The Mechanisms of Inhibition of Advanced Glycation End Products Formation through Polyphenols in Hyperglycemic Condition

Shahpour Khangholi; Fadzilah Adibah Abdul Majid; Najat Jabbar Ahmed Berwary; Farediah Ahmad; Ramlan Bin Abd Aziz

doi:10.1055/s-0035-1558086

Planta Medica, Table of Contents

Planta Med 2016; 82(01/02): 32-45
DOI: 10.1055/s-0035-1558086

Reviews

Georg Thieme Verlag KG Stuttgart · New York

The Mechanisms of Inhibition of Advanced Glycation End Products Formation through Polyphenols in Hyperglycemic Condition

Authors

Shahpour Khangholi

¹Tissue Culture Engineering Laboratory, Universiti Teknologi Malaysia (UTM), Malaysia
Fadzilah Adibah Abdul Majid

¹Tissue Culture Engineering Laboratory, Universiti Teknologi Malaysia (UTM), Malaysia

²Institute of Bio-products Development, Universiti Teknologi Malaysia (UTM), Malaysia
Najat Jabbar Ahmed Berwary

³College of Medicine, Hawler Medical University, Erbil, Iraq
Farediah Ahmad

⁴Department of Biochemistry, Faculty of Sciences, Universiti Teknologi Malaysia (UTM), Malaysia
Ramlan Bin Abd Aziz

²Institute of Bio-products Development, Universiti Teknologi Malaysia (UTM), Malaysia

Abstract

Glycation, the non-enzymatic binding of glucose to free amino groups of an amino acid, yields irreversible heterogeneous compounds known as advanced glycation end products. Those products play a significant role in diabetic complications. In the present article we briefly discuss the contribution of advanced glycation end products to the pathogenesis of diabetic complications, such as atherosclerosis, diabetic retinopathy, nephropathy, neuropathy, and wound healing. Then we mention the various mechanisms by which polyphenols inhibit the formation of advanced glycation end products. Finally, recent supporting documents are presented to clarify the inhibitory effects of polyphenols on the formation of advanced glycation end products. Phytochemicals apply several antiglycation mechanisms, including glucose metabolism, amelioration of oxidative stress, scavenging of dicarbonyl species, and up/down-regulation of gene expression. To utilize polyphenols in order to remedy diabetic complications, we must explore, examine and clarify the action mechanisms of the components of polyphenols.

Key words

AGEs - diabetic complications - polyphenols - antiglycation - hyperglycemia - antioxidant

