Brain-derived neurotrophic factor reduces amyloidogenic processing through control of SORLA gene expression

Journal of Neuroscience

Volumn 29, Issue 49, 2009, Pages 15472-15478

  Rohe, Michael ^a   Synowitz, Michael ^b   Glass, Rainer ^a   Paul, Steven M ^c   Nykjaer, Anders ^d   Willnow, Thomas E ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c ELI LILLY AND COMPANY   (United States)

^d AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; SORTING PROTEIN RELATED RECEPTOR WITH A TYPE REPEATS; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CONTROLLED STUDY; DEGENERATIVE DISEASE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUNTINGTON CHOREA; IN VIVO STUDY; MOUSE; NERVE CELL; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN PROCESSING; RECEPTOR GENE; SENILE PLAQUE; TRANSCRIPTION REGULATION; WILD TYPE;

AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ANIMALS, NEWBORN; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION; HUMANS; HUNTINGTON DISEASE; MAP KINASE SIGNALING SYSTEM; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, KNOCKOUT; NEURONS; RECEPTOR, TRKB; RECEPTORS, LDL; RNA, MESSENGER;

EID: 71849109591     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3960-09.2009     Document Type: Article

References (39)

1. Akatsu H, Yamagata HD, Kawamata J, Kamino K, Takeda M, Yamamoto T, Miki T, Tooyama I, Shimohama S, Kosaka K (2006) Variations in the BDNF gene in autopsy-confirmed Alzheimer's disease and dementia with Lewy bodies in Japan. Dement Geriatr Cogn Disord 22:216-222. (Pubitemid 44310517)
2. Alonso M, Vianna MR, Depino AM, Mello e Souza T, Pereira P, Szapiro G, Viola H, Pitossi F, Izquierdo I, Medina JH (2002) BDNF-triggered events in the rat hippocampus are required for both short-and long-term memory formation. Hippocampus 12:551-560. (Pubitemid 34906483)
3. Andersen OM, Reiche J, Schmidt V, Gotthardt M, Spoelgen R, Behlke J, von Arnim CA, Breiderhoff T, Jansen P, Wu X, Bales KR, Cappai R, Masters CL, Gliemann J, Mufson EJ, Hyman BT, Paul SM, Nykjaer A, Willnow TE (2005) Neuronal sorting protein-related receptor sorLA/LR11 regulates processing of the amyloid precursor protein. Proc Natl Acad Sci U S A 102:13461-13466.
4. Bettens K, Brouwers N, Engelborghs S, De Deyn PP, Van Broeckhoven C, Sleegers K (2008) SORL1 is genetically associated with increased risk for late-onset Alzheimer disease in the Belgian population. Hum Mutat 29:769-770.
5. Böhm C, Seibel NM, Henkel B, Steiner H, Haass C, Hampe W (2006) SorLA signaling by regulated intramembrane proteolysis. J Biol Chem 281:14547-14553. (Pubitemid 43855157)
6. Bothwell M (2006) Evolution of the neurotrophin signaling system in invertebrates. Brain Behav Evol 68:124-132.
7. Chao MV (2003) Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci 4:299-309.
8. Connor B, Young D, Yan Q, Faull RL, Synek B, Dragunow M (1997) Brain-derived neurotrophic factor is reduced in Alzheimer's disease. Brain Res Mol Brain Res 49:71-81.
9. Crowley C, Spencer SD, Nishimura MC, Chen KS, Pitts-Meek S, Armanini MP, Ling LH, McMahon SB, Shelton DL, Levinson AD, Phillips HS (1994) Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76:1001-1011. (Pubitemid 24106381)
