Eugenol prevents amyloid formation of proteins and inhibits amyloid-induced hemolysis

Kriti Dubey; Bibin G. Anand; Dolat Singh Shekhawat; Karunakar Kar

doi:10.1038/srep40744

journal article Open Access Feb 01, 2017

Eugenol prevents amyloid formation of proteins and inhibits amyloid-induced hemolysis

Kriti Dubey Bibin G. Anand Dolat Singh Shekhawat Karunakar Kar

Scientific Reports Vol. 7 No. 1 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/srep40744

Abstract

AbstractEugenol has attracted considerable attention because of its potential for many pharmaceutical applications including anti-inflammatory, anti-tumorigenic and anti-oxidant properties. Here, we have investigated the effect of eugenol on amyloid formation of selected globular proteins. We find that both spontaneous and seed-induced aggregation processes of insulin and serum albumin (BSA) are significantly suppressed in the presence of eugenol. Isothermal titration calorimetric data predict a single binding site for eugenol-insulin complex confirming the affinity of eugenol for native soluble insulin species. We also find that eugenol suppresses amyloid-induced hemolysis. Our findings reveal the inherent ability of eugenol to stabilize native proteins and to delay the conversion of protein species of native conformation into β-sheet assembled mature fibrils, which seems to be crucial for its inhibitory effect.

Topics

No keywords indexed for this article. Browse by subject →

References

50

[1]

Pramod, K., Ansari, S. H. & Ali, J. Eugenol: a natural compound with versatile pharmacological actions. Natural product communications 5, 1999–2006 (2010). 10.1177/1934578x1000501236

[2]

Mnafgui, K. et al. Anti-inflammatory, Antithrombotic and Cardiac Remodeling Preventive Effects of Eugenol in Isoproterenol-Induced Myocardial Infarction in Wistar Rat. Cardiovascular toxicology, doi: 10.1007/s12012-015-9343-x (2015). 10.1007/s12012-015-9343-x

[3]

Cho, J. S., Kim, T. H., Lim, J. M. & Song, J. H. Effects of eugenol on Na + currents in rat dorsal root ganglion neurons. Brain research 1243, 53–62, doi: 10.1016/j.brainres.2008.09.030 (2008). 10.1016/j.brainres.2008.09.030

[4]

Fujisawa, S. et al. Application of bis-eugenol to a zinc oxide eugenol cement. Journal of dentistry 27, 291–295 (1999). 10.1016/s0300-5712(98)00056-6

[5]

Bi, S., Yan, L., Wang, Y., Pang, B. & Wang, T. Spectroscopic study on the interaction of eugenol with salmon sperm DNA in vitro . Journal of Luminescence 132, 6 (2012). 10.1016/j.jlumin.2011.06.060

[6]

Fujisawa, S. & Masuhara, E. Binding of eugenol and o-ethoxybenzoic acid to bovine serum albumin. Journal of dental research 60, 860–864 (1981). 10.1177/00220345810600041801

[7]

Varman, R. M. & Singh, S. Investigation of effects of terpene skin penetration enhancers on stability and biological activity of lysozyme. AAPS PharmSciTech 13, 1084–1090, doi: 10.1208/s12249-012-9840-1 (2012). 10.1208/s12249-012-9840-1

[8]

Pan, C. & Dong, Z. Antiasthmatic Effects of Eugenol in a Mouse Model of Allergic Asthma by Regulation of Vitamin D3 Upregulated Protein 1/NF-kappaB Pathway. Inflammation 38, 1385–1393, doi: 10.1007/s10753-015-0110-8 (2015). 10.1007/s10753-015-0110-8

[9]

Yao, Z. et al. Fractionation of a herbal antidiarrheal medicine reveals eugenol as an inhibitor of Ca2 + -Activated Cl- channel TMEM16A. PloS one 7, e38030, doi: 10.1371/journal.pone.0038030 (2012). 10.1371/journal.pone.0038030

[10]

Kim, H. et al. Effects of naturally occurring compounds on fibril formation and oxidative stress of beta-amyloid. Journal of agricultural and food chemistry 53, 8537–8541, doi: 10.1021/jf051985c (2005). 10.1021/jf051985c

[11]

Orally Administrated Cinnamon Extract Reduces β-Amyloid Oligomerization and Corrects Cognitive Impairment in Alzheimer's Disease Animal Models

Anat Frydman-Marom, Aviad Levin, Dorit Farfara et al.

