Interaction of Glycated Albumin with Receptor for Glycation End Products According to Molecular Modeling Data
- Authors: Belinskaia D.A.1, Goncharov N.V.1,2
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Affiliations:
- Sechenov Institute of Evolutionary Physiology and Biochemistry of the Russian Academy of Sciences
- Research Institute of Hygiene, Occupational Pathology and Human Ecology
- Issue: Vol 109, No 12 (2023)
- Pages: 1810-1831
- Section: EXPERIMENTAL ARTICLES
- URL: https://medjrf.com/0869-8139/article/view/651693
- DOI: https://doi.org/10.31857/S0869813923120026
- EDN: https://elibrary.ru/ZJCOKS
- ID: 651693
Cite item
Abstract
In diabetes mellitus (DM) patients, the accumulation of advanced glycation end products (AGE) leads to inflammation and oxidative stress through the activation of specific receptors for AGE (RAGE). Glycated albumin (gHSA) makes a significant contribution to the overall level of AGE in human body and, as a result, to the pathogenesis of DM and concomitant diseases. The mechanism of interaction of gHSA with RAGE is practically not studied. The purpose of the present paper is to study the binding of gHSA to RAGE using molecular modeling methods, to find the main sites of interaction and structural features of glycation sites that determine the efficiency of complex formation with RAGE. Ten gHSA models were constructed using molecular docking and molecular dynamics (MD) methods; each model corresponded to one modified lysine residue (carboxymethyl-lysine): Lys64, Lys73, Lys137, Lys233, Lys262, Lys317, Lys378, Lys525, Lys573, Lys574. Complexes of gHSA with the V-domain of RAGE were constructed using the macromolecular docking method, and their stability was studied using MD simulation. In the constructed gHSA models, the carboxyl groups of glycated Lys317 and Lys525 form intramolecular salt bridges with surrounding amino acids; in other cases, the carboxyl groups of the modified lysines are free to interact with positively charged amino acid residues on the RAGE surface. According to the macromolecular docking data and subsequent MD simulation, the complex of RAGE with gHSA glycated at Lys233 is most effective in terms of strength and specificity. Specific RAGE complexes with gHSA glycated at Lys317 and Lys574 are not formed. The obtained data on the interaction of gHSA with RAGE will help to understand the role of albumin in the pathophysiology of DM and advance towards the prevention and development of effective therapy for this disease.
About the authors
D. A. Belinskaia
Sechenov Institute of Evolutionary Physiology and Biochemistry of the Russian Academy of Sciences
Author for correspondence.
Email: d_belinskaya@mail.ru
Russia, St. Petersburg
N. V. Goncharov
Sechenov Institute of Evolutionary Physiology and Biochemistry of the Russian Academy of Sciences; Research Institute of Hygiene, Occupational Pathology and Human Ecology
Email: d_belinskaya@mail.ru
Russia, St. Petersburg; Russia, Leningradsky Region, p.o. Kuz’molovsky
References
- Gounden V, Ngu M, Anastasopoulou C, Jialal I (2020) Fructosamine. In: Stat Pearls. StatPearls Publ. Treasure Island (FL).
