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Evaluation of biological activities of Barbarea integrifolia and isolation of a new glucosinolate derivated compound

  • Merve Badem ORCID logo EMAIL logo , Sıla Ozlem Sener , Seyda Kanbolat , Nuriye Korkmaz , Sermet Yildirmiş , Ufuk Ozgen , Rezzan Aliyazicioglu , Emine Salva , Kübra Kaban , Ali Kandemir and İhsan Calıs ORCID logo
Published/Copyright: April 7, 2021
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Abstract

The aim of the present study is to determine the potent biological activities and carry out isolation studies on Barbarea integrifolia. The antioxidant capacity of the species was evaluated by total phenolic content, FRAP, CUPRAC, and DPPH radical scavenging activity. Anticancer activity studies were performed by MTT assay in MDA-MB-231, MCF-7, Hep3B, PC-3, A549, HCT116, L-929 cell lines. It was observed that the remaining aqueous fraction has higher total phenolic content while higher activity in the CUPRAC and FRAP assays was displayed for the methanolic extract and chloroform fraction. The extracts showed anticancer activity as compared with vincristine. It was observed that chloroform fraction has the highest anticancer activity on MCF-7 cell line, while ethyl acetate fraction has the highest anticancer activity on Hep-3B and A549 cell lines. Methanolic extract has the highest anticancer activity on HCT116 and MDA-MB-23 cell lines. The isolation studies have been performed using several chromatographic methods. The chemical structures of compounds have been identified by means of 1H NMR, 13C NMR, 2D-NMR, and MS. Five major compounds, one steroid (β-Sitosterol), one phenolic acid (Rosmarinic acid), one flavonol heteroside (kaempferol 7-O-α-l-rhamnoside-3-O-β-d-(2-O-β- d -glucosyl)-β-d-glucoside), and two glucosinolates (Gluconasturtiin, Gluconasturtiin choline salt) have been isolated.


Corresponding author: Merve Badem, Department of Biochemistry, Faculty of Pharmacy, Karadeniz Technical University, 61080 Trabzon, Turkey, E-mail:

Funding source: Karadeniz Technical University Scientific Research Projects Unit

Award Identifier / Grant number: THD-2018-7353

Acknowledgments

Merve Badem, Sıla Özlem Şener and Nuriye Korkmaz would like to acknowledge the scholarship by the Scientific and Technological Research Council of Turkey (TÜBİTAK). Also, we would like to acknowledge for the financial support provided by Karadeniz Technical University Scientific Research Project Department.

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: The study was financially supported by Karadeniz Technical University Scientific Research Projects Unit under the grant “THD-2018-7353”.

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

References

1. Baytop, T. Therapy with medicinal plants in Turkey (past and present). Istanbul: Istanbul University Publications; 1984.Search in Google Scholar

2. Özbuçak, T, Kutbay, HG, Ergen Akcin, Ö. The contribution of wild edible plants to human nutrition in the Black Sea Region of Turkey. Ethnobot Leaflets 2006;10:98–103.Search in Google Scholar

3. Greer, MA, Whallon, J. Antithyroid effect of barbarin, a naturally-occurring compound from Barbarea. Proc Soc Exp Biol Med 1961;107:802–4. https://doi.org/10.3181/00379727-107-26760.Search in Google Scholar PubMed

4. Seo, B, Yun, J, Lee, S, Kim, M, Hwang, K, Kim, J, et al.. Barbarin as a new tyrosinase inhibitor from Barbarea orthocerus. Planta Med 1999;65:683–6. https://doi.org/10.1055/s-1999-14092.Search in Google Scholar PubMed

5. Hur, J, Yoo, M, Shin, DB, Lee, S. Inhibition of NO production corresponds to the sulforaphane content in Capsella bursa-pastoris and related species in BV-2 cell. Food Sci Biotechnol 2013;22:1085–9. https://doi.org/10.1007/s10068-013-0187-5.Search in Google Scholar

6. Pedras, MSC, Alavi, M, To, QH. Expanding the nasturlexin family: Nasturlexins C and D and their sulfoxides are phytoalexins of the crucifers Barbarea vulgaris and B. verna. Phytochemistry 2015;118:131–8. https://doi.org/10.1016/j.phytochem.2015.08.009.Search in Google Scholar PubMed

7. Ribnicky, DM, Dey, M, Raskin, I. U.S. Patent No. 7,838,045. Washington, DC: U.S. Patent and Trademark Office; 2010.Search in Google Scholar

