Cellular and molecular actions of dinitroaniline and phosphorothioamidate herbicides on Plasmodium falciparum: Tubulin as a specific antimalarial target

Molecular and Biochemical Parasitology

Volumn 145, Issue 2, 2006, Pages 226-238

  Fennell, Brian J ^a   Naughton, Julie Ann ^a   Dempsey, Enda ^a   Bell, Angus ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Dinitroaniline; Malaria; Microtubule; Phosphorothioamidate; Plasmodium; Tubulin

Indexed keywords

AMIPROFOS METHYL; ANTIMALARIAL AGENT; DINITROANILINE; HERBICIDE; ORYZALIN; PHOSPHOROTHIOAMIDATE; TRIFLURALIN; TUBULIN; UNCLASSIFIED DRUG;

ANTIMALARIAL ACTIVITY; ARTICLE; BINDING SITE; CONTROLLED STUDY; COW; ISOTOPE LABELING; MICROTUBULE; MITOSIS; NONHUMAN; PARASITE DEVELOPMENT; PLANT CELL; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL;

ANILINE COMPOUNDS; ANIMALS; ANTIMALARIALS; DINITROBENZENES; HERBICIDES; IMMUNOHISTOCHEMISTRY; L-LACTATE DEHYDROGENASE; MICROSCOPY, FLUORESCENCE; MOLECULAR STRUCTURE; NITROBENZENES; ORGANOTHIOPHOSPHORUS COMPOUNDS; PARASITIC SENSITIVITY TESTS; PLASMODIUM FALCIPARUM; RADIOLIGAND ASSAY; SULFANILAMIDES; TRIFLURALIN; TUBULIN; TUBULIN MODULATORS;

BOVINAE; MAMMALIA; PLASMODIUM FALCIPARUM;

EID: 30544439248     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2005.08.020     Document Type: Article

References (55)

