The marine halophytes Carpobrotus edulis L. and Arthrocnemum macrostachyum L. are potential sources of nutritionally important PUFAs and metabolites with antioxidant, metal chelating and anticholinesterase inhibitory activities

Botanica Marina

Volumn 55, Issue 3, 2012, Pages 281-288

  Custódio, Luísa ^a   Ferreira, Ana Catarina ^a   Pereira, Hugo ^a   Silvestre, Laura ^a   Vizetto Duarte, Catarina ^a   Barreira, Luísa ^a   Rauter, Amèlia Pilar ^b   Alberício, Fernando ^c,d,e   Varela, João ^a  

^a UNIVERSITY OF ALGARVE   (Portugal)

^b UNIVERSITY OF LISBON   (Portugal)

^c INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^d BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^e UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Alzheimer ' s disease; Halophytes; Lipids; Neuroprotection; Oxidative stress; Polyunsaturated fatty acids

Indexed keywords

ANTIOXIDANT; CHELATING AGENT; ENZYME ACTIVITY; FATTY ACID; GRASS; HEAVY METAL; INHIBITOR; MARINE ENVIRONMENT; METABOLITE; OXIDATION; PLANT EXTRACT;

EID: 84867822915     PISSN: 00068055     EISSN: 14374323     Source Type: Journal    
DOI: 10.1515/bot-2012-0098     Document Type: Article

References (76)

