A metabolic profiling approach to an Italian sage leaf extract (SoA541) defines its antioxidant and anti-acetylcholinesterase properties

Journal of Functional Foods

Volumn 29, Issue , 2017, Pages 1-9

  Pacifico, Severina ^a   Piccolella, Simona ^a   Lettieri, Annamaria ^a   Nocera, Paola ^a   Bollino, Flavia ^a   Catauro, Michelina ^a  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

Abietane diterpenes; Antioxidant activity; Cytotoxicity; LC ESI MS MS; Phenols; Salvia officinalis

Indexed keywords

EID: 85002244967     PISSN: 17564646     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jff.2016.11.031     Document Type: Article

References (71)

1. Akhondzadeh, S., Noroozian, M., Mohammadi, M., Ohadinia, S., Jamshidi, A.H., Khani, M., Salvia officinalis extract in the treatment of patients with mild to moderate Alzheimer's disease: A double blind, randomized and placebo-controlled trial. Journal of Clinical Pharmacy and Therapeutics 28 (2003), 53–59.
2. Almela, L., Sánchez-Muñoz, B., Fernández-López, J.A., Roca, M.J., Rabe, V., Liquid chromatograpic–mass spectrometric analysis of phenolics and free radical scavenging activity of rosemary extract from different raw material. Journal of Chromatography A 1120 (2006), 221–229.
3. Arias, E., Gallego-Sandín, S., Villarroya, M., García, A.G., López, M.G., Unequal neuroprotection afforded by the acetylcholinesterase inhibitors galantamine, donepezil, and rivastigmine in SH-SY5Y neuroblastoma cells: Role of nicotinic receptors. Journal of Pharmacology and Experimental Therapeutics 315 (2005), 1346–1353.
4. Asaduzzaman, M., Uddin, M.J., Kader, M.A., Alam, A.H., Rahman, A.A., Rashid, M.,.. Sadik, G., In vitro acetylcholinesterase inhibitory activity and the antioxidant properties of Aegle marmelos leaf extract: Implications for the treatment of Alzheimer's disease. Psychogeriatrics 14 (2014), 1–10.
5. Atanasov, A.G., Waltenberger, B., Pferschy-Wenzig, E.M., Linder, T., Wawrosch, C., Uhrin, P.,.. Stuppner, H., Discovery and resupply of pharmacologically active plant-derived natural products: A review. Biotechnology Advances 33 (2015), 1582–1614.
6. Ayatollahi, A.M., Ghanadian, M., Att-ur-Rahman, R., Mesaik, M.A., Khalid, A.S., Adeli, F., Methoxylated flavones from Salvia mirzayanii Rech. f. and Esfand with immunosuppressive properties. Iranian Journal of Pharmaceutical Research 14 (2015), 955–960.
7. Bakota, E.L., Winkler-Moser, J.K., Berhow, M.A., Eller, F.J., Vaughn, S.F., Antioxidant activity and sensory evaluation of a rosmarinic acid-enriched extract of Salvia officinalis. Journal of Food Science 80 (2015), C711–C717.
8. 2 synthase-1. Journal of Pharmacology and Experimental Therapeutics 342 (2012), 169–176.
9. Ben Jemia, M., Tundis, R., Maggio, A., Rosselli, S., Senatore, F., Menichini, F.,.. Loizzo, M.R., NMR-based quantification of rosmarinic and carnosic acids, GC–MS profile and bioactivity relevant to neurodegenerative disorders of Rosmarinus officinalis L. extracts. Journal of Functional Foods 5 (2013), 1873–1882.
10. Berim, A., Gang, D.R., Methoxylated flavones: Occurrence, importance, biosynthesis. Phytochemistry Reviews 15 (2016), 363–390.
11. Birtić, S., Dussort, P., Pierre, F.-X., Bily, A.C., Roller, M., Carnosic acid. Phytochemistry 115 (2015), 9–19.
12. Borrás-Linares, I., Stojanović, Z., Quirantes-Piné, R., Arráez-Román, D., Švarc-Gajić, J., Fernández-Gutiérrez, A., Segura-Carretero, A., Rosmarinus officinalis leaves as a natural source of bioactive compounds. International Journal of Molecular Sciences 15 (2014), 20585–20606.
