New tricks for an Old natural product: Discovery of highly potent evodiamine derivatives as novel antitumor agents by systemic structure-activity relationship analysis and biological evaluations

Journal of Medicinal Chemistry

Volumn 55, Issue 17, 2012, Pages 7593-7613

  Dong, Guoqiang ^a   Wang, Shengzheng ^a   Miao, Zhenyuan ^a   Yao, Jianzhong ^a   Zhang, Yongqiang ^a   Guo, Zizhao ^a   Zhang, Wannian ^a   Sheng, Chunquan ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

1 METHYLEVODIAMINE; 10 HYDROXYEVODIAMINE; 10 HYDROXYL EVODIAMINE; 12 CHLOROEVODIAMINE; 3 AMINO 10 HYDROXYEVODIAMINE; 3 AMINO 10 HYDROXYL EVODIAMINE; 3 AMINOEVODIAMINE; 3 CHLOROEVODIAMINE; 3 FLUORO 10 HYDROXYEVODIAMINE; 3 FLUOROEVODIAMINE; 3 HYDROXYEVODIAMINE; 4 HYDROXYEVODIAMINE; ANTINEOPLASTIC AGENT; DNA TOPOISOMERASE; DNA TOPOISOMERASE (ATP HYDROLYSING); EVODIA FRUIT; EVODIAMINE; HYDROXYL GROUP; NATURAL PRODUCT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CONTROLLED STUDY; CYTOTOXICITY; DNA BINDING; DNA CLEAVAGE; DRUG EFFICACY; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME INHIBITION; HUMAN; HUMAN CELL; HYDROGEN BOND; MALE; MOLECULAR DOCKING; MOUSE; NONHUMAN; STRUCTURE ACTIVITY RELATION;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; BIOLOGICAL AGENTS; CELL LINE, TUMOR; DRUG SCREENING ASSAYS, ANTITUMOR; EVODIA; HUMANS; QUINAZOLINES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84866328968     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm300605m     Document Type: Article

References (83)

1. Newman, D. J.; Cragg, G. M.; Snader, K. M. Natural products as sources of new drugs over the period 1981-2002 J. Nat. Prod. 2003, 66, 1022-1037 (Pubitemid 36909859)
2. Newman, D. J.; Cragg, G. M. Natural products as sources of new drugs over the last 25 years J. Nat. Prod. 2007, 70, 461-477 (Pubitemid 46595760)
3. Balamurugan, R.; Dekker, F. J.; Waldmann, H. Design of compound libraries based on natural product scaffolds and protein structure similarity clustering (PSSC) Mol. Biosyst. 2005, 1, 36-45 (Pubitemid 43355013)
4. Oberlies, N. H.; Kroll, D. J. Camptothecin and taxol: historic achievements in natural products research J. Nat. Prod. 2004, 67, 129-135 (Pubitemid 38282896)
5. Wall, M. E.; Wani, M. C.; Cook, C. E.; Palmer, K. H.; McPhail, A. T.; Sim, G. A. The Isolation and Structure of Camptothecin, a Novel Alkaloidal Leukemia and Tumor Inhibitor from Camptotheca Acuminata J. Am. Chem. Soc. 1966, 88, 3888-3890
6. Hsiang, Y. H.; Hertzberg, R.; Hecht, S.; Liu, L. F. Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I J. Biol. Chem. 1985, 260, 14873-14878 (Pubitemid 16211028)
7. Kingsbury, W. D.; Boehm, J. C.; Jakas, D. R.; Holden, K. G.; Hecht, S. M.; Gallagher, G.; Caranfa, M. J.; McCabe, F. L.; Faucette, L. F.; Johnson, R. K. Synthesis of water-soluble (aminoalkyl)camptothecin analogues: inhibition of topoisomerase I and antitumor activity J. Med. Chem. 1991, 34, 98-107
8. Garcia-Carbonero, R.; Supko, J. G. Current perspectives on the clinical experience, pharmacology, and continued development of the camptothecins Clin. Cancer Res. 2002, 8, 641-661 (Pubitemid 34742090)
9. Giovanella, B. C.; Stehlin, J. S.; Hinz, H. R.; Kozielski, A. J.; Harris, N. J.; Vardeman, D. M. Preclinical evaluation of the anticancer activity and toxicity of 9-nitro-20(S)-camptothecin (Rubitecan) Int. J. Oncol. 2002, 20, 81-88