10. Desai P, Nebes R, DeKosky ST, Kamboh MI (2005) Investigation of the effect of brain-derived neurotrophic factor (BDNF) polymorphisms on the risk of late-onset Alzheimer's disease (AD) and quantitative measures of AD progression. Neurosci Lett 379:229-234. (Pubitemid 40544540)
11. Dodson SE, Gearing M, Lippa CF, Montine TJ, Levey AI, Lah JJ (2006) LR11/SorLA expression is reduced in sporadic Alzheimer disease but not in familial Alzheimer disease. J Neuropathol Exp Neurol 65:866-872.
12. Dodson SE, Andersen OM, Karmali V, Fritz JJ, Cheng D, Peng J, Levey AI, Willnow TE, Lah JJ (2008) Loss of LR11/SORLA enhances early pathology in a mouse model of amyloidosis: evidence for a proximal role in Alzheimer's disease. J Neurosci 28:12877-12886.
13. Ernfors P, Lee KF, Jaenisch R (1994) Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 368:147-150. (Pubitemid 24101525)
14. Ferrer I, Goutan E, Marín C, Rey MJ, Ribalta T (2000) Brain-derived neurotrophic factor in Huntington disease. Brain Res 866:257-261. (Pubitemid 30313028)
15. Games D, Adams D, Alessandrini R, Barbour R, Berthelette P, Blackwell C, Carr T, Clemens J, Donaldson T, Gillespie F, Guido T, Hagopian S, Johnson-Wood K, Khan K, Lee M, Leibowitz P, Lieberburg I, Little S, Masliah E, McConlogue L, et al. (1995) Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein. Nature 373:523-527.
16. Ge YW, Lahiri DK (2002) Regulation of promoter activity of the APP gene by cytokines and growth factors: implications in Alzheimer's disease. Ann N Y Acad Sci 973:463-467.
17. Hall J, Thomas KL, Everitt BJ (2000) Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat Neurosci 3:533-535. (Pubitemid 30332069)
18. Howells DW, Porritt MJ, Wong JY, Batchelor PE, Kalnins R, Hughes AJ, Donnan GA (2000) Reduced BDNF mRNA expression in the Parkinson's disease substantia nigra. Exp Neurol 166:127-135. (Pubitemid 30824299)
19. Knusel B, Gao H, Okazaki T, Yoshida T, Mori N, Hefti F, Kaplan DR (1997) Ligand-induced down-regulation of Trk messenger RNA, protein and tyrosine phosphorylation in rat cortical neurons. Neuroscience 78:851-862. (Pubitemid 27179664)
20. Lee JH, Chulikavit M, Pang D, Zigman WB, Silverman W, Schupf N (2007) Association between genetic variants in sortilin-related receptor 1 (SORL1) and Alzheimer's disease in adults with Down syndrome. Neurosci Lett 425:105-109. (Pubitemid 47410369)
21. Linnarsson S, Björklund A, Ernfors P (1997) Learning deficit in BDNF mutant mice. Eur J Neurosci 9:2581-2587. (Pubitemid 28082947)
22. Matrone C, Ciotti MT, Mercanti D, Marolda R, Calissano P (2008) NGF and BDNF signaling control amyloidogenic route and Abeta production in hippocampal neurons. Proc Natl Acad Sci U S A 105:13139-13144.
23. Nagahara AH, Merrill DA, Coppola G, Tsukada S, Schroeder BE, Shaked GM, Wang L, Blesch A, Kim A, Conner JM, Rockenstein E, Chao MV, Koo EH, Geschwind D, Masliah E, Chiba AA, Tuszynski MH (2009) Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer's disease. Nat Med 15:331-337.
24. Narisawa-Saito M, Wakabayashi K, Tsuji S, Takahashi H, Nawa H (1996) Regional specificity of alterations in NGF, BDNF and NT-3 levels in Alzheimer's disease. Neuroreport 7:2925-2928.
25. Nyborg AC, Ladd TB, Zwizinski CW, Lah JJ, Golde TE (2006) Sortilin, SorCS1b, and SorLA Vps10p sorting receptors, are novel gamma-secretase substrates. Mol Neurodegener 1:3.