PLoS ONE 2011 10.1371/journal.pone.0016564

[12]

Irie, Y. & Keung, W. M. Rhizoma acori graminei and its active principles protect PC-12 cells from the toxic effect of amyloid-beta peptide. Brain research 963, 282–289 (2003). 10.1016/s0006-8993(02)04050-7

[13]

Liang, Z. H. et al. Protective effects of components of the Chinese herb grassleaf sweetflag rhizome on PC12 cells incubated with amyloid-beta42. Neural regeneration research 10, 1292–1297, doi: 10.4103/1673-5374.162762 (2015). 10.4103/1673-5374.162762

[14]

Kabuto, H., Tada, M. & Kohno, M. Eugenol [2-methoxy-4-(2-propenyl)phenol] prevents 6-hydroxydopamine-induced dopamine depression and lipid peroxidation inductivity in mouse striatum. Biological & pharmaceutical bulletin 30, 423–427 (2007). 10.1248/bpb.30.423

[15]

Aguzzi, A. & O’Connor, T. Protein aggregation diseases: pathogenicity and therapeutic perspectives. Nature reviews. Drug discovery 9, 237–248, doi: 10.1038/nrd3050 (2010). 10.1038/nrd3050

[16]

Greenwald, J. & Riek, R. Biology of amyloid: structure, function, and regulation. Structure 18, 1244–1260, doi: 10.1016/j.str.2010.08.009 (2010). 10.1016/j.str.2010.08.009

[17]

Soldi, G., Plakoutsi, G., Taddei, N. & Chiti, F. Stabilization of a native protein mediated by ligand binding inhibits amyloid formation independently of the aggregation pathway. Journal of medicinal chemistry 49, 6057–6064, doi: 10.1021/jm0606488 (2006). 10.1021/jm0606488

[18]

Swift, B. Examination of insulin injection sites: an unexpected finding of localized amyloidosis. Diabetic medicine: a journal of the British Diabetic Association 19, 881–882 (2002). 10.1046/j.1464-5491.2002.07581.x

[19]

Chatani, E., Imamura, H., Yamamoto, N. & Kato, M. Stepwise organization of the beta-structure identifies key regions essential for the propagation and cytotoxicity of insulin amyloid fibrils. The Journal of biological chemistry 289, 10399–10410, doi: 10.1074/jbc.M113.520874 (2014). 10.1074/jbc.m113.520874

[20]

Wei, Y., Chen, L., Chen, J., Ge, L. & He, R. Q. Rapid glycation with D-ribose induces globular amyloid-like aggregations of BSA with high cytotoxicity to SH-SY5Y cells. BMC cell biology 10, 10, doi: 10.1186/1471-2121-10-10 (2009). 10.1186/1471-2121-10-10

[21]

Wang, F., Hull, R. L., Vidal, J., Cnop, M. & Kahn, S. E. Islet amyloid develops diffusely throughout the pancreas before becoming severe and replacing endocrine cells. Diabetes 50, 2514–2520 (2001). 10.2337/diabetes.50.11.2514

[22]

Holm, N. K. et al. Aggregation and fibrillation of bovine serum albumin. Biochimica et biophysica acta 1774, 1128–1138, doi: 10.1016/j.bbapap.2007.06.008 (2007). 10.1016/j.bbapap.2007.06.008

[23]

Jayamani, J. & Shanmugam, G. Gallic acid, one of the components in many plant tissues, is a potential inhibitor for insulin amyloid fibril formation. European journal of medicinal chemistry 85, 352–358, doi: 10.1016/j.ejmech.2014.07.111 (2014). 10.1016/j.ejmech.2014.07.111

[24]

Gong, H. et al. Effects of several quinones on insulin aggregation. Scientific reports 4, 5648, doi: 10.1038/srep05648 (2014). 10.1038/srep05648

[25]

Dubey, K., Anand, B. G., Temgire, M. K. & Kar, K. Evidence of rapid coaggregation of globular proteins during amyloid formation. Biochemistry 53, 8001–8004, doi: 10.1021/bi501333q (2014). 10.1021/bi501333q

[26]

Gualandi-Signorini, A. M. & Giorgi, G. Insulin formulations – a review. European Review for Medical and Pharmacological Sciences 5, 11 (2001).

