Divergent sequence tunes ligand sensitivity in phospholipid-regulated hormone receptors

Journal of Biological Chemistry

Volumn 288, Issue 28, 2013, Pages 20702-20712

  Musille, Paul M ^a   Pathak, Manish ^a   Lauer, Janelle L ^b   Griffin, Patrick R ^b   Ortlund, Eric A ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION FUNCTIONS; BIOCHEMICAL METHODS; GLUCOSE HOMEOSTASIS; NEOPLASTIC DISEASE; SEQUENCE VARIATIONS; STRUCTURAL EVIDENCE; STRUCTURAL MECHANISMS; THERAPEUTIC POTENTIALS;

GLUCOSE; MAMMALS; MASS SPECTROMETRY; PHOSPHOLIPIDS; PHYSIOLOGY;

LIGANDS;

LIVER RECEPTOR HOMOLOG 1; PHOSPHOLIPID;

ARTICLE; CONTROLLED STUDY; DROSOPHILA; EVOLUTIONARY ADAPTATION; GENE ACTIVATION; GENETIC VARIABILITY; GLUCOSE METABOLISM; HUMAN VERSUS ANIMAL COMPARISON; LIGAND BINDING; LIPID METABOLISM; METABOLIC REGULATION; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; SEQUENCE HOMOLOGY;

DIABETES; GLUCOSE METABOLISM; HORMONE RECEPTORS; MOUSE; PHOSPHATIDYLCHOLINE; PHOSPHOLIPID;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENETIC VARIATION; HUMANS; LIGANDS; MASS SPECTROMETRY; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHATIDYLGLYCEROLS; PHOSPHOLIPIDS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS;

EID: 84880070982     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.472837     Document Type: Article

References (46)

