Reversing allosteric communication: From detecting allosteric sites to inducing and tuning targeted allosteric response

PLoS Computational Biology

Volumn 14, Issue 6, 2018, Pages

  Tee, Wei Ven ^a,b   Guarnera, Enrico ^a   Berezovsky, Igor N ^a,b  

^a BIOINFORMATICS INSTITUTE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMICS; SITE SELECTION; STRUCTURAL DYNAMICS; TUNING;

ALLOSTERIC COMMUNICATION; ALLOSTERIC REGULATION; ALLOSTERIC SITE; ALLOSTERY; EXOSITES; FUNCTIONAL SITES; PERTURBATION MODEL; PROTEIN DYNAMICS; PROTEIN SEQUENCES; STRUCTURE-BASED;

PROTEINS;

3 DEOXY 7 PHOSPHOHEPTULONATE SYNTHASE; 6 PHOSPHOFRUCTOKINASE; ANTHRANILATE SYNTHASE; ASPARTATE CARBAMOYLTRANSFERASE; CYCLIC AMP BINDING PROTEIN; FRUCTOSE 1,6 BISPHOSPHATE; FUMARIC ACID; GLUTAMATE DEHYDROGENASE; MALATE DEHYDROGENASE (DECARBOXYLATING); PHOSPHOGLYCERATE DEHYDROGENASE; SYNTHETASE; THREONINE SYNTHASE; UNCLASSIFIED DRUG; URACIL PHOSPHORIBOSYLTRANSFERASE; LIGAND; PROTEIN; PROTEIN BINDING;

ALLOSTERISM; ARTICLE; BINDING AFFINITY; BINDING SITE; CATALYSIS; LIGAND BINDING; NONHUMAN; OLIGOMERIZATION; PREDICTION; SIGNAL TRANSDUCTION; ALLOSTERIC SITE; CHEMISTRY; MOLECULAR MODEL; PHYSIOLOGY; PROTEIN CONFORMATION; STRUCTURE ACTIVITY RELATION;

ALLOSTERIC REGULATION; ALLOSTERIC SITE; BINDING SITES; LIGANDS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEINS; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 85049369467     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1006228     Document Type: Article

References (56)

