Down regulation of trk but not p75NTR gene expression in single cholinergic basal forebrain neurons mark the progression of Alzheimer's disease

Journal of Neurochemistry

Volumn 97, Issue 2, 2006, Pages 475-487

  Ginsberg, Stephen D ^a   Che, Shaoli ^a   Wuu, Joanne ^b   Counts, Scott E ^b   Mufson, Elliott J ^b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Microarray; Mild cognitive impairment; Neurotrophin; Nucleus basalis; RNA amplification; trkA

Indexed keywords

NERVE GROWTH FACTOR; NEUROTROPHIN RECEPTOR; PROTEIN P75; PROTEIN TYROSINE KINASE A;

ALZHEIMER DISEASE; ARTICLE; BRAIN NERVE CELL; CHOLINERGIC NERVE CELL; CLINICAL ARTICLE; COGNITION; COGNITIVE DEFECT; DNA MICROARRAY; DOWN REGULATION; FEMALE; FOREBRAIN; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IN SITU HYBRIDIZATION; MALE; MINI MENTAL STATE EXAMINATION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; CHOLINE O-ACETYLTRANSFERASE; COGNITION DISORDERS; COHORT STUDIES; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MENTAL STATUS SCHEDULE; NERVE TISSUE PROTEINS; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POSTMORTEM CHANGES; PROSENCEPHALON; RECEPTOR, TRKA; RECEPTORS, NERVE GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEVERITY OF ILLNESS INDEX;

EID: 33645301867     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.03764.x     Document Type: Article

References (68)

