Small-Angle X-ray Scattering Study of Protein Complexes with Tea Polyphenols

Shi, Ce; Tang, Haifeng; Xiao, Jie; Cui, Fengchao; Yang, Kecheng; Li, Ji; Zhao, Qin; Huang, Qingrong; Li, Yunqi

doi:10.1021/acs.jafc.6b04630

Small-Angle X-ray Scattering Study of Protein Complexes with Tea Polyphenols

Journal Article · Tue Jan 03 00:00:00 EST 2017 · Journal of Agricultural and Food Chemistry

DOI:https://doi.org/10.1021/acs.jafc.6b04630· OSTI ID:1432857

Shi, Ce ^[1]; Tang, Haifeng ^[2]; Xiao, Jie ^[3]; Cui, Fengchao ^[1]; Yang, Kecheng ^[1]; Li, Ji ^[3]; Zhao, Qin ^[3]; ^[3]; ^[1]

Changchun Inst. of Applied Chemistry (China)
Changchun Inst. of Applied Chemistry (China); Jilin Univ., Changchun (China)
Rutgers Univ., New Brunswick, NJ (United States)

Exploration of the structure of protein complexes, especially the change in conformation and aggregation behavior of proteins upon ligand binding, is crucial to clarify their bioactivities at the molecular level. We applied solution small-angle X-ray scattering (SAXS) to study the complex structure of bovine serum albumin (BSA) and trypsin binding with tea polyphenols, that is, catechin and epigallocatechin gallate (EGCG). We found that tea polyphenols can steadily promote the aggregation of proteins and protein complexes through their bridging effect. The numbers of proteins in the complexes and in the aggregates of complexes are extracted from SAXS intensity profiles, and their dependences as a function of the molar ratio of polyphenol to protein are discussed. EGCG has stronger capability than catechin to promote complex formation and further aggregation, and the aggregates of complexes have a denser core with a relatively smooth surface. The aggregates induced by catechin are loosely packed with a rough surface. BSA shows higher stability than trypsin in the formation of complex with a well-folded conformation. The synergistic unfolding of trypsin results in larger aggregates in the mixtures with more tea polyphenols. The binding affinity and number of tea polyphenols bound to each protein are further determined using fluorescence spectroscopy. Furthermore, the structure of protein complexes explored in this work is referable in the preparation of protein complex-based particles and the understanding of polyphenol-induced formation and further aggregation of protein complexes.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Center for Protein Sciences Shanghai (NCPSS)

OSTI ID:: 1432857

Journal Information:: Journal of Agricultural and Food Chemistry, Journal Name: Journal of Agricultural and Food Chemistry Journal Issue: 3 Vol. 65; ISSN 0021-8561

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (43)

