Ligands of RAGE-Proteins: Role in Intercellular Communication and Pathogenesis of Inflammation

Abstract

The review contains data on the diversity of endogenous ligands of RAGE receptors (receptor for advanced glycation end products) that play an important role in the signal transduction in (patho) physiological conditions. RAGE takes part in various physiological processes like cell growth and survival, apoptosis and regeneration. They serve as regulators of inflammatory reactions due to their ability to induce secretion of cytokines and chemokines. In addition, they facilitate elimination of apoptotic cells and mediate innate immune response. We discuss mechanisms of soluble RAGE production as well as the role of membrane and soluble forms of the receptor in cell signaling. Several endogenous ligands of RAGE are well-known: advanced glycation end products (AGE), amyloid-beta (Аβ), nuclear high mobility group box 1 proteins (HMGB1), and calcium-binding proteins S100A4, S100A8/A9, S100A12 и S100B. The review is focused on the mechanisms of the ligands production, their secretion from the cells of various origin, interaction with RAGE, and associated intracellular signal transduction pathways. Special attention is paid to the role of RAGE in pathogenesis of inflammation, particularly, in brain injury and neurodegeneration.

About the authors

Yuliya Aleksandrovna Uspenskaya

Krasnoyarsk State Medical University

Author for correspondence.
Email: uspenskaya.yulia@gmail.com
доктор биологических наук, научный сотрудник НИИ молекулярной медицины и патобиохимии Russian Federation

Yuliya Konstantinovna Komleva

Krasnoyarsk State Medical University

Email: yuliakomleva@mail.ru
кандидат медицинских наук, доцент кафедры биохимии с курсами медицинской, фармацевтической и токсикологической химии, научный сотрудник НИИ молекулярной медицины и патобиохимии Russian Federation

Elena Anatol'evna Pozhilenkova

Krasnoyarsk State Medical University

Email: Elena.a.pozhilenkova@gmail.com
кандидат биологических наук, доцент кафедры биохимии с курсами медицинской, фармацевтической и токсикологической химии, исполнительный директор НИИ молекулярной медицины и патобиохимии Russian Federation

Vladimir Valer'evic Salmin

Krasnoyarsk State Medical University

Email: vsalmin@gmail.com
доктор физико-математических наук, зав. кафедрой медицинской и биологической физики Russian Federation

Ol'ga Leonidovna Lopatina

Krasnoyarsk State Medical University

Email: ol.lopatina@gmail.com
кандидат биологических наук, доцент кафедры биохимии с курсами медицинской, фармацевтической и токсикологической химии, научный сотрудник НИИ молекулярной медицины и патобиохимии Russian Federation

Aleksandr Anatol'evich Fursov

Krasnoyarsk State Medical University

Email: fursov_alex@mail.ru
кандидат медицинских наук, ассистент кафедры анестезиологии и реаниматологии Института последипломного образования Russian Federation

Pavel Vyacheslavovich Lavrent'ev

Krasnoyarsk State Medical University

Email: lavran@inbox.ru
преподаватель кафедры медицинской и биологической физики, научный сотрудник НИИ молекулярной медицины и патобиохимии Russian Federation

Ol'ga Anatol'evna Belova

Krasnoyarsk State Medical University

Email: ulyabelova@mail.ru
ассистент кафедры травматологии, ортопедии и ВПХ с курсом ПО им. проф. Л.Л. Роднянского Russian Federation

Alla Borisovna Salmina

Krasnoyarsk State Medical University

Email: allasalmina@mail.ru
доктор медицинских наук, профессор, зав. кафедрой биохимии с курсами медицинской, фармацевтической и токсикологической химии, руководитель НИИ молекулярной медицины и патобиохимии Russian Federation