Full Text

References

References
1 Chang TKH. Activation of pregnane X receptor (PXR) and constitutive androstane receptor (CAR) by herbal medicines. AAPS J 2009; 11: 590-601
2 Masaki H, Okano Y, Sakurai H. Generation of active oxygen species from advanced glycation end-products (AGEs) during ultraviolet light A (UVA) irradiation and a possible mechanism for cell damaging. Biochim Biophys Acta 1999; 1428: 45-56
3 Peng X, Zheng Z, Cheng K, Shan F, Ren G, Chen F, Wang M. Inhibitory effect of mung bean extract and its constituents vitexin and isovitexin on the formation of advanced gglycation end products. Food Chem 2008; 106: 475-481
4 Jagt DLV, Hunsaker LA. Methylglyoxal metabolism and diabetic complications: roles of aldose reductase, glyoxalase-I, betaine aldehyde dehydrogenase and 2-oxoaldehyde dehydrogenase. Chem Biol Interact 2003; 143–144: 341-354
5 Ardestani A, Yazdanparast R. Cyperus rotundus suppresses AGE formation and protein oxidation in a model of fructose-mediated protein glycoxidation. Int J Biol Macromol 2007; 41: 572-578
6 Vasan S, Foiles P, Founds H. Therapeutic potential of breakers of advanced glycation end product-protein crosslinks. Arch Biochem Biophys 2003; 419: 89-96
7 Zhang Q, Ames JM, Smith RD, Baynes JW, Metz TO. A perspective on the Maillard reaction and the analysis of protein glycation by mass spectrometry: probing the pathogenesis of chronic disease. J Proteome Res 2009; 8: 754-769
8 Elosta A, Ghous T, Ahmed N. Natural products as anti-glycation agents: possible therapeutic potential for diabetic complications. Curr Diabetes Rev 2012; 8: 92-108
9 Peyroux J, Sternberg M. Advanced glycation end products(AGEs): pharmacological inhibition in diabetes. Pathol Biol 2006; 54: 405-419
10 Singh VP, Bali A, Singh N, Jaggi AS. Advanced glycation end products and diabetic complications. Korean J Physiol Pharmacol 2014; 18: 1-14
11 Vlassara H. The AGE-receptor in the pathogenesis of diabetic complications. Diabetes Metab Res Rev 2001; 17: 436-443
12 Peppa M, Vlassara H. Advanced glycation end products and diabetic complications: a general overview. Hormones 2005; 4: 28-37
13 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 (Suppl. 01) 3-27
14 Ho SC, Chang PW. Inhibitory effects of several spices on inflammation caused by advanced glycation endproducts. Am J Plant Sci 2012; 3: 995-1002
15 Bopp C, Bierhaus A, Hofer S, Bouchon A, Nawroth PP, Martin E, Weigand MA. Bench-to-bedside review: The inflammation-perpetuating patternrecognition receptor RAGE as a therapeutic target in sepsis. Crit Care 2008; 12: 1-8
16 Hsu D, Zimmer V. Canadian diabetes association national nutrition committee technical review: advanced glycation end-products in diabetes management. Can J Diabetes 2010; 34: 136-140
17 Mathys KC, Ponnampalam SN, Padival S, Nagaraja RH. Semicarbazide-sensitive amine oxidase in aortic smooth muscle cells mediates synthesis of a methylglyoxal-AGE: Implications for vascular complications in diabetes. Biochem Biophys Res Commun 2002; 297: 863-869
18 Yuan Y, Zhao L, Chen Y, Moorhead JF, Varghese Z, Powis SH, Minogue S, Sun Z, Ruan XZ. Advanced glycation end products (AGEs) increase human mesangial foam cell formation by increasing Golgi SCAP glycosylation in vitro . Am J Physiol Renal Physiol 2011; 301: F236-F243
19 Hegab Z, Gibbons S, Neyses L, Mamas MA. Role of advanced glycation end products in cardiovascular disease. World J Cardiol 2012; 4: 90-102
20 Wu CH, Wu CF, Huang HW, Jao YC, Yen GC. Naturally occurring flavonoids attenuate high glucose-induced expression of proinflammatory cytokines in human monocytic THP-1 cells. Mol Nutr Food Res 2009; 53: 984-995
