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Current Computer-Aided Drug Design

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ISSN (Print): 1573-4099
ISSN (Online): 1875-6697

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Research Article

Targeting Peptidyl-prolyl Cis-trans Isomerase NIMA-interacting 1: A Structure-based Virtual Screening Approach to Find Novel Inhibitors

Author(s): Kauê Santana da Costa*, João M. Galúcio, Deivid Almeida de Jesus, Guelber Cardoso Gomes, Anderson Henrique Lima e Lima, Paulo S. Taube, Alberto M. dos Santos and Jerônimo Lameira*

Volume 16, Issue 5, 2020

Page: [605 - 617] Pages: 13

DOI: 10.2174/1573409915666191025114009

Price: $65

Abstract

Background: Peptidyl-prolyl cis-trans isomerase NIMA-interacting 1 (Pin1) is an enzyme that isomerizes phosphorylated serine or threonine motifs adjacent to proline residues. Pin1 has important roles in several cellular signaling pathways, consequently impacting the development of multiple types of cancers.

Methods: Based on the previously reported inhibitory activity of pentacyclic triterpenoids isolated from the gum resin of Boswellia genus against Pin1, we designed a computational experiment using molecular docking, pharmacophore filtering, and structural clustering allied to molecular dynamics (MD) simulations and binding free energy calculations to explore the inhibitory activity of new triterpenoids against Pin1 structure.

Results: Here, we report different computational evidence that triterpenoids from neem (Azadirachta indica A. Juss), such as 6-deacetylnimbinene, 6-Oacetylnimbandiol, and nimbolide, replicate the binding mode of the Pin1 substrate peptide, interacting with high affinity with the binding site and thus destabilizing the Pin1 structure.

Conclusions: Our results are supported by experimental data, and provide interesting structural insights into their molecular mechanism of action, indicating that their structural scaffolds could be used as a start point to develop new inhibitors against Pin1.

Keywords: Cancer targeting, peptidyl-prolyl isomerase, triterpenoids, molecular modeling, natural products, virtual screening.