10. Eckhardt, S. G.; Baker, S. D.; Eckardt, J. R.; Burke, T. G.; Warner, D. L.; Kuhn, J. G.; Rodriguez, G.; Fields, S.; Thurman, A.; Smith, L.; Rothenberg, M. L.; White, L.; Wissel, P.; Kunka, R.; DePee, S.; Littlefield, D.; Burris, H. A.; Von Hoff, D. D.; Rowinsky, E. K.; Phase, I and pharmacokinetic study of GI147211, a water-soluble camptothecin analogue, administered for five consecutive days every three weeks Clin. Cancer Res. 1998, 4, 595-604 (Pubitemid 28193557)
11. Minami, H.; Fujii, H.; Igarashi, T.; Itoh, K.; Tamanoi, K.; Oguma, T.; Sasaki, Y. Phase I and pharmacological study of a new camptothecin derivative, exatecan mesylate (DX-8951f), infused over 30 minutes every three weeks Clin. Cancer Res. 2001, 7, 3056-3064 (Pubitemid 32963824)
12. Liao, J. F.; Chen, C. F.; Chow, S. Y. Pharmacological studies of Chinese herbs. (9) Pharmacological effects of Evodiae fructus J. Formosan Med. Assoc. 1981, 80, 30-38
13. Yu, X.; Wu, D. Z.; Yuan, J. Y.; Zhang, R. R.; Hu, Z. B. Gastroprotective effect of fructus evodiae water extract on ethanol-induced gastric lesions in rats Am. J. Chin. Med. 2006, 34, 1027-1035 (Pubitemid 44921247)
14. Chiou, W. F.; Sung, Y. J.; Liao, J. F.; Shum, A. Y.; Chen, C. F. Inhibitory effect of dehydroevodiamine and evodiamine on nitric oxide production in cultured murine macrophages J. Nat. Prod. 1997, 60, 708-711 (Pubitemid 27318419)
15. Ko, H. C.; Wang, Y. H.; Liou, K. T.; Chen, C. M.; Chen, C. H.; Wang, W. Y.; Chang, S.; Hou, Y. C.; Chen, K. T.; Chen, C. F.; Shen, Y. C. Anti-inflammatory effects and mechanisms of the ethanol extract of Evodia rutaecarpa and its bioactive components on neutrophils and microglial cells Eur. J. Pharmacol. 2007, 555, 211-217 (Pubitemid 46048800)
16. Liu, Y. N.; Pan, S. L.; Liao, C. H.; Huang, D. Y.; Guh, J. H.; Peng, C. Y.; Chang, Y. L.; Teng, C. M. Evodiamine represses hypoxia-induced inflammatory proteins expression and hypoxia-inducible factor 1alpha accumulation in RAW264.7 Shock 2009, 32, 263-269
17. Kobayashi, Y.; Nakano, Y.; Kizaki, M.; Hoshikuma, K.; Yokoo, Y.; Kamiya, T. Capsaicin-like anti-obese activities of evodiamine from fruits of Evodia rutaecarpa, a vanilloid receptor agonist Planta Med. 2001, 67, 628-633 (Pubitemid 32929573)
18. Bak, E. J.; Park, H. G.; Kim, J. M.; Yoo, Y. J.; Cha, J. H. Inhibitory effect of evodiamine alone and in combination with rosiglitazone on in vitro adipocyte differentiation and in vivo obesity related to diabetes Int. J. Obes. 2010, 34, 250-260
19. Wang, T.; Wang, Y.; Kontani, Y.; Kobayashi, Y.; Sato, Y.; Mori, N.; Yamashita, H. Evodiamine improves diet-induced obesity in a uncoupling protein-1-independent manner: involvement of antiadipogenic mechanism and extracellularly regulated kinase/mitogen-activated protein kinase signaling Endocrinology 2008, 149, 358-366
20. Wang, T.; Wang, Y.; Yamashita, H. Evodiamine inhibits adipogenesis via the EGFR-PKCalpha-ERK signaling pathway FEBS Lett. 2009, 583, 3655-3659
21. Jiang, J.; Hu, C. Evodiamine: a novel anti-cancer alkaloid from Evodia rutaecarpa Molecules 2009, 14, 1852-1859
22. Fei, X. F.; Wang, B. X.; Li, T. J.; Tashiro, S.; Minami, M.; Xing, D. J.; Ikejima, T. Evodiamine, a constituent of Evodiae fructus, induces anti-proliferating effects in tumor cells Cancer Sci. 2003, 94, 92-98 (Pubitemid 36575865)
