Yellow Twig (Nauclea orientalis) from Thailand: Strictosamide as the Key Alkaloid of This Plant Species
Abstract
:1. Introduction
2. Results
2.1. Structure Elucidation
2.1.1. Compounds 1–5
2.1.2. Compounds 6–8
2.1.3. Compounds 9–13
2.2. DFT Caculations
2.3. Metabolomics Using LC-MS
2.4. Organ Specific Accumulation and Quantification of Strictosamide (1)
2.5. Enzymatic Deglucosylation of Strictosamide (1)
2.6. Gustatory and Feeding Experiments
3. Discussion
3.1. Possible Biosynthetic Pathways
4. Conclusions
5. Experimental
5.1. General Experimental Procedures
5.2. Plant Material
5.3. Extraction and Isolation
5.3.1. Isolation from Leaves
5.3.2. Isolation from Stembark
5.3.3. Isolation from Wood
5.4. Theoretical Calculation
5.5. Enzymatic Deglucosylation
5.6. Quantification of Strictosamide (3)
5.7. Screening of Alkaloids by LC-MS
5.8. Antifeedant Experiments
5.8.1. Gustatory Experiment
5.8.2. Non-Choice Feeding Assay
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Available online: http://www.plantsoftheworldonline.org (accessed on 27 April 2022).
- Liu, Y.P.; Ju, P.K.; Long, J.T.; Lai, L.; Zhao, W.H.; Zhang, C.; Zhang, Z.J.; Fu, Y.H. Cytotoxic indole alkaloids from Nauclea orientalis. Nat. Prod. Res. 2018, 32, 2922–2927. [Google Scholar] [CrossRef] [PubMed]
- Sichaem, J.; Surapinit, S.; Siripong, P.; Khumkratok, S.; Jong-Aramruang, J.; Tip-pyang, S. Two new cytotoxic isomeric indole alkaloids from the roots of Nauclea orientalis. Fitoterapia 2010, 81, 830–833. [Google Scholar] [CrossRef] [PubMed]
- Haudecoeur, R.; Peuchmaur, M.; Peres, B.; Rome, M.; Taiwe, G.S.; Boumendjel, A.; Boucherle, B. Traditional uses, phytochemistry and pharmacological properties of African Nauclea species: A review. J. Ethnopharmacol. 2018, 212, 106–136. [Google Scholar] [CrossRef] [PubMed]
- Boucherle, B.; Haudecoeur, R.; Queiroz, E.F.; De Waard, M.; Wolfender, J.L.; Robins, R.J.; Boumendjel, A. Nauclea latifolia: Biological activity and alkaloid phytochemistry of a West African tree. Nat. Prod. Rep. 2016, 33, 1034–1043. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.P.; Liu, Q.L.; Zhang, X.L.; Niu, H.Y.; Guan, C.Y.; Sun, F.K.; Xu, W.; Fu, Y.H. Bioactive monoterpene indole alkaloids from Nauclea officinalis. Bioorg. Chem. 2019, 83, 1–5. [Google Scholar] [CrossRef]
- Liew, S.Y.; Mukhtar, M.R.; Hadi, A.H.A.; Awang, K.; Mustafa, M.R.; Zaima, K.; Morita, H.; Litaudon, M. Naucline, a new indole alkaloid from the bark of Nauclea officinalis. Molecules 2012, 17, 4028–4036. [Google Scholar] [CrossRef]
- Fan, L.; Huang, X.J.; Fan, C.L.; Li, G.Q.; Wu, Z.L.; Li, S.G.; He, Z.D.; Wang, Y.; Ye, W.C. Two new oxindole alkaloid glycosides from the leaves of Nauclea officinalis. Nat. Prod. Commun. 2015, 10, 2087–2090. [Google Scholar] [CrossRef]
- Fan, L.; Liao, C.H.; Kang, Q.R.; Zheng, K.; Jiang, Y.C.; He, Z.D. Indole alkaloids from the leaves of Nauclea officinalis. Molecules 2016, 21, 968. [Google Scholar] [CrossRef]
