Glycation and secondary conformational changes of human serum albumin: study of the FTIR spectroscopic curve-fitting technique

Yu-Ting Huang; Hui-Fen Liao; Shun-Li Wang; Shan-Yang Lin; Yu-Ting Huang; Hui-Fen Liao; Shun-Li Wang; Shan-Yang Lin

doi:10.3934/biophy.2016.2.247

AIMS Biophysics

2016, Volume 3, Issue 2: 247-260. doi: 10.3934/biophy.2016.2.247

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Research article

Glycation and secondary conformational changes of human serum albumin: study of the FTIR spectroscopic curve-fitting technique

1.
Department of Biotechnology and Pharmaceutical Technology, Yuanpei University of Medical Technology, Hsin Chu, Taiwan, ROC
2.
Department of Biochemical Science and Technology, National Chiayi University, Chiayi, Taiwan, ROC
3.
Department of Applied Chemistry, National Chiayi University, Chiayi, Taiwan, ROC

Received: 14 March 2016 Accepted: 17 May 2016 Published: 18 May 2016

The aim of this study was attempted to investigate both the glycation kinetics and protein secondary conformational changes of human serum albumin (HSA) after the reaction with ribose. The browning and fluorescence determinations as well as Fourier transform infrared (FTIR) microspectroscopy with a curve-fitting technique were applied. Various concentrations of ribose were incubated over a 12-week period at 37 ± 0.5 ^oC under dark conditions. The results clearly shows that the glycation occurred in HSA-ribose reaction mixtures was markedly increased with the amount of ribose used and incubation time, leading to marked alterations of protein conformation of HSA after FTIR determination.
In addition, the browning intensity of reaction solutions were colored from light to deep brown, as determined by optical observation. The increase in fluorescence intensity from HSA–ribose mixtures seemed to occur more quickly than browning, suggesting that the fluorescence products were produced earlier on in the process than compounds causing browning. Moreover, the predominant α-helical composition of HSA decreased with an increase in ribose concentration and incubation time, whereas total β-structure and random coil composition increased, as determined by curve-fitted FTIR microspectroscopy analysis. We also found that the peak intensity ratios at 1044 cm⁻¹/1542 cm⁻¹markedly decreased prior to 4 weeks of incubation, then almost plateaued, implying that the consumption of ribose in the glycation reaction might have been accelerated over the first 4 weeks of incubation, and gradually decreased. This study first evidences that two unique IR peaks at 1710 cm⁻¹ [carbonyl groups of irreversible products produced by the reaction and deposition of advanced glycation end products (AGEs)] and 1621 cm⁻¹ (aggregated HSA molecules) were clearly observed from the curve-fitted FTIR spectra of HSA-ribose mixtures over the course of incubation time. This study clearly suggests that FTIR spectroscopic curve-fitting technique may be easily used to allow determining the marked changes in the secondary conformational structure and protein aggregation of HSA during ribosylation as well as the production of AGEs.
- human serum albumin (HSA),
- ribose,
- ribosylation,
- FTIR,
- curve-fitting,
- browning,
- fluorescence,
- protein aggregation,
- AGEs
Citation: Yu-Ting Huang, Hui-Fen Liao, Shun-Li Wang, Shan-Yang Lin. Glycation and secondary conformational changes of human serum albumin: study of the FTIR spectroscopic curve-fitting technique[J]. AIMS Biophysics, 2016, 3(2): 247-260. doi: 10.3934/biophy.2016.2.247

