Small Molecules, Peptides and Natural Products: Getting a Grip on 14-3-3 Protein–Protein Modulation

References

• Perkins JR , DibounI, DessaillyBH, LeesJG, OrengoC. Transient protein–protein interactions: structural, functional, and network properties. Structure18 (10), 1233–1243 (2010).
   PubMed Web of Science ®Google Scholar
• Kastritis PL , BonvinAMJJ. On the binding affinity of macromolecular interactions: daring to ask why proteins interact. J. R. Soc. Interface10 (79), 20120835 (2013).
   PubMed Web of Science ®Google Scholar
• Uhart M , BustosDM. Protein intrinsic disorder and network connectivity. The case of 14-3-3 proteins. Front. Genet.5, 10 (2014).
   PubMed Web of Science ®Google Scholar
• De Las Rivas J , FontanilloC. Protein–protein interactions essentials: key concepts to building and analyzing interactome networks. PLoS Comput. Biol.6 (6), e1000807 (2010).
   PubMed Web of Science ®Google Scholar
• Landry CR , LevyED, Abd RabboD, TarassovK, MichnickSW. Extracting insight from noisy cellular networks. Cell155 (5), 983–989 (2013).
   PubMed Web of Science ®Google Scholar
• Kiel C , BeltraoP, SerranoL. Analyzing protein interaction networks using structural information. Annu. Rev. Biochem.77, 415–441 (2008).
   PubMed Web of Science ®Google Scholar
• Kiel C , SerranoL. Structural data in synthetic biology approaches for studying general design principles of cellular signaling networks. Structure20 (11), 1806–1813 (2012).
   PubMed Web of Science ®Google Scholar
• Nooren IM ., ThorntonJM. Structural characterisation and functional significance of transient protein–protein interactions. J. Mol. Biol.325 (5), 991–1018 (2003).
   PubMed Web of Science ®Google Scholar
• Schwartz TW , HolstB. Allosteric enhancers, allosteric agonists and ago-allosteric modulators: where do they bind and how do they act ? Trends Pharmacol. Sci.28 (8), 366–373 (2007).
   PubMed Web of Science ®Google Scholar
• Block P , WeskampN, WolfA, KlebeG. Strategies to search and design stabilizers of protein–protein interactions: a feasibility study. Proteins68 (1), 170–186 (2007).
   PubMed Web of Science ®Google Scholar
• Thiel P , KaiserM, OttmannC. Small-molecule stabilization of protein–protein interactions: an underestimated concept in drug discovery ? Angew. Chem. Int. Ed.51 (9), 2012–2018 (2012).
   PubMed Web of Science ®Google Scholar
• Pommier Y , MarchandC. Interfacial inhibitors: targeting macromolecular complexes. Nat. Rev. Drug Discov.11 (1), 25–36 (2012).
   Web of Science ®Google Scholar
• Choi J , ChenJ, SchreiberS, ClardyJ. Structure of the FKBP12-rapamycin complex interacting with binding domain of human FRAP. Science273 (5272), 239–242 (1996).
   PubMed Web of Science ®Google Scholar
• Tesmer JJ . Crystal structure of the catalytic domains of adenylyl cyclase in a complex with Gs·GTPS. Science278 (5345), 1907–1916 (1997).
   PubMed Web of Science ®Google Scholar
• Renault L , GuibertB, CherfilsJ. Structural snapshots of the mechanism and inhibition of a guanine nucleotide exchange factor. Nature426 (6966), 525–530 (2003).
   PubMed Web of Science ®Google Scholar
• Tan X , Calderon-VillalobosLI, SharonMet al. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature446 (7136), 640–645 (2007).
   PubMed Web of Science ®Google Scholar
• Sheard LB , TanX, MaoHet al. Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature468 (7322), 400–405 (2010).
   PubMed Web of Science ®Google Scholar
• Watson PJ , FairallL, SantosGM, SchwabeJWR. Structure of HDAC3 bound to co-repressor and inositol tetraphosphate. Nature481 (7381), 335–340 (2012).
   PubMed Web of Science ®Google Scholar
• Taylor IW , LindingR, Warde-FarleyDet al. Dynamic modularity in protein interaction networks predicts breast cancer outcome. Nat. Biotechnol.27 (2), 199–204 (2009).
