Prieurianin/endosidin 1 is an actin-stabilizing small molecule identified from a chemical genetic screen for circadian clock effectors in Arabidopsis thaliana

Plant Journal

Volumn 71, Issue 2, 2012, Pages 338-352

  Tõth, Réka ^a   Gerding Reimers, Claas ^b   Deeks, Michael J ^c   Menninger, Sascha ^b,e   Gallegos, Rafael M ^a   Tonaco, Isabella A N ^a   Hübel, Katja ^b   Hussey, Patrick J ^c   Waldmann, Herbert ^b,d   Coupland, George ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^b TU DORTMUND UNIVERSITY   (Germany)

^c DURHAM UNIVERSITY   (United Kingdom)

^d CHEMICAL GENOMICS CENTRE OF THE MAX PLANCK SOCIETY   (Germany)

^e Lead Discovery Center GmbH   (Germany)

Author keywords

actin; Arabidopsis thaliana; chemical genetics; circadian clock; natural product; prieurianin; technical advance; vesicle trafficking

Indexed keywords

ACTIN; ARABIDOPSIS THALIANA; CHEMICAL GENETICS; CIRCADIAN CLOCK; NATURAL PRODUCTS; PRIEURIANIN; TECHNICAL ADVANCES; VESICLE TRAFFICKING;

CLOCKS; DEPOLYMERIZATION;

PROTEINS;

ACTIN; LIMONOID; PRIEURIANIN;

ACTIN FILAMENT; ANIMAL; ARABIDOPSIS; ARTICLE; CELL LINE; CHEMISTRY; CHLOROCEBUS AETHIOPS; CIRCADIAN RHYTHM; CONFOCAL MICROSCOPY; DRUG EFFECT; GENETIC SCREENING; ISOLATION AND PURIFICATION; LIGHT; METABOLISM; MOLECULAR LIBRARY; PLANT GROWTH; RADIATION EXPOSURE; SCANNING ELECTRON MICROSCOPY; SEEDLING; TIME; TRANSGENIC PLANT; TRANSPORT VESICLE; ULTRASTRUCTURE;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; ARABIDOPSIS; CELL LINE; CERCOPITHECUS AETHIOPS; CIRCADIAN CLOCKS; GENETIC TESTING; HYPOCOTYL; LIGHT; LIMONINS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; PLANTS, GENETICALLY MODIFIED; SEEDLING; SMALL MOLECULE LIBRARIES; TIME FACTORS; TRANSPORT VESICLES;

ARABIDOPSIS; ARABIDOPSIS THALIANA; MAMMALIA;

EID: 84864408366     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.04991.x     Document Type: Article

References (53)

