RAGE in tissue homeostasis, repair and regeneration

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 1, 2013, Pages 101-109

  Sorci, Guglielmo ^a   Riuzzi, Francesca ^a   Giambanco, Ileana ^a   Donato, Rosario ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

Author keywords

Cancer; HMGB1; Inflammation; RAGE; S100 protein; Tissue regeneration repair

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCT RECEPTOR; AMYLOID BETA PROTEIN; HIGH MOBILITY GROUP B1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN CDC42; PROTEIN KINASE B; PROTEIN S 100; RAC1 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR 2;

AUTOPHAGY; CELL MIGRATION; CELL PROLIFERATION; HOMEOSTASIS; HUMAN; INFLAMMATION; KERATINOCYTE; LIGAND BINDING; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; REVIEW; SIGNAL TRANSDUCTION; TISSUE REGENERATION; TISSUE REPAIR;

ANIMALS; GLYCOSYLATION END PRODUCTS, ADVANCED; HOMEOSTASIS; HUMANS; MODELS, BIOLOGICAL; RECEPTORS, IMMUNOLOGIC; REGENERATION; SIGNAL TRANSDUCTION; WOUND HEALING;

EID: 84868530905     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.10.021     Document Type: Review

References (125)

1. Schmidt A.M., Yan S.D., Yan S.F., Stern D.M. The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J. Clin. Invest. 2001, 108:949-955.
2. Bierhaus A., Humpert P.M., Morcos M., Wendt T., Chavakis T., Arnold B., Stern D.M., Nawroth P.P. Understanding RAGE, the receptor for advanced glycation end products. J. Mol. Med. 2005, 83:876-886.
3. Donato R. RAGE: a single receptor for several ligands and different cellular responses. The case of certain S100 proteins. Curr. Mol. Med. 2007, 7:711-724.
4. Gebhardt C., Riehl A., Durchdewald M., Németh J., Fürstenberger G., Müller-Decker K., Enk A., Arnold B., Bierhaus A., Nawroth P.P., Hess J., Angel P. RAGE signaling sustains inflammation and promotes tumor development. J. Exp. Med. 2008, 205:275-285.
5. Yan S.F., Ramasamy R., Schmidt A.M. The RAGE axis: a fundamental mechanism signaling danger to the vulnerable vasculature. Circ. Res. 2010, 106:842-853. (Erratum in: Circ. Res. 106 (2010) e6).
6. Sims G.P., Rowe D.C., Rietdijk S.T., Herbst R., Coyle A.J. HMGB1 and RAGE in inflammation and cancer. Annu. Rev. Immunol. 2010, 28:367-388.
7. D'Agati V., Schmidt A.M. RAGE and the pathogenesis of chronic kidney disease. Nat. Rev. Nephrol. 2010, 6:352-360.
8. Rojas A., Figueroa H., Morales E. Fueling inflammation at tumor microenvironment: the role of multiligand/RAGE axis. Carcinogenesis 2010, 31:334-441.
9. Han S.H., Kim Y.H., Mook-Jung I. RAGE: the beneficial and deleterious effects by diverse mechanisms of actions. Mol. Cells 2011, 31:91-97.
10. Cho H.J., Son S.M., Jin S.M., Hong H.S., Shin D.H., Kim S.J., Huh K., Mook-Jung I. RAGE regulates BACE1 and Aβ generation via NFAT1 activation in Alzheimer's disease animal model. FASEB J. 2009, 23:2639-2649.
11. Riuzzi F., Sorci G., Sagheddu R., Donato R. HMGB1-RAGE regulates muscle satellite cell homeostasis via p38-MAPK- and myogenin-dependent repression of Pax7 transcription. J. Cell Sci. 2012, 125:1440-1454.
12. Sakatani S., Yamada K., Homma C., Munesue S., Yamamoto Y., Yamamoto H., Hirase H. Deletion of RAGE causes hyperactivity and increased sensitivity to auditory stimuli in mice. PLoS One 2009, 4:e8309.
13. Huttunen H.J., Fages C., Rauvala H. Receptor for advanced glycation end products (RAGE)-mediated neurite outgrowth and activation of NF-κB require the cytoplasmic domain of the receptor but different downstream signaling pathways. J. Biol. Chem. 1999, 274:19919-19924.