8. Senatore, F, Dagostin, M, Dini, I. Flavonoid glycosides of Barbarea vulgaris L. (Brassicaceae). J Agric Food Chem 2000;48:2659–62. https://doi.org/10.1021/jf990625k.Search in Google Scholar PubMed

9. Fursa, NS, Litvinenko, VI, Krivenchuk, PE. Flavonoids of Armoracia rusticana and Barbarea arcuata. Chem Nat Compd 1969;5:270–1. https://doi.org/10.1007/bf00683854.Search in Google Scholar

10. Dalby-Brown, L, Olsen, CE, Nielsen, JK, Agerbirk, N. Polymorphism for novel tetraglycosylated flavonols in an eco-model crucifer, Barbarea vulgaris. J Agric Food Chem 2011;59:6947–56. https://doi.org/10.1021/jf200412c.Search in Google Scholar PubMed

11. Badenes‐Pérez, FR, Reichelt, M, Gershenzon, J, Heckel, D. Phylloplane location of glucosinolates in Barbarea spp. (Brassicaceae) and misleading assessment of host suitability by a specialist herbivore. New Phytol 2011;189:549–56.10.1111/j.1469-8137.2010.03486.xSearch in Google Scholar PubMed

12. Augustin, JM, Bak, SD, Shinoda, T, Sanmiya, K, Nielsen, JK, Khakimov, B, et al.. UDP-glycosyltransferases from the UGT73C subfamily in catalyse sapogenin 3-O-glucosylation in saponin-mediated insect resistance. Plant Physiol 2012;160:1881–95. https://doi.org/10.1104/pp.112.202747.Search in Google Scholar PubMed PubMed Central

13. Nielsen, NJ, Nielsen, J, Staerk, D. New resistance-correlated saponins from the insect-resistant crucifer Barbarea vulgaris. J Agric Food Chem 2010;58:5509–14. https://doi.org/10.1021/jf903988f.Search in Google Scholar PubMed

14. Agerbirk, N, Olsen, CE, Bibby, BM, Frandsen, HO, Brown, LD, Nielsen, JK, et al.. A saponin correlated with variable resistance of Barbarea vulgaris to the diamondback moth Plutella xylostella. J Chem Ecol 2003;29:1417–33. https://doi.org/10.1023/a:1024217504445.10.1023/A:1024217504445Search in Google Scholar

15. Shinoda, T, Nagao, T, Nakayama, M, Serizawa, H, Koshioka, M, Okabe, H, et al.. Identification of a triterpenoid saponin from a crucifer, Barbarea vulgaris, as a feeding deterrent to the diamondback moth, Plutella xylostella. J Chem Ecol 2002;28:587–99. https://doi.org/10.1023/a:1014500330510.10.1023/A:1014500330510Search in Google Scholar

16. Agerbirk, N, De Nicola, GR, Olsen, CE, Müller, C, Iori, R. Derivatization of isothiocyanates and their reactive adducts for chromatographic analysis. Phytochemistry 2015;118:109–15. https://doi.org/10.1016/j.phytochem.2015.06.004.Search in Google Scholar PubMed

17. Kuzina, V, Nielsen, JK, Augustin, JM, Torp, AM, Bak, S, Andersen, SB. Barbarea vulgaris linkage map and quantitative trait loci for saponins, glucosinolates, hairiness and resistance to the herbivore Phyllotreta nemorum. Phytochemistry 2011;72:188–98. https://doi.org/10.1016/j.phytochem.2010.11.007.Search in Google Scholar PubMed

18. Khakimov, B, Amigo, JM, Bak, S, Engelsen, SB. Plant metabolomics: resolution and quantification of elusive peaks in liquid chromatography–mass spectrometry profiles of complex plant extracts using multi-way decomposition methods. J Chromatogr A 2012;1266:84–94. https://doi.org/10.1016/j.chroma.2012.10.023.Search in Google Scholar PubMed

19. Khakimov, B, Tseng, LH, Godejohann, M, Bak, S, Engelsen, SB. Screening for triterpenoid saponins in plants using hyphenated analytical platforms. Molecules 2016;21:1614. https://doi.org/10.3390/molecules21121614.Search in Google Scholar PubMed PubMed Central

20. Fraisse, D, Carnat, A, Viala, D, Pradel, P, Besle, JM, Coulon, JB, et al.. Polyphenolic composition of a permanent pasture: variations related to the period of harvesting. J Sci Food Agric 2007;87:2427–35. https://doi.org/10.1002/jsfa.2918.Search in Google Scholar

