Alzheimer amyloid peptide Aβ42 regulates gene expression of transcription and growth factors

Journal of Alzheimer's Disease

Volumn 44, Issue 2, 2015, Pages 613-624

  Barucker, Christian ^a,b   Sommer, Anette ^c   Beckmann, Georg ^c   Eravci, Murat ^a   Harmeier, Anja ^a,i   Schipke, Carola G ^d   Brockschnieder, Damian ^c   Dyrks, Thomas ^c   Althoff, Veit ^a   Fraser, Paul E ^e   Hazrati, Lili Naz ^f   George Hyslop, Peter St ^e   Breitner, John C S ^g,h   Peters, Oliver ^d   Multhaup, Gerhard ^a,b  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b MCGILL UNIVERSITY   (Canada)

^c BAYER PHARMA AG   (Germany)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e UNIVERSITY OF TORONTO   (Canada)

^f UNIVERSITY OF TORONTO   (Canada)

^g DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^h MCGILL UNIVERSITY   (Canada)

ⁱ F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

Alzheimer's disease; amyloid ; CSF proteomics; gene regulation; ID1 3; IGFBP; immunohistochemistry; LMO4; transcription factors

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; GROWTH FACTOR; INHIBITOR OF DIFFERENTIATION 1; INHIBITOR OF DIFFERENTIATION 2; LIM HOMEODOMAIN PROTEIN; LIM HOMEODOMAIN PROTEIN 4; MESSENGER RNA; REGULATOR PROTEIN; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN BINDING PROTEIN 5; TAU PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA-PROTEIN (1-42); IGFBP3 PROTEIN, HUMAN; PEPTIDE FRAGMENT;

ADULT; ALZHEIMER DISEASE; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DNA BINDING; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MINI MENTAL STATE EXAMINATION; MOUSE; NEUROBLASTOMA CELL; NEUROTOXICITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN CEREBROSPINAL FLUID LEVEL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ZINC FINGER MOTIF; ANIMAL; BRAIN CORTEX; CEREBROSPINAL FLUID; GENE EXPRESSION REGULATION; GENETICS; HIPPOCAMPUS; METABOLISM; MICROARRAY ANALYSIS; PHYSIOLOGY; PSYCHOLOGICAL RATING SCALE; REAL TIME POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; TUMOR CELL LINE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; CELL LINE, TUMOR; CEREBRAL CORTEX; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 3; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 5; MICE, TRANSGENIC; MICROARRAY ANALYSIS; PEPTIDE FRAGMENTS; PSYCHIATRIC STATUS RATING SCALES; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84921526788     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-141902     Document Type: Article

References (55)

