Biosynthesis and potential functions of the ecdysteroid 20-hydroxyecdysone - A review

Botany

Volumn 86, Issue 9, 2008, Pages 978-987

  Festucci Buselli, Reginaldo A ^a   Contim, Luis A S ^b   Barbosa, Luiz Cláudio A ^a   Stuart, Jeff ^c   Otoni, Wagner C ^a  

^a FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^b UNIVERSIDADE NILTON LINS   (Brazil)

^c PURDUE UNIVERSITY   (United States)

Author keywords

20 hydroxyecdysone (20E); Ecdysone (E); Ecdysteroid (ECD); Pfaffia glomerata (spreng.) pedersen; Phytoecdysteroid (PE); Phytosterol (PS); Zooecdysteroid (ZE)

Indexed keywords

AGROCHEMICAL; BIOCHEMISTRY; BIOTECHNOLOGY; CHEMICAL DEFENSE; HORMONE; MORPHOLOGY; PHYSIOLOGICAL RESPONSE; STEROID;

ARTHROPODA; HEXAPODA; NEMATODA; PFAFFIA GLOMERATA;

EID: 76349124691     PISSN: 19162804     EISSN: None     Source Type: Journal    
DOI: 10.1139/B08-049     Document Type: Review

References (71)

1. Adler, J.H., and Grebenok, R.J. 1995. Biosynthesis and distribution of insect-molting hormones in plants - a review. Lipids, 30: 257-262. doi:10.1007/BF02537830. PMID: 7791535.
2. Adler, J.H., and Grebenok, R.J. 1999. Occurrence, biosynthesis, and putative role of ecdysteroids in plants. Crit. Rev. Biochem. Mol. Biol. 34: 253-264. doi:10.1080/10409239991209282. PMID:10517645.
3. Bandara, B.M.R., Jayasinghe, L., Karunaratne, V., Wannigama, G.P., Bokel, M., Kraus, W., and Sotheeswaran, S. 1989. Ecdysterone from stem of Diploclisia glaucescens. Phytochemistry, 28: 1073-1075. doi:10.1016/0031-9422(89)80185-2.
4. Bathori, M., and Pongracz, Z. 2005. Phytoecdysteroids - from isolation to their effects on humans. Curr. Med. Chem. 12: 153-172. PMID:15638733.
5. Bathori, M., Gergely, A., Kalasz, H., Nagy, G., Dobos, A., and Mathe, I. 2000. Liquid chromatographic monitoring of phytoecdysteroids production of Serratula wolffii. J. Liq. Chromatogr. Relat. Technol. 23: 281-294. doi:10.1081/JLC-100101452.
6. Blackford, M.J.P., and Dinan, L. 1997. The effects of ingested 20-hydroxyecdysone on the larvae of Aglais urticae, Inachisio, Cynthiacardui (Lepidoptera: Nymphalidae) and Tyria jacobaeae (Lepidoptera: Arctiidae). J. Insect Physiol. 43: 315-327. doi:10. 1016/S0022-1910(96)00112-6. PMID: 12769893.
7. Blackford, M.J.P., Clarke, B.S., and Dinan, L. 1997. Distribution and metabolism of exogenous ecdysteroids in the Egyptian cotton leafworm Spodoptera littoralis (Lepidoptera: Noctuidae). Arch. Insect Biochem. Physiol. 34(3): 329-346. doi: < 329::AID-ARCH7 > 3.0.CO;2-P. 10.1002/(SICI)1520-6327(1997)34:3
8. Camps, F., and Coll, J. 1993. Insect allelochemicals from Ajuga plants. Phytochemistry, 32:1361-1370. doi:10.1016/0031-9422(93)85139-I.
9. Chen, J.H., Turner, P.C., and Rees, H.H. 1999. Molecular cloning and characterization of hemolymph 3-dehydroecdysone 3b-reductase from the cotton leafworm, Spodoptera littoralis. A new member of the third superfamily of oxidoreductases. J. Biol. Chem. 274: 10551-10556. doi:10.1074/jbc.274.15.10551. PMID:10187849.
10. Dai, J.D., and Gilbert, L.I. 1997. Programmed cell death of the prothoracic glands of Manduca sexta during pupal-adult meta-morphosis. Insect Biochem. Mol. Biol. 27: 69-78. doi:10.1016/ S0965-1748(96)00068-9. PMID:9061930.
11. Descoins, Jr., C., and Marion-Poll, F. 1999. Electrophysiological responses of gustatory sensilla of Mamestra brassicae (Lepidoptera: Noctuidae) larvae to three ecdysteroids: ecdysone, 20-hydro-xyecdysone and ponasterone A. J. Insect Physiol. 45:871-876. doi:10.1016/S0022-1910(99)00057-8. PMID:12770279.
