Norepinephrine protects against amyloid-β toxicity via TrkB

Journal of Alzheimer's Disease

Volumn 44, Issue 1, 2015, Pages 251-260

  Liu, Xia ^a   Ye, Keqiang ^a   Weinshenker, David ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Amyloid ; Brain derived neurotrophic factor; Locus coeruleus; Neuroprotection; Norepinephrine; Tropomyosin related kinase B

Indexed keywords

ADRENERGIC RECEPTOR; ADRENERGIC RECEPTOR BLOCKING AGENT; ADRENERGIC RECEPTOR STIMULATING AGENT; AMYLOID BETA PROTEIN[25-35]; BRAIN DERIVED NEUROTROPHIC FACTOR; CASPASE 3; ISOPRENALINE; K 252A; NORADRENALIN; PROTEIN KINASE; TROPOMYOSIN RELATED KINASE B; UNCLASSIFIED DRUG; AMYLOID BETA PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CARBAZOLE DERIVATIVE; CASPASE; ENZYME INHIBITOR; INDOLE ALKALOID; MICROTUBULE ASSOCIATED PROTEIN; MTAP2 PROTEIN, RAT; NEUROPROTECTIVE AGENT; STAUROSPORINE AGLYCONE; TYROSINE 3 MONOOXYGENASE;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; BRAIN CELL CULTURE; CELL DEATH; CELL LYSATE; COGNITIVE DEFECT; CONTROLLED STUDY; DIMERIZATION; ENZYME ACTIVITY; HIPPOCAMPAL NEURONAL CULTURE; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; LOCUS CERULEUS; MOUSE; NERVE CELL; NEUROPATHOLOGY; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PHENOTYPE; PRIMARY CULTURE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; WESTERN BLOTTING; ANIMAL; APOPTOSIS; BRAIN; CELL COUNT; CELL CULTURE; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; NEWBORN; PHOSPHORYLATION;

ADRENERGIC AGENTS; AMYLOID BETA-PEPTIDES; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; BRAIN; CARBAZOLES; CASPASES; CELL COUNT; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; INDOLE ALKALOIDS; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; NEUROPROTECTIVE AGENTS; NOREPINEPHRINE; PHOSPHORYLATION; RATS; RECEPTOR, TRKB; TYROSINE 3-MONOOXYGENASE;

EID: 84920834210     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-141062     Document Type: Article

References (46)