21 Iborra RT, Machado-Lima A, Castilho G, Nunes VS, Abdalla DS, Nakandakare ER, Passarelli M. Advanced glycation in macrophages induces intracellular accumulation of 7-ketocholesterol and total sterols by decreasing the expression of ABCA-1 and ABCG-1. Lipids Health Dis 2011; 10: 172
22 Basta G, Lazzerini G, Massaro M, Simoncini T, Tanganelli P, Fu C, Kislinger T, Stern D, Schmidt A, De Caterina R. Advanced glycation end products activate endothelium through signal-transduction receptor RAGE: a mechanism for amplification of inflammatory responses. Circulation 2002; 105: 816-822
23 Magalhaes PM, Appell HJ, Duarte JA. Involvement of advanced glycation end products in the pathogenesis of diabetic complications: the protective role of regular physical activity. Eur Rev Aging Phys Act 2008; 5: 17-29
24 Barlovic DP, Soro-Paavonen A, Jandeleit-Dahm KAM. RAGE biology, atherosclerosis and diabetes. Clin Sci 2011; 121: 43-55
25 Milne R, Brownstein S. Advanced glycation end products and diabetic retinopathy. Amino Acids 2013; 44: 1397-1407
26 Higashimoto Y, Matsui T, Nishino Y, Taira J, Inoue H, Takeuchi M, Yamagishi S. Blockage by phosphorothioate aptamers of advanced glycation end products-induced damage in cultured pericytes and endothelial cells. Microvasc Res 2013; 90: 64-70
27 Tanaka N, Yonekura H, Yamagishi S, Fjimori H, Yamamoto Y, Yamamoto H. The receptor for advanced glycation endproducts is induced by the glycation products themselves and tumour necrosis factor-a through nuclear factor-kB, and by 17 b-estradiol through Sp-1 in human vascular endothelial cells. J Biol Chem 2000; 275: 25781-25790
28 Yamagishi S, Nakamura K, Matsui T. Advanced glycation end products (AGEs) and their receptor (RAGE) system in diabetic retinopathy. Curr Drug Discov Technol 2006; 3: 83-88
29 Yamagishi S. Role of advanced glycation end products (AGEs) and receptor for AGEs (RAGE) in vascular damage in diabetes. Exp Gerontol 2011; 46: 217-224
30 Ahmed N. Advanced glycation endproducts–role in pathology of diabetic complications. Diabetes Res Clin Pract 2005; 67: 3-21
31 Tsilibary EC. Microvascular basement membranes in diabetes mellitus. J Pathol 2003; 200: 537-546
32 Vlassara H, Striker LJ, Teichberg S, Fuh H, Li YM, Steffes M. Advanced glycosylation endproducts induce glomerular sclerosis and albuminuria in normal rats. Proc Natl Acad Sci U S A 1994; 91: 11704-11708
33 Yamamoto Y, Kato I, Doi T, Yonekura H, Ohashi S, Takeuchi M, Watanabe T, Yamagishi S, Sakurai S, Takasawa S, Okamoto H, Yamamoto H. Development and prevention of advanced diabetic nephropathy in RAGE-overexpressing mice. J Clin Invest 2001; 108: 261-268
34 Tan K, Shiu SW, Chow WS, Leng L, Bucala R, Betteridge DJ. Association between serum levels of soluble receptor for advanced glycation end products and circulating advanced glycation end products in type 2 diabetes. Diabetologia 2006; 49: 2756-2762
35 Peng X, Ma J, Chen F, Wang M. Naturally occurring inhibitors against the formation of advanced glycation end-products. Food Funct 2011; 2: 289-301
36 Jack M, Wright D. Role of advanced glycation endproducts and glyoxalase I in diabetic peripheral sensory neuropathy. Transl Res 2012; 159: 355-365
37 Karmakar PS, Goswami RP. Advanced glycation end products (AGEs): itʼs role in the pathogenesis of diabetic complications. Med Update 2012; 22: 277-282
