Production of putative diterpene carboxylic acid intermediates of triptolide in yeast

Molecules

Volumn 22, Issue 6, 2017, Pages

  Forman, Victor ^a,b   Callari, Roberta ^b   Folly, Christophe ^b   Heider, Harald ^b   Hamberger, Bj rn ^c  

^a Evolva A/S   (Denmark)

^b EVOLVA SA   (Switzerland)

^c Michigan State University   (United States)

Author keywords

Dehydroabietadiene; Dehydroabietic acid; Medicinal diterpenes; Miltiradiene; Miltiradienic acid; Nicotiana benthamiana; Saccharomyces cerevisiae; Tripterygium wilfordii; Triptolide

Indexed keywords

ABIETANE DERIVATIVE; CYTOCHROME P450; DEHYDROABIETIC ACID; DITERPENE; EPOXIDE; GLUCOSE; PHENANTHRENE DERIVATIVE; TRIPTOLIDE;

BIOSYNTHESIS; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLIC ENGINEERING; METABOLISM; PHYLOGENY; SACCHAROMYCES CEREVISIAE; SPRUCE; TOBACCO; TRIPTERYGIUM;

BIOSYNTHETIC PATHWAYS; CYTOCHROME P-450 ENZYME SYSTEM; DITERPENES; DITERPENES, ABIETANE; EPOXY COMPOUNDS; GLUCOSE; METABOLIC ENGINEERING; PHENANTHRENES; PHYLOGENY; PICEA; SACCHAROMYCES CEREVISIAE; TOBACCO; TRIPTERYGIUM;

EID: 85021165831     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules22060981     Document Type: Article

References (42)

