Endogenous secretory receptor for advanced glycation end-products inhibits amyloid-β1-42 uptake into mouse brain

Journal of Alzheimer's Disease

Volumn 28, Issue 3, 2012, Pages 709-720

  Sugihara, Takahiro ^a   Munesue, Seiichi ^a   Yamamoto, Yasuhiko ^a   Sakurai, Shigeru ^a   Akhter, Nasima ^a   Kitamura, Yoji ^a   Shiba, Kazuhiro ^a   Watanabe, Takuo ^a   Yonekura, Hideto ^b   Hayashi, Yasuhiko ^a   Hamada, Jun Ichiro ^a   Yamamoto, Hiroshi ^a  

^a KANAZAWA UNIVERSITY   (Japan)

^b KANAZAWA MEDICAL UNIVERSITY   (Japan)

Author keywords

Alzheimer's disease; esRAGE; RAGE; transgenic mice

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; AMYLOID BETA PROTEIN[1-42]; IODINE 125;

ANIMAL EXPERIMENT; ARTICLE; BODY FLUID; BRAIN; BRAIN CIRCULATION; BRAIN CORTEX; BRAIN VENTRICLE; CONTROLLED STUDY; GENE OVEREXPRESSION; HIPPOCAMPUS; HUMAN; IMMUNOGLOBULIN VARIABLE REGION; ISOTOPE LABELING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PUTAMEN; RADIOASSAY; SURFACE PLASMON RESONANCE; THALAMOTOMY; WILD TYPE;

EID: 84863233140     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2011-110776     Document Type: Article

References (52)