1. Bartus R. T. Dean R. L. 3rd, Beer B. Lippa A. S. 1982 The cholinergic hypothesis of geriatric memory dysfunction. Science 217 408 414.
2. Baxter M. G. Chiba A. A. 1999 Cognitive functions of the basal forebrain. Curr. Opin. Neurobiol. 9 178 183.
3. Bennett D. A. Wilson R. S. Schneider J. A. Evans D. A. Beckett L. A. Aggarwal N. T. Barnes L. L. Fox J. H. Bach J. 2002 Natural history of mild cognitive impairment in older persons. Neurology 59 198 205.
4. Bierer L. M. Haroutunian V. Gabriel S. Knott P. J. Carlin L. S. Purohit D. P. Perl D. P. Schmeidler J. Kanof P. Davis K. L. 1995 Neurochemical correlates of dementia severity in Alzheimer's disease: relative importance of the cholinergic deficits. J. Neurochem. 64 749 760.
5. Boissiere F. Faucheux B. Ruberg M. Agid Y. Hirsch E. C. 1997 Decreased TrkA gene expression in cholinergic neurons of the striatum and basal forebrain of patients with Alzheimer's disease. Exp Neurol. 145 245 252.
6. Braak H. Braak E. 1991 Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82 239 259.
7. Capsoni S. Ugolini G. Comparini A. Ruberti F. Berardi N. Cattaneo A. 2000 Alzheimer-like neurodegeneration in aged antinerve growth factor transgenic mice. Proc. Natl Acad. Sci. USA 97 6826 6831.
8. Che S. Ginsberg S. D. 2004 Amplification of transcripts using terminal continuation. Lab. Invest. 84 131 137.
9. Chu Y. Cochran E. J. Bennett D. A. Mufson E. J. 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.
10. Cooper J. D. Lindholm D. Sofroniew M. V. 1994 Reduced transport of [125I]nerve growth factor by cholinergic neurons and down-regulated TrkA expression in the medial septum of aged rats. Neuroscience 62 625 629.
11. Cooper J. D. Salehi A. Delcroix J. D. Howe C. L. Belichenko P. V. Chua-Couzens J. Kilbridge J. F. Carlson E. J. Epstein C. J. Mobley W. C. 2001 Failed retrograde transport of NGF in a mouse model of Down's syndrome: reversal of cholinergic neurodegenerative phenotypes following NGF infusion. Proc. Natl Acad. Sci. USA 98 10 439 10 444.
12. Counts S. E. Chen E.-Y. Che S. Ikonomovic M. D. Wuu J. Ginsberg S. D. DeKosky S. T. Mufson E. J. 2006 Galanin fiber hypertrophy within the cholinergic nucleus basalis during the progression of Alzheimer's disease. Dement. Geriatr. Cogn. Disord. 21 205 221.
13. Counts S. E. Mufson E. J. 2005 The role of nerve growth factor receptors in cholinergic basal forebrain degeneration in prodromal Alzheimer's disease. J. Neuropath. Exper. Neurol. 64 263 272.
14. Counts S. E. Nadeem M. Wuu J. Ginsberg S. D. Saragovi H. U. Mufson E. J. 2004 Reduction of cortical TrkA but not p75 (NTR) protein in early-stage Alzheimer's disease. Ann. Neurol. 56 520 531.
15. De Lacalle S. Cooper J. D. Svendsen C. N. Dunnett S. B. Sofroniew M. V. 1996 Reduced retrograde labelling with fluorescent tracer accompanies neuronal atrophy of basal forebrain cholinergic neurons in aged rats. Neuroscience 75 19 27.
16. DeKosky S. T. Ikonomovic M. D. Styren S. D. Beckett L. Wisniewski S. Bennett D. A. Cochran E. J. Kordower J. H. 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.
17. Eberwine J. Kacharmina J. E. Andrews C. Miyashiro K. McIntosh T. Becker K. Barrett T. Hinkle D. Dent G. Marciano P. 2001 mRNA expression analysis of tissue sections and single cells. J. Neurosci. 21 8310 8314.
18. Fahnestock M. Yu G. Michalski B. Mathew S. Colquhoun A. Ross G. M. Coughlin M. D. 2004 The nerve growth factor precursor proNGF exhibits neurotrophic activity but is less active than mature nerve growth factor. J. Neurochem. 89 581 592.
19. Galvin J. E. Ginsberg S. D. 2004 Expression profiling and pharmacotherapeutic development in the central nervous system. Alzheimer Dis Assoc Disord 18 264 269.
20. Galvin J. E. Ginsberg S. D. 2005 Expression profiling in the aging brain: a perspective. Ageing Res. Rev. 4 529 547.
21. Gilmor M. L. Erickson J. D. Varoqui H. Hersh L. B. Bennett D. A. Cochran E. J. Mufson E. J. 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. Ginsberg S. D. 2005 RNA amplification strategies for small sample populations. Methods 37 229 237.
23. Ginsberg S. D. Che S. 2002 RNA amplification in brain tissues. Neurochem. Res. 27 981 992.
