Evaluation of antioxidant, antidiabetic and anticholinesterase activities of smallanthus sonchifolius landraces and correlation with their phytochemical profiles

International Journal of Molecular Sciences

Volumn 16, Issue 8, 2015, Pages 17696-17718

  Russo, Daniela ^a   Valentão, Patrícia ^b   Andrade, Paula B ^b   Fernandez, Eloy C ^c   Milella, Luigi ^a  

^a UNIVERSITY OF BASILICATA   (Italy)

^b UNIVERSITY OF PORTO   (Portugal)

^c CZECH UNIVERSITY OF LIFE SCIENCES PRAGUE   (Czech Republic)

Author keywords

Anti cholinesterase activity; Anti diabetic activity; Antioxidant activity; Phytochemical profile; Smallanthus sonchifolius

Indexed keywords

ALPHA GLUCOSIDASE; AMYLASE; CAFFEIC ACID; CHLOROGENIC ACID; CHOLINESTERASE; FLAVONOID; GALANTAMINE; PLANT EXTRACT; POLYPHENOL DERIVATIVE; REACTIVE OXYGEN METABOLITE; SMALLANTHUS SONCHIFOLIUS EXTRACT; TANNIN DERIVATIVE; UNCLASSIFIED DRUG; ANTIDIABETIC AGENT; ANTIOXIDANT; CHOLINESTERASE INHIBITOR; GLYCOSIDASE INHIBITOR; NITRIC OXIDE; PHENOL DERIVATIVE; PLANT MEDICINAL PRODUCT;

ALZHEIMER DISEASE; ANTIDIABETIC ACTIVITY; ANTIOXIDANT ACTIVITY; ANTIOXIDANT ASSAY; ARTICLE; CHOLINESTERASE INHIBITION; CONTROLLED STUDY; DPPH RADICAL SCAVENGING ASSAY; FERRIC REDUCING POWER ACTIVITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYPERGLYCEMIA; IC50; LIPID PEROXIDATION; NITRIC OXIDE RADICAL SCAVENGING ACTIVITY; NONHUMAN; PHYTOCHEMISTRY; PRINCIPAL COMPONENT ANALYSIS; SUPEROXIDE RADICAL SCAVENGING ACTIVITY; ANTAGONISTS AND INHIBITORS; ASTERACEAE; CHEMISTRY; DIABETES MELLITUS; DRUG EFFECTS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; PLANT LEAF;

POLYMNIA SONCHIFOLIA; SMALLANTHUS SONCHIFOLIUS;

ALPHA-AMYLASES; ALZHEIMER DISEASE; ANTIOXIDANTS; ASTERACEAE; CHOLINESTERASE INHIBITORS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DIABETES MELLITUS; FLAVONOIDS; GLYCOSIDE HYDROLASE INHIBITORS; HUMANS; HYPOGLYCEMIC AGENTS; LIPID PEROXIDATION; NITRIC OXIDE; PHENOLS; PHYTOCHEMICALS; PLANT EXTRACTS; PLANT LEAVES;

EID: 84938506701     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms160817696     Document Type: Article

References (63)