12. Dinan, L. 1995a. Distribution and levels of phytoecdysteroids within individual plants of the species of the Chenopodiaceae. [Online]. Eur. J. Entomol. 92(1): 295-300. Available from www.eje.cz/pdfarticles/553/eje_092_1_295_Dinan.pdf [accessed 07 December 2007].
13. Dinan, L. 1995b. A strategy for the identification of ecdysteroid receptor agonists and antagonists from plants. [Online]. Eur. J. Entomol. 92(1): 271-283. Available from www.eje.cz/ pdfarticles/552/eje_092_1_271_Dinan.pdf [accessed 07 December 2007]
14. Dinan, L. 1998. A strategy towards the elucidation of the contribution made by phytoecdysteroids to the deterrence of invertebrate predators on plants. Russ. J. Plant Physiol. 45: 296-305.
15. Dinan, L. 2001. Phytoecdysteroids: biological aspects. Phytochemistry, 57: 325-339. doi:10.1016/S0031-9422(01)00078-4. PMID:11393511.
16. Dinan, L., and Lafont, R. 2006. Effects and applications of arthropod steroid hormones (ecdysteroids) in mammals. J. Endocrinol. 191: 1-8. doi:10.1677/joe.1.06900. PMID: 17065383.
17. Dinan, L., Savchenko, T., and Whiting, P. 2001. On the distribution of phytoecdysteroids in plants. Cell. Mol. Life Sci. 58: 1121-1132. doi:10.1007/PL00000926. PMID: 11529504.
18. Entchev, E.V., and Kurzchalia, T.V. 2005. Requirement of sterols in the life cycle of the nematode Caenorhabditis elegans. Semin. Cell Dev. Biol. 16: 175-182. doi:10.1016/j.semcdb.2005.01. 004. PMID:15797828.
19. Feyereisen, R. 1999. Insect P450 enzymes. Annu. Rev. Entomol. 44: 507-533. doi:10.1146/annurev.ento.44.1.507. PMID: 9990722.
20. Gilbert, L.I. 1962. Maintenance of the prothoracic gland by the juvenile hormone in insects. Nature (London), 193: 1205-1207. doi:10.1038/1931205a0.
21. Gilbert, L.I. 2004. Halloween genes encode P450 enzymes that mediate steroid hormone biosynthesis in Drosophila melanogaster. Mol. Cell. Endocrinol. 215: 1-10. doi:10.1016/j.mce.2003. 11.003. PMID:15026169.
22. Gilbert, L.I., Rybczynski, R., and Warren, J.T. 2002. Control and biochemical nature of the ecdysteroidogenic pathway. Annu. Rev. Entomol. 47: 883-916. doi:10.1146/annurev.ento.47. 091201.145302. PMID:11729094.
23. Goodwin, T.W. 1971. Biosynthesis of carotenoids and plant triterpenes. Biochem. J. 123: 293-329. PMID: 4331177.
24. Golovatskaya, I.F. 2004. Effect of ecdysterone on morphological and physiological processes in plants. Russ. J. Plant Physiol. 51: 407-413. doi:10.1023/B:RUPP.0000028689.97402.d5.
25. Grebenok, R.J., and Adler, J.H. 1991. Ecdysteroids distribution during development of spinach. Phytochemistry, 30: 2905-2910. doi:10.1016/S0031-9422(00)98222-0.
26. Grebenok, R.J., and Adler, J.H. 1993. Ecdysteroid biosynthesis during the ontogeny of spinach leaves. Phytochemistry, 33: 341-347. doi:10.1016/0031-9422(93)85514-R.
27. Grebenok, R.J., Ripa, P.V., and Adler, J.H. 1991. Occurrence and levels of ecdysteroids in spinach. Lipids, 26: 666-668. doi:10. 1007/BF02536433.
28. Grebenok, R.J., Venkatachari, S., and Adler, J.H. 1994. Biosynthesis of ecdysone and ecdysone phosphates in spinach. Phytochemistry, 36: 1399-1408. doi:10.1016/S0031-9422(00)89731-9.
29. Ikekawa, N., Morisaki, M., and Fujimoto, Y. 1993. Sterol metabolism in insects: dealkylation of phytosterol to cholesterol. Acc. Chem. Res. 26: 139-146. doi:10.1021/ar00028a002.
