Skip to main content
SpringerLink
Log in

Acylated oleanane-type triterpene saponins from the flowers of Bellis perennis show anti-proliferative activities against human digestive tract carcinoma cell lines

  • Original Paper
  • Biologically Active Natural Products from Microorganisms and Plants
  • Published:
Journal of Natural Medicines Aims and scope Submit manuscript

Abstract

Seven oleanane-type triterpene saponin bisdesmosides, perennisaponins N–T (1–7), were newly isolated from a methanol extract of daisy, the flowers of Bellis perennis L. (Asteraceae). The structures were determined based on chemical and physicochemical data and confirmed using previously isolated related compounds as references. The isolates, including 13 previously reported perennisaponins A–M (8–20), exhibited anti-proliferative activities against human digestive tract carcinoma HSC-2, HSC-4, and MKN-45 cells. Among them, perennisaponin O (2, IC50 = 11.2, 14.3, and 6.9 μM, respectively) showed relatively strong activities. The mechanism of action of 2 against HSC-2 was found to involve apoptotic cell death.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Morikawa T, Li X, Nishida E, Ito Y, Matsuda H, Nakamura S, Muraoka O, Yoshikawa M (2008) Perennisosides I–VII, acylated triterpene saponins with antihyperlipidemic activities from the flowers of Bellis perennis. J Nat Prod 71:828–835

    Article  CAS  PubMed  Google Scholar 

  2. Yoshikawa M, Li X, Nishida E, Nakamura S, Matsuda H, Muraoka O, Morikawa T (2008) Medicinal flowers. XXI. Structures of perennisaponins A, B, C, D, E, and F, acylated oleanane-type triterpene oligoglycosides, from the flowers of Bellis perennis. Chem Pharm Bull 56:559–568

    Article  CAS  PubMed  Google Scholar 

  3. Morikawa T, Li X, Nishida E, Nakamura S, Ninomiya K, Matsuda H, Oda Y, Muraoka O, Yoshikawa M (2010) Medicinal flowers. Part 29. Acylated oleanane-type triterpene bisdesmosides: perennisaponins G, H, I, J, K, L, and M with pancreatic lipase inhibitory activity from the flowers of Bellis perennis. Helv Chim Acta 93:573–586

    Article  CAS  Google Scholar 

  4. Morikawa T, Li X, Nishida E, Nakamura S, Ninomiya K, Matsuda H, Hamao M, Muraoka O, Hayakawa T, Yoshikawa M (2011) Medicinal flowers. XXXII. structures of oleanane-type triterpene saponins, perennisosides VIII, IX, X, XI, and XII, from the flowers of Bellis perennis. Chem Pharm Bull 59:889–895

    Article  CAS  PubMed  Google Scholar 

  5. Morikawa T, Ninomiya K, Takamori Y, Nishida E, Yasue M, Hayakawa T, Muraoka O, Li X, Nakamura S, Yoshikawa M, Matsuda H (2015) Oleanane-type triterpene saponins with collagen synthesis-promoting activity from the flowers of Bellis perennis. Phytochemistry 116:203–212

    Article  CAS  PubMed  Google Scholar 

  6. Schöpke T, Al-Tawaha C, Wray V, Nimtz M, Hiller K (1997) Triterpenoid saponins from Aster bellidiastrum. Phytochemistry 45:125–132

    Article  PubMed  Google Scholar 

  7. Yoshikawa M, Morikawa T, Yamamoto K, Kato Y, Nagatomo A, Matsuda H (2005) Floratheasaponins A–C, acylated oleanane-type triterpene oligoglycosides with anti-hyperlipidemic activities from flowers of the tea plant (Camellia sinensis). J Nat Prod 68:1360–1365

    Article  CAS  PubMed  Google Scholar 

  8. Yoshikawa M, Morikawa T, Li N, Nagatomo A, Li X, Matsuda H (2005) Bioactive saponins and glycosides. XXIII. Triterpene saponins with gastroprotective effect from the seeds of Camellia sinensis—theasaponins E3, E4, E5, E6, and E7–. Chem Pharm Bull 53:1559–1564

    Article  CAS  PubMed  Google Scholar 

  9. Morikawa T, Li N, Nagatomo A, Matsuda H, Li X, Yoshikawa M (2006) Triterpene saponins with gastroprotective effects from tea seed (the seeds of Camellia sinensis). J Nat Prod 69:185–190

