Skip to main content
Log in

Aqueous extract of some indigenous medicinal plants inhibits glycation at multiple stages and protects erythrocytes from oxidative damage–an in vitro study

  • Original Article
  • Published:
Journal of Food Science and Technology Aims and scope Submit manuscript

Abstract

Azadirachta indica, Emblica officinalis, Syzygium cumini and Terminalia bellirica are common in Indian system of traditional medicine for the prevention of diabetes and its complications. The aim of the present study was to comprehensively and comparatively investigate the antiglycation potential of these plant extracts at multiple stages and their possible protective effect against glycated albumin mediated toxicity to erythrocytes. Antiglycation activities of these plant extracts was measured by co-incubation of plant extract with bovine serum albumin-fructose glycation model. The multistage glycation markers- fructosamines (early stage), protein carbonyls (intermediate stage) and AGEs (late stage) are investigated along with measurement of thiols and β aggregation of albumin using amyloid-specific dyes–Congo red and Th T. Protection of erythrocytes from glycated albumin induced toxicity by these plant extracts was assessed by measuring erythrocytes hemolysis, lipid peroxidation, reduced glutathione and intracellular antioxidant capacity. Total phenolics, reducing power and antioxidant activities of the plant extracts were also measured. In vitro glycation assays showed that plant extracts exerted site specific inhibitory effects at multiple stages, with T. bellirica showing maximum attenuation. In erythrocytes, along with the retardation of glycated albumin induced hemolysis and lipid-peroxidation, T. bellirica considerably maintained cellular antioxidant potential. Significant positive correlations were observed between erythrocyte protection parameters with total phenolics. These plant extracts especially T. bellirica prevents glycation induced albumin modifications and subsequent toxicity to erythrocytes which might offer additional protection against diabetic vascular complications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

ABTS:

2, 2′azino-bis (3-ethylbenzothizoline-6-sulphonic acid)

AGEs:

Advanced glycation end products

BHT:

Butylated hydroxyl toluene

BSA:

Bovine serum albumin

DNPH:

di-nitro phenyl hydrazine

DPPH:

2,2′-diphenyl-1-picrylhydrazyl

DTNB:

5, 5-Dithiobis- 2-nitrobenzoic acid

FC:

Folin–Ciocalteu

GAE:

Gallic acid equivalents

LPO:

Lipid peroxidation

MDA:

Malondialdehyde

OS:

Oxidative stress

RP:

Reducing power

Th. T:

Thioflavin T

References

  • Asgary S, Naderi GH, Askari N (2005) Protective effect of flavonoids against red blood cell hemolysis by free radicals. Exp Clin Cardiol 10:88–90

    CAS  Google Scholar 

  • Baker JR, Metcalf PA, Johnson RN, Newman D, Rietz P (1985) Use of protein-based standards in automated colorimetric determinations of fructosamine in serum. Clin Chem 31:1550–1554

    CAS  Google Scholar 

  • Barnaby OS, Cerny RL, Clarke W, Hage DS (2011) Comparison of modification sites formed on human serum albumin at various stages of glycation. Clin Chim Acta 412:277–285

    Article  CAS  Google Scholar 

  • Benzie IFF, Strain JJ (1998) Ferric reducing/antioxidant power assay: direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods Enzymol 299:15–27

    Article  Google Scholar 

  • Bouma B, Kroon-Batenburg LM, Wu YP, Brünjes B, Posthuma G, Kranenburg O et al (2003) Glycation induces formation of amyloid cross-β structure in albumin. J Biol Chem 278:41810–41819

    Article  CAS  Google Scholar 

  • Bourdon E, Loreau N, Blache D (1999) Glucose and free radicals impair the antioxidant properties of serum albumin. FASEB J 13:233–244

    CAS  Google Scholar 

  • Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. LWT Food Sci Technol 28:25–30

    Article  CAS  Google Scholar 

  • Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414:813–820

    Article  CAS  Google Scholar 

  • Candiloros H, Muller S, Ziegler O, Donner M, Drouin P (1996) Role of albumin glycation on the erythrocyte aggregation: an in vitro study. Diabet Med 13:646–650

    Article  CAS  Google Scholar 

  • Cohen MP (2003) Intervention strategies to prevent pathogenetic effects of glycated albumin. Arch Biochem Biophys 419:25–30

    Article  CAS  Google Scholar 

  • Dean PDG, Johnson WS, Middle FA (eds) (1985) Affinity chromatography: a practical approach. IRL Press, Oxford, p 133

    Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77

    Article  CAS  Google Scholar 

  • Goh SY, Cooper ME (2008) The role of advanced glycation end products in progression and complications of diabetes. J Clin Endocrinol Metab 93:1143–11452

    Article  CAS  Google Scholar 

  • Gutierrez RM, Gómez YG, Guzman MD (2011) Attenuation of nonenzymatic glycation, hyperglycemia, and hyperlipidemia in streptozotocin-induced diabetic rats by chloroform leaf extract of Azadirachta indica. Pharmacogn Mag 7:254–259

    Article  Google Scholar 

  • Hudson SA, Ecroyd H, Kee TW, Carver JA (2009) The thioflavin T fluorescence assay for amyloid fibril detection can be biased by the presence of exogenous compounds. FEBS J 276:5960–5972

    Article  CAS  Google Scholar 

  • Kasabri V, Flatt PR, Abdel-Wahab YHA (2010) Terminalia bellirica stimulates the secretion and action of insulin and inhibits starch digestion and protein glycation in vitro. Br J Nutr 103:212–217

    Article  CAS  Google Scholar 

  • Klunk WE, Jacob RF, Mason RP (1999) Quantifying amyloid by congo red spectral shift assay. Methods Enzymol 309:285–305

    Article  CAS  Google Scholar 

  • Konyalioglu S, Karamenderes C (2005) The protective effects of Achillea L. species native in Turkey against H2O2-induced oxidative damage in human erythrocytes and leucocytes. J Ethnopharmacol 102:221–227

    Article  Google Scholar 

  • LeVine H (1999) Quantification of β -sheet amyloid fibril structures with thioflavin T. Methods Enzymol 309:274–284

    Article  CAS  Google Scholar 

  • Lim YY, Quah EPL (2007) Antioxidative tyrosinase inhibiting and antibacterial activities of leaf extracts from medicinal ferns. Food Chem 103:734–740

    Article  CAS  Google Scholar 

  • Luize PS, Tiuman TS, Morello LG, Maza PK, Ueda-Nakamura T, Dias Filho BP et al (2005) Effects of medicinal plant extracts on growth of leishmania (l.) amazonensis and trypanosoma cruzi. Braz J Pharm Sci 41:85–94

    Google Scholar 

  • Martín-Gallán P, Carrascosa A, Gussinyé M, Domínguez C (2003) Biomarkers of diabetes-associated oxidative stress and antioxidant status in young diabetic patients with or without subclinical complications. Free Radic Biol Med 34:1563–1574

    Article  Google Scholar 

  • McPherson JD, Shilton BH, Walton DJ (1988) Role of fructose in glycation and cross-linking of proteins. Biochemistry 27:1901–1907

    Article  CAS  Google Scholar 

  • Modak M, Dixit P, Londhe J, Ghaskadbi S, Thomas P, Devasagaya A (2007) Indian herbs and herbal drugs used for the treatment of diabetes. J Clin Biochem Nutr 40:163–173

    Article  Google Scholar 

  • Mossine VV, Linetsky M, Glinsky GV, Ortwerth BJ, Feather MS (1999) Superoxide free radical generation by Amadori compounds: the role of acyclic forms and metal ions. Chem Res Toxicol 12:230–236

    Article  CAS  Google Scholar 

  • Mukherjee PK, Maiti K, Mukherjee K, Houghton PJ (2006) Leads from Indian medicinal plants with hypoglycemic potentials. J Ethnopharmacol 106:1–28

    Article  CAS  Google Scholar 

  • Nampoothiri SV, Prathapan A, Cherian OL, Raghu KG, Venugopalan VV, Sundaresan A (2011) In vitro antioxidant and inhibitory potential of Terminalia bellirica and Emblica officinalis fruits against ldl oxidation and key enzymes linked to type 2 diabetes. Food Chem Toxicol 49:125–131

    Article  CAS  Google Scholar 

  • Oyaizu M (1986) Studies on products of browning reaction: antioxidative activity of product of browning reaction prepared from glucosamine. Jpn J Nutr 44:307–315

    Article  CAS  Google Scholar 

  • Paiva-Martins F, Fernandes J, Rocha S, Nascimento H, Vitorino R, Amado F et al (2009) Effects of olive oil polyphenols on erythrocyte oxidative damage. Mol Nutr Food Res 53:609–616

    Article  CAS  Google Scholar 

  • Peng X, Cheng KW, Ma J, Chen B, Ho CT, Lo C et al (2008) Cinnamon bark proanthocyanidins as reactive carbonyl scavengers to prevent the formation of advanced glycation endproducts. J Agric Food Chem 56:1907–1911