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[1]
Roth, G.A. Global, regional, and national prevalence, mortality, years of life lost, years lived with disability, and disability-adjusted life years for 10 Causes of Cardiovascular Disease, 1990 to 2015 – a systematic analysis for the Global Burden of Disease. JAMA Oncol., 2015, 3, 1-20.
[2]
Holohan, C.; Van Schaeybroeck, S.; Longley, D.B.; Johnston, P.G. Cancer drug resistance: an evolving paradigm. Nat. Rev. Cancer, 2013, 13(10), 714-726.
[http://dx.doi.org/10.1038/nrc3599] [PMID: 24060863]
[3]
Settleman, J. Cancer: Bet on drug resistance. Nature, 2016, 529(7586), 289-290.
[http://dx.doi.org/10.1038/nature16863] [PMID: 26735017]
[4]
Awasthi, M.; Singh, S.; Pandey, V.P.; Dwivedi, U.N. Molecular docking and 3D-QSAR-based virtual screening of flavonoids as potential aromatase inhibitors against estrogen-dependent breast cancer. J. Biomol. Struct. Dyn., 2015, 33(4), 804-819.
[http://dx.doi.org/10.1080/07391102.2014.912152] [PMID: 24702656]
[5]
Galúcio, J.M.; Monteiro, E.F.; de Jesus, D.A.; Costa, C.H.; Siqueira, R.C.; Santos, G.B.D.; Lameira, J.; Costa, K.S.D. In silico identification of natural products with anticancer activity using a chemo-structural database of Brazilian biodiversity. Comput. Biol. Chem., 2019.83107102
[http://dx.doi.org/10.1016/j.compbiolchem.2019.107102] [PMID: 31487609]
[6]
Azminah, A.; Erlina, L.; Radji, M.; Mun’im, A.; Syahdi, R.R.; Yanuar, A. In silico and in vitro identification of candidate SIRT1 activators from Indonesian medicinal plants compounds database. Comput. Biol. Chem., 2019.83107096
[http://dx.doi.org/10.1016/j.compbiolchem.2019.107096] [PMID: 31377446]
[7]
Rampogu, S.; Son, M.; Baek, A.; Park, C.; Rana, R.M.; Zeb, A.; Parameswaran, S.; Lee, K.W. Targeting natural compounds against HER2 kinase domain as potential anticancer drugs applying pharmacophore based molecular modelling approaches. Comput. Biol. Chem., 2018, 74, 327-338.
[http://dx.doi.org/10.1016/j.compbiolchem.2018.04.002] [PMID: 29702367]
[8]
Zhang, H-Y. Structure-Activity Relationships and Rational Design Strategies for Radical- Scavenging Antioxidants. Curr. Comput. Aided-Drug Des., 2005, 1, 257-273.
[http://dx.doi.org/10.2174/1573409054367691]
[9]
Blume-Jensen, P.; Hunter, T. Oncogenic kinase signalling. Nature, 2001, 411(6835), 355-365.
[http://dx.doi.org/10.1038/35077225] [PMID: 11357143]
[10]
Liao, X.H.; Zhang, A.L.; Zheng, M.; Li, M.Q.; Chen, C.P.; Xu, H.; Chu, Q.S.; Yang, D.; Lu, W.; Tsai, T.F.; Liu, H.; Zhou, X.Z.; Lu, K.P. Chemical or genetic Pin1 inhibition exerts potent anticancer activity against hepatocellular carcinoma by blocking multiple cancer-driving pathways. Sci. Rep., 2017, 7, 43639.
[http://dx.doi.org/10.1038/srep43639] [PMID: 28262728]
[11]
Ranganathan, R.; Lu, K.P.; Hunter, T.; Noel, J.P. Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent. Cell, 1997, 89(6), 875-886.
[http://dx.doi.org/10.1016/S0092-8674(00)80273-1] [PMID: 9200606]
[12]
Zhou, X.Z.; Lu, K.P. The isomerase PIN1 controls numerous cancer-driving pathways and is a unique drug target. Nat. Rev. Cancer, 2016, 16(7), 463-478.
[http://dx.doi.org/10.1038/nrc.2016.49] [PMID: 27256007]
[13]
Bao, L.; Kimzey, A.; Sauter, G.; Sowadski, J.M.; Lu, K.P.; Wang, D.G. Prevalent overexpression of prolyl isomerase Pin1 in human cancers. Am. J. Pathol., 2004, 164(5), 1727-1737.