30. Kolesnikova, M.D., Xiong, Q., Lodeiro, S., Hua, L., and Matsuda, S.P.T. 2006. Lanosterol biosynthesis in plants. Arch. Biochem. Biophys. 447:87-95. doi:10.1016/j.abb.2005.12.010. PMID: 16445886.
31. Lafont, R. 1997. Ecdysteroids and related molecules in animals and plants. Arch. Insect Biochem. Physiol. 35(1-2): 3-20. doi:10.1002/(SICI)1520-6327(1997)35:1/2<3::AID-ARCH2>3.0. CO;2-X.
32. Lafont, R., and Dinan, L. 2003. Practical uses for ecdysteroids in mammals including humans: an update. J. Insect Sci. 3: 1-30. PMID:15841218.
33. Lafont, R., and Koolman, J. 1984. Ecdysone metabolism. In Bio-synthesis, metabolism and mode of action of invertebrate hormones. Edited by J. Hoffmann and M. Porchet. Springer-Verlag, Berlin, Germany. pp. 196-226.
34. Lafont, R., Harmatha, J., Marion-Poll, F., Dinan, L., and Wilson, I.D. 2002. The Ecdysone handbook. 3rd ed. [Online]. Available from ecdybase.org [accessed 07 December 2007].
35. Lorenzi, H., and Matos, F.J.A. 2002. Plantas medicinais no Brasil, nativas e exóticas. Instituto Plantarum de Estudos da Flora LTDA, São Paulo, Brazil. pp. 45-46.
36. Machackova, I., Vagner, M., and Slama, K. 1995. Comparison between the effects of 20-hydroxyecdysone and phytohormones on growth and development in plants. [Online]. Eur. J. Entomol. 92(1): 309-316. Available from www.eje.cz/pdfarticles/565/eje_092_1_309_Machac.pdf [accessed 07 December 2007].
37. Makka, T., Seino, A., Tomita, S., Fujuwara, H., and Sonobe, H. 2002. A possible role of 20-hydroxyecdysone in embryonic development of the silkworm Bombyx mori. Arch. Insect Biochem. Physiol. 51: 111-120. [PMID: 12386839.] doi:10.1002/arch.10055. PMID:12386839.
38. Marion-Poll, F., and Descoins, C. 2002. Taste detection of phytoecdysteroids in larvae of Bombyx mori, Spodoptera littoralis and Ostrinia nubilalis. J. Insect Physiol. 48: 467-476. doi:10.1016/S0022-1910(02)00068-9. PMID: 12770096.
39. Mondy, N., Caïssa, C., Pitoizet, N., Delbecque, J.P., and Corio-Costet, M.F. 1997. Effects of the ingestion of Serratula tinctoria extracts, a plant containing phytoecdysteroids, on the development of the vineyard pest Lobesia botrana (Lepidoptera: Tortricidae). Arch. Insect Biochem. Physiol. 35(1-2): 227-235. doi:10.1002/(SICI)1520-6327(1997)35:1/2.
40. Niwa, R., Matsuda, T., Yoshiyama, T., Namiki, T., Mita, K., Fujimoto, Y., and Kataoka, H. 2004. CYP306A1, a cytochrome P450 enzyme, is essential for ecdysteroid biosynthesis in the prothoracic glands of Bombyx and Drosophila. J. Biol. Chem. 279: 35942-35949. doi:10.1074/jbc.M404514200. PMID: 15197185.
41. Okuzumi, K., Hara, N., Fujimoto, Y., Yamada, J., Nakamura, A., Takahashi, K., and Morisaki, M. 2003. Biosynthesis of phytoec-dysteroids in Ajuga hairy roots:clerosterol as a precursor of cyasterone, isocyasterone and 29-norcyasterone. Tetrahedron Lett. 44: 323-326. doi:10.1016/S0040-4039(02)02565-0.
42. Petryk, A., Warren, J.T., Marques, G., Jarcho, M.P., Gilbert, L.I., Kahler, J., Parvy, J.P., Li, Y., Dauphin-Villemant, C., and O'Connor, M.B. 2003. Shade is the Drosophila P450 enzyme that mediates the hydroxylation of ecdysone to the steroid insect molting hormone 20-hydroxyecdysone. Proc. Natl. Acad. Sci. U.S.A. 100: 13773-13778. doi:10.1073/pnas.2336088100. PMID:14610274.
43. Ramadan, M.F., Zayed, R., and El-Shamy, H. 2007. Screening of bioactive lipids and radical scavenging potential of some solanaceae plants. Food Chem. 103: 885-890. doi:10.1016/j.foodchem. 2006.09.040.