1. Fernández, E. C.; Viehmannová, I.; Lachman, J.; Milella, L. Yacon (Smallanthus sonchifolius (Poeppig & Endlicher) H. Robinson): A new crop in the central europe. Plant Soil Environ. 2006, 52, 564-570.
2. Milella, L.; Salava, J.; Martelli, G.; Greco, I.; Cusimani, E. F.; Viehmannová, I. Genetic diversity between yacon landraces from different countries based on random amplified polymorphic DNAs. Czech J. Genet. Plant Breed. 2005, 41, 73-78.
3. Ojansivu, I.; Ferreira, C. L.; Salminen, S. Yacon, a new source of prebiotic oligosaccharides with a history of safe use. Trends Food Sci. Technol. 2011, 22, 40-46.
4. Fernandez, E. C.; Rajchl, A.; Lachman, J.; Cizkova, H.; Kvasnicka, F.; Kotikova, Z.; Milella, L.; Voldrich, M. Impact of yacon landraces cultivated in the czech republic and their ploidy on the short-and long-chain fructooligosaccharides content in tuberous roots. LWT Food Sci. Technol. 2013, 54, 80-86.
5. Aybar, M. J.; Sanchez Riera, A. N.; Grau, A.; Sanchez, S. S. Hypoglycemic effect of the water extract of Smallantus sonchifolius (yacon) leaves in normal and diabetic rats. J. Ethnopharmacol. 2001, 74, 125-132.
6. Xiang, Z.; He, F.; Kang, T. G.; Dou, D. Q.; Gai, K.; Shi, Y. Y.; Young-Ho, K.; Dong, F. Anti-diabetes constituents in leaves of Smallanthus sonchifolius. Nat. Prod. Commun. 2010, 5, 95-98.
7. Lachman, J.; Fernández, E. C.; Orsák, M. Yacon (Smallanthus sonchifolia (Poepp. et Endl.) H. Robinson) chemical composition and use-A review. Plant Soil Environ. 2003, 49, 283-290.
8. Schorr, K.; da Costa, F. B. Quantitative determination of enhydrin in leaf rinse extracts and in glandular trichomes of Smallanthus sonchifolius (asteraceae) by reversed-phase high-performance liquid chromatography. Phytochem. Anal. 2005, 16, 161-165.
9. Lebeda, A.; Dolezalova, I.; Valentova, K.; Dziechciarkova, M.; Greplova, M.; Opatova, H.; Ulrichova, J. Biological and chemical variability of maca and yacon. Chem. Listy 2003, 97, 548-556.
10. Valentova, K.; Cvak, L.; Muck, A.; Ulrichova, J.; Simanek, V. Antioxidant activity of extracts from the leaves of Smallanthus sonchifolius. Eur. J. Nutr. 2003, 42, 61-66.
11. Valentova, K.; Sersen, F.; Ulrichova, J. Radical scavenging and anti-lipoperoxidative activities of Smallanthus sonchifolius leaf extracts. J. Agric. Food Chem. 2005, 53, 5577-5582.
12. Simonovska, B.; Vovk, I.; Andrensek, S.; Valentova, K.; Ulrichova, J. Investigation of phenolic acids in yacon (Smallanthus sonchifolius) leaves and tubers. J. Chromatogr. A 2003, 1016, 89-98.
13. Lin, F. Q.; Hasegawa, M.; Kodama, O. Purification and identification of antimicrobial sesquiterpene lactones from yacon (Smallanthus sonchifolius) leaves. Biosci. Biotechnol. Biochem. 2003, 67, 2154-2159.
14. Hostettmann, K.; Borloz. A. U.; Marston, A. Natural product inhibitors of acetylcholinesterase. Curr. Org. Chem. 2006, 10, 825-847.
15. Mukherjee, P. K.; Kumar, V.; Mal, M.; Houghton, P. J. Acetylcholinesterase inhibitors from plants. Phytomedicine 2007, 14, 289-300.
16. Bakirel, T.; Bakirel, U.; Keles, O. U.; Ulgen, S. G.; Yardibi, H. In vivo assessment of antidiabetic and antioxidant activities of rosemary (Rosmarinus officinalis) in alloxan-diabetic rabbits. J. Ethnopharmacol. 2008, 116, 64-73.