13. Cho, J.K., Ryu, Y.B., Curtis-Long, M.J., Ryu, H.W., Yuk, H.J., Kim, D.W.,.. Park, K.H., Cholinestrase inhibitory effects of geranylated flavonoids from Paulownia tomentosa fruits. Bioorganic and Medicinal Chemistry 20 (2012), 2595–2602.
14. Chun, K.-S., Kundu, J., Chae, I.G., Kundu, J.K., Carnosol: A phenolic diterpene with cancer chemopreventive potential. Journal of Cancer Prevention 19 (2014), 103–110.
15. Cvetkovikj, I., Stefkov, G., Acevska, J., Petreska Stanoeva, J., Karapandzova, M., Stefova, M.,.. Kulevanova, S., Polyphenolic characterization and chromatographic methods for fast assessment of culinary Salvia species from South East Europe. Journal of Chromatography A 1282 (2013), 38–45.
16. D'Abrosca, B., Fiorentino, A., Ricci, A., Scognamiglio, M., Pacifico, S., Piccolella, S., Monaco, P., Structural characterization and radical scavenging activity of monomeric and dimeric cinnamoyl glucose esters from Petrorhagia velutina leaves. Phytochemistry Letters 3 (2010), 38–44.
17. Deshmukh, R., Kaundal, M., Bansal, V., Samardeep, Caffeic acid attenuates oxidative stress, learning and memory deficit in intra-cerebroventricular streptozotocin induced experimental dementia in rats. Biomedicine & Pharmacotherapy 81 (2016), 56–62.
18. Efferth, T., Koch, E., Complex interactions between phytochemicals. The multi-target therapeutic concept of phytotherapy. Current Drug Targets 12 (2011), 122–132.
19. Farjam, M.H., Rustaiyan, A., Ezzatzadeh, E., Jassbi, A.R., Labdane-type diterpene and two flavone from Salvia sharifii Rech. f. and Esfan. and their biological activities. Iranian Journal of Pharmaceutical Research 12 (2013), 295–400.
20. Ferreira, A., Proença, C., Serralheiro, M.L., Araújo, M.E., The in vitro screening for acetylcholinesterase inhibition and antioxidant activity of medicinal plants from Portugal. Journal of Ethnopharmacology 108 (2006), 31–37.
21. Fournomiti, M., Kimbaris, A., Mantzourani, I., Plessas, S., Theodoridou, I., Papaemmanouil, V.,.. Alexopoulos, A., Antimicrobial activity of essential oils of cultivated oregano (Origanum vulgare), sage (Salvia officinalis), and thyme (Thymus vulgaris) against clinical isolates of Escherichia coli, Klebsiella oxytoca, and Klebsiella pneumoniae. Microbial Ecology in Health and Disease, 26, 2015, 23289.
22. Galasso, S., Pacifico, S., Kretschmer, N., Pan, S.-P., Marciano, S., Piccolella, S.,.. Bauer, R., Influence of seasonal variation on Thymus longicaulis C. Presl chemical composition and its antioxidant and anti-inflammatory properties. Phytochemistry 107 (2014), 80–90.
23. Garozzo, D., Impallomeni, G., Spina, E., Linkage analysis in disaccharides by electrospray mass spectrometry. Carbohydrate Research 221 (1991), 253–257.
24. Goozee, K.G., Shah, T.M., Sohrabi, H.R., Rainey-Smith, S.R., Brown, B., Verdile, G., Martins, R.N., Examining the potential clinical value of curcumin in the prevention and diagnosis of Alzheimer's disease. British Journal of Nutrition 115 (2016), 449–465.
25. Habtemariam, S., The therapeutic potential of rosemary (Rosmarinus officinalis) diterpenes for Alzheimer's Disease. Evidence-Based Complementary and Alternative Medicine, 2016, 2680409 2016.
26. Hossain, M.B., Rai, D.K., Brunton, N.P., Martin-Diana, A.B., Barry-Ryan, C., Characterization of phenolics composition in Lamiaceae spices by LC-ESI-MS/MS. Journal of Agricultural and Food Chemistry 58 (2010), 10576–10581.
