Disruption of a single allele of the nerve growth factor gene results in atrophy of basal forebrain cholinergic neurons and memory deficits

Journal of Neuroscience

Volumn 17, Issue 19, 1997, Pages 7288-7296

  Chen, Karen S ^a   Nishimura, Merry C ^a   Armanini, Mark P ^a   Crowley, Craig ^a   Spencer, Susan D ^a   Phillips, Heidi S ^a  

^a GENENTECH INC   (United States)

Author keywords

Cell death; Cholinergic; Gene deletion; Learning; Memory; Neurotrophin; NGF

Indexed keywords

MESSENGER RNA; NERVE GROWTH FACTOR; NEUROTROPHIN;

ALLELE; ANIMAL CELL; ARTICLE; BRAIN ATROPHY; CELL DEATH; CHOLINERGIC NERVE CELL; COGNITIVE DEFECT; CONTROLLED STUDY; FEMALE; FOREBRAIN; GENE DELETION; GENE MUTATION; HIPPOCAMPUS; LEARNING; MAZE TEST; MEMORY; MOUSE; NONHUMAN; PRIORITY JOURNAL;

EID: 0030799383     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.17-19-07288.1997     Document Type: Article

References (38)

1. Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239-247.
2. Aloe L, Cozzari C, Calissano P, Levi-Montalcini R (1981) Somatic and behavioral postnatal effects of fetal injections of nerve growth factor antibodies in the rat. Nature 291:413-415.
3. Chen KS, Gage FH (1995) Somatic gene transfer of NGF to the aged brain: behavioral and morphological amelioration. J Neurosci 15:2819-2825.
4. Chen KS, Masliah E. Mallory M, Terry RD, Gage FH (1995) Synaptic loss in cognitively impaired aged rats is ameliorated by chronic human nerve growth factor infusion. Neuroscience 68:19-27.
5. Crowley C, Spencer SD, Nishimura MC, Chen KS, Pitts-Mcek S, Armanini MP, Ling LH, McMahon SB, Shelton DL, Levinson AD, Phillips HS (1994) Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholin- ergic neurons. Cell 76:1001-1011.
6. Dekker AJ, Gage FH, Thal LJ (1992) Delayed treatment with nerve growth factor improves acquisition of a spatial task in rats with lesions of the nucleus basalis magnocellularis: evaluation of the involvement of different neurotransmitter systems. Neuroscience 48:111-119.
7. Fischer W, Wictorin K, Bjorklund 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.
8. Fischer W, Bjorklund A, Chen KS, Gage FH (1991) NGF improves spatial memory in aged rodents as a function of age. J Neurosci 11:1889-1906.
9. Fischer W, Chen KS, Gage FH, Bjorklund A (1992) Progressive decline in spatial learning and integrity of forebrain cholinergic neurons in rats during aging. Neurobiol Aging 13:9-23.
10. Fonnum F (1974) A rapid radiochemical method for the determination of choline acetyltransferase. J Neurochem 24:407-409.
11. Gage FH, Armstrong DM, Williams LR, Varon S (1988) Morphologic response of axotomized septal neurons to nerve growth factor. J Comp Neurol 269:147-155.
12. Gerlai R (1996) Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype? Trends Neurosci 19:177-181.
13. Gorin P, Johnson EM (1979) Experimental autoimmune model of nerve growth factor deprivation: effects on developing peripheral sympathetic and sensory neurons. Proc Natl Acad Sci USA 76:5382-5386.
14. Hagg T, Manthorpe M, Vahlsing HL, Varon S (1988) Delayed treatment with nerve growth factor reverses the apparent loss of cholinergic neurons after acute brain damage. Exp Neurol 101:303-312.
15. Hedreen JC, Bacon JC, Price DL (1985) A modified histochemical method to visualize acetylcholinesterase-containing axons. J Histo- chem Cytochem 33:134-140.
16. Hefti F (1986) Nerve growth factor (NGF) promotes survival of septal cholinergic neurons after fimbrial transection. J Neurosci 6:2155-2162.
17. Hefti F, Hartikka J, Knusel B (1989) Function of neurotrophic factors in the adult and aging brain and their possible use in the treatment of neurodegenerative diseases. Neurobiol Aging 10:515-533.
