Automated NMR fragment based screening identified a novel interface blocker to the LARG/RhoA complex

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Gao, Jia ^a   Ma, Rongsheng ^a   Wang, Wei ^b   Wang, Na ^a   Sasaki, Ryan ^c   Snyderman, David ^c   Wu, Jihui ^a   Ruan, Ke ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b PFIZER INC   (United States)

^c Advanced Chemistry Development Inc   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; LEUKEMIA ASSOCIATED RHO GUANINE EXCHANGE FACTOR; NITROGEN 15; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

AQUEOUS SOLUTION; ARTICLE; AUTOMATION; BINDING AFFINITY; BINDING ASSAY; CATALYSIS; COMPLEX FORMATION; ENZYME ACTIVATION; FRAGMENT BASED SCREENING; GEL ELECTROPHORESIS; LIGAND BINDING; MOLECULAR LIBRARY; NUCLEAR MAGNETIC RESONANCE; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; SCREENING; TITRIMETRY;

DRUG EVALUATION, PRECLINICAL; HUMANS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN INTERACTION MAPS; PROTEIN STRUCTURE, TERTIARY; RHO GUANINE NUCLEOTIDE EXCHANGE FACTORS; RHOA GTP-BINDING PROTEIN; SOLUBILITY; WATER;

EID: 84895548281     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088098     Document Type: Article

References (38)