23. Kan, S. F.; Huang, W. J.; Lin, L. C.; Wang, P. S. Inhibitory effects of evodiamine on the growth of human prostate cancer cell line LNCaP Int. J. Cancer 2004, 110, 641-651 (Pubitemid 38746021)
24. Liao, C. H.; Pan, S. L.; Guh, J. H.; Chang, Y. L.; Pai, H. C.; Lin, C. H.; Teng, C. M. Antitumor mechanism of evodiamine, a constituent from Chinese herb Evodiae fructus, in human multiple-drug resistant breast cancer NCI/ADR-RES cells in vitro and in vivo Carcinogenesis 2005, 26, 968-975
25. Yang, Z. G.; Chen, A. Q.; Liu, B. Antiproliferation and apoptosis induced by evodiamine in human colorectal carcinoma cells (COLO-205) Chem. Biodivers. 2009, 6, 924-933
26. Kan, S. F.; Yu, C. H.; Pu, H. F.; Hsu, J. M.; Chen, M. J.; Wang, P. S. Anti-proliferative effects of evodiamine on human prostate cancer cell lines DU145 and PC3 J. Cell. Biochem. 2007, 101, 44-56 (Pubitemid 46652571)
27. Chen, M. C.; Yu, C. H.; Wang, S. W.; Pu, H. F.; Kan, S. F.; Lin, L. C.; Chi, C. W.; Ho, L. L.; Lee, C. H.; Wang, P. S. Anti-proliferative effects of evodiamine on human thyroid cancer cell line ARO J. Cell. Biochem. 2010, 110, 1495-1503
28. Zhang, C.; Fan, X.; Xu, X.; Yang, X.; Wang, X.; Liang, H. P. Evodiamine induces caspase-dependent apoptosis and S phase arrest in human colon lovo cells Anticancer Drugs 2010, 21, 766-776
29. Lee, T. J.; Kim, E. J.; Kim, S.; Jung, E. M.; Park, J. W.; Jeong, S. H.; Park, S. E.; Yoo, Y. H.; Kwon, T. K. Caspase-dependent and caspase-independent apoptosis induced by evodiamine in human leukemic U937 cells Mol. Cancer Ther. 2006, 5, 2398-2407 (Pubitemid 44530477)
30. Huang, H.; Zhang, Y.; Liu, X.; Li, Z.; Xu, W.; He, S.; Huang, Y.; Zhang, H. Acid sphingomyelinase contributes to evodiamine-induced apoptosis in human gastric cancer SGC-7901 cells DNA Cell Biol. 2011, 30, 407-412
31. Wang, C.; Li, S.; Wang, M. W. Evodiamine-induced human melanoma A375-S2 cell death was mediated by PI3K/Akt/caspase and Fas-L/NF-kappaB signaling pathways and augmented by ubiquitin-proteasome inhibition Toxicol. in Vitro 2010, 24, 898-904
32. Ogasawara, M.; Matsubara, T.; Suzuki, H. Inhibitory effects of evodiamine on in vitro invasion and experimental lung metastasis of murine colon cancer cells Biol. Pharm. Bull. 2001, 24, 917-920 (Pubitemid 32750318)
33. Ogasawara, M.; Matsubara, T.; Suzuki, H. Screening of natural compounds for inhibitory activity on colon cancer cell migration Biol. Pharm. Bull. 2001, 24, 720-723 (Pubitemid 32586670)
34. Yang, X. W.; Zhang, H.; Li, M.; Du, L. J.; Yang, Z.; Xiao, S. Y. Studies on the alkaloid constituents of Evodia rutaecarpa (Juss) Benth var. bodinaieri (Dode) Huang and their acute toxicity in mice J. Asian Nat. Prod. Res. 2006, 8, 697-703 (Pubitemid 44915751)
35. Lipinski, C. A.; Lombardo, F.; Dominy, B. W.; Feeney, P. J. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings Adv. Drug Deliv. Rev. 2001, 46, 3-26 (Pubitemid 33653411)
36. Hann, M. M.; Oprea, T. I. Pursuing the leadlikeness concept in pharmaceutical research Curr. Opin. Chem. Biol. 2004, 8, 255-263 (Pubitemid 38759400)
37. Oprea, T. I.; Davis, A. M.; Teague, S. J.; Leeson, P. D. Is there a difference between leads and drugs? A historical perspective J. Chem. Inf. Comput. Sci. 2001, 41, 1308-1315