1. Peters, R.J. Two rings in them all: The labdane-related diterpenoids. Nat. Prod. Rep. 2010, 27, 1521–1530. [CrossRef] [PubMed]
2. Wagh, V.; Patil, P.; Surana, S.; Wagh, K. Forskolin: Upcoming antiglaucoma molecule. J. Postgrad. Med. 2012, 58, 199. [CrossRef] [PubMed]
3. Barrero, A.F.; Alvarez-Manzaneda, E.J.; Altarejos, J.; Salido, S.; Ramos, J.M. Synthesis of Ambroxfi from (-)-sclareol and (+)-cis-abienol. Tetrahedron 1993, 49, 10405–10412. [CrossRef]
4. Zhou, Z.-L.; Yang, Y.-X.; Ding, J.; Li, Y.-C.; Miao, Z.-H. Triptolide: Structural modifications, structure-activity relationships, bioactivities, clinical development and mechanisms. Nat. Prod. Rep. 2012, 29, 457. [CrossRef] [PubMed]
5. Liu, L.; Salnikov, A.V.; Bauer, N.; Aleksandrowicz, E.; Labsch, S.; Nwaeburu, C.; Mattern, J.; Gladkich, J.; Schemmer, P.; Werner, J.; et al. Triptolide reverses hypoxia-induced epithelial-mesenchymal transition and stem-like features in pancreatic cancer by NF-?B downregulation. Int. J. Cancer 2014, 134, 2489–2503. [CrossRef] [PubMed]
6. Yang, S.; Chen, J.; Guo, Z.; Xu, X.-M.; Wang, L.; Pei, X.-F.; Yang, J.; Underhill, C.B.; Zhang, L. Triptolide inhibits the growth and metastasis of solid tumors. Mol. Cancer Ther. 2003, 2, 65–72. [PubMed]
7. Xu, F.; Li, Y.; Li, S.; Ma, Y.; Zhao, N.; Liu, Y.; Qian, N.; Zhao, H.; Li, Y. Complete Freund’s adjuvant-induced acute inflammatory pain could be attenuated by triptolide via inhibiting spinal glia activation in rats. J. Surg. Res. 2014, 188, 174–182. [CrossRef] [PubMed]
8. Cheng, S.; LeBlanc, K.J.; Li, L. Triptolide preserves cognitive function and reduces neuropathology in a mouse model of Alzheimer’s disease. PLoS ONE 2014, 9, e108845. [CrossRef] [PubMed]
9. Brinker, A.M.; Raskin, I. Determination of triptolide in root extracts of Tripterygium wilfordii by solid-phase extraction and reverse-phase high-performance liquid chromatography. J. Chromatogr. A 2005, 1070, 65–70. [CrossRef] [PubMed]
10. Xu, H.; Tang, H.; Feng, H.; Li, Y. Metal-mediate reactions based formal synthesis of triptonide and triptolide. Tetrahedron Lett. 2014, 55, 7118–7120. [CrossRef]
11. Paddon, C.J.; Westfall, P.J.; Pitera, D.J.; Benjamin, K.; Fisher, K.; McPhee, D.; Leavell, M.D.; Tai, A.; Main, A.; Eng, D.; et al. High-level semi-synthetic production of the potent antimalarial artemisinin. Nature 2013, 496, 528–532. [CrossRef] [PubMed]
12. Luo, D.; Callari, R.; Hamberger, B.; Wubshet, S.G.; Nielsen, M.T.; Andersen-Ranberg, J.; Hallstrom, B.M.; Cozzi, F.; Heider, H.; Lindberg Møller, B.; et al. Oxidation and cyclization of casbene in the biosynthesis of Euphorbia factors from mature seeds of Euphorbia lathyris L. Proc. Natl. Acad. Sci. USA 2016. [CrossRef] [PubMed]
13. Pateraki, I.; Andersen-ranberg, J.; Jensen, N.B.; Wubshet, S.G.; Heskes, A.M.; Forman, V.; Hallstrom, B.; Hamberger, B.; Motawia, M.S.; Olsen, C.E.; et al. Total biosynthesis of the cyclic AMP booster forskolin from Coleus forskohlii. Elife 2017, 6, e23001. [CrossRef] [PubMed]
14. Chen, F.; Tholl, D.; Bohlmann, J.; Pichersky, E. The family of terpene synthases in plants: A mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J. 2011, 66, 212–229. [CrossRef] [PubMed]
15. Zerbe, P.; Hamberger, B.; Yuen, M.M.S.; Chiang, A.; Sandhu, H.K.; Madilao, L.L.; Nguyen, A.; Hamberger, B.; Bach, S.S.; Bohlmann, J. Gene discovery of modular diterpene metabolism in nonmodel systems. Plant Physiol. 2013, 162, 1073–1091. [CrossRef] [PubMed]
