Skip to main content

Advertisement

SpringerLink
Log in

Ultra-performance liquid chromatography coupled with quadrupole high-resolution time-of-flight mass spectrometry for metabolite profiling and biological activity of Stellaria pallida (Dumort) Piré

  • Original Research
  • Published:
Medicinal Chemistry Research Aims and scope Submit manuscript

Abstract

Medicinal plants have a wide variety of valuable biological activities. Stellaria pallida (Dumort) Piré is a well-known plant; however, this species’ phytochemical and biological activity assessment is rare. Ultra-performance liquid chromatography coupled with quadrupole high-resolution time-of-flight mass spectrometry (UPLC/QTOF-MS) was used for the metabolic profiling of Stellaria pallida. The total phenol and flavonoid contents were colorimetrically evaluated using Folin–Ciocalteu and aluminum chloride reagents, respectively. The total antioxidant capacity was investigated, and free radical scavenging activities against DPPH, superoxide anion radical (O2−), ABTS+, and Fe2+ chelating capacity were determined. The cytotoxic effect was tested on the Hep-G2, HeLa, HCT116, and MCF-7 cell lines. Cytopathic effect inhibition assay was applied to determine the antiviral activity. Methanol extract contained 25.8 mg GAE/g dry weight and 29.5 mg QE/g dry weight of total phenol and flavonoid contents, respectively. Twenty-two metabolites were identified; three fundamental flavonoid aglycones (apigenin, quercetin, and kaempferol) with their O and/or C-glycosides. Methanol extract significantly scavenged DPPH, superoxide anion radical (O2−), and ABTS+ and showed significant Fe2+ chelating capacity. It showed a significant selective cytotoxic effect, with IC50 ranging from 3.55 µg/mL to 4.84 µg/mL against MCF-7 and Hep-G2, respectively. In addition, the methanol extract showed a wide range of antiviral activity. Stellaria pallida has promising therapeutic potential and could be considered a possible source of natural compounds with several activities.

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
Fig. 5

Similar content being viewed by others

References

  1. Chinnappa CC, Morton JK. Studies on the Stellaria longipes complex (Caryophyllaceae)-biosystematics. Syst Bot. 1984;9:60–73. https://doi.org/10.2307/2418408

    Article  Google Scholar 

  2. National Institute of Science Communication and Information Resources (CSIR). The Wealth of India, An Encyclopedia of India’s Raw Materials Resources, Vol X. New Delhi: CSIR, Dr K S Krishnan Marg; 1976

  3. Yuh-Fung C, Ping-Chung K, Hsiu-Hui C, I-Je K, Fu-Wen L, Chung-Ren S, et al. β-Carboline alkaloids from Stellaria dichotoma var. lanceolata and their anti-inflammatory activity. J Nat Prod. 2010;73:1993–8. https://doi.org/10.1021/np1003627

    Article  CAS  Google Scholar 

  4. Malik AH, Khuroo AA, Dar GH, Khan ZS. Ethnomedicinal uses of some plants in the Kashmir Himalaya. Ind J Tradit Know. 2011;10:362–6.

    Google Scholar 

  5. Morita H, Kayashita T, Shishido A, Takeya K, Itokawa H, Shiro M. Dichotomins A–E, new cyclic peptides from Stellaria dichotoma L. var. lanceolata Bge. Tetrahedron. 1996;52:1165–76. https://doi.org/10.1016/0040-4020(95)00974-4

    Article  CAS  Google Scholar 

  6. Zoll A, Nouvel G. Comparative study of the C-glycosyl flavones of two Caryophyllaceae, Spergularia rubra and Stellaria holostea. Plantes Med Phytother. 1974;8:134–40.

    CAS  Google Scholar 

  7. Kitanov G. Phenolic acids and flavonoids from Stellaria media (L.) Vill. (Caryophyllaceae). Pharmazie. 1992;47:470–1.

    CAS  Google Scholar 

  8. Morikawa T, Sun B, Matsuda H, Wu LJ, Harima S, Yoshikawa M. Bioactive constituents from Chinese natural medicines. XIV. New glycosides of β-carboline-type alkaloid, neolignan, and phenylpropanoid from Stellaria dichotoma L. var. lanceolata andF their antiallergic activities. Chem Pharm Bull (Tokyo). 2004;52:1194–9. https://doi.org/10.1248/cpb.52.1194