[27]

Dische, F. E. et al. Insulin as an amyloid-fibril protein at sites of repeated insulin injections in a diabetic patient. Diabetologia 31, 158–161 (1988). 10.1007/bf00276849

[28]

Siposova, K. et al. Depolymerization of insulin amyloid fibrils by albumin-modified magnetic fluid. Nanotechnology 23, 055101, doi: 10.1088/0957-4484/23/5/055101 (2012). 10.1088/0957-4484/23/5/055101

[29]

Liu, P. et al. Co-assembly of human islet amyloid polypeptide (hIAPP)/insulin. Chem Commun (Camb) 48, 191–193, doi: 10.1039/c1cc14285b (2012). 10.1039/c1cc14285b

[30]

Apetri, M. M., Maiti, N. C., Zagorski, M. G., Carey, P. R. & Anderson, V. E. Secondary structure of alpha-synuclein oligomers: characterization by raman and atomic force microscopy. Journal of molecular biology 355, 63–71, doi: 10.1016/j.jmb.2005.10.071 (2006). 10.1016/j.jmb.2005.10.071

[31]

Dubey, K. et al. Tyrosine- and tryptophan-coated gold nanoparticles inhibit amyloid aggregation of insulin. Amino acids 47, 2551–2560, doi: 10.1007/s00726-015-2046-6 (2015). 10.1007/s00726-015-2046-6

[32]

Sarzehi, S. & Chamani, J. Investigation on the interaction between tamoxifen and human holo-transferrin: determination of the binding mechanism by fluorescence quenching, resonance light scattering and circular dichroism methods. International journal of biological macromolecules 47, 558–569, doi: 10.1016/j.ijbiomac.2010.08.002 (2010). 10.1016/j.ijbiomac.2010.08.002

[33]

Chamani, J., Tafrishi, N. & Momen-Heravi, M. Characterization of the interaction between human lactoferrin and lomefloxacin at physiological condition: Multi-spectroscopic and modeling description. Journal of Luminescence 130, 9 (2010).

[34]

Quenching of fluorescence by oxygen. Probe for structural fluctuations in macromolecules

Joseph R. Lakowicz, Gregorio Weber

Biochemistry 1973 10.1021/bi00745a020

[35]

Chinnathambi, S., Velmurugan, D., Hanagata, N., Aruna, P. & Ganesan, S. Investigations on the interactions of 5-fluorouracil with bovine serum albumin: Optical spectroscopic and molecular modeling studies. Journal of Luminescence 151, 10 (2014). 10.1016/j.jlumin.2014.01.063

[36]

Sun, Y. et al. Studies on the arctiin and its interaction with DNA by spectral methods. Journal of Luminescence 131, 8 (2011).

[37]

Precupas, A., Sandu, R. & Popa, V. T. Quercetin Influence on Thermal Denaturation of Bovine Serum Albumin. J Phys Chem B 120, 9362–9375 (2016). 10.1021/acs.jpcb.6b06214

[38]

Nespoulous, C. et al. Odorant binding and conformational changes of a rat odorant-binding protein.Chem Senses 29, 189–198 (2004). 10.1093/chemse/bjh017

[39]

Mattson, M. P., Begley, J. G., Mark, R. J. & Furukawa, K. Abeta25–35 induces rapid lysis of red blood cells: contrast with Abeta1-42 and examination of underlying mechanisms. Brain research 771, 147–153 (1997). 10.1016/s0006-8993(97)00824-x

[40]

Nakagawa, K. et al. Amyloid beta-induced erythrocytic damage and its attenuation by carotenoids. FEBS letters 585, 1249–1254, doi: 10.1016/j.febslet.2011.03.060 (2011). 10.1016/j.febslet.2011.03.060

[41]

Chiti, F. & Dobson, C. M. Amyloid formation by globular proteins under native conditions. Nature chemical biology 5, 15–22, doi: 10.1038/nchembio.131 (2009). 10.1038/nchembio.131

[42]

Kar, K. & Kishore, N. Enhancement of thermal stability and inhibition of protein aggregation by osmolytic effect of hydroxyproline. Biopolymers 87, 339–351, doi: 10.1002/bip.20834 (2007). 10.1002/bip.20834

[43]

Gulcin, I. Antioxidant activity of eugenol: a structure-activity relationship study. Journal of medicinal food 14, 975–985, doi: 10.1089/jmf.2010.0197 (2011). 10.1089/jmf.2010.0197

