A novel role for the Receptor for Advanced Glycation End-products in neural progenitor cells derived from adult SubVentricular Zone

Molecular and Cellular Neuroscience

Volumn 45, Issue 2, 2010, Pages 139-150

  Meneghini, Vasco ^a   Francese, Maria Teresa ^a   Carraro, Lorenzo ^a   Grilli, Mariagrazia ^a  

^a UNIVERSITY OF EASTERN PIEDMONT   (Italy)

Author keywords

Adult neural progenitor cells; Adult neurogenesis; HMGB 1; NF B; RAGE; SubVentricular Zone

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NESTIN; PROTEIN S100B; SN 50; TRANSCRIPTION FACTOR SOX2;

ADULT STEM CELL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CELL SUBPOPULATION; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; IMMUNOBLOTTING; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SUBVENTRICULAR ZONE;

ANIMALS; CELL DIFFERENTIATION; CEREBRAL VENTRICLES; GLYCOSYLATION END PRODUCTS, ADVANCED; MALE; MICE; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NEUROGENESIS; NF-KAPPA B; RECEPTORS, IMMUNOLOGIC; UP-REGULATION;

EID: 77955773916     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2010.06.005     Document Type: Article

References (65)

1. Arancio O., Zhang H.P., Chen X., Lin C., Trinchese F., Puzzo D., Liu S., Hegde A., Yan S.F., Stern A., et al. RAGE potentiates Abeta-induced perturbation of neuronal function in transgenic mice. EMBO J. 2004, 23:4096-4105.
2. Bernardino L., Agasse F., Silva B., Ferreira R., Grade S., Malva J.O. Tumor necrosis factor-alpha modulates survival, proliferation, and neuronal differentiation in neonatal subventricular zone cell cultures. Stem Cells 2008, 26:2361-2371.
3. Bierhaus A., Schiekofer S., Schwaninger M., Andrassy M., Humpert P.M., Chen J., Hong M., Luther T., Henle T., Kloting I., et al. Diabetes-associated sustained activation of the transcription factor nuclear factor-kappaB. Diabetes 2001, 50:2792-2808.
4. Brazel C.Y., Limke T.L., Osborne J.K., Miura T., Cai J., Pevny L., Rao M.S. Sox2 expression defines a heterogeneous population of neurosphere-forming cells in the adult murine brain. Aging Cell 2005, 4:197-207.
5. Chavakis T., Bierhaus A., Al-Fakhri N., Schneider D., Witte S., Linn T., Nagashima M., Morser J., Arnold B., Preissner K.T., 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.
6. Chen J., Li Y., Katakowski M., Chen X., Wang L., Lu D., Lu M., Gautam S.C., Chopp M. Intravenous bone marrow stromal cell therapy reduces apoptosis and promotes endogenous cell proliferation after stroke in female rat. J. Neurosci. Res. 2003, 73:778-786.
7. Chou D.K., Zhang J., Smith F.I., McCaffery P., Jungalwala F.B. Developmental expression of receptor for advanced glycation end products (RAGE), amphoterin and sulfoglucuronyl (HNK-1) carbohydrate in mouse cerebellum and their role in neurite outgrowth and cell migration. J. Neurochem. 2004, 90:1389-1401.
8. Dattilo B.M., Fritz G., Leclerc E., Kooi C.W., Heizmann C.W., Chazin W.J. The extracellular region of the receptor for advanced glycation end products is composed of two independent structural units. Biochemistry 2007, 46:6957-6970.
9. Denis-Donini S., Caprini A., Frassoni C., Grilli M. Members of the NF-kappaB family expressed in zones of active neurogenesis in the postnatal and adult mouse brain. Brain Res. Dev. Brain Res. 2005, 154:81-89.
10. Denis-Donini S., Dellarole A., Crociara P., Francese M.T., Bortolotto V., Quadrato G., Canonico P.L., Orsetti M., Ghi P., Memo M., et al. Impaired adult neurogenesis associated with short-term memory defects in NF-kappaB p50-deficient mice. J. Neurosci. 2008, 28:3911-3919.