References

  1. Kierdorf K, Fritz G. RAGE regulation and signaling in inflammation and beyond. J Leukoc Biol. 2013;94(1):55–68. doi: 10.1189/jlb.1012519
  2. Borsi V, Cerofolini L, Fragai M, Luchinat C. NMR characterization of the C-terminal tail of full length RAGE in a membrane mimicking environment. J Biomol NMR. 2012;54(3):285–290. doi: 10.1007/s10858-012-9671-0
  3. Xie J, Mendez JD, Mendez-Valenzuela V, Aguilar-Hernandez MM. Cellular signalling of the receptor for advanced glycation end products (RAGE). Cell Signal. 2013;25(11):2185–2197. doi: 10.1016/j.cellsig.2013.06.013
  4. Koch M, Chitayat S, Dattilo BM, Schiefner A, Diez J, Chazin WJ, Fritz G. Structural basis for ligand recognition and activation of RAGE. Structure. 2010;18(10):1342–1352. doi: 10.1016/j.str.2010.05.017
  5. Stogsdill JA, Stogsdill MP, Porter JL, Hancock JM, Robinson AB, Reynolds PR. Embryonic overexpression of receptors for advanced glycation end products by alveolar epithelium induces an imbalance between proliferation and apoptosis. Am J Respir Cell Mol Biol. 2012;47(1):60–66. doi: 10.1165/rcmb.2011-0385OC
  6. Rojas A, Figueroa H, Morales E. Fueling inflammation at tumor microenvironment: the role of multiligand RAGE axis. Carcinogenesis. 2010;31:334–341. doi: 10.1093/carcin/bgp322
  7. Bierhaus A, Nawroth PP. 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. 2009;52(11):2251–2263. doi: 10.1007/s00125-009-1458-9
  8. Harja E, Bu DX, Hudson BI, Chang JS, Shen X, Hallam K, Kalea AZ, Lu Y, Rosario RH, Oruganti S, Nikolla Z, Belov D, Lalla E, Ramasamy R, Yan SF, Schmidt AM. Vascular and inflammatory stresses mediate atherosclerosis via RAGE and its ligands in apoE-/- mice. J Clin Invest. 2008;118(1):183–194. doi: 10.1172/JCI32703
  9. Fang F, Lue LF, Yan S, Xu H, Luddy JS, Chen D, Walker DG, Stern DM, Schmidt AM, Chen JX, Yan SS. RAGE dependent signaling in microglia contributes to neuroinflammation, Aβ accumulation, and impaired learning/memory in a mouse model of Alzheimer’s disease. FASEB J. 2010; 24 (4): 1043-1055. doi: 10.1096/fj.09-139634
  10. Akirav EM, Preston-Hurlburt P, Garyu J, Henegariu O, Clynes R, Schmidt AM, Herold KC. RAGE expression in human T cells: a link between environmental factors and adaptive immune responses. PLoS One. 2012;7:e34698. doi: 10.1371/journal.pone.0034698
  11. Sparvero LJ, Asafu-Adjei D, Kang R, Tang D, Amin N, Im J, Rutledge R, Lin B, Amoscato AA, Zeh HJ. Lotze MT. RAGE (Receptor for Advanced Glycation Endproducts), RAGE ligands, and their role in cancer and inflammation. J Transl Med. 2009;17:7–17. doi: 10.1186/1479-5876-7-17
  12. Chuah YK, Basir R, Talib H, Tie TH, Nordin N. Receptor for advanced glycation end products and itsiInvolvement in inflammatory diseases. Int J Inflam. 2013;2013:403460. doi: 10.1155/2013/403460
  13. Lam JK, Wang Y, Shiu SW, Wong Y, Betteridge DJ, Tan KC. Effect of insulin on the soluble receptor for advanced glycation end products (RAGE). Diabet Med. 2013;30(6):702–709. doi: 10.1111/dme.12166