27. Hou, C.W., Lin, Y.T., Chen, Y.L., Wang, Y.H., Chou, J.L., Ping, L.Y., Jeng, K.C., Neuroprotective effects of carnosic acid on neuronal cells under ischemic and hypoxic stress. Nutritional Neuroscience 15 (2012), 257–263.
28. Hügel, H.M., Jackson, N., Polyphenols for the prevention and treatment of dementia diseases. Neural Regeneration Research 10 (2015), 1756–1758.
29. Ivanović, J., Đilas, S., Jadranin, M., Vajs, V., Babović, N., Petrović, S., Žižović, I., Supercritical carbon dioxide extraction of antioxidants from rosemary (Rosmarinus officinalis L.) and sage (Salvia officinalis L.). Journal of the Serbian Chemical Society 74 (2009), 717–732.
30. Johnson, J.J., Carnosol: A promising anti-cancer and anti-inflammatory agent. Cancer Letters 305 (2011), 1–7.
31. Kennedy, D.O., Pace, S., Haskell, C., Okello, E.J., Milne, A., Scholey, A.B., Effects of cholinesterase inhibiting sage (Salvia officinalis) on mood, anxiety and performance on a psychological stressor battery. Neuropsychopharmacology 31 (2006), 845–852.
32. Kharazian, N., Flavonoid constituents in some species of Salvia L. (Lamiaceae) in Iran. Journal of Sciences Islamic Republic of Iran 25 (2014), 219–227.
33. 25-35-induced Alzheimer's disease model. Nutrition Research and Practice 9 (2015), 480–488.
34. Kontogianni, V.G., Tomic, G., Nikolic, I., Nerantzaki, A.A., Sayyad, N., Stosic-Grujicic, S.,.. Tzakos, A.G., Phytochemical profile of Rosmarinus officinalis and Salvia officinalis extracts and correlation to their antioxidant and anti-proliferative activity. Food Chemistry 136 (2013), 120–129.
35. Lamien-Meda, A., Nell, M., Lohwasser, U., Borner, A., Franz, C., Novak, J., Investigation of antioxidant and rosmarinic acid variation in the sage collection of the genebank in gatersleben. Journal of Agricultural and Food Chemistry 58 (2010), 3813–3819.
36. Lee, Y.K., Yuk, D.Y., Kim, T.I., Kim, Y.H., Kim, K.T., Kim, K.H.,.. Hong, J.T., Protective effect of the ethanol extract of Magnolia officinalis and 4-O-methylhonokiol on scopolamine-induced memory impairment and the inhibition of acetylcholinesterase activity. Journal of Natural Medicines 63 (2009), 274–282.
37. Lu, Y., Foo, L.Y., Polyphenolics of Salvia-a review. Phytochemistry 59 (2002), 117–140.
38. Marcelo, F., Dias, C., Martins, A., Madeira, P.J., Jorge, T., Florêncio, M.H.,.. Rauter, A.P., Molecular recognition of rosmarinic acid from Salvia sclareoides extracts by acetylcholinesterase: A new binding site detected by NMR spectroscopy. Chemistry – A European Journal 19 (2013), 6641–6649.
39. Martins, N., Barros, L., Santos-Buelga, C., Henriquez, M., Silva, S., Ferreira, I.C.F.R., Evaluation of bioactive properties and phenolic compounds in different extracts prepared from Salvia officinalis L. Food Chemistry 170 (2015), 378–385.
40. Mehta, M., Adem, A., Sabbagh, M., New acetylcholinesterase inhibitors for Alzheimer's Disease. International Journal of Alzheimer's Disease, 2012, 2012, 728983.
41. Merad, M., Soufi, W., Ghalem, S., Boukli, F., Baig, M.H., Ahmad, K., Kamal, M.A., Molecular interaction of acetylcholinesterase with carnosic acid derivatives: A neuroinformatics study. CNS & Neurological Disorders - Drug Targets 13 (2014), 440–446.
42. Miroddi, M., Navarra, M., Quattropani, M.C., Calapai, F., Gangemi, S., Calapai, G., Systematic review of clinical trials assessing pharmacological properties of Salvia species on memory, cognitive impairment and Alzheimer's disease. CNS Neuroscience & Therapeutics 20 (2014), 485–495.