- Vlassopoulos A, Lean MEJ, Combet E (2013) Role of oxidative stress in physiological albumin glycation: A neglected interaction. Free Radic Biol Med 60: 318–324. https://doi.org/10.1016/j.freeradbiomed.2013.03.010
- Belsare S, Coté G (2021) Development of a colorimetric paper fluidic dipstick assay for measurement of glycated albumin to monitor gestational diabetes at the point-of-care. Talanta 223(Pt 1): 121728. https://doi.org/10.1016/j.talanta.2020.121728
- Bettiga A, Fiorio F, Di Marco F, Trevisani F, Romani A, Porrini E, Salonia A, Montorsi F, Vago R (2019) The modern western diet rich in advanced glycation end-products (AGEs): An overview of its impact on obesity and early progression of renal pathology. Nutrients 11(8): 1748. https://doi.org/10.3390/nu11081748
- Fritz G (2011) RAGE: A single receptor fits multiple ligands. Trends Biochem Sci 36: 625–632. https://doi.org/10.1016/j.tibs.2011.08.008
- Гаврилова АО, Северина АС, Шамхалова МШ, Шестакова МВ (2021) Роль конечных продуктов гликирования в патогенезе диабетической нефропатии. Сахарный диабет 24(5): 461–469. [Gavrilova AO, Severina AS, Shamkhalova MSH, Shestakova MV (2021) The role of advanced glycation end products in patogenesis of diabetic nephropathy. Sakharnyy Diabet 24(5): 461–469. (In Russ)]. https://doi.org/10.14341/DM12784
- Gill V, Kumar V, Singh K, Kumar A, Kim JJ (2019) Advanced glycation end products (AGEs) may be a striking link between modern diet and health. Biomolecules 9(12): 888. https://doi.org/10.3390/biom9120888
- Smith PK (2017) Do advanced glycation end-products cause food allergy? Curr Opin Allergy Clin Immunol 17: 325–331. https://doi.org/10.1097/ACI.0000000000000385
- Sukkar MB, Wood LG, Tooze M, Simpson JL, McDonald VM, Gibson PG, Wark PAB (2012) Soluble RAGE is deficient in neutrophilic asthma and COPD. Eur Respir J 39: 721–729. https://doi.org/10.1183/09031936.00022011
- Gutowska K, Czajkowski K, Kuryłowicz A (2023) Receptor for the Advanced Glycation End Products (RAGE) Pathway in Adipose Tissue Metabolism. Int J Mol Sci 24(13): 10982. https://doi.org/10.3390/ijms241310982
- Morales ME, Rojas RA, Monasterio AV, González BI, Figueroa CI, Manques M B, Romero EJ, Llanos LJ, Valdés ME, Cofré LC (2013) Lesiones gástricas en pacientes infectados con Helicobacter pylori: Expresión de RAGE (receptor de productos de glicosilización avanzada) y otros inmunomarcadores. Rev Med Chil 141: 1240–1248. https://doi.org/10.4067/S0034-98872013001000002
- Fasano M, Curry S, Terreno E, Galliano M, Fanali G, Narciso P, Notari S, Ascenzi P (2005) The extraordinary ligand binding properties of human serum albumin. IUBMB Life 57(12): 787–796. https://doi.org/10.1080/15216540500404093
- van der Vusse GJ (2009) Albumin as fatty acid transporter. Drug Metab Pharmacokinet 24(4): 300–307. https://doi.org/10.2133/dmpk.24.300
- Giglio RV, Lo Sasso B, Agnello L, Bivona G, Maniscalco R, Ligi D, Mannello F, Ciaccio M (2020) Recent Updates and Advances in the Use of Glycated Albumin for the Diagnosis and Monitoring of Diabetes and Renal, Cerebro- and Cardio-Metabolic Diseases. J Clin Med 9: 3634. https://doi.org/10.3390/jcm9113634
- Arasteh A, Farahi S, Habibi-Rezaei M, Moosavi-Movahedi AA (2014) Glycated albumin: an overview of the In Vitro models of an In Vivo potential disease marker. J Diabetes Metab Disord 13: 49. https://doi.org/10.1186/2251-6581-13-49
- Qiu HY, Hou NN, Shi JF, Liu YP, Kan CX, Han F, Sun XD (2021) Comprehensive overview of human serum albumin glycation in diabetes mellitus. World J Diabetes 12(7): 1057–1069. https://doi.org/10.4239/wjd.v12.i7.1057