38. Manly, C. J.; Chandrasekhar, J.; Ochterski, J. W.; Hammer, J. D.; Warfield, B. B. Strategies and tactics for optimizing the Hit-to-Lead process and beyond-a computational chemistry perspective Drug Discovery Today 2008, 13, 99-109
39. Baruah, B.; Dasu, K.; Vaitilingam, B.; Mamnoor, P.; Venkata, P. P.; Rajagopal, S.; Yeleswarapu, K. R. Synthesis and cytotoxic activity of novel quinazolino-beta-carboline-5-one derivatives Bioorg. Med. Chem. 2004, 12, 1991-1994 (Pubitemid 38471692)
40. Chen, Z.; Hu, G.; Li, D.; Chen, J.; Li, Y.; Zhou, H.; Xie, Y. Synthesis and vasodilator effects of rutaecarpine analogues which might be involved transient receptor potential vanilloid subfamily, member 1 (TRPV1) Bioorg. Med. Chem. 2009, 17, 2351-2359
41. Decker, M. Novel inhibitors of acetyl- and butyrylcholinesterase derived from the alkaloids dehydroevodiamine and rutaecarpine Eur. J. Med. Chem. 2005, 40, 305-313 (Pubitemid 40255773)
42. Hong, Y. H.; Lee, W. J.; Lee, S. H.; Son, J. K.; Kim, H. L.; Nam, J. M.; Kwon, Y.; Jahng, Y. Synthesis and biological properties of benzo-annulated rutaecarpines Biol. Pharm. Bull. 2010, 33, 1704-1709
43. Wang, B.; Mai, Y. C.; Li, Y.; Hou, J. Q.; Huang, S. L.; Ou, T. M.; Tan, J. H.; An, L. K.; Li, D.; Gu, L. Q.; Huang, Z. S. Synthesis and evaluation of novel rutaecarpine derivatives and related alkaloids derivatives as selective acetylcholinesterase inhibitors Eur. J. Med. Chem. 2010, 45, 1415-1423
44. Pin, F.; Comesse, S.; Daïch, A. Intramolecular N -aza-amidoalkylation in association with WitkopeWinterfeldt oxidation as the key step to synthesize Luotonin-A analogues Tetrahedron 2011, 67, 5564-5571
45. Dong, G.; Sheng, C.; Wang, S.; Miao, Z.; Yao, J.; Zhang, W. Selection of evodiamine as a novel topoisomerase I inhibitor by structure-based virtual screening and hit optimization of evodiamine derivatives as antitumor agents J. Med. Chem. 2010, 53, 7521-7531
46. Nakayama, A.; N., Ka; M., ku; H., Te, Straightforward asymmetric total synthesis of (+)-evodiamine, a major indole alkloid in herbal medicine "Wu Zhu Yu" Heterocycles 2008, 76, 861-865
47. Fujii, A.; Hashiguchi, S.; Uematsu, N.; Ikariya, T.; Noyori, R. Ruthenium(II)-Catalyzed Asymmetric Transfer Hydrogenation of Ketones Using a Formic Acid-Triethylamine Mixture J. Am. Chem. Soc. 1996, 118, 2521-2522 (Pubitemid 26120941)
48. Lee, S. H.; Son, J. K.; Jeong, B. S.; Jeong, T. C.; Chang, H. W.; Lee, E. S.; Jahng, Y. Progress in the studies on rutaecarpine Molecules 2008, 13, 272-300
49. Jones, G.; Willett, P.; Glen, R. C.; Leach, A. R.; Taylor, R. Development and validation of a genetic algorithm for flexible docking J. Mol. Biol. 1997, 267, 727-748 (Pubitemid 27170693)
50. Desmond-Maestro-academic-2009-02; http://www.deshawresearch.com.
51. Liu, X.; Jiang, H.; Li, H. SHAFTS: a hybrid approach for 3D molecular similarity calculation. 1. Method and assessment of virtual screening J. Chem. Inf. Model. 2011, 51, 2372-2385
52. Lu, W.; Liu, X.; Cao, X.; Xue, M.; Liu, K.; Zhao, Z.; Shen, X.; Jiang, H.; Xu, Y.; Huang, J.; Li, H. SHAFTS: a hybrid approach for 3D molecular similarity calculation. 2. Prospective case study in the discovery of diverse p90 ribosomal S6 protein kinase 2 inhibitors to suppress cell migration J. Med. Chem. 2011, 54, 3564-3574
