Skip to main content
Log in

Alkaloids from the bulbs of Lycoris longituba and their neuroprotective and acetylcholinesterase inhibitory activities

  • Research Article
  • Published:
Archives of Pharmacal Research Aims and scope Submit manuscript

Abstract

Three novel alkaloids (13), together with nineteen known ones (422), were isolated from the bulbs of Lycoris longituba. Their structures were elucidated on the basis of extensive spectroscopic analyses, which belong to several Amaryllidaceae alkaloid skeletons. Among them, the harmane-type alkaloids (the new compound 1 and the known compounds 5, 6 and 7) were found for the first time from Lycoris genus. The isolates were tested for their neuroprotective activities against CoCl2, H2O2 and Aβ25–35-induced SH-SY5Y cell injuries, and the majority of them exhibited neuroprotective activities of different degrees. The acetylcholinesterase (AChE) inhibitory activities of the isolated alkaloids were also evaluated, while compounds 12, 1420 and 22 exhibited extremely significant AChE inhibitory activities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abramovitch, R.A., and I.D. Spenser. 1964. The nuclear magnetic resonance spectra of the carbolines. Canadian Journal of Chemistry 42: 954–956.

    Article  CAS  Google Scholar 

  • Alonso, R., A. Caballero, P.J. Campos, and M.A. Rodr I Guez. 2010. Photochemistry of acyloximes: Synthesis of heterocycles and natural products. Tetrahedron 66: 8828–8831.

    Article  CAS  Google Scholar 

  • Andrade, J.P., S. Berkov, F. Viladomat, C. Codina, J.A.S. Zuanazzi, and J. Bastida. 2011. Alkaloids from hippeastrum papilio. Molecules 16: 7097–7104.

    Article  PubMed  Google Scholar 

  • Balkau, F., and M.L. Heffernen. 1973. NMR spectra of the carbolines. I. Spectral parameters. Australian Journal of Chemistry 26: 1501–1522.

    Article  CAS  Google Scholar 

  • Bandini, M., A. Eichholzer, M. Tragni, and A. Umani-Ronchi. 2008. Enantioselective phase-transfer-catalyzed intramolecular aza-michael reaction: Effective route to pyrazino-indole compounds. Angewandte Chemie 120: 3282–3285.

    Article  Google Scholar 

  • Bartus, R.T., R.R. Dean, B. Beer, and A.S. Lippa. 1982. The cholinergic hypothesis of geriatric memory dysfunction. Science 217: 408–414.

    Article  CAS  PubMed  Google Scholar 

  • Berkov, S., R. Reyes-Chilpa, C. Codina, F. Viladomat, and J. Bastida. 2007. Revised NMR data for incartine: An alkaloid from Galanthus elwesii. Molecules 12: 1430–1435.

    Article  CAS  PubMed  Google Scholar 

  • Cowden, C.J., M.G. Banwell, and I.C. Ho. 1994. Synthesis of the putative structure of 5, 6-dihydrobicolorine. Journal of Natural Products 57: 1746–1750.

    Article  CAS  Google Scholar 

  • Eldeen, I.M., E.E. Elgorashi, and J. van Staden. 2005. Antibacterial, anti-inflammatory, anti-cholinesterase and mutagenic effects of extracts obtained from some trees used in South African traditional medicine. Journal of Ethnopharmacology 102: 457–464.

    Article  CAS  PubMed  Google Scholar 

  • Elgorashi, E.E., G.I. Stafford, and J. van Staden. 2004. Acetycholinesterase enzyme inhibitory effects of amaryllidaceae alkaloids. Planta Medica 70: 260–262.

    Article  CAS  PubMed  Google Scholar 

  • Ellman, G.L., K.D. Courtney, V.J. Andres, and R.M. Feather-stone. 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology 7: 88–95.

    Article  CAS  PubMed  Google Scholar 

  • Evidente, A., I. Iasiello, and G. Randazzo. 1984. Hippamine, a minor alkaloid from Sternbergia lutea. Journal of Natural Products 47: 1061–1062.

    Article  CAS  Google Scholar 

  • Evidente, A., M. Rosaria Cicala, I. Giudicianni, G. Randazzo, and R. Riccio. 1983. 1H and 13c nmr analysis of lycorine and α-dihydrolycorine. Phytochemistry 22: 581–584.

    Article  CAS  Google Scholar 

  • He, Q., Y. Shen, M. Wang, M. Huang, R. Yang, S. Zhu, L. Wang, Y. Xu, and R. Wu. 2011. Natural variation in petal color in Lycoris longituba revealed by anthocyanin components. PLoS One 6: e22098.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hiroko, S., H. Akihiro, and H. Tohru. 1993. The 1H- and 13C-nuclear magnetic resonance spectra of harman. Reinvestigation of the assignments by one- and two-dimensional methods. Chemical & Pharmaceutical Bulletin 41: 1169–1172.