1. Zhao LN, Long H, Mu Y, Chew LY (2012) The toxicity of amyloid beta oligomers. Int J Mol Sci 13, 7303-7327.
2. Sperling RA, Jack CR Jr., Black SE, Frosch MP, Greenberg SM, Hyman BT, Scheltens P, Carrillo MC, Thies W, Bednar MM, Black RS, Brashear HR, Grundman M, Siemers ER, Feldman HH, Schindler RJ (2011) Amyloid-related imaging abnormalities in amyloid-modifying therapeutic trials: Recommendations from the Alzheimer's Association Research Roundtable Workgroup. Alzheimers Dement 7, 367-385.
3. Jack CR Jr., Knopman DS, Jagust WJ, Shaw LM, Aisen PS, Weiner MW, Petersen RC, Trojanowski JQ (2010) Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade. Lancet Neurol 9, 119-128.
4. Jack CR Jr., Knopman DS, Jagust WJ, Petersen RC, Weiner MW, Aisen PS, Shaw LM, Vemuri P,Wiste HJ,Weigand SD, Lesnick TG, Pankratz VS, Donohue MC, Trojanowski JQ (2013) Tracking pathophysiological processes in Alzheimer's disease: An updated hypothetical model of dynamic biomarkers. Lancet Neurol 12, 207-216.
5. Harmeier A, Wozny C, Rost BR, Munter LM, Hua H, Georgiev O, Beyermann M, Hildebrand PW, Weise C, SchaffnerW, Schmitz D, MulthaupG(2009) Role of amyloidbeta glycine 33 in oligomerization, toxicity, and neuronal plasticity. J Neurosci 29, 7582-7590.
6. Kaden D, Harmeier A, Weise C, Munter LM, Althoff V, Rost BR, Hildebrand PW, Schmitz D, Schaefer M, Lurz R, Skodda S,Yamamoto R, Arlt S, Finckh U, MulthaupG(2012) Novel APP/Abeta mutation K16N produces highly toxic heteromeric Abeta oligomers. EMBO Mol Med 4, 647-659.
7. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, Glabe CG (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489.
8. McLean CA, Cherny RA, Fraser FW, Fuller SJ, Smith MJ, Beyreuther K, Bush AI, Masters CL (1999) Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol 46, 860-866.
9. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539.
10. Gouras GK, Tsai J, Naslund J,Vincent B, Edgar M, Checler F, Greenfield JP, Haroutunian V, Buxbaum JD, Xu H, Greengard P, Relkin NR (2000) Intraneuronal Abeta42 accumulation in human brain. Am J Pathol 156, 15-20.
11. Takahashi RH, Capetillo-Zarate E, Lin MT, Milner TA, Gouras GK (2013) Accumulation of intraneuronal betaamyloid 42 peptides is associated with early changes in microtubule-associated protein 2 in neurites and synapses. PLoS One 8, e51965.
12. Wirths O, Multhaup G, Czech C, Blanchard V, Moussaoui S, Tremp G, Pradier L, Beyreuther K, Bayer TA (2001) Intraneuronal Abeta accumulation precedes plaque formation in beta-amyloid precursor protein and presenilin-1 doubletransgenic mice. Neurosci Lett 306, 116-120.
13. Barucker C, Harmeier A, Weiske J, Fauler B, Albring KF, Prokop S, Hildebrand P, Lurz R, Heppner FL, Huber O, Multhaup G (2014) Nuclear translocation uncovers the amyloid peptide Abeta42 as a regulator of gene transcription. J Biol Chem 289, 20182-20191.
14. Bailey JA, Maloney B, Ge YW, Lahiri DK (2011) Functional activity of the novel Alzheimer's amyloid beta-peptide interacting domain (AbetaID) in the APP and BACE1 promoter sequences and implications in activating apoptotic genes and in amyloidogenesis. Gene 488, 13-22.
15. Maloney B, Lahiri DK (2011) The Alzheimer's amyloid beta-peptide (Abeta) binds a specific DNA Abeta-interacting domain (AbetaID) in the APP, BACE1, and APOE promoters in a sequence-specific manner: Characterizing a new regulatory motif. Gene 488, 1-12.
16. Chishti MA,Yang DS, Janus C, Phinney AL, Horne P, Pearson J, Strome R, Zuker N, Loukides J, French J, Turner S, Lozza G, Grilli M, Kunicki S, Morissette C, Paquette J, Gervais F, Bergeron C, Fraser PE, Carlson GA, George-Hyslop PS, Westaway D (2001) Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J Biol Chem 276, 21562-21570.
17. Schipke CG, Prokop S, Heppner FL, Heuser I, Peters O(2011) Comparison of immunosorbent assays for the quantification of biomarkers for Alzheimer's disease in human cerebrospinal fluid. Dement Geriatr Cogn Disord 31, 139-145.
18. Rappsilber J, Mann M, Ishihama Y (2007) Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc 2, 1896-1906.
19. Dawid IB, Breen JJ, Toyama R (1998) LIM domains: Multiple roles as adapters and functional modifiers in protein interactions. Trends Genet 14, 156-162.