1. Schmidt AM, Vianna M, Gerlach M, Brett J, Ryan J, Kao J, Esposito C, Hegarty H, Hurley W, Clauss M, Wangll F, Pan YC, Tsang TC, Stern D (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 267, 14987-14997.
2. Hofmann MA, Drury S, Fu C, Qu W, Taguchi A, Lu Y, Avila C, Kambham N, Bierhaus A, Nawroth P, Neurath MF, Slattery T, Beach D, McClary J, Nagashima M, Morser J, Stern D, Schmidt AM (1999) RAGE mediates a novel proinflammatory axis: A central cell surface receptor for S100/calgranulin polypeptides. Cell 97, 889-901. (Pubitemid 29375048)
3. Chavakis T, Bierhaus A, Al-Fakhri N, Schneider D, Witte S, Linn T, Nagashima M, Morser. J, Arnold B, Preissner KT, Nawroth PP (2003) The pattern recognition receptor (RAGE) is a counterreceptor for leukocyte integrins: A novel pathway for inflammatory cell recruitment. J Exp Med 198, 1507- 1515.
4. 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 κB (NF-κB) activation. Lab Invest 80, 1101-1110. (Pubitemid 30483229)
5. Hori O, Brett. J, Slattery T, Cao R, Zhang J, Chen J, Nagashima M, Lundh ER, Vijay S, Nitecki D, Morser J, Stern D, Schmidt AM (1995) The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin: Mediation of neurite outgrowth and co-expression of rage and amphoterin in the developing nervous system. J Biol Chem 270, 25752-25761.
6. Yamamoto Y, Harashima A, Saito H, Tsuneyama K, Munesue S, Motoyoshi S, Han D, Watanabe T, Asano M, Takasawa S, Okamoto H, Shimura S, Karasawa T, Yonekura H, Yamamoto H (2011) Septic shock is associated with receptor for advanced glycation endproducts (RAGE) ligation of LPS. J Immunol 186, 3248-3257.
7. He M, Kubo H, Morimoto K, Fujino N, Suzuki T, Takahasi T, Yamada M, Yamaya M, Maekawa T, Yamamoto Y, Yamamoto H (2011) Receptor for advanced glycation end products binds to phosphatidylserine and assists in the clearance of apoptotic cells. EMBO Rep 12, 358-364.
8. Yan SD, Chen X, Fu J, Chen M, Zhu H, Roher A, Slattery T, Zhao L, Nagashima M, Morser J, Migheli A, Nawroth P, Stern D, Schmidt AM (1996) RAGE and amyloid-β peptide neurotoxicity in Alzheimer's disease. Nature 382, 685- 691.
9. Yamamoto Y, Kato I, Doi T, Yonekura H, Ohashi S, Takeuchi M, Watanabe T, Yamagishi S, Sakurai S, Takasawa S, Okamoto H, Yamamoto H (2001) Development and prevention of advanced diabetic nephropathy in RAGE-overexpressing mice. J Clin Invest 108, 261-268. (Pubitemid 32656250)
10. 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, 949- 955.
11. Bucciarelli LG, Wendt T, Rong L, Lalla E, Hofmann MA, Goova MT, Taguchi A, Yan SF, Yan SD, Stern DM, Schmidt AM (2002) RAGE is a multiligand receptor of the immunoglobulin superfamily: implications for homeostasis and chronic disease. Cell Mol Life Sci 59, 1117-1128.
12. Sparvero LJ, Asafu-Adjei D, Kang R, Tang D, Amin N, Im J, Rutledge R, Lin B, Amoscato AA, Zeh HJ, Lotze MT (2009) RAGE (receptor for advanced glycation endproducts), RAGE ligands, and their role in cancer and inflammation. J Transl Med 7, pp. 7-28.
13. Kosik KS, Duffy LK, Dowling MM, Abraham C, McCluskey A, Selkoe DJ (1984) Microtubule-associated protein 2: Monoclonal antibodies demonstrate the selective incorporation of certain epitopes into Alzheimer neurofibrillary tangles. Proc Natl Acad Sci U S A 81, 7941-7945. (Pubitemid 15169178)
14. Hardy JA, Higgins GA (1992) Alzheimer's disease: The amyloid cascade hypothesis. Science 256, 184-185.
15. Giri R, Selvaraj S, Miller CA, Hofman F, Yan SD, Stern D, Zlokovic BV, Kalra VK (2002) Effect of endothelial cell polarity on β-amyloid-induced migration of monocytes across normal and AD endothelium. Am J Physiol Cell Physiol 283, C895-C904. (Pubitemid 34920322)
16. Zou K, Gong JS, Yanagisawa K, Michikawa M (2002) A novel function of monomeric amyloid β-protein serving as an antioxidant molecule against metal-induced oxidative damage. J Neurosci 22, 4833-4841. (Pubitemid 37465598)
17. Zou K, Kim D, Kakio A, Byun K, Gong JS, Kim. J, Kim M, Sawamura N, Nishimoto S, Matsuzaki K, Lee B, Yanagisawa K, Michikawa M (2003) Amyloid β-protein (Aβ)1-40 protects neurons from damage induced by Aβ1-42 in culture and in rat brain. J Neurochem 87, 609-619. (Pubitemid 37310627)
18. Zloković BV, Segal MB, Begley DJ, Davson H, Rakić L (1985) Permeability of the blood-cerebrospinal fluid and blood-brain barriers to thyrotropin-releasing hormone. Brain Res 358, 191-199.
