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DOI: 10.1055/s-0035-1557829
Pheophorbide a from Capsosiphon fulvescens Inhibits Advanced Glycation End Products Mediated Endothelial Dysfunction
Publication History
received 30 November 2014
revised 22 June 2015
accepted 09 July 2015
Publication Date:
26 August 2015 (online)
Abstract
During hyperglycemia, the first step toward the formation of advanced glycation end products is the nonenzymatic glycation between the carbonyl group of a sugar and the primary amino group of a protein. Advanced glycation end products are then produced through more complex reactions. Reactive oxygen species derived from advanced glycation end products may play a key role in inflammation of the endothelium, leading to the complications seen in diabetes. Glycolaldehyde-induced advanced glycation end products have been reported to express proinflammatory cytokines, such as tumor necrosis factor-α and interleukin-1β. This study focused on Capsosiphon fulvescens, a Capsosiphonaceae type of green algae that has shown potential as a functional food material. Pheophorbide a, an anti-glycation compound, was isolated from C. fulvescens by extraction using a mixture of ethanol and water, followed by column fractionation of the resulting extract. The compound separated from C. fulvescens was identified by means of high-performance liquid chromatography combined with mass spectrometry. Pheophorbide a showed scavenging activity of the intracellular reactive oxygen species as well as monocyte adhesiveness inhibitory activity on the human myelomonocytic cell line (THP-1) and human umbilical vein endothelial cells cocultivation system. The mRNA levels of inflammation-related genes such as monocyte chemoattractant protein-1 and interleukin-6 were significantly decreased by pheophorbide a, and advanced glycation end products-stimulated tumor necrosis factor-α and interleukin-1β were downregulated as well. These results indicate that pheophorbide a has significant reactive oxygen species-scavenging activity, monocyte adhesive inhibitory activity, and downregulatory activity of cytokines related to inflammation affecting the endothelium. Pheophorbide a could therefore be a promising candidate for modulating endothelial cell dysfunction.
Key words
Capsosiphon fulvescens - Capsosiphonaceae - pheophorbide a - advanced glycation end product - proinflammatory cytokine - endothelial cell dysfunction* These two authors have contributed equally to this work and should be considered co-first authors.
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References
- 1 Ryden L, Grant PJ, Anker SD, Berne C, Cosentino F, Danchin N, Deaton C, Escaned J, Hammes HP, Huikuri H, Marre M, Marx N, Mellbin L, Ostergren J, Patrono C, Seferovic P, Uva MS, Taskinen MR, Tendera M, Tuomilehto J, Valensi P, Zamorano JL, Achenbach S, Baumgartner H, Bax JJ, Bueno H, Dean V, Erol C, Fagard R, Ferrari R, Hasdai D, Hoes AW, Kirchhof P, Knuuti J, Kolh P, Lancellotti P, Linhart A, Nihoyannopoulos P, Piepoli MF, Ponikowski P, Sirnes PA, Tamargo JL, Torbicki A, Wijns W, Windecker S, De Backer G, Ezquerra EA, Avogaro A, Badimon L, Baranova E, Betteridge J, Ceriello A, Funck-Brentano C, Gulba DC, Kjekshus JK, Lev E, Mueller C, Neyses L, Nilsson PM, Perk J, Reiner Z, Sattar N, Schachinger V, Scheen A, Schirmer H, Stromberg A, Sudzhaeva S, Viigimaa M, Vlachopoulos C, Xuereb RG. ESC Guidelines on diabetes, pre-diabetes, and cardiovascular diseases developed in collaboration with the EASD: the task force on diabetes, pre-diabetes, and cardiovascular diseases of the European Society of Cardiology (ESC) and developed in collaboration with the European Association for the Study of Diabetes (EASD). Eur Heart J 2013; 34: 3035-3087