14. Taguchi A., Blood D.C., del Toro G., Canet A., Lee D.C., Qu W., Tanji N., Lu Y., Lalla E., Fu C., Hofmann M.A., Kislinger T., Ingram M., Lu A., Tanaka H., Hori O., Ogawa S., Stern D.M., Schmidt A.M. Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases. Nature 2000, 405:354-360.
15. Xue J., Rai V., Singer D., Chabierski S., Xie J., Reverdatto S., Burz D.S., Schmidt A.M., Hoffmann R., Shekhtman A. Advanced glycation end product recognition by the receptor for AGEs. Structure 2011, 19:722-732.
16. Fages C., Nolo R., Huttunen H.J., Eskelinen E., Rauvala H. Regulation of cell migration by amphoterin. J. Cell Sci. 2000, 113:611-620.
17. Yan S.S., Wu Z.Y., Zhang H.P., Furtado G., Chen X., Yan S.F., Schmidt A.M., Brown C., Stern A., LaFaille J., Chess L., Stern D.M., Jiang H. RAGE and amyloid-β peptide neurotoxicity in Alzheimer's disease. Nature 1996, 382:685-691.
18. Hofmann M.A., Drury S., Fu C., Qu W., Taguchi A., Lu Y., Avila C., Kambham N., Bierhaus A., Nawroth P., Neurath M.F., Slattery T., Beach D., McClary J., Nagashima M., Morser J., Stern D., Schmidt A.M. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell 1999, 97:889-901.
19. Leclerc E., Fritz G., Vetter S.W., Heizmann C.W. Binding of S100 proteins to RAGE: an update. Biochim. Biophys. Acta 2009, 1793:993-1007.
20. Yamamoto Y., Kato I., Doi T., Yonekura H., Ohashi S., Takeuchi M., Watanabe T., Yamagishi S., Sakurai S., Takasawa S., Okamoto H., Yamamoto H. Development and prevention of advanced diabetic nephropathy in RAGE overexpressing mice. J. Clin. Invest. 2001, 108:261-268.
21. Penfold S.A., Coughlan M.T., Patel S.K., Srivastava P.M., Sourris K.C., Steer D., Webster D.E., Thomas M.C., MacIsaac R.J., Jerums G., Burrell L.M., Cooper M.E., Forbes J.M. Circulating high-molecular-weight RAGE ligands activate pathways implicated in the development of diabetic nephropathy. Kidney Int. 2010, 78:287-295.
22. Riehl A., Németh J., Angel P., Hess J. The receptor RAGE: bridging inflammation and cancer. Cell Commun. Signal. 2009, 7:12.
23. Hock R., Furusawa T., Ueda T., Bustin M. HMG chromosomal proteins in development and disease. Trends Cell Biol. 2007, 17:72-79.
24. Bianchi M.E., Manfredi A.A. High-mobility group box 1 (HMGB1) protein at the crossroads between innate and adaptive immunity. Immunol. Rev. 2007, 220:35-46.
25. Rauvala H., Rouhiainen A. RAGE as a receptor of HMGB1 (Amphoterin): roles in health and disease. Curr. Mol. Med. 2007, 7:725-734.
26. Selkoe D.J. The molecular pathology of Alzheimer's disease. Neuron 1991, 6:487-498.
27. Donato R. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int. J. Biochem. Cell Biol. 2001, 33:637-668.
28. Heizmann C.W. The multifunctional S100 protein family. Methods Mol. Biol. 2002, 172:69-80.
29. Donato R., Cannon B.R., Sorci G., Riuzzi F., Hsu K., Weber D.J., Geczy C.L. Functions of S100 proteins. Curr. Mol. Med. Jul 23 2012, (Epub ahead of print - 20120723-11).
30. Xie J., Reverdatto S., Frolov A., Hoffmann R., Burz D.S., Shekhtman A. Structural basis for pattern recognition by the receptor for advanced glycation end products (RAGE). J. Biol. Chem. 2008, 283:27255-27269.
31. Leclerc E., Fritz G., Weibel M., Heizmann C.W., Galichet A. S100B and S100A6 differentially modulate cell survival by interacting with distinct RAGE (receptor for advanced glycation end products) immunoglobulin domains. J. Biol. Chem. 2007, 282:31317-31331.
32. Fritz G. RAGE: a single receptor fits multiple ligands. Trends Biochem. Sci. 2011, 36:625-632.
33. Matsumoto S., Yoshida T., Murata H., Harada S., Fujita N., Nakamura S., Yamamoto Y., Watanabe T., Yonekura H., Yamamoto H., Ohkubo T., Kobayashi Y. Solution structure of the variable-type domain of the receptor for advanced glycation end products: new insight into AGE-RAGE interaction. Biochemistry 2008, 47:12299-12311.