38 Goova MT, Li J, Kislinger T, Qu W, Bucciarelli LG, Nowygrod S, Wolf BM, Caliste X, Yan SF, Stem DM, Schmidt AM. Blockade of receptors for advanced glycation endproducts restores effective wound healing in diabetic mice. Am J Pathol 2001; 159: 513-525
39 Gould A, Naidoo C, Kruger D, Candy G. The role of advanced glycation end products in the hyperinflammatory response of diabetic wounds. Wound Heal S Afr 2011; 4: 25-28
40 Zhu P, Ren M, Yang C, Hu Y, Ran J, Yan L. Involvement of RAGE, MAPK and NF-jB pathways in AGEs-induced MMP-9 activation in HaCaT keratinocytes. Exp Dermatol 2011; 21: 123-129
41 Owen Jr WF, Hou FF, Stuart RO, Kay J, Boyce J, Chertow GM, Schmidt AM. β ₂-Microglobulin modified with advanced glycation end products modulates collagen synthesis by human fibroblasts. Kidney Int 1998; 53: 1365-1373
42 Peppa M, Brem H, Ehrlich P, Zhang JG, Cai W, Li Z, Croitoru A, Thung S, Vlassara H. Adverse effects of dietary glycotoxins on wound healing in genetically diabetic mice. Diabetes 2003; 52: 2805-2813
43 Xie Y, Chen X. Structures required of polyphenols for inhibiting advanced glycation end products formation. Curr Drug Metab 2013; 14: 414-431
44 Doughari JH, Human IS, Bennade S, Ndakidemi PA. Phytochemicals as chemotherapeutic agents and antioxidants: Possible solution to the control of antibiotic resistant verocytotoxin producing bacteria. J Med Plants Res 2009; 3: 839-848
45 Peng X, Cheng K, Ma J, Chen B, Ho C, Lo C, Chen F, Wang M. Cinnamon bark proanthocyanidins as reactive carbonyl scavengers to prevent the formation of advanced glycation endproducts. J Agric Food Chem 2008; 56: 1907-1911
46 Michalak A. Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Pol J Environ Stud 2006; 15: 523-530
47 Mizutani K, Ikeda K, Yamori K. Resveratrol inhibits AGEs-induced proliferation and collagen synthesis activity in vascular smooth muscle cells from stroke-prone spontaneously hypertensive rats. Biochem Biophys Res Commun 2000; 274: 61-67
48 McIntyre K, Harris C, Saleem A, Beaulieu L, Ta C, Haddad P, Arnason J. Seasonal phytochemical variation of anti-glycation principles in lowbush blueberry (Vaccinium angustifolium). Planta Med 2009; 75: 286-292
49 Tsuji-Naito K, Saeki H, Hamano M. Inhibitory effects of chrysanthemum species extracts on formation of advanced glycation end products. Food Chem 2009; 116: 854-859
50 Ramkissoon JS, Mahomoodally FM, Ahmed N, Subratty HA. Natural inhibitors of advanced glycation end-products. Nutr Food Sci 2012; 42: 397-404
51 Chompoo J, Upadhyay A, Kishimoto W, Makise T, Tawata S. Advanced glycation end products inhibitors from Alpinia zerumbet rhizomes. Food Chem 2011; 129: 709-715
52 Ferchichi L, Derbre S, Mahmood K, Toure 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
53 Lunceford N, Gugliucci A. Ilex paraguariensis extracts inhibit AGE formation more eefficiently than green tea. Fitoterapia 2005; 76: 419-427
54 Sang S, Shao X, Bai N, Lo CY, Yang CS, Ho CT. Tea polyphenol (−)-epigallocatechin-3-gallate: a new trapping agent of reactive dicarbonyl species. Chem Res Toxicol 2007; 20: 1862-1870
55 Obanda DN, Hernandez A, Ribnicky D, Yu Y, Zhang XH, Wang ZQ, Cefalu WT. Bioactives of Artemisia dracunculus L. mitigate the role of ceramides in attenuating insulin signaling in rat skeletal muscle cells. Diabetes 2012; 61: 597-605
56 Taher M, Abdul majid FA, Sarmidi MR. A proanthocyanidin from cinnamomum zeylanicum stimulates phosphorylation of insulin receptor in 3t3-L1 adipocytes. J Teknol 2006; 44: 53-68
57 Zhao HL, Sui Y, Qiao CF, Yip KY, Leung RKK, Tsui SKW, Lee HM, Wong HKT, Zhu X, Siu JJ, He L, Guan J, Liu LZ, Xu HX, Tong PCY, Chan JCN. Sustained antidiabetic effects of a berberine-containing chinese herbal Medicine through regulation of hepatic gene expression. Diabetes 2012; 61: 933-943