1. Wenthur C. J., Gentry P. R., Mathews T. P., Lindsley C. W., Drugs for Allosteric Sites on Receptors. Annu. Rev. Pharmacol. Toxicol. 54, 165–184 (2014). doi: 10.1146/annurev-pharmtox-010611-134525 pmid: 24111540
2. Nussinov R., Tsai C.-J., Allostery in Disease and in Drug Discovery. Cell153, 293–305 (2013). doi: 10.1016/j.cell.2013.03.034 pmid: 23582321
3. Lu S., Li S., Zhang J., Harnessing allostery: a novel approach to drug discovery. Med. Res. Rev. 34, 1242–1285 (2014). doi: 10.1002/med.21317 pmid: 24827416
4. Lu S., Huang W., Zhang J., Recent computational advances in the identification of allosteric sites in proteins. Drug Discov. Today19, 1595–1600 (2014). doi: 10.1016/j.drudis.2014.07.012 pmid: 25107670
5. Guarnera E., Berezovsky I. N., Allosteric sites: remote control in regulation of protein activity. Curr. Opin. Struct. Biol. 37, 1–8 (2016). doi: 10.1016/j.sbi.2015.10.004 pmid: 26562539
6. Berezovsky I. N., Thermodynamics of allostery paves a way to allosteric drugs. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics1834, 830–835 (2013).
7. Gunasekaran K., Ma B., Nussinov R., Is allostery an intrinsic property of all dynamic proteins?Proteins57, 433–443 (2004). doi: 10.1002/prot.20232 pmid: 15382234
8. Fang Z., Grütter C., Rauh D., Strategies for the selective regulation of kinases with allosteric modulators: exploiting exclusive structural features. ACS Chem. Biol. 8, 58–70 (2013). doi: 10.1021/cb300663j pmid: 23249378
9. Knight J. D. R., Qian B., Baker D., Kothary R., Conservation, variability and the modeling of active protein kinases. PLoS One2, e982 (2007). doi: 10.1371/journal.pone.0000982 pmid: 17912359
10. Wootten D., Christopoulos A., Sexton P. M., Emerging paradigms in GPCR allostery: implications for drug discovery. Nat. Rev. Drug Discov. 12, 630–644 (2013). doi: 10.1038/nrd4052 pmid: 23903222
11. May L., Avlani V., Sexton P., Christopoulos A., Allosteric Modulation of G Protein-Coupled Receptors. Curr. Pharm. Des. 10, 2003–2013 (2004). pmid: 15279541
12. Conn P. J., Christopoulos A., Lindsley C. W., Allosteric modulators of GPCRs: a novel approach for the treatment of CNS disorders. Nat. Rev. Drug Discov. 8, 41–54 (2009). doi: 10.1038/nrd2760 pmid: 19116626
13. Harrington P. E., Fotsch C., Calcium sensing receptor activators: calcimimetics. Curr. Med. Chem. 14, 3027–3034 (2007). pmid: 18220738
14. Dorr P., et al. Maraviroc (UK-427,857), a potent, orally bioavailable, and selective small-molecule inhibitor of chemokine receptor CCR5 with broad-spectrum anti-human immunodeficiency virus type 1 activity. Antimicrob. Agents Chemother. 49, 4721–4732 (2005). doi: 10.1128/AAC.49.11.4721-4732.2005 pmid: 16251317
15. Song K., et al. Improved Method for the Identification and Validation of Allosteric Sites. J. Chem. Inf. Model. 57, 2358–2363 (2017). doi: 10.1021/acs.jcim.7b00014 pmid: 28825477
16. Lu S., Ji M., Ni D., Zhang J., Discovery of hidden allosteric sites as novel targets for allosteric drug design. Drug Discov. Today (2017). doi: 10.1016/j.drudis.2017.10.001 pmid: 29030241
17. Bastolla U., Computing protein dynamics from protein structure with elastic network models. Wiley Interdiscip. Rev. Comput. Mol. Sci. 4, 488–503 (2014).
18. Macarron R., et al. Impact of high-throughput screening in biomedical research. Nat. Rev. Drug Discov. 10, 188–195 (2011). doi: 10.1038/nrd3368 pmid: 21358738
19. Surade S., et al. A structure-guided fragment-based approach for the discovery of allosteric inhibitors targeting the lipophilic binding site of transcription factor EthR. Biochem. J458, 387–394 (2014). doi: 10.1042/BJ20131127 pmid: 24313835
