The emerging role of the receptor for advanced glycation end products on innate immunity

International Reviews of Immunology

Volumn 33, Issue 1, 2014, Pages 67-80

  Rojas, Armando ^a   Pérez Castro, Ramón ^a   González, Ileana ^a   Delgado, Fernando ^a   Romero, Jacqueline ^a   Rojas, Israel ^a  

^a UNIVERSIDAD CATÓLICA DEL MAULE   (Chile)

Author keywords

Alarmins; Danger associated molecular patterns; Innate immunity; Pattern recognition receptors; Receptor for advanced glycation end products; Septic inflammation

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; LIGAND; PATTERN RECOGNITION RECEPTOR;

HUMAN; IMMUNOCOMPETENT CELL; INFECTION; INFLAMMATION; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TISSUE INJURY;

ANIMALS; HUMANS; IMMUNITY, INNATE; LIGANDS; RECEPTORS, IMMUNOLOGIC; RECEPTORS, PATTERN RECOGNITION; SIGNAL TRANSDUCTION;

EID: 84893043366     PISSN: 08830185     EISSN: 15635244     Source Type: Journal    
DOI: 10.3109/08830185.2013.849702     Document Type: Review

References (111)

1. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell 2010;140:805-820
2. Janeway CA Jr.The immune system evolved to discriminate infectious nonself from noninfectious self. Immunol Today 1992;13:11-16
3. Lemaitre B, Nicolas E, Michaut L, et al. The dorsoventral regulatory gene cassette Spaetzle/ Toll/Cactus control the potent antifungal response in Drosophila adults. Cell 1996;86:973-983
4. Tang D, Kang R, Coyne CB, et al. PAMPs and DAMPs: Signal 0s that spur autophagy and immunity. Immunol Rev 2012;249:158-175
5. Akira S,Uematsu S, Takeuchi O. Pathogen recognition and innate immunity. Cell 2006;124:783-801
6. Mogensen TH. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 2009;22:240-273
7. Kumagai Y, Akira S. Identification and functions of pattern-recognition receptors. J Allergy Clin Immunol 2010;125:985-992
8. Kenny EF, O'Neill LA. Signalling adaptors used by Toll-like receptors: An update. Cytokine 2008;43:342-349
9. Rojas A, Figueroa H,Morales E. Fueling inflammation at tumormicroenvironment: The role ofmultiligand/ RAGE axis. Carcinogenesis 2010;31:334-341
10. Sugaya K, Fukagawa T,Matsumoto K, et al. Three genes in the humanMHC class III region near the junction with the class II: Gene for receptor of advanced glycosylation end products, PBX2 homeobox gene and a notch homolog, human counterpart of mouse mammary tumor gene int-3. Genomics 1994;23:408-419
11. Schmidt AM, SternMD. Receptor for age (RAGE) is a genewithin themajor histocompatibility class III region: Implications for host response mechanisms in homeostasis and chronic disease. Front Biosci 2001;D1151-D1160
12. Neeper M, Schmidt AM, Brett J, et al. Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J Biol Chem 1992;267:14998-15004
13. Fritz G. RAGE: A single receptor fitsmultiple ligands. Trends Biochem Sci 2011;36:625-632
14. Raucci A,Cugusi S,Antonelli A, et al.Asoluble formof the receptor for advanced glycation endproducts (RAGE) is produced by proteolytic cleavage of the membrane-bound form by the sheddase a disintegrin and metalloprotease 10 (ADAM10). FASEB J 2008;22:3716-3727
15. Parkin E, Harris B. A disintegrin and metalloproteinase (ADAM)-mediated ectodomain shedding of ADAM10. J Neurochem 2008;108:1464-1479
16. Zhang L, Bukulin M, Kojro E, et al. Receptor for advanced glycation end products is subjected to protein ectodomain shedding by metalloproteinases. J Biol Chem 2008;283:35507-35516
17. Wang Y, Wang H, Piper MG, et al. sRAGE induces human monocyte survival and differentiation. J Immunol 2010;185:1822-1835
18. Xie J, Reverdatto S, Frolov A, et al. Structural basis for pattern recognition by the receptor for advanced glycation end products (RAGE). J Biol Chem 2008;283:27255-27269
19. Xie J, Burz DS, He W, et al. Hexameric calgranulin C (S100A12) binds to the receptor for advanced glycated end products (RAGE) using symmetric hydrophobic target-binding patches. J Biol Chem 2007;282:4218-4231