   PubMed Web of Science ®Google Scholar
• Cino EA , KilloranRC, KarttunenM, ChoyWY. Binding of disordered proteins to a protein hub. Sci. Rep.3, 2305 (2013).
   PubMed Web of Science ®Google Scholar
• Tuncbag N , KarG, KeskinO, GursoyA, NussinovR. A survey of available tools and web servers for analysis of protein–protein interactions and interfaces. Brief. Bioinform.10 (3), 217–232 (2009).
   PubMed Web of Science ®Google Scholar
• Moore BW , PerezVJ, GehringM. Assay and regional distribution of a soluble protein characteristic of the nervous system. J. Neurochem.15 (4), 265–272 (1968).
   PubMed Web of Science ®Google Scholar
• Johnson C , CrowtherS, StaffordMJ, CampbellDG, TothR, MacKintoshC. Bioinformatic and experimental survey of 14-3-3-binding sites. Biochem. J.427 (1), 69–78 (2010).
   PubMedGoogle Scholar
• PubMed database. www.pubmed.gov
   Google Scholar
• Aitken A . 14-3-3 proteins: a historic overview. Semin. Cancer Biol.16 (3), 162–172 (2006).
   PubMed Web of Science ®Google Scholar
• Pozuelo Rubio M , GeraghtyKM, WongBHCet al. 14-3-3-affinity purification of over 200 human phosphoproteins reveals new links to regulation of cellular metabolism, proliferation and trafficking. Biochem. J.379 (Pt 2), 395–408 (2004).
   PubMedGoogle Scholar
• Tinti M , MadeiraF, MurugesanG, HoxhajG, TothR, MacKintoshC. ANIA: annotation and integrated analysis of the 14-3-3 interactome. Database2014, bat085–bat085 (2014).
   PubMedGoogle Scholar
• Molzan M , SchumacherB, OttmannCet al. Impaired binding of 14-3-3 to C-RAF in Noonan syndrome suggests new approaches in diseases with increased Ras signaling. Mol. Cell. Biol.30 (19), 4698–4711 (2010).
   PubMed Web of Science ®Google Scholar
• Schumacher B , MondryJ, ThielP, WeyandM, OttmannC. Structure of the p53 C-terminus bound to 14-3-3: implications for stabilization of the p53 tetramer. FEBS Lett.584 (8), 1443–1448 (2010).
   PubMed Web of Science ®Google Scholar
• Hermeking H , BenzingerA. 14-3-3 proteins in cell cycle regulation. Semin. Cancer Biol.16 (3), 183–192 (2006).
   PubMed Web of Science ®Google Scholar
• Corradi V , ManciniM, ManettiF, PettaS, SantucciMA, BottaM. Identification of the first non-peptidic small molecule inhibitor of the c-Abl/14-3-3 protein-protein interactions able to drive sensitive and Imatinib-resistant leukemia cells to apoptosis. Bioorg. Med. Chem. Lett.20 (20), 6133–6137 (2010).
   PubMed Web of Science ®Google Scholar
• Morrison DK . The 14-3-3 proteins: integrators of diverse signaling cues that impact cell fate and cancer development. Trends Cell Biol.19 (1), 16–23 (2009).
   PubMed Web of Science ®Google Scholar
• Coblitz B , ShikanoS, WuMet al. C-terminal recognition by 14-3-3 proteins for surface expression of membrane receptors. J. Biol. Chem.280 (43), 36263–36272 (2005).
   PubMed Web of Science ®Google Scholar
• Yaffe MB , RittingerK, VoliniaSet al. The structural basis for 14-3-3: phosphopeptide binding specificity. Cell91 (7), 961–971 (1997).
   PubMed Web of Science ®Google Scholar
• Muslin AJ , TannerJW, AllenPM, ShawAS. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell84 (6), 889–897 (1996).
   PubMed Web of Science ®Google Scholar
• Liu D , BienkowskaJ, PetosaC, CollierRJJ, FuH, LiddingtonR. Crystal structure of the zeta isoform of the 14-3-3 protein. Nature376 (6536), 191–194 (1995).
   PubMed Web of Science ®Google Scholar
• Xiao B , SmerdonSJ, JonesDHet al. Structure of a 14-3-3 protein and implications for coordination of multiple signalling pathways. Nature376 (6536), 188–191 (1995).