Plant Polyphenols: Chemical Properties, Biological Activities, and Synthesis Quideau, Stéphane; Deffieux, Denis; Douat-Casassus, Céline Angewandte Chemie International Edition, Vol. 50, Issue 3 https://doi.org/10.1002/anie.201000044	journal	January 2011
Characterizing flexible and intrinsically unstructured biological macromolecules by SAS using the Porod-Debye law Rambo, Robert P.; Tainer, John A. Biopolymers, Vol. 95, Issue 8 https://doi.org/10.1002/bip.21638	journal	April 2011
Effects of tea polyphenols on the activities of soybean trypsin inhibitors and trypsin: Effects of tea polyphenols on trypsin inhibitors Huang, Huihua; Kwok, Kin-Chor; Liang, Hanhua Journal of the Science of Food and Agriculture, Vol. 84, Issue 2 https://doi.org/10.1002/jsfa.1610	journal	January 2004
Docking studies and model development of tea polyphenol proteasome inhibitors: Applications to rational drug design Smith, David M.; Daniel, Kenyon G.; Wang, Zhigang Proteins: Structure, Function, and Bioinformatics, Vol. 54, Issue 1 https://doi.org/10.1002/prot.10504	journal	September 2003
Crystallographic analysis reveals common modes of binding of medium and long-chain fatty acids to human serum albumin 1 1Edited by R. Huber Bhattacharya, Ananyo A.; Grüne, Tim; Curry, Stephen Journal of Molecular Biology, Vol. 303, Issue 5 https://doi.org/10.1006/jmbi.2000.4158	journal	November 2000
Principles of Fluorescence Spectroscopy Lakowicz, Joseph R. Springer New York, NY https://doi.org/10.1007/978-0-387-46312-4	book	January 2006
Changes of trypsin in activity and secondary structure induced by complex with trypsin inhibitors and tea polyphenol Huang, Huihua; Zhao, Mouming European Food Research and Technology, Vol. 227, Issue 2 https://doi.org/10.1007/s00217-007-0729-2	journal	August 2007
Interactions of condensed tannins with selected proteins Asquith, Thomas N.; Butler, Larry G. Phytochemistry, Vol. 25, Issue 7 https://doi.org/10.1016/S0031-9422(00)81214-5	journal	January 1986
Influence of the tannin structure on the disruption effect of carbohydrates on protein–tannin aggregates Mateus, Nuno; Carvalho, Elisabete; Luı́s, Catarina Analytica Chimica Acta, Vol. 513, Issue 1 https://doi.org/10.1016/j.aca.2003.08.072	journal	June 2004
Protective Effects of Green Tea Polyphenols in the 6-OHDA Rat Model of Parkinson’s Disease Through Inhibition of ROS-NO Pathway Guo, Shuhong; Yan, Jingqi; Yang, Tangbin Biological Psychiatry, Vol. 62, Issue 12 https://doi.org/10.1016/j.biopsych.2007.04.020	journal	December 2007
Wide-Angle X-Ray Solution Scattering as a Probe of Ligand-Induced Conformational Changes in Proteins Fischetti, R. F.; Rodi, D. J.; Gore, D. B. Chemistry & Biology, Vol. 11, Issue 10 https://doi.org/10.1016/j.chembiol.2004.08.013	journal	October 2004
Predictive QSAR modeling of aldose reductase inhibitors using Monte Carlo feature selection Nantasenamat, Chanin; Monnor, Teerawat; Worachartcheewan, Apilak European Journal of Medicinal Chemistry, Vol. 76 https://doi.org/10.1016/j.ejmech.2014.02.043	journal	April 2014
Albumin causes a synergistic increase in the antioxidant activity of green tea catechins in oil-in-water emulsions Almajano, M. Pilar; Delgado, M. Eugenia; Gordon, Michael H. Food Chemistry, Vol. 102, Issue 4 https://doi.org/10.1016/j.foodchem.2006.06.067	journal	January 2007
Binding of (−)-epigallocatechin-3-gallate with thermally-induced bovine serum albumin/ι-carrageenan particles Li, Jinbing; Wang, Xiaoyong Food Chemistry, Vol. 168 https://doi.org/10.1016/j.foodchem.2014.07.097	journal	February 2015
Glycosylation of bovine serum albumin via Maillard reaction prevents epigallocatechin-3-gallate-induced protein aggregation Xia, Shuqin; Li, Yunqi; Xia, Qiuyang Food Hydrocolloids, Vol. 43 https://doi.org/10.1016/j.foodhyd.2014.05.022	journal	January 2015