[http://dx.doi.org/10.1016/S0002-9440(10)63731-5] [PMID: 15111319]
[14]
Franciosa, G.; Diluvio, G.; Gaudio, F.D.; Giuli, M.V.; Palermo, R.; Grazioli, P.; Campese, A.F.; Talora, C.; Bellavia, D.; D’Amati, G.; Besharat, Z.M.; Nicoletti, C.; Siebel, C.W.; Choy, L.; Rustighi, A.; Sal, G.D.; Screpanti, I.; Checquolo, S. Prolyl-isomerase Pin1 controls Notch3 protein expression and regulates T-ALL progression. Oncogene, 2016, 35(36), 4741-4751.
[http://dx.doi.org/10.1038/onc.2016.5] [PMID: 26876201]
[15]
Girardini, J.E.; Napoli, M.; Piazza, S.; Rustighi, A.; Marotta, C.; Radaelli, E.; Capaci, V.; Jordan, L.; Quinlan, P.; Thompson, A.; Mano, M.; Rosato, A.; Crook, T.; Scanziani, E.; Means, A.R.; Lozano, G.; Schneider, C.; Del Sal, G.A. Pin1/mutant p53 axis promotes aggressiveness in breast cancer. Cancer Cell, 2011, 20(1), 79-91.
[http://dx.doi.org/10.1016/j.ccr.2011.06.004] [PMID: 21741598]
[16]
Hu, X.; Dong, S.H.; Chen, J.; Zhou, X.Z.; Chen, R.; Nair, S.; Lu, K.P.; Chen, L.F. Prolyl isomerase PIN1 regulates the stability, transcriptional activity and oncogenic potential of BRD4. Oncogene, 2017, 36(36), 5177-5188.
[http://dx.doi.org/10.1038/onc.2017.137] [PMID: 28481868]
[17]
Krishnan, N.; Titus, M.A.; Thapar, R. The prolyl isomerase pin1 regulates mRNA levels of genes with short half-lives by targeting specific RNA binding proteins. PLoS One, 2014, 9(1),e85427.
[http://dx.doi.org/10.1371/journal.pone.0085427] [PMID: 24416409]
[18]
Hilton, B.A.; Li, Z.; Musich, P.R.; Wang, H.; Cartwright, B.M.; Serrano, M.; Zhou, X.Z.; Lu, K.P.; Zou, Y. ATR plays a direct antiapoptotic role at mitochondria, which is regulated by prolyl isomerase pin1. Mol. Cell, 2015, 60(1), 35-46.
[http://dx.doi.org/10.1016/j.molcel.2015.08.008] [PMID: 26387736]
[19]
Hwang, Y.C.; Yang, C.H.; Lin, C.H.; Ch’ang, H.J.; Chang, V.H.S.; Yu, W.C.Y. Destabilization of KLF10, a tumor suppressor, relies on thr93 phosphorylation and isomerase association. Biochim. Biophys. Acta, 2013, 1833(12), 3035-3045.
[http://dx.doi.org/10.1016/j.bbamcr.2013.08.010] [PMID: 23994618]
[20]
Lucchetti, C.; Caligiuri, I.; Toffoli, G.; Giordano, A.; Rizzolio, F. The prolyl isomerase Pin1 acts synergistically with CDK2 to regulate the basal activity of estrogen receptor α in breast cancer. PLoS One, 2013, 8(2)e55355
[http://dx.doi.org/10.1371/journal.pone.0055355] [PMID: 23390529]
[21]
Keune, W.J.; Jones, D.R.; Bultsma, Y.; Sommer, L.; Zhou, X.Z.; Lu, K.P.; Divecha, N. Regulation of phosphatidylinositol-5-phosphate signaling by Pin1 determines sensitivity to oxidative stress. Sci. Signal., 2012, 5(252), ra86.
[http://dx.doi.org/10.1126/scisignal.2003223] [PMID: 23193159]
[22]
Khanal, P.; Yun, H.J.; Lim, S.C.; Ahn, S.G.; Yoon, H.E.; Kang, K.W.; Hong, R.; Choi, H.S. Proyl isomerase Pin1 facilitates ubiquitin-mediated degradation of cyclin-dependent kinase 10 to induce tamoxifen resistance in breast cancer cells. Oncogene, 2012, 31(34), 3845-3856.
[http://dx.doi.org/10.1038/onc.2011.548] [PMID: 22158035]
[23]
Min, S.H.; Lau, A.W.; Lee, T.H.; Inuzuka, H.; Wei, S.; Huang, P.; Shaik, S.; Lee, D.Y.; Finn, G.; Balastik, M.; Chen, C.H.; Luo, M.; Tron, A.E.; Decaprio, J.A.; Zhou, X.Z.; Wei, W.; Lu, K.P. Negative regulation of the stability and tumor suppressor function of Fbw7 by the Pin1 prolyl isomerase. Mol. Cell, 2012, 46(6), 771-783.