34. Koch M., Chitayat S., Dattilo B.M., Schiefner A., Diez J., Chazin W.J., Fritz G. Structural basis for ligand recognition and activation of RAGE. Structure 2010, 18:1342-1352.
35. Park H., Boyington J.C. The 1.5Å crystal structure of human receptor for advanced glycation endproducts (RAGE) ectodomains reveals unique features determining ligand binding. J. Biol. Chem. 2010, 285:40762-40770.
36. Nagata S., Hanayama R., Kawane K. Autoimmunity and the clearance of dead cells. Cell 2010, 140:619-630.
37. He M., Kubo H., Morimoto K., Fujino N., Suzuki T., Takahasi T., Yamada M., Yamaya M., Maekawa T., Yamamoto Y., Yamamoto H. Receptor for advanced glycation end products binds to phosphatidylserine and assists in the clearance of apoptotic cells. EMBO Rep. 2011, 12:358-364.
38. Friggeri A., Banerjee S., Biswas S., de Freitas A., Liu G., Bierhaus A., Abraham E. Participation of the receptor for advanced glycation end products in efferocytosis. J. Immunol. 2011, 186:6191-6198.
39. Liu G., Wang J., Park Y.J., Tsuruta Y., Lorne E.F., Zhao X., Abraham E. High mobility group protein-1 inhibits phagocytosis of apoptotic neutrophils through binding to phosphatidylserine. J. Immunol. 2008, 181:4240-4246.
40. Banerjee S., Friggeri A., Liu G., Abraham E. The C-terminal acidic tail is responsible for the inhibitory effects of HMGB1 on efferocytosis. J. Leukoc. Biol. 2010, 88:973-979.
41. Xu D., Young J., Song D., Esko J.D. Heparan sulfate is essential for high mobility group protein 1 (HMGB1) signaling by the receptor for advanced glycation end products (RAGE). J. Biol. Chem. 2011, 286:41736-44144.
42. Hudson B.I., Kalea A.Z., Del Mar Arriero M., Harja E., Boulanger E., D'Agati V., Schmidt A.M. 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. 2008, 283:34457-34468.
43. Watanabe N., Madaule P., Reid T., Ishizaki T., Watanabe G., Kakizuka A., Saito Y., Nakao K., Jockusch B.M., Narumiya S. p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J. 1997, 16:3044-3056.
44. Wasserman S. FH proteins as cytoskeletal organizers. Trends Cell Biol. 1998, 8:111-115.
45. Wallar B.J., Alberts A.S. The formins: active scaffolds that remodel the cytoskeleton. Trends Cell Biol. 2003, 13:435-446.
46. Seth A., Otomo C., Rosen M.K. Autoinhibition regulates cellular localization and actin assembly activity of the diaphanous-related formins FRLα and mDia1. J. Cell Biol. 2006, 174:701-713.
47. Bianchi R., Kastrisianaki E., Giambanco I., Donato R. S100B protein stimulates microglia migration via RAGE-dependent upregulation of chemokine expression and release. J. Biol. Chem. 2011, 286:7214-7226.
48. Sorci G., Riuzzi F., Arcuri C., Giambanco I., Donato R. Amphoterin stimulates myogenesis and counteracts the anti-myogenic factors, bFGF and S100B, via RAGE binding. Mol. Cell. Biol. 2004, 24:4880-4894.
49. Riuzzi F., Sorci G., Donato R. The amphoterin/RAGE pair modulates myoblast proliferation, apoptosis, adhesiveness, migration and invasiveness. Functional inactivation of RAGE in L6 myoblasts results in tumor formation in vivo. J. Biol. Chem. 2006, 281:8242-8253.
50. Riuzzi F., Sorci G., Donato R. RAGE expression in rhabdomyosarcoma cells results in myogenic differentiation and reduced proliferation, migration, invasiveness and tumor growth. Am. J. Pathol. 2007, 171:947-961.
51. Gopinath S.D., Narumiya S., Dhawan J. The RhoA effector mDiaphanous regulates MyoD expression and cell cycle progression via SRF-dependent and SRF-independent pathways. J. Cell Sci. 2007, 120:3086-3098.