1. Abas, L., Benjamins, R., Malenica, N., Paciorek, T., Wisniewska, J., Moulinier-Anzola, J.C., Sieberer, T., Friml, J., and, Luschnig, C., (2006) Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. 8, 249-256. (Pubitemid 43336066)
2. Akiyama, H., and, Kamiguchi, H., (2010) Phosphatidylinositol 3-kinase facilitates microtubule-dependent membrane transport for neuronal growth cone guidance. J. Biol. Chem. 285, 41740-41748.
3. Allingham, J.S., Klenchin, V.A., and, Rayment, I., (2006) Actin-targeting natural products: structures, properties and mechanisms of action. Cell. Mol. Life Sci. 63, 2119-2134. (Pubitemid 44465686)
4. Alvarez, C., and, Sztul, E.S., (1999) Brefeldin A (BFA) disrupts the organization of the microtubule and the actin cytoskeletons. Eur. J. Cell Biol. 78, 1-14. (Pubitemid 29083947)
5. Augustine, R.C., Pattavina, K.A., Tüzel, E., Vidali, L., and, Bezanilla, M., (2011) Actin interacting protein1 and actin depolymerizing factor drive rapid actin dynamics in Physcomitrella patens. Plant Cell, 23, 3696-3710.
6. Baluska, F., Jasik, J., Edelmann, H.G., Salajova, T., and, Volkmann, D., (2001) Latrunculin B-induced plant dwarfism: plant cell elongation is F-actin-dependent. Dev. Biol. 231, 113-124. (Pubitemid 32198391)
7. Bettinger, B.T., Gilbert, D.M., and, Amberg, D.C., (2004) Actin up in the nucleus. Nat. Rev. Mol. Cell Biol. 5, 410-415. (Pubitemid 38579478)
8. Bubb, M.R., Spector, I., Beyer, B.B., and, Fosen, K.M., (2000) Effects of jasplakinolide on the kinetics of actin polymerization. An explanation for certain in vivo observations. J. Biol. Chem. 275, 5163-5170. (Pubitemid 30108919)
9. Bugyi, B., Papp, G., Hild, G., Lorinczy, D., Nevalainen, E.M., Lappalainen, P., Somogyi, B., and, Nyitrai, M., (2006) Formins regulate actin filament flexibility through long range allosteric interactions. J. Biol. Chem. 281, 10727-10736. (Pubitemid 43855494)
10. de Montaigu, A., Toth, R., and, Coupland, G., (2010) Plant development goes like clockwork. Trends Genet. 26, 296-306.
11. Dhonukshe, P., Grigoriev, I., Fischer, R., et al. (2008) Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Proc. Natl Acad. Sci. USA, 105, 4489-4494. (Pubitemid 351754407)
12. Dodd, A.N., Salathia, N., Hall, A., Kevei, E., Toth, R., Nagy, F., Hibberd, J.M., Millar, A.J., and, Webb, A.A., (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science, 309, 630-633. (Pubitemid 41033650)
13. Doherty, C.J., and, Kay, S.A., (2010) Circadian control of global gene expression patterns. Annu. Rev. Genet. 44, 419-444.
14. Fenteany, G., and, Zhu, S., (2003) Small-molecule inhibitors of actin dynamics and cell motility. Curr. Top. Med. Chem. 3, 593-616.
15. Geldner, N., Friml, J., Stierhof, Y.D., Jurgens, G., and, Palme, K., (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature, 413, 425-428. (Pubitemid 32928597)
16. Geldner, N., Anders, N., Wolters, H., Keicher, J., Kornberger, W., Muller, P., Delbarre, A., Ueda, T., Nakano, A., and, Jurgens, G., (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell, 112, 219-230. (Pubitemid 36144111)
17. Geldner, N., Hyman, D.L., Wang, X., Schumacher, K., and, Chory, J., (2007) Endosomal signaling of plant steroid receptor kinase BRI1. Genes Dev. 21, 1598-1602. (Pubitemid 47026363)
18. Grebe, M., Xu, J., Mobius, W., Ueda, T., Nakano, A., Geuze, H.J., Rook, M.B., and, Scheres, B., (2003) Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Curr. Biol. 13, 1378-1387. (Pubitemid 37029427)