- Wang, G.; Hou, L.; Wang, Y.; Liu, H.; Yuan, J.; Hua, H.; Sun, L. Two new neolignans and an indole alkaloid from the stems of Nauclea officinalis and their biological activities. Fitoterapia 2022, 160, 105228. [Google Scholar] [CrossRef]
- Kanchanapoom, T.; Sahakitpichan, P.; Chimnoi, N.; Petchthong, C.; Thamniyom, W.; Nangkoed, P.; Ruchirawat, S. Monoterpene alkaloid glycosides from the leaves of Nauclea orientalis. Phytochem. Lett. 2021, 41, 83–87. [Google Scholar] [CrossRef]
- He, Z.D.; Ma, C.Y.; Zhang, H.J.; Tan, G.T.; Tamez, P.; Sydara, K.; Bouamanivong, S.; Southavong, B.; Soejarto, D.D.; Pezzuto, J.M.; et al. Antimalarial constituents from Nauclea orientalis (L.) L. Chem. Biodivers. 2005, 2, 1378–1386. [Google Scholar] [CrossRef] [PubMed]
- Berger, A.; Valant-Vetschera, K.; Schinnerl, J.; Brecker, L. A revised classification of the sister tribes Palicoureeae and Psychotrieae (Rubiaceae) indicates genus-specific alkaloid accumulation. Phytochem. Rev. 2022, 21, 941–986. [Google Scholar] [CrossRef]
- Berger, A.; Valant-Vetschera, K.; Schinnerl, J.; Brecker, L. Alkaloid diversification in the genus Palicourea (Rubiaceae: Palicoureeae) viewed from a (retro-)biogenetic perspective. Phytochem. Rev. 2022, 21, 915–939. [Google Scholar] [CrossRef]
- Patthy-Lukáts, Á.; Károlyházy, L.; Szabó, L.F.; Podányi, B. First direct and detailed stereochemical analysis of strictosidine. J. Nat. Prod. 1997, 60, 69–75. [Google Scholar] [CrossRef]
- Zhang, Z.Z.; ElSohly, H.N.; Jacob, M.R.; Pasco, D.S.; Walker, L.A.; Clark, A.M. New indole alkaloids from the bark of Nauclea orientalis. J. Nat. Prod. 2001, 64, 1001–1005. [Google Scholar] [CrossRef]
- Itoh, A.; Tanahashi, T.; Nagakura, N. Five tetrahydroisoquinoline-monoterpene glucosides and a tetrahydro-β-carboline-monoterpene glucoside from Alangium lamarckii. J. Nat. Prod. 1995, 58, 1228–1239. [Google Scholar] [CrossRef]
- Kitajima, M.; Yoshida, S.; Yamagata, K.; Nakamura, M.; Takayama, H.; Saito, K.; Seki, H.; Aimi, N. Camptothecin-related alkaloids from hairy roots of Ophiorrhiza pumila. Tetrahedron 2002, 58, 9169–9178. [Google Scholar] [CrossRef]
- Erdelmeier, C.A.J.; Regenass, U.; Rali, T.; Sticher, O. Indole alkaloids with in vitro antiproliferative activity from the ammoniacal extract of Nauclea orientalis. Planta Med. 1992, 58, 43–48. [Google Scholar] [CrossRef]
- Frisch, M.J.; Trucks, G.W.; Schlegel, H.B.; Scuseria, G.E.; Robb, M.A.; Cheeseman, J.R.; Scalmani, G.; Barone, V.; Petersson, G.A.; Nakatsuji, H.; et al. Gaussian 09, Revision B.01; Gaussian, Inc.: Wallingford, CT, USA, 2016. [Google Scholar]
- Kornpointner, C.; Berger, A.; Traxler, F.; Hadžiabdić, A.; Massar, M.; Matek, J.; Brecker, L.; Schinnerl, J. Alkaloid and iridoid glucosides from Palicourea luxurians (Rubiaceae: Palicoureeae) indicate tryptamine and tryptophan iridoid alkaloid formation apart the strictosidine pathway. Phytochemistry 2020, 173, 112296. [Google Scholar] [CrossRef]
