Precursor form of brain-derived neurotrophic factor and mature brain-derived neurotrophic factor are decreased in the pre-clinical stages of Alzheimer's disease

Journal of Neurochemistry

Volumn 93, Issue 6, 2005, Pages 1412-1421

  Peng, Shiyong ^a   Wuu, Joanne ^b   Mufson, Elliott J ^b   Fahnestock, Margaret ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Brain derived neurotrophic factor; Mild cognitive impairment; Neurotrophin; Parietal cortex; Precursor form of brain derived neurotrophic factor; Western blotting

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CHOLINE ACETYLTRANSFERASE; MESSENGER RNA; PROTEIN; PROTEIN PRECURSOR;

AGED; ALZHEIMER DISEASE; ARTICLE; CELL FUNCTION; CELL SURVIVAL; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE COURSE; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MINI MENTAL STATE EXAMINATION; NERVE CELL; NERVE DEGENERATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SCORING SYSTEM; SYNAPTIC MEMBRANE;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; BIOLOGICAL MARKERS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DEATH; CELL SURVIVAL; COGNITION DISORDERS; DISEASE PROGRESSION; DOWN-REGULATION; FEMALE; HUMANS; MALE; NERVE DEGENERATION; NEURONS; NEUROPSYCHOLOGICAL TESTS; PARIETAL LOBE; PROTEIN PRECURSORS;

EID: 20744434559     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03135.x     Document Type: Article

References (69)