1. Fernandez-Marcos, P. J., Auwerx, J., and Schoonjans, K. (2011) Emerging actions of the nuclear receptor LRH-1 in the gut. Biochim. Biophys. Acta 1812, 947-955
2. Musille, P. M., Kohn, J. A., and Ortlund, E. A. (2013) Phospholipid-driven gene regulation. FEBS Lett. 587, 1238-1246
3. Parker, K. L., and Schimmer, B. P. (1997) Steroidogenic factor 1: a key determinant of endocrine development and function. Endocr. Rev. 18, 361-377 (Pubitemid 27246881)
4. Hammer, G. D., and Ingraham, H. A. (1999) Steroidogenic factor-1: its role in endocrine organ development and differentiation. Front. Neuroendocrinol. 20, 199-223 (Pubitemid 29362642)
5. Ueda, H., Sonoda, S., Brown, J. L., Scott, M. P., and Wu, C. (1990) A sequence-specific DNA-binding protein that activates fushi tarazu segmentation gene expression. Genes Dev. 4, 624-635
6. Takahashi, K., and Yamanaka, S. (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676 (Pubitemid 44233629)
7. Yu, J., Vodyanik, M. A., Smuga-Otto, K., Antosiewicz-Bourget, J., Frane, J. L., Tian, S., Nie, J., Jonsdottir, G. A., Ruotti, V., Stewart, R., Slukvin, I. I., and Thomson, J. A. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920
8. Kelly, V. R., Xu, B., Kuick, R., Koenig, R. J., and Hammer, G. D. (2010) Dax1 up-regulates Oct4 expression in mouse embryonic stem cells via LRH-1 and SRA. Mol. Endocrinol. 24, 2281-2291
9. Kelly, V. R., and Hammer, G. D. (2011) LRH-1 and Nanog regulate Dax1 transcription in mouse embryonic stem cells. Mol. Cell Endocrinol. 332, 116-124
10. Wagner, R. T., Xu, X., Yi, F., Merrill, B. J., and Cooney, A. J. (2010) Canonical Wnt/β-catenin regulation of liver receptor homolog-1 mediates pluripotency gene expression. Stem Cells 28, 1794-1804
11. Paré, J. F., Malenfant, D., Courtemanche, C., Jacob-Wagner, M., Roy, S., Allard, D., and Bélanger, L. (2004) The fetoprotein transcription factor (FTF) gene is essential to embryogenesis and cholesterol homeostasis and is regulated by a DR4 element. J. Biol. Chem. 279, 21206-21216
12. Heng, J. C., Feng, B., Han, J., Jiang, J., Kraus, P., Ng, J. H., Orlov, Y. L., Huss, M., Yang, L., Lufkin, T., Lim, B., and Ng, H. H. (2010) The nuclear receptor Nr5a2 can replace Oct4 in the reprogramming of murine somatic cells to pluripotent cells. Cell Stem Cell 6, 167-174
13. Fayard, E., Auwerx, J., and Schoonjans, K. (2004) LRH-1: an orphan nuclear receptor involved in development, metabolism and steroidogenesis. Trends Cell Biol. 14, 250-260 (Pubitemid 38591329)
14. Bookout, A. L., Jeong, Y., Downes, M., Yu, R. T., Evans, R. M., and Mangelsdorf, D. J. (2006) Anatomical profiling of nuclear receptor expression reveals a hierarchical transcriptional network. Cell 126, 789-799 (Pubitemid 44233630)
15. Goodwin, B., Jones, S. A., Price, R. R., Watson, M. A., McKee, D. D., Moore, L. B., Galardi, C., Wilson, J. G., Lewis, M. C., Roth, M. E., Maloney, P. R., Willson, T. M., and Kliewer, S. A. (2000) A regulatory cascade of the nuclear receptors FXR, SHP-1, and LRH-1 represses bile acid biosynthesis. Mol. Cell 6, 517-526
16. Clyne, C. D., Speed, C. J., Zhou, J., and Simpson, E. R. (2002) Liver receptor homologue-1 (LRH-1) regulates expression of aromatase in preadipocytes. J. Biol. Chem. 277, 20591-20597 (Pubitemid 34967360)
17. Sablin, E. P., Krylova, I. N., Fletterick, R. J., and Ingraham, H. A. (2003) Structural basis for ligand-independent activation of the orphan nuclear receptor LRH-1. Mol. cell 11, 1575-1585 (Pubitemid 36776543)
18. Musille, P. M., Pathak, M. C., Lauer, J. L., Hudson, W. H., Griffin, P. R., and Ortlund, E. A. (2012) Antidiabetic phospholipid-nuclear receptor complex reveals the mechanism for phospholipid-driven gene regulation. Nat. Struct. Mol. Biol. 19, 532-537
19. Xu, P. L., Kong, Y. Y., Xie, Y. H., and Wang, Y. (2003) Corepressor SMRT specifically represses the transcriptional activity of orphan nuclear receptor hB1F/hLRH-1. Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao (Shanghai) 35, 897-903
20. Clyne, C. D., Kovacic, A., Speed, C. J., Zhou, J., Pezzi, V., and Simpson, E. R. (2004) Regulation of aromatase expression by the nuclear receptor LRH-1 in adipose tissue. Mol. Cell Endocrinol. 215, 39-44 (Pubitemid 38333241)
21. Lee, J. M., Lee, Y. K., Mamrosh, J. L., Busby, S. A., Griffin, P. R., Pathak, M. C., Ortlund, E. A., and Moore, D. D. (2011) A nuclear-receptor- dependent phosphatidylcholine pathway with antidiabetic effects. Nature 474, 506-510
22. Krylova, I. N., Sablin, E. P., Moore, J., Xu, R. X., Waitt, G. M., MacKay, J. A., Juzumiene, D., Bynum, J. M., Madauss, K., Montana, V., Lebedeva, L., Suzawa, M., Williams, J. D., Williams, S. P., Guy, R. K., Thornton, J. W., Fletterick, R. J., Willson, T. M., and Ingraham, H. A. (2005) Structural analyses reveal phosphatidyl inositols as ligands for the NR5 orphan receptors SF-1 and LRH-1. Cell 120, 343-355 (Pubitemid 40222429)