[http://dx.doi.org/10.1016/j.molcel.2012.04.012] [PMID: 22608923]
[24]
Nagel, R.; Semenova, E.A.; Berns, A. Drugging the addict: non-oncogene addiction as a target for cancer therapy. EMBO Rep., 2016, 17(11), 1516-1531.
[http://dx.doi.org/10.15252/embr.201643030] [PMID: 27702988]
[25]
Nakatsu, Y.; Iwashita, M.; Sakoda, H.; Ono, H.; Nagata, K.; Matsunaga, Y.; Fukushima, T.; Fujishiro, M.; Kushiyama, A.; Kamata, H.; Takahashi, S.; Katagiri, H.; Honda, H.; Kiyonari, H.; Uchida, T.; Asano, T. Prolyl isomerase Pin1 negatively regulates AMP-activated protein kinase (AMPK) by associating with the CBS domain in the γ subunit. J. Biol. Chem., 2015, 290(40), 24255-24266.
[http://dx.doi.org/10.1074/jbc.M115.658559] [PMID: 26276391]
[26]
Nicole Tsang, Y.H.; Wu, X.W.; Lim, J.S.; Wee Ong, C.; Salto-Tellez, M.; Ito, K.; Ito, Y.; Chen, L.F. Prolyl isomerase Pin1 downregulates tumor suppressor RUNX3 in breast cancer. Oncogene, 2013, 32(12), 1488-1496.
[http://dx.doi.org/10.1038/onc.2012.178] [PMID: 22580604]
[27]
Penela, P.; Rivas, V.; Salcedo, A.; Mayor, F. Jr G protein-coupled receptor kinase 2 (GRK2) modulation and cell cycle progression. Proc. Natl. Acad. Sci. USA, 2010, 107(3), 1118-1123.
[http://dx.doi.org/10.1073/pnas.0905778107] [PMID: 20080565]
[28]
Ueberham, U.; Rohn, S.; Ueberham, E.; Wodischeck, S.; Hilbrich, I.; Holzer, M.; Brückner, M.K.; Gruschka, H.; Arendt, T. Pin1 promotes degradation of Smad proteins and their interaction with phosphorylated tau in Alzheimer’s disease. Neuropathol. Appl. Neurobiol., 2014, 40(7), 815-832.
[http://dx.doi.org/10.1111/nan.12163] [PMID: 24964035]
[29]
Moretto-Zita, M.; Jin, H.; Shen, Z.; Zhao, T.; Briggs, S.P.; Xu, Y. Phosphorylation stabilizes Nanog by promoting its interaction with Pin1. Proc. Natl. Acad. Sci. USA, 2010, 107(30), 13312-13317.
[http://dx.doi.org/10.1073/pnas.1005847107] [PMID: 20622153]
[30]
Sakuma, Y.; Nishikiori, H.; Hirai, S.; Yamaguchi, M.; Yamada, G.; Watanabe, A.; Hasegawa, T.; Kojima, T.; Niki, T.; Takahashi, H. Prolyl isomerase Pin1 promotes survival in EGFR-mutant lung adenocarcinoma cells with an epithelial-mesenchymal transition phenotype. Lab. Invest., 2016, 96(4), 391-398.
[http://dx.doi.org/10.1038/labinvest.2015.155] [PMID: 26752745]
[31]
Ryo, A.; Liou, Y-C.; Wulf, G.; Nakamura, M.; Lee, S.W.; Lu, K.P. PIN1 is an E2F target gene essential for Neu/Ras-induced transformation of mammary epithelial cells. Mol. Cell. Biol., 2002, 22(15), 5281-5295.
[http://dx.doi.org/10.1128/MCB.22.15.5281-5295.2002] [PMID: 12101225]
[32]
Hennig, L.; Christner, C.; Kipping, M.; Schelbert, B.; Rücknagel, K.P.; Grabley, S.; Küllertz, G.; Fischer, G. Selective inactivation of parvulin-like peptidyl-prolyl cis/trans isomerases by juglone. Biochemistry, 1998, 37(17), 5953-5960.
[http://dx.doi.org/10.1021/bi973162p] [PMID: 9558330]
[33]
Uchida, T.; Takamiya, M.; Takahashi, M.; Miyashita, H.; Ikeda, H.; Terada, T.; Matsuo, Y.; Shirouzu, M.; Yokoyama, S.; Fujimori, F.; Hunter, T. Pin1 and Par14 peptidyl prolyl isomerase inhibitors block cell proliferation. Chem. Biol., 2003, 10(1), 15-24.
[http://dx.doi.org/10.1016/S1074-5521(02)00310-1] [PMID: 12573694]
[34]
Li, X.; Li, L.; Zhou, Q.; Zhang, N.; Zhang, S.; Zhao, R.; Liu, D.; Jing, Y.; Zhao, L. Synthesis of the novel elemonic acid derivatives as Pin1 inhibitors. Bioorg. Med. Chem. Lett., 2014, 24(24), 5612-5615.