1. Ben Hamed, K., A. Castagna, S. Elkahoui, A. Ranieri and C. Abdelly. 2007. Sea fennel (Crithmum maritimum L.) under salinity conditions: a comparison of leaf and root antioxidant responses. Plant Growth Regul. 53 : 185-194.
2. Bouftira, I., C. Abdelly and S. Sfar. 2009. Antioxidant properties of Mesembryanthemum crystallinum and Carpobrotus edulis extracts. Asian J. Chem. 21 : 549-559.
3. Buwa, L.V. and A.J. Afolayan. 2009. Antimicrobial activity of some medicinal plants used for the treatment of tuberculosis in the Eastern Cape Province, South Africa. Afr. J. Biotechnol. 8 : 6683-6687.
4. Cerón, M.C., M.C. García-Malea, J. Rivas, F.G. Acien, J.M. Fernandez, E. Del Río, M.G. Guerrero and E. Molina. 2007. Antioxidant activity of Haematococcus pluvialis cells grown in continuous culture as a function of their carotenoid and fatty acid content. Appl. Microbiol. Biotechnol. 74: 1112-1119.
5. Chokoe, P.K., P. Masoko, M.P. Mokgotho, R.L. Howard and L.J. Mampuru. 2008. Does seasonal variation influence the phytochemical and antibacterial properties of Carpobrotus edulis ? Afr. J. Biotechnol. 7 : 4164-4171.
6. Dai, J. and R.J. Mumper. 2010. Plant phenolics: extraction, analysis and their antioxidant and anticancer properties. Molecules 15 : 7313-7352.
7. Dillard, C.J. and J.B. German. 2000. Phytochemicals: nutraceuticals and human health. J. Sci. Food Agr. 80 : 1744-1756.
8. El-Wahab, R.H.A., M.S. Zaghloul, M. Wafaa, W.M. Kamel and R.A.A. Moustafa. 2008. Diversity and distribution of medicinal plants in North Sinai, Egypt. Afr. J. Environ. Sci. Technol. 2 : 157-171.
9. Ellman, G.L., K.D. Courtney, V. Andres and R.M. Featherstone. 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7 : 88-95.
10. Evans, W.C. 1997. An index of medicinal plants. A text book of pharmacognosy. J and A Churchill, London. 7: 12-14.
11. Fan, L.-Y. and M.-J. Chiu. 2010. Pharmacological treatment for Alzheimer's disease: current approaches and future strategies. Acta Neurol. Taiwan 19 : 228-245.
12. Fang, Z., S.Y. Jeong, H.A. Jung, J.S. Choi, B.S. Min and M.H. Woo. 2010. Anticholinesterase and antioxidant constituents from Gloiopeltis furcate. Chem. Pharm. Bull. 58 : 1236-1239.
13. Filho, J., K. Medeiros, M. Diniz, L. Batista, P. Athayde-Filho, M. Silva and E. da-Cunha. 2006. Natural products inhibitors of the enzyme acetylcholinesterase. Braz. J. Pharm. 16 : 258-285.
14. Flowers, T.J., H.K. Galal and L. Bromham. 2010. Evolution of halophytes: multiple origins of salt tolerance in land plants. Funct. Plant Biol. 37 : 604-612.
15. Gaeta, A. and R.C. Hider. 2005. The crucial role of metal ions in neurodegeneration: the basis for a promising therapeutic strategy. Br. J. Pharm. 146 : 1041-1059.
16. Geraghty, D.P., K.D.K. Ahuja, J. Pittaway, C. Shing, G.A. Jacobson, N. Jager, J. Saša, C. Narkowicz, C.I. Saunders, M. Ball, A. Pinkard, R.R. Vennavaram and M.J. Adams. 2011. In vitro antioxidant, antiplatelet and anti-inflammatory activity of Carpobrotus rossii (pigface) extract. J. Ethnopharmacol. 134 : 97-103.
17. Giacobini, E. 2004. Cholinesterases: New roles in brain function and in Alzheimer's disease. Neurochem. Res. 28 : 515-522.
18. Ginzberg, A., M. Cohen, U.A. Sod-Moriah, S. Shany, A. Rosenstrauch and S.M Arad. 2000. Chickens fed with biomass of the red microalga Porphyridium sp. have reduced blood cholesterol level and modified fatty acid composition in egg yolk. J. Appl. Phycol. 12 : 325-330.
19. Gomes, N.G.M., M.G. Campos, J.M.C. Órfão and C.A.F. Ribeiro. 2009. Plants with neurobiological activity as potential targets for drug discovery. Prog. Neuro-Psychop. 33 : 1372-1389.