52. Sakaguchi M., Murata H., Yamamoto K., Ono T., Sakaguchi Y., Motoyama A., Hibino T., Kataoka K., Huh N.H. TIRAP, an adaptor protein for TLR2/4, transduces a signal from RAGE phosphorylated upon ligand binding. PLoS One 2011, 6:e23132.
53. Huttunen H.J., Kuja-Panula J., Sorci G., Agneletti A.L., Donato R., Rauvala H. Coregulation of neurite outgrowth and cell survival by amphoterin and S100 proteins through RAGE activation. J. Biol. Chem. 2000, 275:40096-40105.
54. Businaro R., Leone S., Fabrizi C., Sorci G., Donato R., Lauro G.M., Fumagalli L. S100B protects neurons against β-amyloid-induced neurotoxicity via RAGE engagement at low doses and increases β-amyloid neurotoxicity at high doses. J. Neurosci. Res. 2006, 83:897-906.
55. Villarreal A., Aviles Reyes R.X., Angelo M.F., Reines A.G., Ramos A.J. S100B alters neuronal survival and dendrite extension via RAGE-mediated NF-κB signaling. J. Neurochem. 2011, 117:321-332.
56. Riuzzi F., Sorci G., Beccafico S., Donato R. S100B engages RAGE or bFGF/FGFR1 in myoblasts depending on its own concentration and myoblast density. Implications for muscle regeneration. PLoS One 2012, 7:e28700.
57. Kuniyasu H., Chihara Y., Kondo H. Differential effects between amphoterin and advanced glycation end products on colon cancer cells. Int. J. Cancer 2003, 104:722-727.
58. Tafani M., Schito L., Pellegrini L., Villanova L., Marfe G., Anwar T., Rosa R., Indelicato M., Fini M., Pucci B., Russo M.A. Hypoxia-increased RAGE and P2X7R expression regulates tumor cell invasion through phosphorylation of Erk1/2 and Akt and nuclear translocation of NF-κB. Carcinogenesis 2011, 32:1167-1175.
59. Yan W., Chang Y., Liang X., Cardinal J.S., Huang H., Thorne S.H., Monga S.P., Geller D.A., Lotze M.T., Tsung A. High mobility group box 1 activates caspase-1 and promotes hepatocellular carcinoma invasiveness and metastases. Hepatology 2012, 55:1863-1875.
60. Jube S., Rivera Z., Bianchi M.E., Powers A., Wang E., Pagano I.S., Pass H.I., Gaudino G., Carbone M., Yang H. Cancer cell secretion of the DAMP protein HMGB1 supports progression in malignant mesothelioma. Cancer Res. 2012, 72:3290-3301.
61. Moroz O.V., Antson A.A., Grist S.J., Maitland N.J., Dodson G.G., Wilson K.S., Lukanidin E., Bronstein I.B. The structure of S100A12 in a hexameric form and its proposed role in receptor signaling. Acta Crystallogr. D 2002, 58:407-413.
62. Novitskaya V., Grigorian M., Kriajevska M., Tarabykina S., Bronstein I., Berezin V., Bock E., Lukanidin E. Oligomeric forms of the metastasis-related Mts1 (S100A4) protein stimulate neuronal differentiation in cultures of rat hippocampal neurons. J. Biol. Chem. 2000, 275:41278-41286.
63. Koch M., Bhattacharya S., Kehl T., Gimona M., Vasák M., Chazin W., Heizmann C.W., Kroneck P.M., Fritz G. Implications on zinc binding to S100A2. Biochim. Biophys. Acta 2007, 1773:457-470.
64. 2 heterotetramer, calprotectin, illustrates how conformational changes of interacting α-helices can determine specific association of two EF-hand proteins. J. Mol. Biol. 2007, 370:887-898.
65. Ma W., Lee S.E., Guo J., Qu W., Hudson B.I., Schmidt A.M., Barile G.R. RAGE ligand upregulation of VEGF secretion in ARPE-19 cells. Invest. Ophthalmol. Vis. Sci. 2007, 48:1355-1361.
66. Ostendorp T., Leclerc E., Galichet A., Koch M., Demling N., Weigle B., Heizmann C.W., Kroneck P.M., Fritz G. Structural and functional insights into RAGE activation by multimeric S100B. EMBO J. 2007, 26:3868-3878.
67. Reali C., Scintu F., Pillai R., Donato R., Michetti F., Sogos V. S100B counteracts effects of the neurotoxicant trimethyltin on astrocytes and microglia. J. Neurosci. Res. 2005, 81:677-686.
