Complete Deletion of the Neurotrophin Receptor p75NTR Leads to Long-Lasting Increases in the Number of Basal Forebrain Cholinergic Neurons

Journal of Neuroscience

Volumn 22, Issue 7, 2002, Pages 2409-2418

  Naumann, Thomas ^a   Casademunt, Elisabeth ^b   Hollerbach, Ewald ^a   Hofmann, Jutta ^a   Dechant, Georg ^b   Frotscher, Michael ^a   Barde, Yves Alain ^b,c  

^a UNIVERSITY OF FREIBURG   (Germany)

^b MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^c FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

Cell death; Cholinergic neurons; Genetic background; Medial septum; NGF; Optical fractionator; p75NTR

Indexed keywords

NEUROTROPHIN RECEPTOR; NEUROTROPHIN RECEPTOR P75; UNCLASSIFIED DRUG; ACETYLCHOLINE; NERVE GROWTH FACTOR RECEPTOR;

ANIMAL CELL; ARTICLE; BACKCROSSING; CELL COUNT; CHOLINERGIC NERVE CELL; CONGENIC STRAIN; FOREBRAIN; GENE DELETION; GENE MUTATION; KNOCKOUT GENE; MOUSE; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; SEPTUM NUCLEUS; ALTERNATIVE RNA SPLICING; ANIMAL; ANTIBODY SPECIFICITY; CROSS BREEDING; CYTOLOGY; EXON; GENETICS; HIPPOCAMPUS; METABOLISM; MOUSE MUTANT; MUTATION; NERVE CELL; SEPTUM PELLUCIDUM; SPECIES DIFFERENCE; STATISTICS;

ACETYLCHOLINE; ALTERNATIVE SPLICING; ANIMALS; CELL COUNT; CROSSES, GENETIC; EXONS; HIPPOCAMPUS; MICE; MICE, KNOCKOUT; MICE, NEUROLOGIC MUTANTS; MUTATION; NEURONS; ORGAN SPECIFICITY; PROSENCEPHALON; RECEPTOR, NERVE GROWTH FACTOR; RECEPTORS, NERVE GROWTH FACTOR; SEPTUM OF BRAIN; SPECIES SPECIFICITY;

EID: 0036550661     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-07-02409.2002     Document Type: Article

References (45)