11. Ding Q., Keller J.N. Evaluation of rage isoforms, ligands, and signaling in the brain. Biochim. Biophys. Acta 2005, 1746:18-27.
12. Fang F., Lue L.F., Yan S., Xu H., Luddy J.S., Chen D., Walker D.G., Stern D.M., Schmidt A.M., Chen J.X., et al. RAGE-dependent signaling in microglia contributes to neuroinflammation, Abeta accumulation, and impaired learning/memory in a mouse model of Alzheimer's disease. FASEB J. 2010, 24:1043-1055.
13. Geroldi D., Falcone C., Minoretti P., Emanuele E., Arra M., D'Angelo A. High levels of soluble receptor for advanced glycation end products may be a marker of extreme longevity in humans. J. Am. Geriatr. Soc. 2006, 54:1149-1150.
14. Goldstein R.S., Gallowitsch-Puerta M., Yang L., Rosas-Ballina M., Huston J.M., Czura C.J., Lee D.C., Ward M.F., Bruchfeld A.N., Wang H., et al. Elevated high-mobility group box 1 levels in patients with cerebral and myocardial ischemia. Shock 2006, 25:571-574.
15. Goshen I., Kreisel T., Ben-Menachem-Zidon O., Licht T., Weidenfeld J., Ben-Hur T., Yirmiya R. Brain interleukin-1 mediates chronic stress-induced depression in mice via adrenocortical activation and hippocampal neurogenesis suppression. Mol. Psychiatry 2008, 13:717-728.
16. Graham V., Khudyakov J., Ellis P., Pevny L. SOX2 functions to maintain neural progenitor identity. Neuron 2003, 39:749-765.
17. Grilli M., Chiu J.J., Lenardo M.J. NF-kappa B and Rel: participants in a multiform transcriptional regulatory system. Int. Rev. Cytol. 1993, 143:1-62.
18. Grilli M., Memo M. Nuclear factor-kappaB/Rel proteins: a point of convergence of signalling pathways relevant in neuronal function and dysfunction. Biochem. Pharmacol. 1999, 57:1-7.
19. Hassid B.G., Nair M.N., Ducruet A.F., Otten M.L., Komotar R.J., Pinsky D.J., Schmidt A.M., Yan S.F., Connolly E.S. Neuronal RAGE expression modulates severity of injury following transient focal cerebral ischemia. J. Clin. Neurosci. 2009, 16:302-306.
20. Hudson B.I., Carter A.M., Harja E., Kalea A.Z., Arriero M., Yang H., Grant P.J., Schmidt A.M. Identification, classification, and expression of RAGE gene splice variants. FASEB J. 2008, 22:1572-1580.
21. Huttunen H.J., Fages C., Rauvala H. Receptor for advanced glycation end products (RAGE)-mediated neurite outgrowth and activation of NF-kappaB require the cytoplasmic domain of the receptor but different downstream signaling pathways. J. Biol. Chem. 1999, 274:19919-19924.
22. 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 receptor for advanced glycation end products (RAGE) activation. J. Biol. Chem. 2000, 275:40096-40105.
23. Iosif R.E., Ekdahl C.T., Ahlenius H., Pronk C.J., Bonde S., Kokaia Z., Jacobsen S.E., Lindvall O. Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J. Neurosci. 2006, 26:9703-9712.
24. Jackson E.L., Garcia-Verdugo J.M., Gil-Perotin S., Roy M., Quinones-Hinojosa A., VandenBerg S., Alvarez-Buylla A. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 2006, 51:187-199.
25. Jin K., Minami M., Lan J.Q., Mao X.O., Batteur S., Simon R.P., Greenberg D.A. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:4710-4715.
26. Jin K., Wang X., Xie L., Mao X.O., Zhu W., Wang Y., Shen J., Mao Y., Banwait S., Greenberg D.A. Evidence for stroke-induced neurogenesis in the human brain. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:13198-13202.
27. Kalea A.Z., Reiniger N., Yang H., Arriero M., Schmidt A.M., Hudson B.I. Alternative splicing of the murine receptor for advanced glycation end-products (RAGE) gene. FASEB J. 2009, 23:1766-1774.
