α-tubulin mutations alter oryzalin affinity and microtubule assembly properties to confer dinitroaniline resistance

Eukaryotic Cell

Volumn 9, Issue 12, 2010, Pages 1825-1834

  Lyons Abbott, Sally ^a   Sackett, Dan L ^b   Wloga, Dorota ^c   Gaertig, Jacek ^c   Morgan, Rachel E ^d,e   Werbovetz, Karl A ^d   Morrissette, Naomi S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

^d OHIO STATE UNIVERSITY   (United States)

^e UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COCCIDIOSTATIC AGENT; NITROBENZENE DERIVATIVE; ORYZALIN; PROTOZOAL PROTEIN; SULFANILAMIDE DERIVATIVE; TUBULIN;

ARTICLE; BINDING SITE; DRUG EFFECT; GENETICS; METABOLISM; MICROTUBULE; MUTATION; PROTEIN BINDING; TETRAHYMENA THERMOPHILA;

BINDING SITES; COCCIDIOSTATS; DINITROBENZENES; MICROTUBULES; MUTATION; PROTEIN BINDING; PROTOZOAN PROTEINS; SULFANILAMIDES; TETRAHYMENA THERMOPHILA; TUBULIN;

CILIOPHORA; PROTOZOA; TETRAHYMENA THERMOPHILA; TOXOPLASMA GONDII; VERTEBRATA;

EID: 78649890103     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00140-10     Document Type: Article

References (79)

