Oligomeric amyloid decreases basal levels of brain-derived neurotrophic factor (BDNF) mRNA via specific downregulation of BDNF transcripts IV and V in differentiated human neuroblastoma cells

Journal of Neuroscience

Volumn 27, Issue 10, 2007, Pages 2628-2635

  Garzon, Diego J ^a   Fahnestock, Margaret ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Alzheimer; Cell culture; CREB; Exons; Neurotrophin; Real time RT PCR

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MESSENGER RNA; OLIGOMER; RETINOIC ACID;

ALZHEIMER DISEASE; AMNESIA; ARTICLE; BRAIN FUNCTION; BRAIN NERVE CELL; CELL DIFFERENTIATION; COGNITIVE DEFECT; CONTROLLED STUDY; DOWN REGULATION; DRUG BLOOD LEVEL; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SUSTAINED RELEASE PREPARATION;

AMYLOID; AMYLOID BETA-PROTEIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DIFFERENTIATION; CELL LINE, TUMOR; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DOWN-REGULATION; HUMANS; MOLECULAR CONFORMATION; NEUROBLASTOMA; PEPTIDE FRAGMENTS; PHOSPHORYLATION; RNA, MESSENGER; TRETINOIN;

EID: 33847787591     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5053-06.2007     Document Type: Article

References (57)