Characterization of Protein Fold by Wide-Angle X-ray Solution Scattering Makowski, Lee; Rodi, Diane J.; Mandava, Suneeta Journal of Molecular Biology, Vol. 383, Issue 3 https://doi.org/10.1016/j.jmb.2008.08.038	journal	November 2008
Influence of Cd2+, Hg2+ and Pb2+ on (+)-catechin binding to bovine serum albumin studied by fluorescence spectroscopic methods Peng, Mijun; Shi, Shuyun; Zhang, Yuping Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, Vol. 85, Issue 1 https://doi.org/10.1016/j.saa.2011.09.059	journal	January 2012
Trypsins and their role in carcinoma growth Nyberg, P.; Ylipalosaari, M.; Sorsa, T. Experimental Cell Research, Vol. 312, Issue 8 https://doi.org/10.1016/j.yexcr.2005.12.024	journal	May 2006
Changes in Biomolecular Conformation Seen by Small Angle X-ray Scattering Doniach, Sebastian Chemical Reviews, Vol. 101, Issue 6 https://doi.org/10.1021/cr990071k	journal	June 2001
Polyphenol/Peptide Binding and Precipitation Charlton, Adrian J.; Baxter, Nicola J.; Khan, M. Lokman Journal of Agricultural and Food Chemistry, Vol. 50, Issue 6 https://doi.org/10.1021/jf010897z	journal	March 2002
Investigation of Adsorption Behavior of (−)-Epigallocatechin Gallate on Bovine Serum Albumin Surface Using Quartz Crystal Microbalance with Dissipation Monitoring Wang, Xiaoyong; Ho, Chi-Tang; Huang, Qingrong Journal of Agricultural and Food Chemistry, Vol. 55, Issue 13 https://doi.org/10.1021/jf070590l	journal	May 2007
Monitoring the Binding Processes of Black Tea Thearubigin to the Bovine Serum Albumin Surface Using Quartz Crystal Microbalance with Dissipation Monitoring Chitpan, Monthana; Wang, Xiaoyong; Ho, Chi-Tang Journal of Agricultural and Food Chemistry, Vol. 55, Issue 25 https://doi.org/10.1021/jf072236t	journal	December 2007
Mechanisms of Protein Precipitation for Two Tannins, Pentagalloyl Glucose and Epicatechin ₁₆ (4→8) Catechin (Procyanidin) Hagerman, Ann E.; Rice, Mary E.; Ritchard, Nicole T. Journal of Agricultural and Food Chemistry, Vol. 46, Issue 7 https://doi.org/10.1021/jf971097k	journal	July 1998
Protein Interactions Studied by SAXS: Effect of Ionic Strength and Protein Concentration for BSA in Aqueous Solutions Zhang, Fajun; Skoda, Maximilian W. A.; Jacobs, Robert M. J. The Journal of Physical Chemistry B, Vol. 111, Issue 1 https://doi.org/10.1021/jp0649955	journal	January 2007
Effects of pH on the Interactions and Conformation of Bovine Serum Albumin: Comparison between Chemical Force Microscopy and Small-Angle Neutron Scattering Li, Yunqi; Lee, Jooyoung; Lal, Jyotsana The Journal of Physical Chemistry B, Vol. 112, Issue 12 https://doi.org/10.1021/jp077392h	journal	March 2008
Scaling Behaviors of α-Zein in Acetic Acid Solutions Li, Yunqi; Xia, Qiuyang; Shi, Ke The Journal of Physical Chemistry B, Vol. 115, Issue 32 https://doi.org/10.1021/jp203476m	journal	August 2011
Influence of Protein Self-Association on Complex Coacervation with Polysaccharide: A Monte Carlo Study Li, Yunqi; Huang, Qingrong The Journal of Physical Chemistry B, Vol. 117, Issue 9 https://doi.org/10.1021/jp309135m	journal	February 2013
Replica Exchange Monte Carlo Simulation of Human Serum Albumin–Catechin Complexes Li, Yunqi; An, Lijia; Huang, Qingrong The Journal of Physical Chemistry B, Vol. 118, Issue 35 https://doi.org/10.1021/jp5048503	journal	August 2014
Resveratrol, Genistein, and Curcumin Bind Bovine Serum Albumin Bourassa, P.; Kanakis, C. D.; Tarantilis, P. The Journal of Physical Chemistry B, Vol. 114, Issue 9 https://doi.org/10.1021/jp9115996	journal	February 2010