21. Agerbirk, N, Olsen, CE. Glucosinolate hydrolysis products in the crucifer Barbarea vulgaris include a thiazolidine-2-one from a specific phenolic isomer as well as oxazolidine-2-thiones. Phytochemistry 2015;115:143–51. https://doi.org/10.1016/j.phytochem.2014.11.002.Search in Google Scholar PubMed

22. Bianco, G, Agerbirk, N, Losito, I, Cataldi, TR. Acylated glucosinolates with diverse acyl groups investigated by high resolution mass spectrometry and infrared multiphoton dissociation. Phytochemistry 2014;100:92–102. https://doi.org/10.1016/j.phytochem.2014.01.010.Search in Google Scholar PubMed

23. Seo, B, Yun, J, Lee, S, Kim, M, Hwang, K, Kim, J, et al.. Barbarin as a new tyrosinase inhibitor from Barbarea orthocerus. Planta Med 1999;65:683–6. https://doi.org/10.1055/s-1999-14092.Search in Google Scholar PubMed

24. Pedras, MSC, Alavi, M, To, QH. Expanding the nasturlexin family: Nasturlexins C and D and their sulfoxides are phytoalexins of the crucifers Barbarea vulgaris and B. verna. Phytochemistry 2015;118:131–8. https://doi.org/10.1016/j.phytochem.2015.08.009.Search in Google Scholar

25. Barillari, J, Gueyrard, D, Rollin, P, Iori, R. Barbarea verna as a source of 2-phenylethyl glucosinolate, precursor of cancer chemopreventive phenylethyl isothiocyanate. Fitoterapia 2001;72:760–4. https://doi.org/10.1016/s0367-326x(01)00320-3.Search in Google Scholar

26. Fahey, JW, Zalcmann, AT, Talalay, P. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 2001;56:5–51. https://doi.org/10.1016/s0031-9422(00)00316-2.Search in Google Scholar

27. Toribio, A, Boudesocque, L, Richard, B, Nuzillard, JM, Renault, JH. Preparative isolation of glucosinolates from various edible plants by strong ion-exchange centrifugal partition chromatography. Separ Purif Technol 2011;83:15–22. https://doi.org/10.1016/j.seppur.2011.07.001.Search in Google Scholar

28. Matthäus, B, Luftmann, H. Glucosinolates in members of the family Brassicaceae: separation and identification by LC/ESI-MS-MS. J Agric Food Chem 2000;48:2234–9. https://doi.org/10.1021/jf991306w.Search in Google Scholar

29. Andersson, AA, Merker, A, Nilsson, P, Sørensen, H, Aman, P. Chemical composition of the potential new oilseed crops Barbarea vulgaris, Barbarea verna and Lepidium campestre. J Sci Food Agric 1999;79:179–86. https://doi.org/10.1002/(sici)1097-0010(199902)79:2<179::aid-jsfa163>3.0.co;2-n.10.1002/(SICI)1097-0010(199902)79:2<179::AID-JSFA163>3.0.CO;2-NSearch in Google Scholar

30. Badenes‐Pérez, FR, Reichelt, M, Gershenzon, J, Heckel, DG. Phylloplane location of glucosinolates in Barbarea spp. (Brassicaceae) and misleading assessment of host suitability by a specialist herbivore. New Phytol 2011;189:549–56.10.1111/j.1469-8137.2010.03486.xSearch in Google Scholar

31. Agerbirk, N, Olsen, CE, Nielsen, JK. Seasonal variation in leaf glucosinolates and insect resistance in two types of Barbarea vulgaris ssp. arcuata. Phytochemistry 2001;58:91–100. https://doi.org/10.1016/s0031-9422(01)00151-0.Search in Google Scholar

32. Agerbirk, N, Petersen, BL, Olsen, CE, Halkier, BA, Nielsen, JK. 1,4-Dimethoxyglucobrassicin in Barbarea and 4-hydroxyglucobrassicin in Arabidopsis and Brassica. J Agric Food Chem 2001;49:1502–7. https://doi.org/10.1021/jf001256r.Search in Google Scholar

33. Agerbirk, N, Olsen, CE, Heimes, C, Christensen, S, Bak, S, Hauser, TP. Multiple hydroxyphenethyl glucosinolate isomers and their tandem mass spectrometric distinction in a geographically structured polymorphism in the crucifer Barbarea vulgaris. Phytochemistry 2015;115:130–42. https://doi.org/10.1016/j.phytochem.2014.09.003.Search in Google Scholar

34. Singleton, VL, Rossi, JA. Colorimetry of total phenolics with phosphomolybdic–phosphotungstic acid reagents. Am J Enol Vitic 1965;16:144–58. 69.10.5344/ajev.1965.16.3.144Search in Google Scholar

