A structural signature motif enlightens the origin and diversification of nuclear receptors
Autoři:
Brice Beinsteiner aff001; Gabriel V. Markov aff005; Stéphane Erb aff006; Yassmine Chebaro aff001; Alastair G. McEwen aff001; Sarah Cianférani aff006; Vincent Laudet aff007; Dino Moras aff001; Isabelle M. L. Billas aff001
Působiště autorů:
IGBMC (Institute of Genetics and of Molecular and Cellular Biology), Illkirch, France
aff001; Université de Strasbourg, Unistra, Strasbourg, France
aff002; Institut National de la Santé et de la Recherche Médicale (INSERM) U1258, Illkirch, France
aff003; Centre National de la Recherche Scientifique (CNRS) UMR 7104, Illkirch, France
aff004; Sorbonne Université, CNRS, UMR 8227, Integrative Biology of Marine Models, (LBI2M, UMR8227), Station Biologique de Roscoff (SBR), Roscoff, France
aff005; Laboratoire de Spectrométrie de Masse BioOrganique, Université de Strasbourg, CNRS, IPHC UMR 7178, Strasbourg, France
aff006; Marine Eco-Evo-Devo Unit. Okinawa Institute of Science and Technology, Onna-son, Okinawa, Japan
aff007
Vyšlo v časopise:
A structural signature motif enlightens the origin and diversification of nuclear receptors. PLoS Genet 17(4): e1009492. doi:10.1371/journal.pgen.1009492
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009492
Souhrn
Nuclear receptors are ligand-activated transcription factors that modulate gene regulatory networks from embryonic development to adult physiology and thus represent major targets for clinical interventions in many diseases. Most nuclear receptors function either as homodimers or as heterodimers. The dimerization is crucial for gene regulation by nuclear receptors, by extending the repertoire of binding sites in the promoters or the enhancers of target genes via combinatorial interactions. Here, we focused our attention on an unusual structural variation of the α-helix, called π-turn that is present in helix H7 of the ligand-binding domain of RXR and HNF4. By tracing back the complex evolutionary history of the π-turn, we demonstrate that it was present ancestrally and then independently lost in several nuclear receptor lineages. Importantly, the evolutionary history of the π-turn motif is parallel to the evolutionary diversification of the nuclear receptor dimerization ability from ancestral homodimers to derived heterodimers. We then carried out structural and biophysical analyses, in particular through point mutation studies of key RXR signature residues and showed that this motif plays a critical role in the network of interactions stabilizing homodimers. We further showed that the π-turn was instrumental in allowing a flexible heterodimeric interface of RXR in order to accommodate multiple interfaces with numerous partners and critical for the emergence of high affinity receptors. Altogether, our work allows to identify a functional role for the π-turn in oligomerization of nuclear receptors and reveals how this motif is linked to the emergence of a critical biological function. We conclude that the π-turn can be viewed as a structural exaptation that has contributed to enlarging the functional repertoire of nuclear receptors.
