Structural and biological characterization of the tubulin interaction with dinitroanilines

Cytology and Genetics

Volumn 43, Issue 4, 2009, Pages 267-282

  Nyporko, A Yu ^a,b   Yemets, A I ^b   Brytsun, V N ^c   Lozinsky, M O ^c   Blume, Ya B ^a  

^a INSTITUTE OF FOOD BIOTECHNOLOGY AND GENOMICS   (Ukraine)

^b INSTITUTE OF CELL BIOLOGY AND GENETIC ENGINEERING   (Ukraine)

^c INSTITUTE OF ORGANIC CHEMISTRY   (Ukraine)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; PROTOZOA;

EID: 77954510797     PISSN: 00954527     EISSN: 19349440     Source Type: Journal    
DOI: 10.3103/S0095452709040082     Document Type: Article

References (96)

1. Mel'nikov, N.N., in Pestitsidy i regulyatory rosta rastenii (Pesticides and Plant Growth Regulators), Mel'nikov, N.N., Novozhilov, K.V., and Belan, S.R., Eds., Moscow: Khimiya, 1995.
2. Britsun, V.M., Yemets, A.I., Lozins'ky, M.O., and Blume, Ya.B., 2,5-Dinitroanilines: Synthesis and Pesticidal and Antiprotozoan Properties, Bioorg. Acta, 2009, no.2 (in press).
3. Zakharenko, V.A., Gerbitsidy (Herbicides), Moscow: Agropromizdat, 1990.
4. Parka, S.J. and Soper, O.F., The Physiology and Mode of Action of the Dinitroaniline Herbicides, Weed Sci., 1977, vol.25, pp. 79-87.
5. Upadhyaya, M.K. and Noodén, L.D., Mode of Dinitroaniline Herbicide Action, Plant Physiol., 1980, vol.66, pp. 1048-1052.
6. Molin, W.T and Khan, R.A, in Herbicide Activity: Toxicology, Biochemistry and Molecular Biology, Roe, R.M., Ed., Burke (VA, USA): IOS Press, 1997, pp. 143-158.
7. Vaughn, K.C, in Plant Microtubules: Potential for Biotechnology, Nick, P., Ed., Berlin: Springer Verlag, 2000, pp. 193-205.
8. Morejohn, L.C., Bureau, T.E., Molé-Bajer, J., Bajer, A.S., and Fosket, D.E., Oryzalin, a Dinitroaniline Herbicide, Binds to Plant Tubulin and Inhibits Microtubule Polymerization in vitro, Planta, 1987, vol.172, pp. 252-264.
9. Morejohn, L.C. and Fosket, D.E., The Biochemistry of Compounds with Anti-Microtubule Activity in Plant Cells, Pharm. Ther., 1991, vol.51, pp. 217-230.
10. Correa, J.J., Effects of Antimitotic Agents on Tubulin- Nucleotide Interactions, Pharm. Ther., 1991, vol.52, pp. 127-147.
11. Correa, J.J. and Lobert, S., Physiochemical Aspects of Tubulin-Interacting Antimitotic Drugs, Curr. Pharm. Design, 2001, vol.7, pp. 1213-1223.
12. Yemets, A.I. and Blume, Ya.B., Resistance to Herbicides with Antimicrotubular Activity: From Natural Mutants to Transgenic Plants, Fiziol. Rast., 1999, vol.46, no.6, pp. 899-907 [Russ. J. Plant Physiol., 1999, vol. 46, no. 6, pp. 789-796].
13. Jordan, M.A. and Wilson, L., Microtubules As a Target for Anticancer Drugs, Nat. Rev. Cancer, 2004, vol.4, p. 253-265.
14. Dumontet, C., Mechanisms of Action and Resistance to Tubulin-Binding Agents, Exp. Opin. Investig. Drugs, 2000, vol.9, pp. 779-788.
