptor signal transduction and the control of hematopoietic cell development Annu. Rev. Cell Dev. Biol. 12, 91-128 (Pubitemid 26422710)
43. Elliott, S., Lorenzini, T., Yanagihara, D., Chang, D., and Elliott, G. (1996) Activation of the erythropoietin (EPO) receptor by bivalent anti-EPO receptor antibodies J. Biol. Chem. 271, 24691-24697 (Pubitemid 26333213)
44. Fuh, G., Cunningham, B. C., Fukunaga, R., Nagata, S., Goeddel, D. V., and Wells, J. A. (1992) Rational design of potent antagonists to the human growth hormone receptor Science 256, 1677-1680
45. Yoshimura, A., Longmore, G., and Lodish, H. F. (1990) Point mutation in the exoplasmic domain of the erythropoietin receptor resulting in hormone-independent activation and tumorigenicity Nature 348, 647-649 (Pubitemid 120015129)
46. Watowich, S. S., Yoshimura, A., Longmore, G. D., Hilton, D. J., Yoshimura, Y., and Lodish, H. F. (1992) Homodimerization and constitutive activation of the erythropoietin receptor Proc. Natl. Acad. Sci. U.S.A. 89, 2140-2144
47. Watowich, S. S., Hilton, D. J., and Lodish, H. F. (1994) Activation and inhibition of erythropoietin receptor function: Role of receptor dimerization Mol. Cell. Biol. 14, 3535-3549 (Pubitemid 24160761)
48. Cunningham, B. C., Ultsch, M., De Vos, A. M., Mulkerrin, M. G., Clauser, K. R., and Wells, J. A. (1991) Dimerization of the Extracellular Domain of the Human Growth Hormone Receptor by a Single Hormone Molecule Science 254, 821-825 (Pubitemid 21917402)
49. Sivaprasad, U., Canfield, J. M., and Brooks, C. L. (2004) Mechanism for ordered receptor binding by human prolactin Biochemistry 43, 13755-13765 (Pubitemid 39431059)
50. Rowlinson, S. W., Behncken, S. N., Rowland, J. E., Clarkson, R. W., Strasburger, C. J., Wu, Z., Baumbach, W., and Waters, M. J. (1998) Activation of chimeric and full-length growth hormone receptors by growth hormone receptor monoclonal antibodies. A specific conformational change may be required for full-length receptor signaling J. Biol. Chem. 273, 5307-5314 (Pubitemid 28108697)
51. Somers, W., Ultsch, M., De Vos, A. M., and Kossiakoff, A. A. (1994) The X-ray structure of a growth hormone-prolactin receptor complex Nature 372, 478-481
52. Broutin, I., Jomain, J. B., Tallet, E., van Agthoven, J., Raynal, B., Hoos, S., Kragelund, B. B., Kelly, P. A., Ducruix, A., England, P., and Goffin, V. (2010) 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
53. Falke, J. J. and Hazelbauer, G. L. (2001) Transmembrane signaling in bacterial chemoreceptors Trends Biochem. Sci. 26, 257-265 (Pubitemid 32289244)
54. Kline, J. B., Rycyzyn, M. A., and Clevenger, C. V. (2002) Characterization of a novel and functional human prolactin receptor isoform (deltaS1PRLr) containing only one extracellular fibronectin-like domain Mol. Endocrinol. 16, 2310-2322 (Pubitemid 35155542)
55. Gourdou, I., Gabou, L., Paly, J., Kermabon, A. Y., Belair, L., and Djiane, J. (1996) Development of a constitutively active mutant form of the prolactin receptor, a member of the cytokine receptor family Mol. Endocrinol. 10, 45-56 (Pubitemid 26023773)