Skip to main content

Advertisement

SpringerLink
Log in

Biochemical and Molecular Study of Carpobrotus edulis Bioactive Properties and Their Effects on Dugesia sicula (Turbellaria, Tricladida) Regeneration

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

The traditional medicinal properties of Carpobrotus edulis are well recognized, particularly in Tunisia where it is used for wound healing. Thus, in this study, biochemical and molecular properties of its leaves’ bioactive aqueous-acetone extract were investigated. The total phenolic content (TPC) of the extract was estimated to be 184 ± 5 mg/100 g of fresh matter (FM). The qualitative and quantitative polyphenolic profile was determined by ultra performance liquid chromatography with diode array detection (UPLC-DAD) and showed that chlorogenic acid was the major compound (43.7%). The extract exhibits potent antioxidant capacities with IC50 = 56.19 and 58.91 μg/ml, as accessed via the anionic DPPH and cationic ABTS radical scavenging assays, respectively. The extract has high antibacterial properties, especially against the Gram+ Staphylococcus aureus and Bacillus cereus strains. To investigate the extract effect on regeneration, the flatworm Dugesia sicula Lepori, 1948, was used as a model. The macroscopic analysis of planarian cultures in ordinary medium containing phenolic extract at non-toxic concentrations illustrated that the extract caused morphological changes. Additionally, the molecular study through the fluorescence-activated cell sorting (FACS) technique showed that C. edulis polyphenols can harm the stem cells’ development. These results emphasize the ecotoxicological impact of phenolic rejections in the environment on flatworms’ physiology.

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

Similar content being viewed by others

References

  1. Foster, S., Hobbs, C., & Peterson, R. T. (2002). A field guide to western medicinal plants and herbs (p. 448). New York: Houghton Mifflin Co.

    Google Scholar 

  2. Taguri, T., Tanaka, T., & Kouno, I. (2006). Antibacterial spectrum of plant polyphenols and extracts depending upon hydroxyphenyl structure. Biological and Pharmaceutical Bulletin, 29, 2226–2235.

    Article  CAS  Google Scholar 

  3. Puupponen-Pimiä, R., Nohynek, L., Hartman-Schmidlin, S., Kähkönen, M., Heinonen, M., & Mata-Riihinen, K. (2005). Berry phenolics selectively inhibit the growth of intestinal pathogens. Journal of Applied Microbiology, 98, 991–1000.

    Article  Google Scholar 

  4. Novoa, A., & Gonzalez, L. (2014). Impact of Carpobrotus edulis (L.) N.E.Br. on the germination, establishment and survival of native plants: a clue for assessing its competitive strength. PlosONE, 9, 1–12.

    Article  Google Scholar 

  5. Martins, A., Vasas, A., Schelz, Z., Viveiros, M., Molnar, J., Hohmann, J., & Amaral, L. (2010). Constituents of Carpobrotus edulis inhibit P-glycoprotein of MDR1-transfected mouse lymphoma cells. Anticancer Research, 30, 829–836.

    CAS  Google Scholar 

  6. Pirie, A. D., Davies, N. W., Ahuja, K. D., Adams, M. J., Shing, C. M., Narkowicz, C., Jacobson, G. A., & Geraghty, D. P. (2014). Hypolipidaemic effect of crude extract from Carpobrotus rossii (pigface) in healthy rats. Food and Chemical Toxicology, 66, 134–139.

    Article  CAS  Google Scholar 

  7. Omoruyi, E. B., Bradley, G., & Afolayan, J. A. (2012). Antioxidant and phytochemical properties of Carpobrotus edulis (L.) bolus leaf used for the management of common infections in HIV/AIDS patients in Eastern Cape Province. BMC Complementary and Alternative Medicine, 12, 215. doi:10.1186/1472-6882-12-215.

    Article  CAS  Google Scholar 

  8. Navneet, K. Y., Pooja, S., Ankur, O., & Singh, R. K. (2013). In silico approach to uncover the anti-cancerous activity of certain phyto-compounds. Gene Therapy & Molecular Biology, 15, 147–158.

    Google Scholar 

  9. Hayashi, T., Asami, M., Higuchi, S., Shibata, N., & Agata, K. (2006). Isolation of planarian X-ray-sensitive stem cells by fluorescence-activated cell sorting. Development Growth and Differentiation, 48, 371–380.