19. Gullo, V.P., Moiura, I., Nakanishi, K., Cameron, F.A., Conolly, J.D., Duncanson, F.D., Harding, A.E., McCridle, R., and, Taylor, D.A.H., (1975) Structure of prieurianin, a complex tetranorterpenoid nuclear magnetic resonance analysis at nonambient temperatures and x-ray structure determination. J. Chem. Soc., Chem. Commun. 1975, 345-346.
20. Gutierrez, R.A., Stokes, T.L., Thum, K., et al. (2008) Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. Proc. Natl. Acad. Sci. USA, 105, 4939-4944. (Pubitemid 351753850)
21. Hanano, S., Domagalska, M.A., Nagy, F., and, Davis, S.J., (2006) Multiple phytohormones influence distinct parameters of the plant circadian clock. Genes Cells, 11, 1381-1392. (Pubitemid 44780523)
22. Hawes, C., and, Satiat-Jeunemaitre, B., (2001) Electron microscopy. In: Hawes, C., Satiat-Jeunemaitre, B., editors. Plant cell biology: a practical approach. Oxford: Oxford University Press. pp. 235-266.
23. Hehnly, H., and, Stamnes, M., (2007) Regulating cytoskeleton-based vesicle motility. FEBS Lett. 581, 2112-2118. (Pubitemid 46709903)
24. Henty, J.L., Bledsoe, S.W., Khurana, P., Meagher, R.B., Day, B., Blanchoin, L., and, Staiger, C.J., (2011) Arabidopsis actin depolymerising factor4 modulates the stochastic dynamic behaviour of actin filaments in the cortical array of epidermis cells. Plant Cell, 23, 3711-3726.
25. Hicks, G.R., and, Raikhel, N.V., (2009) Opportunities and challenges in plant chemical biology. Nat. Chem. Biol. 5, 268-272.
26. Hirota, T., Lewis, W.G., Liu, A.C., Lee, J.W., Schultz, P.G., and, Kay, S.A., (2008) A chemical biology approach reveals period shortening of the mammalian circadian clock by specific inhibition of GSK-3β. Proc. Natl Acad. Sci. USA, 105, 20746-20751.
27. Hirota, T., Lee, J.W., Lewis, W.G., et al. (2010) High-throughput chemical screen identifies a novel potent modulator of cellular circadian rhythms and reveals CKIα as a clock regulatory kinase. PLoS Biol. 8, e1000559.
28. Hussey, P.J., Ketelaar, T., and, Deeks, M.J., (2006) Control of the actin cytoskeleton in plant cell growth. Annu. Rev. Plant Biol. 57, 109-125. (Pubitemid 44061020)
29. Kim, H., Park, M., Kim, S.J., and, Hwang, I., (2005) Actin filaments play a critical role in vacuolar trafficking at the Golgi complex in plant cells. Plant Cell, 17, 888-902. (Pubitemid 43138228)
30. Koul, O., Daniewski, W.M., Multani, J.S., Gumulka, M., and, Singh, G., (2003) Antifeedant effects of the limonoids from Entandrophragma candolei (Meliaceae) on the gram pod borer, Helicoverpa armigera (Lepidoptera: Noctuidae). J. Agric. Food Chem. 51, 7271-7275.
31. Lee, Y.J., Szumlanski, A., Nielsen, E., and, Yang, Z., (2008) Rho-GTPase-dependent filamentous actin dynamics coordinate vesicle targeting and exocytosis during tip growth. J. Cell Biol. 181, 1155-1168. (Pubitemid 351915489)
32. Lumba, S., Cutler, S., and, McCourt, P., (2010) Plant nuclear hormone receptors: a role for small molecules in protein-protein interactions. Annu. Rev. Cell Dev. Biol. 26, 445-469.
33. Mas, P., (2008) Circadian clock function in Arabidopsis thaliana: time beyond transcription. Trends Cell Biol. 18, 273-281.
34. Mathur, J., and, Hulskamp, M., (2002) Microtubules and microfilaments in cell morphogenesis in higher plants. Curr. Biol. 12, R669-R676. (Pubitemid 35161915)
35. McCullough, B.R., Blanchoin, L., Martiel, J.L., and, De la Cruz, E.M., (2008) Cofilin increases the bending flexibility of actin filaments: implications for severing and cell mechanics. J. Mol. Biol. 381, 550-558.
36. O'Neill, J.S., van Ooijen, G., Dixon, L.E., Troein, C., Corellou, F., Bouget, F.Y., Reddy, A.B., and, Millar, A.J., (2011) Circadian rhythms persist without transcription in a eukaryote. Nature, 469, 554-558.