19. Mann GE, Zlokovic BV, Yudilevich DL (1985) Evidence for a lactate transport system in the sarcolemmal membrane of the perfused rabbit heart: Kinetics of unidirectional influx, carrier specificity and effects of glucagon. Biochim Biophys Acta 819, 241-248. (Pubitemid 16238675)
20. Mackic JB, Stins M, McComb JG, Calero M, Ghiso J, Kim KS, Yan SD, Stern D, Schmidt AM, Frangione B, Zlokovic BV (1998) Human blood-brain barrier receptors for Alzheimer's amyloid-β 1-40. Asymmetrical binding, endocytosis, and transcytosis at the apical side of brain microvascular endothelial cell monolayer. J Clin Invest 102, 734-743. (Pubitemid 28399606)
21. Zlokovic BV, Yamada S, Holtzman D, Ghiso J, Frangione B (2000) Clearance of amyloid β-peptide from brain: transport or metabolism? Nat Med 6, 718.
22. Zlokovic BV (2004) Clearing amyloid through the blood-brain barrier. J Neurochem 89, 807-811.
23. Deane R, Du YS, Submamaryan RK, LaRue B, Jovanovic S, Hogg E, Welch D, Manness L, Lin C, Yu J, Zhu H, Ghiso J, Frangione B, Stern A, Schmidt AM, Armstrong DL, Arnold B, Liliensiek B, Nawroth P, Hofman F, Kindy M, Stern D, Zlokovic B (2003) RAGE mediates amyloid-β peptide transport across the blood-brain barrier and accumulation in brain. Nat Med 9, 907-913. (Pubitemid 36889934)
24. Giri R, Shen Y, Stins M, Du YS, Schmidt AM, Stern D, Kim KS, Zlokovic B, Kalra VK (2000) β-amyloid-induced migration of monocytes across human brain endothelial cells involves RAGE and PECAM-1. Am J Physiol Cell Physiol 279, C1772-C1781.
25. Yonekura H, Yamamoto Y, Sakurai S, Petrova RG, Abedin MJ, Li H, Yasui K, Takeuchi M, Makita Z, Takasawa S, Okamoto H, Watanabe T, Yamamoto H (2003) Novel splice variants of the receptor for advanced glycation end-products expressed in human vascular endothelial cells and pericytes, and their putative roles in diabetes-induced vascular injury. Biochem J 370, 1097-1109. (Pubitemid 36399105)
26. Hanford LE, Enghild JJ, Valnickova Z, Petersen SV, Schaefer LM, Schaefer TM, Reinhart TA, Oury TD (2004) Purification and characterization of mouse soluble receptor for advanced glycation end products (sRAGE). J Biol Chem 279, 50019- 50024.
27. Raucci A, Cugusi S, Antonelli A, Barabino SM, Monti L, Bierhaus A, Reiss K, Saftig P, Bianchi ME (2008) A soluble form of the receptor for advanced glycation end-products (RAGE) is produced by proteolytic cleavage of the membrane-bound form by the sheddase a disintegrin and metalloprotease 10 (ADAM10). FASEB J 10, 3716-3727.
28. Zhang L, Bukulin M, Kojro E, Roth A, Metz VV, Fahrenholz F, Nawroth PP, Bierhaus A, Postina R (2008) Receptor for advanced glycation end products is subjected to protein ectodomain shedding by metalloproteinases. J Biol Chem 283, 35507-35516.
29. Zhang L, Postina R, Wang Y (2009) Ectodomain shedding of the receptor for advanced glycation end products: A novel therapeutic target for Alzheimer's disease. Cell Mol Life Sci 66, 3923-3935.
30. Cheng C, Tsuneyama K, Kominami R, Shinohara H, Sakurai S, Yonekura H, Watanabe T, Takano Y, Yamamoto H, Yamamoto Y (2005) Expression profiling of endogenous secretory receptor for advanced glycation endproducts in human organs. Mod Pathol 18, 1385-1396. (Pubitemid 41348659)
31. Nozaki I, Watanabe T, Kawaguchi M, Akatsu H, Tsuneyama K, Yamamoto Y, Ohe K, Yonekura H, Yamada M, Yamamoto H (2007) Reduced expression of endogenous secretory receptor for advanced glycation endproducts in hippocampal neurons of Alzheimer's disease brains. Arch Histol Cytol 70, 1691-1696.
32. Conner EA, Lemmer ER, Omori M, Wirth PJ, Factor VM, Thorgeirsson SS (2000) Dual functions of E2F-1 in a transgenic mouse model of liver carcinogenesis. Oncogene 19, 5054-5062.
33. Myint KM, Yamamoto Y, Doi T, Kato I, Harashima A, Yonekura H, Watanabe T, Shinohara H, Takeuchi M, Tsuneyama K, Hashimoto N, Asano M, Takasawa S, Okamoto H, Yamamoto H (2006) RAGE control of diabetic nephropathy in a mouse model: Effects of RAGE gene disruption and administration of low-molecular weight heparin. Diabetes 55, 2510-2522. (Pubitemid 44871151)
34. Sakatani S, Yamada K, Homma C, Munesue S, Yamamoto Y, Yamamoto H, Hirase H (2009) Deletion of RAGE causes hyperactivity and increased sensitivity to auditory stimuli in mice. PLoS One 4, e8309.
35. Sakurai S, Yamamoto Y, Tamei H, Matsuki H, Obata K, Hui L, Miura J, Osawa M, Uchigata Y, Iwamoto Y, Watanabe T, Yonekura H, Yamamoto H (2006) Development of an ELISA for esRAGE and its application to type 1 diabetic patients. Diabetes Res Clin Pract 73, 158-165. (Pubitemid 43928158)