68. Bianchi R., Adami C., Giambanco I., Donato R. S100B binding to RAGE in microglia stimulates COX-2 expression. J. Leukoc. Biol. 2007, 81:108-118.
69. Bianchi R., Giambanco I., Donato R. S100B/RAGE-dependent activation of microglia via NF-κB and AP-1. Co-regulation of COX-2 expression by S100B and IL-1β and TNF-α. Neurobiol. Aging 2010, 31:665-677. 10.1016/j.neurobiolaging.2008.05.017.
70. Ponath G., Schettler C., Kaestner F., Voigt B., Wentker D., Arolt V., Rothermundt M. Autocrine S100B effects on astrocytes are mediated via RAGE. J. Neuroimmunol. 2007, 184:214-222.
71. Lu C., He J.C., Cai W., Liu H., Zhou L., Vlassara H. AGE-receptor-1 is a negative regulator of the inflammatory response to advanced glycation endproducts in mesangial cells. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:11767-11772.
72. Foell D., Wittkowski H., Roth J. Mechanisms of disease: a "DAMP" view of inflammatory arthritis. Nat. Clin. Pract. Rheumatol. 2007, 3:382-390.
73. Hsu K., Champaiboon C., Guenther B.D., Sorenson B.S., Khammanivong A., Ross K.F., Geczy C.L., Herzberg M.C. Anti-infective protective properties of S100 calgranulins. Antiinflamm. Antiallergy Agents Med. Chem. 2009, 8:290-305.
74. Pietzsch J., Hoppmann S. Human S100A12: a novel key player in inflammation?. Amino Acids 2009, 36:381-389.
75. Yammani R.R. S100 proteins in cartilage: role in arthritis. Biochim. Biophys. Acta 2012, 1822:600-606.
76. Mikkelsen S.E., Novitskaya V., Kriajevska M., Berezin V., Bock E., Norrild B., Lukanidin E. S100A12 protein is a strong inducer of neurite outgrowth from primary hippocampal neurons. J. Neurochem. 2001, 79:767-776.
77. 2+ signaling in neurons induced by the S100A4 protein. Mol. Cell. Biol. 2006, 26:3625-3638.
78. Ghavami S., Rashedi I., Dattilo B.M., Eshraghi M., Chazin W.J., Hashemi M., Wesselborg S., Kerkhoff C., Los M. S100A8/A9 at low concentration promotes tumor cell growth via RAGE ligation and MAP kinase-dependent pathway. J. Leukoc. Biol. 2008, 83:1484-1492.
79. Ghavami S., Kerkhoff C., Chazin W.J., Kadkhoda K., Xiao W., Zuse A., Hashemi M., Eshraghi M., Schulze-Osthoff K., Klonisch T., Los M. S100A8/9 induces cell death via a novel, RAGE-independent pathway that involves selective release of Smac/DIABLO and Omi/HtrA2. Biochim. Biophys. Acta 2008, 1783:297-311.
80. Origlia N., Bonadonna C., Rosellini A., Leznik E., Arancio O., Yan S.S., Domenici L. Microglial receptor for advanced glycation end product-dependent signal pathway drives β-amyloid-induced synaptic depression and long-term depression impairment in entorhinal cortex. J. Neurosci. 2010, 30:11414-11425.
81. Srikanth V., Maczurek A., Phan T., Steele M., Westcott B., Juskiw D., Münch G. Advanced glycation endproducts and their receptor RAGE in Alzheimer's disease. Neurobiol. Aging 2011, 32:763-777.
82. Chen G.Y., Nuñez G. Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 2010, 10:826-837.
83. Donato R., Sorci G., Riuzzi F., Arcuri C., Bianchi R., Brozzi F., Tubaro C., Giambanco I. S100B's double life: intracellular regulator and extracellular signal. Biochim. Biophys. Acta 2009, 1793:1008-1022.
84. Lue L.F., Walker D.G., Brachova L., Beach T.G., Rogers J., Schmidt A.M., Stern D.M., Yan S.D. Involvement of microglial receptor for advanced glycation endproducts (RAGE) in Alzheimer's disease: identification of a cellular activation mechanism. Exp. Neurol. 2001, 171:29-45.
85. Zhang L., Liu W., Alizadeh D., Zhao D., Farrukh O., Lin J., Badie S.A., Badie B. S100B attenuates microglia activation in gliomas: possible role of STAT3 pathway. Glia 2011, 59:486-498.