    Article  Google Scholar 

  10. Moritz, S., Stöckle, F., Ortmeier, C., Schmitz, H., Rodríguez-Esteban, G., Key, G., & Gentile, L. (2012). Heterogeneity of planarian stem cells in the S/G2/M phase. The International Journal of Developmental Biology, 56, 117–125.

    Article  CAS  Google Scholar 

  11. Charni, M., Harrath, A. H., Sluys, R., Tekaya, S., & Zghal, F. (2004). The freshwater planarian Dugesia sicula Lepori, 1948 (Platyhelminthes, Tricladida) in Tunisia: ecology, karyology, and morphology. Hydrobiologia, 517(1), 161–170.

    Article  Google Scholar 

  12. Fattouch, S., Caboni, P., Coroneo, V., Tuberoso, C. I. G., Angioni, A., Dessi, S., Marzouki, N., & Cabras, P. (2007). Antimicrobial activity of Tunisian quince (Cydonia oblonga Miller) pulp and peel polyphenolic extracts. Journal of Agricultural and Food Chemistry, 55, 963–969.

    Article  CAS  Google Scholar 

  13. Dhaouadi, K., Raboudi, F., Funez-Gomez, L., Pamies, D., Estevan, C., Hamdaoui, M., & Fattouch, S. (2013). Polyphenolic extract of barbary-fig (Opuntia ficus-indica) syrup: RP–HPLC–ESI–MS analysis and determination of antioxidant, antimicrobial and cancer-cells cytotoxic potentials. Food Analytical Methods, 6, 45–53.

    Article  Google Scholar 

  14. Najjaa, H., Zerria, K., Fattouch, S., Ammar, E., & Neffati, M. (2011). Antioxidant and antimicrobial activities of Allium roseum. “lazoul”, a wild edible endemic species in North Africa. International Journal of Food Properties, 14, 371–380.

    Article  CAS  Google Scholar 

  15. Chen, Z., Wu, J. B., Liao, X. J., Yang, W., & Song, K. (2010). Development and validation of an UPLC–DAD–MS method for the determination of leonurine in Chinese motherwort (Leonurus japonicus). Journal of Chromatographic Science, 48, 802–806.

    Article  CAS  Google Scholar 

  16. Fratianni, F., Coppola, R., & Nazzaro, F. (2011). Phenolic composition and antimicrobial and antiquorum sensing activity of an ethanolic extract of peels from the apple cultivar Annurca. Journal of Medicinal Food, 14(9), 957–963.

    Article  CAS  Google Scholar 

  17. Fratianni, F., Cardinale, F., Cozzolino, A., Granese, T., Albanese, D., Di Matteo, M., Zaccardelli, M., Coppola, R., & Nazzaro, F. (2014). Polyphenol composition and antioxidant activity of different grass pea (Lathyrus sativus), lentils (Lens culinaris), and chickpea (Cicer arietinum) ecotypes of the Campania region (southern Italy). Journal of Functional Foods, 7, 551–557.

    Article  CAS  Google Scholar 

  18. Wilson, M. A., Shukitt-Hale, B., Kalt, W., Ingram, D. K., Joseph, J. A., & Wolkow, C. A. (2006). Blueberry polyphenols increase lifespan and thermotolerance in Caenorhabditis elegans. Aging Cell, 5, 59–68.

    Article  CAS  Google Scholar 

  19. Salvetti, A., Rossi, L., Bonuccelli, L., Lena, A., Pugliesi, C., Rainaldi, G., Evangelista, M., & Gremigni, V. (2009). Adult stem cell plasticity: neoblast repopulation in non-lethally irradiated planarians. Developmental Biology, 328, 305–314.

    Article  CAS  Google Scholar 

  20. Fattouch, S., Caboni, P., Coroneo, V., Tuberoso, C. I. G., Angioni, A., Dessi, S., Marzouki, N., & Cabras, P. (2008). Comparative analysis of polyphenolic profiles and antioxidant and antimicrobial activities of Tunisian pome fruit pulp and peel aqueous acetone extracts. Journal of Agricultural and Food Chemistry., 56, 1084–1090.