58 Peng CH, Chyau CC, Chan KC, Chan TH, Wang CJ, Huang CN. Hibiscus sabdariffa polyphenolic extract inhibits hyperglycemia, hyperlipidemia, and glycation-oxidative stress while improving insulin resistance. J Agric Food Chem 2011; 59: 9901-9909
59 Dembinska-Kiec A, Mykkänen O, Kiec-Wilk B, Mykkänen H. Antioxidant phytochemicals against type 2 diabetes. Br J Nutr 2008; 99: ES109-ES117
60 Wang H, Song L, Feng S, Liu Y, Zuo G, Lai F, He G, Chen M, Huang D. Characterization of proanthocyanidins in stems of Polygonum multiflorum Thunb as strong starch hydrolase inhibitors. Molecules 2013; 18: 2255-2265
61 Gurav S, Gulkari V, Duragkar N, Patil A. Systemic review: Pharmacognosy, phytochemistry, pharmacology and clinical applications of Gymnema sylvestre R Br. Pharmacogn Rev 2007; 1: 337-343
62 Eshrat H, Hussain MA. Hyperglycemic, hypolepidemic and antioxidant properties of combination of cucurmin from Curcuma longa Lin. and partially purified product from Abroma augusta Lin. in Streptozotocin induced diabetes. Indian J Clin Biochem 2002; 17: 33-43
63 Seo K, Choi M, Jung U, Kim H, Yeo J, Jeon S, Lee M. Effect of curcumin supplementation on blood glucose, plasma insulin, and glucose homeostasis related enzyme activities in diabetic db/db mice. Mol Nutr Food Res 2008; 52: 995-1004
64 Tang Y, Chen A. Curcumin prevents leptin raising glucose levels in hepatic stellate cells by blocking translocation of glucose transporter-4 and increasing glucokinase. Br J Pharmacol 2010; 16: 1137-1149
65 Xiao J, Ni X, Kai G, Chen X. A review on structure-activity relationship of dietary polyphenols inhibiting alpha-amylase. Crit Rev Food Sci Nutr 2013; 53: 497-506
66 Sajithlal GB, Chithra P, Chandrakasan G. Effect of Curcumin on the advanced glycation and cross-linking of collagen in diabetic rats. Biochem Pharmacol 1998; 56: 1607-1614
67 Kavishankar GB, Lakshmidevi N, Mahadeva Murthy S, Prakash HS, Niranjana SR. Diabetes and medicinal plants-a review. Int J Pharm Biomed Sci 2011; 2: 65-80
68 Hallam KM, Li Q, Ananthakrishnan R, Kalea A, Zou YS, Vedantham S, Schmidt AM, Yan SF, Ramasamy R. Aldose reductase and AGE-RAGE pathways: central roles in the pathogenesis of vascular dysfunction in aging rats. Aging Cell 2010; 9: 776-784
69 Lee EH, Song DG, Lee JY, Pan CH, Um BH, Jung SH. Inhibitory effect of the compounds isolated from Rhus verniciflua on aldose reductase and advanced glycation endproducts. Biol Pharm Bull 2008; 31: 1626-1630
70 Cervantes-Laurean D, Schramm DD, Jacobson EL, Halaweish I, Bruckner GG, Boissonneault GA. Inhibition of advanced glycation end product formation on collagen by rutin and its metabolites. J Nutr Biochem 2006; 17: 531-540
71 Jung SH, Lee JM, Lee HJ, Kim CY, Lee EH, Um BH. Aldose reductase and advanced glycation endproducts inhibitory effect of Phyllostachys nigra . Biol Pharm Bull 2007; 30: 1569-1572
72 Wirasathien L, Pengsuparp T, Suttisri R, Ueda H, Moriyasu M, Kawanishi K. Inhibitors of aldose reductase and advanced glycation end-products formation from the leaves of Stelechocarpus cauliflorus R.E. Fr. Phytomedicine 2007; 14: 546-550
73 Fuente JA, Manzanaro S. Aldose reductase inhibitors from natural sources. Nat Prod Rep 2003; 20: 243-251
74 Baba SP, Hellmann J, Srivastava S, Bhatnagar A. Aldose reductase (AKR1B3) regulates the accumulation of advanced glycosylation end products (AGEs) and the expression of AGE receptor (RAGE). Chem Biol Interact 2011; 191: 357-363