1. Akella, J. S., D. Wloga, J. Kim, N. G. Starostina, S. Lyons-Abbott, N. S. Morrissette, S. T. Dougan, E. T. Kipreos, and J. Gaertig. 2010. MEC-17 is an alpha-tubulin acetyltransferase. Nature 467:218-222.
2. Anders, K. R., and D. Botstein. 2001. Dominant-lethal alpha-tubulin mutants defective in microtubule depolymerization in yeast. Mol. Biol. Cell 12:3973-3986.
3. Anthony, R. G., and P. J. Hussey. 1999. Dinitroaniline herbicide resistance and the microtubule cytoskeleton. Trends Plant Sci. 4:112-116.
4. Anthony, R. G., and P. J. Hussey. 1999. Double mutation in Eleusine indica alpha-tubulin increases the resistance of transgenic maize calli to dinitroaniline and phosphorothioamidate herbicides. Plant J. 18:669-674.
5. Anthony, R. G., S. Reichelt, and P. J. Hussey. 1999. Dinitroaniline herbicideresistant transgenic tobacco plants generated by co-overexpression of a mutant alpha-tubulin and a beta-tubulin. Nat. Biotechnol. 17:712-716.
6. Anthony, R. G., T. R. Waldin, J. A. Ray, S. W. Bright, and P. J. Hussey. 1998. Herbicide resistance caused by spontaneous mutation of the cytoskeletal protein tubulin. Nature 393:260-263.
7. Bhattacharya, G., J. Herman, D. Delfin, M. M. Salem, T. Barszcz, M. Mollet, G. Riccio, R. Brun, and K. A. Werbovetz. 2004. Synthesis and antitubulin activity of N1- and N4-substituted 3,5-dinitro sulfanilamides against African trypanosomes and Leishmania. J. Med. Chem. 47:1823-1832.
8. Bode, C. J., M. L. Gupta, K. A. Suprenant, and R. H. Himes. 2003. The two alpha-tubulin isotypes in budding yeast have opposing effects on microtubule dynamics in vitro. EMBO Rep. 4:94-99.
9. Chan, M. M., and D. Fong. 1990. Inhibition of leishmanias but not host macrophages by the antitubulin herbicide trifluralin. Science 249:924-926.
10. Davis, A., C. R. Sage, L. Wilson, and K. W. Farrell. 1993. Purification and biochemical characterization of tubulin from the budding yeast Saccharomyces cerevisiae. Biochemistry 32:8823-8835.
11. Delye, C., Y. Menchari, S. Michel, and H. Darmency. 2004. Molecular bases for sensitivity to tubulin-binding herbicides in green foxtail. Plant Physiol. 136:3920-3932.
12. Dufour, E., and T. Haertle. 1991. Binding of retinoids and beta-carotene to beta-lactoglobulin. Influence of protein modifications. Biochim. Biophys. Acta 1079:316-320.
13. Fast, N. M., L. Xue, S. Bingham, and P. J. Keeling. 2002. Re-examining alveolate evolution using multiple protein molecular phylogenies. J. Eukaryot. Microbiol. 49:30-37.
14. Foland, T. B., W. L. Dentler, K. A. Suprenant, M. L. Gupta Jr., and R. H. Himes. 2005. Paclitaxel-induced microtubule stabilization causes mitotic block and apoptotic-like cell death in a paclitaxel-sensitive strain of Saccharomyces cerevisiae. Yeast 22:971-978.
15. Fukushige, T., Z. K. Siddiqui, M. Chou, J. G. Culotti, C. B. Gogonea, S. S. Siddiqui, and M. Hamelin. 1999. MEC-12, an alpha-tubulin required for touch sensitivity in C. elegans. J. Cell Sci. 112 (Pt 3):395-403.
16. Gaertig, J., M. A. Cruz, J. Bowen, L. Gu, D. G. Pennock, and M. A. Gorovsky. 1995. Acetylation of lysine 40 in alpha-tubulin is not essential in Tetrahymena thermophila. J. Cell Biol. 129:1301-1310.
17. Gaertig, J., L. Gu, B. Hai, and M. A. Gorovsky. 1994. High frequency vector-mediated transformation and gene replacement in Tetrahymena. Nucleic Acids Res. 22:5391-5398.
18. Gaertig, J., T. H. Thatcher, L. Gu, and M. A. Gorovsky. 1994. Electroporation- mediated replacement of a positively and negatively selectable betatubulin gene in Tetrahymena thermophila. Proc. Natl. Acad. Sci. U. S. A. 91:4549-4553.
19. Gaertig, J., T. H. Thatcher, K. E. McGrath, R. C. Callahan, and M. A. Gorovsky. 1993. Perspectives on tubulin isotype function and evolution based on the observation that Tetrahymena thermophila microtubules contain a single alpha- and beta-tubulin. Cell Motil. Cytoskel. 25:243-253.
