Abstract
A MeOH extract of cultivated Chondrus crispus showed dose-dependent nitric oxide (NO) inhibition of lipopolysaccharide-induced NO production in macrophage RAW264.7 cells. NO inhibition-guided fractionation of the extract led to identification of eicosapentaenoic acid (EPA, 1), arachidonic acid (AA, 2), lutein (3), and eight galactolipids as active components. Based on spectral analysis, the isolated galactolipids were identified as (2S)-1,2-bis-O-eicosapentaenoyl-3-O-β-d-galactopyranosylglycerol (4), (2S)-1-O-eicosapentaenoyl-2-O-arachidonoyl-3-O-β-d-galactopyranosylglycerol (5), (2S)-1-O-(6Z,9Z,12Z,15Z-octadecatetranoyl)-2-O-palmitoyl-3-O-β-d-galactopyranosylglycerol (6), (2S)-1-O-eicosapentaenoyl-2-O-palmitoyl-3-O-β-d-galactopyranosylglycerol (7), (2S)-1,2-bis-O-arachidonoyl-3-O-β-d-galactopyranosylglycerol (8), (2S)-1-O-arachidonoyl-2-O-palmitoyl-3-O-β-d-galactopyranosylglycerol (9), (2S)-1-O-eicosapentaenoyl-2-O-palmitoyl-3-O-(β-d-galactopyranosyl-6-1α-d-galactopyranosyl)-glycerol (10), and (2S)-1-O-arachidonoyl-2-O-palmitoyl-3-O-(β-d-galactopyranosyl-6-1α-d-galactopyranosyl)-glycerol (11). All the isolated compounds showed significant NO inhibitory activity. This is the first report of the isolation and identification of individual galactolipids from C. crispus. Moreover, (2S)-1,2-bis-O-arachidonoyl −3-O-β-d-galactopyranosylglycerol (8) is a novel compound.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aktan F (2004) iNOS-mediated nitric oxide production and its regulation. Life Sci 75:639–653
Banskota AH, Gallant P, Stefanova R, Melanson R, O'Leary SJB (2013a) Monogalactosyldiacylglycerols, potent nitric oxide inhibitors from the marine microalga Tetraselmis chui. Nat Prod Res 27:1084–1090
Banskota AH, Stefanova R, Gallant P, McGinn PJ (2013b) Mono- and digalactosyldiacylglycerols: potent nitric oxide inhibitors from the marine microalga Nannochloropsis granulata. J Appl Phycol 25:349–357
Banskota AH, Stefanova R, Sperker S, Melanson R, O'Leary SJB (2013c) Five new galactolipids from the freshwater microalga Porphyridium aerugineum and their nitric oxide inhibitory activity. J Appl Phycol 25:951–960
Carpentier S, Knaus M, Suh M (2009) Associations between lutein, zeaxanthin, and age-related macular degeneration: an overview. Crit Rev Food Sci Nutr 49:313–316
Christensen LP (2009) Galactolipids as potential health promoting compounds in vegetable foods. Recent Patents Food Nutr Agric 1:50–58
Cox S, Abu-Ghannam N, Gupta S (2010) An assessment of the antioxidant and antimicrobial activity of six species of edible Irish seaweeds. Int Food Res J 17:205–220
Craigie JS (2011) Seaweed extract stimuli in plant science and agriculture. J Appl Phycol 23:371–393
Franklin LA, Yakovleva I, Karsten U, Lüning K (1999) Synthesis of mycosporine-like amino acids in Chondrus crispus (Florideophyceae) and the consequences for sensitivity to ultraviolet B radiation. J Phycol 35:682–693
Hafting JT, Critchley AT, Cornish ML, Hubley SA, Archibald AF (2012) On-land cultivation of functional seaweed products for human usage. J Appl Phycol 24:385–392
Harris WS, Mozaffarian D, Rimm E, Kris-Etherton P, Rudel LL, Appel LJ, Engler MM, Engler MB, Sacks F (2009) Omega-6 fatty acids and risk for cardiovascular disease: a science advisory from the American Heart Association Nutrition Subcommittee of the Council on Nutrition, Physical Activity, and Metabolism; Council on Cardiovascular Nursing; and Council on Epidemiology and Prevention. Circulation 119:902–907
Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597
Jiang R-W, Hay ME, Fairchid CR, Prudhomme J, Roch KL, Aalbersberg W, Kubanek J (2008) Antineoplastic unsaturated fatty acids from Fijian macroalgae. Phytochemistry 69:2495–2500