26. Offe K, Dodson SE, Shoemaker JT, Fritz JJ, Gearing M, Levey AI, Lah JJ (2006) The lipoprotein receptor LR11 regulates amyloid beta production and amyloid precursor protein traffic in endosomal compartments. J Neurosci 26:1596-1603. (Pubitemid 43237030)
27. Reichardt LF (2006) Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 361:1545-1564.
28. Rogaeva E, Meng Y, Lee JH, Gu Y, Kawarai T, Zou F, Katayama T, Baldwin CT, Cheng R, Hasegawa H, Chen F, Shibata N, Lunetta KL, Pardossi- Piquard R, Bohm C, Wakutani Y, Cupples LA, Cuenco KT, Green RC, Pinessi L, et al. (2007) The neuronal sortilin-related receptor SORL1 is genetically associated with Alzheimer disease. Nat Genet 39:168-177.
29. Rohe M, Carlo AS, Breyhan H, Sporbert A, Militz D, Schmidt V, Wozny C, Harmeier A, Erdmann B, Bales KR, Wolf S, Kempermann G, Paul SM, Schmitz D, Bayer TA, Willnow TE, Andersen OM (2008) Sortilinrelated receptor with A-type repeats (SORLA) affects the amyloid precursor protein-dependent stimulation of ERK signaling and adult neurogenesis. J Biol Chem 283:14826-14834.
30. Ruiz-León Y, Pascual A (2004) Regulation of beta-amyloid precursor protein expression by brain-derived neurotrophic factor involves activation of both the Ras and phosphatidylinositide 3-kinase signalling pathways. J Neurochem 88:1010-1018.
31. Scherzer CR, Offe K, Gearing M, Rees HD, Fang G, Heilman CJ, Schaller C, Bujo H, Levey AI, Lah JJ (2004) Loss of apolipoprotein E receptor LR11 in Alzheimer disease. Arch Neurol 61:1200-1205. (Pubitemid 39062672)
32. Schilling G, Becher MW, Sharp AH, Jinnah HA, Duan K, Kotzuk JA, Slunt HH, Ratovitski T, Cooper JK, Jenkins NA, Copeland NG, Price DL, Ross CA, Borchelt DR (1999) Intranuclear inclusions and neuritic aggregates in transgenic mice expressing a mutant N-terminal fragment of huntingtin. Hum Mol Genet 8:397-407. (Pubitemid 29097327)
33. Schindowski K, Belarbi K, Buée L (2008) Neurotrophic factors in Alzheimer's disease: role of axonal transport. Genes Brain Behav 7 [Suppl 1]:43-56.
34. Schmidt V, Sporbert A, Rohe M, Reimer T, Rehm A, Andersen OM, Willnow TE (2007) SorLA/LR11 regulates processing of amyloid precursor protein via interaction with adaptors GGA and PACS-1. J Biol Chem 282:32956-32964. (Pubitemid 350159299)
35. Siegel GJ, Chauhan NB (2000) Neurotrophic factors in Alzheimer's and Parkinson's disease brain. Brain Res Brain Res Rev 33:199-227. (Pubitemid 30697036)
36. Spires TL, Grote HE, Varshney NK, Cordery PM, van Dellen A, Blakemore C, Hannan AJ (2004) Environmental enrichment rescues protein deficits in a mouse model of Huntington's disease, indicating a possible disease mechanism. J Neurosci 24:2270-2276. (Pubitemid 38314558)
37. Tapia-Arancibia L, Aliaga E, Silhol M, Arancibia S (2008) New insights into brain BDNF function in normal aging and Alzheimer disease. Brain Res Rev 59:201-220.
38. Willnow TE, Petersen CM, Nykjaer A (2008) VPS10P-domain receptors - regulators of neuronal viability and function. Nat Rev Neurosci 9:899-909.
39. Zuccato C, Ciammola A, Rigamonti D, Leavitt BR, Goffredo D, Conti L, MacDonald ME, Friedlander RM, Silani V, Hayden MR, Timmusk T, Sipione S, Cattaneo E (2001) Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science 293:493-498. (Pubitemid 32679077)