20. Bertekap R. L., Burford N. T, JrLi Z, Alt A, High-Throughput Screening for Allosteric Modulators of GPCRs. Methods Mol. Biol. 1335, 223–240 (2015). doi: 10.1007/978-1-4939-2914-6_15 pmid: 26260604
21. Sadowsky J. D., et al. Turning a protein kinase on or off from a single allosteric site via disulfide trapping. Proceedings of the National Academy of Sciences108, 6056–6061 (2011).
22. Boehlein S. K., Shaw J. R., Hannah L. C., Stewart J. D., Probing Allosteric Binding Sites of the Maize Endosperm ADP-Glucose Pyrophosphorylase. Plant Physiol. 152, 85–95 (2009). doi: 10.1104/pp.109.146928 pmid: 19889875
23. Badireddy S., et al. Cyclic AMP analog blocks kinase activation by stabilizing inactive conformation: conformational selection highlights a new concept in allosteric inhibitor design. Mol. Cell. Proteomics10, M110.004390 (2011).
24. Krishnamurthy S., Tulsian N. K., Chandramohan A., Anand G. S., Parallel Allostery by cAMP and PDE Coordinates Activation and Termination Phases in cAMP Signaling. Biophys. J. 109, 1251–1263 (2015). doi: 10.1016/j.bpj.2015.06.067 pmid: 26276689
25. Magnaghi P., et al. Covalent and allosteric inhibitors of the ATPase VCP/p97 induce cancer cell death. Nat. Chem. Biol. 9, 548–556 (2013). doi: 10.1038/nchembio.1313 pmid: 23892893
26. Pozdnyakov N., et al. -Secretase Modulator (GSM) Photoaffinity Probes Reveal Distinct Allosteric Binding Sites on Presenilin. J. Biol. Chem. 288, 9710–9720 (2013). doi: 10.1074/jbc.M112.398602 pmid: 23396974
27. Feng Z., Hu G., Ma S., Xie X.-Q., Computational Advances for the Development of Allosteric Modulators and Bitopic Ligands in G Protein-Coupled Receptors. AAPS J. 17, 1080–1095 (2015). doi: 10.1208/s12248-015-9776-y pmid: 25940084
28. Teşileanu T., Colwell L. J., Leibler S., Protein sectors: statistical coupling analysis versus conservation. PLoS Comput. Biol. 11, e1004091 (2015). doi: 10.1371/journal.pcbi.1004091 pmid: 25723535
29. Jardetzky O., Protein dynamics and conformational transitions in allosteric proteins. Prog. Biophys. Mol. Biol. 65, 171–219 (1996). pmid: 9062432
30. Huang W., et al. Allosite: a method for predicting allosteric sites. Bioinformatics29, 2357–2359 (2013). doi: 10.1093/bioinformatics/btt399 pmid: 23842804
31. Guarnera E., Berezovsky I. N., Structure-Based Statistical Mechanical Model Accounts for the Causality and Energetics of Allosteric Communication. PLoS Comput. Biol. 12, e1004678 (2016). doi: 10.1371/journal.pcbi.1004678 pmid: 26939022
32. Mitternacht S., Berezovsky I. N., Binding leverage as a molecular basis for allosteric regulation. PLoS Comput. Biol. 7, e1002148 (2011). doi: 10.1371/journal.pcbi.1002148 pmid: 21935347
33. Mitternacht S., Berezovsky I. N., Coherent conformational degrees of freedom as a structural basis for allosteric communication. PLoS Comput. Biol. 7, e1002301 (2011). doi: 10.1371/journal.pcbi.1002301 pmid: 22174669
34. Huang W., et al. ASBench: benchmarking sets for allosteric discovery: Fig 1. Bioinformatics31, 2598–2600 (2015). doi: 10.1093/bioinformatics/btv169 pmid: 25810427
35. Berezovsky I. N., Guarnera E., Zheng Z., Eisenhaber B., Eisenhaber F., Protein function machinery: from basic structural units to modulation of activity. Curr. Opin. Struct. Biol. 42, 67–74 (2017). doi: 10.1016/j.sbi.2016.10.021 pmid: 27865209
36. Popovych N., Tzeng S.-R., Tonelli M., Ebright R. H., Kalodimos C. G., Structural basis for cAMP-mediated allosteric control of the catabolite activator protein. Proc. Natl. Acad. Sci. U. S. A. 106, 6927–6932 (2009). doi: 10.1073/pnas.0900595106 pmid: 19359484
37. Townsend P. D., et al. The role of protein-ligand contacts in allosteric regulation of the Escherichia coli catabolite activator protein. J. Biol. Chem. 290, 22225–22235 (2015). doi: 10.1074/jbc.M115.669267 pmid: 26187469