86. Glezer I., Simard A.R., Rivest S. Neuroprotective role of the innate immune system by microglia. Neuroscience 2007, 147:867-883.
87. Hanisch U.K., Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 2007, 10:1387-1394.
88. Bierhaus A., Stern D.M., Nawroth P.P. RAGE in inflammation: a new therapeutic target?. Curr. Opin. Investig. Drugs 2006, 7:985-991.
89. Yan S.F., Ramasamy R., Schmidt A.M. Receptor for AGE (RAGE) and its ligands-cast into leading roles in diabetes and the inflammatory response. J. Mol. Med. (Berl.) 2009, 87:235-247.
90. Ramasamy R., Yan S.F., Schmidt A.M. Receptor for AGE (RAGE): signaling mechanisms in the pathogenesis of diabetes and its complications. Ann. N. Y. Acad. Sci. 2011, 1243:88-102.
91. Hofmann Bowman M.A., Schmidt AM A.M. S100/calgranulins EN-RAGEing the blood vessels: implications for inflammatory responses and atherosclerosis. Am. J. Cardiovasc. Dis. 2011, 1:92-100.
92. Yan S.F., Yan S.D., Ramasamy R., Schmidt A.M. Tempering the wrath of RAGE: an emerging therapeutic strategy against diabetic complications, neurodegeneration, and inflammation. Ann. Med. 2009, 41:408-422.
93. Deane R., Singh I., Sagare A.P., Bell R.D., Ross N.T., LaRue B., Love R., Perry S., Paquette N., Deane R.J., Thiyagarajan M., Zarcone T., Fritz G., Friedman A.E., Miller B.L., Zlokovic B.V. A multimodal RAGE-specific inhibitor reduces amyloid β-mediated brain disorder in a mouse model of Alzheimer disease. J. Clin. Invest. 2012, 122:1377-1392.
94. Bartling B., Hofmann H.-S., Weigle B., Silber R.-E., Simm A. Down-regulation of the receptor for advanced glycation end-products (RAGE) supports non-small cell lung carcinoma. Carcinogenesis 2005, 26:293-301.
95. Landesberg R., Woo V., Huang L., Cozin M., Lu Y., Bailey C., Qu W., Pulse C., Schmidt A.M. The expression of the receptor for glycation endproducts (RAGE) in oral squamous cell carcinomas. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 2008, 105:617-624.
96. Tateno T., Ueno S., Hiwatashi K., Matsumoto M., Okumura H., Setoyama T., Uchikado Y., Sakoda M., Kubo F., Ishigami S., Shinchi H., Natsugoe S. Expression of receptor for advanced glycation end products (RAGE) is related to prognosis in patients with esophageal squamous cell carcinoma. Ann. Surg. Oncol. 2009, 16:440-446.
97. Yammani R.R., Carlson C.S., Bresnick A.R., Loeser R.F. Increase in production of matrix metalloproteinase 13 by human articular chondrocytes due to stimulation with S100A4: role of the receptor for advanced glycation end products. Arthritis Rheum. 2006, 54:2901-2911.
98. Schneider M., Kostin S., Strøm C.C., Aplin M., Lyngbaek S., Theilade J., Grigorian M., Andersen C.B., Lukanidin E., Lerche Hansen J., Sheikh S.P. S100A4 is upregulated in injured myocardium and promotes growth and survival of cardiac myocytes. Cardiovasc. Res. 2007, 75:40-50.
99. Kang R., Tang D., Schapiro N.E., Livesey K.M., Farkas A., Loughran P., Bierhaus A., Lotze M.T., Zeh H.J. 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.
100. Kang R., Tang D., Lotze M.T., Zeh H.J. Apoptosis to autophagy switch triggered by the MHC class III-encoded receptor for advanced glycation endproducts (RAGE). Autophagy 2011, 7:91-93.
101. Son S.M., Jung E.S., Shin H.J., Byun J., Mook-Jung I. Aβ-induced formation of autophagosomes is mediated by RAGE-CaMKKβ-AMPK signaling. Neurobiol. Aging 2012, 33:1006.
102. Menendez J.A., Vellon L., Oliveras-Ferraros C., Cufí S., Vazquez-Martin A. mTOR-regulated senescence and autophagy during reprogramming of somatic cells to pluripotency: a roadmap from energy metabolism to stem cell renewal and aging. Cell Cycle 2011, 10:3658-3677.