20. Zong A, Madden M, Ward M, et al. Homodimerization is essential for the receptor for advanced glycation end products (RAGE)-mediated signal transduction. J Biol Chem 2010;285:23137-23146
21. Kierdorf K, Fritz G. RAGE regulation and signaling in inflammation and beyond. J Leukoc Biol 2013;94:55-68
22. Jedrzejas MJ. Pneumococcal virulence factors: Structure and function microbiol Mol Biol Rev 2001;65:187-207
23. Kislinger T, Fu C, Huber B, et al. N(epsilon)-(carboxymethyl)lysine adducts of proteins are ligands for receptor for advanced glycation end products that activate cell signaling pathways andmodulate gene expression. J Biol Chem 1999;274:31740-31749
24. Rojas A,Morales MA. Advanced glycation and endothelial functions: A link towards vascular complications in diabetes. Life Sci 2004;76:715-730
25. Rashid G, Luzon AA, Korzets Z, et al. The effect of advanced glycation end-products and aminoguanidine on TNF-alpha production by rat peritoneal macrophages. Perit Dial Int 2001;21:122-129
26. Cohen MP, Shea E, Chen S, Shearman CW. Glycated albumin increases oxidative stress, activates NF-kappa B and extracellular signal-regulated kinase (ERK), and stimulates ERK-dependent transforming growth factor-beta 1 production in macrophage RAW cells. J Lab Clin Med 2003;141:242-249
27. Alikhani Z, Alikhani M, Boyd CM, et al. Advanced glycation end products enhance expression of pro-apoptotic genes and stimulate fibroblast apoptosis through cytoplasmic and mitochondrial pathways. J Biol Chem 2005;280:12087-12095
28. Schmidt AM, Yan S, Brett J, et al. Regulation of human mononuclear phagocyte migration by cell surface-binding proteins for advanced glycation end products. J Clin Invest 1993;91:2155-2168
29. Graves DT, Kayal RA. Diabetic complications and dysregulated innate immunity. Front Biosci 2008;13:1227-1239
30. Schmidt AM, Yan SD, Wautier JL, Stern D. Activation of receptor for advanced glycation end products: A mechanism for chronic vascular dysfunction in diabetic vasculopathy and atherosclerosis. Circ Res 1999;84:489-497
31. Schmidt AM, Hori O, Cao R, et al. RAGE: A novel cellular receptor for advanced glycation end products. Diabetes 1996;45(Suppl 3):S77-S80
32. BhattacharyyaN, Pal A, Patra S, et al. Activation ofmacrophages and lymphocytes bymethylglyoxal against tumor cells in the host. Int Immunopharmacol 2008;8:1503-1512
33. Rojas A, Caveda L, Romay C, et al. Effect of advanced glycosylation end products on the induction of nitric oxide synthase inmurinemacrophages. Biochem Biophys Res Commun 1996;225:358-362
34. Verdier Y, Zaŕandi M, Penkeq B. Amyloid beta-peptide interactions with neuronal and glial cell plasma membrane: Binding sites and implications for Alzheimer's disease. J Pept Sci 2004;10:229-248
35. Salminen A, Ojala J, Kauppinen A, et al. Inflammation in Alzheimer's disease: Amyloid-beta oligomers trigger innate immunity defence via pattern recognition receptors. Prog Neurobiol 2009;87:181-194
36. Giri R, Shen Y, Stins M, et al. Beta-amyloid-induced migration of monocytes across human brain endothelial cells involves RAGE and PECAM-1. AmJ Physiol Cell Physiol 2000;279:C1772-C1781
37. Turrin NP, Rivest S.Molecular and cellular immune mediators of neuroprotection.Mol Neurobiol 2006;34:221-242
38. Chavakis T, Bierhaus A, Al-Fakhri N, et al. The pattern recognition receptor (RAGE) is a counterreceptor for leukocyte integrins: A novel pathway for inflammatory cell recruitment. J Exp Med 2003;198:1507-1515
39. Orlova VV, Choi EY, Xie C, et al. A novel pathway of HMGB1-mediated inflammatory cell recruitment that requiresMac-1-integrin. EMBO J 2007;26:1129-1139
40. Frommhold D, Kamphues A, Hepper I, et al. RAGE and ICAM-1 cooperate in mediating leukocyte recruitment during acute inflammation in vivo. Blood 2010;116:841-849