20. Gigant, B., P. A. Curmi, C. Martin-Barbey, E. Charbaut, S. Lachkar, L. Lebeau, S. Siavoshian, A. Sobel, and M. Knossow. 2000. The 4 A X-ray structure of a tubulin:stathmin-like domain complex. Cell 102:809-816.
21. Gigant, B., C. Wang, R. B. Ravelli, F. Roussi, M. O. Steinmetz, P. A. Curmi, A. Sobel, and M. Knossow. 2005. Structural basis for the regulation of tubulin by vinblastine. Nature 435:519-522.
22. Gull, K., P. J. Hussey, R. Sasse, A. Schneider, T. Seebeck, and T. Sherwin. 1986. Tubulin isotypes: generation of diversity in cells and microtubular organelles. J. Cell Sci. Suppl. 5:243-255.
23. Gupta, M. L., Jr., C. J. Bode, C. A. Dougherty, R. T. Marquez, and R. H. Himes. 2001. Mutagenesis of beta-tubulin cysteine residues in Saccharomyces cerevisiae: mutation of cysteine 354 results in cold-stable microtubules. Cell Motil. Cytoskel. 49:67-77.
24. Gupta, M. L., Jr., C. J. Bode, G. I. Georg, and R. H. Himes. 2003. Understanding tubulin-Taxol interactions: mutations that impart Taxol binding to yeast tubulin. Proc. Natl. Acad. Sci. U. S. A. 100:6394-6397.
25. Hai, B., J. Gaertig, and M. A. Gorovsky. 2000. Knockout heterokaryons enable facile mutagenic analysis of essential genes in Tetrahymena. Methods Cell Biol. 62:513-531.
26. Hai, B., and M. A. Gorovsky. 1997. Germ-line knockout heterokaryons of an essential alpha-tubulin gene enable high-frequency gene replacement and a test of gene transfer from somatic to germ-line nuclei in Tetrahymena thermophila. Proc. Natl. Acad. Sci. U. S. A. 94:1310-1315.
27. Hugdahl, J. D., C. L. Bokros, V. R. Hanesworth, G. R. Aalund, and L. C. Morejohn. 1993. Unique functional characteristics of the polymerization and MAP binding regulatory domains of plant tubulin. Plant Cell 5:1063-1080.
28. Hugdahl, J. D., and L. C. Morejohn. 1993. Rapid and reversible high-affinity binding of the dinitroaniline herbicide oryzalin to tubulin from Zea mays L. Plant Physiol. 102:725-740.
29. Ishida, T., Y. Kaneko, M. Iwano, and T. Hashimoto. 2007. Helical microtubule arrays in a collection of twisting tubulin mutants of Arabidopsis thaliana. Proc. Natl. Acad. Sci. U. S. A. 104:8544-8549.
30. James, S. W., C. D. Silflow, P. Stroom, and P. A. Lefebvre. 1993. A mutation in the alpha 1-tubulin gene of Chlamydomonas reinhardtii confers resistance to anti-microtubule herbicides. J. Cell Sci. 106:209-218.
31. Jordan, A., J. A. Hadfield, N. J. Lawrence, and A. T. McGown. 1998. Tubulin as a target for anticancer drugs: agents which interact with the mitotic spindle. Med. Res. Rev. 18:259-296.
32. Jordan, M. A. 2002. Mechanism of action of antitumor drugs that interact with microtubules and tubulin. Curr. Med. Chem. Anticancer Agents 2:1-17.
33. Jung, M. K., I. B. Wilder, and B. R. Oakley. 1992. Amino acid alterations in the benA (beta-tubulin) gene of Aspergillus nidulans that confer benomyl resistance. Cell Motil. Cytoskel. 22:170-174.
34. Keller, T. C., III, D. K. Jemiolo, W. H. Burgess, and L. I. Rebhun. 1982. Strongylocentrotus purpuratus spindle tubulin. II. Characteristics of its sensitivity to Ca++ and the effects of calmodulin isolated from bovine brain and S. purpuratus eggs. J. Cell Biol. 93:797-803.
35. Keller, T. C., III, and L. I. Rebhun. 1982. Strongylocentrotus purpuratus spindle tubulin. I. Characteristics of its polymerization and depolymerization in vitro. J. Cell Biol. 93:788-796.
36. Lacey, E. 1990. Mode of action of benzimidazoles. Parasitol. Today 6:112-115.
37. Lacey, E., and R. K. Prichard. 1986. Interactions of benzimidazoles (BZ) with tubulin from BZ-sensitive and BZ-resistant isolates of Haemonchus contortus. Mol. Biochem. Parasitol. 19:171-181.
38. Leander, B. S., and P. J. Keeling. 2003. Morphostasis in alveolate evolution. Trends Ecol. Evol. 18:395-402.