1. Mullard A (2012) Protein-protein interaction inhibitors get into the groove. Nat Rev Drug Discov 11: 172-174.
2. Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, et al. (2004) In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303: 844-848. (Pubitemid 38174664)
3. Oltersdorf T, Elmore SW, Shoemaker AR, Armstrong RC, Augeri DJ, et al. (2005) An inhibitor of Bcl-2 family proteins induces regression of solid tumours. Nature 435: 677-681. (Pubitemid 40825512)
4. Shuker SB, Hajduk PJ, Meadows RP, Fesik SW (1996) Discovering high-affinity ligands for proteins: SAR by NMR. Science 274: 1531-1534. (Pubitemid 26403929)
5. Mayer M, Meyer B (1999) Characterization of ligand binding by saturation transfer difference NMR spectroscopy. Angew Chem Int Edit 38: 1784-1788. (Pubitemid 29290947)
6. Dalvit C, Fogliatto G, Stewart A, Veronesi M, Stockman B (2001) Water-LOGSY as a method for primary NMR screening: Practical aspects and range of applicability. J Biomol NMR 21: 349-359. (Pubitemid 34071389)
7. Gossert AD, Henry C, Blommers MJJ, Jahnke W, Fernandez C (2009) Time efficient detection of protein-ligand interactions with the polarization optimized PO-WaterLOGSY NMR experiment. J Biomol NMR 43: 211-217.
8. Schade M, Oschkinat H (2005) NMR fragment screening: Tackling proteinprotein interaction targets. Curr Opin Drug Discov Dev 8: 365-373. (Pubitemid 40593431)
9. Murray CW, Rees DC (2009) The rise of fragment-based drug discovery. Nat Chem 1: 187-192.
10. Jaiswal M, Gremer L, Dvorsky R, Haeusler LC, Cirstea IC, et al. (2011) Mechanistic Insights into Specificity, Activity, and Regulatory Elements of the Regulator of G-protein Signaling (RGS)-containing Rho-specific Guanine Nucleotide Exchange Factors (GEFs) p115, PDZ-RhoGEF (PRG), and Leukemia-associated RhoGEF (LARG). J Biol Chem 286: 18202-18212.
11. Wang Q, Liu M, Kozasa T, Rothstein JD, Sternweis PC, et al. (2004) Thrombin and lysophosphatidic acid receptors utilize distinct rhoGEFs in prostate cancer cells. J Biol Chem 279: 28831-28834. (Pubitemid 38915749)
12. Guilluy C, Swaminathan V, Garcia-Mata R, O'Brien ET, Superfine R, et al. (2011) The Rho GEFs LARG and GEF-H1 regulate the mechanical response to force on integrins. Nat Cell Biol 13: 722-727.
13. Kitzing TM, Sahadevan AS, Brandt DT, Knieling H, Hannemann S, et al. (2007) Positive feedback between Dia1, LARG, and RhoA regulates cell morphology and invasion. Gene Dev 21: 1478-1483. (Pubitemid 46955720)
14. Zheng R, Iwase A, Shen R, Goodman OB, Jr., Sugimoto N, et al. (2006) Neuropeptide-stimulated cell migration in prostate cancer cells is mediated by RhoA kinase signaling and inhibited by neutral endopeptidase. Oncogene 25: 5942-5952. (Pubitemid 44477288)
15. Rujkijyanont P, Beyene J, Wei KR, Dror Y (2005) Leukemia-related gene expression of bone marrow cells from patients with Shwachman-Diamond syndrome at the pre-leukemic phase. Blood 106: 3433-3433.
16. Wirth A, Benyo Z, Lukasova M, Leutgeb B, Wettschureck N, et al. (2008) G12- G13-LARG-mediated signaling in vascular smooth muscle is required for saltinduced hypertension. Nat Med 14: 64-68.
17. Hata K, Kaibuchi K, Inagaki S, Yamashita T (2009) Unc5B associates with LARG to mediate the action of repulsive guidance molecule. J Cell Biol 184: 737-750.
18. Kristelly R, Gao G, Tesmer JJG (2004) Structural Determinants of RhoA Binding and Nucleotide Exchange in Leukemia-associated Rho Guanine-Nucleotide Exchange Factor. J Biol Chem 279: 47352-47362. (Pubitemid 39518392)
19. Maurer T, Garrenton LS, Oha A, Pitts K, Anderson DJ, et al. (2012) Smallmolecule ligands bind to a distinct pocket in Ras and inhibit SOS-mediated nucleotide exchange activity. Proc Natl Acad Sci U S A 109: 5299-5304.
20. Deng J, Feng E, Ma S, Zhang Y, Liu X, et al. (2011) Design and Synthesis of Small Molecule RhoA Inhibitors: A New Promising Therapy for Cardiovascular Diseases? J Med Chem 54: 4508-4522.
21. Renault L, Guibert B, Cherfils J (2003) Structural snapshots of the mechanism and inhibition of a guanine nucleotide exchange factor. Nature 426: 525-530. (Pubitemid 37522634)
22. Sun Q, Burke JP, Phan J, Burns MC, Olejniczak ET, et al. (2012) Discovery of Small Molecules that Bind to K-Ras and Inhibit Sos-Mediated Activation. Angew Chem Int Edit 51: 6140-6143.
23. Wang YX, Kaiser CE, Frett B, Li HY (2013) Targeting Mutant KRAS for Anticancer Therapeutics: A Review of Novel Small Molecule Modulators. JMed Chem 56: 5219-5230.
24. Congreve M, Carr R, Murray C, Jhoti H (2003) A 'rule of three' for fragment-based lead discovery? Drug Discov Today 8: 876-877. (Pubitemid 37194496)
25. Maili L, Xi-An M, Chaohui Y, He H, Nicholson JK, et al. (1998) Improved WATERGATE pulse sequences for solvent suppression in NMR spectroscopy. J Magn Reson 132: 125-129. (Pubitemid 128450594)
26. Mayer M, Meyer B (2001) Group Epitope Mapping by Saturation Transfer Difference NMR To Identify Segments of a Ligand in Direct Contact with a Protein Receptor. J Am Chem Soc 123: 6108-6117. (Pubitemid 32888480)
27. Pervushin K, Riek R, Wider G, Wuthrich K (1997) Attenuated T-2 relaxation by mutual cancellation of dipole-dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution. Proc Natl Acad Sci U S A 94: 12366-12371.
28. Liu X, Kolpak MX, Wu J, Leo GC (2012) Automatic Analysis of Quantitative NMR Data of Pharmaceutical Compound Libraries. Anal Chem 84: 6914-6918.
29. Golotvin SS, Vodopianov E, Lefebvre BA, Williams AJ, Spitzer TD (2006) Automated structure verification based on H-1 NMR prediction. Magn Reson Chem 44: 524-538. (Pubitemid 43672059)
30. Smurnyy YD, Blinov KA, Churanova TS, Elyashberg ME, Williams AJ (2008) Toward more reliable C-13 and H-1 chemical shift prediction: A systematic comparison of neural-network and least-squares regression based approaches. J Chem Inf Model 48: 128-134. (Pubitemid 351271057)
31. Lipinski CA, Lombardo F, Dominy BW, Feeney PJ (1997) Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 23: 3-25. (Pubitemid 27046991)
32. Hubbard RE, Davis B, Chen I, Drysdale MJ (2007) The SeeDs approach: integrating fragments into drug discovery. Curr Top Med Chem 7: 1568-1581. (Pubitemid 350131015)
33. Hajduk PJ, Huth JR, Fesik SW (2005) Druggability indices for protein targets derived from NMR-based screening data. J Med Chem 48: 2518-2525. (Pubitemid 40516441)
34. Arroyo X, Goldflam M, Feliz M, Belda I, Giralt E (2013) Computer-Aided Design of Fragment Mixtures for NMR-Based Screening. PLoS One 8: e58571.
35. Gasmi-Seabrook GMC, Marshall CB, Cheung M, Kim B, Wang F, et al. Realtime NMR Study of Guanine Nucleotide Exchange and Activation of RhoA by PDZ-RhoGEF. J Biol Chem 285: 5137-5145.
36. Lingel A, Simon B, Izaurralde E, Sattler M (2005) The structure of the flock house virus B2 protein, a viral suppressor of RNA interference, shows a novel mode of double-stranded RNA recognition. EMBO Rep 6: 1149-1155. (Pubitemid 41741698)
37. Wu GS, Robertson DH, Brooks CL, Vieth M (2003) Detailed analysis of grid-based molecular docking: A case study of CDOCKER - A CHARMm-based MD docking algorithm. J Comput Chem 24: 1549-1562.
38. Shang X, Marchioni F, Sipes N, Evelyn CR, Jerabek-Willemsen M, et al. (2012) Rational Design of Small Molecule Inhibitors Targeting RhoA Subfamily Rho GTPases. Chem & Biol 19: 699-710.