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Abstract

The aim of this study was attempted to investigate both the glycation kinetics and protein secondary conformational changes of human serum albumin (HSA) after the reaction with ribose. The browning and fluorescence determinations as well as Fourier transform infrared (FTIR) microspectroscopy with a curve-fitting technique were applied. Various concentrations of ribose were incubated over a 12-week period at 37 ± 0.5 ^oC under dark conditions. The results clearly shows that the glycation occurred in HSA-ribose reaction mixtures was markedly increased with the amount of ribose used and incubation time, leading to marked alterations of protein conformation of HSA after FTIR determination.
In addition, the browning intensity of reaction solutions were colored from light to deep brown, as determined by optical observation. The increase in fluorescence intensity from HSA–ribose mixtures seemed to occur more quickly than browning, suggesting that the fluorescence products were produced earlier on in the process than compounds causing browning. Moreover, the predominant α-helical composition of HSA decreased with an increase in ribose concentration and incubation time, whereas total β-structure and random coil composition increased, as determined by curve-fitted FTIR microspectroscopy analysis. We also found that the peak intensity ratios at 1044 cm⁻¹/1542 cm⁻¹markedly decreased prior to 4 weeks of incubation, then almost plateaued, implying that the consumption of ribose in the glycation reaction might have been accelerated over the first 4 weeks of incubation, and gradually decreased. This study first evidences that two unique IR peaks at 1710 cm⁻¹ [carbonyl groups of irreversible products produced by the reaction and deposition of advanced glycation end products (AGEs)] and 1621 cm⁻¹ (aggregated HSA molecules) were clearly observed from the curve-fitted FTIR spectra of HSA-ribose mixtures over the course of incubation time. This study clearly suggests that FTIR spectroscopic curve-fitting technique may be easily used to allow determining the marked changes in the secondary conformational structure and protein aggregation of HSA during ribosylation as well as the production of AGEs.