[http://dx.doi.org/10.1016/j.bmcl.2014.10.087] [PMID: 25466185]
[35]
Urusova, D.V.; Shim, J.H.; Kim, D.J.; Jung, S.K.; Zykova, T.A.; Carper, A.; Bode, A.M.; Dong, Z. Epigallocatechin-gallate suppresses tumorigenesis by directly targeting Pin1. Cancer Prev. Res. (Phila.), 2011, 4(9), 1366-1377.
[http://dx.doi.org/10.1158/1940-6207.CAPR-11-0301] [PMID: 21750208]
[36]
Gra; Janczyk, W.; Sperl, B.; Elumalai, N.; Kozany, C.; Hausch, F.; Holak, T.A.; Berg, T. Selective targeting of disease-relevant protein binding domains by O-phosphorylated natural product derivatives. ACS Chem. Biol., 2011, 6, 1008-1014.
[http://dx.doi.org/10.1021/cb2001796]
[37]
Marsolier, J.; Perichon, M.; DeBarry, J.D.; Villoutreix, B.O.; Chluba, J.; Lopez, T.; Garrido, C.; Zhou, X.Z.; Lu, K.P.; Fritsch, L.; Ait-Si-Ali, S.; Mhadhbi, M.; Medjkane, S.; Weitzman, J.B. Theileria parasites secrete a prolyl isomerase to maintain host leukocyte transformation. Nature, 2015, 520(7547), 378-382.
[http://dx.doi.org/10.1038/nature14044] [PMID: 25624101]
[38]
Wildemann, D.; Erdmann, F.; Alvarez, B.H.; Stoller, G.; Zhou, X.Z.; Fanghänel, J.; Schutkowski, M.; Lu, K.P.; Fischer, G. Nanomolar inhibitors of the peptidyl prolyl cis/trans isomerase Pin1 from combinatorial peptide libraries. J. Med. Chem., 2006, 49(7), 2147-2150.
[http://dx.doi.org/10.1021/jm060036n] [PMID: 16570909]
[39]
Zhang, Y.; Daum, S.; Wildemann, D.; Zhou, X.Z.; Verdecia, M.A.; Bowman, M.E.; Lücke, C.; Hunter, T.; Lu, K.P.; Fischer, G.; Noel, J.P. Structural basis for high-affinity peptide inhibition of human Pin1. ACS Chem. Biol., 2007, 2(5), 320-328.
[http://dx.doi.org/10.1021/cb7000044] [PMID: 17518432]
[40]
Wei, S.; Kozono, S.; Kats, L.; Nechama, M.; Li, W.; Guarnerio, J.; Luo, M.; You, M.H.; Yao, Y.; Kondo, A.; Hu, H.; Bozkurt, G.; Moerke, N.J.; Cao, S.; Reschke, M.; Chen, C.H.; Rego, E.M.; Lo-Coco, F.; Cantley, L.C.; Lee, T.H.; Wu, H.; Zhang, Y.; Pandolfi, P.P.; Zhou, X.Z.; Lu, K.P. Active Pin1 is a key target of all-trans retinoic acid in acute promyelocytic leukemia and breast cancer. Nat. Med., 2015, 21(5), 457-466.
[http://dx.doi.org/10.1038/nm.3839] [PMID: 25849135]
[41]
Verdecia, M.A.; Bowman, M.E.; Lu, K.P.; Hunter, T.; Noel, J.P. Structural basis for phosphoserine-proline recognition by group IV WW domains. Nat. Struct. Biol., 2000, 7(8), 639-643.
[http://dx.doi.org/10.1038/77929] [PMID: 10932246]
[42]
Moore, J.D.; Potter, A. Pin1 inhibitors: Pitfalls, progress and cellular pharmacology. Bioorg. Med. Chem. Lett., 2013, 23(15), 4283-4291.
[http://dx.doi.org/10.1016/j.bmcl.2013.05.088] [PMID: 23796453]
[43]
Li, K.; Li, L.; Wang, S.; Li, X.; Ma, T.; Liu, D.; Jing, Y.; Zhao, L. Design and synthesis of novel 2-substituted 11-keto-boswellic acid heterocyclic derivatives as anti-prostate cancer agents with Pin1 inhibition ability. Eur. J. Med. Chem., 2017, 126, 910-919.
[http://dx.doi.org/10.1016/j.ejmech.2016.09.089] [PMID: 27997878]
[44]
Pilon, A.C.; Valli, M.; Dametto, A.C.; Pinto, M.E.F.; Freire, R.T.; Castro-Gamboa, I.; Andricopulo, A.D.; Bolzani, V.S. NuBBEDB: an updated database to uncover chemical and biological information from Brazilian biodiversity. Sci. Rep., 2017, 7(1), 7215.
[http://dx.doi.org/10.1038/s41598-017-07451-x] [PMID: 28775335]
[45]
Krieger, E.; Nabuurs, S.B.; Vriend, G. Homology modeling. Methods Biochem. Anal., 2003, 44, 509-523.