- 2 Goldin A, Beckman JA, Schmidt AM, Creager MA. Advanced glycation end products: sparking the development of diabetic vascular injury. Circulation 2006; 114: 597-605
- 3 Maillard LC. The action of amino acids on sugar; the formation of melanoidin by a methodic route. CR Acad Sci Ser 2 1912; 154: 66-68
- 4 Peyroux J, Sternberg M. Advanced glycation endproducts (AGEs): pharmacological inhibition in diabetes. Pathol Biol (Paris) 2006; 54: 405-419
- 5 Reddy VP, Beyaz A. Inhibitors of the Maillard reaction and AGE breakers as therapeutics for multiple diseases. Drug Discov Today 2006; 11: 646-654
- 6 Reddy VP, Obrenovich ME, Atwood CS, Perry G, Smith MA. Involvement of Maillard reactions in Alzheimer disease. Neurotox Res 2002; 4: 191-209
- 7 Schleicher E, Friess U. Oxidative stress, AGE, and atherosclerosis. Kidney Int Suppl 2007; 72: S17-S26
- 8 Ansari NA, Dash D. Amadori glycated proteins: role in production of autoantibodies in diabetes mellitus and effect of inhibitors on non-enzymatic glycation. Aging Dis 2013; 4: 50-56
- 9 Park S, Lakatta EG. Role of inflammation in the pathogenesis of arterial stiffness. Yonsei Med J 2012; 53: 258-261
- 10 Sato T, Iwaki M, Shimogaito N, Wu X, Yamagishi S, Takeuchi M. TAGE (toxic AGEs) theory in diabetic complications. Curr Mol Med 2006; 6: 351-358
- 11 Pangestuti R, Kim SK. Biological activities and health benefit effects of natural pigments derived from marine algae. J Funct Foods 2011; 3: 255-266
- 12 Morand P, Briand X. Excessive growth of macroalgae: A symptom of environmental disturbance. Bot Mar 1996; 39: 491-516
- 13 Park MH, Kim MH. The effect of Capsosiphon fulvecense extract on inhibition of platelet aggregation and serum lipid level in ovariectomized Rats. J Life Sci 2005; 15: 1028-1033
- 14 Vistoli G, De Maddis D, Cipak A, Zarkovic N, Carini M, Aldini G. Advanced glycoxidation and lipoxidation end products (AGEs and ALEs): an overview of their mechanisms of formation. Free Radic Res 2013; 47: 3-27
- 15 Baynes JW, Thorpe SR. Role of oxidative stress in diabetic complications: a new perspective on an old paradigm. Diabetes 1999; 48: 1-9
- 16 Nagai R, Murray DB, Metz TO, Baynes JW. Chelation: a fundamental mechanism of action of AGE inhibitors, AGE breakers, and other inhibitors of diabetes complications. Diabetes 2012; 61: 549-559
- 17 Ferchichi L, Derbré S, Mahmood K, Touré K, Guilet D, Litaudon M, Awang K, Hadi AH, Le Ray AM, Richomme P. Bioguided fractionation and isolation of natural inhibitors of advanced glycation end-products (AGEs) from Calophyllum flavoramulum . Phytochemistry 2012; 78: 98-106
- 18 Park CH, Tanaka T, Kim HY, Park JC, Yokozawa T. Protective Effects of Corni Fructus against Advanced Glycation Endproducts and Radical Scavenging. Evid Based Complement Alternat Med 2012; 2012: 418953
- 19 Peng XF, Ma JY, Chen F, Wang MF. Naturally occurring inhibitors against the formation of advanced glycation end-products. Food Funct 2011; 2: 289-301