75 Nagai R, Unno Y, Hayashi MC, Masuda S, Hayase F, Kinae N, Horiuchi S. Peroxynitrite induces formation of n-(carboxymethyl)lysine by the cleavage of Amadori product and generation of glucosone and glyoxal from glucose novel pathways for protein modification by peroxynitrite. Diabetes 2002; 51: 2833-2839
76 Nagai R, Ikeda K, Higashi T, Sano H, Jinnouchi Y, Araki T, Horiuchi S. Hydroxyl radical mediates N epsilon-(carboxymethyl)lysine formation from Amadori product. Biochem Biophys Res Commun 1997; 234: 167-172
77 Celik I, Temur A, Isik I. Hepatoprotective role and antioxidant capacity of pomegranate (Punica granatum) flowers infusion against trichloroacetic acid-exposed in rats. Food Chem Toxicol 2009; 47: 145-149
78 Gugliucci A, Menini T. The botanical extracts of Achyrocline satureoides and Ilex paraguariensis prevent methylglyoxal-induced inhibition of plasminogen and antithrombin. Life Sci 2002; 72: 279-292
79 Losso JN, Bawadi HA, Chintalapati M. Inhibition of the formation of advanced glycation end products by thymoquinone. Food Chem 2011; 128: 55-61
80 Kamalakkannan N, Rukkumani R, Aruna K, Varma PS, Viswanathan P, Menon VP. Protective effect of n-acetyl cysteine in carbon tetrachloride-induced hepatotoxicity in rats. Iranian J Pharmacol Ther 2005; 4: 118-123
81 Bavarsad Shahripour R, Harrigan MR, Alexandrov AV. N-acetylcysteine (NAC) in neurological disorders: mechanisms of action and therapeutic opportunities. Brain Behav 2014; 4: 108-122
82 Kim J, Kim KM, Kim CS, Sohn E, Lee YM, Jo K, Kim JS. Puerarin inhibits the retinal pericyte apoptosis induced by advanced glycation end products in vitro and in vivo by inhibiting NADPH oxidase-related oxidative stress. Free Radic Biol Med 2012; 15: 357-365
83 Kim JM, Lee YM, Lee GY, Jang DS, Bae KH, Kim JS. Constituents of the roots of Pueraria lobata inhibit formation of advanced glycation end products (AGEs). Arch Pharm Res 2006; 29: 821-825
84 Ahmed I, Lakhani MS, Gillett M, John A, Raza H. Hypotriglyceridemic and hypocholesterolemic effects of anti-diabetic Momordica charantia (karela) fruit extract in streptozotocin-induced diabetic rats. Diabetes Res Clin Pract 2001; 51: 155-161
85 Gugliucci A, Bastos DHM, Schulze J, Souza MF. Caffeic and chlorogenic acids in Ilex paraguariensis extracts are the main inhibitors of AGE generation by methylglyoxal in model proteins. Fitoterapia 2009; 80: 339-344
86 Lin J, Tang Y, Kang Q, Feng Y, Chen A. Curcumin inhibits gene expression of receptor for advanced glycation endproducts (RAGE) in hepatic stellate cells in vitro by elevating PPARg activity and attenuating oxidative stress. Br J Pharmacol 2012; 166: 2212-2227
87 Kaewnarin K, Niamsup H, Shank L, Rakariyatham N. Antioxidant and antiglycation activities of some edible and medicinal plants. Chiang Mai J Sci 2014; 41: 105-116
88 Yamaguchi F, Ariga T, Yoshimura Y, Nakazawa H. Antioxidative and anti-glycation activity of garcinol from Garcinia indica fruit rind. J Agric Food Chem 2000; 48: 180-185
89 Wu J, Hsieh C, Wang H, Chen H. Inhibitory effects of guava (Psidium guajava L.) leaf extracts and its active compounds on the glycation process of protein. Food Chem 2009; 113: 78-84
90 van Acker SA, van den Berg DJ, Tromp MN, Griffioen DH, van Bennekom WP, van der Vijgh WJ, Bast A. Structural aspects of antioxidant activity of flavonoids. Free Radic Biol Med 1996; 20: 331-342
91 Kaurinovic B, Popovic M. Liposomes as a tool to study lipid peroxidation. In: Catala A, editor Lipid peroxidation. Rijeka: InTech; 2012: 155-180