1. Albanese A, Gozzo S, Iacopino C, Altavista MC (1985) Strain-dependent variations in the number of forebrain cholinergic neurons. Brain Res 334:380-384.
2. Bamji SX, Majdan M, Pozniak CD, Belliveau DJ, Aloyz R, Kohn J, Causing CG, Miller FD (1998) The p75 neurotrophin receptor mediates neuronal apoptosis and is essential for naturally occurring sympathetic neuron death. J Cell Biol 140:911-923.
3. Bartus RT, Dean RL, Beer B, Lippa AS (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217:408-414.
4. Bentivoglio AR, Altavista MC, Granata R, Albanese A (1994) Genetically determined cholinergic deficiency in the forebrain of C57BL/6 mice. Brain Res 637:181-189.
5. Bibel M, Barde Y-A (2000) Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system. Genes Dev 14:2919-2937.
6. NTR. EMBO J 18:616-622.
7. Casaccia-Bonnefil P, Carter BD, Dobrowsky RT, Chao MV (1996) Death of oligodendrocytes mediated by the interaction of nerve growth factor with its receptor p75. Nature 383:716-719.
8. Casademunt E, Carter BD, Benzel I, Frade JM, Dechant G, Barde Y-A (1999) The zinc finger protein NRIF interacts with the neurotrophin receptor p75(NTR) and participates in programmed cell death. EMBO J 18:6050-6061.
9. Coyle JT, Price DL, DeLong MR (1983) Alzheimer's disease: a disorder of cortical cholinergic innervation. Science 219:1184-1190.
10. Fagan AM, Garber M, Barbacid M, Silos-Santiago I, Holtzman DM (1997) A role for TrkA during maturation of striatal and basal forebrain cholinergic neurons in vivo. J Neurosci 17:7644-7654.
11. Fischer W, Wictorin K, Björklund A, Williams LR, Varon S, Gage FH (1987) Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature 329:65-68.
12. Frade JM, Barde Y-A (1999) Genetic evidence for cell death mediated by nerve growth factor and the neurotrophin receptor p75 in the developing mouse retina and spinal cord. Development 126:683-690.
13. Frade JM, Rodriguez-Tébar A, Barde Y-A (1996) Induction of cell death by endogenous nerve growth factor through its p75 receptor. Nature 383:166-168.
14. Franklin KB, Paxinos G (1997) The mouse brain. San Diego: Academic.
15. Green MC, Witham BA (1991) Handbook of genetically standardized JAX mice. Bar Harbor, ME: The Jackson Laboratory.
16. Greferath U, Bennie A, Kourakis A, Bartlett PF, Murphy M, Barrett GL (2000) Enlarged cholinergic forebrain neurons and improved spatial learning in p75 knockout mice. Eur J Neurosci 12:885-893.
17. Hagg T (1999) Neuronal cell death: retraction. Science 285:340.
18. Hagg T, Louis J-C, Longo FM, Varon S (1994) Neurotrophic factors, growth factors, and central nervous system trauma. In: The neurobiology of the central nervous system trauma (Salzman SK, Faden IA, eds), pp 245-265. Oxford: Oxford UP.
19. Hagg T, Van der Zee CEEM, Ross GM, Riopelle RJ (1997) Basal forebrain neuronal loss in mice lacking neurotrophin receptor p75. Science 277:838-839.
20. Hefti F (1986) Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections. J Neurosci 6:2155-2162.
21. Jakab RL, Leranth C (1995) Septum. In: The rat nervous system (Paxinos G, ed), pp 405-442. Oxford: Academic.
22. Kaplan DR, Miller FD (1997) Signal transduction by the neurotrophin receptors. Curr Opin Cell Biol 9:213-221.
23. Lee KF, Li E, Huber LJ, Landis SC, Sharpe AH, Chao MV, Jaenisch R (1992) Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69:737-749.
24. Li Y, Holtzman DM, Kromer LF, Kaplan DR, Chua-Couzens J, Clary DO, Knusel B, Mobley WC (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.
25. Lucidi-Phillipi CA, Clary DO, Reichardt LF, Gage FH (1996) TrkA activation is sufficient to rescue axotomized cholinergic neurons. Neuron 16:653-663.
26. Majdan M, Lachance C, Gloster A, Aloyz R, Zeindler C, Bamji S, Bhakar A, Belliveau D, Fawcett J, Miller FD, Barker PA (1997) Transgenic mice expressing the intracellular domain of the p75 neurotrophin receptor undergo neuronal apoptosis, J Neurosci 17:6988-6998.
27. Naumann T, Linke R, Frotscher M (1992) Fine structure of rat septohippocampal neurons. I. Identification of septohippocampal projection neurons by retrograde tracing combined with electron microscopic immunocytochemistry and intracellular staining. J Comp Neurol 325:207-218.
28. Naumann T, Kermer P, Frotscher M (1994) Fine structure of rat septohippocampal neurons. III. Recovery of choline acetyltransferase immunoreactivity after fimbria-fornix transection. J Comp Neurol 350:161-170.
29. Naumann T, Straube A, Frotscher M (1997) Recovery of ChAT immunoreactivity in axotomized rat cholinergic septal neurons despite reduced NGF receptor expression. Eur J Neurosci 9:1340-1349.
30. Perry E, Walker M, Grace J, Perry R (1999) Acetylcholine in mind: a neurotransmitter correlate of consciousness? Trends Neurosci 6:273-280.
31. Peterson DA, Leppert JT, Lee KF, Gage FH (1997) Basal forebrain neuronal loss in mice lacking neurotrophin receptor p75. Science 277:837-839.
32. Peterson DA, Dickinson-Anson HA, Leppert JT, Lee KF, Gage FH (1999) Central neuronal loss and behavioral impairment in mice lacking neurotrophin receptor p75. J Comp Neurol 404:1-20.
33. Schwegler H, Boldyreva M, Pyrlik-Gohlmann M, Linke R, Wu J, Zilles K (1996) Genetic variation in the morphology of the septohippocampal cholinergic and GABAergic system in mice. I. Cholinergic and GABAergic markers. Hippocampus 6:136-148.
34. Simpson EM, Linder CC, Sargent EE, Davisson MT, Mobraaten LE, Sharp JJ (1997) Genetic variation among 129 substrains and its importance for targeted mutagenesis in mice. Nat Genet 16:19-27.
35. Sofroniew MV, Pearson RC, Powell TP (1987) The cholinergic nuclei of the basal forebrain of the rat: normal structure, development and experimentally induced degeneration. Brain Res 411:310-331.
36. Sofroniew MV, Galletly NP, Isacson O, Svendsen CN (1990) Survival of adult basal forebrain cholinergic neurons after loss of target neurons. Science 247:338-342.
37. Van der Zee CEEM, Ross GM, Riopelle RJ, Hagg T (1996) Survival of cholinergic forebrain neurons in developing p75NGFR-deficient mice. Science 274:1729-1732.
38. Vantini G, Schiavo N, Di Martino A, Polato P, Triban C, Callegaro L, Toffano G, Leon A (1989) Evidence for a physiological role of nerve growth factor in the central nervous system of neonatal rats. Neuron 3:267-273.
39. NTR causes defects both in the nervous and the vascular systems. Nat Neurosci 4:1-2.
40. Wahlsten D (1982) Deficiency of corpus callosum varies with strain and supplier of the mice. Brain Res 239:329-347.
41. Wahlsten D, Bulman-Fleming B (1994) Retarded growth of the medial septum: a major gene effect in acallosal mice. Dev Brain Res 77:203-214.
42. Ward NL, Hagg T (1999) p75(NGFR) and cholinergic neurons in the developing forebrain: a re-examination. Dev Brain Res 118:79-91.
43. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
44. Yeo TT, Chua-Couzens J, Butcher LL, Bredesen DE, Cooper JD, Valletta JS, Mobley WC, Longo FM (1997) Absence of p75NTR causes increased basal forebrain cholinergic neuron size, choline acetyltransferase activity, and target innervation. J Neurosci 17:7594-7605.
45. Yoon SO, Casaccia-Bonnefil P, Carter B, Chao MV (1998) Competitive signaling between TrkA and p75 nerve growth factor receptors determines cell survival. J Neurosci 18:3273-3281.