17. García-Fontana, B.; Morales-Santana, S.; Longobardo, V.; Reyes-García, R.; Rozas-Moreno, P.; García-Salcedo, J.; Muñoz-Torres, M. Relationship between proinflammatory and antioxidant proteins with the severity of cardiovascular disease in type 2 diabetes mellitus. Int. J. Mol. Sci. 2015, 16, 9469-9483.
18. Luo, Q.; Cai, Y.; Yan, J.; Sun, M.; Corke, H. Hypoglycemic and hypolipidemic effects and antioxidant activity of fruit extracts from Lycium barbarum. Life Sci. 2004, 76, 137-149.
19. Gupta, R.; Gigras, P.; Mohapatra, H.; Goswami, V. K.; Chauhan, B. Microbial α-amylases: A biotechnological perspective. Process Biochem. 2003, 38, 1599-1616.
20. Anam, K.; Widharna, R. M.; Kusrini, D. α-Glucosidase inhibitor of Terminalia species. Int. J. Pharmacol. 2009, 5, 277-280.
21. Fred-Jaiyesimi, A.; Kio, A.; Richard, W. α-Amylase inhibitory effect of 3β-olean-12-en-3-yl (9Z)-hexadec-9-enoate isolated from Spondias mombin leaf. Food Chem. 2009, 116, 285-288.
22. Valko, M.; Leibfritz, D.; Moncol, J.; Cronin, M. T. D.; Mazur, M.; Telser, J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell B 2007, 39, 44-84.
23. Scherer, R.; Godoy, H. T. Effects of extraction methods of phenolic compounds from Xanthium strumarium L. and their antioxidant activity. Rev. Bras. Plant. Med. 2014, 16, 41-46.
24. Naczk, M.; Pegg, R. B.; Amarowicz, R. Protein-precipitating capacity of bearberry-leaf (Arctostaphylos uva-ursi L. Sprengel) polyphenolics. Food Chem. 2011, 124, 1507-1513.
25. Hagerman, A. E.; Butler, L. G. Protein precipitation method for the quantitative determination of tannins. J. Agric. Food Chem. 1978, 26, 809-812.
26. Rajanandh, M. G.; Kavitha, J. Quantitative estimation of β-sitosterol, total phenolic and flavonoid compounds in the leaves of Moringa oleifera. Int. J. PharmTech Res. 2010, 2, 1409-1414.
27. Edewor, T. I.; Akpor, O. B.; Owa, S. O. Quantification of the total phenolic and flavonoid contents, and antibacterial activity of Dioclea reflexa. Int. J. PharmTech Res. 2014, 6, 1875-1880.
28. Hagerman, A. E. Radial diffusion method for determining tannin in plant extracts. J. Chem. Ecol. 1987, 13, 437-449.
29. Condelli, N.; Caruso, M. C.; Galgano, F.; Russo, D.; Milella, L.; Favati, F. Prediction of the antioxidant activity of extra virgin olive oils produced in the mediterranean area. Food Chem 2015, 177, 233-239.
30. Jimenez-Escrig, A.; Jimenez-Jimenez, I.; Sanchez-Moreno, C.; Saura-Calixto, F. Evaluation of free radical scavenging of dietary carotenoids by the stable radical 2, 2-diphenyl-1-picrylhydrazyl. J. Sci. Food Agric. 2000, 80, 1686-1690.
31. Brune, B. Nitric oxide: No apoptosis or turning it on? Cell Death Differ. 2003, 10, 864-869.
32. Marcocci, L.; Maguire, J. J.; Droy-Lefaix, M. T.; Packer, L. The nitric oxide-scavenging properties of Ginkgo biloba extract EGb 761. Biochem. Biophys. Res. Commun. 1994, 201, 748-755.
33. Ferreres, F.; Gil-Izquierdo, A.; Vinholes, J.; Silva, S. T.; Valentão, P.; Andrade, P. B. Bauhinia forficata link authenticity using flavonoids profile: Relation with their biological properties. Food Chem. 2012, 134, 894-904.