[PMID: 12647402]
[46]
Fiser, A.; Šali, A. Modeller: generation and refinement of homology-based protein structure models. Methods Enzymol., 2003, 374, 461-491.
[http://dx.doi.org/10.1016/S0076-6879(03)74020-8] [PMID: 14696385]
[47]
Case, D.A.; Cheatham, T.E., III; Darden, T.; Gohlke, H.; Luo, R.; Merz, K.M., Jr; Onufriev, A.; Simmerling, C.; Wang, B.; Woods, R.J. The Amber biomolecular simulation programs. J. Comput. Chem., 2005, 26(16), 1668-1688.
[http://dx.doi.org/10.1002/jcc.20290] [PMID: 16200636]
[48]
Wiberg, K.B. A Scheme for Strain Energy Minimization. J. Am. Chem. Soc., 1965, 87, 1070-1078.
[http://dx.doi.org/10.1021/ja01083a024]
[49]
Hestenes, M.R.; Stiefel, E. Methods of conjugate gradients for solving linear systems. J. Res. Natl. Bur. Stand (1934) 1952. 49, 409
[50]
Bas, D.C.; Rogers, D.M.; Jensen, J.H. Very fast prediction and rationalization of pKa values for protein-ligand complexes. Proteins, 2008, 73(3), 765-783.
[http://dx.doi.org/10.1002/prot.22102] [PMID: 18498103]
[51]
Dolinsky, T.J.; Nielsen, J.E.; McCammon, J.A.; Baker, N.A. PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res.,, 2004. 32(Web Server issue)W665-7
[http://dx.doi.org/10.1093/nar/gkh381] [PMID: 15215472]
[52]
Bolzani, V. da S.; Valli, M.; Pivatto, M.; Viegas, C. Natural products from Brazilian biodiversity as a source of new models for medicinal chemistry. Pure Appl. Chem., 2012, 84, 1837-1846.
[http://dx.doi.org/10.1351/PAC-CON-12-01-11]
[53]
ChenAxon Ltda MarvinSketch. , 2014.
[54]
Sunseri, J.; Koes, D.R. Pharmit: interactive exploration of chemical space. Nucleic Acids Res., 2016, 44(W1)W442-8
[http://dx.doi.org/10.1093/nar/gkw287] [PMID: 27095195]
[55]
Thomsen, R.; Christensen, M.H. MolDock: a new technique for high-accuracy molecular docking. J. Med. Chem., 2006, 49(11), 3315-3321.
[http://dx.doi.org/10.1021/jm051197e] [PMID: 16722650]
[56]
Salentin, S.; Schreiber, S.; Haupt, V.J.; Adasme, M.F.; Schroeder, M. PLIP: fully automated protein-ligand interaction profiler. Nucleic Acids Res., 2015, 43(W1)W443-7
[http://dx.doi.org/10.1093/nar/gkv315] [PMID: 25873628]
[57]
ChenAxon Ltda Marvin 2014.
[58]
Lipinski, C.A.; Dominy, B.W.; Feeney, P.J. drug delivery reviews Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv. Drug Deliv. Rev., 1997, 23, 3-25.
[http://dx.doi.org/10.1016/S0169-409X(96)00423-1]
[59]
Veber, D.F.; Johnson, S.R.; Cheng, H-Y.Y.; Smith, B.R.; Ward, K.W.; Kopple, K.D. Molecular properties that influence the oral bioavailability of drug candidates. J. Med. Chem., 2002, 45(12), 2615-2623.
[http://dx.doi.org/10.1021/jm020017n] [PMID: 12036371]
[60]
Muegge, I. Selection criteria for drug-like compounds. Med. Res. Rev., 2003, 23(3), 302-321.
[http://dx.doi.org/10.1002/med.10041] [PMID: 12647312]
[61]
Wang, J.; Cieplak, P.; Kollman, P.A. How Well Does a Restrained Electrostatic Potential (RESP) Model Perform in Calculating Conformational Energies of Organic and Biological Molecules? J. Comput. Chem., 2000, 21, 1049-1074.
[http://dx.doi.org/10.1002/1096-987X(200009)21:12<1049:AID-JCC3>3.0.CO;2-F]
[62]
Frisch, M.J. Gaussian 09 Gaussian, Inc. Wallingford CT 2009, 2-3.
[63]
Echenique, P.; Alonso, J.L. A mathematical and computational review of Hartree-Fock SCF methods in quantum chemistry. Mol. Phys., 2007, 105, 3057-3098.