    Article  CAS  PubMed  Google Scholar 

  10. Yoshikawa M, Morikawa T, Nakamura S, Li N, Li X, Matsuda H (2007) Bioactive saponins and glycosides. XXV. Acylated oleanane-type triterpene saponins from the seeds of tea plant (Camellia sinensis). Chem Pharm Bull 55:57–63

    Article  CAS  PubMed  Google Scholar 

  11. Morikawa T, Matsuda H, Li N, Nakamura S, Li X, Yoshikawa M (2006) Bioactive saponins and glycosides. XXVI. New triterpene saponins, theasaponins E10, E11, E12, E13, and G2, from the seeds of tea plant (Camellia sinensis). Heterocycles 68:1139–1148

    Article  CAS  Google Scholar 

  12. Morikawa T, Nakamura S, Kato Y, Muraoka O, Matsuda H, Yoshikawa M (2007) Bioactive saponins and glycosides. XXVIII. new triterpene saponins, foliatheasaponins I, II, III, IV, and V, from Tencha (the leaves of Camellia sinensis). Chem Pharm Bull 55:293–298

    Article  CAS  PubMed  Google Scholar 

  13. Morikawa T, Matsuda H, Li N, Li X, Yoshikawa M (2007) Bioactive saponins and glycosides. Part 29. Acylated oleanane-type triterpene saponins: theasaponins A6, A7, and B5 from the seeds of Camellia sinensis. Helv Chim Acta 90:2342–2348

    Article  CAS  Google Scholar 

  14. Schöpke T, Hiller K, Wray V, Köppel KD, Yamasaki K, Kasai R (1994) Triterpenoid saponins from Bellis sylvestris, I. Structures of the major deacylsaponins. J Nat Prod 57:1279–1282

    Article  PubMed  Google Scholar 

  15. Burk MJ, Harper TGP, Kalberg CS (1995) Highly enantioselective hydrogenation of β-keto esters under mild conditions. J Am Chem Soc 117:4423–4424

    Article  CAS  Google Scholar 

  16. Asada Y, Ueoka T, Furuya T (1989) Novel acylated saponins from Montbretia (Crocosmia crocosmiiflora). Isolation of saponins and the structures of crocosmiosides A, B and H. Chem Pharm Bull 37:2139–2146

    Article  CAS  Google Scholar 

  17. Morikawa T, Ninomiya K, Imura K, Yamaguchi T, Akagi Y, Yoshikawa M, Hayakawa T, Muraoka O (2014) Hepatoprotective triterpenes from traditional Tibetan medicine Potentilla anserina. Phytochemistry 102:169–181

    Article  CAS  PubMed  Google Scholar 

  18. Morikawa T, Ninomiya K, Akaki J, Kakihara N, Kuramoto H, Matsumoto Y, Hayakawa T, Muraoka O, Wang LB, Wu LJ, Nakamura S, Yoshikawa M, Matsuada H (2015) Dipeptidyl peptidase-IV inhibitory activity of dimeric dihydrochalcone glycosides from flowers of Helichrysum arenarium. J Nat Med 69:494–506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Morikawa T, Ninomiya K, Kuramoto H, Kamei I, Yoshikawa M, Muraoka O (2016) Phenylethanoid and phenylpropanoid glycosides with melanogenesis inhibitory activity from the flowers of Narcissus tazetta var. chinensis. J Nat Med 70:89–101

    Article  CAS  PubMed  Google Scholar 

  20. Karakas FP, Şöhretoğlu D, Liptaj T, Štujber M, Turker AU, Marák J, Çalış I, Yalçın N (2014) Isolation of an oleanane-type saponin active from Bellis perennis through antitumor bioassay-guided procedures. Pharm Biol 52:951–955

    Article  Google Scholar 

  21. Kitagawa I, Sakagami M, Hashiuchi F, Zhou JL, Yoshikawa M, Ren J (1989) Apioglycyrrhizin and araboglycyrrhizin, two new sweet oleanene-type triterpene oligoglycosides from the root of Glycyrrhiza inflata. Chem Pharm Bull 37:551–553

    Article  CAS  Google Scholar 

  22. Morikawa T, Tao J, Toguchida I, Matsuda H, Yoshikawa M (2003) Structures of new cyclic diarylheptanoids and inhibitors of nitric oxide production from Japanese folk medicine Acer nikoense. J Nat Prod 66:86–91