15. Anthony, R.G., Waldin, T.R., Ray, J.A., Bright, S.W.J., and Hussey, P.J., Herbicide Resistance Caused by Spontaneous Mutation of the Cytoskeletal Protein Tubulin, Nature, 1998, vol.393, pp. 260-263.
16. Bogitsh, B.J., Middleton, O.L., and Ribeiro-Rodrigues, R., Effects of the Antitubulin Drug Trifluralin on the Proliferation and Metacyclogenesis of Trypanosoma cruzi Epi- mastigotes, Parasit. Res, 1999, vol.85, pp. 475-1180
17. Traub-Cseko, Y.M., Ramalho-Ortigao, J.M., Dantas, A.P., de Castro, S.L., Barbosa, H.S., and Sowning, K.H., Dini- troaniline Herbicides Against Protozoan Parasites: The Case of Trypanosoma cruzi, Trends Parasit., 2001, vol.17, pp. 136-141.
18. Fosket, D.E. and Morejohn, L.C., Structural and Functional Organization of Tubulin, Ann. Rev. Plant Physiol. Plant. Mol. Biol., 1992, vol.43, pp. 201-240.
19. McKean, P.G., Vaughan, S., and Gull, K., The Extended Tubulin Superfamily, J. Cell Sci., 2001, vol.114, pp. 2723-2733.
20. Nogales, E., Wolf, S.G., and Downing, K.H., Structure of the Tubulin Dimmer by Electron Crystallography, Nature, 1998, vol.391, pp. 199-203.
21. Gogonea, C.B., Gogonea, V., Ali, Y.M., Merz, K.M.Jr., and Siddiqui, S.S., Computational Prediction of the Three-Dimensional Structures for the Caenorhabditis elegans Tubulin Family, J. Mol. Graph. Modell., 1999, vol.17, pp. 90-100.
22. Löwe, J., Li, H., Downing, K.H., and Nogales, E., Refined Structure of Tubulin at 3.5 A Resolution, J. Mol. Biol., 2001, vol.313, pp. 1045-1057.
23. Nyporko, A.Yu. and Blume, Ya.B., Comparative Analysis of Secondary Structure of Tubulins and FtsZ Proteins, Biopolim. Kletka, 2001, vol.17, pp. 61-69.
24. Murzin, A.G., Brenner, S.E., Hubbard, T., and Chothia, C., SCOP: A Structural Classification of Proteins Database for the Investigation of Sequences and Structures, J. Mol. Biol., 1995, vol.247, pp. 536-540.
25. Little, M. and Seehaus, T., Comparative Analysis of Tubulin Sequences, Comp. Biochem. Physiol., 1988, vol.90B, pp. 655-670.
26. Demchuk, O.N. and Blume, Ya.B., Construction of Phylogenetic Tree of Plant Tubulins Basing on the Homology of Their Protein Sequences, Tsitol. Genet., 2005, vol.39, no.2, pp. 3-9.
27. Nogales, E., Whittaker, M., Milligan, R.A., and Downing, K.H., High-Resolution Model of the Microtubule, Cell, 1999, vol.96, pp. 79-88.
28. Meurer-Grob, P., Kasparian, J., and Wade, R.H., Microtubule Structure at Improved Resolution, Biochemistry, vol.40, pp. 8000-8008.
29. Strashnyuk, N.M. and Blume, Ya.B., Obtaining Mutants for Microtubule Protein Genes, Tsitol. Genet., 1993, vol.27, pp. 79-96.
30. Yemets, A.I. and Blume, Ya.B., Mutant Genes of Plant Tubulins As Selective Marker Genes for Genetic Engineering, Tsitol. Genet., 2007, vol.41, no.3, pp. 29-43.
31. Baird, W.V, Blume, Ya.B, and Wick, S, in Plant Microtubules: Potential for Biotechnology, Nick, P., Ed., Berlin: Springer Verlag, 2000, pp. 159-191.
32. Nyporko, A.Yu. and Blume, Y.B., in The Plant Cytoskeleton: A Key Tool for Agro-Biotechnology, Blume, Y.B., Baird, W.V., Yemets, A.I., and Breviario, D., Eds., Dordrecht: Springer, 2008.