  14. Piperi C, Goumenos A, Adamopoulos C, Papavassiliou AG. AGE/RAGE signalling regulation by miRNAs: associations with diabetic complications and therapeutic potential. Int J Biochem Cell Biol. 2015;60:197–201. doi: 10.1016/j.biocel.2015.01.009
  15. Moridi H, Karimi J, Sheikh N, Goodarzi MT, Saidijam M, Yadegarazari R, Khazaei M, Khodadadi I, Tavilani H, Piri H, Asadi S, Zarei S, Rezaei A. Resveratrol dependent down-regulation of receptor for advanced glycation end products and oxidative stress in kidney of rats with diabetes. Int J Endocrinol Metab. 2015;13(2):e23542. doi: 10.5812/ijem.23542
  16. Popa I, Ganea E, Petrescu SM. Expression and subcellular localization of RAGE in melanoma cells. Biochem Cell Biol. 2014;92(2):127–136. doi: 10.1139/bcb-2013-0064
  17. Wang L, Chen K, Liu K, Zhou Y, Zhang T, Wang B, Mi M. DHA inhibited AGEs-induced retinal microglia activation via suppression of the PPARγ/NFκB pathway and reduction of signal transducers in the AGEs/RAGE axis recruitment into lipid rafts. Neurochem Res. 2015;40(4):713–722. doi: 10.1007/s11064-015-1517-1
  18. Munesue S, Yamamoto Y, Urushihara R, Inomata K, Saito H, Motoyoshi S, Watanabe T, Yonekura H, Yamamoto H. Low molecular weight fractions of Japanese soy sauce act as a RAGE antagonist via inhibition of RAGE trafficking to lipid rafts. Food Funct. 2013;4(12):1835–1842. doi: 10.1039/c2fo30359k
  19. Zhang L, Bukulin M, Kojro E, Roth A, Metz VV, Fahrenholz F, Nawroth PP, Bierhaus A, Postina R. Receptor for advanced glycation end products is subjected to protein ectodomain shedding by metalloproteinases. J Biol Chem. 2008;283:35507–35516. doi: 10.1074/jbc.M806948200
  20. Wang Y, Wang H, Piper MG, McMaken S, Mo X, Opalek J, Schmidt AM, Marsh CB. sRAGE induces human monocyte survival and differentiation. J Immunol. 2010;185(3):1822–1835. doi: 10.4049/jimmunol.0903398
  21. Yan SF, Ramasamy R, Schmidt AM. Soluble RAGE: therapy and biomarker in unraveling the RAGE axis in chronic disease and aging. Biochem Pharmacol. 2010;79(10):1379–1386. doi: 10.1016/j.bcp.2010.01.013
  22. Galichet A, Weibel M, Heizmann CW. Calcium regulated intramembrane proteolysis of the RAGE receptor. Biochem Biophys Res Commun. 2008;370(1):1–5. doi: 10.1016/j.bbrc.2008.02.163
  23. Jabaudon M, Futier E, Roszyk L, Chalus E, Guerin R, Petit A, Mrozek S, Perbet S, Cavot-Constantin S, Chartier C, Sapin V, Bazin JE, Constantin JM. Soluble form of the receptor for advanced glycation end products is a marker of acute lung injury but not of severe sepsis in critically ill patients. Crit Care Med. 2011;39(3):480–488. doi: 10.1097/CCM.0b013e318206b3ca
  24. Ciccocioppo R, Imbesi V, Betti E, Boccaccio V, Kruzliak P, Cangemi GС, Maffe GC, Vanoli A, Merante S, De Amici M, Falcone C, Klersy C, Corazza GR. The circulating level of soluble receptor for advanced glycation end products displays different patterns in ulcerative colitis and Crohn’s disease: a cross sectional study. Dig Dis Sci. 2015;60(8):2327–2337. doi: 10.1007/s10620-015-3619-7. doi: 10.1007/s10620-015-3619-7
  25. Creagh-Brown BC, Quinlan GJ, Hector LR, Evans TW, Burke-Gaffney A. Association between preoperative plasma sRAGE levels and recovery from cardiac surgery. Mediators Inflamm. 2013;2013:496031. doi: 10.1155/2013/496031