[44]

Porat, Y., Abramowitz, A. & Gazit, E. Inhibition of amyloid fibril formation by polyphenols: structural similarity and aromatic interactions as a common inhibition mechanism. Chemical biology & drug design 67, 27–37, doi: 10.1111/j.1747-0285.2005.00318.x (2006). 10.1111/j.1747-0285.2005.00318.x

[45]

Pechlaner, M. & Oostenbrink, C. Multiple Binding Poses in the Hydrophobic Cavity of Bee Odorant Binding Protein AmelOBP14. Journal of chemical information and modeling 55, 2633–2643, doi: 10.1021/acs.jcim.5b00673 (2015). 10.1021/acs.jcim.5b00673

[46]

Singh, P. et al. Potential Dual Role of Eugenol in Inhibiting Advanced Glycation End Products in Diabetes: Proteomic and Mechanistic Insights. Scientific reports 6, 18798, doi: 10.1038/srep18798 (2016). 10.1038/srep18798

[47]

Hemaiswarya, S. & Doble, M. Synergistic interaction of eugenol with antibiotics against Gram negative bacteria. Phytomedicine: international journal of phytotherapy and phytopharmacology 16, 997–1005, doi: 10.1016/j.phymed.2009.04.006 (2009). 10.1016/j.phymed.2009.04.006

[48]

Morozova-Roche, L. A. et al. Amyloid fibril formation and seeding by wild-type human lysozyme and its disease-related mutational variants. Journal of structural biology 130, 339–351, doi: 10.1006/jsbi.2000.4264 (2000). 10.1006/jsbi.2000.4264

[49]

Krebs, M. R., Morozova-Roche, L. A., Daniel, K., Robinson, C. V. & Dobson, C. M. Observation of sequence specificity in the seeding of protein amyloid fibrils. Protein science: a publication of the Protein Society 13, 1933–1938, doi: 10.1110/ps.04707004 (2004). 10.1110/ps.04707004

[50]

Lorenzen, N. et al. The role of stable alpha-synuclein oligomers in the molecular events underlying amyloid formation. Journal of the American Chemical Society 136, 3859–3868, doi: 10.1021/ja411577t (2014). 10.1021/ja411577t

Cited By

63

Fabricating Silver Nanoparticles with Antidiabetic d-Pinitol to Restrict Amyloid Formation of Insulin

Om Prakash Mahato, Kailash Prasad Prajapati · 2025

ACS Applied Bio Materials

Cu(II) Specifically Disassembles Insulin Amyloid Nanostructures via Direct Interaction with Cross-β Fibrils

Shikha Mittal, Kailash Prasad Prajapati · 2024

Nano Letters

Rapid Coaggregation of Proteins Without Sequence Similarity: Possible Role of Conformational Complementarity

Kailash Prasad Prajapati, Masihuzzaman Ansari · 2024

Biochemistry

Autooxidation of curcumin in physiological buffer causes an enhanced synergistic anti-amyloid effect

Shikha Mittal, Kailash Prasad Prajapati · 2023

International Journal of Biological...

Amyloid cross-seeding raises new dimensions to understanding of amyloidogenesis mechanism

Paramita Chaudhuri, Kailash P. Prajapati · 2019

Ageing Research Reviews

Aβ 1-40 mediated aggregation of proteins and metabolites unveils the relevance of amyloid cross-seeding in amyloidogenesis

Bibin G. Anand, Kailash P. Prajapati · 2018

Biochemical and Biophysical Researc...

Tyrosine-Generated Nanostructures Initiate Amyloid Cross-Seeding in Proteins Leading to a Lethal Aggregation Trap

Bibin Gnanadhason Anand, Kailash P. Prajapati · 2018

Biochemistry

Metrics

63

Citations

50

References

Details

Published: Feb 01, 2017
Vol/Issue: 7(1)
License: View

Authors

Dolat Singh Shekhawat

K

Karunakar Kar

Cite This Article

Kriti Dubey, Bibin G. Anand, Dolat Singh Shekhawat, et al. (2017). Eugenol prevents amyloid formation of proteins and inhibits amyloid-induced hemolysis. Scientific Reports, 7(1). https://doi.org/10.1038/srep40744

Eugenol prevents amyloid formation of proteins and inhibits amyloid-induced hemolysis

You May Also Like