Klíčová slova:
Crystal structure – Dimerization – Dimers – Electron density – Evolutionary adaptation – Monomers – Phylogenetic analysis – Sequence motif analysis
Zdroje
1. Billas I, Moras D. Allosteric Controls of Nuclear Receptor Function in the Regulation of Transcription. J Mol Biol. 2013;425: 2317–2329. doi: 10.1016/j.jmb.2013.03.017 23499886
2. Gronemeyer H, Gustafsson J-A, Laudet V. Principles for modulation of the nuclear receptor superfamily. Nat Rev Drug Discov. 2004;3: 950–964. doi: 10.1038/nrd1551 15520817
3. Lazar MA. Maturing of the nuclear receptor family. J Clin Invest. 2017;127: 1123–1125. doi: 10.1172/JCI92949 28368290
4. Amero SA, Kretsinger RH, Moncrief ND, Yamamoto KR, Pearson WR. The origin of nuclear receptor proteins: a single precursor distinct from other transcription factors. Mol Endocrinol Baltim Md. 1992;6: 3–7. doi: 10.1210/mend.6.1.1738368 1738368
5. Escriva H, Safi R, Hänni C, Langlois M-C, Saumitou-Laprade P, Stehelin D, et al. Ligand binding was acquired during evolution of nuclear receptors. Proc Natl Acad Sci. 1997;94: 6803–6808. doi: 10.1073/pnas.94.13.6803 9192646
6. Laudet V, Hänni C, Coll J, Catzeflis F, Stéhelin D. Evolution of the nuclear receptor gene superfamily. EMBO J. 1992;11: 1003–1013. 1312460
7. López-Escardó D, Grau-Bové X, Guillaumet-Adkins A, Gut M, Sieracki ME, Ruiz-Trillo I. Reconstruction of protein domain evolution using single-cell amplified genomes of uncultured choanoflagellates sheds light on the origin of animals. Philos Trans R Soc Lond B Biol Sci. 2019;374: 20190088. doi: 10.1098/rstb.2019.0088 31587642
8. Bertrand S, Brunet FG, Escriva H, Parmentier G, Laudet V, Robinson-Rechavi M. Evolutionary Genomics of Nuclear Receptors: From Twenty-Five Ancestral Genes to Derived Endocrine Systems. Mol Biol Evol. 2004;21: 1923–1937. doi: 10.1093/molbev/msh200 15229292
9. Bridgham JT, Eick GN, Larroux C, Deshpande K, Harms MJ, Gauthier MEA, et al. Protein Evolution by Molecular Tinkering: Diversification of the Nuclear Receptor Superfamily from a Ligand-Dependent Ancestor. PLoS Biol. 2010;8: e1000497. doi: 10.1371/journal.pbio.1000497 20957188
10. Robinson-Rechavi M, Maina CV, Gissendanner CR, Laudet V, Sluder A. Explosive Lineage-Specific Expansion of the Orphan Nuclear Receptor HNF4 in Nematodes. J Mol Evol. 2005;60: 577–586. doi: 10.1007/s00239-004-0175-8 15983867
11. Simion P, Philippe H, Baurain D, Jager M, Richter DJ, Di Franco A, et al. A Large and Consistent Phylogenomic Dataset Supports Sponges as the Sister Group to All Other Animals. Curr Biol CB. 2017;27: 958–967. doi: 10.1016/j.cub.2017.02.031 28318975
12. Eick GN, Thornton JW. Evolution of steroid receptors from an estrogen-sensitive ancestral receptor. Mol Cell Endocrinol. 2011;334: 31–38. doi: 10.1016/j.mce.2010.09.003 20837101
13. Markov GV, Laudet V. Origin and evolution of the ligand-binding ability of nuclear receptors. Mol Cell Endocrinol. 2011;334: 21–30. doi: 10.1016/j.mce.2010.10.017 21055443
14. Germain P, Bourguet W. Dimerization of nuclear receptors. Methods Cell Biol. 2013;117: 21–41. doi: 10.1016/B978-0-12-408143-7.00002-5 24143970
15. Brélivet Y, Rochel N, Moras D. Structural analysis of nuclear receptors: From isolated domains to integral proteins. Mol Cell Endocrinol. 2012;348: 466–473. doi: 10.1016/j.mce.2011.08.015 21888944
16. Khorasanizadeh S, Rastinejad F. Nuclear-receptor interactions on DNA-response elements. Trends Biochem Sci. 2001;26: 384–390. doi: 10.1016/s0968-0004(01)01800-x 11406412