   PubMed Web of Science ®Google Scholar
• Takemoto Y , WatanabeH, UchidaK. Chemistry and biology of moverastins, inhibitors of cancer cell migration, produced by Aspergillus. Chem. Biol.12 (12), 1337–1347 (2005).
   PubMedGoogle Scholar
• Sawada M , KuboS, MatsumuraK. Synthesis and anti-migrative evaluation of moverastin derivatives. Bioorg. Med. Chem. Lett.21 (5), 1385–1389 (2011).
   PubMed Web of Science ®Google Scholar
• Kobayashi H , OguraY, SawadaMet al. Involvement of 14-3-3 proteins in the second epidermal growth factor-induced wave of Rac1 activation in the process of cell migration. J. Biol. Chem.286 (45), 39259–39268 (2011).
   PubMed Web of Science ®Google Scholar
• Wang B , YangH, LiuY-Cet al. Isolation of high-affinity peptide antagonists of 14-3-3 proteins by phage display. Biochemistry38 (38), 12499–12504 (1999).
   PubMed Web of Science ®Google Scholar
• Rose R , ErdmannS, BovensSet al. Identification and structure of small-molecule stabilizers of 14-3-3 protein-protein interactions. Angew. Chemie Int. Ed.49 (24), 4129–4132 (2010).
   PubMed Web of Science ®Google Scholar
• Arrendale A , KimK, ChoiJY, LiW, GeahlenRL, BorchRF. Synthesis of a phosphoserine mimetic prodrug with potent 14-3-3 protein inhibitory activity. Chem. Biol.19 (6), 764–771 (2012).
   PubMedGoogle Scholar
• Maki T , KawamuraA, KatoN, OhkandaJ. Chemical ligation of epoxide-containing fusicoccins and peptide fragments guided by 14-3-3 protein. Mol. Biosyst.9 (5), 940–943 (2013).
   PubMedGoogle Scholar
• Yang X , LeeWH, SobottFet al. Structural basis for protein–protein interactions in the 14-3-3 protein family. Proc. Natl. Acad. Sci.103 (46), 17237–17242 (2006).
   PubMed Web of Science ®Google Scholar
• Ottmann C , YasminL, WeyandMet al. Phosphorylation-independent interaction between 14-3-3 and exoenzyme S: from structure to pathogenesis. EMBO J.26 (3), 902–913 (2007).
   PubMed Web of Science ®Google Scholar
• Glas A , BierD, HahneG, RademacherC, OttmannC, GrossmannTN. Constrained peptides with target-adapted crosslinks as inhibitors of a pathogenic protein–protein interaction. Angew. Chem. Int. Ed.53 (9), 2489–2493 (2014).
   PubMed Web of Science ®Google Scholar
• Levy ED , MichnickSW, LandryCR. Protein abundance is key to distinguish promiscuous from functional phosphorylation based on evolutionary information. Philos. Trans. R. Soc. Lond. B. Biol. Sci.367 (1602), 2594–2606 (2012).
   PubMed Web of Science ®Google Scholar
• Landry CR , LevyED, MichnickSW. Weak functional constraints on phosphoproteomes. Trends Genet.25 (5), 193–197 (2009).
   PubMed Web of Science ®Google Scholar
• Simon M , AbelsonJN. Combinatorial Chemistry. In: Methods in Enzymology. Academic Press, NY, USA, 3–493 (1996).
   Google Scholar
• Petosa C , MastersSC, BankstonLAet al. 14-3-3zeta binds a phosphorylated Raf peptide and an unphosphorylated peptide via its conserved amphipathic groove. J. Biol. Chem.273 (26), 16305–16310 (1998).
   PubMed Web of Science ®Google Scholar
• Masters SC , FuH. 14-3-3 proteins mediate an essential anti-apoptotic signal. J. Biol. Chem.276 (48), 45193–45200 (2001).
   PubMed Web of Science ®Google Scholar
• Wu H , GeJ, YaoSQ. Microarray-assisted high-throughput identification of a cell-permeable small-molecule binder of 14-3-3 proteins. Angew. Chemie Int. Ed.49 (37), 6528–6532 (2010).