24. Ginsberg S. D. Che S. 2004 Combined histochemical staining, RNA amplification, regional, and single cell analysis within the hippocampus. Lab. Invest. 84 952 962.
25. Ginsberg S. D. Che S. 2005 Expression profile analysis within the human hippocampus: Comparison of CA1 and CA3 pyramidal neurons. J. Comp Neurol. 487 107 118.
26. Ginsberg S. D. Crino P. B. Lee V. M.-Y. Eberwine J. H. Trojanowski J. Q. 1997 Sequestration of RNA in Alzheimer's disease neurofibrillary tangles and senile plaques. Ann. Neurol. 41 200 209.
27. Ginsberg S. D. Galvin J. E. Chiu T.-S. Lee V. M.-Y. Masliah E. Trojanowski J. Q. 1998 RNA sequestration to pathological lesions of neurodegenerative disorders. Acta Neuropathol. 96 487 494.
28. Ginsberg S. D. Hemby S. E. Lee V. M.-Y. Eberwine J. H. Trojanowski J. Q. 2000 Expression profile of transcripts in Alzheimer's disease tangle-bearing CA1 neurons. Ann. Neurol. 48 77 87.
29. Ginsberg S. D. Hemby S. E. Mufson E. J. Martin L. J. 2006 Cell and tissue microdissection in combination with genomic and proteomic applications, in Neuroanatomical Tract Tracing 3. Molecules-Neurons-Systems Zaborszky L. Wouterlood F. Lanciego J. L., eds) pp. 109 141 Springer/Kluwer/Plenum New York.
30. Higgins G. A. Mufson E. J. 1989 NGF receptor gene expression is decreased in the nucleus basalis in Alzheimer's disease. Exp Neurol. 106 222 236.
31. Holtzman D. M. Li Y. Parada L. F. Kinsman S. Chen C. K. Valletta J. S. Zhou J. Long J. B. Mobley W. C. 1992 p140trk mRNA marks NGF-responsive forebrain neurons: evidence that trk gene expression is induced by NGF. Neuron 9 465 478.
32. Howe C. L. Mobley W. C. 2004 Signaling endosome hypothesis: a cellular mechanism for long distance communication. J. Neurobiol. 58 207 216.
33. Hyman B. T. Trojanowski J. Q. 1997 Consensus recommendations for the post-mortem diagnosis of Alzheimer disease from the National Institute on Aging and the Reagan Institute Working Group on diagnostic criteria for the neuropathological assessment of Alzheimer disease. J. Neuropathol. Exp. Neurol. 56 1095 1097.
34. Johnson D. Lanahan A. Buck C. R. Sehgal A. Morgan C. Mercer E. Bothwell M. Chao M. 1986 Expression and structure of the human NGF receptor. Cell 47 545 554.
35. Kaplan D. R. Miller F. D. 2000 Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 10 381 391.
36. Li Y. Holtzman D. M. Kromer L. F. Kaplan D. R. Chua-Couzens J. Clary D. O. Knusel B. Mobley W. C. 1995 Regulation of TrkA and ChAT expression in developing rat basal forebrain: evidence that both exogenous and endogenous NGF regulate differentiation of cholinergic neurons. J. Neurosci. 15 2888 2905.
37. Mesulam M. M. Mufson E. J. Levey A. I. Wainer B. H. 1983 Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J. Comp Neurol. 214 170 197.
38. Mirra S. S. Heyman A. McKeel D. Sumi S. M. Crain B. J. Brownlee L. M. Vogel F. S. Hughes J. P. van Belle G. 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.
39. Mufson E. J. Bothwell M. Hersh L. B. Kordower J. H. 1989b Nerve growth factor receptor immunoreactive profiles in the normal, aged human basal forebrain: colocalization with cholinergic neurons. J. Comp Neurol. 285 196 217.
40. Mufson E. J. Bothwell M. Kordower J. H. 1989a Loss of nerve growth factor receptor-containing neurons in Alzheimer's disease: a quantitative analysis across subregions of the basal forebrain. Exp Neurol. 105 221 232.
41. Mufson E. J. Counts S. E. Che S. Ginsberg S. D. 2004 cDNA array and quantitative PCR analysis of neurotrophin receptor transcripts in cholinergic basal forebrain neurons in people with mild cognitive impairment (MCI) and Alzheimer's disease. Proc. Soc. Neurosci. 30 335-336.
42. Mufson E. J. Counts S. E. Ginsberg S. D. 2002 Single cell gene expression profiles of nucleus basalis cholinergic neurons in Alzheimer's disease. Neurochem. Res. 27 1035 1048.
43. Mufson E. J. Ginsberg S. D. Ikonomovic M. D. DeKosky S. T. 2003 Human cholinergic basal forebrain: chemoanatomy and neurologic dysfunction. J. Chem. Neuroanat 26 233 242.
44. Mufson E. J. Kordower J. H. 1992 Cortical neurons express nerve growth factor receptors in advanced age and Alzheimer disease. Proc. Natl Acad. Sci. USA 89 569 573.