34. Kussmaul, L.; Hirst, J. The mechanism of superoxide production by NADH: ubiquinone oxidoreductase (complex I) from bovine heart mitochondria. Proc. Natl. Acad. Sci. USA 2006, 103, 7607-7612.
35. De Zwart, L. L.; Meerman, J. H.; Commandeur, J. N.; Vermeulen, N. P. Biomarkers of free radical damage applications in experimental animals and in humans. Free Radic. Biol. Med. 1999, 26, 202-226.
36. Gutteridge, J. M.; Halliwell, B. The measurement and mechanism of lipid peroxidation in biological systems. Trends Biochem. Sci. 1990, 15, 129-135.
37. Halliwell, B.; Chirico, S. Lipid peroxidation: Its mechanism, measurement, and significance. Am. J. Clin. Nutr. 1993, 57, 715S-724S.
38. Corongiu, F. P.; Banni, S. Detection of conjugated dienes by second derivative ultraviolet spectrophotometry. Methods Enzymol. 1994, 233, 303-310.
39. Suba, V.; Murugesan, T.; Arunachalam, G.; Mandal, S. C.; Saha, B. P. Antidiabetic potential of Barleria lupulina extract in rats. Phytomedicine 2004, 11, 202-205.
40. Ahmad, S.; Ullah, F.; Ayaz, M.; Sadiq, A.; Imran, M. Antioxidant and anticholinesterase investigations of Rumex hastatus d. Don: Potential effectiveness in oxidative stress and neurological disorders. Biol. Res. 2015, 48, 20.
41. Ellman, G. L.; Courtney, K. D.; Andres, V., Jr.; Feather-Stone, R. M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 1961, 7, 88-95.
42. Genta, S. B.; Cabrera, W. M.; Mercado, M. I.; Grau, A.; Catalan, C. A.; Sanchez, S. S. Hypoglycemic activity of leaf organic extracts from Smallanthus sonchifolius: Constituents of the most active fractions. Chem. Biol. Interact. 2010, 185, 143-152.
43. Yang, H. Y.; Du, G.; Cheng, X. M.; Yang, X. X.; Liu, M. H.; Dai, Y. Determination of rutin and quercetin in extraction of leaves of yacon with ethanol by using HPLC. Food Res. Dev. 2008, 9, 119-121.
44. Oliveira, R. B.; Chagas-Paula, D. A.; Secatto, A.; Gasparoto, T. H.; Faccioli, L. H.; Campanelli, A. P.; da Costa, F. B. Topical anti-infl ammatory activity of yacon leaf extracts. Res. Bras. Pharmacogn. 2013, 23, 497-505.
45. Russo, D.; Malafronte, N.; Frescura, D.; Imbrenda, G.; Faraone, I.; Milella, L.; Fernandez, E.; de Tommasi, N. Antioxidant activities and qualiquantitative analysis of different Smallanthus sonchifolius ((Poepp. and Endl.) H. Robinson) landrace extracts. Nat. Prod. Res. 2014, 23, 1-5.
46. Valentão, P.; Fernandes, E.; Carvalho, F.; Andrade, P. B.; Seabra, R. M.; Bastos, M. L. Antioxidative properties of cardoon (Cynara cardunculus L.) infusion against superoxide radical, hydroxyl radical, and hypochlorous acid. J. Agric. Food Chem. 2002, 50, 4989-4993.
47. Yan, X.; Suzuki, M.; Ohnishi-Kameyama, M.; Sada, Y.; Nakanishi, T.; Nagata, T. Extraction and identification of antioxidants in the roots of yacon (Smallanthus sonchifolius). J. Agric. Food Chem. 1999, 47, 4711-4713.
48. Sun, T.; Tanumihardjo, S. A. An integrated approach to evaluate food antioxidant capacity. J. Food Sci. 2007, 72, 159-165.
49. Fernandes, F.; Ramalhosa, E.; Pires, P.; Verdial, J.; Valentão, P.; Andrade, P. A.; Bento, A.; Pereira, J. A. Vitis vinifera leaves towards bioactivity. Ind. Crop. Prod. 2013, 43, 434-440.
50. Lim, Y. J.; Oh, C. S.; Park, Y. D.; Eom, S. H.; Kim, D. O.; Kim, U. J.; Cho, Y. S. Physiological components of kiwifruits with in vitro antioxidant and acetylcholinesterase inhibitory activities. Food Sci. Biotechnol. 2014, 23, 943-949.