   PubMed Web of Science ®Google Scholar
• MacBeath G , KoehlerAN, SchreiberSL. Printing small molecules as microarrays and detecting protein−ligand interactions en masse. J. Am. Chem. Soc.121 (34), 7967–7968 (1999).
   Web of Science ®Google Scholar
• Tzivion G , DobsonM, RamakrishnanG. FoxO transcription factors; Regulation by AKT and 14-3-3 proteins. Biochim. Biophys. Acta.1813 (11), 1938–1945 (2011).
   PubMed Web of Science ®Google Scholar
• Morsomme P , BoutryM. The plant plasma membrane H+-ATPase: structure, function and regulation. Biochim. Biophys. Acta Biomembr.1465 (1 – 2), 1–16 (2000).
   Web of Science ®Google Scholar
• Röglin L , ThielP, KohlbacherO, OttmannC. Covalent attachment of pyridoxal-phosphate derivatives to 14-3-3 proteins. Proc. Natl Acad. Sci. USA109 (18), E1051–E1053 (2012).
   PubMed Web of Science ®Google Scholar
• Bier D , RoseR, Bravo-RodriguezKet al. Molecular tweezers modulate 14-3-3 protein–protein interactions. Nat. Chem.5 (3), 234–239 (2013).
   PubMed Web of Science ®Google Scholar
• Berman HM , WestbrookJ, FengZet al. The protein data bank. Nucleic Acids Res.28 (1), 235–242 (2000).
   PubMed Web of Science ®Google Scholar
• Mancini M , CorradiV, PettaSet al. A new nonpeptidic inhibitor of 14-3-3 induces apoptotic cell death in chronic myeloid leukemia sensitive or resistant to imatinib. J. Pharmacol. Exp. Ther.336 (3), 596–604 (2011).
   PubMed Web of Science ®Google Scholar
• Corradi V , ManciniM, SantucciMAet al. Computational techniques are valuable tools for the discovery of protein–protein interaction inhibitors: the 14-3-3σ case. Bioorg. Med. Chem. Lett.21 (22), 6867–6871 (2011).
   PubMed Web of Science ®Google Scholar
• Zhao J , DuY, HortonJRet al. Discovery and structural characterization of a small molecule 14-3-3 protein-protein interaction inhibitor. Proc. Natl. Acad. Sci.108 (39), 16212–16216 (2011).
   PubMed Web of Science ®Google Scholar
• Du Y , FuRW, LouBet al. A time-resolved fluorescence resonance energy transfer assay for high-throughput screening of 14-3-3 protein-protein interaction inhibitors. Assay Drug Dev. Technol.11 (6), 367–381 (2013).
   PubMed Web of Science ®Google Scholar
• Thiel P , RöglinL, MeissnerN, HennigS, KohlbacherO, OttmannC. Virtual screening and experimental validation reveal novel small-molecule inhibitors of 14-3-3 protein–protein interactions. Chem. Commun.49 (76), 8468–8470 (2013).
   PubMed Web of Science ®Google Scholar
• Ghahary A , MarcouxY, Karimi-BusheriFet al. Differentiated keratinocyte-releasable stratifin (14-3-3 sigma) stimulates MMP-1 expression in dermal fibroblasts. J. Invest. Dermatol.124 (1), 170–177 (2005).
   PubMed Web of Science ®Google Scholar
• Gialeli C , TheocharisAD, KaramanosNK. Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J.278 (1), 16–27 (2011).
   PubMed Web of Science ®Google Scholar
• Khokha R , MurthyA, WeissA. Metalloproteinases and their natural inhibitors in inflammation and immunity. Nat. Rev. Immunol.13 (9), 649–665 (2013).
   PubMed Web of Science ®Google Scholar
• Park KD , KimD, ReamtongOet al. Identification of a lacosamide binding protein using an affinity bait and chemical reporter strategy: 14-3-3 ζ. J. Am. Chem. Soc.133 (29), 11320–11330 (2011).
   PubMed Web of Science ®Google Scholar
• An SS , AskovichPS, ZarembinskiTIet al. A novel small molecule target in human airway smooth muscle for potential treatment of obstructive lung diseases: a staged high-throughput biophysical screening. Respir. Res.12, 8 (2011).
   PubMed Web of Science ®Google Scholar
• Yan Y-M , DaiH-Q, DuYet al. Identification of blapsins A and B as potent small-molecule 14-3-3 inhibitors from the insect Blaps japanensis. Bioorg. Med. Chem. Lett.22 (12), 4179–4181 (2012).