1. K.A. Werbovetz Tubulin as an antiprotozoal drug target Mini Rev Med Chem 2 2002 519 529
2. A. Bell Microtubule inhibitors as potential antimalarial agents Parasitol Today 14 1998 234 240
3. V. Sinou, Y. Boulard, P. Grellier, and J. Schrével Host cell and malarial targets for docetaxel (Taxotere™) during the erythrocytic development of Plasmodium falciparum J Eukar Microbiol 45 1998 171 183
4. B.J. Fennell, S. Carolan, G.R. Pettit, and A. Bell Effects of the antimitotic natural product dolastatin 10, and related peptides, on the human malarial parasite Plasmodium falciparum J Antimicrob Chemother 51 2003 833 841
5. J. Schrével, V. Sinou, P. Grellier, F. Frappier, D. Guénard, and P. Potier Interactions between docetaxel (Taxotere) and Plasmodium falciparum-infected erythrocytes Proc Natl Acad Sci USA 91 1994 8472 8476
6. E.A. Usanga, E. O'Brien, and L. Luzzato Mitotic inhibitors arrest the growth of Plasmodium falciaprum FEBS 209 1986 23 27
7. A. Bell, B. Wernli, and R.M. Franklin Effects of microtubule inhibitors on protein synthesis in Plasmodium falciparum Parasitol Res 79 1993 146 152
8. A. Dieckmann-Schuppert, and R.M. Franklin Compounds binding to cytoskeletal proteins are active against Plasmodium falciparum in vitro Cell Biol Int Rep 13 1989 411 418
9. B. Pouvelle, P.J. Farley, C.A. Long, and T.F. Taraschi Taxol arrests the development of blood-stage Plasmodium falciparum in vitro and Plasmodium chabaudi adami in malaria-infected mice J Clin Invest 94 1994 413 417
10. J. Nath, and I. Schneider Anti-malarial effects of the anti-tubulin herbicide trifluralin: studies in Plasmodium falciparum Clin Res 40 1992 331A
11. G.S. Dow, A. Armson, and M.R. Boddy Plasmodium: assessment of the antimalarial potential of trifluralin and related compounds using a rat model of malaria, Rattus norvegicus Exp Parasitol 100 2002 155 160
12. R.E. Fowler, R.E. Fookes, F. Lavin, L.H. Bannister, and G.H. Mitchell Microtubules in Plasmodium falciparum merozoites and their importance for invasion of erythrocytes Parasitology 117 1998 425 433
13. Y.M. Traub-Cseko, J.M. Ramalho-Ortigão, A.P. Dantas, S.L. de Castro, H.S. Barbosa, and K.H. Downing Dinitroaniline herbicides against protozoan parasites: the case of Trypanosoma cruzi Trends Parasitol 17 2001 136 141
14. M.M.-Y. Chan, and D. Fong Inhibition of Leishmanias but not host macrophages by the antitubulin herbicide trifluralin Science 249 1990 924 926
15. Stokkermans TJW, J.D. Schwartzman, K. Keenan, N.S. Morrissette, L.G. Tilney, and D.S. Roos Inhibition of Toxoplasma gondii replication by dinitroaniline herbicides Exp Parasitol 84 1996 355 370
16. K.A. Werbovetz, D.L. Sackett, and D. Delfín Selective antimicrotubule activity of N1-phenyl-3,5-dinitro-N4,N4-di-n-propylsulfanilamide (GB-II-5) against kinetoplastid parasites Mol Pharmacol 64 2003 1325 1333
17. L.C. Morejohn, and D.E. Fosket The biochemistry of compounds with anti-microtubule activity in plant cells Pharmacol Ther 51 1991 217 230
18. J.D. Hugdahl, and L.C. Morejohn Rapid and reversible high-affinity binding of the dinitroaniline herbicide oryzalin to tubulin from Zea mays L Plant Physiol 102 1993 725 740
19. T. Kaidoh, J. Nath, H. Fujioka, V. Okoye, and M. Aikawa Effect and localisation of trifluralin in Plasmodium falciparum gametocytes: an electron microscopic study J Eukar Microbiol 42 1995 61 64
20. M.F. Nankya-Kitaka, G.P. Curley, C.S. Gavigan, A. Bell, and J.P. Dalton Plasmodium chabaudi chabaudi and P. falciparum: inhibition of aminopeptidase and parasite growth by bestatin and nitrobestatin Parasitol Res 8 1998 552 558
21. M.T. Makler, J.M. Ries, and J.A. Williams Parasite lactate dehydrogenase as an assay for Plasmodium falciparum drug sensitivity Am J Trop Med Hyg 48 1993 739 741
22. K. Pattanapanyasat, S. Thaithong, and D.E. Kyle Flow cytometric assessment of hydroxypyridinone iron chelators on in vitro growth of drug-resistant malaria Cytometry 27 1997 84 91
23. A. Zuckerman Harvesting of Plasmodium falciparum with saponin Bull WHO 37 1967 431 436
24. G.W. Lubega, T.G. Geary, R.D. Klein, and R.K. Prichard Expression of cloned β-tubulin genes of Haemonchus contortus in Escherichia coli: interaction of recombinant β-tubulin with native tubulin and mebendazole Mol Biochem Parasitol 62 1993 281 292
25. T. Maniatis, E.F. Fritsch, and J. Sambrook Molecular cloning: a laboratory manual 1982 Cold Spring Harbor Laboratory Press
26. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilising the principle of protein dye binding Anal Biochem 72 1976 248 254
27. F.D. Hess, and D.E. Bayer Binding of the herbicide trifluralin to Chlamydomonas flagellar tubulin J Cell Sci 24 1977 351 360
28. L.C. Morejohn, and D.E. Fosket The biochemistry of compounds with anti-microtubule activity in plant cells Pharmacol Ther 51 1991 217 230