- Berger, A.; Tanuhadi, E.; Brecker, L.; Schinnerl, J.; Valant-Vetschera, K. Chemodiversity of tryptamine-derived alkaloids in six Costa Rican Palicourea species (Rubiaceae-Palicoureeae). Phytochemistry 2017, 143, 124–131. [Google Scholar] [CrossRef]
- Berger, A.; Kostyan, M.K.; Klose, S.I.; Gastegger, M.; Lorbeer, E.; Brecker, L.; Schinnerl, J. Loganin and secologanin derived tryptamine-iridoid alkaloids from Palicourea crocea and Palicourea padifolia (Rubiaceae). Phytochemistry 2015, 116, 162–169. [Google Scholar] [CrossRef] [PubMed]
- Petzelbauer, I.; Splechtna, B.; Nidetzky, B. Galactosyl transfer catalyzed by thermostable β-glycosidases from Sulfolobus solfataricus and Pyrococcus furiosus: Kinetic studies of the reactions of galactosylated enzyme intermediates with a range of nucleophiles. J. Biochem. 2001, 130, 341–349. [Google Scholar] [CrossRef] [PubMed]
- Kengen, S.W.M.; Luesink, E.J.; Stams, A.J.M.; Zehnder, A.J.B. Purification and characterization of an extremely thermostable β-glucosidase from the hyperthermophilic archaeon Pyrococcus furiosus. Eur. J. Biochem. 1993, 213, 305–312. [Google Scholar] [CrossRef]
- Brecker, L.; Ribbons, D.W. Biotransformations monitored in situ by proton nuclear magnetic resonance spectroscopy. Trends Biotechnol. 2000, 18, 197–202. [Google Scholar] [CrossRef]
- Peeters, L.; Foubert, K.; Bald’e, M.A.; Tuenter, E.; Matheeussen, A.; van Pelt, N.; Caljon, G.; Hermans, N.; Pieters, L. Antiplasmodial activity of constituents and their metabolites after in vitro gastrointestinal biotransformation of a Nauclea pobeguinii extract. Phytochemistry 2022, 194, 113029. [Google Scholar] [CrossRef] [PubMed]
- Srivastava, R.P.; Proksch, P. Kontakttoxizität und Fraßhemmung von Chromenen aus Asteraceae gegenüber Spodoptera littoralis (Lepidoptera: Noctuidae). Entomol. Gen. 1991, 15, 265–274. [Google Scholar] [CrossRef]
- Glendinning, J.I.; Tarre, M.; Asaoka, K. Contribution of different bitter-sensitive taste cells to feeding inhibition in a caterpillar (Manduca sexta). Behav. Neurosci. 1999, 113, 840–854. [Google Scholar] [CrossRef] [PubMed]
- Sudžuković, N.; Schinnerl, J.; Brecker, L. Phytochemical meanings of tetrahydro-beta-carboline moiety in strictosidine derivatives. Bioorg. Med. Chem. 2016, 24, 588–595. [Google Scholar] [CrossRef]
- Bailey, P.D. Direct proof of the involvement of a spiro intermediate in the Pictet-Spengler reaction. J. Chem. Res. 1987, 202–203. [Google Scholar]
- Au, T.Y.; Cheung, H.T.; Sternhell, S. New corynanthé alkaloids from Strychnos angustiflora. J. Chem. Soc. Perkin Trans. 1 1973, 13–16. [Google Scholar] [CrossRef]
- Meng, Z.Q.; Liu, W.J.; Li, Z.; Lin, Y.W.; Li, M.X.; An, S.Y.; Ding, G.; Wang, Z.Z.; Xiao, W.; Xu, J.Y. Transformation of strictosamide to vincoside lactam by acid catalysis. Chin. J. Nat. Med. 2013, 11, 188–192. [Google Scholar] [CrossRef] [PubMed]