  26. Kalea AZ, Schmidt AM, Hudson BI. Alternative splicing of RAGE: roles in biology and disease. Front Biosci (Landmark Ed). 2011;16:2756–2770. doi: 10.2741/3884
  27. Gopal P, Reynaert NL, Scheijen JL, Schalkwijk CG, Franssen FM, Wouters EF, Rutten EP. Association of plasma sRAGE, but not esRAGE with lung function impairment in COPD. Respir Res. 2014;15:24. doi: 10.1186/1465-9921-15-24
  28. Giannini C, D′Adamo E, de Georgis T, Chiavaroli V, Verrotti A, Chiarelli F, Mohn A. The possible role of esRAGE and sRAGE in the natural history of diabetic nephropathy in childhood. Pediatr Nephrol. 2012;27(2):269–275. doi: 10.1007/s00467-011-1988-5
  29. Zhu H, Ding Q. Lower expression level of two RAGE alternative splicing isoforms in Alzheimer’s disease. Neurosci Lett. 2015;597:66–70. doi: 10.1016/j.neulet.2015.04.032
  30. Liu XY, Li HL, Su JB, Ding FH, Zhao JJ, Chai F, Li YX, Cui SC, Sun FY, Wu ZY, Xu P, Chen XH. Regulation of RAGE splicing by hnRNP A1 and Tra2β-1 and its potential role in AD pathogenesis. J Neurochem. 2015;133(2):187–198. doi: 10.1111/jnc.13069
  31. Tam XH, Shiu SW, Leng L, Bucala R, Betteridge DJ, Tan KC. Enhanced expression of receptor for advanced glycation end-products is associated with low circulating soluble isoforms of the receptor in Type 2 diabetes. Clin Sci (Lond.). 2011;120(2):81–89. doi: 10.1042/CS20100256
  32. Huang M, Que Y, Shen X. Correlation of the plasma levels of soluble RAGE and endogenous secretory RAGE with oxidative stress in pre-diabetic patients. J Diabetes Complications. 2015;29(3):422–426. doi: 10.1016/j.jdiacomp.2014.12.007
  33. Moriya S, Yamazaki M. Murakami H, Maruyama K, Uchiyama S. Two soluble isoforms of receptors for advanced glycation end products (RAGE) in carotid atherosclerosis: the difference of soluble and endogenous secretory RAGE. J Stroke Cerebrovasc Dis. 2014;23(10):2540–2546. doi: 10.1016/j.jstrokecerebrovasdis.2014.05.037
  34. Moser B, Megerle A, Bekos C, Janik S, Szerafin T, Birner P, Schiefer AI, Mildner M, Lang I, Skoro-Sajer N, Sadushi-Kolici R, Taghavi S, Klepetko W, Ankersmit HJ. Local and systemic RAGE axis changes in pulmonary hypertension: CTEPH and iPAH. PLoS One. 2014;9 (9):e106440. doi: 10.1371/journal.pone.0106440
  35. Fritz G. RAGE: a single receptor fits multiple ligands. Trends Biochem Sci. 2011;36(12):625–632. doi: 10.1016/j.tibs.2011.08.008
  36. Xie J, Reverdatto S, Frolov A, Hoffmann R, Burz DS, Shekhtman A. Structural basis for pattern recognition by the receptor for advanced glycation end products (RAGE). J Biol Chem. 2008;283:27255–27269. doi: 10.1074/jbc.M801622200
  37. Sevillano N, Girόn MD, Salido M, Vergas AM, Vilches J, Salto R. Internalization of the receptor for advanced glycation end products (RAGE) is required to mediate intracellular responses. J Biochem. 2009;145(1):21–30. doi: 10.1093/jb/mvn137
  38. Ahmed N. Advanced glycation endproducts – role in pathology of diabetic complications. Diabetes Res Clin Pract. 2005;67(1):3–21. doi: 10.1016/j.diabres.2004.09.004