- 20 Sero L, Sanguinet L, Blanchard P, Dang BT, Morel S, Richomme P, Seraphin D, Derbre S. Tuning a 96-well microtiter plate fluorescence-based assay to identify AGE inhibitors in crude plant extracts. Molecules 2013; 18: 14320-14339
- 21 Liu H, Gu L. Phlorotannins from brown algae (Fucus vesiculosus) inhibited the formation of advanced glycation endproducts by scavenging reactive carbonyls. J Agric Food Chem 2012; 60: 1326-1334
- 22 Son YK, Jin SE, Kim HR, Woo HC, Jung HA, Choi JS. Inhibitory activities of the edible brown alga Laminaria japonica on glucose-mediated protein damage and rat lens aldose reductase. Fisheries Sci 2011; 77: 1069-1079
- 23 Hargus JA, Fronczek FR, Vicente MG, Smith KM. Mono-(L)-aspartylchlorin-e6. Photochem Photobiol 2007; 83: 1006-1015
- 24 Chan JY, Tang PM, Hon PM, Au SW, Tsui SK, Waye MM, Kong SK, Mak TC, Fung KP. Pheophorbide a, a major antitumor component purified from Scutellaria barbata, induces apoptosis in human hepatocellular carcinoma cells. Planta Med 2006; 72: 28-33
- 25 Cho ML, Lee HS, Kang IJ, Won MH, You SG. Antioxidant properties of extract and fractions from Enteromorpha prolifera, a type of green seaweed. Food Chem 2011; 127: 999-1006
- 26 Deanfield JE, Halcox JP, Rabelink TJ. Endothelial function and dysfunction: testing and clinical relevance. Circulation 2007; 115: 1285-1295
- 27 Hogg N, Darley-Usmar VM, Wilson MT, Moncada S. Production of hydroxyl radicals from the simultaneous generation of superoxide and nitric oxide. Biochem J 1992; 281 (Pt. 2) 419-424
- 28 Cho M, Lee HS, Kang IJ, Won MH, You S. Antioxidant properties of extract and fractions from Enteromorpha prolifera, a type of green seaweed. Food Chem 2011; 127: 999-1006
- 29 Kanner J, Harel S, Granit R. Nitric-oxide as an antioxidant. Arch Biochem Biophys 1991; 289: 130-136
- 30 Schulz K, Kerber S, Kelm M. Reevaluation of the Griess method for determining NO/NO2- in aqueous and protein-containing samples. Nitric Oxide 1999; 3: 225-234
- 31 Wautier MP, Chappey O, Corda S, Stern DM, Schimidt AM, Wautier JL. Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am J Physiol Endocrinol Metab 2001; 280: E685-E694
- 32 Puddu P, Puddu GM, Cravero E, Rosati M, Muscari A. The molecular sources of reactive oxygen species in hypertension. Blood Press 2008; 17: 70-77
- 33 Basta G. Receptor for advanced glycation endproducts and atherosclerosis: From basic mechanisms to clinical implications. Atherosclerosis 2008; 196: 9-21
- 34 Choi BH, Ryoo IG, Kang HC, Kwak MK. The sensitivity of cancer cells to pheophorbide a-based photodynamic therapy is enhanced by NRF2 silencing. PLoS One 2014; 9: e107158
- 35 Dougherty TJ, Gomer CJ, Henderson BW, Jori G, Kessel D, Korbelik M, Moan J, Peng Q. Photodynamic therapy. J Natl Cancer Inst 1998; 90: 889-905
- 36 Buytaert E, Dewaele M, Agostinis P. Molecular effectors of multiple cell death pathways initiated by photodynamic therapy. Biochim Biophys Acta 2007; 1776: 86-107
- 37 Paddock SW. Principles and practices of laser scanning confocal microscopy. Mol Biotechnol 2000; 16: 127-149
- 38 Basta G, Schmidt AM, De Caterina R. Advanced glycation end products and vascular inflammation: implications for accelerated atherosclerosis in diabetes. Cardiovasc Res 2004; 63: 582-592