35. Benzie, IFF, Strain, JJ. Ferric reducing/antioxidant power assay: direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods Enzymol 1999;299:15–27. https://doi.org/10.1016/s0076-6879(99)99005-5.Search in Google Scholar

36. Apak, R, Güçlü, K, Demirata, B, Özyürek, M, Çelik, ES, Bektaşoğlu, B, et al.. Comparative evaluation of various total antioxidant capacity assays applied to phenolic compounds with the CUPRAC assay. Molecules 2007;12:1496–547. https://doi.org/10.3390/12071496.Search in Google Scholar PubMed PubMed Central

37. Albayrak, S, Sağdıç, O, Aksoy, A. Bitkisel ürünlerin ve gıdaların antioksidan kapasitelerinin belirlenmesinde kullanılan yöntemler. Erciyes Üniversitesi Fen Bilimleri. Enstitüsü Dergisi 2010;26:401–9.Search in Google Scholar

38. Güvenalp, Z. Centranthus longiflorus subsp. longiflorus bitkisi üzerinde fitokimyasal araştırmalar. Doktora tezi. Erzurum: Atatürk Üniversitesi Fen Bilimleri Enstitüsü; 1999.Search in Google Scholar

39. Boğa, M. Cirsium leucopsis ve Cirsium sipyleum Bitkilerinden Sekonder Metabolitlerin Saflaştırılması, Antioksidan ve Antikolinesteraz Aktivitelerinin Belirlenmesi. Doktora tezi. İstanbul: İstanbul Üniversitesi Sağlık Bilimleri Enstitüsü; 2012.Search in Google Scholar

40. Ferlinahayati, F, Gultom, RPJ, Herlina, H, Eliza, E. Steroıd compounds from Gynura pseudochina (Lour) DC. Molekul 2017;12:8–13. https://doi.org/10.20884/1.jm.2017.12.1.293.Search in Google Scholar

41. Karaoğlan Sezen, E. Bazı Origanum türleri üzeinde farmakognozik çalışmalar. Doktora tezi. Erzurum: Atatürk Üniversitesi Sağlık Bilimleri Enstitüsü; 2011.Search in Google Scholar

42. Rösch, D, Krumbein, A, Mügge, C, Kroh, LW. Structural investigations of flavonol glycosides from sea buckthorn (Hippophaë rhamnoides) pomace by NMR spectroscopy and HPLC-ESI-MS. J Agric Food Chem 2004;52:4039–46. https://doi.org/10.1021/jf0306791.Search in Google Scholar PubMed

43. Agerbirk, N, Warwick, SI, Hansen, PR, Olsen, CE. Sinapis phylogeny and evolution of glucosinolates and specific nitrile degrading enzymes. Phytochemistry 2008;69:2937–49. https://doi.org/10.1016/j.phytochem.2008.08.014.Search in Google Scholar PubMed

44. İbrahim, N, Allart Simon, I, De Nicola, GR, Iori, R, Renault, JH, Rollin, P, et al.. Advanced NMR-based structural investigation of glucosinolates and desulfoglucosinolates. J Nat Prod 2018;81:323–34. https://doi.org/10.1021/acs.jnatprod.7b00776.Search in Google Scholar PubMed

45. Çalış, İ, Güvenç, A, Armağan, M, Koyuncu, M, Gotfredsen, CH, Jensen, SR. Iridoid glucosides from Eremostachys moluccelloides Bunge. Helv Chim Acta 2007;90:1461–6.10.1002/hlca.200790150Search in Google Scholar

46. Agneta, R, Rivelli, AR, Ventrella, E, Lelario, F, Sarli, G, Bufo, SA. Investigation of glucosinolate profile and qualitative aspects in sprouts and roots of horseradish (Armoracia rusticana) using LC-ESI–hybrid linear ion trap with Fourier transform ion cyclotron resonance mass spectrometry and infrared multiphoton dissociation. J Agric Food Chem 2012;60:7474–82. https://doi.org/10.1021/jf301294h.Search in Google Scholar PubMed

47. Badem, M, Sener, SO, Korkmaz, N, Kanbolat, S, Yildirmiş, S, Ozgen, U, et al.. Phenolic content and enzyme inhibition activities Barbarea auriculata var. paludosa, B. integrifolia and B. plantaginea (Brassicaceae)’s. J Pharm Res Int 2020:86–93. https://doi.org/10.9734/jpri/2020/v32i930486.Search in Google Scholar