43. Morreel, K., Dima, O., Kim, H., Lu, F., Niculaes, C., Vanholme, R.,.. Boerjan, W., Mass spectrometry-based sequencing of lignin oligomers. Plant Physiology 153 (2010), 1464–1478.
44. Ng, Y.P., Or, T.C., Ip, N.Y., Plant alkaloids as drug leads for Alzheimer's disease. Neurochemistry International 89 (2015), 260–270.
45. Orhan, I., Kartal, M., Naz, Q., Ejaz, A., Yilmaz, G., Kan, Y.,.. Choudhary, M.I., Antioxidant and anticholinesterase evaluation of selected Turkish Salvia species. Food Chemistry 103 (2007), 1247–1254.
46. Pacifico, S., Galasso, S., Piccolella, S., Kretschmer, N., Pan, S.-P., Nocera, P.,.. Monaco, P., Winter wild fennel leaves as a source of anti-inflammatory and antioxidant polyphenols. Arabian Journal of Chemistry, 2015, 10.1016/j.arabjc.2015.06.026.
47. Pacifico, S., Gallicchio, M., Lorenz, P., Duckstein, S.M., Potenza, N., Galasso, S.,.. Monaco, P., Neuroprotective potential of Laurus nobilis antioxidant polyphenol-enriched leaf extracts. Chemical Research in Toxicology 27 (2014), 611–626.
48. 2 and Aβ(25–35) oxidative injury in SK-B-NE(C)-2 cells. Journal of Agricultural and Food Chemistry 62 (2014), 11957–11966.
49. Pacifico, S., Piccolella, S., Papale, F., Nocera, P., Lettieri, A., Catauro, M., A polyphenol complex from Thymus vulgaris L. plants cultivated in the Campania Region (Italy): New perspectives against neuroblastoma. Journal of Functional Foods 20 (2016), 253–266.
50. Perry, N.B., Anderson, R.E., Brennan, N.J., Douglas, M.H., Heaney, A.J., McGimpsey, J.A., Smallfield, B.M., Essential oils from dalmatian sage (Salvia officinalis L.): Variations among individuals, plant parts, seasons, and sites. Journal of Agricultural and Food Chemistry 47 (1999), 2048–2054.
51. Perry, E., Howes, M.J., Medicinal plants and dementia therapy: Herbal hopes for brain aging?. CNS Neuroscience & Therapeutics 17 (2011), 683–698.
52. Petiwala, S.M., Johnson, J.J., Diterpenes from rosemary (Rosmarinus officinalis): Defining their potential for anti-cancer activity. Cancer Letters 367 (2015), 93–102.
53. Piccolella, S., Nocera, P., Carillo, P., Woodrow, P., Greco, V., Manti, L.,.. Pacifico, S., An apolar Pistacia lentiscus L. leaf extract: GC-MS metabolic profiling and evaluation of cytotoxicity and apoptosis inducing effects on SHSY5Y and SK-N-BE(2)C cell lines. Food and Chemical Toxicology 95 (2016), 64–74.
54. Pires, C., Martins, N., Carvalho, A.M., Barros, L., Ferreira, I.C.F.R., Phytopharmacologic preparations as predictors of plant bioactivity: A particular approach to Echinacea purpurea (L.) Moench antioxidant properties. Nutrition 32 (2016), 834–839.
55. Qnais, E.Y., Abu-Dieyeh, M., Abdulla, F.A., Abdalla, S.S., The antinociceptive and anti-inflammatory effects of Salvia officinalis leaf aqueous and butanol extracts. Pharmaceutical Biology 48 (2010), 1149–1156.
56. Rodrigues, M.R., Kanazawa, L.K., das Neves, T.L., da Silva, C.F., Horst, H., Pizzolatti, M.G., Santos, A.R., Baggio, C.H., Werner, M.F., Antinociceptive and anti-inflammatory potential of extract and isolated compounds from the leaves of Salvia officinalis in mice. Journal of Ethnopharmacology 139 (2012), 519–526.