16. Hamberger, B.; Bak, S. Plant P450s as versatile drivers for evolution of species-specific chemical diversity. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013, 368, 20120426. [CrossRef] [PubMed]
17. Pateraki, I.; Andersen-Ranberg, J.; Hamberger, B.; Heskes, A.M.; Martens, H.J.; Zerbe, P.; Bach, S.S.; Møller, B.L.; Bohlmann, J.; Hamberger, B. Manoyl oxide (13R), the biosynthetic precursor of forskolin, is synthesized in specialized root cork cells in Coleus forskohlii. Plant Physiol. 2014, 164, 1222–1236. [CrossRef] [PubMed]
18. Ro, D.-K.; Arimura, G.-I.; Lau, S.Y.W.; Piers, E.; Bohlmann, J. Loblolly pine abietadienol/abietadienal oxidase PtAO (CYP720B1) is a multifunctional, multisubstrate cytochrome P450 monooxygenase. Proc. Natl. Acad. Sci. USA 2005, 102, 8060–8065. [CrossRef] [PubMed]
19. Zi, J.; Peters, R.J. Characterization of CYP76AH4 clarifies phenolic diterpenoid biosynthesis in the Lamiaceae. Org. Biomol. Chem. 2013, 11, 7650–7652. [CrossRef] [PubMed]
20. Hansen, N.L.; Heskes, A.M.; Hamberger, B.; Olsen, C.E.; Hallstrom, B.M.; Andersen-Ranberg, J.; Hamberger, B. The terpene synthase gene family in Tripterygium wilfordii harbors a labdane-type diterpene synthase among the monoterpene synthase TPS-b subfamily. Plant J. 2017, 89, 429–441. [CrossRef] [PubMed]
21. Brinker, A.M.; Ma, J.; Lipsky, P.E.; Raskin, I. Medicinal chemistry and pharmacology of genus Tripterygium (Celastraceae). Phytochemistry 2007, 68, 732–766. [CrossRef] [PubMed]
22. Kutney, J.P.; Han, K. Studies with plant-cell cultures of the Chinese herbal plant, Tripterygium wilfordii. Isolation and characterization of diterpenes. Recl. Trav. Chim. Pays-Bas 1996, 93, 77–93. [CrossRef]
23. Takaishi, Y.; Warhshi, N.; Tateishi, H.; Kawazoe, K.; Miyagi, K.; Li, K.; Duan, H. Phenolic diterpenes from Tripterygium wilfordii var. regelii. Phytochemistry 1997, 45, 979–984. [CrossRef]
24. van Tamelen, E.E.; Leiden, T.M. Total Synthesis of I-Triptonide and I-Triptolide. J. Am. Chem. Soc. 1982, 104, 1785–1786. [CrossRef]
25. Zhou, B.; Li, X.; Tang, H.; Miao, Z.; Feng, H.; Li, Y. Total synthesis of novel D-ring-modified triptolide analogs: Structure-cytotoxic activity relationship studies on the D-ring of triptolide. Org. Biomol. Chem. 2011, 9, 3176–3179. [CrossRef] [PubMed]
26. Hamberger, B.; Ohnishi, T.; Hamberger, B.; Séguin, A.; Bohlmann, J. Evolution of Diterpene Metabolism: Sitka Spruce CYP720B4 Catalyzes Multiple Oxidations in Resin Acid Biosynthesis of Conifer Defense against Insects. Plant Physiol. 2011, 157, 1677–1695. [CrossRef] [PubMed]
27. Andersen-Ranberg, J.; Kongstad, K.T.; Nielsen, M.T.; Jensen, N.B.; Pateraki, I.; Bach, S.S.; Hamberger, B.; Zerbe, P.; Staerk, D.; Bohlmann, J.; et al. Expanding the landscape of diterpene structural diversity through stereochemically controlled combinatorial biosynthesis. Angew. Chem. Int. Ed. 2016, 55, 2142–2146. [CrossRef] [PubMed]
28. Dai, Z.; Liu, Y.; Huang, L.; Zhang, X. Production of miltiradiene by metabolically engineered Saccharomyces cerevisiae. Biotechnol. Bioeng. 2012, 109, 2845–2853. [CrossRef] [PubMed]
29. Zhou, Y.J.; Gao, W.; Rong, Q.; Jin, G.; Chu, H.; Liu, W.; Yang, W.; Zhu, Z.; Li, G.; Zhu, G.; et al. Modular pathway engineering of diterpenoid synthases and the mevalonic acid pathway for miltiradiene production. J. Am. Chem. Soc. 2012, 134, 3234–3241. [CrossRef] [PubMed]