28. Kaneko N., Kudo K., Mabuchi T., Takemoto K., Fujimaki K., Wati H., Iguchi H., Tezuka H., Kanba S. Suppression of cell proliferation by interferon-alpha through interleukin-1 production in adult rat dentate gyrus. Neuropsychopharmacology 2006, 31:2619-2626.
29. Kim J.B., Sig Choi J., Yu Y.M., Nam K., Piao C.S., Kim S.W., Lee M.H., Han P.L., Park J.S., Lee J.K. HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain. J. Neurosci. 2006, 26:6413-6421.
30. Kleindienst A., McGinn M.J., Harvey H.B., Colello R.J., Hamm R.J., Bullock M.R. Enhanced hippocampal neurogenesis by intraventricular S100B infusion is associated with improved cognitive recovery after traumatic brain injury. J. Neurotrauma 2005, 22:645-655.
31. Kuhn H.G., Winkler J., Kempermann G., Thal L.J., Gage F.H. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci. 1997, 17:5820-5829.
32. Leung T.H., Hoffmann A., Baltimore D. One nucleotide in a kappaB site can determine cofactor specificity for NF-kappaB dimers. Cell 2004, 118:453-464.
33. Li J., Schmidt A.M. Characterization and functional analysis of the promoter of RAGE, the receptor for advanced glycation end products. J. Biol. Chem. 1997, 272:16498-16506.
34. Lin Y.Z., Yao S.Y., Veach R.A., Torgerson T.R., Hawiger J. Inhibition of nuclear translocation of transcription factor NF-kappa B by a synthetic peptide containing a cell membrane-permeable motif and nuclear localization sequence. J. Biol. Chem. 1995, 270:14255-14258.
35. Lois C., Alvarez-Buylla A. Long-distance neuronal migration in the adult mammalian brain. Science 1994, 264:1145-1148.
36. 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.
37. Ma L., Carter R.J., Morton A.J., Nicholson L.F. RAGE is expressed in pyramidal cells of the hippocampus following moderate hypoxic-ischemic brain injury in rats. Brain Res. 2003, 966:167-174.
38. Maczurek A., Shanmugam K., Munch G. Inflammation and the redox-sensitive AGE-RAGE pathway as a therapeutic target in Alzheimer's disease. Ann. NY Acad. Sci. 2008, 1126:147-151.
39. Manev H., Uz T., Manev R. Glia as a putative target for antidepressant treatments. J. Affect. Disord. 2003, 75:59-64.
40. Mori T., Tan J., Arendash G.W., Koyama N., Nojima Y., Town T. Overexpression of human S100B exacerbates brain damage and periinfarct gliosis after permanent focal ischemia. Stroke 2008, 39:2114-2121.
41. Muhammad S., Barakat W., Stoyanov S., Murikinati S., Yang H., Tracey K.J., Bendszus M., Rossetti G., Nawroth P.P., Bierhaus A., et al. The HMGB1 receptor RAGE mediates ischemic brain damage. J. Neurosci. 2008, 28:12023-12031.
42. Neeper M., Schmidt A.M., Brett J., Yan S.D., Wang F., Pan Y.C., Elliston K., Stern D., Shaw A. Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins. J. Biol. Chem. 1992, 267:14998-15004.
43. O'Keeffe G.C., Barker R.A., Caldwell M.A. Dopaminergic modulation of neurogenesis in the subventricular zone of the adult brain. Cell Cycle 2009, 8:2888-2894.
44. Pizzi M., Spano P. Distinct roles of diverse nuclear factor-kappaB complexes in neuropathological mechanisms. Eur. J. Pharmacol. 2006, 545:22-28.
45. Qin J., Goswami R., Dawson S., Dawson G. Expression of the receptor for advanced glycation end products in oligodendrocytes in response to oxidative stress. J. Neurosci. Res. 2008, 86:2414-2422.
46. Qiu J., Nishimura M., Wang Y., Sims J.R., Qiu S., Savitz S.I., Salomone S., Moskowitz M.A. Early release of HMGB-1 from neurons after the onset of brain ischemia. J. Cereb. Blood Flow Metab. 2008, 28:927-938.