53. MDL Drug Data Report; Symyx Technologies, Inc.: Sunnyvale, CA.
54. Nitiss, J. L. Targeting DNA topoisomerase II in cancer chemotherapy Nature Rev. Cancer 2009, 9, 338-350
55. Jun, K. Y.; Lee, E. Y.; Jung, M. J.; Lee, O. H.; Lee, E. S.; Park Choo, H. Y.; Na, Y.; Kwon, Y. Synthesis, biological evaluation, and molecular docking study of 3-(3′-heteroatom substituted-2′-hydroxy-1′-propyloxy) xanthone analogues as novel topoisomerase II alpha catalytic inhibitor Eur. J. Med. Chem. 2011, 46, 1964-1971
56. Graves, D. E. Drug-DNA Interactions Methods Mol. Biol. 2001, 95, 161-169
57. Peixoto, P.; Bailly, C.; Helene, M.; David-Cordonnier, M.-H. Topoisomerase I-mediated DNA relaxation as a tool to study intercalation of small molecules into supercoiled DNA. In Drug-DNA Interaction Protocols, 2nd ed.; Fox, K. R., Ed.; Humana Press; Totowa, NJ, 2010; Vol. 613, pp 235-256.
58. Suh, D.; Chaires, J. B. Criteria for the mode of binding of DNA binding agents Bioorg. Med. Chem. 1995, 3, 723-728
59. Palchaudhuri, R.; Hergenrother, P. J. DNA as a target for anticancer compounds: methods to determine the mode of binding and the mechanism of action Curr. Opin. Biotechnol. 2007, 18, 497-503
60. Perrin, D.; van Hille, B.; Barret, J. M.; Kruczynski, A.; Etievant, C.; Imbert, T.; Hill, B. T. F 11782, a novel epipodophylloid non-intercalating dual catalytic inhibitor of topoisomerases I and II with an original mechanism of action Biochem. Pharmacol. 2000, 59, 807-819 (Pubitemid 30081704)
61. Huang, H.; Chen, Q.; Ku, X.; Meng, L.; Lin, L.; Wang, X.; Zhu, C.; Wang, Y.; Chen, Z.; Li, M.; Jiang, H.; Chen, K.; Ding, J.; Liu, H. A series of alpha-heterocyclic carboxaldehyde thiosemicarbazones inhibit topoisomerase IIalpha catalytic activity J. Med. Chem. 2010, 53, 3048-3064
62. Vos, S. M.; Tretter, E. M.; Schmidt, B. H.; Berger, J. M. All tangled up: how cells direct, manage and exploit topoisomerase function Nature Rev. Mol. Cell Biol. 2011, 12, 827-841
63. Pommier, Y. DNA topoisomerase I inhibitors: chemistry, biology, and interfacial inhibition Chem. Rev. 2009, 109, 2894-2902
64. Bailly, C. Contemporary Challenges in the Design of Topoisomerase II Inhibitors for Cancer Chemotherapy Chem. Rev. 2012, 112, 3611-3640
65. Denny, W. A.; Baguley, B. C. Dual topoisomerase I/II inhibitors in cancer therapy Curr. Top. Med. Chem. 2003, 3, 339-353
66. Dallavalle, S.; Gattinoni, S.; Mazzini, S.; Scaglioni, L.; Merlini, L.; Tinelli, S.; Beretta, G. L.; Zunino, F. Synthesis and cytotoxic activity of a new series of topoisomerase I inhibitors Bioorg. Med. Chem. Lett. 2008, 18, 1484-1489 (Pubitemid 351226518)
67. Salerno, S.; Da Settimo, F.; Taliani, S.; Simorini, F.; La Motta, C.; Fornaciari, G.; Marini, A. M. Recent advances in the development of dual topoisomerase I and II inhibitors as anticancer drugs Curr. Med. Chem. 2010, 17, 4270-4290
68. Sheng, C.; Miao, Z.; Zhang, W. New strategies in the discovery of novel non-camptothecin topoisomerase I inhibitors Curr. Med. Chem. 2011, 18, 4389-4409
69. Martin, S. F.; Benage, B.; Hunter, J. E. A concise strategy for the syntheses of indole alkaloids of the heteroyohimboid and corynantheioid families. Total syntheses of (±)-tetrahydroalstonine, (±)-cathenamine and (±)-geissoschizine J. Am. Chem. Soc. 1988, 110, 5925-5927