103. Mizushima N., Komatsu M. Autophagy: renovation of cells and tissues. Cell 2011, 147:728-741.
104. Fuchs Y., Steller H. Programmed cell death in animal development and disease. Cell 2011, 147:742-758.
105. Shang L., Ananthakrishnan R., Li Q., Quadri N., Abdillahi M., Zhu Z., Qu W., Rosario R., Touré F., Yan S.F., Schmidt A.M., Ramasamy R. RAGE modulates hypoxia/reoxygenation injury in adult murine cardiomyocytes via JNK and GSK-3β signaling pathways. PLoS One 2010, 5:e10092.
106. Tsoporis J.N., Izhar S., Leong-Poi H., Desjardins J.F., Huttunen H.J., Parker T.G. S100B interaction with the receptor for advanced glycation end products (RAGE): a novel receptor-mediated mechanism for myocyte apoptosis postinfarction. Circ. Res. 2010, 106:93-101.
107. van Zoelen M.A., Schmidt A.M., Florquin S., Meijers J.C., de Beer R., de Vos A.F., Nawroth P.P., Bierhaus A., van der Poll T. Receptor for advanced glycation end products facilitates host defense during Escherichia coli-induced abdominal sepsis in mice. J. Infect. Dis. 2009, 200:765-773.
108. van Zoelen M.A., Wieland C.W., van der Windt G.J., Florquin S., Nawroth P.P., Bierhaus A., van der Poll T. Receptor for advanced glycation end products is protective during murine tuberculosis. Mol. Immunol. 2012, 52:183-189.
109. Sorci G., Giovannini G., Riuzzi F., Bonifazi P., Zelante T., Zagarella S., Bistoni F., Donato R., Romani L. The danger signal S100B integrates pathogen- and danger-sensing pathways to restrain inflammation. PLoS Pathog. 2011, 7:e1001315.
110. van Zoelen M.A., Schouten M., de Vos A.F., Florquin S., Meijers J.C., Nawroth P.P., Bierhaus A., van der Poll T. The receptor for advanced glycation end products impairs host defense in pneumococcal pneumonia. J. Immunol. 2009, 182:4349-4356.
111. van Zoelen M.A., van der Sluijs K.F., Achouiti A., Florquin S., Braun-Pater J.M., Yang H., Nawroth P.P., Tracey K.J., Bierhaus A., van der Poll T. Receptor for advanced glycation end products is detrimental during influenza A virus pneumonia. Virology 2009, 391:265-273.
112. Cunha C., Giovannini G., Pierini A., Bell A.S., Sorci G., Riuzzi F., Donato R., Rodrigues F., Velardi A., Aversa F., Romani L., Carvalho A. Genetically-determined hyperfunction of the S100B/RAGE axis is a risk factor for aspergillosis in stem cell transplant recipients. PLoS One 2011, 6:e27962.
113. Englert J.M., Hanford L.E., Kaminski N., Tobolewski J.M., Tan R.J., Fattman C.L., Ramsgaard L., Richards T.J., Loutaev I., Nawroth P.P., Kasper M., Bierhaus A., Oury T.D. A role for the receptor for advanced glycation end products in idiopathic pulmonary fibrosis. Am. J. Pathol. 2008, 172:583-591.
114. Queisser M.A., Kouri F.M., Königshoff M., Wygrecka M., Schubert U., Eickelberg O., Preissner K.T. Loss of RAGE in pulmonary fibrosis: molecular relations to functional changes in pulmonary cell types. Am. J. Respir. Cell Mol. Biol. 2008, 39:337-345.