    Article  Google Scholar 

  • Ieven, M., B.D.A. Vanden, F. Mertens, A. Vlietinck, and E. Lammens. 1979. Screening of higher plants for biological activities. I. Antimicrobial activity. Planta medica 36: 311–321.

    Article  CAS  PubMed  Google Scholar 

  • Jin, A., X. Li, Y.Y. Zhu, H.Y. Yu, H.F. Pi, P. Zhang, and H.L. Ruan. 2014. Four new compounds from the bulbs of Lycoris aurea with neuroprotective effects against CoCl2 and H2O2-induced SH-SY5Y cell injuries. Archives of Pharmacal Research 37: 315–323.

    Article  CAS  PubMed  Google Scholar 

  • Jin, J., and S.M. Weinreb. 1997. Application of a stereospecific intramolecular allenylsilane imino ene reaction to enantioselective total synthesis of the 5, 11-methanomorphanthridine class of amaryllidaceae alkaloids. Journal of the American Chemical Society 119: 5773–5784.

    Article  CAS  Google Scholar 

  • Jin, Z. 2005. Amaryllidaceae and sceletium alkaloids. Natural Product Reports 22: 111–126.

    Article  CAS  PubMed  Google Scholar 

  • Jokhadze, M., L. Eristavi, J. Kutchukhidze, A. Chariot, L. Angenot, M. Tits, O. Jansen, and M. Frederich. 2007. In vitro cytotoxicity of some medicinal plants from Georgian Amaryllidaceae. Phytotherapy Research 21: 622–624.

    Article  CAS  PubMed  Google Scholar 

  • Kihara, M., L. Xu, K. Konishi, K. Kida, Y. Nagao, S. Kobayashi, and T. Shingu. 1994. Isolation and structure elucidation of a novel alkaloid, incartion, a supposed biosynthetic intermediate, from flowers of Lycoris incarnata. Chemical & Pharmaceutical Bulletin 42: 289–292.

    Article  CAS  Google Scholar 

  • Kitagawa T., S. Uyeo, and N. Yokoyama. 1959. Stereochemistry of lycorenine, homolycorine, pluviine, and their hydrogenation products. Journal of the Chemical Society 3741–3751.

  • Kornienko, A., and A. Evidente. 2008. Chemistry, biology and medicinal potential of narciclasine and its congeners. Chemical Reviews 108: 1982–2014.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li, L., J. Li, Y. Huang, Q. Wu, S. Deng, X. Su, R. Yang, J. Huang, Z. Chen, and S. Li. 2012. Lignans from the heartwood of Streblus asper and their inhibiting activities to Hepatitis B virus. Fitoterapia 83: 303–309.

    Article  CAS  PubMed  Google Scholar 

  • Li, X., H.Y. Yu, Z.Y. Wang, H.F. Pi, P. Zhang, and H.L. Ruan. 2013. Neuroprotective compounds from the bulbs of Lycoris radiata. Fitoterapia 88: 82–90.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y., M. Zhao, and K.L. Parkin. 2011. β-Carboline derivatives and diphenols from soy sauce are in vitro quinone reductase (QR) inducers. Journal of Agricultural and Food Chemistry 59: 2332–2340.

    Article  CAS  PubMed  Google Scholar 

  • Liang, Y.Q., X. Feng, and Z.X. Zhao. 2010. The alkaloids in bulbs of lycoris longituba. Natural Product Research and Development 22: 241–244.

    CAS  Google Scholar 

  • Lopez, S., J. Bastida, F. Viladomat, and C. Codina. 2002. Acetylcholinesterase inhibitory activity of some Amaryllidaceae alkaloids and narcissus extracts. Life Sciences 71: 2521–2529.

    Article  CAS  PubMed  Google Scholar 

  • Louw, C.A., T.J. Regnier, and L. Korsten. 2002. Medicinal bulbous plants of South Africa and their traditional relevance in the control of infectious diseases. Journal of Ethnopharmacology 82: 147–154.

    Article  CAS  PubMed  Google Scholar 

  • Matusch, R., M. Kreh, M.U. Ller, and U. Bildung. 1994. Kristallstruktur und absolute Konfiguration von (-)-N-(Chloromethyl) galanthaminium-chlorid. Helvetica Chimica Acta 77: 1611–1615.