Jiménez-Escrig A, Jiménez-Jiménez I, Pulido R, Saura-Calixto F (2001) Antioxidant activity of fresh and processed edible seaweeds. J Sci Food Agric 81:530–534
Khachik F, Englert G, Daitch CE, Beecher GR, Tonucci LH, Lusby WR (1992) Isolation and structural elucidation of the geometrical isomers of lutein and zeaxanthin in extracts from human plasma. J Chromatogr 582:153–166
Kuo PC, Schroeder RA (1995) The emerging multifaceted roles of nitric oxide. Ann Surg 221:220–235
Laycock MV, Craigie JS (1977) The occurrence and seasonal variation of gigartinine and L-citrullinyl-L-arginine in Chondrus crispus Stack. Can J Biochem 55:27–30
Leblond JD, Timofte HI, Roche SA, Porter NM (2010) Mono- and digalactosyldiacylglycerol composition of glaucocystophytes (Glaucophyta): a modern interpretation using positive-ion electrospray ionization/mass spectrometry/mass spectrometry. Phycol Res 58:222–229
McHugh DJ (2003) A Guide to the Seaweed Industry. FAO Fisheries Technical Paper 441. Chapter 8. Seaweeds used as human food. FAO, Rome. http://www.fao.org/docrep/006/y4765e/y4765e0b.htm
Mouritsen OG, Dawczynski C, Duelund L, Jahreis G, Vetter W, Schröder M (2013) On the human consumption of the red seaweed dulse (Palmaria palmata (L.) Weber & Mohr). J Appl Phycol. doi:10.1007/s10811-013-0014-7
Mullen A, Loscher CE, Roche HM (2010) Anti-inflammatory effects of EPA and DHA are dependent upon time and dose–response elements associated with LPS stimulation in THP-1-derived macrophages. J Nutr Biochem 21:444–450
Naylor J (1976) Production, Trade and Utilization of Seaweeds and Seaweed Products. Part 3. Seaweed as Food. Fisheries Technical Paper no. 159, 73 pp., FAO, Rome. http://www.fao.org/docrep/005/ac860e/ac860e00.HTM
Oshima Y, Yamada SH, Matsunaga K, Moriya T, Ohizumi Y (1994) A monogalactosyl diacylglycerol from a cultured marine dinoflagellate, Scrippsiella trochoidea. J Nat Prod 57:534–536
Rafi MM, Shafaie Y (2007) Dietary lutein modulates inducible nitric oxide synthase (iNOS) gene and protein expression in mouse macrophage cells (RAW 264.7). Mol Nutr Food Res 51: 333–340
Pereira R, Yarish C, Critchley AT (2012) Seaweed aquaculture for human foods in land-based and IMTA systems. In: Meyers RA (ed) Encyclopedia of Sustainability Science and Technology. Springer, Berlin, pp 9109–9128
Pettitt TR, Jones AL, Harwood JL (1989) Lipids of the marine red algae, Chondrus crispus and Polysiphonia lanosa. Phytochemistry 28:399–405
Rupérez P, Saura-Calixto F (2001) Dietary fibre and physicochemical properties of edible Spanish seaweeds. Eur Food Res Technol 212:349–354
Saito A, Idler DR (1966) Sterols in Irish moss (Chondrus crispus). Can J Biochem 44:1195–1199
Sindhu ER, Preethi KC, Kuttan R (2010) Antioxidant activity of carotenoid lutein in vitro and in vivo. Indian J Exp Biol 48:843–848
Wada H, Murata N (1990) Temperature-induced changes in the fatty acid composition of the cyanobacterium, Synechocystis PCC6803. Plant Physiol 92:1062–1069
Young EG, Smith DG (1958) Amino acids, peptides, and proteins of Irish moss, Chondrus crispus. J Biol Chem 233:406–410
Acknowledgments
The authors thank J. Hui and Dr. J. Melanson, National Research Council Canada for HRMS measurement. The Atlantic Innovation Fund (AIF) of the Atlantic Canada Opportunities Agency (ACOA) is thanked for partial funding of cultivated biomass preparation used in this study. This is NRC publication no. 55477.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Banskota, A.H., Stefanova, R., Sperker, S. et al. Lipids isolated from the cultivated red alga Chondrus crispus inhibit nitric oxide production. J Appl Phycol 26, 1565–1571 (2014). https://doi.org/10.1007/s10811-013-0174-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-013-0174-5