17. Brelivet Y, Kammerer S, Rochel N, Poch O, Moras D. Signature of the oligomeric behaviour of nuclear receptors at the sequence and structural level. EMBO Rep. 2004;5: 423–429. doi: 10.1038/sj.embor.7400119 15105832
18. Bourguet W, Ruff M, Chambon P, Gronemeyer H, Moras D. Crystal structure of the ligand-binding domain of the human nuclear receptor RXR-α. Nature. 1995;375: 377–382. doi: 10.1038/375377a0 7760929
19. Eberhardt J, McEwen AG, Bourguet W, Moras D, Dejaegere A. A revisited version of the apo structure of the ligand-binding domain of the human nuclear receptor retinoic X receptor α. Acta Crystallogr Sect F Struct Biol Commun. 2019;75: 98–104. doi: 10.1107/S2053230X18018022 30713160
20. Billas IM, Moulinier L, Rochel N, Moras D. Crystal structure of the ligand-binding domain of the ultraspiracle protein USP, the ortholog of retinoid X receptors in insects. J Biol Chem. 2001;276: 7465–7474. doi: 10.1074/jbc.M008926200 11053444
21. Wisely GB, Miller AB, Davis RG, Thornquest AD, Johnson R, Spitzer T, et al. Hepatocyte nuclear factor 4 is a transcription factor that constitutively binds fatty acids. Struct Lond Engl 1993. 2002;10: 1225–1234. doi: 10.1016/s0969-2126(02)00829-8 12220494
22. Cartailler J-P, Luecke H. Structural and Functional Characterization of π Bulges and Other Short Intrahelical Deformations. Structure. 2004;12: 133–144. doi: 10.1016/j.str.2003.12.001 14725773
23. Cooley RB, Arp DJ, Karplus PA. Evolutionary Origin of a Secondary Structure: π-Helices as Cryptic but Widespread Insertional Variations of α-Helices That Enhance Protein Functionality. J Mol Biol. 2010;404: 232–246. doi: 10.1016/j.jmb.2010.09.034 20888342
24. Kumar P, Bansal M. Dissecting π-helices: sequence, structure and function. FEBS J. 2015;282: 4415–4432. doi: 10.1111/febs.13507 26370783
25. Ludwiczak J, Winski A, da Silva Neto AM, Szczepaniak K, Alva V, Dunin-Horkawicz S. PiPred–a deep-learning method for prediction of π-helices in protein sequences. Sci Rep. 2019;9: 6888. doi: 10.1038/s41598-019-43189-4 31053765
26. Riek RP, Graham RM. The elusive π-helix. J Struct Biol. 2011;173: 153–160. doi: 10.1016/j.jsb.2010.09.001 20828621
27. Watkins RE, Wisely GB, Moore LB, Collins JL, Lambert MH, Williams SP, et al. The human nuclear xenobiotic receptor PXR: structural determinants of directed promiscuity. Science. 2001;292: 2329–2333. doi: 10.1126/science.1060762 11408620
28. Blind RD, Sablin EP, Kuchenbecker KM, Chiu H-J, Deacon AM, Das D, et al. The signaling phospholipid PIP3 creates a new interaction surface on the nuclear receptor SF-1. Proc Natl Acad Sci U S A. 2014;111: 15054–15059. doi: 10.1073/pnas.1416740111 25288771
29. Kruse SW, Suino-Powell K, Zhou XE, Kretschman JE, Reynolds R, Vonrhein C, et al. Identification of COUP-TFII Orphan Nuclear Receptor as a Retinoic Acid–Activated Receptor. PLoS Biol. 2008;6: e227. doi: 10.1371/journal.pbio.0060227 18798693
30. Tan MHE, Zhou XE, Soon F-F, Li X, Li J, Yong E-L, et al. The Crystal Structure of the Orphan Nuclear Receptor NR2E3/PNR Ligand Binding Domain Reveals a Dimeric Auto-Repressed Conformation. PLoS ONE. 2013;8. doi: 10.1371/journal.pone.0074359 24069298
31. Gronemeyer H, Laudet V. Transcription factors 3: nuclear receptors. Protein Profile. 1995;2: 1173–1308. 8681033
32. Adelmant G, Bègue A, Stéhelin D, Laudet V. A functional Rev-erb alpha responsive element located in the human Rev-erb alpha promoter mediates a repressing activity. Proc Natl Acad Sci U S A. 1996;93: 3553–3558. doi: 10.1073/pnas.93.8.3553 8622974