115. Repapi E., Sayers I., Wain L.V., Burton P.R., Johnson T., Obeidat M., Zhao J.H., Ramasamy A., Zhai G., Vitart V., Huffman J.E., Igl W., Albrecht E., Deloukas P., Henderson J., Granell R., McArdle W.L., Rudnicka A.R., Wellcome Trust Case Control Consortium, Barroso I., Loos R.J., Wareham N.J., Mustelin L., Rantanen T., Surakka I., Imboden M., Wichmann H.E., Grkovic I., Jankovic S., Zgaga L., Hartikainen A.L., Peltonen L., Gyllensten U., Johansson A., Zaboli G., Campbell H., Wild S.H., Wilson J.F., Gläser S., Homuth G., Völzke H., Mangino M., Soranzo N., Spector T.D., Polasek O., Rudan I., Wright A.F., Heliövaara M., Ripatti S., Pouta A., Naluai A.T., Olin A.C., Torén K., Cooper M.N., James A.L., Palmer L.J., Hingorani A.D., Wannamethee S.G., Whincup P.H., Smith G.D., Ebrahim S., McKeever T.M., Pavord I.D., MacLeod A.K., Morris A.D., Porteous D.J., Cooper C., Dennison E., Shaheen S., Karrasch S., Schnabel E., Schulz H., Grallert H., Bouatia-Naji N., Delplanque J., Froguel P., Blakey J.D., Britton J.R., Morris R.W., Holloway J.W., Lawlor D.A., Hui J., Nyberg F., Jarvelin M.R., Jackson C., Kähönen M., Kaprio J., Probst-Hensch N.M., Koch B., Hayward C., Evans D.M., Elliott P., Strachan D.P., Hall I.P., Tobin M.D. Genome-wide association study identifies five loci associated with lung function. Nat. Genet. 2010, 42:36-44. NSHD Respiratory Study Team.
116. Hancock D.B., Eijgelsheim M., Wilk J.B., Gharib S.A., Loehr L.R., Marciante K.D., Franceschini N., van Durme Y.M., Chen T.H., Barr R.G., Schabath M.B., Couper D.J., Brusselle G.G., Psaty B.M., van Duijn C.M., Rotter J.I., Uitterlinden A.G., Hofman A., Punjabi N.M., Rivadeneira F., Morrison A.C., Enright P.L., North K.E., Heckbert S.R., Lumley T., Stricker B.H., O'Connor G.T., London S.J. Meta-analyses of genome-wide association studies identify multiple loci associated with pulmonary function. Nat. Genet. 2010, 42:45-52.
117. Zeng S., Zhang Q.Y., Huang J., Vedantham S., Rosario R., Ananthakrishnan R., Yan S.F., Ramasamy R., Dematteo R.P., Emond J.C., Friedman R.A., Schmidt A.M. Opposing roles of RAGE and Myd88 signaling in extensive liver resection. FASEB J. 2011, 26:882-893.
118. Rong L.L., Trojaborg W., Qu W., Kostov K., Yan S.D., Gooch C., Szabolcs M., Hays A.P., Schmidt A.M. Antagonism of RAGE suppresses peripheral nerve regeneration. FASEB J. 2004, 18:1812-1817.
119. Rong L.L., Yan S.F., Wendt T., Hans D., Pachydaki S., Bucciarelli L.G., Adebayo A., Qu W., Lu Y., Kostov K., Lalla E., Yan S.D., Gooch C., Szabolcs M., Trojaborg W., Hays A.P., Schmidt A.M. RAGE modulates peripheral nerve regeneration via recruitment of both inflammatory and axonal outgrowth pathways. FASEB J. 2004, 18:1818-1825.
120. Sbai O., Devi T.S., Melone M.A., Feron F., Khrestchatisky M., Singh L.P., Perrone L. RAGE-TXNIP axis is required for S100B-promoted Schwann cell migration, fibronectin expression and cytokine secretion. J. Cell Sci. 2010, 123:4332-4339.
121. Meneghini V., Francese M.T., Carraro L., Grilli M. A novel role for the receptor for advanced glycation end-products in neural progenitor cells derived from adult subventricular zone. Mol. Cell. Neurosci. 2010, 45:139-150.
122. Beccafico S., Riuzzi F., Puglielli C., Mancinelli R., Fulle S., Sorci G., Donato R. Human muscle satellite cells show age-related differential expression of S100B protein and RAGE. Age 2011, 33:523-541.
123. Hettmer S.H., Wangers A.J. Uncovering the origins of rhabdomyosarcoma. Nat. Med. 2010, 16:171-173.
124. Rossini A., Zacheo A., Mocini D., Totta P., Facchiano A., Castoldi R., Sordini P., Pompilio G., Abeni D., Capogrossi M.C., Germani A. HMGB1-stimulated human primary cardiac fibroblasts exert a paracrine action on human and murine cardiac stem cells. J. Mol. Cell. Cardiol. 2008, 44:683-693.
125. Ranzato E., Patrone M., Pedrazzi M., Burlando B. Hmgb1 promotes wound healing of 3T3 mouse fibroblasts via RAGE-dependent ERK1/2 activation. Cell Biochem. Biophys. 2010, 57:9-17.