41. Foell D, Wittkowski H, Vogl T, Roth J. S100 proteins expressed in phagocytes: A novel group of damage-associated molecular pattern molecules. J Leukoc Biol 2007;81:28-37
42. Wolf R, Mirmohammadsadegh A, Walz A, et al. Molecular cloning and characterization of alternatively spliced mRNA isoforms from psoriatic skin encoding a novel member of the S100 family. FASEB J 2003;17:1969-1971
43. Wolf R, Mascia F, Dharamsi A, et al. Gene from a psoriasis susceptibility locus primes the skin for inflammation. Sci TranslMed 2010;2:61ra90
44. Hessian PA, Edgeworth J, Hogg N. MRP-8 and MRP-14, two abundant Ca(2+)-binding proteins of neutrophils and monocytes. J Leukoc Biol 1993;53:197-204
45. Damo SM, Kehl-Fie TE, Sugitani N, et al. Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens. Proc Natl Acad Sci USA 2013;110:3841-3846
46. Andersson U, Tracey KJ. HMGB1 is a therapeutic target for sterile inflammation and infection. Ann Rev Immunol 2011;29:139-162
47. Ito I, Fukazawa J, Yoshida M. Post-translational methylation of highmobility group box 1 (HMGB1)causes its cytoplasmic localization in neutrophils. The J Biol Chem 2007;282:16336-16344
48. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002;418:191-195
49. Kazama H, Ricci JE, Herndon JM, et al. Induction of immunological tolerance by apoptotic cells requires caspase-dependent oxidation of high-mobility group box-1 protein. Immunity 2008;29:21-32
50. Yamada Y, Fuji T, Ishijima R, et al.The release of highmobility group box 1 in apoptosis is triggered by nucleosomal DNA fragmentation. Arch Biochem Biophys 2011;506:188-193
51. Tang D, Kang R, Cheh CW, et al. HMGB1 release and redox regulates autophagy and apoptosis in cancer cells. Oncogene 2010;29:5299-5310
52. Rovere-Querini P, Capobianco A, Scaffidi P, et al. HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep 2004;5:825-830
53. Messmer D, Yang H, Telusma G, et al. High mobility group box protein 1: An endogenous signal for dendritic cellmaturation and Th1 polarization. J Immunol 2004;173:307-313
54. Yang D, Chen Q, Yang H, et al. High mobility group box-1 protein induces the migration and activation of human dendritic cells and acts as an alarmin. J Leukoc Biol 2007;81:59-66
55. Degryse B, Bonaldi T, Scaffidi P, et al.The highmobility group (HMG) boxes of the nuclear protein HMG1 induce chemotaxis and cytoskeleton reorganization in rat smooth muscle cells. J Cell Biol 2001;152:1197-1206
56. Park JS, Arcaroli J, Yum HK, et al. Activation of gene expression in human neutrophils by highmobility group box 1 protein. AmJ Physiol Cell Physiol 2003;284:C870-C879
57. Palumbo R, Sampaolesi M, De Marchis F, et al. Extracellular HMGB1, a signal of tissue damage, inducesmesoangioblastmigration and proliferation. J Cell Biol 2004;164:441-449
58. Messmer D, Yang H, Telusma G, et al. High mobility group box protein 1: An endogenous signal for dendritic cellmaturation and Th1 polarization. J Immunol 2004;173:307-313
59. TelusmaG,Datta S,Mihajlov I, et al.Dendritic cell activating peptides induce distinct cytokine profiles. Int Immunol 2006;18:1563-1573
60. Rouhiainen A, Kuja-Panula J, Wilkman E, et al. Regulation of monocyte migration by amphoterin (HMGB1) Blood 2004;104:1174-1182
61. Tsung A, Zheng N, Jeyabalan G, et al. Increasing numbers of hepatic dendritic cells promote HMGB1-mediated ischemia-reperfusion injury. J Leukoc Biol 2007;81:119-128
62. Urbonaviciute V, Furnrohr BG, Meister S, et al. Induction of inflammatory and immune responses by HMGB1-nucleosome complexes: Implications for the pathogenesis of SLE. J Exp Med 2008;205:3007-3018
63. Ivanov S, Dragoi AM, Wang X, et al. A novel role for HMGB1 in TLR9-mediated inflammatory responses to CpG-DNA. Blood 2007;110:1970-1981
64. Tian J, Avalos AM,Mao SY, et al. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 2007;8:487-496