33. Borck, K. and Braymer, H.D., The Genetic Analysis of Resistance to Benomyl in Neurospara crassa, J. Gen. Microbiol., 1974, vol.85, pp. 51-56.
34. Thomas, J.H., Neff, N.F., and Botstein, D., Isolation and Characterization of Mutations in the P-Tubulin Gene of Saccharomyces cerevisiae, Genetics, 1985, vol.112, pp. 715-734.
35. Orbach, M.J., Porro, E.B., and Yanofsky, C., Cloning and Characterization of the Gene for β-Tubulin from a Benomyl-Resistant Mutant of Neurospora crassa and Its Use As a Dominant Selectable Marker, Mol. Cell Biol., 1986, vol.6, pp. 2452-2461.
36. Jung, M.K. and Oakley, B.R., Identification of An Amino Acid Substitutions in the ben, β-Tubulin Gene of Aspergillus nidulans That Confers Thiabendazole Resistance and Benomyl Supersensitivity, Cell Motil. Cytoskelet., 1990, vol.17, pp. 87-94.
37. Lee, V.D. and Huang, B., Missense Mutations at Lysine 350 in Tubulin Confer Altered Sensitivity to Microtubule Inhibitors in Chlamydomonas, Plant Cell, 1990, vol.2, pp. 1051-1057.
38. Takahashi, M., Matsumoto, S., Iwasaki, S., and Yahara, I., Molecular Basis for Determining the Sensitivity of Eukaryotes to the Antimitotic Drug Rhizoxin, Mol. Gen. Genet., 1990, vol.222, pp. 169-175.
39. Schilber, M.J. and Huang, B., The ColR4 and ColR16 β-Tubulin Mutations in Chlamydomonas Reinhardtii Confer Altered Sensitivities to Microtubule Inhibitors and Herbicides by Enhancing Microtubule Stability, J. Cell Biol., 1991, vol.113, pp. 605-614.
40. Jung, M.K., Wilder, I.B., and Oakley, B.R., Amino Acid Alterations in the ben (β-Tubulin) Gene of Aspergillus nidulans That Confer Benomyl Resistance, Cell Motil. Cytoskelet., 1992, vol.22, pp. 170-174.
41. Fujimura, M., Kamakura, T., Inoue, H., and Yamaguchi, I., Amino-Acid Alterations in the Beta-Tubulin Gene of Neurospora crassa That Confer Resistance to Carbendazim and Diethofencarb, Curr. Genet., 1994, vol.25, pp. 418-1122
42. Buhr, T.L. and Dickman, M.B., Isolation, Characterization, and Expression of a Second Beta-Tubulin- Encoding Gene from Colletotrichum gloeosporioides F. sp. aeschynomene, Appl. Environ. Microbiol., 1994, vol.60, pp. 4155-4159.
43. Park, S.Y., Jung, O.J., Chung, Y.R., and Lee, C.W., Isolation and Characterization of a Benomyl-Resistant Form of Beta-Tubulin-Encoding Gene from the Phyto- pathogenic Fungus Botryotinia fuckeliana, Mol. Cells, 1997, vol.7, pp. 104-109.
44. Giannakakou, P., Sackett, D.L., Kang, Y.K., Zhan, Z., Buters, J.T., Fojo, T., and Poruchynsky, M.S., Paclitaxel- Resistant Human Ovarian Cancer Cells Have Mutant Beta-Tubulins That Exhibit Impaired Paclitaxel-Driven Polymerization, J. Biol. Chem., 1997, vol.272, pp. 17118-17125.
45. McKay, G.J. and Cooke, L.R., A PCR-Based Method to Characterize and Identify Benzimidazole Resistance in Helminthosporium solani, FEMS Microbiol. Letts., 1997, vol.152, pp. 371-378.
46. Yamamoto, E., Zeng, L., and Biard, W.V., Tubulins Missense Mutations Correlate with Antimicrotubule Drug Resistance in Eleusine indica, Plant Cell, 1998, vol.10, pp. 297-308.