1. Alderson R. F., Alterman A. L., Barde Y. A. and Lindsay R. M. (1990) Brain-derived neurotrophic factor increases survival and differentiated functions of rat septal cholinergic neurons in culture. Neuron 5, 297-306.
2. Ando S., Kobayashi S., Waki H. et al. (2002) Animal model of dementia induced by entorhinal synaptic damage and partial restoration of cognitive deficits by BDNF and carnitine. J. Neurosci. Res. 70, 519-527.
3. Barbacid M. (1995) Neurotrophic factors and their receptors. Curr. Opin. Cell Biol. 7, 148-155.
4. Bartoletti A., Cancedda L., Reid S. W., Tessarollo L., Porciatti V., Pizzorusso T. and Maffei L. (2002) Heterozygous knock-out mice for brain-derived neurotrophic factor show a pathway-specific impairment of long-term potentiation but normal critical period for monocular deprivation. J. Neurosci. 22, 10 072-10 077.
5. Bartus R. T., Dean R. L. III, Beer B. and Lippa A. S. (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217, 408-414.
6. Behrmann M., Geng J. J. and Shomstein S. (2004) Parietal cortex and attention. Curr. Opin. Neurobiol. 14, 212-217.
7. Bennett D. A., Wilson R. S., Schneider J. A., Evans D. A., Beckett L. A., Aggarwal N. T., Barnes L. L., Fox J. H. and Bach J. (2002) Natural history of mild cognitive impairment in older persons. Neurology 59, 198-205.
8. Braak H. and Braak E. (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. (Berl.) 82, 239-259.
9. Broad K. D., Mimmack M. L., Keverne E. B. and Kendrick K. M. (2002) Increased BDNF and trk-B mRNA expression in cortical and limbic regions following formation of a social recognition memory. Eur. J. Neurosci. 16, 2166-2174.
10. Chen Z. Y., Patel P. D., Sant G., Meng C. X., Teng K. K., Hempstead B. L. and Lee F. S. (2004) Variant brain-derived neurotrophic factor (BDNF) (Met66) alters the intracellular trafficking and activity-dependent secretion of wild-type BDNF in neurosecretory cells and cortical neurons. J. Neurosci. 24, 4401-4411.
11. Chu Y., Cochran E. J., Bennett D. A., Mufson E. J. and Kordower J. H. (2001) Down-regulation of trkA mRNA within nucleus basalis neurons in individuals with mild cognitive impairment and Alzheimer's disease. J. Comp. Neurol. 437, 296-307.
12. Connor B., Young D., Yan Q., Faull R. L., Synek B. and Dragunow M. (1997) Brain-derived neurotrophic factor is reduced in Alzheimer's disease. Brain Res. Mol. Brain Res. 49, 71-81.
13. Davies P. (1999) Challenging the cholinergic hypothesis in Alzheimer disease. JAMA 281, 1433-1434.
14. DeKosky S. T., Ikonomovic M. D., Styren S. D., Beckett L., Wisniewski S., Bennett D. A., Cochran E. J., Kordower J. H. and Mufson E. J. (2002) Upregulation of choline acetyltransferase activity in hippocampus and frontal cortex of elderly subjects with mild cognitive impairment. Ann. Neurol. 51, 145-155.
15. Fahnestock M., Michalski B., Xu B. and Coughlin M. D. (2001) The precursor pro-nerve growth factor is the predominant form of nerve growth factor in brain and is increased in Alzheimer's disease. Mol. Cell Neurosci. 18, 210-220.
16. Fahnestock M., Garzon D., Holsinger R. M. and Michalski B. (2002) Neurotrophic factors and Alzheimer's disease: are we focusing on the wrong molecule? J. Neural Transm. Suppl. 241-252.
17. Ferrer I., Marin C., Rey M. J., Ribalta T., Goutan E., Blanco R., Tolosa E. and 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.
18. Garzon D., Yu G. and 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.
19. Ghosh A., Carnahan J. and Greenberg M. E. (1994) Requirement for BDNF in activity-dependent survival of cortical neurons. Science 263, 1618-1623.
20. Giannakopoulos P., Gold G., Michel J. P. and Bouras C. (1998) Cellular vulnerability in brain aging and Alzheimer's disease. Clinical correlates and molecular background. Ann. Med. Intern. (Paris) 149, 187-191.
21. Gilmor M. L., Erickson J. D., Varoqui H., Hersh L. B., Bennett D. A., Cochran E. J., Mufson E. J. and Levey A. I. (1999) Preservation of nucleus basalis neurons containing choline acetyltransferase and the vesicular acetylcholine transporter in the elderly with mild cognitive impairment and early Alzheimer's disease. J. Comp. Neurol. 411, 693-704.
22. Goedert M. (1998) Neurofibrillary pathology of Alzheimer's disease and other tauopathies. Prog. Brain Res. 117, 287-306.
23. Gomez-Isla T., Price J. L., McKeel D. W. Jr, Morris J. C., Growdon J. H. and Hyman B. T. (1996) Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J. Neurosci. 16, 4491-4500.