33. Alexander SPH, Cidlowski JA, Kelly E, Mathie A, Peters JA, Veale EL, et al. THE CONCISE GUIDE TO PHARMACOLOGY 2019/20: Nuclear hormone receptors. Br J Pharmacol. 2019;176: S229–S246. doi: 10.1111/bph.14750 31710718
34. Lanz RB, Jericevic Z, Zuercher WJ, Watkins C, Steffen DL, Margolis R, et al. Nuclear Receptor Signaling Atlas (www.nursa.org): hyperlinking the nuclear receptor signaling community. Nucleic Acids Res. 2006;34: D221–226. doi: 10.1093/nar/gkj029 16381851
35. Laudet V. Evolution of the nuclear receptor superfamily: early diversification from an ancestral orphan receptor. J Mol Endocrinol. 1997;19: 207–226. doi: 10.1677/jme.0.0190207 9460643
36. Ochsner SA, Abraham D, Martin K, Ding W, McOwiti A, Kankanamge W, et al. The Signaling Pathways Project, an integrated ‘omics knowledgebase for mammalian cellular signaling pathways. Sci Data. 2019;6: 252. doi: 10.1038/s41597-019-0193-4 31672983
37. Kojetin DJ, Matta-Camacho E, Hughes TS, Srinivasan S, Nwachukwu JC, Cavett V, et al. Structural mechanism for signal transduction in RXR nuclear receptor heterodimers. Nat Commun. 2015;6: 8013. doi: 10.1038/ncomms9013 26289479
38. Eeckhoute J, Oxombre B, Formstecher P, Lefebvre P, Laine B. Critical role of charged residues in helix 7 of the ligand binding domain in Hepatocyte Nuclear Factor 4alpha dimerisation and transcriptional activity. Nucleic Acids Res. 2003;31: 6640–6650. doi: 10.1093/nar/gkg850 14602925
39. Cooper DN, Ball EV, Krawczak M. The human gene mutation database. Nucleic Acids Res. 1998;26: 285–287. doi: 10.1093/nar/26.1.285 9399854
40. Ehkirch A, Hernandez-Alba O, Colas O, Beck A, Guillarme D, Cianférani S. Hyphenation of size exclusion chromatography to native ion mobility mass spectrometry for the analytical characterization of therapeutic antibodies and related products. J Chromatogr B Analyt Technol Biomed Life Sci. 2018;1086: 176–183. doi: 10.1016/j.jchromb.2018.04.010 29684909
41. Kersten S, Reczek PR, Noy N. The tetramerization region of the retinoid X receptor is important for transcriptional activation by the receptor. J Biol Chem. 1997;272: 29759–29768. doi: 10.1074/jbc.272.47.29759 9368046
42. Kersten S, Kelleher D, Chambon P, Gronemeyer H, Noy N. Retinoid X receptor alpha forms tetramers in solution. Proc Natl Acad Sci U S A. 1995;92: 8645–8649. doi: 10.1073/pnas.92.19.8645 7567990
43. Borel F, de Groot A, Juillan-Binard C, de Rosny E, Laudet V, Pebay-Peyroula E, et al. Crystal structure of the ligand-binding domain of the retinoid X receptor from the ascidian Polyandrocarpa misakiensis. Proteins. 2009;74: 538–542. doi: 10.1002/prot.22294 19004016
44. Gampe RT, Montana VG, Lambert MH, Wisely GB, Milburn MV, Xu HE. Structural basis for autorepression of retinoid X receptor by tetramer formation and the AF-2 helix. Genes Dev. 2000;14: 2229–2241. doi: 10.1101/gad.802300 10970886
45. Wurtz JM, Bourguet W, Renaud JP, Vivat V, Chambon P, Moras D, et al. A canonical structure for the ligand-binding domain of nuclear receptors. Nat Struct Biol. 1996;3: 87–94. doi: 10.1038/nsb0196-87 8548460
46. Egea PF, Mitschler A, Moras D. Molecular Recognition of Agonist Ligands by RXRs. Mol Endocrinol. 2002;16: 987–997. doi: 10.1210/mend.16.5.0823 11981034
47. Bourguet W, Germain P, Gronemeyer H. Nuclear receptor ligand-binding domains: three-dimensional structures, molecular interactions and pharmacological implications. Trends Pharmacol Sci. 2000;21: 381–388. doi: 10.1016/s0165-6147(00)01548-0 11050318
48. Bourguet W, Vivat V, Wurtz J-M, Chambon P, Gronemeyer H, Moras D. Crystal Structure of a Heterodimeric Complex of RAR and RXR Ligand-Binding Domains. Mol Cell. 2000;5: 289–298. doi: 10.1016/s1097-2765(00)80424-4 10882070