65. Ciucci A, Gabriele I, Percario ZA, et al. HMGB1 and cord blood: Its role as immuno-adjuvant factor in innate immunity. PLoS One 2011;6(8):e23766
66. Tal MC, Iwasaki A. Autophagy and innate recognition systems. Curr Top Microbiol Immunol 2009;335:107-121
67. FaureM, Lafont F. Pathogen-induced autophagy signaling in innateimmunity. J InnateImmunMay 3, 2013. [Epub ahead of print]
68. Kang R, Tang D, Schapiro NE, et al. The receptor for advanced glycation end products (RAGE) sustains autophagy and limits apoptosis, promoting pancreatic tumor cell survival. Cell Death Differ 2010;17:666-676
69. Kang R, Livesey KM, Zeh HJ 3rd, et al. Metabolic regulation by HMGB1-mediated autophagy and mitophagy. Autophagy 2011;7:1256-1258
70. He Q, You H, Li XM, et al. HMGB1 promotes the synthesis of pro-IL-1β and pro-IL-18 by activation of p38 MAPK and NF-κB through receptors for advanced glycation end-products in macrophages. Asian Pac J Cancer Prev 2012;13:1365-1370
71. Yamamoto Y, Harashima A, Saito H, et al. Septic shock is associated with receptor for advanced glycation end products ligation of LPS. J Immunol 2011;186:3248-3257
72. Ramsgaard L, Englert JM,Manni ML, et al. Lack of the receptor for advanced glycation end-products attenuates E. coli pneumonia in mice. PLoS One 2011;6:e20132
73. Williams JH, Ireland HE. J Sensing danger-Hsp72 and HMGB1 as candidate signals. J Leuk Biol 2008;83:489-492
74. Chiodoni C, Colombo MP, Sangaletti S.Matricellular proteins: From homeostasis to inflammation, cancer, and metastasis. CancerMetast Rev 2010;29:295-307
75. Ricklin D, Hajishengallis G, Yang K, Lambris JD. Complement: A key system for immune surveillance and homeostasis. Nat Immunol 2010;11:785-797
76. Barber GN. Cytoplasmic DNA innate immune pathways. Immunol Rev 2011;243:99-108
77. Ruan BH, Li X,Winkler AR, et al. J Immunol 2010;185(7):4213-4222
78. Park H, Adsit FG, Boyington JC.The1.5̊A crystal structure of human receptor for advanced glycation endproducts (RAGE) ectodomains reveals unique features determining ligand binding. J BiolChem 2010;285(52):40762-40770
79. Ma W, Rai V, Hudson BI, et al. RAGE binds C1q and enhances C1q-mediated phagocytosis. Cell Immunol 2012;274:72-82
80. Devitt A,Marshall LJ.The innate immune system and the clearance of apoptotic cells. J Leukoc Biol 2011;90:447-457
81. He M, Kubo H, Morimoto K, et al. Receptor for advanced glycation end products binds to phosphatidylserine and assists in the clearance of apoptotic cells. EMBO Rep 2011;12:358-364
82. Friggeri A, Banerjee S, Biswas S, et al. Participation of the receptor for advanced glycation end products in efferocytosis. J Immunol 2011;186:6191-6198
83. Rojas A, Gonzalez I, Rodriguez B, et al. Evidence of involvement of the receptor for advanced glycation end-products (RAGE) in the adhesion of Helicobacter pylori to gastric epithelial cells. Microb Infec 2011;13:818-823
84. Arce-Mendoza A, Rodriguez-de Ita J, Salinas-Carmona MC, Rosas-Taraco AG. Expression of CD64, CD206, and RAGE in adherent cells of diabetic patients infected withMycobacterium tuberculosis. ArchMed Res 2008;39:306-311
85. Tian J, Huang K, Krishnan S, et al. RAGE inhibits RSV syncytia formation by interfering with Fprotein function. J Gen Virol April 4, 2013. [Epub ahead of print].
86. Sorci G, Giovannini G, Riuzzi F, et al. The danger signal S100B integrates pathogen- and dangersensing pathways to restrain inflammation. PLoS Pathog 2011 7:e1001315
87. van Zoelen MA, Schouten M, de Vos AF, et al. The receptor for advanced glycation end products impairs host defense in pneumococcal pneumonia. J Immunol 2009;182:4349-4356
88. Amir J,WaiteM, Tobler J, et al.Therole of hyperglycemia inmechanisms of exacerbated inflammatory responses within the oral cavity. Cell Immunol 2011;272:45-52
89. Rojas A, Delgado-Ĺopez F, Gonźalez I, et al.The receptor for advanced glycation end-products: A complex signaling scenario for a promiscuous receptor. Cell Signal 2013;25:609-614