- 39 Tsouknos A, Nash GB, Rainger GE. Monocytes initiate a cycle of leukocyte recruitment when cocultured with endothelial cells. Atherosclerosis 2003; 170: 49-58
- 40 Nam MH, Lee HS, Seomun Y, Lee Y, Lee KW. Monocyte-endothelium-smooth muscle cell interaction in co-culture: proliferation and cytokine productions in response to advanced glycation end products. Biochim Biophys Acta 2011; 1810: 907-912
- 41 Takahashi M, Ikeda U, Masuyama JI, Kasahara T, Kitagawa SI, Takahashi YI, Kano S, Shimada K. Induction of monocyte chemoattractant protein-1 synthesis in human monocytes during transendothelial migration in-vitro . Circ Res 1995; 76: 750-757
- 42 Schindler R, Mancilla J, Endres S, Ghorbani R, Clark SC, Dinarello CA. Correlations and interactions in the production of interleukin-6 (IL-6), IL-1, and tumor necrosis factor (TNF) in human blood mononuclear cells: IL-6 suppresses IL-1 and TNF. Blood 1990; 75: 40-47
- 43 Choi SY, Jung SH, Lee HS, Park KW, Yun BS, Lee KW. Glycation inhibitory activity and the identification of an active compound in Plantago asiatica extract. Phytother Res 2008; 22: 323-329
- 44 Lee HS, Won NH, Kim KH, Lee H, Jun W, Lee KW. Antioxidant effects of aqueous extract of Terminalia chebula in vivo and in vitro . Biol Pharm Bull 2005; 28: 1639-1644
- 45 Yanagisawa K, Makita Z, Shiroshita K, Ueda T, Fusegawa T, Kuwajima S, Takeuchi M, Koike T. Specific fluorescence assay for advanced glycation end products in blood and urine of diabetic patients. Metabolism 1998; 47: 1348-1353
- 46 Delgado-Andrade C, Rufian-Henares JA, Morales FJ. Lysine availability is diminished in commercial fibre-enriched breakfast cereals. Food Chem 2007; 100: 725-731
- 47 Szabo MR, Iditoiu C, Chambre D, Lupea AX. Improved DPPH determination for antioxidant activity spectrophotometric assay. Chem Pap 2007; 61: 214-216
- 48 Benzie IFF, Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The FRAP assay. Anal Biochem 1996; 239: 70-76
- 49 Biswas M, Haldar PK, Ghosh AK. Antioxidant and free-radical-scavenging effects of fruits of Dregea volubilis . J Nat Sci Biol Med 2010; 1: 29-34
- 50 Halliwell B, Aruoma OI. DNA damage by oxygen-derived species. Its mechanism and measurement in mammalian systems. FEBS Lett 1991; 281: 9-19
- 51 Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983; 65: 55-63
- 52 van Vliet JJH, Vaessen HAMG, van den Burg G, Schothorst RC. Twenty-four-hour duplicate diet study 1994; nitrate and nitrite: method development and intake per person per day. Cancer Lett 1997; 114: 305-307
- 53 Lee HS, Koo YC, Suh HJ, Kim KY, Lee KW. Preventive effects of chebulic acid isolated from Terminalia chebula on advanced glycation endproduct-induced endothelial cell dysfunction. J Ethnopharmacol 2010; 131: 567-574
- 54 Imrich A, Kobzik L. Flow cytometric analysis of macrophage oxidative metabolism using DCFH. Methods Mol Biol 1998; 91: 97-108
- 55 Rodriguez EG, Lefebvre R, Bodnar D, Legrand C, Szentesi P, Vincze J, Poulard K, Bertrand-Michel J, Csernoch L, Buj-Bello A, Jacquemond V. Phosphoinositide substrates of myotubularin affect voltage-activated Ca(2)(+) release in skeletal muscle. Pflugers Arch 2014; 466: 973-985
- 56 Li Y, Kleijn JM, Cohen Stuart MA, Slaghek T, Timmermans J, Norde W. Mobility of lysozyme inside oxidized starch polymer microgels. Soft Matter 2011; 7: 1926-1935