    Article  CAS  PubMed  Google Scholar 

  9. Sun B, Morikawa T, Matsuda H, Tewtrakul S, Wu LJ, Harima S, et al. Structures of new beta-carboline-type alkaloids with antiallergic effects from Stellaria dichotoma(1,2). J Nat Prod. 2004;67:1464–9. https://doi.org/10.1021/np040080a

    Article  CAS  PubMed  Google Scholar 

  10. Morita H, Iizuka T, Choo CY, Chan KL, Itokawa H, Takeya K. Dichotomins J and K, vasodilator cyclic peptides from Stellaria dichotoma. J Nat Prod. 2005;68:1686–8. https://doi.org/10.1021/np050262k

    Article  CAS  PubMed  Google Scholar 

  11. Hodisan V, Sancraian A. Triterpenoid saponins from Stellaria media (L.) Cyr. Farmacia. 1989;37:105–9.

    CAS  Google Scholar 

  12. Kameoka H, Wang CP, Yamaguchi T. The constituents of the essential oil from Stellaria aquatica Scop. nippon Nogeikagaku Kaishi. 1978;52:335–40. https://doi.org/10.1271/nogeikagaku1924.52.8_335

    Article  CAS  Google Scholar 

  13. Pande A, Shukla YN, Tripathi AK. Lipid constituents from Stellaria media. Phytochemistry. 1995;39:709–11. https://doi.org/10.1016/0031-9422(94)00935-M

    Article  CAS  Google Scholar 

  14. Vanhaecke M, Van den Ende W, Lescrinier E, Dyubankova N. Isolation and characterization of a pentasaccharide from Stellaria media. J Nat Prod. 2008;71:1833–6. https://doi.org/10.1021/np800274k

    Article  CAS  PubMed  Google Scholar 

  15. Chon SU, Heo BG, Park YS, Kim DK, Gorinstein S. Total phenolics level, antioxidant activities and cytotoxicity of young sprouts of some traditional Korean salad plants. Plant Foods Hum Nutr. 2009;64:25–31. https://doi.org/10.1007/s11130-008-0092-x

    Article  CAS  PubMed  Google Scholar 

  16. Slavokhotova AA, Rogozhin EA, Musolyamov AK, Andreev YA, Oparin PB, Berkut AA, et al. Novel antifungal α-hairpinin peptide from Stellaria media seeds: structure, biosynthesis, gene structure and evolution. Plant Mol Biol. 2014;84:189–202. https://doi.org/10.1007/s11103-013-0127-z

    Article  CAS  PubMed  Google Scholar 

  17. Rogozhin EA, Slezina MP, Slavokhotova AA, Istomina EA, Korostyleva TV, Smirnov AN, et al. A novel antifungal peptide from leaves of the weed Stellaria media L. Biochimie. 2015;116:125–32. https://doi.org/10.1016/j.biochi.2015.07.014

    Article  CAS  PubMed  Google Scholar 

  18. Giordani C, Simonetti G, Natsagdorj D, Choijamts G, Ghirga F, Calcaterra A, et al. Antifungal activity of Mongolian medicinal plant extracts. Nat Prod Res. 2020;34:449–55. https://doi.org/10.1080/14786419.2019.1610960

    Article  CAS  PubMed  Google Scholar 

  19. Lim BO, Choi SH, Kim EK, Lee SJ, Je JY, Jeon YJ, et al. Antioxidant activity of enzymatic extracts from Stellaria dichotoma. J Med Food. 2008;11:723–32. https://doi.org/10.1089/jmf.2007.0135

    Article  CAS  PubMed  Google Scholar 

  20. Su L, Jiang YY, Liu B. Oligopeptides in plant medicines cited in Chinese Pharmacopoeia. Zhongguo Zhong Yao Za Zhi. 2016;41:2943–52. https://doi.org/10.4268/cjcmm20161601

    Article  PubMed  Google Scholar 

  21. Shan Y, Zheng Y, Guan F, Zhou J, Zhao H, Xia B, et al. Purification and characterization of a novel anti-HSV-2 protein with antiproliferative and peroxidase activities from Stellaria media. Acta Biochim Biophys Sin. 2013;45:649–55. https://doi.org/10.1093/abbs/gmt060

    Article  CAS  PubMed  Google Scholar 

  22. Lihua M, Jie S, Yaqin S, Changmei W, Bin C, Donghao X, et al. Anti-hepatitis B virus activity of chickweed [Stellaria media (L.) Vill.] extracts in cells HepG2.2.15. Molecules. 2012;17:8633–46. https://doi.org/10.3390/molecules17078633

    Article  CAS  Google Scholar 

  23. Wittig R. The origin and development of the Urban flora of central Europe. Urban Ecosyst. 2004;7:323–9. https://doi.org/10.1007/s11252-005-6833-9

    Article  Google Scholar 

  24. Kirtikar KR, Basu BD. Indian Medicinal Plants. Vol. II. Dehradun: International Book Distribution; 2006.

    Google Scholar 

  25. Abu-Ziada ME, ElSherbeny GA, Al-Jubawy HM. Autecology and bioactive metabolites of Stellaria pallida growing in Northeast Nile Delta, Egypt. J Biol Sci. 2015;15:25–32.