20. Guedes, A.C., H.M. Amaro and F.X. Malcata. 2011. Microalgae as sources of high added-value compounds-a brief review of recent work. Biotechnol. Prog. 27: 597-613.
21. Guil-Guerrero, J.L., B. El-Hassan and M.M.R. Fuentes. 2001. Eicosapentaenoic and arachidonic acids purification from the red microalga Porphyridium cruentum. Bioseparation. 9: 299-306.
22. Halliwell, B. 2007. Oxidative stress and cancer: have we moved forward ? Biochem. J. 401 : 1-11.
23. Huang, C.B. and J.L. Ebersole. 2010. A novel bioactivity of omega-3 polyunsaturated fatty acids and their ester derivatives. Mol. Oral Microbiol. 25: 75-80.
24. Igarashi, M., K. Ma, F. Gao, H. Kim, S.I. Rapoport and J. S. Rao. 2011. Disturbed choline plasmalogen and phospholipid fatty acid concentrations in Alzheimer disease prefrontal cortex. J. Alzheimers Dis. 24: 507-517.
25. Julkunen-Tiitto, R. 1985. Phenolic constituents in the leaves of northern willows: methods for the analysis of certain phenolics. J. Agr. Food Chem. 33 : 213-217.
26. Kähkönen, M.P., A.I. Hopia, H.J. Vuorela, J.P. Rauha, K. Pihlaja, T.S. Kujala and M. Heinonen. 1999. Antioxidant activity of plant extracts containing phenolic compounds. J. Agr. Food Chem. 47 : 3954-3962.
27. Ksouri, R., W. Megdiche, A. Debez, H. Falleh, C. Grignon and C. Abdelly. 2007. Salinity effects on polyphenol content and antioxidant activities in leaves of the halophyte Cakile maritima. Plant Physiol. Biochem. 45 : 244-249.
28. Lamaison, L. and A. Carnat. 1990. Teneurs en acide rosmarinique, en dè rivè s hydroxycinnamiques totaux et activitè s antioxydantes chez les Apiacè es, les Borraginacè es et les Lamiacè es mè dicinales. Pharm. Acta Helv. 65: 315-320.
29. Lepage, G. and C.C. Roy. 1984. Improved recovery of fatty acid through direct transesterification without prior extraction or purification. J. Lipid Res. 25 : 1391-1396.
30. Mace, G.S.L. 1963. Anaerobic bacteriology for clinical laboratories. Pharmacognosy 23 : 89-91.
31. Martins, M., D. Ordway, M. Kristiansen, M. Viveiros, C. Leandro, J. Molnar and L. Amaral. 2005. Inhibition of the Carpobrotus edulis methanol extract on the growth of phagocytosed multidrugresistant Mycobacterium tuberculosis and methicillin-resistant Staphylococcus aureus. Fitoterapia 76 : 96-99.
32. Martins, A., A. Vasas, Z. Schelz, M. Viveiros, J. Molnár and L. Amaral. 2010. Constituents of Carpobrotus edulis inhibit P-glycoprotein of mdr1-transfected mouse lymphoma cells. Anticancer Res. 30 : 829-835.
33. Martins, A., A. Vasas, M. Viveiros, J. Molnárd, J. Hohmann and L. Amaral. 2011. Antibacterial properties of compounds isolated from C arpobrotus edulis. Int. J. Antimicrob. Agents 37: 438-444.
34. Mathabe, M.C., R.V. Nikolova, N. Lall and N.Z. Nyazema. 2006. Antibacterial activities of medicinal plants used for treatment of diarrhoea in Limpopo Province, South Africa. J. Ethnopharmacol. 105 : 286-293.
35. Mathew, N., M.G. Anitha, T.S.L. Bala, S.M. Sivakumar, R. Narmadha and M. Kalyanasundaram. 2009. Larvicidal activity of Saraca indica, Nyctanthes arbor-tristis, and Clitoria ternatea extracts against three mosquito vector species. Parasitol. Res. 104 : 1017-1025.
36. Megías, C., E. Pastor-Cavada, C. Torres-Fuentes, J. Girón-Calle, M. Alaiz, R. Jua, J. Pastor and J. Vioque. 2009. Chelating, antioxidant and antiproliferative activity of Vicia sativa polyphenol extracts. Eur. Food Res. Technol. 230 : 353-359.
37. Meot-Duros, L., G. Le Floch and C. Magnè. 2008. Radical scavenging, antioxidant and antimicrobial activities of halophytic species. J. Ethnopharmacol. 116 : 258-262.