Mechanisms of Tannin-Induced Trypsin Inhibition: A Molecular Approach Gonçalves, Rui; Mateus, Nuno; Pianet, Isabelle Langmuir, Vol. 27, Issue 21 https://doi.org/10.1021/la202280c	journal	November 2011
Fabrication of Biopolymeric Complex Coacervation Core Micelles for Efficient Tea Polyphenol Delivery via a Green Process Zhou, Huihui; Sun, Xiaoyi; Zhang, Lili Langmuir, Vol. 28, Issue 41 https://doi.org/10.1021/la303062j	journal	October 2012
Structure of bovine β-lactoglobulin–lactoferrin coacervates Kizilay, Ebru; Seeman, Daniel; Yan, Yunfeng Soft Matter, Vol. 10, Issue 37 https://doi.org/10.1039/C4SM01333F	journal	January 2014
Recent developments on polyphenol–protein interactions: effects on tea and coffee taste, antioxidant properties and the digestive system Bandyopadhyay, Prasun; Ghosh, Amit K.; Ghosh, Chandrasekhar Food & Function, Vol. 3, Issue 6 https://doi.org/10.1039/c2fo00006g	journal	January 2012
A Review of Dietary Polyphenol-Plasma Protein Interactions: Characterization, Influence on the Bioactivity, and Structure-Affinity Relationship Xiao, Jianbo; Kai, Guoyin Critical Reviews in Food Science and Nutrition, Vol. 52, Issue 1 https://doi.org/10.1080/10408398.2010.499017	journal	January 2012
Interactions between Polyphenols and Macromolecules: Quantification Methods and Mechanisms Le Bourvellec, C.; Renard, C. M. G. C. Critical Reviews in Food Science and Nutrition, Vol. 52, Issue 3 https://doi.org/10.1080/10408398.2010.499808	journal	March 2012
Small-angle scattering studies of biological macromolecules in solution Svergun, Dmitri I.; Koch, Michel H. J. Reports on Progress in Physics, Vol. 66, Issue 10 https://doi.org/10.1088/0034-4885/66/10/R05	journal	September 2003
Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies Manach, Claudine; Williamson, Gary; Morand, Christine The American Journal of Clinical Nutrition, Vol. 81, Issue 1 https://doi.org/10.1093/ajcn/81.1.230S	journal	January 2005
PRIMUS: a Windows PC-based system for small-angle scattering data analysis Konarev, Petr V.; Volkov, Vladimir V.; Sokolova, Anna V. Journal of Applied Crystallography, Vol. 36, Issue 5, p. 1277-1282 https://doi.org/10.1107/S0021889803012779	journal	September 2003
GNOM – a program package for small-angle scattering data processing Semenyuk, A. V.; Svergun, D. I. Journal of Applied Crystallography, Vol. 24, Issue 5 https://doi.org/10.1107/S002188989100081X	journal	October 1991
CRYSOL – a Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates Svergun, D.; Barberato, C.; Koch, M. H. J. Journal of Applied Crystallography, Vol. 28, Issue 6 https://doi.org/10.1107/S0021889895007047	journal	December 1995
Investigation of the interaction between (−)-epigallocatechin-3-gallate with trypsin and α-chymotrypsin Wu, Xuli; He, Weiyi; Wang, Wenpu International Journal of Food Science & Technology https://doi.org/10.1111/ijfs.12223	journal	July 2013
Extracellular and Intracellular Polyphenol Oxidases Cause Opposite Effects on Sensitivity of Streptomyces to Phenolics: A Case of Double-Edged Sword Yang, Han-Yu; Chen, Carton W. PLoS ONE, Vol. 4, Issue 10 https://doi.org/10.1371/journal.pone.0007462	journal	October 2009
Investigate the Binding of Catechins to Trypsin Using Docking and Molecular Dynamics Simulation Cui, Fengchao; Yang, Kecheng; Li, Yunqi PLOS ONE, Vol. 10, Issue 5 https://doi.org/10.1371/journal.pone.0125848	journal	May 2015

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37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
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solution small-angle X-ray scattering
tea polyphenol

Small-Angle X-ray Scattering Study of Protein Complexes with Tea Polyphenols

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