- Xie J, Reverdatto S, Frolov A, Hoffmann R, Burz DS, Shekhtman A (2008) Structural basis for pattern recognition by the receptor for advanced glycation end products (RAGE). J Biol Chem 283(40): 27255–27269. https://doi.org/10.1074/jbc.M801622200
- Tramarin A, Naldi M, Degani G, Lupu L, Wiegand P, Mazzolari A, Altomare A, Aldini G, Popolo L, Vistoli G, Przybylski M, Bartolini M (2020) Unveiling the molecular mechanisms underpinning biorecognition of early-glycated human serum albumin and receptor for advanced glycation end products. Anal Bioanal Chem 412(18): 4245–4259. https://doi.org/10.1007/s00216-020-02674-w
- Hanwell MD, Curtis DE, Lonie DC, Vandermeersch T, Zurek E, Hutchison GR (2012) Avogadro: an advanced semantic chemical editor, visualization, and analysis platform. J Cheminform 4(1): 17. https://doi.org/10.1186/1758-2946-4-17
- Hein KL, Kragh-Hansen U, Morth JP, Jeppesen MD, Otzen D, Møller JV, Nissen P (2010) Crystallographic analysis reveals a unique lidocaine binding site on human serum albumin. J Struct Biol 171(3): 353–360. https://doi.org/10.1016/j.jsb.2010.03.014
- Kislinger T, Fu C, Huber B, Qu W, Taguchi A, Du Yan S, Hofmann M, Yan SF, Pischetsrieder M, Stern D, Schmidt AM (1999) N(epsilon)-(carboxymethyl)lysine adducts of proteins are ligands for receptor for advanced glycation end products that activate cell signaling pathways and modulate gene expression. J Biol Chem 274(44): 31740–31749. https://doi.org/10.1074/jbc.274.44.31740
- Yatime L, Andersen GR (2013) Structural insights into the oligomerization mode of the human receptor for advanced glycation end-products. FEBS J 280(24): 6556–6568. https://doi.org/10.1111/febs.12556
- Mohan SK, Gupta AA, Yu C (2013) Interaction of the S100A6 mutant (C3S) with the V domain of the receptor for advanced glycation end products (RAGE). Biochem Biophys Res Commun 434(2): 328–333. https://doi.org/10.1016/j.bbrc.2013.03.049
- Humphrey W, Dalke A, Schulten K (1996) VMD: Visual molecular dynamics. J Mol Graph 14: 28–33. https://doi.org/10.1016/0263-7855(96)00018-5
- Ansari NA, Moinuddin, Ali R (2011) Glycated lysine residues: a marker for non-enzymatic protein glycation in age-related diseases. Dis Markers 30(6): 317–324. https://doi.org/10.3233/DMA-2011-0791
- Abraham MJ, Murtola T, Schulz R, Páll S, Smith JC, Hess B, Lindahl E (2015) GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1–2: 19–25. https://doi.org/10.1016/j.softx.2015.06.001
- Trott O, Olson AJ (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization and multithreading. J Comput Chem 31(2): 455–461. https://doi.org/10.1002/jcc.21334
- Pierce BG, Wiehe K, Hwang H, Kim BH, Vreven T, Weng Z (2014) ZDOCK server: interactive docking prediction of protein-protein complexes and symmetric multimers. Bioinformatics 30(12): 1771–1773. https://doi.org/10.1093/bioinformatics/btu097
- Pierce BG, Hourai Y, Weng Z (2011) Accelerating protein docking in ZDOCK using an advanced 3D convolution library. PLoS One 6(9): e24657. https://doi.org/10.1371/journal.pone.0024657
- Sirois CM, Jin T, Miller AL, Bertheloot D, Nakamura H, Horvath GL, Mian A, Jiang J, Schrum J, Bossaller L, Pelka K, Garbi N, Brewah Y, Tian J, Chang C, Chowdhury PS, Sims GP, Kolbeck R, Coyle AJ, Humbles AA, Xiao TS, Latz E (2013) RAGE is a nucleic acid receptor that promotes inflammatory responses to DNA. J Exp Med 210(11): 2447–2463. https://doi.org/10.1084/jem.20120201