    Article  CAS  Google Scholar 

  26. Dan M, Su M, Gao X, Zhao T, Zhao A, Xie G, et al. Metabolite profiling of Panax notoginseng using UPLC–ESI-MS. Phytochemistry. 2008;69:2237–44. https://doi.org/10.1016/j.phytochem.2008.04.015

    Article  CAS  PubMed  Google Scholar 

  27. Tsugawa H, Cajka T, Kind T, Ma Y, Higgins B, Ikeda K, et al. MS-DIAL: data-independent MS/MS deconvolution for comprehensive metabolome analysis. Nat Methods. 2015;12:523–6. https://doi.org/10.1038/nmeth.3393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Smith CA, O’Maille G, Want EJ, Qin C, Trauger SA, Brandon TR, et al. Metlin: a metabolite mass spectral database. Ther Drug Monit. 2005;27:747–51. https://doi.org/10.1097/01.ftd.0000179845.53213.39

    Article  CAS  PubMed  Google Scholar 

  29. Demarque DP, Crotti AE, Vessecchi R, Lopes JL, Lopes NP. Fragmentation reactions using electrospray ionization mass spectrometry: an important tool for the structural elucidation and characterization of synthetic and natural products. Nat Prod Rep. 2016;33:432–55. https://doi.org/10.1039/c5np00073d

    Article  CAS  PubMed  Google Scholar 

  30. Fabre N, Rustan I, De Hoffmann E, Quetin-Leclercq J. Determination of flavone, flavonol, and flavanone aglycones by negative ion liquid chromatography electrospray ion trap mass spectrometry. J Am Soc Mass Spectrom. 2001;12:707–15. https://doi.org/10.1016/S1044-0305(01)00226-4

    Article  CAS  PubMed  Google Scholar 

  31. Tsimogiannis D, Samiotaki M, Panayotou G, Oreopoulou V. Characterization of flavonoid subgroups and hydroxy substitution by HPLC-MS/MS. Molecules. 2007;12:593–606. https://doi.org/10.3390/12030593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Farag MA, El Fishawy AM, El-Toumy SA, Amer KF, Mansour AM, Taha HE. Antihepatotoxic effect and metabolite profiling of Panicum turgidum extract via UPLC-QTOF-MS. Pharmacogn Mag. 2016;12:S446–53. https://doi.org/10.4103/0973-1296.191455

    Article  PubMed  PubMed Central  Google Scholar 

  33. Ibrahim T, Hegazy M, El-Hela A. Profiling of biologically active metabolites of Spergula fallax L. using high-resolution UPLC-QTOF-MS. Curr Pharma Biotechnol. 2022;23:1758–71. https://doi.org/10.2174/1389201023666220209125306

    Article  CAS  Google Scholar 

  34. Zhou K, Yu L. Total phenolic contents and antioxidant properties of commonly consumed vegetables grown in Colorado. LWT Food Sci Technol. 2006;39:1155–62. https://doi.org/10.1016/j.lwt.2005.07.015

    Article  CAS  Google Scholar 

  35. Rezk BM, Haenen GR, van der Vijgh WJF, Bast A. The antioxidant activity of phloretin: the disclosure of a new antioxidant pharmacophore in flavonoids. Biochem Biophys Res Commun. 2002;295:9–13. https://doi.org/10.1016/s0006-291x(02)00618-6

    Article  CAS  PubMed  Google Scholar 

  36. Hamed ANE, Samy MN, Mahmoud BK, Attia EZZ, Ali TFS, Afifi AH, et al. Flavonoidal glycosides and in vitro antioxidant activity of Bignonia binata Thunb. leaves Family Bignoniaceae and in silico evidence of their potential anti-COVID-19 activity. J Adv Biomed Pharma Sci. 2021;4:98–106. https://doi.org/10.21608/jabps.2021.59606.1118