38. Wu X., et al. Structural basis for a reciprocating mechanism of negative cooperativity in dimeric phosphagen kinase activity. FASEB J. 24, 242–252 (2010). doi: 10.1096/fj.09-140194 pmid: 19783784
39. Smith T. J., Stanley C. A., Untangling the glutamate dehydrogenase allosteric nightmare. Trends Biochem. Sci. 33, 557–564 (2008). doi: 10.1016/j.tibs.2008.07.007 pmid: 18819805
40. Li M., Li C., Allen A., Stanley C. A., Smith T. J., The structure and allosteric regulation of mammalian glutamate dehydrogenase. Arch. Biochem. Biophys. 519, 69–80 (2012). doi: 10.1016/j.abb.2011.10.015 pmid: 22079166
41. Horjales E., Altamirano M. M., Calcagno M. L., Garratt R. C., Oliva G., The allosteric transition of glucosamine-6-phosphate deaminase: the structure of the T state at 2.3 Å resolution. Structure7, 527–537 (1999). pmid: 10378272
42. Bustos-Jaimes I., Ramírez-Costa M., De Anda-Aguilar L., Hinojosa-Ocaña P., Calcagno M. L., Evidence for two different mechanisms triggering the change in quaternary structure of the allosteric enzyme, glucosamine-6-phosphate deaminase. Biochemistry44, 1127–1135 (2005). doi: 10.1021/bi048514o pmid: 15667206
43. Monod J., Changeux J.-P., Jacob F., Allosteric proteins and cellular control systems. J. Mol. Biol. 6, 306–329 (1963). pmid: 13936070
44. Benkovic S. J., deMaine M. M., Mechanism of Action of Fructose 1,6-Bisphosphatase. in Advances in Enzymology - and Related Areas of Molecular Biology45–82 (2006).
45. Hines J. K., Kruesel C. E., Fromm H. J., Honzatko R. B., Structure of inhibited fructose-1,6-bisphosphatase from Escherichia coli: distinct allosteric inhibition sites for AMP and glucose 6-phosphate and the characterization of a gluconeogenic switch. J. Biol. Chem. 282, 24697–24706 (2007). doi: 10.1074/jbc.M703580200 pmid: 17567577
46. Wright S. W., et al. Anilinoquinazoline Inhibitors of Fructose 1,6-Bisphosphatase Bind at a Novel Allosteric Site: Synthesis, In Vitro Characterization, and X-ray Crystallography. J. Med. Chem. 45, 3865–3877 (2002). pmid: 12190310
47. Hsu W.-C., Hung H.-C., Tong L., Chang G.-G., Dual functional roles of ATP in the human mitochondrial malic enzyme. Biochemistry43, 7382–7390 (2004). doi: 10.1021/bi049600r pmid: 15182181
48. Tang Q., Alontage A. Y., Holyoak T., Fenton A. W., Exploring the limits of the usefulness of mutagenesis in studies of allosteric mechanisms. Hum. Mutat. 38, 1144–1154 (2017). doi: 10.1002/humu.23239 pmid: 28459139
49. Chandramohan A., et al. Predicting allosteric effects from orthosteric binding in Hsp90-ligand interactions: Implications for fragment-based drug design. PLoS Comput. Biol. 12, e1004840 (2016). doi: 10.1371/journal.pcbi.1004840 pmid: 27253209
50. Gehrig S., et al. An engineered photoswitchable mammalian pyruvate kinase. FEBS J. 284, 2955–2980 (2017). doi: 10.1111/febs.14175 pmid: 28715126
51. Berman H. M., et al. The Protein Data Bank. Acta Crystallogr. D Biol. Crystallogr. 58, 899–907 (2002).
52. Krissinel E., Henrick K., Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774–797 (2007). doi: 10.1016/j.jmb.2007.05.022 pmid: 17681537
53. Hinsen K., Petrescu A.-J., Dellerue S., Bellissent-Funel M.-C., Kneller G. R., Harmonicity in slow protein dynamics. Chem. Phys. 261, 25–37 (2000).
54. Hinsen K., The molecular modeling toolkit: A new approach to molecular simulations. J. Comput. Chem. 21, 79–85 (2000).
55. Hinsen K., Analysis of domain motions by approximate normal mode calculations. Proteins33, 417–429 (1998). pmid: 9829700
56. Pettersen E. F., et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004). doi: 10.1002/jcc.20084 pmid: 15264254