44. Rewitz, K.F., O'Connor, M.B., and Gilbert, L.I. 2007. Molecular evolution of the insect Halloween family of cytochrome P450s: Phylogeny, gene organization and functional conservation. Insect Biochem. Mol. Biol. 37: 741-753. doi:10.1016/j.ibmb.2007. 02.012. PMID:17628274.
45. Rharrabe, K., Alla, S., Maria, A., Sayah, F., and Lafont, R. 2007. Diversity of detoxification pathways of ingested ecdysteroids among phytophagous insects. Arch. Insect Biochem. Physiol. 65: 65-73. doi:10.1002/arch.20191. PMID: 17523174.
46. Savolainen, V., Wuest, J., Lafont, R., and Connat, J.L. 1995. Effects of ingested phytoecdysteroids in the female soft tick Ornithodoros moubata. Experientia, 51: 596-600. doi:0.1007/BF02128751. PMID:7607304.
47. Sawai, S., Akashi, T., Sakurai, N., Suzuki, H., Shibata, D., Ayabe, S., and Aoki, T. 2006. Plant lanosterol synthase: divergence of the sterol and triterpene biosynthetic pathways in eukaryotes. Plant Cell Physiol. 47: 673-677. doi:10.1093/pcp/pcj032.PMID:16531457.
48. Schaller, H. 2003. The role of sterol in plant growth and development. Prog. Lipid Res. 42:163-175. doi:10.1016/S0163-7827(02)00047-4. PMID:12689617.
49. Schaller, H. 2004. New aspects of sterol biosynthesis in growth and development of higher plants. Plant Physiol. Biochem. 42: 465-476. doi:10.1016/j.plaphy.2004.05.012. PMID:15246059.
50. Schaeffer, A., Bronner, R., Benveniste, P., and Schaller, H. 2001. The ratio of campesterol to sitosterol which modulates growth in Arabidopsis is controlled by sterol methyltransferase 2-1. Plant J. 25:605-615. doi:10.1046/j.1365-313x.2001.00994.x. PMID:11319028.
51. Schmelz, E.A., Grebenok, R.J., Galbraith, D.W., and Bowers, W.S. 1998. Damage-induced accumulation of phytoecdysteroids in spinach: A rapid root response involving the octadecanoic acid pathway. J. Chem. Ecol. 24: 339-360. doi:10.1023/A:1022588610232.
52. Schmelz, E.A., Grebenok, R.J., Galbraith, D.W., and Bowers, W.S. 1999. Insect-induced synthesis of phytoecdysteroids in spinach, Spinacia oleracea. J. Chem. Ecol. 25: 1739-1757. doi:10.1023/ A:1020969413567.
53. Schmelz, E.A., Grebenok, R.J., Ohnmeiss, T.E., and Bowers, W.S. 2000. Phytoecdysteroid turnover in spinach: Long-term stability supports a plant defense hypothesis. J. Chem. Ecol. 26: 2883-2896. doi:10.1023/A:1026454213510.
54. Schmelz, E.A., Grebenok, R.J., Ohnmeiss, T.E., and Bowers, W.S. 2002. Interactions between Spinacia oleracea and Bradysia impatiens: a role for phytoecdysteroids. Arch. Insect Biochem. Physiol. 51: 204-221. doi:10.1002/arch.10062. PMID:12432520.
55. Shiobara, Y., Inoue, S., Kato, K., Nishiguchi, Y., Oishi, Y., Nishimoto, N., De Oliveira, F., Akisue, G., Akisue, M.K., and Hashimot, G. 1993. A nortriterpenoid, triterpenoids and ecdysteroids from Pfaffia glomerata. Phytochemistry, 32: 1527-1530. doi:10.1016/0031-9422(93)85172-N.
56. Skliar, M., Curino, A., Milanesi, L., Benassati, S., and Boland, R. 2000. Nicotiana glauca: another plant species containing vitamin D3 metabolites. Plant Sci. 156: 193-199. doi:10.1016/S0168-9452(00)00254-5. PMID:10936526.
57. Slama, K. 1993. Ecdysteroids: insect hormones, plant defensive factors, or human medicine? Phytoparasitica, 21: 3-8.
58. Slama, K., and Lafont, R. 1995. Insect hormones - ecdysteroids: their presence and actions in vertebrates. [Online]. Eur. J. Entomol. 92(1): 355-377. Available from www.eje.cz/ pdfarticles/576/eje_092_1_355_Slama.pdf [accessed 07 December 2007].