    Article  Google Scholar 

  37. Choi BY. Biochemical basis of anti-cancer- effects of phloretin- A natural dihydrochalcone. Molecules. 2019;24:278 https://doi.org/10.3390/molecules24020278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Hernandes LC, Machado ART, Tuttis K, Ribeiro DL, Aissa AF, Dévoz PP, et al. Caffeic acid and chlorogenic acid cytotoxicity, genotoxicity and impact on global DNA methylation in human leukemic cell lines. Genet Mol Biol. 2020;43:e20190347 https://doi.org/10.1590/1678-4685-GMB-2019-0347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Kumar S, Pandey AK. Chemistry and biological activities of flavonoids: an overview. Sci World J. 2013;2013:162750 https://doi.org/10.1155/2013/162750

    Article  CAS  Google Scholar 

  40. Lin SC, Chen MC, Liu S, Callahan VM, Bracci NR, Lehman CW, et al. Phloretin inhibits Zika virus infection by interfering with cellular glucose utilisation. Int J Antimicrob Agents. 2019;54:80–4. https://doi.org/10.1016/j.ijantimicag.2019.03.017

    Article  CAS  PubMed  Google Scholar 

  41. Ding Y, Cao Z, Cao L, Ding G, Wang Z, Xiao W. Antiviral activity of chlorogenic acid against influenza A (H1N1/H3N2) virus and its inhibition of neuraminidase. Sci Rep. 2017;7:45723 https://doi.org/10.1038/srep45723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Ganeshpurkar A, Saluja AK. The pharmacological potential of rutin. Saudi Pharm J. 2017;25:149–64. https://doi.org/10.1016/j.jsps.2016.04.025

    Article  PubMed  Google Scholar 

  43. Quest. Graph™ IC50 calculator. Bioquest AAT, Inc, 2022. https://www.aatbio.com/tools/ic50-calculator [cited 29/7/2022].

  44. Elliott AC, Woodward WA. Statistical analysis quick reference guidebook: with SPSS examples, first edition. Newbury Park, CA: SAGE Publications, Inc; 2007.

  45. Stefova M, Petkovska A, Ugarkovic S, Stanoeva JP. Strategy for optimized use of LC-MS for determination of the polyphenolic profiles of apple peel, flesh and leaves. Arab J Chem. 2019;12:5180–6. https://doi.org/10.1016/j.arabjc.2016.12.009

    Article  CAS  Google Scholar 

  46. AyaAllah O, Marwa SA, Atef AE. Phytoconstituents and biological investigation of Minuartia genculata Graebn. IJGHC. 2019;8:353–74.

    Google Scholar 

  47. Willems JL, Khamis MM, Saeid WM, Purves RW, Katselis G, Low NH, et al. Analysis of a series of chlorogenic acid isomers using differential ion mobility and tandem mass spectrometry. Anal Chim Acta. 2016;933:164–74. https://doi.org/10.1016/j.aca.2016.05.041

    Article  CAS  PubMed  Google Scholar 

  48. Wang Y, Liang Z, Liao X, Zhou C, Xie Z, Zhu S, et al. Identification of C-glycosyl flavones by high-performance liquid chromatography-electrospray ionization mass spectrometry and quantification of five main C-glycosyl flavones in Flickingeria fimbriata. BMC Chem. 2019;13:94 https://doi.org/10.1186/s13065-019-0616-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Lamyaa FI, Ahmed E, Mona MM, Sameh RH, El-Sayed SA, Mona ESK. Flavonoid investigation, LC–ESI-MS profile and cytotoxic activity of Raphanus raphanistrum L. (Brassicaceae). J Chem Pharm Res. 2016;8:786–93.

    Google Scholar 

  50. Zhang X, Yin J, Liang C, Sun Y, Zhang L. A simple and sensitive UHPLC-Q-TOF-MS/MS method for sophoricoside metabolism study in vitro and in vivo. J Chromatogr B Analyt Technol Biomed Life Sci. 2017;1061–1062:193–208. https://doi.org/10.1016/j.jchromb.2017.07.003

    Article  CAS  PubMed  Google Scholar 

  51. Zhang X, Yin J, Liang C, Sun Y, Zhang L. UHPLC-Q-TOF-MS/MS method based on four-step strategy for metabolism study of fisetin in vitro and in vivo. J Agric Food Chem. 2017;65:10959–72. https://doi.org/10.1021/acs.jafc.7b04265