24. Hariri A. R., Goldberg T. E., Mattay V. S., Kolachana B. S., Callicott J. H., Egan M. F. and Weinberger D. R. (2003) Brain-derived neurotrophic factor val66met polymorphism affects human memory-related hippocampal activity and predicts memory performance. J. Neurosci. 23, 6690-6694.
25. Hayashi M., Yamashita A. and Shimizu K. (1997) Somatostatin and brain-derived neurotrophic factor mRNA expression in the primate brain: decreased levels of mRNAs during aging. Brain Res. 749, 283-289.
26. Hedden T. and Gabrieli J. D. (2004) Insights into the ageing mind: a view from cognitive neuroscience. Nat. Rev. Neurosci. 5, 87-96.
27. Hock C., Heese K., Hulette C., Rosenberg C. and 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.
28. Holsinger R. M., Schnarr J., Henry P., Castelo V. T. and 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.
29. Horch H. W. (2004) Local effects of BDNF on dendritic growth. Rev. Neurosci. 15, 117-129.
30. Hyman B. T., Van Horsen G. W., Damasio A. R. and Barnes C. L. (1984) Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. Science 225, 1168-1170.
31. Hyman C., Hofer M., Barde Y. A., Juhasz M., Yancopoulos G. D., Squinto S. P. and Lindsay R. M. (1991) BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350, 230-232.
32. Ikonomovic M. D., Mufson E. J., Wuu J., Cochran E. J., Bennett D. A. and DeKosky S. T. (2003) Cholinergic plasticity in hippocampus of individuals with mild cognitive impairment: correlation with Alzheimer's neuropathology. J. Alzheimers Dis. 5, 39-48.
33. Johnson J. K., Vogt B. A., Kim R., Cotman C. W. and Head E. (2004) Isolated executive impairment and associated frontal neuropathology. Dement. Geriatr. Cogn. Disord. 17, 360-367.
34. Khachaturian Z. S. (2000) Toward a comprehensive theory of Alzheimer's disease - challenges, caveats, and parameters. Ann. NY Acad. Sci. 924, 184-193.
35. Knusel B., Beck K. D., Winslow J. W., Rosenthal A., Burton L. E., Widmer H. R., Nikolics K. and Hefti F. (1992) Brain-derived neurotrophic factor administration protects basal forebrain cholinergic but not nigral dopaminergic neurons from degenerative changes after axotomy in the adult rat brain. J. Neurosci. 12, 4391-4402.
36. Korte M., Kang H., Bonhoeffer T. and Schuman E. (1998) A role for BDNF in the late-phase of hippocampal long-term potentiation. Neuropharmacology 37, 553-559.
37. Lee R., Kermani P., Teng K. K. and Hempstead B. L. (2001) Regulation of cell survival by secreted proneurotrophins. Science 294, 1945-1948.
38. Levy R. (1994) Aging-associated cognitive decline. Working Party of the International Psychogeriatric Association in collaboration with the World Health Organization. Int. Psychogeriatr. 6, 63-68.
39. Lindholm D., Carroll P., Tzimagiogis G. and Thoenen H. (1996) Autocrine-paracrine regulation of hippocampal neuron survival by IGF-1 and the neurotrophins BDNF, NT-3 and NT-4. Eur. J. Neurosci. 8, 1452-1460.
40. Lindsay R. M., Wiegand S. J., Altar C. A. and DiStefano P. S. (1994) Neurotrophic factors: from molecule to man. Trends Neurosci. 17, 182-190.
41. Lowenstein D. H. and Arsenault L. (1996) The effects of growth factors on the survival and differentiation of cultured dentate gyms neurons. J. Neurosci. 16, 1759-1769.
42. Marini A. M., Jiang X., Wu X., Tian F., Zhu D., Okagaki P. and Lipsky R. H. (2004) Role of brain-derived neurotrophic factor and NF-kappaB in neuronal plasticity and survival: From genes to phenotype. Restor. Neurol. Neurosci. 22, 121-130.
43. Masliah E., Ellisman M., Carragher B., Mallory M., Young S., Hansen L., DeTeresa R. and Terry R. D. (1992) Three-dimensional analysis of the relationship between synaptic pathology and neuropil threads in Alzheimer disease. J. Neuropathol Exp. Neurol. 51, 404-414.
44. McKhann G., Drachman D., Folstein M., Katzman R., Price D. and Stadlan E. M. (1984) Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's disease. Neurology 34, 939-944.
45. Mesulam M., Shaw P., Mash D. and Weintraub S. (2004) Cholinergic nucleus basalis tauopathy emerges early in the aging-MCI-AD continuum. Ann. Neurol. 55, 815-828.
46. Michalski B. and Fahnestock M. (2003) Pro-brain-derived neurotrophic factor is decreased in parietal cortex in Alzheimer's disease. Brain Res. Mol. Brain Res. 111, 148-154.