47. Raucci A., Cugusi S., Antonelli A., Barabino S.M., Monti L., Bierhaus A., Reiss K., Saftig P., Bianchi M.E. A soluble form of 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.
48. Ridder D.A., Schwaninger M. NF-kappaB signaling in cerebral ischemia. Neuroscience 2009, 158:995-1006.
49. Riehl A., Nemeth J., Angel P., Hess J. The receptor RAGE: bridging inflammation and cancer. Cell Commun. Signal. 2009, 7:12.
50. Rolls A., Shechter R., London A., Ziv Y., Ronen A., Levy R., Schwartz M. Toll-like receptors modulate adult hippocampal neurogenesis. Nat. Cell Biol. 2007, 9:1081-1088.
51. Romanko M.J., Rola R., Fike J.R., Szele F.G., Dizon M.L., Felling R.J., Brazel C.Y., Levison S.W. Roles of the mammalian subventricular zone in cell replacement after brain injury. Prog. Neurobiol. 2004, 74:77-99.
52. Rong L.L., Gooch C., Szabolcs M., Herold K.C., Lalla E., Hays A.P., Yan S.F., Yan S.S., Schmidt A.M. RAGE: a journey from the complications of diabetes to disorders of the nervous system - striking a fine balance between injury and repair. Restor. Neurol. Neurosci. 2005, 23:355-365.
53. Rothermundt M., Peters M., Prehn J.H., Arolt V. S100B in brain damage and neurodegeneration. Microsc. Res. Tech. 2003, 60:614-632.
54. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., Weisstaub N., Lee J., Duman R., Arancio O., et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003, 301:805-809.
55. Schmidt A., Kuhla B., Bigl K., Munch G., Arendt T. Cell cycle related signaling in Neuro2a cells proceeds via the receptor for advanced glycation end products. J. Neural Transm. 2007, 114:1413-1424.
56. 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.
57. Shingo T., Sorokan S.T., Shimazaki T., Weiss S. Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells. J. Neurosci. 2001, 21:9733-9743.
58. Takuma K., Fang F., Zhang W., Yan S., Fukuzaki E., Du H., Sosunov A., McKhann G., Funatsu Y., Nakamichi N., et al. RAGE-mediated signaling contributes to intraneuronal transport of amyloid-beta and neuronal dysfunction. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:20021-20026.
59. Widera D., Mikenberg I., Elvers M., Kaltschmidt C., Kaltschmidt B. Tumor necrosis factor alpha triggers proliferation of adult neural stem cells via IKK/NF-kappaB signaling. BMC Neurosci. 2006, 7:64.
60. Winner B., Desplats P., Hagl C., Klucken J., Aigner R., Ploetz S., Laemke J., Karl A., Aigner L., Masliah E., et al. Dopamine receptor activation promotes adult neurogenesis in an acute Parkinson model. Exp. Neurol. 2009, 219:543-552.
61. Yan S.D., Chen X., Fu J., Chen M., Zhu H., Roher A., Slattery T., Zhao L., Nagashima M., Morser J., et al. RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 1996, 382:685-691.
62. Yan S.D., Stern D., Schmidt A.M. What's the RAGE? The receptor for advanced glycation end products (RAGE) and the dark side of glucose. Eur. J. Clin. Invest. 1997, 27:179-181.
63. Yan S.D., Bierhaus A., Nawroth P.P., Stern D.M. RAGE and Alzheimer's disease: a progression factor for amyloid-beta-induced cellular perturbation?. J. Alzheimers Dis. 2009, 16:833-843.
64. Zhai D.X., Kong Q.F., Xu W.S., Bai S.S., Peng H.S., Zhao K., Li G.Z., Wang D.D., Sun B., Wang J.H., et al. RAGE expression is up-regulated in human cerebral ischemia and pMCAO rats. Neurosci. Lett. 2008, 445:117-121.
65. Zimmerman G.A., Meistrell M., Bloom O., Cockroft K.M., Bianchi M., Risucci D., Broome J., Farmer P., Cerami A., Vlassara H., et al. Neurotoxicity of advanced glycation endproducts during focal stroke and neuroprotective effects of aminoguanidine. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:3744-3748.