49. Iwema T, Billas IM, Beck Y, Bonneton F, Nierengarten H, Chaumot A, et al. Structural and functional characterization of a novel type of ligand-independent RXR-USP receptor. EMBO J. 2007;26: 3770–3782. doi: 10.1038/sj.emboj.7601810 17673910
50. Maletta M, Orlov I, Roblin P, Beck Y, Moras D, Billas IML, et al. The palindromic DNA-bound USP/EcR nuclear receptor adopts an asymmetric organization with allosteric domain positioning. Nat Commun. 2014;5. doi: 10.1038/ncomms5139 24942373
51. Ren B, Peat TS, Streltsov VA, Pollard M, Fernley R, Grusovin J, et al. Unprecedented conformational flexibility revealed in the ligand-binding domains of the Bovicola ovis ecdysone receptor (EcR) and ultraspiracle (USP) subunits. Acta Crystallogr D Biol Crystallogr. 2014;70: 1954–1964. doi: 10.1107/S1399004714009626 25004972
52. Iwema T, Chaumot A, Studer RA, Robinson-Rechavi M, Billas IML, Moras D, et al. Structural and evolutionary innovation of the heterodimerization interface between USP and the ecdysone receptor ECR in insects. Mol Biol Evol. 2009;26: 753–768. doi: 10.1093/molbev/msn302 19126866
53. Bonneton F, Chaumot A, Laudet V. Annotation of Tribolium nuclear receptors reveals an increase in evolutionary rate of a network controlling the ecdysone cascade. Insect Biochem Mol Biol. 2008;38: 416–429. doi: 10.1016/j.ibmb.2007.10.006 18342247
54. Chaumot A, Da Lage J-L, Maestro O, Martin D, Iwema T, Brunet F, et al. Molecular adaptation and resilience of the insect’s nuclear receptor USP. BMC Evol Biol. 2012;12: 199. doi: 10.1186/1471-2148-12-199 23039844
55. Williams SP, Sigler PB. Atomic structure of progesterone complexed with its receptor. Nature. 1998;393: 392–396. doi: 10.1038/30775 9620806
56. Krężel W, Rühl R, de Lera AR. Alternative retinoid X receptor (RXR) ligands. Mol Cell Endocrinol. 2019;491: 110436. doi: 10.1016/j.mce.2019.04.016 31026478
57. Yuan X, Ta TC, Lin M, Evans JR, Dong Y, Bolotin E, et al. Identification of an endogenous ligand bound to a native orphan nuclear receptor. PloS One. 2009;4: e5609. doi: 10.1371/journal.pone.0005609 19440305
58. Grebner C, Lecina D, Gil V, Ulander J, Hansson P, Dellsen A, et al. Exploring Binding Mechanisms in Nuclear Hormone Receptors by Monte Carlo and X-ray-derived Motions. Biophys J. 2017;112: 1147–1156. doi: 10.1016/j.bpj.2017.02.004 28355542
59. Billas IML, Iwema T, Garnier J-M, Mitschler A, Rochel N, Moras D. Structural adaptability in the ligand-binding pocket of the ecdysone hormone receptor. Nature. 2003;426: 91–96. doi: 10.1038/nature02112 14595375
60. Nettles KW, Bruning JB, Gil G, O’Neill EE, Nowak J, Hughs A, et al. Structural plasticity in the oestrogen receptor ligand-binding domain. EMBO Rep. 2007;8: 563–568. doi: 10.1038/sj.embor.7400963 17468738
61. Belorusova AY, Rochel N. Structural Studies of Vitamin D Nuclear Receptor Ligand-Binding Properties. Vitam Horm. 2016;100: 83–116. doi: 10.1016/bs.vh.2015.10.003 26827949
62. Ciesielski F, Rochel N, Moras D. Adaptability of the Vitamin D nuclear receptor to the synthetic ligand Gemini: remodelling the LBP with one side chain rotation. J Steroid Biochem Mol Biol. 2007;103: 235–242. doi: 10.1016/j.jsbmb.2006.12.003 17218092
63. Delfosse V, Grimaldi M, Pons J-L, Boulahtouf A, le Maire A, Cavailles V, et al. Structural and mechanistic insights into bisphenols action provide guidelines for risk assessment and discovery of bisphenol A substitutes. Proc Natl Acad Sci U S A. 2012;109: 14930–14935. doi: 10.1073/pnas.1203574109 22927406