47. Mirra S. S., Heyman A., McKeel D., Sumi S. M., Grain B. J., Brownlee L. M., Vogel F. S., Hughes J. P., van Belle G. and Berg L. (1991) The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41, 479-486.
48. Morris J. C. (2002) Challenging assumptions about Alzheimer's disease: mild cognitive impairment and the cholinergic hypothesis. Ann. Neurol. 51, 143-144.
49. Morrison J. H. and Hof P. R. (1997) Life and death of neurons in the aging brain. Science 278, 412-419.
50. Mufson E. J., Chen E. Y., Cochran E. J., Beckett L. A., Bennett D. A. and Kordower J. H. (1999) Entorhinal cortex beta-amyloid load in individuals with mild cognitive impairment. Exp. Neurol. 158, 469-490.
51. Mufson E. J., Ma S. Y., Cochran E. J., Bennett D. A., Beckett L. A., Jaffar S., Saragovi H. U. and Kordower J. H. (2000) Loss of nucleus basalis neurons containing trkA immunoreactivity in individuals with mild cognitive impairment and early Alzheimer's disease. J. Comp. Neurol. 427, 19-30.
52. Mufson E. J., Ma S. Y., Dills J. et al. (2002) Loss of basal forebrain P75(NTR) immunoreactivity in subjects with mild cognitive impairment and Alzheimer's disease. J. Comp. Neurol. 443, 136-153.
53. Mufson E. J., Ikonomovic M. D., Styren S. D., Counts S. E., Wuu J., Leurgans S., Bennett D. A., Cochran E. J. and DeKosky S. T. (2003) Preservation of brain nerve growth factor in mild cognitive impairment and Alzheimer disease. Arch. Neurol. 60, 1143-1148.
54. Narisawa-Saito M., Wakabayashi K., Tsuji S., Takahashi H. and Nawa H. (1996) Regional specificity of alterations in NGF, BDNF and NT-3 levels in Alzheimer's disease. Neuroreport 7, 2925-2928.
55. National Institute on Aging and Reagan Institute (1997) Working Group on diagnosis criteria for the neuropathological assessment of Alzheimer's disease. Consensus recommendations for the postmortem diagnosis of AD. Neurobiol. Aging 18, s1-s3.
56. Pang P. T., Teng H. K., Zaitsev E., Woo N. T., Sakata K., Zhen S., Teng K. K., Yung W. H., Hempstead B. L. and Lu B. (2004) Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 306, 487-491.
57. Peng S., Wuu J., Mufson E. J. and Fahnestock M. (2004) Increased proNGF levels in subjects with mild cognitive impairment and mild Alzheimer disease. J. Neuropathol. Exp. Neurol. 63, 641-649.
58. Perry E. K., Tomlinson B. E., Blessed G., Bergmann K., Gibson P. H. and Perry R. H. (1978) Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia. Br. Med. J. 2, 1457-1459.
59. Petersen R. C. (2000a) Aging, mild cognitive impairment, and Alzheimer's disease. Neurol. Clin. 18, 789-806.
60. Petersen R. C. (2000b) Mild cognitive impairment: transition between aging and Alzheimer's disease. Neurologia 15, 93-101.
61. Phillips H. S., Hains J. M., Armanini M., Laramee G. R., Johnson S. A. and Winslow J. W. (1991) BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer's disease. Neuron 7, 695-702.
62. Ray W. J., Ashall F. and Goate A. M. (1998) Molecular pathogenesis of sporadic and familial forms of Alzheimer's disease. Mol. Med. Today 4, 151-157.
63. Samuel W., Masliah E., Hill L. R., Butters N. and Terry R. (1994) Hippocampal connectivity and Alzheimer's dementia: effects of synapse loss and tangle frequency in a two-component model. Neurology 44, 2081-2088.
64. Terry R. D., Masliah E., Salmon D. P., Butters N., DeTeresa R., Hill R., Hansen L. A. and Katzman R. (1991) Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30, 572-580.
65. Visser P. J., Verhey F. R., Ponds R. W. and Jolles J. (2001) Diagnosis of preclinical Alzheimer's disease in a clinical setting. Int. Psychogeriatr. 13, 411-423.
66. Wakabayashi K., Honer W. G. and Masliah E. (1994) Synapse alterations in the hippocampal-entorhinal formation in Alzheimer's disease with and without Lewy body disease. Brain Res. 667, 24-32.
67. Webster M. J., Weickert C. S., Herman M. M. and Kleinman J. E. (2002) BDNF mRNA expression during postnatal development, maturation and aging of the human prefrontal cortex. Brain Res. Dev. Brain Res. 139, 139-150.
68. Whitehouse P. J., Price D. L., Struble R. G., Clark A. W., Coyle J. T. and Delon M. R. (1982) Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 215, 1237-1239.
69. Xu G., Meyer J. S., Thornby J., Chowdhury M. and Quach M. (2002) Screening for mild cognitive impairment (MCI) utilizing combined mini-mental-cognitive capacity examinations for identifying dementia prodromes. Int. J. Geriatr. Psychiat. 17, 1027-1033.