38. Mesulam, M., A. Guillozet, P. Shaw and B. Quinn. 2002. Widely spread butyrylcholinesterase can hydrolyze acetylcholine in the normal and Alzheimer brain. Neurobiol. Dis. 9 : 88-93.
39. Møller, I.M. 2001. Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52 : 561-591.
40. Moreno, S., T. Scheyer, C. Romano and A. Vojnov. 2006. Antioxidant and antimicrobial activities of rosemary extracts linked to their polyphenol composition. Free Radical Res. 40 : 223-31.
41. Mozaffarian, D. and J.H.Y. Wu. 2011. Omega-3 fatty acids and cardiovascular disease effects on risk factors, molecular pathways, and clinical events. J. Am. Coll. Cardiol. 58: 2047-2067.
42. Mukherjee, P.K., V. Kumar, M. Mal and P.J. Houghton. 2007. Acetylcholinesterase inhibitors from plants. Phytomedicine 14 : 289-300.
43. Natarajan, S., K.P. Shanmugiahthevar and P.D. Kasi. 2009. Cholinesterase inhibitors from Sargassum and Gracilaria gracilis : seaweeds inhabiting South Indian coastal areas (Hare Island, Gulf of Mannar). Nat. Prod. Res. 23: 355-369.
44. Ojima, I. 2009. Novel taxoid-based tumour-targeting drug conjugates. Chim. Oggi. 27: 54-56.
45. Ordoñez, A.A.L., J.D. Gomez, M.A. Vattuone and M.I. Isla. 2006. Antioxidant activities of Sechium edule (Jacq.) Swartz extracts. Food Chem. 97 : 452-458.
46. Ordway, D., J. Hohmann, M. Viveiros, A. Viveiros, J. Molnar, C. Leandro, M.J. Arroz, M.A. Gracio and L. Amaral. 2003. Carpobrotus edulis methanol extract inhibits the MDR efflux pumps, enhances killing of phagocytosed S. aureus and promotes immune modulation. Phytother. Res. 17 : 512-519.
47. Orhan, I., M. Kartal, Q. Naz, A. Ejaz, G. Yilmaz, Y. Kan, B. Konuklugil, B. Şener and M.I. Choudhary. 2007. Antioxidant and anticholinesterase evaluation of selected Turkish Salvia species. Food Chem. 103 : 1247-1254.
48. Pietta, P.G. 2000. Flavonoids as antioxidants. J. Nat. Prod. 63 : 1035-1042.
49. Plaza, M., M. Herrero, A. Cifuentes and Ibáñez, E. 2009. Innovative natural functional ingredients from microalgae. J. Agric. Food Chemi. 57: 7159-7170.
50. Price, A. and G. Hendry. 1991. Iron catalysed oxygen radical formation and its possible contribution to drought damage in nine native grasses and three cereals. Plant Cell Environ. 14 : 477-484.
51. Pulok, K.M., K. Venkatesan, M. Mainak and P.J. Houghton. 2007. Acetylcholinesterase inhibitors from plants. Phytomedicine 14 : 289-300.
52. Pulz, O. and W. Gross. 2004. Valuable products from biotechnology of microalgae. Appl Microbiol. Biotechnol. 65: 635-648.
53. Qureshi, G.A. and H.S. Parvez. 2007. Oxidative stress and neurodegenerative disorders. (1st ed.). Elsevier, Dordrecht, Netherlandds. pp 772.
54. Redondo-Gómez, S., E. Mateos-Naranjo, M.E. Figueroa and J. Davy. 2010a. Salt stimulation of growth and photosynthesis in an extreme halophyte, Arthrocnemum macrostachyum. Plant Biol. 12 : 79-87.
55. Redondo-Gómez, S., E. Mateos-Naranjo and L. Andrades-Moreno. 2010b. Accumulation and tolerance characteristics of cadmium in a halophytic Cd-hyperaccumulator, Arthrocnemum macrostachyum. J. Hazard Mater. 15 : 299-307.
56. Sayre, L.M., D.A. Zelasko, P.L.R. Harris, G. Perry, R.G. Salomon and M.A. Smith. 1997. 4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease. J. Neurochem. 68 : 2092-2097.
57. Schmitz, G. and J. Ecker. 2008. The opposing effects ofn-3 and n-6 fatty acids. Prog. Lipid Res. 47: 147-155.
58. Scott, G. and M.L. Hewett. 2008. Pioneers in ethnopharmacology: The Dutch East India Company (VOC) at the Cape from 1650 to 1800. J. Ethnopharmacol. 115 : 339-360.