- Nagakura, N.; Rüffer, M.; Zenk, M.H. The biosynthesis of monoterpenoid indole alkaloids from strictosidine. J. Chem. Soc. Perkin Trans. 1 1979, 2308–2312. [Google Scholar] [CrossRef]
- Aimi, N.; Nishimura, M.; Miwa, A.; Hoshino, H.; Sakai, S.-I.; Haginiwa, J. Pumiloside and deoxypumiloside; plausible intermediates of camptothecin biosynthesis. Tetrahedron Lett. 1989, 30, 4991–4994. [Google Scholar] [CrossRef]
- Kröhnke, F.; Zecher, W.; Curtze, J.; Drechsler, D.; Pfleghar, K.; Schnalke, K.E.; Weis, W. Syntheses using the Michael addition of phridinium salts. Angew. Chem. Int. Ed. 1962, 1, 626–632. [Google Scholar] [CrossRef]
- Cai, Y.; Zhu, H.; Alperstein, Z.; Yu, W.; Cherkasov, A.; Zou, H. Strictosidine synthase triggered enantioselective synthesis of N-substituted (S)-3,14,18,19-tetrahydroangustines as novel topoisomerase I inhibitors. ACS Chem. Biol. 2017, 12, 3086–3092. [Google Scholar] [CrossRef]
- Peng, X.; Fu, M.; Ou, J.; Cao, R.; Song, H.; Liu, X.Y.; Qin, Y. Total synthesis of angustine and angustoline. Tetrahedron Lett. 2020, 61, 151757. [Google Scholar] [CrossRef]
- Chen, Z.S.; Tian, Z.H.; Zhang, Y.W.; Feng, X.; Li, Y.L.; Jiang, H.Q. Monoterpene indole alkaloids in Uncaria rhynchophlly (Miq.) Jacks chinensis and their chemotaxonomic significance. Biochem. Syst. Ecol. 2020, 91, 104057. [Google Scholar] [CrossRef]
- Guirimand, G.; Courdavault, V.; Lanoue, A.; Mahroug, S.; Guihur, A.; Blanc, N.; Giglioli-Guivarc’h, N.; St-Pierre, B.; Burlat, V. Strictosidine activation in Apocynaceae: Towards a “nuclear time bomb?”. BMC Plant Biol. 2010, 10, 182. [Google Scholar] [CrossRef]
Amount [µg mm−2] | Caffeine | d-Salicine | Aristolochic Acid | Strictosamide (1) |
---|---|---|---|---|
1.13 | 14 | 34 | 12 | 34 |
0.75 | 30 | 44 | 23 | 43 |
0.38 | 41 | 94 | -- | 44 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Songoen, W.; Brunmair, J.; Traxler, F.; Wieser, V.C.; Phanchai, W.; Pluempanupat, W.; Brecker, L.; Schinnerl, J. Yellow Twig (Nauclea orientalis) from Thailand: Strictosamide as the Key Alkaloid of This Plant Species. Molecules 2022, 27, 5176. https://doi.org/10.3390/molecules27165176
Songoen W, Brunmair J, Traxler F, Wieser VC, Phanchai W, Pluempanupat W, Brecker L, Schinnerl J. Yellow Twig (Nauclea orientalis) from Thailand: Strictosamide as the Key Alkaloid of This Plant Species. Molecules. 2022; 27(16):5176. https://doi.org/10.3390/molecules27165176
Chicago/Turabian StyleSongoen, Weerasak, Julia Brunmair, Florian Traxler, Viktoria Chiara Wieser, Witthawat Phanchai, Wanchai Pluempanupat, Lothar Brecker, and Johann Schinnerl. 2022. "Yellow Twig (Nauclea orientalis) from Thailand: Strictosamide as the Key Alkaloid of This Plant Species" Molecules 27, no. 16: 5176. https://doi.org/10.3390/molecules27165176