64. Cuénot L. Théorie de la Préadaptation. Scientia. 1914;8: 60.
65. Gould SJ, Vrba ES. Exaptation—a Missing Term in the Science of Form. Paleobiology. 1982;8: 4–15. doi: 10.1017/S0094837300004310
66. Gavelis GS, Keeling PJ, Leander BS. How exaptations facilitated photosensory evolution: Seeing the light by accident. BioEssays News Rev Mol Cell Dev Biol. 2017;39. doi: 10.1002/bies.201600266 28570771
67. Cornelis G, Vernochet C, Carradec Q, Souquere S, Mulot B, Catzeflis F, et al. Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials. Proc Natl Acad Sci U S A. 2015;112: E487–496. doi: 10.1073/pnas.1417000112 25605903
68. Maex M, Treer D, De Greve H, Proost P, Van Bocxlaer I, Bossuyt F. Exaptation as a Mechanism for Functional Reinforcement of an Animal Pheromone System. Curr Biol CB. 2018;28: 2955–2960.e5. doi: 10.1016/j.cub.2018.06.074 30197090
69. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics. 1999;151: 1531–1545. 10101175
70. Plach MG, Reisinger B, Sterner R, Merkl R. Long-Term Persistence of Bi-functionality Contributes to the Robustness of Microbial Life through Exaptation. PLoS Genet. 2016;12: e1005836. doi: 10.1371/journal.pgen.1005836 26824644
71. Yanai I, Yu Y, Zhu X, Cantor CR, Weng Z. An avidin-like domain that does not bind biotin is adopted for oligomerization by the extracellular mosaic protein fibropellin. Protein Sci Publ Protein Soc. 2005;14: 417–423. doi: 10.1110/ps.04898705 15659374
72. Lebowitz J, Lewis MS, Schuck P. Modern analytical ultracentrifugation in protein science: a tutorial review. Protein Sci Publ Protein Soc. 2002;11: 2067–2079. doi: 10.1110/ps.0207702 12192063
73. Schuck P. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J. 2000;78: 1606–1619. doi: 10.1016/S0006-3495(00)76713-0 10692345
74. Marty MT, Baldwin AJ, Marklund EG, Hochberg GKA, Benesch JLP, Robinson CV. Bayesian Deconvolution of Mass and Ion Mobility Spectra: From Binary Interactions to Polydisperse Ensembles. Anal Chem. 2015;87: 4370–4376. doi: 10.1021/acs.analchem.5b00140 25799115
75. Brünger AT, Karplus M. Polar hydrogen positions in proteins: empirical energy placement and neutron diffraction comparison. Proteins. 1988;4: 148–156. doi: 10.1002/prot.340040208 3227015
76. Brooks BR, Brooks CL, Mackerell AD, Nilsson L, Petrella RJ, Roux B, et al. CHARMM: the biomolecular simulation program. J Comput Chem. 2009;30: 1545–1614. doi: 10.1002/jcc.21287 19444816
77. Best RB, Zhu X, Shim J, Lopes PEM, Mittal J, Feig M, et al. Optimization of the additive CHARMM all-atom protein force field targeting improved sampling of the backbone φ, ψ and side-chain χ(1) and χ(2) dihedral angles. J Chem Theory Comput. 2012;8: 3257–3273. doi: 10.1021/ct300400x 23341755
78. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, et al. Scalable molecular dynamics with NAMD. J Comput Chem. 2005;26: 1781–1802. doi: 10.1002/jcc.20289 16222654
79. Darden T, York D, Pedersen L. Particle mesh Ewald: An N·log(N) method for Ewald sums in large systems. J Chem Phys. 1993;98: 10089–10092. doi: 10.1063/1.464397
