Oligomerization Interface of RAGE Receptor Revealed by MS-Monitored Hydrogen Deuterium Exchange

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Sitkiewicz, Ewa ^a   Tarnowski, Krzysztof ^a   Poznański, Jarosław ^a   Kulma, Magdalena ^a   Dadlez, Michal ^a,b  

^a INSTITUTE OF BIOCHEMISTRY AND BIOPHYSICS   (Poland)

^b UNIVERSITY OF WARSAW   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADVANCED GLYCATION END PRODUCT RECEPTOR; AMYLOID BETA PROTEIN; CELL PROTEIN; DIAPHANOUS 1 PROTEIN; DIMER; MITOGEN ACTIVATED PROTEIN KINASE; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN TIRAP; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CHEMICAL REACTION; CONTROLLED STUDY; DEUTERIUM HYDROGEN EXCHANGE; INTRACELLULAR SIGNALING; LIGAND BINDING; MASS SPECTROMETRY; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; NONHUMAN; OLIGOMERIZATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

DEUTERIUM; EXTRACELLULAR SPACE; HYDROGEN; KINETICS; LIGANDS; MASS SPECTROMETRY; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; RECEPTORS, IMMUNOLOGIC;

EID: 84885041031     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076353     Document Type: Article

References (60)

1. Schmidt AM, Vianna M, Gerlach M, Brett J, Ryan J, et al. (1992) Isolation and characterization of two binding proteins for advanced glycosylation end products from bovine lung which are present on the endothelial cell surface. J Biol Chem 2671498 7:: 14987-97 -14997. PubMed: 1321822.
2. Sturchler E, Galichet A, Weibel M, Leclerc E, Heizmann CW, (2008) Site-Specific Blockade of RAGE-Vd Prevents Amyloid-β Oligomer Neurotoxicity. J Neurosci 28: 5149-5158. doi:10.1523/JNEUROSCI.4878-07.2008. PubMed: 18480271.
3. Yan SD, Chen X, Fu J, Chen M, Zhu H, et al. (1996) RAGE and amyloid-[beta] peptide neurotoxicity in Alzheimer's disease. Nature 382: 685-691. doi:10.1038/382685a0. PubMed: 8751438.
4. Leclerc E, Fritz G, Vetter SW, Heizmann CW, (2009) Binding of S100 proteins to RAGE: An update. Biochim Biophys Acta Mol Cell Res 1793: 993-1007. doi:10.1016/j.bbamcr.2008.11.016. PubMed: 19121341.
5. Chavakis T, Bierhaus A, Al-Fakhri N, Schneider D, Witte S, et al. (2003) The Pattern Recognition Receptor (RAGE) Is a Counterreceptor for Leukocyte Integrins. J Exp Med 198: 1507-1515. doi:10.1084/jem.20030800. PubMed: 14623906.
6. Miyata T, Hori O, Zhang J, Yan SD, Ferran L, et al. (1996) The receptor for advanced glycation end products (RAGE) is a central mediator of the interaction of AGE-beta2microglobulin with human mononuclear phagocytes via an oxidant-sensitive pathway. Implications for the pathogenesis of dialysis-related amyloidosis. J Clin Invest 98: 1088-1094. doi:10.1172/JCI118889. PubMed: 8787669.
7. Yan SD, Zhu H, Zhu A, Golabek A, Du H, et al. (2000) Receptor-dependent cell stress and amyloid accumulation in systemic amyloidosis. Nat Med 6: 643-651. doi:10.1038/76216. PubMed: 10835680.
8. Sousa MM, Yan SD, Stern D, Saraiva MJ, (2000) Interaction of the Receptor for Advanced Glycation End Products (RAGE) with Transthyretin Triggers Nuclear Transcription Factor kB (NF-kB) Activation. Lab Invest 80: 1101-1110. doi:10.1038/labinvest.3780116. PubMed: 10908156.
9. Hori O, Brett J, Slattery T, Cao R, Zhang J, et al. (1995) The Receptor for Advanced Glycation End Products (RAGE) Is a Cellular Binding Site for Amphoterin. J Biol Chem 270: 25752-25761. doi:10.1074/jbc.270.43.25752.
10. Yamamoto Y, Harashima A, Saito H, Tsuneyama K, Munesue S, et al. (2011) Septic shock is associated with receptor for advanced glycation end products ligation of LPS. J Immunol 186: 3248-3257. doi:10.4049/jimmunol.1002253. PubMed: 21270403.