70. D'Souza, A. M.; Spiccia, N.; Basutto, J.; Jokisz, P.; Wong, L. S.; Meyer, A. G.; Holmes, A. B.; White, J. M.; Ryan, J. H. 1,3-Dipolar cycloaddition-decarboxylation reactions of an azomethine ylide with isatoic anhydrides: formation of novel benzodiazepinones Org. Lett. 2011, 13, 486-489
71. Aleksic, M.; Bertosa, B.; Nhili, R.; Uzelac, L.; Jarak, I.; Depauw, S.; David-Cordonnier, M. H.; Kralj, M.; Tomic, S.; Karminski-Zamola, G. Novel Substituted Benzothiophene and Thienothiophene Carboxanilides and Quinolones: Synthesis, Photochemical Synthesis, DNA-Binding Properties, Antitumor Evaluation and 3D-Derived QSAR Analysis J. Med. Chem. 2012, 55, 5044-5060
72. Wang, P.; Leung, C. H.; Ma, D. L.; Lu, W.; Che, C. M. Organoplatinum(II) complexes with nucleobase motifs as inhibitors of human topoisomerase II catalytic activity Chem. Asian J. 2010, 5, 2271-2280
73. Li, X.; Lin, Y.; Wang, Q.; Yuan, Y.; Zhang, H.; Qian, X. The novel anti-tumor agents of 4-triazol-1,8-naphthalimides: synthesis, cytotoxicity, DNA intercalation and photocleavage Eur. J. Med. Chem. 2011, 46, 1274-1279
74. Baviskar, A. T.; Madaan, C.; Preet, R.; Mohapatra, P.; Jain, V.; Agarwal, A.; Guchhait, S. K.; Kundu, C. N.; Banerjee, U. C.; Bharatam, P. V. N-Fused imidazoles as novel anticancer agents that inhibit catalytic activity of topoisomerase IIalpha and induce apoptosis in G1/S phase J. Med. Chem. 2011, 54, 5013-5030
75. Du, L.; Liu, H. C.; Fu, W.; Li, D. H.; Pan, Q. M.; Zhu, T. J.; Geng, M. Y.; Gu, Q. Q. Unprecedented citrinin trimer tricitinol B functions as a novel topoisomerase IIalpha inhibitor J. Med. Chem. 2011, 54, 5796-5810
76. Marshall, K. M.; Holden, J. A.; Koller, A.; Kashman, Y.; Copp, B. R.; Barrows, L. R. AK37: the first pyridoacridine described capable of stabilizing the topoisomerase I cleavable complex Anticancer Drugs 2004, 15, 907-913 (Pubitemid 39482932)
77. Routier, S.; Peixoto, P.; Merour, J. Y.; Coudert, G.; Dias, N.; Bailly, C.; Pierre, A.; Leonce, S.; Caignard, D. H. Synthesis and biological evaluation of novel naphthocarbazoles as potential anticancer agents J. Med. Chem. 2005, 48, 1401-1413 (Pubitemid 40372209)
78. Wei, H.; Ruthenburg, A. J.; Bechis, S. K.; Verdine, G. L. Nucleotide-dependent domain movement in the ATPase domain of a human type IIA DNA topoisomerase J. Biol. Chem. 2005, 280, 37041-37047 (Pubitemid 41587788)
79. Discovery Studio 3.0; Accelrys Software Inc.: San Diego, CA, 2010; http://www.accelrys.com.
80. Shaw, D. E. A fast, scalable method for the parallel evaluation of distance-limited pairwise particle interactions J. Comput. Chem. 2005, 26, 1318-1328 (Pubitemid 41454622)
81. Bowers, K. J.; Chow, E.; Xu, H.; Dror, R. O.; Eastwood, M. P.; Gregersen, B. A.; Klepeis, J. L.; Kolossváry, I.; Moraes, M. A.; Sacerdoti, J. K.; Shan, Y.; Shaw, D. E. Scalable Algorithms for Molecular Dynamics Simulations on Commodity Clusters. Proceedings of the ACM/IEEE Conference on Supercomputing (SC06), Tampa, Florida, November 11-17, 2006.
82. Bowers, K. J.; Dror, R. O.; Shaw, D. E. The midpoint method for parallelization of particle simulations J. Chem. Phys. 2006, 124, 184109
83. Bowers, K. J.; Dror, R. O.; Shaw, D. E. Zonal Methods for the Parallel Execution of Range-Limited N-Body Simulations J. Comput. Phys. 2007, 221, 303-329