- Foloppe N, MacKerell AD Jr (2000) All-atom empirical force field for nucleic acids: I. Parameter optimization based on small molecule and condensed phase macromolecular target data. J Comput Chem 21: 86–104. https://doi.org/10.1002/(SICI)1096-987X(20000130)21:2%3C86::AID-JCC2%3E3.0.CO;2-G
- Jorgensen WL (1981) Quantum and statistical mechanical studies of liquids. 10. Transferable intermolecular potential functions for water, alcohols, and ethers. Application to liquid water. J Am Chem Soc 103(2): 335–340. https://doi.org/10.1021/ja00392a016
- Bussi G, Zykova-Timan T, Parrinello M (2009) Isothermal-isobaric molecular dynamics using stochastic velocity rescaling. J Chem Phys 130(7): 074101. https://doi.org/10.1063/1.3073889
- Parrinello M, Rahman A (1980) Crystal Structure and Pair Potentials: A Molecular-Dynamics Study. Phys Rev Lett 45: 1196–1199. https://doi.org/10.1103/PhysRevLett.45.1196
- Darden T, York D, Pedersen L (1993) Particle mesh Ewald: An N⋅log(N) method for Ewald sums in large systems. J Chem Phys 3: 10089–10092. https://doi.org/10.1063/1.464397
- Hess B, Bekker H, Berendsen HJC, Fraaije JGEM (1997) LINCS: A linear constraint solver for molecular simulations. J Comp Chem 18: 1463–1473.
- Sartore G, Bassani D, Ragazzi E, Traldi P, Lapolla A, Moro S (2021) In silico evaluation of the interaction between ACE2 and SARS-CoV-2 Spike protein in a hyperglycemic environment. Sci Rep 11(1): 22860. https://doi.org/10.1038/s41598-021-02297-w
- Penumutchu SR, Chou RH, Yu C (2014) Structural insights into calcium-bound S100P and the V domain of the RAGE complex. PLoS One 2014 9(8): e103947. https://doi.org/10.1371/journal.pone.0103947
- Sand KM, Bern M, Nilsen J, Noordzij HT, Sandlie I, Andersen JT (2015) Unraveling the Interaction between FcRn and Albumin: Opportunities for Design of Albumin-Based Therapeutics. Front Immunol 5: 682. https://doi.org/10.3389/fimmu.2014.00682
- Wu D, Gucwa M, Czub MP, Cooper DR, Shabalin IG, Fritzen R, Arya S, Schwarz-Linek U, Blindauer CA, Minor W, Stewart AJ (2023) Structural and biochemical characterisation of Co2+-binding sites on serum albumins and their interplay with fatty acids. Chem Sci 14(23): 6244–6258. https://doi.org/10.1039/d3sc01723k
- Schmidt AM, Hasu M, Popov D, Zhang JH, Chen J, Yan SD, Brett J, Cao R, Kuwabara K, Costache G, Simionescu N, Simionescu M, Stern D (1994) Receptor for advanced glycation end products (AGEs) has a central role in vessel wall interactions and gene activation in response to circulating AGE proteins. Proc Natl Acad Sci U S A 91(19): 8807–8811. https://doi.org/10.1073/pnas.91.19.8807
- Chen CY, Abell AM, Moon YS, Kim KH (2012) An advanced glycation end product (AGE)-receptor for AGEs (RAGE) axis restores adipogenic potential of senescent preadipocytes through modulation of p53 protein function. J Biol Chem 287(53): 44498–44507. https://doi.org/10.1074/jbc.M112.399790
- Belinskaia DA, Voronina PA, Shmurak VI, Jenkins RO, Goncharov NV (2021) Serum Albumin in Health and Disease: Esterase, Antioxidant, Transporting and Signaling Properties. Int J Mol Sci 22(19): 10318. https://doi.org/10.3390/ijms221910318
- Schmidt AM, Yan SD, Yan SF, Stern DM (2001) The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest 108(7): 949–955. https://doi.org/10.1172/JCI14002
- Nakamura K, Yamagishi S, Adachi H, Kurita-Nakamura Y, Matsui T, Yoshida T, Imaizumi T (2007) Serum levels of sRAGE, the soluble form of receptor for advanced glycation end products, are associated with inflammatory markers in patients with type 2 diabetes. Mol Med 13(3–4): 185–189.