18. Johnson Jr EM, Gorin PD, Brandeis LD, Pearson J (1980) Dorsal root ganglion neurons are destroyed by exposure in utero to maternal antibody to nerve growth factor. Science 210:916-918.
19. Kawaja MD, Gage FH (1991) Reactive astrocytes are substrates for the growth of adult CNS axons in the presence of elevated levels of nerve growth factor. Neuron 7:1019-1030.
20. Koliatsos VE, Nauta HJW, Clatterbuck RE, Holtzman DM, Mobley WC, Price DL (1990) Mouse nerve growth factor prevents degeneration of axotomized basal forebrain cholinergic neurons in monkeys. J Neurosci 10:3810-3813.
21. Korsching S, Thoenen H (1983) Nerve growth factor in sympathetic ganglia and corresponding target organs of the rat: correlation with density of sympathetic innervation. Proc Natl Acad Sci USA 64:3513-3516.
22. Kromer LF (1987) Nerve growth factor treatment after brain injury prevents neuronal death. Science 235:214-216.
23. Levi-Montalcini R (1987) The nerve growth factor 35 years later. Science 237:1154-1162.
24. Levi-Montalcini R, Angeletti PU (1968) Nerve growth factor. Physiol Rev 48:534-569,
25. Levi-Montalcini R, Booker B (1960) Destruction of the sympathetic ganglia in mammals by an antiserum to a nerve-growth protein. Proc Natl Acad Sci USA 46:384-391,
26. Li Y, Holtzman DM, Kromer LF, Kaplan DR, Chua-Couzens J, Clary DO, Knüsel 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.
27. Lipp H-P, Stagliar-Bozizevic M, Wolfer DP (1995) Behavior in large numbers of knockout mice: results, caveats and perspectives. Behav Genet 25:275.
28. Mobley WC, Rutkowski JL, Tennekoon GI, Gemski J, Buchanan K, Johnston MV (1986) Nerve growth factor increases choline acetyltransferase activity in developing basal forebrain neurons. Mol Brain Res 1:53-62.
29. Nabeshima T, Ogawa S, Ishimaru H, Kameyama T, Fukuta T, Takeuchi R, Hayashi K (1991) Memory impairment and morphological changes in rats induced by active fragment of anti-nerve growth factor-antibody. Biochem Biophys Res Commun 175:215-219.
30. Olton DS, Wenk GL (1987) Dementia: animal models of the cognitive impairments produced by degeneration of the basal forebrain cholinergic system. In: Psychopharmacology: the third generation of progress (Meltzer HY, ed), pp 941-953. New York: Raven.
31. Ruit KG, Elliott JL, Osborne PA, Van Q, Snider WD (1992) Selective dependence of mammalian dorsal root ganglion neurons on nerve growth factor during embryonic development. Neuron 8:1-20.
32. Thoenen H, Bandtlow C, Heumann R (1987) The physiological significance of nerve growth factor in the central nervous system: comparison with the periphery. Rev Physiol Biochem Pharmacol 109:145-178.
33. Van der Zee CE, Fawcett J, Diamond J (1992) Antibody to NGF inhibits collateral sprouting of septohippocampal fibers following entorhinal cortex lesion in adult rats. J Comp Neurol 326:91-100.
34. Van der Zee CE, Lourenssen S, Stanisz J, Diamond J (1995) NGF deprivation of adult rat brain results in cholinergic hypofunction and selective impairments in spatial learning. Eur J Neurosci 7:160-168.
35. 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.
36. Whittemore SR, Seiger A (1987) The expression, localization, and functional significance of β-nerve growth factor in the central nervous system. Brain Res Rev 12:439-464.
37. Will B, Hefti F (1985) Behavioral and neurochemical effects of chronic intraventricular injections of nerve growth factor in adult rats with fimbria lesions. Behav Brain Res 17:17-24.
38. Williams LR, Varon S, Peterson GM, Wictorin K, Fisher W, Bjorklund A, Gage FH (1986) Continuous infusion of nerve growth factor prevents basal forebrain neuronal death after fimbria-fornix transection. Proc Natl Acad Sci USA 83:9231-9235.