39. Lewis, S. A., M. E. Gilmartin, J. L. Hall, and N. J. Cowan. 1985. Three expressed sequences within the human beta-tubulin multigene family each define a distinct isotype. J. Mol. Biol. 182:11-20.
40. Lewis, S. A., W. Gu, and N. J. Cowan. 1987. Free intermingling of mammalian beta-tubulin isotypes among functionally distinct microtubules. Cell 49: 539-548.
41. Lewis, S. A., M. G. Lee, and N. J. Cowan. 1985. Five mouse tubulin isotypes and their regulated expression during development. J. Cell Biol. 101:852-861.
42. Li, H., D. J. DeRosier, W. V. Nicholson, E. Nogales, and K. H. Downing. 2002. Microtubule structure at 8 Å resolution. Structure 10:1317-1328.
43. Liao, G., and G. G. Gundersen. 1998. Kinesin is a candidate for crossbridging microtubules and intermediate filaments. Selective binding of kinesin to detyrosinated tubulin and vimentin. J. Biol. Chem. 273:9797-9803.
44. Lowe, J., H. Li, K. H. Downing, and E. Nogales. 2001. Refined structure of alpha beta-tubulin at 3.5 Å resolution. J. Mol. Biol. 313:1045-1057.
45. Ma, C., C. Li, L. Ganesan, J. Oak, S. Tsai, D. Sept, and N. S. Morrissette. 2007. Mutations in alpha-tubulin confer dinitroaniline resistance at a cost to microtubule function. Mol. Biol. Cell 18:4711-4720.
46. Ma, C., J. Tran, C. Li, L. Ganesan, D. Wood, and N. Morrissette. 2008. Secondary mutations correct fitness defects in Toxoplasma gondii with dinitroaniline resistance mutations. Genetics 180:845-856.
47. McGrath, K. E., S. M. Yu, D. P. Heruth, A. A. Kelly, and M. A. Gorovsky. 1994. Regulation and evolution of the single alpha-tubulin gene of the ciliate Tetrahymena thermophila. Cell Motil. Cytoskel. 27:272-283.
48. Mitra, A., and D. Sept. 2006. Binding and interaction of dinitroanilines with apicomplexan and kinetoplastid alpha-tubulin. J. Med. Chem. 49:5226-5231.
49. Morejohn, L. C., T. E. Bureau, J. Mole-Bajer, A. S. Bajer, and D. E. Fosket. 1987. Oryzalin, a dinitroaniline herbicide, binds to plant tubulin and inhibits microtubule polymerization in vitro. Planta 172:252-264.
50. Morgan, R. E., and K. A. Werbovetz. 2008. Selective lead compounds against kinetoplastid tubulin. Adv. Exp. Med. Biol. 625:33-47.
51. Morrissette, N. S., V. Bedian, P. Webster, and D. S. Roos. 1994. Characterization of extreme apical antigens from Toxoplasma gondii. Exp. Parasitol. 79:445-459.
52. Morrissette, N. S., A. Mitra, D. Sept, and L. D. Sibley. 2004. Dinitroanilines bind alpha-tubulin to disrupt microtubules. Mol. Biol. Cell 15:1960-1968.
53. Morrissette, N. S., and D. Sept. 2008. Dinitroaniline interactions with tubulin: genetic and computational approaches to define the mechanisms of action and resistance, p. 327-350. In Y. B. Blume, W. V. Baird, A. I. Yemets, and D. Breviario (ed.), The plant cytoskeleton: a key tool for agro-biotechnology. Springer Dordrecht, New York, NY.
54. Nogales, E., M. Whittaker, R. A. Milligan, and K. H. Downing. 1999. Highresolution model of the microtubule. Cell 96:79-88.
55. Nogales, E., S. G. Wolf, I. A. Khan, R. F. Luduena, and K. H. Downing. 1995. Structure of tubulin at 6.5 Å and location of the taxol-binding site. Nature 375:424-427.
56. Rathinasamy, K., and D. Panda. 2006. Suppression of microtubule dynamics by benomyl decreases tension across kinetochore pairs and induces apoptosis in cancer cells. FEBS J. 273:4114-4128.
57. Ravelli, R. B., B. Gigant, P. A. Curmi, I. Jourdain, S. Lachkar, A. Sobel, and M. Knossow. 2004. Insight into tubulin regulation from a complex with colchicine and a stathmin-like domain. Nature 428:198-202.
58. Reed, N. A., D. Cai, T. L. Blasius, G. T. Jih, E. Meyhofer, J. Gaertig, and K. J. Verhey. 2006. Microtubule acetylation promotes kinesin-1 binding and transport. Curr. Biol. 16:2166-2172.
59. Reijo, R. A., E. M. Cooper, G. J. Beagle, and T. C. Huffaker. 1994. Systematic mutational analysis of the yeast beta-tubulin gene. Mol. Biol. Cell 5:29-43.