  39. Ulrich P, Cerami A. Protein glycation, diabetes, and aging. Recent Prog Horm Res. 2001;56:1–21. doi: 10.1210/rp.56.1.1
  40. Yamagishi S. Role of advanced glycation end products (AGEs) and receptor for AGEs (RAGE) in vascular damage in diabetes. Exp Gerontol. 2011;46(4):217–224. doi: 10.1016/j.exger.2010.11.007
  41. Ramasamy R, Yan SF, Schmidt AM. RAGE: therapeutic target and biomarker of the inflammatory response — the evidence mounts. J Leukoc Biol. 2009;86 (3):505–512. doi: 10.1189/jlb.0409230
  42. Sharaf H, Matou-Nasri S, Wang Q, Rabhan Z, Al-Eidi H, Al Abdulrahman A, Ahmed N. Advanced glycation endproducts increase proliferation, migration and invasion of the breast cancer cell line MDA-MB-231. Biochim Biophys Acta. 2015;1852(3):429–441. doi: 10.1016/j.bbadis.2014.12.009
  43. Yan SF, D’Agati V, Schmidt AM, Ramasamy R. Receptor for Advanced Glycation Endproducts (RAGE): a formidable force in the pathogenesis of the cardiovascular complications of diabetes & aging. Curr Mol Med. 2007;7(8):699–710. doi: 10.2174/156652407783220732
  44. Leclerc E, Fritz G, Vetter SW, Heizmann CW. Binding of S100 proteins to RAGE: an update. Biochim Biophys Acta. 2009;1793(6):993–1007. doi: 10.1016/j.bbamcr.2008.11.016
  45. Donato R, Cannon BR, Sorci G, Riuzzi F, Hsu K, Weber DJ, Geczy CL. Functions of S100 proteins. Curr Mol Med. 2013;13(1):24–57. doi: 10.2174/156652413804486214
  46. Sedaghat F, Notopoulos A. S100 protein family and its application in clinical practice. Hippokratia. 2008;12(4):198–204.
  47. Ohrt-Nissen S, Friis-Hansen L, Dahl B, Stensballe J, Romner B, Rasmussen LS. How does extracerebral trauma affect the clinical value of S100B measurements? Emerg Med J. 2011;28(11):941–944. doi: 10.1136/emj.2010.091363
  48. Narumi K, Miyakawa R, Ueda R, Hashimoto H, Yamamoto Y, Yoshida T, Aoki K. Proinflammatory Proteins S100A8/S100A9 activate NK cells via interaction with RAGE. J Immunol. 2015;194(11):5539–5548. doi: 10.4049/jimmunol.1402301
  49. Lam AGM, Koppal T, Akama KT, Guo L, Craft JM, Samy B, Schavocky JP, Watterson DM, Van Eldik LJ. Mechanism of glial activation by S100B: involvement of the transcription factor NFκB. Neurobiol Aging. 2001;22(5):765–772. doi: 10.1016/S0197-4580(01)00233-0
  50. Pizza O, Leggiero E, De Benedictis G, Pastore L, Salvatore F, Tufano R, De Robertis E. S100B induces the release of pro-inflammatory cytokines in alveolar type I-like cells. Int J Immunopathol Pharmacol. 2013;26(2):383–391.
  51. Turco F, Sarnelli G, Cirillo C, Palumbo I, De Giorgi F, D′Alessandro A, Cammarota M, Giuliano M, Cuomo R. Enteroglial derived S100B protein integrates bacteria induced Toll-like receptor signalling in human enteric glial cells. Gut. 2014;63(1):105–115. doi: 10.1136/gutjnl-2012-302090
  52. Chen H, Xu C, Jin Q, Liu Z. S100 protein family in human cancer. Am J Cancer Res. 2014;4(2):89–115.
  53. Ligthart S, Sedaghat S, Ikram MA, Hofman A, Franco OH, Dehghan A. EN-RAGE: a novel inflammatory marker for incident coronary heart disease. Arterioscler Thromb Vasc Biol. 2014;34(12):2695–2699. doi: 10.1161/ATVBAHA.114.304306