45. Mufson E. J. Lavine N. Jaffar S. Kordower J. H. Quirion R. Saragovi H. U. 1997 Reduction in p140-trkA receptor protein within the nucleus basalis and cortex in Alzheimer's disease. Exp. Neurol. 146 91 103.
46. Mufson E. J. Li J. M. Sobreviela T. Kordower J. H. 1996 Decreased trkA gene expression within basal forebrain neurons in Alzheimer's disease. Neuroreport 8 25 29.
47. Mufson E. J. Ma S. Y. Cochran E. J. Bennett D. A. Beckett L. A. Jaffar S. Saragovi H. U. 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.
48. Naumann T. Casademunt E. Hollerbach E. Hofmann J. Dechant G. Frotscher M. Barde Y. A. 2002 Complete deletion of the neurotrophin receptor p75NTR leads to long-lasting increases in the number of basal forebrain cholinergic neurons. J. Neurosci. 22 2409 2418.
49. Nykjaer A. Lee R. Teng K. K. et al. 2004 Sortilin is essential for proNGF-induced neuronal cell death. Nature 427 843 848.
50. Pedraza C. E. Podlesniy P. Vidal N. Arevalo J. C. Lee R. Hempstead B. Ferrer I. Iglesias M. Espinet C. 2005 Pro-NGF isolated from the human brain affected by Alzheimer's disease induces neuronal apoptosis mediated by p75NTR. Am. J. Pathol 166 533 543.
51. Peng S. Wuu J. Mufson E. J. Fahnestock M. 2004 Increased proNGF levels in subjects with mild cognitive impairment and mild Alzheimer disease. J. Neuropathol Exp Neurol. 63 641 649.
52. Peng S. Wuu J. Mufson E. J. 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.
53. Petersen R. C. 2004 Mild cognitive impairment as a diagnostic entity. J. Intern. Med. 256 183 194.
54. Ruberti F. Capsoni S. Comparini A. Di Daniel E. Franzot J. Gonfloni S. Rossi G. Berardi N. Cattaneo A. 2000 Phenotypic knockout of nerve growth factor in adult transgenic mice reveals severe deficits in basal forebrain cholinergic neurons, cell death in the spleen, and skeletal muscle dystrophy. J. Neurosci. 20 2589 2601.
55. Salehi A. Verhaagen J. Dijkhuizen P. A. D. Swaab D. F. 1996 Co-localization of high-affinity neurotrophin receptors in nucleus basalis of Meynert neurons and their differential reduction in Alzheimer's disease. Neuroscience 75 373 387.
56. Saragovi H. U. 2005 Progression of age-associated cognitive impairment correlates with quantitative and qualitative loss of TrkA receptor protein in nucleus basalis and cortex. J. Neurochem. 95 1472 1480.
57. SAS Institute. 1999 ) SAS/STAT User's Guide, Version 8. SAS Publishing Cary, NC, USA.
58. Schatteman G. C. Gibbs L. Lanahan A. A. Claude P. Bothwell M. 1988 Expression of NGF receptor in the developing and adult primate central nervous system. J. Neurosci. 8 860 873.
59. Shelton D. L. Sutherland J. Gripp J. Camerato T. Armanini M. P. Phillips H. S. Carroll K. Spencer S. D. Levinson A. D. 1995 Human trks: molecular cloning, tissue distribution, and expression of extracellular domain immunoadhesins. J. Neurosci. 15 477 491.
60. Sofroniew M. V. Howe C. L. Mobley W. C. 2001 Nerve growth factor signaling, neuroprotection, and neural repair. Annu. Rev. Neurosci. 24 1217 1281.
61. Teng K. K. Hempstead B. L. 2004 Neurotrophins and their receptors: signaling trios in complex biological systems. Cell Mol Life Sci. 61 35 48.
62. Tuszynski M. H. 2002 Growth-factor gene therapy for neurodegenerative disorders. Lancet Neurol. 1 51 57.
63. Tuszynski M. H. Thal L. Pay M. et al. 2005 A Phase I clinical trial of nerve growth factor gene therapy for Alzheimer's disease. Nat. Med. 11 551 555.
64. Whitehouse P. J. Price D. L. Struble R. G. Clark A. W. Coyle J. T. Delong M. R. 1982 Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 215 1237 1239.
65. Wilcock G. K. Esiri M. M. Bowen D. M. Smith C. C. 1982 Alzheimer's disease. Correlation of cortical choline acetyltransferase activity with the severity of dementia and histological abnormalities. J. Neurol. Sci. 57 407 417.
66. Winblad B. Palmer K. Kivipelto M. et al. 2004 Mild cognitive impairment - beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment. J. Intern. Med. 256 240 246.
67. Yang Y. Mufson E. J. Herrup K. 2003 Neuronal cell death is preceded by cell cycle events at all stages of Alzheimer's disease. J. Neurosci. 23 2557 2563.
68. Yoon S. O. Casaccia-Bonnefil P. Carter B. Chao M. V. 1998 Competitive signaling between TrkA and p75 nerve growth factor receptors determines cell survival. J. Neurosci. 18 3273 3281.