1. Chalermpalanupap T, Kinkead B, Hu WT, Kummer MP, Hammerschmidt T, Heneka MT, Weinshenker D, Levey AI (2013) Targeting norepinephrine in mild cognitive impairment and Alzheimer's disease. Alzheimers Res Ther 5, 21.
2. Weinshenker D (2008) Functional consequences of locus coeruleus degeneration in Alzheimer's disease. Curr Alzheimer Res 5, 342-345.
3. Wilson RS, Nag S, Boyle PA, Hizel LP, Yu L, Buchman AS, Schneider JA, Bennett DA (2013) Neural reserve, neuronal density in the locus ceruleus, and cognitive decline. Neurology 80, 1202-1208.
4. Braak H, Del Tredici K(2012) Where, when, and in what form does sporadic Alzheimer's disease begin? Curr Opin Neurol 25, 708-714.
5. Braak H, Del Tredici K (2011) The pathological process underlying Alzheimer's disease in individuals under thirty. Acta Neuropathol 121, 171-181.
6. Braak H, Del Tredici K (2011) Alzheimer's pathogenesis: Is there neuron-to-neuron propagation? Acta Neuropathol 121, 589-595.
7. Braak H, Thal DR, Ghebremedhin E, Del Tredici K (2011) Stages of the pathologic process in Alzheimer disease: Age categories from 1 to 100 years. J Neuropathol Exp Neurol 70, 960-969.
8. Elobeid A, Soininen H, Alafuzoff I (2012) Hyperphosphorylated tau in young and middle-aged subjects. Acta Neuropathol 123, 97-104.
9. Hammerschmidt T, Kummer MP, Terwel D, Martinez A, Gorji A, Pape HC, Rommelfanger KS, Schroeder JP, Stoll M, Schultze J, Weinshenker D, Heneka MT (2013) Selective loss of noradrenaline exacerbates early cognitive dysfunction and synaptic deficits in APP/PS1 mice. Biol Psychiatry 73, 454-463.
10. Heneka MT, Nadrigny F, Regen T, Martinez-Hernandez A, Dumitrescu-Ozimek L, Terwel D, Jardanhazi-Kurutz D, Walter J, Kirchhoff F, Hanisch UK, Kummer MP (2010) Locus ceruleus controls Alzheimer's disease pathology by modulating microglial functions through norepinephrine. Proc Natl Acad Sci U S A 107, 6058-6063.
11. Heneka MT, Ramanathan M, Jacobs AH, Dumitrescu-Ozimek L, Bilkei-Gorzo A, Debeir T, Sastre M, Galldiks N, Zimmer A, Hoehn M, Heiss WD, Klockgether T, Staufenbiel M (2006) Locus ceruleus degeneration promotes Alzheimer pathogenesis in amyloid precursor protein 23 transgenic mice. J Neurosci 26, 1343-1354.
12. Kalinin S, Gavrilyuk V, Polak PE, Vasser R, Zhao J, Heneka MT, Feinstein DL (2007) Noradrenaline deficiency in brain increases beta-amyloid plaque burden in an animal model of Alzheimer's disease. Neurobiol Aging 28, 1206-1214.
13. Kalinin S, Polak PE, Lin SX, Sakharkar AJ, Pandey SC, Feinstein DL (2012) The noradrenaline precursor L-DOPS reduces pathology in a mouse model of Alzheimer's disease. Neurobiol Aging 33, 1651-1663.
14. Heneka MT, Galea E, Gavriluyk V, Dumitrescu-Ozimek L, Daeschner J, O'Banion MK, Weinberg G, Klockgether T, Feinstein DL (2002) Noradrenergic depletion potentiates beta-amyloid-induced cortical inflammation: Implications for Alzheimer's disease. J Neurosci 22, 2434-2442.
15. Klotz L, Sastre M, Kreutz A, Gavrilyuk V, Klockgether T, Feinstein DL, Heneka MT (2003) Noradrenaline induces expression of peroxisome proliferator activated receptor gamma (PPARgamma) in murine primary astrocytes and neurons. J Neurochem 86, 907-916.
16. Counts SE, Mufson EJ (2010) Noradrenaline activation of neurotrophic pathways protects against neuronal amyloid toxicity. J Neurochem 113, 649-660.
17. Traver S, Salthun-Lassalle B, Marien M, Hirsch EC, Colpaert F, Michel PP (2005) The neurotransmitter noradrenaline rescues septal cholinergic neurons in culture from degeneration caused by low-level oxidative stress. Mol Pharmacol 67, 1882-1891.
18. Troadec JD, Marien M, Darios F, Hartmann A, Ruberg M, Colpaert F, Michel PP (2001) Noradrenaline provides long-term protection to dopaminergic neurons by reducing oxidative stress. J Neurochem 79, 200-210.
19. Jhang KA, Lee EO, Kim HS, Chong YH (2014) Norepinephrine provides short-term neuroprotection against Abeta1-42 by reducing oxidative stress independent of Nrf2 activation. Neurobiol Aging. doi: 10.1016/j.neurobiolaging.2014.05.020
20. Iwasaki Y, Negishi T, Inoue M, Tashiro T, Tabira T, Kimura N (2012) Sendai virus vector-mediated brainderived neurotrophic factor expression ameliorates memory deficits and synaptic degeneration in a transgenic mouse model of Alzheimer's disease. J Neurosci Res 90, 981-989.
21. Arancibia S, Silhol M, Mouliere F, Meffre J, Hollinger I, Maurice T, Tapia-Arancibia L (2008) Protective effect of BDNF against beta-amyloid induced neurotoxicity in vitro and in vivo in rats. Neurobiol Dis 31, 316-326.
22. 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.
23. Devi L, Ohno M (2012) 7,8-dihydroxyflavone, a smallmolecule TrkB agonist, reverses memory deficits and BACE1 elevation in a mouse model of Alzheimer's disease. Neuropsychopharmacology 37, 434-444.