60. Richards, K. L., K. R. Anders, E. Nogales, K. Schwartz, K. H. Downing, and D. Botstein. 2000. Structure-function relationships in yeast tubulins. Mol. Biol. Cell 11:1887-1903.
61. Sackett, D. L., K. A. Werbovetz, and N. S. Morrissette. 2010. Isolating tubulin from nonneural sources. Methods Cell Biol. 95:17-32.
62. Savage, C., M. Hamelin, J. G. Culotti, A. Coulson, D. G. Albertson, and M. Chalfie. 1989. mec-7 is a beta-tubulin gene required for the production of 15-protofilament microtubules in Caenorhabditis elegans. Genes Dev. 3:870-881.
63. Schatz, P. J., L. Pillus, P. Grisafi, F. Solomon, and D. Botstein. 1986. Two functional alpha-tubulin genes of the yeast Saccharomyces cerevisiae encode divergent proteins. Mol. Cell. Biol. 6:3711-3721.
64. Schatz, P. J., F. Solomon, and D. Botstein. 1986. Genetically essential and nonessential alpha-tubulin genes specify functionally interchangeable proteins. Mol. Cell. Biol. 6:3722-3733.
65. Sullivan, K. F., and D. W. Cleveland. 1986. Identification of conserved isotype-defining variable region sequences for four vertebrate beta tubulin polypeptide classes. Proc. Natl. Acad. Sci. U. S. A. 83:4327-4331.
66. Thomas, J. H., N. F. Neff, and D. Botstein. 1985. Isolation and characterization of mutations in the beta-tubulin gene of Saccharomyces cerevisiae. Genetics 111:715-734.
67. Ursic, D., J. C. Sedbrook, K. L. Himmel, and M. R. Culbertson. 1994. The essential yeast Tcp1 protein affects actin and microtubules. Mol. Biol. Cell 5:1065-1080.
68. Verhey, K. J., and J. Gaertig. 2007. The tubulin code. Cell Cycle 6:2152-2160.
69. Villasante, A., D. Wang, P. Dobner, P. Dolph, S. A. Lewis, and N. J. Cowan. 1986. Six mouse alpha-tubulin mRNAs encode five distinct isotypes: testisspecific expression of two sister genes. Mol. Cell. Biol. 6:2409-2419.
70. Werbovetz, K. A. 2002. Tubulin as an antiprotozoal drug target. Mini Rev. Med. Chem. 2:519-529.
71. Werbovetz, K. A., J. J. Brendle, and D. L. Sackett. 1999. Purification, characterization, and drug susceptibility of tubulin from Leishmania. Mol. Biochem. Parasitol. 98:53-65.
72. Werbovetz, K. A., D. L. Sackett, D. Delfin, G. Bhattacharya, M. Salem, T. Obrzut, D. Rattendi, and C. Bacchi. 2003. Selective antimicrotubule activity of N1-phenyl-3,5-dinitro-N4, N4-di-n-propylsulfanilamide (GB-II-5) against kinetoplastid parasites. Mol. Pharmacol. 64:1325-1333.
73. Williams, N. E., J. E. Honts, and J. Kaczanowska. 1990. The formation of basal body domains in the membrane skeleton of Tetrahymena. Development 109:935-942.
74. Wloga, D., D. M. Webster, K. Rogowski, M. H. Bre, N. Levilliers, M. Jerka- Dziadosz, C. Janke, S. T. Dougan, and J. Gaertig. 2009. TTLL3 is a tubulin glycine ligase that regulates the assembly of cilia. Dev. Cell 16:867-876.
75. Wolf, N., C. L. Regan, and M. T. Fuller. 1988. Temporal and spatial pattern of differences in microtubule behaviour during Drosophila embryogenesis revealed by distribution of a tubulin isoform. Development 102:311-324.
76. Xia, L., B. Hai, Y. Gao, D. Burnette, R. Thazhath, J. Duan, M. H. Bre, N. Levilliers, M. A. Gorovsky, and J. Gaertig. 2000. Polyglycylation of tubulin is essential and affects cell motility and division in Tetrahymena thermophila. J. Cell Biol. 149:1097-1106.
77. Yaffe, M. B., G. W. Farr, D. Miklos, A. L. Horwich, M. L. Sternlicht, and H. Sternlicht. 1992. TCP1 complex is a molecular chaperone in tubulin biogenesis. Nature 358:245-248.
78. Yakovich, A. J., F. L. Ragone, J. D. Alfonzo, D. L. Sackett, and K. A. Werbovetz. 2006. Leishmania tarentolae: purification and characterization of tubulin and its suitability for antileishmanial drug screening. Exp. Parasitol. 114:289-296.
79. Yamamoto, E., L. Zeng, and W. V. Baird. 1998. Alpha-tubulin missense mutations correlate with antimicrotubule drug resistance in Eleusine indica. Plant Cell 10:297-308.