References

[1]	Vanhooren V,Navarrete Santos A,Voutetakis K, et al. (2015) Protein modification and maintenance systems as biomarkers of ageing. Mech Ageing Dev 151: 71–84. doi: 10.1016/j.mad.2015.03.009
[2]	Uribarri J, Woodruff S, Goodman S, et al. (2010) Advanced glycation end products in foods and a practical guide to their reduction in the diet. J Am Diet Assoc 110: 911–916.e12 doi: 10.1016/j.jada.2010.03.018
[3]	Visentin S,Medana C,Barge A, et al. (2010) Microwave-assisted Maillard reactions for the preparation of advanced glycation end products (AGEs). Org Biomol Chem 8: 2473–2477. doi: 10.1039/c000789g
[4]	Horvat S,Jakas A (2014) Peptide and amino acid glycation: new insights into the Maillard reaction. J Pept Sci 10: 119–137.
[5]	Zhang Q,Ames JM,Smith RD, et al. (2009) A perspective on the Maillard reaction and the analysis of protein glycation by mass spectrometry: probing the pathogenesis of chronic disease. J Proteome Res 8: 754–769. doi: 10.1021/pr800858h
[6]	Dar B, Dar M, Bashir S, et al. (2015) Glycosylated hemoglobin (HbA1c): A biomarker of anti-aging. Int J Biol Med Res 6: 5084–5086.
[7]	Sebeková K,Somoza V (2007) Dietary advanced glycation endproducts (AGEs) and their health effects--PRO. Mol Nutr Food Res 51: 1079–1084. doi: 10.1002/mnfr.200700035
[8]	Arasteh A,Farahi S,Habibi-Rezaei M, et al. (2014) Glycated albumin: an overview of the in vitro models of an in vivo potential disease marker. J Diabetes Metab Disord 13: 49.
[9]	Uribarri J,del Castillo MD,de la Maza MP, et al. (2015) Dietary advanced glycation end products and their role in health and disease. Adv Nutr 6: 461–473. doi: 10.3945/an.115.008433
[10]	Takahashi M (2014) Glycation of Proteins. In Glycoscience: Biology and Medicine, Endo T, Seeberger PH, Hart GW, Wong CH, Taniguchi N, eds., Springer Japan, pp. 1339–1345
[11]	Nursten HE (2005) The Maillard Reaction: Chemistry, Biochemistry, and Implications. RSC.
[12]	Laroque D, Inisan C, Berger C, et al. (2008) Kinetic study on the Maillard reaction: Consideration of sugar reactivity. Food Chem 111: 1032–1042 doi: 10.1016/j.foodchem.2008.05.033
[13]	Sattarahmady N,Moosavi-Movahedi AA,Habibi-Rezaei M, et al. (2008) Detergency effects of nanofibrillar amyloid formation on glycation of human serum albumin. Carbohydr Res 343: 2229–2234.
[14]	Monnier VM (1990) Nonenzymatic glycosylation, the Maillard reaction and the aging process. J Gerontol 45: B105–111. doi: 10.1093/geronj/45.4.B105
[15]	Wei Y,Han CS,Zhou J, et al. (2012) D-ribose in glycation and protein aggregation. Biochim Biophys Acta 1820: 488–494. doi: 10.1016/j.bbagen.2012.01.005
[16]	Monnier VM, Cerami A (1981) Nonenzymatic browning in vivo: possible process for aging of long-lived proteins. Science 211: 491–493. doi: 10.1126/science.6779377
[17]	Han C,Lu Y,Wei Y, et al. (2011) D-ribose induces cellular protein glycation and impairs mouse spatial cognition. PLoS ONE 6:e24623. doi: 10.1371/journal.pone.0024623
[18]	Syrový I (1994) Glycation of albumin: reaction with glucose, fructose, galactose, ribose or glyceraldehyde measured using four methods. J Biochem Biophys Methods 28: 115–121. doi: 10.1016/0165-022X(94)90025-6
[19]	Kong FL,Cheng W,Chen J, et al. (2011) D-Ribose glycates β(2)-microglobulin to form aggregates with high cytotoxicity through a ROS-mediated pathway. Chem Biol Interact 194: 69–78. doi: 10.1016/j.cbi.2011.08.003
[20]	Khan MS,Dwivedi S,Priyadarshini M, et al. (2013) Ribosylation of bovine serum albumin induces ROS accumulation and cell death in cancer line (MCF-7). Eur Biophys J 42: 811–818.
[21]	Iannuzzi C,Maritato R,Irace G, et al. (2013) Glycation accelerates fibrillization of the amyloidogenic W7FW14F apomyoglobin. PLoS ONE 8: e80768. doi: 10.1371/journal.pone.0080768
[22]	Adrover M,Mariño L,Sanchis P, et al. (2014) Mechanistic insights in glycation-induced protein aggregation. Biomacromolecules 15: 3449–3462. doi: 10.1021/bm501077j
[23]	Liu J, Ru Q, Ding Y (2012) Glycation a promising method for food protein modification: Physicochemical properties and structure, a review. Food Res Int 49: 170–183.
[24]	Wei Y, Chen L, Chen J, et al. (2009) Rapid glycation with D-ribose induces globular amyloid-like aggregations of BSA with high cytotoxicity to SH-SY5Y cells. BMC Cell Biol 10: 10.
[25]	Kragh-Hansen U,Chuang VT,Otagiri M (2002) Practical aspects of the ligand-binding and enzymatic properties of human serum albumin. Biol Pharm Bull 25: 695–704.