36. Poduslo JF, Curran GL, Berg CT (1994) Macromolecular permeability across the blood-nerve and blood-brain barriers. Proc Natl Acad Sci U S A 91, 5705-5709. (Pubitemid 24174397)
37. Zlokovic BV, Martel CL, Matsubara E, McComb JG, Zheng G, McCluskey RT, Frangione B, Ghiso J (1996) Glycoprotein 330/ megalin: probable role in receptor-mediated transport of apolipoprotein J alone and in a complex with Alzheimer disease amyloid β at the blood-brain and blood-cerebrospinal fluid barriers. Proc Natl Acad Sci U S A 93, 4229-4234.
38. Martel CL, Mackic JB, Matsubara E, Governale S, Miguel C, Miao W, McComb JG, Frangione B, Ghiso J, Zlokovic BV (1997) Isoform-specific effects of apolipoproteins E2, E3, and E4 on cerebral capillary sequestration and blood-brain barrier transport of circulating Alzheimer's amyloid β. J Neurochem 69, 1995-2004. (Pubitemid 27452746)
39. Gospodarska E, Kupniewska-Kozak A, Goch G, Dadlez M (2011) Binding studies of truncated variants of the Aβ peptide to the V-domain of the RAGE receptor reveal Aβ residues responsible for binding. Biochim Biophys Acta 1814, 592-609.
40. Chaney MO, Stine WB, Kokjohn TA, Kuo YM, Esh C, Rahman A, Luehrs DC, Schmidt AM, Stern D, Yan SD, Roher AE (2005) RAGE and amyloid beta interactions: Atomic force microscopy and molecular modeling. Biochim Biophys Acta 1741, 199-205. (Pubitemid 40825005)
41. Harashima A, Yamamoto Y, Cheng C, Tsuneyama K, Myint KM, Takeuchi A, Yoshimura K, Li H, Watanabe T, Takasawa S, Okamoto H, Yonekura H, Yamamoto H (2006) Identification of mouse orthologue of endogenous secretory receptor for advanced glycation end-products: Structure, function and expression. Biochem J 396, 109-115. (Pubitemid 43764502)
42. Sagare A, Deane R, Bell RD, Johnson B, Hamm K, Pendu R, Marky A, Lenting PJ, Wu Z, Zarcone T, Goate A, Mayo K, Perlmutter D, Coma M, Zhong Z, Zlokovic BV (2007) Clearance of amyloid-β by circulating lipoprotein receptors. Nat Med 9, 1029-1031. (Pubitemid 47517512)
43. West MJ, Kawas CH, Stewart WF, Rudow GL, Troncoso JC (2004) Hippocampal neurons in pre-clinical Alzheimer's disease. Neurobiol Aging 25, 1205-1212. (Pubitemid 39094023)
44. Emanuele E, D'Angelo A, Tomaino C, Binetti G, Ghidoni R, Politi P, Bernardi L, Maletta R, Bruni AC, Geroldi D (2005) Circulating levels of soluble receptor for advanced glycation end products in Alzheimer disease and vascular dementia. Arch Neurol 62, 1734-1736. (Pubitemid 41626671)
45. Tanaka N, Yonekura H, Yamagishi S, Fujimori H, Yamamoto Y, Yamamoto H (2000) The receptor for advanced glycation endproducts is induced by the glycation products themselves and TNF-α through NF-κB, and by 17β-estradiol through Sp-1 in human vascular endothelial cells. J Biol Chem 275, 25781-25790.
46. Lander HM, Tauras JM, Ogiste JS, Hori O, Moss RA, Schmidt AM (1997) Activation of the receptor for advanced glycation end products triggers a p21(ras)-dependent mitogen-activated protein kinase pathway regulated by oxidant stress. J Biol Chem 272, 17810-17814. (Pubitemid 27311222)
47. 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. (Pubitemid 27276477)
48. Li JJ, Dickson D, Hof PR, Vlassara H (1998) Receptors for advanced glycosylation endproducts in human brain: Role in brain homeostasis. Mol Med 4, 46-60. (Pubitemid 28134332)
49. Bierhaus A, Schiekofer S, Schwaninger M, Andrassy M, Humpert PM, Chen J, Hong M, Luther T, Henle T, Klöting I, Morcos M, Hofmann M, Tritschler H, Weigle B, Kasper M, Smith M, Perry G, Schmidt AM, Stern DM, Häring HU, Schleicher E, Nawroth PP (2001) Diabetes-associated sustained activation of the transcription factor nuclear factor-kappaB. Diabetes 50, 2792-2808. (Pubitemid 33733131)
50. Stern DM, Schmidt AM, Yan SD, Yan SF (2002) Receptor for advanced glycation endproducts (RAGE) and the complications of diabetes. Ageing Res Rev 1, 1-15. (Pubitemid 38340348)
51. Cho HJ, Son SM, Jin SM, Hong HS, Shin DH, Kim SJ, Huh K, Mook-Jung I (2009) RAGE regulates BACE1 and Aβ generation via NFAT1 activation in Alzheimer's disease animal model. FASEB J 23, 2639-2649.
52. Li M, Shang DS, Zhao WD, Tian L, Li B, Fang WG, Zhu L, Man SM, Chen YH (2002) Amyloid β interaction with receptor for advanced glycation end products up-regulates brain endothelial CCR5 expression and promotes T cells crossing the blood-brain barrier. J Immunol 182, 5778-5788.