[http://dx.doi.org/10.1080/00268970701757875]
[64]
Ditchfield, R.; Hehre, W.J.; Pople, J.A. Self‐Consistent Molecular‐Orbital Methods. IX. An Extended Gaussian‐Type Basis for Molecular‐Orbital Studies of Organic Molecules. J. Chem. Phys., 2004, 54, 724-728.
[http://dx.doi.org/10.1063/1.1674902]
[65]
Mark, P.; Nilsson, L. Structure and Dynamics of the TIP3P, SPC, and SPC/E Water Models at 298 K. J. Phys. Chem. A, 2001, 105, 9954-9960.
[http://dx.doi.org/10.1021/jp003020w]
[66]
Lzaguirre, J.A.; Catarello, D.P.; Wozniak, J.M.; Skeel, R.D. Langevin stabilization of molecular dynamics. J. Chem. Phys., 2001, 114, 2090-2098.
[http://dx.doi.org/10.1063/1.1332996]
[67]
Kräutler, V.; Van Gunsteren, W.F.; Hünenberger, P.H. A fast SHAKE algorithm to solve distance constraint equations for small molecules in molecular dynamics simulations. J. Comput. Chem., 2001, 22, 501-508.
[http://dx.doi.org/10.1002/1096-987X(20010415)22:5<501:AID-JCC1021>3.0.CO;2-V]
[68]
Genheden, S.; Ryde, U. The MM/PBSA and MM/GBSA methods to estimate ligand-binding affinities. Expert Opin. Drug Discov., 2015, 10(5), 449-461.
[http://dx.doi.org/10.1517/17460441.2015.1032936] [PMID: 25835573]
[69]
Hou, T.; Wang, J.; Li, Y.; Wang, W. Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations. J. Chem. Inf. Model., 2011, 51(1), 69-82.
[http://dx.doi.org/10.1021/ci100275a] [PMID: 21117705]
[70]
Naïm, M.; Bhat, S.; Rankin, K.N.; Dennis, S.; Chowdhury, S.F.; Siddiqi, I.; Drabik, P.; Sulea, T.; Bayly, C.I.; Jakalian, A.; Purisima, E.O. Solvated interaction energy (SIE) for scoring protein-ligand binding affinities. 1. Exploring the parameter space. J. Chem. Inf. Model., 2007, 47(1), 122-133.
[http://dx.doi.org/10.1021/ci600406v] [PMID: 17238257]
[71]
Cui, Q.; Sulea, T.; Schrag, J.D.; Munger, C.; Hung, M.N.; Naïm, M.; Cygler, M.; Purisima, E.O. Molecular dynamics-solvated interaction energy studies of protein-protein interactions: the MP1-p14 scaffolding complex. J. Mol. Biol., 2008, 379(4), 787-802.
[http://dx.doi.org/10.1016/j.jmb.2008.04.035] [PMID: 18479705]
[72]
Aqvist, J.; Marelius, J. The linear interaction energy method for predicting ligand binding free energies. Comb. Chem. High Throughput Screen., 2001, 4(8), 613-626.
[http://dx.doi.org/10.2174/1386207013330661] [PMID: 11812258]
[73]
da Costa, K.S.; Leal, E.; dos Santos, A.M.; Lima e Lima, A.H.; Alves, C.N.; Lameira, J.; Lameira, J. Structural analysis of viral infectivity factor of HIV type 1 and its interaction with A3G, EloC and EloB. PLoS One, 2014, 9(2)e89116
[http://dx.doi.org/10.1371/journal.pone.0089116] [PMID: 24586532]
[74]
Lima, A.H.; Dos Santos, A.M.; Alves, C.N.; Lameira, J. Computed insight into a peptide inhibitor preventing the induced fit mechanism of MurA enzyme from Pseudomonas aeruginosa. Chem. Biol. Drug Des., 2017, 89(4), 599-607.
[http://dx.doi.org/10.1111/cbdd.12882] [PMID: 27736019]
[75]
Guo, C.; Hou, X.; Dong, L.; Dagostino, E.; Greasley, S.; Ferre, R.; Marakovits, J.; Johnson, M.C.; Matthews, D.; Mroczkowski, B.; Parge, H.; Vanarsdale, T.; Popoff, I.; Piraino, J.; Margosiak, S.; Thomson, J.; Los, G.; Murray, B.W. Structure-based design of novel human Pin1 inhibitors (I). Bioorg. Med. Chem. Lett., 2009, 19(19), 5613-5616.
[http://dx.doi.org/10.1016/j.bmcl.2009.08.034] [PMID: 19729306]
[76]