    Article  CAS  Google Scholar 

  21. Huang, D. J., Lin, C. D., Chen, H. J., & Lin, Y. H. (2004). Antioxidant and antiproliferative activities of sweet potato (Ipomoea batatas) constituents. Botanical Bulletin- Academia Sinica, 45, 179–186.

    CAS  Google Scholar 

  22. Johnston, K. L., Clifford, M. N., & Morgan, L. M. (2003). Coffee acutely modifies gastrointestinal hormone secretion and glucose tolerance in humans: glycemic effects of chlorogenic acid and caffeine. American Journal of Clinical Nutrition, 78, 728–733.

    CAS  Google Scholar 

  23. Suzuki, A., Yamamoto, N., Jokura, H., Yamamoto, M., Fujii, A., Tokimitsu, I., & Saito, I. (2006). Chlorogenic acid attenuates hypertension and improves endothelial function in spontaneously hypertensive rats. Journal of Hypertension, 24, 1065–1073.

    Article  CAS  Google Scholar 

  24. Koech, K. R., Wachira, F. N., Ngure, R. M., Wanyoko, J. K., Bii, C. C., Karori, S. M., & Keriol, L. C. (2013). Antimicrobial, synergistic and antioxidant activities of tea polyphenols. Microbial pathogens and strategies for combating them: science, technology and education, 6, 971–981.

    Google Scholar 

  25. Prakash, A., Rigelhof, F., & Miller, E. (2001). Antioxidant activity. Medallion Laboratories Analytical Progress, 19, 1–4.

    CAS  Google Scholar 

  26. Bouftira, I., Abdelly, C., & Sfar, S. (2012). Antioxidant and antibacterial properties of Mesembryanthemum crystallinum and Carpobrotus edulis extracts. Advances in Chemical Engineering and Science, 2, 359–365.

    Article  Google Scholar 

  27. Dhaouadi, K., Raboudi, F., Estevan, C., Barrajo, E., Vilanova, E., Hamdaoui, M., & Fattouch, S. (2011). Cell viability effects and antioxidant and antimicrobial activities of Tunisian date syrup (rub el tamer) polyphenolic extracts. Journal of Agricultural and Food Chemistry, 59, 402–406.

    Article  CAS  Google Scholar 

  28. Hattori, M., Kusumoto, I. T., Namba, T., Ishigami, T., & Hara, Y. (1990). Effect of tea polyphenols on glucan synthesis by glucosyltransferase from Streptococcus mutans. Chemical & Pharmaceutical Bulletin, 38, 717–720.

    Article  CAS  Google Scholar 

  29. Zaixiang, L., Hongxin, W., Song, Z., Chaoyang, M., & Zhouping, W. (2011). Antibacterial activity and mechanism of action of chlorogenic acid. Journal of Food Science, 76, M398–M403.

    Article  Google Scholar 

  30. Fernando, C., Cristina, A. L., Sara, T., Francisco, J. T., & María, I. Q. (2013). Benefits of polyphenols on gut microbiota and implications in human health. Journal of Nutritional Biochemistry, 24, 1415–1422.

    Article  Google Scholar 

  31. Sirk, T. W., Friedman, M., & Brown, E. F. (2011). Molecular binding of black tea Theaflavins to biological membranes: relationship to bioactivities. Journal of Agricultural and Food Chemistry, 59, 3780–7787.

    Article  CAS  Google Scholar 

  32. Daglia, M. (2012). Polyphenols as antimicrobial agents. Current Opinion in Biotechnology, 23, 174–181.

    Article  CAS  Google Scholar 

  33. Sakai, F., Agata, K., Orii, H., & Watanabe, K. (2000). Organization and regeneration ability of spontaneous supernumerary eyes in planarians—eye regeneration field and pathway selection by optic nerves. Zoological Science, 17, 375–381.

    CAS  Google Scholar 

  34. Sanchez Alvarado, A., Newmark, P. A., Robb, S. M., & Juste, R. (2002). The Schmidtea mediterranea database as a molecular resource for studying platyhelminthes, stem cells and regeneration. Development, 129, 5659–5665.

    Article  Google Scholar 

  35. Handberg-Thorsager, M., Fernandez, E., & Salo, E. (2008). Stem cells and regeneration in planarians. Frontier Biosciences, 13, 6374–6394.

    Article  CAS  Google Scholar 

  36. Wagner, D. E., Wang, I. E., & Reddien, P. W. (2011). Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science, 332, 811–816.