  54. Leclerc E, Sturchler E, Vetter SW. The S100B/RAGE axis in Alzheimer’s disease. Cardiovasc Psychiatry Neurol. 2010;2010:539581. doi: 10.1155/2010/539581
  55. Anderson PJ, Watts HR, Jen S, Gentleman SM, Moncaster JA, Walsh DT, Jen LS. Differential effects of interleukin-1beta and S100B on amyloid precursor protein in rat retinal neurons. Clin Ophthalmol. 2009;3:235–242. doi: 10.2147/OPTH.S2684
  56. Sathe K, Maetzler W, Lang JD, Mounsey RB, Fleckenstein C, Martin HL, Schulte C, Mustafa S, Synofzik M, Vukovic Z, Itohara S, Berg D, Teismann P. S100B is increased in Parkinson’s disease and ablation protects against MPTP induced toxicity through the RAGE and TNF-α pathway. Brain. 2012;135:3336–3347. doi: 10.1093/brain/aws250
  57. Cappellano G, Carecchio M, Fleetwood T, Magistrelli L, Cantello R, Dianzani U, Comi C. Immunity and inflammation in neurodegenerative diseases. Am J Neurodegener Dis. 2013;2(2):89–107.
  58. Gruden MA, Davudova TB, Malisauskas M, Zamotin VV, Sewell RD, Voskresenskaya NI, Kostanyan IA, Sherstnev VV, Morozova-Roche LA. Autoimmune responses to amyloid structures of Abeta(25-35) peptide and human lysozyme in the serum of patients with progressive Alzheimer’s disease. Dement Geriatr Cogn Disord. 2004;18(2):165–171. doi: 10.1159/000079197
  59. Lee CC, Avalos AM, Ploegh HL. Accessory molecules for Toll-like receptors and their function. Nat Rev Immunol. 2012;12(3):168–179. doi: 10.1038/nri3151
  60. Brencicova E, Diebold SS. Nucleic acids and endosomal pattern recognition: how to tell friend from foe? Front Cell Infect Microbiol. 2013;3:37. doi: 10.3389/fcimb.2013.00037
  61. Kannan K, Ortmann R. Inflammation promoting activity of HMGB-1 In type-II diabetes and as a marker of tissue injury. J Immunol. 2012;188:54.3.
  62. Tadié JM, Bae HB, Banerjee S, Zmijewski JW, Abraham E. Differential activation of RAGE by HMGB1 modulates neutrophil associated NADPH oxidase activity and bacterial killing. Am J Physiol Cell Physiol. 2012;302(1):C249–256. doi: 10.1152/ajpcell.00302.2011
  63. Musumeci D, Roviello GN, Montesarchio D. An overview on HMGB1 inhibitors as potential therapeutic agents in HMGB1 related pathologies. Pharmacol Ther. 2014;141(3):347–357. doi: 10.1016/j.pharmthera.2013.11.001
  64. Yang H, Antoine DJ, Andersson U, Tracey KJ. The many faces of HMGB1: molecular structure-functional activity in inflammation, apoptosis, and chemotaxis. J Leukoc Biol. 2013;93(6):865–873. doi: 10.1189/jlb.1212662
  65. Salmina AB, Komleva YK, Lopatina OL, Kuvacheva NV, Gorina YV, Panina YA, Uspenskaya YA, Petrova MM, Demko IV, Zamay AS, Malinovskaya NA. Astroglial control of neuroinflammation: TLR3-mediated dsRNA-sensing pathways are in the focus. Rev Neurosci. 2015;26(2):143–159. doi: 10.1515/revneuro-2014-0052
  66. LeBlanc PM, Doggett TA, Choi J, Hancock MA, Durocher Y, Frank F, Nagar B, Ferguson TA, Saleh M. An immunogenic peptide in the A-box of HMGB1 protein reverses apoptosis induced tolerance through RAGE receptor. J Biol Chem. 2014;289(11):7777–7786. doi: 10.1074/jbc.M113.541474
  67. LaFerla FM, Green KN, Oddo S. Intracellular amyloid-beta in Alzheimer’s disease. Nat Rev Neurosci. 2007;8(7):499–509. doi: 10.1038/nrn2168