    Article  CAS  Google Scholar 

  • McNulty, J., J.J. Nair, C. Codina, J. Bastida, S. Pandey, J. Gerasimoff, and C. Griffin. 2007. Selective apoptosis-inducing activity of crinum-type Amaryllidaceae alkaloids. Phytochemistry 68: 1068–1074.

    Article  CAS  PubMed  Google Scholar 

  • Pabuccuoglu V., P. Richomme, T. Gozler, B. Kivcak, A.J. Freyer, and M. Shamma. 1989. Four new crinine-type alkaloids from Sternbergia species. Journal of Natural Products 52: 785–791.

  • Pearson, W.H., and B.W. Lian. 1998. Application of the 2-azaallyl anion cyclo-addition method to an enantioselective total synthesis of (+)-coccinine. Angewandte Chemie 37: 1724–1726.

    Article  CAS  Google Scholar 

  • Perry, E.K. 1986. The cholinergic hypothesis—ten years on. British Medical Bulletin 42: 63–69.

    CAS  PubMed  Google Scholar 

  • Roberts, J.D., W.O. Crain Jr, and W.C. Wildman. 1971. Nuclear magnetic resonance spectroscopy. Carbon-13 spectra of nicotine, quinine, and some Amaryllidaceae alkaloids. Journal of the American Chemical Society 93: 990–994.

    Article  CAS  PubMed  Google Scholar 

  • Sener, B., I. Orhan, and J. Satayavivad. 2003. Antimalarial activity screening of some alkaloids and the plant extracts from Amaryllidaceae. Phytotherapy Research 17: 1220–1223.

    Article  CAS  PubMed  Google Scholar 

  • Senol, F.S., I. Orhan, G. Yilmaz, M. Cicek, and B. Sener. 2010. Acetylcholinesterase, butyrylcholinesterase, and tyrosinase inhibition studies and antioxidant activities of 33 Scutellaria L. taxa from Turkey. Food and Chemical Toxicology 48: 781–788.

    Article  CAS  PubMed  Google Scholar 

  • Stanley, L.M., and J.F. Hartwig. 2009. Iridium-catalyzed regio- and enantioselective N-allylation of indoles. Angewandte Chemie 121: 7981–7984.

    Article  Google Scholar 

  • Suau, R., A.I. Gómez, and R. Rico. 1990. Ismine and related alkaloids from Lapiedra martinezii. 1712 29: 1710.

    CAS  Google Scholar 

  • Treu, M., and U. Jordis. 2001. 4aS, 6R, 8aS)-4a, 5, 9, 10, 11, 12-Hexahydro-6H-benzofuro [3a, 3, 2-ef][2] benzazepine-3, 6-diol (Norsanguinine. Molecules 6: M274.

    Article  CAS  Google Scholar 

  • Tsuda, Y., T. Sano, J. Taga, K. Isobe, J. Toda, S. Takagi, M. Yamaki, M. Murata, H. Irie, and H. Tanaka. 1979. Total synthesis of the amaryllidaceae alkaloids, lycorine and zephyranthine. Journal of the Chemical Society, Perkin Transactions 1: 1358–1363.

    Article  Google Scholar 

  • Wang, L., Z. Yin, Y. Cai, X. Zhang, X. Yao, and W. Ye. 2010. Amaryllidaceae alkaloids from the bulbs of Lycoris radiata. Biochemical Systematics and Ecology 38: 444–446.

    Article  CAS  Google Scholar 

  • Wu, W.M., Y.Y. Zhu, H.R. Li, H.Y. Yu, P. Zhang, H.F. Pi, and H.L. Ruan. 2014. Two new alkaloids from the bulbs of Lycoris sprengeri. Journal of Asian Natural Products Research 16: 192–199.

    Article  PubMed  Google Scholar 

  • Zhao, Y., Y. Liang, Y. Chen, H. Sun, M. Wang, and X. Feng. 2011. Chemical constituents of bulbs of Lycoris longituba. Zhongyaocai 34: 1366–1368.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Financial supports from the Ministry of Science and Technology of the People’s Republic of China (International Cooperative Project, Grant No. 2010DFA32430) and Natural Science Foundation of China (No. 81072547, 31270394 and 30873361) are gratefully acknowledged.

Conflict of interest

All the authors have no conflict of interest to declare.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Han-Li Ruan.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhu, YY., Li, X., Yu, HY. et al. Alkaloids from the bulbs of Lycoris longituba and their neuroprotective and acetylcholinesterase inhibitory activities. Arch. Pharm. Res. 38, 604–613 (2015). https://doi.org/10.1007/s12272-014-0397-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12272-014-0397-2

Keywords

Navigation