37. Ou, G.S., Chen, Z.L., and, Yuan, M., (2002) Jasplakinolide reversibly disrupts actin filaments in suspension-cultured tobacco BY-2 cells. Protoplasma, 219, 168-175. (Pubitemid 34592966)
38. Panda, S., Poirier, G.G., and, Kay, S.A., (2002) tej defines a role for poly(ADP-ribosyl)ation in establishing period length of the Arabidopsis circadian oscillator. Dev. Cell, 3, 51-61. (Pubitemid 34778395)
39. Percipalle, P., and, Visa, N., (2006) Molecular functions of nuclear actin in transcription. J. Cell Biol. 172, 967-971.
40. Plautz, J.D., Straume, M., Stanewsky, R., Jamison, C.F., Brandes, C., Dowse, H.B., Hall, J.C., and, Kay, S.A., (1997) Quantitative analysis of Drosophila period gene transcription in living animals. Journal of Biological Rhythms 12, 204-217. (Pubitemid 127477078)
41. Rahman, A., Bannigan, A., Sulaman, W., Pechter, P., Blancaflor, E.B., and, Baskin, T.I., (2007) Auxin, actin and growth of the Arabidopsis thaliana primary root. Plant J. 50, 514-528. (Pubitemid 46634491)
42. Robert, S., Chary, S.N., Drakakaki, G., Li, S., Yang, Z., Raikhel, N.V., and, Hicks, G.R., (2008) Endosidin1 defines a compartment involved in endocytosis of the brassinosteroid receptor BRI1 and the auxin transporters PIN2 and AUX1. Proc. Natl. Acad. Sci. USA, 105, 8464-8469. (Pubitemid 351904779)
43. Roy, A., and, Saraf, S., (2006) Limonoids: overview of significant bioactive triterpenes distributed in plants kingdom. Biol. Pharm. Bull. 29, 191-201. (Pubitemid 43200882)
44. Sarker, S.D., Savchenko, T., Whiting, P., Sik, V., and, Dinan, L., (1997) Two limonoids from Turraea obtusifolia (Meliaceae), prieurianin and rohitukin, antagonise 20-hydroxyecdysone action in a Drosophila cell line. Arch. Insect Biochem. Physiol. 35, 211-217. (Pubitemid 127705627)
45. Sawitzky, H., Liebe, S., Willingale-Theune, J., and, Menzel, D., (1999) The anti-proliferative agent jasplakinolide rearranges the actin cytoskeleton of plant cells. Eur. J. Cell Biol. 78, 424-433. (Pubitemid 29317379)
46. Shin, H., Shin, H.S., Guo, Z., Blancaflor, E.B., Masson, P.H., and, Chen, R., (2005) Complex regulation of Arabidopsis AGR1/PIN2-mediated root gravitropic response and basipetal auxin transport by cantharidin-sensitive protein phosphatases. Plant J. 42, 188-200. (Pubitemid 40589382)
47. Sieberer, T., Seifert, G.J., Hauser, M.T., Grisafi, P., Fink, G.R., and, Luschnig, C., (2000) Post-transcriptional control of the Arabidopsis auxin efflux carrier EIR1 requires AXR1. Curr. Biol. 10, 1595-1598. (Pubitemid 32062662)
48. Smertenko, A.P., Deeks, M.J., and, Hussey, P.J., (2010) Strategies of actin reorganisation in plant cells. J. Cell Sci. 123, 3019-3028.
49. Sorek, N., Gutman, O., Bar, E., et al. (2011) Differential effects of prenylation and S-acylation on type I and II ROPS membrane interaction and function. Plant Physiol. 155, 706-720.
50. Staiger, C.J., Sheahan, M.B., Khurana, P., Wang, X., McCurdy, D.W., and, Blanchoin, L., (2009) Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. J. Cell Biol. 184, 269-280.
51. Sweeney, B.M., (1974) The potassium content of Gonyaulax polyedra and phase changes in the circadian rhythm of stimulated bioluminescence by short exposures to ethanol and valinomycin. Plant Physiol. 53, 337-342.
52. Thoenes, L., and, Gunther, M., (2008) Novel approaches in anti-angiogenic treatment targeting endothelial F-actin: a new anti-angiogenic strategy? Curr. Opin. Mol. Ther. 10, 579-590.
53. Toth, R., and, van der Hoorn, R.A., (2010) Emerging principles in plant chemical genetics. Trends Plant Sci. 15, 81-88.