20. Mao S, Neale GA, Goorha RM (1997) T-cell proto-oncogene rhombotin-2 is a complex transcription regulator containing multiple activation and repression domains. J Biol Chem 272, 5594-5599.
21. Vu D, Marin P, Walzer C, Cathieni MM, Bianchi EN, Saidji F, Leuba G, Bouras C, Savioz A (2003) Transcription regulator LMO4 interferes with neuritogenesis in human SH-SY5Y neuroblastoma cells. Brain Res Mol Brain Res 115, 93-103.
22. Ono Y, Gnocchi VF, Zammit PS, Nagatomi R (2009) Presenilin-1 acts via Id1 to regulate the function of muscle satellite cells in a gamma-secretase-independent manner. J Cell Sci 122, 4427-4438.
23. Guerreiro R, Wojtas A, Bras J, Carrasquillo M, Rogaeva E, Majounie E, Cruchaga C, Sassi C, Kauwe JS, Younkin S, Hazrati L, Collinge J, Pocock J, Lashley T, Williams J, Lambert JC, Amouyel P, Goate A, Rademakers R, Morgan K, Powell J, St George-Hyslop P, Singleton A, Hardy J (2013) TREM2 variants in Alzheimer's disease. N Engl J Med 368, 117-127.
24. Blalock EM, Geddes JW, Chen KC, Porter NM, Markesbery WR, Landfield PW (2004) Incipient Alzheimer's disease: Microarray correlation analyses reveal major transcriptional and tumor suppressor responses. Proc Natl Acad Sci U S A 101, 2173-2178.
25. Agbemenyah HY, Agis-Balboa RC, Burkhardt S, Delalle I, Fischer A (2013) Insulin growth factor binding protein 7 is a novel target to treat dementia. Neurobiol Dis 62C 135-143.
26. Johansson P, Aberg D, Johansson JO, Mattsson N, Hansson O, Ahren B, Isgaard J, Aberg ND, Blennow K, Zetterberg H, Wallin A, Svensson J (2013) Serum but not cerebrospinal fluid levels of insulin-like growth factor-I (IGF-I) and IGF-binding protein-3 (IGFBP-3) are increased in Alzheimer's disease. Psychoneuroendocrinology 38, 1729-1737.
27. Bassil F, Fernagut PO, Bezard E, Meissner WG (2014) Insulin, IGF-1 and GLP-1 signaling in neurodegenerative disorders: Targets for disease modification? Prog Neurobiol 118, 1-18.
28. Bossers K, Wirz KT, Meerhoff GF, Essing AH, van Dongen JW, Houba P, Kruse CG, Verhaagen J, Swaab DF (2010) Concerted changes in transcripts in the prefrontal cortex precede neuropathology in Alzheimer's disease. Brain 133, 3699-3723.
29. Dudek H, Datta SR, Franke TF, Birnbaum MJ, Yao R, Cooper GM, Segal RA, Kaplan DR, Greenberg ME (1997) Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 275, 661-665.
30. Russo VC, Gluckman PD, Feldman EL, Werther GA (2005) The insulin-like growth factor system and its pleiotropic functions in brain. Endocr Rev 26, 916-943.
31. Duan C, Xu Q (2005) Roles of insulin-like growth factor (IGF) binding proteins in regulating IGF actions. Gen Comp Endocrinol 142, 44-52.
32. Uberti D, Cenini G, Bonini SA, Barcikowska M, Styczynska M, Szybinska A, Memo M (2010) Increased CD44 gene expression in lymphocytes derived from Alzheimer disease patients. Neurodegener Dis 7, 143-147.
33. Lammich S, Okochi M, Takeda M, Kaether C, Capell A, Zimmer AK, Edbauer D, Walter J, Steiner H, Haass C (2002) Presenilin-dependent intramembrane proteolysis of CD44 leads to the liberation of its intracellular domain and the secretion of an Abeta-like peptide. J Biol Chem 277, 44754-44759.
34. O'Callaghan P, Sandwall E, Li JP, Yu H, Ravid R, Guan ZZ, van Kuppevelt TH, Nilsson LN, Ingelsson M, Hyman BT, Kalimo H, Lindahl U, Lannfelt L, Zhang X (2008) Heparan sulfate accumulation with Abeta deposits in Alzheimer's disease and Tg2576 mice is contributed by glial cells. Brain Pathol 18, 548-561.
35. van Horssen J, Otte-Holler I, David G, Maat-Schieman ML, van den Heuvel LP, Wesseling P, de Waal RM, Verbeek MM(2001) Heparan sulfate proteoglycan expression in cerebrovascular amyloid beta deposits in Alzheimer's disease and hereditary cerebral hemorrhage with amyloidosis (Dutch) brains. Acta Neuropathol 102, 604-614.
36. Chin J, Massaro CM, Palop JJ, Thwin MT, Yu GQ, Bien-Ly N, Bender A, Mucke L (2007) Reelin depletion in the entorhinal cortex of human amyloid precursor protein transgenic mice and humans with Alzheimer's disease. J Neurosci 27, 2727-2733.
37. Hoe HS, Lee KJ, Carney RS, Lee J, Markova A, Lee JY, Howell BW, Hyman BT, Pak DT, Bu G, Rebeck GW (2009) Interaction of reelin with amyloid precursor protein promotes neurite outgrowth. J Neurosci 29, 7459-7473.