92 Al-Muammar MN, Khan K. Obesity: The preventive role of the pomegranate (Punica granatum). Nutrition 2012; 28: 595-604
93 Aviram M, Dornfeld L, Rosenblat M, Volkova N, Kaplan M, Coleman R, Hayek T, Presser D, Fuhrman B. Pomegranate juice consumption reduces oxidative stress, atherogenic modifications to LDL, and platelet aggregation: studies in humans and in atherosclerotic apolipoprotein E–deficient mice. Am J Clin Nutr 2000; 71: 1062-1076
94 Abdel-Barry JA, Abdel-Hassan IA, Al-Hakiem MH. Hypoglycaemic and antihyperglycaemic effects of Trigonella foenum-graecum leaf in normal and alloxan induced diabetic rats. J Ethnopharmacol 1997; 58: 149-155
95 Hsieh C, Lin Y, Ko W, Peng C, Huang C, Peng R. Inhibitory effect of some selected nutraceutic herbs on LDL glycation induced by glucose and glyoxal. J Ethnopharmacol 2005; 102: 357-363
96 Lizcano LJ, Viloria-Bernal M, Vicente F, Berrueta LA, Gallo B, Martinez-Canamero M, Ruiz-Larrea MB, Ruiz-Sanz JI. Lipid oxidation inhibitory effects and phenolic composition of aqueous extracts from medicinal plants of colombian amazonia. Int J Mol Sci 2012; 13: 5454-5467
97 Lo CY, Li L, Tan D, Pan M, Sang S, Ho C. Trapping reactions of reactive carbonyl species with tea polyphenols in simulated physiological conditions. Mol Nutr Food Res 2006; 50: 1118-1128
98 Wang W, Yagiz Y, Buran TJ, Nunes CDN, Gu L. Phytochemicals from berries and grapes inhibited the formation of advanced glycation end-products by scavenging reactive carbonyls. Food Res Int 2011; 44: 2666-2673
99 Lv L, Shao X, Wang L, Huang D, Ho C, Sang S. Stilbene glucoside from Polygonum multiflorum Thunb.: a novel natural inhibitor of advanced glycation end product formation by trapping of methylglyoxal. J Agric Food Chem 2010; 58: 2239-2245
100 Kiho T, Usui S, Hirano K, Aizawa K, Inakuma T. Tomato paste fraction inhibiting the formation of advanced glycation end-products. Biosci Biotechnol Biochem 2004; 68: 200-205
101 Ramful D, Tarnus E, Rondeau P, Da Silva CR, Bahorun T, Bourdon E. Citrus fruit extracts reduce advanced glycation end products (AGEs)- and H₂O₂-induced oxidative stress in human adipocytes. J Agric Food Chem 2010; 58: 11119-11129
102 Martineau LC, Couture A, Spoor D, Benhaddou-Andaloussi A, Harris C, Meddah M, Leduc C, Burt A, Vuong T, Le PM, Prentki M, Bennett SA, Arnason GT, Haddad PS. Anti-diabetic properties of the Canadian lowbush blueberry Vaccinium angustifolium Ait. Phytomedicine 2006; 13: 612-623
103 Kim KM, Jung DH, Jang DS, Kim YS, Kim JM, Kim HN, Surh YJ, Kim JS. Puerarin suppresses AGEs-induced inflammation in mouse mesangial cells: A possible pathway through the induction of heme oxygenase-1 expression. Toxicol Appl Pharmacol 2010; 244: 106-113
104 Khateeb J, Gantman A, Kreitenberg AJ, Aviram M, Fuhrman B. Paraoxonase 1 (PON1) expression in hepatocytes is upregulated by pomegranate polyphenols: A role for PPAR- pathway. Atherosclerosis 2010; 208: 119-125
105 Huang THW, Peng G, Kota BP, Li GQ, Yamahara J, Roufogalis BD, Li Y. Anti-diabetic action of Punica granatum flower extract: Activation of PPAR-g and identification of an active component. Toxicol Appl Pharmacol 2005; 207: 160-169
106 Lin J, Tang Y, Kang Q, Chen A. Curcumin eliminates the inhibitory effect of advanced glycation end-products (AGEs) on gene expression of AGE receptor-1 in hepatic stellate cells in vitro . Lab Invest 2012; 92: 827-841
107 Goto T, Takahashi N, Hirai S, Kawada T. Various terpenoids derived from herbal and dietary plants function as PPAR modulators and regulate carbohydrate and lipid metabolism. PPAR Res 2010; 2010: 483958