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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Advanced glycation end products (AGEs) have received considerable attention since glycation can easily occur both outside (exogenously) and inside (endogenously) the body 1. AGEs can be exogenously formed during food preparation by heating 2,3, whereas an endogenous glycation reaction is easily triggered by the interaction between a carbohydrate and a protein without the involvement of an enzyme. AGEs slowly accumulate in vivo and make cells stiffer, i.e. less pliable and more prone to damage and premature aging caused by protein dysfunction 4,5,6. Nowadays, a number of studies have confirmed that AGEs are associated with the development or worsening of many degenerative diseases such as cataracts, diabetes, atherosclerosis, chronic renal failure, Parkinson’s disease, Alzheimer's disease, and amyotrophic lateral sclerosis 7,8,9. The process of glycation starts with the formation of a Schiff base, followed by Amadori products, and various intermediate compounds are then produced, followed by the eventual formation of AGEs; this process is also referred as nonenzymatic glycosylation or the Maillard reaction 4,10,11. Thus, the study of AGEs has become one of the most important areas of biochemistry today.
It is well known that all reducing sugars can participate in the glycation reaction in combination with various amino acids 12,13. Sugar type is one of the numerous factors affecting the rate of the Maillard reaction, with pentoses having been found to be more reactive than hexoses. The glycating ability of reducing sugars was found to increase in the following order: D-glucose < D-mannose < D-galactose < D-xylose < D-fructose < D-arabinose < D-ribose 14,15. Among these reducing sugars, D-ribose is the most reactive in the glycation of proteins and results in a more rapid production of AGEs than other sugars in vitro and in vivo 16,17,18.
Recently, the glycation of proteins with ribose (ribosylation) has attracted more attention due to protein aggregation and fibrillation, and the generation of reactive oxygen species (ROS) 15,19,20,21. However, several controversial results have led to a debate on whether glycation or ribosylation alters the protein conformational structure 21,22,23,24. For this reason, ribosylation needs to be further investigated by evaluating the protein secondary conformational structure changes caused by the reaction.
In the present study, human serum albumin (HSA) was used as a model protein. It has been extensively used as a model for protein-folding and ligand-binding studies because it is the most abundant protein constituent of blood plasma in the human body 25,26. There has also been much focus on the effects of glycation on the structure of HSA 27,28, which is divided into three homologous helical domains in which each domain is further subdivided into two subdomains with a common helical motif 29. Nonenzymatic glycation of HSA may affect its protein binding properties, thus resulting in abnormal biological effects 30, and many studies have indicated conformational changes of HSA after drug-protein binding 31. In our previous studies, the effects of ethanol and/or captopril on the secondary structure of HSA before and after protein binding were investigated by Fourier transform infrared (FTIR) microspectroscopy 32,33. Disulfide formation and secondary conformational changes in a captopril-HSA mixture after UV-B irradiation were also detected 34. In this study, we attempt to examine the secondary conformational structure of HSA molecules after ribosylation using transmission FTIR microspectroscopy. UV absorbance, browning, and fluorescence development of Maillard reaction products (MRPs) in the HSA-ribose system were also determined.
Human serum albumin (HSA), D-ribose, and deuterium oxide (D2O) were purchased from Sigma-Aldrich Co. LLC. (St. Louis, MO, USA) and used as supplied without further purification. All the reagents were of analytical grade and were also obtained from Sigma-Aldrich Co. LLC. The potassium bromide (KBr) crystals for the pellets were obtained from Jasco Parts Center (Jasco Co., Tokyo, Japan).
The glycation reaction of HSA with ribose was performed using a modification of the Sadowska-Bartoszmethod detailed in our previous studies 30,31,32,35.
HSA (50 mg/mL) was previously dissolved in D2O with 0.03% sodium azide and incubated with different concentrations of ribose (10-200 mM) for 12 weeks at 37 ± 0.5 ℃ under dark conditions. At pre-defined intervals, the incubated solution was sampled for the following investigations.
(a) Measurement of nonenzymatic browning intensity of the samples using a UV/visible spectrophotometer (Cary 50 Conc., Varian, Australia) at 420 nm 36,37.
(b) Observation of color images of samples using a digital camera.
(c) Since ribose had been reported to be a strong inducer of fluorescence at 370 nm excitation and 440 nm emission 38, thus in this study the fluorescence intensities of HSA and HSA-ribose mixtures were determined using a fluorescence spectrophotometer (F-4500, Hitachi, Japan) by setting at 370 nm excitation and 440 nm emission.