38. Pujadas L, Rossi D, Andres R, Teixeira CM, Serra-Vidal B, Parcerisas A, Maldonado R, Giralt E, Carulla N, Soriano E (2014) Reelin delays amyloid-beta fibril formation and rescues cognitive deficits in a model of Alzheimer's disease. Nat Commun 5, 3443.
39. Bateman RJ, Xiong C, Benzinger TL, Fagan AM, Goate A, Fox NC, Marcus DS, Cairns NJ, Xie X, Blazey TM, Holtzman DM, Santacruz A, Buckles V, Oliver A,Moulder K, Aisen PS, Ghetti B, Klunk WE, McDade E, Martins RN, Masters CL, Mayeux R, Ringman JM, Rossor MN, Schofield PR, Sperling RA, Salloway S, Morris JC (2012) Clinical and biomarker changes in dominantly inherited Alzheimer's disease. N Engl J Med 367, 795-804.
40. Villemagne VL, Burnham S, Bourgeat P, Brown B, Ellis KA, Salvado O, Szoeke C, Macaulay SL, Martins R, Maruff P, Ames D, Rowe CC, Masters CL (2013) Amyloid beta deposition, neurodegeneration, and cognitive decline in sporadic Alzheimer's disease:Aprospective cohort study. Lancet Neurol 12, 357-367.
41. Benilova I, Karran E, De Strooper B (2012) The toxic Abeta oligomer and Alzheimer's disease: An emperor in need of clothes. Nat Neurosci 15, 349-357.
42. Welander H, Franberg J, Graff C, Sundstrom E, Winblad B, Tjernberg LO (2009) Abeta43 is more frequent than Abeta40 in amyloid plaque cores from Alzheimer disease brains. J Neurochem 110, 697-706.
43. Stephan A, Laroche S, Davis S (2001) Generation of aggregated beta-amyloid in the rat hippocampus impairs synaptic transmission and plasticity and causes memory deficits. J Neurosci 21, 5703-5714.
44. Fraser PE, Duffy LK, O'Malley MB, Nguyen J, Inouye H, Kirschner DA (1991) Morphology and antibody recognition of synthetic beta-amyloid peptides. J Neurosci Res 28, 474-485.
45. Leuba G, Vernay A, Vu D, Walzer C, Belloir B, Kraftsik R, Bouras C, Savioz A (2004) Differential expression of LMO4 protein in Alzheimer's disease. Neuropathol Appl Neurobiol 30, 57-69.
46. Kaltschmidt B, Uherek M, Volk B, Baeuerle PA, Kaltschmidt C (1997) Transcription factor NF-kappaB is activated in primary neurons by amyloid beta peptides and in neurons surrounding early plaques from patients with Alzheimer disease. Proc Natl Acad Sci U S A 94, 2642-2647.
47. Pastorcic M, Das HK (2003) Ets transcription factors ER81 and Elk1 regulate the transcription of the human presenilin 1 gene promoter. Brain Res Mol Brain Res 113, 57-66.
48. Sebollela A, Freitas-Correa L, Oliveira FF, Paula-Lima AC, Saraiva LM, Martins SM, Mota LD, Torres C, Alves-Leon S, de Souza JM, Carraro DM, Brentani H, De Felice FG, Ferreira ST (2012) Amyloid-beta oligomers induce differential gene expression in adult human brain slices. J BiolChem287, 7436-7445.
49. Zhao WQ, De Felice FG, Fernandez S, Chen H, Lambert MP, Quon MJ, Krafft GA, Klein WL (2008) Amyloid beta oligomers induce impairment of neuronal insulin receptors. FASEB J 22, 246-260.
50. Liu X, Teng Z, Cui C, Wang R, Liu M, Zhang Y (2014) Amyloid beta-derived diffusible ligands (ADDLs) induce abnormal expression of insulin receptors in rat hippocampal neurons. J Mol Neurosci 52, 124-130.
51. Piriz J, Muller A, Trejo JL, Torres-Aleman I (2011) IGF-I and the aging mammalian brain. Exp Gerontol 46, 96-99.
52. Araki W, Kume H, Oda A, Tamaoka A, Kametani F (2009) IGF-1 promotes beta-amyloid production by a secretaseindependent mechanism. Biochem Biophys Res Commun 380, 111-114.
53. Freude S, Hettich MM,Schumann C, Stohr O,Koch L,Kohler C, Udelhoven M, Leeser U, Muller M, Kubota N, Kadowaki T, Krone W, Schroder H, Bruning JC, Schubert M (2009) Neuronal IGF-1 resistance reduces Abeta accumulation and protects against premature death in a model of Alzheimer's disease. FASEB J 23, 3315-3324.
54. Duron E, Funalot B, Brunel N, Coste J, Quinquis L, Viollet C, Belmin J, Jouanny P, Pasquier F, Treluyer JM, Epelbaum J, le Bouc Y, Hanon O (2012) Insulin-like growth factor-I and insulin-like growth factor binding protein-3 in Alzheimer's disease. J Clin Endocrinol Metab 97, 4673-4681.
55. Salehi Z, Mashayekhi F, Naji M (2008) Insulin like growth factor-1 and insulin like growth factor binding proteins in the cerebrospinal fluid and serum from patients with Alzheimer's disease. Biofactors 33, 99-106.