47. Elard, L. and Humbert, J.F., Importance of the Mutation of Amino Acid 200 of the Isotype 1 Beta-Tubulin Gene in the Benzimidazole Resistance of the Small-Ruminant Parasite Teladorsagia circumcincta, Parasit. Res, 1999, vol.85, pp. 452-1156
48. Gonsales-Garay, M., Chang, L., Blade, K., and Menick, D., CabralF. A Beta-Tubulin Leucine Involved in Microtubule Assembly and Pacitaxel Resistance, J. Biol. Chem., 1999, vol.274, pp. 23875-23882.
49. Giannakakou, P., Gussio, R., Nogales, E., Downing, K.H., Zaharevitz, D., Bollbuck, B., Poy, G., Sackett, D., Nicolaou, K.C., and Fojo, T., A Common Pharmacophore for Epothilone and Taxanes: Molecular Basis for Drug Resistance Conferred by Tubulin Mutations in Human Cancer Cells, Proc. Nat. Acad. Sci. USA, 2000, vol.97, pp. 2904-2909.
50. He, L., Yang, C.P., and Horwitz, S.B., Mutations in Beta Tubulin Map to Domains Involved in Regulation of Microtubule Stability in Epothilone-Resistant Cell Lines, Mol. Cancer. Ther., 2001, vol.1, pp. 3-10.
51. Hua, X.H., Genini, D., Gussio, R., Tawatao, R., Shih, H., Kipps, T.J., Carson, D.A., and Leoni, L.M., Biochemical Genetic Analysis of Indanocine Resistance in Human Leukemia, Cancer Res., 2001, vol.61, pp. 7248-7254.
52. Kavallaris, M., Tait, A.S., Walsh, B.J., He, L., Horwitz, S.B., Norris, M.D., and Haber, M., Multiple Microtubule Alterations Are Associated with Vinca a Alkaloid Resistance in Human Leukemia Cells, Cancer Res., 2001, vol.61, pp. 5803-5809.
53. Hasegawa, S., Miyoshi, Y., Egawa, C., Ishitobi, M., Tamaki, Y., Monden, M., and Noguchi, S., Mutational Analysis of the Class I Beta-Tubulin Gene in Human Breast Cancer, Int. J. Cancer, 2002, vol.101, pp. 46-51.
54. Leroux, P., Fritz, R., Debieu, D., Albertini, C., Lanen, C., Bach, J., Gredt, M., and Chapeland, F., Mechanisms of Resistance to Fungicides in Field Strains of Botrytis cinerea, Pest. Manag. Sci., 2002, vol.58, pp. 876-888.
55. Hari, M., Wang, Y., Veeraraghavan, S., and Cabral, F., Mutations in Alpha-and Beta-Tubulin That Stabilize Microtubules and Confer Resistance to Colcemid and Vinblastine, Mol. Cancer Ther., 2003, vol.7, pp. 597-605.
56. Ma, Z., Yoshimura, M.A., and Michailides, T.J., Identification and Characterization of Benzimidazole Resistance in Monilinia fructicola from Stone Fruit Orchards in California, Appl. Environ. Microbiol., 2003, vol.69, pp. 7145-7152. (Pubitemid 38585363)
57. Ma, Z., Yoshimura, M.A., Holtz, B.A., and Michailides, T.J., Characterization and PCR-Based Detection of Benzimi- dazole-Resistant Isolates of Monilinia laxa in California, Pest. Manag. Sci., 2005, vol.61, pp. 449-457.
58. Martello, L.A., Verdier-Pinard, P., Shen, H.J., He, L., Torres, K., Orr, G.A., and Horwitz, S.B., Elevated Levels of Microtubule Destabilizing Factors in a Taxol Resistant/Dependent A549 Cell Line with An Alpha-Tubulin Mutation, Cancer Res., 2003, vol.63, pp. 1207-1213.