30. Ignea, C.; Ioannou, E.; Georgantea, P.; Loupassaki, S.; Trikka, F.A.; Kanellis, A.K.; Makris, A.M.; Roussis, V.; Kampranis, S.C. Reconstructing the chemical diversity of labdane-type diterpene biosynthesis in yeast. Metab. Eng. 2015, 28, 91–103. [CrossRef] [PubMed]
31. Gonz, F.J.; Almendros, G.; Martin, F. An evaluation of the differences in the composition of humic acids in soils under oak and pine forest by GC-MS after mild degradation. Plant Soil 1987, 103, 83–88.
32. Lanza, A.M.; Curran, K.A.; Rey, L.G.; Alper, H.S. A condition-specific codon optimization approach for improved heterologous gene expression in Saccharomyces cerevisiae. BMC Syst. Biol. 2014, 8, 33. [CrossRef] [PubMed]
33. Peters, R.J.; Flory, J.E.; Jetter, R.; Ravn, M.M.; Lee, H.J.; Coates, R.M.; Croteau, R.B. Abietadiene synthase from grand fir (Abies grandis): Characterization and mechanism of action of the “pseudomature” recombinant enzyme. Biochemistry 2000, 39, 15592–15602. [CrossRef] [PubMed]
34. Williams, D.C.; Wildung, M.R.; Jin, A.Q.; Dalal, D.; Oliver, J.S.; Coates, R.M.; Croteau, R. Heterologous expression and characterization of a “Pseudomature” form of taxadiene synthase involved in paclitaxel (Taxol) biosynthesis and evaluation of a potential intermediate and inhibitors of the multistep diterpene cyclization reaction. Arch. Biochem. Biophys. 2000, 379, 137–146. [CrossRef] [PubMed]
35. Bruckner, K.; Božić, D.; Manzano, D.; Papaefthimiou, D.; Pateraki, I.; Scheler, U.; Ferrer, A.; de Vos, R.C.H.; Kanellis, A.K.; Tissier, A. Characterization of two genes for the biosynthesis of abietane-type diterpenes in rosemary (Rosmarinus officinalis) glandular trichomes. Phytochemistry 2014, 101, 52–64. [CrossRef] [PubMed]
36. Sepúlveda, B.; Astudillo, L.; Rodríguez, J.A.; Yá ez, T.; Theoduloz, C.; Schmeda-Hirschmann, G. Gastroprotective and cytotoxic effect of dehydroabietic acid derivatives. Pharmacol. Res. 2005, 52, 429–437. [CrossRef] [PubMed]
37. Kang, M.S.; Hirai, S.; Goto, T.; Kuroyanagi, K.; Lee, J.Y.; Uemura, T.; Ezaki, Y.; Takahashi, N.; Kawada, T. Dehydroabietic acid, a phytochemical, acts as ligand for PPARs in macrophages and adipocytes to regulate inflammation. Biochem. Biophys. Res. Commun. 2008, 369, 333–338. [CrossRef] [PubMed]
38. Huang, X.C.; Wang, M.; Pan, Y.M.; Yao, G.Y.; Wang, H.S.; Tian, X.Y.; Qin, J.K.; Zhang, Y. Synthesis and antitumor activities of novel thiourea ?- aminophosphonates from dehydroabietic acid. Eur. J. Med. Chem. 2013, 69, 508–520. [CrossRef] [PubMed]
39. Nour-Eldin, H.H.; Hansen, B.G.; Nørholm, M.H.H.; Jensen, J.K.; Halkier, B.A. Advancing uracil-excision based cloning towards an ideal technique for cloning PCR fragments. Nucleic Acids Res. 2006, 34, e122. [CrossRef] [PubMed]
40. Bach, S.S.; Bassard, J.-É.; Ranberg, J.A.; Møldrup, M.E.; Simonsen, H.T.; Hamberger, B. Plant Isoprenoids. In Plant Isoprenoids, Methods in Molecular Biology; Rodríguez, M., Ed.; Springer: New York, NY, USA, 2014; Volume 1153, pp. 285–299.
41. Partow, S.; Siewers, V.; Bjørn, S.; Nielsen, J.; Maury, J. Characterization of different promoters for designing a new expression vector in Saccharomyces cerevisiae. Yeast 2010, 27, 955–964. [CrossRef] [PubMed]
42. Gietz, R.D.; Woods, R.A. Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 2002, 350, 87–96. [PubMed]