(d) Measurement of the secondary conformational structure of HSA by FTIR microspectroscopy (IRT-5000-16/FTIR-6200, Jasco Co., Tokyo, Japan) using a film method on a calcium fluoride (CaF2) plate via a transmission technique 39.
The software, Spectral Manager for Windows (Jasco Co., Tokyo, Japan) and GRAMS spectroscopy software suite (Version 7, Thermo Electron Co., MA, USA), were used for data acquisition and handling. The basic principle of curve fitting was to reconstruct the original amide Ⅰ spectrum, then the baseline was first corrected from 1600-1700 cm-1, followed secondary derivative. The number of bands and positions were taken from their second derivative spectra. Second derivative spectral analysis was previously applied to locate the position of the overlapping components in the amide Ⅰ band and assigned to different secondary structures. Then these peaks obtained in the secondary derivatives were used for the curve fitting. The protein secondary structure and the composition of each component in the amide Ⅰ band of the IR spectra were quantitatively estimated by a least-squares fitting program iterating the curve-fitting process using a Gaussian function. In the fitting process, the heights, widths, and positions of all bands were varied simultaneously. The rationale of any curve fitting procedure was to minimize the differences between the experimental absorption spectrum and the fitted spectrum. The curve fitting was performed by stepwise iterative adjustment towards minimum standard errors of the different parameters determining the shape and position of the absorption peaks. Finally, the proportion of a component was computed to be the fractional area of the corresponding peak divided by the sum of the areas of all the peaks 32,33,34.
All the tests were conducted in triplicate, and mean values with standard deviations were obtained. The significance of the differences between variables was determined using one-way analysis of variance (ANOVA).
It is well known that the Maillard reaction may result in the formation of final browning compounds due to an advanced glycation reaction, so the UV absorbance and browning of MRPs were measured by UV spectroscopy using several reported methods 36,37. The absorbance values (A420) at 420 nm were used as an indicator of browning development in the final stage of the browning reaction. Figure 1-A shows the change in browning intensity of HSA-ribose mixtures during the 12-week incubation period. It clearly indicates that the browning intensity, measured as A420 values of the HSA-ribose mixtures, markedly increased with the concentration of ribose and the incubation time; the higher the concentration of ribose used, the higher the increase in A420 values (p < 0.05). In comparison, there were no changes for HSA or ribose alone (p > 0.05). The reaction mixture formed a gel after 6 weeks at the highest concentration of ribose used (50 mM), and further continuous measurement of UV absorption levels of the gelled samples could no longer be performed by UV spectroscopy. In addition, a large increase in the browning absorbance at 420 nm seems to be exponentially enhanced for the higher concentrations of ribose used in the course of incubation period.
The total color changes of the HSA aqueous solutions after the reaction with or without ribose were visiblyobserved, and the results are shown in Figure 1-B. Obviously, the reaction solutions colored from light to deep brown, suggesting that the Maillard reaction had occurred between the amino acids of HSA and the reactive reducing moieties of ribose. Compared with other sugars such as glucose and fructose, ribose was the most strongly glycative molecule to cause the browning reaction indicating glycation (data not shown), which is consistent with results from other studies 14,15. Moreover, the rate of glycation was also dependent on the type and concentration of monosaccharide 24,40,41. The highest glycating capability of ribose might be due to its planar structure causing the unstable aldofuranose ring to react with the amino groups 24.
Figure 1.The changes in browning intensity (A) and total color appearance (B) of HSA-ribose mixtures over the course of 12 weeks of incubation.
Figure 2.The changes in fluorescence intensity of HSA-ribose mixtures over the course of 12 weeks of incubation.
AGEs are highly heterogeneous compounds classified into two major groups: fluorescent/crosslinking structures and non-fluorescent/ non-crosslinking structures 42. We only investigated the total fluorescence of HSA-ribose mixtures using a fluorescence spectrophotometer in the present study. The results indicate that the fluorescence of the resulting mixtures increased with the length of incubation time, as shown in Figure 2. It is evident that the fluorescence intensityof HSA-ribose mixtures rapidly increased with the amount of ribose used and incubation time. Moreover, the increased fluorescence intensitywas also dependent on the ribose concentration used; the higher the concentration of ribose used, the more rapidly the fluorescence was observed. After incubation for 6-8 weeks, the fluorescence had almost reached a plateau, and over this period, the increase in the fluorescence intensity of the HSA-ribose mixtures seemed to occur more quickly than for browning. This might be because the fluorescent products were produced earlier on in the reaction than the browning compound, which is consistent with the results of Kato et al. 43. In addition, thefaster rate of fluorescence generation for nonenzymatically glycated HSA was possibly related to a faster conversion of the Amadori groups, similar to that of the glycation/fructation of bovine serum albumin or HSA 44,45.