23. Ortlund, E. A., Lee, Y., Solomon, I. H., Hager, J. M., Safi, R., Choi, Y., Guan, Z., Tripathy, A., Raetz, C. R. H., McDonnell, D. P., Moore, D. D., and Redinbo, M. R. (2005) Modulation of human nuclear receptor LRH-1 activity by phospholipids and SHP. Nat. Struct. Mol. Biol. 12, 357-363 (Pubitemid 43093091)
24. Li, Y., Choi, M., Cavey, G., Daugherty, J., Suino, K., Kovach, A., Bingham, N. C., Kliewer, S. A., and Xu, H. E. (2005) Crystallographic identification and functional characterization of phospholipids as ligands for the orphan nuclear receptor steroidogenic factor-1. Mol. Cell 17, 491-502 (Pubitemid 40269114)
25. Sablin, E. P., Blind, R. D., Krylova, I. N., Ingraham, J. G., Cai, F., Williams, J. D., Fletterick, R. J., and Ingraham, H. A. (2009) Structure of SF-1 bound by different phospholipids: evidence for regulatory ligands. Mol. Endocrinol. 23, 25-34
26. Urs, A. N., Dammer, E., Kelly, S., Wang, E., Merrill, A. H., Jr., and Sewer, M. B. (2007) Steroidogenic factor-1 is a sphingolipid binding protein. Mol. Cell. Endocrinol. 265-266, 174-178 (Pubitemid 46273962)
27. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
28. Potterton, E., Briggs, P., Turkenburg, M., and Dodson, E. (2003) A graphical user interface to the CCP4 program suite. Acta Crystallogr. D Biol. Crystallogr. 59, 1131-1137 (Pubitemid 36872348)
29. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
30. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
31. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr D Biol. Crystallogr. 66, 486-501
32. Laskowski, R. A., McArthur, M.W., Moss, D.S. & Thornton, J. M. (1993) Procheck: a program to check the stereochemical quality of protein structure. J. Appl. Crystallogr. 26, 283-291
33. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21
34. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917
35. Chalmers, M. J., Busby, S. A., Pascal, B. D., He, Y., Hendrickson, C. L., Marshall, A. G., and Griffin, P. R. (2006) Probing protein ligand interactions by automated hydrogen/deuterium exchange mass spectrometry. Anal. Chem. 78, 1005-1014 (Pubitemid 43271829)
36. Whitby, R. J., Stec, J., Blind, R. D., Dixon, S., Leesnitzer, L. M., Orband-Miller, L. A., Williams, S. P., Willson, T. M., Xu, R., Zuercher, W. J., Cai, F., and Ingraham, H. A. (2011) Small molecule agonists of the orphan nuclear receptors steroidogenic factor-1 (SF-1, NR5A1) and liver receptor homologue-1 (LRH-1, NR5A2). J. Med. Chem. 54, 2266-2281
37. Ortlund, E. A., Bridgham, J. T., Redinbo, M. R., and Thornton, J. W. (2007) Crystal structure of an ancient protein: Evolution by conformational epistasis. Science 317, 1544-1548 (Pubitemid 47417432)
38. Schoch, G. A., D'Arcy, B., Stihle, M., Burger, D., Bär, D., Benz, J., Thoma, R., and Ruf, A. (2010) Molecular switch in the glucocorticoid receptor: active and passive antagonist conformations. J. Mol. Biol. 395, 568-577
39. Raaijmakers, H. C., Versteegh, J. E., and Uitdehaag, J. C. (2009) The x-ray structure of RU486 bound to the progesterone receptor in a destabilized agonistic conformation. J. Biol. Chem. 284, 19572-19579
40. Bledsoe, R. K., Madauss, K. P., Holt, J. A., Apolito, C. J., Lambert, M. H., Pearce, K. H., Stanley, T. B., Stewart, E. L., Trump, R. P., Willson, T. M., and Williams, S. P. (2005) A ligand-mediated hydrogen bond network required for the activation of the mineralocorticoid receptor. J. Biol. Chem. 280, 31283-31293 (Pubitemid 41291866)
41. Yoo, J., Ko, S., Kim, H., Sampson, H., Yun, J. H., Choe, K. M., Chang, I., Arrowsmith, C. H., Krause, H. M., Cho, H. S., and Lee, W. (2011) Crystal structure of Fushi tarazu factor 1 ligand binding domain/Fushi tarazu peptide complex identifies new class of nuclear receptors. J. Biol. Chem. 286, 31225-31231
42. Bridgham, J. T., Eick, G. N., Larroux, C., Deshpande, K., Harms, M. J., Gauthier, M. E., Ortlund, E. A., Degnan, B. M., and Thornton, J. W. (2010) Protein evolution by molecular tinkering: diversification of the nuclear receptor superfamily from a ligand-dependent ancestor. PLoS Biol. 8, e1000497
43. Watkins, R. E., Wisely, G. B., Moore, L. B., Collins, J. L., Lambert, M. H., Williams, S. P., Willson, T. M., Kliewer, S. A., and Redinbo, M. R. (2001) The human nuclear xenobiotic receptor PXR: structural determinants of directed promiscuity. Science 292, 2329-2333 (Pubitemid 32568055)
44. Nolte, R. T., Wisely, G. B., Westin, S., Cobb, J. E., Lambert, M. H., Kurokawa, R., Rosenfeld, M. G., Willson, T. M., Glass, C. K., and Milburn, M. V. (1998) Ligand binding and co-activator assembly of the peroxisome proliferator-activated receptor-γ. Nature 395, 137-143 (Pubitemid 28425645)
45. Mullaney, B. C., Blind, R. D., Lemieux, G. A., Perez, C. L., Elle, I. C., Faergeman, N. J., Van Gilst, M. R., Ingraham, H. A., and Ashrafi, K. (2010) Regulation of C. elegans fat uptake and storage by acyl-CoA synthase-3 is dependent on NR5A family nuclear hormone receptor nhr-25. Cell Metab. 12, 398-410
46. Wang, D. Y., Kumar, S., and Hedges, S. B. (1999) Divergence time estimates for the early history of animal phyla and the origin of plants, animals and fungi. Proc. Biol. Sci. 266, 163-171 (Pubitemid 29048011)