48. Kuzina, V, Nielsen, JK, Augustin, JM, Torp, AM, Bak, S, Andersen, SB. Barbarea vulgaris linkage map and quantitative trait loci for saponins, glucosinolates, hairiness and resistance to the herbivore Phyllotreta nemorum. Phytochemistry 2011;72:188–98. https://doi.org/10.1016/j.phytochem.2010.11.007.Search in Google Scholar PubMed

49. Perocco, P, Iori, R, Barillari, J, Broccoli, M, Sapone, A, Affatato, A, et al.. In vitro induction of benzo (a) pyrene cell-transforming activity by the glucosinolate gluconasturtiin found in cruciferous vegetables. Cancer Lett 2002;184:65–71. https://doi.org/10.1016/s0304-3835(02)00194-5.Search in Google Scholar

50. Okulicz, M, Bialik, I, Chichłowska, J. The time‐dependent effect of gluconasturtiin and phenethyl isothiocyanate on metabolic and antioxidative parameters in rats. J Anim Physiol Anim Nutr 2005;89:367–72. https://doi.org/10.1111/j.1439-0396.2005.00523.x.Search in Google Scholar

51. Chung, L, Kelloff, G, Steele, V, Pittman, B, Zang, E, Jiao, D, et al.. Chemopreventive efficacy of arylalkyl isothiocyanates and N-acetylcysteine for lung tumorigenesis in Fischer rats. Cancer Res 1996;56:772–8.Search in Google Scholar

52. Stoner, GD, Morse, MA. Isothiocyanates and plant polyphenols as inhibitors of lung and esophageal cancer. Cancer Lett 1997;114:113–19. https://doi.org/10.1016/s0304-3835(97)04639-9.Search in Google Scholar

53. Dayalan Naidu, S, Suzuki, T, Yamamoto, M, Fahey, JW, Dinkova Kostova, AT. Phenethyl isothiocyanate, a dual activator of transcription factors NRF2 and HSF1. Mol Nutr Food Res 2018;62:1700908. https://doi.org/10.1002/mnfr.201700908.Search in Google Scholar PubMed PubMed Central

54. Bhatt, R, Mishra, N, Bansal, PK. Phytochemical, pharmacological and pharmacokinetics effects of rosmarinic acid. J Pharm Sci 2013:28–34. https://doi.org/10.7897/2277-4572.02215.Search in Google Scholar

55. Abedini, A, Roumy, V, Mahieux, S, Biabiany, M, Standaert Vitse, A, Riviere, C, et al.. Rosmarinic acid and its methyl ester as antimicrobial components of the hydromethanolic extract of Hyptis atrorubens Poit. (Lamiaceae). Evid Based Complement Alternat Med 2013:2013–24. https://doi.org/10.1155/2013/604536.Search in Google Scholar PubMed PubMed Central

56. Kang, HS, Park, HJ, Kim, HR, Byun, DS, Choi, JS. Rosmarinic acid as a tyrosinase inhibitors from Salvia miltiorrhiza. Nat Prod Sci 2004;10:80–4.Search in Google Scholar

57. Lin, L, Dong, Y, Zhao, H, Wen, L, Yang, B, Zhao, M. Comparative evaluation of rosmarinic acid, methyl rosmarinate and pedalitin isolated from Rabdosia serra as inhibitors of tyrosinase and α-glucosidase. Food Chem 2011;129:884–9. https://doi.org/10.1016/j.foodchem.2011.05.039.Search in Google Scholar PubMed

58. Baskar, AA, Al Numair, KS, Gabriel Paulraj, M, Alsaif, MA, Muamar, MA, Ignacimuthu, S. β-Sitosterol prevents lipid peroxidation and improves antioxidant status and histoarchitecture in rats with 1,2-dimethylhydrazine ninduced colon cancer. J Med Food 2012;15:335–43. https://doi.org/10.1089/jmf.2011.1780.Search in Google Scholar PubMed

59. Sen, A, Dhavan, P, Shukla, KK, Singh, S, Tejovathi, G. Analysis of IR, NMR and antimicrobial activity of β-Sitosterol isolated from Momordica charantia. Sci Secure J Biotechnol 2012;1:9–13.Search in Google Scholar

60. Okello, EJ, Leylabi, R, McDougall, GJ. Inhibition of acetylcholinesterase by green and white tea and their simulated intestinal metabolites. Food Funct 2012;3:651–61. https://doi.org/10.1039/c2fo10174b.Search in Google Scholar PubMed


Supplementary material

The online version of this article offers supplementary material (https://doi.org/10.1515/znc-2020-0305).


Received: 2020-12-25
Accepted: 2021-03-13
Published Online: 2021-04-07
Published in Print: 2021-09-27

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