    Article  CAS  Google Scholar 

  • Placer ZA, Cushman LL, Johnson BC (1966) Estimation of product of lipid peroxidation (malonyl dialdehyde) in biochemical systems. Anal Biochem 16:359–364

    Article  CAS  Google Scholar 

  • Rahbar S, Figarola JL (2003) Novel inhibitors of advanced glycation endproducts. Arch Biochem Biophys 419:63–79

    Article  CAS  Google Scholar 

  • Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved abts radical cation decolorization assay. Free Radic Biol Med 26:1231–1237

    Article  CAS  Google Scholar 

  • Rondeau P, Bourdon E (2011) The glycation of albumin: structural and functional impacts. Biochimie 93:645–658

    Article  CAS  Google Scholar 

  • Saraswat M, Reddy PY, Muthenna P, Reddy GB (2009) Prevention of non-enzymic glycation of proteins by dietary agents: prospects for alleviating diabetic complications. Br J Nutr 101:1714–1721

    Article  CAS  Google Scholar 

  • Sattarahmady N, Moosavi-Movahedi AA, Ahmad F, Hakimelahi GH, Habibi-Rezaei M, Saboury AA et al (2007) Formation of the molten globule-like state during prolonged glycation of human serum albumin. Biochim Biophys Acta Gen Subj 1770:933–942

    Article  CAS  Google Scholar 

  • Tupe RS, Agte VV (2010) Role of zinc along with ascorbic acid and folic acid during long-term in vitro albumin glycation. Br J Nutr 103:370–377

    Article  CAS  Google Scholar 

  • Uchida K, Kanematsu M, Sakai K, Matsuda T, Hattori N, Mizuno Y et al (1998) Protein-bound acrolein: potential markers for oxidative stress. Proc Natl Acad Sci U S A 95:4882–4887

    Article  CAS  Google Scholar 

  • Vetter SW, Indurthi VSK (2011) Moderate glycation of serum albumin affects folding, stability, and ligand binding. Clin Chim Acta 412:2105–2116

    Article  CAS  Google Scholar 

  • Waczulíkova I, Sikurová L, Cársky J, Strbová L, Krahulec B (2000) Decreased fluidity of isolated erythrocyte membranes in type 1 and type 2 diabetes. The effect of resorcylidene aminoguanidine. Gen Physiol Biophys 19:381–392

    Google Scholar 

  • Wautier JL, Wautier MP, Chappey O, Zoukourian C, Guillausseau PJ, Capron L (1996) Diabetic erythrocytes bearing advanced glycation end products induce vascular dysfunctions. Clin Hemorheol 16:661–667

    Google Scholar 

  • Wu CH, Yeh CT, Shih PH, Yen GC (2010) Dietary phenolic acids attenuate multiple stages of protein glycation and high-glucose-stimulated proinflammatory IL-1beta activation by interfering with chromatin remodeling and transcription in monocytes. Mol Nutr Food Res 54:S127–S140

    Article  CAS  Google Scholar 

  • Wu CH, Huang SM, Lin JA, Yen GC (2011) Inhibition of advanced glycation end product formation by foodstuffs. Food Funct 2:224–234

    Article  CAS  Google Scholar 

  • Yamagishi S, Matsui T (2010) Advanced glycation end products, oxidative stress and diabetic nephropathy. Oxidative Med Cell Longev 3:101–108

    Article  Google Scholar 

Download references

Acknowledgments

The financial assistance from Department of Science and Technology, New Delhi, India is gratefully acknowledged. The authors wish to record their sincere thanks to Principal G. D. Sharma and late Professor R. M. Kothari, for encouragement and helpful suggestions for the research work. We acknowledge Dr. S. Gaikwad (Biochemical Sciences Division, National Chemical Laboratory, and Pune) for help in spectroflurometric analysis. Part of this work was presented at the 43rd National Conference of Nutrition Society of India’s 50th meeting held at National Institute of Nutrition, Hyderabad, India during 11 to12 Nov. 2011.

Author disclosure statement

No competing financial interests exist for any of the authors.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rashmi S. Tupe.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tupe, R.S., Sankhe, N.M., Shaikh, S.A. et al. Aqueous extract of some indigenous medicinal plants inhibits glycation at multiple stages and protects erythrocytes from oxidative damage–an in vitro study. J Food Sci Technol 52, 1911–1923 (2015). https://doi.org/10.1007/s13197-013-1211-8

Download citation

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13197-013-1211-8

Keywords

Navigation