11. He M, Kubo H, Morimoto K, Fujino N, Suzuki T, et al. (2011) Receptor for advanced glycation end products binds to phosphatidylserine and assists in the clearance of apoptotic cells. EMBO Rep 12: 358-364. doi:10.1038/embor.2011.28. PubMed: 21399623.
12. Chen X, Walker DG, Schmidt AM, Arancio O, Lue L-F, et al. (2007) RAGE: a potential target for Abeta-mediated cellular perturbation in Alzheimer's disease. Curr Mol Med 7: 735-742. doi:10.2174/156652407783220741. PubMed: 18331231.
13. Deane R, Wu Z, Zlokovic BV, (2004) RAGE (Yin) Versus LRP (Yang) Balance Regulates Alzheimer Amyloid β-Peptide Clearance Through Transport Across the Blood-Brain Barrier. Stroke 35: 2628-2631. doi:10.1161/01.STR.0000143452.85382.d1. PubMed: 15459432.
14. Muhammad S, Barakat W, Stoyanov S, Murikinati S, Yang H, et al. (2008) The HMGB1 Receptor RAGE Mediates Ischemic Brain Damage. J Neurosci 28: 12023-12031. doi:10.1523/JNEUROSCI.2435-08.2008. PubMed: 19005067.
15. Qiu J, Nishimura M, Wang Y, Sims JR, Qiu S, et al. (2007) Early release of HMGB-1 from neurons after the onset of brain ischemia. J Cereb Blood Flow Metab 28: 927-938. PubMed: 18000511.
16. Bierhaus A, Nawroth PP, (2009) Multiple levels of regulation determine the role of the receptor for AGE (RAGE) as common soil in inflammation, immune responses and diabetes mellitus and its complications. Diabetologia 52: 2251-2263. doi:10.1007/s00125-009-1458-9. PubMed: 19636529.
17. Van Zoelen MAD, Achouiti A, van der Poll T, (2011) RAGE during infectious diseases. Front Biosci (Schol Ed) 3: 1119-1132. PubMed: 21622260.
18. Logsdon CD, Fuentes MK, Huang EH, Arumugam T, (2007) RAGE and RAGE ligands in cancer. Curr Mol Med 7: 777-789. doi:10.2174/156652407783220697. PubMed: 18331236.
19. Li J, Schmidt AM, (1997) Characterization and Functional Analysis of the Promoter of RAGE, the Receptor for Advanced Glycation End Products. J Biol Chem 272: 16498-16506. doi:10.1074/jbc.272.26.16498. PubMed: 9195959.
20. Tanaka N, Yonekura H, Yamagishi S, Fujimori H, Yamamoto Y, et al. (2000) The Receptor for Advanced Glycation End Products Is Induced by the Glycation Products Themselves and Tumor Necrosis Factor-α through Nuclear Factor-κB, and by 17β-Estradiol through Sp-1 in Human Vascular Endothelial Cells. J Biol Chem 275: 25781-25790. doi:10.1074/jbc.M001235200.
21. Ramasamy R, Yan SF, Schmidt AM, (2009) RAGE: therapeutic target and biomarker of the inflammatory response-the evidence mounts. J Leukoc Biol 86: 505-512. doi:10.1189/jlb.0409230. PubMed: 19477910.
22. Ramasamy R, Yan SF, Schmidt AM, (2011) Receptor for AGE (RAGE): signaling mechanisms in the pathogenesis of diabetes and its complications. Ann N Y Acad Sci 1243: 88-102. doi:10.1111/j.1749-6632.2011.06320.x. PubMed: 22211895.
23. Win MTT, Yamamoto Y, Munesue S, Saito H, Han D, et al. (2012) Regulation of RAGE for Attenuating Progression of Diabetic Vascular Complications. Experimental. Diabetes Res(2012): pp. 1-8. doi:10.1155/2012/894605.
24. Neeper M, Schmidt AM, Brett J, Yan SD, Wang F, et al. (1992) Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J Biol Chem 267: 14998-15004.
25. Koch M, Chitayat S, Dattilo BM, Schiefner A, Diez J, et al. (2010) Structural Basis for Ligand Recognition and Activation of RAGE. Structure 18: 1342-1352. doi:10.1016/j.str.2010.05.017. PubMed: 20947022.
26. Park H, Boyington JC, (2010) The 1.5 Å Crystal Structure of Human Receptor for Advanced Glycation Endproducts (RAGE) Ectodomains Reveals Unique Features Determining Ligand Binding. J Biol Chem 2854076 2:: 40762-70 -40770 doi:10.1074/jbc.M110.169276. PubMed: 20943659.
27. Matsumoto S, Yoshida T, Murata H, Harada S, Fujita N, et al. (2008) Solution Structure of the Variable-Type Domain of the Receptor for Advanced Glycation End Products: New Insight into AGE-RAGE Interaction†, ‡. Biochemistry 47: 12299-12311. doi:10.1021/bi800910v. PubMed: 19032093.