    Article  CAS  PubMed  Google Scholar 

  23. Wang LB, Morikawa T, Nakamura S, Ninomiya K, Matsuda H, Muraoka O, Wu LJ, Yoshikawa M (2009) Medicinal flowers. XXVIII. Structures of five new glycosides, everlastosides A, B, C, D, and E, from the flowers of Helichrysum arenarium. Heterocycles 78:1235–1242

    Article  CAS  Google Scholar 

  24. Morikawa T, Wang LB, Ninomiya K, Nakamura S, Matsuda H, Muraoka O, Wu LJ, Yoshikawa M (2009) Medicinal flowers. XXX. Eight new glycosides, everlastosides F–M, from the flowers of Helichrysum arenarium. Chem Pharm Bull 57:853–859

    Article  CAS  PubMed  Google Scholar 

  25. Zhang X, Zhang Y, Gu D, Cao C, Zhang Q, Xu Z, Gong Y, Chen J, Tang C (2013) Increased risk of developing digestive tract cancer in subjects carrying the PLCE1 rs2274223 A > G polymorphism: evidence from a meta-analysis. PLoS One 8:e76425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Matsuda H, Yoshida K, Miyagawa K, Nemoto Y, Asao Y, Yoshikawa M (2006) Nuphar alkaloids with immediately apoptosis-inducing activity from Nuphar pumilum and their structural requirements for the activity. Bioorg Med Chem Lett 16:1567–1573

    Article  CAS  PubMed  Google Scholar 

  27. Kloesch B, Becker T, Dietersdorfer E, Kiener H, Steiner G (2013) Anti-inflammatory and apoptotic effects of the polyphenol curcumin on human fibroblast-like synoviocytes. Int Immunopharmacol 15:400–405

    Article  CAS  PubMed  Google Scholar 

  28. Yokosuka A, Suzuki T, Tatsuno S, Mimaki Y (2014) Steroidal glycosides from the underground parts of Yucca glauca and their cytotoxic activities. Phytochemistry 101:109–115

    Article  CAS  PubMed  Google Scholar 

  29. Tang L, Wang Z, Wu H, Yokosuka A, Mimaki Y (2014) Steroidal glycosides from the underground parts of Dracaena thalioides and their cytotoxic activity. Phytochemistry 107:102–110

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by the MEXT-Supported Program for the Strategic Research Foundation at Private Universities, 2014–2018 (T.M.) and JSPS KAKENHI grant numbers 15K08008 (T.M), 15K08009 (K.N.), and 16K08313 (O.M.).

Author information

Authors and Affiliations

  1. Pharmaceutical Research and Technology Institute, Kindai University, 3-4-1 Kowakae, Higashi-osaka, Osaka, 577-8502, Japan

    Kiyofumi Ninomiya, Chiaki Motai, Eriko Nishida, Niichiro Kitagawa, Kazuya Yoshihara, Takao Hayakawa, Osamu Muraoka & Toshio Morikawa

  2. Antiaging Center, Kindai University, 3-4-1 Kowakae, Higashi-osaka, Osaka, 577-8502, Japan

    Kiyofumi Ninomiya, Osamu Muraoka & Toshio Morikawa

  3. Koshiro Co., Ltd., 2-5-8 Doshomachi, Chuo-ku, Osaka, 541-0045, Japan

    Chiaki Motai & Niichiro Kitagawa

  4. Kyoto Pharmaceutical University, Misasagi, Yamashina-ku, Kyoto, 607-8412, Japan

    Xuezheng Li, Seikou Nakamura, Masayuki Yoshikawa & Hisashi Matsuda

Authors
  1. Kiyofumi Ninomiya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chiaki Motai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eriko Nishida
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Niichiro Kitagawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kazuya Yoshihara
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Takao Hayakawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Osamu Muraoka
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xuezheng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Seikou Nakamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Masayuki Yoshikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Hisashi Matsuda
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Toshio Morikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Hisashi Matsuda or Toshio Morikawa.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 146 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ninomiya, K., Motai, C., Nishida, E. et al. Acylated oleanane-type triterpene saponins from the flowers of Bellis perennis show anti-proliferative activities against human digestive tract carcinoma cell lines. J Nat Med 70, 435–451 (2016). https://doi.org/10.1007/s11418-016-0998-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11418-016-0998-9

Keywords

Search

Navigation