  68. Sadigh-Eteghad S, Sabermarouf B, Majdi A, Talebi M, Farhoudi M, Mahmoudi J. Amyloid-beta: a crucial factor in Alzheimer’s disease. Med Princ Pract. 2015;24(1):1–10. doi: 10.1159/000369101
  69. Igbavboa U, Sun GY, Weisman GA, He Y, Wood WG. Amyloid beta-protein stimulates trafficking of cholesterol and caveolin-1 from the plasma membrane to the Golgi complex in mouse primary astrocytes. Neuroscience. 2009;162(2):328–338. doi: 10.1016/j.neuroscience.2009.04.049
  70. Soscia SJ, Kirby JE, Washicosky KJ, Tucker SM, Ingelsson M, Hyman B, Burton MA, Goldstein LE, Duong S, Tanzi RE, Moir RD. The Alzheimer’s disease-associated amyloid beta-protein is an antimicrobial peptide. PLoS One. 2010;5(3):e9505. doi: 10.1371/journal.pone.0009505
  71. Mondragón-Rodríguez S, Perry G, Zhu X, Boehm J. Amyloid Beta and tau proteins as therapeutic targets for Alzheimer’s disease treatment: rethinking the current strategy. Int J Alzheimers Dis. 2012;2012:630182. doi: 10.1155/2012/630182
  72. Kong W, Zhang J, Gao W, Liu Q, Zhou L, Chai X. β-amyloid protein up-regulates the expression of the receptor for advanced glycation end products by increasing ROS production. Nan Fang Yi Ke Da Xue Xue Bao. 2013;33(8):1132–1136.
  73. Askarova S, Yang X, Sheng W, Sun GY, Lee JC. Role of Aβ-receptor for advanced glycation endproducts interaction in oxidative stress and cytosolic phospholipase A₂ activation in astrocytes and cerebral endothelial cells. Neuroscience. 2011;199:375–385. doi: 10.1016/j.neuroscience.2011.09.038
  74. Rouhiainen A, Kuja-Panula J, Tumova S, Rauvala H. RAGE mediated cell signaling. Methods Mol Biol. 2013;963:239–263. doi: 10.1007/978-1-62703-230-8_15
  75. Gilbert BJ. The role of amyloid β in the pathogenesis of Alzheimer’s disease. J Clin Pathol. 2013;66(5):362–366. doi: 10.1136/jclinpath-2013-201515
  76. Schmidt AM, Sahagan B, Nelson RB, Selmer J, Rothlein R, Bell JM. The role of RAGE in amyloid beta peptide mediated pathology in Alzheimer’s disease. Curr Opin Investig Drugs. 2009;10(7):672–680.
  77. Park H, Boyington JC. The 1.5 А crystal structure of human receptor for advanced glycation endproducts (RAGE) ectodomains reveals unique features determining ligand binding. J Biol Chem. 2010;285(52):40762–40770. doi: 10.1074/jbc.M110.169276
  78. Tian J, Avalos AM, Mao SY, Chen B, Senthil K, Wu H, Parroche P, Drabic S, Golenbock D, Sirois C, Hua J, An LL, Audoly L, La Rosa G, Bierhaus A, Naworth P, Marshak-Rothstein A, Crow MK, Fitzgerald KA, Latz E, Kiener PA, Coyle A.J. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol. 2007;8(5):487–496. doi: 10.1038/ni1457
  79. 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. RAGE is a nucleic acid receptor that promotes inflammatory responses to DNA. J Exp Med. 2013;210(11):2447–2463. doi: 10.1084/jem.20120201
  80. Rai V, Touré F, Chitayat S, Pei R, Song F, Li Q, Zhang J, Rosario R, Ramasamy R, Chazin WJ, Schmidt AM. Lysophosphatidic acid targets vascular and oncogenic pathways via RAGE signaling. J Exp Med. 2012;209(13):2339–2350. doi: 10.1084/jem.20120873

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