28. Xue J, Rai V, Singer D, Chabierski S, Xie J, et al. (2011) Advanced Glycation End Product Recognition by the Receptor for AGEs. Structure 19: 722-732. doi:10.1016/j.str.2011.02.013. PubMed: 21565706.
29. Dattilo BM, Fritz G, Leclerc E, Vander Kooi CW, Heizmann CW, et al. (2007) The Extracellular Region of the Receptor for Advanced Glycation End Products Is Composed of Two Independent Structural Units†. Biochemistry 46: 6957-6970. doi:10.1021/bi7003735. PubMed: 17508727.
30. Xie J, Reverdatto S, Frolov A, Hoffmann R, Burz DS, et al. (2008) Structural Basis for Pattern Recognition by the Receptor for Advanced Glycation End Products (RAGE). J Biol Chem 283: 27255-27269. doi:10.1074/jbc.M801622200. PubMed: 18667420.
31. Kupniewska-Kozak A, Gospodarska E, Dadlez M, (2010) Intertwined Structured and Unstructured Regions of exRAGE Identified by Monitoring Hydrogen-Deuterium Exchange. J Mol Biol 403: 52-65. doi:10.1016/j.jmb.2010.08.027. PubMed: 20732329.
32. Günter F, (2011) RAGE: a single receptor fits multiple ligands. Trends Biochem Sci 36: 625-632. doi:10.1016/j.tibs.2011.08.008. PubMed: 22019011.
33. Kislinger T, Fu C, Huber B, Qu W, Taguchi A, et al. (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: 31740-31749. doi:10.1074/jbc.274.44.31740. PubMed: 10531386.
34. Xie J, Burz DS, He W, Bronstein IB, Lednev I, et al. (2007) Hexameric calgranulin C (S100A12) binds to the receptor for advanced glycated end products (RAGE) using symmetric hydrophobic target-binding patches. J Biol Chem 282: 4218-4231. doi:10.1074/jbc.M608888200. PubMed: 17158877.
35. Ostendorp T, Leclerc E, Galichet A, Koch M, Demling N, et al. (2007) Structural and functional insights into RAGE activation by multimeric S100B. EMBO J 26: 3868-3878. doi:10.1038/sj.emboj.7601805. PubMed: 17660747.
36. Donato R, (2007) RAGE: a single receptor for several ligands and different cellular responses: the case of certain S100 proteins. Curr Mol Med 7: 711-724. doi:10.2174/156652407783220688. PubMed: 18331229.
37. Ishihara K, Tsutsumi K, Kawane S, Nakajima M, Kasaoka T, (2003) The receptor for advanced glycation end-products (RAGE) directly binds to ERK by a D-domain-like docking site. FEBS Lett 550: 107-113. doi:10.1016/S0014-5793(03)00846-9. PubMed: 12935895.
38. Hanford LE, Enghild JJ, Valnickova Z, Petersen SV, Schaefer LM, et al. (2004) Purification and characterization of mouse soluble receptor for advanced glycation end products (sRAGE). J Biol Chem 279: 50019-50024. doi:10.1074/jbc.M409782200. PubMed: 15381690.
39. Zong H, Madden A, Ward M, Mooney MH, Elliott CT, et al. (2010) Homodimerization Is Essential for the Receptor for Advanced Glycation End Products (RAGE)-mediated Signal Transduction. J Biol Chem 285: 23137-23146. doi:10.1074/jbc.M110.133827. PubMed: 20504772.
40. Rai V, Maldonado AY, Burz DS, Reverdatto S, Schmidt AM, et al. (2011) Signal transduction in RAGE: solution structure of C-terminal RAGE (ctRAGE) and its binding to mDia1. J Biol Chem 287: 5133-5144. doi:10.1074/jbc.M111.277731. PubMed: 22194616.
41. Hudson BI, Kalea AZ, del Mar Arriero M, Harja E, Boulanger E, et al. (2008) Interaction of the RAGE Cytoplasmic Domain with Diaphanous-1 Is Required for Ligand-stimulated Cellular Migration through Activation of Rac1 and Cdc42. J Biol Chem 283: 34457-34468. doi:10.1074/jbc.M801465200. PubMed: 18922799.
42. Sakaguchi M, Murata H, Yamamoto K, Ono T, Sakaguchi Y, et al. (2011) TIRAP, an adaptor protein for TLR2/4, transduces a signal from RAGE phosphorylated upon ligand binding. PLOS ONE 6: e23132. doi:10.1371/journal.pone.0023132. PubMed: 21829704.
43. Marcsisin SR, Engen JR, (2010) Hydrogen exchange mass spectrometry: what is it and what can it tell us? Anal Bioanal Chem 397: 967-972. doi:10.1007/s00216-010-3556-4. PubMed: 20195578.