59. Verrills, N.M., Flemming, C.L., Liu, M., Ivery, M.T., Cobon, G.S., Norris, M.D., Haber, M., and Kavallaris, M., Microtubule Alterations and Mutations Induced by Des-oxyepothilon EB: Implications for Drug-Target Interactions, Chem. Biol., 2003, vol.10, pp. 597-607.
60. Delye, C., Menchari, Y., Michel, S., and Darmency, H., Molecular Bases for Sensitivity to Tubulin-Binding Herbicides in Green Foxtail, Plant Physiol., 2004, vol.136, pp. 3920-3932.
61. Loganzo, F., Hari, M., Annable, T., Tan, X., Morilla, D.B., Musto, S., Zsck, A., Kaplan, J., Minnick, A.A.Jr., May, M.K., Ayral-Kaloustian, S., Poruchynsky, M.S., Fojo, T., and Greenberger, L.M., Cells Resistant To HTI-286 Do Not Overexpress P-Glycoprotein But Have Reduced Drug Accumulation and a Point Mutation in Alpha-Tubulin, Mol. Cancer. Ther., 2004, vol.10, pp. 1319-1327.
62. Poruxhynsky, M.S., Kim, J.H., Nogales, E., Annable, T., Loganzo, F., Greenberger, L.M., Sackett, D.L., and Fojo, T., Tumor Cells Resistant to a Microtubule-Depolymerizing Hemiasterlin Analogue, HTI-286, Have Mutations in Alpha-or Beta-Tubulin and Increased Microtubule Stability, Biochemistry, 2004, vol.43, pp. 13944-13954.
63. Ruiz, F., Dupuis-Williams, P., Klotz, C., Forguignon, F., Bergdoll, M., Beisson, J., and Koll, F., Genetic Evidence for Interaction between Eta- and Beta-Tubulins, Eukaryot. Cell, 2004, vol.3, pp. 212-220.
64. Wang, Y., Veeraraghavan, S., and Cabral, F., Intra-Allelic Suppression of a Mutation That Stabilizes Microtubules and Confers Resistance to Colcemid, Biochemistry, 2004, vol.43, pp. 8965-8973.
65. Gokmen-Polar, Y., Escuin, D., Walls, C.D., Soule, S.E., Wang, Y., Sanders, K.L., Lavallee, T.M., Wang, M., Guenther, B.D., Giannakakou, P., and Sledge, G.W., β-Tubulin Mutations Are Associated with Resistance to 2-Methoxyestradiol in MDA-MB-435 Cancer Cells, Cancer Res., 2005, vol.65, pp. 9406-9414.
66. Tresch, S., Plath, P., and Grossmann, K., Herbicidal Cyanoacrylates with Antimicrotubule Mechanism of Action, Pest. Manag. Sci., 2005, vol.61, no.11, pp. 1052-1059.
67. Yang, C.P., Verdier-Pinard, P., Wang, F., Lippaine-Hor-vath, E., He, L., Li, D., Hofle, G., Ojima, I., Orr, G.A., and Horwitz, S.B., A Highly Epothilone B-Resistant A549 Cell Line with Mutations in Tubulin That Confer Drug Dependence, Mol. Cancer. Ther., 2005, vol.4, pp. 987-995.
68. Blackhall, W.J., Drogemuller, M., Schnieder, T., and von Samson-Himmelstjerna, G., Expression of Recombinant Beta-Tubulin Alleles from Cylicocylus nassatus (Cya- thostominae), Parasit. Res., vol.99, 2006, pp. 687-693.
69. Hari, M., Loganzo, F., Annable, T., Tan, X., Musto, S., Morilla, D.B., Nettles, J.H., Snyder, J.P., and Green- berger, L.M., Paclitaxel-Resistant Cells Have a Mutation in the Paclitaxel-Binding Region of Beta-Tubulin (Asp26Glu) and Less Stable Microtubules, Mol. Cancer. Ther., 2006, vol.5, pp. 270-278.