24. Zhang Z, Liu X, Schroeder JP, Chan CB, Song M, Yu SP, Weinshenker D, Ye K (2014) 7,8-dihydroxyflavone prevents synaptic loss and memory deficits in a mouse model of Alzheimer's disease. Neuropsychopharmacology 39, 638-650.
25. Chan CB, Liu X, Pradoldej S, Hao C, An J, Yepes M, Luo HR, Ye K (2011) Phosphoinositide 3-kinase enhancer regulates neuronal dendritogenesis and survival in neocortex. J Neurosci 31, 8083-8092.
26. Giuffrida ML, Grasso G, Ruvo M, Pedone C, Saporito A, Marasco D, Pignataro B, Cascio C, Copani A, Rizzarelli E (2007) Abeta(25-35) and its C-and/or N-blocked derivatives: Copper driven structural features and neurotoxicity. J Neurosci Res 85, 623-633.
27. Millucci L, Raggiaschi R, Franceschini D, Terstappen G, Santucci A (2009) Rapid aggregation and assembly in aqueous solution of A beta (25-35) peptide. J Biosci 34, 293-303.
28. Chen X, Ye H, Kuruvilla R, Ramanan N, Scangos KW, Zhang C, Johnson NM, England PM, Shokat KM, Ginty DD (2005) A chemical-genetic approach to studying neurotrophin signaling. Neuron 46, 13-21.
29. Bishop AC, Ubersax JA, Petsch DT, Matheos DP, Gray NS, Blethrow J, Shimizu E, Tsien JZ, Schultz PG, Rose MD, Wood JL, Morgan DO, Shokat KM (2000) A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 407, 395-401.
30. Zhang F, Kang Z, Li W, Xiao Z, Zhou X (2012) Roles of brain-derived neurotrophic factor/tropomyosin-related kinase B (BDNF/TrkB) signalling in Alzheimer's disease. J Clin Neurosci 19, 946-949.
31. Nagahara AH, Mateling M, Kovacs I, Wang L, Eggert S, Rockenstein E, Koo EH, Masliah E, Tuszynski MH (2013) Early BDNF treatment ameliorates cell loss in the entorhinal cortex of APP transgenic mice. J Neurosci 33, 15596-15602.
32. Lee FS, Chao MV (2001) Activation of Trk neurotrophin receptors in the absence of neurotrophins. Proc Natl Acad Sci U S A 98, 3555-3560.
33. Lee FS, Rajagopal R, Kim AH, Chang PC, Chao MV (2002) Activation of Trk neurotrophin receptor signaling by pituitary adenylate cyclase-activating polypeptides. J Biol Chem 277, 9096-9102.
34. Rajagopal R, Chen ZY, Lee FS, Chao MV (2004) Transactivation of Trk neurotrophin receptors by G-protein-coupled receptor ligands occurs on intracellular membranes. J Neurosci 24, 6650-6658.
35. Huang YZ, Pan E, Xiong ZQ, McNamara JO (2008) Zinc-mediated transactivation of TrkB potentiates the hippocampal mossy fiber-CA3 pyramid synapse. Neuron 57, 546-558.
36. Jang SW, Liu X, Yepes M, Shepherd KR, Miller GW, Liu Y, Wilson WD, Xiao G, Blanchi B, Sun YE, Ye K (2010) A selective TrkB agonist with potent neurotrophic activities by 7,8-dihydroxyflavone. Proc Natl Acad Sci U S A 107, 2687-2692.
37. Sieber-Blum M (1989) Inhibition of the adrenergic phenotype in cultured neural crest cells by norepinephrine uptake inhibitors. Dev Biol 136, 372-380.
38. Sieber-Blum M, Ren Z (2000) Norepinephrine transporter expression and function in noradrenergic cell differentiation. Mol Cell Biochem 212, 61-70.
39. Zhang JM, Dix J, Langtimm-Sedlak CJ, Trusk T, Schroeder B, Hoffmann R, Strosberg AD, Winslow JW, Sieber-BlumM (1997) Neurotrophin-3-and norepinephrine-mediated adrenergic differentiation and the inhibitory action of desipramine and cocaine. J Neurobiol 32, 262-280.
40. Holm PC, Rodriguez FJ, Kresse A, Canals JM, Silos-Santiago I, Arenas E (2003) Crucial role of TrkB ligands in the survival and phenotypic differentiation of developing locus coeruleus noradrenergic neurons. Development 130, 3535-3545.
41. Smith MA, Makino S, Altemus M, Michelson D, Hong SK, Kvetnansky R, Post RM (1995) Stress and antidepressants differentially regulate neurotrophin 3mRNAexpression in the locus coeruleus. Proc Natl Acad Sci U S A 92, 8788-8792.
42. Numan S, Lane-Ladd SB, Zhang L, Lundgren KH, Russell DS, Seroogy KB, Nestler EJ (1998) Differential regulation of neurotrophin and trk receptor mRNAs in catecholaminergic nuclei during chronic opiate treatment and withdrawal. J Neurosci 18, 10700-10708.
43. Alonso-Vanegas MA, Fawcett JP, Causing CG, Miller FD, Sadikot AF (1999) Characterization of dopaminergic midbrain neurons in a DBH:BDNF transgenic mouse. J Comp Neurol 413, 449-462.
44. Fawcett JP, Bamji SX, Causing CG, Aloyz R, Ase AR, Reader TA, McLean JH, Miller FD (1998) Functional evidence that BDNF is an anterograde neuronal trophic factor in the CNS. J Neurosci 18, 2808-2821.
45. Luellen BA, Bianco LE, Schneider LM, Andrews AM (2007) Reduced brain-derived neurotrophic factor is associated with a loss of serotonergic innervation in the hippocampus of aging mice. Genes Brain Behav 6, 482-490.
46. Matsunaga W, Shirokawa T, Isobe K (2004) BDNF is necessary for maintenance of noradrenergic innervations in the aged rat brain. Neurobiol Aging 25, 341-348.