44. Jacob JS, Cistola DP, Hsu F-F, Muzaffar S, Mueller DM, et al. (1996) Human Phagocytes Employ the Myeloperoxidase-Hydrogen Peroxide System to Synthesize Dityrosine, Trityrosine, Pulcherosine, and Isodityrosine by a Tyrosyl Radical-dependent Pathway. J Biol Chem 271: 19950-19956. doi:10.1074/jbc.271.33.19950. PubMed: 8702710.
45. Atwood CS, Perry G, Zeng H, Kato Y, Jones WD, et al. (2004) Copper mediates dityrosine cross-linking of Alzheimer's amyloid-beta. Biochemistry 43: 560-568. doi:10.1021/bi0358824. PubMed: 14717612.
46. Brady JD, Sadler IH, Fry SC, (1996) Di-isodityrosine, a novel tetrametric derivative of tyrosine in plant cell wall proteins: a new potential cross-link. Biochem J 315(1):: 323-327. PubMed: 8670125.
47. Brady JD, Sadler IH, Fry SC, (1998) Pulcherosine, an oxidatively coupled trimer of tyrosine in plant cell walls: its role in cross-link formation. Phytochemistry 47: 349-353. doi:10.1016/S0031-9422(97)00592-X. PubMed: 9433813.
48. Sárkány Z, Ikonen TP, Ferreira-da-Silva F, Saraiva MJ, Svergun D, et al. (2011) Solution Structure of the Soluble Receptor for Advanced Glycation End Products (sRAGE). J Biol Chem 286: 37525-37534. doi:10.1074/jbc.M111.223438. PubMed: 21865159.
49. Konermann L, Pan J, Liu Y-H, (2011) Hydrogen exchange mass spectrometry for studying protein structure and dynamics. Chem Soc Rev 40: 1224-1234. doi:10.1039/c0cs00113a. PubMed: 21173980.
50. Baldwin RL, (2007) Energetics of Protein Folding. J Mol Biol 371: 283-301. doi:10.1016/j.jmb.2007.05.078. PubMed: 17582437.
51. Heldin C-H, (1995) Dimerization of cell surface receptors in signal transduction. Cell 80: 213-223. doi:10.1016/0092-8674(95)90404-2. PubMed: 7834741.
52. Aeschbach R, Amadoò R, Neukom H, (1976) Formation of dityrosine cross-links in proteins by oxidation of tyrosine residues. Biochimica et Biophysica Acta (BBA)- Protein Structure 439: 292-301. doi:10.1016/0005-2795(76)90064-7.
53. Yan L-J, (2009) Analysis of Oxidative Modification of Proteins. In: Coligan JE, Dunn BM, Speicher DW, Wingfield PT, eds. Current Protocols in Protein Science. Hoboken, NJ, USA: John Wiley & Sons, Inc. Available: http://doi.wiley.com/10.1002/0471140864.ps1404s55. Accessed 24 May 2012.
54. Qin G, Rivkin A, Lapidot S, Hu X, Preis I, et al. (2011) Recombinant exon-encoded resilins for elastomeric biomaterials. Biomaterials 32: 9231-9243. doi:10.1016/j.biomaterials.2011.06.010. PubMed: 21963157.
55. Endrizzi BJ, Huang G, Kiser PF, Stewart RJ, (2006) Specific Covalent Immobilization of Proteins through Dityrosine Cross-Links. Langmuir 22: 11305-11310. doi:10.1021/la0618216. PubMed: 17154619.
56. Sevillano N, Girón MD, Salido M, Vargas AM, Vilches J, et al. (2009) Internalization of the Receptor for Advanced Glycation End Products (RAGE) is Required to Mediate Intracellular Responses. J Biochem 145: 21-30. doi:10.1093/jb/mvn137. PubMed: 18849572.
57. Kłoniecki M, Jabłonowska A, Poznański J, Langridge J, Hughes C, et al. (2011) Ion Mobility Separation Coupled with MS Detects Two Structural States of Alzheimer's Disease Aβ1-40 Peptide Oligomers. J Mol Biol 407: 110-124. doi:10.1016/j.jmb.2011.01.012. PubMed: 21237171.
58. Malencik DA, Sprouse JF, Swanson CA, Anderson SR, (1996) Dityrosine: Preparation, Isolation, and Analysis. Anal Biochem 242: 202-213. doi:10.1006/abio.1996.0454. PubMed: 8937563.
59. Krieger E, Joo K, Lee J, Lee J, Raman S, et al. (2009) Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: Four approaches that performed well in CASP8. Proteins 77: 114-122. doi:10.1002/prot.22570. PubMed: 19768677.
60. Murzin AG, Brenner SE, Hubbard T, Chothia C, (1995) SCOP: A structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 247: 536-540. doi:10.1016/S0022-2836(05)80134-2. PubMed: 7723011.