70. Wang, Y., Yin, S., Blade, K., Cooper, G., Menick, D.R., and Cabral, F., Mutations at Leucine 215 of Beta-Tubu- lin Affect Pfclixal Sensitivity by Two Distinct Mechanisms, Biochemistry, 2006, vol.45, pp. 185-194.
71. Ghisi, M., Kaminsky, R., and Mäser, P., Phenotyping and Genotyping of Haemonchus contortus Isolates Reveals a New Putative Candidate Mutation for Benzimidazole Resistance in Nematodes, Vet. Parisit., 2007, vol.144, pp. 313-320.
72. Nyporko, A.Yu., Zhivolup, A.N., and Blume, Ya.B., Comparative Analysis of Primary Structure Mutant Tubulins with Resistance to Antimicrotubular Drugs for Predications of New Mutations with Analogous Properties, Tsitol. Genet., 2003, vol.37, no.2, pp. 69-78.
73. Mudge, L.C., Gossett, B.J., and Murphy, T.R., Resistance of Goosegrass (Eleusine indica) to Dinitroaniline Herbicides, Weed Res., 1984, vol.32, pp. 591-594.
74. Vaughn, K.C and Vaughan, M.A, Structural and Biochemical Characterization of Dinitroaniline-Resistant Eleusine, in Managing Resistance to Agrochemicals, Green, M.B., Le, H.M., and LeBaron, W.K., Eds., Washington, 1990, vol.421, pp. 364-375.
75. Smeda, R.J., Vaughn, K.C., and Morrison, I.N., Trifluralin-Resistant Green Foxtail Setaria viridis L., Beauv. Exhibits Cross-Resistance to Mitotic Disrupter Herbicides, Plant Physiol., 1992, vol.96, p. 114.
76. Blume, Ya.B., Strashnyuk, N.M., Smertenko, A.P., Solo-dushko, V.G., and Gleba, Yu.Yu., Alterations in β-Tubulin Ensure the Resistance to Trifluralin of Nicotiana plumbaginifolia Mutant Lines Obtained in Vitro, Proc. Natl. Acad. Sci. Ukraine, 1996, no.7, pp. 132-137.
77. Yemets, A.J., Nyporko, A.Yu., Swire-Clark, G., Baird, W.V., and Blume, Ya.B., Mechanisms of Plant Resistance to Dinitroanilines and Phosphoroamidates Based on Tubu- lin Mutations, in Abstr. XVII Int. Bot. Congress, Vienna, 2005, p. 292.
78. Lowe, D.B., Swire-Clark, G.A., McCarty, L.B., Whit-well, T., and Baird, W.V., Biology and Molecular Analysis of Dinitroaniline-Resistant Poa annua L., Int. Turf-grass Soc. Res. J., 2001, vol.9, pp. 1019-1025.
79. Cronin, K.E., Hussey, P.J., Ray, J.A., and Waldin, T.R., Herbicide Resistant Plants, World Intellect. Property Org. Int. Publ., 1993, no. WO 93/24637.
80. Ellis, J.R., Taylor, R., and Hussey, P.J., Molecular Modeling Indicates That Two Chemically Distinct Classes of Antimitotic Herbicide Bind to the Same Receptor Site (S), Plant Physiol., 1993, vol.105, pp. 15-18.
81. Murthy, J.V., Kim, H.H., Hanesworth, V.R., Hugdahl, J.D., and Morejohn, L.C., Competitive-Inhibition of High- Affinity Oryzalin Binding to Plant Tubulin by the Phosphoric Amide Herbicide Amiprophos-Methyl, Plant Physiol., 1994, vol.105, pp. 309-320.
82. Nyporko, A.Yu., Yemets, A.I., Klimkina, L.A., and Blume, Ya.B., Sensitivity of Eleusine indica Callus to Trifluralin and Amiprophosmethyl in Correlation with the Binding of These Compounds to Tubulin, Fiziol. Rast., 2002, vol.49, no.3, pp. 459-1166 [Russ. J. Plant Physiol., 2002, no.3, pp. 413-418].