Nonenzymaticglycation leads to the formation of inter- and intramolecular cross-links in proteins. This reaction not only modifies the conformation of proteins but also induces altered biological activity 46. Since albumin has been reported to be highly susceptible to nonenzymatic glycation 27,47, it is of interest to determine the structural alterations in HSA modified by glycation. In order to detect the glycation-induced changes in protein conformation, several targets have been focused on in studies of the products of glycosylation reactions or of changes in either protein or sugar structure using variousmethods 48,49,50. In the present study, we used transmission FTIR microspectroscopy with a curve-fitting technique to investigate the secondary conformational changes of glycated HSA.
Figure 3 shows the representative FTIR spectra of native HSA, ribose, and HSA-ribose (50 mg/mL/50 mM) using a film method on a CaF2 plate via a transmission FTIR technique. The FTIR spectra of all samples in the wave amplitude range between 3800-2200 and 1800-800 cm-1 were examined. The characteristic IR absorption bands and their assignments for native HSA are as follows (in cm-1): 3303 (amide A, N-H stretching), 2960 (C-H stretching), 1654 (amide Ⅰ, C=O stretching), 1542 (amide Ⅱ, C-N stretching and N-H bending), 1464 (C-H2 bending), 1398 (carboxylate) and 1311-1247 cm-1 (Amide Ⅲ, C-N stretching and N-H bending) 51. For native HSA, the bands between 1500 and 1000 cm-1 are in the“fingerprint”region. On the other hand, the FTIR spectrum of ribose shows strong peaks between 1200 and 1000 cm-1. Both peaks at 1085 and 1042 cm-1 can be used to distinguish the presence of ribose attached to HSA. The bands at 3369 and 2933 cm-1 are assigned to the CH and OH vibrational groups of ribose. The bands found in the 1200-1000 cm-1 range correspond to C-O and C-C stretching vibrations and the C-OH and C-C-O bending vibrations of ribose 52. Once ribose was mixed with HSA at the initial stage, the FTIR spectrum of the HSA-ribose mixture was only superimposed by the FTIR spectra of HSA and ribose. Two marked FTIR peaks at 1088 and 1044 cm-1 were due to ribose, except the FTIR peaks belonging to HSA.
Figure 3.Representative FTIR spectra of native HSA, ribose, and HSA-ribose (50 mg/ml/50 mM) determined by a film method on a CaF2 plate via transmission FTIR.
Although the specific stretching and bending vibrations of the peptide backbone in amide Ⅰ, Ⅱ, and Ⅲ bands may provide information on various types of secondary structure, it is well known that the amide Ⅰ band is particularly sensitive to protein secondary structure changes than the others 51,53. Figure 4 shows the curve-fitted amide Ⅰ band of HSA with and without the addition of ribose at the initial stage; the curve-fitted amide Ⅰ bands of both HSA samples and their components, assignments, and compositions are illustrated. The results clearly indicate that the structural composition of native HSA without adding ribose consists of 56.0% α-helix (1652 cm-1), 4.4% random coil (1638 cm-1), and 39.6% β-structure (1677 and 1665 cm-1: β-turn (26.2%);, 1630 and 1620 cm-1: β-sheet (13.3%)), which is consistent with the results of other studies 54,55. The same procedure of fitting was applied to the FTIR spectrum recorded for native HSA after adding ribose at an early stage in the process and yielded the following percentages of secondary structures: 56.5% α-helix (1651 cm-1), 2.6% random coil (1638 cm-1), and 38.9% β-structure (1676 and 1664 cm-1: β-turn (25.7%); 1630 and 1620 cm-1: β-sheet (15.2%)). Both samples exhibited a similar structural composition, suggesting there were no alterations in HSA conformation after the initial addition of ribose.
However, the structural composition of HSA after its reaction with ribose was markedly changed by the amount of ribose added and the length of incubation time, at 37 ± 0.5 ℃ and under dark conditions, as shown in Figure 5. It is evident that the α-helix composition of HSA decreased with an increase in ribose concentration and incubation time, whereas the total β-structure and random coil composition increased.