57. Rodríguez-Pérez, C., Quirantes-Piné, R., Amessis-Ouchemoukh, N., Madani, K., Segura-Carretero, A., Fernández-Gutierrez, A., A metabolite-profiling approach allows the identification of new compounds from Pistacia lentiscus leaves. Journal of Pharmaceutical and Biomedical Analysis 77 (2013), 167–174.
58. Rungsimakan, S., Rowan, M.G., Terpenoids, flavonoids and caffeic acid derivatives from Salvia viridis L. cvar. Blue Jeans. Phytochemistry 108 (2014), 177–188.
59. Russo, P., Frustaci, A., Del Bufalo, A., Fini, M., Cesario, A., From traditional European medicine to discovery of new drug candidates for the treatment of dementia and Alzheimer's disease: Acetylcholinesterase inhibitors. Current Medicinal Chemistry 20 (2013), 976–983.
60. Santos-Gomes, P.C., Seabra, S.M., Andrade, P.B., Fernandez-Ferreira, M., Phenolic antioxidant compounds produced by in vitro shoots of sage (Salvia officinalis L.). Plant Science 162 (2002), 981–987.
61. Savelev, S.U., Okello, E.J., Perry, E.K., Butyryl- and acetyl-cholinesterase inhibitory activities in essential oils of Salvia species and their constituents. Phytotherapy Research 18 (2004), 315–324.
62. Scholey, A.B., Tildesley, N.T., Ballard, C.G., Wesnes, K.A., Tasker, A., Perry, E.K., Kennedy, D.O., An extract of Salvia (sage) with anticholinesterase properties improves memory and attention in healthy older volunteers. Psychopharmacology (Berl) 198 (2008), 127–139.
63. Umukoro, S., Adewole, F.A., Eduviere, A.T., Aderibigbe, A.O., Onwuchekwa, C., Free radical scavenging effect of donepezil as the possible contribution to its memory enhancing activity in mice. Drug Research 64 (2014), 236–239.
64. Van Dooren, T., Princen, K., De Witte, K., Griffioen, G., Derailed intraneuronal signalling drives pathogenesis in sporadic and familial Alzheimer's disease. BioMed Research International, 2014, 2014, 167024.
65. Vladimir-Knežević, S., Blažeković, B., Kindl, M., Vladić, J., Lower-Nedza, A.D., Brantner, A.H., Acetylcholinesterase inhibitory, antioxidant and phytochemical properties of selected medicinal plants of the Lamiaceae family. Molecules 19 (2014), 767–782.
66. Wolfe, K.L., Liu, R.H., Cellular antioxidant activity (CAA) assay for assessing antioxidants, foods, and dietary supplements. Journal of Agricultural and Food Chemistry 55 (2007), 8896–8907.
67. Wu, Y.-B., Ni, Z.-Y., Shi, Q.-W., Dong, M., Kiyota, H., Gu, Y.-C., Cong, B., Constituents from Salvia species and their biological activities. Chemical Reviews 112 (2012), 5967–6026.
68. Zare Shahneh, F., Valiyari, S., Baradaran, B., Abdolalizadeh, J., Bandehagh, A., Azadmehr, A., Hajiaghaee, R., Inhibitory and cytotoxic activities of Salvia officinalis L. extract on human lymphoma and leukemia cells by induction of apoptosis. Advanced Pharmaceutical Bulletin 3 (2013), 51–55.
69. Zhang, H.-Y., Structure-activity relationships and rational design strategies for radical- scavenging antioxidants. Current Computer - Aided Drug Design 1 (2005), 257–273.
70. Zhang, Y., Smuts, J.P., Dodbiba, E., Rangarajan, R., Lang, J.C., Armstrong, D.W., Degradation study of carnosic acid, carnosol, rosmarinic acid, and rosemary extract (Rosmarinus officinalis L.) assessed using HPLC. Journal of Agricultural and Food Chemistry 60 (2012), 9305–9314.
71. Zimmermann, B.F., Walch, S.G., Tinzoh, L.N., Stühlinger, W., Lachenmeier, D.W., Rapid UHPLC determination of polyphenols in aqueous infusions of Salvia officinalis L. (sage tea). Journal of Chromatography B 879 (2011), 2459–2464.