[26]	Santra MK,Banerjee A,Krishnakumar SS, et al. (2004) Multiple-probe analysis of folding and unfolding pathways of human serum albumin. Evidence for a framework mechanism of folding. Eur J Biochem 271: 1789–1797.
[27]	Anguizola J,Matsuda R,Barnaby OS, et al. (2013) Review: Glycation of human serum albumin. Clin Chim Acta 2013; 425: 64–76.
[28]	Singha Roy A,Ghosh P,Dasgupta S (2015) Glycation of human serum albumin alters its binding efficacy towards the dietary polyphenols: A comparative approach. J Biomol Struct Dyn Oct 7:1–46. [In press].
[29]	Peters T (1996) All about Albumin. Biochemistry, Genetics, and Medical Applications. Academic Press, San Diego, CA.
[30]	Khan MW,Rasheed Z,Khan WA, et al. (2007) Biochemical, biophysical, and thermodynamic analysis of in vitro glycated human serum albumin. Biochemistry (Mosc) 72: 146–152. doi: 10.1134/S0006297907020034
[31]	Yang F,Zhang Y,Liang H (2014) Interactive association of drugs binding to human serum albumin. Int J Mol Sci 15: 3580–3595.
[32]	Lin SY,Wei YS,Li MJ,et al (2004). Effect of ethanol or/and captopril on the secondary structure of human serum albumin before and after protein binding. Eur J Pharm Biopharm 57: 457–464. doi: 10.1016/j.ejpb.2004.02.005
[33]	Lin SY, Wei YS, Li MJ (2004) Ethanol or/and captopril-induced precipitation and secondary conformational changes of human serum albumin. Spectrochim Acta A 60: 3107–3111. doi: 10.1016/j.saa.2004.03.001
[34]	Li MJ,Lin SY (2005) Vibrational spectroscopic studies on the disulfide formation and secondary conformational changes of captopril-HSA mixture after UV-B irradiation. Photochem Photobiol 81: 1404–1410. doi: 10.1562/2005-04-25-RN-497
[35]	Sadowska-Bartosz I,Galiniak S,Bartosz G (2014) Kinetics of glycoxidation of bovine serum albumin by glucose, fructose and ribose and its prevention by food components. Molecules 19: 18828–18849. doi: 10.3390/molecules191118828
[36]	Kosaraju SL,Weerakkody R,Augustin MA (2010) Chitosan-glucose conjugates: influence of extent of Maillard reaction on antioxidant properties. J Agric Food Chem 58: 12449–12455. doi: 10.1021/jf103484z
[37]	Ajandouz EH, Tchiakpe LS, Ore FD, et al. (2001) Effects of pH on caramelization and Maillard reaction kinetics in fructose-lysine model systems. J Food Sci 66: 926–931.
[38]	Monacelli F, Storace D, D’Arrigo C, et al. (2013)Structural alterations of human serum albumin caused by glycative and oxidative stressors revealed by circular dichroism analysis. Int J Mol Sci 14: 10694–10709.
[39]	Lee TH,Cheng WT,Lin SY (2010) Thermal stability and conformational structure of salmon calcitonin in the solid and liquid states. Biopolymers 93: 200–207. doi: 10.1002/bip.21323
[40]	Ledesma-Osuna AI, Ramos-Clamont G, Vazquez-Moreno L (2008) Characterization of bovine serum albumin glycated with glucose, galactose and lactose. Acta Biochim Pol 55: 491–497.
[41]	Sompong W,Meeprom A,Cheng H, et al. (2013) A comparative study of ferulic acid on different monosaccharide-mediated protein glycation and oxidative damage in bovine serum albumin. Molecules 18: 13886–13903. doi: 10.3390/molecules181113886
[42]	Wu CH, Huang SM, Lin JA, et al. (2011) Inhibition of advanced glycation endproduct formation by foodstuffs. Food Funct 2: 224–234.
[43]	Kato Y, Matsuda T, Kato N, et al. (1989) Maillard reaction of disaccharides with protein: suppressive effect of nonreducing end pyranoside groups on browning and protein polymerization. J Agric Food Chem 37: 1077–1081. doi: 10.1021/jf00088a057
[44]	Suárez G,Rajaram R,Oronsky AL, et al.(1989). Nonenzymatic glycation of bovine serum albumin by fructose (fructation). Comparison with the Maillard reaction initiated by glucose. J Biol Chem 264: 3674–3679.
[45]	McPherson JD,Shilton BH,Walton DJ (1988) Role of fructose in glycation and cross-linking of proteins. Biochemistry 27: 1901–1907.
[46]	Siddiqui AA,Sohail A,Bhat SA, et al. (2015). Non-enzymatic glycation of almond cystatin leads to conformational changes and altered activity. Protein Pept Lett 22: 449–459.
[47]	Awasthi S,Murugan NA,Saraswathi NT (2015) Advanced glycation end products modulate structure and drug binding properties of albumin. Mol Pharmaceutics 12: 3312–3322. doi: 10.1021/acs.molpharmaceut.5b00318
[48]	Bouma B,Kroon-Batenburg LM,Wu YP, et al. (2003) Glycation induces formation of amyloid cross-beta structure in albumin. J Biol Chem 278: 41810–41819. doi: 10.1074/jbc.M303925200
[49]	Khajehpour M,Dashnau JL,Vanderkooi JM (2006) Infrared spectroscopy used to evaluate glycosylation of proteins. Anal Biochem 348: 40–48. doi: 10.1016/j.ab.2005.10.009