83. Blume, Ya.B., Nyporko, A.Yu., Yemets, A.I., and Baird, W.V., Structural Modeling of Plant a-Tubulin Interaction with Dinitroanilines and Phosphoroamidates, Cell Biol. Int., 2003, vol.27, pp. 171-174.
84. Ravelli, R., Gigant, B., Curmi, P., Jourdain, I., Lachkar, S., Sobel, A., and Knosso, M., Insight Into Tubulin Regulation from a Complex with Colchicines and a Stathmi-Like Domain, Nature, 2004, vol.428, pp. 198-202.
85. Gigant, B., Wang, C., Ravelli, R.B., Roussi, F., Steinmetz, M.O., Curmi, P.A., Sobel, A., and Knossow, M., Structural Basis for the Regulation of Tubulin by Vin- blastine, Nature, 2005, vol.435, pp. 519-522.
86. Robinson, M.W., McFerran, N., Trudgett, A., Hoey, L., and Fairweather, I., A Possible Model of Benzimidazole Binding to β-Tubulin Disclosed by Invoking an Inter Domain Movement, J. Mol. Graphics Modell., 2004, vol.23, pp. 275-284.
87. Snyder, J.P., Nettles, J.H., Cornett, B., Downing, K.H., and Nogales, E., the Binding Conformation of Taxol in P-Tubulin: A Model Based on Electron Crystallographic Density, Proc. Nat. Acad. Sci. USA, 2001, vol.98, pp. 5312-5316.
88. Nettles, J.H., Li, H., Cornett, B., Krahn, J.M., Snyder, J.P., and Downing, K.H., The Binding Mode of Epothilone A on α, β-Tubulin by Electron Crystallography, Science, 2004, vol.305, pp. 866-869.
89. Nogales, E. and Wang, H.W., Structural Mechanisms Underlying Nucleotide-Dependent Self-Assembly of Tubulin and Its Relatives, Curr. Opin. Struct. Biol., 2006, vol.16, pp. 221-229.
90. Nyporko, A.Yu. and Blume, Ya.B., Structural Perturbation of Longitudinal and Lateral Contact Interfaces of Tubulins Induced by Interaction with Microtubule Stabilizing Compounds in Proc. of the 3rd Moscow Conference on Computational Molecular Biology, Moscow, 2007, pp. 235-236.
91. Blume, Ya.B., Nyporko, A.Yu., Yemets, A.I., and Baird, W.V., Are Earlier Predicted Sites of Different Plant Tubulins Involved in Interaction with Dinitroa- nilines? Mol. Biol. Cell, 2002, vol.13, p. 463a.
92. Fennell, B.J., Nuaughton, J.A., Dempsey, E., and Bell, A., Cellular and Molecular Actions of Dinitroaniline and Phosphorothioamidat Herbicides on Plasmodium Falci-parum: Tubulin as a Specific Antimalarial Target, Mol. Biochem. Parasit., 2006, vol.145, pp. 226-238.
93. Morissette, N.S., Mitra, A., Sept, D., and Sibley, L.D., Dinitroanilines Bind α-Tubulin to Disrupt Microtubules, Mol. Biol. Cell, 2004, vol.15, pp. 1960-1968.
94. Mitra, A. and Sept, D., Binding and Interaction of Dini-troanilines with Apicomplexan and Kinetoplastid α-Tubulin, J. Med. Chem., 2006, vol.49, pp. 5226-5231.
95. Morris, G.M., Goodsell, D.S., Halliday, R.S., Huey, R., Hart, W.E., Belew, R.K., and Olson, A.J., Automated Docking Using a Lamarckian Genetic Algorithm and Empirical Binding Free Energy Function, J. Comput. Chem., 1998, vol.19, pp. 1639-1662.
96. Nyporko, A.Yu., Yemets, A.I., and Blume, Ya.B., Protozoan and Plant Tubulins As Specific Targets for Dinitroa- nilines and Phosphoramidates: Common Structural Features and Interactive Sites, in Abstracts of 4th ISGO International Conf. of Structural Genomics, Beijing, 2006, pp. 257-259.