59. Soriano, I.R., Riley, I.T., Potter, M.J., and Bowers, W.S. 2004. Phytoecdysteroids: a novel defense against plant-parasitic nematodes. J. Chem. Ecol. 30: 1885-1899. doi:10.1023/B:JOEC. 0000045584.56515.11. PMID:15609826.
60. Suzuki, M., and Muranaka, T. 2007. Molecular genetics of plant sterol backbone synthesis. Lipids, 42: 47-54. doi:10.1007/s11745-006-1000-5. PMID:17393210.
61. Takeuchi, H., Chen, J.H., O'Reilly, D.R., Rees, H.H., and Turner, P.C. 2000. Regulation of ecdysteroid signaling: molecular cloning, characterization and expression of 3-dehydroecdysone 3a-reductase, a novel eukaryotic member of the short-chain dehydrogenases/reductases superfamily from the cotton leaf-worm, Spodoptera littoralis. Biochem. J. 349: 239-245. doi:10. 1042/0264-6021:3490239. PMID:10861234.
62. Takeuchi, H., Chen, J.H., O'Reilly, D.R., Turner, P.C., and Rees, H.H. 2001. Regulation of ecdysteroid signaling: cloning and characterization of ecdysone oxidase: a novel steroid oxidase from the cotton leafworm, Spodoptera littoralis. J. Biol. Chem. 276: 26819-26828. doi:10.1074/jbc.M104291200. PMID:11373299.
63. Takeuchi, H., Rigden, D.J., Ebrahimi, B., Turner, P.C., and Rees, H.H. 2005. Regulation of ecdysteroid signalling during Drosophila development: identification, characterization and model-ling of ecdysone oxidase, an enzyme involved in control of ligand concentration. Biochem. J. 389: 637-645. PMID:15813704.
64. Tanaka, Y., and Takeda, S. 1993. Ecdysone and 20-hydroxyecdysone supplements to the diet affect larval development in the silkworm, Bombyx mori, differently. J. Insect Physiol. 39: 805-809. doi:10. 1016/0022-1910(93)90111-4.
65. Thummel, C.S. 2001. Molecular mechanisms of developmental timing in C. elegans and Drosophila. Dev. Cell, 1: 453-465. doi:10.1016/S1534-5807(01)00060-0. PMID: 11703937.
66. Warren, J.T., and Hetru, C. 1990. Ecdysone biosynthesis: path-ways, enzymes and the early steps problem. Invertebr. Reprod. Dev. 18: 91-99.
67. Warren, J.T., Petryk, A., Marques, G., Jarcho, M., Parvy, J., Dauphin-Villemant, C., O'Connor, M., and Gilbert, L.I. 2002. Molecular and biological characterization of two P450 enzymes in the ecdysteroidogenic pathway of Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 99: 11043-11048. doi:10.1073/ pnas.162375799. PMID:12177427.
68. Warren, J.T., Petryk, A., Marques, G., Parvy, J.P., Shinoda, T., Itoyama, K., Kobayashi, J., Jarcho, M., Li, Y., O'Connor, M.B., Dauphin-Villemant, C., and Gilbert, L.I. 2004. Phantom encodes the 25-hydroxylase of Drosophila melanogaster and Bombyx mori: a P450 enzyme critical in ecdysone biosynthesis. Insect Biochem. Mol. Biol. 34: 991-1010. doi:10.1016/j.ibmb.2004.06. 009. PMID:15350618.
69. Warren, J.T., Yerushalmi, Y., Shimell, M.J., O'Connor, M.B., Restifo, L.L., and Gilbert, L.I. 2006. Discrete pulses of molting hormone, 20-hydroxyecdysone, during late larval development of Drosophila melanogaster: correlations with changes in gene activity. Dev. Dyn. 235: 315-326. doi:10.1002/dvdy.20626. PMID:16273522.
70. Werck-Reichhart, D., and Feyereisen, R 2000. Cytochromes P450: a success story. Genome Biol. 1(6): Reviews3003.1-Reviews3003.9. doi:10.1186/gb-2000-1-6-reviews3003.
71. Zhang, M.L., and Kubo, I. 1993. Metabolic fate of ecdysteroids in larval Bombyx mori and Heliothis virescens. Insect Biochem. Mol. Biol. 23: 831-843. doi:10.1016/0965-1748(93)90072-Z.