Figure 4.The curve-fitted FTIR amide Ⅰ band of HSA without or with the addition of ribose at the initial stage
Figure 5.The effect of the concentration of added ribose on the secondary conformational composition of the curve-fitted amide Ⅰ band of HSA over the course of 12 weeks of incubation. (Eachdata point represents the mean ± standard deviation(SD) of three independent determinations, but these SD values were too low to show the bars.)
This could be attributed to the loss of helical content due to AGE modification leading to an increase in β-conformation. This is consistent with the results from glycated albumin that showed induced conformational transition from its native α-helical structure to a β-sheeted form 50,56,57, resulting in the formation of protein aggregation and fibrillation 13,27,58,59. Similar results had also been reported that the interconversion from α-helix conformation to β-sheet structures via a random coil state was found in the other studies 60,61,62, in which drug or pressure might induce structural alterations in protein conformational transition from α-helix to random coil and to β-sheet structure.
As was previously mentioned, all reducing sugars are capable of participating in glycation reactions, and ribose is more active in the glycation of proteins than other reducing sugars 14,15,16,17,18. Figure 6 reveals the changes in the ribose consumed in the reaction mixtures during the course of incubation. The peak at 1044 cm-1 was found in the 1200-1000 cm-1 range and corresponded to C-O/C-C stretching vibrations and/or the C-OH/C-C-O bending vibrations of ribose 52. This peak can be used as an internal marker to estimate the practical participation of ribose in glycation reactions between HSA and ribose, as shown in Figure 6. Since the peak intensity of amide Ⅱ band at 1542 cm-1 did not alter over the course of incubation, the peak intensity of 1044 cm-1 was normalized to the peak at 1542 cm-1 to determine the consumption of ribose during the reaction 63,64,65. It is apparent that the peak intensity ratios of 1044 cm-1/1542 cm-1 were markedly decreased with an increase in incubation time up to 4 weeks. After that the changes and the process gradually slowed down. This implies that the glycation process seems to have accelerated over the initial 4-week incubation period and then gradually decreased.
Figure 6.The alterations of ribose consumption for the HSA-ribose reaction mixtures over the course of 12 weeks of incubation.
Nonenzymatic glycation or the Maillard reaction is a process between free amino acid residues of proteins and carbonyl groups of reducing sugars and finally generates AGEs through the formation of a Schiff base and Amadori products 66,67. AGEs are constructed by a class of irreversible heterogeneous compounds formed by glycation 67 and characterized by a brown color, an auto-fluorescence, and intra- and intermolecular cross-linkings, as shown in Figures 1 and 2. After the application of the FTIR curve-fitting technique to the IR spectra of the HSA-ribose mixtures after glycation, a new curve-fitted FTIR peak at 1710 cm-1 was incidentally found after an increase in incubation time, as illustrated in Figure 7. This peak at 1710 cm-1 might be due to the carbonyl groups of the complex, irreversible heterogeneous compounds in AGEs such as carboxymethyllysine, pentosidine, pyrraline, carboxyethyllysine and imidanolone 15,68, although we did not attempt to identifythese compounds. Obviously, the curve-fitted FTIR peak area at 1710 cm-1 increased with incubation time. This clearly shows that the formation of irreversible products and deposition of AGEs gradually occurred in the HSA-ribose mixtures as the incubation time increased.
Figure 7.The changes in peak area at 1710 and 1621 cm-1 from the curve-fitted amide Ⅰ band of the HSA-ribose reaction mixtures over the course of 12 weeks of incubation.
FTIR spectroscopy has been used to monitor the aggregation of proteins during various treatments 69,70. From the curve-fitted FTIR spectra in Figure 7, we can clearly see that an FTIR peak area at 1621 cm-1 was enhanced as the incubation time increased. An increased peak area at 1621 cm-1 could indicate the formation of intermolecular β-sheets within aggregated protein molecules 71,72,73. As the incubation time increases, the gel formation in the reaction mixtures might point toward the aggregation of HSA after ribosylation.
In summary, we present the first application of transmission FTIR microspectroscopy with a curve-fitting technique to investigate the secondary conformational changes of HSA after ribosylation. Moreover, the conformational transition in HSA after ribosylation from its native α-helical structure to a β-sheeted form was confirmed. In particular, two unique IR peaks at 1710 and 1620 cm-1 from the curve-fitted FTIR spectra, the former possibly indicating the gradual formation of the carbonyl groupsof irreversible products of the reaction and the deposition of AGEs in the reaction mixtures of HSA-ribose, and the latter signifying the formation of intermolecularβ-sheets within aggregated HSA molecules after ribosylation.
All Authors declare no conflicts of interest in this paper.
| [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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Figures(7)
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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