59. Smith, M.T., N.R. Crouch, N. Gericke and M. Hirst. 1996. Psychoactive constituents of the genus Sceletium N.E.Br. and other Mesembryanthemaceae : a review. J. Ethnopharmacol. 50 : 119-130.
60. Springfield, E.P., G. Amabeoku, F. Weitz, W. Mabusela and Q. Johnson. 2003. An assessment of two Carpobrotus species extracts as potential antimicrobial agents. Phytomedicine 10 : 434-439.
61. Thring, T.S.A. and F.M. Weitz. 2006. Medicinal plant use in the Bredasdorp/Elim region of the Southern Overberg in the Western Cape Province of South Africa. J. Ethnopharmacol. 103 : 261-275.
62. Trim, A.R. and R. Hill. 1952. The preparation and properties of aucubin, asperuloside and some related glycosides. Biochem. J. 50 : 310-319.
63. Tully, A.M., H.M. Roche, R. Doyle, C. Fallon, I. Bruce, B. Lawlor, D. Coakley and M.J. Gibney. 2003. Low serum cholesteryl esterdocosahexaenoic acid levels in Alzheimer's disease: a case-control study. Br. J. Nutr. 89: 483-489.
64. Tundis, R., F. Menichini, F. Conforti, M.R. Loizzo, M. Bonesi, G. Statti and F. Menichini. 2009. A potential role of alkaloid extracts from Salsola species (Chenopodiaceae) in the treatment of Alzheimer's disease. J. Enzym. Inhib. Med. Chem. 24 : 818-824.
65. van der Watt, E. and J.C. Pretorius. 2001. Purification and identification of active antibacterial components in Carpobrotus edulis L. J. Ethnopharmacol. 76 : 87-91.
66. van Wyk, B.E., B. van Oudtshoorn and N. Gericke. 1997. Medicinal plants of South Africa. Briza Publications, Pretoria, South Africa. pp. 304.
67. Velioglu, Y.S., G. Mazza, L. Gao and B.D. Oomah. 1998. Antioxidant activity and total phenolics in selected fruits, vegetables, and grain products. J. Agr. Food Chem. 46 : 4113-4117.
68. Vina, J., A. Lloret, R. Orti and D. Alonso. 2004. Molecular bases of the treatment of Alzheimer's disease with antioxidants: prevention of oxidative stress. Mol. Aspects Med. 25 : 117-123.
69. Vinutha, B., D. Prashanth, K. Salma, S.L. Sreeja, D. Pratiti, R. Padmaja, S. Radhika, A. Amit, K. Venkateshwarlu and M. Deepak. 2007. Screening of selected Indian medicinal plants for acetylcholinesterase inhibitory activity. J. Ethnopharmacol. 109 : 359-363.
70. Wang, D., L.J. Wang, F.X. Zhu, J.Y. Zhu, X.D. Chen, L. Zou, M. Saito and L. Li. 2008. In vitro and in vivo studies on the antioxidant activities of the aqueous extracts of Douchi (a traditional Chinese salt-fermented soybean food). Food Chem. 107 : 1421-1428.
71. Watson, P. 2007. Warming to the ice plants. Tasmanian Nat. 129 : 8-15.
72. Weinreb, O., S. Mandel, O. Bar-Am and T. Amit. 2011. Iron-chelating backbone coupled with monoamine oxidase inhibitory moiety as novel pluripotential therapeutic agents for Alzheimer's disease: a tribute to Moussa Youdim. J. Neural Transm. 118 : 479-492.
73. Wichi, H.P. 1998. Enhanced tumor development by butylated hydroxyanisole (BHA) from the prospective of effect on forestomach and oesophageal squamous epithelium. Food Chem. Toxicol. 26 : 717-723.
74. Williams, G.M.M., J. Iatropoulos and J. Whysner. 1999. Safety assessment of butylated hydroxyanisole and butylated hydroxyltoluene as antioxidant food additives. Food Chem. Toxicol. 37 : 1027-1038.
75. Williams, P., A. Sorribas and M.-J. R. Howes. 2011. Natural products as a source of Alzheimer's drug leads. Nat. Prod. Rep. 28 : 48-77.
76. Willis, L.M., B. Shukitt-Hale and J.A. Joseph. 2009. Dietary polyunsaturated fatty acids improve cholinergic transmission in the aged brain. Genes Nutr. 4: 309-314.