[50]	GhoshMoulick R,Bhattacharya J,Roy S, et al. (2007). Compensatory secondary structure alterations in protein glycation. Biochim Biophys Acta 1774: 233–242. doi: 10.1016/j.bbapap.2006.11.018
[51]	Yang H,Yang S,Kong J, et al. (2015). Obtaining information about protein secondary structures in aqueous solution using Fourier transform IR spectroscopy. Nat Protoc 10: 382–396. doi: 10.1038/nprot.2015.024
[52]	Roy R,Boskey A,Bonassar LJ (2010) Processing of type I collagen gels using nonenzymatic glycation. J Biomed Mater Res A 93: 843–851.
[53]	Haris PI (2013) Probing protein-protein interaction in biomembranes using Fourier transform infrared spectroscopy. Biochim Biophys Acta 1828: 2265–2271.
[54]	Neault JF, Tajmir-Riahi HA (1998) Interaction of cisplatin with human serum albumin. Drug binding mode and protein secondary structure, Biochim. Biophys Acta 1384: 153–159.
[55]	Bramanti E, Benedetti E (1996) Determination of the secondary structure of isomeric forms of human serum albumin by a particular frequency deconvolution procedure applied to Fourier transform IR analysis. Biopolymers 38: 639–653.
[56]	Zsila F (2013) Subdomain IB is the third major drug binding region of human serum albumin: toward the three-sites model. Mol Pharmaceutics 10: 1668–1682. doi: 10.1021/mp400027q
[57]	Awasthi S,Murugan NA,Saraswathi NT (2015) Advanced glycation end products modulate structure and drug binding properties of albumin. Mol Pharmaceutics 12: 3312–3322.
[58]	Khan TA, Saleemuddin M, Naeem A (2011) Partially folded glycated state of human serum albumin tends to aggregate. Int J Pept Res Ther 17: 271–279. doi: 10.1007/s10989-011-9267-7
[59]	Oliveira LM,Lages A,Gomes RA, et al. (2011) Insulin glycation by methylglyoxal results in native-like aggregation and inhibition of fibril formation. BMC Biochem 5; 12:41. doi: 10.1186/1471-2091-12-41
[60]	Lin SY,Chu HL,Wei YS (2002) Pressure-induced transformation of alpha-helix to beta-sheet in the secondary structures of amyloid beta (1–40) peptide exacerbated by temperature. J Biomol Struct Dyn 19: 619–625.
[61]	Ding F,Borreguero JM,Buldyrey SV, et al. (2003) Mechanism for the alpha-helix to beta-hairpin transition. Proteins 53: 220–228. doi: 10.1002/prot.10468
[62]	Garip S,Yapici E,Ozek NS, et al. (2010) Evaluation and discrimination of simvastatin-induced structural alterations in proteins of different rat tissues by FTIR spectroscopy and neural network analysis. Analyst 135: 3233–3241. doi: 10.1039/c0an00540a
[63]	Yano K,Ohoshima S,Shimizu Y, et al. (1996) Evaluation of glycogen level in human lung carcinoma tissues by an infrared spectroscopic method. Cancer Lett 110: 29–34.
[64]	Podshyvalov A,Sahu RK,Mark S, et al. (2005) Distinction of cervical cancer biopsies by use of infrared microspectroscopy and probabilistic neural networks. Appl Opt 44: 3725–3734. doi: 10.1364/AO.44.003725
[65]	Colagar AH,Chaichi MJ,Khadjvand T (2011) Fourier transform infrared microspectroscopy as a diagnostic tool for distinguishing between normal and malignant human gastric tissue. J Biosci 36: 669–677.
[66]	Nagai R, Shirakawa J, Fujiwara Y, et al. (2014) Detection of AGEs as markers for carbohydrate metabolism and protein denaturation. J Clin Biochem Nutr 55: 1–6. doi: 10.3164/jcbn.13-112
[67]	Rondeau P,Bourdon E (2011) The glycation of albumin: structural and functional impacts. Biochimie 93: 645–658.
[68]	Basta G,Schmidt AM,De Caterina R (2004) Advanced glycation end products and vascular inflammation: implications for accelerated atherosclerosis in diabetes. Cardiovasc Res 63: 582–592. doi: 10.1016/j.cardiores.2004.05.001
[69]	Shivu B,Seshadri S,Li J, et al. (2013) Distinct β-sheet structure in protein aggregates determined by ATR-FTIR spectroscopy. Biochemistry 52: 5176–5183. doi: 10.1021/bi400625v
[70]	Natalello A,Doglia SM (2015) Insoluble protein assemblies characterized by fourier transform infrared spectroscopy. Methods Mol Biol 1258: 347–369. doi: 10.1007/978-1-4939-2205-5_20
[71]	Clark AH,Saunderson DH,Suggett A (1981) Infrared and laser-Raman spectroscopic studies of thermally-induced globular protein gels. Int J Pept Protein Res 17: 353–364.
[72]	Ruggeri FS,Longo G,Faggiano S, et al. (2015) Infrared nanospectroscopy characterization of oligomeric and fibrillar aggregates during amyloid formation. Nat Commun 6: 7831.
[73]	Miller LM,Bourassa MW,Smith RJ (2013) FTIR spectroscopic imaging of protein aggregation in living cells. Biochim Biophys Acta 1828: 2339–2346.

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