   PubMed Web of Science ®Google Scholar
• Jahn T , FuglsangT, OlssonAet al. The 14-3-3 protein interacts directly with the C-terminal region of the plant plasma membrane H(+)-ATPase. Plant Cell.9 (10), 1805–1814 (1997).
   PubMed Web of Science ®Google Scholar
• Maudoux O , BatokoH, OeckingCet al. A plant plasma membrane H+-ATPase expressed in yeast is activated by phosphorylation at its penultimate residue and binding of 14-3-3 regulatory proteins in the absence of fusicoccin. J. Biol. Chem.275 (23), 17762–17770 (2000).
   PubMed Web of Science ®Google Scholar
• Würtele M , Jelich-OttmannC, WittinghoferA, OeckingC. Structural view of a fungal toxin acting on a 14-3-3 regulatory complex. EMBO J.22 (5), 987–994 (2003).
   PubMed Web of Science ®Google Scholar
• Ottmann C , MarcoS, JaspertNet al. Structure of a 14-3-3 coordinated hexamer of the plant plasma membrane H+ -ATPase by combining X-ray crystallography and electron cryomicroscopy. Mol. Cell.25 (3), 427–440 (2007).
   PubMed Web of Science ®Google Scholar
• Varga-Szabo D , PleinesI, NieswandtB. Cell adhesion mechanisms in platelets. Arterioscler. Thromb. Vasc. Biol.28 (3), 403–412 (2008).
   PubMed Web of Science ®Google Scholar
• Camoni L , Di LucenteC, ViscontiS, AducciP. The phytotoxin fusicoccin promotes platelet aggregation via 14-3-3-glycoprotein Ib-IX-V interaction. Biochem. J.436 (2), 429–436 (2011).
   PubMedGoogle Scholar
• De Boer AH , de Vries-van LeeuwenIJ. Fusicoccanes: diterpenes with surprising biological functions. Trends Plant Sci.17 (6), 360–368 (2012).
   PubMed Web of Science ®Google Scholar
• Molzan M , KasperS, RöglinL Stabilization of physical RAF/14-3-3 interaction by cotylenin A as treatment strategy for RAS mutant cancers. ACS Chem. Biol.8 (9), 1869–1875 (2013).
   PubMed Web of Science ®Google Scholar
• Richter A , RoseR, HedbergC, WaldmannH, OttmannC. An optimised small-molecule stabiliser of the 14-3-3-PMA2 protein-protein interaction. Chem. A Eur. J.18 (21), 6520–6527 (2012).
   PubMed Web of Science ®Google Scholar
• Bittner S , BuddeT, WiendlH, MeuthSG. From the background to the spotlight: TASK channels in pathological conditions. Brain Pathol.20 (6), 999–1009 (2010).
   PubMed Web of Science ®Google Scholar
• Anders C , HiguchiY, KoschinskyKet al. A semisynthetic fusicoccane stabilizes a protein–protein interaction and enhances the expression of K+ channels at the cell surface. Chem. Biol.20 (4), 583–593 (2013).
   PubMedGoogle Scholar
• Tzivion G , LuoZ, AvruchJ. A dimeric 14-3-3 protein is an essential cofactor for Raf kinase activity. Nature394 (6688), 88–92 (1998).
   PubMed Web of Science ®Google Scholar
• Dumaz N , MaraisR. Protein kinase A blocks Raf-1 activity by stimulating 14-3-3 binding and blocking Raf-1 interaction with Ras. J. Biol. Chem.278 (32), 29819–29823 (2003).
   PubMed Web of Science ®Google Scholar
• De Vries-van Leeuwen IJ , da Costa PereiraD, FlachKDet al. Interaction of 14-3-3 proteins with the estrogen receptor alpha F domain provides a drug target interface. Proc. Natl Acad. Sci. USA110 (22), 8894–8899 (2013).
   PubMed Web of Science ®Google Scholar
• Skwarczynska M , MolzanM, OttmannC. Activation of NF-κB signalling by fusicoccin-induced dimerization. Proc. Natl Acad. Sci. USA110 (5), E377–E386 (2013).
   PubMedGoogle Scholar