Potter, A.J.; Ray, S.; Gueritz, L.; Nunns, C.L.; Bryant, C.J.; Scrace, S.F.; Matassova, N.; Baker, L.; Dokurno, P.; Robinson, D.A.; Surgenor, A.E.; Davis, B.; Murray, J.B.; Richardson, C.M.; Moore, J.D. Structure-guided design of α-amino acid-derived Pin1 inhibitors. Bioorg. Med. Chem. Lett., 2010, 20(2), 586-590.
[http://dx.doi.org/10.1016/j.bmcl.2009.11.090] [PMID: 19969456]
[77]
Zhou, X.Z.; Lu, P.J.; Wulf, G.; Lu, K.P. Phosphorylation-dependent prolyl isomerization: a novel signaling regulatory mechanism. Cell. Mol. Life Sci., 1999, 56(9-10), 788-806.
[http://dx.doi.org/10.1007/s000180050026] [PMID: 11212339]
[78]
Alzohairy, M.A. Therapeutics Role of Azadirachta indica (Neem) and Their Active Constituents in Diseases Prevention and Treatment. Evidence-Based Complement. Altern. Med., 2016, 2016, 1-11.
[79]
Hao, F.; Kumar, S.; Yadav, N.; Chandra, D. Neem components as potential agents for cancer prevention and treatment. Biochim. Biophys. Acta, 2014, 1846(1), 247-257.
[PMID: 25016141]
[80]
Kikuchi, T.; Ishii, K.; Noto, T.; Takahashi, A.; Tabata, K.; Suzuki, T.; Akihisa, T. Cytotoxic and apoptosis-inducing activities of limonoids from the seeds of Azadirachta indica (neem). J. Nat. Prod., 2011, 74(4), 866-870.
[http://dx.doi.org/10.1021/np100783k] [PMID: 21381696]
[81]
Nagini, S. Neem Limonoids as Anticancer Agents: Modulation of Cancer Hallmarks and Oncogenic Signaling. Enzymes, 2014, 36, 131-147.
[http://dx.doi.org/10.1016/B978-0-12-802215-3.00007-0] [PMID: 27102702]
[82]
Bayer, E.; Goettsch, S.; Mueller, J.W.; Griewel, B.; Guiberman, E.; Mayr, L.M.; Bayer, P. Structural Analysis of the Mitotic Regulator h Pin1 in Solution. J. Biol. Chem., 2003, 278, 26183-26193.
[http://dx.doi.org/10.1074/jbc.M300721200] [PMID: 12721297]
[83]
Lee, T.H.; Chen, C.H.; Suizu, F.; Huang, P.; Schiene-Fischer, C.; Daum, S.; Zhang, Y.J.; Goate, A.; Chen, R.H.; Zhou, X.Z.; Lu, K.P. Death-associated protein kinase 1 phosphorylates Pin1 and inhibits its prolyl isomerase activity and cellular function. Mol. Cell, 2011, 42(2), 147-159.
[http://dx.doi.org/10.1016/j.molcel.2011.03.005] [PMID: 21497122]
[84]
Dunyak, B.M.; Gestwicki, J.E. Peptidyl-Proline Isomerases (PPIases): Targets for Natural Products and Natural Product-Inspired Compounds. J. Med. Chem., 2016, 59(21), 9622-9644.
[http://dx.doi.org/10.1021/acs.jmedchem.6b00411] [PMID: 27409354]
[85]
Campaner, E.; Rustighi, A.; Zannini, A.; Cristiani, A.; Piazza, S.; Ciani, Y.; Kalid, O.; Golan, G.; Baloglu, E.; Shacham, S.; Valsasina, B.; Cucchi, U.; Pippione, A.C.; Lolli, M.L.; Giabbai, B.; Storici, P.; Carloni, P.; Rossetti, G.; Benvenuti, F.; Bello, E.; D’Incalci, M.; Cappuzzello, E.; Rosato, A.; Del Sal, G. A covalent PIN1 inhibitor selectively targets cancer cells by a dual mechanism of action. Nat. Commun., 2017, 8, 15772.
[http://dx.doi.org/10.1038/ncomms15772] [PMID: 28598431]
[86]
Connolly, R.M.; Nguyen, N.K.; Sukumar, S. Molecular pathways: current role and future directions of the retinoic acid pathway in cancer prevention and treatment. Clin. Cancer Res., 2013, 19(7), 1651-1659.
[http://dx.doi.org/10.1158/1078-0432.CCR-12-3175] [PMID: 23322901]
[87]
Schuster, D.; Laggner, C.; Langer, T. Why drugs fail--a study on side effects in new chemical entities. Curr. Pharm. Des., 2005, 11(27), 3545-3559.
[http://dx.doi.org/10.2174/138161205774414510] [PMID: 16248807]

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