    Article  CAS  PubMed  Google Scholar 

  52. Ouyang H, Li T, He M, Li Z, Tan T, Zhang W, et al. Identification and quantification analysis on the chemical constituents from traditional Mongolian medicine flos scabiosae using UHPLC–DAD–Q-TOF-MS combined with UHPLC–QqQ-MS. J Chromatogr Sci. 2016;54:1028–36. https://doi.org/10.1093/chromsci/bmw041

    Article  CAS  PubMed  Google Scholar 

  53. Sato Y, Itagaki S, Kurokawa T, Ogura J, Kobayashi M, Hirano T, et al. In vitro and in vivo antioxidant properties of chlorogenic acid and caffeic acid. Int J Pharm. 2011;403:136–8. https://doi.org/10.1016/j.ijpharm.2010.09.035

    Article  CAS  PubMed  Google Scholar 

  54. Li Y, But PPH, Ooi VEC. Antiviral activity and mode of action of caffeoylquinic acids from Schefflera heptaphylla (L.) Frodin. Antiviral Res. 2005;68:1–9. https://doi.org/10.1016/j.antiviral.2005.06.004

    Article  CAS  PubMed  Google Scholar 

  55. Trendafilova A, Ivanova V, Rangelov M, Todorova M, Ozek G, Yur S, et al. Caffeoylquinic acids, cytotoxic, antioxidant, acetylcholinesterase and tyrosinase enzyme inhibitory activities of six Inula species from Bulgaria. Chem Biodivers. 2020;17:e2000051 https://doi.org/10.1002/cbdv.202000051

    Article  CAS  PubMed  Google Scholar 

  56. Xiao J, Capanoglu E, Jassbi AR, Miron A. Advance on the flavonoid C-glycosides and health benefits. Crit Rev Food Sci Nutr. 2016;56:S29–45. https://doi.org/10.1080/10408398.2015.1067595

    Article  CAS  PubMed  Google Scholar 

  57. Li W, Lu Y. Hepatoprotective effects of sophoricoside against fructose-induced liver injury via regulating lipid metabolism, oxidation, and inflammation in mice. J Food Sci. 2018;83:552–8. https://doi.org/10.1111/1750-3841.14047

    Article  CAS  PubMed  Google Scholar 

  58. Hou DX, Fukuda M, Johnson JA, Miyamori K, Ushikai M, Fujii M. Fisetin induces transcription of NADPH: quinone oxidoreductase gene through an antioxidant responsive element-involved activation. Int J Oncol. 2001;18:1175–9. https://doi.org/10.3892/ijo.18.6.1175

    Article  CAS  PubMed  Google Scholar 

  59. Suh Y, Afaq F, Johnson JJ, Mukhtar H. A plant flavonoid fisetin induces apoptosis in colon cancer cells by inhibition of COX2 and Wnt/EGFR/NF-kappaB-signaling pathways. Carcinogenesis. 2009;30:300–7. https://doi.org/10.1093/carcin/bgn269

    Article  CAS  PubMed  Google Scholar 

  60. Refaat J, Yehia SY, Ramadan MA, Kamel MS. Rhoifolin: a review of sources and biological activities. Int J Pharmacogn. 2015;2:102–9.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pharmacognosy, College of Pharmacy, King Saud University, Riyadh, 11549, Saudi Arabia

    Taghreed A. Ibrahim

  2. Department of Pharmacognosy, Faculty of Pharmacy, Cairo University, Cairo, Egypt

    Taghreed A. Ibrahim

  3. Department of Pharmacognosy, Faculty of Pharmacy, Al-Azhar University, Cairo, 11371, Egypt

    Mostafa M. Hegazy & Atef A. El-Hela

  4. Department of Pharmacognosy, Faculty of Pharmacy, Mansoura University, Mansoura, 35516, Egypt

    Galal T. Maatooq

  5. Department of Pharmacognosy, Faculty of Pharmacy, The Islamic University, Najaf, 54001, Iraq

    Galal T. Maatooq

Authors
  1. Taghreed A. Ibrahim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mostafa M. Hegazy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Galal T. Maatooq
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Atef A. El-Hela
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Taghreed A. Ibrahim.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ibrahim, T.A., Hegazy, M.M., Maatooq, G.T. et al. Ultra-performance liquid chromatography coupled with quadrupole high-resolution time-of-flight mass spectrometry for metabolite profiling and biological activity of Stellaria pallida (Dumort) Piré. Med Chem Res 32, 975–989 (2023). https://doi.org/10.1007/s00044-023-03055-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00044-023-03055-5

Keywords

Search

Navigation