- Steenbeke M, De Bruyne S, De Buyzere M, Lapauw B, Speeckaert R, Petrovic M, Delanghe JR, Speeckaert MM (2021) The role of soluble receptor for advanced glycation end-products (sRAGE) in the general population and patients with diabetes mellitus with a focus on renal function and overall outcome. Crit Rev Clin Lab Sci 58(2): 113–130. https://doi.org/10.1080/10408363.2020.1791045
- UniProt Consortium (2019) UniProt: a worldwide hub of protein knowledge. Nucleic Acids Res 47(D1): D506–D515. https://doi.org/10.1093/nar/gky1049
- Xue J, Rai V, Singer D, Chabierski S, Xie J, Reverdatto S, Burz DS, Schmidt AM, Hoffmann R, Shekhtman A (2011) Advanced glycation end product recognition by the receptor for AGEs. Structure 19(5): 722–732. https://doi.org/10.1016/j.str.2011.02.013
- Castagna R, Donini S, Colnago P, Serafini A, Parisini E, Bertarelli C (2019) Biohybrid Electrospun Membrane for the Filtration of Ketoprofen Drug from Water. ACS Omega 4(8): 13270–13278. https://doi.org/10.1021/acsomega.9b01442
- Ascenzi P, Fasano M (2010) Allostery in a monomeric protein: the case of human serum albumin. Biophys Chem 148(1-3): 16–22. https://doi.org/10.1016/j.bpc.2010.03.001
- Baraka-Vidot J, Guerin-Dubourg A, Bourdon E, Rondeau P (2012) Impaired drug-binding capacities of in vitro and in vivo glycated albumin. Biochimie 94(9): 1960–1967. https://doi.org/10.1016/j.biochi.2012.05.017
- Shaklai N, Garlick RL, Bunn HF (1984) Nonenzymatic glycosylation of human serum albumin alters its conformation and function. J Biol Chem 259(6): 3812–3817.
- Yamazaki E, Inagaki M, Kurita O, Inoue T (2005) Kinetics of fatty acid binding ability of glycated human serum albumin. J Biosci 30(4): 475–481. https://doi.org/10.1007/BF02703721
- Blache D, Bourdon E, Salloignon P, Lucchi G, Ducoroy P, Petit JM, Verges B, Lagrost L (2015) Glycated albumin with loss of fatty acid binding capacity contributes to enhanced arachidonate oxygenation and platelet hyperactivity: relevance in patients with type 2 diabetes. Diabetes 64(3): 960–972. https://doi.org/10.2337/db14-0879
- Henning C, Stübner C, Arabi SH, Reichenwallner J, Hinderberger D, Fiedler R, Girndt M, Di Sanzo S, Ori A, Glomb MA (2022) Glycation Alters the Fatty Acid Binding Capacity of Human Serum Albumin. J Agric Food Chem 70(9): 3033–3046. https://doi.org/10.1021/acs.jafc.1c07218
- Vreven T, Pierce BG, Hwang H, Weng Z (2013) Performance of ZDOCK in CAPRI rounds 20-26. Proteins 81(12): 2175–2182. https://doi.org/10.1002/prot.24432
- Vreven T, Pierce BG, Borrman TM, Weng Z (2017) Performance of ZDOCK and IRAD in CAP-RI rounds 28-34. Proteins 85(3): 408–416. https://doi.org/10.1002/prot.25186
- Vreven T, Vangaveti S, Borrman TM, Gaines JC, Weng Z (2020) Performance of ZDOCK and IRAD in CAPRI rounds 39-45. Proteins 88(8): 1050–1054. https://doi.org/10.1002/prot.25873
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