90. Nogueira-Machado JA, Volpe CM, Veloso CA, Chaves MM. HMGB1, TLR and RAGE: A functional tripod that leads to diabetic inflammation. Expert OpinTher Targets 2011;15:1023-1035
91. Tian J, Avalos AM,Mao SY, et al. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 2007;8:487-496
92. Sakaguchi M, Murata H, Yamamoto K, et al. TIRAP, an adaptor protein for TLR2/4, transduces a signal from RAGE phosphorylated upon ligand binding. PLoS One 2011;6:e23132
93. Chakraborty R, Bhatt KH, Sodhi A. High mobility group box 1 protein synergizes with lipopolysaccharide and peptidoglycan for nitric oxide production in mouse peritoneal macrophages in vitro. Mol Immunol 2013;54:48-57
94. Ghavami S,Rashedi I,DattiloBM, et al. S100A8/A9 at lowconcentration promotes tumor cell growth via RAGE ligation and MAP kinase-dependent pathway. J Leukoc Biol 2008;83:1484-1492
95. Vogl T, Tenbrock K, Ludwig S, et al.Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. NatMed 2007;13:1042-1049
96. Yeh C, Sturgis L, Haidacher J, et al. Requirement for p38 and p44/42 mitogen-activated protein kinases in RAGE-mediated nuclear factor-kB transcriptional activation and cytokine secretion. Diabetes 2001;50:1495-1504
97. Huttunen H, Kuja-Panula J, Rauvala H. RAGE signaling induces CREB-dependent chromogranin expression during neuronal differentiation. J Biol Chem 2002;277:38635-38646
98. Huang JS, Guh JY, Chen HC, et al. Role of receptor for advanced glycation end-product (RAGE)and the JAK/STAT-signaling pathway in AGE-induced collagen production in NRK-49F cells. J Cell Biochem 2001;81:102-113
99. Yan SF, Ramasamy R, Schmidt AM. Soluble RAGE: Therapy and biomarker in unraveling the RAGE axis in chronic disease and aging. Biochem Pharmacol 2010;79:1379-1386
100. Bierhaus A, Schiekofer S, Schwaninger M, et al. Diabetes-associated sustained activation of the transcription factor nuclear factor-kappaB. Diabetes 2001;50:2792-2808
101. Ogier-Denis E,Mkaddem SB, Vandewalle A. NOX enzymes and Toll-like receptor signaling. Semin Immunopathol 2008;30:291-300
102. Guo ZJ, Niu HX, Hou FF, et al. Advanced oxidation protein products activate vascular endothelial cells via a RAGE-mediated signaling pathway. Antioxid Redox Signal 2008;10:1699-1712
103. Sangle GV, Zhao R, Mizuno TM, Shen GX. Involvement of RAGE, NADPH oxidase, and Ras/Raf- 1 pathway in glycated LDL-induced expression of heat shock factor-1 and plasminogen activator inhibitor-1 in vascular endothelial cells. Endocrinology 2010;151:4455-4466
104. Robinson JM, Ohira T, Badwey JA. Regulation of the NADPH-oxidase complex of phagocytic leukocytes.Recent insights from structural biology, molecular genetics, andmicroscopy.Histochem Cell Biol 2004;122:293-304
105. Omori K, Ohira T, Uchida Y, et al. Priming of neutrophil oxidative burst in diabetes requires preassembly of the NADPH oxidase. J Leukoc Biol 2008;84:292-301
106. Ghoreschi K, Laurence A, O'Shea JJ. Janus kinases in immune cell signaling. Immunol Rev 2009;228:273-287
107. Kim YK, Park HK, JYoon YS, et al. Advanced glycation end product (AGE)-induced proliferation of HEL cells via receptor for AGE-related signal pathways. Int J Oncol 2008;33:493-501
108. Yammani RR, Long D, Loeser RF. Interleukin-7 stimulates secretion of S100A4 by activating the JAK/STAT signaling pathway in human articular chondrocytes. Arth Rheum 2009;60:792-800
109. McGettrick AF,O'Neill LA. Localisation and trafficking of Toll-like receptors: An important mode of regulation. Curr Opin Immunol 2010;22:20-27
110. Sevillano N, Giŕon MD, Salido M, et al. Internalization of the receptor for advanced glycation end products (RAGE) is required to mediate intracellular responses. J Biochem 2009;145:21-30
111. Akirav EM, Preston-Hurlburt P, Garyu J, et al. RAGE expression in human T cells: A link between environmental factors and adaptive immune responses. PLoS One 2012;7(4):e34698