1. Aoyama M, Asai K, Shishikura T, Kawamoto T, Miyachi T, Yokoi T, Togari H, Wada Y, Kato T, Nakagawara A (2001) Human neuroblastomas with unfavorable biologies express high levels of brain-derived neurotrophic factor mRNA and a variety of its variants. Cancer Lett 164:51-60.
2. Bramham CR, Messaoudi E (2005) BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog Neurobiol 76:99-125.
3. Chui DH, Tanahashi H, Ozawa K, Ikeda S, Checler F, Ueda O, Suzuki H, Araki W, Inoue H, Shirotani K, Takahashi K, Gallyas F, Tabira T (1999) Transgenic mice with Alzheimer presenilin 1 mutations show accelerated neurodegeneration without amyloid plaque formation. Nat Med 5:560-564.
4. Coleman PD, Yao PJ (2003) Synaptic slaughter in Alzheimer's disease. Neurobiol Aging 24:1023-1027.
5. 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.
6. Cummings BJ, Cotman CW (1995) Image analysis of beta-amyloid load in Alzheimer's disease and relation to dementia severity. Lancet 346:1524-1528.
7. Dahlgren KN, Manelli AM, Stine Jr WB, Baker LK, Krafft GA, LaDu MJ (2002) Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J Biol Chem 277:32046-32053.
8. Datki Z, Papp R, Zadori D, Soos K, Fulop L, Juhasz A, Laskay G, Hetenyi C, Mihalik E, Zarandi M, Penke B (2004) In vitro model of neurotoxicity of Abeta 1-42 and neuroprotection by a pentapeptide: irreversible events during the first hour. Neurobiol Dis 17:507-515.
9. Deshpande A, Mina E, Glabe C, Busciglio J (2006) Different conformations of amyloid β induce neurotoxicity by distinct mechanisms in human cortical neurons. J Neurosci 26:6011-6018.
10. Encinas M, Iglesias M, Liu Y, Wang H, Muhaisen A, Cena V, Gallego C, Comella JX (2000) Sequential treatment of SH-SY5Y cells with retinoic acid and brain-derived neurotrophic factor gives rise to fully differentiated, neurotrophic factor-dependent, human neuron-like cells. J Neurochem 75:991-1003.
11. Feng X, Jiang H, Baik JC, Edgar C, Eide FF (2001) BDNF dependence in neuroblastoma. J Neurosci Res 64:355-363.
12. Ferrer I, Marin C, Rey MJ, Ribalta T, Goutan E, Blanco R, Tolosa E, Marti E (1999) BDNF and full-length and truncated TrkB expression in Alzheimer disease. Implications in therapeutic strategies. J Neuropathol Exp Neurol 58:729-739.
13. Funato H, Enya M, Yoshimura M, Morishima-Kawashima M, Ihara Y (1999) Presence of sodium dodecyl sulfate-stable amyloid beta-protein dimers in the hippocampus CA1 not exhibiting neurofibrillary tangle formation. Am J Pathol 155:23-28.
14. Garzon D, Yu G, Fahnestock M (2002) A new brain-derived neurotrophic factor transcript and decrease in brain-derived neurotrophic factor transcripts 1, 2 and 3 in Alzheimer's disease parietal cortex. J Neurochem 82:1058-1064.
15. Geula C (1998) Abnormalities of neural circuitry in Alzheimer's disease: hippocampus and cortical cholinergic innervation. Neurology 51:S18-S29.
16. Glenner GG, Wong CW (1984) Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 120:885-890.
17. Gong Y, Chang L, Viola KL, Lacor PN, Lambert MP, Finch CE, Krafft GA, Klein WL (2003) Alzheimer's disease-affected brain: presence of oligomeric A beta ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc Natl Acad Sci USA 100:10417-10422.
18. Grundke-Iqbal I, Iqbal K, Tung YC, Quinlan M, Wisniewski HM, Binder LI (1986) Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci USA 83:4913-4917.
19. Hock C, Heese K, Hulette C, Rosenberg C, Otten U (2000) Region-specific neurotrophin imbalances in Alzheimer disease: decreased levels of brain-derived neurotrophic factor and increased levels of nerve growth factor in hippocampus and cortical areas. Arch Neurol 57:846-851.
20. Holsinger RM, Schnarr J, Henry P, Castelo VT, Fahnestock M (2000) Quantitation of BDNF mRNA in human parietal cortex by competitive reverse transcription-polymerase chain reaction: decreased levels in Alzheimer's disease. Brain Res Mol Brain Res 76:347-354.
21. Irizarry MC, Soriano F, McNamara M, Page KJ, Schenk D, Games D, Hyman BT (1997) Aβ deposition is associated with neuropil changes, but not with overt neuronal loss in the human amyloid precursor protein V717F (PDAPP) transgenic mouse. J Neurosci 17:7053-7059.
22. Kaplan DR, Matsumoto K, Lucarelli E, Thiele CJ (1993) Induction of TrkB by retinoic acid mediates biologic responsiveness to BDNF and differentiation of human neuroblastoma cells. Eukaryotic Signal Transduction Group. Neuron 11:321-331.
23. Kokaia Z, Metsis M, Kokaia M, Bengzon J, Elmer E, Smith ML, Timmusk T, Siesjo BK, Persson H, Lindvall O (1994) Brain insults in rats induce increased expression of the BDNF gene through differential use of multiple promoters. Eur J Neurosci 6:587-596.
24. Korte M, Carroll P, Wolf E, Brem G, Thoenen H, Bonhoeffer T (1995) Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci USA 92:8856-8860.
25. Lacor PN, Buniel MC, Chang L, Fernandez SJ, Gong Y, Viola KL, Lambert MP, Velasco PT, Bigio EH, Finch CE, Krafft GA, Klein WL (2004) Synaptic targeting by Alzheimer's-related amyloid β oligomers. J Neurosci 24:10191-10200.
26. Lambert MP, Stevens G, Sabo S, Barber K, Wang G, Wade W, Krafft G, Snyder S, Holzman TF, Klein WL (1994) Beta/A4-evoked degeneration of differentiated SH-SY5Y human neuroblastoma cells. J Neurosci Res 39:377-385.
27. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95:6448-6453.
28. Liu QR, Walther D, Drgon T, Polesskaya O, Lesnick TG, Strain KJ, de Andrade M, Bower JH, Maraganore DM, Uhl GR (2005) Human brain derived neurotrophic factor (BDNF) genes, splicing patterns, and assessments of associations with substance abuse and Parkinson's Disease. Am J Med Genet B Neuropsychiatr Genet 134:93-103.
29. Liu QR, Lu L, Zhu XG, Gong JP, Shaham Y, Uhl GR (2006) Rodent BDNF genes, novel promoters, novel splice variants, and regulation by cocaine. Brain Res 1067:1-12.
30. Lu B (2003) BDNF and activity-dependent synaptic modulation. Learn Mem 10:86-98.
31. Lue LF, Kuo YM, Roher AE, Brachova L, Shen Y, Sue L, Beach T, Kurth JH, Rydel RE, Rogers J (1999) Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol 155:853-862.
32. McAllister AK, Katz LC, Lo DC (1999) Neurotrophins and synaptic plasticity. Annu Rev Neurosci 22:295-318.
33. 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.
34. Metsis M, Timmusk T, Arenas E, Persson H (1993) Differential usage of multiple brain-derived neurotrophic factor promoters in the rat brain following neuronal activation. Proc Natl Acad Sci USA 90:8802-8806.
35. Naslund J, Haroutunian V, Mohs R, Davis KL, Davies P, Greengard P, Buxbaum JD (2000) Correlation between elevated levels of amyloid beta-peptide in the brain and cognitive decline. JAMA 283:1571-1577.
36. Ohara O, Gahara Y, Teraoka H, Kitamura T (1992) A rat brain-derived neurotrophic factor-encoding gene generates multiple transcripts through alternative use of 5′ exons and polyadenylation sites. Gene 121:383-386.
37. Olofsdotter K, Lindvall O, Asztely F (2000) Increased synaptic inhibition in dentate gyrus of mice with reduced levels of endogenous brain-derived neurotrophic factor. Neuroscience 101:531-539.
38. Pahlman S, Ruusala AI, Abrahamsson L, Mattsson ME, Esscher T (1984) Retinoic acid-induced differentiation of cultured human neuroblastoma cells: a comparison with phorbolester-induced differentiation. Cell Differ 14:135-144.
39. Pahlman S, Mamaeva S, Meyerson G, Mattsson ME, Bjelfman C, Ortoft E, Hammerling U (1990) Human neuroblastoma cells in culture: a model for neuronal cell differentiation and function. Acta Physiol Scand Suppl 592:25-37.
40. Patterson SL, Abel T, Deuel TA, Martin KC, Rose JC, Kandel ER (1996) Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16:1137-1145.
41. Peng S, Wuu J, Mufson EJ, Fahnestock M (2005) Precursor form of brain-derived neurotrophic factor and mature brain-derived neurotrophic factor are decreased in the pre-clinical stages of Alzheimer's disease. J Neurochem 93:1412-1421.
42. Phillips HS, Hains JM, Armanini M, Laramee GR, Johnson SA, Winslow JW (1991) BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer's disease. Neuron 7:695-702.
43. Selkoe DJ (1994) Alzheimer's disease: a central role for amyloid. J Neuropathol Exp Neurol 53:438-447.
44. Shieh PB, Hu SC, Bobb K, Timmusk T, Ghosh A (1998) Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron 20:727-740.
45. Silva AJ, Kogan JH, Frankland PW, Kida S (1998) CREB and memory. Annu Rev Neurosci 21:127-148.
46. Stine Jr WB, Dahlgren KN, Krafft GA, LaDu MJ (2003) In vitro characterization of conditions for amyloid-beta peptide oligomerization and fibrillogenesis. J Biol Chem 278:11612-11622.
47. 2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20:709-726.
48. Timmusk T, Lendahl U, Funakoshi H, Arenas E, Persson H, Metsis M (1995) Identification of brain-derived neurotrophic factor promoter regions mediating tissue-specific, axotomy-, and neuronal activity-induced expression in transgenic mice. J Cell Biol 128:185-199.
49. Tong L, Thornton PL, Balazs R, Cotman CW (2001) Beta-amyloid-(1-42) impairs activity-dependent cAMP-response element-binding protein signaling in neurons at concentrations in which cell survival Is not compromised. J Biol Chem 276:17301-17306.
50. Tong L, Balazs R, Thornton PL, Cotman CW (2004) Beta-amyloid peptide at sublethal concentrations downregulates brain-derived neurotrophic factor functions in cultured cortical neurons. J Neurosci 24:6799-6809.
51. Tully T (1998) Toward a molecular biology of memory: the light's coming on! Nat Neurosci 1:543-545.
52. Vitolo OV, Sant'Angelo A, Costanzo V, Battaglia F, Arancio O, Shelanski M (2002) Amyloid beta-peptide inhibition of the PKA/CREB pathway and long-term potentiation: reversibility by drugs that enhance cAMP signaling. Proc Natl Acad Sci USA 99:13217-13221.
53. Walsh DM, Tseng BP, Rydel RE, Podlisny MB, Selkoe DJ (2000) The oligomerization of amyloid beta-protein begins intracellularly in cells derived from human brain. Biochemistry 39:10831-10839.
54. 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.
55. Wu ZL, Ciallella JR, Flood DG, O'kane TM, Bozyczko-Coyne D, Savage MJ (2006) Comparative analysis of cortical gene expression in mouse models of Alzheimer's disease. Neurobiol Aging 27:377-386.
56. Yamamoto-Sasaki M, Ozawa H, Saito T, Rosler M, Riederer P (1999) Impaired phosphorylation of cyclic AMP response element binding protein in the hippocampus of dementia of the Alzheimer type. Brain Res 824:300-303.
57. Yuan J, Yankner BA (2000) Apoptosis in the nervous system. Nature 407:802-809.