29. J.V. Murthy, H.-H. Kim, V.R. Hanesworth, J.D. Hugdahl, and L.C. Morejohn Competitive inhibition of high-affinity oryzalin binding to plant tubulin by the phosphoric amide herbicide amiprophos-methyl Plant Physiol 105 1994 309 320
30. D.W. Hollomon, J.A. Butters, H. Barker, and L. Hall Fungal β-tubulin, expressed as a fusion protein, binds benzimidazole and phenylcarbamate fungicides Antimicrob Agents Chemother 42 1998 2171 2173
31. S. Linder, M. Schliwa, and E. Kube-Granderath Expression of Reticulomyxa filosa α- and β-tubulins in Escherichia coli yields soluble and partially correctly folded material Gene 212 1998 87 94
32. M.E. Oxberry, T.G. Geary, and R.K. Prichard Assessment of benzimidazole binding to individual recombinant tubulin isotypes from Haemonchus contortus Parasitology 122 2001 683 687
33. M.E. Oxberry, T.G. Geary, C.A. Winterrowd, and R.K. Prichard Individual expression of recombinant α- and β-tubulin from Haemonchus contortus: polymerisation and drug effects Protein Express Purif 21 2001 30 39
34. C. Shah, C.Z.-Q. Xu, J. Vickers, and R. Williams Properties of microtubules assembled from mammalian tubulin synthesised in Escherichia coli Biochemistry 40 2001 4844 4852
35. S. Pucciarelli, C. Miceli, and R. Melki Heterologous expression and folding analysis of a β-tubulin isotype from the Antarctic ciliate Euplotes focardii Eur J Biochem 269 2002 6271 6277
36. L.M. MacDonald, A. Armson, Thompson RCA, and J.A. Reynoldson Characterisation of factors favouring the expression of soluble protozoan tubulin proteins in Escherichia coli Protein Express Purif 29 2003 117 122
37. L.M. MacDonald, A. Armson, R.C.A. Thompson, and J.A. Reynoldson Characterisation of benzimidazole binding with recombinant tubulin from Giardia duodenalis, Encephalitozoon intestinalis, and Cryptosporidium parvum Mol Biochem Parasitol 138 2004 89 96
38. M. Nakazawa, D. Moreira, J. Laurent, H. Le Guyader, Y. Fukami, and K. Ito Biochemical analysis of the interaction between elongation factor 1α and α/β-tubulins from a ciliate, Tetrahymena pyriformis FEBS Lett 453 1999 29 34
39. M. Yoshida, Y. Narusaka, E. Minami, and H. Ishii Expression of Neurospora crassa β-tubulin, target protein of benzimidazole fungicides, in Escherichia coli Pestic Sci 55 1999 362 364
40. R.G. Anthony, and P.J. Hussey Dinitroaniline herbicide resistance and the microtubule cytoskeleton Trends Plant Sci 4 1999 112 116
41. A.S. Bajer, and J. Molé-Bajer Drugs with colchicine-like effects that specifically disassemble plant but not animal microtubules Ann NY Acad Sci 466 1986 767 784
42. L.C. Morejohn, and D.E. Fosket Inhibition of plant microtubule polymerisation in vitro by the phosphoric amide herbicide amiprophos-methyl Science 224 1984 874 876
43. J.R. Ellis, R. Taylor, and P.J. Hussey Molecular modeling indicates that two chemically distinct classes of anti-mitotic herbicide bind to the same receptor site(s) Plant Physiol 105 1994 15 18
44. D.H. Young, and V.T. Lewandowski Covalent binding of the benzamide RH-4032 to tubulin in suspension-cultured tobacco cells and its application in a cell-based competitive-binding assay Plant Physiol 124 2000 115 124
45. F.D. Hess The influence of the herbicide trifluralin on flagellar regeneration in Chlamydomonas Exp Cell Res 119 1979 99 109
46. M.M.-Y. Chan, and D. Fong Inhibition of Leishmanias but not host macrophages by the antitubulin herbicide trifluralin Science 249 1990 924 926
47. E. Nogales, S.G. Wolf, and K.H. Downing Structure of the alpha beta tubulin dimer by electron crystallography Nature 391 1998 199 203
48. N.S. Morrissette, A. Mitra, D. Sept, and L.D. Sibley Dinitroanilines bind α-tubulin to disrupt microtubules Mol Biol Cell 15 2004 1960 1968
49. V.D. Lee, and B. Huang Missense mutations at lysine 350 in β-tubulin confer altered sensitivity to microtubule inhibitors in Chlamydomonas Plant Cell 2 1990 1051 1057
50. Y.B. Blume, N.M. Strashnyuk, A.P. Smertenko, V.G. Solodushko, V.A. Sidorov, and Y.Y. Gleba Alteration of β-tubulin in Nicotiana plumbaginifolia confers resistance to amiprophos-methyl Theor Appl Genet 97 1998 464 472
51. J. Wolff, L. Knipling, H.J. Cahnmann, and G. Palumbo Direct photoaffinity labeling of tubulin with colchicines Proc Natl Acad Sci USA 88 1991 2820 2824
52. A.R. Safa, E. Hamel, and R.L. Felsted Photoaffinity labeling of tubulin subunits with a photoactive analogue of vinblastine Biochemistry 26 1987 97 102
53. G. Nasioulas, K. Grammbitter, R.H. Himes, and H. Ponstingl Interaction of a new photosensitive derivative of vinblastine, NAPAVIN, with tubulin and microtubules in vitro Eur J Biochem 192 1990 69 74
54. B. Gigant, C. Wang, and R. Ravelli Structural basis for the regulation of tubulin by vinblastine Nature 435 2005 519 522
55. R. Ravelli, B. Gigant, and P. Curmi Insight into tubulin regulation from a complex with colchicine and a stathmin-like domain Nature 428 2004 198 202