80. Ryckaert J, Ciccotti G, Berendsen HJC. Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys. 1977; 327–341.
81. Bianchetti L, Wassmer B, Defosset A, Smertina A, Tiberti ML, Stote RH, et al. Alternative dimerization interfaces in the glucocorticoid receptor-α ligand binding domain. Biochim Biophys Acta Gen Subj. 2018;1862: 1810–1825. doi: 10.1016/j.bbagen.2018.04.022 29723544
82. Chebaro Y, Sirigu S, Amal I, Lutzing R, Stote RH, Rochette-Egly C, et al. Allosteric Regulation in the Ligand Binding Domain of Retinoic Acid Receptorγ. PLOS ONE. 2017;12: e0171043. doi: 10.1371/journal.pone.0171043 28125680
83. Chebaro Y, Amal I, Rochel N, Rochette-Egly C, Stote RH, Dejaegere A. Phosphorylation of the Retinoic Acid Receptor Alpha Induces a Mechanical Allosteric Regulation and Changes in Internal Dynamics. PLOS Comput Biol. 2013;9: e1003012. doi: 10.1371/journal.pcbi.1003012 23637584
84. Moroy G, Martin E, Dejaegere A, Stote RH. Molecular basis for Bcl-2 homology 3 domain recognition in the Bcl-2 protein family: identification of conserved hot spot interactions. J Biol Chem. 2009;284: 17499–17511. doi: 10.1074/jbc.M805542200 19293158
85. Zanier K, Charbonnier S, Sidi AOMO, McEwen AG, Ferrario MG, Poussin-Courmontagne P, et al. Structural basis for hijacking of cellular LxxLL motifs by papillomavirus E6 oncoproteins. Science. 2013;339: 694–698. doi: 10.1126/science.1229934 23393263
86. Madura JD, Briggs JM, Wade RC, Davis ME, Luty BA, Ilin A, et al. Electrostatics and diffusion of molecules in solution: simulations with the University of Houston Brownian Dynamics program. Comput Phys Commun. 1995;91: 57–95. doi: 10.1016/0010-4655(95)00043-F
87. Lafont V, Schaefer M, Stote RH, Altschuh D, Dejaegere A. Protein-protein recognition and interaction hot spots in an antigen-antibody complex: free energy decomposition identifies “efficient amino acids.” Proteins. 2007;67: 418–434. doi: 10.1002/prot.21259 17256770
88. Khalturin K, Billas IML, Chebaro Y, Reitzel AM, Tarrant AM, Laudet V, et al. NR3E receptors in cnidarians: A new family of steroid receptor relatives extends the possible mechanisms for ligand binding. J Steroid Biochem Mol Biol. 2018;184: 11–19. doi: 10.1016/j.jsbmb.2018.06.014 29940311
Článek vyšel v časopise
PLOS Genetics
2021 Číslo 4
- Distribuce a lokalizace speciálně upravených exosomů může zefektivnit léčbu svalových dystrofií
- Prof. Jan Škrha: Metformin je bezpečný, ale je třeba jej bezpečně užívat a léčbu kontrolovat
- FDA varuje před selfmonitoringem cukru pomocí chytrých hodinek. Jak je to v Česku?
- Masturbační chování žen v ČR − dotazníková studie
- O krok blíže k pochopení efektu placeba při léčbě bolesti
Nejčtenější v tomto čísle
- Aicardi-Goutières syndrome-associated gene SAMHD1 preserves genome integrity by preventing R-loop formation at transcription–replication conflict regions
- Functional assessment of the “two-hit” model for neurodevelopmental defects in Drosophila and X. laevis
- Pathways and signatures of mutagenesis at targeted DNA nicks
- Using genetic variants to evaluate the causal effect of cholesterol lowering on head and neck cancer risk: A Mendelian randomization study