51. Panceri, C. P.; Gomes, T. M.; de Gois, J. S.; Borges, D. L. G.; Bordignon-Luiz, M. T. Effect of dehydration process on mineral content, phenolic compounds and antioxidant activity of cabernet sauvignon and merlot grapes. Food Res. Int. 2013, 54, 1343-1350.
52. Oszmiański, J.; Nowicka, P.; Teleszko, M.; Wojdyło, A.; Cebulak, T.; Oklejewicz, K. Analysis of phenolic compounds and antioxidant activity in wild blackberry fruits. Int. J. Mol. Sci. 2015, 16, 14540-14553.
53. Svobodova, E.; Dvorakova, Z.; Cepkova, P. H.; Viehmannova, I.; Havlickova, L.; Cusimamani, E. F.; Russo, D.; Zela, G. M. Genetic diversity of yacon (Smallanthus sonchifolius (Poepp. & Endl.) H. Robinson) and its wild relatives as revealed by ISSR markers. Biochem. Syst. Ecol. 2013, 50, 383-389.
54. Milella, L.; Martelli, G.; Salava, J.; Fernandez, E.; Ovesna, J.; Greco, I. Total phenolic content, RAPDs, AFLPs and morphological traits for the analysis of variability in Smallanthus sonchifolius. Genet. Resour. Crop Evol. 2011, 58, 545-551.
55. Milella, L.; Caruso, M.; Galgano, F.; Favati, F.; Padula, M. C.; Martelli, G. Role of the cultivar in choosing clementine fruits with a high level of health-promoting compounds. J. Agric. Food Chem. 2011, 59, 5293-5298.
56. Lobo, R.; Sodde, V.; Dashora, N.; Gupta N.; Prabhu, K. Quantification of flavonoid and phenol content from Macrosolen parasiticus (L.) Danser. J. Nat. Prod. Plant Resour. 2011, 11, 96-99.
57. Russo, D.; Bonomo, M. G.; Salzano, G.; Martelli, G.; Milella, L. Nutraceutical properties of Citrus clementina juices. Pharmacologyonline 2012, 1, 84-93.
58. Milella, L.; Bader, A.; de Tommasi, N.; Russo, D.; Braca, A. Antioxidant and free radical-scavenging activity of constituents from two scorzonera species. Food Chem. 2014, 160, 298-304.
59. Ferreres, F.; Lopes, G.; Gil-Izquierdo, A.; Andrade, P. B.; Sousa, C.; Mouga, T.; Valentão, P. Phlorotannin extracts from fucales characterised by HPLC-DAD-ESI-MSn: Approaches to hyaluronidase inhibitory capacity and antioxidant properties. Mar. Drugs 2012, 10, 2766-2781.
60. Ranilla, L. G.; Kwon, Y. I.; Apostolidis, E.; Shetty, K. Phenolic compounds, antioxidant activity and in vitro inhibitory potential against key enzymes relevant for hyperglycemia and hypertension of commonly used medicinal plants, herbs and spices in Latin America. Bioresour. Technol. 2010, 101, 4676-4689.
61. Vinholes, J.; Grosso, C.; Andrade, P. B.; Gil-Izquierdo, A.; Valentão, P.; de Pinho, P. G.; Ferreres, F. In vitro studies to assess the antidiabetic, anti-cholinesterase and antioxidante potential of Spergularia rubra. Food Chem. 2011, 129, 454-462.
62. Takenaka, M.; Yan, X.; Ono, H.; Yoshida, M.; Nagata, T.; Nakanishi, T. Caffeic acid derivatives in the roots of yacon (Smallanthus sonchifolius). J. Agric. Food Chem. 2003, 51, 793-796.
63. Seabra, R. M.; Andrade, P. B.; Valentão, P.; Fernandes, E.; Carvalho, F.; Bastos, M. L. Antioxidant compounds extracted from several plant materials. In Biomaterials from Aquatic and Terrestrial Organisms; Fingerman, M., Nagabhushanam R., Eds; Science Publishers: Enfield, NH, USA, 2006; pp. 115-174.