    Article  CAS  Google Scholar 

  37. Hayashi, T., Shibata, N., Okumura, R., Kudome, T., Nishimura, O., Tarui, H., & Agata, K. (2010). Single-cell gene profiling of planarian stem cells using fluorescent activated cell sorting and its “index sorting” function for stem cell research. Development Growth and Differentiation, 52, 131–144.

    Article  CAS  Google Scholar 

  38. Aloui, S., Raboudi, F., Ghazouani, T., Salghi, R., Hamdaoui, M. H., & Fattouch, S. (2014). Use of molecular and in silico bioinformatic tools to investigate pesticide binding to insect (Lepidoptera) Phenoloxidases (PO): insights to toxicological aspects. Journal of Environmental Science and Health, Part B: Pesticides, Food Contaminants and Agricultural Waste, 49, 654–660.

    Article  CAS  Google Scholar 

  39. Raboudi, F., Fattouch, S., Makni, H., & Makni, M. (2012). Biochemical and molecular analysis of the Pirimicarb effect on Acetylcholinesterase resistance in Tunisian populations of potato aphid Macrosiphum euphorbiae (Hemiptera: Aphididae). Pesticide Biochemistry and Physiology, 104, 261–266.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work has been supported, in part, by a fellowship grant to Emna MEDDEB, by recurrent funding from the Ministry of Higher Education and Scientific Research. We thank Henning Schmitz (Max Planck Institute for Molecular Biomedicine, Münster, Germany) for help with the FACS technique.

Author information

Authors and Affiliations

  1. Laboratory of Protein Engineering and Bioactive-Molecules (LIP-MB), National Institute of Applied Sciences and Technology (INSAT), University of Carthage, Zone Urbaine Nord, 1080, Tunis, Tunisia

    Emna Meddeb, Tesnime Ghazouani & Sami Fattouch

  2. Faculty of Sciences of Bizerte, University of Carthage, Tunis, Tunisia

    Emna Meddeb

  3. Faculty of Sciences of Tunis, University of Tunis El Manar, Tunis, Tunisia

    Mohamed Charni

  4. College of Sciences and Humanities of Dawadmi, Shaqra University, Shangra, Kingdom of Saudi Arabia

    Mohamed Charni

  5. Laboratory of Biotechnology and Food Safety, Istituto di Scienze dell’Alimentazione, ISA-CNR, Avellino, Italy

    Autilia Cozzolino, Florinda Fratianni & Filomena Nazzaro

  6. ISAJC, Bir El Bey, University of Tunis, Tunis, Tunisia

    Faten Raboudi

Authors
  1. Emna Meddeb
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mohamed Charni
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tesnime Ghazouani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Autilia Cozzolino
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Florinda Fratianni
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Faten Raboudi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Filomena Nazzaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sami Fattouch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Emna Meddeb.

Electronic supplementary material

Supplementary Table 1

Antibacterial potentials of the Carpobrotus edulis extracts and Ampicillin as positive control. (DOCX 13 kb)

Supplementary Figure 1

Graphical presentation of the One-way ANOVA of the the Carpobrotus edulis antibacterial potential. (DOCX 45 kb)

Supplementary Figure 2

Planarian in the 7th day of regeneration. A. untreated planarian. B. Planarian treated with 75% MIC. C. Planarian treated with 100% MIC. (DOCX 663 kb)

Supplementary Figure 3

Graphical presentation of the One-way ANOVA of the morphometric characters. (*) Significant results. (DOCX 41 kb)

Supplementary Figure 4

Planarian treated with 15 mg/ml of Carpobrotus edulis polyphenol extract. Eyes are shown by yellow arrows ends. (DOCX 1095 kb)

Supplementary Figure 5

Count different cell populations of irradiated (a), untreated (b) and treated animals with Carpobrotus edulis polyphenols (c). (DOCX 255 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Meddeb, E., Charni, M., Ghazouani, T. et al. Biochemical and Molecular Study of Carpobrotus edulis Bioactive Properties and Their Effects on Dugesia sicula (Turbellaria, Tricladida) Regeneration. Appl Biochem Biotechnol 182, 1131–1143 (2017). https://doi.org/10.1007/s12010-016-2387-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-016-2387-y

Keywords

Search

Navigation